International Journal of Primatology

, Volume 28, Issue 2, pp 271–289 | Cite as

Subgrouping Patterns in a Group of Wild Cebus apella nigritus



Seasonal patterns of group fragmentation, including the size of subgroups and percentage of time spent in subgroups, may provide information on individual decision-making in response to resource distribution. Age-sex class composition of subgroup membership can offer insights into the social dynamics of the group as a whole. At most field sites, capuchins (Cebus spp.) form stable groups with no evidence of group fragmentation. Here I describe seasonal subgrouping patterns, including proportion of time spent in subgroups, subgroup size, age-sex membership, dyadic fidelity, stability of membership, and the effect of subgrouping on individual foraging efficiency, in a group of wild Cebus apella nigritus. From September 1996 to August 1997 the study group at the Estação Biológica de Caratinga, Brazil divided into 148 different subgroups, on 99 of 194 census days. In contrast to expectations for subgrouping patterns as a response to seasonal distribution of resources, the proportion of days spent in subgroups did not vary significantly by season. Subgroup composition was relatively fluid, with multimale multifemale subgroups the most common throughout the year. Unimale multifemale subgroups were restricted to the wet season; in contrast, all-male subgroups and unimale unifemale subgroups occurred in the dry season. For both males and females, low rank predicted membership in smaller subgroups. For males, but not females, subgrouping coincided with increased foraging efficiency, as measured by increased time spent ingesting food and decreased time spent traveling on days with subgrouping compared to days with the group in a cohesive unit.


capuchins fission group size seasonality subgroups 



I thank Karen B. Strier (University of Wisconsin-Madison), José Rímoli (Universidade Católica Dom Bosco), David Morales Torres (Universidad Veracruzana), Sérgio Lucena Mendes (Museo de Biologia Mello Leitão), and Michael Edward Alfaro (Washington State University). Alice Guimarães, Andreia Silene Oliva, Laiena Texeira Dib, Rogério Ribeiro dos Santos, Jairo Gomes, Eduardo Veado, and the EBC staff made work at Caratinga a pleasure. This research was supported by grants from Fulbright/IIE, Wenner-Gren Foundation (Predoctoral Grant 6068), Tinker Foundation/Nave Fund, and a National Science Foundation Graduate Fellowship.


