Dynamics and persistence of rabies in the Arctic

  • Audrey Simon Research Group on Epidemiology of Zoonoses and Public Health, Faculty of Veterinary Medicine, University of Montreal
  • Olivia Tardy Research Group on Epidemiology of Zoonoses and Public Health, Faculty of Veterinary Medicine, University of Montreal
  • Amy Hurford Department of Mathematics and Statistics, Memorial University of Newfoundland, St. John’s, Newfoundland and Labrador
  • Nicolas Lecomte Canada Research Chair in Polar and Boreal Ecology, Department of Biology, University of Moncton
  • Denise Bélanger Research Group on Epidemiology of Zoonoses and Public Health, Faculty of Veterinary Medicine, University of Montreal
  • Patrick Leighton Research Group on Epidemiology of Zoonoses and Public Health, Faculty of Veterinary Medicine, University of Montreal
Keywords: Vulpes lagopus, epidemiological model, Arctic rabies, virus transmission, public health, climate change


Rabies is a major issue for human and animal health in the Arctic, yet little is known about its epidemiology. In particular, there is an ongoing debate regarding how Arctic rabies persists in its primary reservoir host, the Arctic fox (Vulpes lagopus), which exists in the ecosystem at very low population densities. To shed light on the mechanisms of rabies persistence in the Arctic, we built a susceptible–exposed–infectious–recovered (SEIR) epidemiological model of rabies virus transmission in an Arctic fox population interacting with red foxes (Vulpes vulpes), a rabies host that is increasingly present in the Arctic. The model suggests that rabies cannot be maintained in resource-poor areas of the Arctic, characterized by low Arctic fox density, even in the presence of continuous reintroduction of the virus by infected Arctic foxes from neighbouring regions. However, in populations of relatively high Arctic fox density, rabies persists under conditions of higher transmission rate, prolonged infectious period and for a broad range of incubation periods. Introducing the strong cyclical dynamics of Arctic prey availability makes simulated rabies outbreaks less regular but more intense, with an onset that does not neatly track peaks in Arctic fox density. Finally, interaction between Arctic and red foxes increases the frequency and/or the intensity of rabies outbreaks in the Arctic fox population. Our work suggests that disruption of prey cycles and increasing interactions between Arctic and red foxes due to climate change and northern development may significantly change the epidemiology of rabies across the Arctic.


Download data is not yet available.


Aenishaenslin C., Simon A., Forde T., Ravel A., Proulx J.F., Fehlner-Gardiner C., Picard I. & Belanger D. 2014. Characterizing rabies epidemiology in remote Inuit communities in Quebec, Canada: a “one health” approach. Ecohealth 11, 343–355, http://dx.doi.org/10.1007/s10393-014-0923-1.

Altizer S., Dobson A., Hosseini P., Hudson P., Pascual M. & Rohani P. 2006. Seasonality and the dynamics of infectious diseases. Ecology Letters 9, 467–484, http://dx.doi.org/10.1111/j.1461-0248.2005.00879.x.

Anderson R.M., Jackson H.C., May R.M. & Smith A.M. 1981. Population dynamics of fox rabies in Europe. Nature 289, 765–771, http://dx.doi.org/10.1038/289765a0.

Angerbjörn A., Tannerfeldt M. & Erlinge S. 1999. Predator–prey relationships: Arctic foxes and lemmings. Journal of Animal Ecology 68, 34–49, http://dx.doi.org/10.1046/j.1365-2656.1999.00258.x.

Aubert M.F. 1992. Epidemiology of fox rabies. In K. Bogel et al. (eds.): Wildlife rabies control. Pp. 9–18. Kent: Wells Medical Ltd.

Audet A.M., Robbins C.B. & Lariviere S. 2002. Alopex lagopus. Mammalian Species 713, 1–10, http://dx.doi.org/10.1644/1545-1410(2002)713<0001:AL>2.0.CO;2.

Ballard W.B., Follmann E.H., Ritter D.G., Robards M.D. & Cronin M.A. 2001. Rabies and canine distemper in an Arctic fox population in Alaska. Journal of Wildlife Diseases 37, 133–137, http://dx.doi.org/10.7589/0090-3558-37.1.133.

Blackwood J.C., Streicker D.G., Altizer S. & Rohani P. 2013. Resolving the roles of immunity, pathogenesis, and immigration for rabies persistence in vampire bats. Proceedings of the National Academy of Sciences of the United States of America 110, 20837–20842, http://dx./doi.org/10.1073/pnas.1308817110.

