Estuarine, Coastal and Shelf Science 67 (2006) 569e578
www.elsevier.com/locate/ecss
Habitat use by the European eel Anguilla anguilla in Irish waters
T. Arai a,*, A. Kotake b, T.K. McCarthy c
a
International Coastal Research Center, Ocean Research Institute, The University of Tokyo, 2-106-1, Akahama, Otsuchi, Iwate 028-1102, Japan
b
Ocean Research Institute, The University of Tokyo, Nakano, Tokyo 164-8639, Japan
c
Department of Zoology, National University of Ireland, Galway, University Road, Galway, Ireland
Received 17 October 2005; accepted 3 January 2006
Available online 17 February 2006
Abstract
The apparent use of marine and freshwater habitats by European eel Anguilla anguilla was examined by analyzing the strontium (Sr) and
calcium (Ca) concentrations in otoliths of the eels collected from Irish coastal and fresh waters. The age and growth of eels were also examined
using their otolith annuli. The sizes and ages of the female eels were greater than those of the males. The somatic growth rates ranged from 15 to
62 mm/year, which is typical for Ireland and other European countries. Analyses of Sr:Ca ratios along a life history transect in each otolith
showed peaks (maximum more than 25 103) between the core and elver mark corresponding to the period of their leptocephalus and early
glass eel stages in the ocean. Outside the elver mark, the Sr:Ca ratios indicated that eels had remained in different habitats that included freshwater (average Sr:Ca ratios, 0.98e1.78 103) and areas with relatively high salinities (average Sr:Ca ratios, 6.73e8.89 103). Some individuals showed clear evidence of shifts from sea to fresh waters. These findings suggest that Irish eels have the same behavioral plasticity
regarding whether or not to enter freshwater or remain in marine environments as has been recently documented in this species and several other
temperate anguillid species. However, patterns of habitat use in Irish waters were somewhat different than those previously reported for other
habitats.
Ó 2006 Elsevier Ltd. All rights reserved.
Keywords: Anguilla anguilla; age; growth; otolith microchemistry; habitat use; migration
1. Introduction
The life cycle of the European freshwater eel Anguilla
anguilla Linnaeus, 1758 has five principal stages: the leptocephalus, glass eel, elver, yellow eel and silver eel stages
(Bertin, 1956). The spawning area of A. anguilla is in the Sargasso Sea (Schmidt, 1922, 1925). The larvae, leptocephali,
drift on the Gulf Stream and are further transported by the
North Atlantic Current across the Atlantic Ocean (Schmidt,
1922, 1925; Boëtius, 1985). The leptocephali presumably
leave oceanic currents after metamorphosing into glass eels
and then typically migrate upstream as elvers, 6e8 months
after hatching (Arai et al., 2000), to grow in the freshwater
* Corresponding author.
E-mail address: arai@wakame.ori.u-tokyo.ac.jp (T. Arai).
0272-7714/$ - see front matter Ó 2006 Elsevier Ltd. All rights reserved.
doi:10.1016/j.ecss.2006.01.001
habitats of Europe and North Africa during the yellow stage.
At ages that vary widely among individuals of both sexes,
but especially for the larger older females, the yellow eels
metamorphose into silver eels, which migrate downstream to
the ocean to begin their journey to their spawning areas in
the Sargasso Sea (Tesch, 2003).
Recently, the migratory history of several species of
anguillid eels have been studied using microchemical techniques that determine the ratios of strontium to calcium
(Sr:Ca ratio) in their otoliths. The Sr:Ca ratio in the otoliths
of fishes differs according to the time they spend in freshwater
and seawater; this has also been found to be true for anguillid
eels (Tsukamoto et al., 1998; Tzeng et al., 2000; Tsukamoto
and Arai, 2001; Jessop et al., 2002; Arai et al., 2003a,b,
2004; Kotake et al., 2003, 2005). Early studies on the strontium incorporation into eel otoliths of Anguilla japonica
showed that the Sr:Ca level in their otolith strongly correlated
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T. Arai et al. / Estuarine, Coastal and Shelf Science 67 (2006) 569e578
with the salinity of the water and little affected by other factors
such as water temperature, food and physiological factors
(Kawakami et al., 1998). Thus, the Sr:Ca ratios of otoliths
could help in determining whether or not individual eels actually enter freshwater at the elver stage and remain in freshwater, estuarine or marine environments until the silver eel stage,
or whether they move between different habitats with differing
salinity regimes.
