The future biological control of pest populations of European rabbits, Oryctolagus cuniculus

We are grateful to the many people on the IUCN’s Aliens list and elsewhere who provided information on rabbits in South Africa and North America. Four anonymous referees made helpful and constructive comments on an earlier version of the manuscript.

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The Californian strain of MV (natural host: Sylvilagus bachmani), like the Brazilian strain, is highly pathogenic to European rabbits (Fenner and Fantini 1999; Silvers et al. 2006). It causes high mortality in captive wild European rabbits held in quarantine in Australia, despite the host–pathogen coevolution that has already occurred with the Brazilian strain of MV (Silvers et al. 2006). It is not known whether it would interact adversely with the Brazilian strain of MV, or with RHDV, in the field, or how it would coevolve with wild European rabbits in the presence of RHDV and the Brazilian strain of MV. It is likely that genetic recombination could occur between the two strains of MV: Californian MV is related more closely to Brazilian MV than to another leporipoxvirus, Shopes fibroma virus (SFV), and it is known that recombination can occur between MV (strain unknown) and SFV (Block et al. 1985; Labudovic et al. 2004). The competitive ability and pathogenicity of such a recombinant are impossible to predict. However, even if it was likely to prove a useful BCA in Australia, importation of Californian MV might be refused on animal welfare grounds.

This virus is common in Sylvilagus of the mid-western and western United States but uncommon in laboratory Oryctolagus (Weisbroth et al. 1974; Baker 1998). It is transmitted by arthropod vectors, and transmission to domestic rabbits probably occurs exclusively from wild Sylvilagus because the virus is rarely observed in lesions of Oryctolagus. In laboratory rabbits the virus frequently produces squamous cell carcinomas that commonly metastasise to regional lymph nodes and lungs. It is unclear how useful it might be as a BCA in wild rabbits. While the lack of virus in lesions of laboratory Oryctolagus might be expected to reduce transmissibility, it is possible that greater quantities of virus would be produced in wild Oryctolagus in Australia. In any event, it might be possible to artificially select for viral genotypes that produced sufficient virus in lesions of laboratory Oryctolagus for a weakly self-transmitting strain to be developed. Once such a strain existed, natural selection – either in the laboratory or in the wild in Australia – might be expected to increase transmissibility (cf. stabilising selection for virulence in MV: Fenner and Fantini 1999).

The highly lethal and extremely contagious rabbitpox virus causes rare disease outbreaks in laboratory rabbits in the United States and the Netherlands (Fenner 1994). It appears to be an artefact as it is known only from laboratory rabbits. Spread appears to be by aerosol but since insects are usually well controlled in laboratory animal houses, this does not exclude the possibility that vectors could spread the virus. Both described strains have a wide host range and are highly pathogenic for mice as well as rabbits. Mice are also a pest in Australia, but the virus’s wide host range precludes its introduction into Australia.

Lapine rotaviruses can cause diarrhoea in rabbits, but recent evidence suggests that they may be able to infect humans and other animals (De Leener et al. 2004; Matthijnssens et al. 2006). Unless strains with a narrower host range can be found, they are unsuitable for use as BCAs.

EYAV is present in mainland Europe in European rabbits, which are thought to be the reservoir host (Chastel 1998; Charrel et al. 2004). Its pathogenicity in rabbits is unknown. However, EYAV causes disease in humans (Chastel 1998), and is therefore unsuitable for use as a BCA for rabbits.

The nematode Paraspidodera uncinata commonly infects guinea-pigs and octodontid rodents in Brazil, where it has also been recorded in European rabbits (Pinto et al. 2004). It is not known whether it causes disease in rabbits, or if it is present in guinea-pigs in Australia. If it is present in Australian guinea-pigs, its introduction into rabbits in Australia should be investigated. Its potential effects on Australian native rodents would also need to be investigated. The exotic lungworm Protostrongylus rufescens cuniculorum occurs in rabbits overseas, but experiments to assess its potential as a BCA were terminated when it was found that it could also develop in sheep (Williams et al. 1995). The zoonotic raccoon roundworm Baylisascaris procyonis causes fatal cerebrospinal disease in rabbits, but its capacity to infect humans (Sorvillo et al. 2002) precludes its use as a BCA.

Naturally occurring besnoitiosis, caused by protozoan parasites of the genus Besnoitia, occurs in domestic rabbits in Kenya and Argentina (Mbuthia et al. 1993; Venturini et al. 2002; Dubey et al. 2003), but not Australia. Little is known about the unnamed Kenyan species other than it was present in a rabbit submitted for necropsy after sudden death. The pathogenicity of the Argentinean Besnoitia oryctofelisi is unknown. B. oryctofelisi causes illness in its definitive host (domestic cats), mortality in at least one non-target species (gerbils, Meriones unguiculatus), and infection in laboratory mice, and is unlikely to be suitable for introduction into Australia.

Tularemia is a zoonosis caused by the bacterium Francisella tularensis (Petersen and Schriefer 2005). F. tularensis tularensis, the North American Type A subspecies, is the most pathogenic for European rabbits (Hornick 2001). However, tularemia’s pathogenicity for humans and lack of host specificity preclude the introduction of any exotic subspecies into Australia.

A novicida-like subspecies of F. tularensis was recently discovered in a human in northern Australia, in an area where wild rabbits do not occur (Whipp. et al. 2003; M. J. Whipp. pers. comm. Melbourne, 2006). Its host range, geographical distribution, and pathogenicity for rabbits are unknown. Tularemia is not known to occur in rabbits in Australia, but given the risk to humans its deliberate use for biocontrol purposes is most unlikely. It could only be contemplated if: (1) the causative organism was already widespread in areas where rabbits occur but had not spilled over into them; (2) it was shown to be pathogenic in rabbits and capable of persisting in them; (3) it was likely to significantly mitigate the damage caused by rabbits; and (4) its introduction into rabbits would not increase the risk to non-target organisms (particularly humans).

Enzootic abortion of ewes, caused by the bacterium Chlamydophila abortus, has not been reported from Australia or New Zealand (McCauley et al. 2007). C. abortus was formerly part of Chlamydia psittaci but is now regarded as a separate species (Everett et al. 1999). It is important in domestic rabbits under intensive conditions in the Western Cape of South Africa (Zumpt 1976). The bacterial strain involved in South Africa may be more pathogenic to rabbits than strains occurring elsewhere (e.g. in France: see Boucher et al. 2001), but it is unsuitable for use as a BCA because it is not host specific and has zoonotic potential (Everett et al. 1999).