Biodiversity series: The function of biodiversity in the ecology of vector-borne zoonotic diseases

Abstract

This is a critical evaluation of the influence of species diversity within communities of vertebrates on the risk of human exposure to vector-borne zoonoses. Vertebrates serve as natural reservoirs of many disease agents (viral, bacterial, protozoal) that are transmitted to humans by blood-feeding arthropod vectors. We describe the natural history of the Lyme disease zoonosis to illustrate interactions among pathogens, vectors, vertebrate hosts, and risk to humans. We then describe how the presence of a diverse assemblage of vertebrates can dilute the impact of the principal reservoir (the white-footed mouse, Peromyscus leucopus) of Lyme disease spirochetes (Borrelia burgdorferi), thereby reducing the disease risk to humans. Exploring the logic of what we call the dilution effect reveals four conditions that are necessary for it to apply generally to vector-borne zoonoses: (1) the feeding habits of the vector are generalized; (2) the pathogen is acquired by the vector from hosts (as opposed to exclusively transovarial transmission); (3) reservoir competence (the ability of a particular host species to infect a vector) varies among host species; and (4) the most competent reservoir host tends to be a community dominant, as defined by the proportion of the tick population fed by that species. When these conditions are met, vertebrate communities with high species diversity will contain a greater proportion of incompetent reservoir hosts that deflect vector meals away from the most competent reservoirs, thereby reducing infection prevalence and disease risk. Incorporating the likelihood that the abundance of competent reservoirs is reduced in more diverse communities, owing to the presence of predators and competitors, reinforces the impact of the dilution effect on the density of infected vectors. A review of the literature reveals the generality, though not the universality, of these conditions, which suggests that the effects of diversity on disease risk may be widespread. Issues in need of further exploration include (i) the relative importance of diversity per se versus fluctuating numbers of particular species; (ii) the relevance of species richness versus evenness to the dilution effect; (iii) whether the dilution effect operates at both local and regional scales; and (iv) the shape of empirically determined curves relating diversity to measures of disease risk. Further studies linking community ecology with epidemiology are warranted.