S CIENCE’ S C OMPASS ● REVIEW

REVIEW: WILDLIFE Emerging Infectious of Wildlife— Threats to and Human Health Peter Daszak,1, 2* Andrew A. Cunningham,3 Alex D. Hyatt4

species (7), increasing veterinary involvement Emerging infectious diseases (EIDs) of free-living wild can be classified into (8, 9), and advances in -parasite population three major groups on the basis of key epizootiological criteria: (i) EIDs associated (4, 10), the threat of wildlife diseases is with “spill-over” from domestic animals to wildlife populations living in proximity; (ii) now taken more seriously (11–13). EIDs related directly to human intervention, via host or parasite translocations; and (iii) EIDs with no overt human or domestic involvement. These phenomena Common Causal Themes have two major biological implications: first, many wildlife species are reservoirs of The increasing number of wildlife EIDs may that threaten domestic animal and human health; second, wildlife EIDs reflect increasing vigilance, but parallels be- pose a substantial threat to the conservation of global biodiversity. tween causal factors driving the emergence of human and wildlife EIDs suggest that this trend is valid (14)(Fig.1).Diseaseemergencemost he past two decades have seen the highly pathogenic morbillivirus , en- frequently results from a change in ecology of emergence of pathogenic infectious zootic to Asia, was introduced into Africa in host, , or both (15). Human population T diseases, such as acquired immunode- 1889. The panzootic front traveled 5000 km expansion has driven the emergence of EIDs ficiency syndrome, multidrug-resistant tuber- in 10 years, reaching the Cape of Good Hope via increasing population density, especially in culosis, and tick-borne diseases, which rep- by 1897, extirpating more than 90% of Ken- urban areas (dengue, ), and encroach- resent a substantial global threat to human ya’s buffalo population and causing second- ment into wildlife (Ross River health (1). Emergence is associated with a ary effects on predator populations and local disease) (2, 16). This encroachment may have on September 1, 2008 range of underlying causal factors (1, 2). extinctions of the . Populations of been a key factor in Africa for the global emer- These include interactions with zoonotic some species remain depleted and the persis- gence of Marburg and and human pathogens within a host-parasite continuum tence of rinderpest in eastern Africa contin- immunodeficiency virus (HIV) (2, 17). Pres- between wildlife, domestic animal, and hu- ues to threaten bovid populations. sures of human encroachment on shrinking man populations (Fig. 1). In this review, we of cholera, , and oth- wildlife habitat also cause increased wildlife identify a number of EIDs that predominantly er diseases seriously impact human popula- population densities and the emergence of wild- involve wildlife [(3, 4), Table 1, and Web table tions. Such clear-cut panzootic outbreaks of life EIDs (11–13, 18). The international move- 1(5)]. We define wildlife EIDs by applying diseases in wildlife are probably rare events, ment of livestock and modern agricultural prac- criteria similar to those used to define human but a lack of awareness and reporting, partic- tices have led to EIDs such as rinderpest in www.sciencemag.org EIDs (1, 2)andcategorizethemaccordingto ularly during the earlier decades of European Africa and bovine spongiform encephalitis their specific characteristics that are “emerging” expansion, almost certainly belies their true (BSE) in Europe. Similar situations occur in or novel (Table 2) and to their epizootiology. extent. Historically, wildlife diseases have been wildlife populations managed either in situ or in considered important only when agriculture or captivity. The extent of in situ management Wildlife EID, Past and Present human health have been threatened. However, may be substantially underestimated. Recent Parallels between human and wildlife EIDs because of outbreaks of disease in endangered analysis (19)suggeststhat15,000tonsofpea- extend to early human colonization of the globe and the dissemination of exotic patho- Downloaded from gens. In the same way that Spanish conquis- Fig. 1. The host-parasite ecological tadors introduced and to continuum (here parasites include viruses and parasitic prokaryotes). the Americas, the movement of domestic and Most emerging diseases exist other animals during colonization introduced within a host and parasite contin- their own suite of pathogens. The African uum between wildlife, domestic rinderpest panzootic of the late 1880s and animal, and human populations. 1890s is a paradigm for the introduction, Few diseases affect exclusively any spread, and impact of virulent exotic patho- one group, and the complex rela- tions between host populations gens on wildlife populations (4, 6). This set the scene for disease emer- gence. Examples of EIDs that over-

