Advertisement

Nutrient Balancing by Captive Golden Snub-Nosed Monkeys (Rhinopithecus roxellana)

  • Stephanie T. Chen
  • Xi Luo
  • Rong Hou
  • David Raubenheimer
  • Weihong Ji
  • Xuelin Jin
  • Zhi Jiang
  • Xuewei Yu
  • Jiajia Wang
  • Min Li
  • Songtao Guo
  • Baoguo Li
Article

Abstract

An organism’s fitness is tied closely to its ability to obtain food. However, many foods are nutritionally suboptimal on their own, forcing an individual to develop a feeding strategy that actively manages both type and amount of food consumed. Animals in captivity are additionally limited to human provisioned diets, which may be nutritionally inadequate and negatively affect behavior and health. We studied the nutritional intake of captive golden snub-nosed monkeys (Rhinopithecus roxellana) at two locations in China (132 days of continuous, sunrise to sunset focal samples of 7 individuals at each site) and used the Geometric Framework for nutrition to identify their feeding strategy and evaluate diet variation across sites, seasons, and age–sex classes. Captive golden snub-nosed monkeys had a mean nutrient intake of 75% carbohydrates (15% neutral detergent fiber, 60% total nonstructural carbohydrates), 12% fat, and 13% protein (by energy) that differed by location and season owing to differences in the type and amount of food items offered and consumed. Intake at one location differed from that of wild golden snub-nosed monkeys, suggesting that the captive diet was inadequate. These results highlight the importance of developing nutritionally adequate diets for captive animals based on an understanding of their nutritional requirements.

Keywords

Captivity Geometric framework Nutrition 

Notes

Acknowledgements

The authors would like to thank the Shaanxi Provincial Wildlife Rescue Center, Hangzhou Zoo, and their staff for permission to conduct this study and helpful insights on diet planning. Special thanks to Drs. Bobbi Low and Jacinta Beehner (University of Michigan) for advice on methodology and comments on an early draft. This study was supported by the National Nature Science Foundation of China (31672301, 31872247,31270441, 31730104); National Key Programme of Research and Development, Ministry of Science and Technology (2016YFC0503200); Natural Science Basic Research Plan in Shaanxi Province of China (2016JZ009, 2018JC-022); Fok Ying Tung Education Foundation (131105); and The Innovation and Entrepreneurship Training Program of Northwest University. S. T. Chen was supported by an International Institute Individual Fellowship (University of Michigan) and a Fulbright Student Scholarship while collecting data. We thank the editor and several anonymous reviewers for helpful comments on current and previous drafts.

Supplementary material

10764_2018_70_MOESM1_ESM.docx (63 kb)
ESM 1 (DOCX 62 kb)

