Risks of Brucella abortus spillover in the Greater Yellowstone Area

Transcription

1 Rev. sci. tech. Off. int. Epiz., 2013, 32 (1), Risks of Brucella abortus spillover in the Greater Yellowstone Area B. Schumaker Department of Veterinary Sciences, University of Wyoming, 1174 Snowy Range Road, Laramie, WY, 82070, United States of America Summary Recurrent spillover of Brucella abortus from wildlife reservoirs to domestic cattle in the Greater Yellowstone Area (GYA) has prevented the United States from completely eradicating bovine brucellosis. Risks to cattle are a function of the size and location of wildlife and livestock populations, the degree and nature of spatio-temporal interactions between the various hosts, the level of disease in wildlife, and the susceptibility of livestock herds. While the brucellosis prevalence in wild, free-ranging GYA bison (Bison bison) is high, current management actions have successfully limited contact between bison and cattle. Under current management practices, the risks to cattle in the GYA are predominantly from wild elk (Cervus elaphus). Intra- and inter-species transmission events, while uncommon, are nevertheless crucial for the maintenance of brucellosis in the GYA. Future management actions should focus on decreasing elk herd densities and group sizes and on understanding the behavioural and environmental drivers that result in co-mingling that makes transmission possible. Keywords Bison Bovine brucellosis Brucella abortus Cattle Disease management Elk Greater Yellowstone Area Risk assessment Wildlife health. Introduction Seventy-eight years after the start of a state federal cooperative eradication programme, the United States was declared free of Brucella abortus infections in domestic cattle (43). However, persistent bovine brucellosis in elk and bison in the Greater Yellowstone Area (GYA) has kept eradication of the disease beyond reach. The GYA is one of the largest intact temperate-zone ecosystems on earth and includes approximately 28,000 square miles in Montana, Idaho, and Wyoming and encompasses state lands, two national parks, portions of six national forests, three national wildlife refuges, Bureau of Land Management holdings, and private and tribal lands. From 2004 to 2008, brucellosis was detected in nine herds of domestic cattle (Bos taurus) in the GYA: five herds in Wyoming, two in Montana, and two herds in Idaho (12). From 2009 to 2011, eight more infected herds were detected, comprising three cattle herds and one captive bison herd in Wyoming, one cattle herd and two captive bison herds in Montana, and one cattle herd in Idaho (19, 20, 21, 22, 23, 24, 25, 26). All episodes were genetically or epidemiologically linked to elk (2, 14, 16, 40). This exemplifies the statement by Wobeser (46) that it is easier to prevent a disease from entering wildlife than to eradicate it once it is endemic. Disease transmission at the wildlife livestock interface is complicated and multifactorial. The risks to livestock grazing in the GYA are a function of wildlife and livestock population sizes, the degree and nature of spatio-temporal overlap of wildlife in areas where cattle graze, the level of disease prevalence in wildlife, and the susceptibility of the livestock herds in question. Considerable research has been conducted to better understand the various components of transmission risk (11, 17, 36, 41). This paper seeks to identify the extent of and gaps in the knowledge of the drivers of B. abortus transmission risk from wildlife to livestock in the GYA.

