Wildlife Society Bulletin 40(1):25–31; 2016; DOI: 10.1002/wsb.638
Risks Posed by Captive Cervids
Diseases Associated with Translocation of Captive Cervids in North America RICHARD GERHOLD,1 Department of Biomedical and Diagnostic Sciences, College of Veterinary Medicine, University of Tennessee, 2407 River Drive, Knoxville, TN 37996, USA GRAHAM HICKLING, Department of Forestry, Wildlife and Fisheries, University of Tennessee, 2431 Joe Johnson Drive, Knoxville, TN 37996, USA
ABSTRACT The privatization of captive cervids, with associated interstate movement of cervids, poses a
substantial health risk to native free-ranging wildlife and domestic animals in North America. Captive cervid operations provide an avenue for transmission of diseases such as chronic wasting disease that could have significant impact on wild cervid populations. In addition, other infectious parasites and pathogens that are potentially associated with captive cervid operations and translocation include, but are not limited to the agents of brucellosis (Brucella abortus), bovine tuberculosis (Mycobacterium bovis), hemorrhagic disease (Orbivirus spp.), bovine viral diarrhea (Pestivirus spp.), deer meningeal worm (Parelaphostrongylus tenuis), Johne’s disease (Mycobacterium avium paratuberculosis), and various arthropod-borne diseases. Transmission of disease agents into previously uninfected states and provinces through translocation of live animals can have adverse consequences. Monitoring and treatment to combat disease outbreaks associated with livestock– wildlife transmission costs states and provinces hundreds of millions of dollars. Inconsistency in jurisdiction, financial responsibility, and indemnity can lead to distrust and poor working relationships between state or provincial wildlife and agriculture departments. Although infectious disease transmission to humans has not been historically associated with wild deer, the translocation of cervids in conjunction with captivity can potentially lead to transmission of zoonotic disease agents including brucellosis and tuberculosis. We summarize the various disease agents associated with captive cervid operations and activities, potential for disease transmission to native wildlife and livestock, and associated costs. Proactive, rather than reactive, actions to prevent disease transmission from captive to wild animals should be of high priority for animal managers and regulatory agencies. Ó 2016 The Wildlife Society. KEY WORDS captive breeding, cervids, disease, disease transmission.
Numerous parasites and other pathogens that affect captive cervids are capable of infecting not only livestock but also wildlife species adjacent to such facilities. Captive cervid operations, often involving supplemental feeding, introduce numerous disease risk factors that lead to increased efficiency of disease transmission. These risk factors include artificially high numbers of cervids (often in close contact), increased stress, and contamination of food with infectious agents. Collectively, these risk factors enhance transmission opportunities for infectious agents. We address the 2 most important risk factors associated with captive cervids— namely pathogen transmission between captive and wild cervids and the movement of captive cervids to various geographical locations, potentially leading to concurrent movement of pathogens capable of infecting livestock and wild cervids.
Received: 31 July 2015; Accepted: 9 February 2016 1
E-mail:
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Gerhold and Hickling
Disease Risks from Captive Cervids
Past experience has shown that it is rarely physically or monetarily possible to exclude all contact between captive cervids and free-ranging wildlife over the life of a cervid facility. Unless expensive double-fencing is in place, contact will regularly occur at fence-lines. Even the most secure fences have failures that arise from unpredictable adverse events, such as tree-falls and washouts, through improper maintenance over longer periods, or simply through lack of care and attention by operators. In one survey, the most commonly identified risk factor was gates being left open (Wisconsin Department of Natural Resources 2002). Water flow-through, waste material, and carcasses may be found outside the confines of the fenced enclosure and can be a source of pathogen transmission (Miles et al. 2011; K. Schuler, Cornell University, personal communication). Fencing failures can lead to egress of captive cervids, ingress of wildlife, or both. For example, a chronic wasting disease (CWD)-positive elk (Cervus canadensis) pen in Minnesota, USA, was found to have >20 breaches within the fence and wild white-tailed deer (Odocoileus virginianus) were observed within the facility (M. Carstensen, Minnesota Department 25
of Natural Resources [MNDNR], personal communication). The owner of the pen was mandated by the MNDNR to kill wild deer found within the facility for subsequent testing for CWD. In addition, there is an unfortunate tendency for facilities in poor financial condition, or exhibiting other difficulties, to intentionally release animals. For example, the Wisconsin Department of Natural Resources (USA; 2002) identified intentional release of 9 captive cervids into the wild from one facility, with only 3 of the released deer having an ear tag. Unfortunately, the U.S. Department of Agriculture (USDA) CWD program standards do not require that herds monitored for CWD have visible ear tags and operators are not obligated to enter individual animal information into the National or State CWD database (USDA APHIS 2014). Recovery of escaped or released animals is generally impractical and always expensive—one key issue is the difficulty of distinguishing animals from captive versus freeranging populations, especially if escaped cervids are species native to the area and have no external tags or identifications. Even in situations where animals can be identified, captive cervid operators may not have the desire, resources, expertise, or authority to retrieve animals that escape into wildland areas or properties of other landowners; in such cases, costs (labor, supplies, and equipment) for retrieval inevitably