Journal of Comparative Physiology B

, Volume 185, Issue 5, pp 463–486 | Cite as

Stress physiology in marine mammals: how well do they fit the terrestrial model?

  • Shannon Atkinson
  • Daniel Crocker
  • Dorian Houser
  • Kendall Mashburn
Review

Abstract

Stressors are commonly accepted as the causal factors, either internal or external, that evoke physiological responses to mediate the impact of the stressor. The majority of research on the physiological stress response, and costs incurred to an animal, has focused on terrestrial species. This review presents current knowledge on the physiology of the stress response in a lesser studied group of mammals, the marine mammals. Marine mammals are an artificial or pseudo grouping from a taxonomical perspective, as this group represents several distinct and diverse orders of mammals. However, they all are fully or semi-aquatic animals and have experienced selective pressures that have shaped their physiology in a manner that differs from terrestrial relatives. What these differences are and how they relate to the stress response is an efflorescent topic of study. The identification of the many facets of the stress response is critical to marine mammal management and conservation efforts. Anthropogenic stressors in marine ecosystems, including ocean noise, pollution, and fisheries interactions, are increasing and the dramatic responses of some marine mammals to these stressors have elevated concerns over the impact of human-related activities on a diverse group of animals that are difficult to monitor. This review covers the physiology of the stress response in marine mammals and places it in context of what is known from research on terrestrial mammals, particularly with respect to mediator activity that diverges from generalized terrestrial models. Challenges in conducting research on stress physiology in marine mammals are discussed and ways to overcome these challenges in the future are suggested.

Keywords

Stress response Stress physiology Stressor Hypothalamo-pituitary adrenal axis (HPA axis) Cortisol Corticosterone 

References

  1. Acevedo-Whitehouse K, Rocha-Gosselin A, Gendron D (2010) A novel non-invasive tool for disease surveillance of free-ranging whales and its relevance to conservation programs. Anim Conserv 13:217–225Google Scholar
  2. Adams NR, Atkinson S, Hoskinson RM, Abordi A, Briegel J, Jones M, Sanders MR (1990) Immunization of ovariectomized ewes against progesterone, oestrogen or cortisol to detect effects of adrenal steroids on reproduction. J Reprod Fert 89:477–483Google Scholar
  3. Aguilar A, Borrell A (1990) Patterns of lipid content and stratification in the blubber of fin whales (Balaenoptera physalus). J Mammol 71(4):544–554Google Scholar
  4. Aguilera G, Rabadan-Diehl C (2000) Vasopressinergic regulation of the hypothalamic-pituitary-adrenal axis: implications for stress adaptation. Regul Pept 22 96(1–2):23–29Google Scholar
  5. Aguilera G, Kiss A, Luo X, Akbasak BS (1995) The renin angiotensin system and the stress response. Ann NY Acad Sci 771:173–186PubMedGoogle Scholar
  6. Arnason U, Gullberg A, Janke A, Kullberg M, Lehman N, Petrov EA, Vainda R (2006) Pinniped phylogeny and a new hypothesis for their origin and dispersal. Mol Phylogenet Evol 41(2):345–354PubMedGoogle Scholar
  7. Atkinson S, Adams NR (1988) Adrenal glands alter the concentration of oestradiol-17B and its receptor in the uterus of ovariectomized ewes. J Endocrinol 118:375–380PubMedGoogle Scholar
  8. Atkinson S, Williamson P (1987) Measurement of urinary and plasma estrone sulphate concentrations from pregnant sows. Domest Anim Endocrinol 4(2):133–138PubMedGoogle Scholar
  9. Atkinson S, Becker BL, Johanos C, Pietraszek J, Kuhn BCS (1994) Reproductive morphology and status of female Hawaiian monk seals (Monachus schauinslandi) fatally injured by adult male seals. J Reprod Fert 100:225–230Google Scholar
  10. Atkinson S, Combelles C, Vincent D, Nachtigall P, Pawloski J, Breese M (1999) Monitoring of progesterone in captive female false killer whales, Pseudorca crassidens. Gen Comp Endocrinol 115(3):323–332PubMedGoogle Scholar
  11. Atkinson S, DeMaster DP, Calkins D (2008) Anthropogenic causes of the western Steller sea lion Eumetopias jubatus population decline and their threat to recovery. Mammal Rev 38(1):1–18Google Scholar
  12. Atkinson S, St. Aubin D, Ortiz R (2009) Endocrine Systems. In: Perrin WF, Wursig B, Thewissen JGM (eds) Encyclopedia of Marine Mammals. Academic Press, Burlington, pp 375–383Google Scholar
  13. Aumüller G, Seitz J, Lilja H, Abrahamsson PA, von der Kammer H, Scheit KH (1990) Species- and organ-specificity of secretory proteins derived from human prostate and seminal vesicles. Prostate 17(1):31–40PubMedGoogle Scholar
  14. Ayres KL, Booth RK, Hempelmann JA, Koski KL, Emmons CK, Baird RW, Balcomb-Bartok K, Hanson MB, Ford MJ, Wasser SK (2012) Distinguishing the impacts of inadequate prey and vessel traffic on an endangered killer whale (Orcinus orca) population. PLoS One 7(6):e36842PubMedCentralPubMedGoogle Scholar
  15. Baird RW, Stacey PJ (1989) Observations on the reactions of sea lions, Zalophus californianus and Eumetopias jubatus to killer whales, Orcinus orca: evidence of “prey” having a “search image” for predators. Can Field Nat 103(3):426–428Google Scholar
  16. Barrett T, Sahoo P, Jepson PD (2003) Seal distemper outbreak 2002. Microbiol Today 30:162–164Google Scholar
  17. Bechshøft TO, Sonne C, Dietz R, Born EW, Muir DCG, Letcher RJ, Novak MA, Henchey E, Meyer JS, Jenssen BM, Villager GD (2012) Association between complex OHC mixtures and thyroid and cortisol hormone levels in East Greenland polar bears. Environ Res 116:26–35PubMedGoogle Scholar
  18. Bejder L, Samuels A, Whitehead H, Gales N, Mann J, Connor R, Heithaus M, Watson-Capps J, Flaherty C, Krutzen M (2006) Decline in relative abundance of bottlenose dolphins exposed to long-term disturbance. Conserv Biol 20(6):1791–1798PubMedGoogle Scholar
  19. Bennett KA, Moss SEW, Pomeroy P, Speakman JR, Fedak MA (2012) Effects of handling regime and sex on changes in cortisol, thyroid hormones and body mass in fasting grey seal pups. Comp Biochem Physiol A 161:69–76Google Scholar
  20. Berta A, Wyss AR (1994) Pinniped phylogeny. Proc San Diego Soc Nat Hist 29:33–56Google Scholar
  21. Bester MN (1975) The functional morphology of the kidney of the Cape fur seal, Arctocephalus pusillus (Schreber). Modoqua Ser 4:69–92Google Scholar
  22. Biancani B, Da Dalt L, Lacave G, Romagnoli S, Gabai G (2009) Measuring fecal progestogens as a tool to monitor reproductive activity in captive female bottlenose dolphins (Tursiops truncatus). Theriogenology 72:1282–1292PubMedGoogle Scholar
  23. Bodley KB, Mercer JR, Bryden MM (1999) Rate of passage of digesta through the alimentary tract of the New Zealand fur seal (Arctocephalus forsteri) and the Australian sea lion (Neophoca cinerea) (Carnivora: Otariidae). Aust J Zool 47:193–198Google Scholar
  24. Boonstra R, Hik D, Singleton GR, Tinnikov A (1998) The impact of predator-induced stress on the snowshoe hare cycle. Ecol Monogr 79(5):371–394Google Scholar
  25. Bowen WD, Ellis SL, Iverson SJ, Boness DJ (2003) Maternal and newborn life-history traits during periods of contrasting population trends: implications for explaining the decline of harbour seals, Phoca vitulina, on Sable Island. J Zool Lond 261:155–163Google Scholar
  26. Brouwer A, Reijnders PJH, Koeman JH (1989) Polychlorinated biophenyl (PCB)-contaminated fish induces vitamin A and thyroid hormone deficiency in the common seal (Phoca vitulina). Aquat Toxicol 15:99–106Google Scholar
