• Peter Kerr
Part of the NATO Security through Science Series book series


The introduction of myxoma virus into Australia to control the European rabbit is the classical example of biological control for a vertebrate pest species. The subsequent selection for reduction in virulence of myxoma virus strains and the increased resistance to myxoma virus of the new host is one of the paradigms for infectious disease biology. More recently, rabbit hemorrhagic disease virus has also been successfully introduced into Australia as a second biological control agent for rabbits and has been highly effective in the arid and semi-arid parts of the continent but less so in the higher rainfall zones. The use of biotechnology for vertebrate pest control has been explored through projects to develop virally vectored immunocontraceptives for rabbits, foxes, and mice, and although much progress has been made, it must be concluded that there is still a large gap betweenwhat biotechnology can deliver and what is needed for successful biological control of vertebrate pest species. The release of any biological control agentwhether a naturally occurring virus or a genetically engineered organism requires very careful evaluation of the risks and benefits and two examples of this process are discussed.


Biological Control Zona Pellucida Recombinant Virus Cane Toad Wild Rabbit 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. 1.
    F. Fenner and B. Fantini, Biological Control of Vertebrate Pests. The History of Myxomatosis—An Experiment in Evolution (CAB International, New York, 1999).Google Scholar
  2. 2.
    E. C. Rolls, They All Ran Wild (Angus and Robertson, Melbourne, 1969).Google Scholar
  3. 3.
    B. D. Cooke and F. Fenner, Rabbit haemorrhagic disease and the biological control of wild rabbits, Oryctolagus cuniculus, in Australia and New Zealand, Wildl. Res. 29, 689–706 (2002).CrossRefGoogle Scholar
  4. 4.
    P. J. J. Van Rensburg, J. D. Skinner, and R. J. Van Aarde, Effects of feline panleucopaenia on the population characteristics of feral cats on Marion Island, J. App. Ecol. 24, 63–73 (1987).CrossRefGoogle Scholar
  5. 5.
    K. Myers, I. Parer, D. Wood, and B. D. Cooke, The rabbit in Australia, in The European Rabbit. The History and Biology of a Successful Colonizer, edited by H. V. Thompson and C. M. King (Oxford University Press, Oxford, 1999), pp. 108–157.Google Scholar
  6. 6.
    A. E. Newsome, I. A. Parer, and P. Catling, Prolonged prey suppression by carnivores: Predator-removal experiments, Oecologia 78, 458–467 (1989).CrossRefGoogle Scholar
  7. 7.
    K. Williams, I. Parer, B. Coman, J. Burley, and M. Braysher, Managing Vertebrate Pests: Rabbits (Australian Government Publishing Services, Canberra, 1995).Google Scholar
  8. 8.
    F. Fenner and F. N. Ratcliffe, Myxomatosis (Cambridge University Press, Cambridge, 1965).Google Scholar
  9. 9.
    F. Fenner and I. D. Marshall, A comparison of the virulence for European rabbits (Oryctolagus cuniculus) of strains of myxoma virus recovered in the field in Australia, Europe and America, J. Hyg. (Camb.) 55, 149–151 (1957).Google Scholar
  10. 10.
    F. Fenner, M. F. Day, and G. M. Woodroofe, Epidemiological consequences of the mechanical transmission of myxomatosis by mosquitoes, J. Hyg. (Camb.) 54, 285–303 (1956).Google Scholar
  11. 11.
    I. D. Marshall, The influence of ambient temperature on the course of myxomatosis in rabbits, J. Hyg. (Camb.) 57, 484–497 (1959).Google Scholar
  12. 12.
    I. D. Marshall and F. Fenner, Studies in the epidemiology of infectious myxomatosis of rabbits, V: Changes in the innate resistance of wild rabbits between 1951 and 1959, J. Hyg. (Camb.) 56, 288–302 (1958).Google Scholar
  13. 13.
    I. D. Marshall and G. W. Douglas, Studies in the epidemiology of infectious myxomatosis of rabbits, VIII: Further observations on changes in the innate resistance of Australian wild rabbits exposed to myxomatosis, J. Hyg. (Camb.) 59, 117–122 (1961).Google Scholar
