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Models for managing wildlife disease

Published online by Cambridge University Press:  18 August 2016

HAMISH McCALLUM*
Affiliation:
Environmental Futures Research Institute and Griffith School of Environment, Griffith University Nathan campus, 170 Kessels road, Nathan, Queensland 4111, Australia
*
*Corresponding author. Environmental Futures Research Institute and Griffith School of Environment, Griffith University Nathan campus, 170 Kessels road, Nathan, Queensland 4111, Australia. E-mail: h.mccallum@griffith.edu.au

Summary

Modelling wildlife disease poses some unique challenges. Wildlife disease systems are data poor in comparison with human or livestock disease systems, and the impact of disease on population size is often the key question of interest. This review concentrates specifically on the application of dynamic models to evaluate and guide management strategies. Models have proved useful particularly in two areas. They have been widely used to evaluate vaccination strategies, both for protecting endangered species and for preventing spillover from wildlife to humans or livestock. They have also been extensively used to evaluate culling strategies, again both for diseases in species of conservation interest and to prevent spillover. In addition, models are important to evaluate the potential of parasites and pathogens as biological control agents. The review concludes by identifying some key research gaps, which are further development of models of macroparasites, deciding on appropriate levels of complexity, modelling genetic management and connecting models to data.

Type
Special Issue Review
Copyright
Copyright © Cambridge University Press 2015 

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References

REFERENCES

Anderson, R. M. and May, R. M. (1978). Regulation and stability of host–parasite interactions. I. Regulatory processes. Journal of Animal Ecology 47, 219247.Google Scholar
Anderson, R. M. and May, R. M. (1979). Population biology of infectious diseases. Part I. Nature 280, 361367.CrossRefGoogle ScholarPubMed
Anderson, R. M. and May, R. M. (1992). Infectious Diseases of Humans: Dynamics and Control. Oxford University Press, New York.Google Scholar
Barlow, N. D. (1994). Predicting the effect of a novel vertebrate biocontrol agent: a model for viral-vectored immunocontraception of New Zealand possums. Journal of Applied Ecology 31, 454462.Google Scholar
Barlow, N. D. (1997). Modelling immunocontraception in disseminating systems. Reproduction Fertility and Development 9, 5160.Google Scholar
Barlow, N. D., Barron, M. C. and Parkes, J. (2002). Rabbit haemorrhagic disease in New Zealand: field test of a disease-host model. Wildlife Research 29, 649653.Google Scholar
Barlow, N. D. and Kean, J. M. (1998). Simple models for the impact of rabbit calicivirus disease (RCD) on Australasian rabbits. Ecological Modelling 109, 225241.Google Scholar
Beeton, N. and McCallum, H. (2011). Models predict that culling is not a feasible strategy to prevent extinction of Tasmanian devils from facial tumour disease. Journal of Applied Ecology 48, 13151323.CrossRefGoogle Scholar
Bennett, R. and Bowers, R. G. (2008). A baseline model for the co-evolution of hosts and pathogens. Journal of Mathematical Biology 57, 791809.CrossRefGoogle ScholarPubMed
Berger, L., Speare, R., Daszak, P., Green, D. E., Cunningham, A. A., Goggin, C. L., Slocombe, R., Ragan, M. A., Hyatt, A. D., McDonald, K. R., Hines, H. B., Lips, K. R., Marantelli, G. and Parkes, H. (1998). Chytridiomycosis causes amphibian mortality associated with population declines in the rain forests of Australia and Central America. Proceedings of the National Academy of Sciences of the United States of America 95, 90319036.Google Scholar
Bernoulli, D. (1760). Essai d'une nouvelle analyse de la mortalite‚ causee par la petite Varole, et des advantages de l'Inoculation pour la prevenir. Memoires de mathematique et de physique, tires des registres de l'Academie Royale des Sciences, Paris. 145.Google Scholar
