j& z M í G r j u i i A A (o. 3 2 0 / S 2 ! 2 y n a l
á a m d c f S f ^ m ^ ^
Möguleikar í álaveiðum og álaeldi I þ in g i
Bjami Jónsson Má]snr. _ i w j n _____
Norðurlandsdeild Veiðimálastofnunar f ) A KJ O
M á la ly k i l l : ----------^ . jJ . . J _ / L c_______
Þekking á lífsferlum ála sem miðað hefur verið við hérlendis er að mestu byggð á
rannsóknum erlendis frá. Margt er hins vegar ólíkt með lífsháttum ála á Islandi og
annars staðar þar sem hann er að finna. Skipta þar máli staðsetning landsins og
sérstaða íslenskrar náttúru með sínum fjölbreyttu búsvæðum en tegundafæð. Einnig er
ísland eina landið þar sem bæði er að fínna evrópuál og kynblendinga við amerískan
ál. Nýjar erfðafræðirannsóknir staðfesta umfangsmikla blöndun þessara tegunda hér
og að hún skili sér á milli kynslóða ála sem berast til Islands en komi ekki fram
annarsstaðar á útbreiðslusvæði álsins. Álar á Islandi nýta sér fjölbreytt búsvæði í ám
og vötnum og þá er jafnvel að fmna í svo ólíkum búsvæðum sem heitum lækjum,
köldum og dimmum hraunsprungum eða fullsöltum sjó við ströndina.
Hérlendis hefur frá árinu 1999 verið unnið markvisst að margvíslegum rannsóknum á
álum. Þær rannsóknir hafa ekki síst beinst að göngum glerála til landsins, útbreiðslu,
vistfræði og tegundasamsetningu ála á íslandi. Frá því rannsóknimar hófust hafa
glerálar veiðst á 30 stöðum á landinu. Rannsökuð hafa verið áhrif sjávarfalla,
vatnshita, birtu og fleiri þátta á faratferli glerálanna. Einnig hafa daghringir í kvömum
glerálanna verið notaðir til að tímasetja hin ýmsu myndbreytingaskeið hjá álalirfunum
og hve lengi þær eru á leið til landsins. Aðalgöngutími glerálanna er frá apríl og fram
í byrjun júlí en þeirra fyrstu verður vart í mars. Gangan er að mestu yfírstaðinn um
miðjan júlí ár hvert. Þeir þættir sem ráða hvað mestu um göngumar eru sjávarföll og
vatnshiti. Rannsóknir á daghringjum í kvömum glerála sýna að þeir eru um eitt ár á
leiðinni yfir hafið frá Þanghafinu til Islands, en áður var talið að ferðin tæki þá þrjú ár.
Rannsóknir á glerálagögnum hafa ekki síst miðast við að afla þekkingar sem nýta
megi við veiðar á glerálum til álaeldis. Nú fer fram tilraunaeldi á álum í samvinnu
nokkurra aðila sem byggir á áframeldi á glerálum sem veiddir hafa verið hérlendis.
Þær tilraunir hafa lofað góðu og er stefnt að því að auka umfang þeirra á árinu 2006.
Rannsóknir á gulál og bjartál hafa beinst að útbreiðslu ála á íslandi, búsvæðavali,
lífsháttum og nýtingarmöguleikum. Þessar rannsóknir hafa leitt í ljós að ála er að
finna í öllum landshlutum í fjölbreyttum búsvæðum og með ólíka lífshætti. Hluti ála
virðist ala allan aldur sinn í sjó án þess að fara í ferskvatn eða ísalt vatn. Niðurstöður
benda einnig til þess að munur sé á tegundasamsetningu eftir búsvæðum og jafnvel
landshlutum. Það er einstakt á Islandi að víðast er meirihluti ála hrygnur en hængar
eru í minnihluta. Kynákvörðun ála er umhverfisháð og fer kynjahlutfall ála almennt
annarsstaðar á útbreiðslusvæði þeirra eftir búsvæðum. ísland virðist því skera sig hér
úr og er hlutfall hrygna víða allt að 100%. Hrygnur hafa meiri vaxtarmöguleika og
verða stærri en hængamir. Þær eru því eftirsóttari til veiða og til eldis. Talsverðir
vannýttir möguleikar em fyrir hendi í álaveiðum á íslandi en tilfinnanlega skortir enn
meiri rannsóknir og þekkingu á lífsögu álsins, vexti, aldursdreifingu og stofnstærð
eftir svæðum svo skipuleggja megi sjálfbærar veiðar á álum á íslandi. Sérstaklega
virðast veiðar á bjartálum geta gefið góða raun.
Fræðaþing landbúnaðarins 2006. Úrdráttur erindi.
Evolution, 44(5), 1990, pp. 1254-1262
THE EVOLUTIONARY GENETIC STATUS OF ICELANDIC EELS
J o h n C. A v is e , 1 W i l l i a m S. N e l s o n , 1 J o n a t h a n A r n o l d , ' R i c h a r d K . K o e h n ,2
G e o r g e C. W i l l i a m s ,2 a n d V i l h j á l m u r T h o r s t e i n s s o n 3
'D epartm ent o f Genetics, University o f Georgia, Athens, GA 30602 USA
2D epartment o f Ecology and Evolution, S ta te University o f New York,
S tony Brook, N Y 11794 USA
2Hafrannsóknastofnunin, Skúlagötu 4, 101 Reykjavik, Iceland
Abstract. —The Iceland population o f Anguilla eels contains an elevated frequency o f fish with
vertebral numbers lower than those typical o f European localities. Several distinct hypotheses have
been advanced to account for these morphologically atypical fish: for example, they could represent
(1) genetically “pure” Amerícan expatriates, (2) genetically “pure” European types with ontogenetic
abnormalities, or (3) hybrids between American and European forms. Here we critically test these
and other possibilities by examining the joint dístributions o f allozyme markers, mitochondrial
D N A markers, and vertebral numbers in Icelandic eels. The particular pattems o f association
among the genetic and morphological traits demonstrate that the Iceland population includes, in
low frequency, the products o f hybridization between American and European eels. Approximately
2-4% o f the gene pool in the Iceland eel population is derived from American eel ancestry. This
hybrid zone is highly unusual in the biological world, because the mating events in catadromous
eels presumably take place thousands o f kilometers from where the hybrids are observed as maturing
juveniles. The molecular data, in conjunction with the geographic distributions, strongly suggest
that the differences in migrational behavior and morphology between American and European eels
include an important additive genetic component. Evolutionary hypotheses are advanced to account
for the original separation o f North Atlantic eels into American and European populations, and
for the presence o f hybrids in Iceland.
Received May 22, 1989. Accepted December 1, 1989.
N orth A tlan tic eels o f two nom inal
species, Anguilla anguilla and A. rostrata,
inhabit inland and coastal waters o f Europe
and North Africa, and the Americas, re-
spectively. The only known morphological
distinction between the two is num ber of
vertebrae, which typically ranges from 103
to 110 in eels from North America (with an
approximate norm al distribution around
mean 107.1), and from 110 to 120 in eels
from Europe (approximate normal distri-
bution around mean 114.7). Both forms ap-
parently spawn in the tropical west-Atlantic
Oeean (the Sargasso Sea—Fig. 1), yet dis-
perse as larvae to “ appropriate” continental
waters, such that eels with high vertebral
counts arrive in Europe and those with low
vertebraí counts predom inate in the Amer-
icas (Table 1). On reaching sexual maturity,
eels from both continents complete the ca-
tadrom ous life cycle by returning to the Sar-
gasso Sea to reproduce.
The biological and taxonomic relation-
ships o f American and European eels have
Iong been the subject o f debate (review in
Williams and Koehn, 1984). Tucker (1959)
proposed that the vertebral count differ-
ences are entirely ecophenotypic (not ge-
netically based), and arise in response to
different am bient temperatures experienced
along the different migration paths taken by
Iarvae destined for America versus Europe;
thus American and European forms would
belong to a single (perhaps panmictic) pop-
ulation. The hypothesis o f a single popu-
lation became untenable with more recent
demonstrations that American and Euro-
pean eels also differ significantly in fre-
quencies o f traits with unambiguous genetic
basis: malate dehydrogenase (M dh-2) allo-
zymes (review in Williams and Koehn,
1984), and mitochondrial DNA (mtDNA)
restriction sites (Avise et al., 1986). Early
in this century, Schmidt (1925) had shown
that newly produced Iarvae with high ver-
tebral counts were concentrated northeast
o f the Lesser Antilles, while larvae with low
numbers o f vertebrae were found mainly to
the west, between the Greater Antilles and
Bermuda. The deduction, that spawning of
American and European eels was largely al-
lopatric, may help to account for the recent
genetic data indicating two largely separate
gene pools. However, McCleave et al. (1987)
1254
ICELAND EELS 1255
have recently shown that overlap in spawn-
ing areas is probably greater than Schmidt
(1925) had suspected.
Many questions rem ain conceming the
possibility o f hybridization and extent of
gene flow (if any) between American and
European eel popu la tions. Particularly
within northem Europe, a low proportion
o f eels (about 0.3%—Williams et al., 1984)
exhibit vertebral counts normally charac-
teristic o f American forms (i.e., less than
110). Three distinct possibilities have pre-
viously been raised to account for these eels
with Iow vertebral num bers in Europe (Boe-
tius, 1980): (1) occasionaí straying of ge-
netically “pure” American eel larvae into
water masses bound for northem Europe,
(2) occasional action o f environmental in-
fluences that reduce vertebral numbers in
“pure” European eels, and (3) occasional
hybridization between American and Eu-
ropean forms. Opportunities to address these
and other possibilities become magnified in
Iceland, where eel populations show pre-
dom inantly European characteristics, yet
exhibit an elevated frequency o f low ver-
tebral counts and o f the M dh-2a allele nor-
mally associated with the American form
(Table 1).
Here we critically evaluate several alter-
native hypotheses to account for atypical
eels by examining the jo in t morphological
and genetic characteristics o f eels from Ice-
land. Genetic markers (M dh-2 and mt-
DNA) in conjunction with vertebral count
numbers dem onstrate that hybridization
between American and European eels has
indeed contributed to the Iceland eel gene
pool. The genetic data also allow an esti-
mate o f the magnitude o f flow o f American
eel alleles into Iceland, and m otivate spec-
ulation about the evolutionary origins and
mode o f differentiation o fthe American and
European eel populations.
M a t e r ia l s a n d M e t h o d s
A total o f 197 eels was collected from four
sites in Iceland (Fig. 1) as follows: (1) Rey-
khólar (N = 48), (2) Óxnalaekur (N = 70),
(3) Stokkseryi (N = 54), and (4) Villingholt-
vatn (N = 25). Frozen specimens were
shipped to our Iaboratories at Stony Brook
and Georgia, where assays o f M dh-2 and
m tD N A , respectively , were conducted.
( AFRICA
Fig. I. Freshwater geographic dístributions (shad-
ed areas) o f American and European eels; reproduction
occurs in the Sargasso Sea area. Numbered collectíon
locales in Iceland are described in Materials and Meth-
ods.
Numbers o f vertebrae in the Iceland spec-
imens were counted from X-ray photo-
graphs. In addition, 17 eels collected in Aar-
hus, Denmark, and 27 from Long Island,
N.Y., were scored solely for mtDNA geno-
type.
M dh-2 genotypes were assayed by starch
gel electrophoresis (Comparini and Rodino,
1980). m tD N A genotypes were determined
from restriction digestion profiles revealed
in Southem blot assays, using as a probe
previously purified eel m tDNA (Avise et al.,
1986). The DNA isolation and Southem
blotting procedures were similar to those
described by M aniatis et al. (1982). For each
specimen, either or both o f two endonu-
cleases, B glll and Pvull, were used to digest
total genomic DNA. These enzymes were
chosen because each produces gel profiles
that differ by at least two restriction site
changes in American versus European eels
(Avise et al., 1986). Hence the possibility
o f misdiagnosis o f an individual due to con-
vergent m utations at multiple m tDNA sites
is negligible.
For simplicity, in this paper the mito-
chondrial genotype “X ” will refer to the
pooled class o f typically European mtDNA
1256 J. C. AVISE ET AL.
T a b l e 1. Characteristics that distinguish eel populations in North America from those in Europe. AIso shown
are frequencies o f these traits in eels from Iceland.
T rait America Europe Iceland Reference
Vertebral number
Range
Freq. < 1 1 0
Freq. < 1 1 0
Malate dehydrogenase
Freq. M dh-2a
Freq. M dh-2a
Mitochondrial D N A
Freq. “C” genotype
Freq. “C” genotype
103-110
0.994 (N — 1,609)
0.958 (N = 696)
1.00 (N = 109)
1.00 (N = 27)
110-120
0.003 (N = 15,854)
0 .100(iV = 1,079)
0.00 (N = 29)1
0.00 (N = l l ) 2
108-118
0.033 (N = 241)
0.056 (N = 197)
0.129 (N = 241)
0.109 (N = 197)
0.036 (N = 197)
Williams and Koehn
(1984) and refer-
ences therein
Present study
Williams and Koehn
(1984) and refer-
ences therein
Present study
Avise et al. (1986)
Present study
1 EngJand and Ireland.
2 Denmark.
genetic markers (Avise et al., 1986), whiie
m tDNA “C” will refer to American mt-
DNA genotypes. Similarly, M dh-2b will re-
fer to a pooled class o f typically European
electromorphs, distinct from M dh-2a which
is the com m on allele in North America (Ta-
ble 1).
R e s u l t s
Genetic Status o f Fish with
Low Vertebral Counts
In the current sample o f 197 fish from
Iceland, 11 (or 5.6%) exhibited vertebral
counts o f 110 or less. Thís value represents
roughly a 17-fold increase in the frequency
o f such “ low count” eels compared to other
European locales, but is consistent with pre-
vious estimates for the Iceland population
(Table 1). The following comparisons are
based on data summ arized in Table 2 and
Figure 2. These data involve genotype fre-
quencies for m tD N A and M dh-2, their as-
sociations with one another (Table 2), and
th e ir associations w ith verteb ra l count
numbers (Fig. 2). Since Boetius’ (1980) hy-
potheses refer specifically to such low count
fish, we will initially focus attention on the
genetic status o f eels in this lower end of the
frequency distribution o f vertebral numbers
(Fig. 2). We will then examine properties of
the pooled collections o f Icelandic eels.
Hypothesis 1: Icelandic eels with low ver-
tebral counts are American expatriates. If
the Icelandic eels with Iow vertebral num-
bers are “pure” American eels that happen
to have settled in Iceland, they should rep-
resent a random draw from the American
gene pool. They do not. Six o f the 11 eels
with 110 or fewer vertebrae possess mtDNA
genotype “X ” that has not yet been ob-
served in any American locale (Table 1). O f
the remaining five eels with low vertebral
numbers, none is homozygous for M dh-2a/
M dh-2a, the prevalent allozyme genotype in
the Americas. One o f these latter individ-
uals is homozygous for M dh-2b/M dh-2b, a
genotype expected with frequency 0.002 in
America, while the other four are hetero-
zygotes {Mdh-2a/M dh-2b). The probability
that any single eel from America is a het-
erozygote is 0.08; the probability that four
such eels would all be heterozygous is 4 x
10“5. Clearly then, eels with low vertebral
counts in our Iceland sample are not Amer-
ican expatriates collectively, nor with high
likelihood are they pure American eels in-
dividually. Hypothesis 1 also seems unlike-
ly on morphological grounds alone, since all
11 Icelandic eels with “ low” vertebral num-
bers have counts above the American mean.
Hypothesis 2: Icelandic eels with low ver-
tebral counts are ontogenetic abnormalities
within the European gene poo l If the Ice-
landic eels with low vertebral numbers are
“ pure” European eels, they should provide
a random sample (with respect to genes not
involved in vertebral development) from the
European gene pool. They do not. Five o f
the 11 eels with 110 or fewer vertebrae pos-
sess m tD N A genotype “C” that has not yet
ICELAND EELS 1257
T able 2. Numbers (in parentheses) and frequencies
o f the joint M dh-2 /m tD N A genotypes in eels from
Iceland. The cytonuclear associations (and their stan-
dard errors) are summarized using the allelic (D ) and
genotypic (D \, D i, D 3) disequilibríum statistics o f As-
mussen et al. (1987).
M dh-2
chondria a/a a/b b/b Total
c 0.000 0.030 0.005 0.035
(0) (6) (1) (7)
X 0.000 0.188 0.777 0.965
(0) (37) (153) (190)
Total 0.000 0.218 0.782 1.000
(0) (43) (154) (197)
D = 0.011 ± 0.005
D \ = 0.000 ± 0.000
d 2 = 0.022 ± 0.009
d 3 = - 0 .0 2 2 ± 0.009
been observed in any European locale (Ta-
ble 1). O f the remaining six eels with low
vertebral count numbers, five are hetero-
zygous for M dh-2a/M dh-2b, an allozyme ge-
notype observed in Europe with frequency
0.18. Hence the probability that any o f these
latter eels is “ pure” European is less than
20%, and the probability that all five are
E uropeanis2 x 10“4. Clearly, eels with low
vertebral counts in our Iceland sample do
not possess typical European genotypes.
Hypothesis 3: Icela.nd.ic eels are part o f a
selection-mediated cline o f genotype fre-
quencies in one Atlantic eel gene pool. This
possib ility , n o t considered by Boetius
(1980), suggests that the interm ediate allele
and vertebral count frequencies in Iceland
eels (Table 1) represent selection-mediated
responses to an Icelandic habitat that is
somehow interm ediate to m ost American
and European locales. I f so, allele frequen-
cies at several loci might indeed be shifted
concordantly. However, within the Iceland
population, there should be no particular
pattem o f association among unlinked (and
nonepistatic) genes, or between such genes
and vertebral count numbers. But such as-
sociations do exist (Fig. 2). In a 2 x 2 test
o f independence (Sokal and Rohlf, 1969),
involving the m tD N A genotypes “C” and
“X ” and the vertebral count categories <
110 versus >110, there is a highly signifi-
cant association between the American-type
m tDNA and low vertebral count number
No. Vertebrae
F ig . 2. Frequency distribution o f vertebral count
numbers in the current sample o f eels from Iceland.
Shaded areas o f the histogram indicate fish with the
heterozygous genotype M dh-2a/M dh-2b (no M dh-2a/
M dh-2“ homozygotes were observed). In parentheses
are the numbers o f individuals with various vertebral
counts that exhibited the m tDNA-C genotype nor-
mally characteristic o f American eels.
(G = 24.1, P c 0.01). In a similar test in-
volving Mdh, there is a comparably strong
association between M dh-2a and low num-
bers o f vertebrae (G = 21.4, P <c 0.01).
(Associations between the M dh and mt-
DNA genotypes will be discussed later.)
Hypothesis 4: Icelandic eels represent the
founder stock fo r both American and Euro-
pean eelpopulations. U nder this hypothesis,
the Icelandic gene pool contains American
and European genotypes by virtue o f reten-
tion o f polymorphisms from an ancestral
stock in Iceland. This possibility seems very
unhkely since Iceland became habitable only
about 10,000 years ago. Furthermore, any
retained polymorphisms at unlinked and
nonepistatic loci are not expected to be as-
sociated w ithin particular individuals. But
as discussed beyond, such associations be-
tween m tD N A and M dh-2 do exist, as do
associations between these genotypes and
vertebral count numbers.
Hypothesis 5: Icelandic eels with low ver-
tebral counts include F, hybrids between
American and European forms. The most
com m on genotypes expected in F^ hybrids
between American and European eels are
M dh-2a/M dh-2b/m tÐ N A -C , and M dh-2a/
M dh-2b/m tÐ N A -X , depending on whether
an American or European eel was the female
parent in the cross. (From Mendelian cal-
culations, the likelihood that one or the oth-
er o f these genotypic classes is present in an
1258 J. C. AVISE ET AL.
F, is 0.86.) Among the 11 eels with low
vertebral numbers, 5 were M dh-2a/M dh-2b/
m tDNA-C, and 5 were M dh-2a/M dh-2b/
m tDNA-X. This finding suggests that these
indivíduals may indeed be first generation
hybrids, and furtherm ore that the crosses
involved in their production took place in
both directions with respect to sex.
Nonetheless, an analysis o f markers from
multiple nucleargenes would be required to
firmly establish that these indíviduals are
Fi as opposed to later generation hybrids.
For example, a first-generation backcross to
a European eel would be expected to possess
either o f the two M dh/m XD NA genotypes
listed above with probability 0.52. In fact,
there are two initial lines o f evidence to sug-
gest that our Iceíandic eel sample as a whole
includes some non-F! hybrids. First, one
individual with low vertebral count number
exhibited M dh-2b/M dh-2b, a genotype ex-
pected in an F, with probability only 0.04.
Second, even after rem oval o f the 11 eels
with vertebral counts < 110 from our Ice-
land sample, significant associations remain
between lower vertebral count numbers (in
this case 111-113) and both the M dh-2a and
m tD N A -C frequencies (G = 17.2 and 16.8,
respectively; P <s 0.01).
Thus overall, there is strong genetic evi-
dence for hybridization between American
and European eels. M ost o f the eels in Ice-
land w ith low vertebral count numbers are
likely Fi or other early generation hybrids.
In addition, there is a probable invasion of
American genes (via backcrossing) into the
predom inantly European gene pool o f Ice-
landic eels. We will now estimate the rela-
tive contributions o f American and Euro-
pean alleles to the Icelandic stock.
Gene Flow into the Iceland
E el Population
The eel stock in Iceland clearly contains
a mixture of alleles from America and Europe.
The contribution o f European genes to the Ice-
landic gene pool can be estim ated by
M = (qh - q y ( q h - q.J (1)
(Wallace, 1968 p. 81), where qz, qb, and qh
represent the frequencies o f the M dh-2a (or
mtDNA-C) allele in America, Europe, and
íceland, respectively. Using the M dh-2 al-
lele ffequencies sum m arizedin Table 1 (with
qh the weighted average of M dh-2a in the
two surveys), M = 0.977. This value agrees
closely with the estimate of M = 0.964 ob-
tained from a sim ilar analysis o f the m t-
DNA haplotype frequencies (Table 1). Thus
Iceland eels exhibit European genes pre-
dominantly, and both M dh-2 and m tDNA
indicate that only about 2-4% (i.e., 1 — M )
o f the gene pool in the Iceland eel popula-
tion is derived from American eel ancestry.
Interestingly, the percentage shift in the
mean vertebral count num ber in Icelandic
eels toward the American population mean
(9%) appears generally consistent with these
conclusions.
Additional inform ation can be extracted
from the jo in t distributions o f m tDNA and
M dh-2, as sum m arized by allelic (D) and
genotypic (£>,, D 2, and D 3) cytonuclear dis-
equilibria defined by Asmussen et al. (1987).
The param eter D measures the association
between alleles at a nuclear and a cytoplas-
mic locus, and D ,, D 2, and D 3 measure as-
sociations between two cytotypes and the
three respective genotypes at a diallelic nu-
clear locus. These four measures o f disequi-
libria are expected to exhibit certain pat-
tems in a hybrid zone depending on a variety
o f factors such as mating behavior, selec-
tion, and migration. Table 2 shows the cy-
tonuclear disequilibria calculated for Ice-
landic eels. Using the G-test approach
described in Asmussen et al. (1987), the hy-
pothesis that all four disequilibria equal zero
can b e re jec ted íU ^ 13.65, P = 0.001), while
the hypothesis that D, alone equals zero
cannot (G = 0.04, P = 0.84). (Because of
the small expected counts in some cells of
Table 2, we confirmed that the G-value of
13.65 was significant by an exact test that
involved calculating the multinom ial prob-
abilities o f all possible tables wíth the same
marginal counts as those exhibited by Table
2.) We conclude that there are significant
associations between m tD N A and M dh-2
in the Iceland population.
To explain the pattem of cytonuclear as-
sociation in the context of migration of eels
into Iceland, we can apply the models de-
veloped by Asmussen et al. (1989). As ap-
plied to the current situation, we can view
the Iceland stock as being composed of some
ICELAND EELS 1259
fraction o f pure European and American
eels, and some fraction o f hybrids stemming
from random mating in the hybrid zone.
We further assume that the censusing takes
place after mating, migration o f pure Amer-
ican and European eels to Iceland occurs at
a fixed rate per (nonoverlapping) genera-
tion, and genotypes are neutral with respect
to fitness. Recursions for the cytonuclear
genotypic frequencies under this model are
given by Equations (B4) in Asmussen et al.
(1989). The model was fitted to the data of
Table 2 by the m ethod o f maximum like-
lihood, under the assum ption that the Ice-
land eel population is at genetic equilibri-
um. The best goodness-of-fit (G = 8.08, P
= 0.044) was obtained when the per-gen-
eration m igration rates o f pure American
( m x) and pure European (m 2) eels into the
Iceland population were 0.02 and 0.70, re-
spectively. Thus by this approach, the ac-
cumulated proportion o f Icelandic alleles
with European ancestry is M = m 2/(m x +
m 2) = 0.972. This estim ate is virtually iden-
tical to the values obtained above from a
consideration o f the m tDNA and nuclear
genotypes separately (M = 0.964 and 0.977,
respectively).
Spatial Structure o f Genotypes
American and European eels have dis-
tinct dispersal pattem s that take them to the
appropriate continent. In the current study,
we also have the first evidence for nonran-
dom settlement o f eels on a microgeograph-
ic scale. Among the four collection sites in
Iceland, there was significant heterogeneity
in the frequencies o f both the M dh-2a and
m tDNA-C alleles (GH = 19.7 and 20.7, re-
spectively, both P < 0.01), and in frequen-
cies o f fish w ith <110 versus >110 verte-
brae (Gn = 14.3, P < 0.01). For example,
all seven individuals carrying mtDNA-C
were present in the Reykhólar collection, 37
o f the 43 M dh heterozygotes were observed
in the Reykhólar and Öxnalaekur collec-
tions, and all 11 fish with <110 vertebrae
were in Reykhólar and Öxnalaekur. Such
nonrandom spatial distributions o f geno-
types and morphologies raise the possibility
that specific subsets o f eel reproduction
(products o f certain spawns or sets o f
spawns) may occasionally tend to stay to-
gether and settle jointly. Nonetheless, any
particular distribution o f genotypes on a fine
spatial scale would likely be ephemeral,
changing with each round o f reproduction
and current-m ediated migrational influx. I f
this is tm e, the microspatial differences
w ould n o t be expected to accum ulate
through time, and hence are not necessarily
inconsistent with the absence o f dram atic
macrogeographic heterogeneity o f gene fre-
quencies within regions such as N orth
America or Europe (Avise et al., 1986; Wil-
liams and Koehn, 1984). In the future, it
would be o f interest to m onitor tem poral
variation in genotype frequencies at partic-
ular locales.
D is c u s s io n
We have shown that the Reykhólar and
Öxnalaekur samples o f eels in Iceland in-
clude, in low frequency, hybrids between
American and European forms. This hybrid
situation is highly unusual, because the lo-
cation in which the hybrid animals are found
as juveniles and young adults is presumably
far rem oved from where the mating events
take place (some 5,000 km away, in the Sar-
gasso Sea). W hat could account for the orig-
inal genetic separation o f American and Eu-
ropean eels, and for the occurrence o f
hybrids in Iceland? The following scenarios
are based on available genetic and life his-
tory data for eels, and should be viewed as
hypotheses requiring further evaluation.
At some tim e in the past, all N orth At-
lantic eels m ust have belonged to a single
population that subsequently became sep-
arated into American and European forms.
The current nucleotide sequence divergence
in m tDNAs between American and Euro-
pean populations (after correction for with-
in-continent divergence) is approximately
p = 0.03 (Avise et al., 1986). U nder a “con-
ventional” m tD N A clock calibration o f 2%
sequence divergence per m illion years
(Brown et al., 1979; Shields and Wilson,
1987), a separation time o f approximately
1.5 million years ago is suggested. The mul-
tilocus allozym e d istance [N ei’s (1972)
measure] is D = 0.11 codon substitutions
per locus (Williams and Koehn, 1984),
which also suggests a divergence tim e of
perhaps 1-2 million years under some “con-
1260 J. C. AVISE ET AL.
ventional” protein clock calibrations (see
A vise and A quadro , 1982). W hile the
m tD N A and protein estimates o f diver-
gence times are provisional, they both point
to a tim e o f separation in the Pleistocene.
Ancestral eels in the N orth Atlantic prob-
ably exhibited a catadrom ous life cycle [no
species o f Anguillidae is known to pass its
entire life history in freshwater, and all other
Anguilliformes are strictly marine (Mar-
shall, 1966; Moyle and Cech, 1982)]. These
ancestral eels m ay have bred as one popu-
lation, producing larvae destined for one
continent or geographic region. The follow-
ing “dispersal” scenario will assume that
juveniles o f the ancestral population oc-
curred in Europe and secondarily colonized
N orth America, but the arguments hold
equally well i f the direction of continental
colonization is reversed.
Suppose th a t during the P leistocene,
shifting oceanic currents brought some lar-
vae normally destined for Europe within
reach o f the N orth Ameriean coastline, and
that some o f these larvae settled “prema-
turely” (North Atlantic current pattem s are
thought to have varied widely in the Pleis-
tocene, due to global climatic changes as-
sociated w ith glacial advances an d re-
tre a ts —e.g., KefFer e t al., 1988). A fter
maturing in N orth America, and on retum -
ing to the sea to reproduce, these eastward-
swimming eels would likely have first en-
countered “ suitable” waters for spawning in
the westem portion of the Sargasso Sea area,
while eels retum ing westward from Europe
would first encounter suitable spawning
waters in the eastem Sargasso Sea area.
Hence there may have been an initial ten-
dency for assortative mating by continental
origin due simply to the geographic posi-
tioning o f retum ing adults.
Suppose further that these oceanie cur-
rents persisted, and that there was some ini-
tial genetic variation with respect to larval
settlement times. Today, American eels set-
tle in about 1 year and European eels settle
after 2 years or m ore (Williams and Koehn,
1984). Initially, as now, there m ust have
been strong disruptive selection favoring
larval settlem ent on one continent or the
other, eventually leading to the bim odal dis-
tribution o f larval settlement times. Con-
comitantly, this selection pressure should
have provided a fitness advantage to any
genetically based behav io ra l tendencies
(migration routes or mating preferences per
se) leading to assortative m ating among eels
from the two eontinents. Thus once set in
m otion by an initial continental coloniza-
tion event, a selection-driven feedback pro-
cess should have reinforced any original
tendency for premating isolation between
the two eel forms. An im portant component
o f this premating isolation is no doubt the
continuing spatial separation within the
Sargasso Sea of the m ajor concentrations for
breeding o f American versus European eels
(Schmidt, 1925), but hom otypic mating
preferences in sympatry may also be at work
(see McCleave et al., 1987).
A lternatively , a “ v ica rian t” scenario
might be entertained to account for the orig-
inal separation o f American and European
eels. Perhaps a single ancestral population
produced larvae that dispersed to north-
central Atlantic coasts, particularly Green-
land, Ieeland, and northem Scandinavia.
W ith cooling during Pleistocene glacials, this
northem region became uninhabitable, and
forced a southward retreat and disjunction
o f spawning areas. Two separate breeding
grounds may then have produced larvae
destined for N orth America and Europe, re-
spectively. Adaptive choice o f spawning re-
gion would again be accompanied by shifts
in behavior o f larvae enabling them to reach
appropriate temperate coasts. W ith the sub-
sequent retreat of sea ice and the reemer-
gence o f su itab le h ab ita ts no rthw ard ,
spawning areas may then have expanded
and secondarily overlapped, leading to the
current hybrid situation.
In any event, Iceland occupies a position
longitudinally interm ediate to N orth Amer-
ica and Europe (Fig. 1). Sínce we now know
that some hybrid eels occur in Iceland, it
seems reasonable to speculate that this is
the result o f an interm ediate hybrid migra-
tional behavior. This behavior could reflect
larval dispersal along unique currents stem-
ming from the geographically interm ediate
spawning grounds in the Sargasso Sea where
American and European eels presumably
overlap, and/or an interm ediate settlement
tim e from ocean currents sweeping by Ice-
land. A general behavioral intermediacy of
hybrid animals is not unusual (Brown, 1975;
ICELAND EELS 1261
Lamb, 1987), and there is at least one known
precedent for the intermediacy o f hybrids
with respect to migratory behavior: Berthod
and Q uem er (1981; see also Berthod, 1988)
found that hybrids between migratory and
nonmigratory European warblers exhibit
pattem s o f migratory restlessness interme-
diate to those o f their parents.
Nonetheless, there are some potential
problems with this simple hypothesis for
the elevated frequency o f hybrid eels in Ice-
land. Surface currents o f the G ulf Stream,
after crossing the N orth Atlantic, are thought
to pass the British Isles before swinging west
in higher latitudes and reaching Iceland (this
presumably accounts for the great prepon-
derance o f European genotypes in the Ice-
landic eel population). Yet England does not
appear to exhibit an elevated frequency o f
American vertebral count numbers. How-
ever, ocean currents and eddies in the North
Atlantic, particularly at various depths, are
not well understood (Richardson, 1985), and
it is quite possible that certain eddies reach
Iceland via a m ore direct route from the
Sargasso Sea, carrying with them hybrid lar-
vae from an overlap zone in the breeding
area. Or perhaps young eels actively swim
north from the G ulf Stream, at an inter-
mediate settlem ent time, to reach Iceland.
W hat have been the genetic consequences
o f hybridization in eels?—are the hybrids
an evolutionary dead-end, or have they pro-
vided an avenue o f gene exchange between
the American and European forms? For ex-
ample, Boetius (1980) found that mean
numbers o f vertebrae are homogeneous over
m ost o f the European range o f eels, but are
shifted slightly toward American values in
localities such as Scotland and Sweden, a
result that could be interpreted as evidence
for introgression o f American genes into the
northem European gene pool (sample sizes
are not yet large enough to evaluate the pos-
sibility o f a comparable shift in northem
Europe in frequencies o f M dh-2 or m tD N A
genetic markers). Answers to questions
about the m agnitude and pattem o f genetic
introgression depend in large part on as-
sumptions about the ancestral condition of
the American and European gene pools.
Suppose, as an ex trem e exam ple, th a t
American and European eels were at one
tim e fixed for altem ate alleles at M dh-2. An
application o f Equation (1) to the M dh-2
data in Table 1 then suggests that about 10%
o f the nuclear genes in Europe are o f Amer-
ican ancestry, and that about 4% o f the nu-
clear genes in America are o f European an-
cestry. But an altem ative interpretation is
that the presence o f both M dh-2 alleles on
the two continents represents the parallel
retention o f an ancestral polym orphism in
the absence o f any introgression. W ith very
large genetíc samples o f European eels, it
might be possible at least partially to eval-
uate these competing hypotheses: if hybrid-
ization and introgression were predomi-
nantly recent, genetic disequilibrium might
rem ain among alleles at unlinked loci, and
associations could exist between such mark-
er genes and particular morphological fea-
tures such as vertebral counts.
Overall, we have shown that the Icelandic
eel stock includes, in low frequency, the
products o f hybridization between Ameri-
can and European eels. Associations be-
tween M dh-2 and m tD N A genotypes, mor-
phologies, and locations strongly imply that
there is an im portant additive genetic com-
ponent to intermediate (hybrid) eel verte-
bral count numbers and m igrational behav-
ior. While the firm documentation o f hybrids
in Iceland eliminates some o f the hypoth-
eses previously advanced to account for the
unusual properties o f Icelandic eels, the
findings also raise many new questions, par-
ticularly about the specific location o f the
hybrid breeding grounds, and the migra-
tional routes taken by hybrid larvae. Fur-
ther field studies, perhaps in conjunction
with genetic tests, will be required.
A c k n o w l e d g m e n t s
We thank M. Ball and B. Bowen for useful
discussion and help with data analyses and
J. H. M cDonald for running the protein gels.
The Institute o f Freshwater Fisheries in Ice-
land provided generous assistance in ob-
taining specimens for this study. W ork was
supported by NSF G rant BSR-8805360 (to
J.C.A.).
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Correspondíng Editor: R. L. Honeycutt
FOLIA PARASITOLOGICA 54: 141-153, 2007
Parasite communities of eels Anguilla anguilla in freshwater and
marine habitats in Iceland in comparison with other parasite
communities of eels in Europe
Árni Kristmundsson and Sigurður Helgason
Institute for Experimenta! Pathology at Keldur, University of Iceland, v/Vesturlandsveg, IS-l 12 Reykjavik, Iceiand
Key words: Anguilla anguilla, eel, parasites, parasite communities, diversity, species richness, comparison, Iceland
Abstract. Ninety-five eels from one marine and three freshwater localities in Iceland were examined for parasites. Twenty spe-
cies were found, 12 from marine habitat, 12 from freshwater and 4 species were found in both habitats. These are: Eimeria an-
guillae, Chilodonella hexasticha, Tríchodina fultoni, T. jadraníca, Myxidium giardi, Myxobolas kotlani, two Zschokkella spp.,
Derogenes varicus, Deropristis inflata, Diplostomum sp., Plagioporus angalatus, Podocotyle atomon, Anisakis simplex (larva),
Eustrongylides sp. (larva), Hysterothylacium aduncum (larva), Raphidascaris acus (larval and adult stages), Bothríocephalus
claviceps, Proteocephalus macrocephalus, and a pseudophyllidean iarva. Thirteen of these species are new parasite records trom
Icelandic waters. The component community o f marine eels was characterized by low diversity and a high dominance of a single
species. Overall, seven species of helminths were observed, up to five different species occurring in an individual ftsh. The com-
ponent community of the freshwater eels was species-poor with Iow diversity and relatively high dominance of single species. A
between-sites difference in the freshwater eels was considerable; only Diplostomum sp. was found at more then one sampling
site. Similar to previous studies, there is a total replacement of freshwater macroparasite species by marine ones in saline waters.
But unlike research abroad in which species richness decreases with higher salinity, the marine eels in Iceland have considerably
higher richness than the freshwater ones. The parasite communities of freshwater eels in Iceland are, in general species-poorer,
less diverse and having higher Berger Parker (BP) dominance than other eel communities in Europe. Marine eels have on the
other hand comparable species richness, are less diverse and with a high BP dominance.
Five species o f fishes live in the Icelandic freshwater
ecosystem: Atlantic salmon Salmo salar L., brown trout
Salmo trutta L., arctic char Salvelinus alpinus (L.),
three-spined stickleback Gasterosteus aculeatus L., and
eel Anguilla anguilla (L.). According to Albert et al.
(2006), about 15% o f the eel population in Iceland are
hybrids between A. anguilla and the American eel, A.
rostrata (Lesueur). During the last decades, extensive
research on the parasite fauna o f the European eel has
been carried out in many European countries (e.g. Koie
1988, Kennedy 1997, Kennedy et al. 1997, Borgsteede
et al. 1999, Sures et al. 1999, Saraiva et al. 2005). To
date, observations on parasites o f Icelandic freshwater
fishes have been limited; only few papers published,
focusing on parasites o f salmonids (Stephenson 1940,
Brinckmann 1956, Baer 1962, Richter 1981, Richter
1982a, b, c, Malmquist et al. 1986, Frandsen et al. 1989,
Kristmundsson and Richter 2002-2003) and three-
spined sticklebacks (Blair 1973). The present study is
the first one made on the parasite fauna o f eels in Ice-
land. This paper presents the composition and diversity
characteristics o f parasite communities o f freshwater
and marine eels in Iceland in comparison with other
similar studies in Europe.
MATERIALS AND METHODS
Study area and fish eollection. A total number of 95 eels
from one marine (GV) and three freshwater localities (OL, ST,
VV) were examined (Fig. 1). The eels were caught in fyke
nets; samples from OL in September 2000 and 2001; from ST
in August 1999 and August-September 2000; írom VV in
June 2000 and October 2001; from GV in June-July 2001. Eel
length ranged from 34.0 to 63.5 cm (median 53.5 cm) in OL,
from 33.5 to 72.5 cm (median 59.3 cm) in ST, from 33.0 to
71.0 cm (median 54.3 cm) in VV and from 42.0 to 71.0 cm
(median 52.3 cm) in GV (Fig. 2).
Fig. 1. Sampling sites. GV - Grafarvogur (n = 20), a shallow
creek with a salinity of 30-33%o; OL - ditches and tributaries
of the glacial river Olfusa (n = 15); ST - Steinsmyrarfljot
(n = 30), a small shallow lake (max depth <2.5 m); VV - Vi-
filsstadavatn (n = 30), a small shallow lake (max depth <2.5
m). All three freshwater localities harbour brown trout, arctic
char and three-spined sticklebacks; OL also harbours salmon.
A ddress for correspondence: Á. K ristm undsson, Institute for Experim cntal Pathology, University o flce lan d , K eldur v/Vesturlandsveg,
IS -112 Reykjavik, Iceland. Phone: ++354 585 5100; Fax: ++354 567 3979; E-mail: amik@ hi.is
141
mailto:amik@hi.is
Fig. 2. Length distribution of eels from the localities studied.
The eels were brought alive to the Iaboratory and either
kept alive in aquaria until they were examined (completed
within a week of capture), or kept frozen at -20°C for subse-
quent examination. If examined frozen, the gills were excised
and put in 70% alcohol prior to freezing.
Examination o f eels and identifícation o f parasites. The
eels were killed with an overdose of phenoxyethanol, and their
length and weight was determined. The extemal surface, fins,
nostrils, buccal cavity, each gill arch and excised eyes were
examined thoroughiy with a stereoscope. Smears ffom blood
and eye tissues and scrapings from the extemal surface and
from slices of two gill arches ffom each side of a fish were
examined for parasites with a compound microscope. The
visceral cavity and ail major organs (heart, brain, liver, kidney,
spleen, gall bladder, urinary bladder, swim-bladder and go-
nads) were examined thoroughly using both a microscope and
a stereoscope. The alimentary tract was removed; the oe-
sophagus, stomach and intestine, each kept separate in Petri
dishes, were split longitudinaily and scrapings ffom all parts
prepared for a microscopic examination. Finally contents of
the stomach and the intestine were searched for intestínal
helminths using both microscope and stereoscope. Ciliates of
the genera Chilodonelía and Trichodina were identified by the
use of Klein’s silver nitrate technique (Klein 1958). To íden-
tify cestode species, proglottids were stained with Schneider’s
acetocarmine (Ash and Oriel 1987). Final identification to a
species and/or genus level, was based on Bykhovskaya-
Pavlovskaya et al. (1964), Lom and Dyková (1992), Moravec
(1994), Hoffmann (1999) and Buchmann and Bresciani
(2001).
Determ ination o f helminth community structure and
statistical treatment. Specialists are defined as those para-
sites that occur and reproduce almost exclusively in eels
whereas generalists are those that commonly occur in other
families of fishes. Definitions of other ecological terms are
according to Bush et al. (1997). Analysis of the parasite com-
munity structure was carried out at both component and inffa-
community level. The measures of the component community
structure adopted were: species richness (total number of spe-
cies), the Shannon-Wiener (SW) diversity index and its Even-
ness, Simpson’s reciprocal index (SLl/Ð) and the Berger-
Parker dominance index (BP). To get comparative figures
from several other simílar studies, in which different logarithm
(log2) was used, the diversity indices were recalculated from
data given. Additionally, diversity indices and dominance
values from data given in a number of publications in which
those community characteristics where not analysed were
calculated. The measures of the inffacommunity structure
adopted were: mean number of individuals and species per eel,
the maximum number of species per eel, the mean Brillouin’s
index (BI) (all eels and infected eels only) and the maximum
value of the BI. All indices were calculated and defmed ac-
cording to Magurran (1988) using natural iogarithm (In) where
appropriate. The Percentage Similarity index (quantitative
measure) and the Sörensen’s index of similarity (qualiíative)
(Magurran 1988) were used to measure similarities between
localities at the component level. Statistical difference be-
tween the Shannon Wiener diversity indices of the localities
studied was tested using a modified í-test proposed by
Hutcheson (1970).
RESULTS
Composition of the parasite communíties Table 1
Four protozoan species were found. Eimeria anguil-
lae Léger et Hollande, 1922 (Sporozoa: Cocccidia) was
detected in the intestine o f one freshwater and one ma-
rine eel. Tridiodina jadranica Raabe, 1958 (Ciliophora:
Trichodinidae) was ffequent on the gills o f eels from
VY and OL as was Trichodina fu lton i Davis, 1947
(Ciliophora: Trichodinidae) on the skin and gills o f eels
from OL and ST. Chilodonella hexasticha (Kiemik,
1909) (Ciliophora: Chilodonellidae), also on gills and
skin, was found only on eels from OL. Four myxozoan
species, Myxidium giardi Cépéde, 1906 (Bivalvulida:
M^otidiidae), Myxobolus kotlani Molnár, Lom et Malik,
1986 (Bivalvulida: Myxobolidae) and two Zschokkella
spp. (Bivalvulida: Myxidiidae), were observed from
both freshwater and marine localities, the three latter
species only on rare occasions (prevalence: 3.3 to 6.6%)
but M. giardi in high prevalence (30.0 to 93.3%) at all
sampling sites. Myxidium giardi most heavily infected
the gills, but kidneys and various other organs were also
frequently infected. Myxobolus kotlani was detected
ffom fms and two species o f Zschokkella, one in fins
and the other one in the stomach mucosa.
Twelve helminth species were found; seven in the
marine eels and five in freshwater ones. The marine eels
had oniy marine species and the freshwater eels only
freshwater species. Diplostomum sp. (metacercariae)
(Strigeoídea: Diplostomatidae) was found in eels from
all the freshwater sites and was the most prevalent
helminth species at ST (66.6%) and OL (20.0%). An
encapsulated larval stage o f the nematode Eustrongyl-
ides sp. (Dioctophymatiodea: Dioctophymatidae) was
found only in the stomach wall o f eels from W
(13.3%). One specimen o f a third-stage larva o f Ani-
sakis simplex (Rudolphi, 1809) (Ascaridida: Anisaki-
dae) was found in the visceral cavity o f one marine eel.
Nine species o f gastrointestinal helminths were present
in the eels: four species o f digeneans, Deropristis inflata
(Molin, 1859) (Allocreadiodea: Deropristiidae), Dero-
genes varicus (Miiller, 1784) (Hemiuroidea: Derogeni-
dae), Podocotyle atomon (Rudolphi, 1802) (Allocrea-
diodea: Opecoelidae) and Plagioporus angulatus Du-
142
Table 1. Infccted organs, prevalence (P), mean intensity and intensity range of the parasite spccies found at the localities studied.
Locality
(Salinity)
Number of eels examined
OL
(0%o)
15
Intensity
ST
(0%o)
30
Intensity
VV
(0%o)
30
Intensity
GV
(30-33%o)
20
Intensity
Infected Mean Mean
Protozoa organs p Range ±SD P Range ± SD P Range ±SD P Range ±SD
Eimeria anguillae* I 6.6' ND ND _ _ _ _ _ _ 5.0’ ND ND
Chilodonella hexasticha * G/S X ND ND _ - _ - _ „ _ _ _
Trichodina fultoni* G/S X ND ND X ND ND - _ _ - .... „
Trichodina jadranica* G X ND ND _ _ - X ND ND - - _
Metazoa
Myxidium giardi* G/K/VO 93.3 ND ND 33.3 ND ND 30.0 ND ND 70.0 ND ND
Zschokkella sp.-l* F 6.6' ND ND 6.6 ND ND - ... - _ _ -
Zschokkella sp.-2* SW - ~ - - _ 6.6 ND ND 5.01 ND ND
Myxobolus kotlani* F 6.6' ND ND 3.3' ND ND _ _ - 5.0’ ND ND
Diplostomum sp. E 20.0 1-6 3.6 ±2.5 66.6 1-13 3.4 ±2.8 20.0 2-14 6.0 ±5.9 _ - _
Derogenes varicus ST - ~ - _ _ _ _ _ _ 45.0 1-6 1.7 ± 1.6
Deropristis inflata * I - - _ - „ _ „ 85.0 2-379 104.6 ± 123.7
Podocotyle atomon I - - _ _ _ _ _ 20.0 1-3 1.7 ±0.9
Plagioporus angulatus * I - - - __ _ _ - 15.0 1-6 3.7 ±2.5
Anisakis simplex VC _ - _ _ _ _ _ _ _ 5.01 1 1
Hysterothylacium aduncum I - - _ - _ _ _ _ _ 10.0 1-2 1.7 ±0.5
Raphidascaris acus * I - - - 43.3 1-18 4.0 ±5,0 _ _ _ _ _ _
Eustrongylides sp.* SW - - - _ _ 13.3 1-2 1.5 ±0.5 _ „ _
Proteocephalus macrocephalus * I ~ _ _ 16.6 1-2 1.3 ± 0.5 - „ _ „ _ _
Bothriocephalus claviceps* I _ - _ _ _ 26.6 1-25 5.7 ±7.9 _ _ _
pseudophyllidean larva I/IW - - - _ - _ _ „ - 10.0 2 2.0 ±0.0
*New parasite records for Iceland.; G - gills; K - kidney; F - fin; I - intestine; S - skin; E - eye; VC - visceral cavity; IW - intestinal wall; ST - stomach; SW - stomach wall;
VO - various organs; 'only one eel infected; X - species found but prevalence not determined; ND - number of parasites not dctermined.
143
jardin, 1845 (Fasciolata: Opecoelidae); two nematode
species, Raphidascaris acus (Bloch, 1779) (Ascaridida:
Anisakidae) and Hysterothylacium aduncum (Rudolphi,
1802) (larva) (Ascaridida: Anisakidae); and three
cestode species, Bothriocephalus claviceps (Goeze,
1782) (Pseudophyllidea: Bothriocephalidae), Proteo-
cephalus macrocephalus (Creplin, 1825) (Proteocephal-
oidea: Proteocephalidae), and a pseudophyllidean larva.
In marine eels, the eel-specific parasite D. inflata was
by far the most prevalent species (85.0%). In fresh-
water, the nematode R. acus was the most prevalent
intestinal helminth at locality ST (43.3%) and the
cestode B. claviceps at locality W (26.6%). No intesti-
nal helminths were detected at locality OL.
Similarity between communities Tables 2, 3
The only macroparasite species any two sampling
sites had in common was Diplostomum sp. On a qualita-
tive basis (Sörensen’s index), the levels o f total compo-
nent similarity of macroparasite communities between
the three freshwater sites ranged from 0.33 to 0.50. It
was the same for OL-ST and O L -W (0.5) but lower for
S T -W (0.33). On a quantitative basis (Percentage simi-
larity index) the OL-ST values were 54% but 41% for
O L -W and W -S T . The eels from the marine site GV
and those from the three freshwater sites harboured en-
tirely different helminth species. None o f the localities
had any intestinal helminth species in common; there-
fore their intestinal helminth communities were com-
pletely dissimilar. The Sörensen’s index between the
total microparasite component communities was gener-
ally rather high. It was highest for GV-ST (0.75) but
lowest for VV-ST (0.29).
Component community structure Tables 4, 5
The total macroparasite community o f eels from the
marine locality GV was richer (7 species) than the ones
from all freshwater localities (1-3 species). The diver-
sity was, however, significantly lower than from the
freshwater sampling sites ST and W , which had very
similar diversity values and the evenness was consid-
erably lower. The GV’s low diversity reflects its high
Berger-Parker dominance value (0.98), the eel specific
parasite Deropristis inflata being the dominant species.
Eels fforn the sampling site OL had the lowest value in
richness, diversity and evenness, harbouring only one
helminth species, Diplostomum sp. The freshwater lo-
calities ST and VV had very similar Berger-Parker
dominance values (0.54 and 0.52, respectively) but dif-
ferent dominant species, the cestode Bothriocephalus
claviceps and Diplostomum sp., respectively. Consider-
ing only intestinal helminths, all eels from OL were
uninfected; one species was present in W eels, two in
ST eels and six in GV eels. The diversity (SW and SI)
remained similar for GV but dropped for the freshwater
sites. Dominance values increased considerably at ST
and W but remained the same for GV. It was highest at
the freshwater locality VV, where the only species
found, Bothriocephalus claviceps, was completely
domínant and reached 0.90 at ST. The dominant species
for GV and VV remained the same but at sampling site
ST the nematode generalist Raphidascaris acus became
dominant species instead o f Diplostomum sp.
Table 2. Sörensen’s similarity index and Percentage similarity
index (parenthesis) between the total helminth communities
(above the diagonal) and the intestinal helminth communities
(below the diagonal) of the localities studied.
OL ST v v GV
OL - 0.50 (54.0) 0 .50(41 .0 ) 0 (0 )
ST 0 (0 ) - 0 .33(41 .0 ) 0 (0 )
W 0 (0 ) 0 (0 ) - 0 (0 )
GV 0 (0 ) 0 (0 ) 0 (0 ) -
Table 3. Sörensen’s similarity index for total microparasite
component communities of the localities studied.
OL ST VV GV
OL
ST
VV
0.73
0.40 0.29
GV 0.55 0.75 0.57 -
Table 4. The diversity characteristics of the total and intestinal
helminth component community of eels from Icelandic waters.
Locality
W ST OL GV
Total component com m unity
N um ber o f eels 30 30 15 20
N um ber o f species 3 3 1 7
Shannon-W iener index 0.89 0.84 0 0.13
Simpson index 2.25 2.15 1.00 1.05
S-W evenness 0.81 0.77 0 0.06
Berger-Parker dom inance 0.52 0.54 1.00 0.98
Dominant species Bc £>sp Dsp D i
Intestinal com ponent com m unity
N um ber o f species 1 2 0 6
Shannon-W iener index 0.00 0.33 0 0.12
SW evenness 0.00 0.30 0 0.07
Simpson index 1.00 1.23 1.00 1.04
Berger-Parker dom inance 1.00 0.90 - 0.98
Dominant species Bc Ra - Di
Bc - Bothriocephalus claviceps\ /)sp - Diplostom um sp.; Di - D ero-
pristis inflata; Ra - Raphidascaris acus.
Table 5. Testing of statistical difference between the totai
component communities diversity indices of the localities
studied.
W ST OL
W -
ST NS - _
OL *** ***
GV *** *** NS
*** PO.001; NS -not significant difference.
Intestinal infracommunity structure Tables 6, 7
Prevalence o f coexistent helminth species in the in-
testine o f the eels differed markedly between localities.
Considerable differences occurred comparing the ma-
144
Kristmundsson, Helgason: Parasites of Icelandic eels
rine (GV) and freshwater localities (OL, ST, VV). Only
5% of the marine eels were uninfected compared to 50
to 100% o f the freshwater eeis. The prevalence o f infec-
tion also differed considerably between freshwater sam-
pling sites. A great majority (90 to 100%) o f the fresh-
water eels had none or one species o f intestinal
heiminths, few (0 to 10%) were infected with two spe-
cies and none had three helminth species in their intes-
tine. A striking difference was in the mean number o f
helminths per eel, between freshwater and marine sites,
the values being 0.00 to 1.93 in freshwater eels and
90.90 in marine eels. The mean number o f specíes per
eel was also considerably lower in the freshwater eels
(0.0 to 0.60) than the marine eels (1.85), considering all
eels. This difference decreased markedly looking only at
infected eels. Maximum number o f species parasitizing
individual eels was one at W , two at ST and four at the
marine site GV. The mean BI was low at all sampling
sites; the value for the marine locality though was con-
siderably higher than at the freshwater sites, 0.17 and
0.00 to 0.03, respectively (all eels). Considering in-
fected eels only, the BI for GV eels remained noticeably
higher. All eels from VV and OL had either no or one
species, 90% o f the ST eels but 45% o f the GV eels.
Table 6. Prevalence (%) of coexistent intestínal helminth spe-
cies of eels from the localities studied.
Locality
N uraber o f eels exam ined
VV
30
ST
30
OL
15
GV
20
0 species 73.3 50.0 100 5.0
1 species 26.7 40.0 0.0 40.0
2 species 0.0 10.0 0 .0 30.0
3 species 0.0 0.0 0 .0 15.0
4 species 0.0 0.0 0.0 10.0
DISCUSSION
The parasite community structure
A total o f 20 parasite species were observed, 4 proto-
zoans and 16 metazoans (Table 1). All the protozoan
and myxozoan species (Eimeria anguillae, Chilodonella
hexasticha, Trichodina fultoni, T. jadranica , Myxidium
giardi, Myxobolus kotlani, two Zschokkella spp.) and
seven o f the helminth species (Deropristis inflata, Pla-
gioporus angulatus, Raphidascaris acus, Eustrongylides
sp., Bothriocephalus claviceps and Proteocephalus
macrocephalus) are new parasite records from Icelandic
waters. Myxidium giardi, Myxobolus kotlani, E. anguil-
lae, D. inflata, P. macrocephalus and B. claviceps are
more or less strictly host specific, the others are general-
ists. Six species ('Derogenes varicus, D. inflata, Podo-
cotyle atomon, P. angulatus, Anisakis simplex and Hys-
terothylacium aduncum) are marine ones and five are
ffeshwater species (Diplostomum sp. larva, R. acus, Eu-
strongylides sp. larva, P. macrocephalus and B. clavi-
ceps). Myxidium giardi, Myxobolus kotlani, one o f the
Zschokkella spp. and E. anguillae were found both in
freshwater and marine environment. Although reporfed
both from freshwater and marine environment (Lom and
Dyková 1992), Trichodina jadranica and T. fu lton i were
only found on the ffeshwater eels. A total lack of strict
freshwater parasite species ín eels from the GV area
indicate no or only limited travel o f these eels between
fresh- and marine waters.
Myxidium giardi was found in high prevalence (20 to
93%) at all sampling sites but Eimeria anguillae,
Zschokkella spp. and Myxobolus kotlani were found on
rare occasions; only one or two eels ffom each sampling
site were infected. The prevalence o f Chilodonella
hexasticha, Trichodina jadranica and T. fu lton i was not
determined; therefore these data only confirm that these
species exist on eels in the Icelandic ecosystem.
Comparison between sampling sites
The similarity o f the microparasite communities be-
tween the sampling sites is fairly high, 0.29 to 0.75
(Sörensen’s similarity index). Myxidium giardi was
found at all localities and Myxobolus kotlani at all sites
except VV. One of the Zschokkella spp. was found at
both ST and OL, the other at VV and GV. Considering
the similarity indices, the microparasite fauna seems to
be similar both in/on freshwater and marine eels as well
as in/on eels from different freshwater localities. Con-
siderable between-sites difference occurred in the
helminth composition at the freshwater sites. They all
have one species in common, Diplostomum sp., the only
helminth species found at more than one sampling site.
Although the values o f SW diversity and evenness indi-
ces, as well as dominance values, are similar in eels at
sites VV and ST, the total helminth species composition
is quite different. The nematode Raphidascaris acus
(prevalence: 43.3%) and the cestode Proteocephalus
macrocephalus (16.6%) are common in eels from ST
but are not found in the W eels. Similarly, the cestode
Bothriocephalus claviceps (26.6%) and the larval stages
o f the nematode Eustrongylides sp. (13.3%) are quite
common in W but totally absent in ST eels. This is
interesting since both sampling sites are small shallow
and relatively fertile lakes, harbouring the same species
o f fishes, i.e. brown trout, arctic char, three-spined
stickleback and eels. Differences in the composition of
the fish fauna o f these sites could, however, elucidate
these differences to some extent. Brown trout is the
dominant fish species at ST but arctic char at W . Trout
is thought to play a part in the life cycle o f Raphidas-
caris acus, both as a final host and an intermediate or a
paratenic host (Moravec 1994). The existence o f this
helminth species in ST eels could be partly due to how
common brown trout is in the lake. Moravec (1985)
reported that B. claviceps was more frequently found in
smaller eels due to differences in their diet with size.
The eels from VV were considerably smaller than those
from ST. Stefánsson (2000) studied the diet o f eels in
VV and found the tendency for smaller eels to eat pro-
portionally more o f small crustaceans, which are vital in
the life cycle o f B. claviceps (see Moravec 1985). Infor-
mation on the invertebrate fauna o f the lakes is however
145
Table 7. The diversity chavacteristics of the intestinai infracommunity of heiminths from Icelandic waters (helminths iti stomach included) and sevcral other freshwater and saline lo-
calities in Europe.
Freshwater M arine or brackish
tceland UK Germany Ireland Portugal lceland ltaly
Reference Present study Kennedy
1993
Kennedy
1997
Sures
c la l. 1999
Sures and
Streit
2001
Kennedy and
M oriarty
2 00 2
Saraiva et al.2005 Present
study
Kemtedy et.al. 1997 Di Cave et al.
2001
Locality VV ST OL
C lyst O tter
1979-92 1985-96
(m in-m ax) (min-max)
LA RLI 'iVorms Alb
Shannon
1983-2001
(m in-m ax)
Trovela Covo Este Sousa GV Burano Fogliano M onaci Caprolace Comaccio Figeri Acquatina
NO. OF EELS 30 30 15 459 216 61 60 35 19 309 55 79 47 93 20 28 20 44 38 42 33 21
(27-100) (10-43) (11-25)
NO. OF HOLMINÍTHS
X 1.53 1.93 0 1.041 0.771 17.8 15.0 4.7 9.1 16.851 0.95 0.91 0.72 2.48 90.90 10.0 8.4 9.9 2.6 45.9 63.2 10.1
(0 - 10.2 ) (0-7 .0) (2.3-79 .1)
SD 4.68 3.93 0 - 37.2 23.9 18.9 21.2 - 1.52 3.34 0.55 7.31 119.26 11.4 12.2 18.8 3.9 59.9 76.6 27.8
NO. OF HELMINTH SI‘P. (ALL EELS)
X 0.27 0.60 0 0 .6 7 1 0 .511 0.6 0.9 0.3 1.3 1.151 0.49 0.33 0.32 0.57 1.85 1.14 1.25 0.95 0.60 2.2 1.8 0 .8
(0 -1 .44 ) (0-2 .23) (0 .7 -1 .7 )
SD 0.45 0.67 0 - - 0 .8 0.7 0.6 1.5 - 0.63 0.55 0.56 0.70 1.09 0.72 0.85 0.80 0.82 0.8 0.9 0 .8
ntax. 1 2 0 2 1 2 1 3 3 2 5 3 1 2 2 2 4 4 3 3 3 3 4 4 3
(0 -4 ) (0 -5 ) (1 -3 )
NO. OF HOLMINTH SPP. (INF. EEI.•s)
X 1.00 1.20 0 - - 1.4 1.3 1.3 2.2 - - - - - 1.95 1.28 1.56 1.39 1.37 2.2 1.9 1.2
SD 0 0.41 0 - - 0.6 0.5 0.5 1.3 _ - - - _ 1.03 0.61 0.63 0.56 0.59 0.8 0.9 0 .6
B I (ALL EEt.S)
— 0 0.03 0 0.0361 0.0091 0.06 0.07 0.02 0.22 0 .0611 0.035 0.013 0.012 0.024 0.17 0.064 0.167 0.088 0.074 0.37 0.22 0.03
X (0-0 .158) (0-0 .415) (0-0 .162)
SD 0 0 .10 0 _ _ 0.17 0.17 0.08 0.33 - 0.111 0.068 0.076 0.096 0.26 0.181 0.221 0.179 0.180 0.29 0.28 0 .10
max. 0 0.37 0 0 .3661 0.3461 0.66 0.67 0.37 1.02 0 .3 9 9 1 0.461 0.366 0.398 0.549 0.84 0.755 0.557 0.592 0.730 1.08 1.07 0.47
(0-0 .986) (0-0 .957) 0 -0 .922
BI (INF. EELS)
X 0 0.06 0 0 .3 4 8 1 0.43 0.4 0 .10 0.38 0 .227 ' 0.087 0.046 0.057 0.050 0.18 0.499 0.418 0.383 0.142 0.46 0.39 0.29
(0-0 .514) (0-0 .635)
SD 0 0.13 0 - - 0.17 0.19 0.17 0.36 - 0.165 0.125 0.140 0.134 0.26 0.293 0.102 0.172 0.142 0.26 0.26 0.25
% o f eels with 100 90 100 9 2 1 9 7 .1 1 85.3 83.4 95 602 7 3 1 91 96 95 94 45 82 60 75 84 19 42 90
0 or 1 species (61-100) (45.4-100) (36-100)
'Long-term study; median value calculated from data given by authors. 2Values estimated from a histogram given by authors.
146
Kristmundsson, Helgason: Parasites of Icelandic eels
scarce. A difference in the sampling time might also be
an affecting factor. The complete absence o f intestinal
helminths at locality OL is interesting but hard to ex-
plain. The difference in the intestinal infracommunity
between the marine and the freshwater sites in Iceland is
considerable. The total number o f helminths and the
helminth species per eel is much higher in the marine
eels than in the freshwater ones. This is because most o f
the marine eel’s parasites are generalists. Many o f these
are frequently found in distínct fish species common in
Icelandic marine waters, such as Atlantic cod Gadus
morhua, saithe Pollachius virens, dab Limanda limanda
and anglerfish Lophius piscatorius (Koie 1983, 1993,
2000, Eydal and Ólafsdóttir 2002-2003, Eydal et al.
2005).
Comparison with other parasite communities in
Europe
The microparasite fauna observed in this study re-
sembles the one found in similar studies on the Euro-
pean eel. The two strict eel specific microparasites
found in our study, Myxidium giardi and Eimeria an-
guillae, are widespread parasites o f the European eel
(Copland 1981, Orecchia et al. 1987, Koie 1988,
Saraiva and Chubb 1989, Benajiba et al. 1994, Molnár
and Székely 1995, Sures et al. 1999, Outeiral et al.
2002, Aguilar et al. 2005, Maíllo et al. 2005) and Tri-
chodina jadranica, T. fu ltoni and Myxobolus kotlani
have also previously been reported from eels
(Markiewicz and Migala 1980, Molnár et al. 1986, Ly-
holt and Buchmann 1995, Madsen et al. 2000, Aguílar
et al. 2005). On the other hand, based on both measures
o f morphological features and sites o f infection, neither
of the Zschokkella species found seems to be Z. stet-
tinensis, the only reported species in the European eel
(Molnár et al. 1986). An obvious difference between our
study and previous ones is the total lack o f the flagellate
Trypanosoma granulosum in our study, but this species
has been found in most other similar studies in very
high prevalence (Orecchia et al. 1987, Koie 1988,
Saraiva and Chubb 1989, Mo and Sterud 1998, Sures et
al. 1999, Sures and Streit 2001, Outeiral et al. 2002,
Aguilar et al. 2005).
Compared to previous studies, the parasite communi-
ties o f freshwater eels in Iceland are, in general, species-
poorer, less diverse and have higher dominance o f a
single species (Tables 8, 9; Figs. 3, 4). The median
number o f intestínal helminths calculated from the stud-
íes selected for comparison is four species compared to
zero, one and two, respectively, for the three freshwater
localities OL, VV and ST in Iceland. The richest intesti-
nal helminth community, 12 species, was observed in
Lake Esrum Denmark and the lowest (no parasites
found) in 1984 in River Clyst and in 1988 in River Otter
as well as locality OL in Iceland. The richness is com-
parable at ST and W with Lake Balaton in ITungary,
Ooigem and Kerkhove in Belgium and at Markermeer
and S-Ijsselmeer in the Netherlands (Table 8, Fig. 3a).
Considering the total number o f macroparasites found,
Lake Esrum has the richest community, 23 species and
the median values are 7 for previous studies and 1, 3
and 3, respectively, for the Icelandic localities OL, ST
and VV (Table 8, Fig. 3b). Looking at diversity indices
(SW and SI) the values for the Icelandic localities are
considerably lower than the median value for other stud-
ies (Table 8, Fig. 3c, d). The BP dominance index and
the percentage o f eels with 0/1 species, is noticeably
higher for the Icelandic localities than in most other
studies (Table 8, Fig. 3e, f). In the previous studies, the
dominant intestinal species is most often an acantho-
cephalan species but nematode and cestode species are,
however, also quite often dominant. Digenean species
are, however, rarely dominating eel parasite communi-
ties in freshwater. In Iceland the dominant species in
freshwater eels is the nematode Raphidascaris acus and
the cestode Bothriocephalus claviceps, both common
parasites o f eels in Europe and dominant in several stud-
ies (Table 8). All species found at the Icelandic locali-
ties are frequently found in other studies but many of
the most prevalent ones found in previous studies, such
as the monogeneans Pseudodactyiogyrus anguillae and
P. bini (e.g. Koie 1988, Saraiva and Chubb 1989, Mo
and Sterud 1998, Borgsteede et al. 1999), the acantho-
cephalans Acanthocephalus anguillae, A. lucii and
Pomphorhynchus laevis (e.g. Conneely and McCarthy
1986, Koie 1988, Sures et al. 1999, Kennedy and
Moriarty 2002, Norton et al. 2003), the nematodes
Paraquimperia tenerrima, Camallanus lacustris (e.g.
Moravec 1985, Conneely and McCarthy 1986, Koie
1988, Mo and Sterud 1998, Kennedy 2001) and Anguil-
licoia crassus (e.g. Koie 1988, Molnár et al. 1991, Ken-
nedy et al. 1997, Sures et al. 1999) and the crustacean
Ergasilus gibbus (e.g. Conneely and McCarthy 1986,
Koie 1988, Borgsteede et al. 1999, Aguilar et al. 2005),
are absent in this study.
Some differences emerged at the intestinal infra-
community level comparing eels from Iceland to other
similar studies (Table 7). The number o f helminths at
localities ST and VV are much lower than observed in
eels from the River Rhine and River Shannon but fairly
similar to the numbers observed by Saraiva et al. (2005)
in Portugal. Results from River Clyst and River Otter
vary greatly between sampling years, sometimes being
much higher than at ST and W but sometimes lower,
the median value being somewhat lower. O f the locali-
ties in Iceland only ST eels harbour more than one
helminth species and consequently the BI exceeds zero.
Including all eels, the mean BI is low at ST and compa-
rable to most o f the studies considered here. It is al-
though to some extent lower than at Worms in River
Rhine and in some years in River Clyst and River Otter.
Including only infected eels, the BI at ST is lower than
observed elsewhere except for the Portuguese localities,
where the values are comparable (Table 7).
147
Table 8. Comparison of intestinal helminth component communities between the Icelandic freshwater sampling sites and numer-
ous freshwater localities in Europe.
Country Reference Locality
No. o f
intest. sp.
(m in-
max)
Total
no. o f
sp.
SW index
(m in-m ax)
SI i/D
(m in-m ax)
BP dom.
(min—max)
Dom inant
sp.
No. o f
eels
(min—max)
0 or 1 sp.
(%)
(m in-m ax)
Present study OL 0 1 0.00 - 0 15 100
íceland ST 2 3 0.33 1.23 0.90 Ra 30 90
VV 1 3 0.00 1.00 1.00 Bc 30 100
K aie 19881 Lake Esrum 12 23 2 .20 7.73 0.19 Da/Cl 120 nd
Denmark Arreso 6 11 1.21 2.31 0.63 Aa 30 nd
Sjælso 4 12 1.13 2.67 0.50 Pm nd
Norway
M o and
Sterud
1998
Aarungen
Glomma
4
4
7
6 - - - -
3
13 -
Sures e t al.2 ‘LA ’ 6 8 0.35 1.17 0.92 Pa 61 85.3
Gerraany
1999 ‘R H ’ 4 5 0.41 1.23 0.90 Pa 60 83.4
Sures and W orms 4 6 0.42 1.23 0.9 Pa 35 95
Streit 2001 Alb 6 8 1.11 2.12 0.67 Pa 19 60
Schabuss Illmitz 54 0 .884 1.704 0.764
Al/Aa
424 61.5“
A ustria
e t al. 20053 1994-2001 (2 -5 ) (0.37-1.44) (1.11-4.02) (0 .30-0.95) (19-156) (41.5-100)
South 54 0.504 1.364 0.854 Aa/Bc 296 78.34
1996-2001 (2 -5 ) (0 .21 - 0 .8 8 ) (1 .06-1.72) (0 .75-0.97) (5-180) (55.9-86.7)
Kennedy Clyst 34 * 0.714 1.604 0.744 A c / 459 92 '
1993 1981-1992 (0-9) (0-1.04) (1.00-2.67) (0.50-0.88) Bc/Pt (27-100) (61-100)
UK
Kennedy
1997
Otter
1985-1996
44
(0- 8 )
* 1.044
(0-1 .83)
2.384
(1.00-5.55)
0.514
(0 .25-1)
Bc/Pm /Pt/Si
216
(10-43)
9 7 .14
(11.4-100)
N orton4 Test 8 * 1.33 2.72 0.54 Et 50 38
et al. 2003 Thames 8 * 1.46 3.45 0.34 Ng 32 44
Ireland
Kennedy and
M oriarty
2002
C onneeiy and
Shannon
1983-2001
Abbert
4"
( 1- 6)
5
*
7
0 .124
(0.04-0.30)
1.30
1.044
(1.01-1.15)
3.30
0.984
(0 .94-1)
0.4
A l
Ra
309
(11-25)
33
W
(36-100)
nd
M cCarthy Drimneen 7 10 1.16 2.59 0.49 Pl 49 nd
1986' Corrib 9 12 0.52 1.05 0.89 Sb 39 nd
Saraiva e t al. Trovela 4 * 1.30 3.39 0.42 P t 55 91
2005 Covo 3 * 0.69 1.83 0.67 Ct 79 96
Portugal
Este 3 * 0.35 1.20 0.91 Ct 47 95
Sousa 4 * 1.01 2.44 0.52 Ra 93 94
Saraiva and
C h u b b 1989
Este 4 6 n.d. n.d. n.d. Pt7 129 nd
Spain
A guilar
e t al. 2005'
U lla R iver
Tea River
6
7
10
10
1.37
1.52
3.42
4.15
0.39
0.31
Si
Pt
323
200
nd
nd
Seyda 1973' Stotczcyn 6 7 1.28 2.63 0.57 A a 20 nd
Poland Trzebiez 5 8 0.91 1.97 0.67 Bc 33 nd
Dabie 8 10 1.38 2.92 0.53 Aa 30 nd
Schabuss Ooigem 2 36 0.12 1.06 0.97 Pm 30 nd
Belgium
et al. 19972 Kerkhove 2 36 0.12 1.05 0.97 Pm 16 nd
Bavikhove 3 46 0.88 2.08 0.63 A l 31 nd
St. Baafs. 3 40 0.40 1.24 0.90 Aa 30 nd
M olnár and
Hungary Székely
1995*
L. Balaton 2 7 0.68 1.95 0.58 Bc 82 nd
Nether-
lands
Borgsteede et
al. 1999'
N -ljsselm .3
S-Ijsselm .5
3
2
5
4
0.08
0 .02
1.03
1.005
0.99
0.998
Ac
Ac
72
92
nd
nd
M arkerm .5 1 2 0 1.00 1 Ac 99 nd
Forraer M oravec
1 o s s Lake M ácha 7 11 n.d. n.d. n.d. Bc 132 nd
'Values calculated fforn data given by authors; 2Values recalculated from data given by authors, taking only intestinal helm ínths into count;
■’Values recalculated fforn data given by authors using natural logarithm (ln/logc) instead o f log2; 4Long-term study; m edian value calculated from
data given by authors; 5Data from tw o sam pling times pooled; 6N ot looked for ectoparasites in the study; * Only looked for intestinal helminths in
the study; nd - no data. Parasite species abbreviations: A a - Acanthocephalus anguillae, A c - A. clavula, A l - A. lucii, Bc - Bothriocephalus
claviceps, C l - C am allanus lacustrís, C t - Cucullanus truttae, Da - Daniconema anguillae, E t - Echinorhynchus truttae, N g - N icolla gallica,
Pa - Paratenuisentis ambiguus, P l - Pom phorhvnchus laevis, Prn - Proteocephaíus macrocephalus, P t - Paraquim peria tenerrima, Ra - Raphi-
dascaris acus, Sb - Sphaerostom a bramae, S i - Spinitectus inermis.
148
Kristmundsson, Helgason: Parasites of Icelandic eels
Table 9. Comparison of intestinal helminth component communities between the Icelandic marine sampling site and other brack-
ish and marine localities in Europe.
Country Reference
Locality
(Salinity)
No. o f
intest. sp.
(m in-m ax)
Total
no. o f sp.
SW
index
SI
1/D
BP
dom inance
Dom inant
sp.
No. o f
eels
O or 1
sp- (%)
Iceland Present study GV (33%o) 6 7 0.12 1.04 0.98 D i 20 45
Koie U lf Sund (4—8%o) 9 18 1.15 2 .20 0.64 D i 60 nd
Denmark
1988' Ringk. Fjord (10%o)
fsefjord (15-20%«)
W. K attesat (30-34%o)
4
11
6
10
19
9
1.02
0.87
1.16
2.31
1.93
2.47
0.60
0.70
0.59
Pni
D i
D i
24
80
36
nd
nd
nd
Kennedy Bun-ano ( 10-40%o) 6 8 0.97 1.93 0.71 D i 28 82
e ta l. 19972 Fogliano (28-48%o) 3 4 1.06 2.79 0.43 Bp 20 60
M onaci (17-39%») 3 4 1.00 2.58 0.43 D i 44 75
Italy Caprolace (32-44%o)
Valle Figheri (15-35%o)
2
5
3
11
0.86
0.83
1.97
2.03
0.67
0.60
D i
D i
38
33
84
42
Di Cave Coraacchio (23-37%o) 4 7 0.81 1.96 0.65 D i 42 19
et aí. 20 Ö12 Acquatina (30-42%o) 4 6 0.08 1.10 0.95 Bp 21 90
Netherlands
Borgstcede
et al. 1999' Volkerak3 (brackish)4
3 5 0.65 2.35 0.58 A c 98 nd
Outeiral et al. Aurosa (>30%o) 13 18 1.67 4.36 0.37 D i 477 nd
2 0 0 1 , 2 0 0 2 ’ Ferrol (>30%o) 13 17 0.71 1.68 0.73 D i 479 nd
Spain M aíllo et al.
2GÖ52
Encanyissada (3-30%o)
Tancada (8—36%o)
3
1
6
3
0.42
0
1.26
1.00
0.89
1
D i
Di
141
39
nd
nd
Canal Vell (8-30%«) 3 5 0.92 2.24 0.59 Di 36 nd
France
(Corsica)
Tem engo
e ta l. 2005’
U rbino pond (>30%o) 4 5 0.38 1.21 0.91 Di 31 nd
:Values calculated from data given by authors; 2Values recalculated from data given by authors, taking only intestinal helm inths into count; ';Daca
from two sam pling tim es pooled; "'Salinity not given; nd - no data. Parasite species abbreviations: A c - Acanthocephalus clavula, Bp - Bucepha-
lus polym orphus, D i - D eropristis inflata, Pm — Proteocephalus macrocephalus.
Compared to the number of studies of freshwater
eels, relatively few have dealt with parasites o f eels
ífom brackish and full salinity environment (e.g. Koie
1988, Kennedy et al. 1997, Borgsteede et al. 1999, Di
Cave et al. 2001). The number o f intestinal helminth
species at GV (6) in Iceland is either comparable or
higher (Table 9, Fig. 4a) than that observed ín most of
those studies (median value 4 species). Three localities
stand out regarding number o f intestinal helminths, i.e.
the Danish localities Isefjord (11 species) and U lf Sund
(9 species) and from the estuaries in North-West Spain,
Aurosa and Ferrol (Table 9), both with 13 species. Fluc-
tuations in salinity exist at U lf Sund (15 to 20%o) and
Isefjord (4 to 8%o) and consequently the eels from these
iocalities harbour a number o f freshwater species, unlike
the eels ffom GV. Although salinity at Aurosa and
Ferrol exceeded 30%o, these eels seem to travel to
freshwater or low salinity areas resulting in a number o f
ffeshwater species. When the total numbers o f macro-
parasites are compared, 7 are found at GV compared to
3 to 19 at the other localities, with a median value o f 6.5
(Table 9, Fig. 4b). The diversity at the Icelandic locality
(GV) is, on the other hand, generally lower than at the
other localities, with a SW value o f 0.12 and SI value of
1.04, compared to a medían value at the other localities
(SW: 0.87, SI: 2.03); only Acquatina in Italian waters
and Tancada in Spanish waters have lower diversity
(Table 8, Fig. 4c, d). This low diversity reflects GV’s
high BP-dominance, the digenean species Deropristis
inflata being 98% (BP = 0.98) o f all intestinal hel-
minths. Comparable BP dominance figures for the other
localities range ffom 0.37 to 1 with a median value of
0.65 (Table 8, Fig. 4e). The eel-specific trematode D.
inflata is the dominant species at 15 o f 19 localities con-
sidered here, the trematode Bucephalus polymorphus at
2 localities and the ffeshwater cestode Proteocephalus
macrocephalus at U lf Sund, a low-saiine (4 to 8%o) lo-
cality in Danish waters (Table 9, Fig. 4f). All compared
studies share one helminth species, i.e. D. inflata, which
is without doubt the most common parasite o f eels in
saline waters. Apart from Koie’s study (1988), the spe-
cies composition o f the GV’s eels is quite different ffom
other studies made. As in Koie’s (1988) study, most o f
the species found are generalists which commonly para-
sitize many different families o f fishes, such as Atlantic
cod, Gadus morhua (Koie 1993, 2000, Eydal et al.
2005), which is a very common species in Icelandic and
Danish waters. The differences in the aquatic fauna at
these localities most likely explain these dissimilarities.
Comparing the intestinal infracommunity o f GV eels
to other studies (Kennedy et al. 1997, Di Cave et. al.
2001), the mean number o f species is comparable. On
the other hand, the Brillouin’s index is much lower but
the mean number o f helminths per eel considerably
higher (Table 7).
In summary, the parasite communities o f freshwater
eels in Iceland are in general species-poorer, less di-
verse and have higher BP dominance than other eel
communities in Europe. Marine eels, on the other hand
have comparable species richness, are less diverse and,
149
12
11
«101-
~ 9 u aF
Q. 8[
I 7RJ f
1 6
S 5t
I t ?o 3J
° 22
1
0
E 6
X cc> o-D
-- 4
o 3
tno.§ 2
co
1
X
ST (2)
VV(1) —
OL(0) (
■ ST f 1.231
W{1.00J-
Fig. 3. Distribution of diversity characteristics from numerous European freshwater eel communities (based on data from Table
8). For comparison, values ffom the Iceiandic sampling sites are also shown. a - number of intestinal specíes; b - total number of
species; c - Shannon Wiener diversity index; d - Simpson’s diversity index; e - Berger Parker dominance index; f - proportion
(%) of eels parasitized with one or two helminths. Note: the mean value is marked with an X.
with a high BP dominance. Similar to most previous
studies, there is a total replacement of ffeshwater
macroparasite species by marine ones in saline waters.
But unlike research abroad in which species richness
generally decreases with higher salinity, the marine eels
in Iceland have considerably higher species richness
than the freshwater ones. This difference is more due to
few species in freshwater eels rather than high numbers
in the marine ones.
As mentioned before, some parasite species, e.g. the
flagellate Trypanosoma granulosum, the monogenean
Pseudodactylogyrus spp., the swim-bladder nematode
Anguillicola crassus, acanthocephalan species, the
nematodes Paraquimperia tenerrima, Camallanus
lacustris and the crustacean Ergasilus gibbus, which
frequently parasitize ffeshwater eels in Europe, are not
found ín/on the Icelandic eels. Why is this? The biodi-
versity o f a certain ecosystem depends on both biotic
(related to living things) and abiotic factors (related to
nonliving things) such as climate, minerals and light
(Buchmann and Bresciani 2001), as well as on the op-
portunity for new species to colonize that ecosystem.
The overall Icelandic freshwater vertebrate and non-
parasitic invertebrate fauna is species-poor, compared to
other European countries. This is clearly o f great impor-
tance. Commonly parasites need an intermediate host,
most frequently ínvertebrates, to complete their life cy-
cle. Aiso, interaction between físh species is often a
vital part o f a parasites’ life cycle. One fish species is
offen a paratenic or an intermediate host for a parasite
that has a different fish species as a final host. The lack
o f suitable intermediate hosts is therefore, without
doubt, one o f the explanations for few parasites in the
Icelandic eels. Trypanosoma granulosum, for example,
uses the leeches Hemiclepsis marginata and Piscicola
geometra as an intermediate host (Lom and Dyková
1992). These leeches are not a part o f the invertebrate
fauna of Iceland and therefore this parasite cannot be
present. Regarding the acanthocephalans, the isopod
Asellus aquaticus serves as an intermediate host for
Acanthocephalus anguillae and A. lucii (Brown et al.
1986, Williams and Jones 1994) and the amphipods
Gammarus pulex, G. fossarum and G. duebeni celticus
(Irish waters) for Pomphorhynchus laevis (Brown et al.
1986, Williams and Jones 1994). None o f these species
inhabit the Icelandic freshwater system. As a conse-
quence, these acanthocephalans cannot live in Icelandic
freshwater. But why is the Icelandic freshwater fauna so
species poor? The country’s climate at its northem lati-
tude o f 64° to 66°N is rather cold (12 to 13°C mean
temperature in July). However, because o f volcanic ac-
tivity in the country, many Icelandic lakes are rich in
minerals, which create a good basis for the production
o f biotic material and fertile lakes. The northem parts of
Norway and Canada and Alaska which are on simiiar
latitudes as Iceland are, however, much richer in the
vertebrate and invertebrate fauna. Many fish species
which Iive there, e.g. northem pike, Esox lucius
150
Kristmundsson, Helgason: Parasites of Icelandic eels
« F
12l
>11í;io
’ 9 tL
i 9
' f: 5 t: 4-
i 31
2|
oL
GV ÍS)
(a)
■= 3Í-I
5 i£fl o'
cl.
E i
to i
1Í-"
0 L_
(d) j
16Cfl
14o
o
0-12«fl
o 10
ö Q
C O
S 6
£ 4
2
0
1
0.9
x
CJ
t j 0.8 c
ö _ _
0 0.7 c
P3
1 °-6O
2 0.5
œ
0.4
0,3
18
V(7L
(b).
- G V ( 0 .9 8 ) |
(e) í
1.4
1.2
x% 1.0
£ 0.8
05 0.6
0.4
0 .2 -
0
100
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I 80u
a . 70w
S 60
Í 50 5
<fi 40 ©
0 3052
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-G V (0.12) *
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Fig. 4. Distribution of diversity characteristics ffom numerous European eel communities ffom marine and brackish localities
(based on data ffom Table 9). For comparison, values from the Icelandic sampling site are also shown. a - number of intestinal
species; b - total number of species; c - Shannon Wiener diversity index; d - Simpson’s diversity index; e - Berger Parker
dominance index; f - proportion (%) of eels parasitized with one or two helminths. Note: the mean value is marked with an X.
(Crossman 1996), burbot, Lota lota (Cohen et al. 1990),
common carp, Cyprinus carpio carpio (Welcomme
1988, Coad et al. 1995), and grayling, Thymallus thy-
mallus in Norway (Blanc et al. 1971) and Thymallus
arcticus arcticus in Canada (McClanes 1974) and
Alaska (Morrow 1980) do not inhabit Iceland although
abiotic factors, such as temperature, are similar in these
areas. The northem position o f Iceland is therefore not a
suffícient explanation for its poor biodiversity. Most
species o f the present fauna o f Iceland and the northem
part o f Europe and N. America have colonized these
areas during the last 10 thousand years, after the last ice
age. The geographical location o f Iceland has, however,
hampered its eolonisation, whereas the recolonisation of
northem European and N. American areas along rivers
and coastal areas from further south has been much eas-
ier. The only físh species able to colonize Icelandic
freshwater were ana- and catadromic species. The main
reason for poor biodiversity in Icelandic freshwater of
both invertebrates (including parasites) and vertebrates
is most likely the geographical isolation and the short
time span available for their colonisation. For instance,
parasites like Anguillicola crassus and Pseudo-
dactylogyrus bini, which most probably were íntroduced
to Europe with imported eels from Asia, have due to
this isolation not spread to Iceland but also because no
import o f live eels has been permitted. Low winter tem-
perature o f most Icelandic freshwater systems would
seriously hamper a successful development o f A. cras-
sus (Knopf et al. 1998) except in few discrete areas af-
fected by geothermal activity.
Many authors, studying eel parasites, have analysed
their parasíte community characteristics, such as diver-
sity, evenness, species richness and species dominance.
This kind o f analysis is very interesting for comparison
with other similar studies. When comparing data ob-
served in different studies one must be sure that the val-
ues selected for comparison really are comparable. Re-
garding the analysis o f eel parasite communities, au-
thors are evidently using different logarithms for calcu-
lations o f their data, natural logarithm (ln) (e.g. Aguilar
et al. 2005, Saraiva et al. 2005), or logarithm with log
base two (logí) (e.g. Norton et al. 2003, Schabuss et al.
2005). Calculations using these two different logarithms
give considerably different values and hence comparing
diversity characteristícs data derived from calculations
with different logarithms calls for recalculations or else
the comparison is meaningless. For example, the values
o f the SW índex ealculated from a certain data give val-
ues o f 0.12 and 2.20 using natural logarithm but 0.05
and 0.95 using logi, respectively. To avoid further con-
fusion we suggest that the more commonly used natural
logarithm should be applied in future studies.
Acknowledgement. We acknowledge a grant awarded by the
Icelandic Research Council.
151
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K e n n e d y C .R . 1993: T h e dynam ics o f in testinal he lm in th com -
m un ities in ee ls A n g u illa anguilia in a sm all stream : long -
te n n changes in richness and structure. P a ras ito lo g y 107: 7 1 -
78.
KENNEDY C .R . 1997: L ong-te rm and seasonal changes in com po-
s ition and richness o f in testinal helm in th com m unities in eels
A n g u illa a n gu illa o f an iso la ted E nglish river. F o lia Parasito l.
44: 2 6 7 -2 7 3 .
KENNEDY C .R . 2001: M etapopu la tion and com m unity dynam ics
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KENNEDY C .R ., D l C a v e D „ BERRILLI F „ ORECCHIA P. 1997:
C o m p o sitio n and s truc tu re o f helm in th com m unities in eels
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KENNEDY C .R ., MORIARTY C. 2002: L ong-te rm s tab ility in the
richness and stru c tu re o f he lm in th com m unities in eels, A n -
g u illa angu illa , in L ough D erg , R iver Shannon , Ireland . J.
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o f low w a te r tem pera tu re on the developm ent o f A n g u illico la
cra ssu s in the fm a l h o s t A n g u illa anguilla . D is. A quat. O rg.
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(O ste ich thyes, P leu ronectidae) from D anish an d ad jacen t w a-
ters, w ith spec ia l re fe rence to the ir life cycle. O p h e lia 22:
2 0 1 -2 2 8 .
K 0IE M . 1988: P arasites in E u ropean eel A n g u illa angu illa (L .)
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2 1 7 -2 4 3 .
K 0IE M . 2000: M etazoan p arasites o f te leost fishes from A tlan tic
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b ro w n tro u t (Sa lm o tru ttá ) and a rctic char (Sa lve linus a lp inus)
in tw o Ice land ic lakes - P relim inary resu lts. B ull. Scand. Soc.
P arasito l. 1 2 -1 3 : 43.
LOM J„ D y k o v á I. 1992: P ro tozoan Parasites o f F ishes. E lsev ier
S c ience P ub lishers B .V ., A m sterdam , 315 pp.
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T richodina sp. (C iliophora: P eritrich ida) in eel A n g u illa an-
152
Kristmundsson, Helgason: Parasites of Icelandic eels
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P.AGGI L. 1987: P a ra s ito lo g ica l study o f a popu la tion o f T iber
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MARTín M .L . 2001: D ig en ean p arasites o f the E uropean eel
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92.
Received 19 M ay 2006
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Accepted 14 D ecem ber 2006
153
Bændabladió | Fimmtudagur 8. október 2015
Sigurjón Vídalín Guömundsson á Stokkseyri, með góðan feng af iðandi á! í gildru þann 25. september síðastlidinn. Á innfelldu myndinni má sjá álagildruna í laeknum. North Atlantic ehf. I sam-
starfi við Sigurjón býður mönnum veiðiráðgjöf sem fólagið greiðir ef bændur hafa búnað og land sem hægt er nýta en kunna ekki til verka. Sigurjón kortleggur ákjósanleg veiðisvæði og sýnir
hverníg á að leggja gíldrur. Myndir I Helena Sif Zópfioníasdóttir.
Víðir Ísfeíd Ingþórsson hjá North Atlantic ehf. á Ísafírði:
Hvetur bændur til álaveiða
- fyrirtæ kið kaupir ál ti! v innslu og er hann seldur ferskur á Japansm arkað
Slægður áll til útflutnings hjá North Atlantic ehf. á ísafirði.
Fisksölufyrirtcekið North Atlantic
chf. á ísafiriM hefur stundaðvlnnslu
og útílutning á ái tii Japans. Atl
þykir herramannsmarur og er
oróinn mjiig eftirsóttur en fram-
buðiö er m jiig takmnrkað.
VicSir Isfeld Ingþórsson hjá North
Ariantic ehf. segir að állinn sé vcrk-
efni sem hófst hjá fyrirtækinu í fyrra
með þreifíngum á markaði í Japan.
„Við höfum sent út tilrauna-
sendingar við góðar undirtektir. 1
vetur veröur stærri állinn revktur og
seldur innanlands fyrir jólamarkaó-
inn. Islenski dllinn vex hægar en áll
annars staðar og eru vetðisvacði því
viðkvaem fyrir ofveiði. Þess vegna
leggjum vid áherslu á skynsamlega
nýringu á stofnum sem hér er að
ftnna," scgir Víðir.
Hann segist telja að állinn sé van-
nýtt auðlind, en þessa físktegund er
að fínna viða um land, en þó sist
á Noróurlandi og á Austfjörðmn.
Helstn veiðisvæðin ent í vatnasvæð-
um á láglendi sunnan- og vestanlands
og talsvert við Breidaíjörð.
SHlróítar vcióur en ýmsar
hugmyudir
Ýmsar hugmyndir hafa komió upp
i gegnum tiðina um stórtækar ála-
veiðar seni minna hefur þó orðiö
lir. Veiðar á ái voru þó stundaðar á
íslandi t einhverjum mæli frá 1960 til
1964 og þá aðallega i giidrur. Einnig
er hægt að veiða ál í sjó og þá kemur
fyrir aft stangveiðimenn fái ál, cink-
um cfbcitt c rá krók.
Árið 1995 var Álatéíagið hf.
stolhað og var markmiðið að heíja
álaveiðar og eldi sem skila átti 200
tonna framleiðslu á ári. Fékk félag-
ið m.a. sryrk fra acvinnumálanefnd
Reykjavikurborgar það sama haust
en litið hcvrðist þó af ÍTckar: ftam-
gangi málsins. Félagið fékk virðis-
aukaskattsnúmer 1997 sem var siðan
lokað 1998. í grein í Morgunblaöinu
Viðir isfold Ingþórsson.
við stofnun fyrirtækisins var viðtal
við Guðmund Þóroddson, formann
félagsins. Þar kom fram að ála-
eldi í heiminum á þeim tíma hafi
numið um 200.0(M) tonnum. Þar af
hafi um 10-15 þúsund tonn farið á
Evrópuinarkaó og um 1 >S0 þúsund
toun á Japansmarkað. Einnig korn
fram aö ktlóverð á reyktum ál á flug-
vellinum í Kaupmaunahöfn væru um
3 .000 krónur.
Eftirsótt neysluvuru
Áll cr vtða veiddur erlendis þar sem
hann er eftirsótt neysluvara og selst
á háu verði. Framboð á ál hefur
minnkað mjög og er taliö að áll sem
nær ströndum Evrópu hafi fækkað um
90% fiá 1070. Er talið að skýringar sc
m.a. aö leita í breyttu hiiastigi sjávar,
brcvtinga á vatnasvæöum í Evrópu
vegna mannvirkjageröar og vegna
raengunar. Líklegt er talíö að áll kunm
að leita í rikari inæli til Íslands vegna
hlýnunar sjávar.
Geeti ordit) úguif húbótfyrir htemlur
Víðir Isfeid lugþórsson hjá North
Atlantic scgír að álaveiði geii verið
ágæt búbót fyrir bændur og land-
eigendur. Vcrkefnið sé þó enn á úl-
niunastigi hjá fyrirtækinu en óskað hafi
vcriö effir fleiri samstarfsaðilum og
liefur hann reynt að virkja fólk til ála-
veiða. í því augnamiðí auglýsti haiui i
Bændablaðinu i voreftir veiöimönn-
um til að veiða ál iil vinnsíu.
„Okkar markmið ct að koma áia-
veiói á íslandi i góðan lárveg þannig
að hægt sé með reglubuudnum hætti
að nýta auólindina á skynsaman hátt
og skapa verðmæti fyrir þátttakeud-
ur." segir Vióir. Hami segir að þar
sem um þróunarverkefni sé að ræöa,
þá sé enn ekki kominn aimennileg
revnsla á markaðinn. y\llínn séseld-
ur í mismunandi siærðarflokkum og
fítupróscntan skipti lika miklu máli
fyrir kaupendur. Reglulega eru send-
ar út prufusendingar þar sem fítupró-
sentan er mæld i hveijum einasta ál.
Verður þaö gert út þetta ár ti I að fá
yftrsýn yfír árstíðabundna fitupró-
sentu i ál á Islandi. Þrátt fyrir óvissu
um söluverð segist Viðir hafa veriö
að bjóða veiðiraönnum eitt þúsund
krónur fyTÍr kilóið.
Reyndur álaveióimuóur u f
Suóurlandi
Sigurjón Vidalín Guðmundsson á
Stokkseyri, sein er einn fremsti ála-
veiöimaöur á íslandi í dag. gaf sig
fram þegar Viðir augiýsti cftir ála-
veiðimönnum. J-Icfur hann stundað
veiðar á ál, cinkiun í og við Ölfusá.
Hann segiraó Suðurlandið henn vel
til álaveiða sem einkum er veiddur
í gildrur. Hann þekkir vel til álsins
frá unga aidri en hann er læddur <>g
uppaiirtn á Eyrarbakka. Eiginkonan.
Helena S if Zóphoniasdóttir. er
honum líka stundum til aöstoðar viö
álaveiðamar.
Ahuginn á álnum kvikrtaói vió
s/angvciói í O/fusálini
„Hjá m ér vaknaði þe.ssi áhugi á
sinum tima þegar maður var að
veiða á stötig í Olfusánni og veiddi
með beitu og slöng á letingja. Þá var
maður stundum að fá ál og ég fór aö
velia þvi fyrir mcr hvort hann væn
hér i einhveiju magni. Ég hafði þá
einhvcrja hugmyud um að þetta væri
trekar verómætur og eftirsóttur físk-
ur. Framhaldið kom svo skemtntilcga
á óvart. Oftast hef ég þó vcrið eiim
að veiða þetta, en einstaka sinnum
incð öónnn. í Ölfúsinu hefur maóur
stundum hitt á mjög góð ár.
Állinn gengur upp ölfusána og
upp i vatnasvæóin í Flóanuin. Hann
gengur upp í flestar sprænur sem
ganga til sjávar. Maóur hefúr heyrt
Bænd?rilaðið | Fimmtudagur 8. október 2015
All cr ekki ólíkur snák eóa slöngu og er afar lífseigur.
Grillaður áll, glæsilega framreiddur á matardiskí í Japan.
at'því aíl hann t'an lika upp i Þjörsána
þóit ég hafi aldici vcitt á því svæói.
Ég hef vcriö mest i Róanum og
Ölfusinu."
Ahugaverti fisktegund
Lífshlaup álsins, þcssa sérkennilcga
fisks, hcfst i Sargossa-hafi i rúmlega
4.000 kilómetra fjarkcgð frá íslandi.
Áll cr afar lifeeigur. Þótt það fjari
undan honutn við ströndina lifir hann
af á þurru landi þar til flæðir að nýju.
Þá scgir Sigiujón aö hann skriói auó-
vcldlcga milli vatnasvæóa og um
llæóicngjar og gcti vcriö klnkku-
stundum saman á þurru landi án þcss
að vcróa mcint of. Álar fcröast cinnig
um á þurru landi og skriöa jafnvel
upp klcita til aö snciða hjá fossum.
Sigurjón scgir aö vciðin hafi vcrið
ágæt sum árin. en minna þcss á milli.
..Það cr þannig mcð álinn að
vciðin cr sveiílukcnnd. Ég sctti
mig í samband við Víöi í vor þcgar
hann auglýsti cf’tir vciðímonnum i
Bcendablaöinu og sctti þá út nokkrar
gildrur til aö kanna hvort állinn væri
svo sncmma á fcrðinni. Það fcng-
ust cinhvcriir álar cn ckkcn til að
tala um. Þó sýndist rticr að svona
könnun sncmma að vori gcri gclið
visbcndingar um ál á svrcðinti, cn þá
gctur vcrið ágætt að bcita i gildruna,
cnda ckki mikið reti i ánum á þcim
úmo."
All er biriufœlinn og reióist litt
y fir hásumunó
,.Y fir bjanasta tima sumarsins dcttur
veiði alvcg niöur. enda állinn biitu-
t'ælinn og hrcyfir sig þá ckki mikið.
Mcö minnkandi birtu þegar kcmur
frara á haust og hcldur fcr aö kóina,
þá viröist kotna raciri hreyfing á
hann. Sem dæmi var ég meö nokkr-
ar gildrur í hinum ýmsu vötniun í
sumar og var aö kroppa einhver 40
tii 50 kiló samtals yfir limabilió. Oft
og tiðiun var ckkcrt i gildrunum,
enda hefst veiðitiminn ckki af viti
fyrr cn cftir mánaðamói júli-ágúst.
tíesti tirainn er i september og Iram
i október. Siöasta hálfa mánuðinn
komu aftur á móti 40 kiló í tvær
gildrur.
Á haustin cr eins og állinn fari að
hópc sig saman og hreyfa sig meira.
Þá fer hann jafhlramt aö vcra vció-
anlcgri en á sumrin. Ef maður hugsar
lil þess að bændur haíi áliuga á að
stunda þetra sem aukabúgrcin eða
sem tómsrundagaman, þá er mesta
veiðin á hentugum tíma eftir að
heyðnnum lýkur. Þá þarf ekki aö vitja
um gildrur nema á fimiti til tiu daga
tresti. I flestöllura tilfellum sem aðrar
lisktcgundir koma í gildrurnar þá er
hann sprelllifandi þegar vitjað cr og
litið mál að sleppa honum.“
Alaveióur hemja liku viógang
minksins
Sigurjón segist hata ótta.st talsvcrt
að mmkur sem álpaöist i gildrurnar
myndi rifa þær og tæta. Það hafi hins
vegar aldrci gerst og svo virðist scm
minkurinn drepist strax et'tir aö hann
keinur í gildrumar.
„Þaö má scgja að minkavciðin sé
aukahagur við álaveiöamar og fækk-
ar honum þá við ár og vötn um leið.
Það kemur oft minkur í gildrumar
en hann hetúr aldrei skcmmt hjá mér
gildrur i þau tíu ár sem ég hef stundað
þetta. Þó hef ég fengiö tugi minka
og einu sinni kom ég að gildru meó
finmi dauðum niinkuin.“
Dvelur í íslenskum viitnum og ám
i 10 til 12 ár
ÁJlinn gengur i íslenskar ár sem gler-
áll eftir langt ferðalag t’rá hrygningar-
stöðvuuum i Þanghafinu (Sargasso).
Fljótlcga eftir að hann kemur i ámar
umhreytist hann i þaó scm kallað er
guláll. Álar vaxa um 5-6 sentímetra
á ári. en kjörhiti þeirra til vaxtar er
22-23 ÚC. Aðstæður á íslenskum
vainasvæóum bjóóa sjalduast upp á
slíkan hita svo vaxtarhraðinn verð-
ur hægari og hatrn verður seinna
kynþroska en í ám á meginlandi
E\TÓpu. Þegar áll hefúr náð um 35-
100 scntímetra lengd þá sækir hanu
aílur suður í Þanghafió til að hrygna
og drepst aö lokinni hrygningu aö
taiiö er. Þa er hann búinn aö dvcija í
islcnskum ám og vötnum i 10 rii 12
ár og orðinn 500 til 1.000 grömm
aó þyngd.
..Þaó er cinmitt þcssi niötugöngu-
áli scm maöur vill hclst fá. sem
orðínn er 500 úl 1.000 grömm ad
þymgd." segir Sigurjón.
Hann scgir miklar líkur á að áll-
inn fari aö sækja meira til íslands
mcð hJýnandi sjó. Ekki siöur við
hlýnandi lottslag og hxkkun á hita-
stigi vatnasvæðanna. Hingað bcrst
glcrállinn mcð Golfstraumnum og
ræður það dreifmgu áls um landið.
Því or litiö um ál í kalda sjónum íyrir
Noröuríandi og Norðausturlandi cn
þeim mun meira vcstan- og sunn-
anlands.
Lifscigur nted eindœmum
Að sögn Sigtujóns cr lyginni likast
hvcrsu iífscigur állinn er.
„Ég salta álinn yfirlcilt til að drcpa
hann og læt hann þá liggja i salti i
fjóra tíma. Eftir það cr hægt að gcra
aö honum. en mjög oft eru þcir samt
ckki alvcg dauðir cl’tir |>cssa Ijóra
tima. Ef maöur tekur slíkan ál. sem
icgiö hcfur i »alti í íjóra lil fimm tíma
og cr mcð cinhverju lífsmarki. og
sctur hann í rennandi fcrskí vatu, þá
er cins og ckkert hafí í skorisr. Hann
veróursprclllifandi með það satna."
Rœndur sáu oft
iöandi ál vió cngjaslátt
..Þcgar ég var að bytja i álaveiö-
ínm l'yrir rúmum tiu árum var ég
aö ræöa þctta við nicnn á svæöinu
og hvort þcir vissu um góö vciði-
svæði mcðfram bökkum Ölfusár að
austanverðu. Þá sögöu þcir mcr að
þegar þama var stunduöur engja-
siáttur og þeir að ganga hcim yfír
cngin að dagsverkt loknu. þá fannst
mönnum oít eins og jöröin væri á
hreylingu i rökkrinu Þcgar mcnn
bmgðu Ijósum á Ioft sáu menn oft
ál sem var aö skriöa i áttina aö ánni.
Hann fer þvi létt mcð aö skríða á
niilli vatnasvæða. Þá myndar hann
utan um sig slímhjúp scm ver hann,
en liann getur samt tekiö upp súrefni
i gegnum hann.“
Orðatiltækið aö vera háll scm áll
er dregið a f því að slimið gerir hann
hálan og því erfitt aó hafa hendur
á lionum. I slimlmö álsins er eirur
sem getur reynst vaiasamt. komist
það i opiö sár. Eitrið bronur niður
og veröur skaðlaust þegar álJinn cr
reyktur eöa soömn.
Álar þvkja fmir ttl átu í JCina og
hefur N crðió á glerálutn farið yftr
fnnm þúsund dollara fyrir kíióið í
J-long Kong.
í Kóreu eru álar sagðir stinnandi
fyrir karlmenn scm cru fámir að
linasi. Auk þess cru álar borðaðir
með bestu lyst um alla Evrópu og í
Bandarikjimum.
Sagt er að Hinrik 1. Englands-
konungur hafi ctiö yfir sig af áli og
drcpist og Agústus Róinarkeísari er
sagður hafa átt tjörn fulla a f áliun
scr til ánægju.
I.engsti áli sem mældur hefur
verið hér á landi var 130 semímetr-
ar og vó 6,5 kíló. Fullvaxnir álar
á íslandi verða þó sjaldan lengri
en meui á lengd og fjögur kfló að
þyngd. Hængarcru núnni en lirygnur
og sjaldnast lengri eu 50 sentimcrrar
hér á landi.
Getur skilaó ágœtum tekjum
Sigurjón segir að hjá sér hafi þetta
mest verið tómstundaiðja og áJiuga-
mál i gegnum tiðina. Hatm liafi eiu-
hvað dundaö sér vid aö rcykja ál fyrir
sig og láta tnenn hafa i prufúr. El'
menn vilji aftur a móti fara að stunda
þetta af alvöru, þá se öruggt að hægt
sé að fá ágætis verð fyrír áiinn. Þá
geti dlaveióar hentað bændum mjög
vcL þar sein þær er helst hægt að
stunda eflir aö heyskap lýkur.
.Álaveióar i Evrópu hafa dregist
saman um 90°/;. en eftirspumin er
mikil. Evrópusambandið hefurnán-
ast baunað álaveiöar vegna mimik-
andi stofnstærðar. Þá eru einhver
höft i gangi i Evrópu við innflutn-
ingi á cvrópska „Anguilla anguiila"
álnum. Þaö má hins vegar fiytja inn
lil Evrópu eins mikið og manni
sýnist a f amcrikuáinum „Anguilla
rostrata". cn sú tcgund vcióist eiti-
hvað hér iíka."
Sam kvæm t upplýsingum i
blaðinu Fishcnncn's Voicc hcfur
vciói á ál þó cinnig dalað mikið i
Bandaríkjunum. I rikinu Main hefur
vciðin fallið frá þvi aö vcra mcst
nærri 190 þúsund kilö (190 tonn)
a f fullvöxnum ái árið 1974 i það að
vcra vei undir 2.000 kílóum árið
2011 . Á austursirönd öandaríkjanna
hafa mcnn mikið vcitt af örsmáum
gíerál i fínnðin net. Hann helursiðan
verið alinn upp i markaösslærö fyrir
Japansmarkað á 12 til IX manuö-
um. Líklegt er talið aö mikil veiói
á örsmáum glerál vaidi mestu um
versnandi afkomu stofnsins scm og
mengun.
Hlýnandi lofislu}' gtcti aukiö
álagengd til Is/ands
Sigurjón scgir miklar iikur á að a51-
inn tári aö sækja mcira til ísiands
með hlýnandi sjó. Ekki síður við
hlýnandi ioftslag og liækkun á hita-
siigi vatnasvæöanna. Hingað berst
glcrállinn mcð Golfstraumnum og
ræður það drcifingu áls um landið.
Þvi cr iitiö um ái i kalda sjónum fyrir
Noröurlandi og Norö-Austurlandi en
þeim mim meira vestan- og sunn-
anlands.
„Það er scrlcga míkil cftii-spum
cflir ái í Asiu og einkum i Japan.
Állinn scm cg cr að vciða tyrir Viöi
og Nortli Atiantic íer allur til Japans.
Þá vilja Japanir frckar smærri álinn
og það hcntar okkur ágæflega. Hér
á norðurslóðum crum við kannski
ckki rncð kjöraðstæður fy rir ál og
hann vcröur þvi ckki cins sfór og
sunnar í áiftmni.
Misjafut cr cftir löndum hvcrn-
ig ál mcnn viJja hclst. Þannig vilja
Frakkar frekai minni ál en t.d.
Brciar og aðrar þjóðir i kring. Þá cr
misjafnt hvcrnig mcnn vcrka álinn
og Brctar rcykja hann t.d. frckar cn
Hollcndingar og Danir.
J3g setti cinu sinni að gamni minu
auglýsingu á „tíusincss to busmcss"
siðu á nctinu til að kanna áhug-
ann á álnum sem cg var að veiða.
Skem mst er frá að segja að þaö
scttu sig sirax i samband við mig
aóilar fiá Hollandi, Frakklandi og
Bandarikjumun scm allir voru nijög
áhugasamir."
Siguijon segist vita til aö eiu-
hvað sc flutt inn a f rcyktum ál, cn
þar scu vissulcga tækifæri fyrir
íslcnska framlciðsfu á ál.
„Állinn ci að ininu mati klár-
lcga vannýtt aaölind og það cr mun
mcira a f honum cn margur hcidur.
Fólk vcit ckki a f honum vcgna þcss
að hann grefur sig i bornloójuna
þannig að aðcins hausinn stcndur
upp úr.
Þaö má segja aö alls staðar þar
som vatn kcm.st i sjó við Suöur- og
Vcsturland. þar fmnist áll. Mcnn
hal'a verið aó scgja mcr að þcir haíi
vcrið aó fá ál i kolbrúnum pollum
þar scm incnn hcldu aó nær ekkcrt
líf væri. Ég hcld cg hafi aldrci sctt
álagildrur niöur i polla sem ckk; hat'a
cinhvcr álakvikindi álpast i. Það cr
ótrúlcgt hvað hann er víða. Þaö cr
t.d. áll i öllum vötnum i kringuin
Reykjavik. Á árum áður var t.d. veitt
talsvcrc a f ál í Vifilsstaðavatni."
'HKr.
Áll - sextán til tuttugu ættkvíslir
Til ættkvíslarinnar Anguiliídae teljast 16 tii 20
! tegundir ála sem eru nokkuð óltkar að útliíi og
finnasi vída um hcim, aö Suöur-Atlantsbafi og
: austanverðu Kyrrahafi undanskildu.
Tvær tegirodír ála eru þekktar í Atlantshafi: önnur
! cr evrópski áJlinn (Anguilla anguilla) en hinn ameríski
i állinn {Anguilia rosfrata). Evrópski og atneríski áJlinn
j ern ólílcir aö því leyti aó sá evrópski hefur aö mcðalt3li
i 114 hiyggjarfiði en sá ameríski sjö færri. eða 107.
j Sumir álar á íslandi itafa færri hryggjarliði enevrópski
áílinn en fieiri en sá ameríski og eru sérstakir að því
j lcyti og nýjar erfðarannsóknir sýna aö hér sc um að
J ræða bíendinga á milli þessara tveggja tegunda.
Heimkynni cvrópska álsinscrá íslandi, í Færeyjum
i og Bretlandi. Frá Noröur-Noregi að Miðjaröarhafi
! og austur að Svartaiiafi. Hann íínrisr í áni og vötn-
! um i Mið-Asíu og þeim löndura Afríku sem hggja
; aö Miðjaróarhafi auk þess sem hann er þekktur á
j Asóreyjum, Madeira og Kanaricyjum og við norð-
vesturströnd Afriku suður til Senegal. Ameriski állinn
finttst i austanverðri Norður-Ameriku ogá Grænlandi.
Afft 100% hrygnur
I Bjanii Jónsson. fiskifrarðingur hjá Veiðímálastofnun.
sem rannsakað hetúr ála á Islandi, segir i grcin sem má
finnaá landbunaður.is: „Rannsóknirá gulál ogbjartái
hafa l>cinst aö útbreiöslu ála á Islandi, búsvæöavali,
iíísháttmn og nýtingarmöguleikum. Þessar rannsóknir
hafá leitt i ijós að áía er aö finna i ölJum landshlutum á
! fjölbreyttum búsvæöum og með ólika lifshætti. Hluti
• ála virðist ala ailan aldur smn i sjó án þess að íára i
j ferskvam eða ísalt vatn. Nidurstöður benda einiug tíl
i þcss aö munur sé á tcgundasamsetningu eftir búsvæð-
! um og jafnvei iandslilutura. Það er cinstakt á Íslandí
j að víðast er meirihluti ála hxygnur en hængar eru i
i raiimihíuta. Kynákvöróun ála er umhverfisháð og fer
i kynjaliJutfali álu ahnenm annars staöar á útbreiöslu-
svasði þeirra eftir búsvæðuni. ísland viröist þvi skera
sig hér úr og er hlutfali hiygna víöa allt að 100%."
llrogn og Urfur
Alar lirygna á voriu í Þangliafinu (Sargasso-liafinu)
við austurströnd Miö-Ameríku. Jirygning fer fram á
400- 700 metra dýpi í úthafmu þar sera sjávardýpi er
um 6000 m. Hrogn og lirfur eru sviflæg. Lirfumar
(Lepiocephalus) berast með (iclfstramnnum að strönd-
um Evrópu og Amcriku og tekur það ferðalag um eitt
ár. Áður varralið að ferðaíagið tæk; þrjú ár.
GleráU
Liríumar m\rndbreytast þegar þær nálgast strendur og
kallast þá glerálar. Gleráiar em giærir og um 6 -S sm
iangir. Gleráiar sækja að strönd og ganga i ferskvotn. j
Smárn saraan verða þeir guibrúnir á litinn og nefnast
þá álasciöi. Gleráiar og áiasciði ganga i fcrskvatn að j
sumarlagi. Göngur ála cru háóar hita i vatni og gengd
er meiri í hlýium sumrum. E f fossar eru á Jeið ála
upp ttniar þá skríða áiarnir upp raka kletta eða gras
framhja fossum.
Guláll
Lífsskilyrði t'yrir ála í uppeidi (guiála) cru bcst i grunn-
um vötnum á láglendi scm hlýna aö sumarlagi. Álar
i fersku vatnt éta ýmis stnádýr á botninum. Aiar vaxa j
um 5-6 sm á árí. Álar er hitakærir og kjörhiti þcin-a j
til vaxtar er 22-23 °C.
BjuriáU
Þegar áil hefur náð um 35-100 sentimetra lengd þá
sækir hann í Þanghafiö til að hrygna. Hann tekur áður j
miklum útlitsbreytiugum. augun stækka. bakið dökkn- j
ar. kviöur vcrður siilurlitur og slím á húð minnkar. j
Slíraug húð ála er talin vera vöm gcgn breytingu á j
saltituiihaldi vatns.
Állinn hættir aö éta á ákveðnu þroskastig;, magi og
garnir lians skreppa saman en kynt'æri taka aö broskast.
A þcssu skeiði nefhist áll bjaitáll. Hængar eru þá 35—50
sm aö lengd og 60-200 g þungir og lirygnur 45-100 sm j
langar og vega 100 g-2 0 0 0 g. Fundist hafa álar sent eru
125 sm og 6 kg. Það er háð vaxtarskilyröum hvenær
álar yfirgefa fcrskvatn og halda út á haf. Á íslandi eru
álar líklcga X-14 ára þcgar ganga bjartála hefst. Göngur
ála aukast þegar hiti lækkar aö haustt. Gönguraar er
tnestar aö næturiagi. Ferö bjartála á hrygnúigarstöövar i
Þanghafmu crallt aö 6.500 km löng. Talið eraðálarm r j
haldi sig á ura 50 -400 metra dýpi á meöan á feróinni !
stendur. Ál3r deyja að hrygningu lokinm.
Álustofninn i Evrópu
Talið er að fjöldi óln sem nasr ströndum Evrópu hafi !
minnkað um 90% frá 1970. Mögulcgt cr að það stafi
a f náttúrulegum svciflum eða ofveiði, sé a f völdurn !
sníkjudýra eða vegna þess að áll gctur ekki gengið i
ár vcgna hindrana t.d. a f völdum vatnsaflsvirkjana.
Talió cr að fækkun ála megí að einhverju leyti rekja j
til m engunamf völdum PCB.
AlaveuUir og álaeldi
Álaveiöar eru stimdaðar með ftéttuðum netum. Áll j
er mikilvægur matfisknr í strandhéntðum í Evrópu,
m.a. i Danmörku, Þýskalandi, HoIIaudi. Bretlandi og j
i Frakklandi. Reyktur áll er einníghluti at'hefóbundnu :
sænsku jólahlaðborði.
ALARANNSOKNIR
Ný sannindi
um álinn!
Bjarni Jónsson á Norðurlandsdeiid Veiðimálastofnunar á Hólum í
Hjaltadal hefur frá árinu 1999 unnið að viðamiklum rannsóknum
á álum við Island. I gegnum tíðina hefur sjónum vísindamanna í
litlum mæli verið beint að álnum, en rannsóknir Bj-arna hafa þegar
leitt í ijós ýmis ný og áður óþekkt sannindi um álinn.
Á ársfundi Veiðimálastofnunar
nýverið gerði Bjarni stuttlega
grein fyrir rannsóknum sínum,
sem hafa verið unnar í samstarfi
við vísindamenn í Japan, Kanada
og Belgíu. Fram kom í máli hans
að þekking á lífsháttum ála hér
við land hafi tii þessa að mestu
verið byggð á eriendum rann-
sóknum. Hins vegar sé ljóst að
margt sé ólíkt með lífsháttum ála
á Islandi og annars staðar þar sem
hann er að finna. I því sambandi
skipti máli staðsetning iandsins
og sérstaða íslenskrar náttúru
með sínum fjölbreyttu búsvæðum
en tegundafæð. Þá segir Bjarni að
ísiand sé eina iandið þar sem
bæði sé að finna svokailaðan evr-
ópuál og amerískan ál og nýjar
erfðafræðirannsóknir staðfesti að
hér á landi sé einnig að finna
blendinga á milli þessara tveggja
tegunda.
Glerálar veiðst á fjórtán
stöðum á landinu
Bjarni Jónsson segir að áiar á Is-
landi nýti sér fjölbreytt búsvæði í
ám og vötnum og þá sé jafnvel að
finna í svo ólíkum búsvæðum
sem heitum lækjum, köldum og
dimmum hraunsprungum eða
fullsöltum sjó við ströndina.
Rannsóknir Bjarna hafii ekki síst
beinst að göngum glerála til
landsins, útbreiðslu, vistfræði og
tegundasamsetningu ála á Islandi.
Frá því rannsóknirnar hófust hafa
glerálar veiðst á fjórtán stöðum á
landinu. Rannsökuð hafa verið
áhrif sjávarfalla, vatnshita, birtu
og fleiri þátta á atferli glerálanna.
Einnig hafa daghringir í kvörn-
um glerálanna verið notaðir til að
tímasetja hin ýmsu myndbreyt-
ingaskeið hjá álalirfunum, hve
Bjarni lónsson.
lengi þær eru á leið til landsins
og tegundirnar bornar saman.
Eitt ár í stað þriggja
Aðalgöngutími glerálanna er frá
maí og fram í byrjun júlf en
þeirra fyrstu verður vart í endaðan
mars og apríl. Gangan er að
mestu yfirstaðin um miðjan júlf
ár hvert. Samkvæmt rannsóknum
Bjarna eru sjávarföll og vatnshiti
þeir þættir sem ráða hvað mestu
um göngurnar hériendis. Rann-
sóknir á daghringjum í kvörnum
gieráia sýna að þeir eru um eitt ár
á leiðinni yfir hafið frá Þanghaf-
inu til Islands, en áður var talið
að ferðin tæki þá þrjú ár.
Rannsóknir á gulál og bjartál
hafa beinst að útbreiðslu ála á ís-
landi, búsvæðavali og lífshártum.
Þessar rannsóknir hafa leitt í ljós
að ála er að finna í öllum iands-
hlutum í fjölbreyttum búsvæðum
og með ólíka Iífshætti. Hluti ála
virðist ala ailan aldur sinn 1' sjó án
þess að fara f ferskvatn eða ísalt
vatn. Niðurstöður benda einnig
til þess að munur sé á tegunda-
samsetningu eftir búsvæðum og
jafnvel landshlutum.
Fullvaxinn áll
um einn metri að lengd
Fullvaxinn áll getur orðið um
einn metri að lengd og um fjögur
Álar veiddir með rafmagni við Bár á Snæfellsnesi.
sem ala allan aldur sinn í sjó er að finna i hrauninu við
Grindavík.
Glerálar rafveiddir á fjöru vió ósa Vogslækjar á Mýrum.
ÁLARANNSÓKNIR
Glerálar veiddir meö scuba háfum á flóði við Vogslæk á Mýrum.
Tekin erfðasýni af álum.
kíló að þyngd. Hrygnurnar verða
mun stærri en hængarnir. Stærsci
áll sem hefur verið mæidur hér á
landi var 130 cm iangur og vó
6,5 kíló. Fyrscu fimm árin vex ái-
linn um 4-6 cm á ári, en síðan
dregur úr vextinum og eftir það
vex hann um 1-2 cm á ári.
Hængar verða kynþroska 5-10 ára
gamiir og eru þá orðnir 30 tii 50
cm langir. Hrygnurnar verða á
hinn bóginn kynþroska 8-15 ára
og eru þá 50-100 cm. Kyná-
kvörðun hjá álnum er umhverfis-
háð og er hlutfal! hrygna óvenju-
hátt á Islandi. Alinn hefur mjög
næmt lykcarskyn og nocar það við
að ieita uppi bráð sína. Vitað er
að állinn étur orma, snigia,
krabbadýr og skordýr, einnig
hrogn, hornsíli og seiði annarra
fiska.
Lítið hefur verið veitc af ál við
Island á síðustu árum, en fyrir um
fjórum áratugum var hann nýttur
í umtalsverðum mæli. Þannig eru
til upplýsingar um 15 tonna ála-
veiði árið 1961 og var áliinn þá
fluttur lífandi tii Hollands. Árið
eftir var byggt álareykhús og
veiðin var um 22 conn. Síðan dró
ört úr þessum útvegi.
Ekki vitað um stofnstærð
„Það hefur komið í ljós í þessum
rannsóknum að ál er að finna í sjó
allr f kringum landið, en til þessa
hefur verið calið að állinn væri
hér við land aðeins í ferskvatni
eða saltblönduðu vatni - sjávar-
lónum eða árósum. Rannsóknirn-
ar benda hins vegar til að áll sé !
cöluverðu mæli f sjó hér við land
og komi aldrei í ferskvatn. Þess
vegna er mjög erfitt að segja til
um á þessu stigi hversu scór þessi
stofn er hér við land," segir Bjarni
Jónsson í samtali við Ægi. „Með
frekari rannsóknum þurfum við
að leiða í ljós eins og kostur er
hversu stór þessi stofn er," segir
Bjarni. Hann segir að framundan
séu spennandi áiarannsóknir,
meðai annars þurfi að afla víð-
tækra upplýsinga um ýmsa líf-
fræðilega þætti álsins og frekari
nýti ngarmöguiei ka.
Vitjað um álagildrur í Áshildarhoitsvatni í Skagafirði.
4
ICELA NDAIR
C A R G O
Ingi Björn Albertsson, fyrrv. alþingismaður,
rifjar upp áralanga baráttu fyrir kaupum á TF-Líf
VELALAMD ®
V É L A S A L A - T Ú R B ÍH U R {
V A R A H LU T IR * VH IG ER Ð IR :
M I T S U B I S H I
DIESEL ENGINES Vélaland ehf • Vagnhöfði 21 • 110 Reykjavík
V erö í l a u s a s ó l t i kr. 600
IS SN 0 0 0 1 -9 0 3 3
96. á rg a n g u r
4. tö lu b la ö 2003
0 00160
F is k ifr é tt ir FIMMTUDAGUR 1. JÚ N Í 2017
Glerálar sem veiddir voru vorið 2015.
— Sam fe lldar rannsókn ir á álum stundaðar f um 20 ár_________________________________________________________________
Állinn á íslandi hefur sérstöðu
Álar á íslandi eru um
m argt ólíkir álum í
öðrum löndum Evrópu.
Hér er kynblöndun ála
frá Ameríku, næ r allir
álar eru hrygnur og
göngur gleráls hafa ekki
hrunið. Staða álastofna
hér er góð ólíkt því sem
þekkist annars staðar.
KJA RTAN STEFÁNSSON
k ja rtan@ fisk lfrettir.is
Bjarni Jónsson, forstöðumað- u r N áttúrustofu Norður- lands vestra, hefur vaktað og
kortlagt glerálagöngur á íslandi
frá árinu 1999 og stundað marg-
víslegar aðrar rannsókn ir á álum,
svo sem um útbreiðslu, búsvæði,
vistfræði, tegundasam setningu,
nýtingarm öguleika og fleira. Nið-
u rstöður ú r rannsóknum hans
hafa kollvarpað ým sum fyrri
hugm yndum um ála á íslandi.
Frá því að ran n só k n ir B jarna
hófust hafa g lerálar veiðst á um
30 stöðum hér á landi. Seinni
árin hefur Bjarni einbeitt sér að
10 lykilstöðum þar sem h ann hef-
u r kannað árlega göngur glerála.
Einstök lífssaga
Lífssaga áls á sér fá eða engin for-
dæmi. H ann h ry g n ir í Þanghaf-
inu djúpt au stu r a f Flórídaskag-
anum . Þ ar eru tvæ r aðskildar
tegund ir ála, E vrópuáll og Am-
eríkuáll. L irfur ála berast það-
an með straum um til ým issa
landa við N orður-A tlantshaf-
ið. A m eríkuállinn fer norður og
vestu r en Evrópuállin au stu r og
norður.
Á llinn á sér þrjú lífsskeið eft-
ir lirfustigið. Seiðin sem koma
að landi eru eins árs gömul og
nefnast þá glerálar. Eftir að áll
hefur valið sér búsvæði, aðallega
í lækjum og vötnum, nefnist hann
guláll og er hann á því stigi mest-
an hluta ævinnar. H ann verður
kynþroska 7 til 16 ára og umbreyt-
ist þá í bjartál. Þegar kynþroska
er náð gengur hann til sjávar og
syndir í Þanghafið til hrygningar
og deyr að henni lokinni.
Finnst í ö llum landshlutum
Bjarni sagði að glerállinn kæmi
mest hingað ti l lands á tím ahilinu
10. m aí til 10. júní. H ann sagði að
ála væri að finna í öllum lands-
hlutum , búsvæði þeirra væ ru fjöl-
breytt og lífshæ ttir ólíkir. Fram
kom hjá Bjarna að ekki a llir álar
færu upp í ferskvatn. Hluti afþeim
lifir við ströndina og fer aldrei í
ferskt vatn og lifir annaðhvort í
fullsöltum sjó eða ísöltu vatni.
Mest af álunum er á svæðinu
frá Höfn og til Reykhóla. Þeir um-
hverfisþætlir sem ráða álagöngum
hér, sérstaklega á álum sem ganga
upp í vötn, eru aðallega sjávarföll
og vatnshiti.
Á llinn læ tu r yfirleitt lítið fyrir
sér fara. H ann lifir á fjölbreyttu
fæði; sm ádýrum og flugum,
hornsíli og vatnabobbum. Þegar
hann kem ur hingað er hann um
Álar í gildru íVífilsstaðavatni sumarið 2015 en aldrei hefur komið meira í vökt-
unargildrurnar en þá.
Evrópuáli.
mailto:kjartan@fisklfrettir.is
FIMMTUDAGUR 1 .JÚ N Í2017 F isk ifré tt ir 7
é é Það er því ta lsverð uppsveifla í
glerá lag ö ng u m til íslands síðustu
þrjú árin. G lerá lagöngur hafa langt
í f rá dregist eins mikið saman
hlutfalls lega á íslandi og víðast
annars s tað ar í Evrópu.
fimm til sjö sentím etrar að lengd
en getur farið upp í 70 til 120
sentím etra fullvaxinn.
Kynblöndun ála á íslandi
„Seinni árin höfum við stundað
um fangsm iklar erfðarannsóknir
á álum. ísland er eina landið þar
sem finna m á bæði h reina Evrópu-
ála og kynblendinga við amerísk-
an ál. Rannsóknir okkar staðfesta
um fangsm ikla blöndun þessara
tegunda hér. Þessi kynblöndun
kem ur ekki annars staðar fram
á útbreiðslusvæði Evrópuáls-
ins. Við höfum einnig sýnt fram
á að afkvæm i kynblandaðra ála
á Tslandi eru líklegri til að koma
hingað til lands á slóðir foreldr-
anna. Það sannar að lirfu r berast
ekki alveg tilviljunarkennt til ís-
lands ólíkt því sem áður er talið
og finna m á í fræðibókum,“ sagði
Bjarni. „Þá beinast rannsóknir
okkar einnig að áhrifum loftslags-
breytinga á erfðasam setningu og
kynblöndun.“
Skörun vid A m eríku-
álinn í Þanghafinu
Bjarni sagði forvitnilegt að athuga
tím asetninguna á því hvenær
álar frá íslandi koma í Þanghafið
til hrygningar. „A m eríkuállinn
hrygnir aðeins seinna en Evrópu-
állinn. Væntanlega eráll frá íslandi
frekar seint á ferðinni þannig að
hrygning hans og A m eríkuálsins
skarast aðeins. Það útskýrir mögu-
lega erfðablöndunina á álum sem
koma til Islands.“
Aðeins e it t á r t il íslands
Bjarni hefur rannsakað kvarn ir í
glerálum og fullorðnum álum en
út ú r þeim m á lesa áhugaverðar
upplýsingar um lífshæ tti og far.
„Við fundum það ú t með því að
skoða daghringi í kvörnum gler-
ála að þeir voru aðeins eitt á r á
leiðinni ú r Þanghafinu til íslands.
í fræðibókum stóð h in s vegar að
ferðin hingað tæki þrjú ár sem var
rangt.
Við höfum líka efnagreint
kvarn ir gulála. K alsíum hlutfall
árhringja segir til um hvort állinn
hafi alið aldur sinn í söltu vatni
eða fersku. Sem dæm i þá rann-
sökuðum við sjávarála á höfuð-
borgarsvæðinu sem sum ir v irtust
hafa gengið upp í Ú lfarsá, Elliðaár
og nærliggjandi læki og verið þar
í tvö ár en leitað í sjóinn á ný og
ekki farið aftur í ferskt vatn. Aðr-
ir höfðu aðeins dvalið í s jó s a g ð i
Bjarni.
Hæ ngarnir hverfandi
Það er einstakt á íslandi að víðast
hvar er m ikill m eirihluti ála
hrygnur en hængar eru í m iklum
m innihluta. Kynákvörðun ræðst
af umhverfisaðstæðum ogbúsvæð-
um og skiptast því á svæði þar sem
hængar og hrygnur eru ráðandi.
Island virðist því skera sig hér ú r
og er hlutfall hrygna hátt og víðast
allt upp í 100%. „Bækurnar segja
að meira sé af hæng í lækjum og
ísöltu vatni en meira af hrygnum
í vötnum . Rannsóknir okkar leiða
allt annað í ljós hvað ísland varð-
ar. Hér eru hrygnur ráðandi á öll-
um búsvæðum . Þá má geta þess
að við Marokkó, á hinum jaðri
útbreiðslusvæðisins, er aðallega
hæng að finna," sagði Bjarni.
Sveiflur í glerál
Ekki er vitað um stofnstærð áls
á íslandi en rannsókn ir á gler-
ál gefa ágætar vísbendingar um
þróun glerálagangna. „Við höf-
um um 20 ára sögu yfir mæling-
ar á glerál á ákveðnum stöðum.
Glerálagöngur voru þokkalegar
að jafnaði árin 1999 til 2005. Eft-
ir það tók við 10 ára lægð en mik-
il aukning varð aftur árið 2015 og
reyndist 2016 næ r því besta frá
því að m ælingar hófust. Þeir stað-
ir scm búið er að mæla nú í vor
koma einnig vel út. Það er því tals-
verð uppsveifla í glerálagöngum
til íslands síðustu þrjú árin. Gler-
álagöngur hafa langt í frá dregist
eins m ikið sam an hlutfallslega
á íslandi og víða annars staðar í
Evrópu," sagði Bjarni.
Ekki virðast hafa komið fram
jafnm iklar sveiflur í fjölda og
sam setningu gulála m illi ára og er
í fjölda glerála. Bjarni hefur vakt-
að nokkra staði og til að mynda
Vífilsstaðavatn öll árin 1999 til
2016. Þar er ekki sjáanlegt að
magn gulála hafi m innkað í vatn-
inu. Árið 2015 var meira að segja
motveiði þar. Bjarni taldi að draga
mætti a f þessu þá ályktun að dán-
artala glerála réðist að nokkru af
þéttleika.
V an n ý ttir m öguleikar
Hrygnur hafa meiri vaxtarmögu-
leika og verða stæ rri en hængarn-
ir. Þær eru því eftirsóttari til veiða
og til eldis. Bjarni sagði að tals-
verðir vannýttir möguleikar væru
fyrir hendi í álaveiðum á íslandi.
Sérstaklega v irtust veiðar á bjart-
álum geta gefið góða raun. Hins
vegar skorti tilfinnanlega enn
m eiri rannsóknir og þekkingu á
lífsögu álsins, vexti, aldursdreif-
ingu og stofnstærð eftir svæðum
svo skipuleggja m æ tti sjálfbærar
veiðar.
Stadan betri á íslandi
Evrópuállinn er á lista yfir dýr í
ú trým ingarhættu. Þar spila marg-
ir þæ ttir inn í, svo sem ofveiði, sér-
staklega á glerál, búsvæði áls hef-
u r verið skert eða eyðilagt, lokað
á farleiðir og sjúkdómar og sníkju-
dýr hafa herjað á stofnana. Bjarni
sagði að glerálagöngur í Evrópu
væru víðast aðeins 1-5% af því
sem þæ r voru hér á árum áður og
við það bæ ttist að lítill h lu ti þeirra
kæmist upp og lifði til að komast
aftur á hrygningarslóð.
„Staðan á íslandi er betri. M argt
er ólíkt með lífsháttum ála á Is-
landi og annars staðar þar sem
h ann er að ÍTnna. Ylri aðslæ ður
hafa ekki breyst m ikið hér við
land fyrir u tan h lýnun vegna
loftslagsbreytinga. Við erum
ennþá laus við m arga sjúkdóma
og sn ík judýrsem herja á álastofna
í Evrópu. Ekki hefur verið þrengt
eins m ikið að búsvæ ðum álsins
hér og veiðar eru litla r sem engar.
R annsóknir m ínar gefa vísbend-
ingar um að staða álsins sé góð á
íslandi og að álastofninn hér sé á
uppleið,“ sagði Bjarni.
V iðm iðunarreglu r í Evrópu
í ljósi stöðu álastofna í Evrópu
voru settar viðm iðunarreglur
sem miða við að einstökum
rík jum beri að tryggja að hið
m innsta 40% þeirra ála sem lif-
að hafa tak ist að ganga til sjávar,
þ.e. án affalla af m anna völdum,
vegna veiði, eyðileggingar bú-
svæða, tú rb ína virkjana og ann-
arra m anngerðra áhrifaþátta. Þá
ber þeim að leita allra leiða til að
endurheim ta búsvæði og grípa
ti l annarra aðgerða til að fást við
neikvæða m anngerða umhverfis-
þæ tti. Sum ar þjóðir geta vart
náð þessum m arkm iðum , nema
banna álaveiðar og dugir jafnvel
ekki til vegna um hverfisspjalla.
Ö ðrum þjóðum er þetta létt-
ara og ljóst að ekki þarf að fara í
svo íþyngjandi aðgerðir eins og
veiðibann á íslandi til að upp-
fylla þessi m arkm ið, en auðvitað
ber íslenskum stjórnvöldum að
útskýra sérstöðu okkar í þessum
efnum , að sögn Bjarna.
Engin þörf á veiðibanni á ísiandi
Fram er komið frum varp á Al-
þ ingi um bann við veiðum á áli
á íslandi. Bjarni sagði það skjóta
skökku við að sjá slíkar tillögur
þ a r sem ekkert benti til að þeim
álastofnum sem héldu sig hér á
landi væri hæ tta búin. „í greinar-
gerð með frum varpinu er vísað
í skýrslu frá Alþjóðahafrann-
sóknaráðinu, ICES, og látið að því
liggja að ICES leggi til veiðibann
hér. Ég hef skoðað skýrsluna og
þar er enga slíka tillögu að finna.
H ins vegar leggur ICES til bland-
aðar leiðir til að stjórna veiðum og
aðgerðum sem stuðla að uppbygg-
ingu álastofna sem eiga að taka
m ið af s töðunni í hverju landi.
Á íslandi er ekkert sem kallar á
veiðibann eins og áður er getið,“
sagði Bjarni Jónsson.
Bjarni Jónsson við vöktunarstað gleráls við Stokkseyri ívor. Aðstæður voru erf-
iðar, óvenjumikið vantsrennsli og litur á vatni. Engu að síður var góð veiði gler-
ála. Fjöldi glerála var falinn ískjóli við steina á myndinni sem eru undir sjó á flóði.
MYND/HALLDÓR ARINBJARNARSON
www.hampidjan.is
Veiðarfæri
eru
okkar fag T O G T A U G A R
Skarfagörðum 4 , 1 0 4 Reykjavík S ím i:5 3 0 3 3 0 0
http://www.hampidjan.is
FISKIFRÉTTIR 26. ágúst 2005
id ó ttu r
i botni
Noregi í
;ur orð-
ú síðast
cgsráð-
í kostn-
skjóls-
væri út
:r fram
iherrann
ffa flak-
rirtækið
að full-
iu og ná
því og
tjólshús
: í næsta
rar líafa
i og því
hjálpa
lckja út
ipa hon-
tráætlun
um 400
u fimm
3 í hug-
orn því
íeikvætt
ráöherr-
Prepare
ki vera
samtali
lö fyrst
isa llak-
á veröi
nýju að
•otni og
turodd-
taönum.
ra vera
k skips-
arafurð-
ið tæma
irinu er
icildar-
6,4% á
L*r fram
nbands
tur hafi
i þessa
i fyrra.
ir Fiski-
r 8.320
la hefur
lega frá
35.976
íma fyr-
Flestir kannast við það að
á lar eru ferskvatnsfiskar sem
ganga í á r og vötn hér á landi.
H itt er á fæ rra vitorði að hluti
á la sem hingað ganga hafa
aldrei í ferskvatn komið en
dvelja í sjó allan sinn iíftíma.
Þctta eru svokallaðir s jávará la r
sem má veiða í fjörum og á
grunnsævi hér við land. Tiltöiu-
lega stu tt e r síðan synt var fram
á þetta hér á landi en sjávarál-
a r eru þekktir víða annars stað-
ar. Það seni e r óvenjulegt viö
sjávarál hér við land er að hátt
h lutfall hans e r h rygnur og
hann er jafn fran it s tæ rri en
gengur og gerist um ála hér á
landi, að því er B jarni Jónsson,
fisk ifræ öingur h já N orður-
landsdeild Veiðimálastofnunar
á Hólum, sagði í sam tali við
Fiskiíréttir, cn hann hefur með
aðstoð sam starfsm anna sinna
við Tokyo háskóla sýnt fram á
tilvist sjávarála hér við land
fyrstur manna. Vænn sjávaráll sem veiddist í Grafarvoginum.
Sýnt fram á í fyrsta sinn að
sjávarálar finnast við ísland
— hluti álastofnsins við ísland hefur a ldre i í ferskt eða ísa lt vatn
komið en elur allan sinn aldur í sjó sam kvæ m t rannsóknum
Bjarna Jónssonar fiskifræðings
Bjarni
Bjarni sagði aö þótt álar vcidd-
ust aðallega í ferskvatni hcfðu þeir
einnig veiöst í sjó við ísland en
ekki hafói veriö hægt aö
segja til um hvort aö um
lengri eöa skemmri dvöl
hctÖi vcriö aö ræða vió
íull seihtskilyröi. Hins
vegar cr unní aö komast
að niöursiööu uin hvar
og hvenær állinn hef'ur
dvaliö meö því aö mæla
efnasamsetningu t
kvömum fisksins. Ný-
iegar rannsóknir á
kvörnum ála viö Japan hafa til
dæmis sýnt aö hluti tegundarinnar
þar hcfur aldrei komið nálægt
ferskvatni og dvelur ailan sinn ald-
ur í sjó. „Því var ákvcðiö aö fram-
kvæma úttekl á lífssögu ála
veiddra í sjó viö ísland meö þaö aó
augnatniði aö rckja feröir jieirra á
milli sjávar og ferskvatns ásamt
því aö svara þeirri spurningu hvort
einhver hluti þeirra ála sem til ís-
lands koma dvclji allan sinn aldur
í sjó,“ sagöi Bjarni.
Álar veiddir í
G rafarvogi
Bjarni sagöi aö þessar rann-
sóknir heföu farið þannig ffam aö
álar voru veiddir í sjó víösvegar í
kringum landiö. M voru álar scm
veiddir voru í Grafarvogi í Rcykja-
vík valdir sérstaklega fyrir fyrsta á-
fanga rannsóknarinnar. AUs voru
veiddir 50 álar í smáriönar ála-
gildrur í Grafarvogi í júlí til ágúst
2003. Álamir voru lengdarrnæídir,
vigtaóir og kyn ákvaröaö ásamt því
aÖ kynkirtlar voru vigtaöir. sCvam-
ir voru teknar til grcininga á hlut-
falli scltu (Strontium/Calcium) scm
segir fvrir um íifssögu álanna meö
tilliti til vcru i ícrsku vatni og sjó. 1
f)Trsta áfanga verkcfnis-
ins voru kvarnir 15 ála
efnagreindar. Stæröar-
drcifhg ála sem vciddir
voru í margvíslegum bú-
svæöum var oinnig tekin
saman til frckari glöggy-
unar á lífsháttum áia á ís-
landi. Sjálf dhagreinmg
kvarnanna fór fratn hjá
. , samstarsfólki viö Tokyo
jonsson. háskóJa Samhhóa
um rannsóknum voru frainkvæmd
tvö verkefni framhaldsnema í
Kanada og á ísiandi þar scm athug-
uö var svipeerö og ertÖæsamsetning
sjávarála í samanburöi viö ála úr
ferskvatnsbúsvæÖum.
Þrenns konar Iífssaga
Bjarni gat þcss aö í ijós heföi
komið aö allir þeir 50 álar scm
veiddir vom i sjó í Grafarvogi og
rannsakaöir hefðu veriö hrygnur
en taliö heíur veriö aö hænga væri
írcmitr aö finna i slíkum búsvæö-
um Útiii sjávuráianna og hoídafar
rcyndist nokkuö frábrugöið þvi
sem gerist ineðal ála scrn vciddir
voru í ferskvatni. Sjávarálarnir
voru lil aö mynda hlutfallslega
feitari cn ferskvatnsálarnir. L-rföa-
samsetning þeirra var hins vegar
svipttö, og reyndist meirihluti ál-
anna vera Evrópuáll en hluti kyn-
blendingar á milli Evrópuála og
Ameríkuála. Grcining kvarna 15
fiska gálu skýrar niöurstööur um
breytileika í lífssögu álu á íslandi
meö tilliti til dvalar í fersku vatni
og sjó. Skipta má álum viö Isiand i
þrennl eflir lífssögu samkvæmt
greiningu á kvörnum. Hluti þcirra
ála sem veiddir voru í sjó í Grafar-
vogi höföu í fyrsta lagi dvaliö
mestan aklur sinn síóan á glcrála-
stigi í fersku vatni. I öðru iagi
haföi hluti álanna dvaliö nokkurár
í ferskvatni en síðan gerst sjávarál-
ar. í þriöja flokknum voru svo eig-
inlegir sjávaráiar sem höföu aldrei
komiö nálægt fersku vatni.
ÓJíkt öðrum álum
í A tiantshafi
„í þessari rannsókn var í fyrsta
skipti færóar sönnur á aÖ hluti ála
scm berst til islands cyðirallri ævi
sinni í sjó. Það er einnig óvenju-
legt aö stærstur hluti ála sem
dvelja í sjó hér við land skuli vera
hrygnur sem aukinheldur ná mik-
illi stærö miöaö við þaö sem geng-
ur og gcrisl hjá úlum á Íslandí,“
sagöi Bjarni. Hann sagöi aö einnig
heföi komiö í ljós aö hluti þeirra
ála sem gengur í straumvatn dvel-
ur þar fyrstu ár uppvaxtar en geng-
ur því næst í sjó og klárar þar vaxt-
arskeiö sitt. Sú niöurstaöa kom
mjög á óvart, en þelta lifssögu-
form virÖist nokkuö algenut hér-
lendis. Ljóst er aö álar á Islandi
hafa óiíka lífssögu samanboriö viö
Atlanlshafsála í Ameríku og Evr-
ópu. Mögulegt cr að norðlæg stað-
setning íslands geri þaö likiegra
aö álar dvelji allan eöa hluta upp-
vaxtartíma sins i sjó viö landiö.
Aya Kotake h já Tokyo háskóla skoðar hér efnasamsetningu kvarna
ú r íslenskum álum með myndgreiningu. Selta í kvörnum sýnir ferðir
ála á milli fersks vatns og sjávar.
I veidanlegu m agni
A f og til hafa veiöar á ál veriö
stundaöar hér í ám og vötnum af
einhvcrjum krafti en yfirleitt er
hér um takmarkað magn aö ræöa.
Stundum hafa þcssar veiöar alveg
legið niöri. Bjarni var spurður
hvort hann teldi aö unnt væri aö
nýta sjávarál sérstaklcga. „Ég lel
að sjávaráll við ísland sé hér á
mörgum svæöum í vciöanlegu
rnagni. Þessar veiöar má stunda
meö gildrum í fjörum en eúmig
má fara lengra út og ieggja gildr-
ur frá bátum þar sem aöstæöur
eru Iientugar,“ sagöi Bjarni.
Sjávarálar við ísland. Efnagreining kvarna (Calcium/Strontium
hlutfall) staðfestir að hluti ála dvelur allan æviferill sinn í sjó
Bjarni Jónsson, 1 Aya Kotakc,- David LG. Noakes3 og Katsumi Tsukamoto2
'VcidíntálHstofnun Noröurland.sdcild, 551 Sauöárkrókur
^Occan Rcsoarch Invtitutc. Thc Univcrsity ofToUyo YRIDIMÁLASTOJ’N I’N
'Dcparlmcnt ofZnolng}- an'il Axclrod Instilutc oflchthyology, l.'nivcrisily ofGuclph
Inngangur
Landfræðileg lega og jarðfræ ðileg sérstaða íslands gera landið að
óvenjulegasta stað sem vitað er að A tlantshafsálar ferðast til og alist upp á.
Álar á íslandi nýta sér óvenju fjölbreytt búsvæði og njóta þar að nokkru
tegundafæðar á m eðal íslenskra ferskvatnsfiska. Þeir finnast í vötnum,
tjöm um , lækjum, ám, votlendi og ísöltum lónum allt í kringum tandið
(Jónsson og N oakes 2001). Á lar hafa einnig veiðst í sjó við ísland en ekki
hefur verið hægt að segja til um hvort að um lengri eða skemmri dvöl hefur
verið að ræða við full seltuskilyrði. Nýlegar rannsóknirá japanskaálnum
þar sem m ælt liefur verið Strontium /Calcium hutfall i kvöm um
(eym abeinum ) sýna að hluti tegundarinnar hefur aldreí komið nálægt
ferskvatni og dvelur allan sinn aldur í sjó (Tsukamoto et al. 1998; Kotake et
al. 2003). Því var ákveðið að ffamkvæma úttekt á Iífsögu ála veiddra í sjó
við ísland m eð það að augam iði að rekja ferðir þeirra á milli sjávar og
ferskvatns ásam t því að svara þeirri spum ingu hvort einhver hluti þeirra ála
sem til íslands koma dvelji allan sinn aldur í sjó. Álar voru veiddir í sjó
víðsvegar í kringum Iandið en álar veiddir í Grafarvogi í Reykjavík valdir
sérstaklega fyrir fyrsta áfanga rannsóknarinnar.
Mvnd 4. lcngdardrcifing
Mynd 1. Kvamir: Strontium/Calcium hlutfall,
álum safiiað í Grafarvogi 2003
Gerð 1
Gerð 1
Aðferðir
Alls voru veiddir 50 álar í sm áriðnar álagildrur í Grafarvogi í jú li til ágúst
2003. Á lam ir voru lengdarmældír, v ig tað irog kyn ákvarðað ásam t því að
kynkirtlar voru vigtaðir. H lutfallsleg þyngd álanna var reiknuð sem Fulton's
index= (1000x(W /L3). Hlutfallsleg þyngd kynkirtla var einnig ákvörðuð
með þvi að reikna GSI stuðul íýrir alla veidda ála (þyngd kynkirtla
(g)/þyngd (g) x 100) (tafla 1). Einungis þrír álar sýndu m erki þess að þeir
væru að verða bjartálar. A ðrir álar voru greindir sem gulálar. Kvarnir voru
teknar til greininga á hlutfalli Strontium /Calcium sem segir fyrir um lífsögu
álanna með tilliti til vem i fersku vatni og sjó. í fyrsta áfanga verkefnisins
vom kvam ir 15 ála efnagreindar. Lengdardreifm g ála veiddra í
margvíslegum búsvæðum var tekin saman til frekari glöggvunar á
lífsháttum ála á íslandi (mynd 3).
Gerd 3
G crð 2
N = 4
25 '
20' f
15 (I
10 :
5 i
Gcrð 3
N = I
IiAamWWþKAiu.
500 1000 1500 2000
Mvnd 2. Dæmigeröar breytingar á Sr/Ca hlutfalli kvama frá
miðju fram að fremra svæði kvamar (saggittal), 1. blönduð
lífsaga (fcrsk vatns síðan sjór), 2. sjávarálar, 3.
straumvatnsálar nýkomnir i sjó. Einstakir fiskar voru
flokkaðir samkvæmt Sr/Ca hlutfalli utan marka cr má tcngja
glcrálum.
Mynd.3. Vöxtur og lcngdardreifing ála á íslandi eftir búsvæðum
Tafla 1. Mcðallengd. þvngd, holdstuðull og hlutfallslcg þyngd kvnkirtla gul- og bjartála i Grafarvogi 2003.
Ixngd (cm)___________________ Þyngd (r)_____________ Ilnldstuðull (FuUon’x Indcx) MuUMbhg þvngd kynklrtln (GSI)
McðaltallSD Ijglldl mgildi n Meöaltal * SD Láglldl llágild Mcðaltal * SD I II Háglldl n Mcðallal * SD l.ac
1.644 ± 0.380 0,571 2.399 47 0.569 ± 0,318
2,309 * 0.159 2,154 2,472 3 1.596 * 0,162
1.684 * 0.403 0.571 2.472 50 0.630 * 0.396
Niðurstöður
Allir þeir 50 álar sem veiddir vora í sjó í Grafarvogi voru hrygnur.
Lengdardreifmg álanna er sýnd á m ynd 1 og hlutfallsleg lengd m iðað við
þyngd ásam t hlutfalli kynkirtla a f heíldarþyngd í töflu 1 .
Lífsaga ála var greind útfrá kvöm um . M ikill tími fer i greiningu kvam a
einstakra fiska. Greining kvam a 15 fiska gefur sam t skýrar niðurstöður um
breytileika i lifsögu ála á íslandi meö tilliti til dvalar í fersku vatni og sjó.
Hluti þeirra ála sem veiddir voru í sjó í Grafarvogi hafa dvalið m estan aldur
sinn siðan á glerálastigi í fersku vatni (gerð 1), hluti hefur dvalið nokkur ár í
ferskvatni en síðan gerst sjávarálar (gerð 2 ) og hluti ála hefur ekki komið
nálægt fersku vatni og geta því talist 100% sjávaráiar (gerð 3). Á stöðum
merktum m eð rauðum lit á m ynd 3 virðast á lar dvelja fyrst í straumvatni en
fara síðan í sjó til að klára uppvöxt sinn.
Ályktanir
í þessari rannsókn eru í fy rsta sk ip ti sönnur fæ rðar á að h lu ti á la sem berst til
ís lands eyðir allri æ v i sinni í sjó.
Þ að er e inn ig óven ju leg t að s tæ rstu r h lu ti á la sern dve lja í s jó hér v ið Iand
skuli vera hrygnur, sem au k inhe ldu r n á m ikilli stæ rð m iðað við það sem
gengur og gerist h já álum á íslandi.
H luti þeirra á la sem gengur í s traum vatn dvelu r þ a r fy rstu ár uppvax tar en
gengur því n æ st í sjó og k lá rar þar vax ta rske ið sitt. Sú n ið u rs tað a kom m jög á
óvart, en þe tta lífsöguform v irð ist nokk u ð algeng t hérlend is og þegar litið er
á lengdardreifingu á la í m ism unand i búsvæ ðum hérlendis (m ynd 3) er
g rein ileg t að á sum um þessara s tað a v írðast álar dve lja skam m an tím a.
L íklegt e r að á e in m itt þessum stöðum séu á lar sem byrji uppvöx t í læ kjum
sem b jóða upp á góð sk ilyrð i fy rir sm áan og ungan fisk, m eð takm örkuðu
afráni og góðum vax tarsk ily rðum , en þegar að þau búsvæ ði fa ra að vera
takm arkand i m eð auk inn i stæ rð ála, þá leiti þeir í s jó til að k lá ra vöx t sinn
þar sem m eira fram boð e r a f fæ ðu.
L jóst e r að á lar á ís land i ha fa ó lík a lífsögu sam anborió v ið A tlan tshafsá la í
A m eriku og Evrópu. M öguleg t e r að norð læ g s taðse tn ing ís lands geri það
lík legra að á lar dvelji allan eð a h lu ta u ppvax ta rtím a síns í sjó v ið landið.
ÞakkarorO
Vid þökkum Sigriði Ingóltsdóttur. Eik h.Ilarsdóttur og Guðmundi Inga Guðbrandssyni fyrir hjálp við álavciðar og að
hafa yfirstigið vandamál þvi samfara.
Heimildir
Jónsson. B. ogNoakcs. D. L. G.. 2001. Icelandic ccls. Procccdings of thc Inlcmational Symposium: Advancos in ccl biology. 28-30 scptembcr 2001.
Kotakc A. ct a!.. 2003. Variation in migratory history o f Japancsc ccls. Angttillajaponica. collected in coastal watcrs o f thc Amakusa Islands. Japun.
infcrrcd from otolith Sr/Caratios. Marine Biology 142: 849-854.
Tsakumoto, K. c l al.. 1998. Do all frcshwatcr ccls migratc? Nature. 396: 635-636.
Harðardóttir.
ttir að Sigmar
jhúsgæðingur,
:s!uþátt í haust
: pottgæðingur
ái í eldhúsíð tii
nmtilega menn
3
re v r Gíslason.
i. Ekki er vitað
ieiðar Anton
ar annar tveg-
num - eftir að
jhd; lék fyrír
' Döiníiinní á
gar
iin -
.um
n Magnússon.
Ólafur Páll
ðalagi í Dan-
,:t meðal ann-
istarmann af
e r á Jótiandi.
jurfti hann að
tarferð. I iest-
mann og tóku
fleira. Óii Paiii
sladisk hljóm-
uyföi Dananum
en sagði svo:
:amir hafa ráð-
n. og eru nu á
tarinnar út er-
-í* ' \
. ' Y / ■ tQ k J J ** ^ £ * _ • / f , >
t ' * '•,S H
'.7 r
jll *
Gleráll ur sjó er sjaldgæfur og eftirsóttur
Fanaaði fyrstu
glerálana
Bjami Jónsson fiskifræðingur hefur fangað fyrstu gierálana sem náðst hafa í sjó
'hér við land. Glerállinn er eftirsótt vara til átu í Japan og eldis í Evrópu og leggur
sig á litlar 60.000 kr. kílóið.
„E g n á ð i 2 0 0 s tykk jum í h á f við ó sa
A iftá r á M ý ru m u m s íð u s tu m á n a ð a -
m ó t þ e g a r s tæ r s ti s t ra u m u r var. V ar
b ú in n að fa ra v iða u m la n d a ð le ita
f rá þv í í ap ríi í vor,“ seg ir B jam i. „Til
e ru sag n ir u m að g leráll h a fi sés t
vaða u m á v issu m sv æ ð u m Í v t t á tím -
u m . H in s v e g ar h e fu r verið ta lið að
ú tilo k a ð v æ ri a ð re k a s t á h a n n n ú til
dags í e in h v e iju m a g n i og é g h e f ver-
ið s p u rð u r h v o rt é g g æ ti ekk i ey tt
t ím a n u m í e itth v a ð b e tra e n svona
g rú sk .“
G le rá ll e r v e n ju ie g u r u n g u r áll á
le ið ú r Þ a n g h a f in u u p p í á r og v ö tn
og ta lið e r a ð sú fe rð h in g að tak i u m
3 ár. A ilinn h e ít ir ý m su m n ö fn u m
e ftir þvf á h v að a þ ro sk astig i h a n n er.
G le rá ilin n h e itir svo vegna þ e ss að
h a n n e r g læ r. Þ e g a r h a n n g e n g u r u p p
í fe rsk v a tn d ö k k n a r h a n n og h e itir þá
gu iáli. Ú tiitið b rey tis t e n n e r h a n n
v e rð u r k jT iþroska, e f tír að h a fa verið
í á n u m í 6 - 2 0 á r og k a lla st h a n n þá
silfu rá ll. Þ á b re g ð u r h a n n s é r tíl b aka
e f t ir G o ifs tra u m n u m til að a u k a kyn
s itt í K a rab ísk a h a fin u /Þ a n g h a fin u .
B jarn i seg ir b ú ið að eyðileggja b ú -
svæ ði á is v íð a o g e in s sé ofveiði á
h o n u m við s tr e n d u r EvTÓpu. E ld is-
" t : - ' r
f ’i '
V , fí i l
Bjarni Jónsson fiskifræðingur notaði há f
á gönguna við Álftárós.
s tö ð v ar í F rak k lan d i, H o lia n d i og
D a n m ö rk u k a u p i h a n n d ý ru verð í en
m e s t a f h o n u m sé b o rð a ð e in s h a n n
k o m i fy rir og þ á að a lieg a í J a p a n .
K íló íð fa ri á 6 0 .0 0 0 . k r., s am k v æ m t
n ý ju s tu t fð in d u m þ a ð a n o g h a fi
h æ k k a ð ú r 4 0 .0 0 0 á s íð u s tu tv e im u r
á ru m . E kki e r sk e p n a n stór, u m 7 sm
iö n g og e in s og sp ag h e tti a ð sver-
leika.
B ja rn i e r s ta r f s m a ð u r N o rð u r -
la n d s d e ild a r V e ið im á la s to fn u n a r á
H ó lu m f H ja ita d a l og e ftir lé t h iu ta
g le rá ls fe n g s in s á v a tn a iífs sý n in g u
sem s te n d u r yfir á H ó lu m . R es tin n i
f ó r n a r h a n n í þ á g u v ís in d a n n a .
„ S tæ rs tu r h lu t in n fe r tii r a n n s ó k n a í
J a p a n . Is la n d e r e in i s ta ð u r in n í
h e im ín u m sem evrópski og am erísk í
á la s to f iia rn ir m æ ta s t á og því v e rð u r
a th u g a ð h v o rt h é r h a fi verið kyn-
b le n d in g a r á fe rð . S íð an v e rð a tek in
u r þ e im e y rn a b e in sem n o ta m á til að
g re in a a ld u r þ e irra í d ö g u m og tím a -
se tja m y n d b re y tin g a r sem v e rð a á
þ e im á le ið yfir bafið . Þ e im upp lýs-
in g u m e r ek ld h æ g t að n á e ftir a ð ái-
lin n k e m u r í fe rskvatn ."
- E n telurSu líkur á að hægt sé að
veiða glerál í einhverju m agni hér við
land?
„Þ essi f u n d u r e r s te rk v ísb en d in g
u m a ð þ a ð sé m ö g u leg t. E f h æ g t e r
að Í ím ase lja g ö n g u r á h v e rju m s tað
e r a u ð v e it a ð h a n n a g iid ru r sem
h e n ta og ek ld e r vafi á að g leráli ú r
o k k a r h re in a u m h v e rfi se ld is t h æ s ta
verð i. Þ a n n ig að ég e r b ja rtsv n n ."
G L \ .
ALMANAK
Laugardagur 17. J l
191. dagur ársins-
27. vika. Sólris kl.
23.20. Dagurinn le
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14.00.
KROSSGÁ1
Lárétt: 1 íipur 5 kvenman
9 fen 10 hrelnir 12 óþurrk,
17 auðveídu 18 fisks 19 u
Lóðrétt: 1 ciafna 2 spii 3
6 gagniegir 8 saltíögur 11
15 sndlií
12 LAUGARDAGUR 17. J Ú L Í 1999 M ORGUN BLA ÐIÐ
FRETTIR
Gleráll, sem er í raun álaseiði, veiddist í fyrsta sinn í sjó við ósa Álftár á Mýrum
Japanir borga um
60 þúsund krón-
ur
GLERÁLL veiddist í sjó hér við
land í fyrsta sínn fyrir skömmu í
einhverju magni svo vitað sé. Gler-
állinn þykir mikil munaðarvara og
e r gríðarlega verðm ætur en um 60
þúsund krónur fást fyrir kílóið. Það
var Bjarni Jónsson, fiskifræðingur
hjá Veiðimálastofnun á Hólum í
Hjaltadal, sem veiddi um 200 gler-
ála í Alftárósum á Mýrum.
Gleráll e r í raun álaseiði en áll
gengur í gegnum m argar mynd-
breytingar á æviskeiðinu. Seiðin
berast hingað til Iands ú r Þanghaf-
inu svokalíaða eða Saragossahaf-
inu. Állinn elst siðan upp í
ferskvatni í 6 til 15 á r en gengur þá
aftur ú t í Þanghaf til hrj'gningar.
Evrópuállinn svokallaði berst upp
að ströndum allrar Vestur-Evrópu.
Hann kemur fyrst upp að strönd-
um Marokkó og þaðan með strönd-
inni alveg norður til Noregs, einnig
i.il Islands. G lerálarnir sem Bjarni
veiddi draga nafn s itt a f því að á
þessu æviskeiði eru seiðin glæ r og
gagnsæ, þannig að sjá má í þeim
innvdlin. Seiðin voru um 7 sentí-
m etra löng en Bjarni segir seiðin
engu að síður geta verið allt upp í
þriggja ára gömui.
Bjarni segir menn hafa^haldið
því fram að álagöngur til Islands
séu mun minni en á árum áður,
göngur ekki árvissar og það litlar
að nánast ómögulegt sé að verða
var við þær. „Menn hafa sam t mik- .
ið reynt að ná þessum seiðum og
komist næ st þvi með því að ná seið-
um sem hafa yerið nokkrar vikur í
ferskvatni. Állinn breytist hins
vegar ú r glerál í venjulegan ál um
ieið og hann kem ur í ferskvatn,
dökknar á örfáum dögum.
Bjarni segir vísindamenn ekki
hafa veitt glerál í sjó við ísland svo
vitað sé. Hann hefur
fylgst með glerálagöng-
um frá því í apríl og
reynt að tímasetja göng-
um ar með því að vakta
ákveðna staði. „Ég hef
farið víða um og aðallega
skoðað ósasvæði, einkum
á Suður- og Vesturlandi.
Eins hef ég skoðað svæði
á Norðvesturiandi. É g
náði um 200 fiskum ú r
einni göngu, einfaldlega
með því að nota háf.
Flestum var fómað í vís-
indaskyni en um' 50
stykki eru til sýnis á
vatnalífssýningunni á
Hólum. É g get vel
ímyndað sér að glerállinn
gangi hingað að iandinu í
talsverðu magni. Það er
hins vegar nánast ekkert
vitað um hvenær þessar
göngur koma. E n um leið
og upplýsingar fást um
hvert þæ r ganga, hvem-
ig og hvenær verður
kannski hægt að ná
þessu í meira magni.“
Mikil eftirspurn
vegna skorts
Á meðan állinn er ennþá á gler-
álsskeiðinu þvkir hann mjög Ijúf-
fengur og e r mjög verðmætur.
B jam i segir Japana veiða mikið af
glerál við strendur Marokkó, auk
þess sem hann sé veiddur mikið við
strendur Frakklands og Spánar.
„Glerállinn e r borðaður eins og
hann kem ur fyrir. Aðalmarkaður-
inn er í Japan og þar borga menn
upp í 60 þúsund krónur fyrir kOóið.
Kílóverðið var fyrir fáum árum um
40 þúsund krónur þannig að það
'
:< <*ZZZZ>
Hrygningarstöðvar álsins
Áiaseiði berast með hafstraumum upp að ströndum Evrópu úr
Þanghafi og kailast Gleráll þangað tii þau ganga upp í ferskvatnsár.
BJARNI Jdnsson
fiskifræðingur.
virðist vera skortur á glerál. Göng-
u m ar upp að ströndum Norður-Af-
ríku og Evrópu hafa farið minnk-
andi og því verður glerállinn sífeilt
eftirsóttari.“
Tveir stofnar mætast
á ísiandi
Bjam i segir glerálinn grundvöll-
inn að álaeldi. Hingað til hafi eng-
um tekist að klekja ú t ál í eldi til að
láta hann lifa. Glerállinn sé því eina
uppsprettan í eldi á íslandi.
GLERÁLLINN þykir iostætí í Japan og e r borðaður eins og hann
kem ur fyrir.
Áframeldi á ál þyki ekki eins hent-
ugt. „Eftir að hann gengur í fersk-
vatn koma í hann sníkjudýr og
fleira sem menn losna aldrei við.
Það e r heldur ekki hægt að fijtja
inn ál vegna sjúkdómahættu. En
auðvitað er m aður einnig rekinn
áfram af rannsóknaráhuga. ísland
er endastöö Evrópuálsins en hing-
að til lands kem ur einnig Ameríku-
áll. H ér e r því eíni staðurinn í
heiminum þar sem þessir ríæir
stofnar rnætast í náttúrunni og
jafnvel blandast. Það e r því for-
vitnilegt að skoða samspil þeirra.
Við munum meðal annars erfða-
greina þau seiði sem við náðum
með tilliti til þessa. Þá gefa kvarna-
sýni upplýsingar um hvenær þau
klöktust ú t og einnig er hæ gt að
tímasetja myndbreytingar á loið
þeirra yfir hafí.ð hingað til lancis.
Það er ekki hægt eftir að fískurinn
kemur í ferskvatn. Það eru bví
ýmsar upplýsingar sem við IVuun út
8 FISK IFRÉTTIR 10. september 2004
Gierálar veiddir með háfum.
Hrun i álastofninum veldur
miklum áhyggjumí Evrópu
— ESB hyggst grípa til fríðunaraðgerða og þörf talin á frekari rannsóknum hérlendis
eru að eiga sér stað á liafstraumum
í A tlantshafi samfara hlýnun jarð-
ar. Eöa jafnvel aö óþekktur virus
kunni að herja á stofninn.
Aö sama skapi hefur vcriö bcnt
á aö ekki hefur venö varað eins
sterklega við ofveiði á ál og öörum
tegundum og er það m.a. rakiö til
vanþckkingar á lífsháttum tegund-
arinnar. All þykir herramannsmat-
ur og er hans ncitt á margvíslega
vegu. Hann er t.d. grillaöur og
reyktur viöa í Evrópu. Jafnvel gler-
állinn er notaður í forrétti eins og á
Spáni. í Japan þykir áll einnig mik-
ið lostæti í sushi réttum.
ESB íhugar aðgerðir
Evrópusam bandið mun íhuga
aögerðir í haust til verndar álnum.
enda efast fáir lengur um aö hrun
hafi átt sér stað. Spurningin um
hvaö eigi lil bragðs aö taka hefur
hins vegar vafist lyrir stofnunum
ESB. Sérfræöingahópur hefur þó
lagt til aö veiöar á uppvaxandi ál
veröi bannaðar meö öllu. Einnig að
tekinn veröi upp sérstakur skattur á
glerálsveiðar. Hins vegar cr Ijóst aö
þaö mun valda togstreitu á milli
ríkja í Norður- og Suöur-Evrópu,
en gleráll er einkum veiddur viö
Spán Portúgal og Frakkland á meö-
an norðlægari þjóöir leggja áherslu
á veiðar fullvaxins áls. Einnig
valda m ism unandi reglur innan
landanna vandræðum auk þess sem
mjög mism unandi aófcrÖum er
beitt við veiðarnar eftir löndum.
Hrun viröist hafa orðið í álastofninum sem veiðst hefur í töluverð-
um mæli við strendur Evrópulanda. Bjarni Jónsson, fiskifræðingur
og deiidarstjóri norðurlandsdeildar Veiöimálastofnunar, segir Ijóst að
þessar fregnir vti enn frekar undir nauðsvn þessa að rannsaka betur
útbreiöslu og stofnstærö áls í íslenskum ám og vötnum. Ekki sist í
ljósi hugmynda manna hér um veiðar á glerál til áframeldis og eld-
istilraunir sem veriö er að reyna að setja í gang.
Samkvæm t erlendum fréttum
telja hollenskir líffræöingar Ijóst aö
álastofninn á í miklum erfiðleikum
og veldur þaö óvissu um framtíð
25 þúsund álaveiðimanna í Evrópu.
Einnig er mikil óvissa um afdrif
þeirra stofna sem lifa á þessari
fisktegund sem líkist meira slöngu
en fiski. Jafnvel er taliö aö hefö-
bundnar álaveiöar muni líða undir
loka á næstu þrem árum.
Hefur rannasakað
ál síðan 1999
Áll fellur ekki undir Hafrann-
sóknastofnun eins og flestar aörar
fisktegundir í hafinu við landiö,
heldur undir Veiðimálastofnun og
þá um leið landbúnaðarráöuneytiö.
Bjarni Jónsson hefúr stundaö víð-
tækar rannsóknir á gönguhegöun
og göngustærðum áls hingaö til
Iands frá 1999. Heflir hann veitt ál
á um 25 stöðum víóa um land og
hélt hann erindi um ál á alþjóölegri
ráðstefnu á Hólum fyrir skömmu
sem fjallaði m.a. um fiskilíffræöi,
fiskveiöar og fiskveiðistjórnun.
