Cortisol modulates metabolism and energy mobilization in wild-caught pumpkinseed (Lepomis gibbosus)

  • Michael J. LawrenceEmail author
  • Erika J. Eliason
  • Aaron J. Zolderdo
  • Dominique Lapointe
  • Carol Best
  • Kathleen M. Gilmour
  • Steven J. Cooke


Acute elevation of cortisol via activation of the hypothalamic-pituitary-interrenal (HPI) axis aids the fish in dealing with a stressor. However, chronic elevation of cortisol has detrimental effects and has been studied extensively in lab settings. However, data pertaining to wild teleosts are lacking. Here, we characterized the metabolic consequences of prolonged cortisol elevation (96 h) in wild-caught pumpkinseed (Lepomis gibbosus). Pumpkinseed were implanted with cocoa butter alone (sham) or containing cortisol (25 mg kg−1 body weight), and at 24, 48, 72, and 96 h, tissue samples were collected, whole-body ammonia excretion was determined, and whole-organism metabolism was assessed using intermittent flow respirometry. Cortisol-treated pumpkinseed exhibited the highest plasma cortisol concentration at 24 h post-implantation, with levels decreasing over the subsequent time points although remaining higher than in sham-treated fish. Cortisol-treated fish exhibited higher standard and maximal metabolic rates than sham-treated fish, but the effect of cortisol treatment on aerobic scope was negligible. Indices of energy synthesis/mobilization, including blood glucose concentrations, hepatosomatic index, hepatic glycogen concentrations, and ammonia excretion rates, were higher in cortisol-treated fish compared with controls. Our work suggests that although aerobic scope was not diminished by prolonged elevation of cortisol levels, higher metabolic expenditures may be of detriment to the animal’s performance in the longer term.


Teleost Metabolism Aerobic scope Stress Gluconeogenesis Protein catabolism 



The authors would like to thank the Queen’s University Biological Station staff and various members of the Cooke Lab in facilitating this research. We would also like to thank Alexander M. Zimmer and Brett Culbert for their input and assistance in sample analysis.

Author contributions

All authors contributed to the design of the experiment. The experimental series were conducted by M.J.L. and A.J.Z. Assays and data analysis were performed by M.J.L. with help from E.J.E., D.L., C.B., and K.M.G. The manuscript was written by M.J.L. with all authors contributing to revisions.


M.J.L. and C.B. are supported by NSERC PGS-D. A.J.Z. is supported by the Queen Elizabeth II Scholarship. S.J.C. and K.M.G. are supported by an NSERC discovery grant. S.J.C. is further supported by the Canada Research Chairs program.

Supplementary material

10695_2019_680_MOESM1_ESM.docx (70 kb)
ESM 1 (DOCX 78.1 KB)


  1. Algera DA, Brownscombe JW, Gilmour KM, Lawrence MJ, Zolderdo AJ, Cooke SJ (2017a) Cortisol treatment affects locomotor activity and swimming behaviour of male smallmouth bass engaged in paternal care: a field study using acceleration biologgers. Physiol Behav 181:59–68CrossRefPubMedGoogle Scholar
  2. Algera DA, Gutowsky LF, Zolderdo AJ, Cooke SJ (2017b) Parental care in a stressful world: experimentally elevated cortisol and brood size manipulation influence nest success probability and nest-tending behavior in a wild teleost. Fish Physiol Biochem Zool 90(1):85–95CrossRefPubMedGoogle Scholar
  3. Aluru N, Vijayan MM (2009) Stress transcriptomics in fish: a role for genomic cortisol signaling. Gen Comp Endocrinol 164(2):142–150CrossRefPubMedGoogle Scholar
  4. Baltzegar DA, Reading BJ, Douros JD, Borski RJ (2014) Role for leptin in promoting glucose mobilization during acute hyperosmotic stress in teleost fishes. J Endocrinol 220(1):61–72CrossRefPubMedGoogle Scholar
