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      Lifetime glucocorticoid profiles in baleen of right whale calves: potential relationships to chronic stress of repeated wounding by Kelp Gulls

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          Abstract

          Baleen from stranded carcasses of five right whale calves (four southern and one North Atlantic) contain cortisol and corticosterone patterns that may represent longitudinal profiles of stress exposure over time. Calves with high wounding from Kelp Gulls had markedly higher glucocorticoids in postnatal baleen than did less wounded and unwounded calves.

          Abstract

          Baleen tissue accumulates stress hormones (glucocorticoids, GC) as it grows, along with other adrenal, gonadal and thyroid hormones. The hormones are deposited in a linear fashion such that a single plate of baleen allows retrospective assessment and evaluation of long-term trends in the whales’ physiological condition. In whale calves, a single piece of baleen contains hormones deposited across the lifespan of the animal, with the tip of the baleen representing prenatally grown baleen. This suggests that baleen recovered from stranded carcasses of whale calves could be used to examine lifetime patterns of stress physiology. Here we report lifetime profiles of cortisol and corticosterone in baleen of a North Atlantic right whale (‘NARW’— Eubalaena glacialis) calf that died from a vessel strike, as well as four southern right whale (‘SRW’— Eubalaena australis) calves that were found dead with varying severity of chronic wounding from Kelp Gull ( Larus dominicanus) attacks. In all five calves, prenatally grown baleen exhibited a distinctive profile of elevated glucocorticoids that declined shortly before birth, similar to GC profiles reported from baleen of pregnant females. After birth, GC profiles in calf baleen corresponded with the degree of wounding. The NARW calf and two SRW calves with no or few gull wounds had relatively low and constant GC content throughout life, while two SRW calves with high numbers of gull wounds had pronounced elevations in baleen GC content in postnatal baleen followed by a precipitous decline shortly before death, a profile suggestive of prolonged chronic stress. Baleen samples may present a promising and valuable tool for defining the baseline physiology of whale calves and may prove useful for addressing conservation-relevant questions such as distinguishing acute from chronic stress and, potentially, determining cause of death.

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          The concept of allostasis in biology and biomedicine.

          Living organisms have regular patterns and routines that involve obtaining food and carrying out life history stages such as breeding, migrating, molting, and hibernating. The acquisition, utilization, and storage of energy reserves (and other resources) are critical to lifetime reproductive success. There are also responses to predictable changes, e.g., seasonal, and unpredictable challenges, i.e., storms and natural disasters. Social organization in many populations provides advantages through cooperation in providing basic necessities and beneficial social support. But there are disadvantages owing to conflict in social hierarchies and competition for resources. Here we discuss the concept of allostasis, maintaining stability through change, as a fundamental process through which organisms actively adjust to both predictable and unpredictable events. Allostatic load refers to the cumulative cost to the body of allostasis, with allostatic overload being a state in which serious pathophysiology can occur. Using the balance between energy input and expenditure as the basis for applying the concept of allostasis, we propose two types of allostatic overload. Type 1 allostatic overload occurs when energy demand exceeds supply, resulting in activation of the emergency life history stage. This serves to direct the animal away from normal life history stages into a survival mode that decreases allostatic load and regains positive energy balance. The normal life cycle can be resumed when the perturbation passes. Type 2 allostatic overload begins when there is sufficient or even excess energy consumption accompanied by social conflict and other types of social dysfunction. The latter is the case in human society and certain situations affecting animals in captivity. In all cases, secretion of glucocorticosteroids and activity of other mediators of allostasis such as the autonomic nervous system, CNS neurotransmitters, and inflammatory cytokines wax and wane with allostatic load. If allostatic load is chronically high, then pathologies develop. Type 2 allostatic overload does not trigger an escape response, and can only be counteracted through learning and changes in the social structure.
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            A consensus endocrine profile for chronically stressed wild animals does not exist.

