PERSPECTIVE DOI: 10.7589/2014-06-167

Journal of Wildlife Diseases, 51(3), 2015, pp. 543–554 # Wildlife Disease Association 2015

TUBERCULOSIS AND BRUCELLOSIS IN WOOD BISON (BISON BISON ATHABASCAE) IN NORTHERN CANADA: A RENEWED NEED TO DEVELOP OPTIONS FOR FUTURE MANAGEMENT Todd K. Shury,1,5 John S. Nishi,2 Brett T. Elkin,3 and Gary A. Wobeser4 1 Parks Canada Agency, 52 Campus Dr., Saskatoon, Saskatchewan S7N 5B4, Canada 2 EcoBorealis Consulting Inc., Box 39, Site 2, RR1, Millarville, Alberta T0L 1K0, Canada 3 Department of Environment and Natural Resources, Government of the Northwest Territories, 5102-50th Ave., Yellowknife, Northwest Territories X1A 3S8, Canada 4 Department of Veterinary Pathology, Western College of Veterinary Medicine, 52 Campus Dr., Saskatoon, Saskatchewan S7N 5B4, Canada 5 Corresponding author (email: [email protected]) ABSTRACT: Effective, long-term strategies to manage the threat of bovine tuberculosis and brucellosis spillback from northern, diseased bison to the Canadian cattle herd and adjacent disease-free wood bison (Bison bison athabascae) herds have eluded policy makers in recent decades. A controversial plan to depopulate infected herds and repopulate them with diseasefree wood bison was rejected in 1990 because of significant public concern. Since then, technical advances in vaccine technology, genetic salvage, selective culling, and diagnostic test development have occurred. Containment strategies to reduce further spread of these diseases are a necessary first step; recent progress has been made in this area, but challenges remain. This progress has produced more options for management of these herds in northern Canada, and it is time to consider wood bison conservation and long-term disease eradication as equally important goals that must satisfy concerns of conservation groups, agriculture sectors, aboriginal groups, and the general public. Management of wildlife disease reservoirs in other areas, including Yellowstone and Riding Mountain national parks, has demonstrated that effective disease management is possible. Although combinations of different strategies, including vaccination, genetic salvage techniques, and selective culling, that use sensitive and specific diagnostic tests may offer alternatives to depopulation/repopulation, they also have logistic constraints and cost implications that will need consideration in a multistakeholder, collaborative-management framework. We feel the time is right for this discussion, so a longterm solution to this problem can be applied. Key words: Brucellosis, disease management, tuberculosis, wood bison, Wood Buffalo National Park.

that time. The greatest current risk is that the diseases will infect nearby uninfected wood bison (Bison bison athabascae) herds reintroduced as part of national recovery efforts during the past 30 yr (Nishi et al. 2006; Wobeser 2009). Perspectives and views differ not only on the significance of the two diseases but also on how to ultimately manage them, leading to ongoing conflict, which precluded meaningful resolution (Pybus and Shury 2012). Efforts to integrate science, policy, and societal values and perspectives were attempted numerous times, but a longterm solution leading to the eradication of the two diseases remains elusive. A proposal by

BACKGROUND

Bovine tuberculosis (bTB; caused by Mycobacterium bovis) and brucellosis (caused by Brucella abortus) have been present within bison (Bison bison) populations in northern Canada since the 1920s, when the causative organisms were translocated along with infected plains bison (Bison bison bison) from Buffalo National Park, Wainwright, Alberta, Canada (Fuller 2002; Brower 2008). Effective strategies for eradicating these exotic bovine diseases in large, free-ranging bison populations have eluded policy makers, biologists, veterinarians, concerned citizens, and local communities since 543

