A multivariate comparison of the stress response in three salmonid and three cyprinid species: Evidence for inter-family differences

Journal of Fish Biology

Volumn 76, Issue 3, 2010, Pages 601-621

  Pottinger, T G ^a  

^a CENTRE FOR ECOLOGY AND HYDROLOGY   (United Kingdom)

Author keywords

Confinement; Cortisol; Glucose; Lactate; Phylogeny; Time course

Indexed keywords

AMINO ACID; HYDROCORTISONE; LACTIC ACID; GLUCOSE BLOOD LEVEL;

ANIMAL; ARTICLE; BLOOD; COMPARATIVE STUDY; CYPRINIFORMES; GLUCOSE BLOOD LEVEL; METABOLISM; PHYSIOLOGICAL STRESS; PHYSIOLOGY; SALMONID;

AMINO ACIDS; ANIMALS; BLOOD GLUCOSE; CYPRINIDAE; HYDROCORTISONE; LACTIC ACID; SALMONIDAE; STRESS, PHYSIOLOGICAL;

CYPRINIDAE; CYPRINIFORMES; CYPRINUS CARPIO; LEUCISCUS CEPHALUS; ONCORHYNCHUS MYKISS; PISCES; RUTILUS RUTILUS; SALMO TRUTTA; SALMONIDAE; SALVELINUS ALPINUS; SALVELINUS FONTINALIS;

EID: 77449155186     PISSN: 00221112     EISSN: 10958649     Source Type: Journal    
DOI: 10.1111/j.1095-8649.2009.02516.x     Document Type: Article

References (106)

