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Revisiting Brucellosis in the Greater Yellowstone Area (2017)

Chapter: 10 Overall Findings, Conclusions, and Recommendations

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Suggested Citation:"10 Overall Findings, Conclusions, and Recommendations." National Academies of Sciences, Engineering, and Medicine. 2017. Revisiting Brucellosis in the Greater Yellowstone Area. Washington, DC: The National Academies Press. doi: 10.17226/24750.
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Suggested Citation:"10 Overall Findings, Conclusions, and Recommendations." National Academies of Sciences, Engineering, and Medicine. 2017. Revisiting Brucellosis in the Greater Yellowstone Area. Washington, DC: The National Academies Press. doi: 10.17226/24750.
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Suggested Citation:"10 Overall Findings, Conclusions, and Recommendations." National Academies of Sciences, Engineering, and Medicine. 2017. Revisiting Brucellosis in the Greater Yellowstone Area. Washington, DC: The National Academies Press. doi: 10.17226/24750.
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Suggested Citation:"10 Overall Findings, Conclusions, and Recommendations." National Academies of Sciences, Engineering, and Medicine. 2017. Revisiting Brucellosis in the Greater Yellowstone Area. Washington, DC: The National Academies Press. doi: 10.17226/24750.
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Suggested Citation:"10 Overall Findings, Conclusions, and Recommendations." National Academies of Sciences, Engineering, and Medicine. 2017. Revisiting Brucellosis in the Greater Yellowstone Area. Washington, DC: The National Academies Press. doi: 10.17226/24750.
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Suggested Citation:"10 Overall Findings, Conclusions, and Recommendations." National Academies of Sciences, Engineering, and Medicine. 2017. Revisiting Brucellosis in the Greater Yellowstone Area. Washington, DC: The National Academies Press. doi: 10.17226/24750.
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Suggested Citation:"10 Overall Findings, Conclusions, and Recommendations." National Academies of Sciences, Engineering, and Medicine. 2017. Revisiting Brucellosis in the Greater Yellowstone Area. Washington, DC: The National Academies Press. doi: 10.17226/24750.
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Suggested Citation:"10 Overall Findings, Conclusions, and Recommendations." National Academies of Sciences, Engineering, and Medicine. 2017. Revisiting Brucellosis in the Greater Yellowstone Area. Washington, DC: The National Academies Press. doi: 10.17226/24750.
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Suggested Citation:"10 Overall Findings, Conclusions, and Recommendations." National Academies of Sciences, Engineering, and Medicine. 2017. Revisiting Brucellosis in the Greater Yellowstone Area. Washington, DC: The National Academies Press. doi: 10.17226/24750.
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Suggested Citation:"10 Overall Findings, Conclusions, and Recommendations." National Academies of Sciences, Engineering, and Medicine. 2017. Revisiting Brucellosis in the Greater Yellowstone Area. Washington, DC: The National Academies Press. doi: 10.17226/24750.
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Suggested Citation:"10 Overall Findings, Conclusions, and Recommendations." National Academies of Sciences, Engineering, and Medicine. 2017. Revisiting Brucellosis in the Greater Yellowstone Area. Washington, DC: The National Academies Press. doi: 10.17226/24750.
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Suggested Citation:"10 Overall Findings, Conclusions, and Recommendations." National Academies of Sciences, Engineering, and Medicine. 2017. Revisiting Brucellosis in the Greater Yellowstone Area. Washington, DC: The National Academies Press. doi: 10.17226/24750.
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Suggested Citation:"10 Overall Findings, Conclusions, and Recommendations." National Academies of Sciences, Engineering, and Medicine. 2017. Revisiting Brucellosis in the Greater Yellowstone Area. Washington, DC: The National Academies Press. doi: 10.17226/24750.
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Suggested Citation:"10 Overall Findings, Conclusions, and Recommendations." National Academies of Sciences, Engineering, and Medicine. 2017. Revisiting Brucellosis in the Greater Yellowstone Area. Washington, DC: The National Academies Press. doi: 10.17226/24750.
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Suggested Citation:"10 Overall Findings, Conclusions, and Recommendations." National Academies of Sciences, Engineering, and Medicine. 2017. Revisiting Brucellosis in the Greater Yellowstone Area. Washington, DC: The National Academies Press. doi: 10.17226/24750.
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Suggested Citation:"10 Overall Findings, Conclusions, and Recommendations." National Academies of Sciences, Engineering, and Medicine. 2017. Revisiting Brucellosis in the Greater Yellowstone Area. Washington, DC: The National Academies Press. doi: 10.17226/24750.
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Suggested Citation:"10 Overall Findings, Conclusions, and Recommendations." National Academies of Sciences, Engineering, and Medicine. 2017. Revisiting Brucellosis in the Greater Yellowstone Area. Washington, DC: The National Academies Press. doi: 10.17226/24750.
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10 Overall Findings, Conclusions, and Recommendations 1. WHAT’S NEW SINCE 1998? Since the 1998 National Research Council (NRC) report Brucellosis in the Greater Yellowstone Area, 22 cattle herds and 5 privately-owned bison herds in the three Greater Yellowstone Area (GYA) states (Idaho, Montana, and Wyoming) have been infected with Brucella abortus. During the same time period, all other states in the United States achieved and maintained brucellosis class-free status. A 2010 interim rule to regionalize brucellosis control enabled the three GYA states to create designated surveil- lance areas (DSAs) to monitor brucellosis in specific zones and to reduce the economic impact for non- affected zones. However, brucellosis has expanded beyond the original DSAs, requiring outward adjust- ment of DSA boundaries. The increase in cattle infections in the GYA, coupled with the spread in wild- life, has been alarming for producers in the area; moreover, the risk of additional spread from movement of GYA livestock to other areas across the United States is increasing due to the lack of guidance and surveillance, with the potential for spread and significant economic impact outside the GYA. In tracing the genetic lineage of Brucella across the ecosystem and among species, elk are now rec- ognized as a primary host for brucellosis and have been found to be the major transmitter of B. abortus to cattle. All recent cases of brucellosis in GYA cattle are traceable genetically and epidemiologically to transmission from elk, not bison. This is one of the most significant changes in our understanding of bru- cellosis epidemiology in the GYA since 1998. The seroprevalence of brucellosis in elk in some regions has been increasing from what were historically low levels, and data strongly suggest that elk are able to maintain brucellosis infection within populations that have limited to no direct contact with the feed- grounds or with infected bison. Direct contact of elk with cattle is more prevalent than contact of cattle with bison. As a result, the risk of transmission events from elk to cattle may be increasing. In contrast, there have been no cases of transmission from GYA bison to cattle in the 27 herds in- fected with brucellosis since 1998 despite no change in the seroprevalence of brucellosis in bison. This is likely a result of bison management practices outlined in the Interagency Bison Management Plan (IBMP) combined with fewer cattle operations in the GYA region where bison leave Yellowstone National Park (YNP). The 1998 NRC report made eight recommendations for addressing control of brucellosis in the GYA by focusing primarily on reducing the risk of transmission from bison to cattle. The potential for progress in reducing the spread of brucellosis was based in part on the assumption that elk were incapable of maintaining brucellosis in the GYA population without transmission that occurs among elk in feed- grounds or from bison to elk within the ecosystem. As noted above, the scientific evidence no longer sup- ports that assumption, as the current drivers of the spread of B. abortus in the region have changed. Ecological changes within the GYA since 1998 have shifted the dynamics of wildlife populations. The reintroduction of wolves and increases in grizzly bear numbers have impacted the density and distri- bution of elk. Elk populations have expanded on the periphery of the GYA but have decreased inside YNP. The rising number of private landowners has changed how land is used around national parks, with private lands increasingly serving as refugia for elk from hunting. With elk now viewed as the primary source for new cases of brucellosis in cattle and domestic bison, the committee concludes that brucellosis control efforts in the GYA will need to sharply fo- Prepublication Copy—Subject to Further Editorial Revision 169

