Wildlife Research Wildlife Research Society
Ecology, management and conservation in natural and modified habitats

Antibody status and survival of Australian wild rabbits challenged with rabbit haemorrhagic disease virus

S. R. McPhee A B F , K. L. Butler A , J. Kovaliski C , G. Mutze C , L. Capucci D and B. D. Cooke E
+ Author Affiliations
- Author Affiliations

A Department of Primary Industries, 600 Sneydes Road, Werribee, Vic. 3030, Australia.

B Agricultural Technical Services Pty Ltd, 177 Ballan Road, Werribee, Vic. 3030, Australia.

C Department for Water, Land and Biodiversity Conservation, GPO Box 2834, Adelaide, SA 5001, Australia.

D Istituto Zooprofilattico Sperimentale della Lombardia e dell’Emillia, Via Bianchi 7, 25124 Brescia, Italy.

E Invasive Animals Co-operative Research Centre, Building 3, Level D, University of Canberra Campus, Canberra, ACT 2611, Australia.

F Corresponding author. Email: Steve.McPhee@dpi.vic.gov.au

Wildlife Research 36(5) 447-456 https://doi.org/10.1071/WR08137
Submitted: 25 September 2008  Accepted: 18 May 2009   Published: 21 July 2009


In Australia, the epidemiology of rabbit haemorrhagic disease virus (RHDV) is complicated by non-pathogenic forms of calicivirus (bCV) co-circulating with RHDV and providing variable protection from RHDV. Currently no bCV virus-specific antibody tests exist; however, a series of four ELISAs used to detect antibodies to RHDV provided an indirect means to detect antibodies to bCV, enabling antibody categories of seronegative, maternal RHDV, RHDV or bCV to be determined. Rabbits (188) from four locations were challenged with RHDV and logistic regression models determined that, for rabbits <15 months old, survival was dependent on antibody titres alone and the relationship did not vary with age, capture site, gender, liveweight or reproductive status. All rabbits survived challenge after reaching 15 months of age, irrespective of their antibody titres. Where bCV antibodies were prevalent in young rabbits, the bCV category did not adequately summarise all information about rabbit survival that can be obtained from antibody titres. Within antibody categories, 95% of rabbits with RHDV, 33% with bCV, 40% with maternal RHDV and 22% with seronegative antibodies survived. The high survival rate of adults implies that natural outbreaks or controlled releases of RHDV will have little impact on adult breeding rabbits. Therefore, where RHDV and bCV are endemic, conventional rabbit-control programs targeting the immune breeding populations should provide the most predictable outcome for long-term maintenance of low rabbit populations.


We gratefully acknowledge field and laboratory support provided by Pat Daniels, Sharon Koch, Kelly Backhouse, Gail Squires and Vicki Langdon. Norm Simms performed some of the ELISAs with reagents supplied by Dr Lorenzo Capucci’s assistant, Mrs Giuliana Botti from the Istituto Zooprofilattico Sperimentale della Lombardia e dell’Emillia, Italy. We thank the three anonymous referees for constructive critique of the manuscript. The Victorian Institute of Animal Science Animal Ethics Committee approved the protocol (98/99-1812). The study was supported by State and Federal funds administered through the Rabbit Calicivirus Management Group and by the Victorian Department of Sustainability and Environment and the Department of Primary Industries.


Bowen, Z. , and Read, J. (1998). Population and demographic patterns of rabbits (Oryctolagus cuniculus) at Roxby Downs in arid South Australia and the influence of rabbit haemorrhagic disease. Wildlife Research 25, 655–662.
CrossRef |

Bruce, J. S. , and Twigg, L. E. (2004). Rabbit haemorrhagic disease virus: serological evidence of a non-virulent RHDV-like virus in south-western Australia. Wildlife Research 31, 605–612.
CrossRef |

Bruce, J. S. , and Twigg, L. E. (2005). The reintroduction, and subsequent impact, of rabbit haemorrhagic disease virus in a population of wild rabbits in south-western Australia. Wildlife Research 32, 139–150.
CrossRef |

Capucci, L. , Scicluna, M. T. , and Lavazza, A. (1991). Diagnosis of viral haemorrhagic disease of rabbits and the European brown hare syndrome. Revue Scientifique et Technique de l’Office International des Epizooties 10, 347–370.

