Flexible and conservative features of social systems in tufted capuchin monkeys: Comparing the socioecology of Sapajus libidinosus and Sapajus nigritus

American Journal of Primatology

Volumn 74, Issue 4, 2012, Pages 315-331

  Izar, Patrícia ^a   Verderane, Michele P ^a   Peternelli dos Santos, Lucas ^a   Mendonça Furtado, Olívia ^a   Presotto, Andréa ^a   Tokuda, Marcos ^a   Visalberghi, Elisabetta ^b   Fragaszy, Dorothy ^c  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b INSTITUTE OF COGNITIVE SCIENCES AND TECHNOLOGIES   (Italy)

^c University of Georgia   (United States)

Author keywords

Adaptability; Cebus; Food competition; Phylogenetic inertia; Predation risk; Sapajus

Indexed keywords

ADAPTATION; BEHAVIORAL ECOLOGY; COMPARATIVE STUDY; ECOLOGICAL IMPACT; FOOD AVAILABILITY; GROUP SIZE; INFANTICIDE; PHILOPATRY; PHYLOGENETICS; POLYGYNY; PREDATION RISK; PRIMATE; REPRODUCTIVE STRATEGY; SEMIARID REGION; SOCIAL BEHAVIOR; SOCIAL ORGANIZATION; SOCIAL STRUCTURE; SOCIOBIOLOGY;

ATLANTIC FOREST; BRAZIL; CARLOS BOTELHO STATE PARK; PIAUI; SAO PAULO [BRAZIL];

CEBUS; PRIMATES;

EID: 84860330068     PISSN: 02752565     EISSN: 10982345     Source Type: Journal    
DOI: 10.1002/ajp.20968     Document Type: Article

References (98)

