An eco-epidemiological modeling approach to investigate dilution effect in two different tick-borne pathosystems

Abstract

Disease (re)emergence appears to be driven by biodiversity decline and environmental change. As a result, it is increasingly important to study host-pathogen interactions within the context of their ecology and evolution. The dilution effect is the concept that higher biodiversity decreases pathogen transmission. It has been observed especially in zoonotic vector-borne pathosystems, yet evidence against it has been found. In particular, it is still debated how the community (dis)assembly assumptions and the degree of generalism of vectors and pathogens affect the direction of the biodiversity-pathogen transmission relationship. The aim of this study was to use empirical data and mechanistic models to investigate dilution mechanisms in two rodent-tick-pathogen systems differing in their vector degree of generalism. A community was assembled to include ecological interactions that expand from purely additive to purely substitutive. Such systems are excellent candidates to analyze the link between vector ecology, community (dis)assembly dynamics, and pathogen transmission. To base our mechanistic models on empirical data, rodent live-trapping, including tick sampling, was conducted in Wales across two seasons for three consecutive years. We have developed a deterministic single-vector, multi-host compartmental model that includes ecological relationships with non-host species, uniquely integrating theoretical and observational approaches. To describe pathogen transmission across a gradient of community diversity, the model was populated with parameters describing five different scenarios differing in ecological complexity; each based around one of the pathosystems: Ixodes ricinus (generalist tick)-Borrelia burgdorferi and I. trianguliceps (small mammals specialist tick)-Babesia microti. The results suggested that community composition and interspecific dynamics affected pathogen transmission with different dilution outcomes depending on the vector degree of generalism. The model provides evidence that dilution and amplification effects are not mutually exclusive in the same community but depend on vector ecology and the epidemiological output considered (i.e., the "risk" of interest). In our scenarios, more functionally diverse communities resulted in fewer infectious rodents, supporting the dilution effect. In the pathosystem with generalist vector we identified a hump shaped relationship between diversity and infections in hosts, while for that characterized by specialist tick, this relationship was more complex and more dependent upon specific parameter values.

Keywords: Babesia microti; Ixodes ricinus; Ixodes trianguliceps; Lyme disease; community assembly; compartmental model; dilution effect; disease ecology; mechanistic model.