Hostname: page-component-78c5997874-j824f Total loading time: 0 Render date: 2024-11-10T08:33:51.691Z Has data issue: false hasContentIssue false

Vector species richness increases haemorrhagic disease prevalence through functional diversity modulating the duration of seasonal transmission

Published online by Cambridge University Press:  24 July 2015

ANDREW W. PARK*
Affiliation:
Odum School of Ecology, University of Georgia, 140 E. Green Street, Athens, GA 30602, USA Department of Infectious Diseases, College of Veterinary Medicine, University of Georgia, 501 D.W. Brooks Drive, Athens, GA 30602, USA
CHRISTOPHER A. CLEVELAND
Affiliation:
Southeastern Cooperative Wildlife Disease Study (SCWDS), Department of Population Health, College of Veterinary Medicine, University of Georgia, 589 D.W. Brooks Drive, Athens, GA 30602, USA
TAD A. DALLAS
Affiliation:
Odum School of Ecology, University of Georgia, 140 E. Green Street, Athens, GA 30602, USA
JOSEPH L. CORN
Affiliation:
Southeastern Cooperative Wildlife Disease Study (SCWDS), Department of Population Health, College of Veterinary Medicine, University of Georgia, 589 D.W. Brooks Drive, Athens, GA 30602, USA
*
*Corresponding author: Odum School of Ecology, University of Georgia, 140 E. Green Street, Athens, GA 30602, USA. E-mail: awpark@uga.edu

Summary

Although many parasites are transmitted between hosts by a suite of arthropod vectors, the impact of vector biodiversity on parasite transmission is poorly understood. Positive relationships between host infection prevalence and vector species richness (SR) may operate through multiple mechanisms, including (i) increased vector abundance, (ii) a sampling effect in which species of high vectorial capacity are more likely to occur in species-rich communities, and (iii) functional diversity whereby communities comprised species with distinct phenologies may extend the duration of seasonal transmission. Teasing such mechanisms apart is impeded by a lack of appropriate data, yet could highlight a neglected role for functional diversity in parasite transmission. We used statistical modelling of extensive host, vector and microparasite data to test the hypothesis that functional diversity leading to longer seasonal transmission explained variable levels of disease in a wildlife population. We additionally developed a simple transmission model to guide our expectation of how an increased transmission season translates to infection prevalence. Our study demonstrates that vector SR is associated with increased levels of disease reporting, but not via increases in vector abundance or via a sampling effect. Rather, the relationship operates by extending the length of seasonal transmission, in line with theoretical predictions.

