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Acoustic and Temporal Variation in Gelada (Theropithecus gelada) Loud Calls Advertise Male Quality

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Abstract

Many animals rely on information from vocal signals to assess potential competitors and mates. For example, in primates, males use loud calls to assess rivals when the acoustic properties of the calls reliably indicate the condition or quality of the sender. Here, we investigate whether the loud calls of male geladas (Theropithecus gelada) function as a quality signal. Gelada males produce loud calls during ritualistic chases with rival males. Given the physically taxing nature of these displays, we hypothesize that variation in the acoustic properties of loud calls reliably signal male stamina or competitive ability. To test this hypothesis, we examined whether the acoustic properties of the gelada loud call varied in relation to individual, age, status, and exhaustion. Specifically, we examined 12 call parameters (e.g., fundamental frequency) and 3 bout parameters (e.g., number of calls per bout), that have been previously shown to vary across condition in male primates. We found that several acoustic features varied consistently across age and status such that males deemed higher quality in gelada society (e.g., high status) produced more calls per bout, produced calls that were lower in overall frequency measures, and exhibited a greater vocal range. In addition, we found that similar acoustic features varied with exhaustion; after a long chase event, males produced both fewer calls per bout and calls with higher spectral measures. Results from this study are consistent with the hypothesis that gelada loud calls are quality signals, contributing to the growing evidence that primates may use acoustic information to assess the quality of a rival or a potential mate.

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References

  • Aich, H., Moos-Heilen, R., & Zimmermann, E. (1990). Vocalizations of adult gelada baboons (Theropithecus gelada): acoustic structure and behavioural context. Folia Primatologica, International Journal of Primatology, 55(3), 109–132.

    Article  CAS  Google Scholar 

  • Barelli, C., Mundry, R., Heistermann, M., & Hammerschmidt, K. (2013). Cues to androgens and quality in male gibbon songs. PLoS ONE, 8(12), e82748.

    Article  PubMed  PubMed Central  Google Scholar 

  • Bates, D., Maechler, M., Bolker, B., Walker, S., Christensen, R. H. B., et al. (2015). Package lme4. (http://lme4.r-forge.r-project.org/).

  • Beehner, J. C., Gesquiere, L., Seyfarth, R. M., Cheney, D. L., Alberts, S. C., Altmann, J. (2015). Corrigendum to “Testosterone related to age and life-history stages in male baboons and geladas.” [Hormones and Behavior 56/4 (2009) 472–480]. Hormones and Behavior.

  • Bergman, T. J. (2010). Experimental evidence for limited vocal recognition in a wild primate: implications for the social complexity hypothesis. Proceedings of the Royal Society of London B: Biological Sciences, 277, 3045–3053.

    Article  Google Scholar 

  • Bergman, T. J., & Sheehan, M. J. (2013). Social knowledge and signals in primates. American Journal of Primatology, 75, 683–694.

    Article  PubMed  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 

  • Caselli, C. B., Mennill, D. J., Bicca-Marques, J. C., & Setz, E. Z. (2014). Vocal behavior of black-fronted titi monkeys (Callicebus nigrifrons): acoustic properties and behavioral contexts of loud calls. American Journal of Primatology, 76, 788–800.

    Article  PubMed  Google Scholar 

  • Darwin, C. (1871). The descent of man and selection in relation to sex. London: John Murray.

    Book  Google Scholar 

  • Delgado, R. A. (2006). Sexual selection in the loud calls of male primates: signal content and function. International Journal of Primatology, 27(1), 5–25.

    Article  Google Scholar 

  • Dunbar, R. I. M. (1983). Structure of gelada baboon reproductive units. II. Social relationships between reproductive females. Animal Behaviour, 31, 556–564.

    Article  Google Scholar 

  • Dunbar, R. I. M. (1984). Reproductive decisions: An economic analysis of gelada baboon social strategies. Princeton: Princeton University Press.

    Google Scholar 

  • Dunbar, R. I. M., & Dunbar, P. (1975). Social dynamics of gelada baboons. In H. Kuhn, W. P. Luckett, C. R. Noback, A. H. Schultz, D. Starck, & F. S. Szalay (Eds.), Contributions to primatology. Basel: S. Karger.

    Google Scholar 

  • Erb, W. M., Hodges, J. K., & Hammerschmidt, K. (2013). Individual, contextual, and age-related acoustic variation in simakobu (Simias concolor) loud calls. PLoS ONE, 8, e83131.

    Article  PubMed  PubMed Central  Google Scholar 

  • 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, Journal of Primatology, 48, 253–267.

    Article  CAS  PubMed  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. The Journal of the Acoustical Society of America, 111, 1465–1474.