Blower S.M. & Dowlatabadi H. 1994. Sensitivity and uncertainty analysis of complex models of disease transmission: an HIV model as an example. International Statistical Review 62, 229–243, http://dx.doi.org/10.2307/1403510.

Bolzoni L., De Leo G.A., Gatto M. & Dobson A.P. 2008. Body-size scaling in an SEI model of wildlife diseases. Theoretical Population Biology 73, 374–382, http://dx.doi.org/10.1016/j.tpb.2007.12.003.

Carnell R. 2012. Package “lhs”: Latin hypercube samples (version 0.14). Vienna: R Foundation for Statistical Computing. Accessed on the Internet at https://cran.r-project.org/web/packages/lhs/index.html.

CFIA (Canadian Food Inspection Agency) 2018. Rabies in Canada 2018. Accessed on the internet at http://www.inspection.gc.ca/animals/terrestrial-animals/diseases/reportable/rabies/rabies-in-canada/eng/1356156989919/1356157139999 on 13 March 2018.

Chapman R.C. 1978. Rabies: decimation of a wolf pack in Arctic Alaska. Science 201, 365–367, http://dx.doi.org/10.1126/science.566470.

Dobson A. 2004. Population dynamics of pathogens with multiple host species. The American Naturalist 164 Supplement 5, S64–S78, http://dx.doi.org/10.1086/424681.

Elmhagen B., Tannerfeldt M., Verucci P. & Angerbjorn A. 2000. The Arctic fox (Alopex lagopus): an opportunistic specialist. Journal of Zoology 251, 139–149, http://dx.doi.org/10.1111/j.1469-7998.2000.tb00599.x.

Elton C. 1931. Epidemics among sledge dogs in the Canadian Arctic and their relation to disease in the Arctic fox. Canadian Journal of Research 58, 673–692, http://dx.doi.org/10.1139/cjr31-106.

Fekadu M., Shaddock J.H. & Baer G.M. 1982. Excretion of rabies virus in the saliva of dogs. The Journal of Infectious Diseases 145, 715–719, http://dx.doi.org/10.1093/infdis/145.2.715.

Follmann E.H., Ritter D.G. & Baer G.M. 1988. Immunization of Arctic foxes (Alopex lagopus) with oral rabies vaccine. Journal of Wildlife Diseases 24, 477–483, http://dx.doi.org/10.7589/0090-3558-24.3.477.

Follmann E., Ritter D., Swor R., Dunbar M. & Hueffer K. 2011. Preliminary evaluation of Raboral V-RG(R) oral rabies vaccine in Arctic foxes (Vulpes lagopus). Journal of Wildlife Diseases 47, 1032–1035, http://dx.doi.org/10.7589/0090-3558-47.4.1032.

Follmann E.H, Ritter D.G. & Hartbauer D.W. 2004. Oral vaccination of captive Arctic foxes with lyophilized SAG2 rabies vaccine. Journal of Wildlife Diseases 40, 328–334, http://dx.doi.org/10.7589/0090-3558-40.2.328.

Fuglei E. & Ims R.A. 2008. Global warming and effects on the Arctic fox. Science Progress 91, 175–191, http://dx.doi.org/10.3184/003685008X327468.

Gallant D., Slough B.G., Reid D.G. & Berteaux D. 2012. Arctic fox versus red fox in the warming Arctic: four decades of den surveys in north Yukon. Polar Biology 35, 1421–1431, http://dx.doi.org/10.1007/s00300-012-1181-8.

Gilg O., Hanski I. & Sittler B. 2003. Cyclic dynamics in a simple vertebrate predator–prey community. Science 302, 866–868, http://dx.doi.org/10.1126/science.1087509.

Goldsmith E.W., Renshaw B., Clement C.J., Himschoot E.A., Hundertmark K.J. & Hueffer K. 2016. Population structure of two rabies hosts relative to the known distribution of rabies virus variants in Alaska. Molecular Ecology 25, 675–688, http://dx.doi.org/10.1111/mec.13509.

Henden J.-A., Ims R.A., Yoccoz N.G., Hellström P. & Angerbjörn A. 2010. Strength of asymmetric competition between predators in food webs ruled by fluctuating prey: the case of foxes in tundra. Oikos 119, 27–34, http://dx.doi.org/10.1111/j.1600-0706.2009.17604.x.

Hersteinsson P. & Macdonald D.W. 1992. Interspecific competition and the geographical distribution of red and Arctic foxes Vulpes-vulpes and Alopex-lagopus. Oikos 64, 505–515, http://dx.doi.org/10.2307/3545168.

