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The Effect of Crowding on the Social Behavior of the Cooperatively Breeding Cotton-Top Tamarins (Saguinus oedipus)

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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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Chapter  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Baker, K., & Aureli, F. (1997). Behavioral indicators anxiety: an empirical test in chimpanzees. Behaviour, 134, 1031–105.

    Article  Google Scholar 

  • Boccia, M. L., Reite, M., & Laudenslager, M. (1989). On the physiology grooming in a pigtail macaque. Physiological Behaviour, 45, 667–670.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Google Scholar 

  • Calhoun, J. B. (1962). Population density and social pathology. Scientific American, 206, 139–148.

    PubMed  CAS  Google Scholar 

  • Cilia, J., & Piper, D. C. (1997). Marmoset conspecific confrontation: an ethologically-based model anxiety. Pharmacology, Biochemistry, and Behavior, 58, 85–91.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • de Waal, F. B. M. (1989). The myth a simple relation between space and aggression in captive primates. Zoo Biology, 1(Supplement), 141–148.

    Article  Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Honess, P. E., & Marin, C. M. (2006). Behavioural and physiological aspects of stress and aggression in nonhuman primates. Neuroscience Biobehavioral Review, 30, 390–412.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Google Scholar 

  • Judge, P. G., & de Waal, F. B. M. (1993). Conflict avoidance among rhesus monkeys: coping with short-term crowding. Animal Behaviour, 46, 221–232.

    Article  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Koyama, N., & Palagi, E. (2006). Managing conflict: evidence from wild and captive primates. International Journal of Primatology, 27, 1235–1240.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Martin, P., & Bateson, P. (1986). Measuring behaviour: An introductory guide. Cambridge, UK: Cambridge University Press.

    Google Scholar 

  • 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.

    Article  Google Scholar 

  • Moura, A. C. A. (2003). Sibling age and intragroup aggression in cautive Saguinus midas midas. International Journal of Primatology, 24, 639–652.

    Article  Google Scholar 

  • Nash, L. T., & Chilton, S. (1986). Space or novelty? Effects of altered cage size on galago behavior. American Journal of Primatology, 10, 37–50.

    Article  Google Scholar 

  • Nieuwenhuijsen, K., & de Waal, F. B. M. (1982). Effects spatial crowding on social behavior in a chimpanzee colony. Zoo Biology, 1, 5–28.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Pardo, A., Ruiz, M. A., & San Martín, R. (2007). Cómo ajustar e interpretar modelos multinivel con SPSS. Psicothema, 19, 308–321.

    PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Prescott, M. J., & Buchanan-Smith, H. M. (2004). Cage sizes for tamarins in the laboratory. Animal Welfare, 13, 151–158.

    CAS  Google Scholar 

  • Price, E. C. (1991). Competition to carry infants in captive families of cotton-top tamarins. Behaviour, 118(1/2), 67–88.

    Google Scholar 

  • Price, E. C., & McGrew, W. C. (1991). Departures from monogamy in colonies of captive cotton-top tamarins. Folia Primatologica, 57, 16–27.

    Article  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Google Scholar 

  • Sannen, A., Van Elsacker, L., & Eens, M. (2004). Effect spatial crowding on aggressive behavior in a bonobo colony. Zoo Biology, 23, 383–395.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • Schaffner, C. M., & French, J. A. (1997). Group size and aggression: ‘recruitment incentives’ in a cooperatively breeding primate. Animal Behaviour, 54, 171–180.

    Article  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Shutt, K., MacLarnon, A., Heistermann, M., & Semple, S. (2007). Grooming in Barbary macaques: better to give than to receive? Biology Letters, 3, 231–233.

    Article  PubMed  Google Scholar 

  • 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.

    Google Scholar 

  • Snowdon, C. T., & Pickhard, J. (1999). Family feuds: severe aggression among cooperatively breeding cotton-top tamarins. International Journal of Primatology, 20, 651–663.

    Article  Google Scholar 

  • Sutcliffe, A. G., & Poole, T. B. (1984). Intragroup agonistic behavior in captive groups common marmosets Callithrix jacchus. International Journal of Primatology, 5, 473–489.

    Article  Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Westlund, K., Ljungberg, T., Borefelt, U., & Abrahamsson, C. (2000). Postconflict affiliation in common marmosets (Callithrix jacchus jacchus). American Journal of Primatology, 52, 31–46.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  Google Scholar 

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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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Correspondence to José Manuel Caperos.

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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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