Abstract
Infectious diseases that affect wildlife and livestock are challenging to manage and can lead to large-scale die-offs, economic losses, and threats to human health. The management of infectious diseases in wildlife and livestock is made easier with knowledge of disease risk across space and identifying stakeholders associated with high-risk landscapes. This study focuses on anthrax, caused by the bacterium Bacillus anthracis, risk to wildlife and livestock in Montana. There is a history of anthrax in Montana, but the spatial extent of disease risk and subsequent wildlife species at risk are not known. Our objective was to predict the potential geographic distribution of anthrax risk across Montana, identify wildlife species at risk and their distributions, and define stakeholders. We used an ecological niche model to predict the potential distribution of anthrax risk. We overlaid susceptible wildlife species distributions and land ownership delineations on our risk map. We found that there was an extensive region across Montana predicted as potential anthrax risk. These potentially risky landscapes overlapped the ranges of all 6 ungulate species considered in the analysis and livestock grazing allotments, and this overlap was on public and private land for all species. Our findings suggest that there is the potential for a multi-species anthrax outbreak on multiple landscapes across Montana. Our potential anthrax risk map can be used to prioritize landscapes for surveillance and for implementing livestock vaccination programs.
Similar content being viewed by others
References
Anderson R, Lew D, Peterson A (2003) Evaluating predictive models of species’ distributions: criteria for selecting optimal models. Ecol Model 162:211–232.
Bagamian KH, Alexander KA, Hadfield TL, Blackburn JK (2013) Ante-and postmortem diagnostic techniques for anthrax: Rethinking pathogen exposure and the geographic extent of the disease in wildlife. J Wildl Dis 49:786–801.
Bellan SE, Gimenez O, Choquet R, Getz WM (2013) A hierarchical distance sampling approach to estimating mortality rates from opportunistic carcass surveillance data. Methods Ecol Evol 4:361–369.
Blackburn JK (2010) Integrating geographic information systems and ecological niche modeling into disease ecology: a case study of Bacillus anthracis in the United States and Mexico. In: Emerging and Endemic Pathogens. Springer, pp 59–88.
Blackburn JK (2006) Evaluating the spatial ecology of anthrax in North America: Examining epidemiological components across multiple geographic scales using a GIS-based approach.
Blackburn JK, Asher V, Stokke S, Hunter DL, Alexander KA (2014a) Dances with anthrax: wolves (Canis lupus) kill anthrax bacteremic plains bison (Bison bison bison) in southwestern Montana. J Wildl Dis 50:393–396.
Blackburn JK, Goodin DG (2013) Differentiation of springtime vegetation indices associated with summer anthrax epizootics in west Texas, USA, deer. J Wildl Dis 49:699–703.
Blackburn JK, Hadfield TL, Curtis AJ, Hugh-Jones ME (2014b) Spatial and Temporal Patterns of Anthrax in White-Tailed Deer, Odocoileus virginianus, and Hematophagous Flies in West Texas during the Summertime Anthrax Risk Period. Ann Assoc Am Geogr 104:939–958.
Blackburn JK, McNyset KM, Curtis A, Hugh-Jones ME (2007) Modeling the geographic distribution of Bacillus anthracis, the causative agent of anthrax disease, for the contiguous United States using predictive ecologic niche modeling. Am J Trop Med Hyg 77:1103–1110.
Blackburn JK, Mullins JC, Rashid M, Van Ert M, Bowen RA, Hugh-Jones ME, Hadfield TL. A revised prediction of the Western North America lineage of Bacillus anthracis for the continental United States: pathogen re-emergence or under-reporting?.
Blackburn JK, Odugbo MO, Van Ert M, O’Shea B, Mullins J, Perrenten V, Maho A, Hugh-Jones M, Hadfield T (2015) Bacillus anthracis Diversity and Geographic Potential across Nigeria, Cameroon and Chad: Further Support of a Novel West African Lineage. PLoS Negl Trop Dis 9:e0003931.
