The population biology of the acanthocephalan Pomphorhynchus laevis (Müller) in the River Avon

Regular samples of Gammarus pulex and dace Leuciscus leuciscus and occasional grayling Thymallus thymallus and chub L.cephalus were examined from the River Avon, Hampshire, for the presence of the acanthocephalan Pomphorhynchus leavis . The parasite only occurred in medium sized Gammarus due to lower probability of contact with small gammarids and stunted growth and selective mortality amongst older infected ones. No cycles in incidence or development of the parasite in G.pulex were observed. The parasite infected gammarids and grew in all months, and cystacanths were available throughout the year. Despite seasonal feeding activity and dietary preferences, fish fed on Gammarus and acquired infections in all months. Dispersion of P.laevis within the fish population was related to host feeding behaviour. No evidence of seasonal cycles in incidence or intensity of infection in fish was found, and observed monthly changes in the parasite population were related to changes in size structure of the host sample. In dace and grayling P.laevis grew little and matured only in summer, but in chub it grew and produced acanthors all year. The parasite population in fish appeared to be in a state of dynamic equilibrium and gain and loss of parasites took place throughout the year with the level of infection at any moment being determined primarily by the feeding behaviour of the host. This relationship between host diet, water temperature and parasite population size is discussed, and P.laevis in the R. Avon compared with other localities and other parasites.     

Patterns of intermediate host use and levels of association between two conflicting manipulative parasites.

For many parasites with complex life cycles, manipulation of intermediate host phenotypes is often regarded as an adaptation to increase the probability of successful transmission. This phenomenon creates opportunities for either synergistic or conflicting interests between different parasite species sharing the same intermediate host. When more than one manipulative parasite infect the same intermediate host, but differ in their definitive host, selection should favour the establishment of a negative association between these manipulators. Both Polymorphus minutus and Pomphorhynchus laevis exploit the amphipod Gammarus pulex as intermediate host but differ markedly in their final host, a fish for P. laevis and a bird for P. minutus. The pattern of host use by these two conflicting manipulative parasites was studied. Their incidence and intensity of infection and their distribution among G. pulex were first examined by analysing three large samples of gammarids collected from the river Tille, Eastern France. Both parasites had low prevalence in the host population. However, temporal fluctuation in the level of parasitic infection was observed. Overall, prevalence of both parasite species was higher in male than in female G. pulex. We then assessed the degree of association between the two parasites among their intermediate hosts, using two different methods: a host-centred measure and a parasite-centred measure. Both measures gave similar results; showing random association between the two acanthocephalan species in their intermediate hosts. We discuss our results in relation to the selective forces and ecological constraints that may determine the pattern of association between conflicting manipulative parasites.     

Observations on the distribution, specificity and pathogenicity of the acanthocephalan Pomphorhynchus laevis (Müller)

The distribution, specificity and pathogenicity of the acanthocephalan Pomphorhynchus laevis (Müller) were studied in the River Avon, Hampshire. The parasite occurred in every fish species, but three categories of hosts could be distinguished. Using growth and maturation as criteria of specificity, only chub Leuciscus cephalus (L.) and barbel Barbus barbus (L.) were recognized as its preferred hosts. Parasites occasionally matured in trout Salmo trutta (L.) and dace Leuciscus leuciscus (L.), but none grew or matured in other host species. Changes in the abundance of P. laevis along the river were related to changes in the abundance of both the intermediate host, Gammarus pulex , and the preferred hosts, and its occurrence in fish to the importance of G. pulex in their diet. In the upper reaches of the River Avon and in other localities populations could be maintained at a low level by parasites maturing in trout, and presence and abundance at any site depended upon the presence and abundance of both intermediate and definitive hosts especially and upon the dietary preferences of the latter. The absence of P. laevis from many parts of Britain is nevertheless still inexplicable. The parasite caused local damage to the intestinal wall of fish, the extent of which varied from species to species, but did not affect host growth rate or cause direct mortality and P. laevis cannot be regarded as an important pathogen in the River Avon or any other British River.     

