Advertisement

International Journal of Primatology

, Volume 40, Issue 3, pp 300–315 | Cite as

The Effect of Dominance Rank on the Distribution of Different Types of Male–Infant–Male Interactions in Barbary Macaques (Macaca sylvanus)

  • Barbora KuběnováEmail author
  • Julia Ostner
  • Oliver Schülke
  • Bonaventura Majolo
  • Petr Šmilauer
  • Martina Konečná
Article

Abstract

In several cercopithecine species males exhibit a specific type of male–infant–male interaction during which two males briefly manipulate an infant. These interactions typically occur after a male carrying an infant (infant holder) approaches or is approached by another male who is not holding an infant (infant nonholder). The agonistic buffering and relationship management hypotheses explain these interactions as a tool to establish and maintain social bonds among males. Both hypotheses predict that males preferentially use the opportunity to interact and bond with males dominant to themselves. However, the agonistic buffering hypothesis predicts that males preferentially initiate male–infant–male interactions with the highest ranking males available, whereas the relationships management hypothesis predicts that males are more likely to interact with males that are close to them in rank. To test these predictions, we collected data on 1562 male–infant–male interactions during 1430 hours of focal observation of 12 infants in one group of wild Barbary macaques (Macaca sylvanus) in Morocco. Using generalized linear mixed-effect models we found that males preferably initiated interactions with males that were dominant to them. However, we observed this effect only for interactions initiated by the infant holder. In interactions initiated by non-holders, the receiver’s relative rank did not predict the frequency of interactions. Males also initiated more interactions with males close in rank to themselves than distantly ranked males. Our results support the relationship management hypothesis, but also indicate that the different types of male–infant–male interactions may require different explanations.

Keywords

Agonistic buffering Infant handling Macaca sylvanus Male–infant–male interactions Relationship management Social hierarchy 

Notes

Acknowledgments

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 a 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 Desertification of Morocco for research permission and professor Mohamed Mouna (Institute Scientsifique, Rabat, Morocco) and professor Mohamed Quarro (Ecole Nationale Forestière d’Ingénieurs, Salé, Morocco) for their invaluable support and cooperation during the field work. We appreciate the advice and support of Josephine Kalbitz, Adeelia Goffe, Andreas Berghänel, Christopher Young, Christina Haunhorst, and Stanislav Lhota. We are particularly thankful to James Waterman for his support and comments on the earlier version of the manuscript. We also want to thank Dr. Joanna Setchell, Dr. Daphne Kerhoas, and one anonymous referee for their thoughtful and insightful comments on the manuscript.

B. Kuběnová, O. Schülke, J. Ostner, and M. Konečná conceived the idea, formulated the aims of the study, and designed the methodology; B. Majolo provided the study site; B. Kuběnová conducted field work and collected data; P. Šmilauer and B. Kuběnová performed statistical analysis; and B. Kuběnová, O. Schülke, J. Ostner, B. Majolo, and M. Konečná wrote the manuscript.

