Cortisol and finfish welfare

Tim Ellis1, Hijran Yavuzcan Yıldız2, José Fernando López‐Olmeda3, María Teresa Spedicato4, L. Tort5, Øyvind Øverli6, Catarina I.M. Martins7
1Cefas Weymouth Laboratory, Dorset, UK
2Department of Fisheries and Aquaculture, Ankara University, Ankara, Turkey
3Department of Physiology, Faculty of Biology, University of Murcia, Murcia, Spain
4COISPA, Stazione Sperimentale per lo Studio delle Risorse del Mare, 70126, Bari, Italy
5Unit de Fisiología Animal, Faculty of Biosciences, Department of Cell Biology, Physiology and Immunology, Universitat Autonoma de Barcelona, Bellaterra, Spain
6Department of Animal and Aquacultural Sciences, Norwegian University of Life Sciences, Aas, Norway
7CCMAR, Centro de Ciências do Mar, Universidade do Algarve, Campus de Gambelas, 8005-139 Faro, Portugal

Tóm tắt

Từ khóa


Tài liệu tham khảo

Abbink W, Bevelander GS, Rotllant J, Canario AVM, Flik G (2004) Calcium handling in Sparus auratus: effects of water and dietary calcium levels on mineral composition, cortisol and PTHrP levels. J Environ Biol 207:4077–4084

Abrous DN, Wojtowicz JM (2008) Neurogenesis and hippocampal memory system. In: Gage FH, Kempermann G, Song HJ (eds) Adult neurogenesis. Cold Spring Harbour Laboratory Press, Could Spring Harbour, pp 445–461

Almazán-Rueda P, Van Helmond ATM, Verreth JAJ, Schrama JW (2005) Photoperiod affects growth, behaviour and stress variables in Clarias gariepinus. J Fish Biol 67:1029–1039

Aluru N, Vijayan MM (2009) Stress transcriptomics in fish: a role for genomic cortisol signalling. Gen Comp Endocrinol 164:142–150

Alvarellos S, Arjona FJ, Martin del Rio MP, Miguez JM, Mancera JM, Soengas JL (2005) Time course of osmoregulatory and metabolic changes during osmotic acclimation in Sparus auratus. J Exp Biol 208:4291–4304

Alvarellos SS, Polakof S, Arjona FJ, Kleszynska A, Martin del Rio PM, Miguez JM, Soengas JL, Mancera JM (2006) Osmoregulatory and metabolic changes in the gilthead sea bream Sparus auratus after arginine vasotocin (AVT) treatment. Gen Comp Endocrinol 148:348–358

Andersen DE, Reid SD, Moon TW, Perry SF (1991) Metabolic effects associated with chronically elevated cortisol in rainbow trout (Oncorhynchus mykiss). Can J Fish Aquat Sci 48:1811–1817

Anderson DP (1990) Immunological indicators: effects of environmental stress on immune protection and disease outbreaks. Am Fish Soc Symp 8:38–50

Anon (1992) FAWC updates the five freedoms. Vet Rec 131:357

Anon (2009) Scientific opinion of the panel on animal health and welfare on a request from European Commission on general approach to fish welfare and to the concept of sentience in fish. EFSA J 954:1–26

Arends RJ, Mancera JM, Munoz JL, Wendelaar Bonga SE (1999) The stress response of the gilthead seabream (Sparus aurata L.) to air exposure and confinement. J Endocrinol 163:149–157

Arlinghaus R, Cooke SJ, Schwab A, Cowx IG (2007) Fish welfare: a challenge to the feelings-based approach, with implications for recreational fishing. Fish Fish 8:57–71

Arlinghaus R, Schwab A, Cooke SJ, Cowx IG (2009) Contrasting pragmatic and suffering-centred approaches to fish welfare in recreational angling. J Fish Biol 75:2448–2463

Barreto RE, Volpato GL, Pottinger TG (2006) The effect of elevated blood cortisol levels on the extinction of a conditioned stress response in rainbow trout. Horm Behav 50:484–488

Barton BA (1997) Stress in finfish: past, present and future—a historical perspective. In: Iwama GK, Pickering AD, Sumpter JP, Schreck CB (eds) Fish stress and health in aquaculture. Cambridge University Press, Cambridge, pp 1–33

Barton BA (2000) Salmonid fishes differ in their cortisol and glucose responses to handling and transport stress. N Am J Aquacult 62:12–18

Barton BA (2002) Stress in fishes: a diversity of responses with particular reference to changes in circulating corticosteroids. Int Comp Biol 42:517–525

Barton BA, Iwama GK (1991) Physiological changes in fish from stress in aquaculture with emphasis on the response and effects of corticosteroids. Ann Rev Fish Dis 1:3–26

Barton BA, Peter RE (1982) Plasma cortisol response in fingerling rainbow trout, Salmo gairdneri Richardson, to various transport conditions, anaesthesia, and cold shock. J Fish Biol 20:39–51

Barton BA, Toth LT (1980) Physiological stress in fish: a literature review with emphasis on cortisol dynamics. Fish Res Rep Fish Wildl Div 20:1–19

Barton BA, Schreck CB, Barton LD (1987) Effects of chronic cortisol administration and daily acute stress on growth, physiological conditions, and stress responses in juvenile rainbow trout. Dis Aquat Org 2:173–185

Barton BA, Morgan JD, Vijayan MM (2002) Physiological and condition-related indicators of environmental stress in fish. In: Adams SM (ed) Biological indicators of aquatic ecosystem stress. Am Fish Soc, Bethesda, Maryland, pp 111–148

Barton BA, Ribas L, Acerete L, Tort L (2005) Effects of chronic confinement on physiological responses of juvenile gilthead sea bream, Sparus aurata L., to acute handling. Aqua Res 36:172–179

Belanoff JK, Gross K, Yager A, Schatzberg AF (2001) Corticosteroids and cognition. J Psych Res 35:127–145

