Abstract
Several studies show that primates exhibit coping strategies to buffer the effect of increased social tension under crowded conditions. This is the first study to assess the effect of crowding on the social behavior of a cooperative breeding primate. We studied the effect of repeated short-term crowding on the social behavior of 20 cotton-top tamarins (10 breeders, 10 adult–subadult offspring) belonging to 2 large and 3 small groups. We compared scratching and rates of social behavior between 2 conditions: large-outdoor (42.0 m2 × 3.3 m) and small-indoor (3.5 m2 × 2.2 m) enclosures. Our results indicate that scratching increases in breeders and offspring during crowding. However, whereas the social behavior of breeders in small groups was not affected by crowding, breeders in large groups (n = 4) showed increased rates of severe aggression with their offspring during crowding. Offspring of large groups showed a nonsignificant trend to increase mild aggression, and an increased percentage of time in contact and grooming during crowding. This augmentation of grooming occurred in offspring–breeder dyads and also between offspring. These results suggest that helpers from large groups use coping strategies when social tension increases.
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References
Aureli, F., & de Waal, F. B. M. (1997). Inhibition social behavior in chimpanzees under high density conditions. American Journal of Primatology, 41, 213–228.
Aureli, F., & Schaffner, C. M. (2006). Causes, consequences and mechanisms reconciliation. In P. M. Kappeler & C. P. van Schaik (Eds.), Cooperation in primates and humans mechanisms and evolution (pp. 121–136). Berlin: Springer.
Aureli, F., van Panthaleon van Eck, C. J., & Veenema, H. C. (1995). Long-tailed macaques avoid conflicts during short-term crowding. Aggressive Behaviour, 21, 113–122.
Aureli, F., Preston, S. D., & de Waal, F. B. M. (1999). Heart rate responses to social interactions in free-moving rhesus macaques (Macaca mulatta): a pilot study. Journal of Comparative Psychology, 113, 59–65.
Baker, K., & Aureli, F. (1997). Behavioral indicators anxiety: an empirical test in chimpanzees. Behaviour, 134, 1031–105.
Boccia, M. L., Reite, M., & Laudenslager, M. (1989). On the physiology grooming in a pigtail macaque. Physiological Behaviour, 45, 667–670.
Brown, G. M., Schalch, D. S., & Reichlin, S. (1971). Patterns of growth hormone and cortisol responses to psychological stress in the squirrel monkey. Endocrinology, 88, 956–963.
Caine, N. G. (1993). Flexibility and co-operation as unifying themes in Saguinus social organization and behavior: The role predation pressure. In A. B. Rylands (Ed.), Marmosets and tamarins: Systematics, behaviour, and ecology (pp. 200–219). Oxford: Oxford University Press.
Calhoun, J. B. (1962). Population density and social pathology. Scientific American, 206, 139–148.
Cilia, J., & Piper, D. C. (1997). Marmoset conspecific confrontation: an ethologically-based model anxiety. Pharmacology, Biochemistry, and Behavior, 58, 85–91.
de Filippis, B., Chiarotti, F., & Vitale, A. (2009). Severe intragroup aggression in captive common marmosets (Callithrix jacchus). Journal of Applied Animal Welfare Science, 12, 214–222.
de Waal, F. B. M. (1989). The myth a simple relation between space and aggression in captive primates. Zoo Biology, 1(Supplement), 141–148.
Digby, L. J., Ferrari, S. F., & Saltzman, W. (2007). Callitrichines: The role of competition in cooperatively breeding species. In C. J. Campbell, A. Fuentes, K. C. MacKinnon, M. Panger, & S. K. Bearder (Eds.), Primates in perspective (pp. 85–106). New York: Oxford University Press.
Ginther, A. J., & Snowdon, C. T. (2009). Expectant parents groom adult sons according to previous alloparenting in a biparental cooperatively breeding primate. Animal Behaviour, 78, 287–297.
Ginther, A. J., Ziegler, T. E., & Snowdon, C. T. (2001). Reproductive biology of captive male cotton top tamarin monkeys as a function of social environment. Animal Behavior, 61, 65–78.
Honess, P. E., & Marin, C. M. (2006). Behavioural and physiological aspects of stress and aggression in nonhuman primates. Neuroscience Biobehavioral Review, 30, 390–412.
Huck, M., Löttker, P., Böehle, U. R., & Heymann, E. W. (2005). Paternity and kinship patterns in polyandrous moustached tamarins (Saguinus myxtax). American Journal of Physical Anthropology, 127, 449–464.