Otolith microchemistry studies have revealed that some
yellow and silver eels of temperate Anguilla anguilla and
Anguilla japonica never migrate into freshwater, but spend
their entire life history in the ocean (Tsukamoto et al.,
1998). Application of otolith Sr:Ca ratios to trace the migratory history of eels has also revealed otolith signatures intermediate to those of marine and freshwater residents of
A. anguilla (Tzeng et al., 2000), A. japonica (Tsukamoto
and Arai, 2001; Arai et al., 2003a,b; Kotake et al., 2003,
2005), Anguilla rostrata (Jessop et al., 2002), Anguilla
australis, and Anguilla dieffenbachii (Arai et al., 2004), all
of which appeared to reflect estuarine residence, or showed
clear evidence of switching between different salinity environments. It thus appears that a proportion of eels move frequently between different environments during their growth
phase. Therefore, because individuals of several anguillid species have been found to remain in estuarine or marine habitats,
it appears that anguillid eels do not all enter into freshwater
environments and that these species display more a facultative
catadromy (Tsukamoto and Arai, 2001).
Although Sr:Ca ratios have been studied in the otoliths of
yellow and silver eels of the five species of temperate
anguillid eels, there have been only several studies of this
nature on these species including Anguilla anguilla. Therefore,
it is not known if all populations display the same utilization of
both estuarine and marine environments in addition to the typical freshwater environments in A. anguilla. To begin to address
this question, we analyzed the Sr:Ca ratios in the otoliths of
yellow and silver eels of A. anguilla that were caught in
a bay and several rivers on the western side of Ireland.
The objective of this study was to use Sr:Ca ratios to reconstruct the environmental history of the European eel Anguilla
anguilla captured in Irish waters, and thereby to determine the
salinity environments that each individual had experienced
and to compare these data with the age and growth of each
eel. This approach enables a greater understanding of the
biological characteristics and apparent habitat use of the
species.
Derrevaragh (upper part of the River Shannon system) were
influenced by tides and their salinity was 0. All eels were captured commercially by silver eel fishing except for the Castleconnell site in River Shannon. At the sampling site in Galway
Bay, which has fully saline waters, eels were collected by
hand under intertidal stones and seaweeds.
After measurement of total length (TL, to 1 mm), body
weight (BW, to 1 g) and eye diameter (to 0.01 mm), the sex
of each eel >300 mm long was determined by visual observation of the gonads according to Tesch (2003), i.e. eels having
thin, regularly lobed organs were males, while individuals
having more broad and folded curtain-like gonads were
females. An eye index appears to be one of the best indicators
of the onset of reproductive maturation in silver eels of this
species (Pankhurst, 1982). We classified eels with an eye index
less than 6.5 as sexually immature adults (yellow eel), and
those over 6.5 as sexually mature adults (silver eels) (Table 2).
The eye index was calculated according to Pankhurst (1982)
as follows:
2. Materials and methods
2.3. Age estimation and data analyses
2.1. Fish
Following the microchemistry analyses, the otoliths were
repolished to remove the coating. Otoliths were then etched
with 1% HCl for 60 s, stained with 1% toluidine blue and
aged by counting the number of blue-stained transparent
zones, as reported in Arai et al. (2003a,b, 2004). The ages
given in this study are up to the last annuli and do not
include any additional age of less than one year. The mean
positions of the transparent zones for all eels were calculated
A total of 75 specimens of Anguilla anguilla were sampled,
using coghill nets, by electronic fishing and by hand capture
in one bay and six sites of four river systems in Ireland in
November 2003 (Fig. 1, Table 1). None of the sampling sites
in the river systems, River Garavogue, River Moy, River Corrib,
River Shannon (Killaloe, Castleconnell) and Lough
2
Eye index ¼ ½ðA þ BÞ=4 p=TL 100
where A is the horizontal eye diameter (mm) and B is the
vertical eye diameter (mm).
2.2. Otolith preparation and microchemical analysis
Sagittal otoliths were extracted from each fish, embedded
in epoxy resin (Struers, Epofix) and mounted on glass slides.
The otoliths were ground and polished, as described by Arai
et al. (2004), cleaned in an ultrasonic bath, and rinsed with
deionized water prior to being examined.
