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Survival of translocated wild rabbits: importance of habitat, physiological and immune condition

2011; Wiley; Volume: 14; Issue: 6 Linguagem: Inglês

10.1111/j.1469-1795.2011.00472.x

1469-1795

Sonia Cabezas, C. Calvete, S. Moreno,

Animal Ecology and Behavior Studies

Animal ConservationVolume 14, Issue 6 p. 665-675 ORIGINAL ARTICLE Survival of translocated wild rabbits: importance of habitat, physiological and immune condition S. Cabezas, S. Cabezas Doñana Biological Station (CSIC), Americo Vespucio Av., Seville, SpainSearch for more papers by this authorC. Calvete, C. Calvete Agroalimentary Technology Research Center of Aragon (CITA), Carretera de Montañana, Zaragoza, SpainSearch for more papers by this authorS. Moreno, S. Moreno Doñana Biological Station (CSIC), Americo Vespucio Av., Seville, SpainSearch for more papers by this author S. Cabezas, S. Cabezas Doñana Biological Station (CSIC), Americo Vespucio Av., Seville, SpainSearch for more papers by this authorC. Calvete, C. Calvete Agroalimentary Technology Research Center of Aragon (CITA), Carretera de Montañana, Zaragoza, SpainSearch for more papers by this authorS. Moreno, S. Moreno Doñana Biological Station (CSIC), Americo Vespucio Av., Seville, SpainSearch for more papers by this author First published: 07 July 2011 https://doi.org/10.1111/j.1469-1795.2011.00472.xCitations: 13 Sonia Cabezas, Department of Biology, University of Saskatchewan, Saskatoon, SK, Canada S7N 5E2. Email: [email protected] Editor: Steve Redpath Read the full textAboutPDF ToolsRequest permissionExport citationAdd to favoritesTrack citation ShareShare Give accessShare full text accessShare full-text accessPlease review our Terms and Conditions of Use and check box below to share full-text version of article.I have read and accept the Wiley Online Library Terms and Conditions of UseShareable LinkUse the link below to share a full-text version of this article with your friends and colleagues. Learn more.Copy URL Abstract European wild rabbit populations are declining in Mediterranean ecosystems, where the species is of special conservation interest, and translocations are one of the most-used tools to recover populations. We evaluated the effects of habitat and physiological and immune condition on the short- and long-term survival of translocated adult wild rabbits. Rabbits were released in four different habitat treatments frequently used in conservation programmes: additional shelter, additional food, additional shelter plus food, predator exclusion and control. Before releasing the rabbits, we determined their physiological condition from body-mass and serum levels of urea, creatinine and total protein, and their immune condition from the concentrations of antibodies against myxomatosis and rabbit haemorrhagic disease. The risk of dying during the first 18 days post-release was two times lower in the predator exclusion treatment than that in the additional shelter, food, shelter plus food treatments and control. Short-term survival was also negative and positively correlated with creatinine and protein levels, respectively. The risk of dying from 19 to 180 days post-release in the additional food treatment was 10 and nine times lower than in predator exclusion and control, respectively, and negatively correlated with the antibody concentration against myxomatosis. The results suggest that short-term survival was related to predation risk and physiological condition, and long-term survival was related to food availability and myxomatosis incidence. We recommend that translocation programmes should consider using soft-release methods to reduce the risk of predation and ensure that all individuals are released in the best possible physiological condition to increase their short-term survival. We also suggest that the habitat be managed to ensure that the environment