Skip to main content
SpringerLink
Log in

Sex-specific reproductive behaviours and paternity in free-ranging Barbary macaques (Macaca sylvanus)

  • Original Paper
  • Published:
Behavioral Ecology and Sociobiology Aims and scope Submit manuscript

Abstract

In a wide variety of species, male reproductive success is determined by contest for access to females. Among multi-male primate groups, however, factors in addition to male competitive ability may also influence paternity outcome, although their exact nature and force is still largely unclear. Here, we have investigated in a group of free-ranging Barbary macaques whether paternity is determined on the pre- or postcopulatory level and how male competitive ability and female direct mate choice during the female fertile phase are related to male reproductive success. Behavioural observations were combined with faecal hormone analysis for timing of the fertile phase (13 cycles, 8 females) and genetic paternity analysis (n = 12). During the fertile phase, complete monopolisation of females did not occur. Females were consorted for only 49% of observation time, and all females had ejaculatory copulations with several males. Thus, in all cases, paternity was determined on the postcopulatory level. More than 80% of infants were sired by high-ranking males, and this reproductive skew was related to both, male competitive ability and female direct mate choice as high-ranking males spent more time in consort with females than low-ranking males, and females solicited copulations mainly from dominant males. As most ejaculatory copulations were female-initiated, female direct mate choice appeared to have the highest impact on male reproductive success. However, female preference was not directly translated into paternity, as fathers were not preferred over non-fathers in terms of solicitation, consortship and mating behaviour. Collectively, our data show that in the Barbary macaque, both sexes significantly influence male mating success, but that sperm of several males generally compete within the female reproductive tract and that therefore paternity is determined by mechanisms operating at the postcopulatory level.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Alberts SC, Altmann J, Wilson ML (1996) Mate guarding constrains foraging activity of male baboons. Anim Behav 51:1269–1277

    Article  Google Scholar 

  • Altmann SA (1962) A field study of the socio-biology of rhesus monkeys, Macaca mulatta. Ann NY Acad Sci 102:277–285

    Article  Google Scholar 

  • Altmann J (1974) Observational study of behavior: sampling methods. Behaviour 49:227–267

    Article  PubMed  CAS  Google Scholar 

  • Altmann J, Alberts SC, Haines SA, Durbach J, Muruthi P, Coote T, Geffen E, Cheesman DJ, Mututua RS, Saiyalel SN, Wayne RK, Lacy RC, Brudford MW (1996) Behavior predicts genetic structure in a wild primate group. Proc Natl Acad Sci USA 93:5797–5801

    Article  PubMed  CAS  Google Scholar 

  • Andersson M (1994) Sexual Selection. Princeton University Press, Princeton, New Jersey

    Google Scholar 

  • Aujard F, Heistermann M, Thierry B, Hodges JK (1998) Functional significance of behavioral, morphological, and endocrine correlates across the ovarian cycle in semifree ranging female Tonkean macaques. Am J Primatol 46:285–309

    Article  PubMed  CAS  Google Scholar 

  • Bayes MK, Smith KL, Alberts SC, Altmann J, Bruford MW (2000) Testing the reliability of microsatellite typing from faecal DANN in the savannah baboon. Cons Gen 1:173–176

    Article  CAS  Google Scholar 

  • Behboodi E, Katz DF, Samuels SJ, Tell L, Hendrickx AG, Lasley BL (1991) The use of a urinary estrone conjugates assay for detection of optimal mating time in the cynomolgus macaque (Macaca fascicularis). J Med Primatol 20:229–234

    PubMed  CAS  Google Scholar 

  • Berard JD, Nurnberg P, Epplen JT, Schmidtke J (1993) Male rank, reproductive behavior, and reproductive success in free-ranging rhesus macaques. Primates 34:481–489

    Article  Google Scholar 

  • Bercovitch FB (1983) Time budgets and consortships in olive baboons (Papio anubis). Folia Primatol 41:180–190

    Article  Google Scholar 

  • Bercovitch FB (1995) Female cooperation, consortship maintenance and male mating success in savanna baboons. Anim Behav 50:137–149

    Article  Google Scholar 

  • Birkhead TR (2000) Promiscuity: an evolutionary history of sperm competition and sexual conflict. Faber and Faber, London

