Effect of Triaenophorus crassus (Cestoda) infection on behavior and susceptibility to predation of the first intermediate host Cyclops strenuus (Copepoda)

Some parasites have been shown to manipulate host behavior so that parasite transmission to the next host is enhanced. Infection with Triaenophorus crassus Forel (Cestoda) caused alterations in the activity and microhabitat selection of the first intermediate host Cyclops strenuus Fischer (Copepoda) in the laboratory. Infected copepods made more starts to swim but spent less time swimming than uninfected copepods. These changes were independent of the intensity of infection. In a water column illuminated from above, infected copepods approached the surface, whereas uninfected ones remained close to the bottom. In the dark both infected and uninfected copepods stayed near the bottom. Finally, infection with T. crassus increased the probability of C. strenuus being eaten by the second intermediate host, whitefish (Coregonus lavaretus L. s.l.), in the laboratory. In experimental infections, 10-day-old procercoids had significantly lower infectivity for whitefish than older (12-, 14-, and 21-day-old) procercoids. Behavioral changes were detected in infected copepods containing procercoids 12 days old or older but not in experiments with 10-day-old procercoids. These results may indicate that T. crassus changes the behavior of the copepod host only after it has become infective to the next host, which is consistent with the active manipulation hypothesis.     

The influence of food competition and host specificity on the transmission of Triaenophorus crassus (Cestoda) and Cystidicola farionis (Nematoda) to Coregonus lavaretus and Coregonus albula (Pisces:Coregonidae) in Finland

As a superior competitor for planktonic food, vendace (Coregonus albula), when abundant, is expected to displace whitefish (Coregonus lavaretus) from feeding on plankton and to force it to rely more on benthic food. The predicted result would be a reduced abundance of the copepod-transmitted cestode Triaenophorus crassus in whitefish, but an increase in the abundance of the nematode Cystidicola farionis transmitted via benthic amphipods. We studied the occurrence of both parasites in whitefish during 1991-1996 in three interconnected areas at Lake Saimaa, Finland, where the densities of the vendace stocks varied due to natural fluctuation in year-class strengths. In accordance with our hypothesis, some indication of the effect of the density of the vendace population on abundance of C. farionis infection in whitefish was found, but not in the case of T. crassus. Only 0.2% of vendace were infected with T. crassus, while up to 100% of the whitefish in the yearly samples harboured the parasite. In further experiments we clarified which copepod species in Lake Saimaa act as first intermediate hosts of T. crassus, and verified from stomach samples the exposure of both whitefish and vendace to those species. Experimental infections indicated that the infectivity of T. crassus is lower for vendace than for whitefish. We suggest that the reason why vendace stock density does not affect T. crassus infection in whitefish is that T. crassus is transmitted in littoral areas during a short period in spring. At that time of the year copepods are abundant and available to both whitefish and vendace, but since the parasite is less infective to vendace. they do not become infected. At other times of the year, dense vendace stocks may force whitefish to shift to benthic food, which includes amphipods transmitting C. farionis. During vendace stock decline, whitefish may, however, continue to feed on plankton and avoid exposure to C. farionis.     

Helminth position within the intestine of naturally infected pike (Esox lucius) relative to host stomach contents

The positions of 3 cestode species, Triaenophorus crassus Forel, Triaenophorus nodulosus (Pallas), and Proteocephalus pinguis LaRue, and a nematode, Raphidascaris acus (Bloch), within the intestine of naturally infected pike (Esox lucius L.) were evaluated with respect to the presence or absence and state of digestion of host stomach contents. The positions of scolices and strobilae of the cestodes did not vary with respect to host stomach contents. By contrast, R. acus was anterior (near the stomach) when the stomach contained partially digested items, posterior when the stomach was empty, and in an intermediate position when the stomach contained only intact items. These results are interpreted as migration of R. acus, but not T. crassus, T. nodulosus, or P. pinguis, in response to feeding activity of the host. Adult and larval R. acus migrated, but the extent of migration was reduced in hosts harboring T. crassus, more so for larval than adult R. acus.     