  27. Brown JL, Lehnhardt J (1995) Serum and urinary hormone during pregnancy and the peri-and postpartum period in an Asian elephant (Elephas, maximus). Zoo Biol 14(6):555–564Google Scholar
  28. Burgess E, Brown JL, Lanyon JM (2013) Sex, scarring and stress: understanding seasonal costs in a cryptic marine mammal. Conserv Physiol. doi:10.1093/conphys/cot014 Google Scholar
  29. Cabanac AJ, Folkow LP, Blix AS (1989) Volume capacity and contraction control of the seal spleen. J Appl Physiol 82(6):1989–1994Google Scholar
  30. Calkins DG, Atkinson S, Mellish J-A, Waite JN, Carpenter JR (2013) The pollock paradox: juvenile Steller sea lions experience rapid growth on pollock diets in fall and spring. J Exp Mar Biol Ecol 44:55–61Google Scholar
  31. Campagna C, Le Boeuf BJ, Cappozzo HL (1988) Pup abduction and infanticide in southern sea lions. Behaviour 107(1–2):44–60 (17) Google Scholar
  32. Cannon WB (1932) The wisdom of the body. W.W. Norton and Company, Inc., New YorkGoogle Scholar
  33. Cannon WB, Lissak K (1939) Evidence for adrenaline in adrenergic neurons. Am J Physiol 125:138–140Google Scholar
  34. Carrasco GA, Van de Kar LD (2003) Neuroendocrine pharmacology of stress. Eur J Parmacol 463(1–3):235–272Google Scholar
  35. Castellini MA, Costa DP, Huntley AC (1987) Fatty acid metabolism in fasting northern elephant seal pups. J Comp Physiol B 157:445–449PubMedGoogle Scholar
  36. Champagne CD, Houser DS, Costa DP, Crocker DE (2012) The effects of handling and anesthetic agents on the stress response and carbohydrate metabolism in northern elephant seals. PLoS One 7(5):e38442PubMedCentralPubMedGoogle Scholar
  37. Chatterton RTJ, Vogelsong KM, Lu Y, Ellman AB, Hudgens GA (1996) Salivary alpha-amylase as a measure of endogenous adrenergic activity. Clin Physiol 16:433–448PubMedGoogle Scholar
  38. Chiba I, Sakakibara A, Goto Y, Isono T, Yamamoto Y, Iwata H, Tanabe S, Shimazaki K, Akahori F, Kazusaka A, Fujita S (2001) Negative correlation between plasma thyroid hormone levels and chlorinated hydrocarbon levels accumulated in seals from the coast of Hokkaido, Japan. Environ Toxicol Chem 20(5):1092–1097PubMedGoogle Scholar
  39. Chow BA, Hamilton J, Alsom D, Cattet MR, Stenhouse G, Vijayan MM (2010) Grizzly bear corticosteroid binding globulin: cloning and serum protein expression. Gen Comp Endocrinol 167(2):317–325PubMedGoogle Scholar
  40. Clamage DM, Sanford CS, Vander AJ, Mouw DR (1976) Effects of psychosocial stimuli on plasma renin activity in rats. Am J Physiol 231:1290–1294PubMedGoogle Scholar
  41. Clark CW, Ellison WT, Southall BL, Hatch L, Van Parijs SM, Frankel A, Ponirakis D (2009) Acoustic masking in marine ecosystems: intuitions, analysis, and implication. Mar Ecol Progr Ser 395:201–222Google Scholar
  42. Cockrem JF (2013) Individual variation in glucocorticoid responses in animals. Gen Comp Endocrinol 181:45–58PubMedGoogle Scholar
  43. Cooper DS, Ladenson PW (2011) The Thyroid Gland. In: Gardner DG, Shoback D (eds) Greenspan’s basic and clinical endocrinology, 9th edn. McGraw-Hill Medical, McGraw-Hill Companies, Inc., New York, pp 163–226Google Scholar
  44. Costa DP (1982) Energy, nitrogen, and electrolyte flux and sea water drinking in the sea otter Enhydra lutris. Physiol Zool 55(1):35–44Google Scholar
  45. Costa DE, Gedemke J, Webb PM, Houser DS, Blackwell SB (2003) The effect of low frequency sound source (acoustic thermometry of the ocean climate) on the diving behavior of juvenile northern elephant seals, Mirounga augustirostris. J Acoust Soc Am 113(2):3373–3404Google Scholar
  46. Cox TM, Ragen TJ, Read AJ, Vos E, Baird RW, Balcomb K, Barlow J, Caldwell J, Cranford T, Crum L, Amico AD, Spain GD, Fernandez A, Finneran J, Gentry R, Gerth W, Gulland F, Hildebrand J, Houser D, Hullar T, Jepson PD, Ketten D, MacLeod CD, Miller P, Moore S, Mountain DC, Palka D, Ponganis P, Rommel S, Rowles T, Taylor B, Tyack P, Wartzok D, Gisiner R, Mead J, Benner L (2006) Understanding the impacts of anthropogenic sound on beaked whales. J Cetacean Res Manage 7(3):177–187Google Scholar
  47. Creel S, Creel NM, Mills MGL, Monfort SL (1997) Rank and reproduction in cooperatively breeding African wild dogs: behavioral and endocrine correlates. Behav Ecol 8(3):8298–8506Google Scholar
  48. Creel S, Fox JE, Hardy A, Sands J, Garrott B, Peterson RO (2002) Snowmobile activity and glucocorticoid stress responsess in wolves and elk. Conserv Biol 16(3):809–814Google Scholar
  49. Crocker DE, Webb PM, Costa DP, Le Boeuf BJ (1998) Protein catabolism and renal function in lactating northern elephant seals. Physiol Zool 71:485–491PubMedGoogle Scholar
  50. Crocker DE, Costa DP, Le Boeur BJ, Webb PM, Houser DS (2006) Impact of El Nino on the foraging behaviour of female northern elephant seals. Marine Ecol Prog Ser 309:1–10Google Scholar
  51. Crocker DE, Ortiz RM, Houser DS, Webb PM, Costa DP (2012) Hormone and metabolite changes associated with extended breeding fasts in male northern elephant seals (Mirounga angustirostris). Comp Biochem Physiol A 161:388–394Google Scholar
  52. Dailey MD (2001) Parasitic diseases. In: Dierauf LA, Gulland FMD (eds) CRC Handbook of Marine Mammal Medicine. CRC Press, New York, pp 357–379Google Scholar
  53. Danforth E Jr, Burger A (1984) The role of thyroid hormones in the control of energy expenditure. Clin Endocrinol Metab 13(3):581–595PubMedGoogle Scholar
  54. de Kloet ER, Oitzl MS, Joels M (1993) Functional implications of brain corticosteroid receptor diversity. Cell Mol Neurobiol 13:433–455PubMedGoogle Scholar
  55. Delehanty B, Boonstra R (2012) The benefits of baseline glucocorticoid measurements: maximal cortisol production under baseline conditions revealed in male Richardson’s ground squirrels (Urocitellus richardsonii). Gen Comp Endocrinol 178:470–476PubMedGoogle Scholar
  56. Demers LM, Spencer CA (2003) Laboratory medicine practice guidelines: laboratory support for the diagnosis and monitoring of thyroid disease. Clin Endocrinol 58:138–140Google Scholar
  57. Desantis LM, Delehanty B, Weir JT, Boonstra R (2013) Mediating free glucocorticoid levels in the blood of vertebrates: are corticosteroid-binding proteins always necessary? Funct Ecol 27:107–119Google Scholar
  58. Desportes G, Buholzer L, Anderson-Hansen K, Blanchet M-A, Acquarone M, Shephard G, Brando S, Vossen A, Siebert U (2007) Decrease stress; train your animals: the effect of handling methods on cortisol levels in harbor porpoises (Phocoena phocoena) under human care. Aqua Mammals 33(3):286–292Google Scholar
  59. Dhillo WS, Kong WM, Le Roux CW, Alaghband-Zadeh J, Jones J, Carter G, Mendoza N, Meeran K, O’Shea D (2002) Cortisol-binding globulin is important in the interpretation of dynamic tests of the hypothalami–pituitary–adrenal axis. Eur J Endorcinol 146(2):231–235Google Scholar
  60. Di Poi C, Atkinson S, Hoover-Miller A, Blundell G (2015) Maternal buffering of stress response in free-ranging Pacific harbor seal pups in Alaska. Mar Mammal Sci. doi:10.1111/mms.12217
  61. Dimsdale JE, Ziegler M, Mills P, Delehanty SG, Berry C (1990) Effects of salt, race, and hypertension on reactivity to stressors. Hypertension 16:573–580PubMedGoogle Scholar
  62. du Dot TJ, Rosen DAS, Trites AW (2009) Energy reallocation during and after periods of nutritional stress in Steller sea lions: low-quality diet reduces capacity for physiological adjustments. Physiol Biochem Zool 82(5):516–530Google Scholar
  63. Dunn JL, Buck JD, Robeck TR (2001) Bacterial diseases of cetaceans and pinnipeds. In: Dierauf LA, Gulland FMD (eds) CRC Handbook of Marine Mammal Medicine, Part 2. CRC Press, New York, pp 309–335Google Scholar
  64. Dushaw BD, Worcester PF, Cornuelle BD, Howe BM (1993) On equations for the speed of sound in seawater. J Acoustic Soc Am 93(1):255–275Google Scholar