B jarni segir þó Ijóst aö minni
göngur hafa verið a f ál hingað til
lands síðustu tvö árin en næstu ár
þar á undan. Hann segir fréttir a f
hugsanlegu hruni álastofnsins
vissulega valda mönnum áhyggjuin
enda er um sameiginlcgan stofh aö
ræða hjá mörgum þjóðum. Hins
vegar sé ekkert í hans rannsóknum
hér á landí sem bendi til algjörs
hruns og því fuli ástæöa til aö halda
áfram frekari rannsóknum og áætl-
unuin um tilraunaveiðar- og eldi.
Eldi byggist á veiðum
á glerál
Áframeldi byggist á veiöum á
glerál (sciöum álsins) sem gengur
upp i ferskvatn allt í kringum land-
iö. cn þó mest á Suöur- og Vestur-
landi. Hitastig ferskvatns í ám og
lækjum hefur afgerandi áhrif
hvenær áliinn gengur upp. Scgir
Bjarni aö þegar vori vel cins og í ár
þá sé hann t.d. mánuöi fyrr á ferö-
inni en clla.
Bannaó er aó flytja inn glcrál til
áframeldis vegna hættu á im'.IIutn-
ingi smitsjúkdóma og sníkjudýra
sem finnast á uppeldisstöðvum í
Evrópu.
ÁUinn á dularfullan lífsferil og
hefur tekist aö lifa a f í ám cg í ála-
eidisstöðvum, þrátt fyrir mikla of-
veiði og þá staöreynd aö víöa hefur
verið gcngiÖ á náttúrulegar uppcld-
isstöðvar. Þrátt fyrír allt hefur tek-
ist frani á síÖustu ár aö halda uppi
veiðinni meö þeirri endurnýjun
sem ungur gleráll hefur skilað úr
hafinu og upp í ár og læki. Ekki
hefur hins vegar náöst árangur í að
klekja út áli í eldisstöðvum og hafa
lirfur úr slíku klaki aöeins lifað í
skamman tíma.
1% af fyrri stofnstærö
Nú er hins vegar svo komið aó
hrun viróíst hafa oröiö í nátlúru-
lega stofninum a f óútskýröum á-
stæöum. Fjöldi einstaklinga í
stofninuin haföi samkvæmt frétt-
um fallið niöur í 10 próscnt a f fyrri
stofnstærð á síðustu 50 árum. Nú
eru þessi tíu prósent taiin koniin
niður I 1 prösent. AÖ sama skapi
hefiir verö á glerál þrefaldast á síö-
ustu þrem árum, eða í 325 dollara
pundið (um 650 dollara kilóiö).
Hluti skýringarinnar er aö mati sér-
fræðinga sú aö gríðarleg ásókn hef-
ur vcrið í glerál vegna stóraukins
álaeldis. Á sama tíma hafa oröið
breytingar á náttúrulegum Iífsskil-
yrðum áls í hafinu sem eru vís-
indam önnum cnn ráðgáta, en
hrygningarstöðvarnar eru t Sara-
gossohafinu. Hafa sumir vísinda-
menn giskaö á að orsakanna kunni
aö vera að leita í breytingum sem
Bjarni Jónsson n.skifræðingur.
Morphological variability in Icelandic eels
effects of habitats and genetic origin
Caroline Denis and Bjarni Jónsson
Veiðimálastofnun Norðurlandsdeild, 551 Sauðárkrókur. caroIine_denis@hotmail.com
VTiiÐ'IMA LAS’f'OfNlJK
Introduction
T hc &eshwaler ecis o f thc gcnus A ngu illa have uxtique characters such á s a catadrom ous lifc h istory strategy, a long
spaw ning m igration a n d a long leptocephalus larval pcriod (W atanabe. 2003). They spcnd m ost o f their lii'e in
frcshw atcr, bu t undertake a long m igration to the open O cean, andm ore . prccisely to ihe Sárgasso Sca, to spaw n (TCsch,
1977). Rccently il has a lso been found that som e eels caugh t in the open ocean havc apparcntlv nevcr entercd
frcshw atcr, bu t spént thc ir cntire grow th phase m the m arine environm ent (lsu k a m o to e t a t , 1998). Differences in
leng th an d a g c betw ccn scxcs scem s to bc urii\,ersal and occur in a ll species o f the genus despite the ir
geographic ex’tent. Pooic and Reynolds (1996) Ariother differcnce betw cen sexes is thc tendéncy for num bers of
fem ales lo decrcase w ilh distance ypstream from the sea. Oliveira e t at. (2001). (
In this sludy, m otphologic and lifo history difterences be tw een eels ong iná ting frora tlirce different habituts were
observcd. Sam ples w ere taken from a lake, tw o sfream s a n d a m a'rinc site in lcelarid Thc ítrs t objective o f the study
w as to determ ine if eels bclonging to different hab itats a rc charaetenzed by different life h isto iy traits. A t the same
tim c, dilierences in lifc h istm y traits bctw ecn sexes are observed. A secprid objective is-to' chcck if th c num ber of
fcm ale eels indeed decreascs w ith d istance upstream from the sea. A th ird a im c o n s ís ts o f detcrm iriing if it isp o ss ib lc to
distinguish betw een eels originating l'rom different habitats merely on th c b a s is o f morphological traits. A nd i f so,
whicfa charactcristics a re m o st úscful. A nothcr section o f this study is cdncem éd w ith com parison w ith the hybrid foriris
o f A m crican (A. rostrata, 103-111 vertebrae) a n d E uropian (ri. auguilla , 110-119 vertebrae) eels occiuing in leeland
(A lbcrt c t al. in prep.). For tliat purpose w c used data from a gcnetic study, conducted on dte sam e sam plcs.
Ásgautsvatn Grafarvogur
■ ^ L
Material and Methods
Sampttng
Altögcthcr 173 ccls werc cxamincd in this study. origmating from four locations in Iccland. With the cxccption o f Borgarlœkur, ut
lcast 50 individuals werc samplcd pcr Iocation. Thrcc typcs o f habitnts wcrc samplcd for the study: a lake, rcprcscntcd by a sampic
from Ásgautsvntn. StokkseyTÍ (N “56). Two strcam popuialions. onc fróm Bár. Gnindarfirði 04"52) and a sccondi smaller one. Iroht
Borgarlœkur. Mýrum (N“ I5), nnd mannc sample collcctcd in Grofarvogur, Rcykjovik (N“ 50). Bccnusc thecclspccimctts from the
Bár populotion wcrc locking both o f thcir ííns os they hodbeen removcd forgcnclic anolvsis. ítw as impossiblc to mcasurc ali troits.
Thereforc thcy wcre excludcd from ccrtain anolyscs. To cncountcr this technical probiem. thc Borgorlækur, unothcr strcam
population was included in thc anolysis.
Life history
Ali indívidúals wcrc mcosured to thc noarcst 0 I cm (totol Icngth) and weiglicd to tlic ncarcsL 0 .1 g (body wcight), and the Fuiton's
condition tudcx colculatcd ns follows: rulton's CI ” 10ÓOx(Wí'L?). Gonnds wcrc cxamincd ttnd wcighcd to the ntsarost 0,1 g
(gonadal wcight) to dctcrminc scx and maturity stalus. BeCouse ofthe prescncc o f undifferéntiatcd cels in the samplcs. it wus not
always possible to dctcrminc sex. A onc way ANOVA vvas uscd to dcterminc ifthcrc vvcre significant diffcrenccs m mcun totnl
length, body woight and condition indcx botwccn habitats. Post hoc pair-wisc comparisons o f snmple mcans wcrc porformcd with
Bonforroni adjustmcnt. Anulogous tcsts wcre conducted for cbmparison bctwrcn. hybrids arid coinptmson bctwccn scxcs m thc
stream population. To test thc nuli hypbthcsis tlmt ntalcs and fcmalcs oocurm Ihc samc proportions among habitats, a j ?
contingency tablos wris used.
Morphology
Morphometric measuremcms werc takcn with a vcmicr calipcr. Twcnty cxtcmal mcasurcmcnts vvcre made on thc loft side ofcach
fish. Mcasurcd are the pósitioas o f thc fins: thc dorsal tin (prcdorsal lcngth). thc annl ftn (prcannl icngth) and Ihc pcctoral fm
(prcpcctoral lcngth). Only for thc pectoral fin dve lcngth and hcight are mcasurcd (pectoral fui length and pcctoralfin hcight
rcspcctivcly). With respcct togcneral bodv form, body hoight and width vvcrodctormiricd at twodiffcrcnt spotsori thccel: a tthc
beginning o f thc dorsal fin and at V4 6f thc annl fin (body hcight and width at dorsal lin and body hcigln and width nt 'á ánal fin).
Eyc size is another important trait. Thorcfore both diametcrs arc mcasurcd: thc smnll onc (oyc diamcter vcrtical) and thc largc onc
(cyo diamctcr horizontal). Also thc distancc bctwocn thc cycs as wcll as thc distnnco bctwocn thc most distal margins of thc cyes
wcrc mcasurcd. pcrpcndiculítr to thc body axis (orbital distnnce betvvccn eyosand orbital distancc on thccyc). Position ofthceves is
dctcrminod by thc snout-cyc length, vvhich is thc distnnce from thc tip o f thc snout tothcm ost distal morgin o f thc cycs, and tho
postorbital-pcctoral fin icngth. Tltc rcmaining characteristics arc rélated to thc licad shapc: mnximal head widtli (hcad widlii max).
The hcad hcight is mcasurcd at tvvo spots: ni thc maximal hcad width nnd at tlic cnd o f the muxillae (hcad hcight at head width mux
and hoad hciglitat maxiilue). Lcngtli isdclcrmincd forboth uppcrand lowerjaw. Mcasurements vvcrc repeatcd tw iccon 15fish to
assess rchubility, Repcatcd moosurements differed 0.,9 -9,4 %, dcpcnding on tho size o f tlie ciiarnctcr involved. ANÖVAwas usod
to tcst vyhcthcr morphological traits diffcrcd botwccn hubituts. Anulogous ananlyscs vvcre run to usscss dilTcrcnccs among scxcs and
among hybrids. When ricccssary apo.it hoc pair-wisc comparison was conductcd by usmg Bonfcrrotu adjustment. For. these analyscs
data wero sizc-adjustcd by using thc rcsiduals of the variablc regressed againsf towl Icngth. Ovcrall pattcnis o f morphological
varintion was asscsscd with principal componcnt arudysis and discrimmant analysis. Thcse tcsts wcrc also based upon thcsize-
adjustcd datu. Analyses wcredonc using thc SPSS software packngc wilh a diiTcrcncc vvith p-vaiuc of < 0,05 considercd significant.
A lcristtc counts
ln ordor to distinguish fishes of thcdiffcrcnt spocics o f AUnntio cels (A. m guiU a and A. rostrata) tuid the hýbrids betwccn thcsc tvvo
specics. it ís vcry cbnvenicnt lo count tiie numbcr o f vcrtcbrac. The vertebrae counts arc niadc from thc barc spmal columit. A
gcnctic study (Vioky Albert ct nl in progress) conductcd on thc sante samplcs madc a coiriparisoit possible. Thcsc gcnelic rcsults
were rathcr analogous but contained more information. Thcrcforc somc groupings in thc statistical analyses vvcre based on thesc
gcnctic rcsults. On the basts ol thc mcnstie cburits aiid the rcsults b f thc gcnctic study.it vvas possible tíj cotnpore thc mCristic counis
bctvvecn thc hybrid types and run an ANÖVA on thcm. Thís arialysis was doric to súbstantíafc thc mtcrpretatton ofthc mcristic
counts nmong thc hybrids
Frequency dlagramTotal lengtti
Figurc Ib Frcqucncy diagrarn oflotul lct
Acknowledgements
Wc thank Páll V. Kolka Jónsson. Evgcnia Ilinskaia. Katrin Kolbcinsdóttir mid
Eik Elfarsdóttir for valuablc hclp at diftcrcni stagcs o f this work.
Olivcira, K.,McClcavc. J 13. mid Wippclhmctcr, C.S (2001)Kcgtonal vanauou .1111] lliccfTccIol
lokc nwr nrca on sex dintnbulion of Anicncmi ccls Jountal of Fijh Biology. 38:9-13-93
Poolc.VVR nndKcynolda, J.D.(1996)Growthrntcandiqtcntnugrdtion of/VngiuUa anRuilla.
Joum.il o/Flih Blology.Aa 633-642
Tcrch, F W (1977) Tht.
Tsokumolo.K ehtl (199S)Donll frcshv
Wutnnutw, S, (2003) Taxonomy of Ihc frc
Figurc 2 PCA PC-scorcs for ccls from thc thrcc habilat lypcs, tndtcatcd urc thc mcons
of thc dtlfcrcnt hobitat lypcs, with stondord dcvintion Dota on 16 vttnnblcs ndjuslcd
for toUtl lcngth (by unstondardizcd rcstduals) tn ccls bclongmg to thrcc diflcrem
habitnt tvpes (N-163)
Results
T he exccssive am ount o f fem ales p resenl in the w ho le sam ple is rem arkablc. O u to f the 126 eels o f w hich the sex could be
ascerlained, 119 tum ed ou t to be fem ales (94% ); N o m ales w ere observcd am ong tlie eels sam pled in.the lake or marine
habilat, und onlv 7 b f 31 eels exam ined from thc s tteám population w erc m ales. A X :-tesl revealed a signilicant difterencc hi
séx disfributiori am óng habitalsv vvitli tlie streám populatioiis deviating frorit th e others (X : =0,000).
Fem ale eels o f thé stream population are sm a lie rthan those o f th e o th c r habitats. Fem ale cels o f the m arine population are
w ay larger than the otliers ((F=32,098; p=0,00Ó), ftgurc la a n d Ib). Total length for fem ales w as significantiy diflerent
betw een hab itats (F=32,098; p=0;000) N o signilicant diflerences w ere found in total length betw een the sexcs in the strcam
poþululion (F=0,539; p=0,469). Analogous resu ltsw ere found for tlie weight o f thcee ls : a m irum al m ean valuc o f 52,8 g '
w as o b se rv e d in th e strcam population, an interm cdiatc 155,5 g in th c la k e popula tion and a m axim al m ean value o f 313,2 g
in the m urinc sité,
O nly sligh t non significant diflérence w as found in Fu lton’s condition index betw een eels occunng in lakes (C Í=1,556) and
stream s (C l= l ,401). However, these values a re sm aller than th e m ean condition index for eels frora. thc m arine site
(C I= 1.858, AN OV A , (p=0.000 and p=0,000).
U niyariate analysis o f mbrphom efric characters prbduced only significant differences in three ad justed character m cans
bctvvecn populations afler Bonferroni correction for repeated tests. They w ere prepectoral length, length o f the upper jaw
a n d len g th o f the low er jaw. A com parison betw cen luko and s iream popula tions show od the highest num ber o f signiticaiit
differencés in ad justed character m eans (10 ou t o f 20 traiLs). C öm parisón betw een lake and m arine site gives n s e to seven
significant d iðe rö tces in ad justed character m eans and by com paring thc stream w ith the m arine site only five adjustcd
charactere w ere significantly diflérent (table 1). For the stream population it w as possible to com pare the twenty
morphom etric traits am ong sexes. O nly tw o ad justed characters w ere significariffy diflerent betw cen m ales and fem ales, thc
body height a t '/; o f Ihe anal fin (F=5,258; p=0 ,029) und ihe body w id th a t '/: o f th e an a l fin (F=10 ,103;p= 0 ,004).
In Principal Com ponent A nalysis (figure 2 ), 46 .9% ö f the varialion w as cxplained by the first P C A ax is and 18.6% by the
second prineipal com ponent (a second PC A w as a lso run on on ly three o f th e popiilations; A sgautsvatn, B orgarlæ kur and
Grafarvogur, w hich did no t have m issing variab les, table 2). Tlic firsl p rincipal com ponent produccd á h igh positive loading
for predorstil lengih and preanal ienglh. 'l lie re w as a rathcr higli ncgativc load ing lb r body hcight a t dorsul fin. The second
ax is had higli positive louding for p reanal lengtli a n d negalive Ioading for p redorsal length (tablc 2). Thc differences in
m ean scores betw een hab itats were highly significant to r the first PC A (p=0.006) cven w hen w e addcd thc hvbrid sla tus a s a
covariate. B u t in th e lattcr case the hybrid s ta tus itse lf and thc interaction factor w cre not significant (p=0,223 and p=0,607
respcctively) so there w as no interactíon betw cen hab iiat and hybrid sta tus. N either w as therc a significant difference in
m ean scorcs betvvcen scxes (p=0,892) or hybrids (p=0,075) for the first principal coinponcnt. T he four variables, cxcluded
íri th e first unalysis, scem to bé ra ther im portant as revealed by variable loadings in the principál Com pönent A nalysis on the
second sct o f dala (table 2).
Significant correlations w ere found in D iscrim inant A nalysis for botli the first and second function (0,744 p<0 ,000 and
0,433 p=0 ,007 respcctivcly). L ow er jaw , head heigh t u t m axillae and body w id th a t dorsal lin had the h ighestpositive
coeflicients' for the f irs t lunction and body heigh t á t A o f the anal fin, m axim al head vvidth and prcanal length the highest
negátive cocflicients. F o r thc secorid function, upþer ja w lerigth vvith a high negalive coeflicient secm s to play án miportant
ro le in discrim inating bctw een the g roups (tab le 3, figure 3): C lassification accuracy w as m odestly good, w ith 78 .6% o f the
lake population, 57 .9% o l' tlie stream population á n d 50% o f Ihe m arine eels correctly c lassified to the ir respective habítaLs.
Thc num ber o f vertebrae is shovvn in figurc 4. The E uropean éels (A nguilla anguilla) in our sam ple were characterised by a
b road rangé o f vertébrae m uriber (104-118). T hé F í hybrids h a d a significanúy different ran g c (þ=0,000) w h ich covers
sm aller am ounts o f vcrtebrae (103-111), corresponding to the vertebrae num ber o f A m crican eels (Anguilla rostrala ). Thc
F2 hybrids hud an intem icdia te range ( 1 10-137), and vvere significantly different from the F 1 hybrids (p= 0 ,001) bu t no t
from Lhe A . auguilla (p= 1,000).
Tablc 3 Cocflicicnls from ciu
for Ihc powcr of Ihc discnmmt
Uimbda. df imd p-valuc.
ihcm for cach habilal lype (rcd signs)
Conclusions
Atlantic eels in Iceland are predominantly females in all habitat types, with males
being best represented in streams. Eels from the marine habitat were the largest
and had greater relative weight than eels from other habitats examined.
Differences were observed in morphology between eels from altemate habitats,
both in individual characters and Principal Component and Discriminant Analysis.
Eels could to some extend, be classified to tlieir respective habitats based on
overall morphology.
F1 hybrid eels were found to have intermediate vertebrae counts in comparison
with Europian and American eels, while F2 hybrids and higher, had vertebrae
counts similar to that o f Europian eels.
This study reveals strikingly different life history strategíes among Atlantic eels in
lceland, compared to what has been reported for the species. Further, eels appear
to display great flexibility in adjusting their morphology in response to the habitats
they are residing in.
mailto:caroIine_denis@hotmail.com
Miðvikudagur 10. mars 2004 B a e n d n b l a ð i ð
Bjarni Jónsson fiskifræðingur
Állinn er aufilind sem
baendur getn nýO sér
Fyrir skom m n var skýrt frá svari landbúnaöarráðherra á Alþingi við
fyrirspurn Ö ssurar Skarphéðinssonar um álaveiðar og álaeldi hér á
landi. Svar ráðherra var að m estu byggt á þeim rannsóknum sem
B jarni Jónsson, fiskifræ ðingur hjá norðurlandsdeild Veiðim ála-
stofnunar, hefur unnið að í nokkur ár en hann er sá sem m est hefur
stundað vísindalegar rannsóknar á ál hér við land.
Bjarni sagði í samtali Bbl. að
rannsóknir hans hefðu leitt í ljós
að talsverðar göngur gleráia, sem
eru seiði ála, séu hér til lands og að
þeir umhverfisþættir sem ráða
mestu um göngur þeirra séu
sjávarfoll og vatnshiti. Unihverfis-
þættir ráða mestu um hvort gler-
áliinn verður karlkyns eða kven-
kyns. Hér við land er það á þann
veg að mikill meirihluti gleráls
verður hrygnur. Þaer vaxa betur og
verða stærri en hængurinn og
verðmætið er meira. Hann segir að
viðast hér á iandi sé hiutfall
hrygna óvenjuhátt. í S-Evrópu er
umhverfisþátturinn á þann veg að
meirihluti glerálsins verður hæng-
ar sem eru ekki eins hagkvæmir í
eldi og hrygnan.
lækjtun og
vötnum.
Nú er
komið í
ijós að það
er hægt að
stunda
álaveiðar í
sjó hér við
land sem
er þá bara
viðbót við
þá auðlind
sem állinn
er í ám og
vötnum,
þ.e. á! sem dveiur allan aldur sinn í
sjó. Ég tei hiklaust að þarna séu
komnar umtalsverðar sti'andnytjar
fyrir bændur sem land eiga að sjó
og eiga strandlengju sem gefur
kost á áia-
veiðuin. Sömu sögu er að segja af
álaeldi sem líka getur orðið
umtalsverð aukabúgrein en það
byggist á því að veiða glerála og
ala þá áfiam. Það hefur einnig
koniið í ljós að hér við iand mætast
Evrópu-áll og Ameríku-áll og er
það eini staðurinn í heiminum sem
það gerist. Það hafa meira að segja
fúndist kynblendingar þessara
stofna hér við landið og standa yfir
rannsóknir á þeim," sagði Bjarni.
Hann segir að rannsóknir sínar
hafi byrjað á glerálarannsóknum
árið 1999 vestur á Mýrum og voru
það fyrstu vísindasýni af glerál
sem hafa náðst hér við land. Upp
úr því fór hann að kortieggja
göngu gleráls til að fá yfirlit yfir
útbreiðslu hans við landið og
gönguhegðun. Næstu ár á eftir
segist hann hafa vaktað ákveðna
staði við landið á vorin og fram-
kvæmt mælingar á glerálnum og
rannsakaði umhverfisþætti. Hann
segist hafa veitt glerál á 17 stöðum
á svæðinu frá Stokkseyri að
Barðaströnd og eftir því sem þekk-
ing og kunnátta eykst veiðist meira
af glerálnum.
Síðan byrjaði Bjami í fyrra á
nvju rannsóknarverkefni varðandi
sjávarálinn og útbreiðslu hans um-
hverfis landið rneð nytjar í huga.
Hann hefur veitt sjálfur og fengið
fólk til að veiða fyrir sig allt í
kringum landið og komið hefur í
ljós að ái er að finna í öllum lands-
hlutum. „Það kom mér á óvart
hvað veiddist mikið á ákveðnum
Vœnleg búgrein
„Þegar horft hefur verið til
áiaveiða hér á landi fram að þessu
þá hafa menn aðallega veitt álinn í
Þessi áll veiddist i Elliðaánuni otj
var 84,5 sm og þyngdin var 1,3 kg!
Myndin birtist í bókinni Fiskar í ám
og vötnum, sem Landvernd gaf út
1996.
stöðum og eins
iivað állinn er vænn víða við
landið sem heigast af þvi að
hrygnur eru í miklmn meirihiuta
hér sem fyrr segir," sagði Bjarni
Jónsson.
5
Fyrirhugaðar eru endurbætur á aðstöðu fyrir ferðamenn við
Seljalandsfoss. Umhverfisfulltrúi Ferðamálaráðs hefur unnið með
Náttúrustofnun og sveitarstjórn Rangárþings eystra að þessu máli og
munu teikningar af svæðinu vera tilbúnar. Ágúst Ingi Ólafsson,
sveitarstjóri Rangárþings eystra, segir að ekki sé búið að ganga
endanlega frá samningum um hve mikið verður gert á svæðinu enda
málið enn á hönnunarstigi. Aöspurður um hvaöa endurbætur menn
séu helst aó tala um sagði hann að það væri að koma upp
hreinlætisaðstöðu og að lagfæra göngustíga. Bætt aðstaða fyrir
ferðamenn til að borða nestið sitt væri líka inni í myndinni.
10 SUN N U D AC iU K 12. SK I ’T K M IÍE K 1 >!')!) M O KG U N B L A D ID
Veiðistaður glerála í sumar, nærri ósum Álftár á Mýrum.
Glerálar gætu
verið gullnáma
Framboð á glerál til eldis hef- Mýrum og telur útlit fyi*ir að
ur ininnkað verulega síðustu hér á landi séu góðir mögu-
árin og eftirspurn, og þar með leikar að veiða glerál í því
M D l’/ í l r \ m l r i r í n n n f i l o O m V *rnm i o m n r rm ’ o / í r«*n rvvi o/x i F 1.* »
Gleráll í prófíl. Haiui er svo gegnsær að sjá má líffæri hans. Úr nálægð má sjá hjartað slá.
Glerálar í lófa vestur á Mýnun.
ál frá árí til árs. í bók þeirra Guðna
Gudbergssonar og Þórólfs Antons-
sonar „Fiskar í ám og vötnum“ segir
frá því að fiski hafi verið eytt í
Vatnsholtsvötnum á Snæfellsnesi á
ái’unum ÍDG2 og 19C3. í bókinni
steiulur þetta: „lteyndist þá vera 9,7
kg á hektara af ál í öðru vatninu, eða
74% af heildarfiskmassanum og 57%
í hinu vatninu. Sjálfsagt er því áll oft
vanmetinn meðal ferskvatnsfiska
hér á iandi.“
í bókinni er einnig úttekt á nýt-
ingu á ál hér á landi til þessa. Þar
stetidur: „Gömul hefð var fyrir nytj-
un á ál í Lóni, Nesjunt og Suður-
sveit. Þegai’ þar var dregið fyrir sil-
ung og kola í ísöltum lónum veiddist
alltaf töluvert af ál samhliða. Var
hann nýttur til matar, nýr eða
reyktur. Roðið var verkað sem
þvengjaskinn í skó og þótti sterkt
og irtjúkt. Eftir að lagnet urðu alls-
ráðandi við silungsveiðar hætti áll-
inn að veiðast.
Upp úr 1960 voru gerðar tilraunir
íil að nýta ál betur hérlendis. Arið
1961 veiddust 15 tonn af ál víðs veg-
ar um landið og var hann fluttur lif-
andi til Hollands. Árið eftir var út-
hlutað álagildrum til þeiira sem þá
veiði vildu stunda. Hollenskur :íla-
veiðimaður kom til leiðbeiningar og
v;u- áætlað að veiðast myndu 100
tonn. Ehinig var byggt reykliús í
Hafnarfirði eftu- hoilenskii fyrir-
mynd. Aldrei veiddust nema 17 tonn
það árið og fór minnkandi næstu ár.
Einnig lækkaði ineðallengd veidds
áls íu-att þessi ár og bendir það til
þess að veitt hafi verið ofanaf stofn-
inum, endurnýjun hafi ekki verið
nógu lu-öð og vöxtur of hægur til að
mæta þessum veiðum.“
M ögiileikariiir
I> i . > ; n n m ’ M k n f : < U A n nH
Upp úr 1960 voru
gerðar tilraunir til
að nýta ál betur
hérlendis. Árið
1961 veiddust 15
tonn af ál víðs veg-
ar um landið og var
hann fluttur lifandi
til Hollands. Árið
eftir var úthlutað
álagildrum til þeirra
sem þá veiði vildu
stunda.
og komist að því að ál er nánast alls
staðar að finna. Hvað þarf að gera?
Það er mikilvægt að slá ekki slöku
við, halda áfram á þeirri braut sem
mörkuð er, skipuieggja, tímasetja
og staðsetja göngutíma glerála efth-
því sem það er hægt. Þessar veiðar
eru afar tímabundnai- og getur tím-
inn breyst. Þó ég hefði náð þessum
álum vestur af Mýrum kom ég víða
við og veiddi ekki neitt. Það er því
ekki á vísan að róa og enn spurning
um hvert magnið er.“
En bandir eitthvað til að magnið
sé nægilefrt til uð garu ínegi glerúla-
veiðar að arðbærri a tviiinugrein hér
á landi?
„Já, það eru góðar vísbendingar
um það.“
Háar fjárhæðir
u i „m ...i ,„i„
íf;BÉTTII '
Mögulegt að stífla Jökulsá
í Ftjótsdal neðar í farveginui
28 milljarða
í fómarkostn-
að vegna
Eyjabakka?
Það er tæknilega mögulegt að stífla
Jökulsá í Fljótsdal við Hrakstrandar-
foss, nokkrum km neðar en nú er gert
ráð fyrir. Sá kostur hlífir Eyjabökkum
en er tvöfalt dýrari en núverandi til-
högun Fljótsdalsvirkjunar. Helgi
Bjarnason sagði Rögnu Söru
Jónsdóttur nánar frá kostum og
göllum tilhögunarinnar.
LA N D SV lItK JU N hefur tekið virkjunar er 210 M\V en yrði
tii athugunar hugmynd H elga rúm 180 MW sam kvæm t þess-
H allgrím ssonar náttúrufræð- ari hugmynd. Þær aðveitur
ings um tilhögun Fijótsdals- sem fyrirhugaðar eru ásamt
virkjunar sem fram lconi í Eyjabakkalóni eru einnig inni í
Morgunblaðinu fyrir skömmu. þessari hugmynd.
1 viðtali við H elga Hallgríms- Helgi Bjarnason segir að-
son í Morgunblaðinu kvaðst spurður að helsti ókostur um-
hann telja nauðsyniegt að slá ræddrar hugmyndar sé kostn-
af kröfura um hagkvæmni aður. „Stofnkostnaður virkjun-
virkjunarinnar til þess að arinnar yrði um 46 milljarðar
mæta verndarsjónarmiðum. króna sem er nálægt tvöfalt
Benti hann á tillögu sem hann meira en kostnaður núverandi
sagðist hafa bent Landsvirkjun tilhögunar, sem nemur 23 millj-
á en ekki fengið svör við. Fólst örðum króna. Magn efnisins
hún í því að stífia Jökuisá í sem þarf í stífluna er helsti
Gloiáll í prófíl. Hami er svo gegnsæ r að sjá má líffæri lians. Úr mílægð má sjá hjartað slá.
ál frá ári til árs. í bók þeirra Guðna
Gudbergssonar og Þórólfs Antons-
sonar „Fiskar í ám og vötnum" segir
frá þri að fi ski hafi verið eytt í
Vatnsholtsvötnum á Snæfellsnesi á
árunuin 1952 og 1963. I bókinni
stemlur þettíi: „lteyndist þá vera 9,7
kg á hektara af ál í öðru vatninu, eða
7-1% af heildarfiskniassanum og 57%
í hinu vatninu. Sjálfsagt or því áll oft
vanmetinn meðal ferskvatnsfiska
hér á landi."
í bókinni er einnig úttekt á nýt-
ingu á ál hér á landi til þessa. Þar
stendur: „Gömul hefð var fyrir nytj-
un á ál í Lóni, Nesjum og Suður-
svoit. Þegm’ þar var dregið fyrir sil-
ung og kola í ísöltum lónum veiddist
alltaf töluvert af ál samhliða. Var
hann nýttur til matar, nýr eða
reyktur. Roðið var verkað sem
þvengjaskinn í skó og þótti sterkt
og mjúkt. Eftir að lagnet urðu alls-
ráðandi við silungsveiðar hætti áll-
inn að veiðast.
Upp úr 1960 voru gerðar tilraunir
til að nýta ál betur hérlendis. Árið
1961 veiddust 15 tonn af ál víðs veg-
ar uin landið og var hann fluttur lif-
andi til Hollands. Árið eftir var út-
lúutað álagildrum til þeiira sem þá
veiði vildu stunda. Hollenskur ála-
veiðimaður kom til leiðbeiningar og
var áætlað að veiðast myndu 100
tonn. Einnig var byggt reykhús í
Hafnai-firði eftir hollenskri fyrir-
mynd. Aldrei veiddust nema 17 tonn
það árið og fór minnkandi næstu ár.
Einnig laéickaði meðailengd veidds
á/s hratt þessi ár og bendir það til
þess að veitt hafi verið ofanaf stofn-
inum, endurnýjun hafi ekki verið
nógu hröð og vöxtur of hægur til að
mæta þessum veiðum.“
Möguleikaruir
D{n m ; nrvrmn nil Irnm.'A U ..T , ( 1,’/,n n.1
Glerálar í lófa vestur á Mýriim.
Upp úr 1960 voru
gerðar tilraunir til
að nýta ál betur
hérlendis. Árið
1961 veiddust 15
tonn af ál víðs veg-
ar um landið og var
hann fluttur lifandi
til Hollands. Árið
eftir var úthlutað
álagildrum til þeirra
sem þá veiði vildu
stunda.
og komist að því að ál er nánast alls
staðar að finna. Hvað þarf að gera?
Það er mikilvægt að slá ekki slöku
við, halda áfram á þeirri braut sem
mörkuð er, skipuleggja, tímasetja
og staðsetja göngutíma glerála el'tir
því sem það er hægt. Þessai- veiðar
eru afar tímabundnar og getur tím-
inn breyst. Þó ég hefði náð þessum
álum vestur af Mýi-um kom ég víða
við og veiddi ekki neitt. Það er því
ekki á vísan að róa og enn spurning
um hvert magnið er.“
En benclir citthvað til að magnið
sé nægilcgt til að gera megi gleníln-
veiðar að arðbærri atvinnugrein bér
á landi'!
„Já, það eru góðar vísbendingar
um það.“
H áar fjárhæðir
u i ......... , , ...t , i., í i,
FRETTIÍFl
Mögulegt að stífla Jökulsá
í Fljótsdai neðar í farveginm
23 milljarða
í fómarkostn-
að vegna
Eyjafoakka?
Það er tæknilega mögulegt að stífla
Jökulsá í Fljótsdal við Hrakstrandar-
foss, nokkrum km neðar en nú er gert
ráð fyrir. Sá kostur hlífír Eyjabökkum
en er tvöfalt dýrari en núverandi til-
högun Fljótsdalsvirkjunar. Helgi
Bjarnason sagði Rögnu Söru
Jönsdóttur nánar frá kostum og
göllum tilhögunarinnar.
LANDSVIRK JUN hefur tekið virkjunar er 210 MVV en yrði
til athugunar hugmynd Ilelga rúm 180 MW samkvæmt þess-
Hallgrímssonar náttúrufræð- ari hugmynd. Þær aðveitur
ings um tilhögun Fljótsdals- sem fyrirhugaðar eru ásam t
virkjunar sem fram kom í Eyjabakkalóni eru einnig inni í
Morgunblaðinu fyrir skömmu. þessari hugmynd.
í viðtali við H elga Hallgríms- Helgi Bjarnason segir að-
son í Morgunblaðinu kvaðst spurður að helsti ókostur um-
hann tclja nauðsynlegt að slá ræddrar hugmyndar sé kostn-
af kröfum um hagkvæmni aður. „Stofnkostnaður virkjun-
virkjunarinnar til jiess að arinnar yrði um 46 milljarðar
mæta verndarsjónarmiðum. króna sem er nálægt tvöfalt
Benti hann á tillögu sorn hann meira en kostnaður núverandi
sagðist hafa bent Landsvirkjun tilhögunar, sem nemur 23 millj-
á en ekki fengið svör við. Fólst örðum króna. Magn efnisins
hún í því að stífla Jökulsá í sem þarf í stífluna er helsti
Huínarlu'ði eftir hoÚenskri fyrir-
mynd. Aldrei veíddust nema 17 tonn
það áiið og fór minnkandi næstu ár.
Einnig lækkaði meðailengd veidds
áís lu-att þessi ár og bendir það tii
þess að veitt liafi verið ofanaf stofn-
ínum, endurnýjun hafi ekki verið
nógn hröð og viixtur of hægur tii að
mæta þessum veiðum.“
Möguleikamir
Bjami segir að komið hafi í ljós að
á Islandi séu tvær tegundir ála, evr-
ópski áliinn og ameríski állinn. Þeir
era líkir og eru báðii' upprunnir í
Þanghafinu djúpa. Lengi vel voni
áhöld um að um tvær tegundir væri
að ræða, svo iíkar era þær. Onnur
hefur fleiri hryggjarliði en hin. Iðn
þetta eru klííriega tvær tegundir að
sögn Bjarna og Island er eini staður-
inn á jörðinni þar sem útbreiðsla
tegundanna skarast Það er jafnvel
talið liugsanlegt að þriðja áiategund-
in sé hér sem blendiiigur inilli þess-
ara tveggja tegunda og hvergi ann-
ars staðar að finna. Rannsóknir
Bjarna Jónsaonar ogjapanskra sam-
starfemanna hans beinast mcðal
annars að því að skera úr um þetta.
Þá eru áiategundir víðar, nefna má
td. japanska álinn og önnur tegund
gengur í vötn og ár Eyjaáifu svo
dæmi séu tekin. En evrópski állinn
þykir bera af að gæðum.
„Sóknarfærin eru í’óigin í því að
álaeldi stendur og fellur með veiði á
glerál, en framboð á honum hefur
minnkað mikið í Evrópu. Það kem-
ur sjálfsagt margt til, mengun, of-
veiði og spjöll á búsvæðum svo eitt-
hvað sé nefnt," segir Bjarni, en
hvernig eiga menn að veiða g'lerál á
íslandi og er nógu mikið af honum
til þess að menn getí vakið með sér
vonir um arðbæran atvinnuveg?
„Eg veiddi glerálinn einfaldlega S
finriðinn háf og það er algeng að-
ferð. Gleráli er einnig veiddur í þai'
til gerðar gildrur. Eg veiddi eitt-
hvað um 300 glerála nærri ósum
Álftár á Mýrum nú í sumar. Eg er
þó ekki fyrstur til að ná glerál, því
bóndinn í Laxárholti, Unnsteinn
Stefánsson, veiddi nokkuð af glerál
fyrir tveimur árum í samvinnu við
aðila sem stóðu að fyrirtækimi
Norðuráli. Það fyrirtæki stundaði
veiðar á eldri ál og ætlaði að reyna
áiaeldi, en ekki varð úr og það var
einmitt á þeim stöðum sem ég
vciddi sjálfur gierálinn í sumar.
ar um landið og var
hann fluttur lifandi
tii Hoiiands. Árið
eftir var úfhlutað
álagiidrum til þeirra
sem þá veiði viidu
stunda.
Eftir samvinnu við Norðuráls-
menn á sínum tíma, þegar ég vai'
enn starfsmaður Hólaskóla, varð ég
mér úti um styrk til að hetja ála-
rannsóknir á ný og hófst handa af
fullum krafti nú S sumar.“
Hvaða gagn er í að veiða 800
glerála?
„Ég lief hafið satnvinnu við
heimsþekktan japanskan doktor í
fiskifræði, Jun Ayoama, sem hefur
helgað sig álnum. Hann var hér í
sumar og hafði með sér 100 ála ti!
rannsóknar og hann kemur hingað
til lands aftur næsta ár og verður
með mér við rannsóknir víða um
land. Ég hef sent honum 200 glerála
til rannsóknar. Þar verður m.a.
efnasamsetning kvamanna rann-
sökuð, en með því er hægt að stað-
setja hvar í hafinu álarnir voru á
hinum ýmsu vaxtarstigum. Kollegi
minn japanski hefur m.a. kortlagt
erfðir nánast allra áiastofna og
rannsóknir hans snúa m.a. að þvl
núna að setja rafeindabúnað á full-
orðna ála sein eru að ganga til sjáv-
ar. Hann hefur skip og kafbát til af-
nota og ætlunin er að elta merkta
ála niður í Þanghaf og ná hrygning-
unni. Umfang rannsóknanna er
kannski til marks um mikilvægi
þess að aila vitneskju um áiinn,
enda eftirsótt markaðsvara."
Hvað heíur þú þegar gert annað
en komið hefur íhirn og hvað er
mikilvægast að gera næst?
„Ég verð að geta haldið rann-
sóknum mínum áfram og skilað af
mér mun umfangsmeiri úttekt held-
ur en ég hef gögn í á þessari
stundu. Það sein ég hef m.a. gert er
að rcyna að ná utan um útbreiðslu
ála iiér á landi. Ijítíð er vitað um það
og margt bendir til að víða sé miklu
meira af honum heldur en menn
gera sér grein fyrir. Ég hef talað
við fjölda fólks í öilum landshlutum
við og veiddi ekki neitt. Það er því
ekki á vísan að róa og enn spuming
um hvert magnið er.“
En bemlir eitthvað til að magnið
sá nægilegt til að gera megi glerála-
veiðarað arðbærrí atvinnugrein hér
i landi?
„Já, það eru góðar vísbendingar
um það.“
H áar íjárhæ ðir
Hvað erum við að tala um í krón-
um talið?
„Eins og ég gat um áðan hefur
framboð á glerál minnkað og verðið
þar með rokið upp úr öllu valdi. Eldi
stendur og fellur með veiði á glerál
og hann þarf að nást í sjó áður en
hann fer í ferska vatnið. Eg sá ný-
iega á netinu að kílóverðið á glerál
er komið í 70.000 krónur, en það
fara eitthvað yfir 2.000 glei'álar i
kílóið. Þetta er tala sem hækkað
hefur mjög ört'. Fyrr á þessu ári var
verðið t.d. 60.000 krónur og árið
1997 var það um 47.000 krónur.
Annað dæini get ég nefnt og það
varðar Japansmarkað. Hann er
stærstur, en Japanar hafa neytt
75% heiidarframieiðslunnar. Ái-ið
1990 var heildarneyslan 140.000
tonn. Auk Japans eru stórir mark-
aðir á Ítalíu, í Þýskalandi og
Holiandi. Gleráiamarkaðurinn í
Japan veltir 3 milljörðum króna á
ári og 1.200 miHjörðum með fullvax-
inn ál. Þá erum við einungis að taia
um evrópska álinn. Þessar töiur
fékk ég nýverið hjá Rannsóknar-
stofnun fiskiðnaðarins."
Hveryrðu hoistu vandamálin?
„Ónógt framboð af glerál tii eldis
hefur verið vandamál, enda ræðst
framboðið eingöngu af því hvað
tekst að veiða af honum. Það eru
góðir möguleikar á því að hér á
landi sé umtalsvert magn af glerál.
Menn gætu þá veitt hann og selt lif-
andi til eldis. Eða, ef menn vildu ala
álinn þá eru aðstæður tii þess góðar
víða hér á landi og þekking á álaeidi
fyrir hendi. Það hefur verið vöxtur í
álaeldi og þar af leiðandi hafa orðið
framfarir á því sviði, vitneskja urn
sjúkdóma hefur aukist og þar með
vamir gegn þeim, eldisumhverfi
hefur verið bætt svo og vatnsöílun
með tilkomu endumýtingarkerfa.
Framfarir liafa einnig orðið í fram-
leiðslu á gæðafóðri og allt stafar það
af spám um að eftirspumin eftir
eldisál muni enn aukast."
Morgunblaðinu fyrir skömmu.
í viðtaii við Helga Hallgríms-
son í Morgunblaðinu kvaðst
hann teija nauðsyníegt að slá
af kröfum um hagkvæmni
virkjunarinnar fil þess að
mæta verndarsjónarmiðum.
Benti hann á tillögu sem harin
sagðist hafa bent Landsvirkjun
á en ekki fengið svör við. Fólst
hún í þvf að stífla Jökulsá í
Fljótsdal við Hrakstrandar-
foss, sem er nokkrum kíló-
metrum neðar í farvegi árinnar
en fyrirhuguð stífia Eyja-
bakkalóns.
Landsvirkjun hefur nú tekið
hugmyndina til athugunar og
látið reikna út helstu þætti
hennar. Að sögn Helga Bjarna-
sonar, deiidarstjóra umiiverfis-
deildar Landsvirkjunar, yrði yf-
irborðshæð lónsins 640 metra
yfir sjávarmáli og myndi lónið
ná inn að Eyjabakkafossi, þar
sem fyrirhugað stíflustæði er
nú. Flatarmái þess yrði 20 krn'-
þar af færu 18 kma af grónu
landi undir vatn. Til saman-
burðar er flatarmál Eyjabakka-
lóns 43 km2 og 27 km2 gróins
iands fara undir vatn. Lónið
myndi rúma 460 gígalífra en
Eyjabakkalón rúmar 500 gíga-
lftra.
Orkugeta 10-15% miniii
Dýpt lónsins yrði töluvert
meiri en dýpt Eyjabakkalóns.
Stífla þess yrði um 100 m á
hæð og tæpir 4 km á lengd, en
fyrirhuguð stífla Eyjabakka-
ións er 25 m á hæð og 4,2 km á
lengd. I stífluna þyrfti utn 20
milljónir ma af efni, en til sam-
anburðar má geta þess að 1,5
mílljón m3 af efni þarf í fyrir-
hugaða Eyjabakkastífiu.
Vatnsborðssveifla í lóninu yrði
um 40 m en í Eyjabakkalóni er
hún 16 m.
Meðalfallhæð virkjunarinnar
verður 10-15% minni og orku-
geta minnkar sem því nemur.
Mcsta fallhæð lækkar um 23
metra frá núverandi tiihögun,
verður um 600 metrar í stað
623 metra. Orkugeta núver-
andi tilhögunar Fljótsdals-
þessari hugmynd.
Heigi Bjarnason segir að-
spurður að helsti ókostur um-
ræddrar hugmyndar sé kosln-
aður. „Stofnkostnaður virkjun-
arinnar yrði um 46 milljarðar
króna sem er nálægt tvöfait
meira en kostnaður núverandi
tilliögunar, sem nemur 23 milij-
örðum króna. Magn cfnisins
sern þarf í stífluna er helsti
valdur þess að kostnaðurinn fer
upp úr öllu valdi en stífian er
rneira en tvöfalt efnismeiri en
Káralmúkastífla, samkvæmt
núverandi áætiun.
Hli'fir Eyjabökkum
Helsti kostur tiihögunarinnar
er hins vegar sá að við hiífum
Eyjabökkum. En vegna þess
hvað kostnaðurinn er mikið
hærri er ekki ínni í myndinni að
virkja með þcssari tilliögun
með þessum kostnaði, Það er
vegna þess að víð erum ekki
samkeppnisfærir við erlenda
aðila og aðra virkjunarkosti ef
stofnkostnaðuiinn er þetta hár.
Raunverulega má segja að
verðið sem ber í miili sé sá fórn-
arkostnaður sem þarf að greiða
til að vernda Eyjabakkana, eða
20-23 miHjarðar.
Að öðru leyti höfum við gert
þennan samanburð þanrúg að
virkjanirnar eru mjög sam-
bærilegar, miðlunin er svipuð,
stöðvarhúsið er á saina stað,
göngin óbreytt nema hvað þau
styttast um sex kílórnetra. Þó
ber að hafa í huga að þcssi
seinni kostur sekkur landi og
gróðri sem er undir Fellum
(Laugarfeili, Sauðafeili og Haf-
ursfelli) sem er líka mikil fórn,
og það land er ekki síðra en
landið á Eyjabökkum að
margra mati, en um það eru
skiptar skoðanir. Þá vil ég
benda á að svona kostir voru
teknir til skoðunar á fyrri ár-
um þegar verið var að leita
hagkvæmustu lausnar á þess-
ari miðlun. Þeir útreikningar
sem við hofuin gert núna
styðja því aðeins lauslegar
áætlanir fyi’ri ára,“ segir Helgi
Bjarnason.
130. löggjafarþing 2003-2004.
Þskj. 792 — 437. mál.
Svar
landbúnaðarráðherra við fyrirspum Össurar Skarphéðinssonar um íslenska álinn.
Leitað var svara hjá Veiðimálastofnun.
1. H vaða upplýsingar liggja fy r ir um lífshœ tti áls og á lagöngur í íslenskum ám og vot-
lendi?
Upplýsingar um lífshætti ála og álagöngur á íslandi er að fmna í nokkmm greinum í rit-
rýndum tímaritum, bókaköflum, skýrslum, greinargerðum og gagnasöfnum. Þekking á lífs-
háttum ála hérlendis er samt enn tiltölulega takmörkuð og ljóst að þörf er mun meiri rann-
sókna. M ikilvæg vitneskja hefurþó aflast með þeimrannsóknum sem farið hafa fram síðustu
árin.
2. H vaða rannsóknarverkefni varðandi íslenska álinn eru í gangi, hvar eru þ a u vistuð og
hve m iklu fjá rm a g n i er ᜠtlað að verja tilþe irra?
— Rannsóknir á útbreiðslu og lífsháttum ála á íslandi, Verkefnið er vistað á Hólum í Hjalta-
dal og unnið í samvinnu við Tókíó-háskóla í Japan og Guelph-háskóla í Kanada.
— Rannsóknir á sjávarálum við ísland. Verkefnið sem er nýtt er vistað á Hólum og unnið í
samvinnu við Tókíó-háskóla í Japan og Guelph-háskóla í Kanada.
— Rannsóknir á útbreiðslu og tíðni kynblendinga Evrópuáls og Ameríkuáls á Islandi. Verk-
efnið er vistað á Hólum og unnið í samvinnu við Laval-háskóla í Kanada.
— Rannsóknir á erfðasamsetningu ála á íslandi. Verkefnið er vistað á Hólum og unnið í sam-
vinnu við Leuven-háskóla í Belgíu.
— Rannsóknir á glerálagöngum til Islands. Verkefnið er vistað á Hólum og unnið í samvinnu
víð Tókíó-háskóla í Japan og Guelph-háskóla í Kanada.
— Veiðar á glerálum til álaeldis. Verkefnið hefst í vor og er vistað á Hólum og unnið í sam-
vínnu við aðila í fiskeldi og veiðum.
Til framangreindra verkefna sem vistuð eru á Hólum verður varið í íjárlögum 2004 einni
milljón króna.
— Rannsóknir á sníkjudýrum ála. Verkefnið er vistað hjá Rannsóknastöð háskólans í meina-
fræðum að Keldum og kostað a f rannsóknastyrkjum.
3. H vaða rannsóknir hafa áður verið g erðar á lífsháttum íslenska álsins?
A undanfömum áratugum hefur takmarkaðri athygli verið beint að rannsóknum á ál á
íslandi og að mestu verið stuðst v ið rannsóknir erlendis á lífsháttum ála. A f og til hafa þó
verið í gangi svæðisbundnar rannsóknir og átaksverkefni sem hafa miðað að því að auka
nytjar a f ál á Islandi. Suðurlandsdeild Veiðimálastofnunar stóð fyrir rannsóknum á bjartála-
göngum og m ögulegum nytjum a f álaveiðum á Suðurlandi fyrir um 10 ám m og smærri út-
tektir á möguleikum á álaveiðum hafa farið fram á Vesturlandi. Úttekt á fæðuvali ála fór fram
á Hólum í samstarfi við Líffræðistofnun HÍ og ým iss konar gögn um lífshætti ála hafa einnig
safnast samhliða öðrum rannsóknum. M eð umfangsmestu rannsóknum sem farið hafa fram
2
á álum hérlendis eru rannsóknir á glerálagöngum til landsins sem vistaðar eru á Hólum í
Hjaltadal og unnar eru í samstarfi við erlendar rannsókna- og háskólastofnanir. Þrátt fyrir að
mikil þekking hafi aflast á glerálagöngum og veiðum á glerál á síðustu árum er ljóst að þörf
er á mun meiri rannsóknum á lífsháttum ála hérlendis og þá ekki síst því sem snýr að öðrum
lífsskeiðum álsins, gulálum og bjartálum.
4. H versu m iklum fjá rm u n u m hefur verið kostað til þeirra rannsókna sl. 10 ár? Ó skað er
eftir að upphœ ðir séu tilgreindar fy r ir hvert ár.
A safnlið landbúnaðarráðuneytisins hefur verið veitttil rannsókna á glerál: árið 2000 500
þús. kr., árið 2001 700 þús. kr., árið 2002 800 þús. kr. og árið 2003 800 þús. kr.
5. A hvaða svœ ðum landsins er einkum að fin n a ála?
Til skamms tíma var talið að ála væri aðallega að fínna á suðvestanverðu landinu, Suður-
landi og ekki austar en í Berufirði. Einnig að ála væri í takmörkuðum mæli að fínna á norð-
vestanverðu landinu og þeir væru ekki á Austurlandi og Norðurlandi eystra. Nýlegar rann-
sóknir og samantekt upplýsinga frá heimafólki víðs vegar um landið sýna að álar eru út-
breiddir um allt land og nýta sér fjölbreyttari búsvæði en áður var talið, en mest er a f þeim
á svæðinu frá Barðaströnd í vestri, um Vesturland, Suðurland og austur að Homafirði. Ein
mikilvægasta viðbótin við þekkingu á útbreiðslu og búsvæðavali ála á Islandi er að talsvert
er a f álum í sjó á strandsvæðum víða um land.
6. I hvers konar veiðarfœ ri og m eð hvers konar aðferðum er áll einkum veiddur? H afa
verið gerðar einhverjar tilraunir m eð veiðitœ kni íþ v í skyni að auka afla?
Gulálar og bjartálar eru nánast eingöngu veiddir í vængjagildrur í vötnum, eða ám og
lækjum. Það em sömu veiðarfæri og mest em notuð erlendis. Vegna birtuskilyrða veiðast
gulálar helst á vorin áður en nætur verða bjartar og síðla sumars þegar dimma fer að nóttu.
Bjartálar veiðast frá september og fram í nóvember og dæmi em um að þeir hafí veiðst fram
í desember. Veiðitím abil bjartála er því lengra en þekkist í öðm m Evrópulöndum. Aftur á
móti era þeir tímar ársins sem henta til gulálaveiða takmarkaðri hér vegna bjartra sumarnátta
og lágs vatnshita stóran hluta ársins. Álar hreyfa sig lítið um þegar vatnshiti er undir 5°C og
varast gildrar í dagsbirtu. Fyrirutan hefðbundnar veiðiaðferðirhafa verið gerðartilraunirþar
sem notuð em netbúr með beitu á stöðum þar sem erfitt er að koma við öðm m veiðiaðferð-
um. Þær veiðiaðferðir hafa þó ekki gefíst vel. Einnig hefur verið beitt rafveiði við álaveiðar
og gefast þær best í vatnsminni ám og lækjum. Ekki hafa verið gerðar tilraunir sérstaklega
með önnur veiðarfæri. Umfangsmiklar tilraunir hafa aftur á móti farið fram með veiðitækni
til glerálaveiða þar sem notaðar hafa verið ýmsar útgáfur a f gildrum, nótaveiði, rafveiðar og
nokkrar gerðir háfa.
7. Liggja fy r ir upplýsingar um álaveiði sl. 10 ár?
Ekki hefur verið fyrir hendi fast skráningarkerfi fyrir álaveiðar líkt og tíðkast m eð lax- og
silungsveiðar. Því em upplýsingar um veiðitölur a f skornum skammti. Gróflega má þó áætla
að síðustu 10 ár hafí verið veidd á bilinu 5 -1 5 tonn árlega a f álum hérlendis og þá aðallega
bjartál sem veiddur er á haustin þegar hann fer a f stað á hrygningarstöðvamar. M est var á
þessu tímabili veitt a f ál á ámnum 1996-1998 þegar félagsskapur álaveiðimanna, Norðuráll,
stóð fyrir átaki í álaveiðum.
3
8. H vað m eta sérfrœ ðingar íslenska álastofninn stóran, og hve m ikið er lík leg t að m egi
veiða á n þ e s s að ganga o f næ rri honum ?
Rannsóknir á Suðurlandi benda til þess að þar megi veiða yfir 10 tonn af ál á ári án þess
að ganga o f nærri stofninum og á Vesturlandi gæti það farið yflr 20 tonn. E f litið er til lands-
ins alls gætu þessar tölur verið um 5 0 -8 0 tonn. Hér er miðað við ár, vötn, tjamir og ísölt lón
víðs vegar um landið. Nýjar rannsóknir sýna að ál er að finna í sjó í kringum landið og gefa
fyrirheit um að einnig megi veiða talsvert a f ál í sjó og auka þannig m ögulegt veiðimagn enn
frekar. Áætlanir um stærð veiðistofns og veiðiþol byggjast þó á veikum gm nni vegna tak-
markaðrar þekkingar á magni og lífsháttum áls á íslandi. Þörf er mun meiri rannsókna til að
fá skýrari mynd a f mögulegum álanytjum hérlendis.
9. Telur ráðuneytið að veiðar á á l og vinnsla afurða séu líkleg til að g eta vaxið og staðið
undir sér sem atvinnugrein?
Veiðar á álum og vinnsla álaafurða hefur alla möguleika á að verða m ikilvæg aukabúgrein
hérlendis en til að veiðam ar og vinnslan geti orðið öflug atvinnugrein vantar mikla rann-
sókna- og þróunarvinnu.
10. H afa verió gerðar tilraunir m eð áfram eldi á íslenskum glerál? E f svo er, hver virðast
helstu tœ knilegu vandam álin við eldið? Gefa niðurstöður tilrauna tilefni til að m eta
hvort áfram eldi á íslenskum g lerá l væ ri lík leg t til að standa undir sér?
Tilraunir með áframeldi á íslenskum glerálum hafa ekki farið fram til þessa. Gera má ráð
fyrir að tæknileg vandamál við hugsanlegt eldi séu þau sömu og í þeim nágrannalöndum
okkarþar sem slíkt eldi fer fram, svo sem Danmörku og Hollandi. V ið eldi hérlendis mundu
menn hins vegar njóta þess hve mikið framboð er hér a f heitu vatni til slíks eldis og að
hingað hafa ekki borist sníkjudýr sem valdið hafa veralegum skaða í álaeldi víða um heim,
vegna flutnings glerála á m illi landa. Bann við innflutningi erlendra glerála hefur einmitt
verið mikilvæg vöm gegn innflutningi sjúkdóma og sníkjudýra sem plagað hafa náttúralega
fiskistofna og fiskeldi erlendis. Veiðar á íslenskum glerálum era því forsenda þróunar ála-
eldis á Islandi. Kynákvörðun ála er umhverfisháð og ræðst snemma á lífsferlinum. Hrygnur
vaxa mun betur en hængar í eldi og hátt hlutfall hrygna á íslandi getur gert íslenska glerála
enn verðmætari fyrir áframeldi en ella. Hérlendis era aðstæður hagstæðar til álaeldis og lík-
legt að við gætum verið samkeppnisfær við önnur Evrópulönd í álaeldi. Líkt og í öðra fisk-
eldi á íslandi er fjarlægð frá markaðssvæðum einn helsti ókosturinn. Nokkur óvissa ríkir þó
um hvem ig Evrópulöndum muni takast að mæta aukinni framleiðslu og samkeppni við
Asíulönd og þá sérstaklega Kína þar sem framleiðslukostnaður er mjög lítill. Samkvæmt
upplýsingum frá Asíulöndum hefur markaðseftirspum eftir álaafurðum þó aukist samhliða
framleiðsluaukningu.
11. H afa verið gerðar rannsóknir á göngum glerá ls m eð þ a ð fy r ir augum að nota íslenskan
g lerá l til á fram eldis? E r hæ gt á g rundvelliþe irra að m eta hversu m ikils m agns g leráls
m egi afla ú r íslenskum ám til hugsanlegs á fram eldis? H vað gœ ti þ a ð m agn við hestu
aðstœ ður staðið undir m iklu álaeldi?
Síðustu þrjú ár hefur verið í gangi átak í rannsóknum á göngum gleráls til íslands. Áður
en það verkefni hófst höfðu á undanfömum 20 áram verið gerðar nokkrar árangurslitlar
tilraunir til veiða á glerál og vora tilraunaveiðar Jóns Gunnars Schram árin 1992 og 1993 í
M eðallandi og Landbroti þeirra umfangsmestar. Þær rannsóknir á göngum gleráls sem hafa
4
verið í gangi síðustu þrjú árin hafa skilað góðum árangri og mikilsverðum niðurstöðum um
göngur glerála til íslands. Eitt helsta markmið rannsóknanna var að kanna hvort hérlendis
væri m ögulegt að veiða glerála í nægjanlegu magni til álaeldis og að þróa veiðiaðferðir til
glerálaveiða. T akmörkuð þekking var áður á glerálagöngum til landsins og hvernig best væri
að veiða þá, en hún er grundvöllur þess að hægt sé að veiða glerála í atvinnuskyni og for-
senda þess að hægt sé að hefja samkeppnishæft álaeldi á Islandi. Tekist hefur í þessum
rannsóknum að staðfesta að göngumar era árvissar, að hægt er að veiða glerála á fjölda staða
á Islandi og í nægjanlegu magni til að helja tilraunir með álaeldi. A þessu ári mun sú þekking
sem aflast hefur verða nýtt til veiða á glerálum í áframeldi. O f snemmt er að segja til um hve
miklu magni gleráls verður hægt að ná og taka verður tillit til vemdunarsjónarmiða og þess
að göngumar eru misstórar eftir áram.
Fylgiskjal.
B jarn i Jónsson,
Veiðim álastofnun:
MINNISBLAÐ
Almennar upplýsingar um nytjar og lífshætti ála (Anguilia sp.).
Þeir álar sem fmnast hérlendis hrygna í Þanghafmu en lirfur þeirra berast hingað ári síðar
með hafstraumum um 5.000 km leið og nefnast þá glerálar. Þeir taka á nokkram áram út vöxt
sinn í ferskvatni, ísöltum vötnum, árósum eða sjó og era á því æviskeiði kallaðir gulálar.
Eftir um 5 tii 20 ára tíma umbreytast álamir í bjartála og ganga aftur á hrygningarslóð til
hrygningar og ljúka lífsferli sínum. Álar era mest veiddir þegar þeir hafa náð nokkram vexti
sem gulálar eða sem bjartálar á göngu sinni í sjó. Ekki hefur enn tekist að æxla saman álum
og halda álalirfum lifandi nægjanlega lengi til að nota þær í álaeldi. Samkeppnisfært álaeldi
byggist því að veiða glerála og nota þá í áframeldi.
110
N o. 67 (I)
N o . 6 8 (III)
N o .é 9 (I)
N o. 70 (H)
No. 71 (II)
N o . 72 (IV)
JA N BOÍ-TSUS II'
Schm idt, 1913, ! VI, col. 4, St. Croix. 3 specimens: E. 1896.01,16. 6 specimcns: C
1906.02.14. (49-73). 92 specimens: smal! Y. 1911, june, July.
Y. 1913-15. St. C roix and St. Tliomas. (9Í-540).
Boetius & Boetius, 1967. Y. 1966. (180-580).
E. + small Y. 58.8 mm (53-74). Reccived 1912 frotn U.-S. N at. M us. gi
E. 4- small Y. M ud o f a M angrove swamp, Hungry Bay near Hamilton. 56.8 mm (54-60), .
rcccivcd from Prof. M ark, 1915,
Y. 1974. Shatk River. 35 and 43 cm. Borrowed for X-raying from Dr. G ordon R, Wilham. <
son, U.K.
References - (
Boétius. 1. & J . Boétius, 1967: Eels, Anguilla rostrata, LeSueurj in Bermuda. - Vidensk. M eddr Dansl
N arurh . Foren. 130: 63-84 . /
Boétius , / . , 1976: Elvers, Anguilla anguilla and Anguilla rostrata from two Danish iocaiities. Size, body c
weight, devcíopnicnta/ stage and num ber o ( vertebrae re/ated to time o f asccnt. - M eddr Damn,|-;
Fisk.- og H avuders. N .S. 7: 199-220.
B n m n , A.F., 1937: C ontributions to the !ífe histories of the deep sea ecls; Synaphobrancbidae. - Dana ? í
R eport No. 9. ■■
Ege, V., 1939; A revision o f the genus Anguilla Shaw. A systematic, phylogenetíc and geographíal’3.
study. - D ana-R cport No. 16.
Jensen, A.S., 1937: Rernarks on the G reenland eel, its occurrence and reference to Anguilla rosUata,- •'
M edd. orn G ronland. 118(9). í,
Jespersen , P., 1942: Indo-Pacific leptocephalids of the genus Anguilla. Systematic and biologica! stu*t
dies. ~ Ð ana-R eport N o . 22. f ,
Jones, F.R.H ., 1968: Fish m igration. - London, Edw. Arnoid. 325 pp. V
Jubb , R»A., 1961: The fccshwater ce/s (Anguffla spp.) o f Southern Africa. An inrroduction to thcif L'
identification and biology. ~ Arm. o f the Cape Provincial M useums. I: 15-48. { ;
Petersen, C.G.J., 1905: Larval ecls (Leptocephalus brevirostris) of the Atlantic coasts of Europe.
M edd. Komm. H avunders. Ser. Fiskeri. 1 (5). i
Scbm idt, / . , 1909: O n the distribution o f fresh-w ater eeís (Anguilía) throughout the w or/d. I. AtJanticf •
O eean and adjacent regions. - M edd. Komm. Havtinders. Ser. Fiskeri. 3(7).
Schm idt, J., 1912: D anish researches in the Atlantic and M cditcrrancan on the lifc-history o f th . ,
freshwater-eel (Anguilla vulgaris). - Int. revue d.ges. H ydrobiol. u. Hydrographie. 5: 317-342.
Schm idt, / . , 1913: First rep o rt on eel investigatíons. - Rapp. et Proc.-verb. Cons. ín t. Expl. Mer. IS:1
1 1 -3 0 ,1 """. ' ............... ........... ' ' ■
Schm idl, J., 1915: Second report on ee! investigationS/V- Rapp. et Proc.-vcrb. Cons. Int. Expl. Mei. •*
23: 1-24.
Scbm idt, / . , 1925: O n the distribudon o f the Fresh-water Ee!s (Anguilla) throughout the wotld. íí
Indo-Pacific region. — D. KgL Danske Vid. Selsk. Skr., N aturvidensk. og M athem. Afd., 8 . Rækktj
10(4); 327-382.
Sivcrúsen, E., 1938: Undersekelser ovcr forholder meliem spiss- og brcdhodct ál og dercs nænng.-ft:
F iskeridirektoratets Skrifter, Serie Havundersokelser. (R cport on Norwcgian Fishery and Mannt' ,
fnvestigations 5 (8)) i :
Tesch, F.-W ., 1973: D er Aal. Biologíe und Fischereí. - H am burg u.Berítn, Paui Parcy. 306 pp. j.
Vladykov, V.D., 1964: Q uest for the true brecding area o f American Eel {AnguiUa rostrata LeSueur).~St‘
J .F ish . Res. Bd. Can. 27: 1523-1530.
Vladykov, V.D. & Fl. March, 1975: D istribution of Lcptoccphali of the two specics of Anguilla in thíp
wesrern N orth Arlantic based on coilections m ade between 1933 and 1968. — Syllogeus No. 6 .
tiona! M useum o f N atura! Sciences. N ationa! M useums of Canada. Ottavva. J
{•
A T L A N T IC A N G V I L L A , V E R T E B R A E 111
Appendix by E.F. Harding
gstimathn o f numbers o f A. r o s t r a t a in European material.
It is assumed that
, (i) any specimen with TNV less than 109 is certainly A. rostrata.
(ii) theTNV numbers of genuine rostrata in Europe follow (proportionally) the
saine frequencies as in America.
. Of the American material in table 2, 86% have TNV less than 109. Working
from the material in the Primary Table, and ignoring mixed samples, the cor-
respondirtg proportion for elvers is 84 %, and for adults 88 %.
>.'■ Of the European materíal in table 2, 17 specimens have TNV less than 109. By
the above assumptions we may estimate these as being 86 % of the total number of
rostrata present (or at least between 84 % - the elver figure - and 88 %, the adult
figure). The total number may thus be estimated as 17/.86 = 19.8 (or at least
between 17/.88 = 19.3 and 17/.84 = 20.2). Taking 20 as a round fígure, we have
.13% of European material (15854 specimens) as rostrata.
Tlie expected distribution of these 20 by TNV, compared with that observed, is
as follows:
roslrata rostrata
■ TNV observed expected
112 ■> .01
111 .11
110 ? .58
.. 109 J 2 .11
108 7 5.17
, 107 5 6 .10
106 3 4.36
105 1 1.21
104 1 .25
103 0 .09
The absence of an ‘expected mode’ at TNV — 107 in the total European material of
table 2 is not surprising, the observed frequencies at 108,107, 106 (7,5,3) being
well wíthin acceptable statistical variation from the ideal frequencies (5.17, 6.10,
4.36).
Confidence limits for the expected number o írostrata per 1000 European speci-
rnens have been calcuiated, on the basis of assumptions (i) and (ii) above, as con-
fidence limits for the mean o f a Poisson distcibution (see Biometrika Tables for
Statisticians, E.S. Pearson & H.O. Hartley (eds), vol. I, Cambridge University Press
1966, p.227). The central estimate is 20/15854.
Numbers o f A , rostrata pcr 1000 E uropean specimens:
Central estim ate and confidence limits (9 9 % , 9 5 % ,
90%).
Confidence Lower U pper Central
. I-evel Limit Limii Estimate
99% .6 2.3 1.3
95% .7 2.0
9 0% .8 1.9
1 0 8 JAN BOETIUS
Notes to primary table ,:k
Symbols I-IV givcn in brackets aftcr samplc no.s stand for:
1: da ta citcd froin Hterature,
II: unpuhlished data left by Schmidt and co-workers.
Ilí: data w orked up by the au thor from preserved m aterial ieft by Schmidt.
IV: da ta froin rcccnt m ateriaí worked up by rhe aurhor and others.
O thcr symbols:
E: elvers. Y: yellow eels. S: silvcr eels. f ;
M casurem ents given /n nim indtcatc mcan total length. Ranges are given iri hnickets.
; Ko. 1 (III) E. 1906.01 ,30. ‘lcciand ' ~ no locality givcn. 70.3 itira (63-75). y ?
N o .2 (II) Adult cels. 1906.12.?. Rcykjavik. Yj
N o .3 (l) Schmirh 1 9 n . tab .IV , c o l . l . E + small Y. 1 9 1 1 ,0 7 .9 - 19 . á k fo s s , Faxa Bay. At leasttwö'fi'
year classcs the youngest o f vvhich average 76 m m íö l -H6 ). In the prcsent tablc is added a,;:|
specimcn w ith 109 vertcbrae which according to Schm idt’s prim ary notcs has been cxd|;
cludcd w ith o u t comments. • V
N o. 4 (IU) Dvatc and localiry as in no. 3 . Youngest year class avcragc 77 mm (64-92), thc rcmaining y
part (abou t 20 % ) rangc from 95 to 135 mm.
N o .5 (ÍV) Y. 1972.05 .10 . K oila jírd ir near Reykjavik. 302 mm (215-366). Received from Dr.
G udjónsson. cV
No. 6 (IV) Y. 1973, au tum n. Q rjndayik, thc harbour.
N o .7 (IV) Y. 1973, aum m n. Freshw ater ncar Idvtragexdt. (about 100-400). Prof, C.G, Wilíiams.dy
State (Jniv. N ew York a t Stony Brook, has kindly allowcd me to cite his couutings of A
samples no.s 6 and 7 and to check thc principle of counting from his X-rays.
No. 8 (IV) Y. 1975.08. Lóni lictimCiprcl, SE-Iceland. 330 mm (240-420). Received from Skúli j;.
Pálsson. Reykjavtk,
No. 9 (111) E. 1909.08.06. Thorshavn. 66.7 mm (60-73).
No. 10 (I) Schmidt, 1913, tab. IV, col. 2. E, 1911.05.?. Thorshavn. 67.8 rnm (58-79).
No. 11 (III) E, 1912.05.12. ‘Farocs’. 66.6 mm (59-75).
No. 12 (III) E. 1912 .0 6 .04. Sandegærde near Thorshavn. 68.3 rnm (61-81).
No. 13 (III) £ . 1912 ,08 .19 . Small river to Kalbaksfjord. 66.1 mrn (60-73).
No. 14 (III) E. 1913.08.14. ICalbaksfjord. 66.1 mm (60-73).
No. 15 (III) Small Y. 1925. Trangisvaag. 113 mm (92-135).
N o. 16 (í) Schm idt, 1913, tab. IV, col. 3. E. 1906.06,27. Stronmcss,
No. 17 (II) E. D ate and locality as in no. 16.
N o. 18 (1U) E. D ate and locaíky as m no. 16, 68.0 ram (62-73).
N ö. 19 (III) E. 190S.02.05. Stornow ay. 67.2 mm (6Ö-75)t j,
No. 20 (II!) Ii. 1906.07.03 . Bergen. 68.7 mm (65-74) + 1 spcc. 113 mro.
N o . 2 3 (I) S iv e rtse n , 1 9 3 8 , pp 1 0 - 1 1 . Y + S. 1 9 3 1 - 3 2 . P o o ied datíi o í 3 sa m p le s fro in the Arencialht;
distríct. A bout 550 (abon t 250-900). *
N o. 22 (1) Schmidt, 1913, tab. IV, col. 8 . S (9 2 ) . 1905.10.10. Thc Sound ncar Copenltagen. In tht|i
present table is addttd a specimen with 106 vertebrae which according to Schm idt’s prim+í*
ry notes has been cxciuded w ithout commcnts. (ii'
N o .2 3 (I) Schmitlt, 1915, tab. II, col. 1. E. 1911. Nykolting, Scaland. 70.2 mm (59-81).
N o . 24 (II) E. 1 927 .0J.05 . H ojer Sluse (N orth Sea). 70.4 mm (62-80). I
N o .2 5 (I) Roctius, 1976. E and small Y. 1969.07.04. Esvom, Sealand. A bout 84 mm (62-119). |;
No. 26 (IV) Y. 1971.07 .16. Lake Arrcso, Scaland. 225 mni (170-310),
N o. 27 (I) Boetius, 1976. E. 1972. Pooled dara from 3 samples: 197’2.04 .24 , 72.05,14 and 7 2 .0 6 .0 7 :
H ojcr Sluse (N orth Sca). 72 tnm (60-83). r
No. 28(1) Schmidt, 1913, tab. IV, col. 4. S (9 2 ). 1905.10.30. Toom cbridge. :§
N o .2 9 (I) Schmidt, 1913, tab . IV, col. 5 , 6 an d 7. E. 1908, 1909 and 1911. Bristoi Channei. f
N o ,3 0 (II) E. 1932.03 .25 . Epney, Sevcrn. 72.1 mm (59-83).
N o .3 I (I) Schm idt, 1913, tab. ÍV, col. 9. E. 1906. Bayomte.
N o .3 2 (III) E. 1932.03.?. Loirc. 77.1 mm (66-87).
ATLANTIC A H G V I L L A , VERTEBRAE 1 0 9
M 33 (51) E. 1930.12.?. San Scbastian. 74.6 mm (65-83).
M° 34 I) Schmidt, 1913, tab. IV, col. 1.1. E. 1909.
T ' a q (II Schmidt, 1913, tab. IV, col. 11. E and small Y. 1912.01.04. 88 E: 61.8 ntm (51-73),
N° 13 Y: (78-102).
M 36(1} Schmidt, 1913, tab. IV, coí. 10, E. 1911.08.?, Funchal. 66.9 inm (53-75).
NöÍ37 (»*) E' 1921-0 5 -0 2 * 6 5 3 mm (57-74).
vj 38 (IV) Y. 1973.10.10. Funchal. M uscum specimcns (*VÍMF 23019) borrow cd fo rX -ray in g frorn
Dr. G.E. M aul. 40 , 41 and 56 cm.
No -V9 (II) Adult eeis. 1911. Sr. Cruz de Tenerife.
No. 40 (H) A d u lt eels. 1911. Cadiz.
No 41 (I) Schmidt, 1913, tab. ÍV, col. 12. E. 1911.01.26, Cette. 69.4 rnm (58-80).
N o. 42(H ) E. 1930.01.25. Saiammbo. 69.4 mm (62-77).
' No.43 (I) Schmidt, 1913, tab . IV, col. 14. Y, 1906. Ravcnna.
No.44 (I) Schmidt, 1913, tab. IV, coi. 13. E. 1911,01.27, Livorno. 67.7 mm (58-78).
' No. 45 (I) Schmidt, 1913, rab. IV, col. 15. E. 1911.02,23. Comacchio. 67.5 mm (58-73),
No.46 (II) E* 1922.12.?. Livorno. 70.6 mm (58-82).
' |sj0 (47 (UI) E. 1931.05.16 , C om acchio. 61.0 mm (55-69).
No.48 (H) E. ,1920.02.?. P o rtS a id .
No. 49(H ) E. 1920.12.18. M cx, Alexandria.
No.5Ö (11) E. 1922.01.01. M ex, A lexandria. 299 E: 59.3 mm (54-65) and 16 small Y: (67-96').
No.51 (I) Schmidr, 1913, tab. IV, col. 16, S. 1911.05.13.
No.52 (I) Schmidt, 1925, p. 335 and Ege, 1939, p. 128: Red Sea, M assaua. 1870. 228 mm. 115
vertcbrae. Egc, 1939, p. 91, 129 and 149: Nairobi. 1931.12.03. 277, 290 nnd 298 mm.
V ertehrae: 116, 117 and 115. ‘East A fríca’. 471-600 mm, Vertcbrae: 113-116. 6 speci-
mens in sam ple, vertebrae counted in 5 sp. only.
C om m ent. Tesch, 1973, p. 88 considcrs rhe two East African rccocds doubifu l. W ith
reference to ju b b , 1961, p. 25 he rem arks that confusion with A. mossambica is possible.
Vcrtebrac nurnbers of fhis species, howevcr, range between 100 and 1 0 6 .1 have consulted
Ege’s prim ary notes on the East African ecls and also examined the 3 Nairobi speciinens
(ZM UC P 31263-265). I can only confirm Ege’s statemcnrs.
No.53 (1) Jcnsen, 1937. Adult eels. 1841-1920. (E ds from Grecrdand m ennoned by Schmidc, 1909,
1912 and 1913 are idcntical w ith ecls no. 4 and 5 in Jcnsen’s Iisr).
N o.54(ÍV ) í specímen: Adult. 1965.08.28. ílua T unngdliarftk (ZM U C P3 1196). 22 spccimens:
Y + S. The fjord K angcrdluarssoruscq. 452 mm (345-667). Reccivcd from M r. Bjnrne
Pederscn, Færingchavn.
No.55 (í) Schmidt, 1913, rab. V, coí. 1. Y. 1905. St\ Lawrence. (550-750).
No. 56 (IV) Y. 1961, M ay-August. New Foundfand. (400-800). Vericbrae countcd by Dr. G ordon R.
W illiamson w ho kindly has piaccd his data a t my disposal.
N o.57 (IV) E. 1967,08.14. Topsail. New Foundland. 74.6 mm (69-79). Rcceíved froin G ordon R.
W illiamson.
;N o.58 (I) Schmidt, 1909, p. 10 . E. 1872.03.01. W oods Hole. 5 7 .4 mm (52-63).
No. 59 (I) Schinidt, 1913, rab. VI, col. 2. Y. 1906. Tisbury. (400-700).
No.60 (í) Schmidt, 1915, tab. í,co l. 1. E. 1913.05.07. W .G ioucester, Little Rivcr. 57.1 mm (48-66).
. No.61 (í) Ege, 1939, tab. 135. Y. 1935. M ass. (250-500).
No.62 (il) E. 1921.04.18. potom ac River, Chain Bridgc. 54.7 mm (48-61).
No. 63 (III) Datc and locality as in no. 62. 55.8 mm (50-64),
No, 64 (1) Schmidt, 1913, tab. VI, col. 3. Small Y. 1905.05.?. Weldon.
Nn.65 (IV) Y. '1971. A ugust-O ctober. Sapelo ísland. (310-510). Rcceived from Dr. E. Rasmussen.
No.6 6 (n i) E. 1854. Biloxi. (45-53). 9 specímens, ZM U C 164-172. V ertebrae wcre countcd and
publishcd by Petersen, 1905, as follows: 103, 104, 106, 106, 109, 109 and 113 (!). Latcr
(unpublished) counts by Schm idt gave: 102, 104, 105,. 105, 108, 1 0 8 ,1 0 8 ,1 0 8 and 111.
T he sample was re-counted by me frotn X-rays in 1970. 7 specimcns were casily couiued,
2 wece discarded, possibly thc same spccimcns discarded by Pctcrsen. The figures given in
the prcsent tah le are thosc from 1970.
!' 1 0 6 JA N BO ETIU S |
! ■■ •. 4.
ír'-. .'■■ ■■
Total
num ber
of
verte-
brae
Southern Area, cont.
M adeira, cont. Canarylsl. Spain France Tunísia ítaiy
n o .3 7 n o .3 8 no. 39 no. 40 no. 41 no. 42 /io. 43 no. 44 no. 4S
120
119
118
117
116
4
21
1
1
1
5
2
2
12
37
6
21
1
1 5 .3
14 24 15
29 61 33
115
114
113
112
111
46
50 2
16
4
2 1
4
6
4
43
36
18
4
29
27
11
6
1
33 130 70
33 122 42
14 49 28
7 15 5
1 3 1
110
109
108
107
106
105
104
103
N:
M ean:
143 3
114.49 113
2
116.5
22
115.0
152
114.89
101
114.62
133 409 197
114.83 114.63 114.77
Total
num ber
of
verte-
brae
Southem Area, cont. American material
Italy, cont. Egypt Cyprus ! E. Africa Greenland
//o. 46 no. 47 h o . 48 no. 49 //o. SO no. S1 /i o . 52 no. 53 no. S4
120
119
118
117
116
1
2 .3
24 9
65 40
1
1 2
3 3 3
12 21 18
44 45 70 >■
2
6
15
1
2
115
114
113
112
111
106 75
66 66
27 42
10 9
2 1
54 89 97
44 69 82
17 28 35
6 5 9
2 1
28
26
9
2
3
2
1
110
109
108
107
106
1 1 1
2
5
3 7
1 6
105
104
103
2
2
N :
M ean:
303 245
114.88 114.53
181 266 315
114.92 114.83 114.78
89
114.75
9
115.0
6 23
106.2 107.0
A TLA N TIC A N G U I L L A , VERTEBRAE 1 0 7
Total
number
of
verte-
brae
American material, cont.
Canada U.S.A. Mass. Wash. D.C.
/ io . SS /ío. 56 no. S7 no. S8 no. 59 no. 60 / io . 61 tio. 62 no. 63
. 120
119
118
117
116
• 115
' 114
113
112 1
111 1 - 3 I
110 í 2 3 1 19 2 4 3
109 11 12 1 6 -7 61 9 15 24
108 18 21 1 6 23 131 24 36 59
. 107 24 24 2 2 34 162 35 31 76
106 23 30 1 1 16 107 19 27 61
: 105 8 4 11 16 9 3 19
104 1 3 .4 1 3 1 1 \
103 3 1 1 1
N: 86 100 5 19 94 502 99 119 244
Mean: 107.01 106.96 107.4 108.6 106.95 107.35 107.08 107.35 107.04
Primary table___________________ , 1 V>, ,,
í - - . -I I T? xt 1....... 4 ........ , A i - ,. , n ' \ } i% ... A v r ' ; ’r
1 0 4 JAN HOÍ-'Í ' V i
Total European m alerial, N orthern Arca R’
™ ~
num ber
of
vcrtc-
brae
-"'r i J 1 V .i& b '* ’ íU*?.> *■ >N&. ’ \ ' 6>* , ,*>
•; Iceland^ J ; V f ^ t -V ' 'ið * Farocs
íio. V • no)2 no.3 uo. 4 . no. S 110.6 tto.7 no. 8 no. 9 ’>
120
119
118
■ 117-
116
1 1
2 3 t
10 11 1 7 5
2 30 27 2 4 20 ...... 59 3
115
114
113
' 112
111
8 7 62 50 3 3 23 18
9 2 47 42 3 19 18
14 2 19 23 7 10 26
8 2 8 4 5 10 10
7 _ — 4 10 1
10 >
8 i'
1 '
1
1
110
109
108
107
106
') ' ’ 2 ’ ' S).
1 '
■- : 2 : 'f."‘íl;
105
104
103
■ N : ,
. M ean:
48 '15 180 162 6 26 107 99
112.9 114.3 114.69 114.68 : 115.7 113.3 113.89 114.31
Total N orthern Area, conr.
nvtmber
of
verte-
brae
Faroes, cont. Orkncys
no. 10 « 0 .11 « 0 .12 no. 13 no. 14 no. 1S no. 16 no. 17 »0 . 3á
120
■
119 •■T
118 3 1 1 1
117 22 7 2 3f 6' 2
116 55 8 40 7 18 í 15 5 .. *
115 75 25 88 11 28 1 "1 25 9 13
114 80 48 .98 13 24 3 20 8 19
113 42 39 76 5 4 1 7 5 13
112 3 16 29 2 5
1
1 4 ;;
111 7 8 1 ,
110 1 3
109 - - t
108 _ -
107 - 1
106 1
105
104
103
N :
M ean:
280
114.77
145
113.57
350
114.03
41
114,6
83
114.68
6
114.3
75
114.89
31
114.7
58 '■
114.17;
— ■ ■ — -
*N o . of sample tefers ro notes pp 108-110
ATLANTIC A N G U I L L A , VERTEBRAE 105
102 JAN BOETIUS
111 vertcbrae as a maximum (see notes to no. 66). *
Tlius the only possible A. anguilla (out of 1609) from Amcrican coastal areas
seems to be the 112-eel from sample no. 58. Being accompanied by cels wit|,
unusually high vertebrae riumbers it should possibly be considered a hybrid.
Discussion
Position and extension of the spawning area of A. anguilla is a rather well establ)
lished result o f Schmidt’s classic investigations. Corresponding information abog|
A. rostrata is very poor. Vladykov, 1964, has proposed the spawning area of A. r0.J
strata to be situated south of that of A. anguilla (not west of A.a. as did Schmidt||
Spawning of the two Atlantic spedes are likely to overlap in space and possibly alsö|
in time. ,-É
Based on surface current studies, Harden Jones, 1968, has constructed the drift|
of two patches of eel larvae, both hatched in March in each of the two supposcá|
breeding areas. The main routes are re-drawn (from his fig. 21) in fig. 4 in thtj
present paper. On both sides ofthe central A. anguilla-tomt marginal branches at|
added by dotted lines. The northern branch (N) indicates, that A. anguilla larvat|
emerging frotn the southern part of the breeding area end up in northern Europej
As the northern branch has the closest relation to the A. rostrata route it í |
Fig. 4. M ap ancl íully drawn routes o f drifting Atiantic eel larvae re-drawn
from Harden Joncs, 1968. 'i’lie dotted lincs indicate thc supposed routes of
A. anguilla frotn southernly and northcrnly situaced positions within che
European brceding arca. Larvac of southernly origin are seen to form the
northern branch supplying area N with clvcrs whiic iarvae hatchcd in the
northern part of the breeding area end up in area S.
AT LANT IC A N G U I L L A , VERTEBRAE 1 03
to t a l n u m b e r o f v e r t e b r a o
Fig. 5. European elvers. Distributions o f rotal numbcrs o f vcrtcbrac of pooled
samples with rneans á 114.0 and > 114.0.
reasonable to expect a relatively high degree of mixing of the two species in
northern Europe. This is actually what has been stated in the present paper.
Overlapping of the w o breeding areas could possibly cause hybrydization. In
this case also the hybrids vvould most likely end up in northcrn Europe. The
presence of reiatively high numbers of eels with 111 vertebrae in northern and
central areas (table 4) might indicate a small amount of hybrids.
It' was.demonstrated earlier in this paper that samples from certain years showed
low 1 NV values. In fig. 5 FNV distributions of the total material of European pure
elver samples are given for samples with means = 1 1 4 and > 1 1 4 respectively,
Tests for skewness have proved that both distrtbutions are highly symmetrical.
There is hardly reason to believe, that the low vertebrae numbers in the = 1 1 4
group are due to mixing vvith hybrid specimens.
Concludingly it is proposed , that in som e years the process o f d ifferentiation o f
vertebrae num ber seem s to stop a little earlier than usual.
Little is known about the larval TNV during growth. Jespersen, 1942, gave
myomer counts of larvae (of total lengths > 4 0 mm) from the Danish expeditions
1913 and 1920-21. He concluded that for both species the number of myomers
would exceed that of the final vertebrae number by about one. Vladykov &c March,
1975, however, have myomer counts which at an average were 3-4 myomers lower
than those of Jespersen’s. This difference Vladylcov &c March attribute to several
causes: ‘counting technique, different numbers of specimens, variation in size of
specimens, and difference in coilecting localities.’
100 JA N B O E T IU S
A T L A N T I C A N G U Í L L A , V E R T E B R A E 1 0 1
A n g u illa ro s tra ta in Europe o
SchmidtMs.djsoiSsed the problem ofjT>pjsihl£,.iaixinB.ojLAuieriom.attdJi.uxopQ9i-r
StocKs of adult eels in his p apersl9Í2 (p. 337), 1915 (p. 5) and 1922 (p. 204),,)
small overlapping (.5é '%]T)5tweenr3istributions of vertebrae numbers was takog
by hím as an índicatíon of a possíble mixing. %
ín no case did Schmidt publish records oí eels from European stocks with typics),:;
A. rostrata vertebrae numbers. His primary notes (see NPT nos 3 and 22), how. ;:
ever, indicate that eels from Europe with vertebrae numbers 109 and 106 wettiý
present in hismaterial published in 1913. In 1922 he states ‘thatthe stock ofeelsi}|
Europe is, practically speaking, pure, i.e., composed exclusiveiy of Anguilla vulgaris'.i.
The first published evidence about an eel from Europe with TNV typical of ké
rostrata was given by Bruun, 1937, who relates that a specimen (68 mm long, 10S|
vertebrae) was present in a Spanish sample sent to Schmidt from A. Gandoli;;:
Hornyold. This satnple is recorded here as no. 33. .
Bpgrius^ 1 fnimd. that A..rostegfa-w.as.repjesenred.bv small numbers..(aboBfe
•3T4)jn..eívers from two Danish localities. Eels-with4T0-ver.tebrae..werexonsiderel|
‘mos.t .likely’ Á. ras'trata, eels with TNV á 109 as true A. rostrata. This assumptiojj
was supported by cieterminations ofano-dorsal distances. The material is recordcij
here as samples nos 25 and 27. : j
Inspecting the total European material presented liere in table 2 it is seen that anil
expected mode of 107 vertebrae is not present at all. Judging from the table 2 datij
only, the European materiai couid be considered as one (skew) dístribution. Coivj
sequenriy the variation of TNV in AnguiUa anguilla would cover the full rangeolj
the two species. The absence of a 107 modc, however, is not surprising accordin}|
to the statistical considerations given in the appendix. if
A clear 107 mode, however, is demonstrated fbr northern elvers in tabie
Actually all 5 specimens with 107 vertebrae from the total European matcrial a»|
elvers froin the northern area. When placed together with eels from different areaifi
and at different ages the 107 mode is covered as seen in table 2. :)
In table 6 eels with TNV § T10 and á 109 are listed for tbe total Europeaaj
materiai covered by the primary tabie. (t is seen, that in each case the frequenqs
decreases from rhe northern to the central area. In the southern area it cannot fc;2
Tablc 6 . European matcrial. Frequcucics of ccls wilti total mimber of vcrte- : ,
brac ~ 110 and § 109. ,
N um bcr
o f ccls
Area couuted
S 110 vertebr.ic ú 109 vertebrae
Ntim ber % Numbcr %
N orthcrn 9580 47 .49 24 ,2S
C entral 3400 4 .12 2 .06
Southem 2S74 2 .07 0 .00
Total 15854 53 .37 26 2 6
Table 7 .
Ecls with 3 109 vertebrae from European material.
Tot. nb. of Tota! PT
No. Date Locality vertebrae length, inm Stage no.
1 1905.10.10 Denniark, Kallebod Sttand 106 silvcr 9 22
2 1911, Juiy Iccland, Faxa Bav, Alafoss 109 _ smal! ycllow 3 + <
3 1912.05.12 Faroes 106 68 eiver 11
4 1912.06.04 Faroes, Thorshavn 107 62 clver 12
5 1930, Dcc. Spain, San Sebastian 108 68 clvcr 33
6 1932, M arch Francc, Loire 104 73 elver 32
7 1969.07.04 Denniatk, Esrom 109 86 í-group 25
8 _ 108 90 i-grotip 25
9 1971.07.16 Denmark, Arrcso 1.09 218 ycllow 26
10 __ „ 109 247 yeíiow 26
11-23* 1972, Apr.-June Denmark, Hojer 105-109 63-75 elvers 27
24 1973, autum n íceíand, Hverngcrdi 108 - yeílow 7
25 - 108 - yellow 7
26 - - 109 - yeliow 7
*For dctaits, see Boétius, 1976
stated with certainty if A. rostrata is prcscnt at all. Details of the 26 specimens with
vertebrae S 109 are listed in table 7. The specimens are seen to cover the full range
of developmental stages.
Of special interest is the Danish silver eel vvirh 106 vcrtebrae listed as no. 1 in
table 7. The eel was caught together with 127 female silver .4. anguilla leaving the
Baltic on their autumnal migration. 4 . rostrata thus seems capable not only to
, sliare growth conditions witli 4 . anguUla but also to turn silver and leave (for the
Sargasso Sea?) together with true European silver eels.
The eel was caught in 1909. Future records of adult 4 . rostrata in European
vvaters should be considered with a certain caution. During thc Jast decades adult
Ámerican eels have been imported live into several European couritries on a cora-
mercial scale.
Ainerican material
Fhe hitherto unpublished data on TNV of American eels given here do not add
much to what was already known. Ncw data from Greenland (no. 54) and Bermu-
• da (nos 70 and 71) confirm earlier siaternents, that these rvvo arcas are populated
by A. rostrata solely.
Mean TNV values of samples with more than 10 specimens all range betrween
107.0 and 107.5 except for sample no. 58. Thís sarnpie (from Woods Holc, Mass.)
was counted and published by Schmidt, 1909. M eanTNVof the 19 specimens was
extremely high, 108.6, and one of the eels had 112 vertebrae.
Sample no. 66 (from Biloxi, Miss.) vvas originally counted and published by
Petersen, 1905, and claimed to contain a spccimcn with 113 vertcbrae. The sarnple
was recounted by Schmidt and latest from X-rays by me. Both recountings gave
98 J A N B O É T I U S A T L A N T I C A N G U I L L A , V ER TE B R A E 99
Tablc 4. European material.ÍElverstTotal numbers of vertebrae in northcrn, central and soutliern areas.'J
T otal
num bcr of
vectebrae
N orthern area Central area Southcrn area
N um ber % of total Number % of total Numbcr o of total:
120 1 .04 ;
119 4 .07 6 .18 5 .20 ■
118 58 .96 36 1.10 27 1.07
117 287 4.74 177 5.39 163 6.48 :
116 939 IS.SO 517 1S.7S 472 18.77 i
115 1673 27.61 917 2 7.93 808 32.13
114 1684 27.79 901 27.44 642 25.53 i
113 988 16.31 517 1S.7S 300 11.93 '}
112 323 S.30 163 4.96 82 3.26 '.
111 75 1.24 45 1.37 14 .56
110 13 .21 2 . .06 ...... 1 .04
109 4 .07 - -
108 3 .05 1 .03
107 5 .08 - -
106 2 .03 - -
105 1 .02 - _
104 1 .03
N 6059 3283 2515
M ean 114.438 114.504 114.744
S.E. .018 .024 .026
( jt jg , Jjv European m aterial.
: Frequencies o f sample means
of total numbers oí vertebrae.
Sigitaturc: elvers are indica-
tcd by blaclt circles, adiilts by
wliitc circles and ‘mbted’ samp-
les by black and white citcles.
(Thc figure compríses all Eu-
ropean samples except nos 5,
15,38,39 and 52 w herenum -
her o f specimens in sample
was below 10. Samples 3 and
4 were pooled.)
4 -
3 -
2 -
1 - «
— T — i— I— i T T T 1 " 1
N o r t h o f n.. n t »-= •'
• # o • O í
. —,— ,—)—i r i [ i
O
O
0 ®
O • •
» 9 0 9 9 0 9 9 *
r r r
0 O
4 - O
3 - 9
2— •
lL~ $ • •
- O
5- S o u t h u r n a r e a O
— 0 •
3 - • • •
2 - • « • •
- • • « ® o
.1 1 1 I 1 1 1 1 I L 1 J _ _ _ L . J _ _ _ 1___ i_ _ _ 1__ _ 1- . j _ _ _ j _ _ _ i_ _ _
lo t i i l n u m b o r o l v o r to b fo e
Elvers. In table 4 mean vaíues ofTNV are given for the total European materip
of ‘pure’ 0-group elver samples. On average the vertebrae number incrcases fronig
the northern to the southern area by about onc third of a vertebrae.
A rnore detailed information, however, is given in fig. 3 where frequencies of|
TNV means are given for the total European material. The elver material fronif
table 4 is indicated by black circles. From figí 3 is seen, that elver samples with lovf|
TNV means (i.e. á 114.0) occur predominantly in the northern area and are noij
present at all in the southern. f
In table 5 localities and dates are given for all samples with TNV means á lH.O.g
Except for a single sample (France) they all origin from northwestern Europe. Itisf
evident from the primary tablc, that the majority of samples from this region havj|
quite ‘normal’ TNV means. The ascent of low TNV elvers thus seems to be áii|
irregular phenomenon.
Let us consider the year 1906. Referring to table 5 low TNV elvers ascendii#
Iceland, Hebrides and Norway from January, 30th to July, 3rd. In the same yeart|
however, ‘normal’ TSTV elvers ascend at the Orkneys (spi.nos .16-18) June, 27t|i||
i.e. 6 days before the Norwegian ascent. It seems reasonable to suggest that the lo||
TNV elvers from 1906 belong to one and same wave of invasion. The ‘normalg
Orkney elvers could possibly belong to a Iater arriving invasion.
: In table 5 the year 1912 is reptesented by two low TNV samples from the
Faroes. Dates o f collection were May, 12th and june, 4th. From the same year a
sample (no. 13) with ‘normal’ TNV mean was collected August, 19th at the Faroes.
. As in 1906 elvers with iow TNV seem to precede the ‘normal’.
Adults. Two samples from Iceland, 1973 had mean TNV values below 114
(spl.s nos 6 and 7). Eels from these samples no doubt represent more than one year
class. A sample of adult eels from Iceland, 1975, (no.8) had ‘normal’ mean.
Concluding this section it can be stated, that in some years (or short sequenccs of
years) elvers with low TNV mcans occur in Europe as the firsdy arriving part of
• the ascent. Invasion seems predominantiy to take place in northwestern Europe
; and apparently not at all in the Mcditerranean.
Table 5. European m aterial. Localities and datcs o f all samplcs w ith m ean total
number of vertebrac S 114.0.
Stagc
Elvers
Total nb. o f
vertebrae.
M ean
112.9
113.1
113.2
1 13.6
113.6
114.0
Locality Date
PT
no.
Iceland
Hebrides, Stornoway
Norw ay, Bergen
Faroes
France, I.oire
I'arocs, Thorshavn
1906.01.30
1906.02.05
1906.07.03
1912.05.12
1932.03.?
1912.06.04
1
19
20
11
32
12
Adult 113.3
113.9
Iceiand, Grindavik
Iceland, Hvcragerdi
1973, A utum n
1973, Autumn
9 6 J A N B O E T I U S A T L A N T I C A N G U I L L A , V E R T E B R A E 9 7
Fig. 1. Distribution o f to ta l num bers
o f ve rteb rae in to ta l A m erican and
E u ro p e an m a te ria l. A bso lu tc figures
are given in tab le 2.
102 lOí 106 108
T c l a l n u m b ð r o f v u r i c b r a
brae: 1.1 % of che European and 0.6 % of the American material share this nuniber
o f vertebrae.
Compared with Schmidt, 1913, and Ege, '1939, the present material representsí
an extension by a factor 5.7 of the European matcrial and by a factor 1.7 o£ the;
American. In spite of this, the European mean value of vcrtebrae number has;
changed froin 114.73 to 114.62, the Atnerican meau frorn 107.23 to 107.19 onl)1,
The present material contains samples of three categories: 1. pure 0-group
elvers, 2. adult eels only, 3. ‘mixed’ samples where both eivers and small yellow;
eels are present. In table 3 elvers and adults are treated separately and mixed:
samples not considered at aií. t
European adult eels have higher mean number of vertebrae than European elvcrs
while American-aáuksjhaxe lower.mean than. Aroe.ricanÆlv_e.rs, A statistical treat-
, Table L . European and Amcricau material. Total numbers of vettebrae in elvers and
'aduitíj-cxcluclmg mixeci samples with bofh elvers and adnlts.
Europe Amevica
Elvers Adults Elvers Adults
Mean
S.E.
Nb. of eels
114.532 114,672
.012 .040
11840* 1398”
107.284
.042
896
........- ................. -
107.044
.055
595
inent of the table 3 data indicate that the differences mentioned arc significant in
both species.
. goetius, 1976, analysed a ‘mixed’ sample (here given as PT no. 25) and statcd
that vertebrae numbers of the I-group surpassed those of the 0-group elvets. Xhe
ingpa.ta.ceJ.a..vert.eb.i:ae..numbers was suegested to be related to growth. The data
. from table 3 arc consistent vvith this suggestíon.
European material, geographical vartation
For the present considerations the European material is divided in three geographi-
cal uníts: the northern, the central and the southern area. The areas are given in
fig. 2. They roughly correspond to three different migration routes of eel larvae
invading the European continental shelf.
In the text to foliow the symbol T N \? has been introduced for ‘total numbet of
vertebrae’.
20 ________ 10________ 0
M 7 spccimens with vcrrcbrae » 109 excluded.
> t - ^ 109
Fig. 2 . M ap presenting tbe threc areas rcferred Co in the tex t as norrhern,
! reniral and sotithern arcas. Figurcs indicate uumbecs o f ecls from thc area
; hstcd in primary tablc. Circles show sampic localitics. The hatched zonc
inside the ccntral area indicates the so-caiied target arca wherc elvers have
bccn fishcd commcrcialiy.
94 JA N B O É T IU S
From 1915 to his death, 1933, Schmidt and his collaborators continued .1t
work on meristic characters in Atlantic Anguilla, especially counts of total nun
bers of vertebrae of eels from different geograpliica! areas. These data, howcvei
were never published. Thus at his death Schmidt left several notes and protocoi
and also a collection of preserved material of Atlantic elvers, which was nc
worked up at all,
About a decade ago Dr. E. Bertelsen, at that time the director of this instituti
asked me to go through the material in question and decide if the rather scattere
data couid be arranged in such a form, that a publication was justified.
Thís paper ís my answer to Bertelsen’s question, and I have taken the opportunit
to place together all data — published as well as unpublished - known by me abo\:
total numbers of vertebrae in Atlantic Anguilla.
Table 1. Sources and size of material.
N um ber o / eels
Source Europe America
í. Previously published data
Schmidt, 1909, 13 and 15 3041 882
Boétius, 1976 6460
O ther 427 184
II. D ata left by Schmidt 3496 141
III. N ew countings from
Schm idt’s lcft colicction 1965 259
IV. O ther unpublished data 465 143
T otal 15854 1609
Sources of materíal
Vertebrae counts of a total of 72 samples are arranged geographically in tlii
primary table pp 104-107 (currently cited as PT). Additional information abou
stage, season, locality and size is given for individual samples in the notes pp 10i
110 (NPT). In NPT the sample no.s are followed by the symbols I-IV given ii
brackets. Symbois I-IV indicate the source of material and are explained as íollow ■
■ I. Previously published material. Proper referehces to authors are given tn NPV
(As I have had the opportunity also to consult the primary data of Schmidtii
published work, I have been able to give information in NPT, which was no
given by Schmidt himself.)
II, Unpublished data left by Schmidt.
III. New data from Schmidt’s left collection of preserved specimens worked ti
for the present purpose.
A T L A N T I C A N G U I L L A , V E R T E B R A E 95
jV. urner unpuousnea aata worked up trom samples recently received or data
placed at my disposal by coileagues.
Table 1 gives a survey of the proportions of sources I-IV. AU counts in III and tn
ihe:greater part of IV were made by Mr. Paul Juhlin of this institute. Dr. Jorgen
Nielsen arid Mr. G. Brovad, both of the Zoological Museum, Copenhagen, have
kiiidiy given thetr help in preparing the X-rays used for vertebrae counting. Dr.
ÉvF.-Harding, Statistical Laboratory, Cámbridge University, has made the appendix.
The principle of counting was that of Schmidt’s, 1913: The short atlas was
counted as no. 1 and the last hour-glass shaped verrebra was taken as the next but
last vertebra. It has been carefully checked that all samples Iisted in PT have been
cöunted in accordance w'ith this principle.
CjTjble 22 European and American material. Total o f al! stagcs. D istribution o f totai
jmbers o f vertebrae.
h
• , T o t a l
a u m b e r of
v e r t c b r a e
E u r o p e a n m a t e r i a l A m e r i c a n m a t c r i a l
N u m b e r % o f t o t a l * N u m b e r % o f t o t a !
3 . 0 2
M l 9 ' ■ 3 0 . 1 9
2 1 1 1.33
Í Í Í Í 7 . . . 1 0 2 3 6 . 4 5
W l é - 2744 17.31
4 T Í T 5 - 7 4 6 1 1 29.08
4 0 9 3 2S.82
. 1 1 3 2 2 2 1 14.01
1 1 2 6 9 2 4.36 1 .06
' f e i i i i . 1 7 3 1.09 9 . 5 6
■ — 1 1 0 2 7 .17 4 7 2 . 9 2
• 1 0 9 9 .06 1 7 0 10.S7
1 , 0 8 : 7 .04 4 1 6 2 5 . 8 5
■ 1 0 7 5 .03 4 9 1 3 0 . 5 2
, 1 0 6 3 .02 3 5 1 21.81
I J 0 5 . • 1 .01 9 7 6.03
Í 8 Í Ó 4 ' ' "
1 4 0 3
1 .01 20
7
1.24
.44
N 1 5 8 5 4 1 6 0 9
Mean 1 1 4 . 6 1 7 1 0 7 . 1 9 0
.011 . 0 3 2
American versus European vertebrae numbers
in table 2 and fig. 1 distributions are presented of vertebrae numbers of the total
matcrial o f eels from both sides of the Atlantic.
Vertebrae numbers in the Am£ri.can..tna.teríal are secn to rangg_XQ:la.ll2q in the
^mBpeanmjateM-ai-l£láZL2í). The maximum overlapping taking place at 111 verte-
.
Atlantic Anguilla.
A presentation of old and new data
of total numbers of vertebrae
With special reference to the occurrence
oí Anguilla rostrata in Europe
S j a n B o e t tu s
V yfiíÐ anísh'Tnstítute for Fisheries and M arine Research, Charlottenlund C astle,
"ÖK-Z920''C harlottenlund, D enm ark
Abstract
'The author has placed together all published data know n by hím a b o u tja l^ ju ia i lK r íJ j fx s a e b r a c in
' turn. Arlantic sDedes-QLág.er«l/g. To this has been added unpublished results from J. Schmídt and
iffoííTodKÍr sources. M oreover selectetl m aterial from Schmidt’s left collections has been w orked up for
sa'lté4purpose. The materia! is presented in a prim ary table w ith notes to individual sampies.
> ^The European material is considcred for three geoRraphical regions separateiy; a northern. a central
’ nndTsöútSiernTThe areás correspond to d te th re e main rpjjX eiairíM riim sirin Ju s .s ta fed ^ íh 3i:in-[Íte
7ji5ctKönréjpcinT « nmv3711|!SSgrg^^
S#!aslpresent, w tiile i’h the söuthern region specimens o f A . rostra ta were hardly present.
' Matetial o f A. rastra ta from Europe com ptises all developmental stages from 0-group elver to silver eel.
ftpmNorthem sainples from certain years show ed relatively low numbers o f total vertcbrae ín A . anguilla .
Contents
: Preface................................................................................. 93
spSources of material ..........................................................94
Æ- •American. versus European vertebrae numbers 95
- European material, geographical variation . . . 97
‘ *Aneutlla rostrata in Europe. ...................................... 100
íi Smertcan materTal ...................................... 101
Ðiscussion ................................................................ 102
Ptimary ta b le ................................................................ 104
Notes to primary ta b le ............................................... 108
;\References...................................................................... 110
1V Appendíx......................... 1 11
M '
Preface
í The total number of vertebrae was early pointed out by Johannes Schmidt as the
, jbest distinguishing character between the American and European species of An-
̂ gutlla. Especially his classic documentations from 1913 and 1915 have been used
i;.uP5o present days as a base of reference.
VMST/11060
Ganga bjartáls niður úr
Elliðaám og Elliðavatni
Þórólfur Antonsson
Veiðirpálastofnun
Veiðinýting • Lífríki í ám og vötnum • Rannsóknir • Ráðgjöf
Forsíðumynd: Hólmsá í vetrarbúningi /áll
Myndataka: Sara Jonsson / Þórólfur Antonsson
Efnisyfirlit
1. Inngangur .............................................................................................................1
2. Lífshlaup álsins og rannsóknir á íslandi..................................................... 1
2. Söfnun gagna.......................................................................................................3
3. Niðurstöður.......................................................................................................... 3
4. Umræða.................................................................................................................6
5. Þakkarorð.............................................................................................................7
6. Heimildir................................................................................................................7
Inngangur
Gögnum um niðurgöngu ála (bjartál) hefur verið salhað samhliða öðrum rannsóknum
Veiðimálastofnunar á lífríki Elliðaánna (Þórólfur Antonsson og Friðþjófur Amason 2011). All
fer í göngubúning líkt og gönguseiði laxins þegar hann er að búa sig til ferðar til sjávar og nefnist
þá bjartáll. Það kemur til af því að hann verður ljós eða silfraður á kvið og undirgengst
margháttaðar lífeðlisfræðilegar breytingar sem gera honum kleift að breyta úr umhverfí
ferskvatns yfir í sjávarlíf.
Hér verður gerð grein fyrir göngum bjartáls niður Elliðaámar yfír nokkurra ára tímabil en til
þess að setja þessi gögn í samhengi verður farið í stuttu máli yfír lífhlaup áls og vitnað til þeirra
rannsókna sem til em um hann hér á landi og að nokkm til erlendra rannsókna einnig.
Lífshlaup álsins og rannsóknir á íslandi
Tvær tegundir ála, sem ganga í ferskvatn, em í Atlantshafí þ.e. Evrópuáll (Anguilla anguilla) og
Ameríkuáll (Anguilla rostrata). Island er talið eina landið þar sem blendingar þessara tegunda
finnast (Avise et al. 1990) og var hlutfall blendinganna metið 15,5% en annað hreinn Evrópuáll
(Albert o.fl. 2006). Áður var talið að hluti ála hérlendis væm Ameríkuáll (Boetius 1980).
Hérlendis er állinn algengur frá Suðausturlandi vestur um til Snæfellsness en fínnst að nokkm
marki í öllum landshlutum.
Áll hrygnir í sjó en elst upp í fersku vatni (kallast catadromous), öfúgt við laxfískana sem
hrygna i fersku vatni og fara svo til sjávar til að taka út megnið af vextinum þar, en það kallast
anadromous. Menn vom lengi að átta sig á lífsferli álsins og hafa raunar ekki lokað þeim hring
alveg. Eftir miklar rannsóknir Johannes Schmidt fyrir rúmri öld síðan, einangraði hann svæði í
Þanghafinu þar sem hann náði nýklöktum seiðum (Tesch 1977). Nýklakin em seiði álsins
gjörólík fúllorðnum álum, en þau em flöt og glær á litinn. í árdaga vom þau talin sér fisktegund
og kölluð Leptocephalus en síðar kom hið sanna í ljós. Seiðin fylgja Golfstraumnum frá
Þanghafinu en synda einnig með straumnum því ferðahraði þeirra er meiri en straumhraðinn. Út
frá rannsóknum á mynstri í kvömum áls er talið að hann sé rétt um ár á leiðinni (Jónsson og
Noakes 2001, Kuroki o.fl. 2008) en áður var talið að ferðalagið tæki 2-3 ár.
Þegar hin flötu og glæm seiði nálgast strandsvæði Evrópu þá myndbreytast þau og taka á sig
hið sívala form fúllorðins áls en em enn glær á litinn og kallast þá gleráll. Glerállinn gengur
síðan upp í ferskvatn og tekur út megnið af sínum vexti þar. Þó hefur reyndin verið sú hérlendis
1
að hluti hans heldur sig í ísöltum lónum og jafnvel í fullsöltum sjó á strandsvæðum (Ámi
Kristmundsson 2003, Ámi Kristmundsson og Sigurður Helgason 2007).
Gerðar hafa verið rannsóknir á komum gleráls upp í ferskvatn hérlendis (Linton o.fl. 2007,
Kuroki o.fl. 2008). Aðalgöngutími glerálanna er frá apríl og fram í byrjun júlí en þeirra verður
fyrst vart í mars og um miðjan júlí em göngumar yfirstaðnar. Þeir þættir sem ráða hvað mestu
um hvað örvar göngumar upp í ferskvatn em sjávarfoll og vatnshiti (Linton o.fl. 2007, Kuroki
o.fl. 2008). Samkvæmt niðurstöðum Kuroki o.fl. (2008) var meðallengd evrópska glerálsins var
68,3 mm en 67,1 mm hjá blendingunum.
Eftir að í ferskvatn er komið getur glerállinn sigrast á ótrúlegum hindmnum á leið sinni að
heppilegu búsvæði. Virðist þá sem hitastig vatnsins þurfí að vera orðið nokkuð hátt til að hann
ráði við klifur mikils halla og gangi best við hitastig um eða yfír 20°C (Lington o.fl. 2007).
Gömul ömefni benda einnig til að glerállinn hafí lengi skriðið yfír hindranir t.d. Álafoss í
Mosfellsbæ. Síðan sest hann að í lækjum og stöðuvötnum og dökknar á litinn en kviður verður
gulleitur og kallast hann þá guláll. Fæða álsins hefur verið könnuð í Vífílsstaðavatni af Stefáni
Má Stefánssyni (2000). Fæðan var nokkuð fjölbreytt en helstu fæðugerðir vom rykmýslirfur,
vatnabobbar, homsíli og hrogn annarra físka, en sýni vom einungis tekin að haustlagi. Einnig
hafa Ámi Kristmundsson og Sigurður Helgason (2007) gert allítarlega úttekt á sjúkdómum og
sníkjudýmm sem hrjá álinn og vom sýni tekin á fímm stöðum á sunnanverðu landinu.
Niðurstaðan varð að tuttugu og þrjár tegundir sníkjudýra greindust í þessari rannsókn. Níu
þessara tegunda vom fmmdýr en fjórtán fjölfrumungar. Þetta em mun færri tegundir en fundist
hafa erlendis en þar hafa 170 tegundir sníkjudýra verið greindar í álum (Anguilla sp). Ekki var að
sjá alvarleg áhrif sníkjudýranna á álinn nema lítilsháttar vefjaskemmdir frá einni
framdýrategundinni.
Eftir margra ára dvöl í fersku vatni fer állinn að búa sig til farar í sjó á nýjan leik, verður þá
silfraður á kvið og byrjar að ganga niður ámar til sjávar. Verður hér greint frá nokkmm
upplýsingum um niðurgöngu hans.
2
Söfnun gagna
Söfhun gagna fór þannig fram að á vissum árstíma fengu starfsmenn rafstöðvarinnar í
Elliðaánum bjartál í síur vatnsinntaks og einnig í gegnum vélar virkjunarinnar. Frá árinu 1998
voru þeir beðnir að safna ál sem kæmi í síur stöðvarinnar og þeim ál sem hefði farið í gengum
vélamar og oft laskast þannig að þeir náðu honum. Þetta vom allt bjartálar sem bámst til
Veiðimálastofnunar. Eftirfarandi þættir vora skráðir um álana: göngudagur, lengd (cm), þyngd
(g), kyn og magafylling. Kvamir voru teknar til aldursgreininga. Ami Kristmundsson
fisksjúkdómafræðingur á Keldum las hluta kvamanna og bar niðurstöður undir erlendan
sérfræðing, Christopher Moriarty.
Gert var ráð fyrir því að þar sem rafstöðin var rekin með svipuðum hætti árin 1998-2005 (en
það vora þau ár sem sýni bárast), þá hafi fjöldi þeirra ála sem náðust gefið réttar upplýsingar um
göngutíma álanna og úrtakið endurspeglað stærðir, kyn og aldur einstaklinganna í göngunni. Þó
er ekki loku fyrir það skotið að stærri álar hafi náðst í meira mæli en smærri álar þar sem stærð
fiska skiptir máli upp á hve vel þeir sleppa óskaddaðir í gengum vélar virkjunarinnar.
Niðurstöður
Alls bárast 105 bjartálar til
skoðunar, vora flestir árið 2005
eða 29 en enginn árið 2002 og
einn árið 2000. Meðallengdir
vora breytilegar milli ára, en yfir
allt tímabilið var meðallengdin
75,4 cm (SD=11,0) en spönnin
var frá 54,5-103,0 cm (tafla 1 og
mynd 1).
Allir fiskamir vora hrygnur.
Magainnihald var skoðað hjá
öllum fiskunum og reyndust þeir allir vera tómir.
Tafla 1. Meðallengdir og meðalþyngdir bjartáls eftir áram í
Elliðaánum yfir árabilin 1998-2001 og 2003-2005.
Meðal- SD af Meðal- SD af
Ár N lengd (cm) lengd þyngd (g) þyngd
1998 15 77,2 5,02 926,7 251,6
1999 15 72,8 7,85 756,8 254,6
2000 1 92,0 1350,0
2001 4 83,0 5,35 1095,0 263,5
2002 0
2003 28 76,1 12,76 843,4 516,2
2004 13 73,3 13,16 822,7 479,4
2005 29 74,3 12,08 860,7 477,7
AUs 105 75,4 11,02 867,1 432,2
3
Þy
ng
d
(g
)
12
Lengd (cm)
l.mynd. Lengdardreifingbjartála úr Elliðaám 1998-2001 og
2003-2005.
Lengd (cm)
2. mynd. Samband lengdar og þyngdarhjá bjartál úr Elliðaám. Jafna línunnar er
inn á myndinni.
4
Þegar lengdar - þyngdar
samband bjartálsins (2. mynd)
var kannað reyndist jafna
sambandsins vera veldisfall:
Y = 25,2 e°’0458X
Samband lengdar og þyngdar
er ólíkt hjá ál miðað við
margar aðrar fisktegundir eins
og lögun hans gefur til kynna.
Göngutími bjartálsins var frá
247. ársdegi til 363. ársdags en
megingangan var frá um
miðjum september (260.
ársdegi) til miðs nóvember (3.
mynd). Samkvæmt 3 mynd. Göngutími bjartáls niður úr Elliðaám og Elliðavatni.
fyrirliggjandi gögnum gengu
flestir fiskar þann 14. október.
Aldur var lesinn af 33
bjartálum og var niðurstaðan
sú að aldursbilið var frá 13 upp
í 40 ár. Lengd jókst með
auknum aldri en samt voru
nokkrir fískar sem voru
hlutfallslega stórir miðað við
aldur (sjá 4. mynd) á bilinu 18-
21 cm. Þrátt fyrir þetta var
marktækt samhengi milli
lengdar og aldurs (R2=0,57 og
P<0,001).
4. mynd. Meðallengd eftir aldri hjá bjartál í Elliðaám.
901 n n
80 ■ n n
70 ■ ~ 1
60 ■ r i —
5oJ l . l 1 . 1 I . . L J J l . l 1 .1 1.1 1. 1 l . l . I I .
13 19 21 23 25 29 31 33 36 38 40
Aldur (ár)
3 0 '
2 5 '
2 0 '
1 5 '
1 0 '
Std. Dev = 18,95
Mean = 291
N = 104,00
Dagur ársins
5
Umræða
Ekki eru til miklar upplýsingar um bjartál á íslandi. Helst er að finna nokkrar niðurstöður úr
rannsókn Magnúsar Jóhannssonar o.fl. (1996) um grundvöll fyrir veiðum á ál. I þeirri rannsókn
var veitt í tveimur vötnum á Suðurlandi, Ásgautsstaðavatni og Kakkarvatni en einnig í affalli
nokkurra vatna sem heitir Skerflóð. Lengdir bjartála úr þessu verkefni voru heldur minni en frá
greinir í þessari rannsókn eða mest á milli 50-75 cm og að meðaltali um 60 cm en bjartállinn úr
Elliðaám var um 75 cm að meðaltali og spönnin frá 50-100 cm. í umræddu verkefni voru bæði
veiddir gulálar og bjartálar. Reyndist bjartállinn umtalsvert þyngri miðað við lengd og því
feitari, enda er hann að safna orku til fararinnar miklu til Þanghafsins. Magnús o.fl. (1996)
komust einnig að því að helsti göngutími bjartáls var frá síðari hluta september fram í viku af
október. Gangan hætti því nokkuð fyrr en í Elliðaám en þar var megingangan frá miðjum
september, líkt og í Skerflóði, en hélst fram í miðjan nóvember með hámarki um miðjan október.
Miðað við rannsóknina á Suðurlandi er mikill munur á vexti álsins. Aldursdreifing er allt önnur
í bjartálnum þar heldur en var í Elliðaám. Aldur bjartáls í Skerflóði var frá 6 -15 ára en til
samanburðar var hann frá 13 - 40 ára í Elliðaám. Geta verður þess þó að aldursgreining
álakvama er ekki auðveld og Ámi Kristmundsson sem aldursgreindi álinn í Elliðaám bar sínar
greiningar undir sérfræðing erlendis sem vanur er aldursgreiningum á ál. Einnig hefur komið til
ný og betri tækni til aldurgreininga eftir að hægt var að taka skýrar myndir af kvömum og lesa
aldur af tölvuskjá. Vert væri því að greina aldur úr kvömum Magnúsar og félaga með sama hætti
og bera saman niðurstöður þessara tveggja rannsókna á þeim gmnni.
En hverju sem því liður er aldur
áls í Elliðaám mjög hár miðað við
aldur annarra ferskvatnsfiska sem
hérlendis lifa. Miðað við að álar
sem era orðnir 40 ára og að nálgast
100 cm að lengd (að ffádreginni
lengd glerálsins) þá er vöxtur þeirra
ekki nema 2,0-2,5 cm á ári.
5. mynd. K vöm úr bjartál í Elliðaám. Árin merkt m eð gulum punktum.
6
Taka verður fram að þó rætt hafí verið um ál í Elliðaám er líklegt að mestur hluti hans hafi alist
upp í Elliðavatni. Lítið hefur orðið vart við ál þegar rannsóknir hafa farið fram á seiðum laxfíska
í ánum, þó þær hafí staðið yfír í rúm tuttugu ár, en nokkuð hefur veiðst af ál í Elliðavatni þegar
það hefur verið reynt.
Þó enn vanti umtalsvert upp á heildstæða mynd af lífsferli álsins hérlendis hafa samt aflast
upplýsingar um glerál, gulál, fæðu áls, erfðafræði og sjúkdóma á síðustu tveimur áratugum. Þær
niðurstöður sem hér birtast, auka nokkuð við þá þekkingu.
Þakkarorð
Starfsmenn við rafstöðina í Elliðaám söfnuðu bjartál. Samstarfsmenn mínir á Veiðimálastofnun
aðstoðuðu á margan hátt við sýnatökur og Ámi Kristmundsson fisksjúkdómafræðingur
aldursgreindi álinn. Guðni Guðbergsson og Ámi Kristmundsson lásu yfír handrit og færðu margt
til betri vegar. Þessum aðilum öllum er kærlega þakkað.
Heimildir
Albert, V., Jónsson, B. and Bematchez, L. (2006). Natural hybrids in Atlantic eels (Anguilla
anguilla, A. rostrata): evidence for successful reproduction and fluctuating abundance in
space and time. Molecular Ecology 15: 1903-1916
Avise, J.C., Nelson W.S., Amold J., Koehn, R.K., Williams, G.C. and Thorsteinsson V. (1990).
The evolutionary genetic status of Icelandic eels. Evolution 44:1254-1262.
Ámi Kristmundsson 2003. Sjúkdómar/sníkjudýr í villtum álum, Anguilla spp., á íslandi. M.Sc.
ritgerð við Raunvísindadeild Háskóla íslands. 78 bls.
Ámi Kristmundsson and Sigurdur Helgason 2007. Parasite communities of eels Anguilla
anguilla in freshwater and marine habitats in Iceland in comparison with other parasite
comminities of eels in Europe. Folia Parasitologica 54: 141-153.
Boetius, J. (1980). Atlantic Anguilla. A presentation of old and new data of total numbers of
vertebrae with special reference to the occurrence of Anguilla rostrata in Europe. Dana.
Charlottenlund 1:93-l 12.
Jónsson, B. and Noakes, D.L.G. (2001). Icelandic eels. In: Proceedings o f the Intemational
Symposium: Adcances in eel biology (Y. Auditorium, ed.), pp. 33-35, Tokyo, Japan.
Kuroki, M., Kawai, M., Jónsson, B., Aoyama, J., Miller, M.J., Noakes, D.L.G. and Tsukamoto,
7
K. (2008). Inshore migration and otolith microstructure/mircrochemistry af anguillid glass eels
recruited to Iceland. Environmental Biology of Fishes 83:309-325.
Linton, E.D., Jónsson, B., and Noakes D.L.G. (2007). Effects of water temperature on the
swimming and climbing behavior of glass eels, Anguilla spp. Environmental Biology of Fishes
78:189-192.
Magnús Jóhannsson, Róbert Jónsson og Björn Ingi Bjömsson (1996). Veiðar, vinnsla og sala á
ál. Skýrsla Veiðimálastofnunar VMST-S/96001. 24 bls.
Stefán Már Stefánsson 2000. Fæðuval álsins (Anguilla sp.) í Vifilsstaðavatni. Ritgerð fimm
eininga rannsóknarverkeínis. Háskóli Islands, líffræðiskor, Hólum.
Tesch, F.W. (1977). The eel, biology and management of anguillid eels. Chapman and Hall,
London. 434 bls.
Þórólfur Antonsson og Friðþjófúr Ámason (2011). Elliðaár 2010. Rannsóknir á fiskistofnum
vatnakerfísins. VMST/11030. 38bls.
132 | Joint EIFAAC/ICES/CFCM WCEEL REPORT 2 01 4
9 ToR g) Provide guidance on managem ent measures that can be
applied to both EU and non-EU waters
9.1 In troduction
The information in this chapter will be important in guiding new participants to
WGEEL and non-EU countries as to the possible management options that could be
applied in their regions and to considerations of future post-evaluations of EU eel man-
agement plans, and of other management plans outside of the EU.
It should be noted that there is some disparity among Member States regarding the
degree of realisation of these measures: some Members States appear to be implement-
ing the foreseen measures according to their schedule, while others are lagging behind.
However in the following analysis, the apparent absence of management measures of
a particular type does not necessarily indicate a lack of appropriate action, since, for
example, a country that has never had a commercial fishery could not be expected to
take management measures to control one.
During the creation of the Eel Regulation in 2007 the Council of the European Union
noted that in relation to eel there are diverse conditions and needs throughout the
Community which will require different specific solutions. That diversity should be
taken into account in the planning and execution of management measures to ensure
protection and sustainable use of the eel population. In order to ensure that their eel
recovery measures were effective and equitable, it was necessary that Member States
identified the measures they intended to take and the areas to be covered, that this
information be communicated widely and that the effectiveness of the measures be
evaluated.
To that effect Articles 2(8) & 2(10) of the 2007 Eel Regulation 1100/2007 state that:
(8) An Eel Management Plan may contain but is not limited to, the following measures:
• Reducing commercial fishing activity.
• Restricting recreational fishing.
• Restocking measures.
• Structural measures to make rivers passable and improve river habitats, to-
gether with other environmental measures.
• Transportation of silver eel from inland waters to waters from which they
can escape freely to the Sargasso Sea.
• Combating predators*
• Temporary switching off hydro-electric power turbines.
• Measures related to aquaculture.
(10) In the Eel Management Plan, each Member State shall implement appropriate
measures as soon as possible to reduce the eel mortality caused by factors outside the
fishery, including hydroelectric turbines, pumps or predators, unless this is not neces-
sary to attain the objective of the plan.
*Given that the ToR for this section related only to anthropogenic impacts, man-
agement actions undertaken or proposed in relation to Combating Predators were
not included.
Joint EIFAAC/ICES/GFCM WCEEL REPORT 2 01 4 | 133
9 .2 Analysis o f M anagem ent Measures reported
Differing management structures within the EU mean that EMPs and assessment pro-
cedures vary between Member States. Information and data relating to management
measures were obtained from ICES WKEPEMP report (ICES, 2013a), previous ICES
Reports and the Country Reports to the WGEEL from 2013 & 2014, with the list of
Countries included in the analysis derived from Table 10.3 of the WGEEL 2013 report
(ICES, 2013b).
A total of 1362 individual management actions were reported from the 81 EMUs estab-
lished by Member States for the implementation of their EMPs, the precise details of
which can be found in ICES (2013a).
Given the voiume of management measures adopted across the EU, it was decided for
the purposes of this report to filter the available data under the classification of man-
agement actions listed in ICES WKEPEMP (ICES, 2013a), which were:
• Commercial fishery
• Recreational fishery
• Hydropower and obstacles
• Plabitat improvement
• Stocking
• Others
Management actions aimed at control of commercial and/or recreational fisheries were
the most commonly adopted, with slightly fewer measures addressing hydropower
and obstacles to eel movements, and fewer still implementing habitat improvement or
stocking measures (Figure 9.1).
Figure 9.1. The proportion of management actions of various categories implemented in EMPs
across the EU.
|
Commercial fishing
Recreational fishing
Hydropow er and
obstacles
Habitat im provem ent
Stocking
a Others
134 | Joint EiFAAC/ICES/CFCM WCEEL REPORT 2 0 1 4
9.2.1 Aquaculture
Though listed in the Eel Regulation as a possible feature of management measures no
Member States reported any direct actions related to aquaculture.
9.2.2 Fisheries
9.2.2.1 Commercial fishery
Across the EU, 17 countries have adopted management measures to reduce the impact
of commercial and recreational fishing on the eel stock (Figures 9.2 and 9.3). Despite
the large variety of measures proposed by each country, they are in general devoted to
reducing fishing effort, size limit, and to implementing national registers for catches.
In the majority of cases such actions were driven by:
• improvements in fishery administration systems;
• the introduction or extension of closed seasons;
• a reduction in fishing effort..
The diversity of commercial fishery management measures was large but the variation
within these different categories was even larger, ranging from the prohibition of spe-
cific fishing gears such as fykenets in a particular fishing area, to a total ban of com-
mercial eel fisheries (e.g. Norway and Ireland).
Figure 9.2. EU and non-EU countries adopting management measures affecting commercial eel
fisheries: green = measures either in place or intended; white = no known measures; grey= no data.
(Distribution of countries taking measures remains the same, for all life stages of eel).
jo in t EIFAAC/ICES/CFCM WGEEL REPORT 2 014
9.2.2.2 Recreational fishery
I 135
Figure 9.3. EU and non-EU countries adopting management measures affecting recreational fishing
for eel: green = measures either in place or intended; white = no known measures; grey= no data.
The management measures adopted to reduce the impact of recreational fishing on eel
populations covered a wide range of actions, similar in many ways to those used in the
commercial fisheries, and included:
• a complete ban on targeting or capturing eel;
• restricting the fishery at certain periods or liíe stages (e.g. implementing
closed seasons);
• introducing a quota to reduce the numbers caught;
• adjusting gears and hours of fishing thereby reducing their efficiency;
• regulating the fisheries by implementing systems to report catches;
• increase minimum size limit.
9.2.3 Hydroelectric turbines, pumps and obstacles
The impact of hydroelectric turbines and proposed mitigation measures to aid eel
movements were the subject of previous reviews by WGEEL (ICES, 2004; 2008). Exten-
sive reviews focusing on eel passage were produced by the UK Environment Agency
as part of their Eel Manual in 2011;
https://www.gov.uk/govemment/uploads/system/uploads/attach-
ment_data/file/297341/geho0411btqb-e-e.pdf eel passage
https://www.gov.uk/govemment/uploads/system/uploads/attach-
136 jo in t E1FAAC/ ICES/GFCM WCEEL REPORT 2 0 1 4
EMP measures that are intended to mitigate for the problems caused by hydropower,
pumps and obstacles are detailed in Country Reports and their distribution across the
EU is illustrated in Figure 9.4.
It should be noted that whilst coverage of these measures looks w'idespread across
Member States, many of the measures proposed in national or EMU eel management
plans have not yet been implemented or are oniy partially implemented. All continen-
tal life-history stages of eel can be adversely affected by these type of migratory im-
passes. Juvenile eels (glass eei and small yellow eeis) may be obstructed in their
upstream migrations. Silver eels, and large yellow eels in some locations, can be de-
layed in downstream migration due to river discharge regulation and they are likely
to experience significant mortality rates associated with passage downstream through
power generation facilities. Such mortalities, and non-fatal injuries, can result from ei-
ther impingement at turbine intake screens or following entrainment and passage
through turbines. Similar adverse effects on eels can occur at pumping stations, though
generally EMP measures do not specifically address these. However, many of the hy-
dropower mitigation measures are also relevant to problems associated with pumping
stations and other anthropogenic obstacles impeding riverine eel migrations.
Facilitation of natural upstream migration in hydropower impacted eel populations
has been proposed by eight countries in respect of giass eel and nine countries in re-
spect of small yellow eel. This involves either removal of barriers or installation of ap-
propriate eel pass structures. Likewise, removai of obstacles and/or provision of eel
pass facilities has been proposed by nine countries for larger yellow eels and by five
countries for silver eei migrating downstream.
Management measures involving hydropower plant operational protocols or design
features are proposed measures in eleven Member States, though the specific details
are unciear or are subject to future technology advances. A short to medium-term
measure included in the EMPs for several countries is the trapping of silver eels up-
stream o£ hydropower dams for release downstream. This measure aiso provides in-
come for eel fishermen affected by EMP restrictions on commercial eel capture as their
skills are re-employed in such conservation fisheries. Research and surveys to docu-
ment the impact of hydropower on eel populations of individual EMUs have been pro-
posed by seven countries and a number of others lísted a small number of "other"
related measures that appear to be of limited applicability to EMPs elsewhere.
Joint EIFAAC/ICES/CFCM WCEEL REPORT 2 01 4 137
:•*. /
Figure 9.4. EU and non-EU countries adopting management measures relating to hydropower and
obstacles: green = measures either in place or intended; white = no known measures; grey= no data.
9.2.4 Habitat improvement
Measures categorised as habitat improvement in the ICES WKEPEMP report (2013a)
and the Country Reports to the WGEEL in 2014 (see Annex 10) were reported by only
six Member States. The specific measures taken comprise a variety of actions that are
often somewhat vague in nature, ranging from those broadly relating to increasing
habitat connectivity, and water quality improvement, to the adoption of protected ar-
eas, and the benefit to the eel as a consequence of the application of the Water Frame-
work Directive. Broad similarity of measures between countries cannot be assumed.
The distribution of habitat improvement measures by country affecting all eel life
stages is showm in Figure 9.5. Maps for individual life stages are identical, since habitat
improvement measures generally have wide ranging impacts that affect all life stages.
138 | Joint EIFAAC/ICES/GFCM WGEEL REPORT 2 0 1 4
Figure 9.5. Management measures related to Habitat Improvement taken by country affecting all
eel life stages: green = measures either in place or intended; white = no known measures; grey= no
data.
9.2.5 Stocking
In 2008, prior to the inception of EMPs in 2009, twelve countries proposed the use of
stocking in their management plans to enhance eel populations. In 2013, stocking of
glass eel was undertaken in 16 Member States (Figure 9.6). Whilst stocking is a measure
featuring in virtually all of the EMPs for which there are data, only six achieved their
EMP stocking target. Most EMUs have partially reached their targets and a few have
yet to implement the action (ICES, 2013a).
The most common reason given for a country being unable to achieve its stocking tar-
get was a lack of funding to buy glass eel. The impact of holding and maintenance-
feeding of elvers in aquaculture needs to be addressed with regard to their potential
adaptation to culture conditions which are subsequently deleterious when stocked out,
as known from other fish species like salmon and trout.
Given the unknown nature of some of the eel pathogens in the wild, biosecurity must
be of highest priority in any transport/translocation or eel culture system. All equip-
ment, vehicles, tanks, personnel and clothing must be thoroughly disinfected before
and after any contact with eels and critical control points should be established at all
rearing/holding fadlities. Stocking with on grown young yellow eel carries the risk of
spreading disease, reduced genetic fitness and skewed sex ratios, while the stocking of
wild-caught yoimg yellow eels from clean donor sites may be deleterious if they are
stocked in contaminated recipient sites (Walker et al., 2009).
Joint EIFAAC/ICES/CFCM WCEEL REPORT 2014 I 139
Concems about current eel stocking practices have been expressed and its effective
contribution to ensure increased silver eel production has been raised. It has been rec-
ommended that there should be a co-ordinated marking programme of stocked eel and
thereby separable from wild eel in subsequent sampling.
The effects of stocking under EMPs cannot be demonstrated immediately because of
the generational lag time but recent Swedish work indicates that stocked eels behave
in the same way as natural recruits (ICES, 2013b).WGEEL reviewed the use of stocking
as a management measure in their reports from 2010 and 2013 (ICES 2010 & 2013b).
There was almost no new evidence available to WGEEL in 2013 that was not consid-
ered by ICES WGEEL in its 2010 report and the conclusions of both are similar, i.e. that
there is evidence that translocated and stocked eel can contribute to yellow and silver
eel production in recipient waters, but that evidence of further contribution to actual
spawning is limited (by the general lack of knowledge of the spawning of any eel).
Figure 9.6. Management measures related to Stocking taken by country: green = measures either in
place or intended; white = no known measures; grey= no data.
9.2.6 Other management options
Other management options listed by Member States in their EMPs and associated Re-
ports, include a wide range of actions, none of which effectively refer strictly to man-
aging an anthropogenic impact but mostly to other issues ranging from legal
framework enhancement to monitoring and research.
Other management options essentially fall under eight main subgroups:
1) Strengthening of the framework, including:
1 .1 ) Reinforcement of legal framework;
140 | jo in t EIFAAC/ICES/CFCM WCEEL REPORT 2 0 1 4
1.2 ) Reinforcement of co-ordination among agencies and interested par-
ties;
1.3 ) Dissemination, raising of awareness;
1.4) Stakeholders' involvement.
2 ) Reinforcement of fishery reporting structures, including
2.1) Setting up of fisheries reporting systems (other than DCF);
2.2) Use of import/export data to monitor commercial fisheries;
2 .3) Use of catch/retum logbooks to monitor commercial fisheries;
2.4 ) Improvement of fisheries control (enforcement);
2.5 ) Control and contrast of illegal fisheries (enforcement).
3 ) Reinforcement of monitoring frameworks, including
3.1) Catchment surveys, by fykenet or electrofishing (both multispecific
or eel-specific) in defined catchments;
3.2) Establishment of new, or the continuation of existing recruitment
monitoring, most specific for glass eel and many aiming at investigat-
ing potential new sites;
3.3 ) Assessment of sites for silver eel monitoring, the implementation of
or continuation of escapement monitoring;
3.4) Continuation of monitoring of index rivers.
4 ) Assessment of efficacy of technical actions, to
4.1) Enhance accessibility and migration routes;
4.2) Reduce impacts and iosses on eel populations.
5 ) Actions related to restocking, including
5.1) Identification of areas for restocking;
5.2) Implementation of restocking plans;
5.3 ) Investigations of contribution of stocking to the eel stock;
5.4) Pilot studies for restocking actions.
6 ) Actions related to eel quality issues and fish health, such as
6.1) Monitoring of Anguillicola crassus;
6.2 ) Investigations on pathogens and contamination;
6.3) Implementation of sanitary agreements specific for dealers;
6.4 ) Assurance of compliance to Fish Health Directive.
7 ) Inclusion of eel within specific conservation or species protection pro-
grammes.
8 ) Research actions, generic or specifically aimed at:
8.1) Development of models for the assessment of stock indicators;
8.2 ) Development of models to assess compliance with targets;
Joint EIFAAC/ICES/GFCM WGEEL REPORT 2 01 4
8.3 ) Development of indices for assessing management effectiveness;
8.4 ) Setting up of river or basin indexes for recruitment and escapement
quantification;
8.5 ) Development of ecosystem-based models specific for eel;
8 .6 ) Retrieving and analysing historical data.
Some of these actions refer specificaliy to eel stage, i.e. glass eel, yellow and silver eel:
such is the case with specific monitoring targeting recruitment, yellow eel stock or es-
capement. Most of the management options listed here refer to all eel life stages be-
cause they are generic or aimed at enhancing the knowledge base or the general
working framework.
9 .3 Post-evaluation
Ln 2013, the European Commission stated that Member States have been progressively
implementing more and more management measures as foreseen in their EMPs. These
measures include fisheries restrictions, restocking, facilitation of upstream and down-
stream migration, etc. There is however some disparity among Member States regard-
ing the degree of realisation of these measures: some Members States appear to be
implementing the foreseen measures according to schedule, while others are lagging
behind. Some of the most challenging measures to implement are the removal or mod-
ification of large obstacles, usually due to technical and finandal constraints. The re-
covery plans have oniy been in place for several years with many having been
submitted late (ranging from several months to almost two years after the deadline).
Given that it will take at least 2-3 eel generations (i.e. at least ten years) before any
significant trends in the stock status can be observed, it is too early to draw conclusions
as to the effectiveness of these measures.
Of the 81 EMUs established by Member States for the implementation of their EMPs,
progress was made in implementing management measures related to fisheries, but
other anthropogenic management measures, such as improving habitats and passage,
or achieving stocking targets have often been postponed or only partially imple-
m e n t e d . _______ ___________ —— --------------------------------------------- —----
Following the 2012 EMP Reviews (ICES, 2013a) it remains difficult to asses;
come of EMPs against the 40% escapement target spt by the F.ei Regulation. Jhe scien-
tific advrce gleaned from £Ee" sources examined underlines that the effectiveness of
individual management measures cannot always be demonstrated: necessary data are
missing or the measures concerned are not expected to produce their effects immedi-
ately or in the short term. For instance, there is high probability that restrictions on
fisheries for silver eel have contributed to increase in silver eel escapement. However,
management measures targeting eels prior to the silver eel stage (e.g. stocking) are not
expected to have yet contributed to increased silver eel escapement due to generational
lag time (ranging from approximately five years in the Mediterranean lagoons to 25-
30 years in Northem Europe). Non-fisheries measures related to hydropower, pump-
ing stations and migration obstacles are also difficult to evaluate at this point in time,
mainly due to the site specific nature of potential impacts and lack of post evaluation
data.
Joint EIFAAC/ICES/GFCM WGEEL REPORT 2 01 4
The post-evaluation process commencing with the reporting by Member States in 2012
has been first and foremost a synchronized process of national post-evaluations. Na-
tional reports have evaluated to what extent the implementation of the EMP(s) has
been successful, and whether the targets have been achieved.
Conclusions
The stock in the whole distribution area is considered to constitute one single panmictic
population (Palm et al., 2009; Als et al., 2011). This contrasts strongly with the scattered,
small-scale pattem of the continental stock and the national/regional scale of manage-
ment (Dekker, 2000; 2008). Management of the stock by uniform measures all over the
EU (e.g. a common minimum legai size, a common closed season or a shared catch
quotum, etc.) were not feasible or applied, since uniform measures cannot be designed
in a way that would be effective all over the EU (or the wider range of the eel) due to
large variations in eel life history over its natural range.
Regionalised management (a common objective and target, but local action planning,
local measures and local implementation) is central to the EU Eel Regulation (Dekker,
2004; 2009) and on this basis Eel Management Plans have been developed per coun-
try/region. Few cross-boundary EMPs exist. Note, however, that the European eel
range extends beyond the EU and that the management of the eel and anthropogenic
impacts are necessary throughout its range. As such it is hoped that the information
above will be an important and useful reference to new participants to WGEEL and
non-EU countries, suggesting possible management options which could be applied in
their regions and to considerations of future post-evaluations of implemented manage-
ment actions.
Recom m endations
We recommend a comprehensive evaluation of the effectiveness of various manage-
ment measrues across EU and non-EU waters facilitating the prioritisation of manage-
ment actions.
Management guidelines have been produced on various topics; it is recommended that
these are hosted on the EIFAAC web site, so that their specific details can be scruti-
nised.
Heredity (2016), 1 - iO
€ 2016 Macmillan Publishers Limited. part of Springer Nature. All rights reserved 0018-067X/16
w w w .n a tu re .co m /h d y
ORIGINAL ARTICLE
Assessing pre- and post-zygotic barriers between North
Atlantic eels (Anguilla anguilla and A. rostrata)
M W Jacobsen1,5, L Smedegaard1,5, SR Sorensen2, JM Pujolar1, P M unk2, B Jónsson3, E Magnussen4
and M M Hansen1
E lucidating barriers to gene flow is im portant for understanding the dynamics of speciation. Here we investigate pre- and
post-zygotic mechanisms acting between the two hybrid izing species of A tlantíc eels: Angu illa angullla and A. rostrata.
Tem porally varying hybrid ization was examined by analyzing 85 species-díagnostic s ing le-nucleotide polymorphisms (SNPs;
FSx > 0 ,9 5 ) in eel larvae sampled in the spawning region in the Sargasso Sea in 2 0 0 7 (/V = 9 2 ) and 2 0 1 4 ( /V = 460 ). We further
investigated whether genotypes at these SNPs were nonrandomly d istribu ted in pos t-F l hybrids, ind ica ting selection. F inally, we
sequenced the m ítochondria l ATP6 and nuclear A T P 5 c l genes in 19 hybrids, identified using SNP and restriction site
associated DNA (RAD) sequencing data, to test a previously proposed hypothesis of cytonuclear incom patib ility leading to
adenosine triphosphate (ATP) synthase dysfunction and selection against hybrids. No F1 hybrids but only later backcrosses were
observed in the Sargasso Sea in 2 0 0 7 and 2 0 1 4 . This suggests tha t interbreeding between the two species only occurs in some
years, possibly contro lled by environm ental cond itions at the spawning grounds, or th a t interbreeding has d im in ished through
tim e as a result of a dec lin ing number of spawners. Moreover, potential selection was found at the nuclear and the cytonuclear
leveis. Nonetheless, one glass eel ind iv idua l showed a m ism atch, involving an Amerícan ATP6 haplotype and European A T P 5 c l
alleles. This contradicted the presence of cytonuclear incom patib ility but may be explained by th a t (1) cytonuclear
incom pa tib ility is incom plete, (2) selection acts at a later life stage or (3) other genes are im portant fo r protein function . In
to ta l, the study demonstrates the u tility o f genom ic data when exam ining pre- and post-zyotic barriers in natural hybrids.
Heredity advance online publication, 9 November 2016; d o i:10 .1038 /hdy .2016 .96
INTRODUCTION
B lucidating tlie d iffe ren t ty'pes o f p re - o r p o st-zygo tic rep ro d u c d v e
iso la ting b a rrie rs is crucia l fo r u n d e rs ta n d in g sp ec ia tio n (R am sey e t al.,
2003; C o y n e an d O r r 2004; N osil e t a l., 2005; R ieseberg an d W illis,
2007; L ow ry e t a l , 2008). P rezygo tic m e c h an ism s im p ed e m a tin g
th ro u g h , fb r ex am p le , h a b ita t, te m p o ra l o r sexual iso la tion , o r
m ech an ica l iso la tion because o f genita lic in c o m p a tib ility (N osil
e t a l., 2005; Lessios, 2011). O n th e o th e r h a n d , p ostzygo tic selection
acts a fte r tlre zygote has b een fo rm e d because o f red u c ed fitness o f
h yb rid s th a t m a y ev en tually lead to re in fo rce m e n t a n d spec ia tion .
H e re a d is tin c tio n is m a d e b e tw een ex trin s ic a n d in tr in s ic postzygotic
b a rrie rs (M ayr, 1963; N o sil e t al„ 2005; S eehausen et a l , 2014). In
ex trin sic postzygo tic iso la tio n , h y b rid p h en o ty p e s a re m a lad ap te d to
the e n v iro n m e n t re la tive to p a ren ta l p h e n o ty p e s (N osii c t al., 2005;
S ch lu ter, 2009). In tr in s ic p ostzygo tic b a rr ie rs involve g enetic in c o m -
p a tib ility w h en su b o p tim a l allelic c o m b in a tio n s a re b ro u g h t to g e th e r
in hyb rid s . D eleterious co m b in a tio n s wili lead to red u ced fitness o r
in fertility , as d e m o n s tra te d b o th th eo re tica lly (G avrilets, 2003, 2004;
C o y n e a n d O rr , 2004) a n d em piricaU y (B rideau e t al„ 2006;
Presgraves, 2007; M ah e sh w a ri a n d B arbash , 2011). A special case,
th e so -called cy to n u c lea r in co m p a tib ility , involves m ito c h o n d ria l an d
n u c le a r genes (B u rto n e t til., 2013). G en es ffo m b o th g en o m es in te rac t
w ith in p ro te in com plexes o f th e ox ida tive p h o sp h o ry la tio n pa th w ay
th a t is re sponsib le fo r energy (ad en o sin e tr ip h o sp h a te (A T P )) p ro d u c -
tio n (S araste 1999; B allard a n d W h itlo c k , 2004). T h u s , c o ad a p ta tio n
w ith in p o p u la tio n s o r species m ay re su lt in m ism a tch es a n d p ro te in
d y sfu n c tio n in h v b rid s lead ing to re d u c ed fitness (B u rto n et a l , 2013).
E vidence fo r su ch m ism a tch es has b e en sh o w n in several o rgan ism s,
in c lu d in g flies (M eik le jo h n et al„ 2013 ), c o p ep o d s (E llison an d
B u rto n , 2006) a n d m o n k ey flow ers (F ish m an a n d W illis 2006).
N one lheless, th e absence o f co ev o lu tio n is n o t alw ays dele terious.
F o r exam ple, a re c en t s tu d y o f th e redbelly dace (C hrosom us eos)
sh o w ed th a t in tro g re ss io n o f a fo re ign m ito g e n o m e , o f u p to 10 M yr
o f in d e p e n d en t ev o lu tio n , is n o t necessariiy d e le te r io u s b u t m ay ra th e r
h ave benefic ial effects (D e re m ien s et al., 2015). In to ta l, few g o o d cases
o f cy to n u c lea r in co m p a tib ility exist o u ts id e th e la b o ra to ry a n d m o re
em p irica i ev idence is n e ed e d to u n d e rs ta n d th e significance o f th is
m e c h an ism in sp ec ia tio n (B u rto n e t al„ 2013).
H ere w e investigate p re - a n d post-zygo tic b a rrie rs b e tw een th e tw o
siste r species o f N o r th A tlan tic eels: E u ro p ea n (A nguilla anguilla) an d
A m erican eel (A . rostrata) (T esch , 2003). B oth species a re p an m ic tic
(Als et al„ 2011; C ó té e t a l , 2013 ), sh o w h íg h effective p o p u la tio n siz.es
(C ó té e t al„ 2013; P u jo lar e t al., 2013; Jacobsen e t al„ 2014b) an d
spaw n in th e th e rm a l fro n ts o f th e s o u th e m Sargasso Sea (M cC leave
'Department of Bioscience, Aarhus University, Aarhus, Denmark: "’National institute of Aquatic Resources, Charlottenlund, Denmark; '’ Northwest lceland Nature Research
Centre, Saudárkrókur, iceland and '"‘Faculty of Science and Technology, University of the Faroe islands, Torshavn, Faroe Islands
Correspondence: Dr MW Jac.obsen. Departrnent of Bioscience. Aarhus University. Ny Munkegade 114, DK-8000 Aarhus C, Denrnark. E-mail magnus.jacobsen@bios.au.dk
’These authors contributed equally to this work.
Received 14 April 2016; revised 13 August 2016; accepted 22 August 2016
http://www.nature.com/hdy
mailto:magnus.jacobsen@bios.au.dk
Reprodudive isolating barriers in North Atlantic eeis
MW Jacobsen e í al
2
e t al„ 1987; T esch , 2003). T h e ir sp aw n in g show s extensive overlap in
space (S chm id t, 1923; T esch , 2003; M iu ik e t a l , 2010) a n d tim e, w ith
peak sp aw n in g tim e in F e b ru a ty -A p ril fo r A m erican a n d M a rc h -Ju n e
fo r E u ro p ean eel (M cC leave e t a l , 1987; T esch , 2003; M ille r e t al„
2015). A fte r spaw n ing , th e la n 'a e (lep to cep h ali) a re tra n sp o rte d by
ocean c u rre n ts b a ck to th e ir respec tive feed ing g ro u n d s (S chm id t,
1923), w h e re th e y e n te r fresh o r b ra c k ish w a ter as glass eels. A fter a
p e rio d o f 4 -2 0 years as yellow eels, th e y m e ta m o rp h o s e in to silver cels
th a t m ig ra te b a ck to th e Sargasso Sea to sp aw n an d su b seq u en tly d ie
(T esch , 2003). T h e sp aw n in g a n d la rva l m ig ra tio n s a re h igh ly
d iffe ren tia ted in A tlan tic eels w ith a sp aw n in g m ig ra tio n o f
~ 5000 k m fo r E u ro p e a n eel a n d 2500 k m fo r A m e rican eel
(A oyam a, 2009) a n d a s u b se q u e n t d u ra tio n o f larval phases o f ~ 2
years a n d 7 -9 m o n th s (T esch , 2003), respectively , a lth o u g h th is is still
d e b a ted (T esch , 2003; Z e n im o to e t al„ 2011).
M ito g e n o m e seq u en c in g suggests th a t species d ivergence o f A tlan tic
eels w as in itia ted ~ 3 .3 m iilio n years ago (M y r) (Jacobsen e t al„
2014b). H ow ever, g ene flow still o ccu rs, as h y b rid s have b een rc p o rte d
in several s tu d ies (A vise ct aL , 1990; A lb e rt e t a l , 2006; G agnaire e t al„
2009; P u jo la r et aL , 2014a, b ). T h u s , a lth o u g h te m p o ra l a n d spatial
s ep a ra tio n a t th e sp aw n in g g ro u n d s likely c o n stitu te s p rezygotic
b a rrie rs , they a re n o t ab so lu te . N o n e th e less, th e freq u en cy o f
h y b rid iza tio n is u n k n o w n a n d , to d a te , n o F1 h y b rid s have b een
fo u n d in th e Sargasso Sea, w h e re m ere ly tw o seco n d -g e n e ra tio n
backcrosses p rev iousiy have b e en d e tec ted based o n 86 species-
d iag n o stic (Fyx > 0 .9 5 ) s in g le -n u c leo tid e p o ly m o rp h ism s (S N P s) in
sam pies fro m 2007 (P u jo la r e t al„ 2014a). T h e fin d in g o f on ly
backcross ind iv id u a ls b u t n o F1 h y b rid s m ay be exp la ined by
tem p o ra lly vary ing h y b rid iza tio n (P u jo la r e t aL , 2014a). T h is cou ld
re su lt fro m d ifferences in te m p o ra l overiap o f sp aw n in g tim e betw een
th e species across years, p o te n tia lly m e d ia ted b y a n n u a l d ifferences in
th e lo c a tio n o f th e ih e rm a i fro n ts th a t a re h ig h ly d y n a m ic across years
(T esch , 2003; U llm an e t al„ 2007).
F1 h y b rid s have o n ly b een ob serv ed in Ice land (Avise e t al„ 1990;
A lbert et a l , 2006; P u jo la r e t al., 20.14a). T h is is possib ly a co n seq u en ce
o f an in te rm e d ia te la rva l m ig ra tio n b eh aw o r, w h e re F1 h y b rid s e ith e r
actively o r passively ge t t ra n s p o r te d to Ice land , a p p ro x im a te ly lo ca ted
lo n g itu d in a lly in tc rm c d ia tc be tw een N o rth A m erica a n d E u ro p e
(Avise et a l , 1990; P u jo la r e t al„ 2014a). In c o n tin e n ta l E u ro p e and
N o rth A m erica , o n ly few la te r-g e n e ra tio n backcrosses have b een
ob serv ed (A lbert et al„ 2006; P u jo la r e t a l , 2014b), suggesting s tro n g
postzygo tic b a rrie rs . O n e su ch b a rr ie r has b een p ro p o se d to be
cy to n u c lea r in c o m p a tib ility (G ag n a ire e t al„ 2012), b ased o n th e
fin d in g o f s ig n ifican t in te r-sp ec ies n o n sy n o n y m o u s d iffe ren tia tio n in
genes invo lved in th e A T P syn thase co m p lex (G ag n a ire e t a l , 2012).
T h is p ro te in co m p le x is p a r t o f th e ox ida tive p h o sp h o ry la tio n chain
a n d catalyzes th e syn thesis o f A T P f ro m a d en o s in e d ip h o sp h a te
(Saraste, 1999). T h c tvvo genes sh o w in g h ig h est n o n sy n o n y m o u s
d iffe ren tia tio n in A tlan tic eels a re th e m ito c h o n d ria l A T P 6 (A T P
synthasc F0 su b u n it 6) a n d the n u c le a r ATP5cL (A T P synthase F1
su h u n it g a m m a ) genes. T h u s, c o ev o lu tio n likely has o c cu rre d betw een
th ese genes a n d m ism a tch es in h y b rid s a re expec ted to be associaled
w ith postzygo tic selection . S u ch selec tion m ay be lin k ed to the
possib ility o f c o m p le tin g th e m ig ra to ry lo o p ; e ith e r th e sp aw n in g
m ig ra tio n o r th e su b se q u e n t larval phase . B o th life-h isto ry tra its m ay
be associated w ith energetics a n d are sign ifican tly co rre la ted w ith
a m in o acid changes in A T P 6 in fresh w ater eeis (A nguillidae) (Jacobsen
e t al„ 2015 ). A lth o u g h E u ro p ea n eel c an b e re a re d 'm vitro th ro u g h th e
p re lep to cep h a li stage (S o ren sen e t al„ 2016), th e sam e is n o t yet
p ossib le fo r th e A m erican eel an d n o n e o f th e m can p re sen tly be
rea red artificially . T h u s , h y b rid s c an on ly be s tu d ied fro rn w ild -cau g h t
sp ec in ten s (T esch , 2003). H e re rec en t s tu d ie s b ased o n re s tric tio n site
assoc iated D N A (R A D ) seq u en c in g (P u jo la r e t al„ 2014b) an d analysis
o f a su b se t o f sp ec ies-d iagnostic SN Ps (P u jo la r e t al„ 2014a) have
d e tec ted h y b rid s fro rn b e y o n d th e F1 g en era tio n b ackcross levei.
S creen ing fo r u n u su a l A T P 6 ~ A T P 5 cl co m b in a tio n s in su ch hy b rid s
c an be u sed fo r investigating th e possib ility o f cy to n u c lea r in c o m p a t-
ib ility in A tlan tic cels (B licr e t al„ 2001, G ag n airc e t aL , 2012).
T h e use o f sp ec ies-d iagnostic SN Ps to d e tec t h y b rid s m ay , how ever,
involve p o te n tia l p ro b lem s. G e n o m e-w id e d iffe ren tia tio n be tw een
A m erican an d E u ro p ean eel is h ig h ly h e te ro g en eo u s w ith an average
F j t o f 0.041. N evertheless, th o u s a n d s o f SN Ps sh o w fixed differences
a n d are c an d id a te s fo r b e in g u n d e r ciivergent se lec tion be tw een th e
species (Jacobsen e t al„ 2014a). H en ce , it is likely th a t selection acts on
these loci in hyb rid s . As su ch , w h ereas FI h y b rid s sh o u ld be
h e te rozygous fo r all d iag n o stic loci, se lec tion a n d co ad a p ta tio n rnay
d is to r t g eno type frequencies in p o s t-F l hy b rid s , Iead ing to increased
in accu racy in e s tim a tin g n u m b e rs o f g e n era tio n s since in itial
h y b rid iza tio n .
H e re w e ad d ressed th e fo llow ing q u estions. (1) Is th e degree o f
h y b rid iza tio n tem p o ra lly vary ing in th e Sargasso Sea? (2) D oes
selec tion affect d iag n o stic SN Ps an d th e re b y ca teg o riza tio n o f po st-
F1 hybrids? (3) A re A T P 6 ~ A T P 5 c l co m b in a tio n s in p o s t-F l hyb rid s in
a cco rd an ce w itli th e hy p o th esis o f cy to n u c lea r in c o m p a tib ility pa rtly
u n d erly in g postzygo tic b a rr ie rs be tw een th e species? U sing a panel o f
96 n ea r-d iag n o stic SN Ps (P u jo la r e t al„ 2 0 14a) w e analyzed eel larvae
sam p led in th e Sargasso Sea in 2014 ( N = 460), in a d d itio n to new
sam ples fro m M o ro c co (Ar= 2 1 ) a n d th e F aroe Islands ( N = 30). D a ta
w ere u sed fo r assessing te m p o ra l v a ria tio n in h y b rid iza tio n a n d
selec tion in c o m b in a tio n w ith p rev iously p u b lish ed d a ta , in p a rtic u la r
fro m larvae co llected in th e Sargasso Sea in 2007 ( N = 92) and
Ice land ic eels co llected in th e early 2000s ( N = 159). W e ex p ec ted th a t
F1 hy b rid s sh o u ld be o v e rrep re sen te d c o m p a re d w ith backcrosses a t
th e sp aw n in g g ro u n d s b ecause o f postzygo tic barrie rs , in case o f
c o n tin u o u s gene flow b e tw een th e species. F u r th e rm o re , vve sequenced
th e A T P 6 an d A T P 5 c l genes fro m 19 hy b rid s in o rd e r to te st for
species-specific A T P 6 ~ A T P 5 cl m a tch es a n d th u s in d irec tly fo r cyto-
n u c le a r in co m p a tib ility . T hese h y b rid s w ere id en fified in th e p re sen t
an d p rev io u s stud ies (Jacobsen e t al„ 2014a; P u jo la r e t al„ 2014a, b ) by
analyzing spec ies-d iagnostic SN Ps using S T R U C T U R E (P ritch a rd
e t a l , 2000; F a lu sh et a l , 2003, 2007) and N E W H Y B R ID S
(A n d e rso n a n d T h o m p so n , 2002). O verall, o u r s tu d y p ro v id es new
in sigh ts in to th e p re - a n d p o st-zygo tic b a rrie rs invo lved in spec ia tion
ín th e case o f N o r th A tlan tic eels in p a rticu ia r, a n d sp ec ia tio n in th e
o ceans in general.
MATERIALS AND METHODS
Id e n tify in g sp ec ie s a n d h y b r id s a m o n g eel la rv a e f fo m
th e S a rg asso Sea
A total o f 472 candidate Anguilla sp. larvae (leptocephali), sampled in the
Sargasso Sea from 18 March to 15 April 2014, were analyzed io this study. They
represent 47 different Localities along 7 transects at longitude: 68.5°W, 65.5°W,
62.7°W, 59.5°W, 57.0°W, 53.5°W and 50“W (Figures 1 and 2a) and cover the
main part o f the spawning ground shared by the two species that historicatly
híis been ranging from ca. 70 to 58°W (Miller et a l, 2015). A sínglt' sampling
station at longitude 5 i .8°Wr was also included. Sampiing was conducted using a
ring net (diameter: 3.5 m, length: 25 m and nresh size o f 560 pm). Larvae werc
stored in separate eppendorf tubes in either ethanol (96%) or RNAlater. In
addition, new sanrpies also included glass eels colíected in Morocco (Oved
Sebou; íV =21) and yellow eels collected in the Faroe Islands (Streymnes;
N = 15 and Miðvágur; JV= 15) in 2011 (Figure 1 and Table 1).
DNA vvas extractcd using E.Z.N.A. purifications columns (OMEGA Bio-Tek,
Norcross, GA, USA). Species identification was based on PCR o f the
Heredity
Reproductive ísolating barriers in North Atlantic eels
MW Jacobsen et at
3
• n
□ L t1
" i f
□ R H t
C R B f
C M I +
CSTJ
• S A +
□ G G 1
□ g a +
\ \ w
s>míu>i
Q . SNP sicnoivping
□ RAD scqucncmg
BLACK i New data
CiRF-Y t \ e w data publishcd data
WHITT ' Publushcd data
■f j ATP6-ArP5cl sequcncing
Figure 1 Map showing ail íocalities o f new and previously published data anaiyzed ín th is study. Black circles denote localities with new data; gray circles
denote localities with both new and aiready published data and white squares show localities with only data already published. See Table 1 for information
on exact sampling location and sample size.
m itochondriaj cytochrome h gene (CytB) according to Trautner (2006). A total
o f 96 species-diagnostic SNPs (F$y 0.95) developed by Puiolar et a l (2014a)
based on RAD sequencing were then genotyped on 96.96 Dynamic Arrays
(Fluidigm Corporation, San Francisco, CA, USA) using the Fluidigm EPI
instrum entation according to the rnanufacturer’s recommendations. In addi-
tion, genotype data from Pujolar ct al. (2014a), who analyved 280 European ee!s
tor the same 96 SNPs, were reanaiyz.ed in the study. These data consisted o f ecl
larvae collected in the Sargasso Sea (N = 92) in 2007 (caught between 70 and
64°W), yellow and glass eels collectcd in Iceland ( N = 159) in 2000-2003 and
yellow ecls collected in the Faroe Islands (N = 29) in 2011 (for details on exact
sampiing localities see Pujolar et aí., 2014a). ín total, the data set encompassed
803 individuals (Figure land Tahle 1).
All individuals were analvzed using NEWMYBRIDS (Anderson and
Thom pson, 2002). N o prior iníorm ation on ihe origin of individuals was uscd
and an a.ssignment threshold o f >0 .95 was applied. The software assigns
individuais to different hybrid ciasses by calculating the probability o f the
indivídual belonging to a specific hybrid categoiy. In this studv we uscd the
same hybrid categories as i.n Pujolar ct al. (2ÖI4a); pure European eel (AA),
pure American eel (/VR), ftrst-generatson hybrids A A xA R (F l), F1 x f l (F2),
A A x F l (bAA), A R x F l (bAR), bAAxAA, bAA x AR, bA R xAR, bARxAA,
bA A xp'l ancl b A R x F l. T ‘his means that, for example, bA R xA A is an
individual resulting from a pure European eel (AA) mating with a hybrid
backcross (bAR) that again is the result o f a pure American eel (AR) mating
with an F1 hyhrid.
Seven hyforids were assigned to the ‘unusual’ bA RxAA ciass and showed
seven loci that were homozygous in all individuals for the European eel aiiele.
As this is unlikely to happen by chance, and may indicate selection, we
examined these loci further. First, we calcuiated the probability o f observing the
homozygote genotype in all seven individuals. Assuming Hardy-W einberg
proportions we ftrst estimated genotype frequencics in American and European
eel bascd on the allele frequencies observed in each o f the seven bialklic loci.
Subsequently, we used these frequencies to estiniate genotype frequencies in F1
hybrids, backcrosses to American eel (bAR) and bA R x AA hybrids and fm.úly
the individual probabilities (see Supplementarv Notes S1 and S2). Second, the
positions o f alí SNPs were matched to the predicted complementary ÐNA
annotation lile o f the European eel draft genome (Henkel ct. aL, 2012) (http://
www.zfgenomics.com/sub/eel). This allowed us to investigate: (I) whether
SNPs were located within genes (introns+exons) or in noncoding regions; and
(2) the possible íunction o f the gcncs in which those SNPs wcre locatcd. We
were particularly interested in testing whether these genes matched the Gene
Ontology (GO) terms ‘development’ and ‘phosphorylation’ as the recent study
o í Jacobsen et a l (2014a) showed thcse two GO term groups to be
overrepresented in F$-[■ outlier SNPs between European and American eel.
Cytonuclear incompatibility in hybrids
A total o f 19 hybrid individuals were analyzed for the mitochondrial ATP6 and
interacting nucicar ATPScI genes (Table 2). These individuals corresponded to
all previously analyzed hybrid individuals from which DNA or tissue was still
available. The individuals belonged to samples genotyped based on either the
Fluidigm 96.96 Dynamíc Arrays ( N - 12) (Pujolar et al., 2014a; this study) or
RAD sequencing (N = 7) (Pujolar et al., 20i4b). The seven RAD sequenced
individuals from Pujolar eí al. (2014b) were previously analyzed using
STRUCTURE and the ‘gensback’ (G) option. This option aliows testing
whether an individual ha.s an immigrant ancestor in the last G generations
(Pritchard et a l , 2000; Falush et a l , 2003, 2007). However, the study by Pujolar
et al. (2014b) only used a G o f five (corresponding to the fourth-generation
backcross category), and thus some individuais potentially having an older
immigrant ancestor may have been wrongly assigned. As erroneous hybrid
assignment may bias the assessment o f possible cytonuclear selection, we
reanalyzed the data using a G option o f 9 (corresponding to the eight-
generatíon backcross category) and furtherm ore evaluated assignnient power in
STRUCTURE, This is described in detail in Supplementary Note S3.
Both the mitochondrial ATP6 gene that contains five species-diagnostic
nonsynonymous changes and the pait o f the nuclear interactor ATPScl that
Heredity
http://www.zfgenomics.com/sub/eel
Reproductive isolating barriers in North Atiantic eels
MW Jacobsen et al
USA TRANSECTS: T1 T2 T3 T4 T5 T6 T7
4-
i
CUBA
0
H aiti
DO M . R£P.
t#
J J ( 7 4 )
-68.5
4
(1)
J 2 < 2 5 )
-65.5
4-
J 3 (1 9 8 )
-62.7
4
(5 /ÍHYÍC)
J 4 ( 8 0 )
-59.5
4
T5(47)
-57.0
4
T6(47)
-53.5
4
T7(5)
-50.0 Longitudes
4 Lattitude
430.0
•k
1211
w (31)
(6)
4 (16)
^ ( 12)
(5)
' : . (I)
■
%(6)
9
^ .
''ii;: (3)
^(9)
k
1125
1(2X3)
(2X11)
1(6)
SYM BOL SPECIES
% Angnilla rostrata
c % A nguilla anguilla
•k Hybrid caught in 2007
O H ybrid caught in 2014
I
428.9
427.9
( 1 )
<3> 426.8
( 1 )
425.8
424.7
Figure 2 Maps showing (a) sampling localities of the leptocephali larvae caught during the 2 0 1 4 expedition and genotyped in th is study, and (b) the
frequencies of the two species at each of the localities sampled during the 20 1 4 expedition. The two red circles denote the localities from which hybrids
(bARxAA) were detected in 2 0 1 4 and red asterisks show the positions of two hybrids found among larvae sampled in 2007 . The numbers in brackets
denote sample sizes of analyzed larvae for each locality.
covers two quasi-diagnostic nonsynonymous SNPs positioned in the seventh
exon were sequenced. Primers developed by Gagnaire et al. (2012) were used
(Supplementary Table Sl). PCR was perform ed in 20 pl reactions containing
10 pl RedTaq mix (SIGMA-ALDRICH, Brondby, Denmark), 0.25 mw o f each
prim er and 50-100 ng o f DNA. The amplification parameters were: 94 °C for
5 m in, followed by 38 cycles (94 °C for 30 s, 60 °C o r 30 s, 72 °C for 45 s) and
finally 5 m in at 72 °C. Sequencing was conducted using the commercial service
provided by Macrogen (Amsterdam, Holland). The forward primers Ang-
ATP6-L and ATP-ATP5cl-6L were used íor sequencing. Sequence identity was
assessed using BLAST (AlLschul et a l, 1997) (http://blast.ncbi.nlm.nih.gov) for
the ATP6 gene and by evaluating the genotypes at the two quasi-diagnostic
SNPs for ATP5cl gene.
For all analyzed hybrids, the probability o f obtaining the observed ATP5cl
genotypes was calculated based on the assigned hvbrid classes, and the observed
species-specific allele frequencies o f ATP5cl from Gagnaire et al. (2012)
(American = 1/120 and European eel = 76/0 (the numbers correspond to the
frequency ofE uropean and American alleles observed in each species)). H ardy-
Weinberg proportions were assumed. The subsequent P-vitlues were used to
infer deviations from neutral expectations and in combination with the
mitogenome data used to assess possible cytonuclear incompatibility.