Bielby, J., Donnelly, C. A., Pope, L. C., Burke, T. and Woodroffe, R. (2014). Badger responses to small-scale culling may compromise targeted control of bovine tuberculosis. Proceedings of the National Academy of Sciences 111, 91939198.Google Scholar
Blackwood, J. C., Streicker, D. G., Altizer, S. and Rohani, P. (2013). Resolving the roles of immunity, pathogenesis, and immigration for rabies persistence in vampire bats. Proceedings of the National Academy of Sciences 110, 2083720842.Google Scholar
Bolzoni, L. and De Leo, G. A. (2013). Unexpected consequences of culling on the eradication of wildlife diseases: the role of virulence evolution. American Naturalist 181, 301313.Google Scholar
Bradshaw, C. J. A., McMahon, C. R., Miller, P. S., Lacy, R. C., Watts, M. J., Verant, M. L., Pollak, J. P., Fordham, D. A., Prowse, T. A. A. and Brook, B. W. (2012). Novel coupling of individual-based epidemiological and demographic models predicts realistic dynamics of tuberculosis in alien buffalo. Journal of Applied Ecology 49, 268277.Google Scholar
Brooks-Pollock, E., Roberts, G. O. and Keeling, M. J. (2014). A dynamic model of bovine tuberculosis spread and control in Great Britain. Nature 511, 228–+.Google Scholar
Bundy, D. A. P., Walson, J. L. and Watkins, K. L. (2013). Worms, wisdom, and wealth: why deworming can make economic sense. Trends in Parasitology 29, 142148.Google Scholar
Burrows, R., Hofer, H. and East, M. L. (1994). Demography, extinction and intervention in a small population: the case of the Serengeti wild dogs. Proceedings of the Royal Society of London Series B 256, 281292.Google Scholar
Calvete, C. (2006). Modeling the effect of population dynamics on the impact of rabbit hemorrhagic disease. Conservation Biology 20, 12321241.CrossRefGoogle ScholarPubMed
Cashins, S. D., Grogan, L. F., McFadden, M., Hunter, D., Harlow, P. S., Berger, L. and Skerratt, L. F. (2013). Prior infection does not improve survival against the amphibian disease chytridiomycosis. PLoS ONE 8, e56747.Google Scholar
Caswell, H. (1989). Matrix Population Models: Construction, Analysis, and Interpretation. Sinauer Associates Inc., Sunderland, MA, USA.Google Scholar
Childs, J. E., Curns, A. T., Dey, M. E., Real, L. A., Feinstein, L., Bjornstad, O. N. and Krebs, J. W. (2000). Predicting the local dynamics of epizootic rabies among raccoons in the United States. Proceedings of the National Academy of Sciences 97, 1366613671.CrossRefGoogle ScholarPubMed
Choisy, M. and Rohani, P. (2006). Harvesting can increase severity of wildlife disease epidemics. Proceedings of the Royal Society of London Series B: Biological Sciences 273, 20252034.Google Scholar
Cleaveland, S., Kaare, M., Knobel, D. and Laurenson, M. K. (2006). Canine vaccination--Providing broader benefits for disease control. Veterinary Microbiology 117, 4350.Google Scholar
Cooke, B. D. and Fenner, F. (2002). Rabbit haemorrhagic disease and the biological control of wild rabbits, Oryctolagus cuniculus, in Australia and New Zealand. Wildlife Research 29, 689706.CrossRefGoogle Scholar
Cornell, S. (2005). Modelling nematode populations: 20 years of progress. Trends in Parasitology 21, 542545.Google Scholar
Coulson, T., Rohani, P. and Pascual, M. (2004). Skeletons, noise and population growth: the end of an old debate? Trends in Ecology & Evolution 19, 359364.Google Scholar
Cox, D. R., Donnelly, C. A., Bourne, F. J., Gettinby, G., McInerney, J. P., Morrison, W. I. and Woodroffe, R. (2005). Simple model for tuberculosis in cattle and badgers. Proceedings of the National Academy of Sciences 102, 1758817593.Google Scholar
Craig, A. P., Hanger, J., Loader, J., Ellis, W. A. H., Callaghan, J., Dexter, C., Jones, D., Beagley, K. W., Timms, P. and Wilson, D. P. (2014). A 5-year Chlamydia vaccination programme could reverse disease-related koala population decline: predictions from a mathematical model using field data. Vaccine 32, 41634170.Google Scholar