    Google Scholar 

  • Birkhead TR, Kappeler PM (2004) Post-copulatory sexual selection in birds and primates. In: Kappeler PM, van Schaik CP (eds) Sexual selection in primates: new and comparative aspects. Cambridge University, Cambridge, pp 151–171

    Google Scholar 

  • Birkhead TR, Møller AP (1998) Sperm competition and sexual selection. Academic, London

    Google Scholar 

  • Boesch C, Kohou G, Néné H, Vigilant L (2006) Male competition and paternity in wild chimpanzees of the Taï Forest. Am J Phys Anthropol 130:103–115

    Article  PubMed  Google Scholar 

  • Boinski S (1987) Mating patterns in squirrel monkeys (Samiri oerstedii): Implications for seasonal sexual dimorphisms. Behav Ecol Sociobiol 21:13–21

    Article  Google Scholar 

  • Borries C, Launhardt K, Epplen C, Epplen JT, Winkler P (1999) Males as infant protectors in Hanuman langurs (Presbytis entellus) living in multimale groups—defence pattern, paternity and sexual behaviour. Behav Ecol Sociobiol 46:350–356

    Article  Google Scholar 

  • Brauch K, Pfefferle D, Hodges K, Möhle U, Fischer J, Heistermann M (2007) Female sexual behavior and sexual swelling size as potential cues for males to discern the female fertile phase in free-ranging Barbary macaques (Macaca sylvanus) of Gibraltar. Horm Behav 52:375–383

    Article  PubMed  Google Scholar 

  • Cant MA (1998) A model for the evolution of reproductive skew without reproductive suppression. Anim Behav 55:163–169

    Article  PubMed  Google Scholar 

  • Chambers KE, Reichard UH, Möller A, Nowak K, Vigilant L (2004) Cross-species amplification of human microsatellite markers using noninvasive samples from white-handed gibbons (Hylobates lar). Am J Primatol 64:19–27

    Article  PubMed  Google Scholar 

  • Cheney DL, Seyfarth RM (1987) The influence of intergroup competition on the survival and reproduction of female vervet monkeys. Behav Ecol Sociobiol 21:375–386

    Article  Google Scholar 

  • Chism J, Rogers W (1997) Male competition, mating success and female choice in a seasonally breeding primate. Ethology 103:109–126

    Article  Google Scholar 

  • Clutton-Brock TH (1998) Reproductive skew concessions and limited control. TREE 13:288–292

    Google Scholar 

  • Cowlishaw G, Dunbar RIM (1991) Dominance rank and mating success in male primates. Anim Behav 41:1045–1056

    Article  Google Scholar 

  • Creel SR, Mills MGL, Monfort SL (1997) Rank and reproduction in cooperatively breeding African wild dogs: behavioural and endocrine correlates. Behav Ecol 8:298–306

    Article  Google Scholar 

  • Darwin C (1871) The descent of man and the selection in relation to sex. John Murray, London

    Google Scholar 

  • Dewsbury DA (1982) Ejaculate cost and male choice. Am Nat 119:601–610

    Article  Google Scholar 

  • Dixson AF (1998) Primate Sexuality. Oxford University Press, Oxford

    Google Scholar 

  • Dunbar RIM, Cowlishaw G (1992) Mating success in male primates: dominance rank, sperm competition and alternative strategies. Anim Beh 44:1171–1173

    Article  Google Scholar 

  • Eberhard WG (1996) Female control: sexual selection by cryptic female choice. Princeton University Press, Princeton

    Google Scholar 

  • Eberle M, Kappeler PM (2002) Mouse lemurs in space and time: a test of the socioecological model. Behav Ecol Sociobiol 51:131–139

    Article  Google Scholar 

  • Ellis L (1995) Dominance and reproductive success among non-human animals: a cross-species comparison. Ethol Sociobiol 16:257–333

    Article  Google Scholar 

  • Emlen ST, Oring LW (1977) Ecology, sexual selection, and the evolution of mating systems. Science 197:215–223

    Article  PubMed  CAS  Google Scholar 

  • Engelhardt A, Heistermann M, Hodges JK, Nürnberg P, Niemitz C (2006) Determinants of male reproductive success in wild long-tailed macaques (Macaca fascicularis)—male monopolisation, female mate choice or post-copulatory mechanisms? Behav Ecol Sociobiol 59:740–752

    Article  Google Scholar 

  • Glick BB (1980) Ontogenetic and psychobiological aspects of the mating activities of male Macaca radiata. In: Lindburg DG (ed) The macaques: studies in ecology, behaviour and evolution. Van Nostrand Reinhold, New York, pp 345–369