  5. Barton BA (2002) Stress in fishes: a diversity of responses with particular reference to changes in circulating corticosteroids. Integr Comp Biol 42(3):517–525CrossRefPubMedGoogle Scholar
  6. Barton BA, Iwama GK (1991) Physiological changes in fish from stress in aquaculture with emphasis on the response and effects of corticosteroids. Annu Rev Fish Dis 1:3–26CrossRefGoogle Scholar
  7. Barton BA, Schreck CB (1987) Metabolic cost of acute physical stress in juvenile steelhead. Trans Am Fish Soc 116(2):257–263CrossRefGoogle Scholar
  8. Basu N, Nakano T, Grau EG, Iwama GK (2001) The effects of cortisol on heat shock protein 70 levels in two fish species. Gen Comp Endocrinol 124(1):97–105CrossRefPubMedGoogle Scholar
  9. Bergmeyer H (1974) Determination with hexokinase and glucose-6-phosphate dehydrogenase. In: Bergmeyer HU, Gawehn K (eds) Methods of enzymatic analysis, vol 3. Academic Press, Cambridge, pp 1196–1201Google Scholar
  10. Bernier NJ, Bedard N, Peter RE (2004) Effects of cortisol on food intake, growth, and forebrain neuropeptide Y and corticotropin-releasing factor gene expression in goldfish. Gen Comp Endocrinol 135(2):230–240CrossRefPubMedGoogle Scholar
  11. Boonstra R (2013) The ecology of stress: a marriage of disciplines. Funct Ecol 27(1):7–10CrossRefGoogle Scholar
  12. Borowiec BG, Darcy KL, Gillette DM, Scott GR (2015) Distinct physiological strategies are used to cope with constant hypoxia and intermittent hypoxia in killifish (Fundulus heteroclitus). J Exp Biol 218(8):1198–1211CrossRefPubMedGoogle Scholar
  13. Brett JR, Groves TDD (1979) Physiological energetics. In: Hoar W, Randall DJ, Brett JR (eds) Fish physiology, vol VIII. Academic Press, Cambridge, pp 280–352Google Scholar
  14. Breuner CW, Delehanty B, Boonstra R (2013) Evaluating stress in natural populations of vertebrates: total CORT is not good enough. Funct Ecol 27(1):24–36CrossRefGoogle Scholar
  15. Brownscombe JW, Cooke SJ, Algera DA, Hanson KC, Eliason EJ, Burnett NJ, Danylchuk AJ, Hinch SG, Farrell AP (2017) Ecology of exercise in wild fish: integrating concepts of individual physiological capacity, behavior, and fitness through diverse case studies. Integr Comp Biol 57(2):281–292CrossRefPubMedGoogle Scholar
  16. Bucking C (2017) A broader look at ammonia production, excretion, and transport in fish: a review of impacts of feeding and the environment. J Comp Physiol B 187(1):1–18CrossRefPubMedGoogle Scholar
  17. Busacker GP, Adelman IR, Goolish EM (1990) Growth. In: Schreck CB, Moyle PB (eds) Methods for fish biology. American Fisheries Society, Bethesda, pp 363–387Google Scholar
  18. Butler DG (1968) Hormonal control of gluconeogenesis in the North American eel (Anguilla rostrata). Gen Comp Endocrinol 10(1):85–91CrossRefPubMedGoogle Scholar
  19. Carmichael GJ, Tomasso JR, Simco BA, Davis KB (1984) Characterization and alleviation of stress associated with hauling largemouth bass. Trans Am Fish Soc 113(6):778–785CrossRefGoogle Scholar
  20. Chabot D, Steffensen JF, Farrell AP (2016) The determination of standard metabolic rate in fishes. J Fish Biol 88(1):81–121CrossRefPubMedGoogle Scholar
  21. Chan DK, Woo NY (1978) Effect of cortisol on the metabolism of the eel, Anguilla japonica. Gen Comp Endocrinol 35(3):205–215CrossRefPubMedGoogle Scholar
  22. Chrousos GP (2009) Stress and disorders of the stress system. Nature Rev 5(7):374Google Scholar
  23. Clark TD, Jeffries KM, Hinch SG, Farrell AP (2011) Exceptional aerobic scope and cardiovascular performance of pink salmon (Oncorhynchus gorbuscha) may underlie resilience in a warming climate. J Exp Biol 214(18):3074–3081CrossRefPubMedGoogle Scholar