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.     

The effect of the acanthocephalan parasite (Pomphorhynchus laevis) on the drift of its intermediate host (Gammarus pulex)

SUMMARY 1. The drift of Gammarus pulex in a population in which approximately 20% of adults are infected with the acanthocephalan parasite Pomphorhynchus laevis was monitored at margin and mid-river sites in the River Teme, England over a 24-h period in mid-summer.
2. Drift densities showed a diurnal pattern with a large increase at night, independent of parasite burden.
3. There was no significant effect of site (margin or mid-river) on the proportion of parasitized and unparasitized G. pulex found in the drift or the benthos.
4. The drift of parasitized G. pulex was significantly greater than unparasitized animals. Gammarids harbouring only one parasite were found in significantly higher proportions in the drift than those with two or more parasites.
5. At both sites (margin and mid-river) the proportion of unparasitized adult G. pulex in the drift was significantly lower than that in the benthos. However, there was a significantly higher proportion of parasitized animals in the drift than in the benthos.     

Seasonal dynamics of the acanthocephalan Pomphorhynchm laevis (Müller, 1776) in its intermediate and preferred definitive hosts

No seasonal cycle was found in either the prevalence or the intensity of natural Pomphorhynchus laevis infections in Leuciscus cephalus . There was a slight seasonal change in female maturity distribution but only irregular fluctuations in the size structure of the adult parasite population throughout the year. Cystacanths were available in all seasons. Rates of parasite growth, maturation and mortality, but not establishment, increased with water temperature (or factors indirectly associated with elevated water temperature) in laboratory-infected Salmo gairdneri . Increased rates of parasite growth and maturation mask any marked shifts in the size and maturity structure of the adult parasite population which might otherwise be due to the higher turnover of adult parasites in the summer months.     

The population biology of two species of eyefluke, Diplostomum gasterostei and Tylodelphys clavata, in perch

Incidence, intensity and frequency distributions of infections in perch, Perca fluviatilis , with the eyeflukes Tylodelphys clavata and Diplostomum gasterostei were studied in a lake at monthly intervals over a period of two years. T. clavata had appeared in the lake immediately prior to the study, and its levels of infection continued to rise throughout the period of investigation whereas those of D. gasterostei remained relatively steady. The main period of infection of fish by both species of parasites was late summer, but a second and minor infection took place in spring. In the first year after its introduction T. clavata exhibited a seasonal cycle in incidence and intensity of infection and disappeared from fish in summer, but in the second year this cycle was masked by increased variation in development times and lack of synchrony throughout the parasite population. It is concluded that T. clavata has a life span of one year or less and that the parasites die within the fish, mainly in summer. D. gasterostei in contrast has a life span of at least one year, and disappearance of the parasite from the population is probably due to death of some heavily infected fish, although it was not possible to determine if this was due directly to the presence of the parasite.     

The status of brown and rainbow trout, Salmo trutta and S. gairdneri as hosts of the acanthocephalan, Pomphorhynchus laevis

The status of brown and rainbow trout as hosts of Pomphorhynchus laevis was studied in the field and by means of laboratory investigations. Field data indicated that rainbow trout might belong to the group of preferred hosts of P. laevis , whereas brown trout belonged to the group in which the parasite achieved less than optimal growth and maturation. This was confirmed by laboratory infections. In rainbow trout P. laevis attained up to three times the growth rate in brown trout and maturation occurred whereas in brown trout establishment was lower, growth slower and no parasites matured. Changes in the behaviour of infected Gammarus pulex induced by the presence of P. laevis cystacanths were such as to render the shrimps more vulnerable to predation by trout and other surface and mid-water feeding fish, and selective predation upon infeged G. pulex by fish was demonstrated. nvestigations into the stimuli necessary for eversion of cystacanths of P. laevis revealed that the most important factor was a non-specific component of bile, and it was concluded that cystacanths were likely to evert in any species of fish. Recognition of the different status of brown and rainbow trout as hosts of P. laevis still fails to explain some peculiarities in the distribution of the parasite in the British Isles, where in Britain it occurs in trout in only one river but in Ireland in all rivers throughout the country. It is suggested that the Irish parasites may constitute a different strain of P. laevis , since they use a different species of intermediate host and are better able to survive in brown trout.     