1 lap these categories are canine dis- Institute of Ecology, University of , Athens, temper (domestic animals to wild- GA 30602, USA. 2Infectious Disease and Pathology Activity, Division of Viral and Rickettsial Diseases, life), (wildlife to hu- National Center for Infectious Diseases, Centers for mans), cat scratch fever (domestic Disease Control and Prevention, , GA 30333, animals to humans) and (all USA. 3Institute of Zoology, Zoological Society of Lon- three categories). Arrows denote don, Regent’s Park, London NW1 4RY, UK. 4Australian some of the key factors driving Animal Health Laboratory, CSIRO, Private Bag 24, disease emergence. Geelong, Victoria 3220, Australia. *To whom correspondence should be addressed. E- mail: [email protected]

www.sciencemag.org SCIENCE VOL 287 21 JANUARY 2000 443 S CIENCE’ S C OMPASS nuts are fed annually to United Kingdom gar- Anthropogenic global climate change is spill-over, underpins the emergence of a den birds. This form of provisioning has led to likely to cause major changes to the geographic range of wildlife EIDs. Spill-over is a partic- the emergence of by ty- range and of arthropod-borne infec- ular threat to endangered species, because the phimurium DT40 and 086: tious diseases. Expansion of presence of infected reservoir hosts can lower K61 in Britain and Mycoplasma gallisepticum geographical ranges has been proposed to ex- the pathogen’s threshold density and lead to in the United States. because of a high density plain the reemergence of and dengue in local (population) extinction (8, 9, 11). Pop- and diversity of birds at feeding stations (19). South America, central Africa, and Asia during ulations of the African wild dog (Lycaon The maintenance of brucellosis in bison in the the 1980s and 1990s (22). Similarly, the biting pictus) have been declining since the 1960s. Grand Teton National Park (United States) is midge vector for (AHS) This species is now endangered and, with a related to the presence of disease in managed and bluetongue has recently invaded Europe fragmented population of less than 5000, is sympatric elk (20). Even changes in arable and North Africa (23). susceptible to stochastic events such as dis- farming may lead to disease emergence, such as ease outbreaks. Wild dogs became extinct in the shift in agriculture from the eastern United Spill-Over and “Spill-Back” the Serengeti in 1991, concurrent with States to the Midwest, which allowed refores- The of infectious agents from epizootic canine distemper in sympatric do- tation of New England, providing the condi- reservoir animal populations (often domesti- mestic dogs (18, 24). Rabies has also caused tions for Lyme disease emergence (21). cated species) to sympatric wildlife, termed mortality of wild dogs, and a viral variant

Table 1. Selected emerging* infectious diseases (EIDs) of humans and lying emergence. The expanded table (Web table 1) is available as terrestrial wildlife, classified to demonstrate degrees of involvement of supplementary material (5). EIDs that involve only humans, both humans humans, domesticated animals, and wildlife. Taken together with those and domesticated animals, or domesticated animals only are not in- mentioned in text, this list is representative, and examples are chosen cluded. EIDs of marine environments are covered in a separate, related purely to demonstrate the range of pathogens, hosts, and factors under- paper (3).