Blackburn JK, Van Ert M, Mullins JC, Hadfield TL, Hugh-Jones ME (2014c) The Necrophagous Fly Anthrax Transmission Pathway: Empirical and Genetic Evidence from Wildlife Epizootics. Vector-Borne Zoonotic Dis 14:576–583.
Brook RK, McLachlan SM (2009) Transdisciplinary habitat models for elk and cattle as a proxy for bovine tuberculosis transmission risk. Prev Vet Med 91:197–208.
Buechner HK (1960) The Bighorn Sheep in the United States, Its Past, Present, and Future. Wildl Monogr 3–174. doi: 10.2307/3830515.
Burcham M, Edge WD, Marcum CL (1999) Elk use of private land refuges. Wildlife Society Bulletin 27:833–839.
Carstensen M, O’Brien DJ, Schmitt SM (2011) Public acceptance as a determinant of management strategies for bovine tuberculosis in free-ranging US wildlife. Vet Microbiol 151:200–204.
Cheville NF, McCullough DR, Paulson LR (1998) Brucellosis in the greater Yellowstone area. National Academies Press.
Clegg S, Turnbull P, Foggin C, Lindeque P (2007) Massive outbreak of anthrax in wildlife in the Malilangwe Wildlife Reserve, Zimbabwe. Vet Rec 160:113–118.
Costa J, Peterson AT, Beard CB (2002) Ecologic niche modeling and differentiation of populations of Triatoma brasiliensis neiva, 1911, the most important Chagas’ disease vector in northeastern Brazil (hemiptera, reduviidae, triatominae). Am J Trop Med Hyg 67:516–520.
Cross P, Cole E, Dobson A, Edwards W, Hamlin K, Luikart G, Middleton A, Scurlock B, White P (2010) Probable causes of increasing brucellosis in free-ranging elk of the Greater Yellowstone Ecosystem. Ecol Appl 20:278–288.
Dragon D, Elkin B, Nishi J, Ellsworth T (1999) A review of anthrax in Canada and implications for research on the disease in northern bison. J Appl Microbiol 87:208–213.
FAO/IIASA/CISS-CAS/JRC (2008) Harmonized world soil database (version 1.0). FAO, Rome, Italy and Laxenburg, Austria.
Geist V (2006) The North American model of wildlife conservation: a means of creating wealth and protecting public health while generating biodiversity. Gaining Ground: In Pursuit of Ecological Sustainability 285–293.
Gortazar C, Diez-Delgado I, Barasona JA, Vicente J, De La Fuente J, Boadella M (2015) The wild side of disease control at the wildlife-livestock-human interface: a review. Front Vet Sci 1:27.
Gosnell H, Haggerty JH, Travis WR (2006) Ranchland ownership change in the Greater Yellowstone Ecosystem, 1990–2001: implications for conservation. Soc Nat Resour 19:743–758.
Gude JA, Cunningham JA, Herbert JT, Baumeister T (2012) Deer and elk hunter recruitment, retention, and participation trends in Montana. J Wildl Manag 76:471–479.
Haggerty JH, Travis WR (2006) Out of administrative control: absentee owners, resident elk and the shifting nature of wildlife management in southwestern Montana. Geoforum 37:816–830.
Hampson K, Lembo T, Bessell P, Auty H, Packer C, Halliday J, Beesley CA, Fyumagwa R, Hoare R, Ernest E (2011) Predictability of anthrax infection in the Serengeti, Tanzania. J Appl Ecol 48:1333–1344.
Hay SI, Tatem A, Graham A, Goetz S, Rogers D (2006) Global environmental data for mapping infectious disease distribution. Adv Parasitol 62:37–77.
Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A (2005) Very high resolution interpolated climate surfaces for global land areas. Int J Climatol 25:1965–1978. doi: 10.1002/joc.1276.
Hugh-Jones M, Blackburn J (2009) The ecology of Bacillus anthracis. Mol Aspects Med 30:356–367.