fall on the state or province. Disputes over authority and jurisdiction can lead to state or provincial wildlife and agriculture departments having poor working relationships and unwillingness to share resources to ensure compliance. A survey of captive cervid facilities in New York, USA, disclosed that 38 (14%) had escapes and 11 were listed as unsuccessful in their recovery; furthermore, only 60 (21%) of the facilities were known to be under the routine care of a veterinarian (New York State Department of Environmental Conservation 2013). Escaped captive cervids have been documented to cross state lines, leading to jurisdictional disagreement among the state agencies involved. For example, an elk that escaped a Pennsylvania, USA, captive facility in January 2011—because a gate inadvertently was left open—roamed in the wild until being found in neighboring West Virginia, USA, in 2012 (J. Crum, West Virginia Division of Natural Resources [WVDNR] personal communication). Although this animal originally came from Pennsylvania, the state was unwilling to allow it to return given the concern the elk may have been infected with CWD while in West Virginia. The WVDNR confronted intense public resistance when they announced plans to euthanize the animal. The elk was finally moved to a separate facility in West Virginia. Had the elk been an unmarked captive whitetailed deer, it would have been nearly impossible to identify the escaped animal. The Pennsylvania Game Commission was not aware of this facility or that the elk was missing, which further emphasizes how escaped cervids can remain undetected or unknown to wildlife agencies. Of great concern is the risk of introduction of new disease agents into previously uninfected states and provinces through translocation of live cervids that potentially host disease agents or vectors. For many diseases, live-animal diagnostic tests lack the sensitivity to provide any strong 26
guarantee that a given animal is disease free. For example, captive cervid operations have been associated with detection of CWD in native wildlife in areas with no previous indication of the disease having been present (Miller and Wild 2004, Miller and Williams 2004, Carstensen et al. 2010). Originally thought to be geographically limited to a few western states with a relatively low natural rate of expansion, detection of CWD in multiple midwestern and eastern states has been repeatedly documented. The spread of the disease to these distant areas was likely due to marketdriven translocation of infected deer and elk because this distance is too great for infected deer to travel during natural dispersal (Miller and Williams 2004). A particular case in point: CWD was first found in Minnesota in a wild deer (Carstensen et al. 2010). Although the MNDNR tested 3,209 deer in 2009–2010 from the southeastern portion of the state, the only CWD-positive wild deer detected within the state was found within 3 miles (4.8 km) of a captive elk facility that previously had tested positive for CWD (Hildebrand et al. 2013). This captive facility had a low level of compliance with CWD testing and had >20 breaches in the fence, which allowed wild deer into the pen (M. Carstensen, personal communication). A separate example involving movement of a CWD-positive elk from a captive facility in Saskatchewan, Canada, to South Korea resulted in the first CWD-positive case outside North America (Sohn et al. 2002, Kahn et al. 2004). These cases underscore how easily the movement of captive cervids can lead to the translocation of pathogens, not only among states and nations but among continents. The critical issue with disease transmission from captive cervids to free-ranging wildlife is whether such events will result in short-term “spillover,” or long-term maintenance of disease in wild populations. Spillover events can be contained by prompt, intensive remedial actions, but this assumes adequate surveillance efforts are in place to detect wildlife disease outbreaks early enough for remedial responses to be effective. Wildlife surveillance activities can be very expensive, with costs inevitably borne by the state or province (Walsh 2012); thus, proactive surveillance programs are relatively rare. Most commonly, disease outbreaks are first detected by “passive” surveillance (i.e., reports of infected animals from hunters or hunt managers). The low probability of detecting early stage outbreaks means that diseases are typically well-entrenched in the wild population before being detected. For example, bovine tuberculosis (Mycobacterium bovis; TB) in Michigan, USA, wild deer and CWD in Wisconsin wild deer are both considered to have been present for a long time before detection (O’Brien et al. 2006, Jennelle et al. 2014). Endemic diseases are almost impossible to eradicate from free-ranging wildlife populations; worldwide, instances of successful eradication of diseases that have begun cycling in wild populations are extremely rare. The cases of both bovine TB in wild deer in Michigan and the multiple CWD-affected states and provinces with “eradication” efforts have in reality become exercises in long-term control or containment of endemic disease (O’Brien et al. 2011). Consequently, managers and policy-makers need to Wildlife Society Bulletin
