Introduction
The European eel Anguilla anguilla is an important species both economically and ecologically. However, over the last two decades, sharp declines in indices of recruitment and escapement for several species of the temperate zone, including A. anguilla have led biologists to become increasingly concerned regarding their long-term conservation status (Dekker et al., Reference Dekker, Casselman, Cairns, Tsukamoto, Jellyman and Lickers2003). Many reasons for these eels’ decline have been proposed, including overfishing of all life stages, habitat degradation, shifts in oceanic currents, barriers to migration (e.g. weirs, dams), accumulation of xenobiotic compounds and parasites (Casselman, Reference Casselman, Aida, Tsukamoto and Yamauchi2003).
The life cycle of the European freshwater eel A. anguilla has five principal stages: the leptocephalus, glass eel, elver, yellow eel and silver eel stages (Bertin, Reference Bertin1956). The spawning area of A. anguilla is supposed to be in the Sargasso Sea (Schmidt, Reference Schmidt1922, Reference Schmidt1925). The larvae, leptocephali, drift on the Gulf Stream and are further transported by the North Atlantic Current across the Atlantic Ocean (Schmidt, Reference Schmidt1922, Reference Schmidt1925; Boëtius, Reference Boëtius1985). The leptocephali presumably leave oceanic currents after metamorphosing into glass eels and then typically migrate upstream as elvers, 6–12 months after hatching (Arai et al., Reference Arai, Otake and Tsukamoto2000; Wang & Tzeng, Reference Wang and Tzeng2000), to grow in the freshwater habitats of Europe and North Africa during the yellow eel stage. At ages that vary widely among individuals of both sexes, but especially among 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, Reference Tesch2003).
Interest in eel biology has increased recently, not only due to conservation concerns, but also because several studies have shown that the catadromous life cycle of the eel is even more complicated than was previously considered. The migratory history of several species of anguillid eels has been studied using microchemical techniques that determine the ratios of strontium to calcium (Sr:Ca ratio) in their otoliths. Previous studies on the strontium incorporation into anguillid eel otoliths showed that the Sr:Ca level in their otoliths strongly correlated with the salinity of the water and was only slightly affected by other factors, such as water temperature, food and physiological factors (Tzeng, Reference Tzeng1996; Lin et al., Reference Lin, Chang, Iizuka and Tzeng2007; Arai & Chino, Reference Arai and Chino2017). Thus, the Sr:Ca ratios of otoliths could help to determine whether individual eels actually entered fresh water at the elver stage and remained 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 certain yellow and silver eel stages of temperate and tropical anguillid eels never migrate into fresh water, but spend their entire life history in the ocean (Arai & Chino, Reference Arai and Chino2012). Application of otolith Sr:Ca ratios to trace the migratory history of eels has also revealed intermediate otolith signatures between those of marine and freshwater residents for A. anguilla (Arai et al., Reference Arai, Kotake and McCarthy2006; Shiao et al., Reference Shiao, Ložys, Iizuka and Tzeng2006; Lin et al., Reference Lin, Yalçin-Özdilek, Iizuka, Gümüş and Tzeng2011), A. japonica (Tsukamoto & Arai, Reference Tsukamoto and Arai2001; Arai et al., Reference Arai, Kotake, Ohji, Miller, Tsukamoto and Miyazaki2003a, Reference Arai, Kotake, Ohji, Miyazaki and Tsukamoto2003b; Kotake et al., Reference Kotake, Arai, Ozawa, Nojima, Miller and Tsukamoto2003, Reference Kotake, Okamura, Yamada, Utoh, Arai, Miller, Oka and Tsukamoto2005), A. rostrata (Lamson et al., Reference Lamson, Shiao, Iizuka, Tzeng and Cairns2006), A. australis and A. dieffenbachii (Arai et al., Reference Arai, Kotake, Lokman, Miller and Tsukamoto2004), 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 freshwater environments and that these species display more of a diverse migration in habitats (Tsukamoto & Arai, Reference Tsukamoto and Arai2001; Arai & Chino, Reference Arai and Chino2012).
