Biodiversity & Conservation

, Volume 7, Issue 6, pp 705–723 | Cite as

Sterilization as an alternative strategy to control wildlife diseases: bovine tuberculosis in European badgers as a case study

  • F. A. M. Tuyttens
  • D. W. Macdonald


Sterilization has rarely been considered as an alternative to culling or vaccination to control wildlife diseases. Disease control by sterilization, as by culling, has most promise when the host'ss ability for compensatory growth following the removal of density-dependent inhibitions is limited, and when moderate reductions in population density cause disproportionately large reductions in disease prevalence, or even eliminate the disease. For many host/disease examples this will not be the case and vaccination may have overwhelming advantages or may be the only practical option. The impact of sterilization on host density and disease prevalence will develop relatively slowly because sterilization can prevent the recruitment of only one age-cohort at a time. Moreover, unless there is vertical transmission, this age-cohort will consist only of susceptibles. Culling, on the contrary, removes infected as well as susceptible animals. However, for certain disease/host examples, the r elative effectiveness of the different control strategies may be altered considerably if their variable effects on the probability of disease transmission are taken into account. Social perturbation or stress could render certain culling strategies ineffective or even counter-productive. Depending on how disease dynamics are influenced by the host'ss age-structure and reproductive investment, fertility control could offer epidemiological advantages that have been ignored by most disease/host models. We illustrate some of these principles by investigating the theoretical and practical feasibility of an hypothetical sterilization campaign to control bovine tuberculosis in badgers (and hence cattle) in Britain.