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the Canadian Federal Environmental Assessment Review Office (FEARO) to depopulate infected wood bison herds and replace them with disease-free herds in 1990 was rejected because of significant public opposition (Connelly et al. 1990; McCormack 1992; Nishi et al. 2006). Since the FEARO panel recommendation, there have been many scientific and technical advances in disease ecology, vaccine technology, diagnostic testing, genetic salvage techniques, reproductive technologies, and understanding of immune responses to bTB and brucellosis in wildlife species. We highlight relevant scientific and technical advances that may influence disease-management strategies for bTB and brucellosis and propose a path forward for discussion of future management options. We suggest that effective control and containment of these two diseases in northern populations of wood

bison in the short term is a necessary, prior step for successful disease management and eventual eradication. Some containment measures are recent, whereas others have existed for decades, but little or no serious consideration has been given to how these exotic bovine diseases might ultimately be managed or potentially eradicated using options other than depopulation. OVERVIEW OF CURRENT DISEASEMANAGEMENT ACTIVITIES

Currently, infected bison in northern Canada are confined to subpopulations within Wood Buffalo National Park (WBNP) and the adjacent populations along the Slave River lowlands in the Northwest Territories (Fig. 1; Gates et al. 2010; Nishi 2010), and one recently confirmed B. abortus–infected herd

FIGURE 1. Location of diseased and nondiseased wood bison (Bison bison athabascae) herds and associated management areas in northern Canada.

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southwest of WBNP (Government of Alberta 2013). Other free-ranging bison herds in northern Canada (Mackenzie, Ronald Lake, and Hay-Zama) appear free of the two diseases, based on testing in those herds (Tessaro et al. 1993; Wobeser 2009; Government of the Northwest Territories unpubl. data; Government of Alberta 2011, 2013). A 39,000-km2 Bison Control Area (BCA) established northwest of WBNP in 1987 by the Government of the Northwest Territories (and jointly funded with Parks Canada since 1992) to act as a bison-free area and aerial surveillance zone (Nishi et al. 2002b) is the only major disease-management measure that was actively pursued consistently during the past 27 yr. A formal assessment of the BCA program is underway to evaluate and enhance its effectiveness in managing the risk of individuals or small groups of bison moving between the Mackenzie and WBNP populations. The province of Alberta recently proposed a similar buffer zone, using active surveillance to locate and test bison on the southwest side of WBNP, to confirm the disease status of smaller bison herds in the area and as part of Alberta’s strategy to actively manage distribution and abundance of bison from the Hay-Zama herd (Government of Alberta 2011, 2013). Parks Canada initiated a Bison Research and Containment Program in 1995, which funded studies on the prevalence, distribution, and ecologic effects of the two diseases within the WBNP (Gates et al. 2001; Joly and Messier 2005). Funding for this program was discontinued in 2003, despite recommendations for its continuation (Nishi et al. 2006). Canada’s cattle (Bos taurus) are surveyed at slaughter to maintain confidence in their freedom from brucellosis, and there has also been ongoing, targeted serosurveillance at cattle auction markets in northern British Columbia and Alberta (Canadian Food Inspection Agency [CFIA] 2011). No B. abortus cases in cattle have been detected since 1989 (K. Howden, CFIA

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pers. comm.) despite the longevity and rigor of this program. Slaughter surveillance for bTB in domestic cattle and bison is conducted at Canadian federally regulated slaughter plants, with cases found in British Columbia in 2007 and 2011 (CFIA 2012). Despite these sporadic cases, Canada’s domestic herds are officially considered free of bTB and brucellosis. Bison populations within WBNP generally increased during the past 20 yr (Gates et al. 2010), with current estimates of approximately 4,500 bison in the greater WBNP region (Parks Canada & Government of the Northwest Territories [GNWT] unpubl. data) despite being infected with bTB and brucellosis. The Hay-Zama herd in northwestern Alberta expanded until 2008, when a limited entry hunt was instituted to control the distribution and size of the population and to reduce the risk of contact with diseased bison populations to the east. Aerial surveys indicate that the Mackenzie bison herd declined from around 2,000 individuals in 2000 to approximately 714 individuals in 2013, most recently, because of a large anthrax outbreak in 2012 (GNWT unpubl. data). Risk assessment identified the risk was greatest for recovered, freeranging wood bison herds becoming diseased from both bovine bTB and brucellosis compared with domestic cattle and bison (CFIA 1999). That assessment plus concerns regarding increased bison herds and numbers of cattle in northern Alberta led to concern that the risk of disease transmission has also increased, leading to a revision of disease-risk assessment data by the CFIA (R. Morley pers. comm.). POTENTIAL OPTIONS FOR FUTURE MANAGEMENT

