Behavioral Ecology and Sociobiology

, Volume 67, Issue 8, pp 1249–1258 | Cite as

Sex differences in the consequences of maternal loss in a long-lived mammal, the red deer (Cervus elaphus)

  • Daniel Andres
  • Tim H. Clutton-Brock
  • Loeske E. B. Kruuk
  • Josephine M. Pemberton
  • Katie V. Stopher
  • Kathreen E. Ruckstuhl
Original Paper


In several primates, the presence of mothers affects the growth, survival and reproduction of their offspring, but similar effects have not yet been demonstrated in ungulates. Here, we investigate the effects of the mother’s presence in a population of red deer (Cervus elaphus) on the Isle of Rum, Scotland, which is the subject of a long-term, individual-based study. We compared measures of performance including antler growth in young males and age at first reproduction in females and survival of deer with mothers still alive against those that have lost their mothers (orphans). We show that orphaning both before and after weaning increases the risk of a natural death for both sexes. For males, no maternal benefit was detectable past 24 months of age while, for females, post-weaning benefits continued throughout life. Orphaning resulted in compromised male physical condition as measured by a reduced probability of growing antlers by 16 months of age while no evidence for compromised reproduction was found in females. These results support assertions that post-weaning maternal associations affect the development and survival of offspring.


Maternal care Sex differences Orphaning Philopatry Emigration Red deer Cervus elaphus 



We would like to thank the Scottish Natural Heritage for permission to work on the Isle of Rum, the UK National Environmental Research Council for funding the project and the many dedicated field personnel for collecting the detailed data necessary to perform this study, especially Sean and Ali Morris, Martyn Baker and Fiona Guinness. We also thank Gillian Raab, professor emeritus at Napier University, for her helpful guidance with the survival analyses. This research was supported by the National Sciences and Engineering Research Council of Canada CGS and MSFSS scholarships awarded to D. Andres, and an NSERC DG to K.E. Ruckstuhl.

Ethical standards

Research followed the standards set out by the UK Home Office.

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

265_2013_1552_MOESM1_ESM.docx (26 kb)
ESM 1 (DOCX 26.4 kb)