RESULTS
Species distribution in the Sargasso Sea and identification
of hybrids
Species id en tifica tio n o f th e eel larvae co llected in 2014, b a sed o n th e
m ito c h o n d ria l cytochrome b gene, revealed a h ig h e r p ro p o r tio n o f
A m erican th a n E u ro p ean eel in th e tw o w e s te rn m o s t tran sec ts
(F igures 2a a n d b ). T h e freq u en cy o f E u ro p ean eel in c rea sed in the
eastw ard d irc c tio n a n d re ach ed 100% fo r th e fo u r e a s te m m o s t
tran sec ts (F igu re 2b). A t tran sec ts 1 -4 , larvae fro m b o th species w ere
fo u n d , in d ica tin g so m e spatia l ov e rlap o f sp aw n in g g ro u n d s . A m o n g
460 larvae, 358 sh o w ed the E u ro p ean eel CYTB gene, w hereas 102
sh o w ed th e A m e rican eel CYTB gene. T h e d ifference in th e n u m b e r o f
E u ro p ean a n d A m erican eel c au g h t is to so m e ex te n t re la ted to
sam pling , as th e e a s te rn m o s t localities sam p led are expec ted to be
d o m in a te d b y E u ro p e a n eel. A qualita tive ly s im ila r d is tr ib u tio n o f
species in th e Sargasso Sea w as observed in 2007 (M u n k et a l, 2010),
a lth o u g h th e h y b rid la rvae w ere cau g th slightly m o re w estw ards in
2007 (F igure 2b).
Heredity
http://blast.ncbi.nlm.nih.gov
Reproductíve isolating barríers in North Atlantic eels
MW Jacobsen et ai
5
Table 1 Overvtew over samplirtg localities, sample sizes and sequencing approaches of new and reanalyzed data
Locaiity Country Codes Year Sample sizes
New data Published data
Life stage Sequencing approach
Oved Sebou Morocco MA 2011 21 — G SNP genotyping
Faroe Isiands Faroe islands Fi 2011 30 29 Y SNP genotyping
Sargasso Sea — SA 2014/2007 460a 92 L SNP genotyping
iceland Iceland IL 2000-2003 _ 96/63 G/Y SNP genotyping
Lough Erneb Northern Ireiand LE 2008 — 7 G RAD sequencing
Canetb France CA 2008 _ 2 G RAD sequencing
Valenciab Spam VA 2008 _ 7 G RAD sequencing
Rlnghals!> Sweden RH 2008 _ 8 G RAD sequencing
Girondeb France GG 2008 _ 1 G RAD sequencing
St. John riverb USA STJ 1999 — 2 Y RAD sequencing
Mira Riverb Canada Ml 2007 _ 8 G RAD sequencing
Ríviere B!ancheb Canada R8 2007 5/7 G/Y RAD sequencing
Abbreviations: G, gíass eei; Y, yeiiow eei; L, iarvae (leptocephaius); SNP genotyping, Fluidigm singie-nucieotide poiymorphism genotyping; RAD, restriction site associated DNA.
dlnitia!iy, 472 anaiyzed individuais but somewhere discarded because of data quaiity (see results).
bRAD sequenced mdividuals used for hybrid assessment and power anaiysis m STRUCTURE (Suppiementary Note S3).
Table 2 Results of ATP6 and ATP5cl sequencing from the 19 hybrid samples
Individua! Information on individuals Country Information on estimated hybrid classes Sequencing resuits
Location Life stage Year Hybrid cias^ Vaiidation method ATP6 ATP5c1
Steíni Steinsmyrarfljot Y 2000 lceland F1 SNP genotyping AA Heterozygote
Vogsi9 Vogslaekur G 2001 iceíand F1 SNP genotyping AA Heterozygote
Vogsíii Vogslaekur G 2001 iceland F1 SNP genotyping AA Heterozygote
Vifi!2 Vifilsstadvatn G 2002 lceland F1 SNP genotyping AR Heterozygote
STG3 Stokkseyri G 2001 lceland F1 SNP genotyping AA Heterozygote
SSG7 Seijar G 2001 iceíand F1 SNP genotyping AA Heterozygote
SSG10 Seijar G 2001 iceland F1 SNP genotyping AA Heterozygote
Vogsl5 Vogsiaekur G 2001 Iceiand bARxAA SNP genotypíng AA Homozygote AA
VífiiS Vifiisstadvatn Y 2002 lceland bARxAA SNP genotyping AA Heterozygote
STG2 Stokkseyri G 2001 lceland bARxAA SNP genotyping AA Heterozygote
L211 Sargasso Sea L 2007 — bARxAA SNP genotyping AA Homozygote AA
40-450-L2 Sargasso Sea L 2014 — bAR x AA SNP genotyping AA Homozygote AA
NEG3 Mira River G 2007 Canada Third-generation backcross AR RAD sequencing AR Homozygote AR
GG14 Gironde G 2008 France Fourth-generation backcross AA RAD sequencing AA Homozygote AA
RH24 Ringhals G 2008 Sweden Fourth-generation backcross AA RAD sequencing AA Homozygote AA
Cag25 Canet G 2008 France Fifth-generation backcross AA RAD sequencing AA Homozygote AA
C ag l17 Canet G 2008 France Fifth-generation backcross AA RAD sequencing AA Homozygote AA
RBG10 Riviere Blanche G 2007 Canada Later or equal to síxth-generation
backcross AR
RAD sequencing AA Heterozygote
LEG29 Lough Erne G 2008 North
Ireland
Later or equal to sixth-generation
backcross AA
RAD sequencing AR Homozygote AA
Abbreviations; AA, European eel í'A ngu ilia angu illah AR, American ee! ÍAnguilia rostrata); ATP6, m ito c h o n d r ia fA T P S c l, nuciear: G, glass eei; Y, yeiiow eei; L, iarvae (leptocephaius); SNP
genctyping, Fiuidigm smgle-nucleotide poiymorphism genotyping; RAD, restriction site associated DNA.
Tlie presented hybrid ciasses are the ones estimated in this study (see Materíals and methods and Supplementary Notes S3 and S4).
,:The 'bAR x AA' category denotes a second-generatíon backcross; the resuit of a mating beíween a backcrossed male American individua! (F1 xAR) and a female European eel (AA).
O f th e 96 S N Ps g en o ty p ed o n tlie F lu id ig m array , 11 sh o w ed e ith e r
n o v a ria tio n o r h ad h igh levels o f m issin g d a ta across ind iv id u a ls and
w ere o m itte d fro m s u b se q u e n t analyses. T h e final SN P d a ta set
en co m p assed 85 spec ies-d iag n o stic SN Ps. A to ta l o f 12 larvae sh o w ed
a h igh p ro p o r tio n o f m iss in g d a ta a n d w ere o m itle d fro m all fu r th e r
analyses. Five o f th ese re p re sen ted larvae o f o th e r d eep sea (n o n -
Anguilla) eel species sp aw n in g in th e Sargasso Sea, as fu r th e r va lidated
by seq u en c in g th e m ito c h o n d ria l 16S rR N A gene u s in g th e L1854 an d
H 3059 p rim ers (A oyam a et al., 2000) S u p p iem en ta ry T ab le S2).
A to ta i o f 460 eel la rvae fro m 2014 w ere analyzed.
A m o n g th e 460 larvae sam p led in 2014, a to ta l o f 2 ind iv íd u a ls w ere
id e n tified as hyb rid s . B o th sh o w e d th e E u ro p ea n eel m ito c h o n d ria l
g eno type (F igu re 2 b ). U sin g N E W H Y B R ID S , th e tw o h y b rid s w ere
classified as sec o n d -g e n e ra tio n backcrosscs (bA R x AA) be tw een a
firs t-g en e ra tio n back cro ss (A m erican e e lx F1 h y b rid ) m a le a n d a p u re
E u ro p ean eel fem ale. T h is h y b rid class was th e sam e, as fo r th e tw o
Heredity
Reproductive isolating barriers in North Atlantic eels
MW Jacobsen et al
L ater o r cqual to 6lh
generation b ackcrosses A R
L ater o r equal to 6lh
generation b ackcrosses AA
| Homozygotes, AR gcnotype □ Hctcrozygotcs □ Homozygotcs, AA genotypc * Cytonuclear mismatch
P
< 0.032
5 generation backcrosses AA
4 “ gencration backcrosses AA
3"1 generatíon b ackcrosses AR
bA R x A A
F i hybrids
0.0 0.2 0.4 0.6 0.8
Expected genotype frequencies
— I ■
■
■
■ ■
-V /
■ ..............i ■
■
>0.995
0.940
0.880
0.860
0.093
0.943
1.0 0.0 0.2 0.4 0.6 0.8
Observed genotype frequencies
1.0
Figure 3 Expected and observed genotype frequencies at A TP 5c l of the examined hybrids, given the estimated hybrid classes. The estimated expected
frequencies are based on assumed Hardy-Weinberg proportions and previously reported allele frequencies of the A TP 5c l gene in American eel (Gagnaire
e t a l„ 2012). The probabilitíes of the observed genotype combinations are shown to the right and the individual showing ATP6~ATP5cl mismatch is denoted
by an asterisk. Sample sizes (/V) are shown in íhe respective histograms. AA, European eel (A. Anguilla ); AR, American eel (A. rostrata).
Table 3 Allele frequencies of the seven candidate locí for selection and estimated genotype frequencies in bARxAA hybrids
Locus name Allele frequencies AA Allele frequencies AR Expected genotype frequencies in bARxAA hybrids Estirnated probability for 7
índividuals being AA
AR allele AA allele AR allele AA allele AA homozygotes Heterozygotes AR homozygotes
AD272530 0 1 0.995 0.005 0.2538 0.7463 0 [0 .2 5 3 8 ]% 6 .7 7 x 10
AD50216 0 1 0.995 0.005 0.2538 0.7463 0 [0,2538J7 = 6 .7 7 x 1 0 6
AC195199 0.028 0.972 1 0 0.2366 0.7438 0.0212 (0.2366]7 = 4 . 1 5 x l0 - 5
AA69202 0 1 1 0 0.2500 0.7500 0 Í0 .2500í7 = 6 .1 0 x l0 - '5
AA99082 0 1 0.971 0.029 0.2718 0.7283 0 !9.2718]7= 1.09 x 10 " 4
AD148173 0.078 0.922 0.962 0.038 0.2403 0.7044 0.0556 i;0.2403]7 = 4 ,ó 3 x l0 '- 5
AC82954 0.009 0.991 0.986 0.014 0.2559 0.7372 0.0066 [Q.2559]7 = 7 .1 9 x 1 0 5
Abbreviations: AA, European eei (Anguilía a ngu illak AR, American eei (Anguiila rostrata).
Caiculations of the probabiiities for ali seven individuais being homozygotes for the European aiieie (AA homozygotes) are shown in the rightmost coiumn. For aii
Notes S1 and S2.
;alcu!ations see Supplementary
h y b rid larvae sam p led in 2007 (sam p le L125 and L211, F igu re 2b)
(P u jo la r et a l, 2014a), th a t w ere also reanalyzed in th is s tudy . N o
hyb rid s w ere fo u n d a m o n g th e n ew sam p les analyzed from M o ro cco
o r th e Faroe Islands. T h e p e rcen tag e o f b A R x A A h y b rid s in th e
Sargasso Sea w as lo w er in th e 2014 sam p le c o m p a re d vvith 2007:
0 .43% (2 /460 ) vs 2 .17% (2 /92 ). T h is w as also th e case w h en o n ly u sing
th e m o re a b u n d a n t E u ro p ean eel sam ples: 0 .56% (2 /358 ) vs 4 .08%
(2 /49 ). H ow ever, ín b o th cases th e d ifference w as n o t sign ifican t
(F ish e r’s exact test; P = 0.077 a n d P = 0 .136).
A m o n g th e reanalyzed lc e lan d ic h y b rid s , 13 w ere classified as F1
hybrids, 1 as bA A a n d 3 as bA R x AA, as p rev io u s ly fo u n d by P u jo lar
et al. (2014a) analyzing th e sam e ind iv idua ls . F u r th e r analyses o f th e 7
bA R x AA h y b rid s (3 fro m Ice land a n d 4 fro m th e Sargasso Sea)
sh o w ed th a t a t 7 o f th e analvzed 85 loci, all ind iv iduals w ere
h o m o zy g o u s fo r th e E u ro p ea n eel-specific allele (see S u p p lem en ta ry
T ab le S5). T h e p ro b a b ility th a t all 7 ind iv id u a ls a re h o m o zy g o a s a t th c
sam e locus is b e tw een 1.09 x 1 0 “ 4 a n d 4.15 x 1 0 ~ 5 d e p e n d in g o n th e
locus (T able 3, see S u p p le m e n ta ry N o tes S1 an d S2 fo r specific details
a b o u t th e calcu la tions) a n d th e re fo re h igh ly un like ly to o c cu r by
chance . Six o u t o f seven o f these SN Ps w e re lo c a ted inside an n o ta ted
genes. A m o n g these genes, fo u r in c lu d e d G O te rm s re la ted to
dev e lo p m en t, a n d o n e g ene re la ted to p h o sp h o ry la tio n
(S u p p lem en ta ry T ab le S3). T h e freq u en cy assocíated w ith d ifferen t
types o f gene categories w as h ig h e r a m o n g th e seven SN Ps b u t d id n o t
d iffer s ign ifican tly c o m p a re d w ith th e re s t o f th e analyzed SN Ps
(S u p p lem en ta ry T ab le S4).
Assessment o f cytonudear selection and incompatibility
O u t o f th e 19 hyb rid s analyzed , 7 w ere assigned to th e F1 h y b rid
category , 5 to th e sec o n d -g e n e ra tio n b ack cro ss catego ry (b A R x A A )
a n d 7 to th e th ird -g e n e ra tío n backcross c a tego ry o r la te r (T ab le 2).
E stim a tio n o f h y b rid classes fo r th e R A D seq u en ced ind iv idua ls is
desc ribed in detail in S u p p le m e n ta ry N o te S3. O u t o f all Iiybrids,
3 h ad A m erican a n d 16 h a d E u ro p ea n m ito c h o n d ria l D N A ATP 6
Heredity
Reproductive isolating barriers in North Atlantic eels
MW Jacobsen er a/
hap lo types. O bserv 'ed geno tvpes a t th e n u c lea r A ’J 'P Scl g ene overail
fo ilow ed n e u tra l exp ec ta tio n s given th e e s tim a ted h y b rid classes
(F igure 3). H o w ev er, o n e in d iv id u a l in fe rred to be a s ix th g e n era tio n
o r la te r A m erican b ack cro ss (in th e fo llow ing d e n o te d > 6 th ) (RBGIO
T ab le 2 a n d F igu re 3) sh o w ed a n in tro g re ssed E u ro p ean m ito g en o m e
a n d w as he te rozygo te a t A T P S c l (see S u p p le m e n ta ry N o te S4 an d
S u p p lem en ta ry T ab les STl a n d S12 fo r th e calcu la tions o f th e
p ro b ab ilities). C alcu la tio n o f th e p ro b ab ility fo r o n e in d iv id u a l o f
b e in g a n A T P S c l h e te ro zy g o te in th e s ix th o r ia te r gen era tio n
A m e ric an b ackcross levei is !ow , w ith a n e stim ated p ro b a b iiity o f
^ 0 .0 3 2 (F igu re 3). O verall, all in d ir id u aJs sh o w ed a m a tch be tw een
m ito c h o n d ria l a n d n u c lea r gen o ty p e w ith o n e excep tion : o n e indiv i-
dual sam p led in E u ro p e (LEG29; T ab le 2) sh o w ed a co m p le te
m ism a tch be tw een th e A T P 6 a n d A T P 5 c l geno types. T h is ind iv idua l
w as in fe rred to b e a ^ 6 th -g e n e ra tio n E u ro p ea n b ackcross a n d was
h o m o zy g o u s fo r th e E u ro p ea n A T P 5 c l gen o ty p e b u t sh o w ed an
A m erican A T P 6 h a p lo ty p e (F igu re 3).
DISCUSSION
Temporally varying hybridization in North Atlantic eels
O n e in te re s tin g fin d in g in o u r s tu d y is th e lack o f f ir s t-g en e ra tio n (F l)
hyb rid s fo u n d in the Sargasso Sea in 2014 d esp ite th e large n u m b e r o f
eel larvae analyzed ( N = 4 6 0 ) . T h is is in a c co rd an ce w ith th e s tu d y o f
P u jo la r c t al. (2014a) a n d Als c t al. (2 0 1 1), w h o also re p o rte d n o F1
h y b rid s in tiie Sargasso Sea in 2007, a lth o u g h re ly ing o n sm aller
sam p le sizes ( N — 9 2 a n d 388). Su rp ris ing ly , o n ly b A R x A A hybrid s
w ere ob serv ed in th e Sargasso Sea in b o th 2007 a n d 2014. A ithough
the freq u en cy o f th ese h v b rid s dccreased fro m 2007 to 2014, the
d ifferences w ere n o t sign ifican t a n d th e re su lt d o es n o t in itse lf favo r
te m p o ra lly vary ing h y b rid iza tio n . N o n e th e less, a lth o u g h F1 h y b rid s o f
A tlan tic eel m a y sh o w a n inc rease in fitness, th e so -called h y b rid v igor
(see, lo r ex am ple, T e m p le to n , 1986; J o h n so n e t a l , 2 010), p o s t-F l
h y b rid s a re likely to be selected against because o f ex trin sic selection ,
o r in trin sic se lec tion b ecau se of, fo r ex am ple, genetic incom patib ilities .
In d eed , th e p resence o f s tro n g postzygo tic b a rrie rs seem s s u p p o rte d in
A tlan tic eels th a t, d esp ite low average genetic d iffe ren tia tio n , sh o w
m a n v d iag n o stic a n d n e a r-d iag n o stic SN Ps d is tr ib u te d across th e
g e n o m e (Jacobsen e t a l , 2014a). T h e rcsu lts in th is s tu d y also su p p o r t
a postzygo tic c o m p o n e n t o f se lec tion in h y b rid s , as 7 o f th e analyzed
85 loci show ed s tro n g ev idence fo r se lec tion fo r th e E u ro p ean eel-
specific allele. M o re d ire c t s u p p o r t fo r postzygo tic selection can be
fo u n d in Iceland . H e re b o th am p lifie d frag m en t length p o ly m o rp h -
ism - a n d S N P -based s tu d ies o f glass a n d yellow eels re p o r t m o re th an
tw o fo ld h ig h e r ffequencies o f F1 hyb rid s c o m p a re d w ith co m b in e d
first an d seco n d b ackcrosses (A lbert e t a l , 2006; P u jo lar e t a l , 2014a).
Besides b e in g th e on ly p iace w h e re F1 h y b rid s h ave b een fo u n d ,
Ice iand is a lso th e o n ly loca lity w h e re firs t- (bA A ) a n d second-
g c n era tio n b ackcrosses (b A R x A A ) h ave b e en d c te c ted o u ts id e th c
Sargasso Sea. A lth o u g h th is m a y b e because o f d ifferences in h y b rid
ffeq u en c ies b e tw een Ic e lan d an d C o n tin e n ta l E u ro p e a n d N o r th
A m erica , th e re is c u rre n tly n o ev idence fo r th is . in fact, o u t o f several
s tud ies investigating h y b rid iza tio n in A tlan tic eels fro m the m a in la n d
(excl. Ice land ) u s in g m ic ro sa te llite (Als e t a l , 2011: N = 1 0 1 0 ) ,
am p lified ffag m en t len g th p o ly m o rp h ism (A lbert e t a i , 2006:
iV = 379) o r SN P m a rk e rs (P u io la r e t al„ 2014a, b: N = 3 1 0 ) , n o n e
have o b serv ed a n y su ch ind iv idua ls . G iven th ese o b servations, w e fin d
it likely th a t F1 h y b rid s s h o u ld exist in h ig h e r freq u en cy c o m p a re d
w ith la te r-g en e ra tio n b ackcrosses if h y b rid iza tio n is c o n tin u o u s over
tim e . As su ch , w e fin d th a t th e a p p a re n t la ck o f F1 h y b rid s in th e
Sargasso Sea in 2007 a n d 2014 is su rp ris in g an d b e st exp la in ed by
tem p o ra lly vaiyáng h y b rid iza tio n .
T em p o ra lly vary ing h y b rid iza tio n m ay be m e d ia ted by d ifferences in
te m p o ra l o r spatia l overlap o f sp aw n in g b e tw een th e species o v e r tim e.
T h is c o u ld be a re su lt o f a n n u a l v a ria tio n in th e lo ca tio n o f the
th e rm a l fro n ts (P u jo la r c t al„ 2 0 l4 a ) th a t sh o w c o n sid e rab le d ifter-
ences in in ten sity a n d geog raph ical p o s itio n across years (T esch , 2003;
U llm an e t a l., 2007; M u n k e t al„ 2010). In d eed , te m p e ra tu re has
inc reased stead ily o v e r th e p a s t d ecad es in th e Sargasso Sea
(B o n h o m m e a u e t al„ 2008; H u ffa rd e t al„ 2014), w here th e 22.5 °C
iso th e rm m o re o v e r h as m o v e d n o r th w a rd s since ~ 1970 (F ried lan d
et al„ 2007), As th e 22 .5 °C iso th e rm is generally c o n sid e red to b e n e a r
th e n o r th e m iim it o f sp aw n in g o f A tlan tic eels (K leckner and
M cC leave 1988; T e sch a n d W eg n er, 1990), th ese changes a re likely
to b e associated w ith a m o re n o r th e rn d isp lacem e n t o f th e shared
sp aw n in g g ro u n d s . As sucli, the d is tan ces th a t A m erican a n d E u ro p ean
eel n eed to cover to reach th e Sargasso Sea m a y h ave ch an g e d recently ,
p o ten tia lly affecting tim e o f a rriva l a n d h y b rid iza tio n , re su ltin g in
few er hy b rid s b e in g p ro d u c e d . T e m p o ra lly vary ing h y b rid iza tio n has
also been suggested by A lbert e t al. (2006) to exp ia in the decrease in
p ro p o r tio n o f h y b rid s o b serv ed in Ice land fro m 2000 to 2003 w hen
c o m p a rin g glass eei sam ples, a p a tte rn th a t w as fu r th e r su p p o rte d
w hen c o m p a rin g d iffe ren t c o h o rts c o m p ris in g glass eels a n d yellow
eels. Y e ar-to -y ea r v a ria tio n in p o p u la tio n d en sity co u ld a lso explain
th e lack o f F1 h y b rid s in o u r s tudy . In th is sense, b o th E u ro p ean an d
A m erican eel have experien ced d ras tic declines in th e p a st ca. 30 years
(Á s trö m a n d D ekker, 2007), possib ly lin k e d to ín la n d p o ilu tio n , d am s
an d fisheries (B usch a n d B rau n , 2014; L ap o rte e t a l , 2016). T h is
decline suggests possib le red u c ed densities o f sp aw n in g eels th a t cou ld
lead to a red u c ed spatia l overlap a n d h y b rid iza tio n (A lbe rt e t al„ 2006;
Jacobsen e t al„ 2014 b ). As e n v iro n m e n ta l ch an g e w ith in the Sargasso
Sea itse lf m a y affect eel p o p u la tio n sizes (F ried lan d e t al„ 2007;
B o n h o m m e au e t al„ 2008), th ese tw o scen ario s m ay n o t be m u tu a lly
exclusive a n d th e lack o f hy b rid s c o u ld be a co n seq u en ce o f d ifferen t
en v iro n m e n ta l effects.
S am pling b ias in e ith e r space o r tim e m a y also exp la in th e lack o f F1
h y b rid s in o u r s tudy . H o w ev er, a lth o u g h a d is tin c t h y b rid z o n e in
th eo ry c o u ld go u n n o tic e d , th e re is little ev idence fo r th is . I f it d id
in d e e d cxist, it w o u ld be expec ted to b e p re sen t in th e co re a rea o f th e
tw o o v e rla p p in g sp aw n in g areas th a t h is to rica ily h as b een ran g in g
fro m 70 to 58°W (M ille r et al„ 2015), an d th a t w as extensively
sam p led d u r in g ex p ed itio n s in b o th 2007 a n d 2014 (Als e t al„ 2011;
P u jo iar c t al„ 2014a; th is s tudy: F igure 2). A n o th e r p ossib ility is th a t
h y b rid iza tio n o ccu rs as a last o p tio n , w h en in d iv idua ls a re u n a b le to
loca te conspecifics. I f so, F1 h y b rid s s h o u ld b e th e p to d u c t o f e ith e r
E u ro p ean eels a rriv in g to o early o r A m erican eel a rriv in g to o la te a t
th e sp aw n in g area , o r w h e n b o th species a rrive o u ts id e th e p rim a ry
sp aw n in g season . A re c cn t analysis o f all p u b lish ed rcco rd s o f larvae
( c l O m m ) co llected in th e Sargasso Sea suggests th a t th e sp aw n in g
season ex tends fro m 13 F e b ru a ry to 27 A pril in A m erican eel a n d 27
F eb ru a ry to 21 Ju ly in E u ro p ea n eel, w ith ra re sp aw n in g even ts
possib ly o c cu rr in g o u ts id e these p e rio d s (M ille r e t a l , 2015). T hus,
given th a t s am p lin g to o k p lace fro m M arch to A pril d u r in g the 2007
an d 2014 exp ed itio n s to th e Sargasso Sea, a te m p o ra l sam p lin g bias
c a n n o t be ru le d o u t. A w ay o f investigating th is p ossib ility w o u ld be to
analyze n io re sam ples fro m Ice land th a t so fa r is th e o n ly place w here
F1 h y b rid s h ave b e e n o b serv ed (A vise e t al„ 1990; A lb e rt e t al„ 2006;
G agnaire ct al„ 2009; P u jo la r e t al„ 2014a). I f th e a p p a re n t lack o f F1
h y b rid s in 2007 a n d 2014 is tru e , th e n th is p a tte rn sh o u ld also be
re flec ted fo r th e sam e c o h o rts in lce lan d .
Heredity
Reproductive isolating barriers in North fltlantic eels
MW Jacobsen et al
S e le c tio n a t lo c i in n a tu r a l h y b r id s
Id en lif ica tio n o f h y b rid s w as b ased o n a set o f SN Ps th a t sh o w ed
a lm o s t fixed d ifferences b e tw een th e fw o species a n d a re likely to m a rk
c h ro m o so m a l reg ions u n d e r d ív e rg en t se lec tion in A tlan tic eels
(Jacobsen e t a l , 2014a; P u jo la r e t a l., 2014a). T h e use o f genetic
m a rk e rs u n d e r se lecd o n e n h an c e th e ab ility to d e te rm in e th e p o p u la -
tio n o f o rig in o f in d iv id u a ls w ith in specics (N ie lscn e t a l., 2012) a n d
d e tec t p o s t-F l h y b rid s (P u jo la r e t al„ 2014a). H ow ever, it m ay also
invoive p o tc n tia l p ro b le m s w h e n u sed fo r h y b rid a ss ig n m en t by
affecting th e g eno typ ic p ro p o r tio n s th a t h y b rid id en tifica tio n is based
on . Even if n e a r fixa tion o f d iffe ren t alleles in th e tw o species reflects
se lection , i t does n o t in fe r w h e th e r se lec tion is w eak o r s trong . In fact,
even w eak d irec tio n a l se lec tion m a y lead to fixation given suffic ient
tim e a n d low genetic d r if t a n d gene flow . Specificaliv in ou.r s tudy , all
p u ta tiv e sec o n d -g e n e ra tio n bA R x A A b ackcrosses w ere h o m o zy g o u s
fo r th e E u ro p ea n eel allele a t th e sam e 7 S N Ps (o u t o f 85 SN P loci).
T h is o b se rv a tio n is h igh ly u n lik e ly to h a p p e n by ch an ce (T ab le 3) a n d
s tro n g ly suggests a ro le o f se lection . W e find th e m o s t p a rs im o n io u s
ex p lan atio n to be th a t the seven SN Ps a re linked , o r p a rt of, lo
fu n c tio n a l alleles th a t a re c o d o m in a n t a n d sub jec t to s tro n g selection
be tw een the species. T h is co u ld re su lt in ail geno types be ing
h o m o zy g o u s, w hereas a t th e sam e tim e th e geno types a t o th e r loci
a re m o re in acco rd an ce w ith n e u tra l ex p ec ta tio n s , given th e specific
crosses u n d erly in g th e h y b rid s . H ow ever, a lth o u g h th is m a y explain
th e specific geno tvpes a t th ese loci, o m iss io n o f th e loci w o u ld n o t
cause th e h y b rid s to b e assigned to a less co m p le x h y b rid class th a n
b A R x A A , su ch as, fo r exam ple, f irs t-g en e ra tio n AA backcross (F1 x
AA). N o n e th e less, it d e m o n s tra te s th e p o ten tia l p itfalls w h e n using
su ch m a rk e rs in h y b r id a ssessm en t a n d suggests an in c reasin g b ias
w h en a tte m p tin g to id en tify h y b rid s several g en era tio n s b ack in tim e.
F u r th e r inv estig a tio n o f th e g en o m ic p o s itio n s o f th e 7 SN Ps
su p p o rts th a t se lec tion is p lay ing a ro le as (1) 6 o u t o f th e 7 S N Ps w ere
lo ca ted in genes (as o p p o se d to b e in g ra n d o m ly lo ca ted in n o n c o d in g
reg ions) a n d (2) 4 genes m a tc h e d G O te rm s re la ted to d e v e lo p m en t
a n d o n e gene m a tc h e d G O te rm s re la ted to p h o sp h o ry la tio n /e n e rg y
p ro d u c tio n . T h is is in c o n c o rd a n c e w ith th e re c en t s tu d y o f Jacobsen
e t al. (2 0 14a) investigating s p e r ia t io n in N o rth A tlan tic eels, in w h ich
th o se tw o G O te rm catego ries w ere o v errep re sen te d a m o n g genes
associated w itli c a n d id a te SN Ps fo r d ifferen tia l se ie rt io n sh ow ing
FSt = 1 w h en c o m p a rin g E u ro p ea n a n d A m erican eel sam ples.
C y to n u c le a r in c o m p a tib il i ty ' in N o r th A tla n tic eels
T h e cy to n u c lea r in c o m p a tib ility h ypo tlie s is s tates th a t th e re n eed s to
be a m a tc h be tw een c o a d a p te d in te ra c tin g n u c le a r a n d m ito c h o n d ria l
genes th a t m ig h t o th e rw ise lead to p ro te in m a lfu n c tio n a n d conse-
q u e n tly re d u c ed fitness (B lier e t al„ 2001). R esults from o u r s tu d y are
overall in acco rd an ce w ith th is hy 'pothesis as h y b rid ind iv id u a ls
generally sh o w ed a m a tc h b e tw ee n th e p u ta tiv e iy co ad ap ted species-
specific n u c lea r a n d m ito c h o n d ria l alleles. H ow ever, in m o s t cases th e
observed A T P 5 c l geno types, fo u n d w ith in each h y b rid category ,
fo llow ed n e u tra l ex p ec ta tio n s a n d d o th u s n e ith e r su p p o r t n o r
co n tra d ic t th e cy to n u c lea r h ypo thesis. In te resting ly , how ever, on e
A m erica n glass eel b ack cro ss (R BG 10; T ab le 2 an d F igure 3) sam p led
in R iviere B lanche w as h e te ro zy g o u s fo r th e n u c lea r A T P 5 c l gene, b u t
sh o w ed an in tro g re ssed E u ro p e a n m ito c h o n d ria l D N A A T P 6 gene.
C o n sid e rin g th a t th is in d iv id u a l w as e s tim a ted to b e lo n g to a > 6 th -
g e n era tio n backcross, th e p ro b ab ility o f b e in g h e te rozygous a t A T P 5 c l
is lo w ( P ^ 0.032, F igure 3). T h is p o in ts to w a rd selec tion fo r a m a tch
be tw een c o rre sp o n d in g A T P 6 h a p lo typ es a n d A T P S c l allcles a n d th u s
su p p o rts the h y p o th e sis o f cy to n u c lea r incom patib ility '.
O n th e o th e r h a n d , o n e glass eel co llected in Ire lan d a n d iden tified
as a > 6 th -g e n e ra tio n E u ro p ea n back cro ss (LEG 29; T ab le 2 an d
F igure 3) rep re sen ted a c o m p le te m ism a tch , as it sh o w e d the
A m erican m ito c h o n d ria l h ap lo ty p e b u t w as h o m o zy g o u s fo r the
E u ro p ean n u c le a r allele. T h is d e m o n s tra te s th a t th e co m b in a tio n o f
an A m erican A T P 6 h ap lo ty p e a n d tw o E u ro p ean A T P S c l alleles is n o t
im m ed ia te ly le thal, a n d th is is in o p p o s itio n to th e exp ec ta tio n s o f
cy to n u c lea r inco m p a tib ility . T h is can p o ten tia lly b e exp la ined if
in co m p a tib ility is in co m p le te . In su ch a case, ind iv id u a ls sh ow ing
m ism a tch cou ld be viable , a lth o u g h fitness is red u ced . N one theless,
w ith o n ly o n e in d iv id u a l in c lear favo r a n d o n ly o n e th a t co n trad ic ts
the expec ted p a tte rn o f m ito n u c le a r in co m p a tib ility , th is possib ility
c a n n o t be verified a n d th e hy p o th esis o f c y to n u c lea r in co m p a tib ility
c a n n o t be fully accep ted o r re jec ted b a sed o n th e resu its in th is s tudy.
N onetheless, th e fin d in g o f an A T P 6 - A T P 5 c l m ism a tch is su rp ris -
ing, as th e fin d in g o f s ign ifican t in te rspecies n o n sy n o n y m o u s d iffer-
e n tia tio n in genes invo lved in th e A T P syn thase co m p le x (G agnaire
e t a l , 2012), in c o m b in a tio n w ith s tu d ies sh o w in g s tro n g ev idence fo r
positive selec tion w ith in A T P 6 (Jacobsen c t a l , 2014b, 2015), is
d ifficu lt to exp la in w ith o u t cyTonuciear in co m p a tib ility . H ow ever,
th re e ex p lan a tio n s m a y a c c o u n t fo r th e fin d in g o f a co m p le te A T P 6 -
A T P 5 cl m ism a tch even in case o f c o m p le te cy to n u c lea r in c o m p a t-
ibility: (1) c y to n u d e a r se lec tion m ig h t first a c t in a ia te r life stage
b ey o n d th e glass eel stage, (2) c o m p e n sa to ry in te rac tio n s involving
o th e r n u c iea r su b u n its o f th e A TP sy n th ase p ro te in co m p lex m ig h t
o c cu r o r (3) u n id irec tio n a l in co m p a tib ility . G iven th e fu n c tio n o f the
A T P syn thase co m p lex , A T P 6 - A T P 5 c l m ism a tc h is expec ted to lead to
re d u c ed cnergy p ro d u c tio n (Saraste, 1999). H ow ever, i t is possib le th a t
c o m p en sa to ry m e c h an ism s exist eariy in life. F o r exam ple, D ro so p h ila
m u ta n ts sh o w m etab o lic c o m p e n sa tio n th ro u g h increased glycolytic
flux, ke togenesis a n d K rebs’ cycle activ ity d esp ite A T P 6 d y sfunc tion ,
a lth o u g h severely d e le te r io u s p h en o ty p e s a re a lready ob serv ed after
few days a n d m u ta n ts d ie p re m a tu re ly (C e lo tto e t al„ 2011). I f a
s im ila r m e c h an ism ac ts in A tlan tic eels, A TP 6-A TP 5cl m ism a tch m ay
be ob serv ed in ju v en iie ind iv idua ls , w h ereas selection m ay act against
th ís genetic co m b in a tio n la te r in life. C o m p e n sa to ry m ech an ism s m av
also exist, in v o lv ing o th e r n u d e a r su b u n its . In a d d itio n to A T P S c l , 13
o th e r n u c lea r genes a re invo lvcd in th e A T P syn thase p ro te in com p lex
(B allard an d W h itlo ck , 2004). A lth o u g h tra n sc r ip to m e analysis has
sh o w n th a t A T P 5 c l is th e m o s t d iv e rg e n t su b u n it in te rm s o f
d iag n o stic n o n sy n o n y m o u s su b s titu tio n s b e tw een E u ro p ea n and
A m erican eels, d iag n o stic changes also exist in a t least fo u r o th e r
s u b u n its (G agnaire e t al„ 2012). T h u s , A TP syn thase fu n c tio n a n d
h en ce postzygo tic se lec tion m a y d e p e n d o n th e gen o ty p es o f these
su b u n its in co m b in a tio n w ith A T P S c l. A last possib ility is th a t
c y to n u c lea r in co m p a tib ility is u n íd irec tio n a l in A d an tic eels, w ith
A T P 6 - A T P 5 c l m ism a tch b e in g fa ta l in A m e ric an eel, b u t n o t in
E u ro p ea n eel. T h is c o u ld p o te n tia lly exp la in th e observed asy m m e-
Irical p a tte m s o f in tro g re ss io n , f ro m A m erican to E u ro p ea n eel,
re p o rte d in so m e s tu d ies (G agnaire et al„ 2009; W ielgoss e t a l ,
2014). O n th e o th e r h a n d , if u n id irec tio n a l cy to n u c lea r in co m p a tib iiity
o ccu rre d w e w o u ld expect in tro g re ss io n o f th e A m erican m ito g e n o m e
in E u ro p ean eel. H ow ever, Iittle e r id e n c e o f th is exists. In fact, the
ind iv idual seq u en ced in th is s tu d y (LEG 29) sh o w in g A T P 6 - A T P 5 c l
m ism atch is, to o u r know ledge, th e o n iy E u ro p ean ind iv idua l to da te
th a t sh o w th e A m erican m ito g e n o m e (see, fo r exam ple, Avise e t a l ,
1990; D a e m e n e t al„ 2001; Jacobsen e t al„ 2 0 1 4b) besides F1 hyb rid s
fro m Ice land (Avise e t a l , 1990; A lb e rt e t al„ 2006; dfis s tudy). As
su ch , w e fin d th e p ossib ility o f u n id irec tio n a l cy to n u c lea r in c o m p a t-
ib ility unlikely.
Heredity
Reprodudive isolating barriers in North Atlantic eeis
MW Jacobsen et a/
CÖNCLUSION
In co n clu s io n , o u r resu its p ro v id e n ew in sigh ts in to the p re - a n d po st-
zygotic b a rr ie rs a cting be tw een th e tw o species o f A tlan tic eels. T he
lack o f F! hyb rid s , b u t p resen ce o f a few la te r-g e n e ra tio n h y b rid s in
th e Sargasso Sea in b o th 2007 a n d 2014, suggests th a t in te rb reed in g
b e tw een th e tw o species is re s tric te d to so m e years, w hereas in o th e r
years o n ly b ackcrosses o c cu r th a t a re th e re su lt o f in te rb ree d in g in past
g en era tio n s. W e ftn d th e m o s t likely e x p ian a tio n to b e in te ra n n u a i
va ria tio n in th e lo ca tio n o f th e th e rm a l fro n ts in w h ich sp aw n in g takes
p lace th a t m a y su b seq u en tly lead to inc reased o r decreased overiap o f
sp aw n in g tim e of th e tw o species. M o reo v er, o v e rre p re sen ta tio n o f
h o m o zy g o tes fo r so m e SN Ps u sed fo r h y b rid assessm en t w as o bserved
th a t w e in te rp re t as d iv e rg e n t se iec tion be tw een species b e in g
p a rticu la rly s tro n g a t so m e loci. O n o n e side, th is p ro v id es ev idence
fo r postzygo tic b a rrie rs , b u t o n th e o th e r s ide com plicates accu ra te
id en tifica tio n o f p o s t-F l h y b rid classes. Finally, w e fin d so m e ev idence
s u p p o rtin g th e su ggestion o f c y to n u c lea r in c o m p a tib ility invo lv ing th e
m ito c h o n d ria l A TP6 g ene a n d th e n u c le a r ATPScl in te ra c to r gene
(G agnaire et al> 2012 ), b u t m ism a tch es b e tw een th e tw o are n o t
necessarily lethal a n d th e resuJt s h o u ld b e in te rp re te d w ith p recau tio n s
u n ti l m o re d a ta a re available. T h e resu lts o b ta in e d in th is s tu d y are n o t
o n ly im p o r ta n t fo r u n d e rs ta n d in g sp ec ia tio n in A tlan tic eels, b u t also
fo r u n d e rs ta n d in g th e varie ty o f iso la ting b a rr ie rs a c tin g in n a tu re
(C oyne a n d O rr , 2004; N osil et a l , 2005) a n d especialiy in th e m arin e
e n v iro n m e n t (P ueb ía , 2009). H ere , o rg a n ism s like m a n y fishes an d
in v e rteb ra tes sh o w severaí tra its in c o m m o n w ith A tlan tic eels: they
a re d ifficu lt to re a r in captiv ity , sh o w la rge p o p u la tio n sizes, have no
obv ious geog raph ic b a rr ie rs to gene flow a n d sh o w lo n g larval p hases
(P a lu m b i, 1994). All th ese fea tu res p ro m o te lo w genetic drift,
efficiency o f even low selec tion a n d in c reasin g possib ilities fo r
sp ec ia tio n w ith gene flow (P ah m ib i, 1994; R iginos a n d V ic to r, 2001;
Jacobsen et aL> 20L4a). T h u s , b o th th e difficulti.es in s tu d y in g these
o rg an ism s a n d th e overall ev o lu tio n a ry fo rces invo lved in th e ir
spec ia tion m a y b e q u ite s im ila r to th e s itu a tio n in A tlan tic eels.
DATA ARCHIViNG
T h e seq u en ce d a ta a re d e p o sited in G e n b a n k accessions n u m b e rs
K X 818059-K X 818096. T h e FL U ID ÍG M SN P a n d th e RAD SN P da ta
sets a re d ep o sited in D R YAD: D G I:10 .5061 /d ryad .v5m 24 .
CONFLICT OF INTEREST
T h e a u th o rs d eclare n o con fiic t o f in te res t.
ACKNOWLEDGEMENTS
W e acknowledge funding from the Carlsberg Foundation (Grant
2012_01_0272), the Danish Centre for M arine Research, the Danish Council
for Independcnt Rescarch, Natural Scienccs (Grants 09-072.120 and 1323-
00158A to M M H) and EU Interreg (Öresund-Kattegat-Skagerrak) funds
(MARGEN). Wc thank Henrik Sparholt, Peter Rask Moller, jon Svendsen,
Magnus Bohr, Daniel )iro Ayala and Cornelia jaspers for assistance with sorting
o f samples during an. expedition to the Sargasso Sea in 2014, Annie Brandstrup,
Karen-Lise Mensberg, Dorte Meldrup and Dorte Bekkevold for technical
assistance and Louis Bematchez for providing samples o f American eels. Finally,
we thank three anonymous referees for vaiuable com m ents on the manuscript.
AUTHOR CONTRIBUTIONS
MWJ, M MH, PM, LS, and JMP conceived and designed the study. LS and MWJ
conducted the molecular work. MW E LS, M MH, SRS and jM P conducted the
statistical analyses. MWj wrote the manuscript with contributions from MMEI,
LS, SRS, JMP, PM, BJ and EM.
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S u p p le m e n ta ry In fo rm a tio n acco m p a n ie s th is p a p e r o n H e re d ity w ebsite (h ttp ://w w w .n a tu re .c o m /h d y )
http://www.nature.com/hdy
Veiðar, vinnsía og sala á áL
Magiiús jóhannssoii, Róbert Jónsson og
Björn Ingi Bjömsson.
Selfossi, ágúst 19% VMST-S/9Ó00I
V E I Ð I M Á I A
B ókas
Veiðimálastofnun - Suðurlandsdeild
Austurvegi 1 800 Selfoss
2. In n gan gu r.
3. A lm en n t um á la ve ið ar.
4. S ta ð h æ ttir o g ran n só k n ara ð ferð ir.
5. Niðurstöður.
5. I T ilra u n a ve ið a r.
5. 1. I A fli í tilrau n aveiðu n i.
5. I. 2 V in n a v ið veiðar.
5 . 1 . 3 L e n g d o g þyn gd.
5. 1 . 4 A ld u r , v ö x tu r o g kyn.
5. 2 U tb re ið s la áls í vö tn u m a Suóurlan di.
5. 3 T ilrau n avin n sla .
5. 4 M a rk a ð sa th u g u n .
6. U m ræ ð a .
ó. 1 V e ið a r.
6. 2 S tæ rð , a ld u r o g v ö xtu r.
ó. 3 V e ið im ö g u le ik a r á Suðurlan di.
ó. 4 V e r k u n o g m arkað u r.
7. Þ a k k a ro rð .
8. H eim iid ir.
1. Á g rip .
Á1 e r a ð íin n a v íð a um iand en þ ó a ð a lleg a á láglendi sunnan- o g vestanlands. Áll er
v íð a v e id d u r erien dis, þ a r er hann e ftirsó ít n ey slu va ra o g selst á háu v e rð í. L ítilsh áttar
er veitt a f ál en en n þ á er veiðanlegt m agn ó þ e k k t. Verkefni þ essu v a r æ tla ð að sk ý ra
h v o rt g ru n d v ö llu r sé fy rir v e ið u m , vinnslu o g sö lu á ál á S u ð u rla n d i. G e r ð a r vo ru
tilrau n ir m eð v e ið a r o g vin nslu . E in n ig v o m a th u g að ir sö lu m ö g u íe ik a r o g v e rð á
unninni atlirð . I tilra u n av eið u m v a r lö g ð áhersla á tilra u n a v eið a r á b jartál o g lag t m at á
h versu m ik ið m æ tti v e ið a á rle g a a f ál á svæ ðín u . V e r k e fn ið v a r sa m vin n u v erk efh i
V e ið im á la sto fn u n a r , á ta k sv e rk e fn is í atvin n um álum á S e lfo s s i, b æ n d a i
S to k k se y ra rh re p p i o g H afh a r-Þ ríh yrn in g s lt/f. T ílra u n a v e ið a r fó ru fram : n o kk ru m
v ö tn u m í S to k k se y ra rh re p p i su m arið 19 9 5 . A fli v a rð 392 áiar o g 103 k g e ð a 1,8 k g á
ha. A íl i v a r að ja fn a ð i 0 ,20 álar, 0,05 k g í h v e ija á lag ild ru e ft ir n æ tu ria n g a leg u .
M in n a v e id d ist a f b jartál en v o n ir stó ð u til, eð a 2 7 k g sem g e rir um 0,5 k g a fra k stu r á
ha. L ít ið er h æ g t að fuliyrða um h v o rt slíks m eg i v æ n ta á rle g a eð a að bjartálagengd sé
b re y tile g á m illi ár B jartáiiin n v a r a ó a lle g a á ieið út síðari h lu ta se p íe m b e r o g fyrstu
v ik u í o k tó b e r . Flestir álarnir v o ru 45 til 55 sin o g 150 til 2 5 0 g, Guiáíar voru að
ja fn a ð i m inni en bjartálarnir. M e ð a ls tæ rð g u lá la v a r 2 4 2 g o g b jartáia 3 7 1 g. A f
heiidarafla v a r 73 % a f nýtanlegri stæ rð. Ú tffá tilraunaveiðum o g flatarmáli v a tn a þar
sem ál er a ð finn a er raun hæ ft að ársafli a f ái á S u ð u rla n d i g e ti v e r ið 5 til 10 íon n,
Möguleikar fil veiða eru d re ifð ir o g víðast hvar er veiðanlegt magn tiltö lu le g a lítið á
hverjum stað. M e s tu möguleikar virð a st í lá g sv e itu m Rangárvallasýslu, Flóa, Ölfusi o g
S k a ftá rh re p p i. H v o rt g n in d v ö ilu r er fyrir v e ið i fyrir b æ n d u r b y g g is t a ð m iklu lefy i á
a ð stæ ð u m h já h verju m b ón d a. L jó s t vsrðist að ek k i er u m m ik la r te k ju r að ræ ð a ly rir
h vern o g einn landeiganda. Samhliða gulálaveiði æ tti að reyna fre k a bjartálaveiðar þ ví
tiikostnaður v ið þ æ r v e ið a r æ tti í flestu tiífeilum að v e ra minni en v ið gulálaveiðar.
M ik ill b re y tile ik i v a r í h v e á la n iir léttu st í ve rk u n , en þ u n gi e ftir v e rk u n v a r ailt frá 63
% til 74 % a f upphaflegum þu n g a. R ýrn u n virtist fara eftir stæ rð , þ. e. smærri állinn
rýrn a ð i meira en sá stæ rri. L a u s le g a th u gu n á m a rk að í sýndi að m a rk a ð u r er lítil! fyrir
ál in n an ian ds o g fra m b o ð v irð ist einnig lítið. Þ ví er ekki ó lík le g t a ð e f áll væ ri v e id d u r
o g verkaður h ér heima, v æ ru möguleikar á að byggja upp markað. E m s er líkiegt að
e in h v e r m a rk a ð u r sé fyrir fersk a n ái, en auk þ e ss g æ ii ú tfiu tn in g u r k o m ið til gre in a sem
þ ó er ó k a n n a ð . N ið u rstö ð u r h a g k væ m n ism ats b en d a til þ e ss a ð m e ö 10 to n n a v e ið i á
árí e ð a meira, g e ti vinnsla á ál verið h a gk væ m . Þ ví virðist Ijóst að h æ p ið sé að byggja
vin n slu e in g ö n g u á su n n len sk u m ál. H u g sa n ieg t er að sam h lið a á la v e ið u m m æ tti
stu n d a áiaeld i. G ru n d v ö liu r siíks eid is hérlen dis er hins v e g a r ó k a n n að u r.
2. ínngangur.
E v r ó p s k i állinn (Anguilla anguilla L .) er ein a f fim m fisk íe g u n d u n i sem lifa í fersk u
vatn i hér á landi. A1 er a ð finn a v íð a um íand en þ ó a ð a lle g a á lág len di sunnan- o g
vesían lan d s. A ll er v íð a v e id d u r erlen dis, þar er hann eftirsó tt n ey slu v a ra o g selst á háu
v e rð i. L itilsh á tta r er v e itt a f ál en en nþá er v e ið a n le g t m agn ó þ e k k t.
A llin n h rygn ir í sjó (í Þ a n g h a fm u út a f au stu rströn d M ið -A m e rík u ) en elst upp í fersk u
vatn i. L ífs ferill á lsins er þ a n n ig fráb ru g ð in n lifsferli ann arra te g u n d a ísien sk ra
fe rsk v a tn sfisk a sem alast u p p , ým ist í fersk u vatn í e ð a s jó , en h y g n a á va llt í fersk u
vatn i. L ir fú r á lsin s b erast m eð G o lfstra u m n u m að strö n d u m E v r ó p u o g te k u r þ a ð um
e ð a innan v ið 1 ár. G le rá la r o g á la se ið i g a n g a i fe rsk v a tn að su m arlagi. A il í up p eld i
n efnist gu lá il. H an n lifir í ám o g v ö tn u m sem á la se ið in ná að g a n g a í. A liin n er h itak æ r,
k jö rh iti til v a x ta r er 2 2 -2 3 ° C (S a d le r 19 7 9 ). Þ e g a r hann h efú r n áð um 3 5 -10 0 sm
(0 ,1 - 2 ,0 k g ) te k u r hann að g a n g a í Þ an g h a fið til h y g n in g a r . H an n n efnist þ á bjartáll.
N o rsk a r ran n só kn ír hafa sýnt að bjartállinn g e n g u r m est ti! s jáv a r s íð su m a rs o g á
haustin (H a rald sta d ofl. 19 8 5 , B e r g e r s e n o g K iem e n tsen 198 8).
Á ll h efu r lítið v e r ið ra n n sa k a ð u r hérlen dis. Á r ið 19 7 8 tó k M a ría n n a A le x a n d e rsd ó ttir
( 1 9 7 8 ) sam an upplýsingar m a. um á lave iðar. N o k k r a r tilrau n ir h afa verið g e r ð a r m eð
g le rá la v e ið a r a f sta rfsm ö n n u m V e ið im á la sto fn u n a r o g fleiri aðilum (S íg u r ð u r M á r
E in a rsso n 19 8 4 ). Þ á h a fa v e r ið g e rð a r ath u gan ir á te g u n d a rg re in in g u ís len sk ra ála
(A v is e ofl. 19 9 0 , W illia m s ofl. 198 4). Á árunum 199 1 til 1993 v o rn g e rð a r n o k k ra r
rannsóknir á ál o g álaveiðum í Skaftárhreppi (Jón G . Schram 19 9 3 , M a g n ú s
Jóh an n sson 19 9 3).
Verkefni þ essu v a r æ tla ð a ð sk ý ra h v o rt g ru n d v ö llu r sé fy rir v e ið u m , vinnslu o g sölu á
ál á S u ð u rla n d i. G e r ð a r v o ru ve ið ííiira u n ir, tilraun avin n sla (h e itre y k in g ) o g g e rð v e rð -
o g m a rk a ð sa th u g u n innanlands. í tilra u n av eið u m v a r lö g ð á h ersla á tilra u n a v e ið a r á
b jartál. E in n ig v a r la g t m at á þ a ð h versu m ik ið m æ tti v e ið a á rle g a a f ál á svæ ð in u .
V e r k e fn ið v a r sa m vin n u v erk e fn i V eið im á la sto fn u n a r, á ta k sv e rk e fh is i a tv in n u m álu m á
S e lfo ss i, b æ n d a í S to k k se y ra rh re p p i o g H a fn ar-Þ ríh yrn in gs h/f.
3. Almennt um álaveiðar.
AIl er v íð a v e id d u r til m anneidis. I E v r ó p u eru D an ir, S v ía r, P ó lv e r ja r , Þ jó ð v e r ja r , N -
íra r o g íta lir a ð a lv e ið iþ jó ð irn a r. Á r le g v e ið i í E v r ó p u er a .m .k . um 15 bús. to n n o g
neysSa er um 2 2 þús. to n n á ári (D e e ie r 1984, Usui 19 7 4 ). Áilinn er mikiö veiddur í
g ild ixir o g k istu r, en ein n ig á línu. A ll h eíu r lítið verið n ýttur á íslan di. E itth v a ð mun
hann þó h afa verið veiddur ti! m atar o g roðið n o ta ð i skóþvengi. Litlar uppiýsingar
liggja fyrir u m h v e r veiðigetan e r hér á iandi, en í N o re g i eru tö iu r um 3 -1 0 k g veiði a f
b jartái á h e k ta ra (K riste n se n 198 0 ).
A árun um 196 0 tii 19 6 4 v a r v e itt tö íu v ert m agn a f ál til ú tfíu tn in gs. Jón L o ftsso n o g
S am b an d Is le n sk ra S a m v in n u fé la g a sá um sö lu n a o g seldu lifandi o g rey k tan ál til
H o llan d s. V e itt v a r m eð á lag iid ru m v íð s v e g a r á landinu, e in ku m í S k a fta fe ilssý s lu m
o g á M y ru m í Borgarfirði. S u m arið 19 6 1 veiddust 15 tonn á öllu iandinu, ári síðar
v e id d u st 1 7 ton n . V e ið i m in n k að i o g áríð 1963 v a rð aílin n 13 to n n o g 196 4 v a r afli iítiil
(M a ría n n a A le x a n d e rs d ó ttir 19 7 8 ). A fti í Skaftárh rep p i v a r 3 ,5 tonn árið 1 9 6 1 , ári
síöar 4 ,1 to n n o g 1,8 to n n árið 19 6 3 , (Jón G u n n ar S ch ra m 19 9 3 ) Á iiin n fó r
smækkandi o g aflinn minnkaði, líklega v e g n a o f mikiíiar veiði á gu lá l. Á síðari árum
h afa á la v e ið a r frem u r lítið v e r ið stun daðar.
O ft er auðveldast a ó veiða b jartái i g ild ru r eð a kistur á leið tii sjávar. V ið b ja rtá la v e ið a r
eru v e ið itæ k i sett í e ð a v ið útfa ll vatn a. B ja rtá li, sem taiinn er betri m a tllsk u r, er stæ rri
o g íe ita ri en guláll o g h en tar v e i til reykingar. S líkar veiðar g e ta g e tið mikla veiði á
stuttum tím a o g frá Noregi eru dæ m i um þ rig g ja ton n a v e ið i á einni n óttu (Kristensen
1980). Þ á er mikíivægur k o s íu r v ið bjartálaveiðar að þ æ r æ ttu ekkí að ganga nærri
álastofhi viðkomandi v a tn s þ a r sem þ æ r b y g g ja á v e ið i fullvaxinna ála. Állinn er ekk i
taiin m yn d a sta ð b u n d n a sto fn a en h in sveg a r er v e ið iþ o i á h eild arstofn í e v ró p s k a álsin s,
m eð tillíti til n ý lið u n ar, ek k i þ e k k t.
4, Staðhættir og raimsóknaraðferðir.
T ilra u n a v e ið a r fó m fram í Á sg a u tss ta ð a v a tn i o g K a k k a rv a tn i í iandi B ra u ta rtu n g u í
S to k k se y ra rh re p p i. B ja r tá la v e ið a r v o r a kan n aðar í S k e r lló ð i en þar er sa m eig in leg t
afrennsii n o k k u rra v a tn a í S to k k se y ra rh re p p i íii s jávar (m ynd 1). A s g a u ts s ta ð a v a tn er
um 15 ha. a ð stæ rð o g v íð a s t um 2 m djúpt. K a k k a rv a ín er u m 10 ha o g v íð a st 1-2 m
að dýpt. V ö tn in eru b æ ði m eð g ró in n leðju b otn . B a k k a r eru g ró n ir o g g r ý ít ir að hluta,
e in ku m í K a k k a rv a tn i. í vö tn u n u m eru a u k áis staðb un dn ir o g s jó g e n g n ir u rrið a - o g
b le ik ju sto fn a r. V ö tn in h a fa v e r ið n ytjuð íli á la- o g s ilu n g sv e ið a á u n d a n fö rn u m árum .
F rá árinu 19 8 4 hefúr áll v e r ið veiddur á hverju ári. Árleg veiði 19 8 4 til 1990 v a r um 50
til 100 k g í 6 - 8 g ild ru r, a ð ja fn a ð i um 70 k g á ári. V e ið i árann a 19 9 1 v a r 100 til 190
k g í 10 til 20 gildrur, að jafnaðí um 150 k g á ári. Þ efta gerir að jafnaöi um 6 k g á ha. á
0,5 km
f--------------- 1
M yn d i . Y fir litsm y n d y lir v ö ln in þar sem tiira u n a rve iö a r íö ru fram .
ári. E k k i v e ró u r séð að v e ið i hafí fa rið m innkandi. S tæ rð álan n a h efur v e r iö b iö n d u ð
o g e k k i m erk ja n ie g u r m un ur miiii ára (H ö rð u r J ó elsso n rnunnl. uppl).
Veitt v a r í a gn la u sa r á la g ild ru r m eð i8 mm m ö sk v a í le ið a ra o g sm æ rri í p o k a , um 40
sm í þvermái. Giidrurnar voru settar út 25. o g 26. jú ií o g teknar u p p í byrjun 2. tii 8.
n ó ve m b er. I Kakkarvatni voai a ð jafn aði 9 gildrur. E in v a r í innrás 6 í miðvatni o g 2 í
útrás. í A sg a u ts s ta ð a v a tn i v o m 10 tii 13 g ild m r. E in v a r í ú trás o g 7 til 10 í
m iðvatn i. G ild ra rn a r í vö tn u n u m v o ru m eð tv eim u r p o k u m o g le ið a ra á m ílli. í
S k e rfló ð i v a r ein slík g ild ra fram a n a f tim abilínu o g ön n ur m eð tv e im u r v æ n g ju m m eð
g ild r u p o k a í m illi. Sú g iid ra n áði m illi b a k k a í straum vatni o g v a r æ tla ð a ð v e ið a bjartál
á leið tii sjavar. Fyrsta á g ú st v a r sett m un stærri o g öflugri gildra um Im í þvermál.
G ild ra n n a v a r v ít ja ð re g lu le g a , o fta st n ieð u m v ik u m illibili o g afli talinn o g v e g in n úr
h verri g ild ru . H lu tsýn i v o m síðan tekin til e in sta k iin gsm æ lin g a á len gd , þ y n g d o g til
a ld u rsgrein in g ar. F yrir a id u rsg rein in g u v o m k varn ir látnar lig g ja í 9 6 % a lk ó h ó ii y fir
nott. A id u rsg re in in g á ál er erfið þ v í álar eiga tii að m vn d a íleiri en einn árh rin g a ári
(D e e le r 1 9 8 1) .
V ið k ö n n u n á útbreíðslu áis á Suðurlandi (Árnes- Rangávaila- o g
V e s tu r s k a fta fe lIs s ý s lu ) v a r stu ðst v ið lan d ak ort L a n d m æ iin g a íslan ds (m æ lik v a rð i
1:100000 o g 1:50 0 0 0 ) o g sk rá O rk u sto fn u n a r um v ö tn stæ rrí en Í0 h a (H á k o n
Aðalsteinsson ofl. 198 9). S tæ rð vatnanna var fen gin í skránni, en Ieiðrétt e f v ita ð var
a ð vatnið hafi minnkað t. d. v e g n a framræslu. Taiað v a r v ið b æ n d u r í n ágrenn i
v a ín a n n a o g þ e ir sp u rðir h v o rt b e ir v issu til þ e ss að áll væ ri í v ið k o m a n d i va tn i. E in n ig
v a r s tu ð st v ið tiltæ k a r r itað a r h eim ild ir (sbr. M a g n ú s Jóh an n sson 19 9 3 ) o g ó b irt g ö g n
V e ið ím á la sto fn u n a r. U tb re ið slan v a r e in g ö n g u ath u g u ð í v ö tn u m , en læ k ju m o g ám
sleppt.
A fla úr g ild ru m v a r h aid ið íifan di í þar til g e rð u m g e y m slu k a ssa . H lu ti álan n a v a r
tek in n þ a ð a n til tiiraun avinn siu . G e r ð v a r tilraun m eð h e itrey k in g u . K jö tv in n s ia
H a fn ar-Þ ríh y rn in g s sá um tilraun avinn sluna. H e itre y k tu r áll v a r sm a k k a ð u r a f
matreiðsiumeisíumm kunnugum ál. Einnig v o n i fleiri fen g n ir til að sm a k k a o g g e fa álit
sitt á afurðinni. Spurt v a r um eftirfarandi þætti; b ra g ð útlit, áferð, mýkt, salt. Þá var
spurt um ííklegar markaðshorfur. A u k þ e ss v a r g e rð lausleg m a rk a ð s- o g v e rð k ö n n u n
innanlands.
6
5. Niðursíöður.
5. I Tilraimaveióar.
5. i. 1 Afli í tilraunaveiðuni
H eild araíli í tilrau n aveiðu n u rn v a rð 392 álar o g 103 kg.
í Ásgauísstadavatni v e id d u st 12 7 álar (37,1 k g ) í 9 71 g iid ru n æ tu r (ta fla 1). M egin h lu ti
þeirra v a r g u iá ll (9 5 % ). E in u n g is 6 b jartálar (3 ,5 k g ) v e id d u st, flestir í síðarih luta
águst. E inn þ eirra v a r 1 ,5 k g o g v a r þ a ð stæ rsti állin sem ve id d ist. A fli í g iid ru n ó tt v a r
að m eðaita ii 0 ,13 álar o g 0 ,0 4 k g . M e ð a lþ u n g i alira álanna v a r 290 g. í m iðvatn in u
v a r aflinn 100 áiar ( 2 7 ,7 k g ) o g í ú tfailin u 2 7 álar (9 ,4 k g ). A íli í g ild ru n ó tt v a r að
ja fn a ð i m eiri í m iðvatn i en í ú tfa liin u e ð a 0 ,15 álar o g 0 ,13 í ú tfa liin u . / íiarn ir í ú tfa liin u
v o ru hins v e g a r h eld u r þ y n g ri e ð a að ja fn a ð i 348 g o g 2 7 7 g í m iðvatn in u . A íli í
Asgautsstaðavatni v a r 2 ,5 k g á ha. Þ a r a f v a r 0,23 k g bjasrtáll. B esti ve ið itím in n í
Asgautsstaðavatni v a r í fyrrihluti á g ú st o g v a r veiði lítil eftir ágústiok (m yn d 2).
í Kakkarvatni veíddust 22 3 á iar (48,4 k g ) í 8 18 gíidrunætur. Meginhluti þ e irra (9 4 % )
v o ru grein d ir sem gu lá lar. Þ rettán v o ru b jartálar (6 ,4 k g ). F le stir (5 ) b jaríá larm a k o m u
i' útrásin n i síða st í sep íem b er, Afli í g iíd ru n ótt var að jafnaói 0 ,2 7 álar o g 0,0 6 kg.
Meðaiþungí allra ála v a r 2 1 7 g. I miðvatninu v a r aflinn 186 áiar (2 7 ,7 k g ) o g í útfallinu
30 álar (9 ,4 k g ). Afli í giidrunótt v a r að ja fn a ð i m eiri í miðvatni en í útfaliinu eð a
0 ,282 álar o g 0 ,2 1 1 í ú tfa liin u . AÍamir í útfailinu v o n i hins vegar heldur þyngri eð a
að jafnaði 3 1 5 g o g 201 g í miðvatninu. Aflí Kakkarvatns v a r 4,8 k g á ha þar a f v o ru
0 ,64 k g b jartáli. * A fren n sli a f sam tals 58 ha.
T a tla 1. A íli í tilra u n av eið u m í á la g ild ru r í v ö tn u m í S to k k e y ra rh re p p i su m aríð 19 9 5.
V a tn S tæ rð F jö id i H eild araíli A fli á g ild ru n ó tt A fli á ha.
h a g ild ru n . F jö ld i K g F jöldi K g M e ð a lþ . k g
1 2 7 3 7 ,1 0 ,13 0 ,0 4 290 2 ,5
223 48 ,4 0 ,2 7 0,06 2 1 7 4 ,8
42 1 7 ,5 0 ,3 1 0 ,13 4 1 8 0,3
Á s g a u ts ta ð a v . 15 9 7 1
K a k k a rv a tn 10 8 18
S k e rfló ð 5 8 * 136
S am tals 19 2 5 39 2 103 0,20 0,05 263
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Mynd 2. A flí i tilra u n a v eið u m á ál i v ö tn u m v ið Stokkseyri 19 9 5. Veióín í vötnunum
v a r n æ r e in g ö n g u g u lá ll en í ú trás í Skerflóði, b jaríá ll. Á m ynd er afii settur
v ið vitjunardag en er i raun afli á timabílinu frá síðustu viljun aó vitjunardegi.
V tá k n a r v itju n a rd a g án aíla.
U r k o in a ii! n i L o f t h i t i °C
M y n d 3. L o fth iti (só la rh rin g sm eð a lta l, ° C ) o g só la rh rín g sú rk o m a (m m ) á
E y ra rb a k k a á ieg u fím a gildran na.
8
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10
8 -
6
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C~C CN O'J CC
Skerflóö
Lengd mm
□ Guláll
HBiartáll
M yn d 4, L e n g d a rd re ifin g á ál ú r tilraanaveiðum í vö tn u m v ið S ío k k s e y r i árið 1995.
I innrennsli v a r ein giiclra frá 2 5 . jú lí til i I. ágú st. A ílin n v a rð 7 álar ( 1 ,7 kg) á 16
g ild ru n ó ttu m e ð a aó jafnaði 0 ,4 4 álar á gildrunótt. Meöalþunginn v a r 243 g, Afiinn
í K a k k a rv a tn i v a r m jö g d re ífð u r y fir ve ið itím ab ilið (m ynd 2).
I Skerf/óói v a r sé r s ía k le g a reynt að afla bjartáSa á leíð til sjávar. Þar er afrennsli um 58
ha v a tn a sv æ ð is . S a m ta ls v e id d u st 42 álar ( 1 7 ,5 k g ) í 136 g ild ru n æ tu r. Þ e tfa vo ru
n æ r a llt bjarkí/ar. A ð m e ð a lta li ve id d u st 0 ,3 1 áll o g 0 ,13 k g a g ild ru n ó tt. M e ð a lþ u n g i
áianna v a r 4 1 7 g. V e ið ín v a r m jö g Íítíi í ágú st o g fyrri h luta sep tem b er. N æ r alíur
bjartáilinn (83 % a f fjö íd a ) k o m í g ild ru rn ar í síðari hluta sep tem b er o g fyrstu v ik u í
O 4 OO CN
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M vnd 5. Þyngdardreifing á ál úr tilraunaveiðum í vö tn u m v ið Stokkseyri árið 1995,
október (mynd 2), Athyglisvert er að á þeim tím a v a r ú rk o m u sa m t, sem olíi aukn u
vatnsrennsli o g lo fth iti læ k k a ð i (m yn d 3). Afli bjartála 1 Skerflóði varð um 17 k g , e ð a
0,3 k g á ha., en a ð v ið b æ ttu m bjaitálaafla í Ásgautsstaðavatni o g Kakkarvaíni va rð
bjartáiaafiinn sam tais 2 7 k g , e ó a um 0,5 k g á ha.
A th u g a ð v a r h v e rsu stórt h lu ífa ll a f álnum v a r y fir 150 g , sem er áætluð lá g m a rk sstæ rð
til sölu. I v ö tn u n u m voru 68 % álar yfir 150 g sem gerir 2,3 k g a f nýtanlegum ál á
hektara. I Skerflóði v o r u 9 6 % nýtanleg, en þar v a r aðeins einn bjartáll un dir 150 g. A f
heildarafla v a r h lu tfa llið 73 % sem ge rir 75 k g eð a 1,3 k g a f n ýtan legu m ál á h ektara.
1 0
Lengd mm
M yn d 6. S am b an d iengdar o g þyngdar hjá gulál o g bjartál í vötnum vió S to k k s e y r i
árið 19 9 5.
5 . 1 . 2 Vinna viö veiðar.
V itjun gild ran n a í vö tn u n u m tv e im u r (g u lá la v e ið a r) tó k um 2 tím a i senn en þeirra v a r
vítja 9 sinnum á tím abílinu . Samtals tók vitjun því 18 klst. fyrir einn m ann. Akstur va r
lítilí þar sern vö tn in eru í innan við km íja r læ g ð írá bæ . Vitjun á bjartálagildru tók um I
klst. í senn, sam tals 9 k lst. A k s tu r va r sam íais u m 60 km . V in n a v ið a ð korn a ál á
markað v a r áæ tíu ð 6 kist. S a m ta ls v o ru vinnustundimar þ v í 33 o g afíinn þ v í 2,3 k g á
h verja vinnustund. Afrakstur í vötnunum v a r 3 ,2 k g a f nýtanlegum á! á vinnustund við
v e ið a r o g 1,9 k g í b jartáfag íld ru í S ke rfló ð i.
5. 1. 3 Lengd og þyngd.
L en g d a r- o g þ y n g d a rd re ifin g áianna (ú rtak úr afla) k em u r fram á m vn d u m 4 o g 5,
skipt eftir veiðistöðum o g g e rð (bjartáll, gu láll). Minnstu áiarnír í úrtakinu v o ru 36
sm (6 2 g ) o g þ e ir stæ rstu 74 sm (73 0 g ) en flestir vo ru 45 tii 55 sm (1 5 0 -2 5 0 g).
300 400 500 600
Lengd m tn
700 800 900
0,110 ■
0.100 -
0,090
3 0.080 -
.3
0,070 -
0,060 -
0,050 -
0,040 -
3f
B ja r tá ll
500 700 900
Lengd m m
M yn d 7. S am b a n d h lu tfa lls le g s h o ld a stu ð u ls o g len gd ar hjá gu la l o g bjartál.
G u lála r v o ru a ð ja fh a ð i m inni en bjartálarnir. M e ð a ls tæ rð g u lá ia v a r 4 9 sm o g 2 1 2 g ,
en b jaríá la 5 7 ,3 o g 3 7 1 g. M in n sti b jartállinn v a r 40 sm 121 g en atlir a ð rir v o ru y fir
50 sm o g 240 g. A m ynd 6 k em u r fram sam band ien gd a r o g þ yn gd a r. N o k k u r m un ur
ko m fram m illi g u lá la o g b jartála. B ja rtá la r eru þ yn gri en g u lá la r a f sö m u lengd.
H lu tfa llslegu r h o ld a stu ð u ll (þ a r sem leiðrétt er fyrir len gd ) er ein n ig hæ rri h já b ja ríá l en
gu lál sem g e fu r til kyn n a að b ja ríá lar séu þyn gri en gu lá ia r a f sö m u Sengd (m yn d 7).
5. 1 . 4 Aldur, vöxtur og k>7i.
A íd u rsgrein d ir v o ru 52 áiar, 24 b jartálar o g 28 gu lá lar. A ld u r álan n a v a r frá 5 ára til
15 ára. A ld u r b ja ríá lan n a v a r að ja fn a ð i hæ rri en g u lá la (ta fla 2). Y n g s tu g u lá la m ir
vo ru 5 ára en eístu 13 ára. H in s v e g a r v o ru y n g stu b jartálarn ir 6 ára o g þ e ir elstu 15
ára (m ynd 8).
T a fla 2. M e ð a la ld u r a ld u rsgrein d ra g u l- o g bjartála.
B jartáll M e ð a la ld u r (ár) 10,2
S ta ð a lffá v . 2,1
F jö ld i 24
G u láll M e ð a la ld u r (ár) 8,6
S ta ð a lfrá v . 1 0 , 1
F jö ld i 28
V ö x tu r álanna, sem m e ð a lle n g d ir eftir aldri (m yn d 9 o g ta fla 3 ), v irð ist n o k k u ð ja fn
fram að 11 ára aldri (60 til 70 sm ). B ja rtá la r eru að ö llu jö fn u stæ rri en g u lá la r a f sam a
aldri o g hafa þ a r a f le iðan d i v a x ið hraðar. M e ð a lá rs v ö x tu r til 10 ára a ld u rs er 5 ,7 sm
hjá gu lál en 6 ,1 sm hjá bjartái.
K yn v a r a th u g a ð hjá 34 á lum , 2 6 b jartálum o g 8 gu lá lu m . B ja rtá la rn ir v o ru 41 til 73
sm o g gu lá larn ir frá 52 til 66 sm . A llir áíarnir, u ían einn, v o ru h iy g n u r. M innsti
bjartállinn (41 sm ) v a r h æ n gu r (6 ára). M ln n sta b jartálah ryg n an v a r 50 sm (9 ára).
1 4
800
7 0 0 -
6 0 0 -
1 500 -
1 4 0 0 -
-J 300
2 0 0 -
1 0 0
0
3 5 7 9 11 13 15 17
A ld u r ár
M y n d 9. M e ð a lle n g d g u lá la o g b jartála eftir aldri.
5. 2 Ifíhreiösta áls í vöimim á Suðurlandi.
Sam k væ m t v ið íö lu m v ið s ta ð k u n n u g a o g öðrum h eim ildum er ál að tin na í 31
stö ðu vatn i o g tjörn u m (stæ rri en 10 ha) á Suðuriandi. Flest þessara va tn a eru i
lágsveitum o g n álæ g t sjó. 011 n em a tv ö e m í innan v ið 50 m. h æ ð y iir sjávarm áli.
Það sem ein ken n ir g e r ð þ e irra ö ð r u frem u r er h versu sm á o g g m n n þ au eru (ta íla 4).
E ins o g á ðu r er g e t ið er h ér ek k i u m tæ m an di ú tb re ið slu k ö n n u n að ræ ð a þar sem ek k i
eru tekin m eð ár, læ k ir o g smærri vö tn . G e r a m á ráð íy rir að hann sé v íð a að finna s'
ým sum ám o g ek k i síst sk u rð u m o g iæ k ju m í lágsveitu m .
Vitað er að ál er að fínna í Ölfusi, eínkum Ölfusforum, í Ö lfu sá , Flvítá o g í B rú a rá allí
að Spóastöðum. H in s vegar eru ek k i spurnir a f ál ofar í Brúará eð a í Apavatni þ a r sem
þó æ ttu að v e ra g ó ð sk ily rð i fyrir hann (grun nt vatn ). Þ á m á n efh a að ek k i e m spurnir
a f því að áls hafí o r ð ið va rt á v a tn a s v æ ð i Þ jó rsá r o fa n v ið U rrið a fo ss . F ram k o m í
sam tölum v ið m enn, sem o g í r itu ð u m heim ildum , að a llm ö rg v ö tn hafi v e r ið ræ st fram ,
þau m innkað o g sum eru h o rfin v e g n a fram ræ slu.
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T a fla 4. S k rá y fir v ö tn á S u ð u rla n d i stæ rri en 10 ha. þar sem ál er að
finna. S tæ rð va tn an n a er m iðu ð v ið va tn ask á r O rk u sto fn u n a r (H a k o n
A ð a is te in sso n 19 8 9 ).
Meðal- H æ ð yfir
H rep p u r H e iti v a tn s S tæ rð , ha dýpi m sjó m.
S tö ð u v ö tn :
Ö lfu sh rep p u r H líð a rv a tn 330 2,9 1
G a u lv erjab æ ja rh r, K le p p sv a tn 1 3 <2 5
G a u lv erjab æ ja rh r. B æ ja rv a tn 15 <2 10
G au iv/ S to k k s e y ra r h r H ó iav atn 22 <2 5
S to k k se y ra rh r. S k ip a v a tn 24 <2 5
S to k k se y ra rh r. T ra ó a rh o ítsv a tn 33 < 2 4
S to k k sey ra rh r. V a tn v e sta n T rh v. 12 <2 5
S to k k se v ra rh r. V a tn n o rð v . T ó fta v . 10 <2 5
S to k k sey ra rh r. T ó fta v a tn 11 <2 5
S to k k se y ra rh r. L a n g a d æ l 10 <(9 5
S to k k se y ra rh r. K a k k a iæ a tn 10 5
S to k k se y ra rh r. Á s g a u ts s ta ð a v a tn 15 <2 5
S to k k se y ra rh r. S e lv a tn 11 <0 ■j
S to k k s e w a rh r . H a flið a k o tsv a tn 11 <2 9
H ra u n g erðish r. L a u g a rd æ la v a tn 40 <2 22
G rím sn esh r. H e stv a tn 680 2 3 ,7 50
Á lfta v a tn G rím sn eslir . 250 ? 15
V illin g a h o itsh r. K rá k u v a tn 10 <2 5
V illin g ah oltsh r. V illin g a h o ltsv a tn 71 <c'2. 15
Á sa h rep p u r F ra k k a v a tn 74 <2 10
Á sa h rep p u r F írú tsva tn 238 <2 10
V -L a n d e y ja h r. S k ú m s sta ð a v a tn 222 <2 10
V -L a n d e y ja h r. K u g g a v a tn 10 <2 10
R angárv'allahr. L a m b h a g a v a tn 1 1 <2 1 5
M ýrdalshr. O d d n ý ja rtjö rn 31 <2 90
S kaftárh r. M jó á s v a tn 40 <2 15
Skaftárhr. V ík u r f ló ð 14 <2 1 5
Skaftárhr, F ítja r fló ð 50 <2 15
Skaftárhr. S te in sm ý ra rfló ð 10 <2 15
Skaftárhr. S y stra v a tn 24 <2 121
Sjávar/óf!;
V -E yjafja liah r. H o lts ó s 780 <2 0
M ýrdalsh r. D y rh ó la ó s 370 <2 0
1 6
Reykþyngd A
500 -1............. :........... ; : ..................... ...................
4 50 j
400 -j
350 |
300
2 50 ;
200 -j
150 -j
1 0 0 j
50 j
0 100 200 300 400 500 600 700
Ferskþyngd g
Hlutfall af ferskþyngd
74 .0 :
72 .0 J
70 .0 ■;
68.0 j
66.0 ;
6 4 .0 j
6 2.0 j
6 0.0 4
0
M ynd 10. A . F y lg n i þ u n g a hjá fersk u m ál o g ál eftir verk u n . B. F ylg n i h lu tfa ils le g s
þ u n g a hjá ál e ftir ve rk u n o g ferskþ u n ga.
5. 3 7 /7rciunav innsla.
Aöferóir. A llin n v a r tek in n inn lifandi til vin nslu d a ga n a 18. á g ú s í o g 2 5 . sep tem b er.
Fyrir verkun v a r áilinn drepinn i sa ltpæ kli o g síðan slæ gð u r. Því næst var hann
skolaðu r í renn andi va tn i o g slím húð strokin af. Þ á v a r hann settu r a ftu r í p æ kil,
hengdur upp o g slím h ú ð stro k in af ö ð ru sinni, A ð þ v í iokn u v a r állinn h e itre y k tu r i
o
p<0.05
100 200 300 400 500 600 700
Ferskþyngd g
reykofni. Athugað v a r hvernig h ver ein staku r áll léttist við verkun. S e x tá n álar a f
m ism unan di stæ rð u m voru einstaklingsvegnir fyrir o g eftír ve rk u n .
Rýrmm við verkitn. Þ u n gi eftir leg u í sa ltpæ kii va r að m e ð a lla li 9 5 ,6 % , a f
u p p h a íle g u m þunga, 4 ,4 % rymnun, o g eftir slæ gin gu o g heitreykingu 6 8 ,7 %, sem gerir
3 1,3 % rýn iu n . G ó ð sa m svö ru n v a r á milli upphaflegs þ u n g a o g þ u n g a úr ve rk u n
(m ynd 10 A ). M ik ill b re ytile ik i v a r á því hve álarnir iétíu st m ik ið í v e rk u n , en þun gi
eftir v e rk u n v a r alit í fá 63 % til 74 % a f u p p h a fíegu m þun ga.
R ýrnun virtíst fara eftir stæ rð þ ví sk ýr munur k o m fram í hlutfallsiegri rýrnun eftir
stæ ró (rnynd 10 B ) . Á la r u n air 400 g v o ru flestir undir 70 % a f u p p h a fle g u m þ u n g a
eftir ve rk u n o g þeir sem v o ru y fir 400 g v o ru flestir y fir 70 % a f u p p h a fle g u m þ u n ga.
S tæ rstu r hluti þ e ssa á la v o ru b jartáiar.
5. 4 Markaösaihugim.
Markaður.
Innflutningur: In n flu tn in gu r á ál er rnjög lítill eð a aðein s um 10 0 -20 0 k g . á árinu 19 9 4
(sam kvæ m t in n flu tn in gssk ýrsiu m H a g sto fu ísian d s).
Innanlandsframleiðsla: V e r k u n á ál innaniands er iítii í d a g en m ikill áhugi er iyxir að
auka fram ieiðsiu n a t.d . hjá a ð ilu m í H afn arfirði.
Efiirspurn: E ftirsp u rn e ft ir ál virðist ek k i vera mikil. Þ ó er Ijóst að á h u gi er á vörunni
o g hafa m a rg ir sm a k k a ð hana, þá eín kum eriendis. E kk i er ó lík le g t a ð e f áli væ ri
veiddur o g v e rk a ð u r hér heima þá væ ru m ö g u ie ik a r á að byggja upp markað fyrir hann
innanlands o g h u g sa n le g a til ú tflu ín in gs.
Gceði afurðanna. T ii þess að k an n a gæ ð i afurðan n a úr íilrau n avin n siu n n i v a r efn t tii
sm ökku n ar í e ld h ú si B æ n d a sa m ta k a n n a 13. o k tó b e r 19 9 5 . F en g n ir v o ru n o k k rir
starfsm enn sam ta k a n n a o g ein n ig n o kk rir m a tre ið slu m eista ra r til a ð sm a k k a á
a íúrðun um . S p u rt v a r um eftirfarandi þæ tti; b ra g ð , útlit, á fe rð , m ý k t, sa lt o g líklegar
m arkað sh orfu r.
N iðurstöður eru sem hér segir:
1. B ra g ð : F iestu m fann st afurðin bragðast m jö g v e l eri þ ó farm st nokkrum
hún v e r a í d a u fara lagi.
1 8
2. U tiit
3. Á fe rð
4. M ý k t
5. Sait
F iestu m fan n st útiitið g o tí, n o kk ru m þ o k k a ie g t .
A fe r ð þ ó íti g ó ð .
Flestum fann st m ýktin g ó ð , nokkrum fann st hún “óstöðug”.
M æ tti v e ra saltari, sum um fannst afurðin h æ fíie g a sö ltu ð .
6. L ík le g a r m a rk a ð sh o rfu r : F iestir tö ld u að a fu rðin h ljóti að se lja st ve l sem
m atur fyrir sæ lk era o g þ ó ein ku m í v e itin g a -
húsum .
Markaðsverð. S a m k v æ m t k ö n n u n sem ge rð va r í veitingahúsum á Reykjavíkursvæðinu
þá er in n k au p sverð á re y k tu m ál um kr. 1 .50 0 ,- pr. kg.
Framleiðslukostnaður. Miðað við tíu ton n a v e ið i á ári o g 7 0 % nýtingu verður
fram leið slu k o stn a ð u r pr. kg. a fu rð (v e rð ífá vin nsíu) um kr. 1 .2 0 0 .- pr. k g .
Nidurstödur h agk vœmnismats.
N iðu rstöðu r eru þ v í þ æ r a ð , m ið a ð v ið tíu to n n a v e ið i á ári e ð a m eira, þá. g e tu r vin nsia
á ál verið h a g k v æ m . Á þ a ð skal þ ó bent að ek k í er h efð íy rir neysiu á ái á ísiandi
þanníg að m a rk a ð sh o rfu r eru ó þ e k k ta r .
6 . Umræða.
ó. 1 Veiðar.
Aili í tiirau n aveiðu m v a r 0 ,20 áiar, 0,05 k g á g ild ru n ó tt o g 1,8 k g á ha. V e ið i á
flatareiningu v a r b e st í Kakkarvatni, 4,8 k g . A fli sem k g á gildrunótt v a r m estu r í
bjartáiagildruna í S k e rfló ð i, 0 ,13 k g . í tilrau n aveiðu m í S k a ftá rh re p p i árið 19 9 1 v a r
m eðalveiði m jö g m isrnunandi eftir vö tn u m eð a frá 0 ,1 4 til 0 ,6 7 á lar e ö a 0 ,0 9 til 0 ,1 5 k g
á giidrunótt (Jón G . S ch ra m 19 9 3 , M a g n ú s Jóhann sson 19 9 3). Þ e tta er hins v e g a r
mun m inna en ve id d ist í F iíja r fló ð i í L an d b roti árið 19 6 2 , en þá v e id d u st a ð m eð a lia li
3,4 álar á g ild ru n ó tt. V e ið in v a r m est í ágú st eð a um 7,0 á la r á g ild ru n ó tt (Jón G ,
Schram 199 3), E k k i er ijóst hver skýringin er á minni v e ið i nú en áðu r, en samkvæmt
erlendum ath u g u n u m h efu r g le rá la g e n g d til E v ró p u m inn kað hin síðari ár (H a g strö m
o g W ic k s tr ö m , 1990).
1 9
M inna ve id d ist a f b jartál en v æ n ía m átti, e ð a 2 7 k g sern g e rir urn 0 ,5 k g a fra k stu r á ha,
Lítið er h æ gt að fu llyrð a um h v o rt slíks m egi v æ n ta á rle g a e ð a b ja rtá la g e n g d se
b reytileg á m illi ár. I ánni Im sa í N o r e g i, þar sem fy lg s t h efu r v e rið m eð
b jartálagö n gu m í á raraðir, h efu r b ja rtá la g e n g d v e rið að m eð a lta li 2 ,2 7 k g á ha, en
þ ek kt er að tö lu v e rð u r b re ytiie ik i g e tu r v e rið í m agn í b jartála frá ári tíl árs ( V c lle s ta c l
o g Jon sson 198 8, P ig g in s 19 8 5). í N o r e g i eru tö lu r um fra m le ið síu b ja ilá la ailt frá 0,2
k g til 10 k g á ha. Þ a ð er þ e k k í a ð b ja rtá la ge n g d er háð ým su m u m h v erfisþ á tíu m s.s.
hitastigi o g ú rko m u o g áil á þ að til að fresta ú tg ö n g u sinni milíi ára séu a ð stæ ð u r
ó h a gstæ ð ar (V o lle s ta d ofl. 199 4).
Bjartállinn v a r a ð a lle g a á íeið ú t síðari hluta sep tem b er o g fy rstu v ik u í o k tó b e r . Á ð u r
hefur ekki ve rið fy lg s t m eð b ja rtá la g ö n g u m hérlen dis, en þ etta sam ræm ist. v e l erlen dum
n iðurstöðum . I Im sa ánni í N o r e g i v o ru b jartáiar m est á ferð in n i í se p ie m b e r o g
ok tó b er (Vollestad ofl. 19 8 6 ) en í N o r ð u r-N o r e g i v o ru a ð a lg ö n g u rn a r í á g ú st o g
septem ber (B e rg e se n o g K le m e n tse n 198 8). D a g le n g d , vatn sh iti o g va tn sren n sli ásam t
tu n gistöðu era þæ ttir sem ta ld ir eru hafa mest áhrií' á h v en æ r b jarfállin n er á ferð til
sjávar (D e e ie r 198 4). Minnkandi daglengd, lækkandi hitastig að haustinu o g aukið
rennsli v irð a st ráðandi þ æ ttir í h v e n æ r ársins bjartállinn fe r til hafs. í Im sa vo ru
aðalgön gu rn ar þ e g a r vatn sh itin n v a r 9 til 12 ° C en g ö n g u r v irtu st s tö ð v a s t v ið hita
undir 4 °C (V a lle s ta d ofl. 19 8 6 , V a lle s t a d ofl. 199 4).
6. 2 Stœrð, akhir og vöxtiir.
Flestir ve id dir áiar v o ru 45 til 55 sm (15 0 -2 5 0 g). G u lá la r v o r u að ja fn a ð i rninni en
bjartálarnír. M e ð a ls tæ rð g u lá la v a r 2 1 2 g o g b ja ríá la 3 7 1 g , M irm sti b jartállínn v a r 40
sm 121 g, sem v a r h æ n gu r, en allir aðrir v o ru h rygn u r y fir 50 sm o g 240 g . S íæ rð o g
kynjahlutfall gu lá la er s sam ræ m i v ið þ a ð sem þ e k k t er erlen d is (V o ile s ta d o g Jon sson
1986, M o ria try 1989, V o IIe sta d 199 2). í vö tn u n u m v o ru 68 % á la y fir 15 0 g sem
áætlaö er að sé m innsta n ý ta n le g a stæ rð , o g í b jartáiagild ru í S k e rfló ð i 9 6 % , en þ a r va r
aðeins einn bjartáll u n dir 150 g. A f heiidarafla v a r 73 % a f n ýtan le gri stæ rð . I athugun
sem gerð v a r fjóru m v ö tn u m í S ka ftá rh re p p i árið 19 9 1 v a r h lu tfa ll n ý ta n le g s áls y fir
80 % í ölium vötnunum. Þ ar v a r állinn einnig stærri en i þessari kön n un eð a að
meðaltali frá 300 til 9 5 0 g , m isiuunandi eftir v ö tn u m (Jón G . S ch ra m 19 9 3, M a g n ú s
Jóhannsson 1993).
A ldur álanna v a r frem u r hár, Meðalaldur bjartála va r 10 ,2 ár o g gulála 8,6 ár. V ö x tu r
var því h æ gu r e ð a 5 ,7 sm á ári h já gu lá l o g 6 ,1 sm hjá b jartál. Astæðan fyrir því að
2 0
bjartálar v írð a st h afa v a x ið b e fu r en gulálar er trúlega sú að stæ rstu álarnir i hverjum
árgangí (h ra ð v ö x n u stu ) v e rð a iy r r b jartálar en jafnaaldrar þ eirra (V e lie s ta d o g Jon sson
! 986). V ö x tu r g u lá la v a r h eld u r m eiri en í F itjarfló ð i í L a n d b ro ti (5 ,1 sin) en á þ e k k u r
o g fék k st í S te in sm ý ra ríló ð i (6 ,1 sm ) (M a g n ú s Jóhann sson 19 9 3 ). A lg e n g u r á rsv ö x tu r
í n orskum vö tn u m er 5 til 7 sm á ári (V o lle s ta d 198 6) sv o ísien sk i áilin v irð ist hafa
álíka v a xta rh ra ð a o g sá n orsk i.
6. 3 Veiðimöguleikar á Suóurlandi.
Til að kanna h vert væ ri v e ið a n le g t m agn a f ái á S u ðu rlan d i v o ru g e rð a r 3 m ism unan di
áætianir (ta fla 5). Á æ tiu n 1 g e r ir ráð fyrir 1 k g a fla á h e k ta ra o g áæ tlun 2 g e rir ráð
fyrir 5 kg/ha o g áæ tlun 3 , 10 k g a fla á ha. Þ essi afli er á æ tla ð u r ú r v ö tn u m m eð innan
við 2 m m eð a ld vp i. í v ö tn u m m eð 2 -5 m rn eð ald ýp t er fra m ie ið sla á æ tlu ð heim in gi
minni. F ram ieiðsia v a tn a m e ð y íir 5 m m eð a id ýp i er áæ tlu ð 1/5 a f fram leið siu v a tn a
grynnri en 2 m. A æ tla ð a r a fla tö lu r í v ö tn u m eru sa m k v æ m t þ e ssu m fo rsen d u m ailt frá
Tafla 5. Á æ tlu n u m þ a ð m a gn sem unnt er að v e ið a á rleg a a f ál í v ö tn u m á
S u ðu rian d i. S k ip t e ftir hreppum . S já frekari sk ý rin g a r í texta .
Fíreppur S tæ rð
ha
A fli k g á ári
A æ tlu n 1 A æ tlu n 2 Á æ tlu n 3
Stöðuvötn:
Ö l& sh rep p u r 330 165 825 1650
Gaulv/ S to k k se y ra riir 50 50 250 500
Stokkseyrarhr. 14 7 147 73 5 1470
H raungerðishr. 40 163 200 400
Grim sneshr. 680 266 680 1360
V iilingaholtshr. 81 81 405 8 10
Á sahreppur 3 1 2 3 1 2 1560 3 12 0
V -L andeyjahr. 2 3 2 2 3 2 1 16 0 23 20
R angán'ailah r. 11 1 I 55 110
M ýrdalshr. 31 31 155 3 10
Skaftárhr. 15 4 15 4 770 1540
Sam tais 2068 1 6 1 2 6 7 9 5 13590
Áællun 1 . gerir ráö fyrir 1 kg afla á ha. í vötnum meö meðaldýpi innan viö 2 m dýpi.
áætlun 2 gerir ráð fyrír 5 kg/ha og áætlun 3, 10 kg afla á ha. sjá frckar í íexía.
2 1
1,6 til 13 ,6 íonn. H é r eru h á lfsö lí sjávarlón ekkt tekin m eð vegna óvissu urn það
hversu m ikið þau kun n i að g e fa a f sér. Út frá ve ið itilra u n u m í þessari
kön n u n ,veið ireyn siu í v ö tn u m v ið Stokkseyri, í S ka ftá rh rep p i (Magnús Jóhannsson
199 3) o g erlen du m u p p lý s in g u m um afra k stu r vatn a (T e sc h 19 7 7 , D eeSer 198 4,
K ristensen 198 0 , V s l le s t a d o g Jon sson 198 8 ), ásam t tö lu m um afla í þ essu
tilraun averkefni m á æ tla a ð á æ tlu n 2 sé lík leg u st, en þar er g e rt ráð íýrir 6,8 ton n a afla í
vötnum . Til v ið b ó ta r k æ m i fram leið sla á ál úr ám o g læ kju m o g h álfsö ltu in
sjávarlónum . Þ á er o g ó k a n n a ð u r sá m ö g u le ík i að v e ið a ál í sjó , t.d. í sk erja g arð in u m
miili Þ jórsár o g Ö lfu sá r , eri þ a ð er ve l þ e k k t erien dis að hluii á la elst u p p í sö ltu m sjó
(Vollestad 198 6). Þ e tta hefur ekkert verið kannað hérlendis. Þar sem ákveðin ó vissa
er í áæ tlunum sem þ e ssu m m á æ tla að raun hæ ft sé að ársaíli a f ál á S u ð u rla n d i geti
verið 5 til 10 tonn. M ö g u le ik a r tii v e ið a eru d re ifð ir o g v íð a st h v ar er v e ið a n le g t m agn
tiltöluiega lítið á hverjum stað. M e stu möguleikar v irð a st í iágsveitum
R an gárvallasýslu , F ló a , Ö lfu s i o g S kaftárh rep p i.
H vort g n m d v ö liu r sé fy r ir v e ið i b æ n d a b y g g is t að m iklu leyti á a ð stæ ð u m h já hverjum
bónda. L jó st v irð ist a ð ek k i er um m iklar te k ju r að ræ ð a fyrir h vern o g einn
landeiganda. S am h lið a g u lá la v e ið i æ tti að reyn a fre k a b ja rtá la ve ið a r þ ví tilk o stn a ð u r
v ið þæ r ve ið a r ætti í flestu tilfe llu m a ð v e ra rninni en v ið g u lá la v e ið a r. S am k v æ m t
niðurstöðum bjartáiaveiðanna er septembermánuður lík leg a stu r tíi að g e fa m esta veiði.
ó. 4 Verkun og markadur.
Þyngd álanna eftir v e rk u n o g reykingu v a r að meðaltali 6 2 ,4 % og 68,8 % a f
upphaflegum þ u n g a i tv e im u r verku n artilrau n u m . M ik ill b re y lile ik i v a r í h v e álarnir
léttust í verkun en þ u n gi e ft ir v e rk u n v a r allt frá 63 % til 74 % a f u p p h a fle g u m þun ga.
Rýrnun virtist fara e ftir s íæ rð , þ. e. sm æ rri állinn rýrnaði m eira en sá stæ rri.
Sam kvæ m t u p p lýsin gu m frá U su i ( 1 9 7 4 ) er áll eftír ve rk u n í h e itre y k in g u 60 % a f
upprunalegri þyn gd . S k ý r in g in á þ essu m m un gæ ti leg ið í m ism unan di stæ rð á ls o g
ekki er ó lík le g t að ó lík a r a ð fe rð ir v ið söltun o g h eitreyk in g u va ld i m isrnunandi
þyngdaríapi.
Lausleg athugun á m a rk að i sýn di að m a rk að u r er iítill fyrir ál inn anlands o g fram b o ð
viróist einnig lítið. A k v e ð n ir v e itin g a sta ð ir n álæ gt v e ið isv æ ð u m , sem te n g d ir eru
ferðaþjónustu, gæ tu sk a p a ð sér á k v e ð n a serstö ð u m eð því að hafa ál á b o ð stó ln u m .
A thyglisvert er að áh u gi er fy rir vö ru n n i o g m arg ir v irð a st hafa sm a k k a ð ál, einkum
erlendis. Því er ek k i ó lík le g t að e f áll væ ri veiddur o g verkaður hér h eím a væru
möguleikar á að b y g g ja u p p markað. Eins er lík leg t að einhver markaður sé fyrir
ferskan ál en a u k þ e ss g æ ti ú tílu tn in g u r k o m ið tii grein a sem þ ó er ó k a n n að . Fram
kom í sa m íö lu m v ið v e itin g a m e n n að stö ð u g t fram b o ð skipti m iklu máii.
N ið u rstö ð u r h a g k v æ m n ism a ts b en d a til þ e ss að m eð tíu to n n a v e ið i á ári e ð a m eira,
geti vin nsla á ál v e r ið h a g k v æ m . A æ tiu n um v e ið a n leg t m a gn á Su ðu rlan d r g e rir ráð
fyrir að v e ið a n le g t m a gn sé u m 5 til 10 tonn á ári. Þ v í v irð ist Ijóst að h æ p ið sé að
b yg gja vin nslu e in g ö n g u á su n n len sku m ál.
H ér h efu r e in g ö n g u v e r ið ræ tt um ál til n eyslu , en á laeldi, sem stu n d að er v íð a erlen dis
b yg gist e in v ö rð u n g u á að v e id d u r er áll til á fram eld is (U su i 19 7 4 ). Y m is t er n o ta ð u r
gleráll e ð a g u lá ll sem e k k i er kom in n í m arkað sstæ rð . Þ an n ig er sá m ö g u ie ik i íýrir
hendi að sm ár áll sem tæ st í v e ið u m til m anneldls geti n ýst til á ia e ld is hériendis.
G ru n d vö llu r slík s e ld is h é rlen d is er hins v e g a r ókann aður.
7. Þakkarorð
Framleiðnísjóöur Landbúnaðarins o g Atvinnuþróunarsjóður S e lfo s s veittu
fjárhagsstuðning til verkefnisins. H ö rð u r Jóelsso n , S æ v a r J ó e isso n bændur í
B ra u ta rtu n g u í S to k k se y ra r h re p p i v e ittu m a rg v ís leg a a ð s to ð v ið tilra u n aveiða r.
S ío k k se y ra rh re p p u r g a f leyfí til tilraunaveiða í landi hreppsins. Matreiðslumenn o g
íleiri a ð ila r g e r ð u bragðpróíún. Jón A . Bergsveinsson o g Margrét Ofeigsdóttir
aðstoðuðu v ið sý n a ö fíu n o g úrvinnslu gagn a. G u ð n i G u ó b e r g ss o n o g Jón A .
B e rg sv e in ss o n lásu handrit. Ö llu m þ e ssu m aðiium eru fæ rð a r b estu þ ek kir.
8 . Hetmiídir.
A vise, 3. C., N e lso n , W .S . , A r n o ld , J., K o e h n , R .K ., Williams, G .C . o g Thorsteinsson,
V . 1990 . T h e e v a lu tio n a ry g e n e íic sía tu s o f the Ieelan d ic eels. Evohdion.
4 4 (5): 1254-1262.
B ergersen, R . o g K lem e n tse n , A . 198 8. F re sh w a ter eel Anguilla anguilia (L ) from
N o rth Norway w ith emphasis on o c c u rre n ce , fo o d , a g e and downstream
m igration. Nordic Journal o f Freshwaíer Research. 64: 5 4-66 .
D eeler, C .L , 19 8 1. O n íh e a g e and g r o w th o f cu ltu red ee ls , Anguilla anguilia
(L in n eus, 175 8 ). Aquacniíure, 26 (1-2 ): 13-22.
D eeler, C .L . 1984. S y n o p sis o f b io lo g ic a l data on the e e l , , Anguil/a anguilla
(L in n eus, 175 8 ). FAO Fisheries Synposis No. 80, Revision L 73 . b ls
G uerault, D ., Y . D e sa u n a y o g R . L eco m te-F in ig er . 199 4. B io m e try and o to iith o m e try
oíÁnguilla anguilla (L .) g la ss eels: tovvards a m odei fo r sea so n a l v a r ia tio n 9
KÍFÁC'/JCES Fei Working Croup, Oviecio, Spain 199 4.
H agström , O , o g W ic k strö m , H . 1990. Im m igration o f Y o u n g E e ls to th e S k a g e rr a k -
K a tte g a t A r e a 1900 to 1989. Ini. Revue ges. Hydrohiol. 7 0 7 -7 1 6 .
H ákon A ð a lste in sso n , S ig u rjó n R ist, S tefán H erm an n sson o g S v a n u r P álsso n . 1989,
S tö ð u v ö tn á Islandi. S k rá um v ö tn stæ rri en 0,1 km2. O rku sto frm n ,
Vatnsorkudeild, OS-89004/VOD-02: 48 bls.
H araldstad, 0 . , V o lle s ta d , L , A . o g Jon sson , B . 198 5. D e sc e n t o fE u r o p e a n s ilve r
eels, Anguilla anguilla L., in a N o rw e g ia n vvatercourse. ./. Fish. fíiol. 26: 3 7 -
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Jón G unnar Schram . 199 3. Alamnmóbúr 1991. A tvin n u m á la n efh d S k a ftá rh re p p s ,
F Su K irkju b æ jark lau stri: 56 bis.
K ristensen, B , 1980. Alefiske Iferskvann. Landbruksforlaget Oslo. 36 bls.
M agn ús Jóhannsson. 1993, Fiskræktar- og fiskekJismöguieikar í Skafiárhreppi.
A ívin n u m álan em d S ka ftá rh re p p s, V e ið im á la sto fn u n S u ð u rla n d sd e ild ,
F iskeld isbraut F S u K irkju b æ jark lau stri: 39 bis.
Maríanna Alexandersdóttir. 19 7 8 . All á Islandi. Erindi flutt í útvarpi 16, m aí 19 78 .
V eiðim álastofn u n : 9. bls.
M oriarty, C . 1989. T h e silver eel c a íc h on th e lo w e r river S h an n on , Ireland. Furopean
Iniand Fisheríes Ádvisory Commissíon Working Parfy on Fei, Porio, 29 May-
3. june, 1989: 14 bls.
Piggins, D.J. 198 5. The silver eel runs of th e Burrishole river system : 1959-84.
N um bers, w e ig h ts , íiming and sex ratios. ítuernaííonai coimcii fo r íhe
Exploration o f íhe Sea, Anadromous-Catadromous Fish Commiítee C.M.
I985/M:5, Copenhagen,
Sadler, K . 1979. E ffe c í o f temperature on the grovvth and survival o f th e European
eel, Anguiila anguilla L . J.Fish fíioi. i 5, 4 9 9 -5 0 7.
Sígurður M. Einarsson. 1984. Áll, nytsemi hans og ræktun. Frcyr 53: 9 38 -9 4 0 .
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Usui, A. 1974, Eel culture. Fishing N e w s Books Limited, Farnham, Surrey: 1 1 8 bls
2 4
V ^ llestad , L . A . 198 6. L iv sh isto rie n til eu ro p eisk ál. Fau/ia, 29: 1 1 7 - 1 2 5 .
V o lle sta d , L. A . 199 2. Geographic variation in a g e and length ai rn eía m o rp h o sís o f
m aturin g E u ro p ea n eel: environm enta! e ífe c ts and p h e n o ty p ic plasticity.
Journal o f Animal Ecofogy, 6 1: 4 1-4 8 .
V o liesta d , L .A . o g Jon sson , B . 198 6. L ife - h isto ry ch a ra cte ris tic s o f th e E u ro p e a n eel
(A n g u illa an g u illa ) in th e ím sa R iv e r, N o rw a y . Transadions o f American
FisheriesSociety, 1 1 5 : 8 6 4 -8 7 1 .
V allestad , L. A , o g B . Jon sso n , 1988. A 13 -y e a r stu d y o f th e p o p u la tio n d yn a m ics and
g r o w th o f th e European eel Anguilla anguílla in a Norwegian river: E v id e n c e
o f d en sity-d ep en d en t m o rta lity , and d ev e lo p m e n t o f a m o d el fo r p re d ic tin g
yield . Jouni. o f Anim. Ecol., 57: bls. 9 8 3 -9 9 7 .
V o llesta d , L . A ., Jon sso n , B . , H v id ste n , N . A . o g N æ sje , T . F. 199 4. E xp erim e n tal
test o f en viro n m en tal fa c to rs influentin g the sea w a rd m ig ra lio n o f E u ro p ea n
silver eels. Journal o f Fish Biology 45: 6 41 -6 5 1 .
Vollestad, L .A ., Jon sson , B . , H v id síe n , N .A ., N æ sje , T .F ., H a rald sta d , 0 o g R u u d -
ITansen, J. 198 6, E n viro n m en taí F a cto rs R e g u la tin g th e S e a w a r d M ig ra tio n o f
E u ro p ea n S ilv e r E e !s (Anguilla anguilla). Can. ,/. Fish. Aquaí. Sci. 43: 190 9-
19 16 .
Williams, G . C . , R. K . K o e h n , o g V , Thorsteinsson. 1984. Ic e la n d ic eels: Evidence o f
a sin gle sp ec ie s oíAnguiIIa in N o rth A tla n tic . Copeia 1984: 2 2 1 -2 2 3 .
Environ Biol Fish (2008) 83:309-325
DOI 10.1007/s 10641-008-9341 -y
Inshore migration and otolith microstructure/microchemistry
of anguillid glass eels recruited to Iceland
Mari Kuroki • Momoko Kawai • Bjarni Jónsson •
Jun Aoyama • Michael J. Miller •
David L. G. Noakes • Katsumi Tsukamoto
Received: 13 June 2007 / Accepted: 25 October 2007/Published online: 6 March 2008
í© Springer Science + Business Media B.V. 2008
Abstract The timing o f catches o f anguillid glass
eels and their otolith microstructure and microchem-
istry were studied in southwest Iceland, where the
European eel, A nguilla anguilla and American eel, A.
rostrata have been thought to live sympatrically, to
leam about their early life history and the possible
mechanism o f the separation between these two
species ranges. Catches at the site studied suggest
that glass eels may have started upstream migration as
the river temperature warmed in late June and early
M. Kuroki (z+i) • M. Kawai • J. Aoyama • M. J. Miller •
K. Tsukamoto
Ocean Research Institute, The University of Tokyo,
1-15-1 Minamidai, Nakano,
Tokyo 164-8639, Japan
e-mail: mari@ori.u-tokyo.ac.jp
B. Jónsson
Institute of Freshwater Fisheries, Northem Division,
550, Saudárkrókur, Iceland
P , L . G . N o a k es
Department of Zoology and Axelrod Institute
of Ichthyology, University of Guelph,
Guelph, ON NIG 2WI, Canada
Present address:
D. L. G. Noakes
Department of Fisheries and Wildlife, Oregon Hatchery
Research Center, Oregon State, University,
Corvallis, OR 97331-3803, USA
July. The glass eels were mitochondrially identified
into two species, A. anguilla and A. rostrata , although
the latter were likely hybrids between the two species
based on a different study. Otolith analyses showed
no sharp increases in otolith increment width or sharp
decrease o f otolith Sr:Ca ratio in either species, which
are the characteristic changes corresponding to the
onset o f metamorphosis in many anguillid species
including A. rostrata collected in North America and
A. anguilla in Europe. The mean age at recmitment
determined for the glass eels in Iceland were similar
between the two species (336.6±41.7 and 319.3±
36.0 days for A. anguilla and A. rostrata, respective-
ly), as were their total lengths (range 58.0-78.5 mm
and 58.5-73.0 mm). In addition, mean age at
metamoi"phosis (278.0±36.8 and 254.0±47.7 days)
and total age (372.3±50.8 and 352.9±42.6 days) were
also simílar between the two species. However, these
ages o f A. rostrata in Iceland were older than those in
North America, and those o f A. anguilla collected in
Iceland were roughly intermediate between the rest o f
Europe and North Africa. These fmdings support the
hypothesis that the timing o f metamoiphosis is a key
factor for determining the place o f recmitment o f
glass eels and maintaining the geographic separation
between the two species.
Keywords Freshwater eel • Recmitment •
Metamorphosis • Otolith microstmcture • Otolith
microchemistry- Iceland
'£) Springer
mailto:mari@ori.u-tokyo.ac.jp
310 Environ Biol Fish (2008) 83:309-325
Introduction
In the Atlantic Ocean there are two species o f
freshwater eels, the European eel, A nguilla anguilla,
and the American eel, A. rostrata. They have separate
freshwater habitats, along the west coast o f the
Eurasian continent for the former and the east coast
o f the North Am erican continent for the latter
(Schmidt 1909; Boétius 1985). Both species have
been thought to occur in Iceland, which is the only
area o f sympatry (Boétius 1980; Williams et al. 1984;
Avise et al. 1990). Iceland is the westem limit o f the
geographic distribution o f A. anguilla , and the eastem
limit for A. rostrata. Recently it has been suggested
that there is a possibility o f hybridization between
these two species (Avise et al. 1990; Avise 2003;
Albert et al. 2006).
Iceland is located close to the arctic region in the
North Atlantic Ocean, between 63°N and 67°N
(Fig. 1), and is separated from Greenland to the west
by Davis Strait and northern Europe to the east by the
Norwegian Sea and Denmark Strait. There is a large
amount o f geothenual activity on the island because it is
a relatively recently fonned landmass along the northem
end o f the mid-Atlantic ridge where new ocean floor is
being created by tectonic activity. Mean sea surface
temperatures at Reykjavík along southwest Iceland can
vary from about I-2°C in January and Febmary to 11 °C
in July and August (Hanna et al. 2006), which is
28°W 24°W 20°W 16°W 12°W
site where glass eels were collected and the general pattems of
ocean currents near Iceland, which was adapted from Hanna et
al. (2006)
considerably colder than in most other parts o f the
ranges where these two species recmit. Sea surface
temperatures rnay be slightly warmer further offshore
o f Iceland in winter (Hanna et al. 2006), but the water
temperature in coastal areas and freshwater are thought
to be critical factors determining the upstream migra-
tion o f glass eels or elvers in temperate anguillid
species (Linton et al. 2007).
Both A. anguilla and A. rostrata spawn in an
overlapping area o f the Sargasso Sea (Schmidt 1922;
Schoth and Tesch 1982; M cCleave and Kleckner
1987), but it is not well understood how these two
species maintain their specific ranges that are sepa-
rated by the Atlantic Ocean. Schmidt (1925) sug-
gested that their separate ranges were the consequence
o f differences in the larval durations and growth rates
o f the two species. However, Boétius and Harding
(1985) suggested that there was no clear difference in
growth rates during the leptocephalus stage o f both
species after a reexamination o f the specimens
collected by Schmidt (1925). Recent otolith studies
supported Schmidt’s hypothesis, by showing that A.
anguilla started metamorphosing about 50-150 days
later than A. rostrata (Wang and Tzeng 2000; Arai et
al. 2000).
Other differences between the two species are
evident in the sizes that their leptocephali can reach
before metamorphosis and in the sizes o f their glass eels
at recmitment. Data on the maximum total length o f
leptocephali o f the two species indicates that there have
been no A. rostrata leptocephali collected larger than
70 mm (Boétius and Harding 1985; Kleckner and
McCleave 1985), but that A. anguilla leptocephali can
reach sizes up to 85 mm, with peak abundances at
about 70-75 mm (Tesch 1980; Boétius and Harding
1985; Bast and Strehlow 1990). Similarly the glass eels
o f the two species have different size ranges. The
length o f A. rostrata glass eels may range from less
than 50 mm in the southem part o f their range to up to
65 mm in the north (Haro and Krueger 1988; Wang
and Tzeng 2000; Sullivan et al. 2006). Glass eels o f A.
anguilla range from about 55-80 mm, with some
seasonal variation in length (Boétius and Boétius 1989;
Desaunay and Guerault 1997; Wang and Tzeng 2000).
Based on these observations o f their larval sizes
and ages, the difference in duration o f the period o f
passive transport by currents during the leptocephalus
stage could be an important mechanism for the
separation o f the ranges o f the two species. If this is
ö Springer
Environ Biol Fish (2008) 83:309-325 311
the case, both eel species migrating from the Sargasso
Sea to lceland using the same current systems should
have the same timing o f metamorphosis and similar
ages at recruitment. Furthermore, the ages o f Icelan-
dic A. rostrata should be older than those o f the
population in North America, while those o f Icelandic
A. anguilla should be similar or a little younger than
those o f the main population in Europe due to the
distance from the Sargasso Sea. However, there has
been no information on the age o f glass eels that
recruited to Iceland.
In the present study, we report the timing o f the
catches o f anguillid glass eels at the River Vogslækur
in Iceland in relation to water temperature and their
pigmentation stages, and focus on analyses o f their
otolith microstructure and microchemistry to deter-
mine their early life history characteristics. We also
compare the results obtained for the two species in
Iceland with previous information from the main
populations o f each species in Europe and North
America, to evaluate i f the ages o f Icelandic glass eels
differ from those in the main part o f their ranges. Our
objective was to understand the possible mechanisms
that maintain the separation between the two Atlantic
species ranges by examining the glass eels that recruit
to Iceland and to provide some insight on the
evolutionary process o f speciation o f A, anguilla and
A. rostrata.
Materials and methods
Glass eels were collected in 1 to 3 h sampling periods
during nighttime at the base o f a small waterfall
(1.5 m high, 5 m wide) near the mouth o f the River
Vogslækur in southwest Iceland (Fig. I) on 28 June
1999, and during 2-5 sampling days at each quarter
o f the moon from 7 May to 31 July 2000. The
sampling in 1999 was carried out with a 50 cm wide
scoop net, and a 20 cm diameter dip net that was used
to actively catch swimming glass eels at high tide.
The same scoop nets and dip nets were used in 2000,
plus an electric shocker was used at low tide. Water
temperature was measured with a temperature record-
er (MDS-T, Alec Electronics Co., Ltd.) at 20 min
intervals from 11 May to 29 July 2000. Glass eels
were initially placed in 70% ethanol immediately after
sampling, and then later preserved in 96% ethanol.
All glass eels were measured to the nearest millimeter
in total length (TL), and the pigmentatíon stages were
classified based on the stages defined by Bertin
(1956). Because the glass eels were measured after
preservation, the TL data are slight underestimates
due the effect o f shrinkage during preservation. The
total number o f vertebrae (TV) o f 20 glass eels
collected on 27 June 2000 was counted using radio-
graphs (soft-X, Softex C o„ Ltd.).
From the collected glass eel samples, 100 glass eels
(A. anguilla, « = 94; A. rostrata, n = 6) were examined
in 1999, and 231 were examined in 2000 (A. anguilla,
«=217; A. rostrata, «= 14) (Table 1). Genetic identi-
íication o f these glass eels was cam ed out in the
laboratory by comparing their mitochondrial D N A
16S ribosome R N A (mtDNA 16S rRNA) sequences
with those o f morphologically well-identified adults.
Total genomic D N A was extracted according to a
standard protocol (Aoyama et al. 1999). A portion o f
the m tDNA 16S rRNA gene (about 500 base pairs)
Table 1 Number of glass
eels collected at Vogslækur
in Iceland in 1999 and
2 0 0 0 , and the nuniber of
glass eels examined in the
analyses of otolith mícro-
stmcture and microchemis-
try (number in parentheses)
Sampling date Collection Otolith analyses
A. unguilla A. rostrata Total A. anguilla A. rostrata Total
28 June 1999 94 6 100 1 0 (1) 3 (2) 13 (3)
7 May 2000 2 0 2 2 (0) 0 (0) 2 (0 )
5 May 2000 2 0 2 2 (0) 0 (0) 2 (0 )
9 May 2000 2 0 2 2 (0 ) 0 (0 ) 2 (0 )
18 May 2000 26 4 30 4(1) 4(2) 8 (3)
25 May 2000 39 3 42 6 (2 ) 3 (3) 9(5)
27 June 2000 18 2 20 5(5) 2 (2 ) 7(7)
30 May 2000 96 4 100 10 (1 ) 3 (1) 13 (2)
9 July 2000 32 1 33 8 (0 ) 0 (0 ) 8 (0)
Total 311 20 331 49 (10) 15 (10) 64 (20)
'ZA Springer
312 Environ Biol Fish (2008) 83:309-325
was amplifíed by polymerase chain reaction (PCR)
using 2 oligonucleotide primers, L2510 and H3058.
Amplification parameters were 30 cycles o f denatur-
ation at 94°C for 30 s, annealing at 58°C for 30 s and
extension at 72°C for 60 s. Although we tentatively
regarded the specimens examined in this study as A.
anguilla or A. rostrata based on their rntDNA gene
sequences, the existence o f natural hybrids has been
reported in lceland recently by Albert et al. (2006).
That study found that only A. anguilla and hybrids o f
the two species appeared to be present in Iceland,
which as discussed later, also may have been the case
in the present study.
A total o f 49 A. anguilla and 15 A. rostrata were
analyzed for their otolith microstmcmre (Table 1).
Sagittal otoliths were extracted from each individual
and embedded in epoxy resin (Epofix, Strues) and
mounted on glass slides. These samples were then
ground to expose the core and polished with 6 and
1 pm diamond paste on a polishing wheel. Subse-
quently, they were etched with 0.05 M HCl and
vacuum coated with Pt-Pd in an ion-sputter for
observation with a scanning electron microscope
(SEM, Hitachi S-4500). SEM photographs were taken
o f the whole otolith using a magnification o f 130x or
150x and the otolith microstmcmre was photogi'aphed
at l,500x magnification. These photographs were then
used for counting growth increments along the longest
axis o f the otolith. The width o f every 10 successive
increments (average incremental width) was measured.
Four otolith age parameters were used in the smdy:
total age (At), age at recruitment (Ar), age at
metamorphosis (Am), and hatching date (HD). A t
was defined as the total number o f increments outside
the hatch check (0 days) to the edge o f the otolith. Ar
was defined as the number o f increments from the
hatch check to the freshwater rnark, which was the
first heavy check formed near the otolith edge that is
thought to indicate when glass eels reach Iower
salinities in the estuary (Kawakami et al. 1999).
Various studies have found that there is daily
increment fonnation in both the early leptocephalus
and inshore glass eel or elver stages (i.e. Tsukamoto
1989; Umezawa and Tsukamoto 1991; Martin 1995;
Shinoda et al. 2004), so as discussed later in more
detail, increment formation was assumed to be daily
until at least the freshwater mark. Am was the number
o f increments from the hatch check to the onset o f
metamorphosis. Otolith characteristics were used to
estimate the timing o f metamorphosis, because vari-
ous studies on Anguilla and Conger larvae have
indicated that during metamorphosis from the lepto-
cephalus to the glass eel stage, there is a rapid
increase in increment widths and a rapid drop in Sr:
Ca ratios (Otake et al. 1994, 1997; Tzeng and Tsai
1994; Cheng and Tzeng 1996; Arai et al. 1997, 2000;
Correia et al. 2003, 2004; Wang and Tzeng 2000;
Mami et al. 2001; Kuroki et al. 2005). HD was the
possible hatching date o f each individual that was
back-calculated using the At and the sampling date.
To help locate the timing o f metamorphosis in the
otolith microstructure, 10 otoliths o f each o f two
species were examined using life-history transects o f
Sr and Ca concentrations along a line down on the
longest axis frorn the otolith core to the edge using
wave-length dispersive X-ray electron microprobe
(JXA-8900R, JEOL). Strontianite (SrTi03) and Cal-
cite (C aC 0 3) were used as standards. The accelerating
voltage and beam current were 15 k V and 12 nA,
respectively. The electron beam was focused on a
point o f 1 um diameter, with measurements at 1 pm
interval (each counting time was 4 s). Two dimen-
sional X-ray intensity maps o f Sr were made o f the
otoliths o f five specimens o f both species. The beant
current was 50 nA, counting time was 0.4 s, pixel size
was 4 x 4 pm, and the electron beam was focused on a
point o f 1 pm.
Statistical differences between the two species and
2 years in TL, At, An Am, and HD were analyzed using
the M ann-W hitney’s U test. Pigmentation stages o f
glass eels between the 2 years and two species were
examined by analysis o f variance (ANOVA). Statis-
tical significance was accepted at F’<0.05.
Results
Recmitinent o f glass eels to freshwater habitat
A total o f 1,253 glass eels were collected in 1999 (n=
100) and 2000 («= 1,153) at Vogslækur in Iceland. In
1999, all glass eels examined were caught on one date
(28 June). In 2000, the glass eels were sampled during
about 3 months from M ay to July (Fig. 2). The first
catch o f glass eels occurred on 7 M ay («=2), and the
second and third catches were on 5 June («=2) and 9
June («=2). These first small catches were made
using the dip net. Other glass eels were caught by the
£) Springer
Environ Biol Fish (2008) 83:309-325 313
*oo>
o<D
iíi
£
o 1Qo_
0_Q
E3
z
3 Scoop net
□ 1999 (n= 100)
■ 2000 (n= 952)
, 1
b Electric shocker
■ 2000 (n= 195)
i
. C Dip net „ „
..I.............M......................... ‘
May June July
20 ^ <D
15-1
CÐ
c —<
O
• o • o • o •
Fig. 2 The number of anguillid glass eels collected using a a
50 cm wide scoop net, b an electronic shocker and c a 20 cm
diameter dip net at Vogslækur in Iceland on 28 June 1999, and
from 7 May to 31 July 2000. Changes in water temperature at
the Vogslækur site in 2000 (open circles) where glass eels were
collected is aiso shown in the boítom panel
CDJO
E
=3
A. anguilla
□ 1999 (n = 94)
■ 2000 (n = 217)
A. rostrata
□ 1999 (n = 6)
■ 2000 (n= 14)
6 -
2 -
0 - ni i i i i i r ■ I I J i i" r ”i r r
54 56 58 60 62 64 66 68 70 72 74 76 78 80
Total length (mm)
Fig. 3 Total length (TL) of glass eels of Anguúla anguilla (top)
and A. rostrata (bottom) collected at Vogslækur in Iceland in
1999 and 2000
scoop net or with the electric shocker from 17 June to 9
July (n= 1 ,M 7), when water temperatures ranged from
11.5 to 16.2°C (Fig. 2 ). The largest catches occurred
on 30 June and 1 July 2000 on the day o f new moon
when water temperatures were 14.8 and 15.6°C. 66%
o f the total for 2000 (n= 759) were caught during these
2 days, suggesting that there was a simultaneous
movement o f glass eels into the area below the
waterfall, possibly corresponding to a lunar cycle.
Morphology
The mean TL ± SD o f A. anguilla (n= 311) examined in
1999 and 2000 were 67.9±3.9 mm (range 58.0-
78.5 mm, «=94) and 68.5±3.1 mm (67.5-77.0 rnm,
n=217), respectively, and those o f A. rostratci (n= 20),
66.0±4.4 (58.5-73.0 mm, n = 6) and 67.5±3.1 mm
(63.0-72.0 mm, «=14), respectively. There was no
significant difference in TL between the 2 years or
between the two species (p> 0.05). The minimum sizes
o f both species were about the same (58 mm), but the
maximum sizes o f A. anguilla (78 mm) and A. rostrata
(73 mm) differed slightly (Fig. 3).
The pigmentation stages o f glass eels ranged from
the V IAJ to V IB stage in A. anguilla and from the
V Ia iíí to V IB stage in A. rostrata (Table 2 ) . M ost o f
the A. anguilla (98%, n = 305) and A. rostrata (95%,
«= 19) had a well developed pigmentation and were
classifíed at the latter two stages o f V IA|V or V IB.
There was no signifícant difference in pigmentation
stages between years for both species and between
two species. The T V counts o f A. anguilla glass eels
ranged from 110 to 118 (n=18), while the T V o f A.
rostrata were 109 and 110 (n=2), showing over-
lapping ranges (Fig. 4 ) .
Table 2 Pigmentation stage (sample sizes of specimens
examined (n) and total length (TL) of glass eels coilected at
Vogslækur in Iceland 1999 and 2000
Pigmentation stage A. anguilia A. rostruta
n TL (mm) n TL (mm)
VIai 1 70.5 0 -
v iaii 3 59.5-71.5 0 -
VIAII, 2 67.5-72.0 1 69.5
VIAlv 192 58.0-78.5 13 58.5-73.0
VIB 113 60.5-75.0 6 65.7-72.0
Total 311 58.0-78.5 20 58.5-73.0
*£) Springer
3 1 4 Environ Biol Fish (2008) 83:309-325
Total number of vertebrae
Total number of vertebrae and myomeres
Fig. 4 Total number of vertebrae a counted using radiographs
of glass eeis of Anguilla anguilla and A. rostrata collected at
Vogslækur in Iceland on 27 June 2000, and b the total number
of vertebrae (black circles/solid lines) and myomeres in
leptocephali (open circles/dashed lines) of A. angui/la and A.
rostrata frorn multipie locations in North America and Europe,
and the North Atlantic, respectively (adapted from Boetius and
Harding 1985)
A. anguilla A. rostrata
Fig. 5 Scanning electron microscope photographs of the
otolith microstmcture of glass eels of Anguil/a anguilla (left
panels) and A. rostrata (right panels) collected at Vogslækur in
Iceland. 1 hatch check, 2 first feeding check, 3 íreshwater mark
ö Springer
Otolith microstructure
All otoliths of both species analyzed had a core near
the center of the sagittal plane, which was deeply
etched, and a hatch check with a mean diameter of
about 9.85±2.07 p.m for A. anguilla and 9.36±
1.85 ptm for A. rostrata (Fig. 5). The number of
specimens with a freshwater mark was all 10 speci-
mens (100%) in 1999 and 33 of 39 specimens (85%)
examined in 2000 for A. anguilla, while for A.
2
1 .5
1
0 .5
0
_ 2
E
§ 1-5
3
®
o
c
(c 0 .5
o
o
0
2
1.5
1
0 .5
0
0 5 0 100 1 50 2 0 0 2 5 0
Age (days)
Fig. 6 Profiles of otolith increment widths along a transect
from the hatch check (0 days) to the otolith edge of a Anguilla
anguilla and b A. rostrata glass eels collected at Vogslækur in
Iceland in 1999 and 2000, and c other species from previous
studies (Arai et al. 1997, 1999, 2000, 200J). Each data point
represents a 10 increment average
c
A. anguíila
- a - A. rostrata
A. japonica
- ♦ - A. b ico lo r pacifica
- s - A. australis
Environ Biol Fish (2008) 83:309-325 315
Fig. 7 X-ray intensity maps of strontium contents in the ►
otoliths of Anguilla anguilla (left panels A-E , total length of
glass eels were 70.2, 67.6, 69.7, 64.1, 68.3 mm: these
specimens are identical to the five specimens in the left panels
A-E ofFig. 8a, respectively) andX. rostrata (right panels F-J,
65.0. 65.0, 72.0, 70.2, 65.7 mm: these specimens are identical
to the five specimens in the left panels A-E of Fig. 8b,
respectively). The scale bars are 100 um, and the Sr
concentration scale varies from 0 .2 % (blue) to 1 .2 % (red)
rostrata , all three specimens (100%) and 10 o f 12
specimens (83%) in 1999 and 2000 respectively, had
the mark. There were some specimens with one to six
light checks between first feeding check and fresh-
water mark.
A. a n g u illa showed a small peak in otolith
increment width (mean±SD 0.74±0.15 p.m, range
0.43—1.00 |um) at 20-70 days afler hatching (Fig. 6),
and A. rostrata had a peak (0.78±0.14 p.m, 0.59-
1.07 pm) at 20-60 days. Outside this small peak, the
increment width was alrnost constant to the edge o f
the otolith for most specimens o f both A. anguiUa
(range 0.27-0.93 pm) and A. ro s tra ta (0 .2 7-
0.72 pm). We detected no shaip increase in otolith
increment widths or rapid growth zone that was a
characteristic incremental change corresponding to
the onset o f metamorphosis as has been reported in
many anguillid species including A. anguilla collected
in Europe and A. ro s tra ta in North Am erica
(Lecomte-Finiger 1992; Arai et al. 1997, 1999,
2000, 2001; Wang and Tzeng 2000; Marui et al.
2001) (Fig. 6).
Otolith microchemistry and timing o f metamorphosis
The Sr concentration X-ray intensity maps o f the
otoliths o f both A. anguilla and A. rostrata showed a
variety o f pattems o f fluctuations (Fig. 7). The central
regions o f both species had relatively low values,
followed by altemating bands o f high (red and
yellow) and low (green and blue) Sr concentrations.
The outermost region o f all the otoliths o f both
species had blue regions, suggesting exposure to
freshwater or brackish salinity levels. There was no
consistent pattem o f banding o f the high Sr regions
within the otoliths o f either o f the two species.
This type o f variation in Sr also could be seen in
the Sr:Ca ratio pattems along the life-history transects
from the core to edge o f the otolitbs. The line
transects o f the individuals in the left columns o f
Fig. 8a,b correspond to the same individuals in the Sr
concentration X-ray intensity maps in Fig. 7 for both
A. anguilla and A. rostrata, respectively, and gener-
±3 Springer
316 Environ Biol Fish (2008) 83:309-325
Fig. 8 a Plots of otolith increment widths averaged for every ►
ten increments (bold lines') and Sr:Ca ratios measured at 1 |im
intervals (narrow Hnes) in Anguilla anguilla glass eels collected
at Vogslækur in lceland in 1999 and 2000. Each arrow shows
the estimated point of the sharpest drop of SnCa ratios
suggesting the start of metamorphosis. The five specimens /1-
E in the left panels correspond to the specimens A-E in the left
panels of Fig. 7, respectively, b Plots of otolith increment
widths averaged for every ten increments (bold lines) and Sr:Ca
ratios measured at 1 pm intervals (narrow lines) in Anguiila
rostrata glass eels collected at Vogslækur in lceland in 1999
and 2000. Each arrow shows the estimated point of the sharpest
drop of Sr:Ca ratios suggesting the start of metamorphosis. The
fíve specimens A-E in the left panels correspond to the
specimens F-J in the right panels of Fig. 7, respectively
ally similar fluctuations were observed in both
methods o f analysis. The values of Sr:Ca ratios
around the otolith core were 9.57-14.44 for A.
anguilla (Fig. 8a) and 8.23-19.06 for A. rostrata
(Fig. 8b). Sr:Ca ratios in most specimens increased
from the center of the otolith, often showing a peak in
the central region before decreasing until the edge of
the otoliths. Most specimens showed a slightly larger
drop in Sr:Ca values with no further major increases,
or a slight increase in increment widths, the timing of
which corresponded in some specimens. These two
types of changes were used to estimate the possible
timing of metamorphosis or the age at metamorphosis
(Table 3).
Based on these two types o f changes in Sr:Ca ratios
and increment widths, Am was estimated to be about
220-340 days after hatching (mean±SD 287.0±
36.8 days) forÆ angiúlla and 160-330 days (254.0±
47.7 days) for A. rostrata. There was no signifícant
difference in Am between the two species. However, it
was difficult in some specimens to defíne the exact
timing of metamorphosis because distinguishing a last
drop in Sr:Ca ratio was unclear when there was no
clear correspondence to increase in incremental width.
Age at recruitment, total age, and hatching date
The mean /fr±SD, based on the position of the
freshwater mark, of A. anguilla was 332.5±53.0 days
(range 260-416 days, n=10) in 1999, and 337.5±
38.5 days (262-411 days, «=33) in 2000, and for A.
rostrata it was 335.7± 10.7 days (344—365 days, «=3)
in 1999, and 308.4±33.7 days (248-359 days, «=10)
in 2000 (Fig. 9). There was no significant difference
in Ar between the two species in each year and
between the 2 years.
B
30 3
20 2
10
0 0
20 2 -
10 1
0 0
20 2
10 1
0 0
20 2)
10 1
0 0
20 2
10 1
0 0
H
/S ,
30
20
10
0
20
10
0
20
10
0
20
10
0
0 100 200 300 400 0 100 200 300 400
Age (days)
|-20
10
0
'Ö Springer
Sr:Ca
x
1000
S
r:C
ax1000
Table 3 Mean age at metamorphosis (Tm), age at recruitment (Ar), total age (A,) and estimated hatching dates (HD) of glass eels of Anguilla anguiUa and A. rostrata recruited to
various locations
Speeies Sampling location Sampling date n Am (days) n A, (days) n A, (days) HD References
A. anguilla Vogslækur, Iceland 28 June 1999
7 May- 8 July 2000
10 278.0±36.8 43 336.3 ±41.7 49 372,3±50.8 April-September This study
Oued Sebou, Morocco December-January 1989 76 178,0 76 2 1 1 .0 76 216.0 Lecomte-Finiger (1992)
Cape Finisterre, Spaina November 1987 13 186.0 13 191.0 Leeomte-Finiger (1992)
Loire, France January-April 1989 128 185.0 128 245.0 128 245.0 Lecomte-Finiger (1992)
Vilaine, France November-December 1989
January-May 1990
90 180.0 90 237.0 90 242.0 Lecomte-Finiger (1992)
Severn, UK December-Januaiy 1988 30 196.0 30 272.0 30 276.0 Lecomte-Finiger (1992)
Ijmuiden. The Nctherlands March, May 1990 30 176.0 30 245.0 30 250.0 Lecomte-Finiger (1992)
Viskan River, Sweden 13 April 1995 24 346.8±36.6 24 444.6±39.1 November-July Wang and Tzeng (2000)
Sevem River, UK 1 April 1995 11 318.5±27.2 11 420.0±38.3 (peaking in Wang and Tzeng (2000)
Vilaine River, France 5 April 1995 13 350.9±37.6 13 455.4±43.9 January) Wang atid Tzeng (2000)
Minho Rio, Portugal September 1995 8 397.1 ±27.0 8 467.7±26.7 Wang and Tzeng (2000)
Minho River, Portugal 15 May 1996 23 198.0±27.4 23 249.0±22.6 August-October Arai et al. (2000)
A. rostrata Vogslækur, Iceland 28 June 1999
7 May-8 July 2000
10 254.0±47.7 13 319.3±36.0 15 352.9±42.6 May-August Tliis study
Haiti 17 December 1995 25 209.3 ±20.2 25 241.6 ± 18.5 March-October Wang and Tzeng (2000)
Florida, USA 28 February 1995
22 Januaiy 1997
4 214.0± 14.4 4 247.8± 16.2 (peaking in
August)
Wang and Tzeng (2000)
North C-arolina, USA 22 March 1995 2 1 188.8±29.1 2 1 220.4±33.2 Wang and Tzeng (2000)
Annaquatucket River, 14 April 1995 26 189.5 ± 19.6 26 251.8 ± 16.6 Wang and Tzeng (2000)
Rhode Island, USA
Musquash River, New 28 April 1995 17 192.7 ±20.3 17 272.3 ± 15.7 Wang and Tzeng (2000)
Brunswick, Canada
East River, Nova Scotia, 29 May 1995 32 211,4±20.8 32 283.5 ± 18.2 Wang and Tzeng (2000)
Canada
Maine, USA 20 April 1997 15 156.0± 18.9 15 206.0±22.3 August-October Arai et al. (2000)
Pivers Island, North December-April 1985-1994 77 167.2±16.9 Powles and Warlen (2002)
Carolina, USA
Black Creek, Noith 2-23 February 1994 25 175.4± 12.6 Powles and Warlen (2002)
Carolina, USA
Little Egg Inlet, New Februaty-March 1994 22 2 0 1 .2 ± 16.1 Powles and Warlen (2002)
Jersey, USA
Lepreau, New 6 June 1994 43 209.3± 18.1 Powles and Warlen (2002)
Brunswick, USA
■§ aOnly leptocephali (stage IV) were collected from this localion
Environ
Biol Fish
(2008)
83:309-325
317
318 Environ Bioi Fish (2008) 83:309-325
Fig. 9 Age at recruitment
(Ar) (left p anels) and total
age (/!,) (right pcm els) of
glass eels o fA n g n illa
anguilla (top) and A. ros-
trata (hottom ) collected at
Vogslækur in Iceland in
1999 and 2000 inferred from
their otolith microstructure
16-
1 2 -
A. anguilla
□ 1999 (n= 10)
■ 2000 (n = 33)
A. rostrata
□ 1999 (n = 3)
■ 2 0 0 0 (n= 1 0 )
0
200 300 400
Ar (days)
A. anguilla
□ 1999 (n= 10)
■ 2000 (n = 39)
A. rostrata
□ 1999 (n = 3)
■ 2000 ( n = 12)
200 300 400
(days)
500
The mean /it±SD of A. anguilla was 372.0±
53.6 days (range 300-455 days, n=10) in 1999, and
was 372.3±50.8 days (278-463 days, n=39) in 2000,
while that of A. rostrata was 387.0±19.5 days (368-
407 days, n - 3) in 1999, and 344.4±43.0 days (258-
407 days, «=12) in 2000 (Fig. 9). There was no
significant difference in A t between the two species
within each year and between tlie 2 years.
The back-calculated HD for A. anguilla collected
in 1999 ranged from 1 April to 3 September 1998,
and those for specimens collected in 2000, from 2
April to 2 September 1999 (Fig. 10). HD tor A.
rostrata collected in 1999 ranged from 19 May to 9
June 1998, and those in 2000, from 6 May to 26
August 1999. There was no significant difference in
back-calculated HD between the two species in each
year and between the 2 years.
Discussion
Identification problems
We identifíed the glass eels in Iceland based on their
rntDNA gene sequences in this study and they
corresponded to either A. anguilla or A. rostrata.
Recently though, Albert et al. (2006) reported the
possible presence of eels in Iceland that were pure A.
anguilla, and sorne that were natural anguillid eel
hybrids. However, they found no pure A. rostrata
among the specimens that were collected in Iceland
and evaluated using amplifíed fragment length poly-
morphism (AFLP) analysis. They detected 88.4%
2 0 -
15-
_Q
A. anguilla
□ 1998(n=10)
■ 1999 (n = 39)
A. rostrata
□ 1998 (n = 3)
■ 1999(n= 12)
J F M A M J J A | S O | N D
HD
Fig. 10 Estimated hatching dates (H D ) of glass eels of
A ngu illa anguilla (top) and A. rostra ta (h o tto m ) collected at
Vogslækur in Iceland inferred from the total age (A,) estimated
using their otolith microstracture. The hatching dates in the
calendar months of 1998 and 1999 are shown for glass eeis
collected 1999 and 2000, respectively
Æ) Springer
Environ Biol Fish (2008) 83:309-325 319
pure A. anguilla glass eels and 11.6% hybrids of A.
anguilla and A. rostrata at the Vogslækur site in
Iceland during 2000-2003 where we also sampled
glass eels in 1999 and 2000. In the present study,
based on the mtDNA identification of Icelandic eels,
we estimated that the glass eels that were collected
consisted o f about 94% A. anguilla and 6% A.
rostrata. However, the AFLP analyses suggest that
the mtDNA sequences of the A. rostrata identified in
the present smdy might be actually those of hybrids of
a matemal A. rostrata and a patemal A. anguilla,
since no pure A. rostrata were found by Albert et al.
(2006) at this locality or elsewhere in Iceland. If
based on their findings at the Vogslækur site, it is also
possible that about 6% of the A. anguilla glass eels
that we examined in the study could be matemal A.
anguilla hybrids. These considerations might be
partly supported by the distribution of number of
TV for the two species (Fig. 4), which included sorne
intennediate TV values of possible hybrids, although
the number of specimens examined was small. The
ranges of total number of vertebrae of the two species
appear mostly to be separated at 111 vertebrae, with
A. rostrata being as low as 101 and A. anguilla as
high as 120 (Boetius and Harding 1985). Therefore,
the majority of the glass eels examined in the present
study (range 109-118) and in previous research in
Iceland (108-118, Avise et al. 1990) were within the
range of TV of A. anguilla , with only a few having
numbers of vertebrae in the upper range o f A. rostrata
(Fig. 4). However, for convenience in the present
study, we discuss the life history characteristics of the
lcelandic eels using the species names “rt. anguilla"
and "A. rostrata” as they were identified by mtDNA.
Timing of capture of glass eels
The first capture of substantial numbers of glass eels in
mid-June and even larger catches in late June and early
July when the water temperature in the sampling area
had warmed up to about 12-16°C supports the findings
of a laboratory study on glass eels from this site that
showed water temperature was an important factor
controlling the activity and upstream migration in these
two species in Iceland (Linton et al. 2007). The
laboratory study found that swimming activity in-
creased markedly at 12°C and that climbing behavior
was first seen at 14°C. Low Sr:Ca ratio at the
peripheral part of their otoliths suggesting freshwater
exposure time, and the advanced pigmentation stages
of most glass eels, suggests that these glass eels had
been waiting somewhere near the sampling site or
mouth of the river in a fresh or brackish water
environment until water temperatures became warmer.
Most of the glass eels examined were at the latter
two pigmentation stages, supporting the hypothesis
that there were very few recently arrived glass eels at
this site, compared to their continental species ranges
where the earlier stages have been observed (Haro
and Krueger 1988; Boetius and Boetius 1989). Jessop
(2003) found that A. rostrata elvers began actively
swimming upstream when temperatures reached 10—
12°C in the northem region of Nova Scotia, and
upstream migration began when temperatures reached
10°C further to the south in Rhode Island (Haro and
Kxueger 1988). Very low catches of A. anguilla elvers
and juveniles also occur below water temperatures of
10-11°C (White and Knights 1997). The apparent
correspondence of the biggest catch during the new
moon suggest that in addition to increasing water
temperature, the lunar cycle or tidal factors may have
also triggered an increase in the upstream migratory
behavior of the glass eels at this site.
Implications of otolith microstructure
and microchemistry
Both A. anguilla and A. rostrata that recruited to
Iceland showed a unique pattem of increment widths
without any clear rapid growth zone where the widths
increased during metamorphosis from a leptocephalus
to a glass eel. This is a remarkable contrast with all
other anguillid glass eels that have been examined
(Fig. 6), including tropical eels such as A. celebesen-
sis, A. b icolor bicolor, A. b icolor pacifica , and A.
m arm orata (Arai et al. 2001; Mami et al. 2001;
Kuroki et al. 2005), as well as the temperate eels A.
anguilla, A. rostrata, A. ja p o n ica , A. australis and A.
d ie jfenbach ii (Lecomte-Finiger 1992; Cheng and
Tzeng 1996; Arai et al. 1997, 1999, 2000; Wang
and Tzeng 2000; Mami et al. 2001). The rapid growth
zone is considered to be an indication o f an
ontogenetic change in otolith growth associated with
the physiological changes that occur during metamor-
phosis, and the lack of this zone in Icelandic glass
eels suggests that they experienced extraordinaiy
environmental conditions compared to other anguillid
species.
£) Springer
320 Environ Biol Fish (2008) 83:309-325
The raost probable factor to prevent the formation
o f a rapid growth zone in Icelandic eels would be the
low water temperature near Iceland where they likely
metamorphose. Water temperature is well known to
influcnce otolith growth in físhes (Campana and
Neilson 1985; Umezawa and Tsukamoto 1991), and
it has been reported that leptocephali probably
metamorphose to glass eels relatively near their
freshwater habitats (Kleckner and McCleave 1985;
Tsukamoto 1990; Tsukamoto and Umezawa 1994). ln
glass eels that recruit to Iceland, it is possible that the
process o f metamorphosis is greatly prolonged at
lower temperatures, and since the late stage leptoce-
phali and glass eels likely experienced long periods of
lower temperature compared to other species, this
may have affected their otolith deposition pattems.
Although the coastal waters around Iceland are
influenced by wann water from the Gulf Stream
(Schmitz and McCartney 1993), the water tempera-
ture decreases as it moves northward, and the sea
surface temperature just to the south of Iceland in
May has been observed to be 7-8°C (Krauss 1995),
or 1-5°C just to the north o f Iceland in Febmary and
March (Swift and Aagaard 1981). Water temperatures
along the southwest coast o f Iceland and the offshore
areas nearby, appear to rarely get above 11-13°C in
July and August when temperatures are highest
(Hanna et al. 2006). These temperatures are as much
10-15°C lower than those in the coastal waters o f the
main habitats of these two species in Europe and
North America. Therefore, it is probable that the
individuals recmiting to Iceland metamorphosed
under unusually low temperature conditions that
may have caused substantial physiological stress, or
a slowing of the metamorphic process that could have
caused the lack of the fonnation of a rapid growth
zone in their otoliths.
Unlike the unique pattems of increment widths in
Icelandic eels, the change in Sr:Ca ratios showed
pattems in the line transects in both species (Fig. 8a,b)
that were roughly similar to those observed in the
other anguillid eels. The decrease in Sr:Ca ratios at
the likely time of metamorphosis suggested that the
onset o f metamorphosis was not accompanied by a
rapid increase in otolith increment width like that
observed in other anguillid glass eels. The Sr
concentration X-ray intensity maps of the otoliths
reflected the pattems in the line transects and showed
variability that could be related to the differences in
water temperature experienced by the leptocephali
(Fig. 7), if Sr incorporation into the otoliths of these
glass eels is rnainly affected by temperature as it
appears to be in some species (Campana 1999).
Based on studies of yellow and silver eels that
have moved between fieshwater and saltwater envi-
ronnrents (e.g. Tsukamoto et al. 1998; Tsukamoto and
Arai 2001), the blue in the outer parts of the otoliths
of all the X-ray intensity maps and the presence of a
freshwater check in most of the specimens examined
here, suggested that the glass eels in the present study
had arrived at the rnouth of the River Vogslækur
considerably earlier than their time of capture. Yellow
eels that shift habitats appear to show freshwater
residency in Sr concentration X-ray intensity maps
with a consistent blue color (Tsukamoto and Arai
2001), so the glass eels examined here appear to show
evidence of freshwater or brackish water exposure.
The freshwater check has been reported as a mark that
indicated the timing o f entry of glass eels into
freshwater or estuarine habitat (Kawakami et al.
1999), although it has not been well validated yet.
Most of the Icelandic eels (80-100%) had a freshwa-
ter mark at the peripheral part of the otolith. Other
temperate eels such as the Japanese eel (100%,
Kawakami et al. 1999) and the two New Zealand
eels (100%, Mami et al. 2001) were also found to
typically have a freshwater nrark. This rnark was also
observed in some specimens of tropical eels (7-100%,
Mami et al. 2001; 28%, Kuroki et al. 2005), but in
much lower percentages. Differences in the percent-
age of glass eels with a freshwater mark between the
two species in Iceland and other tropical anguillid eels
suggests that the stress of check formation might not
be always caused by a salinity change, but also may
be related to other factors such as a lower temperature
at the estuary.
Estimated hatching date
The present study shows that the two species
recmiting to Iceland had back-calculated HD during
almost the same seasons in spring and summer (A.
anguilla: April to September, A. rostrata: May to
August). Collection data in the Sargasso Sea has
shown that small leptocephali (<10 mm) o f A.
anguilla were present from March to July, while
those o f A. rostrata from February to April (Boetius
and Harding 1985; McCleave and Kleckner 1987;
'£) Springer
Environ Biol Fish (2008) 83:309-325 321
Kleckner and McCleave 1988). The range of the
approximate spawning seasons estimated by these
two methods match fairly well for A. anguilla, but the
spawning season o f A. rostrata estimated from
collection data in the Sargasso Sea is considerably
earlier than the back-calculated HD from the otolith
data of the glass eels mitochonrially identified as A.
rostrata. However, if the A. rostrata identified in this
study were hybrids as discussed above, it is possible
that their spawning season would be more similar to
A. anguilla. It is also possible that the slight mismatch
with the estimated spawning season of A. anguilla in
the Sargasso Sea could be due in part to limited or
biased seasonal and spatial coverage of sampling
suiweys for leptocephali in the spawning area, or that
only eel laiwae bom during the later part of the
spawning season (April to September) could recmit
successfully to Iceland.
However, in the case of Atlantic glass eels that are
likely more adapted to low temperature than most
anguillid eels, there is the possibility that there may
be a period of time after metamorphosis when the
otolith increments are difficult to distinguish or when
there is no deposition of discemable daily rings and
instead, heavy checks are formed. This might explain
some of the partial mismatches between the estimated
back-calculated HD in previous otolith studies and the
peak spawning season based on larval sampling that
has been discussed by McCleave et al. (1998). Cieri
and McCleave (2000) proposed that there may be no
otolith deposition during metamorphosis in the At-
lantic eels, but no heavy check was observed near the
otolith increments corresponding to metamorphosis in
the Icelandic glass eels examined here. In addition,
recent studies on other elopomorph fishes have shown
that otolith daily deposition continues through meta-
morphosis in leptocephali held in the laboratory as
they transformed into the glass eel or juvenile stage
(Chen and Tzeng 2006; Powles et al. 2006). This
suggests that if there is a possible period of lack of
otolith deposition in the otoliths of some Atlantic
glass eels, it is probably not during metamorphosis,
but is more likely when the glass eels have reached
their recmitment areas and stay on the bottom
without feeding or actively migrating inshore. It is
possible that the freshwater mark shows this time
when recruited glass eels stop swimming and wait in
the substrate for the appropriate cues for upstream
migration into ffeshwater. However, in the glass eels
examined in the present study, this possible period
o f donnancy appears to have been short, because
their estimated HD are close to the known spawning
period o f A. anguilla in the Sargasso Sea. Because
daily increment formation also has been observed in
both the early leptocephalus and inshore glass eel or
elver stages (i.e. Tsukamoto 1989; Umezawa and
Tsukamoto 1991; Martin 1995; Shinoda et al. 2004),
and generally occurs in fishes, it appears that
regardless of the inconsistent HD based on At in
some Atlantic glass eel otolith studies, the estimates
o f Ar based on the freshwater mark in anguillid glass
eels may be a reasonable measure of the durations of
their migrations.
Age at recruitment
Using the Ar data in the present study, the exact
duration of larval migration from the spawning area to
the recruitment area including the oceanic glass eel
stage after metamorphosis, could be estimated, since
no heavy checks from the hatch check to freshwater
mark were observed. However, the At estimates
include the freshwater mark, some other heavy checks
further outside and increments extending to the outer
edge of the otolith, which could cause underestima-
tions of age. This makes it difficult to accurately
compare the duration o f larval migration, because
some studies only show At or Ar. The Am in previous
studies vary greatly though (Table 3), and these
values can be used to estimate the relative difference
in approximate durations of larval migrations of glass
eels collected at various sites and times of year.
The Ar determined for the glass eels from Iceland
(Fig. 9) were similar between the two species, as were
their TL (Fig. 3). In addition, Am and At were also
similar between the two species. However, these
characteristics showed differences with those of glass
eels from their main populations (Table 3). The mean
Ar o f glass eels of A. anguilla collected in Iceland
fforn May to July were about 64—125 days older than
glass eels at six sites in southem Europe sampled
fi'om November to May (Lecomte-Finiger 1992; Arai
et al. 2000), but contrarily, the At in Iceland were
about 48-95 days younger than those collected fforn
four sites from southem to northem Europe in
September or April (Wang and Tzeng 2000, Table 3).
Age estimates o f A. anguilla based on various
techniques including otolith microstructure have
•ö Springer
322 Environ Biol Fish (2008) 83:309-325
varied widely (see Lecomte-Finiger 1992; McCleave
et al. 1998; Arai et al. 2000; Wang and Tzeng 2000),
and especially the A, estimates of A. anguilla glass
eels remain controversial. In A. anguilla, difficulty in
interpretation of growth increments in the opaque
region near the otolith edge with unclear increments
and frequent occurrence of checks might cause an
inconsistency in counting results. In contrast, the ages
of A. rostrata were consistent when compared
between the ages of glass eels ffom lceland and their
main population in North America, with the mean Ar
of the glass eeis of A. rostrata collected in iceland
being as rnuch as about 110-152 days older (Arai et
al. 2000; Powles and Warlen 2002), and At also being
as much about 69—133 days older (Wang and Tzeng
2000) (Table 3).
The distance ífom the Sargasso Sea to Iceland is
obviously farther than to North America (about
3,000 km ffom Newfoundland or Labrador in Canada
to Iceland), which would account for the greater ages
of A. rostrata in Iceland, but the distance to Iceland is
not so different from the distance to some parts of
Europe. The variable results for the A r and At of A.
anguilla in different studies might be due in part to
the different sampling locations or times of year of
each study. The distance from the Sargasso Sea to
Iceland is longer than to some parts of Europe, while
perhaps shorter and more direct than to other locations
in Europe. Various processes may affect the larval
growth and transport of the European eel as they cross
the Atlantic basin however, since seasonal changes in
the lengths of glass eels have been observed as they
recruit to southem Europe (Desaunay and Guerault
1997). Seasonal or interannual differences of current
speeds or pathways flowing towards Iceland in the
North Atlantic Current or towards Europe (Krauss
1995), or differences in larval behavior also may
influence the speeds of migration of A. anguilla
across the Atlantic Ocean.
Separation mechanism
Although the estimated period for lai-val migration of
about 1 year was much shorter than Schmidt’s
estimation for A. anguilla o f 2-3 years, the results
obtained here support the hypothesis proposed by
Schmidt that the larval duration is a key factor for
determining the place of recruitment of glass eels and
maintaining the geographic separation between the
two species (Schmidt 1922, 1925). Buoyancy would
be lost during metamorphosis because of a decrease in
the body surface area (fi'om 8.0 cm2 in leptocephali to
2.3 cm2 in glass eels) and water content (from 93% to
less than 80%) with a corresponding increase in body
density (Tsukamoto and Umezawa 1994). This would
induce the detrainment of glass eels frorn a current
and may cause the initiation o f active migration
toward estuaries. The lack of any glass eels with the
body sizes or larval durations similar to A. rostrata in
Iceland may suggest that only leptocephali with
European eel genes (A. anguilla or hybrids) for
timing of metamorphosis can reach Iceland.
“Timing of Metamorphosis” or the equivalent
“Lai-val duration” of Schmidt is determined by growth
rate and the maximum body size of leptocephali
(Kuroki et al. 2006), and each species has its own
geographic range, so it appears that these parameters
relating to the timing of metamorphosis may be
geneticaily well defíned. A recent study suggests that
different species of anguillid leptocephali may have
slightly different growth rates (Kuroki et al. 2006), so
if A. rostrata has a faster growth rate as suggested by
Wang and Tzeng (2000), their leptocephali would be
able to metamorphose into glass eels earlier than A.
anguilla, and would detrain from the Gulf Stream to
recruit to North America, while the leptocephali of A.
anguilla would continue to be transported further by
the Gulf Stream and the North Atlantic Drift and
eventually reach Europe or North Africa. A. rostrata
also appears to have smaller maximum leptocephalus
and glass eel sizes than A. anguilla indicating earlier
metamoi-phosis at a younger age. Since some of the
glass eels of A. rostrata collected in Iceland were
larger than the maximum reported leptocephalus size
of 70 mm (Boétius and Harding 1985; Kleckner and
McCleave 1985) and the size of most o f their glass
eels (Haro and Krueger 1988), it appears likely that
these glass eels were actually hybrids as suggested by
Albert et al. (2006) using AFLP genetic analyses.
Although the sample sizes were small, these A.
rostrata, or possible hybrids, had intemiediate sizes
and ages compared to the two species. In contrast, the
size of the A. anguilla glass eels in Iceland and their
ages were overlapping with samples from the Euro-
pean continent (Boétius and Boétius 1989; Desaunay
and Guerault, 1997, Wang and Tzeng 2000).
The “Timing of Metamorphosis Hypothesis” can
also account for the speciation of the two Atlantic
<£) Springer
Environ Biol Fish (2008) 83:309-325 323
species. Molecular phylogenetic research has sug-
gested that the ancestral species of Atlantic eels
moved fforn the Indian Ocean into the North Atlantic
Ocean through the ancient Tethys Sea rnore than
30 Ma (Aoyama et al. 2001). A possible scenario for
the speciation of the two Atlantic eels would be that
the longitudinal range of the habitat of the ancestral
Atlantic species would have become wider and wider
along the coast of the North Atlantic Ocean, due to
continental drift and the sea floor spreading of the
Atlantic Ocean (Aoyama et al. 2001). When the ocean
expanded further, two distinct groups with different
pattems of larval growth and timing of metamorpho-
sis may have developed. Then the two groups had
gradual shifts of spawning seasons and areas due to
the differences in the migration distance of adults that
may have also contributed to reproductive isolation
fforn each other. Eventually the constraints imposed
by the need for two different patterns of tirning of
metamorphosis resulted in speciation into two spe-
cies. Because of this interesting possible history, the
Icelandic eels that appear to include hybrids living
sympatrically with A. anguilla on a small landmass
isolated from the two main habitats are a good model
for studying the separation mechanism of the two
Atlantic species.
Acknowledgements We are grateful to Elizabeth D. Linton
and Gudmundur Ingi Gudbrandsson for valuable help during
the course of field work in Iceland. The work was supported
by a special grant from the Icelandic Govemment to study
recruitment mechanisms of Icelandic glass eels. This study
was also partially supported by a Grant-in-aid for Scientific
Research (Nos. 10460081, 11691177) from the Ministry of
Education, Culture, Sports, Science and Technology of Japan,
by the “Research for the Future” Program grant No. JSPS-
RFTF 97L00901 from the Japan Society for the Promotion of
Science, by the Research Foundation from Touwa Shouhin
Shinkoukai, and by the Eel Research Foundation from
Nobori-kai.
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ö Springer
Icelandic eels
Bjami Jónsson' & David L. G. Noakes2
'lnstitute o f Freshwater Fisheries at Holar. Holar Hjaltadalur, 551 Saudarkrokur, Iceland
2Department of Zoology, University of Gueiph, Guelph, Ontario, NIG 2WI Canada
Introduction
The geography and geology of Iceland, among with its extreme northem location, make it among the
most unique places Atlantic eels recmit to. Iceland is a small and isolated island in the middle o f the
Atlantic Ocean with its climate and oceanic currents strongly influenced by the Gulf Stream. Iceland is
the only habitat where European eel (.Anguilla cmguillá) and American eel (.Anguilla rostratá) co-occur
(Boetius 1980) and possibly a hybrid between the species (Avise et. al 1990). Due to the isolation and
young age o f the isiand the number of species o f various oiganisms is low. Only six species o f
freshwater físh are found in Iceland, Atlantic salmon (Saimo salar), arctic charr (Salvelinus alpinus),
brown trout (salmo truttá), threespined stickleback (Gasterosteus aculeatus), and the two species o f
Atlantic eels.
Iceland is on top of the North Atiantic ridge and with its ongoing volcanic activities, is moving to east
and west. In the younger areas the bedrock is very permeable to water with the bedrock dissolving
relatively easily in the water. Rivers and lakes in this zone are thus mostly spring fed, characterised by
stable flow as well as stability in temperature and physical characteristics. This water is also rich in
minerals and these systems are generally stable and productive.
The second class o f rivers represents direct runoff rivers that are usually much more unstable in flow,
temperature and productivity than spring fed systems. Direct runoff rivers vary depending on iocation;
in relatively young bedrock formations both drainage pattem and productivity is influenced by the
bedrock being easily eroded in water, whereas in older areas the basaltic bedrock is harder and
dissolves less in water. Direct runoff rivers in these areas are usually unstable in nature and have
relatively low productivity. Direct mnoff rivers that mn through vegetated heathland areas can,
however, be more stable and productive. These rivers also typically have numerous lakes and ponds in
the tributaries (Amthorsson 1979; Gudjonsson 1990). Finally, there are very unstable and cold glacial
rivers, and on the other extreme, rivers and lakes affected by geothermal activities.
The diversity of lakes and rivers and habitats for the few species occupying them is profound. The
ecological relationships are evident in the variability found among freshwater fishes in Iceland. Various
alternative adaptations have emerged and are in the making through dynamic interaction between
diverse watersheds and the few species inhabiting them (Skúlason, Snorrason & Jónsson 1999; Jónsson
6 Skúlason 2000).
Atlantic eels are most common in Southem and Southwest Iceland and have been thought to be rare in
Northwest and Southeast Iceland and absent from Northeast and Eastem Iceland (Saemundsson 1926;
Gudbergsson & Antonsson 1996). Eels have been found to occupy diíferent river types, often above
waterfalls impassable for other fish, variety of fireshwater lakes and ponds, and brackish lakes and
estuaries. Unique habitats for eeis in Iceland include rivers and lakes influenced by geothermal
activities, lava substrate and lava caves (Saemundsson 1926; Gudbergsson & Antonsson 1996).
The histoiy of human settlement is short in Iceiand, only 1000 years, thus human impact on natural
resources has been neglected with only recent traditional fishing for Atlantic eels. Commercial fishing
for eels is minimal and absent for glass eels.
First verified catch of glass eeis occurred in 1999 (this study), but glass eels had been noticed and few
times caught by local people without scientific inspection. Time of recruitment was also only based on
speculation (Jónsson Unpublished). Starting in 1999, a study has been ongoing investigating the
distribution and ecology of Atlantic eels and the recruitment mechanisms o f glass eels entering
Icelandic waters.
Methods
Glass eel recruitment has been monitored in one location, Vogslaekur, SW Iceland for two years from
7 May to 2 August in 2000 and 20 April to 7 August in the year 2001. Sampling has been carried out
on new moon, the first quarter moon, fúll moon and the last quarter moon, and half moon in the estuary
area o f the stream. Sampling was carried out with hand held nets for visuai sampling on high tide and
scooping nets in 2000, and hand held nets and electrofishing on low tide in 2001. Data on water
temperature, ocean temperature and light intensity has been collected throughout the sampling season.
Glass eel sampling has been undertaken by the same sampling techniques in a number of other
locations in Southem and Westem part o f Iceland during the expected peak of the recruitment season in
June and July.
For study on distribution and habitat selection, yellow eeis have been collected from locations spread
over the Icelandic coast from 1999-2001. Sampling was carried out with funnel traps and electrofíshing.
Parallel to the sampling, written and orai references have been gathered about the absence/presence o f
eels, especially in geographical areas where few reports have existed on the presence of eels or they
have been thought to be absent.
Results
Glass eel recruitment
In the year 2000,2 glass eels were collected on the first sampling date in May, but the catch remained
low until middle of June, reached its peak on new moon in the end of June and beginning of July and
was over mid Juiy. Largest catch in one day was 534 glass eels on 30 June, and combined in the season
in Vogslaekur, 1133. In the spring 2001, sampling was launched on new moon 20* o f April with 10
specimens caught. Glass eels were collected at every sampiing date until mid July, after which only
pigmented elvers were observed. Sampling effort was ceased on 7 August. Glass eel recruitment
appeared more spread over the season than in the previous year, partly due to improved sampling
techniques. The peak season appeared to be from middie o f June through first week of July. The
greatest catch was obtained on 28 June, 228 glass eeis, and total o f 1081 glass eels during the season by
the river mouth. Glass eels caught on new moon tended to be glossy, with glass eels collected on the
next sampling dates being more pigmented. Glass eel catch in other iocations exposed to less effort,
ranged from one specimen to 134.
In both years 2000 and 2001 the peak recruitment occurred during the season o f 24h daylight. Amongst
with moon phase, glass eel recruitment into ffeshwater appeared to be closely related to threshold water
temperatures, being most pronounced at the highest water temperatures observed. The connection
between glass eel recruitment and their activity level and upstream migration was further verified by
lab experiments employing difFerent temperatures (Linton & Jónsson in prep.).
During this study (1999-2001), glass eels have been caught in 11 different locations in Iceland. From
interviews with local people and written sources, glass eel recruitment is reported ffom the years 1920-
2001 in 14 additional locations spread over the coast o f Iceland except Eastem Iceland (Fig. 1).
v
rK, “ /5
r
AS»
í___
0 'A f '
’ /
— 4
■50 2
1. Homafjðrdur 14. Álftanes
2. Hali 15. Seljar
3. Eldvatn 16. Vogslaekur
4. Álftaver 17. Laugargerdi
5. Dyrhólaós 18. Stadarsveit
6. Holtsós 19. Saurar
7. Stokkseyri 20. Langavatn
8. Olvusá 21. Bár
9. Vifílsstadalaekur 22. Ogur
10. Ellidaár 23. Stykkishólmur
11. Varmá 14. Eyhildarholtsvatn
12. Borgarlaekur 25. Eyjafjardará
13. Leirulaekur
Fig. 1 Reported glass eel sites in Iceland 1920-2001 iight symbols, and successful
sampling sites for glass eels in the years 1999-2001 dark symbols.
Yellaw eels
Ðuring the course o f the study, eels have been caught in a variety of habitats, streams ( 1 0 ), lakes ( 1 0 )
ponds (1), geothermal waters (3), brackish water in lakes and esturarines (1), and in marine habitats (5).
Of the 30 collection sites for yellow eels, 12 are located outside the geographical range previously
sampled for scientific studies or known to have eels.
From current sample collections and review of the literature and iocal references, it is apparent that eels
occupy a diversity of habitats in all geographicai areas along the Icelandic coast. This includes areas
previously not held to foster eels, such as Eastern Iceland and coastal marine habitats around the island,
see Saemundsson 1926; Gudbergsson & Antonsson 1996.
Discussion
Iceland being on 65 N° near the Arctic Circie makes for a unique setting for glass eel recruitment. The
water temperature is usually very low and much lower than usualiy encountered by the two eel species
elsewhere. Thus, water temperature appears to be a criticai factor influencing glass eel recruitment to
Iceland amongst with moon phase. Recruitment to coastal waters takes place in waves around new
moon in Aprii, May, and June/July, while high water temperatures trigger their upstream migration. In
a lab experiment the highest activity of glass eels was found to be at 12-17°C while threshold
temperature for upstream migration over an artifíciai waterfail was 12-14.5°C (Linton and Jónsson in
prep.). Another striking difference between Iceland and other locations glass eels recruit to, is the
constant daylight during the peak recruitment, while glass eels most commonly recruit elsewhere
during dark nights (Tesch 1977).
In a mtDNA study by Momoko Kawai (2001), looking at species composition of glass eels caught in
1999 and 2000, A. anguilla was the more abundant being about 94% both years, with A. rostraia
representing 6 % of the catch. No signifícant differences were found in time o f recruitment or size of
the two species. The age at recruitment, A. anguilla 365 +/- 44.3 d, and A. rostrata 349+/- 44.3 d, was
also found to be the same for the two species (Kawai et. al poster this conference).
From the above it can be concluded that the recruitment mechanisms of Atlantic eels to Iceland are in
many ways unique for the two species, and that concurrent recruitment and similar recruitment age
provide a challenge to traditional ideas about the life histories and possibly, evolution o f the species.
In this study we confirm that Atlantic eels are spread over all geographical areas in Iceland, but not
mostly confinedto Westem, Southem and South East Iceland (Saemundsson 1926; Gudbergsson &
Antonsson 1996). The diversity of habitats utilised by Atlantic eels is also reinstated, including marine
waters in Southem, Westem, Northem and Eastem Iceland. In a study by Aoyama et. al (in prep.) on
species composition of Icelandic eels, A. anguilla represent 94% and A. rostrata 6% o f eels caught in
Westem and Southem Iceland, the same as found for the glass eels.
Studies on the species status of Icelandic eels have oniy been based on samples o f yeliow eels from
Westem, Southem and South Eastem Iceland (See Boetius 1980, and Avise et. al 1990). These studies
have not taken into account different habitats, life stages (glass eels, yellow eels and silver eels) or
geographical locations. Widespread study on eels in all life stages ffom the different geographical
regions, and information on habitats are needed to unravel the mystery of the ecology and species
status of the Icelandic eels, that might be the so much wanted “black box” to the evolution o f the
Atlantic eels.
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Proceedings of the International Symposium
ADVANCES IN EEL BIOLOGY
Research for the Future Program
Japan Society of the Promotion of Science
Organizing Committee
Katsumi Aida
Katsumi Tsukamoto
Kohei Yamauchi
Yayoi Auditorium
The University of Tokyo
28 - 30 September 2001
M o lec u la r E co logy (2006) 15 ,1 9 0 3 -1 9 1 6 doi: 10.1111 / j.l 365-294X.2006.02917.X
Natural hybrids in Atlantic eels (Anguilla anguilla,
A. rostrata): evidence for successful reproduction and
fluctuating abundance in space and time
VICKY A L B E R T /B JA R N I JÓ N SSO N tand LOUIS BERNATCHEZ*
*Québec-Océan, Département de Biologie, Université Laval, Québec, Canada GIK 7P4, ilnstitute of Freshioater Fisheries, Northem
Division, Sauðárkrókur, Iceland, IS 550
The outcome of natural hybridization is h ighly variable and depends on the nonexclu-
sive effects of both pre- and post-mating reproductive barriers. The objective of this study
was to address three specific questions regarding the dynamics of hybridization between
the American and European eels (Anguilla rostrata and Anguilhi angnilla). U sing 373 AFLP
loci, 1127 ee ls were genotyped, representing different life stages from both continents,
as w ell as multiple Icelandic locations. We first evaluated the extent of hybridization and
tested for the occurrence of hybrids beyond the first generation. Second, w e tested w hether
hybrids were random ly distributed across continents and arnong Icelandic sam pling
sites. Third, we tested for a difference in the proportion of hybrids between glass eel and
yellow eel stages in Iceland. Our results provided evidence for (i) an overall hybrid propor-
tion of 15.5% in Iceland, with values ranging from 6.7% to 100% depending on Iife stages
and locations; (ii) the existence of hybrids beyond the first generation; (iii) a nonrandom geo-
graphic distribution of hybrids in the North Atlantic; and (iv) a higher proportion of first
and later generation hybrids in yellow eels compared to glass eels, as w ell as a significant
latitudinal gradient in the proportion of hybrids in Icelandic freshwater. We propose that
the combined effect of both differential survival of hybrids and variation in hybridization
rate through time best explain these patterns. We discuss the possibility that climate
change, which is impacting many environmental features in the North Atlantic, may have
a determinant effect on the outcome of natural hybridization in Atlantic eels.
