Parasites alter host community structure in a natural experiment

Parasites can profoundly alter host communities. However, the impact of parasites can vary from one community to another. Understanding why the impact of parasites varies across communities is challenging because it requires (i) separating the direct effects of the parasite on the host species from the indirect effects it exerts through the ecological interactions among the hosts and (ii) identifying how the presence of one host alters rates of infection in another. Freshwater fish communities in Trinidad have recently been invaded by a generalist parasitic nematode. This event, combined with our long-term mark-recapture studies of these communities, which began long before the invasion, presented a replicated natural experiment. In this experiment, we measured how host demographic rates responded to two 'treatments': stage of parasite establishment (before, and 1-2 years, 3-5 years and 6-8 years after invasion) and type of community (killifish-guppy communities and killifish-only communities). This design allowed us to infer the direct and indirect impacts of the parasite invasion on killifish communities and determine how the presence of guppies altered infection rates in killifish. The parasitic invasion drastically altered killifish-guppy communities: the ratio of killifish to guppies changed from 1:2 before the invasion to 1:16 after the invasion. Living with guppies amplified the effects of the parasite on killifish, such that parasite-related mortality rates of large adult killifish were twice as high in communities with guppies compared to those without. This effect was driven by a doubling of infection rates in large killifish that live with guppies. In a parallel study, we identified the same patterns of size- and community-dependent infection rates of killifish in five separate river systems, implying that this pattern is general in this system. Our study provides mechanistic insight into how parasites alter community structure under natural conditions, via their direct and indirect impacts on host demographic rates. Our work highlights the value of long-term field studies for our understanding of the impact of parasites on community structure and of ecological interactions in general.