Revisiting Brucellosis in the Greater Yellowstone Area cus on approaches that reduce transmission from elk to cattle and domestic bison (Conclusion 1). Managing wild bison within YNP and in the surrounding private and public lands to reduce the risk of transmission of B. abortus to domestic cattle and domestic bison has been a joint effort by the National Park Service, U.S. Department of Agriculture (USDA), tribal members, and the three states that border YNP. These efforts have been successful. In the committee’s view, a similarly unified effort is now essen- tial to reduce transmission between elk and livestock. As noted above, infected elk populations are ex- panding beyond the traditionally accepted boundaries of the GYA. There is significant risk of brucellosis spreading beyond the GYA because of the uncertainty in locating infected elk and the lack of information about factors that predispose certain cattle operation to B. abortus. In addition, unlike with cattle and bi- son, there is no effective brucellosis vaccine for elk. These changes further complicate what was already a challenging problem in 1998. Now more than ever, there is a need to strategically address this expanding problem in a more coordinated and cost-effective way. Recommendation 1: To address brucellosis in the GYA, federal and state agencies should pri- oritize efforts on preventing B. abortus transmission by elk. Modeling should be used to character- ize and quantify the risk of disease transmission and spread from and among elk, which requires an understanding of the spatial and temporal processes involved in the epidemiology of the disease and economic impacts across the GYA. Models should include modern, statistically rigorous estimates of uncertainty. 2. ADOPTING AN ACTIVE ADAPTIVE MANAGEMENT APPROACH The GYA is a large, complex ecosystem with significant spatial variation. Because the components of the ecosystem are either directly or indirectly linked to one another, any actions that are taken to con- trol brucellosis could impact the entire ecosystem. Management actions will need to be assessed not only for their impact on reducing B. abortus transmission from wildlife to cattle and domestic bison, but also for their impact on other valued ecosystem services and their potential impact outside of the GYA. Adaptive management has been an accepted tool for managing wildlife populations for more than 30 years. Adaptive management was the subject of a recommendation in the 1998 report, but was not discussed in depth. This report provides a more detailed discussion of adaptive management and its use in brucellosis control in the GYA (see Chapter 6). Adaptive management is characterized by flexible deci- sion making and an iterative learning process for making more effective decisions. Management activities are typically conducted as hypothesis testing, the outcomes of which direct subsequent decisions and actions toward the ultimate goal. In the absence of carefully designed management actions that include experimental controls, it is difficult to determine the effectiveness of a particular practice, leading to a slower learning process. Many brucellosis management efforts implemented since the 1998 report may appear to have taken an adaptive management approach; however, those efforts have not followed the basic tenet of employing an active process. More specifically, individual management actions were not designed or established to allow for scientific assessment of effectiveness, which is a central tenet of active adaptive management. A case in point is the study of B. abortus strain 19 (S19) vaccination of feedground elk in Wyoming. WGFD is to be commended for initiating a vaccination program on feedground elk and monitoring its effect— one of the few population-level manipulations of the elk brucellosis system. The conclusion that S19 vac- cination is of marginal value in reducing seroprevalence in feedground elk (Maichak et al., 2017) has pro- vided valuable information on the cost-effectiveness of remote vaccination where elk are concentrated and tolerant of human presence. However, had the study used active adaptive management, it could have led to a faster learning process and more rapid management changes. Examples of aspects that could have been improved include the use of replicate control feedgrounds starting at the initiation of the program, continuous assessment of the program’s efficacy, periodic scientific peer-review throughout the process, and control of temporal changes through the cessation of vaccination in different groups of feedgrounds in different years. The committee recognizes the challenge in how political sensitivity and funding affects flexibility of management actions, which may have been factors impacting this case study. 170 Prepublication Copy—Subject to Further Editorial Revision

Overall Findings, Conclusions, and Recommendations Recommendation 2: In making timely and data-based decisions for reducing the risk of B. abortus transmission from elk, federal and state agencies should use an active adaptive management approach that would include iterative hypothesis testing and mandated periodic scientific assess- ments. Management actions should include multiple, complementary strategies over a long period of time, and should set goals demonstrating incremental progress toward reducing the risk of transmission from and among elk. 3. ADAPTIVE MANAGEMENT OPTIONS TO REDUCE RISK There are a variety of adaptive management options for reducing risk of transmission from wildlife to cattle and domestic bison (see Chapters 5 and 7). No single management approach can independent- ly result in reducing risk to a level that will prevent transmission of B. abortus among wildlife and domestic species (Conclusion 2). To consider any approach in isolation is to miss the bigger picture of a highly interconnected ecosystem and a broader understanding of various factors affecting risk that has evolved since 1998. Some of the most promising options along with their pros and cons are discussed below. While there are knowledge gaps that limit understanding of actual risk, the options below are possible adaptive man- agement approaches to reduce risk of B. abortus transmission and to inform future risk management plans. These approaches would need to be based on an integrated assessment of risk and costs, with prior- ities assigned based on such an assessment. However, these approaches do not necessarily need to be ap- plied uniformly over space and time. The committee acknowledges that many of these actions are the fo- cus of current management efforts. Others are either new or are adaptations of other efforts. 3.1 Population Reduction Reducing the population size of cattle, bison, or elk are all likely to reduce the risk of brucellosis transmission to cattle by reducing the area of potential contact or the number of infected individuals in those areas, even if the disease prevalence in the wildlife hosts remains constant. However, each species has a constituency that would likely oppose any population reduction. Cattle may be logistically easier to control than wildlife, but state and federal managers are unable to directly modify cattle numbers and can only change some of the incentive structures for ranchers and landowners. Bison numbers and distribution are already controlled at the boundaries of YNP, which is inconsistent with the natural regulation policy of the National Park Service. Finally, large reductions in elk populations are unlikely to be widely sup- ported (Peterson et al., 2006). Elk Reducing the elk population is an option for reducing the risk of transmission among elk, cattle, and bison. Unlike bison, transmission among elk appears to be influenced by density. Thus, reducing elk group sizes and/or density may decrease elk seroprevalence over time, and potentially decrease the risk of elk transmission (Conclusion 3). Potential management approaches for elk population reduction include the following: • Hunting. Hunting is currently used to control elk populations, with management unit population targets set as a balance of public demand and population goals. Hunting could also be used as a means of incentivizing targeted population reductions based on brucellosis risk. One option, for example, would be to increase the numbers taken by hunters to the extent possible in known high elk seroprevalence areas, particularly female elk. This option requires sufficient numbers of hunters to access those lands in a timely fashion, requires that herd seroprevalence is known, and would need to be linked to more intensive efforts to better establish seroprevalence esti- Prepublication Copy—Subject to Further Editorial Revision 171

