Skip to main content Accessibility help
×
Home
  • Get access
    Check if you have access via personal or institutional login
  • Cited by 20
  • Print publication year: 2008
  • Online publication date: May 2010

11 - Immaturity in spider monkeys: a risky business

Summary

Introduction

Socialization is an important and complicated process in primates, involving morphological, ecological and social factors, which together serve to channel individuals into age- and gender-specific roles that help determine the population biology of each species. Despite its extreme importance, however, the socialization process has received little attention relative to primatological studies of adult nonhuman primates. Most studies have focused chiefly on social structure, as mediated by adults through dominance or affiliative interactions; mating strategies and their function in mediating the reproductive success of the mature individuals utilizing them; and socioecology, again primarily examining male and female adults' differential need for and utilization of resources and the resultant impact on social structure. This chapter investigates immature spider monkeys, that is, individuals from birth until emigration or attainment of social adulthood. The chapter focuses mainly on the Yucatecan spider monkey, Ateles geoffroyi, a relatively monomorphic and large-brained cebid with a complex social organization and social roles clearly differentiated by gender. Socialization and the immature phase in these spider monkeys will be considered in the broader context of the adult roles they will eventually exhibit and with regard to what is known about immaturity in primates in general.

Background

Much of the data available on immatures is based on infancy and parent–offspring relationships (usually mother–infant) (Gubernick and Klopfer, 1981; Taub, 1984), starting with and building on Harlow's pioneering work (Harlow, 1959; Harlow and Zimmermann, 1959; Harlow, 1971) on attachment and the role of maternal attributes in infant development.

Related content

Powered by UNSILO
References
Ahumada, J. A. (1992). Grooming behavior of spider monkeys (Ateles geoffroyi) on Barro Colorado Island, Panama.Int. J. Primatol., 13, 39–49.
Alexander, R. D. (1974). The evolution of social behavior.Annu. Rev. Ecol. Syst., 5, 325–383.
Allman, J., McLaughlin, T. and Hakeem, A. (1993). Brain weight and life-span in primates.Proc. Natl. Acad. Sci. USA, 90, 118–122.
Altmann, J. (1974). Observational study of behavior: sampling methods.Behaviour, 49, 227–267.
Armstrong, E. (1983). Relative brain size and metabolism in mammals.Science, 220, 1302–1304.
Balau, J. and Redmond, D. E. Jr. (1978). Some sampling considerations in the quantification of monkey behavior under field and captive conditions.Primates, 19, 391–400.
Baldwin, J. D. and Baldwin, J. I. (1974). Exploration and social play in squirrel monkeys (Saimiri).Am. Zool., 14, 303–315.
Boinski, S. (1988). Sex differences in the foraging behavior of squirrel monkeys in a seasonal habital.Behav. Ecol. Sociobiol., 23, 177–186.
Campbell, C. J. (2000). The reproductive biology of black-handed spider monkeys (Ateles geoffroyi): integrating behavior and endocrinology. Unpublished Ph.D. thesis, University of California, Berkeley.
Campbell, C. J. (2003). Female directed aggression in free-ranging Ateles geoffroyi.Int. J. Primatol., 24, 223–238.
Campbell, C. J. (2006a). Copulation in free-ranging black-handed spider monkeys (Ateles geoffroyi).Am. J. Primatol., 68, 507–511.
Campbell, C. J. (2006b). Lethal intragroup aggression by adult male spider monkeys (Ateles geoffroyi).Am. J. Primatol., 68, 1197–1201.
Campbell, C. J., Aureli, F., Chapman, C. A.et al. (2005). Terrestrial behavior of Ateles spp. Int. J. Primatol., 26, 1039–1051.
Cant, J. (1978). Population survey of the spider monkey Ateles geoffroyi at Tikal, Guatemala.Primates, 19, 525–535.
Carpenter, C. R. (1935). Behavior of red spider monkeys in Panama.J. Mammal., 16, 171–180.