References

  1. Amato, K. R., & Garber, P. A. (2014). Nutrition and foraging strategies of the black howler monkey (Alouatta pigra) in Palenque National Park, Mexico. American Journal of Primatology, 76, 774–787.CrossRefGoogle Scholar
  2. Ando, M., Yokota, H. O., & Shibata, E. (2003). Barking stripping preference of sika deer, Cervus nippon, in terms of bark chemical contents. Forest Ecology and Management, 177, 323–331.CrossRefGoogle Scholar
  3. Bauchop, T., & Martucci, R. W. (1968). Ruminant-like digestion of the langur monkey. Science, 161, 698–700.CrossRefGoogle Scholar
  4. Bissel, H. (2014). Nutritional implications of the high-elevation kifestyle of Rhinopithecus bieti. In N. Grow, S. Gursky-Doyen, & A. Krzton (Eds.), High altitude primates. New York: Springer Science+Business Media.Google Scholar
  5. Bleisch, W., & Xie, J. H. (1998). Ecology and behavior of the Guizhou snub-nosed langur (Rhinopithecus brelichi). In N. C. Jablonski (Ed.), The natural history of the doucs and snub-nosed monkeys (pp. 155–190). Singapore: World Scientific Publishing.Google Scholar
  6. Conklin-Brittain, N. L., Knott, C. D., & Wrangham, R. W. (2006). Energy intake by wild chimpanzees and orangutans: Methodological considerations and a preliminary comparison. In G. Hohmann, M. M. Robbins, & C. Boesch (Eds.), Feeding ecology in apes and other primates: Ecological, physical and behavioral aspects (pp. 445–471). Cambridge: Cambridge University Press.Google Scholar
  7. Cook, J. G., Johnson, B. K., Cook, R. C., Riggs, R. A., Delcurto, T., et al (2004). Effects of summer-autumn nutrition and parturition date on reproduction and survival of elk. Wildlife Monographs, 155, 1–61.Google Scholar
  8. Ding, W., & Zhao, Q. K. (2004). Rhinopithecus bieti at Tachen, Yunnan: diet and daytime activities. International Journal of Primatology, 25, 583–598.CrossRefGoogle Scholar
  9. Doran-Sheehy, D., Mongo, P., Lodwick, J., & Conklin-Brittain, N. L. (2009). Male and female western gorilla diet: preferred foods, use of fallback resources, and implications for ape versus Old World monkey foraging strategies. American Journal of Physical Anthropology, 140, 727–738.CrossRefGoogle Scholar
  10. Dröscher, I., Rothman, J. M., Ganzhorn, J. U., & Kappeler, P. M. (2016). Nutritional consequences of folivory in a small-bodied lemur (Lepilemur leucopus): effects of season and reproduction on nutrient balancing. American Journal of Physical Anthropology, 160, 197–207.CrossRefGoogle Scholar
  11. Edwards, M. S., & Ulrey, D. E. (1999). Effect of dietary fiber concentration on apparent digestibility and digesta passage in non-human primates. II. Hindgut- and foregut-fermenting folivores. Zoo Biology, 18, 537–549.CrossRefGoogle Scholar
  12. Felton, A. M., Felton, A., Lindenmayer, D. B., & Foley, W. J. (2009a). Nutritional goals of wild primates. Functional Ecology, 23, 70–78.CrossRefGoogle Scholar
  13. Felton, A. M., Felton, A., Wood, J. T., Foley, W. J., Raubenheimer, D. et al. (2009b). Nutritional ecology of Ateles chamek in lowland Bolivia: How macronutrient balancing influences food choices. International Journal of Primatology, 30, 675–696.CrossRefGoogle Scholar
  14. Guo, S., Li, B., & Watanabe, K. (2007). Diet and activity budget of Rhinopithecus roxellana in the Qinling Mountains, China. Primates, 48, 268–276.CrossRefGoogle Scholar
  15. Guo, S., Hou, R., Garber, P., Raubenheimer, D., Righini, N., et al. (2018). Nutrient-specific compensation for seasonal cold stress in a free-ranging temperate colobine monkey. Functional Ecology, 1–11.  https://doi.org/10.1111/1365-2435.13134.CrossRefGoogle Scholar
  16. Hou, R., He, S., Wu, F., Chapman, C., Pan, R., et al (2018). Seasonal variation in diet and nutrition of the northern-most population of Rhinopithecus roxellana. American Journal of Primatology, 80, e22755.CrossRefGoogle Scholar
