Validation of the occurrence of the American eel Anguilla rostrata (Le Sueur, 1817) in free-draining European inland waters

The screening of 2,735 eels from European waters and aquaculture farms was conducted using mitochondrial Cytochrome b and 16S rRNA gene fragments amplified by polymerase chain reaction. Reaction products were either sequenced directly or subjected to analysis using restriction fragment length polymorphism which resulted in species-specific restriction patterns. Beside the expected European eel, Anguilla anguilla (Linnaeus, 1758), the American eel, Anguilla rostrata (Le Sueur, 1817), was also identified in samples from both aquaculture (N = 40 out of 1,025) and from natural waters (N = 44 out of 1,710). The life stages of American eels identified from several German waters draining to either the Baltic Sea and the North Sea ranged from elver to silver eels. This indicates that stocking with glass eels or elvers must have occurred several times most likely in the period from 1998 to 2002. The application of a fast and precise method for species identification and genetic monitoring of eels delivered for stocking is therefore essential for maintaining the autochthonous species composition in future. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Decline in non-native freshwater eels in Japan: ecology and future perspectives

The occurrence, distribution, and biological characteristics of non-native freshwater eels were analyzed using 5524 eels collected from 16 sites in Japan between 1997 and 2005. Three hundred seventy-four fishes (6.8%) were identified as non-native European eels, Anguilla anguilla, while the remainder (93.2%) were native Japanese eels, A. japonica. The European eel was found at 7 sites (44%), including 3 rivers, 2 freshwater lakes, one brackish lake, and one sea bay, suggesting a wide rage of habitat use. This variability of habitat use was also evidenced by the otolith microchemistry, which showed that they had lived in not only freshwater but also in seawater habitats. The sites with European eel were localized within the vicinity of southern Japan where a number of these eels were cultivated in the early 1970’s, suggesting that some had escaped from the culture ponds or were released intentionally into nearby natural waters. The large body size (mean total length: 803 mm), pigmented skin, enlarged eyes, and relatively matured gonads (mean gonad somatic index: 1.9) found in non-native European eels indicated that most had metamorphosed into the migratory silver phase, suggesting their ability to initiate spawning migration. However, the proportion of European eels in Mikawa Bay in 1997 was more than 12%, which decreased markedly to less than 2% after 2001, corresponding to the recent decline in import of European glass eels for aquaculture. This suggests that the population of European eels will decrease in Japanese waters in the future.     

An Examination of Utilizing External Measures to Identify Sexually Maturing Female American Eels, Anguilla Rostrata, in the St. Lawrence River

It is well established that Anguillid eels undergo a complex suite of morphological and physiological changes during their transformation from resident, yellow-phase juveniles to actively migrating silver-phase eels. While it has been shown that some morphological measures can be used successfully to identify sexually maturing European eels, Anguilla anguilla, as well as Australian short fin, Anguilla australis, and long fin, Anguilla dieffenbachii eels, this relationship has never been quantitatively assessed for American eels, Anguilla rostrata. American eels of varying sexual development were collected from three locations on the St. Lawrence River: Lake St. Lawrence, Quebec City and Kamouraska. Sexual development of each eel was assessed with gonadosomatic index (GSI), oocyte diameter and degree of oocyte development. Morphological measures of total length, weight, head width, pectoral fin length and vertical and horizontal eye diameters were obtained from each fish. We used this data to test two hypotheses: (i) resident yellow phase eels, suspected migrants and known migrants are morphologically indistinguishable; and (ii) if differences exist, they cannot be used to reliably predict gonadal development or migratory status. Univariate analysis (ANOVA and ANCOVA) indicated that there were highly significant differences in all of the measured parameters and thus we were able to reject the first hypothesis. However, we failed to reject the second hypothesis as the high degree of overlap between groups eliminated the ability of any single measure to differentiate between resident and migratory eels. A multivariate discriminant model was developed that could classify only 72–80% of the eels correctly based on their morphological characters. While morphological measures may have some potential as a rapid, cost-effective method of pre-screening individual eels, morphological measures should not be considered a definitive indicator of sexual maturity or migratory status for female American eels in the Upper St. Lawrence River.     

