All roads lead to home: panmixia of European eel in the Sargasso Sea

European eels (Anguilla anguilla) spawn in the remote Sargasso Sea in partial sympatry with American eels (Anguilla rostrata), and juveniles are transported more than 5000 km back to the European and North African coasts. The two species have been regarded as classic textbook examples of panmixia, each comprising a single, randomly mating population. However, several recent studies based on continental samples have found subtle, but significant, genetic differentiation, interpreted as geographical or temporal heterogeneity between samples. Moreover, European and American eels can hybridize, but hybrids have been observed almost exclusively in Iceland, suggesting hybridization in a specific region of the Sargasso Sea and subsequent nonrandom dispersal of larvae. Here, we report the first molecular population genetics study based on analysis of 21 microsatellite loci in larvae of both Atlantic eel species sampled directly in the spawning area, supplemented by analysis of European glass eel samples. Despite a clear East-West gradient in the overlapping distribution of the two species in the Sargasso Sea, we only observed a single putative hybrid, providing evidence against the hypothesis of a wide marine hybrid zone. Analyses of genetic differentiation, isolation by distance, isolation by time and assignment tests provided strong evidence for panmixia in both the Sargasso Sea and across all continental samples of European eel after accounting for the presence of sibs among newly hatched larvae. European eel has declined catastrophically, and our findings call for management of the species as a single unit, necessitating coordinated international conservation efforts.     

Natural selection influences AFLP intraspecific genetic variability and introgression patterns in Atlantic eels

Investigating patterns of genetic variation in hybridizing species provides an opportunity to understand the impact of natural selection on intraspecific genetic variability and interspecific gene exchange. The Atlantic eels Anguilla rostrata and A. anguilla each occupy a large heterogeneous habitat upon which 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 within species and introgressive hybridization in Icelandic eels has never been assessed. We revisited amplified fragment length polymorphism data collected previously using population genomics and admixture analyses to test if (i) genetic variation could be influenced by non-neutral mechanisms at both the intra- and interspecific levels, and if (ii) selection could shape the spatio-temporal distribution of Icelandic hybrids. We first found candidate loci for directional selection within both species. Spatial distributions of allelic frequencies displayed by some of these loci were possibly related with 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, we identified outlier loci at the interspecific level. Non-neutral introgression was strongly suggested for some of these loci. We detected a locus at which 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, supporting the hypothesis that differential survival of admixed genotypes partly explains the spatio-temporal pattern of hybrid abundance previously documented in Iceland.     

The swimbladder nematode Anguillicola crassus in the European eel Anguilla anguilla and the Japanese eel Anguilla japonica: differences in susceptibility and immunity between a recently colonized host and the original host

The swimbladder nematode Anguillicola crassus originates from Asia where it is a parasite of the Japanese eel Anguilla japonica. After its introduction to Europe about 25 years ago, the parasite spread rapidly within the indigenous populations of the European eel Anguilla anguilla and subsequently the prevalence and mean intensity appeared to stabilize. Under experimental and aquaculture conditions the na?ve new host appears to be more susceptible to A. crassus compared to the original host. Both eel species develop a immune response against A. crassus. The antibody response is well characterized for the European eel, but poorly characterized for the Japanese eel. It remains unclear if antibodies have any protective function against A. crassus. Encapsulation of larvae of A. crassus can be observed in naturally infected European eels. However, encapsulation of larvae following experimental infection has not been detected in European eels, but only in Japanese eels. Reinfection experiments and intraperitoneal injection of A. crassus homogenates failed to demonstrate the development of acquired immunity in European eels. Immunization with irradiated third stage larvae provided preliminary evidence for acquired immunity against A. crassus in the Japanese eel, but not in the European eel.     

Conclusive evidence for panmixia in the American eel

Eels are unique species in the biological world. The two North Atlantic eel species, the American eel (Anguilla rostrata) and the European eel (A. anguilla), occupy a broad range of habitats from the Caribbean to Greenland in the western Atlantic and from Morocco to Iceland in the eastern Atlantic, respectively. North Atlantic eels have a catadromous life cycle, spawning only in the Sargasso Sea and spending the majority of their lives in continental (fresh, brackish and coastal) waters. Despite such a wide distribution range, North Atlantic eels have been regarded as a textbook example of panmictic species. In contrast with the large amount of population genetic studies testing the panmixia hypothesis in the European eel, a relatively modest effort has been given to study the population structure of the American eel. In this issue of Molecular Ecology, Côté et al. ( 2013 ) present the most comprehensive American eel data set to date, which includes samples of different life stages obtained throughout all its distribution range in North America. Results show a total lack of genetic differentiation among samples and provide decisive evidence for panmixia in the American eel.     

