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.     

The Distribution and Ecology of Ariosoma Balearicum (Congridae) Leptocephali in the Western North Atlantic

A total of 4589 leptocephali of the congrid eel, Ariosoma balearicum, were examined from 17 cruises in the western North Atlantic Ocean. Myomere counts made on 915 of these indicated there were two ranges of number of myomeres that appear to be associated with separate spawning populations. Those with the higher range (high count: 128–137) were consistently 70–100mm in length in the Sargasso Sea from February to April and 20–80mm in length in the northern Sargasso Sea and Gulf Stream from September to October. Those with the lower range (low count: 120–130) were rare in the northern and eastern Sargasso Sea where they had consistently greater lengths than high count leptocephali and were most abundant in the Florida Current and Providence Channel. The geographic distributions of size and myomere ranges in relation to hydrography provide strong support for the hypothesis that high count eels found along the South Atlantic Bight (SAB) migrate across the Florida Current to spawn in the northwest Sargasso Sea. This migratory pattern is similar to those of Anguilla rostrata and Conger oceanicus, which use the southern Sargasso Sea for development as larvae. However, the distribution of high count leptocephali suggests that they use the entire Sargasso Sea gyre as a development area as larvae before crossing the Florida Current and recruiting to the SAB. The low count eels inhabiting the Bahamas appear to spawn near the banks and their abundance in the Providence Channel and southwest Sargasso Sea suggests most are retained close to the Bahamas. These two distinct styles of spawning, distribution and recruitment of larvae are hypothesized to be related to the different hydrographic regimes of the two juvenile habitats and the resulting constraints on growth and recruitment of larvae. Vertebral and myomere counts reported from other areas suggest there are distinct populations in other regions of the North Atlantic Ocean.     

Qualitative assessment of the diet of European eel larvae in the Sargasso Sea resolved by DNA barcoding

European eels (Anguilla anguilla) undertake spawning migrations of more than 5000 km from continental Europe and North Africa to frontal zones in the Sargasso Sea. Subsequently, the larval offspring are advected by large-scale eastward ocean currents towards continental waters. However, the Sargasso Sea is oligotrophic, with generally low plankton biomass, and the feeding biology of eel larvae has so far remained a mystery, hampering understanding of this peculiar life history. DNA barcoding of gut contents of 61 genetically identified A. anguilla larvae caught in the Sargasso Sea showed that even the smallest larvae feed on a striking variety of plankton organisms, and that gelatinous zooplankton is of fundamental dietary importance. Hence, the specific plankton composition seems essential for eel larval feeding and growth, suggesting a linkage between eel survival and regional plankton productivity. These novel insights into the prey of Atlantic eels may furthermore facilitate eel larval rearing in aquaculture, which ultimately may replace the unsustainable use of wild-caught glass eels.     

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.     

Biometric studies on premetamorphic eel larvae ofAnguilla anguilla (Anguilliformes: Anguillidae) in comparison with younger developmental stages of the species

387 premetamorphic leptocephali of the familyAnguillidae caught off the west coast of Europe were examined taxonomically and compared with the youngest developmental stages of larvae ofAnguilla anguilla caught in the Sargasso Sea 1979 (Schoth, 1982). The total number of myomeres and the number of myomeres up to the third, opistonephritic blood vessel present features of this species which are significantly different from those of the larvae ofAnguilla rostrata and do not change during the whole larval phase. A combination of these two biometric features enables an infallible species identification of the AtlanticAnguilla larvae at all developmental stages. The number of predorsal and preanal myomeres, the preanal length and features of the head cannot be used for a distinction ofAnguilla larvae. One larva, 68.7 mm long, with 107 myomeres, and 44 myomeres to the opistonephritic blood vessel represents the hitherto southernmost record of anA. rostrata larva in the eastern North Atlantic.     

On the geographic distribution and migration of I- and II-group eel larvae as studied during the 1979 Sargasso Sea Expedition

During the 1979 Sargasso Sea Expedition, 423 larvae ofAnguilla anguilla and 5 larvae ofA. rostrata were caught on three Atlantic transects and two cruises in the Sargasso Sea. Results of the identification of the larvae by myomere counts, and limits of the occurrence of I- and II-group larvae are presented. Four standard fishing depths are compared. A range shallower than 25 m was found to be the optimal fishing depth by night for both larval length groups. The geographic distribution of length group I was observed in central and eastern North Atlantic. Available data indicate a migration of these larvae in a north easterly direction. Length measurements of the II-group larvae taken from catches on the European continental slope during the same expedition support this assumption.     