Bender N, Heg-Bachar Z, Oliveira RF, Canario AVM, Taborsky M (2008) Hormonal control of brood care and social status in a cichlid fish with brood care helpers. Physiol Behav 94:349–358

Bernier NJ (2006) The corticotropin-releasing factor system as a mediator of the appetite-suppressing effects of stress in fish. Gen Comp Endocrinol 146:45–55

Bernier NJ, Lin X, Peter RE (1999) Differential expression of corticotropin-releasing factor (CRF) and urotensin I precursor genes, and evidence of CRF gene expression regulated by cortisol in goldfish brain. Gen Comp Endocrinol 116:461–477

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 135:230–240

Bishop JD, Malven PV, Singleton WL, Weesner GD (1999) Hormonal and behavioral correlates of emotional states in sexually trained boars. J Animal Sci 77:3339–3345

Boissy A, Manteuffel G, Jensen MB, Moe RO, Spruijt B, Keeling LJ, Winckler C, Forkman B, Dimitrov I, Langbein J, Bakken M, Veissier I, Aubert A (2007) Assessment of positive emotions in animals to improve their welfare. Physiol Behav 92:375–397

Braithwaite VA, Boulcott P (2007) Pain perception, aversion and fear in fish. Dis Aquat Org 75:131–138

Braithwaite VA, Huntingford FA (2004) Fish and welfare: do fish have the capacity for pain perception and suffering? Animal Welfare 13:S87–S92

Broom DM (2007) Cognitive ability and sentience: which aquatic animals should be protected? Dis Aquat Org 75:99–108

Cameron HA, Gould E (1994) Adult neurogenesis is regulated by adrenal steroids in the dentate gyrus. Neuroscience 61:203–209

Carbonara P, Corsi I, Focardi S, Lembo G, Rochira S, Scolamacchia M, Spedicato MT, McKinley RS (2010) The effects of stress induced by cortisol administration on the repeatability of swimming performance tests in the European sea bass (Dicentrarchus labrax L.). Mar Freshwater Behav Physiol 43:283-296. doi: 10.1080/10236244.2010.504046

Carpenter RE, Summers CH (2009) Learning strategies during fear conditioning. Neurobiol Learn Mem 91:415–423

Carragher JF, Sumpter JP (1990) Corticosteroid physiology in fish. In: Epple A, Scanes CG, Stetson MH (eds) Progress in comparative endocrinology. Wiley Liss, New York, pp 487–492

Carragher JF, Sumpter JP, Pottinger TG, Pickering AD (1989) The deleterious effects of cortisol implantation on reproductive function in two species of trout, Salmo trutta L. and Salmo gairdneri Richardson. Gen Comp Endocrinol 76:310–321

Carrion RL, Alvareollos S, Guzman JM, Martin del Rio M, Miguez JM, Soengas JL, Mancera JM (2002) Energy metabolism in fish tissues related to osmoregulation and cortisol action. Fish Physiol Biochem 27:179–188

Caruso G, Genovese L, Maracchiolo G, Mogica A (2005) Haematological biochemical and immunological parameters as stress indicators in Dicentrarchus labrax and Sparus aurata farmed in off-shore cages. Aquac Int 13:67–73

Casamitjana J (2004) Aquatic zoos: a critical study of UK public aquaria in the year 2004. Captive Animals’ Protection Society, p 136

CCAC: Canadian Council on Animal Care (2005) Guidelines on: the care and use of fish in research, teaching and testing. 94 pp. ( http://ccac.ca/Documents/Standards/Guidelines/Fish.pdf )

Cerdá-Reverter JM, Zanuy S, Carrillo M, Madrid JA (1998) Time-course studies on plasma glucose, insulin, and cortisol in sea bass (Dicentrarchus labrax) held under different photoperiodic regimes. Physiol Behav 64:245–250

Cericato L, Neto JGM, Fagundes M, Kreutz LC, Quevedo RM, Finco J, da Rosa JGS, Koakoski G, Centenaro L, Pottker E, Anziliero D, Barcellos LJG (2008) Cortisol response to acute stress in jundiá Rhamdia quelen acutely exposed to sub-lethal concentrations of agrichemicals. Comp Biochem Physiol C 148:281–286

Chan DKO, Chester Jones I, Mosley W (1968) Pituitary and adrenocorticol factors in the control of water and electrolyte composition of the freshwater European eel (Anguilla anguilla L.). J Endocrinol 42:91–98

Chan DKO, Rankin JC, Chester Jones I (1969) Influences of the adrenal cortex and the corpuscles of Stannius on osmoregulation in the European eel (Anguilla anguilla L.). Gen Comp Endocrinol Suppl 2:342–353

Chandroo KP, Duncan IJH, Moccia RD (2004a) Can fish suffer?: perspectives on sentience, fear and stress. App Anim Behav Sci 86:225–250

Chandroo KP, Yue S, Moccia RD (2004b) An evaluation of current perspectives on consciousness and pain in fishes. Fish Fish 5:281–295

Chrousos GP (1998) Stressors, stress, and neuroendocrine integration of the adaptive response: the 1997 Hans Selye Memorial Lecture. Ann New York Acad Sci 851:311–335

Chrousos GP, Kino T (2009) Glucocorticoid signalling in the cell. Expanding clinical implications to complex human behavioral and somatic disorders. Ann NY Acad Sci 1179:153–166

Davis KB (2006) Management of physiological stress in finfish aquaculture. N Am J Aquacult 68:116–121

Dawkins MS (2006) A user’s guide to animal welfare science. Trends Ecol Evol 21:77–82

de Boeck G, Alsop D, Wood C (2001) Cortisol effect on aerobic and anaerobic metabolism, nitrogen excretion and whole-body composition in juvenile rainbow trout. Physiol Biochem Zool 74(4):858–868

de Kloet ER, Oitzl MS, Joels M (1999) Stress and cognition: are corticosteroids good or bad guys? Trends Neurosci 22:422–426

