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Effect of landscape features on the relationship between Ixodes ricinus ticks and their small mammal hosts

BACKGROUND: The consequences of land use changes are among the most cited causes of emerging infectious diseases because they can modify the ecology and transmission of pathogens. This is particularly true for vector-borne diseases which depend on abiotic (e.g. climate) and biotic conditions (i.e. h...

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Autores principales: Perez, Grégoire, Bastian, Suzanne, Agoulon, Albert, Bouju, Agnès, Durand, Axelle, Faille, Frédéric, Lebert, Isabelle, Rantier, Yann, Plantard, Olivier, Butet, Alain
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4714450/
https://www.ncbi.nlm.nih.gov/pubmed/26767788
http://dx.doi.org/10.1186/s13071-016-1296-9
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author Perez, Grégoire
Bastian, Suzanne
Agoulon, Albert
Bouju, Agnès
Durand, Axelle
Faille, Frédéric
Lebert, Isabelle
Rantier, Yann
Plantard, Olivier
Butet, Alain
author_facet Perez, Grégoire
Bastian, Suzanne
Agoulon, Albert
Bouju, Agnès
Durand, Axelle
Faille, Frédéric
Lebert, Isabelle
Rantier, Yann
Plantard, Olivier
Butet, Alain
author_sort Perez, Grégoire
collection PubMed
description BACKGROUND: The consequences of land use changes are among the most cited causes of emerging infectious diseases because they can modify the ecology and transmission of pathogens. This is particularly true for vector-borne diseases which depend on abiotic (e.g. climate) and biotic conditions (i.e. hosts and vectors). In this study, we investigated how landscape features affect the abundances of small mammals and Ixodes ricinus ticks, and how they influence their relationship. METHODS: From 2012 to 2014, small mammals and questing I. ricinus ticks were sampled in spring and autumn in 24 sites located in agricultural and forest landscapes in Brittany, France. We tested the effects of landscape features (composition and configuration) on the abundances of small mammal species and immature ticks and their relationship. Additionally, we quantified the larval tick burden of small mammals in 2012 to better describe this relationship. RESULTS: The nymph abundance was positively influenced by the larval occurrence and the wood mouse Apodemus sylvaticus abundance the previous spring because they hosted tenfold more larvae than the bank vole Myodes glareolus. The bank vole abundance in spring and autumn had a negative and positive effect, respectively, on the nymph abundance. In agricultural landscapes, wood mice were positively influenced by woodland cover and woodland/hedgerow-grassland ecotone, whereas bank voles showed the opposite or non-significant responses to these landscape variables. The woodland cover had a positive effect on immature ticks. CONCLUSION: The landscape configuration, likely by affecting the landscape connectivity, influences the small mammal communities in permanent habitats. Our study showed that the wood mouse, due to its dominance and to its tolerance to ticks, feeds a substantial proportion of larvae. The acquired resistance to ticks in the bank vole can reduce its role as a trophic resource over time. The nymph abundance seems indirectly influenced by landscape features via their effects on the small mammal community. To enhance our understanding of the epidemiology of tick-borne diseases within landscapes, further studies will integrate data on pathogen prevalence and investigate explicitly the effect of landscape connectivity on host-vector-pathogen systems.
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spelling pubmed-47144502016-01-16 Effect of landscape features on the relationship between Ixodes ricinus ticks and their small mammal hosts Perez, Grégoire Bastian, Suzanne Agoulon, Albert Bouju, Agnès Durand, Axelle Faille, Frédéric Lebert, Isabelle Rantier, Yann Plantard, Olivier Butet, Alain Parasit Vectors Research BACKGROUND: The consequences of land use changes are among the most cited causes of emerging infectious diseases because they can modify the ecology and transmission of pathogens. This is particularly true for vector-borne diseases which depend on abiotic (e.g. climate) and biotic conditions (i.e. hosts and vectors). In this study, we investigated how landscape features affect the abundances of small mammals and Ixodes ricinus ticks, and how they influence their relationship. METHODS: From 2012 to 2014, small mammals and questing I. ricinus ticks were sampled in spring and autumn in 24 sites located in agricultural and forest landscapes in Brittany, France. We tested the effects of landscape features (composition and configuration) on the abundances of small mammal species and immature ticks and their relationship. Additionally, we quantified the larval tick burden of small mammals in 2012 to better describe this relationship. RESULTS: The nymph abundance was positively influenced by the larval occurrence and the wood mouse Apodemus sylvaticus abundance the previous spring because they hosted tenfold more larvae than the bank vole Myodes glareolus. The bank vole abundance in spring and autumn had a negative and positive effect, respectively, on the nymph abundance. In agricultural landscapes, wood mice were positively influenced by woodland cover and woodland/hedgerow-grassland ecotone, whereas bank voles showed the opposite or non-significant responses to these landscape variables. The woodland cover had a positive effect on immature ticks. CONCLUSION: The landscape configuration, likely by affecting the landscape connectivity, influences the small mammal communities in permanent habitats. Our study showed that the wood mouse, due to its dominance and to its tolerance to ticks, feeds a substantial proportion of larvae. The acquired resistance to ticks in the bank vole can reduce its role as a trophic resource over time. The nymph abundance seems indirectly influenced by landscape features via their effects on the small mammal community. To enhance our understanding of the epidemiology of tick-borne diseases within landscapes, further studies will integrate data on pathogen prevalence and investigate explicitly the effect of landscape connectivity on host-vector-pathogen systems. BioMed Central 2016-01-15 /pmc/articles/PMC4714450/ /pubmed/26767788 http://dx.doi.org/10.1186/s13071-016-1296-9 Text en © Perez et al. 2016 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research
Perez, Grégoire
Bastian, Suzanne
Agoulon, Albert
Bouju, Agnès
Durand, Axelle
Faille, Frédéric
Lebert, Isabelle
Rantier, Yann
Plantard, Olivier
Butet, Alain
Effect of landscape features on the relationship between Ixodes ricinus ticks and their small mammal hosts
title Effect of landscape features on the relationship between Ixodes ricinus ticks and their small mammal hosts
title_full Effect of landscape features on the relationship between Ixodes ricinus ticks and their small mammal hosts
title_fullStr Effect of landscape features on the relationship between Ixodes ricinus ticks and their small mammal hosts
title_full_unstemmed Effect of landscape features on the relationship between Ixodes ricinus ticks and their small mammal hosts
title_short Effect of landscape features on the relationship between Ixodes ricinus ticks and their small mammal hosts
title_sort effect of landscape features on the relationship between ixodes ricinus ticks and their small mammal hosts
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4714450/
https://www.ncbi.nlm.nih.gov/pubmed/26767788
http://dx.doi.org/10.1186/s13071-016-1296-9
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