1. Altmann J. 1974. Observational study of behaviour: sampling methods. Behaviour 49:223-265.
2. Aureli F, Schaffner C, Boesch C, Bearder SK, Call J, Chapman CA, Connor R, DiFiore A, Dunbar RIM, Henzi PS, Holekamp K, Korstjens AH, Layton R, Lee P, Lehmann J, Manson JH, Ramos-Fernandez G, Strier KB, van Schaik CP. 2008. Fission-fusion dynamics: new research frameworks. Current Anthropology 49:627-654.
3. Barton RA, Byrne R, Whiten A. 1996. Ecology, feeding competition and social structure in baboons. Behavioral Ecology and Sociobiology 38:321-329.
4. Batalha MA, Martins FR. 2004. Reproductive phenology of the cerrado plant community in Emas National Park (central Brazil). Australian Journal of Botany 52:149-161.
5. Bergstrom ML, Fedigan LM. 2010. Dominance among female white-faced capuchin monkeys (Cebus capucinus): hierarchical linearity, nepotism, strength and stability. Behaviour 147:899-931.
6. Bishop N, Hrdy SB, Teas J, Moore J. 1981. Measures of human influence in habitats of South Asian langurs. International Journal of Primatology 153-167.
7. Boesch C, Boesch-Achermann H. 2000. The chimpanzees of the Taï forest. Oxford: Oxford University Press.
8. Boinski S, Sughrue K, Selvaggi L, Quatrone R, Henry M, Cropp S. 2002. An expanded test of the ecological model of primate social evolution: competitive regimes and female bonding in three species of squirrel monkeys (Saimiri oerstedii, S. boliviensis, and S. sciureus). Behaviour 139:227-261.
9. Boinski S, Kauffman L, Westoll A, Stickler CM, Cropp S, Ehmke E. 2003. Are vigilance, risk from avian predators and group size consequences of habitat structure? A comparison of three species of squirrel monkey (Saimiri oerstedii, S. boliviensis, and S. sciureus). Behaviour 140:1421-1467.
10. Borries C, Larney E, Lu A, Ossi K, Koenig A. 2008. Costs of group size: lower developmental and reproductive rates in larger groups of leaf monkeys. Behavioral Ecology 19:1186-1194.
11. Bronikowski AM, Altmann J. 1996. Foraging in a variable environment: weather patterns and the behavioral ecology of baboons. Behavioral Ecology and Sociobiology 39:11-25.
12. Brown AD, Zunino GE. 1990. Dietary variability in Cebus apella in extreme habitats: evidence for adaptability. Folia Primatologica 54:187-195.
13. Cahan SH, Blumstein DT, Sundström L, Liebig J, Griffin A. 2002. Social trajectories and the evolution of social behavior. Oikos 96:206-216.
14. Carosi M, Linn GS, Visalberghi E. 2005. The sexual behavior and breeding system of tufted capuchin monkeys (Cebus apella). In: Slater PJB, Rosenblatt JS, Snowdon CT, Roper TJ, editors. Advances in the study of behavior. San Diego: Academic Press-Elsevier. p 105-149.
15. Chancellor RL, Isbell LA. 2009. Food site residence time and female competitive relationships in wild gray-cheeked mangabeys (Lophocebus albigena). Behavioral Ecology and Sociobiology 63:1447-1458.
16. Chapman CA, Chapman LJ. 2000. Determinants of group size in primates: the importance of travel costs. In: Boinski S, Garber PA, editors. On the move: how and why animals travel in groups. Chicago: University of Chicago Press. p 24-41.
17. Chapman CA, Rothman JM. 2009. Within-species differences in primate social structure: evolution of plasticity and phylogenetic constraints. Primates 50:12-22.
18. Chapman CA, Wrangham R, Chapman LJ. 1994. Indices of habitat-wide fruit abundance in tropical forests. Biotropica 26:160-171.
19. Clutton-Brock TH. 2004. What is sexual selection? In: Kappeler PM, van Schaik CP, editors. Sexual selection in primates, new and comparative perspectives. Cambridge: Cambridge University Press. p 24-36.
20. Crockett CM, Janson CH. 2000. Infanticide in red howlers: female group size, male membership, and a possible link to folivory. In: van Schaik CP, Janson CH, editors. Infanticide by males and its implications. Cambridge: Cambridge University Press. p 75-98.
21. Di Bitetti MS. 1997. Evidence for an important social role of grooming in a platyrrhine primate. Animal Behaviour 54:199-211.
22. Di Bitetti MS. 2001. Home-range use by the tufted capuchin monkey (Cebus apella nigritus) in a subtropical rainforest of Argentina. Journal of Zoology, London 253:33-45.
23. Di Bitetti MS, Janson CH. 2001. Reproductive socioecology of tufted capuchins (Cebus apella nigritus) in northeastern Argentina. International Journal of Primatology 22:127-142.