Revisiting Brucellosis in the Greater Yellowstone Area mates. Hunter-collected elk samples, as done in Idaho and Wyoming, could also be used to in- crease information on key populations where seroprevalence is critically important or unknown (for example, at the boundary of the DSAs). Higher quotas or more intensive hunter contact ef- forts could allow increased sampling, improving the previously low return and sample quality problems. A challenge of hunting as a management option is that it is imprecise and in some cases, may be seen as undesirable by hunters on whose cooperation it depends. Animals may move, unpredictable weather may make a targeted population inaccessible to hunters during a short hunting season, and activity may disrupt herds. Hunting may also concentrate remaining elk in areas that are not accessible to hunters, such as private land where cattle are grazed, thereby promoting an overall adverse outcome. There are inadequate data to conclusively rec- ommend one or more of these options, as additional and ongoing assessments of the efficacy of these approaches would be needed as part of an active adaptive management approach. • Contraception. A second approach that targets female elk that are at higher risk of transmission during birthing events is contraception. As previously discussed in Chapter 7, GonaCon™ is an immunocontraceptive and is one option suggested for reducing prevalence in bison. Contracep- tion would need to be viewed as experimental in elk. But as noted above, early experimental re- sults in bison suggest that GonaCon™ may help in significantly reducing the elk population and prevalence of brucellosis in elk. Contraception trials in elk were underway as of the writing of this report. The results of these early trials would need to be carefully evaluated to determine whether this tool holds potential as a useful means to help control brucellosis in elk. • Test and removal. Test and removal has been an invaluable part of the brucellosis eradication program for domestic species. As with domestic species, test and removal in elk would need to be part of an integrated program combined with other tools such as quarantine, herd manage- ment to reduce intra-herd transmission, and vaccination. To determine whether this approach might be feasible for elk, a 5-year pilot study was conducted at the Muddy Creek feedground to analyze how test and removal of elk on feedgrounds might reduce seroprevalence of brucellosis. This project targeted female elk, and was able to reduce the prevalence of brucellosis from 37% to 5% during the 5 years of the project by trapping nearly half of the female elk in the feed- ground and eliminating (by humane euthanasia) serologically positive females. Discontinued af- ter 5 years, the project also demonstrated how quickly brucellosis prevalence could resurge in a population without continuing efforts. This “proof of principle” pilot project demonstrates that significant reduction of prevalence is possible in elk through test and removal of positive elk. But given the enormity of the problem in elk, the use of test and removal is limited to very spe- cialized conditions (for example, in reducing feedground density) as large populations appear to be able to maintain a brucellosis reservoir outside the feedgrounds. The logistics and cost of conducting the long-term test and removal programs required for success would be significant, even in the relative “confinement” of elk in a feedground (where they are accessible in a con- centrated population but still move freely), and with the current lack of other tools (such as vac- cination and spatial separation through quarantine) needed to ensure success. Its application will only be effective when used as one part of a comprehensive control strategy, and in isolated or otherwise confined populations of elk that can be captured, tested, held, and removed without interaction with other infected elk or bison. Further analysis would be needed to determine the costs and benefits of this approach. Bison The threat of B. abortus transmission from bison to cattle may currently not be a concern, but bison remain an important reservoir for brucellosis. Therefore, the threat of transmission from bison to elk re- mains and could represent a long-term problem if elk were cleared of the disease. The committee identi- fied the highest priority to be a focus on controlling B. abortus transmission from elk to cattle and domes- 172 Prepublication Copy—Subject to Further Editorial Revision

Overall Findings, Conclusions, and Recommendations tic bison. Further reducing the prevalence of brucellosis in bison may be desirable in the future if efforts are successful in reducing prevalence in elk. Additionally, further reducing prevalence in bison could also enhance the potential for more successful control in the future if new tools, such as an improved vaccine for bison, become available. • Removal of infected bison. Population reduction alone is not likely to reduce brucellosis preva- lence in bison since transmission is frequency dependent rather than density dependent. For this reason, if reduction of brucellosis prevalence is a goal, removal of bison for population management purposes will need to target brucellosis infected individuals, whenever possi- ble (Conclusion 4). • Quarantine and relocation. Sufficient evidence is now available to also include separation and quarantine of test negative bison as a management action, allowing for the eventual relocation of GYA bison to other bison herds (including onto tribal lands). However, there are limitations on the effectiveness of this approach toward population reduction since the time required to con- firm Brucella negative status is prolonged, the number of bison that can be relocated is not large, and relocation sites will reach maximum carrying capacity over time. • Targeted removal within Yellowstone National Park. While this option may not be politically, logistically, socially, or economically feasible, targeted removal of seropositive bison (which would be facilitated by the use of a penside assay) or high-risk bison (such as young, pregnant females) within YNP in the winter could reduce the need for large culls of bison populations that move outside YNP. This could also reduce the episodic swings in the bison population and winter emigrations from YNP that lead to large culls in some years. Additionally, any gains in reducing seroprevalence in bison could be negated by exposure of remaining bison to infected elk within YNP and in elk feedgrounds if concurrent efforts to reduce seroprevalence in elk does not occur. This is particularly important for the Jackson bison herd, for which exposure to elk on the National Elk Refuge continues to be a significant risk, and will need to be considered in bi- son control plans. However, the impact could be assessed using an active adaptive management approach. • Bison genetics. Test and removal of bison provides a valuable opportunity to preserve genetic material and live cells for future use in establishing brucellosis negative and potentially disease resistant bison through cloning techniques. • Contraception. Experimental and modeling results in bison suggest that contraception using a gonadotropin releasing hormone immunocontraceptive (i.e., GonaCon™) may help in reducing prevalence of brucellosis. This approach targets high-risk females, preventing pregnancy and thus abortion and birthing events that increase risk of transmission through shedding of high numbers of bacteria. Contraception would need to be used strategically, recognizing that popula- tion reduction (an outcome of using contraception) may not be acceptable for bison in all areas. 3.2 Feedgrounds The role of the National Elk Refuge and Wyoming elk supplemental winter feedgrounds in main- taining and propagating brucellosis in the GYA is a controversial topic. Feedgrounds have been useful for separating elk from cattle. However, it is widely accepted that the feedgrounds promote transmission of B. abortus among elk and are likely responsible for causing and maintaining elevated seroprevalence in those areas. Molecular genetic characterization of B. abortus isolates from elk, bison, and cattle indicate that Wyoming feedgrounds have the greatest diversity of B. abortus lineages, and strongly suggest that they are the initial source of infection for other elk populations in the GYA, with the exception of some isolates from the Paradise Valley in Montana. Prepublication Copy—Subject to Further Editorial Revision 173

Revisiting Brucellosis in the Greater Yellowstone Area Feedground Interventions The committee reviewed multiple experimental approaches to reduce elk seroprevalence by inter- vention in the feedgrounds. On balance, the data are not yet strong enough to make definitive conclusions on the outcome, particularly if the ultimate outcome is the reduced risk of exposure and infection rates in cattle. Decisions will need to be made that balance the short-term goals of separating elk from cattle with the long-term risk of increased infection among elk in feedgrounds. The potential options below for man- agement interventions in feedgrounds could be further evaluated using an active adaptive management approach, with the interventions applied singularly or in combination. • Balance the timing and use of feedgrounds. Data suggest that ceasing feeding earlier in the sea- son on feedgrounds to encourage dispersal would result in less risk of infection among elk (and bison where intermixing occurs), because calving of elk would occur in a more natural envi- ronment away from the dense population of elk that are present in feedgrounds. This approach would have to be balanced with appropriate management of cattle, with delayed turnout into grazing areas until the risk of exposure during elk calving is reduced, as well as consideration of habitat improvement for elk that would provide forage along migration routes and winter habitat to reduce elk-cattle contact in the absence of the feedgrounds. • Feeding patterns on feedgrounds. Data suggest that feeding in checkerboard patterns and spreading feed more broadly appear to reduce elk to elk contact, and therefore potentially reduce transmission risk. • Test and removal on feedgrounds. The Muddy Creek feedground pilot project provided an ex- ample of temporarily reducing seroprevalence of brucellosis through test and removal of infect- ed female elk. The feedgrounds offer an opportunity to work with a population of elk that is sea- sonally concentrated. This option was discussed in detail above in the “Population Reduction” section, and as previously mentioned in that section, the test and removal strategy will only be effective when used as one part of a comprehensive control strategy for brucellosis. • Contraception in elk. Also discussed above is the option of contraceptive intervention in elk. The feedgrounds provide an opportunity to more easily access female elk for contraceptive ap- plication. • Removal of aborted fetuses. Aborted placentae pose the highest risk of exposure of uninfected elk to brucellosis since the concentration of bacteria is extremely high at the time of abortion. Access to these fetuses is more limited when elk calve in the natural environment. Abortion on feedgrounds offers an opportunity to remove aborted fetuses on a daily basis and to disinfect the abortion site using an appropriate disinfectant (such as sodium hydroxide or sodium hypo- chlorite), thus reducing the likelihood of transmission to other elk. Current feedground practice includes removal of aborted fetuses when identified. However, data are not sufficient to know the impact of doing this on reduction of seroprevalence in elk, and subsequently on reducing in- fection risk for cattle over time. Managers should continue investigating methods of reducing the amount of time aborted fetuses are on the feedground, as well as the number of contacts that elk and bison (i.e., the Jackson bison herd) have with those fetuses. • Other future interventions. Given the enormity of the challenge in accessing elk in the vastness of the open West, feedgrounds offer a unique opportunity to intervene (for example, if an effec- tive elk vaccine is developed) in a relatively smaller land area where elk are concentrated and capture is easier, less dangerous for personnel, and less costly. This potential future opportunity should be weighed against the ongoing costs and benefits of maintaining the feedgrounds in an integrated socioeconomic analysis. 174 Prepublication Copy—Subject to Further Editorial Revision

