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Sneak copulations in long-tailed macaques (Macaca fascicularis): no evidence for tactical deception

Abstract

Sexual competition is highly prevalent within multi-male multi-female primate groups and may lead to copulations in absence of potentially interfering bystanders. Such avoidance of bystanders may result from tactical deception or from simpler mechanisms such as taking advantage of encountered situations without bystanders, operant conditioning or a peripheral positioning of non-alpha males. We investigated which individuals are avoided as bystanders, how individuals react to the presence of bystanders and whether copulation partners separate themselves from the group in a tactical way. Our observations of a group of 15 female and seven male long-tailed macaques housed in three interconnected, but visually separated compartments revealed that both males and females can interrupt sexual behaviour and that bystanders of both sexes were avoided during copulations (n = 256). The strength of the effect of bystanders tended to decrease with the dominance rank of male bystanders, but did not depend on the dominance rank of female bystanders. The audience effects of non-alpha individuals did not depend on the strong audience effect of the alpha male in combination with proximity with the alpha male. The effects that we found for separate bystanders suggest that sexual competition concerns rank dependent male–male competition and rank independent female–female competition. Additionally, both male and female copulation partners paid attention to the presence of bystanders and conducted fewer copulation solicitations in their presence. The timing of a male and female’s separation from the group suggests that exploitation of the peripheral position of non-alpha males, and not tactical deception, may cause these audience effects.

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References

  1. Alfaro JWL (2005) Male mating strategies and reproductive constraints in a group of wild tufted capuchin monkeys (Cebus apella nigritus). Am J Primatol 67:313–328

    PubMed  Article  Google Scholar 

  2. Altmann SA (1962) A field study of the sociobiology of rhesus monkeys, Macaca mulatta. Ann NY Acad Sci 102:338–435

    PubMed  Article  CAS  Google Scholar 

  3. Angst W (1974) Das Ausdrucksverhalten des Javaneraffen Macaca fascicularis Raffles 1821. Parey, Berlin

    Google Scholar 

  4. Berard JD, Nurnberg P, Epplen JT, Schmidtke J (1994) Alternative reproductive tactics and reproductive success in male rhesus macaques. Behaviour 129:177–201

    Article  Google Scholar 

  5. Bruce KE, Estep DQ (1992) Interruption of and harassment during copulation by stumptail macaques, Macaca arctoides. Anim Behav 44:1029–1044

    Article  Google Scholar 

  6. Buchan JC, Alberts SC, Silk JB, Altmann J (2003) True paternal care in a multi-male primate society. Nature 425:179–181

    PubMed  Article  CAS  Google Scholar 

  7. Byrne RW, Whiten A (1990) Tactical deception in primates: the 1990 database. Primate Rep 27:1–101

    Google Scholar 

  8. Byrne RW, Whiten A (1992) Cognitive evolution in primates—evidence from tactical deception. Man 27:609–627

    Article  Google Scholar 

  9. Chapais B (1983) Reproductive activity in relation to male dominance and the likelyhood of ovulation in rhesus monkeys. Behav Ecol Sociobiol 12:215–228

    Article  Google Scholar 

  10. Coltman DW, Bowen WD, Wright JM (1999) A multivariate analysis of phenotype and paternity in male harbor seals, Phoca vitulina, at Sable Island, Nova Scotia. Behav Ecol 10:169–177

    Article  Google Scholar 

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

    Article  Google Scholar 

  12. Davies NB (2000) Multi-male breeding groups in birds: ecological causes and social conflicts. In: Kappeler PM (ed) Primate males: causes and consequences of variation in group composition. Cambridge University Press, Cambridge, pp 11–20

    Google Scholar 

  13. de Bruyn PJN, Tosh CA, Bester MN, Cameron EZ, McIntyre T, Wilkinson IS (2011) Sex at sea: alternative mating system in an extremely polygynous mammal. Anim Behav 82:445–451

    Article  Google Scholar 

  14. de Ruiter JR, van Hooff JARAM (1993) Male-dominance rank and reproductive success in primate groups. Primates 34:513–523

    Article  Google Scholar 

  15. de Ruiter JR, Scheffrahn W, Trommelen GJM, Uiterlinden AG, Martin RD, van Hooff JARAM (1992) Male social rank and reproductive success in wild long-tailed macaques. In: Martin RD, Dixson AF, Wickings EJ (eds) Paternity in primates: genetic tests and theories. Karger, Basel, pp 175–191

    Google Scholar 

  16. de Vries H (1995) An improved test of linearity in dominance hierarchies containing unknown or tied relationships. Anim Behav 50:1375–1389