  24. Cook KV, O’Connor CM, McConnachie SH, Gilmour KM, Cooke SJ (2012) Condition dependent intra-individual repeatability of stress-induced cortisol in a freshwater fish. Comp Biochem Physiol A 161(3):337–343CrossRefGoogle Scholar
  25. Crans, K. D., Pranckevicius, N. A., & Scott, G. R. (2015). Physiological tradeoffs may underlie the evolution of hypoxia tolerance and exercise performance in sunfish (Centrarchidae). J Exp Biol, 218(20): 3264–3275Google Scholar
  26. Crossin GT, Love OP, Cooke SJ, Williams TD (2016) Glucocorticoid manipulations in free-living animals: considerations of dose delivery, life-history context and reproductive state. Funct Ecol 30(1):116–125CrossRefGoogle Scholar
  27. Davis KB, Parker NC (1986) Plasma corticosteroid stress response of fourteen species of warmwater fish to transportation. Trans Am Fish Soc 115(3):495–499CrossRefGoogle Scholar
  28. De Boeck G, Alsop D, Wood C (2001) Cortisol effects on aerobic and anaerobic metabolism, nitrogen excretion, and whole-body composition in juvenile rainbow trout. Physiol Biochem Zool 74(6):858–868CrossRefPubMedGoogle Scholar
  29. DiBattista JD, Anisman H, Whitehead M, Gilmour KM (2005) The effects of cortisol administration on social status and brain monoaminergic activity in rainbow trout Oncorhynchus mykiss. J Exp Biol 208(14):2707–2718Google Scholar
  30. Eliason EJ, Farrell AP (2016) Oxygen uptake in Pacific salmon Oncorhynchus spp.: when ecology and physiology meet. J Fish Biol 88(1):359–388CrossRefPubMedGoogle Scholar
  31. Eliason EJ, Clark TD, Hague MJ, Hanson LM, Gallagher ZS, Jeffries KM, Gale MK, Patterson DA, Hinch SG, Farrell AP (2011) Differences in thermal tolerance among sockeye salmon populations. Science 332(6025):109–112CrossRefPubMedGoogle Scholar
  32. Farrell AP, Eliason EJ, Sandblom E, Clark TD (2009) Fish cardiorespiratory physiology in an era of climate change. Can J Zool 87(10):835–851CrossRefGoogle Scholar
  33. Farrell AP, Eliason EJ, Clark TD, Steinhausen MF (2014) Oxygen removal from water versus arterial oxygen delivery: calibrating the Fick equation in Pacific salmon. J Comp Physiol B 184:855–864CrossRefPubMedGoogle Scholar
  34. Farrell, A. P., MacLeod, K. R., & Scott, C. (1988). Cardiac performance of the trout (Salmo gairdneri) heart during acidosis: effects of low bicarbonate, lactate and cortisol. Comp Biochem Physiol A Physiol 91(2):271–277Google Scholar
  35. Faught E, Vijayan MM (2016) Mechanisms of cortisol action in fish hepatocytes. Comp Biochem Physiol B 199:136–145CrossRefPubMedGoogle Scholar
  36. Foster GD, Moon TW (1986) Cortisol and liver metabolism of immature American eels, Anguilla rostrata (LeSueur). Fish Physiol Biochem 1(2):113–124CrossRefPubMedGoogle Scholar
  37. Fry FEJ (1947) Effects of the environment on animal activity. Publ Ontario Fish Res Lab 68:1–52Google Scholar
  38. Fry F, Hart JS (1948) The relation of temperature to oxygen consumption in the goldfish. Biol Bull 94(1):66–77CrossRefPubMedGoogle Scholar
  39. Gamperl AK, Vijayan MM, Boutilier RG (1994) Experimental control of stress hormone levels in fishes: techniques and applications. Rev Fish Biol Fish 4(2):215–255CrossRefGoogle Scholar
  40. Godin JGJ (1997) Evading predators. In: Godin JGJ (ed) Behavioural ecology of teleost fishes. Oxford University Press, Oxford, pp 191–236Google Scholar
  41. Gregory TR, Wood CM (1999) The effects of chronic plasma cortisol elevation on the feeding behaviour, growth, competitive ability, and swimming performance of juvenile rainbow trout. Physiol Biochem Zool 72(3):286–295CrossRefPubMedGoogle Scholar
  42. Guderley H, Pörtner HO (2010) Metabolic power budgeting and adaptive strategies in zoology: examples from scallops and fish. Can J Zool 88(8):753–763CrossRefGoogle Scholar