Meles meles Mycobacterium bovis fertility control wildlife disease population control 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Anderson, R.M. and May, R.M. (1979) Population biology of infectious diseases: Part I. Nature 280, 361–7.Google Scholar
  2. Anderson, R.M. and May, R.M. (1981) The population dynamics of microparasites and their invertebrate hosts. Phil. Trans. Roy. Soc. Lond. Series B291, 451–524.Google Scholar
  3. Anderson, R.M. and Trewhella, W. (1985) Population dynamics of the badger (Meles meles) and the epidemiology of bovine tuberculosis (Mycobacterium bovis). Phil. Trans. Roy. Soc. Lond. Series B310, 327–81.Google Scholar
  4. Anderson, R.M., Jackson, H.C., May, R.M. and Smith, A. (1981) Population dynamics of fox rabies in Europe. Nature 289, 765–71.Google Scholar
  5. Artois, M. (1997) Managing problem wildlife in the ‘Old World’: a veterinary perspective. J. Reprod. Fertil. Dev. 9, 17–26.Google Scholar
  6. Aubert, M. (1994) Control of rabies in foxes: what are the appropriate measures? Vet. Rec. 134, 55–9.Google Scholar
  7. Bacon, P.J. (1985a) A systems analysis of wildlife rabies epizootics. In Population Dynamics of Rabies in Wildlife (P.J. Bacon, ed.) pp. 109–130. London: Academic Press.Google Scholar
  8. Bacon, P.J. (1985b) Discrete time temporal models of rabies. In Population Dynamics of Rabies in Wildlife (P.J. Bacon, ed.) pp. 148–196. London: Academic Press.Google Scholar
  9. Bacon, P.J. and Macdonald, D.W. (1980) To control rabies: vaccinate foxes. New Sci. 87, 640–5.Google Scholar
  10. Bailey, N.T.J. (1975) The Mathematical Theory of Infectious Diseases. London: Griffin.Google Scholar
  11. Ball, F.G. (1985) Spatial models for the spread and control of rabies incorporating group size. In Population Dynamics of Rabies in Wildlife (P.J. Bacon, ed.) pp. 197–222. London: Academic Press.Google Scholar
  12. Barlow, N.D. (1991a) A spatially aggregated disease/host model for bovine TB in New Zealand possum populations. J. Appl. Ecol. 28, 777–93.Google Scholar
  13. Barlow, N.D. (1991b) Control of endemic bovine TB in New Zealand possum populations: results from a simple model. J. Appl. Ecol. 28, 794–809.Google Scholar
  14. Barlow, N.D. (1996) The ecology of wildlife disease control: simple models revisited. J. Appl. Ecol. 33, 303–14.Google Scholar
  15. Bell, G. and Koufopanou, V. (1986) The cost of reproduction. Oxford Surv. Evol. Biol. 3, 83–131.Google Scholar
  16. Bernton, E.W., Meltzer, M.S. and Holaday, J.W. (1988) Suppression of macrophage activation and T-lymphocyte function in hypoprolactinemic mice. Science 354, 401–4.Google Scholar
  17. Bomford, M. (1990) A role for fertility control in wildlife management? Bureau of Rural Resources Bulletin no. 7, Australian Government Publishing Service, Canberra, Australia.Google Scholar
  18. Brown, D.H. and Zwilling, B.S. (1994) Activation of the hypothalamic-pituitary-adrenal axis differentially affects the anti-mycobacterial activity of macrophages from BCG-resistant and susceptible mice. J. Neuroimmunol. 53, 181–7.Google Scholar
  19. Caughley, G., Pech, R. and Grice, D. (1992) Effect of fertility control on a population’s productivity. Wildlife Res. 19, 623–7.Google Scholar
  20. Cheeseman, C.L., Jones, G.W., Gallagher, J. and Mallinson, P.J. (1981) The population structure, density and prevalence of tuberculosis (Mycobacterium bovis) in badgers (Meles meles) from four areas in south-west England. J. Appl. Ecol. 18, 795–804.Google Scholar
  21. Cheeseman, C.L., Wilesmith, J.W. and Stuart, F.A. (1989) Tuberculosis: the disease and its epidemiology in the badger, a review. Epidemiol. Infect. 103, 113–25.Google Scholar
  22. Cheeseman, C.L., Mallinson, P.J., Ryan, J. and Wilesmith, J.W. (1993) Recolonisation by badgers in Gloucestershire. In The Badger (T.J. Hayden, ed.) pp. 78–93. Dublin: Royal Irish Academy.Google Scholar
  23. Christian, S.F. (1993) Behavioural ecology of the Eurasian badger (Meles meles): space use, territoriality and social behaviour. PhD Thesis, University of Sussex, UK.Google Scholar
  24. Clifton-Hadley, R.S., Sayers, A.R. and Stock, M.P. (1995a) Evaluation of an ELISA for Mycobacterium bovis infection in badgers (Meles meles). Vet. Rec. 137, 555–8.Google Scholar
