International Journal of Primatology

, Volume 20, Issue 1, pp 85–106 | Cite as

Male Migration in Barbary Macaques (Macaca sylvanus) at Affenberg Salem

  • Jutta Kuester
  • Andreas Paul


We analyzed male migration during a 20-year period in the free-ranging Barbary macaque population of Affenberg Salem. Most natal migrations occurred around puberty, but only one third of all males left the natal group. Secondary group transfers were rare. All males immediately transferred to other bisexual groups. Migration rates were highest during periods with high adult female/male ratios within social groups. Immigrants highly preferred groups with fewer males of their own age than in the natal group, and many males immigrated into groups that had no male their own age. These groups originated from a skewed distribution of resident males during group fissions. A comparison of emigrants with their natal peers supports the inbreeding avoidance hypothesis as cause of emigration rather than the male competition avoidance hypothesis. Emigrants had no lower individual rank position and did not come from lower-ranking matrilines. Emigrants had more female maternal relatives, especially sisters. Males without female relatives almost never emigrated. Conversely, there is virtually no indication that emigrants were evicted from the natal group. Emigrants had no increased mortality. Paternity data revealed that the reproductive success of emigrants and natal males is similar, indicating that emigration had no reproductive cost. Many similarities between emigrants and natal males that separated from female maternal kin during group fissions suggest that inner migration during fissions is an alternative way to avoid maternal inbreeding. The mating system resulted in a genetic structure within social groups that largely diminished the chances for paternal inbreeding even without recognizing paternal kin.

