Abstract
We recorded the vocal repertoire and behavior of individuals from 3 groups of wild common marmosets (Callithrix jacchus) via focal sampling and ad libitum sampling in a fragment of Atlantic Rain Forest in Pernambuco, northeast Brazil. Our aims were: 1) to provide a detailed quantitative description of the vocalizations and vocal repertoire of common marmosets in the wild, and to compare the repertoire with that described from conspecific captives; 2) to investigate if differences exist in vocal repertoire between wild individuals of different ages; and 3) to explore the behavioral contexts associated with specific vocalizations in free-living Callithrix jacchus. This is the first study describing common marmoset calls in the wild and it shows that their vocal repertoire comprises 13 different calls. Though wild and captive calls were similar, differences occurred in the form of the alarm calls given for different potential predators, the tsê call, and very brief whistle. In addition, the tsee call did not occur in wild individuals and wild infants did not utter the twitter call. The age of the subjects influenced the call types present in the vocal repertoire, e.g., the loud cry was specific to infants, whereas only adults gave alarm calls. The behavior of both the caller and the potential receivers seemed to affect the frequency of wild common marmoset calls. One could predict intricate vocalization-based communications for the system based on their relatively complex social organization and densely leafed arboreal habitat. Our study confirms the prediction.






Similar content being viewed by others
References
Alonso, C., & Langguth, A. (1989). Ecologia e comportamento de Callithrix jacchus (Primates: Callitrichidae) numa ilha de floresta Atlântica. Revista Nordestina de Biologia, 6, 105–137.
Altmann, S. A. (1967). The structure of primate social communication. In S. A. Altman (Ed.) Social communication among primates (pp. 325–336). Chicago: University of Chicago Press.
Altmann, J. (1974). Observational study of behaviour: sampling methods. Behaviour, 49, 277–267.
Barros, M., Boere, V., Mello Jr., E. L., & Tomaz, C. (2002). Reactions to potential predators in captive-born marmosets (Callithrix penicillata). International Journal of Primatology, 23, 443–454.
Bezerra, B. M., Souto, A. S., & Schiel, N. (2007). Infanticide and cannibalism in a free-ranging plurally breeding group of common marmosets (Callithrix jacchus). American Journal of Primatolology, 69, 945–952.
Bezerra, B. M., Barnett, A. P., Souto, A., & Jones, G. (2008). Prediction by the tayra on the common marmoset and the pale-throated three-toed sloth. Journal of Ethology. Online First, DOI 10.1007/s10164-008-0090-3.
Biebel, M. (2004). Das Ei des Kolumbus. Video Aktiv Digital, 5, 18–20.
Boere, V. (2001). Environmental enrichment for neotropical primates in captivity. Ciência Rural, 31, 543–551.
Boinski, S., & Campbell, A. F. (1995). Use of trill vocalizations to coordinate troop movement among white-faced capuchins: A second field test. Behavior, 132, 875–901.
Bradbury, J. W., & Vehrencamp, S. L. (1998). Principles of Animal Communication. Sunderland, MA: Sinauer Associates.
Burling, R. (1993). Primate calls, human language, and nonverbal communication. Current Anthropology, 34, 25–53.
Camarotti, F. L. M., & Monteiro da Cruz, M. A. O. (1997). Fatores ecológicos e comportamentais implicados na seleção e uso dos locais de pernoite de grupos de Callithrix jacchus em ambiente natural. In M. B. C. Souza, & A. L. L. Menezes (Eds.) A primatologia no Brasil, 6 (pp. 27–42). Natal: EDUFRN and Sociedade Brasileira de Primatologia.
Cheney, D. L., & Seyfarth, R. M. (1990). How monkeys see the world: inside the mind of another species. Chicago: University of Chicago Press.
Cheney, D. L., & Wrangham, R. W. (1987). Predation. In B. B. Smuts, D. L. Cheney, R. M. Seyfarth, R. W. Wrangham, & T. T. Struhsaker (Eds.) Primate societies (pp. 227–239). Chicago: University of Chicago Press.
Cleveland, J., & Snowdon, C. T. (1982). The complex vocal repertoire of the adult cotton-top tamarin (Saguinus oedipus oedipus). Zeitschrift fur Tierpsychologie, 58, 231–270.
