Low-ranking individuals present high and unstable fecal cortisol levels in provisioned free-ranging adult male rhesus macaques (Macaca mulatta) during the birth season in a mountain area of northern China
Social hierarchy commonly exists in animal societies, affecting both the endocrine functioning and the behavior of animals. In nonhuman primates, the relationship between social rank and cortisol levels varies across species and even within species. Here, we assessed the relationships between social rank and fecal cortisol levels in adult male Taihangshan macaques (rhesus macaques, Macaca mulatta tcheliensis) from the provisioned, free-ranging Wulongkou-2 (WLK-2) group inhabiting Wulongkou Scenic Area, Jiyuan, China. From March to May 2014, we recorded 195 agonistic behaviors and collected 54 fresh fecal samples from eight adult male Taihangshan macaques. Males were assigned a social rank according to an agonistic behavior matrix, and enzyme-linked immunosorbent assay was then used to measure the cortisol concentration in the fecal samples. We found that social rank among the eight male Taihangshan macaques in WLK-2 group followed a strict linear hierarchy, and that fecal cortisol levels were significantly higher and more variable in low-ranking males than in more dominant individuals. Age was not significantly associated with social rank or fecal cortisol levels. Our results suggest that social rank and maintenance of the social hierarchy within the WLK-2 group is a chronic stressor, with low-ranking males maintaining heightened stress levels and enlarged reactive scope relative to dominant males. This provides new support for the theory that social environment can influence endocrine functioning.
KeywordsCortisol Rhesus macaques (Macaca mulatta tcheliensis) Social rank Stress
Thanks for the permission and support of Taihangshan Macaque National Nature Reserve throughout this study. Thanks to the National Natural Science Foundation of China (31472018, 31372193). We are grateful to Mr. Kuang Sanao, Mr. Kuang Zhenjing and Mr. Kang Yali for the help in the field. Moreover, thanks the reviewers and editors for the comments, which helped us to improve the manuscript.
Compliance with ethical standards
Conflict of interest
The authors declare that they have no conflicts of interest.
The methods for sampling behaviors and collecting fecal samples used in this study conformed to the guidelines of the China Practice for the Care and Use of Laboratory Animals, and followed protocols approved by the Ethics Committee of Zhengzhou University.
- Chai W (2014) Population ecology and social ecology of rhesus macaque disturbed by ecotourism. Dissertation, Zhengzhou University, Zhengzhou, ChinaGoogle Scholar
- Ejike C, Schreck CB (1980) Stress and social hierarchy rank in coho salmon. Trans Am Fish Soc 109:423–429. https://doi.org/10.1577/1548-8659(1980)109%3c423:SASHRI%3e2.0.CO;2 CrossRefGoogle Scholar
- Jiang X, Wang Y, Ma S (1991) Taxonomic revision and distribution of subspecies of rhesus monkey (Macaca mulatta) in China. Zool Res 12:241–247 (In Chinese) Google Scholar
- Li B, Li H, Zhao D, Zhang Y, Qi X (2006) Study on dominance hierarchy of the Sichuan snub-nosed monkey (Rhinopithecus roxellana) in Qinling Mountains. Acta Theriol Sin 26:18–25 (In Chinese) Google Scholar
- MacLarnon AM, Sommer V, Goffe AS, Higham JP, Lodge E, Tkaczynski P, Ross C (2015) Assessing adaptability and reactive scope: introducing a new measure and illustrating its use through a case study of environmental stress in forest-living baboons. Gen Comp Endocr 215:10–24. https://doi.org/10.1016/j.ygcen.2014.09.022 CrossRefPubMedGoogle Scholar
- Milich KM, Georgiev AV, Petersen RM, Emery Thompson M, Maestripieri D (2018) Alpha male status and availability of conceptive females are associated with high glucocorticoid concentrations in high-ranking male rhesus macaques (Macaca mulatta) during the mating season. Horm Behav 97:5–13. https://doi.org/10.1016/j.yhbeh.2017.09.014 CrossRefPubMedGoogle Scholar
- Rakhovskaya M (2011) Behavior and socioendocrinology of adult male rhesus macaques of Cayo Santiago. Dissertation, University of PennsylvaniaGoogle Scholar
- Song C, Qu W (1996) Scientific survey of Taihangshan Macaque Nature Reserve. China Forestry Publishing House press, BeijingGoogle Scholar
- Wang Y (2014) Comparative study on daily activity budget and social behavior of rhesus macaques under different raising conditions. Dissertation, Zhengzhou University, Zhengzhou, ChinaGoogle Scholar
- Wang B (2015) Social ecology of Taihangshan Macaques (Macaca mulatta tcheliensis): social rank-related issues. Dissertation, Zhengzhou University, Zhengzhou, ChinaGoogle Scholar