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accept the paradigm that there is “no substitution for prevention” of wildlife diseases because once a disease is established, there will be little prospect of eradication. Diseases Associated with Privatization and Translocation of Captive Cervids Chronic wasting disease.—Although the epidemiology of CWD is not completely known, it is thought to be primarily animal-to-animal through exposure to infectious prion agents in feces, urine, or saliva, and by aerosol transmission (Mathiason et al. 2006, Haley et al. 2009, Denkers et al. 2013). Movement of live animals is considered one of the greatest risk factors in spreading CWD to new areas (Miller and Williams 2004). Given there is no reliable live-animal test for CWD, and infected animals may appear normal during the first several months to years of infection, it is impossible to know if cervids are infected prior to being translocated (Keane et al. 2009). Current USDA regulations allow interstate movement of animals from “CWD-certified herds” that have completed testing of eligible (i.e., natural mortalities) animals for 5 years; however, live animals may be moved between the owner’s propagation and shooting premises without any testing. Because subclinically infected animals can shed CWD prions within months of infection, it is possible to infect a premise and produce new infections in animals that do not contact a clinically affected animal. Prions, the agent of CWD, are extremely persistent in the environment and decontamination of an area is difficult and expensive, if not impossible (Tamguney et al. 2009). Modeling of CWD suggests that the disease could have very significant negative population impacts (Almberg et al. 2011). Results from modeling a declining mule deer (Odocoileus hemionus) population in Wyoming, USA, indicated a 19% annual decline in the deer population and concluded that CWD contributed to this decline because removal of CWD from the model resulted in a stable population (DeVivo 2015). Transmission of CWD can occur among mule deer, white-tailed deer, and elk (Williams 2005), so the translocation of any of these species has the potential to trigger emergence of CWD in new locations. In addition, other species including moose (Alces alces) and reindeer (Rangifer tarandus tarandus) can also be infected with CWD (Baeten et al. 2007, Moore et al. 2015). The financial impact of CWD to state agencies is often difficult to measure. Testing and disease surveillance can be a significant cost for agencies. For example, after CWD was first identified in West Virginia in 2005, a minimum of US $2.6 million had been spent on CWD surveillance and monitoring by 2015 (J. Crum, personal communication). This figure surely underestimates the true economic impact of CWD to West Virginia state resources. Four state agencies in Wisconsin spent US$32.3 million in the first 5 years after finding the disease, 83% of which came from the Department of Natural Resources (Wisconsin Department of Natural Resources 2006). The MNDNR spent US $5.2 million from 2003 to 2014 in CWD surveillance and management. However, only 8% of these dollars were from federal cooperative funding, the other 92% were state funds Gerhold and Hickling
Disease Risks from Captive Cervids
primarily derived from deer-hunting fees (M. Carstensen, personal communication). The perceived risk to human health among hunters may lead to decreased license sales, further decreasing agency revenue. Wisconsin documented an 11% decline in hunter participation, corresponding to a license sales decline of >90,000, following the discovery of CWD in the state (Heberlein 2004). To combat CWD in Wisconsin, >US$11 million was allocated to control efforts and these funds led to decreases in game bird stocking and other wildlife programs. Even with these efforts and financial expenditures, management actions to limit the disease impact have been unsuccessful and there is warranted concern of continual spread of the disease. Other diseases associated with captive cervid operations and translocation.—Other diseases found in captive cervid operations that are of concern for wildlife include a variety of bacterial, viral, and parasitic diseases such as brucellosis, bovine TB, hemorrhagic disease (Orbivirus spp.) viruses, malignant catarrhal fever, Parelaphostrongylus tenuis, and various arthropods with associated disease agents. Brucellosis is a zoonotic disease caused by the bacterium Brucella abortus that is a significant threat to the cattle industry given its highly efficient transmission and potential for causing abortion in infected cattle. Elk are known to be susceptible to B. abortus, and experimental infections suggest elk can experience latent infections with surviving calves being serologically and clinically negative until their own first pregnancy (Thorne 2001). Brucellosis testing requirements for imported captive cervids are dependent on the regulations of the importing state; thus, elk being imported into states without these regulations may have unknown Brucella infection status (USDA APHIS 2015). Brucella abortus is able to persist in tissues of an infected fetus, as well as the soil and vegetation, for up to 81 days, depending on ambient conditions; it potentially could persist in fetal tissues for up to 6 months if the fetus was shaded from sunlight (Wray 1975, Aune et al. 2012). Documentation of brucellosis in cattle herds typically results in the state losing its brucellosis-free status. As a result, trade restrictions would then be imposed by USDA, which affects interstate movement of cattle. Moose are especially susceptible to B. abortus and infection in moose is usually fatal (Forbes et al. 1996). Given that moose are declining across much of their range, further disease introductions can lead to substantial population impacts. The highly infectious nature of this disease agent for livestock warrants caution and concern regarding translocation of captive cervids. Mycobacterium bovis, the causative agent of bovine TB, has one of the broadest host ranges of all known pathogens, affecting many groups of mammals including humans (O’Reilly and Daborn 1995). Before the 1990s, M. bovis had rarely been reported in free-ranging cervids in North America, but it is now known to have infected several wild populations. In 1995, the Michigan Department of Natural Resources identified an endemic focus in free-ranging deer in a 5-county area of Michigan’s northeastern Lower Peninsula. Mycobacterium bovis was probably first transmitted from 27