            Given the connection between chronic stress and health, there has been a growing emphasis on identifying chronically stressed wild animals, especially in relation to anthropogenic disturbances. There is considerable confusion, however, in how to identify chronically stressed wild animals, but the most common assumption is that measures of glucocorticoid (GC) function will increase. In an attempt to determine an "endocrine profile" of a chronically stressed wild animal, this review collected papers from the literature that measured baseline GC, stress-induced GC, measures of integrated GC, negative feedback, hypothalamic-pituitary-adrenal axis sensitivity, and/or body weight in chronically stressed animals. The collected studies encompassed laboratory and field studies, numerous diverse species, and multiple techniques for inducing chronic stress. Each paper was ranked according to its relevance to wild animals and scored as to whether the measured response increased, decreased, or stayed the same after exposure to chronic stress. The analyses uncovered so much variation between studies that the literature does not support a generalized endocrine profile in how wild animals respond to chronic stress. The common predictions appear to be based almost entirely on theoretical models rather than empirical data. The three most important variables affecting GC responses were the stressors used to induce chronic stress, the potential for those stressors to induce habituation, and the taxon of the focal species. The best approach for identifying a chronically stressed population appears to be documentation of changes at multiple levels of GC regulation, but the direction of the change (increase or decrease) may be relatively unimportant compared to the fact that the response changes at all. The conclusion is that a consistent, predictable, endocrine response to chronic stress, regardless of the protocol used to induce chronic stress and the species under study, does not exist. Copyright © 2013 Elsevier Inc. All rights reserved.
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              Exposure to chronic stress downregulates corticosterone responses to acute stressors.

              We used captive European starlings (Sturnus vulgaris) to test whether corticosterone responses differed in birds held under normal laboratory conditions or conditions of chronic stress. Surprisingly, both basal corticosterone concentrations and corticosterone responses to acute stress were significantly reduced when birds were chronically stressed. To determine the mechanism underlying this reduced response, animals under both conditions were injected with lactated Ringer's solution (control), adrenocorticotropin (ACTH), arginine vasotocin (AVT), or dexamethasone (DEX). ACTH increased corticosterone concentrations above stress-induced levels in both cases, although maximum responses were lower in chronically stressed birds. AVT did not augment the corticosterone response under nonchronically stressed conditions, but it did under chronically stressed conditions. DEX reduced maximal corticosterone concentrations in both cases. Neither ovine nor rat corticotropin-releasing factor (CRF) altered normal stress responses. These data indicate that changes in responsiveness of the hypothalamic-pituitary-adrenal axis to ACTH and AVT serve to downregulate corticosterone responses during chronic stress. Furthermore, these data lead to the following hypothesis: ACTH output from the pituitary limits maximum corticosterone concentrations under normal conditions, but reduced AVT release from the hypothalamus regulates lower corticosterone concentrations under chronic stress conditions.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                Conserv Physiol
                Conserv Physiol
                conphys
                Conservation Physiology
                Oxford University Press
                2051-1434
                2018
                20 August 2018
                20 August 2018
                : 6
                : 1
                : coy045
                Affiliations
                [1 ]Center for Bioengineering Innovation, Department of Biological Sciences, Northern Arizona University, 617 S. Beaver St., Flagstaff, AZ, USA
                [2 ]Instituto de Conservación de Ballenas, Capital Federal, O’Higgins 4380, Ciudad Autónoma de Buenos Aires, Argentina
                [3 ]Southern Right Whale Health Monitoring Program, Los Alerces 3376, Puerto Madryn, Chubut, Argentina
                [4 ]School of Veterinary Medicine, University of California, 1089 Veterinary Medicine Drive Ground Floor West, Davis, CA, USA
                [5 ]Department of Biology, University of Utah, 257 South 1400 East University of Utah, Salt Lake City, UT, USA
                [6 ]Ocean Alliance/Whale Conservation Institute, 32 Horton St, Gloucester, MA, USA
                [7 ]Diversidad Biológica IV, Universidad Nacional de Córdoba, Av. Vélez Sársfield 299, Córdoba, Argentina
                Author notes
                Corresponding author: Biological Sciences & Center for Bioengineering Innovation, Northern Arizona University, Flagstaff, AZ 86011, USA. Email: aaf269@ 123456nau.edu
                Article
                coy045
                10.1093/conphys/coy045
                6101610
                30151197
                942873e0-d65b-4031-9859-e5c64d5c160c
                © The Author(s) 2018. 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 ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                : 13 April 2018
                : 13 July 2018
                : 30 July 2018
                Page count
                Pages: 12
                Funding
                Funded by: Northern Arizona University 10.13039/100008883
                Funded by: Arizona Board of Regents Technology Research Initiative Fund
                Funded by: Fulbright-Ministerio de Educación y Deportes de la República Argentina
                Categories
                Research Article

                baleen,calves,corticosterone,cortisol,stress,validations
                baleen, calves, corticosterone, cortisol, stress, validations

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