Behavioral Ecology and Sociobiology

, Volume 37, Issue 5, pp 311–319 | Cite as

Is sex-biased maternal care limited by total maternal expenditure in polygynous ungulates?

  • Christophe Pélabon
  • Jean-Michel Gaillard
  • Anne Loison
  • Christine Portier


We examined data on sex-specific differences in neonatal weight, litter size and adult female body weight in 32 populations of polygynous ungulates of 18 different species to test for the existence of a trade-off between sex-biased maternal care and the total amount of maternal expenditure. This corresponds to an extension of the hypothesis of Byers and Moodie (1990) that sex-biased maternal care is limited by a high level of maternal expenditure. We did not find any relationship between sex-biased care and two measures of total maternal expenditure. We highlighted high intraspecific variability in sex-biased care and very low intraspecific variability in total maternal expenditure. Even when this between-population variability in sex-biased care was accounted for, no relationship between sex-biased maternal care and maternal expenditure was detected. Apart from difficulties in finding suitable measures for both variables, two other reasons may account for the lack of a relationship between sex-biased maternal care and total maternal expenditure. Firstly, male offspring seem to be more affected than female offspring by harsh environmental conditions. This may lead to the variation observed in the extent of sex-specific differences in birth weight within a single species. If we assume that for a given maternal expenditure reproductive costs incurred by mothers are highest during harsh conditions, this could indicate the existence of a trade-off between sex-biased maternal care and maternal expenditure at the intra-specific level, thereby supporting the Byers and Moodie hypothesis. Secondly, polygyny is only a poor predictor of sex-biased care and factors such as compensatory growth or extended periods of growth may be expected to modify predictions for different species. Thus, environmental conditions and relative effects of maternal care on male and female lifetime reproductive success are better predictors of sex-biased care than total maternal expenditure.