Digby, L. (1995). Infant care, infanticide, and female reproductive strategies in polygynous groups of common marmosets (Callithrix jacchus). Behavioural Ecology and Sociobiology, 37, 51–61.
Dudzinnski, K. (1998). Contact behaviour and signal exchange in Atlantic spotted dolphins (Stenella frontalis). Aquatic Mammals, 24, 129–142.
Dudzinnski, K. (1999). Intraspecific contact behavior and signal exchange among free-ranging dolphins - the view from underwater. IBI Reports, 9, 93–107.
Epple, G. (1968). Comparative studies on vocalization in marmoset monkeys (Hapalidae). Folia Primatologica, 8, 1–40.
Ferrari, S. F., & Lopes Ferrari, M. A. (1989). A re-evaluation of the social organization of the Callitrichidae, with reference to the ecological differences between genera. Folia Primatologica, 52, 132–147.
Ghanzafar, A. A., & Hauser, M. D. (2001). The auditory behaviour of primates: a neuroethological perspective. Current Opinion in Neurobiology, 11, 712–720.
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.
Halsey, L. G., Bezerra, B. M., & Souto, A. S. (2006). Can wild common marmosets (Callithrix jacchus) solve the parallel strings task? Animal Cognition, 9, 229–233.
Hardie, S. M., & Buchanan-Smith, H. M. (1997). Vigilance in single- and mixed-species groups of tamarins (Saguinus labiatus and Saguinus fuscicollis). International Journal of Primatology, 8, 217–234.
Herzing, D. L. (1996). Vocalizations and associated underwater behaviour of free-raging Atlantic spotted dolphins, Stenella frontalis and bottlenose dolphins, Tursiops truncatus. Aquatic Mammals, 22, 61–79.
Itani, J. (1963). Vocal communication of wild Japanese monkey. Primates, 4, 11–66.
Jones, B. S., Harris, D. H. R., & Catchpole, C. K. (1993). The stability of the vocal signature in phee calls of the common marmoset, Callithrix jacchus. American Journal of Primatology, 31, 67–75.
Kirchhof, J., & Hammerschmidt, K. (2006). Functionally referential alarm calls in tamarins (Saguinus fuscicollis and Saguinus mystax) - Evidence from playback experiments. Ethology, 112, 346–354.
Lamprecht, J. (1999). Biologische Forschung: von der Planung bis zur Publikation. Fürth: Filander Verlag.
Maier, W., Alonso, C., & Langguth, A. (1982). Field observation of Callithrix jacchus. Mammal Biology, 47, 334–346.
Maurus, M., Streit, K. M., Barclay, B., Wiesner, E., & Kühlmorgen, B. (1988). A new approach to finding components essential for intraspecific communication. In D. Todt, P. Goedeking, & D. Symmes (Eds.) Primate vocal communication (pp. 69–87). Berlin: Springer-Verlag.
McLanahan, E. B., & Green, K. M. (1977). The vocal repertoire and analysis of contexts of vocalizations in Leonthopithecus rosalia. In D. G. Kleiman (Ed.) The biology and conservation of the Callitrichidae (pp. 251–269). Washington, DC: Smithsonian Institution Press.
McPhee, M. E. (2003). Effects of captivity on response to a novel environment in the oldfield mouse (Peromyscus polionotus subgriseus). International Journal of Comparative Psychology, 16, 85–94.
Mendes Pontes, A. R., & Soares, M. L. (2005). Sleeping sites of common marmosets (Callithrix jacchus) in defauned urban forest fragments: a strategy to maximize food intake. Journal of Zoology (London), 266, 55–63.
Napier, J. R., & Napier, P. H. (1996). The natural history of the primates. Cambridge, MA: The MIT Press.
Newton-Fisher, N., Harris, S., White, P., & Jones, G. (1993). Structure and function of red fox Vulpes vulpes vocalisations. Bioacoustics, 5, 1–31.
Norcross, J. L., & Newman, J. D. (1993). Context and gender-specific differences in the acoustic structure of common marmoset (Calithrix jacchus) phee calls. American Journal of Primatology, 30, 37–54.
Norcross, J. L., Newman, J. D., & Confrancesco, L. M. (1999). Context and sex differences exist in the acoustic structure of phee calls by newly-paired common marmosets (Callithrix jacchus). American Journal of Primatology, 49, 165–181.