Di Marco P, Priori A, Finoia MG, Massari A, Mandich A, Marino G (2008) Physiological responses of European sea bass Dicentrarchus labrax to different stocking densities and acute stress challenge. Aquaculture 275:319–328. doi: 10.1016/j.aquaculture.2007.12.012

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 208:2707–2718

Dickmeis Y (2009) Glucocorticoids and the circadian clock. J Endocrinol 200:3–22

Donaldson EM (1981) The pituitary-interrenal axis as an indicator of stress in fish. In: Pickering AD (ed) Stress and fish. Academic Press, New York, pp 11–47

Doyle RE, Fisher AD, Hinch GN, Boissy A, Lee C (2010) Release from restraint generates a positive judgement bias in sheep. App Anim Behav Sci 122:28–34

Dunlap KD, Pelczar PL, Knapp R (2002) Social interactions and cortisol treatment increase the production of aggressive electrocommunication signals in male electric fish, Apteronotus leptorhynchus. Horm Behav 42:97–108

Ellis T, North B, Scott AP, Bromage NR, Porter M, Gadd D (2002) The relationships between stocking density and the welfare of farmed rainbow trout. J Fish Biol 61:493–531

Ellis T, James JD, Stewart C, Scott AP (2004) A non-invasive stress assay based upon measuring cortisol release into the water by rainbow trout. J Fish Biol 65:1233–1252

Ellis T, James JD, Scott AP (2005) Branchial release of free cortisol and melatonin by rainbow trout. J Fish Biol 67:535–540

Ellis T, James J, Fridell F, Sundh H, Sundell K, Scott AP (2007a) Non-invasive measurement of cortisol and melatonin in seawater Atlantic salmon tanks. Aquaculture 272:707–716

Ellis T, Bagwell N, Pond M, Baynes S, Scott AP (2007b) Acute viral and bacterial infections elevate water cortisol concentrations. Aquaculture 272:698–706

Espmark AM, Eriksen MS, Salte R, Braastad BO, Bakken M (2008) A note on pre-spawning maternal cortisol exposure in farmed Atlantic salmon and its impact on the behaviour of offspring in response to a novel environment. App Anim Behav Sci 110:404–409

Fabbri E, Capuzzo A, Moon TW (1998) The role of circulating catecholamines in the regulation of fish metabolism: an overview. Comp Biochem Physiol C 120:177–192

Fanouraki E, Papandroulakis N, Ellis T, Mylonas CC, Scott AP, Pavlidis M (2008) Water cortisol is a reliable indicator of stress in European sea bass, Dicentrarchus labrax. Behaviour 145(SI):1267–1281

Fietta P, Delsante G (2009) Central nervous system effects of natural and synthetic glucocorticoids. Psych Clin Neurosci 63:613–622

Flos R, Reig L, Torres P, Tort L (1988) Primary and secondary stress responses to grading and hauling in rainbow trout, Salmo gairdneri. Aquaculture 71:99–106

Fortner NA, Pickford GE (1982) The effects of hypophysectomy and replacement therapy with prolactin, cortisone, or their combination on the blood of the black bullhead Icatalurus melas. Gen Comp Endocrinol 47:111–119

Galhardo L, Oliveira RF (2009) Psychological stress and welfare in fish. Ann Rev Biomed Sci 11:1–20

Galhardo L, Almeida O, Oliveira RF (2011) The role of predictability in the stress response of a cichlid fish. Physiol Behav 102:367–372

Gilham ID, Baker BI (1985) A black background facilitates the response to stress in teleosts. J Endocrinol 105:99–105

Gornati R, Papis E, Rimoldi S, Terova G, Saroglia M, Bernardini G (2004) Rearing density influences the expression of stress-related genes in sea bass (Dicentrarchus labrax L.) HMG-CoA reductase mRNA. Gene 341:111–118

Grassi Milano E, Basari F, Chimenti C (1997) Adrenocortical and adrenomedullary homologs in eight species of adult and developing teleosts: morphology, histology and immunohistochemistry. Gen Comp Endocrinol 108:483–496

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. Phys Biochem Zool 72:286–295

Heath AG (1995) Water pollution and fish physiology. CRC Press, VPI and State University, Blacksburg 359 pp

Herrero MJ, Martinez FJ, Miguez JM (2007) Response of plasma and gastrointestinal melatonin, plasma cortisol and activity rhythms of European sea bass (Dicentrarchus labrax) to dietary supplementation with tryptophan and melatonin. J Comp Physiol [B] 177: 319–326

Huntingford FA, Adams C, Braithwaite VA, Kadri S, Pottinger TG, Sandöe P, Turnbull JF (2006) Current issues in fish welfare. J Fish Biol 68:332–372

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 Mol Integr Physiol 141:353–358

Kagawa N, Mugiya Y (2000) Exposure of goldfish (Carassius auratus) to bluegills (Lepomis macrochirus) enhances expression of stress protein 70 mRNA in the brains and increases plasma cortisol levels. Zool Sci 17:1061–1066

Kestin SC (1994) Pain and stress in fish. RSPCA, Horsham, West Sussex

Kittilsen S, Schjolden J, Beitnes-Johansen I, Shawa JC, Pottinger TG, Sørensen C, Braastad BO, Bakken M, Øverli Ø (2009) Melanin-based skin spots reflect stress responsiveness in salmonid fish. Hormon Behav 56:292–298

Knapp R, Wingfield JC, Bass AH (1999) Steroid hormones and paternal care in the plainfin midshipman fish (Porichthys notatus). Horm Behav 35:81–89

Koolhaas JM, Korte SM, de Boer SF, van der Vegt BJ, van Reenen CG, Hopster H, de Jong IC, Ruis MAW, Blokhuis HJ (1999) Coping styles in animals: current status in behavior and stress-physiology. Neurosci Biobehav Rev 23:925–935

Korte SM (2001) Corticosteroids in relation to fear, anxiety and psychopathology. Neurosci Biobehav Rev 25:117–142