Hugh-Jones M, De Vos V (2002) Anthrax and wildlife. Rev Sci Tech-Off Int Epizoot 21:359–384.
Jones KE, Patel NG, Levy MA, Storeygard A, Balk D, Gittleman JL, Daszak P (2008) Global trends in emerging infectious diseases. Nature 451:990–993.
Joyner TA, Lukhnova L, Pazilov Y, Temiralyeva G, Hugh-Jones ME, Aikimbayev A, Blackburn JK (2010) Modeling the potential distribution of Bacillus anthracis under multiple climate change scenarios for Kazakhstan. PloS One 5:e9596.
Kenefic L, Beaudry J, Trim C, Daly R, Parmar R, Zanecki S, Huynh L, Van Ert M, Wagner D, Graham T (2008) High resolution genotyping of Bacillus anthracis outbreak strains using four highly mutable single nucleotide repeat markers. Lett Appl Microbiol 46:600–603.
Langford E, Dorward W (1977) Erysipelothrix insidiosa recovered from sylvatic mammals in northwestern Canada during examinations for rabies and anthrax. Can Vet J 18:101.
Lobo JM, Jiménez‐Valverde A, Real R (2008) AUC: a misleading measure of the performance of predictive distribution models. Glob Ecol Biogeogr 17:145–151.
McNyset K (2005) Use of ecological niche modelling to predict distributions of freshwater fish species in Kansas. Ecol Freshw Fish 14:243–255.
McNyset K, Blackburn J (2006) Does GARP really fail miserably? A response to. Divers Distrib 12:782–786.
Miller RS, Farnsworth ML, Malmberg JL (2013) Diseases at the livestock–wildlife interface: status, challenges, and opportunities in the United States. Prev Vet Med 110:119–132.
Mongoh MN, Dyer NW, Stoltenow CL, Khaitsa ML (2008) Risk factors associated with anthrax outbreak in animals in North Dakota, 2005: A retrospective case-control study. Public Health Rep 123:352–359.
Morris LR, Proffitt KM, Asher V, Blackburn JK (2015) Elk resource selection and implications for anthrax management in Montana. J Wildl Manag. doi: 10.1002/jwmg.1016.
Mullins JC, Garofolo G, Van Ert M, Fasanella A, Lukhnova L, Hugh-Jones ME, Blackburn JK (2013) Ecological niche modeling of Bacillus anthracis on three continents: evidence for genetic-ecological divergence? PloS One 8:e72451.
Mullins JC, Van Ert M, Hadfield TL, Nikolich MP, Hugh-Jones M, Blackburn JK (2015) Spatio-temporal patterns of an anthrax outbreak in white-tailed deer, Odocoileus virginanus, and associated genetic diversity of Bacillus anthracis. BMC ecology 15(1): 1.
Mullins J, Lukhnova L, Aikimbayev A, Pazilov Y, Van Ert M, Blackburn JK (2011) Ecological Niche Modelling of the Bacillus anthracis A1. a sub-lineage in Kazakhstan. BMC Ecol 11:32.
Muoria PK, Muruthi P, Kariuki WK, Hassan BA, Mijele D, Oguge NO (2007) Anthrax outbreak among Grevy’s zebra (Equus grevyi) in Samburu, Kenya. Afr J Ecol 45:483–489.
Nakazawa Y, Williams RA, Peterson AT, Mead PS, Kugeler KJ, Petersen JM (2010) Ecological niche modeling of Francisella tularensis subspecies and clades in the United States. Am J Trop Med Hyg 82:912–918.
O’Brien DJ, Schmitt SM, Fitzgerald SD, Berry DE, Hickling GJ (2006) Managing the wildlife reservoir of Mycobacterium bovis: the Michigan, USA, experience. Vet Microbiol 112:313–323.
Parkinson R, Rajic A, Jenson C (2003) Investigation of an anthrax outbreak in Alberta in 1999 using a geographic information system. Can Vet J 44:315.
