Wildlife Research Wildlife Research Society
Ecology, management and conservation in natural and modified habitats
REVIEW (Open Access)

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

Robert P. Henzell A B D , Brian D. Cooke B C and Gregory J. Mutze A B

A Department of Water, Land and Biodiversity Conservation, GPO Box 2834, Adelaide, SA 5001, Australia.

B Invasive Animals Cooperative Research Centre, University of Canberra, Bruce, ACT 2601, Australia.

C University of Canberra, Bruce, ACT 2601, Australia.

D Corresponding author. Email: henzell.bob@saugov.sa.gov.au

Wildlife Research 35(7) 633-650 http://dx.doi.org/10.1071/WR06164
Submitted: 1 December 2006  Accepted: 10 June 2008   Published: 17 November 2008

Abstract

European rabbits are exotic pests in Australia, New Zealand, parts of South America and Europe, and on many islands. Their abundance, and the damage they cause, might be reduced by the release of naturally occurring or genetically modified organisms (GMOs) that act as biological control agents (BCAs). Some promising pathogens and parasites of European rabbits and other lagomorphs are discussed, with special reference to those absent from Australia as an example of the range of necessary considerations in any given case. The possibility of introducing these already-known BCAs into areas where rabbits are pests warrants further investigation. The most cost-effective method for finding potentially useful but as-yet undiscovered BCAs would be to maintain a global watch on new diseases and pathologies in domestic rabbits. The absence of wild European rabbits from climatically suitable parts of North and South America and southern Africa may indicate the presence there of useful BCAs, although other explanations for their absence are possible. Until the non-target risks of deploying disseminating GMOs to control rabbits have been satisfactorily minimised, efforts to introduce BCAs into exotic rabbit populations should focus on naturally occurring organisms. The development of safe disseminating GMOs remains an important long-term goal, with the possible use of homing endonuclease genes warranting further investigation.


References

Abbott I. 2008 Historical perspectives of the ecology of some conspicuous vertebrate species in south-west Western Australia. Conservation Science Western Australia 6 1 214

Anderson R. C. (2000). ‘Nematode Parasites of Vertebrates: Their Development and Transmission.’ 2nd edn. (CABI Publishing: Wallingford, UK.)

Angulo E. Bárcena J. 2007 Towards a unique and transmissible vaccine against myxomatosis and rabbit hemorrhagic disease for rabbit populations. Wildlife Research 34 567 577
doi:10.1071/WR06160

Angulo E. Cooke B. 2002 First synthesize new viruses then regulate their release? The case of the wild rabbit. Molecular Ecology 11 2703 2709 doi:10.1046/j.1365-294X.2002.01635.x Pubmed Abstract

Angulo E. Gilna B. 2008 When biotech crosses borders. Nature Biotechnology 26 277 282 doi:10.1038/nbt0308-277 Pubmed Abstract

Anon. 1955 Myxomatosis in hares. The Veterinary Record 67 455

Baker D. G. 1998 Natural pathogens of laboratory mice, rats, and rabbits and their effects on research. Clinical Microbiology Reviews 11 231 266
Pubmed Abstract

Barlow N. D. 2000 The ecological challenge of immunocontraception: editor’s introduction. Journal of Applied Ecology 37 897 902 doi:10.1046/j.1365-2664.2000.00591.x

Baron J. (2006). ‘Against Bioethics.’ (MIT Press: Cambridge, MA.)

Beagley C. T. Okada N. A. Wolstenholme D. R. 1996 Two mitochondrial group I introns in a metazoan, the sea anemone Metridium senile: one intron contains genes for subunits 1 and 3 of NADH dehydrogenase. Proceedings of the National Academy of Sciences of the United States of America 93 5619 5623 doi:10.1073/pnas.93.11.5619 Pubmed Abstract

Beirne B. P. 1963 The meaning and definition of ‘biological control’. Entomophaga 8 237 243 doi:10.1007/BF02377529

Bigalke R. C. , and Pepler D. (1991). Mammals introduced to the mediterranean region of South Africa. In ‘Biogeography of Mediterranean Invasions’. (Eds R. H. Groves and F. di Castri.) pp. 285–292. (Cambridge University Press: Cambridge.)

Block W. Upton C. Mcfadden G. 1985 Tumorigenic poxviruses: genomic organization of malignant rabbit virus, a recombinant between Shope fibroma virus and myxoma virus. Virology 140 113 124 doi:10.1016/0042-6822(85)90450-7 Pubmed Abstract

Bonino N. Soriguer R. C. 2004 Distribución actual y dispersión del conejo europeo (Oryctolagus cuniculus) en Mendoza (Argentina). Mastozoología Neotropical 11 237 241

Boucher S. Gracia E. Villa A. Fernandez A. Nouaille L. Briffaud M. A. Albizu I. Baselga R. 2001 Pathogens in the reproductive tract of farm rabbits. The Veterinary Record 149 677 678
Pubmed Abstract

Brooke R. K. , Lloyd P. H. , and de Villiers A. L. (1986). Alien and translocated terrestrial vertebrates in South Africa. In ‘The Ecology and Management of Biological Invasions in Southern Africa’. (Eds I. A. W. Macdonald, F. J. Kruger and A. A. Ferrar.) pp. 63–74. (Oxford University Press: Cape Town.)

Burt A. 2003 Site-specific selfish genes as tools for the control and genetic engineering of natural populations. Proceedings of the Royal Society of London. Series B. Biological Sciences 270 921 928 doi:10.1098/rspb.2002.2319 Pubmed Abstract

Burt A. , and Trivers R. (2006). ‘Genes in Conflict: the Biology of Selfish Genetic Elements.’ (Harvard University Press: Cambridge.)

