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Relationships between landscape structure and the prevalence of two tick-borne infectious agents, Anaplasma phagocytophilum and Borrelia burgdorferi sensu lato, in small mammal communities

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Abstract

Context

By modifying ecosystems, land cover changes influence the emergence, the spread and the incidence of vector-borne diseases.

Objective

This study aimed at identifying associations between landscape structure and the prevalence of two tick-borne infectious agents, Anaplasma phagocytophilum and Borrelia burgdorferi s.l., in small mammal communities.

Methods

Small mammals were sampled in 24 sites along a gradient of woodland fragmentation and hedgerow network density, and screened for infectious agents with real-time PCR techniques. For each site, structural variables (composition and configuration) of the surrounding landscape at various scales (0–500 m) and variables of wooded habitats connectivity based on graph theory and least cost path distances for the two dominant species, bank voles (Myodes glareolus) and wood mice (Apodemus sylvaticus), were computed.

Results

The A. phagocytophilum prevalence increased with wooded habitats cover (0–500 m), likely through host population size, and increased slightly with bank vole abundance, which has a higher reservoir competence than wood mouse. The B. burgdorferi s.l. prevalence increased with wooded ecotones only at local scales (50–100 m). Wooded habitats connectivity measures did not improve models built with simple land cover variables. A more marked spatial pattern was observed for the prevalence of A. phagocytophilum than B.burgdorferi s.l.

Conclusions

This study highlights the interest of considering together the ecology of infectious agents (e.g. host specificity) and the host species community ecology to better understand the influence of the landscape structure on the spatial distribution of vector-borne infectious agents.

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Acknowledgements

We are very grateful to Agnès Bouju, Floriane Boullot, Axelle Durand, Mathieu Gonnet, Olivier Jambon, Maggy Jouglin, Emmanuelle Moreau, Pranav Pandit, and Ionut Pavel who helped in sampling and preparing small mammal tissues before molecular analyses; to Séverine Barry, Amélie Cohadon, Angélique Pion, and Valérie Poux who helped in the lab for the molecular detection of infectious agents; and to Nelly Dorr and Isabelle Lebert who managed the data base of the OSCAR project (https://www6.inra.fr/oscar/). We thank the ‘Zone Atelier Armorique’ (https://osur.univ-rennes1.fr/za-armorique/) for providing the GIS data and for the access to its field facilities. We thank Henri Lemercier and Benoît Chevallier from the ‘Office National des Forêts’ for facilitating the access to the Villecartier forest. The ‘Tiques et Maladies à Tiques’ team of the ‘Réseau Ecologie des Interactions Durables’ group, supported by the INRA and the CNRS gave a rich thinking environment. This work was funded by the French National Research Agency (ANR-11-Agro-001-04; call for Proposal ‘Agrobiosphere’, OSCAR project). This work is part of the PhD of GP, which was supported by a fellowship from the Brittany region, France. The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

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Author notes

  1. Grégoire Perez

    Present address: UMR BIPAR, INRA-Anses-ENVA, 94701, Maisons-Alfort, France

  2. Amélie Chastagner

    Present address: ANSES, Laboratoire de Ploufragan-Plouzané-Niort, 22440, Ploufragan, France

Authors and Affiliations

  1. UMR CNRS 6553–Université de Rennes 1, ECOBIO, Campus de Beaulieu, 35042, Rennes, France

    Grégoire Perez, Yann Rantier & Alain Butet

  2. BIOEPAR, INRA, Oniris, 44307, Nantes, France

    Grégoire Perez, Suzanne Bastian, Albert Agoulon & Olivier Plantard

  3. EPIA, INRA, VetAgro Sup, 63122, Saint-Genès-Champanelle, France

    Amélie Chastagner & Gwenaël Vourc’h

  4. Evolutionary Ecology Group, University of Antwerp, Campus Drie Eiken, Universiteitsplein 1, 2610, Wilrijk, Belgium

    Amélie Chastagner

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Contributions

GP, SB, AA, GV, OP and AB designed the study. GP, SB, AA, YR, OP and AB participated to the small mammal field sampling. AC performed most of the DNA extractions and the molecular analyses. YR managed the GIS data. GP performed all data analyses and drafted the manuscript. All authors read, commented and approved the manuscript.

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Correspondence to Grégoire Perez.

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Supplementary file1 (TIF 749 kb)

10980_2019_957_MOESM2_ESM.ods

Supplementary file2 (ODS 27 kb). Appendix 1: Example of the habitats landscape connectivity analyses. Final aggregated land cover 5 m-resolution raster file (a) and ‘dPC’ (‘difference in Probability of Connectivity’) metric computed on different graphs (b, c, and d). The sampling patch on the right (surrounded in blue) appears moderately connected with Euclidian distances (b), while it is weakly connected when weighted by least cost paths (c and d) because it is surrounded by a river at North and by roads on other sides (see a). The sampling patch on the left is moderately connected for the wood mouse (c) while it is weakly connected for the bank vole (d) because it is separated to other wooded habitat patches by large grassland or crops patches resulting in fewer connections for this latter species. See Materials and Methods for more details.

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Perez, G., Bastian, S., Chastagner, A. et al. Relationships between landscape structure and the prevalence of two tick-borne infectious agents, Anaplasma phagocytophilum and Borrelia burgdorferi sensu lato, in small mammal communities. Landscape Ecol 35, 435–451 (2020). https://doi.org/10.1007/s10980-019-00957-x

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