Peterson MN (2004) An approach for demonstrating the social legitimacy of hunting. Wildl Soc Bull 32:310–321.
Proffitt KM, Anderson N, Lukacs P, Riordan MM, Gude JA, Shamhart J (2015) Effects of elk density on elk aggregation patterns and exposure to brucellosis. J Wildl Manag 79:373–383.
Proffitt KM, Gude JA, Hamlin KL, Garrott RA, Cunningham JA, Grigg JL (2011) Elk distribution and spatial overlap with livestock during the brucellosis transmission risk period. J Appl Ecol 48:471–478.
Proffitt KM, Gude JA, Hamlin KL, Messer MA (2013) Effects of hunter access and habitat security on elk habitat selection in landscapes with a public and private land matrix. J Wildl Manag 77:514–524.
Salb A, Stephen C, Ribble C, Elkin B (2014) DESCRIPTIVE EPIDEMIOLOGY OF DETECTED ANTHRAX OUTBREAKS IN WILD WOOD BISON (BISON BISON ATHABASCAE) IN NORTHERN CANADA, 1962-2008. J Wildl Dis 50:459–468.
Schorr RA, Lukacs PM, Gude JA (2014) The Montana deer and Elk hunting population: The importance of cohort group, license price, and population demographics on hunter retention, recruitment, and population change. J Wildl Manag 78:944–952. doi: 10.1002/jwmg.732.
Sells SN, Mitchell MS, Nowak JJ, Lukacs PM, Anderson NJ, Ramsey JM, Gude JA, Krausman PR (2015) Modeling risk of pneumonia epizootics in bighorn sheep. J Wildl Manag 79:195–210. doi: 10.1002/jwmg.824.
Shury T, Frandsen D, O’Brodovich L (2009) Anthrax in free-ranging bison in the Prince Albert National Park area of Saskatchewan in 2008. Can Vet J 50:152.
Stockwell D, Peters D (1999) The GARP modelling system: problems and solutions to automated spatial prediction. Int J Geogr Inf Sci 13:143–158.
Turner A, Galvin J, Rubira R, Miller G (1999) Anthrax explodes in an Australian summer. J Appl Microbiol 87:196–199.
Turner WC, Imologhome P, Havarua Z, Kaaya GP, Mfune JK, Mpofu ID, Getz WM (2013) Soil ingestion, nutrition and the seasonality of anthrax in herbivores of Etosha National Park. Ecosphere 4:1-19.
Turner WC, Kausrud KL, Krishnappa YS, Cromsigt JP, Ganz HH, Mapaure I, Cloete CC, Havarua Z, Küsters M, Getz WM (2014) Fatal attraction: vegetation responses to nutrient inputs attract herbivores to infectious anthrax carcass sites. Proc R Soc B Biol Sci 281:20141785.
Van Ness GB (1981) Anthrax. In: Diseases and parasites of white-tailed deer.
Watson R (2012) Public wildlife on private land: Unifying the split estate to enhance trust resources. Duke Envtl Pol F 23:291.
Williams S (2010) Wellspring of wildlife funding. Wildlife Professional, pp 35–38.
Zweig MH, Campbell G (1993) Receiver-operating characteristic (ROC) plots: a fundamental evaluation tool in clinical medicine [published erratum appears in Clin Chem 1993 Aug; 39 (8): 1589]. Clin Chem 39:561.
Acknowledgments
Funding for this study was provided by the National Institutes of Health Grant 1R01GM117617-01 to JKB, the College of Liberals Arts and Sciences, and the Emerging Pathogens Institute at the University of Florida. We thank M.E. Hugh-Jones for information on anthrax in mule deer.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Morris, L.R., Blackburn, J.K. Predicting Disease Risk, Identifying Stakeholders, and Informing Control Strategies: A Case Study of Anthrax in Montana. EcoHealth 13, 262–273 (2016). https://doi.org/10.1007/s10393-016-1119-7
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10393-016-1119-7