Coastal lagoons are increasingly recognized as being in need of fundamental research in addition to the considerable number of applied studies that focus on specific local environmental or natural resource issues (Kennish & Paerl, Reference Kennish and Paerl2010). Lagoons are located at the interface between land and sea, and it has been estimated that they comprise ~13% of the world's coastal areas (Kjerve, Reference Kjerve1990). Lagoons typically provide breeding areas for birds, fishes and crustaceans that can often be used to support local fisheries and ecologically sustainable tourism activities (Kennish & Paerl, Reference Kennish and Paerl2010). However, despite being of great importance in terms of biodiversity, fisheries and recreational activities, coastal lagoons are threatened throughout the world by a series of anthropogenic impacts (Berkes & Seixas, Reference Berkes and Seixas2005; Kennish & Paerl, Reference Kennish and Paerl2010). The threats to lagoon ecosystems and to habitats with which they are linked in terms of hydrodynamics or ecology vary according to region and intensity of human activity (Berkes & Seixas, Reference Berkes and Seixas2005; Kennish & Paerl, Reference Kennish and Paerl2010). The European eel is a typical fish in lagoon systems in Ireland (Moriarty, Reference Moriarty1996). Investigations into this eel's ecology and local migratory behaviour in lagoon ecosystems could provide new perspectives that might underpin lagoon conservation plans and provide new information on the population ecology of the declining European eel.
In this paper, we seek to contribute to a better understanding of the ecology of coastal lagoon populations of eels in north-western Europe. Specifically, we present results of a study of eel migrations in a complex coastal lagoon system and adjacent marine habitats in Ireland through the otolith microchemistry (Sr:Ca ratios). We provide new information on habitat utilization patterns and local movements of European eel and we discuss the life-history plasticity of eels (Arai & Chino, Reference Arai and Chino2012) that enables them to effectively exploit habitats across a wide salinity spectrum.
Materials and methods
Study site
We sampled eels along a short (~2 km) marine–freshwater salinity gradient in four basins of Lough (lake) Ahalia in County Galway, western Ireland (53°23′N 9°34′W, Figure 1). Lough Ahalia is an Atlantic coastal lake that consists of a series of basins forming the lower section of the River Screebe catchment. The system flows into the Atlantic Ocean via a single exit in Camus Bay. The lowest basin (surface area ~25 ha, mean depth = 1.6 m) receives twice daily saline intrusions on flood tides. The saline influence continues, but intensity weakens in the central basin (surface area ~60 ha, mean depth = 2.5 m), which receives saline input on spring tides (i.e. fortnightly). The upper basin (surface area ~40 ha, mean depth = 1.7 m) is entirely freshwater with a single significant inflow from the Screebe River, which drains the upper part of the catchment. The scale and intensity of the saline influence on the lower and central sections varies with the tidal cycle (e.g. spring to neap) and the strength and direction of the wind. The Screebe system supports a recreational fishery for migratory salmon (Salmo salar) and brown trout (S. trutta). This system was chosen for the study because it displays a very marked salinity gradient (0.5–34‰) over a relatively short linear distance (~2 km) and importantly, the eel stock is unexploited.
Fig. 1. Lough Ahalia, showing location in Ireland and the four distinct salinity zones referred to in this study: fresh water (FW; 12 eels), brackish water (BW; 24 eels), marine dominated (MW; 36 eels) and full seawater (SW; 21 eels) collected from four distinct salinity zones.
Salinity
To characterize typical salinity values within the four basins of Lough Ahalia, we collected bimonthly (September 2003–June 2004) salinity data from a series of locations over a 200-m grid (N = 30). Salinity values were recorded every 50 cm throughout the water column using a Hydrolab 4a Datasonde (Hydrolab Inc., USA). Significant variation between salinity values was recorded within each basin so using 90th percentile benthic salinity, we classified them into four distinct salinity zones: freshwater (FW: <0.1‰); brackish water (BW: ~15‰); marine-dominated water (MW: ~25‰) and full seawater (SW: ~34). As eels are typically benthic species, we consider benthic salinities to be most representative of their habitats.