Korte SM, Olivier B, Koolhaas JM (2007) A new animal welfare concept based on allostasis. Physiol Behav 92:422–428

Kühn ER, Corneillie S, Ollevier F (1986) Circadian variations in plasma osmolality, electrolytes, glucose, and cortisol in carp (Cyprinus carpio). Gen Comp Endocrinol 61:459–468

Laidley CW, Leatherland JF (1988) Cohort sampling, anaesthesia and stocking-density effects on plasma cortisol, thyroid hormone, metabolite and ion levels in rainbow trout, Salmo gairdneri Richardson. J Fish Biol 33:73–88

Laidley CW, Woo PTK, Leatherland JF (1988) The stress-response of rainbow trout to experimental infection with the blood parasite Cryptobia salmositica Katz, 1951. J Fish Biol 32:253–261

Lamba VJ, Goswami SV, Sundararaj BI (1983) Circannual and circadian variations in plasma levels of steroids (cortisol, estradiol-17b, estrone, and testosterone) correlated with the annual gonadal cycle in the catfish, Heteropneustes fossilis (Bloch). Gen Comp Endocrinol 50:205–225

Lankford S, Weber G (2006) Potential roles of intraovarian growth factors during follicle maturation in rainbow trout (Oncorhynchus mykiss). Meeting Abstract

Lankford SE, Adams TE, Cech JJ (2003) Time of day and water temperature modify the physiological stress response in green sturgeon, Acipenser medirostris. Comp Biochem Physiol A 135:291–302

Leatherland JF (1993) Stocking density and cohort sampling effects on endocrine interactions in rainbow trout. Aquacult Int 1:137–156

Levine A, Zagoory-Sharon O, Feldman R, Lewis JG, Weller A (2007) Measuring cortisol in human psychobiological studies. Physiol Behav 90:43–53

Li HW, Brocksen RW (1977) Approaches to the energetic costs of interspecific competition for space by rainbow trout (Salmo gairdneri). J Fish Biol 11:329–341

Li Y, Takei Y (2003) Ambient salinity-dependent effects of homologous natriuretic peptides (ANP, VNP, and CNP) on plasma cortisol level in the eel. Gen Comp Endocrinol 130:317–323

López-Olmeda JF, Montoya A, Oliveira C, Sánchez-Vázquez FJ (2009) Synchronization to light and restricted-feeding schedules of behavioral and humoral daily rhythms in gilthead sea bream (Sparus aurata). Chronobiol Int 26:1389–1408

Lund V, Mejdell CM, Röcklinsberg H, Anthony R, Håstein T (2007) Expanding the moral circle: fish as objects of moral concern. Dis Aquat Org 75:109–118

Marino G, Di Marco P, Mandich A, Finoia MG, Cataudella S (2001) Changes in serum cortisol, metabolites, osmotic pressure and electrolytes in response to different blood sampling procedures in cultured sea bass (Dicentrarchus labrax L.). J Appl Ichthyol 17:115–120

Martins CIM, Schrama JW, Verreth JAJ (2006) The effect of group composition on the welfare of African catfish (Clarias gariepinus). App Anim Behav Sci 97:323–333

Martins CIM, Galhardo L, Noble C, Damsgård B, Spedicato MT, Zupa W, Beauchaud M, Kulczykowska E, Massabuau J-C, Carter T, Planellas SR, Kristiansen T (2011) Behavioural indicators of welfare in farmed fish. Fish Physiol Biochem. doi: 10.1007/s10695-011-9518-8

Mateo JM (2008) Inverted-U shape relationship between cortisol and learning in ground squirrels. Neurobio Learn Memory 89:582–590

Mazeaud MM, Mazeaud F (1981) Adrenergic responses to stress in fish. In: Pickering AD (ed) Stress and fish. Academic Press, London, pp 50–75

Mazeaud MM, Mazeaud F, Donaldson EM (1977) Primary and secondary effects of stress in fish: some new data with a general review. Trans Am Fish Soc 106:201–212

McCormick SD (1996) Effects of growth hormone and insulin-like growth factor I on salinity tolerance and gill Na+, K+-ATPase in Atlantic salmon (Salmo salar): Interactions with cortisol. Gen Comp Endocrinol 101:3–11

McCormick MD (2001) Endocrine control of osmoregulation in Teleost fish. Am Zool 41:781–794. doi: 10.1093/icb/41.4.781

McEwen BS, Wingfield JC (2010) What is in a name? Integrating homeostasis, allostasis and stress. Horm Behav 57:105–116

Metcalfe JD (2009) Welfare in wild-capture marine fisheries. J Fish Biol 75:2855–2861

Mikics E, Kruk MR, Haller J (2004) Genomic and non-genomic effects of glucocorticoids on aggressive behaviour in male rats. Psychoneuroendocrinol 29:618–635

Milligan CL (1996) Metabolic recovery from exhaustive exercise in rainbow trout. Comp Biochem Physiol A 113:51–60. doi: 10.1016/0300-9629(95)02060-8

Milligan CL (2003) A regulatory role of cortisol in muscle glycogen metabolism in rainbow trout Oncorhynchus mykiss Walbaum. J Exp Biol 206:3167–3173. doi: 10.1242/jeb.00538

Milligan CL, Hooke GB, Johnson C (2000) Sustained swimming at low velocity following a bout of exhaustive exercise enhances metabolic recovery in rainbow trout. J Exp Biol 203:921–926

Molinero A, Gómez E, Balasch J, Tort L (1997) Stress by fish removal in the sea bream Sparus aurata: a time course study on the remaining fish in the same tank. J Appl Aquacult 7:1–12

Mommsen TP, Vijayan MM, Monn TW (1999) Cortisol in teleosts: dynamics, mechanisms of action, and metabolic regulation. Rev Fish Biol Fish 9:211–268

Moreira PSA, Volpato GL (2004) Conditioning of stress in Nile tilapia. J Fish Biol 64:961–969

Moreira PSA, Pulman KGT, Pottinger TG (2004) Extinction of a conditioned response in rainbow trout selected for high or low responsiveness to stress. Horm Behav 46:450–457

