Effects of handling regime and sex on changes in cortisol, thyroid hormones and body mass in fasting grey seal pups

Comparative Biochemistry and Physiology - A Molecular and Integrative Physiology

Volumn 161, Issue 1, 2012, Pages 69-76

  Bennett, Kimberley A ^a   Moss, Simon E W ^a   Pomeroy, Paddy ^a   Speakman, John R ^b   Fedak, Mike A ^a  

^a UNIVERSITY OF ST ANDREWS   (United Kingdom)

^b Institute of Biological and Environmental Sciences   (United Kingdom)

Author keywords

Glucocorticoid; Handling frequency; Phocid; Postweaning fast; Stress; T3; T4

Indexed keywords

HYDROCORTISONE; THYROID HORMONE; LIOTHYRONINE; THYROXINE;

ANIMAL CARE; ANIMAL EXPERIMENT; ARTICLE; BLOOD SAMPLING; BODY MASS; CELLULAR STRESS RESPONSE; CONTROLLED STUDY; DIET RESTRICTION; ENDOCRINE SYSTEM; ENERGY BALANCE; FEMALE; HYDROCORTISONE BLOOD LEVEL; MALE; NONHUMAN; SEX DIFFERENCE; THYROID HORMONE BLOOD LEVEL; ANIMAL; BLOOD; BODY WEIGHT; METABOLISM; MOTIVATION; PHOCA; SEXUAL DEVELOPMENT;

ANIMALIA; HALICHOERUS GRYPUS; PHOCIDAE;

ANIMALS; BODY WEIGHT; FASTING; FEMALE; HANDLING (PSYCHOLOGY); HYDROCORTISONE; MALE; SEALS, EARLESS; SEX CHARACTERISTICS; THYROXINE; TRIIODOTHYRONINE;

EID: 84857363695     PISSN: 10956433     EISSN: 15314332     Source Type: Journal    
DOI: 10.1016/j.cbpa.2011.09.003     Document Type: Article

References (112)

