Do eel parasites reflect the local crustacean community? A case study from the Rhine River system

In 2003, the parasite fauna of 197 European eels Anguilla anguilla, captured at three different locations (Laufenburg, Karlsruhe and Beneeden Leeuwen) in the River Rhine, was analysed. The eels harboured a total of 18 species, among them the protozoa (Myxidium giardi, Myxobolus kotlani and Trypanosoma granulosum), acanthocephalans (Acanthocephalus anguillae, Acanthocephalus lucii, Echinorhynchus truttae, Pomphorhynchus laevis), nematodes (Paraquimperia tenerrima, Pseudocapillaria tomentosa, Camallanus lacustris, Raphidascaris acus, Spinitectus inermis and Anguillicola crassus), cestodes (Bothriocephalus claviceps and Proteocephalus macrocephalus) and monogeneans (Pseudodactylogyrus sp.). The parasite fauna at the different locations is discussed with respect to the crustacean fauna present at these locations. The investigation shows that changes in the composition of the crustacean fauna, due to the anthropogenic breakdown of a biogeographic barrier, are reflected in the composition of the intestinal eel parasite fauna.     

The metazoan parasites of freshwater fishes in the Corrib catchment area, Ireland

A survey of the parasites of 243 fish belonging to 13 species, from the Corrib catchment area, western Ireland, was undertaken. At least 32 species of metazoan parasites were shown to be present. Diplostomum gasterostei, Tylodelphys clavata, Eubothrium salvelini, Cucullanus truttae, Raphidascaris acus, Ergasilus gibbus and Salmincola gordoni appear to be first records for Ireland and Phyllodistomum conostomum has not previously been reported from the British Isles. New host records involving Lamptera planeri, Salvelinus alpinus, Abramis brama, Noemacheilus barbatulus, Anguilla anguilla and Pungitius pungitius for the British Isles are given.     

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.     

Peculiarities of the parasitofauna of Atlantic salmon parr (Salmo salar L.), brown trout (Salmo truttae L.), and char (Salvelinus alpinus L.) in the Utsjoki River system (Northern Finland)

Data on the parasite diversity in Salmonidae fish parr from different parts of the Utsjoki River obtained during 1993-1995 and 2006-2007 are presented. Three fish species, Salmo salar L., S. truttae L., and Salvelinus alpinus L., were examined on the presence of helminthes. Twenty species of salmon parasites were found, the majority of which are the parasites with complicated life cycles. Infusorians C apriniana piscium, myxosporidia Chloromyxum januaricus and Myxobolus neurobius, metacercaria of the genera Diplostomum and Apatemon, and the nematode Raphidascaris acus larvae were the most numerous in salmon parasite fauna. Brown trout had the most number of specific parasite species, whereas char was infested by protozoan parasites only.     

A note on the occurrence of the digenetic trematode Sphaerostoma bramae (Müller) in the intestine of the European eel, Anguilla anguilla (L.)

The allocreadiid digenean Sphaerostoma bramae (Müller) was found in three of 602 eels, Anguilla anguilla (L.), caught over a period of 25 months from drains and rivers in the lower River Trent drainage area. Eleven, 15 and 32 specimens of S. bramae were found in the posterior 40% of the respective host's intestine. Concurrent infestations with Proteocephalus macrocephalus, Acanthocephalus clavula and Rhaphidascaris acus were observed. The results are discussed in relation to the helminthology and ecology of the eel.     

Parasite fauna of the European river lamprey Lampetra fluviatilis (L.) from Lake Onega

Data on the parasite fauna of the adult European river lamprey Lampetra fluviatilis (L.) from Lake Onega are reported. Ten parasite species are found, including trematodes Diplostomum petromyzifluviatilis and D. spathaceum (metacercariae), cestode Proteocephalus longicollis, nematodes Cucullanus truttae and Raphidascaris acus, acanthocephalan Echinorhynchus salmonis, ectoparasitic infusoria Chilodonella hexastica, Trichodina tenuidens, and Trichodinella epizootica, and fungus Saprolegnia parasitica. Three species are found to be dominate, namely D. petromyzifluviatilis, Cucullanus truttae, and P. longicollis. Comparative analysis of the parasite faunas of the lampreys from other basins is carried out. Some similarity in the parasite faunas of lampreys and salmonids is discovered.     