Parasitic infection manipulates sodium regulation in the freshwater amphipod Gammarus pulex (L.)

The acanthocephalan parasite Polymorphus minutus induces both physiological and behavioural effects in its intermediate host, Gammarus pulex. The net effect of parasite infection is to increase the likelihood of transmission to the definitive host. Osmoregulation is an energetically expensive mechanism that allows G. pulex to survive in dilute media. Any factor influencing osmoregulation is thus likely to affect the allocation of resources to other areas. This study investigated whether P. minutus infection alters sodium regulation in G. pulex. Haemolymph sodium concentration, water permeability and sodium fluxes were measured over the salinity acclimation range of G. pulex. Water permeability was unaltered by either acclimation salinity or parasite infection. Acclimation to 12‰ significantly raised the haemolymph sodium concentration, reduced the sodium influx, and increased the sodium efflux, to the same extent in both uninfected and infected G. pulex. However, parasite infection induced a significant increase in haemolymph sodium concentration in G. pulex acclimated to 6‰, which was not observed in uninfected G. pulex acclimated to the same salinity. Also, both sodium influx and sodium efflux were significantly lower in parasitized G. pulex acclimated to 6‰, when compared to uninfected G. pulex acclimated to the same salinity. It was concluded that the parasite induced disturbances to sodium regulation in G. pulex acclimated to 6‰ were a functional consequence of the manipulative strategy employed to alter behaviour, rather than a primary target.     

The effect of the acanthocephalan parasite Pomphorhynchus laevis on the lipid and glycogen content of its intermediate host Gammarus pulex

Besides conspicuous changes in behaviour, manipulative parasites may also induce subtle physiological effects in the host that may also be favourable to the parasite. In particular, parasites may be able to influence the re-allocation of resources in their own favour. We studied the association between the presence of the acanthocephalan parasite, Pomphorhynchus laevis, and inter-individual variation in the lipid and glycogen content of its crustacean host, Gammarus pulex (Amphipoda). Infected gravid females had significantly lower lipid contents than uninfected females, but there was no difference in the lipid contents of non-gravid females and males that were infected with P. laevis. In contrast, we found that all individuals that were parasitised by P. laevis had significantly increased glycogen contents, independent of their sex and reproductive status. We discuss our results in relation to sex-related reproductive strategies of hosts, and the influence they may have on the level of conflict over energy allocation between the host and the parasite.     

Population biology of Camallanus oxycephalus Ward and Magath, 1916 (Nematoda: Camallanidae) in white bass in western Lake Erie.

The distribution and abundance of the nematode Camallanus oxycephalus infecting white bass, Morone chrysops, in western Lake Erie was studied for over 2 years. Infection was generally more frequent and of higher intensity in large fish. The frequency distributions of nematode abundance in all segments of the fish population followed the negative binomial distribution. The data show seasonal cycles in population structure, site selection, intensity of infection, maturation, and reproduction. Infection occurs during July and August with a resulting peak in population density; during late summer and autumn, mortality, probably density-dependent, reduces the population by 30 to 60%; surviving worms are eliminated at 1 year of age. Growth and development of female worms is arrested from November to April, then proceeds at a rapid rate until the worms release their larvae and die. This growth pattern is probably related to temperature but may also involve host hormone cycles. The dispersal period of the nematode coincides with the annual maximum density of the intermediate host, a cyclopoid copepod,and is interpreted as an adaptation which increases the probability of successful transmission. Because the number of larvae produced by each female worm is a function of body volume, natural selection has favored rapid spring growth and attainment of large body size relative to the male worm. Both seasonal timing in the life cycle and the number of larvae produced are important factors in determining the abundance of this and perhaps other parasites. Evidence is presented suggesting that fluctuations of environmental parameters may disrupt the timing of transmission and alter the distribution and abundance of the parasite. It is hypothesized that the magnitude of such changes in parasite abundance may be related to the complexity of the host-parasite system.     