Keyioords: AFLP, Anguilla, climate changes, fitness, hybrid zone, hybridization
Received 5 July 2005; revision received 28 September 2005; accepted 22 fanuary 2006
Abstract
Introduction
in recent years (Arnold 1992, 1997, 2004; Dowling & Secor
1997; Barton 2001; Mallet 2005).
lt is increasingly accepted that aside from the development
of stable hybrid zones (Barton & Hewitt 1985), interbreeding
between distinct species or populations can result in a
variety of evolutionary outcomes, including reinforcement
(sensu Dobzhansky 1937), genetic extinction (Rhymer &
Simberloff 1996; Huxel 1999), speciation (Templeton 1981),
enhanced genetic diversity (Rieseberg et al. 1999), and
novel genetic combinations (Anderson & Stebbins 1954;
Lewontin & Birch 1966; Arnold 2004; Seehausen 2004).
Moreover, the viewpoint that natural hybridization may
play a significant role in animal evolution has been revived
The resulting outcome of natural hybridization is highly
variable and depends on the nonexclusive premating and
postmating reproductive barriers (Aldridge 2005). Post-
mating isolation has been discussed in the recent debate on
hybrids' fitness relative to the parental forms in the wild
and the evolutionary potential of natural hybridization
(Arnold 1997). Hybrid íitness may vary greatly and is
inversely proportional to the strength of the barriers.
This variability is explained in part by the heterogeneity
in space and time of endogenous as well as exogenous
postmating selection pressures (e.g. Grant & Grant 1996),
which in tum determine the fate of hybrids relative to the
parental forms with which they coexist in a particular
environment. Superior hybrid fitness may be due to
C o rre sp o n d en c e : V icky A lb e rt, Fax: 418 656-7176;
E -m ail: v icky .a lbert@ bio .u lava l.ca
© 2006 B lackw ell P u b lish in g L td
mailto:vicky.albert@bio.ulaval.ca
1904 V. ALBERT, B. J Ó N S S O N and L. B E R N A T C H E Z
heterosis via lreterozygote advantage, silencing of deleterious
recessive alleles or epistatic interactions, while reduced
hybrid fitness may be caused by the disruption of co-adapted
gene complexes. Although heterosis may prevail in tlre
first hybrid generation, liybrid fitness may vary between
hybrid classes (Arnoid & Hodges 1995) as outbreeding
depression accompanied by reduced fitness may occur in
subsequent generations (e.g. Edmands 1999; Gharrett et al.
1999). While variation in the relative fitness of hybrids lias
been obsert'ed (Arnold & Hodges 1995; Burke & Arnold
2001) and theoretically predicted (Barton 2001), hybrid
superiority relative to at least one of tlre parental forms is
increasingly being documented (reviewed in Arnold 1997;
Arnold et al. 1999).
In controlling the number of hybrids produced, premat-
ing reproductive barriers may as well play an important
role in determining the genotypic composition and fate of
a hybrid zone (Aldridge 2005). These barriers may be of
different sources such as spatial, seasonal or behavioural
isolation. For instance, the level of reproductive isolation
might result from spatial and/or temporal overlap during
reproduction periods (e.g. Emelianov et al. 2001; Bailey
et al. 2004). Environmental factors might as well influence
tlie level of hybridization by reducing the relative reproduc-
tive success for one gender in one of the parental form (e.g.
Williams et al. 2001). Disturbance dynamics which often
break down the isolating barriers might as well afíect the
level of gene flow in a specific habitat (e.g. Bleeker &
Hurka 2001). Being affected by local ecological condi-
tions, it is the strength and potentially the interaction of
isolating barriers that will determine the extent of hybridiza-
tion between two parental forms. It is therefore necessary
to consider potential factors related to both pre- and post-
mating barriers that will restrict contacts between the two
hybridizing species or lineages in order to fully understand
the role of natural hybridization in evolution (Bailey et al.
2004).
In this study, we document the dynamics of introgressive
hybridization between the American and European eels
(Anguilla rostrata and Anguilla anguilla). The life cycle of the
two species begins in the Sargasso Sea (North Atlantic
Ocean, 19.5-30°N, 48-79°W) where the larvae, called
leptocephali, appear at the surface. Leptocephali then
passively and perhaps actively follow the Gulf Stream and
the North Atlantic drift to reach their respective continent:
North America for the American eels and Europe for the
European eels. This journey is longer for European com-
pared to American eels and may last from 7 months to up
to 3 years depending on authors (reviewed in Arai et al.
2000). Once larvae have reached a minimal threshold size,
they undergo metamorphosis into glass eel (Otake 2003).
The glass eel actively swims towards shore and gradually
develops pigmentation. This life stage may Iast from 20 days
to more than 160 days, depending on water temperature
and to a lesser extent on salinity conditions (Briand et al.
2005; Linton et al. in press). Once glass eels have lost their
transparency, they are called elvers and later on yellow
eels. Yellow eels are able to adapt and exploit almost all
aquatic habitats, from coastal environments to headwaters.
Feunteun et al. (2003) identified four different movement
behaviours of eels during their yellow eel stage: founders,
pioneers, lrome-range dwellers and nomads. All those
behaviours represent different life strategies towards
reaching a minimal threshold size before migrating back to
the spawning grounds. After 3 to 20 years spent in their
feeding grounds as yellow eels (Aoyama & Miller 2003),
at the onset of maturation, they metamorphose into silver
eels and begin their migration to the Sargasso Sea, where
they reproduce and die.
Spawning grounds of both species overlap in space
and time (McCleave et al. 1987), thus setting the stage for
interbreeding. Although their biological species status
is not debated anymore, Atlantic eels differ only slightly in
morphology (Avise 2003), vertebrae count being the only
quasi-diagnostic phenotypic character (Boetius 1980). In
North America and continental Europe, eels rarely present
ambiguous vertebrae counts. However, the occurrence of
eels with American-like number of vertebrae in northern
Europe, and particularly in Iceland has been pointed out
previously (Boétius 1980; Williams etal. 1984; Avise et al.
1990). Genetic analyses indicated that these eels were most
likely of hybrid ancestry (Avise et al. 1990), although the
markers used did not allow clarification of their hybrid
status (e.g. first or later generation hybrids). This was
due to the nondiagnostic nature of the allozyme loci used
(Mdh-2), and the maternal inheritance of mitochondrial
DNA (Avise et al. 1990). In a recent study that aimed to
clarify the status of ambiguous Icelandic individuals using
microsatellite markers, Mank & Avise (2003) concluded that
'available microsatellite data are inadequate to critically
test [the] hypothesis... that some Icelandic eels are of hybrid
ancestry'. Sample size and geographic coverage of Icelandic
locations were also both very limited in previous studies,
allowing the nature of the dynamics of hybridization betweeir
Atlantic eel species to remain inconclusive.
In this study, we revisit this question with the amplified
fragment length polymorphism (AFLP) characterization
of over 1 10 0 eels representing different life stages from
both continents, as well as multiple Icelandic locations.
The AFLP technique can relatively easily reveal polymor-
phisms at hundreds of loci, and represents a very efficient
technique for hybrid identification between closely related
species (Congiu et al. 2001; Young et al. 2001; Bensch et al.
2002; Lucchini 2003; Bensch & Akesson 2005). Hybrid
individuals were thus identified and classified in order
to document the extent of hybridization, and to test for the
occurrence of hybrids beyond the first generation. Second,
we tested the null hypothesis of no differences in the
© 2006 B lackw ell P u b lish in g L td , M olecular Ecology, 15 ,1903-1916
N A T U R A L H Y B R I D I Z A T I O N IN A T L A N T I C EELS 1905
proportion of hybrid eels between the glass and yellow eel
stages in Iceland. Finally, we documented the distribution
of hybrids across both continents and within Iceland in
order to test the null hypothesis of the random geographic
distribution of hybrids.
M aterials and m ethods
Samples
A total of 1127 eels were analysed. Icelandic samples (n =
748) were collected from 10 sites between 2000 and 2003,
covering most of the known geographic distributional range
in Iceland (Fig. 1, Table 1). From a previous study, genomic
DNA of eels was available for eight sampling locations
(m = 379); four from North America, three frorn continental
Europe, and one from North Africa (Fig. 1, Table 1; see
details in Wirth & Bernatchez 2001, 2003). These were
considered baseline populations and used to identify the
most informative AFLP loci, which were used for assessing
the hybrid status of each individual eel.
Fig . 1 G eo g ra p h ic d is tr ib u tio n o f eel s a m p lin g sites in Iceland (top
p an e l) , N o r th A m erica a n d E u ro p e (b o tto m pan el). S ta r sy m b o ls
re fe r to lo c a tio n s w h e re b o th g la s s e e ls a n d y e llo w e e ls w e re
c o lle c te d . lc e la n d ic s a m p le s a re Ö x n a læ k u r (Ö X ); S to k k s e y ri
(ST); G ra fa rv o g u r (GR); V ífilss ta d av a tn (VI); Seljar (SE); V o g slæ k u r
(VO); B ár (BA); R ey k h ó la r (RE); V a tn sd a lu r (VA); S a u ö á rk ró k u r
(SA). N o r th A m erican e e l loca tions: M ed o m a k R iver (ME); B oston
IT arbor (BO); W ye R iv er (W Y); S t-Johns R iver (SJ). E u ro p e a n eel
loca tions: E lbe R iv e r (EL); G ra n d L ieu L ake (GL); M in h o R iver
(M I); M o u lo u y a o u e d (M O).
© 2006 B lackw ell P u b lish in g L td , M olecular Ecology, 1 5 ,1903-1916
North American and continental European samples
consisted of either all glass eels (BO, GL, MI, MO), or all
yellow eels (ME, WY, SJ, EL). Yellow eels represent a mixture
of different cohorts, and should therefore represent the
average genetic composition at a given location over many
years. T emporal genetic variation between cohorts has been
reported (Dannewitz et al. 2005); however, it is very weak
relative to interspecific differences (Wirth & Bematchez
2003), and should therefore be inconsequential in assessing
hybrid status. In Iceland, yellow eels were sampled at all
1 0 locations, whereas glass eels of several cohorts were
available at four of these sites (ST, VI, SE, VO), which
allowed the comparison of hybrid occurrence at two dif-
ferent life stages. Life stages, sampling years and sample
sizes are detailed in Table 1.
AFLP genotyping
Fin clip and muscle tissue samples were digested and total
genomic DNA extracted and purified using MultiScreen
lysate clearing plate and MultiScreen% BAC plate from
Montage BAC96 Miniprep Kit (Millipore). The AFLP pro-
cedure of Vos et nl. (1995) was íollowed in order to produce
a DNA fingerprint for each of five selective primer com-
binations (EcoRI-AAC/Msel-CTA; EcoRI-AAC/Msel-CTT;
EcoRI-AGG/ Msel-CTT; EcoRI-ACT/MscI-CTC; EcoRI-ACT/
MscI-CTT with the EcoRI primer bearing the fluorescent
dye). Each sample and primer combination was electro-
phoresed on a Base Station DNA Fragment Analyzer (MJ
Research), with an internal lane GeneScan®-500 [ROXJ™
size standard (Applied Biosystems). Tracking and peak
identification was completed using c a r t o g r a p h e r DNA
Fragment Analysis software (version 1.2.6). DNA finger-
prints were smoothed and peaks with intensity over the
threshold value were scored. Unambiguous loci were then
identified and selected (N = 373) on the basis of reproduci-
bility of fragment size (in base pairs), proximity to other
loci, and signal intensity. The software a p l p - s u r v version
1.0 (Vekemans 2002) was used to calculate the number and
proportion of polymorphic loci, as well as the expected
heterozygosity (HE) assuming Hardy-Weinberg equilibrium
within each sampling site and grouping (North America,
Europe, Iceland). As the occurrence of hybríds may cause
deviations from Hardy-Weinberg equilibrium assumption,
expected heterozygosity should be interpreted cautiously.
Difference in proportion of polymorphic loci between
groups was tested by performing a nonparametric a n o v a
(Kruskal-Wallis method) in s a s (release 8.02; SAS Institute).
Individual hybrid status
The power of selected loci to discriminate hybrid status
was assessed using the population assignment simulator
in a f l p o p (version 1 .1 ; Duchesne & Bernatchez 2002). Based
1906 V. ALBERT, B. J Ó N S S O N and L. B E R N A T C H E Z
Table 1 Life stage, sampling year, a n d s am p le s ize (n) fo r each s am p iin g s ite sep a ra te ly . P ro p o rtio n o f p o ly m o rp h ic locí, expected
h e te ro z y g o s ity (H E), a n d a b so lu te n u m b e r o f p u re A m erican (A m ), F,, FN, a n d p u re E u ro p ea n (Eu) for th e A m e rican , E u ro p ea n , a n d
Ice land ic sam p le s as vvell as fo r e ach s a m p lin g s ite sep a ra te ly . G rep re se n ts g la ss eels a n d Y, y e llo w eels. D ash s ig n s (—) in d ic a te no
o b se rv a tio n s in th e status categ o ry . P o p u la tio n ab b re v ia tio n s a re d e fin e d in Fig. 1 legend
P o p u la tio n
Lífe
s tag e Y ear n
P o ly m o rp h ic
loci (%) h e A m F, Fn Eu
A m erican
ME Y 99 45 54.7 0.193 43 — 2 -
BO G 99 50 52.5 0.193 49 — 1 —
WY Y 99 48 52.5 0.192 48 — — —
SJ Y 99 50 49.1 0.187 50 — - —
T otal 193 60.3 0.192 190 — 3 —
E u ro p ean
EL Y 99 49 52.8 0.193 — — — 49
GL G 99 49 48.5 0.185 — — — 49
M I G 99 45 54.4 0.189 — — — 45
M O G 99 43 61.7 0,195 — — — 43
T otal 186 61.1 0.191 — — — 186
Ice land ic
SA Y 03 6 71.6 0.244 — 6 — —
VA Y 00 18 71.6 0.248 — 4 2 12
RE Y 01 13 75.9 0.217 — 6 — 7
BA Y 03 49 71 0.210 — 6 — 43
V O G 00 50 53.6 0.196 — 9 3 38
VO G 01 50 72.7 0.210 — 4 1 45
VO G 02 49 52.3 0.191 — 1 — 48
VO G 03 49 53.1 0.196 — 3 2 44
VO Y 01 36 70 0.212 — 3 0 31
SE G 01 48 71.8 0.211 — 7 2 39
SE Y 01 46 69.4 0,209 — 14 4 28
VI G 01 50 72.1 0.215 — 4 4 42
VI Y 02 45 70.5 0.232 — 5 5 35
GR Y 03 45 71.3 0.222 — 1 2 42
ST G 01 46 68.6 0.207 — 1 2 43
ST G 03 50 53.4 0.188 — — 1 49
ST Y 03 49 69.7 0.213 — 6 2 41
Ö X Y 03 49 72.1 0.213 — 2 2 45
T o tal 748 68.1 0.214 — 82 34 632
on allelic frequencies observed in the North American
and European baseline populations, the a f l p o p simulator
randomly generated 10 0 0 genotypes of each of the six
following categories: pure American, pure European,
fírst generation hybrids (Fj), backcrosses (BCt and BC,),
and second generation hybrids (F,). Those 6000 simulated
individuals were then blindly reassigned to their most
probable category. Since the probability of erroneous assign-
ment between the BCf, BC2 and F, hybrid categories was
relatively high (see Results), we subsequently combined these
into a single category of later generation hybrids (FN). Thus,
we determined the most likely status of all available samples
according to four categories: pure American, pure European,
first generation hybrid (F,), and later generation hybrids (FN).
We then used a v e r s i o n of the s t r u c t u r e p r o g r a m
adapted to d o m i n a n t markers (v'ersion 2.2; D. Falush e t a l .,
unpublished) t o e s t i m a t e i n d i v i d u a l ' s admixture propor-
tion, in this case the proportion of an individuaTs genome
originating from either the American or the European
eel gene pool. The Marcov chain Monte Carlo (MCMC)
algorithm implemented in the program clusters individuals
into the presumed number of populations, minimizing
the Hardy-Weinberg and gametic phase disequilibrium
within populations, but also accounting for the genotypic
ambiguity inherent in dominant markers such as AFLP (in
which the presence of a band does not allow to distinguish
between heterozygote and homozygote). Both American
and European gene pools were assumed to represent
two baseline populations (k = 2 ) without considering the
prior information on the species of origin. American and
European eel samples clustered vrery distinctively into two
clusters, except for three American eels (see Results). This
confirmed that the assumption of two populations in the
admixture model could unambiguously discriminate
© 2006 B lackw ell P u b lish in g L td , M olecular Ecology, 15 ,1903-1916
N A T U R A L H Y B R I D I Z A T I O N IN A T L A N T I C EELS 1907
both species and allow the identification of individuals with
hybrid ancestry. All American, European, and Icelandic
samples were then run by s t r u c t u r e , assuming two
populations for 50 000 iterations in the burn-in and 50 000
supplementary iterations.
Based on the 90% posterior probability interval of the
admixture value, individuals were assigned to the four
possible genetic status as follows: pure if their probability
interval overlapped with 0 (pure American eel) or 1 (pure
European eel), first generation hybrid (F;) if their probability
interval overlapped with 0.5 but not with either 0 or 1 ,
and later generation hybrid if it did not overlap with either
0, 0.5 or 1 . This methodology is conservative as it is most
likely underestimating the number of later generation
hybrids in favour of first generation hybrids and pure
American or European eels. Theory predicts that, depending
on the pedigree of individuals, some of the later generation
hybrids can be characterized by a proportion of both parental
gene pools (e.g. American and European eel) which is equal
or close to that of a first generation hybrid or pure parental
forrn (e.g. Epifanio & Philipp 1997).
s t r u c t u r e results were then compared to those obtained
using the program n e w h y b r i d s (Anderson & Thompson
2002). Using Bayesian statistics and MCMC, this program
computes the posterior probability that each individual
belongs to one of the following classes: American, European,
F,, BClr BC2, and F2 category. The clustering method of this
latter program is based on an inheritance model defined
in terms of genotype frequencies and is useful when popu-
lations are known to consist of pure and recent hybrids.
Assuming Jeffrey's like priors for the mixing proportion
and the allelic frequencies, the same data set was run for
50 000 iterations in the burn-in and 50 000 supplementary
iterations.
Hybrid proportiort vs. life stages and sampling sites
We determined whether there was a difference in the pro-
portion of hybrids between the glass and yellow eel stages
by performing a static cohort analysis on eels from the
four Icelandic sites where both glass and yellow eels were
sampled (ST, VI, SE, VO). The proportion of first genera-
tion hybrids, the proportion of later generation hybrids,
and the total proportion of hybrids (combining the first and
later generation) were compared between the glass and
yellow eel stages (CATMOD procedure in s a s release 8.02;
SAS Institute). Assuming a constant rate of hybridization,
this cohort analysis is an efficient means to evaluate the
relative hybrid fitness, allowing an estimate of the viability
of hybrids in natural conditions (Bert & Arnold 1995).
However, since we could not assess differential survival
during the oceanic stages (larv'al stage prior to freshwater
and silver eel stage following yellow eel metamorphosis),
our interpretations are based on differential survival in
freshwater only. Moreover, there are currently no data
available to evaluate the temporal variation in the pro-
portion of hybrids reaching Iceland. In order to evaluate
this possibility, we compared the proportion of hybrids
between different time periods according to the life stages
and the year eels were sampled. More specifically, we
considered that yeUow eel samples collected in 2000 were
the oldest of all samples and all samples were classified
into eight different time periods. We thus considered yellow
eels collected in 20 0 0 as belonging to the time period 1 ,
yellow eels collected in 20 01 to the time period 2 , yellow
eels coUected in 2002 as eels from the time period 3, and
yellow eels collected in 2003 belonging to the time period
4. We considered the glass eel samples collected in 2000
as eels from the time period 5, glass eels collected in 2001 as
eels from the time period 6, glass eels collected in 2 0 0 2 as
eels from the time period 7, and finally glass eels collected
in 2003 as eels from the time period 8 . This allowed us
to statistically test for heterogeneity in the occurrence of
hybrids (Fv FN, and both categories combined) between
the different time periods. We used the chi-squared (y})
permutation method of Roff & Bentzen (1989) avaUable from
the executable MONTE in the r e a p program (McElroy ef al.
1992), with 1000 permutations to detennine test significance.
Finally, heterogeneity in the geographic distribution
of hybrids, both across continents and within Iceland, was
first tested using a chi-squared (%2) permutation test on the
occurrence of pure, first, and later generation hybrid eels.
The association between the proportions of hybrids (F2 and
Fn categoríes combined) among Icelandic yellow eels and
latitude was assessed by the Pearson correlation using s a s
(release 8.02; SAS Institute). The two hybrid categories
were pooled in order to reduce sampling bias due to the
low occurrence of first or later generation hybrid in several
sites after confirming the absence of significant difference
in the geographic distribution between Fj and FN hybrids
(X2 = 13.77, P = 0.12). The correlation between mean
length of eels in each site and latitude was assessed as well
(Pearson correlation in s a s ) .
Results
Individual hybrid status
A total of 373 AFLP Ioci were resolved among all continental
American and European eel samples, of which 120 had
a frequency differential of 0 .1 0 or higher between both
species. A relatively high polymorphism was observed,
whereby, 60% or more of the AFLP loci were polymorphic,
depending on sample locations (Table 1). Namely, a highly
significant difference in proportion of polymorphic loci was
observed between the three sampling groups (K = 10.14,
P = 0.0063), where Icelandic samples were characterized
by a higher proportion of polymorphic loci compared
© 2006 B lackw ell P u b lish in g L td , M olecular Eœ logy, 15 ,1903-1916
1908 V. ALBERT, B. J Ó N S S O N and L. B E R N A T C H E Z
Samples
Fig . 2 A d m ix tu r e p r o p o r t io n s o f N o r th
A m erican , E u ro p ean , a n d Icelandic sam ples.
E ach in d iv id u a l is re p re s e n te d b y a ve rtica l
b a r; the p ro p o r tio n o f b lack a n d w h ite in
each b a r re p re sen ts th e p ro p o r tio n o f the
in d iv id u a l 's g e n o m e fro rn A nguilla rostrata
(A m erican) a n d Anguilla anguilla (E u ropean )
ancestry , respec tive ly . T he d o tte d h o rizo n ta l
lin e in d ic a tes th e 0.5 a d m ix tu re level. N u ll
va lues re fer to a d m ix tu re p ro p o rtio n s sm aller
th a n 0.001, w h ile 1 refers to ad m ix tu re va lues
la rg e r th a n 0.999.
to North American and European samples, as would be
expected for admixed vs. pure gene pools.
Based on the simulation and reassignment procedures
performed with a f l p o p using the six e e l categories (pure
American, pure European, Fv F2, BC,, BC2), the assignment
success for pure American, pure European, and F, eels was
98.1%, 97.6%, and 83.2% respectively. However, misassign-
ments in F„ BC (, and BC2 were relatively high: 29.8%, 12.3%,
and 12.6%, respectively. In order to reduce misassign-
ment and also increase hybrid sample size for subsequent
statistical analyses, F, and backcrosses were pooled into a
single later generation hybrid category (FN), which resulted
in a misassignment rate of 8.1%, 7.6%, and 16.4% for the
BCj, BC„ and F2, respectively, and a misassignment of 8.9%
over all status categories.
The results of s t r u c t u r e revealed that the geographic
distribution of admixture proportion differs substantially
among continental American, European, and Iceíandic
samples (Figs 2 and 3, and Table 1). Samples from both
continents were essentially composed of eels with either
a pure American or European eel genome. Most icelandic
indivíduals were characterized by a genome of pure
European ancestry. However, 15.5% of Icelandic samples
were classified as admixed with variable degrees of their
genome from American eel ancestry. Hybrid proportion
within each yellow eel sample ranged from 6 .6 to 1 0 0 %.
No pure American eel was observed among the Icelandic
samples. Using this information to assess the genetic status
of all individual eels based on the 90% posterior probability
interval of the admixture value, the continental European
samples consisted of only pure European eels, while the
null hypothesis of pure American ancestry was rejected for
three North American individuals. These had estimates
of 7%, 20%, and 21% of their genorne from European eel
ancestry, and were identifíed as later generation hybrids
(since their 90% probability interval did not overlap either
with 0 or 0.5). In contrast, the null hypothesis of pure
European eel ancestry was rejected for 15.5% (n = 116) of
all Icelandic samples analysed. A total of 70.7% (n = 82) of
putative hybrids in Iceland fell into the first generation
E L G L M! M O S A V A R E 8 A V O S E V I G R S T Ö X M E B O W Y SJ
Europe lceland North
America
Fig . 3 Proportions of p u re A n g u ilk rostrata (closed bars), p u re Anguilla
anguilla (o p en b a rs ), f irs t g e n e ra tio n (d o tted ) , a n d Ia te r g en era tio n
h v b rid s (striped ) w ith in each sam p lin g s iles fo r co n tin en ta l E urope,
Ice land , a n d N o rth A m erica . P o p u la tio n ab b re v ia tio n s a re d e fin ed
in Fig. 1 legend .
category, whereas 29.3% (n = 34) of all hybrids were
classified as later generation hybrids, which confirmed
the occurrence of hybrids beyond the first generation,
and therefore, the viability and capacity of first generation
hybrids to reproduce.
The individual status categories obtained from the soft-
ware s t r u c t u r e were confirmed by the software n e w h y -
b r i d s , whereby 95 % of the 1127 assignments were identical.
Moreover, the proportion of each status categories detected
by s t r u c t u r e and n e w h y b r i d s in each sampling location
did not differ significantly and were highly correlated
(R2 = 0.979). Given such a high congruence between both
methods, we retained and interpreted the detailed results
O Í STRUCTURE.
Hybrid proportion vs. life stages and sampíing sites
The static cohort analysis rejected the null hypothesis of no
difference in the proportion of hybrids between glass and
© 2006 B lackw ell P u b lish in g L td , M olecular Ecology, 1 5 ,1903-1916
N A T U R A L H Y B R Í D I Z A T I O N IN A T L A N T I C EELS 1909
0.20 -
- f 0.15 -
oQ.
o 0.10
CL
0.05 -
0.00
A 0.25 - 0.12 ^ 0.35 - o = 40.09° y 2 - 36.10 O o Xz = 13.35
P< 0.001 0.10 ^ P = 0.061 0,30 - * P< 0.001
* 0.08 -
0.06 ° ♦
0.25
0.20
♦
O 0 0.15
♦ 0.04
♦
0.10
* ♦
♦ 0.02 0.05♦
0.00 0 . 0 0 - ♦
1 2 3 4 5 6 7
Time period
2 3 4 5 6
Time períod
1 2 3 4 5 6 7
Time period
Fig . 4 R e la tio n sh ip b e tw ee n th e p ro p o r tio n
o f F, (A), Fn (B), o r F, a n d FN co m b in ed (C)
w ith tim e p e rio d (d e fin ed in M ate ria ls a n d
m e th o d s section). C h i-sq u a re ('/}) a n d P
v a lu e s a re p re s e n te d . S olid d ia m o n d s re fe r
to y e llo w eel sam p le s a n d o p e n d ia m o n d s
to th e g la ss eel sam p les .
T a b le 2 P ro p o r tio n s o f p u re , first (F,), a n d la te r g e n e ra tio n h y b rid s
(FN) in th e g ia ss eei an d y e llo w eel s am p le s co llected in V o g slæ k u r
(VO), S to k k sey ri (ST), V íf ilss tad av a tn (VI), a n d Seljar (SE)
Site
Life
s tag e
P u re
E u ro p ea n
S ta tu s c a tego ry
F. f n
VI G 84.0 8.0 8.0
Y 77.8 11.1 11.1
SE G 81.3 14.6 4.2
Y 60.9 30.4 8.7
v o G 88.4 8.6 3.0
Y 86.1 8.3 5.5
ST G 95.8 1.0 3.1
Y 83.7 12.2 4.1
0.8
0.6
0.4
0.2
0 -
63.5
R 2 = 0.4865
P = 0.025
• ST
64 64.5 65
Latitude
65.5 66
Fig . 5 P e a rso n co rre la tio n (R2) b e tw e e n the p ro p o r tio n o f h y b rid s
a n d la titu d e (firs t a n d la te r g e n e ra lio n h y b rid s co m b in ed ) in
Ice land ic sam p les .
yellow eels in Iceland. In seven out of eight comparisons,
higher proportions of hybrids in yellow eel relative to
glass eel samples were observed, the exception being
the first generatíon hybrids in Vogslækur (VO) (Table 2).
The categorical model analysis revealed no significant
interaction between sampling site and life stage (P = 0.5461).
Thereíore, a main effect model, which did not consider
the interaction between sampling sites and life stages, was
run. The proportion of hybrids varied significantly among
sampling sites (P = 0.0036) and between life stages (P =
0.0155), but sampling site had no significant effect on
the difference in the proportion of hybrids observed
between glass eels and yellow eels. On the other hand, the
proportion of first generation hybrids and the proportion
of first and later generation hybrids combined varied
significantly betwæen time periods (P< 0 .0 0 1), whíle the
variation in the proportion of later generation hybrids was
near statistical significance (P = 0.061; Fig. 4). Moreover,
a temporal trend was observed whereby the proportion of
hybrids reaching ícelandic waters seemed to decrease from
2000 to 2003, based on the analysis of glass eel samples
(time period 5-8). The addition of yellow eel samples (time
period 1-4) further supported this pattem.
A x2 permutation test confírmed the nonrandom distribu-
tion of hybrids between Iceland and both continents (x2 =
59.16, P < 0.001). A second analysis based only on Icelandic
samples confirmed a highly significant nonrandom geogra-
phic distribution (%2 = 75.52, P < 0.001). A significantly
positive correlation was observed between the proportion
of hybrids and latitude, explaining 48.7% of the variance
in hybrid proportion (P = 0.025; Fig. 5). The proportion
of explained variance remained high (39%) and near
statistical significance (P = 0.073) even when removing the
Sauárkrókur sample (n = 6 ) from analysis. The correlation
between mean length of eels and latitude explained 2 1 %
of the variance and mean length tended to slightly increase
with latitude, but was not significant (P = 0.1826).
D iscu ssion
The objective of this study was to address three specific
questions regarding the dynamics of hybridiz,ation between
/Atlantic eels. We first evaluated the extent of hybridiza-
tion and tested for the occurrence of hybrids beyond the
first generation. Second, we tested whether hybrids were
randomly distributed across continents and among Icelandic
sampling sites. Third, we tested for a difference in the
proportion of hybrids between glass eel and yellow eel
stages in Iceland. Our results provided evidence for (i)
an overall hybrid proportion of 15.5% in Iceland, and
the existence of hybrids beyond the first generation; (ii)
a nonrandom geographic distribution of hybrids in the
North Atiantic; and (iii) a higher proportion of first and
later generation hybrids in the yellow eel stage compared
© 2006 B lackw ell P u b lish in g L td , Molecular Ecology, 15 ,1903-1916
1910 V. ALBERT, B. J Ó N S S O N and L. B E R N A T C H E Z
to the glass eel stage, as well as a significant latitudinal
gradient in the proportion of hybrids in lcelandic fresh-
water. Below, we discuss the possible causes and conse-
quences of these findings.
Extent ofhybridization and existence ofhybrids beyond F7
generation
Avise et al. (1990) previously confirmed the existence of
hybrid eels in lceland. However, Iimited sample sizes pre-
cluded these authors from confidently estimating their
proportion. Here, with the hundreds of markers and
samples, we found that 15.5% of al) Icelandic eels analysed
were of hybrid origin. The broad coverage of sampling
sites confirmed that hybrids are ubiquitous in Iceland,
being present in all locations, representing nearly half of
the eels analysed at some sampling sites (1 0 0 % hybrids in
the low sample size taken in SA). In contrast, we found no
evidence for the occurrence of introgressed eels in Europe.
This result was unexpected, given the previous report of
a few European eels with intermediate vertebrae counts
(Boetius 1980). However, the abnormal vertebrae counts
(< 109) were reported quasi-exclusively in northern Europe
(Iceland, Denmark and Faroes, except for one report in
both France and Spain). Our sampling coverage for the
northern part of the species' distributional range in Europe
precludes rigorously ruling out the occurrence of intro-
gressed eels. On the other hand, our results suggest that
a small proportion of American eels may be introgressed.
Interestingly, the three eels for which a pure American origin
was rejected were from the two northernmost sampling
sites. This observation, although preliminary, corrobo-
rates previous observations that the probability of finding
introgressed Atlantic eels may be higher at northern
latitudes.
Based on previous studies, it has remained unknown
whether hybrids are infertile, and therefore an evolutionary
dead end or, in contrast, a possible avenue for maintaining
gene flow between American and European eels. This study
provides the first evidence for the relatively common
occurrence of second or later generation hybrid eels, which
represented approximately 30% of all hybrid specimens
and approximately 5% of all Icelandic eels analysed. These
proportions demonstrate that hybrids between American
and European eels are viable, fertile, and can migrate back
to the Sargasso Sea for reproducing beyond the first filial
generation.
In situations of contentious species status, hybrid zones
have long been recognized as a means to assess taxonomic
status. Here, despite temporal and spatial reproductive
sympatry and interbreeding, American and European
eels remain reproductively isolated and almost entirely
genetically dístinct, therefore fulfilling the críteria of
distinct biological species despite the potential for gene
flow between them (Coyne & Orr 2004). Since there are
no obvious physical barriers during spawning to prevent
hybridization between American and European eels, their
persistence as distinct species could result from behavioural
and/or ecological reproductive isolating barriers (e.g. Young
et al. 2001; Taylor 2004), and/or as a result of sufficiently
strong natural selection overcoming the homogenizing
effects of gene flow (e.g. Schneider et al. 1999). In such a case,
ecological speciation processes, rather than strict geo-
graphic isolation, could be responsible for maintaining the
reproductive isolation between American and European
eels. This, however, would not necessarily exclude a possible
role for past allopatric separation in the maintenance of their
reproductive isolation through endogenous processes,
such as the accumulation of genotypic incompatibilities.
The nucleotide sequence divergence estimate of 3.7%
between the two monophyletic mitochondrial DNA clades
that characterize American and European eels (Avise et al.
1986) suggests that they evolved in allopatry, perhaps
during hundreds of thousands of generations, before their
secondary contact. Indeed, the dual role of both historical
contingency and ecological detenninism has been previously
reported in other fishes (Bernatchez et al. 1999; Taylor &
McPhail 2000; Fraser & Bernatchez 2005).
Geographic distribution ofhybrids
The second main observation of this study was the con-
firmation that both and later generation hybrid eels
are found almost exclusively in Iceland. What factors
may be responsible for this pattern? It has previously
been documented that American and European eel larvae
are not segregated during their migration (Kleckner &
McCleave 1985 in Wang & Tzeng 2000) and consequently,
it seems unlikely that Icelandic Iarvae would have their own
migration route. Alternatively, interspecific differences in
additive genetic basis for adaptive migratory behaviours
and/or larval development could result in intermediate
migration in hybrids (Rogers et al. 2002). Under this scenario,
it would therefore be more likely that hybrids would end
up in Iceland, which position is somewhat intermediate
between both continents. The possibility for orientated
swimming of the leptocephali larvae appears unlikely
given the small size of the larvae, the high current velocity
they must cope with, and the large distance to be covered
(McCleave et al. 1998). Therefore, processes that could
be responsible for the higher occurrence of hybrid eels in
Iceland are more likely to be associated with developmental
schedule and passive drift (McCleave 1987). Studies of daily
growth increments indicated that there is a significant
difference in larval duration between American and European
eels: 200 and 350 days respectively (Wang & Tzeng
2000). Even if the daily deposition on the leptocephali
otolith is still contentious (see Lecomte-Finiger 1994;
© 2006 B lackw ell P u b lish in g L td , M olecular Ecology, 1 5 ,1903-1916
N A T U R A L H Y B R I D I Z A T I O N IN A T L A N T I C EELS 1911
Cieri & McCleave 2000; Wang & Tzeng 2000), there is
no doubt that the larval stage duration is longer for the
European relative to the American eel. Given that fish
larval development is partially under additive genetic
control (Rogers & Bernatchez, in preparation), hybrids
could spend intermediate time as a larva and therefore be
more likely to successfully colonize freshwater habitats at
intermediate locations between continents, such as Iceland.
Differential growth rate between American (0.21 mm/day)
and European eel larvae (0.15 m m /day) has also been
reported (Wang & Tzeng 2000), which could further increase
the probability of colonizing freshwater habitats in inter-
mediate locations between continents. The premigration
metamorphosis of yellow eels is timed at both the develop-
mental and behavioural level (Haro 2003), such that eels
must reach a minimum threshold size before undertaking
their downstream migration (Oliveira 1999). Since minimal
threshold size also apparently applies to leptocephali
(Otake 2003), and given the interspecific difference in
the average size of glass eel (Wang & Tzeng 2000), hybrids
with intermediate growtli may also be characterized by an
intermediate time spent as larvae.
Hybrid proportion in Icelandic samples
Two distinct and confounding patterns were observed
regarding the proportion and distribution of hybrids in
Iceland. First, the proportion of hybrids was significantly
higher in yellow eels compared to glass eels. Then, we
also observed a variation in hybrid proportion with
year of arrival in glass eels. Since yellow eels were collected
approximately in the same time period as the glass eels, the
higher hybrid proportion in the yellow eels could result
from either a higher survival of eels in Icelandic freshwater
and/or to a temporal trend in the reduction of hybrids
reaching Iceland. Here, we discuss the potential scenarios
that could be responsible for the patterns we observed,
given the strengths and limitations of our data set.
Natural selection may influence the hybrids' relative
fitness in terms of differential survival, and as such,
modulate the observed proportion of hybrids. Examples
where first generation hybrids (F,) showed equal or higher
fitness relative to at least one of the parental forms are
common in plants (e.g. Burke et al. 1998; Orians et al. 1999;
Campbell & Waser 2001; Campbeil 2003; Song et al. 2004;
Kirk et al. 2005), and several examples exist in animals
as well (e.g. Grant & Grant 1992; Scribner 1993; Emms &
Arnold 1997; Hotze ta l. 1999; Parris 2001; Perry et al. 2001;
Schweitzer et al. 2002). However, few studies have evalu-
ated relative fitness beyond the first hybrid generation.
Most studies directly comparing survival of first and later
generation hybrids were performed in laboratory or con-
trolled conditions (e.g. Moore & Koenig 1986; Saino & Villa
1992; Howard et al. 1993; Wang et al. 1997; Campbell et al.
1998; Vilá & D'Antonio 1998; Fritsche & Kaltz 2000; Good
etal. 2000; Hauser et al. 2003; Burgess & Husband 2004;
Gilk et al. 2004; Rosenfield et al. 2004; Facon etal. 2005). As
a result, the evolutionary processes as well as the potential
outcome of hybridization in natural settings remain
largely unexplored in animals (Burke & Arnold 2001; but
see Grant & Grant 1992; Emms & Arnold 1997; Perry et al.
2001; Schweitzer et al. 2002). Here, assuming that the pro-
portion of hybrids arriving in Icelandic waters is relatively
constant, the higher frequency of both Fj and later genera-
tion hybrids in yellow eels relative to glass eels would indi-
cate a higher relative survival of hybrids. In animals,
higher hybrid survival has previously been documented
for the Darwin's finches Geospiza fortis, Geospiza scandens,
and Geospiza fuliginosa. Thus, Grant & Grant (1992)
compared the survival of natural first and later generation
hybrids to the parental forms and observed a higher sur-
vival in both categories. Other examples of natural hybrids
with a higher relative fitness also exist (e.g. Moore &
Koenig 1986; Saino & Villa 1992; Howard et al. 1993; Bert
& Arnold 1995; Good et al. 2000; Rubidge & Taylor
2004). According to environment-dependent hybrid zone
models, superior hybrid srrrvival is more likely to be observed
in novel habitats or in a novel combination of environmental
factors (Howard et al. 1993). For instance, when surveying
two ecologically differentiated taxa in sedge (Carex curvula),
Choler et al. (2004) found that genotype integrity was
maintained in optimal habitats, and that hybrids were
favoured in marginal habitats. Genetic introgression was
thus considered 'as a potential to widen a species' niche'.
The situation may be similar for North Atlantic eels.
Iceland, where hybrids are observed, is located at the limit
of the northern distribution range of the European eel, and
may therefore be considered as representing a marginal
habitat relative to the typical environments to which pure
European eels are mainly adapted to.
As recognized earlier by Grant & Grant (1996): 'the key
to understand the spatial patterning of hybridization and
the relative fitness of hybrids could lie in the ecology
and breeding behaviour.' Here, we discuss hypothetical
ecological and/ or behavioural causes that could explain
a higher hybrid survival in Iceland. Admittedly, however,
the veracity of these hjqiotheses must await further experi-
mental investigations. European freshwaters are warmer
on average than Icelandic waters and the average length
of the growing season is longer in continental Europe
(Einarsson 1984). A higher hybrid survival raises the hypo-
thesis that hybrid eels with hybrid genotypic combinations
could be better adapted (either due to a shift in the mean or
an increased variance of a phenotypic trait) than pure
European eels to environmental conditions experienced in
Iceland, thus increasing survival probability. For instance,
American eels face colder winters on average relative to
European eels (Seager et al. 2002). American eels are thus
© 2006 B lackw ell P u b lish in g L td , Molecular Ecology, 1 5 ,1903-1916
1912 V. ALBERT, B. J Ó N S S O N and L. B E R N A T C H E Z
potentially exposed to a larger range of temperatures than
European eels, which could perhaps provide physiological
advantages to hybrid eels relative to European eels in
Iceland. Nonetheless, experiments on temperature physio-
logical tolerance and adaptation of Atlantic eels in natural
environments are lacking aird difficult to realize. Eels in
the laboratory typically stop feeding and gradually reduce
their activity to complete torpor when exposed to low
temperatures (Nyman 1972; Sadler 1979; Walsh et al. 1983;
Linton et al. in press). Moreover, observation varies con-
siderably from one laboratory experiment to another.
For instance, Nyman (1972) reported that European eels
did not feed or search for food when temperatures were
lower than 14 °C and the same observation was made in
the American eels (Barila & Stauffer 1980). In contrast, other
studies mentioned lower feeding temperatures such as
8 °C (Walshef al. 1983) or 10 °C (Bruun 1963 inNyman 1972).
Second, a possible role for natural selection in explaining
a higher proportion of hybrids in yellow eels relative to
glass eels in Icelandic freshwaters was also suggested by a
positive relationship between the proportion of hybrids
and latitude. This observation raises the hypothesis of
differential survival favouring hybrids that may correlate
with a thermal latitudinal gradient. Thus, while there are
no good records for freshwater temperature per se, it is
known that mean water temperature correlates with
mean air temperature, and that mean yearly air tempera-
ture decreases with latitude in our sampling area, resulting
in shorter summers and colder winters at more northern
latitudes (Einarsson 1984). Water temperature has a major
influence on eels' metabolism (Sadler 1979), oxygen con-
sumption, and enzyme activities (Walsh et al. 1983), as well
as behaviours such as feeding, aggression, and habitat
selectivity (Nyman 1972; Barila & Stauffer 1980). Tlrere-
fore, different thermal optima between pure European
and hybrid eels could result in differential performance
and perhaps survival depending on the thermal regime.
Although this possibility cannot be ruled out entirely, it
seems less likely that the observed latitudinal gradient in
the proportion of hybrids is associated with a variation in
the proportion of hybrids arriving in Iceland. First, yellow
eel samples were composed of eels from different cohorts,
which should buffer the impact of the yearly variation.
Second, we found no significant sampling site effect on the
size of yellow eels that were collected. Although size only
represents an approximation of age, the lack of association
between rnean eel size and latitude suggests that difference
in age between yellow eels from different locations cannot
explain alone the latitudinal pattern we observe.
Third, temporal changes in the relative survival of
hybrids in the ocean associated with global warming could
explain the apparent temporal decrease in the proportion
of hybrids arriving in Icelandic waters. For instance, Perry
et al. (2005) demonstrated that many exploited and non-
exploited fishes from the North Sea, have responded
markedly to recent increases in sea temperature, whereby
the distribution of 21 out of 36 species surveyed shifted
either in mean latitude, depth or both over the last 25 years.
In Atlantic eels, the Den Oever glass eel recruitment index
declined markedly since the late 1980s, which coincided
with consistently positive sea surface temperature
anomalies since then (ICES 2001; Knights 2003). Under the
hypothesis that the thermal physiological optirna is lower
for hybrids relative to pure eel larvae, higher temperature
could result in increased relative survival of pure European
eels, and in an apparent reduction of the proportion of
hybrid eels arriving in Icelandic waters.
An additional, nonexclusive cause of the variation in
the proportion of hybrids arriving in Iceland could reside
in the modification of the oceanic circulation (Knights 2003;
Wirth & Bernatchez 2003). Thus, the ongoing warming
of the Sargasso Sea/Sub-Tropical Gyre is hypothesized
to inhibit sprmg thermocline mixing and nutrient mixing,
which would have marked impact on productivity in the
spawning area of the Atlantic eels and could reduce the
amount of food available for the leptocephali (Bates 2001).
Moreover, modifications in oceanic currents could reduce
transport rate and hence probably prolong migration of
leptocephali, exacerbating impacts of low nutrition and
exposing them for a longer period to predation (Knights
2003). Under the hypothesis that hybrids are genetically
intermediate between European and American eels, and
knowing that European eels are adapted to a longer
oceanic migration period relative to American eels (Arai
et al. 2000; Wang & Tzeng 2000), it is plausible that ongoing
changes in oceanic circulation could result in a lower
proportion of hybrids reaching Icelandic waters relative to
pure European eels.
Besides differential survival between hybrids and pure
European eels, both in freshwater and in the ocean, addi-
tional factors may explain the higher proportion of hybrids
we observed in yellow eel compared to glass eel samples.
Spatial variation in hybrid zone dynamics has been reported
in several species (e.g. Bleeker & Hurka 2001; Williams
et al. 2001; Watano et al. 2004; Aldridge 2005). In the same
way, temporal variation in the extent of spatial overlap
could also result in variation in the extent of hvbridization.
For instance, Watano et al. (2004) found an important role
of the size and position of the distribution gap in two Pinus
species to explain the differences in level and pattern
of introgression in two distinct contact sites. Moreover,
Emeiianov et al. (2001) proposed that year-to-year variation
in population densities could be an important factor lead-
ing to temporal variation in natural hybridization. Clearly,
recruitment in American and European eels has declined
sharply in recent decades (Castonguay et al. 1994; Dekker
2000; Haro et al. 2000; ICES 2001), possibly by up to 90%
in some European rivers (Dekker 2003). We propose that
© 2006 B lackw ell P u b lish in g L td , M olecular Ecology, 1 5 ,1903-1916
N A T U R A L H Y B R I D I Z A T I O N IN A T L A N T I C EELS 1913
such demographic decline could decrease densities of
eels on spawning grounds in the Sargasso Sea. Decreased
densities could in turn reduce the area of overlap during
spawning and therefore the number of hybrids being
produced. The decreasing trend in hybrid proportion tirriv-
ing in Icelandic waters from 2000 to 2003 tends to support
this hypothesis, although a longer time series will be
necessary to verify it.
Admittedly, this study does not allow to confidently
conclude on the nature of possible causes for the higher
proportion of hybrids observed in the yellow eels compared
to glass eels in Iceland. However, since pre- and postmating
isolating barriers are nonexclusive processes, we propose
that the combined effect of both differential survival of
hybrids and variation in hybridization rate through time
may best explain the patterns we observe. Indeed, climate
change is impacting many environmental features and
could have a determinant effect on the outcome of natural
hybridization in Atlantic eels. Moreover, the complexity
of Atlantic eels' life cycle, which comprises several critical
stages, may exacerbate the impact of environmental con-
ditions on the production and survival of hybrids. Clearly,
experimental investigations, as well as additional field data,
will be necessary for elucidating the role of both selective
and demographic factors influencing the dynamics of
natural hybridization in Atlantic eels.
Implications for natural hybridization studies
The diverse array of outcomes in hybridizing species
calls for more studies of introgressive hybridization in
natural environments. This study added to the diversity
of possible outcomes of hybridization in that hybridization
between American and European eels results in a very
unique case of hybrid zone, whereby hybrids are located
thousands of kilometres away from where interbreeding
occurs. To our knowledge, it is the first documentation
of such a hybrid zone. Second, this study illustrated
that interspecific hybridization is a very dynamic process,
whereby the combination of both pre- and postmating
mechanisms may result in pronounced spatio-temporal
fluctuations in the proportion of hybrids found in nature.
It also suggests that post-F ̂hybrids may ha ve higher fitness
than parental forms under specific circumstances, and
demonstrates that introgressive hybridization is a possible
avenue for maintaining gene exchanges between American
and European eels. Overall, our results add to the increasing
number of studies showing that natural hybridization may
play a significant role in adaptation and evolution.
A ck now ledgem ents
W e a re g ra te fu l to R. S a in t-L au ren t a n d L. P a p illo n fo r la b o ra to ry
ass is tan ce , to P. D u c h e sn e a n d D. F a lu sh fo r a n a ly tica l adv ices . W e
sin ce re ly th a n k T. W irth fo r p ro v id ín g D N A sam p le s a n d E.
E lfa rsd ó ttir, S. In g ó lfsd ó ttir , a n d G . I. G u ö b ra n d sso n fo r a ss is tan ce
w ith field w o rk . F inally , w e a ck n o w le d g e su b jec t e d ito r G. W aliis ,
as w e ll a s M . C as to n g u a y , A . M . G ale a n d th re e a n o n y m o u s referees
fo r th e ir h e lp fu l c o m m e n ts o n th e m a n u sc rip t. T h is re sea rch w as
su p p o r te d b y a FQ R N T (F onds d e re c h e rch e s u r la n a tu re e t les
te c h n o lo g ie s d u Q u é b ec ) p o s tg r a d u a te s c h o la rs h ip s to V .A .,
the C an a d ia n R esearch C h a ir in c o n se rv a tio n g en etics o f a q u a tic
re s o u rc e s , a n d a g r a n t fro m S c ien ce a n d E n g in e e r in g R e s e a rc h
C an a d a (NSERC, D isco v ery g ra n t p ro g ra m ) to L.B.
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© 2006 B lackw ell P u b lish in g L td , M olecular Ecology, 1 5 ,1903-1916
1 1 3
Age at recruitment of Icelandic eels (Ánguilla rostrcUa and A. anguilla)
as revealed by otoiith microstructure
Momoko K a v v a i\ Bjami JónssonJun Aoyama1, Davíd L. G. Noakes3 & Katsumi Tsukamoto1
u2Department Marine Bíoscience, Ocean Research Institute,
The University ofTokyo, 1-15-1 Minamidai, Nakano.Tokyo 164-8639, Japan
2 Insritute of Freshwater Fisheries at Holar, Holar Hjaltadal, IS 551 Saudarkrokyur, Iceiand
3 Department of Zoology, University of Guelph, Guelph, Ontario, NIG 2WI, Canada
In the Atlantic Ocean there are tvvo species of freshwater eels, the American eel, Anguilla rostrata, and the
European eel, A. anguilla. Both A. rostrata and A. anguilla spawn in an overlapping area of the Sargasso sea
(Schmidt, 1922; Scotch and Tesch, 1982; McCIeave et al., 1987), but they have separated freshwater habiíais
along the east coast of the North American contínent for the forroer and the west coast of Eurasian continent for
the latter (Schraidt, 1909; Boetius, 1985). Both species occur in lceland, the only area of sympatry (Boetíus,
1980; Wiliiams and Koehn, 1984; Avise et a l, 1990).
It is not vvell understood how these two species mainíain separate species ranges in their freshwater
habitats that are separated bv the Atlantic Ocean. It has been suggested fhat their separate ranges were the
consequence of differences in the larval growth rates of the íwo species (Schmidt, 1925; Wang and Tzeng, 2000;
Arai et al., 2000), however this hypothesis has not been verified (Boetius and Harding, 1985).
In this study, we anaiyzed otolith microstructure of the glass eels of boíh species collected in Iceland to
compare theír ages aí recruitment aimed at providing nevv knowledge about the recraitment mechanism of the
two Atlantic eel species. We also compare the resulis obtained for the two Icelandic eels with previous
knowledge obtained from the main populations of each species in North America and Europe, to test the
hypothesis that the ages of Icelandic glass eels differ from those in the rnain part of their ranges. Our objective
is to reveal the possibie mechanisms that maintain the separation between the two species ranges and to provide
some instght on the evoiutionary' process o f speciation of the two Atlantíc eels.
Materials and Meíhods
Glass eels of A. rostrala (63-72 mm TL) and A. anguilla (58-78.5 mm TL) were collected by hand net at the
mouth of a small river in Vogslækur, in southwest Iceland on 28 June 1999, and during 7 May to 8 July 2000.
They were initialiy placed in 70% ethanol immediately after sampling, and then preserved in 96% ethanol.
Identífication of species were carried out using moiecular genetic techniques (Aoyama et ai., 2000). Thirteen A.
rostrata and 44 A. anguiUa collected in 1999 and 2000 vvere analyzed. Total age and incremental width were
analyzed from otoliths.
Introduction
2,0 (B )
1.0
0 0
200 400 200 400
3 4.0 - ~*~A.bicolor pacifica'pacij
’IíS
ys
~°~A. austraús
~6r~A. rosrrata
A.japonica
-°—A.anguílla
200
A g e (days)
400
Fg. 1 P ro llia s o f o to iith inc rem en tal w id th s iro m th e co re to th e edge.
(A ) Ice ia n d ic A. anguilla, (B ) Ice land ic A. ro s ira ia , ( Q p rev io u s reports .
1 1 4
Results
The average total age at recruitment of A. rostrala was 349 ± 44.3 d, and that of A. anguilla was 365 ± 44.3 d.
There was no sigmficam difference in total age between two species (p > 0.05; Mann-Whitnev D'-test). Otolith
microstracture differed from that previously reported in anguillíd eels.
We detected no sharp increase in otolith increment width, or rapid growth zone that is a characterisíic
incremental change corresponding £o the onset of metamorphosis as has been reported from many anguiiiid
species (Arai et al., 1997,1999a, 1999b; Wang and Tzeng, 2000) (Fig. 2).
Discussion
Compared to the age at recraitment of their main population in North America the average total ages of the glass
eels of A. rosiraia collected ín Iceland were as much as 100 days older. On the other hand, A. anguilla was 100
days younger than the Europeart popuiation (Wang and Tzeng, 2000) (Fíg. 2). The distance from the Sargasso
Sea to Iceland ís obviously farther than to North America (about 3000 km from Newfoundland or Labrador m
Canada to Iceland), which would account for íhe greater ages oí A. rostrata ín Iceland. The distance between
Iceland and Ireland or England is about 1000 km.
Similarlv, IceJandic A. anguilla have been
suggested to have a shorter migration time than
other European A. anguilla because of the shorter
distance than to some parts of Europe.
The lack of a drastic increasing otolith
incremental zone in ícelandic glass eels suggests
that they experienced extraordinary environmental
conditions. The most.probable factor to prevent
the formation of a rapid growth zone in Icelandic
eels wouid be the low vvater temperature in the
coastai waters of Iceland. Water temperature is
welí known to influence otolith growth in fishes
(Campana and Neilson, 1985), .and it has been
reported that leptocephali metamorphose to glass
eeis in the coastal waters near their freshwater habitals (Kleckner and McCleave, 1985). The sea temperature
just to the souíh of Iceland in May has been obsetved to be 1 - 8 °C (Krauss 1995; Swíft and Aagaard, 1981),
which is about 10-20°C lower than in the coasíal vvaters of the main habitats of these two species in North
America and Europe. Therefore, it is probable that the indivíduals recruiting to-Iceland metamorphosed under
unusuaily low temperature conditions that may have caused substantial physiological stress. This stress couid
have interfered with the formation of a rapid growth zone in their otoiiths.
As a whole, the results suggest that both species may follow the same migration route from the Sargasso
Sea to Iceland and that the timing of metamorphosis could be an important factor in dectding the place to which
glass eels recruit
References
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(A) Icelandic eels
( A. anguilla)
(B) Icelandi eets
(A. rostrata)
(C) European eels
(A. angvá.lla) □
(D) American eels
(A. rosiraia)
400 500
Fig. 2 Total age of gSass eeis (A. B) this study, (C, D)
Wang and Tzeng (2000).
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Proceedings of the Intemational Symposium
ADVANCES IN EEL BIOLOGY
Research for the Future Program
Japan Society of the Promotion of Scienee
Organizing Committee
Katsumi Aida
Katsumi Tsukamoto
Kohei Yamauchi
Yayoi Auditorium
The University of Tokyo
28 - 30 September 2001
M o lec u la r E co logy (2009) 18 ,1678-1691 doi: 10.1111 /j.l365-294X .2009.04142.x
Natural selection influences AFLP intraspecific genetic
variability and introgression pattems in Atlantic eels
P. A. G A G N A IR E /V . ALBERT,t B. JÓ N S SO N t and L. BERNATCH EZt
*lnstitut des Sciences de l'Evolution (ISEM UMR 5554 CNRS-UMII), Uníversíté de Montpellier II, CC 065, Place E. Bataillon,
34095 Montpellíer cedex 5, France, ilnstitut de Biologie Intégrative et des Systémes (IBIS), Universíté Laval, Québec, Canada G1V 0A6,
%Institute ofFreshivater Fisheries, Northern Division, Saudárkrókur, Iceland, IS 550
Investigating pattem s of genetic variation in hybridizing species provides an opportunity
to understand the impact o f natural selection on intraspecific genetic variability and inter-
specific gene exchange. The Atlantic eels Anguilla rostrata and A. anguilla each occupy a
large heterogeneous habitat upon w hich natural selection could differentially shape
genetic variation. They also produce viable hybrids only found in Iceland. However, the
possible footprint of natural selection on patterns of genetic variation w ithin species and
introgressive hybridization in Icelandic eels has never been assessed. We revisited amplified
fragm ent length polym orphism data colleeted previously u sing population genom ics
and admixture analyses to test if (i) genetic variation could be influenced by non-neutral
m echanism s at both the intra- and interspecific levels, and if (ii) selection could shape
the spatio-tem poral distribution of Icelandic hybrids. We first found candidate loci for
directional selection w ith in both species. Spatial d istributions of a lle lic frequencies
disp layed by som e of these loci were p ossib ly related w ith the geographical patterns of
life-history traits in A. rostrata, and could have been shaped by natural selection associated
with an environmental gradient along European coasts in A. anguilla. Second, w e identified
outlier loci at the interspecific level. Non-neutral introgression was strongly suggested for
som e of these loci. We detected a locus at w hich typical A. rostrata allele hardly crossed the
species genetic barrier, whereas three other loci showed accelerated pattems of introgression
into A. anguilla in Iceland. Moreover, the level of introgression at these three loci increased
from the glass eel to the yellow eel stage, supporting the hypothesis that differential
survival o f admixed genotypes partly explains the spatio-temporal pattem of hybrid abund-
ance previously documented in Iceland.
Keywords: AFLP, Anguilla, introgressive hybridization, natural selection, outlier loci, species
genetic barrier
Received 5 November 2008; revision received 5 January 2009; accepted 22 january 2009
Abstract
C o rre sp o n d en c e : L ou is B em atch e z , Fax: 1 418 656 7176;
E -m ail: lo u is .b em atch ez@ b io .u lav a l.ca
Disceming the relative influence of neutral vs. selective
processes acting in natural populations is a fundamental
step towards the comprehension of species' evolution.
Populations living in heterogeneous habitats are likely to
undergo diverse selective constraints that can differentially
shape genetic variation among them, occasionally leading
to reproductive isolation (Mayr 1947). Direct observation
Introduction
of the genetic effects of natural selection can be conveniently
assessed when adaptive phenotypic traits and genes
underlying these adaptations are known. In most nonmodel
organisms, a priori knowledge concerning the genes
governing adaptive traits is often not available, thus, it
becomes necessary to use indirect methods to identify loci
potentially under selection. Such 'population genomics'
approaches are based on the principle of screening sufficient
number of molecular markers randomly distributed
across the whole genome in a large number of individuals,
to detect loci whose level of differentiation between popula-
tions exceeds that expected under neutral expectations.
© 2009 B lackw ell P u b lish m g L td
mailto:louis.bematchez@bio.ulaval.ca
N A T U R A L S E L E C T I O N F O O T P R I N T S IN A T L A N T IC EELS 1679
These 'outlier loci' are assumed to be located in the vicinity
of actual genes under selection due to genetic hitchhiking
(Beaumont & Nichols 1996; Luikart et al. 2003; Beaumont &
Balding 2004; Beaumont 2005; Stinchcombe & Hoekstra
2007; Via & West 2008). Ideally, outlier identification in a
genome scan needs to be followed up with approaches
such as bacterial artificial chromosome (BAC) library
screening to identify functionally important polymorphic
sites (e.g. Wilding et al. 2001; Wood et al. 2008). Nevertheless,
such an approach provides an efficient means to estimate
the proportion of loci involved in adaptive divergence, and
compare sets of outlier loci identified in various selective
contexts (e.g. Wilding et al. 2001; Campbell & Bernatchez
2004; Rogers & Bematchez 2007). For instance, population
genomics allowed specifying the role of environmental
factors in shaping the distribution of genetic diversity
along environmental gradients (Bonin et al. 2006; Jump
et al. 2006). In addition, the analysis of differentiation
patterns among the genomes of closely related species
suggests that divergent selection usually concems a few
loci at which gene flow is dramatically reduced, whereas
most of the genome appears permeable to gene exchange
(Scotti-Saintagne et al. 2004; Savolainen et al. 2006; Minder
& Widmer 2008).
Population genomics has also improved our under-
standing of the architecture of genetic barriers between
hybridizing species. Mosaic genomes reveal delays, or
even barriers to introgression at loci undergoing negative
selection in hybrids and in the recipient species (Martinsen
et al. 2001). Such effects can be due to disruption of epistatic
interactions between co-adapted genes by recombination
and may be largely responsible for hybrids inferiority
(Burke & Amold 2001). Conversely, hybridization may also
accelerate the rate of introgression at positively selected loci
(Kim & Rieseberg 1999; Martin et al. 2006; Whitney et al.
2006). Therefore, hybridization can have a variety of effects
in species evolution, and contrasted footprints are expected
to be found at the genome level between neutral, negatively
and positively selected genes. A genome-scan approach is
appropriate to observe these differential pattems of intro-
gression and help to understand the particular architecture
of the barrier to gene flow between hybridizing species
(Rieseberg et al. 1999; Rogers et al. 2001).
The present study aimed at testing the influence of natural
selection on genetic variation at various scales in Atlantic
eels. The two Atlantic eel species Anguilla rostrata and A.
anguilla each occupies a large heterogeneous habitat,
corresponding to most of North America and Europe
(including Iceland and Northem Africa), respectively. It is
widely accepted that each of the two Atlantic eel species
has a unique spawning area, both located and overlapping
in the Sargasso Sea (Schmidt 1925; McCleave etal. 1987;
see Appendix Sl, Supporting Information). This aspect of
eel life history led to the prediction that genes should be
randomly exchanged within each species, which has been
supported by a number of studies (e.g. De Ligny & Pante-
louris 1973; Comparini et al. 1977; Avise et al. 1986; Lintas
et al. 1998). However, the use of microsatellite markers later
revealed weak albeit significant genetic differentiation
in the European eel (Wirth & Bematchez 2001; Daemen et al.
2001). Genetic patterns corresponding to isolation by
distance (Wirth & Bematchez 2001; Maes & Volckaert 2002)
and isolation by time (Dannewitz et al. 2005; Maes etal.
2006; Pujolar et al. 2006) were also documented, therefore
contradicting the results of earlier studies. In both species,
a latitudinal cline of allozymic variation potentially induced
by natural selection was also reported (Williams et al. 1973;
Koehn & WiIIiams 1978; Maes & Volckaert 2002). Therefore,
the potentially confounding effects of natural selection on
species genetic diversity must be investigated in greater
detail to understand the nature of population structure in
Atlantic eels.
Molecular analyses also recently showed that both eel
species interbreed to produce viable hybrids that are only
encountered in Iceland (Avise et al. 1990; Albert et al. 2006).
Albert et al. (2006) further revealed that F, hybrids can
successfully migrate back to the Sargasso Sea and reproduce.
Passive larval transport through the Gulf Stream combined
with heterogeneity of larval duration were proposed to
explain why hybrids are geographically limited to Iceland
(Albert et al. 2006; Kettle & Haines 2006). Furthermore,
a puzzling spatio-temporal pattern emerged from the
proportions of hybrids observed in Icelandic rivers. Albert
et al. (2006) found higher first- and later-generation hybrid
proportions in yellow eels compared to glass eels, and a
latitudinal increase towards the north in the proportion of
hybrids. However, the possibility of a temporal decrease
in hybridization rate hampered tests of the hjqsothesis of
differential survival between purebreds and hybrids in
Iceland. Also, identification of loci potentially under the
effect of selection was out of the scope of Albert et al.'s 2006
study. Therefore, the influence of natural selection on hybrid
and pure European eel abundance in Iceland remains
untested. Here, our main objective was to use population
genomics and admixture statistical methods to revisit the
amplified fragment length polymorphism (AFLP) data of
Albert et al. (2006), in order to test if (i) intraspecific genetic
structure of each species and if (ii) hybrid proportions
and genetic composition found in Icelandic rivers were
influenced by natural selection.
M aterials and m ethods
Study species, sampling sites
Five developmental stages characterize the complex life
cycle of Atlantic eels (Tesch 2003). The oceanic pelagic
larvae, which undergo a several month drift through the
© 2009 B lackw ell P u b lish in g L td
1 6 8 0 P . A . G A G N A I R E E T A L .
Table 1 Sampling location, abbreviation, date and size of each sample. Sampling year and iife stage (G, glass eel; Y, yellow eel) were only
provided when all individuals were homogeneous for these characteristics. Number of individuals in each of the six categories defined with
NewHybrids was determined and detailed for each sample: Aro (parental A. rostrata), Aan (parental A. anguilla), F, (Aro x Aan), F, (Fi x F,),
BCa„ (Aro x F,) and BCAan (Aan x F,)
NewHybrids' categories
S a m p lin g lo ca tio n S am p le a b b re v ia tio n S am p lin g d a te S a m p lin g size Life s tag e A ro F, F, BCAr0 BCAan A an
N o rth A m erica
M ed o m a k R iver M E 1999 45 Y 45 — — — — —
B oston H a rb o r BO 1999 50 G 50 — — — — —
W ye R iver WY 1999 48 Y 48 — - — - —
St Jo h n s R iver SJ 1999 50 Y 50 — — — — —
Total A m erica A ro 1999 193 193 — — — — —
E u ro p e
E lbe R iver EL 1999 49 Y — — — — — 49
G ra n d L ieu L ake G L 1999 49 G 49
M in h o R iver M I 1999 45 G — — — — — 45
M o u lo u y a O u e d M O 1999 43 G - — - — - 43
Total E u ro p e A an 1999 186 — — — — — 186
Ice lan d
S a u d á rk ró k u r SA 2003 6 Y — 4 — — 2 —
V a tn sd a lu r VA 2000 18 Y — 1 2 — 2 13
R ey k h ó la r RE 2001 13 Y - 5 1 — — 7
Bár BA 2003 49 Y — 4 — — 2 43
V og slæ k u r V O 2000 50 G — 8 - — 5 37
2001 50 G — 3 1 — 2 44
2002 49 G — 1 — — — 48
2003 49 G — 3 — — 2 44
2001 36 Y — 2 1 — 3 30
Seljar SE 2001 48 G - 4 2 — 4 38
2001 46 Y — 11 1 — 7 27
V ífilss tad av a tn VI 2001 50 G — 1 2 — 6 41
2002 45 Y — 4 — — 6 35
G ra fa rv o g u r G R 2003 45 Y — 1 — — 2 42
S tokksey ri ST 2001 46 G - — 2 — 1 43
2003 50 G — — — — 1 49
2003 49 Y — 5 1 — 1 42
Ö x n a læ k u r o x 2003 49 Y — 1 — — 4 44
Total Ice land 748 — 58 13 — 50 627
Ice lan d A. anguilla sa m p le IC 2001 57 Y — — — — — 57
Ice lan d F, s am p le (70%) F, 33 — 33 — — — —
Ic e lan d F2 s am p le (50%) F2 11 — — 11 — —
lc e lan d BCAan sam p le (70%) BCAan 38 - — - — 38 —
North Atlantic Ocean, are called leptocephali. Larvae
metamorphose into glass eels when they reach the contin-
ental shelves, and then temporarily settle in estuaries where
they become pigmented. This corresponds to the transient
elver stage that precedes the yellow eel phase. After 3-
20 years spent in their growing continental habitat, yellow
eels metamorphose into sexually mature silver eels and
migrate back to the Sargasso Sea to reproduce. The present
study focuses on the glass eel and the yellow eel stages.
Table 1 provides information concerning sampling
location and date, sample size, life stage and individual
hybrid status of the 1127 eels analysed with 373 AFLP loci
by AlbertjrfflL_(2006} (see also Appendix S l, for a map
showing the geographical distribution of sampling sites).
In order to perform pairwise comparisons with Anguilla
anguilla samples from the European continent, we built an
Icelandic sample by pooling pure European eel individuals
from the yellow eel samples of Seljar and Vogslækur, both
collected in 2001 (called IC in Table 1 and Appendix Sl).
These two samples were chosen because they were tempo-
rally close to the European samples collected in 1999 and
not geographically distant in Iceland.
© 2009 B lackw ell P u b lish in g L td
N A T U R A L S E L E C T I O N F O O T P R I N T S IN A T L A N T IC EELS 1681
Hybrid category assignment
We used N ew H ybrids software, w hich im plem ents
a multilocus allele-frequency model-based method for
determining hybrid status (Anderson & Thompson 2002).
This method performs individual clustering without any
a priori knowledge of parental allele frequencies, and has
the advantage of specifically assuming a mixture of parental
and various hybrid classes in its probability model.
Six categories corresponding to parental (pure American
and pure European), Fu F2 and backcrosses (with BCAro
individuals generated by crossing events between an Fj
and a pure Anguilla rostrata and BCAj„ individuals between
an F, a pure A. anguilla) were considered. Individual
posterior probabilities to belong to each hybrid category
were estimated by Markov chain Monte Carlo method
in a Bayesian framework. We initially set a posterior
probability threshold of 0.7, above which individuals
were assigned. This threshold was subsequently lowered to
0.5 for the F2 category. Calculations were run using Jeffreys-
type priors and a burn-in period of 50 000 iterations
followed by 50 000 sweeps for sampling from the posterior
distribution.
Outlier loci detection
We used the Dfdist program implementing the hierarchical-
Bayesian approach of Beaumont & Balding (2004) to detect
outlier loci. Null allele frequencies were first estimated
at each locus of the empirical AFLP data set using
Zhivotovsky's (1999) Bayesian approach , enabling Fsx
values to be estimated for each locus (Weir & Cockerham
1984). A mean 'neutral' FST value supposedly uninfluenced
by selected loci was then calculated after removal of 30%
of the highest and 30% of the lowest FST values found in
the empirical data set (see Bonin et al. 2006; Miller et al.
2007; Nosil et al. 2008). This 'trimmed' Fsx value was used
to target the mean Fsx of 50 000 loci generated by
coalescent simulation. Therefore, the FST distribution of
these simulated loci was expected to be close to that of
the neutral empirical data set. The outlier threshold was
defined by an envelope delimited by the 0.005 and 0.995
quantiles of simulated Fsx. However, because the power
to detect footprints of balancing selection is generally
low (Beaumont & Nichols 1996; Beaumont & Balding 2004),
only outliers that were candidates for directional selection
were considered.
We searched for directional selection footprints at the
intraspecific levels in North American and European
locations, together with Iceland, by comparing all possible
pairs of samples in each species. As some trimmed Fsx
values were less than 0.005 or even slightly negative, they
suggested that neutral FST was close to zero between some
eel samples of the same species. Therefore, in order to
perform locus simulations with Dfdist, a small positive Fsx
of 0.005 was used (Miller et al. 2007). In this way, detection
of outlier loci was more conservative. Moreover, pairwise
analyses allow the identification of loci that are outliers in
multiple pairs of populations. We considered loci that were
detected as outliers in more than two pairwise comparisons
as the most likely candidates, thus reducing type I error
(Nosil et al. 2008). We then conducted an interspecific
analysis by pooling pure individuals from the same species
into an A. rostrata (Aro) and an A. anguilla (Aan) sample.
Individuals from Iceland were not included in this anal-
ysis to avoid the influence of putative Iceland-specific
selection.
Locus-specific introgression level
In order to detect the potential effects of natural selection in
Icelandic hybrids, we tested departure from theoretical
frequencies at each locus in each hybrid category. Because
the determination of hybrid status with NewHybrids
showed that only pure individuals occurred in continental
locations of Europe (A . anguilla) and America (A. rostrata)
(Table 1, see also Albert et al. 2006), we used the pooled
A. rostrata (Aro) and A. anguilla (Aan) samples to estimate
parental allele frequencies. At each locus in each species,
we assumed Hardy-Weinberg equilibrium to estimate
the frequency of the null allele from the square root of
the null homozygote frequency. Using these observed
parental frequenties, expected allele frequenties were then
calculated for each of the three hybrid categories found in
Iceland: F„ F2 and BCAan (see Results). A binomial test
was then performed to test for significant deviation between
observed and expected frequencies of band presence at
each locus in each hybrid category. A Bonferroni correction
was applied to avoid false positive detection due to type I
errors.
Maximum-likelihood estimates ofhybrid indices
We also applied a complementary approach based on
the estimate of hybrid indices over nondiagnostic loci
(Rieseberg et al. 1998, 1999). This allows the detection of
candidate loci for which the introgression pattern has
possibly been influenced by selection (Rogers et al. 2001).
The model assumed two separated parental populations
that both contributed to an admixed population. Hybrid
indexfor an individual is an estimate of the proportion of its
ancestors that belonged to each parental species at the
generation before the first interbreeding event in its
ancestry. Therefore, the joint estimate of hybrid index over all
individuals reflects the relative contribution of each parental
source to the admixed population based on individuals.
Hybrid indices were estimated from allele frequencies
of both parental samples assessed with the square root
© 2009 B lackw ell P u b lish in g L td
1682 P. A. G A G N A I R E E T A L .
T ab le 2 N u m b e r o f p o ly m o rp h ic loci a n d o u tlie r loci fo u n d in e ach in traspecific p a irw is e c o m p a riso n fo r b o th A tlan tic eel spec ies. F o r e ach
s a m p le pa ir, th e m e a n v a lu e a n d th e r a n g e o f o u tlie r FSJ, th e tr im m e d FST v a lu e a n d th e p re s u m e d n e u tra l FsT v a lu e fo u n d w íth m ic ro sa te llite
m a rk e rs (W irth & B em atchez_2003) a re p ro v id e d , a lo n g w ith th e la titu d in a l d is ta n c e se p a ra tin g localities. S am p le ab b re v ia tio n s a re as
ín d ic a te d in Table 1
N o. o f N o . o f M ea n o u tlie r Fsr L a titu d in a l
S am p le p a ir p o ly m o rp h ic loci o u tlie r loci v a iu e (m in Fgj — m ax fgy) X rim m ed Fgj N e u tra l fST d is tan ce (deg ree)
Anguilla rostrata
M E vs. BO 311 5 0.2089 (0.1646-0.2584) 0.0061 -0 .0005 1.75
M E vs. W Y 304 8 0.1978 (0.0920-0.3068) 0.0018 0.0034 5.20
M E vs. SJ 299 5 0.1504 (0.0812-0.2584) -0 .0004 0.0005 14.18
BO v s. W Y 295 5 0.2777 (0.0678-0.4086) 0.0011 -0 .0008 3.45
BO vs. SJ 304 3 0.2418 (0.1752-0.2888) 0.0067 -0 .0016 12.43
W Y vs. SJ 301 8 0.1627 (0.0679-0.2867) 0.0015 0.0037 8.98
A nguilla anguilla
IC vs. EL 291 13 0.3381 (0.1423-0.6496) 0.0102 0.0016 9.70
IC vs. G L 291 9 0.2537 (0.1399-0.4388) 0.0110 -0 .0009 17.48
IC vs. M I 293 12 0.2460 (0.0902-0.4344) 0.0018 -0 .0008 22.70
IC vs. M O 303 7 0.2747 (0.1557-0.5605) 0.0054 0.0011 29.40
EL vs. GL 300 4 0.1767 (0.1355-0.2685) 0.0030 0.0003 7.78
EL vs. M I 305 9 0.2127 (0.0912-0.2773) 0.0032 0.0016 13.00
E L v s .M O 311 7 0.2813 (0.1208-0.4405) 0.0058 0.0017 19.70
G L vs. M I 294 2 0.1863 (0.1658-0.2068) -0 .0012 0.0005 5.22
G L vs. M O 295 4 0.1480 (0.1116-0.1700) -0 .0003 0.0007 11.92
M I vs. M O 300 0 — -0.0041 0.0024 6.70
procedure. Likelihood functions were constructed following
the method described in Rogers et al. (2001), and hybrid
indices as well as their support (two log-likelihood units)
were determined under the likelihood framework using
r software ( r Development Core Team 2004). The joint
estimate of hybrid index over all Icelandic individuals
was therv used to calculate theoretical allele frequencies
in the introgressed population of Iceland. For each locus,
the deviation of observed frequencies from theoretical
expectations was used to detect the possible influence of
directional selection.
Correlation tests
Because the pattem of an AFLP locus consists of binary
data, we used binomial logistic regression to test correlations
between genotypes and other explanatory factors. We
tested for the influence of the categorical factor 'life stage'
(glass eel or yellow eel stage) and the continuous factors
'body length' and 'sample latitude' using r ( r Development
Core Team 2004). Yellow eel body length was considered as
a rough surrogate for individual age.
R esults
Intraspecific outlíer detection
Trimmed FST values were close to zero in each of the six
pairwise comparisons performed between Anguilla rostrata
samples (Table 2). Outliers were detected in each comparison,
and showed pairwise Fsx values ranging from 0.068 to 0.409
whereas neutral loci Fst ranged between -0.038 and 0.211
(Fig. 1). A total of 22 out of 325 polymorphic loci were
outliers in at least one comparison, five of them were
detected in two pairs of samples and three were involved
in more than two pairwise comparisons. Among these, loci
L65 and L260 were detected as outliers in all comparisons
involving the Wye River and Medomak River samples,
respectively, whereas locus L179 was the only outlier to
appear in comparisons between pairs that did not involve
a sample in common (Fig. 1).
Low pairwise trimmed Fsx values calculated between
A. anguilla samples revealed very weak neutral differen-
tiation throughout the European eel distribution range
(Table 2). Outliers were detected in every pairwise com-
parison except between Minho River and Moulouya
Oued (Fig. 2). Fsx values at outlying loci ranged from
0.090 to 0.650, whereas neutral loci showed Fsx values
ranging from -0.038 to 0.277. Nine out of the 334 poly-
morphic loci were outliers in one of the 10 pairwise com-
parisons performed, whereas seven were detected in two
different pairs (Fig. 2). Among the six loci that were associ-
ated with a particular sample in more than two comparisons,
five were associated with Iceland (L144, L278, L306, L337
and L372) and one with Elbe station (L22). Five other loci
involved in more than two comparisons also appeared
in independent sample pairs (Lll, L17, L32, L69 and L368)
(Fig-2).
© 2009 B lackw ell P u b lish in g L td
N A T U R A L S E L E C T I O N F O O T P R I N T S IN A T L A N T I C EELS 1683
o
CQ
'S l ^
L65
O 6
l l l l
Mí i.ií) \\ Y s,i
L179
n
ML IK! W Y Si
362
L260
i
- ■ 1 ■
VII. IK! W V SJ
GO
rt c c O ' («_
M E BO
Heterozygosity
W Y
Fig . 1 R esu lts o f D fd is t a n a ly se s fo r A nguilla rostrata in trasp ec ific c o m p a riso n s . ^ST vs. h e te ro z y g o s ity p lo t is p ro v id e d fo r e ac h p a irw ise
c o m b in a tio n o f sam p les . O p e n c irc les re p re s e n t n e u tra l loci fa llin g b e lo w th e 0.995 q u a n ti le 's b ro a d line , w h e re a s c a n d id a te loci xm der
d iv e rg e n t se lec tio n a re re p re s e n te d b y b la c k c ircles a cc o m p a n ie d b y th e lo cu s n u m b er. L ow er a n d m id d le lin e s in each p lo t, respectively ,
re p re sen t th e 0.005 q u a n tile a n d m e a n Fsl- v a lu e o v e r th e ra n g e o f he te rozygosity . F ram es a t th e u p p e r r ig h t c o n ta in b a rp lo ts s h o w in g
d o m in a n t a lle le fre q u en c y in e ac h lo ca lity fo r th e th re e o u tlie r loci d e te c te d in m o re th a n tw o s am p le p a irs .
A significant positive correlation was found between
latitudinal distance separating European localities and the
number of outliers in the corresponding pairwise compar-
isons (Spearman's p = 0.57, P = 0.04). This correlation was
more obvious when Iceland was excluded (Spearman's
p = 0.90, P = 0.01). Moreover, there was a significant
positive correlation between trimmed ^st values and the
number of outliers found in pairwise comparisons between
A. anguilla localities (Spearman's p = 0.72, P = 0.009), which
was also more obvious after withdrawing Iceland (Spear-
man's rho = 0.93, P = 0.004). No such correlation could be
found when applying these tests in A. rostrata. No outlier
among the 22 foimd between A. rostrata samples and the 27
between A. anguílla samples was detected as intraspecilic
outlier in both species.
Interspecific outlier detection
The interspecific comparison had a trimmed FST value of
0.0685. A total of 27 out of 321 (8.4%) polymorphic loci
were identified as outliers in this analysis (Fig. 3). Three
were also identified as A. rostrata intraspecific outliers
(L243, L263 and L370) and four as intraspecific outliers in
A. anguilla (L6 , L278, L368 and L372). In this last case, Iceland
was always involved in the intraspecific comparisons in
which these outliers were detected.
Locus specific introgression level
The determination of individual hybrid status with
NewHybrids revealed the occurrence of 33 F„ 8 F2, and 38
© 2009 B lackw ell P u b lish in g L td
1684 P. A. G A G N A I R E E T A L .
—
tH
o
Lll
ÍC
L17
■ I I I I
L69
L22
I ■
L144
I I I I
L306
. I I I I
K* íil. Ol. \li MC>
L32
L278
L337
L368
. I I I I
L372
I I I I
EL GL
Heterozygozity
Fig. 2 R esu lts o f D fd is t a n a ly se s fo r A nguilla anguilla in trasp ec ific co m p ariso n s. P lo ts w e re c o n s tru c ted a s in Fig. 1, fo r e v e ry p a irw is e
c o m p a riso n in th e E u ro p e a n eel. F ram es a t th e u p p e r r ig h t c o n ta in b a rp lo ts s h o w in g d o m in a n t a lle le freq u e n c y in e a c h lo ca lity fo r th e 11
o u tlie r loci d e te c te d in a t le a s t th re e s a m p le p a irs .
BCAan individuals with a posteríor probability greater than
70% (Table 1). At the 50% posterior probability level, 11
individuals were identified as F2 hybrids. No BCAr0
indivídual was found in the samples. Results of binomial
tests between allele frequencies estimated in each of the
three hybrid categories detected, and the corresponding
theoretical frequencies calculated from parental sources,
are shown in Fig. 4a for F„ 4b for F2 and 4c for BCAan hybrid
categories. Seven loci showed cumulatively a bias towards
A. rostrata parental frequencies in at least one hybrid
category and an outlying behaviour in the interspecific
comparison. Among them, loci L6 , L368 and L372 were
also outliers in pure A. anguilla intraspecific comparisons
involving Iceland. On the other hand, the interspecific
outlier locus L236 showed a strong bias towards A. anguilla
parental frequencies in each hybrid category.
Maximum-likelihood estimates ofhybrid indices
After removal of loci that showed less than 1% frequency
difference between A. rostrata and A. anguilla pooled samples,
303 loci out of 373 were retained to estimate hybrid indices.
Differences between dominant (presence of AFLP band)
allele frequencies of parental samples ranged from 1 to
98%. Based on these loci, the joint maximum-likelihood
estimate of hybrid index over all Icelandic individuals was
0.135 (two units of support: 0.129-0.140). This reconfirmed
that individual genetic composition most likely originated
© 2009 B lackw ell P u b lish in g L td
N A T U R A L S E L E C T I O N F O O T P R I N T S IN A T L A N T I C EELS 1685
H e te ro z y g o s i ty
Fig . 3 R esu lts o f D fd is t a n a ly s is fo r in te rs p e c if ic c o m p a r is o n ,
sh o w in g o u tlie r c a n d id a te loci fo r d iv e rg e n t se lec tio n b e tw e e n th e
tw o A tlan tic eel spec ies.
from A. anguilla, but that Icelandic eels were introgressed
by A. rostrata, as reported by Albert et al. (2006). The distribu-
tion of locus frequency deviation from theoretical expectations
using this 0.135 joint hybrid index is presented in Fig. 5.
With the exception of locus L192, all loci that significantly
deviated from theoretical frequencies in at least one hybrid
category (Fig. 4) showed the same deviation direction
with the hybrid index approach (Fig. 5). Setting a 95%
threshold to detect loci that departed the most from
neutral expectatíons at both extremities of the distribution
allowed us to refine the identification of markers potentially
under selection. Five loci showed an overrepresentation
of European alleles, and among these, three were detected
to significantly deviate from theoretical frequencies in at
Fig . 4 T h ree -d im en s io n a l p lo ts sh o w in g th e re su lts o f locus
d e v ia tio n te s ts in h y b r id c a tego ries . In e ac h p lo t, th e g rey -co lo u red
sq u a re d su rface s h o w s th e th e o re tic a l p ro b a b ility o f o b se rv in g th e
d o m in a n t m a rk e r a s a fu n c tio n o f b a n d p re sen c e f req u en cy in each
p a re n ta l spec ies. F o r e ac h locus, th e d iffe ren ce b e tw e e n o b se rv ed
a n d th eo re tic a l f req u en cy o f b a n d p re sen c e w a s re p re s e n te d (on ly
if s ign ifican t) b y a v e rtic a l lin e jo in in g th e lo cu s co o rd in a te s to its
p ro jec tion o n th e theo re tical su rface. Vertical lines w e re red -co lou red
w h e n loca lized a b o v e th e su rface a n d b lu e -co lo u re d w h e n localized
u n d e r. Loci w e re re p re s e n te d b y p o in ts w h o s e s ize in d ic a ted if
th e y w e re in te r s p e c if ic o u t l ie r s ( la rg e p o in ts a c c o m p a n ie d b y
Iocus n u m b e r) o r n o t (sm all p o in ts ). T h e co lo u r o f a p o in t w as
y e llo w w h e n b a n d fre q u e n c y w a s b ia se d to w a rd s A nguilla anguilla
p a re n ta l f r e q u e n c y a n d g re e n w h e n b ia s e d to w a rd s A . rostrata.
Loci w h o s e d e v ia t io n w a s s till s ig n if ic a n t a f te r B o n fe rro n i
co rrec tio n h a d a b ro a d e r d e v ia tio n lin e a n d th e ir id e n tify in g
n u m b e r w a s la b e lled w ith a l ig h t b ro w n tag . R esu lts a re p ro v id e d
in s e p a ra te p lo ts fo r e a c h h y b r id c a te g o ry o b ta in e d w ith
N e w H y b rid s : F, (4a), F2 (4b) a n d BCAan (4c).
0.2
BaW'áfteq'ietlcV
imríMTninj
© 2009 B lackw ell P u b lish in g L td
1686 P. A. G A G N A I R E E T A L .
co
-2 ö
L o ci ordered b y deviation value
Fig . 5 D e v ia tio n o f o b se rv e d m a rk e r freq u en c ie s from th eo re tic a l e x p ec ta tio n s g ív e n th e 0.135 e s tim a te d h y b r íd in d ex o v e r a ll in d iv id u a ls ,
fo r th e w h o le Ic e la n d ic s a m p le u s in g p o ly m o r p h ic loc i. D e v ia t io n v a lu e s a re re p re s e n te d b y b la c k h is to g r a m s o rd e re d f ro m loci
ch a rac te riz e d b y a n alle lic c o m p o s itio n o f A nguilla rostrata (n eg a tiv e d ev ia tio n ) to A . anguilla o rig in (p o s itiv e d e v ia tio n ). Loci th a t sh o w ed
s ig n ific an t d e v ia tio n a f te r B on fe rro n i co rrec tio n in a t le a s t o n e h y b r id ca teg o ry (Fig. 4) w e re la b e lled w ith th e ir id e n tific a tio n n u m b er. This
n u m b e r is fo llo w e d b y a b lack c ircle if th e lo cu s w a s a lso a n in te rsp ec ífic o u tlie r, a n d / o r a n o p e n c irc le if th e lo cu s w a s a lso a n in traspecific
o u tlie r in a t le a s t tw o p a írw is e c o m p a ris o n s in v o lv in g Ice land . T h e tw o h o riz o n ta l lines d e lim it loci w h o se a b so lu te d e v ia tio n v a lu e
ex ceed ed th e o n e -s id ed 95% c o n fid en c e in te rv a l fo r th e d is tr ib u tio n o f loci d e v ia tio n 's a b so lu te va lue .
least one hybrid category. The locus L236, which showed
highly reduced introgression pattern in each hybrid
category, was in the A. anguilla part of the distribution, but
its deviation value did not exceed the 95% threshold. Eleven
loci showing allele frequencies biased towards the
American eel composition were outside the one-sided
95% confidence interval. Among these, five markers were
already detected in deviation tests performed with hybrid
categories. Moreover, loci L6 , L368 and L372, which were
outliers at the interspecific level, and in pure A anguilla
intraspecific comparisons involving Iceland, were all
located in this A. rostrata distribution extreme.
Correlations between locus band patterns and explanatory
factors in Iceland
Marker states at loci L6 , L368 and L372 were also associated
wíth the life stage categorical factor in Iceland (Table 3).
For each of these three loci, the frequency of the A. rostrata
allele showed a significant increase from the glass eel to the
yellow eel stage. Moreover, a significant positive correlation
was detected with the body length of parental Icelandic
yellow eels for loci L6 and L368. In addition, dominant
allele frequency at locus L278 was significantly correlated
with the latitude of Icelandic sampling locations. Because
these correlations could be explained either by an increase
in a sample's hybrid proportion with latitude or the
transition from glass eel to yellow eel stage (Albert et al.
2006), the same tests were also performed after withdrawal
of all hybrid categories. Significant relationships were still
detected with pure Icelandic A. anguilla only (Table 3).
D iscu ssion
The present study aimed to document the possible influence
of natural selection on patterns of genetic diversity in
Atlantic eels. More specifically, we tested if (i) intra and
interspecífic genetic variation were influenced by direc-
tional selection, and if (ii) interspecific hybrids frequencies
could be related to differential survival in Icelandic rivers.
We first found candidate loci for directional selection
within both species. In Anguilla rostrata, the spatial distri-
butions of allelic frequencies displayed by some of these
loci were possibly related with the geographical patterns of
life-history traits (see below). We also identified a positive
correlation between the number of outlier loci and the
estimate of neutral differentiation, as well as the latitudinal
distance in A. anguilla. Second, we found outlier loci at the
interspecific level. Non-neutral introgression was also
suggested for some loci. Namely, we detected a locus at
© 2009 B lackw ell P u b lish in g L td
N A T U R A L S E L E C T I O N F O O T P R I N T S IN A T L A N T I C EELS 1687
T a b le 3 R esu lts of log is tic re g re ss io n s th a t re v e a led s ig n ific a n t re ia tio n sh ip s b e tw e e n alle lic c o m p o s itio n a t a g iv en lo cu s a n d e ith e r
catego rica l (life s tag e ) o r c o n tin u o u s v a ria b le s (b o d y le n g th a n d s a m p le ia titu d e ). C o rre la tio n s w ith th e life -stag e fac to r w e re te s te d u s in g
d a ta fro m th e fo u r Ice lan d ic lo ca litie s fo r w lú c h g lass e els a n d y e llo w eels w e re b o th availab le . T h ese loca lities w e re V o g slæ k u r (VO), Seljar
(SE), V ífilss tad av a tn (VI) a n d S to k k sey ri (ST) (see A p p e n d ix S l) . C o rre la tio n s w ith b o d y le n g th a n d s am p le ía titu d e w e re te s ted o n all
Ice lan d ic lo ca litie s . S a m p le s c o n s is te d of a ll th e in d iv id u a ls a v a ila b ie fo r th e lo c a litíe s c o n s id e re d (P u re + h y b r id s ) , o r w e re re s tr ic te d
to in d iv id u a ls id e n tif ie d a s p u re A . anguilla (P u re on ly ), o r to p u re E u ro p ea n y e llo w eels (P u re y e llo w on ly ). T h e P -v a lu e is p ro v id e d fo r
e ac h te st
L ocus id e n tify in g n o . F a c to r te s te d L ocalities a n a ly se d In d iv id u a ls a n a ly se d P v a lu e
L6 Life s tag e V O + SE + VI + ST P u re + h y b r id s 1.27 x lO "9
P u re o n ly 4.07 x ÍO '7
B ody le n g th A ll Ice land ic P u re y e llo w o n ly 7.72 x lO -3
L368 Life s tag e V O + SE + V I + ST P u re + h y b r id s 1.23 x lO "7
P u re o n ly 1.59 x K T 3
B ody le n g th AIl Ice land ic P u re y e llo w o n ly 3.27 x 10-5
L372 L ife s tag e V O + SE + V I + ST P u re + h y b r id s 6.60 x 10-9
P u re o n ly 8.56 x 10"8
B ody le n g th A ll Ice land ic P u re y e llo w o n ly 1 .0 8 x 1 0 - '
L278 S am p le la titu d e A ll Ice land ic P u re + h y b r id s 6.20 x ÍCT12
P u re on ly 2.36 x 10“7
which the typical A. rostrata allele hardly crossed the
species genetic barrier, whereas three other loci showed
accelerated patterns of introgression into A. anguilla in
Iceland. Moreover, the level of introgression at these three
loci increased from the glass eel to the yellow eel stage. We
discuss the evolutionary consequences of hybridization in
Atlantic eels in the light of these results.
Local differentiation at the species level; evidencefor one
generation selection footprint?
Regarding the large number of locí studied in a genome
scan, one important issue of outlier detection is to deal with
type I errors generating false positives. In our case, given
the 0.995 threshold used to detect loci under directional
selection, we expected 373 * 0.005 or approximately two loci
to be detected as outliers only by chance in each comparison.
However, the method of Beaumont & Balding (2004)
performs a false-positive correction to avoid this issue.
Furthermore, our study at the species level involved multiple
pairwise comparisons. We could therefore identify outlier
loci involved in multiple comparisons, further reducing
the likelihood of type I error.
We detected in each species outlier loci that were asso-
ciated with a particular sample in at least three different
pairwise comparisons. Allele frequencies at these markers
could have been shaped by locality-specific selective
forces. Unfortunately, in the absence of detailed environ-
mental data conceming factors that could play a selective
role, no correlation could be examíned between outlier
locus frequencies and ecological variables. However,
geographical patterns in life-history traits can provide a
first basis to propose hypothetical explanations for such
associations, and set the stage for future research on the
role of natural selection in shaping genetic variation
observed in eels. Of course, these must be considered as
exploratory. For instance, the A. rostrata glass eel phase
duration is longer and characterized by a slower growth
rate in northern localities than in the south (WangJyTzeng
1998). This latitudinal variation was interpreted as a con-
sequence of coastal water temperature that could influence
the speed of glass eels' development. If temperature controls
such a vital trait, it could also affect glass eels' mortality,
hence providing a basis for differential selection. Atlantic
Ocean surface temperatures near North America coasts
show that the influence of the warm Gulf Stream water
masses does not extend to the north of Boston (see Wirth &
Bematchez 2003 for a map). This raises the hypothesis that
AFLP markers, such as L260 that showed unusually high
Fsx values in all three comparisons involving the northern-
most Medomak River, could be candidate for selection by
temperature in A. rostrata.
In A. anguilla, five loei showed unusually high Fsx values
in at least three different pairwise comparisons when
Iceland was compared with European samples (L144, L278,
L306, L337 and L372). Icelandic eels are likely to be charac-
terized by some particular traits because they are supposed
to have a shorter migration and experience unique ecolo-
gical conditions during their continental growth compared
to their Europeancongeners (Albertet«I./006). Therefore,
it was not surprising to find five Iceland-specific outliers
among a total of six locality-specific outliers in the European
eel. This result supported that the outlier behaviour of
such loci was probably related with the existence of
selective factors that exclusively operate in the 'outlying
locality'.
In both species, some outlier loci were also involved
between independent sample pairs, possibly indicating
© 2009 B lackw ell P u b lish in g L td
1688 P. A. G A G N A I R E E T A L .
that some selective factors could influence genetic variation
on broader geographical scales. This was particularly the
case in A. anguilla, where a significant positive correlation
between latitudinal distance separating European localities
and the number of outliers in pairwise comparisons was
observed. Due to genetic linkage between genes responsible
for local adaptation and some neutral loci, theory also
predicts that natural selection could facilitate neutral
genetic differentiation via genetic hitchhiking (Charlesworth
etal. 1997). This was supported by the positive correlation
between trimmed FST values and the number of outliers
found in pairwise comparisons between A. anguilla localities.
This raised the hypothesis that the weak albeit significant
neutral genetic differentiation previously reported in the
European eel (Daemen et al. 2001; Wirth & Bematchez 2001,
2003; Maes & Volckaert 2002) could be indirectly induced
by natural selection associated with a latitudinal environ-
mental gradient along the European coasts. What was
previously described as an 'isolation-by-distance' pattern
could therefore be interpreted as an 'isolation-by-adaptation'
footprint (Nosil etal. 2008). However, both processes are
not necessarily exclusive. Clearly, a more thorough test
of the hypothesis of isolation-by-adaptation as a single
generation process will need a wider sampling coverage,
and the use of a meaningful set of ecological variables
instead of latitude alone in order to identify causal agents
of selection.
Genetic architecture ofthe species barrier
Natural hybridization between Atlantic eels in Iceland
provided an opportunity to study the architecture of puta-
tive genetic barriers between A. rostrata and A. anguilla.
Depending on the number of genomic regions involved in
reproductive isolation, and on their distribution throughout
the genome, the permeability of hybrid zones to gene flow
can be highly variable (Barton & Hewitt 1985; Kim &
Rieseberg 1999; Wu 2001). The AFLP genome-scan approach
is a way to concomitantly assess the proportion of loci
that flow more or less freely between species and that
of 'speciation loci' that hardly cross the species barrier, and
are therefore characterized by introgression delays or
segregation distortions in hybrids. Most of the following
interpretations conceming the different pattems of intro-
gression found at interspedfic outlier loci rely on the hypothesis
that each species consists of a panmictic or quasi-panmictic
pool of individuals. Iceland was also assumed to consist of
a mixture of pure European eels and various hybrid crosses,
among which F„ F2 and BCAajrl were probabilistically
categorized using NewHybrids. Although the panmictic
status of each species is still debated, these assumptions
seem reasonable considering the very low levels of intras-
pecific genetic differentiation evidenced in a previous
study (Wirth & Bematchez 2003).
The low interspecific trimmed FST value of 0.06 found
between pooled continental samples (i.e. without Iceland)
was close to the previous neutral differentiation level
found with microsatellite markers (0.007-0.040, Wirth &
Bematchez 2003), and indicated either a recent co-ancestry,
shared ancestral polymorphism, or a significant level of
introgression. Overall, individual admixture proportions
determined with Structure (Pritchard et al. 2000) in Albert
et al. (2006), along with the present NewHybrids results,
and the 0.135 overall hybrid index found in Iceland, sup-
ported the existence of asymmetrical genetic introgression
from A. rostrata towards A. anguilla. Therefore, the European
eel's genome seems permeable to the inflow of genes from
the American eel. On the other hand, gene flow between
species appeared strongly reduced at some AFLP loci after
comparison between pooled continental samples. The 8.4%
of outlier loci detected between Atlantic eel species was
consistently within the 1.5-15.1% range of outliers docu-
mented between closely related species in previous studies
(Campbell & Bematchez 2004; Scotti-Saintagne et ál. 2004;
Savolainen et ál. 2006; Rogers & Bernatchez 2007; Minder &
Widmer 2008). Among the 27 interspecific outliers iden-
tified, the study of deviation from theoretical frequencies
in Icelandic hybrid categories revealed three contrasting
locus behaviours. First, in Iceland, five loci showed a
strong bias towards parental A. anguilla allelic frequencies.
Among these, only locus L236 still significantly deviated
from theoretical frequencies after Bonferroni correction.
This deviation was observed in each hybrid category, and
systematically corresponded to the strongest introgression
delay of A. rostrata allele into A. anguilla genome among all
markers. Locus L236 is therefore potentially linked with a
genomic region undergoing diverging selection between
both eel species, or perhaps involved in Dobzhansky-
Muller incompatibilities inducing hybrid inferiority (Burke
& Amold 2001). Second, nine interspecific outliers were in
conformity with expected allele frequencies in each hybrid
category, and only showed moderate departures from
neutral expectations using the hybrid index approach.
Some of these loci could have been identified by type I
errors, as they were not located far above the 0.995 quantile
in the single interspecific comparison made for outlier
detection. Type I error was however, improbable for three
other loci showing a clear interspecific outlying behaviour
(L78, L263 and L353). Conformity with theoretical expec-
tations in hybrid categories and in the whole Icelandic
sample rather suggested that allelic combinations at these
loci did not have a strong influence on hybrid fitness. The
interspecific outlier behaviour of such loci may therefore
be best explained by divergent selection between parental
species unaffecting hybrid fitness. Third, the 13 remaining
loci were all distinguished by allelic frequencies biased
towards A. rostrata, exceeding neutral expectations in at
least one hybrid category. Among the seven markers that
© 2009 B lackw ell P u b lish in g L td
N A T U R A L S E L E C T I O N F O O T P R I N T S IN A T L A N T I C EELS 1689
still significantly deviated after Bonferroni correction, loci
L6 , L368 and L372 also fell outside the 95% confidence
interval defined in the hybrid index approach, suggesting
that they were undergoing positive selection in Iceland.
Because the overrepresentation of A. rostrata alleles at these
loci was also independently observed in hybrids and pure
Icelandic A. anguilla, an Iceland-specific selective factor
favouring A. rostrata's alleles in Iceland best explains accel-
erated introgression at these markers (see below).
On the basis of the behaviour of loci studied at different
scales, two main mechanisms may be invoked for shaping
the pattems of differential introgression at different markers
between Atlantíc eel species. Asymmetrical genetic intro-
gression from A. rostrata to A. anguilla was already demon-
strated (Albert et al. 2006), but here we found some loci with
accelerated rates of introgression in Iceland. Hybridization
could thus allow genetic segments carrying neutral but
also locally favourable genes to cross the genetic barrier
between species. In the face of introgression, genetic
swamping would tend to homogenize the genetic com-
position of the two species, but loci under divergent selection,
or potentially involved in endogenous incompatibilities
such as L236 could maintain separation of some genomic
regions among species. The fact that these regions appeared
at low density compared to neutrally flowing loci in this
genome scan suggests that the genetic barrier between
Atlantic eel species may be very porous (Wu 2001).
Adaptive consequences ofhybridization between
Atlantic eels
The Iceland-limited occurrence of hybrids was proposed
to rely on their intermediate larval behavíour and/or
development compared to purebreds (discussed in Albert
et al. 2006). Because of its geographical localization at
mid-distance between North America and Europe and its
ecological uniqueness compared to the European core
habitat, Iceland can also be considered a marginal habitat
of the European eel natural distribution. The restricted
distribution of hybrids could indicate that they have higher
survival in this habitat compared to purebreds (Albert et al.
2006). Contrasted performance between purebreds and
hybrids regarding habitat ecology have been proposed in
the alpine sedge Carex curvula, which maintained its gen-
otype integrity in optimal habitats but showed high levels
of introgression at ecological margins (Choler_efal.
2004). In that study, correlation between pattems of geno-
typic distribution and ecological conditions suggested
that genetic introgression could be a way to widen this
species' niche. In such a case, allospecific genes possibly
responsible for local adaptation in marginal habitats should
introgress more rapidly than any other allospecific neutral
gene via introgressive hybridization. Indeed, differential
survival is supposed to favour individuals carrying these
introgressed-adapted alleles, but should have a random
effect on urdinked neutral genes. Loci L6 , L368 and L372
are good candidates for such adaptive introgression
induced by positive selection, because their allelic com-
positions were strongly biased towards A. rostrata frequen-
cies in Iceland. Moreover, the increase in introgression level
observed at these loci during continental growth (i.e. at
transition from glass to yellow eel, and during yellow eel
growth for L6 and L368) indicated that allelic frequencies
changed during the continental phase. The fact that this
temporal enrichment in A. rostrata's alleles was not observed
at other loci is not compatible with the hypothesis that it
reflects a temporal decrease in the introgression rate, because
this should also have affected other loci. A segregatíon
distortíon induced by co-adapted gene complexes or a
spatio-temporal variation in hybrids' proportíon could
neither be invoked, because the same significant variations
in allelic frequencies were also found with pure Icelandic
A. anguilla individuals. Consequently, we propose that our
results reflect the existence of ecological factors driving
differential survival in Iceland in favour of introgressed
individuals at loci L6 , L368 and L372. Moreover, a latitudinal
gradient of selection associated with such ecological factors
providing an advantage for introgressed individuals at
hígh latitudes could also explain the latitudinal increase
in the proportion of hybrids towards the North of Iceland
(Albert et al. 2006). Although these ecologícal factors still
remain to be identified, temperature would be a logical
candidate to investigate in future studies.
It is notoriously difficult to provide evidence for adaptive
introgression in natural surveys, because positively selected
alleles are predicted to rapidly fix in the introgressed
population (Bartoxy2001). However, the case of Atlantic
eels could be particularly useful in this respect, because of
the very high levels of neutral gene flow observed at the
species scale. The panmixia hypothesis assumes that within
each species, alleles are randomly exchanged between
individuals at each generation, independent of their
continental origin. Therefore, larval pools that recruit at
different continental locations should not differ in their
allelic composition when starting to disperse from the
spawning area. As larval transport by the Gulf Stream is
likely to be an additional source of genetic homogenization
during dispersal, only oceanic selection could differentially
shape genetic variation among pools of recruiting larvae.
The eventual footprint of positive selection observed in
Iceland could therefore correspond to a single generation
process.
Conclusions and perspectives for future research
This genome scan provided evidence that both intraspecific
and interspecific genetic diversity are influenced by natural
selection in Atlantic eels. Genetic differentiation pattems
© 2009 B lackw ell P u b lish in g L td
1690 P. A. G A G N A I R E E T A L .
found at the species scale suggested that differential
mortality associated with local conditions where young eel
settle could indirectly shape neutral genetic variation via
genetic linkage with loci under selection. Hence, the nature
of genetic variation in Atlantic eels could be not only
spatial or temporal, but also ecological. In order to provide
a better understanding of some novel aspects raised in this
study, a genome-wide functional single nucleotide poly-
morphism (SNP) scan could enable fhe identification of coding
genes under potential selection following preliminary
efforts to increase SNP discovery (Namroud et al. 2008).
Wood et al. (2008) also recently showed that potentially
selected regions can fall outside coding sequences, and that
BAC library screening was an appropriate way to follow
up an AFLP genome scan. Such markers and approaches
could be applied towards further investigating the effect of
natural selection on changes of allele frequencies at putative
'adaptive genes' throughout the eel's complex life cycle.
Namely, the comparison between leptocephali of different
ages could help in understanding the impact of selection
on genetic variation in the marine environment, whereas
the analysis of glass and yellow eels would provide
information on selection operating in continental waters,
and as such, enable estimation of the nature and relative
importance of selection operating either in the marine or
continental environments.
A cknow ledgem ents
W e a c k n o w le d g e s u b je c t e d i to r H . E lle g re n , tw o a n o n y m o u s
re fe rees, a s w e ll as P. B erreb i a n d A . W h ite ley fo r th e ir h e lp fu l
c o m m e n ts o n th e m a n u s c r ip t . T h is re s e a rc h w a s s u p p o r te d b y
a g ra n t fro m Science a n d E n g in ee rin g R esearch C an a d a (NSERC,
D isco v e ry g ra n t p ro g ra m ) a s w e ll a s a C a n a d ia n R e sea rch C h a ir
to L.B.
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© 2009 B lackw ell P u b lish in g L td
Environmental Biology o f Fishes (2007) 78:189-192
DOI 10.1007/s 10641-005-1367-9
© Springer 2006
Effects of water temperature on the swimming and climbing behaviour
of glass eels, Anguilla spp.
Elizabeth D. L intona'c, Bjarni Jónssona,b, & David L.G. N oakesa~d
aDeparíment of Zoology and Axelrod Institute of Ichthyology, University of Guelph, NIG 2WI, Guelph,
Ontario, Canada (e-mail: bjarni.jonsson@veidimal.is)
bInstitute of Freshwater Fisheries at Hólar, 551, Hólar, Saudárkrókur, Iceland
LDillon Consulting, 5 Cherry Blossom Road, Unit I , N3H 4R7, Camhridge, Ontario, Canada
‘'Current. address: Department of Fisheries & Wildlife, Oregon Hatchery Research Center, Oregon State
University, Corvallis, Oregon, 97331-3803 USA
Received 8 January 2005 Accepted 13 July 2005
Key words: tem perature, m igration, marine, freshwater, Iceland
Synopsis
We used controlled laboratory experiments to test the hypothesis that glass eels, Anguilla spp., display
distinct locom otion behaviour patterns at different water temperatures. The threshold and peak temper-
atures for active swimming were lower than those for vertical climbing. These differences in threshold and
peak tem peratures for swimming and climbing behaviour correspond to field observations on these eels
entering freshwater rivers in Iceland. The differences in threshold and peak tem peratures account for the
observations that glass eels first swim into freshwater and then later begin upstream movement over
waterfalls or other barriers.
Introduction
The life cycle o f freshwater eels, Anguilla species, is
one of the most complex o f any fish species. One of
the most striking parts o f this life cycle is the
complex transition of the marine leptocephalus
larva to the freshwater glass eel (Aida et al. 2003).
Among many other changes, this involves the ini-
tiation of active swimming and vertical climbing
behaviour o f the glass eels into freshwater rivers
and streams. W ater tem perature is arguably the
chief environmental variable governing the peri-
odicity and magnitude o f upstream eel migration
within brackish and freshwater systems (M artin
1995. White & Knights 1997). Field studies com-
monly report the threshold tem perature at which
inland movement is initiated and the tem perature
at which peak m igration occurs (Gandolfi et al.
1984, W hite & Knights 1997), whereas laboratory
experiments have largely focused on thermal
preference tests (Barila & Stauffer 1980, Tosi et al.
1990, Chen & Chen 1991). No study has investi-
gated the different activities o f glass eels during
their upstream migration.
We collected glass eels below the waterfall
(1.5 m high, 5 m wide) at the m outh o f the River
Vogslækur, Iceland (6 4 ° 3 0 'N , 22° W), which is
within the tide line from the Atlantic Ocean. When
the water tem perature was between 6.9 and 11.8°C
we captured glass eels only close to the substrate
and we did not observe any eels swimming or
crawling up the cliffs of the waterfall. At temper-
atures between 13.0 and 17.6°C, we caught glass
eels swimming near the surface o f the water or
mailto:bjarni.jonsson@veidimal.is
190
climbing up the waterfall’s cliffs but did not cap-
ture any near the substrate. These field observa-
tions lead us to form ulate the hypothesis that
increasing water tem peratures in the spring and
summer were responsible for the upstream migra-
tion o f the glass eels. We predicted that swimming
behaviour would be initiated at a lower tempera-
ture than would vertical climbing behaviour, once
the initial threshold for activity was passed.
Materials and methods
W e tested our field-generated hypothesis that glass
eels display dístinct behaviour patterns at different
water tem peratures by observing glass eels under
controlled conditions. We captured glass eels,
Anguilla spp., for our experiments (total length
6.8 ± 0.03 cm; m eandtSE) below the aforemen-
tioned waterfall between 30 June and 3 July 2000,
during m orning and evening high tides. W ater
tem peratures during capture ranged between 10
and 18°C. Iceland is the only location where both
European eel, Anguilla anguilla (Linnaeus), and
American eel, A. rostrata (LeSueur), and possibly
their hybrids, with the are sympatric in freshwater.
F rom m t D N A study, it is estimated that
approxim ately 95% of the individuals entering the
River Vogslækur are o f A. anguilla origin and 5%
are A. rostrata type (Jónsson & Noakes 2001,
Kawai 2001). We did not attem pt to differentiate
between species in our study, as there was no
indication of behavioural differences at this life
stage. We held eels in 401 tanks in 18-20°C
dechlorinated water for 2 - 3 weeks at the ínstitute
o f Freshwater Fisheries at H ólar under the natural
Icelandic summer photoperiod (24L: 0D). We
changed holding water daily and did not feed eels
until experiments were complete. There was no
m ortality or m orbidity in the eels during holding
or experimentation.
We performed two laboratory experiments to
assess the influence o f tem perature on the swim-
ming and climbing activities o f glass eels. For all
trials, we randomly selected 28 - 30 glass eels from
the holding tank at approxim ately the same time
each day and transferred them to a glass aquarium
(46 x 31x35 cm) containing dechlorinated water
o f the designated tem perature. Eels were accli-
m ated for 30 min prior to experimentation, with
the exception that an additional 40-min acclima-
tion period at 7°C preceeding acclimation at 4°C.
N o specimen was used for more than one trial. The
sampling location was simulated by providing a
running water stimulus and lining the bottom of
the aquarium with a m onolayer o f flat stones.
We recorded swimming activity at 4, 7, 12, 17,
22 and 25°C (± 0 .5 °C for each tem perature) for
1.75 h (Panasonic S-VHS video camera). A sub-
mersible pum p drew water in at its base and dis-
charged it above the water level in the aquarium at
a rate of 5.3 1 m in“ ' to provide the running water
stimulus. We made eight point counts of the
num ber o f glass eels swimming above the substrate
immediately following acclimation and every
15 min thereafter for 1.75 h by later viewing the
video recordings. We enum erated swimming
activity over 1.75 h, instead of the planned 2 h,
because we extended the initial 15-min acclimation
period to 30 min midway through the trials.
We assessed climbing activity at 4, 7, 12, 14.5,
17, 19.5, 22 and 25°C (± 1.0°C for each tempera-
ture) by enum erating the num ber o f eels that
climbed an artificial waterfall over a 2-h period.
We used intermediate tem peratures o f 14.5 and
19.5°C to investigate climbing activity between
tem peratures where there were large differences in
climbing counts. We placed a piece o f wood cov-
ered with coarse net on a 35° angle at one end of
the aquarium , serving as the waterfall. W ater flo-
wed out o f a 1 cm diam eter hose from an upper
holding tank at a rate of 8.2 1 min-1, creating the
waterfall and a pool that spilled over and moist-
ened the entire slope. A funnel-shaped net
encompassed the pool, trapping the eels that sur-
m ounted the waterfall. The water level in the
aquarium was m aintained by an overfiow hose
inserted into the side of the aquarium .
Results and discussion
The swimming activity o f the eels did not vary over
the observation time (p < 0.001; d f= 7 ) (Friedm an
2-way ANOVA; Siegel 1964), therefore we calcu-
lated the mean number o f eels that swam at each
tem perature from the eight poínt counts. The
threshold tem perature for swimming was between
4 and 7°C and the threshold tem perature for ver-
tical movement over the waterfall was between 12
191
Table I. Mean number of swimming glass eels (Anguilla spp.)
calculated from point counts made over 1.75 h and the number
of glass eels that climbed over an artificial waterfall in a 2-h
period at water temperatures between 4 and 25°C.
Temperature (°C) Number of eels
Mean swimming
value (±SE)
Climbing count
4 0 (0 ) 0
7 5.9 (0.8) 0
12 17(1) 0
14.5 n/a 5
17 15 (1) 19
19.5 n/a 19
22 1 0 ( 1) 27
25 9.6 (0.8) 22
n/a - not applicable; trial not performed at specified tempera-
ture.
and 14.5°C (Table 1). Swimming activity peaked
at 12°C and climbing activity was highest a t 22°C
(Table 1). The distribution o f the mean num ber of
swimming eels at each tem perature was signifi-
cantly different than the distribution of the count
of eels that climbed the waterfall at each temper-
ature common to the two experiments (p < 0.001,
Kolm ogorov-Sm irnov two-sample test; Sie.gel
1964).
The higher threshold and maximum tempera-
tures for climbing activity relative to swimming
activity, as well as the different distributions of the
num ber o f swimming and climbing eels at the
tem peratures com m on to both experiments, agree
with the prediction from our field hypothesis that
glass eels display distinct behaviour patterns at
different water tem peratures. O ur findings have
im portant implications, as natural and anthropo-
genic vertical obstacles exist in m any watercourses.
For example, the inland penetration of eels in
northerly locations may be reduced com pared to
southern locations where water tem peratures are
warmer. Similarly, the timing o f movement into
freshwater may be inversely related to latitude, as
a result of lower tem peratures o f more northern
streams. Thermal discharge into freshwater sys-
tems, whether natural or anthropogenic, and cli-
matic changes could also have signiíicant effects
on the upstream m igration o f glass eels.
In our study, the threshold tem peratures for the
two types o f upstream movement, swimming and
climbing behaviours were different, but largely in
agreement with m igratory data we collected in the
field. Studies elsewhere in the range o f these species
have found that the threshold tem perature for
swimming movement is between 12 and 19°C in
A. rosíraía elvers (Sorensen & Bianchini 1986) and
range from 14 to 16°C (White & Knights 1997), 10
to 12°C (Gascuel 1986) and 7°C (Tongiorgi et al.
1986) in A. anguilla glass eels, elvers and juveniles.
Com parable studies to our climbing behaviour
experiments are lacking.
O ur results also illustrate that at tem peratures
between 17 and 25°C glass eels exhibit both swim-
ming and climbing behaviours. Therefore, it is
probable that a t these tem peratures overall migra-
tory activity will be highest. This finding corre-
sponds to field reports that A. anguilla glass eel,
elver and juvenile migration is highest when fresh-
water tem peratures range from 13 to 17°C (Gan-
dolfi et al. 1984), 18 to 20°C (W hite& K nights 1997)
and 20 to 25°C (Ezzat & El-Serafy 1977).
Our study represents the first laboratory exper-
iments on the effects o f water tem perature on the
different locom otor behaviour patterns that glass
eels or elvers exhibit during their m igratory ascent.
Understanding how the distinct m igratory behav-
iour patterns o f glass eels are influenced by an
im portant environmental variable such as water
tem perature is key in our study o f the upstream
movement o f eels.
Acknowledgements
We extend many thanks to M om oko Kawai,
G udm undur Ingi Gudbrandsson, the folks at
Brúarland, and H alldór O ttó A rinbjarnarson for
their assistance in the field. The Icelandic Student
Innovation Fund, the Icelandic Agricultural Pro-
ductivity Fund, the Icelandic Governm ent, and an
Operating G rant from N SERC C anada provided
funding for this research.
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Genome-wide single-generation signatures of local
selection in the panmictic European eel
J. M. PU IO LA R ,* M. W. JACO BSEN,* T. D. ALS , t j J. F R YD ENB ERG / K. MU N C H, § B. JÓ N SSO N ,!
J. B. JIAN,** L. C H E N G , f f G. E. M A E S , J t § § L- BERNATCHEZW and M. M. HANSEN*
*Department of Bioscience, Aarhus University, Ny Munkegade 114, Bldg. 1540, DK-S000 Aarhus C, Denmark, iNntional
Institute of Aquatic Resources, Technical University of Denmark, Vejlsovej 39, DK-8600 Silkeborg, Denmark, %Department of
Biomedicine-Human Genetics, Aarhus University, DK-8000 Aarhus C, Denmark, §Bioinformatics Research Center, Aarhus
University, DK-8000 Aarhus C, Denmark, ^Biopoi, Marine Biology and Biotechnology Center, Einbúastigur 2, IS545
Skagastrond, Iceland, **BGI-Shenzhen, Beishan Industrial Zone, Main Building, Yantian District, 518083 Shenzhen, China,
f t BGI-Europe, Copenhagen Bio Science Park, Ole Maaloes Vej 3, DK-2200 Copenhagen, Denmark, %%Laboraton/ of Biodiversity
and Evolutionany Genomics, University of Leuven (KU Leuven), Deberiotstraat 32, B-3000 Leiwen, Belgium, §§Centre for
Sustainable Tropical Fisheries and Aquaculture, School of Marine and Tropical Biology, James Cook University, Townsville,
Qld 4811, Australia, ^ IB IS (Institut de Biologie Intégrative et des Systémes), Université Laval, Québec City, QC, Canada GIV
0A6
Abstract
Next-generation sequencing and the collection of genom e-wide data allow identifying
adaptive variation and footprints of directional selection. Using a large SNP data set
from 259 RAD-sequenced European eel individuals (glass eels) from eight locations
betw een 34 and 64°N, w e examined the patterns of genom e-wide genetic diversity
across locations. We tested for local selection by searching for increased population
differentiation using FsT~t»ased outlier tests and by testing for significant associations
betw een allele frequencies and environmental variables. The overall low genetic dif-
ferentiation found (Fst = 0.0007) indicates that most of the genom e is hom ogenized by
gene flow, providing further evidence for genomic panmixia in the European eel. The
lack of genetic substructuring was consistent at both nuclear and mitochondrial SNPs.
U sing an extensive number of diagnostic SNPs, results showed a low occurrence of
hybrids betw een European and American eel, mainly lim ited to Iceland (5.9%),
although individuals with signatures of introgression several generations back in time
were found in mainland Europe. Despite panmixia, a sm all set of SNPs show ed high
genetic differentiation consistent with single-generation signatures of spatially varying
selection acting on glass eels. After screening 50 354 SNPs, a total of 754 potentially
locally selected SNPs were identified. Candidate genes for local selection constituted a
w ide array of functions, including calcium signalling, neuroactive ligand-receptor
interaction and circadian rhythm. Remarkably, one of the candidate genes identified is
PERIOD, possib ly related to differences in local photoperiod associated with the >30°
difference in latitude between locations. Genes under selection were spread across the
genom e, and there were no large regions of increased differentiation as expected when
selection occurs w ithin just a single generation due to panmixia. This supports the
conclusion that most of the genome is hom ogenized by gene flow that removes any
effects of diversifying selection from each new generation.
Keywords: anguilla, local adaptation, panmixia, spatially varying selection
Received 20 January 2014; revision received 11 April 2014; accepted 11 April 2014
C o rre sp o n d en c e : Jose M . P u jo lar, Fax: +45 89422722;
E-m aiI: jm a rtin @ b io lo g y .a u .d k
© 2014 Jo h n W iley & S ons Ltd
mailto:jmartin@biology.au.dk
L OCAL SEL E CT IO N IN THE E U R O P E A N EEL 2515
Introduction
Identifying which regions of the genome are under
selection is essential for understanding the selective
pressures acting upon natural populations and distin-
guishing between neutral and adaptive genetic variation
(Nielsen 2005; Stapley et nl. 2010; Radwan & Babik
2012; Bourret et al. 2013). Species that occupy heteroge-
neous environments (i.e. temperature, salinity) along
their geographical distribution experience spatially
varying selective pressures, often resulting in local
adaptation of ecologically important traits (Kawecki &
Ebert 2004; Fraser et al. 2011). Beginning with Levene
(1953), a number of studies have shown that balancing
selection due to spatial heterogeneitv is an important
mechanism responsible for the maintenance of genetic
polymorphism (reviewed in Hedrick 2006). While poly-
morphism in a varying environment may be maintained
even when dispersal results in complete mixing of the
gene pool, in such case localities will not differentiate
genetically and there will be no local adaptation
(Kawecki & Ebert 2004). Recent population genomic
studies predict the observation of single points of selec-
tion across the genome when gene flow is high, as loci
subject to strong selection will tend to diverge indepen-
dently from other genes, while highly differentiated
genomic regions due to genome hitchhiking are
expected with reduced gene flow (Feder & Nosil 2010;
Yeaman & Otto 2011; Yeaman & Whitlock 2011; Feder
et al. 2012). Genomic regions displaying increased dif-
ferentiation referred to as genomic islands of divergence
have been observed in many taxa from fungi (Ellison
et al. 2011) and invertebrates (Nosil et al. 2008; Nadeau
et al. 2012) to fishes (Hohenlohe et al. 2010; Jones et al.
2012a,b; Bradbury et al. 2013; Gagnaire et al. 2013;
Hemmer-Hansen et al. 2013) and humans (Hoffer et al.
2012).
An excellent opportunity to study the interplay
between spatially varying selection and gene flow exists
in the European eel (Anguilla anguilla), a putatively
panmictic species occupying a broad range of habitats
from subarctic environments in Iceland, Norwray and
northwestern Russia to subtropical environments in
North Africa and the Mediterranean Sea. The European
eel is a facultative catadromous species with a complex
life cycle, spawning in the remote Sargasso Sea and
spending most of their life in continental (fresh, brack-
ish and coastal) waters (Van den Thillart et al. 2009).
After spawning, larvae are advected towards the coasts
of Europe and North Africa, where they arrive follow-
ing first the Gulf Stream and later the North Atlantic
Drift Current. Upon reaching the continental shelf,
larvae metamorphose into glass eels and move into con-
tinental growth habitats, settle and become pigmented
yellow eels. After a period of intense feeding of (on
average) 7 years for males and 11 years for females,
they metamorphose into partially mature silver eels that
migrate back to the Sargasso Sea covering a distance of
5000-6000 km, spawn and die (Van den Thillart et al.
2009). In the Sargasso Sea, European eel spawns in
partial spatial and temporal sympatry v\rith its sister
species, the American eel Angiiilla rostrata, which
provides opportunity to interbreed. European and
American eels are known to hybridize, but hybrids
have been reported almost exclusively in Iceland (Avise
et al. 1990; Albert et al. 2006; Pujolar et al. 2014).
Despite the broad geographical distribution of the
species, the European eel is regarded as a textbook
example of panmixia, with the existence of a single ran-
domly mating population. In the most comprehensive
study to date genotyping over 10 0 0 individuals at 2 1
microsatellite loci, AIs et al. (2011) showed a very low
and nonsignificant genetic differentiation between
geographical locations across Europe and a lack of
substructuring among larvae collected in the Sargasso
Sea, providing very strong support for panmixia. In
American eel, the recent study of Cóté et al. (2013)
genotyping over 2000 individuals representing 1 2
cohorts at 18 microsatellite loci over a large geographi-
cal scale in North America showred a total lack of
genetic differentiation among samples, hence providing
decisive evidence for panmixia in American eel. In con-
trast, significant geographical clines at some allozyme
loci have been detected in both European (Maes &
Volckaert 2002) and American eels (Koehn & Williams
1978). Moreover, Gagnaire et al. (2012a) found evidence
for spatially varying selection at 13 of 73 candidate
genes showing correlations between allele frequencies
and environmental variables across the entire distribu-
tion range of American eel, particularly determined by
temperature regimes. In the case of eels, owing to the
apparent panmixia and random larval dispersal across
habitats, any signature of spatially varying selection in
a given generation is expected to be lost in the subse-
quent generation (Gagnaire et al. 2012a), hence prevent-
ing heritable trans-generational local adaptation.
This study aimed at investigating the influence of
spatially varying selection on genetic diversity and
potential adaptive divergence in European eel using a
population genomics approach. The fact that most
population genetic studies in eels have used neutral
markers prompts for the investigation of the potential
influence of natural selection on the genetic variation of
the species.
Our first goal was to validate the lack of background
level of neutral differentiation between locations, and
for that we used a RAD-sequencing approach (Baird
et al. 2008; Hohenlohe et al. 2010; Davey et al. 2011) to
© 2014 John Wiley & Sons Ltd
2516 J. M. P U JO L A R E T A L .
T a b le 1 S a m p lin g d e ta ils in c lu d in g n u m b e r o f E u ro p ea n eel (g lass eels) in d iv id u a ls , g e o g rap h ica l co o rd in a te s , s a m p lin g d a te a n d
sea -su rface te m p e ra tu re (°C) a t r iv e r m o u th av e rag e d acro ss th e 10, 30 a n d 90 d a y s p re c e d in g s a m p lin g d a te
L o ca tio n C o d e N C o o rd in a te s S a m p lin g d a te T em p-10 d a y T em p-30 d a y T em p-90 d a y
V o g slæ k u r , Ic e lan d ICE 34 6 4 °69 'N /22°33 'W 2 /7 /2 0 0 1 9.53 9.38 8.45
Ringhcils, S w ed en RH G 30 57 °21 'N /12°27 'E 1 5 /3 /2 0 0 8 4.76 4.77 4.19
L o u g h E m e, N o r th e m Ire la n d LG 33 5 4 °4 6 'N /7 °7 7 'W 1 /7 /2 0 0 8 13.93 13.81 13.85
B u rrish o o le , I re la n d BG 29 5 3 °9 0 'N /9 °5 8 'W 1 4 /3 /2 0 0 5 9.36 9.79 9.57
G iro n d e , F rance G G 37 44°86 'N / 0°42'W 1 6 /4 /2 0 0 8 11.55 11.78 11.26
C an e t, F rance C A G 32 4 2 °7 0 'N /3 °1 5 'E 2 3 /1 /2 0 0 8 12.73 12.61 13.24
V alenc ia , S p a in VG 31 3 9 °4 6 'N /0 °2 4 'W 1 5 /1 /2 0 1 0 14.06 14.16 15.05
O v e d S ebou , M orocco M O R 33 3 4 °2 6 'N /6 °7 0 'W 2 8 /4 /2 0 0 1 17.53 17.82 17.57
identify 453 062 SNPs from 259 individuals sampled
from eight locations across the species range. As part of
testing the panmixia hypothesis, we were interested in
testing whether genetic differentiation was consistent at
nuclear and mitochondrial loci. We were also interested
in testing for the presence of hybrids across Europe to
assess whether hybridization could have influenced
results, using diagnostic SNPs between European and
American eels.
Our second goal was to contrast the outcome of
neutral vs. adaptive differentiation in European eel.
Using a subset of 50 354 SNPs with minor allele fre-
quency >0.05, we tested for single-generation footprints
of spatially varying selection with two main analytical
approaches, one that identifies outliers as those markers
with greater differentiation among all SNPs and a sec-
ond based on determining positive associations between
SNP frequencies and environmental variables. Follow-
ing the positive associations observed by Gagnaire et al.
(2012a) in American eel, variables used were degrees
north latitude, degrees east/west longitude and sea-sur-
face temperature at river moutlis, corresponding to the
sampling locations. Candidate genes were functionally
annotated to assess potential functions of genes under
selection. We specifically wanted to test whether genes
under selection were grouped into clusters/islands as
observed in other species (Nosil et al. 2008; Hohenlohe
et al. 2010; Jones et al. 2012a,b; Nadeau et al. 2012;
Bradbury et al. 2013; Gagnaire et al. 2013; Hemmer-Hansen
et al. 2013) or more spread across the genome as
expected to occur within just a single generation under
a panmixia scenario.
M aterials and m ethods
Sampling
A total of 259 European eel (Anguilla anguilla) individu-
als were collected for RAD sequencing at eight locations
across the geographical distribution of the species,
ranging from Iceland to Morocco (Table 1; Fig. 1). All
samples were glass eels collected during January in the
Mediterranean and March/April in the Atlantic, except
samples from Iceland and Northern Ireland, which
were collected in July. Genomic DNA was extracted
using standard phenol-chloroform extraction.
RAD tag sequencing, RAD data analysis and SNP
identification
Genomic DNA from each individual was digested with
restriction enzyme EcoRl. RADs for all 259 European eel
individuals were sequenced (10 individuals per lane)
on an Illumina Genome Analyzer II by Beijing Genom-
ics Institute (BGI, Hong Kong) using paired-end reads
(for details see Pujolar et al. 2013).
Sequence reads from the Illumina runs were sorted
according to barcode tag. Sequences were quality-filtered
© 2014 John Wiley & Sons Ltd
LO CA L S ELE CT IO N IN THE E U R O P E A N EEL 2517
using FASTX-Toolkit (http://hannonlab.cshl.edu/fastx-
toolkit), and reads with ambiguous barcodes/poor qual-
ity were removed from the analysis. Any read that
presented a single nucleotide position with a Phred
score lower than 10 was eliminated. This corresponds
to the threshold generally used in SNP discovery stud-
ies (Van Bers et al. 2010; Ellison et al. 2011; Scaglione
et al. 2012; Wagner et al. 2012). Final read length was
trimmed to 75 nucleotides to reduce sequencing errors
present at the tail of the sequences (Pujolar et al. 2013).
For SNP calling, only the fírst (left) paired read was
used due to the lower coverage of the second paired-
end reads (Etter et al. 2011).
The un-gaped aligner b o w t ie version 0.12.8 (Lang-
mead et al. 2009) was used to align sequence reads to
the European eel genome draft (www.eelgenome.com),
which consists of 179 Mbp of small contigs and
923 Mbp of larger contigs or scaffolds (Henkel et al.
2012). A maximum of two mismatches between the
individual reads and the genome were allowed. Reads
with altemative (two or more) alignments were
excluded to avoid paralogous sequences.
Reference-aligned reads were processed using the
ref_map.pl pipeline in s t a c k s version 0.9995 (Catchen
et al. 2013). First, exactly matching reads were aligned
together into stacks and subsequently merged to form
putative loci. A minimum stack depth of 10 reads was
used. Subsequently, a maximum-likelihood framework
was used to call SNPs, and a catalogue was built of all
existing loci and alleles against which all individuals
were matched. Finally, the program Populations in
Stacks was used to process all the SNP data across
individuals.
Prior to the SNP analysis, loci in the catalogue were
further filtered to remove paralogs and otherwise spuri-
ous loci according to the following three criteria: (i) loci
with higher-than-average number of reads were
excluded, because an extremely high coverage might be
an indication of the presence of more than one locus
(twice the standard deviation from the mean number of
reads was used as threshold); (ii) loci with more than
two alleles were eliminated because those might result
from sequencing errors; and (iii) loci deviating from
Hardy-Weinberg equilibrium (HWE), tested using
g e m e p o p version 4.2 (Raymond & Rousset 1995), were
excluded after adjusting significance levels for multiple
comparisons using the sequential Bonferroni technique
(Rice 1989). As a final filtering step, minimum percent-
age of individuals in a population required to process a
locus was set to 66.67%.
RAD analysis was also conducted separately for
mitochondrial SNPs by aligning all reads against the
European eel mitogenome (GenBank Accession no.
NC_006531) in b o v v t ie .
SNP analysis
Genome-wide measures of genetic diversity, including
nucleotide diversity (II) and observed (Hp) and
expected (HJ heterozygosities, were calculated in
Stacks (Table 2). Differences in genetic diversity among
samples were tested by one-way a n o v a using s t a t i s t i c a
version 6.0 (StatSoft Inc). Deviations from HWE, differ-
ences in allele and genotype frequencies among samples,
F-statistics for all samples and all sample pairs and iso-
lation by distance (IBD) were tested using g e n e p o p (Ray-
mond & Rousset 1995). In all cases, significance levels
were corrected for multiple comparisons using the
sequential Bonferroni technique (Rice 1989). Pairwise
Fst values were used to conduct a multivariate ordina-
tion by multidimensional scaling (MDS) analysis using
s t a t i s t i c a . IBD was tested using Mantel test (Mantel
1967) by correlating linearized genetic distance (FST/
(1 —FST)) v s . geographical distance (shortest waterway
distance in kilometre between sample pairs). All analy-
ses were conducted considering (i) all nuclear DNA
sequences and (ii) all mitochondrial sequences.
Finally, we tested the presence of hybrid individuals
in the data set using s t r u c t u r e v.2 .3 .4 (Pritchard et al.
2000). For this purpose, the analysis also included a
sample of 30 RAD-sequenced American eel (yellow and
glass eels) Anguilla rostrata individuals collected in
Quebec, Nova Scotia and Florida (Pujolar et al. 2013). A
preliminary analysis was conducted using 20 random
European and American eel individuals to identify
diagnostic species-specific SNPs fixed at different alleles
in each species (FST = 1) following the same approach
as in Pujolar et al. (2014). We identified a total of 2148
diagnostic SNPs between European and American eels
that were used for hybrid identification in the data set.
The analysis in s t r u c t u r e was performed using
1 < k < 9, with 10 replicates per k to check the consis-
tency of results. We assumed an admixture model and
uncorrelated allele frequencies, and we did not use
population priors. A burn-in length of 100 000 steps fol-
lowed by 1 million additional iterations was performed.
The most likely k was determined using the criterion of
Evanno et al. (2005). The presence and nature of hybrids
was further tested using the Gensback setting in
s t r u c t u r e . When using prior population information for
individuals, the program tests whether each individual
has an immigrant ancestor in the last G generations,
where G = 0 corresponds to the individual being an
immigrant itself. The analysis was performed with G = 5.
Tests for local selection
Evidence of local selection was tested by searching for
increased population differentiation using FST-based
© 2014 Jo h n W iley & S ons L td
http://hannonlab.cshl.edu/fastx-
http://www.eelgenome.com
2518 J. M . P U J O L A R E T AL .
T a b le 2 D iv e rs ity in d ice s ac ro ss E u ro p e a n eel (g lass eels) sam p les c o n s id e rin g (i) n u c le a r D N A seq u e n c es a n d (ii) m ito c h o n d ria l
seq u en c es
L ocation N
N u c lea r M ito c h o n d ria l
tfo H c 4) H e O M N A T N A
V o g slæ k u r, Tceland 34 0.036 (0.006) 0.040 (0.008) 0.041 (0.008) 0.056 (0.012) 0.057 (0.012) 1.34 55
R in g h a ls , S w e d en 30 0.039 (0.007) 0.041 (0.008) 0.042 (0.008) 0.056 (0.006) 0.057 (0.005) 1.54 63
L o u g h E rne, N o r th e m Ire la n d 33 0.033 (0.006) 0.038 (0.007) 0.039 (0.008) 0.064 (0.009) 0.065 (0.009) 1.51 62
B urrishoo le , I re la n d 29 0.036 (0.007) 0.039 (0.008) 0.040 (0.008) 0.050 (0.006) 0.051 (0.007) 1.44 59
G iro n d e , F ran ce 37 0.035 (0.006) 0.039 (0.007) 0.034 (0.008) 0.064 (0.007) 0.065 (0.008) 1.56 64
C an e t, F rance 32 0.036 (0.006) 0.039 (0.007) 0.040 (0.008) 0.068 (0.010) 0.070 (0.010) 1.46 60
V alencia , S p a in 31 0.035 (0.006) 0.039 (0.008) 0.034 (0.008) 0.069 (0.008) 0.070 (0.008) 1.46 60
O v ed S ebou , M orocco 33 0.036 (0.006) 0.040 (0.008) 0.041 (0.008) 0.067 (0.010) 0.068 (0.010) 1.59 65
H 0, o b se rv e d h e te ro z y g o sity ; H e, ex p ec te d h e te ro zy g o sity ; (t>, n u c le o tid e d iv e rs ity ; M N A , m e a n n u m b e r o f a lle les; T N A , to ta l n u m b e r
o f a lle les.
S ta n d a rd d e v ia tio n in p a re n th e se s .
outlier analyses implemented in l o s i t a n (Antao et al.
2008) and b a y e s c a n (Foll & Gaggiotti 2008) and by test-
ing for significant associations between allele frequen-
cies and environmental variables using b a y e n v (Coop
et al. 2010). Loci showing either significantly greater
population differentiation or significant covariance with
environmental variables relative to reference SNP distri-
butions were considered candidates for being under
local selection. In all three approaches, only SNPs with
a minor allele frequency >0.05 were included in the
analysis.
The selection detection workbench l o s i t a n (http://
popgen.eu/soft/lositan/) uses a coalescent-based simu-
lation approach to identify outliers based on the distri-
butions of heterozygosity and FST (Beaumont &
Nichols 1996). First, l o s i t a n was run using all SNPs to
estimate the mean neutral FST as recommended by
Antao et al. (2008). After the fírst run, the mean neutral
Fst was recomputed by removing those SNPs outside
the confidence interval to obtain a better approxima-
tion of the mean neutral FST. This mean was then used
to conduct a second and final run of l o s i t a n using all
SNPs. An estimate of P-value was obtained for each
SNP. We used a strict threshold of 0.995 and a false
discovery rate of 0 .1 to minimize the number of false
positives.
Outlier SNPs were also detected using the Bayes-
ian test of FoII & Gaggiotti (2008) implemented in
b a y e s c a n (http:/ / cmpg.unibe.ch/software/bayescan/).
The method is based on a logistic regression model that
separates locus-specific effects of selection from popula-
tion-specific effects of demography. Loci under selection
are detected after comparing the posterior probabilities
of a neutral model considering only population-specific
Fst parameters and a model includmg selection via a
locus-specific Fst component to describe the observed
allele frequencies. Outlier analysis was conducted on
the whole data set divided according to sampling loca-
tion. b a y e s c a n runs were implemented using default
values for all parameters, including a total of 100 000
iterations after an initial burn-in of 50 000 steps. A
íj-value of 1 0 % was used.
As an alternative to these FST-based outlier tests, we
also searched for SNP-environment associations using
b a y e n v (Coop et ál. 2010), which tests for covariance
between candidate SNP allele frequencies and environ-
ment variables that exceed the expected covariances
under genetic drift. In the first step, the program is run
to estimate the covariate matrix using an MCMC algo-
rithm. In the second step, the program is run to esti-
mate the Bayes Factors (BF) for the environmental
variables of interest. A BF >3 was considered indicative
of an allele frequency correlation with an environmental
variable. Results were compared over five independent
runs for consistency. Environmental variables used
included degrees north latitude, degrees east/west
longitude and sea-surface temperature at river mouth
averaged across the 10 days, 30 days and 3 months
preceding the sampling date. Temperature data were
obtained from the IRI (Intemational Research Institute
for Climate and Society) Climate Data Library (http://
iridl.ldeo.columbia.edu/SOURCES/.NOAA/.NCDC/.
OISST).
Gene predictions for the European eel genome
(http://www.zfgenom ics.org/sub/eel) were used to
establish the genomic position of the candidate SNPs
for local selection using a custom-made script. SNPs
were considered to be located in a gene when
included in complete coding sequences (CDS) and ex-
onic and intronic regions. Functional annotation of
© 2014 Jo h n W iley & Sons Ltd
http://www.zfgenomics.org/sub/eel
L O CA L SEL E CT IO N IN THE E U R O P E A N EEL 2519
these genes was obtained using the B la s t2 G o suite
(Götz et nl. 2008), which conducts b l a s t similarity
searches and maps Gene Ontology (GO) terms to the
homologous sequences found. Only ontologies with E-
value < 1 E-6 , annotation cLit-off >55 and a GO weight
>5 were considered for annotation. A more systematic
functional interpretation of the set of candidate genes
was obtained using the Kyoto Encyclopedia of Genes
and Genomes (KEGG) pathway approach for higher-
order functional annotation implemented in the
Database for Annotation, Visualization and Integrated
Discovery ( d a v i d ) web-server v6.7 (http://david.abcc.
ncifcrf.gov). Zebrafish Danio rerio was used as refer-
ence genome for annotation. Prior to the analysis in
d a v i d , a local b l a s t was conducted for significant
matches directly against zebrafish Ensembl proteins
using b l a s t x . Zebrafish Ensembl Gene IDs were
obtained from the corresponding Ensembl protein
entries using the b i o m a r t data mining tool in the En-
sembl website (http://www.ensembl.org/biomart/).
Gene functional analysis in d a v i d was conducted defín-
ing the zebrafish IDs corresponding to those genes
including a locally selected SNP as 'Gene list' and the
zebrafish IDs corresponding to all genes as 'Back-
ground'. Standard settings of gene count = 2 and
ease = 0 .1 were used.
Finally, the pattenis of differentiation across genome
regions were characterized to test whether genes
putatively under selection were grouped into clusters
(genomic islands of differentiation) or more scattered
across the genome. We estimated the levels of genetic
differentiation between populations by calculating aver-
age F St for 50-kb genomic sliding windows. Altemative
slidtng windows (10 0 and 200 kb) were also tested. ^st
was calculated between the two most ecologically and
geographically differing locations, Iceland and Morocco.
Windows were restricted to the 30 longest scaffolds
(903 936-2 025 234 bp) from the European eel draft
genome.
R esults
RAD sequencing
Sequencing of the RAD libraries generated an average
of 9.59 million reads of 90 bp per individual. After
trimming sequences to 75 bp and quality filtering, on
average, 7.90 million (82.19%) reads per individual
were retained. Mean quality score of the retained reads
was 38.65, with a GC content of 41.1% (Table 3). An
average of 69.96% of the quality-filtered reads aligned
to the European eel draft genome and 4.46% of the
reads were discarded due to altemative (two or more)
alignments.
Aligned reads were assembled into an average of
526 821 stacks and subsequently into a set of 335 343
loci (Table 3). A total of 118 016 (35.5%) reads per indi-
vidual were discarded due to insufficient depth of cov-
erage. Loci with a minimuni stack depth of 10 reads
were retained to construct a catalogue of 527 504 loci,
using a total of 80 individuals (10 individuals per loca-
tion). Prior to SNP discovery, loci were further filtered
to minimize errors in sequencing, alignment or assem-
bly. First, 815 loci showing >57.35 reads (twice the stan-
dard deviation from the mean number of reads,
19.16 ± 19.09) were discarded, as a lúgher-than-average
number of reads suggest the presence of more than one
locus. Second, 40 270 loci showing three alleles per indi-
vidual were eliminated. Tlurd, 1749 loci not adjusting
to Hardy-Weinberg proportions after Bonferroni correc-
tion were also removed, representing either loci at
which all individuals were heterozygotes or loci at
which one single individual was homozygote for an
allele not observed in the rest of the individuals.
Finally, after a fíltering step selecting only loci geno-
typed in >66.7% of individuals in all sampling locations,
a total of 72 932 loci were retained for SNP discovery.
Using the program Population in Stacks, a total of
453 062 SNPs were discovered. After aligning against
T a b le 3 S ta tis tics d e sc rib in g th e d is tr ib u tio n o f d iffe re n t p ro p e r tie s o f RA D seq u en ces a f te r each s te p o f filte r in g (FASTX -Toolkit),
a lig n m e n t to th e eel d ra f t g e n o m e (b o v v tie ) a n d a ssem b ly in to loci (R ef_m ap .p l)
FASTX
R aw re a d s
9593701
F ilte red re a d s
7S99505
% E lim in a ted
17.81
M ean Q
38.65
Q i
37.97
M ed Q3
39.40 40.22
% A %C
29.5 20.7
%G %T
20.4 29.3
BO W TIE
R eads
7899505
A lig n e d
5527660
% A lig n ed
69.96
N o n a lig n ed
2018833
% N o n a lig n e d
25.59
D isca rd ed
353042
% D isca rd ed
4.46
R EF_M A P
R ead s
5527660
Stacks
526821
Loci
335343
Loci u s e d
217326
% Loci u s e d Loci d is c a rd e d
64.50 118016
% Loci d is c a rd e d
35.50
© 2014 Jo h n W iley & S ons L td
http://david.abcc
http://www.ensembl.org/biomart/
2520 J. M. P U JO L A R ET AL .
the European eel mitogenome, a total of 11 loci and 41
SNPs were identified as mitochondrial.
Genetic diversity and differentiation
Measures of genetic variability across locations consid-
ering all identified SNPs are summarized in Table 2. No
differences in values of observed heterozygosity
(H0 = 0.038-0.039), expected heterozygosity (He = 0.038-
0.041) and nucleotide diversity (II = 0.034—0.042) were
found across locations (P > 0.05 in all comparisons). No
differences were observed when H0, He and n were
calculated using all (fixed and variable) positions. Simi-
larly, genetic diversity was similar across locations
(He = 0.056-0.069; II = 0.051-0.070) when considering
only mitochondrial RADs (41 SNPs at 11 loci).
When investigating the genetic structure among loca-
tions, all pairwise Fst comparisons were not significant
(P > 0.05), with an average pairwise Fst value of 0.0007.
Comparison of allele frequencies across locatíons
showed highly significant differences at only 26 of
453 062 SNPs after Bonferroni correction for multiple
testing. An MDS plotting the first and second coordi-
nates obtained from pain\dse genetic distances showed
all samples clustering togetlier fitting no apparent geo-
graphical pattem (Fig. Sla, Supporting infonnation). A
Mantel test showed no correlation between genetic and
waterway distances (r = —0.232; P = 0.250), which
suggests no IBD pattem (Fig. 2a).
When considering only mitochondrial markers (41
SNPs), genetic differentiation was low (FST = 0.0002),
and no significant differences were found when com-
paring allele frequencies across locations after Bonfer-
roni correction. Flowever, pairwise FST values were
significant at five of 28 comparisons, all involving
Iceland. Concordantly, Iceland was the most distant
sample in the MDS analysis (Fig. Slb, Supporting infor-
mation) and also contributed to the observed positive
but nonsignificant pattern of IBD (r = 0.311; P = 0.107;
Fig. 2b).
Using 2148 species-diagnostic nuclear SNPs with an
Fst value of 1 between the two species, s t r u c t u r e was
used to investigate the possible presence of admixed
individuals in the data set. A scenario with two groups
(K = 2) corresponding to the two species was inferred
to be the most likely (Fig. 3). Occurrence of hybrids
was low, with a total of three admixed mdividuals
found within European eel: one from Gironde with an
admixture proportion of 0.053 (0.037-0.070) and two
from Iceland with admixture proportions of 0.190
(0.176-0.218) and 0.192 (0.176-0.217), respectively. Addi-
tionally, three individuals (two from Canet and one
from Ringhals) presented an admixture proportion of
0.03. Within American eel, one single admixed individ-
(a) w Multi-/?-squared = 0.05487; F = 1.509 ; df = 26; P = 0.250
Distance(km)
(b) Multi-R-squared = 0.09678; F = 2.786 ; df = 26; P = 0.107
Distance(km)
Fig. 2 M an te l te st c o rre la tin g p a irw is e lin e a riz ed g enetic d is-
tances ( F s r / ( l - F s T)) vs. g e o g ra p h ic a l d is ta n ce s (sh o rte s t w a te r-
w a y d is ta n c e in k ilo m e tre ) b e tw e e n a ll g la ss eel s a m p lin g
lo ca tio n s co n s id e rin g (a) a ll RA D seq u en c es a n d (b) m ito c h o n -
d r ia l R A D seq u en c es on ly .
ual was found, with an admixture proportion of 0.056
(0.041-0.073). Using the Gensback setting in s t r u c t u r e ,
the two admixed individuals from Iceland were classi-
fied as first-generation backcrosses, while the admixed
individual from Gironde was classified as a third-gener-
ation backcross, same as the admixed American eel
individual.
Finally, all individuals were identified as European
or American eel on the basis of the mitochondrial RADs
(Fig. 3). Five of 41 SNPs were diagnostic, that is, fíxed
at different alleles. All European eels plus the three
hybrids from Iceland and Gironde showed the European
eel-diagnostic mitochondrial alleles, except one individ-
© 2014 John Wiley & Sons Ltd
LOCA L S EL E CT IO N IN THE E U R O P E A N EEL 2521
AR
VG GG
AA
BG CAG LG RHG ICE MOR
Fig. 3 A d m ix tu re a n a ly s is u s in g s t r u c t u r e . (a) In d iv id u a ls w e re a ss ig n e d on th e b a s is o f th e m o s t like ly K (in th is case, K = 2). Each
v e rtic a l lin e re p re s e n ts o n e in d iv id u a l, p a r titio n e d in to seg m e n ts a cco rd in g to a d m ix tu re p ro p o r tio n o f E u ro p e a n eel (AA; g reen ) a n d
A m e rican eel (AR; re d ). L o ca tio n s a re lab e lled as in T ab le 1. (b) Id en tif íca tio n o f all in d iv id u a ls a s E u ro p e a n o r A m e ric a n ee l o n th e
b a sis o f th e m ito c h o n d r ia l R A D s is a lso in c lu d e d (b o tto m pan el).
ual from Lough Erne identified as pure European eel
on the basis of all nuclear loci presenting the five Amer-
ican eel-diagnostic mitochondrial alleles. All American
eels plus the admixed American eel individual showed
the American eel-diagnostic mitochondrial alleles,
except one individual identified as pure American eel
on the basis of all nuclear loci that presented the five
European eel-diagnostic mitochondrial alleles.
Local selection
In all tests for local selection, a total of 50 354 SNPs
with a minor allele frequency >0.05 were included in
the analysis. Using l o s i t a n , a total of 670 SNPs repre-
senting 639 unique loci were identified as outliers possi-
bly under directional selection, after applying a
signifícance level of 0.995. A smaller number of outlier
loci were identified using b a y e s c a n : 33 SNPs represent-
ing 30 unique loci, all of which were part of the outliers
identified using l o s i t a n . A s expected when considering
that both l o s i t a n and b a 'í'E S C an are f ST-based methods,
all outhers showed high Fst values (0.04-0.12) compared
with the background FST.
Bayesian tests for SNP-environment associations in
b a y e n v identifíed a total of 87 candidate SNPs repre-
senting 74 unique loci: 12 SNPs representing 12 unique
loci associated with latitude, 29 SNPs representing 28
unique Ioci associated with longitude and 51 SNPs
representing 49 unique loci associated with tempera-
ture, with a few SNPs being correlated with more than
one variable. Highly similar results were obtained
when using the three temperature data sets (last
10 days, last 30 days and last 90 days prior to sam-
pling), with only eight nonshared candidate SNPs
across data sets.
Collectively, a total of 754 potentially locally selected
SNPs were identified, only three of which were com-
mon to both FST-based and SNP-environment associa-
tion approaches. These three SNPs showed both strong
SNP-environmental correlations ( b a y e n v ) and increased
Fst relative to the reference-based threshold ( l o s i t a n
and b a y e s c a n ) . By contrast, 84 candidate loci exceeded
the reference-based significance threshold solely for the
b a y e n v test of environmental association, without being
significant outliers in FST.
When genomic position of the locally selected SNPs
was investigated, a hit with a gene was obtained for
39.8% of the SNPs. Thus, no hits were obtained for
60.2% of the SNPs, although 10.2% were located in
upstream (5000 bp) regions of the genes. Most hits
represented intronic regions (86.9%), with CDS and
exons representing only 7.8% and 5.3% of the hits,
respectively.
Among hits, 255 (65.4%) were associated with one or
more among 1476 unique GO terms, for a total of 2628
term occurrences. Subsequently, the KEGG pathway
approach for higher-order functional annotation was
implemented using the tool d a \ t d . Using zebrafish as
reference genome, a total of 335 zebrafish genes homol-
ogous to European eel were mapped to KEGG path-
ways. Enriched KEGG pathways using a standard
setting of gene count = 2 are summarized in Table 4.
The pathway with the highest number of genes was
neuroactive ligand-receptor interaction (eight genes),
including several genes implicated in behaviour such as
dopamine receptor, glutamate receptor subunit AMPA3
and alpha-lD adrenoreceptor. Other pathways of partic-
ular interest were calcium signalling pathway (six
genes) and circadian rhythm (two genes), including
PERIOD.
Finally, average FST values calculated using a 50-kb
sliding window were plotted for the 30 longest scaf-
folds (Fig. 4). Fst was low throughout the scaffolds,
with just a few narrow peaks. No regions of the
scaffolds with pronounced divergence peaks were
observed, consistent with panmixia removing any effect
of diversifying selection from each new generation.
Similar results were obtained when using altemative
(10 0 and 200 kb) sliding windows.
D iscu ssion
Further evidence for genomic panmixia
This study represents the first high-density SNP-based
genome scan of genetic diversity and differentiation in
(© 2014 Jo h n W iley & S ons L td
2522 J. M. P U JO L A R E T A L .
Table 4 K EG G pathways and genes identified using the Fst outlier approach implemented in lositan/bayescan and by testing for
associations with environmental variables in bayenv
KEGG p a th w a y G en e A p p ro a c h
C alc iu m s ig n a liin g p a th w a y A T P ase , C a++ tra n sp o rtin g , ca rd iac m u sc le , s lo w tw itch 2a Fst o u tlie r
C a lc iu m ch an n e l, v o lta g e -d e p en d e n t, L type , a lp h a 1S s u b u n it F s t o u tlie r
C a lc iu m ch an n e l, v o lta g e -d e p en d e n t, L ty p e , a lp h a 1S s u b u n it, a FST o u tlie r
S im ila r to N -m e th y 1-D-aspartate re c ep to r c h an n e l s u b u n it ep s ilo n 1 Fst o u tlie r
S im ila r to N e u ro m e d in -K re c e p to r (NKR) F g r o u tlie r
S im ila r to a lp h a - lD a d re n o re ce p to r Fst o u tlie r
N e u ro a c tiv e l ig a n d - re c e p to r D o p a m in e re c ep to r D1 Fst o u tlie r
in te ra c tio n G a m m a -a m in o b u ty ric acid (GABA) A re c ep to r , a lp h a 1 Fst o u tlie r
G lu ta m a te re c ep to r, io n o tro p ic , A M P A 4b; g lu ta m a te recep to r,
io n o tro p ic , A M P A 4a; g lu ta m a te re c ep to r, io n o tro p ic , A M P A 2a;
g lu ta m a te recep to r, io n o tro p ic , A M P A lb ; g lu ta m a te recep to r,
io n o tro p ic , A M P A la ; s im ila r to g lu ta m a te re cep to r, io n o tro p ic , A M P A
4; g lu ta m a te re c ep to r, io n o tro p ic , A M P A 3b; g lu ta m a te re c ep to r,
io n o tro p ic , A M P A 3a
Fst o u tlie r
P y rim id in e rg ic re c e p to r P2Y, G -p ro tem co u p le d , 4-like Fst o u tlie r
S im ila r to a d e n o s in e A1 re c ep to r Fst o u tlie r
Focal a d h e s io n In teg rin , a lp h a 5 F s t o u tlie r
P h o s p h a ta s e a n d te n sin h o m o lo g B BAYENV
T alin 1 Fst o u tlie r
V -crk sa rco m a v iru s CT10 o n co g en e h o m o lo g (av ian )-like Fst o u tlie r
V -raf m u r in e sa rco m a v ira l o n co g en e h o m o lo g B1 F s t o u tlie r
C a lp a in 2, (m /II ) la rg e s u b u n it, like Fst o u tlie r
W n t s ig n a llin g C -te rm in a l b in d in g p ro te in 2 Fst o u tlie r
M A D h o m o lo g 2 (D rosoph ila ) F g - f o u tlie r
S ec re ted fr iz z led -re la ted p ro te in 1 F s t o u tlie r
W in g le ss -ty p e M M T V in te g ra tio n s ite fam ily , m e m b e r 7b F g r o u tlie r
W in g le ss -ty p e M M T V in te g ra tio n s ite fam ily , m e m b e r 8b F s t o u tlie r
M u c in - ty p e O -g ly c an b io sy n th e s is U D P -N -ace ty l-a lpha-D -galactosam ine: p o ly p e p tid e N -
a ce ty lg a lac to sam in y ltran sfe ra se 7
BAY EN V
W D re p e a t d o m a in 51B, like BAYENV
C irc a d ian rh y th m P e rio d c irca d ian p ro te in h o m o lo g 2 BAYENV
P erio d c ircad ian p ro te in hom olog -Iike 2 Fst o u tlie r
K EG G , K yo to E n c y c lo p e d ia o f G en es a n d G enom es.
the European eel. AIl analyses of genetic diversity,
genetic differentiation and isolation by distance are con-
sistent with the interpretation of genomic panmixia that
European eels sampled along the coasts of Europe and
northem Africa belong to a single spatially homogenous
population. The low levels of genetic differentiation in
our study, revealed by both nuclear (FST = 0.0007) and
mitochondrial loci (FST = 0.0002), are concordant with
the recent study of Als et al. (2011), the most extensive
study to date in terms of spatial sampling, which
showed nonsignificant genetic differentiation among
samples using 21 microsatellite loci, with an FST value
of 0.00076 among larvae in the Sargasso Sea and
0.00024 among glass eels samples across Europe. Very
low mean FST values have also been reported in all
other studies on European eel that included large num-
bers of sampling sites and individuals (e.g. Wirth &
Bernatchez 2001: FST = 0.0017; Dannewitz et aí. 2005:
Tst = 0.0014; Maes et al. 2006: FST = 0.0099), the only
© 2014 John Wiley & Sons Ltd
exception being a recent study showing a microsatellite
Fst value of 0.02 (this about 10 times more than
reported in other studies) and a mitochondrial FST of
0.11 (Baltazar-Soares et al. 2014).
Random matmg and larval dispersal may lead to the
lack of spabal structure found in European eel despite
its broad geographical distribution from Iceland to
Morocco. While congregating at a single dominant
spawning site could lead to panmixia, the vastness
(c. 3 x 106 km2) and heterogenous hydrographic struc-
ture of the Sargasso Sea plus changes in oceanographic
conditions caused by ocean-atmospheric regime shifts
may affect the location of spawning areas by silver eels
(Friedland et al. 2007). Based on the occurrence of eel
larvae, it has been proposed that particular thermal
fronts within the subtropical convergence zone charac-
terized by steep temperature and salinity gradients
are used by eels to locate spawning areas and facih-
tate mating (McCIeave 1993; Munk et al. 2010).
LOCA L S EL E CT IO N IN THE E U R O P E A N EEL 2523
scaffoldl scaffold11 scaffold14 scaffold141 scaffold142 scaffold178
Ö.Ö15 -
0.010 - ,
aooo-i'Ayv^ ^ J 'S /'V
-0.005 -
-0 .0 1 0 -
u j V A f r w A v ' V \
scaffold196 scaffold2 scaffold21 scaffold24 scaffold254 scaffold27
0.015 -
0.010 - .
0.005 - V A
0.000 - \
-0.005 -
-0.010 -
iAAâ / '
scaffold3 scaffold30 scaffold31 scaffold34 scaffold36 scaffold4
0.015 -
0.010 -
S 0.005 - / \
0.000 - \ J
-0 .005 -
-0.010 -
V V ^ / V A a,
scaffold46 scaffold5 scaffold54 scaffoldð scaffold63 scaffold68
0.010
0.005
0.000
-0.005
-0.010 ■
0.015 •
0.010 ■
0.005 ■
0.000 •
-0.005 ■
-0.010 •
scatfold7 scaffol
'V 'A u ^ v \
scaffold84 scaffold90
■ i i i i i i i
500 1000 1500 2000 500 1C00 1500 2000
lots of average FSt calculated using a 50-kb
i i i i i i i i i i i i i i i i
500 1000 1500 2000 500 1000 1500 2000 500 1000 1500 2000 500 1000 1500 2000
bp (x1000)
s lid in g w in d o w fo r th e 30 lo n g est sca ffo ld s in th e E u ro p ea n eel g en o m e.
Hydrographic profíling studies show that the position
and strength of the thermal fronts are highly variable
and unstable (Munk et al. 2010), which suggests no pos-
sibilities of philopatry of adults to the original birth-
place within the Sargasso Sea and hence random
mixing of individuals. In regard to larval dispersal,
despite circulation patterns and oceanic currents in the
Atlantic Ocean bemg complex, it is well established that
European eel larvae are advected towards Europe fol-
lowing the Gulf Current and the North Atlantic Current
(Lecomte-Finiger 1994). An alternative shorter transat-
lantic journey following the Subtropical Counter Cur-
rent towards the Azores and Europe has been proposed
for southern European eels (Munk et al. 2010) that
would explain the observed highly significant heteroge-
neity in size and condition between Mediterranean and
North European glass eels (Pujolar et al. 2007), with
Mediterranean samples showing smaller size and condi-
tion. A shorter transatlantic migration route for Medi-
terranean larvae was also indicated in the modelling
study of Kettle & Haines (2006). The putative existence
of different larval migratory routes contrasts with the
lack of spatial genetic structure in our study, in which
European eel samples were compared with the largest
number of markers to date. In accordance with Als et al.
(2 0 1 1 ), this seems to indicate that larval migration is
random and that any segregation of individuals that
might occur in the Sargasso Sea (either spatial or tem-
poral) is not reinforced by larval homing to the parental
original freshwater habitat.
Low occurrence of hybrids irt Europe
Our study identified a total of 214S SNP markers that
were diagnostic betw'een European and American eels
(F s t = 1 a s they were fixed for different alleles), which
were used for hybrid identification. Admixture analysis
showed a low level of hybridization, with three hybrids
among European glass eels (two in Iceland and one in
Gironde) and one single hybrid among American eels.
We observed a hybrid occurrence of 5.9% in Iceland
that fits the values found in previous studies, ranging
from 2^4% to 15.5% (Avise et al. 1990; Albert et al. 2006;
Pujolar et al. 2014). By comparison, four out of 225
(1 .8 %) individuals were identified as hybrids in main-
land Europe, one individual with a 0.05 admixture pro-
portion and three individuals with a 0.03 admixture
proportion. The low occurrence of hybrids in mainland
Europe is in agreement with the recent study of Als
et al. (2011) that identified 0.2% of hybrids (one in Ire-
land and one in Belgium) using 21 microsatellites. Col-
lectively, our data corroborate previous findings that a
moderate percentage of Icelandic eels have American
eel ancestry, showing that a much lower percentage of
eels in mainland Europe is of admixed origin.
The low occurrence of hybrids in mainland Europe
also suggests strong natural selection against hybrids.
As a consequence of reduced hybrid viability and/or
fertility, hybridizing individuals usually experience
several costs that result in selection against heterospeci-
fic pairing (i.e. development instability; Coyne & Orr
© 2014 Jo h n W iley & S ons Ltd
2524 J. M. P U JO L A R ET AL .
2004). Recently, Gagnaire et al. (2012b) identified a pos-
sible cytonuclear incompatibility between North Atlan-
tic eels after showing that positive selection has
operated on both the mitochondrial atpó gene and its
nuclear interactor atp5cl. However, our data show that
individuals presenting the nuclear genome of one spe-
cies and the mitogenome of the other species are viable.
One individual from Lough Erne (Northem Ireland)
presented a pure European nuclear genome, but an
American mitogenome. The reverse pattern was also
observed, and European eel mtDNA was found in an
individual with a pure American nuclear genome. This
suggests that, albeit rare and sporadic, hybridization
over several generations is possible and can occur in
both directions.
Single-generation signatures of selection
Considering the high historical effective population size
estimated for the European eel (from 100 000 to 1 x 106
individuals; Pujolar et al. 2013), random drift is expected
to be negligible, while natural selection (together with
gene flow) would be the major force determining allele
frequency differences, in a patteni that is expected to
vary from locus to locus. Effectively, the great majority of
SNPs in our study showed no appreciable differences in
allele frequencies among sampling locations, whereas a
small set of SNPs showed significantly high genetic
differentiation, consistent with the action of natural
selection.
The low levels of baseline differentiation ( F S t of
0.0007) found in the European eel with no highly differ-
entiated genome regions except a few narrow peaks
suggest that most of the genome is homogenized by
gene flow. When gene flow is high, strong divergence
selection acting directly on individual target genes that
diverge independently from other genes is expected
(i.e. direct selection with no hitchhiking), while genomic
islands of divergence due to genome hitchhiking are
expected in the case of reduced gene flow (Feder et al.
2012). The observation of single points of selection
rather than regions (islands) under selection in our
study is in agreement with panmixia in the European
eel.
After screening over 50 000 SNPs with a minor allele
frequency >0.05, we identified several candidate genes
possibly undergoing divergent selection associated with
the highly variable environmental conditions used by
the European eel along its geographical range. Our
results are in accordance with the study of Gagnaire
et al. (2012a) in American eel, which showed significant
correlations between allele frequencies at 13 loci and
the same variables used in our study (temperature,
latitude and longitude).
We found large variation betw'een the approaches
used (Fst outlier vs. environment association methods),
and few7 SNPs were identified as targets of local selec-
tion by both methods. This is in agreement with recent
studies in which genes that showed positive SNP-envi-
ronment associations were not outliers in analyses of
population structure (Hancock et al. 2010; Ma et al.
2010; Keller et al. 2012), which suggests that the SNP-
environment association approach is more sensitive to
subtle/gradual shifts in allele frequencies and may be
complementary (rather than concordant) to FST-based
outlier methods when testing for selection (Coop et al.
2010). Nevertheless, some of the putative targets of local
selection in our study showed both high FST and SNP-
environment associations, including genes in two
important pathways, calcium signalling and circadian
rhythm.
Calcium serves a number of functions in fish and
controls processes as diverse as fertilization, develop-
ment, learning and memory, mitochondrial function,
muscle contraction and secretion (Berridge et al. 2000).
It is also recognized as very important in ion exchange
and osmoregulation. Spatially varying selection in
regard to osmoregulation seems plausible in the Euro-
pean eel, because the species is facultatively catadro-
mous and can occupy either freshwater or salt water
(i.e. marine and brackish) habitats (Daverat et al. 2006).
Within the circadian rhythm pathway, the gene that
showed the strongest and most consistent evidence for
local selection across all analyses was the central circa-
dian gene PERIOD (per), showing both a highly
increased population differentiation in the outlier FST
approach and a strong pattern of covariance wdth two
environmental variables, temperature and latitude
(allele frequencies ranged from 0.12 in Ringhals to 0.02
in the Mediterranean locations and Morocco). Many
organisms exhibit circadian rhythms based on 24-h
intervals regulated by endogenous biochemical
oscillators or clocks that enable organisms to organize
physiological and behavioural processes to occur at bio-
logically advantageous times in a day (Hastings et al.
1991). Changing photoperiod lengths can also be an
important environmental cue controlling seasonal activi-
ties. Clocks can be synclironized with environmental
factors, most notably changes in temperature and light
intensity, which is consistent with the statistical associa-
tion in our study between PERIOD allele frequencies
and temperature and Iatitude. PERIOD could be under
local selection, in this case related to differences in local
photoperiod associated with the >30° difference in lati-
tude between the geographically most extreme locations
(Iceland vs. Morocco).
The remaining genes showed high FST but no SNP-
environment associations, including many genes associated
© 2014 Jo h n W iley & S ons Ltd
LOCAL S EL E CT IO N IN THE E U R O P E A N EEL 2525
with behaviour, namely dopamine receptor DRDl, glu-
tamate receptor subunit AMPA3 and alpha-lD adreno-
receptor. Dopamine and glutamate are neurotransmitters
mediating a wide range of actions, including stress and
aggressiveness and also locomotion and exploring
behaviour. Social behaviour related to aggressiveness
(agonistic behaviour) could be important for food acces-
sibility and size-related sex determination in eels.
Alpha-ID adrenoreceptors are also involved in a variety
of stimulus-induced changes in locomotor behaviours.
It should be noted that due to the methodological
approach used (i.e. RAD sequencing), SNPs under
selection could be underestimated because only a por-
tion of the restriction fragments will be located in actual
gene-coding regions.
Impossibility of local adaptation
High gene flow associated with the particular life his-
tory characteristics of eels prevents heritable trans-gen-
erational local adaptation. Genomic panmixia suggests
that larval dispersal is random and there is no larval
homing to the parental original freshwater habitat. As a
consequence, the offspring of surviving individuals
experiencing specific local conditions (e.g. high tempera-
ture) have no chance to retum to the parental habitat in
which the phenotype was originally advantageous and
selected for. Despite evidence for single-generation foot-
prints of spatially varying selection, local adaptation is
impossible in the case of eels and locally adapted SNPs
in a given generation may not be favoured by selection
in the next generation. In fish, a similar scenario in
which strong selection occurs in every generation was
suggested for lagoon populations of the European sea
bass Dicentrnrchus labrax (Lemaire et al. 2000). As spawn-
ing only occurs at sea, any adaptation to the lagoon
environment is Iost as surviving young adults migrate
from the lagoons to the open sea to mate with individu-
als from marine populations. Spatially and temporally
varying selection has also been reported previously in
several marine invertebrates, including blue mussel
(Mytilus edulis) (Koehn et al. 1976) and acorn bamacle
(Semibalanus balanoides) (Véliz et al. 2004).
The resilience of a species depends on its vulnerabil-
ity in the face of environmental changes, which can lead
to either genetic (local adaptation) or plastic (pheno-
typic plasticity) responses (Hoffmann & Willi 2008).