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 15:385–394

Morgan MJ, Wilson CE, Crim LW (1999) The effect of stress on reproduction in Atlantic cod. J Fish Biol 54:477–488

Mormède P, Andanson S, Aupérin B, Beerda B, Guémené D, Malmkvist J, Manteca X, Manteuffel G, Prunet P, van Reenen CG, Richard S, Veissier I (2007) Exploration of the hypothalamic–pituitary–adrenal function as a tool to evaluate animal welfare. Physiol Behav 92:317–339

Munro AD, Pitcher TJ (1985) Steroid hormones and agonistic behavior in a cichlid teleost, Aequidens pulcher. Hormones Behav 19:353–371

Neave N (2008) Hormones and behaviour: a psychological approach. University Press, Cambridge

Nichols DJ, Weisbart M (1984) Plasma cortisol concentrations in Atlantic salmon, Salmo salar: episodic variations, diurnal change, and short term response to adrenocorticotropic hormone. Gen Comp Endocrinol 56:169–176

Noakes DLG, Leatherland JF (1977) Social dominance and interrenal cell activity in rainbow trout, Salmo gairdneri (Pisces: Salmonidae). Env Biol Fish 2:131–136

North BP, Turnbull JF, Ellis T, Porter MJ, Migaud H, Bron J, Bromage NR (2006) The impact of stocking density on the welfare of rainbow trout (Oncorhynchus mykiss). Aquaculture 255:466–479

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 Zoo 82:709–719

Oliveira RF, Canario AVM, Bshary R (1999) Hormones, behaviour and conservation of littoral fishes: current status and prospects for future research. In: Almada VC, Oliveira RF, Gonçalves EJ (eds) behaviour and conservation of littoral fishes. Instituto Superior de Psicologia Aplicada, Lisbon, pp 149–178

Olla BL, Davis MW, Schreck CB (1992) Comparison of predator avoidance capabilities with corticosteroid levels induced by stress in juvenile coho salmon. Trans Am Fish Soc 121:544–547

Orchinik M (1998) Glucocorticoids, stress and behavior: shifting the timeframe. Hormones Behav 34:320–327

Ortuno J, Esteban MA, Mesequer J (2002a) Effects of phenoxyethanol on the innate immune system of gilthead sea bream (Sparus aurata) exposed to crowding stress. Vet Immunol Immunopathol 89:29–36

Ortuno J, Esteban MA, Mesequer J (2002b) Lack of effect of combining different stressors on innate immune responses of sea bream (Sparus auratus L.). Vet Immunol Immunopathol 84:17–27

Øverli Ø, Pottinger TG, Carrick TR, Øverli E, Winberg S (2001) Brain monoaminergic activity in rainbow trout selected for high and low stress responsiveness. Brain Behav Evol 57:214–224

Øverli Ø, Kotzian S, Winberg S (2002a) Effects of cortisol on aggression and locomotor activity in rainbow trout. Hormones Behav 42:53–61

Øverli Ø, Pottinger TG, Carrick TR, Øverli E, Winberg S (2002b) Differences in behaviour between rainbow trout selected for high- and low-stress responsiveness. J Exp Biol 205:391–395

Øverli Ø, Winberg S, Pottinger TG (2005) Behavioral and neuroendocrine correlates of selection for stress responsiveness in rainbow trout—a review. Int Comp Biol 45:463–474

Øverli Ø, Sørensen C, Pulman KGT, Pottinger TG, Korzan W, Summers CH, Nilsson GE (2007) Evolutionary background for stress-coping styles: relationships between physiological, behavioral, and cognitive traits in non-mammalian vertebrates. Neurosci Biobehav Rev 31:396–412

Pagnotta A, Brooks L, Milligan L (1994) The potential regulatory role of cortisol in the recovery from exhaustive exercise in rainbow trout. Can J Zool 72:2136–2146

Pavlidis M, Greenwood L, Paalavuo M, Mölsa H, Laitinen JT (1999) The effect of photoperiod on diel rhythms in serum melatonin, cortisol, glucose, and electrolytes in the common dentex, Dentex dentex. Gen Comp Endocrinol 113:240–250

Perera TD, Park S, Nemirovskaya Y (2008) Cognitive role of neurogenesis in depression and antidepressant treatment. Neuroscientist 14:326–338

Peruzzi S, Varsamos S, Chatain B, Fauvel C, Menu B, Falguière Sévére A, Flik G (2005) Haematology and physiological characteristics of diploid and triploid sea bass Dicentrarchus labrax L. Aquaculture 244:359–367

Pickering AD (1992) Rainbow trout husbandry: management of the stress response Aquaculture 100:125–139

Pickering AD (1993) Growth and stress in fish production. Aquaculture 111:51–63

Pickering AD, Pottinger TG (1983) Seasonal and diel changes in plasma cortisol levels of the brown trout, Salmo trutta L. Gen Comp Endocrinol 49:232–239

Pickering AD, Pottinger TG (1987a) Poor water quality suppresses the cortisol response of salmonid fish to handling and confinement. J Fish Biol 30:363–374

Pickering AD, Pottinger TG (1987b) Crowding causes prolonged leucopenia in salmonid fish, despite interrenal acclimation. J Fish Biol 30:701–712

Pickering AD, Stewart A (1984) Acclimation of the interrenal tissue of the brown trout, Salmo trutta L., to chronic crowding stress. J Fish Biol 24:731–740

Pickering AD, Schreck C, Maule AG, Kaattari SL, Leatherland J, Farbridge KJ, Vijayan MM, Flett PA, Dickhoff WW (1993) In: Muir JF, Roberts RJ (eds) Stress and adaptation, recent advances in aquaculture IV. Blackwell, London, pp 153–192

Planas J, Gutiérrez J, Fernández J, Carrillo M, Canals P (1990) Annual and daily variations of plasma cortisol in sea bass, Dicentrarchus labrax L. Aquaculture 91:171–178