1. Aaltonen T M, Jokinen E I, Lappivaara J, Markkula S E, Salo H M, Leppänen H, Lammi R. Effects of primary- and secondary-treated bleached kraft mill effluents on the immune system and physiological parameters of roach. Aquatic Toxicology 2000, 51:55-67.
2. Balon E K. About the oldest domesticates among fishes. Journal of Fish Biology 2004, 65((Suppl. A)):1-27.
3. Baroudy E, Elliott J M. Racial differences in eggs and juveniles of Windermere charr, Salvelinus alpinus. Journal of Fish Biology 1994, 45:407-415.
4. Barton B A. Stress in finfish: past, present, and future-a historical perspective. Fish Stress and Health in Aquaculture 1997, 1-33. Iwama G KPickering A DSumpter J PSchreck C B. In, eds), pp., Cambridge, Cambridge University Press
5. Barton B A. Salmonid fishes differ in their cortisol and glucose responses to handling and transport stress. North American Journal of Aquaculture 2000, 62:12-18.
6. Barton B A. Stress in fishes: a diversity of responses with particular reference to changes in circulating corticosteroids. Integrative and Comparative Biology 2002, 42:517-525.
7. Basu N, Nakano T, Grau E G, Iwama G K. The effects of cortisol on heat shock protein 70 levels in two fish species. General and Comparative Endocrinology 2001, 124:97-105.
8. Bau F, Ferroni-Claverie N, Parent J-P. Réponses physiologiques de sept espèces de poissons lacustres à un stress de capture (filet maillant et épuisette). Bulletin Francais de la Peche et de la Pisciculture 2001, 357/360:157-168.
9. Benfey T J, Biron M. Acute stress response in triploid rainbow trout (Oncorhynchus mykiss) and brook trout (Salvelinus fontinalis). Aquaculture 2000, 184:167-176.
10. Blahová J, Dobšíková R, Svobodová Z, Kaláb P. Simultaneous determination of plasma cortisol by high performance liquid chromatography and radioimmunoassay methods in fish. Acta Veterinaria Brno 2007, 76:59-64.
11. Blanchet S, Páez D J, Bernatchez L, Dodson J J. An integrated comparison of captive-bred and wild Atlantic salmon (Salmo salar): implications for supportive breeding programs. Biological Conservation 2008, 141:1989-1999.
12. Bracewell P, Cowx I G, Uglow R F. Effects of handling and electrofishing on plasma glucose and whole blood lactate of Leuciscus cephalus. Journal of Fish Biology 2004, 64:65-71.
13. Bradshaw D. Environmental endocrinology. General and Comparative Endocrinology 2007, 152:125-141.
14. Cairns M T, Johnson M C, Talbot A T, Pemmasani J K, McNeill R E, Houeix B, Sangrador-Vegas A, Pottinger T G. A cDNA microarray assessment of gene expression in the liver of rainbow trout (Oncorhynchus mykiss) in response to a handling and confinement stressor. Comparative Biochemistry and Physiology D 2008, 3:51-66.
15. Clements S P, Hicks B J, Carragher J F, Dedual M. The effect of a trapping procedure on the stress response of wild rainbow trout. North American Journal of Fisheries Management 2002, 22:907-916.
16. Congleton J L, LaVoie W J, Schreck C B, Davis L E. Stress indices in migrating juvenile Chinook salmon and steelhead of wild and hatchery origin before and after barge transportation. Transactions of the American Fisheries Society 2000, 129:946-961.
17. Dabrowska H, Dabrowski K, Meyer-Burgdorff K, Hanke W, Gunther K-D. The effect of large doses of vitamin C and magnesium on stress responses in common carp, Cyprinus carpio. Comparative Biochemistry and Physiology A 1991, 99:681-685.
18. Davis L E, Schreck C B. The energetic response to handling stress in juvenile coho salmon. Transactions of the American Fisheries Society 1997, 126:248-258.
19. Dror M, Sinyakov M S, Okun E, Dym M, Sredni B, Avtalion R R. Experimental handling stress as infection-facilitating factor for the goldfish ulcerative disease. Veterinary Immunology and Immunopathology 2006, 109:279-287.
20. Einarsdóttir I E, Nilssen K J. Stress responses of Atlantic salmon (Salmo salar L) elicited by water level reduction in rearing tanks. Fish Physiology and Biochemistry 1996, 15:395-400.
21. Elofsson U O E, Mayer I, Damsgård B, Winberg S. Intermale competition in sexually mature Arctic charr: effects on brain monoamines, endocrine stress responses, sex hormone levels, and behaviour. General and Comparative Endocrinology 2000, 118:450-460.