For electron microprobe analyses, all otoliths were PtePd
coated by a high vacuum evaporator. All otoliths were used
for ‘‘life history transect’’ analysis of Sr and Ca concentrations,
which were measured along the longest axis of each otolith
from the core to the edge using a wavelength dispersive
X-ray electron microprobe (JEOL JXA-8900R), as described
in Arai et al. (1997, 2004). Wollastonite (CaSiO3) and Tausonite (SrTiO3) were used as standards. The accelerating voltage
and beam current were 15 kV and 1.2 108 A, respectively.
The electron beam was focused on a point 10 mm in diameter,
with measurements spaced at 10 mm intervals. The detection
limits of Ca and Sr were 88.7 and 196.5 mg/g, respectively,
and their standard deviations (SD) were in the range of
0.14e0.26% and 0.22e0.24%, respectively.
T. Arai et al. / Estuarine, Coastal and Shelf Science 67 (2006) 569e578
571
Fig. 1. Map showing the collection sites (numbered) of the European eel Anguilla anguilla in Irish waters. There are shown only rivers studied in the present study.
Numbers adjacent to symbols indicate fished sites.
and correlated to elemental analysis points. The relative ages
at particular elemental analysis points could then be
assigned.
The growth rate for each individual was calculated by
dividing the TL of individuals minus 70 mm, which is
the mean sizes of the glass eel when they recruit to coasts
(Svedang et al., 1996) following the formula: growth
rate ¼ (TL 70)/Age.
2.4. Statistical analyses
Differences among data were tested first by analysis of variance (ANOVA) and then with Scheffe’s multiple range tests
for pairwise comparisons. The significance of the correlation
coefficient and regression slope were tested by Fisher’s
Z-transformation and an analysis of covariance (ANCOVA)
(Sokal and Rohlf, 1995).
3. Results
3.1. Biological characteristics
The eye index of Anguilla anguilla collected from seven
sites ranged from 2.7 to 10.8 (Table 2). Sex in all eels collected
from Galway Bay could not be differentiated, and thus these
eels were identified as yellow eels (Table 2). Based on the result and the Pankhurst criteria (1982), there were in total 37
yellow and 37 silver eels (Table 2), and one female from River
Garavogue that could not be identified as either yellow or silver stage (Table 2).
Total lengths of Anguilla anguilla collected from seven
sites ranged from 129 to 805 mm (Table 1). The total lengths
of the yellow eels ranged from 326 to 407 mm with
a mean SD of 360 42.0 mm for males; for females, they
ranged from 477 to 725 mm with a mean of 614 68.8 mm.
The total lengths of the silver eels ranged from 334 to
e
27.7e49.5
22
36.7 6.6
e
11e20
16
17 3.3
e
358e651
118
520 106.0
e
585e800
420
662 64.6
Male
Female
7. Lough Derrevaragh
1
10
15.4e29.6
25.0 5.1
7e12
10 2.0
28e73
276e357
Not determined
6. River Shannon, Castleconnell
10
319 27.8
53 15.9
19.9e28.8
30.1e54.9
23.9 4.3
40.7 12.0
11e16
9e18
13 2.2
15 3.7
356e388
323e955
356e388
564e805
Male
Female
5. River Shannon, Killaloe
5
5
379 13.1
648 95.4
379 13.1
536 248.6
42.0 13.3
2e6
4 1.4
2e39
129e299
Undifferentiated
4. Galway Bay
10
212 59.5
16 12.7
21.6e46.2
26.4e38.7
28.5 10.0
31.2 4.6
347e407
534e740
Male
Female
3. River Corrib, Galway
5
9
379 29.2
613 71.5
87 15.6
423 159.6
68e103
257e685
12 3.6
18 3.7
6e15
12e23
14.5e36.3
22.5e40.9
28.0 8.3
31.0 6.6
8e19
14e17
11 4.7
15 1.5
67e127
178e447
326e360
453e643
Male
Female
2. River Moy, Mayo
5
5
342 12.9
542 83.2
82 25.1
288 132.8
Range
17.2e21.9
16.9e27.9
19.2 2.3
23.3 4.0
Mean SD
Range
13e18
13e24
16 1.9
19 3.9
Mean SD
Range
64e154
100e532
88 37.8
299 146.2
Mean SD
Range
345e430
344e655
Mean SD
371 34.6
519 107.2
Male
Female
1. River Garavogue, Sligo
5
5
Growth rate
(mm/year)
Age
(years)
Body weight
(g)
Total length
(mm)
No. of fish
examined
Sex
Sampling location
Table 1
Biological characteristics of 75 specimens used for otolith microchemistry analyses. Numbers for each sampling location correspond to Fig. 1
19.7e62.0
T. Arai et al. / Estuarine, Coastal and Shelf Science 67 (2006) 569e578
572
430 mm with a mean SD of 372 27.4 mm for males; for
females, they ranged from 344 to 805 mm with a mean of
604 127.7 mm. There were significant differences in the total lengths between the sexes for both yellow and silver eels
(ANOVA, df ¼ 17e35, p < 0.0005e0.0001). However, no significant differences occurred in the total lengths between yellow and silver eels in either sex (ANOVA, df ¼ 20e32,
p > 0.5).