  25. Clifton-Hadley, R.S., Wilesmith, J.W., Richards, M.S., Upton, P. and Johnston, S. (1995b) The occurrence of Mycobacterium bovis infection in cattle in and around an area subject to extensive badger (Meles meles) control. Epidemiol. Infect. 114, 179–93.Google Scholar
  26. Clutton-Brock, T.H. (1991) The Evolution of Parental Care. Princeton: Princeton University Press.Google Scholar
  27. Coyne, M.J., Smith, G. and McAllister, F.E. (1989) Mathematical model for the population biology of rabies in raccoons in the mid-Atlantic states. Am. J. Vet. Res. 50, 2148–54.Google Scholar
  28. De Jong, M.C.M., Diekman, O. and Heesterbeek, J.A.P. (1995) How does transmission of infection depend on population size? In Epidemic Models, their Structure and Relation to Data (D. Mollison, ed.) pp. 84–94. Cambridge: Cambridge University Press.Google Scholar
  29. Djiane, J. and Kelly, P.A. (1993) Prolactin. In Reproduction in Mammals and Man (C. Thibault et al., eds) pp. 121–133. Paris: Ellipses.Google Scholar
  30. Doncaster, C.P. and Macdonald, D.W. (1996) Interspecific variation in the movement behaviour of foxes (Vulpes vulpes): a reply to White, Saunders and Harris. J. Animal Ecol. 65, 126–7.Google Scholar
  31. Dunnet, G.M., Jones, D.M. and McInerney, J.P. (1986) Badgers and Bovine Tuberculosis-Review of Policy. London: HMSO.Google Scholar
  32. Fagan, J. (1993) Tuberculosis in badgers in Ireland: pathology. In The Badger (T.J. Hayden, ed.) pp. 117–122. Dublin: Royal Irish Academy.Google Scholar
  33. Gao, Y. and Short, R.V. (1993) The control of rodent populations. Oxford Rev. Reproduct. Biol. 15, 265–310.Google Scholar
  34. Garrott, R.A. (1995) Effective management of free-ranging ungulate populations using contraception. Wildlife Soc. Bull. 23, 445–52.Google Scholar
  35. Goodger, J., Nolan, A., Russel, W.P. et al. (1994) Serodiagnosis of Mycobacterium bovis infection in badgers: development of an indirect ELISA using a 25 kDA antigen. Vet. Rec. 135, 82–5.Google Scholar
  36. Hayden, T.J. (1993) The badger: epidemiological darkness is plight enough. In The Badger (T.J. Hayden, ed.) pp. 196–211. Dublin: Royal Irish Academy.Google Scholar
  37. Hedge, U.C. (1991) Immunomodulation of the mother during pregnancy. Med. Hypoth. 35, 159–64.Google Scholar
  38. Ishigami T. (1991) The influence of psychic acts on the progress of pulmonary tuberculosis. Am. Rev. Tuber. Pulmon. Dis. 2, 470–84.Google Scholar
  39. Jöchle, W. and Jöchle, M. (1993) Reproduction in a feral cat population and its control with a prolactin inhibitor, cabergoline. J. Reprod. Fertil. Suppl 47, 419–24.Google Scholar
  40. Kermack, W.O. and McKendrick, A.G. (1927) Contributions to the mathematical theory of epidemics, part I. Proc. Roy. Soc. Edin. A 115, 700–21.Google Scholar
  41. Khansari, D.N., Murgo, A.J. and Faith, R.E. (1990) Effects of stress on the immune system. Immunol. Today 11, 170–5.Google Scholar
  42. King, E.G., Lovell, D.J. and Harris, S. (in press) Effect of climate on the survival of Mycobacterium bevis and its transmission to cattle herds in south west Bntain. In proceedings of the First European Vertebrate Pest Management Conference, University of York, 1-3 September 1997.Google Scholar
  43. Lettelier, C., Fizet, D., Baltz, T. and Vezon, G. (1994) Immunosuppressive activity of sera of pregnant women on cytotoxic T-lymphocyte-mediated cytolysis. Gynecol. Obstet. Invest. 37, 1–5.Google Scholar
  44. Little, T.W.A., Swan, C., Thompson, H.V. and Wilesmith, J.W. (1982) Bovine tuberculosis in domestic and wild mammals in an area of Dorset. II. The badger population, its ecology and tuberculosis status. J. Hyg. 89, 211–24.Google Scholar
  45. Luft, B.J. and Remington, J.S. (1982) Effect of pregnancy on resistance to Listeria monocytogenes and Toxoplasma gondii infections in mice. Infect. Immun. 38, 1164–71.Google Scholar
  46. Macdonald, D.W. (1995) Wildlife rabies: the implications of Britain-unresolved questions for the control of wildlife rabies: social perturbation and interspecific interactions. In Rabies in a Changing World, Proceedings of the British Small Animal Veterinary Association, Cheltenham, UK.Google Scholar
  47. MAFF (Ministry of Agriculture, Fisheries and Food) (1976-1997) Bovine Tuberculosis in Badgers, 1st-20th Report. London: MAFF Publications.Google Scholar
