REVIEWS Detecting disease and parasite threats to endangeredspecies and ecosystems Hamish McCallum and Andy Dobson T here are numerous examples of parasites and diseases posing major threats to populations of endangered species. The impact of malaria on much of the Hawaiian avifaunal and that of distemper on the black- footed ferret (Mustela nigr@es)2 are perhaps the best known cases, although recent reviews of the effect of disease on birds3 and African mammals4 suggest that the prob- lem is widespread. Disease may have caused the most notorious of Australia’s extinctions: that of the thylacine or marsupial wolf (see Box 1). Nevertheless, disease re- mains a relatively neglected topic in conservation biology. Ecologists have recently begun to acknowledge the importance of disease and parasites in the dynamics of populations. Diseases and parasites have probably been responsible for a number of extinctions on islands and on large land masses, but the problem has only been identified in retrospect. In contrast, endemic pathogens and parasites may operate as keystone species, playing a crucial role in maintaining the diversity of ecological communities and ecosystems. Will recent advances in the understanding of parasite population biology allow us to predict threats to endangered species and communities? A particular problem is that an epidemic often only becomes ap parent after it has reached extreme levels. This may be because mor- bid animals are removed rapidly Hamish McCallum is at the Dept of Zoology and Centre for Conservation Biology, University of Queensland, St Lucia, Queensland 4072, Australia; Andy Dobson is at the Dept of Biology, Princeton University, Princeton, NJ 08544-1003, USA. by scavengers or predators, or simply because of the inac- cessibility of many wildlife populationss. - Since the pioneering work of Anderson and May in the late 1970#, there has been increasing interest in the impact of diseases and parasites at a population (as distinct from individual) level. In 1987, the Society for Conservation Biology included a special session on disease in its annual meetings. In this review, we focus on developments since that meeting that relate to wild populations of threatened species. Diseases and parasites pose particularly severe problems in captive populations, in which animals are held at high density, may be stressed and may be exposed to cross-species transmissiong. Reintroduced animals and wild populations’0 involved in reintroduction or translocation programs are also at risk. If a disease were affecting your endangered population, what might you see? Mathematical models of microparasitic diseases (typi- callyviruses, bacteria and protozoa) that primarily affect host mortality show that pathogens present in most hosts do not depress population equilibria far below their disease-free carrying capacityll. The same models show that highly patho- genic diseases also have a minor effect on host populations. These models thus suggest that if a disease is detectable at high prevalence (i.e. it occurs in most hosts), it is probably mild and unlikely to be a major problem to an endangered species, and that diseases shown to be highly pathogenic in the laboratory are also unlikely to cause problems, particu- larly in low-density populations, because infected animals die before the disease can be spread. These conclusions are subject to two major qualifications. First, they are single-host species models. Many pathogens implicated in extinctions have other reservoir hosts within 190 0 1995, Else&r Science Ltd which they are relatively benignlJ. The implications of this are ex- plored in the following section. Second, the models assume that the disease primarily increases mortality. If the main effect on the host is that fecundity is decreased, diseases present at high prevalence may have a major impact on their host population12 (Fig. 1). Similar conclusions can be drawn from models of macro- parasitic (typically helminth) in- fectionsl3. However, things are complicated considerably by the likelihood that parasite fecundity and survival will decline in heavily infected hosts. If these density dependent constraints on parasite survival and fecundity are weak, parasites with low pathogenicity per parasite have the most impact on hosts; in contrast, if parasite fecundity or survival is strongly density dependent, parasites with higher pathogenicity will have greater impact on their hostsl2. Box 2 shows how these simple models can be used to quantify the impact of a parasite or pathogen on a host popu- lation, provided that data are available on the effects on host individuals and on the extent of infection within the host population. It is important to remember, however, that these results apply only to single-host infections that can be assumed to be at equilibrium. A pulse of mortality in a population, coupled with high disease prevalence or mean parasite burden, is often used intuitively to infer that a disease is affecting a populatiorW. Such a pattern may, however, be quite misleading. Given that the equilibrium prevalence of benign infections is high, one may simply be observing a relatively harmless infection with the deaths occurring for a quite separate reason. Figure 2 shows disease prevalence in dead and dying hosts as a function of pathogenicity. Surprisingly, the more patho genie a disease, the smaller the proportion of morbid hosts that will carry it. The figure also shows the prevalence of dis- ease in the total population and the extent of disease impact. For pathogens that are specific to a single host species, a substantial difference will be apparent in disease preva- lence between morbid hosts and the general population. However, a similar pattern would also be observed if some third factor, such as stress, caused morbidity and low resist- ance to infection. Parasites and pathogens with reservoir hosts Pathogens that infect a range of host species have caused a variety of problems for endangered species. For example, canine distemper virus caused a large decline in the last re- maining free-living colony of black-footed ferretsz. Although TREE uol. IO, no. 5 May 1995