Heritable local adaptation can allow species to cope
with environmental variability. This has been shown in
the mummichog Fundulus heteroclitus, in which local
populations have evolved pollution tolerance allowing
them to survive concentrations of contaminants that are
lethal to populations from clean environments, in a
response that is not plastic but adaptive and heritable
(Nacci et al. 2010; Whitehead et al. 2011). Gagnaire et al.
(2012a) argued that locally selected polymorphisms are
not easily maintained by spatially varying selection in
the panmictic American eel and that under such condi-
tions phenotypic plasticity provides a more functionally
adaptive response to spatial environmental variation.
As such, high phenotypic plasticity could explain the
presence of eels in extremely heterogenous environ-
ments across Europe in terms of salinity, temperature,
substrate, depth or productivity, as well as the large
variance observed in life history traits such as age at
maturity or growth rate.
C onciusions
Analysis of hundreds of thousands of SNPs provides
compelling support for the notion that European eel is
a panmictic species. Panmixia at the genomic level
agrees with previous genetic studies using neutral
markers (microsatellites and AFLP) and is also concor-
dant with the hybrid ecological-genetic model of And-
rello et al. (2011). Mitochondrial SNPs in our study also
showed no differentiation (41 SNPs: Fsx = 0.0002),
which contrasts with the significant differences recently
reported by Baltazar-Soares et al. (2014), with a mito-
chondrial Fsx of 0.11. Reasons for such a high discrep-
ancy betvv'een studies are unclear; they might be related
to differences in sample sizes, but this clearly deserves
further investigation.
The results also demonstrate that the occurrence of
hybrids between European and American eel is rare
outside Iceland. Nevertheless, the extensive number of
SNPs allows for tracking hybridization several genera-
tions back in time and indicates the presence of intro-
gressed individuals that may contribute to genuine
gene flow between the species. Despite panmixia, some
genes are identified that are candidates for being under
local selection within generations. By considering their
functions and the ecological and geographical diversity
covered by the sampled sites, it is also biologically
plausible that they are indeed under selection.
Although phenotypic plasticity undoubtedly plays a
major role in the persistence of eels in a range of highly
variable environments, the present study and the
related study by Gagnaire et al. (2012a) of American eel
draw attention to the importance of spatially and tem-
porally varying selection in high gene flow organisms,
among which European and American eel represent
extreme cases. Future work directions include testing
whether the same genes are under spatially varying
selection in glass eels and yellow/silver eels or whether
the response involves a different set of genes. The latter
option seems plausible considering the different selec-
tive pressures that affect eels in early vs. late life stages.
© 2014 John W ile y & Sons Ltd
2526 J. M. P U JO L A R E T AL .
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m ix ia in the E u ro p e a n eel. N ature, 409, 1037-1040.
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J.M.P. and L.B. conceived and designed the
project. J.M.P., M.W.J., T.D.A., K.M. and M.M.H.
conducted bioinformatics and population genomics
analyses. J.B.J., L.C. and J.F. were involved in data gen-
eration. J.M.P. wrote the manuscript with contributions
from M.M.H., M.W.J., L.B., G.E.M., T.D.A., K.M., B.J.,
J.B.J., J.F. and L.C.
Data accessib ility
Sequence reads have been deposited in the NCBI
Sequence Read Archive (Project Number PRJNAl95555).
Raw SNP data and a custom-made script are available
from Dryad database (http://datadryad.org) under
doi:10.5061 /dryad.s8v7q.
Supporting inform ation
A dditional supporting inform ation m ay be found in the online ver-
sion o f this article.
Fig. S1 P lo ts from M u lti-D im e n s io n a l S ca ling a n a ly sis b ased
o n p a irw is e Fst v a lu e s c o n s id e rin g (a) all R A D seq u en ces a n d
(b) m ito c h o n d ria l R A D seq u e n c es on ly .
© 2014 John W ile y & Sons Ltd
http://datadryad.org
Heredity (2014), 1-11
© 2014 Macmillan Publishers Limited All rights reserved 0018-067X/14
www.nature.com/hdy
ORIGINAL ARTICLE
Assessing patterns of hybridization between North Atlantic
eels using diagnostic single-nucleotide polymorphisms
JM Pujolar1, M W Jacobsen1, TD Ais2,3, J Frydenberg1, E M agnussen4, B Jónsson5, X J ia n g 6,
L C heng7, D Bekkevold2, GE M aes8,9, L Bernatchez10 and MM H ansen1
The two North Atlantic eel species, the European eel (Anguilla anguilla) and the American eel (Anguilla rostrata), spawn in
partial sympatry in the Sargasso Sea, providing ample opportunity to interbreed. In this study, we used a RAD (Restriction site
Associated DNA) sequencing approach to identify species-specific diagnostic single-nucleotide polymorphisms (SNPs) and
design a low-density array that combined with screening of a diagnostic mitochondrial DNA marker. Eels from lceland
[N = 159) and from the neighboring Faroe Islands [N = 29) were genotyped, along with 94 larvae (49 European and 45
American eel) collected in the Sargasso Sea. Our SNP survey showed that the majority of lcelandic eels are pure European eels
but there is also an important contribution of individuals of admixed ancestry (10.7%). Although most of the hybrids were
identified as F1 hybrids from European eel female x American eel male crosses, backcrosses were also detected, including a
first-generation backcross (F1 hybrid x pure European eel) and three individuals identified as second-generation backcrosses
originating from American eel x F1 hybrid backcrosses interbreeding with pure European eels. In comparison, no hybrids were
observed in the Faroe Islands, the closest bodies of land to lceland. It is possible that hybrids show an intermediate migratory
behaviour between the two parental species that ultimately brings hybrid larvae to the shores of lceland, situated roughly
halfway between the Sargasso Sea and Europe. Only two hybrids were observed among Sargasso Sea larvae, both backcrosses,
but no F1 hybrids, that points to temporal variation in the occurrence of hybridization.
Heredity advance online publication, 15 January 2014; doi:10.1038/hdy.2013.145
Keywords: admixture analysis; anguilla; hybridization; RAD sequencing; SNPs
IN TR O DU CTIO N
T h e s tu d y o f h y b rid iza tio n b e tw een in d iv id u a ls fro m genetica ily
d is tin c t p o p u la tio n s o r species is o f co n sid e rab le in te re s t to u n d e r-
s tan d th e d y n a m ic s o f s p ec ia tio n a n d ad ap tiv e d ivergence (M allet,
1995; G ra n t a n d G ra n t, 2002; R ieseberg a n d W illis, 2007; H ew itt,
2011; S to ltin g e t ciL, 2013). In p a rticu la r, h y b rid zones are w idely
recogn ized as ‘w in d o w s’ o r ‘n a tu ra l la b o ra to rie s ’ fo r e v o lu tio n a ry
s tu d ie s co n ce rn in g m o d e ls o f sp ec ia tio n , selective fo rces invo lved in
sp ec ia tio n , gen e flow be tw een species a n d th e m a in te n an c e o f species
b o u n d a rie s (H e w itt, 1988, 2011; H a rr is o n , 1990; M allet, 1995; P e tit
a n d Excoffier, 2009). A key q u e s tio n in m a n y in s tan ces o f hyb rid iza -
t io n c o n ce m s w h e th e r h y b rid iza tio n is re s tric te d to F l h y b rid s a n d
f irs t-g en e ra tio n backcrosses a fte r w h ic h g enetic in c o m p a tib ilitie s a n d /
o r n a tu ra l se lec tion e lim in a te h y b rid ofifspring, o r i f h y b rid iza tio n
p ro ceed s to th e e x te n t th a t in tro g re ss io n o ccu rs (A lle n d o rf et a l ,
2001). In th e la t te r case, in c o m p le te re p ro d u c tiv e iso la tio n m ay have
im p o r ta n t b earin g s o n th e e v o lu tio n a ry tra jec to rie s o f species by
d ecreas ing d ivergence b e tw ee n species b u t a lso by a llow ing favourab le
n ew m u ta tio n s a n d allelic c o m b in a tio n s to tran sg ress species b o u n d -
aries. T h is h o ld s p a rtic u la r ly t ru e fo r pe lag ic m a rin e e n v iro n m e n ts
w h ere few o b v io u s physical b a rrie rs are p re s e n t a n d s p ec ia tio n -w ith -
g ene-flow processes m ay b e c o m m o n (F ed er e t «/., 2012).
A p ecu lia r p a tte m o f h y b rid iz a tio n is fo u n d in th e tw o N o r th
A tlan tic eel species, th e E u ro p ea n [A nguilla anguilla) a n d the
A m e rican eei (A. rostrata). B o th species show w id e d is tr ib u tio n
ranges, w ith th e E u ro p ea n eel b e in g fo u n d in th e e as te rn A tlan tic
fro m M o ro cco to lce land in c lu d in g th e M ed ite r ra n ea n Sea a n d the
A m erican eel b e in g fo u n d in th e w este rn A tlan tic fro rn th e C arib b ean
to G reen lan d . N o r th A tlan tic eels a re facu lta tively c a tad ro m o u s ,
sp aw n in g in p a rtia l sy m p a try in lro n ta l zo n es o f th e so u th e rn
Sargasso Sea. A fte r sp aw n in g , larvae (lep to c ep h ali) a re tra n s p o r te d
b y surface c u rre n ts o f th e G u lf S tream to th e sh o res o f E u ro p e /N o r th
Afirica a n d N o rtlr A m erica , respectively. W lien larvae reach th e
c o n tin e n ta l shelf, th e y u n d e rg o m e ta m o rp h o s is in to glass eels th a t
c o m p ie te th e m ig ra tio n in to fresh , b rac ld sh a n d coasta l w a ters as
yellow eels. A fter a h ig h ly va riab le feed in g p e rio d o f 5 -3 0 years, yellow
eels m e ta m o rp h o s e in to silver eels th a t m ig ra te fro m tlie ir h igh ly
d isp ersed fo rag ing areas to th e c o m m o n sp aw n in g g ro u n d in th e
Sargasso Sea, w h ere th e y re p ro d u c e o n ly o n ce a n d d ie (van den
T h illa r t e t al., 2009 ). M o lec u la r s tu d ie s in b o th species have
^Department of Bioscience, Aarhus University, Aarhus C, Denmark; 2National Institute of Aquatic Resources, Technical University of Denmark, Silkeborg, Denmark; 3Department
of Biomedicine-Human Genetics, Aarhus University, Aarhus C, Denmark; 4Faculty of Science and Technology, University oí the Faroe Islands, Torshavn, Faroe Islands; 5Biopol,
Marine Biology and Biotechnology Center, Skagastrond, lceland; 6BGI-Shenzhen, Shenzhen, China; 7BGI-Europe, Copenhagen Bio Science Park, Copenhagen, Denmark;
8Laboratory of Biodiversity and Evolutionary Genomics, Deberiotstraat 32, University of Leuven (KU Leuven), Leuven, Belgium; 9Centre for Sustainable Tropical Fisheries and
Aquaculture, School of Marine and Tropical Biology, James Cook University, Townsville, Queensland, Australia and 10IBIS (Institut de Biologie Intégrative et des Systémes),
Université Laval, Québec City, Québec, Canada
Correspondence: Dr JM Pujolar, Department of Bioscience, Aarhus University, Ny Munkegade 114, Building 1540, Aarhus 8000, Denmark.
E-mail: jmartin@blology.au.dk
Received 27 August 2013; revised 9 December 2013; accepted 10 December 2013
http://www.nature.com/hdy
mailto:jmartin@blology.au.dk
Hybridization between North Atlantic eels
JM Pujolar et at
d e m o n s tra te d th a t th e y a re p a n m ic tic (Als et a i , 2011; C ó té e t a l ,
2013 ). R em arkab iy , a lth o u g h m ito c h o n d r ia l D N A lineages o f th e tw o
species a re reciprocaU y m o n o p h y le tic (Avise e t a l , 1986), low
d iffe ren ta tio n is fo u n d a t m ic ro sa te llite loci, w ith Fyp values o f
0 .055 a n d 0 .018 re p o r te d in p re v io u s s tu d ie s (M a n k a n d Avise,
2003; W ir th a n d B ernatchez , 2003).
I t is w ell e s tab lish ed tlra t th e sp aw n in g g ro u n d s o f th e tw o species
o verlap in th e S argasso Sea a n d th e re is a lso overlap in sp aw n in g tim e ,
w ith th e A m erican eel sp aw n in g in F e b ru a ry -A p ril a n d th e E u ro p ea n
eel sp aw n m g in M a rc h - J u n e (M cC leave e t a l , 1987). E u ro p ean an d
A m erica n eels a re k n o w n to h y b rid ize b u t h y b rid s a re ob serv ed a lm o s t
exclusively in Iceland . T h e íir s t ev id en ce o f h y b rid s in Ice land cam e
fro m th e s tu d y o f Avise e t al. (1990) based o n a llozym es, m ito c h o n -
d ria l D N A m a rk e rs a n d v e rteb ra l c o u n ts th a t d e m o n s tra te d th a t
Ice lan d p o p u la tio n s in c lu d e h y b rid s in lo w freq u en c ies o f 2 -4 % . T he
lack o f d is c r im in a to ry p o w e r o f th e m a rk e rs u sed d id n o t a llow
d e te rm in in g th e s ta tu s o f h y b rid s a n d q u a n ti íy the ra te o f in tro g re s-
s ion . T h is w as a lso a p ro b le m in a la te r s tu d y u s in g m ic ro sa te llite loci,
a sc rib ed p rim a r ily to h o m o p la s y (M a n k a n d Avise, 2003). A m o re
ex tensive s tu d y o n th e s ta tu s o f eels in lce lan d w as c o n d u c te d u sing
a m p lifie d f rag m e n t le n g th p o ly m o rp h ism analysis o f eels s am p led a t
m u ltip le Ice land ic lo c a tio n s (A lbert et a i , 2006). T h e s tu d y revealed
an overaE h y b rid p ro p o r t io n o f 15.5% in Iceland , ran g in g ffo m 6.7 to
100% across lo ca tio n s, a n d th e occu i'rence o f h y b rid s b ey o n d th e first
g e n e ra tio n . H ow ever, th e m a rk e rs u sed w ere n o t ab le to classify la ter-
g e n e ra tio n (p o s t-F l) h yb rid s . H en ce , th e n a tu re o f in tro g ress io n in
Ice land ic eels re m a in s largely un reso lv ed . O u ts id e Ice land , o n ly few
h y b rid s have b e e n id en tifie d . A lb e rt e t al. (2006) observed n o hyb rid s
o u t o f 186 E u ro p e a n eels a n d 3 la te r-g e n e ra tio n h y b rid s o u t o f 193
A m erica n eels. Als e t a l (2011) id en tified a s ing le h y b rid a m o n g
S argasso Sea eel la rvae a n d tliree p u ta tiv e h y b rid s a m o n g E u ro p ean
glass eels, in c lu d in g o n e in d iv id u a l fro m Iceland . H ow ever, g iven the
l im ited re s o lu tio n o f availab le m a rk e rs , i t is u n c e r ta in w h e th e r
h y b rid iza tio n has b een u n d e re s tim a te d .
H e re , w e use a R A D (R e str ic tio n s ite A ssoc ia ted D N A ) seq u en c in g
a p p ro a c h (B aird e t al., 2008; H o h e n lo h e e t a i , 2010) to id en tify
s in g le -n u c leo tid e p o ly m o rp h ism s (S N P s) d iag n o stic fo r E u ro p ean a n d
A m erican eels. W e u se a su b se t o f th e se SN Ps to analyze p a tte rn s ,
d ire c tio n a lity a n d e v o lu tio n o f h y b rid iza tio n , w hereas a d e ta iled
analysis o f g en o m ic d ivergence be tw een th e species w ill be p resen ted
in a fo r th c o m in g p aper. Specifically, w e analyze eels fro m Ice land , the
N o r th A tlan tic F a ro e Is lan d s a n d th e sp aw n in g reg io n in th e Sargasso
Sea to ad d re ss th e foU ow ing q u e stio n s: (1) H as th e level o f
h y b rid iza tio n in p re v io u s s tu d ie s b een u n d e re s tim a ted ? (2) W h ich
h y b rid classes a re p re sen t; d o e s h y b rid iza tio n lead to in tro g re ss io n o r
is it re s tric te d to F I h y b rid s a n d p e rh a p s firs t-g en e ra tio n backcrosses?
(3 ) Is th e h ig h o c cu rre n ce o f h y b rid s re s tric ted to Ice land o r can
h y b rid s a lso b e fo u n d in th e n e ig h b o u r in g F aroe Islands th a t a re the
c losest b o d ie s o f la n d to Iceland? In a d d it io n to c la rify ing im p o r ta n t
aspec ts o f th e b io lo g y o f eels, th e re su lts w ill a d d to o u r u n d e rs tan d in g
o f sp ec ia tio n a n d h y b rid iza tio n processes in pelagic m a rin e
e n v iro n m e n ts .
MATERIALS AND M ETHO DS
Sampling
A total o f 50 pure N orth Atlantic eels, 25 European and 25 American eels, were
used for RAD sequencing and SNP discovery. All individuals were later
conlirm ed as pure species using the developed SNP markers. European eels
were collected usLng fyke nets at one location in the westem M editerranean,
Valencia (Spain), and two locations in the easlcm Atlantic, Bordeaux (Fmnce)
and Burrishoole (Ireland). American eels were collected along the western
Atlantic coast at Riviere Blanche (Quebec), Mira River (Nova Scotia) ;md
St Johns River (Florida). Genomic DNA was purified using standard phenol/
chloroform extraction.
A total o f 282 eels were included in the subsequent study o f hybridization.
Icelandic samples (jV = 159) were collected at 9 sites between 2000 and 2003,
covering most o f the known geographical distribution range o f the species in
Iceland, from Vatndalsa in the northern coast to Steinsmyrarfljot in the
southern coast (Figure I). The eels were not the same individuals analyzed by
Albert et a i (2006) and Gagnaire ct al. (2009), but they came from the sanie
samples. Sampling locations, life stages and num ber o f individuals sampled are
detailed in Table 1. Glass eels were caught by electrofishing, whereas yellow eels
were caught w ith traps. Samples firom the Faroe Islands (N = 29) were
collected at two locations (Grodiusvam and Kaldbaksbotnur) in 2011 using
fyke nets. The study was supplem ented w ith the analysis o f European and
American eel larvae collected in the Sargasso Sea during M arch-April 2007 as
part o f the Danish Galathea 3 expedition (for details see Als et al., 2011).
Samples o f the two species were collected at 37 stations covering 600 km o f the
Subtropical Convergence ffontal zone in the Sargasso Sea (64-70 'W and
24-30 JN) using a ring net o f diam eter 3.5 m equipped with a 25 m long net o f
560 pm mesh. A subset o f 94 larvac (49 European and 45 American eel) were
included in the present study (Table 2). DNA from ethanol-preserved larvae
was extracted using the EZNA kit (Omega Biotek, Norcross, GA, USA).
Individual larvae were initially identified as European o r American eel based
on the analysis o f the mitochondrial cytochrome b gene (Trautner, 2006).
RAD tag sequencing, RAD data analysis and SNP identification
Genomic DNA trom each individual was digested with restriction enzyme
EcoRI. All 50 individuals (25 European eels and 25 American eels) were
RAD-sequenced (10 individuals per lane) on an Illumina Genome Analyzer II
Figure 1 Sampling locations of European eels, including detailed locations
in lceland (labelled as in Table 1).
Heredity
Hybridization between North Atlantic eels
JM Pujolar e f al
Table 1 Details of genetic samples for North Atlantic eels including
sampling locations, code, geographic location, life stage, year of
sampling and number of individuals
Location Code Location Life stage Year N
lceland
Vatnsdalsá VA 65.49, -2 0 .3 4 Y 2000 10
Vogslækur VO 64.69, -2 2 .3 3 G 2001 27
Seljar SE 64.56, -2 2 .3 1 G 2001 10
Grafarvogur GR 64.15, -2 1 .8 1 Y 2003 10
Vifilsstadvatn VI 64.07, -2 1 .8 7 Y 2002 10
G 2001 33
Gríndavik GD 63.83, -2 2 .4 2 Y 2003 10
Olfus OL 63.93, -2 1 .6 2 G 2000 16
Stokkseyri ST 63.81, -2 1 .0 4 G 2001 10
Steinsmyrarfljot SM 63.61, -1 7 .9 2 Y 2000 23
Faroe Islands
Grothusvatn GV 61.84, -6 .8 3 Y 2011 15
Kaldbaksbotnur KA 62.06, -6 .9 1 Y 2011 14
Abbreviations: G, glass eels; Y, yellow eels.
Table 2 Details of larvae sampling in the Sargasso Sea including
transect, station, geographic coordinates and species sampled
Transect Station Lon. W Lat. N 44 AR
1 6 63.6 24.3 0 1
1 7 64.0 25.16 4 1
1 8 64.01 26.01 4 1
1 9 64.01 26.31 4 2
1 10 63.58 27.01 1 0
1 11 63.6 27.2 4 1
1 12 64.0 27.42 1 1
1 13 63.59 28.01 2 0
2 16 67.01 28.29 2 0
2 17 67.0 27.44 3 1
2 19 66.6 26.3 0 1
2 20 67.0 25.5 0 2
2 21 66.6 25.37 2 2
2 22 67.0 25.19 1 3
2 23 67.0 24.6 3 4
2 24 67.05 24.31 1 0
3 25 69.59 24.6 0 3
3 26 69.58 25.29 1 2
3 27 69.58 25.27 7 2
3 28 69.59 26.34 6 8
3 29 69.6 26.6 1 1
3 30 70.05 27.32 1 4
3 31 70.02 27.59 0 4
3 32 70.02 26.6 0 1
3 33 70.01 30.0 1 0
Abbreviations: AA. Anguilla anguilla-, AR, A. rostrata-. Lat., latitude; Lon., longitude.
by Beijing Genomics Institute (BGI, H ong Kong) using paired-end reads (for
details see Pujolar ct a l , 2013).
Sequence reads from the IUumina (San Diego, CA, USA) runs vvere sorted
according to barcode tag. Sequences were quality-filtered using FASTX-Toolkit
(http://hannoniab.cshl.edu/fastx_toolkit) and rcads with ambiguous barcodcs/
poor quality were removed ffom the analysis. A m inim um Phred score o f 10
(equivalent to 90% probability o f being correct) per nucleotide position was
chosen, meaning that reads were dropped if a -nucleotide position had a score
o f < 10. This is the Phred score generally used in SNP discovery studies (Van
Bers ct al., 2010; EUison et al., 2011; Scaglione e ta l , 2012; W agner et al„ 2012).
Final read length was trim m ed to 80 nucleotides in order to reduce sequencing
errors present at the tail o f the sequences. For subsequent analyses, only the
first (left) paired-read was used. The DNA fragments created by RAD tag
library preparation have a restriction site at one end and are random ly sheared
at the other end that results in each instance o f a restriction site sequence
being sampled many times by thc first rcads and the genomic DNA scqucnce
in the nearby region being randomly sampled at a lower coverage by the
second paired-end reads (Etter et a l, 2011), which are therefore less suitable
for caUing SNPs.
Sequence reads were aligned to the European eel genome draft (www.eel-
genome.com) (Henkel et aL, 2012) using the ungapped aligner Bowtie version
0.12.8 (Langmead ct al., 2009). A m aximum o f two mismatches between the
individual reads and the genome were allowed and alignments were suppressed
for a piuticular read when m ore than one reportable alignment existed, thereby
decreashig the risk o f paralogous sequences in the data.
The reference-aligned data were tlren used to assemble tlie RAD sequences
into loci and idcntify aUeles using thc ref_map.pl pipeline in Stacks version
0.9995 (Catchen et a i, 2011). First, exactly m atching sequences are aligned
together into stacks that are in turn merged to form putative loci. At each
locus, nucleotide positions are examined and SNPs are caUed using a
m axim um likelihood framework. Second, a catalog is created o f aU possible
loci and alleles. Third, each individual is m atched against the catalog. A
m inim um stack depth o f 10 reads was used, which is the num ber o f exactly
matching reads that must be found to create a stack in an individual. Finally,
the program Populations in Stacks was used to process aU the SNP data across
individuals. Loci were processed when present in both species in at least
66.67% of the individuals.
Genomc-wide measures o f genetic divcrsity, including obscrved (H0) and
expected (H e) heterozygosíties, were calculated at each nucleotide site for aU
individuals. Genetic differentiation between European and American eel
samples measured by was estimated for aU individual SNPs.
SNP low-density array design and scoring
Species-diagnostic SNPs were chosen to design a 96-SNP genotyping array on
the basis o f the following criteria: (1) a m inim um Fst value o f 0.95, (2) target
SNP is present along with no more than five additional singleton SNPs per
locus and (3) the presence o f at least lOObp llanking sequence when extending
the RAD loci using the European eel genome to allow for optimal prim er
design. SNPs meeting those criteria were labeUed as diagnostic for the purpose
o f the study, aldrough not 100% fixed. AU selected SNPs were distributed
across different scaffolds and contigs in the eel genome in order to guarantee a
good representation o f the genome.
SNPs were genotyped on 96.96 Dynamic Arrays (Fluidigm Coiporation, San
Francisco, CA, USA) using the Fluidigm EPl instrum entation and according to
the m anufacturer’s protocols. The Fluidigm system uses nano-fluidic circuitry
to simultaneously genotype up to 96 samples w ith 96 loci (see Seeb et a l, 2009
for a description o f the Fluidigm system methodology). Genotypes were called
and the data compiled using the Fluidigm SNP Genotv'ping Analysis software.
Each assay was assessed for plot quality and expected clustering patterns.
Hybrid identification
Hybrids were identified using STRUCTURE (Pritchard et a l, 2000) and
NEWHYBRIDS (Anderson and Thom pson, 2002). We used STRUCTURE to
estimate individual admixture proportions and their probabUity intervals. For
this purpose we assumed an adm ixture model, uncorrelated allele frequencies
and we did not use population priors. Given that two panmictic species were
analyzed, we assumed K — 2 and conducted 10 runs to check the consistency o f
results. A burn-in o f 100 000 steps followed by 1000 000 additional Markov
Chain M onte Carlo iterations were performed.
Rather than assigning individuals to a single hybrid category, NEWHY-
BRIDS uscs a Bayesian framcwork to com pute the posterior probability o f one
individual belonging to each parental and dislinct hybrid class (F l, F2 and
backcrosses between F1 x European eel and F1 x American eel). The genotype
Heredity
http://hannoniab.cshl.edu/fastx_toolkit
Hybridization between North Atlantic eels
JM Pujolar et al
frequency class file was expanded to include third-generation hybrid classes
originating from crosses between backcrosses and pure European eels, pure
American eels and F1 hybrids. The sofhvare was run for 100000 iterations in
the burn-in, followed by 100 000 M arkov Chain M onte Carlo iterations in each
analysis.
Before the analysis, the power o f the selected SNP markers to discriminate
hybrid status was assessed using HYBRIDLAB (Nielsen e ta l , 2006), a program
for generating simulated hybrids from population samples. Based on the
obscrved allelic frequencies at the selected SNPs in the European and Amcrican
eel baseline populations, the program generated 10000 random genotypes
o f each o f the following 12 categories: (1) pure European eel, (2) pure
American eel, (3) F1 hybrid, (4) F2 hybrid, (5) first-generation backcross
European eel x F1 hybrid, (6) first-generation backcross American eel x F1
hybrid, (7) second-generation backcross between -generation backcross
(European eel x F1 hybrid) and European eel, (8) second-generation backcross
between first-generation backcross (European eel x F1 hvbrid) and American
eel, (9) second-generation backcross between first-generation backcross
(European e e lx F1 hybrid) and F1 hybrid, (10) second-generation backcross
between first-generation backcross (American eel x F1 hybrid) and European
eel, (11) second-generation backcross between first-generation backcross
(American eel x F1 hybrid) and American eel and (12) second-generation
backcross between first-generation backcross (American eel x F1 hybrid) and
F1 hybrid. All simulated individuals were then blindly reassigned to their most
probable category using both STRUCTURE and NEWHYBRIDS.
RESULTS
RAD sequencing
S e q u en cin g o f th e R A D lib raries g e n e ra ted a n average o f 8.8 m illion
reads p e r in d iv id u a l o f 90 b p , be fo re any q u a lity filtering , ran g in g
fro m 4.4 to 13.4 m illio n reads. A fte r q u a lity filtering , o n average
7.3 m illio n (8 2 .7% ) seq u en ces p e r in d iv id u a l w ere re la in ed . R eta in ed
sequences p re sen te d a m e a n q u a lity sco re o f 38.5, a m e d ia n o f 39.2
a n d a G C c o n te n t o f 4 0 .6% , w ith n o a p p a re n t d ifferences o b served
b e tw een species (T able 3).
R eta in ed seq u en ces w ere a ligned to tlie E u ro p ea n eel d ra ft g enom e.
As expec ted , a h ig h e r n u m b e r o f E u ro p ean eel sequences a ligned
(67 .16% ) in c o m p a ris o n w ith A m e ric a n eel sequences (61 .33% ). T h e
n u m b e r o f sequences d isca rd ed b ecau se o f a lte m ativ e a lig n m en ts was
s im ila r fo r b o th species (1 .6% ; Table 3).
A ligned sequences w ere a ssem b led in to a n average o f 663 555 stacks
p e r in d iv id u a l a n d su b se q u en tiy in to a se t o f 322 314 loci. U sing a
m in im u m coverage o f 10 read s, an average o f 214 178 (66 .45% ) loci
w ere re ta in e d a n d 108,136 (33 .55% ) loc i w ere d isca rd ed p e r in d iv i-
d u a l because o f in su ffic ien t d e p th o f coverage. S im ilar n u m b e rs o f loci
w ere re ta in e d in b o th species (T able 3).
A cata log o f 502 526 loc i w as c o n s tru c ted u s in g ali in d iv id u a ls . A
to ta l o f 9 5 8 8 4 loci (19% ) sh a red b e tw een th e tw o species in a t ieast
66 .67% o f in d iv id u a ls p e r species w ere re ta in e d fo r S N P discovery.
U sing th e p ro g ra m P o p u la tio n s in Stacks, a to ta l o f 767 015 SN Ps
w ere id en tified . W h en ca lcu la tin g Es r values be tw een th e tw o species
fo r each SN P de te c ted , 3348 SN Ps sh o w ed a n FS p > 0 .9 5 .
SNP genotyping
S u p p le m e n ta ry Table 1 show s de ta ils o f 86 d ia g n o stic SN Ps fo r N o r th
A tlan tic eels a n d gives th e c o n 'e sp o n d in g allele frequencies fo r
E u ro p ea n a n d A m e ric an eel, to g e th e r w ith th e p o s itio n in th e
E u ro p ea n eel d ra f t g en o m e . W e exc lu d ed 10 m a rk e rs (o u t o f the
o rig in a l 96; 10.4% ) because o f p r im e r m is m a tc h o r in c o rre c t/m u ltip le
p ro d u c t am p lific a tio n . A to ta l o f 75 o u t o f 86 SN Ps (87 .2% ) h a d an
jFSt va lue o f 1.0 b e tw een E u ro p ea n a n d A m erican eei. T h e re m a in in g
9 SN Ps (12 .8% ) h a d an P ST o f 0 .9 5 -0 .9 6 .
Hybrid identification
In o rd e r to te s t the p o w e r o f th e m ark e rs , a to ta l o f 120 000
in d iv id u a ls w ere s im u la ted u s in g 86 SN Ps fo r 12 eel categories
in c lu d in g first- a n d s ec o n d -g e n e ra tio n backcrosses a n d reass igned
b lindiy . U sing S T R U C T U R E , a d m ix tu re p ro p o r t io n values ran g ed
fi'om 0 .995 (p u re E u ro p ean eel) to 0 .004 (p u re A m erican eel). F irst-
g en era tio n backcrosses sh o w ed u n iq u e a d m ix tu re p ro p o r tio n s (0.75
Table 3 Statistics describing the distribution of different properties of RAD sequences after each step of filtering (FASTX-Toolkit), alignment
to the eel draft genome (Bowtie) and assemblage into loci (Ref_map.pl)
FASTX
Species Raw reads Filtered reads % Eliminated Mean Q Q1 Med Q3 %A %C %G %T
All 8 8 1 0 898 7 2 81642 17.32 38.45 37.80 39.24 40 29.8 20.5 20.1 29.6
AA 8 76 9 8 31 7 007 835 19.92 38.36 37.72 39.10 40 29.7 20.5 20.1 29.6
AR 8 8 5 1 9 6 4 7 555450 14.72 38.53 37.88 39.37 40 29.8 20.5 20.1 29.6
Bowtie
Species Reads Aligned % Aligned Nonaligned % Nonaligned Discarded % Discarded
All 7 281642 4 707 002 64.25 2 504043 34.15 117 695 1.60
AA 7 0 0 7 8 3 5 4 768089 67.16 2 2 1 8 1 7 6 31.22 115152 1.63
AR 7 555450 4 6 4 5 9 1 5 61.33 2789 910 37.09 120238 1.58
R efjvap
Species Reads Stacks Loci Loci used % Loci used Loci discarded % Loci discarded
All 4 707 002 663 555 322314 214178 66.45 108136 33.55
AA 4 768089 745193 333871 224896 67.36 109 309 32.74
AR 4 6 4 5 9 1 5 581918 310756 203 638 65.53 107 118 34.47
Abbreviations: AA, Anguilla anguilla-, AR, A. rostrata; RAD, Restriction site Associated DNA.
Heredity
Hybridization between North Atiantic eels
JM Pujolar et al
a n d 0 .25). H ow ever, F1 a n d F2 h y b rid s a n d s ec o n d -g en e ra tio n
backcrosses c o u ld n o t b e co m p le te ly d is tin g u ish ed (F igu re 2). U sing
N E W H Y B R ID S , a co rre c t a ss ig n m e n t w as m a d e fo r 100% o f F1
h y b rid s , 89% o f F2 hy b rid s , 97% o f firs t-g en e ra tio n backcrosses a n d
9 4 -9 9 % o f se c o n d -g e n e ra tio n backcrosses (T able 4 ). T h is suggests
th a t o u r m a rk e rs have e n o u g h d is c r im in a to ry p o w e r to coiTectly
id en tify u p to th ird -g e n e ra tio n hyb rid s.
W h en th e e m p iric a l d a ta w ere e x am in ed w ith ST R U C T U R E ,
s im ila r resu lts w ere o b ta in e d across rep lic a te ru n s , il lu s tra tin g th a t
th e b ase line d a ta c o n sis tin g o f 25 E u ro p ea n a n d A m eric an eel cou ld
be c lassified w ith h ig h co n fid en ce (F igu re 3a). All Sargasso Sea larvae
id e n tif ie d as A m erican eel u s in g th e c y to c h ro m e b m ito c h o n d ria l
m a rk e r w ere suggested to b e n o n a d m ix e d . H ow ever, a m o n g p u ta tiv e
E u ro p ea n eel la rvae , tw o in d iv id u a ls w ere clearly h y b rid s , w ith
a d m ix tu re p ro p o r tio n s sug g estin g th a t th e y w ere sec o n d -g e n e ra tio n
backcrosses (F igu re 3a). All 29 in d iv id u a ls fro m F aroe Islands w ere
classified as p u re E u ro p ea n eels (F ig u re 3 b ). H ow ever, in Ice land , 142
in d iv id u a ls (89 .3% ) w ere p u re E u ro p ean eels, w h ereas 17 in d iv id u a ls
(10 .7% ) w ere classified as ad m ix e d w ith d iffe ren t degrees o f A m erican
eel an ce s try (F igu re 3 b ). O u t o f th e 17 ad m ix ed in d iv id u a ls ,
13 sh o w ed a 90% p ro b a b ility in te rv a l o v e rlap p in g 0.5, suggestive o f
e ilh e r F l o r F2 h y b rid s . T h e re m a in in g fo u r in d iv id u a ls sh o w ed
a d m ix tu re p ro p o r tio n s suggestive o f backcrosses.
A c o n firm a tio n o f th e in d iv id u a l s ta tu s catego ries o b ta in e d ffo m
ST R U C T U R E a n d a d e ta iled c lass ifica tion o f th e h y b rid s was
c o n d u c ted in N E W H Y B R ID S (T able 5 ). Id e n tif ic a tio n o f p u re a n d
h y b rid in d iv id u a ls c o rre s p o n d e d 100% to th e re su lts o b ta in e d
w ith ST R U C T U R E . All A m eric an eel la rvae w ere id e n tified as
p u re A m erican eels. O f th e E u ro p ea n eel larvae, 96% w ere p u re
E u ro p ea n eels, w hereas th e re m a in in g 2 in d iv id u a ls w ere id en tified as
sec o n d -g e n e ra tio n backcrosses b e tw een firs t-g en e ra tio n backcrosses
(A m erican eel x F1 h y b rid ) a n d p u re E u ro p ean eels. All F a roe Islands
B k k
A A b A A x A A b A A b A A x F I b A R x A A F1
0 .995 0 .8 7 2 0 .7 5 0 0 .6 2 5 0 .625 0 .500
F2 b A A xA R b A R x F I
0 .5 0 0 0 .375 0 .375
b A R b A R x A R A R
0 .2 5 0 0 .128 0 .004
0.001 0 .0 2 4 0 .028 0 .0 3 6 0 .023 0 .0 0 3 0 .0 3 7 0 .0 2 3 0 .0 3 6 0 .0 2 7 0 .0 2 3 0.001
Figure 2 Admixture analysis of simulated individuals in STRUCTURE. A total o f 12 categories were simulated: pure European eel (AA), pure American eel
(AR), F1 hybrid, F2 hybrid, first-generation backcross European eel x F1 (bAA), first-generation backcross American eel x F1 (bAR) and second-generation
backcrosses (b A A xA A , b A A x A R , b A A x F l , b A Rx AA , bAR x AR and bAR x F l) . Average admixture proportion value and s.d. values are presented for
each simulated category.
Table 4 Assignment probability of simulated individuals in NEWHYBRIDS
Assignment probability
AA AR F1 F2 bAA bAR bAA x AA bAA x AR bAA x F1 bAR x AA bAR x AR bAR x F1
AA
AR
1.000
1.000
i n n n
— — — - —
— —
—
—
r 1
F2 — —
J..U U U
0.885 — — _ _ 0.064 _ _ 0.052
bAA — — — — 0.971 — 0.019 — — 0.010 — —
bAR — — — — — 0.973 — 0.012 — — 0.014 —
bAAx AA — — — — 0.001 — 0.990 — — — — —
bAA x AR — — — — — 0.012 — 0.988 — — — —
bAAx F1 — — — 0.062 — — — — 0.937 — — —
bAR x AA — — — — 0.013 — — — — 0.987 — —
bARxAR — — — — — 0.009 — — — — 0.991 —
bAR x F1 — — — 0.068 — — — — — — - 0.932
A total of 12 categories were simulated: pure European eel (AA), pure American eel (AR), F1 hybrid, F2 hybrid, first-generation backcross European eel x F1 (bAA), first-generation backcross
American eel x F1 (bAR) and second-generation backcrosses (bAA x AA, bAA x AR, bAA x F l , bAR x AA, bAR x AR and bAR x F l) .
Heredity
Hybridization between North Atlantic eels
JM Pujolar et al
European eel
< ►
E u r o p e a n e e l l a r v a e
Am erican eel American eel larvae
M---------- M --------------------------- ►
20 40
Faroe Islands Iceland
Individual no.
Figure 3 Admixture analysis in STRUCTURE, assuming the presence of two groups (K = 2); European and American eels. Individual admixture proportions
along with 95% credible intervals are shown for each individual. Top panel shows baseline individuals of European eels and American eels followed by
American eel larvae and European eel larvae from the Sargasso Sea. Bottom panel shows eels from the Faroe Islands and from lceland.
Table 5 Assignment probability in NEWHYBRIDS of all lcelandic and Sargasso Sea hybrids
Location Individual Assignment probability
AA AR F1 F2 bAA bAR bAA X AA bAA X AR bAA X F1 bAR x AA bARxAR bARx F1
VA VADA-1 0.000 0.000 1.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000
VA VADA-2 0.000 0.000 1.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000
VO VOGG-11 0.000 0.000 1.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000
VO VOGG-5 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000 1.000 0.000 0.000
VO VOGG-9 0.000 0.000 1.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000
SE SSG-10 0.000 0.000 1.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000
SE SSG-7 0.000 0.000 1.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000
VI VFG-9 0.000 0.000 1.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000
VI VIFIG-2 0.000 0.000 1.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000
VI VIFIG-5 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000 1.000 0.000 0.000
OL OLFG-5 0.000 0.000 1.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000
ST STG-2 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000 1.000 0.000 0.000
ST STG-3 0.000 0.000 1.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000
SM STEG-1 0.000 0.000 1.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000
SM STEG-31 0.000 0.000 1.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000
SM STEG-38 0.000 0.000 1.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000
SM STEG-40 0.000 0.000 0.000 0.000 0.983 0.000 0.000 0.000 0.017 0.000 0.000 0.000
Sargasso L-125 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000 1.000 0.000 0.000
Sargasso L-211 0.000 0.000 0.000 0.000 0.005 0.000 0.000 0.000 0.000 0.995 0.000 0.000
Categories include pure European eel (AA), pure American eel (AR), F1 hybrid, F2 hybrid, first-generation backcross European eel x F1 (bAA), first-generation backcross American eel x F1 (bAR)
and second-generation backcrosses (bAA x AA, bAA x AR, bAA x F l, bAR x AA, bAR x AR and bAR x F l) . Locations are labelled as in Table 1.
in d iv id u a ls w ere c o n íirm e d as p u re E u ro p ea n eels. W ith respec t to
Iee lan d ic in d iv id u a ls , NEWHYBRJLDS c o n firm e d th e re su lts f ro m
ST R U C T U R E (142 p u re E u ro p ea n eels a n d 17 h y b rid s ). O u t o f 17
ad m ix ed in d iv id u a ls , 13 w ere F1 h y b rid s w ith a p ro b a b ility o f
P = 1.00. T h e fo u r la te r-g e n e ra tio n h y b rid s id en tif ie d in c lu d ed
o n e firs t-g en e ra tio n backcross b e tw een p u re E u ro p ea n eel a n d F1
Heredity
Hybridization between North Atlantic eels
JM Pujolar et al
h y b rid , w hereas th e re m a in in g th re e in d iv id u a ls rep re sen ted
s ec o n d -g e n e ra tio n back cro sses b e tw een f irs t-g en e ra tio n backcrosses
(A m erican eel x F1 h y b rid ) a n d p u re E u ro p e a n eels.
A cross lo ca tio n s in Ice land , h y b rid s w ere d e te c te d in 7 o u t o f
9 lo ca tio n s (F igu re 4 ), in c lu d in g th e n o r th e rn m o s t (V atnsdaisá) a n d
s o u th e m m o s t (S te in sm y ra rfljo t) lo c a tio n s , w ith a p ro p o r t io n ran g in g
fro m 5 to 20% . O n ly a t tw o lo c a tio n s (G ra fa rv o g u r a n d G rin d av ik )
w ere all in d iv id u a ls id en tified as p u re E u ro p ea n eels. F1 h y b rid s w ere
fo u n d in all lo c a tio n s in w h ic h h y b rid s w ere p re sen t, w hereas
backcrosses w ere fo u n d a t fo u r lo c a tio n s (V ogslæ kur, V ifilstadvatn ,
S tokksey ri a n d S te in sm y ra rf ljo t) . A cross life stages, tlre p ro p o r t io n o f
hy b rid s ra n g e d fro m 9 to 20 % in glass eels a n d fro m 0 to 20% in
yellow eels.
W e f ii r th e r ex p lo red th e n a tu re o f th e six in d iv id u a ls id en tified as
la te r-g e n e ra tio n h y b rid s (fo u r Ice land ic in d iv id u a ls a n d tw o Sargasso
Sea larvae) b y c o m p a rm g th e o b se rv ed p ro p o r t io n o f h e te ro zy g o te
loci a t eac h in d iv id u a l w ith th e e x p ec te d p ro p o r t io n in first-
g e n e ra tio n backcrosses (E u ro p e an e e l x F l ) a n d s ec o n d -g en e ra tio n
100i ---- ---- ---- ---- ---- ---- ---- ---- ----
8 0 -
Jfí
« 6 0 -
•o
'>
VA VO SE GR VI GD OL ST SM
Sam pling location
Figure 4 Proportion of pure European eels (light grey), F1 hybrids (dark
grey) and later-generation hybrids (black) in all lcelandic locations, labelled
as in Table 1.
b ackcrosses be tw een firs t-g en e ra tio n backcrosses (A m erica n eel x F l )
an d E u ro p ean eels (F igu re 5 ), u s in g th e s im u la ted d a ta fro m
HYBRIDLAB. In a cco rd an ce w ith N E W H Y B R ID S , o n ly o n e in d iv i-
du a l f ro m Iceland clearly p re sen ted a n ob serv ed h e te ro zy g o sity vvithin
th e ex p ec ted values fo r fir s t-g en e ra tio n backcrosses (E u ro p e an Eel x
F l) . T h e re m a in in g th re e in d iv id u a ls fro m Ice la n d p re sen te d m u ch
h ig h e r h e te rozygosity values th a n firs t-g en e ra tio n backcrosses, con -
c o rd a n t w ith seco n d -g e n e ra tio n backcrosses b e tw een f irs t-g en e ra tio n
backcrosses (A m erican eel x F l ) a n d p u re E u ro p ea n eels. O b se rv ed
heterozygosities fo r th e tw o Sargasso la rvae fitted th e e x p ec ta tio n fo r
sec o n d -g e n e ra tio n backcrosses b u t w ere a lso w ith in th e 5% u p p e r-
m o s t d is tr ib u tio n o f fir s t-g en e ra tio n backcrosses.
ln a d d itio n to S N P g en o ty p in g , all in d iv id u a ls w ere id en tified as
E u ro p ean o r A m erican eel o n th e basis o f th e m ito c h o n d ria l
cy to c h ro m e b gene. A ll h y b rid in d iv id u a ls (2 E u ro p ea n eel larvae
fro m th e Sargasso Sea a n d 17 Ice land ic in d iv id u a ls ) sh o w ed th e
E u ro p ean eel m ito c h o n d ria l h ap lo ty p e . S u rprising ly , 1 in d iv id u a l o u t
o f th e 142 Ice land ic in d iv id u a ls id en tified as p u re E u ro p ean eels (o n
th e basis o f th e SN P a rra y w ith a 100% p ro b a b ility u s in g b o th
ST R U C T U R E a n d N E W H Y B R ID S ) p re sen te d th e A m eric an eel
m ito c h o n d ria l h ap lo ty p e .
DISCUSSION
Species-diagnostic markers for detecting hybridization
T h e g rea te r cap ac ity to analyze g e n o m e -w id e p a tte rn s o f v a ria tio n
u s in g g e n o ty p in g -b y -seq u e n c in g ap p ro a ch e s has im p ro v ed th e m eans
o f id en tify in g h y b rid s a n d e x am in in g th e genetic a n d ev o lu tio n a ry
co n sequences o f species h y b rid iza tio n . U sing a n a rray o f d ia g n o stic
R A D -genera ted SN Ps w ith h ig h e st F s t va lues b e tw een E u ro p ean a n d
A m erican eel, w e w ere ab le to reh ab ly id en tify h y b rid s u p to th e th ird
gen era tio n . S im u la tio n s sh o w ed a h ig h d is c r im in a to ry p o w er o f th e
m ark ers , as w e w ere able to co rrec tly id en tify 100% o f F1 hy b rid s a n d
99% o f backcrosses w ith p u re p a re n ta l species. O u r re su lts co n firm
th a t SN Ps are effective m a rk e rs to s tu d y h y b rid iza tio n a n d de tec t
in tro g re ss io n (H o h e n lo h e et a l , 2011, 2013; A m ish e t a l., 2012;
N u ssb e rg e r e t aL, 2013). B ecause o f th e ir re la tively lo w m u ta tio n ra te
a n d co n se q u en tly low n u m b e r o f alleles, SN Ps a re m o re likely to b e
d iag n o stic loci th a n h ig h ly p o ly m o rp h ic m a rk e rs such as m ic ro -
sate llites th a t p re sen t a h ig h e r p ro b a b ility o f allele sh a r in g betw een
re la ted species d u e to h o m o p la sy (B alloux a n d G o u d e t, 2002 ).
Expected proportion
of he te ro zyg o u s loci o u r w ca
J ó ó ó
V _ i _ i
S >«/) >
Figure 5 Comparison of observed and expected proportion of heterozygous loci in (1) first-generation backcrosses European eel x F1 (dark grey) and
(2) second-generation backcrosses between first-generation backcrosses American eel x F1 hybrid and European eels (light grey) based on 10000 simulated
individuals per category using HYBRIDLAB. Arrows indicate observed proportion of heterozygous loci.
Heredity
Hybridization between North Atlantic eels
JM Pujolar e f a/
Has hybridization in North Atlantic eels been nnderestimated?
T h e h ig h d is c r im in a to iy p o w er o f th e set o f d iag n o stic loci allow s us
to ad d re ss th e q u e s tio n o f w h e th e r p rev io u s s tu d ies have u n d e r-
e s tim a te d th e n u m b e r o f h y b rid s b e tw ee n th e tw o species. T h is seem s
o n ly to a m in o r e x te n t to be th e case. Als e t al. (2011) id en tified a
s ing le h y b rid a m o n g la rvae co llec ted in th e Sargasso Sea, w hereas the
p re sen t s tu d y id e n tifie d tw o h y b rid s a m o n g a su b sa m p le o f th e sam e
larvae, b o th sec o n d -g e n e ra tio n backcrosses. A n eel la rvae s u n 'e y
c o n d u c te d in th e S argasso Sea in M a rc h -A p r il 2007 d u r in g th e
D a n ish G a la th ea 3 m a r in e e x p ed itio n , f ro m w h ich th e la rvae in c lu d e d
in o u r s tu d y are d e riv ed , shovved b o th species c o o ccu rr in g a t m o s t o f
th e 37 sam p lin g s ta t io n s d is tr ib u te d a lo n g th e lo n g itu d e s 64 W,
65 °W , 6 7 c W a n d 7 0 ' W b e tw een 24 a n d 30° la titu d e , w ith A m erican
eel b e in g p re d o m in a n t in th e W est a n d g rad u a lly b e in g rep laced by
E u ro p ea n eel to w a rd s th e E ast (Als e t a l , 2011). N evertheless, th e
o b se rv a tio n in o u r s tu d y o f o n ly 2 p u ta tiv e h y b rid s o u t o f 96
in d iv id u a ls (2 .0 6 % ) does n o t s u p p o r t tlie ex istence o f a d is tin c t
m a r in e h y b rid zo n e w h e re th e tw o N o r th A tlan tic eel species adm ix .
F u r th e rm o re , th e tw o la rvae id e n tif ie d as h y b rid s w ere sam p led a t
s ta t io n s > 600 k m a p a r t: o n e h y b rid w as co llected a t lo n g itu d e 64 °W /
la titu d e 27.42 °N in tlre m id -e a s te rn S argasso Sea, w hereas th e o th e r
h y b rid w as co llected a t lo n g itu d e 6 9 .6 'W /la t i tu d e 26 °N in th e
w este rn Sargasso Sea.
I t is su rp ris in g th a t th e tw o h y b rid s fro m th e Sargasso Sea w ere
s e c o n d -g e n e ra tio n backcrosses, w h ereas n o F l h y b rid s o r first-
g e n e ra tio n backcrosses w ere observ ed . O n e possib le e x p la n a tio n co u ld
b e th a t th e o c cu rre n ce o f h y b rid iza tio n d iffers b e tw een years, a p a tte rn
th a t h a s p rev io u s ly b e en suggested to exp la in te m p o ra lly v a ry in g
p ro p o r t io n s o f h y b rid s o b se rv ed in Ice lan d (Avise et a l , 1990; A lbert
e t a l , 2 0 0 6 ). T h is c o u ld be because o f d ifferences in te m p o ra l overlap
o f sp aw n in g t im e be tw een th e species across years, possib ly m ed ia ted
b y a m o re s o u th e rn o r n o r th e rn d isp la ce m e n t o f th e rm a l fro n ts across
years. In d e ed , th e th e rm a l fro n ts w h e re eels a re a ssu m ed to spaw n
s h o w c o n sid e ra b le d ifferences in in te n s ity a n d geog rap h ica l p o s itio n
b e tw ee n years (M u n k e t a l , 2010).
N o h y b rid s w ere d e te c te d in th e F a roe Islands. In the case o f
Ic e lan d ic eels, th e set o f d ia g n o stic m a rk e rs co n firm s th a t hyb rid s
a re c o m m o n . T h e p ro p o r t io n o f hybi'id in d iv id u a ls fo u n d in o u r
s tu d y (1 0 .7% ) is lo w er th a n th e values re p o r te d by A lb e rt e t al. (2006)
u s in g am p lified frag m e n t le n g th p o ly m o rp h ism m ark e rs (15 .5% ).
H ow ever, th e h ig h e r p ro p o r t io n o f h y b rid s in th e la tte r s tu d y
m ig h t be b e cau se o f th e d iffe ren t lo c a tio n s sam p led across s tud ies.
T h e tw o lo ca tio n s w ith th e h ig h e s t p e rcen tag e o f hy b rid s in th e
s tu d y o f A lb e rt e t al. (2006) w ere n o t in c lu d e d in o u r s tudy : th e
n o r th e a s te rn m o s t lo c a tio n , S au d a rk ro k u r , c o n s ti tu te d b y 100%
h y b rid s , a n d th e n o r th w e s te rn m o s t lo c a tio n , R eykholar, c o n s ti tu te d
b y 4 5 % h y b rid s . W lren c o m p a r in g lo c a tio n s across s tu d ies, h y b rid s
w ere fo u n d in all ío c a tio n s sh a red , a l th o u g h h y b rid p ro p o r tio n s
w ere o n iy s im ila r a t o n e lo c a tio n , V ogslaekur (11 .1% in o u r s tu d y
a n d 11.9% in A lb e rt e t a l , 2 0 0 6 ). O n ly a t o n e lo ca tio n , S tokkseyri, th e
p ro p o r t io n o f h y b rid s w as h ig h e r in o u r s tu d y (20% ) in c o m p a ris o n
w ith th e A lbert e t al. (2006) s tu d y (8 .3 % ). A t th e re m a in in g lo ca tio n s,
h y b rid p ro p o r t io n s w ere h ig h e r in A lbert e t al. (2 0 0 6 ). H ow ever, th e
overall h y b rid p ro p o r t io n in b o th s tu d ie s w as w ell h ig h e r th a n th e
v alues re p o r te d by th e earlie r s tu d y o f Avise e t al. (1990) th a t
suggested th a t — 2 -4 % o f th e gene p o o l o f Ice land ic eels is
d e riv ed fro m A m e rican eel ancestry . T h e low er h y b rid iza tio n d e tec ted
m ig h t be a ttr ib u ta b le to th e lo w re so lu tio n o f th e m ark e rs u sed
(a llozym es a n d m ito c h o n d r ia l D N A ) in c o m p a ris o n w ith a m p lified
f rag m en t le n g th p o ly m o rp h ism s (A lb e rt e t al., 2006 ) o r SN Ps
(th is s tu d y ).
Patterns of hybridization
T h e inc reased re so lu tio n o f o u r a rray o f d ia g n o stic R A D -genera ted
SN P m arke rs sheds new lig h t o n th e s ta tu s o f h y b rid s a n d th e n a tu re
o f in tro g re ss io n in Ice land ic eels. A cco rd in g to o u r SN P survey, p u re
E u ro p ea n eels m a d e u p th e m a jo rity o f lce lan d ic eels b u t th e re is also
an im p o r ta n t in flux o f in d iv id u a ls o f ad m ix e d ancestry . In o u r s tu d y
hyb rid s en co m p assed : F1 hy b rid s re su ltin g from crosses betw een
E u ro p ean eel fem ales a n d A m e rican eel m ales, f ir s t-g en e ra tio n back-
crosses be tw een p u re E u ro p ea n eels a n d F1 h y b rid s (o n e in d iv id u a l)
a n d sec o n d -g e n e ra tio n backcrosses be tw een firs t-g en e ra tio n back-
c rosses (p u re A m e ric a n e e l x F l h y b rid ) a n d p u re E u ro p ea n eels
( th ree in d iv id u a ls ). N o n e o f th e ad m ix e d in d iv id u a ls w ere F2 hy b rid s
re su ltin g fro m crosses b e tw een F1 hyb rid s. A lth o u g h th e h y b rid
classes o b serv ed w ere re s tric ted to th e first th re e g en era tio n s , th e
f in d in g o f A m erican eel m tD N A in a n in d iv id u a l w ith a seem ing ly
p u re E u ro p ea n n u c le a r g e n o m e suggests th a t successfu l h y b rid iza tio n
o ver several g en era tio n s is possib le , a l th o u g h rare . In th is sense, la te r
h y b rid s m ig h t have b e en m issed becau se o f lo w sam p le sizes. I t sh o u ld
a lso be n o te d th a t SN Ps th a t a re fixed b e tw een species a re likely to
m a rk c h ro m o so m a l re g io n s u n d e r s tro n g d irec tio n a l selec tion o r
g en o m ic in c o m p a tib ilitie s (G ag n aire e t a l , 20 1 2 ). D u rin g su b seq u en t
gen era tio n s o f backcross ing , se lec tion c o u ld rem o v e in trog ressed
alleles a t d iag n o stic m ark e rs . T h e n u m b e r o f in d iv id u a ls rep re sen tin g
m u ltig e n e ra tio n backcrosses co u ld th e re fo re in p rin c ip le be
u n d e re s tim a ted .
A lth o u g h F1 h y b rid s a re likely to o u tp e rfo rm e ith e r p u re p a ren ta l
species in su iw iving d u e to h y b rid v ig o r (T em p le to n , 1986; Jo h n so n
e t a l , 2010 ), in m a n y species F l h y b rid s have b een s h o w i to be
in fertile , o ften reg a rd ed as a n e v o lu tio n a ry d e ad e n d w h e n h y b rid s are
u n ab le to p ro d u c e v iab le progeny. T h is is n o t th e case o f th e E u ro p ean
eel, as o u r s tu d y show s the p resen ce o f firs t- a n d sec o n d -g en e ra tio n
backcrosses in Ice lan d th a t n o t o n ly in d ic a tes th a t F1 h y b rid s are
viab le a n d can su rv ive in Ice land , b u t a lso th a t th ey can successfu lly
m ig ra te b ack to th e Sargasso Sea as s ilver eels a n d re p ro d u c e as p a r t o f
th e sp aw n in g stock. O u r s tu d y also show s th a t it is possib le fo r a
backcross o r ig in a te d from a cross be tw een an F1 a n d an A m erican eel
to re tu rn to th e Sargasso a n d in te rb ree d w ith a p u re E u ro p ea n eel,
w ith th e re su ltin g sec o n d -g e n e ra tio n b ackcross ev en tually se ttlin g
d o w n in Iceland.
A ltem atively , th o se in d iv id u a ls id e n tified as s ec o n d -g en e ra tio n
backcrosses m ig h t be firs t-g en e ra tio n backcrosses b e tw een E u ro p ean
eel x F l h y b rid sh o w in g h ig h e r- th an -ex p e c ted h e te rozygosities
(F igu re 5). O n e m e c h an ism th a t c o u ld exp la in th is is in tr in s ic
o u tb re e d in g d ep re ss io n (T em p le to n , 1986; A llen d o rf et a l , 2001 )
th o u g h t to b e because o f g enetic in c o m p a tib ilitie s b e tw een species
invo lv ing d e le te r io u s e p ista tic in te ra c tio n s c au sed by th e co m b in a tio n
o f in c o m p a tib le alleles fro m d iffe ren t loci in hy b rid s (D obzhansky ,
1936; M uller, 1942). I t is o ften fo u n d th a t F2 h y b rid s sh o w red u c ed
fitness because o f d is ru p tio n o f sets o f c o -a d a p te d genes by
re c o m b in a tio n th a t o c cu rs in tlie seco n d o r la te r g e n e ra tio n s w hen
a ss o rtm e n t o f alleles a t d iffe ren t loci takes p lace (G h a rre tt a n d
Sm oker, 1991; Jo h n so n e t a l , 2010 ). Eels a re h ig h ly fecu n d , w ith an
e s tim a te d m e a n fe c u n d ity o f 3 .6 m illio n o f eggs p e r fem ale
(M acN am ara a n d M cC arthy , 2012); the re fo re , even th o u g h th e
expec ted p ro p o r t io n o f h e te ro zy g o u s loci in firs t-g en e ra tio n back-
crosses is 50% , th e re w ill b e v a ria n ce a ro u n d th is n u m b e r. In a large
n u m b e r o fo f f s p r in g from a sing le cross, th e re w o u ld co n seq u e n tly be
so m e in d iv id u a ls th a t sh o w h ig h h e te ro z y g o sity fo r d iag n o stic alleles
at loci th a t p re su m ab ly a re u n d e r se lec tion . T hese in d iv id u a ls m ig h t
be fu n c tio n a lly c loser to F1 h y b rid s , w ith m o re sets o f c o -ad ap ted
alleles fro m each o f th e p a re n ta l species re la tive to average
Heredity
Hybridization between North Atlantic eels
JM Pujolar ef al
backcrosses, w h e re p ro n o u n c e d d is ru p t io n o f c o -a d a p te d gene c o m -
plexes is expected . Finaliy, a h ig h e r- th an -ex p e c te d h e te rozygosity
co u ld a lso b e ex p la in ed by p ro d u c tio n o f p a rtly u n re d u c ed gam etes
in F1 h y b rid s g iven rise to tr ip lo id p ro g e n y w h en back cro ssed to
e ith e r p a re n ta l species ( Jo h n so n a n d W rig h t, 1986; C astillo et al.,
2 0 0 7 ), a lth o u g h h e te ro zy g o sity va lues sh o u ld vary ra n d o m ly a n d n o t
necessarily fit the o b se rv ed p a tte rn o f d ev ia tin g backcrosses.
In to ta l, w e fin d it m o s t likely th a t th e d ev ia tin g backcrosses a re
in d e e d se c o n d -g e n e ra tio n backcrosses, as th ey w ere id en tified as su ch
w ith h ig h p ro b a b ility u s in g N ew H y b rid s a n d as th e o b serv ed
h e te ro zy g o sity m a tc h e d ex p ec ta tio n s fo r th is ty p e o f cross. T h e
f in d in g th a t F1 h y b rid s can back cro ss to o n e s p e d e s (A m erican eel)
a n d in th e su b se q u e n t g e n e ra tio n b ackcross to th e o th e r species
(E u ro p e an eel) is re m ark ab le . A t p re sen t, th e u n d e rly in g m e ch an ism s
c a n n o t b e id en tified . H ow ever, as E u ro p ea n a n d A m e rican eels have
d iffe ren t p eak spaw m ing tim e ( M cC leave e t a i , 1987), th is is likely to
be an im p o r ta n t p rezy g o tic re p ro d u c tiv e iso la tio n m e ch an ism . T h is
m a y b e b ro k e n u p in h y b rid s le ad in g to in te rm e d ia te sp aw n in g t im e
a n d a h ig h e r p ro b a b ility o f in te rb ree d in g w ith e ith e r o f th e p a re n ta l
species.
Why are hybrids primarily found in Iceland?
A lth o u g h genetic m a rk e rs have sh o w n th e o ccu rre n ce o f hyb rid s in
Ice lan d (Avise e t a i , 1990; A lb e rt c t a l , 2 0 0 6 ), th e g eo g rap h ic ran g e
lim it o f h y b rid s a n d th e ir p resen ce in o th e r E u ro p ea n lo ca tio n s has
re m a in e d u n c e r ta in . T h e o b se i'v a tio n in o u r s tu d y o f 100% p u re
E u ro p ean eels in th e F a ro e Is lands, w h ich a re th e c losest b o d ies o f
la n d to Ic e la n d a t a d is ta n ce o f 450 k m , suggests th a t h y b rid s d o n o t
sp re ad m u c h to w ard s th e E ast a n d are lim ited to Iceland . E arly
in d ic a tio n s tlia t h y b rid s m ig h t o c cu r in th e F a roe Is lands cam e fro m
th e s tu d y o f B oétiu s (1980) based o n to ta l n u m b e r o f v erteb rae ,
p rev io u s ly reg a rd e d as th e b e s t d is tin g u ish in g ch a rac te r b e tw een
E u ro p ean a n d A m erican eels. In a c o m p reh e n siv e su rvey o f over
15 000 in d iv id u a ls c o m p ris in g all o f E u ro p e a n d N o r th A frica,
N o r th e m E u ro p e a n lo c a tio n s sh o w ed 1^1% in d iv id u a ls w ith relatively
lo w v e rteb rae c o u n ts , as is ty p ica l o f A m e ric a n eel. A lth o u g h ve rteb rae
co u n ts in Ita ly (N = 1287) ra n g e d b e tw een 111 a n d 119, in d iv id u a ls
sh o w in g v e rteb ra e c o u n ts o f < 1 1 0 w ere o b se rv ed in b o th Iceland
(1 0 8 -1 1 0 ) a n d F a ro e Is lan d s (1 0 6 -1 1 0 ) th a t p o in te d to th e presence
o f e ith e r p u re A m e ric a n eels o r h y b rid s in N o r th e rn E u ro p e a n d a
rela tively h ig h deg ree o f mLxing b e tw een th e tw o species. H ow ever, the
o b se rv a tio n in o u r s tu d y o f 100% p u re E u ro p ea n eel in d iv id u a ls w ith
n o s ig n a tu re s o f a d m ix e d a n ce s try in th e F aroe Is lan d s suggests th a t
th e sh ift to w a rd s A m e ric a n values in v e rte b ra e c o u n ts o b served by
B oétiu s (1980) is n o t b ecau se o f th e p resen ce o f h y b rid s a n d m ig h t be
th e re su lt o f a h ig h v a ria b ility in th is tra it.
W h y a re h y b rid s b e tw een E u ro p e a n a n d A m erican eel fo u n d
p rim arO y in Iceland? H y b rid s c o u ld ex h ib it a genetica lly d e fin e d
in te rm e d ia te d u ra t io n o f th e larval p h a se sy n ch ro n ized w ith an
in te rm e d ia te d e v e io p m e n t tim e (Avise e t a l , 1990). T h is w o u ld
ex p la in th e p resen ce o f h y b rid s in Ic e lan d th a t is s o m e w h a t s itu a ted
halfw ay e n ro u te fro m th e S argasso Sea to E u rope. H ow ever, th e
m ig ra tio n d u ra t io n o f E u ro p e a n a n d A m erican eel la rv ae fro m th e
Sargasso Sea to th e ir respective c o n tin e n ts re m a in s un reso lv ed a n d
h ig h ly d e b a ted , a lth o u g h i t is o b v io u s th a t m ig ra tio n d is tan ce is m u c h
lo n g e r fo r E u ro p ea n th a n fo r A m erica n eels. F o r E u ro p ean eels,
m ig ra tio n t im e e s tim a te s ran g e fro m 7 to 9 m o n th s to 2 years
d e p e n d in g o n th e a s s u m p tio n s a n d m e th o d s u sed , w hereas estim ates
fo r A m eric an eels ran g e b e tw een 6 a n d 12 m o n th s ( B o n h o m m e au
e t al. , 2009 ). D iffe ren t la rva l m ig ra tio n d u ra t io n is a lso s u p p o r te d by a
tra n s c r ip to m e s tu d y o f la rvae o f b o th eel species co llected in the
Sargasso Sea (B em atch ez et al., 2 0 1 1 ). L arvae show ed very s im ila r
tra n s c r ip to m e pro files a t dififerent age stages, b u t th e re w as a
s ign ifican t delay o f u p - a n d d o w n -re g u la tio n in E u ro p ea n as o p p o sed
to A m erican eels, c o n sis te n t w ith th e a s s u m p tio n o f a s h o r te r larval
stage a n d m ig ra tio n tim e in tlie la tter.
I t is possib le to sp ecu la te th a t h y b rid s m ig h t sh o w a n in te rm e d ia te
m ig ra to ry b e h av io u r a n d larval d e v e lo p m en ta l (m e ta m o rp h o s is )
b e tw een th e tw o N o r th A tlan tic p a re n ta l species th a t u ltim a te ly
b rin g s h y b rid la rvae to th e sh o re s o f Ice land . Several s tu d ie s have
sh o w n a n in te rm e d ia te m ig ra to ry b e h a v io u r in h yb rid s . E x p e rim en -
tally p ro d u c e d h y b rid s o f a n exclusively m ig ra to iy E u ro p ea n p o p u la -
tio n a n d a p a rtia lly m ig ra to ry A frican p o p u la tio n ofi th e b lackcap
Sylvia atricapilla sh o w ed in te rm e d ia te m ig ra to ry restlessness a n d an
in te rm e d ia te p e rcen tag e o f b ird s d isp lay in g restlessness c o m p a re d
w ith th e tw o p a re n ta l s tocks (B e rth o ld a n d Q u e m er , 1981). Sim ilarly,
hyb rid s b e tw een c o m m o n re d s ta r ts P hocnicurus phoei:icurus a n d b lack
re d s ta r ts P. ochruros sh o w e d in te rm e d ia te tim e co u rse o f m ig ra to ry
activ ity re la tive to th e p a re n ta l species (B e rth o ld a n d Q u e m e r , 1995).
In fish, h y b rid s be tw een coasta l c u t th ro a t t ro u t (O ncorhynchus clarki
clarki) a n d stee lh ead t r o u t (O . m ykiss ) sh o w ed b o th in te rm e d ia te
sw im m in g ab ility a n d in te rm e d ia te m ig ra to ry b e h a v io u r to th a t o f
e ith e r species (M o o re e t a l , 20 1 0 ). H en ce , it is p lau sib le th a t hyb rid s
b e tw een E u ro p ean a n d A m erican eels w o u ld a lso sh o w in te rm e d ia te
m ig ra to ry b e hav iou r, a lth o u g h tliis re m a in s to be investigated .
T h e q u e sd o n still re m a in s o f w hy h y b rid eels are a b u n d a n t in
Tceland b u t n o t in th e n e ig h b o u rin g F aroe Islands. H e re it sh o u ld b e
n o te d th a t th e N o r th A tlan tic C u rre n t ( th e n o rth e a s tw a rd ex ten sio n
o f th e G u lf S tream ) t ra n s p o r tin g th e eel la rv ae ac tu a lly separa te s in to
tw o b ran ch es ~ 1 0 0 0 k m so u th w es t o f Iceland . T h e o n e b ra n c h passes
th e Faroese sh e lf a n d c o n tin u e s in to tlre N o r th Sea a n d N o rw eg ian
Sea to w ard s th e co as t o f N orw ay. T h e o th e r b ra n ch , th e I rm in g e r
C u rre n t, sh ifts in a n o rth w e s te rn d ire c tio n to w a rd s a n d a lo n g th e w est
coasts o f Iceland . H ence , in te rm s o f m ig ra to ry ro u te s , eels fro m
Ice land a n d th e F a roe Is lands a re ex p ec ted to b e sep a ra ted by
> 1 0 0 0 k m , even th o u g h th e sh o rte s t d irec t w a terw ay d is tan ce is
c o n sid e rab ly sho rte r.
Biological implications o f pattems o f hybridization
E u ro p ean a n d A m e rican eel re p re sen t cx tre m e life h is to rie s a n d a
p e cu lia r h y b rid iz a tio n scen ario invo lv ing tw o p a n m ic tic species an d
yet a very loca lized o ccu rren ce o f h yb rid s . N evertheless, even very low
g en e flow b e tw een th e species m a y b e b io log ica lly s ig n ifican t a n d
co u ld exp la in th e su rp ris in g ly low gen etic d iffe ren tia tio n be tw een
N o r th A tlan tic eels o b serv ed in p rev io u s s tu d ie s (M an k a n d Avise,
2003; W irth a n d B ernatchez , 2003). A t eq u ilib r iu m , F$r sh o u ld be
ap p ro x im a te ly equal to l / ( l + 4 N em ) (W rig h t, 1931), w h ere N e
d en o tes effective p o p u la tio n size a n d m is m ig ra tio n ra te p e r
gen e ra tio n . E s tim a tes o f lo n g -te rm N e in A tlan tic eels d e riv ed fro m
m ic ro sa te llite m a rk e rs are o n th e o rd e r o f 4 0 0 0 -1 0 0 0 0 (W irth a n d
B ernatchez , 2003; P u jo la r e t a l., 2 0 1 1 ), w hereas a recen t s tu d y
em p lo y in g RA D seq u en c in g suggests th a t h is to rica l N c in E u ro p ean
eel m ay b e as h ig h as ca. 1000 0 0 to 1 000 000 ( P u jo la r e t a l , 2013). If
w e a ssu m e th a t F ^r b e tw een th e species is ca. 0.05 (ro u g h ly re flec ting
th e e stim ates by M an k an d Avise, 2003; W ir th a n d B ernatchez , 20 0 3 )
th e n a t N e values o f 4000 to 1 0000 th is w o u ld c o rre s p o n d to
m ig ra tio n ra te s o f 1.2 x 10 ~ 3 a n d 4.8 x 10 ~ 4, w hereas fo r N e values
o f 100000 a n d 1 OOOOOOm it w o u ld be as low as 4.8 x 1 0 -5 a n d
4.8 x 1 0 - 6 . H ence , d e p en d in g o n w h ich o f th e N e estim ates b est
reflects th e tru c N e, i t w o u ld o n ly tak e a lo w to very lo w level o f
gene flow to m a in ta in overall Iow gen etic d ififeren tiation betrween
th e species.
Heredity
Hybridization between North Atlantic eels
JM Pujolar et al
10
W e p re d ic t th a t th e o c c u rren ce o f low g enetic d iffe ren tia tio n
b e tw een closely re la ted a n d occasio n a lly h y b rid iz in g species m ay be
a c o m m o n o c cu rre n ce a m o n g m a rin e fishes a n d in v e rteb ra tes
e x h ib itin g la rge effective p o p u la tio n sizes, even i f gene flow is
q u a n tita tiv e ly v e ry low. In th e N o r th e rn H e m isp h e re , p laice (Pleur-
onectes p la tesa ) a n d f lo u n d e r (P la tich thys flesus) rep re sen t a g o o d
ex am p le o f h y b rid iz in g spec ies tlia t c o u ld be u sed fo r fu r th e r s tu d y in g
th e g en era lity o f su ch p a t te m s ( K ijew ska e t a l , 2 0 0 9 ).
DATA ARCHIVING
All seq u en c in g files (.fastq ) c an b e fo u n d o n N C B I’s S equence Read
A rchive u n d e r p ro je c t n u m b e r P R J N A l95555 (E u ro p ean eel) a n d
PR JN A 230782 (A m e ric a n eei).
CONFLICT OF INTEREST
T h e a u th o rs dec lare n o c o n flic t o f in te res t.
ACKNOWLEDGEMENTS
W e t h a n k R u s s e l P o o l e , J a v i e r L o b o n , E r í c F e u n t e u n a n d p a r t i c i p a n t s i n t l i e
G a l a t h e a 3 E e l P r o j e c t f o r p r o v i s i o n o f s a m p l e s , K a r e n - L i s e D M e n s b e r g , D o r t e
M e l d r u p a n d A n n i e B r a n d s t r u p f o r t e c h n i c a l a s s i s t a n c e a n d t h r e e a n o n y m o u s
r e v i e w e r f o r c o n s t r u c t i v e c o m m e n t s o n t h e m a n u s c r i p t . W e a c k n o w l e d g e
f u n d i n g f f o m t h e D a n i s h C o u n c i l f o r I n d e p e n d e n t R e s e a r c h , N a t u n i l S c i e n c e s
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http://www.nature.com/hdy
Ulrik er al. BMC Evolutionary Biology 2014, 14:138
http://www.biomedcentral.eom/1471 -2148/14/138 ( b m c
Evolutionary Biology
R E S E A R C H A R T I C L E O pen Access
Do North Atlantic eels show parallel patterns of
spatially varying selection?
Malene G Ulrik1 f , José Martín P u jo lar1 f , Anne-Laure Ferchaud1, Maqnus W Jacobsen1, Thomas D Als2'3,
Pierre A lexandre Gaqnaire4, Jane Frydenberq1, Peder K Bocher1, Bjarni Jónsson5, Louis Bernatchez6
and M ichael M Hansen1"
Abstract
Background: The tw o North Atlantic eel species, the European and the American eei, represent an ideal system in
which to study parallel selea ion patterns due to their sister species status and the presence o f ongo ing gene flow.
A panel o f 80 coding-gene SNPs previously analyzed in American eel was used to genotype European eel individuals
(glass eels) from 8 sampling locations across the species distribution. We tested fo r single-generation signatures o f
spatially varying selection in European eel by searching fo r elevated genetic d ifferentia tion using Fs r based outlie r
tests and by testing fo r significant associations between allele frequencies and environm ental variables.
Results: We found signatures o f possible selection at a total o f 11 coding-gene SNPs. Candidate genes for local
selection constitu ted m ainly genes w ith a major role in metabolism as well as defense genes. Contrary to what
has been found for American eel, on ly 2 SNPs in our study correlated w ith differences in tem perature, which
suggests tha t o ther explanatory variables may play a role. None o f the genes found to be associated w ith
explanatory variables in European eel showed any correlations w ith environm ental factors in the previous study in
American eel.
Conclusions: The d iffe rent signatures o f selection between species could be due to distinct selective pressures
associated w ith the m uch longer larval m igration for European eel relative to American eel. The lack o f parallel
selection in North Atlantic eels could also be due to most phenotypic traits being polygenic, thus reducing the
likelihood o f selection acting on the same genes in both species.
Keywords: Adaptation, European eel, Genetic-by-environm ent associations, Parallel selection, Single nucleotide
polym orphism s
Background
Parallel adaptive changes under replicated environmental
conditions have been particularly valuable for under-
standing evolutionary processes in natural populations.
One of the classical questions in evolutionary bioiogy
concerns whether different species and populations
within species will adapt to the same agent of selection
in the same way or whether the response will involve
different traits and genes [1,2]. Parallel genotypic adapta-
tion appears to be frequent and occurs at all taxonomic
levels from microbes and plants to humans [3,4] and is
* Correspondence: michael.m.hansen(S>biology.au.dk
+Equal contributors
'Department o f Bioscience, Aarhus University, Ny Munkegade 114, 8ldg.
1540, DK-8000 Aarhus C, Denmark
Full list o f author information is available at the end o f the artide
BioMed Central
likely to result in changes at a relatively small number of
genes ]5]. For instance, the study of Colosimo et al. [6]
demonstrated that selection on a single gene, ectodyspla-
sin (Eda), is responsible for the parallel reduction of armor
plates in freshwater populations of threespine sticldeback
Gasterosteus aculeatus. However, more complex physio-
logical processes relevant in the context of parallel fresh-
water adaptation of threespine sticklebacks are influenced
by several genes, each of small effect [7-10]. Using a
survey of the published literature on parallel adaptation
of independent lineages of natural populations, Conte
et al. [5] concluded that divergence at loci under selection
is most likely to be based on standing genetic variation
derived from a common ancestor rather than mutations
occurring de novo after divergence. Hence, probability
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Page 2 o f 11
of gene reuse is plausibly higher in closely related spe-
cies, which are likely to show similar divergence at loci
subjected to similar selection pressures [11].
An excellent opportunity to test for genetic parallelism
exists in the two North Atlantic eel species, the European
eel (Anguilla anguilla) and the American eel (A rostrata).
Both species are morphologically almost indistinguishable,
with the number of vertebrae being regarded as the best
diagnostic character between species [12]. Divergence
time between the two species remains largely unresolved,
encompassing between 1.5 and 5.8 million years [13-15].
Remarkably, although mitochondrial DNA Iineages of the
two species are reciprocally monophyletic [13], differenti-
ation at nuclear loci is surprisingly low (FST = 0.055 [16];
Fs t = 0.018 ]17]; FST = 0.06 [18]; Fsx = 0.09 [19]), suggest-
ive of ongoing gene flow. In this sense, it is well estab-
lished that the spawning grounds of the two species
overlap in the Sargasso Sea and there is also overlap in
spawning time [20]. European and American eels are
known to hybridize, with hybrids observed almost exclu-
sively in Iceland [21-23]. Hence, the sister species status of
European and American eel and the low but biologically
significant gene flow makes them an adequate system in
which to test the occurrence of selection at homologous
loci within each species.
North Atlantic eels have a catadromous life cycle and
after spawning in the Sargasso Sea, larvae are transported
by the Gulf Stream and other currents to the shores of
North America and Europe/North Africa, respectively.
Upon reaching the continental shelf, larvae metamorphose
into glass eels, which complete the migration into riverine,
estuarine and coastal feeding habitats and grow up as
yellow eels. After a highly variable feeding stage, yellow
eels metamorphose into partially mature silver eels that
migrate back to the Sargasso undertaking a journey of
about 2,000 km for the American eel and 5,000-6,000 km
for the European eel. Upon arriving in the Sargasso Sea,
eels reproduce and die [24]. During the continental phase,
eels occupy a broad range of habitats from the Caribbean
to Greenland in the western Atlantic (American eel)
and from Morocco to Iceland in the eastern Atlantic
(European eel). The presence of eels in extremely hete-
rogenous environments in terms of temperature (i.e.
from subtropical to subarctic), salinity (i.e. from fresh-
water to marine), substrate, depth or productivity along
their geographic distribution makes them ideal species
in which to study the consequences of spatially varying
selective pressures that often result in local adaptation
of ecologically important traits [1,25,26]. Beginning with
Levene [27], who introduced the first theoretical model
for examining the impact of diversifying selection in
space, a number of studies have shown that balancing
selection due to spatial heterogeneity is an important
mechanism responsible for the maintenance of genetic
polymorphism (reviewed in [28]). Genetic variation in a
spatially heterogenous environment may be maintained
even when dispersal results in complete mixing of the
gene pool [1]. However, under such a panmixia scenario,
in which offspring are distributed to environments at ran-
dom independently of the environment experienced by
the parents, local selection cannot to lead to local adapta-
tion [29]. In the case of eels, owing to panmixia in both
European [19,30] and American eel [31] and random Iar-
val dispersal across habitats, heritable trans-generational
local adaptation is not possible although single-generation
footprints of selection can still be detected. In this sense,
significant geographic clines at allozyme Ioci have been
detected in both European [32] and American eel [33].
In the most comprehensive study to date, Gagnaire
et al. [26] found evidence for spatially varying selection
at 13 coding genes in American eel showing significant
correlations between allele frequencies and environmental
variables (latitude, longitude and temperature) across the
entire species range.
In this study, we tested for single-generation signatures
of spatial varying selection in European eel and compared
the results to those obtained by Gagnaire et al. [26]. We
genotyped glass eels from 8 sampling locations across the
geographic distribution of the species, using the same set
of SNPs analyzed by Gagnaire et al. [26] in American eel.
We used two main analytical approaches, one that identi-
fies outliers as those markers with greater difierentiation
among all SNPs and a second based on determining
positive associations between allele frequencies and en-
vironmental factors. Following the positive associations
observed by Gagnaire et al. [26] in American eel, vari-
ables used in our study were degrees North latitude, de-
grees East/West longitude and sea-surface temperature
at river mouth. We specifically wanted to test whether
the same genes were under spatially varying selection in
both European and American eel, hence providing evi-
dence for parallel patterns of local selection, or whether
the response involved a different set of genes. Considering
their sister species status and the existence of gene flow
between species, together with the similar environmental
conditions they encounter [34], we hypothesize that the
two North Atlantic eel species show parallel patterns of
selection at the same loci.
Results
Genetic diversity values for all genotyped individuals at 80
SNPs are summarized in Table 1. 17 out of 80 loci were
monomorphic and 63 were polymorphic in European eel,
although frequency of the most common allele was >0.95
at 27 loci. Diversity indices were higher in American eel
(H0 = 0.302; Hc = 0.306; P95 = 0.896; P99 = 0.922) than in
European eel (H0 = 0.149; He = 0.157; P95 = 0.429; P99 =
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Ulrik et al. BMC Evolutionary Biology 2014, 14:138
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Page 3 o f 11
Table 1 Details of all genes and loci studied, including observed (H0) and expected (He) heterozygosities at all loci in
American (AR) and European eel (AA)
Locus Gene AR
H 0 H e
AA
H 0 He
40S_S18_1401 40s ribosomal protein s18 0.389 0.375 0.344 0.312
60S_L10A_21874 60s ribosomal protein L10a 0.250 0.219 0.282 0.306
ACT_A3B_8646 Aainin alpha 3b 0.300 0.255 0.006 0.006
ACTB_21752 Beta-aain 0.474 0.411 0.213 0.244
ACYL_13914 Acyl carrier protein 0.421 0.388 0.320 0.310
ADH_3 Alcohol dehydrogenase class-3 0.263 0.361 0.229 0.351
ADSS_L1_15447 Adenylosuccinate synthetase isozyme 1 0.158 0.229 0.016 0.016
ALD_R Aldose reduaase 1 . 0 0 0 0.500 0.395 0.345
ALDH_2_16634 Aldehyde dehydrogenase 2 0.947 0.499 0.468 0.428
ANK_R_13478 Ankyrin repeat domain-comtaining protein 1 0.250 0.289 0.000 0.000
ANN_A11_16176 Annexin A11 0 . 2 0 0 0.180 0.171 0.172
ANX_2_249 Annexin A2-A 0 . 1 0 0 0.375 0.016 0.034
ARF_4_18099 ADP-ribsylation factor 4 0.444 0.346 0.019 0.019
ATP_BC_259 ATP-bindincasette sut>family A member 1 0.450 0.439 0 . 0 2 2 0 . 0 2 2
BPNT_1_18778 3'(5'),5'-biphosphate nucleotidase 1 0.263 0.411 0.025 0.025
CLIC_5_10148 Chloride intracellular channel 5 0.250 0.219 0.521 0.492
COM7591 Cytochrome oxidase subunit I 0.000 0.000 0 . 0 1 0 0.009
COP_9_18132 266S protease regulatory subunit 7 0.300 0.255 0.035 0.034
CSDE_1_11069 Cold shock domain-containing protein E1 0.316 0.266 0.019 0.019
CSDE_1_19713 Cold shock domain-containing protein E1 0.474 0.411 0.066 0.064
CST_21113 Cystatin precursor 0.421 0.499 0.379 0.393
CYT_BC1_9061 Cytochrome b-c1 complex subunit 2 0 . 2 0 0 0.180 0.000 0.000
EF_1G_4796 Translation eiongation faaor 1 gamma 0.400 0.320 0 . 0 0 0 0.000
EF2_10494 Translation elongation faaor 2 0 . 2 0 0 0.180 0 . 0 0 0 0.000
EIF_3F_341 Translation elongation faaor 3 subunit F 0 .2 1 1 0.332 0.113 0.146
EIF_3J_11587 Translation elongation factor 3 subunit J 0.300 0.375 0.079 0.082
FER_H_20955 Ferritin heavy subunit 0.421 0.432 0.009 0.009
FGB_47 Fibrinogen Beta Chain 0.300 0.255 0.000 0.000
GAPDH_20355 Glyceraldehyde-3-phoshpate dehydrogenase 0 . 2 0 0 0.180 0 . 2 2 2 0.197
GDE1_2508 Glycerophosphochlorine phosphodiesterase 0.389 0.313 0.000 0.000
GOG_B1_15792 Golgin sub-family B member 1 0.150 0.289 0.050 0.049
GPX_4_19607 Glutathione peroxidase 4 0 . 1 0 0 0.095 0.000 0 . 0 0 0
HMG_T_9973 High mobility group-T protein 0.050 0.049 0.025 0.025
HSP_90A_15666 Heat shock protein 90 alpha 0.158 0.229 0.063 0.061
HSP_90B_21100 Heat shock protein 90 beta 0.150 0.139 0.107 0.107
HSPE_ 1 _17854 10 kDa heat shock protein 0.368 0.362 0.009 0.009
IF_RF2_19747 Interferon regulatory faaor 2 0.150 0.139 0.000 0.000
JAM_3_13916 Junaional adhesion molecule 3b 0.053 0.051 0.131 0.165
KRT_13_20618 Keratin 0.350 0.499 0.325 0.317
KRT_A_15738 Keratin alpha-like 0.000 0.000 0 . 0 2 2 0 . 0 2 2
LBL_L2_20921 No hit 0.000 0.000 0.000 0 . 0 0 0
LDH_B_9441 Laaase dehydrogenase B 0.600 0.455 0.025 0.025
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Table 1 Details of all genes and loci studied, induding observed (H0) and expected (He) heterozygosities at all loci in
American (AR) and European eel (AA) (Continued)
MDHJ393 Malate dehydrogenase 0.263 0.450 0.298 0.493
MYH_14857 Superfast myosin heavy chain 0.300 0.255 0.563 0.496
NADH_4_21742 NADH dehydrogenase subunit 4 0 . 0 0 0 0.0180 0 . 0 0 0 0 . 0 0 0
NADH_5_17101 NADH dehydrogenase subunit 5 0 . 0 0 0 0.255 0 . 0 0 0 0.019
NADH1_10_21119 NADH dehydrogenase 1 alpha subunit 10 0.300 0.455 0 . 0 0 0 0 . 0 0 0
NCP_2_15547 Nucleolar complex protein 2 0.350 0.289 0.085 0.087
NEX_19953 Nexilin 0.450 0.489 0.476 0.496
NGD_21138 Neuroguidin 0.450 0.469 0.238 0.273
NRAP_1541 Nebulin-related anchoring protein 0.500 0.455 0.031 0.031
PA2G4_2600 Proliferation associated protein 2G4 0.444 0.401 0.442 0.481
PFNJ5113 Profilin-2 0.400 0.375 0 . 0 0 0 0 . 0 0 0
PGDJ8096 6 -phosphogluconate dehydrogenase 0 . 0 0 0 0 . 0 0 0 0.042 0.053
PGI_1 Phosphoglucose isomerase-1 0 .2 1 1 0.188 0.338 0.348
PGI_2 Phosphoglucose isomerase-2 0.368 0.478 0.456 0.498
PGKJJ1454 Phosphoglycerate kinase 1 0.474 0.362 0.090 0.092
PRP_40_16504 Pre-mRNA-processing factor 40 homolog A 0.150 0.219 0.205 0.214
PSA_4_21534 Proteasome subunit alpha type-4 0.350 0.439 0.484 0.498
PSME_1_21196 Proteasome aaivator 0.235 0.458 0.441 0.457
RFC_3_18186 Replication faaor C subunit 3 0.350 0.289 0.416 0.368
RTF_1_21288 RNA polymerase-associated protein RTF1 homolog 0.632 0.432 0.339 0.374
SDH_0 Sorbitol dehydrogenase 0 . 0 0 0 0 . 0 0 0 0 . 0 0 0 0 . 0 0 0
SLC_25A5_19808 ADP/ATP translocase 2 0.450 0.499 0.006 0.006
SM_22_6449 Transgelin 0.550 0.499 0.074 0.083
SN4_TDR_374 Taphylococcal nuclease domain-containing protein 1 0.526 0.465 0.182 0.191
TENT_02_11046 No hit 0 .1 1 1 0.105 0.318 0.362
TENT_03_12589 Collagen type XXVIII alpha 1 a 0.150 0.219 0.041 0.040
TENT_05_19704 No hit 0.500 0.461 0.013 0.013
TENT_06_16512 Protein Phosphatase regulatory subunit 0.105 0.266 0.510 0.484
TENT_07_21161 No hit 0.700 0.451 0.744 0.477
TNNT_2E_20968 Troponin T2e 0 . 0 0 0 0 . 0 0 0 0.168 0.196
TRIM_35_8416 Tripartite motif-contaning protein 35 0.368 0.450 0.361 0.426
TTN_B_20952 Titin b 0.421 0.332 0.003 0.003
TUB_A_19211 Tubulin alpha 2 0.550 0.489 0 . 0 1 0 0.009
UBI_A52_5049 Ubiquitin A-52 residue ribosomal protein fusion product 1 0.474 0.362 0.058 0.056
UGP_2_2128 UDP-glucose pyrophosphorylase 2 0.316 0.808 0.236 0.771
UGP_A_2307 Glycerol-3-phosphate transporter subunit 0.600 0.334 0.733 0.466
UNA_SINE2_16912 Eel Short interspersed elements 0 . 0 0 0 0 . 0 0 0 0 . 0 0 0 0 . 0 0 0
ZETAJ5177 Tyr 3-monooxygenase/írp 5-monooxygenase aaivation protein 0.421 0.388 0.246 0.245
0.610), suggestive of a strong ascertainment bias effect due
to the fact that SNPs were identified in American eel.
Three loci deviated significandy from Hardy-Weinberg ex-
pectations after Bonferroni correction: locus UGP_2_2128,
showing a deficit of heterozygotes, and loci TENT_0721161
and UGP_A_2307, showing an excess of heterozygotes.
However, those loci were not excluded from the analysis
as they could reflect selection.
Two loci (ALD_R and PSME_1_21196) were geno-
typed at all locations except Tiber, so all tests for selec-
tion were conducted considering all 8 locations and 78
loci (excluding ALD_R and PSME_1_21196) and on a
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restricted data set with 7 locations (excluding Tiber)
and 80 loci.
Overall genetic differentiation was low (FST = 0.0079).
Using STRUCTURE, a scenario with turo clusters (K = 2)
corresponding to the two species was the most likely,
with no substructuring within species (Figure 1). In the
same analysis, a total of 5 individuals from Iceland were
identified as admixed individuals with 90% probability
intervals that did not overlap with zero. While the SNPs
used in this study were not species-diagnostic, results
were concordant with the study of Pujolar et al. [23], in
which the same individuals were identified as admixed
on the basis of 86 species-diagnostic SNPs, encompassing
four F1 hybrids and one second generation backcross.
Hybrids were only observed in Iceland and were absent
in the remaining European locations. All hybrid individ-
uals were removed from further analyses.
The selection detection workbench LOSITAN identified
three outlier loci possibly under diversifying selection
using the full data set, GAPDH_20355, MYH_14857 and
ALDH_2_16634, with p < 0.05 (Table 2). When using the
restricted data set with 7 locations, a further outlier was
also identified, ALD_R (p = 0.000). Using the complete
data set with 8 locations BAYESCAN identified a single
outlier, GAPDH_20355, showing a high FST value of 0.123
relative to the background FST (Table 2). At this locus,
the alpha coefficient was positive, suggestive of diversi-
fying selection. When using the restricted data set with
7 locations, ALD_R was also identified as outlier in
addition to GAPDH_20355, showing a high FST value of
0.091 and a positive alpha coefficient.
A generalized linear model between allelic frequencies
and explanatory variables using the full data set revealed
significant associations with temperature (2 loci), latitude
(3 loci) and longitude (5 loci) (Table 3). One locus
(GAPDH_20355) showed a significant association with
both latitude and longitude. No interactions with explana-
tory variables were found at any locus. Locus ALD_R
showed a positive association with longitude when using
the restricted data set with 7 locations (p = 0.016).
On the other hand, one positive association was found
using BAYENV, locus GAPDH_20355 and latitude, with
a Bayes Factor of 7.450 (Table 3), while no associations
were found for the rest of loci (Bayes Factor <3). In
addition, a positive association was found between locus
ALD_R and longitude, with a Bayes Factor of 3.295,
when considering the reduced data set with 7 locations.
Overall, we identified a total of 11 candidate loci, 4
from outlier tests plus 7 additional loci from the analysis
of association of allelic frequencies with explanatory
variables.
Discussion
Signatures o f local selection in European eel
The observation of a small set of SNPs showing signifi-
cantly high genetic differentiation in comparison with
the background FST and significant associations betv\reen
allele ffequencies and environmental variables is consist-
ent with the action of spatially varying selection associ-
ated with the highly heterogenous habitats that glass eels
colonize throughout their geographic range. Our findings
fit the general prediction that selective pressures fre-
quently vary in space, often resulting in local selection
of ecologically adaptive traits [1].
Overall, we found signatures of selection at a total of
11 loci. We found discordances between the two approaches
used (Fst outlier tests vs. environmental-association
methods), with few SNPs identified as targets of selec-
tion by both methods and with a higher number of can-
didates identified using a generalized linear model. This
is in agreement with recent studies showing that SNPs
positively correlated with environmental variables were
not FST outliers [35-37]. It has been suggested that SNP-
environment associations are more sensitive to detect sub-
tle clines in allele frequencies than FST outlier tests and
tliat both approaches might be complementary but not
concordant when testing for selection [38].
Nevertheless, three loci in our study (GAPDH, ALDH2
and ALD_R) showed higher genetic differentiation than
the background FST together with significant associations
between allele frequencies and environmental variables.
All three are genes with major metabolic functions:
GAPDH (Glyceraldehide 3-phosphate dehydrogenase)
is part of the glycolysis pathway and catalyzes the
American European
eel < eel ■>
Figure 1 Adm ixture analysis using STRUCTURE. Individuals were assigned assuming the presence of two groups (K = 2). Each vertical line
represents one individual, partitioned into segments according to the proportion of European eel (light) and American eel (dark).
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Table 2 Detection of outlier loci using the FST-outlier approach implemented in LOSITAN and BAYESCAN based on the
full data set with 8 locations (78 loci) and a reduced data set with 7 locations (80 loci)
LOSITAN
Locus Gene Het F s t p value
8 populations
MYH_14857 Superfast myosin heavy chain 0.490 0.042 0.018
GAPDH_20355 Glyceraldehyde-3-phosphate dehydrogenase 0.213 0.246 0.000
ALDH_2_16634 Aldehyde dehydrogenase 2 0.428 0.032 0.047
7 populations
GAPDH_20355 Glyceraldehyde-3-phosphate dehydrogenase 0.231 0.256 0.000
ALDH_2_16634 Aldehyde dehydrogenase 2 0.435 0.036 0.012
ALD_R Aldose reductase 0.346 0.156 0.000
BAYESCAN
Locus Gene BPP q value alpha F s r
8 populations
GAPDH_20355 Glyceraldehyde-3-phosphate dehydrogenase 1.000 0.000 3.376 0.123
7 populations
GAPDH_20355 Glyceraldehyde-3-phosphate dehydrogenase 1.000 0.000 2.424 0.116
ALD_R Aldose reductase 1.000 0.000 2.150 0.091
Heterozygosity and F^r values are detailed for all outlier loci detected in LOSITAN. Bayesian posterior probabilities (BPP), q values, alpha coefficients and Fjt values
are detailed for all outlier loci detected in BAYESCAN.
conversion of glyceraldehyde 3-phosphate to D-
glycerate 1,3-bisphosphate; ALDH2 (Aldehyde dehydro-
genase 2) belongs to the aldehyde dehydrogenase family
of enzymes that catalyze acetaldehyde to acetic acid and is
the second enzyme of the major oxidative pathway of alco-
hol metabolism; ALD_R (Aldose reductase) catalyzes the
reduction of glucose to sorbitol, the first step in the polyol
pathway of glucose metabolism. Besides these genes, a
positive environment correlation was observed for PGI<
(Phosphoglycerate kinase), which is a transferase enzyme
in glycolysis acting in the first ATP-generating step of the
glycolytic pathway. Surprisingly, none of the above genes
linked to metabolism showed positive associations with
temperature, arguably an environmental variable of key
importance influencing enzymatic activities and metabolic
pathways [39,40]. In eels, decreased metabolic activities
have been observed below certain threshold temperatures
in both European [41] and American eel [42], and distinct
behaviour patterns such as upstream migration of glass
eels have been shown to be temperature-related [43].
Since it could be argued that temperature at other time in-
tervals might be more relevant than the 30 day-interval
used in our study, we re-conducted a generaiized linear
model between allelic frequencies at GAPDH, ALDH2
and ALD_R with temperature using other time intervals
(10 days, 3 months, 6 months, 12 months). No significant
associations were found at any of the locus, which sug-
gests that other agents of selection than temperature
could underlie the significant associations found. In the
case of aldose reductase, this is an enzyme induced by
hyperosmolarity stress [4-4]. Spatially varying selection
in European eel regarding osmoregulation seems plausible,
since eels occupy highly variable habitats across Europe in
terms of salinity, including both fresh and salt-water (i.e.
marine and brackish) habitats [45].
Besides genes involved in metabolic functions, several
genes involved in defense response showed a positive
environment correlation, including TRIM35 (Tripartite
motif-containing protein 35), CST (Cystatin precursor),
PSA4 (Proteasome subunit alpha-4) and UBIA52 (Ubiqui-
tin A52), all involved in catalytic activity. Interestingly,
TRIM35 is a gene implicated in processes associated with
innate immunity [46]. Together with other TRIM family
genes, TRIM35 is located on a region of significantly ele-
vated genetic diversity (LG XIII) in the threespine sticlde-
back, which suggests that the polymorphism increase on
LG XIII has been likely driven by selection on innate
immunity genes [7]. While allele frequencies at TRIM35
were positively correlated with temperature, allele fre-
quencies at CST, UBIA52 and PSA4 were associated with
geographic coordinates. As in the case of metabolism, it is
possible that other explanatory variables (e.g. productivity,
oxygen level, salinity, pollution and parasite load) may
play a role in defense response rather than temperature
or geographic coordinates.
No apparent parallel patterns of selection in North
Atlantic eels
The contrasting pattern of spatially varying selection ob-
served in European eel (this study) and American eel
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Table 3 Statistical associations between allele frequencies and a set of three expianatory variables (TEMP,
temperature; LAT, latitude; LON, longitude) assessed using generalized linear models (GLM) and BAYENV based on the
full data set with 8 locations (78 loci) and a reduced data set with 7 locations (80 loci)
GLM
Locus Gene p value
8 populations
TRIM_35_8416 Tripartite m otif-contain ing protein 35 TEMP (r = 0.78; p = 0.023)
NEX_19953 Nexilin LAT (r = 0.80; p = 0.018)
GAPDH_20355 Glyceraldehyde-3-phosphate dehydrogenase LAT (r = 0.72; p = 0.045) + LON (r = 0.74; p = 0.042)
KRT_13_20618 Keratin TEMP (r = 0.81; p = 0.015)
UBI_A52_5049 Ubiquitin A-52 LON (r = 0.72; p = 0.044)
P G K J J 1 4 5 4 Phosphoglycerate kinase LON (r = 0.76; p = 0.031)
PSA_4_21534 Proteasome subunit alpha type-4 LAT (r = 0.80; p = 0.018)
ALDH_2_16634 Aldehyde dehydrogenase 2 LON (r = 0.72; p = 0.044)
CST_21113 Cystatin precursor LON (r = 0.72 p = 0.043)
7 populations
TRIM_35_8416 Tripartite m otif-contain ing protein 35 TEMP (r = 0.77; p = 0.042)
NEX_19953 Nexilin LAT (r = 0.76; p = 0.045)
GAPDH_20355 Glyceraldehyde-3-phosphate dehydrogenase LON (r = 0.73; p = 0.046)
KRT_13_20618 Keratin TEMP (r = 0.82; p = 0.023)
PSA_4_21534 Proteasome subunit alpha type-4 LAT (r = 0.76; p = 0.047)
ALD_R Aldose reductase
VOOÖIICLíN00ÖIIzo
BAYENV
Locus Gene BF
8 populations
GAPDH_20355 Glyceraldehyde-3-phosphate dehydrogenase LAT(BF = 7.450)
7 populations
GAPDH_20355 Glyceraldehyde-3-phosphate dehydrogenase LAT(BF = 4.501)
ALD_R Aldose reductase LON (BF = 3.295)
Correlation coefficients and p-values are detailed for all loci showing significant associations using GLM. Bayes Factors (BF) are presented for all positive
associations in BAYENV.
[26] using the same panel of candidate SNPs suggests no
common genetic-by-environment associations between
North Atlantic eels. Using generalized linear modeis,
Gagnaire et al. [26] found significant associations with
environmental variables at 8 loci within glass eels (ACP,
ANX2, GPX4, HSP90A, MDH, NRAP, PRP40 and UGP2),
none of which are common with the 10 loci that showed
significant associations in our study using the same statis-
tical approach (ALDH, ALD_R, CST, GAPDH, I<RT, NEX,
PGK, PSA4, TRIM35, UBLA.52) and also conducted on
glass eels.
However, two loci (TRIM35 and CST) showed some
evidence of selection in both species. In American eel,
TRIM35 showed the highest FSt value detected betu'een
localities (FST = 0.174) although no correlation with envir-
onmental variables was detected at this locus. CST showed
signatures of selection within cohorts of juveniles but not
within glass eels [26].
While most loci under selection in Gagnaire et al. [26]
represented metabolic genes associated with temperature,
those genes with a major role in metabolism in our
study (GAPDH, ALD_R, ALDH, PGI<) did not show a
positive association with temperature despite the
similar temperature ranges encountered by both spe-
cies (European eel: 4.2-15.1°C, American eel: 3.4-19.8°
C). However, the different signatures of selection
between species could be due to distinct selective
pressures associated with the much longer larval mi-
gration for European eel than for American eel, with
estimates ranging from 7 months to 2 years for Euro-
pean eel depending on the assumptions and methods
used, whereas estimates for American eel range be-
tween 6 and 12 months [47]. The one extra year that
possibly European eel larvae spend in the open sea
could impose a different set of selective agents rela-
tive to American eel.
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In contrast with our findings, the recent survey of Conte
et al. [5] on published literature of repeated phenotypic
evolution in natural populations concluded that the prob-
ability of gene reuse was high (on average 55%). However,
the survey was based on candidate gene studies, which
might have biased upward the reuse estimates. The lack of
parallel selection patterns in North Atlantic eels is un-
anticipated owing to the sister species status of European
and American eel and the permeable barrier to gene flow
between species. A recent study using a RAD-sequencing
approach to identify diagnostic markers between the two
species found a small proportion of fíxed SNPs (<0.5%),
while most of the SNPs showed low non-significant differ-
entiation that suggest that most of the genome is homoge-
nized by gene flow [23]. One possible explanation to the
lack of parallel selection is that complex phenotypic
traits affected by local selection might have a highly
polygenic basis, hence influenced by several genes, each
with a smail contribution to the ultimate function
[48,49]. Parallel selection is more likely to occur when
the adaptive response is controlled by a single gene, i.e.
the Eda gene and armor plate reduction [6,50] and the
Kit ligand Kitlg gene and pigmentation [51] in three-
spine sticklebacks or the melonacortin-1 receptor M clr
and colour pattern in beach mice [52]. More complex
traits are likely to involve a higher number of genes,
thus reducing the likelihood of selection acting on the
same genes in multiple species or locations, as it has
been argued in the case of osmoregulation in threespine
sticklebacks [7,8]. Similarly, partial parallel patterns of
genetic differentiation have been observed between two
whitefish sympatric species pairs (a normal benthic and
a dwarf limnetic) across lakes, suggestive of polygenic
adaptation [53-55].
Condusions
The distinct signatures of selection between North
American eels could be attributable to differences in larval
migration between species. Alternatively, the fact that
many genes of small effect likely shape adaptive pathways
(i.e. metabolism, growth, osmoregulation, pathogen resist-
ance) could explain the private signatures of spatially vary-
ing selection with no shared genetic-by-environment
associations between European and American eel. As an
alternative to candidate loci approaches, high-density
genome-wide scans using next-generation sequencing
and genotyping-by-sequencing approaches [7,56] might
be more adequate. A recent study using RAD (Restric-
tion site Associated DNA) sequencing generated a SNP
resource for European eel consisting of 82,4-25 loci and
over 375,000 SNPs [57] that provides a valuable tool for
future studies on parallel selection in both North Atlantic
eels on a genome-wide scale.
Methods
Ethical statement
No experiments were conducted on the animals and ani-
mal manipulation was limited to sacrificing fish, using the
least painful method to obtain tissue samples for DNA ex-
traction. In all cases, in order to minimize the suffering of
the animals used in the study, fish were deeply anaesthe-
tized with MS-222 (3-amonobenzoic acid ethyl ester) or
2-phenoxyethanol 1% and then painlessly sacrificed. All
procedures were conducted by technical staff, who had all
the necessary fishing and animal ethics permits (piease see
in the Additional file 1: Appendix 1).
Sampling
A total of 321 European eel (Anguilla anguilla) individuals
were collected at 8 locations across the geographical distri-
bution of the species, from Iceland to the Mediterranean
Sea (Table 4; Figure 2). AU individuals were glass eels
caught by electrofishing (Iceland) and fyke nets (remaining
localities). Individuals from Iceland were collected at four
separate sampling sites in southwestern Iceland, but
pooled to increase sample size. Additionally, 20 American
eel (Anguilla rostrata) individuals collected at Riviére
Blanche (Québec, Canada), Mira River (Nova Scotia,
Canada), Wye River (MD, US), Medomak River (ME,
US) and Boston Harbor (MA, US) were used for com-
parison. Genomic DNA was extracted using standard
phenol-chloroform extraction.
SNP genotyping
We examined the panel of 100 coding-gene SNPs devel-
oped by Gagnaire et al. [26] in American eel. 20 out of
the 100 primer sets did not give good amplification
products in European eel and were excluded. All indi-
viduals were genotyped at 80 coding-gene SNPs: 47
SNPs that were detected as outliers between samples
from Florida and Québec using RNA-sequencing data
(including 4 SNPs identified within allozyme-coding genes
showing clinal variation in Williams et al. [33]) and 33
SNPs that were not outliers (Table 2). SNP genotyping
was conducted using the Kbioscience Competitive AUele-
Specific PCR genotyping system (KASPar) (Kbioscience,
Hoddeston, UI<).
Data analysis
AUele frequencies, measures of genetic diversity including
polymorphism at the 95% (P95) and 99% level (P99), ob-
served (H0) and expected (He) heterozygosities and devia-
tions from Hardy-Weinberg equilibrium were calculated
using GENEPOP [58]. In all cases, significance levels were
corrected for multiple comparisons using the sequential
Bonferroni technique [59].
Overall genetic differentiation (Fsx) was calculated in
GENEPOP. Population structure was further investigated
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Table 4 Sampling details induding n u m b er of individuals per sampling location (N), latitude, longitude and
sea-surface temperature at river mouth averaged across the 30 days preceding the sampling date
Country Location N Latitude Longitude Date Tem p (°C)
Spain Valencia 44 39°46' N 0°24' W 15 January 2010 15.05
Italy Tiber 39 41°73' N 12°23' E 30 December 2007 14.17
South France Canet 40 42°70' N 3*15' E 23 January 2008 13.24
West France Gironde 40 44°86’ N 0°42' W 16 April 2008 11.26
Ireland Burrishoole 39 53°90’ N 9°58' W 14 March 2005 9.57
Northern Ireland Lough Erne 39 54°46' N 7°77' W 1 July 2008 13.85
Sweden Ringhals 40 57°21‘ N 12°27' E 15 March 2008 4.19
lceland 40 May - June 2001 8.45
Stokkseyri 10 63*81' N 21°04'W
Vifilsstadvatn 10 64°07' N 21°87’ W
Seljar 10 64°56' N 22*31 'W
Vogslækur 10 64°69' N 22°33' W
using STRUCTURE v.2.3.4 [60], which also allowed us to
test the presence of hybrids in the data set. We assumed
an admixture model, uncorrelated allele frequencies and
we did not use population priors. Given that two panmic-
tic species were analyzed, we assumed k= 2 and con-
ducted 10 replicates to check the consistency of results. A
burn-in length of 100,000 steps followed by one million
additional iterations was performed.
We used two different approaches to test for evidence
of local selection. First, we seai'ched for elevated popula-
tion differentiation using Fsx-based outlier analyses. We
used the selection detection workbench LOSITAN [61],
which uses a coalescent-based simulation approach to
identify outliers based on the distributions of heterozygos-
ity and FST [62]. First, LOSITAN was run using all SNPs
to estimate the mean neutral FST as recommended by
Antao et al. [61]. After the fírst run, the mean neutral Fsx
was re-computed by removing those SNPs outside the
confidence interval in order to obtain a better approxima-
tion of the mean neutral Fsx. This mean was then used to
conduct a second and final run of LOSITAN using all
SNPs. The analysis was performed on the whole data set
divived according to sampling location. An estimate of p
value was obtained for each SNP. We used a threshold of
0.95 and a false discovery rate of 0.1 to minimize the num-
ber of false positives.
Outlier SNPs were also detected using BAYESCAN
[63], a Bayesian method based on a logistic regression
model that separates locus-specific effects of selection
from population-specific effects of demography. Outlier
analysis was conducted on the whole data set divided
according to sampling location. BAYESCAN runs were
implemented using default values for all parameters,
including a total of 100,000 iterations after an initial
lc e la n d
R in g h a ls
R lv ié re B la n ch o
Lough E rne
# #
B u r r lsh o o lo
#
M odom ak r i v e r ^ ^ M ira r lv o r
B o s to n h a r b o r ^
G lro n d e # Cane t
• ^ T ib o r
Wye r iv e r ^ - V a le n c ia #
0 500 1 ooo (Otometors
Figure 2 Sampling locations of European eel (circles) and American eei (stars) individuals used for comparison.
http://www.biomedcentral.eom/1471
Ulrik et al. BMC Evolutionary Biology 2014, 14:138
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Page 10 of 11
burn-in of 50,000 steps. Posterior probabilities, q values
and alpha coefficients (positive values indicate diversify-
ing selection, negative values are indicative of balancing
selection) were calculated. A q-value of 10% was used
for significance.
As an alternative to FSx'Outlier tests, our second ap-
proach for identifying targets of local selection was to
test for significant statistical associations between al-
lelic frequencies and environmental variables following
Gagnaire et al. [26], using a generalized linear model in
r. Environmental variables used included degrees North
latitude, degrees East/West longitude, and sea-surface
temperature at river mouth averaged across the 30 days
preceding the sampling date. Sea-surface temperature
data were retrieved from the IRI (International Research
Institute for Climate and Society) Climate Data Library
(http://iridl.Ideo.columbia.edu/) database “NOAA NCDC
OISST version2 AVHRR SST: Daily Sea Surface Tem-
perature”. We also searched for SNP-environment associa-
tions using BAYENV [38], which tests for covariance
between candidate SNP allele frequencies and environ-
ment variables that exceed the expected covariances under
genetic drift. First, SNP frequencies at all loci were used to
describe how allele frequencies covary across populations,
hence avoiding population-specific effects of demography
(even though a panmixia scenario is most likely to apply
for European eel). After the covariance matrbc was esti-
mated, the program determined the Bayes factors for the
environmental variables of interest. Bayes Factors >3 were
considered indicative of an allele frequency correlation
with an environmental variable.
Availability of supporting data
The data set supporting the results of this aiticle is available
from Dryad: http://datadryad.Org/resource/doi:10.5061/
dryad.jn800/l.
Additional file
Competing interests
The authors dedare no competing interest.
Authors' contributions
MMH and LB conceived and designed the project. MGU and JMP conducted
population genetics analyses with help from MMH, TDA, ALF and MWJ. MGU
and JMP wrote the manuscript with contributions from MMH, LB, PAP, ALF,
MWJ, TDA, JF, PKB and BJ. All authors read and approved the final version of
the manuscript.
Acknowledgements
We thank Eieonora Ciccotti, Russell Poole, Javier Lobón-Cervia. Eric Feunteun,
Francoise Daverat and Hákan Wickstrom for providing samples, Annie
Brandstrup for technical assistance, Virqinia Senepani for help in preparing
the figures and Mads F. Schou for help in statistical analysis. We
acknowledge funding from the Danish Council for Independent Reasearch,
Natural Sciences (grant 09-072120 to MMH).
Author details
'Department o f Bioscience, Aarhus University, Ny Munkegade 114, Bldg.
1540, DK-8000 Aarhus C, Denmark. JNational Institute of Aquatic Resources,
Technical University o f Denmark, Vejlsovej 39, DK-8600 Silkeborg, Denmark.
3Department o f Biomedicine-Human Genetics, Aarhus University, DK-8000
Aarhus C, Denmark. 4ISEM (Institut des Sciences de l'Evolution Montpellier),
Université Montpellier II, 34095 Montpellier, France. sBiopol, Marine Biology
and Biotechnology Center, Einbúastígur 2, IS545 Skagastrond, lceland. 6IBIS
(Institut de Biologie Intégrative et des Systémes), Université Laval, G1V 0A6
Québec, Canada.
Received: 27 March 2014 Accepted: 16 June 2014
Published: 20 June 2014
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doi:10.1186/1471-2148-14-138
Cite th is article as: Ulrik er a/.: Do North Atlantic eels show parallel
patterns o f spatially varyinq selection? 8MC Evolutionary Bioloqy
2014 14:133.
http://www.biomedcentral.eom/1471
Pujolar et al. BMC Genomics (2015) 16:600
DOI 10.1186/sl 2864-015-1754-3
( b m c
Genomics
R E S E A R C H ART I CLE Open Access
Signatures of natural selection between life ^ c“M"k
cycle stages separated by metamorphosis
in European eel
J. M. Pujolar1*, M. W. Jacobsen1, D. Bekkevold2, J. Lobón-Cerviá3, B. Jónsson4, L. Bernatchez5 and M. M. Hansen1
Abstract
Background: Species showing com plex life cycles provide excellent opportunities to study the genetic associations
between life cycle stages, as selective pressures may differ before and after metamorphosis. The European eel presents
a com plex life cycle w ith tw o metamorphoses, a first metamorphosis from larvae in to glass eels (juvenile stage)
and a second m etam orphosis in to silver eels (adult stage). We tested the hypothesis tha t d ifferent genes and
gene pathways w ill be under selection at d ifferent life stages when com paring the genetic associations between
glass eels and silver eels.
Results: We used tw o sets o f markers to test for selection: first, we genotyped individuals using a panel o f 80
coding-gene single nucleotide polymorphisms (SNPs) developed in American eel; second, we investigated selection at
the genome level using a total o f 153,423 RAD-sequencing generated SNPs widely distributed across the genome.
Using the RAD approach, outlier tests identified a total o f 2413 (1.57 %) potentially seleaed SNPs. Functional annotation
analysis identified signal transduction pathways as the most over-represented group o f genes, including MAPK/Erk
signalling, calcium signalling and GnRH (gonadotropin-releasing hormone) signalling. Many o f the over-represented
pathways were related to growth, while others could result from the different conditions that eels inhabit during their life
cycle.
Concluslons: The observation o f different genes and gene pathways under seleaion when comparing glass eels vs. silver
eels supports the adaptive decoupling hypothesis for the benefits o f metamorphosis. Partitioning the life cycle into
discrete m orpholog ica l phases may be overall beneficial since it allows the d ifferent life stages to respond
independently to the ir unique selection pressures. This m ight translate in to a m ore effective use o f food and
niche resources and /o r performance o f phase-specific tasks (e.g. feeding in the case o f glass eels, m igrating and
reproducing in the case o f silver eels).
Keywords: Adaptative decoupling hypothesis, Complex life cycles, Metamorphosis, RAD sequencing, Selection
Background
Many animals show complex Iife cycles organized into
morphologically distinct phases separated by abrupt
metamorphic transitions (metamorphosis), as opposed
to single static or continuously changing phases jTJ.
Complex life cycles are ubiquitous in nature and have
evolved many times independently [1-3]. Life stages are
believed to represent alternative adaptations for optimal
food and niche exploitation as well as conflicting tasks
* Correspondence: jmartin@biology.au.dk
’ Department o f Bioscience, Aarhus University, Aarhus C, Aarhus, Denmark
Full list o f author information is available at the end of the article
(e.g. feeding, growth, mate-finding, dispersal, reproduction).
Since Darwin, evolutionary biologists have been interested
in understanding the genetic associations between life
cycle stages and to what extent discrete phases are free to
evolve independently from one another. Metainorphosis
marks drastic morphological, physiological, behavioural
and ecological changes in the life cycles of animals [4].
Given the dramatic changes associated with metamor-
phosis, selection could differ before and after metamor-
phosis, and opposing selection might be more common
than complimentary selection [5, 6]. In regard to the bene-
fits of metamorphosis, the adaptive decoupling hypothesis
[1] predicts that traits separated by metamorphosis should
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link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain
Dedication waiver (http://creativecommons.Org/publicdomain/zero/l.0/) applies to the data made available in this
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Pujoiar et al. BMC Genomics (2015) 16:600 Page 2 o f 15
be genetically uncorrelated, allowing distinct phases to re-
spond independently to different selective forces, without
correlated negative effects on traits of alternative phases.
Studies testing the adaptive decoupling hypothesis have
found contradictory results and the genetic associations
between life cycle stages separated by metamorphosis re-
main poorly understood |6j.
Our species of interest is the European eel {Anguilla
anguilla), a facultative catadromous fish with a particu-
larly complex life cycle that includes two metamor-
phoses. After spawning in the remote Sargasso Sea,
larvae of European eel are transported to the coasts of
Europe and North Africa following the Gulf Stream and
North Atlantic current. On reaching the continental
shelf, eels undergo a first metamorphosis from larvae
into glass eels (juvenile stage), which complete their mi-
gration into continental feeding habitats as yellow eels.
After an extensive feeding/growing period, eels undergo
a second metamorphosis into silver eels (adult stage).
The so-called “silvering metamorphosis” encompasses
morphological (colour, eye size, body length and weight)
as well as physiological modifications (e.g. loss of digestive
tract), together witli tlie development of gonads. These
changes are beforehand preparation for the íuture spaun-
ing migration back to the Sargasso Sea, where eels repro-
duce and die £7].
The European eel is an ideal species in which to study
local selection. First, it presents a large effective popula-
tion size (estimated from 100,000 to lxlO 6 individuals;
[8]) that renders natural selection the major force deter-
mining genetic differences; hence the role of random
genetic drift is expected to be negligible. Second, it is
present across extremely heterogenous environments in
terms of temperature (from subarctic habitats in Iceland,
Norway and northwestern Russia to subtropical habitats
in North Africa and the Mediterranean Sea), salinity
(from fresh water to brackish and marine habitats), sub-
strate, depth and productivity along its geographic distri-
bution [9]. Despite such a wide distribution range, there
is recent conclusive evidence for panmixia in European
eel, i.e. the existence of a single randomly mating popu-
lation. In the most comprehensive study to date geno-
typing over 1000 individuals obtained throughout all the
distribution range in Europe at 21 microsatellite loci, /ds
et al. [10] showed a very low and nonsignificant genetic
diffferentiation across Europe (FST = 0.00024) and a lack
of substructuring among larvae collected in the Sargasso
Sea (Fst = 0.00076). Moreover, no significant genetic dif-
ferentiation was observed when comparing tlie samples
obtained in Europe vs. the larvae obtained from the
spawning area (FST = -0.00012). Panmixia was also con-
firmed at the genomic level in a study using a large
dataset of > 450,000 SNPs from 259 RAD-sequenced
European eels [11], which showed low levels of genetic
differentiation (Fsx = 0.0007). Previous studies based on
cohort analysis showed an unpatterned genetic hetero-
geneity (genetic patchiness) as samples did not group
together according to sampling location or cohort, and
consequently no pattern on Isolation-by-Distance or
Isolation-by-Time was detected [12, 13]. If European
eel larvae showed phylopatry to the parental original
freshwater habitats, genetic differences would be ex-
pected across Europe; hence, the lack of genetic struc-
turing found suggest no larval homing and random
larval migratory routes [10, 11]. One consequence of
panmixia and random dispersal of larvae across habitats
is that long-term local adaptation is not possible in eels,
despite the high potential for selective responses due to
high mortalities in both early and late life stages [14].
Any signature of spatially varying selection in a given
generation is expected to be lost in the subsequent gen-
eration, preventing heritable trans-generational local
adaptation [15]. However, single-generation signatures
of local selection are still detectable [11, 15].
Studies of adaptive evolution in European eel have fo-
cused on the detection of signatures of local selection in
glass eels. Using a panel of 100 coding-gene single nu-
cleotide polymorphisms (SNPs), Ulrik et al. [16] found
signatures of selection at 11 loci in European eel, which
constituted genes with a role in metabolism as well as
defense response. As an alternative to candidate gene
approaches, Pujolar et al. [11] tested for footprints of se-
lection in glass eels at the genome level using 50,354
SNPs generated by RAD sequencing. A total of 754
potentially locally selected SNPs were identified. Candi-
date genes for local selection constituted a wide array
of functions, including calcium signalling, neuroactive
ligand-receptor interaction and circadian rhythm.
The power and efficiency of next generation sequen-
cing (NGS) technologies are enabling research use of
genomic data to address ecological and evolutionary
questions at a genome-wide scale for model and non-
model species [17, 18]. The insights that are obtained
through NGS methods, as well as high throughput geno-
typing methods in general, have led to unprecedented
progress in many areas, from bridging ecological and
evolutionary concepts to identifying the molecular basis
of local selection and adaptation [17, 19-24]. The aim of
our study is to test for selection acting upon different life
cycle stages separated by metamorphosis in European
eel, in particular between glass eels (juvenile stage) and
silver eels (adult stage). First, we used a candidate gene
approach and genotyped individuals from three sampling
locations (Iceland, Ireland and Spain) using a panel of
100 coding-gene SNPs. Second, we performed RAD-
sequencing of individuals from two sampling locations
(Ireland and Spain), which allowed us to test for signa-
tures of local selection at the genome level using a total
Pujolar ef al. BMC Genomics (2015) 16:600 Page 3 o f 15
of 153,4-23 SNPs widely distributed across the genome.
Following the shifts in selection exerted by the dramatic
physiological, morphological and ecological changes that
accompany metamorphosis, our prediction is that differ-
ent genes and gene pathways will be under selection at
different life stages, and those will appear as outlier loci
(higher genetic differentiation relative to the back-
ground) when comparing glass eels vs. silver eels.
Ultimately, the identification of genes showing marked
differences when comparing life stages separated by
metamorphosis can provide insights into how European
eel can cope with the incredible variety of conditions
and environments encountered throughout its complex
life cycle. It can also provide general insights into adap-
tive genomic evolution in natural populations of marine
fishes.
Results
SNP g e n o typ in g
Details of all polymorphic loci, including frequency of
the most common allele across all sampling locations in
our study in silver eels and glass eels are presented in
Table 1. A total of 61 out of 80 SNPs were polymorphic,
although at 19 loci minor allele frequency (MAF) was <
0.05 in all samples. Genetic diversity values are summa-
rized in Table 2. Genetic diversity measures were very
similar across samples and no significant differences
were found across sampling locations in silver eels, i.e.
He (Spain: 0.227; Ireland: 0.233; Iceland: 0.224; p = 0.96);
AR (Spain: 1.60; Ireland: 1.62; Iceland: 1.62; p = 0.99).
Moreover, no differences were found in genetic diversity
measures when silver eels were compared to glass eels
(p > 0.05). Three loci deviated significantly from HWE at
all locations (UGP2, heterozygote deficit; TENT7and
UGPA, heterozygote excess) but were not excluded from
the analysis, since departures from HWE might be due
to selection.
Genetic differentiation across silver eel samples was low
and not significant (FST = 0.0018; p = 0.330). A similar low
genetic differentiation was found when considering all sil-
ver eel and glass eel samples (FST = 0.0026; p = 0.079) or
when comparing pooled silver eels vs. pooled glass eels
(Fst = 0.0021; p = 0.807). Low Fsx values were also ob-
tained when compared silver eels vs. glass eels in all sam-
ples: Spain (FST = 0.0036; p = 0.851), Ireland (FST = 0.0016;
p = 0.943) or Iceland (FST = 0.0065; p = 0.976).
Prior to the selection analysis, we investigated the
presence of hybrids in the silver eel data set using
STRUCTURE. Two individuals from Iceland (VADA-1
and VADA-2) were identified as hybrids showing a 50 %
admixture proportion, and were consequently removed
from the analysis (data not shown).
Results from outlier tests are summarized in Table 3.
Using LOSITAN, a total of 3 outliers were identified
when comparing all samples in our study (3 silver eels, 3
glass eels): GAPDH, ALD_R and CLIC5. When compar-
ing the 3 silver eel samples, two outliers were identified:
CLIC5 and LDHB. When comparing silver eels vs. glass
eels in all samples separately, different outlier loci were
identified at each location: CLIC5 when comparing silver
eels and glass eels from Spain; CST and CSDEl when
comparing silver eels and glass eels from Ireland; and
GAPDH when comparing silver eels and glass eels from
Iceland. GAPDH was also detected as outlier when
comparing pooled silver eels vs. pooled glass eels. When
using BAYESCAN, fewer outliers were identified in
comparison with LOSITAN, all showing high FST values:
GAPDH (Fst = 0.27) and ALD_R (FST = 0.12) when con-
sidering all samples and GAPDH (FST = 0.33) when com-
paring silver eeis and glass eels from Iceland.
RAD sequencing
After sequencing of the RAD libraries, average number
of reads (90 bp) per individual was 12.2 million for silver
eels and 9.6 million for glass eels. After trimming to
75 bp and quality filtered, the average number of high
quality reads retained was 10.7 million (86.8 %) for silver
eels and 7.9 million (82.2 %) for glass eels. A similar per-
centage of reads were uniquely aligned to the European
eel draft genome (69.3-70.0 %), while 25.6-26.3 % of se-
quences did not align and 4.5 % were discarded due to
multiple alignments.
Aligned reads were then assembled into a total of
348,342 loci using Stacks (Table 4). After discarding
27.12 % of loci due to insufficient coverage, 253,864 loci
were used to construct a catalog of loci of SNPs for all
individuals. At this point, a more strict filtering was ap-
plied and we eliminated 846 loci due to extremely high
coverage (>57.3 reads, which is twice the standard devi-
ation from the mean number of reads), 144 loci at which
all individuals were either all heterozygotes or all homo-
zygotes, and 55,075 loci due to the presence of more
tlran 2 alleles in a single individual, possibly reflecting
paralogs or sequencing error. After a final filtering step
selecting only loci genotyped in >66.7 % of individuals in
all sampling locations, a total of 77,337 RAD loci were
retained. Using Populations in Stacks, a total of 558,022
SNPs were discovered, including 153,423 SNPs with a
minor allele frequency > 0.05.
Measures of genetic diversity at 77,337 loci at all sam-
pling locations are summarized in Table 5. The Valencia
silver eel sample showed similar heterozygosities (H0 =
0.048; He = 0.052) and nucleotide diversity (Pi = 0.053)
compared to the Valencia glass eel sample (H0 = 0.047;
He = 0.051; Pi = 0.052) and the Burrishoole glass eel sample
(H0 = 0.047; He = 0.051; Pi = 0.052). The Burrishoole silver
eel sample showed slightly lower diversity (H0 = 0.040; Hc =
0.042; Pi = 0.045), presumably due to lower sample size.
Pujolar er al. BMC Genomics (2015) 16:600 P a g e 4 o f1 5
Table 1 Details of all polymorphic loci, including frequency of the most common allele across all silver eel (SE) and glass eel (GE)
samples
Locus Gene Ireland lceland Spain
SE GE SE GE SE GE
40S_S18_1401 40s ribosomal protein s l8 0.829 0.846 0.828 0.807 0.838 0.750
60S_L10A_21874 60s ribosomal protein L10a 0.846 0.782 0.776 0.839 0.775 0.779
ACT_A3B_8646 Actinin alpha 3b 1 . 0 0 0 1 . 0 0 0 1 . 0 0 0 1 . 0 0 0 1 . 0 0 0 1 . 0 0 0
ACTB_21752 Beta-actin 0.788 0.808 0.906 0.862 0.863 0 . 8 8 6
ACYLJ3914 Acyl carrier protein 0.750 0.776 0.758 0.823 0.738 0.826
ADH_3 Alcohol dehydrogenase class-3 0.737 0.859 0.733 0.690 0.795 0.761
ADSS_L1_15447 Adenylosuccinate synthetase isozyme 1 1 . 0 0 0 0.987 1 . 0 0 0 0.984 1 . 0 0 0 1 . 0 0 0
ALD_R Aldose reduaase 0.759 0.838 — 0.537 0.859 0.936
ALDH_2_16634 Aldehyde dehydrogenase 2 0.638 0.763 0.600 0.550 0 . 6 8 8 0.682
ANK_R_13478 Ankyrin repeat domain-comtaining protein 1 1 . 0 0 0 1 . 0 0 0 1 . 0 0 0 1 . 0 0 0 1 . 0 0 0 1 . 0 0 0
ANN_A11_16176 Annexin A11 0.897 0.923 0.807 0.919 0.900 0.852
ANX_2_249 Annexin A2-A 0.987 0.949 1 . 0 0 0 0.983 0.975 1 . 0 0 0
ARF_4_18099 ADP-ribsylation factor 4 0.987 1 . 0 0 0 0.969 0.983 0.988 0.977
ATP_BC_259 ATP-bindincasette sub-family A member 1 1 . 0 0 0 1 . 0 0 0 1 . 0 0 0 1 . 0 0 0 0.988 0.989
BPNT_1_18778 3'(5'),5'-biphosphate nucleotidase 1 0.971 1 . 0 0 0 0.985 1 . 0 0 0 1 . 0 0 0 1 . 0 0 0
CLIC_5_10148 Chloride intracellular channel 5 0.568 0.487 0.521 0.492 0.521 0.492
COL17591 Cytochrome oxidase subunit I 1 . 0 0 0 1 . 0 0 0 1 . 0 0 0 1 . 0 0 0 1 . 0 0 0 1 . 0 0 0
COP_9_18132 266S protease regulatory subunit 7 0.950 0.962 0.968 0.968 0.988 0.966
CSDE_1_11069 Cold shock domain-containing protein E1 1 . 0 0 0 1 . 0 0 0 1 . 0 0 0 1 . 0 0 0 1 . 0 0 0 1 . 0 0 0
CSDE_1_19713 Cold shock domain-containing protein E1 0.950 1 . 0 0 0 0.968 0.983 0.963 0.977
CST_21113 Cystatin precursor 0.782 0.597 0.726 0.661 0.775 0.750
CYT_BC1_9061 Cytochrome b-cl complex subunit 2 1 . 0 0 0 1 . 0 0 0 1 . 0 0 0 1 . 0 0 0 1 . 0 0 0 1 . 0 0 0
EF_1G_4796 Translation elongation factor 1 gamma 1 . 0 0 0 1 . 0 0 0 1 . 0 0 0 1 . 0 0 0 1 .0 0 0 1 . 0 0 0
EF2_10494 Translation elongation factor 2 1 . 0 0 0 1 . 0 0 0 1 . 0 0 0 1 . 0 0 0 1 . 0 0 0 1 . 0 0 0
EIF_3F_341 Translation elongation factor 3 subunit F 0.872 0.892 0.967 0.967 0.910 0.932
EIF_3J_11587 Translation elongation faaor 3 subunit J 0.963 0.974 0.940 0.968 0.950 0.930
FER_H_20955 Ferritin heavy subunit 0.988 1 . 0 0 0 1 . 0 0 0 0.983 1 . 0 0 0 1 . 0 0 0
FGB_47 Fibrinogen Beta Chain 1 . 0 0 0 1 . 0 0 0 1 . 0 0 0 1 . 0 0 0 1 . 0 0 0 1 . 0 0 0
GAPDH_20355 Glyceraldehyde-3-phoshpate dehydrogenase 0.962 0.962 0.969 0.589 0.974 1 . 0 0 0
GDE1_2508 Glycerophosphochlorine phosphodiesterase 1 . 0 0 0 1 . 0 0 0 1 . 0 0 0 1 . 0 0 0 1 . 0 0 0 1 . 0 0 0
GOG_B1_15792 Golgin sub-family B member 1 0.987 0.987 0.970 0.968 1 . 0 0 0 0.966
GPX_4_19607 Glutathione peroxidase 4 1 . 0 0 0 1 . 0 0 0 1 . 0 0 0 1 . 0 0 0 1 . 0 0 0 1 . 0 0 0
HMG_T_9973 High mobility group-T protein 0.988 0.988 1 . 0 0 0 0.984 0.988 0.966
HSP_90A_15666 Heat shock protein 90 alpha 0.988 0.949 0.984 0.968 0.988 0.977
HSP_90B_21100 Heat shock protein 90 beta 0.895 0.949 0.966 0.984 1 . 0 0 0 1 . 0 0 0
HSPE_1_17854 10 kDa heat shock protein 1 . 0 0 0 1 . 0 0 0 1 . 0 0 0 0.984 1 . 0 0 0 1 . 0 0 0
IF_RF2_19747 Interferon regulatory factor 2 1 . 0 0 0 1 . 0 0 0 1 . 0 0 0 1 . 0 0 0 1 . 0 0 0 1 . 0 0 0
JAM_3_13916 Junctional adhesion molecule 3b 0.938 0.885 0.984 0.952 0.950 0.893
KRT_13_20618 Keratin 0.808 0.795 0.821 0.783 0.800 0.796
KRT_A_15738 Keratin alpha-like 0.975 1 . 0 0 0 0.952 0.984 0.960 0.988
LBL_L2_20921 No hit 1 . 0 0 0 1 . 0 0 0 1 . 0 0 0 1 . 0 0 0 1 . 0 0 0 1 . 0 0 0
LDH_B_9441 Laaase dehydrogenase B 1 . 0 0 0 1 . 0 0 0 0.952 0.950 1 . 0 0 0 1 . 0 0 0
Pujolar ef al. BMC Genomics (2015) 16:600 Page 5 o f 15
Table 1 Detaíls of all polymorphic loci, íncluding frequency of the most common aiíele across all silver eel (SE) and glass eeí (GE)
samples (Continued)
MDHJ393 Maiate dehydrogenase 0.449 0.592 0.567 0.603 0.615 0.476
MYH_14857 Superfast myosin heavy chain 0,514 0.473 0.500 0.516 0.425 0.489
MADH_4_21742 NADH dehydrogenase subunit 4 1 . 0 0 0 1 . 0 0 0 1 . 0 0 0 1 . 0 0 0 1 . 0 0 0 1 . 0 0 0
NADH_5_17101 NADH dehydrogenase subunit 5 0,974 1 . 0 0 0 1 . 0 0 0 1 . 0 0 0 1 . 0 0 0 0,977
NADH1 J0_21119 NADH dehydrogenase 1 alpha subunit 1 0 1 . 0 0 0 1 . 0 0 0 1 . 0 0 0 1 . 0 0 0 1 , 0 0 0 1 . 0 0 0
NCP„2_15547 Nudeoíar compíex protein 2 0.974 0.934 1 . 0 0 0 0.967 0,962 0.932
NEX_19953 Nexiíin 0.592 0.608 0.485 0.567 0.577 0.523
NGD_21138 Neuroguidin 0.795 0.842 0.906 0.758 0.825 0.852
NRAP_1541 Nebuiin-related anchoring protein 1 . 0 0 0 0.987 0.984 1 . 0 0 0 0.988 0.989
PA2G4_2600 Proliferation associated protein 2G4 0.663 0,645 0.652 0.550 0.575 0.580
PFNL15113 Profilin-2 1 . 0 0 0 1 . 0 0 0 1 . 0 0 0 1 . 0 0 0 1 . 0 0 0 1 . 0 0 0
PGD_18096 ð-phosphogluconate dehydrogenase 0.987 0.961 0.969 0.967 0.988 0.966
PGIJ Phosphoglucose isomerase-1 0.800 0.797 0.742 0.750 0.675 0.807
PGI_2 Phosphoglucose isomerase-2 0.552 0.566 0553 0.500 0.625 0.556
PGK_1_11454 Phosphogiycerate kinase 1 0.947 0.961 0.909 0.903 0.975 0.939
PRP_40_16504 Pre-mRNA-processing factor 40 homolog A 0.829 0.842 0.833 0.903 0.846 0.845
PSA_4_21534 Proteasome subunit alpha type-4 0.513 0.434 0.550 0.550 0.590 0.432
P5ME_1_21196 Proteasome aaivator 0.719 0.583 - 0,621 0.625 0.667
RFC_3_18186 Replication factor C subunit 3 0.763 0.776 0.773 0.717 0.800 0.784
RTF_1_21288 RNA pofymerase-associated protein RTF1 0.756 0.724 0.900 0.758 0.846 0.750
SDH_0 Sorbitoí dehydrogenase 1 . 0 0 0 1 . 0 0 0 1 . 0 0 0 1 . 0 0 0 1 . 0 0 0 1 . 0 0 0
5LC„25A5_19808 ADP/ATP translocase 2 1 . 0 0 0 1 . 0 0 0 0.967 0.984 1 , 0 0 0 1 . 0 0 0
5M_22_6449 Transgelin 0,963 0.934 0.946 0.952 0.950 0.955
SN4_TDR_374 Taphyiococcal nuclease domain-contaíning protein 0.962 0.910 0.919 0,862 0 . 8 8 8 0.909
TENT_02_11046 No hlt 0.744 0.711 0.739 0.774 0.713 0.784
TENT_03_12589 Coilagen type XXVii! alpha 1 a 0.949 0.987 1 . 0 0 0 0.968 0.988 0.966
TENT_05_19704 No hit 1 . 0 0 0 0.987 0.968 0.983 1 , 0 0 0 1 . 0 0 0
TENT_06_16512 Protein Phosphatase regulatory subunit 0.603 0.581 0.600 0.533 0.575 0.625
T£NT_07_21161 No hit 0.419 0.368 0.348 0.397 0.350 0.286
TNNT_2E_20968 Troponin T2e 0.949 0.885 0.913 0.875 0.838 0.895
TR1M_35_8416 Tripartite motif-contaning protein 35 0.692 0.658 0.750 0.629 0.641 0.698
TTN_B_20952 Titin b 1 . 0 0 0 1 . 0 0 0 1 . 0 0 0 1 . 0 0 0 1 . 0 0 0 1 . 0 0 0
TU B_A_19211 Tubulin aípha 2 1 . 0 0 0 1 . 0 0 0 1 . 0 0 0 1 . 0 0 0 1 . 0 0 0 1 . 0 0 0
UBI„A52_5049 Ubiquitin A-52 ribosomal protein fusion product 1 0.987 0.974 0.967 0.917 1 . 0 0 0 0.989
UGP„2_2128 UDP-gíucose pyrophosphorylase 2 0.671 0.541 0.531 0.690 0.663 0.546
UGP_A_2307 Glyceroi-3-phosphate transporter subunlt 0.671 0.603 0.600 0.613 0.600 0.636
UNA_SINE2_16912 Eel Short interspersed elements 1 . 0 0 0 1 . 0 0 0 1 . 0 0 0 1 . 0 0 0 1 . 0 0 0 1 . 0 0 0
ZETAJ5177 Tyr 3-monooxygenase 0.739 0.865 0.810 0.783 0.756 0.852
Prior to the analysis of local selection, the presence of
hybrids in the data set was assessed in STRUCTURE using
a subset of diagnostic SNPs between North Atlantic eeis
and prevíously analyzed RAD-sequenced American eeís
for comparison. A scenario with K = 2 groups correspond-
ing to the two North Atlantic eel species was suggested.
Within European eel, all RAD-sequenced silver eels were
identified as pure European eel, with no hybrids in the
data set.
In the RAD data set, outlíer tests were first conducted
comparíng silver eels (N = 31) and glass eels (N = 31)
from Valencia using 153,423 SNPs, A total of 2413 SNPs
Pujolar et al. BMC Genomics (2015) 16:600 Page 6 o f 15
Table 2 Summary of genetic diversity indices at 80 SNPs
inciuding observed (H0) and expected heterozygosities (He),
polymorphism at the 95 % and 99 % level, mean (MNA) and
total number of alleles (TNA) and allelic richness (AR) in all silver
eel (SE) and glass eel (GE) samples
N H0 He P95 P99 MNA TNA AR
Spain-SE 40 0.232 0.227 0.625 0.844 1.84 118 1.60
Spain-GE 44 0.224 0.228 0.641 0.859 1 . 8 6 119 1.63
Ireland-SE 40 0.226 0.233 0.641 0.891 1.89 1 2 1 1.62
Ireland-GE 39 0.236 0.233 0.656 0.844 1.84 118 1.62
lceland-SE 33 0 . 2 2 2 0.224 0.581 0.855 1 . 8 6 119 1.62
lceland-GE 40 0.272 0.249 0.625 0.938 1.94 124 1 . 6 6
Table 3 Candidate genes under selection at 80 SNPs in
LOSITAN and BAYESCAN. SE = Silver eels; GE = Glass eels
Samples LOSITAN BAYESCAN
All samples (SE + GE) ALD_R ALD-R
(He = 0.34;Fsr = 0.12; (BPP = 1.00; q = 0.000;
p = 0 .0 0 1 ) alpha = 2 .1)
GAPDH GAPDH
(He = 0.17; Fsr = 0.27; (BPP = 1.00; q = 0.000;
p = 0 .0 0 1 )
CLIC_5_10148
(He = 0.50; Fsr = 0.05;
p = 0.009)
alpha = 2 .6 )
Silver eels (SE) CLIC_5_10148
(He = 0.51;Fsr = 0.09;
p = 0.003)
LDH_B_9441
(He = 0.03; Fsr = 0.03;
p = 0.047)
SE(pooled) vs. GAPDH
GE(pooled)
(He = 0.14; Fsr = 0.05;
p = 0 .0 1 0 )
Spain (SE vs. GE) CLIC_5_10148
(He = 0.51; Fjr = 0.08;
p = 0.018)
Ireland (SE vs. GE) CST_21113
(He = 0.44; Fsr = 0.07;
p = 0.023)
CSDE_1_19713
(He = 0.05; Fsr = 0.04;
p = 0.049)
lceland (SE vs. GE) GAPDH GAPDH
(He = 0.41; Fst = 0.33; (BPP = 1.00; q = 0.000;
p = 0 .0 0 1 ) alpha = 2.4)
putatively under selection were identified by LOSITAN
and 1472 SNPs by BAYESCAN. Since the LOSITAN
outliers encompassed those outliers identified by BAYES
CAN, the rest of the analysis was conducted only for the
LOSITAN outliers.
Out of the 2413 candidate SNPs, a hit with a gene was
obtained for 1089 (45.13 %) of the SNPs, while the
remaining 1324 SNPs (54.87 %) were located in noncod-
ing regions of the genome. Among hits, 966 were
located in introns and 123 in exons, including 48 in
complete coding sequences (CDS). Hits represented a
total of 1018 unique genes, of which 835 (82.02 %) genes
were successfully annotated using BLASTX. Subsequently,
the KEGG pathway approach for higher-order functional
annotation was implemented in DAVID. Using zebrafish
as reference genome, a total of 616 zebrafish genes hom-
ologous to European eel were mapped to KEGG pathways.
Enriched KEGG pathways using a standard setting of
gene count = 2 are summarized in Table 6. The path-
ways with the highest number of genes were MAPK/
Erk signalling, calcium signalling, focal adhesion, cell
adhesion and GnRH signalling. A list of all annotated
genes is provided in Additional file 1: Table Sl.
We also tested for outliers between silver eels and glass
eels from Burrishoole, although adult sample size was low
(N = 10), as a way to confirm the results above. A total of
2228 putative SNPs under selection were identified by
LOSITAN and 1888 SNPs by BAYESCAN, the latter being
all included in the list of LOSITAN outliers. Among all
outlier SNPs, a hit with a gene was obtained for 949 of the
SNPs, 838 corresponding to introns and 111 to exons
(including 42 in CDS). In total, 770 (81.13 %) of the hits
were successfully annotated using BLASTX. Subsequently,
a total of 557 zebrafish genes homologous to European eel
were mapped to KEGG pathways in DAVID. The path-
way with the highest number of genes was endocytosis
(15 genes), while other highly-represented pathways
included regulatory and signalling pathways (Table 7). Im-
portantly, despite the limited number of RAD-sequenced
adults from Burrishoole, over-represented patliways were
similar to the ones found when comparing silver eels and
glass eels from Valencia. Shared over-represented path-
ways included signalling (i.e. MAPK/Erk, GnRH, cal-
cium or insulin) pathways and cell and focal adhesion.
A list of all annotated genes is provided in Additional
file 2: Table S2.
Finally, average FST values between silver eels and glass
eels from Valencia calculated using a 50-kb sliding
window were plotted for the 30 largest scaffolds. FST was
low throughout the scaffolds, with just a few narrow
peaks. No regions of the scaffolds with pronounced
divergence peaks were observed, consistent with pan-
mixia removing any effect of diversifying selection from
each new generation. Similar results were obtained when
Pujolar e t al. BMC Genomics (2015) 16:600 Page 7 o f 15
Table 4 Statistics describing the distribution of dífferent properties of RAD sequences after each step of filtering (FASTX-Toolkit),
alignment to the eel draft genome (BOWTIE) and assemblage into loci (STACKS) in silver eels (SE) and glass eels (GE)
FASTX
Group Raw reads Filtered reads % Eliminated Mean Q Q1 Med Q3 % A % C % G % T
SE 12234656 10692256 13.2 38.7 38 39.7 40 28.7 22.0 20.4 28.7
GE 9593701 7899505 17.8 38.7 38 39.4 40.2 29.5 20.7 20.4 29.4
BOWTIE
Group Reads Aligned % Aligned Non-aligned % Non-aligned Discarded % Discarded
SE 10692256 7433827 69.3 2782716 26.3 475668 4.5
GE 7899505 5527660 70.0 2018833 26.0 353043 4.5
STACKS
Group Reads Stacks Loci Loci used % Loci used Loci discarded % Loci discarded
SE 7433827 547017 348342 253864 73.9 94482 27.1
GE 5527660 526821 335343 217326 64.5 118016 35.5
using alternative (100-kb and 200-kb) sliding windows.
Figure 1 shows an example of the plots obtained for the
tlnree largest scaffolds (1, 3 and 21) in tlte European eel
draft genome. A total of 4, 5 and 6 peaks representing
outlier SNPs with higher FST relative to the background
were observed in scaffolds 1, 3 and 21, respectively. The
average distance between outlier SNPs was around
300,000 bp in scaffolds 1 and 3 and around 220,000 bp
in scaffold 21. The closest distance between outlier SNPs
was 9000 bp in scaffold 1, 19,000 bp in scaffold 21 but
around 125,000 bp in scaffold 3.
Discussion
Evidence fo r selection acting upon d iffe ren t life stages in
European eel
We examined the patterns of genomic diversity across
life cycle stages in European eel, using a combined ap-
proach of candidate coding-gene SNPs and a large-scale
genomic analysis of 153,423 SNPs generated by RAD se-
quencing. We compared two life cycle stages separated
by metamorphosis, glass eels (juvenile stage) and silver
eels (adult stage), and identifíed signatures of directional
selection. All available information indicates that eel
mortality in nature is very high and only a small fraction
Table 5 Summary of genetic diversity indices at 77,337 RAD-loci
including observed (H0) and expected heterozygosities (He) and
nucleotide diversity (Pi) considering only variant positions and
considering all positions in all silver eel (SE) and glass eel (GE)
samples
N Variant positions All positions
H0 He Pi H0 He Pi
Spain-SE 31 0.0479 0.0523 0.0532 0.0046 0.0050 0.0051
Spain-GE 31 0.0465 0.0508 0.0518 0.0044 0.0048 0.0049
Ireland-SE 1 0 0.0401 0.0420 0.0448 0.0039 0.0041 0.0043
Ireland-GE 29 0.0469 0.0505 0.0515 0.0045 0.0048 0.0049
of the glass eels entering European coasts reach the sil-
ver eel stage and migrate back to the Sargasso Sea [25].
Bonhommeau et al. [26] estimated a glass eel survival
rate of 10 %, while Áström and Dekker [14] estimated a
natural mortality rate of M = 0.14 per year and a fishery
mortality rate of F = 0.54 per year. Hence, the observa-
tion of outlier loci showing high genetic differentiation
when comparing glass eels vs. silver eels is consistent
with the action of natural selection acting upon eels.
FST-based outlier tests are based on the detection of loci
that show significantly high differentiation with signifi-
cance determined by simulations assuming specific
population structure models [271 and are being exten-
sively used at present in studies aiming at detecting
signatures of selection on a genome scale [28-31], al-
though results should be interpreted with caution (see
Bierne et al. [32] for a critique of outlier tests).
Using the SNP panel developed by Gagnaire et al. [15]
in American eel, a total of four loci showed higher
genetic differentiation tlaan the background FST when
comparing glass eel and silver eel samples. GAPDH
(Glyceraldehyde 3-phosphate dehydrogenase) is a gene
with a major metabolic function and catalyzes the con-
version of glyceraldehyde 3-phosphate to D-glycerate
1,3-biphosphate in the glycolysis pathway. In this sense,
GAPDH has been linked to growth differences in gene
expression studies in fishes [33]. CST (Cystatin precur-
sor) is a gene involved in catalytic activity that takes part
in defense response. CLIC5 (Chloride intracellular chan-
nel 5) is a gene involved in chloride ion transport, which
is important for pH regulation, volume homeostasis,
organic solute transport, cell migration, cell proliferation
and differentiation. CSDEl (Cold shock domain-containing
protein El) is a RNA-binding protein involved in regula-
tion of transcription. However, all outliers were location-
specific (GAPDH in Iceland, CLIC5 in Spain and CST and
CSDE in Ireland) and none was common across locations.
Pujolar et al. BMC Gerom ics (2015) 16:600 Page 8 o f 15
Table 6 Over-represented KEGG pathways when comparing
glass eels and silver eels from Valencia (Spain), including gene
count
Term Count
dre04010:MAPKÆrk signalling pathway 1 0
dre04510:Focal adhesion 9
dre04020:Calcium signalling pathway 8
dre04514:Cell adhesion molecules (CAMs) 7
dre04912:GnRH signalling pathway 7
dre04512:ECM-receptor interaction 6
dre04270:Vascular smooth muscle contraction 6
dre045B0:Tight junction 6
dre00230:Purine metabolism 6
dre04080:Neuroactive ligand-receptor interaction 6
dre04070:Phosphatidylinositol signalling system 5
dre04914:Progesterone-mediated oocyte
maturation
5
dre04910:lnsulin signalling pathway 5
dre00564:Glycerophospholipid metabolism 4
dre00562:lnositol phosphate metabolism 4
dre04370:VEGF signalling pathway 4
dre04540:Gap junction 4
dre04210:Apoptosis 4
dre04916:Melanogenesis 4
dre04810:Regulation of actin cytoskeleton 4
dre00534:Heparan sulfate biosynthesis 3
dre00480:Glutathione metabolism 3
dre04650:Natural killer cell mediated cytotoxicity 3
dre04620:Toll-like receptor signalling pathway 3
dre04012:ErbB signalling pathway 3
dre00240:Pyrimidine metabolism 3
dre04350:TGF-beta signalling pathway 3
dre04114:Oocyte meiosis 3
dre04120:Ubiquitin mediated proteolysis 3
dre04144:Endocytosis 3
dre00590:Arachidonic acid metabolism 2
dre00450:5elenoamino acid metabolism 2
dre00250:Alanine, aspartate and glutamate
metabolism
2
dre00030:Pentose phosphate pathway 2
dre00270:Cysteine and methionine metabolism 2
dre04621:NOD-like receptor signalling pathway 2
dre00310:lysine degradation 2
dre00330:Arginine and proline metabolism 2
dre04150:mTOR signalling pathway 2
dre04622:RIG-l-like receptor signalling pathway 2
dre04920:Adipocytokine signalling pathway 2
Table 6 Over-represented KEGG pathways when comparing
glass eels and silver eels from Valencia (Spain), including gene
count (Continued)
dre00010:Glycolysis / Gluconeogenesis 2
dre04260:Cardiac muscle contraction 2
dre04520:Adherens junction 2
dre04630:Jak-STAT signalling pathway 2
dre04142:Lysosome 2
dre03040:Spliceosome 2
This suggests that if the outliers detected indeed do repre-
sent selection, then they do not result from a universal se-
lection agent affecting eels in all places but rather location-
specific factors affecting eels locally.
A much larger number of candidate genes putatively
under selection were identified after screening a total of
153,423 RAD-generated SNPs across the genome: 2413
when comparing glass and silver eels from Spain and
2228 in the case of Ireland. Functional annotation ana-
lysis using DAVID identified signal transduction path-
ways as the most over-represented. Signal transduction
involves tlie binding of an extracellular signalling mol-
ecule (ligand) to a specific cell-surface receptor. The
activation of the receptor leads to an altered response
inside the cell. Examples of cellular responses to extra-
cellular stimulation that require signal transduction
include changes in metabolism and gene expression. Fol-
lowing are some major pathways identified in our study:
- MAPK/Erk signalling: a complex key signalling path-
way that is involved in the regulation of normal cell pro-
liferation, sui*vival, growth and differentiation [34]; the
pathway includes mitogen-activated protein kinases that
ultimately activate transcription factors and alter gene
transcription.
- GnRH signalling: secretion of gonadotropin-releasing
hormone from the hypothalamus acts upon its receptor
in the anterior pituitary to regulate the production and
release of FSH (follicle-stimulating hormone) and LH
(luteinizing hormone); together, FSH and LH regulate
many aspects of gonadal function in both males and
females, including normal growth, sexual development
and reproductive function [35].
- Calcium signalling: calcium ions serve a number of
important functions and regulate processes as diverse as
fertilization, development, learning and memory, mito-
chondrial function, muscle contraction and secretion;
calcium ions are also recognized as very important in
ion exchange and osmoregulation [36].
- Insulin-like growth factor signalling: this pathway
plays a central role in the neuroendocrine regulation of
animal growth and development. In fish, additional func-
tions include osmoregulatory acclimation, reproductive
development and tissue regeneration. Insulin-Iilce growth
Pujolar ef al. BMC Genomics (2015) 16:600 Page 9 o f 15
Table 7 Over-represented KEGG pathways when comparing
glass eels and silver eels from Burrishole (Ireland), including
gene count
Term Count
dre04144:Endocytosis 15
dre04514:Cell adhesion molecules (CAMs) 8
dre04510:Focal adhesion 8
dre04010:MAPK/Erk signalling pathway 8
dre04270:Vascular smooth muscle contraction 7
dre04912:GnRH signalling pathway 7
dre04020:Calcium signalling pathway 7
dre04080:Neuroactive ligand-receptor interaction 7
dre04060:Cytokine-cytokine receptor interaction 6
dre04142:Lysosome 6
dre04310:Wnt signalling pathway 6
dre04810:Regulation of aain cytoskeleton 6
dre04512:ECM-receptor interaction 5
dre04630Jak-STAT signalling pathway 5
dre04916:Melanogenesis 5
dre03040:Spliceosome 5
dre04120:Ubiquitin mediated proteolysis 5
dre04530:Tight junction 5
dre00051:Fruaose and mannose metabolism 4
dre04540:Gap junaion 4
dre04012:ErbB signalling pathway 4
dre04910:lnsulin signalling pathway 4
dre04110:Cell cycle 4
dre00512:0-Glycan biosynthesis 3
dre00520:Amino sugar and nucleotide sugar metabolism 3
dre00564:Glycerophospholipid metabolism 3
dre04920:Adipocytokine signalling pathway 3
dre04070:Phosphatidylinositol signalling system 3
dre04520:Adherens junaion 3
dre00290:Valine, leucine and isoleucine biosynthesis 2
dre00531:Glycosaminoglycan degradation 2
dre00532:Chondroitin sulfate biosynthesis 2
dre00534:Heparan sulfate biosynthesis 2
dre00640:Propanoate metabolism 2
dre00620:Pyruvate metabolism 2
dre00270:Cysteine and methionine metabolism 2
dre04130:SNARE interaaions in vesicular transport 2
dre00970:Aminoacyl-tRNA biosynthesis 2
dre04622:RIG-l-iike receptor signalling pathway 2
dre04330:Notch signalling pathway 2
dre04340:Hedgehog signalling pathway 2
dre03320:PPAR signalling pathway 2
Table 7 Over-represented KEGG pathways when comparing
glass eels and silver eels from Burrishole (Ireland), including
gene count (Continued)
dre00562:lnositol phosphate metabolism 2
dreOOOI 0:Glycolysis / Gluconeogenesis 2
dre04650:Natural killer cell mediated cytotoxicity 2
dre04620:Toll-like receptor signalling pathway 2
dre04914:Progesteronemediated oocyte maturation 2
factor signalling is mediated by two ligands, insulin-like
growth factor 1 (IGF-1) and factor 2 (IGF-2), both of
which were identified as outliers. The production of
IGF-1 is stimulated by growth hormone and is positively
correlated with growth as shown in coho salmon [37] or
sea bream [38].
- Focal adhesion: Related to signalling pathways, focal
adhesion was also over-represented in our analysis. Focal
adhesions are large protein assembles through which
both mechanical force and regulatory signals are trans-
mitted and have central roles in cell migration and mor-
phogenesis as well as regulating cell proliferation and
differentiation [39].
Other over-represented pathways were related to me-
tabolism (i.e. purine metabolism, glycerophospholipid
metabolism) and detoxification of xenobiotics (i.e. gluta-
thione metabolism). The latter included cytochrome
CYP2J6, a member of the cytochrome P450 superfamily
of enzymes that catalyze many reactions involved in
drug metabolism.
Overall, when we consider the functions of the genes,
it seems biologically plausible that the genes identified
as outliers are indeed under selection. Many of the over-
represented pathways were related to growth, while
others could result from the different conditions and
habitats that eels inhabit throughout their life cycle. In
this sense, examination of otoiith data suggests a high
plasticity of habitat use by eels [9], with one or several
movements between fresh and brackish waters through-
out the lifetime of an individual. When only a single
habitat switch event was detected, it occurred between 3
and 5 years of age, which could explain the differences
found in our study at osmoregulation genes between
glass eels and silver eels.
When comparing across methods, a much larger num-
ber of genes putatively under selection were identified
using tlie RAD genome scan approach. This is expected,
since we screened only 80 SNPs with the American eel
SNP panel, while we interrogated over 150,000 SNPs
with the RAD approach. However, when considering
percentage rather than total number of markers under
selection, results were similar. For instance, in the case
of Valencia we found 1.57 % of SNPs putatively under
selection using the RAD approach (2413 out of 153,423
Pujolar e t al. BMC Genomics (2015) 16:600 Page 10 of 15
-0 .0 0 5 .
1,000 1 ,5 0 0 2,000
0 .0 1 5
Scaffold 21
Scaffold 1
-0 .0 0 5 .
0 .0 1 5 '
—i-------------------------- 1---------------------------1------------------------ r~
5 0 0 1 ,0 0 0 1 ,5 0 0 2 ,0 0 0
Scaffold 3
0.000
- 0 .0 0 5 . (
0 5 0 0 1 ,0 0 0 1 ,5 0 0 2 ,0 0 0
b p ( x l 0 0 0 )
Fig. 1 Plots o f average FSi- calculated using a 50-kb sliding w indow for the three largest scaffolds (I, 3 and 21) in the European eel genom e
SNPs screened), with a similar percentage (1.25 %, 1 out-
lier out of 80) found using the American eel SNP array.
In the case of Burrishoole, candidate SNPs under selec-
tion were 1.45 % (2228 out of 153,423) using the RAD
approach and 2.5 % (2 out of 80) using the American eel
SNP array. Finally, it should be noted that outliers were
not shared across methods, which is explained by the
different nature of the markers. All SNPs included in
the array were Iocated in coding-genes, while the SNPs
discovered using the RAD approach were mostly lo-
cated in non-coding genes, since RAD tags are restric-
tion site generated markers randomly distributed across
the genome.
S up port fo r th e ad ap tive decou plin g hypothesis
The observation in our study of a large number of out-
lier loci showing higher Fsx values relative to the back-
ground when comparing glass eels and silver eels fits the
prediction that in the case of animals with complex life
cycles, different genes and gene pathways will be under
selection at different life stages. This is in accordance
with the adaptive decoupling hypothesis for the benefits
of metamorphosis [1], which predicts no correlation be-
tween traits separated by metamorphosis, thereby each
life stage can respond independently to its unique select-
ive pressures.
Moran (T[ hypothesized that the genetic decoupling
of pre- and post-metamorphosis life stages explains the
origin and persistence of complex life cycles, as alterna-
tive phases can be regarded as adaptations for a more
effective exploitation of resources and adaptations to
perform phase-specific tasks. In the case of eels, the sil-
vering metamorphosis, which represents the passage
from juvenile to adult, is accompanied by drastic modi-
fications at the physiological, morphological and eco-
logical level that could explain the shifts in selection
acting across life cycle stages. Changes occur both ex-
ternally (increase in eye size, change in colour from yel-
low-ish to silver, increase in body size and weight) and
internally (degeneration of the digestive track, changes of
visual pigments, development of gonads). While the ju-
venile stage is perfectly adapted for feeding, adults are not
able to feed anymore following metamorphosis, relying
solely on fat reserves to reach the Sargasso Sea. However,
Pujolar et al. BMC Genomics (2015) 16:600 Page 11 of 15
the adult stage is best adapted for migration, mating and
reproducing.
If selection vvere complementary between life cycle
stages separated by metamorphosis, the same genes and
pathways would be expected to be under selection be-
fore and after metamorphosis and no outlier loci show-
ing high diíferentiation would be expected. By contrast,
in our study we found up to 2413 outlier loci, suggestive
of opposing selection betxv'een life cycle stages, as pre-
dicted by the adaptive decoupling hypothesis.
Alternatively, results in our study could reflect changes
in genetic frequencies over time rather than a selection
effect. One possibility we cannot rule out is a temporal
effect, since juveniles and adults in our sampling were
not from the same cohort. Following the same cohort in
time would be ideal to test our hypothesis of opposing
selection during different life stages separated by meta-
morphosis, however this is virtually impossible in eels.
Age at maturity (at which the silvering metamorphosis
occurs) is highly variable in eels, ranging from 6 to
20 years or more _[7]. This means tliat individuals ffom
the same cohort will become silver eels at different times
and that adult eel samples for genetic studies are mostly
made up of a mix of different cohorts. Nevertheless, the
observation of a parallel pattern of genetic differentiation
in Valencia and Burrishoole when comparing glass eels
and silver eels, with many over-represented genes and
pathways being shared by the two locations, lends sup-
port to a selection effect.
G enom ic d is trib u tio n o f cand idate genes under selection
Genomic regions displaying elevated differentiation relative
to the rest of the genome (genomic islands of divergence)
have been described in many species, as exemplified in the
case of sticldebacks [28, 29]. In marine fishes, genomic
islands of divergence might be unexpected because of their
extremely high effective population sizes (Ne). Due to the
effects of Ne on the level of linkage disequilibrium, a fast
decay of linkage disequilibrium should be generally ex-
pected (reviewed in [40]), which in turn might preclude
hitchhiking and ultimately the observation of genomic
islands of divergence.
That might be the case of eels. In our study comparing
glass eels and silver eels, outlier SNPs showing liigh gen-
etic differentiation consistent with selection did not group
into clusters but were generally spread across the genome.
Similarly, no apparent genomic islands of divergence were
found when investigating the genomic distribution of out-
lier SNPs between European and American eel [41].
In contrast to the pattern observed in European eel,
genomic clustering of some highly divergent SNPs was ob-
served in Atlantic herring [30], a species with a very large
efiective population size. Elevated genomic differentiation
across large genomic blocks (up to 15 Mb) was also
reported in Atíantic cod [31, 42], which suggests that gen-
omic islands of divergence can occur in marine fishes.
However, it is likely that the different pattern observed in
eels (no clustering of genes) vs. Atlantic herring and
Atlantic cod (clustering of genes) might be due to the dif-
ferent impact of evolutionary forces acting upon the
panmictic European eel and other species that are genetic-
ally sub-structured. Therefore, unlike in eels, significant
linkage disequilibrium might occur in Atlantic herring
and Atlantic cod, thus allowing hitchhiking to accumulate,
which ultimately results in the clustering of genes with lo-
calized elevated differentiation relative to the background.
Finally, it should be noted that by using an FST-outlier
approach, the number of loci under selection might be
underestimated. While standard tests of selection (i.e.
outlier tests) are powerful tools to detect “hard selective
sweeps”, in which a new advantageous mutation arises
and spreads quickly to fixation due to natural selection
[43], other scenarios might be more difficult to detect.
Those include soft sweeps, in which an allele already
present in the population (i.e. standing variation) be-
comes selectively favoured or when multiple independ-
ent mutations at a single locus are all favoured [44], and
polygenic adaptation, in which simultaneous selection
occurs on variants at many loci [22, 45]. Both scenarios
lead to shifts in allele frequencies rather than fixation,
thus tend to be more difficult to detect than hard sweeps
using standard tests of selection [23, 45, 46]. Considering
the high historical effective population size estimated for
the European eel (from 100,000 to lxlO 6 individuals)
and associated high genetic variability [8], soft sweeps
might be more common than hard sweeps and hence
our study might have uncovered only a fraction of the
genes under selection across life stages in European eel.
Condusions
Our data supports the adaptive decoupling hypothesis
for the benefits of metamorphosis in European eel since
genes and gene pathways under selection were different
in pre- and post-silvering metamorphosis. The differ-
ences found between juveniles and adults suggests that
partitioning the life cycle into discrete stages may be
more effective than a single stage in the case of eels.
This way,each life stage can perform specific tasks more
effectively, i.e. feeding in glass eels, reproducing in silver
eels.
Methods
Ethical s ta tem en t
No experiments were conducted on the animals and ani-
mal manipulation was limited to sacrificing fish, using
the least painful method to obtain tissue samples for
DNA extraction. In all cases, in order to minimize the
suffering of the animals used in the study, fish were
Pujolar er al. BMC Genomics (2015) 16:600 Page 12 of 15
deeply anaesthetized with MS-222 (3-amonobenzoic acid
ethyl ester) or 2-phenoxyethanol 1 % and then painlessly
sacrificed. All procedures were conducted by technical
staff, who had all the necessary fishing and animal ethics
permits. In Iceland, sampling was approved by Holar
University College Ethical Committee and conducted
according to guidelines and laws on animal welfare in
Iceland. In Ireland, all sampling was carried out under
authorisation (Sec. 4) of the Fisheries Act 1959-2003 by
permission of the Department of Agriculture, Food and
Marine. In Spain, samples were obtained from profes-
sional fishermen with sampling and ethical treatment of
animals approved by the Consejeria de Medio Ambiente
of the Comunidad Autonoma de Valencia.
Sampling
A total of 113 silver eels (aduit stage) were collected at
three locations across tlie geographical distribution of
the species: (i) Valencia (Spain) in the Mediterranean Sea;
(ii) Burrishoole (Ireland), in the North Atlantic Ocean;
and (iii) four separate sampling sites in southwestern
Iceland that were pooled to increase sample size (Table 8).
All silver eels were caught using fyke nets. Silver eels were
compared to previously analyzed glass eels collected in
the same locations [11, 16]. We also used previously ana-
lyzed American eels for comparison [8, 16]. Genomic
DNA was extracted using standard phenol-chloroform
extraction.
SNP genotyping
A panel of 100 coding-gene single nucleotide polymor-
phisms (SNPs) developed by Gagnaire et al. [15] in
American eel was applied to all 113 silver eels in our
study (40 from Spain, 40 from Ireland and 33 fforn
Iceland). In a preliminary analysis, 20 out of the 100 pri-
mer sets did not give good amplification products in
European eel and were excluded. Subsequently, all indi-
viduals were genotyped at 80 SNPs [16], using the
Kbioscience Competitive Allele-Specific PCR genotyping
system (KASPar) (Kbioscience, Hoddeston, UK).
Within-sample genetic diversity was assessed by ob-
served and expected heterozygosities, polymorphism and
mean and total number of alleles using GENEPOP [47]
and standardized allelic richness using FSTAT [48]. Dif-
ferences in genetic diversity among samples were tested
by one-way ANOVA using STATISTICA (StatSoft Inc).
Deviations from Hardy-Weinberg equilibrium and differ-
ences in allele frequencies among samples were calcu-
lated using GENEPOP. Significance levels for multiple
comparisons were corrected using Bonferroni [49].
Prior to the test for selection, we tested the presence of
hybrid individuals in the dataset using STRUCTURE [50].
We included a set of 20 American eels for reference and
conducted the analysis assuming a I< = 2 scenario given
that two panmictic species were analyzed. We assumed an
admixture model, uncorrelated allele frequencies and we
did not use population priors. A burn-in length of 100,000
steps followed by one million additional iterations was
performed.
