title: The ecology of fish parasites with particular reference to helminth parasites and their salmonid fish hosts in Welsh rivers: a review of some of the central questions.
abstract: Ecological studies carried out in Welsh rivers on the feeding behaviour of salmonid fish, their helminth parasites and intermediate hosts in the early 1950s and in 1998 have been used as a basis to review the literature dealing with the following questions. First, how are the helminth populations dispersed in space-time? Second, to what extent are the distributional patterns and the life history strategies of the parasites influenced by physicochemical factors? Third, to what extent are populations of helmith parasites in salmonid fish influenced by host characteristics including the genome, sex, age, size, social position and Feeding behaviour? Fourth, are the populations of parasites regulated in a density-dependent manner? Fifth, do the parasites influence the survival and wellbeing of their salmonid hosts and the evolution of sex? Sixth, to what extent is the parasite community influenced by environmental changes including those of an anthropogenic nature and can the parasites be used as bioindicators of pollution? As with most parasites the helminth species found were highly overdispersed thus making it necessary to undertake a log10 (1 + x) conversion for statistical analyses. Statistical analyses confirm that the genome, age and sex of salmonid fish hosts, the station and seasonal change in radiation levels were significant factors in predicting the number of parasites. The evidence given supports the hypothesis that the feeding behaviour and habitat selection by the host fish, their position in the social hierarchy and the overdispersed nature of the transmission sites are the key factors in causing differences in the parasitic fauna related to host species, age, size and sex. Differences in the helminth parasite community related to station can be explained on the basis of differences in water types, sediments and chemistry. Although the evidence presented is in accord with the consensus view that temperature is correlated with seasonal changes in the abundance of many species of helminth parasites, it is argued that it may not be the direct causative mechanism. It is postulated that the life history strategy that results in a decline in abundance of the more vulnerable adult parasites in the gut of the salmonid hosts during the summer has arisen as a result of evolutionary pressures. At this time, the gut environment is particularly inhospitable because of the temperature-related enhancement of the host's immune mechanism and the increased gut turnover rate. In contrast, the larval stages in the immunologically and metabolically more benign intermediate host would be under less intensive selective pressures. It is postulated therefore that evolutionary pressures have caused the parasites to leave the definitive host and concentrate their reproductive efforts in the intermediate hosts during the warmer months. Evidence is given in support of the hypothesis that the parasite populations are regulated in a density-dependent manner and that the regulatory mechanisms may involve the host's immune mechanisms and intraspecies competition and interspecies competition of an exploitative or interference nature. Quantitative studies using 'K' factor analysis and biochemical research to elucidate the nature of the interference mechanisms are required to test this hypothesis. The absence of age-related resistance indicates an old and stable relationship in which the immunosuppressive and immunoavoidance mechanisms of the parasites and hosts, respectively, are in balance. This indicates that the introduction of novel parasites or new genetic strains of host fish could result in harmful epidemics. Despite causing tissue damage, there was no evidence of parasite-induced mortality among the salmonids in the Teifi. This finding is in accord with the generally accepted view that most freshwaters are not troubled by parasite problems. although parasites are present in abundance. In fact, parasite abundance in the salmonid fish in the Teifi was positively correlated with the condition factor and the adipose index. Two testable hypotheses were advanced to explain these observations. First, the more dominant well-conditioned fish in the hierarchy are more likely to acquire parasites because they ingest more food items and spend more time in sheltered habitats with depositing sediments where transmission mainly occurs. Second, the parasites may release factors that stimulate the host's immune and endocrinological systems to produce factors that enhance somatic growth and inhibit reproduction of the host. This benign relationship is considered to be indicative of long-term coevolution. The sex of the fish had a significant influence on the abundance of the parasites in total and also on particular species with the bias in all cases being in favour of the female fish. This review shows that sex bias in parasitism is generally not strong and that male bias in parasitism is not a general rule. Taken as a whole, the results fail to support most of the predictions based on the Hamilton-Zuk and the immunocompetence hypotheses. Possible hypotheses to explain why parasitism tends to be higher in female than in male trout include testosterone immunosuppression, corticosteroid-based immune suppression and differences between the size and behaviour of the sexes. However, the latter two hypotheses have more credence, although testosterone levels are higher in female than male trout. Between the early 1950s and 1998 there has been a marked decline in the prevalence, abundance and diversity of the helminth parasite communities in salmonid fish as well as their intermediate hosts. Possible reasons for these declines include heavy metal pollution, increased acidity and habitat degradation linked to changes in land use. It is concluded that although helminth parasites can provide supplementary information on pollution. the use of biotic indices based on the Biological monitoring working party (BMWP) or River invertebrate prediction and classification system (RIVPACS) methods are preferable. However, as these methods were designed to measure the impact of organic pollution they lack the sensitivity for measuring metal pollution. It is advocated therefore that new biomonitoring methods should be developed to measure the impact of heavy metal pollution using biotic indices based on the sampling of the susceptible invertebrate communities inhabiting depositing sediments in the transmission sites of helminth parasites.
authors.affiliation: School of Biological Sciences, University of Sussex, Falmer, Brighton, East Sussex, BN1 9QG, UK.
authors.forename: J D
authors.initials: JD
authors.lastname: Thomas
mesh_terms: D000818:Animals; D004463:Ecology; D005393:Fish Diseases / Q000453:epidemiology / Q000469:parasitology* / Q000473:pathology; D005399:Fishes; D005618:Fresh Water / Q000032:analysis / Q000737:chemistry / Q000469:parasitology; D006374:Helminthiasis, Animal / Q000453:epidemiology / Q000469:parasitology*; D006376:Helminths / Q000254:growth & development / Q000302:isolation & purification* / Q000502:physiology*; D006790:Host-Parasite Interactions; D008018:Life Cycle Stages; D011156:Population Density; D012487:Salmonidae / Q000469:parasitology*; D012737:Sex Factors; D013997:Time Factors; D006113:United Kingdom