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.

High prevalence of Leucocytozoon parasites in fresh water breeding gulls

“…However, parasite gametocytes were observed in some of the blood smears, thus supporting the conclusion that the identified lineages can complete development in the analysed gull species. Co-infections by multiple parasite species are well documented across many animal systems (Rigaud et al 2010;Knowles et al 2013) and we found that a substantial proportion of the gulls were infected with two or more parasites. To what extent parasites in co-infections compete within the host is poorly investigated but it is possible that infections by one parasite may protect the host from other infections.…”

An ecosystem approach to understanding and managing within-host parasite community dynamics

“…Interestingly, as the nematodes re-infected the treated hosts there was a parallel reduction in coccidia burdens, which also returned to pre-treatment levels 4 weeks following treatment [42]. Hence, these within-host communities appear to be highly stable to perturbation, demonstrating resistance [only one coinfecting parasite group (of 20 species measured) responded to a reduction in nematodes] and resilience because both nematodes and coccidians rapidly returned to pre-treatment levels.…”

“…The within-host ecosystem may be considered to be stable if there is little change in parasite community composition or structure (presence/absence or burden of species within that community) after the perturbation. For example, in a study of the parasite community of wild wood mice, Knowles et al [42] showed that although anthelmintic drug treatment reduced nematode infections (the target parasite), burdens quickly returned to pre-treatment levels.…”

“…The localization of such interactions is illustrated by evidence of competitive release between the nematode Heligmosomoides polygyrus and coccidial parasite Eimeria hungaryensis in wild mice [42]. Experimental removal via drug treatment of the nematode resulted in a dramatic increase in E. hungaryensis intensity, which inhabits the same section of the small intestine as H. polygyrus.…”

“…With this in mind, we suggest several key issues, inspired by the ecosystem ecology concepts described in the previous sections, which should be considered to help predict the outcome of coinfection both for the parasites and host condition ( Figure 2). We illustrate the application of our framework using the coinfection study between the helminth H. polygyrus and coccidia E. hungaryensis in wild wood mice (Figure 3) [42]; while this example is with only two parasite species, a stepwise approach of adding Figure 2. A framework with specific questions to ask when developing predictions of parasite-parasite and parasite-host competition and their impact on host health.…”