  1. Altmann, J. (1974a). Observational study of behavior: Sampling methods. Behaviour, 49, 227–267.PubMedGoogle Scholar
  2. Altmann, S. (1974b). Baboons, space, time, and energy. American Zoologist, 14, 221–248.Google Scholar
  3. Baldwin, J. D., & Baldwin, J. I. (1981). The squirrel monkeys, genus Saimiri. In A. F. Coimbra-Filho & R. A. Mittermeier (Eds.), Ecology and behavior of neotropical primates I (pp. 277–330). Rio de Janeiro: Academia Brasileira de Ciências.Google Scholar
  4. Boinski, S. (2000). Social manipulation within and between troops mediates primate group movement. In S. Boinski & P. A. Garber (Eds.), On the move: How and why animals travel in groups (pp. 421–446). Chicago: University of Chicago Press.Google Scholar
  5. Boubli, J. P. (1999). Feeding ecology of black-headed uacaris (Cacajao melanocephalus melanocephalus) in Pico da Neblina National Park, Brazil. International Journal of Primatology, 20, 719–749.CrossRefGoogle Scholar
  6. Chapman, C. A. (1988). Patch use and patch depletion by the spider and howling monkeys of Santa Rosa National Park, Costa Rica. Behaviour, 105, 99–116.Google Scholar
  7. Chapman, C. A. (1990). Association patterns of spider monkeys: The influence of ecology and sex on social organization. Behavioral Ecology and Sociobiology, 26, 409–414.CrossRefGoogle Scholar
  8. Chapman, C. A., Wrangham, R. W., & Chapman, L. J. (1995). Ecological constraints on group size: An analysis of spider monkey and chimpanzee subgroups. Behavioral Ecology and Sociobiology, 36, 59–70.CrossRefGoogle Scholar
  9. Chepko-Sade, B. D., & Sade, D. S. (1979). Patterns of group splitting within matrilineal kinship groups: A study of social group structure in Macaca mulatta (Cercopithecidae: Primates). Behavioral Ecology and Sociobiology, 5, 67–87.CrossRefGoogle Scholar
  10. Defler, T. R. (1999). Fission-fusion in the black-headed uacari (Cacajao melanocephalus) in eastern Colombia. Neotropical Primates, 7, 5–8.Google Scholar
  11. Di Bitetti, M. (1997). Evidence for an important social role of allogrooming in a platyrrhine primate. Animal Behavior, 54, 199–211.CrossRefGoogle Scholar
  12. Di Bitetti, M. S., & Janson, C. H. (2000). When will the stork arrive? Patterns of birth seasonality in Neotropical primates. American Journal of Primatology, 50, 109–130.PubMedCrossRefGoogle Scholar
  13. Di Bitetti, M. S., & Janson, C. H. (2001). Reproductive socioecology of tufted capuchins (Cebus apella nigritus) in northeastern Argentina. International Journal of Primatology, 22, 127–142.CrossRefGoogle Scholar
  14. Dittus, W. P. J. (1988). Group fission among wild toque macaques as a consequence of female resource competition and environmental stress. Animal Behaviour, 36, 1626–1645.CrossRefGoogle Scholar
  15. Fedigan, L. M., Rose, L. M., & Avila, R. M. (1996). See how they grow, tracking capuchin monkey (Cebus capucinus) populations in regenerating Costa Rican dry forest. In M. A. Norconk, A. L. Rosenberger, & P. A. Garber (Eds.), Adaptative radiations of neotropical primates (pp. 289–307). New York: Plenum Press.Google Scholar
  16. Ferrari, S. F. (1988). The behaviour and ecology of buffy-headed marmoset, Callithrix flaviceps (O Thomas, 1903). PhD Thesis, University College London.Google Scholar
  17. Fukuda, F. (1989). Habitual fission-fusion and social organization of the Hakone troop T of Japanese macaques in Kanagawa Prefecture, Japan. International Journal of Primatology, 10, 419–439.Google Scholar
  18. Guimarães, A. (1998). Ecology and social behavior of buffy headed marmosets, Callithrix flaviceps. Neotropical Primates, 6, 51–52.Google Scholar
  19. Izar, P. (2003). Female social relationships of Cebus apella nigritus in a Southeastern Atlantic forest: An analysis through ecological models of primate social evolution. Behaviour, 141, 71–99.CrossRefGoogle Scholar