cattle to deer in the mid-1900s, when bovine TB was widespread in cattle of the area (O’Brien et al. 2006). In 2005, M. bovis was discovered in deer in Minnesota in conjunction with an outbreak of M. bovis in beef cattle (Carstensen and DonCarlos 2011). In Manitoba, Canada, a herd of 2,500–4,000 elk has been implicated in an outbreak of M. bovis in cattle herds surrounding Riding Mountain National Park (Lees et al. 2003). Mycobacterium bovis infection in wildlife is thought to have been established via commingling of wild cervids with infected livestock or contaminated feed, such as when elk and cattle feed on the same hay bales. Indeed, Miller and Sweeney (2013) identified commingling and supplemental feeding as key risk factors for M. bovis transmission to wildlife. Commingling of deer with livestock has intensified in recent decades as wild deer populations and the number of game ranches have increased. In some locations, exotic hoofstock or native cervids are being released or baited into areas where they mix with cattle and feral swine, increasing the risk of 2- or 3-way pathogen exchange (Cooper et al. 2010). To date, the only apparently successful eradication of M. bovis in wild cervids has been in Minnesota, which had by far the smallest and most recent of the 3 outbreaks. Greater than 10,000 Minnesota deer were tested, with the deer population in the affected area reduced by an estimated 55% in 4 years at an estimated cost of US$86 million in federal and state expenditures (Carstensen and DonCarlos 2011, Glaser et al. 2016). The future expenditure needed to achieve M. bovis eradication in Michigan has been estimated to be US$1.5 million annually over the next 30 years (Cosgrove et al. 2012); however, this would require taxpayer dollars, with concomitant uncertainty in public and political commitment to such a long-term effort. Hemorrhagic disease, caused by epizootic hemorrhagic disease (EHDV) and blue tongue (BTV) viruses transmitted by Culicoides midges, is one of the most important diseases of wild deer (Howerth et al. 2001); domestic sheep are also susceptible to BTV. There are multiple native serotypes of EHDV and BTV circulating in the United States that lead to variable morbidity and mortality in deer (Howerth et al. 2001), with sporadic reports of major mortality events in certain regions. Unfortunately, multiple nonendemic serotypes of these viruses have been introduced into the United States during the past several years. Isolations of these nonendemic serotypes were obtained from wild and captive white-tailed deer in Arkansas (BTV-3), Kansas (EHDV-6), Texas (EHDV-6, BTV-12), and Michigan (EHDV-6). The BTV-3, BTV-12, and EHDV-6 all represent viruses that were not known to occur in the United States prior to 1999 (U.S. Animal Health Association 2009, Ruder et al. 2015). The exact mechanism of the nonnative viruses being introduced into the United States is not known; however, translocation of cervids offers an avenue of further transmission. Adult cattle and calves with lesions associated with EHD have been recently reported; however, it is uncertain which viral strains are responsible (Garrett et al. 2015). Viruses that contain genetic material of both native and exotic EHD viruses have been found in moribund deer, 28
demonstrating that potential for virus reassortment (Allison et al. 2010). Although significant population impacts due to these nonnative or reassorted serotypes have not been reported in wild or domestic animals, the epidemiology and disease potential of these viruses in cattle and native deer is incompletely known. The construction of autogenous HD vaccines that occurs in captive cervid facilities may influence HD virus natural selection and reassortment process given the likelihood of partial immune protection of circulating EHD and BT strains in artificially dense cervid populations. Cases of bovine viral diarrhea (Pestivirus spp.; BVD) and malignant catarrhal fever (MCF) have been reported in confined deer (Hong et al. 2000, Passler et al. 2010). Cases of BVD typically manifest as diarrhea and dehydration, and are febrile, thus, leading to low morbidity and high mortality (van Campen et al. 2001). Abortions can occur in infected animals, and still-born and mummified fetuses have been observed in white-tailed deer infected with BVD. Lesions of animals infected with MCF are variable, including lacrimal and nasal discharge; ocular opacities; and reddening and necrosis of oral mucosa, lips, gums, hard and soft pallet, and buccal mucosa (Heuschele and Reid 2001). Transmission of BVD can be maintained in deer by congenital infection through persistently infected fawns (Passler et al. 2010). Typically BVD and MCF are not observed in deer, but Passler et al. (2010) suggested that captive deer may be a source of infection for domestic livestock. Parelaphostrongylus tenuis (i.e., meningeal worm or brain worm) is a nematode parasite found in the meninges of white-tailed deer in the eastern United States. Although P. tenuis rarely causes clinical signs or lesions in white-tailed deer, it can cause severe neurological morbidity or mortality in aberrant or dead-end hosts such as elk, moose, llamas (Lama glama), alpacas (Vicugna pacos), and numerous other cloven-hoof stock, including goats (Capra hircus aegagrus; Anderson 1972; Lankester 2001, 2010; Whitehead and Bedenice 2009). P. tenuis has also been documented as a cause of morbidity and mortality in domestic cattle and horses (Tanabe et al. 2010, Mitchell et al. 2011). Clinical signs include ataxia, circling, head tilt, hind limb paresis, arched neck, blindness, and eventual death (Anderson 1972, Lankester 2001). Hosts are infected by ingesting terrestrial snails and slugs infected with third-stage larvae. Experimentally infected elk were competent patent hosts for P. tenuis and passed larvae in their feces (Samuel et al. 1992). Currently, there is no commercially available antibody test to detect P. tenuis antemortem; fecal exams have variable sensitivity because larvae are inconsistently shed and testing may have been performed during the prepatent period, when larvae are not shed. Even necropsy exams in conjunction with nested Polymerase Chain Reaction (a technique that amplifies DNA of target organism) has variable sensitivity in diagnosing P. tenuis infection (Dobey et al. 2014). Currently within the United States and Canada, P. tenuis is only found in the eastern and midwestern regions, but there is warranted concern about the potential for introduction of infected cervids from east to west. This is of particular concern given the increased number of Wildlife Society Bulletin
