Research Article: Individual and environmental risk factors associated with fecal glucocorticoid metabolite concentrations in zoo-housed Asian and African elephants

Date Published: September 4, 2019

Publisher: Public Library of Science

Author(s): Janine L. Brown, Kathy Carlstead, Jessica D. Bray, David Dickey, Charlotte Farin, Kimberly Ange-van Heugten, Edna Hillmann.


A recent large-scale welfare study in North America involving 106 Asian (Elephas maximus) and 131 African (Loxodonta africana) elephants at 64 accredited facilities identified links (i.e., risk factors) between zoo environmental factors and a number of welfare outcomes (stereotypic behavior, ovarian acyclicity, hyperprolactinemia, walking and recumbence, body condition, health status, serum cortisol). For this population of elephants, we used the same epidemiological methods to examine associations between those risk factors and two additional welfare outcomes, mean concentration and individual variability (CV) of fecal glucocorticoid metabolite concentrations (FGM) as indicators of stress. Results indicate that African elephants are more responsive to social stressors than Asians, and that poor joint health is a stress-related welfare problem for Asian, but not African elephants in the North American population. For both species, higher FGM concentrations were associated with zoos located at more northern latitudes, whereas lower FGM concentrations were associated with having free access to indoor/outdoor spaces, and spending more time in managed interactions with staff. Also important for captive management, elephants having diverse enrichment options and belonging to compatible social groups exhibited reduced intra-individual variability in FGM concentrations. Our findings show that aspects of the zoo environment can be potential sources of stress for captive elephants, and that there are management activities that may facilitate coping with zoo conditions. Given species differences in factors that affected FGM, targeted, species-specific management approaches likely are needed to ensure good welfare for all elephants.

Partial Text

Modern zoos strive to ensure animals under human care experience a high standard of welfare that meets emotional and physical health needs [1]. Asian (Elephas maximus) and African (Loxodonta africana) elephants in zoos have received considerable scrutiny in the last two decades because of concerns over welfare and management practices [2]. To create sustainable captive populations, it is important that zoo animal programs evaluate the basic husbandry needs of individual animals, as well as the more complex factors that may affect welfare in a captive environment. For example, an earlier study of 112 female zoo-housed elephants in North America found a significant effect of “facility” on longitudinal serum cortisol concentrations, but no significant effect of “species” or “management” (i.e., free contact—elephants and people share the same space; or protected contact—elephants and people are separated by a barrier) [3], suggesting that facility-specific factors exist that may affect stress and welfare status in captive elephants.

The elephant study population ranged in age from 0 to 64 years (mean age: Asian, 34.3 ±1.5; African, 27.7 ±1.1 years). Table 2 presents seasonal mean FGM concentrations for each species. Overall FGM concentrations were higher in Asian (124.4 ± 4.9 ng/g) than African (97.7 ± 3.0 ng/g) elephants. There was a significant main effect of species (F = 27.86, df1,2 = 1,927, P = 0.000), but not season (F = 1.30, df1,2 = 3,927, P = 0.0001). In all seasons, Asian elephants had higher mean concentrations than Africans.

Epidemiological analyses of the EWP data point to a number of individual, social, housing and management factors that might affect adrenal activity in the zoo-housed elephant population in North America. A higher risk of elevated FGM concentrations was found for Asian elephants with joint abnormalities, and African elephants housed in mixed-sex herds, whereas all elephants housed in northern latitudes had an increased risk of higher FGM in the spring (Asians) or all seasons (Africans). More importantly, the results point to management factors that decrease FGMs in both species: having choice of being indoors and out, and management interactions with staff (Africans). The variability in FGM concentrations (CV) was reduced by enrichment and social groupings, and increased by having a choice of indoor and outdoor spaces. Interestingly, univariate analyses indicated that walking distance and all three space experience variables were negatively correlated to FGM in Asian elephants, but positively associated in African elephants. These patterns suggest there are species differences in how housing space is experienced, which may indicate that species-specific management protocols are needed.

Results elucidate species differences in FGM concentrations of elephants in relation to a variety of zoo environments. A stress-related welfare problem was identified among Asian elephants with joint health problems. African elephants appear to be more responsive to social stressors than Asians, which fits with their natural history. African elephants form complex, multi-tiered social groups that are important to survival, whereas Asian herds are smaller and bonds are more fluid [63]. One factor that reduced FGMs for both species was more time being managed, suggesting time spent with keepers has a positive effect. More time being managed also was associated with reduced stereotypy [43]. Finally having diverse enrichment options and contact with multiple social groups also appears to be calming for elephants, reducing intra-individual variability in FGMs. Together, all evidence points to the beneficial effects of diverse enrichment opportunities, including cognitive enrichment for zoo-housed elephants. We conclude that there are many avenues for further research on stress in zoo-housed elephants, and monitoring FGMs longitudinally is a proven non-invasive method for determining factors contributing to adrenal function, stress and coping responses in elephants. The species differences in FGM responses to zoo factors suggests that a one-size-fits-all management strategy may not be appropriate, and that more species-specific approaches to husbandry are needed.