24. Di Fiore A, Rendall D. 1994. Evolution of social organization: a reappraisal for primates by using phylogenetic methods. Proceedings of the National Academy of Sciences, USA 91:9941-9945.
25. Dunbar RIM. 1996. Determinants of group size in primates: a general model. In: Maynard SJ, Runciman WG, Dunbar RIM, editors. Evolution of social behaviour patterns in primates and man. London: British Academy Press. p 33-57.
26. Eason P. 1981. Harpy eagle attempts predation on adult howler monkey. The Condor 91:469-470.
27. Ferreira RG, Izar P, Lee PC. 2006. Exchange, affiliation and protective interventions in semi-free ranging brown capuchin monkeys (Cebus apella). American Journal of Primatology 68:765-776.
28. Ferreira RG, Lee PC, Izar P. 2008. Food competition in a semi-free-ranging Cebus apella group. Folia Primatologica 79:463-475.
29. Fragaszy DM, Visalberghi E, Fedigan L, Rylands AB. 2004a. Taxonomy, distribution and conservation: where and what arethey, and how did they get there? In: Fragaszy D, Fedigan L, Visalberghi E, editors. The complete capuchin: the biology of the genus Cebus. Cambridge: Cambridge University Press. p 13-35.
30. Fragaszy DM, Visalberghi EM, Fedigan LM. 2004b. The complete capuchin: the biology of the genus Cebus. Cambridge: Cambridge University Press.
31. Fragaszy D, Izar P, Visalberghi E, Ottoni EB, de Oliveira MG. 2004c. Wild capuchin monkeys (Cebus libidinosus) use anvils and stone pounding tools. American Journal of Primatology 64:359-366.
32. Hill R, Dunbar RIM. 1998. An evaluation of the roles of predation rate and predation risk as selective pressures on primate grouping behaviour. Behaviour 135:411-430.
33. Hill RA, Lee PC. 1998. Predation risk as an influence on group size in cercopithecoid primates: Implications for social structure. Journal of Zoology, London 245:447-456.
34. Isbell LA. 1991. Contest and scramble competition: patterns of female aggression and ranging behaviour among primates. Behavioral Ecology 2:143-155.
35. Isbell LA. 2004. Is there no place like home? Ecological bases of female dispersal and philopatry and their consequences for the formation of kin groups. In: Chapais B, Berman C, editors. Kinship and behavior in primates. New York: Oxford University Press. p 71-108.
36. Isbell LA, Young TP. 2002. Ecological models of female social relationships in primates: similarities, disparities, and some directions for future clarity. Behaviour 139:177-202.
37. Isbell LA, Pruetz JD, Young TP. 1998. Movements of adult female vervets (Cercopithecus aethiops) and patas monkeys (Erythrocebus patas) as estimators of food resource size, density, and distribution. Behavioral Ecology and Sociobiology 42:123-133.
38. Izar P. 2002. Estratégias de forrageamento em Cebus apella. In: Albuquerque FS, editor. org Anais XX Encontro Anual de Etologia. Natal: UFRN. p 51-63.
39. Izar P. 2004. 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.
40. Izar P, Stone A, Carnegie SD, Nakai ES. 2009. Sexual selection, female choice and mating systems. In: Garber P, Estrada A, Bicca-Marques JC, Heymann E, Strier KB, editors. South American primates: testing new theories in the study of primate behavior, ecology, and conservation. New York: Springer Press. p 157-189.
41. Izawa K. 1980. Social behaviour of wild black-capped capuchin (Cebus apella). Primates 21:443-467.
42. Jack K, Fedigan LM. 2009. Female dispersal in a female-philopatric species, Cebus capucinus. Behaviour 146:471-497.
43. Janson CH. 1986. The mating system as a determinant of social evolution in capuchin monkeys (Cebus). In: Else J, Lee PC, editors. Primate ecology and conservation, Vol. 2. Cambridge: Cambridge University Press. p 169-180.
44. Janson CH. 1990. Social correlates of individual spatial choice in foraging groups of brown capuchin monkeys, Cebus apella. Animal Behaviour 40:910-921.
45. Janson CH. 2000. Primate socio-ecology: the end of a golden age. Evolutionary Anthropology 9:73-86.
46. Kappeler PM, van Schaik CP. 2002. Evolution of primate social systems. International Journal of Primatology 23:707-740.
47. Koenig A. 2000. Competitive regimes in forest-dwelling Hanuman langur females (Semnopithecus entellus). Behavioral Ecology and Sociobiology 48:93-109.
48. Koenig A, Borries MK, Chalise M, Winkler P. 1997. Ecology, nutrition, and timing of reproductive events in an Asian primate, the Hanuman langur (Presbytis entellus). Journal of Zoology, London 243:215-235.
49. Komers PE, Brotherton NM. 1997. Female space use is the best predictor of monogamy in mammals. Proceedings of the Royal Society of London, B. Biological Sciences 264:1261-1270.