A population analysis of the variability of the hooklets in the cestode Triaenophorus crassus

The paper presents data on the variability of attachment organs in the cestode Triaenophorus crassus, a parasite of freshwater fishes. The greatest range of variability of all the characters is typical of whitefish, a fish with a long life cycle, while the shortest one is characteristic of vendace and young of trout. It is suggested that the stay of the parasite in fishes, associated with host age, is accompanied by the increase in average sizes of hooks and variability range. Such an approach together with the analysis of hooks variability gives the possibility to estimate the participation of secondary intermediate hosts in the circulation of the parasite in the water body.     

Accumulation of plerocercoids of Triaenophorus crassus in the second intermediate host Coregonus lavaretus and their effect on growth of the host

Patterns of accumulation of Triaenophorus crassus in its second intermediate host whitefish Coregonus lavaretus s.l. were studied between 1991 and 1996 from two host populations in two separate areas of Lake Saimaa, Finland. Whitefish were infected commonly with several T. crassus plerocercoids and the parasites were aggregated into the oldest hosts. In one host population the annual parasite accumulation was 0·9 parasites in all host age groups between 3 and 8 years. In the other host population the annual accumulation was 1·6 parasites in 3–5-year-old fish, but increased up to 3 to 4 parasites per year in fish over 5 years old. The increase did not coincide with the period of maturation or any increase in whitefish growth, both of which could alter the food intake of the fish. The sharp increase in the annual accumulation suggests a threshold intensity above which the probability of acquiring further parasites increases. In spite of a heavy aggregation of parasites there was no evidence of parasite-induced host mortality. The annual increase in mean abundance was not correlated with the mean annual weight increase in 2–4-year-old fish within cohorts. However, evidence of a negative effect of parasites on whitefish growth was revealed by back-calculation of lengths of uninfected and infected whitefish and correlations between length or weight of fish and intensity of infection with fish age. Both analyses suggested that larger young fish harboured more parasites than the smaller ones while in older fish the reverse was true, a pattern that has not been shown earlier for parasitized fish.     

Species composition and specific features of distribution of bivalves from the superfamily Pisidioidea (Mollusca, Bivalvia) in the coastal zone of the Lower Tuloma Reservoir and in the Tuloma River Estuary (Kola Peninsula, Russia)

The fauna of bivalves of superfamily Pisidioidea from the coastal zone of the Lower Tuloma Reservoir and the estuary of the Tuloma River was studied in 2004–2005. Seventeen species mollusks were found. The influence of some ecological factors on the mollusks is analyzed. The most important factor in the Lower Tuloma Reservoir is the tidal rise; in the estuary of the Tuloma River, it is the time of coast exposure and water salinity.     

Diapause of copepods as an element for stabilizing the parasite system of some fish helminths

The analysis of infection dynamics of copepods, which are the intermediate hosts of three helminth species of freshwater fishes (Triaenophorus crassus, Proteocephalus exiguus and P. percae), has shown that diapause in the life cycle of the copepods is favourable for preserving the infection in the waterbody until physiological prerequisites for successful infection of the final host are acquired. The peculiarity of a copepod's life cycle may determine the strategy of a parasite in its preimaginal phase as a waiting stage, and the duration of the residence of helminth larvae in copepods that have an obligatory diapause, is one of the elements the provide stability in parasite systems.     

'Global worming': first record of an epidemic of Triaenophorus crassus in a population of Arctic charr Salvelinus umbla

In May 2005, an epidemic of the cestode Triaenophorus crassus occurred in the Salvelinus umbla population of Lake Grundlsee, an oligotrophic Austrian Alpine Lake. Based on catches with a standardized multi-mesh gillnet survey 53% of S. umbla were infected with up to 17 cysts of T. crassus per fish. This is the first documented record of an epidemic of this tapeworm in S. umbla .     

