Wildlife Disease in U.S. National Parks: Historical and Coevolutionary Perspectives A. ALONSO AGUIRRE* College of Veterinary Medicine Oregon State University Corvallis, OR 97331, U.SA.

EDWARD E. STARKEY Cooperative Park Studies Unit College of Forestry Oregon State University Corvallis, OR 97331, U.SA.

Abstract: Diseases o f wildlife have significant management implications in a number o f lands o f the U.£ National Park Service due to increasing interactions between wildlife and domestic animals. We review the paleontology, history, and coevolution o f infectious diseases in North American ungulate,g We provide two examples related to bovine brucellosis in bison in Yellowstone National Park and lungworm-pneumonia complex in bighorn sheep in several western national park£ These examples illustrate the difficulty o f numaging wild populations and their diseases in national parks and other protected areag In some instances, h u m a n intervention may be justifiable in order to protect native population~ domestic a n t m a ~ and h u m a n s from acquiring a disease

*Present addres~ Wildlife Laboratotqe~ Irm, P.O. Box 1522, Fort CoHin~ CO 80522, U.£A Paper subrattted August 31, 1993; revised manuscript accepted February 14, 1994.

654 ConservationBiology,Pages 654-661 Volume8, No. 3, September 1994

Enfermedades de la vida silvestre en los Parques Nacionales de EEUU: Perspectivas hist6ricas y coevolutivas R e s u m e n : Las enfermedades de f a u n a silvestre tlenen tmpticaciones de manejo stgniflcativas en diferentes dreas protegidas p o t el Servicio Nacional de Parques de los Estados Unldo~ debldo al aumento de las interacciones entre ganado dor~stico y ungulados silvestre~ En este articulo re. visamos la paleontologttg histori~ y evoluci6n de las enfer. medades infecciosas en ungulados norteamericanos. Se provee y como eJemplo dos casos relactonados a la brucelosis bovina en bisonte americano en el Parque Nactonal de Yellowstone y al complejo de nemdtodos p u l m o n a r e s p n e u m o n i a bacteriana que afecta al borrego cimarr6n en diferentes parques nacionales del oeste de los Estados Unido& Estos ejemplos ilustran las diflcultades de manejar poblactones silvestres y sus enfermedades en parques nacionales y otras dreas protegida~ En algunas tnstancia~ se justificaria la intervenci6n h u m a n a para proteger de la adquisici6n de enfermedades a poblaciones nativas de faurug animales dorndstico~ y humano~

Aguirre & Starkey

Introduction Wildlife diseases represent significant management concerns in a n u m b e r of lands of the U.S. National Park Service (NPS) due to increasing interactions between wildlife and domestic animals. Although the NPS M a n a g e m e n t Policies (NPS 1988) serves as the primary guide for all servicewide policy issues, diseases are briefly described under the policy of "native" or "exotic" to park ecosystems: "The native animal life is defined as all animal species [including pathogenic organisms] that as a result of natural processes o c c u r or occurred on lands n o w designated as parks. Any species that have m o v e d onto park lands directly or indirectly as the result of human activities are not considered native" (NPS 1988:4-5). Diseases are categorized under the pest management policy, which specifies that pests are animal or plant populations that interfere with the purposes of the park. Strategies for managing pest populations are to be influenced by w h e t h e r the pest is an exotic or native species. In most cases, however, no substantiated evidence exists to classify viral, bacterial, and parasitic animal diseases in this manner in the National Park System. Circumstantial evidence is supported in limited cases by DNA technology, paleopathology of bones and preserved tissues, and historic accounts of the movement and distribution of diseases during epidemic situations. The following review of the paleontology, history, and coevolution of selected infectious diseases in North American ungulates should increase the awareness of biologists, veterinarians, and conservationists of the origin and m o v e m e n t of diseases on this continent. Also, this article identifies the need for a better understanding of wildiife ecology and management fields as they relate to epidemiology and population medicine.

Historical Perspective Many of today's animal diseases have a history of millions of years. Paleopathologic findings of disease conditions among fossil animals provide evidence of the geographic and evolutionary origin of infectious agents. Recent studies have demonstrated the presence of prePleistocene fossil microorganisms in vertebrates (Brothwell & Sandison 1967; Luff 1984). It is difficult, however, to determine w h e t h e r bacteria or fungi present in a fossil are antemortem or postmortem. Undoubtedly, bacterial and viral diseases w e r e present in early mammals, but few microorganisms left evidence on animal bones, mummified specimens, or animals preserved by desiccation or immersion. Written records, the only remaining source of information, are more recent and frequently puzzling to interpret (Hare 1967). The origin of parasitism during the early Paleozoic has