The eels of Lake Kariba: distribution, taxonomic status, age, growth and density

It had been predicted that eels would disappear from Lake Kariba because juveniles would be unable to surmount the dam which was closed in 1958. This prediction has been proved wrong. In 1970–71 an abundant population of eels was discovered in the lake, mostly at depths from 25–40 m. The eels have intermingled characters of both the mottled Anguilla nebulosa labiata and the plain-colored A. mossambica . A clear separation of these two taxa was impossible and therefore conspeciflc status of these two species is suspected; the name A. n. labiata is retained for the population.
The age structure of the eel cohorts suggests that juveniles surmount the dam in their second year of life and then spend approximately 7 years in streams of the lake drainage. The fastest maturing individuals which are in best condition then emigrate to the ocean, whereas the slower maturing eels remain in the lake longer. The oldest eel in the samples was 18 years old.
The catch per unit of effort for hoopnets was 2.35 kg in the upper part of the lake and 0.41 kg for the lower part of the lake. The density at Namazambwe was assessed at 46 eels per 1 ha. The unexploited eel population of Lake Kariba could form a valuable resource.     

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.     

Migratory patterns and contribution of stocking to the population of European eel in Lithuanian waters as indicated by otolith Sr:Ca ratios

Otolith Sr:Ca ratios were examined to evaluate the contribution of the stocked eel Anguilla anguilla elvers, which have been stocked in Lithuanian waters and mixed with naturally recruited eels for several decades, to the native eel population. Stocked eels were identified by the freshwater signature (Sr:Ca ratios <2·24 × 10⁻³) on the otolith after the glass eel stage. Naturally recruited eels, that had migrated through the North and Baltic Seas, were characterized by an extended seawater and brackish-water signature (Sr:Ca ratios >3·23 × 10⁻³) after the glass eel stage. Of 108 eels analysed, 21 eels had otolith Sr:Ca ratio profiles consistent with stocking while 87 showed patterns of natural recruitment. The ages of naturally recruited eels arriving in Lithuanian fresh waters varied from 1 to 10 years, with a mean ±  s.d . age of 5·2 ± 2·1 years. Eels from the inland Lake Baluošai were all freshwater residents of stocked origin. Stocked eels, however, accounted for only 20% of the eels from the Curonian Lagoon and 2% of eels sampled in Baltic coastal waters. This finding does not support the hypothesis that the eel fishery in the Curonian Lagoon depends mostly on stocking.     

Consumption, abundance and habitat use of Anguilla anguilla in a mesotrophic reservoir

The role of the eel Anguilla anguilla as a piscivorous species was investigated in a biomanipulation experiment in the mesotrophic Saidenbach Reservoir. The distribution and abundance of the eels were investigated by point abundance sampling, snorkelling and scuba diving. Also, the total yearly consumption of the eel population was compared with the standing stock of prey fishes and the production of roach Rutilus rutilus eggs. A restricted availability of shelter habitats at low water levels had no influence on the distribution of the eels during the nocturnal activity period. Fishes were consumed in low numbers but in high proportions of biomass by large eels. The maximum estimate of the annual consumption of the prey fish standing stock by the eels was 19%. Fish eggs were consumed during a small time period by a large proportion of the eels but the total consumption was <10% of the total annual production of roach eggs. By consuming small individuals of planktivorous fishes, the eels contribute to the biomanipulation programme in the Saidenbach Reservoir.     

Distribution of genetic variation in farmed and natural stocks of european eel

European eel ( Anguilla anguilla ; Teleostei) is a valuable commercial species. However, over the past 25 years, the population of European eel has been declining to such a degree that major concerns have been raised for its long‐term conservation. Since little information is available on the life‐cycle and genetic structure of European eel, it has been difficult to evaluate the existence of any population substructuring. Molecular genetic methods contribute to a better knowledge of the demography and population structure in marine fish. In addition, management strategies and conservation goals must consider information on genetic substructuring as well as on life history patterns.
The aim of the study is to provide more detailed knowledge on the genetic variability, demography and population substructuring of European eel by analysing and comparing natural and farmed individuals. Natural eel samples have been obtained in two geographical sites (Netherlands, France) including temporal samples in a short‐scale (within years) and a long‐scale (between years). Simultaneously, farmed glass eels have been grown in two separate batches during one year. Batches have been monitored and genetic samples have been obtained during the year.
A combination of selection‐sensitive (allozymes) and selection‐neutral markers (microsatellites) has been used in the study since selection seems to play an important role in the determination of the quality of future eel spawners. Results suggest a positive correlation between growth and genetic variability since individuals attaining a large length and mass present significant higher heterozygosities.     

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.     

