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

Gandy, S., Kilbride, E., Biek, R. , Millins, C. and Gilbert, L. (2022) No net effect of host density on tick-borne disease hazard due to opposing roles of vector amplification and pathogen dilution. Ecology and Evolution, 12(9), e9253. (doi: 10.1002/ece3.9253) (PMID:36091342) (PMCID:PMC9448966)

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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.

Item Type:Articles
Status:Published
Refereed:Yes
Glasgow Author(s) Enlighten ID:Biek, Professor Roman and Kilbride, Mrs Elizabeth and Gandy, Miss Sara and Gilbert, Dr Lucy and Millins, Dr Caroline
Creator Roles:
Gandy, S.Conceptualization, Data curation, Formal analysis, Investigation, Methodology, Project administration, Validation, Visualization, Writing – original draft, Writing – review and editing
Kilbride, E.Investigation, Methodology, Resources, Writing – review and editing
Biek, R.Conceptualization, Funding acquisition, Methodology, Project administration, Resources, Supervision, Writing – review and editing
Millins, C.Conceptualization, Methodology, Project administration, Supervision, Writing – review and editing
Gilbert, L.Conceptualization, Funding acquisition, Methodology, Project administration, Supervision, Writing – review and editing
Authors: Gandy, S., Kilbride, E., Biek, R., Millins, C., and Gilbert, L.
College/School:College of Medical Veterinary and Life Sciences > School of Biodiversity, One Health & Veterinary Medicine
Journal Name:Ecology and Evolution
Publisher:Wiley
ISSN:2045-7758
ISSN (Online):2045-7758
Published Online:06 September 2022
Copyright Holders:Copyright © 2022 The Authors
First Published:First published in Ecology and Evolution 12(9): e9253
Publisher Policy:Reproduced under a Creative Commons License
Data DOI:10.5061/dryad.rv15dv49r

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