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free-ranging white-tailed deer in various parts of the western region where suitable intermediate hosts, including Deroceras laeve, are known to occur (Frest and Johannes 2000). If P. tenuis became established in white-tailed deer in western North America, it would likely be impossible to eradicate the parasite from these hosts and would represent a substantial threat to native wild cervids including moose, elk, and caribou (Rangifer tarandus). To further demonstrate the potential for novel parasite infections, a retrospective exam of suspect P. tenuis-infected domestic and wild ungulates disclosed a P. odocoilei-like infection in a goat from Tennessee, USA (Dobey et al. 2014). It is unknown whether this was a recent introduction of this parasite into Tennessee, however, it demonstrates how parasite species could be imported into previously uninfected regions and thus lead to morbidity and mortality of domestic animals. Similar to P. tenuis, Elaphostrongylus rangiferi is an important neurological disease of cervids in Europe that has also been found Newfoundland, Canada. The parasite was introduced into the Canadian province by translocation of captive reindeer from Norway (Lankester and Fong 1989). Moose, as well as domestic animals including sheep and goats, are known to become infected with E. rangiferi. Translocation of cervids from regions where E. rangiferi is endemic to other regions can lead to increased parasite distribution. Further examples of parasite distribution from translocated cervids includes Rumenfilaria andersoni, which historically was found in moose from North America (Lankester and Snider 1982). Translocation of white-tailed deer to Finland in the 1930s likely led to introduction of R. andersoni to reindeer (Laaksonen et al. 2015). The prevalence of R. andersoni parasites is substantially greater in reindeer compared with deer and moose in Finland, suggesting a lack of adaptation of the parasite in the reindeer host. The health impacts of R. andersoni in reindeer are currently unknown, but a high density of R. andersoni microfilariae may have systemic effects (Laaksonen et al. 2015). Ectoparasitic infection is additionally of concern with translocation and transmission of Ehrlichia ruminantium, which is the causative agent of heartwater. Although this pathogen is not currently known to occur in the United States, introduction of one of the vectors—the tropical bont tick (Amblyomma variegatum)—from the Caribbean could be sufficient to introduce the disease into the United States (Uilenberg 1981). Once in the United States, the disease could be spread by a North American species—the gulf coast tick (Amblyomma maculatum)—which has been shown to be a competent vector of E. ruminantium in the laboratory (Uilenberg 1982). Given the pathogen has a wide host range, there is warranted concern about disease transmission among wild and domestic ruminants. Clinical disease includes neurological impairment, pulmonary edema, diarrhea, anorexia, and potential mortality (Uilenberg 1981). Mortality rates in susceptible livestock can be as high as 90%. The potential for Amblyomma ticks to survive on hosts during translocation provides an avenue of transmission for E. ruminantium disease, either through international Gerhold and Hickling
Disease Risks from Captive Cervids
movement of wild hoof-stock or, if introduced into the United States, through movement of captive cervids. Exotic Damalinia sp. louse infestations in western United States native deer species are another example of a likely introduced ectoparasite causing disease in native wildlife. These exotic lice are thought to have been introduced through the translocation of exotic cervids (Bildfell et al. 2004). Infestation in combination with deer chewing and licking of hair leads to loss of haircoat and poor body condition (Bildfell et al. 2004). Fawns and adult females appear to be most affected by the parasite, with hair loss syndrome increasing overwinter mortality of fawns (McCoy et al. 2014). These examples underscore the implications of nonnative arthropods and their potential effects on wildlife and domestic animal populations. Past experience in many countries has shown that diseases that are controllable when restricted to livestock species become almost impossible to eradicate once spread to freeranging wildlife. In numerous recent wildlife disease outbreaks in the United States and Canada, captive cervid facilities have been implicated as a key epidemiological risk factor that has triggered, or at least contributed to, emergence and spread of serious diseases such as CWD and bovine TB. Response to these outbreaks has been necessarily reactive, enormously expensive, and controversial, with uncertain success (O’Brien et al. 2006, 2011; Jennelle et al. 2014). A key recommendation of this review is that proactive, rather than reactive, actions to prevent disease transmission from captive to wild animals should have high priority for animal managers and regulatory agencies. In this context, operation of captive cervid facilities located adjacent to wild cervid populations, and interstate translocation of cervids between such facilities, are risk factors that should be managed proactively. Such measures include targeted disease surveillance of wildlife surrounding captive cervids and lobbying to retain the jurisdiction (with ample funding and manpower) to regulate captive cervid operations in states and provinces that allow captive cervid farming. However, whenever possible, efforts should focus on eliminating or banning captive cervid facilities via working with local or national wildlife agencies, livestock associations, and public health departments. Finally, wildlife agencies should make efforts to catalog the direct and indirect financial revenues generated from consumptive and nonconsumptive utilization of native cervid and other wildlife populations and disseminate this information to legislatures and stakeholders; thus, allowing them to comprehend the negative economic impact that can result when introduction of disease agents results in negative wildlife population impacts.
ACKNOWLEDGMENTS We thank Krysten Schuler, James Crum, and Michelle Carstensen for reviewing earlier versions of this manuscript and J. McDonald, the 2 reviewers, and T. Boal for editing.
