Age-specific reproductive success and cost in female Alpine ibex

Abstract

In female mammals, reproduction requires high energy expenditure because of gestation and lactation, possibly leading to a fitness cost. Several studies, however, failed to find the expected negative correlation between current and future reproductive success, likely because of individual heterogeneity in reproductive potential. We compared reproductive performance and costs of reproduction for 40 female Alpine ibex in one established population with 29 females translocated from the same population to a new colony. We investigate factors affecting pregnancy, fecundity and overwinter survival of juveniles, after accounting for individual heterogeneity. In both populations, prime-aged females experienced a strong reproductive cost. Senescent females, however, showed no evidence of reproductive costs. The colonizing population showed lower reproductive cost and better age-specific reproductive performance than the established population. We found a general pattern of low age-specific fecundity and reproductive success that was affected by environmental constraints. Age-specific reproductive success was unrelated to longevity. Although about 84 % of adult females appeared to conceive, independently of environmental constraints, energy was allocated to reproduction in a highly conservative manner, leading to low age-specific fecundity (only 36 and 21 % of prime-aged and senescent females were seen with a kid) but high kid survival (100 % to weaning and 92 % to 1 year). Our results suggest that females embarked on lactation only if they had a very high probability of raising their offspring. Our study highlights how reproductive performance and costs in this species vary with age and environment, and are the result of a highly conservative reproductive tactic.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3

References

  1. Beauplet G, Barbraud C, Dabin W, Küssener C, Guinet C (2006) Age-specific survival and reproductive performances in fur seals: evidence of senescence and individual quality. Oikos 112:430–441

    Article  Google Scholar 

  2. Bérubé CH, Festa-Bianchet M, Jorgenson JT (1996) Reproductive costs of sons and daughters in Rocky Mountain bighorn sheep. Behav Ecol 7:60–68

    Article  Google Scholar 

  3. Bonenfant C et al (2009) Empirical evidence of density-dependence in populations of large herbivores. Adv Ecol Res 41:313–357

    Article  Google Scholar 

  4. Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information—theoretic approach, 2dn. Springer Verlag, New York

    Google Scholar 

  5. Cam E, Link WA, Cooch EG, Monnat JY, Danchin E (2002) Individual covariation in life-history traits: seeing the trees despite the forest. Am Nat 159:96–105

    Article  PubMed  Google Scholar 

  6. Clutton-Brock TH (1984) Reproductive effort and terminal investment in iteroparous animals. Am Nat 123:212–229

    Article  Google Scholar 

  7. Clutton-Brock TH (1988) Reproductive success: studies of individual variation in contrasting breeding systems. University of Chicago Press, Chicago

    Google Scholar 

  8. Clutton-Brock TH, Guinness FE, Albon SD (1983) The costs of reproduction to red deer hinds. J Anim Ecol 52:367–383

    Article  Google Scholar 

  9. Clutton-Brock TH, Albon SD, Guinness FE (1989) Fitness costs of gestation and lactation in wild mammals. Nature 337:260–262

    Article  CAS  PubMed  Google Scholar 

  10. Clutton-Brock TH, Stevenson IR, Marrow P, MacColl AD, Houston AI, McNamara JM (1996) Population fluctuations, reproductive costs and life-history tactics in female Soay sheep. J Anim Ecol 65:675–689

    Article  Google Scholar 

  11. Côté SD, Festa-Bianchet M (2001) Reproductive success in female mountain goats: the influence of age and social rank. Anim Behav 62:173–181

    Article  Google Scholar 

  12. Couturier M (1962) Le bouquetin des Alpes, Grenoble

  13. Dematteis A (2005) Ecologia riproduttiva delle femmine di stambecco nella popolazione delle Alpi Marittime. Scienze Veterinarie. Università degli studi di Torino, Torino, p 213

    Google Scholar 

  14. Descamps S, Boutin S, Berteaux D, Gaillard JM (2006) Best squirrels trade a long life for an early reproduction. Proc R Soc B 273:2369–2374