Norcross, J. L., Newman, J. D., & Fitch, W. (1994). Responses to natural and synthetic phee calls by common marmoset (Callithrix jacchus). American Journal of Primatology, 33, 15–29.
Oliveira, D. A. G., & Ades, C. (2004). Long-distance calls in neotropical primates. Anais da Academia Brasileira de Ciências, 76, 393–398.
Omedes Regas, A. (1983). Estudio de la cominicación social del tití plateado. Anthropos, 26, 81–83.
Owren, M., & Linker, C. (1995). Some analysis methods that may be useful to acoustic primatologists. In E. Zimmermann, J. D. Newman, & U. Juergens (Eds.) Current topics in primate vocal communication (pp. 1–28). New York: Plenum Press.
Passamani, M. (1995). Field observation of a group of Geoffroy’s marmosets mobbing a Margay cat. Folia Primatologica, 64, 163–166.
Pistorio, A. L., Vintch, B., & Wang, X. (2006). Acoustic analysis of vocal development in a New World primate, the common marmoset (Callithrix jacchus). Journal of the Acoustical Society of America, 120, 1655–1670.
Ploog, D. W. (1967). The behavior of squirrel monkeys (Saimiri sciureus) as revealed by sociometry, bioacoustics and brain stimulation. In S. T. Altman (Ed.) Social communication among primates (pp. 149–184). Chicago: University of Chicago Press.
Pook, A. G. (1976). A comparative study of the vocalizations of the saddleback tamarin, Saguinus fucsicolis and the common marmoset, Callithrix jacchus (Callithrichidae; Primates). Unpublished Ph.D thesis. University of Reading, U.K.
Pook, A. G. (1977). A comparative study of the use of contact calls in Saguinus fuscicolis and Callithrix jacchus. In D. Kleiman (Ed.) The biology and conservation of Callithrichidae (pp. 271–280). Washington, DC: Smithsonian Institution Press.
Rice, W. R. (1989). Analyzing tables of statistical tests. Evolution, 43, 223–225.
Roush, R. S., & Snowdon, C. T. (1999). The effect of social status on food-associated calling behaviour in captive cotton-top tamarins. Animal Behaviour, 58, 1299–1305.
Schiel, N. (2000). Das estratégias de captura do Callithrix jacchus (Primates, Callithichidae) à capacidade de fuga da presa. (Master thesis). Departamento de Zoologia: Universidade Federal de Pernambuco, Pernambuco. Available from Universidade Federal de Pernambuco, Pernambuco, Brazil.
Schiel, N., & Huber, L. (2006). Development of social learning in free-living marmosets (Callithrix jacchus). American Journal of Primatology, 68, 1150–1160.
Shopmann, V. J. (1999). Auf Schritt und Tritt: Richtmikros sollen dem Schall immer dicht auf den fersen bleiben. Video Aktiv Digital, 4, 24–28.
Siegel, S., & Castellan Jr., J. (1988). Nonparametric statistics for the behavioral science. New York: McGraw-Hill.
Smith, T. (2006). Individual olfactory signatures in common marmosets (Callithrix jacchus). American Journal of Primatology, 68, 585–604.
Snowdon, C. T. (1988). Communications as social interaction: Its importance in ontogeny and adults behavior. In D. Todt, P. Goedeking, & D. Symmes (Eds.) Primate vocal communication (pp. 108–122). Berlin: Springer-Verlag.
Snowdon, C. T. (1989). The structure and usage of long calls in marmosets and tamarins. In P. K. Seth, & S. Seth (Eds.) Perspectives in primate biology (pp. 83–92). New Delhi: Today & Tomorrow’s Printers & Publishers.
Snowdon, C. T. (2001). Social process in communication and cognition in callitrichid monkeys: A review. Animal Cognition, 4, 247–257.
Snowdon, C. T., & Elowson, M. (2004). Babbling in pygmy marmosets: development after infancy. Behaviour, 138, 1235–1248.
Snowdon, C. T., & Hodun, A. (1981). Acoustic adaptations in pygmy marmoset contact calls: Location cues vary with distances between conspecifics. Behavioural Ecology and Sociobiology, 9, 295–300.