    Google Scholar 

  • Grob B, Knapp LA, Martin RD, Anzenberger G (1998) The major histocompatibility complex and mate choice: inbreeding avoidance and selection of good genes. Exp Clin Immunogen 15:119–129

    Article  CAS  Google Scholar 

  • Harcourt AH (1995) Sexual selection in primates: what are male genitalia good for? Evol Anthropol 4:121–129

    Article  Google Scholar 

  • Harcourt AH, Purvis A, Liles L (1996) Sperm competition: mating system, not breeding season, affects testes size of primates. Funct Ecol 9:468–476

    Article  Google Scholar 

  • Hasegawa T, Hiraiwa-Hasegawa M (1990) Sperm competition and mating behaviour. In: Nishida T (ed) The chimpanzees of the Mahale mountains: sexual and life history strategies. University of Tokyo Press, Tokyo, pp 115–132

    Google Scholar 

  • Heistermann M, Ziegler T, van Schaik CP, Launhardt K, Winkler P, Hodges JK (2001) Loss of oestrus, concealed ovulation and paternity confusion in free-ranging Hanuman langurs. Proc R Soc Lond B 268:2445–2451

    Article  CAS  Google Scholar 

  • Heistermann M, Brauch K, Möhle U, Pfefferle D, Dittami J, Hodges K (2008) Female ovarian cycle phase affects the timing of male copulatory and other sexual behaviors in free-ranging Barbary macaques (Macaca sylvanus) of Gibraltar. Am J Primatol 70:44–53

    Article  PubMed  CAS  Google Scholar 

  • Hrdy SB (1979) Infanticide among animals: a review, classification, and examination of the implications for the reproductive strategies of females.. Ethol Sociobiol 1:13–40

    Article  Google Scholar 

  • Hrdy SB, Whitten PL (1987) Patterning of sexual activity. In: Smuts BB, Cheney DL, Seyfarth RM, Wrangham RW, Strusaker TT (eds) Primate societies. University of Chicago Press, Chicago, pp 370–384

    Google Scholar 

  • Huffman MA (1987) Consort intrusion and female mate choice in Japanese macaques (Macaca fuscata). Ethology 75:221–234

    Article  Google Scholar 

  • Ims RA (1988) The potential for sexual selection in males: effect of sex ratio and spatio temporal distribution of receptive females. Evol Ecol 3:338–352

    Article  Google Scholar 

  • Janson CH (1984) Female choice and mating system of the brown capuchin monkey Cebus apella. Z Tierpsychol 65:177–200

    Google Scholar 

  • Johnstone RA (2000) Models of reproductive skew: a review and synthesis. Ethology 106:5–26

    Article  Google Scholar 

  • Kumar A, Kurup GU (1985) Sexual behaviour of the lion-tailed macaque (Macaca silenus). In: Heltne P (ed) The lion-tailed macaque: status and conservation. Alan R Liss, New York, pp 109–130

    Google Scholar 

  • Kümmerli R, Martin RD (2005) Male and female reproductive success in Macaca sylvanus in Gibraltar: no evidence for rank dependence. Int J Primatol 26:1229–1249

    Article  Google Scholar 

  • Küster J, Paul A (1984) Female reproductive characteristics in semi-free ranging Barbary macaques (Macaca sylvanus L. 1758). Folia Primatol 43:69–83

    Article  PubMed  Google Scholar 

  • Küster J, Paul A (1988) Rank relations of juvenile and subadult natal males of Barbary macaques (Macaca sylvanus) at Affenberg Salem. Folia Primatol 51:33–44

    Article  Google Scholar 

  • Küster J, Paul A (1992) Influence of male competition and female mate choice on male mating success in Barbary macaques (Macaca sylvanus). Behaviour 120:192–217

    Article  Google Scholar 

  • Küster J, Paul A, Arnemann J (1994) Kinship, familiarity and mating avoidance in Barbary macaques, Macaca sylvanus. Anim Behav 48:1183–1194

    Article  Google Scholar 

  • Küster J, Paul A, Arnemann J (1995) Age-related and individual differences of reproductive success in male and female Barbary macaques (Macaca sylvanus). Primates 36:461–476