  48. Marks, C.A., Nijk, M., Gigliotti, F., Busana, F. and Short, R.V. (1996) Field assessment of a cabergoline baiting campaign for reproductive control of the red fox (Vulpes vulpes). Wildlife Res. 23, 161–8.Google Scholar
  49. May, R.M. and Anderson, R.M. (1979) Population biology of infectious diseases: Part II. Nature 280, 455–61.Google Scholar
  50. McAleer, P.D. (1990) The relationship between badger density and the incidence of bovine tuberculosis in County Galway. Irish Vet. J. 43, 77–80.Google Scholar
  51. McCarthy, J. (1993) The badger vaccination trial in West Cork: progress report. In The Badger (T.J. Hayden, ed.) pp. 181–188. Dublin: Royal Irish Academy.Google Scholar
  52. Mollison, D. (1984) Simplifying simple epidemic models. Nature 310, 224–5.Google Scholar
  53. Mollison, D. (1985) Sensitivity analysis of simple endemic models. In Population Dynamics of Rabies in Wildlife (P.J. Bacon, ed.) pp. 223–234. London: Academic Press.Google Scholar
  54. Morris, R.S. and Pfeiffer, D.U. (1991) Bovine tuberculosis complicated by feral reservoir: is there an answer? Symposium on Tuberculosis, Massey University, Palmerstown North, New Zealand.Google Scholar
  55. Muirhead, R.H., Gallagher, J. and Burn K.J. (1974) Tuberculosis in wild badgers in Gloucestershire: epidemiology. Vet. Rec. 95, 552–5.Google Scholar
  56. Neal, E. (1986) The Natural History of the Badger. London: Croom Helm.Google Scholar
  57. Nettles, V.F. (1997) Potential consequences and problems with wildlife contraceptives. J. Reprod. Fertil. Dev. 9, 137–44.Google Scholar
  58. Neville, P.F. and Remfry, J. (1984) Effect of neutering on two groups of feral cats. Vet. Rec. 114, 447–50.Google Scholar
  59. Nolan, A. and Wilesmith, J.W. (1994) Tuberculosis in badgers (Meles meles). Vet. Microbiol. 40, 179–91.Google Scholar
  60. O’Corry-Crowe, G., Eves, J. and Hayden, T.J. (1993) Sett distribution, territory size and population density of badgers (Meles meles) in east Offaly. In The Badger (T.J. Hayden, ed.) pp. 35–56. London: Academic Press.Google Scholar
  61. O’Reilly, L.M. and Daborn, C.J. (1995) The epidemiology of Mycobacterium bovis infections in animals and man: a review. Tubercle Lung Dis. 76 (suppl. 1), 1–46.Google Scholar
  62. Pech, R.P. and Hone, J. (1988) A model for the dynamics and control of an outbreak of foot and mouth disease in feral pigs in Australia. J. Appl. Ecol. 25, 63–77.Google Scholar
  63. Pech, R.P. and McIllroy, J.C. (1990) A model of the velocity of advance of foot and mouth disease in feral pigs. J. Appl. Ecol. 27, 635–50.Google Scholar
  64. Rasheed, F.N., Bulmer, J.N., De Francisco, A. et al. (1995) Relationships between maternal malaria and malarial responses in mothers and neonates. Parasite Immunol. 17, 1–10.Google Scholar
  65. Roberts, M.G. (1992) The dynamics and control of bovine tuberculosis in possums. IMA J. Math. Appl. Med. Biol. 9, 19–28.Google Scholar
  66. Roberts, M.G. (1996) Bovine tuberculosis in possum populations, and its eradication or control by culling or vaccination. J. Animal Ecol. 65, 451–64.Google Scholar
  67. Roper, T.J. and Lüps, P. (1993) Disruption of territorial behaviour in badgers Meles meles. Z. Saugetierkunde 58, 252–5.Google Scholar
  68. Saunders, I.W. (1980) A model for myxomatosis. Math. Biosci. 48, 1–15.Google Scholar
  69. Saunders, G. and McIlroy, J. (1996) The effect of imposed sterility on the survival, fecundity, territoriality and social structure of foxes. Fourth International Conference on Fertility Control for Wildlife Management, 8-11 July, Great Keppel Island, Great Barrier Reef, Queensland, Australia.Google Scholar
  70. Sherwin, B. (1990) enetic implications of reduced fertility. Fertility Control in Wildlife Conference 21-24 November, Melbourne, Australia.Google Scholar
  71. Smith, A.D.M. (1985) A continuous time deterministic model of temporal rabies. In Population Dynamics of Rabies in Wildlife (P.J. Bacon, ed.) pp. 131–145. London: Academic Press.Google Scholar
  72. Smith, P., Moore, H.D. and Cowan, D.P. (1995) Review of the potential of immunocontraceptives for wildlife management in the UK, Project No. VC0403, MAFF, UK.Google Scholar