Type
Special Issue Article
Copyright
Copyright © Cambridge University Press 2015 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Anderson, R. M. and May, R. M. (1992). Infectious Diseases of Humans: Dynamics and Control. Oxford University Press, Oxford.Google Scholar
Borkent, A. and Grogan, W. L. (2009). Catalog of the New World biting midges north of Mexico (Diptera: Ceratopogonidae). Zootaxa 2273, 148.Google Scholar
Cadotte, M. W., Carscadden, K. and Mirotchnick, N. (2011). Beyond species: functional diversity and the maintenance of ecological processes and services. Journal of Applied Ecology 48, 10791087.Google Scholar
Chesson, P. (2000). Mechanisms of maintenance of species diversity. Annual Review of Ecology and Systematics 31, 343366.Google Scholar
Craine, J. M., Ocheltree, T. W., Nippert, J. B., Towne, E. G., Skibbe, A. M., Kembel, S. W. and Fargione, J. E. (2012). Global diversity of drought tolerance and grassland climate-change resilience. Nature Climate Change 3, 6367.Google Scholar
Diekmann, O., Heesterbeek, H. and Britton, T. (2013). Mathematical Tools for Understanding Infectious Disease Dynamics. Princeton University Press, Princeton, NJ.Google Scholar
Díaz, S. and Cabido, M. (2001). Vive la différence: plant functional diversity matters to ecosystem processes. Trends in Ecology & Evolution 16, 646655.Google Scholar
Dye, C. (1986). Vectorial capacity: must we measure all its components? Parasitology Today 2, 203209.Google Scholar
Gaydos, J. K., Davidson, W. R., Elvinger, F., Howerth, E. W., Murphy, M. and Stallknecht, D. E. (2002). Cross-protection between epizootic hemorrhagic disease virus serotypes 1 and 2 in white-tailed deer. Journal of Wildlife Diseases 38, 720728.Google Scholar
Gibbs, E. P. J. and Greiner, E. C. (1989). Bluetongue and epizootic hemorrhagic disease. The Arboviruses: Epidemiology and Ecology 2, 3070.Google Scholar
Jones, K. E., Patel, N. G., Levy, M. A., Storeygard, A., Balk, D., Gittleman, J. L. and Daszak, P. (2008). Global trends in emerging infectious diseases. Nature 451, 990993.Google Scholar
Keeling, M. J. and Rohani, P. (2008). Modeling Infectious Diseases in Humans and Animals. Princeton University Press, Princeton, NJ.Google Scholar
Lambin, E. F., Tran, A., Vanwambeke, S. O., Linard, C. and Soti, V. (2010). Pathogenic landscapes: interactions between land, people, disease vectors, and their animal hosts. International Journal of Health Geographics 9, 54.Google Scholar
Leps, J., De Bello, F., Lavorel, S. and Berman, S. (2006). Quantifying and interpreting functional diversity of natural communities: practical considerations matter. Preslia 78, 481501.Google Scholar
Lord, C. C. (2010). The effect of multiple vectors on arbovirus transmission. Israel Journal of Ecology & Evolution 56, 371392.Google Scholar
Mellor, P. S., Boorman, J. and Baylis, M. (2000). Culicoides biting midges: their role as arbovirus vectors. Annual Review of Entomology 45, 307340.Google Scholar
Nettles, V. F. and Stallknecht, D. E. (1992). History and progress in the study of hemorrhagic disease of deer. Transactions of the North American Wildlife and Natural Resources Conference 57, 499–516.Google Scholar
Park, A. W., Magori, K., White, B. A. and Stallknecht, D. E. (2013). When more transmission equals less disease: reconciling the disconnect between disease hotspots and parasite transmission. PloS ONE 8, e61501.Google Scholar
Petchey, O. L. and Gaston, K. J. (2002). Functional diversity (FD), species richness and community composition. Ecology Letters 5, 402411.Google Scholar
Roy, P. (1996). Orbiviruses and their Replication. In Fields Virology (ed. Fields, B.N.), pp. 17091731. Lippincott-Raven, Philadelphia, PA.Google Scholar
Sala, O., Chapin, F., Armesto, J., Berlow, E., Bloomfield, J., Dirzo, R., Huber-Sanwald, E., Huenneke, L., Jackson, R., Kinzig, A., Leemans, R., Lodge, D., Mooney, H., Oesterheld, M., Poff, N., Sykes, M., Walker, B., Walker, M. and Wall, D. (2000). Global biodiversity scenarios for the year 2100, Science 287, 17701774.CrossRefGoogle ScholarPubMed
Sardelis, M. R., Turell, M. J., Dohm, D. J. and O'Guinn, M. L. (2001). Vector competence of selected North American Culex and Coquillettidia mosquitoes for West Nile virus. Emerging Infectious Diseases 7, 10181022.Google Scholar
Smith, K. E., Stallknecht, D. E. and Nettles, V. F. (1996). Experimental infection of Culicoides lahillei (Diptera: Ceratopogonidae) with epizootic hemorrhagic disease virus Serotype 2 (Orhivirus: Reoviridae). Journal of Medical Entomology 33, 117122.Google Scholar
Stallknecht, D., Kellogg, M., Blue, J. and Pearson, J. (1991). Antibodies to bluetongue and epizootic hemorrhagic disease viruses in a barrier island white-tailed deer population. Journal of Wildlife Diseases 27, 668674.CrossRefGoogle Scholar
Tilman, D. (1997). The influence of functional diversity and composition on ecosystem processes. Science 277, 13001302.Google Scholar
Toé, L., Tang, J., Back, C., Katholi, C. R. and Unnasch, T. R. (1997). Vector–parasite transmission complexes for onchocerciasis in West Africa. Lancet 349, 163166.CrossRefGoogle ScholarPubMed
Vigil, S. L., Grogan, W. L., Wlodowski, J. C., Parris, J., Edwards de Vargas, S., Shaw, D., Cleveland, C. and Corn, J. L. (2014). New records of biting midges of the genus Culicoides latreille from the Southeastern United States (Diptera: Ceratopoginidae). Insecta Mundi 394, 114.Google Scholar
Supplementary material: File

Park supplementary material

Park supplementary material 1

Download Park supplementary material(File)
File 768.1 KB