Diversity, decoys and the dilution effect: how ecological communities affect disease risk

Abstract

SUMMARY Growing interest in ecology has recently focused on the hypothesis that community diversity can mediate infection levels and disease (‘dilution effect’). In turn, biodiversity loss — a widespread consequence of environmental change — can indirectly promote increases in disease, including those of medical and veterinary importance. While this work has focused primarily on correlational studies involving vector-borne microparasite diseases (e.g. Lyme disease, West Nile virus), we argue that parasites with complex life cycles (e.g. helminths, protists, myxosporeans and many fungi) offer an excellent additional model in which to experimentally address mechanistic questions underlying the dilution effect. Here, we unite recent ecological research on the dilution effect in microparasites with decades of parasitological research on the decoy effect in macroparasites to explore key questions surrounding the relationship between community structure and disease. We find consistent evidence that community diversity significantly alters parasite transmission and pathology under laboratory as well as natural conditions. Empirical examples and simple transmission models highlight the diversity of mechanisms through which such changes occur, typically involving predators, parasite decoys, low competency hosts or other parasites. However, the degree of transmission reduction varies among diluting species, parasite stage, and across spatial scales, challenging efforts to make quantitative, taxon-specific predictions about disease. Taken together, this synthesis highlights the broad link between community structure and disease while underscoring the importance of mitigating ongoing changes in biological communities owing to species introductions and extirpations.

Parasite diversity and coinfection determine pathogen infection success and host fitness

“…Specifically, Echinostoma and Ribeiroia, which are often reported as the most virulent parasites (47) (although Echinostoma caused little pathology in this study), were the most common parasites with other species added to communities as richness progressively increased. These findings parallel a key criterion of the "dilution effect" for host diversity, in which the most competent hosts need to be basally nested components of more diverse assemblages (48,49). Combining these observations with our experimental findings suggest that, because of antagonism among coinfecting species and the low average level of pathogenicity in this group of parasites, parasite diversity can also function as a mechanism of the dilution effect by reducing the success of virulent species.…”

Biodiversity inhibits parasites: Broad evidence for the dilution effect

“…Thus, we call for increased focus on the mechanisms causing diversitydisease patterns. For example, nonfocal host species can inhibit disease spread by regulating host populations via competition or predation, interfering with the transmission process, or altering host behavior (6,8). Theoretical models can generally delineate which mechanisms can promote or inhibit disease (27,28), but experimental tests that assess the relative importance of these mechanisms, their generality across disease systems, and their dependence on temporal and spatial scales remain scarce.…”

“…These concurrent patterns have prompted suggestions that biodiversity and the spread of diseases may be causally linked. For example, the dilution effect hypothesis proposes that diverse host communities inhibit the abundance of parasites through several mechanisms, such as regulating populations of susceptible hosts or interfering with the transmission process (6)(7)(8). Thus, diverse communities may inhibit the proliferation of parasites, thereby promoting the stability of ecological communities and ecosystem services (e.g., nutrient cycling, carbon sequestration, and natural product production) (9).…”

Host and parasite diversity jointly control disease risk in complex communities

“…On the other hand, increases in host diversity are also hypothesized to promote parasite diversity by enhancing colonization opportunities and supporting a wider suite of parasite life cycles (host diversity begets parasite diversity hypothesis; ref. 16), such that host diversity and parasite diversity correlate positively (17,18). Rather than contradicting each other, these seemingly divergent perspectives on the diversity-disease relationship emphasize differences in both terminology and ecological process.…”