Stability of within-host-parasite communities in a wild mammal system

Abstract

Simultaneous infection by multiple parasite species is ubiquitous in nature. Interactions among co-infecting parasites may have important consequences for disease severity, transmission and community-level responses to perturbations. However, our current view of parasite interactions in nature comes primarily from observational studies, which may be unreliable at detecting interactions. We performed a perturbation experiment in wild mice, by using an anthelminthic to suppress nematodes, and monitored the consequences for other parasite species. Overall, these parasite communities were remarkably stable to perturbation. Only one non-target parasite species responded to deworming, and this response was temporary: we found strong, but short-lived, increases in the abundance of Eimeria protozoa, which share an infection site with the dominant nematode species, suggesting local, dynamic competition. These results, providing a rare and clear experimental demonstration of interactions between helminths and co-infecting parasites in wild vertebrates, constitute an important step towards understanding the wider consequences of similar drug treatments in humans and animals.

Keywords: Heligmosomoides polygyrus; co-infection; community ecology; helminth; interaction.

Figures

Figure 1.

Effects of the anthelminthic drug Ivermectin on target (nematodes) and non-target (Eimeria) parasites. (a) Effect of Ivermectin administered one to three weeks previously on nematode infection probability. (b) Nematode infection probability over time since first capture (c) Effect of Ivermectin administered one to three weeks previously on Eimeria spp. infection intensity. (d) Eimeria spp. infection intensity over time since first capture. In (b) and (d), arrows indicate times of treatment (solid arrows denote repeated treatment; dashed arrows denote single treatment); single-treatment mice (dashed line, filled squares) are grouped with repeated treatment mice (solid line, filled circles) until four weeks, at which point they become different. Data are means and s.e.m. from raw data.

Figure 2.

Infection intensity over time since first capture for (a) Eimeria hungaryensis and (b) Eimeria apionodes across Ivermectin treatment groups. While E. hungaryensis infection intensity increased after each treatment, and more closely mirrored the dynamics of nematode infection probability, E. apionodes was less affected by treatment. Arrows indicate times of treatment (solid arrows denote repeated treatment; dashed arrows denote single treatment); single-treatment mice (dashed line, filled squares) are grouped with repeated treatment mice (solid line, filled circles) until four weeks, at which point they become different. Data are means and s.e.m. from raw data.

Figure 3.

(a) Summary of Ivermectin treatment effects on non-target parasites. Effect size estimates (Hedge's g) for the effect of treatment on non-target parasite response variables. Negative g-values indicate suppressive effects of nematodes (treatment resulted in higher infection intensities or infection probability for the non-target parasite than control mice), positive values indicate the opposite. Effect sizes were calculated either for parasite infection probability (using the odds ratio to calculate g), or from the difference in mean oocyst counts per gram faeces, on a log scale as used in statistical analyses. (b) Frequency histogram of the absolute effect sizes shown in (a), showing skew of the distribution towards primarily weak interactions.