Influence of oceanic factors on Anguilla anguilla (L.) over the twentieth century in coastal habitats of the Skagerrak,southern Norway

The European eel (Anguilla anguilla L.) is distributed in coastal and inland habitats all over Europe, but spawns in the Sargasso Sea and is thus affected by both continental and oceanic factors. Since the 1980s a steady decline has been observed in the recruitment of glass eels to freshwater and in total eel landings. The eel is considered as critically endangered on the International Union for the Conservation of Nature and Natural Resources Red List of species. The Skagerrak beach seine survey from Norway constitutes the longest fishery-independent dataset on yellow/silver eels (starting in 1904). The Skagerrak coastal region receives larvae born in the Sargasso Sea spawning areas that have followed the Gulf Stream/North Atlantic Drift before they penetrate far into the North Sea. The Skagerrak coastal time series is therefore particularly valuable for exploring the impacts of oceanic factors on fluctuations in eel recruitment abundance. Analyses showed that Sargasso Sea surface temperature was negatively correlated with eel abundance, with a lag of 12 years revealing a cyclic and detrimental effect of high temperatures on the newly hatched larvae. The North Atlantic Oscillation index and inflow of North Atlantic water into the North Sea were negatively correlated with eel abundance, with a lag of 11 years. Increased currents towards the North Atlantic during high North Atlantic Oscillation years may send larvae into the subpolar gyre before they are ready to metamorphose and settle, resulting in low recruitment in the northern part of the distribution area for these years. The Skagerrak time series was compared with glass eel recruitment to freshwater in the Netherlands (Den Oever glass eel time series), and similar patterns were found revealing a cycle linked to changes in oceanic factors affecting glass eel recruitment. The recent decline of eels in the Skagerrak also coincided with previously documented shifts in environmental conditions of the North Sea ecosystem.     

Spawning ofConger oceanicus andConger triporiceps (Congridae) in the Sargasso Sea and subsequent distribution of leptocephali

Synopsis Distribution of leptocephali ofConger in the Western North Atlantic Ocean was studied using specimens from our collections, specimens from other collections, and various existing collection records. The presence of leptocephali ofConger oceanicus andConger triporiceps < 30 mm long over deep water in the southwestern Sargasso Sea in autumn and winter implies a protracted spawning period there. The subtropical convergence zone, meandering east-west across the Sargasso Sea, is probably the northern limit of spawning of both species. Spawning may also occur close to the Bahamas and Antilles.C. triporiceps may spawn also in the Caribbean Sea judging by the capture of small leptocephali in the western Caribbean and of the more southerly continental distribution of its juveniles. The claim of Johannes Schmidt in 1931 that the EuropeanC. conger spawns across the North Atlantic into the western Sargasso Sea is probably incorrect, because leptocephali ofConger are rare in the eastern Sargasso Sea and becauseC. triporiceps, with myomere numbers overlapping those ofC. conger, was recently described in the western North Atlantic. With increasing size, leptocephali ofC. oceanicus and a portion ofC. triporiceps spread westward and northward in the Florida Current and Gulf Stream, but larger leptocephali especially ofC. triporiceps are found also in the Caribbean and Gulf of Mexico. Spawning ofC. oceanicus in the Sargasso Sea indicates that adults cross the Florida Current-Gulf Stream, and successful leptocephali cross the current in the opposite direction to colonize juvenile habitat on the continental shelf, a migratory pattern similar to that of the American eelAnguilla rostrata (Anguillidae).     

Distribution of leptocephali of the freshwater eels,genus <Emphasis Type="Italic">Anguilla</Emphasis>, in the waters off west Sumatra in the Indian Ocean

A research cruise was conducted in the eastern Indian Ocean off west Sumatra, Indonesia, in June 2003 to learn about the spawning and larval ecology of the tropical freshwater eels of the genus Anguilla in the region. A total of 43 anguillid leptocephali were collected during the cruise and they were genetically identified as 41 Anguilla bicolor bicolor, 1 Anguilla marmorata, and 1 Anguilla interioris. A. bicolor bicolor leptocephali were 44.1–55.5 mm TL and most of them were at the fully grown stage. Reexamination of the historical data of Jespersen (1942) also suggested a relatively low abundance of small size leptocephali (<40 mm) of this species off west Sumatra. Although the study area has long been considered to be a spawning site of A. bicolor bicolor, the distributions of leptocephali from the two surveys and the patterns of ocean currents in the region suggest the possibility that the main spawning area of this species is located farther offshore.     

