Diving activity of migrating silver eel with and without Anguillicola crassus infection

Infection with the swim bladder nematode Anguillicola crassus has been hypothesised to threaten the spawning migration success of the endangered European eel (Anguilla anguilla). To examine this assumption, we compared the swimming behaviour of one Anguillicola crassus infested eel in the North Sea and three parasite‐free eels in the Baltic using data recovered from data storage tags attached to migrating silver eels. In both areas, eel activity was characterized by frequent diving behaviour throughout the water column during the night, with reduced activity during the day. Despite substantial damage of the swim bladder, the behaviour of the infested eel from the North Sea was within the same range of migrating and diving activity parameters as the three parasite‐free eels from the Baltic Sea. All eels had a similar frequency distribution of descent or ascent speeds and a similar average horizontal migration speed. The diving speeds and dive ranges exclude the possibility that the eels were in continuous hydrostatic equilibrium during their migrations and suggests therefore that the role of the swim bladder in vertical migration is likely to be more complex than currently thought. Our results suggest that eels infested by Anguillicola crassus are capable of diving in a similar manner to uninfested eels during the first stretch of their spawning migration.     

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.     

Head morphology and piscivory of European eels,Anguilla anguilla,predict their probability of infection by the invasive parasitic nematode Anguillicoloides crassus

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Transmission of neozoic Anguillicoloides crassus and established Camallanus lacustris in ruffe Gymnocephalus cernuus

In the present study, groups of ruffe Gymnocephalus cernuus, reared singly, were exposed to defined numbers of Anguillicoloides crassus or Camallanus lacustris under controlled laboratory conditions. Infection took place orally through feeding G. cernuus with axenically cultured and laboratory infected copepods, in which the parasites had developed to the infective third stage (L3). Mean prevalence (94·3%) and infection probability (38·5%) for the established C. lacustris were significantly higher than for the neozoic A. crassus (14·3 and 1·0%, respectively). Peripheral blood leukocytes were significantly increased in infected fish, apparently independent of exposure level, parasite species or intensity of infection compared to the controls. In infected fish, the gonado‐somatic index (I_G) was significantly reduced by c. 50%, and the spleen‐somatic index (I_S) was significantly increased compared to controls. Both parasites raised similar physiological and immunological responses in G. cernuus, which was able to effectively reject the neozoic A. crassus.     

Distribution,prevalence and intensity of Anguillicola crassus (Nematoda) infection in Anguilla anguilla in the Republic of Ireland

This study is the first comprehensive documentation of the geographical range of Anguillicola crassus in its host, the European eel Anguilla anguilla, in the Republic of Ireland. The prevalence and intensity of infections across 234 sites and 93 river basins in Ireland comprising rivers, lakes and transitional waters (estuaries) were analysed. While only 32% of the river basins were affected by this nematode, they correspond to 74% of the total wetted area. Significant differences in infection levels among water body types were found with lakes and transitional waters yielding the highest values, which can be attributed to the proportions of juvenile (total length, L_T < 300 mm) A. anguilla caught. There were no significant differences in infection levels between water body types for adult A. anguilla or between sexes for any water body type. Prevalence was significantly lower in juvenile compared with adult A. anguilla captured in rivers and a positive correlation between infection levels and host size‐classes was found. Future efforts should focus on monitoring the spread of A. crassus infections and assessing the swimbladder health of A. anguilla in Ireland.     

Colonization, larval survival and epidemiology of the nematode Anguillicola crassus, parasitic in the eel, Anguilla anguilla, in Britain

In late 1987, immature Anguillicola crassus were reported for the first time in Britain from eels from two river systems. By late 1988, gravid adults were present in a number of rivers in the east of England in two discrete centres of distribution: one in East Anglia correlated with the route taken by lorries exporting eels to the continent, and one in the R. Thames correlated with the import of eels to London. The parasite was firmly established in the R. Trent, where prevalence levels reached 100% in some places. Laboratory investigations showed that adult parasites and their eggs remained viable even after infected eels had been maintained for 4 weeks in 100% sea water. Hatching of eggs declined with increasing salinity, but was not totally inhibited by sea water. Survival and infectivity of freeliving second stage larvae were maximal in natural fresh water (95% survival for 4 months, and 50% still infective to copepod intermediate hosts after 70 days), but declined in alkaline water and with increased salinity. Nevertheless, in 100% sea water, 50% of larvae were still infective after 8 days. Specificity to the intermediate host was low, and eels of all sizes could be infected. These characteristics, plus a high reproductive potential, give the parasite exceptional colonization potential and ability, enabling it to survive natural movements of eels from catchment to catchment and to increase rapidly within a new locality. The ability of free-living larvae to adhere to the substratum and survive in sea water enables them to survive in eel-transport lorries from which they will not readily be removed by flushing, the normal cleansing procedure. It is concluded that there were two separate introductions of the parasite to Britain; via the eel import trade through London, and, totally unexpectedly, via the eel export trade in lorries traversing East Anglia. The parasite is now firmly established in Britain and will continue to spread by natural movements of eels but especially by human-assisted movements of infected eels for stocking and market. This latter practice is recognized as a major factor in introducing and disseminating fish parasites.     