WildlifeDiseasein U.S.N~onal Parks

655

been reviewed by Clarke (1908). No lesions due to accident or infection have been described among vertebrates prior to the Carboniferous period. Parasitism of animals during that period could be p r e c e d e d by commensalism or partial parasitism (Haldane 1949). According to Moodie (1967), disease progressed during the geologic history of the earth. Cases such as caries, osteoperiostitis, necroses, hyperostoses, fractures and many infective processes first appeared during the Cretaceous, and they w e r e highly prominent among the dinosaurs, mosasaurs, plesiosaurs, crocodiles, and turties. Diseases affecting dinosaurs may have contributed to their extinction and may have b e c o m e extinct with them (Bakker 1986). The mammals of the early Cenozoic acquired certain diseases from preceding forms, such as caries and other primitive diseases. Evidence of disease in mammals is more prevalent during the late Cenozoic, increasing considerably during the Quaternary. Common fossil pathologic lesions include caries, "lumpy jaw," fistulae, and pyorrhea alveolaris in threetoed horses during the early Tertiary in North America (Moodie 1967); deforming arthritides in a Pleistocene giant wolf in California (Moodie 1967); osteomyelitis in reindeer; traumatic exostoses and osteomalacia in an early carnivore from the Washakie Eocene in Wyoming, 70 million years ago; and rickets (Moodie 1967). Necroses due to M y c o b a c t e r i u m are commonly reported in fossil vertebrates (Baker & Brothwell 1980). Webster ( 1 7 9 9 ) d o c u m e n t e d significant human and animal dieoffs in one of the earliest and best sources of historical information on infectious diseases in America. This publication was followed by the classic book by Fleming ( 1 8 7 1 ) on animal epizootics. Later, Fleming ( 1 8 8 2 ) w r o t e a second volume outlining a chronologic synopsis of diseases arranged according to species from B.C. 2048 to A.D. 1844. These works include primarily diseases of domestic animals and give an extensive historical review of the introduction of livestock diseases in North America. Bierer ( 1 9 7 4 ) offers an excellent compilation of animal disease reports in America for the period from 1656 to 1939. The earliest wildlife disease in the Americas occurred in Peru during 1544. Wild and domesticated alpacas ( L a m a p a c o s ) were dying in great numbers from a cutaneous disease (Fleming 1871). Diseases reported during the late 1700s include severe and widespread rabies epizoodemics in wild foxes and dogs ( 1 7 6 9 ) and distemper in dogs and cats (1796). Anthrax was a c o m m o n disease in humans and animals, with extensive outbreaks reported in the West Indies during 1770 (Fleming 1871). Reports of disease in wild animals became more evident in the literature w h e n w e learned of their potential threat to humans and the livestock industry. An example was the last outbreak of foot-and-mouth disease in California (1924). The disease first appeared in swine that were fed garbage from Asian ships that

Conservation Biology Volume 8, No. 3, Y~ptember 1994

656

WildlifeDiseasein U.S.NationalParks

docked in San Francisco harbor. The difficulty in eliminating this outbreak was increased by the presence of the disease in wild deer in the Stanislaus National Forest. An interagency effort and the killitlg of 22,000 deer resulted in the complete eradication of foot-and-mouth disease in the United States in 1925 (Davis et al. 1981).

Coevohtionary Perspective Most placental mammals originated in Europe and Asia in the early Cenozoic Era, more than 70 million years B.C. The adaptive radiation of ungulates c o m m e n c e d in the Eocene, diverging to p r o d u c e the contemporary Perissodactyla and Artiodactyla. Most of the large North American mammals migrated through the Bering Strait, as demonstrated by fossil records. Migration took place during the Miocene and Pliocene (10 million years B.C.) and the Pleistocene (1.5 million years B.C.). Exceptions to these massive migrations are the horse, the peccary ( Tayassu tajacu ), the pronghorn antelope (Antilocapra americana), and the musk ox (Ovibos moschatus). The Equidae w e r e distributed in b o t h North and South America and became extinct during the Pleistocene. Peccary and p r o n g h o r n originated and remained in North America. Musk ox originated in North America, migrated to Asia, t h e n r e t u r n e d to North America (Gilbert 1978; Eisenberg 1981). The Miocene bovid and cervid evolutionary history represents an adaptive response of medium-sized herbivores to the expansion and increasing availability of vegetation resulting from the cooling and drying of large terrestrial habitats. The diversity of these habitats provided opportunity for the local speciation of ungulates (Gilbert 1978; Eisenberg 1981, 1987). During this period, infectious agents and parasites could have evolved with the dispersal of ungulates. The vegetation patterns and environmental changes occurring during the Pleistocene resulted in different populations of hosts and parasites being exposed to a variety of habitats that differentially adapted them to specific selection regimes. Among ungulate radiations (early separations of various phyletic lines), Bovidae represent the most successful recent adaptation to open habitats by large terrestrial herbivores (Eisenberg 1981 ). Parasitism acted as one of the selective forces in bovid evolution. A balanced condition persisted between host and parasite involving a series of adaptations c o n c e r n e d primarily with the chances of infection, parasite virulence, and host resistance (Zuckerman & Weiss 1973).

