Effects of the eyefluke, Diplostomum spathaceum, on the behaviour of dace (Leuciscus leuciscus)

The behaviour of dace infected with Diplostomum spathaceum was investigated in the laboratory. As the number of parasites present in the eye increased, the efficiency with which the fish fed on Gammarus pulex declined. The loss of efficiency was compensated for by an increase in the time devoted to feeding. Heavily infected fish spent more time in the surface layers of the water. This may increase the likelihood that a gull might eat the fish and thereby continue the life-cycle of the parasite. The parasite modifies the behaviour of its host in a way that increases the parasite's chances of survival at the expense of the host.     

Potential interactions between metazoan parasites of the Mayan catfish Ariopsis assimilis and chemical pollution in Chetumal Bay,Mexico

The effect of pollutants on the intensity of infection of metazoan parasites in the Mayan catfish, Ariopsis assimilis was investigated. Data were collected on pollutants and metazoan parasites from 76 catfish from five localities in Chetumal Bay in October, 1996. Nineteen pollutants (pesticides, polychlorinated biphenyls (PCBs) and polycyclic aromatic hydrocarbons (PAHs)) were found in the catfish livers. Heavy metal content was not determined. Nineteen metazoan parasite species were recovered. After controlling for fish length and sampling station, there was a significant negative linear relationship between the intensity of the larval digenean Mesostephanus appendiculatoides and 1,1,1,-trichloro-2,2-bis (4-chlorophenyl) ethane (DDT) concentrations. This negative relationship may be explained either by the effect of the pesticide on the mortality of (i) free-living larval forms, (ii) metacercariae in the fish, (iii) infected fish or (iv) intermediate host snails. There were significant differences between fish parasitized and not parasitized with M. appendiculatoides with respect to their DDT concentrations. There were also significant differences between the variances of the mean Clark's coefficient of condition values between catfish parasitized and not parasitized by M. appendiculatoides, with the variance of non-parasitized catfish being significantly larger. The results provided statistical evidence that DDT has a detrimental effect on M. appendiculatoides infection intensity. Furthermore, the significantly larger variance value of Clark's coefficient for non-parasitized fish suggested that DDT affects both the parasite and general host condition.     

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.     

The effects of parasite age and intensity on variability in acanthocephalan-induced behavioural manipulation

Numerous parasites with complex life cycles are able to manipulate the behaviour of their intermediate host in a way that increases their trophic transmission to the definitive host. Pomphorhynchus laevis, an acanthocephalan parasite, is known to reverse the phototactic behaviour of its amphipod intermediate host, Gammarus pulex, leading to an increased predation by fish hosts. However, levels of behavioural manipulation exhibited by naturally-infected gammarids are extremely variable, with some individuals being strongly manipulated whilst others are almost not affected by infection. To investigate parasite age and parasite intensity as potential sources of this variation, we carried out controlled experimental infections on gammarids using parasites from two different populations. We first determined that parasite intensity increased with exposure dose, but found no relationship between infection and host mortality. Repeated measures confirmed that the parasite alters host behaviour only when it reaches the cystacanth stage which is infective for the definitive host. They also revealed, we believe for the first time, that the older the cystacanth, the more it manipulates its host. The age of the parasite is therefore a major source of variation in parasite manipulation. The number of parasites within a host was also a source of variation. Manipulation was higher in hosts infected by two parasites than in singly infected ones, but above this intensity, manipulation did not increase. Since the development time of the parasite was also different according to parasite intensity (it was longer in doubly infected hosts than in singly infected ones, but did not increase more in multi-infected hosts), individual parasite fitness could depend on the compromise between development time and manipulation efficiency. Finally, the two parasite populations tested induced slightly different degrees of behavioural manipulation.     

Interaction of a host plant and its holoparasite: effects of previous selection by the parasite

If parasites decrease the fitness of their hosts one could expect selection for host traits (e.g. resistance and tolerance) that decrease the negative effects of parasitic infection. To study selection caused by parasitism, we used a novel study system: we grew host plants (Urtica dioica) that originated from previously parasitized and unparasitized natural populations (four of each) with or without a holoparasitic plant (Cuscuta europaea). Infectivity of the parasite (i.e. qualitative resistance of the host) did not differ between the two host types. Parasites grown with hosts from parasitized populations had lower performance than parasites grown with hosts from unparasitized populations, indicating host resistance in terms of parasite’s performance (i.e. quantitative resistance). However, our results suggest that the tolerance of parasitic infection was lower in hosts from parasitized populations compared with hosts from unparasitized populations as indicated by the lower above‐ground vegetative biomass of the infected host plants from previously parasitized populations.     

