International Journal of Primatology

, Volume 36, Issue 2, pp 429–440 | Cite as

Role of Emitter and Severity of Aggression Influence the Agonistic Vocalizations of Geoffroy’s Spider Monkeys (Ateles geoffroyi)

  • José D. Ordóñez-GómezEmail author
  • Jacob C. Dunn
  • Víctor Arroyo-Rodríguez
  • María G. Méndez-Cárdenas
  • Alejandra Márquez-Arias
  • Ana M. Santillán-DohertyEmail author


Natural selection has resulted in the acoustic convergence of many animal vocalizations. During agonistic interactions vocalizations may vary depending on the role an individual plays in the interaction and on the severity of the attack. Motivation-structural rules describe how aggressors are thought to have evolved to use low-frequency vocalizations, whereas victims often use high-frequency vocalizations. This is because call frequency (Hz) is negatively related to body size across species. Motivational theory predicts that during more severe attacks, vocal structure will also change in response to increased arousal, leading to the production of noisy (high-entropy) vocalizations. Little is known about the acoustic characteristics of vocalizations produced during agonistic encounters in primates, and the limited available data are highly biased toward Old World species. Here, we evaluated the effect of the role of the emitter (aggressor or victim) and the severity of the behavior (with or without contact) on the acoustic parameters of 185 agonistic vocalizations emitted by 15 spider monkeys (Ateles geoffroyi) in two captive groups. Our results supported the predictions of both the motivation-structural rules and motivational theory: Call frequency (Hz) was lower in aggressors than in victims and lower during high-severity encounters than low-severity encounters. Further, average entropy was higher during high-severity encounters. These findings suggest that the agonistic vocalizations of spider monkeys convey information about both the role of the emitter and the severity of the interaction.


Agonism Arousal Entropy Motivation-structural rules Motivational theory 



We thank to G. Castañeda-López, N. Arce-Peña, and J. Hernández-Meléndez for their important help in the field and Roger Mundry for providing instructions and scripts for the pDFA analysis. We also appreciate the support of the Posgrado en Ciencias Biológicas from the Universidad Nacional Autónoma de México and the Estación de Primatología from the Universidad Veracruzana. J. D. Ordóñez-Gómez was supported by a fellowship from the CONACyT and J. C. Dunn was supported by the Isaac Newton Trust. Finally, we thank Robert Seyfarth, Dorothy Cheney, two anonymous reviewers, and the editor-in-chief, Joanna Setchell for their very helpful suggestions and comments on previous versions of the manuscript.

Supplementary material

10764_2015_9833_MOESM1_ESM.doc (88 kb)
ESM 1 (DOC 88 kb)


