You are not currently logged in.

Access your personal account or get JSTOR access through your library or other institution:


Log in to your personal account or through your institution.

Are All Hosts Created Equal? Partitioning Host Species Contributions to Parasite Persistence in Multihost Communities

Andy Fenton, Daniel G. Streicker, Owen L. Petchey and Amy B. Pedersen
The American Naturalist
Vol. 186, No. 5 (November 2015), pp. 610-622
DOI: 10.1086/683173
Stable URL:
Page Count: 13
Subjects: Ecology & Evolutionary Biology Biological Sciences
  • Download PDF
  • Add to My Lists
  • Cite this Item
Are All Hosts Created Equal? Partitioning Host Species Contributions to Parasite Persistence in Multihost Communities
We're having trouble loading this content. Download PDF instead.


AbstractMany parasites circulate endemically within communities of multiple host species. To understand disease persistence within these communities, it is essential to know the contribution each host species makes to parasite transmission and maintenance. However, quantifying those contributions is challenging. We present a conceptual framework for classifying multihost sharing, based on key thresholds for parasite persistence. We then develop a generalized technique to quantify each species’ contribution to parasite persistence, allowing natural systems to be located within the framework. We illustrate this approach using data on gastrointestinal parasites circulating within rodent communities and show that, although many parasites infect several host species, parasite persistence is often driven by just one host species. In some cases, however, parasites require multiple host species for maintenance. Our approach provides a quantitative method for differentiating these cases using minimal reliance on system-specific parameters, enabling informed decisions about parasite management within poorly understood multihost communities.

Notes and References

This item contains 46 references.