Fish collection
European eels were sampled between September 2003 and November 2004 using unbaited summer fyke nets (Poole, Reference Poole1990) at sites along the salinity gradient in four basins of Lough Ahalia (Figure 1). In FW, BW, MW and SW basins, eels were collected on 19 August 2004, 17 September 2003 and 19 August 2004, 13 May 2004, 7–9 October 2004 and 19 November 2004 and 15 October 2004, respectively. Fyke nets are selective for eels of total length (TL) >300 mm (McCarthy et al., Reference McCarthy, Cullen and O'Connor1999). A total of 93 specimens (FW = 12, BW = 24, MW = 36, SW = 21) were used in this study. Fish sampling was in accordance with a guide for animal experimentation at National University of Ireland (NUI) and fish-handling approval was granted by the animal experiment committee of NUI.
After measurement of TL (to 1 mm), body weight (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 (Reference Tesch2003), 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, Reference Pankhurst1982). 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). The eye index was calculated according to Pankhurst (Reference Pankhurst1982) as follows:
$${\rm Eye}\,{\rm index} = \lcub {{[ {\lpar {A + B} \rpar /{\rm 4}} ] }^{\rm 2} \times \pi /{\rm TL}} \rcub \times {\rm 1}00$$where A is the horizontal eye diameter (mm) and B is the vertical eye diameter (mm).
Based on the result and the Pankhurst criteria (Pankhurst, Reference Pankhurst1982), there were in total 69 yellow (all FW, BW and SW eels and 12 MW eels) and 24 MW silver eels (Table 1). We analysed the migratory histories for yellow and silver eels separately in MW eels.
Table 1. Biological characteristics of Anguilla anguilla specimens used for otolith microchemistry analyses
FW, fresh water; BW, brackish water; MW, marine-dominated water; SW, seawater.
Y, yellow eel; S, silver eel.
M, male; F, female; U, undifferentiated.
Otolith preparation and microchemical analysis
Sagittal otoliths were extracted from each fish, embedded in epoxy resin (Struers, Epofix) and mounted on glass slides. Otoliths were ground and polished as described by Arai et al. (Reference Arai, Kotake and McCarthy2006), cleaned in an ultrasonic bath, and rinsed with deionized water prior to being examined.
For electron microprobe analyses, all otoliths (93 specimens) were platinum (Pt)-palladium (Pd) coated by a high vacuum evaporator. 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. (Reference Arai, Kotake and McCarthy2006). Wollastonite (CaSiO3) and Tausonite (SrTiO3) were used as standards. The accelerating voltage and beam current were 15 kV and 1.2 × 10−8 A, respectively. The electron beam was focused on a point 10 µm in diameter, with measurements spaced at 10 µm intervals.
Trace elemental signatures in the edge of otoliths accumulate in the final part of the fish's life before natural death or capture and have been used to trace migrations (Arkhipkin et al., Reference Arkhipkin, Schuchert and Danyushevsky2009; Schuchert et al., Reference Schuchert, Arkhipkin and Koenig2010). Sr:Ca ratios of otolith edges were examined for all specimens.
Statistical analyses
Differences among data for comparisons of biological characteristics such as TL and body weight of four salinity basins (FW, BW, MW and SW) in yellow and silver eels, the average Sr:Ca ratios outside of the elver mark and the average Sr:Ca ratios in otolith edges for FW, BW, MW and SW yellow eels and MW silver eels, were tested by a Kruskal–Wallis test. Differences between data for comparison of the average Sr:Ca ratios outside of the elver mark between the two types for MW silver eels were analysed using the Mann–Whitney U-test (Sokal & Rohlf, Reference Sokal and Rohlf1995).
Results
Biological characteristics
The TL of Anguilla anguilla collected from four salinity zones ranged from 278–919 mm (Table 1). The TL of the yellow eels ranged from 278–436 mm (358 ± 53.8 mm; mean ± SD) and 338–755 mm (489 ± 107 mm) for males and females, respectively. For silver eels, TL ranged from 298–434 mm (354 ± 32.4 mm) and 359–919 mm (540 ± 193 mm) for males and females, respectively. There were significant differences in total length between FW and SW and between MW and SW in yellow eels for females (Kruskal–Wallis test, df = 23, P < 0.05–0.01). However, no significant differences occurred in total lengths between other salinity zones (14 combinations) in yellow and silver eels for females and males (Kruskal–Wallis test, df = 2 to 32, P > 0.05).