Adaptive Radiation and Niche The concept of niche relates to the evolution, adaptations, and limitations of a species. Ecologists use two definitions of niche, one emphasizing animal functions and the other emphasizing habitat resources (Bailey

Conservation Biology Volume 8, No. 3, September 1994

Aguirre& Starkey 1984). The second allows the concept of empty niche. Habitat resources may be available but unused because of the extinction or extirpation of a species or because evolution has not created the appropriate species to use those resources. Each species is adapted to a narrow range of resources; for example, three species of metastrongyloid nematodes are found within distinct niches in mink lung tissue, localized in alveolar ducts and terminal bronchioles, in peribronchial connective tissue, and bronchi. Parasite competition would be unlikely due to the presence of three empty niches: alveoli, lamina propria of the bronchial bifurcation, and pulmonary arteries (Price 1980). Epidemiologic interference is a term used to exemplify the niche concept in parasite evolution. It prevents massive, multiple, and fatal infections of young hosts, affecting the time of disease o c c u r r e n c e and altering the rate of natural immunization. An epidemic caused by a virus can suppress epidemics caused by other similar agents (Halpin 1975; Thrusfield 1986). Epizootics of pasteurellosis in bighorn sheep (Ovis canadensis) are commonly associated with respiratory viruses such as bovine syncytial respiratory virus or parainfluenza-3 virus. One respiratory virus may prevent infection with the other.

Genetic Coevolution Parasites induce specific reactions and changes in physiology, immunity, and host behavior (Anderson 1978; Anderson & May 1979; Lewis 1981). The host uses these changes to counteract the parasite attack. Actions of parasites on populations select for individuals with increased resistance to the parasite invasion. For this reason the pathogenicity of the parasite will tend to decrease through evolutionary time ( T h o m p s o n 1982; May 1985). Eventually, the host population may escape from the parasite infection (Anderson & May 1982). Concurrent evolution and selection of parasites in developing hosts lead to parasite speciation (Anderson 1982). For example, the genus Parelapbostron~lus is known only from North America, but it has systematic and biological similarities to Elapbostron~lus of Eurasian cervlds (Anderson & Prestwood 1971 ).

Host Specificity Parasites are host-specific in most cases as a consequence of evolutionary processes (Manter's Rule: the closer the life histories of parasite and host the m o r e specific is the parasite) (Parsons 1983). Cross infections may occur, however, in animals sharing part of their habitat or food resources. Where diversity is high, cross infections are high, keeping realized niches m u c h smaller than potential niches, amplifying spatial segregation, and causing distributional gaps between parasite species. One possible explanation for these gaps may be

Agu/rre & ~arkey that infectious agents are maintained by the capacity of the vectors or predators that travel b e t w e e n populations carrying a parasite highly pathogenic to one host but innocuous to another (Canning & Wright 1972; Clarke 1976; Nickol 1979). In North America, Franctsella tularensts is maintained primarily by a wild rabb i t - w o o d tick cycle, but a wide range of other mammal and arthropod species may b e c o m e peripherally involved as hosts and vectors of the organism (Quan 1993). Natural Selection and Competition Endemic diseases may function as vehicles of natural selection. For example, Darwin noted in Paraguay that feral horses, cattle, and dogs w e r e susceptible to umbilical myiasis. The susceptibility to this endemic disease kept animal densities low (Whitlock 1977). Parasites may be used as ' ~ e a p o n s of competition" (May & Anderson 1979). Parelaphostrongylus tenuis is highly pathogenic to moose (Alces alces), causing severe neur o l o g i c disease ( K a r n s 1 9 6 7 ) . W h i t e - t a i l e d d e e r ( Odocoileus virginianus ) are considered normal hosts and are resistant to the infection. Deer contacts with m o o s e w e r e devastating as n o r t h e r n forests w e r e cleared. Woodland caribou (Rangifer tarandus) and wapiti (Cervus elaphus) have also been restricted and replaced in some parts of their range by the parasite (Anderson 1971). Reintroductions of these species into ranges now occupied by white-tailed deer have failed and are practically impossible (Kelsall & Prescott 1971; Saunders 1973). The differential pathogenicity of P. tenuis makes white-tailed deer a p o t e n t c o m p e t i t o r (Anderson 1972). Mule deer (Odocoileus hemionus) in the western and southwestern United States are infected with Elaeophora schneider~ a nematode inhabiting the carotid arteries. Mule deer are resistant to pathogenic effects, but in abnormal hosts such as wapiti, moose, domestic goats, and sheep the microfilarial stage dies, causing blindness and brain damage. The parasite is transmitted by horseflies of the genera Tabanus and Hybomithra (Thorne et al. 1982). Parasites also may influence the temporal and spatial population dynamics of the host (Kemper 1982). Protostrongylus stilesi and P. rushi are parasitic lungworms predisposing bighorn sheep to secondary bacterial and/ or viral pneumonia. The lungworm-pneumonia complex is considered the most important mortality factor of Rocky Mountain bighorn sheep. It has decimated pop. ulations t h r o u g h o u t their historic geographic range, causing radical shifts in distribution (Forrester 1971). Parasites may influence community structure, producing long-term changes by modifying predator-prey interactions. The more parasitized individuals are more susceptible to predation (Anderson 1979). Intraspecific