22. Fabbri E, Capuzzo A, Moon T W. The role of circulating catecholamines in the regulation of fish metabolism: an overview. Comparative Biochemistry and Physiology C 1998, 120:177-192.
23. Falahatkar B, Barton B A. Preliminary observations of physiological responses to acute handling and confinement in juvenile beluga Huso huso L. Aquaculture Research 2007, 38:1786-1789.
24. Fernandes-de-Castilho M, Pottinger T G, Volpato G L. Chronic social stress in rainbow trout: does it promote physiological habituation? General and Comparative Endocrinology 2008, 155:141-147.
25. Fevolden S-E, Røed K H, Fjalestad K T, Stien J. Poststress levels of lysozyme and cortisol in adult rainbow trout: heritabilities and genetic correlations. Journal of Fish Biology 1999, 54:900-910.
26. Gagnona A, Jumarie C, Hontela A. Effects of Cu on plasma cortisol and cortisol secretion by adrenocortical cells of rainbow trout (Oncorhynchus mykiss). Aquatic Toxicology 2006, 78:59-65.
27. Gesto M, Soengas J L, Miguez J M. Acute and prolonged stress responses of brain monoaminergic activity and plasma cortisol levels in rainbow trout are modified by PAHs (naphthalene, β-naphthoflavone and benzo(a)pyrene) treatment. Aquatic Toxicology 2008, 86:341-351.
28. Høgåsen H R, Prunet P. Plasma levels of thyroxine, prolactin, and cortisol in migrating and resident wild arctic char, Salvelinus alpinus. Canadian Journal of Fisheries and Aquatic Sciences 1997, 54:2947-2954.
29. Höglund E, Balm P H M, Winberg S. Behavioural and neuroendocrine effects of environmental background colour and social interaction in Arctic charr (Salvelinus alpinus). Journal of Experimental Biology 2002, 205:2535-2543.
30. Iversen M, Finstad B, Nilssen K J. Recovery from loading and transport stress in Atlantic salmon (Salmo salar L.) smolts. Aquaculture 1998, 168:387-394.
31. Jeney Z, Valtonen E T, Jeney G, Jokinen E I. Effects of pulp and paper mill effluent (BKME) on physiology and biochemistry of the roach (Rutilus rutilus L.). Archives of Environmental Contamination and Toxicology 1996, 30:523-529.
32. Jhingan E, Devlin R H, Iwama G K. Disease resistance, stress response and effects of triploidy in growth hormone transgenic coho salmon. Journal of Fish Biology 2003, 63:806-823.
33. Jørgensen E H, Balm P H M, Christiansen J S, Plotitsyna N, Ingebrigtsen K. Influence of o'p-DDD on the physiological response to stress in Arctic charr (Salvelinus alpinus). Aquatic Toxicology 2001, 54:179-193.
34. Jørgensen E H, Vijayan M M, Aluru N, Maule A G. Fasting modifies Aroclor 1254 impact on plasma cortisol, glucose and lactate responses to a handling disturbance in Arctic charr. Comparative Biochemistry and Physiology C 2002, 132:235-245.
35. Kagawa N, Mugiya Y. Exposure of goldfish (Carassius auratus) to bluegills (Lepomis macrochirus) enhances expression of stress protein 70 mRNA in the brains and increases plasma cortisol levels. Zoological Science 2000, 17:1061-1066.
36. Kakuta I. Reduction of stress response in carp, Cyprinus carpio L., held under deteriorating environmental conditions, by oral administration of bovine lactoferrin. Journal of Fish Diseases 1998, 21:161-167.
37. Kloas W, Stahl L, Hanke W. Characterization of corticosteroid receptors in two fish species, euryhaline tilapia and stenohaline carp. Annals of the New York Academy of Sciences 1998, 839:602-603.
38. Korte S M, Koolhaas J M, Wingfield J C, McEwen B S. The Darwinian concept of stress: benefits of allostasis and costs of allostatic load and the trade-offs in health and disease. Neuroscience and Biobehavioral Reviews 2005, 29:3-38.
39. Kubokawa K, Watanabe T, Yoshioka M, Iwata M. Effects of acute stress on plasma cortisol, sex steroid hormone and glucose levels in male and female sockeye salmon during the breeding season. Aquaculture 1999, 172:335-349.
40. Künzl C, Kaiser S, Meier E, Sachser N. Is a wild mammal kept and reared in captivity still a wild animal? Hormones and Behavior 2003, 43:187-196.