Because of the FEARO panel recommendation to depopulate and repopulate infected wood bison herds (Connelly et al. 1990), policy focus and discussion centered almost exclusively around that one option (Shury et al. 2006), which was controversial and divisive (Nishi et al.

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2006; Pybus and Shury 2012). There was limited discussion of alternative management strategies among wildlife management agencies until recently. If an environmental assessment process was to occur now, the recommended approach might be different because of recent, major scientific/technical advances. Most bison management agencies in Canada agree that disease eradication is a desirable, long-term goal for bison conservation, but the technical options of how to accomplish that have not been well reviewed. We discuss these potential options in detail in the following sections. Genetic salvage options

Wood bison in the greater WBNP region are the most genetically diverse wood bison population in existence (Wilson and Strobeck 1999). Other nondiseased wood bison populations were salvaged directly or indirectly from WBNP and, consequently, were subject to a founder effect resulting in comparatively less genetic diversity (Wilson and Strobeck 1999; McFarlane et al. 2006). Genetic diversity is important for conservation for the long term because it allows populations to be resilient and to adapt to changing future conditions (Wilson et al. 2003, 2005). Indeed, a key recommendation from the FEARO panel was to conduct genetic salvage in conjunction with removal of diseased bison in and around WBNP to reintroduce genetically representative bison (Connelly et al. 1990). Experience developed through liveanimal salvage programs also increased understanding and confidence in methods for salvaging nondiseased wood bison from infected populations. A test and removal program was successfully instituted in state lands surrounding Yellowstone National Park (US), in which bison with brucellosis were either removed or sent back to the park (Treanor et al. 2011). The Hook Lake Wood Bison Recovery Project (HLWBRP) in the Northwest Territories (Canada) demonstrated that young calves can be

salvaged successfully and remain free from brucellosis, but that additional quarantine techniques would be required for successful salvage of tuberculosis-infected bison (Nishi et al. 2001, 2002a). Calves (2 wk old) were captured from infected herds near WBNP, bottle raised, and subjected to repeated testing. Brucellosis was never discovered in the salvaged herd, but following a single, confirmed case of bTB, in a subadult bull, during a routine slaughter and necropsy in March 2005 (LutzeWallace et al. 2006), epidemiologic investigation and herd depopulation revealed 13 additional cases (Himsworth et al. 2010b). Latent infection in a founder female captured in 1996 was likely responsible for infecting the salvaged herd (Himsworth et al. 2010b). Additional quarantine procedures and newer serologic tests for bTB may have detected this animal much earlier, preventing subsequent infections (Himsworth et al. 2010a). During the depopulation phase of the HLWBRP, a pilot project was conducted to investigate the feasibility of harvesting germplasm and ova from mature wood bison (Thundathil et al. 2007). Recently, further techniques for salvaging semen from the caudal epididymis of harvested, male wood bison for cryopreservation of semen for use in artificial insemination were completed (Aurini et al. 2009; Krishnakumar et al. 2011; Pegge et al. 2011). Concurrent research on development and feasibility of advanced reproductive techniques for wood bison were undertaken and were very successful. The reproductive cycle of female wood bison is well described, leading to techniques for successful embryo transfer and manipulation of the reproductive cycle to allow superovulation and artificial insemination (McCorkell 2008, 2010; Adams et al. 2010; Palomino et al. 2010, 2011, 2012). These techniques could be used in the field to salvage valuable genetic diversity of wood bison in diseased herds if depopulation or targeted removal of infected herds or individuals was considered a potential future

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option. Advanced reproductive technologies could have a key role in conserving genetic diversity from depopulated bison and establishing new, or augmenting existing, diseasefree herds. Vaccine development