  43. Gustaveson AW, Wydoski RS, Wedemeyer GA (1991) Physiological response of largemouth bass to angling stress. Trans Am Fish Soc 120(5):629–636CrossRefGoogle Scholar
  44. Hawlena D, Schmitz OJ (2010) Physiological stress as a fundamental mechanism linking predation to ecosystem functioning. Am Nat 176(5):537–556CrossRefPubMedGoogle Scholar
  45. Herrera M, Aragão A, Hachero I, Ruiz-Jarabo I, Vargas-Chacoff L, Mancera JM, Conceição L (2012) Physiological short-term response to sudden salinity change in the Senegalese sole (Solea senegalensis). Fish Physiol Biochem 38:1741–1751CrossRefPubMedGoogle Scholar
  46. Herrera M, Ruiz-Jarabo I, Vargas-Chacoff L, De La Roca E, Mancera JM (2015) Metabolic enzyme activities in relation to crowding stress in the wedge sole (Dicologoglossa cuneata). Aquac Res 46:2808–2818CrossRefGoogle Scholar
  47. Hoogenboom MO, Armstrong JD, Miles MS, Burton T, Groothuis TG, Metcalfe NB (2011) Implantation of cocoa butter reduces egg and hatchling size in Salmo trutta. J Fish Biol 79(3):587–596CrossRefPubMedGoogle Scholar
  48. Hopkins TE, Wood CM, Walsh PJ (1995) Interactions of cortisol and nitrogen metabolism in the ureogenic gulf toadfish Opsanus beta. J Exp Biol 198(10):2229–2235PubMedGoogle Scholar
  49. Inui Y, Yokote M (1975) Gluconeogenesis in the eel-IV gluconeogenesis in the hydrocortisone-administered eel. Bull Jap Soc Scient Fish 41:973–981CrossRefGoogle Scholar
  50. Jentoft S, Aastveit AH, Torjesen PA, Andersen Ø (2005) Effects of stress on growth, cortisol and glucose levels in non-domesticated Eurasian perch (Perca fluviatilis) and domesticated rainbow trout (Oncorhynchus mykiss). Comp Biochem Physiol A 141(3):353–358CrossRefGoogle Scholar
  51. Johansen IB, Lunde IG, Røsjø H, Christensen G, Nilsson GE, Bakken M, Øverli Ø (2011) Cortisol response to stress is associated with myocardial remodeling in salmonid fishes. J Exp Biol 214(8):1313–1321CrossRefPubMedGoogle Scholar
  52. Johansen IB, Sandblom E, Skov PV, Gräns A, Ekström A, Lunde IG et al (2017) Bigger is not better: cortisol-induced cardiac growth and dysfunction in salmonids. J Exp Biol 220(14):2545–2553CrossRefPubMedGoogle Scholar
  53. Johnston, I. A. (1981). Structure and function of fish muscles. Symp Zool Soc Lond 48:71–113.Google Scholar
  54. Keppler D, Decker K (1974) Glycogen: determination with amyloglucosidase. In: Bergmeyer HU (ed) Methods of enzymatic analysis. Academic Press, New York, pp 1127–1131Google Scholar
  55. Laiz-Carrión R, Sangiao-Alvarellos S, Guzmán JM, Del Río MPM, Míguez JM, Soengas JL, Mancera JM (2002) Energy metabolism in fish tissues related to osmoregulation and cortisol action. Fish Physiol Biochem 27(3–4):179–188CrossRefGoogle Scholar
  56. Laiz-Carrión R, Del Río MPM, Miguez JM, Mancera JM, Soengas JL (2003) Influence of cortisol on osmoregulation and energy metabolism in gilthead seabream Sparus aurata. J Exp Zool A 298(2):105–118CrossRefGoogle Scholar
  57. Lankford SE, Adams TE, Miller RA, Cech JJ Jr (2005) The cost of chronic stress: impacts of a nonhabituating stress response on metabolic variables and swimming performance in sturgeon. Physiol Biochem Zool 78(4):599–609CrossRefPubMedGoogle Scholar
  58. Lawrence MJ, Wright PA, Wood CM (2015) Physiological and molecular responses of the goldfish (Carassius auratus) kidney to metabolic acidosis, and potential mechanisms of renal ammonia transport. J Exp Biol 218(13):2124–2135CrossRefPubMedGoogle Scholar
  59. Lawrence MJ, Eliason EJ, Brownscombe JW, Gilmour KM, Mandelman JW, Cooke SJ (2017) An experimental evaluation of the role of the stress axis in mediating predator-prey interactions in wild marine fish. Comp Biochem Physiol A 207:21–29CrossRefGoogle Scholar
