Abstract
Researchers studying nonhuman primate vocal repertoires suggest that convergent environmental, social, and motivational factors account for intra- and interspecific vocal variation. We provide a detailed overview of the vocal repertoire of white-faced capuchins, including acoustic analyses and contextual information of vocal production and vocal usage by different age-sex classes in social interactions. The repertoire is a mixture of graded and discrete vocalizations. In addition, there is general support for structural variation in vocalizations with changes in arousal level. We also identified several combined vocalizations, which might represent variable underlying motivations. Lastly, by including data on the social contexts and production of vocalizations by different age-sex classes, we provide preliminary information about the function of vocalizations in social interactions for individuals of different rank, age, and sex. Future studies are necessary to explore the function of combined vocalizations and how the social function of vocalizations relate to their acoustic structure, because social use of vocalizations may play an important role in shaping vocal evolution.
Similar content being viewed by others
References
Arnold, K., & Zuberbühler, K. (2006). The alarm calling system of adult male putty-nosed monkeys, Cercopithecus nictitans martini. Animal Behavior, 72, 643–653.
Bauers, K. A. (1993). A functional analysis of staccato grunt vocalizations in the stumptailed macaque (Macaca arctoides). Ethology, 94, 147–161.
Bauers, K. A., & de Waal, F. B. M. (1991). “Coo” vocalizations in stump-tailed macaques: a controlled functional analysis. Behaviour, 119, 143–160.
Bermejo, M., & Omedes, A. (1999). Preliminary vocal repertoire and vocal communication of wild bonobs (Pan paniscus) at Lilungu (Democratic Republic of Congo). Folia Primatologica, 70, 328–357.
Blount, B. (1985). “Girney” vocalizations among Japanese macaque females: Context and function. Primates, 26, 424–435.
Blumstein, D., & Armitage, K. B. (1997). Does social complexity drive the evolution of communicative complexity? A comparative test with ground-dwelling sciurid alarm calls. American Naturalist, 150, 179–200.
Boinski, S. (1993). Vocal coordination of troop movement among white-faced capuchin monkeys, Cebus capucinus. American Journal of Primatology, 30, 85–100.
Boinksi, S., & Campbell, A. F. (1995). Use of trill vocalizations to coordinate troop movement among white-faced capuchins: A second field test. Behaviour, 132, 875–901.
Boinski, S., & Campbell, A. F. (1996). The “huh” vocalization of white-faced capuchins: A spacing call disguised as a food call? Ethology, 102, 826–840.
Cheney, D. L., & Seyfarth, R. M. (1997). Reconciliatory grunts by dominant females influence victims' behaviour. Animal Behavior, 54, 409–418.
Cheney, D. L., Seyfarth, R. M., & Silk, J. B. (1995). The role of grunts in reconciling opponents and facilitating social interactions among female baboons. Animal Behavior, 50, 249–257.
Cleveland, J., & Snowdon, C. T. (1982). The complex vocal repertoire of the adult cotton-top tamarin (Saguinus oedipus oedipus). Zeitshrift für Tierpsychologie, 58, 231–270.
Crockford, C., & Boesch, C. (2005). Call combinations in wild chimpanzees. Behaviour, 142, 397–421.
Di Bitetti, M. S. (2001). Food-associated calls in the tufted capuchin monkey (Cebus apella): Unravelling the mysteries of an apparently altruistic behavior in an apparently selfish animal. Ph.D. dissertation, State University of New York, Stony Brook, NY.
Di Bitetti, M. S. (2003). Food-associated calls of tufted capuchin monkey (Cebus apella nigritus) are functionally referential signals. Behaviour, 140, 565–592.
Digweed, S. M., Fedigan, L. M., & Rendall, D. (2005). Variable specificity in the anti-predator vocalizations and behaviour of the white-faced capuchin, Cebus capucinus. Behaviour, 142, 997–1021.
Digweed, S. M., Fedigan, L. M., & Rendall, D. (2007). Who cares who calls? Selective responses to the lost calls of socially dominant group members in the white-faced capuchin (Cebus capucinus). American Journal of Primatology, 69, 1–7.
Dittus, W. P. J. (1984). Toque macaque food calls: Semantic communication concerning food distribution in the environment. Animal Behavior, 32, 470–477.
Dunteman, G. H. (1989). Principal components analysis. Beverly Hills, CA: Sage.
Evans, C. S., & Evans, L. (1999). Chicken food calls are functionally referential. Animal Behavior, 58, 307–319.
Fedigan, L. M. (1993). Sex differences and intersexual relations in adult white-faced capuchins (Cebus capucinus). International Journal of Primatology, 14, 853–877.
