Effects of physiological changes and social life events on adrenal glucocorticoid activity in female zoo-housed Asian elephants (Elephas maximus)

Abstract

Ensuring good health and welfare is an increasingly important consideration for conservation of endangered species and includes breeding of individuals managed under human care. Understanding how factors in the captive environment affect individual animal wellbeing can be aided by long-term monitoring of biological functioning. This study involved longitudinal assessments (4 to 28 years) of reproductive and adrenal hormones in zoo-housed female Asian elephants (Elephas maximus) (age range 4 to ~71 years) to elucidate patterns in adrenal glucocorticoid (GC) activity in association with reproductive and demographic factors, and examine individual response to major social changes. Concentrations of serum and urinary cortisol covaried more consistently with physiological changes (ovarian cycle phase, puberty, pregnancy, lactational anestrus, and age) than with social life events (births, deaths, and facility transfers). Cortisol fluctuated across the ovarian cycle with mean concentrations being higher in the follicular than in the luteal phase, and concentrations were highest in lactational anestrous compared to all other reproductive states. The elephants in this study exhibited substantial individuality in adrenal GC response to major social change, reinforcing the need to assess welfare on an individual basis and to consider factors influencing the impact of perceived stressors, such as social relationships, social support, temperament, and life history. Outcomes from this study deepen our understanding of Asian elephant physiology and highlight the importance of taking intrinsic patterns of hormone secretion into account when evaluating the impact of external factors. Finally, a better understanding of the impact of social change and resiliency in response to real and perceived stressors allows us to improve social management to enhance welfare in both captive settings and free-ranging environments.

Supporting Zoo Asian Elephant (Elephas maximus) Welfare and Herd Dynamics with a More Complex and Expanded Habitat

“…The continued and regular ovarian cycling observed in females throughout the construction period and transition to the new habitat represents one indicator of normal reproductive health and welfare for the female elephants in this study. In our previous long-term study of gonadal [ 75 ] and adrenal activity [ 102 ] of female Asian elephants, we found that major life events—births, deaths, changes in herd structure—had minimal effect on estrous-cycle dynamics over time and adrenal responses were activated only short-term, suggesting that the Oregon Zoo’s female elephants are quite resilient and maintain normal reproductive and adrenal health. Historically, male elephants at the Oregon Zoo exhibited typical annual musth cycles [ 71 ].…”

“…Jakob-Hoff et al [ 115 ] observed increased vigilance and apprehension in zoo elephants exposed to short periods of construction noise, but construction disturbance occurred over an extended time in the current study, so there was potential for habituation and there was no evidence of any lasting negative effects. Although the females in this study historically have not exhibited signs of chronic stress [ 102 ], Carlstead and Brown [ 116 ] argue that high variability in longitudinal FGM data may be a better measure of increased reactivity than increased mean levels, because the best indicator of chronic stress in animals subjected to intense stressors of long duration or repetitiveness may be more frequent or exaggerated glucocorticoid responses to new and acutely presented stressors (Mason et al, in prep).…”

“…In this time period, Female 2 spent more time with M-juvenile than did the other females, and although her agonistic interactions with M-juvenile decreased in the new habitat, courtship and mating-related behaviors were observed by staff, and these interactions can temporarily increase adrenal activity and thus affect overall glucocorticoid concentrations [ 51 ] For Female 3, the confounding factor of reproductive state needs to be considered. Glaeser et al [ 102 ] showed that serum cortisol covaried with reproductive state in female Asian elephants, and with her first calf, Female 3 exhibited her highest mean serum cortisol concentrations during lactational anestrous, followed by pregnancy, then normal cycling. In the current study, she was in lactational anestrous for the first 34 of 140 weeks of construction, and then resumed normal cycling while continuing to nurse her calf, so reproductive state alone does not account for her increase in median concentrations during construction.…”

Diurnal variation in serum concentrations of cortisol in captive African (Loxodonta africana) and Asian (Elephas maximus) elephants

“…For example, serum concentrations of cortisol are significantly negatively correlated with progesterone during the average 14‐week long estrous cycles in captive African elephants (Bechert et al, 1999). In Asian elephants, no difference in serum cortisol concentrations during the estrous cycle was found (Oliveira et al, 2008); however, a subsequent study with a greater number of Asian elephants did find regular cortisol peaks during the second half of the follicular phase followed by lower levels during the luteal phase (Fanson et al, 2014; Glaeser et al, 2020) similar to African elephants. Progesterone can: (1) increase the rate of dissociation of GCs from receptors by binding GC and mineralocorticoid receptors; (2) modulate the receptor number in the hippocampus; and (3) diminish the effectiveness of cortisol feedback on stress responsiveness (Kudielka & Kirschbaum, 2005).…”

Effects of Positive Reinforcement Training and Novel Object Exposure on Salivary Cortisol Levels under Consideration of Individual Variation in Captive African Elephants (Loxodonta africana)

“…In both elephant species, studies revealed inter-individual variation in GC responses to captive husbandry situations in all sampling matrices (African elephant, blood: [ 21 ], saliva: [ 31 ]; Asian elephant, feces: [ 55 ], blood and urine: [ 56 ]). The individual factors shown to influence GC levels within or between individual elephants include age (African elephant: [ 57 ]; Asian elephant: [ 56 ]), sex (wild African elephant: [ 19 ]), facility [ 23 ], personality (African elephant: [ 29 ]; Asian elephant: [ 55 ]), day time [ 28 , 29 , 58 , 59 , 60 ] and reproductive status or ovarian cycle phase (African and Asian elephant: [ 61 ]; African elephant: [ 62 , 63 ]; Asian elephant: [ 56 , 64 , 65 ]).…”