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Individual Variation of Whinnies Reflects Differences in Membership Between Spider Monkey (Ateles geoffroyi) Communities

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Abstract

Contact calls, which function to coordinate group movement and maintain contact between conspecifics, are predicted to show high levels of acoustic variability and individual distinctiveness. We investigated interindividual variation in whinnies, a contact call, between two geographically distinct communities of wild Geoffroyi’s spider monkeys (Ateles geoffroyi), which were experiencing different degrees of stability in membership due to immigration. We recorded whinnies from 18 subjects, including 9 females ranging within the Otoch Ma’ax Yetal Kooh Reserve, Punta Laguna, Mexico, and 9 females ranging within the Santa Rosa Sector, Area de Conservación Guanacaste, Costa Rica. We examined 13 acoustic parameters of female whinnies using principal component analysis and discriminant function analysis. Individual acoustic variability was significantly different between the two communities. A higher percentage of the whinnies of females were assigned to the correct caller in the community with only 3 individuals immigrating within 36 mo before and during data collection than in the community with 15 immigrant individuals during the same period. We suggest that the variation in interindividual distinctiveness for each community was influenced by the stability of the vocal environment, which was quantitatively different between communities because of changes in membership.

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References

  • Amorim, M. C. P., & Vasconcelos, R. O. (2008). Variability in the mating calls of the Lusitanian toadfish Halobatrachus didactylus: cues for potential individual recognition. Journal of Fish Biology, 73, 1267–1283.

    Article  Google Scholar 

  • Aubin, T., & Jouventin, P. (2002). How to vocally identify kin in a crowd: the penguin model. Advances in the Study of Behaviour, 31, 243–277.

    Article  Google Scholar 

  • Aureli, F., Di Fiore, A., Murillo-Chacon, E., Kawamura, S., & Schaffner, C. M. (2013). Male philopatry in spider monkeys revisited. American Journal of Physical Anthropology. doi:10.1002/ajpa.22331.

    PubMed  Google Scholar 

  • Aureli, F., & Schaffner, C. M. (2008). Social interactions, social relationships and the social system of spider monkeys. In C. J. Campbell (Ed.), Spider monkeys: Behavior, ecology and evolution of the genus Ateles (pp. 236–265). Cambridge, U.K.: Cambridge University Press.

    Google Scholar 

  • Aureli, F., Schaffner, C. M., Boesch, C., Beader, S. K., Call, J., Chapman, C .A., et al. (2008). Fission-fusion dynamics: New research frameworks. Current Anthropology, 49, 627–654.

    Google Scholar 

  • Bartlett, P., & Slater, P. J. B. (1999). The effect of new recruits on the flock specific call of budgerigars (Melopsittacus undulatus). Ethology, Ecology and Evolution, 11, 139–147.

    Article  Google Scholar 

  • Bee, M. A., Kozich, C. E., Blackwell, K. J., & Gerhardt, H. C. (2001). Individual variation in advertisement calls of territorial male green frogs, Rana clamitans: implications for individual discrimination. Ethology, 107, 65–84.

    Article  Google Scholar 

  • Benson-Amram, S., Heinen, V. K., Dryer, S. L., & Holekamp, K. E. (2011). Numerical assessment and individual call discrimination by wild spotted hyaenas (Crocuta crocuta). Animal Behaviour, 82, 743–752.

    Article  Google Scholar 

  • Bouchet, H., Blois-Heulin, C., Pellier, A.-S., Zuberbühler, K., & Lemasson, A. (2012). Acoustic variability and individual distinctiveness in the vocal repertoire of red capped mangabeys (Cercocebus torquatus). Journal of Comparative Psychology, 126, 45–56.

    Article  PubMed  Google Scholar 

  • Brown, C. H., & Gomez, R. (1992). Functional design features in primate vocal signals: The acoustic habitat and sound distortion. In T. Nishida, W. M. McGrew, P. Marler, M. Pickford, & F. B. M. de Waal (Eds.), Topics in primatology (Vol. 1). Tokyo: University of Tokyo Press.

