Swimming performance of silver eels is severely impaired by the swim-bladder parasite Anguillicola crassus

Infection with the swim-bladder parasite Anguillicola crassus is suggested as one of the principal causes of the collapse of the European eel population. This nematode has been introduced in Europe from Asia in the 80s and parasitized in a short time Anguilla eel species in different geographical regions across the globe. The parasites drain energy due to their sanguivorous feeding and they cause mechanical damage on the swim-bladder wall. These two effects are hypothesized to impair the spawning migration of the European eel. In this study, we have investigated both effects on swimming performance. We hypothesized that parasitic sanguivorous activities - related to parasite weight - reduce swimming endurance, while mechanical damage of the swim-bladder impairs buoyancy control. Eighty eels suffering various degrees of infection were introduced in swim-tunnels and subjected to a swimming fitness test. The relation between A. crassus infection and swimming efficiency was measured for large female silver eels swimming at various speeds. Infected eels had lower cruising speeds and a higher cost of transport. Eels without parasites, but with a damaged swim-bladder showed similar effects. Almost half of the eels that contained damaged swim-bladders (43%) stopped swimming at low aerobic swimming speeds (< 0.7 m/s). Simulated migration trials in a recent related study have confirmed that eels with a high parasite level or with damaged swim-bladder show early migration failure (< 1000-km). Reduced swimming performance appears to be associated with swim-bladder dysfunction. As we found that especially silver eels have much higher infection levels than yellow eels, it is concluded that migrating silver eels with severely infected or damaged swim-bladders are unable to reach the spawning grounds.     

Escapement success of silver eels from a German river system is low compared to management‐based estimates

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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.     

Relationship between European eel Anguilla anguilla infection with non‐native parasites and swimming behaviour on encountering accelerating flow

The effect of Anguillicola crassus, Pseudodactylogyrus bini and Pseudodactylogyrus anguillae infection on the behaviour of downstream migrating adult European eels Anguilla anguilla as they encountered accelerating water velocity, common at engineered structures where flow is constricted (e.g. weirs and bypass systems), was evaluated in an experimental flume. The probability of reacting to, and rejecting, the velocity gradient was positively related to A. crassus larval, adult and total abundance. High abundance of Pseudodactylogyrus spp. reduced this effect, but A. crassus was the strongest parasitic factor associated with fish behaviour, and abundance was positively related to delay in downstream passage. Delayed downstream migration at hydraulic gradients associated with riverine anthropogenic structures could result in additional energetic expenditure for migrating A. anguilla already challenged by A. crassus infection.     

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.     

Hematology patterns of migrating European eels and the role of EVEX virus

We show that European eels infected with the rhabdovirus EVEX (Eel Virus European X) virus, developed hemorrhage and anemia during simulated migration in large swim tunnels, and died after 1000-1500 km. In contrast, virus-negative animals swam 5500 km, the estimated distance to the spawning ground of the European eel in the Sargasso Sea. Virus-positive eels showed a decline in hematocrit, which was related to the swim distance. Virus-negative eels showed a slightly increased hematocrit. Observed changes in plasma lactate dehydrogenase (LDH), total protein and aspartate aminotransferase (AAT) are indicative of a serious viral infection. Based on these observations, we conclude that eel virus infections may adversely affect the spawning migration of eels, and could be a contributing factor to the worldwide decline of eel.     

Effects of the swimbladder parasite Anguillicola crassus on the migration of European silver eels Anguilla anguilla in the Baltic Sea

In a mark–recapture study in 2006, migrating European Anguilla anguilla silver eels were caught, tagged and released in the Baltic Sea and recaptures in commercial pound nets examined for possible effects on migration of infection with the swimbladder parasite Anguillicola crassus . The overall recapture rate was 36%. The prevalence of infection was lowest at the northernmost sampling site. There were no significant differences between infected and uninfected A. anguilla in condition indices, body fat content and estimated migration speeds. Parasite infection intensity levels were significantly negatively correlated with times and distances covered between release and recapture, but did not correlate with migration speed. It appears that more heavily infected A. anguilla were relatively more vulnerable to recapture in pound nets. It is hypothesized that parasite-induced damage to the swimbladder inhibited vertical migrations and infected A. anguilla tended to migrate in shallower coastal waters, relatively close to the shore.     