References

  1. Altmann, J. (1974). Observational study of behavior: Sampling methods. Behaviour, 49(3), 227–266.CrossRefGoogle Scholar
  2. Bates, D., Maechler, M., Bolker, B., Walker, S., & others. (2014). lme4: Linear mixed-effects models using Eigen and S4. R package version, 1(7), 1–23.Google Scholar
  3. Bauer, B., Sheeran, L. K., Matheson, M. D., Li, J.-H., & Wagner, R. S. (2014). Male Tibetan macaques (Macaca thibetana) choice of infant bridging partners. Zoological Research, 35(3), 222–230.PubMedGoogle Scholar
  4. Berghänel, A., Schülke, O., & Ostner, J. (2010). Coalition formation among Barbary macaque males: The influence of scramble competition. Animal Behaviour, 80(4), 675–682.CrossRefGoogle Scholar
  5. Berghänel, A., Ostner, J., Schröder, U., & Schülke, O. (2011). Social bonds predict future cooperation in male Barbary macaques, Macaca sylvanus. Animal Behaviour, 81(6), 1109–1116.CrossRefGoogle Scholar
  6. Bernstein, I. S., & Cooper, M. A. (1998). Ambiguities in the behavior of Assamese macaques. American Journal of Primatology, 45, 170–171.Google Scholar
  7. Bissonnette, A., de Vries, H., & van Schaik, C. P. (2009). Coalitions in male Barbary macaques, Macaca sylvana: strength, success and rules of thumb. Animal Behaviour, 78(2), 329–335.CrossRefGoogle Scholar
  8. Busse, C. D., & Gordon, T. P. (1984). Infant carrying by adult male mangabeys (Cercocebus atys). American Journal of Primatology, 6(3), 133–141.CrossRefGoogle Scholar
  9. Busse, C., & Hamilton, W. J. (1981). Infant carrying by male chacma baboons. Science, 212(4500), 1281–1283.CrossRefGoogle Scholar
  10. Chalmers, N. R. (1968). The social behaviour of free living mangabeys in Uganda. Folia Primatologica, 8(3–4), 263–281.CrossRefGoogle Scholar
  11. Collins, D. A. (1986). Interactions between adult male and infant yellow baboons (Papio c. cynocephalus) in Tanzania. Animal Behaviour, 34(2), 430–443.CrossRefGoogle Scholar
  12. De Vries, H., Stevens, J. M., & Vervaecke, H. (2006). Measuring and testing the steepness of dominance hierarchies. Animal Behaviour, 71(3), 585–592.CrossRefGoogle Scholar
  13. de Waal, F. B., van Hooff, J. A., & Netto, W. J. (1976). An ethological analysis of types of agonistic interaction in a captive group of Java-monkeys (Macaca fascicularis). Primates, 17(3), 257–290.CrossRefGoogle Scholar
  14. Deag, J. M. (1974). A study of the social behavior and ecology of the wild Barbary macaque, Macaca sylvanus, L. 1758. Unpublished doctoral dissertation, University of Bristol.Google Scholar
  15. Deag, J. M. (1980). Interactions between males and unweaned Barbary macaques: Testing the agonistic buffering hypothesis. Behaviour, 75, 54–81.CrossRefGoogle Scholar
  16. Deag, J. M., & Crook, J. H. (1971). Social behaviour and ‘agonistic buffering’ in the wild Barbary macaque Macaca sylvana L. Folia Primatologica, 15(3–4), 183–200.CrossRefGoogle Scholar
  17. Dunbar, R. I. M. (1984). Infant-use by male gelada in agonistic contexts: Agonistic buffering, progeny protection or soliciting support? Primates, 25(1), 28–35.CrossRefGoogle Scholar
  18. Estrada, A., & Sandoval, J. M. (1977). Social relations in a free-ranging troop of stumptail macaques (Macaca arctoides): Male-care behaviour I. Primates, 18(4), 793–813.CrossRefGoogle Scholar
  19. Henkel, S., Heistermann, M., & Fischer, J. (2010). Infants as costly social tools in male Barbary macaque networks. Animal Behaviour, 79(6), 1199–1204.CrossRefGoogle Scholar
  20. Holm, S. (1979). A simple sequentially rejective multiple test procedure. Scandinavian Journal of Statistics, 6, 65–70.Google Scholar
  21. Kalbitz, J., Schülke, O., & Ostner, J. (2017). Triadic male-infant-male interaction serves in bond maintenance in male Assamese macaques. PLoS One, 12(10), e0183981.CrossRefGoogle Scholar
