Multiparasite communities in animals and humans: frequency, structure and pathogenic significance.

Helminth parasites were studied in the wood mouse, Apodemus sylvaticus, in southern England in September of each of four successive years (1994-1997). Nine species of helminths were recorded: five nematodes (Heligmosomoides polygyrus, Syphacia stroma, Pelodera strongyloides, Trichuris muris, Capillaria murissylvatici), two cestodes (Microsomacanthus crenata, Taenia taeniaeformis) and two trematodes (Corrigia vitta, Brachylaemus recurvum). In total, 134 mice were examined and 91.8% carried at least one species of helminth. The majority of mice carried two to three species (60.5%) and the highest combination was six of the nine species recorded in the study. The patterns of between-year variations in the prevalence and abundance of infection were different for each of the six species for which sufficient quantitative data were available to enable statistical analysis. For H. polygyrus, the most important source of variation arose from between-year differences, host age and the interaction of these factors: abundance increased with host age but in 1995 the age pattern was markedly different from that in the remaining years. The abundance of C. vitta also varied significantly between years but additionally there was a strong independent age effect. For M. crenata, the year x age interaction was significant, indicating that abundance among different age cohorts varied from year to year but there was also a weak significant main effect of age arising from the youngest age cohort carrying no parasites and the oldest age cohort the heaviest infections. For P. strongyloides the only significant factor was between-year variation with 1995 being a year of exceptionally low prevalence and abundance of infection. No significant between-year variation was detected for S. stroma but there was a strong sex effect (males carrying heavier infections) and an age effect (older mice of both sexes carrying heavier infections). The abundance of Trichuris muris varied only in relation to host age, worm burdens growing in intensity with increasing age, but there was also a significant interaction between year and host sex with respect to prevalence. For the remaining three species, the prevalence of infections was too low (< 8.2%) to enable any meaningful interpretation. This analysis emphasizes the need for carefully controlled statistical procedures in aiding the interpretation and the prioritization of the factors affecting worm burdens in wild rodents.

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Helminth infections in Apodemus sylvaticus in southern England: interactive effects of host age, sex and year on the prevalence and abundance of infections.

Males and females can differ in levels of parasitism and such differences may be mediated by the costs of sexual selection or by ecological differences between the genders. In threespine stickleback, Gasterosteus aculeatus, males exhibit paternal care and territorial nest defence and the costs of reproduction may be particularly high for males relative to females. We monitored levels of parasitism for 15 years in a population of stickleback infected by four different parasite species. Consistent with general predictions, overall parasite prevalence (total parasitism) was greater in males than in females. However, this excess did not occur for each species of parasite. Males had higher prevalence of a cestode Cyathocephalus truncatus and a trematode Bunodera sp. relative to females, while females had higher prevalence of a cestode Schistocephalus solidus and nematodes. This suggested ecological sources to differences in parasitism rather than reproductive costs and therefore we examined diet of unparasitized stickleback, predicting that differences in dietary niche would influence relative parasitism. This was partially confirmed and showed that female stomach contents had increased frequency of pelagic items, the major habitat for the primary host of S. solidus whereas males exhibited increased frequency of benthic items, the dominant habitat of C. truncatus and Bunodera. Temporal shifts in the extent and direction of differential parasitism among years between the sexes were associated with temporal shifts in dietary differences. Our results, combined with those in the literature, suggest that ecological differences between genders could be a more important component to patterns of parasitic infection in natural populations than currently appreciated.

