Causes and predictors of nest mortality in a European rabbit population
Abstract
We conducted a study on nest mortality of an individually marked population of European rabbits (Oryctolagus cuniculus L., 1758) living in a field enclosure. Over 4 years, we determined maternities and quantified pup mortality during the nest period of 703 pups born in subterranean breeding burrows. Overall, pup mortality occurred in 42.7% of the litters, whereas 32.4% of all born pups were affected. Mortality was highest during the first few postnatal days. In about 50% of the cases, we managed to quantify different causes of mortality such as malnutrition, flooding, cooling of the pups, infanticide, or predation. The pups’ body mass on postnatal day 1, the thermal environment and the number of litter mates were the most important predictors of nest mortality. Litter mortality risk decreased with increasing soil temperature around the subterranean nests. A comparatively higher average pup body mass lowered the nest mortality risk of a litter, whereas this effect was more pronounced when soil temperatures were low. Furthermore, mortality was lowest in medium-sized litters, most probably due to the balance between the thermal benefits of huddling with litter siblings and the costs of having them due to the lower share of milk obtained by the individual pups in larger litters. In addition, nest mortality depended on characteristics of the mother; mortality was increased in litters of low-ranking females and of mothers with lower body mass. In conclusion, our study highlights multiple causes and the effects of different environmental and social factors on nest mortality of this small mammal.
Keywords
Oryctolagus cuniculus Litter size Maternal characteristics Siblings Thermal environmentPreview
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References
- Alberts, J.R., 1978. Huddling by rat pups: group behavioral mechanisms of temperature regulation and energy conservation. J. Comp. Physiol. Psychol. 92, 231–245.PubMedCrossRefGoogle Scholar
- Bates, D., 2005. Fitting linear mixed models in R. R News 5, 27–39.Google Scholar
- Bautista, A., Drummond, H., Martínez-Gómez, M., Hudson, R., 2003. Thermal benefit of sibling presence in the newborn rabbit. Develop. Psychobiol. 43, 208–215.CrossRefGoogle Scholar
- Brambell, F.W.R., 1944. The reproduction of the wild rabbit Oryctolagus cuniculus (L.). Proc. Zool. Soc. Lond. B 114, 1–45.Google Scholar
- Burnham, K.P., Anderson, D.R., 2002. Model Selection and Inference: A Practical Information-Theoretical Approach. Springer, Berlin, Germany.Google Scholar
- Caruso, S., Siracusa, A.M., 2001. Factors affecting the abundance of wild rabbits (Oryctolagus cuniculus) in agro-ecosystems of the Mount Etna park. Hystrix Ital. J. Mammal. 12, 45–49.Google Scholar
- Cole, L., 1954. The population consequences of life-history phenomena. Q. Rev. Biol. 29, 103–137.PubMedCrossRefGoogle Scholar
- Coureaud, G., Schaal, B., Coudert, P., Hudson, R., Rideaud, P., Orgeur, P., 2000a. Mimicking natural nursing conditions promotes early pup survival in domestic rabbits. Ethology 106, 207–225.CrossRefGoogle Scholar
- Coureaud, G., Schaal, B., Coudert, P., Rideaud, P., Fortun-Lamothe, L., Hudson, R., Orgeur, P., 2000b. Immediate postnatal suckling in the rabbit: its influence on pup survival and growth. Reprod. Nutr. Dev. 40, 19–32.PubMedCrossRefGoogle Scholar