Parasitological study of a population of Tiber River eels (Anguilla anguilla)

A study was conducted on the parasitofauna of Anguilla anguilla caught in the section of the Tiber river south of Rome (Italy). The sample examined consisted of 417 specimens that were classified by stage (elver, young yellow eel, yellow eel and silver eel) and season of sampling. The following species were identified: Trypanosoma granulosum, Eimeria anguillae, Myxidium giardi, Sphaerospora reichenowi, Myxobolus sp., Trichodina anguilli, Ichthyohodo sp., Gyrodactylus anguillae, Bothriocephalus claviceps, Proteocephalus macrocephalus, Raphidascaris acus, Acanthocephalus clavula. Each parasite species was considered in its prevalence according to stage and season. For some parasite the pathogenic effect was also examined in a histological study of serial sections. The results of the statistical analysis of the single parasitic infection as related to different seasons pointed to marked seasonal trends only in some species (Trypanosoma granulosum and Gyrodactylus anguillae). The intensity of infection assessed for acanthocephalan infection only was found to affect neither weight nor condition index (weight/length3). No difference in weight or condition index was found to be ascribable to the presence or absence of a species. An attempt to find a rule-of-thumb algorithm to gauge the overall effect to parasitic diseases failed to give sufficiently significant results.     

Parasites of underyearling kamchatka mykiss Parasalmo mykiss mykiss (Osteichithyes:Salmonidae) in the Utkholok River (North-Western Kamchatka)

Eight species of parasites, Apiosoma piscicolum piscicolum, Apatemon sp., Diplostomum sp., Bunoderidae gen. sp., Crepidostomum metoecus, Hysterothylacium gadi aduncum, Salvelinema salmonicola, and Cucullanus truttae had been found in underyearling Kamchatka mykiss (with fork length 28-41 mm) from the Utkholok River, North-Western Kamchatka. Infestation rate of the fishes with each parasite species was rather low. Presence of C. truttae in underyearling Kamchatka mykiss could not be explained by the conceptual model of its life cycle proposed by Moravec (1979). Spatial and temporal isolation of underyearling Kamchatka mykiss and ammocoetes, as the elements of a local food web, suggest that the lamprey larvae do not participate in the transmission of C. truttae to underyearling Kamchatka mykiss.     

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.     

The dynamics of a declining population of the acanthocephalan Acanthocephalus clavula in eels Anguilla anguilla in a small river

Changes in the size and composition of a population of the acanthocephalan Acanthocephalus clavula in eels, Anguilla anguilla , and flounders, Platichthys flesus , its definitive hosts, in a small river are described over a period of 4.5 years in the course of which the population underwent a steady and continuous decline. Parasite prevalence and abundance declined more rapidly initially and then more gradually, and during the period the frequency distribution changed from overdispersed to being close to random on most occasions. Throughout the whole period newly recruited parasites were found in eels, and adult females continued to mature and produce acanthors. Data on the distribution and occurrence of the intermediate host Asellus meridianus in the river suggested that in the latter part of the decline it was no longer possible for the parasite to complete its life cycle in some parts of the river, and the cause of the parasite population decline is believed to be the decrease in abundance of the intermediate host as a result of interspecific competition with a congeneric species. During this latter period, immigration of infected eels from another river in the catchment may have contributed to the maintenance of the parasites in the locality, but it is considered that the decline in the river was representative of what was happening in other parts of the catchment and that the whole parasite population in the catchment was declining for the same reason.     

