Animal Cognition

, Volume 20, Issue 2, pp 221–232 | Cite as

Triadic awareness predicts partner choice in male–infant–male interactions in Barbary macaques

  • Barbora KubenovaEmail author
  • Martina Konecna
  • Bonaventura Majolo
  • Petr Smilauer
  • Julia Ostner
  • Oliver Schülke
Original Paper


Social knowledge beyond one’s direct relationships is a key in successfully manoeuvring the social world. Individuals gather information on the quality of social relationships between their group companions, which has been termed triadic awareness. Evidence of the use of triadic awareness in natural contexts is limited mainly to conflict management. Here we investigated triadic awareness in wild Barbary macaques (Macaca sylvanus) in the context of bridging interactions defined as male–infant–male interactions whereby a male (initiator, holder) presents an infant to another male (receiver, non-holder) in order to initiate an affiliative interaction with that male. Analyses based on 1263 h of focal observations on ten infants of one wild social group in Morocco supported the hypothesis that males use their knowledge of the relationship between infants and other adult males when choosing a male as a partner for bridging interactions. Specifically, (i) the number of bridging interactions among holder–infant–receiver triads was positively affected by the strength of the infant–receiver relationship and (ii) when two males were available as bridging partners, a male was more likely to be chosen as the receiver the stronger his social relationship with the infant relative to the other available male. This demonstrates that non-human primates establish triadic awareness of temporary infant–male relationships and use it in a naturally occurring affiliative context. Our results contribute to the discussion about the mechanism underlying the acquisition of triadic awareness and the benefits of its usage, and lend support to hypotheses linking social complexity to the evolution of complex cognition.


Triadic awareness Social cognition Infant handling Bridging Male–infant–male interactions Barbary macaques 



This study was supported by grant 009/2014/P and 04-151/2016/P provided by the Grant Agency of the University of South Bohemia, Christian-Vogel Fond for Field Research of the Gesellschaft für Primatologie and by the scholarship of the German Academic Exchange Service DAAD. We are grateful to the Haut Commissariat aux Eaux et Forêts et à la Lutte Contre la Désertification of Morocco for research permission and professor Mohamed Mouna (Institute Scientifique, Rabat, Morocco) and professor Mohamed Quarro (Ecole Nationale Forestière d’Ingénieurs, Salé, Morocco) for their invaluable support and cooperation during the field work. We are thankful for the support and comments of all our collaborators and colleagues that contributed to the realization of the study and preparation of the manuscript. We particularly appreciate advices and support from James Waterman, Josephine Kalbitz, Adeelia Goffe, Andreas Berghänel, Christopher Young, Christina Haunhorst and Stanislav Lhota. Special thank goes to Els van Lavieren, the director of the Moroccan Primate Conservation Foundation, for her help and effort related to the protection of wild populations of Barbary macaques. We also want to thank Dr. Sarah Boysen and two anonymous referees for their thoughtful and insightful comments on the manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

Our study was observational and non-invasive. All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. All procedures performed in this study were in accordance with the standards of the International Primate Society for the use of non-human primates in research.

Supplementary material

10071_2016_1041_MOESM1_ESM.docx (22 kb)
Supplementary material 1 (DOCX 22 kb)
10071_2016_1041_MOESM2_ESM.tiff (687 kb)
Fig. S1 Distribution of the strength of the relationship (measured as composite sociality index, CSI) between infant–male dyads (TIFF 686 kb)