RAD sequencing
A subset of 41 silver eels (31 from Spain and 10 ffom
Ireland) were RAD-sequenced [51, 52] at BGI (Beijing
Genomics Institute, Hong Kong). In short, genomic DNA
for each individual was digested with restriction enzyme
EcoRI, ligated to a modified Illumina P1 adapter containing
Table 8 Sampling details including sampling date and locations and number of individuals genotyped using the American eel SNP
chip and number of individuals RAD sequended in all glass eel and silver eel samples
Country Location Coordinates Sampling date N-chip N- RAD
1) Glass eels
Spain Valencia 39° 46' N / 0° 24' W 2 0 1 0 44 31
Ireland Burrishoole 53° 90' N / 9° 58' W 2005 39 29
lceland Stokkseyri 63° 81' N / 21° 04' W 2 0 0 1 1 0 -
Vifilsstadvatn 64° 07' N / 21° 87’ W 2 0 0 1 1 0 -
Seljar 64° 56' N / 22° 31' W 2 0 0 1 1 0 -
Vogslækur 64° 69' N / 22° 33' W 2 0 0 1 1 0 -
2) Silver eels
Spain Valencia 39° 46' N / 0° 24' W 2 0 1 0 40 31
Ireland Burrishoole 53° 90' N / 9° 58' W 2 0 1 0 40 1 0
lceland Vatnsdalsá 65° 49' N / 20° 34' W 2 0 0 0 9 -
Grafarvogur 64° 15' N / 21° 81'W 2003 1 0 -
Vifilsstadvatn 64° 07' N / 21° 87'W 2 0 0 2 9 -
Grindavik 63° 83' N / 22° 42' W 2003 5 -
Pujolar e t al. BMC Genomics (2015) 16:600 Page 13 of 15
individual-spedfic barcodes and sheared to an average size
of 500 bp. Sheared DNA was separated by electrophoresis
on a 2 % agarose gel and fragments in the 350-500 bp size
range were selected. After treating dsDNA ends with end
blunting enzymes and adding 3’-adenine overhangs, a
modified Illumina P2 adapter was ligated. The final step
consisted in enriching the libraries by PCR amplification.
The libraries for the 41 silver eels were constructed to-
gether with those for 259 glass eels reported in Pujolar et
al. [llj , using the same methodology and conditions. RADs
for each individual were sequenced (10 individuals per se-
quencing lane) on an Iilumina Genome Analizer II.
The analysis of the RAD data was conducted simultan-
eously for the 41 silver eels plus 60 glass eels (31 from
Valencia and 29 from Burrishoole) that were first ana-
lyzed in Pujolar et al. [11] but were re-analyzed together
with the silver eels. This way, the same software and pa-
rameters were used for filtering, alignment to the eel
genome and SNP discovery, i.e. using the same version
of Stacks (version 1.09). Gene annotation and functional
annotation analysis were also conducted simultaneously
for silver eels and glass eels.
The 90 bp-long RAD sequences obtained from the
Illumina runs were sorted according to barcode and
quality filtered using the FASTX-Toolkit [53]. Criterion
for quality filtering was that all nucleotides positions
must have a minimum Phred score of 10, otherwise the
read was discarded. Final read length was trimmed to 75
nucleotides in order to minimize sequencing errors usu-
ally found at the tails of the sequences [8].
Quality-filtered reads were then aligned to the European
eel draft genome (www.eelgenome.com) using the un-
gapped aligner BOWTIE [54]. A maximum of two mis-
matches between reads and genome were allowed. In
order to avoid paralogs, reads with alternative (two or
more) alignments to the genome were excluded.
Assembly of RAD sequences into loci and SNP identi-
fication were performed using the ref.map.pl pipeline in
Stacks version 1.09 [55]. First, pstacks was used to align
exactly-matching sequences into stacks that were subse-
quently merged to form putative loci. At each locus, nu-
cleotide positions were examined and SNPs were called
using a maximum likelihood framework. A minimum
stack depth of 10 was used. Second, cstacks was used to
build a catalog of all existing loci and alleles after mer-
ging loci from multiple individuals. Third, sstacks was
used to match all individuals against the catalog. Finally,
the program Populations in Stacks was used to process
all SNP data across individuals. The minimum percent-
age of individuals in a population required to process a
locus was set to 66.67 %.
Prior to the SNP analysis, loci in the catalog were fur-
ther filtered in order to remove paralogs and otherwise
spurious loci according to the following three criteria:
exclude loci with extremely higher coverage as it might
indicate the presence of more than one locus (threshold
used was twice the standard deviation from the mean
number of reads); exclude tri-allelic loci since the pres-
ence of more than two alleles might result from sequen-
cing errors; exclude loci containing SNPs with observed
heterozygosity (H0) of 1 (all individuals genotyped were
heterozygotes) or 0 (all individuals homozygotes), sug-
gestive of the presence of more than one locus.
Measures of genome-wide genetic diversity, including
observed and expected heterozygosities and nucleotide di-
versity were calculated in Stacks. Differences in genetic di-
versity among samples were tested by one-way ANOVA
using STATISTICA. Deviations from Hardy-Weinberg
equilibrium and genetic differentiation were calculated in
GENEPOP.
We also tested for hybrids using a subset of species-
specific diagnostic SNPs (FSt = 1) between European and
American eel [56]. The analysis in STRUCTURE in-
cluded RAD sequenced individuals in this study together
with a sample of 30 RAD-sequenced American eels for
comparison. STRUCTURE was run following the param-
eters described above.
Identifica tion o f candidate SNPs under selection
Candidate SNPs for being under directional selection
were identified using two different outlier tests. First, we
used the selection detection workbench LOSITAN [57],
which uses a coalescent-based simulation approach to
identify outliers based on the distributions of heterozy-
gosity and FST [58]. A neutral mean FST was enforced by
removing potentially non-neutral loci after calculating
an initial mean FST, as recommended by Antao et al.
[57]. We used a very strict threshold of 0.995 and a 10 %
false discovery rate to minimize thte number of false
positives. Second, outlier SNPs were also detected using
BAYESCAN [59], a Bayesian method based on a logistic
regression model that separates locus-specific effects of
selection from population-specific effects of demog-
raphy. BAYESCAN runs were implemented using default
values for all parameters, including a total of 100,000
iterations after an initial burn-in of 50,000 steps. Poster-
ior probabilities, q values and alpha coefficients were
calculated. A q-value of 10 % was used for significance.
C andidate gene an no ta tion
Genomic position of the candidate SNPs for local selec-
tion were established on the basis of the gene predictions
for the European eel genome (http://\\rww.zfgenomics.org/
sub/eel) using a custom-made script [11]. SNPs were con-
sidered to be located in a gene when included in CDS
(complete coding sequences), exonic and intronic regions.
Functional annotation of those genes was obtained using
Blast2Go [60], which conducts BLAST similarity searches
http://www.eelgenome.com
http:////rww.zfgenomics.org/
Pujolar et al. BMC Genomics (2015) 16:600 Page 14 of 15
and maps GO (Gene Ontology) terms to the homologous
sequences found. Only ontologies with E-value < 1E-6,
annotation cut-off > 55 and a GO Weight > 5 were consid-
ered for annotation. Additionally, functional interpretation
of the set of candidate genes was obtained using the
DAVID (Database for Annotation, Visualization and Inte-
grated Discovery) web-server v6.7 [61]. We conducted the
analysis in DAVID to establish whether several genes were
associated with the same function or pathway and there-
fore facilitate interpretation of our results, regardless of
statistical significance. The zebrafish [Danio rerio) genome
was used as reference for annotation. Prior to the analysis
in DAVID, a local BLAST was conducted for significant
matches directly against zebrafish Ensembl proteins using
BLASTX. Zebrafish Ensembl Gene IDs were obtained
from the corresponding Ensembl protein entries using the
Biomart data mining tool [62]. Gene functional analysis in
DAVID was conducted defming the zebraíish lDs corre-
sponding to those genes including a locally selected SNP
as ‘Gene list’ and the zebrafish IDs corresponding to all
genes as 'Background’. Standard settings of gene count = 2
and ease = 0.1 were used.
Finally, patterns of differentiation across genome re-
gions were characterized to test whether genes putatively
under selection were grouped into clusters (genomic
islands of differentiation) or more scattered across the
genome. We estimated levels of genetic differentiation
between glass eels and silver eels in Valencia by calculat-
ing average FST for 50-kb genomic sliding windows.
Alternative sliding windows (100 and 200-kb) were also
tested. Windows were restricted to the 30 largest scaf-
folds (903,936 - 2,025,234 bp) from the European eel
draft genome.
A vailab ility o f su pp orting data
The data set supporting the results of this article is
available from Dryad: http://datadryad.org/resource/
doi:10.5061/dryad.kclql. All sequencing files (.fastq)
can be found on the NCBI's Sequence Read Archive
under accession number SAMN03786011.
Competing interests
Tha authors declare that they have no competing interests.
Authors' contributions
MMH and LB conceived and aesigned the projea. JMP conducted population
genetics analyses with help from MMH and MWJ. JMP wrote the manuscript
with contributions from MMIH, LB, MWJ, DB, BJ and JLC. All authors read and
approved the final version o f the manuscripc
Acknowledgements
We thank Russel Poole for providing samples and Annie Brandstrup for
technical assistance. We acknowledge funding from the Danish Council for
Independent Reasearch, Natural Sciences (grant 09-072120 to MMH).
Author details
'Department o f Bioscience, Aarhus University, Aarhus C, Aarhus, Denmark.
2National institute o f Aquatic Resources, Technical University o f Denmark,
Silkeborg, Denmark. 3National Museum o f Natural Sciences (CSIC), Madrid,
Spain. 4Biopol, Marine Biology and Biotechnology Center, Skagastrond,
lceland. sIBIS (Institut de Biologie Intégrative et des Systémes), Université
Laval, Québec, Canada.
Received: 16 December 2014 Accepted: 6 July 2015
Pub lished online: 13 A u g u st2 0 1 5
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Additional file 1: Table S1. List all annotated genes detected as outliers
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JOINT EIFAAC/ICES/GFCM WGEEL REPORT
2014
ICES A d viso ry Committee
ICES CM 201 4/ACOM:l 8
Ref. ACOM, WGRECORDS, SSGEF, FAO, EIFAAC & GFCM
Report of the Joint EIFAAC/ICES/GFCM
Working Group on Eel
3-7 November 2014
Rome, Italy
ICES Intemational Council for the Exploration of the Sea
CIEM Conseil Internationai pour l’Exploration de la Mer
International Council for the Exploration of the Sea
Conseil International pour l'Exploration de la Mer
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Denmark
Telephone (+45) 33 38 67 00
Telefax (+45) 33 93 42 15
w w w .ices.dk
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R ecom m ended format for purposes of citation:
ICES. 2014. Report of the Joint EIFAAC/ICES/GFCM W orking Group on Eel, 3 -7 N o-
vem ber 2014, Rome, Italy. ICES CM 2014/ACOM:18. 203 pp.
For perm ission to reproduce material from this publication, p lease apply to the Gen-
eral Secretary.
The docum ent is a report o f an Expert Group under the auspices of the Intem ational
Council for the Exploration of the Sea and does not necessarily represent the v iew s of
the Council.
© 2014 Intem ational Council for the Exploration of the Sea
http://www.ices.dk
mailto:info@ices.dk
Jo in t E IF A A C /IC E S /C F C M WCEEL REPORT 2 0 1 4
C o n te n ts
Executive su m m ary................................................................................................................................5
1 In trodu ction ..................................................................................................................................... 8
1.1 M ain task s...............................................................................................................................8
1.2 P artidpants............................................................................................................................ 9
1.3 The European eel: life history and production ......................................................... 9
1.4 A nthropogenic im pacts on the s to ck ............................................................................9
1.5 The m anagem ent framework of e e l ............................................................................10
1.5.1 EU and M ember State w aters........................................................................10
1.5.2 Non-EU states......................................................................................................11
1.5.3 Other intem ational legislative drivers.......................................................11
1.6 A ssessm ents to m eet m anagem ent n e e d s ................................................................ 12
1.7 C onclusion ............................................................................................................................13
2 ToR a): A ssess the latest trends in recruitm ent, stock and fish eries,
in c lu d in g effort, and other anthropogenic factors in dicative o f the
status o f the stock, and report on the state o f the in tem ation a l stock and
its m ortality ................................................................................................................................... 14
2.1 Recruitment tren d s............................................................................................................14
2.1.1 Tim e-series available........................................................................................14
2.1.2 Sim ple geom etric m ean s................................................................................. 16
2.1.3 GLM based tren d ...............................................................................................19
2.1.4 Are there significant changes in trend?.................................................... 21
2.2 Tim e-series of yellow and silver eel abundance.....................................................36
2.3 Comm ercial fishery landings trends...........................................................................36
2.4 Recreational and non-com m ercial fish eries............................................................. 39
2.5 M isreporting of data, and illegal fisheries................................................................ 40
2.6 N on-fishery anthropogenic m ortalities.....................................................................40
2.7 Eel stocking.......................................................................................................................... 41
2.7.1 Trends in stocking.............................................................................................41
2.8 Aquaculture production of European ee l..................................................................46
2.9 Environm ental drivers.....................................................................................................47
2.10 Tables ....................................................................................................................................48
3 ToR e) Further d evelop the stock-recruitm ent relation sh ip and
associated reference points, u sin g the latest availab le d a ta .....................................60
3.1 Introduction......................................................................................................................... 60
3.2 Reference points used or im plicated in previous ICES A d v ice .........................60
3.3 Objectives and targets/lim its of the Eel R egu lation .............................................. 61
3.4 M ultiple criteria..................................................................................................................62
Jo in t E IF A A C /IC E S /G FC M WGEEL REPORT 2 0 1 4
3.4.1 Knock-on effects of spaw ning stock d ep letion .......................................62
3.4.2 Sensitivity to extem al or random perturbations................................... 63
3.4.3 Speed of recovery...............................................................................................63
3.5 General stock-recruit relation, short-lived species protocol..............................64
3.6 The age com position of the silver eel run escaping to the o cea n .....................64
3.7 A ssessm ent m eth od s........................................................................................................ 65
3.7.1 Trend-based assessm en t.................................................................................65
3.7.2 Eel specific reference points based on stock recruitment
relationship ..........................................................................................................68
3.7.3 Quantitative assessm ent applying generic reference p oints 74
3.8 A provisional harvest control rule for ee l................................................................. 78
3.9 Future developm ent priorities......................................................................................80
3.10 Tables ....................................................................................................................................81
4 ToR c) O verview of availab le data and gaps for stock a ssessm en t........................83
4.1 Introduction......................................................................................................................... 83
4.2 Consideration of data required.....................................................................................83
4.2.1 Stock assessm ent................................................................................................83
4.2.2 Data needs for stock-recruitm ent relationship.......................................85
4.3 Data quality issu es.............................................................................................................87
4.4 Data available vs gap s......................................................................................................88
4.5 Prioritization for future work (based on identified gap s)...................................88
4.6 Recom m endation from this chapter............................................................................89
5 ToR d) Identification o f su itable too ls (m odels, reference p o in ts etc.) in
both data rich and data poor s itu a tio n s............................................................................ 90
5.1 Introduction......................................................................................................................... 90
5.2 M ethods available to assess silver eel production and escap em en t 90
5.2.1 M ethods based on catching or counting silver eels...............................90
5.2.2 M ethods based on yellow eel p rox ies........................................................92
5.2.3 M odel-based approaches to estim ate potential and actual
silver eel escapem ent........................................................................................94
5.2.4 U se of other m ethods and extrapolations to calculate or
estim ate biom ass reference p o in ts.............................................................102
6 ToR b) R eview the life-h istory traits and m ortality factors b y ecoregion
.......................................................................................................................................................... 103
6.1 Introduction....................................................................................................................... 103
6.2 Life-history traits relevant to eel assessm en t.........................................................104
6.3 ICES ecoregion vs other geographic sca les ............................................................ 106
7 ToR f (i)) Explore the standardization of m ethods for data collection ,
an alysis and a ssessm en t........................................................................................................107
7.1 Introduction....................................................................................................................... 107
7.2 Available inform ation in eel p rodudng countries...............................................107
J o in t E IF A A C /IC E S /G FC M WGEEL REPORT 201 4
7.3 Startdardized approach................................................................................................. 109
7.4 R ecom m endations.......................................................................................................... 115
7.5 Tables....................................................................................................................................115
8 ToR f (ii)) ... and w ork w ith ICES DataCentre to d evelop a database
appropriate to eel a long ICES standards (and w id er geography)........................125
8.1 Introduction....................................................................................................................... 125
8.2 WGEEL Stock A ssessm ent database........................................................................ 125
8.3 Existing databases............................................................................................................126
8.3.1 Recruitment Index database......................................................................... 126
8.3.2 EU-POSE Project-DBEEL database.............................................................127
8.3.3 Intem ational Eel Quality D atab ase............................................................128
8.3.4 Data Collection Fram ew ork ......................................................................... 128
8.4 Pros and cons for ICES DataCentre hosting an eel database............................ 129
8.5 Work Plan for developing a w orking group d atab ase...................................... 129
8.6 C onclu sion ......................................................................................................................... 130
9 ToR g) Provide guidance on m anagem ent m easures that can be applied
to both EU and non-EU w aters........................................................................................... 132
9.1 Introduction....................................................................................................................... 132
9.2 A nalysis o f M anagem ent M easures reported ....................................................... 133
9.2.1 A quaculture........................................................................................................134
9.2.2 Fisheries................................................................................................................134
9.2.3 Hydroelectric turbines, pum ps and obstacles..........................................135
9.2.4 Habitat im provem ent......................................................................................137
9.2.5 Stocking................................................................................................................138
9.2.6 Other m anagem ent op tion s.......................................................................... 139
9.3 Post-evaluation................................................................................................................. 141
9.4 C on clu sion s....................................................................................................................... 142
9.5 R ecom m endations...........................................................................................................142
A nnex 1: Reference l i s t .................................................................................................... 143
A nnex 2: Participants lis t ................................................................................................. 149
A n n ex3: M eetin g agen d a................................................................................................155
A nn ex 4: WGEEL responses to the generic ToRs for R egion al and
Sp ecies W orking G roups.......................................................................................................157
A n n ex5: Research n e e d s .................................................................................................164
A nnex 6: Forward Focus o f the WGEEL.................................................................... 166
A nnex 7: Formal recom m endations of WGEEL 2014........................................... 169
A nnex 8: WGEEL responses to the T echnical R ev iew Group
m inu tes, 2013 ............................................................................................................................. 171
Jo in t E IF A A C /IC E S /G FC M WGEEL REPORT 2 0 1 4
A n n ex9: G lossary ..............................................................................................................196
A nn ex 10: Country Reports 2013-2014: Eel stock, físh eries and habitat
reported b y cou n try .................................................................................................................201
Executive su m mary
Jo in t E IF A A C /IC E S /C F C M WCEEL REPORT 2 0 1 4
The Joint EIFAAC/ICES/GFCM W orking Group on Eel [WGEEL] m et at FAO HQ,
Rome, Italy from 3 -7 Novem ber 2014. The group w as chaired by A lan Walker (UK)
and there w ere 44 participants representing 20 countries, the General Fisheries Com-
m ission of the Mediterranean (GFCM) and the EU's DG MARE. Information w as also
provided by correspondence from Estonia and Finland for use by the W orking Group.
WGEEL m et to consider questions posed by ICES (in relation to the M oU betw een the
EU and ICES), EIFAAC and GFCM and also generic questions for regional and species
W orking Groups posed by ICES. The terms of reference w ere addressed by review ing
w orking docum ents prepared ahead of the m eeting as w ell as the developm ent of doc-
um ents and text for the report during the m eeting. The w ork is sum m arised in the
fo llow in g points:
The WGEEL glass eel recruitment index has increased in the last three years, to 3.7%
of the 1960-1979 reference level in the 'North Sea' series, and to 12.2% in the 'Else-
where' series. The 'recruiting yellow eel' index has risen to 36% of the same reference
period, from a low of 7% in 2013. The reference period for glass eel indices starts at
1960 because there is only one dataset m eeting the index requirem ents before this year.
The reference period for 'recruiting y ellow eel' is set as the sam e years to be consistent
w ith the glass eel indices.
Statistical analyses of recruitment indices using segm ented regression A N O V A and
Bayesian approaches detected a significant breakpoint (an upturn) in both North Sea
and Elsewhere indices in 2011-2012. It w as not possible to determine whether this up-
turn can be considered a trend shift, as this short positive trend could be the result of
the tim e-series auto-correlation. H ow ever, if these positive trends are confirm ed and
continue in the future w ithout anv changes, the recruitment indices w ou ld be expected
to exceed the reference level around 2030 in "North Sea" and 2045 in "Elsewhere" in-
dices. Better understanding of the functioning of the population is required to make
these analyses more robust. There is no statistical evidence of an u ptum in the recruit-
ing yellow eel time-series.
F ollow ing the 2012 reporting of the assessed area, the levels of silver eel escapem ent
biom ass w ere as follows: escaping silver eel (Bcurrem 12 000 t), present potential escape-
m ent in the absence of anthropogenic mortality (Bbest 49 000 t), and 'pristine' potential
escapem ent w ith no anthropogenic m ortality (Bo 194 000 t). This indicates that current
(2012) silver eel escapem ent biom ass from the assessed area w as at 6% of the 'pristine'
state, or equal to 25% of the present potential if no anthropogenic im pacts existed.
The total landings from commercial fisheries in 2013, provided in Country Reports,
w ere 2470 t of eel. The current state of know ledge on level of underreporting, m is-
reporting and illegal fisheries is insufficient to include these in the assessm ent. Catch
and landings data for recreational fisheries are not consistently reported in the Country
Reports: inconsistencies in environm ents, fishing gears, life stages sam pled. Therefore,
it w as not possible to assess the m ost recent total landings and catches of recreational
and non-com m ercial fisheries.
A bout 39 m illion glass eels and 15 m illion yellow eels w ere stocked in 2013. Aquacul-
ture production has s low ly decreased to about 5000 t in 2013. N o n ew data on the im-
pacts of non-fishing anthropogenic factors w ere available to WGEEL 2014: EU Member
States w ill provide updates next year w ithin their 2015 Eel M anagem ent Plan Progress
Reports to the EU Com m ission.
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The w orking group review ed the life-history trait (LHT) inform ation available in the
Country Reports that w ould be required to conduct an eel stock assessm ent based on
m ethods proposed for "Data-limited stocks" (DLS) by WKLIFE. Data w ere lim ited but
large variations in LHTs w ere found, both for regional populations as a w hole and for
the sex (male, fem ale) and eel stage (glass, yellow , silver) categories, leading the work-
ing group to tentatively conclude that DLS approaches based on LHT m ay not be suit-
able for eels. Furthermore, the w orking group noted that the presently adopted
national and 'w hole stock' spatial scales of eel assessm ent were m ore relevant than the
standard ICES Ecoregions.
The data requirem ents for intem ational stock assessm ent, the data available and the
gaps in those data w ere review ed by the working group. Reported comm ercial land-
ings from countries that have not im plem ented Eel M anagem ent Plans (because they
are not subject to the EC Eel Regulation) accounted for about 27 to 39% of the total
reported eel catch in som e years. Therefore, the addition of data from countries not
covered by the stock assessm ent so far is urgently required, but so too are im prove-
m ents in the spatial coverage and quality of data for the EU countries im plem enting
and reporting on EMPs. The GFCM is working w ith the Mediterranean cm mtries to
provide their required data, w ith the support of the w orking group.
The w orking group review ed the application of approaches used to estim ate local or
national silver eel escapem ent, categorised as m ethods based on catching and counting
silver eels versus m ethods based on yellow eel proxies, w ith the latter including short
descriptions of 'eel m odels' sum m arising m odel approach and processes, data require-
m ents and m odel outputs. This review is intended as a starting point for those w ish ing
to im plem ent n ew local and national eel stock assessm ents.
The w orking group further developed the m ethods proposed to conduct the intem a-
tional, w hole-stock assessm ent, noting that the Eel Regulation's lim it for the escape-
m ent b iom ass o f (maturing) silver eels at 40% of the natural escapem ent (in the absence
of any anthropogenic impacts) is equivalent to the ICES Biim . Given that the estim ate of
present silver eel escapem ent biom ass from reporting EU coim tries is 6% of Bo, far be-
low the 40% lim it set by the EU Eel Regulation, the w orking group focussed attention
on the shape of the line of the m odified Precautionary Diagram below Bum (i.e. 40%).
The R eview Group for ICES-WGEEL (2013) suggested the application of criteria for
short-lived stocks (ICES 2013a), im plying total anthropogenic m ortality (L A ) = 0 for
Bcmrent <40% of Bo. The working group considered that because the spaw ning escape-
m ent com prises m any year classes and annual perturbations in recruitment, produc-
tion or spaw ning stock w ere buffered by up to 40+ year classes alive in any one year,
the eel w as 'long lived' in relation to ICES harvest control m les. Therefore, in the ab-
sence of indication on the required rate of stock recovery (the Eel Regulation terms it
"in the long term"), and pending an im provem ent of the analysis of stock-and-recm it
data, the w orking group proposed the basis of the harvest control rule for quantitative
assessm ents (category 1), i.e. a proportional reduction in LAiim below Bum d ow n to LAum
= 0 at Bcurrent = 0. The w orking group noted, however, that the unusual form of the ten-
tative stock-recm itm ent relationship m ight suggest that the mortality rate w ou ld have
to reach zero at a spaw ning-stock biom ass > 0, but the shape of the line is m ore im-
portant for setting advice in the im m ediate future than the point at w hich it intersects
the x-axis.
A standardized assessm ent approach applied across the entire eel-producing countries
w ou ld provide a m eans to address gaps in data reporting, and to exam ine the compa-
rability of national estim ates that are presently based on different data and analyses.
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The w orking group review ed and tabulated the eel- and anthropogenic-data available
from eel-producing countries. The m ost com m on data available are yellow eel densi-
ties. H ow ever, these are not available from lakes, large/deep/w ide river sections and
transitional waters, and since these habitats can represent the majority of the w etted
area in an EMU, this w ill require n ew m ethods to convert catch per unit effort data to
density data. The w orking group proposed a coordinated research program to develop
this standardised / cross-calibrating assessm ent m ethod.
The w orking group recom m ended the creation of a digitised data reporting database,
to make the preparation of assessm ents m ore effident, to provide a readily accessible
historical archive, and to facilitate national reporting to all international fora (e.g. ICES,
EU, CITES, DCF). The long-term objective of such standardization is to facilitate the
creation of an intem ational database of eel stock parameters updated annually. The
w orking group catalogued the existing eel databases (recm itm ent, POSE, eel quality)
and d eveloped a structured plan for storing data w ithin the ICES Data Portal.
The w orking group catalogued the variety of m anagem ent m easures that are being
im plem ented w ithin the national and local Eel M anagem ent Plans. These actions were
categorised as those relating to commercial fisheries; recreational fisheries; hydro-
pow er and obstacles; habitat im provem ent; stocking; and, others. This catalogue is in-
tended as a starting reference for those w ish ing to im plem ent n ew programs of
m anagem ent m easures.
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1 Introduction
1.1 Main tasks
The Joint EIFAAC/ICES/GFCM W orking Group on Eel [WGEEL] (chaired by: Alan
Walker, UK) m et at FAO HQ in Rome, Italy betw een 3 -7 N ovem ber 2014 to consider
(a) terms of reference (ToR) set by ICES, EIFAAC and GFCM in response to the request
for A dvice from the EU (through the M oU betw een the EU and ICES), EIFAAC and
GFCM, and (b) relevant points in the Generic ToRs for Regional and Species W orking
Groups.
The m eeting w as preceded by a Task Leaders coordination m eeting on Sunday 2 N o-
vem ber and the full m eeting w as opened at 09:00 am on M onday 3 N ovem ber (the
m eeting agenda is provided in Annex 7). The terms of reference w ere met. The report
chapters are linked to ToR according to the follow ing structure:
The report chapters are linked to ToR (as indicated in the table below ) but the order
that they are presented in the report is slightly different from the order of the ToR. The
m ain b ody of the report is structured in three parts: description of the data and trends
used in the present assessm ent of stock status (Chapter 2); developm ent of the assess-
m ent m ethod (Chapters 3 to 8); and, m anagem ent options (Chapter 9).
ToR a) Assess the latest trends in recruitment, stock and fisheries, including
effort, and other anthropogenic factors indicative of the status of the
stock, and report on the state of the intemational stock and its
mortality
Chapter 2
ToRb) Review the life-history traits and mortality factors by ecoregion Chapter 6
ToRc) Overview of available data and gaps for stock assessment Chapter 4
ToR d) Identification of suitable tools (models, reference points etc) in both
data rich and data poor situations
Chapter 5
ToRe) Further develop the stock-recruitment relationship and assodated
reference points, using the latest available data
Chapter 3
ToRf) Explore the standardization of methods for data collection, analysis
and assessment, and work with ICES DataCentre to develop a
database appropriate to eel along ICES standards (and wider
geography)
Chapter 7&8
ToRg) Provide guidance on management measures that can be applied to
both EU and non-EU waters
Chapter 9
ToTh) Address the generic EG ToR from ACOM Annex 3
The responses to the recom m endations of the R eview Group of the 2013 (the Technical
M inutes, Annex 9 of the 2013 report) are provided in Annex 7.
In response to the ToR, the W orking Group considered 18 Country Report W orking
D ocum ents subm itted by participants (Annex 10); other references cited in the Report
are g iven in A nnex 1. A dditional information w as supplied by correspondence, by
those W orking Group mem bers unable to attend the m eeting. A glossary of terms and
list o f acronym s used w ithin this docum ent is provided in Annex 9.
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1.2 Participants
Forty-four experts attended the m eeting, representing 20 countries, the EU DG MARE
and the Secretariat of the General Fisheries C om m ission of the M editerranean (GFCM).
A full address list for the m eeting participants is provided in Annex 2. Albania, M on-
tenegro, Tunisia and Turkey were represented at the w orking group for the first time.
1.3 The European eel: life history and production
The European eel (Anguilla anguilla) is distributed across the majority of coastal coirn-
tries in Europe and North Africa, w ith its southem lim it in Mauritania (30°N) and its
northern lim it situated in the Barents Sea (72°N) and spanning all of the M editerranean
basin. C om m ission D ecision 2008/292/EC of 4 April 2008 established that the Black Sea
and the river system s connected to it did not constitute a natural eel habitat for
European eel for the purposes of the Regulation establishing m easures for the recovery
of the stock of European eel (EC 1100/2007: European Council, 2007).
European eel life history is com plex and atypical am ong aquatic species, being a long-
lived sem elparous and w id ely dispersed stock. The shared single stock is genetically
panm ictic and data indicate the spaw ning area is in the southw estern part of the Sar-
gasso Sea and therefore outside Com m unity Waters. The n ew ly hatched leptocephalus
larvae drift w ith the ocean currents to the continental shelf of Europe and North Africa
w here they m etam orphose into glass eels and enter continental waters. The growth
stage, know n as yellow eel, m ay take place in marine, brackish (transitional), or fresh-
waters. This stage m ay last typically from tw o to 25 years (and could exceed 50 years)
prior to m etam orphosis to the silver eel stage and maturation. Age-at-m aturity varies
according to temperature (latitude and longitude), ecosystem characteristics, and den-
sity-dependent processes. The European eel life cycle is shorter for populations in the
southern part of their range com pared to the north. Silver eels then migrate to the Sar-
gasso Sea where they spaw n and die after spawning, an act not yet w itnessed in the
w ild .
The am ount of glass eel arriving in continental waters declined dramatically in the
early 1980s, w ith tim e-series indices (see below for further detail) reaching m inim a in
2011 of less than 1% in the continental North Sea and less than 5% elsew here in Europe
com pared to the m eans for 1960-1979 levels (ICES, 2011a). The reasons for this decline
are uncertain but m ay include overexploitation, pollution, non-native parasites and
other diseases, migratory barriers and other habitat loss, m ortality during passage
through turbines or pum ps, and/or oceanic-factors affecting migrations. These factors
w ill have been m ore or less important on local production throughout the range of the
eel, and therefore m anagem ent has to take into account the diversity of conditions and
im pacts in Com m unity Waters, in the planning and execution of m easures to ensure
the protection and sustainable use of the population of European eel. The recruitment
indices have increased in the m ost recent three years, but on ly so far to about 4 and
12% of the m ean levels of the 1960-1979 reference period.
1.4 Anthropogenic impacts on the stock
Anthropogenic m ortality m ay be inflicted on eel by fisheries (including w here catches
supply aquaculture for consum ption), hydropow er turbines and pum ps, pollution and
indirectly by other forms of habitat m odification and obstacles to migration.
Fisheries exploit the phase recruiting to continental waters (glass eel), the immature
grow th phase (yellow eel) and the m aturing phase (silver eel). Fisheries are prosecuted
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by registered and non-registered vessels, or fisheries not linked to vessels, such as fixed
traps, fixed net gears, m obile (bank-based) net gears, and rod and line. The exploited
life stage and the gear types em ployed vary betw een local habitat, river, country and
intem ational regions.
1.5 The management framework of eel
1.5.1 EU and Member State waters
G iven that the European eel is a panm ictic stock w ith w idespread distribution, the
stock, fisheries and other anthropogenic impacts, w ithin EU and M ember State waters,
are currently m anaged in accordance w ith the European Eel Regulation EC N o
1100/2007, "establishing measures for the recovery o f the stock o f European eel" (European
Council, 2007). This regulation sets a framework for the protection and sustainable use
of the stock of European eel of the species Anguilla anguilla in Com m unity Waters, in
coastal lagoons, in estuaries, and in rivers and com m unicating inland waters of M em-
ber States that flow into the seas in ICES Areas III, IV, VI, VII, VIII, IX or into the Med-
iterranean Sea.
The Regulation sets the national m anagem ent objectives for Eel M anagem ent Plans
(EMPs) (Article 2.4) to "reduce anthropogenic mortalities so as to perm it w ith high
probability the escapem ent to the sea of at least 40% of the silver eel biom ass relative
to the best estim ate of escapem ent that w ould have existed if no anthropogenic influ-
ences had im pacted the stock. The EMP shall be prepared w ith the purpose of achiev-
ing this objective in the long term." Each EMP constitutes a m anagem ent plan adopted
at national level w ithin the framework of a Com m unity conservation m easure as re-
ferred to in Article 24(l)(v) of Council Regulation (EC) N o 1198/2006 of 27 July 2006 on
the European Fisheries Fund, thereby m eaning that the im plem entation of m anage-
m ent m easures for an EMP qualifies, in principal, for funding support from the EFF.
The Regulation sets reporting requirem ents (Article 9) such that M ember States m ust
report on the m onitoring, effectiveness and outcom es of EMPs, including the propor-
tion of silver eel b iom ass that escapes to the sea to spawn, or leaves the national terri-
tory, relative to the target level of escapement; the level of fishing effort that catches eel
each year; the level of mortality factors outside the fishery; and the am ount of eel less
than 12 cm in length caught and the proportions utilized for different purposes. These
reporting requirem ents w ere further developed by the Com m ission in 2011/2012 and
published as guidance for the production of the 2012 reports. This guidance adds the
requirem ent to report fishing catches (as w ell as effort), and provides explanations of
the various biom ass, m ortality rates and stocking metrics, as follows:
• Silver eel production (biomass):
• Bo The am ount of silver eel biom ass that w ou ld have existed
if no anthropogenic influences had im pacted the stock;
• Bcurrent The am ount of silver eel biom ass that currently escapes to
the sea to spawn;
• Bbest The am ount of silver eel biom ass that w ou ld have existed
if no anthropogenic influences had im pacted the current stock, included
re-stocking practices, hence only natural m ortality operating on stock.
• A nthropogenic mortality (impacts):
• ZF The fishing mortality rate, sum m ed over the age-groups in
the stock, and the reduction effected;
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• EH The anthropogenic mortality rate outside the fishery,
sum m ed over the age-groups in the stock, and the reduction effected
(e.g. turbines, parasites, viruses, contaminants, predators, etc);
• EA The sum of anthropogenic m ortalities, i.e. L A = EF + EH.
It refers to mortalities sum m ed over the age-groups in the stock.
• Stocking requirements:
• R(s) The am ount of eel (<20 cm) restocked into national waters
annually. The source of these eel should also be reported, at least to orig-
inating M ember State, to ensure full accounting of catch vs stocked (i.e.
avoid 'double banking'). N ote that R(s) for stocking is a n ew sym bol
devised by the W orkshop to differentiate from "R" w hich is usually con-
sidered to represent Recruitment of eel to continental waters.
In July 2012, Member States first reported on the actions taken, the reduction in anthro-
p ogenic m ortalities achieved, and the state of their stock relative to their targets. In
M ay 2013, ICES evaluated these progress reports in terms of the technical im plem en-
tation of actions (ICES 2013a). In October 2014, the EU Com m ission reported to the
European Parliament and the Council w ith a statistical and scientific evaluation of the
outcom e of the im plem entation of the Eel M anagem ent Plans. In 2015 and 2018, EU
M em ber States w ill again report on progress w ith im plem enting their EMPs.
1.5.2 Non-EU states
The Eel R egulation 1100/2007 only applies to EC Member States but the eel distribution
extends m uch further than this. The w hole-stock (intem ational) assessm ent (see Sec-
tion 1.5) requires data and information from both EU and non-EU countries producing
eels. Som e non-EU countries provide such data to the WGEEL and m ore countries are
being supported to achieve this through efforts of the General Fisheries Com m ission
of the M editerranean (GFCM).
The GFCM is currently undertaking a series of case studies to develop regional m ulti-
annual m anagem ent plans for shared stocks. Priority fisheries include the case of Eu-
ropean eel w hich is shared by all countries in the region. A technical docum ent w as
produced in 2014, w ith the assistance of national focal points on eel, w hich gathers the
state of the art in terms of data availability, m anagem ent m easures in force, fishery
description, biological parameters and stock status (where available). GFCM Member
countries have requested the GFCM Secretariat to produce guidelines to im prove the
assessm ent and m anagem ent of this important fishery. The participation of GFCM in
the Joint EIFAAC/ICES/GFCM WGEEL has contributed to strengthen collaboration
w ith ICES and EIFAAC experts w hose availability and w illingness to cooperate is very
m uch appreciated. The next m eeting of the GFCM Scientific A dvisory Com m ittee
(SAC) in March 2015 w ill discuss and eventually approve the plan of action outlined
during the 2014 WGEEL m eeting. The inclusion of this action plan for eel in the work
program of SAC for the next year w ill allow the search for supporting funds, if possible
w ith the assistance of EU.
1.5.3 Other international legislative drivers
The European eel w as listed in A ppendix II of the Convention on International Trade
in Endangered Species (CITES) in 2007, although it did not com e into force until March
2009. Since then, any intem ational trade in this species needs to be accom panied by a
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permit. A ll trade into and out of the EU is banned, but trade from non-EU range States
to non-EU countries is still permitted.
The International U nion for the Conservation of Nature (IUCN) has assessed the Eu-
ropean eel as 'critically endangered' on its Red List, in 2009 and again in 2014 although
recognising th a t" if the recently observed increase in recruitment continues, m anage-
m ent actions relating to anthropogenic threats prove effective, and/or there are positive
effects of natural influences on the various life stages of this species, a listing of Endan-
gered w ou ld be achievable" and therefore "strongly recom m end an update of the sta-
tus in five years".
M ost recently, the European eel has been added to A ppendix II of the Convention on
M igratory Species (CMS), w hereby Parties (covering alm ost the entire distribution of
European eel) to the Convention call for cooperative conservation actions to be devel-
oped am ong Range States.
1.6 Assessments to meet management needs
The EC obtains recurring scientific advice from ICES on the state of the eel stock and
the m anagem ent of the fisheries and other anthropogenic factors that impact it, as spec-
ified in the M em orandum of Understanding betw een EU and ICES. In support of this
advice, ICES is asked to provide the EU w ith estim ates of catches, fishing mortality,
recruitm ent and spaw ning stock, relevant reference points for m anagement, and infor-
m ation about the level of confidence in parameters underlying the scientific advice and
the origins and causes of the main uncertainties in the inform ation available (e.g. data
quality, data availability, gaps in m ethodology and know ledge). The EU is required to
arrange - through M ember States or directly - for any data collected both through the
Data Collection Framework (DCF) and legally disposable for scientific purposes to be
available to ICES.
ICES requests inform ation from national representatives to the joint EI-
FAAC/ICES/GFCM W orking Group on Eel (WGEEL) on the status of national eel pro-
duction each year, and ICES provides assessm ents at regional and w hole-stock levels.
C om plexities of the eel life history across the continental range of production, and lim -
ited k now ledge and data of production and impacts for large parts o f this distribution,
m ake it very difficult to apply a classical fisheries stock assessm ent based on the prin-
ciples of a stock-recruitm ent relationship (but see below ) and the assum ption that mor-
tality due to fishing far outw eighs other anthropogenic and natural mortalities.
Therefore, the ICES advice has, to date, been based on a tim e-series of recruitment in-
dices from fishery-dependent and -independent sources, com paring index levels in re-
cent years w ith those of a historic reference period and expressing the former as a
proportion of the latter.
Looking to the future, the regular provision by EU M ember States of estim ates of es-
capem ent biom ass and rates of mortality associated w ith anthropogenic im pacts as
part of the process of EMP Review, and similar but voluntary reporting by non-EU
coim tries producing eels, provides a m eans of international eel assessm ent.
The status of eel production in EMUs is assessed by national or sub-national fishery/en-
vironm ent m anagem ent agencies to m eet the terms of the national EMPs. The setting
for data collection varies considerably betw een countries, depending on the m anage-
m ent actions taken, the presence or absence of various anthropogenic im pacts, but also
on the type of assessm ent procedure applied. A dditionally, the assessm ent fram ework
varies from area to area, even w ithin a single country. Accordingly, a range o f m ethods
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m ay be em ployed to establish silver eel escapem ent lim its (40% of Bo) and m anagem ent
targets for individual rivers, EMUs and nations, and for assessing com pliance of cur-
rent escapem ent (Bcun-ent) w ith these lim its/targets. These m ethods require data on var-
iou s com binations of catch, recruitment indices, length/age structure, recruitment,
abundance (as biom ass and/or density), length/age structure, m aturity ogives, to esti-
m ate silver eel biom ass, and fishing and other anthropogenic m ortality rates.
The ICES Study Group on Intemational Post-Evaluation of Eel (SGIPEE) (ICES 201 Ob,
201 lb ) and WGEEL (ICES 2010a, 201 lb ) derived a framework for post hoc sum m ing up
of EMU / national 'stock indicators' of silver eel escapem ent biom ass and anthropo-
genic m ortality rates. This approach w as first applied by WGEEL in 2013 based on the
national stock indicators reported by EU Member States in 2012 in their first EMP Pro-
gress Reports. H ow ever, not all countries w ith EMPs reported. The approach w ill be
applied again in 2015, after the Member States provide their second EMP progress re-
ports, and hopefu lly w ith the addition of data from non-EU countries as w ell to in-
crease the spatial coverage of data for this assessm ent approach.
The w orking group is also developing the application of the 'traditional' Stock-Recm it-
m ent (S-R) relationship and associated reference points, as the S-R relationship re-
m ains a key function for the study of population dynam ics in the perspective of
m anagem ent advice. The ultim ate objective is a m ethod to derive biological reference
points adapted specifically to the European eel.
The actual spaw ning-stock biom ass (in the Sargasso Sea) has never been quantified, so
the best available proxy tim e-series is the quantity of silver eel that leaves continental
w aters to m igrate to the spaw ning grounds; hereafter termed the 'escapem ent bio-
m ass'. A s escapem ent biom ass has only been reported by EU M em ber States once, in
2012, and not yet reported by non-EU states, WGEEL has attem pted to derive historic
tim e-series of stock-w ide escapem ent from landing statistics. In the absence of stock-
w id e quantification of recruitment, the working group has applied an index of glass
eel recruitment to continental waters, lagged by tw o years to account for the presum ed
transit tim e of eel Tarvae' betw een spaw ning area and continental waters. The classical
Ricker and Beverton and H olt approaches to describe S-R relationships do not provide
a good fit to these eel 'data'. The working group continues to explore w ays to describe
these data, m ost recently using data-driven General A dditive M odel (GAM) approach,
and fit eel-specific reference points.
1.7 Conclusion
This report of the joint EIFAAC/ICES/GFCM W orking Group on Eel is a further step in
an ongoing process of docum enting the stock of the European eel, and associated fish-
eries and other anthropogenic impacts, and developing m ethodology for giv ing scien-
tific advice on m anagem ent to effect a recovery in the intem ational, panm ictic stock.
The M oU betw een the EU and ICES requires an assessm ent of the status of the eel stock
every year. A s recruitment and landings data are reported to the w orking group every
year, these form the basis of the annual assessm ent. N ew national b iom ass and anthro-
pogenic mortality stock indicators are scheduled to be available in 2015,2018 and every
six years thereafter.
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2 ToR a): Assess the latest trends in recruitment, stock and f isher-
ies, including effort, and other anthropogenic factors indicative
of the status of the stock, and report on the state o f the inter-
national stock and its mortality
The purpose of this chapter is to provide the information for the intem ational stock
assessm ent in support of the ICES Advice. Sections 2.1 and 2.2 provide updates on
trends in recruitment indices, and yellow and silver eel abundance information, re-
spectively. Section 2.1 includes an exam ination of m ethods to test for significant
changes in these trends. Sections 2.3, 2.4 and 2.5 provide inform ation on commercial
landings, recreational fisheries, and first attempts by the working group to sum m arise
inform ation on m isreporting of catches and estim ates of illegal catches. Section 2.6 up-
dates inform ation on eel stocking and 2.7 on eel aquaculture. The chapter concludes
w ith a first attempt to collate information on the potential environm ental drivers on
the stock, fo llow ed by the tables for the chapter.
2.1 Recruitment trends
2.1.1 Time-series available
The recruitment tim e-series data are derived from fishery-dependent sources (i.e. catch
records) and also from fishery-independent surveys across m uch of the geographic
range of European eel (Figure 2.1). The stages are categorized as glass eel, yotm g sm all
eel and larger yellow eel recruiting to continental habitats. The WGEEL is currently
also building up data from yellow eel series, but these are related to standing stock.
The yellow eel series used there all com e from trapping ladders.
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.
i í
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Figure 2.1. Location of the eel recruitment monitoring sites in Europe, circle = glass eel (white), glass
eel and young ye llow eels (blue), yellow diamond = yellow eel series. The lines show the different
Eel M anagem ent Units in Europe.
The glass eel recruitment series have also been classified according to tw o areas: N orth
Sea and Elsewhere Europe, as it cannot be ruled out that the recruitment to the tw o
areas have different trends (ICES, 2010b). The Baltic area does not contain any pure
glass eel series. The yellow eel recruitment series are either com prised of a m ixture of
glass eel and you ng yellow eel, or as in the Baltic, of young yellow eel only.
The WGEEL has collated information on recruitment in 52 time-series. The series code,
nam e, com m ents about the data collection m ethod, the intem ational region, whether
they are part of the North Sea or Elsewhere series, the country, EMU, river, location,
sam pling type, data units, life stages sam pled, first and last year of data, w hether they
are active in the year of assessm ent, and whether or not there are m issing data in the
series, are all fully described in electronic Table E2.1 available on the w orking group
w eb page.
Som e series date back as far as 1920 (glass eel, Loire, France) and even to the beginrdng
of 20th century (yellow eel, Gota A lv, Sweden). The status o f the series can be described
as follow ing:
• 38 tim e-series w ere updated to 2014 (29 for glass eel or glass + yellow , and
nine for yellow eel (Table 2.1).
• three series (one for glass eel and tw o for yellow eel) have been updated to
2013 only (Table 2.2).
• Som e of the series have been stopped, as the consequence of a lack of recruits
in the case of the fishery-based surveys (Ems in Germany, 2001; Vidaa in
Jo in t E IF A A C /IC E S /G FC M WCEEL REPORT 2 0 1 4
Denmark, 1990), as a consequence of a lack of financial support (the Tiber in
Italy, 2006), or from 2008 to 2011, as a consequence of the introduction of a
n ew quota system and incom plete geographical reporting for the five fish-
ery based French series (Table 2.3).
The num ber of available series has declined from a peak of 33 series in 2008 for the
glass eel, and glass eel and young yellow eel series. The m axim um num ber of yellow
eel series increased to 12 in 2009 (Figure 2.2). Before 1960, the num ber of glass eel or
glass eel + yellow eel series, w hich w ill be used to build the WGEEL recruitment index
for glass eel, is quite small, w ith six series before 1959 (Figure 2.2). Those are D en Oever
(scientific survey), the Loire (total catch), the Ems (mixture of catch and trap and
transport), the Gironde (total catch), the Albufera de Valencia in the Mediterranean,
and the Adour, w hich dates as far back as 1928, and is based on cpue. For the latter
how ever, on ly the years 1928 to 1931 are available and the series on ly resum es in 1966.
year
Figure 2.2. Trend in num ber of series giving a report any specific year, data split per life stage.
2 .1.2 Simple geometric means
The calculation of the geom etric m ean of all series show that the recruitment is increas-
ing in 2014 from a m inim um in 2009 (Figures 2.3 and 2.4). Figure 2.3, although con-
sistent w ith the trend provided by WGEEL since 2002, m ight be biased by the loss of
m ost Bay of Biscay series from 2008 to 2012. The scaling is perform ed on the 1979-1994
average of each series, and seven series w ithout data during that period are excluded
J o in t E IF A A C /IC E S /G FC M WCEEL REPORT 2 0 1 4
from the analysis1. This scaling is sim ply to standardise the series so that they can all
be presented on the sam e y-axis, and this period of years is not presented as a reference
tim e period.
1000%-
<D
cu>
§
T-I
or̂ -
O J
T3O
rö
100% -
!0%-
1%-
Figure 2.3. Tim e-series o f glass eel and yellow eel recruitment in European rivers w ith dataseries
having data for the 1979-1994 period (45 sites). Each series has been scaled to its 1979-1994 average,
for illustrative purposes. Note the logarithmic scale on the y-axis. The m ean values and their boot-
strap confidence interval (95%) are represented as black dots and bars. Geometric means are pre-
sented in red. The shaded values correspond to pre-1960 where the num ber of glass eel dataseries
available is low er and w ill not be ind uded in the calculation of the reference period.
W hen looking at the separate trends for both glass eel and yellow eel series, as intro-
duced by the WGEEL in 2006 (ICES, 2006), the increase seem s m ostly due to glass eel
series w hich sh ow a positive trend from 2011 w hile yellow eel series show a w ider
variation, and a large surge in 2014, that remains to be confirm ed. N ote that no lag w as
added to the yellow eel series but that the age of yellow eels m ight range from one to
several years old (Figure 2.4).
Follow ing the recom m endation of RGEEL (ICES, 2013b: M inutes of the Technical Re-
view ), in 2014 the sam e figure is built from all series available, and a n ew scaling based
on the 2000-2010 (included) w as performed. This leaves out tw o series: Vida and YFSl.
The scale from this graph show s an increase from the current level (1) to around a 100
1 'the series left out are : Bres, Fre, Inag, Klit, Maig, Nors, Sle.
Jo in t E IF A A C /IC E S /G FC M WGEEL REPORT 2 0 1 4
tim es that value in the 1970s, and m ore than 100 tim es that level before the 1970s for
the longest series (Figure 2.5).
1950 1975 2000
year
Figure 2.4. T im e-series of glass eel and yellow eel recruitment in Europe w ith 45 series out of 52
available to the working group. Each series has been scaled to its 1979-1994 average. The mean
values of com bined ye llow and glass eel series and their bootstrap confidence interval (95%) are
represented as black dots and bars2. The brown line represents the m ean value for ye llow eel, the
blue line represents the mean value for glass eel series. The range of the series is indicated by a
grey shade. The tim e period 1900-1950 that w ill not be used to calculate the reference is shaded in
w hite. N ote that individual series from Figure 4.3 were rem oved for clarity. Note also the logarith-
mic scale on the y-axis.
2 This is the sam e as in Figure 4.3.
Joint EIFAAC/ICES/GFCM WGEEL REPORT 2014
1000
100
Figure 2.5. Time-series of glass eel and yellow eel recruitment in Europe. Same graph as Figure 4.4
but the series have been scaled to their 2000-2009 average (blue box). Two series3 have been ex-
cluded from the initial number (52) that did not have data in the period 2000-2009. The mean values
of combined yellow and glass eel series and their bootstrap confidence interval (95%) are repre-
sented as black dots and bars. The brown line represents the mean value for yellow eel, the blue
line represents the mean value for glass eel series. The range of the series is indicated by a grey
shade. Note the logarithmic scale on the y-axis.
2 .1 .3 GLM based trend
The WGEEL recruitment index is a reconstructed prediction using a simple GLM (Gen-
eralised Linear Model): glass eel ~ year: area + site, where glass eel is individual glass eel
series, site is the site monitored for recruitment and area is either the North Sea or
Elsewhere Europe. The GLM uses a gamma distribution and a log link. The dataseries
comprising only glass eel, or a mixture of glass eel and what is mostly young of the
year eel are grouped and later labelled glass eel series.
In the case of yellow eel series, only one estimate is provided: yellow eel ~ year + site.
The trend is reconstructed using the predictions from 1960 for 40 glass eel series and
for 12 yellow eel series. This analysis rebuilds all the series by extrapolating the missing
values. The series are then averaged. Some zero values have been excluded from the
GLM analysis: 12 for the glass eel model and one for the yellow eel model (see Table
E2-1V
3 Vidaa and Y FSl.
Joint EIFAAC/ICES/CFCM WCEEL REPORT 2014
The reference period for pre-1980 recruitment level is 1960-1979, as four series availa-
ble from 1950 to 1960 are excluded because they were based on total catch of commer-
cial glass eel, which are known to have been affected by changes in fishing practises,
and the progressive shift from hand nets to push net fisheries from 1940 to 1960 (Briand
et al, 2008: see paragraph 24.1.1). After 1960, the number of available series increases
rapidly (Figure 2.2). Though no such biases are known for the yellow series recruitment
series, the same reference period has been chosen, to provide consistent results.
After high levels in the late 1970s, there has been a rapid decrease in the glass eel re-
cruitment trends (Figures 2.6 and 2.7; note the logarithmic scales).
year
Figure 2.6. WGEEL recruitment index: mean of estimated (GLM) glass eel recruitment for the con-
tinental North Sea and elsewhere in Europe updated to 2014. The GLM (recruit = area: year + site)
was fitted on 40 series comprising either pure glass eel or a mixture of glass eels and yellow eels
and scaled to the 1960-1979 average. No series are available for glass eel in the Baltic area. Note the
logarithmic scale on the y-axis.
Joint EIFAAC/ICES/CFCM WCEEL REPORT 2014
year
Figure 2.7. Mean of estimated (GLM) yellow eel recruitment and smoothed trends for Europe up-
dated to 2014. The GLM (recruit ~ year + site) was fitted to 12 yellow eel series and scaled to the
1960-1979 average. Note the logarithmic scale on the y-axis.
In conclusion, the WGEEL recruitment index is currently low but increasing for both
regional glass eel series: the current level with respect to 1960-1979 averages is 3.7%
for the North Sea and 12.2% elsewhere in the distribution area (Tables 2.4 and 2.5). For
yellow eel recruitment series, the recruitment has risen to 36% of the 1960-1979 period.
2 .1 .4 Are there s ignificant changes in trend?
Given these recent increases in recruitment indices, the w orking group examined three
statistical methods to test whether these were significant changes to the trends (i.e.
break points, uptums). The objective of the first two methods, CUSUM and segmented
regression, w as to identify breakpoints in the whole time-series. The third method, the
Bayesian approach, w as used to detect a breakpoint in the last ten years and to simulate
future recruitment to explore a trajectory of recruitment recovery
2.1.4.1 CUSUM
Trends were calculated using the cumulative sums method (CUSUM (W oodward and
Goldsmith 1964; Ibanez et al., 1993). A cumulative sum represents the m nning total of
the deviations of the first observation from a mean based on the same interval. In gen-
eral, the CUSUM approach to detect change points performs well, has been well-doc-
umented and is relatively easy to implement (Breaker, 2007). Breakpoints that m ay not
Joint EIFAAC/ICES/GFCM WGEEL REPORT 2014
be possible to detect in the original data often become easier to detect when the
CUSUM is plotted. For a time-series with data sampled for each year (t), a reference
value k is chosen (here w e chose the standardized mean logarithmic of the glass and
yellow eel time-series).
After subtracting k from each datapoint, the residuals are added successively to calcu-
late the cum ulative sums (CSt):
t
CSt = k)
i= 1
The successive values of CSt are plotted versus time (years) to produce the so-called
CUSUM chart. The local mean between two breaking points is the slope of the cumu-
lative sum curve between the two points, plus the reference value k. Changes in the
average level of the process are reflected as changes in the slope of the CUSUM plot.
For successive values equal to k, the slope will be horizontal; for successive values
low er than k, the slope w ill be negative and proportional; and for successive values
higher than k, the slope w ill be positive and proportional. The year of the change in the
slope of the CUSUM is the year that a shift occurs. Breakpoints were visually identified
on the CUSUM trajectories as abrupt changes (as opposed to a gradual change) in di-
rection of slope.
CUSUM were first calculated on the whole time period (from 1960 to 2014) to define
the main breakpoints (Table 2.6). Since two main periods were defined, CUSUM were
then calculated on the second period, from 1980 onwards, to focus on the decline (Table
2.6).
A ll of the CUSUM calculated showed smooth trajectories with few breakpoints (Fig-
ures 2.8 and 2.9). This was due to the low amplitude in inter-annual fluctuations com-
pared to the overall change around the total average of the time-series.
Figure 2.8. CUSUM calculated on the original glass eel time-series ('North Sea' and 'Elsewhere Eu-
rope'), with CUSUM values plotted against the y-axis and year shown on the x-axis.
Joint EIFAAC/ICES/GFCM WCEEL REPORT 2014
20
❖ ♦
15
& ❖ ♦ ♦ ♦
♦ ♦ *
♦ ♦ □ □ □ □ ♦
♦ n n D D D n ♦
d B d d G q
□ □ ♦ ♦Incusumnorth
♦ □
□
□ Incusum elsewhere
Figure 2.9. CUSUMS calculated on the natural logarithm of glass eel time-series ('North Sea' and
'Elsewhere Europe'), from 1980 to 2014, with CUSUM values plotted against the y-axis and year
shown on the x-axis.
The blue lines on Figures 2.10 and 2.11 show two distinct periods with breakpoints in
1980 for the 'North Sea' time-series and two years later for the 'Elsewhere Europe' time-
series. The slopes of the CUSUM become negative after these breakpoints. W hile the
time trend for 'North Sea' time-series only shows one breakpoint, the trend for 'Else-
where Europe' time-series displays three breakpoints with a relatively stable period
between 1982 and 1990 (Figure 2.11). CUSUM calculated over the later period (starting
in 1980) show two breakpoints for the 'North Sea' time-series and one for the 'Else-
where Europe' time-series (Figures 2.10 and 2.11).
Joint EIFAAC/ICES/GFCM WGEEL REPORT 2014
0
-5
-10
-15
-20
-25
-30
-35
-40
>north
•e lse w h e re
11 m i m
0 m o
l£> u d CD
01 oi cn
T—I tH T—i
T T T T T T T T !
O l ( N 1/1
co n
0 ) 0 1 0 1
T— I rH c— 1
T T T T T T r T T T T T T
T o
oo
CT1
! 1 í i I I I l " T iT "T i T i l ! I l " l I' i I' l i !
m i í O l r M l / I C O H T
C T I C T I C T l O O O r H t H
C T I C T I C T I O O O O O
H r l H N i N N f M f ' l
Figure 2.10. Step diagram representing the slopes calculated on the logarithm of the different time-
series for 'North Sea' and 'Elsewhere Europe' time-series, (see Table 2.6 for details on k), with slope
values plotted against the y-axis and year shown on the x-axis.
Figure 2.11. Step diagram representing the slopes calculated on the logarithm of the different time-
series, for 'North Sea' and 'Elsewhere Europe' time-series, after the decline in recruitment (see Ta-
ble 2.6 for details on k), with slope values plotted against the y-axis and year shown on the x-axis.
2.1 .4 .2 Segmented regression
The R package ''segmented'' was used to perform the segmented regression (Muggeo,
2003; 2008). This algorithm estimates the positions of a given number of breakpoints,
starting from a user-defined initial condition (i.e. breakpoints locations), by iteratively
fitting linear segmented models with the following predictor:
Joint EIFAAC/ICES/GFCM WCEEL REPORT 2014
/ ? ! * £ + /?2 O i - V O +
(Zi - V0+ = (Z i - V») X I ( Z i > xþ)
where /?x is the left slope, zL is the independent variable, /?2 is the difference-in-slope
before and after a breakpoint, iþ is the breakpoint and /(•) is the indicator function,
equal to one when the argument is true, otherwise it is zero.
This m odel is strongly affected by the initial conditions for the breakpoints locations
and it is not intended to determine the number of breakpoints in a time-series. There-
fore, this algorithm is nested into a double loop: the first to compare the null model
(i.e. the linear regression w ith no breakpoints) and different segmented models with j
breakpoints (j = 1...4) and the second to compare several initial conditions, sampled
random ly from all the combinations of j possible breakpoints locations (here the sub-
sample is the 10% of all possible combinations). The Bayesian Information Criteria
(BIC) is used to determine the performance of each resulting model. BIC was preferred
to the Akaike Information Criteria (AIC) as it has a higher penalty on the number of
parameters. The model associated with the lowest value of BIC is selected.
This method has been applied to the three time-series: the logarithm of glass eels re-
cruiting in the 'North Sea' area (north), the logarithm of glass eels recruiting in the
'Elsewhere Europe' area (elsewhere) and the logarithm of yellow eels (yellow). The
results are summarized in Table 2.7 and Figures 2.12 to 2.14.
Joint EIFAAC/ICES/CFCM WCEEL REPORT 2014
a)
year
b)
year
Fignre 2.12. Segmented regression performed on the log of glass eel recruitment at the 'North Sea'
(a) and on the log of glass eel recruitment 'EIsewhere Europe' time-series (b).
Joint EIFAAC/ICES/GFCM WGEEL REPORT 2014
The calibration of the segmented regression model on the 'North Sea' time-series se-
lected the model with four breakpoints (1981,1984,1996 and 2012) (Figure 2.12a). The
1981, 1984 and 1996 are breakpoints between regressions with negative slope, while
the 2012 breakpoint identifies a change in the sign of the slope, from negative to posi-
tive (Figure 2.13).
The m odel selected in the 'Elsewhere Europe' time-series identified three breakpoints
(1972, 1978 and 2011), subdividing the time-series into four different periods with dif-
ferent slopes (Figure 2.12b) that change sign at each breakpoint (Figure 2.13).
- l
I B l f i N N N N i V O O J C X
w o i c r i c n s i o i í j i o i a i i í p
0 IM <1 U5 03
01 <?. ( íi cr, cn
c". c . er. c ó">
Figure 2.13. Step diagram representing the slopes calculated using the segmented regression model
on the two recruitment time-series ('North Sea' and 'Elsewhere Europe').
No breakpoints were identified for the yellow eel time-series and the null model was
selected (Figure 2.14). This regression showed a significant (p<0.001) negative slope
(/?=-0.049).
Joint EIFAAC/ICES/GFCM WGEEL REPORT 2014
year
Figure 2.14. Segmented regression performed on the log of the yellow eel time-series.
The significance of using 2011 as a breakpoint in the recruitment time-series w as tested
using the model developed by SGIPEE (ICES, 2011b):
R~year + pmax(year, 2011)
Where pmax is the maximum between the year and 2011. This model was calibrated
on both recruitment time-series. An Analysis of Variance (AN O VA) revealed that the
term pmax(.) was significantly different from zero (p<0.001 for both 'North Sea' and
'Elsewhere Europe').
2.1 .4 .3 Bayesian approach
The Bayesian Eel Recruitment Trend (BERT) model is based on exponential trends (
d £
and 2) and auto-correlated perturbations ‘ . This type of perturbation structure sim-
ulates whether recruitment above the central trend in a particular year is more often
follow ed by recruitment above or below the trend. This is the usual w ay to incorporate
environmental fluctuations (e.g. climate, oceanic conditions) which are generally auto-
correlated in time. This approach w as adapted from that developed to set up the glass
eel quota in France (Beaulaton et al., in press.)
The possibility of a single regime shift w as introduced with an indicator random vari-
able I to test the credibility of this break point (Kuo and Mallick, 1998). The posterior
distribution of ̂ can be interpreted as the probability that a shift in the trend should
t
be included in the model. The shift occurs at Jt which was chosen between 2003 and
2014, according to categorical distribution.
Joint EIFAAC/ICES/GFCM WGEEL REPORT 2014
The model is writte as:
í t f t, V ‘+" for t< X íUf,
' {/? ,,• for
e t = P ' e , - \ + r l ,
iid
rjt □ Norm(0,o)
I □ Bernoulli(p,)
W D dcat(rep(0.1,10))
R t a
where ' the recruitment index the year ^, shiJi the year of the regime shift, 1 the
slope before the regime shift, + the slope after the regime shift, I the indicator
8
random variable to select or not the regime shift, ' the auto-correlated perturbations,
P the auto correlation coefficient and the independent and identically distributed
residuals of mean 0 and standard deviation ® . I is drawn from a Bem oulli distribu-
Ð t
tion of probability 1 . shî is drawn from a categorical distribution w ith a 10 values
probability vector of 0.1.
The a priori distributions are chosen as least informative.
pU d u n if( - 1 ,1 )
<j U d g a m m a (0 .0 1,0 .0 1)
ax,a 2 □ d n orm (0 ,0 .0 1)
lo g ( i? 0)Q d n o rm (0 ,0 .0 l) + dnorm(0, 1)
p j □ d b eta(0 .5 ,0 .5 )
where dunif, dgamma, dnorm and dbata are the density fimctions respectively for uni-
form, gamma normal and beta distributions in jags.
Bayesian inferences were performed by M arkov Chain Monte Carlo from the R pack-
age 'rjags' (Plummer, 2013).
The recruitment time-series 'Elsewhere Europe' and 'North Sea' over the period 1980
to 2013 were used to target the analysis on breakpoints in the recent period. The refer-
ence recruitment corresponds to the average recruitment during the reference period
1960-1973 (Chapter 2.1). This reference recruitment was used as a proxy for the stock
recovery.
For the 'Elsewhere Europe' series, the BERT model gives a credibility of 35.1% for a
trend shift between 2004 and 2013. The distribution of years with breakpoints is pre-
sented in Figure 2.15. Note that the special case w ith P and ŝhP js the
equivalent Bayesian approach of the test proposed by SGIPEE (ICES, 2011b). In that
case, the credibility of a trend shift in 2011 is 72.3%. This result shows the importance
of taking account of autocorrelation in the analysis for such trends.
Joint EIFAAC/ICES/GFCM WGEEL REPORT 2014
For the 'North Sea' serieS/ with the full model, the credibility of a regime shift increased
to 73.7% w ith the more likely breakpoint in 2013 (Figure 2.16).
co
ö
.Q
Ö
<D
o
CNI
Ö
O
Ö
2004 2005 2006 2007 2008 2009 2010 2011 2012 2013
year of trend shift
Figure 2.15. Credibility of (equivalent in classical statistics to "the probability to have") a trend
shift according to year for the "Elsewhere Europe" time-series.
ö
oo
ö
TD
<D
O
Ö
2004 2005 2006 2007 2008 2009 2010 2011 2012 2013
year oftrend shift
Figure 2.16. Credibility of (equivalent in classical statistics to "the probability to have") a trend
shift according to year for the "North Sea" series.
Joint EIFAAC/ICES/GFCM WCEEL REPORT 2014
2.1 .4 .4 Conclusion on the break points detected
A ll methods applied on the complete time-series (1960-2014) detected a breakpoint
arotmd 1980, indicating a change in the slope sign from positive to negative, except the
segmented regression on the glass eel recruitment in the 'North Sea' for w hich the
breakpoint corresponded to an increased negative slope. This result confirms the shift
in trend observed in the recruitment series during the 1980s and the consequent decline
of the recruitment until the most recent years.
The m odels detected several other breakpoints that occurred before 2010. These break-
points were not related to a change in the trend but to steeper declines in recruitment.
Most m odels (except the CUSUM applied to the glass eel recruitment in the 'Elsewhere
Europe' series) detected a breakpoint in 2011-2012 with a change of slope sign. The
significance of this breakpoint was confirmed by the A N O V A and by the Bayesian ap-
proach, but it was not possible to determine whether this breakpoint can be considered
a trend shift yet, as this short positive trend could be the result of the time-series auto-
correlation. Moreover, there is no evidence of a trend change in the yellow eel tim e-
series.
2.1 .4 .5 Evaluation of recruitment recovery based on trend analysis
This objective of this section is to determine whether or not trends in recruitment are
m oving towards recovery.
It is obvious that a decreasing trend in recruitment is not compatible w ith recovery of
the stock. A n increase in recruitment, confirmed by lagged increases of the standing
stock and silver eel escapement (when data w ill be available) is a necessary condition
to consider a recovery. H ow ever a short-term increase w ill not necessarily certify re-
covery. A t least, an increase over a period that corresponds to the average lifespan
should be recorded before giving a positive answer to recovery. Since life traits and
contributions to spaw ning stock vary geographically, the definition of the average
lifespan for eel is not simple and more work is needed.
Another w ay to evaluate whether the trend is m oving towards recovery is to calculate
how long it w ill take, given the present trend, to reach recruitment reference. In this
analysis the recruitment reference is defined as the average recruitment observed dur-
ing the period from 1960 to 1979.
The projections of the recruitment are presented in Figures 2.17 and 2.18 for 'Elsewhere
Europe' and 'North Sea' respectively. Since a trend shift is considered in only 35.1% of
the cases for the 'Elsewhere Europe' series, the trend of recruitment is predicted to
slightly decrease in the next years and the credibility (akin to statistical 'probability')
to be above the reference recruitment does not exceed 35% in the next 30 years (Figure
2.19). For the "North Sea" series, the trend is increasing (Figure 2.18) but w ill only
reach the reference recruitment in the long term (Figure 2.20).
Joint EIFAAC/ICES/CFCM WGEEL REPORT 2014
100 -
80 -
£ 60 -
20 -
/ \
* /
I I I I I
I___1__1__L_
1980 1990 2000 2010 2020 2030
season
Figure 2.17. Evolution from 1980 to 2014 (point) and projection from 2015 to 2030 (box and whiskers
plot) of recruitment for 'Elsewhere Europe' time-series. In the box and whiskers plot, the horizontal
segment in bold represents the median, the box represents the inter-quartile range, and the whisk-
ers represent the extreme values.
100 -
o
0
1980 1990 2000 2010 2020 2030
season
Figure 2.18. Evolution from 1980 to 2014 (point) and projection from 2015 to 2030 (box and whiskers
plot) of recruitment for the 'North Sea' time-series. In the box and whiskers plot, the horizontal
segment in bold represents the median, the box represents the inter-quartile range, and the whisk-
ers represent the extreme values.
Joint EIFAAC/ICES/CFCM WGEEL REPORT 2014
<D
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-i >
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ID <£> r- C D O o "t— <M CO <o < D r-- 00 O O -i—CM CO ■̂ro <Ðr— 00 C0 O CM c O <oT—T—T—t—T—CM CM CM CM CM CM CM CM CM CM CO co CO CO CO CO CO co co CO ■sj- ’CT-st 3 ■nTo o o O o O O O O O O O O O O o o o o o o O o o O o O o O o o
CM CM CM CM CM CM CM CM CM CM CM CM <MCM <MCM CM CM CM CMCM CMCM CM CM OMCM <M CM CM CM
year
Figure 2.19. Evolution of the credibility (equivalent in classical statistics to the 'probability') to be
above the reference recruitment (1960-1979 average recruitment) for the 'Elsewhere Europe' time-
series.
> ^o ©
jo E
Oj - t í
<D E
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o £4-J
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= cr
l o o
<d
£ o
b • -
1.0 n
0.8 -
0.6 -
0.4 -
0.2 -
0.0
m < x r - - - c D G ) O T - c M c o ' q - L r ; C D r - - c o c D O T - c \ j c o ' < T i o < o r - - c o c D O ' = - c \ i c O ' q - t nt — ■ t - ’t— C NCMCMCNCMCNCMCNCMCNJ COcOcOcOCOCOCOCOCOCO' s 3 ' ^ r ,s r ,< r ’T ,sr o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o
< M C M C M < M C M C M < M C M C M < M < M C M C M C M C M C M C M C M C M C M C M C M C M C M C M C M C M C M < M C M C M
year
Figure 2.20. Evolution of the credibility (equivalent in classical statistics to the 'probability7) to be
above the reference recruitment (1960-1979 average recruitment) for the 'North Sea' time-series.
Joint EIFAAC/ICES/CFCM WCEEL REPORT 2014
If a trend shift is set between 2004 and 2013 (i.e. assuming that the recent increases in
recruitment trend continue in the future), the credibility to exceed the reference recruit-
ment w ill be around 50% for 'Elsewhere Europe' in 2021, and for 'North Sea' in 2018,
and higher than 95% after 2045 for 'Elsewhere Europe' and after 2029 for 'North Sea'
recruitment (Figures 2.21 and 2.22).
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t — - t - t - t - t - C N C N C N C N C N C N C N C N C N C N C O C O c O c O C O c O c D C O C O C O ’,< r ' ^ r ' ^ r ' ^ r ,̂ r ' a -
o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o
C N C N C N C N C N C N C N C N C N C N C N C N C N C N C N C N C N C N C N C N C N C N C N C N C N C N C N C N C N C N C N
yea r
Figure 2.21. Evolution of the credibility (equivalent in classical statistics to the 'probabilityO to be
above the reference recruitment (1960-1979 average recruitment) for 'Elsewhere Europe' assuming
a trend shift set between 2004 and 2013.
Joint EIFAAC/ICES/GFCM WCEEL REPORT 2014 35
2 ^ § ®
xi E
03 -t±
C3 E
X3 O
o £
o
— c:
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b • -
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l O O N C O O O ’r - C N C O ' í l í X D N œ i a j O T - O ' J c O ^ l O C O N C O C D O T - C N c O ' v r i O
T - ' t - ' t - ' í - ' r - C N l C M C N C N C N C N C M C N C N C N O O C O C O C O C O C O c O c O C O c O ' s r ' q - ^ r ' q - ’s r ’sro o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o
CN CN CN CN CN CN CN CN CN CN CN CN CN CN CN CN CN CN CN CN CN CN CN CN CN CN CN CN CN CN CN
year
Figure 2.22. Evolution of the credibility (equivalent in classical statistics to the 'probabilityO to be
above the reference recruitment (1960-1979 average recruitment) for the 'North Sea' time-series as-
suming a trend shift set between 2004 and 2013.
In conclusion, the recent increases in recruitment time-series observed over the last
three years are not sufficient to be sure that the stock is m oving towards a recovery. If
these positive trends are confirmed and continue in the future without anv changes,
the recruitment might be expected to exceed the average 1960-1979 level around the
year 2030 in 'North Sea' and around the year 2045 in the 'Elsewhere Europe' times-
series. However, much im proved understanding of the functioning of the stock is re-
quired to make these trend analyses more robust.
2.1 .4 .6 Indicators that might trigger an update assessment
The w orking group considered the question posed by the ICES Generic ToRs, to define
or propose indicators that could be used to decide when an update assessment is re-
quired.
First and foremost, the working group reiterated that the '3B and I A ' stock indicators
should be estimated on an annual basis, and for each individual EMU, in order to up-
date the precautionary diagram approach. It is also essential that the glass eel and yel-
low eel data used to build recruitment and standing stock indices are collected
annually.
Regarding indicators to trigger an update assessment, the w orking group proposed
that a regime shift (change of sign in the trend) in recruitment time-series that was
detected w ith a high probability in the recent past might be a suitable trigger for an
update assessment. It that case, explanations of this regime shift should be explored.
Biological processes of the population dynamics and possibly the biological reference
points should be re-evaluated in consequence. Specific w ork is clearly required to de-
fine more precisely such quantitative indicators for an update assessment.
36 Joint EIFAAC/ICES/CFCM WGEEL REPORT 2014
2.2 T im e-series of yellow and silver eel abundance
In addition to the glass eel and (young) yellow eel recruitment series, yellow eel and
silver eel indices may be used in the future, though data are scarce, and m ay be uncer-
tain. Moreover, yellow and silver eel data may be more representative for the local area
where they are collected than for the global stock status because of the contrasts in
population dynamics and anthropogenic pressures at the distribution area scale.
Several Country Reports present information on long-term monitoring of yellow eel
abundance in various habitats, and these values have been updated in the WGEEL da-
tabase. Descriptions of the time-series are presented in Table 2.8. M ethodologies vary
from electrofishing and traps in rivers to beach-seines, fykenets and trawls in larger
waterbodies.
Information on long-term changes in yellow eel abundance in many cases is the only
w ay to assess the status of eel production in the absence of a significant fishery. A de-
velopm ent towards standardized methods w as suggested by W KESDCF to be in-
cluded in the revisions to the DCF (ICES 2012a).
2.3 Commerclal fishery landings trends
A t the present 2014 status, dataseries presented in this report contains information ob-
tained from the Country Reports, FAO capture database and by personal communica-
tion from WGEEL participants (Table E2-2).
A review of the catches and landing reports in the Country Reports showed a great
heterogeneity in landings data. Some countries make reference to an official system,
w hich then reports either total landings or landings split by Management Unit or Re-
gion. Some countries do not have any centralized system. Furthermore, some countries
have revised their dataseries, with extrapolations to the whole time-series, during the
process of compiling their Eel Management Plan (i.e. Poland, Portugal).
Landings data sourced from the FAO database are presented for countries not report-
ing to WGEEL. These are the Mediterranean countries: Egypt, Tunisia, Morocco, Tur-
key and Albania. The quality of some of the Mediterranean data should be reviewed,
as some figures seems to be urtreliable, e.g. 2012 Egypt data show large variations that
were of uncertain provenance given that there w as uncertainties about the presence of
a catch reporting system.
2.3.1.1 Collection of landings statistics by country (from CRs)
Changes in follow ing the descriptions of the landing statistics per country compared
to 2013 WGEEL are highlighted in italics.
Norway: Provided official landing statistics (Fisheries Directorate) calculated accord-
ing to the number of licences. Fishing for eel has been banned in N orw ay since January
1, 2010.
Sweden: Data on eel landings in coastal areas are based on sales notes sent to the ap-
propriate agency and in recent years also from a logbook system. There is a discrep-
ancy between the data derived from the traditional sales notes system and the more
recent logbook system. During the most recent years this difference was considerable,
e.g. in 2011 sales notes reported 238 tonnes, whereas the logbooks system registered
355 tonnes (all from the marine areas). Landings data from freshwaters come from a
Joint EIFAAC/ICES/CFCM WCEEL REPORT 2014
system w ith monthly or yearly journals. Fishing for eels in private waters w as not re-
ported before 2005. Data from logbooks and joum als are stored at the Swedish A gency
for Marine and Water Management.
Finland: The statistical data are collected by the FGFRI. Data from professional fishers
are collected by logbooks and recreational questionnaires. Data are available for 1976-
1988 and from 2003 onwards.
Estonia: The catch statistics are based on logbooks from inland and coastal fisheries.
Data are available for 1964 to 1992 (Lake Vörtsjárv) and from 1993 onwards for all ar-
eas.
Latvia: Eel landings are reported in monthly logbooks detailing date, number and type
of gear, and fishing time. Logbooks from coastal and inland fisheries were collected by
local Boards of M IW A and transmitted to BIOR for data summarization and storage.
Lithuania: Fisheries companies provide information according to their logbooks about
catch on a monthly basis to the authority issuing permits: a Regional environmental
protection department under the Ministry of Environment of the Republic of Lithuania
if a com pany is engaged in inland fisheries (including the Curonian Lagoon), or the
Fisheries Service of the Ministry of Agriculture of the Republic of Lithuania if a com-
pany is engaged in maritime fisheries. Data on recreational fisheries are collected using
questionnaires.
Poland: The (approximate) data on inland catches were obtained by surveying selected
fisheries facilities, and then extrapolating the results for the entire river basin. The data
from the lagoons and coastal waters were drawn from offidal catch statistics (log-
books).
Germany: Eel landings statistics from coastal fishery are based on logbooks. The obli-
gation to deliver the inland catch statistics separate for both stages has only recently
been established in most states. Fishers have to deliver the information to the authori-
ties at least on a monthly basis. Data are missing for the some states for inland landings
in 2013.
Denmark: From ls t July 2009, professional fishing operations are based on licences and
landings and number and type of gear must be registered with the Danish AgriFish
Agency. The professional fishermen in saline areas are given a licence to use a limited
number of gears in order to meet the 50% reduction within five years follow ing the EU
eel regulation.
Netherlands: For Lake IJsselmeer, statistics from the auctions around Lake IJsselmeer
are now kept by the Fish Board. For the inland areas outside Lake IJsselmeer, no de-
tailed records of catches and landings were available until 2010. In January 2010, the
Ministry of Economic Affairs, Agriculture and Innovation introduced an obligatory
catch recording system for inland eel fishers. Since 2012, eel fishers are required to also
report effort (type of gear and number of gear) within the obligatory catch recording
system. Catches and landings in marine waters are registered in EU logbooks.
Belgium: There is no commercial fishery for eel in inland waters in Belgium. Commer-
cial fisheries for silver eel in coastal waters or the sea are negligible.
Ireland: Until 2008, eel landing statistics in Ireland were collected from voluntary dec-
larations. From 2005 to 2008 this was im proved by issuing catch declaration forms with
the licence. From 2009, commercial fishing of eel has been closed.
Joint EIFAAC/ICES/GFCM WGEEL REPORT 2014
United Kingdom: In England and Wales, the Environment A gency authorizes com-
mercial eel fishing. It is a legal requirement that all eel fishers submit a catch retum,
giving details of the number of days fished, the location and type of water fished, and
the total w eight of eel caught and retained, or a statement that no eel have been caught.
Annual eel and glass eel net authorizations and catches are summarized by gear type
and Environment Agency region (soon to be RBDs) and reported in their "Salmonid
and Freshwater Fisheries Statistics for England and W ales" series (www.environment-
agency.gov.uk/research/library/publications/33945.aspx). The yellow and silver eel
catches reported to the Environment A gency have historically been reported to the W G
as a single catch for England and Wales. Since 2005, catches have been recorded ac-
cording to the "nearest w aterbody" and reported separately for yellow and silver eels.
In Northem Ireland, overall policy responsibility for the supervision and protection of
eel fisheries, and for the establishment and development of those fisheries, rests with
the Department of Culture, Arts and Leisure (DCAL). Catch returns from the one re-
maining commercial fishery are collated at a single point of collection and marketing,
and reported to D CAL.
There have been no large-scale commercial fisheries for eel in Scotland for many years,
and no catch data are available. Fishing for eel has been effectively banned for a num-
ber of years.
France: The marine commercial fisheries in Atlantic coastal areas, estuaries and tidal
part of rivers in France have been monitored by the "Direction des Péches Maritimes
et de TAquaculture" (DPMA) of the Ministry of Agriculture and fisheries through the
Centre National de Traitement Statistiques (CNTS, ex-CRTS) from 1993 to 2008, and
now by France-Agrimer. This system is evolving and is supposed to include marine
commercial fishermen from Mediterranean lagoons. In this system, glass eels are dis-
tinguished from sub-adult eel, but yellow and silver eels are only recently separated.
The commercial and recreational fishermen in rivers (and in lakes) have been moni-
tored since 1999 by the O N EM A (Office National de l'Eau et des M ilieux Aquatiques,
ex-CSP) in the frame of the « Suivi National de la Péche aux Engins et aux filets »
(SNPE). These two monitoring systems are based on mandatory reports of captures
and effort (logbooks) using similar fishing forms collected monthly (or daily for glass
eel) with the help of some local data collectors. Information for 2013 is not fully pro-
vided.
Spain: Data on eel landings in the Country Report are mostly collected from fishers'
guild reports and fish markets (auctions). The precision of the information of the
catches and landings differs greatly among Spanish Autonom ies (regions). No data
available for marine fishery.
Portugal: The eel fishery is managed by D G PA (General Directorate of Fisheries and
Aquaculture) with responsibility in coastal waters, and AFN (National Forestry Au-
thority) w ith responsibility in inland waters. Fisheries managed by D G PA have oblig-
atory landing reports, while in inland waters, landing reports are obligatory in some
fishing areas but in other areas only if requested by the Authorities.
Italy: The management framework for the Data Collection Framework (DCF) is the
same as has been set up for the eel management under EC Regulation 1100/2007. In the
eleven Regions that preferred to delegate eel management to central govem m ent (Di-
rectorate-General for Sea Fishing and Aquaculture of the Ministry of Agricultural,
Food and Forestry Policy) where commercial eel fishing has been stopped completely
since the year 2009, no data collection is carried out. In the remaining nine regions,
Joint EIFAAC/ICES/GFCM WGEEL REPORT 201 4
where eel fisheries are ongoing, eel fishery data are collected with a standard method-
ology, as foreseen by the Italian National Plan for the Data Collection Framework. De-
tailed data on catches and landings (by life stage, by type of fishing gear, by EMU,
commercial and recreational, etc.) are available from 2009.
Montenegro: No data on catch are available. Scientific estimation of total catch in re-
cent year shows that about 60 tons of eel are landed, of which about 50% is taken by
illegal fisheries.
Algeria: Data are available in the FAO database, but the quality of this information is
not confirmed.
Greece: Fishing in the lagoons is based on the use of fixed barrier traps, which catch
fishes during their seasonal or ontogenic offshore migration every year from Septem-
ber to January. Barrier traps (V-shape traps) are passive, fixed gears and are part of the
fence installed at the interface between the lagoon and the sea (for more details see
A rdizzone et al, 1988). The fishermen cooperatives usually have the adequate infra-
structure to store live eels up to their sale (the largest quantity of these are exported to
other European countries, such as Italy and Germany). The total fishery of the eels and
the total fishery of the rest species must be declared every month to the regional au-
thorities.
Turkey: Data are available in the FAO database, but the quality of this information is
not confirmed.
Egypt: Data are available in the FAO database, but the quality of this information is
not confirmed. Reported figure 5000 tons for 2012 is unreliable.
Tunisia: Data are available in the FAO database, the level of catch w as confirmed by
the Tunisian participants to WGEEL.
Morocco: Data are available in the FAO database, but the quality of this information is
not confirmed.
2 .4 Recreational and non-com m ercial fisheries
M ore data for recreational catch and non-commercial landings were available in 2014
compared w ith previous WGEEL reports. For the purpose of compilation and cross-
checking, two sources of data were used; Country Reports and the (draft) ICES WGRFS
2014 report (Table 2.9). This analysis showed some discrepancies between sources and
not reporting, even if required by the EU Data Collection Framework (Council Regu-
lation (EC) No 199/2008 and Council Decision 2008/949/EC). Recreational fishery data
on eels are to be collected, where appropriate, in the follow ing areas:
• Baltic (ICES Subdivisions 22-32);
• North Sea (ICES Division IV and Vlld) and Eastern Arctic (ICES Division I
and II);
• North Atlantic (ICES Division V-XIV);
• Mediterranean and Black Sea.
The EC (DG-MARE) has indicated some general principles in the forthcoming modifi-
cations to the DCF (anticipated 2018 onwards) which are relevant to diadromous spe-
cies, including improvement in the quality of data and coverage of recreational
Joint EIFAAC/ICES/GFCM WGEEL REPORT 2014
fisheries. The ICES workshop about eel and salmon data collection (ICES, 2012a) rec-
ommended the collection of data on all recreational and commercial eel and salmon
fisheries regardless of how the catches are made.
The data reported in the Country Reports were incomplete in some cases because they
omitted marine or inland waters, reported only passive gears catches w hile angling is
not prohibited, or because some of the countries are not fully sampling recreational
catches, focusing only on a selected life stage. These facts make it impossible in 2014 to
assess the most recent total landings and catches of recreational and non-commercial
fisheries.
Another data gap is the amount of eels released by recreational fishermen and the as-
sociated catch & release (C&R) mortality. An estimate of the amount of released eels
was only provided by the Netherlands and partially (marine angling only) for the UK
(England) and Denmark. In most countries it is prohibited for recreational anglers to
retain eels but catch & release fisheries on eel area allowed in all coimtries. The amount
of fish released by recreational anglers can be substantial (Ferter et al, 2013) and catch
and release mortality can be high (median 11% , mean 18%, range 0-95%, n = 274 stud-
ies; Bartholomew and Bohnsack, 2005) depending on species and factors like hooking
location, temperature and handling time. Unfortunately, no studies have been con-
ducted to estimate catch and release mortality in eel. During the 2012 evaluation of tihe
EMPs, most countries did not report recreational catches (landed and/or released) and
if an estimate of the amount of released eel was presented, C& R mortality was assumed
to be "zero".
2.5 M isreporting of data, and iliegal fisheries
M ost coimtries did not report the level of underreporting, misreporting and illegal fish-
eries in their Country Reports. The limited data that were presented judged insufficient
to draw conclusions on the level of misreporting or illegal fishing. Some countries
reported the existence of illegal practices but those were not quantified. It can be con-
sidered that the current state of knowledge is insufficient to give an idea of the level of
misreporting of data and illegal fisheries at the stock level (Table 2.10).
2.6 N on-fishery anthropogenic m ortallties
ICES derived a framework for intemational assessment based on national/regional bi-
omass and mortality stock indicators. LA, the lifetime anthropogenic mortality rate, is
the addition of EF the fishery mortality and LH all other anthropogenic mortalities
(e.g. hydropow er, barriers, etc.). Member States are required to report their estimates
of the indicators in 2012, 2015, 2018 and every six years thereafter. In 2012, £ H and £F
mortality estimates were not reported for almost half of the EMUs. Furthermore, for
the EMUs for which mortality estimates were reported data were only available for 1 -
4 years. In 24 of 43 EMUs for which both mortality estimates were reported for at least
one year, the rate due to F was greater than that due to H in the most recent year re-
ported. H was greater than F in 15 EMUs, and the two rates were equal in the other
four EMUs.
In time, these mortality stock indicators will provide a suitable series to analyse trends
in mortality for both fisheries and other anthropogenic mortalities. A t this point in time
little can be said with regard to trends in anthropogenic mortalities due to the short
time-series (1^4 years).
Joint EIFAAC/ICES/GFCM WCEEL REPORT 2014
2 .7 Eel stocking
2.7 .1 Trends in stocking
Data on the amount of stocked glass eel and young yellow eel were obtained from
Country Reports and are provided in Electronic Tables E2.3 and E2.4. respectively.
Note that various countries use different size and weight classes of young yellow eels
for stocking purposes.
Stocking of glass eel peaked in the late 1970s and early 1980s, followed by steep de-
clined to a low in 2009 (Figure 2.23). The decline is most likely due to the increase in
price of glass eel from ~€50 kg in the early 1980s to more than €400 kg in the late 2000s
(see Figure 10-6 in WGEEL, 2013). The increase after 2009 is presumably caused by the
implementation of EMPs, because stocking of glass eel is one of the management
measures in m any EMPs. The impact of the price on the amount of stocked glass eel
was particularly clear in 2014, when a strong supply of glass eels meant the price
dropped sharply to around €100 kg and a sharp increase in stocked glass eels was ob-
served.
French stocking data are only available since 2010. Before 2010 stocking occurred in
France but the data are not reported in the Country Report. The time-series only shows
the reported amount of stocking and m ay underestimate the true amount of stocking
that has occurred.
The stocking of young yellow eels has been increasing since the late 1980s (Figure 2.24).
The explanation for this increase is, however, less obvious but m ay also have to do with
the increased price for glass eel.
The proportion of glass eel amongst stocked eel has increased in the recent years (Fig-
ure 2.25).
S2
o
-Q
£
3
Z
CM CM CM CM
Year
Figure 2.23. Reported stocking of glass eel in Europe (Sweden, Finland, Estonia, Latvia, Lithuania,
Poland, Germany, the Netherlands, Belgium, Northem Ireland, Spain, Greece, France (no data be-
fore 2010)) in millions stocked. 2013-2014 data not fully available.
Joint EIFAAC/ICES/CFCM WGEEL REPORT 2014
T — T - ' t - T — T - T - T - X — r - T - T - T - T - C M C N C N C M
Year
Figure 2.24. Reported stocking of young yellow eel in Europe (Sweden, Finland, Estonia, Latvia,
Lithuania, Poland, Germany, Denmark, the Netherlands, Belgium, and Spain), in millions stocked.
2013-2014 data not fully available.
□Young yellow eel nGlass
100%
Year
Figure 2.25. Stocking proportion in numbers stocked between on-grown and glass eel in Europe.
The follow ing present an overview of stocking practices in various countries. Where
information is new or different from that presented in WGEEL 2013, this is highlighted
in italics.
Norway: No stocking on a national level.
Sweden: Until the 1990s, the transport of medium sized yellow eels from the west coast
to the east coast (Sáttál) dominated the stocking programmes. Recently, however, quar-
antined glass eel (i.e. ongrown) stocking is the only action left. Trollháttan eel (from
Göta Alv) has alw ays been a small quantity, and this transport ended in 2005. In 2013,
catches at Trollháttan were transported upstream past three hydropow er plants and
Joint EIFAAC/ICES/GFCM WGEEL REPORT 2014
released in Lake Vánern, i.e. "assisted migration". In 2012 and 2013, glass eels were
again imported from River Severn (UK), after a few years when they had been supplied
by French glass eels. According to the Swedish EMP, about 2.5 million glass eels (in
practice ongrown cultured eels) will be stocked annually. A ll stocked eel have been
chemically marked since 2009.
Finland: In 1989, it w as decided to carry on stocking only with glass eels reared in a
careful quarantine. Since then, glass eels originating in River Sevem in the UK have
been imported through a Swedish quarantine and restocked in almost one hundred
lakes in Southem Finland and in the Baltic along the south coast of Finland. A ll stocked
eel have been chemically marked since 2009.
Estonia: A historical database is available on stocking of glass eel/young yellow eel in
Estonia, w ith records back to 1950. In 1956 stocking of glass eels into L. Vörtsjárv was
started. However, stocking has been irregular. The stocking rate w ith glass eels in L.
Vörtsjárv has been relatively low: annual average in 1956-2000 w as about 37 ind.ha*1
w ith a maximum of 80 ind.ha4 in 1976-1984. Estonia had a state stocking programme
of fish, including eel, for 2002-2010. During the period 2011-2014, the stocking of eel
into the Lake Peipsi basin is supported by the European Fisheries Fund (EFF) up to a
limit of 255 000 euros (co-financing up to one third of total annual financing). In 2011,
680 000 glass eels were stocked; in 2012, 910 000 glass eels and 120 000 ongrown cul-
tured eels were stocked; and in 2013, 810 000 glass eels were stocked. A s the market
price of glass eel in 2014 was extremely low, 900 kg or 3 million of glass eels and 193 000
of ongrown cultured eels were stocked into Estonian lakes.
Latvia: Data on stocking from 1945-1992 were obtained from archives of USSR institu-
tion Balribvod that w as responsible for fish stocking and fisheries control in the former
USSR. Since 1992, every stocking of fish in natural waterbodies in Latvia must be re-
ported to Ministry of Agriculture (BIOR) by special documents. In 2011, Latvia started
stocking again. Glass eel were imported from UK Glass Eel by a supplier from Czech
Republic. Generally, few people ("commission") representing the local municipality
and the fish supplier actually participate in stocking to certify the fact.
Lithuania: Stocking of Lithuanian inland waterbodies with glass eel originating in
France or the United Kingdom began in 1956. During 1956-2007, a total of 148 lakes
and reservoirs covering an area of 95 618 ha was stocked. About 50 million glass and
juvenile eels were stocked in total. Stocking activities started again in 2011 within EMP
framework. In 2011-2014, Fisheries Service under M inistry of Agriculture used support
of European Fisheries Fund and stocked lakes releasing 1 million glass eels and 1 mil-
lion ongrown cultured eels.
Poland: Eel stocking was initiated in regions within current Polish borders around the
beginning of the 20th century. This was done mainly in rivers in the Vistula River basin
and in the Vistula Lagoon. The stocking material of the day originated from the coasts
of the United Kingdom (glass eel), although the Vistula Lagoon w as also stocked with
eel (20-30 cm total length) from the River Elbe. In 2011, Poland started stocking within
the EMP framework. Data on stocking by private stakeholders comes from eel import-
ers. A ll eels are foreign source: glass eels from France and England, and ongrown/cul-
tured yellow eels from Denmark, Germany and Sweden.
Germany: There is no central database on stocking, but some data are available. Data
provided for 2011-2013 not yet complete and have to be considered as the minimum
numbers.
Joint EIFAAC/ICES/CFCM WGEEL REPORT 2014
Denmark: Stocking by fishers in inland waters has taken place for decades, in places
where recruitment of young eel was limited or absent because of migration barriers or
distance to the ocean. Glass eels are imported mostly from France and are grow n in
heated culture to a w eight of 2-5 g before they are stocked. Stocking is done as a man-
agement measure. In 2014 a total of 1.6 million 2-5 gram eels were stocked. In fresh-
water 1.34 million eel of size 2-5 gram were stocked in lakes and rivers as a
management measure and 0.26 million were stocked in marine waters.
Netherlands: Glass eel and young yellow eel are used for stocking inland waters for as
long as anyone can remember, mostly by local action of stakeholders. Future stocking
of 1-1.6 t of glass eel is foreseen. A ll stocked glass eel are sourced outside the Nether-
lands. The main stocking material is glass eels in the Netherlands. However, the aver-
age w eight of stocked young yellow eel decreased from ~30g to ~3 g between 1920 and
2014.
Belgium: Glass eel stocking in Belgium, both in Flanders and in Wallonia, has been
carried out from 1964 onwards, with glass eel from the catching station at N ieuw poort
(River Yser). H owever, due to the low catches after 1980 and the shortage of glass eel,
together w ith regionalisation of the fisheries, this stocking w as stopped in Wallonia. In
Flanders, stocking w as continued after 1980 with foreign glass eel imported mostly
from the U K or France. Also, yellow eels were restocked, mostly from the Netherlands,
but this was ceased after 2000 as yellow eels used for stocking contained high levels of
contaminants. In Wallonia, glass eel stocking was again initiated in 2011, in the frame-
w ork of the Belgian EMP. Quantities of glass eel stocked amount to 40 and 50 kg for
W allonia in 2011 and 2012 respectively. In Flanders 156 kg, 140 kg and 500 kg were
stocked respectively in 2012,2013 and 2014. The glass eel were supplied from the Neth-
erlands but originated from France. In 2013, 140 kg was stocked in Flemish waters us-
ing glass eel supplied by a French company (SAS Anguilla, Charron, France).
Ireland: Purchase of glass eel for stocking from outside the state does not currently
take place. The only stocking that takes place is an assisted upstream migration around
the barriers on the Shannon, Eme and Lee. Assisted migration of upstream migrating
pigmented small eel takes place in the Shannon (Ardnacrusha) and Eme (Cathaleen's
Fall), and of pigmented young eel (bootlace) on the Shannon (Parteen Regulating
Weir). Prior to 2009, small amounts of glass eel and pigmented small eels were taken
in the Shannon Estuary and in neighbouring catchments and these were stocked into
the Shannon above Ardnacrusha and Parteen H ydropower Stations.
UK: There is no stocking of ongrown eel anywhere in UK. Glass eel from the England
and W ales fishery are stocked into river systems of England and Wales: 53.6 kg in 2010,
50.1 kg in 2011, 41.5 kg in 2012, 65.7 kg in 2013, 55.6 kg in 2014. No eel stocking takes
place in Scotland. In Northem Ireland, recmitment of glass eel and pigmented small
eel to Lough Neagh has been supplemented by stocking of purchased glass eel since
1984, and these eel have been sourced from the glass eel fishery in England and Wales.
However, in 2010, the 996 kg of glass eel purchased from UK Glass Eel Ltd originated
from fisheries in San Sebastian, Spain and the west coast of France: no glass eels from
UK waters were purchased. In 2011 and 2012, glass eel from UK and French sources
were stocked into Lough Neagh though all were purchased from U K Glass Eels Ltd. In
2013 and 2014,1866 kg and 2680 kg respectively of entirely UK sourced glass eels were
stocked into L. Neagh. 2014 was also the first time that glass eel going into Lough
N eagh (and the River Lagan) were marked using Strontium Chloride.
France: A public tender of 2 million Euros for stocking (and stocking monitoring) has
been made each year since 2010. In 2014 this public tender was made twice. Glass eels
Joint EIFAAC/ICES/GFCM WGEEL REPORT 2014
are all stocked in the EMU in which they are caught. Thus, there is no stocking in EMU
where there isn't a glass eel fishery. Glass eels have been quarantined in fish sellers'
tanks for the duration of sanitary analyses. A ll stocking sites are monitored to assess
the efficiency of stocking. The first nationally organized stocking action started in 2010.
In 2010, two projects representing 150 k € (including monitoring) for 200 kg restocked
were selected. However, no glass eel were restocked because of the end of the glass eel
season. However, 209 kg (glass eel mean weight 0.233 g and thus 900 000 glass eels)
were restocked in the Loire River in July 2010 after these glass eel were collected from
a CITES seizure. In 2011, eleven projects were selected for a total amount of 4024 kg.
H owever, only 747.5 kg were really restocked, partly because of late selection process
and partly because of lack of supply. In 2012, eleven projects were selected for a total
amount of 3475 kg, and 3086 kg were really restocked. In 2013, eleven projects were
selected for a total amount of 3400 kg, and 2940 kg have really been restocked. In 2014,
eleven projects were selected for a total amount of 6307 kg, and 5656 kg have really
been restocked. Apart from this national restocking programme, some local restocking
m ay have taken place but the quantity, quality (glass eel or yellow eel), origins and
objectives are unknown. For example: there has been a long history of stocking in Lake
Grand Lieu (Adam, 1997) to enhance a fishery with a maximum of more than 2 t of
glass eels in the 1960s and more than 1.5 t of elvers in the 1990s.
Spain: N o stocking is managed on a national level. Each Autonom y has its own rules
and experience conceming stocking. In Spain, different stocking experiences have
been carried out:
• In Navarra stocking is carried out in the Ebro River but only as a measure of
artifidal maintenance of the presence of eel in the rivers.
• Since 1988, C. Valenciana fishermen from the Albufera and from the Bullent
and M olinell Rivers must give a percentage of their glass eels catches for
restocking. These glass eels are raised in the public Centre for the Production
and Experimentation of W arm Water Fishes until they reach a w eight of 8-
10 g. Fattened eels are released up in the river waters and wetlands of C.
Valenciana and other autonomous regions. The EMP of C. Valenciana con-
tains a detailed stocking plan.
• In Asturias, the Head Office of Fishery purchased 6 kg and 8 kg of glass eel
that w ere released in Sella and Nalón Rivers in 2010 and 2011 respectively.
The price per kg of glass eel was 531.8 € in 2010 and 577.8 € in 2011. No
stocking w as performed during 2012-2014.
• In Catalonia Inner River Basins and the Ebro RBD, different stocking expe-
riences have been carried out since 1996. During 1998-2007, fishermen gave
5% of their seasonal glass eel catches approximately for stocking in the Flu-
via, M uga, Ter and Ebro Rivers. No stocking was performed during 2012-
2014.
• In Cantabria, 40% of the total glass eel landings of the 2010-2011 fishing sea-
son were used for restocking. Some of the catches were kept alive in tanks
by the Council and stocked w eekly along the fishing period in different river
basins depending on the source of landings. The rest of the glass eels were
cultured and stocked at different stages of their life cycle, aiming to assess
the efficiency of each of the methods. No data available for the 2012-2014.
• In the Basque Country, a new pilot study started in the Oria River in 2011.
In a first phase, 2400 young eels trapped in the Orbeldi trap (in Usurbil,
Joint EIFAAC/ICES/GFCM WCEEL REPORT 2014
Gipuzkoa) were translocated up to the Ursuaran River (in Idiazabal, Gipuz-
koa). Both rivers belong to the same river basin (Oria River basin). During
2012, and within the same project, 2.8 kg of glass eels from the fishery were
stocked directly in the Oria River and another amount was kept for fattening
in an eel farm: 1.7 kg of on-grown glass eel w as stocked after. In 2013,
6250 glass eels from the fishery in the Urola River were stocked directly up-
stream. During the summer 2011,2012,2013 and 2014, different electric fish-
ing operations have been carried out aiming to monitor the restocked
individuals.
Portugal: No stocking on a national level.
Italy: The new glass eel regulation foresees that glass eel fisheries can continue on a
local scale, provided that 60% is used for stocking in national inland waters open to the
sea, and provided that fishers compile specific and detailed logbooks of catches and
sales. This new system, together with reinforced controls by the Corpo Forestale dello
Stato, shall ensure that information on recruitment in Italy is available from year to
year, that most glass eel is conveyed to stocking and that illegal fishing is definitively
prevented. Up to 2010, the new regulation was not in force, its definite approval being
achieved in 2011. From 2011, the new regulation being in force, fishing has started
again and catches are declared to the Ministry on a w eekly basis. In 2013, 67 kg glass
eel, 126 kg ongrown eel and 9.4 kg bootlace eels were stocked. A t present, it is not
possible to document where exactly restocking were performed, as provinces and re-
gions have not provided this information. Overall, the two first years of implementa-
tion of the new regulatory framework for glass eel fisheries (2011 and 2012) must be
considered as a pilot period, accoimting for the setting up of the declaration system. A t
present (2013 and 2014), filling of the forms is still lacking, and the details of the docu-
ments of purchase and sale are also deficient. This does not allow complete traceability
of movements on the Italian territory. To overcome this problem, a full traceability sys-
tem is currently being studied, developed in collaboration w ith the Corpo Forestale
dello Stato - Unit CITES. This system should ensure the full traceability of all glass eel
movements, either from national waters or imported, also aiming to definitively erad-
icate illegal fishing of glass eels.
Greece: In the past some scarce, empirical and small scale attempts were undertaken
with the aim of im proving local fisheries. Glass eel stocking was performed in the Lake
Pamvotis (EMU-1) and the Kalama's delta (EMU-1), while young reared eels were in-
troduced in the Lake Pamvotis and at the estuaries of W estem Greece rivers (Econo-
midis, 1991; Economidis et ai, 2000). There is no information conceming the number of
eels or their characteristics, and no data exists about the results of these experiments.
Then in 2010 and 2012, two more stockings took place in Messolonghi -Aitoliko lagoons
(EMU 1) and in River Acherondas (EMU 1) according to the protocol suggested by the
HEMP. In 2013, eel stocking was performed in River Acherondas (EMU 1), w ith eels
provided by a private company in Epirus. The agency responsible for the eel releases
in 2013 w as the Regional Fisheries Authorities of Epirus-Westem Macedonia. Accord-
ing to a decision (AAA: BAIOOPIT N02) in 2013, they have proceeded to the release of
10% of glass eels, imported by the aquaculture units in Epims.
2 .8 Aquaculture production of European eel
Aquaculture production data for European eel limited to European countries from
2004 to 2013 are compiled from different sources: Country Reports to WGEEL 2014
Joint EIFAAC/ICES/GFCM WGEEL REPORT 2014
(Table 2.11), FAO (Table 2.12) and FEAP (Federation of National Aquaculture associa-
tions) (Table 2.13). Some discrepancies exist between FAO and FEAP databases and the
Country Reports, but overall the trend in aquaculture production is decreasing from
8000-9000 tonnes in 2004 to approximately 5000 tonnes in 2013 (Figure 2.26). Some of
the discrepancies between FAO and the Country Report data m ay result from the pos-
sibility that eel that is used for stocking is not being reported to the FAO.
Figure 2.26. Different sources of data for aquaculture production of European eel in Europe from
2005 to 2013, in tons.
2.9 Environmental drivers
This year, the working group members were asked to include in their country reports
any information that they thought was relevant to consideration of the potential envi-
ronmental drivers influencing the stock. This information has been compiled and is
presented in Table 2.14. Though those were not alw ays reported in the country reports,
they have been often assessed as having large effect in continental water, either as pos-
sibly continental w ide change (e.g. temperature, eutrophication) or on a more local
scale (unlike the oceanic factors).
Joint EIFAAC/ICES/GFCM WGEEL REPORT 2014
Table 2.1. European eel recruitment time-series updated to 2014.
2.10 Tables
CODE NAME COUNTRY AREA STACE
Ring Ringhals scientific survey Sweden North sea gls.
Stel Stellendam scientific estimate Netherlands North sea gls.
Kavl K'avlingeán trapping all Sweden Baltic ylw.
Yser Ijzer Nieuwpoort sdentific Belgium North sea gls.
YFS2 IYFS2 scientific estimate Sweden North sea gls.
Dala Dal'alven trapping all Sweden Baltic ylw.
SeEA Sevem EA commercial catch UK British Isle gls.
SeHM Sevem HMRC commercial catch UK British Isle gls.
Imsa Imsa Near Sandnes trapping all Norway North sea gls.
MiSp Minho Spanish part commerdal
catch
Spain Atlantic Ocean gls.
Fre Frémur France North sea gls.+
ShaA Shannon Ardnacmsha trapping Ireland British Isle gls.+
Albu Albufera de Valencia commercial
catch
Spain Mediterannean
Sea
gls.
Nalo Nalon Estuary commercial catch Spain Atlantic Ocean gls.
Feal River Feale Ireland Atlantic Ocean gls.+
RhDO Rhine DenOever sdentific Netherlands North sea gls.
Rhij Rhine Ijmuiden sdentific Netherlands North sea gls.
Ronn R"onne A ° trapping all Sweden North sea ylw.
Katw Katwijk sdentific estimate Netherlands North sea gls.
Laga Lagan trapping all Sweden North sea ylw.
MiPo Minho Portugese part
commercial catch
Portugal Atlantic Ocean gls.
GiSc Gironde scientific estimate France Atlantic Ocean gls.
Lauw Lauwersoog scientific estimate Netherlands North sea gls.
Ebro Ebro delta lagoons Spain Mediterannean
Sea
gls.
Meus Meuse Lixhe dam trapping Belgium North sea ylw.
Gota Gáta Alv trapping all Sweden North sea ylw.
Morr M"ornxmsán trapping all Sweden Baltic ylw.
Mota Motala Str”om trapping all Sweden Baltic ylw.
ShaP Shannon Parteen trapping partial Ireland British Isle ylw.
Bann Bann Coleraine trapping partial Northem
Ireland
British Isle gls.+
ylw.
Maig River Maigue Ireland Atlantic Ocean gls.
Inag River Inagh Ireland Atlantic Ocean gls.+
Visk Viskan Sluices trapping all Sweden North sea gls.+
Eme Eme Ballyshannon trapping all Ireland British Isle gls.+
Sle Slette A Denmark North sea gls.+
KUt Klitmoeller A Denmark North sea gls.+
AICP Albufera de Valencia commercial
cpue
Spain Mediterannean
Sea
gls.
Nors Nors A Denmark North sea gls.+
Table 2.2. European eel recruitment time-series; those only updated to 2013.
Joint EIFAAC/ICES/GFCM WGEEL REPORT 2014
C O D E N AM E COUNTRY AREA STACE
Gude Guden Á
trapping all
Denmark North Sea Ylw.
Bres Bresle France Atlantic Ocean Gls + ylw.
Hart Harte trapping
all
Denmark Baltic Sea Ylw.
ble 2.3. European eel recruitment time-series; those stopped or not updated to 2013 at least.
CODE NAME COUNTRY AREA STAGE LAST
YEAR
YFSl IYFS scientific estimate Sweden North sea gls. 1989
Vida Vidaa Herjer sluice commerdal
catch
Denmark North sea g ls . 1990
Ems Ems Herbrum commercial catch Germany North sea gls. 2001
Tibe Tiber Fiumara Grande com-
merdal catch
Italy Mediterannean
Sea
gls. 2006
AdCP Adour Estuary (cpue) com-
mercial cpue
France Atlantic Ocean gls. 2008
AdTC Adour Estuary (catch) com-
mercial catch
France Atlantic Ocean gls. 2008
GiCP Gironde Estuary (cpue)
commerdal cpue
France Atlantic Ocean g ls . 2008
GiTC Gironde Estuary (catch) com-
merdal catch
France Atlantic Ocean gls. 2008
Loi Loire Estuary commercial catch France Atlantic Ocean gls. 2008
SevN Sévres Niortaise Estuary com-
merdal cpue
France Atlantic Ocean g ls . 2008
Vil Vilaine Arzal trapping all France Atlantic Ocean gls. 2011
Joint EIFAAC/ICES/CFCM WGEEL REPORT 2014
Table 2.4. GLMglass eel - year: area + site average of predicted values for 40 glass eel series, values
given in percentage of the 1960-1979 period.
1960 1970 1980 1990 2 0 0 0 2 0 1 0
EE NS EE NS EE NS EE NS EE NS EE NS
0 130 192 97 87 119 72 39 13 20 4 4.5 0.4
1 1 1 2 107 50 78 90 54 18 3 9 1 4.2 0.4
2 143 164 53 10 1 102 30 25 7 13 2 6 .1 0.6
3 174 205 59 45 49 25 29 6 14 2 8.6 1.1
4 95 107 89 120 57 9 29 7 8 1 12.2 3.7
5 125 70 68 51 54 8 35 4 9 1
6 76 80 1 1 1 96 36 8 28 4 7 0
7 78 88 103 75 65 9 44 4 7 1
8 129 113 1 1 2 54 65 9 18 3 6 1
9 57 80 140 86 47 4 23 5 4 1
Table 2.5. GLM yellow e e l y e a r + site average of predicted values for 12 yellow eel series, values
given in percentage of the 1960-1979 period.
1950 1960 1970 1980 1990 2000 2 0 10
0 175 158 51 90 29 17 13
1 232 169 55 37 36 18 12
2 227 164 103 47 20 33 1 1
3 367 137 125 42 13 19 7
4 181 54 59 31 49 26 36
5 275 102 110 60 16 9
6 130 141 33 44 9 15
7 145 95 67 44 2 1 2 1
8 147 159 61 57 18 14
9 313 104 54 33 23 7
Joint EIFAAC/ICES/GFCM WCEEL REPORT 2014
Table 2.6. Summary of the breakpoints identified in the glass eel time-series using the CUSUM method.
K T im e p e r io d T im e - s e r ie s B r e a k p o in t s
k l CKNorth 1960-2014 Glass eels 'North Sea' 1981
klc;i£l£Isewhere 1960-2014 Glass eels 'Elsewhere Europe' 1970,1982,1990
k 2 GENorlh 1980-2014 Glass eels 'North Sea' 1983
k 2cEEIscwhere 1980-2014 Glass eels 'Elsewhere Europe' 1990,1997
kScENorth 1980-2014 Ln(glass eels 'North Sea') 2000, 2013
kSGEEisewhere 1980-2014 Ln(glass eels 'Elsewhere Europe') 2000
Table 2.7. Breakpoints estimation for each time-series using the segmented regression method.
T im e p e r io d T im e - s e r ie s B r e a k p o in t s
1960-2014 Glass eels 'North Sea' 1981,1984, 1996, 2012
1960-2014 Glass eels 'EIsewhere Europe' 1972,1978, 2011
1960-2014 Yellow eels -
Joint EIFAAC/ICES/GFCM WGEEL REPORT 2014
Table 2.8. Time-series of yellow and silver eel described in the country reports for 2014.
G ear START En d M issing Y ears U n it STAGE CODE Lo c a t io n N am e COUNTRY
fykenet survey 1960 2013 0 Index yellow eel DenB Den Burg, Texel Den Burg fykenet survey Netherlands
electro fishing 1979 2013 13 eel.m-2 yellow eel VesV Vester Vedsted brook Vester Vested elecrofishing Denmark
beach seine survey 1925 2013 4 eel.haul-1 yellow + silver eel ska Skagerrak Skagerrak Beach Seine Survey Norway
fykenet survey 1977 2013 2 eel. net-1 yellow eel Barseback Swedish west coast monitoring Sweden
fykenet survey 2002 2013 1 eel. net-1 yellow eel Kullen Swedish west coast monitoring Sweden
fykenet survey 1976 2013 2 eel. net-1 yellow eel Vendelsö Swedish west coast monitoring Sweden
fykenet survey 2002 2013 0 eel. net-1 yellow eel Hakefjorden Swedish west coast monitoring Sweden
fykenet survey 1998 2013 1 eel. net-1 yellow eel Fjallbacka Swedish west coast monitoring Sweden
Elecrified trawl 1988 2013 0 n/ha yellow eel Ijsselmeer Northern Ijsselmeer trawl survey Netherlands
Elecrified trawl 1988 2013 0 n/ha yellow eel Ijsselmeer Southern Ijsselmeer trawl survey Netherlands
fykenet survey 1995 2013 2 kg/fyke/day (?) yellow eel Zandvliet Belgium
fykenet survey 1995 2013 3 kg/fyke/day (?) yellow eel Antwerpen Belgium
fykenet survey 1997 2013 2 kg/fyke/day (?) yellow eel Steendorp Belgium
fykenet survey 1997 2013 4 kg/fyke/day (?) yellow eel Kastel Belgium
2006 2013 0 kg/ha silver eel BadB Baddoch Burn Baddoch Burn Scoltland
1966 2013 24 kg/ha silver reel GirB Girnoch Bum Girnoch Brun Scoltland
1999 2013 4 kg/ha silver eel Shie Shieldaig Shiledaig Scoltland
1991 2011 5 cpue silver eel BITl BITS-1
1991 2010 0 cpue silver eel BIT4 BITS-4
1988 2011 2 cpue silver eel NSIB NS-IBTS
1988 2005 6 cpue silver eel Pand Pandalus
1975 2013 0 number silver eel ImsS Imsa Imsa Siver Norway
1996 2013 0 number silver eel Frem Frémur Frémur France
Joint EIFAAC/ICES/GFCM WGEEL REPORT 2014
T ab le 2.9. Recreational fisheries data for European eels.
R e t a in e d
I n l a n d M a r in e
C o u n t r y / A n g p a s s i v e t o t a l A n g l i p a s s iv e t o t a l T o t a l
Y E A R L I N G G E A R S I N L A N D N G G E A R S M A R I N E R E T A I NE
D
Norway
2013 NP NP NP NP
Sweden
2013 NP NP NP NP
Finland
2010 9 9 1 1 10
Estonia
2012 0.02 0.02 0.02
Latvia
2012 NC NP 0.102 0.102 0.102
Lithuania
2013 3 NP 3 NC NP 3
Poland
2013 26.7 NP 26.7 <1 NP <1 27
Germany
2013 NC NC NC NC 240
Denmark
2013 NC 8 8 50 50 58
Netherland
s
I 53
R e l e a s e d
I N L A N D
A N G L I
N G
P A S S I V E
G E A R S
M a r in e
T O T A L
I N L A N D
A N G
L I N G
P A S S I V E T O T A L T O T A L
G E A R S M A R I N E R E L E A S E
D
NC NC
NC NP
NC NC
NC NP
NC NP NC NC
NC NP NC NP
NC NP NC NP
NC NC NC NC
NC NC 70000 NC
W
54 |
R e t a in e d
I n l a n d M a r in e
C o u n t r y / A n g p a s s i v e t o t a l A n g l i p a s s i v e t o t a l T o t a l
Y E A R L I N G G E A R S I N L A N D N G G E A R S M A R I N E R E T A I N E
D
2010
Belgium
2013
(Flanders)
2013
(Wallonia)
UK
(England/
Wales)
2012
UK
(Scotland)
2013
Ireland
2013
France
2012
Portugal
2013
Spain
2013
Italy
2013
53 NP
NC
NP
N P
NP
NP
NC
NC
NC
8 2 .6 ?
NP
NP
NP
NP
NP
5.3
NP
NP
53 26 NP
5.3
NC NP
NP NP
5000 NP
(#)
NP NP
NP NP
NC NP
NC NP
26 79
5.3
NC 2.4* 2.4* 2.4*
Joint EIFAAC/ICES/GFCM WGEEL REPORT 2014
R e l e a s e d
I N L A N D M A R I N E
A N G L I P A S S I V E T O T A L A N G P A S S I V E T O T A L T O T A L
N G G E A R S I N L A N D L I N G G E A R S M A R I N E R E L E A S E
D
143 NP 143 25 NP 25 168
NC NP NC NP
NC NP NP NP
NC NP 32000 NP
w
NC NP NC NP
NC NP NC NP
NC NC NC NP
NC NP NC NP
NC NP NC NP
Joint EIFAAC/ICES/CFCM WCEEL REPORT 2014 55
C O U N T R Y /
Y E A R
A n g
L I N G
R e t a in e d
I N L A N D
P A S S I V E T O T A L
G E A R S I N L A N D
M a r i n e
A n g l i p a s s i v e
N G G E A R S
T O T A L
M A R I N E
T o t a l
R E T A I N E
D
R e l e a s e d
I n l a n d
A N G L I P A S S I V E
N G G E A R S
M a r i n e
T O T A L A N G
I N L A N D l i n g
P A S S I V E
G E A R S
T O T A L
M A R I N E
T o t a l
R E L E A S E
D
Moxitenegr
o
2013 NC NP NC NC NC NP NC NC
Albania
2013 NC NP NC NP NC NP NC NP
Greece
2013 NP NP NP NP NC NP NC NP
Turkey
2013 NC NC NC NC NC NC NC NC
Tunisia
2013 NC NP NC NP NC NP NC NP
Joint EIFAAC/ICES/GFCM WGEEL REPORT 2014
Table 2.10. Estimation of underreported catches (in kg) of eel in 2013, by stage, as declared to the working group.
Glass eel Yellow eel SlLVER EEL COMBINED
(Y + S)
EMU
ÖO bO "bO
h* 60
co
115
U
£
Ohcu
. . DL . . . Ú
nd
er
re
pt
.
%
'bO
Dh(U
1-
Vh<UT3
3 To
ta
l
ca
tc
he
s
(k
g)
(3o
T3
f f l
"tlO
cx
4!
...........P4 U
nd
er
re
pt
.
%
U
nd
er
re
pt
.
(k
g)
To
ta
l
ca
tc
he
s
(k
g) Ol<V
•§
15u
"Ö
13
gncu
Pá U
nd
er
re
pt
.
%
U
nd
er
re
pt
.
(k
g)
To
ta
l
ca
tc
he
s
(k
g) C/5
•M03
U
TÍ
€
Eh<yP4 U
nd
er
re
pt
.
%
U
nd
er
re
pt
.
(k
g)
To
ta
l
ca
tc
he
s
(k
g)
FI 3000 4-5 150 3150
LT 12 555 0.1 14.2 12 569
PL 48 631 56.5 27 500 76131
NL 4.4
FR 5525 11.7 647 6172 23 738 0.3 65 23 803 - - 892 - - - 957 -
UK 344 0 0 344 321 000 0 0 321 000 72 000 0 0 72 000 393 000 0 0 0
Joint EIFAAC/ICES/CFCM WCEEL REPORT 201 4
Table 2.11. Aquaculture production of European eel in Europe from 2005 to 2013, in tons. Source:
Country Reports. N R . = not reported.
2004 2005 2006 2007 2008 2009 2010 201 1 2012 201 3
Denmark 1500 1700 1900 1617 1740 1707 1537 1156 1093 824
Estonia 26 19 27 52 45 30 20 25 35 NR
Germany 328 329 567 740 749 667 681 660 706 757
Netherlands 4500 4500 4200 4000 3700 3200 2000 2300 2600 2900
Portugal 1,5 1,4 1,1 0.5 0.4 1,1 NR 0,6 NR NR
Sweden 158 222 191 175 172 139 91 94 93 92
Poland 1 1 1 1 1 1 1 1,5 1,5 1,5
Italy 1220 1131 807 1000 551 587 NR NR NR NR
Spain 424 427 403 478 461 450 411 391 352 210
Total 8157 8329 8096 8063 7419 6781 4741 4602 4880,5 4784,5
Table 2.12. Aquaculture production of European eel in Europe from 2004 to 2012, in tons. Source:
FAO FishStat.
2004 2005 2006 2007 2008 2009 2010 201 1 2012
Denmark 1823 1673 1699 1614 895 1659 1532 1154 1061
Estonia 7 40 40 45 47 30 22 10 NR
Germany 322 329 567 440 447 385 398 660 460
Netherlands 4500 4000 5000 4000 3700 2800 3000 3000 1800
Portugal 2 1 2 1 1 1 NR 1 NR
Sweden 158 222 191 175 172 0 0 90 93
Poland NR NR NR NR NR NR NR NR NR
Italy 1220 1132 807 1000 551 567 647 1000 450
Spain 424 427 403 479 534 488 423 434 373
Greece 557 372 385 454 489 428 372 370 320
Hungary 11 5 NR NR NR NR NR NR NR
Total 9024 8201 9094 8208 6836 6358 6394 6719 4557
58 | Joint EIFAAC/ICES/GFCM WCEEL REPORT 2014
Table 2.13. Aquaculture production of European eel in Europe from 2004 to 2013, in tons. Source:
FEAP.
2004 2005 2006 2007 2008 2009 2010 2011 2012 2013
Denmark 1500 1610 1760 1870 1870 1500 1899 1154 1061 1061
Estonia NR NR NR NR NR NR NR NR NR NR
Germany NR NR NR NR NR NR NR NR NR NR
Netherlands 4500 4500 4200 3000 3000 3200 3000 2800 2300 2000
Portugal NR NR NR NR NR NR NR NR NR NR
Sweden 158 222 191 175 172 170 170 NR 93 93
Poland NR NR NR NR NR NR NR NR NR NR
Italy 1220 1132 808 1000 550 568 568 1100 1100 1100
Spain 390 405 440 280 390 510 446 402 350 315
Greece 500 500 385 454 489 428 428 372 304 304
Hungary 20 20 20 NR NR NR NR NR NR NR
Total 8288 8389 7804 6779 6471 6376 6511 5828 5208 4873
Joint EIFAAC/ICES/GFCM WGEEL REPORT 2014
T able 2.14. P ossib le environm ental drivers sum m arized from country reports.
COUNTRY
CODE
COMMENT ON ENVIRONMENTAL DRIVERS
NO Some rivers are still severely affected by chronic or episodic acid water. The areas
affected by acidification have likely been among the most important areas for eel in
Norway. Based on surveys in 13 rivers that are now limed, it seems that occurrence
and density of eel was reduced due to acidification (Thorstad et al., 2011, Larsen et al.r
2014). Densities of eel increased more than four-fold after liming when compared wdth
pre-liming levels.
LV Some research results related to climate change in Latvia and possible effects are
published in: Climate change in Latvia and adaptation to it /eds. Maris Klavins and
Agrita Briede. - Riga: University of Latvia press, 2012. -188 pp. Increase of water
temperature and eutrophication would be factors improving eel living conditions in
Latvia.
BE Improvement of wrater quality by installing purification units is an on-going process
(within the objectives of the Water Framework Directive). In summary following
management measures are planned for restoration of eel habitat and accessibility of
the rivers: • 90% of prior obstacles should be removed by 2015, other 10%- 2021; •
resolving by migration barriers ti.ll 2027; • implementation of measures to attain the
good quality class of prior rivers.
UK The following impacts have been assessed for all RBDs in England and Wales;
commercial fisheries, tidal gates, pumping stations, surface water abstractions and
hydropower installations. The main impact that has not been assessed is the impact of
manmade barriers, but work is ongoing to quantify the impact. The impact of the
recreational fishery, predators and contaminants and parasites is treated as part of
natural mortality.
FR In France same impacts of climate change and water pollution effects has studied.
Since 1960 the river Gironde discharge has been highly decreasing, lightly in the river
Loire while the discharge remained stable in Seine. Moreover the summer
temperature in the Gironde estuary has increased of 2.5 °C in 30 years. In France the
concentration in nitrate has increased until the 1990s and has been stabilized since.
Metallic and organic pollution is not well known and evolutions are site-specific (Le
Treut ed. 2013)
ES There is no information regarding how the environment in Spain has changed in the
last 50 years that might have influenced eel production.
AL Development of agriculture, construction of dams, development of industrial
activities, have generated varies kind of impacts on ecological dynamics (physical and
biological)
GR In Greece national report was concluded that arrangement of facilities improving
accessibility up from barriers are expensive and by doubtful results. Interventions in
lowland ecosystems near the estuaries will be significantly more effective, as
suggested in the Greek Management Plan for the Eel.
Joint EIFAAC/ICES/CFCM WGEEL REPORT 2014
3 ToR e) Further develop the stock-recruitm ent relationship and
associated reference points, using the latest available data
3.1 Introduction
This chapter w ill first summarise past ICES advice on eel with a focus on reference
points, and discuss the objectives and targets of the Eel Regulation; then discuss op-
tions for providing advice, in particular focused on mortality reference points. Then,
w e present the derivation of reference points for the eel, using three different ap-
proaches; this part is essentially a rewriting of the preliminary results of WGEEL
(2013). Future improvement of the analysis of the stock-recruit-relation w ill require
additional data, for which w e supply recommendations. Finally, the recent upturn in
recruitment is put into perspective, contrasting the observed upturn to the change in
spawner escapement assessed in 2012.
3.2 Reference points used or implicated in previous ICES Advice
Since 1998 (ICES, 1999 through to ICES, 2010), ICES has given advice4 that the stock
has shown a long-term decline; that fishing and other anthropogenic impacts should
4ICES 1999 (ad\dce) advised "The eel stock is outside safe biological limits and the cur-
rent fishery isn ot sustainable. (...) Actions that would lead to a recovery of the recruit-
ment are needed. The possible actions are 1) restricting the fishery and/or 2) stocking
of glass eel."
ICES (2000) (advice) recommended "that a recovery plan should be implemented for
the eel stock and that the fishing mortality be reduced to the low est possible level until
such a plan is agreed upon and implemented."
ICES (2001) (advice) recommended "that an intemational rebuilding plan is developed
for the whole stock. Such a rebuilding plan should include measures to reduce exploi-
tation of all life stages and restore habitats. Until such a plan is agreed upon and im-
plemented, ICES recommends that exploitation be reduced to the low est possible
level."
ICES (2002) (advice) recommended "that an intemational recovery plan be developed
for the whole stock on an urgent basis and that exploitation and other anthropogenic
mortalities be reduced to as close to zero as possible, until such a plan is agreed upon
and implemented. [...] Exploitation, which provides 30% of the virgin (F=0) spawning
stock biomass is generally considered [...] a reasonable provisional reference target.
H owever, for eel a preliminary value could be 50%."
ICES (2006) (advice) advice read: "An important element of such a recovery plan
should be a ban on all exploitation (including eel harvesting for aquaculture) until clear
signs of recovery can be established. Other anthropogenic impacts should be reduced
to a level as close to zero as possible."
ICES (2008a) (advice) concluded "There is no change in the perception of the status of
the stock. The advice remains that urgent actions are needed to avoid further depletion
of the eel stock and to bring about a recovery."
ICES (2009) (advice) reiterated its previous advice that "all anthropogenic impacts on
production and escapement of eels should be reduced to as close to zero as possible
until stock recovery is achieved".
Joint EIFAAC/ICES/GFCM WGEEL REPORT 2014
be reduced; that a recovery plan should be compiled and implemented; that prelimi-
nary reductions in mortality to as close to zero as possible are required until such a
plan is implemented, until stock recovery has been achieved, until there is clear evi-
dence that the stock is increasing, that both the recruitment and adult stock are increas-
in g ,, and of sustained increase in both recruitment and the adult stock.
ICES (2002) discussed a potential reference value for spaw ning-stock biomass: "a pre-
cautionary reference point for eel must be stricter than universal provisional reference
targets. Exploitation, which provides 30% of the virgin (F = 0) spaw ning-stock biomass
is generally considered to be such a reasonable provisional reference target. However,
for eel a preliminary value could be 50%." That is: ICES advised to set a spawning stock
biomass limit above the universal value of 30%, at a value of 50% of Bo. ICES (2007)
added: "an intermediate rebuilding target could be the pre-1970s average SSB level
which has generated normal recruitments in the past."
ICES has not advised on specific values for mortality-based reference points, but the
w ordings "the lowest possible level" and "as close to zero as possible" im ply that the
mortality limit should be set close to zero. Over the years, the implied time frame for
this advice has changed from "until a plan is agreed upon and implemented", to "until
stock recovery is achieved" and "until there is clear evidence that the stock is increas-
ing". The first and third phrases are more interim precautionary mortality advice than
clear reference points.
3.3 Objectives and targets /lim its of the Eel Regulation
The Eel Regulation (Covmcil Regulation 1100/2007) sets a limit for the escapement of
(maturing) silver eels at 40% of the natural escapement (in the absence of any anthro-
pogenic impacts and at historic recruitment). That is: a limit is set at 40% of Bo, in-be-
tween the universal level and the more precautious level advised. ICES (2008) noted
that its 2002 advice w as "higher than the escapement level of at least 40% set by the EU
Regulation."
Because current recruitment is generally far below the historical level, a retum to the
limit level is not to be expected within a short range of years, even if all anthropogenic
impacts are rem oved (Áström and Dekker, 2007). The Eel Regulation indeed expects to
achieve its objective "in the long term", but it does not specify an order of magnitude
for that duration. Noting the general objective to protect and recover the European eel
ICES (2010c) (advice) reiterated its previous advice that "all anthropogenic mortality
(e.g. recreational and commercial fishing, barriers to passage, habitat alteration, pollu-
tion, etc.) affecting production and escapement of eels should be reduced to as close to
zero as possible until there is clear evidence that the stock is increasing."
ICES (2011 advice) and ICES (2012 advice) reiterated its previous advice that "all an-
thropogenic mortality (e.g. recreational and commercial fishing, hydropower, pollu-
tion) affecting production and escapement of eels should be reduced to as close to zero
as possible until there is clear evidence that both recruitment and the adult stock are
increasing."
ICES (2013 advice) once more advised "that all anthropogenic mortality (e.g. recrea-
tional and commercial fishing, hydropower, pollution) affecting production and es-
capement of silver eels should be reduced to as close to zero as possible, until there is
clear evidence of sustained increase in both recruitment and the adult stock."
Joint EIFAAC/ICES/GFCM WCEEL REPORT 2014
stock, w e conclude that a further deterioration of the status of the stock is to be avoided,
which im plicitly sets an upper limit on anthropogenic mortality (in the order of mag-
nitude of E A = 0.92, see below.
The 40% biomass limit of the Eel Regulation applies to all management units, without
differentiation between the units. Whether or not that implies that the corresponding
mortality limit (EA = 0.92) also applies to all units or not, is unclear. However, since it
is unknow n whether or not all areas contribute to successful spawning, a uniform mor-
tality limit for all areas w ill constitute a risk-averse approach (Dekker, 2010).
3.4 Multiple criteria
The Eel Regulation set a biomass limit at 40% of Bo. The current silver eel escapement
Bcurrent, however, is estimated to be below that limit, at 6-18% (depending on the data
source used; ICES, 2013b), and Bcum-nt is unlikely to restore to 40% of Bo in the near
future; it is even more likely to decline for several years, due to the dow nward trend
in recruitment observed in the past decade. A mortality limit of E A = 0.92 w ill corre-
spond to the 40% biomass limit in the long run, but establishing/maintaining mortality
at that level in the current, depleted state will not allow the stock to recover. The ques-
tion arises what mortality limit to apply for the current, depleted state. WGEEL (ICES,
2010b) only considered an ultimate mortality limit (EA = 0.92). WGEEL (ICES, 2011a)
followed standard ICES protocols and applied a reduction in the limit mortality in pro-
portion to the biomass of the spawner escapement (setting the limit for EA = 0.92 at
Bcunent = 40% of Bo and at E A = 0 for Bcurrent = 0). The Review Group for WGEEL sug-
gested the application of criteria for short-lived stocks (ICES, 2013b), im plying E A = 0
for Bcurrent < 40% of Bo. The discussion of WKLIFE for short-lived species is not yet being
available (WKLIFE-4, November 2014), while ICES (2014) specifies a harvest control
rule for short-lived species but does not elaborate on its background. We therefore dis-
cuss the rationale for specific short-lived-species criteria, and their relevance for eel.
3.4.1 Knock-on effects o f spawning stock depletion
In short-lived species, the number of age groups in the spawning stock is low; at the
extreme, for an annual species (spawning at age 1), there is just a single year class in
the spaw ning stock. A depletion of the spawning stock in one year w ill have conse-
quences for the next year class, and because of the presence of just a single year class,
knock-on effects are to be expected for several more generations. Or conversely, an
effort to restore the stock w ill rapidly translate into a recovery of the whole stock. In
case the stock is depleted, an immediate action to reduce the anthropogenic mortality
to the lowest possible level w ill be required, to avoid knock-on effects for the coming
generations.
For eel, the spawning escapement comprises many year classes (see Section 3.6, below);
knock-on effects of current depletion/protection do not result in proportional de-
cline/recovery of the spawning stock. Instead, prolonged protection is required to in-
crease the size of the spawning stock in the long run. Section 3.72.2.2 (below) indicates
that, despite the increased level of protection in recent years, the spawner escapement
reported in 2012 actually went dow n by 4%. Knock-on effects are dampened, are
smoothed out, by the m any year classes in the silver eel run.
Joint EIFAAC/ICES/CFCM WGEEL REPORT 2014
3.4.2 Sensitivity to external or random perturbations
In addition to the effects of management actions, the spawning stock size of short-lived
species is sensitive to unpredictable extemal pertubations (e.g. environmental condi-
tions). A single year of unfavourable conditions w ill have a large effect on the spawn-
ing stock in the year(s) after. The fewer year classes in the spawning stock, the larger
the effect of an incidental low year class (though, on the other hand, the low er the num-
ber of years affected).
For eel, the spawner escapement comprises m any year classes. Additionally, recmit-
ment monitoring has shown a multi-decadal decline at a rather constant rate, perturbed
by relatively small year-to-year variation. The causing factors for the decline are not
w ell known; both, a depletion of spawner escapement from the continent and unfa-
vourable oceanic conditions have been suggested. W hatever the ultimate cause, the
long-lasting decline in recmit series indicates that short-term perturbations have had
relatively small impact.
3.4.3 Speed of recovery
The current silver eel run Bcurrent is estimated to be below the 40% limit of the Eel Reg-
ulation, at 6-18% (depending on the data source used; ICES, 2013b), and Bcurrent is un-
likely to restore to 40% in the short mn. Depending on the protocol applied, advised
mortality levels m ay range from L A = 0.92 to L A = 0. Clearly, the low er the mortality
level achieved, the faster recovery of the stock can be expected and the lower the risk
of a continued decline or worse (Figure 8.1) (though multiple generation times might
be required to achieve full recovery; Aström and Dekker, 2007). The previous Sections
(3.4.1 and 3.4.2) did not indicate biological arguments for either a low or a high mor-
tality advice. There appears to be no biological groimd for a mortality advice at low
spaw ning stock biomass (SSB < Bum), other than the ultimate limit L A < 0.92. A high or
a low mortality reference point probably is more a reflection of a low or high ambition
level. WGEEL considers that to be outside its remit.
Figure 3.1. Schematic overview of different harvest control rules.
Joint EIFAAC/ICES/GFCM WGEEL REPORT 2014
3.5 General stock-recru it relation, short-lived species protocol
ICES in 2002 advised "Exploitatíon, which provides 30% of the virgin (F = 0) spaw ning-
stock biomass is generally considered to be ... a reasonable provisional reference tar-
get. H ow ever, for eel a preliminary value could be 50%". This advice was based on
comparison of the eel to fish stocks in general and a tentative estimate based on life-
history parameters (Dekker, 2003). Subsequent analyses (Dekker, 2004; ICES, 2013b)
have indicated that the stock-recruit relatíon might actually show signs of strong de-
pensatíon and/or overwhelm ing environmental drivers, in partícular evidenced by re-
cruitment declining faster than the spawner escapement. Though neither the
depensatíon nor the effect of environmental drivers has been proven beyond doubt, it
is clear that reference points based on the data w ill be more strict than the standard
advice (30% of Bo), or even the extra precautíous level (50% of Bo).
The eel is a long-lived semelparous species. The suggestion made by the Review Group
2013 (ICES, 2013b, Annex 9) to apply a protocol for short-lived species actually contra-
dicts the real life history parameters of the eel. Stacking a non-fitting protocol, on top
of an assumed (standard) stock-recruit relatíon that is contradicted by the data would,
in the view of WGEEL, be unwise and w ould imdermine the credibility of the resulting
reference point.
3.6 The age composltion of the silver eel run escaping to the ocean
In countries where silver eel fisheries exist, catches are regularly sampled; at other
places, incidental samples have been analysed, or age distributíons have been derived
from research traps. Results vary from region to region, from river to river, within and
between the seasons, but overall, a w ide range of ages is found (Figure 3.2). In southem
regions, female silver eels tend to be relatívely young (e.g. six years in Mediterranean
lagoons; Figure 3.2), with only ten different year classes in the silver eel run. In north-
em regions, female silver eels are usually much older (e.g. 17 years in inland waters in
Sweden; Figure 3.2) with up to 20 different year classes in the catch. Overall, some
thirty age groups are regularly represented in the silver eel run from all over the con-
tinent. In additíon, there are sites showing an uncommon age composition, such as
Burrishoole in western Ireland, and sites in Scotland, where growth under oligotrophic
conditions is extremely slow, mean age of the silver eel is about 31 years, adding at
least ten extra age groups to the continental mn. Though these exceptíonal sites are
uncommon, their unusual age compositíon can be of cm cial importance, w hen consid-
ering the populatíon dynamics of the eel stock.
It is unknow n what areas contribute to successful spawning to what degree. Hence, we
are not able to provide an estímate of the number of age groups actually contributíng
to the spaw ning successfully, but it seems highly likely that a considerable number of
year classes contribute each year.
Joint EIFAAC/ICES/CFCM WCEEL REPORT 2014
Figure 3.2. Age composition of the silver eel run from a number of selected sites.
3.7 Assessment methods
3.7.1 T ren d-based assessment
3.7.1.1 Introduction and objectives for Trend-based assessment
Glass eel recruitment series are the most used to describe the status of the European
eel stock as they are w ell-known and certainly the most reliable (see for example Jacoby
and Gollock, 2014).
Trend-based assessment is a valuable and robust tool to assess stock status, especially
in data-poor situations. This kind of method has several advantages: it requires few
kinds of data, it relies on few assumptions and consequently it is quite robust, simple
and easy to understand, and harvest control rules m ay be easily defined. This kind of
approach has been implemented for various European stocks and has been w idely im-
plemented by Fisheries and Oceans, Canada (DFO, 2006) for the developm ent of the
precautionary approach, and is generally recommended by ICES for data-poor situa-
tions (ICES, 2012c).
The objective of the following text is to derive stock indicators only based on the value
and trend of abundance index (here recruitment) of the stock.
3.7 .1 .2 Method for Trend-based assessment
The recruitment series contains two important pieces of information about the status
of the stock:
• the absolute value can inform on how close or far recruitment is from a 'nor-
mal' level;
• the trend of the recruitment can inform on an improvement or deterioration
of the status of the stock.
Joint EIFAAC/ICES/GFCM WGEEL REPORT 2014
The principle of the analysis is thus to establish a reference level for the absolute value
and the trend of recruitment. For the reference value of the recruitment (Rreferenœ) the
mean recruitment of the baseline period 1960-1979 (= 1) is the most logical (see Chapter
2).
The trend is computed as the exponential trend observed during the most recent years
(0 indicates stable, positive value indicates an increase in recruitment, while a negative
value indicates a decrease). A range of periods over which the trend was calculated
w as explored and a five year period appeared to be an appropriate compromise, re-
flecting the recent evolution in recruitment while smoothing interannual variability.
Com bining both pieces of information in a status-and-trend diagram, four zones are
defined:
• green zone: if recruitment is above Rreferenœ and the trend is positive (i.e. re-
cruitment status is good and no deterioration is expected);
• yellow zone: if recruitment is above Rreferenœ but the trend is negative (i.e.
recruitment status is good but m ay deteriorate in future);
• orange zone: if recruitment is below Rreferenœ but the trend is positive (i.e.
recruitment status is bad but signs of possible improvements are observed);
• red zone: if recruitment is below Rreferenœ and the trend is negative (i.e. re-
cruitment status is bad and may deteriorate in future).
This approach is illustrated using the 'Elsewhere Europe' and 'North Sea' glass eel re-
cruitment series (Chapter 2).
3.7 .1 .3 Results on Trend-based assessment
Figure 3.3 shows the two recruitment series compared to the reference level defined
above. Both recruitment series had oscillated between the four zones during the 1960s
and the 1970s; before entering the critical zone (red) during the 1980s. Both series enter
the cautious zone (orange) in the mid-1990s. The most recent years have entered into
the cautious zone (orange), with an increasing trend in 2014 but a level of recruitment
still low compared to the reference.
Joint EIFAAC/ICES/GFCM WGEEL REPORT 2014
5 years exponential trend
o
o -
CN
o
m -
-0.4 -0.2 0.0 0.2 0.4
5 years exponential trend
Figure 3.3. Recruitment status-and-trend with respect to the four zones (green=healthy zone, yel-
low=cautious zone, orange=other cautious zone, red=critical zone) for 'Elsewhere Europe' (upper
panel) and 'North Sea' (lower panel) glass eel recruitment time-series
3.7 .1 .4 Discussion on, and management consequences of, Trend-based assessment
The recruitment is used here as a proxy of the status of the stock. To have a more com-
plete approach this method should also be applied to other life stages (yellow and sil-
ver) of the eel as soon as robust indices for these life stages become available.
This approach is quite simple and relies on the most reliable series available. However,
this kind of approach also has the disadvantages of sim plidty in that (i) it cannot be
used to make future predictions, (ii) it ignores the complex spatial structure of the
stock, and (iii) it is very difficult to explain changes using the method alone, e.g. a pos-
itive increase may be the result of appropriate management measures but may also
result from favourable environmental conditions. However, it is a good signal for stock
status.
Joint EIFAAC/ICES/GFCM WGEEL REPORT 2014
In period of stability at a 'normal' recruitment (around R t a r g e t ) the recruitment oscillated
between the four zones. This may not be a desired feature. A margin around R t a r g e t and
the 0 trend m ay solve the problem but needs to be developed.
The status-and-trend diagrams provide a comprehensive and consistent view on the
current recruitment status and evolution. Despite an increase in recent years, the re-
cruitment appears to be in critical status and far from recovery to the healthy zone.
Management actions should thus be continued as long as the recruitment is not in the
healthy zone.
3 .7 .2 Eel specific reference points based on stock recruitm ent relationship
3.7.2.1 Introduction and objectives
ICES provides fisheries advice that is consistent with the broad intemational policy
norms of the Maximum Sustainable Yield (MSY) approach, the precautionary ap-
proach, and an ecosystem approach, while at the same time responding to the specific
needs of the management bodies requesting advice (ICES, 2014). For long-lived stocks
with population size estimates, ICES bases its advice on attaining an anthropogenic
mortality rate at or below the mortality that corresponds to long-term biomass targets
( B m sy ) . BMSY-trigger is a biomass level triggering a more cautious response. Below B m sy -
trigger, the anthropogenic mortality advised is reduced, to reinforce the tendency for
stocks to rebuild. Below BMSY-trigger, ICES applies a proportional reduction in mortality
reference values (i.e. a linear relation between the mortality rate advised and biomass).
The objective of this chapter is to derive from information available the stock indicators
required to manage eel fully in the general framework setup by ICES (ICES, 2014).
3.7 .2 .2 Deriving biological reference point
3.7.2.2.1 Classical method for deriving biological reference point
B m s y is the biomass level for which the stock can be on average exploited with a maxi-
mum production (MSY) providing it is exploited at F m s y (ICES, 2014; Figure 3.4). To
determine this level the production (yield) should be related to the stock size (B)
through fisheries mortalities (F) through the production function.
In the case of eel, fisheries are scattered throughout Europe in small scale fisheries tar-
geting glass eel and/or yellow eel and/or silver eel (Dekker, 2000; 2003). Moreover, un-
like other marine species, eel is suffering the impact of many other anthropogenic
mortalities (pollution, obstacle to migration, etc.). For these reasons, and given the cur-
rent knowledge, it is impossible to sim ply and reliably determine the production func-
tion and thus derive MSY, B m s y and F m sy .
ICES (2014) also define biological reference points based on the precautionary ap-
proach to avoid a significant risk of impaired reproduction. B u m is defined as "the stock
size below which there may be reduced reproduction resulting in reduced recruit-
ment". B p a is the precautionary reference point derived from B u m by adding a safety
m argin to take into account the uncertainty in stock estimates and to avoid reaching
B l i m .
Joint EIFAAC/ICES/GFCM WGEEL REPORT 2014
Biomass Reference Points
♦
♦
M S Y B trigger
or ♦ ♦
® p a
or
♦ MSYB escapement
I1111 ♦1
iiiiiiii
♦♦1
■1iii
ý \/ ý
lim 200 300 B msy 400 500
S S B
Figure 3.4. Illustration of biomass-based biological reference points. Biim and Bpa are precautionary
reference points related to the risk of impaired reproductive capacity, while MSY Besupemcnt often
equal to Bpa is used in the advice framework for short-lived species. MSY Bwgger is the parameter in
the ICES MS Y framework which triggers advice on a reduced fishing mortality relative to F m sy . B m sy
is the average biomass expected if the stock is exploited at F m sy . Diamonds show the variable re-
cruitment versus SSB that have been observed over the years. Recruitment can be seen to be gener-
ally lower below Biim. (ICES, 2014).
Biim can be determined by the examination of the stock-recruitment relationship.
The recruitment used here for illustrative purposes is the 'Elsewhere Europe' series of
glass eel recruitment (Chapter 2), pending the combination of this and the 'North Sea'
series.
The actual spaw ning-stock biomass (in the Sargasso Sea) has never been observed. The
best available proxy is the silver eel escapement that exists after all of the fisheries and
other mortalities (both natural and anthropogenic) in the continental and littoral wa-
ters have occurred. This can be derived from the landing statistics as explained in ICES
(2013b), and used here again in the absence of new data.
The Ricker model presents an overcompensation that leads to a maximum production
at an intermediate level of SSB (Ricker, 1954). The Beverton and Holt model presents a
compensation for high recruitment. In that case, for high SSB, the recruitment does not
increase as fast as the SSB (Beverton and Holt, 1957). Both Ricker and Beverton-Holt
have maximum recruits per spawner at the origin, declining monotonically with in-
creasing spawner abundance, and recruitment increases faster than SSB for SSB less
than the value for maximum gain.
The hockey-stick model is a simplification of these models corresponding to a one-
breakpoint segmented regression with the first segment passing through the origin and
the second being horizontal and corresponding to a plateau. This last model assumes
Joint EIFAAC/ICES/GFCM WCEEL REPORT 2014
that recruitment is independent of SSB above some change point, below which recruit-
ment declines linearly towards the origin at lower values of SSB.
The fitting of these three models of stock-recruitment relationship to the 'Elsewhere
Europe' glass eel recruitment index w as tested using the Akaike Information Criterion
(AIC) (Akaike, 1974).
The A IC for each model (Table 3.1) show no strong preference for one or the other
model. Figure 3.5 shows the result of the hockey-stick model. The breakpoint is at the
very high biomass (> 40 000 tonnes).
B Current(1 0 0 0 t O nne S)
Figure 3.5. Hockey-stick regression between proxy for European eel spawning-stock biomass
(proxy silver eel escapement: estimated Bcurrem) and recruitment index between 1950 and 2010. Two-
digit labels indicate the years of silver eel escapement, recruitment occurs two years Iater; the
dashed lines indicate 95% confidence interval. Note the breakpoint in the regression line at the far
right, at B = 43 000 tonnes.
According to the hockey-stick model, the stock has virtually never been above the Bum
(the breakpoint) since 1950. However, such a relationship provides an unrealistic fit to
the data: observed recruitment has been below that predicted by the model ever since
1995 but nearly a lw ays above in the 1960s and 1970s. These difficulties m ay also be due
to unreliable SSB (or R) data. They are derived from landings data and expert
know ledge about the exploitation rate (ICES, 2013b). There are m any gaps and uncer-
tainties in these data.
3.7 .2 .2 .2 Method for deriving eel-specific biological reference points
G iven these limitations, it is difficult to derive any biological reference points using
classical approach, but the S-R relationship remains a key function for the study of
population dynamics in a perspective of management advice. It w as thus dedded to
design an eel spedfic analysis to better take into account of the existing data.
Instead of fitting an imposed form of stock-recruitment, a data-driven method is de-
signed follow ing Dekker (2004) and ICES (2012b). A G A M (General Additive Model:
Hastie and Tibshirani, 1990) is fitted on the same data used for the classical approach,
using a cubic spline smoother of order 3 for the SSB.
Joint EIFAAC/ICES/CFCM WCEEL REPORT 2014
This kind of model allows the incorporation of factors that m ay directly affect this S-R
relationship. To illustrate this possibility, a G AM is fitted with a linear effect of the
year, to test for a progressive change in S-R relationship like a degradation of the re-
productive efficiency, and a smoothed effect of North Atlantic Oscillation (NAO) (av-
erage of monthly mean N A O indices (http://www.noaa.gov/) during the two years
between escapement and recruitment); as a proxy of oceanic condition.
Figure 3.6 illustrates the result of this G AM (AIC -25.73) and Figure 3.7 shows the GAM
that included the year and N A O effects (AIC -31.66). These curves show two points of
inflexion, the first for low value of biomass (about 15 000 tonnes) and a second at inter-
mediate value (about 30 000 tonnes).
x
<D
TD
C
■*—>
C.
<D
E
o
<D
Cd
10 20 30
BCurrent(1000 tons)
40
Figure 3.6. Illustration of European eel stock-recruitment relationship fitted by a GAM.
http://www.noaa.gov/
Joint EIFAAC/ICES/CFCM WGEEL REPORT 2014
X
0~o
o
c
0
E
o
0a:
0 10 20 30
^current (1 0 0 0 t o n s )
40
Figure 3.7. Illustration of the GAM fitting for recruitment with a year effect and smoothed effect of
spawning-stock biomass and NAO index. Since the stock-recruit relationship depends not only on
the current biomass Bcumcnt, but also on extemal covariates (i.e. NAO), predictions (regression lines)
can be generated for the whole range of biomasses, for different values of the NAO-index. The
graph provides predicted regression lines, spanning the data range in recruitment indices and the
range in NAO values.
Com parison of A IC values suggests that curves fitted with G AM perform better than
classical S-R relationship.
The right-hand part of the G A M fit is very similar to a Ricker curve. If w e mimic the
G A M fitting w ith a two-breakpoint curve (AIC = -24.28), the limit biomass is foimd at
27 800 tonnes (95% confidence interval: 23100-33 500 tonnes) that is 14% Bo (as estimate
by sum m ing estimates delivered by each EMU, resulting in a value of 193 000 tonnes).
However, the left-hand part of the G A M fit is unusual: it w ould suggest that when the
spaw ning biomass decreases, the recruitment is lower than w ould be expected w ith a
classical relationship. This effect is known as an Allee effect (Allee, 1931) and in the
fisheries literature as depensation (Hilbom and Walters, 1992). It can seriously acceler-
ate population decline and drive a population to extinction, or at least heavily hinder
its recovery (Walters and Kitchell, 2001).
This notion can be further developed by plotting in the same figure the 'pristine' re-
placement line for L A = 0, as determined by the line crossing the origin and the point
of coordinates Bo, pristine recruitment (Ro). In our example, the Ro is approximated by
the mean recruitment of 1960-1979 (1 by definition). In this case, the pristine replace-
ment line is above the stock-recruitment relationship at low values of recmitment (Fig-
ure 3.8). In such circumstances, recruitment w ould produce fewer spawners than the
previous generation, even in the absence of any anthropogenic mortalities.
Joint EIFAAC/ICES/CFCM WGEEL REPORT 2014
By definition, where the lower confidence bound of the S-R relationship crosses the
replacement line, the probability of a recruitment that cannot replace the current bio-
mass is a = 5%. Where the mean predicted recruitment crosses the replacement line,
there is a 50% chance of further deterioration. We label the biomass resulting in a mean
predicted recruitment equal to the replacement line as BstoP/ and the biomass at which
the 5% low er boimd crosses the replacement line as Bstoppa.
In our example, BstoPPa w ould be at 18 900 tonnes and BstoP w ould be 13 200 tonnes.
(Figure 3.8), biomass w ould have been below Bstoppasince 1998, and current escapement
has remained close to Bstop since 2005.
Taken at face value (see below) the BstoPPa reference point w ould have suggested a min-
im izing of all anthropogenic mortality to zero, 15 years ago, and a high risk that the
stock w as in the depensatory trap from 2005.
<D■o
c
c<u
E
0>a:
10 15
BcurrentOOOO tonnes)
20 25 30
Figure 3.8. Stock-recruitment relationship fitted by a GAM and 'pristine' replacement line. For B stop
and Bstoppa explanation, see text.
The recent increase of recruitment may appear contradictory w ith a stock in a depen-
sation trap. Our analyses are based on estimate of SSB derived from landings data and
expert know ledge about the exploitation rate (ICES, 2013b). M oreover Bo is the sum of
data provided by countries and taken at face value. They are m any gaps and uncer-
tainties in these data, and any change in these m ay produce different curve and lead to
different conclusion.
A t this time, however, it is difficult to link this increase to a change in silver eel escape-
ment (our proxy for spawner biomass). Based on the data provided by the Member
States in their first EMP progress reports in 2012, no improvement of silver eel escape-
ment could be detected shortly after the implementation of the EMPs (Table 3.2). In
fact, a comparison of the available data on silver eel escapement of 2010 (after imple-
mentation of the EMPs) and 2008 (before the implementation) suggests a decrease of
4.3% (-544 tonnes). Noting the many uncertainties in the assessments (ICES, 2013a), it
is unclear whether this is within confidence limits of the estimates or not. However,
the recent increase in recruitment does not correspond to the reported trend in silver
Joint EIFAAC/ICES/CFCM WCEEL REPORT 2014
eel escapement, whether assuming a three or four year- interval between silver eel es-
capement and corresponding glass eel arrival.
A n improvement in environmental condition m ay produce, temporarily, higher re-
cruitment than expected. Besides, this increase is not yet fully consider as a trend shift.
Note also that the last recruitment data are not yet place in these figures. Finally the
observed data m ay be explained by other phenomenon like regime shift due to ocean
change, decrease of recruitment efficiency due to spawner quality, etc.
However, these are the best data available to the working group at this time. Even
though no firm conclusions can be drawn on the existence of a depensatory stock-re-
cruitment relationship, due to flaws underlined above, the managers should consider
this phenomenon as being possible for eel and even that eel is already in the depensa-
tion trap. This latter hypothesis w ould urge an immediate and complete reduction of
all anthropogenic impacts (fisheries and other impacts) to zero.
3.7.3 Quantitative assessment applying generic reference points
3.7.3.1 Method
"The ICES approach uses both fishing mortality rates and biomass reference points"
(ICES, 2014).
The Eel Regulation specifies a Iimit reference point (40% Bo) for the biomass of the es-
caping silver eel, but does not specify a mortality limit. That is: the endpoint of the
recovery process is specified, but not the route (the time required, the speed of recov-
ery) towards that point. However, a mortality limit (above the 40% Bo) of lifetime mor-
tality L A = 0.92 can be shown to correspond to the 40% biomass limit (Dekker 2010;
ICES 201 la; 201 lb). The Eel Regulation, however, does not indicate what approach
should be made to rebuild the stock (or correspondingly, what time-scale for rebuild-
ing the stock is acceptable). For ICES, it will be in-line with its existing advice policy to
recommend a linear reduction in mortality below the 40% limit adopted by the EU.
Since it is very difficult to derive biological reference points (BRP) from eel data using
classical methods (see above), w e here consider using these reference points derived
from the EU eel regulation.
In the 2010 Report of ICES Study Group on Intemational Post-Evaluation of Eel (SGI-
PEE) (ICES, 2010a), a pragmatic framework to post-evaluate the status of the eel stock
and the effect of management measures was designed and presented, including an
overview of potential post-evaluation tests and an adaptation of the classical ICES pre-
cautionary diagram to the eel case. In the 'classicaT Precautionary Diagram, annual
fishing mortality (averaged over the dominating age groups) is plotted vs. the spawn-
ing-stock biomass. In the 'm odified' Precautionary diagram, lifetime anthropogenic
mortality E A (or the spawner potential ratio %SPR on a logarithmic scale) is plotted
against silver eel escapement (in percentage of Bo). This 'm odified' diagram allows for
comparisons between EMUs (%-wise SSB; lifetime summation of anthropogenic mor-
tality) and comparisons of the status to limit/target values, while at the same time al-
low ing for the integration of local stock status estimates (by region, EMU or country)
into status indicators for larger geographical areas (ultimately: stock wide).
In 2012, EU Member States post-evaluated the implementation of their Eel Manage-
ment Plans, and provided estimates of national stock indicators; the '3Bs & E A ' (Bcurrent,
Bbest, Bo & EA) for before, and since implementation of their EMPs (putatively 2008-
2012). ICES (2013a) reviewed those progress reports, concluding that information was
Joint EIFAAC/ICES/GFCM WGEEL REPORT 2014
not alw ays completely reported or available, and the quality of the national data and
assessment were hard to evaluate. Subsequently, the WGEEL decided to use the re-
ported stock indicators in good faith, but recognising that their quality needs to be as-
sured in the future.
3.7.3.2 Results
Since not all countries have reported (and not for all years from 2009 onwards), the
presented stock-wide sum represents the reporting countries; not all countries within
the distribution area, and not even all countries within the EU. Moreover, the set of
countries reporting indicators has changed over the years; therefore, the sum of report-
ing countries cannot be compared between the years. WGEEL decided to restrict the
graphical presentation to the latest data year, 2011. In some countries, additional man-
agement measures have been taken in 2012 (e.g. Sweden closing the fishery in SE-west),
but these have not been considered in this report.
The diagrams present the indicators per EMU (Figure 3.9; top), and per country (Figure
3.9; bottom); each plot also contains the Sum of tlre reported areas. Some countries (no-
tably France) did not report all stock indicators for each EMU (in particular Bo), but did
so for the country as a whole. Thus, France is not represented in the top plot, but it is
in the bottom, and continent-wide sums differ between the plots. The difference in out-
comes between the plots emphasizes the importance of a consistent and full-coverage
set of stock indicators.
Finally, Figure 3.10 presents the status of each EMU in relation to the m odified Precau-
tionary Diagram (i.e. the background colour that applies to the zone where the EMU
bubble sits in the m odified Precautionary Diagram) in a map, where data-defident ar-
eas have been shown by a ©. This map indicates that major areas have not assessed
their part of the stock; while the sum of the reporting countries is far aw ay from the
required stock-wide total.
Joint
E
IFA
A
C
/IC
E
S/C
FC
M
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CEEL
REPORT
2
0
14
Joint EIFAAC/ICES/CFCM WGEEL REPORT 2014
4
10
Spawner escapement, percent8ge of pristine (%)
Figure 3.9. Modified Precautionary Diagram, illustrating the method to examine the status of the
European eel stock (horizontal, spawner escapement expressed as a percentage of the pristine es-
capement) and the anthropogenic impacts (vertical, expressed as lifetime mortality ZA). Data are
those reported in the 2012 progress reports (ICES 2013a). The size of the points (bubbles) indicates
the size of B b cs t, while their location indicates the status of eel in the EMU in terms of spawning
biomass against the 40% target, and anthropogenic mortality against the rate equivalent to that bi-
omass target (i.e. LA = 0.92 if B m rrcn t >40% Bo or EA = 0.92 * B c u r r e n t / ( 4 0 % Bo) if Bcun-ent <40% Bo). Green
indicates the local stock is fully compliant, amber indicates that one target is reached but not the
other, and red indicates that neither target is reached. In most cases, the 2011 indicators are shown;
when these were missing, the 2010 indicators are used. Top: stock indicators by EMU and for the
sum of the reported EMUs (59 EU-EMUs are missing); bottom: stock indicators by country and for
the sum of the reported countries (26 EU and no-EU countries are missing). Note that non-reporting
EMUs/countries do not show up in these plots.
Joint EIFAAC/ICES/CFCM WCEEL REPORT 2014
Figure 3.10. Stock indicators from the modified Precautionary Diagram (Figure 3.6), plotted on the
location of their EMU. The size of each bubble corresponds to B b est, the biomass of escaping silver
eels if no anthropogenic impacts had affected the current stock. The colour of each bubble corre-
sponds to the position of the indicators, relative to the reference limits of the modified Precaution-
ary Diagram (the background colour in Figure 3.9, above). For EMUs/countries that did not report
their stock indicators (or incompletely), a © of arbitrary size is shown. Data from the 2012 progress
reports (ICES 2013a). In most cases, the 2011 indicators are shown; when these were missing, the
2010 indicators are used. For France, indicators have only been reported for the country as a whole,
not for the constituting EMUs; that country-total is shown (shaded red), along with the EMUs (®).
3.7 .3 .3 Discussion on and consequences for management
The reference points taken here are those derived from the EU eel regulation, data are
those reported by country and taken at face value and some country/EMU have not
fully provided data. Am ong non-reporting countries, some have not involved in a
stock recovery process. Keeping these limitations in mind, the stocks can be assessed
as not within sustainable limits conforming to the Eel Regulation and ICES policies.
For those EMUs that reported, the overall escaping biomass is 18% of Bo (cf EU limit
40% Bo) and the anthropogenic mortality (EA) is 0.41 compared to the limit of 0.42. For
countries that reported (so including those that reported at country but not EMU lev-
els), the overall escaping biomass is 6% Bo, and the anthropogenic mortality (EA) is
1.40 compared to the limit of 0.14.
Management actions should thus be continued and even amplified for some
EMUs/countries until their mortality is decreased below the reference point and ulti-
mately that their biomass increases above the limit biomass.
3.8 A provisional harvest control rule for eel
Assessment of the eel stock is not an easy task: because crucial knowledge of basic
biological characteristics is incomplete; because the stock is scattered over an extremely
large area, in typically small-scaled habitats; because the impacts vary from area to
area; and because the stock has experienced a multidecadal decline and is now at a
very low level.
Joint EIFAAC/ICES/CFCM WCEEL REPORT 2014
Three complementary approaches to the eel assessment are presented having their
ow n advantage and flaws. They all underline the bad status of the eel stock (recruit-
ment and biomass), despite the encouraging recent increase in recruitment. The trend-
based approach w ould lead to the conclusion that management actions should be con-
tinued as long as the recruitment is not in the healthy zone. The classical approach
w ould lead to the conclusion that already taken action are not suffident at least in some
EMUs/countries. The eel specific approach w ould lead to an eel stock possibly in a
depensatory trap that required an immediate and complete reduction of all anthropo-
genic impacts (fisheries and other impacts) to zero. It can thus be concluded that a min-
ima management actions should be continued if not amplified.
In 2012, ICES convened WKLIFE (ICES, 2012d), to investigate the feasibility of devel-
oping m ethodology for providing assessments and advice on data-deficient stocks.
WKLIFE, however, did not include the assessment of the European eel in its consider-
ations, because "ICES does not have an accepted time-series of stock-wide catch for
eel". In 2013, the Review Group for WGEEL (ICES, 2013a) nevertheless suggested the
application of WKLIFE's criteria for short-lived stocks. In Section 3.4, the rationale for
applying those criteria have been discussed, concluding that there is no biological ar-
gument for applying those criteria.
WKLIFE considers seven types of stocks (Table 3.3), none of which strictly applies to
eel. Rather than enforcing one of these categories on the eel, WGEEL recommends de-
veloping a category for eel on its own. Unlike all other stocks, there is no realistic option
to develop a single, stock-wide assessment based on primary data. Instead, WGEEL
has developed an approach for an international assessment, in which only national
stock indicators are used (Dekker, 2010; ICES 2010a,b; 2011a,b; 2012b; 2013b). Hence,
the intemational stock assessment is based on national data only through the national
stock indicators, not directly on the data themselves. This cascaded approach enables
the assessment of the state of the stock in individual EMUs, allows to contrast indices
of spawner escapement and total anthropogenic mortality to agreed reference points
for these EMUs, and provides the information for the analysis of the stock-recruitment-
relation and environmental drivers. Until complete spatial coverage has been achieved,
the stock-recruit analysis is hampered by incomplete data.
ICES in 2002 provided advice on a minimum limit to the spawning stock ("Exploita-
tion, which provides 30% of the virgin (F=0) spawning-stock biomass is generally con-
sidered to be [...] a reasonable provisional reference target. However, for eel a
preliminary value could be 50%.").
In the Eel Regulation, EU decided to adopt a limit of 40%, that corresponds to a mor-
tality limit LA um = 0.92 w hen Bcunent > Bum. According to the Regulation, this reference
point applies to all Eel Management Units, irrespective of the achievements in other
Eel Management Units or the status of the stock as a whole.
A s indicated above (Section 3.4.3), there is no biological argument to adopt a specific
harvest control rule for EA when Bcummt < Biim. Analysis (Section 3.7.2.2.2) of the availa-
ble data, however, indicates that current recruitment might be insufficient to replace
current spawner escapement, and severe management actions might be required im-
mediately. H owever, the quality of the data and hence the reliability of the analysis are
not beyond doubt, and the working group recommends substantial steps forward, im-
proving the database as w ell as the comprehensiveness of the analysis (below).
A s the WGEEL considers the European eel to be a long-lived species in relation to har-
vest control rules, and pending an improvement of the analysis of stock-and-recruit
Joint EIFAAC/ICES/GFCM WGEEL REPORT 2014
data, W G E E L recommends that I C E S provides advice on the basis of the harvest con-
trol rule for quantitative assessments (category 1), i.e. a proportional reduction in E A iim
beloW Blim down tO E A lim = 0 at Bcurrent = 0.
Future developm ent priorities
In this chapter, the (potential) relation between the size of the spawning stock and the
subsequent year-class strength has been analysed, extending the analyses in previous
working group reports. To this end, an index of the spawning stock was derived (pro-
portional to the landings (Dekker, 2004; ICES, 2012b); proportional to the landings tak-
ing into account an expert estimate of the relative fishing pressure over the decades
(ICES, 2013b)). It is well acknowledged that other factors - including spawner quality,
ocean climate and conditions in the spawning area - might have an influence too (ICES,
2008). However, few studies have attempted to analyse more than one factor at a time
(Dekker 2004; ICES, 2013b). Hence, different views on the causes of the recruitment
decline exist, but no progress is actually made towards a comprehensive analysis.
Looking forwards, therefore, the working group recommends:
• an existing or new workshop is requested to compile and make available
time-series of indices of eel quality, preferably from 1950 forward;
• a workshop on ocean climate indices relevant to the eel (WKOCRE), in co-
operation with the working group on oceanic hydrography (WGOH) is or-
ganized, to compiles and make available time-series of indices that might
relate to the survival of spawners and/or larvae in the ocean;
• that WGEEL makes available time-series of (reconstructed) spawner escape-
ment and documents how these time-series have been derived; consider sil-
ver eel run reconstructions to be based on either silver eel landings data,
yellow eel landings data, or other historical sources of information;
• that a workshop/study group (i.e. one or 2-3 years?) is established to analyse
the stock-recruitment relation for the European eel, taking into account the
potential effects of spawner quality and ocean climate indices.
Jo in t EIFAAC/ICES/CFCM WGEEL REPORT 2014 | 81
3 .10 Tables
Table 3.1. AIC for attempts to fit three stock-recruitm ent m odels to yElsewhere Europe' glass eel
recruitment index. Smaller values of AIC indicate a better fit.
P a r a m e t e r n u m b e r AIC
Ricker 2 28.68
Beverton 2 29.08
Hockey stick (one-breakpoint) 2 29.04
GAM 3 -25.73
GAM + year + NAO 5.8 -31.67
Table 3.2. A com parison of silver eel escapement of the years 2008 (prior to the im plem entation of
EMPs) and 2010 (after im plem entation of the IMPs). In the case of Poland, the Netherlands, Bel-
gium and Spain (marked in red), post-im plem entation data were only available for 2011, in the case
of France (marked in blue) only for 2009.
B c u r re n t
2 0 0 8 (T)
B cu r re n t
2 0 1 0 (T)
D iff (t )
2 0 1 0 /2 0 0 8
%Diff
2 0 1 0 /2 0 0 8
SE 3463 3533 70 2.0
FI
EE
LV 1.7 1.7 0 0.0
LI 7.1 14.6 7.5 105.6
PL 469 199 -270 -57.6
CZ
DE 2192 1919.2 -272.8 -12.4
DK 129.5 129.5 0 0.0
NL 439 482 43 9.8
BE 49 48 -1 -2.0
LU
IE 142.6 216.4 73.8 51.8
GB 1707 1588.2 -118.8 -7.0
FR 2574.4 2234.6 -339.8 -13.2
ES 1173.7 1421.3 247.6 21.1
PT
IT 269 285.5 16.5 6.1
GR
Total 12 617 12 073 -544 -4.3
Table 3.3. Generic categorization of stocks by WKLIFE and its applicability for eel assessm ents.