  65. Dvorakova MC, Kummer W (2005) Immunohistochemical evidence for species-specific coexistence of catecholamines, serotonin, acetylcholine and nitric oxide in glomus cells of rat and guinea pig aortic bodies. Ann Anat 187:323–331PubMedGoogle Scholar
  66. Eales JG (1985) The peripheral metabolism of thyroid hormones and regulation of thyroidal status in poikilotherms. Can J Zool 63:1217–1231Google Scholar
  67. Eales JG (1988) The influence of nutritional state on thyroid function in various vertebrates. Am Zool 28:351–362Google Scholar
  68. Ehrhardt RA, Slepetis RM, Siegal-Willott J, Van Amburgh ME, Bell AW, Boisclair YR (2000) Development of a specific radioimmunoassay to measure physiological changes of circulating leptin in cattle and sheep. J Endocrinol 166:519–928PubMedGoogle Scholar
  69. Engelhard GH, Brasseur SMJM, Hall AJ, Burton HR, Reijnders PJH (2002) Adrenocortical responsiveness in southern elephant seal mothers and pups during lactation and the effect of scientific handling. J Comp Physiol B 172:315–328PubMedGoogle Scholar
  70. Engelhardt FR, Ferguson JM (1980) Adaptive hormone changes in harp seals, Phoca groenlandica, and gray seals, Halichoerus grypus, during the postnatal period. Gen Comp Endocrinol 40(4):434–445PubMedGoogle Scholar
  71. Ensminger DC, Somo DA, Houser DS, Crocker DE (2014) Metabolic responses to adrenocorticotropic hormone (ACTH) vary with life-history stage in adult male northern elephant seals. Gen Comp Endocrinol 204:150–157PubMedGoogle Scholar
  72. Everly GS, Lating JM (2013) A clinical guide to the treatment of the human stress response. Springer Science and Business Media, New YorkGoogle Scholar
  73. Fair PA, Becker PR (2000) Review of stress in marine mammals. J Aquat Ecosyst Stress Recovery 7(4):335–354Google Scholar
  74. Fair PA, Montie E, Balthis L, Reif JS, Bossart GD (2011) Influences of biological variables and geographic location on circulating concentrations of thyroid hormones in wild bottlenose dolphins (Tursiops truncatus). Gen Comp Endocrinol 174:184–194PubMedGoogle Scholar
  75. 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 206:203–212PubMedGoogle Scholar
  76. Fernández A, Edwards J, Martín V, Rodríguez F, de los Monteros AE, Herráez P, Castro P, Jaber JR, Arbelo M (2005) Gas and fat embolic syndrome involving a mass stranding of beaked whales (family Ziphiidae) exposed to anthropogenic sonar signals. J Vet Pathol 42:446–457Google Scholar
  77. Fleshner M, Deak T, Spencer RL, Laudenslager ML, Watkins LR, Maier SF (1995) A long-term increase in basal levels of corticosterone and a decrease in corticosteroid-binding globulin after acute stressor exposure. Endocrinology 136(12):5336–5342PubMedGoogle Scholar
  78. Fossi MC, Marsili L, Neri G, Natoli A, Politi E, Panigada S (2003) The use of non-lethal tool for evaluating toxicological hazard of organochlorine contaminants in Mediterranean cetaceans: new data 10 years after the first paper published in MPB. Marine Pollut Bull 46:972–982Google Scholar
  79. Gardiner KJ, Hall AJ (1997) Diel and annual variation in plasma cortisol concentrations among wild and captive harbor seals (Phoca vitulina). Can J Zool 75:1773–1780Google Scholar
  80. Gar-Elnabi MEM, Taha RM, Olivier MAA, Faraha M, Bushara YM (2013) Assessment of human thyroid function using radioimmunoassay and enzyme-linked immunosorbent assay. J Exp Clin Med 30:317–321Google Scholar
  81. Gatesy J, Hayashi C, Cronin MA, Arctander P (1996) Evidence from milk casein genes that cetaceans are close relatives of hippopotamid artiodactyls. Mol Biol Evol 13:954–963PubMedGoogle Scholar
  82. Geraci JR, Harwood J, Lounsbury VJ (1999) Marine mammal die-offs: causes, investigations, and issues. In: Twiss JR Jr, Reeves RR (eds) Conservation management of marine mammals. Smithsonian Institution Press, Washington DC, pp 367–395Google Scholar
  83. Gerlinsky CD, Trites AW, Rosen DA (2014) Steller sea lion (Eumetopias jubatus) have greater blood volumes, higher diving metabolic rates and longer aerobic dive limit when nutritionally stressed. J Exp Biol 217:769–778PubMedGoogle Scholar
  84. Goldstein DS (1995) Stress, catecholamines and cardiovascular disease. Oxford University Press, New YorkGoogle Scholar
  85. Goldstein DR (2003) Catecholamines and stress. Endocr Reg 37:69–80Google Scholar
  86. Goodman-Lowe GD, Atkinson S, Carpenter JR (1997) Initial defecation time and rate of passage of digesta in adult Hawaiian monk seals, Monachus schauinslandi. Can J Zool 75:433–438Google Scholar
  87. Gow R, Thomson S, Rieder M, Van Uum S, Koren G (2010) An assessment of cortisol analysis in hair and its clinical implications. Forensic Sci Int 196:32–37PubMedGoogle Scholar
  88. Groeschel M, Braam B (2011) Connecting chronic and recurrent stress to vascular dysfunction: no relaxed role for the renin-angiotensin system. Am J Physiol Renal Physiol 300:F1–F10PubMedGoogle Scholar
  89. Guinet C, Servera N, Mangin S, Georges J-Y, Lacroix A (2004) Change in plasma cortisol and metabolites during the attendance period ashore in fasting lactating subantarctic fur seals. Comp Biochem Physiol A 137:523–531Google Scholar
  90. Gulland FMD, Haulena M, Lowenstine LJ, Munro C, Graham PA, Bauman J, Harvey J (1999) Adrenal function in wild and rehabilitated Pacific harbor seals (Phoca vitulina richardii) and in seals with phocine herpesvirus-associated adrenal necrosis. Mar Mammal Sci 15(3):810–827Google Scholar
  91. Guyton AC, Hall JE (2000) Textbook of Medical Physiology, 10th edn. WB.Saunders Company, PhiladelphiaGoogle Scholar
  92. Hall JE (1986) Control of sodium excretion by angiotensin II: intrarenal mechanisms and blood pressure regulation. Am J Physiol 250:R960–R972PubMedGoogle Scholar
  93. Hallegraeff GM (1993) A review of harmful algal blooms and their apparent global increase. Phycologia 32(2):79–99Google Scholar
  94. Hance AJ, Robin ED, Halter JB, Lewiston N, Robin DA, Cornell L, Caligiuri M, Theodore J (1982) Hormonal changes and enforced diving in the harbor seal Phoca vitulina. II. Plasma catecholamines. Am J Physiol Reg I 242(5):R528–R532Google Scholar
  95. Harcourt RG, Turner E, Hall A, Waas JR, Hindell M (2010) Effects of capture stress on free-ranging, reproductively active male Weddle seals. J Comp Physiol A 196:147–154Google Scholar
  96. Harvell CD, Mitchell CE, Ward JR, Altizer S, Dobson AP, Ostfeld RS, Samuel MD (2002) Climate warming and disease risks for terrestrial and marine biota. Science 296:2158–2162PubMedGoogle Scholar
  97. Helle E, Osson M, Jensen S (1976) PCB levels correlated with pathological changes in seal uteri. Ambio 5:261–263Google Scholar
  98. Hildebrand JA (2005) Impacts of anthropogenic sound. In: Reynolds JE et al (eds) Marine mammal research: conservation beyond crisis. The Johns Hopkins University Press, Baltimore, pp 101–124Google Scholar
  99. Hildebrand JA (2009) Anthropogenic and natural sources of ambient noise in the ocean. Mar Ecol Prog Ser 395:5–20Google Scholar
  100. Hochachka PW, Liggins GC, Guyton GP, Schneider RC, Stanek KS, Hurford WE, Creasy RK, Zapol DG, Zapol WM (1995) Hormonal regulatory adjustments during voluntary diving in Weddell seals. Comp Biochem Physiol B 112(2):361–375PubMedGoogle Scholar
  101. Hogg CJ, Vickers ER, Rogers TL (2005) Determination of testosterone in saliva and blow of bottlenose dolphins (Tursiops truncatus) using liquid chromatography–mass spectrometry. J Chromatogr B 814:339–346Google Scholar
  102. Hogg CJ, Rogers TL, Shorter A, Barton K, Miller PJO, Nowacek D (2009) Determination of steroid hormones in whale blow: it is possible. Mar Mammal Sci 25(3):605–618Google Scholar