    Article  PubMed Central  PubMed  Google Scholar 

  15. Festa-Bianchet M, Côté SD (2008) Body and horn growth. Mountain goats. Island Press, Washington, pp 91–117

    Google Scholar 

  16. Festa-Bianchet M, Jorgenson JT (1998) Selfish mothers: reproductive expenditure and resource availability in bighorn ewes. Behav Ecol 9:144–150

    Article  Google Scholar 

  17. Festa-Bianchet M, Gaillard J-M, Jorgenson JT (1998) Mass- and density-dependent reproductive success and reproductive costs in a capital breeder. Am Nat 152:367–379

    Article  CAS  PubMed  Google Scholar 

  18. Festa-Bianchet M, Jorgenson JT, Réale D (2000) Early development, adult mass, and reproductive success in bighorn sheep. Behav Ecol 11:633–639

    Article  Google Scholar 

  19. Fisher RA (1930) The genetical theory of natural selection. Clarendon, Oxford

    Book  Google Scholar 

  20. Floriani D (1975) Stambecco. Sui sentieri del RE. Cuneo, pp 98–104

  21. Fox CW, Roff DA, Fairbairn DJ (2001) Evolutionary ecology: concepts and case studies. Oxford University Press, Oxford

    Google Scholar 

  22. Gaillard J-M, Festa-Bianchet M, Yoccoz NG, Loison A, Toïgo C (2000) Temporal variation in fitness components and population dynamics of large herbivores. Annu Rev Ecol Syst 31:367–393

    Article  Google Scholar 

  23. Gittleman JL, Thompson SD (1988) Energy allocation in mammalian reproduction. Am Zool 3:863–875

    Google Scholar 

  24. Green WCH, Rothstein A (1991) Trade-offs between growth and reproduction in female bison. Oecologia 86:521–527

    Article  Google Scholar 

  25. Hamel S, Côté SD, Gaillard J-M, Festa-Bianchet M (2009) Individual variation in reproductive costs of reproduction: high-quality females always do better. J Anim Ecol 78:143–151

    Article  PubMed  Google Scholar 

  26. Hamel S, Côté SD, Festa-Bianchet M (2010a) Maternal characteristics and environment affect the costs of reproduction in female mountain goat. Ecology 91:2034–2043

    Article  PubMed  Google Scholar 

  27. Hamel S, Gaillard J-M, Yoccoz NG, Loison A, Bonenfant C, Descamps S (2010b) Fitness costs of reproduction depend on life speed: empirical evidence from mammalian populations. Ecol Lett 13:915–935

    Article  PubMed  Google Scholar 

  28. Jones OR et al (2008) Senescence rates are determined by ranking on the fast-slow life-history continuum. Ecol Lett 11:664–673

    Article  PubMed  Google Scholar 

  29. Langvatn R, Mysterud A, Stenseth NC, Yoccoz NG (2004) Timing and synchroNew York of ovulation in red deer constrained by short northern summers. Am Nat 163:763–772

    Article  PubMed  Google Scholar 

  30. Largo E et al (2008) Can ground counts reliably monitor ibex Capra ibex populations? Wildl Biol 14:489–499

    Article  Google Scholar 

  31. Lindström J (1999) Early development and fitness in birds and mammals. Trends Ecol Evol 14:343–348

    Article  PubMed  Google Scholar 

  32. Loison A, Toïgo C, Appolinaire J, Michallet J (2002) Demographic processes in colonizing populations of isard (Rupicapra pyrenaica) and ibex (Capra ibex). J Zool 256:199–205

    Article  Google Scholar 

  33. Martin JG, Festa-Bianchet M (2010) Bighorn ewes transfer the costs of reproduction to their lambs. Am Nat 176:414–423

    Article  PubMed  Google Scholar 

  34. Maudet C et al (2002) Microsatellite DNA and recent statistical methods in wildlife conservation management: applications in Alpine ibex [Capra ibex (ibex)]. Mol Ecol 11:421–436

    Article  CAS  Google Scholar 

  35. McNamara JM, Houston AI (1996) State-dependent life histories. Nature 380:215–221

    Article  CAS  PubMed  Google Scholar 

  36. Morin A (2013) Age-dependent costs of reproduction in female Alpine chamois (Rupicapra rupicapra). Master thesis, Université de Sherbrooke, Sherbrooke, pp 22–66