1. Anderson S.S., Fedak M.A. Grey seal energetics: females invest more in male offspring. J. Zool. Lond. 1987, 211:667-679.
2. ob mice. Endocrinology 1998, 139:4000-4003.
3. Atkinson S. Reproductive biology of seals. Rev. Reprod. 1997, 2:175-194.
4. Baker J.D., Fowler C.W. Pup weight and survival of northern fur seals Callorhinus ursinus. J. Zool. Lond. 1992, 227:231-238.
5. Beck C.A., Bowen W.D., Iversen S. Sex differences in the seasonal patterns of energy storage and expenditure in a phocid seal. J. Anim. Ecol. 2003, 72:280-291.
6. Belthoff J.R., Dufty Jnr.,A.M. Corticosterone, body condition and locomotor activity: a model for dispersal in screech owls. Anim. Behav. 1998, 55:405-415.
7. Bennett K.A., Speakman J.R., Moss S.E.W., Pomeroy P., Fedak M.A. Effects of mass and body composition on fasting fuel utilisation in grey seal pups (Halichoerus grypus: Fabricius): an experimental study using supplementary feeding. J. Exp. Biol. 2007, 210:3043-3053.
8. Bennett K.A., McConnell B.J., Moss S.E.W., Speakman J.R., Pomeroy P., Fedak M.A. Effects of age and body mass on development of diving capabilities of gray seal pups: costs and benefits of the postweaning fast. Physiol. Biochem. Zool. 2010, 83:911-923.
9. Bergendahl M., Vance M.L., Iranmanesh A., Thorner M.O., Veldhuis J.D. Fasting as a metabolic stress paradigm selectively amplifies cortisol secretory burst mass and delays the time of maximal nyctohemeral cortisol concentrations in healthy men. J. Clin. Endocrinol. Metab. 1996, 81:692-699.
10. Bianco A.C., Nunes M.T., Hell N.S., Maciel R.M.B. The role of glucocorticoids in the stress-induced reduction of extra-thyroidal 3,5,3'-triiodothyronine generation in rats. Endocrinology 1987, 120:1033-1038.
11. Blake N.G., Eckland D.J.A., Foster O.J.F., Lightman S.L. Inhibition of hypothalamic thyrotropin-releasing hormone messenger ribonucleic acid during food deprivation. Endocrinology 1991, 129:2714-2718.
12. Blas J., Bortolotti G.R., Tella J.L., Baos R., Marchant T.A. Stress response during development predicts fitness in a wild, long-lived vertebrate. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:8880-8884.
13. Bollaert P.E., Fieux F., Charpentier C., Lévy B. Baseline cortisol levels, cortisol response to corticotropin, and prognosis in late shock. Shock 2003, 19:13-15.
14. Burns J.M. The development of diving behaviour in juvenile Weddell seals: pushing physiological limits in order to survive. Can. J. Zool. 1999, 77:737-747.
15. Burns J.M., Skomp N., Bishop N., Lestyk K., Hammill M. Development of aerobic and anaerobic metabolism in cardiac and skeletal muscles from harp and hooded seals. J. Exp. Biol. 2010, 213:740-748.
16. Busch D.S., Hayward L. Stress in a conservation context: a discussion of glucocorticoid actions and how levels change with conservation-relevant variables. Biol. Conserv. 2009, 142:2844-2853.
17. Busch D.S., Sperry T.S., Wingfield J.C., Boyd E.H. Effects of repeated, short-term, corticosterone administration on the hypothalamo-pituitary-adrenal axis of the white-crowned sparrow, Zonatrichia leucophrys gambelii. Gen. Comp. Endocrinol. 2008, 158:211-223.
18. Challet E., Le Maho Y., Robin J.P., Malan A., Cherel Y. Involvement of corticosterone in the fasting-induced rise in protein-utilization and locomotor-activity. Pharmacol. Biochem. Behav. 1995, 50:405-412.
19. Chatfield C. The Analysis of Time Series: an Introduction 1989, Chapman and Hall, London, New York.
20. Cheikh R.B., Chomard P., Dumas P., Autissier N. Influence of prolonged fasting on thyroid hormone modulation of lypolysis in isolated epididymal adipocytes of Wistar rats. Eur. J. Endocrinol. 1994, 131:516-521.
21. Cherel Y., Leloup J., Le Maho Y. Fasting in king penguin II. Hormonal and metabolic changes during molt. Am. J. Physiol. 1988, 254:R178-R184.
22. Cherel Y., Robin J.-P., Le Maho Y. Physiology and biochemistry of long-term fasting in birds. Can. J. Zool. 1988, 66:159-166.
23. Cherel Y., Robin J.-P., Walch O., Karmann H., Netchitailo P., Le Maho Y. Fasting in king penguin I. Hormonal and metabolic changes during breeding. Am. J. Physiol. 1988, 254:R170-R177.
