International Journal of Primatology

, Volume 32, Issue 3, pp 708–720 | Cite as

Interactions Between Third Parties and Consortship Partners in Tonkean Macaques (Macaca tonkeana)

  • Arianna De MarcoEmail author
  • Roberto Cozzolino
  • Francesco Dessì-Fulgheri
  • Bernard Thierry


Sexual competition is potentially disruptive for the cohesion of social groups because stress and conflicts can extend to other group members. The displays and interactions of sexual partners are liable to influence the behavior of group-mates, which may need to observe them to anticipate possible consequences. We studied 2 captive groups of Tonkean macaques (Macaca tonkeana) to test whether group-mates pay more attention to consort partners, modify their activities and social interactions, and exhibit signs of stress during periods of sexual consortships. We found that group-mates approached the top-ranking male more frequently and were more frequently oriented toward the consort pair at the time of consortship than at other times. Group-mates spent less time sleeping, and devoted less time to manipulating the environment and more time to monitoring during consortship. This indicates that consortships may incur costs in individuals not involved in sexual competition. However, Tonkean macaques did not exhibit any signs of increased stress during consortship periods, as their rates of scratching and yawning did not differ between consortship and nonconsortship periods. This study shows that not only direct competitors but also other individuals monitor the behavior of sexual partners. It is likely that group-mates obtain information this way about ongoing action, and take decisions accordingly.


Macaca tonkeana Polyadic interaction Sexual consortship Social tension Stress 



We thank the managers and keepers of the Orangerie Zoo of Strasbourg and the Parco Faunistico di Piano dell’Abatino of Rieti for valuable assistance, and V. Pallage for statistical advice. We also thank the editor and 2 anonymous reviewers for constructive comments.


