Biodiversity and the dilution effect in disease ecology

Many infectious diseases of humans are caused by pathogens that reside in nonhuman animal reservoirs and are transmitted to humans via the bite of an arthropod vector. Most vectors feed from a variety of host species that differ dramatically in their reservoir competence; that is, their probability of transmitting the infection from host to vector. We explore a conceptual model of what we termed the "dilution effect," whereby the presence of vertebrate hosts with a low capacity to infect feeding vectors (incompetent reservoirs) dilute the effect of highly competent reservoirs, thus reducing disease risk. Using Lyme disease as an example, we demonstrate the presence and estimate the magnitude of the dilution effect for local sites in eastern New York State. We found that the prevalence of Lyme disease spirochetes, Borrelia burgdorferi, in field-collected Ixodes ticks (37.6% and 70.5% for nymphal and adult stages, respectively) was dramatically lower than expected, (∼90% and >95% for nymphal and adult stages, respectively) if ticks fed predominantly on highly competent reservoirs, white-footed mice (Peromyscus leucopus) and eastern chipmunks (Tamias striatus). We inferred the role of additional host species using an empirically based model that incorporated data on tick burdens per host, relative population densities of hosts, and reservoir competence of each host. Assuming an empirically realistic reservoir competence of 5% for non-mouse and non-chipmunk hosts, we determined that alternative hosts must provide 61% and 72% of larval and nymphal meals, respectively. Using computer simulations, we assembled simulated host communities that differed in species richness, evenness, and net interactions between alternative hosts and mice. We found that increasing species richness (but not evenness) reduced disease risk. Effects were most pronounced when the most competent disease reservoirs were community dominants and when alternative hosts had a net negative influence on the dominance of mice as a host for ticks. Our results highlight a critical role of biodiversity and host community ecology in the transmission of vector-borne zoonotic diseases that in turn has important consequences for human health.