  1. Altmann J (1974) Observational study of behavior: sampling methods. Behaviour 49:227–266CrossRefPubMedGoogle Scholar
  2. Aureli F, Cozzolino R, Cordischi C, Scucchi S (1992) Kin-oriented redirection among Japanese macaques: an expression of a revenge system? Anim Behav 44:283–291CrossRefGoogle Scholar
  3. Bachmann C, Kummer H (1980) Male assessment of female choice in hamadryas baboons. Behav Ecol Sociobiol 6:315–321. doi: 10.1007/BF00292774 CrossRefGoogle Scholar
  4. Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw. doi: 10.18637/jss.v067.i01 Google Scholar
  5. Berghänel A, Ostner J, Schröder U, Schülke O (2011) Social bonds predict future cooperation in male Barbary macaques, Macaca sylvanus. Anim Behav 81:1109–1116CrossRefGoogle Scholar
  6. Bernstein IS, Cooper MA (1998) Ambiguities in the behavior of Assamese macaques. Am J Primatol 45:170–171Google Scholar
  7. Bissonnette A, De Vries H, van Schaik CP (2009) Coalitions in male Barbary macaques, Macaca sylvanus: strength, success and rules of thumb. Anim Behav 78:329–335. doi: 10.1016/j.anbehav.2009.05.010 CrossRefGoogle Scholar
  8. Bowerman BL, O’Connell RT (1990) Linear statistical models: an applied approach. PWS-Kent Publishing Company, BostonGoogle Scholar
  9. Busse CD, Gordon TP (1984) Infant carrying by adult male mangabeys (Cercocebus atys). Am J Primatol 6:133–141CrossRefGoogle Scholar
  10. Busse C, Hamilton WJ (1981) Infant carrying by male chacma baboons. Science 212:1281–1283. doi: 10.1126/science.212.4500.1281 CrossRefPubMedGoogle Scholar
  11. Call J, Aureli F, De Waal FBM (2002) Postconflict third-party affiliation in stumptailed macaques. Anim Behav 63:209–216CrossRefGoogle Scholar
  12. Chalmers NR (1968) The social behaviour of free living mangabeys in Uganda. Folia Primatol 8:263–281CrossRefPubMedGoogle Scholar
  13. Cheney DL, Seyfarth RM (1980) Vocal recognition in free-ranging vervet monkeys. Anim Behav 28:362–367CrossRefGoogle Scholar
  14. Cheney DL, Seyfarth RM (1989) Redirected aggression and reconciliation among vervet monkeys, Cercopithecus aethiops. Behaviour 110:258–275CrossRefGoogle Scholar
  15. Cheney DL, Seyfarth RM (1999) Recognition of other individuals’ social relationships by female baboons. Anim Behav 58:67–75CrossRefPubMedGoogle Scholar
  16. Cheney DL, Seyfarth RM, Smuts B (1986) Social relationships and social cognition in nonhuman primates. Science 234:1361–1366CrossRefPubMedGoogle Scholar
  17. Cheney DL, Seyfarth RM, Silk JB (1995) The responses of female baboons (Papio cynocephalus ursinus) to anomalous social interactions: evidence for causal reasoning? J Comp Psychol 109:134CrossRefPubMedGoogle Scholar
  18. Clutton-Brock T (2002) Breeding together: kin selection and mutualism in cooperative vertebrates. Science 296:69–72CrossRefPubMedGoogle Scholar
  19. Cohen S, Wills TA (1985) Stress, social support, and the buffering hypothesis. Psychol Bull 98:310CrossRefPubMedGoogle Scholar
  20. Collins DA (1986) Interactions between adult male and infant yellow baboons (Papio c. cynocephalus) in Tanzania. Anim Behav 34:430–443CrossRefGoogle Scholar
  21. Connor RC (2007) Dolphin social intelligence: complex alliance relationships in bottlenose dolphins and a consideration of selective environments for extreme brain size evolution in mammals. Philos Trans R Soc Lond B Biol Sci 362:587–602CrossRefPubMedPubMedCentralGoogle Scholar