Pottinger TG (2008) The stress response in fish: mechanisms, effects and measurement. In: Branson E (ed) Fish welfare. Blackwell, Oxford, pp 32–48

Pottinger TG (2010) A multivariate comparison of the stress response in three salmonid and three cyprinid species: evidence for inter-family differences. J Fish Biol 76:601–621

Pottinger TG, Carrick TR (2001) Stress responsiveness affects dominant-subordinate relationships in rainbow trout. Hormones Behav 40:419–427

Pottinger TG, Moran TA (1993) Differences in plasma cortisol and cortisone dynamics during stress in two strains of rainbow trout (Oncorhynchus mykiss). J Fish Biol 43:121–130

Pottinger TG, Pickering AD (1992) The influence of social interaction on the acclimation of rainbow trout, Oncorhynchus mykiss (Walbaum) to chronic stress. J Fish Biol 41:435–447

Pottinger TG, Pickering AD, Hurley MA (1992) Consistency in the stress response of individuals of two strains of rainbow trout, Oncorhynchus mykiss. Aquaculture 103:275–289

Poulsen SB, Jensen LF, Nielsen KS, Malte H, Aarestrup K, Svendsen JC (2011) Behaviour of rainbow trout Oncorhynchus mykiss presented with a choice of normoxia and stepwise progressive hypoxia. J Fish Biol 79:969–979

Procarione LS, Barry TP, Malison JA (1999) Effects of high rearing densities and loading rates on the growth and stress responses of juvenile rainbow trout. N Am J Aquacult 61:91–96

Prunet P, Cairns MT, Winberg S, Pottinger TG (2008) Functional genomics of stress responses in fish. Rev Fish Sci 16(S1):157–166

Radley JJ, Morrison JH (2005) Repeated stress and structural plasticity in the brain. Ageing Res Rev 4:271–287

Rance TA, Baker BI, Webley G (1982) Variations in plasma cortisol concentrations over a 24-hour period in the rainbow trout Salmo gairdneri. Gen Comp Endocrinol 48:269–274

Redding JM, Patiño R, Schreck CB (1984) Clearance of corticosteroids in yearling coho salmon, Oncorhynchus kisutch, in fresh water and seawater and after stress. Gen Comp Endocrinol 54:433–443

Redgate ES (1974) Neural control of pituitary adrenal activity in Cyprinus carpio. Gen Comp Endocrinol 22:35–41

Reid SG, Bernier NJ, Perry SF (1998) The adrenergic stress response in fish: control of catecholamine storage and release. Comp Biochem Physiol C 120:1–27

Remage-Healey L, Bass AH (2004) Rapid, hierarchical modulation of vocal patterning by steroid hormones. J Neurosci 24:5892–5900

Remage-Healey L, Bass AH (2006) A rapid neuromodulatory role for steroid hormones in the control of reproductive behaviour. Brain Res 1126:27–35

Remage-Healey L, Nowacek DP, Bass AH (2006) Dolphin foraging sounds suppress calling and elevate stress hormone levels in a prey species, the Gulf toadfish. J Exp Biol 209:4444–4451

Roche H, Bogé G (1996) Fish blood parameters as a potential tool for identification of stress caused by environmental factors and chemical intoxication. Mar Environ Res 41:27–43

Roque A, Yavuzcan Yildiz H, Carazo I, Duncan N (2010) Physiological stress responses of sea bass (Dicentrarchus labrax) to hydrogen peroxide (H2O2) exposure. Aquaculture 304:104–107

Rose JD (2002) The neurobehavioral nature of fishes and the question of awareness and pain. Rev Fish Sci 10:1–38

Rose JD (2007) Anthropomorphism and ‘mental welfare’ of fishes. Dis Aquat Org 75:139–154

Rotllant J, Tort L (1997) Cortisol and glucose responses after acute stress by net handling in the sparid red porgy previously subjected to crowding stress. J Fish Biol 51:21–28

Rotllant J, Arends RJ, Mancera JM, Flik G, Wendelaar Bonga SE, Tort L (2000) Inhibition of HPI axis response to stress in gilthead sea bream (Sparus aurata) with physiological plasma levels of cortisol. Fish Physiol Biochem 23:13–22

Rotllant J, Balm PHM, Pérez-Sánchez J, Wendelaar-Bonga SE, Tort L (2001) Pituitary and interrenal function in gilthead sea bream (Sparus aurata L., Teleostei) after handling and confinement stress. Gen Comp Endocrinol 121:333–342

Rotllant J, Ruane NM, Caballero MJ, Montero D, Tort L (2003) Confinement stress response in sea bass (Dicentrarchus labrax) is characterised by an increased biosynthetic capacity of interrenal tissue, with no effect on ACTH sensitivity. Comp Biochem Physiol 136A:613–620

Rotllant J, Ruane NM, Dinis MT, Canario AVM, Power DM (2006) Intra-adrenal interactions in fish: catecholamine stimulated cortisol release in sea bass (Dicentrarchus labrax L.). Comp Biochem Physiol A 143:375–381

Ruane NM, Carballo EC, Komen J (2002) Increased stocking density influences the acute physiological stress response of common carp Cyprinus carpio (L.). Aquacult Res 33:777–784

Ruyet JP-L, Labbé L, Bayon NL, Sévère A, Roux AL, Delliou HL, Quéméner L (2008) Combined effects of water quality and stocking density on welfare and growth of rainbow trout (Oncorhynchus mykiss). Aquat Liv Res 21:185–195

Sánchez JA, López-Olmeda JF, Blanco-Vives B, Sánchez-Vázquez FJ (2009) Effects of feeding schedule on locomotor activity rhythms and stress response in sea bream. Physiol Behav 98:125–129

Sandhu N, Vijayan MM (2011) Cadmium-mediated disruption of cortisol biosynthesis involves suppression of corticosteroidogenic genes in rainbow trout. Aquat Toxicol 103:92–100