Cross, P. C., Creech, T. G., Ebinger, M. R., Manlove, K., Irvine, K., Henningsen, J., Rogerson, J., Scurlock, B. M. and Creel, S. (2013). Female elk contacts are neither frequency nor density dependent. Ecology 94, 20762086.Google Scholar
Csilléry, K., François, O. and Blum, M. G. B. (2012). abc: an R package for approximate Bayesian computation (ABC). Methods in Ecology and Evolution 3, 475479.Google Scholar
Daszak, P., Cunningham, A. A. and Hyatt, A. D. (2000). Emerging infectious diseases of wildlife- threats to biodiversity and human health. Science 287, 443449.Google Scholar
Davis, S., Abbasi, B., Shah, S., Telfer, S. and Begon, M. (2015). Spatial analyses of wildlife contact networks. Journal of the Royal Society Interface 12. 20141004. doi: 10.1098/rsif.2014.1004 Google Scholar
de Castro, F. and Bolker, B. (2005). Mechanisms of disease-induced extinction. Ecology Letters 8, 117126.Google Scholar
Dobson, A. and Foufopoulos, J. (2000). Emerging infectious pathogens of wildlife. Philosophical Transactions of the Royal Society of London Series B: Biological Sciences 356, 10011012.Google Scholar
Donnelly, C. A., Woodroffe, R., Cox, D. R., Bourne, F. J., Cheeseman, C. L., Clifton-Hadley, R. S., Wei, G., Gettinby, G., Gilks, P., Jenkins, H., Johnston, W. T., Le Fevre, A. M., McInerney, J. P. and Morrison, W. I. (2006). Positive and negative effects of widespread badger culling on tuberculosis in cattle. Nature 439, 843846.Google Scholar
Dwyer, G., Levin, S. A. and Buttel, L. (1990). A simulation model of the population dynamics and evolution of myxomatosis. Ecological Monographs 60, 423447.Google Scholar
Dye, C. (1996). Serengeti wild dogs: what really happened? Trends in Ecology and Evolution 11, 188189.CrossRefGoogle ScholarPubMed
Ebert, D. and Bull, J. J. (2003). Challenging the trade-off model for the evolution of virulence: is virulence management feasible? Trends in Microbiology 11, 1520.Google Scholar
Ezeamama, A. E., McGarvey, S. T., Hogan, J., Lapane, K. L., Bellinger, D. C., Acosta, L. P., Leenstra, T., Olveda, R. M., Kurtis, J. D. and Friedman, J. F. (2012). Treatment for Schistosoma japonicum, reduction of intestinal parasite load, and cognitive test score improvements in school-aged children. Plos Neglected Tropical Diseases 6, 10.Google Scholar
Fa, J. E., Sharples, C. M., Bell, D. J. and DeAngelis, D. (2001). An individual-based model of rabbit viral haemorrhagic disease in European wild rabbits (Oryctolagus cuniculus). Ecological Modelling 144, 121138.Google Scholar
Fenner, F. and Fantini, B. (1999). Biological Control of Vertebrate Pests: The History of Myxomatosis; An Experiment in Evolution. CABI Publishing, Wallingford, Oxon, UK; New York, NY, USA.Google Scholar
Fenton, A. and Perkins, S. E. (2010). Applying predator-prey theory to modelling immune-mediated, within-host interspecific parasite interactions. Parasitology 137, 10271038.Google Scholar
Ferguson, N. M., Donnelly, C. A. and Anderson, R. M. (2001). The foot-and-mouth epidemic in Great Britain: pattern of spread and impact of interventions. Science 292, 11551160.Google Scholar
Ferrari, M. J., Bjornstad, O. N. and Dobson, A. P. (2005). Estimation and inference of R0 of an infectious pathogen by a removal method. Mathematical Biosciences 198, 1426.Google Scholar
Freuling, C. M., Hampson, K., Selhorst, T., Schroder, R., Meslin, F. X., Mettenleiter, T. C. and Muller, T. (2013). The elimination of fox rabies from Europe: determinants of success and lessons for the future. Philosophical Transactions of the Royal Society of London Series B-Biological Sciences 368, 20120142. doi: 10.1098/rstb.2012.0142.Google Scholar
Frick, W. F., Pollock, J. F., Hicks, A. C., Langwig, K. E., Reynolds, D. S., Turner, G. G., Butchkoski, C. M. and Kunz, T. H. (2010). An emerging disease causes regional population collapse of a common North American bat species. Science 329, 679682.Google Scholar