Chapman, C. A. (1990). Association patterns of spider monkeys: the influence of ecology and sex on social organization.Behav. Ecol. Sociobiol., 26, 409–414.
Chapman, C. A. and Chapman, L. J. (1987 ). Social responses to the traumatic injury of a juvenile spider monkey (Ateles geoffroyi).Primates, 28, 271–275.
Chapman, C. A. and Chapman, L. J. (1990). Reproductive biology of captive and free-ranging spider monkeys.Zoo Biology, 9, 1–9.
Chapman, C. A., Fedigan, L. M., Fedigan, L. and Chapman, L. J. (1989). Post-weaning resource competition and sex ratios in spider monkeys.Oikos, 54, 315–319.
Chapman, C. A., Wrangham, R. W. and Chapman, L. J. (1995). Ecological constraints on group size: an analysis of spider monkey and chimpanzee subgroups.Behav. Ecol. Sociobiol., 36, 59–70.
Charnov, E. and Berrigan, D. (1993). Why do female primates have such long life spans and so few babies? Or life in the slow lane.Evol. Anthropol., 2, 191–194.
Cheney, D. (1977). The acquisition of rank and the development of reciprocal alliances among free-ranging immature baboons.Behav. Ecol. Sociobiol., 2, 303–318.
Cheney, D. (1978a). Interactions of immature male and female baboons with adult females.Anim. Behav., 26, 389–408.
Cheney, D. L. (1978b). The play partners of immature baboons.Anim. Behav., 26, 1038–1050.
Clark, A. B. (1978 ). Sex ratio and local resource competition in a prosimian primate.Science, 201, 163–165.
Clark, C. B. (1977). A preliminary report on weaning among chimpanzees of the Gombe National Park, Tanzania. In Primate Biosocial Development, ed. Chevalier-Skolnikoff, S. and Poirier, F. E., New York: Garland, pp. 235–260.
Clutton-Brock, T. H. and Harvey, P. H. (1977). Primate ecology and social organization.J. Zool, 183, 1–39.
Coehlo, A. M. Jr., Bramblett, C. A., Quick, L. B. and Bramblett, S. S. (1976). Resource availablity and population density in primates: a sociobioenergetic analysis of the energy budgets of Guatemalan howler and spider monkeys.Primates, 17, 63–80.
Crockett, C. M. and Janson, C. H. (2000). Infanticide in red howlers: female group size, male membership, and a possible link to folivory. In Infanticide by Males and its Implications, ed. Schaik, C. P. and Janson, C. H., Cambridge: Cambridge University Press, pp. 75–98.
Crook, J. H. (1972). Sexual selection, dimorphism, and social organization in the primates. In Sexual Selection and the Descent of Man, 1871–1971, ed. Campbell, B. G., Chicago: Aldine, pp. 231–281.
Deaner, R. O., Barton, R. A. and van Schaik, C. P. (2003). Primate brains and life histories: renewing the connection. In Primate Life Histories and Socioecology, ed. Kappeler, P. and Pereira, M., Chicago: University of Chicago Press, pp. 233–265.
Eisenberg, J. F. (1973). Reproduction in two species of spider monkeys, Ateles fusciceps and Ateles geoffroyi.J. Mammal., 54, 955–957.
Eisenberg, J. F. (1976). Communication mechanisms and social integration in the black spider monkey, Ateles fusciceps robustus and related species.Smithson. Contrib. Zool., 213, 1–108.
Epple, G. (1975). Parental care in Saguinus fuscicollis spp. (Callithricidae). Folia Primatol., 24, 221–238.
Fairbanks, L. A. (1993). Juvenile vervet monkeys: establishing relationships and practicing skills for the future. In Juvenile Primates: Life History, Development and Behavior, ed. Pereira, M. E. and Fairbanks, L. A., Oxford: Oxford University Press, pp. 211–227.
Fairbanks, L. A. (2000). The developmental timing of primate play: a neural selection model. In Biology, Brains, and Behavior: The Evolution of Human Development, ed. Parker, S. T., Langer, J. and McKinney, M. L., Santa Fe, CA: School of American Research Press, pp. 131–158.