24. Coulson J.C. The growth of grey seal calves on the Farne Islands, Northumberland. Trans. Nat. Hist. Soc. 1959, 13:86-100. Northumberland, Durham and Newcastle upon Tyne.
25. Crawley M.J. Statistical Computing: an Introduction to Data Analysis Using S-Plus 2002, John Wiley and Sons, Ltd., Chichester.
26. Creel J.E., Fox A., Hardy J., Sands B.Garrott, Peterson R.O. Snowmobile activity and glucocorticoid stress responses in wolves and elk. Conserv. Biol. 2002, 16:809-814.
27. Cremaschi G.A., Gorelik G., Klecha A.J., Lysionek A.E., Genaro A.M. Chronic stress influences the immune system through the thyroid axis. Life Sci. 2000, 67:3171-3179.
28. Dallman M.F., Bhatnagar S. Chronic stress and energy balance: role of the hypothalamo-pituitary-adrenal axis. Coping with the Environment: Neural and Endocrine Mechanisms 2001, Volume IV:179-210. Oxford University Press, New York. B.S. McEwen, H.M. Goodman (Eds.).
29. Divertie G.D., Jensen M.D., Miles J.M. Stimulation of lipolysis in humans by physiological hypercortisolemia. Diabetes 1991, 40:1228-1232.
30. Djurhuus C.B., Gravholt C.H., Nielsen S., Mengel A., Christiansen J.S., Schmitz O.E., Moller N. Effects of cortisol on lipolysis and regional interstitial glycerol levels in humans. Am. J. Physiol. 2002, 283:E172-E177.
31. Djurhuus C.B., Gravholt C.H., Nielsen S., Pedersen S.B., Moller N., Schmitz O. Additive effects of cortisol and growth hormone on regional and systemic lipolysis in humans. Am. J. Physiol. 2004, 286:E488-E494.
32. Dohler K.D., Gartner K., von zur Muhlen A., Dohler U. Activation of anterior pituitary, thyroid and adrenal gland in rats after disturbance stress. Acta Endocrinol. 1977, 86:489-497.
33. du Dot T.J., Rosen D.A., Richmond J.P., Kitasky A.S., Zinn S.A., Trites A.W. Changes in glucocorticoids, IGF-1 and thyroid hormones as indicators of nutritional stress and subsequent refeeding in Steller sea lions (Eumatopias jubata). Comp. Biochem. Physiol. A 2009, 152:524-534.
34. Engelhard G.H., van den Hoff J., Broekman M., Baarspul A.N.J., Field I., Burton H.R., Reijnders P.J.H. Mass of weaned elephant seal pups in areas of high and low disturbance. Polar Biol. 2001, 24:244-251.
35. Engelhard G.H., Brasseur S.M.J.M., Hall A.J., Burton H.R., Reijnders P.J.H. Adrencortical responsiveness in southern elephant seal mothers and pups during the lactation period and the effect of scientific handling. J. Comp. Physiol. B. 2002, 172:315-328.
36. Fedak M.A., Anderson S.S. The energetics of lactation: accurate measurements from a large wild mammal, the grey seal (Halichoerus grypus). J. Zool. Lond. 1982, 198:473-479.
37. Fedak M.A., Arnbom T., Boyd Il.L. The relation between the size of southern elephant seal mothers, the growth of their pups and the use of maternal energy, fat and protein during lactation. Physiol. Zool. 1996, 69:887-911.
38. Friedl K.E., Moore R.J., Hoyt R.W., Marchitelli L.J., Martinez-Lopez L.E., Askew E.W. Endocrine markers of semistarvation in healthy lean men in a multistressor environment. J. Appl. Physiol. 2000, 88:1820-1830.
39. Friedman Y., Bacchus R., Raymond R., Joffe R.T., Nobrega J.N. Acute stress increases thyroid hormone levels in rat brain. Biol. Psychiatry 1999, 45:234-237.
40. Gardiner K.J., Hall A.J. Diel and annual variation in plasma cortisol concentrations among wild and captive harbor seals (Phoca vitulina). Can. J. Zool. 1997, 75:1773-1780.
41. Goutte A., Angelier F., Welcker J., Moe B., Clément-Chastel C., Gabrielsen G.W., Bech C., Chastel O. Long term survival effect of corticosterone manipulation in Black-legged kittiwakes. Gen. Comp. Endocrinol. 2010, 167:246-251.
42. Green P.K., Wilkinson C.W., Woods S.C. Intraventricular corticosterone increases the rate of body-weight gain in underweight adrenalectomized rats. Endocrinology 1992, 130:269-275.
43. Guinet C., Servera N., Mangin S., Georges J.-Y., Lacroix A. Change in plasma cortisol and metabolites during the attendance period ashore in fasting lactating subantarctic fur seals. Comp. Biochem. Physiol. A. 2004, 137:523-531.
44. Gulland F.M.D., Haulena M., Lowenstine L.J.E.A. Adrenal function in wild and rehabilitated Pacific harbor seals (Phoca vitulina richardii) and in seals with phocine herpesvirus-associated adrenal necrosis. Mar. Mamm. Sci. 1999, 15:810-827.