  103. Holt MM, Noren DP, Veirs V, Emmons CK, Veirs S (2008) Speaking up: killer whales (Orcinus orca) increase their call amplitude in response to vessel noise. J Acoust Soc Am 125(1):EL27–EL32Google Scholar
  104. Houser DS, Crocker DE, Webb PM, Costa DP (2001) Renal function in suckling and fasting pups of the northern elephant seal. Comp Biochem Physiol A 129:405–415Google Scholar
  105. Houser DS, Champagne CD, Crocker DE (2007) Lipolysis and glycerol gluconeogenesis in simultaneously fasting and lactating northern elephant seals. Am J Physiol Integr Comp Physiol 293:R2376–R2381Google Scholar
  106. Houser DS, Yeates LC, Crocker DE (2011) Cold stress induces an adrenocortical response in bottlenose dolphins (Tursiops truncatus). J Zoo Wildlife Med 42(4):565–571Google Scholar
  107. Hunt KE, Rolland RM, Kraus SD, Wasser SK (2006) Analysis of fecal glucocorticoids in the North Atlantic right whale (Eubalaena glacialis). Gen Comp Endocrinol 148:260–272PubMedGoogle Scholar
  108. Hunt KE, Moore MJ, Rolland RM, Kellar NM, Hall AJ, Kershaw J, Raverty SA, Davis CE, Yeates LC, Fauquler DA, Rowles TK, Kraus S (2013) Overcoming the challenges of studying conservation physiology in large whales: a review of available methods. Conserv Physiol. doi:10.1093/conphys/cot006 Google Scholar
  109. Hurford WE, Hochachka PW, Schneider RC, Guyton GP, Stanek KS, Zapol DG, Liggins GC, Zapol WM (1996) Splenic contraction, catecholamine release, and blood volume redistribution during diving in the Weddell seal. J Appl Physiol 80(1):298–306PubMedGoogle Scholar
  110. Isanhart JP, McNabb FMA, Smith PN (2005) Effects of perchlorate exposure on resting metabolism, peak metabolism, and thyroid function in the prairie vole (Microtus ochrogaster). Environ Toxicol Chem 24(3):678–684PubMedGoogle Scholar
  111. Jepson PD, Arbelo M, Deaville R, Patterson IAR, Castro P, Baker JR, Degollada E, Ross HM, Herráez P, Pocknell AM, Rodriguez E, Howie FE, Espinosa A, Reid RJ, Jaber JR, MartinV Cunningham AA, Fernandez A (2003) Gas-bubble lesions in stranded cetaceans: was sonar responsible for a spate of whale deaths after an Atlantic military exercise? Nature 425:575–576PubMedGoogle Scholar
  112. Kanatous SB, Davis RW, Watson R, Polasesk L, Williams TM, Mathieu-Costello O (2002) Aerobic capacities in the skeletal muscles of Weddell seals: key to longer dive durations. J Exp Biol 205:3601–3608PubMedGoogle Scholar
  113. Kannan K, Blankenship AL, Jones PD, Giesy JP (2000) Toxicity reference values for the toxic efficts of polychlorinated biphenyls to aquatic mammals. Hum Ecol Risk Assess 6(1):181–201Google Scholar
  114. Kastelein RA, Staal C, Wiepkema PR (2003) Food consumption, food passage time, and body measurements of captive Atlantic bottlenose dolphins (Tursiops truncatus). Aqua Mamm 29(1):53–66Google Scholar
  115. Kawauchi H, Sasaki T (1978) Isolation and primary structure of adrenocorticotropin from several species of whale. Int J Pept Prot Res 12(5):318–324Google Scholar
  116. Keech AL, Rosen DAS, Booth RK, Trites AW, Wasser SK (2010) Fecal triiodothyronine and thyroxine concentrations change in response to thyroid stimulation in Steller sea lions (Eumetopias jubatus). Gen Comp Endocrinol 166:180–185PubMedGoogle Scholar
  117. Kellar NM, Trego ML, Marks CI, Dizon AE (2006) Determining pregnancy from blubber in three species of delphinids. Mar Mammal Sci 22(1):1–16Google Scholar
  118. Kellar NM, Trego ML, Marks CI, Chivers SJ, Danil K, Archer FI (2009) Blubber testosterone: a potential marker of male reproductive status in short-beaked common dolphins. Mar Mammal Sci 25(3):507–522Google Scholar
  119. Kelso EJ, Champagne CD, Tift MS, Houser DS, Crocker DE (2012) Sex differences in fuel use and metabolism during development in fasting juvenile northern elephant seals. J Exp Bio 215:2637–2645Google Scholar
  120. Kennedy-Stoskopf S (2001) Viral diseases. In: Dierauf LA, Gulland FMD (eds) CRC handbook of marine mammal medicine, Part 2. CRC Press, New York, pp 285–307Google Scholar
  121. Keogh MJ, Atkinson S (2015) Endocrine and immunological responses to adrenocorticotrophic hormone (ACTH) administration in juvenile harbor seals (Phoca vitulina) during winter and spring. Comp Biochem Phys A (in press)Google Scholar
  122. Keogh MJ, Atkinson S, Maniscalco JM (2013) Body condition and endocrine profiles of Steller sea lion (Eumetopias jubatus) pups during the early postnatal period. Gen Comp Endocrinol 184:42–50PubMedGoogle Scholar
  123. Kielhorn CE, Dillaman RM, Kinsey ST, McLellan WA, Gay DM, Dearolf JL, Pabst DA (2013) Locomotor muscle profiles of a deep (Kogia breviceps) versus shallow (Tursiops truncatus) diving cetaceans. J Morphol 274:663–675PubMedGoogle Scholar
  124. Kirk, GW (2014) The Invention of the “Stressed Animal” and the Development of a Science of Animal Welfare 1947–1986 In: Cantor D, Ramsden E (eds) Stress, Shock and Adaptation in the 20th Century. University of Rochester Press, New YorkGoogle Scholar
  125. Kirkegaard M, Sonne C, Dietz R, Letcher RJ, Jensen AL, Hansen SS, Jenssen BM, Grandjean P (2011) Alterations in thyroid hormone status in Greenland sled dogs exposed to whale blubber contaminated with organohalogen compounds. Ecotox Environ Saf 74:157–163Google Scholar
  126. Kiyota M, Okamura H (2005) Harassment, abduction and mortality of pups by nonterritorial male northern fur seals. J Mammal 86(6):1227–1236Google Scholar
  127. Kjeld M (2001) Concentrations of electrolytes, hormones, and other constituents in fresh postmortem blood and urine of fin whales (Balaenoptera physalus). Can J Zool 79:438–446Google Scholar
  128. Kjer KM, Honeycutt RL (2007) Site specific rates of mitochondrial genomes and the phylogeny of Eutheria. BMC Evol Biol 7:8PubMedCentralPubMedGoogle Scholar
  129. Koolhaas JM, Bartolomucci A, Buwalda B, de Boer SF, Flügge G, Korte SM, Meerlo P, Murison R, Olivier B, Palanza P, Richter-Levin G, Sgoifo A, Steimer T, Stiedl O, van Dijk G, Wöhr M, Fuchs E (2011) Stress revisited: a critical evaluation of the stress concept. Neurosci Biobehav Rev 35:1291–1301PubMedGoogle Scholar
  130. Koopman HN, Iverson SJ, Gaskin DE (1996) Stratification and age-related differences in blubber fatty acids of the male harbor porpoise (Phocoena phocoena). J Comp Physiol B 165:628–639PubMedGoogle Scholar
  131. Kooyman GL, Sinnett EE (1982) Pulmonary shunts in harbor seals and sea lions during simulated dives to depth. Physiol Zool 55(1):105–111Google Scholar
  132. Koren L, Whiteside D, Fahlman A, Ruckstuhl K, Kutz S, Checkley S, Dumond M, Wynne-Edwards K (2012) Cortisol and corticosterone independence in cortisol-dominant wildlife. Gen Comp Endocrinol 177:113–119PubMedGoogle Scholar
  133. Korte SM, Prins J, Vinkers CH, Olivier B (2009) On the origin of allostasis and stress induced pathology in farm animals: celebrating Darwin’s legacy. Vet J 182(3):378–383PubMedGoogle Scholar
  134. Kretzmann MB, Gemmell NJ, Meyer A (2001) Microsatellite analysis of population structure in the endangered Hawaiian monk seal. Conserv Biol 15(2):457–466Google Scholar
  135. Labrada-Martagón V, Zenteno-Savín T, Mangel M (2014) Linking physiological approaches to marine vertebrate conservation: using sex steroid hormone determinations in demographic assessments. Conserv Physiol. doi:10.1093/conphys/cot035 Google Scholar
  136. Laidre KL, Stirling I, Lowry LF, Wiig O, Heide-Jorgensen MP, Ferguson SH (2008) Quantifying the sensitivity of arctic marine mammals to climate-induced habitat change. Ecol Appl 18(2):S97–S125PubMedGoogle Scholar
  137. Laidre KL, Heide-Jorgensen MP, Stern H, Richard P (2012) Unusual narwhal sea ice entrapment and delayed autumn freeze-up. Polar Biol 35:149–154Google Scholar
