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      Management factors affecting adrenal glucocorticoid activity of tourist camp elephants in Thailand and implications for elephant welfare

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          Abstract

          Elephant camps are among the most popular destinations in Thailand for tourists from many countries. A wide range of management strategies are used by these camps, which can have varied impacts on health and welfare of elephants. The objectives of this study were to examine relationships between FGM (fecal glucocorticoid metabolite) concentrations and camp management factors (work routine, walking, restraint, rest area, foraging), and to other welfare indicators (stereotypic behaviors, body condition, foot health, and skin wounds). Data were obtained on 84 elephants (18 males and 66 females) from 15 elephant camps over a 1-year period. Elephants were examined every 3 months and assigned a body condition score, foot score, and wound score. Fecal samples were collected twice monthly for FGM analysis. Contrary to some beliefs, elephants in the observation only program where mahouts did not carry an ankus for protection had higher FGM concentrations compared to those at camps that offered riding with a saddle and shows. Elephants that were tethered in the forest at night had lower FGM concentrations compared to elephants that were kept in open areas inside the camps. There was an inverse relationship between FGM concentrations and occurrence of stereotypy, which was not anticipated. Thus, assessing adrenal activity via monitoring of FGM concentrations can provide important information on factors affecting the well-being of elephants. Results suggest that more naturalistic housing conditions and providing opportunities to exercise may be good for elephants under human care in Thailand, and that a no riding, no hook policy does not necessarily guarantee good welfare.

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          Most cited references63

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          Akaike's information criterion in generalized estimating equations.

          W. Pan (2001)
          Correlated response data are common in biomedical studies. Regression analysis based on the generalized estimating equations (GEE) is an increasingly important method for such data. However, there seem to be few model-selection criteria available in GEE. The well-known Akaike Information Criterion (AIC) cannot be directly applied since AIC is based on maximum likelihood estimation while GEE is nonlikelihood based. We propose a modification to AIC, where the likelihood is replaced by the quasi-likelihood and a proper adjustment is made for the penalty term. Its performance is investigated through simulation studies. For illustration, the method is applied to a real data set.
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            Stereotypies: a critical review

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              Use of fecal glucocorticoid metabolite measures in conservation biology research: considerations for application and interpretation.

              Fecal glucocorticoid metabolite analyses are increasingly being used by a variety of scientists (e.g., conservation biologists, animal scientists) to examine glucocorticoid (i.e., stress hormone) secretion in domestic and wild vertebrates. Adrenocortical activity (i.e., stress response) is of interest to conservation biologists because stress can alter animal behavior, reduce resistance to disease, and affect population performance. The noninvasiveness of fecal-based assessments is attractive, particularly when studying endangered species, because samples can often be obtained without disturbing the animal. Despite such advantages, many confounding factors inhibit the utility of this technique in addressing conservation problems. In particular, interpretation of fecal glucocorticoid metabolite (FGM) measures may be confounded by the length of time animals are held in captivity, normal seasonal and daily rhythms, body condition, sample storage and treatment techniques, diet of the animal, assay selection, animal status (i.e., social ranking, reproductive status), sample age and condition, and sample mass. Further complicating interpretation and utility of these measures is the apparent species-specific response to these factors. The purpose of this paper is to discuss the factors that confound interpretation of FGM measures, summarize research that addresses these issues, and offer an agenda for future research and interpretation. We urge conservation biologists to carefully consider confounding factors and the relationship between FGM secretion and population performance and biological costs when investigating effects of environmental and human-induced disturbances on wildlife. The crisis nature of many decisions in conservation biology often requires decisions from limited data; however, confirmatory results should not be posited when data are incomplete or confounding factors are not understood. Building reliable databases, and research with surrogate species when possible, will aid future efforts and enhance the utility of FGM assays.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: ResourcesRole: ValidationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Formal analysisRole: Funding acquisitionRole: MethodologyRole: SupervisionRole: Writing – review & editing
                Role: ConceptualizationRole: Funding acquisitionRole: MethodologyRole: Project administration
                Role: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: Validation
                Role: Funding acquisitionRole: MethodologyRole: Project administrationRole: SupervisionRole: ValidationRole: Writing – review & editing
                Role: ConceptualizationRole: Formal analysisRole: MethodologyRole: SoftwareRole: SupervisionRole: Writing – review & editing
                Role: ConceptualizationRole: MethodologyRole: Resources
                Role: ConceptualizationRole: Methodology
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: SupervisionRole: ValidationRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                1 October 2019
                2019
                : 14
                : 10
                : e0221537
                Affiliations
                [1 ] Center of Elephant and Wildlife Research, Chiang Mai University, Chiang Mai, Thailand
                [2 ] Department of Companion Animals and Wildlife Clinics, Faculty of Veterinary Medicine, Chiang Mai University, Chiang Mai, Thailand
                [3 ] Center for Species Survival, Smithsonian Conservation Biology Institute, Front Royal, VA, United States of America
                [4 ] Department of Veterinary Bioscience and Veterinary Public Health, Faculty of Veterinary Medicine, Chiang Mai University, Chiang Mai, Thailand
                [5 ] Department of Food Animal Clinic, Faculty of Veterinary Medicine, Chiang Mai University, Chiang Mai, Thailand
                [6 ] Excellent Center of Veterinary Public Health, Chiang Mai University, Chiang Mai, Thailand
                [7 ] National Elephant Institute, Lampang, Thailand
                University of Tasmania, AUSTRALIA
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Author information
                http://orcid.org/0000-0003-3898-7755
                http://orcid.org/0000-0002-3806-9746
                http://orcid.org/0000-0001-9319-5596
                Article
                PONE-D-19-13481
                10.1371/journal.pone.0221537
                6771993
                31574099
                0660f82b-4a2c-4094-bdb1-5ca57ad5b97e