  60. Lawrence M, Jain-Schlaepfer S, Zolderdo A, Algera D, Gilmour K, Gallagher A, Cooke SJ (2018) Are 3-minutes good enough for obtaining baseline physiological samples from teleost fish. Can J Zool 96:774–786CrossRefGoogle Scholar
  61. Lawrence MJ, Zolderdo AJ, Godin JGJ, Mandelman JW, Gilmour KM, Cooke SJ (2019) Cortisol does not increase risk of mortality to predation in juvenile bluegill sunfish: a manipulative experimental field study. J Exp Zool A 331:253–261CrossRefGoogle Scholar
  62. Lee CG, Farrell AP, Lotto A, Hinch SG, Healey MC (2003) Excess post-exercise oxygen consumption in adult sockeye (Oncorhynchus nerka) and coho (O kisutch) salmon following critical speed swimming. J Exp Biol 206(18):3253–3260CrossRefPubMedGoogle Scholar
  63. Leung LY, Woo NY (2010) Effects of growth hormone, insulin-like growth factor I, triiodothyronine, thyroxine, and cortisol on gene expression of carbohydrate metabolic enzymes in sea bream hepatocytes. Comp Biochem Physiol A 157(3):272–282CrossRefGoogle Scholar
  64. Liew HJ, Chiarella D, Pelle A, Faggio C, Blust R, De Boeck G (2013) Cortisol emphasizes the metabolic strategies employed by common carp, Cyprinus carpio at different feeding and swimming regimes. Comp Biochem Physiol A 166(3):449–464CrossRefGoogle Scholar
  65. Liew HJ, Fazio A, Faggio C, Blust R, De Boeck G (2015) Cortisol affects metabolic and ionoregulatory responses to a different extent depending on feeding ration in common carp, Cyprinus carpio. Comp Biochem Physiol A 189:45–57CrossRefGoogle Scholar
  66. Lim CB, Chew SF, Anderson PM, Ip YK (2001) Reduction in the rates of protein and amino acid catabolism to slow down the accumulation of endogenous ammonia: a strategy potentially adopted by mudskippers (Periophthalmodon schlosseri and Boleophthalmus boddaerti) during aerial exposure in constant darkness. J Exp Biol 204(9):1605–1614PubMedGoogle Scholar
  67. Lima SL, Dill LM (1990) Behavioral decisions made under the risk of predation: a review and prospectus. Can J Zool 68(4):619–640CrossRefGoogle Scholar
  68. Madison BN, Tavakoli S, Kramer S, Bernier NJ (2015) Chronic cortisol and the regulation of food intake and the endocrine growth axis in rainbow trout. J Endocrinol 226(2):103–119CrossRefPubMedGoogle Scholar
  69. Madliger CL, Franklin CE, Hultine KR, van Kleunen M, Lennox RJ, Love OP, Rummer JL, Cooke SJ (2017) Conservation physiology and the quest for a “good” Anthropocene. Conserv Physiol.
  70. McConnachie SH, O’Connor CM, Gilmour KM, Iwama GK, Cooke SJ (2012) Supraphysiological cortisol elevation alters the response of wild bluegill sunfish to subsequent stressors. J Exp Zool A 317(5):321–332CrossRefGoogle Scholar
  71. McDonald MD, Wood CM (2004) The effect of chronic cortisol elevation on urea metabolism and excretion in the rainbow trout (Oncorhynchus mykiss). J Comp Physiol B 174(1):71–81CrossRefPubMedGoogle Scholar
  72. Mesa MG, Poe TP, Gadomski DM, Petersen J (1994) Are all prey created equal? A review and synthesis of differential predation on prey in substandard condition. J Fish Biol 45:81–96CrossRefGoogle Scholar
  73. Metcalfe NB (1986) Intraspecific variation in competitive ability and food intake in salmonids: consequences for energy budgets and growth rates. J Fish Biol 28(5):525–531CrossRefGoogle Scholar
  74. Milligan CL (2003) A regulatory role for cortisol in muscle glycogen metabolism in rainbow trout Oncorhynchus mykiss. Walbaum J Exp Biol 206(18):3167–3173CrossRefPubMedGoogle Scholar
  75. Mommsen TP, French CJ, Hochachka PW (1980) Sites and patterns of protein and amino acid utilization during the spawning migration of salmon. Can J Zool 58(10):1785–1799CrossRefGoogle Scholar