Key words

Sex-biased care Maternal expenditure Ungulates Neonatal dimorphism 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Anderson SS, Fedak MA (1987) Grey seal, Halichoerus grypus, energetics:females invest more in male offspring. J Zool Lond 211:667–679Google Scholar
  2. Asher GW, Adam JL (1985) Reproduction of farmed red and fallow deer in northern New Zealand. Biology of deer production. R Soc N Z 22:217–224Google Scholar
  3. Baker RJ (1987) GLIM 3.77 reference manual, 2nd edn, Numerical Algorithms Group, OxfordGoogle Scholar
  4. Bannikov AG, Zhirnov LV, Lebedeja LS, Fandeen AA (1967) Biology of the saïga. Israel Program for Scientific Translation, JerusalemGoogle Scholar
  5. Bartmann RM, White GC, Carpenter LH (1992) Compensatory mortality in a Colorado mule deer population. Wildl Monogr 121:1–39PubMedGoogle Scholar
  6. Benton MJ (1988) The phylogeny and classification of the tetrapods, vol 2. Mammals. Oxford University Press, New YorkGoogle Scholar
  7. Berger J (1992) Facilitation of reproductive synchrony by gestation adjustment in gregarious mammals: anew hypothesis. Ecology 73:323–329Google Scholar
  8. Birgersson B, Ekvall K (1994) Suckling time and fawn growth in fallow deer (Dama dama). J Zool Lond 232:641–650Google Scholar
  9. Blaxter KL, Hamilton WJ (1980) Reproduction in farmed red deer. 2. Calf growth and mortality. J Agric Sci Camb 95:275–284Google Scholar
  10. Braza F, San José C (1988) An analysis of mother-young behaviour of fallow deer during lactation period. Behav Proc 17:93–106Google Scholar
  11. Braza F, San José C, Bloom A (1988) Birth measurements, parturition dates and progeny sex ratio of Dama dama in Donana, Spain. J Mammal 69:607–610Google Scholar
  12. Byers JA, Moodie JD (1990) Sex-specific maternal investment in pronghorn, and the question of a limit on differential provisioning in ungulates. Behav Ecol Sociobiol 26:157–164Google Scholar
  13. Calder WA (1984) Size, function and life history. Harvard University Press, CambridgeGoogle Scholar
  14. Clutton-Brock TH (1988) Reproductive success. Studies of individual variation in contrasting breeding systems. Chicago University Press, ChicagoGoogle Scholar
  15. Clutton-Brock TH (1991) The evolution of parental care. Princeton University Press, PrincetonGoogle Scholar
  16. Clutton-Brock TH (1992) The evolution of sex differences and the consequences of polygyny in mammals. In: Bateson P (ed) The development and integration of behaviour. Cambridge University Press, Cambridge, pp 229–253Google Scholar
  17. Clutton-Brock TH, Albon SD, Guinness FE (1982) Red deer:the behaviour and ecology of the two sexes. Chicago University Press, ChicagoGoogle Scholar
  18. Clutton-Brock TH, Guinness FE, Albon SD (1983) The cost of reproduction to red deer hinds. J Anim Ecol 52:367–783Google Scholar
  19. Doney JM, Ryder ML, Gunn RG, Grubb P (1974) Colour conformation, affinities, fleece and patterns of inheritance of the Soay sheep. In: Jewell PA, Milner C, Morton Boyd J (eds) Island survivors. Althone Press, London, pp 88–125Google Scholar
  20. English AW (1992) Management strategies for farmed Chital deer. In: Brown RD (ed) The biology of deer. Springer, Berlin Heidelberg New York, pp 189–196Google Scholar
  21. Eisenberg JF (1981) The mammalian radiations. Chicago University Press, ChicagoGoogle Scholar
  22. Felsenstein J (1985) Phylogenies and the comparative method. Am Nat 125:1–15CrossRefGoogle Scholar
  23. Festa-Bianchet M (1988) Nursing behaviour of bighorn sheep: correlates of ewe age, parasitism, lamb age, birthdate and sex. Anim Behav 36:1445–1454Google Scholar
  24. Fletcher IC (1971) Relationships between frequency of suckling, lamb growth and post-partum oestrus behaviour in ewes. Anim Behav 19:108–111Google Scholar
  25. Gaillard JM, Pontier D, Brandt S, Jullien JM, Allainé D (1992) Sex differentiation in postnatal growth rate: a test in wild boar population. Oecologia 90:167–171Google Scholar
  26. Gaillard JM, Delorme D, Jullien JM (1993) Croissance précoce et poids à l'entrée de l'hiver chez le faon de chevreuil (Capreolus capreolus). Mammalia 57:359–366Google Scholar
