REVIEW Mechanisms of disease-induced extinction Francisco de Castro* and Benjamin Bolker Department of Zoology, University of Florida, 223 Bartram Hall, Box 118525, Gainesville, FL 32611-8525, USA *Correspondence: E-mail: fdcastro@ufl.edu Abstract Parasites are important determinants of ecological dynamics. Despite the widespread perception that parasites (in the broad sense, including microbial pathogens) threaten species with extinction, the simplest deterministic models of parasite dynamics (i.e. of specialist parasites with density-dependent transmission) predict that parasites will always go extinct before their hosts. We review the primary theoretical mechanisms that allow disease-induced extinction and compare them with the empirical literature on parasitic threats to populations to assess the importance of different mechanisms in threatening natural populations. Small pre-epidemic population size and the presence of reservoirs are the most commonly cited factors for disease-induced extinction in empirical studies. Keywords Dynamics, reservoir, frequency-dependent, parasite, spatial, specialist. 2 Ecology Letters (2005) 8: 117–126 INTRODUCTION Parasites and disease are frequently cited as important drivers of population and community dynamics (Anderson & May 1992; McCallum & Dobson 1995; Levin et al. 1997; Hudson & Greenman 1998; Norman et al. 1999; Kohler & Hoiland 2001; Hudson et al. 2002; Shea & Chesson 2002 3 ; MacNeil et al. 2003). In conservation biology, disease is presented as a threat to population viability and a contributing factor to disease extinction (McCallum & Dobson 1995). However, the simplest disease models – which have formed the theoretical foundation for the field of disease ecology – suggest that disease alone cannot drive host populations extinct (Anderson & May 1992). More specifically, determi- nistic models of directly transmitted specialist parasites with density-dependent transmission predict that disease will always die out when the host population falls below a (non- zero) threshold density, before the host population can go extinct (Swinton et al. 1998; McCallum et al. 2001); stochastic models suggest that disease will often go extinct by so-called Ôfade-outÕ even above this threshold (Bartlett 1960; Black 1966; Keeling & Grenfell 1997). The first part of this paper reviews the important exceptions to these simple conclu- sions – the qualitative mechanisms that drive disease-induced extinction in theoretical models. The second reviews the existing empirical literature on disease-induced extinction, and makes a first attempt to assess the relative importance of the different mechanisms in natural systems. The literature search was performed in the ISI Web of Science, selecting any article containing the words [Ôextinct*Õ AND (ÔdiseaseÕ OR Ôparasit*Õ OR ÔpathogenÕ)] in the title, abstract or keywords. In total, 336 references were found. References to the coefficient of extinction of some substance (typically in the context of human physiology and medicine), articles that only vaguely mentioned disease as a possible threat for populations, and those referring to the extinction of parasites (rather than hosts) were dropped (260 in total). The remaining articles (76), which are the base of this review, were classified as either theoretical (33) or empirical (43) (some quantitative simulation models of specific host– parasite systems were included in the empirical rather than the theoretical section). We are aware that the so-called Ôgray literatureÕ, not covered by the Web of Science, contains many references on conservation subjects, but we feel confident that our reference base is representative. We have not included cases of captive populations, since they are subjected to conditions very different from wild populations. THEORETICAL MECHANISMS The list of adjectives qualifying Ôdisease modelsÕ above – deterministic, density-dependent, specialist – suggests the mechanisms that allow diseases to drive their hosts extinct in models. Disease can drive populations temporarily or permanently to low numbers or densities, predisposing them to extinction by demographic stochasticity or Allee effects; diseases with frequency-dependent or spatial transmission can remain at high incidence even when populations have become globally rare; and diseases that can exploit other hosts (biotic reservoirs) or survive and grow in the environment (abiotic reservoirs) can remain at high incidence independent of population crashes in the focal host (Table 1). Ecology Letters, (2005) 8: 117–126 doi: 10.1111/j.1461-0248.2004.00693.x Ó2004 Blackwell Publishing Ltd/CNRS