41. Lister A, Nero V, Farwell A, Dixon D G, Van der Kraak G. Reproductive and stress hormone levels in goldfish (Carassius auratus) exposed to oil sands process-affected water. Aquatic Toxicology 2008, 87:170-177.
42. Lucas M D, Drew R E, Wheeler P A, Verrell P A, Thorgaard G H. Behavioral differences among rainbow trout clonal lines. Behavior Genetics 2004, 34:355-365.
43. Lyytikäinen T, Pylkkö P, Ritola O, Lindström-Seppä P. The effect of acute stress and temperature on plasma cortisol and ion concentrations and growth of Lake Inari Arctic charr, Salvelinus alpinus. Environmental Biology of Fishes 2002, 64:195-202.
44. McDonald D G, Robinson J G. Physiological responses of lake trout to stress: effects of water hardness and genotype. Transactions of the American Fisheries Society 1993, 122:1146-1155.
45. McDonald D G, Goldstein M D, Mitton C. Responses of hatchery-reared brook trout, lake trout, and splake to transport stress. Transactions of the American Fisheries Society 1993, 122:1127-1138.
46. Mesa M G. Effects of multiple acute stressors on the predator avoidance ability and physiology of juvenile Chinook salmon. Transactions of the American Fisheries Society 1994, 123:786-793.
47. Mesa M G, Maule A G, Schreck C B. Interaction of infection with Renibacterium salmoninarum and physical stress in juvenile Chinook salmon: physiological responses, disease progression, and mortality. Transactions of the American Fisheries Society 2000, 129:158-173.
48. Mommsen T P, Vijayan M M, Moon T W. Cortisol in teleosts: dynamics, mechanisms of action, and metabolic regulation. Reviews in Fish Biology and Fisheries 1999, 9:211-268.
49. Momoda T S, Schwindt A R, Feist G W, Gerwick L, Bayne C J, Schreck C B. Gene expression in the liver of rainbow trout, Oncorhynchus mykiss, during the stress response. Comparative Biochemistry and Physiology D 2007, 2:303-315.
50. Norris D O, Donahue S, Dores R M, Lee J K, Maldonado T R, Woodling J D. Impaired adrenocortical response to stress by brown trout, Salmo trutta, living in metal-contaminated waters of the Eagle River, Colorado. General and Comparative Endocrinology 1999, 113:1-8.
51. Øverli Ø, Olsen R E, Løvik F, Ringo E. Dominance hierarchies in Arctic charr, Salvelinus alpinus L.: differential cortisol profiles of dominant and subordinate individuals after handling stress. Aquaculture Research 1999, 30:259-264.
52. Øverli Ø, Winberg S, Pottinger T G. Behavioral and neuroendocrine correlates of selection for stress responsiveness in rainbow trout-a review. Integrative and Comparative Biology 2005, 45:463-474.
53. Øverli Ø, Sørensen C, Pulman K G T, Pottinger T G, Korzan W, Summers C H, Nilsson G E. Evolutionary background for stress coping styles: relationships between physiological, behavioral, and cognitive traits in non-mammalian vertebrates. Neuroscience and Biobehavioral Reviews 2007, 31:396-412.
54. Pankhurst N W, Dedual M. Effects of capture and recovery on plasma levels of cortisol, lactate and gonadal steroids in a natural population of rainbow trout. Journal of Fish Biology 1994, 45:1013-1025.
55. Pankhurst N W, Ludke S L, King H R, Peter R E. The relationship between acute stress, food intake, endocrine status and life history stage in juvenile farmed Atlantic salmon, Salmo salar. Aquaculture 2008, 275:311-318.
56. Pickering A D, Pottinger T G. Stress responses and disease resistance in salmonid fish: effects of chronic elevation of plasma cortisol. Fish Physiology and Biochemistry 1989, 7:253-258.
57. Pickering A D, Pottinger T G, Christie P. Recovery of the brown trout, Salmo trutta L., from acute handling stress: a time-course study. Journal of Fish Biology 1982, 20:229-244.
58. Pickering A D, Pottinger T G, Sumpter J P. Independence of the pituitary-interrenal axis and melanotroph activity in the brown trout, Salmo trutta L., under conditions of environmental stress. General and Comparative Endocrinology 1986, 64:206-211.
59. Pottinger T G. Physiological changes in carp, Cyprinus carpio L., retained in anglers keepnets. Journal of Fish Biology 1998, 53:728-742.
60. Pottinger T G, Carrick T R. Modification of the plasma cortisol response to stress in rainbow trout by selective breeding. General and Comparative Endocrinology 1999a, 116:122-132.