Long-term stability in the richness and structure of helminth communities in eels,Anguilla anguilla,in Lough Derg,River Shannon,Ireland

A data set on intestinal helminth parasites was collected in the course of an 18 year investigation into the biology of eels in Meelick Bay, Lough Derg, River Shannon. This was used to test two hypotheses relating to the composition and structure of intestinal helminth communities, namely that eels in large rivers do not harbour richer and more diverse communities than those in small rivers but that community composition and structure are more stable over time than in small rivers. The helminth community was species poor, with only six species comprising the component community and a maximum infracommunity richness of three species. The community was overwhelmingly dominated by the acanthocephalan Acanthocephalus lucii, reflecting the importance of its intermediate host Asellus aquaticus in the eels' diet. The remaining helminth species contributed to species richness but made very little contribution to community diversity. Population levels of Acanthocephalus lucii fell and remained low between 1992 and 2000, probably reflecting increased movement of eels from other parts of the lough into Meelick Bay. Diversity values were low, but similar to those reported from other rivers in Britain and Europe. The results provided support for both hypotheses and indicated that in respect of richness, diversity and dominance, the helminth communities of eels in the River Shannon were typical of, and comparable to, those of other large rivers throughout Europe.     

Ecological parasitology of polymorphic Arctic charr, Salvelinus alpinus (L.), in Thingvallavatn, Iceland

The helminth endoparasite fauna in four Arctic charr morphs, Salvelinus alpinus (L.), small benthivorous (SB), large benthivorous (LB), planktivorous (PL) and piscivorous (PI) charr, from Thingvallavatn, Iceland consisted of: Crepidostomum farionis (Trematoda: Allocreadiidae); Diplosttomum sp. (Trematoda: Diplostomatidae); Eubothrium salvelini; Diphyllobothrium dendriticum; D. ditremum (Cestoda: Pseudophyllidae); Proteocephalus longicollis (Cestoda: Proteocepha-lidae): and Philonema oncorhynchi (Nematoda: Filariidae). The morphs exhibited distinctive patterns in prevalences and parasite burdens (mean intensity and mean relative density of parasites). SB charr had high prevalence and parasite burden of the eye fluke Diplostomum sp. and none to very light infections of the other parasite species. LB charr had relatively high prevalence and parasite burden of the intestinal fluke C. farionis , whereas infections of the remaining parasite species were light to moderate. PL and PI charr had high prevalences and worm burdens of Diphyllobothrium spp. and P. longicollis . PL charr differed from PI charr in higher worm burden off P. longicollis and lighter burden of £. salvelini . Prevalences of P. oncorhynchi were high in PL and PI charr. Association of parasite intensities and age and length offish were investigated. The different infection patterns among the morphs agree well with their partitioning in food and habitat utilization, and confirm that there is a high degree of ecological segregation between the morphs. The results demonstrate the importance of ecological factors influencing transmission efficiency of parasites to the fish host.     

Parasites of Salmo trutta L. from the Tirino River. II. Host-parasite interactions of helminth species

The hundred and sixteen brown trout (Salmo trutta L.) which were examined for helminth parasites were captured in the River Tirino, (L'Acquila - Italy). Six parasite species (Phyllodistomum simile, Crowcrocaecum testiobliquum, Crepidostomum metoecus, Cyathocephalus truncatus, Truttaedacnitis truttae and Dentitruncus truttae) were recovered. Ecological studies on each helminth species recovered have been carried out analysing the following aspects; the preference of each parasite species for certain microhabitats in the host; the incidence and intensity of each parasitic infection according to sex, age and season.     

Helminths of pond-reared walleye from Wisconsin

One hundred extended growth walleye fingerlings, Sander vitreus (Percidae), collected on 6 October 2004, from 1 rearing pond at the Lake Mills State Fish Hatchery in Lake Mills, Wisconsin, were examined for parasites. Diplostomum sp. (Trematoda: Diplostomatidae), Contracaecum sp. (Nematoda: Anisakidae), Bothriocephalus cuspidatus (Cestoda: Bothriocephalidae), and Proteocephalus sp. (Cestoda: Proteocephalidae) were the only parasites found. The first 3 species occurred as larval stages. Diplostomum sp. and Contracaecum sp. had similar prevalences, mean intensities, and mean abundances (72%, 2.2, and 1.6 and 71%, 2.1, 1.5, respectively) in walleye fingerlings. A headlamp technique used by the Wisconsin Department of Natural Resources personnel generated a prevalence of Diplostomum sp. in the lens that overestimated the prevalence of Diplostomum sp. found in a random subsample of 100 fingerlings examined with a microscope. Proteocephalus sp. and B. cuspidatus infected 14 and 12 fingerlings, respectively.     

