Ecological Effects
Both T.muris and S.obvelata are typically found in the caecum or proximal colon, so competition for resources physical space which the parasites occupy may contribute to the negative association observed between these species. While T. muris shows plasticity in its site of establishment in caecectomised mice (Panesar & Croll, 1980), it obtains nutrients from the intraepithelial space of the gut lining while embedded (T. D. Lee & Wright, 1978; Panesar & Croll, 1980), whereas S. obvelata are typically found free in the lumen, meaning that competition for a physical niche is perhaps unlikely, and the grounds for antagonistic niche competition between these species is unclear. While T. muris and mature C. hepaticum exist in separate organs, the infective stage of C. hepaticum does pass through the gut wall, meaning that changes in gut tissue histology by one parasite may be beneficial to another.
Prevalence of the microparasite Sarcocystis sp. is negatively associated with infection with C. hepaticum . Sarcocystis muriviperae has been shown to form cysts in the liver of laboratory mice (Paperna & Finkelman, 1996), while mice experimentally infected with S.dispersa show histopathological changes in the liver parenchyma (Skárková, 1986). Any impacts upon the liver caused byS. dispersa mean it could potentially be in competition for a spatial niche with C. hepaticum.
Positive associations between mites and C. hepaticum could indicate a role for ectoparasites as indicators of condition, with endoparasitic infection causing reduced fur quality or reduced levels of grooming. Alterations in grooming behaviour have been recorded in rodents coinfected with Toxoplasma sp. (Queiroz, Viel, Papa, Lescano, & Chieffi, 2013), though whether this could result from helminth coinfection is unclear. Wild deer mice (Peromyscus maniculatus ) show natural increases in ectoparasite prevalence, which are prevented by treatment with an antihelminthic (Pedersen & Antonovics, 2013). While mites of wild bank voles (Myodes glareolus ) showed a positive association with both fleas in the fur andCalodium spp. (referred to as Capillaria spp. ) dissected from the gastrointestinal tract, coinfected individuals had higher body mass in both instances, suggesting that these interactions may be immune mediated rather than a change in host condition (Perkins, White, Pascoe, & Gillingham, 2017). This is supported by the positive association observed between SMI and mite abundance in our study mice. Fur mite abundance was the only measure found to be associated with SMI in this study, bringing into question the significance of infection, and associated coinfection, on the fitness of the host. While this does not take into account reproductive fitness, that different aggregations of parasites within hosts do not seem to be strongly linked to host condition is notable.
Interactions between parasites could also arise from similarities or dissimilarities in transmission method, as might be expected from associations observed within guilds. All three helminth macroparasites observed here are typically transmitted orally (Flynn, 2007), a factor that could underpin positive associations observed betweenT.muris and C.hepaticum . The impact of life-cycle discrepancies may in turn interact with individual host behaviour e.g. more exploratory animals may expose themselves to more fleas, which infect hosts by detecting vibrations in the environment, while hosts which spend more time socialising may experience higher mite burden, as mites are typically passed directly between animals (Bordes, Blumstein, & Morand, 2007; Dizney & Dearing, 2013, 2016).
As the data were derived from cross sectional cull data it was not possible to infer direct causal links explaining associations between parasite species, and any observed relationships may potentially be mediated by some unaccounted-for variable. We have tried to mitigate this possibility by including a number of relevant physiological and ecological parameters in all models. The reported associations are therefore independent of possible confounding factors such as sex, age or season, and provide a robust framework from which the mechanisms of parasite interactions can be further hypothesised and tested.