Quantifying dilution and amplification in a community of hosts for tick-borne pathogens

Recent controversy over whether biodiversity reduces disease risk (dilution effect) has focused on the ecology of Lyme disease, a tick-borne zoonosis. A criticism of the dilution effect is that increasing host species richness might amplify disease risk, assuming that total host abundance, and therefore feeding opportunities for ticks, increase with species richness. In contrast, a dilution effect is expected when poor quality hosts for ticks and pathogens (dilution hosts) divert tick blood meals away from competent hosts. Even if host densities are additive, the relationship between host density and tick encounters can be nonlinear if the number of ticks that encounter a host is a saturating function of host density, which occurs if ticks aggregate on the remaining hosts rather than failing to find a host before death. Both dilution and amplification are theoretical possibilities, and assessing which is more prevalent required detailed analyses of empirical systems. We used field data to explore the degree of tick redistribution onto fewer individuals with variation in intraspecific host density and novel data-driven models for tick dynamics to determine how changes in vertebrate community composition influence the density of nymphs infected with the Lyme bacterium. To be conservative, we allowed total host density to increase additively with species richness. Our long-term field studies found that larval and nymphal ticks redistribute onto fewer individuals as host densities decline, that a large proportion of nymphs and adults find hosts, and that mice and chipmunks feed a large proportion of nymphs. White-footed mice, eastern chipmunks, short-tailed shrews, and masked shrews were important amplification hosts that greatly increased the density of infected nymphs. Gray squirrels and Virginia opossums were important dilution hosts. Removing these two species increased the maximum number of larvae attached to amplification hosts by 57%. Raccoons and birds were minor dilution hosts under some conditions. Even under the assumption of additive community assembly, some species are likely to reduce the density of infected nymphs as diversity increases. If the assumption of additivity is relaxed, then species that reduce the density of small mammals through predation or competition might substantially reduce disease risk.