Vital population statistics based on length frequency analysis of the exploited Japanese eel (Anguilla japonica) stock in the Kao‐Ping River,southern Taiwan

Vital statistics such as growth, mortality, and maturity parameters are crucial in understanding the population dynamics of a species. A total of 7 074 Japanese eels (Anguilla japonica) in the lower reach of the Kao‐Ping River, southern Taiwan, were collected with eel tubes in 1998 ～ 2004 and shrimp nets in 2004 ～ 2007. Data from 2004 were excluded due to mixed gear information and escapement of cultured eels; in subsequent years escaped cultured eels were identified and excluded from analyses. The estimated asymptotic length in the von Bertalanffy growth function (84.5–110 cm) was smaller, while the Brody growth parameter (0.30–0.44 year^?1) was higher using electronic length frequency analysis (ELEFAN) than when using Shepherd’s length composition analysis (SLCA). The total instantaneous mortality rate (Z) was around 1 for periods 1998–2003 and 2 year^?1 for 2005–2007 using length‐converted catch curves. The 95% confidence intervals of Z did not overlap for two of the periods, suggesting that the mortality rates were significantly higher during 2005–2007, possibly due to the introduction of shrimp nets. The maturity function differed significantly between sexes, indicating that females become silver eels at a larger size. The Japanese eels in the lower reach of the Kao‐Ping River were likely heavily exploited, thus management and conservation actions are strongly recommended.     

Validation of annulus in otolith and estimation of growth rate for Japanese eel <Emphasis Type="Italic">Anguilla japonica</Emphasis> in tropical southern Taiwan

The age of Japanese eels (Anguilla japonica) is often estimated from otoliths, but this method has not been fully validated, particularly in tropical areas where the annulus in otolith is considered to be less distinct than in temperate areas. To validate the annuli in Japanese eel otoliths from southern Taiwan, known-age (2 year-old) cultured eels from an eel farm and wild eels from Kao-Ping River were collected. It was found that 26 out of 31 cultured eels (83.9%) showed two clear annuli and the remained 5 eels showed either one or three annuli. The mean (± SD) age of the cultured eels was 1.97 ± 0.4 years. Meanwhile, a clear peak in the mean monthly marginal increment ratio of the otolith in wild yellow and silver eels occurred once a year during winter (November to March). The annual deposition of presumed annuli in otoliths of Japanese eel was validated and the age and growth rate estimation for Japanese eels in the tropical southern Taiwan is deemed feasible. The growth rate of cultured eels was significantly faster than that of wild eels, but it did not differ significantly between sexes for wild silver, yellow or cultured eels. The von Bertalanffy Growth Function parameters (K, and t ₀ ) of the wild eels were estimated as 0.114 ± 0.028 year⁻¹, 1178 ± 171 mm and −0.8 ± 0.2 years, respectively.     

Migration,residency and habitat utilisation by wild and cultured Japanese eels (Anguilla japonica) in a shallow brackish lagoon and inflowing rivers using acoustic telemetry

This study monitored post-release movements of 20 wild Japanese eels (Anguilla japonica) [mean ± S.D. 520.8 ± 92.3 mm total length (TL), 217.9 ± 146.3 g body mass (BM)] in a brackish water lagoon in northeastern Japan using acoustic telemetry to elucidate how wild Japanese eels use different river, estuary and marine environments. In addition, 12 cultured Japanese eels (TL = 578.9 ± 18.0 mm, BM = 344.9 ± 25.5 g) were released to understand the comparative behaviours of wild and cultured eels. Both types of eels were simultaneously released in the southern inner part of the lagoon in September 2016 where there are freshwater influences from a river. Following release, eight of the wild eels (40%) were largely sedentary near the released point (river mouth) and stayed at the site for overwinter. Nonetheless, several individuals showed behavioural plasticity of habitat use: three wild eels moved towards the northern part of the lagoon with stronger influence from the sea during May–July 2017. Two wild eels showed clear repeated movements from the lagoon to a river at night and returned to the lagoon by dawn for more than a week every day, and one wild eel migrated upstream for overwintering. Signals from 55% of the wild eels could be detected for more than 6 months, whereas those from all of the cultured eels were lost by December 2016, indicating a short resident time of large cultured eels (BM > 200 g) released in a brackish water area. One wild silver eel migrated to the outer sea during the ebb tide at night in November 2016, probably triggered by the decrease in water temperature (from c. 20°C to c. 13°C), and seven cultured eels similarly moved to the outer sea during October–November 2016. The results revealed the similarities (e.g., nocturnal movements) and differences (e.g., stay period and seasonal movements) in the behavioural characteristics of wild and cultured eels and indicated that habitat connectivity among river, estuary and coastal waters is crucial for enabling eels to efficiently utilise these productive habitats through their behavioural plasticity.     