2 72 Rev. sci. tech. Off. int. Epiz., 32 (1) Wildlife and livestock populations Approximately 4,600 bison occupy the GYA, most of which are found in, and adjacent to, Yellowstone National Park (YNP) (3,700) and in the areas surrounding Jackson, Wyoming (900) (13, 47). Bison hunting presently occurs only in select national forest areas in Wyoming and Montana, with most bison in the Jackson herd utilising the National Elk Refuge during the winter, drawn to the supplemental feed made available to elk. The 2011 summer count for the Yellowstone bison herd was 3,700 animals, divided between central (1,400) and northern (2,300) breeding populations (47). Bison naturally migrate outside of YNP boundaries in winter months in search of forage at lower elevations, and the modelled food-limiting carrying capacity for bison within YNP is 6,200 individuals (32). However, even at lower population numbers, interactive effects of severe winters and herd density with population numbers greater than 4,200 have led to large-scale dispersal to lower elevations outside of YNP (34). Plumb et al. (32) recommended that the Yellowstone bison herd be maintained with less than 4,500 animals to limit largescale movements outside the park during average winter conditions. Approximately 125,000 elk occupy the GYA across 25 federal and state elk management jurisdictions. Agencies manage elk and their habitat resources through complex interagency cooperation. Elk hunting occurs in all involved elk management jurisdictions except YNP. At the turn of the 20th Century, due in large part to commercial hunting practices, there were reported to be only 50,000 elk remaining in the entire continental United States, mainly inhabiting areas of the GYA (37). Supplemental winter elk feeding began in Jackson, Wyoming, in 1910 as an effort to help elk avoid starvation during harsh winters and decrease their impacts on agricultural lands (38). This practice was expanded in 1912 with the creation of the National Elk Refuge. Presently, there are 23 elk feedgrounds in north-west Wyoming (the National Elk Refuge and 22 state operations) that support approximately 25,000 elk, depending on winter severity. Supplemental feeding ultimately led to unintended negative consequences. The number of elk is above management targets in many areas in the GYA (10). Feeding practices have artificially increased their population density from November to April and allowed for more intraspecies transmission of diseases during the winter months. For example, longer feeding seasons are associated with higher B. abortus seroprevalence (8). Cattle in the GYA are managed on large private lands and public grazing allotments. Unlike many other parts of the United States, GYA cattle are, for the most part, seasonally free-ranging and share habitat with wild ungulate species, especially during summer months on public grazing allotments. In the northern GYA, 266 cattle are grazed in the winter and 1,363 in the spring on adjacent public and private lands north and west of YNP and within habitat occupied by bison and elk during the winter (29). In Wyoming, over 270,000 cattle occupy counties that overlap the southern GYA (44). Bacterial transmission The risk period for B. abortus transmission from elk and bison to cattle is generally well defined. Data suggest that bison and elk in the GYA exhibit a high degree of birth synchrony, with the majority (80%) of bison calving late- April to late-may, and elk calving between mid-may to mid- June (3, 4). Feedground data from the southern portion of the GYA in Wyoming have shown birth dates for elk that are later in the year, but parturition is unlikely after the third week of June (9, 30). If one includes abortions in the last 90 days of pregnancy, late-january to mid-june is the most likely period for B. abortus transmission (34). The probability of B. abortus transmission between elk (or from elk to cattle) is likely low during elk calving (May through June) because elk dams segregate themselves while giving birth and meticulously clean the birth site (27). Thus, birth sites are dispersed, and the likelihood of other elk or cattle encountering infected birth tissues and fluids is low. However, transmission risk may be higher during the brucellosis abortion period from February through April when many elk congregate in larger groups on lowerelevation winter habitat that overlaps with cattle-grazing areas (18). Spontaneous abortions by elk that are not segregated from the herd could expose many susceptible elk (or cattle) to infected fetuses and birth tissues. In contrast to elk, bison are gregarious during parturition, and pregnant female herd mates will nuzzle newborn calves (42). Mobbing events of a newborn calf are likely important to the maintenance of B. abortus infections (28). Bison conservation continues to be a priority; however, for decades, livestock producers and regulatory personnel have viewed Yellowstone bison as a potential source of pathogens for livestock in the GYA (31). However, current management practices, which maintain spatial and temporal separation between bison and cattle, makes the risk of B. abortus transmission from bison to cattle in the GYA negligible (29, 36). Maintenance of the disease in wildlife reservoirs must come from persistent transmission either within or between elk and bison populations. It has been a long-held belief by many in the United States brucellosis research