  138. Landys MM, Ramenofsky M, Wingfield JC (2006) Actions of glucocorticoids at a seasonal baseline as compared to stress-related levels in the regulation of periodic life processes. Gen Comp Endocrinol 148:132–149PubMedGoogle Scholar
  139. Langtimm CA, Beck CA (2003) Lower survival probabilities for adult Florida manatees in years with intense coastal storms. Ecol App 13(1):257–268Google Scholar
  140. Larkin ILV, Fowler VF, Reep RL (2007) Digesta passage rates in the Florida manatee (Trichechus manatus latirostris). Zoo Biol 26:503–515PubMedGoogle Scholar
  141. Lasley BL, Kirkpatrick JF (1991) Monitoring ovarian function in captive and free-ranging wildlife by means of urinary and fecal steroids. Wildlife Med 22(1):23–31Google Scholar
  142. Le Boeuf BJ, Mesnick S (1990) Sexual behavior of male northern elephant seals: I.Lethal injuries to adult females. Behavior 116(1–2):143–162Google Scholar
  143. Le Boeuf BJ, Reiter J (1991) Biological effects associated with El Nino Southern Oscillation, 1982–83, on northern elephant seals breeding at Ano Nuevo, California. In: Trillmich F, Ono KA (eds) Pinnipeds and El Niño. Springer, Berlin Heidelberg, pp 206–218Google Scholar
  144. Leob WF (2000) A mouse is not a man is not a dog 2000 or species specificity in clinical chemistry. Rev Med Vet 151(1):619–622Google Scholar
  145. Levine S, Ursine H (1991) What is Stress? In: Brown MR, Koob GF, Rivier C (eds) Stress: neurobiology and neuroendocrinology. Marcel Decker, New YorkGoogle Scholar
  146. Levy BH, Tasker JG (2012) Synaptic regulation of the hypothalamic-pituitary-adrenal axis and its modulation by glucocorticoids and stress. Front Cell Neurosci 6:24PubMedCentralPubMedGoogle Scholar
  147. Lewis EL (2009) The practical salinity scale of 1978 and its antecedents. Mar Geodesy 5(4):350–357Google Scholar
  148. Li XS, Li S, Wynveen P, Mork K, Kellermann G (2014) Development and validation of a specific and sensitive LC-MS/MS method for quantification of urinary catecholamines and application in biological variation studies. Anal Bioanal Chem 406(28):7287–7297PubMedGoogle Scholar
  149. Lidgard DC, Boness DJ, Bowen WD, McMillan JI (2008) The implications of stress on male mating behaviour and success in a sexually dimorphic polygynous mammal, the grey seal. Horm Behav 53:241–248PubMedGoogle Scholar
  150. Limberger D (1990) El Niño’S effect on South American pinniped species. El Sev Oceanogr Ser 52:417–432Google Scholar
  151. Lusseau D, Bejder L (2007) The Long-term consequences of short-term responses to disturbance experiences from whalewatching impact assessment. Int J Comp Psychol 20:228–236Google Scholar
  152. Maluf NSR (1989) Renal anatomy of the manatee, Trichechus manatus (Linnaeus). Am J Anat 184:269–286PubMedGoogle Scholar
  153. Maniscalco JM, Calkins DG, Parker P, Atkinson S (2008) Causes and extent of natural mortality among Steller sea lion (Eumetopias jubatus) pups. Aquat Mammals 34:277–287Google Scholar
  154. Mansour AAH, McKay DW, Lien J, Orr JC, Banoub JH, Oien N, Stenson G (2002) Determination of pregnancy status from blubber samples in minke whales (Balaenoptera acutorostrata) with age and reproductive activity. Mar Mammal Sci 18:112–120Google Scholar
  155. Martensson J (1986) The effect of fasting on leukocyte and plasma glutathione and sulfur amino acid concentrations. Metabolism 35(2):118–121PubMedGoogle Scholar
  156. Mashburn KL, Atkinson S (2004) Evaluation of adrenal function in serum and feces of Steller sea lions (Eumetopias jubatus): influences of molt, gender, sample storage, and age on glucocorticoid metabolism. Gen Comp Endocrinol 136(3):371–381PubMedGoogle Scholar
  157. Mashburn KL, Atkinson S (2007) Seasonal and predator influences on adrenal function in adult Steller sea lions: gender matters. Gen Comp Endocrinol 150:246–252PubMedGoogle Scholar
  158. Mashburn KL, Atkinson S (2008) Variability in leptin and adrenal response in juvenile Steller sea lions (Eumetopias jubatus) to adrenocorticotropic hormone (ACTH) in different seasons. Gen Comp Endocrinol 155:352–358PubMedGoogle Scholar
  159. Matkin CO, Barrett-Lennard L, Ellis G (2002) Killer whales and predation on Steller sea lions. In: Demaster DP, Atkinson S (eds) Stelller sea lion decline: Is it food II, vol AK-SG-02-02. University of Alaska Sea Grant College Program, 80 Fairbanks, pp 61–66Google Scholar
  160. McEwen BS (1999) Stress and hippocampal plasticity. Annu Rev Neurosci 22:105–122PubMedGoogle Scholar
  161. McEwen BS (2000) Allostasis and allostatic load: implications for neuropsychopharmacology. Neuropsychopharmacology 22(2):108–124PubMedGoogle Scholar
  162. McEwen BS (2012) Brain on stress: how the social environment gets under the skin. Proc Nat Acad Sci 109(2):17180–17185PubMedCentralPubMedGoogle Scholar
  163. McEwen BS, Wingfield JC (2003) The concept of allostasis in biology and biomedicine. Horm Behavior 43(1):2–15Google Scholar
  164. McEwen BS, Wingfield JC (2007) Allostasis and allostatic load. In Fink G (ed) Encyclopedia of Stress. Academic Press, New York, pp 135–141Google Scholar
  165. McEwen BS, Wingfield JC (2010) What is in a name? Integrating homeostasis, allostasis and stress. Horm Behav 57:105–111PubMedCentralPubMedGoogle Scholar
  166. Melin SR, DeLong RL, Siniff DB (2008) The effects of El Nino on the foraging behavior of lactating California sea lions (Zalophus californianus californianus) during the nonbreeding season. Can J Zool 86(3):192–206Google Scholar
  167. Mellish JE, Calkins DG, Christen DR, Horning M, Rea LD, Atkinson S (2006) Temporary captivity as a research tool: comprehensive study of wild pinnipeds under controlled conditions. Aquat Mammal 32(1):25–65Google Scholar
  168. Meyer JS, Novak MA (2012) Hair cortisol: a novel biomarker of hypothalamic-pituitary-adrenocortical activity. Endocrinology 153(9):4120–4127PubMedCentralPubMedGoogle Scholar
  169. Miksis-Olds JL, Donaghay PL, Miller JH, Tyack PL, Nystuen JA (2007) Noise level correlates with manatee use of foraging habitats. J Acoust SocAm 121(5):3011–3020Google Scholar
  170. Minton JE (1994) Function of the hypothalamic-pituitary-adrenal axis and the sympathetic nervous system in models of acute stress in domestic farm animals. J Anim Sci 72:1891–1898PubMedGoogle Scholar
  171. Monclus R, Rodel HG, von Holst D (2006) Fox odour increases vigilance in European rabbits: a study under semi-natural conditions. Ethology 112(12):1186–1193Google Scholar
  172. Monnett C, Gleason JS (2006) Observations of mortality associated with extended open-water swimming by polar bears in the Alaskan Beaufort Sea. Polar Biol 29:681–687Google Scholar
  173. Murdaugh HV, Schmidt-Nielsen B, Wood JW, Mitchell WL (1961) Cessation of renal function during diving in the trained seal (Phoca vitulina). J Cell Compar Physl 58(3):261–265Google Scholar
  174. Myers MJ, Rea LD, Atkinson S (2006) The effect of age, season and geographic region on thyroid hormones in Steller sea lions (Eumetopias jubatus). Comp Biochem Physiol A 145:90–98Google Scholar
  175. Myers MJ, Litz B, Atkinson S (2010) The effects of age, season and geographic region on circulating serum cortisol concentrations in threatened and endangered Steller sea lions (Eumetopias jubatus). Gen Comp Endocrinol 165:72–77PubMedGoogle Scholar
  176. Mӧstl E, Palme R (2002) Hormones as indicators of stress. Domest Anim Endocrin 23:67–74Google Scholar
  177. National Academy of Sciences (NAS) (2005) Marine mammal populations and ocean noise. Determining when noise causes biologically significant effects. National Academies Press,Washington, DCGoogle Scholar
  178. Nicol SC, Andersen NA, Tomasi TE (2000) Seasonal variations in thyroid hormone levels in free-living echidnas (Tachyglossus aculeatus). Gen Comp Endocrinol 117:1–7PubMedGoogle Scholar