Random amplified polymorphic DNA analysis of eel genome

Eel family is a huge one, in which many kinds of eels especially some migratory eels, bear strong resemblance to each other, and are therefore difficult to be identified. In this study 29 random primers were used to make RAPD analysis for Japaneses eel (Anguilla japonica), European eel (Anguilla anguilla) and Pike eel (Muraenesox cinereus).And totally 299 fragments were counted.Shared or specific fragments were counted and genetic similarity or genetic distance were calculated.The genetic similarity between Japanese eel and Pike eel is 0.68 and the genetic distance between them is 0.32;those between European eel and Pike eel are 0.72 and 0.28 respectively,and between Japanese eel and European eel are 0.74 and 0.25 respectively.The method has been shown to be suitable to molecular identification of eels.It provides an alternative approach to determine the relationship between species.     

Decline of North Atlantic eels: a fatal synergy?

Panmictic species pose particular problems for conservation because their welfare can be addressed effectively only on a global scale. We recently documented by means of microsatellite analysis that the European eel (Anguilla anguilla) is not panmictic but instead shows genetic isolation by distance. In this study, we extended the analysis to the American eel (A. rostrata) by applying identical analytical procedures and statistical power. Results obtained for the American eel were in sharp contrast with those obtained for the European eel: the null hypothesis of panmixia could not be rejected, and no isolation by distance was detected. This implies that the species must be managed as a single population. Using Bayesian statistics, we also found that the effective population sizes for both species were surprisingly low and that the populations had undergone severe contractions, most probably during the Wisconsinan glaciation. The apparent sensitivity of eels to climatic changes affecting the strength and position of the Gulf Stream 20,000 years ago is particularly worrying, given the effects of the ongoing global warming on the North Atlantic climate. Moreover, additional short-term stresses such as surging glass eel prizes, overfishing and lethal parasitic infections negatively affect eel population size. The fascinating transatlantic migration and life cycle of Atlantic eels is also their Achilles' heel as these negative short- and long-term effects will probably culminate in a fatal synergy if drastic conservation measures are not implemented to protect these international biological resources.     

Growth of European eel Anguilla anguilla along the southern Baltic coast of Germany and implication for the eel management

To detect growth differences of European eel Anguilla anguilla along the southern German Baltic coast 728 yellow eels, with total lengths ranging from 256 to 944 mm and ages ranging from 3 to 15 years were collected from six coastal areas from 2005 to 2009. The estimation of the growth performance was based on the otolith increments. The mean growth rate of the female yellow eels varied from 56 to 62 mm?year^–1. No significant differences in the mean growth rate were detected between eels from inner and open coastal areas. The overall mean annual increment of eels was estimated at 59 mm?year^?1. Specific growth rates (SGR) of female yellow eels decreased with increasing age from 0.68 %?day^?1 in the first year to 0.05 %?day^?1 in the tenth year. Results indicate that no separation is needed in the development of population models or management initiatives based on the growth performance of eel in inner and open coastal waters of the southern German Baltic coast.     

Taxonomic revision,ecology and endangerment categorization of the Andean catfish Astroblepus ubidiai (Teleostei: Astroblepidae)

The European eel (Anguilla anguilla Linnaeus 1758) is a species typical for waters of Western Europe. Thanks to early expeditions on the Atlantic Ocean by the Danish biologist Johannes Schmidt who found small (<10mm) leptocephali larvae in the Sargasso Sea about 100 years ago, we have now a strong indication where the spawning site for this species is located. The American eel (Anguilla rostrata, LeSueur) also spawns in the Sargasso Sea. The spawning time and location of both species have been supported and refined in recent analyses of the available historical data. Subsequent ichthyoplankton surveys conducted by McCleave (USA) and Tesch (Germany) in the 1980s indicated an increase in the number of leptocephali <10 mm , confirming and refining the Sargasso Sea theory of Johannes Schmidt. Distinctions between the European and American eel are based on morphological characteristics (number of vertebrae) as well as molecular markers (allozymes, mitochondrial DNA and anonymous genomic-DNA. Although recognised as two distinct species, it remains unclear which mechanisms play a role in species separation during larval drift, and what orientation mechanism eels use during migration in the open sea. The current status of knowledge on these issues will be presented. The hypothesis that all European eel migrate to the Sargasso Sea for reproduction and comprise a single randomly mating population, the so called panmixia theory, was until recently broadly accepted. However, based on field observations, morphological parameters and molecular studies there are some indications that Schmidt’s claim of complete homogeneity of the European eel population and a unique spawning location may be an overstatement. Recent molecular work on European eel indicated a genetic mosaic consisting of several isolated groups, leading to a rejection of the panmixia theory. Nevertheless, the latest extensive genetic survey indicated that the geographical component of genetic structure lacked temporal stability, emphasising the need for temporal replication in the study of highly vagile marine species. Induced spawning of hormone treated eels in the aquarium was collective and simultaneous. In this work for the first time group spawning behaviour has ever been observed and recorded in eels. Studies in swim-tunnels indicate that eels can swim four to six times more efficiently than non-anguilliform fish such as trout. After a laboratory swim trial of eels over 5,500 km, the body composition did not change and fat, protein and carbohydrate were used in the same proportion. This study demonstrated for the first time that European eel are physiologically able of reaching the Sargasso Sea without feeding. Based on catches of newly hatched larvae, temperature preference tests and telemetry tracking of mature hormone treated animals, it can be hypothesised that spawning in the Sargasso Sea is collective and simultaneous, while presumably taking place in the upper 200 m of the ocean. Successful satellite tracking of longfin female eels in New Zealand has been performed to monitor migration pathways. Implementation of this new technology is possible in this species because it is three times larger than the European eel. In the future, miniaturisation of tagging technology may allow European eels to be tracked in time by satellite. The most interesting potential contribution of telemetry tracking of silver eels is additional knowledge about migration routes, rates, and depths. In combination with catches of larvae in the Sargasso Sea, it may elucidate the precise spawning locations of different eel species or groups. Only then, we will be able to define sustainable management issues by integrating this novel knowledge into spawners escapement and juvenile fishing quota.     