3 Rev. sci. tech. Off. int. Epiz., 32 (1) 73 community that B. abortus infections in elk would not persist without persistent reinfections from GYA bison or increased transmission rates on southern GYA feedgrounds (4). However, current research suggests that elk maintain the disease independently of bison (33, 36). In addition, private lands across the GYA that do not allow hunting access act as pseudo-feedgrounds by providing refuge for elk during authorised hunting seasons. Researchers have seen an increase in seroprevalence among elk congregating in these areas (7). Elk that winter in central YNP showed 53% winter range overlap with Yellowstone bison in December and 76% overlap in May (15). A considerable percentage of elk locations (18%) were within 100 m of bison, with co-mingling correlated with snowpack. However, such elk do not show evidence of an increase in B. abortus exposure compared with populations that are spatio-temporally separated from bison (15, 33). A comprehensive risk assessment of all elk herds that overlap with GYA bison concurs with this observation (36). Based on the degree of home-range overlap and the relative level of exposure in the wildlife residing in YNP, it appears that bison provide little risk of transmitting B. abortus to elk in overlapping herds. On the contrary, bison could potentially have significant exposure to infectious material from elk. In a local area of co-mingling, bison are more dominant than elk and may drive elk off grazing areas, increasing their opportunity for exposure to residual elk infectious material but decreasing the opportunity for elk to be exposed to bison infectious material. Although elk within the same population share a home range, the level of disease transmission between herdmates was roughly a third of that within the GYA bison population (36). Behavioural differences between bison and elk likely account for this lowered rate of transmission (42). Thus, transmission risks to elk from bison or other elk from outside their own population were negligible. chance of interspecific contact (5). The dataset can also be used to assess the spatio-temporal interactions of cattle and elk. Unpublished analyses show that, in late spring and summer, elk and cattle come within 50 m to 100 m of each more often than would be expected under the assumption of randomness; these interactions remain rare, but in the majority of cases the animals continue to draw closer together and co-mingling occurs (Heinrich Dohna, University of California Davis, unpublished data). Lack of available forage and other environmental pressures during severe winters in the GYA are likely to increase comingling. These events, while infrequent, are extremely important in the maintenance of disease prevalence in the GYA ecosystem. Unlike a disease transmitted by direct animal-to-animal contact (although it can be transmitted through live birth), brucellosis is generally believed to be primarily transmitted through bacterial shedding into the environment. Consequently, susceptible and infected animals do not have to be in the same place at the same time for the pathogen to be transmitted; animals can come into contact with the bacterium if they graze in areas previously inhabited by infected animals. The reported minimal infectious dose for cattle by the conjunctival route is approximately 103 CFU to 108 CFU of the bacterium (39). The number of days a B. abortus-contaminated birth site is infective depends upon the amount of time that it takes for an infected fetus or tissues to be scavenged or for ultraviolet radiation and drying to kill the bacteria. Aune et al. (1) and Cook et al. (6) found that fetuses would be scavenged prior to ultraviolet degradation of bacteria (1 to 78 days, mean = 18.2). These data were used by Kilpatrick et al. (29) to estimate the persistence of infectivity in an infected site. Although managers have been concerned over the high level of Brucella antibody prevalence in bison, current management practices have successfully prevented the spatio-temporal overlap of bison and cattle (45). It is unclear how much spatio-temporal overlap between bison or elk and cattle is required for disease spillover to occur. It is also unknown how close a susceptible domestic cow has to be to B. abortus-infected tissues before it would be likely to investigate tissues and thus risk infectious contact. Researchers at the Starkey Experimental Forest in Eastern Oregon, an area with a climate and habitats similar to many national forests in the Intermountain West (a region between the Rocky mountains in the east and the Cascade Range and Sierra Nevada in the west) (35), have conducted extensive research focusing on competition between cattle and elk for forage and space. The results of the studies showed a general pattern of larger ungulate species displacing smaller species (i.e. cattle displacing elk, which in turn displace deer). This decreases the Modelling and risk assessment The dynamics of the Yellowstone bison population have been extensively modelled, however, quantitative assessments of the risk of pathogen spillover from wildlife to cattle have been a more recent pursuit (29, 36). Estimates of the risk of bacterial transmission from GYA bison to cattle grazing in the northern portion of the GYA are heterogeneous across the spatial landscape and vary with bison population numbers and winter severity (29, 36). Assessments that included elk and bison showed that, despite substantial shedding of Brucella bacteria from bison in some winters, elk represent the major risk to domestic cattle (36). Natural herd migration and boundary management operations are important in minimising the contribution of bison to cattle exposure risk, which supports continued boundary management operations to ensure spatio-temporal separation between bison and cattle.

4 74 Rev. sci. tech. Off. int. Epiz., 32 (1) Conclusion While transmission events within and between wildlife and livestock populations in the GYA are likely uncommon, these rare events are nevertheless the basis for maintaining brucellosis in the greater Yellowstone ecosystem (Heinrich Dohna, University of California Davis, unpublished data). There is a need for a deeper understanding of the behavioural and environmental drivers that make co-mingling and transmission possible. Although bison have been the major management target over the 78-year history of the State Federal Cooperative Brucellosis Eradication Plan, there is scientific justification to increasingly focus efforts on elk cattle interactions. Minimal opportunity exists for B. abortus transmission from bison to elk under current natural conditions in the northern GYA. Therefore, management practices aimed at reducing bison seroprevalence are unlikely to substantially reduce transmission risk from elk to cattle. Strategies that decrease elk herd densities and group sizes and reduce elk-to-elk transmission may prove to be important in minimising pathogen spillover to cattle grazing in the GYA. Acknowledgements The author is grateful to M.E. Kauffman and D. O Toole for critically reviewing the manuscript. Les risques de diffusion de Brucella abortus dans la région du Grand Yellowstone B. Schumaker Résumé La diffusion récurrente de Brucella abortus parmi les animaux d élevage de la région du Grand Yellowstone à partir d espèces sauvages réservoirs est un obstacle à l éradication complète de la brucellose bovine aux États-Unis. Les risques auxquels les bovins sont exposés dépendent de la taille et de la localisation du cheptel domestique et des populations d animaux sauvages, de l intensité et de la nature des interactions spatiotemporelles entre les divers hôtes, de la prévalence dans la faune sauvage et de la sensibilité des troupeaux domestiques. Chez le bison sauvage (Bison bison) vivant en liberté dans le Grand Yellowstone, la prévalence de l infection brucellique est élevée mais des mesures de gestion appropriées ont réussi à limiter les contacts entre les bisons et les bovins. Dans le contexte actuel de gestion de ces espèces, l essentiel du risque auquel sont exposés les bovins du Grand Yellowstone provient du cerf élaphe sauvage (Cervus elaphus). Les cas de transmission intra-espèce et inter-espèces sont assez rares, mais suffisent néanmoins à entretenir l infection brucellique dans cet écosystème. À l avenir, les mesures de gestion devront s attacher en priorité à faire baisser la densité des troupeaux de cerfs élaphes et à réduire la taille des groupes, et à élucider les facteurs comportementaux et environnementaux qui favorisent les rapprochements propices à la transmission de la brucellose. Mots-clés Bison Bovin Brucella abortus Brucellose bovine Cerf élaphe Évaluation du risque Gestion sanitaire Grand Yellowstone Santé de la faune sauvage.