  17. Huang, S. (2014). Noninvasive study of nutrient metabolism, stress and immune status in sichuan golden monkey (Rhinopithecus roxellana) in the environment of captivity. Doctoral dissertation, Nanjing Agricultural University. Google Scholar
  18. Irwin, M. T., Raharison, J. L., Raubenheimer, D. R., Chapman, C. A., & Rothman, J. M. (2014). Nutritional correlates of the “lean season”: effects of seasonality and frugivory on the nutritional ecology of diademed sifakas. American Journal of Physical Anthropology, 153, 78–91.CrossRefGoogle Scholar
  19. Irwin, M. T., Raharison, J. L., Raubenheimer, D. R., Chapman, C. A., & Rothman, J. M. (2015). The nutritional geometry of resource scarcity: effects of lean seasons and habitat disturbance on nutrient intakes and balancing in wild sifakas. PLoS One, 10(6), e0128046.CrossRefGoogle Scholar
  20. Johnson, C. A., Raubenheimer, D., Rothman, J. M., Clarke, D., & Swedell, L. (2013). 30 days in the life: daily nutrient balancing in a wild chacma baboon. PLoS One, 8, e70383.CrossRefGoogle Scholar
  21. Kirkpatrick, R. C. (1998). Ecology and behavior in snub-nosed and douc langurs. In N. C. Jablonski (Ed.), The natural history of the doucs and snub-nosed monkeys (pp. 155–190). Singapore: World Scientific Publishing.CrossRefGoogle Scholar
  22. Kuhar, C. W., Fuller, G. A., & Dennis, P. M. (2013). A survey of diabetes prevalence in zoo-housed primates. Zoo Biology, 32, 63–69.CrossRefGoogle Scholar
  23. Less, E. H., Bergl, R., Ball, R., Dennis, P. M., Kuhar, C. W., et al (2014a). Implementing a low-starch biscuit-free diet in zoo gorillas: the impact on behavior. Zoo Biology, 33, 63–73.CrossRefGoogle Scholar
  24. Less, E. H., Lukas, K. E., Bergl, R., Ball, R., Kuhar, C. W., et al (2014b). Implementing a low-starch biscuit-free diet in zoo gorillas: the impact on health. Zoo Biology, 33, 74–80.CrossRefGoogle Scholar
  25. Li, Y. (2006). Seasonal variation of diet and food availability in a group of Sichuan snub-nosed monkeys in Shennongjia nature reserve, China. American Journal of Primatology, 68, 217–233.CrossRefGoogle Scholar
  26. Li, Y., Jiang, Z., Li, C., & Grueter, C. C. (2010). Effects of seasonal folivory and frugivory on ranging patterns in Rhinopithecus roxellana. International Journal of Primatology, 31, 609–626.CrossRefGoogle Scholar
  27. Mason, G. J., Burn, C. C., Dallaire, J. A., Kroshko, J., Kinkaid, H. M., & Jeschke, J. M. (2013). Plastic animals in cages: behavioural flexibility and responses to captivity. Animal Behaviour, 85, 1113–1126.CrossRefGoogle Scholar
  28. Maynard, A. B., & Loosli, J. K. (1969). Animal nutrition. New York: McGraw-Hill.Google Scholar
  29. Mogan, K. N., & Tromborg, C. T. (2007). Sources of stress in captivity. Applied Animal Behaviour Science, 102, 262–302.CrossRefGoogle Scholar
  30. Nakagawa, N. (2009). Feeding rate as valuable information in primate feeding ecology. Primates, 50, 131–141.  https://doi.org/10.1007/s10329-009-0129-2.CrossRefPubMedGoogle Scholar
  31. National Bureau of Statistics of China (2013). China yearbook of statistics 2013. Beijing: China National Statistics Press Online. http://www.stats.gov.cn/english/.
  32. Nijboer, J., & Direnfeld, E. S. (1996). Comparison of diets fed to southeast Asian colobines in north American and European zoos, with emphasis on temperate browse composition. Zoo Biology, 15, 499–507.CrossRefGoogle Scholar
  33. Pond, W. G., Church, D. C., Pond, K. R., & Schoknecht, P. A. (2005). Basic animal nutrition and feeding. Hoboken: John Wiley & Sons.Google Scholar
  34. Raubenheimer, D. (2011). Toward a quantitative nutritional ecology: the right-angled mixture triangle. Ecological Monographs, 81, 407–427.CrossRefGoogle Scholar
  35. Raubenheimer, D., & Simpson, S. J. (2004). Organismal stoichiometry: quantifying non-independence among food components. Ecology, 85, 1203–1216.CrossRefGoogle Scholar