Calvete C. Angulo E. Estrada R. Moreno S. Villafuerte R. 2005 Quarantine length and survival of translocated European wild rabbits. Journal of Wildlife Management 69 1063 1072 doi:10.2193/0022-541X(2005)069[1063:QLASOT]2.0.CO;2

Capucci L. Fallacara F. Grazioli S. Lavazza A. Pacciarini M. L. Brocchi E. 1998 A further step in the evolution of rabbit haemorrhagic disease virus: the appearance of the first consistent antigenic variant. Virus Research 58 115 126 doi:10.1016/S0168-1702(98)00106-3 Pubmed Abstract

Catchpole J. Norton C. C. 1979 The species of Eimeria in rabbits for meat production in Britain. Parasitology 79 249 257 Pubmed Abstract

Cavagnaro J. B. 1988 Distribution of C3 and C4 grasses at different altitudes in a temperate arid region of Argentina. Oecologia 76 273 277 doi:10.1007/BF00379962

Cerling T. E. Wang Y. Quade J. 1993 Expansion of C4 ecosystems as an indicator of global ecological change in the late Miocene. Nature 361 344 345 doi:10.1038/361344a0

Chapman J. A. , and Ceballos G. (1990). The cottontails. In ‘Rabbits, Hares and Pikas: Status Survey and Conservation Action Plan’. (Eds J. A. Chapman and J. E. C. Flux.) pp. 95–110. (IUCN: Gland, Switzerland.)

Charrel R. N. Attoui H. Butenko A. M. Clegg J. C. Deubel V. et al 2004 Tick-borne virus diseases of human interest in Europe. Clinical Microbiology and Infection 10 1040 1055 doi:10.1111/j.1469-0691.2004.01022.x Pubmed Abstract

Chastel C. 1998 Erve and Eyach: two viruses isolated in France, neuropathogenic for man and widely distributed in Western Europe. Bulletin de L’Académie Nationale de Médecine 182 801 810 Pubmed Abstract

Coman B. (1999). ‘Tooth & Nail: the Story of the Rabbit in Australia.’ (Text Publishing: Melbourne.)

Cooke B. D. 1983 Changes in the age-structure and size of populations of wild rabbits in South Australia, following the introduction of European rabbit fleas, Spilopsyllus cuniculi (Dale), as vectors of myxomatosis. Australian Wildlife Research 10 105 120 doi:10.1071/WR9830105

Cooke B. D. (1999 a). Rabbit Calicivirus Disease Program Report 2: epidemiology, spread and release in wild rabbit populations in Australia. A report of research conducted by participants in 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. 1999 b Notes on the life-history of the rabbit flea Caenopsylla laptevi ibera Beaucournu & Marquez, 1987 (Siphonaptera: Ceratophyllidae) in eastern Spain. Parasite (Paris, France) 6 347 354 Pubmed Abstract

Cooke B. D. 2002 Rabbit haemorrhagic disease: field epidemiology and the management of wild rabbit populations. Review scientifique et technique de l’Office international des Epizooties 21 347 358

Cooke B. D. Fenner F. 2002 Rabbit haemorrhagic disease and the biological control of wild rabbits, Oryctolagus cuniculus, in Australia and New Zealand. Wildlife Research 29 689 706 doi:10.1071/WR02010

Cooke B. D. McPhee S. Robinson A. J. 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 doi:10.1071/WR00092

Corbet G. B. (1994). Taxonomy and origins. In ‘The European Rabbit: the History and Biology of a Successful Colonizer’. (Eds H. V. Thompson and C. M. King.) pp. 1–7. (Oxford University Press: Oxford.)

Couch L. K. 1929 Introduced European rabbits in the San Juan Islands, Washington. Journal of Mammalogy 10 334 336 doi:10.2307/1374122

Cox J. C. Pye D. Edmonds J. W. Shepherd R. 1980 An investigation of Encephalitozoon cuniculi in the wild rabbit Oryctolagus cuniculus in Victoria, Australia. Journal of Hygiene 84 295 300 Pubmed Abstract

Cunningham A. A. 1996 Disease risks of wildlife translocations. Conservation Biology 10 349 353 doi:10.1046/j.1523-1739.1996.10020349.x

Daszak P. Cunningham A. A. Hyatt A. D. 2001 Anthropogenic environmental change and the emergence of infectious diseases in wildlife. Acta Tropica 78 103 116 doi:10.1016/S0001-706X(00)00179-0 Pubmed Abstract

de Almeida A. J. Mayen F. L. de Oliveira F. C. R. 2006 Espécies do gênero Eimeria observadas em fezes de coelhos domésticos (Oryctolagus cuniculus) criados no município de Campos dos Goytacazes, estado do Rio de Janeiro, Brasil. Revista Brasileira de Parasitologia Veterinaria = Brazilian Journal of Veterinary Parasitology; Orgao Oficial Do Colegio Brasileiro de Parasitologia Veterinaria 15 163 166 Pubmed Abstract

De Leener K. Rahman M. Matthijnssens J. Van Hoovels L. Goegebuer T. van der Donck I. Van Ranst M. 2004 Human infection with a P[14], G3 lapine rotavirus. Virology 325 11 17 doi:10.1016/j.virol.2004.04.020 Pubmed Abstract