  1. Allison PD (2010) Survival analysis using SAS: a practical guide. SAS Institute, CaryGoogle Scholar
  2. Brookshier JS, Fairbanks WS (2003) The nature and consequences of mother daughter associations in naturally and forcibly weaned bison. Can J Zool 81:414–423CrossRefGoogle Scholar
  3. Clutton-Brock TH (1991) The evolution of parental care. Princeton University Press, PrincetonGoogle Scholar
  4. Clutton-Brock TH (1994) The costs of sex. In: Short R, Balaban E (eds) The differences between the sexes. Cambridge University Press, CambridgeGoogle Scholar
  5. Clutton-Brock TH, Albon S, Guinness F (1981) Parental investment in male and female offspring in polygynous mammals. Nature 289:487–489CrossRefGoogle Scholar
  6. Clutton-Brock TH, Guinness FE, Albon SB (1982) Red deer: behavior and ecology of two sexes. The University of Chicago Press, ChicagoGoogle Scholar
  7. Clutton-Brock T, Coulson T, Milner-Gulland E, Thomson D, Armstrong H (2002) Sex differences in emigration and mortality affect optimal management of deer populations. Nature 415:633–637CrossRefPubMedGoogle Scholar
  8. Dixon KR, Chapman JA (1980) Harmonic mean measure of animal activity areas. Ecology 61:1040–1044CrossRefGoogle Scholar
  9. Etter DR, Nixon CM, Sullivan JB, Thomas JA (1995) Emigration and survival of orphaned female whitetailed deer in Illinois. Can J Zool 73:440–445CrossRefGoogle Scholar
  10. Fairbanks LA (2000) Maternal investment throughout the life span in Old World monkeys. In: Whitehead P, Jolly C (eds) Old World monkeys. Cambridge University Press, CambridgeGoogle Scholar
  11. Fairbanks L, McGuire M (1986) Age, reproductive value, and dominance-related behaviour in vervet monkey females: cross-generational influences on social relationships and reproduction. Anim Behav 34:1710–1721CrossRefGoogle Scholar
  12. Foster EA, Franks DW, Mazzi S, Darden SK, Balcomb KC, Ford JKB, Croft DP (2012) Adaptive prolonged postreproductive life span in killer whales. Science 337:1313–1313CrossRefPubMedGoogle Scholar
  13. Giuliano WM, Demarais S, Zaiglin RE, Sumner ML (1999) Survival and movements of orphaned white-tailed deer fawns in Texas. J Wildl Manag 63:1390–1390Google Scholar
  14. Green WCH, Griswold JG, Rothstein A (1989) Post-weaning associations among bison mothers and daughters. Anim Behav 38:847–858CrossRefGoogle Scholar
  15. Grovenburg TW, Jenks JA, Jacques CN, Klaver RW, Swanson CC (2009) Aggressive defensive behavior by free-ranging white-tailed deer. J Mammal 90:1218–1223CrossRefGoogle Scholar
  16. Guinness FE, Clutton-Brock TH, Albon SD (1978) Factors affecting calf mortality in red deer (Cervus elaphus). J Anim Ecol 47:817CrossRefGoogle Scholar
  17. Guinness FE, Hall MJ, Cockerill RA (1979) Mother–offspring association in red deer (Cervus elaphus) on Rhum. Anim Behav 27:536–544CrossRefGoogle Scholar
  18. Holand O, Weladji RB, Mysterud A, Roed K, Reimers E, Nieminen M (2012) Induced orphaning reveals post-weaning maternal care in reindeer. Eur J Wildl Res 58:589–596CrossRefGoogle Scholar
  19. Holekamp KE, Smale L (2010) Provisioning and food sharing by lactating spotted hyenas, Crocuta crocuta (Mammalia: Hyaenidae). Ethology 86:191–202CrossRefGoogle Scholar
  20. Holzenbein S, Marchinton RL (1992) Emigration and mortality in orphaned male white-tailed deer. J Wildl Manag 56:147–153CrossRefGoogle Scholar
  21. Jaeggi AV, van Noordwijk MA, van Schaik CP (2008) Begging for information: mother–offspring food sharing among wild Bornean orangutans. Am J Primatol 70:533–541CrossRefPubMedGoogle Scholar
  22. Jolicoeur H, Crete M (1988) Winter survival and habitat use of orphaned and non-orphaned moose calves in southern Quebec. Can J Zool 66:919–924CrossRefGoogle Scholar
  23. Kaminski G, Brandt S, Baubet E, Baudoin C (2005) Life-history patterns in female wild boars (Sus scrofa): mother–daughter postweaning associations. Can J Zool 83:474–480CrossRefGoogle Scholar
  24. Mirza SN, Provenza FD (1992) Effects of age and conditions of exposure on maternally mediated food selection by lambs. Appl Anim Behav Sci 33:35–42CrossRefGoogle Scholar
  25. Murray CM, Gilby IC, Mane SV, Pusey AE (2008) Adult male chimpanzees inherit maternal ranging patterns. Curr Biol 18:20–24CrossRefPubMedGoogle Scholar
  26. Nelson ME (1998) Development of migratory behavior in northern white-tailed deer. Can J Zool 76:426–432CrossRefGoogle Scholar
  27. Nowak R, Porter RH, Lévy F, Orgeur P, Schaal B (2000) Role of mother–young interactions in the survival of offspring in domestic mammals. Rev Reprod 5:153–163CrossRefPubMedGoogle Scholar
  28. Nussey DH, Metherell B, Moyes K, Donald A, Guinness FE, Clutton-Brock TH (2007) The relationship between tooth wear, habitat quality and late-life reproduction in a wild red deer population. J Anim Ecol 76:402–412CrossRefPubMedGoogle Scholar
  29. Oostindjer M, Bolhuis JE, Mendl M, Held S, van den Brand H, Kemp B (2011) Learning how to eat like a pig: effectiveness of mechanisms for vertical social learning in piglets. Anim Behav 82:503–511CrossRefGoogle Scholar
  30. Pavelka MS, Fedigan LM, Zohar S (2002) Availability and adaptive value of reproductive and postreproductive Japanese macaque mothers and grandmothers. Anim Behav 64:407–414CrossRefGoogle Scholar
  31. Pollard JC, Asher GW, Littlejohn RP (2002) Weaning date affects calf growth rates and hind conception dates in farmed red deer (Cervus elaphus). Anim Sci 74:111–116Google Scholar
  32. Reiter J, Stinson NL, Boeuf BJ (1978) Northern elephant seal development: the transition from weaning to nutritional independence. Behav Ecol Sociobiol 3:337–367CrossRefGoogle Scholar
  33. Sanga U, Provenza FD, Villalba JJ (2011) Transmission of self-medicative behaviour from mother to offspring in sheep. Anim Behav 82:219–227CrossRefGoogle Scholar
  34. Silk JB (2007a) The adaptive value of sociality in mammalian groups. Philos T Roy Soc B 362:539–559CrossRefGoogle Scholar
  35. Silk JB (2007b) Social components of fitness in primate groups. Science 317:1347–1351CrossRefPubMedGoogle Scholar
  36. Stokes ME (1999) Recent advances in categorical data analysis. SAS, SUGI Proceedings. Accessed 19 March 2013
  37. Surbeck M, Mundry R, Hohmann G (2011) Mothers matter! Maternal support, dominance status and mating success in male bonobos (Pan paniscus). Proc R Soc Lond B 278:590–598CrossRefGoogle Scholar
  38. van Noordwijk MA (2012) From maternal investment to lifetime maternal care. In: Mitani J, Call J, Kappeler P, Palombit R, Silk J (eds) The evolution of primate societies. University of Chicago Press, ChicagoGoogle Scholar
  39. Williams SC (2008) Surviving survival analysis: an applied introduction. Institute for Advanced Analytics. Accessed 19 March 2013
  40. Woodson DL, Reed ET, Downing RL, McGinnes BS (1980) Effect of fall orphaning on white-tailed deer fawns and yearlings. J Wildl Manag 44:249–252CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Daniel Andres
    • 1
  • Tim H. Clutton-Brock
    • 2
  • Loeske E. B. Kruuk
    • 3
    • 4
  • Josephine M. Pemberton
    • 4
  • Katie V. Stopher
    • 4
  • Kathreen E. Ruckstuhl
    • 1
  1. 1.Department of Biological SciencesUniversity of CalgaryCalgaryCanada
  2. 2.Department of ZoologyUniversity of CambridgeCambridgeUK
  3. 3.Division of Evolution, Ecology & Genetics, Research School of BiologyThe Australian National UniversityCanberraAustralia
  4. 4.Institute of Evolutionary Biology, School of Biological SciencesUniversity of EdinburghEdinburghUK

Personalised recommendations