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.     

Distribution and prevalence of Anguillicola crassus in eels from the tidal Thames catchmentb

Data gathered between 1988 and 1992 document the spread of the parasitic nematode Anguillicola crassus among eels in the tidal Thames catchment. Eel samples revealed a parasite prevalence ranging between 12 and 32% with a variation in intensity of infection of between one and five nematodes per infected host. Differences in the salinity regime between sampling points may be linked to the range of levels of infection in eels because of the saline tolerance limits of parasite developmental stages. The euryhaline teleost, the smelt ( Osmerus eperlanus ) found throughout the tidal river has been shown by others to be able to transfer nematode larval stages experimentally to large eels. Smelt found in the tidal Thames thus could possibly act as a further intermediate host to the eel population. The results support the theories proposed by previous workers that the parasite originally entered the tidal Thames via the commercial trade in live eels.     

The life cycle of Paraquimperia tenerrima: a parasite of the European eel Anguilla anguilla

Previous studies on the life history of the nematode eel specialist Paraquimperia tenerrima (Nematoda: Quimperiidae) have failed to determine whether an intermediate host is required in the life cycle. In the laboratory, eggs failed to hatch below 10 degrees C, hatching occurring only at temperatures between 11 and 30 degrees C. Survival of the free-living second stage larvae (L2) was also temperature dependent, with maximal survival between 10 and 20 degrees C. Total survival of the free-living stages (eggs and L2) is unlikely to exceed a month at normal summer water temperatures, confirming that parasite could not survive the 6 month gap between shedding of eggs in spring and infection of eels in early winter outside of a host. Eels could not be infected directly with L2, nor could a range of common freshwater invertebrate species. Third stage larvae (L3) resembling P. tenerrima were found frequently and abundantly in the swimbladder of minnows Phoxinus phoxinus from several localities throughout the year and were able to survive in this host in the laboratory for at least 6 months. Third stage larvae identical to these larvae were recovered from minnows experimentally fed L2 of P. tenerrima, and eels infected experimentally with naturally and experimentally infected minnows were found to harbour fourth stage larvae (L4) and juvenile P. tenerrima in their intestines. Finally, the whole life cycle from eggs to adult was completed in the laboratory, confirming that minnows are an obligate intermediate host for P. tenerrima.     

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.     

First record of Anguillicoloides crassus (Nematoda) in American eels (Anguilla rostrata) in Canadian estuaries, Cape Breton, Nova Scotia

In the summer of 2007, American eels, Anguilla rostrata, from 2 localities on Cape Breton Island, were found to be infected with the swim bladder nematode Anguillicoloides crassus. This is the first documented report of this highly invasive parasite in Canadian waters. More than half of the yellow eels in Mira River (6 of 10), and 1 eel (of 5) from Sydney Harbour were infected. Parasite intensity ranged from 1 to 11 worms per eel. The occurrence of A. crassus at these 2 localities suggests the need for a more extensive survey on the distribution of this exotic parasite in eel populations throughout Cape Breton Island.     

Effect of salinity on hatching, survival and infectivity of Anguillicola crassus (Nematoda: Dracunculoidea) larvae

The effect of salinity on hatching, larval survival and infectivity of Anguillicola crassus was studied under experimental conditions using eggs obtained from naturally infected eels. Egg hatching rate, second-stage larval survival and larval infectivity were maximal in fresh water and declined with increase in salinity. Larvae survived up to 100 d in fresh water, 70 d in 50 % sea water and 40 d in 100% sea water. Infectivity experiments demonstrated that salinity influenced transmission success throughout the life cycle by decreasing total infectivity of the larval population in utero within female A. crassus and when larvae were free-living in the aquatic environment. Infectivity was age-dependent in relation to salinity. Larvae were infective to intermediate and paratenic hosts for up to 80 d in fresh water, 21 d in 50% sea water and up to 8 d in 100% sea water. The data confirm field observations that infection levels decrease with an increase in salinity. The study contributes to experimental verification of the colonization abilities of A. crassus and supports the hypothesis that A. crassus can be disseminated and transmitted in brackish water. The importance of regular monitoring and stringent hygiene practices in the transportation of eels is emphasized.     

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.     

Anguillicola crassus (Nematoda, Dracunculoidea); first documented record of this swimbladder parasite of eels in Ireland

In summer 1998 European eels infected with the swimbladder nematode Anguillicola crassus were detected in the Erne catchment, Ireland, probably introduced recently through the commercial eel trade.     

