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

Temporal dynamics of rabbit haemorrhagic disease virus infection in a low-density population of wild rabbits (Oryctolagus cuniculus) in New Zealand

J. Henning A D , D. U. Pfeiffer B , P. R. Davies A , J. Meers C and R. S. Morris A
+ Author Affiliations
- Author Affiliations

A EpiCentre, Massey University, Palmerston North, PO Box 11-222, New Zealand.

B Royal Veterinary College, North Mymms, Hertfordshire AL9 7TA, UK.

C University of Queensland, St Lucia, Qld 4072, Australia.

D Corresponding author. Present address: School of Veterinary Science, University of Queensland, Brisbane, Qld 4072, Australia. Email: J.Henning@uq.edu.au

Wildlife Research 33(4) 293-303 https://doi.org/10.1071/WR03059
Submitted: 8 July 2003  Accepted: 20 April 2006   Published: 27 June 2006


A longitudinal capture–mark–recapture study was conducted to determine the temporal dynamics of rabbit haemorrhagic disease (RHD) in a European rabbit (Oryctolagus cuniculus) population of low to moderate density on sand-hill country in the lower North Island of New Zealand. A combination of sampling (trapping and radio-tracking) and diagnostic (cELISA, PCR and isotype ELISA) methods was employed to obtain data weekly from May 1998 until June 2001. Although rabbit haemorrhagic disease virus (RHDV) infection was detected in the study population in all 3 years, disease epidemics were evident only in the late summer or autumn months in 1999 and 2001. Overall, 20% of 385 samples obtained from adult animals older than 11 weeks were seropositive. An RHD outbreak in 1999 contributed to an estimated population decline of 26%. A second RHD epidemic in February 2001 was associated with a population decline of 52% over the subsequent month. Following the outbreaks, the seroprevalence in adult survivors was between 40% and 50%. During 2000, no deaths from RHDV were confirmed and mortalities were predominantly attributed to predation. Influx of seronegative immigrants was greatest in the 1999 and 2001 breeding seasons, and preceded the RHD epidemics in those years. Our data suggest that RHD epidemics require the population immunity level to fall below a threshold where propagation of infection can be maintained through the population.


We gratefully acknowledge Robin Chrystall and George Robinson, who allowed us to conduct this study on their property. We thank Rex Munn, George Robinson and Phillip Thompson from the Manawatu–Wanganui Regional Council (Horizons Manawatu–Wanganui) for their comprehensive help in relation to all rabbit issues, including night counts, rabbit shooting and building a rabbit fence. We are indebted to Dugald Hall, who conducted many of the PCRs. We are grateful to Solis Norton and Sonja Kay for their help with radio-tracking and Dr Cord Heuer’s help with the statistical analysis. This research was supported financially by the Foundation for Research, Science and Technology, NZ; the Institute of Veterinary, Animal and Biomedical Sciences, Massey University; and by the German Academic Exchange Service. All field work involving live animals was approved by the Massey University Animal Ethics Committee.


Begon M. (Ed.) (1979). ‘'Investigating Animal Abundance: Capture-Recapture for Biologists.’ (Edward Arnold Limited: London.)

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 rabbit calicivirus related to Rabbit haemorrhagic disease virus but nonpathogenic. Journal of Virology 70, 8614–8623.
PubMed |

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

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 | PubMed |

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

Courchamp, F. , Say, L. , and Pontier, D. (2000). Detection, identification, and correction of a bias in a epidemiological study. Journal of Wildlife Diseases 36, 71–78.
PubMed |

Cowan D. P. (1983). Aspects of the behavioural ecology of a free-living population of the European wild rabbit, Oryctolagus cuniculus L. in southern England. Ph.D. Thesis, University of London.

Daly, J. C. (1980). Age, sex and season: factors which determine the trap response of the European wild rabbit, Oryctolagus cuniculus. Australian Wildlife Research 7, 421–432.
CrossRef |

Dawson-Saunders B., and Trapp R. G. (Eds.) (1994). ‘Basic and Clinical Biostatistics.’ (Appleton and Lange: Norwalk, CT.)

Dunnet, G. M. (1957). A test of the recapture method of estimating the number of rabbits, Oryctolagus cuniculus (L.) in a warren. CSIRO Wildlife Research 2, 90–100.

Dunsmore, J. D. (1974). The rabbit in subalpine south-eastern Australia. I. Population structure and productivity. Australian Wildlife Research 1, 1–16.
CrossRef |

Fraser, K. W. (1988). Reproductive biology of rabbits, Oryctolagus cuniculus (L.), in Central Otago, New Zealand. New Zealand Journal of Ecology 11, 79–88.