W'dd//feD/seaseill U.S Nat/ona/Parks

657

competition may be strongly influenced by parasitism. Highly parasitized individuals are often inferior competitors, occupy less favorable habitats, have an inferior social status, and demonstrate an inability to establish territories (Davies 1978; Holmes 1982).

Commensalistic Interactions Persistence of host-parasite interactions may lead to increased resistance by the host and the attenuation of the parasite, directing the pattern from virulence to commensalism. The parasite may remain virulent and maintain a stable association with a sensitive host for long periods of time (Gillespie 1975). Commensalism is known to occur in some infections of ruminants. In Africa, wild ungulates contract mild Trypanosoma infections with high morbidity in endemic areas. The parasitemias are sufficiently high for parasites to be ingested by vectors maintaining the cycle under natural conditions. Domestic ruminants that have lived there for centuries present a more severe disease with high morbidity and low mortality, but sufficient cattle survive to perpetuate the parasite. Exotic livestock are highly susceptible, presenting fatal infections (Murray et al. 1979). Because the same parasite p r o d u c e s these graded responses, the differences depend on the host response. Selection for host resistance has been more effective in native wildlife living in enzootic areas for a long time. Selection also has p r o d u c e d some resistance in indigenous cattle that have been exposed to the parasite, but animals from non-enzootic areas are highly susceptible. Coevolution does not necessarily exclude the persistence of stable associations b e t w e e n virulent parasites and their hosts. A classic example is rabbit myxomatosis (Fenner & Ratcliff 1965). The m y x o m a virus is a highly pathogenic disease of domestic European rabbits (Oryctolagus cuniculus), producing a benign localized fibroma in its natural host, the wild tapeti (Sylvilagus brasiliensis). The disease is mechanically transmitted by a vector. Rabbits w e r e introduced in 1859 and became a pest of major significance in Australia. The virus was successfully introduced during 1950 to control the rabbit populations. Myxomatosis caused 99% mortality on initial release, spreading rapidly during s u m m e r months w h e n mosquito populations w e r e abundant. It was predicted that the disease would disappear after each summer due to the absence of susceptible hosts, lowered transmission rates, and lack of vectors. The virus, however, had the capacity to survive throughout the winter, conferring a great selective advantage on viral mutants able to cause a less lethal disease. Such mutants appeared within the first year and became dominant in 3 to 4 years. Rabbits recovering from the disease are immune, which suggests that selection for genetically more resistant animals should rapidly occur. Ap-

Conservation Biology Volume 8, No. 3, September 1994

658

WildlifeDiseasein U.S. NaHonalParks

parently a stable virus-host association was established and has persisted for m o r e than 30 years, and virions of intermediate virulence evolved, eventually b e c o m i n g the dominant type (Parsons 1983). Genetically, the original, highly lethal virus has b e e n replaced by a h e t e r o g e n o u s collection of strains of lower virulence. The case of myxomatosis (and trypanosomiasis) illustrates that a virulent microparasite can persist in hosts with long generation times. These examples may provide evidence that commensalism is not necessarily the o u t c o m e of coevolution, although it does not e x c l u d e the possibility of c o m m e n s a l i s m evolving from virulence. The disease response may be due to selection for r e d u c e d sensitivity in the host rather than selection for avirulence in the parasite (Alexander 1981; Allison 1982). Another example of reduced sensitivity of the host related to resistance with a genetic basis is shown in some studies of sylvatic plague. During outbreak situations, wild rats from cities with a recent history of plague have higher survival rates than rats with no recent exposure to the disease (Levin 1983). Decreased virulence could reduce the rate of parasite transmission to the intermediate host; for example, the virulence of s o m e arboviruses increases w h e n they are directly transmitted to the host. Vectors and reservoir hosts tend to distribute disease p r o b l e m s evenly over the entire species range (Ewald 1983). Ancient diseases such as anthrax and rabies are examples of extremely virulent diseases that remain highly virulent rather than evolving toward mutualism (Peterson 1991).

