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Rhesus macaques (Macaca mulatta) recognize group membership via olfactory cues alone

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Abstract

The ability to distinguish group members from conspecifics living in other groups is crucial for gregarious species. Olfaction is known to play a major role in group recognition and territorial defense in a wide range of mammalian taxa. Although primates have been typically regarded as microsmatic (having a poor sense of smell), increasing evidence suggests that olfaction may play a greater role in primates’ social life than previously assumed. In this study, we carried out behavioral bioassays using a signaler-receiver paradigm to investigate whether rhesus macaques (Macaca mulatta) can discriminate between body odors of female group members and females from different social groups. We conducted the study on the research island Cayo Santiago, Puerto Rico, in the non-mating season and controlled for kinship and familiarity using extensive pedigree and demographic data. Our results indicate that both males and females inspect out-group odors significantly longer than in-group odors. Males licked odors more often than females, and older animals licked more often than younger ones. Furthermore, individuals tended to place their nose longer towards odors when the odor donor’s group rank was higher than the rank of their own group. Reuse of odor samples decreased odor intensity (rated by human experimenters) during the course of a given test day and with longer exposure to ambient air; however, the reuse of odor samples did not significantly influence the response behaviors. Our findings uncover key roles of olfactory communication in a species not possessing distinct scent glands and thus shed light into the evolution of primate olfactory communication.

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Acknowledgments

We thank the Caribbean Primate Research Center for permission to conduct this study and appreciate the support of the staff of the Cayo Santiago Field Station, especially the census taker Edgar Davila, Julio Resto, Nahirí Rivera, and Giselle Caraballo Cruz for their cooperation throughout the experimental study and during the collection of the DNA samples. Fred Bercovitch, Matt Kessler, John Berard, Michael Krawczak, Peter Nürnberg, and Jörg Schmidtke are acknowledged for starting the genetic database of the Cayo Santiago population in the 1990s. Furthermore, we are grateful to Stefanie Bley and Laura Muniz for improving the genetic database and to Linda Vigilant for providing laboratory access. We also thank Michael Krawczak and Olaf Junge for access to a management program of genetic data (FINDSIRE). Megan Hoffman is kindly acknowledged for her invaluable support during the field period, Kati Drechsel for her assistance during the collection of odor samples, and Doreen Langos for her continuous support in the field. We are further extremely grateful to Roger Mundry and Lars Kulik for their support during the statistical analysis and to Cleve Hicks, Jo Bennett, and the three anonymous reviewers for their valuable comments on earlier drafts of the manuscript. The population of Cayo Santiago was supported by grant number 8 P40 OD012217 from the National Center for Research Resources (NCRR), the Office of Research Infrastructure Programs (ORIP) of the National Institutes of Health and the Medical Sciences Campus of the University of Puerto Rico. The content of this publication is solely the responsibility of the authors and does not necessarily represent the official views of NCRR or ORIP. The study was conducted within the Jr. Research Group of Primate Kin Selection, an Emmy-Noether Group funded by the German Research Foundation (grant no. WI 1808/1-1, 1-2, 2-1, 3-1 awarded to AW). We thank the Max Planck Institute for Evolutionary Anthropology in Leipzig for their logistic support and for hosting the Jr. Research Group of Primate Kin Selection and the University of Leipzig for graduate funding awarded to SH.

Ethical standards

This study was conducted in accordance with the guidelines of the Association for the Study of Animal Behaviour/Animal Behavior Society for the use of animals in research, the legal requirements of the country in which the work was carried out, and all institutional guidelines. All research procedures were approved by the CPRC and the Institutional Animal Care and Use Committee (IACUC) of the University of Puerto Rico (protocol number 4060105).

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Authors and Affiliations

  1. Behavioral Ecology Research Group, Institute of Biology, Faculty of Bioscience, Pharmacy and Psychology, University of Leipzig, Talstrasse 33, 04103, Leipzig, Germany

    Stefanie Henkel, Angelina Ruiz Lambides, Ruth Thomsen & Anja Widdig

  2. Department of Developmental and Comparative Psychology, Max Planck Institute for Evolutionary Anthropology, Deutscher Platz 6, 04103, Leipzig, Germany

    Stefanie Henkel

  3. Junior Research Group of Primate Kin Selection, Department of Primatology, Max Planck Institute for Evolutionary Anthropology, Deutscher Platz 6, 04103, Leipzig, Germany

    Angelina Ruiz Lambides & Anja Widdig

  4. Caribbean Primate Research Center, University of Puerto Rico, Medical Sciences Campus, Puerto Rico, USA

    Angelina Ruiz Lambides

  5. Leibniz Institute for Zoo and Wildlife Research, Alfred-Kowalke-Str. 17, 10315, Berlin, Germany

    Anne Berger

  6. Department of Anthropology, University College London, Gower Street, London, WC1E 6BT, UK

    Ruth Thomsen

  7. Department of Primatology, Max Planck Institute for Evolutionary Anthropology, Deutscher Platz 6, 04103, Leipzig, Germany

    Ruth Thomsen

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  1. Stefanie Henkel
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  2. Angelina Ruiz Lambides
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  3. Anne Berger
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  4. Ruth Thomsen
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  5. Anja Widdig
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Correspondence to Stefanie Henkel.

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Communicated by E. Huchard

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Henkel, S., Lambides, A.R., Berger, A. et al. Rhesus macaques (Macaca mulatta) recognize group membership via olfactory cues alone. Behav Ecol Sociobiol 69, 2019–2034 (2015). https://doi.org/10.1007/s00265-015-2013-y

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  • DOI: https://doi.org/10.1007/s00265-015-2013-y

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