Gibb, J. A. (1993). Sociality, time and space in a sparse population of rabbits (Oryctolagus cuniculus). Journal of Zoology 229, 581–607.

Gibb, J. A. , and Fitzgerald, B. M. (1998). Dynamics of sparse rabbits (Oryctolagus cuniculus), Orongorongo Valley, New Zealand. New Zealand Journal of Zoology 25, 231–243.

Gibb J. A., and Williams J. M. (1994). The rabbit in New Zealand. In ‘The European Rabbit: The History and Biology of a Successful Coloniser’. (Eds G. B. Corbet, J. E. C. Flux, P. M. Rogers, C. P. Arthur, R. C. Soriguer, K. Myers, I. Parer, D. Wood, B. D. Cooke, J. A. Gibb, J. M. Williams, F. Fenner, J. Ross, H. V. Thompson and C. M. King.) pp. 158–200. (Oxford University Press: Oxford, UK.)

Gibb, J. A. , Ward, G. D. , and Ward, C. P. (1969). An experiment in the control of a sparse population of wild rabbits (Oryctolagus cuniculus L.) in New Zealand. New Zealand Journal of Science 12, 509–534.

Gibb, J. A. , Ward, C. P. , and Ward, G. D. (1978). Natural control of a population of rabbits, Oryctolagus cuniculus (L.), for ten years in the Kourarau enclosure. New Zealand Department of Scientific and Industrial Research Bulletin 223, 1–89.

Gibb, J. A. , White, A. J. , and Ward, C. P. (1985). Population ecology of rabbits in the Wairarapa, New Zealand. New Zealand Journal of Ecology 8, 55–82.

Henderson, B. A. (1979). Regulation of the size of the breeding population of the European rabbit, Oryctolagus cuniculus, by social behaviour. Journal of Applied Ecology 16, 383–392.

Henning, J. , Heuer, C. , and Davies, P. R. (2005a). Attitudes of New Zealand farmers to methods used to control wild rabbits. Preventive Veterinary Medicine 67, 171–194.
CrossRef | PubMed |

Henning, J. , Schnitzler, F. R. , Pfeiffer, D. U. , and Davies, P. R. (2005b). Influence of weather conditions on fly abundance and its implications for transmission of rabbit haemorrhagic disease virus in the North Island of New Zealand. Medical and Veterinary Entomology 19, 251–262.
CrossRef | PubMed |

Henning, J. , Meers, J. , Davies, P. R. , and Morris, R. S. (2005c). Survival of Rabbit haemorrhagic disease virus (RHDV) in the environment. Epidemiology and Infection 133, 719–730.
CrossRef | PubMed |

Henning, J. , Davies, P. R. , and Meers, J. (2006). Seropositivity to rabbit haemorrhagic disease virus in non-target mammals during periods of viral activity in a population of wild rabbits in New Zealand. Wildlife Research 33, 305–311.

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 |

Marchandeau, S. , Chaval, Y. , and le Goff, E. (2000). Prolonged decline in the abundance of wild European rabbits (Oryctolagus cuniculus) and high immunity level over three years following the arrival of rabbit haemorrhagic disease. Wildlife Biology 6, 141–147.

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 estimating prevalence of immunity to Rabbit haemorrhagic disease virus (RHDV) in populations of Australian wild rabbits (Oryctolagus cuniculus). Wildlife Research 29, 635–647.
CrossRef |

Moriarty, A. , Saunders, G. , and Richardson, B. J. (2000). Mortality factors acting on adult rabbits in central-western New South Wales. Wildlife Research 27, 613–619.
CrossRef |

Morisse, J.-P. , le Gall, G. , and Boilletot, E. (1991). Hepatitis of viral origin in Leporidae: introduction and aetiological hypotheses. Revue scientifique et technique de l'Office International des Epizooties 10, 283–295.

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

Myers, K. (1958). Further observations on the use of field enclosures for the study of the wild rabbit, Oryctolagus cuniculus (L.). CSIRO Wildlife Research 3, 40–49.

Myers, K. , and Poole, W. E. (1959). A study of the biology of the wild rabbit, Oryctolagus cuniculus (L.), in confined populations. I. The effects of density on home range and the formation of breeding groups. CSIRO Wildlife Research 4, 14–27.

Myers, K. , and Poole, W. E. (1961). A study of the biology of the wild rabbit, Oryctolagus cuniculus (L.), in confined populations. II. The effects of season and population increase on behaviour. CSIRO Wildlife Research 6, 1–41.

Myers, K. , and Poole, W. E. (1962). A study of the biology of the wild rabbit, Oryctolagus cuniculus (L.), in confined populations. III. Reproduction. Australian Journal of Zoology 10, 225–267.
CrossRef |

Mykytowycz, R. (1958). Social behaviour of an experimental colony of wild rabbits, Oryctolagus cuniculus (L.). Establishment of the colony. CSIRO Wildlife Research 3, 7–25.

