Abstract
The health implications of increasing exposure of marine mammals to environmental and anthropogenic stressors have been of major concern, warranting a better understanding of underlying physiology. This study screened gene expression profiles of ten stress and immune-related biomarkers using real-time polymerase chain reaction in both wild and aquarium belugas, reporting their reference ranges. Blood (n = 75) and skin (n = 73) samples were collected from wild belugas following live capture–release health assessments during 2008, 2012–2014 in Bristol Bay (58.86°N, 158.70°W), and subsistence hunts during 2012–2014 in Eastern Chukchi Sea (69.75°N, 163.05°W) in Alaska. Blood samples were also collected from five aquarium belugas (41.3733°N, 71.9533°W) in Mystic, Connecticut, under behavioral control. Live-captured whales showed significant (p < 0.05) down-regulation of interferon-gamma (IFNγ) pre- versus post-examination blood along with increasing serum cortisol levels, indicative of physiological response to capture stress. Wild belugas also displayed higher levels of inflammatory IFNγ when compared to aquarium whales. When compared to blood, skin samples displayed higher differentiation among the two wild populations based on t tests, principle component analysis and general linear model analysis including significant (multiple-test-corrected p < 0.05) seasonal and/or spatial effects. Interleukins IL10 and IL12, transforming growth factor beta (TGFβ), glucocorticoid receptor (Nr3c1), Toll-like receptor-4 (TLR4), and aryl hydrocarbon receptor (AHR) were the most informative biomarkers in skin reflecting gene expression changes between populations. Overall, biomarkers listed in this study were suggested as promising indicators of health status in belugas, and confirmed usefulness of skin as a minimally invasive matrix to capture population-level differences in free-ranging cetaceans.
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Acknowledgements
This study was funded by Office of Naval Research (ONR Award No: N00014-14-1-0411). The authors thank the Department of Wildlife Management, North Slope Borough, Barrow, AK, the Point Lay field team and the community of Point Lay, AK. The authors also thank the Bristol Bay field team along with the Bristol Bay Marine Mammal Council and Bristol Bay Native Association. The Alaska Beluga Whale Committee encouraged health studies on belugas. In addition, the authors acknowledge the Mystic Aquarium animal care team, the Arctic Coast husbandry team and research staff for their collaboration and assistance in sampling aquarium whales. This constitutes scientific contribution #286 from the Sea Research Foundation.
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Funding for this study is provided by Office of Naval Research, Marine Mammals and Biology Program (ONR Award No: N00014-14-1-0411).
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All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. Sampling of belugas in Bristol Bay, AK, was conducted under National Marine Fisheries Service Scientific Research Permit #782-1719 (for the year 2008) and #14245 (for the years 2012–2014), and IACUC #AFSC/NWFC 2012-1 (for the years 2012–2014). Sampling of subsistence-hunted whales from Eastern Chukchi Sea was conducted under permit #17350 issued to the Department of Wildlife Management, North Slope Borough, AK. The research samples admitted at Mystic Aquarium between 2008 and 2012 were under NOAA/NMFS permit #42-1908; samples admitted from 2013 and 2014 were under permit #17298. This article does not contain any studies with human participants performed by any of the authors.
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Unal, E., Goertz, C.E.C., Hobbs, R.C. et al. Investigation of molecular biomarkers as potential indicators of health in wild belugas (Delphinapterus leucas). Mar Biol 165, 182 (2018). https://doi.org/10.1007/s00227-018-3439-3
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DOI: https://doi.org/10.1007/s00227-018-3439-3