provides the appropriate conditions (i.e. food and shelter) for individuals and population persistence. Immune condition should be taken into account and translocation programmes should consider the origin of donor populations to reduce the variability of pathogen and virus strains. References Amici, A., France, O., Mastrodiacono, P., Merendino, N., Nardini, M. & Tomáis, G. (2000). Short term acute heat stress in rabbits: functional, metabolic and immunological effects. World Rabbit Sci. 3, 11– 16. Angulo, E. (2003). Factores que afectan a la distribución y abundancia del conejo en Andalucía. PhD thesis, Madrid Complutense University, Madrid. Angulo, E. & Villafuerte, R. (2003). Modelling hunting strategies for the conservation of wild rabbit populations. Biol. Conserv. 115, 291– 301. Argüello, J.L. (1991). La enfermedad hemorrágica viral del conejo: vacunación y repuesta inmune. Rev. Sci. Tech. Office Int. Epizoot. 10, 459– 470. Branco, M. (1995). Contribuçao para o estudo da genética bioquímica e populacional do coelho, Oryctolagus cuniculus. PhD thesis, University of Porto, Porto. Cabezas, S., Calvete, C. & Moreno, S. (2006). Vaccination success and body condition in the European wild rabbit: applications for conservation strategies. J. Wildl. Mgmt. 70, 154– 160. Cabezas, S. & Moreno, S. (2007). An experimental study of translocation success and habitat improvement in wild rabbits. Anim. Conserv. 10, 340– 348. Calvete, C., Angulo, E. & Estrada, R. (2005). Conservation of European wild rabbit populations when hunting is age and sex selective. Biol. Conserv. 121, 623– 634. Calvete, C., Angulo, E., Estrada, R., Moreno, S. & Villafuerte, R. (2005). Quarantine length, blood biochemical parameters and survival of translocated European wild rabbits. J. Wildl. Mgmt. 69, 1063– 1072. Calvete, C. & Estrada, R. (2004). Short-term survival and dispersal of translocated European wild rabbit. Improving the release protocol. Biol. Conserv. 120, 507– 516. Calvete, C., Estrada, R., Lucientes, J., Osacar, J.J. & Villafuerte, R. (2004a). Effects of vaccination against viral haemorrhagic disease (VHD) and myxomatosis on long-term mortality rates of European wild rabbits. Vet. Rec. 155, 388– 392. Calvete, C., Estrada, R., Osacar, J.J., Lucientes, J. & Villafuerte, R. (2004b). Short-term negative effects of vaccination campaigns against myxomatosis and viral haemorrhagic disease (VHD) on the survival of European wild rabbits. J. Wildl. Mgmt. 68, 198– 205. Calvete, C., Estrada, R., Villafuerte, R., Osácar, J.J. & Lucientes, J. (2002). Epidemiology of viral haemorrhagic disease and myxomatosis in free-living population of wild rabbits. Vet. Rec. 150, 776– 782. Calvete, C., Pelayo, E. & Sampietro, J. (2006). Habitat factors related to wild rabbit population trends after the initial impact of rabbit haemorrhagic disease. Wildl. Res. 33, 467– 474. Calvete, C., Villafuerte, R., Lucientes, J. & Osacar, J.J. (1997). Effectiveness of traditional wild rabbit restocking in Spain. J. Zool. (Lond.) 241, 1– 7. Catalán, I., Rodríguez-Hidalgo, P. & Tortosa, F. (2008). Is habitat management an effective tool for wild rabbit (Oryctolagus cuniculus) population reinforcement?Eur. J. Wildl. Res. 54, 449– 453. Cooke, B.D. & Berman, D. (2000). Effect of inoculation route and ambient temperature on the survival time of rabbits, Oryctolagus cuniculus (L.), infected with rabbit haemorrhagic disease virus. Wildl. Res. 27, 137– 142. Cooke, B.D. & Fenner, F. (2002). Rabbit haemorrhagic disease and the biological control of wild rabbits, Oryctolagus cuniculus, in Australia and New Zealand. Wildl. Res. 29, 689– 706. DelGiudice, G.D., Mech, L.D. & Seal, U.S. (1990). Effects of winter undernutrition on body composition and physiological profiles of White-Tailed Deer. J. Wildl. Mgmt. 54, 539– 550. Delibes, M. & Hiraldo, F. (1981). The rabbit as prey in the Iberian Mediterranean ecosystems. In Proceedings