The parasite fauna of the fish of the Shropshire Union Canal, Cheshire

A survey was made of the parasites of 603 roach Rutilus rutilus (L.), 15 bream Abramis brama (L.), 201 perch Perca fluviatilis L., 30 pike Esox lucius L. and four eels Anguilla anguilla (L.) caught in the Shropshire Union Canal at Backford, Cheshire from December 1964 to August 1966. Twenty-seven species of parasites were found, 17 in roach, seven in bream, ten in perch, ten in pike and two in the eel. Two species of Protozoa, seven species of Monogenea, five species of Digenea, six species of Cestoda, two species of Nematoda, one species of Acanthocephala, two species of Hirudinea, one species of Crustacea and mollusc glochidia were recorded. The following parasites are believed to be new records for the British Isles: Henneguya oviperda (Cohn, 1895), Dactylogyrus suecicus Nybelin, 1936, D. wunderi Bykhovskii, 1931, Asymphylodora kubanicum (Isaichikov, 1923), and Philometra rischta Skryabin, 1917.
One table shows the species of parasites found, together with data on the site of occurrence in the host, and the percentage and intensity of infection of the fish. A second table compares the occurrence of the parasites in four other localities in the British Isles, Loch Lomond Scotland, Llyn Tegid (Bala Lake), Merionethshire, Rostherne Mere, Cheshire and the River Lugg, Herefordshire. A further column gives the normal hosts in the U.S.S.R.
A limited comparison is made of the numerical occurrence of six species of parasites in the canal, Llyn Tegid and Druzno Lake, Poland. It is concluded that unless relatively large samples of fish of all length groups are collected on a regular basis throughout the year such comparisons will have little meaning.
The concept of the characterization of parasite faunas is briefly noted. It is suggested that the high degree of host specificity shown by many of the species of parasites is evidence in support of the concept.     

A description of rodlet cells from the alimentary canal of Anguilla anguilla and their relationship with parasitic helminths

Rodlet cells in intestinal epithelia of infected and uninfected European eels Anguilla anguilla from brackish and fresh water were studied by light and electron microscopy. Deropristis inflata (Trematoda) was found in eels from brackish water, whereas eels from fresh water were infected with Acanthocephalus clavula (Acanthocephala). In a comparison between uninfected and infected eels from brackish water, a higher number of rodlet cells was recorded in the intestinal epithelia of infected fish. Evidence is presented that rodlet cells secrete their contents in a holocrine manner into the lumen of the eel intestine. The occurrence of organelles within the mature rodlet cell was rare. ? 1998 The Fisheries Society of the British Isles     

Discontinuous distributions of the fish acanthocephalans Pomphorhynchm laevis and Acanthocephalus anguillae in Britain and Ireland: an hypothesis

The current distributions of the freshwater fish acanthocephalans Pomphorhynchus laevis and Acanthocephalus anguillae are described and shown to be discontinuous and mutually exclusive, both regionally and locally, in the British Isles. An hypothesis is erected to account for this pattern. It is suggested that as the continental freshwater cyprinids colonized post-glacial mainland Britain via the eastward-flowing rivers and the Thames-Rhine link, they brought with them both species of acanthocephalan. The present, more extensive distribution of P. laevis in the British Isles and Ireland is explained by (1) early formation of a marine strain that colonized the Baltic and North Sea and estuaries of North Sea rivers, (2) later transfers of infected barbel to other English rivers from the R. Thames by man, and (3) transfers to Ireland of infected cyprinids from England by man. Different and restricted availability of preferred definitive and intermediate hosts subsequently resulted in the formation of distinct strains in England and Ireland. The distribution of A. anguillae can be explained by similar anthropogenic influences, but since its definitive and intermediate hosts are more widely available, strain formation has not yet been detected. Competitive interactions between the two parasites in the intestine of the definitive hosts are thought to be responsible for their mutual exclusiveness.     