Gandon, S., Hochberg, M. E., Holt, R. D. and Day, T. (2013). What limits the evolutionary emergence of pathogens? Philosophical Transactions of the Royal Society of London Series B-Biological Sciences 368, 20120086.Google Scholar
Gascoyne, S. and Laurenson, M. K. (1994). Response to Burrows. Journal of Wildlife Diseases 30, 297299.Google Scholar
Gerber, L., McCallum, H., Lafferty, K., Sabo, J. and Dobson, A. (2005). Exposing extinction risk analysis to pathogens: is disease just another form of density dependence? Ecological Applications 15, 14021414.Google Scholar
Grenfell, B. T., Bjørnstad, O. N. and Kappey, J. (2001). Travelling waves and spatial heirarchies in measles epidemics. Nature 414, 716723.Google Scholar
Gross, J. E. and Miller, M. W. (2001). Chronic wasting disease in mule deer: disease dynamics and control. Journal of Wildlife Management 65, 205215.CrossRefGoogle Scholar
Hallam, T. G. and McCracken, G. F. (2011). Management of the Panzootic white-nose syndrome through culling of bats. Conservation Biology 25, 189194.Google Scholar
Haydon, D. T., Randall, D. A., Matthews, L., Knobel, D. L., Tallents, L. A., Gravenor, M. B., Williams, S. D., Pollinger, J. P., Cleaveland, S., Woolhouse, M. E. J., Sillero-Zubiri, C., Marino, J., Macdonald, D. W. and Laurenson, M. K. (2006). Low-coverage vaccination strategies for the conservation of endangered species. Nature 443, 692695.Google Scholar
Heisey, D. M., Osnas, E. E., Cross, P. C., Joly, D. O., Langenberg, J. A. and Miller, M. W. (2010 a). Linking process to pattern: estimating spatiotemporal dynamics of a wildlife epidemic from cross-sectional data. Ecological Monographs 80, 221240.Google Scholar
Heisey, D. M., Osnas, E. E., Cross, P. C., Joly, D. O., Langenberg, J. A. and Miller, M. W. (2010 b). Rejoinder: sifting through model space. Ecology 91, 35033514.Google Scholar
Hilborn, R. and Mangel, M. (1997). The Ecological Detective. Princeton University Press, Princeton.Google Scholar
Hill, A. B. (1965). The environment and of disease: association or causation? Proceedings of the Royal Society of Medicine 58, 295300.Google Scholar
Hodges, J. S. (2010). Are exercises like this a good use of anybody's time? Ecology 91, 3496–U3492.Google Scholar
Hood, G. M., Chesson, P. and Pech, R. P. (2000). Biological control using sterilizing viruses: host suppression and competition between viruses in non-spatial models. Journal of Applied Ecology 37, 914925.Google Scholar
Hudson, P. J., Dobson, A. P. and Newborn, D. (1998). Prevention of population cycles by parasite removal. Science 282, 22562258.Google Scholar
Iman, R. L. and Conover, W. J. (1980). Small sample sensitivity analysis techniques for computer models, with an application to risk assessment. Communications in Statistics: Theory and Methods A9, 17491842.Google Scholar
Ionides, E. L., Breto, C. and King, A. A. (2006). Inference for nonlinear dynamical systems. Proceedings of the National Academy of Sciences 103, 1843818443.CrossRefGoogle ScholarPubMed
Jolles, A. E., Ezenwa, V. O., Etienne, R. S., Turner, W. C. and Olff, H. (2008). Interactions between macroparasites and microparasites drive infection patterns in free-ranging African buffalo. Ecology 89, 22392250.Google Scholar
Joly, D. O. and Messier, F. (2004). Testing hypotheses of bison population decline (1970–1999) in Wood Buffalo National Park: synergism between exotic disease and predation. Canadian Journal of Zoology 82, 11651176.Google Scholar
Joly, D. O. and Messier, F. (2005). The effect of bovine tuberculosis and brucellosis on reproduction and survival of wood bison in Wood Buffalo National Park. Journal of Animal Ecology 74, 543551.Google Scholar
Jones, M., Hamede, R. and McCallum, H. (2012). The Devil is in the detail: conservation biology, animal philosophies and the role of animal ethics committees. In Science Under Seige: Zoology under Threat (ed. Banks, P., Lunney, D. and Dickman, C.), pp. 7988. Royal Zoological Society of New South Wales, Mosman, NSW.Google Scholar