Disease and Geography of Impact on wildlife Factors associated Pathogen Hosts‡ Refs. class of EID† emergence populations with emergence

Humans–domestic animals–wildlife disease 1 Hendra virus Humans, horses, fruit Australia, Unknown Unknown (16) (paramyxovirus) reservoir Papua New on September 1, 2008 Guinea disease 1 Nipah virus Humans, domestic pigs Malaysia and Unknown Unknown (45) (paramyxovirus) and dogs, fruit Singapore Cryptosporidiosis 4 Cryptosporidium Humans, cattle, wild Europe, USA Unknown Farming practices, (36) parvum (protozoan rodents and other emergence of parasite) mammals HIV, cross- species transfer Humans–wildlife Hantavirus pulmonary Sin Nombre and other Humans, Peromyscus spp., Americas, esp. Probably little ENSO event and (37)

syndrome 1 strains of hantavirus and other rodents SW USA impact human www.sciencemag.org (bunyaviruses) encroachment Marburg virus and Marburg and Ebola Humans and nonhuman Sub-Saharan High mortality in Marburg: (17) Ebola virus virus (filoviruses) primates, insectivorous or Africa, captive and wild translocation of hemorrhagic fever 1 fruit bat reservoir Indonesia, nonhuman infected suspected Philippines primates monkeys for lab research; Ebola: contact with infected human

or nonhuman Downloaded from carcasses or patients Human monocytotropic Ehrlichia chaffeensis, E. Humans, cervids, horses, USA, Europe, Apparently little Uncertain (64) granulocytotropic phagocytophila and dogs and others Africa impact, but ehrlichioses 1,4 E. equi (tick-borne underresearched rickettsia) Plague 4 Humans, wide range of Panglobal, High mortality in Enzootic foci are (65) (bacterium) mammalian (especially notably prairie dog remnants of last rodent) hosts India, SW towns during panzootic USA epizootics outbreak in leading to early 1900s declines in endangered black-footed ferret Domestic animals–wildlife Canine distemper 3 Canine distemper virus Wide range of carnivores USA, Africa Extinction of Spill-over from (7, 24) (morbillivirus) African wild dog domesticated and black-footed dogs ferret populations; threat to Ethiopian wolf

444 21 JANUARY 2000 VOL 287 SCIENCE www.sciencemag.org S CIENCE’ S C OMPASS common in sympatric domestic dogs has patric populations of susceptible domesti- (global). The latter threatens to been identified from one such incident (25). cated animals. Brucellosis was probably spill back to domestic livestock (8, 9)and, The geographic expansion of human popula- introduced into America with cattle. In Yel- ultimately, to humans. tions and the consequent encroachment of lowstone National Park (United States), the domestic dog carriers may explain the emer- presence of this disease in elk and bison is Emergence Owing to Host or Parasite gence and impact of rabies in wild dogs in the considered a potential threat to domesti- Translocations Serengeti (25). cated cattle grazing at the park boundaries The translocation of wildlife for conserva- Spill-over epizootic outbreaks represent (20). Other examples of spill-over infec- tion, agriculture, and hunting occurs on a aseriousthreatbothtowildlifeand,via tions include sarcoptic mange in foxes (Eu- global scale, with an inherent risk of exposure reverse spill-over (“spill-back”), to sym- rope) and wombats (Australia) and bovine of wildlife species to exotic infectious agents

Table 1. (continued)

Disease and Geography of Impact on wildlife Factors associated Pathogen Hosts‡ Refs. class of EID† emergence populations with emergence