                This is an open access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.

                History
                : 26 May 2019
                : 8 August 2019
                Page count
                Figures: 0, Tables: 7, Pages: 18
                Funding
                Funded by: National Research Council of Thailand
                Award ID: 170183
                Award Recipient :
                Funded by: Royal Golden Jubilee Ph.D. program, Thailand Research Fund
                Award ID: PHD/0187/2558
                Award Recipient :
                Funded by: Chiang Mai University
                Award Recipient :
                This work was supported by the National Research Council of Thailand (NRCT) (grant number 170183) http://www.trf.or.th/ for CT, the Royal Golden Jubilee Ph.D. program, Thailand Research Fund (TRF) (grant number PHD/0187/2558) for KN and PB http://rgj.trf.or.th/main/home/, and Chiang Mai University http://www.cmu.ac.th for CT for a research grant. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Vertebrates
                Amniotes
                Mammals
                Elephants
                Biology and Life Sciences
                Psychology
                Behavior
                Social Sciences
                Psychology
                Behavior
                Biology and Life Sciences
                Ecology
                Ecosystems
                Forests
                Ecology and Environmental Sciences
                Ecology
                Ecosystems
                Forests
                Ecology and Environmental Sciences
                Terrestrial Environments
                Forests
                Biology and Life Sciences
                Biochemistry
                Hormones
                Lipid Hormones
                Cortisol
                Biology and Life Sciences
                Biochemistry
                Hormones
                Steroid Hormones
                Cortisol
                Medicine and Health Sciences
                Public and Occupational Health
                Physical Activity
                Physical Fitness
                Exercise
                Medicine and Health Sciences
                Sports and Exercise Medicine
                Exercise
                Biology and Life Sciences
                Sports Science
                Sports and Exercise Medicine
                Exercise
                Biology and Life Sciences
                Biochemistry
                Metabolism
                Metabolites
                Biology and Life Sciences
                Agriculture
                Animal Management
                Animal Welfare
                Biology and Life Sciences
                Physiology
                Biological Locomotion
                Walking
                Medicine and Health Sciences
                Physiology
                Biological Locomotion
                Walking
                Custom metadata
                We confirm that data cannot be released publicly because there are ethical and legal restrictions on sharing our de-identified data set. The data contain potentially identifying or sensitive client information and could be used by animal rights organizations to launch media attacks against camps, and so we had to assure them their information would be safe from potential abuse. There is enough information in the camp descriptions to make them identifiable. In terms of who has imposed the restriction, we assured the camps that we would not release their data to gain participation. Data are available from the Chiang Mai University Institutional Data Access / Ethics Committee (Assoc. Prof. Dr. Nattawooti Sthitmatee, e-mail: nattawooti.s@ 123456cmu.ac.th , drneaw@ 123456gmail.com ) for researchers who meet the criteria for access to confidential data. This was acknowledged by Reviewer 1 as well, who said “not making all of their data accessible is reasonable in this situation.”

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