  27. Gauthier D, Barrette C (1985) Suckling and weaning in captivewhite-tailed and fallow deer. Behaviour 94:128–149Google Scholar
  28. Gittleman JL, Luh HK (1992) On comparing comparative methods. Annu Rev Ecol Syst 23:383–404Google Scholar
  29. Gittleman JL, Thompson SD (1988) Energy allocation in mammalian reproduction. Am Zool 28:863–875Google Scholar
  30. Grafen A (1989) The phylogenetic regression. Philos Trans R Soc Lond B 326:119–157Google Scholar
  31. Green WCH, Berger J (1990) Maternal investment in sons and daughters: problems of methodology. Behav Ecol Sociobiol 27:99–102Google Scholar
  32. Green WCH, Rothstein A (1991) Sex bias or equal opportunity? Patterns of maternal investment in bison. Behav Ecol Sociobiol 29:373–384Google Scholar
  33. Harvey PH, Mace GM (1982) Comparisons between taxa and adaptive trends. In: King's College Sociobiology group (eds) Current problems in sociobiology. Cambridge University Press, Cambridge, pp 343–361Google Scholar
  34. Harvey PH, Pagel MD (1991) The comparative method in evolutionary biology. Oxford University Press, OxfordGoogle Scholar
  35. Harvey PH, Purvis A (1991) Comparative method for explaining adaptations. Nature 351:619–624PubMedGoogle Scholar
  36. Heptner VG, Nasimovich AA, Bannikov AG (1989) Mammals of the Soviet Union. Brill, LeidenGoogle Scholar
  37. Hogg JT, Hass CC, Jenni DA (1992) Sex-biased maternal expenditure in rocky mountain bighorn sheep. Behav Ecol Sociobiol 31:243–251Google Scholar
  38. Holter JB, Hayes HH (1977) Growth in white-tailed deer fawns fed varying energy and constant protein. J Wildl Manage 41:506–510Google Scholar
  39. Jeffrey RCV, Hanks J (1981) Body growth of captive eland Taurotragus onyx in Natal. S Afr J Zool 16:183–189Google Scholar
  40. Johnson DE (1951) Biology of the elk calf, Cervus canadensis nelsoni. J Wildl Manage 15:396–410Google Scholar
  41. Jorgenson JT, Festa-Bianchet M, Lucherini M, Wishart WD (1993) Effects of body size, population density and maternal characteristics on age of first reproduction in bighorn ewes. Can J Zool 71:2509–2517Google Scholar
  42. Kojola I (1993) Early maternal investment and growth in reindeer. Can J Zool 71:753–758Google Scholar
  43. Krebs CJ, Cowan I McT (1962) Growth studies of reindeer fawns. Can J Zool 40:863–869Google Scholar
  44. Langenau EE, Lerg JM (1976) The effects of winter nutritional stress on maternal and neonatal behavior in penned white-tailed deer. Appl Anim Ethol 2:207–223Google Scholar
  45. Langvatn R (1977) Criteria of physical condition, growth and development in cervidae suitable for routine studies. Nordic Council for Wildlife Research, StockholmGoogle Scholar
  46. Lavigueur L, Barrette C (1992) Suckling, weaning, and growth in captive woodland caribou. Can J Zool 70:1753–1766Google Scholar
  47. Lee PC, Moss CJ (1986) Early maternal investment in male and female African elephant calves. Behav Ecol Sociobiol 18:353–361Google Scholar
  48. Lee PC, Majluf P, Gordon IJ (1991) Growth, weaning and maternal investment from a comparative perspective. J Zool Lond 225:99–114Google Scholar
  49. Lloyd PH, Rasa OAE (1989) Status, reproductive success and fitness in Cape mountain zebra (Equus zebra zebra). Behav Ecol Sociobiol 25:411–420Google Scholar
  50. Martin P (1984) The meaning of weaning. Anim Behav 32: 1257–1258Google Scholar
  51. Maynard Smith J (1980) A new theory of sexual investment. Behav Ecol Sociobiol 7:247–251Google Scholar
  52. Mc Ewan EH, Whitehead PE (1972) Reproduction in female reindeer and caribou. Can J Zool 50:43–46Google Scholar
  53. Millar JS (1977) Adaptative features of mammalian reproduction. Evolution 31:370–386Google Scholar
  54. Miles DB, Dunham AE (1993) Historical perspectives in ecology and evolutionary biology: The use of phylogenetic comparative analyses. Annu Rev Ecol Syst 24:587–619Google Scholar
  55. Mitchell GJ (1980) The pronghorn antilope in Alberta. GJ Mitchell, Univ Regina. Sask Monogr 165 ppGoogle Scholar