Are eels (Anguilla anguilla L.) planktonic feeders? Evidence from parasite communities

The metazoan parasite communities of eels Anguilla anguilla were investigated in three riverine localities and one lake in Devon. Altogether 21 species of parasite, the majority of the British eel parasite fauna, were recorded. Parasite communities in the three riverine localities were more similar to each other than to that of the lake. The four parasite component communities were typical and representative of those from eels in other parts of the U.K. They were characterized by low species diversity and domination by a single species: Pseudodacytlogyrus anguillae in the rivers and Diplostomum spathaceum in the lake. Both the dominant species and the majority of parasite species, and hence individuals, in any locality infected eels directly by free swimming planktonic larval stages or indirectly by the ingestion of infected planktonic copepod intermediate hosts. Examination of other species of fish in each locality showed that only Raphidascaris acus utilized a fish species as an intermediate or paratenic host to infect eels. Increases in prevalence and intensity of infection with size of eel by helminths such as Camallanus lacustris and Paraquimperia tenerrima were observed in localities in which transmission of these parasites could not have involved another fish species. Over 63% of the specialist, specific parasites of eels throughout Europe employ planktonic transmission to their hosts, as do several species of the commoner generalists. A study of eel parasite communities thus leads to the conclusion that eels are widely and closely associated in their habits with plankton and that eels of all sizes feed regularly upon planktonic copepods: the widely accepted view of eels as being more or less exclusively benthic in habit and feeding behaviour requires re-appraisal.     

Development of Anguillicola crassus (Dracunculoidea, Anguillicolidae) in experimentally infected Balearic congers Ariosoma balearicum (Anguilloidea, Congridae).

The development of Anguillicola crassus in experimentally infected Ariosoma balearicum (Anguilloidea, Congridae) kept in seawater was studied in the laboratory. In parallel trials the effect of water salinity on the development of larval A. crassus in European eels Anguilla anguilla was also investigated using eels kept in seawater of a salinity of 34 per thousand. Both eel species were orally inoculated with L3 larvae of A. crassus and then maintained for up to 3 mo at 18 degrees C in seawater. 110 d post infection, no adult but larval (L3 and L4) stages of A. crassus were detected in the swimbladder wall of Balearic congers, although this period of time was sufficient for the parasites to develop to the adult stage in European eel kept in seawater. The results presented suggest that the definitive host specificity of A. crassus comprises species of the family Anguillidae (i.e. the genus Anguilla), but not members of the Congridae. Theoretically however, A. balearicum might serve as a metaparatenic host. Factors determining the definitive host range of A. crassus remain to be elucidated. Water salinity does not seem to act as a factor affecting definitive host specificity once the parasite has become ingested by the eel.     

Occurrence of Anguillicola crassus (Nematoda: Dracunculoidea) in Japanese eels Anguilla japonica from a river and an aquaculture unit in SW Taiwan

The infection by swimbladder nematodes of the genus Anguillicola (Dracunculoidea: Anguillicolidae) was examined in 2 populations of the Japanese eel Anguilla japonica in SW Taiwan. Wild eels from the Kao-Ping river were compared with cultured eels from an adjacent aquaculture unit. Only the cosmopolitan species Anguillicola crassus was present. Among wild eels, prevalence of infection varied between 21 and 62%, and mean intensity between 1.7 and 2.7 for adult worms. Similar intensity values (1.3 to 2.8) were recorded for the larvae. In cultured eels, prevalence as well as mean intensities were higher. In the cultured hosts, mean larval intensities exceeded those of adult worms 2-fold, and maximum larval intensities were 4- to 5-fold higher than in eels from the river. In cultured eels, dead larvae were also more abundant than in wild eels. We conclude that infrapopulations of A. crassus in Japanese eels are regulated by the defense system of this host, intraspecific density-dependent regulation being less likely as the major regulatory mechanism. No influence of the parasite on eel condition was found in either wild or cultured eels, indicating a low or moderate pathogenic effect of A. crassus on this host. This study shows that A. crassus is moderately common in cultured and wild Japanese eels in Taiwan, where the parasite is endemic.     