Fichtel, C., & Hammerschmidt, K. (2002). Responses of redfronted lemurs (Eulemur fulvus rufus) to experimentally modified alarm calls: Evidence for urgency-based changes in call structure. Ethology, 108, 763–777.
Fichtel, C., & Hammerschmidt, K. (2003). Responses of squirrel monkeys to experimentally modified mobbing calls. Journal of the Acoustic Society of America, 113, 2927–2932.
Fichtel, C., Hammerschmidt, K., & Jürgens, U. (2001). On the vocal expression of emotion. A multiparametric analysis of different states of aversion in the squirrel monkey. Behaviour, 138, 97–116.
Fichtel, C., & Kappeler, P. M. (2002). Anti-predator behaviour of group-living Malagasy primates: Mixed evidence for a referential alarm call system. Behavioral Ecology and Sociobiology, 51, 262–275.
Fichtel, C., Perry, S., & Gros-Louis, J. (2005). Alarm calls of white-faced capuchin monkeys: An acoustic analysis. Animal Behavior, 170, 165–176.
Fischer, J. (1998). Barbary macaques categorize shrill barks into two call types. Animal Behavior, 55, 799–807.
Fischer, J., & Hammerschmidt, K. (2001). Functional referents and acoustic similarity revisited: The case of Barbary macaque alarm calls. Animal Cognition, 4, 29–35.
Fischer, J., & Hammerschmidt, K. (2002). An overview of the Barbary macaque, Macaca sylvanus, vocal repertoire. Folia Primatologica, 73, 32–45.
Fischer, J., Hammerschmidt, K., Cheney, D. L., & Seyfarth, R. M. (2002). Acoustic features of male baboon loud calls: Influences of context, age, and individuality. Journal of the Acoustic Society of America, 111, 1465–1474.
Fischer, J., Hammerschmidt, K., & Todt, D. (1995). Factors affecting acoustic variation in Barbary macaque (Macaca sylvanus) disturbance calls. Ethology, 101, 51–66.
Fischer, J., Kitchen, D. M., Seyfarth, R. M., & Cheney, D. L. (2004). Baboon loud calls advertise male quality: Acoustic features and their relation to rank, age, and exhaustion. Behavioral Ecology and Sociobiology, 56, 140–148.
Fischer, J., Metz, M., Cheney, D. L., & Seyfarth, R. M. (2001). Categorical responses of Chacma baboons to graded bark variants? Animal Behavior, 61, 925–931.
Frankie, G. W., Vinston, S. B., Newstrom, L. E., & Barthell, J. F. (1988). Nest and and habitat preferences of Centris bees in the Costa Rican dry forest. Biotropica, 20, 301–310.
Freese, C., & Oppenheimer, J. (1981). The capuchin monkeys, genus Cebus. In A. Coimbra-Filho, & R. Mittermeier (Eds.), Ecology and behavior of neotropical primates (vol. 1). Rio de Janeiro: Academia Brasileira de Ciencias.
Gouzoules, S., & Gouzoules, H. (2000). Agonistic screams differ among four species of macaques: The significance of motivational-structural rules. Animal Behavior, 59, 501–512.
Gros-Louis, J. (2002). Contexts and behavioral correlates of trill vocalizations in wild white-faced capuchin monkeys (Cebus capucinus). American Journal of Primatology, 57, 189–202.
Gros-Louis, J. (2004a). The function of food-associated calls from the perspective of the signaller. Animal Behavior, 67, 431–440.
Gros-Louis, J. (2004b). White-faced capuchins' responses to naturalistic and experimentally presented food-associated calls. Journal of Comparative Psychology, 118, 396–402.
Gros-Louis, J. (2006). Acoustic description and contextual analysis of food-associated calls in Cebus capucinus. International Journal of Primatology, 27, 273–294.
Hammerschmidt, K., & Fischer, J. (1998). The vocal repertoire of Barbary macaques: A quantitative analysis of a graded signal system. Ethology, 104, 203–216.
Hammerschmidt, K., & Todt, D. (1995). Individual differences in vocalizations of young barbary macaques (Macaca sylvanus): A multi-parametric analysis to identify critical cues in acoustic signaling. Behaviour, 132, 381–399.
Harcourt, A. H., Stewart, K. J., & Hauser, M. (1993). Functions of wild gorilla close calls. I. Repertoire, context and interspecific comparison. Behaviour, 124, 89–122.
Hauser, M. D. (1993). The evolution of nonhuman primate vocalizations: Effects of phylogeny, body size, and social context. American Naturalist, 142, 528–542.
Hauser, M. D. (1998). Functional referents and acoustic similarity: Field playback experiments with rhesus monkeys. Animal Behavior, 55, 1647–1658.
Klecka, W. (1980). Discriminant analysis. Beverly Hills, CA: Sage.