Joseph, M. B., Mihaljevic, J. R., Arellano, A. L., Kueneman, J. G., Preston, D. L., Cross, P. C. and Johnson, P. T. J. (2013). Taming wildlife disease: bridging the gap between science and management. Journal of Applied Ecology 50, 702712.CrossRefGoogle Scholar
Keeling, M. J. and Grenfell, B. T. (1997). Disease extinction and community size: modeling the persistence of measles. Science 275, 6567.Google Scholar
Kollipara, A., George, C., Hanger, J., Loader, J., Polkinghorne, A., Beagley, K. and Timms, P. (2012). Vaccination of healthy and diseased koalas (Phascolarctos cinereus) with a Chlamydia pecorum multi-subunit vaccine: evaluation of immunity and pathology. Vaccine 30, 18751885.Google Scholar
Lachish, S., Jones, M. E. and McCallum, H. I. (2007). The impact of devil facial tumour disease on the survival and population growth rate of the Tasmanian devil. Journal of Animal Ecology 76, 926936.Google Scholar
Lachish, S., McCallum, H. and Jones, M. (2009). Demography, disease and the devil: life-history changes in a disease-affected population of Tasmanian devils Sarcophilus harrisii . Journal of Animal Ecology 78, 427436.Google Scholar
Lachish, S., McCallum, H., Mann, D., Pukk, C. and Jones, M. (2010). Evaluation of selective culling of infected individuals to control Tasmanian devil facial tumor disease. Conservation Biology 24, 841851.Google Scholar
Lacy, R. C. (1993). Vortex: a computer simulation model for population viability analysis. Wildlife Research 20, 4565.Google Scholar
LaDeau, S. (2010). Advances in modeling highlight a tension between analytical accuracy and accessibility. Ecology 91, 34883492.Google Scholar
Lankester, M. W. (2010). Understanding the impact of meningeal worm, Parelaphostrongylus tenuis, on moose populations. Alces 46, 5370.Google Scholar
Lele, S. R. (2010). Model complexity and information in the data: could it be a house built on sand? Ecology 91, 3493–U3491.Google Scholar
Lion, S. and Boots, M. (2010). Are parasites ‘‘prudent’’ in space? Ecology Letters 13, 12451255.Google Scholar
Lips, K. R., Brem, F., Brenes, R., Reeve, J. D., Alford, R. A., Voyles, J., Carey, C., Livo, L., Pessier, A. P. and Collins, J. P. (2006). Emerging infectious disease and the loss of biodiversity in a Neotropical amphibian community. Proceedings of the National Academy of Sciences 103, 31653170.Google Scholar
Lloyd-Smith, J. O., George, D., Pepin, K. M., Pitzer, V. E., Pulliam, J. R. C., Dobson, A. P., Hudson, P. J. and Grenfell, B. T. (2009). Epidemic dynamics at the human-animal interface. Science 326, 13621367.Google Scholar
Maslo, B. and Fefferman, N. H. (2015). A case study of bats and white-nose syndrome demonstrating how to model population viability with evolutionary effects. Conservation Biology 29, 11761185.Google Scholar
May, R. M. and Anderson, R. M. (1978). Regulation and stability of host-parasite interactions. II. Destabilizing processes. Journal of Animal Ecology 47, 249267.Google Scholar
May, R. M. and Anderson, R. M. (1979). Population biology of infectious diseases. Part II. Nature 280, 455461.Google Scholar
May, R. M. and Anderson, R. M. (1983). Epidemiology and genetics in the co-evolution of parasites and hosts. Proceedings of the Royal Society of London Series B 219, 281313.Google Scholar
McCallum, H. (2008). Tasmanian devil facial tumour disease: lessons for conservation biology. Trends in Ecology & Evolution 23, 631637. doi: http://dx.doi.org/10.1016/j.tree.2008.07.001.Google Scholar
McCallum, H. (2012). Disease and the dynamics of extinction. Philosophical Transactions of the Royal Society of London Series B: Biological Sciences 367, 28282839.Google Scholar
McCallum, H. and Hocking, B. A. (2005). Reflecting on ethical and legal issues in wildlife disease. Bioethics 19, 336347.Google Scholar
McCallum, H. and Jones, M. (2006). To lose both would look like carelessness: Tasmanian devil facial tumour disease. PLoS Biology 4, 16711674.Google Scholar
McCallum, H., Barlow, N. D. and Hone, J. (2001). How should transmission be modelled? Trends in Ecology and Evolution 16, 295300.Google Scholar