Stable isotope analyses provide new insights into ecological plasticity in a mixohaline population of European eel

Recent studies have shown that anguillid eel populations in habitats spanning the marine–freshwater ecotone can display extreme plasticity in the range of catadromy expressed by individual fishes. Carbon and nitrogen stable isotope analysis was used to differentiate between European eels (Anguilla anguilla) collected along a short (2 km) salinity gradient ranging from <1‰ to ~30‰ in Lough Ahalia, a tidal Atlantic lake system. Significant differences were recorded in mean δ¹³C, δ¹⁵N and C:N values from eels collected from fresh, brackish and marine-dominated basins. A discriminant analysis using these predictor variables correctly classified ca. 85% of eels to salinity zone, allowing eels to be classified as freshwater (FW), brackish (BW) or marine (MW) residents. The results of the discriminant analysis also suggested that a significant proportion of eels moved between habitats (especially between FW and BW). Comparisons of several key population parameters showed significant variation between eels resident in different salinity zones. Mean condition and estimated age was significantly lower in MW eels, whilst observed length at age (a correlate of growth) was significantly higher in MW eels, intermediate in BW and lowest in FW eels. This study has demonstrated that the ecology of eels found along a short salinity gradient can be extremely plastic and that stable isotope analysis has considerable utility in demonstrating intra-population variation in diadromous fishes.     

A description of rodlet cells from the alimentary canal of Anguilla anguilla and their relationship with parasitic helminths

Rodlet cells in intestinal epithelia of infected and uninfected European eels Anguilla anguilla from brackish and fresh water were studied by light and electron microscopy. Deropristis inflata (Trematoda) was found in eels from brackish water, whereas eels from fresh water were infected with Acanthocephalus clavula (Acanthocephala). In a comparison between uninfected and infected eels from brackish water, a higher number of rodlet cells was recorded in the intestinal epithelia of infected fish. Evidence is presented that rodlet cells secrete their contents in a holocrine manner into the lumen of the eel intestine. The occurrence of organelles within the mature rodlet cell was rare. ? 1998 The Fisheries Society of the British Isles     

Optimizing the mass marking of fish with alizarin red S: an example with glass eels

Fish marking is an essential tool for fisheries management, especially for evaluating the stocking of endangered fish species to support conservation and sustainable use of fish stocks. Batch marking of young European eels Anguilla anguilla (L.) prior to stocking is recommended as the benefits of stocking for the spawning stock can be evaluated by recapturing marked fish over time, therefore mass marking of young eels with substances such as alizarin red S (ARS) is becoming increasingly important. To improve the marking method and reduce marking costs when immersing glass eels in an ARS solution, eight laboratory experiments under varying conditions (e.g., temperature, ARS concentration, immersion time, osmotic induction, fish density) and with ARS from different suppliers were carried out. The results show that optimal marking of glass eels can be carried out in the field or during transport by putting approximately 50 g of glass eels per liter in 150 mg L⁻¹ ARS solution for 3 h at 10–15°C. Lower concentrations did not result in reliable marking. Water temperatures of 5°C and below can have a stunning effect on the eels and increase mortality significantly, regardless of the concentration of ARS. Glass eel densities below 50 g L⁻¹ in the marking bath increase marking costs unnecessarily, while a higher density of 100 g L⁻¹ resulted in significantly higher mortality and lower marking success. A somewhat more difficult but less expensive alternative is to bathe the fish in a saline solution of 1% (10 PSU) of 80 mg L⁻¹ ARS for 3 h at 10°C. Costs can also be significantly reduced by choice of supplier for ARS, but care should be taken as the quality of the powder appears to vary (mean percentage of sufficiently marked eels ranged from 59% to 91% among suppliers in the present study) and can lead to marking failure. The optimal marking conditions can help ensure that stocked glass eels can be reliably identified in future studies to assess stocking benefits while reducing costs.     

