Assessing Stress in Zoo-Housed Western Lowland Gorillas (Gorilla gorilla gorilla) Using Allostatic Load

Edes, Ashley N.; Wolfe, Barbara A.; Crews, Douglas E.

doi:10.1007/s10764-016-9899-8

Cited by 19 publications

(31 citation statements)

References 76 publications

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“…(Goymann & Wingfield, 2004 g., cortisol, interleukin-6, and epinephrine) in a study on aging among free-ranging rhesus macaques and incorporated allostasis theory to discuss their results. To date, however, only one study group has constructed a multibiomarker ALI and used it to test for associations with other study variables (e.g., sex, age, and mortality risk) in the manner reported for human samples (Edes, Wolfe, & Crews, 2016a, 2016b.…”

Section: Allostatic Load During Growth a N D De V E L O P Me N Tmentioning

confidence: 99%

“…As an illustration of applying an ALI to a nonhuman primate species, recently allostatic load was examined in a captive group of western lowland gorillas (Gorilla gorilla gorilla; Edes et al, 2016a). This ALI included seven biomarkers (albumin, cortisol, CRH, DHEA-S, glucose, IL-6, and TNF-a) and was constructed using the quartile associated with highest morbidity and mortality risk, similar to reported research on humans.…”

Section: Allostatic Load During Growth a N D De V E L O P Me N Tmentioning

confidence: 99%

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Allostatic load and biological anthropology

Edes

Crews

2017

American J Phys Anthropol

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Multiple stressors affect developing and adult organisms, thereby partly structuring their phenotypes. Determining how stressors influence health, well-being, and longevity in human and nonhuman primate populations are major foci within biological anthropology. Although much effort has been devoted to examining responses to multiple environmental and sociocultural stressors, no holistic metric to measure stress-related physiological dysfunction has been widely applied within biological anthropology. Researchers from disciplines outside anthropology are using allostatic load indices (ALIs) to estimate such dysregulation and examine life-long outcomes of stressor exposures, including morbidity and mortality. Following allostasis theory, allostatic load represents accumulated physiological and somatic damage secondary to stressors and senescent processes experienced over the lifespan. ALIs estimate this wear-and-tear using a composite of biomarkers representing neuroendocrine, cardiovascular, metabolic, and immune systems. Across samples, ALIs are associated significantly with multiple individual characteristics (e.g., age, sex, education, DNA variation) of interest within biological anthropology. They also predict future outcomes, including aspects of life history variation (e.g., survival, lifespan), mental and physical health, morbidity and mortality, and likely health disparities between groups, by stressor exposures, ethnicity, occupations, and degree of departure from local indigenous life ways and integration into external and commodified ones. ALIs also may be applied to similar stress-related research areas among nonhuman primates. Given the reports from multiple research endeavors, here we propose ALIs may be useful for assessing stressors, stress responses, and stress-related dysfunction, current and long-term cognitive function, health and well-being, and risk of early mortality across many research programs within biological anthropology. K E Y W O R D Saging, allostasis, frailty, growth and development, nonhuman primates, senescence, stress | I N T R O D U C T I O NTraditional research foci within biological anthropology include variations in stress, morbidity, and mortality (for reviews, see Ice & James, 2007;Little, 2010). Despite this long-term focus, the field continues to pursue a reliable, relatively easy to apply metric for assessing lifetime stress and stress-related outcomes. We suggest incorporating the theory of allostasis and methods for assessing allostatic load within anthropological theory and methodology to aid in closing this gap. As a theory, allostasis was developed to explain how mammalian physiological responses to stressors in their environments evolved to maximize the probability of survival while limiting somatic damage (Korte, Koolhaas, Wingfield, & McEwen, 2005;McEwen & Stellar, 1993;McEwen & Wingfield, 2003;Sterling, 2004Sterling, , 2012Sterling & Eyer, 1988). Unfortunately, such beneficial defensive responses come at a cost and, over time, repeated allostatic activi...

