Skip to main content

Advertisement

Log in

Investigation of molecular biomarkers as potential indicators of health in wild belugas (Delphinapterus leucas)

  • Original paper
  • Published:
Marine Biology Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Altemus M, Rao B, Dhabhar FS, Ding W, Granstein RD (2001) Stress-induced changes in skin barrier function in healthy women. J Invest Dermatol 117(2):309–317

    CAS  PubMed  Google Scholar 

  • Beineke A, Siebert U, Wohlsein P, Baumgartner W (2010) Immunology of whales and dolphins. Vet Immunol Immunopathol 133(2–4):81–94

    CAS  PubMed  Google Scholar 

  • Bolkenius U, Hahn D, Gressner AM, Breitkopf K, Dooley S, Wickert L (2004) Glucocorticoids decrease the bioavailability of TGF-beta which leads to a reduced TGF-beta signaling in hepatic stellate cells. Biochem Biophys Res Commun 325(4):1264–1270

    CAS  PubMed  Google Scholar 

  • Bowen L, Miles AK, Murray M, Haulena M, Tuttle J, Van Bonn W, Adams L, Bodkin JL, Ballachey B, Estes J, Tinker MT, Keister R, Stott JL (2012) Gene transcription in sea otters (Enhydra lutris); development of a diagnostic tool for sea otter and ecosystem health. Mol Ecol Resour 12(1):67–74

    CAS  PubMed  Google Scholar 

  • Broeders S, Huber I, Grohmann L, Berben G, Taverniers I, Mazzara M, Roosens N, Morisset D (2014) Guidelines for validation of qualitative real-time PCR methods. Trends Food Sci Technol 37(2):115–126

    CAS  Google Scholar 

  • Buckman AH, Veldhoen N, Ellis G, Ford JK, Helbing CC, Ross PS (2011) PCB-associated changes in mRNA expression in killer whales (Orcinus orca) from the NE pacific ocean. Environ Sci Technol 45(23):10194–10202

    CAS  PubMed  Google Scholar 

  • Burek-Huntington KA, Dushane JL, Goertz CEC, Measures LN, Romero CH, Raverty SA (2015) Morbidity and mortality in stranded Cook Inlet beluga whales Delphinapterus leucas. Dis Aquat Org 114(1):45–60

    PubMed  Google Scholar 

  • Bustin SA, Benes V, Garson JA, Hellemans J, Huggett J, Kubista M, Mueller R, Nolan T, Pfaffl MW, Shipley GL, Vandesompele J, Wittwer CT (2009) The MIQE guidelines: minimum information for publication of Quantitative real-time PCR Experiments. Clin Chem 55(4):611

    CAS  PubMed  Google Scholar 

  • Castellini JM, Meiselman HJ, Castellini MA (1996) Understanding and interpreting hematocrit measurements in pinnipeds. Mar Mamm Sci 12(2):251–264

    Google Scholar 

  • Castellote M, Mooney TA, Quakenbush L, Hobbs R, Goertz C, Gaglione E (2014) Baseline hearing abilities and variability in wild beluga whales (Delphinapterus leucas). J Exp Biol 217(Pt 10):1682–1691

    PubMed  Google Scholar 

  • Chen T, Cao X (2010) Stress for maintaining memory: HSP70 as a mobile messenger for innate and adaptive immunity. Eur J Immunol 40(6):1541–1544

    CAS  PubMed  Google Scholar 

  • Dhabhar FS, Mcewen BS (1997) Acute stress enhances while chronic stress suppresses cell-mediated immunity in vivo: a potential role for leukocyte trafficking. Brain Behav Immun 11(4):286–306

    CAS  PubMed  Google Scholar 

  • Du Q, Min S, Chen LY, Ma YD, Guo XL, Wang Z, Wang ZG (2012) Major stress hormones suppress the response of macrophages through down-regulation of TLR2 and TLR4. J Surg Res 173(2):354–361

    CAS  PubMed  Google Scholar 

  • Dunn OJ (1961) Multiple comparisons among means. J Am Stat Assoc 56(293):52–64

    Google Scholar 

  • Elenkov IJ, Chrousos GP (1999) Stress hormones, Th1/Th2 patterns, pro/anti-inflammatory cytokines and susceptibility to disease. Trends Endocrinol Metab 10(9):359–368