Overall Findings, Conclusions, and Recommendations Incremental Closure of Feedgrounds Closure of feedgrounds appears to be an obvious approach to control brucellosis in the GYA, but there are impacts of feedground closure that will need to be considered and assessed. First, while there is still some uncertainty, scientific evidence suggests that brucellosis in elk is self-sustaining in some areas without continuous reintroduction of infected feedground elk. If future work continues to support this conclusion, it is possible that closure of feedgrounds would not have any impact on brucellosis prevalence in more remote elk populations away from the feedgrounds. Closure of feedgrounds would, however, po- tentially reduce the “seeding” of new areas with infected elk where a reservoir does not currently exist. Second, anecdotal evidence suggests that feedgrounds reduce exposure of cattle to infected elk during the high-risk period of abortion or calving. Observational data to support this notion are weak at present. Thus, an unintended outcome of closing feedgrounds could be increased exposure of cattle to infected elk if cattle are turned onto grazing areas at the time that elk are calving. Feedground closure has been the subject of increased discussion due to disease concerns in addition to brucellosis. In particular, at the time of this report, the spread of chronic wasting disease (CWD) and the distinct possibility that feedgrounds will be a primary source of transmission for many years into the future has led to more active discussions on closing of feedgrounds (the role of feedgrounds in the trans- mission of other diseases of elk was discussed in Chapter 7). Reduced use and/or strategic closing of feedgrounds may have a positive impact on elk health in general, although the data supporting the tradeoff of increased winter population loss with reduced disease impacts on overall elk population (measured, for example, in terms of number of cow-calf pairs) are unclear. The committee was not tasked to review the role of feedgrounds in propagation of CWD in elk, but notes that the concern is supported by scientific evidence. There are insufficient data available to know with certainty what the impact across the entire GYA would be of reducing the use of and possibly closing elk supplemental feedgrounds. However, the weight of evidence nonetheless suggests that reduced use or incremental closure of feedgrounds could ben- efit elk health in the long-term, and could reduce the overall prevalence of brucellosis in elk on a broad population basis (Conclusion 5). The closure of feedgrounds is likely to bring increased short-term risk due to the potential for in- creased elk-cattle contact while the seroprevalence in elk remains high. In the longer term, closing feed- grounds may result in reduced elk seroprevalence. Incremental closure of feedgrounds would enable a bioeconomic assessment to be conducted to determine both short- and long-term costs and benefits. Re- duced use or incremental closure of feedgrounds is not a stand-alone solution to control of brucello- sis in the GYA, and will need to be coupled with other management actions to address the problem at a system level (Conclusion 6). The committee endorses the long-term goal presented in the WGFD Brucellosis Management Action Plans and the USFWS/NPS elk and bison management plan for the Na- tional Elk Refuge to reduce use and/or incrementally close supplemental feedgrounds. Recommendation 3: Use of supplemental feedgrounds should be gradually reduced. A strate- gic, stepwise, and science-based approach should be undertaken by state and federal land managers to ensure that robust experimental and control data are generated to analyze and evaluate the im- pacts of feedground reductions and incremental closure on elk health and populations, risk of transmission to cattle, and brucellosis prevalence. 3.3 Spatial and Temporal Separation One of the fundamental principles of infectious disease control is spatial and temporal separation of individuals and groups to reduce the risk of transmission. This principle underlies progress made in re- ducing bison and cattle contact outside YNP as part of the IBMP. Bison management to prevent brucello- sis transmission has been successful in part due to spatial and temporal separation from cattle, both be- cause bison are largely contained within YNP and Grand Teton National Park, and when outside the parks Prepublication Copy—Subject to Further Editorial Revision 175

Revisiting Brucellosis in the Greater Yellowstone Area they are managed to reduce cattle contact. In addition, a relatively small and decreasing number of cattle are grazed close to areas where bison roam outside the park, helping to keep the risk of exposure minimal. Recommendation 4: Agencies involved in implementing the IBMP should continue to maintain a separation of bison from cattle when bison are outside Yellowstone National Park boundaries. Spatial and temporal separation plays an important role in reducing transmission risk from elk. Sep- aration of susceptible and infected animals during high-risk periods (for example, immediately prior to and following abortion and full-term birth) has been and should continue to be utilized as a risk reduction tool, and is further discussed below in the context of specific management approaches. National policy for responding to the identification of infected cattle and domestic bison herds includes time-tested approach- es toward maintaining separation of infected and susceptible animals, including hold orders and quaran- tine during follow-up testing. These actions are valuable tools for reducing risk. Other options include the timing and use of grazing allotments, biosecurity measures, and hazing of elk. Removal of bison for population management purposes could target B. abortus infected bison if further reducing the prevalence of brucellosis is a goal; however, until tools become available that would simultaneously allow for an eradication program in elk, additional aggressive control measures in bison seem unwarranted. Grazing Allotments At least 75% of the cattle herds infected since 1998 had previously grazed on or immediately adja- cent to public rangeland. Historically, reduction of B. abortus transmission risk has not been considered by agencies when making decisions about assigning grazing allotments. Case-control studies along with more frequent cattle testing would be required to more definitively link public land access to brucellosis infection risk in cattle. However, a more science-based approach in grazing allotment use could be taken to reduce risk. For example, government agencies such as the USDA Forest Service and the U.S. Depart- ment of the Interior (DOI) Bureau of Land Management could leave grazing allotments empty or modify the use and timing of grazing allotments in relation to the risk of transmission and knowledge of elk mi- gration patterns. Additionally, the formula used annually to adjust grazing fees could be changed to a risk- based, marketplace approach through legislative authorization. To do so would require an understanding of when and where the risks are higher and lower, and the development and use of a risk map that over- lays cattle and elk locations relative to the grazing allotments. Decisions should be made in consultation with state wildlife agency partners to estimate when elk are less likely to be on federal grazing allotments during the time when abortion and calving events occur, and to consider other factors that reduce the like- lihood of interactions between elk and cattle on grazing allotments. Increased knowledge of elk transmis- sion risk in grazing allotments will be critical to taking a targeted approach toward risk reduction by spa- tial and temporal separation. If delayed access is unacceptable to producers, increased fees and/or brucellosis testing prior to and after turnout on grazing allotments could be implemented. Requiring evi- dence of brucellosis calfhood and adult vaccination for grazers using higher risk lands could also be re- quired. The benefits from this approach are somewhat uncertain due to, for example, a limited under- standing of where and when cattle are getting infected (addressed later in the “Research Agenda” section). However, if designed appropriately, iterative learning through an active adaptive management approach will over time provide the data as to whether this approach is effective and worth continuing. Biosecurity Measures There are multiple biosecurity measures that individual producers can take that reduce exposure of cattle and domestic bison to B. abortus infected elk. Measures such as fencing of haystacks and delaying turnout on summer pasture until the risk of elk calving is reduced have been discussed in the report. There are adequate data to indicate these approaches can reduce exposure, and published cost-benefit analysis has provided the individual producer with sufficient information to make personal decisions. However, as previously discussed, the external impacts (externalities) of individual producer actions have not been thoroughly investigated. In general, actions taken by individual producers should be in proportion to the 176 Prepublication Copy—Subject to Further Editorial Revision