  1. Alberts, S. C., Altmann, J., & Wilson, M. L. (1996). Mate guarding constrains foraging activity of male baboons. Animal Behaviour, 51, 1269–1277.CrossRefGoogle Scholar
  2. Altmann, J. (1974). Observational study of behavior: sampling methods. Behaviour, 49, 227–265.PubMedCrossRefGoogle Scholar
  3. Aujard, F., Heistermann, M., Thierry, B., & Hodges, J. K. (1998). Functional significance of behavioral, morphological and endocrine correlates across the ovarian cycle in semi-free ranging female Tonkean macaques. American Journal of Primatology, 46, 285–309.PubMedCrossRefGoogle Scholar
  4. Bercovitch, F. B. (1983). Time budgets and consortships in olive baboons (Papio anubis). Folia Primatologica, 41, 180–190.CrossRefGoogle Scholar
  5. Bergman, T. J., Beehner, J. C., Cheney, D. L., & Seyfarth, R. M. (2003). Hierarchical classification by rank and kinship in baboons. Science, 302, 1234–1236.PubMedCrossRefGoogle Scholar
  6. Bergman, T. J., Beehner, J. C., Cheney, D. L., Seyfarth, R. M., & Whitten, P. L. (2006). Interactions in male baboons: the importance of both males’ testosterone. Behavioral Ecology and Sociobiology, 59, 480–489.CrossRefGoogle Scholar
  7. Bovet, D., & Washburn, D. A. (2003). Rhesus macaques categorise conspecifics according to their dominance relations. Journal of Comparative Psychology, 117, 400–405.PubMedCrossRefGoogle Scholar
  8. Cerda-Molina, A. L., Hernández-López, L., Rojas-Maya, S., Murcia-Mejia, R., & Mondragón-Ceballos, R. (2006). Male-induced sociosexual behavior by vaginal secretions in Macaca arctoides. International Journal of Primatology, 27, 791–807.CrossRefGoogle Scholar
  9. Cheney, D. L., & Seyfarth, R. M. (Eds.). (1990). How monkeys see the world. Chicago: University of Chicago Press.Google Scholar
  10. Clutton-Brock, T. H., & Parker, G. A. (1995). Sexual coercion in animal societies. Animal Behaviour, 49, 1345–1365.CrossRefGoogle Scholar
  11. Crockford, C., Witting, R. M., Seyfarth, R. M., & Cheney, D. L. (2007). Baboons eavesdrop to deduce mating opportunities. Animal Behaviour, 73, 885–890.CrossRefGoogle Scholar
  12. Dasser, V. (1988). A social concept in Java monkeys. Animal Behaviour, 36, 225–230.CrossRefGoogle Scholar
  13. De Marco, A., Cozzolino, R., Dessì-Fulgheri, F., & Thierry, B. (2010). Conflicts induce affiliative interactions among bystanders in a tolerant species of macaque (Macaca tonkeana). Animal Behaviour, 80, 197–203.CrossRefGoogle Scholar
  14. Demaria, C., & Thierry, B. (2001). A comparative study of reconciliation in rhesus and Tonkean macaques. Behaviour, 138, 397–410.CrossRefGoogle Scholar
  15. Deschner, T., Heistermann, M., Hodges, K., & Boesch, C. (2003). Timing and probability of ovulation in relation to sex skin swelling in wild West African chimpanzees, Pan troglodytes verus. Animal Behaviour, 66, 551–560.CrossRefGoogle Scholar
  16. Dixson, A. F. (1998). Primate sexuality. Oxford: Oxford University Press.Google Scholar
  17. Domb, L. G., & Pagel, M. (2001). Sexual swellings advertise female quality in wild baboons. Nature, 410, 204–206.PubMedCrossRefGoogle Scholar
  18. Drapier, M., Ducoing, A. M., & Thierry, B. (1999). An experimental study of collective performance at a foraging task in Tonkean macaques. Behaviour, 136, 99–117.Google Scholar
  19. Drapier, M., Chauvin, C., & Thierry, B. (2002). Tonkean macaques find food sources from cues conveyed by group-mates. Animal Cognition, 5, 159–165.PubMedCrossRefGoogle Scholar
  20. Emery, M. A., & Whitten, P. L. (2003). Size of sexual swellings reflects ovarian function in chimpanzees (Pan troglodytes). Behavioral Ecology and Sociobiology, 54, 340–351.CrossRefGoogle Scholar
  21. Hausfater, G. (1975). Dominance and reproduction in baboons. Basel: Karger.Google Scholar
  22. Hdry, S. B., & Whitten, P. L. (1987). Patterning of sexual activity. In B. B. Smuts, D. L. Cheney, R. M. Seyfarth, R. W. Wrangham, & T. T. Struhsaker (Eds.), Primate societies (pp. 370–384). Chicago: University of Chicago Press.Google Scholar
  23. Higham, J. P., MacLarnon, A. M., Ross, C., Heistermann, M., & Semple, S. (2008). Baboon sexual swellings: Information content of size and color. Hormones and Behavior, 53, 452–462.PubMedCrossRefGoogle Scholar
  24. Higham, J. P., Semple, S., MacLarnon, A. M., Heistermann, M., & Ross, C. (2009). Female reproductive signaling, and male mating behavior, in the olive baboon. Hormones and Behavior, 55, 60–67.PubMedCrossRefGoogle Scholar
  25. Huffman, M. A. (1987). Consort intrusion and female mate choice in Japanese macaques (Macaca fuscata). Ethology, 75, 221–234.CrossRefGoogle Scholar
  26. Judge, P. G., & Mullen, S. (2005). Quadratic postconflict affiliation among bystanders in a hamadryas baboon group. Animal Behaviour, 69, 1345–1355.CrossRefGoogle Scholar
  27. Koyama, N. F., & Dunbar, R. I. M. (1996). Anticipation of conflict chimpanzees. Primates, 76, 79–86.CrossRefGoogle Scholar
  28. Maestripieri, D., & Roney, J. R. (2005). Primate copulation calls and postcopulatory female choice. Behavioral Ecology, 16, 106–113.CrossRefGoogle Scholar
  29. Manson, J. H. (1994). Male aggression: a cost of female mate choice in Cayo Santiago rhesus macaques. Animal Behaviour, 48, 473–475.CrossRefGoogle Scholar
  30. Masataka, N., & Thierry, B. (1993). Vocal communication of Tonkean macaques in confined environments. Primates, 34, 169–180.CrossRefGoogle Scholar
  31. Matsubara, M. (2003). Costs of mate guarding and opportunistic mating among wild male Japanese macaques. International Journal of Primatology, 24, 1057–1075.CrossRefGoogle Scholar