    CAS  PubMed  Google Scholar 

  • Elenkov IJ, Chrousos GP (2006) Stress system—organization, physiology and immunoregulation. NeuroImmunoModulation 13(5–6):257–267

    CAS  PubMed  Google Scholar 

  • Engelhard GH, Brasseur SM, Hall AJ, Burton HR, Reijnders PJ (2002) Adrenocortical responsiveness in southern elephant seal mothers and pups during lactation and the effect of scientific handling. J Comp Physiol B 172(4):315–328

    CAS  PubMed  Google Scholar 

  • Fair PA, Schaefer AM, Romano TA, Bossart GD, Lamb SV, Reif JS (2014) Stress response of wild bottlenose dolphins (Tursiops truncatus) during capture-release health assessment studies. Gen Comp Endocrinol 206:203–212

    CAS  PubMed  Google Scholar 

  • Fair PA, Schaefer AM, Houser DS, Bossart GD, Romano TA, Champagne CD, Stott JL, Rice CD, White N, Reif JS (2017) The environment as a driver of immune and endocrine responses in dolphins (Tursiops truncatus). PLoS One 12(5):e0176202

    PubMed  PubMed Central  Google Scholar 

  • Fonfara S, Siebert U, Prange A (2007) Cytokines and acute phase proteins as markers for infection in harbor porpoises (Phocoena phocoena). Mar Mammal Sci 23(4):931–942

    CAS  Google Scholar 

  • Fonfara S, Kakuschke A, Rosenberger T, Siebert U, Prange A (2008) Cytokine and acute phase protein expression in blood samples of harbour seal pups. Mar Biol 155(3):337–345

    CAS  Google Scholar 

  • Fossi MC, Marsili L (2011) Multi-trial ecotoxicological diagnostic tool in cetacean skin biopsies. In: Uday K (ed) Skin biopsy—perspectives. InTech, Rijeka, pp 317–336 (ISBN: 978-953-307-290-6 ed)

    Google Scholar 

  • Gárate I, Garcia-Bueno B, Madrigal JL, Caso JR, Alou L, Gomez-Lus ML, Mico JA, Leza JC (2013) Stress-induced neuroinflammation: role of the toll-like receptor-4 pathway. Biol Psychiatry 73(1):32–43

    PubMed  Google Scholar 

  • Ghasemi A, Zahediasl S (2012) Normality tests for statistical analysis: a guide for non-statisticians. Int J Endocrinol Metab 10(2):486–489

    PubMed  PubMed Central  Google Scholar 

  • Gonzalez-Herrera L, Valenzuela A, Marchal JA, Lorente JA, Villanueva E (2013) Studies on RNA integrity and gene expression in human myocardial tissue, pericardial fluid and blood, and its postmortem stability. Forensic Sci Int 232(1–3):218–228

    CAS  PubMed  Google Scholar 

  • Gupta S, Halushka MK, Hilton GM, Arking DE (2012) Postmortem cardiac tissue maintains gene expression profile even after late harvesting. BMC Genom 13(1):26

    CAS  Google Scholar 

  • Hoffman JI, Thorne MA, Trathan PN, Forcada J (2013) Transcriptome of the dead: characterization of immune genes and marker development from necropsy samples in a free-ranging marine mammal. BMC Genom 14:52

    CAS  Google Scholar 

  • Hunt KE, Moore MJ, Rolland RM, Kellar NM, Hall AJ, Kershaw J, Raverty SA, Davis CE, Yeates LC, Fauquier DA, Rowles TK, Kraus SD (2013) Overcoming the challenges of studying conservation physiology in large whales: A review of available methods. Conserv Physiol 1(1):cot006-cot006

    Google Scholar 

  • Huntington HP (2009) A preliminary assessment of threats to arctic marine mammals and their conservation in the coming decades. Mar Policy 33(1):77–82

    Google Scholar 

  • Ierardi JL, Mancia A, McMillan J, Lundqvist ML, Romano TA, Wise JPS, Warr GW, Chapman RW (2009) Sampling the skin transcriptome of the North Atlantic right whale. Comp Biochem Physiol Part D Genom Proteom 4(3):154–158