Holmala K. & Kauhala K. 2006. Ecology of wildlife rabies in Europe. Mammal Review 36, 17–36, http://dx.doi.org/10.1111/j.1365-2907.2006.00078.x.

Huettmann F., Magnuson E.E. & Hueffer K. 2017. Ecological niche modeling of rabies in the changing Arctic of Alaska. Acta Veterinaria Scandinavica 59, 18–29, http://dx.doi.org/10.1186/s13028-017-0285-0.

Kim B.I., Blanton J.D., Gilbert A., Castrodale L., Hueffer K., Slate D. & Rupprecht C.E. 2014. A conceptual model for the impact of climate change on fox rabies in Alaska, 1980-2010. Zoonoses and Public Health 61, 72–80, http://dx.doi.org/10.1111/zph.12044.

Knobel D.L., Cleaveland S., Coleman P.G., Fevre E.M., Meltzer M.I., Miranda M.E., Shaw A., Zinsstag J. & Meslin F.X. 2005. Re-evaluating the burden of rabies in Africa and Asia. Bulletin of the World Health Organization 83, 360–368, http://dx.doi.org/10.1590/S0042-96862005000500012.

Konovalov G.V., Kantorovich R.A., Buzinov I.A. & Riutova V.P. 1965. Experimental investigations into rage and rabies in polar foxes, natural hosts of the infection. II. An experimental morphological study of rabies in polar foxes. Acta Virologica 9, 235–239.

Krebs C.J. 2011. Of lemmings and snowshoe hares: the ecology of northern Canada. Proceedings of the Royal Society Biological Sciences Series B 278, 481–489, http://dx.doi.org/10.1098/rspb.2010.1992.

Lai S., Bety J. & Berteaux D. 2015. Spatio-temporal hotspots of satellite-tracked Arctic foxes reveal a large detection range in a mammalian predator. Movement Ecology 3, article no. 37, http://dx.doi.org/10.1186/s40462-015-0065-2.

Lecomte N., Careau V., Gauthier G. & Giroux J.F. 2008. Predator behaviour and predation risk in the heterogeneous Arctic environment. Journal of Animal Ecology 77, 439–447, http://dx.doi.org/10.1111/j.1365-2656.2008.01354.x.

Lembo T., Hampson K., Haydon D.T., Craft M., Dobson A., Dushoff J., Ernest E., Hoare R., Kaare M., Mlengeya T., Mentzel C. & Cleaveland S. 2008. Exploring reservoir dynamics: a case study of rabies in the Serengeti ecosystem. Journal of Applied Ecology 45, 1246–1257, http://dx.doi.org/10.1111/j.1365-2664.2008.01468.x.

Mansfield K.L., Racloz V., McElhinney L.M., Marston D.A., Johnson N., Ronsholt L., Christensen L.S., Neuvonen E., Botvinicin A.D., Rupprecht C.E. & Fooks A.R. 2006. Molecular epidemiological study of Arctic rabies virus isolates from Greenland and comparison with isolates from throughout the Arctic and Baltic regions. Virus Research 116, 1–10, http://dx.doi.org/10.1016/j.virusres.2005.08.007.

Marino S., Hogue I.B., Ray C.J. & Kirschner D.E. 2008. A methodology for performing global uncertainty and sensitivity analysis in systems biology. Journal of Theoretical Biology 254, 178–196, http://dx.doi.org/10.1016/j.jtbi.2008.04.011.

McCallum H., Barlow N. & Hone J. 2001. How should pathogen transmission be modelled? Trends in Ecology & Evolution 16, 295–300, http://dx.doi.org/10.1016/S0169-5347(01)02144-9.

Mørk T., Bohlin J., Fuglei E., Åsbakk K. & Tryland M. 2011. Rabies in the Arctic fox population, Svalbard, Norway. Journal of Wildlife Diseases 47, 945–957, http://dx.doi.org/10.7589/0090-3558-47.4.945.

Mørk T. & Prestrud P. 2004. Arctic rabies—a review. Acta Veterinaria Scandinavica 45, 1–9, http://dx.doi.org/10.1186/1751-0147-45-1.

Morters M.K., Restif O., Hampson K., Cleaveland S., Wood J.L. & Conlan A.J. 2013. Evidence-based control of canine rabies: a critical review of population density reduction. Journal of Animal Ecology 82, 6–14, http://dx.doi.org/10.1111/j.1365-2656.2012.02033.x.