The leucocyte enzyme cytochemistry of the Indian eel, Anguilla bicolor bicolor McClelland

Activity of peroxidase, alkaline phosphatase, acid phosphatase, α-naphthyl acetate esterase and naphthol-AS-D chloroacetate esterase in the leucocytes of the Indian eel, Anguilla bicolor bicolor McClelland, was studied. But for some minor differences, the enzyme pattern of the leucocytes, especially neutrophil peroxidase, of the Indian eel closely resembled that of the New Zealand eels, suggesting that the Indian eel is phylogenetically more closely allied to the New Zealand eels than to the European eel.     

Size selectivity of fyke nets for European eel Anguilla anguilla

Size selectivity of fyke nets for European eels Anguilla anguilla was investigated by reviewing the results of published experimental studies. A general size selectivity model was then derived that can be easily incorporated into demographic models to simulate population dynamics, assess and monitor abundance and length structure of eel stocks and forecast the consequences of different management options.     

Differential effects of origin and salinity rearing conditions on growth of glass eels of the American eel Anguilla rostrata: implications for stocking programmes

In this study, growth patterns were monitored in controlled fresh and brackish water (BW) conditions for 7 months during Anguilla rostrata glass eel and elver stages. Null hypotheses tested were that there is no significant difference in growth between glass eels (1) collected from two geographic regions typified by different sex ratios, (2) reared in fresh and BW and (3) due to origin × salinity interactions. It was found that young A. rostrata from Mira River (MR, Cape Breton, Nova Scotia, Canada, an area where both males and females occur) grew faster than those from Grande-Rivière-Blanche (Québec, Canada, an area where population are highly skewed towards females; 99–100%). Anguilla rostrata from both origins also grew faster in BW, although there was a trend for origin × salinity interactions whereby this effect was more pronounced for fish from the MR. The results support the hypothesis that salinity can influence growth patterns, as possibly can quantitative genetic differences between A. rostrata glass eels from different origins. Possible explanations for these patterns and potential consequences for sex determination and translocation programmes are discussed.     

Oceanic fronts in the Sargasso Sea control the early life and drift of Atlantic eels

Anguillid freshwater eels show remarkable life histories. In the Atlantic, the European eel (Anguilla anguilla) and American eel (Anguilla rostrata) undertake extensive migrations to spawn in the oceanic Sargasso Sea, and subsequently the offspring drift to foraging areas in Europe and North America, first as leaf-like leptocephali larvae that later metamorphose into glass eels. Since recruitment of European and American glass eels has declined drastically during past decades, there is a strong demand for further understanding of the early, oceanic phase of their life cycle. Consequently, during a field expedition to the eel spawning sites in the Sargasso Sea, we carried out a wide range of dedicated bio-physical studies across areas of eel larval distribution. Our findings suggest a key role of oceanic frontal processes, retaining eel larvae within a zone of enhanced feeding conditions and steering their drift. The majority of the more westerly distributed American eel larvae are likely to follow a westerly/northerly drift route entrained in the Antilles/Florida Currents. European eel larvae are generally believed to initially follow the same route, but their more easterly distribution close to the eastward flowing Subtropical Counter Current indicates that these larvae could follow a shorter, eastward route towards the Azores and Europe. The findings emphasize the significance of oceanic physical–biological linkages in the life-cycle completion of Atlantic eels.     

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.