    Google Scholar 

  • Iwasaki A, Medzhitov R (2004) Toll-like receptor control of the adaptive immune responses. Nat Immunol 5(10):987–995

    CAS  PubMed  Google Scholar 

  • Lee J, Hever A, Willhite D, Zlotnik A, Hevezi P (2005) Effects of RNA degradation on gene expression analysis of human postmortem tissues. Faseb J 19(10):1356–1358

    CAS  PubMed  Google Scholar 

  • Lehnert K, Ronnenberg K, Weijs L, Covaci A, Das K, Hellwig V, Siebert U (2016) Xenobiotic and immune-relevant molecular biomarkers in harbor seals as proxies for pollutant burden and effects. Arch Environ Contam Toxicol 70(1):106–120

    CAS  PubMed  Google Scholar 

  • Lewis S, Handy RD, Cordi B, Billinghurst Z, Depledge MH (1999) Stress proteins (HSP’s): methods of detection and their use as an environmental biomarker. Ecotoxicology 8(5):351–368

    CAS  Google Scholar 

  • Lowry L, O’Corry-Crowe G, Goodman D (2012) Delphinapterus leucas (Cook Inlet Subpopulation). The IUCN Red List of Threatened Species, e.T61442A17691385. http://www.iucnredlist.org/details/61442/0. Accessed 12 Oct 2018

  • Lunardi D, Abelli L, Panti C, Marsili L, Fossi MC, Mancia A (2016) Transcriptomic analysis of bottlenose dolphin (Tursiops truncatus) skin biopsies to assess the effects of emerging contaminants. Mar Environ Res 114:74–79

    CAS  PubMed  Google Scholar 

  • Maleszewski J, Lu J, Fox-Talbot K, Halushka MK (2007) Robust immunohistochemical staining of several classes of proteins in tissues subjected to autolysis. J Histochem Cytochem 55(6):597–606

    CAS  PubMed  Google Scholar 

  • Mancia A, Lundqvist ML, Romano TA, Peden-Adams MM, Fair PA, Kindy MS, Ellis BC, Gattoni-Celli S, McKillen DJ, Trent HF, Chen YA, Almeida JS, Gross PS, Chapman RW, Warr GW (2007) A dolphin peripheral blood leukocyte cDNA microarray for studies of immune function and stress reactions. Dev Comp Immunol 31(5):520–529

    CAS  PubMed  Google Scholar 

  • Mancia A, Warr GW, Chapman RW (2008) A transcriptomic analysis of the stress induced by capture-release health assessment studies in wild dolphins (Tursiops truncatus). Mol Ecol 17(11):2581–2589

    CAS  PubMed  Google Scholar 

  • Mancia A, Warr GW, Almeida JS, Veloso A, Wells RS, Chapman RW (2010) Transcriptome profiles: diagnostic signature of dolphin populations. Estuar Coasts 33(4):919–929

    Google Scholar 

  • Miles AK, Bowen L, Ballachey BE, Bodkin JL, Murray M, Estes JL, Keister RA, Stott JL (2012) Variations of transcript profiles between sea otters Enhydra lutris from Prince William Sound, Alaska, and clinically normal reference otters. Mar Ecol Prog Ser 451:201–212

    Google Scholar 

  • Moore SE, Huntington HP (2008) Arctic marine mammals and climate change: impacts and resilience. Ecol Appl 18(sp2):S157–S165

    PubMed  Google Scholar 

  • Moore SE, Reeves RR, Southall BL, Ragen TJ, Suydam RS, Clark CW (2012) A new framework for assessing the effects of anthropogenic sound on marine mammals in a rapidly changing Arctic. Bioscience 62(3):289–295

    Google Scholar 

  • Müller S, Lehnert K, Seibel H, Driver J, Ronnenberg K, Teilmann J, van Elk C, Kristensen J, Everaarts E, Siebert U (2013) Evaluation of immune and stress status in harbour porpoises (Phocoena phocoena): can hormones and mRNA expression levels serve as indicators to assess stress? BMC Vet Res 9(1):145