Fedigan, L. M. and Baxter, M. J. (1984). Sex differences and social organization in free-ranging spider monkeys (Ateles geoffroyi).Primates, 25, 279–294.
Fruth, B., Hohmann, G. and McGrew, W. C. (1999). The Pan species. In The Nonhuman Primates, ed. Dolhinow, P. and Fuentes, A., Mayfield, CA: Mayfield Publishing Company, pp. 64–72.
Goldizen, A. W. (1987). Tamarins and marmosets: communal care of offspring. In Primate Societies, ed. Smuts, B. B., Cheney, D. L., Seyfarth, R. M., Wrangham, R. W. and Struhsaker, T. T., Chicago: University of Chicago Press, pp. 34–43.
Gonzalez-Kirchner, J. P. (1999). Habitat use, population density and subgrouping pattern of the Yucatan spider monkey (Ateles geoffroyi yucatanensis) in Quintana Roo, Mexico.Folia Primatol., 70, 55–60.
Goodall, J. (1968). The behaviour of free-living chimpanzees in the Gombe Stream Reserve.Anim. Behav. Monogr., 1, 161–311.
Goodall, J. (1971). In the Shadow of Man. London: Collins.
Goodall, J. (1983). Population dynamics during a 15 year period in one community of free-living chimpanzees in the Gombe National Park, Tanzania.Z. Tierpsychol., 61, 1–60.
Goodall, J. (1986). The Chimpanzees of Gombe: Patterns of Behavior. Cambridge, MA: Belknap Press.
Gubernick, D. J. and Klopfer, P. H., eds. (1981). Parental Care in Mammals. New York: Plenum Press.
Harcourt, A. H. and Stewart, K. J. (1981). Gorilla male relationships: can differences during immaturity lead to contrasting reproductive tactics in adulthood?Anim. Behav., 29, 206–210.
Harlow, H. F. (1959). Love in infant monkeys.Sci. Am., 200, 68–74.
Harlow, H. F. (1971). Learning to Love. New York: Ballentine Books.
Harlow, H. F. and Zimmermann, R. R. (1959). Affectional responses in the infant monkey.Science, 130, 421–432.
Harvey, P. H., Martin, R. D. and Clutton-Brock, T. H. (1987). Life histories in comparative perspective. In Primate Societies, ed. Smuts, B. B., Cheney, D. L., Seyfarth, R. M., Wrangham, R. W. and Struhsaker, T. T., Chicago: University of Chicago Press, pp. 181–196.
Harvey, P. H., Read, A. F. and Promislow, D. E. L. (1989). Life history variation in placental mammals: unifying the data with theory.Oxford Surv. Evol. Biol., 6, 13–31.
Hayaki, H. (1983). The social interactions of juvenile Japanese monkeys on Koshima islet.Primates, 24, 139–153.
Hoage, R. J. (1978). Parental care in Leontopithecus rosalia rosalia: sex and age differences in carrying behavior and the role of prior experience. In The Biology and Conservation of the Callitrichidae, ed. Kleiman, D. G., Washington, DC: Smithsonian Institution Press, pp. 293–305.
Izawa, K., Kimura, K. and Nieto, A. S. (1979). Grouping of the wild spider monkey.Primates, 20, 503–512.
Janson, C. H. (1990). Ecological consequences of individual spatial choice in foraging groups of brown capuchin monkeys, Cebus apella.Anim. Behav., 40, 922–934.
Janson, C. H. and van Schaik, C. P. (1993). Ecological risk aversion in juvenile primates: slow and steady wins the race. In Juvenile Primates: Life History, Development, and Behavior, ed. Pereira, M. and Fairbanks, L. A., New York: Oxford University Press, pp. 57–74.
Klein, L. L. and Klein, D. B. (1977). Feeding behaviour of the Colombian spider monkey. In Primate Ecology: Studies of Feeding and Ranging Behavior in Lemurs, Monkeys and Apes, ed. Clutton-Brock, T. H., London: Academic Press, pp. 153–182.