Nadin-Davis S.A., Sheen M. & Wandeler A.I. 2012. Recent emergence of the Arctic rabies virus lineage. Virus Research 163, 352–362, http://dx.doi.org/10.1016/j.virusres.2011.10.026.

Niezgoda M., Briggs D.J., Shaddock J. & Rupprecht C.E. 1998. Viral excretion in domestic ferrets (Mustela putorius furo) inoculated with a raccoon rabies isolate. American Journal of Veterinary Research 59, 1629–1632.

Norén K., Hersteinsson P., Samelius G., Eide N.E., Fuglei E., Elmhagen B., Dalen L., Meijer T. & Angerbjörn A. 2012. From monogamy to complexity: social organization of Arctic foxes (Vulpes lagopus) in contrasting ecosystems. Canadian Journal of Zoology 90, 1102–1116, http://dx.doi.org/10.1139/z2012-077.

Pamperin N.J, Follmann E.H. & Petersen B. 2006. Interspecific killing of an Arctic fox by a red fox at Prudhoe Bay, Alaska. Arctic 59, 361–364, http://dx.doi.org/10.14430/arctic284.

Prager K.C., Mazet J.A., Dubovi E.J., Frank L.G., Munson L., Wagner A.P. & Woodroffe R. 2012. Rabies virus and canine distemper virus in wild and domestic carnivores in northern Kenya: are domestic dogs the reservoir? Ecohealth 9, 483–498, http://dx.doi.org/10.1007/s10393-013-0815-9.

Prestrud P., Krogsrud J. & Gjertz I. 1992. The occurrence of rabies in the Svalbard islands of Norway. Journal of Wildlife Diseases 28, 57–63, http://dx.doi.org/10.7589/0090-3558-28.1.57.

Pujol G., Iooss B. & Janon A. 2017. Package “sensitivity”: global sensitivity analysis of model outputs (version 1.15.0). Vienna: R Foundation for Statistical Computing. Accessed on the Internet at https://cran.r-project.org/web/packages/sensitivity/index.html.

R Core Team 2017. R: a language and environment for statistical computing. Vienna: R Foundation for Statistical Computing. Accessed on the Internet at https://www.R-project.org/.

Rausch R.L. 1958. Some observations on rabies in Alaska, with special reference to wild canidae. Journal of Wildlife Management 22, 246–260, http://dx.doi.org/10.2307/3796457.

Rausch R.L. 1972. Observations on some natural-focal zoonoses in Alaska. Archives of Environmental Health 25, 246–252, http://dx.doi.org/10.1080/00039896.1972.10666170.

Ritter D. 1981. Rabies. In R.A. Dieterich (ed.): Alaskan wildlife diseases. Pp. 6–12. Fairbanks: University of Alaska, Fairbanks.

Shirley M.D.F., Elmhagen B., Lurz P.W.W., Rushton S.P. & Angerbjörn A. 2009. Modelling the spatial population dynamics of Arctic foxes: the effects of red foxes and microtine cycles. Canadian Journal of Zoology 87, 1170–1183, http://dx.doi.org/10.1139/Z09-104.

Simon A., Belanger D., Berteaux D., Hueffer K., Rees E. & Leighton P.A. In press. Ecology of rabies in the Arctic fox (Vulpes lagopus). In D. Gregory & R. Tinline (eds.): Taking the bite out of rabies: the evolution of rabies management in Canada. Toronto: University of Toronto Press.

Soetaert K., Petzoldt T. & Setzer RW. 2010. Solving differential equations in R: package deSolve. Journal of Statistical Software 33, 1–25, http://dx.doi.org/10.18637/jss.v033.i09.

Tyul'ko Z.S. & Kuzmin I.V. 2002. Simulation of rabies epizootic process in fox populations at a limited carrying capacity of biotopes. Russian Journal of Ecology 33, 331–337, http://dx.doi.org/10.1023/A:1020265726669.

WHO 2013. World Health Organization expert consultation on rabies. Second report. WHO Technical Report Series 982. Geneva: World Health Organization.

Wu J., Dhingra R., Gambhir M. & Remais J.V. 2013. Sensitivity analysis of infectious disease models: methods, advances and their application. Journal of The Royal Society Interface 10, article no. 20121018, http://dx.doi.org/10.1098/rsif.2012.1018.
How to Cite
Simon A., Tardy O., Hurford A., Lecomte N., Bélanger D., & Leighton P. (2019). Dynamics and persistence of rabies in the Arctic. Polar Research, 38. https://doi.org/10.33265/polar.v38.3366
Research Articles