Field evidence of host size-dependent parasitism in two manipulative parasites

The distribution of parasites within host natural populations has often been found to be host age-dependent. Host mortality induced by parasites is the commonest hypothesis proposed for explaining this pattern. Despite its potential importance in ecology, the parasitism intensity in relation with the host age has rarely been studied in the field. The 2 manipulative acanthocephalans, Polymorphus minutus and Pomphorhynchus laevis, use the amphipod Gammarus pulex as an intermediate host, and their infection intensity and incidence among G. pulex populations were examined by analyzing 2 large samples of hosts collected in eastern France. Both parasites had low prevalence in the host populations, but their mean abundances were highly related with gammarid age. For the 2 acanthocephalans, results reported a disappearance or an absence of heavily infected hosts in the older host age classes. These results suggested that parasites that alter intermediate host behavior for enhancing their transmission success to the definitive host reduce the survival of their intermediate host. In conclusion, manipulative parasites might act as a mechanism regulating the density of gammarid populations.     

Host-parasite relationships of longnose dace, Rhinichthys cataractae, from the Ford River, Michigan.

A total of 1,115 longnose dace, Rhinichthys cataractae (family Cyprinidae), were examined for parasites from May 1983 through October 1986 from 3 localities in the Ford River in Michigan's Upper Peninsula. Thirteen parasite species (1 Monogenea, 2 Digenea, 2 Cestoda, 4 Nematoda, 1 Acanthocephala, 3 Protozoa) infected dace. The parasite faunas of dace, taxonomically and in species number, were similar between localities. Posthodiplostomum minimum minimum, Neascus sp., and Rhabdochona canadensis were the most common helminths infecting dace from each locality. The first 2 species did not exhibit consistent seasonal infection patterns between years, whereas the prevalence and mean intensity of R. canadensis in dace from the downriver locality were higher in summer 1983, 1984, and 1985. The intensity of infection of each of these helminth species significantly increased with host length. The prevalences and mean intensities of P. m. minimum, Neascus sp., and R. canadensis as well as the helminth infracommunity diversity were highest in dace from the upriver locality. The major factors that influenced parasite intensity were environmental factors that occurred when and where a fish began its life, the sequence of events that occurred in each habitat the fish encountered during its life, and the length of exposure (age of fish). Dace have isolationist helminth infracommunities arising from factors including ectothermy, a simple enteric system, restricted vagility, and being gape-limited. Allogenic helminths with indirect life cycles predominate in the depauperate helminth fauna of dace.     

The sites occupied by the acanthocephalan Pomphorhynchus laevis in the alimentary canal of fish.

The distribution of the acanthocephalan Pomphorhynchus laevis along the alimentary tract of several species of freshwaster fish was studied in both natural and experimental infections. The parasite exhibits a clear preference for a particular region of the alimentary canal, which differs from host species to host species, but it is capable of surviving in all regions of the intestine. In some species, but not in all, its growth rate may be reduced in regions outside of the preferred site. The parsite remains in the same site throughout the period of infection, emigrations occurring only preparatory to complete loss of the parasite from the host. The presence of cestodes in the region of the preferred site has no effect upon the distribution of the parasite. At high levels of infection the range of the parsite's distribution is extended. The feeding of larval parasites to fish by stomach tube also leads to an extension of range, whereas when fish are allowed to feed on cystacanths removed from their intermediate host the parasite establishes in a more anterior position than usual and in a site that it does not occupy to any extent in natural infections. It is concluded that the distribution of P. laevis in the alimentary canal of fish is determined primarily by the process of liberation, activation and establishment of the parasite, and that it normally attaches in the first available space and remains there. Unsuitable physico-chemical or feeding conditions affect only its growth, not the site that it occupies. It is suggested that P. laevis may be atypical in this respect.     