LITERATURE CITED Allison, A. B., V. H. Goekjian, A. C. Potgieter, W. C. Wilson, D. J. Johnson, P. P. C. Mertens, and D. E. Stallknecht. 2010. Detection of a 29
novel reassortant epizootic hemorrhagic disease virus (EHDV) in the USA containing RNA segments derived from both exotic (EHDV-6) and endemic (EHDV-2) serotypes. Journal of General Virology 91:430–439. Almberg, E., P. Cross, C. Johnson, D. Heisey, and B. Richards. 2011. Modeling routes of chronic wasting disease transmission: environmental prion persistence promotes deer population decline and extinction. PLoS ONE 6:e19896. Anderson, R. C. 1972. The ecological relationships of meningeal worm and native cervids in North America. Journal of Wildlife Diseases 8:304–310. Aune, K., J. Rhyan, R, Russell, T. Roffe, and B. Corso. 2012. Environmental persistence of Brucella abortus in the Greater Yellowstone area. Journal of Wildlife Management 76:253–261. Baeten, L., B. Powers, J. Jewell, T. Spraker, and M. Miller. 2007. A natural case of chronic wasting disease in free-ranging moose (Alces alces shirasi). Journal of Wildlife Diseases 43:309–314. Bildfell, R., J. Mertins, J. Mortenson, and D. Cottam. 2004. Hair-loss syndrome in black-tailed deer of the Pacific Northwest. Journal of Wildlife Diseases 40:670–681. Carstensen, M., L. Cornicelli, D. Pauly, E. Hildebrand, and E. Butler. 2010. Intensified chronic wasting disease surveillance in Minnesota’s southeastern wild deer herd. Minnesota Department of Natural Resources. http://files.dnr.state.mn.us/publications/wildlife/research2010/health.pdf. Accessed 12 Jul 2015. Carstensen, M., and M. W. DonCarlos. 2011. Preventing the establishment of a wildlife disease reservoir: a case study of bovine tuberculosis in wild deer in Minnesota, USA. Veterinary Medicine International 2011:413240. doi: 10.4061/2011/413240 Cooper, S. M., H. M. Scott, G. R. de la Garza, A. L. Deck, and J. C. Cathey. 2010. Distribution and interspecies contact of feral swine and cattle on rangelands in South Texas: implications for disease transmission. Journal of Wildlife Diseases 46:152–164. Cosgrove, M. K., H. Campa III, D. S. L. Ramsey, S. M. Schmitt, and D. J. O’Brien. 2012. Modeling vaccination and targeted removal of white-tailed deer in Michigan for bovine tuberculosis control. Wildlife Society Bulletin 36:676–684. Denkers, D. D., J. Hayes-Klug, K. Anderson, D. Seeling, N. Haley, S. Dahmes, D. Osborne, K. Miller, R. Warren, C. Mathiason, and E. Hoover. 2013. Aerosol transmission of chronic wasting disease in whitetailed deer. Journal of Virology 87:1890–1892. DeVivo, M. 2015. Chronic wasting disease ecology and epidemiology of mule deer in Wyoming. Dissertation, University of Wyoming, Laramie, USA. Dobey, C. L., C. Grunenwald, S. J. Newman, L. Muller, and R. W. Gerhold. 2014. Retrospective study of central nervous system lesions and association with Parelaphostrongylus species by histology and specific nested polymerase chain reaction in domestic camelids and wild ungulates. Journal of Veterinary Diagnostic Investigation 26:748–754. Forbes, L. B., S. V. Tessaro, and W. Lees. 1996. Experimental studies on Brucella abortus in moose (Alces alces). Journal of Wildlife Diseases 32:94–104. Frest, T. J., and E. J. Johannes. 2000. An annotated checklist of Idaho land and freshwater mollusks. Journal of the Idaho Academy of Science 36:1–51. Garrett, E., E. Po, E. Bichi, S. Hexum, R. Melcher, and A. Hubner. 2015. Clinical disease associated with epizootic hemorrhagic disease virus in cattle in Illinois. Journal of the American Veterinary Medical Association 247:190–195. Glaser, L., M. Carstensen, S. Shaw, S. Robbe-Austerman, A. Wunschmann, D. Grear, T. Studer, and B. Thomsen. 2016. Descriptive epidemiology and whole genome sequence analysis for an outbreak of bovine tuberculosis in beef cattle and white-tailed deer in northwestern Minnesota. PLoS ONE 11(1):e0145735. Haley, N. J., D. M. Seelig, M. D. Zabel, G. C. Telling, and E. A. Hoover. 2009. Detection of CWD prions in urine and saliva of deer by transgenic mouse bioassay. PLoS ONE 4(3):e4848. Heberlein, T. 2004. “Fire in the Sistine Chapel”: how Wisconsin responded to chronic wasting disease. Human Dimensions of Wildlife 9:165–179. Heuschele, W., and H. Reid. 2001. Malignant catarrhal fever. Pages 157– 164 in E. S. Williams, and I. K. Barker, editors. Infectious diseases of wild mammals. Third edition. Iowa State Press, Ames, USA. Hildebrand, E., M. Carstensen, L. Cornicelli, D. Pauly, and M. Dexter. 2013. Chronic wasting disease management in Minnesota
