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A Noninvasive Method for Estimating Nitrogen Balance in Free-Ranging Primates

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Abstract

The vital role of body protein as an energy reserve has received little focus in studies of wild primates. Owing to the relatively low protein content of fruit, some frugivorous primates could face a protein deficit if body protein is catabolized for energy during periods of low fruit availability. Such an imbalance can be detected if fatty acids, amino acids, and nitrogen (N) catabolites are reincorporated or recycled back to tissues. Here we describe a method to quantify protein recycling by measuring standardized urea concentration and N isotope signatures from urine samples collected from wild Bornean orangutans (Pongo pygmaeus wurmbii). Our overall goal was to explore if concentrations of urea and δ15N values could be used as indicators of the amount of protein consumed and the degree of protein recycling, respectively, in wild, free-ranging primates. We examine the relationships between urea concentration, δ15N values, protein intake, and fruit availability. Urea concentration increased with fruit availability, reflecting a slight increase in protein consumption when fruit was abundant. However, we found no relationship between δ15N values and fruit availability, suggesting that orangutans avert a negative protein balance during periods of low fruit availability. These noninvasive methods complement recent advances in primate energy balance research and will contribute to our understanding of adaptations of primates during periods of fruit shortage.

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Acknowledgments

We thank the Directorate of Nature Conservation (PHKA), the Gunung Palung National Park office (BTNGP), the Indonesian Institute of Sciences (LIPI), the Center for Research and Development in Biology (PPPB), and the State Ministry of Research and Technology (RISTEK) for their sponsorship and for granting permission to conduct research in Gunung Palung National Park. We thank Dr. Raphael Kudela and Dr. Paul Koch for fruitful discussions in the early stages of this research project and for providing us with access to their laboratories and supplies for our analyses. We thank the University of Santa Cruz Stable Isotope Laboratory and Dyke Andreasen for the use of the facility. We are grateful to Brett Walker, Dr. Sora Kim, and Dr. Nancy Conklin-Brittain for their advice on sample preparation for our analyses and the interpretation of our results. We also thank all of the dedicate field assistants, research assistants, field managers, and students who assisted with data and sample collection. This research was supported by L. S. B. Leakey Foundation grants (E. R. Vogel, N. J. Dominy, and C. D. Knott), The George Washington University Selective Excellence Fund (to the Center for the Advanced Study of Hominid Paleobiology for E. R. Vogel and to the Department of Statistics and the Biostatistics Center for M. D. Larsen), David and Lucile Packard Foundation Fellowship in Science and Engineering (no. 2007–31754, N. J. Dominy), National Geographic Society (C. D. Knott), The National Science Foundation no. BCS-0643122 (E. R. Vogel, N. J. Dominy, and C. D. Knott), U.S. Fish and Wildlife Service (C. D. Knott), the Wenner-Gren Foundation (C. D. Knott), Harvard University (C. D. Knott), and The Mellon Foundation (C. D. Knott). This research was approved by UCSC CARC IACUC (no. 20061056–122204).

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Authors and Affiliations

  1. Department of Anthropology and the Center for Human Evolutionary Studies, Rutgers University, New Brunswick, NJ, 08901, USA

    Erin R. Vogel

  2. The Center for the Advanced Study of Hominid Paleobiology, Department of Anthropology, The George Washington University, Washington, DC, 20052, USA

    Erin R. Vogel

  3. Departments of Geology and Anthropology, University of Cincinnati, Cincinnati, OH, 45221, USA

    Brooke E. Crowley

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

    Cheryl D. Knott

  5. Department of Ocean Sciences, University of California Santa Cruz, Santa Cruz, CA, 95064, USA

    Melissa D. Blakely

  6. Department of Statistics, The George Washington University, Washington, DC, 20052, USA

    Michael D. Larsen

  7. Department of Anthropology, Dartmouth College, Hanover, NH, 03755, USA

    Nathaniel J. Dominy

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Vogel, E.R., Crowley, B.E., Knott, C.D. et al. A Noninvasive Method for Estimating Nitrogen Balance in Free-Ranging Primates. Int J Primatol 33, 567–587 (2012). https://doi.org/10.1007/s10764-011-9543-6

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  • DOI: https://doi.org/10.1007/s10764-011-9543-6

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