    Article  Google Scholar 

  • Kutsukake N, Nunn CL (2006) Comparative tests of reproductive skew in male primates: the roles of demographic factors and incomplete control. Behav Ecol Sociobiol 60:695–706

    Article  Google Scholar 

  • Lathuillière M, Ménard N, Gautier-Hion A, Crouau-Roy B (2001) Testing the reliability of non-invasive genetic sampling by comparing analyses of blood and fecal samples in Barbary macaques (Macaca sylvanus). Am J Primatol 55:151–158

    Article  PubMed  Google Scholar 

  • Launhardt K, Borries C, Hardt C, Epplen JT, Winkler P (2001) Paternity analysis of alternative male reproductive routes among the langurs (Semnopithecus entellus) of Ramnagar. Anim Behav 61:53–64

    Article  PubMed  Google Scholar 

  • Manson JH (1992) Measuring female mate choice in Cayo Santiago rhesus macaques. Anim Behav 44:405–416

    Article  Google Scholar 

  • Marshall TC, Slate J, Kruuk LEB, Pemberton JM (1998) Statistical confidence for likelihood-based paternity inference in natural populations. Mol Ecol 7:639–655

    Article  PubMed  CAS  Google Scholar 

  • Martin P, Bateson P (1993) Measuring behaviour. Cambridge University Press, Cambridge

    Google Scholar 

  • Marvan R, Stevens JMG, Roeder AD, Mazura I, Bruford MW, de Ruiter JR (2006) Male dominance rank, mating and reproductive success in captive bonobos (Pan paniscus). Folia Primatol 77:364–376

    Article  PubMed  CAS  Google Scholar 

  • Matsubara M, Sprague DS (2004) Mating tactics in response to costs incurred by mating with multiple males in wild female Japanese macaques. Int J Primatol 25:901–917

    Article  Google Scholar 

  • McElligott AG, Hayden TJ (2000) Lifetime mating success, sexual selection and life history of fallow bucks (Dama dama). Behav Ecol Sociobiol 48:203–210

    Article  Google Scholar 

  • Ménard N, Vallet D (1996) Demography and ecology of Barbary macaques (Macaca sylvanus) in two different habitats. In: Fa JE, Lindburg DG (eds) Evolution and ecology of macaque societies. Cambridge University Press, New York, pp 106–131

    Google Scholar 

  • Modolo L, Salzburger W, Martin RD (2005) Phylogeography of Barbary macaques (Macaca sylvanus) and the origin of the Gibraltar colony. Proc Natl Acad Sci USA 102:7392–7397

    Article  PubMed  CAS  Google Scholar 

  • Möhle U, Heistermann M, Dittami J, Reinberg V, Hodges JK (2005) Patterns of anogenital swelling size and their endocrine correlates during ovulatory cycles and early pregnancy in free-ranging Barbary macaques (Macaca sylvanus) of Gibraltar. Am J Primatol 66:351–368

    Article  PubMed  Google Scholar 

  • Moore NP, Kelly PF, Cahill JP, Hayden TJ (1995) Mating strategies and mating success of fallow (Dama dama) bucks in a non-lekking population. Behav Ecol Sociobiol 36:91–100

    Article  Google Scholar 

  • Muller MN, Kahlenberg SM, Emery Thompson M, Wrangham RW (2007) Male coercion and the costs of promiscuous mating for female chimpanzees. Proc Roy Soc Lond B 274:1009–1014

    Article  CAS  Google Scholar 

  • Newcomer SD, Zeh JA, Zeh DW (1999) Genetic benefits enhance the reproductive success of polyandrous females. P Natl Acad Sci USA 94:10236–10241

    Article  Google Scholar 

  • Nikitopoulos E, Heistermann M, de Vries H, van Hooff JARAM, Sterck EHM (2005) A pair choice test to identify female mating pattern relative to ovulation in long-tailed macaques, Macaca fascicularis. Anim Behav 70:1283–1296

    Article  Google Scholar 

  • Nunn CL (1999) The evolution of exaggerated sexual swellings in primates and the graded-signal hypothesis. Anim Behav 58:229–246

    Article  PubMed  Google Scholar 

  • Nunn CL, Altizer SM (2004) Sexual selection, behaviour and sexually transmitted diseases. In: Sexual selection in primates: new and comparative perspectives. Cambridge University Press, New York, pp 117–130