Spatio-temporal dynamics of the parasitic nematode Anguillicola crassus in Flanders, Belgium

Despite Egusa's earlier warning of the damage that the parasitic nematode Anguillicola crassus could inflict on the European eel Anguilla anguilla, its introduction in Europe was a fact in the early 1980s. Based on an elaborate dataset on Anguillicola crassus infection of 11 river catchments, this paper presents the results of a detailed study on the dispersal of the parasite in Flanders, Belgium, and the host-parasite relationship. In addition, data from 1986 and 1997 are used for comparative purposes, providing a perspective on the temporal infection pattern over 15 yr. The presence of A. crassus in Flanders was first discovered in 1985; 2 yr later a survey revealed a prevalence of 34.1% and a mean infection intensity of 5.5, based on adult nematodes only, and 10 yr later the parasite was present at all 11 sites sampled. Prevalence had increased to 62.5 % but the mean infection intensity had decreased to 3.9 adults per infected eel. Finally, in the year 2000, a third study revealed that A. crassus was present in 139 of 140 investigated sites; a further increase in prevalence to 68.7% and a decrease in mean infection intensity to 3.4 adults per infected eel was observed. When all larval stages were taken into account, mean prevalence amounted to 88.1% and mean intensity to 5.5 adults. The high infection level in Flanders is thought to be the result of restocking with glass eel and yellow eel, both of which are susceptible to A. crassus. The general infection parameters were similar in all 11 river catchments. It is possible that in Flanders both prevalence and mean infection intensity are stabilizing due to density-dependent regulation of the parasite infrapopulation. Fibrotic swimbladder walls were observed, mainly in large eels, and 20% of the total number of nematodes consisted of encapsulated larvae in the surveys of 1997 and 2000; 8 cases of swimbladder regeneration were observed.     

Infection status of the sea eel (Astroconger myriaster) purchased from the Noryangjin fish market with anisakid larvae]

Although the sea eel (Astroconger myriaster) is suspected as one of the most important fish host for human anisakiasis in Korea, no report has been made on the infection status of the sea eel with anisakid larvae. In the present study, 26 sea eels (Astroconger myriaster) were purchased from the Noryangjin fish market in Seoul, and anisakid larvae were collected from their viscera, muscle, head and skin. The collected larvae were classified by their morphological types. A total of 1,351 anisakid larvae were collected from 15 of 26 fish examined. Among them, 1,269 were recovered from the viscera, 66 from the muscle, and 16 from the head and skin. Morphologically, most of the anisakids were classified into 6 known larval types, Anisakis type I (564 larvae) of Berland (1961), Contracaecum type A (409) and type D (5) of Koyama et al. (1969), Contracaecum type C' (83) and type D' (117) of Chai et al. (1986), and Contracaecum type V (1) of Yamaguti (1935). Remaining 172 specimens were new in the available literature, hence, designated as Contracaecum type A' (new type). The present results revealed that the sea eels caught in the Korean waters are heavily infected with anisakid larvae, not only in their viscera but also in the muscle, and Anisakis type I was the most common among the 7 larval types.     

The population biology of Camallanus lacustris (Zoega) in eels, Anguilla anguilla (Linnaeus), and their status as its host

The population biology of Camallanus lacustris (Zoega) and the status of the eel, Anguilla anguilla (Linnaeus), as its definitive host have been studied in a small Devon lake. No clear seasonal pattern in prevalence and abundance was observed, and recruitment of the new generation may occur in all seasons. However, reproduction exhibits some seasonality as adult nematodes were the commonest stage in the parasite population from early summer onwards and production of first-stage larvae appeared to occur primarily during this period. These larvae were viable, and shown experimentally to be infective to copepods. The occurrence of the nematode and its development to full maturity in eels, the absence of its typical definitive host ( Perca fluviatilis Linnaeus) from the lake and the absence of the nematode from other species of fish in the lake indicate that eels serve as the only, true definitive host of the nematode in this locality. It is suggested that account must be taken of this alternative host when the population of C. lacustris is investigated in the future.     

The effects of 11-ketotestosterone on occupation of downstream location and seawater in the New Zealand shortfinned eel, Anguilla australis

The androgen 11-ketotestosterone (11KT) is associated with the physiological and morphological changes that occur during the transformation of sedentary ('yellow') freshwater eels (Anguilla spp.) into their migratory form ('silver') prior to their spawning migration in the ocean. In this study, we investigate the possible role of 11KT in modulating behaviors consistent with downstream migration; i.e., downstream and salinity preference in the New Zealand shortfinned eel (A. australis). Unlike silvering, 11KT did not induce preference for downstream locations, scored as presence at the downstream ends of 35 m raceways. Likewise, there was no evidence for increased salinity preference in 11KT-treated yellow eels, scored as preference for sea water over fresh water in a choice experiment. However, the 11KT treatment induced higher frequency of movements between fresh water and sea water, which may indicate restlessness.     

