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      Assessment of stress levels and reproductive condition in giant pandas: insights from hair, faecal and saliva samples

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          Abstract

          This study demonstrates the potential of using hair as a reliable indicator of chronic stress levels in pandas, emphasizing the role of the relationship between sex hormones and cortisol in monitoring reproductive health and stress in wildlife.

          Abstract

          Concerted conservation efforts have brought the giant panda ( Ailuropoda melanoleuca) back from the brink of extinction, but pandas continue to face anthropogenic threats in the wild and breeding success in captivity remains low. Because stress can have detrimental impacts on reproduction, monitoring stress- and sex-steroid levels would help assess the effectiveness of conservation mitigation measures in panda populations as well as monitor the welfare and reproductive health of captive animals. In this proof-of-concept study, we used faecal sex steroid and cortisol concentrations ( n = 867 samples collected from five males and five females at Beijing Zoo every 4 days over the course of 12 months) as a reference to investigate if testosterone, estradiol, progesterone and cortisol can be meaningfully measured in panda hair ( n = 10) using radio-immuno-assays. Additionally, we calculated the ratio of testosterone to cortisol (T:C ratio) for each male, which can provide a biomarker of stress and physical performance. Our findings revealed distinct monthly variations in faecal sex-steroid and cortisol concentrations, reflecting reproductive seasonality and visitor-related stress among individual pandas. Notably, the oldest male had a significantly lower T:C ratio than other males. Our results confirm that the level of sex steroids and cortisol can be assayed by panda hair, and the hair cortisol concentrations correlate significantly with that in faeces with one month lag behind ( r = 0.68, P = 0.03). However, the concentrations of hormones detected in saliva are lower than those in faeces by two orders of magnitude, making it difficult to ensure accuracy. By assessing the applicability of hair, faecal and salivary sampling, we can infer their utility in monitoring the reproductive status and acute and chronic stress levels of giant pandas, thereby providing a means to gauge the success of ongoing habitat restoration efforts and to discuss the feasibility of sample collection from wild populations.

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          Allostatic load biomarkers of chronic stress and impact on health and cognition.

          The allostatic load model expands the stress-disease literature by proposing a temporal cascade of multi-systemic physiological dysregulations that contribute to disease trajectories. By incorporating an allostatic load index representing neuroendocrine, immune, metabolic, and cardiovascular system functioning, numerous studies have demonstrated greater prediction of morbidity and mortality over and beyond traditional detection methods employed in biomedical practice. This article reviews theoretical and empirical work using the allostatic load model vis-à-vis the effects of chronic stress on physical and mental health. Specific risk and protective factors associated with increased allostatic load are elucidated and policies for promoting successful aging are proposed.
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            Hair cortisol as a biological marker of chronic stress: current status, future directions and unanswered questions.

            The detrimental effects of stress on human health are being increasingly recognized. There is a critical need for the establishment of a biomarker that accurately measures its intensity and course over time. Such a biomarker would allow monitoring of stress, increase understanding of its pathophysiology and may help identify appropriate and successful management strategies. Whereas saliva and urine cortisol capture real-time levels, hair cortisol analysis presents a complementary means of monitoring stress, capturing systemic cortisol exposure over longer periods of time. This novel approach for cortisol quantification is being increasingly used to identify the effects of stress in a variety of pathological situations, from chronic pain to acute myocardial infarctions. Because of its ability to provide a long-term, month-by-month measure of systemic cortisol exposure, hair cortisol analysis is becoming a useful tool, capable of answering clinical questions that could previously not be answered by other tests. In this paper we review the development, current status, limitations and outstanding questions regarding the use of hair cortisol as a biomarker of chronic stress. Copyright © 2011 Elsevier Ltd. All rights reserved.
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              Testosterone and cortisol jointly regulate dominance: evidence for a dual-hormone hypothesis.

              Traditional theories propose that testosterone should increase dominance and other status-seeking behaviors, but empirical support has been inconsistent. The present research tested the hypothesis that testosterone's effect on dominance depends on cortisol, a glucocorticoid hormone implicated in psychological stress and social avoidance. In the domains of leadership (Study 1, mixed-sex sample) and competition (Study 2, male-only sample), testosterone was positively related to dominance, but only in individuals with low cortisol. In individuals with high cortisol, the relation between testosterone and dominance was blocked (Study 1) or reversed (Study 2). Study 2 further showed that these hormonal effects on dominance were especially likely to occur after social threat (social defeat). The present studies provide the first empirical support for the claim that the neuroendocrine reproductive (HPG) and stress (HPA) axes interact to regulate dominance. Because dominance is related to gaining and maintaining high status positions in social hierarchies, the findings suggest that only when cortisol is low should higher testosterone encourage higher status. When cortisol is high, higher testosterone may actually decrease dominance and in turn motivate lower status. Copyright © 2010 Elsevier Inc. All rights reserved.
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                Author and article information