    Google Scholar 

  • Candiotti, A., Zuberbühler, K., & Lemasson, A. (2012). Convergence and divergence in Diana monkey vocalizations. Biology Letters, 8, 382–385.

    Article  PubMed  Google Scholar 

  • Catchpole, C. K., & Slater, P. J. B. (2008). Bird song: Biological themes and variations (2nd ed.). Cambridge, U.K.: Cambridge University Press.

    Book  Google Scholar 

  • Chapman, C. A. (1990). Association patterns of spider monkeys: the influence of ecology and sex of social organization. Behavioral Ecology and Sociobiology, 26, 409–414.

    Article  Google Scholar 

  • Chapman, C. A., Chapman, L. J., & Lefebvre, L. (1989). Spider monkey alarm calls: honest advertisement or warning kin? Animal Behaviour, 39, 197–198.

    Article  Google Scholar 

  • Chapman, C. A., & Weary, D. M. (1990). Variability in spider monkeys’ vocalizations may provide basis for individual recognition. American Journal of Primatology, 22, 279–284.

    Article  Google Scholar 

  • Cheney, D. L., & Seyfarth, R. M. (1980). Vocal recognition in free-ranging vervet monkeys. Animal Behaviour, 28, 362–367.

    Article  Google Scholar 

  • Crockford, C., Herbinger, I., Vigilant, L., & Boesch, C. (2004). Wild chimpanzees produce group-specific calls: a case for vocal learning? Ethology, 110, 221–243.

    Article  Google Scholar 

  • Delgado, R. A. J. (2007). Geographic variation in the long calls of male orangutans (Pongo spp.). Ethology, 113, 487–498.

    Article  Google Scholar 

  • 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, 829–835.

    Article  PubMed  Google Scholar 

  • Egnor, S. E. R., & Hauser, M. D. (2005). A paradox in the evolution of primate vocal learning. Trends in Neuroscience, 27, 649–654.

    Article  Google Scholar 

  • Ehret, G. (1990). Categorical perception of sound signals: Facts and hypotheses from animal studies. In S. Harnad (Ed.), Categorical perception: The groundwork of cognition (pp. 301–331). Cambridge, U.K.: Cambridge University Press.

    Google Scholar 

  • Eisenberg, J. F. (1976). Communication mechanisms and social integration in the black spider monkey, Ateles fusciceps robustus, and related species. Smithsonion Contributions to Zoology, 213, 1–108.

    Article  Google Scholar 

  • Farabaugh, S. M., Linzenbold, A., & Dooling, R. J. (1994). Vocal plasticity in Budgerigars (Melopsittacus undulatus): evidence for social factors in the learning of contact calls. Journal of Comparative Psychology, 108, 81–92.

    Article  PubMed  CAS  Google Scholar 

  • Fedurek, P., & Slocombe, K. E. (2011). Primate vocal communication: a useful tool for understanding human speech and language evolution? Human Biology, 83, 153–172.

    Article  PubMed  Google Scholar 

  • Fischer, J. (2002). Developmental modifications in the vocal behavior of non-human primates. In A. A. Ghazanfar (Ed.), Primate audition: Ethology and neurobiology (pp. 109–125). London: CRC Press.

    Google Scholar 

  • Fischer, J., Hammerschmidt, K., Cheney, D. L., & Seyfarth, R. M. (2001). Acoustic features of female chacma baboon barks. Ethology, 107, 33–54.

    Article  Google Scholar 

  • 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 Acoustical Society of America, 111, 1465–1474.

    Article  PubMed  Google Scholar 

  • Fitch, W. T. S. (1997). Vocal tract length and formant frequency dispersion correlate with body size in rhesus macaques. Journal of the Acoustical Society of America, 102, 1213–1222.

    Article  PubMed  CAS  Google Scholar 

  • Ford, S. M., & Davis, L. C. (1992). Systematics and body size: implications for feeding adaptations in New World Monkeys. American Journal of Physical Anthropology, 88, 415–468.

    Article  PubMed  CAS  Google Scholar 

  • Ghazanfer, A. A., & Santos, L. (2004). Primate brains in the wild: the sensory bases for social interactions. Nature Reviews Neuroscience, 5, 603–616.