82 | Joint EIFAAC/ICES/GFCM WGEEL REPORT 2014
WKLIFE CATEGORY Q u a l if y in g c r it e r ia A p p l ic a t io n t o eel
Category 1 - data rich
stocks (quantitative
assessments)
full analytical assessments
and forecasts
Partial spatial coverage; assessments
for some areas incomplete
Category 2 - negligible
landings stocks
landings are negligible in
comparison to discards
In cases where eel is caught as a
bycatch, it is m ost often retained;
when retumed to the water, survival
is usually high.
Category 3 - stocks
w ith analytical
assessm ents and
forecasts that are only
treated qualitatively
assessments and forecasts
which for a variety of
reasons are merely indicative
of trends in fishing
mortality, recruitment and
biomass
Partial spatial coverage, known trends
in mortality and biomass need not be
indicative for un-assessed areas.
Category 4 - stocks for
which survey-based
assessm ents indicate
trends
survey indices are available
that provide reliable
indications of trends in total
mortality, recruitment and
biomass
N o such stock-wide surveys exist,
other than the recruitment surveys,
which are considered to be
representative for larger regions.
Category 5 - stocks
for which reliable
catch data are available
for short time-series
catch curve analyses can be
undertaken and an estimate
of exploitation provided
Catch-curve analyses are not wide-
spread, and need not at all be
indicative for other areas.
Category 6 - data-
limited stocks
only landings data are
available;
Following the implementation of the
Eel Regulation, much more detailed
data have become available. Life-
history-parameter-based assessments
for the eel vary from region to region.
Category 7 - stocks
caught in minor
amounts as by-catch
primarily caught as by-catch
species in other targeted
fisheries
Eel is most often the target species of
its fisheries
Jo in t EIFAAC/ICES/GFCM WGEEL REPORT 201 4
4 ToR c) Overview of available data and gaps for stock assessment
4.1 Introduction
Chapter 3 highlights the range of data (at various geographic scales) required for the
various stock assessment methods, and the fact that much of these data are not yet
available to the working group and therefore elements of the assessment of whole-
stock status remain uncertain. To facilitate the collection and reporting of these data,
the following chapters of this report summarise the required, available and missing
data (with reference to the methods discussed in chapter 3), consider a range of meth-
ods available for the provision of such data, and means by which this provision can be
improved.
4 .2 Consideration o f data required
4.2.1 Stock assessment
The data requirements for eel stock assessment at national and international have been
previously discussed and summarized by the ICES Workshop on Eel and Salmon DCF
Data (ICES, 2012a). Generally, the data required for the assessment and management
of European eel fall into three broad categories:
• Data requested by ICES to undertake annually recurring intemational as-
sessment;
• Data requested by ICES or another scientific/ technical review group to pe-
riodically (2012, 2015, 2018, 2024, and every six years thereafter) establish
stock reference points, post-evaluate the Eel Regulation and implementation
of EMPs; and
• Data required by Member States to determine silver eel escapement levels
relative to the target set out in the national EMPs and undertake river-spe-
cific stock assessments according to EMPs. (Even though these data are used
for the local stock assessment, they form the basis for the next level, the in-
temational stock assessment. Therefore they are included here.)
The general framework for intemational stock assessment and post-evaluation in Eu-
ropean eel has been established and discussed in previous reports, and further devel-
oped here in Chapter 3. In principal, the approach of the intemational assessment
consists of the post hoc summing up of stock indicators, based on estimates for:
• Bcurrent, the amount of silver eel biomass that currentlv escapes to the sea to
spawn, corresponding to the assessment year;
• Bo, spawner escapement biomass in absence of any anthropogenic impacts
('pristine');
• Bbest, spawner escapement biomass corresponding to recent natural recruit-
ment that would have survived if there was only natural mortality and no
stocking, corresponding to the assessment year;
• E A , the sum of anthropogenic mortality rates, i.e. L A = E F (the fishing mor-
tality rate, summed over the age groups in the stock.) + L H (the anthropo-
genic mortality rate outside the fishery, summed over the age groups in the
stock) or % S P R , the ratio of actual escapement B cunent to best achievable
spawner escapement Bbest. S G I P E E ( I C E S , 2011b) indicated that estimates of
either L A or % S P R usually refer to anthropogenic impacts in the most recent
Joint EIFAAC/ICES/GFCM WCEEL REPORT 2014
year, not to impacts summed over the life history of any individual or cohort
in the current stock.
At present, the international stock assessment is based on national data only through
the national stock indicators, not directly on the data themselves. The approach of re-
gional stock assessment and post-hoc summing up of indicators for total stock assess-
ment appears to be more pragmatic then a "central assessment". Most of the necessary
monitoring structures and data should be available at the EMU level, and the interpre-
tation of the results is easier. Additionally, the local assessments at EMU level are re-
quired for post-evaluation of EMPs. Member States have been and are requested to
report the indicators in their EMP reviews, along with data on the amount of glass eel
recruiting to continental waters. The associated country data currently requested by
ICES through the annual stock 'assessment' report to WGEEL are, where appropriate:
• Quantity of glass or yellow eel recruitment, derived from commercial or rec-
reational fisheries, or fisheries-independent surveys (further explained be-
low);
• Catches and landings by EMU, stage (yellow, silver eels), gear, commercial
and recreational, and marine fisheries, and length frequency;
• Catches and landings of eel <12 cm by EMU, with proportion retained for
restocking and destination;
• Quantity and origin of eel restocked, by glass eel, bootlace or ongrown;
• Aquaculture production weight of eel, distinguishing between that sold for
stocking versus sold for consumption, quantity and source of seed;
• Fishing capacity by EMU, e.g. number companies, boats, fishermen, by stage
(glass, yellow, silver) and by marine fisheries;
• Fishing effort by EMU, e.g. number licences fished, number of net nights, by
stage (glass, yellow and silver) and by marine fisheries;
• Catch per unit of effort (cpue) for commerdal and recreational fisheries, by
EMU, stage (glass, yellow, silver) and for marine fisheries;
• Other anthropogenic impacts (non-fisheries), including type and quantity of
impact, e.g. turbines - mortality rate and amount of silver eel killed in
tonnes;
• Scientific surveys of the stock: abundance of recruitment, yellow eel stand-
ing stock, silver eel, by sampling method;
• Catch composition by age and length, for commercial catches and sdentific
surveys, by sub-catchments, catchments or EMU;
• Other biological sampling to inform biological characteristics, e.g. length,
weight and growth, parasites and pathogens, contaminants and predators,
by sub-catchments, catchments or EMU.
Jo in t EIFAAC/ICES/GFCM WGEEL REPORT 201 4
In addition to the aforementioned stock indicators, ICES (2012b) requested the follow-
ing data by EMU:
• Wetted area habitat, by water type (lacustrine, riverine, transitional and la-
goon, coastal);
• Production values per unit area, e.g. kg/ha.
• R(s*) The amount of eel (<20 cm) restocked into national waters annually.
The source of these eel should also be reported, at least to originating Mem-
ber State, to ensure full accounting of catch vs restocked (i.e. avoid 'double
banking').
(Note that R(s*) for restocking is a new symbol devised by the WKESDCF to differ-
entiate from "R" which is usually considered to represent Recruitment of eel to con-
tinental waters.)
4.2.2 Data needs for stock-recruitment relationship
4.2.2.1 Recruitment
Information on recruitment is essential to follow up natural variations and results of
management actions over the area of distribution of the European eel. Recruit surveys
(glass eel, young yellow eel) are the prime source of information on the status of the
oceanic reproduction. Even though they play a minor role in the national assessments,
these are essential to the overall evaluation of the Eel Regulation. Before the 3B and EA
approach had been established, the ICES stock assessments of European eel has been
based largely on examining trends in glass eel and yellow eel recruitment time-series.
These time-series have consisted of a combination of fisheries-dependent and fisheries-
independent data on both glass eel and young yellow eel stages. It was cautioned al-
ready by the WGEEL (ICES, 2008) that data discontinuities, particularly related to data
from commercial fisheries, can be expected following implementation of EMPs (e.g.
management measures affecting fishing effort, season quota, size limits), and CITES
restrictions, although at that time it was unknown to what extent this might impact on
the dataseries. Loss of monitoring sites was highlighted already by SGIPEE (ICES,
2010a). Several fishery dependent time-series were lost due to restrictions of the fishery
and for other reasons. The present availability of recruitment series for the calculation
of the recruitment index series is also given in Chapter 2.
It is vital that the existing recruitment time-series are maintained in order to provide
consistent baseline intemational assessments. ICES (2012a) therefore recommended
that eel recruitment time-series identified by ICES as contributing to the annual inter-
national stock assessment process should be included in the new version of the Data
Collection Framework (DCF, formally going to be known as DC-MAP). SGIPEE (ICES,
201 Oa) pointed out that the absence of any intemationally driven requirement to main-
tain a recruitment dataseries needed to be corrected and highlighted the recommenda-
tions of WGEEL (ICES, 2008) and EU Contract 98/076: Establishment of an international
recruitment monitoring system for glass eel. Furthermore, SGIPEE (ICES, 201 Oa) rec-
ommended that efforts to establish time-series for glass eel in non-EU countries (e.g.
Norway, Turkey, Egypt, Tunisia, and Morocco) should be continued.
Joint EIFAAC/ICES/GFCM WGEEL REPORT 2014
Recruitment data required
• Location of data collection
• Stage and size of eel
• Indicator data collected (numbers, biomass)
• Capture and sampling method
• Time-series
• Capture effort
In addition to the typical stock assessment efforts on the continental life stages of eel,
standardized larval surveys as carried out by Germany in 2011 and Germany and Den-
mark in 2014 (Hanel, pers. comm.; Hanel et al.r 2014) with a clear target on monitoring
and evaluating eel leptocephali (or egg) densities in the Sargasso Sea need to be con-
tinued on a regular basis to enable more immediate detection of changes in reproduc-
tive success and possible spawning-stock biomass than can be achieved by monitoring
medium- and longer-term trends in continental recruitment. In the long run, such data
may also help to explain variations or apparent inconsistencies in the stock-recruit-
ment relationship. Therefore, ICES (2012a) recommended that the new DCF (-MAP)
supported the need for intemational surveys at sea of eel in the spawning area in the
Sargasso Sea.
4.2.2.2 Spawning stock
Whereas a rather well accepted recruitment series exists for the European part of the
eel distribution area, information on spawner stock biomass is limited. The actual
spawning-stock biomass (in the Sargasso Sea) has never been observed. The best avail-
able proxy is the escapement of silver eels that exists after all of the fisheries and other
mortalities (both natural and anthropogenic) in the continental and coastal waters have
occurred.
For present and future reports according to EU Regulation 1100/2007, Member States
will provide the best estimate of silver eel escapement for each EMU. However, no
direct estimate of historical escapement at the stock scale is available. Therefore,
WGEEL (ICES, 2013b) attempted to reconstruct a time-series of escapement for the past
60 years from proxy data. The idea is to use the landings, prioritizing the silver eel
fishery since they are the closest to the escapement. If it is not possible to use silver eel
data, information from the yellow eel fishery may be used, although it will complicate
the procedure. The methodology for the estimation of silver eel escapement from land-
ings data has been discussed in ICES (2012b; 2013b).
In the previous attempts to reconstruct historic silver eel escapement for the whole
stock, several shortcomings were noted.
So far, only EMUs or countries could be considered that provided both catches and
Bcurrent. If either of these data had not been available, the EMU/country was not taken
into account in our estimate. One should notice that some EMU/countries with high
stock and/or catches have thus been left out (e.g. Norway, marine part of Denmark,
Portugal and North Africa).
Of further considerable concem for predicting this relationship is whether significant
changes in effort or gear have occurred. Such changes would affect the relation be-
tween landings and escapement if the expert-supplied exploitation rate estimates do
not account for this.
Jo in t EIFAAC/ICES/CFCM WCEEL REPORT 2014
WGEEL (ICES, 2012b) still noted, despite some improvements, a considerable degree
of heterogeneity and unreliability in the landings dataseries. It has hence to be con-
cluded that if the WGEEL continues to develop the stock-recruitment relationship us-
ing these methods, it is of utmost importance that catch series are improved and that
the splitting of these data by stage is also improved. The work on estimates of yellow
eel landings should be continued as well because these may provide proxies for silver
eel from missing ecoregions.
The data requirements for (improved) establishing of the stock-recruitment relation-
ship can thus be summarized as follows:
• Increase the amount of information available (all countries constituting eel
habitats should deliver the stock indicators and landings data).
• Provide data for all relevant habitats. If necessary develop habitat-specific
assessment methods.
• Increase reliability and homogeneity of landings data, including a standard-
ization of methods at least to some degree (e. g. regional standardization or
standardization within a subset of methods).
• Improve the separate reporting for glass, yellow and silver eels.
• Provide information on fishing effort.
• Provide information on exploitation rates (all anthropogenic impacts, in-
cluding non-fisheries factors).
• Achieve better geographical coverage, including the countries outside the
EU but within the eel distribution area. This includes recruitment and silver
eel escapement data.
• Establish regular larval surveys in the ocean (Sargasso Sea).
4.3 Data quality issues
During establishing the framework for intemational stock assessment in European eel,
ICES (2012b) discussed the need for quality control on the national assessments, be-
cause the quality of the international stock assessment depends on the quality of na-
tional assessments and the consistency (and completeness) of these local and national
assessments. SGIPEE (ICES, 201 la) started to develop quality criteria for the data and
models underpinning the estimates of the "3Bs& £A". These quality criteria could be
used initially by the member states as a check list when preparing their progress re-
ports for the EU. At a later stage the quality criteria may be used as a tool (to assess
quality of the estimates and identify over- and underestimates) during the post-evalu-
ation of European eel stocks. The following recommendations on intemational stock
assessment were formulated during ICES (2010b):
• the reporting on stock status by countries is standardized;
• the minimal information on stock status required is B cum ent, Bbest and Bo (or
equivalent trios, e.g. Bcurrent, EA and Bo);
• quality criteria for national stock assessments are considered, and imple-
mented;
• intercalibration between assessment methods be executed to standardize re-
sults.
Joint EIFAAC/ICES/GFCM WGEEL REPORT 2014
As a first step, SGIPEE (ICES, 201 la) and WGEEL (ICES, 2012b) developed a scorecard,
whlch could be used for a basic check for bias in the data (Annex 9 in ICES, 2012b).
This scorecard is an attempt to summarize some of the important criteria that, however,
needs further development: the list of criteria should be reviewed and realistic stand-
ards for these criteria should be formulated. Another important step during the evalu-
ation of the "3Bs& EA" is to predict if certain biases will produce an overestimate or
underestimate. Finally a decision needs to be made on which "rule of aggregation" to
apply when moving from the individual criteria, to the three estimates and to the over-
all quantification of the status of an EMUs "3Bs& ZA" estimate.
4 .4 Data available vs gaps
Given all of these data requirements, the working group has reviewed the available
information provided in the Country Reports about the stock indicators and the habitat
coverage achieved by the countries. The electronic table "Chapter 4 Table E4-1" accom-
panying this report reveals considerable gaps of such information.
The stock indicator, Bo, pristine biomass, is reported from 71 EMUs out of the
129 EMUs/countries in the area of European eel distribution. Stock and mortality indi-
cators are lacking from many countries, especially from the eastem and southern parts
of the Mediterranean Sea. The indicator Bbest is reported by 80 EMUs and the current
escapement, Bcurrent, by 69 EMUs. Data on total mortality exist from 63 EMUs. In many
countries riverine and lake habitats were assessed based on estimates of habitat specific
productivity. Coastal and estuarine habitats have considerable data gaps.
Table E4-1 also summarizes the existence of recruitment time-series as reported in the
2014 country reports to the WGEEL. Most monitoring sites are located in the North Sea
region, several of them fishery independent. In the Biscay region only two sites for
glass eel monitoring are still in operation. In the Mediterranean Sea only Italy reports
data from one site in the Lazio eel management unit. For further information on re-
cruitment series see also Chapter 2.
4 .5 Prioritization for future work (based on identified gaps)
The prioritization of the gaps in terms of impact on the quality of the intemational
stock assessment for eel has to be based on the discussion on shortcomings and limita-
tions in the present assessment. Two major aspects can be extracted:
1) Improve the amoimt and the quality of the data (stock indicators, landings
etc.) delivered by the countries already contributing somehow to the stock
assessment. This also includes information on habitats, which so far are not
sufficiently covered by the assessment, e.g. coastal and transitional waters.
It is known that these may form important habitats for eel but there are con-
siderable gaps in data on eel stocks in these habitats.
2 ) Include data from countries in the distribution area of European eel, from
which information is lacking more or less completely (or for certain stages,
e. g. glass eel recruitment), but which may be of considerable relevance due
to the size of their local stocks.
Whereas the first aspect has been discussed before, the second aspect will be explained
shortly here. Stock assessment on a total population scale sets demands for stock indi-
cators from a representative majority of habitats producing eel all over the area of dis-
tribution. So far, information is missing for a considerable part of the distribution area.
Jo in t EIFAAC/ICES/CFCM WCEEL REPORT 2014
A total of 38 countries are considered to produce eel across Europe, Africa and Asia
and have presently (or have had in the past) eel capture fisheries production according
to FAO (2011). Of these, 19 countries are in the EU and have produced EMPs.
The relative role these countries play in eel exploitation can be roughly derived by ex-
amining eel capture fisheries statistics. The annual catches of eel reported to FAO sta-
tistics for 2007-2009 have been summarized in ICES (2011a, Table 3.2). Note that ICES
(2008) has previously identified some inconsistencies in the FAO eel statistics, so the
data should be viewed with caution, but they may be used here for illustrative pur-
poses. In each year, European countries that have implemented EMPs account for most
of the eel exploitation, but non-EU EMP countries account for considerable produc-
tions in the region of 27 to 39% of the total catch (Figure 3.1 in ICES 2011a). In the latter
group, Egypt accounts for most of the eel yields, but Albania, Tunisia and Turkey also
contribute. For further information see also Chapter 2.
These figures clearly indicate that even rough information from these countries outside
of the EU will increase the quality and plausibility of the intemational stock assess-
ment. However, in the absence of information on relative catches of yellow and silver
eel in these statistics, and in silver eel characteristics of these countries, it is difficult to
provide any greater understanding of the relative contribution (potential) of these
other countries to the spawning stock and therefore future recmitments.
Whereas the inclusion of data from countries not covered by the stock assessment so
far is urgently needed, improvements in amount and quality (homogeneity, reliability
etc.) of data have to be achieved as well for the EU countries during the implementation
of the Eel Management Plans. These two approaches to data enhancement and im-
provement should not be viewed as mutually exclusive as both need to be pursued to
improve the collective ability to assess and to manage the eel stock. Furthermore, if,
when and in which quality data from the so far missing countries can be provided is
unclear. Meanwhile, the EU / European countries have the ongoing responsibility to
ensure that their own contributions as good as possible.
4 .6 Recommendation from this chapter
R e c o m m e n d a t io n A d r e s s e d t o
Intemational coordination with countries outside the EU to ACOM / ICES Secretariat / EU /
achieve adequate spatial coverage of eel stock assessment. GFCM / EEFAAC
Joint EIFAAC/ICES/GFCM WCEEL REPORT 2014
5 ToR d) Identification of suitable tools (models, reference points
etc.) in both data rich and data poor situations
5.1 Introduction
The purpose of this chapter is to provide a source of reference for those wishing to
implement eel stock assessments in their coimtries. The chapter draws on reports pre-
vious Working Group, Study Group and Workshop reports, Country Reports and
other publications (e.g. EMPs, EMP Progress Reports, EU-POSE and EU-SLIME project
reports), and summarises the application of approaches to assess eel at various geo-
graphic scales and under various data situations.
The methods applied in various EU and other countries, their data requirements and
outputs, are summarised in the accompanying electronic table, Table E5-1.
5.2 Methods available to assess silver eel production and escapement
The methods available to determine the potential escapement, in the absence of anthro-
pogenic impacts, and actual escapement of silver eel are outlined below. Silver eel es-
capement is the amount of eel that have successfully passed and survived all of the
potential anthropogenic and natural mortality impacts in continental freshwaters, es-
tuaries and coastal waters (or fresh and saline waters) on their emigration to the oce-
anic spawning groimd.
5.2.1 Methods based on catching or counting silver eels
There are several means by which silver eel escapement can be estimated (at least) di-
rectly from catching or counting eels. The EIFAC/ICES Working Group on Eels re-
viewed these methods in 2008 (ICES, 2008). The following develops from this review,
and adds consideration of the major practical issues associated with deploying these
methods at geographical scales appropriate for basin district or national assessments.
5.2.1.1 Whole River or total traps; “ index” sites
Wolf traps, or related systems, or use of winged nets deployed for research purposes
can provide precise estimates of migrating eel population dynamics and under some
circumstances all silver eels can be counted and weighed. However, this is usually only
possible in smaller river systems where discharge pattem s allow for silver eel trapping
throughout the migration season. Examples of this type of silver eel escapement esti-
mation include the studies imdertaken on the Norwegian River Imsa (Vollestad and
Jonsson, 1988), the French Rivers Frémur (Feunteun et al., 2000) and Oir (Acou et al,
2009), and the Irish Burrishoole river basin (Poole et al, 1990).
There are several issues with applying this method for eel stock assessment that mean
it is not widely suitable. There are exceptionally high resource requirements associated
with installing and maintaining the traps. Given that the trap is required to fish the
entire river width, there are likely to be relatively few suitable sites within EMUs. It is
worth noting in this context that WKESDCF (ICES, 2012a) recommends the adoption
of one index site per EMU, not specifying full detail of what constitutes an index site.
Full and accurate measures of silver eel escapement require that traps operate through-
out the entire period when emigrating fish are passing the site, and that they are all
captured. However, the capture efficiency of the trap can be reduced by varying flow
conditions. Given the considerable size range of silver eels (e.g. 35 to 100+ cm length)
in some basins, the trap design may not be suitable to catch eels across the whole size
Jo in t EIFAAC/ICES/CFCM WCEEL REPORT 201 4
range; i.e. is size selective. This is often the case with commercial gears (see below),
especially where the fishery is controlled by a minimum size limit for the catch. In such
circumstances, the catch may not accurately represent the full run.
5.2.1.2 Partial research traps and partial commercial fisheries
Where trap efficiency is not 100%, mark-recapture methods (e.g. using passive inte-
grated transmitters (PIT) or extemally attached high visibility tags) can be employed
to estimate capture efficiency of the trap. The proportion of marked eels recaptured
provides an estimate of the capture efficiency of the fishery. The catch is then raised by
this efficiency to estimate the size of the run. A comprehensive measure of capture
efficiency would incorporate the varying effects of river condition and fish size. Note
therefore that mark-recapture methods require a model-based approach to raise the
catch to the whole population based on estimates of capture efficiencies: all the meth-
ods require some form of model-based approach to raise catches in account of fishery
selectivity/efficiency and/or accounting for downstream parts of the basin.
5.2.1.3 Fisheries-based assessments; mark-recapture
Commercial silver eel fisheries can, depending on their location and scale, provide
good opportunities for direct estimation of the numbers and biomass of silver eels es-
caping from eel producing systems. The approach of using tagging with mark-recap-
ture can be used to estimate passage at commercial fisheries, in just the same way as a
research trap. Provided that scientists have full access to the fishery and that the com-
mercial operation permits the time and intervention to check the whole catch for tags,
it is possible to determine the efficiency (proportion of run or local stock that is cap-
tured) of the eel capture systems involved (see above). Examples of such investigations,
of population dynamics and seasonal patterns of seaward migrating eels, include those
undertaken on the River Loire, Rivers Shannon and Corrib, River Bann (Lough Neagh
outlet), the River Imsa, the Baltic Basin and the St Lawrence River. Catch and effort
data from closely monitored fisheries in enclosed waterbodies such as Lough Neagh
(Northem Ireland) allow detailed assessments of eel production. However, such large
and discrete eel fisheries constitute only about 5% of the continental fisheries, with the
remainder consisting of very small and disparate fisheries.
As with scientific monitoring studies, difficulties can occur when the fishing season
does not cover the full migration period or when there is significant eel production
downstream of the fishery area. Use of mark-recapture methods for estimating fishery
capture efficiency allows for estimation of the numbers and biomass of migrating eels
at the fishing sites. This can involve use of a variety of tags and marks (see Concerted
Action for Tagging of Fish: www.hafro.is/catag). Experimental fisheries could be es-
tablished in data poor areas and used to improve fishery monitoring methodologies.
5.2.1.4 Fish Counters and sonar
Coimters and various acoustic technologies can allow for the estimation of silver eel
escapement in locations where eel capture is not possible. McCarthy et al. (2008) used
hydroacoustic methods to investigate variations in numbers of silver eels migrating
downstream in the headrace canal of the Ardnacrusha hydropower plant in the River
Shannon, Ireland. Resistivity counters have been trialled successfully for counting em-
igrating silver eel in the UK (J. Hateley, pers. comm.), as have high-frequency multi-
beam sonar (DIDSON®) in the UK, Ireland and the Netherlands (J. Hateley and W.
Dekker*.* http://www.imares.wur.nl/NL/onderzoek/faciliteiten/didson/). The Didson
http://www.hafro.is/catag
http://www.imares.wur.nl/NL/onderzoek/faciliteiten/didson/
Joint EIFAAC/ICES/GFCM WCEEL REPORT 2014
may not be suitable for deployment in rivers >15 m width if a full width coimt is re-
quired, and the main constraint at sites of appropriate dimensions is that the site must
have a suitable profile with minimum or little shadowing of the beam (Briand et al,
2014; Bilotta et al., 2011; Keeken et al, 2011). Such eel counts, and linked data on size
frequencies of the migrating eels, are only possible in locations where other fish species
with target strengths in the same range as the silver eels are not also migrating down-
stream at the same time as eels. Work is in progress in Ireland, UK, Poland, Sweden
and other European countries that should lead to improved sampling protocols and to
more widespread use of this method for estimation of eel escapement rates.
5.2.1.5 Acoustic or radio tracking of individual fish
Where resources permit, mark-recapture escapement estimation at a partial fishery or
trap (generally for silver eel) can be usefully supplemented for verification, or in some
cases substituted, by acoustic (or radio) tracking with upstream and downstream re-
cording receivers. This has the distinct advantage of observing the fish that pass an
obstacle or fishery rather than estimating them from numbers not recaptured. This
work is expensive and generally carried out at a research scale with small numbers of
tags (rarely more than 100 individuals in any one study, and usually only tens). Tele-
metric tracking can be an alternative means of eel passage estimation at sites where
there is no possibility of a mark-recapture set-up, such as at large river hydropower
sites, or used as a verification method for DIDSON® or similar hydroacoustic escape-
ment assessments (McCarthy et ai, 2013). Where there is no tagged eel recovery, care
needs to be taken to ensure that tracked tagged fish are still viable having passed
through the tagged area, for example that the tagged fish have not been taken by mo-
bile predators, or are not simply moving downstream in a moribund state.
5.2.1.6 General issues with catch, count and proxy approaches
Few fisheries or in-river traps are operated at the very downstream extreme of the
study basin, and therefore they miss any silver eel produced from the habitats further
downstream. This is especially a problem when the study basin includes the estuary or
even coastal waters. Given the practical and logistical difficulties associated with meth-
ods relying solely on capture of silver eels, not least the ability to catch the eels in a
manner that is representative of the entire run, there are relatively few places across
Europe where this method can be adopted.
A further limitation of these direct approaches, as it relates to European assessment
and management of eel, is their inability to provide a measure of potential 'pristine'
silver eel production in the absence of data from the appropriate historic period. Alt-
hough such historic data exist and have been used for a small number of river basins,
e.g. Burrishoole (Ireland), Neagh/Bann (UK N. Ireland), the approach cannot be used
to back-calculate from present to historic production. Thus, while a new direct ap-
proach might be deployed in a river basin, it can only provide an estimate of silver eel
production from now onwards, assuming constant conditions. In the absence of his-
toric data, therefore, we are reliant on models of eel production to estimate pristine
levels.
5.2.2 Methods based on yellow eel proxies
The use of proxy indicators from sedentary eels and habitat population models is an-
other approach that has been applied to estimate silver eel escapement (e.g. Feunteun
et al, 2000; Aprahamian et ah, 2007; Lobon-Cervia and Iglesias, 2008). In many river
systems, surveys are commonly conducted to characterize the sedentary 'yellow eel'
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component of the local stock. Mark-recapture or other more locally adequate methods
could be used to estimate density of yellow and pre-migrant silver eels. A number of
morphological characteristics have been identified that indicate pre-migrant status of
eel, i.e. that they should be expected to emigrate as silver eels in the next migrant sea-
son (Feunteun et al, 2000; Durif et al., 2005). It is possible therefore to estimate silver
eel production from a water course based on the numbers of such 'pre-migrant' eels
(Feunteun et al., 2000; Acou et al, 2009).
The approach introduces two main sources of uncertainty in any estimate of silver eel
production. First, if it is conducted in only one year it assumes that all eels classed as
pre-migrants will actually become silver eels in the following migration season. Rather,
evidence suggests that some pre-migrants may not emigrate in the year of marking (E.
Feunteun, pers. comm.), and that studies using this method should be conducted over
a number of years.
The second assumption is that the eels sampled during the surveys are representative
of the eel population across the river basin, such that the survey results can be raised
to the system, typically according to the relative wetted areas. These procedures
should nevertheless be standardized so that methodologies used can provide repre-
sentative estimates of silver eel production, e.g. sampling at the beginning of the mi-
gratory season (late summer in southem latitudes and middle summer in northem
latitudes). Several habitat types representative of each catchment should be evaluated
in order to be able to extrapolate for the whole catchment and include it in habitat
population models. Eel mortality rates need to be determined throughout the river ba-
sin including the estuary as well as fresh-water habitat.
Acou et al. (2009) estimated silver eel production from two coastal river systems of
western France, the Frémur and Oir. In the Frémur, 29 surveys covered about 2.3% of
the wetted area of fluvial habitat, and four sites each in two still waters, and up to
32 sections of the Oir, accoimting for 8% of fluvial habitat but only along a 7.5 km length
of river.
Obtaining population density estimates for yellow eels in large water bodies including
still waters is often difficult or impossible. Studies suggest that eels are often confined
to shoreline margins of still waters because of the presence of cover and food (Jellyman
and Chisnall, 1999; Schulze et al, 2004), though this is a topic that has received rela-
tively little study. Whilst that presence of eels has also been recorded along the shore-
line margins of many lake systems throughout Ireland (Poole, 1994; Moriarty, 1996;
Rosell et al, 2005), these findings are commonly associated with seasonality, given that
the shallow waters warm up quickest thereby promoting eel feeding behaviour in these
regions. However, commercial fishing experience and scientific survey data have re-
vealed that as water temperatures begin to rise throughout the summer months, eels
are more commonly found in the deeper (>9 m) waters (Matthews et al., 2003; Allen et
al, 2006; R. Poole, pers. comm.). Nevertheless, extrapolation of fluvial densities across
the entire surface area of still waters may overestimate eel production from some still
waters. In the Frémur, France, (Acou et al, 2009), only a 2.5 m wide shoreline strip of
fluvial habitats produced eel and thus eels were absent from about 95% of the fluvial
wetted area. It is clear that the proportion of water surface area occupied by eel can be
a highly individual calculation and care needs to be taken in extrapolating between
areas, to avoid grossly underestimating or over-estimating eel production in many wa-
ters.
The surveys have a significant resource requirement and therefore numbers and dis-
tribution of surveys is often limited. To date we are unaware of any study testing the
Joint EIFAAC/ICES/CFCM WGEEL REPORT 2014
number and distribution of surveys against the accuracy of their representation of the
actual yellow eel population in a river system. Statistical methods are available to aid
sampling design (e.g. power analysis), but these must be incorporated with spatial in-
formation on habitat diversity and distributions in order to develop statistically robust
stratified sampling programmes.
5.2.3 Model-based approaches to estimate potential and actual silver eel
escapement
The level of complexity that characterizes the life cycle of eel populations makes the
simulation of its dynamics particularly challenging. Studies have already focused on
the development of population dynamics models for several eel species including the
American eel (Anguilla rostrata) (Reid, 2001), shortfin (A. australis) and longfin eel (A.
dieffenbachia) (Francis and Jellyman, 1999), and European eel (A. anguilla). The Euro-
pean SLIME (Dekker et al.f 2006) and POSE Projects (Walker et al.r 2013) reviewed de-
velopments in quantitative modelling of European eel populations and tested different
models in light of the management target proposed by the EC.
The number and diversity of models developed for Anguillid species is considerable,
starting with the age-structured and life table models of Sparre (1979) and Rossi (1979),
respectively, and to date including input-output, stochastic and/or spatially distrib-
uted demographic, VPA-like, and multi-stage stock-recruitment models, and covering
a single life stage (glass eel) to the global stock. De Leo et al. (2009) provided a repre-
sentative summary of the features of many of the models that have been used over the
years to describe the dynamics of eels and predict the status of the stock. Because of
the complex life cycle of eels the range of information needed to describe this and the
complexity of the model that could be used, is high. Similarly, the range of information
needed to estimate unexploited and current stock sizes and escapement is considera-
ble. This includes standard type of stock assessment inputs/estimates such as recruit-
ment levels, catch data but also less common factors such as stage-specific stock
estimates and indices of habitat quality.
This discussion focussed only on those models that have been applied in EMPs and/or
are under continuing development, compared to those models that are not, as far as
we can establish, being used in EMPs or subject to further developments. These mod-
els, listed in alphabetical order, are as follows:
• Demographic model of the Camargue (DemCam)
• Eel Density Analysis 2.0 (EDA)
• German Eel Model (GEM)
• Scenario-based Model of Eel Production II (SMEPII)
• Swedish analytical model (SWAM)
• Model of eel population within a Hydrographic network (GloBang)
• Length-Based Virtual Population Analyses (LVPA)
• Dutch eel models
• version of CAGEAN model (Deriso et al, 1980)
A further model, GEMAC (glass eel model to assess compliance) exists as a glass eel-
specific model used in France to determine actual glass eel settlement after fishing,
glass eel fisheries mortality and other anthropogenic factors at that stage, and natural
mortality from the glass eel arriving at the coast/estuary. It has been described in the
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SLIME report, but it is not yet used in producing recruitment time-series data but
could, given expert time and data, be used to improve estimates of recruitment of glass
eel or give absolute recruitment estimate. However, as it is not designed to produce
silver eel biomass and anthropogenic mortality reference points, it is not considered
here.
There are considerable differences between these models in terms of their level of com-
plexity, data requirements, real cases in which they can be applied, etc. Knowledge of
these differences is very important in order to identify the right model to apply to
quantify potential and actual eel production and silver escapement, depending on eel
population characteristics and data situations. The following descriptions are summa-
rised from the reports of the SLIME (Dekker et al., 2006) and POSE (Walker et al., 2013)
reports.
5.2.3.1 Demographic model o f the Camargue (DemCam)
Modeí approach and processes
DemCam is a stage-, age-, and length-structured model that provides a detailed de-
scription of the status of the eel stock in a homogeneous water body, considering the
main aspects (both natural and anthropogenic) that affect eel population dynamics. A
general formulation makes it suitable to describe the demography of other different eel
stocks, providing that a sufficient number of data are available for parameter calibra-
tion. The model is designed to simulate the condition of the stock in actual, pristine
and future conditions imder different scenarios.
The model is deterministic with an annual time step, using density-dependent juvenile
mortality, growth of undifferentiated, male and female eels, fishing mortality and
length-dependent maturation.
The model evaluates the consequences of fisheries, restocking, maturation, growth and
natural mortality on the yellow and silver eel population and it explicitly accormt for
the dynamics of glass eels to capture the effects of anthropogenic and other factors on
this part of the population.
Data requirements
The model requires annual indicators of recruitment and fishing effort, and biological
parameters, either directly assessed for the studied population (when data are availa-
ble) or taken from literature. These required parameters are: Annual recruitment (time-
series or index); Sex ratio (at silver stage or at 30 cm); Density-dependent juvenile mor-
tality (back calculated from historical maximum); Sex-specific body growth (otolith,
age at silvering); Sexual maturation (silver size); adult mortality (literature, or know);
Fishing mortality (know, estimated).
Further model developments foreseen but not planned at this time, can focus on im-
proving the description of sex differentiation in small yellow eels and producing m ark-
recapture estimates of yellow and silver eel abundance. The model also needs to be
calibrated against length distributions of yellow and silver eel catches, to allow the
ability to carry out sensitivity analyses on parameters and outputs, and to bootstrap
input data.
Joint EIFAAC/ICES/CFCM WGEEL REPORT 2014
Model outputs
The output of the model is number of eels in a given time at a given age, size, sex and
m aturation stage. Based on this information, the user can estimate the number of mi-
grating silver eels for any given time.
The model defines the eel stock and the harvest structured by age, length, sex and mat-
uration stage (yellow or silver) on an annual basis. The output consists of biomass and
number of eels in catches, and yellow and silver eel stock by age, length, sex and mat-
uration structure under different management scenarios, such as stocking, fishing reg-
ulations, and/or different environmental conditions.
5.2.3.2 Eei Density Analysis (EDA 2.0): A statistic model to assess European eel {Anguilla
anguilla ) escapement in a river network
Model approach and processes
This is a framework of eel density analyses rather than a fixed, end-user model. It re-
lates yellow eel densities to environmental variables, including anthropogenic impacts,
and is extrapolated from survey sites to the river basin. The predicted yellow eel stock
is then converted to a silver eel escapement, using a conversion rate.
The modelling tool is based on a geolocalized river network database to predict yellow
eel densities and silver eel escapement. There are six main steps in the model applica-
tion:
1 ) Relate observed yellow eel presence/absence and densities to descriptor pa-
rameters: sampling methods, environmental conditions (distance to the sea,
relative distance, temperature, Strahler stream order, elevation and slope,
etc.), anthropogenic conditions (obstacles, fisheries, etc.) and time (year
trends);
2 ) Extrapolate yellow eel density in each river stretch by applying the statisti-
cal model calibrated in step 1;
3 ) Calculate the overall yellow eel stock abundance by multiplying these den-
sities by the surface of each stretch and summing them;
4 ) Estimate a potential silver eel escapement of each stretch by converting yel-
low to silver eel abundance using a fixed conversion rate;
5 ) Calculate effective escapement by reducing potential escapement with silver
eel mortalities during downstream migration;
6 ) Sum the effective escapement from all the stretches to give estimate at EMU
scale.
It is also possible to give an estimate of the pristine escapement by running the EDA
model w ith anthropogenic conditions artificially set to zero and time variable datasets
before 1980.
Data requirements
The model needs information on the yellow eel population, environmental character-
istics, and anthropogenic impacts on eel production. The data required on the eel pop-
ulation are the presence/absence and densities of yellow eel, typically derived from
scientific surveys (e.g. electro-fishing surveys).
Jo in t EIFAAC/ICES/GFCM WGEEL REPORT 2014
The environmental data are the distances to the sea and source, and the relative dis-
tance (between sea limit and the more upstream source), the temperature in each seg-
ment of the river network, the mean rainfall, the elevation, slope and stream order
(Strahler and Shreve). EDA is designed to be applied at the EMU or larger scale. It uses
the CCM v2.1 (Catchment characterisation and Modelling) a European hydrographical
databases (Vogt et al, 2007, http://ccm.irc.ec.europa.eu/) to derive the environmental
descriptors. The CCM2 database includes a hierarchical set of river stretches and catch-
ments based on the Strahler order, a lake layer and structured hydrological feature
codes based on the Pfafstetter system (De Jager et al, 2010). The primary catchment
referred to is the drainage area; this is the smallest entity in this hierarchy and is
drained by CCM river stretch.
The anthropogenic impacts are described by the obstacle pressure (cumulative number
of dams and their pass-ability), the land use, and fisheries.
Model outputs
The outputs of the model are the yellow eel density in each reach of river network, and
the overall yellow eel stock abundance and a potential silver eel escapement at pristine
and actual conditions. The biomass and number of yellow eel and eel escapement are
optional.
5.2.3.3 German Eel Model (GEM)
Model approach and processes
The German eel model was developed specifically for describing the dynamics of the
eel population of the River Elbe system, especially for estimating the escapement of
silver eel between 2005 and 2007. The age-based model is data driven and was adapted
to the available dataseries estimated relationships. The model treats the productive
area as a single unit, so does not take into account spatial aspects like different habitat
pattems, area dependent growth, etc. Nor does it account for the potential effects of
density on eel production processes such as growth and mortality rates.
The model is based on the structure of the Virtual Population Analysis (VPA), but the
GEM works in the opposite direction. The initial population in number, by age group,
at the beginning of year one is estimated. Then the model estimates the number of eels
of each age group which leave the system for various reasons (natural mortality, fish-
eries, predation, turbines, etc.) in the same year. The population at the beginning of the
following year is then estimated based on the remaining population, and the numbers
of immigrating elvers and restocked eels.
The following parameters are assumed to be stable during the total model period:
• Growth and weight-length relationship;
• Relative age distribution of eel eaten by cormorants;
• Relative age distribution of silvering eel;
• Mean weight of eel in the stomach of cormorants;
• Relative age distribution of immigrating eels.
The natural mortality is split into two components: the effect of cormorants and the
remaining natural mortality. It is assumed that the age distributions of eel caught in
fisheries and those eaten by predators are similar to the age distribution of the stock.
Also, that turbines and pum ping stations only impact silver eels.
http://ccm.irc.ec.europa.eu/
Joint EIFAAC/ICES/CFCM WCEEL REPORT 2014
Note that for the Elbe dataset at least, analyses have shown that the size and the relative
age distribution of the initial year has relative low effects concerning the year tx if the
period between the initial year and the year tx is more than 18 years. Thus, GEM re-
quires a 'training' dataset of at least 18 years.
Data requirements
The following input data are required for the model:
• Catch in kg by fishermen and angler per year;
• Number of restocked eel by age group and year;
• Number of immigrating elvers by age group and year (if data are not avail-
able for each year, estimates based on international time-series can be used);
• Catch in kg by cormorants per year;
• Mortality of silver eels due to hydropower plants and water removals in %
per year.
Input data are provided as numbers per cohort, with various counts or length distri-
butions converted to age profiles based on survey data. The model requires descrip-
tions conceming the weight-length relationship and the growth of eel to estimate the
mean weight of eel by age group and to transform length-based estimates into age-
based estimates.
The relative age distribution of eel captured by cormorants is required for estimating
the total number of eel consumed by cormorants. It is assumed that the proportion of
eel in the food of cormorants is dependent on the density of eel.
The model also contains the option to add stochastic noise to the input data which are
normally distributed with a mean of zero and a given variance. If the variance is real-
istic this option can be used for estimating the confidence intervals of the escaping sil-
ver eels by means of bootstrap methods.
Outputs
Model outputs are population size, catch by fishermen, catch by anglers, catch by cor-
morants, mortality by other natural reasons, and silver eel escapement, all expressed
as numbers per cohort.
5.2.3.4 Scenario-based Model of Eel Populations (SMEP II)
Model approach and processes
SMEP II is a software package developed to model the dynamics and exploitation of
eel populations (Aprahamian et al, 2007). It is based on the scale of a river basin, and
simulates the freshwater phase of eel production. It is a population dynamics model
that simulates both the biological characteristics of the eel population and a number of
potential anthropogenic influences on that population. Biological processes modelled
include growth, natural mortality, sexual differentiation, maturation (silvering) and
migration within the basin. Anthropogenic influences include environmental and hab-
itat quality, fishing practices, barriers to migration and stocking.
The population dynamics model used is a length-based model that describes the dy-
namics of a population of eels for the duration of its stay in the river basin. The model
is also sex-, stage-, and area-specific and accounts for density dependent effects, and
habitat structure and quality. Therefore, it tracks changes in undifferentiated, yellow
Joint EIFAAC/ICES/CFCM WCEEL REPORT 2014
(male and female) and silver (male and female) eels within four seasons and for each
reach in the basin. The model does not make any assumptions about the d)mamics of
eels that have migrated from the river back to the sea (i.e. on silver eels once they exit
the basin). Since only partial simulation of the population dynamics is possible (the salt
water phase of population's life is not simulated), processes such as recruitment cannot
be modelled explicitly and therefore, information about them needs to be provided
extemally (or estimated).
Model outputs are provided both as numbers and biomass of eel, per sex and life stage,
river reach and year; and length-frequency distributions. SMEP II is designed to pro-
vide time-series or equilibrium outputs for each reach and summarised for the catch-
ment for: undifferentiated eels, male and female yellow and silver eels: in terms of
numbers, density and biomass, length-frequency distributions, sex ratios, and pre-
dicted catch numbers and biomass. The model can be used to project the population
forward from a predetermined starting condition or estimate the starting conditions
that could lead to a given population size or structure. As a projection tool, the user
may vary anthropogenic influences and levels of recruitment in order to create 'what-
if' management scenarios, relative to the given reference point.
Data requirements
SMEP II must at least have information describing the eel life-history processes, and
the size and structure of the river basin and the level of annual recmitment, in order to
predict potential production under 'pristine', constant conditions. Where data are
available, either for historic or present conditions, these can also be applied to charac-
terise the yellow eel population (in the past or present), impacts on escapement (e.g.
fishing or turbines), inputs such as stocking events, and changes in the available area
and quality of habitat. These additional data allow the user to set the model to simulate
escapement under various conditions (past, present and future), and to alter the effects
of impacts and inputs in order to examine their relative influence on escapement.
The biological processes that apply to the life cycle of eels in the study river are defined
by the user from river-specific information, or can be parameterised according to val-
ues from neighbouring rivers or from the scientific literature.
Recruitment of eel is described according to the length of recruits (mean and standard
deviation), the maximum number of recmits in any year, and a time-series of recmit-
ment as an index of that maximum.
The model also needs information to describe the effect of density on the dynamics of
eels if such effects are to be taken into account in the calculations. This is characterised
according to the level of eel density biomass at or above which the density-dependent
variations in biological processes take a strong effect.
In terms of the spatial component of the model, the user defines the number and to-
pography of the reaches, their length and wetted area, as well as information about
obstacles that might constrain the movements of eels between the reaches. The user
also sets the speed at which eels move between reaches.
Where anthropogenic impacts are to be included in the model, fishing is described as
catch weight by stage (glass, yellow, silver eels) and assigned to specific reaches sea-
sons and years, and turbine mortality is described as the proportion of eel that are
killed when passing a turbine.
100 | Joint EIFAAC/ICES/CFCM WCEEL REPORT 2014
If stocking is to be simulated, this is described in terms of the number and length dis-
tribution (mean length and range) of stocked eels, the reach where they are stocked,
and the season and year when the stocking takes place.
Modet output
SMEP II reports the results of simulations in a series of .csv files that provide, for each
reach in every year: the density and biomass of undifferentiated, male and female yel-
low eels; numbers and weight of emigrating male and female silver eels; the proportion
of females; and the numbers and weight of 'catch'.
End-of-run files provides summaries of density and biomass of undifferentiated, males
and female yellow eels, biomass of male and female silver eels, and 'catch' (numbers
and biomass) of undifferentiated, yellow and silver eels, and the length frequency of
eels, stages and sexes in each reach.
5.2.3.5 GlobAng, a model o f eel population dynamics w ithin a hydrographicai network
GlobAng is designed to perform simulations of eel population dynamics within a hy-
drographical network. After calibration with real field data, the model is able to eval-
uate the putative pristine silver eel escapement in response to a variety of management
scenarios, especially when the spatial (reach) dimension is important. The main
strengths of GlobAng are that it takes the river system into account, permits testing of
spatial management scenarios and can be used to analyse impacts of barriers. It also
takes into account density dependent processes and non-linearity in the relationship
between recruitment and silver eel escapement.
Data requirements
GlobAng requires a description of the connectivity and carrying capacities of river sys-
tem reaches and a recruitment time-series. Additional data, such as time-series of age
structure of yellow or silver eels or eel population distribution throughout the catch-
ment, are required for calibration and validation procedures.
Modei approach and processes
GloBang integrates growth, recruitment, sexual differentiation, maturation, natural
mortality and migration within a watershed. Impacts of fishing and migration barriers
can also be simulated. The time step is the week. Sex determinism, natural mortality
and movement depend on density.
Modei output
The main outputs are sex and age structure of yellow eels in each reach and silver eel
escapements either for long run (equilibrium) or over time.
5.2.3.6 Swedish analytical models (SWAM)
SWAM was originally developed for the Swedish (coastal) fisheries (west and east
coast), to investigate how yellow and silver eel fisheries, fishery restrictions and glass
eel restocking affect present and future spawner escapement (and catch) in a specified
homogenous water body. Estimated present and potential spawner escapements can
also be related to estimated escapement at some earlier time representing a more pris-
tine stock. The main strengths of SWAM are its simplicity, transparency and flexibility
(it can be applied to many different types of systems, using little data), and that it gives
analytical solutions that are well defined and do not depend on simulations, and allow
Jo in t EIFAAC/ICES/CFCM WCEEL REPORT 2014
for changes between what is used as an input or an output (e.g. either using data on
either recruitment or catch). Its main weakness is that it is dependent on parameter
estimates from other sources, and that it omits many (possibly important) biological
processes (e.g. using one size where all eels of one sex silver or migrate, or for sexual
differentiation).
Data requirements
In general, only externally determined parameter estimates are used as input, but re-
cruitment time-series can also be incorporated. No tuning or calibration process is in-
corporated in the models. The input must be a continuous series of annual length
frequencies of commercial landings.
Modeí approach and processes
Following classic fishery modelling, only recruitment, mortality (natural and fishing)
and average growth are considered annually.
Model output
Both equilibrium and time-dependent deterministic solutions can be derived. The main
output is proportional spawner escapement, either as equilibrium solutions or over
time since management actions have been applied. Depending on available input, es-
timates can be made of silver and yellow eel catch and spawner escapement in num-
bers (or biomass) or recruitment into the yellow eel fishery (in numbers) for a specific
year (based on data on yellow eel catch).
5.2.3.7 Length-Based Virtual population analysis
Data requirements
Fishery modelling, only recruitment, mortality (natural and fishery induced), growth
and maturation by size class to the silver eel stage and subsequent escapement each
year are considered. The model requires data on total number of eels landed per size
class per year, derived from landings statistics and catch composition sampling. A
breakdown of catches by gear type results in gear-specific outputs. Additionally, pa-
rameter values are required for growth, and for natural (non-fishery) mortality.
Modei approach and processes
The LVPA model quantifies the population state and the impact of fishing, based on
total landings in numbers by length class in recent years.
Modei output
The model aims to provide a critical post-evaluation of management measures imple-
mented during the data years. A minimum of assumptions and a maximum of data
ensure a close tracking of the true population. Derivation of reference points is straight
forward, but has not yet been elaborated. The outputs are population numbers, partial
fishing mortality for each gear type, and silver eel.
5.2.3.8 Dutch eel models
The Dutch EMP reporting relies on models in three components to produce data for
reporting (Bierman et al, 2012; Van de Wolfshaar, 2014). These consist of three inter-
acting processes: a dynamic population model for yellow eel for estimating %SPR, an
102 | Joint EIFAAC/ICES/CFCM WCEEL REPORT 2014
extended yellow eel model for estimating mortality rates, and a static spatial model for
yellow and silver eel. Their use and interaction is described in Bierman et al. (2012).
The population model starts with recruitment data and applies growth, natural mor-
tality, fishing mortality, and maturation parameters on a rate basis to follow cohorts
through to silver eel. The extended yellow eel model uses fitting the data on catches
per unit of effort from stock surveys, or length-frequency distributions from retained
catches, to assess yellow eel stock trends and compare fishing mortality estimates with
actual measurements derived from stock biomass surveys. The static spatial popula-
tion model estimates standing stock biomass of yellow and silver eel to further derive
biomass of silver eel escapement using geographic data of fresh water bodies with spa-
tially-structured eel density data.
Data requirem ents/ Mode/ approach and processes
The method uses a mix of rate-based process with actual survey and fisheries data, and
geographic information.
Modei output
The Dutch method produces the three biomass and summed anthropogenic mortality
rate reference points required for local EMP and intemational reporting.
5.2.3.9 CAGEAN model (Deriso, 1980) and Simplified eel population model (Dekker,
2008)
Modei approach and processes; summary
These two models, based on classical fisheries rate based processes, each feature once
in use by WGEEL reporting countries (Poland and Lithuania) to supply Bcurrent and Bbest
B from basic fishery data.
5.2.4 Use of other methods and extrapolations to calculate or estimate bio-
mass reference points
5.2.4.1 Wetted area based estimations
Many countries or EMU assessors use some means of extrapolating from habitat area
data to derive the biomass reference points, particularly Bo, but also combining with
knowledge of eel specific parameters to aid calculation of Bbest. There are variable de-
grees of sophistication applied, ranging from simple map-based water area measure-
ment combined with application of literature-derived eel carrying capacities, to
detailed reach-based modelling approaches verified with field survey data. The most
robust of these approaches use GlS-determined wetted area, with natural and man-
made barriers defined and field verification to give reach-based accessibility parame-
ters. This approach can often interlink with WFD assessments of river continuity
and/or estimates of population level targets for other species (e.g. migratory salmonids
in Northern European countries). A good example is that used for the Irish EMPs based
on a wetted area model originally designed for defining Atlantic salmon habitat-based
stock reference points (McGinnity et al, 2011).
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6 ToR b) Review the life—history traits and m ortality factors by
ecoregion
6.1 Introduction
The working group explored whether the ICES approach to assessing Data-Limited
Stocks (DLS) might offer an altemative approach for assessing the stock status of the
European eel. This DLS approach has been developed within the WKLIFE I, II, III re-
ports (WKLIFE IV met the week before WGEEL 2014 but the report was not available
for WGEEL to consider). As the new ICES model for providing advice aims to deliver
this at the ecoregion scales (Figure 6.1), the working group explored these eel life-his-
tory traits at this scale, compared to other geographic scales typically applied to eel
assessment.
104 | Joint EIFAAC/ICES/GFCM WCEEL REPORT 2014
Ecoregions based on iCES Advice ACFM/ACE report (2004)
iCES Convention area (FAO area 27) includes regions A-G, L
Zones H-J, M are outside the !CES area
A: Greenland and lceland Seas
B: Barents Sea
C: Faroes
D: Norwegian Sea
E: Celtic Sea
F: North Sea
G: South European Atlantic Shelf
H: Western Mediterranean Sea
I: Adriatic-lonian Seas
J: Aegean-Levantine Seas
K: Oceanic northeast Atlantic
L: Baltic Sea
M: Black Sea
Figure 6.1. ICES ecoregions.
6.2 L ife-h istory traits relevant to eel assessment
The work of WKLIFE suggests that in the absence of quantitative data, life-history traits
may be used to assess stocks. The life-history traits used by some of the DLS ap-
proaches to define reference points for sustainable exploitation, that appear potentially
relevant to eel are: growth parameters using the von Bertalanffy function; various L50
matured, where 50% of the population by length has silvered; Length and age; Fecun-
dity; Weight-at-age and Length-weight relationship.
Due to their outstanding complexity in life cycle, with oceanic reproduction and larval
transport, ascending as glass eels in rivers, growing as yellow eels in a diversity of
marine, brackish, or freshwater habitats, and - after metamorphosis - leaving the fresh-
water habitat for a period of oceanic migration to distant spawning grounds, the eel is
Jo in t EIFAAC/ICES/CFCM WCEEL REPORT 2014 1
not assessable or manageable in the same way as most other marine exploited fish spe-
cies. The presence of different life stages and metamorphoses, its longevity and sem-
elparity and the exceptional migration advocates the need to use specific eel-oriented
life-history traits, different from the ones used in other fish stock assessments.
Moreover, eels are eurytopic and have a widespread geographic range from the warm
waters of the North African continent to cold Scandinavian river systems. The high
natural variability in habitats where they live, added to the variety of anthropogenic
pressures in these different habitats, provokes an exceptional plasticity in traits over
the local stocks. Probably the most striking examples of this are the extreme differences
in sex ratio and size and age at silvering over a latitudinal gradient.
Furthermore, while in most marine species mainly the adult sized fish is exploited, in
eel, immature life stage are targeted by fisheries, from recruiting glass eel, resident yel-
low eels and migrating potential spawners in the silver stage.
In European eel, in contrast to other marine species where detailed and comprehensive
monitoring data e.g. fecundity and reproduction potential, allow "finger on the pulse"
management, uncertainties and gaps in knowledge about essential phases in eel's life
history (especially concerning reproduction, fecundity and migration success) hamper
stock assessment and management.
All the above illustrates why assessment based on a classical set of life-history traits, as
used by most exploited marine species, is not feasible for eel, and advocates the need
for a specific eel-based approach with an expanded set of eel-specific life-history traits.
An overview of the potential eel-specific life-history traits is given in Table 6.1. These
may be classified as traits related to silvering process, population, quality and growth.
As both sex and stage (yellow or silver) are crucial factors when describing an eel pop-
ulation, most parameters have to be split into those categories.
Males at silvering are smaller than females at silvering and most often also younger.
The size at silvering is used both as a quality factor (condition) but also for the conver-
sion between length and weight (and vice versa) when calculating the production in
biomass. Other, population-related traits include sex ratio and mean age. Age is of out-
most importance in all models as this affects the lifetime mortalities.
Quality-related traits such as good condition and sufficient energy accumulated
through lipid stores is required for fuelling the migration and production of gametes.
Fecundity and lipid content are parameters not yet used in any eel quantitative model to
our knowledge. However, as quality/fitness in this long-migrating species probably is
a determining factor for a successful reproduction, those parameters may be consid-
ered in the future in more complex models. Also growth rate and von Bertalanffy param-
eters are relevant descriptors for growth.
The working group examined the information provided in Country Reports to ascer-
tain what life-history trait data were available by country. Data on the various life-
history traits are available, and a summary of their availability is provided in the elec-
tronic Table E6-1 accompanying this report. Time constraints within the meeting pre-
cluded a more detailed compilation and analysis but this is recommended in the future
(see below). Previous working group reports (ICES 2010; 2011) and scientific papers
(e.g. Vollestad, 1992; Tesch, 1977) provide further details.
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6.3 ICES ecoregion vs other geographlc scales
Available data show large and progressively increasing levels of variation in the eel
life-history traits at basin, country and ecoregion scales. For example, length at silvering
for females is 471-675 mm within the ecoregion Westem Mediterranean Sea and 420-
1120 in Celtic Sea Ecoregion. Age at silvering for females in Celtic Sea Ecoregion ranges
from 8-28 years but for Westem Mediterranean Sea the range in age at silvering is 7-
12 years. In marine species the degree of variability of LHTs within an ecoregion is
considerable lower than the degree of variability of LHTs in eels even in the same EMU.
Marine fish stocks may inhabit large sea areas and the management unit may with
good reason be an ecoregion. However, the use of life-history traits in assessment on
an ICES ecoregion scale is considered not appropriate for assessment of the eel stock.
The WGEEL proposes that the Eel Management Unit is the most appropriate geo-
graphic scale for the assessment of data-limited eel stocks in alignment of the EU's Eel
Regulation (EC 1100/2007), and that data on life-history characteristics be collated at
the spatial scale of the eel management unit (EMU) as part of the development of the
European Eel Stock Annex (see Annex 4).
Table 6.1. O verview of eel life-history traits information available, as reported in the country re-
ports to the WGEEL 2014. *L50 = the length at which 50% of the population has silvered, as defined
by WKLIFE.
L if e - F I i s t o r y t r a it s Y e llo w
EELS
MALES
Y e l l o w eels
FEMALES
SlLVER EELS
MALES
SlLVER EELS
FEMALES
POPULATION
Silvering related
traits
Length at silvering
(average, range,
L50*)
N /A N/A X X
Weight at silvering
(average, range)
N /A N /A X X
Age at silvering
(average, range)
N/A N /A X X
Population related
traits
Sex ratio (100*
F/(F+M))
X X X X
Condition/qualitv
related traits
Fecundity (average,
range)
N /A N /A X
Lipid level (average,
range)
X X
Condition factor
(average, range)
X X X
Length/weight
relationship
X X X X X
Growth related traits
Von Bertalanffy
parameters: Lmf, K, to
X X X X X
Growth (cm/year) X X X X X
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7 ToR f (i)) Explore the standardization of methods for data co l-
lection, analysis and assessment
7.1 Introduction
Eel is thought to be one (panmictic) population spread over Europe, (including the
Mediterranean) and parts of North Africa, but local conditions vary so much that uni-
form stock-wide management is impractical. For those countries with the EU, the de-
velopment and implementation of protecdon measures has therefore been delegated
to the national / regional levels and management / assessment is at the national, EMU
or individual river level as set out in the Eel Management Plans.
The EU Member States (MS) have used an extensive variety of methods to determine
stock indicators to meet both national and intemational obligations, with only little
coordination or standardization among MS. This means that full intemational stand-
ardization (facilitating Community support) may need to be more flexible than for tra-
ditional marine fisheries, although there might be scope for a general move to more
standardized approaches, which might aid quality control in the future. The standard-
ization and coordination of the data collection, analysis and reporting would imequiv-
ocally facilitate post-evaluation of the EMUs, and will provide for more cost-effective
data collection and analysis (ICES, 2013a). In addition, an appropriate eel whole-stock
assessment, could only be achieved if all the eel-producing habitats (rivers, lakes, tran-
sitional and coastal waters) are taking into account. Thus, to achieve a population-
wide, international assessment it is necessary to try to standardize the assessment
method as much as possible, taking into accoimt the data available in the various coun-
tries, such an approach is outlined in Section 7.3. The first step is to analyse what in-
formation is available in each of the eel producing coimtries and based on this
compilation we can explore the options for a common methodology for assessment.
7.2 Available inform ation in eel producing countries
Four tables have been designed to analyse the available information in eel producing
countries: two of them dealing with commercial and recreational fisheries respectively,
one regarding the information compiled in the EU surveys, and one referring to na-
tional surveys. The aim of these tables was to have a general idea of the available in-
formation, so the parameters have been grouped in general categories and are much
less detailed than in other sections of the present report. A colour code has been estab-
lished to determine the level of data available per EMU at the country level in those
countries having a management plan, or per Country in those not having a plan (Table
7.1). The table has been fulfilled taking into account the expert knowledge of the coun-
try representatives in the meeting in the case of Norway, Sweden, Latvia, Lithuania,
Poland, Germany, Denmark, Netherlands, Belgium, Ireland, United Kingdom, France,
Spain, Portugal, Italy, Montenegro, Albania, Greece, Turkey, Tunisia. Information
from Malta, Slovenia, Croatia, Egypt and Algeria has been recorded from the GFCM
Background technical document on eel fisheries and aquaculture in the Mediterranean
Sea (under revision). No information has been obtained for Finland, Estonia, Russia,
Luxemburg, Slovenia, Bosnia-Herzegovina, Cyprus, Lebanon, Israel, Libya and Mo-
rocco.
The exploited stages change depending on the Country, and fisheries has been forbid-
den in some Coimtries following implementation of EMPs (Table 7.2). Among glass
eel fishing countries, data regarding capacity, effort and landings exists in France, Por-
tugal, United Kingdom and Italy, whereas in Spain only catch information is collected
108 | Jo int EIFAAC/ICES/GFCM WGEEL REPORT 2014
in all the EMUs. In those countries with an existing EMP, within the EC Eel Regulation,
yellow and silver eel fisheries are widely distributed. In the rest of the Mediterranean
countries, except from Tunisia which compiles data regarding effort and catches and
landings, the only available fishery data relate to catches and landings.
In European countries with an existing EMP, recreational fishery capacity and catches
and landings data are documented, except from United Kingdom and Spain (Table
7.3). But among the countries reporting data, Denmark, Germany and Belgium do not
collect effort data. Only Lebanon records fishery data in the case of the Mediterranean
countries without an existing EMP within the remit of the EC Eel Regulation (European
Commission, 2007).
Most of the EU countries record WFD data and are able to determine eel abundance
using these surveys (Table 7.4) even if this abundance might be underestimated in most
of the cases because few of them have eel specific surveys. In the same way, except
from Spain, all the countries having commercial fisheries have implemented DCF and
record biological data within this framework. However, most of the countries where
recreational fishery is performed have not implemented DCF. Though most countries
have collected DCF data for commercial fishery, there are concems that it does not
meet the requirements for eel. Conventional marine fisheries management is built
upon regionally coordinated data collection programmes feeding into a stock-specific
assessment. Given the substantial convergence in methodologies across the ICES as-
sessed stocks (mostly age-based cohort assessments to reconstruct populations based
on catches, with a subordinate role for standing stock surveys of juveniles for assess-
ment tuning only), this allows for a substantial standardization in data collection pro-
grammes, as in the current DCF Regulation. For eel the situation is much more
complex, and the standardized approach applied to marine species is inappropriate.
The WKESDCF Workshop (ICES, 2012a) reviewed brief overviews of the data collec-
tion programmes for eel currently implemented under the DCF and the problems and
concems identified by those Member States represented at the meeting. It was evident
that Member States had adopted very different approaches to meeting the require-
ments of the DCF, further highlighting the ambiguities in the current measures relating
to diadromous species. Some Member States had collected no information because they
believed (rightly or wrongly) that the measures did not apply to diadromous species
in their waters; others had collected only the data specified in Commission Decision
2010/93, using data in assessments, but not all equally efficient or not on an annual
basis; and others had developed pilot studies to cover a wide range of sampling re-
quired to address national and international obligations for assessments. Workshop
participants identified examples of the problems that they had encountered with the
current data collection requirements for diadromous species; these included:
• Inadequate geographical coverage;
• Incompatibility of the requirements with the wide range of fishing methods
employed;
• Requirements are based on fisheries and not local river conditions (i.e. each
river basin, and part, is subject to different recruitment patterns and hum an
pressures leasing to localised differences in stock structures);
• Reduction or closure of fisheries removes the requirement to collect data;
• No fisheries-independent data collection requirement, especially in the ab-
sence of fisheries;
• No requirement to collect recruitment data;
Jo in t EIFAAC/ICES/GFCM WGEEL REPORT 2014 I 109
• Inappropriate requirements for age analysis;
• No data collection on non-fisheries anthropogenic factors affecting stocks;
• Bycatch sampling is of limited use and value;
• M aturity data are not required for assessment.
It is hoped that some of these concems can be addressed as part of the next revision of
the DCF (formerly known as EU-MAP).
There are large differences in the information recorded in national surveys among the
eel producing countries (Table 7.5). Those countries without an EMP don 't compile
data regarding recruitment or anthropogenic mortality but, they do have some popu-
lation surveys and data regarding some biological parameters.
Even the countries that already have an EMP (those in the EU), have a very different
level of information. Recruitment data are mainly collected in southem EU countries,
and these countries also have some information on populations, but some of them use
Eel specific electrofishing surveys, while others use other kinds of passive sampling
methods. Most of the EU countries collect some information that allows them to esti-
mate escapement. Even if it is not collected routinely, almost all the EU countries have
some information regarding biological parameters; but data regarding natural mortal-
ity are lacking in most cases. Some non-fishery anthropogenic mortality data are col-
lected, many countries have data on hydropower mortality; some of them have data
conceming barriers, intakes (water diversion structures) and predation. However, in
the case of predation many countries consider this mortality as natural.
In summary, most of the countries within the eel distribution range have some data
regarding fisheries, but many of them, especially the non-EU Mediterranean countries,
lack scientific (fishery-independent) eel specific surveys. The EU countries compile in-
formation within the WFD and DCF directives, but these data are 1) not available in
the non-EU countries, though some operate a similar programme, and 2) the data rec-
orded in the DCF have been shown not to be useful for stock assessment purposes.
Therefore, taking into account the common available information, a standardized ap-
proach should be based on yellow eel density; preferable from surveys, such as those
within the WFD, and if this is not available, from fisheries data (though these data are
generally in the form of cpue and will need to be converted to density estimates).
7.3 Standardized approach
One set of data that is common among most countries within the eel's natural range is
that collected as part of the Water Framework Directive (WFD) program (Table 7.4). It
consists in most cases of multispecies electric fishing assessments, distributed over a
catchment. These data have the potential to be converted into yellow eel standing stock
estimates for a catchment/ RBD / EMU, using current models (EDA, SMEPII: see Chap-
ter 5). From the yellow eel standing stock estimate, it is possible to estimate silver eel
escapement based on maturation schedule (Bevacqua et al., 2006), eye index (Pank-
hurst, 1982), colour measurements using a spectrophotometer (Durif et al, 2009a) and
/or a combination of methods (Acou et al., 2005; Durif et al, 2009b) (reviewed in Section
4.4 of WGEEL, 2010).
WFD is focused on assessing the status if fish populations in fresh and transitional wa-
ter, it has the advantage in that it is collected throughout the EU countries and the
disadvantage that similar data are not collected (currently) in the non-EU countries.
In relation to eel there are also some limitations of the data:
110 | Jo int EIFAAC/ICES/GFCM WGEEL REPORT 2014
1) In some countries eel does not contribute to the metric for assessing good
ecological status (GES) for fish and thus eel are not assessed quantitatively
as part of the program.
2 ) Sampling is undertaken on a 3- and sometime 6-year rolling program so an-
nual assessments would not be available.
3 ) It is a multispecies method and so may underestimate the eel component in
the population, but can be address through calibration of the technique
(Baldwin and Aprahamian, 2012).
4 ) Quantitative assessments for eel are mainly confined to rivers that can be
sampled using electric fishing, in most cases this means that the eel popula-
tions in lakes, large rivers, transitional and coastal waters have not been
quantitatively assessed and for these habitats the riverine estimates of silver
eel production are used as proxies for these water bodies. However, these
habitats are most effectively sampled using passive gears with catches ex-
pressed in terms of catch per unit of effort (cpue). In order to use such data
in the assessment there is a need to be able to convert the cpue estimate into
a density estimate, this would then allow the data to be integrated with that
collected using electric fishing and analysed in a similar way to that col-
lected for WFD for non-riverine habitats or non EU countries (Figure 7.1).
Though there are limitations to the dataset, it is a near universal set of data collected in
a near standard way available throughout much of the eel's distribution range. Its spa-
tial coverage may be limited as in most cases it is confined to those areas which can be
effectively sampled using electric fishing and would need to be expanded to cover
lakes, large section of river and transitional waters, especially as the latter habitats rep-
resent the majority of the wetted area in an EMU. There is the limitation that a complete
assessment, using all the data, for an EMU would only be possible on a three year (pos-
sibly six year) basis, this does not prevent partial annual assessments within the EMU,
and may be just as valid. For those countries where eel does not contribute to the metric
for the assessment of GES and therefore may not be quantitatively sampled, it may be
possible to alter protocols to include eel. It is important to note that the suggestion for
a standardized approach is based on the yellow eel component of the stock, the WFD
database is one source of such data, there may be others, but to convert yellow eel
density data into silver eel escapement the same procedure, outlined in Figure 7.1,
would still need to be followed.
Jo in t EIFAAC/ICES/GFCM WGEEL REPORT 2014 I 111
Yellow eel (Scientific and /or fishery) survey
Net/trap-
CPUE
DATA GAP
Electric fishing
Anthropogenic.
mortality
Yellow eel
Densitv
SMEPÍI/EDA
Yelloweel standing
stock SMEPIí/EDA— i
Eyeindex
Colour
Silvereel escapement
Anthropogenic.
mortaiity
Mortality
Sex ratio
Maturation
schedule
Growth rate
Silvereel production
Figure 7.1. Flow diagram show ing how yellow eel data collected as part of the WFD program and
from other sources can be used to estim ate silver eel escapement.
For such an approach there is a need to:
1 ) Undertake a study to convert cpue data to density data across a variety of
habitats, some work in this area, is currently underway in Ireland and, will
start in France in 2015, but is needed to be undertaken in a w ider range of
habitats and countries. Associated with this is a need to standardize on the
measurement of wetted area. Analysis in 2010 of the use of wetted area mod-
els for estimating silver eel production revealed a lack of consistency within
and between countries on how production area is determined and reported.
The types of habitat considered in these estimates varied between EMUs and
countries and differences were found in the estimates areas and these cre-
ated uncertainty for stock assessment at the intemational level. A consistent
approach, including all types of natural eel habitat is necessary, and may
require more data collection to inform this process (ICES, 2010b).
2 ) Validate the models (EDA, SMEP II) and other approaches outlined in
WGEEL (ICES, 2010b) to estimate silver eel escapement. A preliminary com-
parison has been made between the predictions by the silvering model
(Bevacqua et al, 2006) and the number of silver eels as determined by the
112 Joint EIFAAC/ICES/CFCM WGEEL REPORT 2014
silver index (Durif et al., 2009b). The dataset used for the validation was dif-
ferent from that used to develop the model. The test data consisted of
lengths of 1102 eels (male and female at different stages) collected in France
in different types of water habitats. The predicted number of silver eels was
very close to what the silver index determined (Figure 7.2). In the dataset
13% of the eels at were the pre-silver stage and 35% at the silver stage; the
model predicted that 41% of the eels were silver. This value is intermediate
between the estimate of strictly silver eels and a broader estimate which
would encompass pre-silver eels. Figure 7.3 shows that the model behaves
very well in the >600 mm, length classes with less than 3% difference with
the index estimations. The main difference occurs in the 500 mm length class
(6% difference).
Figure 7.2. Percentages of silver eels (blue: as determined using the silver index; green: as predicted
according to the silvering rate m odel) according to each size dass.
■ silver index
model
300 400 500 600 700 800 900 1000 1100
length class(mm)
Figure 7.3. Percentages of silver eels (blue: as determined using the silver index; green: as predicted
according to the silvering rate m odel) according to each size class.
Jo in t EIFAAC/ICES/GFCM WGEEL REPORT 2014 I 113
3 ) Spatially model life-history traits (growth, mortality, maturation schedule,
sex ratio) in order to transport parameters from data-rich to data-poor
EMUs. As an example data have been collected on the age and size of silver
eel across their natural range. The mean length of female eel increased sig-
nificantly with latitude (p <0.01), from 575 to 697 mm between 37-70° lati-
tude, explaining 4% of the variability (Figure 7.4). There was no relationship
between male size and latitude remaining constant at between 290-470 mm
(Figure 7.4).
latitude
Figure 7.4. M ean length of silver eel in relation to latitude; fem ale (red), male (blue).
Age at silvering, increased significantly with latitude for males and females (Figure
7.5). Average growth rate decreased significantly with latitude for female and male eel
(Figure 7.6).
114 | Joint EIFAAC/ICES/GFCM WGEEL REPORT 2014
laötude
Figure 7.5. M ean age of silver eel in relation to latitude; fem ale (red), male (blue).
latitude
Figure 7.6. M ean growth rate of eel in relation to latitude; fem ale (red), male (blue).
An A nalysis of Covariance (ANCOVA) m odel incorporating latitude, longitude, year
and habitat explained 35% and 62% of the variability in length and age of m ales at
silvering, respectively, and 33% and 65% of the variability in length and age of fem ales
at silvering, respectively (p < 0.01).
4 ) Combine the im pacts of anthropogenic (fisheries, hydropow er, water diver-
sion structures, barriers, predation etc.) mortality together w ith the assess-
m ent of silver eel escapem ent to estim ate overall silver eel production.
Jo in t EIFAAC/ICES/GFCM WCEEL REPORT 201 4 I 115
7.4 Recommendations
It is recom m ended that a program of research be undertaken w ith the aim of standard-
ising / cross calibrating the assessm ent m ethods used to estim ate silver eel escapem ent
from yellow eel abundance data, w ith the follow ing objectives:
1 ) Validate the m odels (EDA, SMEPII and others) and other approaches out-
lined in WGEEL (2010) that are used to estim ate silver eel escapem ent from
yellow eel abundance data.
2 ) Cross calibrate yellow eel catch per unit of effort (cpue) w ith density data
across a variety of habitats (rivers, lakes, transitional water and coastal w a-
ters).
3 ) D evelop a consistent approach to m easuring w etted area across all types of
natural eel habitat.
4 ) Spatially m odel the life-history traits currently used in the m odels (growth,
m ortality, maturation scliedule, sex ratio) in order to transport parameters
from data-rich to data-poor EMUs.
5 ) Com bine the im pacts o f anthropogenic (fisheries, hydropow er, water diver-
sion structures, barriers, predation etc.) mortality into the overall assess-
m ent of silver eel escapem ent.
7.5 Tables
Table 7.1: Coding used to classify data availability.
NP NP: "N o t Pe r t in e n t ", where th e questio n asked does n o t apply t o th e in d iv id u a l case
( for example where c a t c h d a t a are absent as there is no fishery
OR WHERE A HABITAT TYPE DOES NO T EXIST IN AN EMU).
Parameter compiled in 100% of the EMUs or country area
Parameter compiled in >50% of the EMUs or country area
Parameter compiled in <50% of the EMUs or country area
This parameter is not compiled
1 1 6 | Jo int EIFAAC/ICES/CFCM WGEEL REPORT 2014
Table 7.2. Available commercial fishery data by coimtry (blanks m ean no inform ation was availa-
ble).
Capacity Effort Catches & Land-
ings
G
la
ss
Y
el
lo
w
Si
lv
er
G
la
ss
Y
el
lo
w
Si
lv
er
G
la
ss
Y
el
lo
w
Si
lv
er
NO NP NP NP NP NP NP NP NP NP
SE NP NP NP
FI
EE
LV NP NP NP
LT NP NP NP
RU
PL NP NP NP
DE NP NP NP
DK NP NP NP
NL NP NP NP
BE NP NP NP NP NP NP NP NP NP
LU NP
IE NP NP NP NP NP NP NP NP NP
UK
FR
ES
PT NP NP NP
IT
MT NP NP NP NP NP NP NP NP NP
SI NP NP NP NP NP NP NP NP NP
HR NP NP NP
BA
ME NP NP NP
AL NP NP NP NP NP NP
GR NP NP NP NP NP NP
TR NP NP NP
CY NP NP NP NP NP NP NP NP NP
SY
LB NP NP NP NP
Jo in t EIFAAC/ICES/GFCM WGEEL REPORT 2014 I 117
Capacity Effort
Catches & Land-
ings
G
la
ss
Y
el
lo
w
Si
lv
er
G
la
ss
Y
el
lo
w
Si
lv
er
G
la
ss
Y
el
lo
w
Si
lv
er
IL
EG NP NP NP
LY
TN NP NP NP
DZ NP NP NP
MA
Table 7.3. Available recreational fishery data per by Country (blanks m ean no information was
available).
Capacity Effort
Catches &
Landings
G
la
ss
Y
el
lo
w
Si
lv
er
G
la
ss
Y
el
lo
w
Si
lv
er
G
la
ss
Y
el
lo
w
Si
lv
er
NO NP NP NP NP NP NP NP NP NP
SE NP NP NP NP NP NP NP NP NP
FI
EE
LV NP NP NP
LT NP NP NP
RU
PL NP NP NP NP NP NP
DE NP NP NP
DK NP NP NP
NL NP NP NP
BE NP NP NP
LU
IE NP NP NP NP NP NP NP NP NP
UK NP 1 NP NP .
FR NP | NP NP NP NP NP
ES
PT NP NP NP NP NP NP NP NP NP
IT
118 | Joint EIFAAC/ICES/CFCM WCEEL REPORT 2014
Capacity Effort
Catches &
Landings
MT
G
la
ss
Y
el
lo
w
Si
lv
er
G
la
ss
Y
el
lo
w
Si
lv
er
G
la
ss
Y
el
lo
w
Si
lv
er
SI
HR
BA
ME NP NP NP
AL NP NP NP NP NP NP NP NP NP
GR NP NP NP NP NP NP NP NP NP
TR NP NP NP
CY NP NP NP NP NP NP NP NP NP
SY
LB NP NP NP
IL
EG |:
LY
TN NP NP NP NP NP NP NP NP NP
DZ
MA
Jo in t EIFAAC/ICES/CFCM WGEEL REPORT 201 4 I 119
Table 7.4. Information recorded in the EU m onitoring programs by Country.
H
3 o >r §
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mcn 33 c3
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z 2 2
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2
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2 2 2
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23 23 23 Eel specific
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2 2
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2
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2 2
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2 2
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2
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2
3
2
3
2
3
2
3 Y/N
2 2
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2 2
3
2
3
2
3
2
3
2
3 Glass eel surveys
2 2
-3
2 2
3
2
3
2
3
2
3
2
3 Yellow surveys
2 2 2
3
2
3
2
3
2
3
2
3 Silver surveys
an3
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2 2
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2
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2
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2
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2
3
2
3
2
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2 2
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2
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2
3
2
3
2
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2
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2
3 Glass eel surveys
2 2 2 2
3
2
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2
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2
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2 2 2
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2
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2
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3
2
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2
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Joint
EIFAAC/ICES/G
FCM
W
CEEL
REPORT
2014
2>
O
N
H
2
r-< tnO r rca cn-< n>
2H 2-a 2a
2
a 2a
2
a
2
a 2a Y/N
2
a
2
-a
2
a
2
a
2
a
2
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2
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2
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2
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a
2
a
2
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2’-d 2-a 2a 2a 2a 2a 2a 2a Biometrics
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2
a
2-a 2a 2a 2a 2a
2
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2
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2
-a
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O
na
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a
2
a
2
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2
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2
-a
20 2a 2a 2a 2a 2a Y/N
2
-a
2
a
2
a
2
a
2
a
2
a
2
a
2
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2
-a
2
a
2
a
2
a
2
a
2
a
2
a
2
a Yellow surveys
2
-a
2
a
2
a
2
a
2
a
2
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ona
2
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2
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2
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2
a
2
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a
2
a Sex
Joint
EIFAAC/ICES/CFCM
W
CEEL
REPORT
201 4
122 Joint EIFAAC/ICES/CFCM WCEEL REPORT 2014
Table 7.5. Information recorded in national surveys per eel producing Country.
Recruitment data R in ln p -ira l n a r a m p - N n n f i s h p r u m n r -
Glass eel Young yellow eel
Population Escapement
ters tality
C
at
ch
es
C
PU
E
Su
rv
ey
Tr
ap
C
at
ch
es
C
PU
E
Su
rv
ey
Tr
ap
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l
sp
ec
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-
tr
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in
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8 ToR f (ii)) ... and work with ICES DataCentre to develop a data -
base appropriate to eel along ICES standards (and wider geogra-
phy)
8.1 Introduction
Chapter 4 of thi-s report outlines the data requirem ents and gaps for the different stock
assessm ents undertaken by the w orking group, and at the w orkshop on evaluating
progress of eel m anagem ent plans (WKEPEMP) in 2012 (ICES, 2012a). Chapter 5 refers
to the different m odels created by different countries to estim ate production and silver
eel escapem ent and their data requirements. The overall conclusion of these chapters
is the need for the collection of eel-specific data and the efficient availability of these
data to the w orking group from countries w ithin the distribution range of the eel.
WGEEL 2013 (ICES, 2013) noted a critical need for the im provem ent in the quality and
consistency of data reporting at the national and EMU level. This inconsistency in re-
porting affects the intem ational stock assessm ents and lim its our ability to provide
m anagem ent advice for the eel stock. Currently the w orking group m em bers need to
trawl through all country reports and m anually extract the relevant data. This is time
consum ing - a d igitised reporting database w ould ensure a m ore efficient use of time
at the w orking group session. The recom m endation from the WGEEL in 2013 w as a
standardization of data table formats for use in the country reports. The standardiza-
tion tables are offered as a format w hich w ill facilitate national reporting to all interna-
tional fora requiring eel data. The long-term objective of such standardization is to
facilitate the creation of an international database of eel stock parameters.
The next step in digitising and standardising the data used by the w orking group is to
address the storage issues for the data required annually for the stock assessm ents.
Currently, data are stored in various spreadsheet files and databases created by m em -
bers but u sing their institute facilities such as com puter software and servers. The time
taken to update and m aintain these databases is done on a voluntary basis. This is not
a good long-term strategy how ever and therefore a structured plan for storing data
needs to be created, not least because of the im portance of the stock assessm ents in the
ICES advice and evaluation of the Eel Regulation.
8.2 WGEEL Stock Assessment database
There is a requirem ent for a reporting tem plate and database to facilitate the ease of
extracting data from the Country Reports for use in the stock assessm ent and data anal-
yses undertaken by the w orking group.
Actíort plan for developing the database
• D igitise Country Reports
• Facilitate a streamlined, standardised reportíng process in EXCEL for
the im m ediate future u sing the tem plate from WGEEL 2013; w ith the
prospect o f creating a SQL or ACCESS database w ith rem ote access for
data providers in the future.
• Circulate EXCEL tem plate to Country Report lead authors
• Facilitate Stock A ssessm ent w ith a stock assessm ent database containing:
• Recruitment tim e-series
126 | Jo in t ElFAAC/ICES/GFCM WCEEL REPORT 2014
• Research data - (to be decided in the future)
* yellow eel / standing stock data (see Chapter 7)
* silver eel data
• Encourage participation of all countries w ithin the eel distribution area and
ensure all databases can capture data from different regions. U se WGS1984
(latitude/longitude) geoereferencing.
• Countries outside EU
• ICES countries
• GFCM countries
• EIFAAC countries
8.3 Existing databases
It is not the aim of the task group to reinvent the w heel. There are a num ber of data-
bases that have been created in the past, both w ithin the w orking group and during
various intem ational projects. A discussion is required to determ ine h ow useful the
data held in these databases are to the stock assessm ents carried out by the w orking
group, and how to adopt those that can be used. In the fo llow in g text w e provide a
prelim inary consideration of som e exam ple databases.
8.3.1 Recruitment Index database
The recruitment index database w as created at the WGEEL m eeting in Rom e in 2006
(ICES, 2006) and is stored on a postgres (postgis) server accessible to the m em bers of
the WGEEL. The database w as initially designed to store a range of data from catches
to effort. To date it has on ly been used to m aintain the recruitment time-series. H ow -
ever, it has the capacity to include yellow and silver eel series. The design links a loca-
tion table w ith three tables describing either the recruitment series or the yellow or the
silver eel series, and finally to use a final table to store data (Figure 8.1).
Jo in t EIFAAC/ICES/GFCM WGEEL REPORT 2014 127
Figure 8.1. Schematic design of the eel recruitment index database.
8.3.2 EU-POSE Project-DBEEL database
The aim of the EU-POSE project (Walker et al., 2013) w as to provide EU eel scientists
and m anagers w ith a com prehensive know ledge of the techniques m ost suitable for
the assessm ent of their local eel stocks, and thereby to support the conservation and
m anagem ent of eel through the Eel M anagem ent Plan process. POSE developed a da-
tabase structure for eel (DBEEL) in order to facilitate the collation and dissem ination
of data for analysis by different m odels (see Chapter 5).
This structure (Figure 8.2) could be adopted at the international level to support the
coordinated assessm ent and m anagem ent of eel, and the intercalibrations requiring ex-
changes o f eel data. H ow ever, m anagem ent of the database is a substantial task requir-
ing resources, funding and quality control measures.
128 | Jo in t EIFAAC/ICES/GFCM WGEEL REPORT 2014
A. Geographicdata:
i. RiverBasinDistrict
ii. Catchment
iii. Riversegment
iv. Rivernode
v. lake
vi. Seaoutiet
B. Environmental data:
i. Temperature
íi. Slope
iii. Ðistancetosea
iv. Habitattype
v. Wetted area
vi. Ecological productivity
vii. Non-calcareouspercentage
C. Pressure Impact data:
í. Habitatloss
ii. EcologicalStatus
ili. Stocking
iv. Obstruction:
i. Chemical
ii. Physical
v. Predators:
i. Fishery
ii. Wildlife
Figure 8.2. Database structure for the EU-POSE DBEEL.
8.3.3 International Eel Quality Database
In recent years WGEEL has considered the risks o f reduced biological quality of (silver)
eels. The reduction of the fitness of potential spawners, as a consequence of (specific)
contam inants and diseases, and the potential m obilization of h igh loads of reprotoxic
chem icals during migration, m ight be key factors that decrease the probability of suc-
cessful m igration and reproduction. An increasing am ount of evidence indicates that
eel quality m ight be an im portant issue in understanding the reasons for the decline of
the species. A n international Eel Q uality Database already exists and is stored at In-
stituut voor Natuur- en Bosonderzoek (INBO) in Belgium . It is updated on an annual
basis by the institute w ith the relevant data, and a n ew application is currently under
developm ent. The database is a com pilation of eel quality data over the w orld, includ-
ing contam inants and diseases. The new application w ill be a m ore efficient system
(m igrating from Excel worksheets to an A ccess database) and w ill include opportuni-
ties to include m ore data fields and validation m echanism s. The database has been ex-
panded now to include all anguillid species and hence w ill be renam ed (from EEQD
(European Eel Quality Database) to EQD (Eel Q uality Database)). Further developm ent
of the database is foreseen in the future.
8.3.4 Data Collection Framework
Since 2000, an EU fram ework for the collection and m anagem ent of fisheries data has
been in place. This fram ework w as reformed last in 2008 resulting in the Data Collec-
tion Framework (DCF). Under this framework the M ember States (MS) collect, m anage
and m ake available a w id e range of fisheries data n eeded for scientific advice. The
data are collected on the basis of N ational Programm es in w hich the MS indicate w hich
data are collected, the resources they allocate for the collection and h ow data are col-
lected. M ember States m ust report annually on the im plem entation of their National
Programm es and the Scientific, Technical and Econom ic Com m ittee for Fisheries
E. Biological Processes:
i. Migration
Differentíation
iii. Maturation
iv. Mortality
V. Growth
D. Seientifio Observation data:
i. Scientificfishing
i. Electrofishing
ii. Scientific gear fishing
i. Gear characterístics
ii. M igration monitoring
Jo in t EIFAAC/ICES/GFCM WGEEL REPORT 2014 | 129
(STECF) evaluates these Annual Reports. Part of these data collected by the MS is up-
loaded in databases m anaged by the Joint Research Centre (JRC) in response to data
calls issued by DG MARE. These data are analysed by experts o f the STECF and form
the basis for scientific op inions and recom m endations form ulated in STECF reports.
The resulting scientific advice is used to inform the decision m aking process for the
C om m on Fisheries Policy (CFP).
If the recom m endations of WKESDCF (ICES, 2012a) and various STECF m eeting re-
ports are accepted, the n ew DCF (formerly to be called EU-MAP) program m e, w hen
agreed, w ill result in the collection of biological com m ercial and fishery-independent
data on eels that w ou ld prove useful for stock assessm ents by the w orking group in
the future. The WGEEL needs to consider a data call to use these data at future w orking
groups and a d iscussion should be had w ith STECF to create a platform for this to
happen on a rolling basis.
8 .4 Pros and cons for ICES DataCentre hosting an eel database
If the w orking group are successful in applying to the ICES DataCentre to host the
database, a num ber of issues m ust be addressed:
• Can ICES DataCentre hold data from countries outside the ICES area? The
w orking group works in collaboration w ith countries from ICES, GFCM and
EIFAAC. The Italian Beam Trawl Survey is carried out in areas outside ICES
countries but is hosted by the DataCentre so this is not anticipated to be a
problem for eel data.
• The data supplied to the DataCentre are public data in agreem ent w ith the
ICES data policy ('http://w w w .ices.dk/m arine-data/guidelines-and-pol-
icv/Pages/ICES-data-policy.aspxl. The only exception is com m ercial fisher-
ies data that is com m ercially sensitive inform ation and therefore commercial
data policy applies. The w orking group w ou ld need to get a data agreem ent
from all data providers in relation to data publication.
• Is there another alternative host organisation where the data remains
private but has the funds and expertise required?
• W ho has access to the database?
• It is very im portant that the w orking group can easily access the data
rem otely, so that work can progress outside the dates of annual m eet-
ings, and w hen m eetings occur in different countries. It has yet to be
established in DataCentre access w ould only be available at the ICES
headquarters in Copenhagen. Currently a copy of the recruitment da-
tabase is stored on one of the WGEEL m em ber's com puter, and R<->
postgres interaction is easy to set up.
It is the conclusion of the w orking group that the best option is to work w ith ICES
DataCentre to address the issues outlined above but that a solution m ay not be possible
w ithout needing an alternative host centre.
8.5 Work Plan fo r developing a working group database
The task of creating a standardised database for the WGEEL stock assessm ent cannot
be done w ithin the short time frame of the annual m eeting. A work plan w ith tasks has
been outlined b elow and it is the intention of the group to work on these topics over
the com ing year.
http://www.ices.dk/marine-data/guidelines-and-pol-
130 | Jo in t EIFAAC/ICES/CFCM WGEEL REPORT 2014
• Finalise additions and im provem ents to the stock assessm ent recruitment
tables.
• Create Stock A ssessm ent (Recruitment) Database Fact Sheet outlining (draft
tem plate available):
• Role of database
• O utlíne w hat is captured in the relational database
■ Tables
* Fields (units)
■ C ode requirem ents (EMU)
• O utput from database
■ Reporting requirements for WGEEL and structure, raw data/ sum -
m ary data
■ Creation of output queries
■ A ccess to export data from database
• Export to R.
• Create and fill m etadata docum ent for database (draft tem plate available)
• ICES DataCentre requires com pliance w ith the IS019115.
• The m etadata describes the data captured in the database, listing the
ow ners of the data w ith relevant contact details. The Metadata w ill
m ake it easier to retrieve, use and m anage the inform ation resource.
• C om plete DataCentre Request Form.
• Liaise w ith datacentre in the creation of:
• SQL database
• U ser friendly interface for adding data rem otely
• Suitable/relevant output queries to assist stock assessm ent process at
WGEEL
• Rem ote access to raw data for stock assessm ent at WGEEL and other eel
w orkshops created in the future
• M aintenance program m e
■ Request form s for changes/additions to colum ns in tables
■ Request form s for additional fields w ithin a colum n
* Arrangem ent in place to add tables to database for other life stages
should additional stock assessm ent analysis be created.
• Once a database tem plate and interface have been designed by ICES. The
w orking group w ill need to create a docum ent for users on h ow to fill in the
form.
• Other: liaise w ith ICES over the long-term storage of data files created at
w orking groups.
• W hat happens to files on SharePoint after a num ber o f years; are they
archived or deleted?
8 .6 Conclusion
It is proposed that all country report authors w ill adopt the digital tem plate created in
WGEEL 2013, to ensure the efficient operation of the w orking group. This efficient han-
Jo in t EIFAAC/ICES/GFCM WGEEL REPORT 2014
dling and processing o f data has been recom m ended in several previous reports (in-
cluding ICES, 2001; ICES, 2010a, ICES, 2013b). Concerted action is required in 2015 by
key m em bers o f the w orking group in cooperation w ith the ICES DataCentre, to ensure
these recom m endations are not reiterated next year.
132 | Jo in t EIFAAC/ICES/GFCM WGEEL REPORT 2014
9 ToR g) Provide guidance on management measures that can be
applied to both EU and non-EU waters
9.1 Introduction
The inform ation in this chapter w ill be im portant in gu id ing n ew participants to
WGEEL and non-EU countries as to the possible m anagem ent options that could be
applied in their regions and to considerations o f future post-evaluations of EU eel man-
agem ent plans, and of other m anagem ent plans outside of the EU.
It should be noted that there is som e disparity am ong M ember States regarding the
degree of realisation of these measures: som e M embers States appear to be im plem ent-
ing the foreseen m easures according to their schedule, w hile others are lagging behind.
H ow ever in the fo llow in g analysis, the apparent absence of m anagem ent m easures of
a particular type does not necessarily indicate a lack of appropriate action, since, for
exam ple, a country that has never had a com m ercial fishery could not be expected to
take m anagem ent m easures to control one.
D uring the creation of the Eel Regulation in 2007 the Council of the European U nion
noted that in relation to eel there are diverse conditions and needs throughout the
C om m unity w hich w ill require different specific solutions. That d iversity should be
taken into account in the planning and execution of m anagem ent m easures to ensure
protection and sustainable use of the eel population. In order to ensure that their eel
recovery m easures w ere effective and equitable, it w as necessary that M em ber States
identified the m easures they intended to take and the areas to be covered, that this
inform ation be com m unicated w id ely and that the effectiveness of the m easures be
evaluated.
To that effect Articles 2(8) & 2(10) o f the 2007 Eel Regulation 1100/2007 state that:
(8) A n Eel M anagem ent Plan m ay contain but is not lim ited to, the fo llow in g measures:
• R educing com m ercial fishing activity.
• Restricting recreational fishing.
• Restocking m easures.
• Structural m easures to m ake rivers passable and im prove river habitats, to-
gether w ith other environm ental m easures.
• Transportation of silver eel from inland waters to waters from w hich they
can escape freely to the Sargasso Sea.
• Com bating predators.*
• Temporary sw itching off hydro-electric pow er turbines.
• M easures related to aquaculture.
(10) In the Eel M anagem ent Plan, each M ember State shall im plem ent appropriate
m easures as soon as possib le to reduce the eel mortality caused by factors outside the
fishery, including hydroelectric turbines, pum ps or predators, unless this is not neces-
sary to attain the objective of the plan.
*Given that the ToR for this section related only to anthropogenic im pacts, man-
agem ent actions undertaken or proposed in relation to Combating Predators were
not included.
Jo in t EIFAAC/ICES/GFCM WGEEL REPORT 2014 1 133
9.2 Analysis of Management Measures reported
Differing m anagem ent structures w ithin the EU m ean that EMPs and assessm ent pro-
cedures vary betw een Member States. Information and data relating to m anagem ent
m easures were obtained from ICES WKEPEMP report (ICES, 2013a), previous ICES
Reports and the Country Reports to the WGEEL from 2013 & 2014, w ith the list of
Countries included in the analysis derived from Table 10.3 of the WGEEL 2013 report
(ICES, 2013b).
A total of 1362 individual m anagem ent actions w ere reported from the 81 EMUs estab-
lished by M ember States for the im plem entation of their EMPs, the precise details of
w hich can be found in ICES (2013a).
G iven the volum e of m anagem ent m easures adopted across the EU, it w as decided for
the purposes of this report to filter the available data under the classification of man-
agem ent actions listed in ICES WKEPEMP (ICES, 2013a), w hich were:
• Commercial fishery
• Recreational fishery
• H ydropow er and obstacles
• Habitat im provem ent
• Stocking
• Others
M anagem ent actions aim ed at control of commercial and/or recreational fisheries w ere
the m ost com m only adopted, w ith slightly fewer m easures addressing hydropow er
and obstacles to eel m ovem ents, and few er still im plem enting habitat im provem ent or
stocking m easures (Figure 9.1).
Commercial fishing
Recreational fishing
Hydropower and
obstacles
Habitat improvement
Stocking
Others
Figure 9.1. The proportion of m anagem ent actions of various categories im plem ented in EMPs
across the EU.
1 3 4 | Joint EIFAAC/ICES/CFCM WCEEL REPORT 2014
9.2.1 Aquaculture
Though listed in the Eel Regulation as a possible feature of m anagem ent m easures no
M ember States reported any direct actions related to aquaculture.
9.2.2 Fisheries
9.2.2.1 Commercial fishery
Across the EU, 17 countries have adopted m anagem ent m easures to reduce the im pact
of com mercial and recreational fishing on the eel stock (Figures 9.2 and 9.3). D espite
the large variety of m easures proposed by each country, they are in general devoted to
reducing fishing effort, size limit, and to im plem enting national registers for catches.
In the majority of cases such actions w ere driven by:
• im provem ents in fishery administration systems;
• the introduction or extension of closed seasons;
• a reduction in fishing effort..
The diversity of commercial fishery m anagem ent m easures w as large but the variation
w ithin these different categories w as even larger, ranging from the prohibition of spe-
cific fishing gears such as fykenets in a particular fishing area, to a total ban of com -
mercial eel fisheries (e.g. N orw ay and Ireland).
v s .
/
Figure 9.2. EU and non-EU countries adopting m anagem ent m easures affecting commercial eel
fisheries: green = m easures either in place or intended; w hite = no know n measures; grey= no data.
(D istribution of countries taking measures remains the same, for all life stages o f eel).
Jo in t EIFAAC/ICES/GFCM WCEEL REPORT 201 4 I 135
9.2.2.2 Recreational fishery
&
T '
c
• 'y
r ’
• .
Figure 9.3. EU and non-EU countries adopting m anagem ent m easures affecting recreational fish ing
for eel: green = m easures either in place or intended; w hite = no know n measures; grey= no data.
The m anagem ent m easures adopted to reduce the im pact of recreational fishing on eel
populations covered a w id e range o f actions, sim ilar in m any w ays to those u sed in the
comm ercial fisheries, and included:
• a com plete ban on targeting or capturing eel;
• restricting the fishery at certain periods or life stages (e.g. im plem enting
closed seasons);
• introducing a quota to reduce the num bers caught;
• adjusting gears and hours of fishing thereby reducing their efficiency;
• regulating the fisheries by im plem enting system s to report catches;
• increase m inim um size limit.
9.2.3 Hydroelectric turbines, pumps and obstacles
The im pact of hydroelectric turbines and proposed m itigation m easures to aid eel
m ovem ents w ere the subject of previous review s by WGEEL (ICES, 2004; 2008). Exten-
sive review s focusing on eel passage were produced by the UK Environm ent A gency
as part of their Eel M anual in 2011;
https://w w w .gov.uk/governm ent/uploads/system /uploads/attach-
m ent_data/file/297341/geho0411btqb-e-e.pdf eel passage
https://www.gov.uk/government/uploads/system/uploads/attach-
136 Joint EIFAAC/ICES/GFCM WGEEL REPORT 2014
EMP m easures that are intended to m itigate for the problem s caused by hydropow er,
pum ps and obstacles are detailed in Country Reports and their distribution across the
EU is illustrated in Figure 9.4.
It should be noted that w hilst coverage of these m easures looks w idespread across
M em ber States, m any of the m easures proposed in national or EMU eel m anagem ent
plans have not yet been im plem ented or are only partially im plem ented. A ll continen-
tal life-history stages of eel can be adversely affected by these type of m igratory im-
passes. Juvenile eels (glass eel and sm all yellow eels) m ay be obstructed in their
upstream m igrations. Silver eels, and large yellow eels in som e locatíons, can be de-
layed in downstream m igration due to river discharge regulation and they are likely
to experience significant m ortality rates associated w ith passage downstream through
pow er generation facilities. Such mortalities, and non-fatal injuries, can result from ei-
ther im pingem ent at turbine intake screens or follow ing entrainment and passage
through turbines. Similar adverse effects on eels can occur at pum ping stations, though
generally EMP m easures do not specifically address these. H ow ever, m any of the hy-
dropow er m itigation m easures are also relevant to problem s associated w ith pum ping
stations and other anthropogenic obstacles im peding riverine eel m igrations.
Facilitation of natural upstream m igration in hydropow er im pacted eel populations
has been proposed by eight countries in respect of glass eel and nine countries in re-
spect o f sm all yellow eel. This in volves either rem oval of barriers or installation of ap-
propriate eel pass structures. Likewise, rem oval of obstacles and/or provision of eel
pass facilities has been proposed by nine countries for larger yellow eels and by five
countries for silver eel m igrating downstream .
M anagem ent m easures involving hydropow er plant operational protocols or design
features are proposed m easures in eleven M ember States, though the specific details
are unclear or are subject to future technology advances. A short to m edium -term
m easure included in the EMPs for several countries is the trapping of silver eels up-
stream of hydropow er dam s for release downstream . This m easure also provides in-
com e for eel fisherm en affected by EMP restrictions on com m ercial eel capture as their
skills are re-em ployed in such conservation fisheries. Research and surveys to docu-
m ent the im pact of hydropow er on eel populations of individual EM Us have been pro-
posed by seven countries and a number of others listed a sm all num ber of "other"
related m easures that appear to be of lim ited applicability to EMPs elsew here.
Jo in t EIFAAC/ICES/CFCM WGEEL REPORT 2014 I 1 37
«
°-«-o /
Figure 9.4. EU and non-EU countries adopting management measures relating to hydropower and
obstacles: green = measures either in place or intended; white = no known measures; grey= no data.
9.2.4 Habitat improvement
M easures categorised as habitat im provem ent in the ICES WKEPEMP report (2013a)
and the Country Reports to the WGEEL in 2014 (see Annex 10) w ere reported by only
six M ember States. The specific m easures taken com prise a variety of actions that are
often som ew hat vague in nature, ranging from those broadly relating to increasing
habitat connectivity, and water quality im provem ent, to the adoption of protected ar-
eas, and the benefit to the eel as a consequence of the application of the Water Frame-
work Directive. Broad similarity of m easures betw een countries cannot be assum ed.
The distribution of habitat im provem ent m easures by country affecting all eel life
stages is show n in Figure 9.5. Maps for individual life stages are identical, since habitat
im provem ent m easures generally have w id e ranging im pacts that affect all life stages.
138 | Joint EIFAAC/ICES/CFCM WGEEL REPORT 2014
Figure 9.5. M anagem ent measures related to Habitat Improvement taken by country affecting all
eel Iife stages: green = measures either in place or intended; w hite = no know n measures; grey= no
data.
9.2.5 Stocking
In 2008, prior to the inception of EMPs in 2009, tw elve countries proposed the use of
stocking in their m anagem ent plans to enhance eel populations. In 2013, stocking of
glass eel w as undertaken in 16 Member States (Figure 9.6). W hilst stocking is a measure
featuring in virtually all of the EMPs for w hich there are data, on ly six achieved their
EMP stocking target. M ost EMUs have partially reached their targets and a few have
yet to im plem ent the action (ICES, 2013a).
The m ost com m on reason given for a country being unable to achieve its stocking tar-
get w as a lack of funding to buy glass eel. The im pact of hold ing and m aintenance-
feeding of elvers in aquaculture needs to be addressed w ith regard to their potential
adaptation to culture conditions w hich are subsequently deleterious w hen stocked out,
as know n from other fish species like salm on and trout.
G iven the unknow n nature of som e of the eel pathogens in the w ild , biosecurity m ust
be of h ighest priority in any transport/translocation or eel culture system . A ll equip-
ment, vehicles, tanks, personnel and clothing m ust be thoroughly disinfected before
and after any contact w ith eels and critical control points should be established at all
rearing/holding facilities. Stocking w ith on grow n you ng yellow eel carries the risk of
spreading disease, reduced genetic fitness and skew ed sex ratios, w hile the stocking of
w ild-caught you ng yellow eels from clean donor sites m ay be deleterious if they are
stocked in contam inated recipient sites (Walker et a l, 2009).
Jo in t EIFAAC/ICES/CFCM WGEEL REPORT 201 4 | 139
C oncem s about current eel stocking practices have been expressed and its effective
contribution to ensure increased silver eel production has been raised. It has been rec-
om m ended that there should be a co-ordinated marking program m e of stocked eel and
thereby separable from w ild eel in subsequent sam pling.
The effects of stocking under EMPs cannot be dem onstrated im m ediately because of
the generational lag tim e but recent Swedish work indicates that stocked eels behave
in the sam e w ay as natural recruits (ICES, 2013b).WGEEL review ed the use of stocking
as a m anagem ent m easure in their reports from 2010 and 2013 (ICES 2010 & 2013b).
There w as alm ost no n ew evidence available to WGEEL in 2013 that w as not consid-
ered by ICES WGEEL in its 2010 report and the conclusions of both are similar, i.e. that
there is evidence that translocated and stocked eel can contribute to yellow and silver
eel production in recipient waters, but that evidence of further contribution to actual
spaw ning is lim ited (by the general lack of know ledge of the spaw ning of any eel).
T
4
<•
„ O *
Figure 9.6. M anagem ent m easures related to Stocking taken by country: green = m easures either in
place or intended; w hite = no know n measures; grey= no data.
9 .2 .6 Other management options
Other m anagem ent options listed by Member States in their EMPs and associated Re-
ports, include a w id e range of actions, none of w hich effectively refer strictly to man-
aging an anthropogenic im pact but m ostly to other issues ranging from legal
fram ework enhancem ent to m onitoring and research.
Other m anagem ent options essentially fall under eight m ain subgroups:
1 ) Strengthening of the framework, including:
1.1) Reinforcem ent of legal framework;
140 I Jo in t EIFAAC/ICES/CFCM WCEEL REPORT 2014
1.2 ) Reinforcem ent of co-ordination am ong agencies and interested par-
ties;
1.3 ) D issem ination, raising of awareness;
1.4) Stakeholders' involvem ent.
2 ) Reinforcem ent of fishery reporting structures, including
2 .1 ) Setting up of fisheries reporting system s (other than DCF);
2.2 ) U se of im port/export data to m onitor com m ercial fisheries;
2.3 ) U se of catch/return logbooks to m onitor com m ercial fisheries;
2 .4 ) Im provem ent of fisheries control (enforcement);
2.5 ) Control and contrast of illegal fisheries (enforcement).
3 ) Reinforcem ent of m onitoring frameworks, including
3 .1) Catchm ent surveys, by fykenet or electrofishing (both m ultispecific
or eel-specific) in defined catchments;
3 .2) Establishm ent of new , or the continuation of existing recruitment
m onitoring, m ost specific for glass eel and m any aim ing at investigat-
ing potential n ew sites;
3.3 ) A ssessm ent of sites for silver eel m onitoring, the im plem entation of
or continuation of escapem ent monitoring;
3.4 ) Continuation of m onitoring of index rivers.
4 ) A ssessm ent of efficacy of technical actions, to
4.1 ) Enhance accessibility and m igration routes;
4.2 ) Reduce im pacts and losses on eel populations.
5 ) A ctions related to restocking, including
5.1 ) Identification of areas for restocking;
5.2 ) Im plem entation of restocking plans;
5.3 ) Investigations of contribution of stocking to the eel stock;
5.4 ) Pilot studies for restocking actions.
6 ) A ctions related to eel quality issues and fish health, such as
6 .1) M onitoring of Anguillicola crassus;
6.2 ) Investigations on pathogens and contamination;
6.3 ) Im plem entation of sanitary agreem ents specific for dealers;
6.4 ) Assurance of com pliance to Fish H ealth Directive.
7 ) Inclusion of eel w ithin specific conservation or species protection pro-
gram m es.
8 ) Research actions, generic or specifically aim ed at:
8 .1 ) D evelopm ent of m odels for the assessm ent of stock indicators;
8.2 ) D evelopm ent of m odels to assess com pliance w ith targets;
Joint EIFAAC/iCES/GFCM WCEEL REPORT 2014
8.3 ) Development of indices for assessing management effectiveness;
8.4 ) Setting up of river or basin indexes for recruitment and escapement
quantification;
8.5 ) Development of ecosystem-based models specific for eel;
8.6 ) Retrieving and analysing historical data.
Some of these actions refer specifically to eel stage, i.e. glass eel, yellow and silver eel:
such is the case with specific monitoring targeting recruitment, yellow eel stock or es-
capement. Most of the management options listed here refer to all eel life stages be-
cause they are generic or aimed at enhancing the knowledge base or the general
working framework.
9.3 Post-evaluation
In 2013, the European Commission stated that Member States have been progressively
implementing more and more management measures as foreseen in their EMPs. These
measures include fisheries restrictions, restocking, facilitation of upstream and down-
stream migration, etc. There is however some disparity among Member States regard-
ing the degree of realisation of these measures: some Members States appear to be
implementing the foreseen measures according to schedule, while others are lagging
behind. Some of the most challenging measures to implement are the removal or mod-
ification of large obstacles, usually due to technical and financial constraints. The re-
covery plans have only been in place for several years with many having been
submitted late (ranging from several months to almost two years after the deadline).
Given that it will take at least 2-3 eel generations (i.e. at least ten years) before any
significant trends in the stock status can be observed, it is too early to draw conclusions
as to the effectiveness of these measures.
Of the 81 EMUs established by Member States for the implementation of their EMPs,
progress was made in implementing management measures related to fisheries, but
other anthropogenic management measures, such as improving habitats and passage,
or achieving stocking targets have often been postponed or only partially imple-
mented.
Following the 2012 EMP Reviews (ICES, 2013a) it remains difficult to assess the out-
come of EMPs against the 40% escapement target set by the Eel Regulation. The scien-
tific advice gleaned from the sources examined underlines that the effectiveness of
individual management measures cannot always be demonstrated: necessary data are
missing or the measures concemed are not expected to produce their effects immedi-
ately or in the short term. For instance, there is high probability that restrictions on
fisheries for silver eel have contributed to increase in silver eel escapement. However,
management measures targeting eels prior to the silver eel stage (e.g. stocking) are not
expected to have yet contributed to increased silver eel escapement due to generational
lag time (ranging from approximately five years in the Mediterranean lagoons to 25-
30 years in Northem Europe). Non-fisheries measures related to hydropower, pump-
ing stations and migration obstacles are also difficult to evaluate at this point in time,
mainly due to the site specific nature of potential impacts and lack of post evaluation
data.
142 | Joint EIFAAC/ICES/GFCM WGEEL REPORT 2014
The post-evaluation process commencing with the reporting by Member States in 2012
has been first and foremost a synchronized process of national post-evaluations. Na-
tional reports have evaluated to what extent the implementation of the EMP(s) has
been successful, and whether the targets have been achieved.
9.4 Conclusions
The stock in the whole distribution area is considered to constitute one single panmictic
population (Palm et al., 2009; Als et a l, 2011). This contrasts strongly with the scattered,
small-scale pattern of the continental stock and the national/regional scale of manage-
ment (Dekker, 2000; 2008). Management of the stock by uniform measures all over the
EU (e.g. a common minimum legal size, a common closed season or a shared catch
quotum, etc.) were not feasible or applied, since uniform measures cannot be designed
in a way that would be effective all over the EU (or the wider range of the eel) due to
large variations in eel life history over its natural range.
Regionalised management (a common objective and target, but local action planning,
local measures and local implementation) is central to the EU Eel Regulation (Dekker,
2004; 2009) and on this basis Eel Management Plans have been developed per coun-
try/region. Few cross-boundary EMPs exist. Note, however, that the European eel
range extends beyond the EU and that the management of the eel and anthropogenic
impacts are necessary throughout its range. As such it is hoped that the information
above will be an important and useful reference to new participants to WGEEL and
non-EU countries, suggesting possible management options which could be applied in
their regions and to considerations of future post-evaluations of implemented manage-
ment actions.
9.5 Recommendations
We recommend a comprehensive evaluation of the effectiveness of various manage-
ment measures across EU and non-EU waters facilitating the prioritisation of manage-
ment actions.
Management guidelines have been produced on various topics; it is recommended that
these are hosted on the EIFAAC web site, so that their specific details can be scruti-
nised.
Joint EIFAAC/ICES/GFCM WGEEL REPORT 2014 I 143
Annex 1: Reference list
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144 | Joint EIFAAC/ICES/GFCM WGEEL REPORT 2014
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Joint ElFAAC/ ICES/GFCM WCEEL REPORT 2014 I 147
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P a l m , S ., D a n n e w i t z , J ., P r e s t e g a a r d , T ., W ic k s t r o m , H . 2 0 0 9 . P a n m ix i a i n E u r o p e a n e e l r e v i s i t e d :
n o g e n e t i c d i f f e r e n c e b e t w e e n m a t u r i n g a d u l t s f r o m s o u t h e r n a n d n o r t h e m E u r o p e . H e r e d -
i t y , 1 0 3 , 8 2 - 8 9 .
P a n k h u r s t , N .W . 1 9 8 2 . R e la t i o n o f v i s u a l c h a n g e s t o t h e o n s e t o f s e x u a l m a t u r a t io n i n t h e E u r o -
p e a n e e l , A n g u i l l a A n g u i l l a (L .) . J o u r n a l o f F i s h B i o l o g y 2 1 : 1 2 7 - 1 4 0 .
P l u m m e r , M . 2 0 1 3 . P a c k a g e 'r ja g s '. T h e c o m p r e h e n s i v e R a r c h i v e n e t w o r k <h t t p : / / c r a n .r - p r o -
j e c t .o r g /> .
P o o l e , W .R ., R e y n o l d s , J .D .R . a n d M o r ia r t y , C . 1 9 9 0 . O b s e r v a t i o n s o n t h e s i l v e r e e l m i g r a t i o n s
o f t h e B u r r i s h o o le r i v e r s y s t e m , I r e la n d . 1 9 5 9 - 1 9 8 8 . I n t . R e v u e G e s H y d r o b i o l . 7 5 (6 ); 8 0 7 -
8 1 5 .
R e id , K . B . 2 0 0 1 . T h e d e c l i n e o f A m e r ic a n e e l ( A n g u i l l a r o s t r a ta ) i n L a k e O n t a r i o /S t L a w r e n c e
R iv e r e c o s y s t e m : a m o d e l l i n g a p p r o a c h t o id e n t i f i c a t i o n o f d a t a g a p s a n d r e s e a r c h p r io r i t i e s .
A n n A r b o r , M i c h ig a n , L a k e O n t a r i o C o m m it t e e , G r e a t L a k e s F i s h e r y C o m m i s s i o n .
R ic k e r , W . E . 1 9 5 4 . S t o c k a n d R e c r u i t m e n t J o u r n a l o f t h e F i s h e r i e s R e s e a r c h B o a r d o f C a n a d a ,
1 1 (5 ) : 5 5 9 - 6 2 3 . d o i : 1 0 .1 1 3 9 / f 5 4 - 0 3 9 .
R o s e l l , R ., D . E v a n s a n d M . A l l e n . 2 0 0 5 . T h e e e l f i s h e r y i n L o u g h N e a g h , N o r t h e r n I r e la n d - A n
e x a m p l e o f s u s t a i n a b l e m a n a g e m e n t ? F i s h e r i e s M a n a g e m e n t a n d E c o l o g y 1 2 (6 ) : 3 7 7 - 3 8 5 .
R o s s i , R . 1 9 7 9 . A n e s t i m a t e o f t h e p r o d u c t i o n o f t h e e e l p o p u l a t i o n i n t h e V a l l i o f C o m m a c c h io
( P o D e l t a ) d u r i n g 1 9 7 4 - 1 9 7 6 . B o l l e t t in o d e Z o o l o g i a 4 6 , 2 1 7 - 2 2 3 .
S c h u l z e , T ., U . K a h l , R . J. R a d k e a n d J. B e n n d o r f . 2 0 0 4 . C o n s u m p t i o n , a b u n d a n c e a n d h a b i t a t u s e
o f A n g u i l l a a n g u i l l a i n a m e s o t r o p h i c r e s e r v o ir . J o u m a l o f F i s h B i o l o g y 6 5 (6 ) : 1 5 4 3 - 1 5 6 2 .
S p a r r e , P . 1 9 7 9 . S o m e n e c e s s a r y a d j u s t m e n t s f o r u s i n g t h e c o m m o n m e t h o d s i n e e l a s s e s s m e n t s .
In : E e l r e s e a r c h a n d m a n a g e m e n t . ( T h u r o w , F ., e d . ) , p a p e r s p r e s e n t e d t o a n E I F A C /I C E S
S y m p o s i u m , H e l s i n k i , 9 - 1 1 J u n e 1 9 7 6 , R a p o r t s e t P r o c é s - V e r b a u x d e s R é io n s , C o n s e i l I n -
t e m a t i o n a l p o u r T E x p lo r a t io n d e la M e r 1 7 4 , 4 1 - 4 4 .
T e s c h F .W . 2 0 0 3 . T h e e e l - B i o l o g y a n d m a n a g e m e n t o f a n g u i l l i d e e l s , L o n d o n , C h a p m a n H a l l ,
4 3 4 p p .
T h o r s t a d , E .B ., L a r s e n , B .M ., F i n s t a d , B ., H e s t h a g e n , T ., H v i d s t e n , N .A . , J o h n s e n , B .O ., N æ s j e ,
T .F . a n d S a n d l u n d , O .T . 2 0 1 1 . K u n n s k a p s o p p s u m m e r i n g o m á l o g f o r s l a g t i l
o v e r v á k i n g s s y s t e m i n o r s k e v a s s d r a g . N I N A R a p p o r t 6 6 1 : 1 - 6 9 . I n N o r w e g i a n .
http://cran.r-pro-%e2%80%a8ject.org/
http://cran.r-pro-%e2%80%a8ject.org/
148 1 Joint EIFAAC/ICES/GFCM WGEEL REPORT 2014
V a n D e W o l f s h a a r , K .E ., T ie n , N . , W in t e r , H .V . , D e G r a a f , M ., a n d B ie r m a n , S . 2 0 1 4 . A s p a t i a l
a s s e s s m e n t m o d e l f o r E u o o p e a n e e l ( A n g u i l l a a n g u i l la ) i n a d e l t a , t h e N e t h e r l a n d s .
K n o w l e d g s a n d M a n a g e m n t o f A q u a t i c E c o s y s t e m s , 4 1 2 , 0 2 .
V o g t } ., S o i l l e P . , e t a l. 2 0 0 7 . A p a n - E u r o p e a n r i v e r a n d c a t c h m e n t d a t a b a s e . L u x e m b o u r g , J o in t
R e s e a r c h C e n t r e - I n s t i t u t e f o r E n v ir o n m e n t a n d S u s t a in a b i l i t y : 1 2 0 .
V o l l e s t a d , L . A . a n d J o n s s o n , B . 1 9 8 8 . A 1 3 y e a r s t u d y o f t h e p o p u l a t i o n d y n a m i c s a n d g r o w t h o f
t h e E u r o p e a n e e l A n g u i l l a a n g u i l la i n a N o r w e g i a n R iv e r ; e v i d e n c e f o r d e n s i t y - d e p e n d a n t
m o r t a l i t y , a n d d e v e l o p m e n t o f a m o d e l f o r p r e d i c t i n g y i e l d . J o u r n a l o f A n i m a l E c o l o g y , 5 8 ;
9 8 3 - 9 9 7 .
V o l l e s t a d , L . A . 1 9 9 2 . G e o g r a p h i c v a r i a t io n i n a g e a n d l e n g t h a t m e t a m o r p h o s i s o f m a t u r i n g
E u r o p e a n e e l : e n v i r o n m e n t a l e f f e c t s a n d p h e n o t y p i c p l a s t i d t y . J o u r n a l o f A n i m a l E c o l o g y ,
6 1 : 1 . 4 1 - 4 8 .
W a lk e r A .M . , A p o s t o l a k i P ., P a w s o n M ., W a l t o n } ., S c u t t - P h i l l ip s J. a n d M a r t i n T . 2 0 0 9 . D e v e lo p -
i n g G u id e l in e s f o r b e s t p r a c t ic e in s to c k in g e e l f o r e n h a n c e m e n t p u r p o s e s . C e f a s P r o j e c t C 3 2 4 3
f u n d e d b y t h e F i s h e r i e s C h a l l e n g e F u n d , M a r in e & F i s h e r i e s A g e n c y , D e f r a , U K . 6 2 p p .
W a lk e r , A . M ., E . A n d o n e g i , P . A p o s t o l a k i , M . A p r a h a m i a n , L . B e a u la t o n , D . B e v a c q u a , C . B r i-
a n d , A . C a n n a s , E . D e E y t o , W . D e k k e r , G . A . D e L e o , E . D ia z , P . D o e r i n g - A r j e s , E . F l a d u n g ,
C . J o u a n i n , P . L a m b e r t , R . P o o l e , R . O e b e r s t a n d M . S c h ia v in a . 2 0 1 3 . L o t 2 : P i l o t p r o j e c t t o
e s t i m a t e p o t e n t i a l a n d a c t u a l e s c a p e m e n t o f s i l v e r e e l . F in a l p r o j e c t r e p o r t , S e r v i c e c o n t r a c t
S 1 2 .5 3 9 5 9 8 , S t u d i e s a n d P i lo t P r o j e c t s f o r C a r r y i n g o u t t h e C o m m o n F i s h e r i e s P o l i c y , B r u s -
s e l s , E u r o p e a n C o m m i s s i o n , D ir e c t o r a t e - G e n e r a l f o r M a r i t im e A f f a i r s a n d F i s h e r i e s (D G
M a r e ) : 3 5 8 p p .
W a lt e r s , C . a n d K i t c h e l l J .F . 2 0 0 1 . C u l t i v a t i o n / d e p e n s a t i o n e f f e c t s o n j u v e n i l e s u r v í v a l a n d r e -
c r u i t m e n t : i m p l i c a t i o n s f o r t h e t h e o r y o f f i s h i n g . C a n a d ia n J o u r n a l o f F i s h e r i e s a n d A q u a t i c
S c i e n c e s 5 8 : 3 9 - 5 0 .
W o o d w a r d , R . H . , a n d G o l d s m i t h , P . L . 1 9 7 0 . L e s s o m m e s c u m u l é e s . I n M a t h é m a t i q u e s e t s t a t i s -
t i q u e s p o u r l ' in d u s t r i e . M o n o g r a p h i e s IC I , 3 -1 e t 3 - 8 , P a r is .
Joint EiFAAC/ICES/CFCM WGEEL REPORT 2014 149
Annex 2: Participants list
N a m e INSTITUTE PHONE/FAX E-MAIL
Jan
A n d e r s s o n
M ír a n
A p r a h a m ia
n
S v a g z d y s
A r v y d a s
L a u r e n t
B e a u la to n
C la u d e
B e lp a ir e
M e h r e z
B e s ta
J a n is
B ir z a k s
S w e d i s h U n iv e r s i t y o f
A g r ic u l t u r a l S c ie n c e s
D e p t . o f A q u a t ic
R e s o u r c e s
I n s t i t u t e o f C o a s ta l
R e s e a r c h
S im p e v a r p 1 0 0
S E -5 7 2 9 5 F ig e h o lm
S w e d e n
P h o n e + 4 6 10-
4 7 8 4 1 1 2
j a n .a n d e r s s o n @ s lu .s e
E n v ir o n m e n t A g e n c y
R ic h a r d F a ir c lo u g h
H o u s e
K n u t s fo r d R o a d
W a r r in g to n W A 4 IH T
U n i t e d K in g d o m
F is h e r y S e r v ic e u n d e r
M in is t r y o f A g r ic u l tu r e
N a u jo j i U o s t o 8 A
K la ip e d a
L ith u a n ia
O n e m a - p ð le O n e m a -
In ra
6 5 r o u te d e S a in t B r ie u c
3 5 0 4 2 R e n n e s
F r a n c e
I N B O R e s e a r c h I n s t itu t e
f o r N a t u r e a n d F o r e s t
D u b o is la a n 14
1 5 6 0 G r o e n e n d a a l -
H o e i la a r t
B e lg iu m
D ir e c t io n G é n é r a le d e la
R lc h e e t d e
F A q u a c u ltu r e
M in is t é r e d e
l 'a g r ic u ltu r e
3 0 r u e A la in S a v a r y
1 0 0 2 T u n is B e lv é d é r e
T u n is ia
I n s t itu t e o f F o o d S a fe ty ,
A n im a l H e a lth a n d
E n v ir o n m e n t
L e ju p e s 3
R ig a
L a tv ia
P h o n e
+ 4 4 1 9 2 5 5 4 2 7 1 3
m ir a n .a p r a h a m ia n # e n v ir o n m e n t -
a g e n c y .g o v .u k
P h o n e
+ 3 7 0 6 0 3 3 6 5 5 1
P h o n e
+ 3 3 6 8 1 4 7 5 2 7 1
P h o n e
+ 3 2 4 7 5 6 7 8 9 9 2
a r v y d a s r u s n e @ g m a il .c o m
L a u r e n t .b e a u I a to n @ o n e m a .fr
C la u d e .B e lp a ir e @ in b o .b e
P h o n e + 2 1 6
7 1 8 9 0 5 9 3
F a x + 2 1 6 71 7 9 9
4 01
m e h r e z b e s t a @ g m a il .c o m
P h o n e
+ 3 7 1 6 7 6 1 2 5 3 6
ja n is .b ir z a k s @ b io r .g o v .lv
mailto:jan.andersson@slu.se
mailto:arvydasrusne@gmail.com
mailto:Laurent.beauIaton@onema.fr
mailto:Claude.Belpaire@inbo.be
mailto:mehrezbesta@gmail.com
mailto:janis.birzaks@bior.gov.lv
150 Joint EIFAAC/ICES/GFCM WCEEL REPORT 2014
N a m e INSTITUTE P h o n e / F a x E-MAIL
C e d r ic
B r ia n d
F a b r iz ío
C a p o c c io n i
E le o n o r a
C ic c o tt i
M im o z a
C o b a n i
M a r tin
D e G r a a f
W il le m
D e k k e r
I n s t i t u t io n
d 'a m é n a g e m e n t d e la
V ila ín e
b d d e B r e ta g n e , B P l l
5 6 1 3 0 L a R o c h e
B e m a r d
F r a n c e
C o n s ig i io p e r la r ic e r c a
e la s p e r im e n t a z io n e in
a g r ic o ltu r a (C R A )
C e n tr o d i r ic e r c a p e r la
p r o d u z io n e d e l l e c a m i e
i l m ig l io r a m e n t o
g e n e t i c o (P C M )
V ia S a la r ia , 31
0 0 0 1 6 M o n t e r o t o n d o
R o m a
I ta ly
D ip a r t a m e n t o d i
B io lo g ia
U n iv e r s i t á T o r V e r g a ta
V ia d e l la R ic e r c a
S c ie n t i f ic a
0 0 1 3 3 R o m e
I ta ly
F is h e r y & A q u a c u lt u r e
s p e c ia i is t
F is h e r ie s D ir e c to r a te
M in is t r y o f
E n v ir o n m e n t , F o r e s tr y
a n d W a ter
A d m in i s t r a t io n
R m g a e D u r r e s it , N r .2 7
T ir a n a
A lb a n ia
I m a r e s
H a r in g k a d e 1
1 9 7 0 A B I jm u id e n
N e t h e r la n d s
S w e d i s h U n iv e r s i t y o f
A g r ic u l t u r a l S c ie n c e s
D e p a r t m e n t o f A q u a t ic
R e s o u r c e s
I n s t it u t e fo r F r e s h w a te r
R e s e a r c h
S t á n g h o lm s v á g e n 2
1 7 8 9 3 D r o t t n in g h o lm
S w e d e n
P h o n e
+ 3 3 2 9 9 9 0 8 8 4 4
c e d r ic .b r ia n d @ e p tb -v i la in e .fr
P h o n e + 3 9 (
9 0 0 9 0 2 6 3
fa b r iz io .c a p o c c io n i@ e n te c r a .i t
P h o n e + 39
0 6 7 2 5 9 5 9 6 9
c ic c o t t i@ u n ir o m a 2 .it
P h o n e + 3 5 5
6 7 2 0 5 5 7 7 8
M im o z a .C o b a n i@ m o e .g o v .a l
c o b a n im im i@ y a h o o .c o m
P h o n e
+ 3 1 3 1 7 4 8 6 8 2 6
P h o n e
+ 4 6 7 6 1 2 6 8 1 3 6
m a r t in .d e g r a a f@ w u r .n l
W il le m .D e k k e r @ s lu .s e
mailto:cedric.briand@eptb-vilaine.fr
mailto:fabrizio.capoccioni@entecra.it
mailto:ciccotti@uniroma2.it
mailto:Mimoza.Cobani@moe.gov.al
mailto:cobanimimi@yahoo.com
mailto:martin.degraaf@wur.nl
mailto:Willem.Dekker@slu.se
Joint EIFAAC/ICES/CFCM WGEEL REPORT 2014
N a m e INSTITUTE P h o n e / F a x E-MAIL
E s t ib a liz A Z T I-T e c n a lia A Z T I
D ía z S u k a r r ie ta
T x a tx a r r a m e n d i u g a r te a
z/g
E -4 8 3 9 5 S u k a r r ie ta
(B iz k a ia )
S p a in
C o n o r A g r i- F o o d a n d B io -
D o la n S c ie n c e s I n s t i t u t e fo r
N o r t h e m I r e la n d , A F B I
1 8 a N e w f o r g e L a n e
Belfast B T 9 5 P X
U n i t e d K in g d o m
I s a b e l C e n tr o d e
D o m in g o s O c e a n o g r a f ia /F a c u ld a d
e d e C ié n c ia s ,
U n i v e r s id a d e L is b o a
I n s t i tu t o d e
O c e a n o g r a f ia / F C U L ,
C a m p o G r a n d e
1 7 4 9 -0 1 6 L is b o n
P o r t u g a l
L F A - M V
I n s t i t u te o f F is h e r ie s
F is c h e r w e g 4 0 8
G e r m a n y
I n s t i t u t e o f M a r in e
R e s e a r c h
5 3 9 2 S to r e b o
N o r w a y
A g r i- F o o d a n d B io -
S c ie n c e s I n s t i tu t e fo r
N o r t h e r n I r e la n d , A F B I
1 8 a N e w f o r g e L a n e
Belfast B T 9 5 P X
U n i t e d K in g d o m
E u r o p e a n C o m m is s io n
R u e J o s e p h I I 9 9
B r u s s e ls
B e lg iu m
N a t io n a l M a r in e
F is h e r ie s R e s e a r c h
I n s t itu t e
u l. K o lla ta ja 1
8 1 -3 3 2 G d y n ia
P o la n d
R e in h o ld T h i in e n I n s t i t u t e o f
H a n e l F is h e r ie s E c o lo g y
P a lm a i l l e 9
2 2 7 6 7 H a m b u r g
G e r m a n y
M a lte
D o r o w
C a r o lin e
D u r if
D e r e k E v a n s
E v a n g e lia
G e o r g it s i
L u k a s z
G ie d r o jc
P h o n e
+ 3 4 6 6 7 1 7 4 4 1 2
F a x + 3 4 9 4 6 8 7 0
0 0 6
P h o n e
+ 4 4 2 8 9 0 2 5 5 6 8 9
e d ia z @ a z t i .e s
C d o la n l0 @ q u b .a c .u k
P h o n e + 3 5 1 21
7 5 0 0 9 7 0
id o m in g o s @ f c .u l ,p t
P h o n e
+ 4 9 3 8 1 8 1 1 3 4 0 3
P h o n e
+ 4 7 9 7 6 2 7 2 6 9
P h o n e + 4 4 2 8
9 0 2 5 5 5 5 1
m .d o r o w @ lfa .m v n e t .d e
c a r o lin e .d u r if@ im r .n o
d e r e k .e v a n s @ a fb in i .g o v .u k
P h o n e
+ 3 2 4 8 5 8 3 7 3 2 2
P h o n e
+ 4 8 5 1 5 9 2 0 7 1 1
E v a n g e lia .G E O R G I T S I @ e c .e u r o p a .e
u
lg ie d r o j c @ m ir .g d y n ia .p l
lu k a s z .g ie d r o jc @ m ir .g d y n ia .p l
P h o n e
+ 4 9 4 0 3 8 9 0 5 2 9 0
r e in h o ld .h a n e l@ t i .b u n d .d e
mailto:ediaz@azti.es
mailto:Cdolanl0@qub.ac.uk
mailto:idomingos@fc.ul
mailto:m.dorow@lfa.mvnet.de
mailto:caroline.durif@imr.no
mailto:derek.evans@afbini.gov.uk
mailto:lgiedrojc@mir.gdynia.pl
mailto:lukasz.giedrojc@mir.gdynia.pl
mailto:reinhold.hanel@ti.bund.de
152 | Joint ElFAAC/ICES/CFCM WGEEL REPORT 2014
N a m e INSTITUTE P h o n e / F a x E-MAIL
P ila r
H e m a n d e z
J a s o n
G o d f r e y
M e j d e d d in e
K r a ie m
E m m a n u i l
(M a n o s )
K o u tr a k is
P a tr ic k
L a m b e r t
C h ia r a
L e o n e
I n fo r m a t io n
M a n a g e m e n t O ff ic e r
G F C M S e c r e ta r ia t
F o o d a n d A g r ic u l tu r e
O r g a n is a t io n o f th e
U n i t e d N a t io n s (F A O )
V ia V it to r ia C o lo n n a 1
R o m e
I ta ly
M a r in e S c o t la n d S c ie n c e
F r e s h w a te r F is h e r ie s
L a b o r a to r y
F a s k a lly , P i t lo c h r y
P e r th s h ir e P H 1 6 5L B
U n i t e d K in g d o m
D ir e c t e u r d u
L a b o r a to ir e
d 'A q u a c u I tu r e
I n s t i t u t N a t ío n a l d e s
S c ie n c e s e t T e c h n o lo g ie s
d e la M e r
2 8 , r u e d u 2 M a r s 1 9 3 4 -
S a la m m b ö
2 0 2 5 T u n is
T u n is ia
F is h e r ie s R e s e a r c h
I n s t itu t e
H e l le n ic A g r ic u l t u r a l
O r g a n iz a t io n
N e a P e r a m o s
K a v a la
G r e e c e
N a t io n a l R e s e a r c h
I n s t i tu t e o f S c ie n c e a n d
T e c h n o lo g y fo r
E n v ir o n m e n t a n d
A g r ic u l t u r e
Ir s te a
5 0 a v e n u e d e V e r d u n
3 3 6 1 2 C e s ta s C e d e x
F r a n c e
D ip a r t ím e n t o d i
B io lo g ia
U n iv e r s i t á d i R o m a T o r
V e r g a ta
V ia d e l la R ic e r c a
S c ie n t i f ic a
0 0 1 3 3 R o m e
I ta ly
P h o n e + 39
0 6 5 7 0 5 4 6 1 7
p i la r .h e m a n d e z @ fa o .o r g
P h o n e
+ 4 4 1 2 2 4 2 9 4 4 4 4
J a s o n .G o d fr e y @ s c o t la n d .g s i .g o v .u k
P h o n e + 2 1 6 71
7 3 0 4 2 0 /5 4 8
F a x + 2 1 6 71 7 3 2
622
m e jd .k r a ie m @ in s tm .m r t .tn
P h o n e
+ 3 0 2 5 9 4 0 2 2 6 9 1
m a n o s k @ in a le .g r
P h o n e
+ 3 3 6 6 9 4 6 9 8 2 6
F a x + 33 5 5 7
8 9 0 8 0 1
p a tr ic k .la m b e r t@ ir s te a .fr
P h o n e
+ 3 9 0 6 7 2 5 9 5 9 6 7
C h ia r a .le o n e @ u n ir o m a 2 .i t
mailto:pilar.hemandez@fao.org
mailto:Jason.Godfrey@scotland.gsi.gov.uk
mailto:mejd.kraiem@instm.mrt.tn
mailto:manosk@inale.gr
mailto:patrick.lambert@irstea.fr
mailto:Chiara.leone@uniroma2.it
Joint EIFAAC/iCES/CFCM WCEEL REPORT 2014 153
N a m e i n s t i t u t e P h o n e / F a x e - m a i l
T .K . N a t io n a l I n iv e r s i ty o f P h o n e tk .m c c a r th y @ n u ig a lw a y .ie
M c C a r th y I r e la n d G a lw a y
R y a n I n s t itu te , Z o o lo g y
S c h o o l o f N a tu r a l
S c íe n c e s , N U I G
G a lw a y , I r e la n d
+ 3 5 3 8 6 4 0 1 8 2 2 3
D a n i lo U n iv e r s i t y o f P h o n e + 3 8 2 6 7 d a n i lo m r d a k @ g m a i l .c o m
M r d a k M o n t e n e g r o
F a c u l ty o f S c ie n c e s a n d
M a t h e m a t ic s
G .W a s h in g to n S tr e e t
P O 5 4 5 5
M o n t e n e g r o
2 5 5 0 3 5
T o m a s z N a t io n a l M a r in e P h o n e n e r m e r @ m ir .g d y n ia .p l
N e r m e r F is h e r ie s R e s e a r c h
I n s t itu t e
u l . K o lla ta ja 1
8 1 -3 3 2 G d y n ia
P o la n d
+ 4 8 6 6 7 5 5 5 2 5 8
M ic h a e l D a n i s h T e c h n ic a l P h o n e m ip @ a q u a .d t u .d k
I n g e m a n n
P e d e r s e n
U n iv e r s t i t y
V e js o e v e j 3 9
8 6 8 0 S ilk e b o r g
D e n m a r k
+ 4 5 3 5 8 8 3 1 0 0
C ia r a I n la n d F is h e r ie s I r e la n d P h o n e + c ia r a .o le a r y @ f is h e r ie s ir e la n d .ie
O 'L e a r y 3 0 4 4 L a k e D r iv e
C it y w e s t B u s in e s s
C a m p u s
D u b l i n 2 4
I r e la n d
3 5 3 1 8 8 4 2 6 0 0
§ iik r a n
Y a lg in
Ö z d i le k
A s s o c i a t e P r o fe s s o r
F a c u l t y o f S c ie n c e a n d
L ite r a tu r e
(J a n a k k a le O n S e k iz
M a r t U n iv e r s i t y
T u r k e y
y a lc in .o z d i le k @ g m a il .c o m
R u s s e l l M a r in e I n s t itu t e P h o n e r u s s e l l .p o o le @ m a r in e .ie
P o o le F u r n a c e , N e w p o r t
C o u n t y M a y o
I r e la n d
+ 3 5 3 8 7 6 2 9 6 3 9 2
R o b e r t A g r i - f o o d a n d P h o n e r o b e r t .r o s e l l@ a fb in i .g o v .u k
R o s e l l B io s c i e n c e s I n s t itu t e
(A F B I)
A F B I H e a d q u a r te r s
1 8 a N e w f o r g e L a n e
B T 9 5 P X B e lfa s t
U n i t e d K in g d o m
+ 4 4 2 8 9 0 2 5 5 5 0 6
mailto:tk.mccarthy@nuigalway.ie
mailto:danilomrdak@gmail.com
mailto:nermer@mir.gdynia.pl
mailto:mip@aqua.dtu.dk
mailto:ciara.oleary@fisheriesireland.ie
mailto:yalcin.ozdilek@gmail.com
mailto:russell.poole@marine.ie
mailto:robert.rosell@afbini.gov.uk
154 | Joint EIFAAC/ICES/GFCM WGEEL REPORT 2014
N a m e INSTITUTE P h o n e / F a x E-MAIL
A r g y r is
S a p o u n id is
F is h e r ie s R e s e a r c h
I n s t itu t e
H e i le n i c A g r ic u l t u r a l
O r g a n iz a t io n
N e a P e r a m o s
G r e e c e
P h o n e
+ 3 0 2 5 9 4 0 2 2 6 9 1
a s a p o u n @ in a le .g r
M a r c e llo
S c h ia v in a
P o l i t e c n ic o d i M i la n o
v ia P o n z i o 3 4 /5
M ila n o 2 0 1 3 3
I ta ly
P h o n e + 39
2 2 3 9 9 4 0 3 0
m .s c h ia v in a @ g m a il .c o m
A y e s h a E n v ir o n m e n t A g e n c y P h o n e + 4 4 a y e s h a . ta y lo r @ e n v ir o n m e n t -
T a y lo r R ic h a r d F a ir c lo u g h
H o u s e
K n u ts f o r d R o a d
W a r r in g to n W A 4 Í IH T
U n i t e d K in g d o m
1 9 2 5 5 4 2 1 6 9 a g e n c y .g o v .u k
E va
T h o r s ta d
N o r w e g ia n I n s t itu t e fo r
N a t u r e R e s e a r c h
7 4 8 5 T r o n d h e im
N o r w a y
P h o n e
+ 4 7 9 1 6 6 1 1 3 0
e v a .th o r s ta d @ n in a .n o
A la n W a lk e r
C h a ir
C e n tr e fo r
E n v ir o n m e n t , F is h e r ie s
a n d A q u a c u lt u r e
S c ie n c e (C e fa s )
L o w e s t o f t L a b o r a to r y
P a k e f ie ld R o a d
N R 3 3 O H T L o w e s t o f t
S u f f o lk
U n i t e d K in g d o m
P h o n e + 4 4 (0 )
1 5 0 2 5 6 2 2 4 4
a la n .w a lk e r @ c e fa s .c o .u k
H á k a n
W ic k s tr ö m
S w e d i s h U n iv e r s i t y o f
A g r ic u l t u r a l S c ie n c e s
D e p t . o f A q u a t ic
R e s o u r c e s
I n s t it u t e o f F r e s h w a te r
R e s e a r c h
S t á n g h o lm s v á g e n 2
1 7 8 9 3 D r o t t n in g h o lm
S w e d e n
P h o n e + 4 6 7 6 -
1 2 6 81 3 4
F a x + 46 1 0 -4 7 8
4 2 6 9
h a k a n .w ic k s t r o m @ s lu .s e
K la u s
W y s u ja c k
T h iin e n - I n s t i t u t e o f
F is h e r ie s E c o lo g y
W u lf s d o r f e r W e g 2 0 4
2 2 9 2 6 A h r e n s b u r g
G e r m a n y
P h o n e
+ 4 9 4 1 0 2 7 0 8 6 0 1
3
k la u s .w y s u ja c k @ t i.b u n d .d e
T o m a s
Z o lu b a s
F is h e r ie s S e r v ic e u n d e r
M in is t r y o f A g r ic u l tu r e
N a u jo j i u o s t o 8°
K la ip e d a
L it h u a n ia
P h o n e
+ 3 7 0 6 5 6 4 4 7 1 4
t o m a s .z o lu b a s @ z u v .l t
mailto:asapoun@inale.gr
mailto:m.schiavina@gmail.com
mailto:eva.thorstad@nina.no
mailto:alan.walker@cefas.co.uk
mailto:hakan.wickstrom@slu.se
mailto:klaus.wysujack@ti.bund.de
mailto:tomas.zolubas@zuv.lt
Joint EIFAAC/ICES/GFCM WGEEL REPORT 2014 155
Annex 3: Meeting agenda
Sunday 2nd Nov
Meeting of task leaders in the afternoon - 15:00-18.00
Monday 3rd
08.30
09.00-09.30
09:30-10:00
10:00-10:15
10.45-11.00
11.00-11.15
11.15-11.30
11.30-11.45
11.45-12.00
12.00-12.15
12.15-12.30
12.30-13:30
13:30-17:00
18:00-19:00
Tuesday 4th
08:30-09:00
09:00-17:00
17:00-18:00
19.00
Wednesday 5th
08:30-09:30
08:30-13:00
14.00-15.00
15:00-17:00
18:00
Thursday 6th
08:30-12:30
Arrival
Introductions, ToR
GFCM presentation on status of eel fisheries and aquaculture in
Mediterranean
Italian presentation on Eel escapement from Mediterranean la
goons
Country Report highlights (two slides, 5 minutes per Country)
Norway, Sweden, Latvia,
Lithuania, Poland, Denmark
Germany, Netherlands, Belgium
United Kingdom, Ireland, France
Spain, Portugal, Italy
Greece, Turkey, Albania
Montenegro, Bosnia & Herzegovina, Tunisia
Lunch
All Task Groups breakout
Sub-group/Task leaders co-ordination meeting
Plenary
All Task Groups breakout
Sub-group/Task leaders co-ordination meeting
WGEEL dinner
Introduction to WGEEL (Russell Poole, Ethiopia Room)
All Task Groups breakout
Plenary - Tasks to present key results
DEADLINE FOR DRAFT REPORT on SP
Circulate Report for comments
Reading draft chapters for content
156 Joint EIFAAC/ICES/CFCM WCEEL REPORT 2014
13:30-17:00
Friday 7th
08:30-11:00
11:00-17:00
17:00
17:00
Plenary - identify and discuss report issues
Agree Advice drafts
Task groups Revise Chapters
Final documents on SharePoint\Report 2014\Friday 1700 Re
port
Close Working Group
Joint EIFAAC/ICES/CFCM WCEEL REPORT 2014 I 157
Annex 4: WGEEL responses to the generic ToRs for Regional and
Species Working Groups
The Working Group was asked, where relevant, to consider the questions posed by
ICES under their generic ToRs for regional and species Working Groups. This was the
first time that WGEEL had directly considered these ToRs. WGEEL responses to the
generic ToR are given in the table below.
G e n e r ic T o R q u e s t i o n s WCEEL RESPONSE
F or th e eco reg ion :
a) C o n s id e r e co sy s tem o v e rv ie w s w h e re
av a ilab le , a n d p ro p o s e a n d p o ss ib ly
im p le m e n t in c o rp o ra tio n o f e co sy s tem
d r iv e rs in th e b a s is fo r adv ice .
b ) F o r th e e co reg io n o r fish e rie s (su g g est
s e p a ra te fo r g lass , y e llow , s ilv e r eel
f ish e rie s) c o n s id e re d b y th e W o rk in g
G ro u p , p ro d u c e a b r ie f r e p o r t su m m a ris in g
fo r th e s to ck s a n d f ish e rie s w h e re th e item
is re le v an t:
• M ix ed fish e rie s o v e rv ie w a n d
co n sid e ra tio n s ;
• S p ec ies in te ra c tio n e ffects a n d
eco sy s tem d riv e rs ;
• E co sy stem effec ts o f fishe rie s;
• E ffects o f re g u la to ry ch an g e s
in th e a ss e ss m e n t o r p ro jec-
tio n s;
Anguilla anguilla is a c a ta d ro m o u s sp ec ies a n d th e re fo re
o ccu p ies m a rin e , tra n s itio n a l a n d f re s h w a te r
e n v iro n m e n ts d u r in g its lifecycle. T h e e co sy s tem
fu n c tio n (ro le) o f Anguilla anguílla in e ac h o f th e se
e n v iro n m e n ts is n o t w e ll u n d e rs to o d .
A b rie f e co sy s tem o v e rv ie w w ill b e p r o v id e d in th e
in itia l W G EEL s to ck a n n ex th a t s h o u ld b e d e v e lo p e d in
2015 (see b e lo w ) a n d e n v iro n m e n ta l in f lu e n c e s o n th e
s to ck a re in c o rp o ra te d in th e a n n u a l ad v ic e a n d m a y
a d d re s s a w id e ra n g e o f fa c to rs a ffec tin g ee ls a t d iffe ren t
s tag e s in th e ir life cycle.
C o n s id e ra tio n h a s a n d w ill b e b e e n g iv en to p o ss ib le
e co sy s tem d r iv e rs in b o th f r e s h w a te r a n d th e m a r in e
e n v iro n m e n t, b u t a t p re s e n t i t is n o t p o ss ib le to
in c o rp o ra te s u c h d riv e rs in th e a s s e s s m e n t p ro cess .
i) M o st ee ls a re c a u g h t in ta rg e te d fish e rie s in c o asta l
w a te rs , tra n s itio n a l (b rack ish ) a n d f re sh w a te r . Som e
m ix e d fish e rie s d o o c cu r (e.g. G e rm a n f r e s h w a te r fyke
n e t fisheries). Eels m a y b e c a p tu re d a s b y c a tch in
co m m e rc ia l a n d rec re a tio n a l f ish e rie s (see C h a p te r 2).
T h e re is l im ite d in fo rm a tio n o n n u m b e r o f eels c a p tu re d
a s b y ca tch , o r o n th e ir su rv iv a l w h e n th e re a re
re g u la tio n s re q u ir in g o b lig a to ry re le a se o f eel c a p tu re d
in o th e r fish e rie s (for in s ta n c e b y re c re a tio n a l a n g lin g ).
T h e re a re few d a ta o n b y c a tch o f o th e r sp ec ie s in
ta rg e te d eel fish e rie s .
ii) S pecies in te ra c tio n e ffec ts a n d eco sy s tem d r iv e rs
s h o u ld b e s u m m a ris e d in th e in itia l s to ck a n n ex
p ro p o s e d fo r 2015/2016 - see a n n e x b e lo w .
iii) T h e c u rre n t f ish e ry p ro b a b ly h a s little d ire c t in flu en ce
o n a q u a tic e co sy s tem s, w ith th e p o ss ib le e x œ p tio n o f
loca l b y ca tch issu es . H o w e v e r, th e e e l is a n im p o r ta n t
jm d fre q u e n tly d o m in a tin g sp ec ie s in th e eco sy stem , a n d
its s u b s ta n tia l re d u c tio n , w h e th e r d u e to f ish e rie s o r
o th e r c au se s m a y h a v e h a d a m o re p ro fo u n d effect.
T h e re is lim ited k n o w le d g e o n th e m a g n itu d e o f th e se
effects.
iv ) In re c en t y ears , m a n y eel f ish e rie s h a v e b e e n sub jec t
to m a n a g e m e n t c o n tro ls a n d c lo su res , w ith re s u ltin g
re d u c tio n s in e x p lo ita tio n ra te s . T h is h a s re s u lte d in
in c re a s in g sen s itiv ity o f a ss e ss m e n t p ro c e d u re s to th e se
va lues.
Joint EIFAAC/ICES/GFCM WGEEL REPORT 2014
G e n e r ic T o R q u e s t io n s W G E E L RESPONSE
For all stocks:
c) If n o s to ck an n ex is a v a ilab le th is s h o u ld
b e p re p a re d p r io r to th e m ee tin g , b a se d o n
th e p re v io u s y e a r 's a s s e ss m e n t a n d fo rec a st
m e th o d u s e d fo r th e a d v ice , in c lu d in g
an a ly tic a l a n d d a ta - lim ite d m e th o d s .
d ) A u d it th e a ss e ss m e n ts a n d fo recasts
c a r r ie d o u t fo r e a c h s to ck u n d e r
c o n s id e ra tio n b y th e W o rk in g G ro u p a n d
w r i te a s h o rt re p o rt.
e) P ro p o se sp ec ific a c tio n s to b e ta k e n to
im p ro v e th e q u a lity a n d tra n s m is s io n of
th e d a ta ( in c lu d in g im p ro v e m e n ts in d a ta
co llection).
f) P ro p o se in d ic a to rs o f s to ck s ize (o r of
c h a n g e s in s to ck size) th a t c o u ld b e u s e d to
d e c id e w h e n a n u p d a te a sse ssm e n t is
r e q u ire d a n d su g g e s t th re s h o ld % (or
a b so lu te ) c h an g e s th a t th e EG th in k s
s h o u ld tr ig g e r a n u p d a te a sse ssm e n t o n a
s to ck b y s to ck b asis .
g) P re p a re p la n n in g fo r b e n c h m ark s n e x t
y ea r , a n d p u t fo rw a rd p ro p o s a ls for
b e n c h m a rk s o f in te g ra te d eco sy stem , m u lti
o r s in g le sp ec ie s fo r 2016.
h ) C h ec k th e e x is tin g s ta tic p a r ts o f th e
p o p u la r a d v ic e a n d u p d a te a s re q u ire d .
C o u n tr ie s p re p a re n a tio n a l re p o r ts a n n u a l ly fo r th e
w o rk in g g ro u p . W G E E L h a s n o t y e t d ra f te d a s to ck
an n ex to p ro v id e d e ta ils o f th e a sse ssm e n t. A s to ck an n ex
fo r W G EEL s h o u ld b e in itia te d in 2015, in c lu d in g a
p o ss ib le b e n ch m ark . W G EEL p ro p o s e s to e s ta b lis h a
b e n c h m a rk -ty p e s tu d y g ro u p in 2015 th a t w ill d e v e lo p
a n in itia l s to ck an n ex . B ased o n th is , a b e n c h m a rk
w o rk s h o p c o u ld b e h e ld in 2016. T h e fin a l o u tp u t s h o u ld
b e a b e n c h m a rk e d s to ck an n ex . A su g g e s te d S tock A n n ex
te m p la te fo r W G EEL is g iv e n b e lo w .
T h e W o rk in g G ro u p d o e s n o t ro u tin e ly a u d i t
a sse ssm en ts . In p u t d a ta a n d o u tp u ts a re c h ec k ed b y
a p p ro p r ia te c o u n try / re g io n re p re s e n ta tiv e s d u r in g e ac h
m e e tin g . S om e m o d e l d e v e lo p m e n ts h a v e b e e n su b jec t to
re v ie w b y th e W o rk in g G ro u p a n d th e m o d e llin g
a p p ro a c h e s h a v e b e e n d e sc rib e d e ith e r in th e p e e r-
re v ie w e d l i te ra tu re a n d /o r in th e SLIM E- a n d PO SE -
pro jec ts . A n u m b e r o f m e m b e rs o f th e W o rk in g G ro u p
h a v e a lso b e e n in v o lv e d in c o lla b o ra tiv e e ffo rts to
ex p lo re fu r th e r m o d e l d e v e lo p m e n ts . F o r e x am p le , close
lin k s h a v e b e e n e s ta b lish e d w ith th e E C O K N O W S
pro ject.
S tock an n ex a n d e le c tro n ic re p o r tin g a re p la n n e d to
c o n tr ib u te to im p ro v e d a ta q u a li ty in fu tu re .
F o r im p ro v e m e n ts to d a ta q u a lity , see C h a p te r 7 o f th is
re p o rt. F o r im p ro v e m e n ts to d a ta tra n sm iss io n , see
C h a p te r 8 o f th is re p o rt.
T o ta l la n d in g s a n d e ffo rt d a ta a re in c o m p le te . T h e re is a
g re a t h e te ro g e n e ity a m o n g th e tim e -se rie s o f la n d in g s
b e ca u se o f in c o n sis te n c ies in re p o r tin g b y , a n d b e tw ee n ,
c o u n tr ie s a n d in c o m p le te re p o rtin g . C h a n g e s in
m a n a g e m e n t p ra c tic es h a v e a lso a ffe c ted th e re p o r tin g o f
n o n -c o m m e rc ia l a n d re c re a tio n a l f isheries.
M an y E U M em b e r S ta te s h a v e n o t c o m p le te ly re p o r te d
s to ck in d ic a to rs (22 o f 81 E M P s d id n o t r e p o r t all
b io m a s s in d ic a to rs a n d 38 d id n o t re p o r t a ll m o r ta lity
in d ic a to rs in 2012), a n d th e re a re in c o n sis te n c ies in th e
a p p ro a c h e s u s e d to c a lcu la te re p o r te d s to ck in d ic a to rs .
T h e d is tr ib u tio n a rea o f th e eel e x te n d s c o n s id e ra b ly
b e y o n d th e EU, a n d d a ta fro m c o u n tr ie s in th e se o th e r
re g io n s w e re n o t av a ilab le . A c o m p le te re p o r tin g o f
in d ic a to rs co v er in g th e ra n g e o f th e E u ro p e a n eel is
re q u ire d fo r a fu ll a s s e ss m e n t o f th e s tock . T o fac ilita te
th is , d a ta co llection a n d an a ly s is s h o u ld be
in te m a tio n a lly s ta n d a rd iz e d .
See C h a p te r 2 o f th is re p o rt.
R ep o r tin g to th e EU ta k e s p la c e e v e ry th re e y ears , see EU
R eg u la tio n (2007-1100).
B io m ass a n d m o rta li ty in d ic a to rs a re p ro p o s e d fo r th is
p ro cess , 3Bs & A (F & H ).
A b e n c h m a rk is n o t e n v isa g e d in 2015. See a n n ex on
p ro p o s a l fo r a b e n c h m a rk - ty p e s to ck an n ex b e lo w .
See C h a p te r 2 o f th is re p o r t a n d i t is a lso u n d e r ta k e n
d u r in g th e a d v ic e d ra f t in g p ro cess .
Joint EIFAAC/iCES/GFCM WGEEL REPORT 2014 I 159
G e n e r ic T o R q u e s t io n s WGEEL RESPONSE
i) In th e a u tu m n , w h e re a p p ro p r ia te , check
fo r th e n e e d to re o p e n th e a d v ic e b a se d o n
th e s u m m e r s u rv e y in fo rm a tio n a n d th e
g u id e lin e s in A G C R E FA (2008 rep o rt) . T h e
r e le v a n t g ro u p s w ill re p o r t o n th e
A G C R E FA 2008 p ro c e d u re o n re o p e n in g o f
th e a d v ic e b e fo re 13 O c to b er a n d w ill
r e p o r t o n re o p e n e d a d v ic e b e fo re 29
O c to b er .
j) T ake in to a c c o u n t n e w g u id a n c e on
g iv in g c a tch a d v ic e (A C O M , D e cem b er
2013).
k) U p d a te , q u a lity c h eck a n d re p o r t
r e le v a n t d a ta fo r th e stock:
i) L o a d fish e rie s d a ta o n e ffo rt a n d catches
( la n d in g s , d is c a rd s , b y ca tch , in c lu d in g
e s tim a te s o f m is re p o r tin g w h e n
a p p ro p r ia te ) in th e IN T E R C A T C H d a ta b a s e
b y fishe rie s/fle e ts , e i th e r d ire c tly or, w h e n
re le v a n t, th ro u g h th e re g io n a l d a ta b ase .
D a ta s h o u ld b e p ro v id e d to th e d a ta
c o o rd in a to rs a t d e a d l in e s sp ec ified in th e
T oR s o f th e in d iv id u a l g ro u p s . D ata
s u b m itte d a f te r th e d e a d l in e s c a n be
in c o rp o ra te d in th e a ss e ss m e n ts a t th e
d ís c re t io n o f th e E x p e rt G ro u p chair;
ii) A b u n d a n c e s u rv e y resu lts ;
iii) E n v iro n m e n ta l d riv e rs .
1) P ro d u c e a n o v e rv ie w o f th e s a m p lin g
ac tiv itie s o n a n a tio n a l b a s is b a se d o n th e
IN T E R C A T C H d a ta b a s e o r, w h e re re lev a n t,
th e re g io n a l d a ta b ase .
For update advice stocks:
m ) P ro d u c e a f irs t d ra f t o f th e ad v ice o n th e
fish s to ck s a n d fish e rie s u n d e r
c o n s id e ra tio n s acc o rd in g to A C O M
g u id e lin e s a n d im p le m e n tin g th e g en eric
in tro d u c tio n to th e ICES a d v ic e (Section
1.2). If n o c h an g e in th e a d v ic e is n e e d e d ,
o n e p a g e 's a m e a d v ic e a s la s t y eari s h o u ld
b e d ra f te d .
T h is is n o t re le v a n t to W G EEL.
T h is is a d d re ss e d th ro u g h th e A d v ic e D ra ftin g G ro u p
th a t c o n v en es a f te r th e W G EEL.
See C h a p te r 2 o f th is re p o rt.
Eei d a ta a re n o t c u rre n tly in ICES D a tab a ses . D a ta
r e p o r te d u s in g a n n u a l C o u n try R ep o rts , a n d W G EEL
m a in ta in s re le v a n t d a ta b a s e s u s e d c o n sis te n tly in th e
a d v ice , s u c h a s re c ru itm e n t a n d s ilv e r ee! t im e se rie s a n d
th e Eei Q u a lity D a tab ase .
E n v iro n m e n ta l d r iv e rs a re re le v a n t a t th e loca l lev e l fo r
in d iv id u a l c a tch m e n t a sse ssm e n ts , b u t th e se a re n o t
re le v a n t a t th e in te m a tio n a l scale, w ith th e p o ss ib le
e x ce p tio n o f ocean ic e n v iro n m e n ta l in f lu en c e s o n
s p a w n in g s to ck a n d la rv a l m ig ra tio n s .
G lobal e n v iro n m e n ta l d r iv e rs a re n o t c u rre n tly
in c o rp o ra te d , o r m a y b e e v e n re le v a n t, to th e
in te m a tio n a l a sse ssm en t.
T h e In te rC a tc h d a ta b a s e is n o t u s e d b y W G EEL.
F o r d a ta b a s e a n d re c o m m e n d a tio n s fo r fu tu re d a ta
m a n a g e m e n t, see C h a p te r 8 o f th is re p o rt.
N o n e o f th e q u e s tio n s p o s e d in th is sec tio n o f th e g e n eric
T oR im p ly a ch a n g e in th e p ro c e d u re s th a t W G EEL
n o rm a lly fo llo w s e v e ry y ear. T h e is su e s ra is e d in T oR 'n '
a re a d d re s s e d ro u tin e ly in th e W G E E L re p o rt.
A d v ice is d ra f te d a n n u a l ly b y th e W G a n d re f in e d b y th e
AD G EEL.
A n in itia l s to ck a n n ex d e sc rib in g th e a sse ssm e n t
m e th o d s u s e d s h o u ld be d e v e lo p e d in 2015 (see ab o v e
a n d be low ).
160 | Joint EiFAAC/ICES/GFCM WCEEL REPORT 2014
G e n e r ic T o R q u e s t io n s __________________________ WGEEL r e sp o n se ___________________________
n ) F o r th e eel s tock , w h e n p o ss ib le p r io r to See a b o v e a n d C h a p te r 2 o f th is re p o rt.
th e m ee tin g :
i) U p d a te th e a ss e ss m e n t u s in g th e m e th o d
(an a ly tica l, fo rec a st o r t re n d s in d ic a to rs ) as
d e sc rib e d in th e s to ck annex .
ii) P ro d u c e a b r ie f r e p o r t o f th e w o rk
c a r r ie d o u t re g a rd in g th e stock,
s u m m a ris in g fo r th e s to ck s a n d fishe rie s
w h e re th e ite m is re lev an t:
1. In p u t d a ta (in c lu d in g in fo rm a tio n from
th e f ish in g in d u s try a n d N G O th a t is
p e r t in e n t to th e a ss e ss m e n ts a n d
p ro jec tio n s);
2. W h ere m is re p o r tin g o f c a tch es is
s ig n ific an t, p ro v id e q u a lita tiv e a n d w h e re
p o ss ib le q u a n ti ta t iv e in fo rm a tio n a n d
d e sc rib e th e m e th o d s u s e d to o b ta in th e
in fo rm a tio n ;
3. S tock s ta tu s a n d c a tch o p tio n s fo r n e x t
y ear;
4. H is to r ic a l p e rfo rm a n c e o f th e a sse ssm e n t
a n d b r ie f d e sc rip tio n o f q u a lity is su e s w ith
th e a sse ssm en t;
5. In c o o p e ra t io n w ith th e S ecre ta ria t,
u p d a te th e d e sc r ip t io n o f m a jo r re g u la to ry
c h a n g e s (tech n ica l m e a su re s , TACs, effo rt
c o n tro l a n d m a n a g e m e n t p la n s) a n d
c o m m e n t o n th e p o te n tia l e ffects o f su ch
ch an g e s in c lu d in g th e effec ts o f n ew ly
a g re e d m a n a g e m e n t a n d reco v ery p lan s .
D e sc rib e th e flee ts th a t a re in v o lv e d in th e
fish e ry .
o) R ev iew th e o u tc o m e s o f W K M SR REF2 See C h a p te r 3 o f th is re p o rt.
fo r th e sp ec ific s to ck s o f th e EG. C alcu la te
re fe ren ce p o in ts fo r s to ck s w h e re the
in fo rm a tio n ex ists b u t th e ca lcu la tio n s h a v e
n o t b e e n d o n e y e t a n d re so lve
in c o n sis te n c ies b e tw e e n M SY a n d
p re c a u t io n a ry re fe ren ce p o in ts if p o ssib le .
Benchmarking and development of a stock annex for European eel
The goal of a benchmark is consensus on an assessment methodology that is to be used
in future update assessments, laid down in a stock annex. This assessment methodol-
ogy can be an analytical assessment, but can also be non-analytical, for instance based
on trends in an assessment or in a selected set of (survey) indicators, with or without
forecasts. The result will be the 'best available' method that ICES advice can be based
on. ICES benchmark workshops are the normal way of benchmarking stock assessment
methodology. Hence, the term benchmark refers to methodology for assessing a fish
stock that is the result of an intense process to decide on the most appropriate scientif-
ically defensible way of interpreting or using biological knowledge, available data, and
models to address management needs.
A Benchmark workshop is set up around a group of stocks with similar issues that
need to be dealt with. Members consist of;
• Stock assessment experts;
Joint EIFAAC/ICES/GFCM WGEEL REPORT 2014
• Data collection experts;
• Experts on ecosystem /environment /fisheries information;
• Stakeholders;
• External experts (invited by ICES on the basis of the issues at hand).
The preparation of the actual workshop should be guided by an ICES convener, a stock
expert from the ICES community. The technical chair during the workshop should be
one of the external experts. The external experts are invited by ICES and are responsi-
ble for guiding the meeting on a scientific level (also during the preparation) and in the
end auditing the resulting stock annexes.
The stock annex describes the methodology agreed by the benchmark workshop and
the assumptions on which this is based; specifically:
1) the data used as basis for advice and procedures to raised data and to handle
missing data;
2 ) the methodology and standard settings of the assessment model;
3 ) the assumptions for which these settings are valid;
4) the diagnostics that should be checked to validate the assumptions;
5) reference points.
WGEEL has not yet drafted a stock annex to provide details of the assessment. As part
of the international co-ordination and planning for a standardized assessment ap-
proach for eel, a stock annex for WGEEL should be initiated in 2015, including a possi-
ble benchmark, and WGEEL proposes to establish a benchmark-type study group in
2015 to undertake this task. Based on this, a benchmark workshop could be held in
2016.
A suggested Stock Annex template for WGEEL is given below.
Suggested Stock Annex template for WGEEL
(additions or changes to the general ICES stock annex template are suggested and
marked with yellow).
A. General
A.l. Stock definition
A.2. Fishery
A.3. Ecosystem aspects
A.4. Non-fishery anthropogenic impacts
B. Data
B.l. Commercial catch
B.2 Recreational catch
B.3 Time -eries data (e.g. recruitment, silver eel)
B.4 Other data (e.g. stocking, aquaculture)
B.5 Local assessment data (e.g. WFD, DCF)
\
162 | Joint EIFAAC/ICES/CFCM WGEEL REPORT 2014
B.6. Biological
B.7. Other relevant data (e.g. habitat, eel contaminants and parasites and diseases)
C. Assessm ent: data and method
Definition of stock indicators and EU-regulation and stock recovery objectives
Description of local stock assessment models
Stock indicators (see below*)
Reference points
Development of stock indicator/management advice framework (including risk analy-
sis)
D. B io log ica l Reference Points
Biological reference points do not currently exist for eel, with the exception of the EU
escapement target, and these are under development in the working group.
The following table is an example for other species' template.
Txpe 1 'alue Technical basis
MSY
Appioacli
M S \ Bin22H X X X t Explaiu
F msv Xxx Explaiu
Precautionaiy
Approacli
Bum X X X t Explain
Bp.i X X X t Explaiu
Furn Xxx Explain
Fpa Xxx Explaiu
(Only include latest reference points, add some text if necessary)
Intemational stock assessment and quality control of local outputs.
E. O ther Issues
H.l. Historical overview of previous assessment methods (optional subsection)
F. References
* Stock ind icators
S ilver eel production (biomass)
1) Bo The amount of silver eel biomass that would have existed if no anthro-
pogenic influences had impacted the stock;
2 ) Bcurrent The amount of silver eel biomass that currently escapes to the sea to
spawn. N B - listed in the ICES template as Bpost;
3 ) Bbest The amount of silver eel biomass that would have existed if no anthro-
pogenic influences had impacted the current stock, included re-stocking
practices, hence only natural mortality operating on stock;
4) Wetted area habitat, by water type (lacustrine, riverine, transitional & la-
goon, coastal);
5 ) Production values per unit area, e.g. kg/ha.
Joint EIFAAC/ICES/GFCM WGEEL REPORT 2014
Anth ropogen ic m orta lity (impacts)
6 ) EF The fishing mortality rate, summed over the age groups in the stock, and
the reduction effected;
7) EH The anthropogenic mortality rate outside the fishery, summed over the
age-groups in the stock, and the reduction effected (e.g. turbines, parasites,
viruses, contaminants, predators, barriers, pumping stations, etc);
8 ) EA The sum of anthropogenic mortalities, i.e. EA = EF + EH. It refers to
mortalities summed over the age groups in the stock.
Restock ing requirements:
9 ) R(s*) The amount of eel (<20 cm) restocked into national waters annually.
The source of these eel should also be reported, at least to originating Mem-
ber State, to ensure full accounting of catch vs restocked (i.e. avoid 'double
banking').
164 | Joint EIFAAC/ICES/GFCM WCEEL REPORT 2014
Annex 5: Research needs
As noted throughout the WGEEL 2014 report, there are many data and knowledge
defidencies that hinder stock assessment (at local, national and international levels),
identification and quantification of impacts (natural and anthropogenic), and the de-
velopment and implementation of locally and internationally effective management
measures. With the inclusion of the GFCM countries into the WGEEL, the need for
international co-ordination and stock assessment now extends far beyond the EU and
covers the whole range of eel.
Mortality based indicators and reference points routinely refer to mortality levels as-
sessed in (the most) recent years. ICES (2011) noted that the actual spawner escapement
will lag behind, because cohorts contributing to recent spawner escapement have ex-
perienced earlier mortality levels before. As a consequence, stock indicators based on
assessed mortalities do not match with those based on measured spawner escapement.
There is therefore, a need for both biomass and mortality reference points.