https://web.uvic.ca/%7Ereimlab/sdarticle.pdf

Ecological causes of sex-biased parasitism in threespine stickleback

Summary 1. Two published data sets of helminths of the wood mouse Apodemus sylvaticus (L.) were analysed to test the hypothesis that the structure of these component communities is influenced by interactions between species. A range of tests, with differing null models, was applied to tease out the importance of controlling for subgroupings (e.g. sex, age, site, year, season) within the data when searching for significant associations based on prevalence (co-occurrence, presence/absence) or abundance (quantitative associations) data. 2. Significant differences from null models were detected for associations based on prevalence, but when subgroup constraints were taken into consideration, most lost significance. Among three and 15 pair-wise associations possible in data sets 1 and 2, respectively, only that between Trichuris muris and Heligmosomoides polygyrus was not dependent on context, and that between H. polygyrus and Catenotaenia pusilla , while always positive, varied in magnitude among sites of capture. 3. Pair-wise comparisons of abundance revealed three significant associations, only one of which ( H. polygyrus with C. pusilla ) still remained significant after controlling for quantified extrinsic and intrinsic factors . With increasing burdens of H. polygyrus , mice carried more of other helminth species and this relationship remained significant after controlling for confounding factors. 4. Overall, positive co-occurrences of pairs of helminths of A. sylvaticus were highly context dependent and quantitative associations were weak and not convincing. Therefore, interactions between parasites are unlikely to play a dominant role among the processes that structure the component community of helminths in wood mice, in selected study sites in the south of England.

https://besjournals.onlinelibrary.wiley.com/doi/pdf/10.1111/j.1365-2656.2005.00995.x

Do the helminth parasites of wood mice interact

Seasonal fluctuations in the prevalence and abundance of infection with intestinal helminths were studied in Apodemus sylvaticus (wood mouse, n = 399), from three contrasting habitats in southern England, to test the hypothesis that both intrinsic (host sex, age) and extrinsic (season, site) factors influence parasite species richness and abundance. Five species of helminths were recovered but only one of these (Capillaria murissylvatici) was site-specific (Dungeness). Total species richness was therefore 5 at Dungeness and 4 at the other two sites. Mean species richness was 1.4, but in adult mice there was a pronounced difference between the sites, and an independent highly significant effect of season. Syphacia stroma and Corrigia vitta both showed marked differences between sites in respect of prevalence and abundance of infection. Capillaria murissylvatici was encountered at Dungeness mostly in the spring whereas seasonal changes in abundance of S. stroma were consistent across all three sites. Seasonal fluctuations in the abundance of Catenotaenia pusilla were compounded by differences between sites. Host sex was not a significant factor in any species, although a posteriori analysis of S. stroma worm burdens for the Isle of Wight site revealed a moderate local sex effect. Overall the principal determinants of variation in helminth burdens were the extrinsic factors, site and season.

Seasonal and site specific variation in the component community structure of intestinal helminths in Apodemus sylvaticus from three contrasting habitats in south-east England.

Seasonal variation in most of the metazoan parasites of a Wood mouse population was investigated by a statistical analysis of their frequencies in 11 samples of about 30 mice trapped regularly over one year. Numbers of the flea Ctenophthalmus nobilis, most mesostigmatid mites and the beetle Leptinus testaceus were correlated with breeding in the mouse population and may have been directly linked with it as all ofthese arthropods are common in Wood mouse nests. The tick Ixodes ricinus was abundant over the summer but scarce in winter. Its preponderance on male hosts is doubtless because they cover more ground than females. Flukes were commonest in summer, probably as a result ofthe period of intensive feeding on invertebrates by the mice which usually occurs in early summer. Female mice were more heavily infected, perhaps because of their increased food requirements in the breeding season. Abundance of flukes declined with the turnover in the mouse population in autumn. The infestation pattern of the nematode Capillaria muris sylvatici is similar and the possibility of an invertebrate vector is discussed. While older mice were generally more heavily infected with helminths than were young, this was least marked in the tapeworm Cataenotaenia lobata (which most likely has a mite as an intermediate host and may be picked up as soon as juveniles start grooming) and the roundworm Syphacia stroma (eggs of which are almost certainly transferred by body contact between hosts)

R. Langley

Papers

Seasonal variations in infestations of parasites in a Wood mouse Apodemus sylvaticus population in the West of Ireland