Exotic or Native Diseases in National Parks: Two Examples

Aguirre & S~arlcey

infections in animals and presented mutational changes adapting to other s p e c i e s such as B. a b o r t u s (Meyer 1976b). No substantial evidence exists, however, to account for the diversity of characteristics or parentage in Brucella spp. Brucella abortus biovars 1, 2, and 4 are found in bison (Bos bison) and wapiti. These isolates are phenotypically identical to the ones isolated from cattle ( N I ~ & APHIS 1989). Besides DNA fingerprinting technology or bacterial isolations from prehistoric animal tissues, there are no feasible methods to p r o v e the origin of bovine brucellosis. Historical evidence and recent DNA serotyping, however, indicate that the disease is exotic and was introduced from Europe w h e n the Spanish brought infected cattle during the 1500s (Bierer 1974). Brucella abortus biovars 1 and 2 w e r e isolated from 11 out of 72 bison sampled in W o o d Buffalo National Park, Canada. No strains could be considered unique to bison. Biovar 2 has b e e n rarely isolated in North America; thus, this could be a useful epidemiologic marker to trace brucellosis infections. The p r e s e n c e of different biovars in wapiti and bison in the Greater Yellowstone Ecosystem suggests that these species have b e e n historically exposed to m o r e than one source of infection (Tessaro et al. 1990). C o m p u t e r analysis of DNA w e r e p e r f o r m e d to determine the origin of B. a b o r t u ~ The probability of mutational changes occurring in evolutionary time and the lack of genetic differences a m o n g B. a b o r t u s biovar 1 isolated from bison, wapiti, and cattle w e r e considered (NPS & APHIS 1989). It was suggested that bovine brucellosis biovar 1 is exotic to North America, but additional research is needed on the phylogeny and evolution of Bovidae and Brucellae.

Bovine Brucellosis in the Greater Yellowstone Ecosystem

Lungworm-Pneumonia Complex in Bighorn Sheep

The determination of Brucella abortus as native or exotic to North American ungulates has b e e n an important issue addressed by several state and federal agencies (NPS & Animal & Plant Health I n s p e c t i o n Service [APHIS] 1989). I f a disease is found to be native to a park ecosystem, it should be p r o t e c t e d except w h e n its control is r e c o m m e n d e d (NPS 1988). The identification of the origin of Brucella is necessary in epidemiologic research, which depends on the classification of a bacterial species into biotypes, serotypes, or biovars. These biovars constitute epidemiologic markers providing information on the o c c u r r e n c e of the disease and the origin of infections (Arnaud-Bosq & Roux 1985). Meyer ( 1 9 7 6 a ) summarized the evolution and t a x o n o m y of the genus B r u c e l l g suggesting that two species may have c o m m o n ancestors and can mutate from one species to another in laboratory conditions. Extensive research in the former Soviet Union concluded that B. melitensis is the main ancestor for other brucellosis

Fish and game agencies have applied intensive managem e n t techniques ranging from habitat manipulation and population control to range extension and winter feeding and parasite control programs to mitigate bighorn mortality due to lungworm-pneumonia complex. Bigh o r n populations, h o w e v e r , c o n t i n u e to decline in m u c h of their range (Uhazy et al. 1973). Mortality resulting from bacterial b r o n c h o p n e u m o n i a is apparently limiting the relative a b u n d a n c e o f b i g h o r n s h e e p t h r o u g h o u t N o r t h A m e r i c a ( F o r r e s t e r 1971). Protostrongylosis may contribute to onset and increase the severity of pneumonia, but it is not an essential component in the pathogenesis of the p n e u m o n i a c o m p l e x (Spraker et al. 1984). Acute epizootics are characterized by outbreaks affecting all the age cohorts in a population and reducing animal numbers drastically. Spraker et al. ( 1 9 8 4 ) referred to these occurrences as "all-age dieoffs" and "spontaneous s u m m e r lamb mortality" involving Pasteurella spp. as the primary pathogenic bacteria.

