Abstract

BackgroundIdentifying the mechanisms driving disease risk is challenging for multi-host pathogens, such as Borrelia burgdorferi sensu lato (s.l.), the tick-borne bacteria causing Lyme disease. Deer are tick reproduction hosts but do not transmit B. burgdorferi s.l., whereas rodents and birds are competent transmission hosts. Here, we use a long-term deer exclosure experiment to test three mechanisms for how high deer density might shape B. burgdorferi s.l. prevalence in ticks: increased prevalence due to higher larval tick densities facilitating high transmission on rodents (M1); alternatively, reduced B. burgdorferi s.l. prevalence because more larval ticks feed on deer rather than transmission-competent rodents (dilution effect) (M2), potentially due to ecological cascades, whereby higher deer grazing pressure shortens vegetation which decreases rodent abundance thus reducing transmission (M3).MethodsIn a large enclosure where red deer stags were kept at high density (35.5 deer km−2), we used an experimental design consisting of eight plots of 0.23 ha, four of which were fenced to simulate the absence of deer and four that were accessible to deer. In each plot we measured the density of questing nymphs and nymphal infection prevalence in spring, summer and autumn, and quantified vegetation height and density, and small mammal abundance.ResultsPrevalence tended to be lower, though not conclusively so, in high deer density plots compared to exclosures (predicted prevalence of 1.0% vs 2.2%), suggesting that the dilution and cascade mechanisms might outweigh the increased opportunities for transmission mechanism. Presence of deer at high density led to shorter vegetation and fewer rodents, consistent with an ecological cascade. However, Lyme disease hazard (density of infected I. ricinus nymphs) was five times higher in high deer density plots due to tick density being 18 times higher.ConclusionsHigh densities of tick reproduction hosts such as deer can drive up vector-borne disease hazard, despite the potential to simultaneously reduce pathogen prevalence. This has implications for environmental pathogen management and for deer management, although the impact of intermediate deer densities now needs testing.Graphical abstract

Highlights

  • Identifying the mechanisms driving disease risk is challenging for multi-host pathogens, such as Borrelia burgdorferi sensu lato (s.l.), the tick-borne bacteria causing Lyme disease

  • A particular gap in knowledge that this study aims to fill is the potential role of deer in regulating nymphal infection prevalence (NIP) and Lyme disease hazard through their cascading effects on vegetation and transmission hosts such as rodents

  • Mechanisms 2: dilution effect The dilution effect mechanism implies that the relative proportion of the larval tick population feeding on deer vs rodents is higher in high deer density plots compared to exclosures

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Summary

Introduction

Identifying the mechanisms driving disease risk is challenging for multi-host pathogens, such as Borrelia burgdorferi sensu lato (s.l.), the tick-borne bacteria causing Lyme disease. Gandy et al Parasites Vectors (2021) 14:509 species but not in those acting as transmission hosts for the mosquito-borne Everglades virus. This increased the proportion of mosquito blood meals taken from transmission hosts [2]. Two studies conducted in the Netherlands investigated the impacts of cattle grazing on small mammals, tick density and tick-borne pathogen (Borrelia burgdorferi) prevalence [4, 5]. Gassner et al [4] observed fewer rodents and ticks in grazed plots while Sprong et al [5] found no effects of cattle grazing on the density of infected nymphs (DIN)

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