Progress has been made in the past decade in understanding the immune response to various Brucella spp. and M. bovis antigens. Before 1990, there were few, if any, vaccine options for use in bison for either pathogen. Since then, DNA vaccines have shown some efficacy in laboratory animals (Lima et al. 2003; Pan et al. 2003; Nor and Musa 2004; Rhee et al. 2004; Luo et al. 2006a, b; Li et al. 2008; Mir et al. 2009; Silva et al. 2009; Lee et al. 2010), cattle, and bison (Clapp et al. 2011). Combined bTB and brucellosis vaccines are more efficacious than either vaccine component alone in cattle (Hu et al. 2009a, b, 2010). Similarly, there is progress in modeling different brucellosis vaccine strategies in Yellowstone National Park (Treanor et al. 2010; White et al. 2011) and in vaccine-delivery mechanisms, including injectable (Denisov et al. 2010) and oral plant-based formulations (Musiychuk et al. 2005; Rigano et al. 2006; Streatfield 2006; Floss et al. 2010). Plant-based, purified, subunit vaccines could potentially be applied in forage crops, such as alfalfa or clover, for mass vaccination delivery to freeranging bison herds (Rigano et al. 2006). Further research is required to implement these combinations, but the basic science to allow such novel applications is well established. Delivery of any vaccine to wild populations poses significant challenges, including what proportion of the population to vaccinate, how often to vaccinate, and how to deliver vaccines without compromising their efficacy. In the 1960s, bison in WBNP were hazed into corral capture pens and vaccinated to protect against anthrax (Tessaro 1989), but those roundups incurred significant bison mortality, and it is likely that oral vaccines or remotely delivered vaccines would be more widely

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acceptable and logistically realistic over such a large geographic area. Regardless, significant challenges still face any vaccination program in free-ranging bison. Oral bTB vaccines, with live bacille Calmette-Gue´rin (BCG) strain of M. bovis, were developed and tested for brush-tailed possums (Trichosurus vulpecula), European badgers (Meles meles), and wild boar (Sus scrofa) and are currently being tested in field trials to determine efficacy and usefulness in reducing bTB in wildlife reservoirs (Cross et al. 2007, 2009; Corner et al. 2010; Buddle et al. 2011). Thus, development of an oral or injectable vaccine for bTB or brucellosis in bison is a real possibility but will require further speciesspecific research. Other countries, realizing the benefits of vaccine development as a viable tool for managing bTB, are investing targeted resources to that end (Gortazar and Boadella 2014; Sheridan 2014) with effective vaccines developed in a 5–10-yr time frame for European badgers and brush-tailed possums. Potential also exists for vaccination against other important bison diseases, such as anthrax (Koya et al. 2005; Gorantala et al. 2011). Diagnostic test development

The caudal fold tuberculin test is the standard, live-animal diagnostic test for bTB currently in use in North America, even though few studies have documented its effectiveness in bison. Based on a few (n518) experimentally infected bison, sensitivity estimates range from 66%, using old type tuberculin, to 100%, using purifiedprotein derivative tuberculin (Thoen et al. 1988; Tessaro 1989). Evidence from captive cervid herds in Nebraska (US) demonstrate that skin tests do not perform well in some noncattle species (Waters et al. 2011), and validation studies to determine optimal screening and confirmatory tests are needed for bison. The caudal fold test is not sufficiently sensitive to detect all clinical cases of bTB in bison, and newly developed serologic tests may be more sensitive (Himsworth et al. 2010a). Several serologic