  22. Dasser V (1988) A social concept in Java monkeys. Anim Behav 36:225–230CrossRefGoogle Scholar
  23. De Vries H, Netto WJ, Hanegraaf PL (1993) Matman: a program for the analysis of sociometric matrices and behavioural transition matrices. Behaviour 125:157–175CrossRefGoogle Scholar
  24. De Waal FBM (1986) The integration of dominance and social bonding in primates. Q Rev Biol 61:459–479CrossRefPubMedGoogle Scholar
  25. De Waal FBM (1991) Complementary methods and convergent evidence in the study of primate social cognition 1). Behaviour 118:297–320. doi: 10.1163/156853991X00337 CrossRefGoogle Scholar
  26. De Waal FBM (2007) Chimpanzee politics: power and sex among apes. JHU Press, BaltimoreGoogle Scholar
  27. De Waal FBM, van Hooff JA, Netto WJ (1976) An ethological analysis of types of agonistic interaction in a captive group of Java-monkeys (Macaca fascicularis). Primates 17:257–290CrossRefGoogle Scholar
  28. Deag JM (1980) Interactions between males and unweaned Barbary macaques: testing the agonistic buffering hypothesis. Behaviour 75(1):54–81CrossRefGoogle Scholar
  29. Deag JM, Crook JH (1971) Social behaviour and “agonistic buffering” in the wild Barbary macaque Macaca sylvana L. Folia Primatol 15:183–200CrossRefPubMedGoogle Scholar
  30. Dunbar RIM (1984) Infant-use by male gelada in agonistic contexts: agonistic buffering, progeny protection or soliciting support? Primates 25:28–35CrossRefGoogle Scholar
  31. Engh AL, Siebert ER, Greenberg DA, Holekamp KE (2005) Patterns of alliance formation and postconflict aggression indicate spotted hyaenas recognize third-party relationships. Anim Behav 69:209–217CrossRefGoogle Scholar
  32. Estrada A, Sandoval JM (1977) Social relations in a free-ranging troop of stumptail macaques (Macaca arctoides): male-care behaviour I. Primates 18:793–813CrossRefGoogle Scholar
  33. Ferreira RG, Izar P, Lee PC (2006) Exchange, affiliation, and protective interventions in semifree-ranging brown capuchin monkeys (Cebus apella). Am J Primatol 68:765–776. doi: 10.1002/ajp.20277 CrossRefPubMedGoogle Scholar
  34. Fooden J (2007) Systematic review of the Barbary macaque, Macaca sylvanus (Linnaeus, 1758). Fieldiana Zool 113:1–60CrossRefGoogle Scholar
  35. Hamilton WD (1964) The genetical evolution of social behavior, I & II. J Theor Biol 104:451–471Google Scholar
  36. Hennessy MB, Kaiser S, Sachser N (2009) Social buffering of the stress response: diversity, mechanisms, and functions. Front Neuroendocrinol 30:470–482CrossRefPubMedGoogle Scholar
  37. Hinde RA (1976) Interactions, relationships and social structure. Man 11:1–17CrossRefGoogle Scholar
  38. Hrdy SB (1976) Care and exploitation of nonhuman primate infants by conspecifics other than the mother. Adv Study Behav 6:101–158CrossRefGoogle Scholar
  39. Hrdy SB (2005) Evolutionary context of human development: the cooperative breeding model. In: Carter CS, Anhert L, Grossmann KE, Hrdy SB, Lamb ME, Porges SW, Sachser N (eds) Attachment and bonding: a new synthesis. MIT Press, Cambridge, MA, pp 9–32Google Scholar
  40. Johnson CM (2010) Observing cognitive complexity in primates and cetaceans. J Comp Psychol 23:587–624Google Scholar
  41. Judge P (1982) Redirection of aggression based on kinship in a captive group of pigtail macaques. Int J Primatol 3:225–237Google Scholar
  42. Judge PG (1991) Dyadic and triadic reconciliation in pigtail macaques (Macaca nemestrina). Am J Primatol 23:225–237CrossRefGoogle Scholar