Effects of eel restocking on the distribution of the swimbladder nematode Anguillicola crassus in Flanders, Belgium

Data on the distribution in 1986 of the parasitic nematode in the swimbladder of the European eel (Anguilla anguilla L.) in Flanders (Belgium) are reported. In stations where imported eels have been used for restocking, samplings generally show high infection rates thus enhancing the spread of Anguillicola crassus in Flanders.     

Influence of Anguillicola crassus (Nematoda) and Ichthyophthirius multifiliis (Ciliophora) on swimming activity of European eel Anguilla anguilla

We investigated the swimming activity of 70 European eels Anguilla anguilla in relation to natural infection with 2 parasite species: the eel-specific swimbladder nematode Anguillicola crassus and the non-specific skin and gill protozoan Ichthyophthirius multifiliis. We measured how long individual eels exposed to a water current in a swimming channel with a steady-stream profile could withstand the water current. The parasites affected the swimming behaviour of eels in different ways. The maximum period of time the fish were able to swim against the current was not correlated with infection by A. crassus. In contrast, infection with I. multifiliis reduced the swimming time. The protozoan has a higher pathogenicity than the swimbladder nematode, at least in closed systems, where I. multifiliis is able to spread within a few days. Reduction in swimming capacity after infection with the ciliate averaged 47 % compared to capacity prior to infection. Thus, our results do not support the previously suggested strong negative relation between swimming activity of eels and intensity of A. crassus infection, at least in the short-term. However, there are indications in the literature that the pathological effects of A. crassus on the eel swimmbladder may involve a higher energy demand, possibly manifested in a prolonged spawning migration. As a result, eels heavily infected with this parasite may arrive too late at the spawning site to participate in mating. This could ensure a selection of 'good genes'.     

Are Lithuanian eels fat enough to reach the spawning grounds?

Stocks of the European eel Anguilla anguilla have been in a steep decline since the 1980s. Stocking of water bodies with juvenile eels captured in the wild to establish or enhance local populations has been a common practise in Europe for many decades. However, the degree of contribution by stocked eels to natural spawning capacity is poorly known and extensively debated. There have been suggestions that eels derived from stocking are less likely to contribute to the spawning stock due to a lack of navigational capability and lower fitness related to insufficiency of energetic resources. Results of the current study indicated that eels translocated long distances from the point of capture and released into inland waters in Lithuania are successfully undergoing the silvering process. A proportion of 23.7% (N = 27) among all migrating eels were described to be at the yellow (SI, SFII or SFIII) eel stage and downstream movements of these eels should be attributed to local movements, rather than spawning migration; 76.3% were assigned to the silver eel stage. This study suggests that 36.8% (N = 32) of downstream migrating silver eels of stocked origin had accumulated sufficient energetic resources for spawning migration and gonadal development and should be able to traverse the 7900-km distance to the presumptive spawning grounds in the Sargasso Sea. The rest of migrating silver eels (63.2%, N = 55) had insufficient energetic resources; the average potential swimming range of these eels was estimated to be 6135 ± 683 km.     