Capucci, L. , Fusi, P. , Lavazza, A. , Pacciarini, M. L. , and Rossi, C. (1996). Detection and preliminary characterisation of a new calicivirus related to rabbit haemorrhagic disease but non-pathogenic. Journal of Virology 70, 8614–8623.
CAS | PubMed |

Capucci, L. , Nardin, A. , and Lavazza, A. (1997). Sercoconversion in an industrial unit of rabbits infected with a non-pathogenic rabbit haemorrhagic disease-like virus. Veterinary Record 140, 647–650.
CAS | PubMed |

Collins, B. J. , White, J. R. , Lenghaus, C. , Morrissy, C. J. , and Westbury, H. A. (1996). Presence of rabbit haemorrhagic disease virus in rabbit tissues as revealed by monoclonal antibody dependent capture ELISA. Journal of Virological Methods 58, 145–154.
CrossRef | CAS | PubMed |

Cooke B. D. (1999). Rabbit Calicivirus Disease Program Report 2: epidemiology, spread and release in wild rabbit populations in Australia. A report of research conducted by participants of the Rabbit Calicivirus Disease Monitoring and Surveillance Program and Epidemiology Research Program. Prepared for the RCD Management Group, Bureau of Rural Sciences, Canberra.

Cooke, B. D. (2002). Rabbit haemorrhagic disease: field epidemiology and the management of wild rabbit populations. Revue Scientifique et Technique – Office International des Épizooties 21, 347–358.

Cooke, B. D. , Robinson, A. J. , Merchant, J. C. , Nardin, A. , and Capucci, L. (2000). Use of ELISAs in field studies of rabbit haemorrhagic disease (RHD) in Australia. Epidemiology and Infection 124, 563–576.
CrossRef | CAS | PubMed |

Cooke, B. D. , McPhee, S. , Robinson, A. J. , and Capucci, L. (2002). Rabbit haemorrhagic disease: does a pre-existing RHD-like virus reduce the effectiveness of RHD as a biological control in Australia. Wildlife Research 29, 673–682.
CrossRef |

Dudzinski, M. L. , and Mykytowycz, R. (1961). The eye lens as an indicator of age in the wild rabbit in Australia. CSIRO Wildlife Research 6, 156–159.

Guillon, P. , Ruvoën-Clouet, N. , Le Moullac-Vaidye, B. , Marchandeau, S. , and Le Pendu, J. (2008). Association between expression of the H histo-blood group antigen, α1,2fucosyltransferases polymorphism of wild rabbits, and sensitivity to rabbit haemorrhagic disease. Glycobiology 19, 21–28.
CrossRef | PubMed |

Henzell, R. P. , Cunningham, R. B. , and Neave, H. M. (2002). Factors affecting the survival of Australian wild rabbits exposed to rabbit haemorrhagic disease. Wildlife Research 29, 523–542.
CrossRef |

Kovaliski, J. (1998). Monitoring the spread of rabbit haemorrhagic disease virus as a new biological agent for the control of European rabbits in Australia. Journal of Wildlife Diseases 34, 421–428.
CAS | PubMed |

McCullagh P. , and Nelder J. A. (1983). ‘Generalised Linear Models.’ (Chapman and Hall Ltd: London.)

