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      Multi-year patterns in testosterone, cortisol and corticosterone in baleen from adult males of three whale species

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          Abstract

          Baleen from three adult male whales (North Atlantic right, bowhead and blue) contains regularly spaced areas of high testosterone content suggestive of annual testosterone cycles. Patterns in glucocorticoids (cortisol and corticosterone) show potential relationships with breeding-related stress as well as with entanglement in fishing gear and possible disease episodes.

          Abstract

          Male baleen whales have long been suspected to have annual cycles in testosterone, but due to difficulty in collecting endocrine samples, little direct evidence exists to confirm this hypothesis. Potential influences of stress or adrenal stress hormones (cortisol, corticosterone) on male reproduction have also been difficult to study. Baleen has recently been shown to accumulate steroid hormones during growth, such that a single baleen plate contains a continuous, multi-year retrospective record of the whale’s endocrine history. As a preliminary investigation into potential testosterone cyclicity in male whales and influences of stress, we determined patterns in immunoreactive testosterone, two glucocorticoids (cortisol and corticosterone), and stable-isotope (SI) ratios, across the full length of baleen plates from a bowhead whale ( Balaena mysticetus), a North Atlantic right whale ( Eubalaena glacialis) and a blue whale ( Balaenoptera musculus), all adult males. Baleen was subsampled at 2 cm (bowhead, right) or 1 cm (blue) intervals and hormones were extracted from baleen powder with methanol, followed by quantification of all three hormones using enzyme immunoassays validated for baleen extract of these species. Baleen of all three males contained regularly spaced peaks in testosterone content, with number and spacing of testosterone peaks corresponding well to SI data and to species-specific estimates of annual baleen growth rate. Cortisol and corticosterone exhibited some peaks that co-occurred with testosterone peaks, while other glucocorticoid peaks occurred independent of testosterone peaks. The right whale had unusually high glucocorticoids during a period with a known entanglement in fishing gear and a possible disease episode; in the subsequent year, testosterone was unusually low. Further study of baleen testosterone patterns in male whales could help clarify conservation- and management-related questions such as age of sexual maturity, location and season of breeding, and the potential effect of anthropogenic and natural stressors on male testosterone cycles.

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          Seasonal changes in plasma glucocorticoid concentrations in free-living vertebrates.

          The vertebrate stress response helps animals respond to environmental dangers such as predators or storms. An important component of the stress response is glucocorticoid (GC) release, resulting from activation of the hypothalamic-pituitary-adrenal axis. After release, GCs induce a variety of behavioral and physiological changes that presumably help the animal respond appropriately to the situation. Consequently, GC secretion is often considered an obligatory response to stressful situations. Evidence now indicates, however, that free-living species from many taxa can seasonally modulate GC release. In other words, the magnitudes of both unstressed and stressed GC concentrations change depending upon the time of year. This review examines the growing evidence that GC concentrations in free-living reptiles, amphibians, and birds, but not mammals, are commonly elevated during the breeding season. This evidence is then used to test three hypotheses with different focuses on GC's energetic or behavioral effects, as well as on GC's role in preparing the animal for subsequent stressors. These hypotheses attempt to place annual GC rhythms into a physiological or behavioral context. Integrating seasonal differences in GC concentrations with either different physiological states or different life history stages provides clues to a new understanding of how GCs actually help in survival during stress. Consequently, understanding seasonal modulation of GC release has far-reaching importance for both the physiology of the stress response and the short-term survival of individual animals.
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            Reproduction and resistance to stress: when and how.