Why do parasitized hosts look different? Resolving the “chicken-egg” dilemma

Phenotypic differences between infected and non-infected hosts are often assumed to be the consequence of parasite infection. However, pre-existing differences in hosts’ phenotypes may promote differential susceptibility to infection. The phenotypic variability observed within the host population may therefore be a cause rather than a consequence of infection. In this study, we aimed at disentangling the causes and the consequences of parasite infection by calculating the value of a phenotypic trait (i.e., the growth rate) of the hosts both before and after infection occurred. That procedure was applied to two natural systems of host–parasite interactions. In the first system, the infection level of an ectoparasite (Tracheliastes polycolpus) decreases the growth rate of its fish host (the rostrum dace, Leuciscus leuciscus). Reciprocally, this same phenotypic trait before infection modulated the future level of host sensitivity to the direct pathogenic effect of the parasite, namely the level of fin degradation. In the second model, causes and consequences linked the growth rate of the fish host (the rainbow smelt, Osmerus mordax) and the level of endoparasite infection (Proteocephalus tetrastomus). Indeed, the host’s growth rate before infection determined the number of parasites later in life, and the parasite biovolume then decreased the host’s growth rate of heavily infected hosts. We demonstrated that reciprocal effects between host phenotypes and parasite infection can occur simultaneously in the wild, and that the observed variation in the host phenotype population was not necessarily a consequence of parasite infection. Disentangling the causality of host–parasite interactions should contribute substantially to evaluating the role of parasites in ecological and evolutionary processes. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Nested assemblages resulting from host size variation: the case of endoparasite communities in fish hosts

Nested species subsets are a common pattern in many types of communities found in insular or fragmented habitats. Nestedness occurs in some communities of ectoparasites of fish, as does the exact opposite departure from random assembly, anti-nestedness. Here, we looked for nested and anti-nested patterns in the species composition of communities of internal parasites of 23 fish populations from two localities in Finland. We also compared various community parameters of nested and anti-nested assemblages of parasites, and determined whether nestedness may result simply from a size-related accumulation of parasite species by feeding fish hosts. Nested parasite communities were characterised by higher prevalence (proportion of infected fish) and intensities of infection (number of parasites per fish) than anti-nested communities; the two types of non-random communities did not differ with respect to parasite species richness, however. In addition, the correlation between fish size and the number of parasite species harboured by individual fish was much stronger in nested assemblages than in anti-nested ones, where it was often nil. These results were shown not to be artefacts of sampling effort or host phylogeny. They apply to both assemblages of adult and larval parasites, which were treated separately. Since species of larval parasites are extremely unlikely to interact with one another in fish hosts, the establishment of nestedness appears independent of the potential action of interspecific interactions. The species composition of these parasite communities is not determined from within the community, but rather by the extrinsic influence of host feeding rates and how they amplify differences among parasite species in probabilities of colonisation or extinction. Nested patterns occur in parasite communities whose fish hosts accumulate parasites in a predictable fashion proportional to their size, whereas anti-nested communities occur in parasite communities whose fish hosts do not, possibly because of dietary specialisation preventing them from sampling the entire pool of parasite species available locally. Thus, nestedness in parasite communities may result from processes somewhat different from those generating nested patterns in free-living communities.     

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.     

Assortative pairing with respect to parasite load in the beetle Timarcha maritima (Chrysomelidae)

Because of their effects on host reproductive behaviour, parasites are theoretically expected to create sometimes assortative mating among hosts, with heavily parasitized individuals pairing together and lightly parasitized ones pairing among themselves. We investigated the influence of protozoan gut parasites on the pairing pattern of the chrysomelid beetle Timarcha maritima. In the field, fecundity was negatively correlated with the parasite load of females, unpaired males were significantly more heavily infected than paired ones and, among pairs, males and females were matched for parasite load. Mate choice experiments in the laboratory showed that males have some ability to avoid heavily infected partners when given the choice between two females. Male competitiveness, measured as their mobility, was also negatively correlated with parasite load. These results indicate that parasite-related assortative pairing in this beetle could result from parasitized females being less fecund and parasitized males less competitive.     