  22. Kleindorfer, S., & Wasser, S. (2004). Infant handling and mortality in yellow baboons (Papio cynocephalus): Evidence for female reproductive competition? Behavioral Ecology and Sociobiology, 56(4), 328–337.CrossRefGoogle Scholar
  23. Kuester, J., & Paul, A. (1992). Influence of male competition and female mate choice on male mating success in Barbary macaques (Macaca sylvanus). Behaviour, 120(3), 192–216.Google Scholar
  24. Kuběnová, B., Konečná, M., Majolo, B., Šmilauer, P., Ostner, J., & Schülke, O. (2017). Triadic awareness predicts partner choice in male–infant–male interactions in Barbary macaques. Animal Cognition, 20(2), 221–232.CrossRefGoogle Scholar
  25. Kümmerli, R., & Martin, R. D. (2008). Patterns of infant handling and relatedness in Barbary macaques (Macaca sylvanus) on Gibraltar. Primates, 49(4), 271–282.CrossRefGoogle Scholar
  26. Maestripieri, D. (1994). Social structure, infant handling, and mothering styles in group-living Old World monkeys. International Journal of Primatology, 15(4), 531–553.CrossRefGoogle Scholar
  27. Maestripieri, D. (1997). Gestural communication in macaques: Usage and meaning of nonvocal signals. Evolution of Communication, 1(2), 193–222.CrossRefGoogle Scholar
  28. McFarland, R., & Majolo, B. (2011). Grooming coercion and the post-conflict trading of social services in wild Barbary macaques. PLoS One, 6(10), e26893.CrossRefGoogle Scholar
  29. Ménard, N., von Segesser, F., Scheffrahn, W., Pastorini, J., Vallet, D., et al (2001). Is male-infant caretaking related to paternity and/or mating activities in wild Barbary macaques (Macaca sylvanus)? Comptes Rendus de l’Académie des Sciences. Série III, Sciences de la Vie, 324(7), 601.PubMedGoogle Scholar
  30. Minge, C., Berghänel, A., Schülke, O., & Ostner, J. (2016). Patterns and consequences of male–infant relationships in wild Assamese macaques (Macaca assamensis). International Journal of Primatology, 37(3), 350–370.CrossRefGoogle Scholar
  31. Mitani, J. C. (2009). Male chimpanzees form enduring and equitable social bonds. Animal Behaviour, 77(3), 633–640.CrossRefGoogle Scholar
  32. Ogawa, H. (1995). Bridging behavior and other affiliative interactions among male Tibetan macaques (Macaca thibetana). International Journal of Primatology, 16(5), 707–729.CrossRefGoogle Scholar
  33. Packer, C. (1980). Male care and exploitation of infants in Papio anubis. Animal Behaviour, 28(2), 512–520.CrossRefGoogle Scholar
  34. Paul, A. (1999). The socioecology of infant handling in primates: Is the current model convincing? Primates, 40(1), 33–46.CrossRefGoogle Scholar
  35. Paul, A., Kuester, J., & Arnemann, J. (1996). The sociobiology of male-infant interactions in Barbary macaques, Macaca sylvanus. Animal Behaviour, 51(1), 155–170.CrossRefGoogle Scholar
  36. Preuschoft, S., Paul, A., & Kuester, J. (1998). Dominance styles of female and male Barbary macaques (Macaca sylvanus). Behaviour, 135(6), 731–755.Google Scholar
  37. Preuschoft, S., & van Schaik, C. P. (2000). Dominance and communication. In F. Aureli & F. B. M. de Waal (Eds.), Natural conflict resolution (pp. 77–105). Berkeley: University of California Press.Google Scholar
  38. R Core Team (2014). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. 2013.Google Scholar
  39. Schino, G., Speranza, L., Ventura, R., & Troisi, A. (2003). Infant handling and maternal response in Japanese macaques. International Journal of Primatology, 24(3), 627–638.CrossRefGoogle Scholar
  40. Seyfarth, R. M. (1976). Social relationships among adult female baboons. Animal Behaviour, 24(4), 917–938.CrossRefGoogle Scholar
  41. Silk, J. B. (1994). Social relationships of male bonnet macaques: Male bonding in a matrilineal society. Behaviour, 130(3), 271–291.CrossRefGoogle Scholar