Dubey J. P. Sreekumar C. Lindsay D. S. Hill D. Rosenthal B. M. Venturini L. Venturini M. C. Greiner E. C. 2003 Besnoitia oryctofelisi n. sp. (Protozoa: Apicomplexa) from domestic rabbits. Parasitology 126 521 539 Pubmed Abstract

Dunlap T. R. 1997 Remaking the land: the acclimatization movement and Anglo ideas of nature. Journal of World History 8 303 319 doi:10.1353/jwh.2005.0062

Dunsmore J. D. 1966 a Nematode parasites of free-living rabbits, Oryctolagus cuniculus (L.), in eastern Australia. I. Variations in the number of Trichostrongylus retortaeformis (Zeder). Australian Journal of Zoology 14 185 199 doi:10.1071/ZO9660185

Dunsmore J. D. 1966 b Nematode parasites of free-living rabbits, Oryctolagus cuniculus (L.), in eastern Australia. II. Variations in the numbers of Graphidium strigosum (Dujardin) Railliet and Henry. Australian Journal of Zoology 14 625 634 doi:10.1071/ZO9660625

Dunsmore J. D. 1966 c Nematode parasites of free-living rabbits, Oryctolagus cuniculus (L.), in eastern Australia. III. Variations in the numbers of Passalurus ambiguus (Rudolphi). Australian Journal of Zoology 14 635 645 doi:10.1071/ZO9660635

Dunsmore J. D. (1981). The role of parasites in population regulation of the European rabbit (Oryctolagus cuniculus) in Australia. In ‘Worldwide Furbearer Conference Proceedings’. (Eds J. A. Chapman and D. Pursley.) pp. 654–669. (University of Maryland: Frostburg, MD.)

Durant P. , and Guevara M. A. (2001). A new rabbit species (sylvilagus, Mammalia: Leporidae) from the lowlands of Venezuela. Revista de Biología Tropical [online] 49, 369–381. [sighted 18 December 2007] Available from World Wide Web: <http://www.scielo.sa.cr/scielo.php?script=sci_arttext&pid=S0034-77442001000100036&lng=en&nrm=iso>

Duszynski D. W. Marquardt W. C. 1969 Eimeria (Protozoa: Eimeriidae) of the cottontail rabbit Sylvilagus audubonii in northeastern Colorado, with descriptions of three new species. Journal of Protozoology 16 128 137 Pubmed Abstract

Duszynski D. W. , and Upton S. J. (2001). Cyclospora, Eimeria, Isospora and Cryptosporidium spp. In ‘Parasitic Diseases of Wild Mammals’. (Eds W. M. Samuel, M. J. Pybus and A. A. Kocan.) pp. 416–459. (Iowa State University Press: Ames, IA.)

Edwards G. P. Dobbie W. Berman McK, D. 2002 Population trends in European rabbits and other wildlife of central Australia in the wake of rabbit haemorrhagic disease. Wildlife Research 29 557 565 doi:10.1071/WR00097

Epstein H. E. Gill R. A. Paruelo J. M. Lauenroth W. K. Jia G. J. Burke I. C. 2002 The relative abundance of three plant functional types in temperate grasslands and shrublands of North and South America: effects of projected climate change. Journal of Biogeography 29 875 888 doi:10.1046/j.1365-2699.2002.00701.x

Everett K. D. E. Bush R. M. Andersen A. A. 1999 Emended description of the order Chlamydiales, proposal of Parachlamydiaceae fam. nov. and Simkaniaceae fam. nov., each containing one monotypic genus, revised taxonomy of the family Chlamydiaceae, including a new genus and five new species, and standards for the identification of organisms. International Journal of Systematic Bacteriology 49 415 440 Pubmed Abstract

Fenner F. (1994). Rabbitpox virus. In ‘Virus Infections of Rodents and Lagomorphs’. (Ed. A. D. M. E. Osterhaus.) pp. 51–57. (Elsevier: Amsterdam.)

Fenner F. , and Fantini B. (1999). ‘Biological Control of Vertebrate Pests: The History of Myxomatosis – an Experiment in Evolution.’ (CABI Publishing: Wallingford, UK.)

Fenner F. , and Ratcliffe F. N. (1965). ‘Myxomatosis.’ (Cambridge University Press: Cambridge.)

Ferrand N. , and Branco M. (2007). The evolutionary history of the European rabbit (Oryctolagus cuniculus): major patterns of population differentiation and geographic expansion inferred from protein polymorphism. In ‘Phylogeography of Southern European Refugia’. (Eds S. Weiss and N. Ferrand.) pp. 207–235. (Springer: Berlin/Heidelberg/New York.)

FitzSimons F. W. 1906 The wild animals of South Africa. Natal Agricultural Journal 9 142 153

Flux J. E. C. 1993 Relative effect of cats, myxomatosis, traditional control, or competitors in removing rabbits from islands. New Zealand Journal of Zoology 20 13 18


Flux J. E. C. (1994). World distribution. In ‘The European Rabbit: the History and Biology of a Successful Colonizer’. (Eds H. V. Thompson and C. M. King.) pp. 8–21. (Oxford University Press: Oxford.)

Flux J. E. C. (2008). A review of competition between rabbits (Oryctolagus cuniculus) and hares (Lepus europaeus). In ‘Lagomorph Biology: Evolution, Ecology and Conservation’. (Eds P. C. Alves, N. Ferrand and K. Hackländer.) pp. 241–249. (Springer: Berlin/Heidelberg.)