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tests for bTB, including the Cervid TB StatPakTM (Chembio Diagnostics Ltd, Medford, New York, USA), EnferPlex TB AssayTM (Enfer Group, Kildare, Ireland), and IDEXX TB AssayTM (IDEXX Laboratories, Westbrook, Maine, USA), were developed for cattle and cervids (Lyashchenko et al. 2000; Whelan et al. 2008, 2010; O’Brien et al. 2009; Buddle et al. 2010; Schiller et al. 2010; Clegg et al. 2011), but few, if any, are validated for bison. c-Interferon assays also have broad utility in cattle testing, but little work has been performed in bison (Schiller et al. 2010), although these tests were useful in African buffalo (Syncerus caffer; Michel et al. 2011). Combinations of cell-mediated tests and serologic tests offer optimal sensitivity for diagnosis of bTB in most wildlife species (Lyashchenko et al. 2008; Buddle et al. 2009, 2010; Chambers et al. 2009; Drewe et al. 2009), and that may apply to bison as well. Importantly, tests for differentiating infected from vaccinated animals were developed in cattle and could be adapted for use in free-ranging bison (Vordermeier et al. 2009; Jones et al. 2012; Waters et al. 2012). Selective culling (test and removal)

New diagnostic tests for bTB and the potential to combine diagnostic tests into a single format may improve potential for an effective test-and-removal program in bison. The caudal fold test requires animals be held or recaptured within 72 h of tuberculin injection, making it impractical for field use in wildlife populations (de Lisle et al. 2002). The 1990 FEARO report rejected ‘‘identification of diseased animals’’ as a potential option because of the logistic problems associated with holding animals and poor sensitivity of existing tests (Connelly et al. 1990). Selective removal of M. bovis– infected elk (Cervus canadensis) and whitetailed deer (Odocoileus virginianus), in Riding Mountain National Park, Manitoba, using a combination of blood-based assays successfully reduced prevalence in this wildlife reservoir (Shury and Bergeson

2011; Shury et al. 2014). Similar approaches were successful in limiting the spread of bTB in forest buffalo in South African national parks (de Garine-Wichatitsky et al. 2010). Combinations of different strategies, whereby animals positive for M. bovis or B. abortus are removed and test-negative animals are vaccinated to provide protection against future exposure, should be explored further to develop a feasible option for disease management in wild bison populations. Bison can be captured individually through helicopter net-gunning and darting (Joly and Messier 2004), and a range of mass-capture techniques exist that could be used to capture bison (Haigh 1999). Although these options are expensive and logistically challenging in such a large geographic area, they may be much more socially acceptable than depopulation. DISCUSSION AND CONCLUSIONS

In a recent review on tuberculosis in wildlife in Canada, Wobeser (2009, p. 1175) stated that one of the main reasons that management of bTB in wildlife is considerably more challenging than in domestic livestock is because: ‘‘While there may be general support for the principle of tuberculosis eradication, there may be less support for specific methods; and it is inherently difficult to reduce populations of many wild species, or to maintain them at low density, without using methods that have low public acceptance. Management of disease may involve risks to biodiversity and ecological integrity that are unacceptable to large segments of society.’’ Garnering and maintaining social license to undertake wildlife-management actions that involve culling or depopulation was one of the major roadblocks in finding a solution to the northern diseased-bison issue during the past two decades. Recent experience with pilot trials that relied on culling of European badgers to help control bovine tuberculosis in the UK provides a real example of this phenomenon (Jones

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et al. 2013; Munro 2013; Whitehead 2013; Woolhouse and Wood 2013). Opinions differ on whether management is even required for bTB and brucellosis in wood bison populations, and the only option seriously considered to date is mass culling, something that modern urban societies often find unacceptable (Carter et al. 2009). This created an impasse to the discussion of alternative methods and hampered serious attempts at building bridges among disparate government agencies and stakeholder groups with different goals (Nishi et al. 2006). Diseased bison in the greater WBNP region exist in a remote and expansive wilderness area, so diseasemanagement options require significant dedicated resources and time, as well as ongoing social and political support. We suggest that the time has come for a thorough technical review and evaluation of risks and options and for a collaborative management process to resolve the northern diseased-bison issue in a comprehensive, inclusive manner that will establish long-term goals and objectives with broad societal acceptance. To achieve meaningful resolution, it will be necessary to consider and balance objectives for wood bison conservation and long-term disease eradication. Conservation of wood bison requires development and implementation of specific, long-term strategies that address the potential for spillover of M. bovis and B. abortus into established, nondiseased wood bison populations as well as spillback to cattle and commercial bison herds. Current control strategies, such as the BCA and the Alberta Wood Bison Management Strategy, are designed to prevent spread of the two diseases into nondiseased wood bison herds in the Northwest Territories and cattle in Alberta, respectively. However, that may be insufficient over the long term, especially if diseased wood bison herds continue to grow and more land is developed for cattle grazing in northern Alberta. To date, the two diseases do not appear to have spread between infected and noninfected bison herds in the Northwest Territories.