  179. Nilsson P, Hollmen T, Atkinson S, Mashburn K, Tuomi P, Esler D, Mulcahy D, Rizzolo D (2008) Effects of ACTH capture, and short term confinement on glucocorticoid concentrations in harlequin ducks (Histrionicus histrionicus). Comp Biochem Physiol A 149(1):275–283Google Scholar
  180. Nishihara H, Satta Y, Nikaido M, Thewissen JCM, Stanhope MJ, Okada N (2005) A retroposon analysis of Afrotherian phylogeny. Mol Biol Evol 22(9):1823–1833PubMedGoogle Scholar
  181. Noda K, Akiyoshi H, Aoki M, Shimada T, Ohashi F (2007) Relationship between transportation stress and polymorphonuclear cell functions of bottlenose dolphins, Tursiops truncatus. J Vet Med Sci 69(4):379–383PubMedGoogle Scholar
  182. Nordstrom CA (2002) Haul-out selection by Pacific harbor seals (Phoca vitulina richardii): isolation and perceived predation risk. Mar Mammal Sci 18(1):194–205Google Scholar
  183. Oki C, Atkinson S (2004) Diurnal patterns of cortisol and thyroid hormones in the harbor seal (Phoca vitulina) during summer and winter seasons. Gen Comp Endocrinol 136:289–297PubMedGoogle Scholar
  184. Olsen E, Grahl-Nielsen O (2003) Blubber fatty acids of minke whales: stratification, population identification and relation to diet. Mar Biol 142:13–24Google Scholar
  185. Ortiz RM (2001) Osmoregulation in marine mammals. J Exp Biol 204:1831–1844PubMedGoogle Scholar
  186. Ortiz RM, Worthy GAJ (2000) Effects of capture on adrenal steroid and vasopressin concentrations in free-ranging bottlenose dolphins (Tursiops truncatus). Comp Biochem Physiol A 125(3):317–324Google Scholar
  187. Ortiz CL, Costa D, Le Boeuf BJ (1978) Water and energy flux in elephant seal pups fasting under natural conditions. Physiol Zool 51:166–178Google Scholar
  188. Ortiz RM, Worthy GAJ, Byers FM (1999) Estimation of water turnover rates of captive West Indian manatees (Trichechus manatus) held in fresh and salt water. J Exp Biol 202:33–38PubMedGoogle Scholar
  189. Ortiz RM, Wade CE, Ortiz CL (2000) Prolonged fasting increases the response of the renin-angiotensin-aldosterone system, but not vasopressin levels, in postweaned northern elephant seal pups. Gen Comp Endocrinol 119(2):217–223PubMedGoogle Scholar
  190. Ortiz RM, Wade CE, Ortiz CL (2001) Effects of prolonged fasting on plasma cortisol and TH in postweaned northern elephant seal pups. Am J Physiol Reg I 280(3):R790–R795Google Scholar
  191. Ortiz RM, Houser DS, Wade CE, Ortiz CL (2003) Hormonal changes associated with the transition between nursing and natural fasting in northern elephant seals (Mirounga angustirostris). Gen Comp Endocrinol 130(1):78–83PubMedGoogle Scholar
  192. Ortiz RM, Crocker DE, Houser DS, Webb PM (2006) Angiotensin II and aldosterone increase with fasting in breeding adult male northern elephant seals (Mirounga angustirostris). Physiol Biochem Zool 79(6):1106–1122PubMedGoogle Scholar
  193. Parks SE, Johnson M, Nowack D, Tyack PL (2011) Individual right whales call louder in increased environmental noise. Biol Let 7:33–35Google Scholar
  194. Pedemera-Romano C, Aurioles-Gamboa D, Valdez RA, Brousset DM, Romano MC, Galindo F (2010) Serum cortisol in California sea lion pups (Zalophus californianus californianus). Anim Welfare 19:275–280Google Scholar
  195. Petrauskas LR, Atkinson S (2006) Variation of fecal corticosterone concentrations in captive Steller sea lions (Eumetopias jubatus) in relation to season and behavior. Aquat Mamm 32(2):168–174Google Scholar
  196. Petrauskas L, Atkinson S, Gulland F, Mellish J-A, Horning M (2008) Monitoring glucocorticoid response to rehabilitation and research procedures in California and Steller sea lions. J Exp Zool A 309(2):73–82Google Scholar
  197. Pietraszek J, Atkinson S (1994) Concentrations of estrone sulfate and progesterone in plasma and saliva, vaginal cytology, and bioelectric impedance during the estrous cycle of the Hawaiian monk seal (Monachus schauinslandi). Mar Mammal Sci 10(4):430–441Google Scholar
  198. Queisser N, Schupp N (2012) Aldosterone, oxidative stress, and NF-ҡB activation in hypertension-related cardiovascular and renal diseases. Free Radical Bio Med 53:314–327Google Scholar
  199. Raeside JI, Ronald K (1981) Plasma concentration of oestrone, progesterone and corticosteroids during late pregnancy and after parturition in the harbour seal. J Reprod Fertil 61:135–139PubMedGoogle Scholar
  200. Read AJ, Drinker P, Northridge S (2006) Bycatch of marine mammals in US and global fisheries. Conserv Biol 20(1):163–169PubMedGoogle Scholar
  201. Reiderson TH, McBain JF, Dalton LM, Rinaldi MG (2001) Mycotic diseases. In: Dierauf LA, Gulland FMD (eds) CRC handbook of marine mammal medicine. CRC Press, New York, pp 337–355Google Scholar
  202. Reiter J, Panken KJ, Le Boeuf BJ (1981) Female competition and reproductive success in northern elephant seals. Anim Behav 29:670–687Google Scholar
  203. Ridgway SH, Patton GS (1971) Dolphin thyroid: some anatomical and physiological findings. Z Vergl Physiologie 71(2):129–141Google Scholar
  204. Riedman M (1990) The pinnipeds: seals, sea lions, and walruses (No. 12). Univ of California PressGoogle Scholar
  205. Riedman ML, Le Boeuf BJ (1982) Mother-pup separation and adoption in northern elephant seals. Behav Ecol Sociobiol 11(3):203–215Google Scholar
  206. Risch D, Corkeron PJ, Ellison WT, Van Parijs SM (2012) Changes in humpback whale song occurrence in response to an acoustic source 200 km away. PLoS One 7(1):e29741PubMedCentralPubMedGoogle Scholar
  207. Robard D (1974) Statistical quality control and routing data procesing for radioimmunoassays and immunoradiometric assays. Clin Chem Lab Med 20:1255–1270Google Scholar
  208. Robeck TR, Schneyer AL, McBain JF, Dalton LM, Walsh MT, Czekala NM, Kraemer DC (1993) Analysis of urinary immunoreactive steroid metabolites and gonadotropins for characterization of the estrous cycle, breeding period, and seasonal estrous activity of captive killer whales (Orcinus orca). Zoo Biol 12:173–187Google Scholar
  209. Robinson G, del Pino EM (1985) El Nino in the Galapagos Islands: the 1982–83 Event. Publication of the Charles Darwin Foundation for the Galapagos Islands (Contribution No. 388), Quito, EcuadorGoogle Scholar
  210. Rolland RM (2000) A review of chemically-induced alterations in thyroid and vitamin A status from field studies of wildlife and fish. J Wildl Dis 36(4):615–635PubMedGoogle Scholar
  211. Rolland RM, Parks SE, Hunt KE, Castellote M, Corkeron PJ, Nowacek DP, Wasser SK, Kraus SD (2012) Evidence that ship noise increases stress in right whales. Proc R Soc B 279:2363–2368PubMedCentralPubMedGoogle Scholar
  212. Romano T, Keogh M, Kelly C, Feng P, Berk L, Schlundt CE, Carder DA, Finneran JJ (2004) Anthropogenic sound and marine mammal health: measures of the nervous and immune systems before and after intense sound exposures. Can J Fish Aquat Sci 61:1124–1134Google Scholar
  213. Romero LM (2002) Seasonal changes in plasma glucocorticoid concentrations in free-living vertebrates. Gen Comp Endocrinol 128:1–24PubMedGoogle Scholar
  214. Romero LM (2004) Physiological stress in ecology: lessons from biomedical research. Trends Ecol Evol 19(5):249–255PubMedGoogle Scholar
  215. Romero LM, Butler LK (2007) Endocrinology of stress. Int J Comp Psychol 20:89–95Google Scholar
  216. Romero LM, Dickens MJ, Cyr NE (2009) The reactive scope model - A new model integrating homeostasis, allostasis, and stress. Horm Behav 55:375–389PubMedGoogle Scholar
  217. Rosen DAS, Kumagai S (2008) Hormone changes indicate that winter is a critical period for food shortages in Steller sea lions. J Comp Physiol B 178:573–583PubMedGoogle Scholar