The body weight of A. anguilla collected from the four salinity zones ranged from 36–1836 g (Table 1). The body weight of the yellow eels ranged from 36–146 g (81 ± 34.4 g; mean ± SD) for males and from 71–896 g (240 ± 195 g) for females. For silver eels, the body weight ranged from 46–128 g (78 ± 21.2 g) for males and from 97–1836 g (540 ± 193 g) for females. There were significant differences in body weight between FW and SW and between MW and SW in yellow eels for females (Kruskal–Wallis test, df = 22, P < 0.05–0.005), but no significant differences occurred in total length between other salinity zones (14 combinations) in yellow and silver eels for females and males (Kruskal–Wallis test, df = 2 to 28, P > 0.05).
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 centre of the otolith; outside the otolith core, however, there were generally three different patterns (Figure 2). All otolith specimens had a central core region with high Sr:Ca ratio with a maximum of more than 25 × 10−3 (Figure 2) surrounded by an elver mark corresponding to the period of their leptocephalus and early glass eel stages in the ocean that could be observed with a light microscope. The radius of the elver mark in Anguilla anguilla ranged from 110–210 µm.
Fig. 2. Sr:Ca profiles measured along line transects from the core (0 µm) to the edge of the otolith for all the A. anguilla specimens collected in the four zones of Lough Ahalia. Y: yellow eel, S: silver eel. FW: freshwater, BW: brackish water, MW: marine dominated, SW: full seawater. The line history transects showed a single movement from one low salinity habitat to a high salinity habitat, were separated (one from a BW yellow eel, the other from an SW yellow eel). In MW, the line history transects were separated as three categories, constantly low values (19 silver eels) and relatively high values of all (12) yellow and 5 silver eels.
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/or silver stages (Figure 2): (1) constantly low values generally ranging from ~1.93–3.99 × 10−3 (all FW yellow eels and 19 MW silver eels); (2) relatively high values generally ranging from ~6.22–9.48 × 10−3 with no apparent movement into fresh water (23 BW yellow eels, all MW yellow eels, 5 MW silver eels and 20 SW yellow eels); and (3) values that showed a single movement at ~500 µm from one low salinity habitat (1.90–3.30 × 10−3) to a high salinity habitat (7.48–8.22 × 10−3) (two specimens; one from a BW yellow eel, the other from an SW yellow eel).
The average Sr:Ca ratios (± SD) outside of the elver mark for FW, BW, MW and SW yellow eels and MW silver eels were 3.34 ± 0.33 × 10−3, 7.25 ± 0.76 × 10−3, 7.50 ± 0.54 × 10−3, 8.33 ± 0.82 × 10−3 and 3.93 ± 2.04 × 10−3, respectively. There were significant differences in the average Sr:Ca ratios between eight combinations for FW, BW, MW and SW yellow eels and MW silver eels (Kruskal–Wallis test, df = 18 to 40, P < 0.0005–0.0001; Table 2); however, no significant differences were found for those of two combinations (Kruskal–Wallis test, df = 24 to 29, P > 0.05; Table 2). Interestingly, a significant difference was also found in the average Sr:Ca ratios between the two types (constantly low values (2.94 ± 0.60, N = 19) and relatively high values were found (7.52 ± 0.91, N = 5)) for MW silver eels (Mann–Whitney U-test, df = 4, P < 0.0005) (Figure 2).
Table 2. Statistical results (P value) of the average otolith Sr:Ca ratios outside of the elver mark between each habitat in yellow and silver eels
FW: fresh water; BW: brackish water; MW; marine dominated; SW: seawater.
The average Sr:Ca ratios (± SD) in otolith edges for FW, BW, MW and SW yellow eels and MW silver eels were 3.18 ± 0.80 × 10−3, 6.67 ± 1.58 × 10−3, 7.43 ± 2.32 × 10−3, 8.15 ± 1.92 × 10−3 and 3.74 ± 2.18 × 10−3, respectively. There were significant differences in the average Sr:Ca ratios between seven combinations for FW, BW, MW and SW yellow eels and MW silver eels (Kruskal–Wallis test, df = 13–41, P < 0.01–0.0001; Table 3); however, no significant differences were found for those of three combinations (Kruskal–Wallis test, df = 16 to 30, P > 0.05; Table 3).
