CAN DISEASES REGULATE WILD POPULATIONS?

Although the mortality from a disease can be dramatic, there often is little relationship between observed mortality and the effective­ness of a disease in limiting or regulating a host population.

However, there are cases where diseases can substantially influence wildlife popula­tions, especially on initial introduction to a population. Some microorganisms can sup­press wild host populations through reduced survival, reduced fecundity, or both (Scott 1988, Tompkins and Begon 1999, Hudson et al. 2003). In a classic case, myxoma virus, a poxvirus, has caused a long-term depression of European rabbit (Oryctolagus cuniculus) populations in Australia (Fenner and Ratcliffe 1965) and Europe (Ross 1982). Rabies also can temporarily suppress affected host populations (Bacon 1985). Canine distemper, a viral disease, has caused severe declines of some African lion (Panthera leo) populations (Morell 1994) as well as near extinction of black-footed ferrets (Mustela nigripes) (Thorne and Williams 1988).

Among macroparasites, there are a num­ber of studies with evidence for helminth and arthropod parasites effectively controlling wild animal populations through reduced survival or fecundity of the hosts (Tompkins and Begon 1999). The parasites involved included two spe­cies of fleas, four species of mites, two species of bugs, one species of fly, and three species of nematodes; the affected hosts included eight species of birds and three of mammals.

Among toxins, there is strong evidence that during their regular use, dichlorodiphenyltri­chloroethane (DDT) and other environmental toxins suppressed populations of raptors and fish-eating birds (Hickey and Anderson 1968). For example, use of DDT depressed peregrine falcon (Falco peregrinus) populations by reduc­ing eggshell thickness, interfering with cal­cium carbonate deposition in eggshells, and altering reproductive behaviors (Enderson and Berger 1970). Significant recovery of several raptorial and other bird species occurred after banning many persistent and bioaccumulative pesticides in the United States (Anderson et al. 1975, Spitzer et al. 1978, Grier 1982, Grue et al. 1983, Bolen and Robinson 2003).

Pathogens infecting a broad range of host species can cause serious problems for endan­gered populations (McCallum and Dobson 1995), and species-wide extinctions have been linked to diseases. For example, there is good evidence that avian malaria (Plasmodium relic- tum capistranoae) and avian pox (Poxviridae) have caused some population suppressions, local extirpations, and even species extinctions among native Hawaiian birds. These losses involved some complex interactions among the native hosts, introduced species of hosts, parasites, and vectors, as well as well as habitat (Warner 1968, van Riper et al. 1986). Interest­ingly, there also is recent evidence for limited species recovery among some native Hawaiian birds that did not become extinct (Woodworth et al. 2005). While it is highly likely that disease caused at least some of these extinctions, the evi­dence still is indirect. The first known definitive report of a parasite causing species extinction is the loss of a land snail (Pardula turgida) brought about by a microsporidian parasite (Steinhausia spp.) (Cunningham and Daszak 1998).

Bighorn sheep (Oris canadensis) introduced into Lava Beds National Monument, California, were locally extirpated from effects of Pasteu- rella multocida pneumonia in July 1980 follow­ing their apparent contact with domestic sheep on adjacent grazing leases (Foreyt and Jessup 1982). The response of managers to prevent this loss was complicated by political conflicts among the several federal and state agencies and ranchers with responsibilities for the ani­mals or land. There also is evidence that local populations of prairie dogs (Cynomys spp.) can be extirpated by bubonic plague in short-grass prairies (Kartman et al. 1962, Barnes 1982).

Rinderpest, a morbillivirus infection, historically caused substantial reductions among wild ungulate populations in Africa, including local extirpations of some species and significant changes in the species composition of African ungulates in many regions (Talbot and Talbot 1963, Holmes 1982, Plowright 1982, McCallum and Dobson 1995). This introduced pathogen swept through southern Africa between 1890 and 1899 and killed up to 90% ofthe populations of some native wild species (Plowright 1982). Rinderpest is benign in its ancient cattle host (McCallum and Dobson 1995), but highly virulent to the wildebeest (Connochaetes taurinus) and cape buffalo (Syncerus caffer), as well as introduced cattle recently exposed to this morbillivirus (Plowright 1982). Rinderpest exemplifies a disease in populations lacking past exposure or innate immunity; the causative virus infected a large proportion of the susceptible populations and mortality was high. Wild ungulates were blamed as reservoir hosts for susceptible breeds of European cattle and were slaughtered in areas around cattle ranches. However, control of rinderpest in Tanganyika wildlife through use of a vaccine in cattle in the 1950s provided evidence that cattle, rather than wildlife, played a central role as rinderpest reservoirs (Branagan and Hammond 1965). Plowright later concluded that even large populations, in excess of 100,000, of susceptible wild African ungulates were unable to sustain rinderpest infections in the absence of cattle (Plowright 1982).

Mathematical models of microparasitic diseases were developed to assess expected impacts of these diseases on their hosts (McCallum and Dobson 1995). Some generaliza­tions that emerged are that most pathogens do not depress host population equilibria far below their disease-free carrying capacity (Anderson 1979), and that parasites highly pathogenic for individuals usually have only a minor effect on host populations. Often, if a disease is detect­able at high prevalence, it probably is mild and unlikely to be a major problem to an endangered species. Also some parasites highly pathogenic in the laboratory are unlikely to cause problems in low-density populations because infected animals die before the disease can be spread.

These conclusions are subject to two major qualifications. First, they apply to single-host species models, and many pathogens implicated in extinctions of one host have other reservoir hosts in which they are relatively benign (van Riper et al. 1986, Thorne and Williams 1988). Thus if a pathogen is a generalist and an endangered species is susceptible, the pathogen can cause the endangered species to decline if it has a sympatric host species (reservoir species). Second, the mathematical models assume the disease primarily increases host mortality. If the disease decreases fecundity, then diseases at high prevalence may have a significant impact on host populations without causing increased deaths (McCallum 1994); DDT had such effects (Enderson and Berger 1970). Similar generalizations have been drawn from models of helminth and other macroparasitic infections (Anderson 1980).

Where diseases affect hosts differentially, occurrence of sympatric populations of vertebrate hosts with a shared parasite can result in one host benefiting by a greater impact of the para­site on the other (Hudson and Greenman 1998).

However, it must be recognized that para­site infections or toxins are only one of several elements affecting host population numbers over time (Scott 1988). It often is difficult to clearly distinguish the specific role of diseases as decimating factors. It is even more difficult to document their roles as welfare factors in interactions with nutrition, stress, genetic prob­lems, predator-prey interactions, accidents, climate, or other ancillary factors.

Diseases may exert selective pressures on various social behaviors. For example, mat­ing behaviors, social avoidance, group size, and group isolation may have been affected by selection pressures to reduce transmission of pathogens (Loehle 1995).

A final, positive note is that while parasites can be detrimental to host fitness in one envi­ronment, they can be beneficial to it in another. There is some evidence that parasitized individuals may enjoy a selective advantage over unparasitized conspecific hosts in some circumstances (Thomas et al. 2000).