Lions and Prions and Deer Demise Michael W. Miller1*, Heather M. Swanson2, Lisa L. Wolfe1, Fred G. Quartarone1, Sherri L. Huwer1, Charles H. Southwick3, Paul M. Lukacs1 1 Colorado Division of Wildlife, Wildlife Research Center, Fort Collins, Colorado, United States of America, 2 City of Boulder Open Space and Mountain Parks, Boulder, Colorado, United States of America, 3 Department of Ecology and Evolutionary Biology, University of Colorado at Boulder, Boulder, Colorado, United States of America Abstract Background: Contagious prion diseases – scrapie of sheep and chronic wasting disease of several species in the deer family – give rise to epidemics that seem capable of compromising host population viability. Despite this prospect, the ecological consequences of prion disease epidemics in natural populations have received little consideration. Methodology/Principal Findings: Using a cohort study design, we found that prion infection dramatically lowered survival of free-ranging adult (.2-year-old) mule deer (Odocoileus hemionus): estimated average life expectancy was 5.2 additional years for uninfected deer but only 1.6 additional years for infected deer. Prion infection also increased nearly fourfold the rate of mountain lions (Puma concolor) preying on deer, suggesting that epidemics may alter predator–prey dynamics by facilitating hunting success. Despite selective predation, about one fourth of the adult deer we sampled were infected. High prevalence and low survival of infected deer provided a plausible explanation for the marked decline in this deer population since the 1980s. Conclusion: Remarkably high infection rates sustained in the face of intense predation show that even seemingly complete ecosystems may offer little resistance to the spread and persistence of contagious prion diseases. Moreover, the depression of infected populations may lead to local imbalances in food webs and nutrient cycling in ecosystems in which deer are important herbivores. Citation: Miller MW, Swanson HM, Wolfe LL, Quartarone FG, Huwer SL, et al. (2008) Lions and Prions and Deer Demise. PLoS ONE 3(12): e4019. doi:10.1371/ journal.pone.0004019 Editor: Matthew Baylis, University of Liverpool, United Kingdom Received November 3, 2008; Accepted November 25, 2008; Published December 24, 2008 Copyright: 2008 Miller et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Funding: Our funding came from the Colorado Division of Wildlife, the City of Boulder, and the US Department of Agriculture, Animal&Plant Health Inspection Service, Veterinary Services. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist. * E-mail: mike.miller@state.co.us Introduction Prion diseases affect several mammalian species worldwide, with notable economic and health implications [1,2]. Two of the known prion diseases are contagious: scrapie of domestic sheep and goats [3] and chronic wasting disease of several species in the deer family [4,5]. Chronic wasting disease epidemics occur naturally in some native North American deer (Odocoileus spp.), wapiti (Cervus elaphus nelsoni), and moose (Alces alces) populations [5,6], but whether prion disease was part of the evolutionary history of these host species or is a newly emerging pathogen remains unknown [4–6]. Another lingering uncertainty is the effect of natural prion infection on individual host survival and the cumulative impacts of epidemics on population performance and stability. In the absence of empirical data, such effects have been forecast using models [6–8] parameterized from observations of natural and experimental prion infections in captive deer [4,8–10]. Regardless of whether transmission is assumed to be density- or frequency- dependent, unmanaged epidemics are predicted to depress deer populations over the course of several decades. If manifested as predicted, the impacts of prion disease epidemics would extend not only to the health and stability of affected host populations, but also perhaps to the health and stability of ecosystems where these species are the primary large herbivores and important as prey. To begin understanding the implications of prion disease epidemics for native ecosystems and food webs, we measured the effects of prion infection on survival of mule deer (O. hemionus) residing on Table Mesa and the lower slopes of Green and Bear mountains southwest of Boulder in northcentral Colorado, USA, an area collectively referred to here as ‘‘Table Mesa’’. Results Annual survival of prion-infected adult (.2 year old) deer (0.53, 95% binomial confidence interval [CI] 0.39–0.66; n = 57) was markedly lower than survival of uninfected deer (0.82, 95% binomial CI 0.70–0.91; n = 57) (x2 = 9.65, P = 0.0019, hazard ratio = 3.84, 95% CI 1.64–8.99; Table 1) (Fig. 1A). Estimated average life expectancy for infected deer was only an additional 1.6 years, compared to an additional 5.2 years for uninfected deer. Overall survival was similar between sexes (x2 = 0.07, P = 0.79; Table 1). Nearly 75% of the infected deer that died did so during the winter months (November–April) (Fig. 1A). Thirteen of the 27 infected deer that died apparently succumbed to the ‘‘chronic wasting’’ syndrome [4,5] and 11 others were killed by mountain lions (Puma concolor) (Fig. 2). Few of the deer killed by mountain lions were recorded as noticeably ill by field observers prior to their deaths, suggesting that relatively PLoS ONE | www.plosone.org 1 December 2008 | Volume 3 | Issue 12 | e4019