Overall Findings, Conclusions, and Recommendations risk of elk entering their property, or otherwise to the risk of their cattle making contact with elk. There is a need to approach biosecurity measures as a shared responsibility, with incentives provided to producers to implement these biosecurity measures in high-risk areas (for example, within the DSA). Hazing of Elk Hazing has been used by state wildlife agencies as a key part of the bison management plan for keeping bison and cattle separated after movement of bison outside YNP. Hazing is currently being authorized as a tool for Wyoming, but the efficacy of different hazing methods to reduce the time elk spend in contact with cattle has not been measured, and therefore the costs and benefits of hazing elk are unknown. Hazing of elk could be considered on a targeted basis in known high-risk areas. The impact of hazing in high risk areas would need to be further studied to determine if hazing was effective in prevent- ing contact between elk and cattle, or if it simply scatters elk into new locations in an unpredictable manner. 3.4 Testing, Surveillance, and Designated Surveillance Areas Regionalization is now a well-accepted approach to allow subnational disease containment without jeopardizing the disease status of an entire nation. The success of regionalization relies on robust risk as- sessment, knowledge of the location and extent of infected animals within and immediately outside the boundary of a control zone, and effective boundary management and enforcement. With the last remain- ing vestige of brucellosis limited to the GYA, the United States adopted a regionalized approach through a 2010 interim rule that required creation of DSAs within the three GYA states (Idaho, Montana, and Wyoming). This approach minimizes the economic impact of finding occasional “spillover” disease in GYA cattle and domestic bison herds, and provides a means for all three of the GYA states to be classi- fied as “free” of brucellosis. The DSA zoning concept is a valuable approach toward brucellosis control in the GYA. The successful use of DSAs is dependent on responsible and timely adjustments of DSA boundaries based on adequate surveillance, particularly of elk. There is no federal guidance for conducting wildlife surveillance outside of the DSA at a level re- quired to monitor the geographic expansion of brucellosis in elk. Each state independently conducts wild- life surveillance outside of the DSA, with no uniform data-based guidelines or requirements for states to reference in determining when to expand their DSA as a result of finding infected or exposed wildlife outside of established DSA boundaries. This lack of uniformity in rules and standards has resulted in an uneven approach to surveillance and to establishing boundaries that accurately reflect risk. No infected cattle herds have been identified outside of established DSA boundaries, an indication that the DSA con- cept is effective in preventing movement of infected livestock outside of the DSA. However, seropositive elk have been identified outside of the DSAs. It is therefore likely that cattle in the same geographic area are at risk. If DSA boundaries are not expanded in a timely manner in response to finding seropositive wildlife, there is an increased probability that exposed or infected cattle and domestic bison herds in that area may not be detected in time to prevent further spread of infection as cattle and domestic bison are marketed and moved. Further raising the risk of brucellosis spread outside the DSAs is a gap in slaughter surveillance for non-DSA cattle in the GYA states. There is no major slaughter capacity in Montana or Wyoming where surveillance samples can be collected to detect whether brucellosis has expanded in cattle beyond the DSA boundaries. In addition, the current national brucellosis slaughter surveillance program is not de- signed specifically to address the increased surveillance needs in the GYA or associated states. This gap in slaughter surveillance for non-DSA cattle in the three GYA states further raises the risk of brucellosis spreading beyond the DSAs. Lastly, USDA Animal and Plant Health Inspection Service (APHIS) has not reviewed Brucellosis Management Plans for GYA states since 2012. Prepublication Copy—Subject to Further Editorial Revision 177

Revisiting Brucellosis in the Greater Yellowstone Area The lack of data-based guidance and uniformity in conducting wildlife surveillance outside the DSA, the absence of a GYA focused approach for national surveillance, and the infrequent over- sight of state brucellosis management plans has created an increased risk for spread of brucellosis in cattle and domestic bison outside the DSA boundaries and beyond the GYA (Conclusion 7). The impact of brucellosis spread could be substantial. Recommendation 5: In response to an increased risk of brucellosis transmission and spread beyond the GYA, USDA-APHIS should take the following measures: 5A: Work with appropriate wildlife agencies to establish an elk surveillance program that uses a modeling framework to optimize sampling effort and incorporates multiple sources of uncertainty in observation and biological processes. 5B: Establish uniform, risk-based standards for expanding the DSA boundaries in response to finding seropositive wildlife. The use of multiple concentric DSA zones with, for example, different surveillance, herd management, biosecurity, testing, and/or movement requirements should be con- sidered based on differing levels of risk, similar to current disease outbreak response approaches. 5C: Revise the national brucellosis surveillance plan to include and focus on slaughter and market surveillance streams for cattle in and around the GYA. 3.5 Vaccination Vaccination is a time-tested, proven method of infectious disease control. Brucellosis vaccination has been an important part of the program to eradicate brucellosis from domestic cattle, and is effective when used in conjunction with other disease management approaches such as quarantine, herd manage- ment to reduce intra-herd transmission, and test and removal. However, all 22 infected cattle herds identi- fied since the 1998 report were at minimum official calfhood vaccinated herds, including some that were calfhood and adult vaccinated. It is important to note that direct exposure to a high infectious dose of the bacteria (for example, through direct contact with aborted fetus and placenta) can reduce the protective benefit of the vaccine. Therefore, while it is not appropriate to conclude based on these data that vaccina- tion is an ineffective management tool to prevent infection, it illustrates the need for vaccines to be com- bined with other management approaches in control programs. Vaccination does have a role in preventing further transmission by significantly reducing abortions, which is considered a very high-risk event with regard to transmission among cattle. An improved vaccine for each of the three species (elk, bison, and cattle) would help suppress and eventually eliminate brucellosis in the GYA. For free-ranging bison and elk, appropriate and cost- effective vaccine delivery systems would be critical. Rabies vaccination of wildlife and domestic animals is a classic example of successful vaccination campaigns to protect public health, domestic animal health, and wildlife health. It has been used very effectively in North America for reducing prevalence in domes- tic dogs to near zero using traditional vaccines. Species-specific vaccine-laden baits have also been used to greatly reduce disease in wildlife (fox, skunk, and raccoon), and thus reduce exposure risk to humans and domestic animals. Relevant to a national park, the opposite approach has been used in Tanzania where a “ring” vaccination approach around Serengeti National Park is used very effectively to control rabies transmission from domestic dogs outside the park to wildlife within the park. But even use of a highly effective vaccine for immunization of cattle in and around the GYA would not be the solution to brucellosis management in the GYA unless coupled with an effective vaccine for elk or other means to prevent further expansion of B. abortus infected elk outside current DSA boundaries. However, until the issue of infected elk transmitting B. abortus to cattle is fully addressed, there will still be a perception of risk by other states that will likely drive continued brucellosis testing of cattle leaving the DSAs even if cattle are vaccinated with a highly effective vaccine. Nevertheless, the committee concludes that the sig- nificant reduction in risk of transmission among vaccinated cattle provides sufficient reason to con- tinue calfhood and adult vaccination of high-risk cattle when coupled with other risk reduction ap- proaches (Conclusion 8). 178 Prepublication Copy—Subject to Further Editorial Revision