Assessing patterns of hybridization between North Atlantic eels using diagnostic single-nucleotide polymorphisms

The two North Atlantic eel species, the European eel (Anguilla anguilla) and the American eel (Anguilla rostrata), spawn in partial sympatry in the Sargasso Sea, providing ample opportunity to interbreed. In this study, we used a RAD (Restriction site Associated DNA) sequencing approach to identify species-specific diagnostic single-nucleotide polymorphisms (SNPs) and design a low-density array that combined with screening of a diagnostic mitochondrial DNA marker. Eels from Iceland (N=159) and from the neighboring Faroe Islands (N=29) were genotyped, along with 94 larvae (49 European and 45 American eel) collected in the Sargasso Sea. Our SNP survey showed that the majority of Icelandic eels are pure European eels but there is also an important contribution of individuals of admixed ancestry (10.7%). Although most of the hybrids were identified as F1 hybrids from European eel female × American eel male crosses, backcrosses were also detected, including a first-generation backcross (F1 hybrid × pure European eel) and three individuals identified as second-generation backcrosses originating from American eel × F1 hybrid backcrosses interbreeding with pure European eels. In comparison, no hybrids were observed in the Faroe Islands, the closest bodies of land to Iceland. It is possible that hybrids show an intermediate migratory behaviour between the two parental species that ultimately brings hybrid larvae to the shores of Iceland, situated roughly halfway between the Sargasso Sea and Europe. Only two hybrids were observed among Sargasso Sea larvae, both backcrosses, but no F1 hybrids, that points to temporal variation in the occurrence of hybridization.     

Vertical distributions, diel and ontogenetic vertical migrations and net avoidance of leptocephali of Anguilla and other common species in the Sargasso Sea

Day- and night-time vertical distributions and their ontogeneticchanges in Anguilla leptocephali and other common species ofleptocephali were determined and compared during five cruisesin the Sargasso Sea using an opening - closing 2-m ring netto sample discrete depth strata between 0 m and 350 m deep.No difference in vertical distribution was ever found betweenAnguilla rostrata (American eel) and A. anguilla (European eel).Anguilla leptocephali <5 mm long did not exhibit a diel verticalmigration, as they were distributed between 50 m and 300 m bothby day and by night. The vertical distribution of these smalllepto-cephali is probably roughly representative of the depthdistribution of adult spawning. Anguilla     

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.     

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.     

Inshore migration and otolith microstructure/microchemistry of anguillid glass eels recruited to Iceland

The timing of catches of anguillid glass eels and their otolith microstructure and microchemistry were studied in southwest Iceland, where the European eel, Anguilla anguilla and American eel, A. rostrata have been thought to live sympatrically, to learn about their early life history and the possible mechanism of the separation between these two species ranges. Catches at the site studied suggest that glass eels may have started upstream migration as the river temperature warmed in late June and early July. The glass eels were mitochondrially identified into two species, A. anguilla and A. rostrata, although the latter were likely hybrids between the two species based on a different study. Otolith analyses showed no sharp increases in otolith increment width or sharp decrease of otolith Sr:Ca ratio in either species, which are the characteristic changes corresponding to the onset of metamorphosis in many anguillid species including A. rostrata collected in North America and A. anguilla in Europe. The mean age at recruitment determined for the glass eels in Iceland were similar between the two species (336.6 ± 41.7 and 319.3 ± 36.0 days for A. anguilla and A. rostrata, respectively), as were their total lengths (range 58.0–78.5 mm and 58.5–73.0 mm). In addition, mean age at metamorphosis (278.0 ± 36.8 and 254.0 ± 47.7 days) and total age (372.3 ± 50.8 and 352.9 ± 42.6 days) were also similar between the two species. However, these ages of A. rostrata in Iceland were older than those in North America, and those of A. anguilla collected in Iceland were roughly intermediate between the rest of Europe and North Africa. These findings support the hypothesis that the timing of metamorphosis is a key factor for determining the place of recruitment of glass eels and maintaining the geographic separation between the two species.     