  • Nürnberg P, Sauermann U, Kayser M, Lanfer C, Manz E, Widdig A, Berard J, Bercovitch FB, Kessler M, Schmidtke J, Krawczak M (1998) Paternity assessment in rhesus macaques (Macaca mulatta): multilocus DNA fingerprinting and PCR marker typing. Am J Primatol 44:1–18

    Article  PubMed  Google Scholar 

  • Parker GA (1998) Sperm competition and the evolution of ejaculates: towards a theory base. In: Birkhead TR, Møller AP (eds) Sperm competition and sexual selection. Academic, London, pp 3–54

    Chapter  Google Scholar 

  • Paul A (1989) Determinants of male mating success in a large group of Barbary macaques (Macaca sylvanus) at Affenberg Salem. Primates 30:461–476

    Article  Google Scholar 

  • Paul A (1997) Breeding seasonality affects the association between dominance and reproductive success in non-human male primates. Folia Primatol 68:344–349

    Article  PubMed  CAS  Google Scholar 

  • Paul A, Küster J, Arnemann J (1992) DNA fingerprinting reveals that infant care by male Barbary macaques (Macaca sylvanus) is not parental investment. Folia Primatol 58:93–98

    Article  PubMed  CAS  Google Scholar 

  • Paul A, Küster J, Timme A, Arnemann J (1993) The association between rank, mating effort, and reproductive success in male Barbary Macaques (Macaca sylvanus). Primates 34:491–502

    Article  Google Scholar 

  • Penn DJ, Potts WK (1999) The evolution of mating preferences and major histocompatibility complex genes. Am Nat 153:145–164

    Article  Google Scholar 

  • Pereira ME, Weiss ML (1991) Female mate choice, male migration, and the threat of infanticide in ringtailed lemurs. Behav Ecol Sociobiol 28:141–152

    Article  Google Scholar 

  • Poole JH (1989) Mate guarding, reproductive success and female choice in African elephants. Anim Beh 37:842–849

    Article  Google Scholar 

  • Preston BT, Stevenson IR, Pemberton JM, Wilson K (2001) Dominant rams lose out by sperm depletion. Nature 409:681–682

    Article  PubMed  CAS  Google Scholar 

  • Reeder DM (2003) The potential for cryptic female choice in primates: behavioural, anatomical and physiological considerations. In: Jones CB (ed) Sexual selection and reproductive competition in primates: new perspectives and directions. American Society of Primatologists, Norman, pp 255–303

    Google Scholar 

  • Reeve HK, Emlen ST, Keller L (1998) Reproductive sharing in animal societies: reproductive incentives or incomplete control by dominant breeders? Behav Ecol 9:267–278

    Article  Google Scholar 

  • Say L, Pontier D, Natoli E (2001) Influence of oestrus synchronization on male reproductive success in the domestic cat (Felis catus L.). Proc R Soc Lond B 268:1049–1053

    Article  CAS  Google Scholar 

  • Schwensow N, Eberle M, Sommer S (2008) Compatibility counts: MHC-associated mate choice in a wild promiscuous primate. Proc R Soc B 275:555–564

    Article  PubMed  Google Scholar 

  • Setchell JM (2005) Do female mandrills prefer brightly colored males? Int J Primatol 26:715–735

    Article  Google Scholar 

  • Setchell JM, Charpentier M, Wickings J (2005) Mate guarding and paternity in mandrills: factors influencing alpha male monopoly. Anim Behav 70:1105–1120

    Article  Google Scholar 

  • Shideler SE, Shackleton CHL, Moran FM, Stauffer P, Lohstroh PN, Lasley BL (1993) Enzyme immunoassays for ovarian steroid metabolites in the urine of Macaca fascicularis. J Med Primatol 22:301–312

    PubMed  CAS  Google Scholar 

  • Small MF (1989) Female choice in nonhuman primates. Ybk Phys Anthropol 32:103–127

    Article  Google Scholar 

  • Small MF (1990) Promiscuity in Barbary Macaques (Macaca sylvanus). Am J Primatol 20:267–282

    Article  Google Scholar 

  • Small MF (1994) When Mr. Right is too much effort. New Scientist 143:30–33

    Google Scholar 

  • Smuts BB (1985) Sex and friendships in baboons. Aldine, New York

    Google Scholar 

  • Soltis J (2004) Mating systems. In: Thierry B, Singh M, Kaumanns W (eds) Macaque societies: a model for the study of social organization. Cambridge University Press, Cambridge, pp 135–151