    PubMed  PubMed Central  Google Scholar 

  • Neely MG, Morey JS, Anderson P, Balmer BC, Ylitalo GM, Zolman ES, Speakman TR, Sinclair C, Bachman MJ, Huncik K, Kucklick J, Rosel PE, Mullin KD, Rowles TK, Schwacke LH, Van Dolah FM (2018) Skin transcriptomes of common bottlenose dolphins (Tursiops truncatus) from the Northern Gulf of Mexico and southeastern U.S. Atlantic coasts. Mar Genom 38:45–58

    Google Scholar 

  • Nielsen O, Burek-Huntington K, Loseto LL, Morell M, Romero CH (2018) Alphaherpesvirus: isolation, identification, partial characterisation, associated pathologic findings, and epidemiology in beluga whales (Delphinapterus leucas) in Alaska and Arctic Canada. Arctic Sci 4(3):338–357

    Google Scholar 

  • Noël M, Loseto LL, Helbing CC, Veldhoen N, Dangerfield NJ, Ross PS (2014) PCBs are associated with altered gene transcript profiles in Arctic beluga whales (Delphinapterus leucas). Environ Sci Technol 48(5):2942–2951

    PubMed  Google Scholar 

  • Norman SA, Goertz CE, Burek KA, Quakenbush LT, Cornick LA, Romano TA, Spoon T, Miller W, Beckett LA, Hobbs RC (2012) Seasonal hematology and serum chemistry of wild beluga whales (Delphinapterus leucas) in Bristol Bay, Alaska, USA. J Wildl Dis 48(1):21–32

    PubMed  Google Scholar 

  • Norman SA, Hobbs RC, Goertz CE, Burek-Huntington KA, Shelden KEW, Smith WA, Beckett LA (2016) Potential natural and anthropogenic impediments to the conservation and recovery of Cook Inlet beluga whales, Delphinapterus leucas. Mar Fish Rev 77:89–105

    Google Scholar 

  • O’Corry-Crowe GM, Suydam RS, Rosenberg A, Frost KJ, Dizon AE (1997) Phylogeography, population structure and dispersal patterns of the beluga whale Delphinapterus leucas in the Western Nearctic revealed by mitochondrial DNA. Mol Ecol 6(10):955–970

    Google Scholar 

  • Panjwani NN, Popova L, Srivastava PK (2002) Heat shock proteins gp96 and hsp70 activate the release of nitric oxide by APCs. J Immunol 168(6):2997

    CAS  PubMed  Google Scholar 

  • Panti C, Spinsanti G, Marsili L, Casini S, Frati F, Fossi MC (2011) Ecotoxicological diagnosis of striped dolphin (Stenella coeruleoalba) from the Mediterranean basin by skin biopsy and gene expression approach. Ecotoxicology 20(8):1791–1800

    CAS  PubMed  Google Scholar 

  • Peltier J, Perez J, Bellocq A, Escoubet B, Fouqueray B, Baud L (2003) Transforming growth factor-beta 1 increases glucocorticoid binding and signaling in macrophages through a Smad- and activated protein-1-mediated process. Kidney Int 63(6):2028–2036

    CAS  PubMed  Google Scholar 

  • Pfaffl MW, Tichopad A, Prgomet C, Neuvians TP (2004) Determination of stable housekeeping genes, differentially regulated target genes and sample integrity: bestKeeper–excel-based tool using pair-wise correlations. Biotechnol Lett 26(6):509–515

    CAS  PubMed  Google Scholar 

  • Prigent L, Robineau M, Jouneau S, Morzadec C, Louarn L, Vernhet L, Fardel O, Sparfel L (2014) The aryl hydrocarbon receptor is functionally upregulated early in the course of human T-cell activation. Eur J Immunol 44(5):1330–1340

    CAS  PubMed  Google Scholar 

  • Ramirez K (1999) Animal training: Successful animal management through positive reinforcement. John G Shedd Aquarium, Chicago

    Google Scholar 

  • Robeck TR, Monfort SL, Calle PP, Dunn JL, Jensen E, Boehm JR, Young S, Clark ST (2005) Reproduction, growth and development in captive beluga (Delphinapterus leucas). Zoo Biol 24(1):29–49