Higher parasite richness, abundance and impact in native versus introduced cichlid fishes

Empirical studies suggest that most exotic species have fewer parasite species in their introduced range relative to their native range. However, it is less clear how, ecologically, the loss of parasite species translates into a measurable advantage for invaders relative to native species in the new community. We compared parasitism at three levels (species richness, abundance and impact) for a pair of native and introduced cichlid fishes which compete for resources in the Panama Canal watershed. The introduced Nile tilapia, Oreochromis niloticus, was infected by a single parasite species from its native range, but shared eight native parasite species with the native Vieja maculicauda. Despite acquiring new parasites in its introduced range, O. niloticus had both lower parasite species richness and lower parasite abundance compared with its native competitor. There was also a significant negative association between parasite load (abundance per individual fish) and host condition for the native fish, but no such association for the invader. The effects of parasites on the native fish varied across sites and types of parasites, suggesting that release from parasites may benefit the invader, but that the magnitude of release may depend upon interactions between the host, parasites and the environment.     

A double test of the parasite manipulation hypothesis in a burrowing bivalve

The parasite manipulation hypothesis predicts that parasites should be selected to manipulate host behaviour to facilitate transmission to the next host. The bivalve Macoma balthica burrows less deep when parasitized by the trematode Parvatrema affinis. Shallow burrowing increases the likelihood of ingestion by birds, their final hosts, and therefore this has been interpreted as manipulation by the parasite. When unparasitized, M. balthica displays seasonal changes in burrowing depth, becoming less accessible to predators in winter. If shallow burrowing of parasitized individuals is due to direct manipulation by the parasite, the availability of parasitized individuals should be high throughout the year, or at least especially in the season when most birds are present and potential transmission rates are highest. We compared burrowing depths of parasitized and unparasitized individuals in a single population during seven consecutive years. Parasitized individuals showed reduced burrowing depths but, in contrast to the prediction, the effect of parasites on availability to predators was smallest, not largest, in the season with the highest bird numbers. The parasite P. affinis competes for energy with the host, and M. balthica with low energy stores are known to reduce depth of burrowing. When we included size-corrected somatic ash-free dry mass (as an estimate of the energy stores) in our statistical analysis, the effect of infection on burrowing depth disappeared. Thus the effect of infection on burrowing depth is likely to be an unavoidable, indirect effect of the channelling of energy towards the parasite, causing the starving individual to take greater risks in the acquisition of food. Since both the seasonal pattern and the magnitude of increased availability of parasitized individuals are inadequate, the increased exposure of parasitized M. balthica to the final host does not seem to represent an example of adaptive host manipulation by the parasite.     

Parasite mediated mortality and host immune response explain age-related differences in blood parasitism in birds

An important pattern in host-parasite assemblages is a higher intensity of parasites in juveniles than in adults, but the reasons for these differences remain obscure. Three non-mutually exclusive hypotheses have been proposed: (1) heavily parasitized juveniles die before being recruited into the adult population ('selection' hypothesis); (2) the development of an acquired immunity by the host in front of the parasite reduces the intensity of the parasite in adult hosts ('immunity' hypothesis); and (3) differences in behavior makes adults less exposed to the parasite than juveniles ('vector exposure' hypothesis). Having rejected the 'vector exposure' hypothesis in a previous study, here we tested the 'selection' and 'immunity' hypotheses in feral pigeons (Columba livia) infected by the blood parasite Haemoproteus columbae. In agreement with the 'selection' hypothesis, young (but not adult) pigeons that were highly parasitized had a lower probability of surviving until adulthood, independent of their body condition. However, selection was not strong enough to account for the observed differences in parasite intensity between age-classes, and after selection parasite intensity of survivors still remained 85% higher in juveniles than in adults. In contrast, the 'immunity' hypothesis offered a greater explanatory power. The intensity of blood parasites in young pigeons, but not in adults, decreased over time so dramatically that by the time they had become adults their intensities were indistinguishable from that typically seen in adults. Therefore, while selection against highly parasitized juveniles can contribute to some extent to a reduction in parasitism seen in the adult population, age-specific blood parasitism in feral pigeons is best explained as a transitory phase just before the host develops an effective immune response.     