    Google Scholar 

  • Soltis J, Mitsunaga F, Shimizu K, Yanagihara Y, Nozaki M (1999) Female mating strategy in an enclosed group of Japanese macaques. Am J Primatol 47:263–278

    Article  PubMed  CAS  Google Scholar 

  • Soltis J, Thomsen R, Matsubayashi K, Takenaka O (2000) Male infanticide by resident males and female counter-strategies in wild Japanese macaques (Macaca fuscata). Behav Ecol Sociobiol 48:195–202

    Article  Google Scholar 

  • Soltis J, Thomsen R, Takenaka O (2001) The interaction of male and female reproductive strategies and paternity in wild Japanese macaques, Macaca fuscata. Anim Behav 62:485–494

    Article  Google Scholar 

  • Sprague DS (1998) Age, dominance rank, natal status, and tenure among male macaques. Am J Phys Anthropol 105:511–521

    Article  PubMed  CAS  Google Scholar 

  • Steenbeek R (2000) Infanticide by male and female choice in wild Thomas langurs. In: van Schaik CP, Janson C (eds) Infanticide by males and its implications. Cambridge University Press, Cambridge, pp 153–177

    Google Scholar 

  • Stumpf RM, Boesch C (2006) The efficacy of female choice in chimpanzees of the Tai Forest, Cote dÌvoire. Behav Ecol Sociobiol 60:749–765

    Article  Google Scholar 

  • Taberlet P, Griffin S, Goossens B, Questiau S, Manceau V, Escaravage N, Waits LP, Bouvet J (1996) Reliable genotyping of samples with very low DNA quantities using PCR. Nucleic Acids Res 24:3189–3194

    Article  PubMed  CAS  Google Scholar 

  • Taberlet P, Waits LP, Luikart G (1999) Noninvasive genetic sampling: look before you leap. TREE 14:323–327

    PubMed  Google Scholar 

  • Taub DM (1980) Female choice and mating strategies among wild Barbary macaques (Macaca sylvanus L.). In: Lindburg DG (ed) The Macaques: studies in ecology, behaviour and evolution. Van Nostrand Reinhold Co., New York, pp 287–344

    Google Scholar 

  • Tregenza T, Wedell N (2002) Polyandrous females avoid costs of inbreeding. Nature 415:71–73

    Article  PubMed  CAS  Google Scholar 

  • Trivers RL (1972) Parental investment and sexual selection. In: Campbell B (ed) Sexual selection and the decent of man. Aldine, Chicago, pp 136–179

    Google Scholar 

  • van Noordwijk MA, van Schaik CP (2004) Sexual selection and the careers of primate males: paternity concentration, dominance-acquisition tactics and transfer decisions. In: Kappeler PM, van Schaik CP (eds) Sexual selection in primates: new and comparative aspects. Cambridge University, Cambridge, pp 208–229

    Google Scholar 

  • Van Schaik CP, Höstermann M (1994) Predation risk and the number of adult males in a primate group: a comparative test. Behav Ecol Sociobiol 35:261–272

    Article  Google Scholar 

  • Van Schaik CP, Kappeler PM (1997) Infanticide risk and the evolution of male-female association in primates. Proc Roy Soc Lond B 264:1687–1694

    Article  Google Scholar 

  • van Schaik CP, Hodges JK, Nunn CL (2000) Paternity confusion and the ovarian cycles of female primates. In: van Schaik CP, Janson C (eds) Infanticide by males and its implications. Cambridge University Press, Cambridge, pp 361–387

    Google Scholar 

  • van Schaik CP, Pradhan GR, van Noordwijk MA (2004) Mating conflict in primates: infanticide, sexual harassment and female sexuality. In: Kappeler PM, van Schaik CP (eds) Sexual selection in primates: new and comparative aspects. Cambridge University Press, Cambridge, pp 131–150

    Google Scholar 

  • Vigilant L, Hofreiter M, Siedel H, Boesch C (2001) Paternity and relatedness in wild chimpanzee communities. Proc Natl Acad Sci USA 98:12890–12895

    Article  PubMed  CAS  Google Scholar 

  • von Segesser F, Ménard N, Gaci B, Martin RD (1999) Genetic differentiation within and between isolated Algerian subpopulations of Barbary macaques (Macaca sylvanus): evidence from microsatellites. Mol Ecol 8:433–442