Feeding habitat and silvering stage affect lipid content and fatty acid composition of European eel Anguilla anguilla tissues

Lipids, particularly fatty acids (FAs), are major sources of energy and nutrients in aquatic ecosystems and play key roles during vertebrate development. The European eel Anguilla anguilla goes through major biochemical and physiological changes throughout its lifecycle as it inhabits sea- (SW), and/or brackish- (BW) and/or freshwater (FW) habitats. With the ultimate goal being to understand the reasons for eels adopting a certain life history strategy (FW or SW residency vs. ‘habitat shifting’), we explored differences in lipid content and FA composition of muscle, liver and eyes from eels collected across Norwegian SW, BW and FW habitats, and at different lifecycle stages (yellow to silver). FW and SW eels had a higher lipid content overall compared to BW eels, reflecting differences in food availability and life history strategies. SW eels had higher proportions of certain monounsaturated FAs (MUFAs; 18:1n-9, 20:1n-9), and of the essential polyunsaturated FAs 20:5n-3 (eicosapentaenoic acid, EPA) and 22:6n-3 (docosahexaenoic acid) than FW eels, reflecting a marine-based diet. In contrast, the muscle of FW eels had higher proportions of 18:3n-3, 18:2n-6 and 20:4n-6 (arachidonic acid), as is typical of FW organisms. MUFA proportions increased in later stage eels, consistent with the hypothesis that the eels accumulate energy stores prior to migration. In addition, the decrease of EPA with advancing stage may be associated with the critical role that this FA plays in eel sexual development. Lipid and FA information provided further understanding of the habitat use and overall ecology of this critically endangered species.     

Isolation and characterization of two different 5S rDNA in Anguilla anguilla and in Anguilla rostrata: possible markers of evolutionary divergence

We cloned and sequenced the HaeIII 350‐bp 5S ribosomal DNA (rDNA) band of Anguilla rostrata and designed specific primers from this sequence. Polymerase chain reaction performed with these primers is able to distinguish DNA samples obtained from European (Anguilla anguilla) and American (Anguilla rostrata) eels. Two amplicons of 1200 bp and 600 bp were obtained, respectively, from A. rostrata and A. anguilla, and the whole 5S rDNA repeated unit from these eels was cloned and sequenced. Southern blot experiments, using four different restriction enzymes and the 5S nontranscribed spacers regions as probe, are able to point out specific diversity in these eels.     

Do young on‐grown eels,Anguilla anguilla (Linnaeus, 1758), outperform glass eels after transition to a natural prey diet?

Survival rates among European eels, Anguilla anguilla (Linnaeus, 1758), on‐grown using a formulated diet in a commercial aquaculture facility, were compared with glass eels from the same cohort following their transition to a natural prey diet in the laboratory. Treatments included zero, 42‐day, and 196‐day periods of grow‐out prior to 30‐day experimental periods when eels were fed Chironomus spp. larvae (10 tanks, each containing 240‐L water and 40 glass or 10 on‐growing eels; 12:12 hr photoperiod; water temperature 18°C). All glass eels survived, compared to 87% (42‐day) and 99% (196‐day) for on‐grown eels. Although the eels on‐grown for 196 days had a high survival rate, they did lose weight. Farm‐reared eels may have accumulated sufficient resources over the 196‐days to survive the first 30 days after weaning from a formulated diet, but not for an additional 30 days (84% survival). Lack of superior survival rates among on‐grown eels challenges the presumed benefits of releasing on‐grown eels for population restoration.     

Interspecific and sexual differences in riverine distribution of tropical eels Anguilla spp.