Isolation and characterization of short tandem repeats in an invasive swimbladder nematode,parasitic in Atlantic freshwater eels,Anguillicola crassus

We describe the isolation and characterization of seven polymorphic short tandem repeats (STR) for the eel parasite Anguillicola crassus. This invasive swimbladder nematode endemic in East Asia was recently introduced into Europe. The number of alleles for each STR ranged from 13 to 39 per locus with observed heterozygosities between 0.49 and 0.98. The Taiwanese population displayed higher genetic diversity compared to the Irish sample, an observation consistent with the Asian biogeographical origin of the nematode. Availability of the reported STR will facilitate the investigation of the population genetic structure with regard to multiple invasions.     

Metazoan parasites of Neogobius fishes in the Slovak section of the River Danube

Metazoan parasites were investigated in three non‐native fishes (monkey goby Neogobius fluviatilis, bighead goby Neogobius kessleri and round goby Neogobius melanostomus) collected from the former and current main channel of the River Danube and from the River Hron, Slovakia, in November 2003. Thirteen parasite species were identified: Triaenophorus crassus, Diplostomum sp., Tylodelphys clavata, Metorchis xanthosomus, Nicolla skrjabini, Gyrodactylus proterorhini, Pomphorhynchus laevis, Contracoecum sp., Raphidascaris acus, Anguillicola crassus, Unio tumidus, Anodonta anatina and Pseudoanodonta complanata. The maximum parasite diversity was found in N. fluviatilis. Total parasite abundance was significantly higher in N. kessleri, but no significant differences among sampling sites were observed. Pomphorhynchus laevis and glochidia of Anodonta anatina reached 100% prevalence in N. kessleri in the new channel of the Danube and, in general, these species were also the most prevalent parasites in all three goby species. For endoparasites, gobies served mostly as intermediate (digenean, cestodes and nematodes) or paratenic (acantocephalan and nematodes) hosts. All parasite species found are common parasites in the Middle Danube basin. No parasites specific to Neogobius, known from their native populations, were observed.     

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.     

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 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.     

Genetic signatures in an invasive parasite of Anguilla anguilla correlate with differential stock management

In this article, it is shown that available genetic tools for the omnipresent parasite Anguillicoloides crassus in European eels Anguilla anguilla are sensitive to different immigration rates into local A. anguilla stocks for two separated river systems. Relying on four highly polymorphic microsatellite markers, it was inferred that under natural recruitment, nematode samples meet Hardy–Weinberg expectations for a single panmictic population, while genetic signals show signs for a strong Wahlund effect most likely due to very recent population mixing under frequent restocking of young A. anguilla. This was indicated by a low but significant F_ST value among within‐host populations (infrapopulations) along with high inbreeding indices F_IS consistent over all loci. The latter signal is shown to stem from high levels of admixture and the presence of first‐generation migrants, and alternative explanations such as marker‐ and sex‐specific biases in the nematode populations could be dismissed. Moreover, the slightly increased degree of relatedness within infrapopulations in the stocked river system cannot explain the excessive inbreeding values found and are most likely a direct consequence of recent influx of already infected fish harbouring parasites with different genetic signatures. Applying a simulation approach using known variables from the nematode's invasion history, only the artificial introduction of a Wahlund effect leads to a close match between simulated and real data, which is a strong argument for using the parasite as a biological tag for detecting and characterizing fish translocation.     

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.     

Assessment of Epinephelus coioides (Hamilton, 1822) aquaculture systems in the Gulf of Tonkin,Vietnam, by using fish parasites

The parasite fauna of Epinephelus coioides can be used as an indicator to assess different aquaculture systems. A total of 133 E. coioides were collected from fishermen (wild fish) and marine fish farms (net cages, pond farms) in the Gulf of Tonkin (Ha Long, Cat Ba and Nghia Hung), Vietnam in 2013 and 2014, and examined for the presence of protozoan and metazoan parasites. Different patterns of parasite infections were found. The monogenean Pseudorhabdosynochus spp. was predominant in the net cage system; and the protozoans Trichodina spp. and Cryptocaryon irritans were found exclusively in pond and net cage cultivation sites in Nghia Hung and Cat Ba. These three species were assessed in addition to seven further indicator species and two dominance indices, to visualize the potential of assessing different aquaculture systems in Vietnam. This suggests the use of former shrimp ponds for grouper cultivation, reducing the pressure to further extend net cage cultivation in already highly influenced mariculture regions in Vietnam.     