  14. 14.
    K. M. Saint, N. French, and P. Kerr, Genetic variation in Australian isolates of myxoma virus: an evolutionary and epidemiological study, Arch. Virol. 146, 1105–1123 (2001).PubMedCrossRefGoogle Scholar
  15. 15.
    P. J. Kerr, J. M. Merchant, L. Silvers, G. Hood, and A. J. Robinson, Monitoring the spread of myxoma virus in rabbit populations in the southern tablelands of New South Wales, Australia, II: Selection of a virus strain that was transmissible and could be monitored by polymerase chain reaction, Epidemiol. Infect. 130, 123–133 (2003).PubMedCrossRefGoogle Scholar
  16. 16.
    P. J. Kerr and S. M. Best, Myxoma virus in rabbits, Rev. Sci. Technol. Off. Int. Epiz. 17, 256–268 (1998).Google Scholar
  17. 17.
    L. Capucci, P. Fusi, A. Lavazza, M. L. Pacciarini, and C. Rossi, Detection and preliminary characterization of a new calicivirus related to rabbit haemorrhagic disease virus but non pathogenic, J. Virol. 70, 8614–8623 (1996).PubMedGoogle Scholar
  18. 18.
    S. R. Moss, S. L. Turner, R. C. Trout, P. J. White, P. J. Hudson, A. Desai, M. Armesto, N. L. Forrester, and E. A. Gould, Molecular epidemiology of rabbit haemorrhagic disease virus, J. Gen. Virol. 83, 2461–2467 (2002).PubMedGoogle Scholar
  19. 19.
    N. L. Forrester, R. C. Trout, S. L. Turner, D. Kelly, B. Boag, S. Moss, and E. A. Gould, Unraveling the paradox of rabbit haemorrhagic disease virus emergence, using phylogenetic analysis; possible implications for rabbit conservation strategies, Biol. Conserv. 131, 296–306 (2006).CrossRefGoogle Scholar
  20. 20.
    B. D. Cooke, S. McPhee, A. J. Robinson, and L. Capucci, Rabbit haemorrhagic disease: Does a pre-existing RHDV-like virus reduce the effectiveness of RHD as a biological control in Australia, Wildl. Res. 29, 673–682 (2002).CrossRefGoogle Scholar
  21. 21.
    A. J. Robinson, P. D. Kirkland, R. I. Forrester, L. Capucci, B. D. Cooke, and A. W. Philbey, Serological evidence for the presence of a calicivirus in Australian wild rabbits, Oryctolagus cuniculus, before the introduction of rabbit haemorrhagic disease virus (RHDV): Its potential influence on the specificity of a competitive ELISA for RHDV, Wildl. Res. 29, 655–652 (2002).CrossRefGoogle Scholar
  22. 22.
    S. Marchandeau, G. Le Gall-Recule, S. Bertagnoli, J. Aubineau, G. Botti, and A. Lavazza, Serological evidence for a non-protective RHDV-like virus, Vet. Res. 36, 53–62 (2005).PubMedCrossRefGoogle Scholar
  23. 23.
    P. J. White, R. A. Norman, and P. J. Hudson, Epidemiological consequences of a pathogen having both virulent and avirulent modes of transmission: the case of rabbit haemorrhagic disease virus, Epidemiol. Infect. 129, 665–677 (2002).PubMedCrossRefGoogle Scholar
  24. 24.
    G. Mutze, P. I. Bird, J. Kovaliski, D. Peacock, S. Jennings, and B. D. Cooke, Emerging epidemiological patterns in rabbit haemorrhagic disease, its interactions with mxyomatosis, and their effects on rabbit populations in South Australia, Wildl. Res. 29, 577–590 (2002).CrossRefGoogle Scholar
  25. 25.
    J. Read and Z. Bowen, Population dynamics, diet and aspects of the biology of feral cats and foxes in arid South Australia, Wildl. Res. 28, 195–203 (2001).CrossRefGoogle Scholar
  26. 26.
    J. S. O’Keefe, J. E. Tempero, M. X. J. Motha, M. F. Hansen, and P. H. Atkinson, Serology of rabbit haemorrhagic disease virus in wild rabbits before and after the release of the virus in New Zealand, Vet. Microbiol. 66, 29–40 (1999).PubMedCrossRefGoogle Scholar
  27. 27.
    J. P. Parkes, G. L. Norbury, R. P. Heyward, and G. Sullivan, Epidemiology of rabbit haemorrhagic disease (RHD) in the South Island, New Zealand, 1997–2001, Wildl. Res. 29, 543–555 (2002).CrossRefGoogle Scholar
  28. 28.
    A. J. Robinson, P. T. M. So, W. J. Muller, B. D. Cooke, and L. Capucci, Statistical models for the effect of age and maternal antibodies on the development of rabbit haemorrhagic disease in Australian wild rabbits, Wildl. Res. 29, 663–671 (2002).CrossRefGoogle Scholar
