Host and parasite diversity jointly control disease risk in complex communities

Host-parasite interactions are embedded within complex communities composed of multiple host species and a cryptic assemblage of other parasites. To date, however, surprisingly few studies have explored the joint effects of host and parasite richness on disease risk, despite growing interest in the diversity-disease relationship. Here, we combined field surveys and mechanistic experiments to test how transmission of the virulent trematode Ribeiroia ondatrae was affected by the diversity of both amphibian hosts and coinfecting parasites. Within natural wetlands, host and parasite species richness correlated positively, consistent with theoretical predictions. Among sites that supported Ribeiroia, however, host and parasite richness interacted to negatively affect Ribeiroia transmission between its snail and amphibian hosts, particularly in species-poor assemblages. In laboratory and outdoor experiments designed to decouple the relative contributions of host and parasite diversity, increases in host richness decreased Ribeiroia infection by 11-65%. Host richness also tended to decrease total infections by other parasite species (four of six instances), such that more diverse host assemblages exhibited similar to 40% fewer infections overall. Importantly, parasite richness further reduced both per capita and total Ribeiroia infection by 15-20%, possibly owing to intrahost competition among coinfecting species. These findings provide evidence that parasitic and free-living diversity jointly regulate disease risk, help to resolve apparent contradictions in the diversity-disease relationship, and emphasize the challenges of integrating research on coinfection and host heterogeneity to develop a community ecology-based approach to infectious diseases.