  20. Izawa, K. (1976). Group sizes and compositions of monkeys in the Upper Amazon Basin. Primates, 17, 367–399.CrossRefGoogle Scholar
  21. Izawa, K. (1980). Social behavior of the wild black-capped capuchin (Cebus apella). Primates, 21, 443–467.CrossRefGoogle Scholar
  22. Izawa, K. (1990). Social changes within a group of wild black-capped capuchins (Cebus apella) in Colombia (II). Field studies of New World Monkeys, La Macarena Colombia. Japan and Colombia Cooperative Study of Primates, Vol 3, pp. 1–6.Google Scholar
  23. Izawa, K. (1992). Social changes within a group of wild black-capped capuchins (Cebus apella) (III). Field studies of New World Monkeys, La Macarena, Colombia, Vol. 7, pp. 9–14.Google Scholar
  24. Izawa, K. (1994a). Group division of wild black-capped capuchins. Field Studies of New World Monkeys, La Macarena, Colombia, Vol. 9, pp. 5–14.Google Scholar
  25. Izawa, K. (1994b). Social changes within a group of wild black-capped capuchins (IV). Field studies of New World Monkeys, La Macarena Colombia, Vol. 9, pp. 15–21.Google Scholar
  26. Izawa, K. (1997). Social changes within a group of wild black-capped capuchins V. Field studies of New World Monkeys, La Macarena Colombia, Vol. 11, pp. 1–10.Google Scholar
  27. Jack, K., & Fedigan, L. (2004a). Male dispersal patterns in white-faced capuchins, Cebus capucinus Part 1: Patterns and causes of natal emigration. Animal Behaviour, 67, 761–769.CrossRefGoogle Scholar
  28. Jack, K., & Fedigan, L. (2004b). Male dispersal patterns in white-faced capuchins, Cebus capucinus. Part 2: Patterns and causes of secondary dispersal. Animal Behaviour, 67, 771–782.CrossRefGoogle Scholar
  29. Janson, C. H. (1984). Female choice and mating system of brown capuchin monkey Cebus apella (Primates: Cebidae). Zeitshrift für Tierpschychologie, 65, 177–200.Google Scholar
  30. Janson, C. (1986). The mating system as a determinant of social evolution in capuchin monkeys (Cebus). In J. G. Else & P. C. Lee (Eds.), Primate ecology and conservation. New York: Cambridge University Press.Google Scholar
  31. Jolly, A. (1972). Troop continuity and troop spacing in Propithecus verreauxi and Lemur catta at Berenty (Madagascar). Folia Primatologica, 17, 335–362.CrossRefGoogle Scholar
  32. Jones, C. B. (1995). Howler subgroups as homeostatic mechanisms in disturbed habitats. Neotropical Primates, 3, 7–9.Google Scholar
  33. Kinzey, W. G., & Cunningham, E. P. (1994). Variability in Platyrrhine social organization. American Journal of Primatology, 34, 185–198.CrossRefGoogle Scholar
  34. Koyama, N. (1970). Changes in dominance rank and division of a wild Japanese monkey troop in Arashiyama. Primates, 11, 335–390.CrossRefGoogle Scholar
  35. Kummer, H. (1968). Social organization of hamadryas baboons. A field study. Bibliotheca Primatologica, 6, 1–189.Google Scholar
  36. Lynch, J. W. (2001). Male behavior and endocrinology in wild tufted capuchin monkeys, Cebus apella nigritus. Ph.D. dissertation, University of Wisconsin-Madison.Google Scholar
  37. Lynch Alfaro, J. W. (2005). Male mating strategies and reproductive constraints in wild tufted capuchin monkeys, Cebus apella nigritus. American Journal of Primatology, 67, 313–328.CrossRefGoogle Scholar
  38. Lynch, J. W., & Rímoli, J. (2000). Demography of a group of tufted capuchin monkeys (Cebus apella nigritus) at the Estação Biológica de Caratinga, Minas Gerais, Brazil. Neotropical Primates, 8, 44–49.Google Scholar
  39. Lynch, J. W., Ziegler, T. E., & Strier, K. B. (2002). Individual and seasonal variation in fecal testosterone and cortisol in wild male tufted capuchin monkeys, Cebus apella nigritus. Hormones and Behavior, 41, 275–287.PubMedCrossRefGoogle Scholar