Overall Findings, Conclusions, and Recommendations 4. BIOECONOMICS: A FRAMEWORK FOR MAKING DECISIONS Economic resources for managing disease risks in the GYA are scarce. Any management strategies that impose costs on agencies and other stakeholders while producing few to no benefits will not be adopted. Costs are not limited to direct monetary costs of undertaking management actions, and benefits are not limited to reduced economic risks to cattle producers; the costs and benefits also include the posi- tive and negative impacts to the ecological processes of the region that are valued (either directly or indi- rectly) by stakeholder groups. Moreover, many costs and benefits ultimately depend on how individual ranchers, landowners, and resource users respond to changes in risk. Many of these benefits and costs will not be realized in the short term, and thus a long-term perspective and clearly communicating that per- spective is needed in managing the entire system. A significant change since the 1998 report has been the development of systems-level approaches to solving coupled socioeconomic, biological, and ecological problems. It is now common to find multidis- ciplinary teams of scientists involved in addressing some of society’s most complex problems that are particularly difficult to solve because of their interactions with multiple underlying factors that are chang- ing or not well understood. Brucellosis control in the GYA is a prime example of such a problem, and can benefit from a systems-level approach. Bioeconomic modeling provides a valuable framework for systems-level decision making that is able to take into account the socioeconomic costs and benefits of reducing transmission from wildlife to domestic cattle and bison, and is able to promote coordi- nation and targeting of actions spatially and temporally based on expected costs and benefits, including potential impacts beyond the GYA. Quantitative models that include short- and long-term epidemiological and economic risks can help managers decide how to target resources to activities based on the costs and benefits of those activities. Part of this framework includes a periodic, performance-based evaluation of effectiveness. It would also be important to tie the allocation of public financial resources to risk reducing behaviors. While the Statement of Task requests a cost-benefit analysis for various management options, a lack of critical information severely limits the ability to develop a comprehensive empirical assessment at this time. There are significant knowledge gaps for key economic and disease ecology relations, in- cluding the effectiveness, cost, and unanticipated impacts of various candidate management options to control brucellosis in the broader GYA system. Given this and other considerations, a benefit-cost as- sessment with specific, quantified results to guide prescriptive actions is beyond the scope of this report. Even though it may take some time to develop a bioeconomic model, such a model will be essential for decision makers in managing scarce resources to determine the most appropriate and cost-effective solu- tions. Consideration of research needs relative to closing the gaps in knowledge that limit cost-benefit analysis are considered below in the final section of this chapter (see “Research Agenda”). A coupled systems/bioeconomic framework is vital for evaluating the socioeconomic costs and benefits of reducing brucellosis in the GYA, and would be needed to weigh the potential costs and benefits of particular management actions within an adaptive management setting. A bioeconomic framework is also needed to identify appropriate management actions to target spatial-temporal risks, including risks beyond the GYA (Conclusion 9). 5. A CALL TO STRATEGIC ACTION A statement made in the 1998 report is particularly noteworthy given the increase in brucellosis in cattle in the GYA since 1998. “Because neither sufficient information nor technical capability is available to implement a brucellosis eradication program in the GYA at present, eradication as a goal is more a statement of principle than a workable program. The best that will be possible in the near future will be reduction of the risk of transmission of B. abortus from wildlife to cattle.” The current committee similar- ly concurs that eradication of brucellosis from the GYA remains idealistic, but is still not currently feasi- ble for multiple scientific, social, political, and economic reasons. The term “eradication” denotes a com- plete absence of a disease agent, in this case within the GYA, and is distinct from “elimination” of Prepublication Copy—Subject to Further Editorial Revision 179

Revisiting Brucellosis in the Greater Yellowstone Area brucellosis in a given population such as domestic cattle. Thus, while eradication of brucellosis in the GYA remains a distant goal, significant progress toward reducing or eliminating brucellosis transmission from wildlife to domestic species is possible. Undoubtedly, sufficient societal and political will along with sufficient financial resources will be required for success. Managing an ecosystem as complex as the Greater Yellowstone Ecosystem will require coor- dination and cooperation from multiple stakeholders, and will require expertise across many disci- plines to understand the intended and unintended costs and benefits of actions (Conclusion 10). Ad- dressing brucellosis under the new and changing conditions in the region necessitates a more systematic, rigorous, and coordinated approach at several levels—from priority setting to information gathering, data sharing, and wildlife and disease management—than has occurred thus far. The current approaches are likely to remain insufficient to decrease the risk of brucellosis in the region. A strategic plan is needed to coordinate future efforts, fill in critical knowledge and information gaps, and determine the most appropriate management actions under a decision-making framework that is flexible and accounts for risks and costs (Conclusion 11). 5.1 Coordinating a Complex System Management of brucellosis in the GYA is under the jurisdiction of various state, federal, private, and tribal authorities. Each entity has its own mission and goals, and at times these goals may conflict with one another. In addition, there are private landowners, hunters, and ranchers whose actions can im- pact and are impacted by the decisions of others. To date, the efforts undertaken by various state and fed- eral entities have been conducted in a piecemeal fashion, resulting in a disjointed and uneven approach. Moreover, actions taken have not been effective in addressing the problem, because they have not ad- dressed the issues on a systems level. While each state has the right to establish independent management approaches, management actions within each state can have external impacts for the other two states in the GYA and beyond; similarly, each federal agency has the right to establish independent management approaches for their area of jurisdiction, yet there may be unintended consequences that impact the mis- sion and goals of other agencies. This points to the need for a coordinated, mutually agreed upon ap- proach among state and federal agencies charged with managing brucellosis in the GYA. Coordinated efforts across federal, state, and tribal jurisdictions are needed, recognizing first- ly that B. abortus in wildlife spreads without regard to political boundaries, and secondly that the current spread of brucellosis will have serious future implications if it moves outside of the GYA (Conclusion 12). Future progress will depend on actions of private and public stakeholders, and will re- quire integrating multiple scientific approaches. Therefore, a greater level of transparency in management actions, data collection, and data sharing will be required at both state and federal levels to inform the actions of private and public stakeholders. Recommendation 6: All federal, state, and tribal agencies with jurisdiction in wildlife man- agement and in cattle and domestic bison disease control should work in a coordinated, transparent manner to address brucellosis in multiple areas and across multiple jurisdictions. Effectiveness is dependent on political will, a respected leader who can guide the process with goals, timelines, measured outcomes, and a sufficient budget for quantifiable success. Therefore, participation of leadership at the highest federal (Secretary) and state (Governor) levels for initiating and coordi- nating agency and stakeholder discussions and actions, and in sharing information is critical. 5.2 Integration of Management Approaches Historically, there was great interest in brucellosis at the highest levels of government through the Greater Yellowstone Interagency Brucellosis Committee. The GYIBC functioned effectively for a num- ber of years, but its success ultimately suffered from a lack of authority to mandate changes across the region. While the threat has expanded since 1998, the participation of essential stakeholders has dimin- ished due to loss of interest caused by lack of a positive outcome or productive movement in the disease 180 Prepublication Copy—Subject to Further Editorial Revision

Overall Findings, Conclusions, and Recommendations progression within the wildlife populations. There is a need to reinvigorate this interest with buy-in and participation of leadership, and development of a mechanism for coordinating policy and management actions. This coordinating mechanism will need to operate under a political mandate from leadership, and will need to involve all public and private entities with a stake in brucellosis control. The coordinating mechanism will need to be adequately funded and will need to operate independently to make science- based recommendations directly to leadership with the authority to implement the recommended actions. The following considerations are critical when developing a mandate for high-level coordination: • Establishing goals and objectives on an ecosystem-wide basis, with performance-based measures and outcome assessment tied to funding decisions. • Acknowledging the interrelationships of all elements of the ecosystem that requires a regional solution, with shared costs and possible redistribution of funds among agencies and states that have a stake in the outcome. • Developing a long-term solution to managing or controlling brucellosis in the GYA that facili- tates collaboration across jurisdictions (federal, state, tribal, and private). • Developing standardized methods and rules governing the borders, operation, testing protocols, and movement requirements of the designated surveillance areas. Current methods and rules are loosely defined and specific to each state, and they do not appear to be based on a formal as- sessment of risk and outcomes. (Management of the designated surveillance areas was previous- ly discussed.) • Sharing of information and data across the tri-state area to successfully control the spread of brucellosis in the GYA. As noted above, each state has the authority to approach brucellosis control independently; however, the problem requires a systems-level approach and systems- level analysis of data to assess the performance of management policies and actions. The success of an interagency group is dependent on leadership and on its participants. Thus it would be imperative for a federal agency with regulatory oversight of brucellosis (such as USDA) to take leadership in moving the discussions forward. One approach for harmonized policy development includes the formation of a national level coordinating council with representation of stakeholders from all federal agency, tribal, and state jurisdictions. An example of an effective interagency group is the Coordinating Council (CC) for the National Animal Health Laboratory Network (NAHLN). The CC (originally termed a Steering Committee) is led by USDA and includes representatives from state departments of agriculture, and national and state laboratories. The original Steering Committee was formed in 2002, and it drafted and recommended policies and operational protocols for the NAHLN that have withstood the test of time. The success of this approach has hinged on the participation and agreement of high-level leadership from multiple government agencies when critical and sometimes controversial issues were discussed. 5.3 Integration of Scientific Approaches A forum to coordinate scientific approaches toward brucellosis control among all states and agencies with jurisdiction in the GYA would be a valuable mechanism to ensure that science in- forms policy. Such a body would share information, prioritize research projects, limit duplication of ef- forts, advise on management actions, and serve as a potential venue for communicating scientifically sound and agreed-upon messages and policies to the public. The research forum established by the Wyoming Consortium for the Advancement of Brucellosis Science (CABS) serves as a good example of a setting that brings together scientists to draw conclusions based on data with the intent to inform policy decisions. Broadening the mandate of a scientific working group like CABS to include coordination of brucellosis control across the entire ecosystem would provide a valuable forum to ensure that the best available science is being considered with regard to ecological rather than political boundaries. A scientific working group could be advisory to a national level coordi- Prepublication Copy—Subject to Further Editorial Revision 181