  36. Raubenheimer, D., Simpson, S. J., & Mayntz, D. (2009). Nutrition, ecology and nutritional ecology: toward an integrated framework. Functional Ecology, 23, 4–16.CrossRefGoogle Scholar
  37. Remis, M. J. (2002). Food preferences among captive western gorillas (Gorilla gorilla gorilla) and chimpanzees (Pan troglodytes). International Journal of Primatology, 23, 231–249.CrossRefGoogle Scholar
  38. Ren, B. P., Li, B. G., Li, M., & Wei, F. W. (2010). Inter-population variation of diets of golden snub-nosed monkeys (Rhinopithecus roxellana) in China. Acta Theriologica Sinica, 30, 357–364.Google Scholar
  39. Reynolds, V., Lloyd, A. W., Babweteera, F., & English, C. J. (2009). Decaying Raphia farinifera palm trees provide a source of sodium for wild chimpanzees in the Budongo Forest, Uganda. PLoS ONE, 4(7), e6194.CrossRefGoogle Scholar
  40. Robbins, C. T. (2012). Wildlife feeding and nutrition. New York: Academic Press.Google Scholar
  41. Rothman, J. M., Dierenfeld, E. S., Hintz, H. F., & Pell, A. N. (2008). Nutritional quality of gorilla diets: Consequences of age, sex, and season. Oecologia, 155, 111–122.CrossRefGoogle Scholar
  42. Rothman, J. M., Raubenheimer, D., & Chapman, C. A. (2011). Nutritional geometry: Gorillas prioritize non-protein energy while consuming surplus protein. Biology Letters, 7, 847–849.CrossRefGoogle Scholar
  43. Rothman, J. M., Chapman, C. A., & Van Soest, P. J. (2012). Methods in primate nutritional ecology: A user’s guide. International Journal of Primatology, 33, 542–566.CrossRefGoogle Scholar
  44. Simpson, S. J., & Raubenheimer, D. (2012). The nature of nutrition: A unifying framework from animal adaptation to human obesity. Princeton: Princeton University Press.CrossRefGoogle Scholar
  45. Simpson, S. J., Batley, R., & Raubenheimer, D. (2003). Geometric analysis of macronutrient intake in humans: the power of protein? Appetite, 41, 123–140.CrossRefGoogle Scholar
  46. Smith, B. K., Remis, M. J., & Dierenfeld, E. S. (2014). Nutrition of the captive western lowland gorilla (Gorilla gorilla gorilla): a dietary survey. Zoo Biology, 33, 1–7.CrossRefGoogle Scholar
  47. Stephens, S. A., Salas, L. A., & Direnfeld, E. S. (2006). Bark consumption by the painted ringtail (Pseudochirulus forbesi larvatus) in Papau New Guinea. Biotropica, 38, 617–624.CrossRefGoogle Scholar
  48. Wang, Z. Y., Ding, Y. H., He, J. H., & Yu, J. (2004). An updating analysis of the climate change in China in recent 50 years. Acta Meterologica Sinica, 62, 900–904.Google Scholar
  49. Waterman, P. G., Ross, J. A. M., Bennett, E. L., & Davies, A. G. (1988). A comparison of the floristics and leaf chemistry of the tree flora in 2 Malaysian rain forests and the influence of leaf chemistry on populations of colobine monkeys in the old-world. Biological Journal of the Linnean Society, 34, 1–32.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • Stephanie T. Chen
    • 1
    • 2
    • 3
  • Xi Luo
    • 1
    • 2
  • Rong Hou
    • 1
    • 2
  • David Raubenheimer
    • 4
  • Weihong Ji
    • 5
  • Xuelin Jin
    • 6
  • Zhi Jiang
    • 7
  • Xuewei Yu
    • 7
  • Jiajia Wang
    • 1
    • 2
  • Min Li
    • 1
    • 2
  • Songtao Guo
    • 1
    • 2
  • Baoguo Li
    • 1
    • 2
  1. 1.Shaanxi Key Laboratory for Animal Conservation, and College of Life SciencesNorthwest UniversityXi’anChina
  2. 2.Center for Excellence in Animal Evolution and GeneticsChinese Academy of SciencesKunmingChina
  3. 3.Department of StatisticsNorth Carolina State UniversityRaleighUSA
  4. 4.The Charles Perkins CentreUniversity of SydneySydneyAustralia
  5. 5.Human and Wildlife Interactions Research Group, Institute of Natural Mathematical SciencesMassey UniversityAlbanyNew Zealand
  6. 6.Shaanxi Zoology InstituteXi’anChina
  7. 7.Hangzhou ZooHangzhouChina

Personalised recommendations