of the World Lagomorph Conference: 614– 622. K. Myers & C.D. MacInnes (Eds) Ontario: University of Guelph and Wildlife Research, Ministry of Natural Resources. Delibes-Mateos, M., Ferreras, P. & Villafuerte, R. (2009). European rabbit population trends and associated factors: a review of the situation in the Iberian Peninsula. Mamm. Rev. 39, 124– 140. Fernández, N. (2005). Spatial patterns in European rabbit abundance after a population collapse. Landsc. Ecol. 20, 897– 910. Ferrer, M. & Negro, J.J. (2004). The near-extinction of two large European predators: the super-specialists pay a price. Conserv. Biol. 18, 344– 349. Fullagar, P.J. (1977). Observations on myxomatosis in a rabbit population with immune adults. Aust. Wildl. Res. 4, 263– 280. Griffith, B., Scott, M., Carpenter, J. & Reed, C. (1989). Translocation as a Species Conservation tool: Status and Strategy. Science 245, 477– 480. Griffith, B., Scout, M., Carpenter, J.W. & Reed, C. (1993). Animal translocations and potential disease transmission. J. Zoo. Wildl. Med. 24, 231– 236. Harder, D.J. & Kirkpatrick, L.R. (1994). Physiological methods in wildlife research. In Research and management techniques for wildlife and habitats: 275– 306. T.A. Bookhout, (Ed.) Bethesda: The Wildlife Society. Heisey, D.M. & Fuller, T.K. (1985). Evaluation of survival and cause-specific mortality rates using telemetry data. J. Wildl. Mgmt. 49, 668– 674. Jacobson, H.A., Kirkpatrick, R.L. & McGinnes, B.S. (1978). Disease and physiologic characteristics of two cottontail populations in Virginia. Wildl. Monogr. 60, 5– 53. Letty, J., Aubineau, J., Marchandeau, S. & Clobert, J. (2003). Effect of translocation on survival in wild rabbit (Oryctolagus cuniculus). Mamm. Biol. 68, 250– 255. Letty, J., Marchadeau, S., Reitz, F., Clobert, J. & Sarrazin, F. (2002). Survival and movements of translocated wild rabbits (Oryctolagus cuniculus). Game Wildl. Sci. 19, 1– 23. Letty, J., Marchandeau, S., Clobert, J. & Aubineau, J. (2000). Improving translocation success: an experimental study of anti-stress treatment and release method for wild rabbits. Anim. Conserv. 3, 211– 219. Lombardi, L., Fernández, N., Moreno, S. & Villafuerte, R. (2003). Habitat-related differences in rabbit (Oryctolagus cuniculus) abundance, distribution, and activity. J. Mamm. 84, 26– 36. Macdonald, D.W., Tattersall, F.H., Rushton, S., South, A.B., Rao, S., Maitland, P. & Strachan, R. (2000). Reintroducing the beaver (Castor fiber) to Scotland: a protocol for identifying and assessing suitable release sites. Anim. Conserv. 3, 125– 133. McKillop, I.G., Butt, P., Lill, J., Pepper, H.W. & Wilson, C.J. (1998). Long-term cost effectiveness of fences to manage European wild rabbits. Crop Prot. 17, 393– 400. McPhee, S.R., Berman, D., Gonzales, A., Butler, K.L., Humphrey, J., Muller, J., Waddington, J.N., Daniels, P., Koch, S. & Marks, C.A. (2002). Efficacy of a competitive enzyme-linked immunosorbent assay (ELISA) for estimating prevalence of immunity to rabbit haemorrhagic disease virus (RHDV) in populations of Australian wild rabbits (Oryctolagus cuniculus). Wildl. Res. 29, 635– 647. McPhee, S.R., Butler K, L., Kovaliski, J., Mutze, G., Capucci, L. & Cooke, B.D. (2009). Antibody status and survival of Australian wild rabbits challenged with rabbit haemorrhagic disease virus. Wildl. Res. 36, 447– 456. Moorhouse, T.P., Gelling, M. & Macdonald, D.W. (2009). Effects of habitat quality upon reintroduction success in water voles: Evidence from a replicated experiment. Biol. Conserv. 142, 53– 60. Moreno, S., Beltrán, J.F., Cotilla, I., Kuffner, B., Laffite, R., Jordán, G., Ayala, J., Quintero, C., Jiménez, A., Castro, F., Cabezas, S. & Villafuerte, R. (2007). Long-term decline of the European wild rabbit (Oryctolagus cuniculus) in south-western Spain. Wildl. Res. 34, 652– 658. Moreno, S., Villafuerte, R., Cabezas, S. & Lombardi, L. (2004). Wild rabbit restocking for predator conservation in Spain. Biol. Conserv. 