Abstract
Before we can quantify the degree to which reproductive activities constitute a cost (i.e., depress an organism's probable future reproductive output), we need to determine the timescale over which such costs are paid. This is straightforward for species that acquire and expend resources simultaneously (income breeders), but more problematical for organisms that gather resources over a long period and then expend them in a brief reproductive phase (capital breeders). Most snakes are capital breeders; for example, female aspic vipers (Vipera aspis) in central western France exhibit a 2- to 3-year reproductive cycle, with females amassing energy reserves for one or more years prior to the year in which they become pregnant. We use long-term mark-recapture data on free-living vipers to quantify the appropriate timescale for studies of reproductive costs. Annual survival rates of female vipers varied significantly during their cycle, such that estimates of survival costs based only on years when the females were ‘reproductive’ (i.e., produced offspring) substantially underestimated the true costs of reproduction. High mortality in the year after reproducing was apparently linked to reproductive output; low energy reserves (poor body condition) after parturition were associated with low survival rates in the following year. Thus, measures of cost need to consider the timescale over which resources are gathered as well as that over which they are expended in reproductive activities. Also, the timescale of measurement needs to continue long enough into the post-reproductive period to detect delayed effects of reproductive ‘decisions’.
Similar content being viewed by others
References
Bell, G. (1980) The costs of reproduction and their consequences. American Naturalist 116, 45-76.
Bell, G. and Koufopanou, V. (1986) The cost of reproduction. In: R. Dawkins and M. Ridley (eds) Oxford Surveys in Evolutionary Biology. Oxford University Press, Oxford, pp. 83-131.
Blackburn, D.G. (1982) Evolutionary origins of viviparity in the Reptilia. I. Sauria. Amphibia-Reptilia 3, 185-205.
Blackburn, D.G. (1985) Evolutionary origins of viviparity in the Reptilia. II. Serpentes, Amphisbaenia, and Icthyosauria. Amphibia-Reptilia 6, 259-291.
Bonnet, X., Naulleau, G. and Mauget, R. (1994) The influence of body condition on 17-βestradiol levels in relation to vitellogenesis in female Vipera aspis(Reptilia, Viperidae). General and Comparative Endocrinology 93, 424-437.
Bonnet, X. and Naulleau, G. (1996) Catchability in snakes: consequences on breeding frequency estimates. Canadian Journal of Zoology 74, 233-239.
Bonnet, X., Bradshaw, D. and Shine, R. (1998) Capital versus income breeding: an ectothermic perspective. Oikos 83, 333-342.
Bonnet, X., Naulleau, G., Shine, R. and Lourdais, O. (2000) Reproductive versusecological advantages to larger body size in female snakes (Vipera aspis). Oikos 89, 509-518.
Bull, J.J. and Shine, R. (1979) Iteroparous animals that skip opportunities for reproduction. American Naturalist 114, 296-316.
Cherel, Y. (1995) Nutrient reserve storage, energetics, and food consumption during the prebreeding and premoulting foraging periods of king penguins. Polar Biology 15, 209-214.
Cherel, Y., Charassin, J.B. and Handrich, Y. (1993) Comparison of body reserves build-up in prefasting chicks and adults of king penguins (Aptenodytes patagonicus). Physiological Zoology 66, 750-770.
Cichon, M., Olejniczak, P. and Gustafsson, L. (1998) The effect of body condition on the cost of reproduction in female collared flycatchers Ficedula albicollis. Ibis 140, 128-130.
Clutton-Brock, T.H. (1991) The Evolution of Parental Care. Princeton University Press, Princeton, New Jersey.
Daan, S., Deerenberg, C. and Dijkstra, C. (1996) Increased daily work precipitates natural death in the kestrel. Journal of Animal Ecology 65, 539-544.
Drent, R.H. and Daan, S. (1980) The prudent parent: energetic adjustments in avian breeding. In: H. Klomp and J.W. Woldendorp (eds) The Integrated Study of Bird Populations. North-Holland, Amsterdam.
Fitch, H.S. (1981) Sexual size differences in reptiles. Miscellaneous Publications of the Museum of Natural History, University of Kansas 70, 1-72.
Gregory, P.T. (1982) Reptilian hibernation. In: C. Gans and F.H. Pough (eds) Biology of the Reptilia, Vol. 13, Academic Press, London, pp. 53-154.
Gustafson, L. and Sutherland, W. (1988) The costs of reproduction in the collared flycatcher Ficedula albicollis. Nature 335, 813-815.
James, C.D. and Whitford, W.G. (1994) An experimental study of phenotypic plasticity in the clutch size of a lizard. Oikos 70, 49-56.