Flux J. E. C. , and Angermann R. (1990). The hares and jackrabbits. In ‘Rabbits, Hares and Pikas: Status Survey and Conservation Action Plan’. (Eds J. A. Chapman and J. E. C. Flux.) pp. 61–94. (IUCN: Gland, Switzerland.)

Flux J. E. C. , Duthie A. G. , Robinson T. J. , and Chapman J. A. (1990). Exotic populations. In ‘Rabbits, Hares and Pikas: Status Survey and Conservation Action Plan’. (Eds J. A. Chapman and J. E. C. Flux.) pp. 147–153. (IUCN: Gland, Switzerland.)

Forrester N. L. Trout R. C. Turner S. L. Kelly D. Boag B. Moss S. Gould E. A. 2006 Unravelling the paradox of rabbit haemorrhagic disease virus emergence, using phylogenetic analysis; possible implications for rabbit conservation strategies. Biological Conservation 131 296 306
doi:10.1016/j.biocon.2006.05.005

Froggatt W. W. 1906 Rabbits and ants. Agricultural Gazette of New South Wales 17 1113 1119

Fu A. Q. 1984 The coccidian species of rabbit and their distribution in China. Chinese Journal of Rabbit Farming 1 34 37


Gibb J. A. (1990). The European rabbit Oryctolagus cuniculus. In ‘Rabbits, Hares and Pikas: Status Survey and Conservation Action Plan’. (Eds J. A. Chapman and J. E. C. Flux.) pp. 116–120. (IUCN: Gland, Switzerland.)

Gibb J. A. , and Williams J. M. (1994). The rabbit in New Zealand. In ‘The European Rabbit: the History and Biology of a Successful Colonizer’. (Eds H. V. Thompson and C. M. King.) pp. 158–204. (Oxford University Press: Oxford.)

Goddard M. R. Leigh J. Roger A. J. Pemberton A. J. 2006 Invasion and persistence of a selfish gene in the Cnidaria. PLoS ONE 1 1 e3
doi:10.1371/journal.pone.0000003 Pubmed Abstract

Gould F. Magori K. Huang Y. 2006 Genetic strategies for controlling mosquito-borne diseases. American Scientist 94 238 246

Grès V. Marchandeau S. Landau I. 2002 Description d’une nouvelle espèce d’Eimeria (Coccidia, Eimeridea) chez le lapin de garenne Oryctolagus cuniculus en France. Zoosystema 24 203 207


Griffith B. Scott J. M. Carpenter J. W. Reed C. 1993 Animal translocations and potential disease transmission. Journal of Zoo and Wildlife Medicine 24 231 236


Grigliatti T. A. , Meister G. , and Pfeifer T. A. (2007). TAC–TICS: Transposon-based biological pest management systems. In ‘Novel Biotechnologies for Biocontrol Agent Enhancement and Management’. (Eds M. Vurro and J. Gressel.) pp. 327–351. (Springer: Dordrecht.)

Hamilton P. B. Stevens J. R. Holz P. Boag B. Cooke B. Gibson W. C. 2005 The inadvertent introduction into Australia of Trypanosoma nabiasi, the trypanosome of the European rabbit (Oryctolagus cuniculus), and its potential for biocontrol. Molecular Ecology 14 3167 3175
doi:10.1111/j.1365-294X.2005.02602.x Pubmed Abstract

Hardy C. M. Hinds L. A. Kerr P. J. Lloyd M. L. Redwood A. J. Shellam G. R. Strive T. 2006 Biological control of vertebrate pests using virally vectored immunocontraception. Journal of Reproductive Immunology 71 102 111 doi:10.1016/j.jri.2006.04.006 Pubmed Abstract

Heckathorn S. A. , McNaughton S. J. , and Coleman J. S. (1999). C4 plants and herbivory. In ‘C4 Plant Biology’. (Eds R. F. Sage and R. K. Monson.) pp. 285–312. (Academic Press: San Diego.)

Henzell R. 2007 Genomic age series. Part 5: Prospects for managing vertebrate pests in Australia with GMO technologies. Agricultural Science 20 41 45

Henzell R. P. Cunningham R. B. Neave H. M. 2002 Factors affecting the survival of Australian wild rabbits exposed to rabbit haemorrhagic disease. Wildlife Research 29 523 542
doi:10.1071/WR00083

Hershkovitz P. (1972). The recent mammals of the Neotropical region: a zoogeographic and ecological review. In ‘Evolution, Mammals and Southern Continents’. (Eds A. Keast, F. C. Erk and B. Glass.) pp. 311–431. (State University of New York: Albany, NY.)

Hobbs R. P. Twigg L. E. 1998 Coccidia (Eimeria spp.) of wild rabbits in southwestern Australia. Australian Veterinary Journal 76 209 210 doi:10.1111/j.1751-0813.1998.tb10131.x Pubmed Abstract

Hobbs R. P. Twigg L. E. Elliot A. D. Wheeler A. G. 1999 Evaluation of the association of parasitism with mortality of wild European rabbits Oryctolagus cuniculus (L.) in southwestern Australia. Journal of Parasitology 85 803 808 doi:10.2307/3285814 Pubmed Abstract

Hoddle M. S. (1999). Biological control of vertebrate pests. In ‘Handbook of Biological Control’. (Eds T. S. Bellows and T. W. Fisher.) pp. 955–974. (Academic Press: San Diego, CA.)

Holt R. D. , Hochberg M. E. , and Barfield M. (1999). Population dynamics and the evolutionary stability of biological control. In ‘Theoretical Approaches to Biological Control’. (Eds B. A. Hawkins and H. V. Cornell.) pp. 219–230. (Cambridge University Press: Cambridge.)