Infection with acanthocephalans increases the vulnerability of Gammarus pulex (Crustacea, Amphipoda) to non-host invertebrate predators

Phenotypic alterations induced by parasites in their intermediate hosts often result in enhanced trophic transmission to appropriate final hosts. However, such alterations may also increase the vulnerability of intermediate hosts to predation by non-host species. We studied the influence of both infection with 3 different acanthocephalan parasites (Pomphorhynchus laevis, P. tereticollis, and Polymorphus minutus) and the availability of refuges on the susceptibility of the amphipod Gammarus pulex to predation by 2 non-host predators in microcosms. Only infection with P. laevis increased the vulnerability of amphipods to predation by crayfish, Orconectes limosus. In contrast, in the absence of refuges, the selectivity of water scorpions, Nepa cinerea, for infected prey was significant and did not differ according to parasite species. When a refuge was available for infected prey, however, water scorpion selectivity for infected prey differed between parasite species. Both P. tereticollis- and P. laevis-infected gammarids were more vulnerable than uninfected ones, whereas the reverse was true of P. minutus-infected gammarids. These results suggest that the true consequences of phenotypic changes associated with parasitic infection in terms of increased trophic transmission of parasites deserve further assessment.     

Protection first then facilitation: a manipulative parasite modulates the vulnerability to predation of its intermediate host according to its own developmental stage

Many trophically transmitted parasites with complex life cycles manipulate their intermediate host behavior in ways facilitating their transmission to final host by predation. This facilitation generally results from lowering host's antipredatory defenses when the parasite is infective to the final host. However, a recent theoretical model predicts that an optimal parasitic strategy would be to protect the intermediate host from predation when noninfective, before switching to facilitation when the infective stage is reached. We tested this hypothesis in the fish acanthocephalan parasite Pomphorhynchus laevis using the amphipod Gammarus pulex as intermediate host. Gammarids parasitized by noninfective stage of P. laevis (acanthella) hid significantly more under refuges than uninfected ones. In addition, acanthella-infected gammarids were less predated upon by trout than uninfected ones. As predicted, a switch toward decreased antipredatory behavior of G. pulex and enhanced vulnerability to predation was found when P. laevis reached the stage infective to its final host. The parasites appear to be able to exploit plasticity in host antipredatory responses, and shift the host optimal response toward their own optimal balance.     

The population biology of two species of eyefluke, Diplostomum spathaceum and Tylodelphys clavata, in roach and rudd

Infections of roach ( Rutilis rutilus ), and rudd ( Scardinius erythrophthalmus ), by the eyeflukes Diplostomun spathaceum and Tylodelphys clavata were studied in a lake over a three year period. T. clavata first appeared at the beginning of the study. Roach were heavily infected by both parasites, whereas the rudd contained very few specimens of either species. A small number of roach-rudd hybrids were also examined, and appeared to have a susceptibility intermediate between the parental types.
Levels of T. clavata in roach increased throughout the study. This parasite had a life span of a year or less in the fish, and was continuously lost from the population. This loss was balanced by a minor infection period in April/May and a major one extending from August until January. The fish continued to accumulate infections until they reached a size of about 130 mm, but thereafter intensity fluctuated about the level reached.
D. spathaceum infections similarly increased throughout the period of study, and there was a suggestion of a wave of infection in the spring. This parasite has a much longer life span, and levels of infection increased with fish size, only falling in the largest, and therefore oldest, hosts.
The major changes in the parasite populations in the roach were reflected, to a lesser extent, in the rudd. Both species were over-dispersed, but the data from roach was too heterogeneous to fit to any theoretical models, whereas that from the rudd was found to conform to a Negative Binomial distribution.     

