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

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          Abstract

          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.

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          Coping styles in animals: current status in behavior and stress-physiology.

          This paper summarizes the current views on coping styles as a useful concept in understanding individual adaptive capacity and vulnerability to stress-related disease. Studies in feral populations indicate the existence of a proactive and a reactive coping style. These coping styles seem to play a role in the population ecology of the species. Despite domestication, genetic selection and inbreeding, the same coping styles can, to some extent, also be observed in laboratory and farm animals. Coping styles are characterized by consistent behavioral and neuroendocrine characteristics, some of which seem to be causally linked to each other. Evidence is accumulating that the two coping styles might explain a differential vulnerability to stress mediated disease due to the differential adaptive value of the two coping styles and the accompanying neuroendocrine differentiation.
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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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              Individual variation in glucocorticoid stress responses in animals.

              When stimuli from the environment are perceived to be a threat or potential threat then animals initiate stress responses, with activation of the hypothalamo-pituitary-adrenal axis and secretion of glucocorticoid hormones (cortisol and corticosterone). Whilst standard deviation or standard error values are always reported, it is only when graphs of individual responses are shown that the extensive variation between animals is apparent. Some animals have little or no response to a stressor that evokes a relatively large response in others. Glucocorticoid responses of fish, amphibian, reptiles, birds, and mammals are considered in this review. Comparisons of responses between animals and groups of animals focused on responses to restraint or confinement as relatively standard stressors. Individual graphs could not be found in the literature for glucocorticoid responses to capture or restraint in fish or reptiles, with just one graph in mammals with the first sample was collected when animals were initially restrained. Coefficients of variation (CVs) calculated for parameters of glucocorticoid stress responses showed that the relative magnitudes of variation were similar in different vertebrate groups. The overall mean CV for glucocorticoid concentrations in initial (0 min) samples was 74.5%, and CVs for samples collected over various times up to 4 h were consistently between 50% and 60%. The factors that lead to the observed individual variation and the extent to which this variation is adaptive or non-adaptive are little known in most animals, and future studies of glucocorticoid responses in animals can focus on individual responses and their origins and significance. Copyright © 2013 Elsevier Inc. All rights reserved.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Funding acquisitionRole: MethodologyRole: Project administrationRole: ResourcesRole: SupervisionRole: ValidationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Formal analysisRole: Funding acquisitionRole: MethodologyRole: Writing – review & editing
                Role: Formal analysisRole: InvestigationRole: MethodologyRole: Writing – original draft
                Role: Formal analysisRole: MethodologyRole: SoftwareRole: Supervision
                Role: Data curationRole: Formal analysisRole: MethodologyRole: Software
                Role: Formal analysisRole: MethodologyRole: SupervisionRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                4 September 2019
                2019
                : 14
                : 9
                : e0217326
                Affiliations
                [1 ] Center for Species Survival, Smithsonian Conservation Biology Institute, Front Royal, Virginia, United States of America
                [2 ] Department of Animal Science, North Carolina State University, Raleigh, North Carolina, United States of America
                [3 ] Department of Statistics, North Carolina State University, Raleigh, North Carolina, United States of America
                Humboldt-Universitat zu Berlin, GERMANY
                Author notes

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

                ‡ These authors also contributed equally to this work.

                Author information
                http://orcid.org/0000-0003-3898-7755
                Article
                PONE-D-19-12913
                10.1371/journal.pone.0217326
                6726191
                31483790
                b9a51aa9-e160-4c6c-ac3f-357372c4384b

                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
                : 7 May 2019
                : 20 August 2019
                Page count
                Figures: 1, Tables: 9, Pages: 18
                Funding
                This work was part of a large-scale project “Using Science to Understand Zoo Elephant Welfare”, awarded to JLB, KC by a 2010 National Leadership Grant from the Institute for Museum and Library Services (IMLS) (grant no. LG-25-10-0033-10) from the U.S. Additional funding was from the Shared Earth Foundation to JLB ( https://sharedearth.org). 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
                Earth Sciences
                Geography
                Cartography
                Latitude
                Biology and Life Sciences
                Biochemistry
                Metabolism
                Metabolites
                Biology and Life Sciences
                Biochemistry
                Hormones
                Lipid Hormones
                Cortisol
                Biology and Life Sciences
                Biochemistry
                Hormones
                Steroid Hormones
                Cortisol
                Earth Sciences
                Seasons
                Medicine and Health Sciences
                Epidemiology
                Medical Risk Factors
                Biology and Life Sciences
                Agriculture
                Animal Management
                Animal Welfare
                Earth Sciences
                Seasons
                Spring
                Custom metadata
                Due to ethical and legal restrictions on sharing our de-identified data set, data may be made available upon request. The data contain potentially identifying or sensitive client information and are owned by a third-party organization – Vistalogic, Inc. Data are available from Cheryl Meehan at Vistalogic, Inc. ( https://www.vistalogic.net) for researchers who meet the criteria for access to confidential data ( info@ 123456vistalogic.net ).

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