                Contributors
                Journal
                Conserv Physiol
                Conserv Physiol
                conphys
                Conservation Physiology
                Oxford University Press
                2051-1434
                2024
                03 July 2024
                03 July 2024
                : 12
                : 1
                : coae044
                Affiliations
                Key Laboratory for Biodiversity and Ecological Engineering of Ministry of Education , Department of Ecology, College of Life Sciences, Beijing Normal University , No.19, Xinjiekouwai Street, Haidian District, Beijing 100875, China
                Key Laboratory for Biodiversity and Ecological Engineering of Ministry of Education , Department of Ecology, College of Life Sciences, Beijing Normal University , No.19, Xinjiekouwai Street, Haidian District, Beijing 100875, China
                Key Laboratory for Biodiversity and Ecological Engineering of Ministry of Education , Department of Ecology, College of Life Sciences, Beijing Normal University , No.19, Xinjiekouwai Street, Haidian District, Beijing 100875, China
                Beijing Key Laboratory of Captive Wildlife Technologies, Beijing Zoo , No.137, Xizhimenwai Street, Xicheng District, Beijing 100044, China
                Beijing Key Laboratory of Captive Wildlife Technologies, Beijing Zoo , No.137, Xizhimenwai Street, Xicheng District, Beijing 100044, China
                Beijing Key Laboratory of Captive Wildlife Technologies, Beijing Zoo , No.137, Xizhimenwai Street, Xicheng District, Beijing 100044, China
                Beijing Key Laboratory of Captive Wildlife Technologies, Beijing Zoo , No.137, Xizhimenwai Street, Xicheng District, Beijing 100044, China
                Beijing Key Laboratory of Captive Wildlife Technologies, Beijing Zoo , No.137, Xizhimenwai Street, Xicheng District, Beijing 100044, China
                Beijing Key Laboratory of Captive Wildlife Technologies, Beijing Zoo , No.137, Xizhimenwai Street, Xicheng District, Beijing 100044, China
                Beijing Key Laboratory of Captive Wildlife Technologies, Beijing Zoo , No.137, Xizhimenwai Street, Xicheng District, Beijing 100044, China
                Beijing Key Laboratory of Captive Wildlife Technologies, Beijing Zoo , No.137, Xizhimenwai Street, Xicheng District, Beijing 100044, China
                Beijing Key Laboratory of Captive Wildlife Technologies, Beijing Zoo , No.137, Xizhimenwai Street, Xicheng District, Beijing 100044, China
                Department of Biology , Irving K. Barber Faculty of Sciences, The University of British Columbia , Okanagan, Kelowna, British Columbia V1V 1V7, Canada
                Key Laboratory for Biodiversity and Ecological Engineering of Ministry of Education , Department of Ecology, College of Life Sciences, Beijing Normal University , No.19, Xinjiekouwai Street, Haidian District, Beijing 100875, China
                Author notes
                Corresponding authors: Xuefeng Liu, Beijing Zoo, No.137, Xizhimenwai Street, Xicheng District, Beijing 100044, China. Email: lxf9722@ 123456163.com ; Dingzhen Liu, College of Life Sciences, Beijing Normal University, No.19, Xinjiekouwai Street, Haidian District, Beijing 100875, China. Email: dzliu@ 123456bnu.edu.cn
                Author information
                https://orcid.org/0000-0003-1780-6134
                https://orcid.org/0000-0002-1870-6197
                Article
                coae044
                10.1093/conphys/coae044
                11221559
                38962510
                c3fedcb0-d0be-4deb-9e02-e1917eeacbee
                © The Author(s) 2024. Published by Oxford University Press and the Society for Experimental Biology.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( https://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                : 11 December 2023
                : 29 May 2024
                : 08 June 2024
                : 14 June 2024
                Page count
                Pages: 14
                Funding
                Funded by: Beijing Zoo;
                Award ID: 2021-Animal-037
                Funded by: National Forestry and Grassland Administration, DOI 10.13039/501100007825;
                Award ID: 21300211
                Funded by: National Natural Science Foundation of China, DOI 10.13039/501100001809;
                Award ID: 32270506
                Award ID: 31772466
                Categories
                Research Article
                AcademicSubjects/SCI00840

                chronic stress,conservation,cortisol,estrogen,fur,giant panda,non-invasive hormone monitoring,progesterone,sex steroid,testosterone

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