Declines in large wildlife increase landscape-level prevalence of rodent-borne disease in Africa
- aDepartment of Ecology, Evolution, and Marine Biology, University of California, Santa Barbara, CA 93106;
- bDepartment of Biology and
- fWoods Institute for the Environment, Stanford University, Stanford, CA 94305;
- cDivision of Mammals, National Museum of Natural History, Smithsonian Institution, Washington, DC 20013;
- dDivision of Vector-Borne Infectious Diseases, National Center for Infectious Diseases, Centers for Disease Control and Prevention, Fort Collins, CO 80521;
- eDepartment of Biology, Colorado Sate University, Fort Collins, CO 80523;
- gDepartment of Plant Sciences, University of California, Davis, CA 95616; and
- hDepartment of Biological Sciences, University at Buffalo, The State University of New York, Buffalo, NY 14260
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Contributed by Rodolfo Dirzo, March 26, 2014 (sent for review December 10, 2013)

Significance
Understanding the effects of biodiversity loss on zoonotic disease is of pressing importance to both conservation science and public health. This paper provides experimental evidence of increased landscape-level disease risk following declines in large wildlife, using the case study of the rodent-borne zoonosis, bartonellosis, in East Africa. This pattern is driven not by changes in community composition or diversity of hosts, as frequently proposed in other systems, but by increases in abundance of susceptible hosts following large mammal declines. Given that rodent increases following large wildlife declines appear to be a widespread pattern, we suggest this relationship is likely to be general.
Abstract
Populations of large wildlife are declining on local and global scales. The impacts of this pulse of size-selective defaunation include cascading changes to smaller animals, particularly rodents, and alteration of many ecosystem processes and services, potentially involving changes to prevalence and transmission of zoonotic disease. Understanding linkages between biodiversity loss and zoonotic disease is important for both public health and nature conservation programs, and has been a source of much recent scientific debate. In the case of rodent-borne zoonoses, there is strong conceptual support, but limited empirical evidence, for the hypothesis that defaunation, the loss of large wildlife, increases zoonotic disease risk by directly or indirectly releasing controls on rodent density. We tested this hypothesis by experimentally excluding large wildlife from a savanna ecosystem in East Africa, and examining changes in prevalence and abundance of Bartonella spp. infection in rodents and their flea vectors. We found no effect of wildlife removal on per capita prevalence of Bartonella infection in either rodents or fleas. However, because rodent and, consequently, flea abundance doubled following experimental defaunation, the density of infected hosts and infected fleas was roughly twofold higher in sites where large wildlife was absent. Thus, defaunation represents an elevated risk in Bartonella transmission to humans (bartonellosis). Our results (i) provide experimental evidence of large wildlife defaunation increasing landscape-level disease prevalence, (ii) highlight the importance of susceptible host regulation pathways and host/vector density responses in biodiversity–disease relationships, and (iii) suggest that rodent-borne disease responses to large wildlife loss may represent an important context where this relationship is largely negative.
Footnotes
- ↵1To whom correspondence should be addressed. E-mail: rdirzo{at}stanford.edu.
Author contributions: H.S.Y., R.D., K.M.H., D.J.M., and T.P.Y. designed research; H.S.Y., R.D., K.M.H., D.J.M., S.A.B., M.Y.K., L.M.O., D.J.S., and K.D. performed research; H.S.Y. and R.D. analyzed data; and H.S.Y., R.D., K.M.H., and D.J.M. wrote the paper.
The authors declare no conflict of interest.
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1404958111/-/DCSupplemental.
Freely available online through the PNAS open access option.