  218. Ross PS, Pohajdak B, Bowen WD, Addison RF (1993) Immune function in free-ranging harbor seal (Phoca vitulina) mothers and their pups during the nursing period. J Wildl Dis 29(1):21–29PubMedGoogle Scholar
  219. Routti H, Arukwe A, Jenssen BM, Letcher RJ, Nyman M, Bachman C, Gabrielsen GW (2010) Comparative endocrine disruptive effects of contaminants in ringed seals (Phoca hispida) from Svalbard and the Baltic Sea. Comp Biochem Physiol 152:306–312Google Scholar
  220. Sands J, Creel S (2004) Social dominance, aggression and faecal glucocorticoid levels in a wild population of wolves, Canis lupus. Anim Behav 67(3):387–396Google Scholar
  221. Sapolsky RM, Krey LC, McEwen BS (1986) The neuroendocrinology of stress and aging: the glucocorticoid cascade hypothesis. Endocr Rev 7(3):284–301PubMedGoogle Scholar
  222. Sapolsky RM, Romero LM, Munck AU (2000) How do glucocorticoids influence stress response? Integrating permissive, suppressive, stimulatory and preparative actions. Endocr Rev 21(1):55–89PubMedGoogle Scholar
  223. 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):635–647Google Scholar
  224. Schulkin J (1999) The neuroendocrine regulation of behavior. Cambridge University Press, New York, p 323Google Scholar
  225. Schwacke LH, Zolman ES, Balmer BC, De Guise S, George RC, Hoguet J, Hohn AA, Kucklick JR, Lamb S, Levin M, Litz JA, McFee WE, Place NJ, Townsend FI, Wells RS, Rowles TK (2012) Anaemia, hypothyroidism and immune suppression associated with polychlorinated biphenyl exposure in bottlenose dolphins (Tursiops truncatus). Proc R Soc B 279:48–57PubMedCentralPubMedGoogle Scholar
  226. Selye H (1936) A syndrome produced by diverse nocuous agents. Nature 138:32Google Scholar
  227. Shane SH (1995) Behavior patterns of pilot whales and Risso’s dolphins off Santa Catalina Island, California. Aqua Mamm 21(3):195–197Google Scholar
  228. Shimamura M, Yasue H, Ohshima K, Abe H, Kato H, Kishiro T, Goto M, Munechika I, Okada N (1997) Molecular evidence from retroposons that whales form a clade within even-toed ungulates. Nature 388:666–670PubMedGoogle Scholar
  229. Sivle LD, Kvadsheim PH, Fahlman A, Lam FPA, Tyack PL, Miller PJO (2012) Changes in dive behavior during naval sonar exposure in killer whales, long-finned pilot whales and sperm whales. Frontiers in Physiology 3:1Google Scholar
  230. Slade RW (1992) Limited MHC polymorphism in the southern elephans seal: implications for MHC evolution and marine mammal population biology. Proc Royal Soc Lond Ser B Biol Sci 249.1325:163–171Google Scholar
  231. Sonne C (2010) Health effects from long-range transported contaminants in Arctic top predators: an integrated review based on studies of polar bears and relevant model species. Environ Int 36:461–491PubMedGoogle Scholar
  232. Sonne C, Iburg T, Leifsson PS, Born EW, Letcher RJ, Dietz R (2011) Thyroid gland lesions in organohalogen contaminated East Greenland polar bears (Ursus maritimus). Toxicol Environ Chem 93(4):789–805Google Scholar
  233. Sormo EG, Jussi I, Jussi M, Braathen M, Skaare JU, Jenssen BM (2005) Thyroid hormone status in gray seal (Halichoerus grypus) pups from the Baltic Sea and the Atlantic Ocean in relation to organochlorine pollutants. Environ Toxicol Chem 24(3):610–616PubMedGoogle Scholar
  234. Spencer CA, Lum SMC, Wilber JF, Kaptein EM, Nicoloff JT (1983) Dynamics of serum thyrotropin and thyroid hormone changes in fasting. J Clin Endocr Metab 56(5):883–888PubMedGoogle Scholar
  235. Spoon TR, Romano TA (2012) Neuroimmunological response of beluga whales (Delphinapterus leucas) to translocation and a novel social environment. Brain Behav Immun 26:122–131PubMedGoogle Scholar
  236. St. Aubin DJ (1987) Stimulation of thyroid hormone secretion by thyrotropin in beluga whales, Delphinapterus leucas. Can J Vet Res 51:409–412Google Scholar
  237. St. Aubin DJ (2001) Endocrinology. In: Dierauf LA, Gulland FMD (eds) Marine Mammal Medicine. CRC Press, Boca Raton, pp 165–192Google Scholar
  238. St. Aubin DJ, Dierauf LA (2001) Stress and marine mammals. In Dierauf LA, Gulland FMD (eds) Marine Mammal Medicine. CRC Press, Boca Raton, pp 253–269Google Scholar
  239. St. Aubin DJ, Geraci JR (1986) Adrenocortical function in pinniped hyponatremia (Phoca hispida). Mar Mammal Sci 2(4):243–250Google Scholar
  240. St. Aubin DJ, Geraci JR (1988) Capture and handling stress suppresses circulating levels of thyroxine (T4) and triiodothyronine (T3) in beluga whales Delphinapterus leucas. Physiol Zool 61(2):170–175Google Scholar
  241. 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 46:796–803Google Scholar
  242. St. Aubin DJ, Geraci JR (1990) Adrenal responsiveness to stimulation by adrenocorticotropic hormone (ACTH) in captive beluga whales (Delphinapterus leucas). Can Bull Fish Aquat Sci 224:149–157Google Scholar
  243. St. Aubin DJ, Geraci JR (1992) Thyroid hormone balance in beluga whales, Delphinapterus leucas: dynamics after capture and influence of thyrotropin. Can J Vet Res 56:1–5Google Scholar
  244. St. Aubin DJ, Ridgway SH, Wells RS, Rhinehart H (1996) Dolphin thyroid and adrenal hormones: circulating levels in wild and semidomesticated Tursiops truncatus, and influence of sex, age, and season. Mar Mammal Sci 12(1):1–13Google Scholar
  245. St. Aubin DJ, DeGuise S, Richard PR, Smith TG, Gerack JR (2001) Hematology and plasma chemistry as indicators of health and ecological status in beluga whales, Delphinapterus leucas. Arctic 54(3):317–331Google Scholar
  246. 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 Mammal Sci 29(1):14–35Google Scholar
  247. Subramanian N, Bray MA (1987) Interleukin 1 releases histamine from human basophils and mast cells in vitro. J Immunol 138(1):271–275PubMedGoogle Scholar
  248. Suzuki M, Tobayama T, Katsumata E, Yoshioka M, Aida K (1998) Serum cortisol levels in captive killer whale and bottlenose dolphin. Fish Sci 64(4):643–647Google Scholar
  249. Suzuki M, Nozawa A, Ueda K, Bungo T, Terao H, Asahina K (2012) Secretory patterns of catecholamines in Indo-Pacific bottlenose dolphins. Gen Comp Endocrinol 177:76–81PubMedGoogle Scholar
  250. Tabuchi M, Veldhoen N, Dangerfield N, Jeffries S, Helbing CC, Ross PS (2006) PCB-related alteration of thyroid hormones and thyroid hormone receptor gene expression in free-ranging harbor seals (Phoca vitulina). Environ Health Perspect 114(7):1024–1031PubMedCentralPubMedGoogle Scholar
  251. Teruhisa U, Ryoji H, Taisuke I, Tatsuya S, Fumihiro M, Tatsuo S (1981) Use of saliva for monitoring unbound free cortisol levels in serum. Clin Chim Acta 110:245–253Google Scholar
  252. Theodorou J, Atkinson S (1998) Monitoring total androgen concentrations in saliva from captive Hawaiian monk seals (Monachus schauinslandi). Mar Mammal Sci 14(2):304–310Google Scholar
  253. Thomas JA, Kastelein RA, Awbrey FT (1990) Behavior and blood catecholamines of captive belugas during playbacks of noise from an oil drilling platform. Zoo Biol 9(5):393–402Google Scholar
  254. Thomasi TE, Hellgren EC, Tucker TJ (1998) Thyroid hormone concentrations in black bears (Ursus americanus): hibernation and pregnancy effects. Gen Comp Endocrinol 109:192–199Google Scholar
  255. Thomson CA, Geraci JR (1986) Cortisol, aldosterone, and leukocytes in the stress response of bottlenose dolphins, Tursiops truncatus. Can J Fish Aquat Sci 43(5):1010–1016Google Scholar
  256. Touma C, Palme R, Sachser N (2001) Different types of oestrous cycle in two closely related South America rodents (Cavia aperea and Galea musteloides) with different social and mating systems. Reproduction 121:791–801PubMedGoogle Scholar
  257. Touma C, Sachser N, Mӧstl E, Palme R (2003) Effects of sex and time of day on metabolism and excretion of corticosterone in urine and feces of mice. Gen Comp Endocrinol 130:267–278PubMedGoogle Scholar