The body weights of Anguilla anguilla collected from seven
sites ranged from 2 to 955 g (Table 1). The body weights of
the yellow eels ranged from 68 to 98 g with a mean of
79 16.3 g for males; for females, they ranged from 182 to
651 g with a mean of 429 152.6 g. The body weights of
the silver eels ranged from 64 to 154 g with a mean of
90 24.6 g for males; for females, they ranged from 100 to
955 g with a mean of 431 223.0 g. There were significant
differences in the body weights between the sexes for both yellow and silver eels (ANOVA, df ¼ 17e35, p < 0.01e0.0001),
but not between yellow and silver eels in each sex (ANOVA,
df ¼ 20e32, p > 0.5). Close linear relationships appeared
between total length and body weight for each sex in either
yellow or silver eels (ANCOVA, df ¼ 29e35, p < 0.0005e
0.0001), except for yellow eel males due to the limited number
of specimens (three specimens) (Fig. 2).
The ages of Anguilla anguilla collected from seven sites
based on the number of annual rings in their otoliths ranged
from 2 to 24 years (Table 1). The ages of A. anguilla yellow
eels ranged from 6 to 13 years with a mean SD of
9.0 3.6 years for males; for females, they ranged from 11
to 22, with a mean of 17 3.5 years. The ages of the silver
eels ranged from 8 to 19 years with a mean SD of
14 3.1 years for males; for females, they ranged from 9 to
24 years with a mean of 17 3.8 years. The ages of the males
of both yellow eels and silver eels were significantly less
(ANOVA, df ¼ 17e35, p < 0.05) on average than those of females. However, no significant differences occurred in the
ages between yellow and silver eels in either sex (ANOVA,
df ¼ 20e32, p > 0.5). A close linear relationship occurred between age and total length in female yellow eels (ANCOVA,
df ¼ 29, p < 0.05), while no linear relationship existed in
male yellow eels or in silver eels of either sex (ANCOVA,
df ¼ 5e35, p > 0.05) (Fig. 3). There was also a close significant linear relationship between age and body weight in
male silver eels (ANCOVA, df ¼ 35, p < 0.05), while no linear
relationship existed in yellow eels of either sex or in female
silver eels (ANCOVA, df ¼ 5e35, p > 0.05) (Fig. 3).
The somatic growth rates of Anguilla anguilla collected
from seven sites ranged from 14.5 to 62.0 mm/year (Table 1).