    Article  Google Scholar 

  • Gros-Louis, J. (2006). Acoustic analysis and contextual description of food-associated calls in white-faced capuchin monkeys (Cebus capucinus). International Journal of Primatology, 27, 273–294.

    Article  Google Scholar 

  • Hammerschmidt, K., & Todt, D. (1995). Individual differences in vocalisations of young Barbary macaques (Macaca sylvanus): a multi-parametric analysis of to identify critical cues in acoustic signalling. Behaviour, 132, 381–399.

    Article  Google Scholar 

  • Janik, V. M., & Slater, P. J. B. (2000). The different roles of social learning in vocal communication. Animal Behaviour, 60, 1–11.

    Article  PubMed  Google Scholar 

  • Janzen, D. H. (1986). Guanacaste National Park: Tropical, ecological and cultural restoration. Editorial Universidad Estatal a Distancia, Costa Rica/Fundación Parque Nacionales. San Jose, Costa Rica.

  • 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.

    Article  Google Scholar 

  • Jorgensen, D. D., & French, J. A. (1998). Individuality but not stability in marmoset long calls. Ethology, 104, 729–742.

    Article  Google Scholar 

  • Kondo, N., & Watanabe, S. (2009). Contact calls: information and social function. Japanese Psychological Research, 51, 197–208.

    Article  Google Scholar 

  • Lemasson, A., & Hausberger, M. (2004). Patterns of vocal sharing and social dynamics in a captive group of Campbell’s monkeys (Cercopithecus campbelli campbelli). Journal of Comparative Psychology, 118, 347–359.

    Article  PubMed  Google Scholar 

  • Lemasson, A., Ouattara, K., Petit, E. J., & Zuberbühler, K. (2011). Social learning of vocal structure in a nonhuman primate? BMC Evolutionary Biology, 11, 362.

    Article  PubMed  Google Scholar 

  • Marler, P. (2004). Bird calls: A cornucopia for communication. In P. Marler & H. Slabbekoom (Eds.), Nature’s music: The science of birdsong (pp. 132–176). San Diego: Elsevier Academic Press.

    Chapter  Google Scholar 

  • Mulard, H., Aubin, T., White, J. F., Hatch, S. A., & Danchin, É. (2008). Experimental evidence of vocal recognition in young and adult black-legged kittiwakes. Animal Behaviour, 76, 1855–1861.

    Article  Google Scholar 

  • Notman, H., & Rendall, D. (2005). Contextual variation in chimpanzee pant hoots and its implications for referential communication. Animal Behaviour, 70, 177–190.

    Article  Google Scholar 

  • Owren, M. M., Seyfarth, R. M., & Hopp, S. L. (1992). Categorical vocal signalling in nonhuman primates. In H. Papousek & U. Jürgens (Eds.), Nonverbal vocal communication: Comparative and developmental approaches (pp. 102–122). Cambridge, U.K.: Cambridge University Press.

    Google Scholar 

  • Pastor-Nieto, R. (2001). Grooming, kinship, and co-feeding in captive spider monkeys (Ateles geoffroyi). Zoo Biology, 20, 293–303.

    Article  Google Scholar 

  • Ramos-Fernández, G. (2005). Vocal communication in a fission-fusion society: do spider monkeys stay in touch with close associates? International Journal of Primatology, 26, 1077–1092.

    Article  Google Scholar 

  • Ramos-Fernández, G. (2008). Communication in spider monkeys: The function and mechanisms underlying the use of whinny. In C. J. Campbell (Ed.), Spider monkeys: Behavior, ecology and evolution of the genus Ateles (pp. 220–235). Cambridge, U.K.: Cambridge University Press.

    Google Scholar 

  • Ramos-Fernández, G., & Ayala-Orozco, B. (2003). Population size and habitat use of spider monkeys at Punta Laguna, Mexico. In L. K. Marsh (Ed.), Primates in fragments: Ecology and conservation (pp. 191–209). New York: Kluwer Academic/Plenum Press.

