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Tolerant and intolerant macaques differ in the context specificity of their calls and how they ‘comment’ on the interactions of others

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Abstract

The ‘social complexity hypothesis for communicative complexity’ posits that living in a complex social system requires complex communication skills. Since the complexity of a system can be measured by the amount of uncertainty it produces, we tested this hypothesis by studying species of macaque that differ in social tolerance and uncertainty of social interactions. We studied vocal communication in groups of macaques belonging to four species: Japanese and rhesus macaques, which are characterized by low levels of social tolerance and low uncertainty in the outcome of social interactions, and Tonkean and crested macaques, which display high levels of tolerance and uncertainty in interactions. We recorded the vocalizations emitted by adult females in agonistic, affiliative and neutral contexts. We measured call duration, entropy and time and frequency energy quantiles and processed these variables using cluster analyses and permutational multivariate analyses of variance. We found that tolerant macaques had a weaker relationship between the acoustic structure of calls and their context of emission compared to intolerant macaques. The study of ‘commenting calls’, i.e. calls made by individuals attending interactions between groupmates, also showed that their acoustic structure was more differentiated from other calls in tolerant Tonkean and crested macaques than in intolerant rhesus macaques. The flexibility of vocal production therefore appears to be correlated with the level of uncertainty of social interactions. Species with more complex social interactions were also those with higher degree of freedom in the association between acoustic structure and social context, which supports the social complexity hypothesis.

Significance statement

Is there a relationship between the complexity of social systems and the complexity of communication skills? Animals living in complex social environments are expected to use a wide variety of messages related to different goals and contexts. The complexity of a system can be assessed by the amount of uncertainty it can produce. We investigated the complexity of vocal communication by comparing two species of macaque displaying low uncertainty in their social interactions, with two other macaque species displaying high levels of uncertainty in their interactions. The comparison showed that call flexibility was related to uncertainty levels. Species with higher levels of uncertainty had weaker associations between acoustic structure and social context. These results support the hypothesis of a link between social system complexity and communication complexity, which has important implications for our understanding of the evolution of social and communication systems.

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Data availability

The dataset generated and analysed in the study is available as supplementary material (ESM2).

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Acknowledgements

We thank the keepers and managers of the Parco Faunistico di Piano dell’Abatino in Rieti, the Zoo de l’Orangerie in Strasbourg, the Biomedical Primate Research Center in Rijswijk and the Primate Research Institute in Inuyama for their valuable help. We are grateful to S. Louazon and V. Biquand for their technical assistance. The Indonesian State Ministry of Research and Technology (RISTEK), the Directorate General of Forest Protection and Nature Conservation (PHKA), the Agricultural University of Bogor, the Department for the Conservation of Natural Resources (BKSDA, North Sulawesi), and the staff of the Macaca Nigra Project supported the collection of data in crested macaques.

Funding

The Fondazione Ethoikos, the Fondation des Treilles and the Département d’Écologie, Physiologie et Éthologie (CNRS IPHC) funded the work. The Japan Society for the Promotion of Science funded the collection of data in Japanese macaques. An Eole Scholarships granted by the French-Dutch Network financed the collection of data in rhesus macaques.

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Authors and Affiliations

  1. Physiologie de la Reproduction et des Comportements, CNRS, INRAE, Université de Tours, Nouzilly, France

    Nancy Rebout, Jean-Christophe Lone, Reinier F. van den Berg & Bernard Thierry

  2. Fondazione Ethoikos, Radicondoli, Italy

    Nancy Rebout, Arianna De Marco & Andrea Sanna

  3. Parco Faunistico di Piano dell’Abatino, Poggio San Lorenzo, Italy

    Arianna De Marco

  4. Centre for Comparative and Evolutionary Psychology, Department of Psychology, University of Portsmouth, Portsmouth, UK

    Jérôme Micheletta

  5. Macaca Nigra Project, Tangkoko Reserve, Batu Putih, Indonesia

    Jérôme Micheletta

  6. Department of Biology, Animal Behaviour & Cognition, Utrecht University, Utrecht, Netherlands

    Elisabeth H. M. Sterck

  7. Animal Science Department, Biomedical Primate Research Center, Rijswijk, Netherlands

    Elisabeth H. M. Sterck & Jan A. M. Langermans

  8. Department Population Health Sciences, Veterinary Faculty, Utrecht University, Utrecht, Netherlands

    Jan A. M. Langermans

  9. EthoS (Éthologie Animale et Humaine), Université de Rennes, Normandie Université, CNRS, Rennes, France

    Alban Lemasson

  10. Institut Universitaire de France, Paris, France

    Alban Lemasson

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  1. Nancy Rebout
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  2. Arianna De Marco
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  9. Bernard Thierry
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Correspondence to Bernard Thierry.

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The study followed the ASAB/ABS guidelines for the treatment of animals in behavioural research as published in Animal Behaviour (2005, 69:i–vi). It complied with the legal requirements of the French, Italian, Dutch, Japanese and Indonesian governments. Research was observational and did not include any experimental intervention, so no review by an ethics committee was required.

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Rebout, N., De Marco, A., Sanna, A. et al. Tolerant and intolerant macaques differ in the context specificity of their calls and how they ‘comment’ on the interactions of others. Behav Ecol Sociobiol 76, 67 (2022). https://doi.org/10.1007/s00265-022-03177-7

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