male migration natal migration group transfer group choice Barbary macaque Macaca sylvanus function inbreeding avoidance male competition 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Altmann, J., Altmann, S. A., Hausfater, G., and McCuskey, S. (1977). Life histories of yellow baboons: Physical development, reproductive parameters, and infant mortality. Primates 18: 315-330.Google Scholar
  2. Altmann, J., Alberts, S. C., Haines, S. A., Dubach, J., Muruthi, P., Coote, T., Geffen, E., Cheesman, D. J., Mutata, R. S., Saiyalel, S. N., Wayne, R. K., Lacy, R. C., and Bruford, M. W. (1996). Behavior predicts genetic structure in a wild primate group. Proc. Natl. Acad. Sci. USA 93: 5797-5801.Google Scholar
  3. Bartecki, U. (1986). the social position of male Barbary macaques (Macaca sylvanus) in a semifree-ranging population. Primates 27: 173-183.Google Scholar
  4. Berard, J. D. (1989). Life histories of male Cayo Santiago macaques. Puerto Rico Health Sci. J. 8: 61-64.Google Scholar
  5. Bernstein, I. S., and Ehardt, C. L. (1986). Modification of aggression through socialization and the special case of adult and adolescent male rhesus monkeys (Macaca mulatta). Am. J. Primatol. 10: 213-227.Google Scholar
  6. Boelkins, R. C., and Wilson, A. P. (1972). Intergroup social dynamics of the Cayo Santiago rhesus (Macaca mulatta) with special reference to changes in group membership by males. Primates 13: 125-140.Google Scholar
  7. Cheney, D. L., and Seyfarth, R. M. (1983). Non-random dispersal in free-ranging vervet monkeys: Social and genetic consequences. Am. Nat. 122: 392-412.Google Scholar
  8. Clutton-Brock, T. H. (1989). Female transfer and inbreeding avoidance in social mammals. Nature 337: 70-72.Google Scholar
  9. Colvin, J. D. (1986). Proximate causes of male emigration at puberty in rhesus macaques. In Rawlins, R. G., and Kessler, M. J. (eds.), The Cayo Santiago Macaques, SUNY Press, New York, pp. 131-158.Google Scholar
  10. Deag, J. M. (1984). Demography of the Barbary macaque at Ain Khala in the Moroccan Moyen Atlas. In Fa, J. E. (ed.), The Barbary Macaque: A Case Study in Conservation, Plenum, New York, pp. 113-133.Google Scholar
  11. de Ruiter, J. R., and van Hooff, J. A. R. a. M. (1993). Male dominance rank and reproductive success in primate groups. Primates 34: 513-523.Google Scholar
  12. de Turckheim, G., and Merz, E. (1984). Breeding Barbary macaques in outdoor open enclosures. In Fa, J. E. (ed.), The Barbary Macaque: A Case Study in Conservation, Plenum, New York, pp. 241-261.Google Scholar
  13. Drickamer, L. C., and Vessey, H. (1973). Group changing in free-ranging male rhesus monkeys. Primates 14: 359-368.Google Scholar
  14. Fa, J. E. (1982). A survey of population and habitat of the Barbary macaque Macaca sylvanus L. in North Morocco. Biol. Conserv. 24: 45-66.Google Scholar
  15. Gouzoules, S. (1984). Primate mating system, kin associations, and cooperative behavior: Evidence for kin recognition. Yearbk. Phys. Anthropol. 27: 99-134.Google Scholar
  16. Grieger, M. (1984). Verhalten alter Berberaffenweibchen (Macaca sylvanus LINNE, 1758). Ein Vergleich zwischen alten Berberaffenweibchen und ihren adulten Töchtern, Diploma thesis, University of Göttingen, Göttingen.Google Scholar
  17. Hamilton, W. D., Axelrod, R., and Tanese, R. (1990). Sexual reproduction as an adaptation to resist parasites. Proc. Natl. Acad. Sci. USA 87: 3566-3573.Google Scholar
  18. Henzi, S. P., and Lucas, J. W. (1980). Observations on the inter-troop movement of adult vervet monkeys (Cercopithecus aethiops). Folia Primatol. 33: 220-235.Google Scholar
  19. Inoue, M., Mitsunaga, F., Ohsawa, H., Takenaka, A., Sugiyama, Y., Gaspard, S. A., and Takenaka, O. (1991). Male mating behaviour and paternity discrimination by DNA-fingerprinting in a Japanese macaque group. Folia Primatol. 56: 202-210.Google Scholar
  20. Koyama, N. (1970). Changes in dominance rank and division of a wild Japanese monkey troop in Arashiyama. Primates 11: 335-390.Google Scholar
  21. Kuester, J., and Paul,, A. (1988). rank relations of juvenile and subadult natal males of Barbary macaques (Macaca sylvanus) at Affenberg Salem. Folia Primatol. 51: 33-44.Google Scholar
  22. Kuester, J., and Paul, A. (1989). Reproductive strategies of subadult Barbary macaque males at Affenberg Salem. In Rasa, A. E., Vogel, C., and Voland, E. (eds.), Sociobiology of Reproductive Strategies in Animals and Humans, Chapman and Hall, London, pp. 93-109.Google Scholar
