Heligmosomid infections in bank voles are associated with higher prevalence and greater abundance of other helminth species

The heligmosomid nematodes Heligmosomum mixtum and Heligmosomoides glareoli are dominant helminths infecting bank voles (Clethrionomys glareolus) in the temperate forests of NE Poland. Both are relatively long-lived species that accumulate in hosts with increasing host age. Based on studies showing that the closely related species, Heligmosomoides bakeri is immunomodulatory in murine hosts, we hypothesized that heligmosomid-infected bank voles should show higher prevalence and abundance with other helminths. To test this hypothesis, we analysed a database containing quantitative data on helminth parasites of bank voles (n = 922), comprising worm burdens recorded during 4 surveys, conducted at 3- to 4-year intervals, in 3 forest sites, during late summer of each year. After controlling for both intrinsic and extrinsic factors, the presence of heligmosomid nematodes was significantly associated with higher species richness of other helminth species, with the greater likelihood of voles carrying other helminth species, with higher worm burdens of other helminths and with significant positive covariance of heligmosomid burdens with those of other concurrently residing helminths. These patterns might be explained by a number of biological processes, including correlated host exposure or correlated host susceptibility not driven by the parasitic infections themselves. However, we consider it most likely that these results are consistent with the idea that like H. bakeri, the heligmosomid nematodes of bank voles employ non-specific immunomodulation to facilitate their own long-term survival, with the consequence that other concurrently infecting intestinal helminths benefit.