  43. Kikusui T, Winslow JT, Mori Y (2006) Social buffering: relief from stress and anxiety. Philos Trans R Soc Lond B Biol Sci 361:2215–2228CrossRefPubMedPubMedCentralGoogle Scholar
  44. Kitchen DM, Cheney DL, Seyfarth RM (2005) Male chacma baboons (Papio hamadryas ursinus) discriminate loud call contests between rivals of different relative ranks. Anim Cogn 8:1–6CrossRefPubMedGoogle Scholar
  45. Kuester J, Paul A, Arnemann J (1994) Kinship, familiarity and mating avoidance in Barbary macaques, Macaca sylvanus. Anim Behav 48:1183–1194CrossRefGoogle Scholar
  46. Kümmerli R, Martin RD (2008) Patterns of infant handling and relatedness in Barbary macaques (Macaca sylvanus) on Gibraltar. Primates 49:271–282CrossRefPubMedGoogle Scholar
  47. Lehmann J, Korstjens AH, Dunbar RIM (2007) Group size, grooming and social cohesion in primates. Anim Behav 74:1617–1629. doi: 10.1016/j.anbehav.2006.10.025 CrossRefGoogle Scholar
  48. Ménard N, Scheffrahn W, Vallet D, Zidane C, Reber C (1992) Application of blood protein electrophoresis and DNA fingerprinting to the analysis of paternity and social characteristics of wild Barbary macaques. In: Martin RD, Dixson AF, Wickings EJ (eds) Paternity in primates: genetic tests and theories. Karger, Basel, pp 155–174Google Scholar
  49. Ménard N, von Segesser F, Scheffrahn W, Pastorini J, Vallet D, Gaci B, Martin RD, Gautier-Hion A (2001) Is male–infant caretaking related to paternity and/or mating activities in wild Barbary macaques (Macaca sylvanus)? Comptes Rendus Académie Sci Sér III Sci Vie 324:601Google Scholar
  50. Moscovice LR, Di Fiore A, Crockford C, Kitchen DM, Wittig R, Seyfarth RM, Cheney DL (2010) Hedging their bets? Male and female chacma baboons form friendships based on likelihood of paternity. Anim Behav 79:1007–1015CrossRefGoogle Scholar
  51. Nagasawa M, Mitsui S, En S, Ohtani N, Ohta M, Sakuma Y, Onaka T, Mogi K, Kikusui T (2015) Oxytocin-gaze positive loop and the coevolution of human-dog bonds. Science 348:333–336. doi: 10.1126/science.1261022 CrossRefPubMedGoogle Scholar
  52. Nguyen N, van Horn RC, Alberts SC, Altmann J (2009) “Friendships” between new mothers and adult males: adaptive benefits and determinants in wild baboons (Papio cynocephalus). Behav Ecol Sociobiol 63:1331–1344CrossRefPubMedPubMedCentralGoogle Scholar
  53. Ogawa H (1995a) Bridging behavior and other affiliative interactions among male Tibetan macaques (Macaca thibetana). Int J Primatol 16:707–729CrossRefGoogle Scholar
  54. Ogawa H (1995b) Recognition of social relationships in bridging behavior among Tibetan macaques (Macaca thibetana). Am J Primatol 35:305–310CrossRefGoogle Scholar
  55. Ostner J, Vigilant L, Bhagavatula J, Franz M, Schülke O (2013) Stable heterosexual associations in a promiscuous primate. Anim Behav 86:623–631. doi: 10.1016/j.anbehav.2013.07.004 CrossRefGoogle Scholar
  56. Paul A (1999) The socioecology of infant handling in primates: Is the current model convincing? Primates 40:33–46CrossRefPubMedGoogle Scholar
  57. Paul A, Kuester J, Arnemann J (1992) DNA fingerprinting reveals that infant care by male Barbary macaques (Macaca sylvanus) is not paternal investment. Folia Primatol 58:93–98CrossRefPubMedGoogle Scholar
  58. Paul A, Kuester J, Arnemann J (1996) The sociobiology of male-infant interactions in Barbary macaques, Macaca sylvanus. Anim Behav 51:155–170CrossRefGoogle Scholar