  37. Moyes K, Coulson T, Morgan BJT, Donald A, Morris SJ, Clutton-Brock TH (2006) Cumulative reproduction and survival costs in female red deer. Oikos 115:241–252

    Article  Google Scholar 

  38. Nakagawa S, Schielzeth H (2010) Repeatability for Gaussian and non-Gaussian data: a practical guide for biologists. Biol Rev 85:935–956

    PubMed  Google Scholar 

  39. Pinheiro JC, Bates DM (2000) Mixed-effects models in S and S-PLUS. Springer-Verlag, New York

    Book  Google Scholar 

  40. Pistorius PA, Bester MN, Hofmeyr GJ, Kirkman SP, Taylor FE (2008) Seasonal survival and the relative cost of first reproduction in adult female southern elephant seals. J Mamm 89:567–574

    Article  Google Scholar 

  41. R Development Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing. Vienna. ISBN 3-900051-07-0. URL http://www.R-project.org

  42. Ratti P, Habermehl KH (1977) Untersuchen zur Altersschätzung und Alterbestimmung beim Alpensteinbock (Capra ibex ibex) im Kanton Graubunden. Z Jagdwiss 4:188–213

    Google Scholar 

  43. Roff DA (1992) The evolution of life histories. Chapman and Hall, New York

    Google Scholar 

  44. Stearns SC (1992) The evolution of life histories. Oxford University Press, Oxford

    Google Scholar 

  45. Tavecchia G et al (2005) Predictors of reproductive cost in female Soay sheep. J Anim Ecol 74:201–213

    Article  Google Scholar 

  46. Therrien J-F, Côté SD, Festa-Bianchet M, Ouellet J-P (2007) Conservative maternal care in an iteroparous mammal: a resource allocation experiment. Behav Ecol Sociobiol 62:193–199

    Article  Google Scholar 

  47. Toïgo C, Gaillard J-M, Gauthier D, Girard I, Martinot JP, Michallet J (2002) Female reproductive success and costs in an alpine capital breeder under contrasting environments. Ecoscience 9:427–433

    Google Scholar 

  48. Toïgo C, Gaillard J-M, Festa-Bianchet M, Largo É, Michallet J, Maillard D (2007) Sex- and age-specific survival of the highly dimorphic Alpine ibex: evidence for a conservative life-history tactic. J Anim Ecol 76:679–686

    Article  PubMed  Google Scholar 

  49. van Noordwijk AJ, de Jong G (1986) Acquisition and allocation of resources: their influence on variation in life history tactics. Am Nat 128:137–142

    Article  Google Scholar 

  50. Weladji RB et al (2006) Good reindeer mothers live longer and become better in raising offspring. Proc R Soc B 273:1239–1244

    Article  PubMed Central  PubMed  Google Scholar 

  51. Williams GC (1966) Natural selection, the cost of reproduction, and a refinement of Lack’s principle. Am Nat 100:67–690

    Article  Google Scholar 

  52. Wilson AJ, Nussey DH (2009) What is individual quality? An evolutionary perspective. Trends Ecol Evol 25:207–214

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

Funding was provided by the Alpi Marittime Natural Park and the Province of Cuneo, Italy. We thank the Alpi Marittime Natural Park for their long-term effort in research and management of mountain ungulates. Particular thanks are due to the park wardens for capturing and monitoring animals. We thank Livio Martino, Fabrizio Rostagno, Arianna Menzano and Paolo Tizzani for help in fieldwork. Thanks to Fanie Pelletier for preliminary data analysis and to Audrée Morin for developing the permutation test. We also thank Jean-Michel Gaillard, Carole Toïgo, and an anonymous reviewer for insightful comments on previous draft of this paper.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Marco Rughetti.

Additional information

Communicated by Jean-Michel Gaillard.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Rughetti, M., Dematteis, A., Meneguz, P.G. et al. Age-specific reproductive success and cost in female Alpine ibex. Oecologia 178, 197–205 (2015). https://doi.org/10.1007/s00442-014-3192-3

Download citation

Keywords

  • Capra ibex
  • Environmental constraints
  • Individual heterogeneity
  • Permutation test
  • Reproductive cost