Geography, deer, and host biodiversity shape the pattern of Lyme disease emergence in the Thousand Islands Archipelago of Ontario, Canada.

Lisa Werden,Jeff Bowman,L Robbin Lindsay,Claire M Jardine,Patrick A Leighton,Ian K Barker,Emily K Gonzales,J Stephen Dumler

doi:10.1371/journal.pone.0085640

Abstract

In the Thousand Islands region of eastern Ontario, Canada, Lyme disease is emerging as a serious health risk. The factors that influence Lyme disease risk, as measured by the number of blacklegged tick (Ixodes scapularis) vectors infected with Borrelia burgdorferi, are complex and vary across eastern North America. Despite study sites in the Thousand Islands being in close geographic proximity, host communities differed and both the abundance of ticks and the prevalence of B. burgdorferi infection in them varied among sites. Using this archipelago in a natural experiment, we examined the relative importance of various biotic and abiotic factors, including air temperature, vegetation, and host communities on Lyme disease risk in this zone of recent invasion. Deer abundance and temperature at ground level were positively associated with tick abundance, whereas the number of ticks in the environment, the prevalence of B. burgdorferi infection, and the number of infected nymphs all decreased with increasing distance from the United States, the presumed source of this new endemic population of ticks. Higher species richness was associated with a lower number of infected nymphs. However, the relative abundance of Peromyscus leucopus was an important factor in modulating the effects of species richness such that high biodiversity did not always reduce the number of nymphs or the prevalence of B. burgdorferi infection. Our study is one of the first to consider the interaction between the relative abundance of small mammal hosts and species richness in the analysis of the effects of biodiversity on disease risk, providing validation for theoretical models showing both dilution and amplification effects. Insights into the B. burgdorferi transmission cycle in this zone of recent invasion will also help in devising management strategies as this important vector-borne disease expands its range in North America.

Highlights

In eastern North America, Lyme disease is a serious emerging health risk caused by the bacterium Borrelia burgdorferi, which is transmitted to humans by the bite of an infected blacklegged tick (Ixodes scapularis) [1]
We examined the relative importance of proximity to the United States, deer abundance, temperature at ground level, canopy cover, leaf litter, small mammal species richness, number of I. scapularis nymphs, and relative abundance of mice in explaining the number of nymphs (NON), the prevalence of B. burgdorferi infection in nymphs (NIP), and the number of infected nymphs (NIN) in the heavily-visited Thousand Islands region
Average daily minimum temperature July-September Relative abundance of Peromyscus leucopus Small mammal species richness Percent canopy cover Average number of pellet groups per hectare Distance from United States mainland Average depth of leaf litter Interaction between Mice and Richness Number of small mammals trapped per 100 trap nights Nymphs caught per 2 person hours of dragging

Summary

Introduction

In eastern North America, Lyme disease is a serious emerging health risk caused by the bacterium Borrelia burgdorferi, which is transmitted to humans by the bite of an infected blacklegged tick (Ixodes scapularis) [1]. Reducing the risk of Lyme disease, as measured by the number of infected nymphal blacklegged ticks in the environment [2], [3], requires a better understanding of the factors that predict the distribution of B. burgdorferi and its vectors. As incompetent reservoirs [7], [8] and hosts mainly for adult ticks, deer are unlikely to have an effect on rates of B. burgdorferi infection. The effect of deer abundance on tick populations varies across eastern North America [4], [9]. Positive correlations have been seen on isolated islands and using deer exclosures [10,11,12], while studies in areas open to deer movement found little or no correlation between deer population density and the number of blacklegged ticks [9], [13], [14]

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Results

Discussion

Conclusion