45. Hadley M.E. Endocrinology 1992, Prentice Hall, New Jersey.
46. Hall A.J., McConnell B.J., Barker R.J. Factors affecting first-year survival in grey seals and their implications for life history strategy. J. Anim. Ecol. 2001, 70:138-149.
47. Hall A.J., McConnell B.J., Barker R.J. The effect of total immunoglobulin levels, mass and condition on the first-year survival of grey seal pups. Funct. Ecol. 2002, 16:462-474.
48. Hall A.J., Thomas G.O., McConnell B.J., Barker R.J. Exposure to persistent organic pollutants and first-year survival probability in gray seal pups. Environ. Sci. Technol. 2009, 43:6364-6369.
49. Harcourt R.G., Turner E., Hall A., Waas J.R., Hindell M. Effects of capture stress on free-ranging, reproductively active male Weddell seals. J. Comp. Physiol. A 2010, 196:147-154.
50. Harlow H.J., Lindzey F.G., van Sickle W.D., Gern W.A. Stress response of cougars to nonlethal pursuit by hunters. Can. J. Zool. 1992, 70:136-139.
51. Harris R.B.S., Zhou J., Youngblood B.D., Rybkin I.I., Smagin G.N., Ryan D.H. Effect of repeated stress on body weight and body composition of rats fed low- and high-fat diets. Am. J. Physiol. 1998, 275:R1928-R1938.
52. Harwood J., Prime J.H. Some factors affecting the size of British grey seal populations. J. Appl. Ecol. 1978, 15:401-411.
53. Heath J. Corticosterone levels during nest departure of juvenile American Kestrels. Condor 1997, 99:806-811.
54. Helmreich D.L., Crouch M., Dorr N.P., Parfitt D.P. Peripheral tri-iodothyronine (T3) levels during escapable and inescapable footshock. Physiol. Behav. 2006, 87:114-119.
55. Hunt K.E., Trites A.W., Wasser S.K. Validation of a fecal glucocorticoid assay for Steller sea lions (Eumatopias jubatus). Physiol. Behav. 2004, 80:595-601.
56. Ihaka R., Gentleman R. R: a language for data analysis and graphics. J. Comput. Graph. Stat. 1996, 5:299-314.
57. Kern M., Bacon W., Long D., Cowie R.J. Possible roles for corticosterone and critical size in the fledging of nestling pied flycatchers. Physiol. Biochem. Zool. 2001, 74:651-659.
58. Kioukia-Fougia N., Antoniou K., Bekris S., Liapi C., Christofidis I., Papadopoulou-Daifoti Z. The effects of stress exposure on the hypothalamic-pituitary-adrenal axis, thymus, thyroid hormones, and glucose levels. Prog. Neuropsychopharmacol. Biol. Psychiatry 2002, 26:823-830.
59. Laugero K.D., Moberg J.P. Energetic response to repeated restraint stress in rapidly growing mice. Am. J. Physiol. 2000, 279:E33-E43.
60. Le Boeuf B.J., Morris P., Reiter J. Juvenile survivorship of northern elephant seals. Elephant Seals: Population Ecology, Behavior and Physiology 1994, 121-136. University of California Press, Berkeley, Los Angeles, London. B.J. Le Boeuf, R.M. Laws (Eds.).
61. Legaspi A., Albert J.D., Calvano S.E., Brennan M.F., Lowry S.F. Proteolysis of skeletal-muscle in response to acute elevation of plasma cortisol in man. Surg. Forum 1985, 36:16-18.
62. Lewis M., Campagna C., Uhart M., Ortiz C.L. Ontogenetic and seasonal variation in blood parameters in southern elephant seals. Mar. Mamm. Sci. 2001, 17:862-872.
63. Lidgard D.C., Boness D.J., Bowen W.D., McMillan J.I. The implications of stress on male mating behaviour and success in a sexually dimorphic polygymous mammal, the grey seal. Horm. Behav. 2008, 53:241-248.
64. Lovallo W.R., Farag N.H., Vincent A.S., Thomas T.L., Wilson M.F. Cortisol responses to mental stress, exercise and meals following caffeine intake in men and women. Pharmacol. Biochem. Behav. 2006, 83:441-447.
65. Mantha L., Palacios E., Deshaies Y. Modulation of triglyceride metabolism by glucocorticoids in diet-induced obesity. Am. J. Physiol. 1999, 277:R455-R464.
66. Mashburn K.L., Atkinson S. Evaluation of adrenal function in serum and feces of Steller sea lions (Eumatopias jubatus): influences of molt, gender, sample storage and age on glucocorticoid metabolism. Gen. Comp. Endocrinol. 2004, 136:371-381.
67. Mashburn K.L., Atkinson S. Seasonal and predator influences on adrenal function in adult Steller sea lions: gender matters. Gen. Comp. Endocrinol. 2007, 150:246-252.