Revisiting Brucellosis in the Greater Yellowstone Area nating council, encompassing multiple scientific disciplines to include expertise in ecology, biology, in- fectious diseases, disease modeling, vaccines, social sciences, and economics. As noted previously, sharing of information and data is essential for making progress on a system wide approach toward brucellosis control. It will be important to ensure that publicly funded data and other scientific information essential to informing management actions are openly and freely available. One role of the scientific working group could be in developing or recommending appropriate policies that govern open access, as an open data policy would facilitate exchange of information and data across boundaries and jurisdictions. Although some data on elk population size and seroprevalence are available, they are not available as raw data or in machine-readable formats, which makes them difficult to use. Ad- ditionally, cattle, bison, and elk space-use data are critical to understanding risk, yet they are not easily accessible to the public as privacy concerns limit the sharing of certain data on private entities. However, transparency and sharing of data for cattle, elk, and bison are important for a system-wide analysis of risk and smarter decision making based on risk. The committee finds that the lack of openly accessible da- ta has limited the amount of scientific progress on controlling brucellosis, slowed the learning pro- cess, and limited critical information necessary for making decisions. Unless there are legal re- strictions related to privacy concerns, data should be shared across agencies and should be made more accessible (for example, placing data online in interoperable formats or providing access to raw data). 6. RESEARCH AGENDA Eliminating B. abortus transmission within wildlife populations (elk and bison) and from wildlife to cattle and domestic bison in the GYA—and by extension, eliminating it from the United States—is not feasible unless critical knowledge gaps are addressed. An integrated, multi-disciplinary approach is nec- essary for addressing multiple aspects of the problem, thus research teams will need to include members from various disciplines who provide relevant expertise and understanding. This will also require collabo- ration and coordinated communications among the university, agency, and nonprofit research communi- ties. Recommendation 7: The research community should address the knowledge and data gaps that impede progress in managing or reducing risk of B. abortus transmission to cattle and domes- tic bison from wildlife. The committee identifies several knowledge gaps across various disciplines, and includes a relative ranking in relation to how crucial the gaps are and how likely it would be to impact near-future management decisions. Where appropriate, the critical knowledge and data gaps are noted by species (for example, both elk and bison are specified for some areas while only elk are noted for others). It is important to emphasize that research should be cross-disciplinary to address the problem on a sys- tems level. 6.1 Brucellosis Disease Ecology and Cattle Risk Recommendation 7A: Top priority should be placed on research to better understand brucel- losis disease ecology and epidemiology in elk and bison, as such information would be vital in in- forming management decisions. Research would need to (1) identify and understand the factors driving the rate and direction of B. abortus spread in elk and whether they can be targeted by any management actions; (2) estimate the risk of elk-cattle contact and B. abortus transmission, and the factors that can mitigate that risk and ideally eliminate transmission; and (3) refine and update models of disease dynamics to assimilate data for forecasting and informing alternative actions in active adaptive management. Genetic and serological data from elk suggest that B. abortus has primarily spread in northwestern and northeastern directions from the Wyoming feedgrounds but with limited spread into southern Wyo- ming and Idaho. Further work is needed to predict the future rate and direction of B. abortus spread in elk, identify factors that may limit that progression, and subsequently determine possible management actions 182 Prepublication Copy—Subject to Further Editorial Revision

Overall Findings, Conclusions, and Recommendations that can target those factors. It will be important to design a study with an appropriate level of surveil- lance to further understand how brucellosis is self-sustaining in elk populations outside the feedgrounds. Collecting and establishing a repository of genetic isolates of B. abortus from elk and collecting samples of elk DNA would be useful. Currently there are few predictors of where and when transmission from elk to cattle is likely to oc- cur, and the effectiveness of local efforts to mitigate that risk is unknown. Measuring cattle risk at local and regional scales is critical to devising management actions that mitigate that risk. Case-control studies investigating why some ranching properties have had more elk to cattle transmission than others would help to elucidate whether there are local herd plans that are associated with lower risks despite similar broader scale transmission risks (e.g., elk density and seroprevalence). Further work on estimating the risk of elk-cattle contact and transmission and the factors that can mitigate that risk are critical to achieving the ideal of eliminating transmission into cattle. 6.2 Economic and Risk Analysis Although there have been economic studies on the producer level, there has not been a bioeconomic analysis on comprehensive disease management strategies for the GYA as a system. Such an analysis would be critical in determining the costs and benefits of options as part of a decision-making framework. However, a number of knowledge gaps currently limit the ability to conduct at comprehensive analysis. Recommendation 7B: To inform elk management decisions, high priority should be given to studies that would provide a better understanding of economic risks and benefits. It is critical to un- derstand the following to conduct a comprehensive bioeconomic analysis: • Information on values associated with GYA wildlife. This includes use values stemming from hunting, park visitation, wildlife viewing inside and outside Yellowstone and Grand Teton Na- tional Parks, and non-use values related to conservation of wildlife stocks. This would also in- clude an evaluation of management actions perceived as undesirable, such as supplemental feed- ing, bio-bullets (which are no longer used), mass culls, and culls within YNP boundaries, including a temporal component of those actions (for example, whether short-term culling for long-term goals might be acceptable). • Information on social and private incentives for separating cattle from elk, both on private lands (hazing) and public lands (e.g., spatial-temporal grazing decisions). • Information on incentives of other landowners to manage lands for elk habitat/refuge. • Information about the costs and the effectiveness of the various actions (even as basic as vac- cination) for reducing transmission and at various levels of effort. 6.3 Land Use Land use changes have likely contributed to changes in elk numbers and distributions. As previously noted, land acquisitions by owners who discourage or prohibit access by hunters create elk refugia from hunting, which potentially contributes to larger elk populations and increased numbers of large elk aggre- gations. These population changes could enhance brucellosis transmission and reservoir maintenance in- dependent of bison. Land use decisions by both livestock producers and natural resource agencies that control grazing allotments (such as the USDA Forest Service and the DOI Bureau of Land Management) may impact the risk of transmission from wildlife to cattle and domestic bison. Similarly, the risk of transmission is impacted by the locations of elk feedgrounds relative to the spatial and temporal distribu- tions of elk and cattle. However, there are limited data on the drivers of land use changes and how these changes contribute to the maintenance and spread of brucellosis in the GYA. A better understanding of these drivers and their impacts would be useful to inform land use policy, as well as land owner and man- agement agency actions to reduce risk of B. abortus transmission. Prepublication Copy—Subject to Further Editorial Revision 183

