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Vector communities under global change may exacerbate and redistribute infectious disease risk

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Abstract

Vector-borne parasites may be transmitted by multiple vector species, resulting in an increased risk of transmission, potentially at larger spatial scales compared to any single vector species. Additionally, the different abilities of patchily distributed vector species to acquire and transmit parasites will lead to varying degrees of transmission risk. Investigation of how vector community composition and parasite transmission change over space due to variation in environmental conditions may help to explain current patterns in diseases but also informs our understanding of how patterns will change under climate and land-use change. We developed a novel statistical approach using a multi-year, spatially extensive case study involving a vector-borne virus affecting white-tailed deer transmitted by Culicoides midges. We characterized the structure of vector communities, established the ecological gradient controlling change in structure, and related the ecology and structure to the amount of disease reporting observed in host populations. We found that vector species largely occur and replace each other as groups, rather than individual species. Moreover, community structure is primarily controlled by temperature ranges, with certain communities being consistently associated with high levels of disease reporting. These communities are essentially composed of species previously undocumented as potential vectors, whereas communities containing putative vector species were largely associated with low levels, or even absence, of disease reporting. We contend that the application of metacommunity ecology to vector-borne infectious disease ecology can greatly aid the identification of transmission hotspots and an understanding of the ecological drivers of parasite transmission risk both now and in the future.

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Data availability

The datasets used and/or analyzed during the current study available from the corresponding author on reasonable request.

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Acknowledgements

We thank S. Budischak for comments on a draft of the manuscript. Additionally, we thank D.E. Stallknecht for sharing hemorrhagic disease reports and SCWDS technicians for support in Culicoides field collections.

Funding

The Culicoides surveys were funded through a Cooperative Agreement with the United States Department of Agriculture, Animal and Plant Health Inspection Service Veterinary Services. Specifically, we acknowledge Cooperative Agreements 0691130808CA, 0791130808CA, 0891130808CA, 0991130808CA, 1091130808CA, 1191130808CA, and 1291130808CA, Veterinary Services, Animal and Plant Health Inspection Service, U.S. Department of Agriculture. AWP acknowledges funding from the McDonnell Foundation (grant number 220020193). Additional funds were provided through sponsorship from the fish and wildlife agencies of Alabama, Arkansas, Florida, Georgia, Kansas, Kentucky, Louisiana, Maryland, Mississippi, Missouri, North Carolina, Puerto Rico, South Carolina, Tennessee, Virginia, and West Virginia; through the Federal Aid to Wildlife Restoration Act (50 Stat. 917) and Grant Agreement 06ERAG0005, Biological Resources Division, U.S. Geological Survey, U.S. Department of the Interior; and through Cooperative Agreements 0696130032CA, 0796130032CA, 0896130032CA, 0996130032CA, 1096130032CA, 1196130032CA, and 1296130032CA, Veterinary Services, Animal and Plant Health Inspection Service, U.S. Department of Agriculture.

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Authors and Affiliations

  1. Southeastern Cooperative Wildlife Disease Study (SCWDS), Department of Population Health, College of Veterinary Medicine, University of Georgia, Athens, GA, USA

    Christopher A. Cleveland, Stacey Vigil, Daniel G. Mead & Joseph L. Corn

  2. Center for Ecology of Infectious Diseases, Odum School of Ecology, University of Georgia, Athens, GA, USA

    Christopher A. Cleveland & Andrew W. Park

  3. Department of Biological Sciences, University of South Carolina, Columbia, SC, 29205, USA

    Tad A. Dallas

  4. Odum School of Ecology, University of Georgia, 140 E. Green Street, Athens, GA, 30602, USA

    Andrew W. Park

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  1. Christopher A. Cleveland
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  2. Tad A. Dallas
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  3. Stacey Vigil
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  5. Joseph L. Corn
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Contributions

CAC, TAD, and AWP made substantial contributions to conception and design, and analysis and interpretation of data; CAC, SV, DGM, and JLC made substantial contributions to the acquisition of data. All authors were involved in drafting the manuscript or revising it critically for important intellectual content and have given final approval of the version to be published.

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Correspondence to Christopher A. Cleveland, Tad A. Dallas or Andrew W. Park.

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Christopher A. Cleveland and Tad A. Dallas are joint first authors.

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Cleveland, C.A., Dallas, T.A., Vigil, S. et al. Vector communities under global change may exacerbate and redistribute infectious disease risk. Parasitol Res 122, 963–972 (2023). https://doi.org/10.1007/s00436-023-07799-2

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