Inglett, B. J., French, J. A., Simmons, L. G., & Vires, K. W. (1989). Dynamics intrafamily aggression and social reintegration in lion tamarins. Zoo Biology, 8, 67–78.
Johnson, L. D., Petto, A. J., & Sehgal, P. K. (1991). Factors in rejection and survival captive cotton-top tamarins (Saguinus oedipus). American Journal of Primatology, 25, 91–102.
Judge, P. G. (2000). Coping with crowding conditions. In F. Aureli & F. B. M. de Waal (Eds.), Natural conflict resolution (pp. 129–154). Berkeley, CA: University of California Press.
Judge, P. G., & de Waal, F. B. M. (1993). Conflict avoidance among rhesus monkeys: coping with short-term crowding. Animal Behaviour, 46, 221–232.
Judge, P. G., & de Waal, F. B. M. (1997). Rhesus monkey behaviour under diverse population densities: coping with long-term crowding. Animal Behaviour, 54, 643–662.
Judge, P. G., Griffaton, N. S., & Fincke, A. M. (2006). Conflict management by hamadryas baboons (Papio hamadryas hamadryas) during crowding: a tension-reduction strategy. American Journal of Primatology, 68, 993–1006.
Koyama, N., & Palagi, E. (2006). Managing conflict: evidence from wild and captive primates. International Journal of Primatology, 27, 1235–1240.
Lázaro-Perea, C., Arruda, M. F., & Snowdon, C. T. (2004). Grooming as a reward? Social function of grooming between females in cooperatively breeding marmosets. Animal Behavior, 67, 627–636.
Löttker, P., Huck, M., Zinner, D. P., & Heymann, E. W. (2007). Grooming relationships between breeding females and adult group members in cooperatively breeding moustached tamarins (Saguinus mystax). American Journal of Primatology, 69, 1–14.
Martin, P., & Bateson, P. (1986). Measuring behaviour: An introductory guide. Cambridge, UK: Cambridge University Press.
McGrew, W. C., & McLuckie, E. C. (1986). Philopatry and dispersion in the cotton top tamarin, Saguinus oedipus oedipus: An attempted laboratory simulation. International Journal of Primatology, 7, 401–422.
Moura, A. C. A. (2003). Sibling age and intragroup aggression in cautive Saguinus midas midas. International Journal of Primatology, 24, 639–652.
Nash, L. T., & Chilton, S. (1986). Space or novelty? Effects of altered cage size on galago behavior. American Journal of Primatology, 10, 37–50.
Nieuwenhuijsen, K., & de Waal, F. B. M. (1982). Effects spatial crowding on social behavior in a chimpanzee colony. Zoo Biology, 1, 5–28.
Novak, M. A., O’Neill, P., & Suomi, S. J. (1992). Adjustments and adaptations to indoor and outdoor environments: continuity and change in young adult rhesus monkeys. American Journal of Primatology, 28, 125–38.
Pardo, A., Ruiz, M. A., & San Martín, R. (2007). Cómo ajustar e interpretar modelos multinivel con SPSS. Psicothema, 19, 308–321.
Peñate, L., Peláez, F., & Sánchez, S. (2009). Reconciliation in captive cotton-top tamarins (Saguinus oedipus), a cooperative breeding primate. American Journal of Primatology, 71, 895–900.
Prescott, M. J., & Buchanan-Smith, H. M. (2004). Cage sizes for tamarins in the laboratory. Animal Welfare, 13, 151–158.
Price, E. C. (1991). Competition to carry infants in captive families of cotton-top tamarins. Behaviour, 118(1/2), 67–88.
Price, E. C., & McGrew, W. C. (1991). Departures from monogamy in colonies of captive cotton-top tamarins. Folia Primatologica, 57, 16–27.
Sánchez, S., Peláez, F., Gil-Burmann, C., & Kaumanns, W. (1999). Costs of infant-carrying in the cotton-top tamarin (Saguinus oedipus). American Journal of Primatology, 48, 99–111.
Sánchez, S., Peláez, F., & Gil-Burmann, C. (2002). Why do cotton-top tamarin female helpers carry infants? A preliminary study. American Journal of Primatology, 57, 43–49.
Sánchez, S., Peláez, F., Morcillo, A., & Gil-Burmann, C. (2005). Effect the enclosure on carriers’ body weight loss in the cotton-top tamarin (Saguinus oedipus). American Journal of Primatology, 66, 279–284.