Circulation pattern and transmission dynamics of the supra-population of the nematode Cystidicoloides tenuissima (Zeder) in the River Swincombe, England

The circulation pattern and transmission dynamics of larval and adult Cystidicoloides tenuissima in all its intermediate and definitive hosts were investigated and quantified at three sites in a small upland stream over a period of 1 year. Both brown trout, Salmo trutta , and salmon parr, S. salar , were suitable definitive hosts, but because of the greater importance of the mayfly intermediate host in the diet of trout, between 73 and 98% of the parasite infrapopulation in fish circulated through this species. Trout was the only required host, and was alone responsible for the perpetuation of the parasite suprapopulation in the river. Around 99% of the parasite's eggs produced originated from trout but, of these, 90% or more failed to be ingested by an insect. Larval parasites were found in 18 species of insects, but could develop to the infective third stage in only one species, the mayfly Leptophlebia marginata. Two common but unsuitable species harboured up to 80% of the larval parasites, and less than 10% actually circulated through L. marginata. Differences in circulation pattern between sites could be related more to differences in fish feeding preferences than to differences in fish or insect density, but monthly differences in transmission rate reflected both fish diet and insect abundance. The overall mean transmission rate of eggs to larvae in L. marginata varied between 0.25 and 0.87%, but transmission rates of these larvae to fish were far higher, from 10.8 to 39.8%. The relative importance of ecological factors, host community structure and parasite specificity in determining circulation routes and transmission efficiencies are discussed.     

Histopathological changes caused by Enteromyxum leei infection in farmed sea bream Sparus aurata

Histological examinations were carried out on the stomach, pyloric caeca and 4 different parts of the intestine, as well as the rectum, hepatopancreas, gall bladder and spleen of 52 sea bream Sparus aurata spontaneously infected by Enteromyxum leei. Fifteen fish from a non-infected farm were included as a control. Clinical signs appeared only in extensively and severely infected fish. We observed Enteromyxum leei almost exclusively in the intestinal tract, and very rarely in the intrahepatic biliary ducts or gall bladder. We observed heavily infected intestinal villi adjacent to parasite-free villi. Histological changes indicated a parasite infection gradually extending from villus to villus, originating from an initial limited infected area probably located in the rectum. The parasite forms were exclusively pansporoblasts located along the epithelial basement membrane. Periodic acid-Schiff (PAS)-Alcian blue was the most useful histological stain for identifying the parasite and characterising the degree of intestinal infection. We observed severe enteritis in infected fish, with inflammatory cell infiltration and sclerosis of the lamina propria. The number of goblet cells was considerably and significantly decreased in heavily infected fish. The intestines of 4 of the 5 survivor fish were totally free of parasites and showed severe chronic enteritis with a regenerative epithelium, suggesting that an acquired immune process may spontaneously eliminate parasites.     

Effects of Acanthocephalus lucii (Acanthocephala) on intermediate host survival and growth: implications for exploitation strategies

Intermediate host exploitation by parasites is presumably constrained by the need to maintain host viability until transmission occurs. The relationship between parasitism and host survival, though, likely varies as the energetic requirements of parasites change during ontogeny. An experimental infection of an acanthocephalan (Acanthocephalus lucii) in its isopod intermediate host (Asellus aquaticus) was conducted to investigate host survival and growth throughout the course of parasite development. Individual isopods were infected by exposure to fish feces containing parasite eggs. Isopods exposed to A. lucii had reduced survival, but only early in the infection. Mean infection intensity was high relative to natural levels, but host mortality was not intensity dependent. Similarly, a group of naturally infected isopods harboring multiple cystacanths did not have lower survival than singly infected isopods. Isopods that were not exposed to the parasite exhibited sexual differences in survival and molting, but these patterns were reversed or absent in exposed isopods, possibly as a consequence of castration. Further, exposed isopods seemed to have accelerated molting relative to unexposed controls. Infection had no apparent effect on isopod growth. The effects of A. lucii on isopod survival and growth undermine common assumptions concerning parasite-induced host mortality and the resource constraints experienced by developing parasites.     