Kraemer, H. C., Horvat, J. R., Doering, C. and McGinnis, P. R. (1982). Male chimpanzee development focusing on adolescence: integration of behavioral with physiological changes.Primates, 23, 393–405.
Lee, P. C. (1984). Ecological constraints on the social development of vervet monkeys.Behaviour, 91, 245–262.
Macedonia, J. M. (1991). Vocal communication and anti-predator behavior in the ring-tailed lemur (Lemur catta) with a comparison to the ruffed lemur (Varecia variagatta). Unpublished Ph.D. thesis, Duke University, Durham, NC.
Martin, P. and Caro, T. (1985). On the functions of play and its role in behavioral development. In Advances in the Study of Behavior, ed. Rosenblatt, J. S., Beer, C., Busnel, M. C. and Slater, P. J. B., Orlando, FL: Academic Press, pp. 59–103.
Martin, R. D. (1996). Scaling of the mammalian brain: the maternal energy hypothesis.News Physiol. Sci., 11, 149–156.
McDaniel, P. S. (1994). The social behavior and ecology of the black-handed spider monkey (Ateles geoffroyi). Unpublished Ph.D. thesis, Saint Louis University, St. Louis, MO.
Meaney, M. J., Stewart, J. and Beatty, W. W. (1985). Sex differences in social play: the socialization of sex roles. In Advances in the Study of Behavior, ed. Rosenblatt, J. S., Beer, C., Busnel, M. C. and Slater, P. J. B., Orlando, FL: Academic Press, pp. 2–58.
Milton, K. (1981). Estimates of reproductive parameters for free-ranging Ateles geoffroyi.Primates, 22, 574–579.
Milton, K. (1993). Diet and social organization of a free-ranging spider monkey population: the development of species-typical behavior in the absence of adults. In Juvenile Primates: Life History, Development, and Behavior, ed. M. E. Pereira and L. A. Fairbanks, New York: Oxford University Press, pp. 173–181.
Milton, K. and Hopkins, M. E. (2005). Growth of a reintroduced spider monkey (Ateles geoffroyi) population on Barro Colorado Island, Panama. In New Perspectives in the Study of Mesoamerican Primates, ed. Estrada, A., Garber, P. A., M. Pavelka, and Luecke, L., New York: Springer Verlag, pp. 417–435.
Nishida, T. and Kawanaka, K. (1985). Within-group cannibalism by adult male chimpanzees.Primates, 26, 247–284.
Nunes, A. and Chapman, C. A. (1995). A re-evaluation of factors influencing the sex ratio of spider monkey populations with new data from Maraca Island, Brazil.Folia Primatol., 68, 31–33.
Pagel, M. and Harvey, P. H. (1993). Evolution of the juvenile period in mammals. In Juvenile Primates: Life History, Development and Behavior, ed. Pereira, M. E. and Fairbanks, L. A., New York: Oxford University Press, pp. 28–37.
Pereira, M. (1984). Age changes and sex differences in the social behavior of juvenile yellow baboons (Papio cynocephalus). Unpublished Ph.D. thesis, University of Chicago, Chicago, IL.
Pereira, M. E. (1988a). Effects of age and sex on intra-group spacing behaviour in juvenile savannah baboons, Papio cynocephalus cynocephalus.Anim. Behav., 36, 184–204.
Pereira, M. E. (1988b). Agonistic interactions of juvenile savanna baboons. I. Fundamental features. Ethology, 79, 195–217.
Pereira, M. E. (1989). Agonistic interactions of juvenile savanna baboons. II. Agonistic support and rank acquisition. Ethology, 80, 152–171.
Pereira, M. E. (1995). Development and social dominance among group-living primates.Am. J. Primatol., 37, 143–175.