50. Kutsukake N, Nunn C. 2006. Comparative tests of reproductive skew in male primates: the roles of demographic factors and incomplete control. Behavioral Ecology and Sociobiology 60:695-706.
51. Lee PC, Houser MD. 1998. Long-term consequences of changes in territory quality on feeding and reproductive strategies of vervet monkeys. Journal of Animal Ecology 67:347-358.
52. Lindenfors P, Froberg L, Nunn CL. 2004. Females drive primate social evolution. Proceedings of the Royal Society B: Biological Sciences 271:S101-S103.
53. Lynch-Alfaro JW. 2005. Male mating strategies and reproductive constraints in a group of wild tufted capuchin monkeys (Cebus apella nigritus). American Journal of Primatology 67: 313-328.
54. Lynch-Alfaro JW. 2007. Subgrouping patterns in a group of wild Cebus apella nigritus. International Journal of Primatology 28:271-289.
55. McGraw WS, Zuberbühler K. 2008. Socioecology, predation, and cognition in a community of West African monkeys. Evolutionary Anthropology 17:254-266.
56. Nunn CL, van Schaik CP. 2000. Social evolution in primates: the relative roles of ecology and intersexual conflict. In: van Schaik CP, Janson CH, editors. Infanticide by males and its implications. Cambridge: Cambridge University Press. p 388-412.
57. O'Brien TG, Robinson JG. 1991. Allomaternal care by female wedge-capped capuchin monkeys: effects of age, rank and relatedness. Behaviour 119:31-50.
58. Oliveira MM, Langguth A. 2006. Rediscovery of Marcgrave's capuchin monkey and designation of a neotype for Simia flavia Schreber 1774 (Primates, Cebidae). Boletim do Museu Nacional, Rio de Janeiro: Zoologia 523:1-16.
59. Oliveira VB, Linares AM, Corrêa GLC, Chiarello AG. 2008. Predation on the black capuchin monkey Cebus nigritus (Primates: Cebidae) by domestic dogs Canis lupus familiaris (Carnivora: Canidae) in the Parque Estadual Serra do Brigadeiro, Minas Gerais, Brazil. Revista Brasileira de Zoologia 25:376-378.
60. Ostner J, Nunn CL, Schülke O. 2008. Female reproductive synchrony predicts skewed paternity across primates. Behavioral Ecology 19:1150-1158.
61. Pazol K, Cords M. 2005. Seasonal variation in feeding behavior, competition and female social relationships in a forest dwelling guenon, the blue monkey (Cercopithecus mitis stuhlmanni), in the Kakamega Forest, Kenya. Behavioral Ecology and Sociobiology 58:566-577.
62. Perry S. 1996. Female-female relationships in wild white-faced capuchin monkeys, Cebus capucinus. American Journal of Primatology 40:167-182.
63. Pinha OS. 2007. Interações sociais em grupos de macacos-prego (Cebus libidinosus) no Parque Nacional de Brasília. Master Thesis, Universidade de Brasília, Brazil.
64. Pope TR. 2000. Reproductive success increases with degree of kinship in cooperative coalitions of female red howler monkeys (Alouatta seniculus). Behavioral Ecology and Sociobiology 48:253-267.
65. Presotto A, Izar P. 2010. Spatial reference of black capuchin monkeys in Brazilian Atlantic Forest: egocentric or allocentric? Animal Behaviour 80:125-132.
66. Rasoloarison RM, Rasolonandrasana B, Ganzhorn JU, Goodman SM. 1995. Predation on vertebrates in the Kirindy forest, Western Madagascar. Ecotropica 1:59-65.
67. Rendall D, Di Fiore AF. 2007. Homoplasy, homology, and the perceived special status of behavior in evolution. Journal of Human Evolution 52:504-521.
68. Rímoli J, Strier KB, Ferrari SF. 2008. Seasonal and longitudinal variation in the behavior of free-ranging black tufted capuchins Cebus nigritus (Goldfuss, 1809) in a fragment of Atlantic Forest in Southeastern Brazil. In: Ferrari SF, Rímoli J, editors. A Primatologia no Brasil 9. Aracaju: Sociedade Brasileira de Primatologia, Biologia Geral e Experimental-UFS. p 130-146.
69. Robbins AM, Stoinski TS, Fawcett KA, Robbins MM. 2009. Leave or conceive: natal dispersal and philopatry of female mountain gorillas in the Virunga volcano region. Animal Behaviour 77:831-838.
70. Ryan SJ, Starks PT, Milton K, Getz WM. 2008. Intersexual conflict and group size in mantled howler monkeys: a 23- year evaluation. International Journal of Primatology 29:405-420.
71. Sabbatini G, Stammati M, Tavares MCH, Visalberghi E. 2008. Behavioural flexibility of a group of capuchin monkeys (Cebus libidinosus) in the National Park of Brasília (Brazil): consequences of cohabitation with visitors. Brazilian Journal of Biology 68:685-693.