  56. Moore GH, Littlejohn RP, Cowie GM (1988) Factors affecting liveweight gain in red deer calves from birth to weaning. N Z J Agric Res 31:279–283Google Scholar
  57. Møller AP, Birkhead TR (1992) A pairwise comparative method as illustrated by copulation frequency in birds. Am Nat 139:644–656Google Scholar
  58. Mulley RC, English AW, Kirby A (1990) The reproductive performance of farmed fallow deer (Dana dama) in New South Wales. Aust Vet J 67:281–286Google Scholar
  59. Novak RM (1991) Walker's mammals of the world, 5th edn. John Hopkins University Press, BaltimoreGoogle Scholar
  60. Oftedal OT (1984) Milk composition, milk yield and energy output at peak lactation:a comparative review. Symp Zool Soc Lond 51:33–85Google Scholar
  61. Oftedal OT (1985) Pregnancy and lactation. In: Hudson RJ, White RG (eds) Bioenergetics of wild herbivores. CRC Press, Boca Raton, pp 215–238Google Scholar
  62. Pemberton JM, Dancie O (1983) Live weights of fallow deer (Dama dama) in British deer parks. J Zool Lond 199: 171–177Google Scholar
  63. Peters RH (1983) The ecological implications of body size. Cambridge University Press, CambridgeGoogle Scholar
  64. Petit T, Poilane A, Poilane JF, Seitre J, Seitre R (1989) Croissance de l'oryx d'Arabie. Mammalia 53:97–108Google Scholar
  65. Pontier D, Gaillard JM, Allainé D, Trouvilliez J, Gordon I, Duncan P (1989) Postnatal growth rate and adult body weight in mammals: a new approach. Oecologia 80:390–394Google Scholar
  66. Pontier D, Gaillard JM, Allainé D (1993) Maternal investment per offspring and demographic tactics in placental mammals. Oikos 66:424–430Google Scholar
  67. Read AF, Harvey PH (1989) Life history differences among the eutherian radiations. J Zool Lond 219:329–353Google Scholar
  68. Robbins CT, Robbins BL (1979) Fetal and neonatal growth patterns and maternal reproductive effort in ungulates and subungulates. Am Nat 114:101–116Google Scholar
  69. Robertson A, Hiraiwa-Hasegawa M, Albon SD, Clutton-Brock TH (1992) Early growth and suckling behaviour of Soay sheep in fluctuating population. J Zool Lond 227:661–671Google Scholar
  70. Robinette WL, Archer AL (1971) Notes on ageing criteria and reproduction of Thomson's gazelle. E Afr Wildl J 9:83–98Google Scholar
  71. Sadleir RMFS (1969) The ecology and reproduction in wild and domestic mammals. Methuen, LondonGoogle Scholar
  72. Sadleir RMFS (1984) Ecological consequences of lactation. Acta Zool Fenn 171:179–182Google Scholar
  73. San José C, Braza F (1993) Adoptive behaviour in fallow deer (Damn dama) Z. Säugetierk 58:122–123Google Scholar
  74. Schwartz CC, Hundertmark KJ (1993) Reproductive characteristics of Alaskan moose. J Wildl Manage 57:454–468Google Scholar
  75. Skogland T (1990) Density dependence in a fluctuating wild reindeer herd; maternal vs. offspring effects. Oecologia 84:442–450Google Scholar
  76. Talbot LM, Talbot MH (1963) The wildebeest in western Masailand. Wildl Monogr 12:88 ppGoogle Scholar
  77. Thorne ET, Dean RE, Hepworth WC (1976) Nutrition during gestation in relation to successful reproduction in elk. J Wildl Manage 440:330–335Google Scholar
  78. Trivers RL, Willard DE (1973) Natural selection of parental ability to vary the sex ratio of offspring. Science 179:90–92PubMedGoogle Scholar
  79. Verme LJ (1963) Effect of nutrition on growth of white tailed deer fawns. North Am Wildl Conf 24:431–443Google Scholar
  80. Verme LJ (1989) Maternal investment in white-tailed deer. J Mammal 70:438–442Google Scholar
  81. Walmo OC (1981) Mule and black-tailed deer of North America. University of Nebraska Press, LincolnGoogle Scholar
  82. Wolff JO (1988) Maternal investment and sex ratio adjustment in American bison. Behav Ecol Sociobiol 23:127–133Google Scholar

Copyright information

© Springer-Verlag 1995

Authors and Affiliations

  • Christophe Pélabon
    • 1
  • Jean-Michel Gaillard
    • 1
  • Anne Loison
    • 1
  • Christine Portier
    • 1
  1. 1.Laboratoire de Biométrie Génétique et Biologie des Populations, URA CNRS 2055Université Lyon IVilleurbanne CedexFrance

Personalised recommendations