Management and restoration of European eel population (Anguilla anguilla): An impossible bargain

The European eel panmicitic population has been declining at least since the 1980s throughout its distribution area. The stocks are now ten times lower than they were initially. The causes of this decline are reviewed in this paper: marine causes such as Gulf Stream shifts are thought to reduce survival of leptocephali larvae during their transoceanic migration, but inland causes are also suspected, i.e. overfishing of all continental stages, obstructions to upstream and downstream migrations, habitat loss, water quality, parasite and xenobiotic contamination, which together contribute to reducing quality and quantity of spawner escapement from European inland waters to sea. Restoration programs have been conducted in several inland hydrosystems in Europe. If local fisheries have been sustained mainly by stocking elvers and glass eels, no significant restoration of the population has been observed suggesting that restoration plans are inefficient, despite significant efforts and relevant technologies (fish passage). The causes for the failure of restoration projects are listed and discussed, and it is shown that the minimum scale to work at is the catchment area. But international cooperation is required to coordinate programs, to determine common objectives and policies. Concepts for sustainable restoration and management are provided and discussed together with the general interest of eel population as a biointegrator of the quality and integrity of inland hydrosystems.     

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.     

Swim bladder nematodes (Anguillicoloides crassus) disturb silvering in European eels (Anguilla anguilla)

The introduced parasite Anguillicoloides crassus is thought to play an important role in the decline of freshwater eel (Anguilla spp.) populations. These nematodes are known to negatively affect many fitness-related traits in eels. We used experimental infections to study the effect of A. crassus on the relative size or mass of organs, and the expression of functionally relevant genes (total of 12 parameters) that are involved in the silvering process of Anguilla anguilla. Our results showed that the liver mass, the hemoglobin α-chain, and androgen receptors α expression levels were significantly higher in infected eels, whereas the freshwater rod opsin expression level and the gut mass were significantly lower in infected eels. Our results suggested that infected eels were at a more advanced stage in the silvering process than uninfected counterparts of similar size. These results may be explained by 2 hypotheses. First, A. crassus could trigger physiological mechanisms involved in the silvering process as a side-effect of infection. Second, eels may adjust their life history traits in response to infection. The implications for eel migration and reproductive success may be either negative or positive, depending on whether the response to A. crassus infection results in an additional cost of the parasite or is due to the phenotypic plasticity of the host.     

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.     

Factors determining length distribution and abundance of the European eel, Anguilla anguilla, in the River Mondego (Portugal)

1. The distribution and abundance of the European eel, Anguilla anguilla, were investigated in the Mondego River, a strongly modified river in central Portugal. Nine freshwater sites, located below the first impassable obstacle to eel migration, were surveyed for 2 years. The study was conducted monthly during the first year and seasonally during the second year. Fish were caught by electric fishing and, physical and biotic variables potentially influencing eel length distribution and abundance were determined at each sampling session. 2. Canonical correspondence analysis (CCA) was used to explain the relationships between abiotic and biotic habitat variables, and eel length distribution. Spatial variation was strongly associated with distance from the sea, number of obstacles, river width and percentage of instream cover. Depth, river flow, water temperature and cannibalism had weaker effects on the longitudinal distribution, but contributed as explanatory variables for the model. The influence of spatial variables outweighed the importance of temporal variables as predictors in this model. 3. Length distribution changed in space from a dominance of small eels (<100 mm) closer to the sea to larger eels (≥250 mm) in the upper reaches of the river. The smallest length class (eels <100 mm) was strongly associated with wider stretches where instream cover, mainly composed of aquatic submerged macrophytes, was abundant (>75% area coverage). On the contrary, larger eels (≥250 mm) preferred deeper stretches with stronger river flow and less instream cover. 4. The effect of biotic interactions with conspecifics as well as with the non‐native red swamp crayfish Procambarus clarkii, in sites with poor instream cover, modified this general pattern of distribution leading to fewer eels <100 mm at some sites closer to the sea. Therefore, despite the ubiquity and plasticity shown by this species, there were clear ontogenetic variations in habitat use such that the first two canonical axes of a CCA accounted for 58.4% of the spatial variability in size structure.