McCallum, H., Jones, M., Hawkins, C., Hamede, R., Lachish, S., Sinn, D. L., Beeton, N. and Lazenby, B. (2009). Transmission dynamics of Tasmanian devil facial tumor disease may lead to disease- induced extinction. Ecology 90, 33793392.Google Scholar
McCallum, H. I. and Dobson, A. P. (1995). Detecting disease and parasite threats to endangered species and ecosystems. Trends in Ecology and Evolution 10, 190194.Google Scholar
Minteer, B. A. and Collins, J. P. (2005). Ecological ethics: building a new tool kit for ecologists and biodiversity managers. Conservation Biology 19, 18031812.CrossRefGoogle Scholar
Mutze, G., Bird, P., Cooke, B. and Henzell, R. (2008). Geographic and seasonal variation in the impact of rabbit haemorrhagic disease on European rabbits, Oryctolagus cuniculus, and rabbit damage in Australia. In Lagomorph Biology: Evolution, Ecology, and Conservation (eds. Alves, P. C., Ferrand, N. and Hacklander, K.), pp. 279293. Springer-Verlag Berlin, Heidelberger Platz 3, D-14197 Berlin, Germany.Google Scholar
Mutze, G. J., Sinclair, R. G., Peacock, D. E., Capucci, L. and Kovaliski, J. (2014). Is increased juvenile infection the key to recovery of wild rabbit populations from the impact of rabbit haemorrhagic disease? European Journal of Wildlife Research 60, 489499.Google Scholar
O'Keefe, K. J. and Antonovics, J. (2002). Playing by different rules: the evolution of virulence in sterilizing pathogens. American Naturalist 159, 597605.CrossRefGoogle ScholarPubMed
Parris, K. M., McCall, S. C., McCarthy, M. A., Minteer, B. A., Steele, K., Bekessy, S. and Medvecky, F. (2010). Assessing ethical trade-offs in ecological field studies. Journal of Applied Ecology 47, 227234.Google Scholar
Pinfold, T. L., Brown, G. K., Bettiol, S. S. and Woods, G. M. (2014). Mouse model of devil facial tumour disease establishes that an effective immune response can be generated against the cancer cells. Frontiers in Immunology 5, 251.Google Scholar
Plowright, R. K., Sokolow, S. H., Gorman, M. E., Daszak, P. and Foley, J. E. (2008). Causal inference in disease ecology: investigating ecological drivers of disease emergence. Frontiers in Ecology and the Environment 6, 420429.Google Scholar
Pollak, J. P. and Lacy, R. C. (2014). MetaModel Manager. Version 1.0.1. Chicago Zoological Society, Brookfield, Illinois, USA.Google Scholar
Pope, L. C., Butlin, R. K., Wilson, G. J., Woodroffe, R., Erven, K., Conyers, C. M., Franklin, T., Delahay, R. J., Cheeseman, C. L. and Burke, T. (2007). Genetic evidence that culling increases badger movement: implications for the spread of bovine tuberculosis. Molecular Ecology 16, 49194929.Google Scholar
Potapov, A., Merrill, E. and Lewis, M. A. (2012). Wildlife disease elimination and density dependence. Proceedings of the Royal Society of London Series B: Biological Sciences 279, 31393145.Google Scholar
Prentice, J. C., Marion, G., White, P. C. L., Davidson, R. S. and Hutchings, M. R. (2014). Demographic processes drive increases in wildlife disease following population reduction. PLoS ONE 9, e86563. doi: 10.1371/journal.pone.0086563 Google Scholar
Rees, E. E., Pond, B. A., Tinline, R. R. and Belanger, D. (2013). Modelling the effect of landscape heterogeneity on the efficacy of vaccination for wildlife infectious disease control. Journal of Applied Ecology 50, 881891.Google Scholar
Restif, O., Hayman, D. T. S., Pulliam, J. R. C., Plowright, R. K., George, D. B., Luis, A. D., Cunningham, A. A., Bowen, R. A., Fooks, A. R., O'Shea, T. J., Wood, J. L. N. and Webb, C. T. (2012). Model-guided fieldwork: practical guidelines for multidisciplinary research on wildlife ecological and epidemiological dynamics. Ecology Letters 15, 10831094.Google Scholar
Roberts, M. G., Smith, G. and Grenfell, B. T. (1995). Mathematical models for macroparasites of wildlife. In Ecology of Infectious Diseases in Natural Populations (ed. Grenfell, B. T. and Dobson, A. P.), pp. 177208. Cambridge University Press, Cambridge.Google Scholar