McPhee, S. R. , Berman, D. , Gonzales, A. , Butler, K. L. , Humphrey, J. , Muller, J. , Waddington, J. N. , Daniels, P. , Koch, S. , and Marks, C. A. (2002). Efficacy of a competitive enzyme linked immunosorbent assay (cELISA) for diagnosis of prevalence of immunity to rabbit haemorrhagic disease virus (RHDV) in populations of Australian wild rabbits Oryctolagus cuniculus. Wildlife Research 29, 635–647.
CrossRef |

Moss, S. R. , Turner, S. L. , Trout, R. C. , White, P. J. , Hudson, P. J. , Desai, A. , Armesto, M. , Forrester, N. L. , and Gould, E. A. (2002). Molecular epidemiology of rabbit haemorrhagic disease virus. Journal of General Virology 83, 2461–2467.
CAS | PubMed |

Mutze, G. , Cooke, B. , and Alexander, P. (1998). The initial impact of rabbit hemorrhagic disease on rabbit populations in South Australia. Journal of Wildlife Diseases 34, 221–227.
CAS | PubMed |

Mutze, G. , Bird, P. , Peacock, D. , Jennings, S. , and Cooke, B. D. (2002). Emerging epidemiological patterns in rabbit haemorrhagic disease and myxomatosis and their effects on rabbit populations in South Australia. Wildlife Research 29, 577–590.
CrossRef |

Mutze G. , Bird P. , Cooke B. , and Henzell R. (2008). Geographic and seasonal variation in the impact of rabbit haemorrhagic disease on rabbits and rabbit damage in Australia. In ‘Lagomorph Biology: Evolution, Ecology and Conservation’. (Eds P. C. Alves, N. Ferrand and K. Hackländer.) pp. 279–293. (Springer: Heidelberg, Germany.)

Nagesha, H. S. , McColl, K. A. , Collins, B. J. , Morrissy, C. J. , Wang, L. F. , and Westbury, H. A. (2000). The presence of cross-reactive antibodies to rabbit haemorrhagic disease virus in Australian wild rabbits prior to the escape of the virus from quarantine. Archives of Virology 145, 749–757.
CrossRef | CAS | PubMed |

Neave H. M. (1999). Rabbit Calicivirus Disease Program Report 1: overview of effects on Australian wild rabbits populations and implications for agriculture and biodiversity. A report of research conducted by participants of the Rabbit Calicivirus Disease Monitoring and Surveillance Program and Epidemiology Research Program. Prepared for the RCD Management Group, Bureau of Rural Sciences, Canberra.

O’Keefe, J. S. , Tempero, J. E. , Motha, M. X. J. , Hansen, M. F. , and Atkinsona, P. H. (1999). Serology of rabbit haemorrhagic disease virus in wild rabbits before and after the release of the virus in New Zealand. Veterinary Microbiology 66, 29–40.
CrossRef | CAS | PubMed |

Robinson, A. J. , So, P. T. M. , Muller, W. , Cooke, B. D. , and Capucci, L. (2002a). Statistical models for the effect of age and maternal antibodies on the development of rabbit haemorrhagic disease in Australian wild rabbits. Wildlife Research 29, 663–671.
CrossRef |

Robinson, A. J. , Kirkland, P. D. , Forrester, R. I. , Capucci, L. , Cooke, B. D. , and Philbey, A. W. (2002b). Serological evidence for the presence of a calicivirus in 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. Wildlife Research 29, 655–662.
CrossRef |

Rodak, L. , Smid, B. , Valicek, L. , Vesely, T. , Stepanek, J. , Hampl, J. , and Jurak, E. (1990). Enzyme-linked immunosorbent assay of antibodies to rabbit haemorrhagic disease virus and determination of its major structural proteins. The Journal of General Virology 71, 1075–1080.
CrossRef | CAS | PubMed |

Sahai H. , and Khurshid A. (1995). ‘Statistics in Epidemiology: Methods, Techniques and Applications.’ (CRC Press: Boca Raton, FL.)

Stern R. , Coe R. , Allan E. , and Dale I. Ed. (1994). ‘Good Statistical Practice for Natural Resources Research.’ (CABI Publishing: Wallingford, UK.)

Strive, T. , Wright, J.D. , and Robinson, A. J. (2009). Identification and partial characterisation of a new lagovirus in Australian wild rabbits. Virology 384, 97–105.
CrossRef | CAS | PubMed |

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