Pereira, M. E. and Altmann, J. (1985). Development of social behavior in free-living nonhuman primates. In Nonhuman Primate Models for Human Growth and Development, ed. Watts, E. S., New York: Alan R. Liss, pp. 217–309.
Pereira, M. E. and Fairbanks, L. A., eds. (1993a). Juvenile Primates: Life History, Development, and Behavior. New York: Oxford University Press.
Pereira, M. E. and Fairbanks, L. A. (1993b). What are juvenile primates all about? In Juvenile Primates: Life History, Development and Behavior, ed. Pereira, M. E. and Fairbanks, L. A., New York: Oxford University Press, pp. 3–12.
Pereira, M. E. and Leigh, S. R. (2003). Modes of primate development. In Primate Life Histories and Socioecology, ed. Kappeler, P. M. and Pereira, M. E., Chicago: University of Chicago Press, pp. 149–176.
Poirier, F. E. and Smith, E. O. (1974). Socializing functions of primate play.Am. Zool., 14, 275–287.
Pusey, A. E. (1983). Mother-offspring relationships in chimpanzees after weaning.Anim. Behav., 31, 363–377.
Pusey, A. E. (1990). Behavioral changes at adolescence in chimpanzees.Behaviour, 115, 203–245.
Ramos-Fernández, G. (2001). Patterns of association, feeding competition and vocal communication in spider monkeys, Ateles geoffroyi. Unpublished Ph.D. thesis, University of Pennsylvania, Philadelphia.
Ramos-Fernández, G. and Ayala-Orozco, B. (2003). Population size and habitat use of spider monkeys in Punta Laguna, Mexico. In Primates in Fragments: Ecology and Conservation, ed. Marsh, L. K., New York: Kluwer, pp. 191–210.
Ramos-Fernández, G., Ayala-Orozco, B., Bonilla-Moheno, M. and Garcia-Frapolli, E. (2005). Conservación comunitaria en Punta Laguna: fortalecimiento de instituciones locales para el desarollo sostenible. Congreso “Casos exitosos de desarollo sostenible del Tropico”, Vera Cruz, Mexico.
Ramos-Fernández, G., Vick, L. G., Aureli, F., Schaffner, C. M. and Taub, D. M. (2003). Behavioral ecology and conservation status of spider monkeys in the Otoch Ma'ax Yetel Kooh Protected Area.Neotrop. Primates, 11, 155–158.
Rhine, R. J. (1975). The order of movement of yellow baboons (Papio cynocephalus).Folia Primatol., 23, 73–104.
Robinson, J. G. (1981). Spatial structure in foraging groups of wedge-capped capuchin monkeys Cebus nigrivittatus.Anim. Behav., 29, 1036–1056.
Ross, C. and Jones, K. E. (1999). Socioecology and the evolution of primate reproductive rates. In Comparative Primate Socioecology, ed. Lee, P. C., Cambridge: Cambridge University Press, pp. 73–110.
Sacher, G. A. (1975). Maturation and longevity in relation to cranial capacity in hominid evolution. In Primate Functional Morphology and Evolution, ed. Tuttle, R. H., The Hague: Mouton, pp. 417–441.
Sacher, G. and Staffeldt, E. (1974). Relation of gestation time to brain weight for placental mammals: implication for the theory of vertebrate growth.Am. Nat., 108, 593–615.
Seyfarth, R. M. and Cheney, D. L. (1980). The ontogeny of vervet monkey alarm-calling behaviour: a preliminary report.Z. Tierpsychol., 54, 37–56.
Seyfarth, R. M. and Cheney, D. L. (1986). Vocal development in vervet monkeys.Anim. Behav., 24, 1450–1468.
Shimooka, Y. (2003). Seasonal variation in association patterns of wild spider monkeys (Ateles belzebuth belzebuth) at La Macarena, Colombia.Primates, 44, 83–90.
Silk, J. B. (1983). Local resource competition and facultative adjustment of sex ratio in relation to competitve abilities.Am. Nat., 121, 56–66.