Humans–domestic animals–wildlife (continued) Canine parvovirus disease 1 Canine parvovirus Canids Europe, USA Suspected cause of novel (66) of gray wolf , contact population with domestic declines; threat dogs to Ethiopian wolf Varroasis 2 Varroa jacobsoni Wild and domesticated Panglobal Catastrophic mass Introduction of (28) (mite) honeybees except mortality, e.g., hosts into Australasia 75% loss of enzootic region and C. Africa feral colonies in California Neurotropic velogenic Newcastle disease Double-crested cormorants, Canada, USA High mortality Unknown (67) on September 1, 2008 Newcastle disease 2 virus , gulls, poultry rates (up to 80 (paramyxovirus) to 90%) Sarcoptic mange 2 Sarcoptes scabiei Mammals Australia, UK, Recent threat to Dispersal of (68) (mite) Sweden wildlife in infected Sweden; wildlife; emerging threat domestic to wombats in dog–wildlife Australia interactions Wild animals only Amphibian Batrachochytrium Range of amphibian species, Australia, Mass mortalities, Unknown; (40, 41) chytridiomycosis 1 dendrobatidis including anurans and Central population evidence www.sciencemag.org (fungus) salamanders and North declines, local indicates America and possibly introduced global pathogen and extinctions possibly associated with climate change in C. America Viral chorioretinitis Wallal virus and Kangaroo spp. Australia Substantial Unknown; (69) “Kangaroo blindness” 1 possibly Warrego mortalities possibly Downloaded from virus; vector-borne weather related orbivirus Crayfish plague 2 Aphanomyces astaci Crayfish Europe High mortality Introduction of (70) () rates with infected North population American declines, crayfish (in threatening which the native species infection is with extinction enzootic and nonlethal) Captive wild animals Steinhausiosis Steinhausia sp. Partula snails Global extinction Unknown (54, 55) (protozoan parasite) of P. turgida Avian malaria spp. Birds High mortality in Translocation of (71) (protozoan susceptible naı¨ve animals parasites) species, e.g., to enzootic penguins regions Pneumonia Ophidian Epizootics with Unknown (72) paramyxovirus high mortality rates *Before this review, few wildlife diseases had been labeled “emerging” (19, 73). The criteria used to distinguish emerging from established infectious diseases are described in the introduction and in Table 2. †EID are classified on the basis of their “emerging” characteristics, according to criteria listed in Table 2. EID of captive wild animals are not classified since geographic range is not relevant in these cases. ‡Not all hosts are listed. The identity of reservoir hosts for some EID remains uncertain.

www.sciencemag.org SCIENCE VOL 287 21 JANUARY 2000 445 S CIENCE’ S C OMPASS (4, 8, 9). Translocation and introduction of pials. These animals evolved in the absence linked to declines in Central American and animals to new geographic regions corre- of , and only recently, af- Australian rain forests (40). The emergence spond to increased human global travel and ter human intervention (translocation), they of chytridiomycosis in amphibians radically commerce as underlying factors for infec- have been exposed to the parasite (32). The changes our view of wildlife EIDs, because it tious disease emergence (2, 14). The translo- feeding of contaminated neonate mice to cap- is the first such disease to emerge in “pris- cation of fish, and possibly amphibians, may tive callitrichid primates (marmosets and tine” sites, to infect a wide range of hosts, and have driven the emergence of ranavirus tamarins) led to the emergence of callitrichid to cause declines and possibly extinctions in epizootics as threats to freshwater fish and hepatitis (32), caused by a variant of the disparate regions. Hypotheses for the rela- wild herpetofauna (26). Similarly, a rabies zoonotic pathogen, lymphocytic choriomen- tively synchronous emergence of amphibian epizootic in the mid-Atlantic region of the ingitis virus (LCMV). The zoonotic risk of chytridiomycosis globally include human-as- United States resulted from translocation of LCMV is mirrored by the transfer of patho- sisted introduction to previously unexposed infected raccoons from a southeastern U.S. gens from humans to wildlife species. For amphibian populations (41), or an alteration enzootic focus (27). The introduction of po- example, measles contracted from humans of preexisting host-parasite relations owing to tential hosts into new geographic areas with- threatens wild mountain gorillas habituated to climate change (42). out co-introduction of pathogens can also tourists, and poliovirus has killed chimpan- result in disease emergence. For example, zees in the Gombe National Park in Tanzania The Zoonotic Threat varroasis, a disease of honeybees caused by (33). Most human EIDs result from exposure to the mite Varroa jacobsoni, spread globally Captive breeding programs aim to main- zoonotic pathogens, that is, those transmitted (except Australia) after the European honey- tain genetically viable, healthy populations naturally between animals and humans, with bee (Apis mellifera) was introduced into Asia for subsequent release into the wild. The or without establishment of a new life-cycle (28). potential transfer of pathogens into previous- in humans. Wildlife play a key role in their This form of emergence is a particular ly unexposed wild populations in often sen- emergence by providing a “zoonotic pool” concern to conservation programs that bring sitive, protected areas represents a serious from which previously unknown pathogens allopatric endangered species into close prox- challenge to conservation efforts (8, 9, 13). may emerge (2). This occurs classically for imity or that alter basic host-parasite vari- This can impinge on release programs even influenza virus, which causes pandemics in ables such as population density and structure when no apparent disease is observed. The humans after periodic exchange of be- (8, 9, 11, 13). Molecular analyses of a newly release of captive-reared field crickets (Gryl- tween the viruses of wild and domestic birds, discovered herpesvirus associated with dis- lus campestris) was suspended in England pigs, and humans. Recent nucleic acid se- on September 1, 2008 ease in captive elephants indicate that a nor- after the discovery of unidentified, potential- quence analyses have demonstrated direct mally benign herpesvirus of the African ele- ly exotic parasites that were not associated transmission of to humans phant can be lethal to its Asian cousin (29). with ill-health, but that posed a disease threat (43) and have identified potential nonhuman Another notable example is the exposure of to sympatric wild species at release sites (34). primate reservoirs from which HIV types 1 zoo animals in the United Kingdom to food The loss of host-specific parasites from en- and 2 originated (44). hosts contaminated by the BSE agent (30). Scrapie- dangered species in captive breeding pro- for Ebola and Marburg viruses have proved like spongiform encephalopathies thought to grams is also a substantial threat to biodiver- more elusive (17), although fruit or insectiv- result from exposure to the BSE agent have sity conservation. In addition to ethical obli- orous bats, insectivores, and rodents have