Hornick R. 2001 Tularemia revisited. The New England Journal of Medicine 345 1637 1639 doi:10.1056/NEJM200111293452211 Pubmed Abstract

Hudson J. B. (1994). Herpesviridae. In ‘Virus Infections of Rodents and Lagomorphs’. (Ed. A. D. M. E. Osterhaus.) pp. 81–84. (Elsevier: Amsterdam.)

HVPCWG (Humane Vertebrate Pest Control Working Group) (2004). A national approach towards humane vertebrate pest control. Discussion paper arising from the proceedings of an RSPCA Australia/AWC/VPC joint workshop, August 4–5, Melbourne. RSPCA Australia, Canberra.

Jaksic F. M. 1998 Vertebrate invaders and their ecological impacts in Chile. Biodiversity and Conservation 7 1427 1445 doi:10.1023/A:1008825802448

Jaksic F. M. , and Fuentes E. R. (1991). Ecology of a successful invader: the European rabbit in central Chile. In ‘Biogeography of Mediterranean Invasions’. (Eds R. H. Groves and F. di Castri.) pp. 273–283. (Cambridge University Press: Cambridge.)

Jaksic F. M. Soriguer R. C. 1981 Predation upon the European rabbit (Oryctolagus cuniculus) in Mediterranean habitats of Chile and Spain: a comparative analysis. Journal of Animal Ecology 50 269 281 doi:10.2307/4044

Jin L. Valentine B. A. Baker R. J. Löhr C. V. Gerlach R. F. Bildfell R. J. Moerdyk-Schauwecker M. 2008 An outbreak of fatal herpesvirus infection in domestic rabbits in Alaska. Veterinary Pathology 45 369 374 doi:10.1354/vp.45-3-369 Pubmed Abstract

Johnson R. C. 1977 The spirochetes. Annual Review of Microbiology 31 89 106 doi:10.1146/annurev.mi.31.100177.000513 Pubmed Abstract

Katona K. Bíró Z. Hahn I. Kertész M. Altbäcker V. 2004 Competition between European hare and European rabbit in a lowland area, Hungary: a long-term ecological study in the period of rabbit extinction. Folia Zoologica 53 255 268

Kirkpatrick R. D. 1959 a San Juan rabbit in Indiana. Outdoor Indiana 3 1 2


Kirkpatrick R. D. (1959 b). San Juan rabbit investigation. Final Report. Indiana Department of Conservation, Indianapolis.

Kirkpatrick R. D. 1960 The introduction of the San Juan rabbit (Oryctolagus cuniculus) in Indiana. Proceedings of the Indiana Academy of Sciences 69 320 324


Kovaliski J. 1998 Monitoring the spread of rabbit hemorrhagic disease virus as a new biological agent for control of wild European rabbits in Australia. Journal of Wildlife Diseases 34 421 428
Pubmed Abstract

Kuijper D. P. J. van Wieren S. E. Bakker J. P. 2004 Digestive strategies in two sympatrically occurring lagomorphs. Journal of Zoology 264 171 178 doi:10.1017/S0952836904005722

Labudovic A. Perkins H. van Leeuwen B. Kerr P. 2004 Sequence mapping of the Californian MSW strain of Myxoma virus. Archives of Virology 149 553 570 doi:10.1007/s00705-003-0222-6 Pubmed Abstract

Lavazza A. , and Capucci L. (2008). How many caliciviruses are there in rabbits? A review on RHDV and correlated viruses. In ‘Lagomorph Biology: Evolution, Ecology and Conservation’. (Eds P. C. Alves, N. Ferrand and K. Hackländer.) pp. 263–278. (Springer: Berlin/Heidelberg.)

Lever C. (1985). ‘Naturalized Mammals of the World.’ (Longman: Harlow.)

Levine N. D. Ivens V. 1972 Coccidia of the Leporidae. Journal of Eukaryotic Microbiology 19 572 581 doi:10.1111/j.1550-7408.1972.tb03531.x

Licois D. Wyers M. Coudert P. 2005 Epizootic rabbit enteropathy: experimental transmission and clinical characterization. Veterinary Research 36 601 613 doi:10.1051/vetres:2005021 Pubmed Abstract

Licon Luna R. M. 2000 First report of myxomatosis in Mexico. Journal of Wildlife Diseases 36 580 583 Pubmed Abstract

Lidicker W. Z. (1991). Introduced mammals in California. In ‘Biogeography of Mediterranean Invasions’. (Eds R. H. Groves and F. di Castri.) pp. 263–271. (Cambridge University Press: Cambridge.)

Long J. L. (2003). ‘Introduced Mammals of the World: their History, Distribution and Influence.’ (CSIRO Publishing/CABI: Melbourne.)