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 virus from quarantine. Archives of Virology 145, 749–757.
CrossRef | PubMed |

Nowotny, N. , Bascunana, C. R. , Ballagi-Pordany, A. , Gavier-Widen, D. , Uhlen, M. , and Belak, S. (1997). Phylogenetic analysis of rabbit haemorrhagic disease and European brown hare syndrome viruses by comparison of sequences from the capsid protein gene. Archives of Virology 142, 657–673.
CrossRef | PubMed |

O’Hara P. J. (1997). ‘Decision on the Application to Approve the Importation of Rabbit Calicivirus as a Biological Control Agent for Feral Rabbits. 2 July 1997.’ (Ministry of Agriculture: NZ.)

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

Parer, I. , and Fullager, P. J. (1986). Biology of rabbits, Oryctolagus cuniculus, in subtropical Queensland. Australian Wildlife Research 13, 545–557.
CrossRef |

Parkes, J. P. , Norbury, G. L. , Heyward, R. P. , and Sullivan, G. (2002). Epidemiology of rabbit haemorrhagic disease (RHD) in the South Island, New Zealand, 1997–2001. Wildlife Research 29, 543–555.
CrossRef |

Reddiex, B. , Hickling, G. J. , Norbury, G. L. , and Frampton, C. M. (2002). Effects of predation and rabbit haemorrhagic disease on population dynamics of rabbits (Oryctolagus cuniculus) in North Canterbury, New Zealand. Wildlife Research 29, 627–633.
CrossRef |

Richardson, B. J. , Hayes, R. A. , Wheeler, S. H. , and Yardin, M. R. (2002). Social structures, genetic structures and dispersal strategies in Australian rabbit (Oryctolagus cuniculus) populations. Behavioral Ecology and Sociobiology 51, 113–121.
CrossRef |

Robinson, A. J. , Kirkland, P. D. , Forrester, R. I. , Capucci, L. , Cooke, B. D. , and Philbey, A. W. (2002a). 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. Wildlife Research 29, 655–662.
CrossRef |

Robinson, A. J. , So, P. T. M. , Muller, W. J. , Cooke, B. D. , and Capucci, L. (2002b). 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 |

Saunders, G. , Choquenot, D. , McIlroy, J. , and Packwood, R. (1999). Initial effects of rabbit haemorrhagic disease on free-living rabbit (Oryctolagus cuniculus) populations in central-western New South Wales. Wildlife Research 26, 69–74.
CrossRef |

Shien, J. H. , Shieh, H. K. , and Lee, L. H. (2000). Experimental infections of rabbits with Rabbit haemorrhagic disease virus monitored by polymerase chain reaction. Research in Veterinary Science 68, 255–259.
CrossRef | PubMed |

Smid, B. , Valicek, L. , Rodak, L. , Stephanek, J. , and Jurak, E. (1991). Rabbit haemorrhagic disease: an investigation of some properties of the virus and evaluation of an inactivated vaccine. Veterinary Microbiology 26, 77–85.
CrossRef | PubMed |

Smith, G. C. , Pugh, B. , and Trout, R. C. (1995). Age and sex bias in samples of wild rabbits, Oryctolagus cuniculus, from wild populations in southern England. New Zealand Journal of Zoology 22, 115–121.

Thompson, J. , and Clark, G. (1997). Rabbit calicivirus now established in New Zealand. Surveillance 24, 5–6.

Thrusfield M. (Ed.) (1995). ‘Veterinary Epidemiology.’ (Blackwell Science: London.)

Watson, J. S. (1957). Reproduction of the wild rabbit, Oryctolagus cuniculus (L.) in Hawke's Bay, New Zealand. New Zealand Journal of Science and Technology B 38, 451–482.

Webb, N. J. (1993). Growth and mortality in juvenile European wild rabbits (Oryctolagus cuniculus). Journal of Zoology 230, 665–677.

Wilkinson R., and Fitzgerald G. (Eds.) (1998). ‘Public Attitudes to Rabbit Calicivirus Disease in New Zealand.’ (Manaaki Whenua Press: Lincoln, Canterbury.)

Wood, D. H. (1980). The demography of a rabbit population in an arid region of New South Wales, Australia. Journal of Animal Ecology 49, 55–79.

Zheng, T. , Napier, A. M. , Parkes, J. P. , O’Keefe, J. S. , and Atkinson, P. H. (2002). Detection of RNA of Rabbit haemorrhagic disease virus from New Zealand wild rabbits. Wildlife Research 29, 683–688.
CrossRef |

Rent Article (via Deepdyve) Export Citation Cited By (7)