been confirmed in 58 zoo animals of 17 gations to conserve parasite assemblages been tentatively implicated. The link to bats www.sciencemag.org species (31). Recommendations have been along with their more favored hosts (35), the is strengthened because (i) they can support published to preempt the potentially disas- maintenance of established host-parasite re- replication of experimentally inoculated vi- trous consequences to wildlife, agriculture, lations may be important for the overall well- rus, (ii) human infection has occurred near and public health should BSE be introduced being of the host species both at an individual bat-roosting sites, and (iii) Ebola virus sub- into free-living wildlife (31). level (maintenance of immunity) and at a types have been identified in geographically Risk factors for disease emergence in con- population level (maintenance of genetic di- dispersed regions (including Madagascar and servation programs are complex. For exam- versity) (8, 9, 11–13). the Philippines). Sequence analysis suggests ple, epizootic toxoplasmosis, with high mor- that separate Ebola outbreaks are associated Downloaded from tality rates, has occurred in captive lemurs, Emergence Without Overt Human with distinct emergence events, occurring ei- New World primates, and Australian marsu- Involvement ther directly from the primary reservoir, or Correlations between emergence of human via secondary or tertiary intermediate hosts. diseases (such as cryptosporidiosis, hemor- Similar chain events are thought to have oc- Table 2. Definition and classification of EIDs of rhagic fevers, cholera, and malaria) and curred in Australia for Hendra virus (fruit bat wildlife based on fundamental epizootiological pa- rameters derived from (1, 2). EIDs of humans are weather patterns [flooding, the El Nin˜o reservoir, horses, and humans) and Menangle defined as diseases that are newly recognized, newly Southern Oscillation (ENSO)] are common virus (fruit bat reservoir, domesticated pigs, appeared in the population, or are rapidly increasing (36, 37). These patterns may also cause and humans) (16), and in Malaysia and Sin- in incidence or geographic range (1, 2). Here, and in changes in parasite and intensity gapore for Nipah virus (fruit bat reservoir), Table 1, we classify EIDs according to their specific and host mortality rates in wild animals such which causes a fatal disease of humans, dogs, characteristics that are emerging or novel. E, emerg- as the 3- to 4-year cycles of population crash- and pigs (45). The involvement of fruit bats ing, new or increasing; R, recognized. es in feral sheep on the St. Kilda archipelago, in this high-profile group of EIDs has impli- Scotland (38), and major epizootics of AHS cations for further zoonotic disease emer- Incidence or EID Infectious Host geographic every 10 to 15 years in South Africa (39). gence. A number of species are to type agent species range There is increasing evidence that the frequen- remote oceanic islands, and these may harbor cy and severity of these events are influenced enzootic, potentially zoonotic, pathogens. 1E E E by anthropogenic effects on the climate. Searches for new zoonotic pathogens have 2R E E A newly discovered fungal disease, cuta- become part of the strategy to counter emerg- 3R E R 4R R E neous chytridiomycosis, has recently been ing disease threats to humans, and knowledge identified as the cause of amphibian mortality from studies of known pathogens can assist in