Impacts of the swimbladder nematode Anguillicola crassus on Anguilla anguilla: variations in liver and spleen masses

Variations in the liver and spleen masses of the eel Anguilla anguilla were analysed in relation to the parasite load of Anguillicola crassus at autopsy (current infection by swimbladder lumen worms) and in relation to the severity of damage observed in the swimbladder (a way of assessing the intensity of past infections). None of these measures of parasite pressure were shown to account for variation in the relative liver mass, either when controlling for somatic mass or eel age. In marked contrast, a significant increase in spleen size was revealed in eels harbouring many lumen worms and also in eels with severe damage in the swimbladder. Splenic enlargement was nearly two‐fold higher among severely affected eels (harbouring more than seven lumen parasites and showing severe damage in the swimbladder) than among infection‐free eels (no lumen parasites and no pathological signs in the swimbladder). Several possible hypotheses are reviewed before arguing for an adaptive host response involving the haematological and immunological functions of the spleen. Indeed, among eels with no pathological signs in the swimbladder, the relative spleen mass was positively associated with the mass of lumen parasites, which suggests a hyper‐synthesis of blood cells by the spleen in response to the bloodsucking activity of lumen worms. Nevertheless, among eels with no lumen parasites at autopsy, there was still an increase in spleen size in relation to the severity of the swimbladder damage, which also suggests a hyper‐synthesis of splenic immune cells (lymphocytes and macrophages) in reaction to damaged tissues and particularly to larvae in the swimbladder wall.     

Water quality as a determinant of the composition of fish parasite communities

To investigate the relationship between fish parasite communities and water quality level, metazoan parasites were examined in 157 specimens of chub (Leuciscus cephalus L.), sampled in four lowland water courses (northern Italy): Ticino river (unpolluted), Naviglio Pavese Canal (slightly polluted), Lambro river near the Merone village (polluted) and near Monza (severely polluted). Dactylogyrus vistulae, Paradiplozoon ergensi, Bucephalus polymorphus, Acanthocephalus anguillae and larval stages of Tylodelphys clavata were found in all the sampled sites. The distribution of Lamproglena pulchella and Pomphorhynchus laevis was limited to the unpolluted and slightly polluted river sectors, while Asymphylodora tincae, glochidia, along with larval stages of Diplostomum spathaceum, were absent in the severely polluted site. The variability of the calculated infection indices (prevalence, mean abundance and mean intensity), the degree of interactivity among parasites, as well as parameters of species richness and diversity suggest that the structure of parasite communities are affected by the water contamination level.     

Proximate factors affecting the larval life history of Acanthocephalus lucii (Acanthocephala)

The growth and eventual size of larval helminths in their intermediate hosts presumably has a variety of fitness consequences. Therefore, elucidating the proximate factors affecting parasite development within intermediate hosts should provide insight into the evolution of parasite life histories. An experimental infection that resulted in heavy intensities of an acanthocephalan (Acanthocephalus lucii) in its isopod intermediate host (Asellus aquaticus) permitted the examination of parasite developmental responses to variable levels of resource availability and intraspecific competition. Isopods were infected by exposure to egg-containing fish feces, and larval infrapopulations were monitored throughout the course of A. lucii development. The relative rate of parasite growth slowed over time, and indications of resource constraints on developing parasites, e.g., crowding effects, were only observed in late infections. Consequently, the factors likely representative of resource availability to larval parasites (host size and molting rate) primarily affected parasite size in late infections. Moreover, at this stage of infection, competitive interactions, gauged by variation in worm size, seemed to be alleviated by greater resources, i.e., larger hosts that molted more frequently. The relatively rapid, unconstrained growth of young parasites may be worse for host viability than the slower, resource-limited growth of larger parasites.