68. Matalka K.Z. Neuroendocrine and cytokines-induced responses to minutes, hours, and days of mental stress. Neurobiol. Lett. 2003, 24:283-292.
69. McCann T.S., Fedak M.A., Harwood J. Parental investment in southern elephant seals, Mirounga leonina. Behav. Ecol. Sociobiol. 1989, 25:81-87.
70. McMahon C.R., Burton H.R., Bester M.N. Weaning mass and the future survival of juvenile southern elephant seals, Mirounga leonina, at Macquarie Island. Antarct. Sci. 2000, 12:149-153.
71. McMahon C., van den Hoff J., Burton H. Handling intensity and the short- and long-term survival of elephant seals: addressing and quantifying research effects on wild animals. Ambio 2005, 34:426-429.
72. Mellish J.-A.E., Iverson S.J., Bowen W.D. Variation in milk production and lactation performance in grey seals and consequences for pup growth and weaning characteristics. Physiol. Biochem. Zool. 1999, 72:677-690.
73. Muehlenbein M.P., Watts D.P. The costs of dominance: testosterone, cortisol and intestinal parasites in wild male chimpanzees. Biopsychosoc. Med. 2010, 9:21.
74. Müllner A., Linsenmair K.E., Wikelski M. Exposure to ecotourism reduces survival and affects stress response in hoatzin chicks (Opisthocomus hoazin). Biol. Conserv. 2004, 118:549-558.
75. Myers M.J., Litz B., Atkinson S. The effects of age, sex, season and geographic region on circulating cortisol concentrations in threatened and endangered Steller sea lions (Eumatopias jubata). Gen. Comp. Endocrinol. 2010, 165:72-77.
76. Nordoy E.S., Blix A.S. Energy sources in fasting grey seal pups evaluated with computed tomography. Am. J. Physiol. 1985, 249:R471-R476.
77. Nordoy E.S., Ingebretsen O.C., Blix A.S. Depressed metabolism and low protein catabolism in fasting grey seal pups. Acta Physiol. Scand. 1990, 139:361-369.
78. Nordoy E.S., Stijfhoorn D.E., Raheim A., Blix A.S. Water flux and early signs of entrance into phase III of fasting in grey seal pups. Acta Physiol. Scand. 1992, 144:477-482.
79. Nordoy E.S., Aakvaag A., Larsen T.S. Metabolic adaptations to fasting in harp seal pups. Physiol. Zool. 1993, 66:926-945.
80. Noren S.R., Iverson S.J., Boness D.J. Development of the blood and muscle oxygen stores in gray seals (Halichoerus grypus): implications for juvenile diving capacity and the necessity of a terrestrial postweaning fast. Physiol. Biochem. Zool. 2005, 78:482-490.
81. Noren S.R., Boness D.J., Iverson S.J., McMillan J., Bowen W.D. Body condition at weaning affects the duration of the postweaning fast in gray seal pups (Halichoerus grypus). Physiol. Biochem. Zool. 2008, 81:269-277.
82. Ortiz R.M., MacKenzie D.S., Worthy G.A.J. Thyroid hormone concentrations in captive and free-ranging West Indian manatees (Trichechus manatus). J. Exp. Biol. 2000, 203:3631-3637.
83. Ortiz R.M., Noren D.P., Litz B., Ortiz C.L. A new perspective on adiposity in a naturally obese mammal. Am. J. Physiol. 2001, 281:E1347-E1351.
84. Ortiz R.M., Wade C.E., Ortiz C.L. Effects of prolonged fasting on plasma cortisol and TH in postweaned northern elephant seal pups. Am. J. Physiol. 2001, 280:R790-R795.
85. Padernera-Romano C., Aurioles-Gamboa D., Valdez R.A., Brousset D.M., Romano M.C., Galindo F. Serum cortisol in California sea lion pups (Zalophus californianus californianus). Anim. Welf. 2010, 19:275-280.
86. Padgett D.A., Glaser R. How stress influences the immune response. Trends Immunol. 2003, 24:444-448.
87. Pomeroy P.P., Fedak M.A., Rothery P., Anderson S. Consequences of maternal size for reproductive expenditure and pupping success of grey seals at North Rona, Scotland. J. Appl. Ecol. 1999, 68:235-253.
88. Ponsalle P., Srivastava L.S., Uht R., White J.D. Glucocorticoids are required for food deprivation-induced increases in hypothalamic neuropeptide Y expression. J. Neuroendocrinol. 1992, 4:585-591.
89. Reidarson T.H., McBain J.F. Hematologic, biochemical, and endocrine effects of dexamethasone on bottlenose dolphins (Tursiops truncatus). J. Zoo Wildl. Med. 1999, 30:310-312.
90. Reilly J.J. Adaptations to prolonged fasting in free-living, weaned gray seal pups. Am. J. Physiol. 1991, 260:R267-R272.