  42. Silk, J. B., & Samuels, A. (1984). Triadic interactions among Macaca radiata: Passports and buffers. American Journal of Primatology, 6(4), 373–376.CrossRefGoogle Scholar
  43. Smith, E. O., & Peffer-Smith, P. G. (1982). Triadic interactions in captive Barbary macaques (Macaca sylvanus, Linnaeus, 1758): “Agonistic buffering”? American Journal of Primatology, 2(1), 99–107.CrossRefGoogle Scholar
  44. Smuts, B. B. (1985). Sex and friendship in baboons. New York: Aldine.Google Scholar
  45. Stein, D. M. (1981). The nature and function of social interactions between infant and adult male yellow baboons (Papio cynocephalus). In PhD thesis. University of Chicago.Google Scholar
  46. Stein, D. M. (1984). The sociobiology of infant and adult male baboons (Vol. 5). Norwood: Ablex Publishing Corporation.Google Scholar
  47. Taub, D. M. (1980). Testing the ‘agonistic buffering’ hypothesis. Behavioral Ecology and Sociobiology, 6(3), 187–197.CrossRefGoogle Scholar
  48. Taub, D. M. (1984). Male caretaking behavior among wild Barbary macaques (Macaca sylvanus). In D. M. Taub (Ed.), Primate paternalism (pp. 20–55). New York: Van Nostrand Reinhold.Google Scholar
  49. Thierry, B., Bynum, E., Baker, S., Kinnaird, M., Matsumura, S., et al (2000). The social repertoire of Sulawesi macaques. Primate Research, 16, 203–226.CrossRefGoogle Scholar
  50. Trivers, R. (1972). Parental investment and sexual selection. In B. Campbell (Ed.), Sexual selection and the descent of man (pp. 136–176). London: Heinemann.Google Scholar
  51. Van Schaik, C. P., & Paul, A. (1996). Male care in primates: Does it ever reflect paternity? Evolutionary Anthropology: Issues, News, and Reviews, 5(5), 152–156.CrossRefGoogle Scholar
  52. Whitten, P. L. (1987). Infants and adult males. In B. B. Smuts, D. L. Cheney, R. M. Seyfarth, & T. T. Struhsaker (Eds.), Primate societies (pp. 343–357). Chicago: University of Chicago Press.Google Scholar
  53. Widdig, A., Streich, W. J., & Tembrock, G. (2000). Coalition formation among male Barbary macaques (Macaca sylvanus). American Journal of Primatology, 50(1), 37–51.CrossRefGoogle Scholar
  54. Wiper, S. M., & Semple, S. (2007). The function of teeth chattering in male Barbary macaques (Macaca sylvanus). American Journal of Primatology, 69(10), 1179–1188.CrossRefGoogle Scholar
  55. Young, C., Hähndel, S., Majolo, B., Schülke, O., & Ostner, J. (2013). Male coalitions and female behaviour affect male mating success independent of dominance rank and female receptive synchrony in wild Barbary macaques. Behavioral Ecology and Sociobiology, 67(10), 1665–1677.CrossRefGoogle Scholar
  56. Young, C., Majolo, B., Heistermann, M., Schülke, O., & Ostner, J. (2014). Responses to social and environmental stress are attenuated by strong male bonds in wild macaques. Proceedings of the National Academy of Sciences of the USA, 111(51), 18195–18200.CrossRefGoogle Scholar
  57. Zhao, Q.-K. (1996). Male-infant-male interactions in Tibetan macaques. Primates, 37(2), 135–143.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Zoology, Faculty of ScienceUniversity of South BohemiaČeské BudějoviceCzech Republic
  2. 2.Department of Behavioral Ecology, Johann-Friedrich-Blumenbach Institute for Zoology and AnthropologyGeorg August University GöttingenGöttingenGermany
  3. 3.Primate Research InstituteKyoto UniversityInuyamaJapan
  4. 4.Research Group Primate Social EvolutionGerman Primate CentreGöttingenGermany
  5. 5.Leibniz ScienceCampus Primate CognitionGerman Primate Center and Georg August University GöttingenGöttingenGermany
  6. 6.School of PsychologyUniversity of LincolnLincolnUK
  7. 7.Department of Ecosystem Biology, Faculty of ScienceUniversity of South BohemiaČeské BudějoviceCzech Republic

Personalised recommendations