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Host functional connectivity and the spread potential of Lyme disease

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Abstract

Context

In the ecology of Lyme disease emergence, it remains unclear to what extent spread of the tick vector (Ixodes scapularis) and the pathogen (Borrelia burgdorferi) are dependent upon the dispersal of vertebrate hosts in spatially heterogeneous landscapes. Yet, empirical measure of these complex ecologically driven spread processes present conceptual and methodological challenges despite important public health implications.

Objectives

To examine the relationship between landscape characteristics and tick-borne disease spread, we modeled the influence of landscape connectivity for a simplified vertebrate host community (white-footed mouse—Peromyscus leucopus, American robin—Turdus migratorius, white-tailed deer—Odocoileus virginianus) on the potential spread of the tick population compared to the pathogen in a spatially-structured landscape.

Methods

We parameterized a hybrid demographic-dispersal connectivity model by combining a series of reported host dispersal and tick burden estimates with empirically-measured tick abundance and pathogen prevalence sampled from a Lyme-endemic island landscape in Thousand Islands National Park (Ontario, Canada) and simulated several tick- and pathogen-spread scenarios.

Results

The extent of tick spread by mice [amount of reachable habitat (ARH) = 18.0%] is considerably similar to that of robins (ARH = 18.7%), while deer support the greatest tick spread extent (ARH = 82.0%). Infected mice carrying ticks support the highest pathogen spread (ARH = 19.8%). Short-distance pathogen spread and long-distance tick spread were facilitated by intermediate stepping stone habitat fragments.

Conclusions

We provide evidence that host functional connectivity mediates tick spread differently than pathogen spread, and depends strongly on landscape configuration. Our study therefore emphasizes the importance of landscape spatial heterogeneity on the ecological processes that influence regional tick-borne disease spread.

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Data availability

Original data used for this study were collected as part of another project and can be accessed from the original article (Werden et al. 2014). Landscape connectivity analyses were performed using Conefor, a software package freely available at www.conefor.org (Saura and Torne 2009). In particular, the Conefor version for directed graphs, as those we considered in our analyses, can be directly downloaded at http://www.conefor.org/files/usuarios/conefor_directed.zip.

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Acknowledgements

Field and laboratory work was conducted as part of another project (Werden et al. 2014) and was supported by Emily Gonzales at Thousand Islands National Park (TINP); Jeff Bowman at the Ontario Ministry of Natural Resources and Forestry (OMNRF); Ian K. Barker at the Canadian Wildlife Health Cooperative (CWHC) and Robbin Lindsay at the Public Health Agency of Canada. We thank the numerous students and staff from the OMNRF, CWHC, PHAC, and TINP who contributed to field data collection and lab work. We thank the associate editor and reviewers for their constructive comments.

Funding

M-JF was supported by NSERC Discovery Grant #5134. SS was supported by grant AGL2012-31099 from the Spanish Ministry of Economy and Competitiveness. AGW was partially supported by the University of Toronto, Department of Ecology & Evolution, and by Ontario Graduate Scholarships.

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Authors and Affiliations

  1. Li Ka Shing Knowledge Institute, St. Michael’s Hospital, 209 Victoria St., Toronto, ON, M5B 1T8, Canada

    Alexander G. Watts

  2. Department of Ecology & Evolutionary Biology, University of Toronto, Toronto, ON, M5S 3B2, Canada

    Alexander G. Watts & Marie-Josée Fortin

  3. Departamento de Sistemas y Recursos Naturales, Universidad Politécnica de Madrid, Ciudad Universitaria s/n, 28040, Madrid, Spain

    Santiago Saura

  4. European Commission, Joint Research Centre (JRC), Directorate D - Sustainable Resources, Via E. Fermi 2749, 21027, Ispra, VA, Italy

    Santiago Saura

  5. Department of Pathobiology and Canadian Wildlife Health Cooperative, University of Guelph, Guelph, ON, N1G 2W1, Canada

    Claire Jardine & Lisa Werden

  6. Department of Pathology and Microbiology, Faculty of Veterinary Medicine, Université de Montréal, Saint-Hyacinthe, QC, J2S 7C6, Canada

    Patrick Leighton

  7. Thousand Islands National Park, Mallorytown, ON, K0E 1R0, Canada

    Lisa Werden

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  1. Alexander G. Watts
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Correspondence to Alexander G. Watts.

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Watts, A.G., Saura, S., Jardine, C. et al. Host functional connectivity and the spread potential of Lyme disease. Landscape Ecol 33, 1925–1938 (2018). https://doi.org/10.1007/s10980-018-0715-z

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