The growth rates of A. anguilla yellow eels ranged from
25.9 to 46.2 mm/year with a mean of 34.7 10.4 mm/year
for males; for females, they ranged from 26.9 to 49.5 mm/
year with a mean of 34.1 6.8 mm/year. The growth rates
of the silver eels ranged from 14.5 to 36.3 mm/year with
a mean of 23.1 5.4 mm/year for males; for females, they
ranged from 16.9 to 54.9 mm/year with a mean of
32.1 10.4 mm/year. The growth rates differed significantly
between yellow and silver eels in males and between sexes
T. Arai et al. / Estuarine, Coastal and Shelf Science 67 (2006) 569e578
573
Table 2
Developmental stage of 75 specimens used for otolith microchemistry analyses nd: not determined. Numbers for each sampling location correspond to Fig. 1
Sampling location
Sex
Mean SD
Range
1. River Garavogue, Sligo
Male
Female
5
5
7.5 1.1
8.3 1.6
6.5e9.1
6.8e10.8
Silver
Silver
nd
5
4
1
2. River Moy, Mayo
Male
5
8.3 1.6
6.3e10.6
Female
5
6.8 1.2
5.9e8.2
Yellow
Silver
Yellow
Silver
1
4
3
2
Male
5
6.9 0.7
6.3e7.9
Female
9
6.8 0.9
5.9e8.6
Yellow
Silver
Yellow
Silver
2
3
4
5
3. River Corrib, Galway
4. Galway Bay
Undifferentiated
5. River Shannon, Killaloe
Male
Female
6. River Shannon, Castleconnell
7. Lough Derrevaragh
No. of fish
examined
10
Eye index
No. of
fish
Yellow
10
5
5
9.5 1.3
8.6 1.3
7.3e10.5
7.1e10.2
Silver
Silver
5
5
nd
10
3.6 0.8
2.7e5.1
Yellow
10
Male
Female
1
10
8.8
5.9 1.1
3.9e7.0
Silver
Yellow
Silver
1
7
3
in silver eels (ANOVA, df ¼ 20e35, p < 0.01e0.001), but not
between yellow and silver eels in females or between sexes in
yellow eels (ANOVA, df ¼ 17e32, p > 0.5).
3.2. Otolith microchemistry
The Sr:Ca ratios in the transects along the radius of each
otolith showed the same common feature of a high ratio
near the center of the otolith in all specimens; outside the otolith core, however, there were generally three different patterns
(Fig. 4). All otolith specimens had a central core region with
high Sr:Ca ratios with a maximum of more than 25 103
(Fig. 4) surrounded by an elver mark that could be observed
with a light microscope. The radius of the elver mark in Anguilla anguilla ranged from 124 to 196 mm with a mean SD
of 162 14.3 mm. The high Sr:Ca ratios in the central core
region during the leptocephalus stage may be derived from
the large amounts of gelatinous extracellular matrix that fill
their bodies until metamorphosis (Arai et al., 1997). This
material is composed of sulfated glycosaminoglycans
(GAG), which are converted into other compounds during
metamorphosis (Pfeiler, 1984). The drastic decrease in Sr at
the outer region in both river and seawater samples after metamorphosis to glass eels, may occur because these sulfated
polysaccharides have an affinity to alkali earth elements, and
are particularly high in Sr, suggesting that a high Sr content
in the body has a significant influence on otolith Sr content
through the saccular epithelium in the inner ear, and the sudden loss of Sr-rich GAG during metamorphosis probably
results in the lower Sr concentration in otoliths after metamorphosis (Arai et al., 1997). Outside of the high Sr core, there
was considerable variation in the Sr:Ca ratios in the otoliths
of some of the eels of both species.
nd
Developmental
stage
In Anguilla anguilla, the change in Sr:Ca values outside the
elver mark was generally divided into three types corresponding to the elver, yellow and silver stages (Fig. 4): (1) constantly low values generally ranging between about 0.79 and
2.47 103 (mean values in each site: 0.98e1.78 103)
(64 specimens from all sites except for Galway Bay), (2) relatively high values generally ranging between about 6.73 and
8.89 103 (mean: 7.46 0.79) with no apparent movement
into freshwater (nine specimens from Galway Bay), and
(3) values that change between high and low values at various
distances outside the elver mark within an overall range of
3.87e6.51 103, with a single movement from one high salinity habitat (5.64e8.73 103) to a low salinity habitat
(0.86e1.55 103) (two specimens; one from River Corrib,
the other from Galway Bay). The most interesting individual
of the third type (Galway Bay specimen, age 3 years yellow
eel) apparently lived in seawater for 1e5 years (River Corrib
specimen, age 15 years silver eel) after recruitment, and then
moved to freshwater for the remainder of its life up to capture.
There were 64 specimens of A. anguilla that showed the type
(1) pattern of low Sr:Ca values in their otoliths, which is apparently indicative of long-term residence in freshwater habitats after upstream migration during the elver stage. Nine
specimens showed type (2) values, indicating that they had experienced high salinity during their growth phase. Two others
showed type (3) evidence of remaining in areas with relatively
high salinity for several years before entering freshwater
habitats.