  76. Mommsen TP, Vijayan MM, Moon TW (1999) Cortisol in teleosts: dynamics, mechanisms of action, and metabolic regulation. Rev Fish Biol Fish 9(3):211–268CrossRefGoogle Scholar
  77. Momoda TS, Schwindt AR, Feist GW, Gerwick L, Bayne CJ, Schreck CB (2007) Gene expression in the liver of rainbow trout, Oncorhynchus mykiss, during the stress response. Comp Biochem Physiol D 2(4):303–315Google Scholar
  78. Morgan JD, Iwama GK (1996) Cortisol-induced changes in oxygen consumption and ionic regulation in coastal cutthroat trout (Oncorhynchus clarki clarki) parr. Fish Physiol Biochem 15(5):385–394CrossRefPubMedGoogle Scholar
  79. Nawata CM, Wood CM (2009) mRNA expression analysis of the physiological responses to ammonia infusion in rainbow trout. J Comp Physiol 179(7):799–810CrossRefGoogle Scholar
  80. Norin T, Clark TD (2016) Measurement and relevance of maximum metabolic rate in fishes. J Fish Biol 88(1):122–151CrossRefPubMedGoogle Scholar
  81. Norin T, Malte H, Clark TD (2014) Aerobic scope does not predict the performance of a tropical eurythermal fish at elevated temperatures. J Exp Biol 217(2):244–251CrossRefPubMedGoogle Scholar
  82. O’Connor CM, Gilmour KM, Arlinghaus R, Van Der Kraak G, Cooke SJ (2009) Stress and parental care in a wild teleost fish: insights from exogenous supraphysiological cortisol implants. Physiol Biochem Zool 82(6):709–719CrossRefPubMedGoogle Scholar
  83. O’Connor CM, Gilmour KM, Arlinghaus R, Matsumura S, Suski CD, Philipp DP, Cooke SJ (2010) The consequences of short-term cortisol elevation on individual physiology and growth rate in wild largemouth bass (Micropterus salmoides). Can J Fish Aquat Sci 68(4):693–705CrossRefGoogle Scholar
  84. Overli O, Kotzian S, Winberg S (2002) Effects of cortisol on aggression and locomotor activity in rainbow trout. Horm Behav 42(1):53–61CrossRefPubMedGoogle Scholar
  85. Pankhurst NW (2016) Reproduction and development. In: Schreck CB, Tort L, Farrell AP, Brauner CJ (eds) Fish physiology, vol 35. Academic Press, Cambridge, pp 295–331Google Scholar
  86. Perry SF, Capaldo A (2011) The autonomic nervous system and chromaffin tissue: neuroendocrine regulation of catecholamine secretion in non-mammalian vertebrates. Auton Neurosci 165(1):54–66CrossRefPubMedGoogle Scholar
  87. Perry SF, Reid SD (1993) β-Adrenergic signal transduction in fish: interactive effects of catecholamines and cortisol. Fish Physiol Biochem 11:195–203CrossRefPubMedGoogle Scholar
  88. Pickering AD, Pottinger TG (1989) Stress responses and disease resistance in salmonid fish: effects of chronic elevation of plasma cortisol. Fish Physiol Biochem 7(1):253–258CrossRefPubMedGoogle Scholar
  89. Pickering AD, Pottinger TG, Christie P (1982) Recovery of the brown trout, Salmo trutta L, from acute handling stress: a time-course study. J Fish Biol 20(2):229–244CrossRefGoogle Scholar
  90. Reid SD, Moon TW, Perry SF (1992) Rainbow trout hepatocyte beta-adrenoceptors, catecholamine responsiveness, and effects of cortisol. Am J Phys 262(5):R794–R799Google Scholar
  91. Reid SG, Vijayan MM, Perry SF (1996) Modulation of catecholamine storage and release by the pituitary-interrenal axis in the rainbow trout, Oncorhynchus mykiss. J Comp Physiol B 165(8):665–676CrossRefPubMedGoogle Scholar
  92. Romero LM, Dickens MJ, Cyr NE (2009) The reactive scope model—a new model integrating homeostasis, allostasis, and stress. Horm Behav 55(3):375–389CrossRefPubMedGoogle Scholar
  93. Sadoul B, Vijayan MM (2016) Stress and growth. In: Schreck CB, Tort L, Farrell AP, Brauner CJ (eds) Fish physiology, vol 35. Academic Press, Cambridge, pp 167–205Google Scholar
  94. Sapolsky RM, Romero LM, Munck AU (2000) How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocr Rev 21(1):55–89Google Scholar