Literature Cited
  • ['Anderson, R. M., and R. M. May. 1978. Regulation and stability of host-parasite population interactions. I. Regulatory processes. Journal of Animal Ecology 47:219–247.']
  • ['Barbour, A. D. 1996. Modeling the transmission of schistosomiasis: an introductory view. American Journal of Tropical Medicine and Hygiene 55:135–143.']
  • ['Begon, M. 2008. Effects of host diversity on disease dynamics. Pages 12–29 in R. O. Ostfeld, F. Keesing, and V. T. Evier, eds. Infectious disease ecology: effects of ecosystems on disease and of disease on ecosystems. Princeton University Press, Princeton, NJ.']
  • ['Begon, M., R. G. Bowers, N. Kadiankis, and D. E. Hodgkinson. 1992. Disease and community structure: the importance of host self-regulation in a host-host-pathogen model. American Naturalist 139:1131–1150.']
  • ['Biek, R., A. O’Hare, D. Wright, T. Mallon, C. McCormick, R. J. Orton, S. McDowell, H. Trewby, R. A. Skuce, and R. R. Kao. 2012. Whole genome sequencing reveals local transmission patterns of Mycobacterium bovis in sympatric cattle and badger populations. PLoS Pathogens 8:e1003008.']
  • ['Bielby, J., C. A. Donnelly, L. C. Pope, T. Burke, and R. Woodroffe. 2014. Badger responses to small-scale culling may compromise targeted control of bovine tuberculosis. Proceedings of the National Academy of Sciences of the USA 111:9193–9198.']
  • ['Bowers, R. G., and M. Begon. 1991. A host-host-pathogen model with free-living infective stages, applicable to microbial pest control. Journal of Theoretical Biology 148:305–329.']
  • ['Bowers, R. G., and J. Turner. 1997. Community structure and the interplay between interspecific infection and competition. Journal of Theoretical Biology 187:95–109.']
  • ['Carslake, D., M. Bennett, S. Hazel, S. Telfer, and M. Begon. 2006. Inference of cowpox virus transmission rates between wild rodent host classes using space-time interaction. Proceedings of the Royal Society B: Biological Sciences 273:775–782.']
  • ['Cleaveland, S., M. K. Laurenson, and L. H. Taylor. 2001. Diseases of humans and their domestic mammals: pathogen characteristics, host range and the risk of emergence. Philosophical Transactions of the Royal Society B: Biological Sciences 356:991–999.']
  • ['Diekmann, O., and J. A. P. Heesterbeek. 2000. Mathematical epidemiology of infectious diseases: model building, analysis and interpretation. Wiley, Chichester.']
  • ['Dobson, A. 2004. Population dynamics of pathogens with multiple host species. American Naturalist 164(suppl.):S64–S78.']
  • ['Donnelly, C. A., R. Woodroffe, D. R. Cox, J. Bourne, G. Gettinby, A. M. Le Fevre, J. P. McInerney, and W. I. Morrison. 2003. Impact of localized badger culling on tuberculosis incidence in British cattle. Nature 426:834–837.']
  • ['Fenton, A., and A. B. Pedersen. 2005. Community epidemiology framework for classifying disease threats. Emerging Infectious Diseases 11:1815–1821.']
  • ['Fenton, A., D. G. Streicker, O. L. Petchey, and A. B. Pedersen. 2015. Data from: Are all hosts created equal? partitioning host species contributions to parasite persistence in multihost communities. American Naturalist, Dryad Digital Repository,']
  • ['Fenton, A., M. E. Viney, and J. Lello. 2010. Detecting interspecific macroparasite interactions from ecological data: patterns and process. Ecology Letters 13:606–615.']
  • ['Funk, S., H. Nishiura, H. Heesterbeek, W. J. Edmunds, and F. Checchi. 2013. Identifying transmission cycles at the human-animal interface: the role of animal reservoirs in maintaining gambiense human African trypanosomiasis. PLoS Computational Biology 9:e1002855.']
  • ['Gray, D. J., G. M. Williams, Y. Li, and D. P. McManus. 2008. Transmission dynamics of Schistosoma japonicum in the lakes and marshlands of China. PLoS ONE 3:e4058.']
  • ['Greenman, J. V., and P. J. Hudson. 1999. Host exclusion and coexistence in apparent and direct competition: an application of bifurcation theory. Theoretical Population Biology 56:48–64.']
  • ['———. 2000. Parasite-mediated and direct competition in a two-host shared macroparasite system. Theoretical Population Biology 57:13–34.']
  • ['Hairston, N. G. 1965. An analysis of age-prevalence data by catalytic models: a contribution to the study of bilharziasis. Bulletin of the World Health Organization 33:163–175.']
  • ['Haydon, D. T., S. Cleaveland, L. H. Taylor, and M. K. Laurenson. 2002. Identifying reservoirs of infection: a conceptual and practical challenge. Emerging Infectious Diseases 8:1468–1473.']
  • ['Holt, R. D., A. P. Dobson, M. Begon, R. G. Bowers, and E. M. Schauber. 2003. Parasite establishment in host communities. Ecology Letters 6:837–842.']
  • ['Holt, R. D., and J. Pickering. 1985. Infectious disease and species coexistence: a model of Lotka-Volterra form. American Naturalist 126:196–211.']
  • ['Ionides, E. L., C. Breto, and A. A. King. 2006. Inference for nonlinear dynamical systems. Proceedings of the National Academy of Sciences of the USA 103:18438–18443.']
