The spread of the eel swimbladder nematode Anguillicola crassus through the Erne system, Ireland

The spread of Anguillicola crassus was documented and showed an increase in both prevalence (9·9%) and mean intensity (6·7). Infected eels Anguilla anguilla were recorded 30 km downstream of the first recorded sites of infection. Migrating silver eels from commercial nets near the outlet of the Erne during October-December 1999 were also infected. Continued spread of A. crassus through Ireland's major wild eel fisheries now appears likely.     

Anal redness in European eels as an indicator of infection by the swimbladder nematode, Anguillicola crassus

Anal redness in European eels Anguilla anguilla is related to the prevalence and mean abundance of the swimbladder nematode Anguillicola crassus and may provide a simple, non-invasive diagnostic tool for A. crassus infection.     

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.     

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.     

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.     

First record of ostracods as natural intermediate hosts of Anguillicola crassus, a pathogenic swimbladder parasite of eels Anguilla spp

The ostracod Physocypria nipponica (Ostracoda: Candonidae) was found (prevalence 14.2%) to be the only intermediate host of the nematode Anguillicola crassus (Nematoda: Anguillicolidae), a pathogenic swimbladder parasite of eels, in a greenhouse-heated culture pond at Isshiki, Aichi Prefecture, Japan. Japanese eels Anguilla japonica from the same pond were found to be infected by adult A. crassus (prevalence 71.8%, intensity 1 to 6). This indicates that A. crassus could complete its life cycle under conditions of modern eel-culture technology where copepods were absent due to the unfavorable water quality for them, by utilizing ostracods as the intermediate host.     

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.     

Dynamics and predicted decline of Anguillicola crassus infection in European eels, Anguilla anguilla, in Neusiedler See, Austria

The eel population in Neusiedler See has been maintained by regular massive stocking since 1958. After the establishment of the National Park Neusiedler See-Seewinkel in 1993, eel stocking was prohibited and the population, together with the specific parasites of eels, was predicted to decline to extinction within 10 years. This investigation was undertaken to document the decline and extinction of the Anguillicola crassus population in eels. From 1994 to 2001, 720 eels were collected from two sites in the lake. Prevalence and abundance of A. crassus were lower in spring than in summer and autumn and larger eels harboured more parasites than smaller ones. Neither year of study nor sampling site were correlated with parasite infection levels. No significant trend in the population parameters of A. crassus was detected over the 8 years of the survey. This suggested that there had been no significant decline in the eel population. This suggestion was confirmed by investigations of the fishery, which also found evidence of regular illegal stocking. The stability of the A. crassus population over the past decade seems to reflect the lack of change in eel population density. No mass mortalities of eels occurred over the period despite the many similarities between Neusiedler See and Lake Balaton in Hungary. Differences in eel size, eel diet and the lack of large-scale insecticide use are discussed as possible explanations for the absence of eel mass mortalities in Neusiedler See.     

Humoral immune response of European eel Anguilla anguilla experimentally infected with Anguillicola crassus

A humoral immune response of the European eel Anguilla anguilla elicited by an experimental infection was demonstrated for the first time against the swimbladder nematode Anguillicola crassus. Eels were experimentally infected once or repeatedly and the antibody response was observed over a period of 325 d. Specific antibodies against A. crassus in the peripheral blood of the eels were measured using an ELISA and the immunoblot technique. Anti-A. crassus antibodies were first observed 8 wk post infection, and appeared to be independent of both the number of infective third stage larvae (L3) administered and the frequency of administration. However, individual eels showed great differences in the course of the antibody response. The late appearance of antibodies in the peripheral blood supports the hypothesis that not the invading L3 but rather the adult parasites elicit the production of specific antibodies. A stage-specific antibody response against the L3 was not observed. Main antigens are located in the body wall, especially in the gelatinous outer cuticle, of adult A. crassus.     

Evaluation of an ELISA and immunoblotting for studying the humoral immune response in Anguillicola crassus infected European eel Anguilla anguilla

The applicability of an enzyme-linked immunosorbent assay (ELISA) for the detection of anguillicolosis in feral eels was examined using a crude antigen preparation from the body wall of adult Anguillicola crassus. The screening consisted of samples from 100 feral European eels Anguilla anguilla. As a reference the actual status of infection was determined by dissection of the eels' swim-bladders. The ELISA results were compared with a background value calculated from the results obtained from 43 non-infected farm eels. The screened samples had a high prevalence of A. crassus (83 %); however, the specificity and the negative predictive value of the ELISA were low compared to the high positive predictive value. Nonetheless, the reproducibility (precision) of the test was satisfactory, and for the non-infected reference group specificity was 97.7 %. Although the ELISA, as used in the present study, is not applicable for diagnostic purposes, it represents a useful tool for the investigation of the specific humoral immune response of eels against A. crassus under controlled experimental conditions. Immunoblots using crude antigen preparations from different parts of adult A. crassus as well as a crude somatic third-stage (L3) antigen preparation illustrated that only antigens associated with the body wall of adult A. crassus are potentially suitable for diagnostic purposes. Despite the fact that antibodies against Raphidascaris acus cross-reacted with 3 body wall antigens of A. crassus, the most encouraging results were obtained with the antigen preparation from the outer cuticle of adult A. crassus which yielded a conspicuous, broad band at about 100 kDa.     