Sandi C (1996) Novelty-related rapid locomotor effects of corticosterone in rats. Eur J Neurosci 8:794–800

Santos GA, Schrama JW, Mamauag REP, Rombout JHWM, Verreth JAJ (2010) Chronic stress impairs performance, energy metabolism and welfare indicators in European seabass (Dicentrarchus labrax): the combined effects of fish crowding and water quality deterioration. Aquaculture 299:73–80

Santulli A, Modica A, Messina L, Ceffa L, Curatolo A, Rivas G, Fabis G, D’Amelio V (1999) Biochemical responses of European sea bass (Dicentrarchus labrax L.) to the stress induced by off shore experimental seismic prospecting. Mar Pollut Bull 38:1105–1114. doi: 10.1016/S0025-326X(99)00136-8

Schjolden J, Basic D, Winberg S (2009) Aggression in rainbow trout is inhibited by both MR and GR antagonists. Physiol Behav 98:625–630

Schreck CB (1981) Stress and compensation in teleostean fishes: response to social and physical factors. In: Pickering AD (ed) Stress and fish. Academic Press, London, pp 295–321

Schreck CB (1982) Stress and rearing of salmonids. Aquaculture 28:241–249

Schreck CB (1990) Physiological, behavioural and performance indicators of stress. Am Fish Soc Symp 8:29–37

Schreck CB (2010) Stress and fish reproduction: the roles of allostasis and hormesis. Gen Comp Endocrinol 165:549–556

Schreck CB, Patino R, Pring CK, Winton JR, Holway JE (1985) Effects of rearing density on indices of smoltification and performance of coho salmon, Oncorhynchus kisutch. Aquaculture 45:345–358

Scott AP, Hirschenhauser K, Bender N, Oliveira R, Earley RL, Sebire M, Ellis T, Pavlidis M, Hubbard PC, Huertas M, Canario A (2008) Non-invasive measurement of steroids in fish-holding water: important considerations when applying the procedure to behaviour studies. Behaviour 145(Suppl. SI):1307–1328

Seidelin M, Madsen SS, Byrialsen A, Kristiansen K (1999) Effects of insulin-like growth factor-I and cortisol on Na+, K+-ATPase expression in osmoregulatory tissues of brown trout (Salmo trutta). Gen Comp Endocrinol 113:331–342

Shelbourne JE (1975) Marine fish cultivation: pioneering studies on the culture of the larvae of the plaice (Pleuronectes platessa L.) and the sole (Solea solea L.). MAFF Fish Investig Ser II 27(9):29

Shrimpton JM, McCormick SD (1999) Responsiveness of gill Na+/K+-ATPase to cortisol is related to gill corticosteroid receptor concentration in juvenile rainbow trout. J Exp Biol 202:987–995

Silva P, Martins CIM, Engrola S, Marino G, Øyvind Ø, Conceição L (2010) Individual variation in stress physiology and behaviour in the flatfish Senegalese sole: evidences for coping styles. Appl Anim Behav Sci 124:75–81

Singley JA, Chavin W (1975) Serum cortisol in normal goldfish (Carassius auratus L.). Comp Biochem Physiol 50A:77–82

Sink TD, Lochmann RT, Fecteau KA (2008) Validation, use and disadvantages of enzyme-linked immunosorbent assay kits for detection of cortisol in channel catfish, largemouth bass, red pacu, and golden shiners. Fish Physiol Biochem 34:95–101

Sloman KA, Metcalfe NB, Taylor AC, Gilmour KM (2001) Plasma cortisol concentrations before and after social stress in rainbow trout and brown trout. Physiol Biochem Zoo 74:383–389

Sloman KA, Montpetit CJ, Gilmour KM (2002) Modulation of catecholamine release and cortisol secretion by social interactions in the rainbow trout, Oncorhynchus mykiss. Gen Comp Endocrinol 127:136–146

Small BC (2005) Effect of fasting on nychthemeral concentrations of plasma growth hormone (GH), insulin-like growth factor I (IGF-I), and cortisol in channel catfish (Ictalurus punctatus). Comp Biochem Physiol 142:217–223

Sneddon LU (2009) Pain perception in fish: indicators and endpoints. ILAR J 50:338–342

Sneddon LU, Braithwaite VA, Gentle MJ (2003) Do fishes have nociceptors? Evidence for the evolution of a vertebrate sensory system. Proc R Soc Lond B Biol Sci 270:1115–1121

Sørensen C, Nilsson GE, Summers CH, Øverli Ø (2011a) Social stress reduces forebrain cell proliferation in rainbow trout (Oncorhynchus mykiss). Behav Brain Res (in press)

Sørensen C, Bohlin LC, Øverli Ø, Nilsson GE (2011b) Cortisol reduces cell proliferation in the telencephalon of rainbow trout (Oncorhynchus mykiss). Physiol Behav 102:518–523

Stolte EH, de Mazon AF, Leon-Koosterziel KM, Jesiak M, Bury NR, Sturm A, Huub FJ, Savelkoul HFJ, Verburg van Kemenade BML, Flik G (2008) Corticosteroid receptors involved in stress regulation in common carp, Cyprinus carpio. J Endocrinol 198:403–417

Sumpter JP (1992) The stress response and its consequences in cultured fish. Bul Inst Zool Acad Sinica Monogr 16:229–236

Sumpter JP (1993) The deleterious effects of stress and their significance to aquaculture. In: Barnabé G, Kestemont P (eds) Production, environment and quality. European Aquaculture Society Special Publication No. 18. Ghent, Belgium, pp 157–165

Sumpter JP (1997) The endocrinology of stress. In: Iwama GK, Pickering AD, Sumpter JP, Schreck CB (eds) Fish stress and health in aquaculture. Cambridge University Press, Cambridge, pp 95–118

Sumpter JP, Pottinger TG, Weaver MR, Campbell PM (1994) The wide ranging effects of stress on fish. In: Davey KG, Peter RE, Tobe SS (eds) Perspectives in comparative endocrinology. NRC, Canada, pp 535–538