  59. Peake TM, Terry AMR, McGregor PK, Dabelsteen T (2002) Do great tits assess rivals by combining direct experience with information gathered by eavesdropping? Proc R Soc Lond B Biol Sci 269:1925–1929CrossRefGoogle Scholar
  60. Perry S, Barrett HC, Manson JH (2004) White-faced capuchin monkeys show triadic awareness in their choice of allies. Anim Behav 67:165–170CrossRefGoogle Scholar
  61. Quinn GP, Keough MJ (2002) Experimental design and data analysis for biologists. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  62. R Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, p 2013Google Scholar
  63. Range F, Noë R (2005) Can simple rules account for the pattern of triadic interactions in juvenile and adult female sooty mangabeys? Anim Behav 69:445–452CrossRefGoogle Scholar
  64. Riedman ML (1982) The evolution of alloparental care and adoption in mammals and birds. Q Rev Biol 57:405–435CrossRefGoogle Scholar
  65. Ruiter JD, Geffen E (1998) Relatedness of matrilines, dispersing males and social groups in long-tailed macaques (Macaca fascicularis). Proc R Soc Lond B Biol Sci 265:79–87CrossRefGoogle Scholar
  66. Schino G, Tiddi B, Di Sorrentino EP (2006) Simultaneous classification by rank and kinship in Japanese macaques. Anim Behav 71:1069–1074CrossRefGoogle Scholar
  67. Schino G, Tiddi B, Di Sorrentino EP (2007) Agonistic support in juvenile Japanese macaques: cognitive and functional implications. Ethology 113:1151–1157CrossRefGoogle Scholar
  68. Schmid VS, De Vries H (2013) Finding a dominance order most consistent with a linear hierarchy: an improved algorithm for the I&SI method. Anim Behav 86:1097–1105CrossRefGoogle Scholar
  69. Schülke O, Bhagavatula J, Vigilant L, Ostner J (2010) Social bonds enhance reproductive success in male macaques. Curr Biol 20:2207–2210. doi: 10.1016/j.cub.2010.10.058 CrossRefPubMedGoogle Scholar
  70. Schwarz G (1978) Estimating the dimension of a model. Ann Stat 6:461–464CrossRefGoogle Scholar
  71. Seed AM, Clayton NS, Emery NJ (2007) Postconflict third-party affiliation in rooks, Corvus frugilegus. Curr Biol 17:152–158. doi: 10.1016/j.cub.2006.11.025 CrossRefPubMedGoogle Scholar
  72. Silk JB (1999) Male bonnet macaques use information about third-party rank relationships to recruit allies. Anim Behav 58:45–51CrossRefPubMedGoogle Scholar
  73. Silk JB (2007a) Social components of fitness in primate groups. Science 317:1347–1351CrossRefPubMedGoogle Scholar
  74. Silk JB (2007b) The adaptive value of sociality in mammalian groups. Philos Trans R Soc Lond B Biol Sci 362:539–559CrossRefPubMedPubMedCentralGoogle Scholar
  75. Silk JB, Samuels A (1984) Triadic interactions among Macaca radiata: passports and buffers. Am J Primatol 6:373–376CrossRefGoogle Scholar
  76. Silk JB, Altmann J, Alberts SC (2006) Social relationships among adult female baboons (Papio cynocephalus) I. Variation in the strength of social bonds. Behav Ecol Sociobiol 61:183–195CrossRefGoogle Scholar
  77. Silk JB, Beehner JC, Bergman TJ, Crockford C, Engh AL, Moscovice LR, Wittig RM, Seyfarth RM, Cheney DL (2009) The benefits of social capital: close social bonds among female baboons enhance offspring survival. Proc R Soc B: Biol Sci 276:3099–3104CrossRefGoogle Scholar
  78. Small MF (1990) Promiscuity in Barbary macaques (Macaca sylvanus). Am J Primatol 20:267–282CrossRefGoogle Scholar
  79. Smuts BB (1985) Sex and friendship in baboons. Aldine, New YorkGoogle Scholar