Jönsson, K.I., Tuomi, J. and Järemo J. (1995a) Reproductive effort tactics: balancing pre-and postbreeding costs of reproduction. Oikos 74, 35-44.
Jönsson, K.I., Tuomi, J. and Järemo J. (1995b) On the consequences of pre-and postbreeding costs in the evolution of reproductive effort tactics. Écoscience 2, 311-320.
Jönsson, K.I. (1997) Capital and income breeding as alternative tactics of resource use in reproduction. Oikos 78, 57-66.
Lee, S.J., Witter, M.S., Cuthill, I.C. and Goldsmith, A.R. (1996) Reduction in escape performance as a cost of reproduction in gravid starlings, Sturnus vulgaris. Proceedings of the Royal Society, London B 263, 619-623.
Luiselli, L., Capula, M. and Shine, R. (1996) Reproductive output, costs of reproduction, and ecology of the smooth snake, Coronella austriaca, in the eastern Italian Alps. Oecologia 106, 100-110.
Madsen, T. and Shine, R. (1993) Costs of reproduction in a population of European adders. Oecologia 94, 488-495.
McCleery, R.H., Clobert, J., Julliard, R. and Perrins, C.M. (1996) Nest predation and delayed cost of reproduction in the great tit. Journal of Animal Ecology 65, 96-104.
Naulleau, G. and Bonnet, X. (1996) Body condition threshold for breeding in a viviparous snake. Oecologia 107, 301-306.
Naulleau, G., Bonnet, X. and Duret, S. (1996) Déplacements et domaines vitaux des femelles reproductrices de vipères aspic Vipera aspis(Reptilia, Viperidae) dans le centre ouest de la France. Bulletin de la Société Herpétologique de France 78, 5-18.
Nilsson, J.A. and Svensson, E. (1996) The cost of reproduction: a new link between current reproductive effort and future reproductive success. Proceedings of the Royal Society, London B 263, 711-714.
Nur, N. (1988) The costs of reproduction in birds: an examination of the evidence. Ardea 76, 155-168.
Olsson, M., Shine, R. and Bak-Olsson E. (2000) Locomotor impairment of gravid lizards: is the burden physical or physiological? Journal of Evolutionary Biology 13, 263-268.
Pough, F.H. (1980) The advantages of ectothermy for tetropods. American Naturalist 115, 92-112.
Saint Girons, H. (1952) Ecologie et éthologie des vipères de France. Annales des Sciences Naturelles, Zoologie 14, 263-343.
Saint Girons, H. (1957a) Croissance et fécondité de Vipera aspis(L). Vie et Milieu 8, 265-286.
Saint Girons, H. (1957b) Le cycle sexuel chez Vipera aspis(L). dans l'ouest de la France. Bulletin Biologique de France et de Belgique 91, 284-350.
Schaffer, W.M. (1974) Optimal reproductive effort in fluctuating environments. American Naturalist 964, 783-900.
Seigel, R.A., Huggins, M.M. and Ford, N.B. (1987) Reduction in locomotor ability as a cost of reproduction in snakes. Oecologia 73, 481-485.
Shine, R. (1980) Costs of reproduction in reptiles. Oecologia 46, 92-100.
Shine, R. and Schwarzkopf, L. (1992) The evolution of reproductive effort in lizards and snakes. Evolution 46, 62-75.
Sibly, R.M. and Calow, P. (1984) Direct and absorption costing in the evolution of life cycles. Journal of Theoretical Biology 111, 463-473.
Sinervo, B. and DeNardo, D.F. (1996) Costs of reproduction in the wild: path analysis of natural selection and experimental tests of causation. Evolution 50, 1299-1313.
Stearns, S.C. (1992) The evolution of life histories. Oxford University Press, Oxford.
Tombre, I.M. and Erikstad, K.E. (1996) An experimental study of incubation effort in high-arctic barnacle geese. Journal of Animal Ecology 65, 325-331.
Williams, G.C. (1966a) Adaptation and Natural Selection: A Critique of Some Current Evolutionary Thought. Princeton University Press, New Jersey.
Williams, G.C. (1966b) Natural selection, the costs of reproduction, and a refinement of Lack's principle. American Naturalist 100, 687-690.
Winkler, D.W. and Wallin, K. (1987) Offspring size and number: a life history model linking effort per offspring and total effort. American Naturalist 129, 708-720.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Bonnet, X., Naulleau, G., Shine, R. et al. What is the appropriate timescale for measuring costs of reproduction in a `capital breeder' such as the aspic viper?. Evolutionary Ecology 13, 485–497 (1999). https://doi.org/10.1023/A:1006712713698
Issue Date:
DOI: https://doi.org/10.1023/A:1006712713698