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      Urinary Cortisol Increases During a Respiratory Outbreak in Wild Chimpanzees

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          Abstract

          Abstract: In mammals, the excretion of cortisol can provide energy toward restoring homeostasis and is a major component of the stress response. However, chronically elevated cortisol levels also have suppressive effects on immune function. As mounting an immune response is energetically costly, sick individuals may conserve energy by exhibiting certain sickness behaviors, such as declining activity levels. Due to the complex interplay between immune function and sickness behaviors, endocrinological correlates have received growing attention in the medical community, but so far, this subject was investigated rarely. Furthermore, given the complexities of studying illnesses and immunity in natural settings, correlates of sickness behaviors have yet to be studied in non-human primates in the wild.

          Methods: We measured urinary cortisol levels using liquid chromatography–mass spectrometry in a group of wild habituated chimpanzees in Taï National Park, Côte d'Ivoire, before, during, and after a respiratory disease outbreak (main causative pathogen: human respiratory syncytial virus A, with coinfections of Streptococcus pneumoniae). Changes in cortisol levels were then related to urinary neopterin levels, a biomarker of immune system activation.

          Results: Urinary cortisol levels were found to be more than 10-fold higher during the outbreak in comparison with levels before and after the outbreak period. Increasing cortisol levels were also associated with increasing neopterin levels. Interestingly, rather atypical patterns in a diurnal decline of cortisol levels were found during infection periods, such that levels remained raised throughout the day.

          Conclusion: In conclusion, cortisol increase was related to cellular immune response. Our results suggest that cortisol is a mediator of infectious disease pathogenicity through its impact on the immune system and that wild chimpanzees may be facing energetic stress when sick. By monitoring immune challenges in wild-living animals, our study demonstrates that immune defenses have costs and that these costs are context-specific.

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          Most cited references59

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          Conclusions beyond support: overconfident estimates in mixed models

          Mixed-effect models are frequently used to control for the nonindependence of data points, for example, when repeated measures from the same individuals are available. The aim of these models is often to estimate fixed effects and to test their significance. This is usually done by including random intercepts, that is, intercepts that are allowed to vary between individuals. The widespread belief is that this controls for all types of pseudoreplication within individuals. Here we show that this is not the case, if the aim is to estimate effects that vary within individuals and individuals differ in their response to these effects. In these cases, random intercept models give overconfident estimates leading to conclusions that are not supported by the data. By allowing individuals to differ in the slopes of their responses, it is possible to account for the nonindependence of data points that pseudoreplicate slope information. Such random slope models give appropriate standard errors and are easily implemented in standard statistical software. Because random slope models are not always used where they are essential, we suspect that many published findings have too narrow confidence intervals and a substantially inflated type I error rate. Besides reducing type I errors, random slope models have the potential to reduce residual variance by accounting for between-individual variation in slopes, which makes it easier to detect treatment effects that are applied between individuals, hence reducing type II errors as well.
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            How stress influences the immune response.

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              Hormonal and immunological mechanisms mediating sex differences in parasite infection.

              S L Klein (2004)
              The prevalence and intensity of infections caused by protozoa, nematodes, trematodes, cestodes, and arthropods is higher in males than females. The primary thesis of this review is that immunological differences exist between the sexes that may underlie increased parasitism in males compared to females. Several field and laboratory studies link sex differences in immune function with circulating steroid hormones; thus, the roles of sex steroids, including testosterone, oestradiol, and progesterone, as well as glucocorticoids will be discussed. Not only can host hormones affect responses to infection, but parasites can both produce and alter hormone concentrations in their hosts. The extent to which changes in endocrine-immune interactions following infection are mediated by the host or the parasite will be considered. Although males are more susceptible than females to many parasites, there are parasites for which males are more resistant than females and endocrine-immune interactions may underlie this sex reversal. Finally, although immunological differences exist between the sexes, genetic and behavioural differences may explain some variability in response to infection and will be explored as alternative hypotheses for how differences between the sexes contribute to dimorphic responses to parasites.
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                Author and article information

                Contributors
                Journal
                Front Vet Sci
                Front Vet Sci
                Front. Vet. Sci.
                Frontiers in Veterinary Science
                Frontiers Media S.A.
                2297-1769
                21 August 2020
                2020
                : 7
                : 485
                Affiliations
                [1] 1Max Planck Institute for Evolutionary Anthropology , Leipzig, Germany
                [2] 2Endocrinology Laboratory, German Primate Center, Leibniz Institute for Primate Research , Göttingen, Germany
                [3] 3Epidemiology of Highly Pathogenic Microorganisms, Robert Koch Institute , Berlin, Germany
                [4] 4Taï Chimpanzee Project, Centre Suisse de Recherches Scientifiques en Côte d'Ivoire , Abidjan, Côte d'Ivoire
                Author notes

                Edited by: Jeremy N. Marchant-Forde, Livestock Behavior Research Unit (USDA-ARS), United States

                Reviewed by: Liza Rose Moscovice, Leibniz Institute for Farm Animal Biology (FBN), Germany; Moira Harris, Harper Adams University, United Kingdom

                *Correspondence: Verena Behringer Verena_behringer@ 123456eva.mpg.de

                This article was submitted to Animal Behavior and Welfare, a section of the journal Frontiers in Veterinary Science

                Article
                10.3389/fvets.2020.00485
                7472655
                32974394
                488beabd-3cde-426e-8ff0-97e6e8ce158a
                Copyright © 2020 Behringer, Preis, Wu, Crockford, Leendertz, Wittig and Deschner.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 03 April 2020
                : 29 June 2020
                Page count
                Figures: 2, Tables: 2, Equations: 0, References: 83, Pages: 9, Words: 7395
                Funding
                Funded by: Max-Planck-Gesellschaft 10.13039/501100004189
                Funded by: Deutsche Forschungsgemeinschaft 10.13039/501100001659
                Funded by: H2020 European Research Council 10.13039/100010663
                Categories
                Veterinary Science
                Original Research

                disease monitoring,non-invasive,pan troglodytes,ecoimmunology,costly immune responses

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