  • ['Ishikawa, H., H. Ohmae, R. Pangilinan, A. Redulla, and H. Matsuda. 2006. Modeling the dynamics and control of Schistosoma japonicum transmission on Bohol island, the Philippines. Parasitology International 55:23–29.']
  • ['Keesing, F., R. D. Holt, and R. S. Ostfeld. 2006. Effects of species diversity on disease risk. Ecology Letters 9:485–498.']
  • ['Kilpatrick, A. M., P. Daszak, M. J. Jones, P. P. Marra, and L. D. Kramer. 2006. Host heterogeneity dominates West Nile virus transmission. Proceedings of the Royal Society B: Biological Sciences 273:2327–2333.']
  • ['Krebs, J. R., R. M. Anderson, T. Clutton-Brock, C. A. Donnelly, S. Frost, W. I. Morrison, R. Woodroffe, and D. Young. 1998. Badgers and bovine TB: conflicts between conservation and health. Science 279:817–818.']
  • ['Kuiken, T., E. C. Holmes, J. McCauley, G. F. Rimmelzwaan, C. S. Williams, and B. T. Grenfell. 2006. Host species barriers to influenza virus infections. Science 312:394–397.']
  • ['Lembo, T., D. T. Haydon, A. Velasco-Villa, C. E. Rupprecht, C. Packer, P. E. Brandao, I. V. Kuzmin, A. R. Fooks, J. Barrat, and S. Cleaveland. 2007. Molecular epidemiology identifies only a single rabies virus variant circulating in complex carnivore communities of the Serengeti. Proceedings of the Royal Society B: Biological Sciences 274:2123–2130.']
  • ['Lloyd-Smith, J. O., D. George, K. M. Pepin, V. E. Pitzer, J. R. C. Pulliam, A. P. Dobson, P. J. Hudson, and B. T. Grenfell. 2009. Epidemic dynamics at the human-animal interface. Science 326:1362–1367.']
  • ['Lloyd-Smith, J. O., S. J. Schreiber, P. E. Kopp, and W. M. Getz. 2005. Superspreading and the effect of individual variation on disease emergence. Nature 438:355–359.']
  • ['LoGiudice, K., R. S. Ostfeld, K. A. Schmidt, and F. Keesing. 2003. The ecology of infectious disease: effects of host diversity and community composition on Lyme disease risk. Proceedings of the National Academy of Sciences of the USA 100:567–571.']
  • ['Montresor, A., A. F. Gabrielli, A. Yajima, N. Lethanh, B.-A. Biggs, G. J. Casey, T. T. Tinh, D. Engels, and L. Savioli. 2013. Markov model to forecast the change in prevalence of soil-transmitted helminths during a control programme: a case study in Vietnam. Transactions of the Royal Society of Tropical Medicine and Hygiene 107:313–318.']
  • ['Pedersen, A. B., S. Altizer, M. Poss, A. A. Cunningham, and C. L. Nunn. 2005. Patterns of host specificity and transmission among parasites of wild primates. International Journal for Parasitology 35:647–657.']
  • ['Roeder, P., J. Mariner, and R. Kock. 2013. Rinderpest: the veterinary perspective on eradication. Philosophical Transactions of the Royal Society B: Biological Sciences 368:20120139.']
  • ['Rudge, J. W., J. P. Webster, D.-B. Lu, T.-P. Wang, G.-R. Fang, and M.-G. Basanez. 2013. Identifying host species driving transmission of Schistosomiasis japonica, a multihost parasite system, in China. Proceedings of the National Academy of Sciences of the USA 110:11457–11462.']
  • ['Shrestha, S., B. Foxman, D. M. Weinberger, C. Steiner, C. Viboud, and P. Rohani. 2013. Identifying the interaction between influenza and pneumococcal pneumonia using incidence data. Science Translational Medicine 5:191ra84.']
  • ['Streicker, D. G., A. Fenton, and A. B. Pedersen. 2013. Differential sources of host species heterogeneity influence the transmission and control of multihost parasites. Ecology Letters 16:975–984.']
  • ['Streicker, D. G., A. S. Turmelle, M. J. Vonhof, I. V. Kuzmin, G. F. McCracken, and C. E. Rupprecht. 2010. Host phylogeny constrains cross-species emergence and establishment of rabies virus in bats. Science 329:676–679.']
  • ['Tompkins, D. M., A. W. Sainsbury, P. Nettleton, D. Buxton, and J. Gurnell. 2002. Parapoxvirus causes a deleterious disease in red squirrels associated with UK population declines. Proceedings of the Royal Society B: Biological Sciences 269:529–533.']
  • ['Viana, M., S. Cleaveland, J. Matthiopoulos, J. Halliday, C. Packer, M. E. Craft, K. Hampson, et al. 2015. Dynamics of a morbillivirus at the domestic-wildlife interface: canine distemper virus in domestic dogs and lions. Proceedings of the National Academy of Sciences of the USA 112:1464–1469.']
  • ['Viana, M., R. Mancy, R. Biek, S. Cleaveland, P. C. Cross, J. O. Lloyd-Smith, and D. T. Haydon. 2014. Assembling evidence for identifying reservoirs of infection. Trends in Ecology and Evolution 29:270–279.']
  • ['Williams, G. M., A. C. Sleigh, Y. S. Li, Z. Feng, G. M. Davis, H. G. Chen, A. G. P. Ross, R. Bergquist, and D. P. McManus. 2002. Mathematical modelling of Schistosomiasis japonica: comparison of control strategies in the People’s Republic of China. Acta Tropica 82:253–262.']
  • ['Woolhouse, M. E. J., L. H. Taylor, and D. T. Haydon. 2001. Population biology of multihost pathogens. Science 292:1109–1112.']