Conservation Biology Volume 8, No. 3, September 1994

Aguirre & ~ k e y The issue of "exotic" versus "native" related to lungworm-pneumonia complex is complicated because Protostrongylus rushi and P. sttlesi are considered native to North America and unique to bighorn sheep. On the other hand, some strains of Pasteurella spp. are considered exotic. Pasteurella m u l t o c i d a is primarily involved with fatal pneumonia in domestic sheep. Betah e m o l y t i c P. h a e m o l y t i c a b i o t y p e s T and A w e r e introduced by domestic sheep and cattle. Pasteurella h a e m o l y t i c a and P. m u l t o c t d a have been recovered from bighorn sheep. Complicating the scenario, bighorns are carriers of nonhemolytic P. h a e m o l y t i c a biotype T, apparently a unique and endemic strain affecting bighorn sheep in North America. This biotype has been associated with several stress-related dieoffs but does not affect domestic sheep. The bighorn strain causes necrotizing bronchopneumonia, whereas both domestic livestock strains cause fatal septicemia and fibrinous b r o n c h o p n e u m o n i a (Spraker et al. 1984; Onderka et al. 1988; Callan et al. 1991). Because different biotypes have been identified in both domestic and wild sheep, it is reasonable to conclude that lungworm-pneumonia complex in bighorn sheep has both native and exotic factors that are required for the disease to be expressed. Even if one were to take the more narrow definition of exotic to mean a disease originating outside park boundaries, this disease complex w o u l d qualify as both native and exotic. The examples of bovine brucellosis in bison and the lungworm-pneumonia complex in bighorn sheep illustrate the difficulty of managing wild populations and their diseases in National Parks based solely on the classification as exotic or native as described in the NPS Management Policies. In most cases, diseases in wildlife species in national parks are both native and exotic because diseases are manifested through imbalances of resistance that are held in equilibrium by factors inherent to the host, the agent, and the environment. These factors will nearly always be a combination of e x o t i c - resulting from human intervention, for e x a m p l e - - a n d native. Given these arguments, intervention may be justifiable and p r o p e r in order to protect native populations, domestic animals, and humans from acquiring a disease within the park boundaries. The circumstances involved in each case must be considered. Controlling the spread of diseases to lands or populations outside the park boundaries also may be justified under these definitions. Control programs within or throughout national parks should be well documented, coordinated, and understood prior to implementation.

Acknowledgments This research was partially funded through Cooperative Agreement No. C A - 9 0 0 0 - 8 - O ( O 6 , Subagreement No.

WildlifeDiseasein U.£ N~lonal Parks

659

20, ~ o m the Pacific Northwest Regional Office of the National Park Service. J. 17, Behnke, D. E. Hansen, and B. Z i m m e r m a n are gratefully a c k n o w l e d g e d for their thoughtful reviews in previous drafts of this manuscript.

Hteratere Cited Alexander, M. 1981. Why microbial predators and parasites do not eliminate their prey and hosts. Annual Review of Microbiology 35:113-133. Allison, A. C. 1982. Co-evolution between hosts and infectious disease agents and its effects on virulence. Pages 245-267 in 1ZM. Anderson and P~M. May, editors. Population biology of infectious diseases. Springer-Verlag, New York Anderson, 1~ C. 1971. Neurologic disease in reindeer (Rangifer tarandus tarandus) introduced into Ontario. Canadian Journal of Zoology 49:159-166. Anderson, R.C. 1972. The ecological relationships of meningeal worm and native cervids in North America. Journal of Wildlife Diseases 8:304-310. Anderson, R.C. 1978. The regulation of host population growth by parasitic species. Parasitology 76:119-157. Anderson, R.C. 1979. The influence of parasitic infection on the dynamics of host population growth. Pages 245-281 in IZ M. Anderson, B. D. Turner, and L. 1~ Taylor, editors. Population dynamics. Blackwell, Oxford, England. Anderson, IZ C., and A. IC Prestwood. 1971. Lungworms. Pages 81-126 in J.W. Davis and R.C. Anderson, editors. Parasitic diseases of wild mammals. Iowa State University Press, Ames, Iowa. Anderson, R. M. 1982. Coevolution of hosts and parasites. Parasitology 85:411-426. Anderson, P~M., and IZ M. May. 1979. Population biology of infectious diseases. I. Nature 280:361-367. Anderson, R.M., and 17,M. May. 1982. Population biology of infectious diseases. Springer-Verlag, New York Arnaud-Bosq, C., and J. Roux. 1985. General mathematical methodology for analyzing biotope-biotype correspondences of bacteria application to the epidemiology of Brucella melttensts in France. Bulletin World Health Organization 63:1079-1088. Bailey, J.A. 1984. Principles of wildlife management. John Wiley & Sons, New York Baker, J., and D. Brothwell. 1980. Animal diseases in archaeology. Academic Press, New York. Bakker, R.T. 1986. The Dinosaur heresies: New theories unlocking the mystery of the dinosaurs and their extinction. William Marrow and Co., New York Bierer, B.W. 1974. History of animal plagues of North America: With occasional reference to other diseases and diseased conditions. U.S. Department of Agriculture, Washington, D.C.

