Cooperation with closely bonded individuals reduces cortisol levels in long-tailed macaques

Martina Stocker; Matthias Claudio Loretto; Elisabeth H.M. Sterck; Thomas Bugnyar; Jorg J.M. Massen

doi:10.1098/rsos.191056

Cooperation with closely bonded individuals reduces cortisol levels in long-tailed macaques

Martina Stocker^*
, Matthias Claudio Loretto
, Elisabeth H.M. Sterck
, Thomas Bugnyar
, Jorg J.M. Massen

^*Corresponding author for this work

University of Vienna
Biomedical Primate Research Centre
Max Planck Institute of Animal Behavior
University of Konstanz
Biomedical Primate Research Centre BPRC)

Research output: Contribution to journal › Article › Academic › peer-review

Abstract

Many animal species cooperate with conspecifics in various social contexts. While ultimate causes of cooperation are being studied extensively, its proximate causes, particularly endocrine mechanisms, have received comparatively little attention. Here, we present a study investigating the link between the hormone cortisol, cooperation and social bonds in long-tailed macaques (Macaca fascicularis). We tested 14 macaques in a dyadic cooperation task (loose-string paradigm), each with two partners of different social bond strength and measured their salivary cortisol before and after the task. We found no strong link between the macaques’ cortisol level before the task and subsequent cooperative success. By contrast, we did find that the act of cooperating in itself led to a subsequent decrease in cortisol levels, but only when cooperating with closely bonded individuals. Two control conditions showed that this effect was not due to the mere presence of such an individual or the pulling task itself. Consequently, our study shows an intricate way in which the hypothalamic–pituitary–adrenal axis is involved in cooperation. Future studies should reveal whether and how our findings are driven by the anxiolytic effect of oxytocin, which has been associated with social bonding.

Original language	English
Article number	191056
Number of pages	12
Journal	Royal Society Open Science
Volume	7
Issue number	5
DOIs	https://doi.org/10.1098/rsos.191056
Publication status	Published - 1 May 2020

Funding

Ethics. The study complied with the Association for the Study of Animal Behaviour Behaviour/Animal Behaviour Society Guidelines for the Use of Animals in Research (Animal Behaviour, 2018, 135, I-X) and was carried out after approval of the BPRC’s Animal Welfare Committee (IvD 002a) and in accordance with the Dutch legal requirements. The macaques were never water or food deprived and training/testing was based on their voluntary participation. Data accessibility. All data and R scripts are archived in the Dryad Digital Repository: https://dx.doi.org/10.5061/dryad. g6kh12j [94]. Authors’ contributions. M.S. and J.M. conceived of the study and designed it; M.S. carried out animal training, data collection, hormone and data analysis and drafted the manuscript; M.S. and M.L. carried out the statistical analyses; E.S. and T.B. contributed to the interpretation of the findings; J.M. coordinated the study and helped draft the manuscript. All authors gave final approval for publication. Competing interests. We have no competing interests. Funding. M.S. and J.M. were supported by the FWF (Austrian Science Fund, P 26806 to J.M.) and the IPS (International Primatological Society, Research Grant to J.M. and M.S.); M.L. was supported by the FWF (Austrian Science Fund, P 29705) and by the European Union’s Horizon 2020 research and innovation programme under the Marie Sklodowska-Curie grant agreement no. 798091. Acknowledgements. We thank Annet Louwerse and Jan Langermans for allowing us to conduct the study at the BPRC, Caroline Olesen, Lisette van den Berg, Saskia Visser-van Soest and Willem van der Spek for supporting us in the work with the macaques, Daniella Mortier, Linda Hofman, Elisabeth Pschernig and Ruth Sonnweber for their help/advice concerning the hormone analyses, and Tjeerd Fluitsma for building the test apparatuses. Finally, we would like to thank Loeske Kruuk, Sarah Brosnan and the anonymous reviewers for their constructive comments on earlier versions of this manuscript.

Keywords

Cooperation
Glucocorticoid hormone
Loose-string paradigm
Macaca fascicularis
Salivary cortisol
Social bonds

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title = "Cooperation with closely bonded individuals reduces cortisol levels in long-tailed macaques",

abstract = "Many animal species cooperate with conspecifics in various social contexts. While ultimate causes of cooperation are being studied extensively, its proximate causes, particularly endocrine mechanisms, have received comparatively little attention. Here, we present a study investigating the link between the hormone cortisol, cooperation and social bonds in long-tailed macaques (Macaca fascicularis). We tested 14 macaques in a dyadic cooperation task (loose-string paradigm), each with two partners of different social bond strength and measured their salivary cortisol before and after the task. We found no strong link between the macaques{\textquoteright} cortisol level before the task and subsequent cooperative success. By contrast, we did find that the act of cooperating in itself led to a subsequent decrease in cortisol levels, but only when cooperating with closely bonded individuals. Two control conditions showed that this effect was not due to the mere presence of such an individual or the pulling task itself. Consequently, our study shows an intricate way in which the hypothalamic–pituitary–adrenal axis is involved in cooperation. Future studies should reveal whether and how our findings are driven by the anxiolytic effect of oxytocin, which has been associated with social bonding.",

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AB - Many animal species cooperate with conspecifics in various social contexts. While ultimate causes of cooperation are being studied extensively, its proximate causes, particularly endocrine mechanisms, have received comparatively little attention. Here, we present a study investigating the link between the hormone cortisol, cooperation and social bonds in long-tailed macaques (Macaca fascicularis). We tested 14 macaques in a dyadic cooperation task (loose-string paradigm), each with two partners of different social bond strength and measured their salivary cortisol before and after the task. We found no strong link between the macaques’ cortisol level before the task and subsequent cooperative success. By contrast, we did find that the act of cooperating in itself led to a subsequent decrease in cortisol levels, but only when cooperating with closely bonded individuals. Two control conditions showed that this effect was not due to the mere presence of such an individual or the pulling task itself. Consequently, our study shows an intricate way in which the hypothalamic–pituitary–adrenal axis is involved in cooperation. Future studies should reveal whether and how our findings are driven by the anxiolytic effect of oxytocin, which has been associated with social bonding.

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Cooperation with closely bonded individuals reduces cortisol levels in long-tailed macaques

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