Macedonia, J. M. (1990). What is communicated in the antipredator calls of lemursh: Evidence from playback experiments with ringtailed and ruffed lemurs. Ethology, 86, 177–190.
Macedonia, J. M. (1993). The vocal repertoire of the ring-tailed lemur (Lemur catta). Folia Primatologica, 61, 186–217.
Manser, M. B. (2001). The acoustic structure of suricate's alarm calls vary with predator class and response urgency. Proceedings of the Royal Society of London Series B, 268, 2485–2491.
Manson, J. H., Perry, S., & Parish, A. R. (1997). Nonconceptive sexual behavior in bonobos and capuchins. International Journal of Primatology, 18, 767–786.
Marler, P. (1965). Communication in monkeys and apes. In I. DeVore (Ed.), Primate behavior: Field studies in monkeys and apes (pp. 544–584). New York: Holt, Rinehart and Winston.
Marler, P. (1976). Social organization, communication and graded signals: the chimpanzee and the gorilla. In P. Bateson, & R. A. Hinde (Eds.), Growing points in ethology (pp. 239–280). Cambridge, U.K.: Cambridge University Press.
Marler, P. (1977). The structure of animal communication sounds. In T. H. Bullock (Ed.), Recognition of complex acoustic signals (pp. 17–35). Berlin: Springer.
McComb, K., & Semple, S. (2005). Coevolution of vocal communication and sociality in primates. Biology Letters, 1, 381–385.
McShane, L. J., Estes, J. A., Riedman, M. L., & Staedler, M. M. (1995). Repertoire, structure and individual variation of vocalizations in the sea otter. Journal of Mammology, 76, 414–427.
Mitani, J. (1985). Sexual selection and adult male orangutan long calls. Animal Behavior, 33, 272–283.
Morton, E. S. (1977). On the occurrence and significance of motivation-structural rules in some bird and mammal sounds. American Naturalist, 111, 855–869.
Morton, E. S. (1982). Grading, discreteness, redundancy, and motivational-structural rules. In D. Kroodsma, & E. H. Miller (Eds.), Acoustic communication in birds (pp. 183–212). New York: Academic Press.
Oppenheimer, J. R. (1973). Social and communicatory behavior in the Cebus monkey. In C. R. Carpenter (Ed.), Behavioral regulators of behavior in primates (pp. 251–271). Cranbury, N J: Associated University Presses.
Owings, D. H., & Morton, E. S. (1998). Animal Vocal Communication: A new approach. Cambridge, U.K: Cambridge University Press.
Owren, M. J., & Rendall, D. (2001). Sound on the rebound: Bringing form and function back to the forefront in understanding nonhuman primate vocal signaling. Evolutionary Anthropology, 10, 58–71.
Palombit, R. A. (1992). A preliminary study of the vocal communication in wild long-tailed macaques (Macaca fascicularis), I. Vocal repertoire and call emission. International Journal of Primatology, 13, 143–182.
Palombit, R. A., Cheney, D. L., & Seyfarth, R. M. (1999). Male grunts as mediators of social interaction with females in wild chacma baboons (Papio cynocephalus ursinus). Behaviour, 136, 221–242.
Perry, S. (1995). Social relationships in wild white-faced capuchin monkeys, Cebus capucinus. Ph.D. thesis, University of Michigan, Ann Arbor.
Perry, S. (1996). Intergroup encounters in wild white-faced capuchin monkeys, Cebus capucinus. American Journal of Primatology, 40, 167–182.
Perry, S. (1998). Male-male social relationships in wild white-faced capuchins, Cebus capucinus. Behaviour, 135, 139–172.
Perry, S., Baker, M., Fedigan, L., Gros-Louis, J., Jack, K., MacKinnon, K., et al. (2003). Social conventions in wild white-faced capuchin monkeys: Evidence for traditions in a neotropical primate. Current Anthropology, 44, 241–268.
Perry, S., Barrett, H. C., & Manson, J. H. (2004). White-faced capuchins show triadic awareness in their choice of allies. Animal Behavior, 67, 165–170.
Range, F., & Fischer, J. (2004). Vocal repertoire of sooty magabeys (Cercocebus torquatus atys) in the Taï National Park. Ethology, 110, 301–321.
Rendall, D., Seyfarth, R. M., Cheney, D. L., & Owren, M. J. (1999). The meaning and function of grunt variants in baboons. Animal Behavior, 57, 583–592.
Robbins, R. L., & McCreery, E. K. (2003). African wild dog pup vocalizations with special reference to Morton's model. Behaviour, 140, 333–351.
Robinson, J. G. (1979). Vocal regulation of use of space by groups of titi monkeys Callicebus moloch. Behavioral Ecology and Sociobiology, 5, 1–15.