Conservation Biology . Volume 8, No. 3, September 1994

660

Wddli[eDisease in U.S. National Parks

Brothweli, D., and A. T. Sandison. 1967. Diseases in antiquity: A survey of the diseases, injuries and surgery of early populations. Charles C. Thomas, Springfield, Illinois. Callan R.J., T.D. Bunch, G.W. Workman, and R.E. Mock. 1991. Development of pneumonia in desert bighorn sheep after exposure to a flock of exotic wild and domestic sheep. Journal of the American Veterinary Medical Association 198:1052-1056. Canning, E. U., and C. A. Wright. 1972. Behavioural aspects of parasite transmission. Academic Press, London, England.

A.suirre & Starkey

Haldane, J. B. S. 1949. Disease and evolution. LaRicerca Scientifica Supplement 19:68-76. Halpin, B. 1975. Patterns of animal disease. Williams & Wilkins Company, Baltimore, Maryland. Hare, R. 1967. The antiquity of diseases caused by bacteria and viruses: A review of the problem from a bacteriologist's point of view. Pages 11 5-131 in D. Brothweil and A.T. Sandison, editors. Diseases in antiquity: A survey of the diseases, injuries and surgery of early populations. Charles C. Thomas, Springfield, Illinois.

Clarke, B.C. 1976. The ecological genetics of host-parasite relationships. Pages 8 7 - 1 0 4 in A.E. IZ Taylor and R. MuUer, editors. Genetic aspects of host-parasite relationships. Symposia of the British Society of Parasitology, vol. 14. BlacJcweli, London, England.

Hoimes, J. c. 1982. Impact of infectious disease agents on the population growth and geographical distribution of animals. Pages 35-51 in R. M. Anderson and R. M. May, editors. Population biology of infectious disease. Springer-Verlag, New York.

Clarke, J. M. 1908. The beginnings of dependent life. 4th Annual Report. Director of Science Division, New York State Education Department, New York.

Karns, P. D. 1967. Pneumostrongylus tenuis in deer in Minnesota and implications for moose. Journal of Wildlife Management 31:299-303.

Davies, N.B. 1978. Ecological questions about territorial behaviour. Pages 317-350 inJ. R. Krebs and N. B. Davies, editors. Behavioural ecology: An evolutionary approach. Blackwell, Oxford, England.

Kelsali, J. P., and W. Prescott. 1971. Moose and deer behavior in snow in Fundy National Park, New Brunswick. Canadian Wildlife Service Report Series No. 5. Information Canada, Ottawa, Ontario, Canada.

Davis, J.W., L. Karstad, and D.O. Trainer. 1981. Infectious diseases of wild mammals, 2nd edition. Iowa State University Press, Ames, Iow&

Kemper, J. T. 1982. The evolutionary effect of endemic infectious disease: Continuous models for an invariant pathogen. Journal of Mathematical Biology 15:65-77.

Eisenberg, J. F. 1981. The Mammalian radiations: An analysis of trends in evolution, adaptation, and behavior. The University of Chicago Press, Chicago, Illinois.

Levin, S.A. 1983. Some approaches to the modeling of coevolutionary interactions. Pages 2 1 - 6 6 in M.H. Nitecki, editor. Coevolution. University of Chicago Press, Chicago, Illinois.

Eisenberg, J. F. 1987. The evolutionary history of the Cervidae with special reference to the South American radiation. Pages 60--64 in C. M. Wemmer, editor. Biology and management of the Cervidae. Smithsonian Institution Press, Washington, D.C.

Lewis, J. W. 1981. On the coevolution of pathogen and host. I. General theory of discrete time coevolution. Journal of Theoretical Biology 93:927-951.

Ewald, P.W. 1983. Host-parasite relations, vectors, and the evolution of disease severity. Annual Review of Ecology and Systematics 14:465--485. Fenner, F., and F.N. Ratcliff. 1965. Myxomatosis. Cambridge University Press, Cambridge, England. Fleming, G. 1871. Animal plagues: Their history, nature, and prevention, vol. I. Chapman & Hall, London, England. Fleming, G. 1882. Animal plagues: Their history, nature, and prevention, vol. II (A.D. 1800-1844). Balliere, Tindall and Cox, Paris, France. Forrester, D.J. 1971. Bighorn sheep lungworm-pneumonia complex. Pages 158-173 in J.W. Davis and 1Z C. Anderson, editors. Parasitic diseases of wild mammals. Iowa State University Press, Ames, Iowa. Gilbert, D.L. 1978. Evolution and taxonomy. Pages 1-11 in J. L Schmith and D. L Gilbert, editors. Big game of North America: Ecology and management. Stackpole Books, Harrisburg, Pennsylvani~ Gillespie, J.H. 1975. Natural selection for resistance to epidemics. Ecology 56:493-495.