91. Reilly J.J., Fedak M.A. Measurement of the body composition of living gray seals by hydrogen isotope dilution. J. Appl. Physiol. 1990, 69:885-891.
92. Reiter J., Stinson N.L., Le Boeuf B.J. Northern elephant seal development: the transition from weaning to nutritional independence. Behav. Ecol. Sociobiol. 1978, 3:337-367.
93. Rich E.L., Romero L.M. Exposure to chronic stress downregulates corticosterone responses to acute stressors. Am. J. Physiol. 2005, R1628-R1636.
94. Robin J.-P., Boucontet L., Chillet P., Groscolas R. Behavioral changes in fasting emperor penguins: evidence for a "refeeding signal" linked to a metabolic shift. Am. J. Physiol. 1998, 274:R746-R753.
95. Romero L.M., Reed J.M. Collecting baseline corticosterone samples in the field: is under 3 min good enough?. Comp. Biochem. Physiol. A 2005, 140:73-79.
96. Romero L.M., Wikelski M. Exposure to tourism reduces stress-induced corticosterone levels in Galápagos marine iguanas. Biol. Conserv. 2002, 108:371-374.
97. Rosen D.A., Kumegai S. Hormone changes indicate that winter is a critical time for food shortages in Steller sea lions. J. Comp. Physiol. B 2008, 178:573-583.
98. Samra J.S., Clark M.L., Humphreys S.M., MacDonald I.A., Bannister P.A., Frayn K.N. Effects of physiological hypercortisolemia on the regulation of lipolysis in subcutaneous adipose tissue. J. Clin. Endocrinol. Metab. 1998, 83:626-631.
99. Sapolsky R.M., Romero L.M., Munck A.U. How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparatory actions. Endocr. Rev. 2000, 2:55-89.
100. Schumacher U., Heidemann G., Skirnisson K., Schumacher W., Pickering R.M. Impact of captivity and contamination level on blood parameters of harbour seals (Phoca vitulina). Comp. Biochem. Physiol. A. 1995, 112:455-462.
101. Simmons P.S., Miles J.M., Gerich J.E., Haymond M.W. Increased proteolysis - an effect of increases in plasma cortisol within the physiologic range. J. Clin. Invest. 1984, 73:412-420.
102. Sinclair A. Mammal populations: fluctuation, regulation, life history theory and their implications for conservation. Frontiers of Population Ecology 1996, 127-154. CSIRO, Melbourne, Australia. R.B. Floyd, W. Sheppard, P.J. De Barro (Eds.).
103. Spencer C.A., Lum S.M.C., Wilber J.F., Kaptein E.M., Nicoloff J.T. Dynamics of serum thyrotropin and thyroid hormone changes in fasting. J. Clin. Endocrinol. Metab. 1983, 56:883-888.
104. St Aubin D., Geraci J.R. Capture and handling stress suppresses circulating levels of thyroxine (T4) and triiodothyronine (T3) in beluga whales Delphinapterus leucas. Physiol. Zool. 1988, 6:170-175.
105. Tataranni P.A., Larson D.E., Snitker S., Young J.B., Flatt J.P., Ravussin E. Effects of glucocorticoids on energy metabolism and food intake. Am. J. Physiol. 1996, 271:E317-E325.
106. Thorson P.H., Le Boeuf B.J. Developmental aspects of diving in northern elephant seal pups. Elephant Seals: Population, Ecology, Behavior and Physiology 1994, 271-289. University of California Press, Berkeley, Los Angeles, London. B.J. Le Boeuf, R.M. Laws (Eds.).
107. Viscarra J.A., Vásquez-Medina J.P., Crocker D.E., Ortiz R.M. GLUT4 is upregulated despite decreased insulin signaling during prolonged fasting in northern elephant seal pups. Am. J. Physiol. 2010, 300:R150-R154.
108. Walker B.G., Boersma P.D., Wingfield J.C. Physiological and behavioural differences in Magellanic penguin chicks in undisturbed and tourist-visuted locations of a colony. Conserv. Biol. 2005, 19:1571-1577.
109. Walker B.G., Boersma P.D., Wingfield J.C. Habituation of adult Magellanic penguins to human visitation as expressed through behavior and corticosterone secretion. Conserv. Biol. 2006, 20:146-154.
110. Weiler H.A., Wang Z., Atkinson S.A. Whole body lean mass is altered by dexamethasone treatment through reductions in protein and energy utilization in piglets. Biol. Neonate 1997, 71:53-59.
111. Worthy G.A.J., Lavigne D.M. Mass loss, metabolic rate, and energy utilisation by harp and gray seal pups during the postweaning fast. Physiol. Zool. 1987, 60:352-364.
112. Zhou J., Yan X., Ryan D., Harris R.B.S. Sustained effects of repeated restraint stress on muscle and adipocyte metabolism in high fat fed rats. Am. J. Physiol. 1999, 277:R757-R766.