  1. Altmann, J. (1974). Observational study of behaviour: Sampling methods. Behaviour, 49, 227–267.CrossRefPubMedGoogle Scholar
  2. Aureli, F., & Schaffner, C. M. (2008). Social interactions, social relationships and the social system of spider monkeys. In C. J. Campbell (Ed.), Spider monkeys: The Biology, Behavior and Ecology of the Genus Ateles (pp. 236–265). Cambridge, U.K.: Cambridge University Press.Google Scholar
  3. Banse, R., & Scherer, K. R. (1996). Acoustic profiles in vocal emotion expression. Journal of Personality and Social Psychology, 70, 614–636.Google Scholar
  4. Bates, D., Maechler, M., & Bolker B. (2011). lme4: Linear mixed-effects models using S4 classes. R package version 0.999375–42.
  5. Berry, D. A., Herzel, H., Titze, I. R., & Story, B. (1996). Bifurcations in excised larynx experiments. Journal of Voice, 10, 129–138.CrossRefPubMedGoogle Scholar
  6. Box, G. E. P., & Cox, D. R. (1964). An analysis of transformations. Journal of the Royal Statistical Society. Series B (Methodological), 26, 211–252.Google Scholar
  7. Chapman, C. A., & Weary, D. M. (1990). Variability in spider monkey´s vocalizations may provide basis for individual recognition. American Journal of Primatology, 22, 279–284.CrossRefGoogle Scholar
  8. Chapman, C. A., Wrangham, R. W., & Chapman, L. J. (1995). Ecological constraints on group size: An analysis of spider monkey and chimpanzee subgroups. Behavioral Ecology and Sociobiology, 36, 59–70.Google Scholar
  9. Collias, N. E. (1960). An ecological and functional classification of animal sounds. In W. E. Lanyon & W. N. Tavolga (Eds.), Animal sounds and communication (pp. 368–391). Washington, DC: American Institute of Biological Sciences.Google Scholar
  10. Darwin, C. (1872). The expressions of the emotions in man and animals. New York: D. Appleton.CrossRefGoogle Scholar
  11. Eisenberg, J. F., & Kuehn, R. E. (1966). The behavior of Ateles geoffroyi and related species. Washington: Smithsonian Miscellaneous.Google Scholar
  12. Ey, E., Pfefferle, D., & Fischer, J. (2007). Do age- and sex-related variations reliably reflect body size in non-human primate vocalizations? A review. Primates, 48, 253–257.Google Scholar
  13. 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.Google Scholar
  14. Fitch, W. T., Neubauer, J., & Herzel, H. (2002). Calls out of chaos: the adaptive significance of nonlinear phenomena in mammalian vocal production. Animal Behaviour, 63, 407–418.Google Scholar
  15. Gaona-González, A., Santillán-Doherty, A. M., Arenas-Rosas, R. V., Muñoz-Delgado, J., Aguillón-Pantaleón, M. A., Ordóñez-Gómez, J. D., & Márquez-Arias, A. (2011). Recording vocalizations with bluetooth technology. Behavior Research Methods, 43, 340–352.Google Scholar
  16. Goudbeek, M., & Scherer, K. (2010). Beyond arousal: valence and potency/control cues in the vocal expression of emotion. Journal of the Acoustical Society of America, 128, 1322–1336.Google Scholar
  17. Gouzoules, H., & Gouzoules, S. (1989). Design features and developmental modification of pigtail macaque, Macaca nemestrina, agonistic screams. Animal Behaviour, 37, 383–401.CrossRefGoogle Scholar
  18. Gouzoules, H., & Gouzoules, S. (2000). Agonistic screams differ among four species of macaques: the significance of motivation-structural rules. Animal Behaviour, 59, 501–512.Google Scholar
  19. Gouzoules, S., Gouzoules, H., & Marler, P. (1984). Rhesus monkey (Macaca mulatta) screams: representational signalling in the recruitment of agonistic aid. Animal Behaviour, 32, 182–193.Google Scholar
  20. Hauser, M. D. (1993). The evolution of nonhuman primate vocalizations: Effects of phylogeny, body weight, and social context. The American Naturalist, 142, 528–542.CrossRefPubMedGoogle Scholar
  21. King, J. A. (1973). The ecology of aggressive behavior. Annual Review of Ecology and Systematics, 4, 117–138.Google Scholar
  22. Lemasson, A., Remeuf, K., Rossard, A., & Zimmermann, E. (2012). Cross-taxa similarities in affect-induced changes of vocal behavior and voice in arboreal monkeys. PLoS ONE, 7(9), e45106.CrossRefPubMedCentralPubMedGoogle Scholar
  23. Lenth, R. V. (2013). Using the lsmeans Package. The University of Iowa. Updated with lsmeans Version 1.10, July 4, 2013.Google Scholar
  24. McCowan, B., & Rommeck, I. (2006). Bioacoustic monitoring of aggression in grouped-housed rhesus macaques. Journal of Applied Animal Welfare Science, 9, 261–268.Google Scholar
  25. Morton, E. S. (1977). On the occurrence and significance of motivation-structural rules in some bird and mammal sounds. The American Naturalist, 111, 855–869.CrossRefGoogle Scholar
  26. Mundry, R., & Sommer, C. (2007). Discriminant function analysis with nonindependent data: consequences and an alternative. Animal Behaviour, 74, 965–976.Google Scholar
  27. Nieburg, H. L. (1970). Agonistics-rituals of conflict. Annals of the American Academy of Political and Social Science, 391, 56–73.CrossRefGoogle Scholar
  28. Owren, M. J., Amoss, R. T., & Rendall, D. (2011). Two organizing principles of vocal production: Implications for nonhuman and human primates. American Journal of Primatology, 73, 530–544.Google Scholar
  29. Owren, M. J., & Rendall, D. (1997). An affect-conditioning model of nonhuman primate vocal signaling. In D. H. Owings, M. D. Beecher, & N. S. Thompson (Eds.), Perspectives in Ethology (pp. 299–346). New York: Plenum Press.Google Scholar
  30. 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.CrossRefGoogle Scholar
  31. R Development Core Team. (2007). R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.
  32. 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.CrossRefGoogle Scholar
  33. Slocombe, K. E., Kaller, T., Call, J., & Zuberbühler, K. (2010). Chimpanzees extract social information from agonistic screams. PloS ONE, 5(7), e11473.CrossRefPubMedCentralPubMedGoogle Scholar
  34. Slocombe, K. E., & Zuberbühler, K. (2005). Agonistic screams in wild chimpanzees (Pan troglodytes schweinfurthii) vary as a function of social role. Journal of Comparative Psychology, 119, 67–77.CrossRefPubMedGoogle Scholar
  35. Slocombe, K. E., & Zuberbühler, K. (2007). Chimpanzees modify recruitment screams as a function of audience composition. Proceedings of the National Academy of Sciences of the United States of America, 104, 17228–17233.Google Scholar
  36. Symington, M. M. (1990). Fission-fusion social organization in Ateles and Pan. International Journal of Primatology, 11, 47–61.CrossRefGoogle Scholar
  37. Teixidor, P., & Byrne, R. W. (1999). The ‘whinny’ of spider monkeys: Individual recognition before situational meaning. Behaviour, 136, 279–308.CrossRefGoogle Scholar
  38. Venables, W. N., & Ripley, B. D. (2002). Modern applied statistics with S. New York: Springer Science + Business Media.CrossRefGoogle Scholar
  39. Wilden, I., Herzel, H., Peters, G., & Tembrock, G. (1998). Subharmonics, biphonation, and deterministic chaos in mammal vocalization. Bioacoustics: The International Journal of Animal Sound and its Recording, 9, 171–196.Google Scholar
  40. Wittig, R. M., Crockford, C., Langergraber, K. E., & Zuberbühler, K. (2014). Triadic social interactions operate across time: a field experiment with wild chimpanzees. Proceedings of the Royal Society B, 281, 20133155.Google Scholar

Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  1. 1.Posgrado en Ciencias BiológicasUniversidad Nacional Autónoma de MéxicoMexico CityMexico
  2. 2.Division of Biological AnthropologyUniversity of CambridgeCambridgeU.K.
  3. 3.Centro de Investigaciones en EcosistemasUniversidad Nacional Autónoma de MéxicoMoreliaMexico
  4. 4.Instituto de Investigaciones AntropológicasUniversidad Nacional Autónoma de MéxicoMexico CityMexico
  5. 5.NeurocienciasInstituto Nacional de Psiquiatría Ramón de la Fuente MuñizMexico CityMexico

Personalised recommendations