    Article  PubMed  Google Scholar 

  • 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, 140–148.

  • Fischer, J., Noser, R., & Hammerschmidt, K. (2013). Bioacoustic field research: a primer to acoustic analyses and playback experiments with primates. American Journal of Primatology, 75, 643–663.

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Fitch, W. T., & Hauser, M. D. (1995). Vocal production in nonhuman primates: acoustics, physiology, and functional constraints on “honest” advertisement. American Journal of Primatology, 37, 191–219.

    Article  Google Scholar 

  • Gerhardt, H. C., Tanner, S. D., Corrigan, C. M., & Walton, H. C. (2000). Female preference functions based on call duration in the gray tree frog (Hyla versicolor). Behavioral Ecology, 11, 663–669.

    Article  Google Scholar 

  • Hall, K. R. L., & DeVore, I. (1965). Baboon social behavior. In I. DeVore (Ed.), Primate behavior: Field studies of monkeys and apes (pp. 53–110). New York: Holt, Rinehart and Winston.

    Google Scholar 

  • Holt, M. M., Noren, D. P., Dunkin, R. C., & Williams, T. M. (2015). Vocal performance affects metabolic rate in dolphins: implications for animals communicating in noisy environments. The Journal of Experimental Biology, 218, 1647–1654.

    Article  PubMed  Google Scholar 

  • Inoue, M. (1988). Age gradations in vocalization and body weight in Japanese monkeys (Macaca fuscata). Folia Primatologica, 51, 76–86.

    Article  CAS  Google Scholar 

  • Kawai, M., Ohsawa, H., Mori, U., & Dunbar, R. (1983). Social organization of gelada baboons: Social units and definitions. Primates, Journal of Primatology, 24, 13–24.

    Article  Google Scholar 

  • Kitchen, D. M., Seyfarth, R. M., Fischer, J., & Cheney, D. L. (2003). Loud calls as indicators of dominance in male baboons (Papio cynocephalus ursinus). Behavioral Ecology and Sociobiology, 53, 374–384.

    Google Scholar 

  • le Roux, & Bergman. (2012). Indirect rival assessment in a social primate, Theropithecus gelada. Animal Behaviour, 83, 249–255.

    Article  Google Scholar 

  • McComb, K. (1991). Female choice for high roaring rates in red deer, Cervus elaphus. Animal Behaviour, 41, 79–88.

    Article  Google Scholar 

  • Méndez-Cárdenas, M., Randrianambinina, B., Rabesandratana, A., Rasoloharijaona, S., & Zimmermann, E. (2008). Geographic variation in loud calls of sportive lemurs (Lepilemur ssp.) and their implications for conservation. American Journal of Primatology, 70, 828–838.

    Article  PubMed  Google Scholar 

  • Mori, U. (1979a). Social structure of gelada baboons. In M. Kawai (Ed.), Ecological and sociological studies of gelada baboons (Vol. 16, pp. 243–247). Basel: S. Karger.

    Google Scholar 

  • Mori, U. (1979b). Unit formation and the emergence of a new leader. In M. Kawai (Ed.), Ecological and sociological studies of gelada baboons (Vol. 16, pp. 155–181). Basel: S. Karger.

    Google Scholar 

  • Mougeot, F., Irvine, J. R., Seivwright, L., Redpath, S. M., & Piertney, S. (2004). Testosterone, immunocompetence, and honest sexual signaling in male red grouse. Behavioral Ecology, 15, 930–937.

    Article  Google Scholar 

  • Mundry, R., & Fischer, J. (1998). Use of statistical programs for nonparametric tests of small samples often leads to incorrect p values: Examples from animal behaviour. Animal Behaviour, 56, 256–259.

    Article  PubMed  Google Scholar 

  • Mundry, R., & Sommer, C. (2007). Discriminant function analysis with nonindependent data: consequences and an alternative. Animal Behaviour, 74, 965–976.

    Article  Google Scholar 

  • Neumann, C., Assahad, G., Hammerschmidt, K., Perwitasari-Farajallah, D., & Engelhardt, A. (2010). Loud calls in male crested macaques, Macaca nigra: a signal of dominance in a tolerant species. Animal Behaviour, 79, 187–193.

    Article  Google Scholar 

  • Pfefferle, D., & Fischer, J. (2006). Sounds and size: identification of acoustic variables that reflect body size in hamadryas baboons, Papio hamadryas. Animal Behaviour, 72, 43–51.