  29. 29.
    G. Oogjes, Ethical aspects and dilemmas of fertility control of unwanted wildlife: An animal welfarist’s perspective, Reprod. Fertil. Dev. 9, 163–168 (1997).PubMedCrossRefGoogle Scholar
  30. 30.
    S. K. Gupta, N. Srivastava, S. Choudhury, A. Rath, N. Sivapurapu, G. K. Gahlay, and D. Batra, Update on zona pellucida glycoproteins based contraceptive vaccine, J. Reprod. Immunol. 62, 79–89 (2004).PubMedCrossRefGoogle Scholar
  31. 31.
    C. H. Tyndale-Biscoe, Virus-vectored immunocontraception of feral mammals, Reprod. Fertil. Dev. 6, 9–16 (1994).CrossRefGoogle Scholar
  32. 32.
    R. J. Jackson, D. J. Maguire, L. A. Hinds, and I. A. Ramshaw, Infertility in mice induced by a recombinant ectromelia virus expressing mouse zona pellucida glycoprotein 3, Biol. Reprod. 58, 152–159 (1998).PubMedCrossRefGoogle Scholar
  33. 33.
    M. L. Lloyd, G. R. Shellam, J. M. Papadimitriou, and M. A. Lawson, Immunocontraception is induced in BALB/c mice inoculated with murine cytomegalovirus expressing mouse zona pellucida 3, Biol. Reprod. 68, 2024–2032 (2003).PubMedCrossRefGoogle Scholar
  34. 34.
    G. R. Shellam, The potential of murine cytomegalovirus as a viral vector for immunocontraception, Reprod. Fertil. Dev. 6, 129–137 (1994).CrossRefGoogle Scholar
  35. 35.
    L. N. Farroway, G. R. Singleton, M. A. Lawson, and D. A. Jones, The impact of murine cytomegalovirus (MCMV) on enclosure populations of house mice (Mus domesticus), Wildl. Res. 29, 1–17 (2002).CrossRefGoogle Scholar
  36. 36.
    A. D. Arthur, R. P. Pech, and G. R. Singleton, Predicting the effect of immunocontraceptive recombinant murine cytomegalovirus on population outbreaks of house mice (Mus musculus domesticus) in mallee wheatlands, Wildl. Res. 32, 631–637 (2005).CrossRefGoogle Scholar
  37. 37.
    P. J. Kerr and R. J. Jackson, Myxoma virus as a vaccine vector for rabbits: antibody levels to influenza virus haemagglutinin presented by a recombinant myxoma virus, Vaccine 13, 1722–1726 (1995).PubMedCrossRefGoogle Scholar
  38. 38.
    P. J. Kerr, R. J. Jackson, A. J. Robinson, J. Swan, L. Silvers, N. French, H. Clarke, D. F. Hall, and M. K. Holland, Infertility in female rabbits (Oryctolagus cuniculus) alloimmunized with the rabbit zona pellucida protein ZPB either as a purified recombinant protein or expressed by recombinant myxoma virus, Biol. Reprod. 61, 601–613 (1999).CrossRefGoogle Scholar
  39. 39.
    S. M. Mackenzie, E. A. McLaughlin, H. D. Perkins, N. French, T. Sutherland, R. J. Jackson, B. Inglis, W. J. Muller, B. H. van Leeuwen, A. J. Robinson, and P. J. Kerr, The immunocontraceptive effects on female rabbits (Oryctolagus cuniculus) infected with recombinant myxoma virus expressing rabbit ZP2 and ZP3, Biol. Reprod. 74, 511–521 (2006).PubMedCrossRefGoogle Scholar
  40. 40.
    R. J. Russell and S. J. Robbins, Cloning and molecular characterization of the myxoma virus genome, Virology 170, 147–159 (1989).PubMedCrossRefGoogle Scholar
  41. 41.
    S. M. Best and P. J. Kerr, Coevolution of host and virus: The pathogenesis of virulent and attenuated strains of myxoma virus in resistant and susceptible European rabbits, Virology 267, 36–48 (2000).PubMedCrossRefGoogle Scholar
  42. 42.
    D. M. Wood, C. Liu, and B. S. Dunbar, Effect of alloimmunization and heteroimmunization with zonae pellucidae on fertility in rabbits, Biol. Reprod. 25, 439–450 (1981).PubMedCrossRefGoogle Scholar
  43. 43.
    S. M. Skinner, T. Mills, H. J. Kirchick, and B. S. Dunbar, Immunization with zona pellucida proteins results in abnormal ovarian follicular differentiation and inhibition of gonadotropin-induced steroid secretion, Endocrinology 115, 2418–2432 (1984).PubMedCrossRefGoogle Scholar
  44. 44.
    L. E. Twigg and C. K. Williams, Fertility control of overabundant species; can it work for feral rabbits?, Ecology Letters 2, 281–285 (1999).CrossRefGoogle Scholar
  45. 45.