  73. Stanford, J., Stainsby, K. and Mahmood, K.H. (1993) Could vaccination be the answer to badger tuberculosis problem? In The Badger (T.J. Hayden, ed.) pp. 174–180. Dublin: Royal Irish Academy.Google Scholar
  74. Stewart, P. (1997) The social behaviour of the European badger, Meles meles. DPhil. Thesis, University of Oxford, Oxford.Google Scholar
  75. Swinton, J., Tuyttens, F.A.M., Macdonald, D.W. and Cheeseman, C.L. (1997) Social perturbation and bovine tuberculosis in badgers: fertility control and lethal control compared. Phil. Trans. Roy. Soc. Lond. Series B 352, 619–31.Google Scholar
  76. Szekeres-Bartho, J. (1990) Endocrine regulation of the immune system during pregnancy. Arch. Immunol. Therap. Experiment. 38, 126–40.Google Scholar
  77. Thong, Y.H., Steele, R.W., Vincent, M.M., Hensen, S.A. and Bellanti, J.A. (1973) Impaired in vitro cell-mediated immunity to rubella virus during pregnancy. N. Engl. J. Med. 289, 604–6.Google Scholar
  78. Tinline, R.R. (1988) Persistence of rabies in widlife. In Rabies (J.B. Campbell and K.M. Charlton, eds) pp. 301–322. Boston: Kluwer Academic Press.Google Scholar
  79. Tuyttens, F.A.M. (1996) Badgers and bovine tuberculosis. In The WildCRU Review: the Tenth Anniversary Report of the Wildlife Conservation Research Unit at Oxford University (D.W. Macdonald and F.H. Tattershall, eds) pp. 168–174. Oxford: WildCRU.Google Scholar
  80. Tuyttens, F.A.M. and Macdonald, D.W. (in press) Fertility control: On option for non-lethal control of wild carnivores? Animal Welfare.Google Scholar
  81. Tuyttens, F.A.M., Macdonald, D.W. and Cheeseman, C.L. (1997a) The evolution and function of territorial scent-marking behaviour in the Eurasian badger (Meles meles). Fourth Benelux Congress of Zoology, Utrecht, 14-15 November 1997.Google Scholar
  82. Tuyttens, F.A.M., Macdonald, D.W. and Cheeseman, C.L. (1997b) How removal experiments can help to test hypotheses about territoriality in badger and other mammals. Seventh International Theriological Congress, Acapulco (Mexico), 6-11 September 1997.Google Scholar
  83. van Zon, A.A.J.C. and Eling, W.M.C. (1980) Depressed malarial immunity in pregnant mice. Infect. Immun. 28, 630–2.Google Scholar
  84. VBC (Vertebrate Biocontrol Centre) (1994) The cooperative Research Centre for Biological Control of Vertebrate Pest Populations: Annual Report 1993-1994. Lyneham, Australia.Google Scholar
  85. Verstegen, J.P.L., Onclin, K., Silva, L.D.M. and Donnay, I. (1993) Abortion induction in the cat using prostaglandin F and a new anti-prolactinic agent, cabergoline. J. Reprod. Fertil. suppl. 47, 411–7.Google Scholar
  86. Waltman, P. (1974) Deterministic threshold models in the theory of epidemics. Lecture Notes in Biomathics 1. New York: Springer.Google Scholar
  87. White, P.C.L. and Harris, S. (1995a) Bovine tuberculosis in badger (Meles meles) populations in southwest England: the use of spatial stochastic simulation model to understand the dynamics of the disease. Phil. Trans. Roy. Soc. Lond. Series B349, 391–413.Google Scholar
  88. White, P.C.L. and Harris, S (1995b) Bovine tuberculosis in badger (Meles meles) populations in southwest England: an assessment of past, present and possible future control strategies using simulation modelling. Phil. Trans. Roy. Soc. Lond. Series B349, 415–432.Google Scholar
  89. Wilesmith, J.W. (1983) Epidemiological features of bovine tuberculosis in cattle herds in Great Britain. J. Hyg. 90, 159–76.Google Scholar
  90. Wilesmith, J.W. (1991) Control of disease in the presence of wildlife: the TB example. Symposium on Tuberculosis. Publication no. 132, Veterinary Continuing Education, Palmerston North, New Zealand.Google Scholar
  91. Woodroffe, R. (1992) Factors affecting reproductive success in the European badger, Meles meles L. DPhil. Thesis, University of Oxford, Oxford.Google Scholar
  92. Zemlicka, D.E. (1993) Evaluation of tubal ligation and vasectomy on pair-bond and territorial display behaviors in captive coyotes. Symposium on Contraception in Wildlife Management 26-28 October, Denver.Google Scholar

Copyright information

© Kluwer Academic Publishers 1998

Authors and Affiliations

  • F. A. M. Tuyttens
    • 1
  • D. W. Macdonald
    • 1
  1. 1.Wildlife Conservation Research Unit, Department of ZoologyUniversity of OxfordOxfordUK

Personalised recommendations