Marchandeau S. Bertagnoli S. Peralta B. Boucraut-Baralon C. Letty J. Reitz F. 2004 Possible interaction between myxomatosis and calicivirosis related to rabbit haemorrhagic disease affecting the European rabbit. The Veterinary Record 155 589 592 Pubmed Abstract

Marlier D. Dewrée R. Delleur V. Licois D. Lassence C. Poulipoulis A. Vindevogel H. 2003 Description des principales étiologies des maladies digestives chez le lapin européen (Oryctolagus cuniculus). Annales de Médecine Vétérinaire 147 385 392

Martín-Alonso J. M. Skilling D. E. González-Molleda L. del Barrio G. Machín Á. Keefer N. K. Matson D. O. Iversen P. L. Smith A. W. Parra F. 2005 Isolation and characterization of a new Vesivirus from rabbits. Virology 337 373 383
doi:10.1016/j.virol.2005.04.018 Pubmed Abstract

Matthee C. A. van Vuuren B. J. Bell D. Robinson T. J. 2004 A molecular supermatrix of the rabbits and hares (Leporidae) allows for the identification of five intercontinental exchanges during the Miocene. Systematic Biology 53 433 447 doi:10.1080/10635150490445715 Pubmed Abstract

Matthijnssens J. Rahman M. Martella V. Xuelei Y. De Vos S. De Leener K. Ciarlet M. Buonavoglia C. Van Ranst M. 2006 Full genomic analysis of human rotavirus strain B4106 and lapine rotavirus strain 30/96 provides evidence for interspecies transmission. Journal of Virology 80 3801 3810 doi:10.1128/JVI.80.8.3801-3810.2006 Pubmed Abstract

Mbuthia P. G. Gathumbi P. K. Bwangamoi O. Wasike P. N. 1993 Natural besnoitiosis in a rabbit. Veterinary Parasitology 45 191 198 doi:10.1016/0304-4017(93)90074-W Pubmed Abstract

McCauley L. M. E. Lancaster M. J. Young P. Butler K. L. Ainsworth C. G. V. 2007 Comparison of ELISA and CFT assays for Chlamydophila abortus antibodies in ovine sera. Australian Veterinary Journal 85 325 328 doi:10.1111/j.1751-0813.2007.00189.x Pubmed Abstract

McIntosh M. T. Behan S. C. Mohammed F. M. Lu Z. Moran K. E. et al 2007 A pandemic strain of calicivirus threatens rabbit industries in the Americas. Virology Journal 4 96 doi:10.1186/1743-422X-4-96 Pubmed Abstract

McLeod R. (2004). ‘Counting the Cost: Impact of Invasive Animals in Australia, 2004.’ (Cooperative Research Centre for Pest Animal Control: Canberra.)

McLeod S. R. Twigg L. E. 2006 Predicting the efficacy of virally-vectored immunocontraception for managing rabbits. New Zealand Journal of Ecology 30 103 120

Measures L. N. Anderson R. C. 1983 Development of the stomach worm Obeliscoides cuniculi (Graybill) in lagomorphs, woodchucks and small rodents. Journal of Wildlife Diseases 19 225 233
Pubmed Abstract

Mutze G. Bird P. Kovaliski J. Peacock D. Jennings S. 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 doi:10.1071/WR00100

Mutze G. , Bird P. , Cooke B. , and Henzell R. (2008). Geographic and seasonal variation in the impact of rabbit haemorrhagic disease on wild rabbits, Oryctolagus cuniculus, 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: Berlin/Heidelberg.)

Myers K. , Parer I. , Wood D. , and Cooke B. D. (1994). The rabbit in Australia. In ‘The European Rabbit: the History and Biology of a Successful Colonizer’. (Eds H. V. Thompson and C. M. King.) pp. 108–157. (Oxford University Press: Oxford.)

Mykytowycz R. 1957 Ectoparasites of the wild rabbit, Oryctolagus cuniculus (L.), in Australia. CSIRO Wildlife Research 2 63 65

Mykytowycz R. 1958 Contact transmission of infectious myxomatosis of the rabbit, Oryctolagus cuniculus (L.). CSIRO Wildlife Research 3 1 6


Norbury G. 2001 Advances in New Zealand mammalogy, 1990–2000: lagomorphs. Journal of the Royal Society of New Zealand 31 83 97


Norbury G. , and Reddiex B. (2005). European rabbit. In ‘The Handbook of New Zealand Mammals’. (Ed. C. M. King.) pp. 131–150. (Oxford University Press: Melbourne.)

Ojeda R. A. Campos C. M. Gonnet J. M. Borghi C. E. Roig V. G. 1998 The MaB Reserve of Ñacuñán, Argentina: its role in understanding the Monte Desert biome. Journal of Arid Environments 39 299 313
doi:10.1006/jare.1998.0398

Olsen P. (1998). ‘Australia’s Pest Animals: New Solutions to Old Problems.’ (Bureau of Rural Sciences: Canberra, & Kangaroo Press: Sydney.)

Onderka D. K. Papp-Vid G. Perry A. W. 1992 Fatal herpesvirus infection in commercial rabbits. The Canadian Veterinary Journal. La Revue Veterinaire Canadienne 33 539 543 Pubmed Abstract

Pakandl M. 1988 Description of Eimeria vejdovskyi sp.n. and redescription of Eimeria media Kessel, 1929 from the rabbit. Folia Parasitologica 35 1 9 Pubmed Abstract

PCE (Parliamentary Commissioner for the Environment) (1998). ‘The Rabbit Calicivirus Disease Saga: a Biosecurity/Biocontrol Fiasco.’ (PCE: Wellington.)

Pech R. P. Hood G. M. 1998 Foxes, rabbits, alternative prey and rabbit calicivirus disease: consequences of a new biological control agent for an outbreaking species in Australia. Journal of Applied Ecology 35 434 453 doi:10.1046/j.1365-2664.1998.00318.x

Percy D. H. , and Barthold S. W. (2007). ‘Pathology of Laboratory Rodents and Rabbits.’ 3rd edn. (Blackwell: Ames, IA.)