  23. Kuester, J., and Paul, A. (1992). Influence of male competition and female mate choice on male mating success in Barbary macaques (Macaca sylvanus). Behaviour 120: 192-217.Google Scholar
  24. Kuester, J., and Paul, A. (1997). Group fission in Barbary macaques (Macaca sylvanus) at “Affenberg Salem.” Int. J. Primatol. 18: 941-966.Google Scholar
  25. Kuester, J., Paul, A., and Arnemann, J. (1992). Paternity determination by oligonucleotide DNA fingerprinting in Barbary macaques (Macaca sylvanus). In Martin, R. D., Dixson, A. F., and Wickings, E. J. (Eds.), Paternity in Primates: Genetic Tests and Theories, Karger, Basel, pp. 141-154.Google Scholar
  26. Kuester, J., Paul, A., and Arnemann, J. (1994). Kinship, familiarity and mating avoidance in Barbary macaques (Macaca sylvanus). Anim. Behav. 48: 1183-1194.Google Scholar
  27. Kuester, J., Paul, A., and Arnemann, J. (1995). Age-related and individual differences of reproductive success in male and female Barbary macaques (Macaca sylvanus). Primates 36: 461-476.Google Scholar
  28. Lacy, R. C., Petric, A., and Warneke, M. (1993). Inbreeding and outbreeding in captive populations of wild animal species. In Thornhill, N. W. (ed.), The Natural History of Inbreeding and Outbreeding, University of Chicago Press, Chicago, pp. 352-374.Google Scholar
  29. Maynard Smith, J. (1978). The Evolution of Sex, Cambridge University Press, Cambridge.Google Scholar
  30. Mehlman, P. T. (1985). Intergroup dynamics of the Barbary macaque (Macaca sylvanus L.), Ghomaran Rif Mountains, Morocco. Am. J. Phys. Anthropol. 66: 204 (abstr.).Google Scholar
  31. Mehlmann, P. T. (1986). Male intergroup mobility in a wild population of the Barbary macaque (Macaca sylvanus), Ghomaran Rif Mountains, Morocco. Am. J. Primatol. 10: 67-81.Google Scholar
  32. Melnick, D. J. (1987). The genetic consequences of primate social organization: A review of macaques, baboons and vervet monkeys. Genetica 73: 117-135.Google Scholar
  33. Melnick, D. J., and Hoelzer, G. A. (1996). The population genetic consequences of macaque social organization and behavior. In Fa, J. E., and Lindburg, D. G. (eds.), Evolution and Ecology of Macaque Societies, Cambridge University Press, Cambridge, pp. 413-443.Google Scholar
  34. Melnick, D. J., Pearl, M. C., and Richard, A. F. (1984). Male migration and inbreeding avoidance in wild rhesus monkeys. Am. J. Primatol. 7: 229-243.Google Scholar
  35. Ménard, N., and Vallet, D. (1993a). Population dynamics of Macaca sylvanus in Algeria: An 8-year study. Am. J. Primatol. 30: 101-118.Google Scholar
  36. Ménard, N., and Vallet, D. (1993b). Dynamics of fission in a wild Barbary macaque group (Macaca sylvanus). Int. J. Primatol. 14: 479-500.Google Scholar
  37. Ménard, N., and Vallet, D. (1996). Demography and ecology of barbary macaques (Macaca sylvanus) in two different habitats. In Fa, J. E., and Lindburg, D. G. (eds.), Evolution and Ecology of Macaque Societies, Cambridge University Press, Cambridge, pp. 106-131.Google Scholar
  38. Mitton, J. B. (1993). Theory and data pertinent to the relationship between heterozygosity and fitness. In Thornhill, N. W. (ed.), The Natural History of Inbreeding and Outbreeding, University of Chicago Press, Chicago, pp. 17-41.Google Scholar
  39. Mohnot, S. M. (1978). Peripheralization of weaned male juveniles in Presbytis entellus. In Chivers, D. J., and Herbert, J. (eds.), Recent Advances in Primatology, Academic Press, New York, pp. 87-91.Google Scholar
  40. Moore, J. (1993). Inbreeding and outbreeding in primates: What's wrong with “the dispersing sex”? In Thornhill, N. W. (ed.), The Natural History of Inbreeding and Outbreeding, University of Chicago Press, Chicago, pp. 392-426.Google Scholar
  41. Moore, J., and Ali, R. (1984). Are dispersal and inbreeding avoidance related? Anim. Behav. 32: 94-112.Google Scholar
  42. Moore, J., and Ali, R. (1985). Inbreeding and dispersal—Reply to Packer (1985). Anim. Behav. 33: 1367-1369.Google Scholar
  43. Norikoshi, K., and Koyama, N. (1975). Group shifting and social organization among Japanese monkeys. In Kondo, S., Kawai, M., Ehara, A., and Kawamura, S. (eds.), Proc. Symp. 5th Congr. Int. Primatol. Japan Science Press, Tokyo, pp. 43-61.@ref alpha = Packer, C. (1979). Inter-troop transfer and inbreeding avoidance in Papio anubis. Anim. Behav. 27: 1–36.Google Scholar