    Chapter  Google Scholar 

  • Rukstalis, M., Fite, J. E., & French, J. A. (2003). Social change affects vocal structure in a callitrichid primate (Callithrix kuhlii). Ethology, 109, 327–340.

    Article  Google Scholar 

  • Shimooka, Y., Campbell, C. J., Di Fiore, A., Felton, A. M., Izawa, K., Link, A., et al. (2008). Demography and group composition of Ateles. In C. J. Campbell (Ed.), Spider monkeys: Behavior, Ecology and Evolution of the Genus Ateles (pp. 329–348). Cambridge: Cambridge University Press.

  • Snowdon, C. T., & Elowson, A. M. (1999). Pygmy marmosets modify call structure when paired. Ethology, 105, 893–908.

    Article  Google Scholar 

  • Snowdon, C. T., Elowson, A. M., & Roush, R. S. (1997). Social influences on vocal development in new world primates. In C. T. Snowdon & M. Hausberger (Eds.), Social influences on vocal development (pp. 234–248). Cambridge, U.K.: Cambridge University Press.

    Chapter  Google Scholar 

  • Spehar, S. N., & Di Fiore, A. (2013). Loud calls as a mechanism of social coordination in a fission-fusion taxon, the white-bellied spider monkeys (Ateles belzebuth). Behavioral Ecology and Sociobiology, 67, 947–961.

    Article  Google Scholar 

  • Spillman, B., Dunkel, L. P., van Noordwijk, M. A., Amda, R. N. A., Lameira, A. R., Wich, S. A., et al. (2010). Acoustic properties of long calls given by flanged male orang-utans (Pongo pygmaeus wurmbii) reflect both individual identity and context. Ethology, 116, 385–395.

    Google Scholar 

  • Tabachnick, B. G., & Fidell, L. S. (2007). Using multivariate statistics (5th ed.). London: Pearson International.

    Google Scholar 

  • Teixidor, P., & Byrne, R. W. (1997). Can spider monkeys (Ateles geoffroyi) discriminate vocalizations of familiar individuals and strangers? Folia Primatologica, 68, 254–264.

    Article  CAS  Google Scholar 

  • Teixidor, P., & Byrne, R. W. (1999). The ‘whinny’ of spider monkeys: individual recognition before situational meaning. Behaviour, 136, 279–308.

    Article  Google Scholar 

  • Waser, P. M. (1977). Individual recognition, intragroup cohesion and intergroup spacing: evidence from sounds playback to forest monkeys. Behaviour, 60, 28–74.

    Article  Google Scholar 

  • Wiley, R. H. (1994). Errors, exaggeration, and deception in animal communication. In L. Real (Ed.), Behavioral mechanisms in ecology (pp. 157–189). Chicago: University of Chicago Press.

    Google Scholar 

  • Wright, T. F., Dahlin, C. R., & Salinas-Melgoza, A. (2008). Stability and change in vocal dialects of the yellow-napped amazon. Animal Behaviour, 76, 1017–1027.

    Article  PubMed  Google Scholar 

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Acknowledgments

We thank Elvin Murillo, Roger Blanco, and María Marta Chavarría at Area de Conservación Guanacaste (Santa Rosa) and Nicola Forshaw, Eulogio Canul-Aban, Macedonio Canul-Chan, Juan Canul-Chan, Augusto Canul-Aban, Laura Vick, and staff at Pronatura (Punta Laguna). In addition, we thank Eric Patel and Catherine Crockford for advice on vocalization analysis, and Roger Mundry for advice on the DFA procedure. Research at Santa Rosa and Punta Laguna was supported by The British Academy, the Wenner-Gren Foundation, the Leakey Foundation, and the North of England Zoological Society. C. J. Santorelli was supported by a University of Chester Gladstone bursary and the Santander University Scheme.

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Correspondence to Claire J. Santorelli.

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Santorelli, C.J., Aureli, F., Ramos-Fernández, G. et al. Individual Variation of Whinnies Reflects Differences in Membership Between Spider Monkey (Ateles geoffroyi) Communities. Int J Primatol 34, 1172–1189 (2013). https://doi.org/10.1007/s10764-013-9736-2

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