  258. Trillmich F, Ono KA (1991) Pinnipeds and El Nino. Springer, New York, pp 66–74Google Scholar
  259. Tripovich JS, Hall-Aspland S, Charrier I, Arnould JPY (2012) The behavioural response of Australian fur seals to motor boat noise. PLOS one 7(5):e37228PubMedCentralPubMedGoogle Scholar
  260. Tripp KM, Verstegen JP, Deutsch CJ, Bonde RK, de Wit M, Manire CA, Gaspard J, Harr KE (2011) Evaluation of adrenocortical function in Florida Manatees (Trichechus manatus latirostris). Zoo Biol 30:17–31PubMedGoogle Scholar
  261. Trumble SJ, O’Neil D, Cornick LA, Gulland FMD, Castellini MA, Atkinson S (2012) Endocrine changes in harbor seal (Phoca vitulina) pups undergoing rehabilitation. Zoo Biol 32(2):134–141PubMedGoogle Scholar
  262. Tseng YP, Huang YC, Kyle GT, Yang MC (2011) Modeling the impacts of cetacean-focused tourism in Taiwan: observations from cetacean watching boats: 2002–2005. Environ Manag 47:56–66Google Scholar
  263. Turnbull BS, Cowan DF (1998) Myocardial contraction band necrosis in stranded cetaceans. J Comp Pathol 118:317–327PubMedGoogle Scholar
  264. Tyack PL (2008) Implications for marine mammals of large-scale changes in marine acoustic environment. J Mammal 89(3):549–558Google Scholar
  265. Uhen MD (2007) Evolution of marine mammals: back to the sea after 300 million years. Anat Record 290:514–522Google Scholar
  266. Urick RJ (1983) Principles of underwater sound, 3rd edn. McGraw Hill, New YorkGoogle Scholar
  267. van der Heyden JT, Docter R, van Toor H, Wilson JH, Hennemann G, Krenning EP (1986) Endocrinol Metab 251(2):E156–E163Google Scholar
  268. Van Dolah FM, Doucette GJ, Gulland FMD, Rowles TL, Bossart GD (2003) Impacts of algal toxins on marine mammals. In: Bossart GD, Fournier M, O’Shea TJ (eds) (Vos JG., Toxicology of marine mammalsTaylor & Francis, London pp, pp 247–270Google Scholar
  269. Vázquez-Medina JP, Crocker DE, Forman HJ, Ortiz RM (2010) Prolonged fasting does not increase oxidative damage or inflammation in northern elephant seal pups. J Exp Biol 213:2524–2530PubMedCentralPubMedGoogle Scholar
  270. Vázquez-Medina JP, Zenteno-Savin T, Elsner R, Ortiz RM (2012) Coping with physiological oxidative stress: a review of antioxidant strategies in seals. J Comp Physiol B 182:741–750PubMedCentralPubMedGoogle Scholar
  271. Velten BP, Dillaman RM, Kinsey ST, McLellan WA, Pabst DA (2013) Novel locomotor muscle design in extreme deep-diving whales. J Exp Biol 216:1862–1871PubMedGoogle Scholar
  272. Verrier D, Atkinson S, Guinet C, Groscolas R, Arnould JPY (2012) Hormonal responses to extreme fasting in subantarctic fur seal (Arctocephalus tropicalis) pups. Am J Physiol Reg I 302:R929–R940Google Scholar
  273. Villanger GD, Jenssen BM, Fjeldberg RR, Letcher RJ, Muir DCG, Kirkegaard M, Sonne C, Dietz R (2011) Exposure to mixtures of organohalogen contaminants and associative interactions with thyroid hormones in East Greenland polar bears (Ursus maritimus). Environ Int 37:694–708PubMedGoogle Scholar
  274. von Euler US (1946) A specific sympathomimetic ergone in adrenergic nerve fibres (sympathin) and it’s relations to adrenalin and noradrenaline. Acta Physiol Scand 12:73–96Google Scholar
  275. Walker LA, Czekala NM, Cornell LH, Joseph BE, Dahl KD, Lasley BL (1987) Analysis of the ovarian cycle and pregnancy of the killer whale by urinary hormone measurement. Biol Reprod 39(5):1013–1020Google Scholar
  276. Walker LA, Cornell L, Dahl KD, Czekala NM, Dargen CM, Joseph B, Hsueh AJ, Lasley BL (1988) Urinary concentrations of ovarian steroid hormone metabolites and bioactive follicle-stimulating hormone in killer whales (Orcinus orcus) during ovarian cycles and pregnancy. Biol Reprod 39(5):1013–1020PubMedGoogle Scholar
  277. Wang D, Atkinson S, Hoover-Miller A, Li QX (2005) Analysis of organochlorines in harbor seal (Phoca vitulina) tissue samples from Alaska using gas chromatography/ion trap mass spectrometry by an isotopic dilution technique. Rapid Commun Mass Spectrom 19:1815–1821PubMedGoogle Scholar
  278. Wang D, Atkinson S, Hoover-Miller A, Lee S, Li QX (2007) Organochlorines in harbor seal (Phoca vitulina) tissues from the northern Gulf of Alaska. Environ Pollut 146:268–280PubMedGoogle Scholar
  279. Wang D, Li QX, Atkinson S (2010) Tissue distribution of polychlorinated biphenyls and organochlorine pesticides and potential toxicity to Alaskan northern fur seals assessed using PCBs congener specific mode of action schemes. Arch Environ Contam Toxicol 58:478–488PubMedGoogle Scholar
  280. Wasser SK, Hunt KE, Brown JL, Cooper K, Crockett CM, Bechert U, Millspaugh JJ, Larson S, Monfort SL (2000) A generalized fecal glucocorticoid assay for use in a diverse array of nondomestic mammalian and avian species. Gen Comp Endocrinol 120:260–275PubMedGoogle Scholar
  281. Weilgart LS (2007) The impacts of anthropogenic ocean noise on cetaceans and implications for management. Can J Zool 85:1091–1116Google Scholar
  282. Weingartner GM, Thomton SJ, Andrews RD, Enstipp MR, Barts AD, Hochacka PW (2012) The effects of experimentally induced hyperthyroidism on the diving physiology of harbor seals (Phoca vitulina). Front Physiol 3:380PubMedCentralPubMedGoogle Scholar
  283. Weise MJ, Costa DP, Kudela RM (2006) Movement and diving behavior of male California sea lion (Zalophus californianus) during anomalous oceanographic conditions of 2005 compared to those of 2004. Geogr Res Let 33(22)Google Scholar
  284. Weissman C (1990) The metabolic response to stress: an overview and update. Anesthesiology 73(2):308–327PubMedGoogle Scholar
  285. Wenberg GM, Holland JC (1973) The circannual variations of thyroid activity in the woodchuck (Marmota monax). Comp Biochem Physiol 44A:775–780Google Scholar
  286. Whealtly KE, Nichols PD, Hindell MA, Harcourt RG, Bradshaw CJA (2007) Temporal variation in the vertical stratification of blubber fatty acids alters the diet predictions for lactating Weddell seals. J Exp Mar Ecol 352:103–113Google Scholar
  287. Wingfield JC (2013) Ecological processes and the ecology of stress: the impacts of abiotic and environmental factors. Functional Ecol 27:37–44Google Scholar
  288. Wright AJ, Soto NA, Baldwin AL, Bateson M, Beal CM, Clark C, Deak T, Edwards E, Ferandez A, Godinho A, Hatch L, Kakuschke A, Lusseau D, Martineau D, Romero ML, Weilgart LS, Wintle BA, Notarbartolo-di-Sciara G, Martin V (2007) Do marine mammals experience stress related to anthropogenic noise? Int Comp Phychol 20:274–316Google Scholar
  289. Yochem PK, Gulland FMD, Stewart BS, Haulena M, Mazet JAK, Boyce WM (2008) Thyroid function testing in elephant seals in health and disease. Gen Comp Endocrinol 155:627–632Google Scholar
  290. Zenteno-Savin T, Castellini MA (1998a) Changes in the plasma levels of vasoactive hormones during apnea in seals. Comp Biochem Physiol 119C:7–12Google Scholar
  291. Zenteno-Savin T, Castellini MA (1998b) Plasma angiotensin II, arginine vasopressin and atrial natriuretic peptide in free ranging and captive seals and sea lions. Comp Biochem Physiol 119C:1–6Google Scholar
  292. Zhou A, Wei Z, Read RJ, Carrell RW (2006) Structural mechanism for the carriage and release of thyroxine in the blood. Proc Nat Acad Sci 103(36):13321–13326PubMedCentralPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Shannon Atkinson
    • 1
  • Daniel Crocker
    • 2
  • Dorian Houser
    • 3
  • Kendall Mashburn
    • 1
  1. 1.School of Fisheries and Ocean Sciences, Juneau CenterUniversity of Alaska FairbanksJuneauUSA
  2. 2.Department of BiologySonoma State UniversityRohnert ParkUSA
  3. 3.National Marine Mammal FoundationSan DiegoUSA

Personalised recommendations