We compared growth rates according to the life history
types as estimated Sr:Ca ratios in otoliths between type
(1) and type (2); we could not include type (3) due to its small
sample size. Significant differences in growth rates were found
between Galway Bay (type 2) and Castleconnell site in River
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T. Arai et al. / Estuarine, Coastal and Shelf Science 67 (2006) 569e578
4. Discussion
Fig. 2. Relationships between body weight and total length of Anguilla anguilla collected in Irish waters in November, 2003. All specimens for each
sex (top), yellow eels for each sex (middle) and silver eels for each sex (bottom) are shown. The asterisk (*) indicates statistical significance.
Shannon (type 1) and between Galway Bay (type 2) and male
eels in River Garavogue (type 1) (ANOVA, df ¼ 13e18,
p < 0.01e0.05), but no significant differences existed for the
other 53 of 55 combinations (ANOVA, df ¼ 9e19, p > 0.05).
The silver eels of Anguilla anguilla examined during this
study showed the same sexual dimorphism in size and body
weight that is present in other temperate anguillid species.
The female silver eels in this study were significantly larger
than the males, and this is typical for this species (Panfili
et al., 1994; Poole and Reynolds, 1996; McCarthy et al.,
1999) and for other temperate species such as Anguilla rostrata
(Oliveira, 1999), Anguilla japonica (Kotake et al., 2003, 2005),
Anguilla australis and Anguilla dieffenbachii (Jellyman et al.,
2001; Arai et al., 2004). Based on a number of previous studies,
Tesch (2003) concluded that the TL of European silver eels during their downstream migration was typically 350e460 mm in
males and 500e610 mm in females. At that life history stage,
their ages were 2e15 years (6 years in average) in males and
4e20 years (8.7 years in average) in females. In Irish waters,
the TL and age of silver eels were as mentioned above (Table 1).
Therefore, the mean growth rates of A. anguilla examined in
several Irish waters of 15e62 mm/year during this study are
typical for Ireland (14e46 mm/year; Moriarty, 1983; Poole
and Reynolds, 1996) and for other European countries such as
Germany (48 mm/year; Berg, 1985), Norway (62 mm/year;
Vollestad and Jonsson, 1986), Poland (41 mm/year; Nagiec and
Bahnsawy, 1990), and France (53 mm/year; Panfili et al., 1994).
There were no significant positive correlations between age
and TL for either sex in silver eels or between age and BW
for female silver eels, although a significant positive correlation
was found between age and BW for male silver eels. Furthermore, no significant differences occurred in age, TL and BW
between yellow and silver eels in each sex. A large variation
in age, TL and BW, and considerable overlap in age and size
of yellow and silver eels indicated that the eels did not start their
downstream migration at a certain fixed age or body size. However, the Australian shortfin eel Anguilla australis needs to attain
a minimum size and an age prior to migration; both these criteria
are extremely variable among populations; and there is considerable overlap in size and age for becoming silver and yellow
shortfin eels (De Silva et al., 2002). In the European eel there is
no critical size or age when they become silvery, nor are size and
age at maturity positively related (Svedang et al., 1996). These
results indicate that the mass of anguillid eels could have no
bearing on their readiness to undertake the spawning migration.
The analyses of patterns of variation of the Sr:Ca ratios in
the otoliths from the Anguilla anguilla examined during this
study indicated that a variety of environmental salinities had
been experienced in the habitats that were occupied during
the growth phase of these individuals. The otolith microchemistry of these eels indicated that most of them had entered
freshwater relatively quickly after recruitment and had stayed
in freshwater until maturation. Nine eels from Galway Bay appeared to have remained in relatively high salinities up until
maturation. In addition, a few individuals of this species
showed evidence of shifts from one salinity level to another,
and at least two specimens showed clear evidence of two
such shifts. This type of variability in otolith microchemistry
and evidence of marine residency also has been found among
T. Arai et al. / Estuarine, Coastal and Shelf Science 67 (2006) 569e578
575
Fig. 3. Relationships between age and total length (left) and between age and body weight (right) of Anguilla anguilla collected in Irish waters in November 2003.
All specimens for each sex (top), yellow eels for each sex (middle) and silver eels for each sex (bottom) are shown. The asterisk (*) suggests statistical significance.
Anguilla japonica from various localities in Japanese coastal
waters (Tsukamoto and Arai, 2001; Arai et al., 2003a,b;
Kotake et al., 2003, 2005) and a river system in Taiwan (Tzeng
et al., 2002). Otolith analyses of the yellow- and silver eel
stages of A. anguilla also have shown evidence of marine residency in the North Sea and Baltic Sea (Tsukamoto et al.,
1998; Tzeng et al., 2000). Similarly, exclusive marine
residency has been inferred for the American eel, Anguilla
rostrata (Jessop et al., 2002) and New Zealand eels, Anguilla
australis and Anguilla dieffenbachii (Arai et al., 2004).