Petersen J. M. Schriefer M. E. 2005 Tularemia: emergence/re-emergence. Veterinary Research 36 455 467 doi:10.1051/vetres:2005006 Pubmed Abstract

Phillips S. Zenger K. R. Richardson B. J. 2002 Are Sydney rabbits different? Australian Zoologist 32 49 55

Pinto R. M. Gomes D. C. Menezes R. C. Gomes C. T. Noronha D. 2004 Helminths of rabbits (Lagomorpha, Leporidae) deposited in the helminthological collection of the Oswaldo Cruz Institute. Revista Brasileira de Zoologia 21 599 604


Reddiex B. Hickling G. J. Norbury G. L. 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
doi:10.1071/WR00088

Reglero M. Vicente J. Rouco C. Villafuerte R. Gortazar C. 2007 Trypanosoma spp. infection in wild rabbits (Oryctolagus cuniculus) during a restocking program in southern Spain. Veterinary Parasitology 149 178 184 doi:10.1016/j.vetpar.2007.08.001 Pubmed Abstract

Regnery D. C. 1971 The epidemic potential of Brazilian myxoma virus (Lausanne strain) for three species of North American cottontails. American Journal of Epidemiology 94 514 519 Pubmed Abstract

Robinson A. J. Kirkland P. D. Forrester R. I. Capucci L. Cooke B. D. Philbey A. W. 2002 Serological evidence for the presence of a calicivirus in Australian wild rabbits, Oryctolagus cuniculus, before the introduction of rabbit haemorrhagic disease (RHDV): its potential influence on the specificity of a competitive ELISA for RHDV. Wildlife Research 29 655 662 doi:10.1071/WR00096

Rogers P. M. , Arthur C. P. , and Soriguer R. C. (1994). The rabbit in continental Europe. In ‘The European Rabbit: the History and Biology of a Successful Colonizer’. (Eds H. V. Thompson and C. M. King.) pp. 22–63. (Oxford University Press: Oxford.)

Rolls E. (1969). ‘They All Ran Wild: the Story of Pests on the Land in Australia.’ (Angus and Robertson: Sydney.)

Sage R. F. , Wedlin D. A. , and Li M. (1999). The biogeography of C4 photosynthesis: patterns and controlling factors. In ‘C4 Plant Biology’. (Eds R. F. Sage and R. K. Monson.) pp. 313–373. (Academic Press: San Diego.)

Silvers L. Inglis B. Labudovic A. Janssens P. A. van Leeuwen B. H. Kerr P. J. 2006 Virulence and pathogenesis of the MSW and MSD strains of Californian myxoma virus in European rabbits with genetic resistance to myxomatosis compared to rabbits with no genetic resistance. Virology 348 72 83 doi:10.1016/j.virol.2005.12.007 Pubmed Abstract

Simpson G. G. (1980). ‘Splendid Isolation: the Curious History of South American Mammals.’ (Yale University Press: New Haven, CT.)

Smith A. T. , Formozov N. A. , Hoffmann R. S. , Changlin Z. , and Erbajeva M. A. (1990). The pikas. In ‘Rabbits, Hares and Pikas: Status Survey and Conservation Action Plan’. (Eds J. A. Chapman and J. E. C. Flux.) pp. 14–60. (IUCN: Gland, Switzerland.)

Sorvillo F. Ash L. R. Berlin O. G. W. Yatabe J. Degiorgio C. Morse S. A. 2002 Baylisascaris procyonis: an emerging helminthic zoonosis. Emerging Infectious Diseases 8 355 359 Pubmed Abstract

Stodart E. 1968 Coccidiosis in wild rabbits, Oryctolagus cuniculus (L.), at four sites in different climatic regions in eastern Australia. II. The relationship of oocyst output to climate and to some aspects of the rabbit’s physiology. Australian Journal of Zoology 16 619 628 doi:10.1071/ZO9680619

Stodart E. , and Parer I. (1988). Colonisation of Australia by the rabbit, Oryctolagus cuniculus (L.). CSIRO Division of Wildlife and Ecology Project Report No. 6. CSIRO, Australia.

Strayer D. S. Cabirac G. Sell S. Leibowitz J. L. 1983 Malignant rabbit fibroma virus: observations on the culture and histopathologic characteristics of a new virus-induced rabbit tumor. Journal of the National Cancer Institute 71 91 104 Pubmed Abstract

Strong K. L. Halliday R. B. 1992 Biology and host specificity of the genus Psoroptes Gervais (Acarina: Psoroptidae), with reference to its occurrence in Australia. Experimental & Applied Acarology 15 153 169 doi:10.1007/BF01195788

Suckow M. A. , Brammer D. W. , Rush H. G. , and Crisp C. E. (2002). Biology and diseases of rabbits. In ‘Laboratory Animal Medicine’. (Eds J. G. Fox, L. C. Anderson, F. M. Loew and F. W. Quimby.) pp. 329–364. (Academic Press: London.)

Swan C. Perry A. Papp-Vid G. 1991 Herpesvirus-like viral infection in a rabbit. The Canadian Veterinary Journal 32 627 628 Pubmed Abstract

Thomas C. Finn M. Twigg L. Deplazes P. Thompson R. C. A. 1997 Microsporidia (Encephalitozoon cuniculi) in wild rabbits in Australia. Australian Veterinary Journal 75 808 810 doi:10.1111/j.1751-0813.1997.tb15658.x Pubmed Abstract

Thompson H. V. (1994). The rabbit in Britain. In ‘The European Rabbit: the History and Biology of a Successful Colonizer’. (Eds H. V. Thompson and C. M. King.) pp. 64–107. (Oxford University Press: Oxford.)