Table 3. Statistical results (P value) of Sr:Ca ratios in otolith edges between each habitat in yellow and silver eels
FW, fresh water; BW, brackish water; MW; marine dominated; SW, seawater.
Discussion
The variation of otolith Sr:Ca ratios indicated that Anguilla anguilla experienced a variety of environmental salinities in a tidal Atlantic lake system of Ireland. The otolith microchemistry of these eels indicated that 91 of 93 (98%) eels had entered each salinity environment basin relatively quickly after recruitment and had stayed in each environment basin until maturation without movement to another salinity environment. Only 2 of 93 (2%) eels had shifted their habitat once in their lives (Figure 2). The result suggests that each individual might have an environmental habitat preference, although each individual could move along a short (<2 km) salinity gradient. The apparent habitat use and movement patterns in this study support the findings of previous research on other temperate eels that appear typically to have notably localized home ranges but do very occasionally move to different areas. For example, studies on A. rostrata have determined that their yellow eels have a restricted home range and that they return to their initial habitat after foraging outside their territory (Bozeman et al., Reference Bozeman, Helfman and Richardson1985; Ford & Mercer, Reference Ford and Mercer1986; Oliveira, Reference Oliveira1997) or return to their home range after being artificially displaced (Parker, Reference Parker1995). Similarly, studies of New Zealand eels concluded that the large eels have restricted home ranges and typically only move short distances within these streams (Burnet, Reference Burnet1969; Chisnall & Hicks, Reference Chisnall and Hicks1993; Jellyman & Sykes, Reference Jellyman and Sykes2003).
Harrod et al. (Reference Harrod, Grey, McCarthy and Morrissey2005) showed that the somatic composition of eels differed along the salinity gradient in Lough Ahalia, which is the same study site as this study. The lipid-treated C:N data showed differences in body composition, with BW eels having lower mean lipid-treated C:N than eels from FW or MW. These differences were due to a small but significant reduction in mean carbon content in BW fish. The greatest contrast between BW eels and eels from other salinity zones was dietary, with BW eels feeding at a lower trophic level. Harrod et al. (Reference Harrod, Grey, McCarthy and Morrissey2005) suggested that their diet may include an increased proportion of macroinvertebrates relative to eels from the other salinity zones, and the most abundant littoral macroinvertebrate taxa in the BW zone are isopods (e.g. Sphaeroma spp.) and amphipods (Gammarus spp.). These taxa have low mean carbon content relative to values typically recorded from other benthic invertebrates (Salonen et al., Reference Salonen, Sarvala, Hakala and Viljanen1976; Penczak, Reference Penczak1985; Frost et al., Reference Frost, Tank, Turner and Elser2003) or fishes, both from Lough Ahalia, or other systems (Penczak, Reference Penczak1985; Tanner et al., Reference Tanner, Brazner and Brady2000). The reduced muscle carbon content in BW eels relative to FW or MW fish may be related to differences in diet. Therefore, the diverse salinity habitat uses found in this study might also be related to the feeding preference of each eel because we found significant differences in their somatic growth (TL and body weight) between FW and SW and between MW and SW in yellow eels for females. There was some evidence that in Lough Ahalia, faster growth was associated with increased salinity (Harrod et al., Reference Harrod, Grey, McCarthy and Morrissey2005). Similar patterns of enhanced growth in brackish water have been observed in A. anguilla (Fernandez-Delgado et al., Reference Fernandez-Delgado, Hernando, Herrera and Bellido1989) and other species of Anguilla, e.g. A. rostrata (Lamson et al., Reference Lamson, Shiao, Iizuka, Tzeng and Cairns2006) and A. japonica (Tzeng et al., Reference Tzeng, Iizuka, Shiao, Yamada and Oka2003). Tzeng et al. (Reference Tzeng, Iizuka, Shiao, Yamada and Oka2003) have suggested that the energetic costs of osmoregulation are minimized in eels in salinities closest to that of their body fluids (10.5–14), and they propose that this may contribute to the better growth seen in marine and brackish eels. However, marine and estuarine productivity tend to be higher than that in adjacent fresh waters at higher latitudes (Gross, Reference Gross1987; Gross et al., Reference Gross, Coleman and McDowall1988) and mixohaline eels may simply have access to greater food resources.