Sánchez, S. M., Peláez, F., Fidalgo, A. M., Morcillo, A., & Caperos, J. M. (2008). Body weight increase in expectant males and helpers of cotton-top tamarin (Saguinus oedipus): a symptom of the couvade syndrome? Psicothema, 20(4), 825–829.
Sannen, A., Van Elsacker, L., & Eens, M. (2004). Effect spatial crowding on aggressive behavior in a bonobo colony. Zoo Biology, 23, 383–395.
Savage, A. (1995). The cotton-top tamarin SSP husbandry manual. Retrieved from http://www.csew.com/cottontop/.
Savage, A., Giraldo, L. H., Soto, L. H., & Snowdon, C. T. (1996a). Demography, group composition, and dispersal in wild cottontop tamarin (Saguinus oedipus) groups. American Journal of Primatology, 38, 85–100.
Savage, A., Snowdon, C. T., Giraldo, L. H., & Soto, L. H. (1996b). Parental care patterns and vigilance in wild cotton-top tamarins. In N. A. Norconk, A. L. Rosenberg, & P. A. Garber (Eds.), Adaptative radiations in neotropical primates (pp. 173–185). New York: Plenum Press.
Schaffner, C. M., & Caine, N. G. (2000). The peacefulness cooperatively breeding primates. In F. Aureli & F. B. M. de Waal (Eds.), Natural conflict resolution (pp. 155–169). Berkeley, CA: University California Press.
Schaffner, C. M., & French, J. A. (1997). Group size and aggression: ‘recruitment incentives’ in a cooperatively breeding primate. Animal Behaviour, 54, 171–180.
Schaffner, C. M., Aureli, F., & Caine, N. G. (2005). Following the rules: why small groups tamarins do not reconcile conflicts. Folia Primatologica, 76, 67–76.
Shutt, K., MacLarnon, A., Heistermann, M., & Semple, S. (2007). Grooming in Barbary macaques: better to give than to receive? Biology Letters, 3, 231–233.
Snowdon, C. T. (1996). Infant care in cooperatively breeding species. In P. J. B. Slater, J. S. Rosenblatt, C. T. Snowdon, & M. Milinsky (Eds.), Advances in the study of Behaviour Vol. 25: Parental care: Evolution, mechanisms, and adaptive significance (pp. 643–689). New York: Academic Press.
Snowdon, C. T., & Pickhard, J. (1999). Family feuds: severe aggression among cooperatively breeding cotton-top tamarins. International Journal of Primatology, 20, 651–663.
Sutcliffe, A. G., & Poole, T. B. (1984). Intragroup agonistic behavior in captive groups common marmosets Callithrix jacchus. International Journal of Primatology, 5, 473–489.
Tardif, S. D. (1997). The bioenergetics of parental of behavior and the evolution of alloparental care in marmosets and tamarins. In N. G. Solomon & J. A. French (Eds.), Cooperative breeding in mammals (pp. 11–33). Cambridge, UK: Cambridge University Press.
van Wolkenten, M. L., Davis, J. M., Gong, M. L., & de Waal, F. B. M. (2006). Coping with acute crowding by Cebus apella. International Journal of Primatology, 27, 1241–1256.
Videan, E., & Fritz, J. (2007). Effects short- and long-term changes in spatial density on the social behavior captive chimpanzees (Pan troglodytes). Applied Animal Behavioural Science, 102, 95–105.
Westlund, K., Ljungberg, T., Borefelt, U., & Abrahamsson, C. (2000). Postconflict affiliation in common marmosets (Callithrix jacchus jacchus). American Journal of Primatology, 52, 31–46.
Zahed, S. R., Kurian, A. V., & Snowdon, C. T. (2010). Social dynamics and individual plasticity infant care behavior in cooperatively breeding cotton-top tamarins. American Journal of Primatology, 72, 296–306.
Acknowledgments
We acknowledge the primate breeding and husbandry staff of the UAM for their technical support. We thank Charles Snowdon, Joanna Setchell, and 2 anonymous reviewers for their valuable advice and comments. We also thank Antonio Pardo for his statistical advice and Amanda Davies for her helpful notes. Contract grant sponsors were Spanish MCINN-SGPI (contract grant no. PSI2009-08581PSIC).
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Caperos, J.M., Sánchez, S., Peláez, F. et al. The Effect of Crowding on the Social Behavior of the Cooperatively Breeding Cotton-Top Tamarins (Saguinus oedipus). Int J Primatol 32, 1179–1189 (2011). https://doi.org/10.1007/s10764-011-9534-7
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DOI: https://doi.org/10.1007/s10764-011-9534-7