Comparison of electrophoretic and meristic characters of 0-group eel larvae from the Sargasso Sea

Marked differences between continental samples of American and European eels have been detected electrophoretically in allele frequencies at the MDH-2 locus. Starch gel electrophoresis carried out on board F. R. V. Anton Dohrn during the eel expedition to the Sargasso Sea in 1979 revealed a similar clear-cut genetic difference in a sample of 0-groupAnguilla leptocephali, thus confirming the classical theory of Schmidt (1932). The MDH-2 genotypes provide an additional diagnostic character for the distinction between youngA. anguilla andA. rostrata leptocephali. Species identification by biochemical genetic characters did not correspond with that by meristic characters (myomere numbers) in ca. 13 % of the specimens studied; this discrepancy mainly concerns leptocephali of theA. anguilla genotype. The results obtained are critically discussed.     

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.     

Length composition and abundance of eel larvae,Anguilla anguilla (anguilliformes: Anguillidae), in the iberian basin (northeastern Atlantic) during July–September 1984

376 leptocephali ofAnguilla anguilla (L., 1758) from the Iberian Basin were analysed. The observed horizontal trends of abundance and particularly the mean sizes contradict the expectations based on the hypothesis of larvae distribution exclusively by drift with Gulf and North Atlantic Currents, and support the hypothesis of an active larval migration also south of the Azores.     

Introduced American eels Anguilla rostrata in European waters: life‐history traits in a non‐native environment

This study investigated growth, condition and development of American eels Anguilla rostrata that were introduced into a European river to estimate their competitive potential in a non‐native habitat. Results demonstrate that A. rostrata develops normally in European waters and successfully competes with the native European eel Anguilla anguilla. In addition, A. rostrata appears to be more susceptible to the Asian swimbladder nematode Anguillicola crassus than A. anguilla and could support the further propagation of this parasite. Detected differences in fat content and gonad mass between Anguilla species are assumed to reflect species‐specific adaptations to spawning migration distances. This study indicates that A. rostrata is a potential competitor for the native fauna in European fresh waters and suggests strict import regulations to prevent additional pressure on A. anguilla and a potential further deterioration of its stock situation.     

A phylogeny of freshwater eels inferred from mitochondrial genes

The genus Anguilla Shaw of Family Anguillidae consists entirely of freshwater eels, including 15 species and 2 subspecies. Conventionally, variegated markings and the length of the dorsal fin are the major morphological features used for reconstruction of phylogenetic relationships. The evolutionary history of these species remains unclear, especially for the Atlantic eels, whose habitats are far from the Metropolis in the Indo-Pacific region. This study reexamined the phylogenetic relationships of 12 Anguilla species by sequencing of the cytochrome b and 12S rRNA genes. In our analysis, species bearing similar coloration patterns or dorsal fin morphology are not necessarily clustered in the same clade, indicating that these morphological features might be unstable or might have occurred independently in different lineages during evolution. Combining our molecular data and geographical evidence, we speculate that (1) Anguilla first radiated about 20 million years ago, (2) the ancestors of Atlantic eels did not migrate by drifting through the Tethys Seaway at the leptocephali stage but instead trekked across the Central American Isthmus to the Sargasso Sea for spawning at the adult stage, and (3) multiple radiation events had occurred at the Metropolis during Anguilla evolution.     

Occurrence of exotic eels in natural waters of South Korea

We surveyed the proportion of anguillid eel species inhabiting South Korea natural waters. From September 2014 to August 2015, 429 eels were collected in various habitats for identification using morphological features and DNA-based molecular methods. We found 424 Japanese eels (Anguilla japonica, 98.8%), two European eels (A. anguilla, 0.5%), one American eel (A. rostrata, 0.23%), one tropical eel (A. marmorata, 0.23%), and one short-finned eel (A. bicolor pacifica, 0.23%). Three (A. anguilla, A. rostrata, and A. bicolor pacifica) are exotic species to the natural waters of South Korea; this study is the first record of their distribution in this region. Specifically, A. anguilla was found in the Lake Soyang and Cheongpyeong, while A. rostrata was found only in the Lake Cheongpyeong, and A. bicolor pacifica was found in the Geum River estuary.