    Article  Google Scholar 

  17. de Vries H (1998) Finding a dominance order most consistent with a linear hierarchy: a new procedure and review. Anim Behav 55:827–843

    PubMed  Article  Google Scholar 

  18. de Vries H, Netto WJ, Hanegraaf PLH (1993) Matman—a program for the analysis of sociometric matrices and behavioral transition matrices. Behaviour 125:157–175

    Article  Google Scholar 

  19. Development Core Team R (2009) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  20. Dixson AF (1998) Primate sexuality: comparative studies of the prosimians, monkeys, apes, and human beings. Oxford University Press, Oxford

    Google Scholar 

  21. Dixson AF, Anderson MJ (2002) Sexual selection, seminal coagulation and copulatory plug formation in primates. Folia Primatol 73:63–69

    PubMed  Article  Google Scholar 

  22. Engelhardt A, Pfeifer AB, Heistermann M, Niemitz C, Van Hooff J, Hodges JK (2004) Assessment of female reproductive status by male longtailed macaques, Macaca fascicularis, under natural conditions. Anim Behav 67:915–924

    Article  Google Scholar 

  23. Engelhardt A, Hodges JK, Heistermann M (2007) Post-conception mating in wild long-tailed macaques (Macaca fascicularis): characterization, endocrine correlates and functional significance. Horm Behav 51:3–10

    PubMed  Article  Google Scholar 

  24. Engh AL, Funk SM, Van Horn RC, Scribner KT, Bruford MW, Libants S, Szykman M, Smale L, Holekamp KE (2002) Reproductive skew among males in a female-dominated mammalian society. Behav Ecol 13:193–200

    Article  Google Scholar 

  25. Garcia C, Shimizu K, Huffman M (2009) Relationship between sexual interactions and the timing of the fertile phase in captive female Japanese macaques (Macaca fuscata). Am J Primatol 71:868–879

    PubMed  Article  Google Scholar 

  26. Gouzoules H (1974) Harrassment of sexual behavior in the stumptailed macaque (Macaca arctoides). Folia Primatol 22:208–217

    PubMed  Article  CAS  Google Scholar 

  27. Gygax L (1995) Hiding behaviour of long-tailed macaques (Macaca fascicularis): I. Theoretical background and data on mating. Ethology 101:10–24

    Article  Google Scholar 

  28. Hayakawa S (2007) Female defensibility in small troops of Japanese macaques vis-à-vis nontroop males and copulation on the periphery of the troop. Int J Primatol 28:73–96

    Article  Google Scholar 

  29. Hill RA, Dunbar RIM (1998) An evaluation of the roles of predation rate and predation risk as selective pressures on primate grouping behaviour. Behaviour 135:411–430

    Article  Google Scholar 

  30. Hochberg Y (1988) A sharper Bonferroni procedure for multiple tests of significance. Biometrika 75:800–802

    Article  Google Scholar 

  31. Hogg JT (1987) Intrasexual competition and mate choice in Rocky-Mountain bighorn sheep. Ethology 75:119–144

    Article  Google Scholar 

  32. Honjo S, Cho F, Fujinara T, Yoshioka Y, Masuko K, Kurihara K, Yabe M, Noguchi Y (1978) Breeding of cynomolgous monkeys through successive generations by indoor cage system. Jpn J Med Sci Biol 31:301–310

    PubMed  CAS  Google Scholar 

  33. Huang B, Wey TW, Blumstein DT (2011) Correlates and consequences of dominance in a social rodent. Ethology 117:573–585

    Article  Google Scholar 

  34. Janson CH (1990) Social correlates of individual spatial choice in foraging groups of brown capuchin monkeys, Cebus apella. Anim Behav 40:910–921

    Article  Google Scholar 

  35. Janson CH, van Schaik CP (2000) The behavioral ecology of infanticide by males. In: van Schaik CP, Janson CH (eds) Infanticide by males and its implications. Cambridge University Press, Cambridge, pp 469–494

    Chapter  Google Scholar 

  36. Kavanagh M, Laursen E (1984) Breeding seasonality among long-tailed macaques, Macaca fascicularis, in Peninsular Malaysia. Int J Primatol 5:17–29

    Article  Google Scholar 

  37. Kummer H (1968) Social organization of Hamadryas baboons: a field study. University of Chicago Press, Chicago

    Google Scholar 

  38. Kummer H, Anzenberer G, Hemelrijk CK (1996) Hiding and perspective taking in long-tailed macaques (Macaca fascicularis). J Comp Psychol 110:97–102

    PubMed  Article  CAS  Google Scholar 

  39. Lambert DM, Millar CD, Jack K, Anderson S, Craig JL (1994) Single-locus and multilocus DNA-fingerprinting of communally breeding pukeko—do copulations or dominance ensure reproductive success. Proc Natl Acad Sci U S A 91:9641–9645