72. Saito C. 1996. Dominance and feeding success in female Japanese macaques, Macaca fuscata: effects of food patch size and inter-patch distance. Animal Behaviour 51:967-980.
73. Sih A, Bell AM, Johnson JC, Ziemba RE. 2004. Behavioral syndromes: an integrative overview. The Quarterly Review of Biology 79:241-277.
74. Silva Jr JS. 2001. Especiação nos macacos-prego e caiararas, gênero Cebus Erxleben, 1777 (Primates, Cebidae). Doctoral Thesis, Rio de Janeiro, Universidade Federal do Rio de Janeiro. 377p.
75. Snaith TV, Chapman CA. 2007. Primate group size and socioecological models: do folivores really play by different rules? Evolutionary Anthropology 16:94-106.
76. Spironello WR. 2001. The brown capuchin monkey (Cebus apella). Ecology and home range requirements in Central Amazonia. In: Bierregaard Jr RO, Gascon C, Lovejoy TE, Mesquita R, editors. Lessons from Amazonia: the ecology and conservation of a fragmented forest. New Haven & London: Yale University Press. p 271-283.
77. Stanford CB. 2002. Avoiding predators: expectations and evidence in primate antipredator behavior. International Journal of Primatology 23:741-757.
78. Sterck EHM. 1999.Variation in langur social organization in relation to the socioecological model, human habitat alteration, and phylogenetic constraints. Primates 40:199-213.
79. Sterck EHM, Watts DP, van Schaik CP. 1997. The evolution of female social relationships in nonhuman primates. Behavioral Ecology and Sociobiology 41:291-310.
80. Strier KB. 1989. Effects of patch size on feeding associations in muriquis (Brachyteles arachnoides). Folia Primatologica 52:70-77.
81. Strier KB. 1994. Myth of the typical primate. Yearbk Phys Anthropol 37:233-271.
82. Strier KB. 2003. Primate behavioral ecology: from ethnography to ethology and back. Am Anthropol 105:16-27.
83. Strier KB. 2009. Seeing the forest through the seeds: mechanisms of primate behavioral diversity from individuals to populations and beyond. Current Anthropology 50:213-228.
84. Taira JT. 2007. Consumo do palmito juçara (Euterpe edulis) por macacos-prego (Cebus nigritus): estratégia de forrageamento ótimo ou requinte de um gourmet? Master Thesis, Universidade de São Paulo, Brazil.
85. Teichroeb JE, Sicotte P. 2008. Test of the ecological-constraints model on ursine colobus monkeys (Colobus vellerosus) in Ghana. American Journal of Primatology 71:49-59.
86. Terborgh J. 1983. Five new world primates. A study in comparative ecology. Princeton, NJ: Princeton University Press.
87. Thierry B. 2008. Primate socioecology, the lost dream of ecological determinism. Evolutionary Anthropology 17:93-96.
88. Trivers RL. 1972. Parental investment and sexual selection. In: Campbell B, editor. Sexual selection and the descent of man. Chicago: Aldine. p 136-179.
89. van Belle S, Estrada A. 2008. Group size and composition influence male and female reproductive success in black howler monkeys (Alouatta pigra). American Journal of Primatology 70:613-619.
90. van Schaik CP. 1983. Why are diurnal primates living in groups? Behaviour 87:120-144.
91. van Schaik CP. 1989. The ecology of social relationships amongst female primates. In: Standen V, Foley RA, editors. Comparative socioecology, Oxford: Blackwell. p 195-218.
92. van Schaik CP, Hörstermann M. 1994. Predation risk and the number of adult males in a primate group: a comparative test. Behavioral Ecology and Sociobiology 35:261-272.
93. Visalberghi E, Fragaszy D, Izar P, Ottoni EB. 2005. Terrestriality and tool use. Science 308:951-952.
94. Visalberghi E, Fragaszy D, Ottoni EB, Izar P, Oliveira MG, Andrade FRD. 2007. Characteristics of hammer stones and anvils used by wild bearded capuchin monkeys (Cebus libidinosus) to crack open palm nuts. American Journal of Physical Anthropology 132:426-444.
95. Vogel ER, Janson C. 2007. Predicting the frequency of food-related agonism in white faced capuchin monkeys (Cebus capucinus) using a novel focal-tree method. American Journal of Primatology 69:533-550.
96. Wrangham RW. 1980. An ecological model of female-bonded primate groups. Behaviour 75:262-300.
97. Zhang S. 1995. Activity and ranging patterns in relation to fruit utilization by brown capuchin monkeys (Cebus apella) in French Guiana. International Journal of Primatology 16:489-507.
98. Ziegler TE, Santos CV, Pissinatti A, Strier KB. 1997. Steroid excretion during the ovarian cycle in captive and wild muriquis, Brachyteles arachnoides. American Journal of Primatology 42:311-321.