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.