    Google Scholar 

  • Romano TA, Felten SY, Olschowka JA, Felten DL (1994) Noradrenergic and peptidergic innervation of lymphoid organs in the beluga, Delphinapterus leucas: an anatomical link between the nervous and immune systems. J Morphol 221(3):243–259

    CAS  PubMed  Google Scholar 

  • Romano TA, Olschowka JA, Felten SY, Quaranta V, Ridgway SH, Felten DL (2002) Immune response, stress, and environment: implications for cetaceans. In: Pfeiffer CJ (ed) Molecular and cell biology of marine mammals. Krieger Publishing Company, Malabar, pp 253–279

    Google Scholar 

  • Romano TA, Keogh MJ, Schlundt C, Carder D, Finneran J (2004) Anthropogenic sound and marine mammal health: measures of the nervous and immune systems before and after intense sound. Can J Fish Aquat Sci 61:1124–1134

    Google Scholar 

  • Romero LM, Meister CJ, Cyr NE, Kenagy GJ, Wingfield JC (2008) Seasonal glucocorticoid responses to capture in wild free-living mammals. Am J Physiol Regul Integr Comp Physiol 294(2):R614–R622

    CAS  PubMed  Google Scholar 

  • Schmitt TL, St. Aubin DJ, Schaefer AM, Dunn JL (2010) Baseline, diurnal variations, and stress-induced changes of stress hormones in three captive beluga whales, Delphinapterus leucas. Mar Mammal Sci 26(3):635–647

    CAS  Google Scholar 

  • Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 3(6):1101–1108

    CAS  PubMed  Google Scholar 

  • Sherry JP (2003) The role of biomarkers in the health assessment of aquatic ecosystems. Aquat Ecosyst Health Manag 6(4):423–440

    CAS  Google Scholar 

  • Sitt T, Bowen L, Blanchard MT, Smith BR, Gershwin LJ, Byrne BA, Stott JL (2008) Quantitation of leukocyte gene expression in cetaceans. Dev Comp Immunol 32(11):1253–1259

    CAS  PubMed  Google Scholar 

  • Sitt T, Bowen L, Lee CS, Blanchard MT, McBain J, Dold C, Stott JL (2016) Longitudinal evaluation of leukocyte transcripts in killer whales Orcinus orca). Vet Immunol Immunopathol 175:7–15

    CAS  PubMed  Google Scholar 

  • Spoon TR, Romano TA (2012) Neuroimmunological response of beluga whales (Delphinapterus leucas) to translocation and a novel social environment. Brain Behav Immun 26(1):122–131

    CAS  PubMed  Google Scholar 

  • St. Aubin DJ, Geraci JR (1989) Adaptive changes in hematologic and plasma chemical constituents in captive beluga whales, Delphinapterus leucas. Can J Fish Aquat Sci 46(5):796–803

    CAS  Google Scholar 

  • St. Aubin DJ, Smith TG, Geraci JR (1990) Seasonal epidermal molt in beluga whales, Delphinapterus leucas. Can J Zool 68:359–367

    Google Scholar 

  • St. Aubin DJ, Deguise S, Richard PR, Smith TG, Geraci JR (2001) Hematology and plasma chemistry as indicators of health and ecological status in beluga whales, Delphinapterus leucas. Arctic 54(3):317–331

    Google Scholar 

  • St. Aubin DJ, Forney KA, Chivers SJ, Scott MD, Danil K, Romano TA, Wells RS, Gulland FMD (2013) Hematological, serum, and plasma chemical constituents in pantropical spotted dolphins (Stenella attenuata) following chase, encirclement, and tagging. Mar Mamm Sci 29(1):14–35

    Google Scholar 

  • Stevens EA, Mezrich JD, Bradfield CA (2009) The aryl hydrocarbon receptor: a perspective on potential roles in the immune system. Immunology 127(3):299–311

    CAS  PubMed  PubMed Central  Google Scholar 

  • Stratakis CA, Chrousos GP (1995) Neuroendocrinology and pathophysiology of the stress system. Ann N Y Acad Sci 771:1–18