30
deer herd: coordinated response to southeast detection, 2010–2013. Minnesota Department of Natural Resources. http://files.dnr.state.mn.us/ publications/wildlife/research2013/health.pdf. Accessed 12 Jul 2015. Hong, L., N. Dyer, J. Keller, and T. B. Crawford. 2000. Newly recognized herpesvirus causing malignant catarrhal fever in white-tailed deer (Odocoileus virginianus). Journal of Clinical Microbiology 38:1313–1318. Howerth, E., D. Stallknecht, and P. Kirkland. 2001. Bluetongue, epizootic hemorrhagic disease, and other orbivirus-related diseases. Pages 77–97 in E. S. Williams, and I. K. Barker, editors. Infectious diseases of wild mammals. Third edition. Iowa State Press, Ames, USA. Jennelle C. S., V. Henaux, G. Wasserberg, B. Thiagarajan, R. E. Rolley, and M. Samuel. 2014. Transmission of chronic wasting disease in Wisconsin white-tailed deer: implications for disease spread and management. PLoS ONE 9(3):e91043. Kahn, S., C. Dube, L. Bates, and A. Balachandran. 2004. Chronic wasting disease in Canada: part 1. Canadian Veterinary Journal 45:397–404. Keane, D., D. Barr, R. Osborn, J. Langenberg, K. O’Rourke, D. Schneider, and P. Bochsler. 2009. Validation of use of rectoanal mucosa-associated lymphoid tissue for immunohistochemical diagnosis of chronic wasting disease in white-tailed deer (Odocoileus virginianus). Journal of Clinical Microbiology 47:1412–1417. Laaksonen, S., A. Oksanen, and E. Hoberg. 2015. A lymphatic dwelling filarioid nematode, Rumenfilaria andersoni (Filarioidea; Splendidofilariinae), is an emerging parasite in Finnish cervids. Parasites and Vectors 8:228. Lankester, M. W. 2001. Extrapulmonary lungworms of cervids. Pages 228– 246 in W. M. Samuel, M. J. Pybus, and A. A. Kocam, editors. Parasitic diseases of wild mammals. Second edition. Iowa State University Press, Ames, USA. Lankester, M. 2010. Understanding the impact of meningeal worm, Parelaphostrongylus tenuis on moose populations. Alces 46:53–70. Lankester, M., and D. Fong. 1989. Distribution of elaphostrongyline nematodes (Metastrongyloide:Protsrongylidae) in cervids and possible effects of moving Rangifer spp. into and within North America. Alces 25:133–145. Lankester, M. W., and J. B. Snider. 1982. Rumenfilaria andersoni n. gen., n. sp. (Nematoda: Filarioidea) in moose, Alces alces (L.), from northwestern Ontario, Canada. Canadian Journal of Zoology 60:2455–2458. Lees, V. W., S. Copeland, and P. Rousseau. 2003. Bovine tuberculosis in elk (Cervus elaphus manitobensis) near Riding Mountain National Park, Manitoba, from 1992 to 2002. Canadian Veterinary Journal 44:830–831. Mathiason, C. K., J. G. Powers, S. J. Dahmes, D. A. Osborn, K. V. Miller, R. J. Warren, G. L. Mason, S. A. Hays, J. Hayes-Klug, D. M. Seelig, M, Wild, L. Wolfe, T. Spraker, M. Miller, C. Sigurdon, G. Telling, and E. Hoover. 2006. Infectious prions in the saliva and blood and deer with chronic wasting disease. Science 314:133–136. McCoy, R. H., S. Murphie, M. Szykman, and B. Murphie. 2014. Influence of hair loss syndrome on black-tailed deer fawn survival. Journal of Wildlife Management 78:1177–1188. Miles, S. L., K. Takizawa, C. P. Gerba, and L. L. Pepper. 2011. Survival of infectious prions in water. Journal of Environmental Science and Health Part A, Toxic/Hazardous Substances & Environmental Engineering 46:938–943. Miller, M. W., and S. J. Sweeney. 2013. Mycobacterium bovis (bovine tuberculosis) infection in North American wildlife: current status and opportunities for mitigation of risks of further infection in wildlife populations. Epidemiology and Infection 141:1357–1370. Miller, M. W., and M. Wild. 2004. The epidemiology of chronic wasting disease in captive white-tailed and mule deer. Journal of Wildlife Diseases 40:320–327. Miller, M. W., and E. S. Williams. 2004. Chronic wasting disease of cervids. Current Topics in Microbiological Immunity 284:193–214. Mitchell, K., J. Peters-Kennedy, T. Stokol, R. W. Gerhold, R. Beckstead, and T. Divers. 2011. Parelaphostrongylus tenuis infections as a cause of meningomyelitis in 5 calves. Journal of Veterinary Internal Medicine 23:1097–1103. Moore, S., R. Kunkle, E. Nicholson, J. Richt, A. Hamir, W. Wade, and J. Greenlee. 2015. Transmission of chronic wasting disease to sentinel reindeer (Rangifer tarandus tarandus). Abstract submitted to American College of Veterinary Pathologists Meeting. U.S. Department of Agriculture. http://www.ars.usda.gov/research/publications/publications. htm?SEQ_NO_115¼317903. Accessed 12 Jul 2015.