Lernaea cyprinacea (Copepoda, Lernaeidae) from crucian carp Carassius carassius from the Dlinnoje Lake in the middle stream of the Vychegda River

Till 1996 the Vychegda River's flood lakes at the territory of the biological station of the Syktyvkar University were overflowed every spring by water so that fishing took place from time to time. In 1996 a low flood level and intensive fishing resulted in the change of the infection rate of crucians by Lernaea, as well as in the change of the size and sex ratios of the crucian population in the Dlinnoje Lake. Thus, the size pattern of the crucian population became simpler, and it led to the changes in parasite-host relation. As a result, the intensity of the invasion of crucians by Lernaea cyprinacea have increased and the distribution of the parasite in the host population does not fit by the negative-binomial distribution. Crucian females and males play an equal role in the maintenance of the parasite population. In 1984 crucian females of medium and large body length played the main role in that process. Functions of other host groups (fishes of small body length, males) were different. Up to 2001 a significance of "k"-exponent of the negative-binomial distribution, describing the number of copepods in the mature part of crucian population, changed with a small range that suggests a stability of parasite-host relationship in the investigated crucian groups. We suppose that after a period of an unstable state in 1997-2000 the population of the parasite reached a new stable state.     

Larval morphology, genetic divergence, and contrasting levels of host manipulation between forms of Pomphorhynchus laevis (Acanthocephala)

Studies on parasite species with a wide geographic and ecological range may be confounded by still equivocal taxonomic identification. Here, we investigated genetic polymorphism and behavioural changes induced in a common intermediate host, in two different forms of Pomphorhynchus laevis based on the morphology of the larval infective stage (cystacanth). A 'smooth type' (S) and a 'wrinkled type' (W) of cystacanth were distinguished based on their surface and shape. We analysed sequence divergence at both nuclear (ribosomal gene 18S rDNA, and ribosomal internal transcribed spacers, ITS1/ITS2) and mitochondrial (cytochrome c oxidase subunit 1) genes of P. laevis cystacanths and adults at various geographical scales. A high level of sequence divergence at ITS1, ITS2 and cytochrome c oxidase subunit 1 (11, 8 and 20%, respectively) was found between these two forms. The divergence pattern consistently discriminated two groups independently of geographic origin or host, and was congruent with larval morphology. The two forms also strongly differed in the intensity of behavioural change induced in their common intermediate host, Gammarus pulex, with the S-type parasite inducing a positive phototactism, whereas W-type infected gammarids were as photophylic as uninfected ones. Overall, our data strongly support the specific status of these two forms. We suggest that smooth cystacanths correspond to P. laevis, whereas wrinkled cystacanths might correspond to the previously described and poorly documented, Pomphorhynchus tereticollis, considered a synonym of P. laevis. This study also confirms the value of a joint analysis of internal transcribed spacers and cytochrome c oxidase subunit 1 genes to biogeographic studies on these species. Finally, we emphasize the importance of linking morphological and biological characteristics of acanthocephalan cystacanths to molecular data, in the study of the evolutionary ecology and systematics of this group.     

Long-term stability in the population levels of the eyefluke Tylodelphys podicipina (Digenea: Diplostomatidae) in perch

Annual changes in the population size of the metacercariae of Tylodelphys podicipina in the eyes of perch in a small eutrophic lake were studied over ten years by following changes in prevalence, abundance and overdispersion of parasites throughout the life of each year class of fish. The population increased rapidly in the first two years after its introduction to the lake, but for the next six years fluctuated within very narrowly constrained limits before declining as a result of a catastrophic decline in the perch population. No evidence of parasite-induced host mortality was found: the decline in parasite abundance throughout the life of each year class was due to density-independent parasite mortality within the fish as a result of natural variation in the life span of the metacercariae. Levels of infection in the first year of a year class were determined principally by transmission processes, as transmission could only occur over a very brief period when release of cercariae from parent generation snails coincided with the presence of perch fry. Transmission appeared to be density-independent, and infection levels in perch to be determined by the dimensions of the transmission' window' and subsequently modified by parasite mortality. No evidence of host responses or any other regulatory factor of fish origin was found, and the infrapopulations in perch appear to be non-equilibrial and unstable. Although the possibility of regulatory processes acting on infrapopulations of the parasite in other hosts remains, the importance of transmission windows in determining infrapopulation levels in fish is emphasized.