- Cowan, D.P., 1987. Aspects of the social organization of the European rabbit (Oryctolagus cuniculus). Ethology 75, 197–210.CrossRefGoogle Scholar
- Denenberg, V.H., Huff, R.L., Ross, S., Sawin, P.B., Zarrow, M.X., 1963. Maternal behaviour in the rabbit: the quantification of nest building. Anim. Behav. 11, 494–499.CrossRefGoogle Scholar
- Deutsch, J.A., 1957. Nest building behaviour of domestic rabbits under semi-natural conditions. Br. J. Anim. Behav. 5, 53–54.CrossRefGoogle Scholar
- Drummond, H., Vázquez, E., Sánchez-Colón, S., Martínez-Gómez, M., Hudson, R., 2000. Competition for milk in the domestic rabbit: survivors benefit from littermate deaths. Ethology 106, 511–526.CrossRefGoogle Scholar
- Elwood, R.W., Ostermeyer, M.C., 1984. Infanticide by male and female Mongolian gerbils: ontogeny, causation and function. In: Hausfater, G., Hrdy, S. (Eds.), Infanticide. Comparative and Evolutionary Perspectives. Aladine Press, New York, USA, pp. 367–386.Google Scholar
- Gaines, M.S., Rose, R.K., 1976. Population dynamics of Microtus ochrogaster in eastern Kansas. Ecology 57, 1145–1161.CrossRefGoogle Scholar
- Getz, L.L., Solomo, N.G., Pizzuto, T.M., 1990. The effect of predation of snakes on social organization of the prairie vole, Microtus ochrogaster. Am. Midl. Nat. 123, 365–371.CrossRefGoogle Scholar
- Getz, L.L., Simms, L.E., McGuire, B., 2000. Nestling survival and population cycles in the prairie vole, Microtus ochrogaster. Can. J. Zool. 78, 1723–1731.CrossRefGoogle Scholar
- Gibb, J.A., 1993. Sociality, time and space in a sparce population of rabbits (Oryctolagus cuniculus). J. Zool. Lond. 229, 581–607.CrossRefGoogle Scholar
- Gilbert, C., Blanc, S., Giroud, S., Trabalon, M., Le Maho, Y., Perret, M., Ancel, A., 2007. Role of huddling on the energetic of growth in a newborn altricial mammal. Am. J. Physiol. Regul. Integr. Comp. Physiol. 293, R867–R876.PubMedCrossRefGoogle Scholar
- Götz, A.A., Wolf, M., Stefanski, V., 2008. Psychosocial maternal stress during pregnancy: effects on reproduction for F0 and F1 generation laboratory rats. Physiol. Behav. 93, 1055–1060.PubMedCrossRefGoogle Scholar
- Graham, I.M., Lambin, X., 2002. The impact of weasel predation on cyclic field-vole survival: the specialist predator hypothesis contradicted. J. Anim. Ecol. 71, 946–956.CrossRefGoogle Scholar
- Hastings, K.K., Testa, J.W., 1998. Maternal and birth colony effects on survival of Wedell seal offspring from McMurdo Sound, Antarctica. J. Anim. Ecol. 67, 722–740.CrossRefGoogle Scholar
- Heise, S., Lippke, J., 1997. Role of female aggression in prevention of infanticidal behaviour in male common voles, Microtus arvalis (Pallas, 1779). Aggress. Behav. 23, 293–298.CrossRefGoogle Scholar
- Heppell, S.S., Caswell, H., Crowder, L.B., 2000. Life histories and elasticity patterns: perturbation analysis for species with minimal demographic data. Ecology 81, 654–665.CrossRefGoogle Scholar
- Hoogland, J.L., 1985. Infanticide in prairie dogs. Lactating females kill offspring in close kin. Science 230, 1037–1040.PubMedCrossRefGoogle Scholar
- Hudson, R., Trillmich, F., 2008. Sibling competition and cooperation in mammals: challenges, developments and prospects. Behav. Ecol. Sociobiol. 62, 299–307.CrossRefGoogle Scholar
- Hudson, R., Bilkó, À., Altbäcker, V., 1996. Nursing, weaning and the development of independent feeding in the rabbit. Z. Säugetierkd. 61, 39–48.Google Scholar
- Hull, D., 1973. Thermoregulation in young mammals. In: Whittow, G.C. (Ed.), Comparative Physiology of Thermoregulation. vol. 3: special aspects of thermoregulation. Academic Press, New York, USA, pp. 167–200.CrossRefGoogle Scholar
