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

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...

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Autores principales: Gandy, Sara, Kilbride, Elizabeth, Biek, Roman, Millins, Caroline, Gilbert, Lucy
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9448966/
https://www.ncbi.nlm.nih.gov/pubmed/36091342
http://dx.doi.org/10.1002/ece3.9253
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author Gandy, Sara
Kilbride, Elizabeth
Biek, Roman
Millins, Caroline
Gilbert, Lucy
author_facet Gandy, Sara
Kilbride, Elizabeth
Biek, Roman
Millins, Caroline
Gilbert, Lucy
author_sort Gandy, Sara
collection PubMed
description 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.
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spelling pubmed-94489662022-09-09 No net effect of host density on tick‐borne disease hazard due to opposing roles of vector amplification and pathogen dilution Gandy, Sara Kilbride, Elizabeth Biek, Roman Millins, Caroline Gilbert, Lucy Ecol Evol Research Articles 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. John Wiley and Sons Inc. 2022-09-06 /pmc/articles/PMC9448966/ /pubmed/36091342 http://dx.doi.org/10.1002/ece3.9253 Text en © 2022 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd. https://creativecommons.org/licenses/by/4.0/This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
spellingShingle Research Articles
Gandy, Sara
Kilbride, Elizabeth
Biek, Roman
Millins, Caroline
Gilbert, Lucy
No net effect of host density on tick‐borne disease hazard due to opposing roles of vector amplification and pathogen dilution
title No net effect of host density on tick‐borne disease hazard due to opposing roles of vector amplification and pathogen dilution
title_full No net effect of host density on tick‐borne disease hazard due to opposing roles of vector amplification and pathogen dilution
title_fullStr No net effect of host density on tick‐borne disease hazard due to opposing roles of vector amplification and pathogen dilution
title_full_unstemmed No net effect of host density on tick‐borne disease hazard due to opposing roles of vector amplification and pathogen dilution
title_short No net effect of host density on tick‐borne disease hazard due to opposing roles of vector amplification and pathogen dilution
title_sort no net effect of host density on tick‐borne disease hazard due to opposing roles of vector amplification and pathogen dilution
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9448966/
https://www.ncbi.nlm.nih.gov/pubmed/36091342
http://dx.doi.org/10.1002/ece3.9253
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