446 21 JANUARY 2000 VOL 287 SCIENCE www.sciencemag.org S CIENCE’ S C OMPASS this surveillance. Telford et al. (46) com- may also impact humans, either directly thought. This case highlights the inherent pared guilds of deer tick-transmitted zoonotic (Marburg virus importation into Germany) or problems parasites present to the conserva- pathogens in Eurasian Ixodes spp. ticks with via effects on domesticated animals (the in- tion community, in which there is reliance on those described from America and discovered troduction of AHS into Spain with zebra). captive propagation and reintroduction as a a novel , “deer tick virus,” related to Although there are numerous examples safeguard against extinction. Global extinc- the virulent Powassan virus. This work of disease emergence after pathogen intro- tion as a secondary effect of disease occurred showed similar host-parasite guilds in wild- duction (Table 1), there undoubtedly are after mass mortality of the eel grass (Zostera life host-vector assemblages separated since many more that have not been identified as marina) on the U.S. Atlantic seaboard caused the Pleistocene, and has important impli- such. For example, the decline of red squir- by the slime mold Labyrinthula zosterae. cations for future targeting of surveillance rels in Britain, recorded since 1900, may Here, a Z. marina eelgrass-specific limpet, efforts. have been caused by a parapoxvirus trans- Lottia alveus, was driven to extinction after mitted from introduced grey squirrels in more than 90% loss of its habitat (55). These “Pathogen Pollution”: Implications for which it is benign (51). Whether the patho- two cases also highlight the consequences of Global Biodiversity gen was co-introduced to Britain with the ignoring diseases of , which are One of the costs of human domination of the grey squirrel, or whether the establishment the most speciose form of life (47) and are Earth’s ecosystem is increasing global bio- of this reservoir host in Britain led to an crucial components of most ecosystems. geographical homogeneity caused by the increased exposure of red squirrels to a widespread introduction of nonnative flora preexisting pathogen, is unknown. Perspectives and fauna into new areas (14, 47). This an- The mechanics of pathogen pollution in- There is a clear economic cost of wildlife thropogenic form of invasion, sometimes volve international traffic in agricultural ma- EIDs. For example, in 1994, postexposure termed “biological pollution” (14, 47, 48) has terials, domesticated animals, food crops, and prophylaxis for 665 people who had potential caused loss of biodiversity globally, particu- timber, and in biologically contaminated contact with a single rabid kitten in a pet store larly on oceanic islands (49). wastes such as landfill and ballast water (47, in New Hampshire cost $1.1 million, and it Similar loss of biodiversity occurs when 48). Global hotspots of biodiversity and wil- has been estimated that the economic burden disease is introduced into naı¨ve populations. derness sites such as the Gala´pagos and - of Lyme disease treatment in the United The introduction of smallpox, typhus, and arctica are not exempt (52). Evidence of in- States may be around $500 million per an- measles by the conquistadors in the 15th and troduced disease in Antarctic wildlife (anti- num (56). The cost of importing AHS into 16th centuries resulted in catastrophic depop- bodies to the domestic chicken pathogen, in- Spain was estimated at $20 million (23). In on September 1, 2008 ulation and 50 million deaths among native fectious bursal disease virus, in Antarctic Australia, a recent epizootic of pilchards re- South Americans (4). A number of epizootio- penguins) has prompted legislation to main- duced fisheries production by around A$12 logical equivalents of these “first-contact” tain stricter controls against pathogen pollu- million over 3 years (57). The economic depopulations have occurred, but considering tion (52). impacts of zoonotic EIDs may be difficult to the global scale of anthropogenic domestic The impact of pathogen pollution may be and may have complex consequences. and feral animal introduction, their true ex- augmented by secondary