    Article  Google Scholar 

  • Reby, D., McComb, K., Cargnelutti, B., Darwin, C., Fitch, W. T., & Clutton-Brock, T. (2005). Red deer stags use formants as assessment cues during intrasexual agonistic interactions. Proceedings of the Royal Society of London B: Biological Sciences, 272(1566), 941–947.

    Article  Google Scholar 

  • Riede, T., Arcadi, A. C., & Owren, M. J. (2007). Nonlinear acoustics in the pant hoots of common chimpanzees (Pan troglodytes): vocalizing at the edge. The Journal of the Acoustical Society of America, 121, 1758–1767.

    Article  PubMed  Google Scholar 

  • Snyder-Mackler, N., Alberts, S. C., & Bergman, T. J. (2014). The socio-genetics of a complex society: female gelada relatedness patterns mirror association patterns in a multilevel society. Molecular Ecology, 23, 6179–6191.

    Article  PubMed  Google Scholar 

  • Spillmann, B., Dunkel, L. P., Van Noordwijk, M. A., Amda, R. N., Lameira, A. R., 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.

    Article  Google Scholar 

  • Thomas, R. J. (2002). The costs of singing in nightingales. Animal Behaviour, 63, 959–966.

    Article  Google Scholar 

  • Titze, I. R., & Riede, T. (2010). A cervid vocal fold model suggests greater glottal efficiency in calling at high frequencies. PLoS Computational Biology, 6, e1000897.

    Article  PubMed  PubMed Central  Google Scholar 

  • Tomasello, M., & Call, J. (1997). Primate cognition. New York: Oxford University Press.

    Google Scholar 

  • Vehrencamp, S. (2000). Handicap, index, and conventional signal elements of bird song. In Y. Espmark, T. Amundsen, & G. Rosenqvist (Eds.), Animal signals: signalling and signal design in animal communication (pp. 227–300). Trondheim: Tapir Academic Press.

    Google Scholar 

  • Wagner, W. E. (1992). Deceptive or honest signalling of fighting ability? A test of alternative hypotheses for the function of changes in call dominant frequency by male cricket frogs. Animal Behaviour, 44, 449–462.

    Article  Google Scholar 

  • Ward, S., Speakman, J. R., & Slater, P. J. (2003). The energy cost of song in the canary, Serinus canaria. Animal Behaviour, 66, 893–902.

    Article  Google Scholar 

  • Wich, S. A., Van der Post, D. J., Heistermann, M., Möhle, U., Van Hooff, J., & Sterck, E. H. M. (2003). Life-phase related changes in male loud call characteristics and testosterone levels in wild Thomas langurs. International Journal of Primatology, 24, 1251–1265.

    Article  Google Scholar 

  • Zahavi, A. (1975). Mate selection: a selection for a handicap. Journal of Theoretical Biology, 53, 205–214.

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

We thank the Ethiopian Wildlife Conservation Authority (EWCA) as well as the wardens and staff of the Simien Mountain National Park for permission and support in conduction research on geladas. We are extremely grateful to M. Gomery for her assistance recording vocalizations, R. Mundry for statistical advice, and K. Hammerschmidt for help with acoustic analysis and software. We also thank all the members of the University of Michigan Gelada Research Project for assistance in data collection and valuable insight on analyses and interpretation. Many thanks go to the editors J. Setchell and J. Higham, as well as to C. Neumann and an anonymous reviewer for insightful comments that greatly improved the manuscript. This project was funded by the National Science Foundation (IOS-1255974, BCS-0715179, BCS-1231790), the NSF Graduate Research Fellowship Program, the Leakey Foundation, and the University of Michigan.

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Authors and Affiliations

  1. Department of Anthropology, University of Michigan, Ann Arbor, MI, 48109, USA

    Marcela E. Benítez & Jacinta C. Beehner

  2. Department of Psychology, University of Michigan, Ann Arbor, MI, 48109, USA

    Marcela E. Benítez, Jacinta C. Beehner & Thore J. Bergman

  3. Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, MI, 48109, USA

    Thore J. Bergman

  4. Department of Zoology and Entomology, University of the Free State, Qwaqwa, South Africa

    Aliza le Roux

  5. Cognitive Ethology Laboratory, German Primate Center, 37077, Göttingen, Germany

    Julia Fischer

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  1. Marcela E. Benítez
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  2. Aliza le Roux
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  4. Jacinta C. Beehner
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Correspondence to Marcela E. Benítez.

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Handling Editor: James Higham

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Benítez, M.E., le Roux, A., Fischer, J. et al. Acoustic and Temporal Variation in Gelada (Theropithecus gelada) Loud Calls Advertise Male Quality. Int J Primatol 37, 568–585 (2016). https://doi.org/10.1007/s10764-016-9922-0

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