Revisiting Brucellosis in the Greater Yellowstone Area Recommendation 7C: Studies and assessments should be conducted to better understand the drivers of land use change and their effects on B. abortus transmission risk. The studies should be designed to determine how changes in land use contribute to altered elk numbers and distributions, how land use changes affect the spread and maintenance of brucellosis in elk throughout the GYA, and how the spatial distributions of livestock producers, grazing allotments, and elk contribute to risks of elk to cattle transmission. Increased understanding of land use changes and their effects on elk distributions and interactions with livestock will facilitate the development of resource management approaches and poli- cies that minimize B. abortus transmission risks. 6.4 Elk Diagnostics Elk diagnostic testing will become increasingly important in the future as evidence suggests an ex- pansion of B. abortus-infected elk ranges beyond current DSAs, transmission of B. abortus from elk to cattle, and maintenance in elk populations outside of the winter feed grounds in Wyoming. While assays for testing of cattle for Brucella infection have a long history of success in effectively identifying B. abor- tus positive cattle, none of the current diagnostic assays have optimal characteristics for rapid, sensitive and specific determination of disease status in elk. This is especially important due to the particular chal- lenges in handling elk, obtaining specimens, and holding animals in pens until testing is completed. Recommendation 7D: Priority should be given to developing assays for more accurate detec- tion of B. abortus infected elk, optimally in a format capable of being performed “pen-side” to pro- vide reliable rapid results in the field. 6.5 Brucella Genetics Although infection biology of B. abortus is better understood now than in 1998, there are still a number of major knowledge gaps in ruminants. Infection biology studies in elk, bison, and cattle have been largely neglected, and have been greatly limited by onerous Select Agent requirements, the lack of large animal biocontainment facilities, and the substantial costs for large animal experiments. It is important to note that scientific research in understanding brucellosis and progress in brucello- sis diagnostics and vaccines has been hampered by the Select Agent Rule (implemented in 1997), which requires B. abortus to be handled, stored, transported, and distributed with significant restrictions. These restrictions have increased the cost of brucellosis research, and have constrained brucellosis research in elk and bison to two U.S. laboratories. The higher cost of research and limited number of facilities capa- ble of conducting brucellosis research also deters the next generation of scientists from pursuing research in brucellosis. Thus, the committee is supportive of current proposals and measures being taken to remove B. abortus from the Select Agent List. Recommendation 7E: Research should be conducted to better understand the infection biology of B. abortus. To do so would require collecting B. abortus isolates from GYA elk, bison, and cattle, and conducting comparative genomic analyses of those isolates to understand the underlying mechanisms for its adaptation in elk as a primary and likely self-sustaining host. It would also be useful to establish a bi- orepository of samples (e.g., serum, tissues, B. abortus isolates, DNA, RNA) with relevant metadata. Such a repository would have significant research value for future researchers to understand host and pathogen genetic characterization. A multi-user oversight group would be needed to manage the biorepos- itory’s acquisition, cataloguing, and use of valuable samples for vaccine research and diagnostic test de- velopment. 184 Prepublication Copy—Subject to Further Editorial Revision

Overall Findings, Conclusions, and Recommendations 6.6 Elk Immunology Compared to bison and cattle, little is known about the elk protective immune response, and even less is known about genetic susceptibility to B. abortus. Unless more research is conducted on elk immu- nology and genetics, development of a safe and effective elk vaccine will remain a distant goal. Recommendation 7F: To aid in the development of an efficacious vaccine for elk, studies should be conducted to understand elk functional genomics regulating immunity to B. abortus. 6.7 Vaccine and Vaccine Delivery System The development of a more effective vaccine for each of the three ruminant species involved in maintenance and transmission of B. abortus in the GYA would significantly enhance progress in control- ling brucellosis in the GYA. The development of an effective vaccine for elk, including an acceptable method of delivery, would be a major advance in expanding adaptive management options for eliminating brucellosis in domestic species. There are currently no effective brucellosis vaccines for elk, and current approved vaccines for bison and cattle have limited effectiveness against infection. Recommendation 7G: The research community should (1) develop an improved brucellosis vaccine for cattle and bison to protect against infection as well as abortion, and (2) develop a vac- cine and vaccine delivery system for elk. These new vaccines should consider mucosal vaccination ap- proaches and possibly incorporate a microencapsulation approach to improve vaccine efficacy. In addi- tion, any new vaccine should be compatible with parenteral or oral delivery, and should allow differentiation of infected from vaccinated animals (DIVA compatible). An effective vaccine for elk is needed to control brucellosis in the GYA. However, delivery of vaccines to wide-ranging animals such as elk and bison over varied terrain would be logistically challenging. A vaccine delivery system that depends on baiting would be needed. Furthermore, assessments are needed to determine how effective vaccines and vaccine delivery systems would be implemented. 7. CONCLUDING REMARKS Since 1998, significant changes have occurred in understanding and managing brucellosis in the GYA. Even over the course of the committee’s review, there were rapid changes in management practices and new cases of brucellosis in cattle and domestic bison, which reemphasizes the difficulty in handling this complex and expanding problem. Brucellosis was eliminated from cattle in the United States after nearly a century of dedicated funding and resources from USDA, states, and livestock producers. With increasing incidence of brucellosis in cattle and domestic bison herds in the GYA in the past few decades due to transmission from elk, significant resources are needed to address a problem that is expanding in scale and scope; without the changes and investments necessary to aggressively address this problem in a coordinated and cost-effective manner, brucellosis will likely spread beyond the GYA into other parts of the United States resulting in serious economic and potential public health consequences. Efforts to re- duce brucellosis in the GYA will depend on significant cooperation among federal, state, and tribal enti- ties and private stakeholders as they determine priorities and next steps in moving forward. The report’s intent is to be useful for decision makers and stakeholders as they address the challenging matter of bru- cellosis in the GYA. REFERENCES Maichak, E.J., B.M. Scurlock, P.C. Cross, J.D. Rogerson, W.H. Edwards, B. Wise, S.G. Smith, and T.J. Kreeger. 2017. Assessment of a strain 19 brucellosis vaccination program in elk. Wildlife Society Bulletin 41:70-79. Peterson, M.N., A.G. Mertig, and J. Liu. 2006. Effects of Zoonotic Disease Attributes on Public Attitudes Towards Wildlife Management. Journal of Wildlife Management 70(6):1746-1753. Prepublication Copy—Subject to Further Editorial Revision 185

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Brucellosis is a nationally and internationally regulated disease of livestock with significant consequences for animal health, public health, and international trade. In cattle, the primary cause of brucellosis is Brucella abortus, a zoonotic bacterial pathogen that also affects wildlife, including bison and elk. As a result of the Brucellosis Eradication Program that began in 1934, most of the country is now free of bovine brucellosis. The Greater Yellowstone Area (GYA), where brucellosis is endemic in bison and elk, is the last known B. abortus reservoir in the United States. The GYA is home to more than 5,500 bison that are the genetic descendants of the original free-ranging bison herds that survived in the early 1900s, and home to more than 125,000 elk whose habitats are managed through interagency efforts, including the National Elk Refuge and 22 supplemental winter feedgrounds maintained in Wyoming.

In 1998 the National Research Council (NRC) issued a report, Brucellosis in the Greater Yellowstone Area, that reviewed the scientific knowledge regarding B. abortus transmission among wildlife—particularly bison and elk—and cattle in the GYA. Since the release of the 1998 report, brucellosis has re-emerged in domestic cattle and bison herds in that area. Given the scientific and technological advances in two decades since that first report, Revisiting Brucellosis in the Greater Yellowstone Area explores the factors associated with the increased transmission of brucellosis from wildlife to livestock, the recent apparent expansion of brucellosis in non-feedground elk, and the desire to have science inform the course of any future actions in addressing brucellosis in the GYA.

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