or “knock-on” ef- For example, the recent proposal to ban blood tent has probably been grossly underestimat- fects that are difficult to predict. High mor- donation in the United States by persons who ed. MacPhee and Marx (50) implicate the tality of rabbits after the introduction of myx- have spent longer than 6 months cumulative- introduction of infectious diseases in the omatosis in the United Kingdom caused pop- ly in the United Kingdom during 1980–96 www.sciencemag.org striking loss of biodiversity after human col- ulation declines in stoats, buzzards, and owls and are considered as potential carriers of the onization of continental landmasses and large (4). Myxomatosis also led to local extinction BSE agent, will reduce the U.S. blood supply islands over the past 40,000 years, including of the endangered large blue butterfly, by by 2.2% (58). The cost of introduced disease many of the Pleistocene megafaunal extinc- reducing grazing pressure on heathlands to human, livestock, and crop health is tions. If pathogens have been introduced on a which, in turn, removed the habitat for an ant over $41 billion per year in the United States global scale within recent human history, species that assists developing butterfly lar- (48). Although the value of biodiversity and how many wildlife diseases currently consid- vae (12). The effect on rain forest ecology significance of disease threats can be calcu- ered native actually originated from these after disease-mediated local extinction of lated (59), the cost of global biodiversity loss Downloaded from introduction events? Anthropogenic introduc- multispecies amphibian assemblages is yet to due to disease is yet to be assessed. tion of exotic pathogens, which we term here be assessed, but is likely to be substantial There are few regulations concerning ex- pathogen pollution (human-mediated patho- (41). otic disease threats to wild animals, and few gen invasion), is implicated in many wildlife Vitousek et al. (47) suggest that introduc- systems for surveillance are in place. Current EIDs listed in Table 1, often acting in consort tion of alien species is the next most impor- measures for the detection and control of with spill-over events to drive emergence. tant cause of extinction to habitat loss. The human and livestock EIDs are inadequate for Pathogen pollution poses a substantial introduction of pathogens might achieve a the identification of similar threats to wild- threat to global biodiversity. First, it has the similar status. Introduced diseases have been life. The conservation community has drawn potential to cause catastrophic depopulation implicated in the local extinction of a number up guidelines to prevent the release of ani- of the new and naı¨ve host population. Sec- of species (7–11, 18, 24, 25) and the global mals carrying exotic pathogens to novel areas ond, when introduced diseases become enzo- (species) extinction of Hawaiian birds (53), (8, 9). These recommendations are currently otic, initial declines may be followed by the thylacine (11), Mascarene reptiles (49), underused: of almost 700 terrestrial verte- chronic population depression, and if the Pleistocene megafauna (50), and others. In brate translocations (within conservation pro- threshold host density for disease transmis- the first definitively proven example of ex- grams) per year between 1973 and 1986 in sion is lowered, local extinction may occur. tinction by infection, a microsporidian para- the United States, Australia, Canada, and In some cases, the success of invading host site extirpated the captive remnant population New Zealand, 24% occurred without any dis- species may be enhanced by parasite-mediat- of the Polynesian tree snail, Partula turgida ease screening, and fewer than 25% involved ed competition (“apparent competition”) due (54). Thus, the 20 or so other species of investigations into causes of death of the to the impact of co-introduced diseases on Partula occurring solely in captivity may be translocated animals (60). resident species (10). Disease co-introduction at greater risk of extinction than previously Future strategies for wildlife EID surveil-

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