  44. Paul, A. (1984). Zur Sozialstruktur und Sozialisation semi-freilebender Berberaffen (Macaca sylvanus L. 1758), Ph.D. thesis, University of Kiel, Kiel.Google Scholar
  45. Paul, A., and Kuester, J. (1985). Intergroup transfer and incest avoidance in semifree-ranging Barbary macaques (Macaca sylvanus) at Salem (FRG). Am. J. Primatol. 8: 317-322.Google Scholar
  46. Paul, A., and Kuester, J. (1988). Life history patterns of semi-free-ranging Barbary macaques (Macaca sylvanus) at Affenberg Salem (FRG). In Fa, J. E., and Southwick, C. H. (eds.), Ecology and Behavior of Food-Enhanced Primate Groups, Alan R. Liss, New York, pp. 199-228.Google Scholar
  47. Paul, A., Kuester, J., and Arnemann, J. (1992). DNA fingerprinting reveals that infant care by male Barbary macaques (Macaca sylvanus) is not paternal investment. Folia Primatol. 58: 93-98.Google Scholar
  48. Paul, A., Kuester, J., and Podzuweit, D. (1993a). Reproductive senescence and terminal investment in female Barbary macaques (Macaca sylvanus). Int. J. Primatol. 14: 105-124.Google Scholar
  49. Paul, A., Kuester, J., Timme, A., and Arnemann, J. (1993b). The association between rank, mating effort, and reproductive success in male Barbary macaques (Macaca sylvanus). Primates 34: 491-502.Google Scholar
  50. Pope, T. H. (1990). The reproductive consequences of male cooperation in the red howler monkey: Paternity exclusion in multi-male and single-male troops using genetic markers. Behav. Ecol. Sociobiol. 27: 439-446.Google Scholar
  51. Pusey, A. (1990). Mechanisms of inbreeding avoidance in nonhuman primates. In Feierman, J. R. (ed.), Pedophilia: Biosocial Dimensions, Springer, New York, pp. 201-220.Google Scholar
  52. Pusey, A. E., and Packer, C. (1987). Dispersal and philopatry. In Smuts, B. B., Cheney, D. L., Seyfarth, R. M., Wrangham, R. W., and Struhsaker, T. T. (eds.), Primate Societies, University of Chicago Press, Chicago, pp. 250-266.Google Scholar
  53. Ralls, K., and Ballou, J. (1982). Effects of inbreeding on infant mortality in captive primates. Int. J. Primatol. 3: 491-505.Google Scholar
  54. Rowell, T. E., and Chism, J. (1986). Sexual dimorphism and mating systems: jumping to conclusions. Hum. Evol. 1: 215-219.Google Scholar
  55. Smith, D. G. (1995). Absence of deleterious effects of inbreeding in rhesus macaques. Int. J. Primatol. 16: 855-870.Google Scholar
  56. Sugiyama, Y. (1967). Social organization of Hanuman langurs. In Altmann, S. A. (ed.), Social Communication Among Primates, University of Chicago Press, Chicago, pp. 221-236.Google Scholar
  57. Sugiyama, Y. (1976). Life history of male Japanese monkeys. Adv. Stud. Behav. 7: 255-284.Google Scholar
  58. Sugiyama, Y., and Ohsawa, H. (1982). Population dynamics of Japanese monkeys with special reference to the effects of artificial feeding. Folia Primatol. 39: 238-263.Google Scholar
  59. Timme, A. (1989). Differentielle Aufzuchtsstrategien semi-freilebender Berberaffenmütter (Macaca sylvanus L. 1758) in Abhängigkeit vom mütterlichen Rang und dem Geschlecht der Infantes, Ph.D. thesis, University of Göttingen, Göttingen.Google Scholar
  60. Vessey, S. H., Meikle, D. B., and Drickamer, L. C. (1989). Demographic and descriptive studies at La Parguera, Puerto Rico. Puerto Rico Health Sci. J. 8: 121-127.Google Scholar
  61. Walters, J. R. (1987). Kin recognition in nonhuman primates. In Fletcher, D. J. C., and Michener, C. D. (eds.), Kin Recognition in Animals, Wiley & Sons, Chichester, pp. 360-393.Google Scholar
  62. Wickings, E. J., Bossi, T., and Dixson, A. F. (1993). Reproductive success in the mandrill, Mandrillus spinx: Correlations of male dominance and mating success with paternity, as determined by DNA-fingerprinting. J. Zool. Lond. 231: 563-574.Google Scholar
  63. Winkler, P., Loch, H., and Vogel, C. (1984). Life history of Hanuman langurs (Presbytis entellus): Reproductive parameters, infant mortality, and troop development. Folia Primatol. 43: 1-23.Google Scholar
  64. Zhao, Q.-K. (1994). Mating competition and intergroup transfer of males in Tibetan macaques (Macaca thibetana) at Mt. Emei, China. Primates 35: 57-68.Google Scholar

Copyright information

© Plenum Publishing Corporation 1999

Authors and Affiliations

  • Jutta Kuester
    • 1
  • Andreas Paul
    • 2
  1. 1.Allgem. Zoologie & NeurobiologieRuhr-Universität BochumBochumGermany
  2. 2.Institut für Zoologie & AnthropologieUniversität GöttingenGöttingenGermany

Personalised recommendations