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Section: Allostatic Load During Growth a N D De V E L O P Me N Tmentioning

confidence: 99%

Section: Allostatic Load During Growth a N D De V E L O P Me N Tmentioning

confidence: 99%

Allostatic load and biological anthropology

Edes

Crews

2017

American J Phys Anthropol

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“…Previously, we established that AL is positively associated with age and significantly different between males and females in this sample [Edes et al, in press]. To determine if there were differences in AL by rearing history (mother‐reared, nursery‐reared, wild‐caught), we used two ANCOVAs.…”

Section: Methodsmentioning

confidence: 99%

“…Although some nonhuman primate stress studies have incorporated an allostatic framework [Goymann and Wingfield, ; Maestripieri and Hoffman, ], only one has estimated AL using biomarkers to test associations with life history and health outcomes [Edes et al, in press]. Previously, we applied AL to a group of western lowland gorillas ( Gorilla gorilla gorilla ) in human care ( n = 27).…”

Section: Introductionmentioning

confidence: 99%

Rearing history and allostatic load in adult western lowland gorillas (Gorilla gorilla gorilla) in human care

2016

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Disrupted rearing history is a psychological and physical stressor for nonhuman primates, potentially resulting in multiple behavioral and physiological changes. As a chronic, soma-wide stressor, altered rearing may be best assessed using a holistic tool such as allostatic load (AL). In humans, AL estimates outcomes of lifetime stress-induced damage. We predicted mother-reared gorillas would have lower AL than nursery-reared and wild-caught conspecifics. We estimated AL for 27 gorillas housed at the Columbus Zoo and Aquarium between 1956 and 2014. AL estimates were calculated using biomarkers obtained during previous anesthetic events. Biomarkers in the high-risk quartile were counted toward a gorilla's AL. Rearing history was categorized as mother-reared, nursery-reared, and wild-caught. Using ANCOVA, rearing history and AL are significantly associated when age and sex are entered as covariates. Wild-caught gorillas have significantly higher AL than mother-reared gorillas. Neither wild-caught nor mother-reared gorillas are significantly different from nursery-reared gorillas. When examined by sex, males of all rearing histories have significantly lower AL than females. We suggest males face few stressors in human care and ill effects of rearing history do not follow. Wild-caught females have significantly higher AL than mother-reared females, but neither is significantly different from nursery-reared females. Combined with our previous work on AL in this group, wherein females had twofold higher AL than males, we suggest females in human care face more stressors than males. Disrupted rearing history may exacerbate effects of these stressors. Providing opportunities for females to choose their distance from males may help reduce their AL.

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“…Herein, we explore whether updating our original ALIs to include cholesterol and triglycerides better predicts risk of all-cause morbidity, cardiac disease, and mortality in gorillas. We hope this report will build on the foundation of our previous research [65][66][67][68] to help guide those interested in pioneering allostatic load methodology across taxa. As the ability to measure physiological markers from noninvasive tissue samples like urine and feces increases, this research also may extend to studying and monitoring populations in the wild.…”

Section: Allostatic Load Indices With Cholesterol and Triglycerides Pmentioning

confidence: 99%

Allostatic Load Indices With Cholesterol and Triglycerides Predict Disease and Mortality Risk in Zoo-Housed Western Lowland Gorillas (Gorilla gorilla gorilla)

et al. 2020

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Allostatic load, or the physiological dysregulation accumulated due to senescence and stress, is an established predictor of human morbidity and mortality and has been proposed as a tool for monitoring health and welfare in captive wildlife. It is estimated by combining biomarkers from multiple somatic systems into allostatic load indices (ALIs), providing a score representing overall physiological dysregulation. Such ALIs have been shown to predict disease and mortality risk in western lowland gorillas. In these prior analyses, we were unable to include lipid markers, a potential limitation as they are key biomarkers in human models. Recently, we were able to assay serum cholesterol and triglycerides and add them to our previous ALI. We then re-examined associations with health outcomes using binomial generalized linear models. We constructed ALIs using 2 pooling strategies and 2 methods. By itself, a 1-unit increase in allostatic load was associated with higher odds of all-cause morbidity and mortality, but results were mixed for cardiac disease. However, the best fit models for all-cause morbidity and cardiac disease included only age and sex. Allostatic load was retained alongside age in the best fit models for mortality, with a 1-unit increase associated with 23% to 45% higher odds of death. Compared with previous results, ALIs containing cholesterol and triglycerides better predict disease risk in zoo-housed western lowland gorillas, as evidenced by larger effect sizes for some models and better goodness of fit for all ALIs. Based on these results, we address methodology for future allostatic load research on wildlife.

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Assessing Stress in Zoo-Housed Western Lowland Gorillas (Gorilla gorilla gorilla) Using Allostatic Load

Cited by 19 publications

References 76 publications

Allostatic load and biological anthropology

Allostatic load and biological anthropology

Rearing history and allostatic load in adult western lowland gorillas (Gorilla gorilla gorilla) in human care

Allostatic Load Indices With Cholesterol and Triglycerides Predict Disease and Mortality Risk in Zoo-Housed Western Lowland Gorillas (Gorilla gorilla gorilla)

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