Robinson, J. G. (1982). Vocal systems regulating within-group spacing. In C. T. Snowdon, C. H. Brown, & M. R. Petersen (Eds.), Primate communication (pp. 94–116). Cambridge, U.K.: Cambridge University Press.
Robinson, J. G. (1984). Syntactic structures in the vocalizations of wedge-capped capuchin monkeys, Cebus olivaceus. Behaviour, 90, 46–79.
Schott, D. (1975). Quantitative analysis of the vocal repertoire of squirrel monkeys (Saimiri scieureus). Zeitshrift für Tierpsychologie, 38, 225–250.
Schrader, L., & Hammerschmidt, K. (1997). Computer-aided analysis of acoustic parameters in animal vocalizations: A multi-parametric approach. Bioacoustics, 7, 247–265.
Schrader, L., & Todt, D. (1993). Contact call parameters covary with social context in common marmosets, Callithrix j. jacchus. Animal Behavior, 46, 1026–1028.
Seyfarth, R. M., Cheney, D. L., & Marler, P. (1980). Monkey responses to 3 different alarm calls: Evidence for predator classification and semantic communication. Science, 210, 801–803.
Todt, D., Hammerschmidt, K., Ansorge, V., & Fischer, J. (1995). The vocal behavior of Barbary macaques (Macaca sylvanus): Call features and their performance in infants and adults. In E. Zimmerman, J. D. Newman, & U. Jurgens (Eds.), Current topics in primate vocal communication (pp. 141–160). New York: Plenum Press.
Watts, J. M., & Stookey, J. M. (1999). Effects of restraint and branding on rates and acoustic parameters of vocalization in beef cattle. Applied Animal Behavior Science, 62, 125–135.
Weary, D. M., Braithwaite, L. A., & Fraser, D. (1998). Vocal response to pain in piglets. Applied Animal Behavior Science, 56, 161–172.
Wiley, R. H., & Richards, D. G. (1978). Physical constraints on acoustic communication in the atmosphere: Implications for the evolution of animal vocalization. Behavioral Ecology and Sociobiology, 3, 69–94.
Zimmerman, E. (1985). The vocal repertoire of the adult Senegal bushbaby (Galago senegalensis senegalensis). Behaviour, 94, 212–233.
Zuberbühler, K. (2000). Referential labelling in Diana monkeys. Animal Behavior, 59, 917–927.
Zuberbühler, K. (2002). A syntactic rule in forest monkey communication. Animal Behavior, 63, 293–299.
Zuberbühler, K., Cheney, D. L., & Seyfarth, R. M. (1999). Conceptual semantics in a nonhuman primate. Journal of Comparative Psychology, 113, 33–42.
Acknowledgments
All authors received support from The Max Planck Institute for Evolutionary Anthropology during the analysis phase of the project. The following sources supported J. J. Gros-Louis during data collection: a dissertation research award from the American Psychological Association, an NSF predoctoral research fellowship and an NSF doctoral dissertation improvement grant, and a Vessa Notchev Fellowship from SDE-GWIS and The University of Pennsylvania. The following sources supported S. E. Perry during data collection: The Max Planck Institute for Evolutionary Anthropology, the L.S.B. Leakey Foundation, the National Geographic Society, NSF (NSF-NATO postdoctoral fellowship no. 9633991, a graduate fellowship, and POWRE grant no. 9870429), the Wenner-Gren Foundation, the UCLA Academic Senate, the Rackham (University of Michigan) Graduate School, the Evolution and Human Behavior Program, the University of Michigan Alumnae Society, the Killam Trust, and Sigma Xi. We thank the Costa Rican National Park Service, the Area Conservación Tempisque, the community of San Ramon de Bagaces, Hacienda Pelón de la Bajura, and Brin d'Amour Estates for permission to work in areas of the monkeys' home ranges. J. Anderson, K. Atkins, T. Bishop, F. Campos, G. Dower, M. Duffy, L. Johnson, E. Kennedy, S. Kessler, M. Mendoza F., W. Lammers, T. Lord, W. Meno, J. C. Ordoñez J., N. Parker, B. Pav, K. Potter, K. Pyle, K. Ratliff, H. Ruffler, C. Schmitt, A. Steele, and M. Varley provided assistance in behavioral data collection and recordings. J. Silk wrote the program FOCOBS for data collection. K. Hammerschmidt designed and provided technical assistance for the LMA program.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Gros-Louis, J.J., Perry, S.E., Fichtel, C. et al. Vocal Repertoire of Cebus capucinus: Acoustic Structure, Context, and Usage. Int J Primatol 29, 641–670 (2008). https://doi.org/10.1007/s10764-008-9263-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10764-008-9263-8