Silk, J. B., Samuels, A. and Rodman, P. S. (1981). The influence of kinship, rank, and sex on affiliation and aggression between adult female and immature bonnet macaques (Macaca radiata).Behaviour, 78, 111–137.
Smith, E. O. (1978). Social Play in Primates. New York: Academic Press.
Stanford, C. (1995). The influence of chimpanzee predation on group size and anti-predator behaviour in red colobus monkeys.Anim. Behav., 49, 577–587.
Stanford, C. B., Wallis, J.Matama, H. and Goodall, J. (1994). Patterns of predation by chimpanzees on red colobus monkeys in Gombe National Park, Tanzania, 1982–1991.Am. J. Phys. Anthropol., 94, 213–228.
Symington, M. M. (1987). Sex ratio and maternal rank in wild spider monkeys: when daughters disperse.Behav. Ecol. Sociobiol., 20, 421–425.
Symington, M. M. (1988). Food competition and foraging party size in the black spider monkey (Ateles paniscus chamek).Behaviour, 105, 117–134.
Symington, M. M. (1990). Fission-fusion social organization in Ateles and Pan.Int. J. Primatol., 11, 47–61.
Taub, D. M. (1984). Male caretaking behaviour among wild Barbary macaques (Macaca sylvanus). In Primate Paternalism, ed. Taub, D. M., New York: Van Nostrand Reinhold, pp. 20–55.
Terborgh, J. W. (1983). Five New World Primates: A Study in Comparative Ecology. Princeton, NJ: Princeton University Press.
Terborgh, J. W. and Janson, C. H. (1986). The socioecology of primate groups.Annu. Rev. Ecol. Syst., 17, 111–135.
Valero, A., Schaffner, C. M., Vick, L. G., Aureli, F. and Ramos-Fernández, G. (2006). Intragroup lethal aggression in wild spider monkeys.Am. J. Primatol., 68, 732–737.
Roosmalen, M. G. M. (1985). Habitat preferences, diet, feeding strategy and social organization of the black spider monkey (Ateles paniscus paniscus Linnaeus 1758) in Surinam.Acta Amazonica, 15, 3–238.
van Roosmalen, M. G. M. and Klein, L. L. (1988). The spider monkeys, genus Ateles. In Ecology and Behaviour of Neotropical Primates, Vol. 2, ed. Mittermeier, R. A., Rylands, A. B., Coimbra-Filho, A. F. and Fonseca, G. A. B., Washington, DC: World Wildlife Fund, pp. 455–537.
Schaik, C. P. (1983). Why are diurnal primates living in groups?Behaviour, 87, 120–144.
Schaik, C. P. and Janson, C. H. (2000). Infanticide by Males and Its Implications. Cambridge: Cambridge University Press.
Schaik, C. P. and Noordwijk, M. A. (1985). Evolutionary effect of the absence of felids on the social organization of the macaques on the island of Simeulue (Macaca fascicularis fusca, Miller 1903).Folia Primatol., 44, 138–147.
Schaik, C. P. and Noordwijk, M. A. (1989). The special role of male Cebus monkeys in predation avoidance and its effect on group composition.Behav. Ecol. Sociobiol., 24, 265–276.
Vick, L. G. and Taub, D. M. (1995). Ecology and behavior of spider monkeys (Ateles geoffroyi) at Punta Laguna, Mexico.Am. J. Primatol., 36, 160.
Vick, L. G., Ramos-Fernández, G. and Taub, D. M. (2001). El infanticidio en los monos aranas (Ateles geoffroyi yucatanensis) en Punta Laguna, Mexico. 1er Congreso mexicano de Primatología, Mérida, México, September, 2001.
Walters, J. R. (1981). Inferring kinship from behaviour: maternity determinations in yellow baboons.Anim. Behav., 29, 126–136.
Walters, J. R. (1987). Transition to adulthood. In Primate Societies, ed. Smuts, B. B., Cheney, D. L., Seyfarth, R. M., Wrangham, R. W. and Struhsaker, T. T., Chicago: Chicago University Press, pp. 358–369.