Soini, P. (1988). The pygmy marmoset, genus Cebuella. In R. A. Mittermeier, A. B. Rylands, A. F. Coimbra-Filho, & G. A. B. da Fonseca (Eds.) Ecology and behavior of neotropical primates, Vol. 2 (pp. 79–129). Washington, DC: World Wildlife Fund.
Soltis, J., Bernhards, D., Donkin, H., & Newman, J. D. (2002). Squirrel monkey chuck call: vocal responses to playback chucks based on acoustic structure and affiliative relationship with the caller. American Journal of Primatology, 57, 119–130.
Souto, A., Bezerra, B. M., Schiel, N., & Huber, L. (2007). The saltatory search in free-living common marmosets: Environmental and age influences. International Journal of Primatology, 28, 881–893.
Stevenson, M. F., & Poole, T. B. (1976). An ethogram of the common marmoset, Callithrix jacchus: General behavioral repertoire. Animal Behaviour, 24, 428–451.
Stevenson, M. F., & Rylands, A. B. (1988). The marmosets, genus Callithrix. In A. R. Mittermeier, B. A. Rylands, A. Coimbra-Filho, & B. A. G. Fonseca (Eds.) Ecology and behaviour of neotropical primates, Vol. 2 (pp. 131–222). Washington, DC: World Wildlife Fund.
Struhsaker, T. T. (1967). Auditory communication among vervet monkeys (Cercopithecus aethiops). In S. A. Altmann (Ed.) Social communication among primates (pp. 281–324). Chicago: University of Chicago Press.
Taglialatela, J. P., Savage-Rumabaugh, S., & Baker, L. A. (2003). Vocal production by language-competent Pan paniscus. International Journal of Primatology, 24, 1–17.
Tanaka, T., Sugiura, H., & Masataka, N. (2006). Cross-sectional and longitudinal studies of the development of group differences in acoustic features of coo calls in two groups of Japanese macaques. Ethology, 112, 7–21.
Uster, D., & Zuberbühler, K. (2001). The functional significance of Diana monkey ‘clear’ calls. Behaviour, 138, 741–756.
Weiss, D. J., Garibaldi, B. T., & Hauser, M. D. (2001). The production and perception of long calls in cotton-top tamarins (Saguinus oedipus): Acoustic analyses and playback experiments. Journal of Comparative Psychology, 115, 258–271.
Winter, M. (1977). Some aspects of the ontogeny of vocalizations of hand-reared common marmoset. In H. Rothe, H. J. Wolters, & J. P. Hearn (Eds.) Biology and behaviour of marmosets. Proceedings of the marmoset workshop (pp. 127–139). Gottingen: Eigenverlag Rothe.
Winter, M., & Rothe, H. (1979). Darstellung des Lautrepertoires handaufgezogener Weiß-büscheläffchen (Callithrix jacchus) unter besondere Berücksichtigung der fließenden Übergange zwischen den einzelnen Lautgruppen. Primates, 20, 259–276.
Yamamoto, M. E. (1991). Comportamento social do gênero Callithrix em cativeiro. In A. B. Rylands, & C. Vale (Eds.) A Primatologia no Brasil 3 (pp. 63–81). Belo Horizonte: Littera Maciel/Biodiversitas.
Zimmermann, E., & Hafen, T. G. (2001). Colony specificity in social call of mouse lemurs (Microcebus ssp.). American Journal of Primatology, 54, 129–141.
Acknowledgments
We thank 2 anonymous referees for their valuable suggestions and Edmilson Mazza for valuable statistical advises. We also thank Lewis Halsey, Adrian Barnett, Valdir Luna, Daniel Pessoa, Diego Ástua, Nicola Schiel, and Maria Adélia Oliveira for their comments on earlier versions of the manuscript. The Brazilian Council for Technological and Scientific Development (CNPq) provided a scholarship to B. M. Bezerra (grant no. 130770/2005). This study complies with Brazilian law and is part of the ongoing common marmoset long-term research project at the study site.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Bezerra, B.M., Souto, A. Structure and Usage of the Vocal Repertoire of Callithrix jacchus . Int J Primatol 29, 671–701 (2008). https://doi.org/10.1007/s10764-008-9250-0
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10764-008-9250-0