    PubMed  Article  CAS  Google Scholar 

  40. Manson JH (1996) Male dominance and mount series duration in Cayo Santiago rhesus macaques. Anim Behav 51:1219–1231

    Article  Google Scholar 

  41. Massen JJM, Overduin-de Vries AM, de Vos-Rouweler AJM, Spruijt BM, Doxiadis GGM, Sterck EHM (2012) Male mating tactics in captive rhesus macaques, Macaca mulatta: the influence of dominance, markets and relationship quality. Int J Primatol 33:73–92

    PubMed  Article  Google Scholar 

  42. Niemeyer CL, Anderson JR (1983) Primate harassment of matings. Ethol Sociobiol 4:205–220

    Article  Google Scholar 

  43. Niemeyer CL, Chamove AS (1983) Motivation of harassment of matings in stumptailed macaques. Behaviour 87:298–323

    Article  Google Scholar 

  44. Nikitopoulos E, Heistermann M, De Vries H, Van Hooff J, Sterck EHM (2005) A pair choice test to identify female mating pattern relative to ovulation in longtailed macaques, Macaca fascicularis. Anim Behav 70:1283–1296

    Article  Google Scholar 

  45. Noldus LPJJ (1991) The Observer: a software system for collection and analysis of observational data. Behav Res Meth Instrum Comput 23:415–429

    Article  Google Scholar 

  46. Overduin-de Vries AM, Massen JJM, Spruijt BM, Sterck EHM (2012) Sneaky monkeys: an audience effect of male rhesus macaques (Macaca mulatta) on sexual behavior. Am J Primatol 74:217–228

    Article  Google Scholar 

  47. Paul A, Kuester 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 

  48. Ruiz de Elvira M, Herndon JG (1986) Disruption of sexual behaviour by high ranking rhesus monkeys (Macaca mulatta). Behaviour 96:227–239

    Article  Google Scholar 

  49. Soltis J (2002) Do primate females gain nonprocreative benefits by mating with multiple males? Theoretical and empirical considerations. Evol Anthropol 11:187–197

    Article  Google Scholar 

  50. 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 

  51. Stephenson GR (1975) Social structure of mating activity in Japanese macaques. In: Kondo S, Kawai M, Ehara A, Kawamura S (eds) Proceedings of the Fifth Congress of the International Primatological Society. Japan Science Press, Tokyo, pp 63–115

    Google Scholar 

  52. van Schaik CP, van Noordwijk MA (1985) Evolutionary effect of the absence of felids on the social organization of the macaques on the island of Simeulue (Macaca fascicularis, Miller 1903). Folia Primatol 44:138–147

    Article  Google Scholar 

  53. Vernes MK, Louwerse AL (2010) BPRC's enrichment manual for macaques and marmosets. Biomedical Primate Research Centre, Rijswijk

    Google Scholar 

  54. Willisch CS, Neuhaus P (2009) Alternative mating tactics and their impact on survival in adult male alpine ibex (Capra ibex ibex). J Mammal 90:1421–1430

    Article  Google Scholar 

  55. Willisch CS, Biebach I, Koller U, Bucher T, Marreros N, Ryser-Degiorgis MP, Keller LF, Neuhaus P (2012) Male reproductive pattern in a polygynous ungulate with a slow life-history: the role of age, social status and alternative mating tactics. Evol Ecol 26:187–206

    Article  Google Scholar 

  56. Wilson ME (1981) Social dominance and female reproductive behaviour in rhesus monkeys (Macaca mulatta). Anim Behav 29:472–482

    Article  Google Scholar 

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Acknowledgments

We would like to thank Nick Stolk for his contribution to the data collection, three anonymous reviewers for the thoughtful comments and the animal caretakers for their care for the monkeys. This research was funded by the Biomedical Primate Research Centre, Rijswijk, the Netherlands.

Ethical standards

This research complied with protocols approved by the Animal Ethical Committee of the Biomedical Primate Research Centre and with the legal requirements of the Netherlands.

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Correspondence to A. M. Overduin-de Vries.

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Communicated by E. Huchard

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Overduin-de Vries, A.M., Olesen, C.U., de Vries, H. et al. Sneak copulations in long-tailed macaques (Macaca fascicularis): no evidence for tactical deception. Behav Ecol Sociobiol 67, 101–111 (2013). https://doi.org/10.1007/s00265-012-1430-4

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Keywords

  • Tactical deception
  • Audience effect
  • Mating tactics
  • Sexual competition
  • Primates
  • Monopolization
  • Macaques