The swimbladder nematode Anguillicola crassus in American eels (Anguilla rostrata) from middle and upper regions of Chesapeake Bay.

The patterns of infection of American eels Anguilla rostrata, with the introduced swimbladder nematode Anguillicola crassus, in tributaries of middle and upper Chesapeake Bay are described. A total of 423 subadult eels was collected from 8 Bay tributaries from spring 1998 to fall 1999. Also, 30 elvers were collected from Ocean City, Maryland, in spring 1998. The numbers of juvenile and adult specimens of A. crassus in the swimbladder wall and lumen were counted. No elvers were infected. In subadult eels, prevalence of adult and juvenile stages combined ranged from 13% to 82%; mean intensity ranged from 2.6 to 9.0 worms per eel. Infection levels were highest for Susquehanna River eels (northernmost river) and lowest in the southernmost sites: St. Jerome's Creek and the Pocomoke River. Although eels from these 2 localities were larger, the low infection rates there are most likely due to reduced transmission in higher salinity water and not to eel size. Eels with both adult and juvenile stages of A. crassus were more common than expected by chance. This might be explained by inhibition of juveniles migrating into the swimbladder lumen when adults are already present there.     

Biased sex ratio in the European eel (Anguilla anguilla) swim-bladder parasite Anguillicola crassus, experimentally induced by 11-ketotestosterone

Parasites are intimately connected to the host in which they live, and some may be affected by the polluted environment of their host. The present study describes the effect of a steroid hormone (11-ketotestosterone) on the sex ratio of the invasive hematophagous nematode Anguillicola crassus Kuwahara, Niimi & Itagaki, 1974, when experimentally injected to European eels, Anguilla anguilla. Our results showed that this steroid induced a significant male-biased ratio in the nematode A. crassus infrapopulations, suggesting that the presence of endocrine disruptors in the environment may lead to skewed sex ratios among parasites.     

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.     

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'.     

Vaccination of eels (Anguilla japonica and Anguilla anguilla) against Anguillicola crassus with irradiated L3

The original host of the swimbladder nematode Anguillicola crassus, the Japanese eel (Anguilla japonica) and the recently colonized European eel (Anguilla anguilla) were immunized with 40 irradiated (500 Gy) 3rd-stage larvae (L3) of this parasite and challenged with an infection of 40 normal L3. The immunization induced a significant reduction of the number of adult worms developing from the challenge infection in A. japonica, but not in A. anguilla. The induced resistance (calculated using the relation of the number of adult worms in immunized eels and in non-immunized control eels) in A. japonica was 87.3%+/-30.4%. Following a single infection, the percentage of adult worms found in A. japonica was lower as compared to A. anguilla, and the few adult worms were much smaller, revealing a lower susceptibility of A. japonica to A. crassus in comparison to A. anguilla. Both eel species developed an antibody response against A. crassus, but the level of antibody responses was not positively correlated with the protection against infection, suggesting that the antibody response is not a key element in resistance of eels against A. crassus. This study suggests that the original host of A. crassus is able to mount efficient protective immune responses against its parasite, whereas the newly acquired host seems to lack this ability.     

An enhanced humoral immune response against the swimbladder nematode, Anguillicola crassus, in the Japanese eel, Anguilla japonica, compared with the European eel, A. anguilla.

The humoral immune response in the two eel species, Anguilla japonica and Anguilla anguilla against two fractions of antigens in Anguillicola crassus were studied. Within species, both eel species showed significantly elevated titres compared with controls when immunized with antigens from Anguillicola crassus. In interspecific comparison, Anguilla japonica showed significantly elevated titres in comparison with Anguilla anguilla. Immunization of Anguilla anguilla caused a significantly decrease in the plasma levels of protein in comparison with control fish and all groups of Anguilla japonica. In contrast, Anguilla japonica showed significantly lower plasma levels of Ig in all groups compared with Anguilla anguilla. The different susceptibilities to Anguillicola crassus between the natural host, Anguilla japonica, and the naive, Anguilla anguilla, is partly due to differences in the ability of the two eel species to mount a humoral immune response.     

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.     

Spatial and temporal variation in Anguillicola crassus counts: results of a 4 year survey of eels in Mediterranean lagoons

We present the results of a survey of anguillicolosis in the Rh6ne River delta. From January 1997 to December 2000, a total of 13,319 eels (Anguilla anguilla from elver to silver phase) were examined, in which we found 22,227 swimbladder nematodes (Anguillicola crassus adults and pre-adults). A generalised linear model (GLM) framework was used to explore the relative contribution of various factors to the occurrence, intensity and abundance of the parasite. We reveal a major influence of the month of sampling, and we document the existence of a seasonal pattern with regular peaks in early summer and late winter. In contrast, the year of sampling is of secondary importance, and no particular trend in the development of the infection can be detected. More than a decade after the first record of A. crassus in the Rh?ne River delta, anguillicolosis has thus attained a constant infection rate of nearly 50%, with a mean number of 3 or 4 macroscopic lumen worms per infected eel. The eel length strongly influences the intensity and the abundance of the nematode, but has little if any effect on the probability of being infected. There exists a linear relationship between eel size and the number of parasites, but not between eel size and prevalence. We observe a decrease in the proportion of infected individuals among elver eels. We discuss this result in relation to the possible mortality of heavily infected individuals and/or a change in the eels' alimentary diet.     

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.     

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.