Circulation of parasites among fishes from lakes in the Caribou Mountains,Alberta, Canada

Circulation of 24 macroparasite species among 12 species of fish was evaluated within samples of hosts collected from 9 lakes on an isolated plateau in northern Alberta, Canada. Twenty-seven parasite taxa (24 species plus the larval stages of Triaenophorus crassus, T. stizostedionis, and Raphidascaris acus) had the potential to be circulated among hosts. Sixteen parasite taxa were recovered from a single host species within a lake. Of the 11 remaining nonspecialist taxa, 4 were larval stages that matured in fish or birds and 7 were adults. Eight of the 11 cases of circulation among hosts involved lake whitefish, and this host was involved in the transmission of 5 species to piscivorous fishes. Despite evidence for the circulation of 7 taxa among the 4 species of sympatric Salmonidae, 60-99% of all worms were recovered from just 1 species of host. These results indicated that approximately 60% of the parasite taxa that infected fish in these lakes were absolute host specialists. The remaining 40% of parasite taxa had restricted host ranges, with most examples of parasite circulation limited to the 2 species of sympatric coregonid.     

The helminth parasites of the bullhead Cottus gobio (L.) and the stone loach Noemacheilus barbatulus (L.) from the River Avon, Hampshire

Specimens of Cottus gobio and Noemacheilus barbatulus from the River Avon, Hampshire, were examined between July 1970 and July 1971. Both fish were found to act as hosts for Nicolla gallica (adult), Pomphorhynchus laevis (adult) and Triaenophorus nodulosus (plerocercoid). The incidence and intensity of infection were lower in N. barbatulus than in C. gobio , and this was related to differences in host diet. A small number of N. barbatulus were also found to harbour Proteocephalus torulosus . Seasonal cycles of incidence and intensity were evident in N. gallica , with a peak occurring in the winter. P. laevis and T. nodulosus showed no such cycles. Increasing host size was associated with a higher infection of both N. gallica and P. laevis , but not T. nodulosus . The diet of the host was considered to be important in influencing this increase. Differences in host reproductive condition affected the population levels of N. gallica only, where an increased parasite burden was evident in gravid female fish. This was considered to influence the observed increase in incidence and intensity of this parasite during the winter. None of the parasites showed any seasonal maturation cycles. There was no evidence of any interactions between the parasite populations. Host diet and the availability of infective larvae were considered to be the most important features influencing the number of parasites which became established, and the rate at which this occurred. Temperature probably acted indirectly on the establishment of N. gallica , by controlling the availability of the larval stages, and also, by influencing the host reproductive condition, on the length of time for which the parasite was retained by the host.     

An example of anthropogeneous succession in the ecosystem of the Verkhnetulomsky Water Reservoir (the Tuloma River Basin, the Kola region)

The destruction of initial biocenoses in the ecosystem of the Verkhnetulomsky Water Reservoir caused deep succession processes. As a result of the loss of the amphipod group in the benthos, replacement of the trophic links in fishes took place in the biocenosis of the reservoir. Benthos feeders changed over to the feeding on zooplankton and, as a result, became the constituent of the predators'diet. The structure of parasitic systems has changed. The parasites using amphipods as intermediate hosts have been and, on the contrary, the abundance of parasites infesting fishes through feeding of the latter on zooplankton has increased. Among the parasites, Triaenophorus crassus Forel became the cause of the appearance of stable triaenophorosis focus.     

An invasion record for the swimbladder nematode Anguillicoloides crassus in European eel Anguilla anguilla in a deep warm-monomictic [corrected] lake, from invasion to steady state

