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Dominance rank and the presence of sexually receptive females predict feces-measured body temperature in male chimpanzees

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Abstract

Quantifying the costs of mating is key for understanding life-history trade-offs. As a reflection of metabolic rate, body temperature is one metric for assaying these costs. However, conventional methods for measuring body temperature are invasive and unsuitable for the study of free-living populations of endangered species, including great apes. A promising proxy for body temperature is fecal temperature, the internal temperature of fecal deposits shortly following defecation. We validated this method with humans, finding that maximum fecal temperature is a reliable proxy for rectal temperature. We then applied this method to wild chimpanzees (Pan troglodytes schweinfurthii) at Ngogo, Kibale National Park, Uganda. We collected and analyzed 101 fecal temperature measurements from 43 adult chimpanzees (male: N = 28; female: N = 15). Chimpanzee fecal temperature ranged from 33.4 to 38.9 °C, with a mean of 35.8 °C. Although fecal temperature was not predicted by sex, age, or ambient temperature, male fecal temperature was 1.1 °C higher on days when sexually receptive females were present and was positively correlated with male dominance rank. Post hoc analyses showed that overall copulation rates, but not aggression rates, were positively correlated with fecal temperature, suggesting that sexual physiology and behavior best explain mating-related temperature variation. Together, these results indicate fecal temperature is a reliable proxy for core body temperature in large-bodied mammals, captures metabolic costs associated with male mating behavior, and represents a valuable noninvasive tool for biological field research.

Significance statement

Body temperature illuminates an animal’s physiological condition and energy expenditure, but it is difficult to measure in wild animals. Consequently, basic data on body temperature and its socioecological correlates in wild animals are scant, especially when noninvasive measures must be used. To address this problem, we demonstrated that the temperatures of fecal deposits reliably estimate body temperatures in a large bodied primate and are approximately as reliable as invasive, subcutaneous transponder methods used in other mammals. We then found that fecal temperature in chimpanzees varied by ecologically and reproductively relevant variables including time of year, the presence of sexually receptive females, and dominance rank. Sexual behavior was likely responsible for increased male fecal temperature, as overall copulation frequency, but not aggression, was correlated with fecal temperature. We therefore provide evidence that fecal temperature can be used to assay body temperature and address questions regarding physiological condition and metabolic expenditure.

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Acknowledgments

We thank the Uganda Wildlife Authority, Uganda National Council for Science and Technology, and Makerere University Biological Field Station for permission to work in Kibale National Park. Thanks to David Watts and John Mitani for establishing and maintaining long-term chimpanzee research at Ngogo. We are indebted to Chris Aliganyira, Natasha Bartolotta, Charles Birungi, Rebecca Davenport, Brian Kamugyisha, Godfrey Mbabazi, Lawrence Ndangizi, Alfred Tumusiime, Ambrose Twineomujuni, and David Watts for help with data collection. For logistical and/or analytical support, we thank Sam Angedakin, Charles Businge, Cheryl Knott, Roger Mundry, Rachna Reddy, and Carol Rowney. We also thank two anonymous reviewers and David Watts for constructive comments on the manuscript.

Funding

JDN was supported by the National Science Foundation (Award no. 1613393), National Geographic Society (Award no. 9824-15), Nacey Maggioncalda Foundation, and Boston University. AAS was supported by the National Science Foundation (Award no. 1540259), University of Michigan, and Arizona State University. KEL was supported by the National Institutes of Health Award 5R01AG049395 through the National Institute on Aging.

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Authors and Affiliations

  1. Department of Anthropology, Boston University, Boston, MA, 02215, USA

    Jacob D. Negrey

  2. Department of Pathobiological Sciences, University of Wisconsin-Madison, Madison, WI, 53706, USA

    Jacob D. Negrey

  3. Department of Anthropology, University of Texas at Austin, Austin, TX, 78705, USA

    Aaron A. Sandel

  4. School of Human Evolution and Social Change and Institute of Human Origins, Arizona State University, 900 S. Cady Mall, Tempe, AZ, 85281, USA

    Kevin E. Langergraber

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  1. Jacob D. Negrey
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Correspondence to Jacob D. Negrey.

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The authors declare that they have no conflict of interest.

Ethical approval

All applicable international, national, and institutional guidelines for the use of animals were followed. Noninvasive data collection from chimpanzees received a review exemption from Boston University’s Institutional Animal Care and Use Committee. Similarly, this study did not require approval from Boston University’s Institutional Review Board.

Informed consent

Although this study was not considered human subjects research by Boston University’s Institutional Review Board, human participants provided written consent.

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Communicated by D. P. Watts

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Negrey, J.D., Sandel, A.A. & Langergraber, K.E. Dominance rank and the presence of sexually receptive females predict feces-measured body temperature in male chimpanzees. Behav Ecol Sociobiol 74, 5 (2020). https://doi.org/10.1007/s00265-019-2788-3

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