Experimental transmission of Enteromyxum scophthalmi (Myxozoa), an enteric parasite of turbot Scophthalmus maximus

Several experiments were designed to elucidate the modes of transmission of the myxozoan parasite Enteromyxum scophthalmi to turbot Scophthalmus maximus. Direct transmission of the infections was achieved by cohabitation of infected and test fish, through waterborne contamination from the effluent of a tank containing infected fish, and via the oral route using parasite-infected intestines. The transmission of the turbot enteromyxosis was successful in all the fish exposed to the parasite by the 3 routes; accumulated mortality reached 100% at the end of most experiments. The progress of the infections was monitored by study of the histopathology. Influence of the mode of exposure was observed, with the oral route the fastest to initiate the parasite infections. The temperature also affected the course of the infections, which were established earlier at higher water temperature. Direct fish-to-fish transmission of the disease explains the rapid spreading of the turbot enteromyxosis in farms.     

The viability of the free living larvae of Anguillicola crassus

The viability of Anguillicola crassus larvae was studied under various environmental conditions. High températures and nigh salt concentrations considerably shorten the lifetime of the larvae. This is possibly one of the reasons why infection does not occur as massively in marine biotopes as it usually does in fresh water.     

Spatiotemporal and gender‐specific parasitism in two species of gobiid fish

Parasitism is considered a major selective force in natural host populations. Infections can decrease host condition and vigour, and potentially influence, for example, host population dynamics and behavior such as mate choice. We studied parasite infections of two common marine fish species, the sand goby (Pomatoschistus minutus) and the common goby (Pomatoschistus microps), in the brackish water Northern Baltic Sea. We were particularly interested in the occurrence of parasite taxa located in central sensory organs, such as eyes, potentially affecting fish behavior and mate choice. We found that both fish species harbored parasite communities dominated by taxa transmitted to fish through aquatic invertebrates. Infections also showed significant spatiotemporal variation. Trematodes in the eyes were very few in some locations, but infection levels were higher among females than males, suggesting differences in exposure or resistance between the sexes. To test between these hypotheses, we experimentally exposed male and female sand gobies to infection with the eye fluke Diplostomum pseudospathaceum. These trials showed that the fish became readily infected and females had higher parasite numbers, supporting higher susceptibility of females. Eye fluke infections also caused high cataract intensities among the fish in the wild. Our results demonstrate the potential of these parasites to influence host condition and visual abilities, which may have significant implications for survival and mate choice in goby populations.     

Reproductive potential of Schistocephalus solidus‐infected male three‐spined stickleback Gasterosteus aculeatus from two U.K. populations

Male three‐spined stickleback Gasterosteus aculeatus from two U.K. populations with endemic infections of the cestode Schistocephalus solidus were brought into the laboratory prior to the breeding season and transferred to nesting tanks under conditions designed to stimulate sexual maturation. Nesting and courtship behaviours were scored over a 35 day period, after which fish were euthanized and the liver, spleen, kidney and gonads were weighed. Among G. aculeatus from a park pond in Leicester, U.K., infected males rarely engaged in reproductive behaviours and exhibited reduced indices of sexual development, body condition and general health, with effects being largely independent of relative parasite mass (parasite index, I_P). In contrast, the reproductive behaviour of infected fish from Kendoon Loch in Dumfriesshire, U.K. appeared to be less severely affected, with infected fish regularly building nests and courting females under laboratory conditions. This was paralleled by a more limited effect of infection on physiological indicators of development, condition and general health. Furthermore, behavioural and physiological variables typically correlated with I_P among infected fish from this population. Although comparing the performance of infected fish from the two populations directly was difficult due to potentially confounding factors, the results support the findings of recent studies showing that the effects of S. solidus on host reproduction are unlikely to be uniform across G. aculeatus populations. One possibility is that variation in the effects of infection arises from differences in the co‐evolutionary association times of G. aculeatus with the parasite.     

Histopathology of fish parasite infections – importance for populations

There is a bewildering array of fish parasites and probably all fish species harbour one or more species. Under normal conditions hosts often show little or no signs of infection, either clinically or at the organ and tissue level. All tissues can be infected, including the blood. Coelozoic species generally do not elicit significant host responses. Any developmental stages, however, where these migrate through the host tissues may produce a cellular response if resident for sufficient time. Histozoic parasites are generally more likely to evoke a pathological response since they are invariably in more intimate contact with immunocompetent host cells such as lymphocytes and phagocytes. In some cases, particularly with protistan infections, host response can be dramatic and cause significant disease due to organ dysfunction, with subsequent mortalities. Infections of the external epithelia caused by a variety of parasites including Monogenea and Copepoda are also significant, especially when large numbers are present. Resulting tissue necrosis compromises osmoregulation and facilitates entry of prokaryote infections. Parasites have numerous strategies to evade detection within the host, but even ‘protected’ intracellular forms, e.g. microsporeans and muscle‐invading myxozoans are recognized when they outgrow their accommodation or large cysts rupture, presenting parasite antigens to the host. In most instances, an evolutionary balance has been achieved between the host and the parasite and even when histopathology is evident, this is frequently localized and does not unduly impair performance of the affected organ. Examples include chronic inflammation, granuloma formation and focal fibrosis. This paper outlines the principle histopathological responses to a variety of parasite groups and provides a more detailed treatment of selected parasitic infections in marine and freshwater fish species to illustrate the relative importance of acute and chronic parasitic infections for host survival.