This study is the first account of the establishment and development of the neozoic nematode parasite Anguillicoloides crassus in its host, the European eel Anguilla anguilla, in a deep, warm-monomictic [corrected] lake. A 21 year study of A. crassus took place in Upper Lake Constance (ULC), Europe's second largest pre-alpine lake. The study included two extensive surveys, one in 1991 during the initial parasite invasion phase and the second in 2006 when the infection was well established. The subtropical swimbladder nematode A. crassus was first recorded in A. anguilla in ULC in 1989. Prevalence reached 60% in 1992 and remained at this level until 2007. In 2008, prevalence decreased to 48%. Infection intensity peaked in 1993 at a mean value of 16 adult parasites per host fish. Around 90% of all A. anguilla examined displayed swimbladder lesions, with a significant trend to increasing severity over time. Moreover, heavy swimbladder lesions were seen in c. 10% of A. anguilla ready to migrate to their spawning habitat. Both ruffe Gymnocephalus cernuus and sunfish Lepomis gibbosus serve as paratenic hosts for A. crassus in ULC. Gymnocephalus cernuus seems to be the main vector, and infection is especially frequent in spring possibly caused by reduced immune system efficacy of G. cernuus during winter. In 1991, hypochromic anaemia was prevalent in ULC A. anguilla acutely infected with A. crassus, whereas in 2006 blood values were indicative of chronic infection. The growth and survival rates of A. anguilla during their continental phase were not noticeably altered in infected fish, but damage to the swimbladder probably impairs migration potential and thus the subsequent breeding success of the oceanic phase.     

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'.     

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.     

Infectivity of two nematode parasites, Camallanus lacustris and Anguillicola crassus, in a paratenic host, the three-spined stickleback Gasterosteus aculeatus

Three-spined sticklebacks Gasterosteus aculeatus are frequent paratenic hosts of the nematode parasites Anguillicola crassus and Camallanus lacustris. As paratenic hosts, sticklebacks could spread infection by carrying high numbers of infective stages. In contrast, low infective ability of either parasite for the paratenic host could hinder the spread of infection. In the present study, G. aculeatus was, for the first time, infected under controlled laboratory conditions with defined doses of the parasites. Sticklebacks were exposed to 6, 12, 18 and 24 parasite larvae to determine the infective ability of the 2 nematode species. There were significantly higher infection rates for C. lacustris (18 to 49%) than for A. crassus (4 to 14%) at each exposure dose. In C. lacustris-infected sticklebacks, infection rates tended to be highest after exposure to 12 C. lacustris larvae and lowest after exposure to 24 parasites. In A. crassus-infected sticklebacks, no effect of parasite exposure dose on infection rates was observed. Immunity parameters such as respiratory burst activity and lymphocyte proliferation of head kidney leukocytes recorded 18 wk post exposure were not significantly affected by either parasite or exposure dose. Granulocyte:lymphocyte ratios were elevated only within the stickleback group showing the highest infection intensity of C. lacustris, i.e. to those exposed 18 parasites.     

Metazoan parasites of whitefish Coregonus clupeaformis (Mitchill) and cisco C. artedii Lesueur from Southern Indian Lake, Manitoba

Metazoan parasites of whitefish Coregonus clupeaformis and cisco C. artedii from Southern Indian Lake, Manitoba were studied to reveal: species composition, differences with host age, sex, and location and season of capture. Whitefish hosted 19 species, 18 of which were also in cisco with generally lower intensity levels. Parasites exhibited definite patterns of abundance with host age and season, the primary causes being dietary and behavioural. No differences in parasite abundance existed between host sexes. Ranking of cisco parasites was significantly different between two sampling sites while whitefish parasites did not differ. Whitefish and cisco from sites 40 miles (64 km) apart had significantly different abundances of Tetracotyle intermedia but not Triaenophorus crassus . An increase in the abundance of copepod-vectored cestodes with a concomitant decrease in abundance of amphipod-vectored parasites is predicted after flooding and diversion.     

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.     

The karyotypes of Triaenophorus nodulosus and T. crassus (Cestoda: Pseudophyllidea)

Two species of the genus Triaenophorus were found to have widely different chromosome sets. The karyotype of T. nodulosus consists of 26 biarmed chromosomes ranging from 1.45 to 6.75 microns long. The diploid set of T. crassus contains 18 chromosomes with a well-distinguished first pair of large metacentric homologues. All the chromosomes with the exception of the last pair of acrocentric elements are biarmed. Their absolute length ranges from 1.50 to 8.50 microns. The possible pathways of karyotype differentiation and the evolution of these species are discussed.     

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.