No net effect of host density on tick-borne disease hazard due to opposing roles of vector amplification and pathogen dilution

Sara Gandy*, Elizabeth Kilbride, Roman Biek, Caroline Millins, Lucy Gilbert

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

2 Citations (Scopus)

Abstract

To better understand vector-borne disease dynamics, knowledge of the ecological interactions between animal hosts, vectors, and pathogens is needed. The effects of hosts on disease hazard depends on their role in driving vector abundance and their ability to transmit pathogens. Theoretically, a host that cannot transmit a pathogen could dilute pathogen prevalence but increase disease hazard if it increases vector population size. In the case of Lyme disease, caused by Borrelia burgdorferi s.l. and vectored by Ixodid ticks, deer may have dual opposing effects on vectors and pathogen: deer drive tick population densities but do not transmit B. burgdorferi s.l. and could thus decrease or increase disease hazard. We aimed to test for the role of deer in shaping Lyme disease hazard by using a wide range of deer densities while taking transmission host abundance into account. We predicted that deer increase nymphal tick abundance while reducing pathogen prevalence. The resulting impact of deer on disease hazard will depend on the relative strengths of these opposing effects. We conducted a cross-sectional survey across 24 woodlands in Scotland between 2017 and 2019, estimating host (deer, rodents) abundance, questing Ixodes ricinus nymph density, and B. burgdorferi s.l. prevalence at each site. As predicted, deer density was positively associated with nymph density and negatively with nymphal infection prevalence. Overall, these two opposite effects canceled each other out: Lyme disease hazard did not vary with increasing deer density. This demonstrates that, across a wide range of deer and rodent densities, the role of deer in amplifying tick densities cancels their effect of reducing pathogen prevalence. We demonstrate how noncompetent host density has little effect on disease hazard even though they reduce pathogen prevalence, because of their role in increasing vector populations. These results have implications for informing disease mitigation strategies, especially through host management.

Original languageEnglish
Article numbere9253
JournalEcology and Evolution
Volume12
Issue number9
DOIs
Publication statusPublished - Sept 2022
Externally publishedYes

Bibliographical note

Funding Information:
We would like to thank Colin McClean from Glen Tanar estate, Malcolm Nicol from Ballogie estate, Paul Chapman from Birse community trust, and the Scottish Natural Heritage for letting us conduct our field work. Sara Gandy was funded by the University of Glasgow and the Macaulay Development Trust. Lucy Gilbert was supported by the Scottish Government's Rural and Environmental Science and Analytical Services Division including as part of the Centre of Expertise on Animal Disease Outbreaks (EPIC).

Funding Information:
We would like to thank Colin McClean from Glen Tanar estate, Malcolm Nicol from Ballogie estate, Paul Chapman from Birse community trust, and the Scottish Natural Heritage for letting us conduct our field work. Sara Gandy was funded by the University of Glasgow and the Macaulay Development Trust. Lucy Gilbert was supported by the Scottish Government's Rural and Environmental Science and Analytical Services Division including as part of the Centre of Expertise on Animal Disease Outbreaks (EPIC).

Publisher Copyright:
© 2022 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd.

Keywords

  • Borrelia burgdorferi
  • dilution effect
  • host community
  • Lyme disease
  • ticks
  • transmission hosts

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