A total of 261 individuals of the four tropical eel species, Anguilla celebesensis, Anguilla marmorata, Anguilla bicolor pacifica and Anguilla interioris, were collected from 12 locations around Sulawesi Island, Indonesia, to gain knowledge about the riverine distribution of tropical eels. Anguilla marmorata was predominant in the lower reaches of Poso River (94·4% of total eel catch in the sampling area), Poso Lake (93·3%), three small inlet rivers of Tomini Bay (100%) and Laa River (92·3%). Anguilla celebesensis occurred frequently in the inlet rivers of Poso Lake (63·5%). Anguilla bicolor pacifica and Anguilla interioris were rare (1.5 and 0.4%, respectively). Otolith Sr:Ca ratio electron‐probe micro analysis (EPMA) for individual migratory histories revealed that 15 A. celebesensis caught in Poso Lake and its inlet rivers were categorized into 14 river eels (Sr:Ca < 2·5) showing upstream migration seemingly at their elver stage and only one sea eel (Sr:Ca ≥ 6·0) that stayed in the marine habitat for the majority of its life after recruiting to Sulawesi Island before its late upstream migration. In A. marmorata, 19 examined eels from Poso Lake and its inlet rivers were all river eels, while 17 eels from the lower reaches of Poso River were two river eels, six sea eels and nine estuarine eels (2·5 ≤ Sr:Ca < 6·0) that mostly lived in the brackish water. The sex ratio of A. celebesensis was highly skewed towards a dominance of females (99%). In A. marmorata, females were predominant in Poso Lake (95·2%), its inlet rivers (94·7%) and Laa River (100%), while males were more frequent in the lower reaches of Poso River (76·5%) and small inlet rivers of Tomini Bay (94·1%). These results indicate that the riverine distribution pattern of tropical eels differs among species and between sexes.     

A comprehensive hypothesis on the migration of European glass eels (Anguilla anguilla)

The European eel (Anguilla anguilla) is a catadromous fish that spawns in the Sargasso Sea. As larvae, eels cross the Atlantic Ocean and reach the continental slope of Europe, where they metamorphose into post‐larval glass eels. These reach the continent, where some enter fresh water, some remain in marine waters, and others move between fresh and marine waters. After 5–25 years, as adult silver eels, they migrate back from fresh water to the Sargasso Sea to spawn and die. The glass eel stage is a critical step during which the eels cross the continental shelf and recruit to estuaries, where they facultatively transition to fresh water. Extensive research has been conducted to understand the behavioural mechanisms and environmental cues that aid and guide glass eels' migration. Glass eels follow odours and salinity gradients, they avoid light, and they change orientation and depth according to the tides. Recent work revealed that European glass eels also use Earth's magnetic field and lunar cues to orient. However, while we understand many aspects of their orientation behaviour, a unifying theory describing how glass eels migrate from the continental slope to fresh water is lacking. The goal of this review is to develop a comprehensive hypothesis on the migration of European glass eels, integrating previous knowledge on their orientation behaviour with recent findings on magnetic and celestial orientation. This review follows the journey of a hypothetical glass eel, describing the nature and the role of orientation cues involved at each step. I propose that, although glass eels have the sensory capacity to use multiple cues at any given time, their migration is based on a hierarchical succession of orientation mechanisms dictated by the physical properties of the environments that they occupy: (i) lunar and magnetic cues in pelagic water; (ii) chemical and magnetic cues in coastal areas; and (iii) odours, salinity, water current and magnetic cues in estuaries.     

Karyological and gonadal sex of eels(Anguilla anguilla) from the German Bight and the lower River Elbe

Yellow eels(Anguilla anguilla) taken during summer from random commercial trapnet samples in the littoral area of Helgoland (n=116) and from a freshwater area of the River Elbe near Hamburg (n=109) were examined with regard to their karyological (i.e. existence of female sex chromosomes) and gonadal sex. In 47 % and 21 % of the two samples, respectively, chromosomes were unidentifiable because of insufficient numbers of mitotic plates. All eels from Helgoland, except one phenotypically undetermined fish, exhibited female gonads: 48 had female sex chromosomes and 13 were karyologically males. As found previously in the River Elbe, eels with male gonads predominated (n=55); 25 were undifferentiated. Of the gonadal males 26 were karyological males and 16 karyological females; the rest could not be identified by chromosome patterns. In contrast, all but one of the Elbe eels with female gonads (n=28) had female sex chromosomes. Some aspects of the sex reversal documented in the eel are considered.     