Rocke, T. E., Kingstad-Bakke, B., Berlier, W. and Osorio, J. E. (2014). A recombinant raccoon poxvirus vaccine expressing both Yersinia pestis F1 and truncated V antigens protects animals against Lethal Plague. Vaccines 2, 772784.Google Scholar
Rushmore, J., Caillaud, D., Hall, R. J., Stumpf, R. M., Meyers, L. A. and Altizer, S. (2014). Network-based vaccination improves prospects for disease control in wild chimpanzees. Journal of the Royal Society Interface 11, 20140349. doi: 10.1098/rsif.2014.0349 Google Scholar
Rushton, S. P., Gurnell, J., Lurz, P. W. W. and Fuller, R. M. (2002). Modeling impacts and costs of gray squirrel control regimes on the viability of red squirrel populations. Journal of Wildlife Management 66, 683697.Google Scholar
Ryan, S. J. and Walsh, P. D. (2011). Consequences of non-intervention for infectious disease in African great Apes. PLoS ONE 6, e29030.Google Scholar
Samuel, W. M., Pybus, M. J., Welch, D. A. and Wilke, C. J. (1992). Elk as a potential host for meningeal worm - implications for translocation. Journal of Wildlife Management 56, 629639.Google Scholar
Saunders, G., Cooke, B., McColl, K., Shine, R. and Peacock, T. (2010). Modern approaches for the biological control of vertebrate pests: an Australian perspective. Biological Control 52, 288295.Google Scholar
Scheele, B. C., Hunter, D. A., Grogan, L. F., Berger, L., Kolby, J. E., McFadden, M. S., Marantelli, G., Skerratt, L. F. and Driscoll, D. A. (2014). Interventions for reducing extinction risk in Chytridiomycosis-threatened amphibians. Conservation Biology 28, 11951205.Google Scholar
Smith, G. C., Cheeseman, C. L., Clifton-Hadley, R. S. and Wilkinson, D. (2001). A model of bovine tuberculosis in the badger Meles meles: an evaluation of control strategies. Journal of Applied Ecology 38, 509519.Google Scholar
Smith, G. C., McDonald, R. A. and Wilkinson, D. (2012). Comparing Badger (Meles meles) management strategies for reducing Tuberculosis incidence in cattle. PLoS ONE 7, e39250. doi: 10.1371/journal.pone.0039250 Google Scholar
Smith, G. C., Budgey, R. and Delahay, R. J. (2013). A simulation model to support a study of test and vaccinate or remove (TVR) in Northern Ireland. National Final Report Wildlife Management Centre, Sand Hutton, York, YO41 1LZ http://www.dardni.gov.uk/fera-tvr-modelling-report.pdf.Google Scholar
Smith, M. J., Telfer, S., Kallio, E. R., Burthe, S., Cook, A. R., Lambin, X. and Begon, M. (2009). Host-pathogen time series data in wildlife support a transmission function between density and frequency dependence. Proceedings of the National Academy of Sciences of the United States of America 106, 79057909.Google Scholar
Sterner, R. T. and Smith, G. C. (2006). Modelling wildlife rabies: transmission, economics, and conservation. Biological Conservation 131, 163179.Google Scholar
Streicker, D. G., Recuenco, S., Valderrama, W., Gomez Benavides, J., Vargas, I., Pacheco, V., Condori Condori, R. E., Montgomery, J., Rupprecht, C. E., Rohani, P. and Altizer, S. (2012). Ecological and anthropogenic drivers of rabies exposure in vampire bats: implications for transmission and control. Proceedings of the Royal Society of London Series B: Biological Sciences 279, 33843392.Google Scholar
Szilagyi, A., Scheuring, I., Edwards, D. P., Orivel, J. and Yu, D. W. (2009). The evolution of intermediate castration virulence and ant coexistence in a spatially structured environment. Ecology Letters 12, 13061316.Google Scholar
Tischendorf, L., Thulke, H. H., Staubach, C., Muller, M. S., Jeltsch, F., Goretzki, J., Selhorst, T., Muller, T., Schluter, H. and Wissel, C. (1998). Chance and risk of controlling rabies in large-scale and long-term immunized fox populations. Proceedings of the Royal Society of London Series B: Biological Sciences 265, 839846.Google Scholar
Tompkins, D. M., Dunn, A. M., Smith, M. J. and Telfer, S. (2011). Wildlife diseases: from individuals to ecosystems. Journal of Animal Ecology 80, 1938.Google Scholar