Tizzani P. , Lavazza A. , Capucci L. , and Meneguz P. G. (2002). Presence of infectious agents and parasites in wild population of cottontail (Sylvilagus floridanus) and consideration on its role in the diffusion of pathogens infecting hares. European Association of Zoo- and Wildlife Veterinarians (EAZWV) 4th scientific meeting, joint with the annual meeting of the European Wildlife Disease Association (EWDA) May 8–12, 2002, Heidelberg, Germany.

Torres J. M. Sanchez C. Ramirez M. A. Morales M. Bárcena J. Ferrer J. Espuna E. Pages-Mante A. Sanchez-Vizcaino J. M. 2001 First field trial of a transmissible recombinant vaccine against myxomatosis and rabbit hemorrhagic disease. Vaccine 19 4536 4543 doi:10.1016/S0264-410X(01)00184-0 Pubmed Abstract

Trout R. C. Tittensor A. M. 1989 Can predators regulate wild rabbit Oryctolagus cuniculus population density in England and Wales? Mammal Review 19 153 173 doi:10.1111/j.1365-2907.1989.tb00409.x

Twigg L. E. Lowe T. J. Martin G. R. Wheeler A. G. Gray G. S. Griffin S. L. O’Reilly C. M. Robinson D. J. Hubach P. H. 2000 Effects of surgically imposed sterility on free-ranging rabbit populations. Journal of Applied Ecology 37 16 39 doi:10.1046/j.1365-2664.2000.00471.x

Tyndale-Biscoe C. H. 1994 Virus-vectored immunocontraception of feral mammals. Reproduction, Fertility and Development 6 281 287 doi:10.1071/RD9940281

van Leeuwen B. H. Kerr P. J. 2007 Prospects for fertility control in the European rabbit (Oryctolagus cuniculus) using myxoma virus-vectored immunocontraception. Wildlife Research 34 511 522 doi:10.1071/WR06167

Venturini L. Petrucelli M. Piscopo M. Ungaza J. M. Venturini M. C. Bacigalupe D. Basso W. Dubey J. P. 2002 Natural Besnoitia sp. infection in rabbits from Argentina. Veterinary Parasitology 107 273 278 doi:10.1016/S0304-4017(02)00156-5 Pubmed Abstract

Viggers K. L. Lindenmayer D. B. Spratt D. M. 1993 The importance of disease in reintroduction programmes. Wildlife Research 20 687 698 doi:10.1071/WR9930687

Webb S. D. , and Marshall L. G. (1982). Historical biogeography of recent South American land mammals. In ‘Mammalian Biology in South America’. (Eds M. A. Mares and H. H. Genoways.) pp. 39–52. (University of Pittsburgh: Linesville, PA.)

Weisbroth S. H. , Flatt R. E. , and Kraus A. L. (Eds) (1974). ‘The Biology of the Laboratory Rabbit.’ (Academic Press: New York.)

Weiss R. A. 2002 Virulence and pathogenesis. Trends in Microbiology 10 314 317 doi:10.1016/S0966-842X(02)02391-0 Pubmed Abstract

Whipp M. J. Davis J. M. Lum G. de Boer J. Zhou Y. Bearden S. W. Petersen J. M. Chu M. C. Hogg G. G. 2003 Characterisation of a novicida-like subspecies of Francisella tularensis isolated in Australia. Journal of Medical Microbiology 52 839 842 doi:10.1099/jmm.0.05245-0 Pubmed Abstract

White P. C. L. , and Newton-Cross G. (2000). An introduced disease in an invasive host: the ecology and economics of rabbit calicivirus disease (RCD) in rabbits in Australia. In ‘The Economics of Biological Invasions’. (Eds C. Perrings, M. Williamson and S. Dalmazzone.) pp. 117–137. (Edward Elgar: Cheltenham, UK.)

Wilber J. L. (1999). ‘Pathology of the Rabbit.’ Available at: http://morfz.com/patho_rabbit.pdf [Accessed 8 November 2007.]

Williams C. K. , Parer I. , Coman B. J. , Burley J. , and Braysher M. L. (1995). ‘Managing Vertebrate Pests: Rabbits.’ Bureau of Resource Sciences/CSIRO Division of Wildlife and Ecology. (Australian Government Publishing Service: Canberra.)

Williams R. T. 1972 The distribution and abundance of the ectoparasites of the wild rabbit, Oryctolagus cuniculus (L.), in New South Wales, Australia. Parasitology 64 321 330 Pubmed Abstract

Wilson J. C. Fuller S. J. Mather P. B. 2002 Formation and maintenance of discrete wild rabbit (Oryctolagus cuniculus) population systems in arid Australia: habitat heterogeneity and management implications. Austral Ecology 27 183 191 doi:10.1046/j.1442-9993.2002.01169.x

Wilson J. R. Hattersley P. W. 1989 Anatomical characters and digestibility of leaves of Panicum and other grass genera with C3 and different types of C4 photosynthetic pathway. Australian Journal of Agricultural Research 40 125 136 doi:10.1071/AR9890125

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 doi:10.2307/4277

Zenger K. R. Richardson B. J. Vachot-Griffin A.-M. 2003 A rapid population expansion retains genetic diversity within European rabbits in Australia. Molecular Ecology 12 789 794 doi:10.1046/j.1365-294X.2003.01759.x Pubmed Abstract

Zumpt I. F. 1976 Some diseases of domestic rabbits encountered in the western Cape. Journal of the South African Veterinary Association 47 117 122 Pubmed Abstract


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