  32. Mayagoitia, L., Santillan-Doherty, A. M., Lopez-Vergara, L., & Mondragon-Ceballos, R. (1993). Ethology. Ecology and Evolution, 5, 435–446.Google Scholar
  33. McGregor, P. K. (Ed.). (2005). Animal communication networks. Cambridge: Cambridge University Press.Google Scholar
  34. Michael, R. P., & Keverne, E. (1968). Pheromones in the communication of sexual status in primates. Nature, 218, 746–749.PubMedCrossRefGoogle Scholar
  35. Nunn, C. L. (1999). The evolution of exaggerated sexual swellings in primates and the graded signal hypothesis. Animal Behaviour, 58, 229–246.PubMedCrossRefGoogle Scholar
  36. Pagel, M. (1994). The evolution of conspicuous advertisement in Old World monkeys. Animal Behaviour, 47, 1333–1341.CrossRefGoogle Scholar
  37. Petit, O., & Thierry, B. (1994). Aggressive and peaceful interventions in conflicts in Tonkean macaques. Animal Behaviour, 48, 1427–1436.CrossRefGoogle Scholar
  38. Pfefferle, D., Heistermann, M., Hodges, J. K., & Fischer, J. (2008). Male Barbary macaques eavesdrop on mating outcome: a playback study. Animal Behaviour, 75, 1885–1891.CrossRefGoogle Scholar
  39. Plavcan, J. M. (2004). Sexual selection, measures of sexual selection, and sexual dimorphism in primates. In P. M. Kappeler & C. P. van Schaik (Eds.), Sexual selection in primates (pp. 230–252). Cambridge: Cambridge University Press.CrossRefGoogle Scholar
  40. Polizzi di Sorrentino, E., Schino, G., Visalberghi, E., & Aureli, F. (2010). What time is it? Coping with expected feeding time in capuchin monkeys. Animal Behaviour, 80, 117–123.CrossRefGoogle Scholar
  41. Pradhan, G. R., Engelhardt, A., & van Schaik, C. P. (2006). The evolution of female copulation calls in primates: a review and a new model. Behavioral Ecology and Sociobiology, 59, 333–343.CrossRefGoogle Scholar
  42. Quinn, G. P., & Keough, M. J. (2002). Experimental design and data analysis for biologists. Cambridge: Cambridge University Press.Google Scholar
  43. Silk, J. B. (1999). Male bonnet macaques use information about third party rank relationships to recruit allies. Animal Behaviour, 58, 45–51.PubMedCrossRefGoogle Scholar
  44. Smuts, B. B., & Smuts, R. W. (1993). Male aggression and sexual coercion of females in nonhuman primates and other mammals: evidence and theoretical implications. Advances in the Study of Behavior, 22, 1–63.CrossRefGoogle Scholar
  45. Snowdon, C. T. (2004). Sexual selection and communication. In P. M. Kappeler & C. P. van Schaik (Eds.), Sexual selection in primates (pp. 57–70). Cambridge: Cambridge University Press.CrossRefGoogle Scholar
  46. Thierry, B. (1985). Patterns of agonistic interactions in three species of macaque (Macaca mulatta, M. fascicularis, M. tonkeana). Aggressive Behavior, 11, 223–233.CrossRefGoogle Scholar
  47. Thierry, B. (1986). Affiliative interference in mounts in a group of Tonkean macaques (Macaca tonkeana). American Journal of Primatology, 14, 89–97.CrossRefGoogle Scholar
  48. Thierry, B. (2010). The macaques: a double-layered social organization. In C. J. Campbell, A. Fuentes, K. C. MacKinnon, S. K. Bearder, & R. M. Stumpf (Eds.), Primates in perspective (2nd ed., pp. 229–241). Oxford: Oxford University Press.Google Scholar
  49. Thierry, B., Anderson, J. R., Demaria, C., Desportes, C., & Petit, O. (1994). Tonkean macaque behaviour from the perspective of the evolution of Sulawesi macaques. In J. J. Roeder, B. Thierry, J. R. Anderson, & N. Herrenschmidt (Eds.), Current primatology ((pp, Vol. 2, pp. 103–117). Strasbourg: Université Louis Pasteur.Google Scholar
  50. Thierry, B., Heistermann, M., Aujard, F., & Hodges, J. K. (1996). Long-term data on basic reproductive parameters and evaluation of endocrine, morphological and behavioral measures for monitoring reproductive status in a group of semi-free ranging Tonkean macaques (Macaca tonkeana). American Journal of Primatology, 39, 47–62.CrossRefGoogle Scholar
  51. Tomasello, M., Call, J., & Hare, B. (1998). Five primate species follow the visual gaze of conspecifics. Animal Behaviour, 55, 1063–1069.PubMedCrossRefGoogle Scholar
  52. Valone, T. J. (2007). From eavesdropping on performance to copying the behavior of others, a review of public information use. Behavioral Ecology and Sociobiology, 62, 1–14.CrossRefGoogle Scholar
  53. van Schaik, C. P., Pradhan, G. R., & van Noordwijk, M. A. (2004). Mating conflict in primates: Infanticide, sexual harassment and female sexuality. In P. M. Kappeler & C. P. van Schaik (Eds.), Sexual selection in primates (pp. 131–150). Cambridge: Cambridge University Press.CrossRefGoogle Scholar
  54. Wood, J. N., Glynn, D. D., Phillips, B. C., & Hauser, M. D. (2007). The perception of rational, goal-directed action in nonhuman primates. Science, 317, 1402–1405.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2011

Authors and Affiliations

  • Arianna De Marco
    • 1
    • 2
    • 3
    Email author
  • Roberto Cozzolino
    • 4
  • Francesco Dessì-Fulgheri
    • 3
  • Bernard Thierry
    • 2
    • 5
  1. 1.Parco Faunistico di Piano dell’AbatinoPoggio San LorenzoItaly
  2. 2.Département Ecologie, Physiologie et EthologieCentre National de la Recherche ScientifiqueStrasbourgFrance
  3. 3.Dipartimento di Biologia Evoluzionistica Leo PardiUniversità degli Studi di FirenzeFlorenceItaly
  4. 4.EthoikosRadicondoliItaly
  5. 5.Institut Pluridisciplinaire Hubert CurienUniversité de StrasbourgStrasbourgFrance

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