Toni, T., Welch, D., Strelkowa, N., Ipsen, A. and Stumpf, M. P. H. (2009). Approximate Bayesian computation scheme for parameter inference and model selection in dynamical systems. Journal of the Royal Society Interface 6, 187202.Google Scholar
Townsend, S. E., Lembo, T., Cleaveland, S., Meslin, F. X., Miranda, M. E., Putra, A. A. G., Haydon, D. T. and Hampson, K. (2013). Surveillance guidelines for disease elimination: a case study of canine rabies. Comparative Immunology, Microbiology and Infectious Diseases 36, 249261. doi: http://dx.doi.org/10.1016/j.cimid.2012.10.008 Google Scholar
Tripp, D. W., Rocke, T. E., Streich, S. P., Abbott, R. C., Osorio, J. E. and Miller, M. W. (2015). Apparent field safety of a raccoon poxvirus-vectored plague vaccine in free-ranging prairie dogs (Cynomys spp.), Colorado, USA. Journal of Wildlife Diseases 51, 401410.Google Scholar
Viana, M., Cleaveland, S., Matthiopoulos, J., Halliday, J., Packer, C., Craft, M. E., Hampson, K., Czupryna, A., Dobson, A. P., Dubovi, E. J., Ernest, E., Fyumagwa, R., Hoare, R., Hopcraft, J. G. C., Horton, D. L., Kaare, M. T., Kanellos, T., Lankester, F., Mentzel, C., Mlengeya, T., Mzimbiri, I., Takahashi, E., Willett, B., Haydon, D. T. and Lembo, T. (2015). Dynamics of a morbillivirus at the domestic–wildlife interface: Canine distemper virus in domestic dogs and lions. Proceedings of the National Academy of Sciences 112, 14641469.Google Scholar
Waller, L. A. (2010). Bridging gaps between statistical and mathematical modeling in ecology. Ecology 91, 35003502.CrossRefGoogle ScholarPubMed
Wasserberg, G., Osnas, E. E., Rolley, R. E. and Samuel, M. D. (2009). Host culling as an adaptive management tool for chronic wasting disease in white-tailed deer: a modelling study. Journal of Applied Ecology 46, 457466.Google Scholar
Wearing, H. J., Rohani, P. and Keeling, M. J. (2005). Appropriate models for the management of infectious diseases. Plos Medicine 2, 621627.Google Scholar
Wells, K., Brook, B. W., Lacy, R. C., Mutze, G. J., Peacock, D. E., Sinclair, R. G., Schwensow, N., Cassey, P., O'Hara, R. B. and Fordham, D. A. (2015). Timing and severity of immunizing diseases in rabbits is controlled by seasonal matching of host and pathogen dynamics. Journal of the Royal Society Interface 12, 2014118420141184.Google Scholar
White, P. J., Norman, R. A. and Hudson, P. J. (2002). Epidemiological consequences of a pathogen having both virulent and avirulent modes of transmission: the case of rabbit haemorrhagic disease virus. Epidemiology and infection 129, 665677.Google Scholar
Wild, G., Gardner, A. and West, S. A. (2009). Adaptation and the evolution of parasite virulence in a connected world. Nature 459, 983986.Google Scholar
Wilkinson, D., Smith, G. C., Delahay, R. J. and Cheeseman, C. L. (2004). A model of bovine tuberculosis in the badger Meles meles: an evaluation of different vaccination strategies. Journal of Applied Ecology 41, 492501.Google Scholar
Williams, C. K., Davey, C. C., Moore, R. J., Hinds, L. A., Silvers, L. E., Kerr, P. J., French, N., Hood, G. M., Pech, R. P. and Krebs, C. J. (2007). Population responses to sterility imposed on female European rabbits. Journal of Applied Ecology 44, 291301.Google Scholar
Wobeser, G. (2002). Disease management strategies for wildlife. Revue Scientifique Et Technique De L Office International Des Epizooties 21, 159178.Google Scholar
Wolfe, L. L., Miller, M. W. and Williams, E. S. (2004). Feasibility of “test-and-cull” for managing chronic wasting disease in urban mule deer. Wildlife Society Bulletin 32, 500505.Google Scholar
Woods, G. M., Kreiss, A., Belov, K., Siddle, H. V., Obendorf, D. L. and Muller, H. K. (2007). The immune response of the Tasmanian Devil (Sarcophilus harrisii) and Devil Facial Tumour Disease. EcoHealth 4, 338345.Google Scholar
Woolhouse, M. E. J., Webster, J. P., Domingo, E., Charlesworth, B. and Levin, B. R. (2002). Biological and biomedical implications of the co-evolution of pathogens and their hosts. Nature Genetics 32, 569577.Google Scholar