  95. Schreck CB, Tort L (2016) The concept of stress in fish. In: Schreck CB, Tort L, Farrell AP, Brauner CJ (eds) Fish physiology, vol 35. Academic Press, Cambridge, pp 1–34Google Scholar
  96. Serra-Llinares RM, Tveiten H (2012) Evaluation of a fast and simple method for measuring plasma lactate levels in Atlantic cod, Gadus morhua (L). Int J Fish Aquacult 4(11):217–220Google Scholar
  97. Sloman KA, Motherwell G, O’Connor K, Taylor AC (2000) The effect of social stress on the standard metabolic rate (SMR) of brown trout, Salmo trutta. Fish Physiol Biochem 23(1):49–53CrossRefGoogle Scholar
  98. Sloman KA, Desforges PR, Gilmour KM (2001) Evidence for a mineralocorticoid-like receptor linked to branchial chloride cell proliferation in freshwater rainbow trout. J Exp Biol 204(22):3953–3961PubMedGoogle Scholar
  99. Smith HW (1929) The excretion of ammonia and urea by the gills of fish. J Biol Chem 81(3):727–742Google Scholar
  100. Soivio A, Oikari A (1976) Haematological effects of stress on a teleost, Esox lucius L. J Fish Biol 8(5):397–411CrossRefGoogle Scholar
  101. Sokolova IM (2013) Energy-limited tolerance to stress as a conceptual framework to integrate the effects of multiple stressors. Integr Comp Biol 53(4):597–608CrossRefPubMedGoogle Scholar
  102. Sopinka NM, Patterson LD, Redfern JC, Pleizier NK, Belanger CB, Midwood JD, Crossin GT, Cooke SJ (2015) Manipulating glucocorticoids in wild animals: basic and applied perspectives. Conserv Physiol 3(1).
  103. Sopinka NM, Donaldson MR, O’Connor CM, Suski CD, Cooke SJ (2016) Stress indicators in fish. In: Schreck CB, Tort L, Farrell AP, Brauner CJ (eds) Fish physiology, vol 35. Academic Press, Cambridge, pp 405–462Google Scholar
  104. Stoot LJ, Cairns NA, Cull F, Taylor JJ, Jeffrey JD, Morin F, Mandelman JW, Clark TD, Cooke SJ (2014) Use of portable blood physiology point-of-care devices for basic and applied research on vertebrates: a review. Conserv Physiol 2(1).
  105. Storer JH (1967) Starvation and the effects of cortisol in the goldfish (Carassius auratus L). Comp Biochem Physiol 20(3):939–948CrossRefGoogle Scholar
  106. Suski CD, Killen SS, Morrissey MB, Lund SG, Tufts BL (2003) Physiological changes in largemouth bass caused by live-release angling tournaments in southeastern Ontario. N Am J Fish Manag 23(3):760–769CrossRefGoogle Scholar
  107. Suski CD, Cooke SJ, Danylchuk AJ, O’Connor CM, Gravel MA, Redpath T, Hanson KC, Gingerich AJ, Murchie KJ, Danylchuk SE, Koppelman JB, Goldberg TL (2007) Physiological disturbance and recovery dynamics of bonefish (Albula vulpes), a tropical marine fish, in response to variable exercise and exposure to air. Comp Biochem Physiol A 148(3):664–673CrossRefGoogle Scholar
  108. Torres JJ, Somero GN (1988) Metabolism, enzymic activities and cold adaptation in Antarctic mesopelagic fishes. Mar Biol 98(2):169–180CrossRefGoogle Scholar
  109. Tripathi G, Verma P (2003) Pathway-specific response to cortisol in the metabolism of catfish. Comp Biochem Physiol B 136(3):463–471CrossRefPubMedGoogle Scholar
  110. Tsui TKN, Hung CYC, Nawata CM, Wilson JM, Wright PA, Wood CM (2009) Ammonia transport in cultured gill epithelium of freshwater rainbow trout: the importance of Rhesus glycoproteins and the presence of an apical Na+/NH4+ exchange complex. J Exp Biol 212(6):878–892CrossRefPubMedGoogle Scholar
  111. Verdouw H, Van Echteld CJA, Dekkers EMJ (1978) Ammonia determination based on indophenol formation with sodium salicylate. Water Res 12(6):399–402CrossRefGoogle Scholar
  112. Vijayan MM, Ballantyne JS, Leatherland JF (1991) Cortisol-induced changes in some aspects of the intermediary metabolism of Salvelinus fontinalis. Gen Comp Endocrinol 82(3):476–486CrossRefPubMedGoogle Scholar