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The HLWBRP demonstrated that liveanimal salvage from herds with brucellosis (and tuberculosis with improvements in diagnostic testing) is possible and feasible, and the Yellowstone Interagency Brucellosis Management Plan demonstrated that disparate groups can eventually come together with a common set of goals and objectives toward disease management. Successful management of bTB in wild cervids around Riding Mountain National demonstrated that sustained multiagency disease management is both possible and successful with sustained vision and funding (Shury and Bergeson 2011). With enough vision and foresight, we believe that Canada can avoid being forced into an uncomfortable compromise by the legal system, as happened with the brucellosis issue and bison and elk in the US. The HLWBRP demonstrated that community involvement and a structured approach to disease management can be successful in dealing with brucellosis, but more-stringent disease-control practices are required for elimination of bTB (Himsworth et al. 2010b). There is strong evidence that bison are currently the only wildlife reservoir of M. bovis and B. abortus in northern Canada (Shury et al. 2006; Wobeser 2009), making eradication of these two pathogens a realistic objective without compromising the ecological integrity of northern ecosystems. This is in contrast to other parts of the world where multiple species are potential reservoirs of B. abortus (Kriek 2006; Zanella et al. 2008). Technical and scientific advances in recent decades improve the feasibility of management strategies that involve combinations of vaccination, selective culling, and genetic salvage. We hope this article acts as a catalyst to begin a renewed, inclusive process to explore and address the northern diseased-bison issue in a responsible discussion of realistic alternatives using a collaborative, adaptive-management framework. There is sufficient scientific and technical knowledge on various management options

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to inform and develop achievable objectives for decision makers. What is needed next is a long-term commitment for meaningful engagement of governments (federal, provincial, and territorial), aboriginal organizations, local communities, and agricultural and environmental organizations to prioritize management objectives and coordinate and implement achievable disease-management actions. Important first steps will be to inform public understanding of northern diseased bison and better address social acceptance of different options. Although these options require further research and development before being field ready, they should not be prematurely dismissed because they may eventually lead to effective and socially acceptable disease-management strategies. Management strategies grounded in the best available science are necessary to break the impasse in the status quo, which has centered on the socially controversial recommendation to remove herds infected with M. bovis and B. abortus in and around WBNP and to replace them with nondiseased wood bison. Our main point is that an option focused only on depopulation and repopulation will be mired in controversy and is unlikely to have the social license to proceed, so it is time to consider a wider range of options that might be feasible, instead of dwelling on one that is not. LITERATURE CITED Adams GP, McCorkell RB, Jurgielewicz VC, Ambati D, Woodbury MR. 2010. Estrous synchronization and fixed-time AI in wood bison (Bison bison athabascae). Reprod Fertil Dev 22:255–255. Aurini LC, Whiteside DP, Elkin BT, Thundathil JC. 2009. Recovery and cryopreservation of epididymal sperm of plains bison (Bison bison bison) as a model for salvaging the genetics of wood bison (Bison bison athabascae). Reprod Domest Anim 44:815–822. Brower J. 2008. Lost tracks: Buffalo National Park, 1909–1939. AU Press, Edmonton, Alberta, Canada, 184 pp. Buddle BM, Livingstone PG, De Lisle GW. 2009. Advances in ante-mortem diagnosis of tuberculosis in cattle. N Z Vet J 57:173–180.

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Submitted for publication 11 June 2014. Accepted 4 February 2015.