Conservation Biology Volume 8, No. 3, September 1994

Luff, R.-M. 1984. Animal remains in archaeology. Shire Publications, Aylesbury, England. May, 17, M. 1985. Host-parasite associations: Their population biology and population genetics. Pages 243-361 in D. Rollinson and R. M. Anderson, editors. Ecology and genetics of hostparasite interactions. Linnean Society of London, Academic Press, Londoti, England. May, R~M., and R~M. Anderson. 1979. Population biology of infections diseases: Part II. Nature 280:455-461. Meyer M. E. 1976at Evolution and taxonomy in the genus Brucelia. Concepts on the origins of the contemporary species. American Journal of Veterinary Research 37:199-202. Meyer M. E. 1976b. Evolution and taxonomy in the genus Brucell~" Contemporary evolutionary status of the species Brucelia abortus. American Journal of Veterinary Research 37:203-205. Moodie, IZ L. 1967. General considerations of the evidences of pathological conditions found among fo~il animal& Pages 31-46 in D. Brothwell and A. T. Sandison editors. Diseases in antiquity: A survey of the diseases, injuries and surgery of early populations. Charles C. Thomas, Springfield, Illinois.

Aguirre & Starkey Murray M., W.I. Morrison, and P. IC Murray. 1979. Trypanotolerance---a review. Wild Animal Review 31:2-12. National Park Service. 1988. Management policies. National Park Service, U.S. Department of Interior, Washington, D.C.

Wildlife Diseasein U.S. N~ional Parks

661

Spraker T. IL, C. P. Hibler, G. G. Schoonveld, and W. S. Adney. 1984. Pathologic changes and microorganisms found in bighorn sheep during a stress-related die-off. Journal of Wildlife Diseases 20:319-327.

National Park Service and Animal & Plant Health Inspection Service. 1989. Workshop on brucellosis in the Greater Yellowstone Area executive summary. Washington, D.C.

Tessaro, S.V., L B. Forbes, and C. Turcotte. 1990. A survey of brucellosis and tuberculosis in bison in and around W o o d Buffalo National Park, Canada. Canadian Veterinary Journal 31:174-180.

Nickol, B.B. 1979. Host-parasite interfaces. Academic Press, New York.

Thompson, J.N. 1982. Interaction and coevolution. John Wiley & Sons, New York.

Onderka, D. IC, S.A. Rawluk, and W. D. Wishart. 1988. Susceptibility of Rocky Mountain bighorn sheep and domestic sheep to pneumonia induced by bighorn and domestic livestock strains of Pasteurella haemolyticg Canadian Journal of Veterinary Research 52:439-444.

Thome E.T., N. Kingston, W. R. JoUey, and 1L C. Bergstrom. 1982. Diseases of wildlife in Wyoming, 2nd edition. Wyoming Game and Fish Department, Cheyenne, Wyoming.

Parsons, P.A. 1983. The evolutionary biology of colonizing species. Cambridge University Press, New York. Peterson M.J. 1991. The Wildlife Society publications are appropriate outlets for the results of host-parasite interaction studies. Wildlife Society Bulletin 19:360-369. Price, P. W. 1980. Evolutionary biology of parasites. Princeton University Press, New Jersey. Quan, T.J. 1993. Plague and tularemia in rodent populations. Pages 5 4 - 5 6 in M. E. Fowler, editor. Zoo & wild animal medicine: Current therapy 3. W.B. Saunders, Philadelphia, Pennsylvania. Saunders, B. F. 1973. Meningeal w o r m in white-tailed deer in northwestern Ontario and moose population densities. Journal of Wildlife Management 37:327-330.

Thrusfield, M. 1986. Veterinary epidemiology. Butterworths, Boston, Massachusetts. Uhazy, L. S.,J. C. Holmes, andJ. G. Stelfox. 1973. Lungworms in the Rocky Mountain bighorn sheep of western Canada. Canadian Journal of Zoology 51:817-824. Webster, N. 1799. A brief history of epidemic and pestilential diseases: With the principal phenomena of the physical world, which precede and accompany them, and observations deduced from the facts stated. 2 vols. Hudson & Goodwin, New York. Whitlock, J. H. 1977. The population biology of disease. Corn e r University, Ithaca, New York. Zuckerman, A., and D.W. Weiss, editors. 1973. Dynamic aspects of host-parasite relationships, vol. 1. Academic Press, New York.

ComervationBiology Volume 8, No. 3, September 1994