Teles M, Gravato C, Pacheco M, Santos MA (2004) Juvenile sea bass biotransformation, genotoxic and endocrine responses to β-naphthoflavone, 4-nonylphenol and 17β-estradiol individual and combined exposures. Chemosphere 57:147–158

Teles M, Pacheco M, Santos MA (2006) Biotransformation, stress and genotoxic effects of 17β-estradiol in juvenile sea bass (Dicentrarchus labrax L.). Environ Int 32:470–477

Thorpe JE, McConway MG, Miles MS, Muir JS (1987) Diel and seasonal changes in resting plasma cortisol levels in juvenile Atlantic salmon, Salmo salar L. Gen Comp Endocrinol 65:19–22

Tintos A, Míguez JM, Mancera JM, Soengas JL (2006) Development of a microtitre plate indirect ELISA for measuring cortisol in teleosts, and evaluation of stress responses in rainbow trout and gilthead sea bream. J Fish Biol 68:251–263

Tort L (2010) Stress in farmed fish: its consequences in health and performance. In: Koumoundouros G (ed) Recent advances in aquaculture research. Transworld Research Network, Trivandrum, pp 55–84

Tort L, Montero D, Robaina L, Fernández-Palacios H, Izquierdo MS (2001) Consistency of stress response to repeated handling in the gilthead sea bream, Sparus aurata. Aquacult Res 32:593–598

Tort L, Puigcerver M, Crespo S, Padrós F (2002) Cortisol and haematological response in sea bream and trout subjected to the anaesthetics clove oil and 2-phenoxyethanol. Aquacult Res 33:907–910

Tort L, Pavlidis M, Woo NYS (2011) Stress and welfare in sparid fishes. In: Pavlidis M, Mylonas C (eds) Sparidae. Biology and Aquaculture. Wiley-Blackwell, Oxford, pp 75–94

Turnbull J, Bell A, Adams C, Bron J, Huntingford F (2005) Stocking density and welfare of cage farmed Atlantic salmon: application of a multivariate analysis. Aquaculture 243:121–132

Tytler P, Hawkins AD (1981) Vivisection, anaesthetics and minor surgery. In: Hawkins AD (ed) Aquarium systems. Academic Press, London, pp 247–278

Uchida K, Kaneko T, Tagawa M, Hirano T (1998) Localization of cortisol receptor in branchial chloride cells in chum salmon fry. Gen Comp Endocrinol 109:175–185

van de Nieuwegiessen PG, Boerlage AS, Verreth JAJ, Schrama JW (2008) Assessing the effects of a chronic stressor, stocking density, on welfare indicators of juvenile African catfish, Clarias gariepinus Burchell. App Anim Behav Sci 115:233–243

Varsamos S, Flik G, Pepin JF, Wendelaar Bonga SE, Breuil G (2006) Husbandry stress during early life stages affects the stress response and health status of juvenile sea bass, Dicentrarchus labrax. Fish Shellfish Immunol 20:83–96

Vazzana M, Cammarata M, Cooper EL, Parrinello N (2002) Confinement stress in sea bass (Dicentrarchus labrax) depresses peritoneal leukocyte cytotoxicity. Aquaculture 210:231–243

Verburg-van Kemenade BML, Stolte EH, Metz JR, Chadzinska M (2009) Neuroendocrine-immune interactions in teleost fish. Fish Neuroendocrinol, Elsevier, pp 313–364

Vijayan MM (2011) Hormone response to stress. In: Farrell AP (ed) Encyclopedia of fish physiology from genome to environment. Elsevier, San Diego

Volkoff H, Xu M, MacDonald E, Hoskins L (2009) Aspects of hormonal regulation of appetite in fish with emphasis on goldfish, Atlantic cod and winter flounder: notes on actions and responses to nutritional, environmental and reproductive changes. Comp Biochem Physiol A 153:8–12

Weber ED, Borthwick SM, Helfrich LA (2002) Plasma cortisol response of juvenile chinook salmon to passage through Archimedes lifts and a Hidrostal pump. N Am J Fish Manage 22:563–570

Wedemeyer GA, Barton BA, McLeay DJ (1990) Stress and acclimation. In: Schreck CB, Moyle PB (eds) Methods for fish biology. Am Fish Soc, Bethesda, Maryland, pp 451–489

Wendelaar Bonga SE (1997) The stress response in fish. Physiol Rev 77:591–625

Winberg S, Lepage O (1998) Elevation of brain 5-HT activity, POMC expression, and plasma cortisol in socially subordinate rainbow trout. Am J Physiol Reg Int Comp Physiol 274:R645–R654

Wolkowitz OM, Burke H, Epel ES, Reus VL (2009) Glucocorticoids: mood, memory and mechanisms. Ann N Y Acad Sci 1179:19–40

Wong EYH, Herbert J (2006) Raised circulating corticosterone inhibits neuronal differentiation of progenitor cells in the adult hippocampus. Neuroscience 137:83–92

Wong S, Dykstra M, Campbell J, Earley R (2008) Measuring water-borne cortisol in convict cichlids (Amatitlania nigrofasciata): is the procedure a stressor? Behaviour 1245:1283–1305

Yamada H, Satoh R, Ogoh M, Takaji K, Fujimoto Y, Hakuba T, Chiba H, Kambegawa A, Iwata M (2002) Circadian changes in serum concentrations of steroids in Japanese char Salvelinus leucomaenis at the stage of final maturation. Zool Sci 19:891–898

Yeates JW, Main DSCJ (2008) Assessment of positive welfare: a review. Vet J 175:293–300

Yildiz YH, Ergonul MB (2010) Is prophylactic formalin exposure a stress source for gilthead sea bream (Sparus aurata) and sea bass (Dicentrarchus labrax)? Ankara Univ Vet Fak Derg 57:113–118

Zhao CM, Deng W, Gage FH (2008) Mechanisms and functional implications of adult neurogenesis. Cell 132:645–660