Wildlife Society Bulletin
40(1)
New York State Department of Environmental Conservation. 2013. Surveillance plan for chronic wasting disease in New York State 2013– 2014. New York State Department of Environmental Conservation. http:// www.dec.ny.gov/docs/wildlife_pdf/cwdsurplan13web.pdf. Accessed 12 Jul 2015. O’Brien, D. J., S. M. Schmitt, S. D. Fitzgerald, and D. E. Berry. 2011. Management of bovine tuberculosis in Michigan wildlife: current status and near term prospects. Veterinary Microbiology 151:179–187. O’Brien, D. J., S. M. Schmitt, S. D. Fitzgerald, D. E. Berry, and G. J. Hickling. 2006. Managing the wildlife reservoir of Mycobacterium bovis: the Michigan, USA, experience. Veterinary Microbiology 112:313–323. O’Reilly, L. M., and C. J. Daborn 1995. The epidemiology of Mycobacterium bovis infections in animals and man: a review. Tubercle and Lung Disease 76(Suppl. 1):1–46. Passler, T., S. Ditchkoff, M. D. Givens, K. V. Brock, R. W. DeYoung, and P. H. Walz. 2010. Transmission of bovine viral diarrhea virus among white-tailed deer (Odocoileus virginianus). Veterinary Research 41:20. Ruder, M. G., T. Lysyk D. Stallknecht, L. Foil, D. Johnson, C. Chase, D. Dargatz, and P. Gibbs. 2015. Transmission and epidemiology of bluetongue and epizootic hemorrhagic disease in North America: current perspectives, research gaps, and future directions. Vector-Borne and Zoonotic Diseases 15:348–363. Samuel, W., M. Pybus, D. Welch, and C. Wilke. 1992. Elk as a potential host for meningeal worm: implications for translocation. Journal of Wildlife Management 56:629–639. Sohn, H. J., J. Kim, K. Choi, J. Nah, Y. Joo, Y. Jean, S. Ahn, O. Kim, and A. Balachandran. 2002. A case of chronic wasting disease in an elk imported to Korea from Canada. Journal of Veterinary Medical Science 64:855–858. Tamguney, G., M. Miller, L. Wolfe, T. Sirochman, D. Glidden, C. Palmer, A. Lemus, S. DeArmond, and S. Prusiner. 2009. Asymptomatic deer excrete infectious prions in feces. Nature 461:529–532. Tanabe, M., R. W. Gerhold, and R. B. Beckstead. 2010. Molecular confirmation of Parelaphostrongylus tenuis infection in a horse with verminous encephalitis. Veterinary Pathology 47:759. Thorne, E. T. 2001. Brucellosis. Pages 372–396 in E. S. Williams, and I. K. Barker, editors. Infectious diseases of wild mammals. Third edition. Iowa State Press, Ames, USA. Uilenberg, G. 1981. Heartwater disease. Pages 345–360 in M. Ristic, and I. McIntyre, editors. Diseases of cattle in the tropics: economic and zoonotic relevance. Martinus Nijhoff, London, England, United Kingdom. Uilenberg, G. 1982. Experimental transmission of Cowdria ruminantium by the Gulf coast tick, Amblyomma maculatum: danger of introducing
Gerhold and Hickling
Disease Risks from Captive Cervids
heartwater and benign African theilerisosis onto the American mainland. American Journal of Veterinary Research 43:1279–1282. United States Animal Health Association. 2009. Epizootic hemorrhagic disease. Report of the Committee on Wildlife Diseases. United States Animal Health Association. http://www.usaha.org/Portals/6/Reports/ 2009/report-wd-2009.pdf. Accessed 12 Jul 2015. United States Department of Agriculture’s Animal and Plant Health Inspection Services [USDA APHIS]. 2014. Chronic wasting disease program standards. https://www.aphis.usda.gov/animal_health/animal_ diseases/cwd/downloads/cwd_program_standards_2014.pdf. Accessed 12 Jul 2015. United States Department of Agriculture’s Animal and Plant Health Inspection Services [USDA APHIS]. 2015. Interstate transportation requirements for wild caught cervids. https://www.aphis.usda.gov/ animal_health/animal_diseases/cwd/downloads/interstate_ transportation_ requirements_for_wild_caught_cervids.pdf. Accessed 15 Feb 2016. van Campen H., K. Frolich, and M. Hofman. 2001. Pestivirus infections. Pages 232–244 in E. S. Williams, and I. K. Barker, editors. Infectious diseases of wild mammals. Third edition. Iowa State Press, Ames, USA. Walsh, D. P., editor. 2012. Enhanced surveillance strategies for detecting and monitoring chronic wasting disease in free-ranging cervids. U.S. Geological Survey Open-File Report 2012-1036. http://pubs.usgs.gov/of/ 2012/1036/. Accessed 22 Feb 2016. Williams, E. S. 2005. Chronic wasting disease. Veterinary Pathology 42:530–549. Whitehead, C. E., and D. Bedenice. 2009. Neurologic diseases in llamas and alpacas. Veterinary Clinics of North America: Food Animal Practice 25:385–405. Wisconsin Department of Natural Resources. 2002. Summary of a statewide audit and inspection of Wisconsin’s captive white-tailed deer farms. Wisconsin Department of Natural Resources. http://www.cwd-info.org/ pdf/DeerFarmAudit.pdf. Accessed 15 Jul 2015. Wisconsin Department of Natural Resources. 2006. An evaluation: chronic wasting disease. Wisconsin Department of Natural Resources Report 06-13. http://legis.wisconsin.gov/lab/reports/06-13full.pdf. Accessed 15 Jul 2015. Wray, C. 1975. Survival and spread of pathogenic bacteria of veterinary importance within the environment. Veterinary Bulletin 45:543–550.
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