  40. Malik, I., Seth, P. K., & Southwick, C. H. (1985). Group fission in free-ranging rhesus monkeys of Tughlaqabad, Northern India. International Journal of Primatology, 6, 411–422.Google Scholar
  41. Martin, R. D. (1972). A preliminary field-study of the lesser mouse lemur (Microcebus murinus J. F. Miller 1777). Forschitte der Verhaltensforschung, 9, 43–89.Google Scholar
  42. Martin, R. D. (1973) A review of the behaviour and ecology of the lesser mouse lemur (Microcebus murinus J. F. Miller 1777). In R. P. Michael & J. H. Crook (Eds.), Comparative ecology and behaviour of primates (pp. 1–6). New York: AcademicPress.Google Scholar
  43. Matheson, M. D., Johnson, J. S., & Feuerstein, J. (1996). Male reunion displays in tufted capuchin monkeys (Cebus apella). American Journal of Primatology, 40, 183–188.CrossRefGoogle Scholar
  44. Matsumoto-Oda, A., Hosaka, K., Huffman, M. A., & Kawanaka, K. (1998). Factors affecting party size in chimpanzees of the Mahale mountains. International Journal of Primatology, 19, 999–1011.CrossRefGoogle Scholar
  45. Mendes, S. L. (1989). Estudo ecológico de Alouatta fusca (Primates: Cebidae) na Estação Biológica de Caratinga, MG. Revista Nordestina de Biologia, 6, 71–104.Google Scholar
  46. Miller, L. E. (1996). The behavioral ecology of wedge-capped capuchin monkeys (Cebus olivaceus). In M. A. Norconk, A. L. Rosenberger, & P. A. Garber (Eds.), Adaptive radiations of neotropical primates (pp. 271–288). New York: Plenum Press.Google Scholar
  47. Milton, K. (1984). Habitat, diet and activity pattern of free-ranging woolly spider monkeys (Brachyteles arachnoides E. Geoffroy 1808). International Journal of Primatology, 5, 491–514.Google Scholar
  48. Morland, H. S. (1991) Preliminary report on the social organization of ruffed lemurs (Varecia variegata variegata) in a northeast Madagascar rain forest. Folia Primatologica, 56, 157–161.CrossRefGoogle Scholar
  49. Nishida, T., & Hiraiwa-Hasegawa, M. (1987). Chimpanzees and bonobos: Cooperative relationships among males. In B. Smuts, D. Cheney, R. Seyfarth, R. Wrangham, & T. Struhsaker (Eds.), Primate societies (pp. 165–180). Chicago: University of Chicago Press.Google Scholar
  50. Panger, M. A. (1997). Hand preference and object-use in free-ranging white faced capuchin monkeys (Cebus capucinus) in Costa Rica. Ph.D. dissertation. University of California, Berkeley.Google Scholar
  51. Perry, S. (1995). Social Relationships in Wild White-Faced Capuchin Monkeys, Cebus capucinus. Ph.D. dissertation, UMI.Google Scholar
  52. Perry, S. (1996a). Female-female social relationships in wild white-faced capuchin monkeys (Cebus capucinus). American Journal of Primatology, 40, 167–182.CrossRefGoogle Scholar
  53. Perry, S. (1996b). Intergroup encounters in wild white-faced capuchins (Cebus capucinus). International Journal of Primatology, 17, 309–330.Google Scholar
  54. Philips, K. A., & Shauver Goodchild, L. M. (2005). Reunion displays in captive male brown capuchins (Cebus apella). Primates, 46, 121–125.CrossRefGoogle Scholar
  55. Rigamonti, M. M. (1993). Home range and diet in red ruffed lemurs (Varecia variegata rubra). on the Masoala Peninsula, Madagascar. In P. M. Kappeler & J. U. Ganzhorn (Eds.), Lemur social systems and their ecological basis (pp. 25–39). New York: Plenum Press.Google Scholar
  56. Rímoli, J. (2001). Ecologia de macacos-pregos (Cebus apella nigritus, Goldfuss, 1809, Primates, Cebidae) na Estação Biológica de Caratinga (MG): implicações para a conservação de fragmentos de Mata Atlântica. Ph.D. dissertation. Centro de Ciência Biológicas, Universidade Federal do Pará.Google Scholar
  57. Rímoli, J., & Ferrari, S. (1997). Comportamento e ecologia de macacos-prego (Cebus apella nigritus, GOLDFUSS 1809) na Estação Biológica de Caratinga (MG). Programa e Resumos, VIII Congresso Brasileiro de Primatologia. João Pessoa, PB, Brasil, p. 231.Google Scholar