A century of research on the larval distributions of the Atlantic eels: a re‐examination of the data

The spawning areas of the Atlantic freshwater eels were discovered about a century ago by the Danish scientist Johannes Schmidt who after years of searching found newly hatched larvae of the European eel, Anguilla anguilla, and the American eel, Anguilla rostrata, in the southern Sargasso Sea. The discovery showed that anguillid eels migrate thousands of kilometers to offshore spawning areas for reproduction, and that their larvae, called leptocephali, are transported equally long distances by ocean currents to their continental recruitment areas. The spawning sites were found to be related to oceanographic conditions several decades later by German and American surveys from 1979 to 1989 and by a Danish survey in 2007 and a German survey in 2011. All these later surveys showed that spawning occurred within a restricted latitudinal range, between temperature fronts within the Subtropical Convergence Zone of the Sargasso Sea. New data and re‐examinations of Schmidt's data confirmed his original conclusions about the two species having some overlap in spawning areas. Although there have been additional collections of leptocephali in various parts of the North Atlantic, and both otolith research and transport modelling studies have subsequently been carried out, there is still a range of unresolved questions about the routes of larval transport and durations of migration. This paper reviews the history and basic findings of surveys for anguillid leptocephali in the North Atlantic and analyses a new comprehensive database that includes 22612 A. anguilla and 9634 A. rostrata leptocephali, which provides a detailed view of the spatial and temporal distributions and size of the larvae across the Atlantic basin and in the Mediterranean Sea. The differences in distributions, maximum sizes, and growth rates of the two species of larvae are likely linked to the contrasting migration distances to their recruitment areas on each side of the basin. Anguilla rostrata leptocephali originate from a more western spawning area, grow faster, and metamorphose at smaller sizes of <70 mm than the larvae of A. anguilla, which mostly are spawned further east and can reach sizes of almost 90 mm. The larvae of A. rostrata spread west and northwest from the spawning area as they grow larger, with some being present in the western Caribbean and eastern Gulf of Mexico. Larvae of A. anguilla appear to be able to reach Europe by entering the Gulf Stream system or by being entrained into frontal countercurrents that transport them directly northeastward. The larval duration of A. anguilla is suggested to be quite variable, but gaps in sampling effort prevent firm conclusions. Although knowledge about larval behaviour is lacking, some influences of directional swimming are implicated by the temporal distributions of the largest larvae. Ocean–atmosphere changes have been hypothesized to affect the survival of the larvae and cause reduced recruitment, so even after about a century following the discovery of their spawning areas, mysteries still remain about the marine life histories of the Atlantic eels.     

Anguillicola crassus infection in Anguilla rostrata from small tributaries of the Hudson River watershed, New York, USA

We studied the invasion of the exotic nematode parasite Anguillicola crassus in the American eel Anguilla rostrata using tributaries of the Hudson River estuary. Yellow-phase American eels were sampled from 6 tributaries, and their swim bladders were examined for nematode infection. Prevalence averaged 39% with an intensity of 2.4 nematodes per eel. Parasite distribution was not significant along a latitudinal gradient; on the other hand, physical barriers (dams and natural waterfalls) significantly reduced infections upstream. Urbanization may increase the susceptibility of eels to infection; we found significantly elevated infection rates when urbanized lands exceeded 15% of the tributary catchment area. Yellow-phase eel condition was not affected by parasite infection. The invasion of the entire Hudson River watershed is ongoing and therefore will continue to be a management concern. Further analysis of the parasite-host interaction in North America is warranted.     

A checklist of the protozoan and metazoan parasites of European eel (Anguilla anguilla): checklist of Anguilla anguilla parasites

A comprehensive literature review on prevalence and distribution of parasites of the European eel (Anguilla anguilla) in European waters was conducted to set a baseline for future trend analyses and biodiversity considerations. The resulting checklist compiled from peer reviewed journals as well as grey literature including scientific reports, conference contributions, PhD theses and own survey data includes all protozoan and metazoan parasites of the European eel from freshwater, brackish and marine habitats. Parasites are arranged according to phylum and family. Species within families are listed alphabetically. Infected host organs, recorded habitats, localities, countries and literature citations are provided for each species. A total of 161 parasite species ? taxa from 30 countries are listed. With the trypanorhynch cestode Tentacularia coryphaenae a new host record could be documented. Furthermore, three new locality records of parasitic nematodes could be added based on own survey data: Anisakis simplex from an eel caught in the Baltic Sea, Eustrongylides mergorum for German freshwaters, and Goezia anguillae from the Tagus estuary in Portugal. Special consideration was given to the distribution of the swimbladder nematode Anguillicola crassus. A map and table of first reported records of this neozoan parasite species for 25 countries as well as a survey map indicating all published localities documented in the checklist are provided.     