    L. E. Twigg, T. J. Lowe, G. R. Martin, A. G. Wheeler, G. S. Gray, S. L. Griffin, C. M. O’Reilly, D. J. Robinson, and P. H. Hubach, Effects of surgically imposed sterility on free-ranging rabbit populations, J. Appl. Ecol. 37, 16–39 (2000).CrossRefGoogle Scholar
  46. 46.
    C. K. Williams, C. C. Davey, R. J. Moore, L. A. Hinds, L. E. Silvers, P. J. Kerr, N. French, G. M. Hood, R. P. Pech, and C. J. Krebbs, Populations responses to sterility imposed on female European rabbits, J. Appl. Ecol., in press.Google Scholar
  47. 47.
    J. M. Merchant, P. J. Kerr, N. Simms, G. M. Hood, R. Pech, and A. J. Robinson, Monitoring the spread of myxoma virus in rabbit (Oryctolagus cuniculus) populations on the southern tablelands of New South Wales, Australia, III: Release, persistence and rate of spread of an identifiable strain of myxoma virus, Epidemiol. Infect. 130, 135–147 (2003).PubMedCrossRefGoogle Scholar
  48. 48.
    G. H. Reubel, S. Beaton, D. Venables, J. Pekin, J. Wright, N. French, and C. M. Hardy, Experimental inoculation of European red foxes with recombinant vaccinia viruses expressing zona pellucida C proteins, Vaccine 23, 4417–4426 (2005).PubMedCrossRefGoogle Scholar
  49. 49.
    T. Strive, C. M. Hardy, N. French, J. D. Wright, N. Nagaraja, and G. H. Reubel, Development of canine herpesvirus based antifertility vaccines for foxes using bacterial artificial chromosomes, Vaccine 24, 980–988 (2006).PubMedCrossRefGoogle Scholar
  50. 50.
    A. D. Hyatt, H. Parkes, and Z. Zupanovic, Identification, Characterization and Assessment of Venezuelan Viruses for Potential Use As Biological Control Agents Against the Cane Toad (Bufo marinus) in Australia: A Report from the Australian Animal Health Laboratory (CSIRO, Geelong, Australia, 1998).Google Scholar
  51. 51.
    G. M. Maniatis, L. A. Steiner, and V. M. Ingram, Tadpole antibodies against frog hemoglobin and their effect on development, Science 165, 67–69 (1969).CrossRefPubMedGoogle Scholar
  52. 52.
    A. J. Robinson, A. D. Hyatt, J. Pallister, N. H. R. Hamilton, and D. C. T. Halliday. Biocontrol approaches to canetoad control, Proceedings of Cane Toad control workshop, Kununurra (in Press, 2006).Google Scholar
  53. 53.
    R. Thresher and N. Bax. The science of producing daughterless technology; possibilities for using daughterless technology; maximizing the impact of carp control in: Proceedings of the National Carp Control Workshop, Edited by K. L. Lapidge (Cooperative Research Centre for Pest Animal Control, Canberra, Australia, 2003).Google Scholar
  54. 54.
    B. Coman, Environmental impact associated with the proposed use of Rabbit Calicivirus Disease for integrated rabbit control in Australia. Prepared for the Australian and New Zealand Rabbit Calicivirus Program, (1996).Google Scholar
  55. 55.
    C. K. Williams, Development and use of virus-vectored immunocontraception, Reprod. Fertil. Dev. 9, 169–178 (1997).PubMedCrossRefGoogle Scholar
  56. 56.
    P. Kerr, B. van Leeuwen, H. Perkins, M. Holland, W. Gu, R. Jackson, C. Williams, and A. Robinson, Development of fertility control for wild rabbits in Australia using a virally-vectored immunocontraceptive, in Enhancing Biocontrol Agents and Handling Risks, edited by M. Vurro and J. Gressel (IOS Press, Amsterdam, 2001), pp. 14–27.Google Scholar
  57. 57.
    E. Angulo and B. Cooke, First synthesize new viruses then regulate their release? The case of the wild rabbit, Mol. Ecol. 11, 2703–2709 (2002).PubMedCrossRefGoogle Scholar
  58. 58.
    D. C. Regnery, The epidemic potential of Brazilian myxoma virus (Lausanne strain) for three species of North American cottontails, Am. J. Epidemiol. 94, 514–519 (1971).PubMedGoogle Scholar
  59. 59.
    F. Fenner, Biological control as exemplified by smallpox eradication and myxomatosis, Proc. R. Soc. (Lond.) B 218, 259–285 (1983).CrossRefGoogle Scholar

Copyright information

© Springer 2007

Authors and Affiliations

  • Peter Kerr
    • 1
  1. 1.CSIRO EntomologyCanberraAustralia

Personalised recommendations