  58. Robinson, J. G. (1988a). Demography and group structure in wedge-capped capuchin monkeys, Cebus olivaceus. Behaviour, 104, 202–232.Google Scholar
  59. Robinson, J. G. (1988b). Group size in wedge-capped capuchin monkeys Cebus olivaceus and the reproductive success of males and females. Behavioral Ecology and Sociobiology, 23, 187–197.CrossRefGoogle Scholar
  60. Robinson, J. G., & Janson, C. H. (1987). Capuchins, squirrel monkeys, and atelines: Socioecological convergence with Old World Primates. In B. Smuts, D. Cheney, R. Seyfarth, R. Wrangham, & T. Struhsaker (Eds.), Primate societies (pp. 69–82). Chicago: University of Chicago Press.Google Scholar
  61. Soini, P. (1986). A synecological study of a primate community in the Pacaya-Samiria national Reserve, Peru. Primate Conservation, 7, 63–71.Google Scholar
  62. Strier, K. B. (1992). Faces in the forest: The endangered Muriqui monkeys of Brazil. New York: Oxford University Press.Google Scholar
  63. Strier, K. B., Mendes, S. L, Bragança, A. M., Coelho, C. C., Costa, C. G., Diaz, L. G., et al. (1999). Census of the primate community at the Estação Biológica de Caratinga, Minas Gerais, Brazil. Neotropical Primates, 7, 134–135.Google Scholar
  64. Strier, K. B., Mendes, F. D. C., Rímoli, J., & Rímoli, A. O. (1993). Demography and social structure of one group of muriquis (Brachyteles arachnoides). International Journal Primatology, 14, 513–526.CrossRefGoogle Scholar
  65. Strier, K. B., Mendes, S. L., & Santos, R. R. (2001). The timing of births in sympatric brown howler monkeys (Alouatta fusca clamitans) and northern muriquis (Brachyteles arachnoides hypoxanthus). American Journal Primatology, 55, 87–100.CrossRefGoogle Scholar
  66. Strier, K. B., Ziegler, T. E., & Wittwer, D. J. (1999). Seasonal and social correlates of fecal testosterone and cortisol levels in wild male muriquis (Brachyteles arachnoides). Hormones and Behaviour, 35, 125–134.CrossRefGoogle Scholar
  67. Symington, M. M. (1990). Fission-fusion social organization in Ateles and Pan. International Journal of Primatology, 11, 47–61.CrossRefGoogle Scholar
  68. Tattersall, I. (1982). The primates of Madagascar. Press, New York: Columbia University.Google Scholar
  69. van Noordwijk, M. A., & van Schaik, C. P. (1987). Competition among female long-tailed macaques, Macaca fascicularis. Animal Behavior, 35, 577–589.CrossRefGoogle Scholar
  70. van Schaik, C. P., van Noordwijk, M. A., de Boer, R. J., & den Tonkelaar, I. (1983). The effect of group size on time budgets and social behaviour in wild long-tailed macaques (Macaca fascicularis). Behavioral Ecology and Sociobiology, 13, 173–181.CrossRefGoogle Scholar
  71. White, F. J. (1991) Social organization, feeding ecology, and reproductive strategy of ruffed lemurs, Varecia variegata. In A. Ehara, T. Kimura, O. Takenaka, & M. Iwamonto (Eds.), Primatology today (pp. 81–84). Amsterdam: Elsevier.Google Scholar
  72. White, F. J., & Wrangham, R. W. (1988) Feeding competition and patch size in the chimpanzee species Pan paniscus and Pan troglodytes. Behaviour, 105, 148–164.Google Scholar
  73. Wrangham, R. W. (1980). An ecological model of female-bonded primate groups. Behaviour, 75, 262–300.Google Scholar
  74. Wrangham, R. W., & Smuts, V. V. (1980). Sex differences in the behavioural ecology of chimpanzees in the Gombe National Park, Tanzania. Journal of Reproduction and Fertility, 28, 13–31.PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2007

Authors and Affiliations

  1. 1.Department of Anthropology, College Hall 208 and Center for Reproductive BiologyWashington State UniversityPullmanUSA

Personalised recommendations