Assessing Stress in Zoo-Housed Western Lowland Gorillas (Gorilla gorilla gorilla) Using Allostatic Load
- 781 Downloads
Stress contributes to the development of chronic degenerative diseases in primates. Allostatic load is an estimate of stress-induced physiological dysregulation based on an index of multiple biomarkers. It has been applied to humans to measure effects of stress and predict health outcomes. Assessing allostatic load in nonhuman primates may aid in understanding factors promoting compromised health and longevity in captive populations, as well as risk assessment among wild populations following human activities. We applied an allostatic load index to gorillas housed at the Columbus Zoo and Aquarium (N = 27, 1956–2014) using data from medical records and biomarkers from banked serum. We estimated allostatic load using seven biomarkers (albumin, cortisol, corticotropin-releasing hormone, dehydroepiandrosterone sulfate, glucose, interleukin-6, and tumor necrosis factor alpha) and then examined this index for associations with age, sex, number of stressful events, parturition, physiological health measures, and age at death. Stressful events were defined as agonistic interactions with wounding, translocations, and anesthetizations. Allostatic load positively associated with age and total number of lifetime stressful events. Allostatic load was significantly higher in females than in males. Allostatic load was not associated with number of pregnancies and was not different between nulliparous and parous females. Allostatic load associated positively with serum creatinine and triglyceride levels, showed a nonsignificant negative association with cholesterol, and did not associate significantly with age at death. These results demonstrate the potential utility of allostatic load for exploring long-term stress and health risks, as well as for evaluating environmental stressors for gorillas and other nonhuman primates in captivity and in the wild.
KeywordsAllostatic load Biomarkers Captivity Gorillas Stress
The authors thank Michelle Forman and Rebecca Makii for their assistance in recording information from keeper and medical records. This research would not have been possible without the assistance of veterinarians, keepers, and staff at the Columbus Zoo and Aquarium. We also thank two anonymous reviewers, the associate editor, and the editor-in-chief for their constructive feedback on earlier versions of this manuscript. Partial funding for this research was provided by The Ohio State University Department of Anthropology. The authors have no conflicts of interest.
- Cannon, W. B. (1932). The wisdom of the body. New York: W.W. Norton.Google Scholar
- Cavigelli, S. A., & Caruso, M. J. (2015). Sex, social status and physiological stress in primates: the importance of social and glucocorticoid dynamics. Philosophical Transactions B, 370(1669). doi: 10.1098/rstb.2014.0103.
- Crews, D. E., Harada, H., Aoyagi, K., Maeda, T., Alfarano, A., et al. (2012). Allostatic load among elderly Japanese living on Hizen-Oshima Island. International Journal of Physical Anthropology, 31, 18–29.Google Scholar
- Dill, D. B., Adolph, E. F., & Wilber, C. G. (1964). Adaptation to the environment. Washington, DC: American Physiological Society.Google Scholar
- Edes, A. N., Wolfe, B. A., & Crews, D. E. (2016). Rearing history and allostatic load in adult western lowland gorillas (Gorilla gorilla gorilla) in human care. Zoo Biology, 35(2), 167–173.Google Scholar
- Harder, J. D. (2012). Reproduction and hormones. In N. J. Silvy (Ed.), The wildlife techniques manual (Vol. 1, pp. 502–525). Baltimore: John Hopkins University Press.Google Scholar
- Leahy, R., & Crews, D. E. (2012). Physiological dysregulation and somatic decline among elders: modeling, applying and re-interpreting allostatic load. Collegium Anthropologicum, 36(1), 11–22.Google Scholar
- Leeds, A., Boyer, D., Ross, S. R., & Lukas, K. E. (2015). The effects of group type and young silverbacks on wounding rates in western lowland gorilla (Gorilla gorilla gorilla) groups in North American zoos. Zoo Biology, 34, 296–304.Google Scholar
- Linton, E. A., McLean, C., Nieuwenhuyzen Kruseman, A. C., Tilders, F. J., Van der Veen, E. A., & Lowry, P. J. (1987). Direct measurement of human plasma corticotropin-releasing hormone by “two-site” immunoradiometric assay. The Journal of Clinical Endocrinology & Metabolism, 64(5), 1047–1054.Google Scholar
- McEwen, B. S. (1998a). Protective and damaging effects of stress mediators. Seminars in Medicine of the Beth Israel Deaconess Medical Center, 338(3), 171–179.Google Scholar
- Nadler, R. D., Herndon, J. G., & Wallis, J. (1986). Adult sexual behavior: Hormones & reproduction. In G. Mitchell & J. M. Erwin (Eds.), Comparative primate biology: Behavior, conservation, and ecology (pp. 363–407). New York: Alan R. Liss.Google Scholar
- Nelson, R. J. (2011). An introduction to behavioral endocrinology (4th ed.). Sunderland: Sinauer Associates.Google Scholar
- Read, A.-L. (2006). A preliminary behavioural comparison of two captive western lowland gorilla (Gorilla gorilla gorilla) breeding groups. Paper presented at the 8th Annual Symposium on Zoo Research, Colchester Zoo.Google Scholar
- Robbins, M. M. (2007). Gorillas: Diversity in ecology and behavior. In C. J. Campbell, A. Fuentes, K. C. Mackinnon, M. Panger, & S. K. Bearder (Eds.), Primates in perspective (pp. 305–321). Oxford: Oxford University Press.Google Scholar
- Sterling, P., & Eyer, J. (1988). Allostasis: A new paradigm to explain arousal pathology. In S. Fisher & J. Reason (Eds.), Handbook of life stress, cognition and health (pp. 629–649). New York: John Wiley & Sons.Google Scholar
- Tworoger, S. S., & Hankinson, S. E. (2006). Collection, processing, and storage of biological samples in epidemiological studies: sex hormones, carotenoids, inflammatory markers, and proteomics as examples. CEBP Focus: Biorepository and Biospecimen Science, 15(9), 1578–1581.Google Scholar
- Watts, D. P. (2003). Gorilla social relationships: A comparative overview. In A. B. Taylor & M. L. Goldsmith (Eds.), Gorilla biology: A multidisciplinary perspective (pp. 302–327). Cambridge: Cambridge University Press.Google Scholar
- Zaragoza, F., Ibáñez, M., Mas, B., Laiglesia, S., & Anzola, B. (2011). Influence of environmental enrichment in captive chimpanzees (Pan troglodytes spp.) and gorillas (Gorilla gorilla gorilla): behavior and faecal cortisol levels. Revista Cientificia, XXI(5), 447–456.Google Scholar