  80. Smuts BB, Gubernick DJ (1992) Male–infant relationships in nonhuman primates: paternal investment or mating effort? In: Hewlett BS (ed) Father–child relations: cultural and biosocial contexts. Aldine de Gruyter, New York, pp 1–30Google Scholar
  81. Stein DM (1984) The sociobiology of infant and adult male baboons. Ablex Publishing Corporation, NorwoodGoogle Scholar
  82. Sterck EHM, Watts DP, van Schaik CP (1997) The evolution of female social relationships in nonhuman primates. Behav Ecol Sociobiol 41:291–309CrossRefGoogle Scholar
  83. Taub DM (1980) Testing the “agonistic buffering” hypothesis. Behav Ecol Sociobiol 6:187–197CrossRefGoogle Scholar
  84. Thierry B, Bynum E, Baker S, Kinnaird MF, Matsumura S, Muroyama Y, O’Brien TG, Petit O, Watanabe K (2000) The social repertoire of Sulawesi macaques. Primate Res 16:203–226CrossRefGoogle Scholar
  85. Tomasello M, Call J (1997) Primate cognition. Oxford University Press, OxfordGoogle Scholar
  86. van Hooff JARAM, van Schaik CP (1994) Male bonds: affiliative relationships among nonhuman primate males. Behaviour 130:309–337. doi: 10.1163/156853994X00587 CrossRefGoogle Scholar
  87. van Schaik CP, Paul A (1996) Male care in primates: does it ever reflect paternity? Evol Anthropol Issues News Rev 5:152–156CrossRefGoogle Scholar
  88. Widdig A, Streich WJ, Tembrock G (2000) Coalition formation among male Barbary macaques (Macaca sylvanus). Am J Primatol 50:37–51CrossRefPubMedGoogle Scholar
  89. Wingfield JC, Hegner RE, Dufty Jr AM, Ball GF (1990) The “challenge hypothesis”: theoretical implications for patterns of testosterone secretion, mating systems, and breeding strategies. Am Nat 136:829–846CrossRefGoogle Scholar
  90. Woodroffe R, Vincent A (1994) Mother’s little helpers: patterns of male care in mammals. Trends Ecol Evol 9:294–297. doi: 10.1016/0169-5347(94)90033-7 CrossRefPubMedGoogle Scholar
  91. Young C, Majolo B, Schülke O, Ostner J (2014a) Male social bonds and rank predict supporter selection in cooperative aggression in wild Barbary macaques. Anim Behav 95:23–32CrossRefGoogle Scholar
  92. Young C, Majolo B, Heistermann M, Schülke O, Ostner J (2014b) Responses to social and environmental stress are attenuated by strong male bonds in wild macaques. Proc Natl Acad Sci 111:18195–18200CrossRefPubMedPubMedCentralGoogle Scholar
  93. Zhao Q-K (1996) Male-infant-male interactions in Tibetan macaques. Primates 37:135–143. doi: 10.1007/BF02381401 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Barbora Kubenova
    • 1
    • 2
    • 6
    Email author
  • Martina Konecna
    • 1
  • Bonaventura Majolo
    • 3
  • Petr Smilauer
    • 4
  • Julia Ostner
    • 2
    • 5
    • 6
  • Oliver Schülke
    • 2
    • 5
    • 6
  1. 1.Department of Zoology, Faculty of ScienceUniversity of South BohemiaCeske BudejoviceCzech Republic
  2. 2.Department of Behavioral Ecology, Johann-Friedrich-Blumenbach Institute for Zoology and AnthropologyGeorg August University GöttingenGöttingenGermany
  3. 3.School of PsychologyUniversity of LincolnLincolnUK
  4. 4.Department of Ecosystem Biology, Faculty of ScienceUniversity of South BohemiaCeske BudejoviceCzech Republic
  5. 5.Research Group Primate Social EvolutionGerman Primate CentreGöttingenGermany
  6. 6.Leibniz ScienceCampus Primate CognitionGerman Primate Center and Georg August University GöttingenGöttingenGermany

Personalised recommendations