Thermal preferenda and behavior of Atlantic eels (genus Anguilla) in relation to their spawning migration

Synopsis The final preferred temperatures (FPTs) of adult premigratory and migratory life-history phases of American eels, Anguilla rostrata, were determined by chronic tests in a horizontal thermal gradient. Mean FPTs were between 17 and 20°C and were not significantly different between life-history phases, acclimation temperatures, illumination regimes, photoperiods or sexual maturation states. Thermal behavior of eels was highly variable, both among individuals of the various test groups and among repeated tests of single individuals. Light inhibited behavioral thermoregulation by promoting shelter-seeking. The following inferences are drawn from the laboratory findings and observations of migrating A. rostrata and A. anguilla (European eels) in the North Atlantic: (1) decreasing temperatures may initiate downstream migration of silver eels, (2) eels may select temperatures close to their FPT in thermally stratified environments, but will tolerate higher and lower temperatures depending on illumination or other physical constraints, (3) the oceanic phase of the migration to the Sargasso Sea may take place at relatively shallow depths in the open ocean, probably within the upper 1000 meters. The strong eurythermality observed in eels may facilitate their occupation of and migration through thermally diverse and unpredictable habitats.     

American eels produce and release bile acid profiles that vary across life stage

The American eel (Anguilla rostrata) is an imperilled fish hypothesized to use conspecific cues, in part, to coordinate long-distance migration during their multistage life history. Here, holding water and tissue from multiple American eel life stages was collected and analysed for the presence, profile and concentration of bile acids. Distinct bile acid profiles were identified in glass, elver, yellow eel and silver eel holding waters using ultraperformance liquid chromatography high-resolution mass spectrometry and principal component analysis. Taurochenodeoxycholic acid, taurodeoxycholic acid, cholic acid, deoxycholic acid, taurolithocholic acid and taurocholic acid were detected in whole tissue of American glass eels and elvers, and in liver, intestine and gallbladder samples of late-stage yellow eels. Bile acids were not a major component of silver eel washings or tissue. This study is novel because little was previously known about bile acids produced and emitted into the environment by American eels. Future behavioural studies could evaluate whether any bile acids produced by American eels influence conspecific migratory behaviour.     

How does salinity influence habitat selection and growth in juvenile American eels Anguilla rostrata?

The influence of salinity on habitat selection and growth in juvenile American eels Anguilla rostrata captured in four rivers across eastern Canada was assessed in controlled experiments in 2011 and 2012. Glass eels were first categorized according to their salinity preferences towards fresh (FW), salt (SW) or brackish water (BW) and the growth rate of each group of elvers was subsequently monitored in controlled FW and BW environments for 7 months. Most glass eels (78–89%) did not make a choice, i.e. they remained in BW. Salinity preferences were not influenced by body condition, although a possible role of pigmentation could not be ruled out. Glass eels that did make a choice displayed a similar preference for FW (60–75%) regardless of their geographic origin but glass eels from the St Lawrence Estuary displayed a significantly higher locomotor activity than those from other regions. Neither the salinity preferences showed by glass eels in the first experiment nor the rearing salinities appeared to have much influence on growth during the experiments. Elvers from Nova Scotia, however, reached a significantly higher mass than those from the St Lawrence Estuary thus supporting the hypothesis of genetically (or epigenetically) based differences for growth between A. rostrata from different origins. These results provide important ecological knowledge for the sustained exploitation and conservation of this threatened species.     

Estuarine habitat preferences of <Emphasis Type="Italic">Anguilla australis</Emphasis> and <Emphasis Type="Italic">A. reinhardtii</Emphasis> glass eels as inferred from laboratory experiments

We tested the habitat preferences of Anguilla australis (shortfin) and A. reinhardtii (longfin) glass eels using circular tanks in an aquarium, containing four types of estuarine habitat (sand, mud, rocks/cobbles and seagrass). Shortfin eels either showed a tendency to occur in heterogeneous habitats, or in rocks/cobbles. Longfin glass eels showed a significant preference for rocks/cobbles in both experiments. Tests on shortfin and longfin glass eels in tanks with only rocks/cobbles available showed that eels were not clumped, indicating that individuals select habitat for re-settlement independently. Therefore, we assumed that the uneven distribution of glass eels observed in the habitat type experiments were the result of habitat preference. Given a choice of habitats in tank experiments, shortfin and longfin glass eels preferred habitats containing structure, and in particular, rocks/cobbles.