Two distinct groups of Sr:Ca ratios were found in MW silver eels (Figure 3). Such distribution was not found in other salinity environments. The lower Sr:Ca ratio value individuals (19 eels) might just migrate from the freshwater upstream for downstream migration as silver eels for spawning in the Atlantic Ocean. In contrast, the higher Sr:Ca ratio value individuals (5 eels) might reside in the MW environment as with MW yellow eel individuals or might come from the SW environment.
Fig. 3. Distribution of the mean Sr:Ca ratio values outside the elver mark in each otolith of the specimens used in the present study.
Otolith Sr:Ca ratios from the otolith edge provide information on the environment experienced by the fish prior to capture (Arkhipkin et al., Reference Arkhipkin, Schuchert and Danyushevsky2009; Schuchert et al., Reference Schuchert, Arkhipkin and Koenig2010). The criteria ratios of FW, BW, MW and SW in Lough Ahalia were 3.18 × 10−3, 6.67 × 10−3, 7.43 × 10−3 and 8.15 × 10−3. However, the criterion ratios of fresh water varied among study sites ranging from 0.72–5.29 × 10−3 (Arai et al., Reference Arai, Kotake and McCarthy2006; Shiao et al., Reference Shiao, Ložys, Iizuka and Tzeng2006; Tabouret et al., Reference Tabouret, Bareille, Claverie, Pécheyran, Prouzet and Donard2010). It is apparent that the otolith Sr:Ca ratios of Anguilla anguilla living in fresh water can vary substantially between regions. Furthermore, the criterion ratios of seawater also varied among study sites ranging from >4.9–6.0 × 10−3 (Arai et al., Reference Arai, Kotake and McCarthy2006; Tabouret et al., Reference Tabouret, Bareille, Claverie, Pécheyran, Prouzet and Donard2010). This may be due to region-specific spatial and temporal variation in Sr:Ca concentrations in the water (Kraus & Secor, Reference Kraus and Secor2004; Munro et al., Reference Munro, McMahon and Ruzycki2005), different equipment used for measurement of otolith Sr:Ca ratios or the effect of water temperatures (Campana, Reference Campana1999; Elsdon & Gillanders, Reference Elsdon and Gillanders2002; Martin et al., Reference Martin, Thorrold and Jones2004).
Gross (Reference Gross1987) 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 fresh water 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 fresh water or seawater. Estuaries function as a nursery and feeding grounds for the juveniles of many fish species (Lenanton, Reference Lenanton1982). Many commercially important fish can be present because estuaries provide suitable food resources, as well as shelter, absence of turbulence, and reduced predation (Blaber et al., Reference Blaber, Young and Dunning1985). These conditions may confine the eel to estuarine waters; hence, estuary-dependent eels are predominant in the European eel Anguilla anguilla (Arai et al., Reference Arai, Kotake and McCarthy2006; Shiao et al., Reference Shiao, Ložys, Iizuka and Tzeng2006), Japanese eel A. japonica (Tsukamoto & Arai, Reference Tsukamoto and Arai2001; Arai et al., Reference Arai, Kotake, Ohji, Miller, Tsukamoto and Miyazaki2003a, Reference Arai, Kotake, Ohji, Miyazaki and Tsukamoto2003b; Kotake et al., Reference Kotake, Arai, Ozawa, Nojima, Miller and Tsukamoto2003, Reference Kotake, Okamura, Yamada, Utoh, Arai, Miller, Oka and Tsukamoto2005), American eel A. rostrata (Lamson et al., Reference Lamson, Shiao, Iizuka, Tzeng and Cairns2006) and New Zealand eels A. australis and A. dieffenbachii (Arai et al., Reference Arai, Kotake, Lokman, Miller and Tsukamoto2004). For A. anguilla in Ireland, the ecological implications for habitat use are similar to those in other regions. These eels migrate flexibly among freshwater, brackish water and seawater environments.
Author ORCID
Takaomi Arai, 0000-0001-9440-7933
Financial support
This work was supported in part by Universiti Brunei Darussalam under the Competitive Research Grant Scheme (Vot No. UBD/OVACRI/CRGWG(003)).