- Kasparian, K., Millar, J.S., 2004. Effects of extra food on nestling growth and survival in red-backed voles (Clethryonomys gapperi). Can. J. Zool. 82, 1219–1244.CrossRefGoogle Scholar
- Künkele, J., 1992. Infanticide in wild rabbits (Oryctolagus cuniculus). J. Mammal. 73, 317–320.CrossRefGoogle Scholar
- Lau, C., Simpson, C., 2004. Animal models for the study of the effect of prolonged stress on lactation in rats. Physiol. Behav. 82, 193–197.PubMedCrossRefPubMedCentralGoogle Scholar
- Leon, M., 1986. Development of thermoregulation. In: Blass, E.M. (Ed.), Handbook of Behavioural Neurobiology. vol. 8: developmental psychobiology and developmental neurobiology. Plenum Press, New York, USA, pp. 297–322.CrossRefGoogle Scholar
- Lloyd, H.G., McCowan, D., 1968. Some observations on the breeding burrows of the wild rabbit Oryctolagus cuniculus on the island of Skokholm. J. Zool. Lond. 156, 540–549.CrossRefGoogle Scholar
- Mendl, M., 1988. The effects of litter size on variation in mother-offspring relationships and behavioural and physical development in several mammalian species (principally rodents). J. Zool. Lond. 215, 15–34.CrossRefGoogle Scholar
- Millar, J.S., 2007. Nest mortality in small mammals. Ecoscience 14, 286–291.CrossRefGoogle Scholar
- Millar, J.S., McAdam, A.G., 2001. Life on the edge: the demography of short-season populations of deer mice. Oikos 93, 69–76.CrossRefGoogle Scholar
- Millar, J.S., Havelka, M.A., Sharma, S., 2004. Nest mortality in a population of small mammals. Acta Theriol. 49, 269–273.CrossRefGoogle Scholar
- Moreno, S., Villafuerte, R., 1995. Traditional management of scrubland for the conservation of rabbits Oryctolagus cuniculus and their predators in Doñana National Park, Spain. Biol. Conserv. 73, 81–85.CrossRefGoogle Scholar
- Moreno, S., Beltran, J.F., Cotilla, I., Kuffer, B., Laffite, R., Jordan, G., Ayala, J., Quintero, C., Jimenez, A., Castro, F., Cabezas, S., Villafuerte, R., 2007. Long-term decline of the European wild rabbit (Oryctolagus cuniculus) in southwestern Spain. Wildl. Res. 24, 652–658.CrossRefGoogle Scholar
- Mulder, J.L., Wallage-Drees, J.M., 1979. Red fox predation on young rabbits in breeding burrows. Netherland J. Zool. 29, 144–149.CrossRefGoogle Scholar
- Myers, K., 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 Wildl. Res. 6, 1–41.CrossRefGoogle Scholar
- Nagelkerke, N.J.D., 1991. A note on a general definition of the coefficient of determination. Biometrika 78, 691–692.CrossRefGoogle Scholar
- Oli, M.K., Dobson, F.S., 2003. The relative importance of life-history variables to population growth rate in mammals: Cole’s prediction revisited. Am. Nat. 161, 422–440.PubMedCrossRefGoogle Scholar
- Palomares, F., 2001. Comparison of three methods to estimate rabbit abundance in a Mediterranean environment. Wildl. Soc. Bull. 29, 578–585.Google Scholar
- Palomares, F., 2003. The negative impact of heavy rains on the abundance of a Mediterranean population of European rabbits. Mamm. Biol. 68, 224–234.CrossRefGoogle Scholar
- Poigner, J., Szendrõ, Z., Lévai, A., Radnai, I., Biró-Németh, E., 2000. Effects of birth weight and litter size on growth and mortality in rabbits. World Rabbit Sci. 8, 17–22.Google Scholar
- R Development Core Team, 2007. R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing. ISBN:3-900051-07-0 <https://doi.org/wwwR-projectorg>.