    CAS  PubMed  Google Scholar 

  • Thomas JA, Kastelein RA, Awbrey FT (1990) Behaviour and blood catecholamines of captive beluga whales during playbacks of noise from an oil drilling platform. Zoo Biol 9:393–402

    Google Scholar 

  • Thompson LA, Romano TA (2015) Beluga (Delphinapterus leucas) granulocytes and monocytes display variable responses to in vitro pressure exposures. Front Physiol 6:128

    PubMed  PubMed Central  Google Scholar 

  • Thomson CA, Geraci JR (1986) Cortisol, aldosterone, and leucocytes in the stress response of bottlenose dolphins, Tursiops truncatus. Can J Fish Aquat Sci 43(5):1010–1016

    Google Scholar 

  • Trinchieri G (2003) Interleukin-12 and the regulation of innate resistance and adaptive immunity. Nat Rev Immunol 3(2):133–146

    CAS  PubMed  Google Scholar 

  • Tsai M, Chen I, Wang J, Chou S, Li T, Leu M, Ho H, Yang WC (2017) A probe-based qRT-PCR method to profile immunological gene expression in blood of captive beluga whales (Delphinapterus leucas). PeerJ 5:e3840

    PubMed  PubMed Central  Google Scholar 

  • Tyack PL (2008) Implications for marine mammals of large-scale changes in the marine acoustic environment. J Mammal 89(3):549–558

    Google Scholar 

  • Van Dolah FM, Neely MG, McGeorge LE, Balmer BC, Ylitalo GM, Zolman ES, Speakman T, Sinclair C, Kellar NM, Rosel PE, Mullin KD, Schwacke LH (2015) Seasonal variation in the skin transcriptome of common bottlenose dolphins (Tursiops truncatus) from the Northern Gulf of Mexico. PLoS One 10(6):e0130934

    PubMed  PubMed Central  Google Scholar 

  • Van Furth R (1998) Human monocytes and cytokines. Res Immunol 149(7):719–720. https://doi.org/10.1016/S0923-2494(99)80045-5

    Article  PubMed  Google Scholar 

  • Vazzana M, Celi M, Arizza V, Calandra G, Buscaino G, Ferrantelli V, Bracciali C, Sarà G (2017) Noise elicits hematological stress parameters in Mediterranean damselfish (Chromis chromis, perciformes): a mesocosm study. Fish Shellfish Immunol 62:147–152

    CAS  PubMed  Google Scholar 

  • Walsh JE (2008) Climate of the arctic marine environment. Ecol Appl 18(2 Suppl):S3–S22

    PubMed  Google Scholar 

  • Weirup L, Muller S, Ronnenberg K, Rosenberger T, Siebert U, Lehnert K (2013) Immune-relevant and new xenobiotic molecular biomarkers to assess anthropogenic stress in seals. Mar Environ Res 92:43–51

    CAS  PubMed  Google Scholar 

  • Winter JS, Gow KW, Perry YS, Greenberg AH (1990) A stimulatory effect of interleukin-1 on adrenocortical cortisol secretion mediated by prostaglandins. Endocrinology 127(4):1904–1909

    CAS  PubMed  Google Scholar 

  • Zabka TS, Romano TA (2003) Distribution of MHC II (+) cells in skin of the Atlantic bottlenose dolphin (Tursiops truncatus): an initial investigation of dolphin dendritic cells. Anat Rec A Discov Mol Cell Evol Biol 273A(1):636–647

    Google Scholar 

  • Zhu Y, Wang L, Yin Y, Yang E (2017) Systematic analysis of gene expression patterns associated with postmortem interval in human tissues. Sci Rep 7(1):5435

    PubMed  PubMed Central  Google Scholar 

Download references

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.

Funding

Funding for this study is provided by Office of Naval Research, Marine Mammals and Biology Program (ONR Award No: N00014-14-1-0411).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ebru Unal.

Ethics declarations

Conflict of interest

The authors declare that they have no conflicts of interest.

Ethical approval

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.

Additional information

Communicated by U. Siebert.

Reviewed by K. Cammen and an undisclosed expert.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

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

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00227-018-3439-3

Navigation