Silver eel,Anguilla anguilla (Linnaeus, 1758), migration patterns in lowland rivers and lagoons in the North‐Eastern region of their distribution range

Escapement success and migration patterns of silver eels Anguilla anguilla (L.) was studied by acoustic telemetry in three natural free‐flowing and one dammed river and in Curonian Lagoon in Lithuania. Mean downstream migration speed and escapement success were almost the same in the shorter 210 km dammed river (52%, 13.6 km/day) and the considerably longer 300–480 km free‐flowing rivers (53%, 10.7 km/day). Despite the similarity between migration speed in the Curonian Lagoon (14.6 km/day) to that in rivers, migration success was significantly higher (71%) in the Lagoon. Although a majority of silver eels in Lithuania start migrating downstream in spring, the peak of eel migration into the Baltic Sea was observed during late fall. Overall migration success in the rivers and the Lagoon was 35%. Relatively low escapement may have negative consequences on the success on eel stock restoration and must be addressed when strategically planning for the production of spawners.     

Migrating silver eels return from the sea to the river of origin after a false start

The European eel''s singular spawning migration from European waters towards the Sargasso Sea remains elusive, including the early phase of migration at sea. During spawning migration, the movement of freshwater resident eels from river to sea has been thought to be irreversible. We report the first recorded incidents of eels returning to the river of origin after spending up to a year in the marine environment. After migrating to the Baltic Sea, 21% of the silver eels, tagged with acoustic transmitters, returned to the Narva River. Half returned 11–12 months after moving to the sea, with 15 km being the longest upstream movement. The returned eels spent up to 33 days in the river and migrated to the sea again. The fastest specimen migrated to the outlet of the Baltic Sea in 68 days after the second start—roughly 1300 km. The surprising occurrence of returning migrants has implications for sustainable management and protection of this critically endangered species.     

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.     

Environmental cues and extended estuarine residence in seaward migrating eels (Anguilla australis)

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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.     

Timing and pattern of annual silver eel migration in two European watersheds are determined by similar cues

Many animals perform long‐distance migrations in order to maximize lifetime reproductive success. The European eel migrates several thousand kilometers between their feeding habitats in continental waters (fresh‐, brackish, and sea water) and their spawning area in the Sargasso Sea. Eels residing in freshwaters usually initiate their spawning migration as silver eels during autumn, triggered by diverse environmental cues. We analyzed the time series of silver eel downstream migration in Burrishoole, Ireland (1971–2015), and Imsa, Norway (1975–2015), to examine factors regulating the silver eel migration from freshwater to the sea. The migration season (90% of the run) generally lasted from 1 August to 30 November. Environmental factors acting in the months before migration impacted timing and duration of migration, likely through influencing the internal processes preparing the fish for migration. Once the migration had started, environmental factors impacted the day‐to‐day variation in number of migrants, apparently stimulating migration among those eels ready for migration. Both the day‐to‐day variation in the number of migrants and the onset of migration were described by nearly identical models in the two rivers. Variables explaining day‐to‐day variation were all associated with conditions that may minimize predation risk; number of migrants was reduced under a strong moon and short nights and increased during high and increasing water levels. Presence of other migrants stimulated migration, which further indicates that silver eel migration has evolved to minimize predation risk. The onset of migration was explained mainly by water levels in August. The models for duration of the migration season were less similar between the sites. Thus, the overall migration season seems governed by the need to reach the spawning areas in a synchronized manner, while during the actual seaward migration, antipredator behavior seems of overriding importance.