    Article  Google Scholar 

  • Waitt C, Little AC, Wolfensohn S, Honess P, Brown AP, Buchanan-Smith HM, Perrett DI (2003) Evidence from rhesus macaques suggests that male coloration plays a role in female primate mate choice. Proc R Soc Lond B 270:144–146

    Article  Google Scholar 

  • Weingrill T, Lycett JE, Henz SP (2000) Consortship and mating success in chacma baboons (Papio cynocephalus ursinus). Ethology 106:1033–1044

    Article  Google Scholar 

  • Weingrill T, Lycett JE, Barrett L, Hill RA, Henzi SP (2003) Male consortship behaviour in chacma baboons: the role of demographic factors and female conceptive probabilities. Behaviour 140:405–427

    Article  Google Scholar 

  • Widdig A, Bercovitch FB, Streich WJ, Sauermann U, Nürnberg P, Krawczak M (2004) A longitudinal analysis of reproductive skew in male rhesus macaques. Proc R Soc Lond B 271:819–826

    Article  Google Scholar 

  • Wilcox AJ, Weinberg CR, Baird DD (1995) Timing of sexual intercourse in relation to ovulation. New Engl J Med 333:1517–1522

    Article  PubMed  CAS  Google Scholar 

  • Wolff JO, Macdonald DW (2004) Promiscuous females protect their offspring. TREE 19:127–134

    PubMed  Google Scholar 

  • Zeh JA, Zeh DW (2001) Reproductive mode and the genetic benefits of polyandry. Anim Behav 61:1051–1063

    Article  Google Scholar 

  • Ziegler T, Hodges JK, Winkler P, Heistermann M (2000) Hormonal correlates of reproductive seasonality in wild female hanuman langurs (Presbytes entellus). Am J Primatol 51:119–134

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

This study was conducted as part of the Gibraltar Barbary macaque project (GBMP). We express our gratitude to Dr. John Cortes of the Gibraltar Ornithological and Natural History Society and Marc Pizarro of the Gibraltar Veterinary Clinic for their support and cooperation. We also thank Brian Gomilla for his help in collection of behavioural data and Nina Stobbe, Dana Pfefferle and Brian Gomilla for their help in collecting faecal samples, Dr. Eckhard Heymann and Dr. Dietmar Zinner are acknowledged for help with the statistics. We are grateful to Dr. N. Menard for her advice on the methodology of microsatellite analysis and suitability of genetic markers and Dr. L. Modolo for providing access to blood samples used for the genetic validation tests. Dana Pfefferle, Andrea Heistermann and Jutta Hagedorn provided support in hormone analyses, and Dr. C. Roos and Dr. M. Eberle provided advice in paternity analysis. We thank the Royal Air Force Gibraltar for permission to enter the study area. The study was conducted completely noninvasively and under the permission of GOHNS, the authority responsible for any research on the Gibraltar Barbary macaques. We adhered to the Guidelines of the Use of Animals in Research, the legal requirements of Gibraltar and the guidelines of the involved institutes. The study was supported by a grant (GRK 289/3-03) from the Deutsche Forschungsgemeinschaft (DFG).

Author information

Authors and Affiliations

  1. Department of Reproductive Biology, German Primate Center, Kellnerweg 4, 37077, Goettingen, Germany

    Katrin Brauch, Keith Hodges, Antje Engelhardt, Kerstin Fuhrmann & Michael Heistermann

  2. Department of Behavioural Biology, University of Muenster, Badestrasse 13, 48149, Muenster, Germany

    Katrin Brauch

  3. Gibraltar Ornithological and Natural History Society, Gibraltar Natural History Field Centre, Upper Rock Nature Reserve, Gibraltar, Germany

    Eric Shaw

Authors
  1. Katrin Brauch
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Keith Hodges
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Antje Engelhardt
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Kerstin Fuhrmann
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Eric Shaw
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Michael Heistermann
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Michael Heistermann.

Additional information

Communicated by A. Widdig

Rights and permissions

Reprints and permissions

About this article

Cite this article

Brauch, K., Hodges, K., Engelhardt, A. et al. Sex-specific reproductive behaviours and paternity in free-ranging Barbary macaques (Macaca sylvanus). Behav Ecol Sociobiol 62, 1453–1466 (2008). https://doi.org/10.1007/s00265-008-0575-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00265-008-0575-7

Keywords

Search

Navigation