            Environmental and social stresses have deleterious effects on reproductive function in vertebrates. Global climate change, human disturbance and endocrine disruption from pollutants are increasingly likely to pose additional stresses that could have a major impact on human society. Nonetheless, some populations of vertebrates (from fish to mammals) are able to temporarily resist environmental and social stresses, and breed successfully. A classical trade-off of reproductive success for potential survival is involved. We define five examples. (i) Aged individuals with minimal future reproductive success that should attempt to breed despite potential acute stressors. (ii) Seasonal breeders when time for actual breeding is so short that acute stress should be resisted in favour of reproductive success. (iii) If both members of a breeding pair provide parental care, then loss of a mate should be compensated for by the remaining individual. (iv) Semelparous species in which there is only one breeding period followed by programmed death. (v) Species where, because of the transience of dominance status in a social group, individuals may only have a short window of opportunity for mating. We suggest four mechanisms underlying resistance of the gonadal axis to stress. (i) Blockade at the central nervous system level, i.e. an individual no longer perceives the perturbation as stressful. (ii) Blockade at the level of the hypothalamic-pituitary-adrenal axis (i.e. failure to increase secretion of glucocorticosteroids). (iii) Blockade at the level of the hypothalamic-pituitary-gonad axis (i.e. resistance of the reproductive system to the actions of glucocorticosteroids). (iv) Compensatory stimulation of the gonadal axis to counteract inhibitory glucocorticosteroid actions. Although these mechanisms are likely genetically determined, their expression may depend upon a complex interaction with environmental factors. Future research will provide valuable information on the biology of stress and how organisms cope. Such mechanisms would be particularly insightful as the spectre of global change continues to unfold.
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              Evidence that ship noise increases stress in right whales.

              Baleen whales (Mysticeti) communicate using low-frequency acoustic signals. These long-wavelength sounds can be detected over hundreds of kilometres, potentially allowing contact over large distances. Low-frequency noise from large ships (20-200 Hz) overlaps acoustic signals used by baleen whales, and increased levels of underwater noise have been documented in areas with high shipping traffic. Reported responses of whales to increased noise include: habitat displacement, behavioural changes and alterations in the intensity, frequency and intervals of calls. However, it has been unclear whether exposure to noise results in physiological responses that may lead to significant consequences for individuals or populations. Here, we show that reduced ship traffic in the Bay of Fundy, Canada, following the events of 11 September 2001, resulted in a 6 dB decrease in underwater noise with a significant reduction below 150 Hz. This noise reduction was associated with decreased baseline levels of stress-related faecal hormone metabolites (glucocorticoids) in North Atlantic right whales (Eubalaena glacialis). This is the first evidence that exposure to low-frequency ship noise may be associated with chronic stress in whales, and has implications for all baleen whales in heavy ship traffic areas, and for recovery of this endangered right whale population.
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                Author and article information

                Journal
                Conserv Physiol
                Conserv Physiol
                conphys
                Conservation Physiology
                Oxford University Press
                2051-1434
                2018
                21 September 2018
                21 September 2018
                : 6
                : 1
                : coy049
                Affiliations
                [1 ]Department of Biological Sciences, Center for Bioengineering Innovation, Northern Arizona University, Flagstaff, AZ, USA
                [2 ]Biology Department, University of Massachusetts Boston, Boston, MA, USA
                [3 ]Arctic Aquatic Research Division, Fisheries and Oceans Canada, Winnipeg, MB, Canada
                [4 ]Department of Biological Sciences, University of Manitoba, Winnipeg, MB, Canada
                [5 ]Department of Birds and Mammals, Greenland Institute of Natural Resources, Nuuk, Greenland
                [6 ]Marine Mammal Center, Woods Hole Oceanographic Institution, Woods Hole, MA, USA
                Author notes
                Corresponding author: Department of Biological Sciences, Center for Bioengineering Innovation, Northern Arizona University, Flagstaff, AZ 86011, USA. Tel: +503-501-8380. Email: Kathleen.Hunt@ 123456nau.edu
                Editor: Dr Steven Cooke
                Author information
                http://orcid.org/0000-0002-8058-5517
                Article
                coy049
                10.1093/conphys/coy049
                6148970
                30254748
                21e22cfd-ae44-4a61-8718-7f3ebc6d2fe3
                © 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
                : 27 April 2018
                : 05 August 2018
                : 1 September 2018
                Page count
                Pages: 16
                Categories
                Toolbox

                baleen,glucocorticoids,marine mammals,reproduction,stress,testosterone

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