The occurrence and evolution pathway of the migratory diversity of the anguillid eels is not clear, but it has been considered to be due to genetics or environmental adaptation
(Nordeng, 1983; Gross, 1985). The European eel is considered
576
T. Arai et al. / Estuarine, Coastal and Shelf Science 67 (2006) 569e578
Fig. 4. Plots of the Sr:Ca ratios in the otoliths measured along line transects from the core (0 mm) to the edge of the otoliths of all the specimens collected in Irish
waters. Mean ages at each distance from the core in all eels examined in this study and life history stages for the life history transect are shown.
to be a panmictic population (Daemen et al., 2001). Whether
the divergent migratory contingents of eels have different
genotype structures needs to be examined. However, there is
a widely held view that life histories in salmonid fishes are
selected for and adapted to maximize the production of progeny (Schaffer and Elson, 1975; Gross, 1985). In evolutionary
terms, the persistence of migration needs to be seen in relation
to the balance of advantages obtained and the costs incurred
from migration by the population/species. Advantages include
such aspects as increased food supply, avoidance of potentially
harmful environmental conditions and/or a movement to more
favorable ones, the occupation of habitats that have specific or
specialized habitat requirements, and the availability of more
living space. Costs of migration include mortalities resulting
from migration itself and changed environmental conditions
that may be intolerable (McDowall, 1988).
T. Arai et al. / Estuarine, Coastal and Shelf Science 67 (2006) 569e578
Gross (1987) proposed that diadromy occurs when the gain
in fitness from using a second habitat minus the migration
costs of moving between habitats exceeds the fitness from
staying in only one habitat. When glass eels migrate from offshore seawater to upstream freshwater for habitat and feeding,
they have to overcome the osmotic pressure of a saline environment. If they stayed in the estuary habitat, their osmoregulatory cost would be lower than that in either freshwater or
seawater. Estuaries have function as a nursery and feeding
grounds for the juveniles of many fish species (Lenanton,
1982). Many commercially important fish can be present, because estuaries provide suitable food resources as well as shelter, absence of turbulence, and a reduction of predation
(Blaber et al., 1985). These conditions may confine the eel
to the estuarine waters; hence, estuary-dependent eels are predominant in the European eel Anguilla anguilla (Tzeng et al.,
2000), Japanese eel Anguilla japonica (Tsukamoto and Arai,
2001; Arai et al., 2003a,b; Kotake et al., 2003, 2005),
American eel Anguilla rostrata (Jessop et al., 2002) and
New Zealand eels, Anguilla australis and Anguilla dieffenbachii (Arai et al., 2004). In A. anguilla in Ireland, however,
the ecological implications for habitat use are somewhat different than in other regions because the estuarine living space
is limited by high altitude land patterns in many coastal areas.
Thus, most eels might be compelled to grow in either freshwater or coastal seawater. Although we did not examine silver
eels collected in coastal seawater, typical freshwater resident
eels were predominant and, interestingly, a few of the eels
we examined from Ireland’s water did shift habitats from seawater to freshwater during their lifetime. Furthermore, somatic
growth rates did not differ between freshwater and seawater
resident eels in most eels in the present study. Accordingly,
these conditions may result in the majority of Irish eels entering the estuaries of the larger, productive, river systems being
attracted to the freshwater habitats. Consequently, because of
the availability of extensive mesotrophic and eutrophic lake
habitats in many Irish river systems, freshwater-dependent
eels are more abundant in this country. To test this hypothesis,
analyses of the otolith Sr:Ca ratios of silver-phase eels during
their spawning migration in the Irish coastal waters need to be
made, and their degree of migratory type should be compared.
Acknowledgements
The authors would like to thank Ms M. Morrissey,
Mr E. MacLoughlin and the commercial fishermen who
helped us obtain our eel samples. This work was supported
in part by Grants-in-Aid Nos. 15780130 and 15380125 from
the Ministry of Education, Culture, Sports, Science, and Technology of Japan. The work also represents a contribution to
a project on eels supported by the Higher Education Authority,
Ireland, under the PRTLI-3 Programme.
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