- Rashwan, A.A., Marai, I.F.M., 2000. Mortality in young rabbits: a review. World Rabbit Sci. 8, 111–124.Google Scholar
- Reid, D.G., Krebs, C.J., Kenney, A., 1995. Limitation of collared lemming population growth at low densities by predation mortality. Oikos 73, 387–389.CrossRefGoogle Scholar
- Riedman, M.L., Estes, J.A., Staedler, M.M., Giles, A.A., Carlson, D.R., 1994. Breeding patterns and reproductive success of California sea otters. J. Wildl. Manage. 58, 391–399.CrossRefGoogle Scholar
- Rödel, H.G., Bora, A., Kaiser, J., Kaetzke, P., Khaschei, M., von Holst, D., 2004. Density-dependent reproduction in the European rabbit: a consequence of individual response and age-dependent reproductive performance. Oikos 104, 529–539.CrossRefGoogle Scholar
- Rödel, H.G., Bora, A., Kaetzke, P., Khaschei, M., Hutzelmeyer, H., Zapka, M., von Holst, D., 2005. Timing of breeding and reproductive performance of female European rabbits in response to winter temperature and body mass. Can. J. Zool. 83, 935–942.CrossRefGoogle Scholar
- Rödel, H.G., Wibbelt, G., Starkloff, A., von Holst, D., 2007. Post-natal remains of the foetal membranes affect growth and survival of wild European rabbits pups. Mamm. Biol. 72, 313–319.CrossRefGoogle Scholar
- Rödel, H.G., Starkloff, A., Bautista, A., Friedrich, A.C., von Holst, D., 2008a. Infanticide and maternal offspring defence in European rabbits under natural breeding conditions. Ethology 114, 22–31.CrossRefGoogle Scholar
- Rödel, H.G., Prager, G., Stefanski, V., von Holst, D., Hudson, R., 2008b. Separating maternal and litter size effects on early postnatal growth in two species of altricial mammals. Physiol. Behav. 93, 826–834.PubMedCrossRefGoogle Scholar
- Rödel, H.G., Hudson, R., von Holst, D., 2008c. Optimal litter size for individual growth of European rabbit pups depends on their thermal environment. Oecologia 155, 677–685.PubMedCrossRefGoogle Scholar
- Sokoloff, G., Blumberg, M.S., 2001. Competition and cooperation among huddling infant rats. Develop. Psychobiol. 39, 65–75.CrossRefGoogle Scholar
- Thompson, H.V., King, C.M., 1994. The European Rabbit. History and Biology of a Successful Colonizer. Oxford University Press, Oxford, UK.Google Scholar
- Thompson, H.V., Worden, A.N., 1956. The Rabbit. Collins New Naturalist, London, UK.Google Scholar
- von Holst, D., 1998. The concept of stress and its relevance for animal behavior. Adv. Stud. Behav. 27, 1–131.CrossRefGoogle Scholar
- von Holst, D., Hutzelmeyer, H., Kaetzke, P., Khaschei, M., Rédel, H.G., Schrutka, H., 2002. Social rank, fecundity and lifetime reproductive success in wild European rabbits Oryctolagus cuniculus. Behav. Ecol. Sociobiol. 51, 245–254.CrossRefGoogle Scholar
- von Holst, D., Hutzelmeyer, H.D., Kaetzke, P., Khaschei, M., Schönheiter, R., 1999. Social rank, stress, fitness, and life expectancy in wild rabbits. Naturwissenschaften 86, 338–393.Google Scholar
- Wallage-Drees, J.M., 1989. A field study on seasonal changes in circadian activity of rabbits. Z. Säugetierkd. 54, 22–30.Google Scholar
- Wallage-Drees, J.M., Michielsen, N.C., 1989. The influence of food supply on the population dynamics of rabbits, Oryctolagus cuniculus (L.), in a Dutch dune area. Z. Säugetierkd. 54, 304–323.Google Scholar
- Zarrow, M.X., Denenberg, V.H., Anderson, C.O., 1965. Rabbit: frequency of suckling in the pup. Science 150, 1835–1836.PubMedCrossRefGoogle Scholar