The diverse range of data collection and analysis methods used by countries to estimate
their stock indicators, and the uncertainties associated with extrapolating from local to
national stock assessments mean that there are inevitable but so far unquantifiable lev-
els of uncertainty in the national and stock-wide assessments. These uncertainties need
to be addressed at local, national and intemational levels, either through standardiza-
tion of methods, setting minimum standards for data and methods (cf Data Collection
Framework (DCF)), or both.
To undertake the International Stock Assessment there are a number of components,
outlined below. These are all interrelated and will need to be addressed in a systematic
manner to maximise standardization across countries. The programme has two main
objectives; estimation of spawning-stock biomass and mortality, in the case of the latter
this has been separated into an assessment of anthropogenic and natural mortality.
1. Spawning-Stock Biomass assessment
• An intemational calibration and standardization of the methods used to es-
timate silver eel escapement from eel standing stock estimates. Calibration
between electro-fishing streams, catch per unit effort in lakes, estuaries, and
other large waterbodies; validation, and intercalibration between methods.
Links to DCF, WFD and EU Regulation.
• A coordinated programme of work should be undertaken to address the as-
sessment of densities or standing stock of eels in large open waterbodies,
such as lakes, deep rivers, transitional and coastal waters. This should in-
clude a cross-calibration of yellow eel catch per unit of effort with density
data across a variety of habitats. Links to SGAESAW, DCF, WFD and EU
Regulation;
• Spatially model the life-history traits used in the assessment models
(growth, mortality, maturation schedule, sex ratio) to transport parameters
from data-rich to data-poor EMUs;
• An international pilot study under the auspices of the new DCF is required
to establish minimum standards for data collection on the basis of current
expert judgement; to analyse achieved precision levels where adequate da-
tabases exist; and to stimulate further analysis when and where more data
become available within the framework of the DCF.
Joint EIFAAC/ICES/GFCM WGEEL REPORT 2014 I 165
• Intemational surveys at sea of eel in the spawning area in the Sargasso Sea.
Links to DCF.
2. Mortality assessment
• The stock response to implemented management actions, in terms of silver
biomass, will be slow and difficult to monitor. There is a need for developíng
methods of quantifying anthropogenic mortalities and their sum Tifetime
mortality' and estimating the same across the entire distribution of the eel.
WKESDCF recommends that the new DCF should include support for the
collection of data necessary to establish the mortality caused by fisheries and
non-fisheries anthropogenic factors. Links to DCF, WFD, EU Regulation.
• A whole eel distribution approach to assessing stocking and determining
net benefit to the stock, including an evaluation of the mortality of the
stocked fish in relation to the mortality the fish would have experienced if
left in situ. Links to EU traceability, CITES, EU Regulation and ICES advice.
• It is recommended that research to investigate factors that cause Natural
Mortalíty (M) to vary in space and time be given the high priority. Thus,
further data collection and research should be encouraged to support and
improve the knowledge of this difficult research topic in order to obtain
more reliable stock assessments. This will need to include an assessment of
density-dependent influences (DD) on eel population dynamics that occur
at the local level and whether DD will play a role at the continental scale in
the decline/recovery of the eel stock.
166 ! Joint EiFAAC/ICES/GFCM WGEEL REPORT 2014
Annex 6: Forward Focus of the WGEEL
This report is a further step in an ongoing process of documenting stock and fisheries
of the eel (A n g u i l l a a n g u i l l á ) and developing methodology for giving scientific advice
on management to effect a recovery in the international, panmictic stock.
The focus of the WGEEL in the coming years will be on the following key areas:
1) Source the appropriate assessment data from across the range of the Euro-
pean eel, by working with the EU, EIFAAC, ICES and GFCM members;
2 ) Complete development of eel-specific stock assessment methods, working
with ACOM;
3 ) Contribute to the development of a standardization and unification of the
assessment process across the entire distribution of the European eel, work-
ing with EU, EIFAAC, ICES and GFCM members;
4 ) Develop the focus of management advice on the pragmatic use of mortality
indicators (immediate impact) as intermediate or short-term goals, leaving
biomass indicators (long-term impact) for the longer-term goals, working
with ACOM and the EU Commission;
5 ) Develop an advice process for managing stock recovery and achieving sus-
tainable anthropogenic impact, by working with ACOM.
6.1 Complete data coverage
6.1.1 The contribution of GFCM countries and the Secretariat to WGEEL 2014 and fu-
ture work is welcomed and the WGEEL anticipates having new data covering a greater
distribution of eel in the near future.
The GFCM has informed that a proposal to include eel in the list of priority species
within the new GFCM Data Collection Reference Framework (DCRF) will be formu-
lated to the Scientific Advisory Committee (SAC) and relevant bodies December 2014
and March 2015. The WGEEL will be informed regularly of the outcomes of these dis-
cussions and will be consulted on the frequency of collection of biological data so these
can be aligned those in other EU countries.
The GFCM experts participating at the WGEEL 2014 agreed on a plan of action during
2014-2015 to fill some information gaps and to be in the position to provide the mini-
mum necessary set of data to be incorporated to the 2015 full international stock as-
sessment of European eel. The primary objective of this action plan is to collect current
and historical data under the guidance of WGEEL experts. These data will be gathered
by the GFCM in a standardised database. The Italian team who have some previous
experience of eel data collection and assessment in coastal lagoons will lead these ac-
tions, in consultation with some other WGEEL experts. The French experience on Med-
iterranean rivers could be also taken into account for the inland systems. A first
regional stock assessment exercise with the most suitable models could be carried out
in a two day (back-to-back) Mediterranean workshop immediately preceding the 2015
meeting of WGEEL.
Details of the action plan will be proposed to the SAC and agreed actions will be exe-
cuted in the 2014-2015 period in collaboration with ICES and EIFAAC.
Joint EiFAAC/ICES/CFCM WCEEL REPORT 2014
All these actions are subject to the approval of the SAC and the Commission and to the
allocation of funds to cover a consultant on a part-time basis and the travel expenses
to the 2015 WGEEL including the two day regional workshops preceding WGEEL 2015.
6.1.2 The WGEEL will seek data and participation from other countries, e.g. the Russian
Federation, where European eel is of interest.
6.1.3 New data from within the EU may also become available through national imple-
mentation of the EU - Multi-annual Plan (EU-MAP - the follow-on to the EU Data
Collection Framework, DCF). However, this regulation may not be implemented until
2017 or 2018 at least. Most of the recommendations of the ICES WKESDCF for the better
alignment of eel (and salmon) data collection with international and national stock as-
sessment, have been accepted but it is uncertain whether and when these might be
adopted into European fisheries legislation. The WGEEL will continue to monitor these
developments and contribute scientific expertise wherever required.
6.2 Improved methods of whole-stock assessment
The WGEEL has developed three approaches (tiers) to the international stock assess-
ment: an index based assessment (recruitment; possibly older yellow and/or silver eel
in future); the modified Precautionary Diagram derived from EU limits (the 40% bio-
mass 'target'); and, eel-specific reference points based on a tentative stock-recruitment
relationship. All three approaches have been approved in principle by the RGEEL and
ACOM in 2013, although some issues over the specifics of the stock indicator and S-R
approaches meant that the ICES Advice 2013 was based on the recruitment trend stock
assessment alone.
The data gaps in the EU limits approach remain to be filled, but it is anticipated that
the next round of national EMP Progress Reports in 2015 along with the new data from
GFCM countries will contribute substantial improvements in data coverage. There
were also some questions about the form of management advice on mortality limits,
both when eel biomass (escapement, a proxy for spawning stock) was below or above
the EU's limit reference point of 40% Bo. These questions must be resolved as a matter
of urgency.
The stock-recruitment relationship was (is) based on tentative data relationships and
assumptions about historic exploitation rates. The use of these extra data allows the
derivation of eel-specific reference points, but at the costs of uncertainties in data and
processes. The working group was not able to improve upon these source data in 2014
but will continue to pursue this.
6.3 Standardizatlon and quality assurance
There is an urgent requirement to test, and where necessary improve, the quality of
data and analyses used in deriving these stock indicators (independent review).
A full international stock assessment should include data from all parts of the natural
range of European eel. There is an urgent requirement, therefore, to support the devel-
opment of suitable assessment data in the remainder of the productive range of the
European eel.
This ICES standard approach could be developed for the European eel, adopting a
standardized international data collection (e.g. based on WFD fish monitoring of fresh
and transitional waters but modified to be eel-spedfic; see Chapter 7) and analysis to
support the intemational stock assessment. Note this international data collection and
analysis would not replace the local stock assessment (which is necessary to support
168 ! Joint EIFAAC/iCES/GFCM WCEEL REPORT 2014
local management). There is an urgent need for planning (data exchange and method-
ologies), and for tuning expectations and opportunities. The urgency of this require-
ment and the size of the task are such that it should be pursued outside the normal
annual cycle of the WGEEL. WGEEL 2014 has made proposals for study groups and
workshops to progress these actions.
6.4 Management advice based on interim mortality-based indicators
The Eel Regulation specifies a limit reference point (40% Bo) for the biomass of the es-
caping silver eel. Due to the long lifespan of eel, however, it will take at least 5-10 years
before the first effect of a management measure impacting on the glass eel or yellow
eel stage would be expected to be visible in estimates of escapement biomass. In con-
trast, the impact of management actions on mortality indicators should be apparent
almost immediately. It will be in line with the conventional ICES procedure and the
modified Precautionary Diagram to focus on immediate effects (mortality indicators
A, F and H), ignoring the inherent time lag in spawner escapement (biomass indicator).
Defining mortality targets and trajectories to reduce mortality to achieve standard ICES
targets within a defined time period would improve the chance of recovering the eel
stock.
6.5 Management advice for stock recovery
If the recent increase in recruitment indices continues, then everyone will face a new
challenge of how to manage and sustain a recovery of the productive stock, and asso-
ciated sustainable exploitation.
Annex 7: Formal recommendations of WGEEL 2014
Joint EiFAAC/ICES/CFCM WGEEL REPORT 2014 169
N u m b e r R e c o m m e n d a t io n T o
1 I n t e m a t io n a l c o o r d in a t io n w i t h c o u n t r ie s o u t s i d e th e
E u r o p e a n U n io n p u r s u e d to a c h ie v e c o m p le t e s p a t ia l
c o v e r a g e o f d a ta fo r e e l s t o c k a s s e s s m e n t .
IC E S S e c r e ta r ia t ; E U ;
G F C M ; E IF A A C
2 A s W G E E L c o n s id e r s th e e e l a l o n g - l i v e d s p e c ie s in
t e r m s o f h a r v e s t c o n tr o l r u le s , a n d p e n d i n g a n
im p r o v e m e n t o f th e a n a ly s i s o f s to c k -a n d -r e c r u it d a ta ,
W G E E L r e c o m m e n d s th a t IC E S p r o v id e s a d v ic e o n th e
b a s i s o f th e h a r v e s t c o n tr o l m l e fo r q u a n t i ta t iv e
a s s e s s m e n t s ( c a t e g o r y 1 ), i .e . a p r o p o r t io n a l r e d u c t io n
in EAiim b e l o w Biim, d o w n t o ZAiim = 0 a t B c ira t = 0 .
A C O M
3 A n I n te r n a t io n a l p r o g r a m m e o f r e s e a r c h b e
u n d e r t a k e n to s t a n d a r d iz e a n d c r o s s c a l ib r a te th e
a s s e s s m e n t m e t h o d s u s e d to e s t im a t e s i lv e r e e l
e s c a p e m e n t t h r o u g h o u t th e d is t r ib u t io n o f th e
E u r o p e a n e e l .
S C I C O M , G F C M , E U ,
E I F A A C (a l l w o r k in g w i t h
W G E E L ); s e e d r a ft
R e s o lu t io n e n c lo s e d
4 A n e x i s t i n g o r n e w w o r k s h o p i s r e q u e s t e d to c o m p il e
a n d m a k e a v a i la b le t im e - s e r ie s o f in d ic e s o f e e l q u a l it y ,
p r e fe r a b ly f r o m 1 9 5 0 fo r w a r d .
S C I C O M
5 A w o r k s h o p o n o c e a n c l im a t e in d ic e s r e le v a n t to th e
e e l (W K O C R E ), in c o o p e r a t io n w i t h W G O H c o m p i l e s
a n d m a k e s a v a i la b le t im e - s e r ie s o f in d ic e s th a t m ig h t
r e la te to th e m ig r a t o r y s u c c e s s o f s p a w n e r s a n d /o r
la r v a e in th e o c e a n .
S C I C O M
6 A w o r k s h o p / s t u d y g r o u p i s e s t a b l is h e d to a n a ly s e th e
s t o c k - r e c r u i t m e n t r e la t io n (W K E S R ) fo r t h e E u r o p e a n
e e l , t a k in g in t o a c c o u n t t h e p o t e n t ia l e f f e c t s o f s p a w n e r
q u a l i t y a n d o c e a n c l im a t e in d ic e s .
A C O M , S C IC O M
7 A S t u d y G r o u p o n E s ta b l is h in g a n E e l S to c k A n n e x
(S G E E S A ), c h a ir e d b y N N , c o u n tr y , w i l l b e e s t a b l is h e d
a n d w i l l m e e t in C o u n tr y A , x x - y y O c to b e r 2 0 1 5 a n d in
C o u n tr y B , x x - y y m o n th 2 0 1 6 to d e v e l o p a n in i t ia l s to c k
a n n e x in t w o s te p s : a ) d e f in e th e s to c k , a n t h r o p o g e n ic
im p a c t s a n d d a ta a v a ila b le fo r a s s e s s m e n t s ; b ) d e s c r ib e
th e a s s e s s m e n t m e t h o d a n d r e q u ir e d d a ta , in c lu d in g
b io lo g ic a l r e fe r e n c e p o in t s .
IC E S S e c r e ta r ia t
170 | Joint EIFAAC/ICES/GFCM WGEEL REPORT 2014
Recommendations from WGEEL to itself
N u m b e r R e c o m m e n d a t io n
In th e in t e r e s t o f lo n g - t e r m p la n n in g a n d in t e m a t i o n a l
c o - o r d in a t io n , w e r e c o m m e n d d a ta o n l i f e - h is t o r y
c h a r a c te r is t ic s b e c o l la t e d a t th e s p a t ia l s c a le o f th e e e l
m a n a g e m e n t u n i t (E M U ) a s p a r t o f t h e d e v e l o p m e n t o f
th e E u r o p e a n E e l S to c k A n n e x .
W G E E L m a k e s a v a ila b le t im e - s e r ie s o f ( r e c o n s tr u c te d )
s p a w n e r e s c a p e m e n t a n d d o c u m e n t s h o w t h is t im e -
s e r i e s h a v e b e e n d e r iv e d ; c o n s id e r s i lv e r e e l r u n
r e c o n s t r a c t io n s t o b e b a s e d o n e i t h e r s i lv e r e e l la n d in g s
d a ta , y e l l o w e e l la n d in g s d a ta , o r o t h e r h is t o r ic a l
s o u r c e s o f in fo r m a t io n
It i s p r o p o s e d th a t a l l c o u n t r y r e p o r t a u t h o r s w i l l a d o p t
t h e d ig i t a l t e m p la t e c r e a t e d in W G E E L 2 0 1 3 , to e n s u r e
th e e f f i c ie n t o p e r a t io n o f th e w o r k in g g r o u p . T h is
e f f i c ie n t h a n d l in g a n d p r o c e s s in g o f d a ta h a s b e e n
r e c o m m e n d e d in s e v e r a l p r e v io u s r e p o r ts ( in c lu d in g
IC E S , 2 0 0 1 ; IC E S , 2 0 1 0 a , IC E S , 2 0 1 3 b ) . C o n c e r te d
a c t io n i s r e q u ir e d in 2 0 1 5 b y k e y m e m b e r s o f th e
w o r k in g g r o u p in c o o p e r a t io n w i t h th e IC E S
D a t a c e n t r e , t o e n s u r e t h e s e r e c o m m e n d a t io n s a r e n o t
r e i t e r a te d n e x t y e a r .
A n in t e m a t i o n a l p r o g r a m m e o f r e s e a r c h b e u n d e r t a k e n
t o s t a n d a r d iz e a n d c r o s s c a l ib r a te th e a s s e s s m e n t
m e t h o d s u s e d to e s t im a t e s i lv e r e e l e s c a p e m e n t
t h r o u g h o u t t h e d is t r ib u t io n o f th e E u r o p e a n e e l .
ToR FOR FUTURE (LETTER
CODE INDICATES TOR 2 0 1 4 )
b ) R e v ie w t h e l i f e - h is t o r y
tr a i t s a n d m o r t a l i t y fa c to r s
b y e c o r e g io n
e ) F u r th e r d e v e l o p th e
s t o c k - r e c r u i t m e n t
r e la t io n s h ip a n d a s s o c ia t e d
r e fe r e n c e p o in t s , u s i n g th e
la t e s t a v a i la b le d a ta
f ) ( ii) w o r k w i t h IC E S
D a t a C e n tr e t o d e v e l o p a
d a t a b a s e a p p r o p r ia t e t o e e l
a lo n g IC E S s t a n d a r d s (a n d
w id e r g e o g r a p h y )
f ) (i) E x p lo r e th e
s t a n d a r d iz a t io n o f
m e t h o d s fo r d a ta
c o l le c t io n , a n a ly s i s a n d
a s s e s s m e n t
Joint EiFAAC/ICES/CFCM WGEEL REPORT 2014 | 171
Annex 8: WGEEL responses to the Technical Review Group minutes,
2013 .......................................................................................................................
The Working Group considered and responded to the Technical Review Group
minutes on the 2013 WGEEL Report. Typographical and editorial changes were made
in the 2013 report and indicated [DONE] in the Technical Minutes and won't be ad-
dressed here. Responses in this table will either indicate where the issue is addressed
in the report or a response will be made directly on the table.
No. T e c h n ic a l M in u te WGEEL response
GENERAL COMMENTS OVERVIEW
1 T h e W o r k in g G r o u p (p . 1 8 0 ) h a s a s k e d
IC E S to a d v i s e o n w h i e h o f th e th r e e
a s s e s s m e n t a p p r o a c h e s (a n a ly s is o f
r e c r u it m e n t tr e n d s , u s e o f s to c k
in d ic a t o r s b y c o u n t r y o r E M U , a n d
s in g le in t e r n a t io n a l a s s e s s m e n t ) s h o u l d
b e p u r s u e d , a l t h o u g h i t g iv e s n o
in d ic a t io n o f i t s o w n v i e w s . T h e a n s w e r
i s a ll th r e e .
2 T h e W o r k in g G r o u p s h o u l d c la r ify w h a t
d a ta n e e d t o b e o b t a in e d in o r d e r to
d e v e l o p s u c h a n in t e m a t i o n a l s p e c ie s -
w i d e a s s e s s m e n t in t h e fu tu r e .
a n t h r o p o g e n ic m o r t a l i t y ( im p a c ts ) ;
6 ) £ F T h e f i s h in g m o r t a l i t y r a te , s u m m e d o v e r th e a g e -
g r o u p s in t h e s to c k , a n d th e r e d u c t io n e f f e c t e d ;
7) T h e a n t h r o p o g e n ic m o r t a l i t y r a te o u t s i d e th e f is h e r y ,
s u m m e d o v e r th e a g e - g r o u p s in t h e s to c k , a n d th e r e d u c t io n
e f f e c t e d ( e .g . t u r b in e s , p a r a s i t e s , v ir u s e s , c o n ta m in a n t s ,
p r e d a to r s , b a r r ie r s , p u m p i n g s t a t io n s , e tc );
8 ) L A T h e s u m o f a n t h r o p o g e n ic m o r ta l i t ie s , i .e . Z A = L F +
L H . It r e fe r s to m o r t a l i t ie s s u m m e d o v e r th e a g e - g r o u p s in th e
s to c k .
r e s t o c k in g r e q u ir e m e n ts :
7 ) R (s* ) T h e a m o u n t o f e e l (< 2 0 c m ) r e s t o c k e d in t o n a t io n a l
w a t e r s a n n u a l ly . T h e s o u r c e o f t h e s e e e l s h o u l d a l s o b e
r e p o r te d , a t le a s t to o r ig in a t in g M e m b e r S ta te , to e n s u r e fu l l
a c c o u n t in g o f c a t c h v s r e s t o c k e d ( i.e . a v o id ' d o u b le b a n k in g ') .
T h e R e v ie w G r o u p s e e m s to r e fe r t o th e s e n t e n c e "A d e c i s io n
n e e d s to b e m a d e a s to w h e t h e r IC E S a c c e p t s a n y o r a l l o f th e
th r e e a s s e s s m e n t a p p r o a c h e s p r e s e n t e d " . In o u r v i e w , th e r e i s
n o d o u b t th a t a ll th r e e m e t h o d s h a v e th e ir p r o s a n d c o n s . T h e
q u e s t io n r a is e d , h o w e v e r , i s w h i c h o f th e th r e e i s c o n s id e r e d to
b e b e s t fo r p r o v id in g a d v ic e - n o t in g th a t th e m e t h o d s d if fe r
c o n s id e r a b ly in d e t a i l , in c r e d ib i l i t y a n d in s p e c i f i c i t y t o e e l . S o
fa r , a d v ic e w a s e s s e n t ia l l y b a s e d o n th e r e c r u itm e n t tr e n d s ,
w h i c h d o e s in f o r m a b o u t t h e w o r r y in g s t a t u s o f t h e s to c k , b u t
d o e s n o t in d ic a t e w h e t h e r th e im p le m e n t a t io n o f th e E e l
R e g u la t io n h a s r e s u lt e d in a d e q u a t e p r o t e c t io n o r n o t .
T h e s e w e r e d e v e l o p e d b y t h e W o r k in g G r o u p in 2 0 0 9 -2 0 1 1
a n d in c o r p o r a t e d in th e E U R e p o r t in g T e m p la t e fo r 2 0 1 2
r e p o r t in g a s f o l lo w s :
s i lv e r e e l p r o d u c t io n (b io m a s s ) :
1) Bo T h e a m o u n t o f s i lv e r e e l b io m a s s th a t w o u l d h a v e
e x i s t e d i f n o a n t h r o p o g e n ic in f lu e n c e s h a d im p a c t e d th e s to c k ;
2 ) Bcurrcnt T h e a m o u n t o f s i lv e r e e l b io m a s s th a t c u r r e n t ly
e s c a p e s to th e s e a to s p a w n . N B - l i s t e d in th e IC E S t e m p la t e
a s B p o s t;
3 ) Bbest T h e a m o u n t o f s i lv e r e e l b io m a s s th a t w o u l d h a v e
e x i s t e d i f n o a n t h r o p o g e n ic in f lu e n c e s h a d im p a c t e d th e
c u r r e n t s to c k , in c l u d e d r e - s t o c k in g p r a c t ic e s , h e n c e o n ly
n a t u r a l m o r ta l i t y o p e r a t in g o n s to c k ;
4 ) W e t te d a r e a h a b ita t , b y w a te r t y p e ( la c u s t r in e , r iv e r in e ,
t r a n s it io n a l & la g o o n , c o a s ta l) ;
5 ) P r o d u c t io n v a lu e s p e r u n i t a r e a , e .g . k g /h a .
172 Joint EIFAAC/ICES/GFCM WCEEL REPORT 2014
T h e W o r k in g G r o u p h a s a ls o r a is e d th e
i s s u e o f w h e t h e r a n n u a l a s s e s s m e n t s ,
b e t w e e n t h o s e r e q u ir e d fo r r e p o r t in g
u n d e r th e E e l R e g u la t io n , a r e n e c e s s a r y ;
t h e y a r e s a id to b e u s e f u l fo r m o n it o r in g
th e tr e n d in s t a t u s , b u t n o s t r o n g c a s e i s
m a d e f o r c o n d u c t in g t h e m . W h ile
l i m i t in g t h e a s s e s s m e n t s t o e v e r y th ir d
y e a r m ig h t p r o v id e m o r e t im e to
d e v e l o p n e w m e t h o d s , c o n s id e r a t io n
s h o u l d b e g i v e n to t h e d i f f ic u l t y o f
m a in t a in in g a n d p o p u l a t in g th e
d a t a b a s e s u s e d t o u n d e r t a k e th e
a s s e s s m e n t s i f t h e y a r e n o t u n d e r ta k e n
a n n u a l ly .
S in c e a r e b u i ld in g o b j e c t iv e h a s a lr e a d y
b e e n d e f in e d f o r t h e E u r o p e a n e e l , th e r e
i s n o n e e d t o d e v e l o p a l t e m a t e r e fe r e n c e
p o in t s . T h e o b j e c t iv e o f e x c e e d in g 40%
o f p r is t in e s p a w n in g b io m a s s h a s b e e n
t a k e n to c o r r e s p o n d t o th e te r m u s e d b y
th e W o r k in g G r o u p o f BMSYwgger (b u t s e e
c o m m e n t s b e lo w ) . A lt e r n a te o b je c t iv e s ,
b a s e d o n r e c r u itm e n t tr e n d in d ic a t o r s
(Rtarget a n d Rdown) a r e n o t u s e f u l fo r
in f o r m in g m a n a g e m e n t d e c i s i o n s a s
t h e y c a n n o t b e m e a s u r e d d ir e c t ly
a g a in s t s i lv e r e e l b io m a s s o r r e m o v a l
r a te o b je c t iv e s .
T h e d e v e l o p m e n t o f t h e r e la t io n s h ip
b e t w e e n s t o c k ( p r o x y v a lu e fo r s i lv e r e e l
b io m a s s ) a n d r e c r u itm e n t ( in d e x o f
g la s s e e l s f r o m E ls e w h e r e E u r o p e ) i s t o o
p r e l im in a r y to j u s t i f y p r o v id in g
a l t e m a t i v e , m o r e p r e c a u t io n a r y ,
r e fe r e n c e p o in t s ( B s » P a n d B s to PPa ) t o th e
40 % o f p r i s t in e b io m a s s v a lu e .
T h e P r e c a u t io n a r y D ia g r a m fo r e e l
s h o w s Bcorrent o n th e x - a x is , a n d it w o u l d
b e m o r e a p p r o p r ia t e t o s h o w Bscst ( th e
e x p e c t e d b io m a s s in t h e a b s e n c e o f
a n t h r o p o g e n ic im p a c t s ) .
In a d d i t io n , th e P r e c a u t io n a r y D ia g r a m
s h o w s t h e m a x im u m r e m o v a l ra te , 60%
( c o r r e s p o n d in g t o L A = 0 .9 2 ) , b e in g
a p p l i e d a t BMsytrigger, b u t t h i s r e m o v a l r a te
c a n o n ly b e s u s t a in e d a t o r a b o v e th e
p r is t in e b io m a s s (Bo) w it h o u t r e d u c in g
e s c a p e m e n t b e l o w 40% o f Bo.
A g r e e d . C o o r d in a t io n o f d a ta , th e ir s t o r a g e a n d a p p l ic a t io n a re
n o w d i s c u s s e d in C h a p te r s 7 a n d 8 .
T h is c o m m e n t i s d e a lt w i t h in C h a p te r 3 .
T h is c o m m e n t i s d e a lt w i t h in C h a p te r 3.
T h is c o m m e n t i s d e a lt w i t h in C h a p t e r 3 . Bb«t i s a c t u a l ly s h o w n
in th e d ia g r a m s , a s t h e s i z e o f t h e b u b b le s . T h e r e la t io n t o Bo i s
r e le v a n t , in r e la t io n to th e m a n a g e m e n t ta r g e t t o r e s to r e
s p a w n e r e s c a p e m e n t to 40% o f th e p r is t in e b io m a s s .
A g r e e d .
Joint EIFAAC/ICES/GFCM WGEEL REPORT 2014 I 173
8 W e s u g g e s t th a t e e l i s a c t u a l ly m o r e
a k in to a 's h o r t l iv e d s to c k w i th p o p u la t io n
s iz e e s t im a te s ' (IC E S 2 0 1 3 a ) b e c a u s e th e
a n t h r o p o g e n ic m o r t a l i t y i s c a lc u la t e d a s
a s in g le l i f e t im e v a lu e (E A ), a n d th a t
m o r t a l i t y o c c u r s b e f o r e th e f i s h s p a w n .
F o r s u c h s to c k s , th e IC E S M S Y a p p r o a c h
is a im e d a t a c h ie v in g a ta r g e t
e s c a p e m e n t (M S Y Bescapemem) w h ic h
w o u l d a c c o r d w i t h t h e 40% o f Bo
r e fe r e n c e p o in t s e t b y th e E U .
9 IC E S ( 2 0 1 3 a ) h a s a l s o p r o p o s e d th a t
c a t c h e s s h o u l d b e l im i t e d t o th e s t o c k
b io m a s s in e x c e s s o f t h e ta r g e t
e s c a p e m e n t , a n d th a t n o c a tc h s h o u l d b e
a l l o w e d u n l e s s t h e e s c a p e m e n t c a n b e
a c h ie v e d e a c h y e a r . O n th is b a s is ,
F ig u r e 6 -1 m ig h t ta k e th e f o r m o f F ig u r e
1 (T ec h M in u t e s ) .
1 0 D e p e n s a t i o n i s a g a in h ig h l ig h t e d b y th e
W o r k in g G r o u p a s a p r o c e s s w h ic h m a y
b e a f f e c t in g E u r o p e a n e e l . T h e e v id e n c e
p u t f o r w a r d to s u p p o r t t h e d e p e n s a t io n
h y p o t h e s i s i s a s to c k a n d r e c r u itm e n t (S -
R ) r e la t io n s h ip th a t i s b a s e d o n a p a r t ia l
in d e x o f s i lv e r e e l s p a w n in g e s c a p e m e n t
a n d a r e la t iv e in d e x o f g la s s e e l
r e c r u itm e n t . I n th e IC E S r e v ie w o f th e
2 0 1 2 W G E E L r e p o r t (IC E S 2 0 1 2 , A n n e x
1 1 ) , a lt e r n a te h y p o t h e s e s fo r t h e p a t t e m
in g la s s e e l in d ic e s a n d s i lv e r e e l in d ic e s
w e r e d e s c r ib e d . T h e s e a l t e m a t iv e
h y p o t h e s e s a r e s t i l l w o r t h y o f
c o n s id e r a t io n . D e p e n s a t i o n i s d e f in e d in
S -R a n a ly s i s a s r e c r u it s p e r s p a w n e r th a t
in c r e a s e f r o m th e o r ig in a n d th e n
d e c l in e a t a n in t e r m e d ia t e s p a w n e r
a b u n d a n c e . T h e c a u s a l m e c h a n is m s o f
d e p e n s a t i o n a r e p r im a r i ly a s s o c ia t e d
w i t h A l l e e e f f e c t s , b y w h i c h s p a w n in g
s u c c e s s i s c o m p r o m i s e d b y l o w s p a w n e r
a b u n d a n c e . T o d e m o n s t r a t e
d e p e n s a t io n , th e r e c r u it s a n d s p a w n e r s
m u s t b e in s im ila r u n i t s . P r o d u c t io n o f
g la s s e e l th a t i s l o w r e la t iv e t o h is to r ic
a b u n d a n c e i s n o t s u f f i c ie n t to
d e m o n s t r a t e d e p e n s a t io n .
T h is c o m m e n t i s d e a lt w i t h in C h a p t e r 3 .
T h is c o m m e n t i s d e a lt w i t h in C h a p te r 3 .
T h is c o m m e n t is d e a lt w i t h in Q i a p t e r 3 .T h e t e n t a t iv e s to c k -
r e c r u itm e n t - r e la t io n b a s e d o n th e a v a i la b le d a ta in d ic a t e s th a t
a m u c h m o r e p r e c a u t io u s m a n a g e m e n t a p p r o a c h i s r e q u ir e d to
r e s to r e th e s t o c k , th a n w o u l d b e e x p e c t e d fo r a n o n -
d e p e n s a t o r y r e la t io n . T h e R e v ie w G r o u p a p p e a r s t o r e v e r s e
th e b u r d e n o f p r o o f .
174 Joint EIFAAC/ICES/CFCM WCEEL REPORT 2014
IX It c o u ld b e th a t th e l o w v a lu e s o f th e
g la s s e e l in d ic e s s in c e th e 1 9 9 0 s a r e th e
r e s u l t o f l e s s f a v o u r a b le s u r v iv a l
c o n d i t io n s o f t h e e a r ly l i f e s t a g e s
( p o s s ib l y d u e t o a r e g im e s h if t ) p e r h a p s
e x a c e r b a te d b y r e d u c e d s p a w n e r
q u a l i t y a s s o c ia t e d w i t h c o n t a m in a n t s o r
o t h e r fa c to r s in fr e s h w a te r . T h e r e m a y
b e s u b s e q u e n t c o m p e n s a t o r y r e s p o n s e s
in t h e s p a w n e r p r o d u c t io n in th e
c o n t in e n t a l p h a s e o f t h e l i f e c y c le th a t
r e s u l t s i n a s p a w n e r to s p a w n e r r a t io
w h i c h i s g r e a te r th a n o n e , b e fo r e
p o t e n t ia l s p a w n e r s a r e k i l l e d in
c o n t in e n t a l a r e a s . E v id e n c e i s p r o v id e d
in t h e r e p o r t o f s o m e o f th e s e , in c lu d in g
in c r e a s e d s i z e a n d p r o p o r t io n f e m a le s
a m o n g s i lv e r e e l s a s a b u n d a n c e h a s
d e c l in e d ( s e e S e c t io n s 9 .1 1 .1 a n d 9 .1 1 .2 ) .
I t i s n o t a b le th a t m a r in e m o r ta l i t y o f
A t la n t ic s a lm o n , w h i c h i s m o s t u n l ik e ly
to d e m o n s t r a t e d e p e n s a t i o n d u r in g th e
m a r in e p h a s e , a l s o s h o w s s ig n s o f
h a v in g b e e n a f f e c t e d b y a r e g im e s h i f t
a r o u n d 1 9 9 0 (IC E S 2 0 1 3 b )
1 2 T h e m a n a g e m e n t a d v ic e i s th e s a m e
r e g a r d le s s o f w h e t h e r th e S -R d y n a m ic
i s d u e t o n o n - s t a t io n a r i t y ( d e n s i t y
in d e p e n d e n t o r d e n s i t y d e p e n d e n t
p h e n o m e n o n a s s o c ia t e d w i t h r e d u c e d
r e s o u r c e s ) o r d e p e n s a t io n ; to m a in ta in
a n d in c r e a s e r e c r u it m e n t , t h e s p a w n e r
b io m a s s m u s t b e in c r e a s e d .
13 T h e c o m b in e d r e p o r t o f th e M a r c h a n d
S e p t e m b e r m e e t i n g s e x c lu d e s a n y
in f o r m a t io n o n t h e w o r k u n d e r t a k e n to
a d d r e s s T o R 'd ' t o 'g ' . T h e W K E P E M P
r e p o r t (IC E S 2 0 1 3 c ) c o n t a in s s o m e o f th e
in f o r m a t io n c o l la t e d d u r in g th e M a r c h
m e e t in g . T h e s u m m a r y ta b le s o f t h e k e y
s to c k ín d ic a t o r s b y E M U , r e fe r r e d to a s
th e 3 B s & E A -a p p r o a c h , w h i c h are
s u m m a r iz e d la te r in th e P A s u m m a r y
p lo t s o f s t a t u s b y E M U a n d c o u n t r y in
S e c t io n 6 .5 o f th is r e p o r t , a r e p r o v id e d
i n IC E S (2 0 1 3 c ) a n d a s im ila r ta b le
s h o u l d h a v e b e e n in c l u d e d in th is
r e p o r t , a s a r e s p o n s e to T o R 'e ' a n d 'f '.
G i v e n th a t t h e s e s t o c k in d ic a to r s a r e
p r o p o s e d a s k e y in d ic a t o r s o f s to c k
s t a t u s a n d p r o g r e s s b y s t a t e s in
a c h ie v in g s t o c k r e b u i ld in g o b je c t iv e s ,
r e a d e r s o f t h is r e p o r t w o u l d h a v e
b e n e f i t e d i f a s e c t io n d e s c r ib in g t h e s e
s t o c k in d ic a t o r s , th e ir o r ig in , a n d h o w
t h e y a r e u s e d t o a s s e s s s to c k s t a t u s h a d
b e e n p r o v id e d .
A s p o in t 10 .
A g r e e d , a n d fu r th e r d e a l t w i t h in C h a p te r 3 .
A g r e e d , b u t i t w a s d e s ig n e d th a t w a y a t th e t im e t o k e e p s o m e
r o le s e p a r a t io n b e t w e e n t h e t e c h n ic a l r e v i e w o f t h e E M P s
(W K E P E M P ) a n d th e w o r k o f th e W G . C o m m e n t n o t e d fo r
fu t u r e r e fe r e n c e .
Joint ElFAAC/iCES/CFCM WGEEL REPORT 2014 175
14 T h e W o r k in g G r o u p h a s a d i f f ic u l t ta s k
to p u l l t o g e t h e r d a ta f r o m a la r g e a n d
d iv e r s e g r o u p o f c o u n t r ie s a n d to
d e v e l o p u n i f i e d a s s e s s m e n t s o f th e e e l
s to c k . H o w e v e r , th e r e p o r t i s n o t c le a r ly
s t r u c tu r e d , a n d s e c t i o n s n e i t h e r f u l ly
a d d r e s s s p e c i f i c T o R ( e .g . T o R 'j' i s
a d d r e s s e d in S e c t io n s 4 , 5 , 6 , 9 , 1 0 a n d
1 1 ) n o r p r o v id e c o m p le t e a n s w e r s to
s p e c i f i c a d v is o r y q u e s t io n s
15 T h r o u g h o u t t h e r e p o r t , r e fe r e n c e p o in t s
a r e f r e q u e n t ly r e fe r r e d t o a s 'ta r g e ts '
w h e n t h e y a r e a c t u a l ly ' l im it s ' . T h is is
a n im p o r t a n t d is t in c t io n w h i c h h a s
s íg n i f ic a n t im p l i c a t io n s fo r
m a n a g e m e n t .
1 6 T h e r e a r e s e v e r a l s e c t io n s in w h ic h
f ig u r e n u m b e r s h a v e b e e n d u p l ic a t e d .
T h is i s d i f f i c u l t t o a v o id w h e n
c o m p i l in g a la r g e r e p o r t q u ic k ly , b u t it
c o u ld b e r e d u c e d b y e m p lo y i n g th e
n o r m a l IC E S c o n v e n t io n fo r n u m b e r in g
f ig u r e s a n d ta b le s
Sections 1 -3 , Opening, Agenda &
Introduction
1 7 T h e T o R w o u l d b e e a s ie r t o f in d i f t h e y
w e r e p la c e d in a s t a n d - a lo n e s e c t io n a t
th e s ta r t o f th e r e p o r t . It w o u l d a l s o b e
h e lp f u l t o in d ic a t e w h i c h m a n a g e m e n t
b o d y ( i e s ) a r e r e q u e s t in g th e a d v ic e (S e e
T e c h n ic a l R e v ie w 2 0 1 2 ) . It i s h e lp f u l th a t
s o m e s e c t io n s o f t h e r e p o r t a r e p r e fa c e d
b y th e T o R w h i c h t h e y a d d r e s s ; i t
w o u l d a l s o b e h e lp f u l i f t h e l i s t o f T o R
a t th e b e g in n in g o f t h e r e p o r t s h o w e d
th e s e c t i o n in w h i c h e a c h T o R is
c o n s id e r e d
1 8 A n n e x 3 a p p e a r s to in d ic a t e t h a t th e
T o R a r e p r o p o s e d b y t h e W o r k in g
G r o u p i t s e l f , b u t c la r if ic a t io n is r e q u ir e d
o n th e c u s t o m e r ( s ) fo r th e a d v ic e a n d
th e p r e c i s e m a n a g e m e n t n e e d s . I t m ig h t
b e h e lp f u l i f fu t u r e T o R r e f le c t th e
u l t im a t e a d v i s o r y n e e d (e .g . a n
a s s e s s m e n t o f th e s t a t u s o f th e e e l s to c k
a c r o s s i t s r a n g e ) r a th e r th a n th e p r o c e s s
f o r a c h ie v in g t h a t n e e d ( e .g . c o m p ila t io n
o f d a ta ) .
1 9 T h e R e v ie w G r o u p r e c o m m e n d s th a t in
f u t u r e th e W o r k in g G r o u p p r o v id e s a n
A n n e x l i s t i n g th e R e v ie w G r o u p 's
c o m m e n t s a n d e i t h e r p r o v id e s a
r e s p o n s e o r in d ic a t e s w h e r e in th e
r e p o r t th a t r e s p o n s e c a n b e fo u n d .
D o n e - th e r e p o r t s tr u c t u r e h a s b e e n r e d e s i g n e d t o la r g e ly
f o l l o w t h e r e c o m m e n d a t io n s o f th e R G E E L 2 0 1 3 , a n d c h a p t e r
t i t l e s a n d c o n t e n t la r g e ly o r g a n is e d t o a d d r e s s in d iv id u a l
T o R s .
It i s r e fe r r e d t o a s a 'ta r g e t ' in th e R e g u la t io n ; w i l l b e r e fe r r e d
t o a s a T im it ' in W G E E L .
A g r e e d .
D o n e - T h e T o R , t h e b o d i e s r e q u e s t in g th e A d v i c e , a n d d e t a i l
o f w h i c h r e p o r t c h a p te r a d d r e s s e s w h i c h T o R , a r e a ll p r o v id e d
in th e I n tr o d u c t io n to th e r e p o r t (C h a p te r 1 ). T h e c h a p t e r t i t le s
i n c l u d e t h e T o R to w h i c h t h e y a r e a d d r e s s e d .
D o n e - th e T o R fo r 2 0 1 4 w e r e d e s ig n e d t o r e f le c t th e a d v is o r y
n e e d .
D o n e
176 Joint ElFAAC/iCES/CFCM WCEEL REPORT 2014
20
21
22
2 3
In th e a b s e n c e o f a S to c k A n n e x a l l d a ta
a n d m e t h o d s u s e d s h o u ld (a s fa r a s
p r a c t ic a b le ) b e p r o v id e d in th e r e p o r t; it
i s n o t r e a s o n a b le to e x p e c t th e r e a d e r to
l o o k t h r o u g h m o r e th a n 1 5 E x p e r t
G r o u p r e p o r ts to f in d th e r e le v a n t
in f o r m a t io n . W h e r e t h e v o lu m e o f d a ta
is t o o g r e a t t o b e in c l u d e d in t h e r e p o r t ,
th e in f o r m a t io n s h o u l d b e s u m m a r iz e d
a n d s o u r c e s g iv e n .
p . i i i , S e c t io n B , C h a p te r 1 0 , l s t
p a r a . U n c le a r w h a t 'e x p o r t s ' m e a n s ; i s
i t e x p o r t s o u t o f th e E U , o r e x p o r t s o u t
o f th e f i s h in g c o u n tr y ?
p .2 0 : I m p le m e n t a t io n o f th e E M P s h a s
n o w in t r o d u c e d d is c o n t in u i t ie s in d a ta
t r e n d s ( e .g . f i s h e r i e s d e p e n d e n t
r e c r u itm e n t s e r ie s ) ; th e W o r k in g G r o u p
s h o u ld c o n s id e r th e im p l i c a t io n s a n d
r e v ie w th e n e e d t o s h i f t f r o m f is h e r ie s -
b a s e d to s c ie n t i f ic s u r v e y - b a s e d
a s s e s s m e n t s .
S to c k A n n e x p la n n e d in F u tu r e F o c u s .
S e e u n d e r r e s p o n s e to G e n e r ic T o R s A n n e x
Section 4, In troduction to stock
assessm ent, reference po in ts and
stock status
In S e c t io n 4 .2 , th e W o r k in g G r o u p
p r e s e n t s a n a r r o w v i e w o f w h a t a re
t e r m e d 's t a n d a r d s t o c k a s s e s s m e n t
t e c h n iq u e s ' a n d s u g g e s t s th a t , i f t h e s e
t e c h n iq u e s w e r e a p p l i e d to e e l , th e
a s s e s s m e n t w o u l d b e m e a n in g le s s .
H o w e v e r , t h e p r o b le m i s n o t w i t h e e l
b i o lo g y o r e c o lo g y , i t r e s id e s w i t h th e
la c k o f a d e q u a t e b a s ic s to c k a s s e s s m e n t
d a ta fo r E u r o p e a n e e l , i n c l u d in g c a tc h
d a ta , b io lo g ic a l d a ta in c l u d in g le n g t h
a n d w e i g h t a t a g e a n d s t a g e ( y e l lo w v s
s i lv e r e e l ) a n d e s t im a t e s o f e x p lo i t a t io n
r a te s a c r o s s th e s p e c ie s r a n g e . I f t h e s e
d a ta w e r e a v a ila b le , th e E u r o p e a n e e l
c o u ld v e r y w e l l l e n d i t s e l f to s ta n d a r d
a s s e s s m e n t a p p r o a c h e s , s u c h a s
s ta t is t ic a l c a t c h a t a g e o r c o h o r t
a n a ly s e s . I f s u c h in f o r m a t io n w a s
c o l la t e d a n d in t e g r a t e d o v e r a l l r e g io n s ,
t h is w o u l d c o n s t i t u t e a n in t e m a t io n a l
a s s e s s m e n t to w h i c h W G E E L a s p ir e s .
T h e r e fe r e n c e s to p r e v i o u s W G E E L
r e p o r ts , w h i c h a r e th e s o u r c e o f t h e t e x t
in th is s e c t io n , do not provide scientific
support for discounting standard
assessm ent procedures. I n th e
m e a n t im e , th e r e r e m a in s a n u r g e n t n e e d
t o in t r o d u c e fu r th e r q u a l i t y c o n tr o l in to
t h e s e p a r a t e r e g io n a l a s s e s s m e n t s
u n d e r ta k e n .
O u t o f th e f i s h in g c o u n tr y
T h e n e e d t o s h i f t to s c ie n t i f ic s e r ie s a n d t h e r is k o f l o s in g th e
f i s h e r y b a s e d s e r ie s h a s b e e n a d d r e s s e d b y t h e W G E E L b e fo r e
t h e im p le m e n t a t io n o f th e m a n a g e m e n t p la n . T h e W G E E L h a s
r e p e a t e d ly m a d e r e c o m m e n d a t io n s t o tr y to a d d r e s s th is
p r o b le m , S e e S G IP P E E '1 1 , W G E E L , '0 9 &: 1 0 & 11 & '1 2 , a n d
W K E S D C F
S e c t io n 4 .2 a c t u a l ly in d ic a t e d th a t a s t a n d a r d , c e n t r a l is e d , a g e -
b a s e d a p p r o a c h c o u ld i n d e e d b e f o l l o w e d ; w e d o n o t d is a g r e e
o n th a t .
T h e p o in t m a d e i n S e c t io n 4 .2 ( h ig h l ig h t e d b y a n e x a m p le o f
a g e 5 y e a r o ld e e l s , c o m b in in g r e c r u it in g y e l l o w e e l s f r o m
S c a n d in a v ia w i t h e s c a p in g s i lv e r e e l f r o m t h e M e d i t e r r a n e a n )
i s th a t th e r e s u lt s (e .g . m o r t a l i t y a t a g e 5 ) w o u l d b e d i f f i c u l t to
in t e r p r e t , a n d w o u l d h a r d ly r e la te t o a n y m a n a g e m e n t a c t io n .
T h e a s s e s s m e n t i s f e a s ib le , b u t w o u l d h a v e s e v e r e ly r e s tr ic te d
a p p l ic a t io n .
Joint EIFAAC/ICES/GFCM WGEEL REPORT 2014 I 177
2 4 p .2 3 , S e c 4 .3 : I t w o u l d b e h e lp f u l to
c le a r ly p r e s e n t th e m a n a g e m e n t
o b j e c t iv e s (e .g . th e E U R e g u la t io n )
a g a in s t w h i c h th e th r e e a s s e s s m e n t
m e t h o d s d e s c r ib e d in S e c t io n 4 .3 a re
c o n d u c t e d
2 5 p .2 3 , S e c 4 .3 , p a r a 2: th e r e fe r e n c e s to
D L S G u id a n c e a r e u n c le a r ; th e n a m e
s h o u l d b e s p e l t o u t ín fu l l t h e f ir s t t im e
i t i s m e n t io n e d a n d t h e c o r r e c t r e fe r e n c e
s h o u l d b e in c lu d e d . F u r th e r m o r e th e
r e fe r e n c e s t o M e t h o d s 1 .1 .2 ( I fe s t im a te d
s to c k b io m a ss in th e in te r m e d ia te y e a r ís less
th a n M S Y Btr,sgrr) a n d 5 .3 ( l f c a tc h e s h a ve
d e c lin e d s ig n i f ic a n t ly o v e r a p e r io d o f t i m e
a n d th is is co n s id e re d to be r e p r e s e n ta t iv e o f
a s u b s ta n tia l r e d u c t io n in b io m a ss , a
r e c o v e ry p la n a n d p o s s ib ly z e r o ca tch is
a d v ise d ) d o n o t a p p e a r t o m a t c h th e te x t .
2 6 p .2 4 , p a r a 1 , l i n e 3: th e r e p o r t r e fe r s to 'a
d is c u s s io n o n h o w to d ea l w i th a (rea l o r
p e r c e iv e d ) b rea k in a h i th e r to c o n s is te n t,
m u ltid e c a d a l d e c lin e ( fo r w h ic h D L S
C u id a n c e d o es n o t p r o v id e a m e th o d ) '; th is
s t a t e m e n t i s u n c le a r ; th e r e i s n o t a
b r e a k , i t i s a n u p t u m .
2 7 p .2 4 , p a r a 1, l in e 5 -6 : t h e r e p o r t s ta te s ,
'F in a lly , th e a va ila b le d a ta in d ic a te th a t
r e c r u i tm e n t h a s d e c lin e d m o re r a p id ly th a n
th e ( r e c o n s tr u c te d ) s p a w n e r e sc a p e m e n t,
w h ic h m a y in d ic a te a. a n in a p p r o p r ia te
r e c o n s tr u c t io n o f t h e t r e n d in s p a w n e r
e s c a p e m e n t , o r b. a n o n -s ta b le s to c k - r e c r u i t
r e la t io n s h ip (e .g . c h a n g e in ocean
c o n d i t io n s ) , o r c. a d e p e n s a to n / s to c k -
r e c r u i tm e n t r e la t io n s h ip .'. H o w e v e r th is
i s t o b e e x p e c te d ; in a c o m p e n s a t o r y S -R
r e la t io n s h ip s , r e c r u itm e n t (R ) w i l l
d e c l in e fa s te r th a n s p a w n e r e s c a p e m e n t
(S ) w h e n S i s l e s s th a n t h e s p a w n e r s
r e q u ir e d to a c h ie v e M S Y (Smsy). (R w i l l
d e c l in e l e s s r a p id ly th a n S w h e n S >
S msy)
2 8 p .2 4 , S e c 4 .4 , p a r a 2: I t i s s u g g e s t e d , ' th e
n e t e f fe c t o f t h e a c t io n s ta k e n in 2 0 0 9 o n th e
to ta l 2 0 0 9 s i lv e r ee l e s c a p e m e n t is p ro b a b ly
s m a l l , f a r b e lo w th e ta r g e ts o f t h e E M P s
a n d /o r th e u l t im a te l y s u s ta in a b le le v e l. '
T h e s e c o n c l u s io n s a r e n o t j u s t i f ie d
w it h o u t a l i s t o f t h e a c t io n s ta k e n a n d
th e l i f e s t a g e s l ik e ly a f f e c t e d
T h is c o m m e n t i s d e a l t w i t h in C h a p te r 3 . D o n e .
T h is c o m m e n t i s d e a lt w i t h in C h a p te r 3 .
T h is c o m m e n t ís d e a l t w i t h in C h a p t e r s 2 a n d 3 .
T h is c o m m e n t is d e a lt w i t h in C h a p t e r 3 .
B o th a B e v e r to n & H o l t - t y p e a n d R ic k e r - t y p e r e la t io n a re
c o n c a v e b e t w e e n M S Y a n d t h e o r ig in , t h a t is : s p a w n in g s to c k
d e c r e a s e s fa s t e r t h a n th e r e s u lt in g r e c m it m e n t . T h e e e l d a ta
a p p e a r to in d ic a t e th e o p p o s i t e .
IC E S -W K E P E M P 2 0 1 3 p r o v id e d th a t l i s t . C h a p t e r 4 i s in t e n d e d
to s k e tc h th e f r a m e w o r k fo r s to c k a s s e s s m e n t a n d r e fe r e n c e
p o in t s , w h i l e d e d ic a t e d c h a p t e r s p r o v id e f u l l d e t a i l . D O N E
Section 5, Trend based assessm ent
and reference po in ts
178 | Joint ElFAAC/ICES/GFCM WGEEL REPORT 2014
2 9 L it t le in f o r m a t io n is p r o v id e d o n th e
d e r iv a t io n o f t h e r e c r u itm e n t in d ic e s
u s e d in t h i s a s s e s s m e n t ; T a b le 5 -1 r e fe r s
to ' th e tw o r e c r u i tm e n t se r ie s p r e s e n te d in
C h a p te r 9 ', b u t th a t s e c t io n d e a ls w i t h
th r e e l i f e s t a g e s ( g la s s , y e l l o w a n d
g la s s + y e l lo w ) a n d t w o a r e a s ( N o r th S e a
a n d E ls e w h e r e ) . (N B C o m m e n t s o n th e
t im e s e r ie s a n a ly s i s a r e p r e s e n t e d fo r
S e c t io n 9 b e lo w .)
3 0 C h o ic e o f t h e b a s e l in e p e r io d i s a k e y
e l e m e n t o f t h e s e a n a ly s e s , a n d th is i s
n o t e x p la in e d e i t h e r h e r e o r in th e
g e n e r a l d i s c u s s i o n o f d a ta c o m p ila t io n
(C h a p te r 9 ) . T h e p e r io d 1 9 6 0 -1 9 7 9 is
c h o s e n a s a b a s e l in e b e c a u s e 'th e s to c k
w a s co n s id e re d to be 'h e a l th y ' d u r in g th is
p e r io d ', b u t e l s e w h e r e th e r e p o r t s a y s
th a t y e l l o w e e l r e c r u it s h a v e b e e n
d e c l in in g s in c e th e 1 9 6 0 s (p . i)
A g r e e d , th e t a b le s 4 .3 4 .4 a n d 4 .5 d e s c r ib e t h e c u r r e n t s ta t e o f
s e r i e s u s e d ( w h ic h a r e u p d a t e d , w h i c h a r e n o t ) . W e n o w
e x p la in th a t th e g la s s e e l t r e n d i s b a s e d o n b o t h g la s s e e l a n d
g la s s e e l + y e l lo w e e l (C h a p te r 2 ). T h e f u l l d e s c r ip t io n o f th e
s e r i e s a v a ila b le a n d th e ir p o s s ib l e w e a k n e s s e s i s d e s c r ib e d in
a n E -ta b le a c c o m p a n y in g th a t c h a p t e r . T h is d e s c r ip t io n
c o m p r i s e s th e f ir s t y e a r , la s t y e a r , d u r a t io n , m is s in g y e a r s , a n d
th e e x p e r t i s e o f a p o s s ib l e c h a n g e in t h e tr e n d o v e r th e y e a r s .
N o s e le c t io n w a s d o n e th is y e a r o n th e s e r ie s , b u t t h e w g e e l
a c k n o w le d g e s th e n e e d t o w o r k o n t h e w e ig h in g o f t h o s e
s e r ie s . T h e r e m ig h t b e u p to 3 s e r i e s in t h e s a m e p la c e , a n d
g e o g r a p h ic a l , w i t h r e s p e c t to a b s o l u t e r e c r u itm e n t , s o m e s e r ie s
w i l l h a v e m u c h m o r e w e ig h t t h a n o th e r s .
T h is i s n o w a n s w e r e d i n C h a p te r 2 . T h e W G E E L a c k n o w le d g e s
th a t th e p e r io d o f r e fe r e n c e le a d s t o a d i f f i c u l t y in th e
in t e r p r e t a t io n , b u t c h o o s in g a d i f f e r e n t p e r io d m ig h t le a d far
f e w e r s e r ie s a v a ila b le . F ig u r e 4 .2 a n d 4 .3 p r e s e n t s th e r a w d a ta
in a w a y th a t i s c o n s i s t e n t w i t h p r e v i o u s r e p o r ts f r o m 2 0 0 2 .
A I s o
3 1
32
p .2 6 , T a b le 5 -1 : th e c a p t io n r e fe r s t o a
r e fe r e n c e p e r io d o f 1 9 6 0 -8 0 ; s h o u ld th is
b e 1 9 6 0 -7 9 (o r i t i s in c o n s i s t e n t w i t h th e
r e fe r e n c e p e r io d u s e d e l s e w h e r e ) ?
T h e r e p o r t d r a w s a f ir m c o n c lu s ío n
f r o m th e tr e n d a n a ly s i s th a t ' th e s to c k
r e m a in s in th e c r it ic a i z o n e . ' T h is i s b a s e d
o n th e c h o s e n b a s e l in e , a n d a d d i t io n a l
a n a ly s e s s h o u l d b e p r e s e n t e d t o c o n f ir m
w h e t h e r th e r e p o r t 's c o n d u s i o n o n
t r e n d s i s u p h e l d u s i n g a lte r n a te
b a s e l in e s . T h e e x t e n t t o w h i c h th e
r e c r u it m e n t in d e x v a r ie s w i t h b a s e l in e
c h o ic e w o u l d a l s o h e lp in t h e e v a lu a t io n
o f th e r o b u s t n e s s o f th is m e t h o d .
T h e c o n c e p t o f a 'b a s e l i n e / a p e r io d
w h e n th e p o p u l a t io n w a s 'h e a l th y ' , h a s
a r e le v a n c e th a t g o e s b e y o n d C h a p te r
5 . T h e a n a ly t ic a l a p p r o a c h o f C h a p te r 6
i s b a s e d o n a h y p o t h e t i c a l p o p u l a t io n
th a t i s u n a f f e c t e d b y a n t h r o p o g e n ic
a c t iv i t ie s , w h i c h i s a n o t h e r w a y o f
s a y in g a b a s e l in e p o p u la t io n . T h e s e
b a s e l in e s s h o u l d b e c o n s is t e n t .
T h e W G E E L h a s c o n s id e r e d i n c l u d in g d a ta b e fo r e 1 9 6 0 . T h e
u n b i a s e d d a ta b e f o r e 1 9 6 0 a r e n o t n u m e r o u s e n o u g h to
p r o v id e a tr e n d th a t w e c o u ld b e c o n f id e n t in . A s a r e s u lt , th e
g r a p h s w e r e a d a p t e d w i t h s h a d i n g fo r d a ta b e f o r e 1 9 5 0 a n d
o n ly th e v a lu e s a f te r 1 9 6 0 a r e p r e s e n t e d in th e W G E E L
r e c r u it m e n t in d e x .
T h e y e l lo w e e l s e r i e s i s b a s e d o n fo u r u n b ia s e d s e r i e s a f te r
1 9 4 6 , a n d t h e r e fe r e n c e p e r io d fo r t h o s e s e r ie s h a s n o t b e e n
c h a n g e d .
T h e b a s e l in e i s c h o s e n a s f o l l o w i n g :
1 980 : b r e a k p o in t in r e c r u itm e n t
1 960 : b e fo r e w e d o n ' t h a v e e n o u g h d a ta .
Joint EiFAAC/ICES/GFCM WGEEL REPORT 2014 179
3 4
35
3 3 It i s n o t c le a r th a t th e p r e s e n t a t io n o f th e
r e c r u itm e n t t r e n d s in F ig u r e 5 -3 a d d s
s ig n i f íc a n t ly t o F ig u r e s 5 -1 a n d 5 -2 ,
p a r t ic u la r ly g i v e n th a t th e 5 -y e a r
e x p o n e n t ia l tr e n d a p p e a r s to b e q u it e
s e n s i t i v e t o r e la t iv e ly s m a l l a n n u a l
f lu c t u a t io n s in R a n d m a n y o f th e d a ta
p o in t s a r e s u p e r im p o s e d .
T h e r e fe r e n c e p o in t s u s e d in t h e s e
a n a ly s e s a r e n o t r e fe r e n c e p o in t s fo r
m a n a g e m e n t , a n d m a n a g e r s m a y b e
c o n f u s e d b y th e in t r o d u c t io n o f t h e n e w
s t a t u s t e r m in o lo g y ; th e u s e o f a 'h ig h
c a u t io u s ' z o n e i s c o n f u s in g , a n d th e
d is t in c t io n w i t h t h e 'c a u t io u s ' z o n e s
m a y a l s o b e m is l e a d i n g ( fo r e x a m p le , a
s t r o n g ly d e c r e a s in g tr e n d w h e n R/Rtarga
i s m a r g in a l ly g r e a te r th a n 1 .0 ( c a u t io u s
z o n e ) w o u l d a p p e a r t o p o s e m u c h
g r e a te r r is k to t h e s t o c k th a n a s t r o n g ly
p o s i t iv e t r e n d w i t h R / R t a r Sc t m a r g in a l ly
l e s s t h a n 1 .0 ( h ig h c a u t io u s z o n e ) ) .
F o r a p a n m ic t ic s p e c ie s , a d e c l in e in
r e c r u itm e n t to n o r t h e m a r e a s b u t n o t in
s o u t h e m a r e a s i s n o t c o n s i s t e n t w i t h
d e p e n s a t io n .
O v e r a l l , t h e tr e n d a n a ly s e s c o n f ir m th e
c o n t in u in g s e v e r e ly d e p le t e d s t a t e o f th e
r e c r u it m e n t , a n d th is i s c le a r ly
d e s c r ib e d . A n u m b e r o f c o m m e n t s a r e
m a d e a b o u t t h e r e c e n t u p t u m in th e
r e c m it m e n t in d ic e s , a n d t h is r a is e s th e
i s s u e o f d e t e r m in in g w h e n t h e s e
c h a n g e s s h o u l d b e c o n s id e r e d
s ig n if ic a n t .
3 6 T h e W o r k in g G r o u p m ig h t c o n s id e r
w h e t h e r e x a m in a t io n o f p r e v i o u s y e a r -
t o - y e a r v a r ia t io n in t h e in d ic e s (e .g .
a n n u a l c h a n g e s , s e q u e n c e s o f
in c r e a s e /d e c r e a s e s , e tc ) c o u ld b e u s e d to
e v a lu a t e th e s ig n if ic a n c e o f r e c e n t
c h a n g e s . A s in d ic a t e d , i t w o u l d b e
d e s ir a b le to b e a b le t o p r e s e n t s im ila r
t r e n d s in y e l l o w a n d /o r s i lv e r
a b u n d a n c e , e v e n i f t h e s e t r e n d s m a y
r e f le c t lo c a l d i f f e r e n c e s in p o p u la t io n
d y n a m i c s a n d a n t h r o p o g e n ic im p a c t s .
3 7 p . 2 6 , S e c 5 .2 : Rdown i s b a s e d o n th e 5%
q u a n t i le o f r e c r u itm e n t . S in c e th e r e a r e
2 0 y e a r s b e t w e e n 1 9 6 0 a n d 1 9 7 9 , it
a p p e a r s th a t R d ow n s h o u l d b e th e
r e c m it m e n t d u r in g th e p o o r e s t
r e c r u itm e n t y e a r b e t w e e n 1 9 6 0 a n d
1 9 7 9 . I f th is i s c o r r e c t , i t s h o u l d b e
s t a t e d in t h e te x t .
A g r e e d . A d d r e s s e d in C h a p te r 3 .
W e n o w k e e p o n ly th e F ig u r e 5 .3 . A s s a id in th e r e p o r t ,
d if f e r e n t p e r io d to c a lc u la t e th e tr e n d h a v e s b e e n t e s t e d a n d 5
y e a r s s e e m s to th e b e s t c o m p r o m is e . T h e f ig u r e s h a s b e e n
e n la r g e d
T h e E U h a s a g r e e d o n a b io m a s s l im i t r e fe r e n c e p o in t , b u t h a s
n o t a d o p t e d a n y m o r t a l i t y r e fe r e n c e p o in t . IC E S a d v ic e s o far
h a s e s s e n t ia l ly b e e n b a s e d o n t h e tr e n d in r e c m it m e n t o n ly .
T h a t is: m a n a g e m e n t a n d a d v ic e a d d r e s s d i f f e r e n t d im e n s io n s .
T h e r e fe r e n c e p o in t s d i s c u s s e d in t h i s s e c t io n c a n b e a p p l ie d
fo r m a n a g e m e n t , a s e x e m p l i f ie d b y th e ir a p p l ic a t io n b y D F O
in C a n a d a . In o r d e r to h e lp t o a l i g n IC E S a d v ic e w i t h E U
p o l ic ie s o n e e l , C h a p te r 3 d i s c u s s e s t h e th r e e d if f e r e n t
a s s e s s m e n t a p p r o a c h e s . E la b o r a t io n o f th e t r e n d - b a s e d
a s s e s s m e n t a n d d e r iv a t io n o f c o r r e s p o n d in g r e fe r e n c e p o in t s is
o n e o p t io n ; a d v i s in g E U o n b io m a s s a n d m o r t a l i t y r e fe r e n c e
p o in t s a n o th e r .
T h e d e c l in e h a p p e n s e v e r y w h e r e . W e n o t e th a t i t m ig h t n o t b e
c o n s is t e n t w i t h o t h e r h y p o t h e s e s e i th e r .
T h is i s n o w a d d r e s s e d in C h a p te r 2 .
T h is is d o n e fo r r e c r u itm e n t . N o a n a ly s i s w a s d o n e t h is y e a r o n
th e y e l l o w a n d s i lv e r e e l t r e n d s , a s i t i s f e l t th a t t h o s e m ig h t
o n ly r e f le c t lo c a l c h a n g e .
F ig u r e s 5 .1 a n d 5 .2 c a n c e l le d in th is y e a h s r e p o r t
180 | Joint EIFAAC/ICES/CFCM WGEEL REPORT 2014
3 8 p .2 6 , l i n e 5: th e r e fe r e n c e t o u s i n g tr e n d
a n a ly s i s in th e d e v e l o p m e n t o f th e P A
b y F is h e r ie s a n d O c e a n s , C a n a d a is
u n c le a r .
3 9 p . 2 9 , F ig u r e 5 -3 : T h e y - a x is s h o u ld
in d ic a t e t h a t R / R i a r g « i s e x p r e s s e d a s a %.
T h e r e a s o n fo r u s i n g a f iv e y e a r
e x p o n e n t ia l c h a n g e fo r th e x - a x is s h o u ld
b e e x p la i n e d in th e te x t .
Section 6, Quantitative assessm ent
app ly ing generic reference points
4 0 S e c t io n 6 .2 p r o v id e s a n im p o r ta n t
d e s c r ip t io n o f th e m a n a g e m e n t
o b j e c t iv e s a n d s h o u l d b e t h e b a s i s fo r
th e m a n a g e m e n t a d v ic e . H o w e v e r , th e
E U 's r e fe r e n c e p o in t o f 40 % o f p r is t in e
b io m a s s i s r e fe r r e d to a s a 'ta r g e t ' ( l in e s
3 a n d 9 ) b u t a l s o a s a t r ig g e r p o in t ( l in e
9 ) a n d a s a ' l im it ' r e fe r e n c e p o in t ( l in e
15); í t i s im p o r t a n t t o b e c le a r w h e t h e r
t h is i s a t a r g e t o r a l im it .
4 1 S e c t io n 6 .3 r e fe r s t o ' s t o c k in d ic a to r s
3 B s & E A ' b u t i t i s n o t im m e d i a t e ly c le a r
w h i c h b io m a s s r e fe r e n c e p o in t s a re
b e i n g r e fe r r e d to ( th e g lo s s a r y d e f in e s
s e v e n b io m a s s r e fe r e n c e p o in t s ) .
4 2 It w o u l d b e h e lp f u l t o p r o v id e a
d e f in i t i o n o f t h e r e le v a n t in d ic a t o r s (Bo,
Bmrrait Bbest a n d E A ? ) in a t e x t t a b le a n d
r e la t e t h e s e t o t h e IC E S r e fe r e n c e p o in t s
(e .g . BMSY-tTÍgger).
T h e r e fe r e n c e i s s u p p l i e d a f e w i i n e s f u r th e r d o w n th e p a g e , in
t h e s e c t io n th a t e la b o r a t e s o n th is .
F ig u r e c o r r e c te d .
A c k n o w le d g e d ; c o r r e c t e d in t h i s y e a r 's r e p o r t.
C o r r e c t .
It a p p e a r s th a t v a lu e s a r e n o t p r o v id e d D o n e - th e m is s in g v a lu e s fo r t h e s e s t o c k in d ic a t o r s fo r E U
fo r a l l E M U s a n d th e r e a s o n fo r th is c o u n t r ie s h a v e b e e n h ig h l ig h t e d a g a in in C h a p te r 4 . S o lu t io n s
n e e d s t o b e d i s c u s s e d a n d s o lu t io n s f i l l t h e s e g a p s h a v e b e e n c o n s id e r e d t h r o u g h C h a p t e r s 4 a n d
e x p lo r e d . [N B : H o w e v e r , in r e la t io n to 7-
th is a n d f o l l o w i n g c o m m e n t s o n S e c t io n
6 , s e e t h e ' O v e r v i e w - G e n e r a l
c o m m e n t s ' r e g a r d in g t h e P r e c a u t io n a r y
D ia g r a m .]
Joint EIFAAC/ICES/GFCM WCEEL REPORT 2014 I 181
4 3
4 4
4 5
4 6
47
T h e a s s e s s m e n t r e s u lt s p r e s e n t e d
a p p e a r to h a v e b e e n ta k e n d ir e c t ly fr o m
M e m b e r S ta te s ' 2 0 1 2 p r o g r e s s r e p o r ts
o n t h e ir E M P s, a n d n o n e w a n a ly s is
s e e m s to h a v e b e e n u n d e r t a k e n b y th e
W o r k in g G r o u p . T h e r e i s c le a r ly a n e e d
f o r s o m e d e g r e e o f q u a l i t y /c o n s i s t e n c y
r e v ie w . I t i s n o t p o s s ib l e to p r o v id e fu l l
d e t a i l s o f t h e s e a s s e s s m e n t s w i t h in
r e a s o n a b le l im i t s o f s p a c e , b u t s o m e k e y
p o in t s n e e d t o b e e x p la i n e d to a l l o w
r e a d e r s t o j u d g e th e s t r e n g t h o f th e
a p p r o a c h a n d t h e l im it s to i t s
in t e r p r e ta t io n . P lu s b u l le t p o in t s ................
T h e im p a c t o f t h e s e g a p s o n th e o v e r a ll
a s s e s s m e n t m a y v a r y w i t h th e t y p e o f
g a p . D a t a f r o m P o r t u g a l a r e m is s in g ,
b u t d a ta f r o m a d j o in in g E M U s o n th e
I b e r ia n P e n in s u la m a y p r o v id e a v a lid
p r o x y . G a p s in b r o a d r e g io n s a r e m o r e
p r o b le m a t ic . T h e M e d i t e r r a n e a n b a s in
m a y b e a s im p o r t a n t a s th e A t la n t ic fo r
E u r o p e a n e e l p r o d u c t io n , b u t th e r e a re
n o d a t a f o r a b o u t 3 /4 o f th e
M e d it e r r a n e a n c o a s t l in e . I f w e c a r m o t
a s s e s s e e l s t a t u s th e r e , i t l e a v e s a la r g e
g a p in th e p ic t u r e fo r t h e s p e c ie s a s a
w h o l e . C a n t e n t a t iv e o r p r e l im in a r y
c o n c l u s io n s b e d r a w n o n th e b a s i s o f
r e p o r te d la n d in g s fo r th is
r e g io n ? R e p o r t e d e e l la n d in g s in n o n -
E U M e d i t e r r a n e a n c o u n t r ie s
(p a r t ic u la r ly E g y p t ) a r e v e r y la r g e ,
p e a k in g a t > 4 0 0 0 1 in 2 0 0 6 (F ig u r e 9 - 1 0 ) ,
w h i c h e x c e e d e d to ta l r e p o r te d
E u r o p e a n la n d in g s a t th a t t im e .
D o m a n y o r m o s t E M U s h a v e
s u b s t a n t ia l e e l p r o d u c t io n a r e a s in
s a l in e w a t e r s th a t a r e n o t f i s h e d a n d
la c k b io lo g i c a l d a ta ? If s a l in e a r e a s a re
p o o r ly c o v e r e d o r n o t c o v e r e d in
m o d e i s , w h a t i s t h e e f f e c t o n th e
a s s e s s m e n t s ? W o u ld in c l u s io n o f
u n f i s h e d s a l in e w a t e r s in m o d e l s b o o s t
s i lv e r e e l p r o d u c t io n a n d r a is e th e
m o d e l l e d Boim.-nt f o r th a t E M U ?
E e l g r o w t h i s m o r e r a p id ín s a l in e th a n
f r e s h w a t e r (IC E S 2 0 0 9 ); d o m o d e ls ta k e
th is in t o a c c o u n t?
T h e W G E E L a r e w e l l a w a r e o f t h is p r o b le m a n d th e i s s u e h a s
b e e n r a is e d w i t h A C O M a n d t h e E U . D i s c u s s e d in M a r c h 2 0 1 3
a n d i n W K E P E M P . B e in g p a r t ly a d d r e s s e d i n th e 2 0 1 4 W G E E L
T o R s , b u t p e e r - r e v ie w o f th e E M P a s s e s s m e n t s r e m a in s a
t e c h n ic a l a n d r e s o u r c e s i s s u e b e y o n d th e t im e r e s o u r c e
a v a ila b le w i t h in t h e W G E E L .
I n c o m p le t e r e p o r t in g b y E IF A A C /IC E S
m e m b e r s i s c le a r ly a n o n g o in g p r o b le m ,
a n d th e W o r k in g G r o u p s h o u l d c le a r ly
s p e l l o u t in T a b le s th e d a ta / in d ic a to r s
th a t h a v e b e e n p r o v id e d b y E M U o r
c o u n t r y ( d i s t in g u i s h i n g E U -M S s) .
L a c k o f d a ta f r o m la r g e a r e a s i s a h u g e p r o b le m in e e l
a s s e s s m e n t . H o w e v e r , th e s e v e r i t y o f t h e p r o b le m d if fe r s ,
d e p e n d i n g o n th e f o c u s . F o r e v a lu a t in g
l o c a l /n a t io n a l / r e g io n a l /E U - w id e m a n a g e m e n t , b io m a s s a n d
m o r ta l i t y in d ic e s a n d th e ir p o s i t i o n r e la t iv e t o c o r r e s p o n d in g
r e fe r e n c e p o in t s p r o v id e s m e a n in g f u l a n d r e l ia b le in f o r m a t io n
fo r th e a r e a s th a t d o p r o v id e d a ta . F o r a n a ly s in g s t o c k - w id e
r e la t io n s , s u c h a s th e s to c k - r e c r u i t - r e la t io n , la c k o f d a ta fr o m
m a n y a r e a s i s a s e r io u s p r o b le m . N o t e , h o w e v e r , th a t t r e n d s in
r e c r u itm e n t a n d t r e n d s in la n d in g s h a v e s h o w n o n ly l i t t le
d if f e r e n t ia t io n b e t w e e n a r e a s in t h e p a s t (D e k k e r 2 0 0 4 ) - th e
l a n d in g s - b a s e d a n a ly s i s o f t h e s t o c k -r e c r u i t - r e la t io n w o u l d b e
v a l id , e v e n o n a s u b s e t o f th e d a ta .
G iv e n th e e x t r e m e v a r ia t io n b e t w e e n n e a r b y h a b ita t s (e .g .
r iv e r s v e r s u s la g o o n s ) , b u t a l s o b e t w e e n l i k e w i s e h a b ita t s in
n e a r b y c o u n tr ie s , w e s e e l i t t le p o in t in t e n t a t iv e f i l l in g in .
D u p l i c a t in g in f o r m a t io n f r o m s o m e a r e a s t o f i l l th e g a p fo r
n e a r b y a r e a s w o u l d b o i l d o w n to r a i s in g t h e s t a t is t ic a l
w e ig h in g fa c to r fo r th e k n o w n a r e a s , w h i l e th e q u a l i t y o f t h o s e
d a t a is o f t e n n o t b e y o n d d o u b t .
E e ls d o o c c u r ín m a n y s a l in e w a te r s , a n d s e v e r a l c o u n t r ie s
h a v e in c l u d e d t h e ir s a l in e / c o a s t a l a r e a s in th e ir m a n a g e m e n t
p la n s a n d a s s e s s m e n t s . O t h e r a r e a s a r e u n c o v e r e d , b u t t h e s e
h a v e m a in ly b e e n id e n t i f i e d in o u r r e s u l t s (e .g . w e e p i n g f a c e s
in F ig 6 -2 ) . T h e c o n tr a s t s ín l i f e h i s t o r y c h a r a c te r is t ic s b e t w e e n
f r e s h a n d s a l in e w a t e r s i s n o t f u n d a m e n t a l ly d i f f e r e n t f r o m th e
c o n tr a s t s b e t w e e n o th e r a r e a s .
A s in d ic a t e d in th e r e p o r t , t h e in t e m a t i o n a l a s s e s s m e n t t a k e s
a s i t s p r im e in p u t s t h e 3 B & E A in d ic e s f r o m E e l M a n a g e m e n t
U n it s , a n d th e a s s e s s m e n t s fo r e a c h o f t h o s e u n i t s is
c o n s id e r e d t o h a v e u s e d th e a p p r o p r ia t e p a r a m e te r s .
T h is w a s ta b u la t e d in th e M a r c h m e e t i n g a n d r e p o r t in th e
W K E P E M P 2 0 1 3 . I t i s a l s o t a b u la t e d in C h a p t e r 4 , o f t h is r e p o r t
in c l u d in g t h e c o u n t r ie s o u t s i d e o f t h e E U .
182 Joint EIFAAC/ICES/CFCM WCEEL REPORT 2014
4 8 p. 3 2 , S e c 6 .5 , l i n e 1 & F ig u r e 6 -1 s ta t e s
th a t t h e P r e c a u t io n a r y D ia g r a m s p lo t
th e 3 B s & £ A . In fa c t t h e y a p p e a r to
p lo t B c u r r e n t / B o ( % ) a g a in s t £ A . T h e
b o u n d a r i e s b e t w e e n th e c o lo u r e d z o n e s
in F ig u r e 6 -1 s h o u l d b e d e f in e d in th e
t e x t a n d /o r t h e f ig u r e c a p t io n .
4 9 p .3 5 - 3 6 , F ig u r e s 6 .1 a n d 6-2 : i t i s n o t
c le a r h o w t h e o v e r a l l s u m f o r £ A ( fr o m
th e E M U o r c o u n t r y d a ta ) i s d e r iv e d .
T h e o v e r a l l r a t io fo r t h e b io m a s s
in d ic a t o r c o u ld b e e s t im a t e d a s EBeumnt /
£Bo f o r r e p o r t in g ju r is d ic t io n s . F o r Z A ,
d o e s th e r e p o r t c a lc u la t e th e o v e r a ll
V a l u e a S : ( C B b e s t — £ B c u r r e n t ) / £ B b e s t ?
5 0 p .3 5 : In F ig u r e 6 -1 , s c a l in g th e b u b b le s
b y Bbest c o n f u s e s t h e p r o d u c t iv e c a p a c i t y
( I a r g e a r e a s c a n p r o d u c e lo t s o f e e ls )
w it h th e r e a l iz e d p r o d u c t io n .
5 1 F o r c o m m u n ic a t i o n t o m a n a g e r s , it
m ig h t b e b e t t e r to n o t u s e Bbest t o s c a le
th e b u b b le s b u t r a th e r u s e s im ila r s iz e d
s y m b o l s fo r a ll E M U s o r c o u n t r ie s b u t
w it h t w o c o lo u r s r e p r e s e n t in g th e
f o l l o w i n g c o n d it io n s : a w h i t e s y m b o l to
in d ic a t e Bbest/Bo < 40%Bo ( i .e . fa i lu r e to
m e e t t h e ta r g e t e v e n in th e a b s e n c e o f a ll
a n t h r o p o g e n ic m o r ta l it y ) a n d a s o l id
s y m b o i to in d ic a t e Bbcst/Bo > = 40%Bo
( p o t e n t ia l to a t t a in t h e t a r g e t in th e
a b s e n c e o f m o r ta l i t y ) . T h is w o u l d s h o w
w h e t h e r th e fa i lu r e o f a n E M U o r
c o u n t r y t o a c h ie v e i t s o b j e c t iv e (Bcurrent/Bo
< 40%Bo) i s d u e to in s u f f i c ie n t
m a n a g e m e n t in t e r v e n t io n in th e g iv e n
y e a r v e r s u s fa i lu r e to m e e t th e ta r g e t
d u e to l o w p o t e n t ia l p r o d u c t io n in th a t
y e a r .
5 2 T h e in f o r m a t io n th a t n e e d s t o b e
c o m m u n ic a t e d to m a n a g e r s i s w h e r e
Bcurrcnt i s r e la t iv e t o 40%Bo a n d £ A ( th e
th r e e c o lo u r s ) a n d w h e r e Bbcsi w o u l d b e
r e la t iv e to Bo. In th is c a s e , u s i n g t h e s a d
o r h a p p y fa c e s y m b o l s c o u ld b e u s e d to
c o m m u n ic a t e th is in f o r m a t io n ( s a d fa c e
m e a n s Bbest w a s b e l o w 40%Bo, h a p p y
f a c e m e a n s Bbest > = 40%Bo) w i t h th e s a m e
c o io u r s c h e m e o f r e d , y e l lo w , a n d g r e e n
t o d e s c r ib e th e c u r r e n t s ta t e o f th e s to c k ,
a n d th e w h i t e s y m b o l s t o in d ic a t e n o
in f o r m a t io n . T h is s c h e m e w o u l d a v o id
p la c i n g t h e la r g e r e d s y m b o l fo r F r a n c e
a s i t c u r r e n t ly a p p e a r s in F ig u r e 6 .2 .
In fa c t , l in e s 3 -6 o f th a t p a r a g r a p h d id th a t .
T h e f u n c t io n a l r e la t io n b e t w e e n £ A a n d % S P R w a s d i s c u s s e d
in IC E S -S G IP E E (2 0 1 0 ) , in th e w id e r s e t t in g o f d e v e l o p i n g th e
r e q u ir e d m e t h o d o lo g y . T h e 2 0 1 3 r e p o r t e x p la i n e d
m e t h o d o lo g y in c o m m o n w o r d s , a n d r e fe r r e d b a c k to th e
s o u r c e s , in o r d e r to p u t p r im e f o c u s o n th e r e s u lt s .
B b e s t n o t n e c e s s a r i ly r e la t e s to p r o d u c t io n a re a ; t h e m a jo r p a r t
o f Bbest i s d e r iv e d f r o m a s in g le c o u n tr y ! S c a l in g t h e b u b b le s b y
Bcurrentt w o u l d m ix t h e in f o r m a t io n o n t h e s i z e /p r o d u c t iv i t y
w it h th a t o n £ A .
W e d is a g r e e . T h e s c a l in g o f t h e b u b b le s d o e s h ig h l ig h t t h e
r e la t iv e im p o r ta n c e o f d i f f e r e n t a r e a s /c o u n t r ie s , w h i l e th e
in f o r m a t io n o n w h e t h e r a im s h a v e o r n o t b e e n a c h ie v e d is
a d e q u a t e ly r e p r e s e n t e d in th e b a c k g r o u n d c o lo u r . T h e
s u g g e s t e d c h a n g e w o u l d r e d u c e th e in f o r m a t io n c o n t e n t o f th e
p lo t , a n d w o u l d n o t s im p l i f y th e in t e r p r e ta t io n .
T h e R e v ie w G r o u p s u g g e s t s r e p la c in g c o lo u r s b y s a d / h a p p y
s y m b o l s , w h i l e l o s in g th e in f o r m a t io n o n th e r e la t iv e
im p o r t a n c e o f a r e a s . T h e la r g e r e d b u b b le fo r F r a n c e
d o m in a t e s th e p lo t , r e f le c t in g t h e d o m in a t in g s h a r e o f t h e to ta l
s t o c k b e in g lo c a t e d in F r a n c e . W e d o n o t u n d e r s t a n d w h a t th e
R e v ie w G r o u p w a n t s t o a c h ie v e , b y r e m o v i n g e s s e n t ia l
in f o r m a t io n .
Joint EiFAAC/ICES/CFCM WCEEL REPORT 2014 183
53 p .3 6 , S e c 6 .6 : th e f ir s t p a r a g r a p h s ta t e s , T h is i s e d it in g .
'T h e a n th r o p o g e n ic m o r ta l i t y L A is
e s t im a te d to be j u s t a t (a vera g ed o ve r
r e p o r t in g E M U s ) o r fa r a b o ve (a vera g ed
o v e r r e p o r t in g c o u n tr ie s ) th e p r e c a u tio n a r y
le v e l th a t w o u ld be in a cc o rd a n ce w i th IC E S
g e n e ra l p o l ic ie s fo r re c o v e r in g s to ck s (fo r
E M U su rn s: L A = 0 .4 1 w i th ta r g e t 0 .4 2 ; f o r
c o u n t r y s u m s : L A = 1 .4 0 w i th ta r g e t 0 .1 4 ) . '
It i s d i f f ic u l t t o u n d e r s t a n d t h e v a lu e s
f o r t h e t a r g e t Z A s . In r e fe r e n c e to F ig u r e
6 .1 , t h e s u m o f t h e b io m a s s in d ic a t o r
o v e r a ll E M U s ( to p p a n e l o f F ig u r e 6 -1 )
s h o w s th e BcunWBo a t a v a lu e o f 18%
w h i c h w o u l d g í v e a m a x im u m £ A o f
0 .4 1 a c c o r d in g t o t h e r u le (0 .9 2 *
Bcurren,/40%Bo = 0.92 * 18%Bo / 40%Bo). F o r
t h e c o u n t r y s u m , B curroi t/Bo e q u a ls 6%
w h i c h w o u l d g i v e a m a x im u m E A o f
0.14 (0.92 * 0.06/0.40). P e r h a p s th e
f o l l o w i n g w o u l d b e c le a r e r to th e
r e a d e r : ‘ T h e b io m a ss o fe s c a p in g s i lv e r eel
CBcurrmt) e s t im a te d o v e r a ll E M U s r e p o r tin g
w a s 1 8 % o fB o . T h e m a x im u m L A f o r th a t
le v e l o f s p a w n e r p r o d u c tio n eq u a ls 0 .41 (i.e.
0 .9 2 * 0 .1 8 /0 .4 0 ) . T h e e s t im a te d rea lize d £ A
w a s 0 .4 2 , a t th e m a x im u m leve l. T h e
b io m a ss o fe s c a p in g s i lv e r ee l e s t im a te d o v e r
a ll r e p o r t in g c o u n tr ie s w a s 6 % o fB o . T h e
m a x im u m L A f o r th a t le v e l o f s p a w n e r
p r o d u c tio n e q u a ls 0 .1 4 (i.e . 0 .9 2 *
0 .0 6 /0 .4 0 ) . T h e e s t im a te d r e a lize d L A w a s
1 .4 0 , g r e a t ly a b o ve th e L A l i m i t /
A n d
B u t t h i s c o m m e n t s h o u l d b e c o n s id e r e d
i n th e l i g h t o f w h a t w a s m e n t io n e d
a b o v e r e g a r d in g £ A = 0 .9 2 fo r Bbcs, = Bo
r a th e r t h a n fo r Bcuncnt = 40% Bo.
Section 7, Eel spec ific reference
po in ts based on the S-R re la tionsh ip
5 4 T h e d e v e l o p m e n t o f t h e a p p r o p r ia t e
t im e s e r i e s h a s p r o v e n t o b e x h e W G E E L in t e n d s to d e v e l o p a S to c k A n n e x in t h e f u tu r e to
c h a l l e n g in g . E f fo r t s o f E U M e m b e r a d d r e s s t h is i s s u e - s e e A n n e x 4: R e s p o n s e t o G e n e r ic T o R s
S ta te s to p r o v id e e s t im a t e s o f
e x p lo i t a t io n r a te s w i t h w h i c h to d e r iv e
e s t im a t e s o f t o t a l a b u n d a n c e a n d o f
s p a w n e r s i s a n im p o r t a n t s t e p .
H o w e v e r , t h e W o r k in g G r o u p n e e d s to
d o c u m e n t t h e in p u t d a ta , t h e m e t h o d s
fo r a g g r e g a t in g f r o m lo c a l s c a le s to
e c o r e g io n a n d e v e n t u a l l y t h e s p e c ie s
s c a le , a n d to b e c le a r e r o n th e
l im i t a t io n s o f t h e d a ta a n d th e m o d e ls
u s e d . A s p r e s e n t e d , th e r e r e m a in m a jo r
i s s u e s w i t h h o w th e c a t c h e s a r e
c o l le c t e d , c o l la t e d a n d p a r t i t i o n e d in t o
l i f e s t a g e , a n d h o w m is s in g d a ta a r e___________________________________________________________________________________
184 | Joint EIFAAC/ICES/CFCM WGEEL REPORT 2014
t r e a te d . T h e r e c o n s t r u c t io n o f c a tc h e s
b a c k in t im e fo r a l l c o u n t r ie s i s n o t
c u r r e n t ly a c c e p ta b le b a s e d o n th e
in f o r m a t io n p r o v id e d b y th e W o r k in g
G r o u p . I f t h is c o m p o n e n t o f th e
r e c o n s t r u c t io n i s f la w e d , th e n a ll
s u b s e q u e n t a n a ly s e s a n d d is c u s s i o n s
a r e p r e m a tu r e .
5 5 I d e a l ly , o n e w o u l d w a n t t o u n d e r t a k e
t h e S -R a n a ly s i s w i t h a b io m a s s e s t im a t e
f o r th e e n t ir e p a n m ic t ic s to c k , b u t th e r e
i s c le a r ly s u b s t a n t ia l s i lv e r e e l
p r o d u c t io n w h i c h i s o u t s i d e th e s c o p e
c o v e r e d in th e a n a ly s is . F o r e x a m p le ,
s i lv e r e e l f i s h e r i e s a r e g e n e r a l ly d ir e e t e d
a t p r o d u c t io n f r o m r iv e r s y s t e m s , w h e r e
s i lv e r e e l s c a n b e r e a d i ly c a u g h t b y
in t e r c e p t o r y g e a r a t p r e d ic t a b le t im e s o f
t h e y e a r . S i lv e r e e l s p r o d u c e d in s a l in e
a r e a s c a n n o t b e r e a d i ly c a u g h t b y
in t e r c e p t o r y g e a r a n d a r e g e n e r a l ly n o t
s u b je c t t o t a r g e t e d f is h e r ie s (w d th th e
e x c e p t i o n o f th e B a lt ic S e a ) . In a d d i t io n ,
in th e e a s t e m a n d s o u t h e m
M e d it e r r a n e a n S e a , th e r e a r e e e l
f i s h e r i e s w h i c h m a y r iv a l in s i z e t h o s e
o f E u r o p e a n c o u n t r ie s (F ig . 9 -1 0 ) , b u t
la n d in g s f r o m t h e s e c o u n t r ie s a r e n o t
in c l u d e d in th e a n a ly s is , p e r h a p s
b e c a u s e th e r e a r e in s u f f i c ie n t h a r v e s t
d a ta . The question therefore arises as
to how robust the approach is without
these data. If th e b io m a s s v a lu e u s e d in
th e m o d e l u n d e r e s t im a t e s t h e tr u e s to c k
b io m a s s b u t i s l in e a r ly r e la t e d to it , it
m a y b e r e g a r d e d a s a b io m a s s in d e x
r a th e r t h a n a n e s t im a t e . H o w e v e r , th e r e
i s a n e e d t o d e t e r m in e w h e t h e r th e
in d e x m a y b e b ia s e d a n d w h e t h e r t h e S -
R a n a ly s i s w o u l d b e v a l id i f th is
b io m a s s in d e x w a s 90% , 50% , 25% e tc o f
t h e t r u e b io m a s s v a lu e .
5 6 N o e v i d e n c e h a s b e e n p r e s e n t e d in t h is
r e p o r t t o r e in fo r c e th e d e p e n s a t io n
a r g u m e n t , a n d s u c h a c o n c lu s io n is
p r e m a tu r e . I f t r u e b io m a s s is g r e a te r
th a n c a lc u la t e d b io m a s s , w o u l d th e
p r o p o s e d c o n c lu s io n s r e g a r d in g s to c k
d y n a m i c s a t l o w r e c r u itm e n t r e m a in
v a lid ?
E g y p t d a ta d o e s n o t s e e m r e l ia b le ( s e e c a t c h d a ta C h a p t e r 2 ).
W e a r e w o r k in g to o b t a in d a ta fo r m is s in g c o u n t ie s , b u t in th e
m e a n t im e s o m e a r e s t i l l m is s in g . T h u s o u r S S B s e r ie s a re
in c o m p le t e a n d ta k e t h e a s s u m p t io n th a t m is s in g d a ta a r e
p r o p o r t io n a l to d o c u m e n t e d d a ta a n d t h u s th a t m is s in g S SB
a r e p r o p o r t io n a l to d o c u m e n t e d SSB .
U n d e r e s t im a t e o f S S B t r a n s la t e s th e c u r v e to t h e r ig h t , a n d
d o e s n o t c h a l l e n g e th e Bstoppa c o n c e p t . H o w e v e r d e e p e r
a n a ly s i s i s n e e d e d to ta c k le t h is p o in t .
S e e C h a p te r 3 a n d c o m m e n t 10
Joint EIFAAC/ICES/GFCM WGEEL REPORT 2014 185
5 7 T h e m a n a g e m e n t a d v ic e fo r E u r o p e a n
e e l i s t h e s a m e w h e t h e r th e d e c l in e s in
i n d ic e s o f r e c r u itm e n t a r e d u e to
d e p e n s a t i o n , d e c l in e s in th e s u r v iv a l o f
th e e a r ly l i f e s t a g e s a t s e a o r d e c l in e s in
s i lv e r e e l s p a w n e r q u a l i t y a s s o c ia t e d
w ít h c o n t in e n t a l fa c to r s . R e g a r d le s s o f
th e m e c h a n is m , th e o n ly a c t io n th a t c a n
b e ta k e n to in c r e a s e r e c r u itm e n t is to
in c r e a s e s p a w n in g e s c a p e m e n t b y
r e d u c in g a n t h r o p o g e n ic m o r ta l i t y o n
th e c o n t in e n t a l s t a g e s o f E u r o p e a n e e l .
T h e r e i s n o g u a r a n t e e th a t r e d u c in g
m o r t a l i t y a t t h o s e s t a g e s w i l l r e s u lt in
in c r e a s e d r e c r u it m e n t , b u t i t i s m o r e
l i k e ly th a t r e c r u itm e n t w i l l c o n t in u e to
b e l o w o r d e c l in e fu r th e r i f
a n t h r o p o g e n ic m o r ta l i t y r a t e s r e m a in
h ig h , a s e s t im a t e d in th is a s s e s s m e n t .
5 8 T h e d e t a i l e d d i s c u s s i o n in S e c t io n 7 is
n o t e s s e n t ia l fo r p r o v id in g m a n a g e m e n t
a d v ic e . H ig h e r p r io r i ty f o r th e W o r k in g
G r o u p is i m p r o v i n g t h e c a tc h d a ta ,
b io lo g i c a l s a m p l in g a n d t h e in d ic e s o f
a b u n d a n c e f r o m t h is p o in t fo r w a r d .
5 9 S e c t io n 7 .7 (p .5 3 ) c o n s id e r s th e
e s t im a t i o n o f Biim. H o w e v e r , i f Bo i s 1 9 3
k t ( n o t m i l l i o n t o n s - s e e e d ito r ia l
c o m m e n t s ) th e n th e l im it r e fe r e n c e
p o in t in t h e E U E e l R e g u la t io n (40% o f
Bo) is a b o u t 7 7 k t , w h i c h i s >70% g r e a te r
th a n a n y Bmrrent in th e h is to r ic a l t im e
s e r ie s . T h is w o u l d im p ly th a t th e s t o c k
h a s n o t b e e n s u s t a in a b ly m a n a g e d fo r
m o r e th a n 6 0 y e a r s , w h i c h t h e n c a s t s
d o u b t o n u s i n g th e 1 9 6 0 -7 9 p e r io d a s a
b a s e l in e fo r a s s e s s m e n t . T h e r e a re
c le a r ly v a r io u s p o s s ib l e e x p la n a t io n s fo r
t h e s e a n o m a l ie s ( in c o r r e c t e s t im a t io n o f
Bo, (3 su , e tc ) a n d t h e y n e e d t o b e
e x p lo r e d .
6 0 In t h e a b s e n c e o f a S to c k A n n e x , a l l th e
p a r a m e t e r s u s e d in th e e q u a t io n s a n d
th e ir s u f f i x e s n e e d to b e d e f in e d a n d
p a r a m e t e r v a lu e s u s e d in th is m o d e l
( r e fe r r e d t o in S e c t io n s 7 .4 a n d 7 .5 )
s h o u l d b e p r o v id e d in t h e r e p o r t. D a ta
a r e p r o v id e d fo r 6 7 o f th e 81 E M U s b u t
m o r e in f o r m a t io n s h o u ld b e p r o v id e d
o n w h e r e th e d a t a h a v e c o m e fr o m a n d
f l a w s a s s o c ia t e d w i t h th e m .
D is c u s s e d in C h a p te r 3 .
A n d s e e # 1 2 a ls o
D o n ' t a g r e e . E s s e n t ia l fo r a d d r e s s in g th e m a n a g e m e n t
r e s p o n s e to v e r y l o w s to c k a n d r e c r u itm e n t . W e r e r e q u e s t e d to
f o l l o w u p t h is l in e o f t h in k in g b y A C O M .
S e e C h a p te r 3 .
W G E E L in t e n d s t o d e v e l o p a S to c k A n n e x in th e f u tu r e to
a d d r e s s th is i s s u e - s e e A n n e x 4: R e s p o n s e t o G e n e r ic T o R s
186 | Joint EIFAAC/ICES/GFCM WGEEL REPORT 2014
6 1 p .3 8 . S e c 7 .2 , l i n e 2: th e t e x t s u g g e s t s
th a t th e b e s t a v a i la b le p r o x y fo r S SB is
th e e s c a p e m e n t th a t e x i s t s a f te r a l í o f th e
f i s h e r i e s a n d o t h e r m o r t a l i t ie s (b o th
n a tu r a l a n d a n t h r o p o g e n ic ) in
c o n t in e n t a l a n d li t to r a l w a te r s h a v e
o c c u r r e d . H o w e v e r t h is in f o r m a t io n is
a ls o u n a v a i la b le , s o th e r e a l p r o x y is
r e p o r te d la n d in g s .
6 2 p .4 0 , p a r a 2: th e r e p o r t s t a t e s th a t th e
c a t c h e s w e r e fu r th e r d iv id e d b y s t a g e
( y e l lo w a n d s i lv e r e e l ) b a s e d o n
c o l le c t e d s e r i e s m a d e a v a ila b le to
W G E E L o r b y e x p e r t k n o w le d g e . T h is
in f o r m a t io n s h o u l d b e in c l u d e d in a
t a b le .
6 3 p .4 0 , S e c 7 .1 1 .1 : (N B S e c t io n n u m b e r is
in c o r r e c t .) A l l t h e p a r a m e t e r s u s e d in
th e e q u a t io n s a n d th e ir s u f f ix e s n e e d to
b e d e f in e d : s a p p e a r s to r e fe r t o s i lv e r
e e l s b u t i s n o t r e a l ly r e q u ir e d ; H
a p p e a r s to b e t h e in s t a n t a n e o u s r a te o f
a n t h r o p o g e n ic m o r ta l i t y b u t i s la te r s e t
a t 0 s o c o u ld b e o m it t e d ; 't ' i s u n d e f in e d
b u t i s s h o w n t o r e fe r to y e a r in S e c 7 .5
a n d , a s s u c h , s h o u l d b e s h o w n a s a
s u f f ix (a t p r e s e n t i t a p p e a r s to b e a
v a r ia b le ) . F o r c la r ity , a s y m b o l o th e r
t h a n P s h o u l d b e u s e d fo r e x p lo i t a t io n
r a te , a s i t i s e a s i l y c o n f u s e d w i t h th e
b io m a s s s y m b o l .
6 4 p .4 0 , S e c 7 .4 : T h e u s e o f e x p e r t o p in io n
to d e r iv e s t a r t in g v a lu e s fo r e x p lo i t a t io n
r a te s i s a g o o d b e g in n in g in th e e f f o r t to
d e v e l o p e s t im a t e s o f s i lv e r e e l
e s c a p e m e n t . H o w e v e r , th e r e is
in s u f f i c ie n t in f o r m a t io n to a l l o w th e
r e a d e r to u n d e r s t a n d h o w th e e x p e r t
o p in io n s o n e x p lo i t a t io n r a te w e r e
d e v e l o p e d , w h y t h e a g g r e g a t io n fo r
IC E S e c o r e g io n s a t t h is s t a g e , a n d h o w
t h e e x p lo i t a t io n r a te s fo r a n e c o r e g io n
a n d t im e p e r io d w e r e d e t e r m in e d
6 5 p .4 7 , b e l o w F ig u r e 7 .6 , l in e 3: a r e fe r e n c e
is g iv e n t o ' e q u a t io n (0 ) ', b u t o n ly o n e
e q u a t io n is n u m b e r e d (p .4 1 ) s o th is is
n o t v e r y h e lp f u l .
6 6 p .4 9 , F ig u r e 7-8 : th e r e a p p e a r s to b e a
l e v e l i n g o r u p t u m o f e s c a p e m e n t in th e
B a lt ic , N o r t h S e a a n d C e lt ic S e a b u t n o t
B a y o f B is c a y a n d M e d ite r r a n e a n ; c a n
th is b e a t t r ib u te d t o t h e m a n a g e m e n t
m e a s u r e s ?
6 7 p .5 1 , F ig u r e 7 -10 : n e e d to m a k e c le a r in
c a p t io n th a t c a t c h e s a r e s i lv e r e e l s o n ly .
S e c 7 .4 .1 f r o m W G E E L 2 0 1 3 e x p l i c i t l y e x p la in s h o w w e a s s e s s
e s c a p e m e n t a f te r a n t h r o p o g e n ic m o r t a l i t ie s in th e c o n t in e n ta l
p h a s e . M o r e o v e r m e m b e r s t a t e s a r e r e q u ir e d b y th e e e l
r e g u la t io n to d e l iv e r e s c a p e m e n t f ig u r e (a r t ic le 9 .1 .a )
W G E E L in t e n d s to d e v e l o p a S to c k A n n e x in th e f u t u r e to
a d d r e s s th is i s s u e - s e e A n n e x 4: R e s p o n s e to G e n e r ic T o R s
S e c t io n d e le t e d in th is y e a r 's r e p o r t
W G E E L in t e n d s t o d e v e l o p a S to c k A n n e x in th e f u tu r e to
a d d r e s s t h is i s s u e - s e e A n n e x 4: R e s p o n s e t o G e n e r ic T o R s
S e c t io n d e le t e d in t h is y e a r 's r e p o r t
T h e f ig u r e 7 -8 s h o w s m o r e v a r ia t io n f r o m y e a r t o y e a r a n d n o
c le a r u p t u m . S e e a l s o C h a p te r 3.
W G E E L in t e n d s t o d e v e l o p a S to c k A r tn e x in th e f u tu r e to
a d d r e s s th is i s s u e - s e e A n n e x 4: R e s p o n s e t o G e n e r ic T o R s
Joint EIFAAC/iCES/CFCM WGEEL REPORT 201 4 187
6 8 p .5 1 , S e c 7 .6 , p a r a 2: L in e s 2 - 5 p r o v id e
a n a w k w a r d a n d in c o r r e c t d e s c r ip t io n
o f S - R r e la t io n s h ip s . T h e B e v e r t o n -
H o l t f u n c t ío n h a s m a x im u m
r e c r u itm e n t o c c u r r in g a t in f in i t e
s p a w n e r a b u n d a n c e , n o t c o m p e n s a t io n
f o r h ig h r e c r u itm e n t . B o th R ic k e r a n d
B e v e r t o n -H o lt h a v e m a x im u m r e c r u its
p e r s p a w n e r a t th e o r ig in , d e c l in in g
m o n o t o n i c a l l y w i t h in c r e a s in g s p a w n e r
a b u n d a n c e , a n d r e c r u itm e n t in c r e a s e s
f a s te r t h a n S S B fo r S S B l e s s t h a n th e
v a lu e fo r m a x im u m g a in .
6 9 p .5 3 , s e c o n d F ig u r e 7 -9 : y - a x is la b e l
s h o u l d b e 'B io m a s s / Bo (% )' a n d th is
s h o u l d b e r e f le c t e d in t h e c a p t io n .
70 p .5 4 , S e c t io n 7 .8 , p a r a 5: T h is p a r a g r a p h
p r o v id e s a c o n f u s i n g (o r in c o r r e c t )
e x p la n a t ío n o f th e r e p la c e m e n t l in e ; in
th e a b s e n c e o f d e n s i t y - d e p e n d e n t
p r o c e s s e s t h e p o t e n t ia l fo r s p a w n in g
s t o c k p r o d u c t io n s h o u l d d e f in e d b y th e
g r a d ie n t o f th e S -R r e la t io n s h ip n o t b y
th e r e p la c e m e n t l in e .
71 F ig u r e 9 -9 , s h o w i n g 'T o ta l la n d in g s (a ll
li fe s ta g e s ) fr o m 2 0 1 3 C o u n tr y R e p o r ts ( n o t
a ll c o u n tr ie s rep o r ted ); th e co rrec ted tr e n d
h a s m is s in g d a ta f i l i e d b y G L M . ' s h o u ld b e
m o v e d t o th is s e c t io n o f th e r e p o r t a s
t h i s i s th e f ig u r e fo r m o d e l l e d la n d in g s .
F ig u r e 9 -9 s h o u l d n o t a p p e a r in S e c t io n
9 a s i t g iv e s th e im p r e s s io n to th e r e a d e r
th a t l a n d in g s a r e r e p o r te d fo r a ll t h o s e
c o u n t r ie s b a c k t o 1 9 4 5 .
Section 8, D iscussion o f assessm ent
m ethods and resu lts
Section 9, Data and trends
72 S e c t io n 9 .1 d e s c r ib e s t h e t im e - s e r ie s o f
d a t a o n g la s s a n d y e l lo w e e l
r e c r u it m e n t . T h e s e le c t io n o f t ím e s e r ie s
a n d th e m e t h o d u s e d to c o m b in e th e m
n e e d m o r e e x p la n a t io n ( s e e a ls o
e d i t o r ia l c o m m e n t s ) . T h e fa c t th a t s o m e
t im e s e r i e s h a v e b e e n te r m in a te d
b e c a u s e o f la c k o f r e c r u it s (e .g . E m s a n d
V id a a ) s u g g e s t s th a t th e u s e o f t im e
s e r i e s s t a r t in g a n d e n d in g a t d if f e r e n t
t im e s m a y in t r o d u c e b ia s e s . I t is
r e c o g n is e d th a t e f f o r t s m u s t b e m a d e to
m a k e th e b e s t u s e o f a v a i la b le d a ta , b u t
t h e d a t a c a n b e t e s t e d to s e e w h e t h e r
s u c h b ia s e s e x i s t . F o r e x a m p le , i f th e r e
w e r e t w o g r o u p s o f t im e s e r i e s w i t h
g r o u p 1 s p a n n in g th e p e r io d fr o m 1 9 8 0
t o 2 0 0 0 a n d g r o u p 2 th e p e r io d fr o m
1 9 8 0 to t h e p r e s e n t , th e g r o u p s c o u ld b e
c o m p a r e d o v e r th e in i t i a l p e r io d t o s e e
_________ w h e t h e r th e i o s s o f g r o u p 1 m ig h t _________
D e s c r ip t io n r e v i s e d C h a p te r 3 .
S e e # 5 9
S in c e w e h a v e c o n c e r n a b o u t Bo e s t im a t e , t h e b io m a s s i n th e
s t o c k - r e c r u i t m e n t g r a p h a r e k e p t in t o n n e s
P a r a g r a p h r e m o v e d in th is y e a r 's r e p o r t
S in c e th e c h a p t e r h a s b e e n r e s t r u c tu r e d , th e r e i s n o m o r e
r e a s o n t o m o v e th is f ig u r e
None
T h e W G E E L 2 0 1 0 c o n s id e r e d s p a t ia l s tr u c tu r e o f th e
r e c r u itm e n t . T a b le 2 .1 p l 5 , fo r th e s e r i e s d i s c o n t in u e d in
F r a n c e , t h e c lu s t e r s a r e d if f e r e n t , g r o u p s l ( A d o u r 2 s e r ie s ,
G ir o n d e 2 s e r ie s ) , 3 L o ir e , 5 V ila in e . P le a s e a l s o lo o k a t f ig u r e
2 .1 6 p a g e 43: T h e B is c a y s e r ie s a r e in r e d o n t h e r ig h t , t h e y
h a v e th e s a m e tr e n d a s t h o s e in B r i t is h I s l e s o r t h e
M e d ite r r a n e a n .
188 I Joint EIFAAC/ICES/GFCM WCEEL REPORT 2014
in t r o d u c e a b ia s in th e la t e r y e a r s .
7 3 L im it e d in f o r m a t io n i s p r o v id e d o n th e
t im e s e r i e s th a t a r e e x c lu d e d fr o m th e
a n a ly s i s a n d t h e r e a s o n s . I t w o u l d b e
h e lp f u l to in c l u d e in T a b le s 9 -1 to 9 -3
( A n n e x 7 ) t h e s ta r t a n d e n d d a t e o f th e
t im e s e r ie s , th e n u m b e r o f y e a r s fo r
w h i c h e s t im a t e s a r e a v a ila b le , a n d a n y
c o m m e n t s a b o u t p o t e n t ia l u n c e r ta in ty
in t h e d a ta , e .g . i f s a m p l in g i s c o n d u c t e d
u p s t r e a m o f a f is h e r y . M o r e
e x p la n a t io n i s r e q u ir e d o n th e
f lu c t u a t in g n a t u r e o f t h e r e c r u itm e n t
s e r i e s in F ig u r e s 9 -3 , 9 -4 a n d 9 -5 .
7 4 S e c t io n 9 .2 d e s c r ib e s t r e n d s in y e l lo w
e e l a n d s i lv e r e e l a b u n d a n c e f r o m a
s m a l l n u m b e r o f m o n it o r in g
p r o g r a m m e s . T h e d a ta a r e n o t
p r e s e n t e d in ta b u la r f o r m a n d a re
d i f f ic u l t t o in t e r p r e t f r o m F ig u r e 9 -7 .
T h e d a ta a r e l im i t e d b u t s u f f i c ie n t to
s u g g e s t th a t th e r e la t io n s h ip b e t w e e n
r e c r u it m e n t a n d y e l lo w / s i l v e r
a b u n d a n c e c a n b e c o m p le x . T h e s e
c o m p le x i t i e s p r o v id e a n o t h e r r e a s o n fo r
s u g g e s t i n g n o n - s t a t io n a r i t y in a n y S - R
r e la t io n s h ip s .
7 5 T h e c o n v e r s io n o f s t o c k ín g n u m b e r s to
g la s s e e l e q u iv a le n t s s h o u l d a t t e m p t to
i n c l u d e a l l m o r t a l i t y b e t w e e n c a p tu r e
a n d r e le a s e (p .1 0 4 ) . I t i s n o t c le a r w h y
t h is h a s n o t b e e n m o d e l l e d .
7 6 S to c k ín g r e m a in s a n im p o r ta n t , a n d
c o n t e n t io u s , i s s u e fo r e e l m a n a g e m e n t
a n d s o m o r e s h o u l d b e m a d e o f t h e s e
d a ta . I t m a y b e p o s s ib l e , f o r e x a m p le , to
a s s e s s t h e p r o p o r t io n a l lo s s o r g a in o f
g la s s e e l e q u iv a le n t s in d i f f e r e n t a r e a s to
a s s e s s t h e e x t e n t th a t s t o c k in g c o u ld b e
im p a c t in g s t o c k a b u n d a n c e .
7 7 p .6 2 , S e c 9 .1 1 .1 a n d F ig u r e 9 -1 : It is
u n c le a r w h a t t h e f ig u r e i s s h o w in g ; th e
n u m b e r o f a v a i la b le t im e s e r ie s s h o u ld
n e v e r d e c r e a s e , s o i s t h i s th e n u m b e r o f
'a c t iv e ' t im e -s e r ie s ? D o e s th is ig n o r e
g a p s in th e t im e s e r ie s ?
N o n e a r e e x c lu d e d , s e r ie s a r e n o w s c a le d t o t h e ir a v e r a g e
v a lu e b e fo r e t h e G L M . T h e s e r ie s th a t a r e e x c lu d e d f r o m s c a le d
g r a p h s a r e d e s c r ib e d n o w
T h e W G E E L h a s r e m o v e d th e y e l lo w e e l a n d s i lv e r e e l tr e n d
s e r i e s g r a p h , t h o s e s h o u l d n o t b e c o n s id e r e d a s r e p r e s e n ta t iv e
o f th e tr e n d in s to c k s iz e .
T h e r e la t io n b e t w e e n r e c r u it s a n d s u b s e q u e n t y e l lo w e e l
a b u n d a n c e h a s n o r e la t io n t o th e s t o c k - r e c r u it - r e la t io n .
A n t h r o p o g e n ic m o r t a l i t y o n y e l lo w a n d s i lv e r e e l in te r fe r e .
A n a s s u m e d a n d r e a s o n a b le M w a s a p p l ie d a n d th a t m o s t ly in
o r d e r to fa c i l i t a t e c o m p a r i s o n s b e t w e e n d if f e r e n t s i z e s o f e e l s
u s e d fo r s to c k in g . T h e p o s s ib l e m o r t a l i t ie s w h e n u s i n g
d if f e r e n t m e t h o d s t o c a tc h g la s s e e l s i s a t o ta l ly d i f f e r e n t i s s u e
th a t h a s n o t h in g t o d o w i t h t h i s s im p le w a y o f " e q u a l is a t io n " ,
a n d h a s t o b e a d d r e s s e d in a n o t h e r c o n te x t .
T h is i s tr u e a n d a n e t b e n e f i t i s a p r e r e q u is i t e f o r s t o c k in g . T h is
i s s u e h a s b e e n d e a l t w i t h in r e c e n t W G E E L R e p o r ts , e .g . in th e
c h a p te r o n S T O C K E E L in th e W G E E L R e p o r t f r o m 2 0 1 1 1 .
Y es a c t iv e s e r ie s , c o r r e c te d in t h e c a p t io n n o w .
Joint EIFAAC/ICES/CFCM WCEEL REPORT 2014 189
7 8 p .6 2 , f in a l p a ra : i t a p p e a r s th a t t im e
s e r i e s a r e o n ly u s e d in th e a n a ly s i s i f
t h e y e x c e e d a c e r ta in n u m b e r o f y e a r s ,
a n d i t w o u l d b e h e lp f u l i f th is w a s
e x p la i n e d h e r e r a th e r th a n in S e c t io n
9 .1 1 .3 ; h o w la r g e a g a p i s a c c e p ta b le ?
T h e t im e s e r i e s a r e s c a le d to th e 1 9 7 9 -9 4
m e a n , b u t it i s n o t c le a r w h e t h e r d a ta
m u s t b e a v a i la b le fo r th a t fu l l p e r io d o r
fo r a c e r ta in n u m b e r o f y e a r s w i t h in it;
th i s i s a p o t e n t ia l s o u r c e o f b ia s . It
a p p e a r s th a t a n y t im e s e r ie s s p a n n ín g
th e 1 9 7 9 -9 4 p e r io d m ig h t b e u s e d ; s o
h o w w a s th e 3 5 y e a r l im i t d e t e r m in e d ?
7 9 p .6 4 , p a r a 2: t o a id r e a d in g in f u tu r e
y e a r s , s p e c i f i c y e a r s s h o u l d b e
r e fe r e n c e d , i .e . 'In 2 0 1 2 , . . . ' , e tc . r a th e r
t h a n 'L a s t y e a r , . . . ' .
8 0 Is a n y la g (n e g a t iv e ) a p p l i e d to th e
y e l l o w e e l t im e s e r ie s to c o m p a r e t h e m
w it h t h e g la s s e e l s - o r s h o u l d it b e ? T h e
y - a x i s c a p t io n in d ic a t e s a r a t io , b u t th e
d a ta s h o w %; th is s h o u l d b e th e s a m e a s
F ig u r e 9 -4 .
Y es in 2 0 1 3 th e s e r ie s h a d to h a v e d a t a in th e 1 9 7 9 -1 9 9 4 p e r io d
f o r th e c a lc u la t io n o f t h e W G E E L r e c r u it m e n t in d e x , n o t in
2 0 1 4 . 3 5 y e a r s l im it w a s o n ly u s e d t o l i m it th e n u m b e r o f s e r ie s
s h o w n in g r a p h 4 .3 a n d 4 .4 p r e s e n t in g th e r a w d a ta . T h e o n ly
l im it a t io n n o w i s o f c o u r s e h a v in g d a ta in th e b a s e l in e p e r io d .
N o t e d
81
8 2
8 3
p .6 5 : F ig u r e 9 -4 i s n o t r e fe r r e d t o in th e
t e x t a n d h a s a c o n f u s i n g c a p t io n ; th e
t im e s e r i e s o f g la s s a n d y e l lo w e e l a r e
n o t s h o w n in th e f ig u r e a s s u g g e s t e d ; in
a d d i t io n th e d i f f e r e n c e b e t w e e n th e
'm e a n v a lu e s ' s h o w n in F ig u r e s 9 -2 a n d
9 -4 i s u n c le a r (o r a r e t h e y t h e s a m e ? ) .
p .6 6 , p a r a 4: t h e f ir s t t w o s e n t e n c e s s a y
th e s a m e th in g ; n o in d ic a t io n i s g iv e n o f
th e s ta t e o f th e r e c r u itm e n t in d ic e s
b e t w e e n 2 0 0 6 a n d 2 0 1 2 ( i.e . w h e r e th e
in d ic e s h a v e in c r e a s e d .)
p .6 8 , F ig u r e 9 -5 : i t s h o u ld b e p o s s ib l e to
a d d c o n f id e n c e l im it s fo r t h e G L M
e s t im a t e s .
N o , a n d n o i t w o u l d b e d i f f ic u l t t o h a v e a n id e a o f t h e a g e
s t r u c tu r e o f t h e d if f e r e n t s e r i e s w h i c h in c lu d e B a lt ic s e r i e s a n d
s o m e o th e r p la c e s in E u r o p e . T h e s c a l i n g i s d o n e o n t h e s a m e
p e r io d a s t h e g la s s e e l s e r ie s , t h o u g h i t c o u ld h a v e s p a n n e d a
lo n g e r p e r io d a s m o r e th a n fo u r r e l ia b le s e r i e s w e r e a v a ila b le
a f te r 1 9 4 6 . B u t w e h a v e c h o s e n t o b e c o n s i s t e n t b e t w e e n th e
t w o t im e t r e n d s .
N o t e th a t f ig u r e s 4 .5 4 .6 a n d th e t a b le s 4 .1 4 .2 c o n s i s t e n t ly
e x p r e s s th e r e c r u itm e n t a s a p e r c e n ta g e o f th e b a s e l in e p e r io d
1 9 6 0 -1 9 8 0 .
W e d o n o t u n d e r s t a n d th is c o m m e n t . T h e f ig u r e d o e s s h o w th e
a v e r a g e o f t h e g la s s e e l ( in b lu e ) a n d y e l l o w e e l ( in b r o w n )
s e r ie s . S o m e t e x t h a s b e e n a d d e d to c la r if y w h y t h is f ig u r e is
d r a w n . T h e v a lu e i s t h e s a m e a s in f ig u r e 4 .3 a n d th is h a s b e e n
e x p la in e d b y a f o o t n o t e r e fe r e n c e .
N o t e d
8 4 p .6 9 , F ig u r e 9 -6 : in d ic a t e s th a t th e r e i s a
s m o o t h e d tr e n d w i t h c o n f id e n c e
in t e r v a ls b u t th e r e i s n o d e s c r ip t io n o f
h o w th e s m o o t h i n g w a s p e r fo r m e d .
8 5 p . 6 9 -7 0 : It i s d i f f ic u l t to c o n c lu d e
a n y t h i n g f r o m th e d e s c r ip t io n o f th e
y e l l o w e e l t im e s e r ie s . T h e r e i s n o
r e fe r e n c e to F ig u r e 9 -7 in t h e te x t , a n d it
i s n o t c le a r w h a t c o n c lu s io n i s d r a w n
f r o m t h e s e d a ta .
N o . W e w o u l d t h e n h a v e to d o th e a v e r a g e o f th e c o n f id e n c e
in t e r v a ls o f th e p r e d ic t io n s o f a l l s i t e s . A n d th is w o u l d n o t b e
m e a n in g f u l .
P o in t t a k e n , s m o o t h i n g r e m o v e d
N o o v e r a l l c o n c lu s io n s , f ig u r e d e le t e d f r o m t h e r e p o r t
Y e llo w e e l a b u n d a n c e
190 | Joint EIFAAC/ICES/GFCM WGEEL REPORT 2014
8 6 T a b le 9 -6 ( A n n e x 7): I t w o u l d b e h e lp f u l
t o c la r ify th e d i f f e r e n c e b e t w e e n y e a r s
fo r w h i c h th e r e a r e n o d a ta , y e a r s w h e n
th e f i s h e r y w a s c lo s e d a n d y e a r s w i t h a
f i s h e r y b u t n o c a tc h ( if th is o c c u r s ) .
8 7 p .7 1 a n d F ig u r e 9 -8 : t h e t e x t r e fe r s to
th r e e S c o t t is h d a ta s e r ie s b u t o n ly o n e is
s h o w n in th e f ig u r e . A d d i t i o n a l d a ta
s e r i e s f r o m S w e d e n a n d F r a n c e a r e
d e s c r ib e d b u t a r e n o t p r e s e n t e d in
t a b le s o r f ig u r e s . W h y n o t?
8 8 p p 7 2 - 7 6 : S e c t io n s 9 -3 a n d 9 -4 b o th
d e s c r ib e la n d in g s d a ta f r o m th e
C o u n t r y R e p o r t s a n d it i s u n c le a r w h y
th e r e a r e t w o s e c t io n s .
8 9 p .7 3 , S e c 9 .3 : th e r e i s n o s p e c i f i c
d e s c r ip t io n o f th e r e p o r te d /e s t im a t e d
[W G E E L : W H A T I S M I S S I N G H E R E ?]
in t h is s e c t io n a n d m o r e in f o r m a t io n is
p r o v id e d e l s e w h e r e in t h e r e p o r t; m o r e
in f o r m a t io n is r e q u ir e d o n h o w
d if f e r e n t p a r ts o f th e f i s h e r i e s h a v e
c h a n g e d ( i.e . g la s s , y e l l o w . s i lv e r e e l) .
H o w h a s th e E U R e g u la t io n a f f e c t e d th e
d a ta , i .e . n a t io n a l c lo s u r e s a n d o th e r
m e a s u r e s ?
9 0 p .7 3 , F ig u r e 9 -9 : T h is f ig u r e s h o u ld n o t
b e p r e s e n t e d in S e c t io n 9 a s it g iv e s th e
im p r e s s io n th a t l a n d in g s a r e r e p o r te d
fo r a l l t h o s e c o u n t r ie s b a c k t o 1 9 4 5 . If
s u c h m o d e l l in g r e s u lt s a r e p r e s e n t e d ,
m in im a l ly , a n a c c o m p a n y in g p a n e l
s h o u l d s h o w th e to ta l r e p o r te d
la n d in g s , t h e m o d e l l e d p r e d ic t e d
la n d in g s , a n d th e p r o p o r t io n o f th e
p r e d ic t e d la n d in g s w h ic h a r e r e p o r te d ;
F ig u r e 2 s h o w s a n e x a m p le d e v e l o p e d
u s i n g th e d a ta in T a b le 9 .6 . It is s tr ik in g
th a t th e r e p o r te d la n d in g s d u r in g 1 9 4 5
t o a b o u t 1 9 9 2 t o t a l le d a b o u t 1 0 0 0 0 t
a n n u a l ly .
9 1 p .7 3 , p a r a 3: ( t h e r e fe r e n c e t o F ig u r e 8 -
1 0 s h o u l d b e F ig u r e 9 -1 0 .) I t w o u l d b e
m o r e h e lp f u l to c o m p a r e th e m e a n c a tc h
o v e r a n u m b e r o f y e a r s in c o u n t r ie s
r e p o r t in g t o W G E E L a n d c o u n t r ie s n o t
r e p o r t in g t o W G E E L r a th e r th a n
h ig h l ig h t i n g 2 0 0 6 .
9 2 p .7 8 , T a b le 9 -7 a n d 9 -8 : It i s u n c le a r
w h a t c a n b e d r a w n f r o m T a b le 9 -7 a n d
n o e x p la n a t io n is p r o v id e d in th e te x t .
S im ila r ly , n o c o n c l u s io n s a r e d r a w n
f r o m T a b le 9 -8 .
I n fo r m a t io n i s g i v e n in th e m a in t e x t ( c o l le c t io n o f la n d in g s
s t a t is t ic s b y c o u n tr y )
D o n e , f ig u r e 9 -8 d e le t e d f r o m t h e r e p o r t , t a b le m o v e d t o th e
a c c o m p a n y in g e l e c t r o n ic a n n e x .
S e c t io n 9 -3 d e s c r ib e c o m m e r c ia l la n d in g s , s e c t io n 9 -4 is
d e d ic a t e d to r e c r e a t io n a l c a tc h e s .
T h is s e c t io n d e a ls o n ly w i t h la n d in g s t a t is t ic s a n d t y p e o f
r e p o r t in g
A g r e e d ; a s w a s d o n e in o u r p r e v i o u s r e p o r ts .
T h e r e m a r k a b le l e v e l o f u n d e r r e p o r t in g h a s b e e n
a n a ly s e d /d is c u s s e d b y D e k k e r (2 0 0 3 ) . T h e a p p a r e n t s ta b i l i t y
f r o m 1 9 4 5 to 1 9 9 2 i s v e r y m is le a d in g . D e t a i l e d in fo r m a t io n ,
c o m p a r a b le o v e r t im e , f r o m a r e a s w i t h c o n s i s t e n t d a ta , d o
s h o w th e d e c l in e .
G r a p h d e le t e d f r o m t h e r e p o r t .
N o t e d
I n fo r m a t io n f u l f i l l e d
Joint EIFAAC/ICES/CFCM WGEEL REPORT 2014 191
93
94
95
96
97
98
99
p .8 1 : S e c t io n s 9 .5 d e a l s w i t h th e
c o m p ila t io n o f d a ta o n s t o c k in g a n d
S e c t io n s 9 .6 e v a lu a t e s th e s í z e a n d
o r ig in o f s t o c k e d f i s h a n d th e
d e v e l o p m e n t o f 'g la s s e e l e q u iv a le n t s ' .
T h e s e S e c t io n s s e e m o u t o f p la c e in th is
s e q u e n c e , a s s e c t io n 9 .7 i s a b o u t f i s h in g
e f fo r t . S e c t io n 9 .5 , 9 .6 , a n d 9 .8 d e s e r v e
th e ir o w n m a in s e c t io n , g iv e n th e
q u e s t i o n a n d th e a m o u n t o f d e ta il .
p .8 1 : i t w o u l d b e h e lp f u l to c la r ify th a t
th e d a ta p r e s e n t e d in F ig u r e s 9 -1 1 a n d
9 -1 2 a r e d e r iv e d f r o m T a b le s 9 -9 a n d 9 -
1 0 r e s p e c t iv e ly ; w h i l e in f o r m a t io n is
p r o v id e d o n t h e s t o c k in g p r o g r a m m e s
in e a c h c o u n tr y , i t w o u l d b e h e lp f u l to
p r o v id e a s u m m a r y th a t e x p la in s th e
o v e r a l l t r e n d s in t h e d a ta . A r e th e r e
d i f f e r e n c e s in th e r e g io n a l tr e n d s ? W h a t
c a u s e d t h e d e c l in e in g la s s e e l s to c k in g
f r o m a r o u n d 1 9 9 0 a n d th e in c r e a s e in
y e l l o w e e l s t o c k in g a r o u n d th e s a m e
t im e ? F ig u r e 9 -1 3 p r e s e n t s t h e r a t io o f
y e l l o w t o g la s s e e l s t o c k in g , b u t i s n o t
r e fe r r e d to in t h e te x t .
S e c t io n 9 .6 d e le t e d f r o m th e r e p o r t .
p . 1 0 2 , l i n e 6: A n a n n u a l m o r t a l i t y o f
0 .1 3 8 fo r g la s s e e l s s e e m s u n l ik e ly . If
th e tr u e m o r t a l i t y i s h ig h e r th a n th is ,
t h e n th e e s t im a t e o f t h e n u m b e r o f
' g l a s s e e l e q u iv a le n t s ' s t o c k e d w i l l b e
u n d e r e s t im a t e d .
p .1 0 6 - 1 0 7 , F ig u r e s 9 -1 3 & 9 -14 : T h e
c a p t io n s r e fe r to U n i t e d K in g d o m (G B );
N o r t h e r n I r e la n d i s p a r t o f U K b u t n o t
p a r t o f G B , s o e i th e r U K o r G B s h o u ld
b e r e fe r r e d to . N B : w i t h r e fe r e n c e to
o t h e r s e c t io n s , G B i s n o t a n E U M e m b e r
S ta te , U K is .
p .1 0 7 : S e c t io n 9 .7 d e a ls w i t h e f fo r t ,
w h i c h p o t e n t ia l ly p r o v id e s a m e a n s fo r
a s s e s s in g t r e n d s in e x p lo i t a t io n u s e d in
r u n - r e c o n s t r u c t io n a p p r o a c h , b u t n o
r e fe r e n c e is m a d e to t h e s e d a ta in
S e c t io n 7 .
p .1 0 9 : S e c t io n 9 .8 p r e s e n t s d a ta o n
a q u a c u l t u r e f r o m th r e e s o u r c e s , w h ic h
s h o w e s s e n t ia l l y th e s a m e tr e n d s . N o
e x p la n a t io n i s p r o v id e d fo r t h e d e c l in e
i n e e l a q u a c u l t u r e p r o d u c t io n , a l t h o u g h
t h is a p p e a r s s u r p r is in g a t a t im e w h e n
a v a i la b i l i t y o f w i ld c a u g h t e e l m u s t b e
d e c l in in g . I s th is b e c a u s e o f d i f f ic u l t ie s
o f o b t a in in g j u v e n i le e e l s fo r o n -
g r o w in g ?
Section 10, G lass eel land ings and
trade
S e c t io n s 1 0 .2 t o 1 0 .4 d e a l w i t h g la s s e e l
c a t c h e s a n d t r a d e , a n d t h u s c o v e r m u c h
N o t e ta k e n fo r f u t u r e r e p o r ts . T h e c h a n g e in g la s s e e l v e r s u s
y e l l o w e e l s t o c k in g is m a in ly d u e t o t h e in c r e a s e d u s e o f
la r g e r , p r e - g r o w n e e l s fo r r e s to c k in g .
F o r s o m e e a s t e m E u r o p e a n c o u n t r ie s i t i s n o t p o s s ib l e to
r e s t o c k w i t h g la s s e e l s in e a r ly s p r in g d u e t o ic e c o v e r .
I f M = 0 .1 3 8 i s th a t u n l ik e ly , th e n u m b e r s a r e u n d e r e s t im a t e d .
H o w e v e r , th e id e a b e h in d th e e q u iv a le n t s i s m a in ly t o m a k e
d if f e r e n t s t o c k in g m a t e r ia ls c o m p a r a b le a n d to s im p l i f y
fu r th e r c a lc u la t io n s . B e s id e s , t h e W G E E L m a d e a n e x t e n s iv e
r e v ie w o n n a tu r a l m o r t a l i t ie s in t h e 2 0 1 2 R e p o r t (C h a p te r 7 in
IC E S C M 2 0 1 2 /A C O M :1 8 )
IC E S v o c a b u la r y (IC E S R e fe r e n c e C o d e s
R E C O V o c a b u la r y v 2 .0 q ) U n i t e d K in g d o m i s a b b r e v ia t e d a s
G B (a n d N I r e la n d G B -N IR )
E ffo r t s e c t io n n o t u p d a t e d t h is y e a r
C a u s e o f n e g a t iv e tr e n d i s a c o m b in a t io n o f g la s s e e l
a v a i la b i l i t y a n d p r ie e s , a n d lo w e r m a r k e t d e m a n d .
C o m m e n t n o t e d f o r f u t u r e r e fe r e n c e .
192 | Joint EIFAAC/ICES/GFCM WCEEL REPORT 2014
o f th e s a m e g r o u n d a s S e c t io n s 9 .1 ,9 .5
a n d 9 .6 . S e c t io n s 1 0 .5 a n d 1 0 .7 a d d r e s s
s t o c k in g a n d a q u a c u l tu r e a n d th e r e fo r e
o v e r la p w i t h s u b s e c t io n s 9 .5 , 9 .6 a n d
9 .8 . O v e r a l l t h e s e s e c t io n s a re
c o n f u s in g , a n d i t w o u l d b e h e lp f u l to
id e n t i f y c le a r o b j e c t iv e s fo r c o l la t in g
t h e s e d a ta ; th e a n a ly s i s c o u ld t h e n b e
d ir e c t e d t o w a r d s a c h ie v in g t h o s e a im s .
T h e s e o b j e c t iv e s m ig h t b e t o ( r e l ia b ly )
q u a n t i fy t h e a n t h r o p o g e n ic l o s s e s to
s t o c k s f r o m f i s h in g a n d a d d i t io n s to
s t o c k s f r o m s t o c k in g , a n d a s s e s s l ik e ly
f u tu r e tr e n d s .
1 0 0 T h e r e i s a r e q u ir e m e n t u n d e r E M P s th a t
t h o s e M S s w i t h g la s s e e l f i s h e r ie s m u s t
s e t a s id e 60% fo r s t o c k in g , b u t th e r e is
n o r e q u ir e m e n t fo r M S s t o p u r c h a s e
t h e s e e e l s . S e c t io n 1 0 .8 c o n c lu d e s th a t
t h e s t o c k in g ta r g e t i s n o t b e in g a c h ie v e d
b y a l l M S s . W h y a r e t h e r e m a in in g
c o u n t r ie s n o t s t o c k in g a n d n o t r e a c h in g
t a r g e t s - fu n d in g ? Is t h e W o r k in g
G r o u p a b le to c o m m e n t o n w h e r e
t r a c e a b i l i ty i s w o r k in g a n d w h y d a ta
p r e s e n t e d in C o u n t r y R e p o r t s , E u r o S ta t ,
e tc . d if fe r ?
1 0 1 T h e in f o r m a t io n in S e c t io n 1 0 .2 to 1 0 .4
a p p e a r s t o b e r e le v a n t t o th e E U -C IT E S
C o m m it t e e in r e la t io n t o C IT E S
d i s c u s s i o n s o n th e l i s t i n g o f e e l , b u t i t is
n o t c le a r w h e t h e r t h e y a r e p r o v id e d fo r
o r u s e d b y th a t c o m m it t e e .
1 0 2 p .1 1 5 , f in a l p a ra ; i t i s s ta t e d , ‘E u r o S ta t
c a n w e l l d e sc r ib e g la s s eel e x p o r ts in
E u r o p e ’ d e s p i t e a n u m b e r o f c a v e a ts
b e in g h ig h l ig h t e d ; d o e s t h is c o m m e n t
a p p l y to th e r a w o r c o r r e c te d E u r o S ta t
d a ta ?
Section 11, Assessm ent o f qua lity o f
eel stocks
1 0 3 S e c t io n 1 1 .2 p r o v id e s a u s e f u l r e v ie w o f
r e c e n t l i t e r a tu r e o n c o n t a m in a n t s ,
d i s e a s e s a n d p a r a s i t e s o n t h e q u a l i t y o f
e m ig r a t in g e e ls . A n u p d a t e i s p r o v id e d
o n in c i d e n c e o f A n g u i l l ic o la c ra ssu s in
d i f f e r e n t c o u n t r ie s b u t m u c h o f th e
in f o r m a t io n i s n o t q u a n t i ta t iv e . S e c t io n
1 1 .3 p r o v id e s p r e l im in a r y r e s u lt s f r o m a
m o d e l e s t im a t in g th e r e p r o d u c t iv e
p o t e n t ia l o f s i lv e r e e l s w h e n t h e y r e a c h
th e S a r g a s s o S e a , d e p e n d i n g o n o r ig in ,
s iz e , s e x , a n d in it ia l fa t c o n te n t . W h ile
th e r e p o r t in d ic a t e s m a n y u n c e r ta in t ie s
in th e m o d e l , t h e r e s u lt s h ig h l ig h t s o m e
in t e r e s t in g a n d p o t e n t ia l ly im p o r ta n t
c o n s id e r a t io n s c o n c e m i n g th e
r e p r o d u c t iv e p o t e n t ia l o f e e l f r o m
_________ d if f e r e n t a r e a s ( p a r t ic u la r ly th e e f f e c t s
T h is w a s a d d r e s s e d in S e c t io n 1 0 .7 o f t h e 2 0 1 3 r e p o r t . T h e t im e
f r a m e fo r W G E E L m e e t i n g is in s u f f i c ie n t fo r a d e t a i l e d tr a d e
d a ta a n a ly s i s t o s c r u t in iz e p o s s ib l e s o u r c e s fo r d i f f e r e n c e s in
s o u r c e d a ta
S R G r e q u e s t IC E S a d v ic e a n d s ig h t o f th e d a ta a n d r e p o r t . T h is
w a s c o m p l i e d w it h .
C o r r e c te d E u r o s ta t d a ta .
C o m m e n t n o t e d fo r f u t u r e r e fe r e n c e .
Joint EIFAAC/ICES/CFCM WGEEL REPORT 2014 I 193
o f d is t a n c e to th e s p a w n in g a r e a s a n d
s i z e a t e m ig r a t io n ) .
T h e W o r k in g G r o u p m ig h t c o n s id e r
in c o r p o r a t in g u n c e r t a in t ie s in t o th e
m o d e l , t h u s a l l o w i n g a n a s s e s s m e n t , fo r
e x a m p le , o f t h e p r o p o r t io n o f e e l s th a t
h a v e a g r e a te r t h a n X % p r o b a b i l i t y o f
h a v in g a r e p r o d u c t iv e p o t e n t ia l > Y,
1 0 4 W h ile t h e c u r r e n t r e s u lt s a r e v e r y
in t e r e s t in g , i t i s p r e m a t u r e to s ta te , 'T h e
n e w f ig u r e s s h o w c o n s id e ra b le v a r ia t io n in
r e p r o d u c tio n p o te n t ia l b e tw e e n
c o u n tr ie s /c a tc h m e n ts . ' (S e c t io n 1 1 .6 ) , a n d
th e W o r k in g G r o u p s h o u l d b e m o r e
c a u t ío u s a b o u t th e ir c o n c lu s io n s .
1 0 5 M o r e w o r k i s r e q u ir e d o n s o m e o f th e
m o d e l in p u t s ( e .g . e n e r g y c o s t s o f
m ig r a t io n u n d e r o c e a n ic c o n d it io n s
( e f f e c t s o f c u r r e n ts a n d p r e s s u r e a t
d if f e r e n t d e p t h s ) , th e in f lu e n c e o f
s h o a l in g , e tc ) .
1 0 6 M o n i t o r in g e e l q u a l i t y i s a n e x p e n s iv e
u n d e r t a k i n g a n d a t th e m o m e n t n o
g u id a n c e i s a v a i la b le t o p r io r i t iz e w h a t
a s s e s s m e n t s s h o u l d b e c o n d u c t e d th a t
w i l l g iv e m e a n in g f u l in fo r m a t io n .
W h i le th is i s p o t e n t ia l ly im p o r ta n t
w o r k , it s h o u l d b e e v a lu a t e d a g a in s t
o t h e r d a t a d e f ic ie n c i e s a n d r e s e a r c h
n e e d s to e n s u r e th a t i t i s th e h ig h e s t
p r io r i t y a re a fo r im p r o v i n g th e
a s s e s s m e n t a n d m a n a g e m e n t o f e e l; a t
p r e s e n t c o l le c t in g a d e q u a t e in fo r m a t io n
o n c a tc h e s , b io lo g ic a l c h a r a c te r is t ic s ,
a n d a b u n d a n c e in d ic e s th a t c a n b e u s e d
t o d e l i v e r a s t o c k w i d e a s s e s s m e n t m u s t
b e a h ig h e r p r io r ity . A n y p r o g r e s s
m a d e o n i m p r o v i n g t h e k n o w le d g e
a b o u t th e e f f e c t s o f c o n t a m in a n t s w i l l b e
d if f ic u l t t o in c o r p o r a te in a s to c k w id e
a s s e s s m e n t th a t d o e s n ' t e x i s t .
Section 12, Local stock assessm ent
1 0 7 T h is s e c t io n m a k e s p r o p o s a l s fo r A g r e e d .
s t a n d a r d iz in g d a ta c o l le c t io n to s im p l i f y
a n d i m p r o v e p r o v i s io n o f r e p o r ts t o a
r a n g e o f c u s t o m e r s / f o r a . S u c h e f fo r t s
a r e to b e c o m m e n d e d , a l t h o u g h th e
W o r k in g G r o u p s h o u l d b e c a u t io u s
a b o u t s e e k in g e x c e s s i v e d e t a i l in th e
d a t a r e p o r t in g .
1 0 8 O t h e r in f o r m a t io n r e q u ir e m e n t s a r e t o T h is i s n o t a n a c t io n a b le r e c o m m e n d a t io n .
a d d r e s s c o m m it m e n t s o n m o n it o r in g
a c t iv i t i e s o r c o m m itm e n t s t o C IT E S a n d
i t i s n o t c le a r th a t t h e s e s h o u l d b e le d b y
S c ie n c e , i n c l u d in g IC E S .
C o m m e n t n o t e d . W e s t i l l b e l i e v e th e f ig u r e s s h o w v a r ia t io n a s
in d ic a t e d . T h e s h o r t c o m in g s o f th e m o d e l a n d u n c e r t a in t ie s
w it h r e s p e c t to th e d a ta , u s e d to e la b o r a t e th e f ig u r e s h a v e
b e e n d is c u s s e d .
F u l ly a g r e e d .
C o m m e n t n o te d .
194 | Joint ElFAAC/iCES/CFCM WGEEL REPORT 2014
109 T h e p r io r i t ie s fo r th e a s s e s s m e r t t a re
p r o b a b ly :
C a t c h -e f fo r t - c p u e (S e c 1 2 .2 )
S to c k ( n o t s to c k in g ) in d ic a to r
t a b le (S e c 1 2 .6 )
E s t im a te o f B o (S ec 1 2 .1 1 .2 )
B io lo g ic a l d a ta (S e c 1 2 .9 )
M a n a g e m e n t m e a s u r e s
o v e r v i e w ( fo r e s t im a t in g c h a n g e s in
e x p . r a te s ) (S e c 1 2 .8 )
M a n a g e m e n t m e a s u r e s d e t a i l s
( in c l u d in g e x p e c te d e f f e c t o n th e s to c k )
(S e c 1 2 .1 1 .3 )
O th e r d a t a ta b le s l i s t e d a r e u s e d fo r
r e s p o n d i n g t o o th e r c o m m itm e n t s
u n r e la t e d t o th e a s s e s s m e n t o f th e E U
E e l R e c o v e r y R e g u la t io n .
Sections 1 3 and 14, Forward focus
and Research needs
110 S e c t io n 1 3 p r o v id e s a b r ie f h is t o r y o f e e l
m a n a g e m e n t o v e r th e p a s t ~ 5 y e a r s a n d
a n e v a lu a t io n o f th e a s s e s s m e n t s
p r o v id e d in S e c t io n s 4 -8 . I t c o v e r s m u c h
o f th e s a m e g r o u n d a s S e c t io n 8 a n d
m ig h t s e n s i b l y b e c o m b in e d w i t h o r
r e p la c e th a t s e c t io n . S e c t io n 14
a d d r e s s e s d a ta d e f i d e n c i e s a n d r e s e a r c h
n e e d s id e n t i f i e d b y th e W o r k in g G r o u p ,
a l t h o u g h m o r e d e t a i l o n s o m e r e s e a r c h
a r e a s i s p r o v id e d in o t h e r s e c t io n s a n d
n o t a ll t h e p r o p o s a l s a r e fo r r e s e a r c h . It
w o u l d b e h e lp f u l t o h a v e a ll th e d a ta
d e f ic ie n c i e s a n d r e s e a r c h n e e d s
d e s c r ib e d in s im ila r d e t a i l in o n e
s e c t io n . T h is n e e d s t o b e a c c o m p a n ie d
b y a n e v a l u a t i o n o f th e p r io r it ie s f o r th e
v a r io u s p r o p o s a l s a n d a m o r e
s y s t e m a t ic e x a m in a t io n o f w h a t is
f e a s ib le . S u c h a n e x a m in a t io n w o u l d
a s s i s t in d e t e r m in in g w h i c h a n a ly s e s
s h o u l d b e p u r s u e d a n d w h i c h d r o p p e d .
A t p r e s e n t i t is d i f f ic u l t t o d e t e r m in e
w h e t h e r e e l q u a l i t y , fo r e x a m p le , is th e
m o s t p r e s s in g r e s e a r c h n e e d o r ju s t h a s
th e m o s t f e r v e n t a d v o c a t e .
111 I t w o u l d b e h e lp f u l i f f u t u r e T o R c le a r ly
r e f le c t e d (a ) th e s p e c i f i c a d v is o r y
r e q u ir e m e n t s ( e .g . r e p o r t o n th e s t a t u s
o f t h e E u r o p e a n e e l s t o c k b y r e g io n ) , (b )
m e t h o d o lo g ic a l d e v e l o p m e n t s t o m e e t
t h o s e a d v is o r y n e e d s ( r e p o r t o n th e
fu r th e r d e v e l o p m e n t a s t o c k -
r e c r u itm e n t r e la t io n s h ip fo r E u r o p e a n
e e l ) , (c ) o th e r i s s u e s r e q u ir in g a t t e n t io n
in o r d e r t o p r o v id e t h e a d v ic e (e .g .
r e s e a r c h a n d d a ta n e e d s ) (e .g . r e p o r t o n
th e d e v e l o p m e n t o f m e t h o d s to
__________ in c o r p o r a t e e e l q u a l i t y in c u r r e n t__________
A c t io n e d to s o m e e x t e n t in th is r e p o r t a n d n o t e d fo r fu tu r e
r e fe r e n c e a n d d e v e lo p m e n t .
A g r e e d . T im e c o n s tr a in t s p r e v e n t e d t h i s d u r in g t h e 2 0 1 4
m e e t i n g b u t i t i s n o t e d fo r 2 0 1 5 .
D o n e - t h e 2 0 1 4 T o R w e r e d e s ig n e d w i t h t h is r e c o m m e n d a t io n
in m in d , a n d r e c o m m e n d a t io n s fo r T o R fo r 2 0 1 5 a r e s im ila r ly
d e s ig n e d .
Joint EIFAAC/ICES/GFCM WGEEL REPORT 2014 I 195
112
113
a s s e s s m e n t s . )
I t is n o t c le a r w h e r e R e c o m m e n d a t io n 1
o r ig in a t e s f r o m in th e r e p o r t.
T h e f o l l o w i n g r e c o m m e n d a t io n s a re
m a d e in t h e r e p o r t b u t n o t in c lu d e d in
A n n e x 4:
p .1 3 2 : It i s r e c o m m e n d e d th a t a ll
c o u n t r ie s a d h e r e to th e c o n d i t io n s la id
o u t in th e E e l R e g u la t io n o f 2 0 0 9 a n d
e s t a b l i s h th e r e q u ir e d in t e r n a t ío n a l
t r a c e a b i l i ty s y s t e m in l in e w i t h A r t ic le
12.
p .1 5 4 : W G E E L 2 0 1 3 r e c o m m e n d e d th e
d e v e l o p m e n t o f s ta n d a r d iz e d a n d
h a r m o n iz e d p r o t o c o l s fo r th e e s t im a t io n
o f e e l q u a l i t y t h r o u g h th e o r g a n iz a t io n
o f a W o r k s h o p o f a P la n n in g G r o u p o n
th e M o n it o r in g o f E e l Q u a li t y ) .
p .1 5 5 , S e c 11 .8 : W e r e c o m m e n d th a t
m o n it o r in g o f s i lv e r e e l q u a l i t y s h o u ld
b e in t r o d u c e d a s p a r t o f n e w o r e x i s t in g
p r o g r a m m e s (D C F /D C M A P ) .
p .1 8 5 : It i s r e c o m m e n d e d th a t r e s e a r c h
t o in v e s t ig a t e fa c to r s th a t c a u s e N a tu r a l
M o r ta l i t y (M ) to v a r y in s p a c e a n d t im e
b e g iv e n th e h ig h p r io r ity . T h u s fu r th e r
d a t a c o l le c t io n a n d r e s e a r c h s h o u ld b e
e n c o u r a g e d to s u p p o r t a n d im p r o v e th e
k n o w le d g e o f t h is d i f f i c u l t r e se a r c h
t o p ic in o r d e r to o b t a in m o r e a n d m o r e
r e l ia b le s t o c k a s s e s s m e n t s .
It is n o t c le a r w h y s o m e ta b le s a r e in
th is A n n e x w h i l e o t h e r s a r e in th e tex t .
[N B Is th e r e a s t a n d a r d IC E S fo r m a t;
e .g . p la c i n g a ll t a b le s a n d f ig u r e s a t th e
e n d o f e a c h s e c t io n ? ]
R e c o m m e n d a t io n s a r e c o l la t e d in A n n e x 7.
M o s t t a b le s a r e n o w p la c e d a t th e e n d o f r e le v a n t c h a p te r s ,
w it h th e e x c e p t io n o f s o m e la r g e ta b le s th a t a r e p r o v id e d a s
a c c o m p a n y in g e l e c t r o n ic ta b le s .
196 I Joint EIFAAC/ICES/CFCM WCEEL REPORT 2014
Annex 9: Glossary
Eel life history
Eels are quite unlike other fish. Consequently, eel fisheries and eel biology come with
a specialized jargon. This section provides a quick introduction. It is by no means in-
tended to be exhaustive.
There are two species of eel in the North
Atlantic, the European eel (Anguilla anguilla)
and the American eel (A. rostrata).
The European eel Anguilla anguilla (L.) is
found and exploited in fresh, brackish and
coastal waters in almost all of Europe and
along the Mediterranean coasts of Africa and
Asia. The life cycle has not been fully eluci-
dated but current evidence supports the view
that recruiting eel to European continental
waters originate in a single spawning stock in
the Atlantic Ocean, presumably in the Sar-
gasso Sea area, where the smallest larvae have
been found. Larvae (Leptocephali) of progres-
sively larger size are found between the Sar-
gasso Sea and European continental shelf
waters. While approaching the continent, the
laterally flattened Leptocephalus transforms
into a rounded glass eel, which has the same
shape as an adult eel, but is unpigmented.
Glass eel migrate into coastal waters and estuaries mostly between October and
March/April, before migrating, as pigmented elvers, on into rivers and eventually into
lakes and streams between May and September. Following immigration into continen-
tal waters, the prolonged yellow eel stage (known as yellow eel) begins, which lasts for
up to 20 or more years. During this stage, the eels may occupy freshwater or inshore
marine and estuarine areas, where they grow, feeding on a wide range of insects,
worms, molluscs, crustaceans and fish. Sexual differentiation occurs when the eels are
partly grown, though the mechanism is not fully understood and probably depends
on local stock density. At the end of the continental growing period, the eels mature
and return from the coast to the Atlantic Ocean; this stage is known as the silver eel.
Female silver eels are twice as large and may be twice as old as males.
Glass eel
Leptocephalus
Eggs
Ocean
\
Eiver
Continent
Yellow eel
Spawning
Silvcr ecl
The life cycle of the European eel. The nam es of the m ajor
life stages are indicated; spawning and eggs have never been
observed in the w ild and are therefore only tentatively in-
cluded. (D ia g ra m : W il le m D e k k e r ) .
joint EIFAAC/ICES/GFCM WGEEL REPORT 2014 I 197
B o o t la c e , I n t e r m e d ia t e s iz e d e e ls , a p p r o x . 1 0 - 2 5 c m in le n g t h . T h e s e t e r m s a r e m o s t
f in g e r l in g o f t e n u s e d in r e la t io n to s to c k in g . T h e e x a c t s i z e o f th e e e l s m a y v a r y
c o n s id e r a b ly . T h u s , i t i s a c o n f u s i n g te r m .
E e l R iv e r B a s in " M e m b e r S ta te s s h a l l id e n t i f y a n d d e f in e t h e in d iv id u a l r iv e r b a s in s ly i n g
o r E e l w i t h in th e ir n a t io n a l te r r ito r y th a t c o n s t i t u t e n a tu r a l h a b i ta t s fo r t h e E u r o p e a n
M a n a g e m e n t e e l ( e e l r iv e r b a s in s ) w h ic h m a y in c l u d e m a r i t im e w a te r s . I f a p p r o p r ia t e
U n i t j u s t i f ic a t io n i s p r o v id e d , a M e m b e r S ta te m a y d e s ig n a t e th e w h o l e o f i t s
n a t io n a l t e r r ito r y o r a n e x i s t i n g r e g io n a l a d m in is t r a t iv e u n i t a s o n e e e l r iv e r
b a s in . In d e f in in g e e l r iv e r b a s in s , M e m b e r S ta te s s h a l l h a v e t h e m a x im u m
p o s s ib l e r e g a r d fo r t h e a d m in is t r a t iv e a r r a n g e m e n t s r e fe r r e d t o in A r t ic le 3 o f
D ir e c t iv e 2 0 0 0 /6 0 /E C [ i.e . R iv e r B a s in D is t r ic t s o f th e W a te r F r a m e w o r k
D ir e c t iv e ] ." E C N o . 1 1 0 0 /2 0 0 7 .
Y o u n g e e l , in i t s f ir s t y e a r f o l l o w i n g r e c r u it m e n t f r o m th e o c e a n . T h e e l v e r
s t a g e i s s o m e t im e s c o n s id e r e d to e x c lu d e th e g la s s e e l s t a g e , b u t n o t b y
e v e r y o n e . T o a v o id c o n f u s io n , p ig m e n t e d 0 + c o h o r t a g e e e l a r e in c l u d e d in th e
g la s s e e l te r m .
Y o u n g , u n p i g m e n t e d e e l , r e c r u it in g f r o m th e s e a in t o c o n t in e n t a l w a t e r s .
W G E E L c o n s id e r t h e g la s s e e l te r m to in c l u d e a l l r e c r u it s o f th e 0 + c o h o r t a g e .
T h e a r e a o f la n d a n d s e a , m a d e u p o f o n e o r m o r e n e ig h b o u r in g r iv e r b a s in s
t o g e t h e r w i t h t h e ir a s s o c ia t e d s u r fa c e a n d g r o u n d w a t e r s , t r a n s it io n a l a n d
c o a s t a l w a t e r s , w h i c h is id e n t i f i e d u n d e r A r t ic le 3 (1 ) o f th e W a te r F r a m e w o r k
D ir e c t iv e a s th e m a in u n i t fo r m a n a g e m e n t o f r iv e r b a s in s . T h e te r m i s u s e d in
r e la t io n to th e E U W a te r F r a m e w o r k D ir e c t iv e .
M ig r a to r y p h a s e f o l l o w i n g th e y e l l o w e e l p h a s e . E e l in th is p h a s e a r e
c h a r a c te r iz e d b y d a r k e n e d b a c k , s i lv e r y b e l ly w i t h a c le a r ly c o n tr a s t in g b la c k
la te r a l l in e , e n la r g e d e y e s . S i lv e r e e l u n d e r t a k e d o w n s t r e a m m ig r a t io n
t o w a r d s t h e s e a , a n d s u b s e q u e n t ly w e s t w a r d s . T h is p h a s e m a in ly o c c u r s in
th e s e c o n d h a l f o f c a le n d a r y e a r s , a l t h o u g h s o m e a r e o b s e r v e d t h r o u g h o u t
w in t e r a n d f o l l o w i n g s p r in g .
S to c k in g ( fo r m e r ly c a l le d r e s to c k in g ) i s t h e p r a c t ic e o f a d d i n g f i s h [ e e ls ] to a
w a t e r b o d y f r o m a n o th e r s o u r c e , to s u p p le m e n t e x i s t i n g p o p u l a t io n s o r to
c r e a te a p o p u l a t io n w h e r e n o n e e x is t s .
S i lv e r in g i s a r e q u ir e m e n t fo r d o w n s t r e a m m ig r a t io n a n d r e p r o d u c t io n . It
m a r k s th e e n d o f t h e g r o w t h p h a s e a n d th e o n s e t o f s e x u a l m a t u r a t io n . T h is
tr u e m e t a m o r p h o s i s i n v o l v e s a n u m b e r o f d i f f e r e n t p h y s i o lo g ic a l f u n c t io n s
( o s m o r e g u la t o r y , r e p r o d u c t iv e ) , w h i c h p r e p a r e th e e e l fo r t h e l o n g r e tu r n tr ip
t o t h e S a r g a s s o S e a . U n l ik e s m o lt i f i c a t io n in s a lm o n id s , s i lv e r in g o f e e l s i s
la r g e ly u n p r e d ic ta b le . I t o c c u r s a t v a r io u s a g e s ( f e m a le s : 4 - 2 0 y e a r s ; m a le s 2 -
1 5 y e a r s ) a n d s i z e s ( b o d y le n g t h o f f e m a le s : 5 0 - 1 0 0 cm ; m a le s : 3 5 - 4 6 c m )
(T e s c h , 2 0 0 3 ) .
Y e l l o w e e l L if e - s ta g e r e s id e n t in c o n t in e n t a l w a t e r s . O f t e n d e f in e d a s a s e d e n t a r y p h a s e ,
(B r o w n e e l ) b u t m ig r a t io n w i t h in a n d b e t w e e n r iv e r s , a n d t o a n d f r o m c o a s ta l w a t e r s
o c c u r s a n d th e r e fo r e in c lu d e s y o u n g p ig m e n t e d e e l s ( 'e lv e r s ' a n d b o o t la c e ) .
E lv e r
G la s s e e l
R iv e r B a s in
D is t r ic t
S i lv e r e e l
S to c k in g
T o s i lv e r
( s i lv e r in g )
198 | Jo in t EIFAAC/ICES/GFCM WCEEL REPORT 2014
Eel reference po in ts/popu la tion dynam ics
C u r e n t
e s c a p e m e n t
b io m a s s ( B cu rren t)
B e s t a c h ie v a b le
b io m a s s (B b c s t)
P r is t in e b io m a s s
(Bo)
BMSY-triggcr
B s to p
T h e a m o u n t o f s i lv e r e e l b io m a s s th a t c u r r e n t lv e s c a p e s t o t h e s e a t o s p a w n ,
c o r r e s s p o n d in g to th e a s s e s s m e n t y e a r .
S p a w n in g b io m a s s c o r r e s p o n d in g to r e c e n t n a tu r a l r e c r u it m e n t t h a t w o u l d
h a v e s u r v iv e d i f th e r e w a s o n ly n a t u r a l m o r t a l i t y a n d n o s to c k in g ,
c o r r e s s p o n d in g t o th e a s s e s s m e n t y e a r .
S p a w n e r e s c a p e m e n t b io m a s s in a b s e n c e o f a n y a n t h r o p o g e n ic im p a c t s .
L im it
a n t h r o p o g e n ic
m o r t a l i t y (Ai™)
L im it s p a w n e r
e s c a p e m e n t
b io m a s s ( B n m )
P r e c a u t io n a r y
a n t h r o p o g e n ic
m o r t a l i t y (Apa)
P r e c a u t io n a r y
s p a w n e r
e s c a p e m e n t
b io m a s s (B Pa)
R target
S p a w n e r p e r
r e c r u itm e n t (S P R )
% SP R
E F
E H
£ A
" 3 B s & A "
V a lu e o f s p a w n in g - s t o c k b io m a s s (S S B ) w h i c h t r ig g e r s a s p e c i f i c
m a n a g e m e n t a c t io n , in p a r tic u la r : t r ig g e r in g a lo w e r l im it fo r m o r t a l i t y to
a c h ie v e r e c o v e r y o f th e s to c k .
B io m a s s o f th e s p a w n in g s to c k , a t w h i c h r e c r u it m e n t i s s e v e r e ly im p a ir e d ,
a n d th e n e x t g e n e r a t io n is ( o n a v e r a g e ) e x p e c t e d t o p r o d u c e a n e q u a l ly l o w
s p a w n in g - s t o c k b io m a s s a s th e c u r r e n t.
B io m a s s o f th e s p a w n in g s to c k a t w h i c h r e c r u it m e n t i s s e v e r e ly im p a ir e d ,
a n d th e n e x t g e n e r a t io n h a s a 5% c h a n c e to p r o d u c e a n e q u a l ly l o w
s p a w n in g - s t o c k b io m a s s a s th e c u r r e n t.
A n t h r o p o g e n ic m o r t a l it y , a b o v e w h í c h th e c a p a c i t y o f s e l f - r e n e w a l o f th e
s to c k i s c o n s id e r e d to b e e n d a n g e r e d a n d c o n s e r v a t io n m e a s u r e s a r e
r e q u e s t e d (C a d im a , 2 0 0 3 ) .
S p a w n e r e s c a p e m e n t b io m a s s , b e l o w w h i c h th e c a p a c i t y o f s e l f - r e n e w a l o f
th e s to c k i s c o n s id e r e d to b e e n d a n g e r e d a n d c o n s e r v a t io n m e a s u r e s a r e
r e q u e s t e d (C a d im a , 2 0 0 3 ) .
A n t h r o p o g e n ic m o r ta l i t y , a b o v e w h i c h th e c a p a c i t y o f s e l f - r e n e w a l o f th e
s to c k i s c o n s id e r e d to b e e n d a n g e r e d , t a k in g in t o c o n s id e r a t io n th e
u n c e r ta in ty in th e e s t im a t e o f th e c u r r e n t s t o c k s ta tu s .
T h e s p a w n e r e s c a p e m e n t b io m a s s , b e l o w w h i c h t h e c a p a c i t y o f s e l f - r e n e w a l
o f th e s t o c k i s c o n s id e r e d t o b e e n d a n g e r e d , t a k in g in t o c o n s id e r a t io n th e
u n c e r ta in ty in th e e s t im a t e o f th e c u r r e n t s t o c k s ta tu s .
T h e G e o m e tr ic M e a n o f o b s e r v e d r e c r u it m e n t b e t w e e n 1 9 6 0 a n d 1 9 7 9 ,
p e r io d s in w h i c h th e s to c k w a s c o n s id e r e d h e a lt h y .
E s t im a te o f s p a w n e r p r o d u c t io n p e r r e c r u it in g in d iv id u a l .
R a t io o f S P R a s c u r r e n t ly o b s e r v e d to S P R o f th e p r is t in e s to c k , e x p r e s s e d in
p e r c e n ta g e . % S P R i s a ls o k n o w n a s S p a w n e r P o t e n t ia l R a t io .
T h e f i s h in g m o r t a l i t y r a te . s u m m e d o v e r th e a g e - g r o u p s in t h e s to c k .
T h e a n t h r o p o g e n ic m o r t a l i t y r a te o u t s i d e t h e f is h e r y , s u m m e d o v e r t h e a g e -
g r o u p s in t h e s to c k .
T h e s u m o f a n t h r o p o g e n ic m o r ta l it ie s , i .e . Z A = E F + E H .
R e fe r s t o t h e 3 b io m a s s in d ic a t o r s (Bo, Bbest a n d B cm -rent) a n d a n t h r o p o g e n ic
m o r t a l i t y r a te (E A ).
Defmition
40% EU Target: "The objective of each Eel Management Plan shall be to reduce anthro-
pogenic mortalities so as to permit with high probability the escapement to the sea of
at least 40% of the silver eel biomass relative to the best estimate of escapement that
would have existed if no anthropogenic influences had impacted the stock". The
WGEEL takes the EU target to be equivalent to a reference limit, rather than a target.
Acronyms
Joint EIFAAC/ICES/CFCM WGEEL REPORT 2014 1 199
A c r o n y m s D e f in it io n
A C E A d v i s o r y C o m m it t e e o n th e E n v ir o n m e n t
A C F M (IC E S ) A d v i s o r y C o m m it t e e o n F is h e r ie s M a n a g m e n t
A C O M (IC E S ) A d v i s o r y C o m m it t e e o n M a n a g e m e n t
A F N N a t io n a l F o r e s tr y A u th o r i ty
A IC A k a ik e I n fo r m a tio n C r ite r io n
A N C O V A A n a l y s i s o£ C o v a r ia n c e
A N O V A A n a l y s i s o£ V a r ia n c e
B E R T B a y e s ia n E e l R e c r u i tm e n t T r e n d m o d e l
B IC B a y e s ia n In fo r m a tio n C r ite r io n
B IO R I n s t i t u te o f F o o d S a fe ty , A n im a l H e a l t h a n d E n v ir o n m e n t " B IO R " , L a tv ia
C C M C a t c h m e n t C h a r a c te r is a t io n a n d M o d e l l in g
C IT E S C o n v e n t io n o n I n te r n a t io n a l T r a d e in E n d a n g e r e d S p e c ie s
C N T S C e n tr e N a t io n a l d e T r a it e m e n t S ta t is t iq u e s , F r a n c e ( e x C R T S )
C O M M E U C o m m is s io n
C P U E C a tc h p e r u n i t o f e f fo r t
C R C o u n t r y R e p o r t
C U S U M C u m u la t iv e S u m C o n tr o l C h a r t
D B E E L D a t a b a s e o n E e l (E U P O S E p r o je c t)
D C A L D e p a r t m e n t o f C u ltu r e , A r ts & L e is u r e , N . I r e la n d
D C F D a ta C o l le c t io n F r a m e w o r k
D F O D e p a r t m e n t o f F i s h e r ie s a n d O c e a n s
D G -M A R E D ir e c to r a t e -G e n e r a l fo r M a r it im e A f fa ir s a n d F is h e r ie s , E U C o m m is s io n
D G P A G e n e r a l D ir e c to r a te o f F is h e r ie s a n d A q u a c u lt u r e , P o r tu g a l
D L S D a ta -L im it e d S to c k s
D P M A D ir e c t io n d e s F S ch es M a r it im e s e t d e T A q u a c u ltu r e , F r a n c e
E IF A A C E u r o p e a n I n la n d F is h e r ie s & A q u a c u lt u r e A d v i s o r y C o m m is s io n
E M P E el M a n a g m e n t P la n
E M U E e l M a n a g e m e n t U n i t
EFF E u r o p e a n F is h e r ie s F u n d
F A O F o o d a n d A g r ic u l t u r e O r g a n is a t io n
F E A P T h e F e d e r a t io n o f E u r o p e a n A q u a c u lt u r e P r o d u c e r s
F G F R I F in n is h G a m e a n d F is h e r ie s R e s e a r c h I n s t itu t e
G A M G e n e r a l i s e d A d d i t i v e M o d e l
G E M G e r m a n E e l M o d e l
G F C M G e n e r a l F is h e r ie s C o m m is s io n o f th e M e d i t e r r a n e a n
G IS G e o g r a p h ic I n f o r m a t io n S y s t e m s
G L M G e n e r a l i s e d L in e a r M o d e l
G lo b A n g F r e n c h M o d e l o f E e l P o p u la t io n D y n a m ic s
H P S H y d r o p o w e r S ta t io n
IC E S I n te r n a t io n a l C o u n c í l fo r th e E x p lo r a t io n o f t h e S e a
L H T L ife H i s t o r y T ra it
L 5 0 L 5 0 = th e le n g t h (L) a t w h i c h h a lf (50% ) o f a f i s h s p e c ie s m a y b e a b le t o s p a w n
L V P A L e n g t h - b a s e d V ir tu a l P o p u la t io n A s s e s s m e n t
2 0 0 | joint EIFAAC/ICES/CFCM WGEEL REPORT 2014
A c r o n y m s D e f in it io n
M IW A M a r in e a n d I n la n d W a te r s A d m in i s t r a t io n
M S M e m b e r S ta te
M S Y M a x im u m S u s ta in a b le Y ie ld
N A O N o r t h A t la n t ic O s c i l la t io n
O N E M A O f f ic e N a t io n a l d e l'E a u e t d e s M i l ie u x A q u a t iq u e s , F r a n c e (e x -C S P )
P O S E P i lo t p r o je c t s to e s t im a t e p o t e n t ia l a n d a c tu a l e s c a p e m e n t o f s i lv e r e e l
R B D R iv e r B a s in D is tr ic t
R G E E L R e v ie w G r o u p o n E e l (IC E S )
S G IP E E S t u d y G r o u p o n I n te r n a t io n a l P o s t - E v a lu a t io n o n E e ls
S L IM E R e s t o r a t io n th e E u r o p e a n E e l p o p u ia t io n ; p i lo t s t u d ie s f o r a s c ie n t i f ic
f r a m e w o r k in s u p p o r t o t s u s t a in a b le m a n a g e m e n t
S M E P II S c e n a r io -b a s e d M o d e l to r E e l P o p u la t io n s , v l l
S N P E S u iv i n a t io n a l d e la p e c h e a u x e n g in s e t a u x f i l e t s
S P R E s t im a t e o f s p a w n e r p r o d u c t io n p e r r e c r u it in g in d iv id u a l .
S Q L S p e c ia l p u r p o s e p r o g r a m m in g la n g u a g e fo r m a n a g in g d a ta
SSB S p a w n in g - S t o c k B io m a s s
S T E C F S c ie n t i f ic , T e c h n ic a l a n d E c o n o m ic C o m m it t e e fo r F is h e r ie s , E U C o m m is s t o n
S W A M S w e d i s h A n a ly t ic a l M o d e l s
T o R T e r m s o f R e fe r e n c e
V P A V ir tu a l P o p u la t io n A n a ly s i s
W G W o r k in g G r o u p
W G E E L J o in t E I F A A C /IC E S /G F C M W o r k in g G r o u p o n E e l
W K E P E M P T h e W o r k s h o p o n E v a lu a t in g P r o g r e s s w i t h E e l M a n a g e m e n t P la n s
W K E S D C F W o r k s h o p o n E e ls a n d S a lm o n in t h e D a ta C o l le c t io n F r a m e w o r k
W F D W a te r F r a m e w o r k D ir e c t iv e
W K L IF E W o r k s h o p o n th e D e v e l o p m e n t o f A s s e s s m e n t s b a s e d o n L I F E -h is to r y tr a its
a n d E x p lo i ta t io n C h a r a c te r is t ic s
W K P G M E Q W o r k s h o p o f a P la n n in g G r o u p o n t h e M o n it o r in g o f E e l Q u a l i t y u n d e r th e
s u b je c t " D e v e lo p m e n t o f s t a n d a r d iz e d a n d h a r m o n iz e d p r o t o c o ls f o r th e
e s t im a t io n o f e e l q u a lity "
W G R F S W o r k in g G r o u p o n R e c r e a t io n a l F is h e r ie s S u r v e y s
Y F S l Y o u n g F is h S u r v e y : N o r t h S e a S u r v e y lo c a t io n
Joint EIFAAC/ICES/CFCM WGEEL REPORT 2014 ii
Annex 10: Country Reports 2 0 1 3 -2 0 1 4 : Eel stock, fisheries and hab i-
ta t reported by country
In preparatíon for the Working Group, partícipants of each country have prepared a
Country Report, in which the most recent information on eel stock and fishery are pre-
sented. These Country Reports aim at presenting the best information which does not
necessarily coincide with the official status.
Participants from the following countries provided an updated report to the 2014 meet-
ing of the Working Group on Eels:
• Belgium
• Denmark
• Estonia
• Finland
• France
• Germany
• Greece
• Ireland
• Italy
• Latvia
• Lithuania
• Montenegro
• Netherlands
• Norway
• Poland
• Portugal
• Spain
• The United Kingdom of Great Britain and Northern Ireland
For practical reasons, this report presents the Country Reports in electronic format only
(URL).
Countrv Reports 2013/2014.