118, 183– 193. Moreno, S., Villafuerte, R. & Delibes, M. (1996). Cover is safe during the day but dangerous at night: the use of vegetation by European wild rabbits. Can. J. Zool. 74, 1656– 1660. Muguruza, R., Simón, M.C., Girones, O., Muzquiz, J.L., Garcia, J., Ortega, C. & Alonso, J.L. (1993). Enfermedad vírica hemorrágica del conejo: determinación de la mínima dosis infectante en la reproducción experimental por las vías intramuscular y aerosol. Med. Vet. 10, 163– 168. Muñoz, G. (1960) Anverso y reverso de la mixomatosis. 1st edn. Madrid, Dirección General de Montes, Caza y Pesca Fluvial, . Madrid, Spain, 58–76. Pagés, A., Artigas, C. & Espuña, E. (1991). Serological profile (by ELISA) of the active and passive immunity on rearing does vaccinated with and oil inactivated vaccine against RHD. International Symposium on RHD, Beijing. Palomares, F. (2003). Warren building by Europen rabbits (Oryctolagus cuniculus) in relation to cover availability in a sandy area. J. Zool. (Lond.) 259, 63– 67. Ross, J., Tittensor, A.M., Fox, A.P. & Sanders, M.F. (1989). Myxomatosis in farmland rabbit populations in England and Wales. Epidemiol. Infect. 103, 333– 357. Seddon, P.J., Armstrong, D.P. & Maloney, R.F. (2007). Developing the science of reintroduction biology. Conserv. Biol. 12, 303– 312. Seddon, P.J. & Ismail, K. (2002). Influence of ambient temperature on diurnal activity of Arabian oryx: Implications for reintroduction site selection. Oryx 36, 50– 55. Short, J., Kinnear, J.E. & Robley, A. (2002). Surplus killing by introduced predators in Australia, evidence for ineffective anti-predator adaptations in native prey species?Biol. Conserv. 103, 283– 301. Simón, M.C., Girones, O., Alonso, J.L., Muzquiz, J.L., García, J., Ortega, C. & Muguruza, C. (1993). Enfermedad vírica hemorrágica en conejo industrial: eficacia de una vacuna inactivada en la protección frente a la inoculación experimental. Med. Vet. 10, 44– 48. Soriguer, R.C. (1988). Alimentación del conejo (O. cuniculus L, 1758) en Doñana. SO, Spain. Doñana Acta Vert. 15, 141– 150. Stirrat, S.C. (2003). Body condition and blood chemistry of agile wallabies (Macropus agilis) in the wet–dry tropics. Wildl. Res. 30, 59– 67. Temple, S.A. (1987). Do predators always capture substandard individuals disproportionately from prey populations?Ecology 68, 669– 674. Therneau, T.M. & Grambsch, P.M. (2001). Modeling survival data: extending the Cox Model. 2nd edn. New York: Springer-Verlag. Viggers, K.L., Lindenmayer, D.B. & Spratt, D.M. (1993). The importance of disease in reintroduction programmes. Wildl. Res. 20, 687– 698. Villafuerte, R. (1994). Riesgo de predación y estrategias defensivas del conejo, Oryctolagus cuniculus, en el Parque Nacional de Doñana. PhD thesis, University of Cordoba, Spain Villafuerte, R., Calvete, C., Blanco, J.C. & Lucientes, J. (1995). Incidence of viral hemorrhagic disease in wild rabbit populations in Spain. Mammalia 59, 651– 659. Villafuerte, R., Lazo, A. & Moreno, S. (1997). Influence of food abundance and quality on rabbit fluctuations: conservation and management implications in Doñana National Park (SW Spain). Rev. Ecol. (Terre Vie) 52, 345– 356. Villafuerte, R. & Moreno, S. (1997). Predation risk, cover type, and group size in European rabbits in Doñana (SW Spain). Acta Theriol. 42, 225– 230. Warren, R.J. & Kirkpatrick, R.L. (1978). Indices of nutritional status in cottontail rabbits fed controlled diets. J. Wildl. Mgmt. 42, 154– 158. Wolf, M.C., Griffith, B., Reed, C. & Temple, S.A. (1996). Avian and mammalian translocations: Update and reanalysis of 1987 survey data. Conserv. Biol. 10, 1142– 1154. Woodford, M.H. & Rossiter, D.P.B. (1993). Disease risks associated with wildlife translocation projects. Rev. Scient. Tech. Office Int. Epizoot. 12, 115– 135. Citing Literature Volume14, Issue6December 2011Pages 665-675 ReferencesRelatedInformation