5 Rev. sci. tech. Off. int. Epiz., 32 (1) 75 Riesgo de extensión de Brucella abortus en la zona del Gran Yellowstone B. Schumaker Resumen Los recurrentes episodios de extensión de Brucella abortus de los reservorios salvajes al ganado vacuno doméstico en la zona del Gran Yellowstone han impedido que los Estados Unidos logren erradicar por completo la brucelosis bovina. Los riesgos a que está expuesto el ganado dependen de distintos factores: tamaño y localización de las poblaciones de bovinos salvajes y domésticos; grado y naturaleza de las interacciones espacio-temporales entre los diversos hospedadores; nivel de la enfermedad en la fauna salvaje; y susceptibilidad de los rebaños vacunos. Aunque la prevalencia de la brucelosis es elevada en las poblaciones salvajes de bisontes (Bison bison) que viven en libertad en el Gran Yellowstone, las medidas de gestión actuales han servido para reducir el contacto entre esas poblaciones y el ganado vacuno. Con el dispositivo de gestión que actualmente se aplica, los riesgos más importantes para el ganado del Gran Yellowstone provienen esencialmente del ciervo común salvaje (Cervus elaphus). Los episodios de transmisión intra e interespecífica, aunque infrecuentes, no dejan de ser cruciales para que la brucelosis se mantenga presente en la zona del Gran Yellowstone. Las futuras medidas de gestión deberían centrarse en reducir la densidad de rebaños de ciervos comunes y el tamaño de los grupos y en entender los factores etológicos y ambientales que favorecen los contactos que a su vez hacen posible la transmisión. Palabras clave Bisonte Brucelosis bovina Brucella abortus Ciervo común Determinación del riesgo Ganado vacuno Gestión de enfermedades Salud de la fauna salvaje Zona del Gran Yellowstone. References 1. Aune K., Rhyan J.C., Russell R., Roffe T.J. & Corso B. (2012). Environmental persistence of Brucella abortus in the greater Yellowstone area. J. Wildl. Manag., 76 (2), Beja-Pereira A., Bricker B., Chen S., Almenddra C., White P.J. & Luikart G. (2009). DNA genotyping suggests that recent brucellosis outbreaks in the Greater Yellowstone Area originated from elk. J. Wildl. Dis., 45, Berger J. & Cain S.L. (1999). Reproductive synchrony in brucellosis-exposed bison in the southern Greater Yellowstone Ecosystem and in noninfected populations. Conservation Biology, 13 (2), Cheville N., McCullough D.R. & Paulson L.R. (1998). Brucellosis in the Greater Yellowstone Area. National Research Council, Washington, DC. 5. Coe P.K., Johnson B.K., Stewart K.M. & Kie J.G. (2005). Spatial and temporal interactions of elk, mule deer and cattle. In The Starkey Project: a synthesis of long-term studies of elk and mule deer. Reprinted from the 2004 Transactions of the North American Wildlife and Natural Resources Conference (M.J. Wisdom, ed.). Alliance Communications Group, Lawrence, Kansas, Cook W.E., Williams E.S. & Dubay S.A. (2004). Disappearance of bovine fetuses in northwestern Wyoming. Wildl. Soc. Bull., 32 (1), Cross P.C., Cole E.K., Dobson A.P., Edwards W.H., Hamlin K.L., Luikart G., Middleton A.D., Scurlock B.M. & White P.J. (2010). Probable causes of increasing brucellosis in free-ranging elk of the Greater Yellowstone Ecosystem. Ecol. Applic., 20 (1),

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