The liver stage of Plasmodium berghei inhibits host cell apoptosis

Plasmodium berghei is the causative agent of rodent malaria and is widely used as a model system to study the liver stage of Plasmodium parasites. The entry of P. berghei sporozoites into hepatocytes has extensively been studied, but little is known about parasite-host interaction during later developmental stages of the intracellular parasite. Growth of the parasite far beyond the normal size of the host cell is an important stress factor for the infected cell. Cell stress is known to trigger programmed cell death (apoptosis) and we examined several apoptotic markers in P. berghei-infected cells and compared their level of expression and their distribution to that of non-infected cells. As none of the apoptotic markers investigated were found altered in infected cells, we hypothesized that parasite infection might confer resistance to apoptosis of the host cell. Treatment with peroxide or serum deprivation induced apoptosis in non-infected HepG2 cells, whereas P. berghei-infected cells appeared protected, indicating that the parasite interferes indeed with the apoptotic machinery of the host cell. To prove the physiological relevance of these results, mice were infected with high numbers of P. berghei sporozoites and treated with tumour necrosis factor (TNF)-alpha/D-galactosamine to induce massive liver apoptosis. Liver sections of these mice, stained for degraded DNA, confirmed that infected cells containing viable parasites were protected from programmed cell death. However, in non-treated control mice as well as in TNF-alpha-treated mice a small proportion of dead intracellular parasites with degraded DNA were detected. Most hepatocytes containing dead parasites provoked an infiltration of immunocompetent cells, indicating that these cells are no longer protected from cell death.     

Geographical variation in blood parasites in feral pigeons: the role of vectors

Prevalence and intensity of blood parasites are known to vary in space within a same species, yet the causes underlying such variation are poorly known. Theoretically, blood parasites variation can be attributed to differences to exposure to parasite vectors and/or to differences in host susceptibility. Here, we show that prevalence of Haemoproteus columbae in feral pigeons Columba livia varied among five near-by populations (range 15%-100%), paralleled by variation in the abundance of its main vector, the louse flies Pseudolynchia canariensis. Geographic variation in intensity of blood parasites did not covary with abundance of vectors. Within populations, older individuals had a higher probability of being parasitized than younger ones, whereas younger birds, when infected, suffered higher intensities. Furthermore, we found no evidence of sex-related differences neither in prevalence nor in intensity of blood parasite infections. To demonstrate that geographical variation in prevalence was actually due to differences in vector exposure, we conducted two experiments based on translocation of unparasitized pigeons from a vector-free area to an area where both the parasite and vector were abundant. With the first experiment, we demonstrated that unparasitized pigeons were not resistant to the parasite because when transmission was possible pigeons became parasitized in a few months. With the second experiment, in which half of the pigeons were prevented from contacts with the vector, we ruled out the posibility that pigeons we considered as unparasitized would have suffered from latent infections. Therefore, both observational and experimental evidence supports the view that vector abundance is the major factor influencing the spatial variation in prevalence of H. columbae in pigeons.     

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.     

Impact of a caged-trout farm on parasites of Galaxias maculatus in Lake Moreno, southern Argentina

The present study was conducted to determine the impact of a caged-trout farm on the helminth parasites of the wild fish puyen chico (Galaxias maculatus) in Lake Moreno, southern Argentina. Samples of water, fish (G. maculatus), and snails (Heleobia hatcheri) were taken at 4 sampling stations in January 2001. Wild fish were parasitized by 8 helminth species, all of which are endemic in the region; therefore, the farm did not introduce any helminth parasite to G. maculatus. Fish captured near the farm were not infected by the digenean Steganoderma szidati, whereas the abundance of the digenean Acanthostomoides apophalliformis in these fish was significantly lower than that in fish captured away from the farm. This lower abundance may be explained by the absence in this area of the snail H. hatcheri, the parasite's first intermediate host, because of the effect of sediments and ammonium produced by the farm. To our knowledge, this is the first study in the Americas linking fish-farm pollution to helminth parasites in wild fish.