  113. Vijayan MM, Pereira C, Grau EG, Iwama GK (1997) Metabolic responses associated with confinement stress in tilapia: the role of cortisol. Comp Biochem Physiol C 116(1):89–95Google Scholar
  114. Vijayan MM, Raptis S, Sathiyaa R (2003) Cortisol treatment affects glucocorticoid receptor and glucocorticoid-responsive genes in the liver of rainbow trout. Gen Comp Endocrinol 132(2):256–263CrossRefPubMedGoogle Scholar
  115. Wells RM, Pankhurst NW (1999) Evaluation of simple instruments for the measurement of blood glucose and lactate, and plasma protein as stress indicators in fish. J World Aquacult Soc 30(2):276–284CrossRefGoogle Scholar
  116. Wendelaar Bonga S (1997) The stress response in fish. Physiol Rev 77(3):591–625CrossRefPubMedGoogle Scholar
  117. Wilson R, Wright P, Munger S, Wood C (1994) Ammonia excretion in freshwater rainbow trout (Oncorhynchus mykiss) and the importance of gill boundary layer acidification: lack of evidence for Na+/NH4+ exchange. J Exp Biol 191(1):37–58PubMedGoogle Scholar
  118. Wilson AD, Binder TR, McGrath KP, Cooke SJ, Godin JGJ (2011) Capture technique and fish personality: angling targets timid bluegill sunfish, Lepomis macrochirus. Can J Fish Aquat Sci 68(5):749–757CrossRefGoogle Scholar
  119. Winberg S, Höglund E, Overli O (2016) Variation in the neuroendocrine stress response. In: Schreck CB, Tort L, Farrell AP, Brauner CJ (eds) Fish physiology, vol 35. Academic Press, Cambridge, pp 35–74Google Scholar
  120. Wiseman S, Osachoff H, Bassett E, Malhotra J, Bruno J, VanAggelen G, Vijayan MM (2007) Gene expression pattern in the liver during recovery from an acute stressor in rainbow trout. Comp Biochem Physiol D 2(3):234–244Google Scholar
  121. Wood CM, Milligan CL, Walsh PJ (1999) Renal responses of trout to chronic respiratory and metabolic acidosis and metabolic alkalosis. Am J Phys 277(2):R482–R492Google Scholar
  122. Wood CM, Kajimura M, Sloman KA, Scott GR, Wals PJ, Almeida-Val VM, Val AL (2007) Rapid regulation of Na+ fluxes and ammonia excretion in response to acute environmental hypoxia in the Amazonian oscar, Astronotus ocellatus. Am J Phys 292(5):R2048–R2058Google Scholar
  123. Wright PA (1995) Nitrogen excretion: three end products, many physiological roles. J Exp Biol 198(2):273–281PubMedGoogle Scholar
  124. Wright PA, Wood CM (2009) A new paradigm for ammonia excretion in aquatic animals: role of Rhesus (Rh) glycoproteins. J Exp Biol 212(15):2303–2312CrossRefPubMedGoogle Scholar
  125. Yada T, Tort L (2016) Stress and disease resistance: immune system and immunoendocrine interactions. In: Schreck CB, Tort L, Farrell AP, Brauner CJ (eds) Fish physiology, vol 35. Academic Press, Cambridge, pp 365–403Google Scholar
  126. Zimmer AM, Nawata CM, Wood CM (2010) Physiological and molecular analysis of the interactive effects of feeding and high environmental ammonia on branchial ammonia excretion and Na+ uptake in freshwater rainbow trout. J Comp Physiol B 180(8):1191–1204CrossRefPubMedGoogle Scholar
  127. Zolderdo AJ, Algera DA, Lawrence MJ, Gilmour KM, Fast MD, Thuswaldner J, Willmore WG, Cooke SJ (2016) Stress, nutrition and parental care in a teleost fish: exploring mechanisms with supplemental feeding and cortisol manipulation. J Exp Biol 219(8):1237–1248CrossRefPubMedGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Fish Ecology and Conservation Physiology Laboratory, Department of BiologyCarleton UniversityOttawaCanada
  2. 2.Department of Ecology, Evolution & Marine BiologyUniversity of CaliforniaSanta BarbaraUSA
  3. 3.Queen’s University Biological StationQueen’s UniversityElginCanada
  4. 4.St. Lawrence River Institute of Environmental SciencesCornwallCanada
  5. 5.Department of BiologyUniversity of OttawaOttawaCanada

Personalised recommendations