61. Pottinger T G, Carrick T R. A comparison of plasma glucose and plasma cortisol as selection markers for high and low stress-responsiveness in female rainbow trout. Aquaculture 1999b, 175:351-365.
62. Pottinger T G, Carrick T R. Contrasting seasonal modulation of the stress response in male and female rainbow trout. Journal of Fish Biology 2000, 56:667-675.
63. Pottinger T G, Carrick T R. Stress responsiveness affects dominant-subordinate relationships in rainbow trout. Hormones and Behavior 2001, 40:419-427.
64. Pottinger T G, Moran T A. Differences in plasma cortisol and cortisone dynamics during stress in two strains of rainbow trout (Oncorhynchus mykiss). Journal of Fish Biology 1993, 43:121-130.
65. Pottinger T G, Pickering A D, Hurley M A. Consistency in the stress response of individuals of two strains of rainbow trout, Oncorhynchus mykiss. Aquaculture 1992, 103:275-289.
66. Pottinger T G, Balm P H M, Pickering A D. Sexual maturity modifies the responsiveness of the pituitary-interrenal axis to stress in male rainbow trout. General and Comparative Endocrinology 1995, 98:311-320.
67. Pottinger T G, Carrick T R, Hughes S E, Balm P H M. Testosterone, 11-ketotestosterone and estradiol-17β modify baseline and stress-induced interrenal and corticotropic activity in trout. General and Comparative Endocrinology 1996, 104:284-295.
68. Pottinger T G, Yeomans W E, Carrick T R. Plasma cortisol and 17b-estradiol levels in roach, Rutilus rutilus (L.), exposed to acute and chronic stress. Journal of Fish Biology 1999, 54:525-532.
69. Pottinger T G, Carrick T R, Appleby A, Yeomans W E. High blood cortisol levels and low cortisol receptor affinity: is the chub, Leuciscus cephalus, a cortisol-resistant teleost? General and Comparative Endocrinology 2000, 120:108-117.
70. Quabius E S, Nolan D T, Allin C J, Bonga S E W. Influence of dietary exposure to polychlorinated biphenyl 126 and nutritional state on stress response in tilapia (Oreochromis mossambicus) and rainbow trout (Oncorhynchus mykiss). Environmental Toxicology and Chemistry 2000, 19:2892-2899.
71. Quigley J T, Hinch S G. Effects of rapid experimental temperature increases on acute physiological stress and behaviour of stream dwelling juvenile Chinook salmon. Journal of Thermal Biology 2006, 31:429-441.
72. Reddy P K, Vijayan M M, Leatherland J F, Moon T W. Does RU486 modify hormonal responses to handling stressor and cortisol treatment in fed and fasted rainbow trout? Journal of Fish Biology 1995, 46:341-359.
73. Romero L M. Physiological stress in ecology: lessons from biomedical research. TRENDS in Ecology and Evolution 2004, 19:249-255.
74. Rosen H. A modified ninhydrin colorimetric analysis for amino acids. Archives of Biochemistry and Biophysics 1957, 67:10-15.
75. Ruane N M, Bonga S E W, Balm P H M. Differences between rainbow trout and brown trout in the regulation of the pituitary-interrenal axis and physiological performance during confinement. General and Comparative Endocrinology 1999, 115:210-219.
76. Ruane N M, Huisman E A, Komen J. Plasma cortisol and metabolite level profiles in two isogenic strains of common carp during confinement. Journal of Fish Biology 2001, 59:1-12.
77. Ruane N M, Huisman E A, Komen J. The influence of feeding history on the acute stress response of common carp (Cyprinus carpio). Aquaculture 2002a, 210:245-257.
78. Ruane N M, Carballo E C, Komen J. Increased stocking density influences the acute physiological stress response of common carp Cyprinus carpio (L.). Aquaculture Research 2002b, 33:777-784.
79. Sadler J, Pankhurst N W, Pankhurst P M, King H. Physiological stress responses to confinement in diploid and triploid Atlantic salmon. Journal of Fish Biology 2000, 56:506-518.
80. Sandodden R, Finstad B, Iversen M. Transport stress in Atlantic salmon (Salmo salar L.): anaesthesia and recovery. Aquaculture Research 2001, 32:87-90.
81. Sharpe C S. Physiological stress responses to automated and hand vaccine injection procedures in yearling coho salmon. North American Journal of Aquaculture 2007, 69:180-184.
82. Sharpe C S, Thompson D A, Blankenship H L, Schreck C B. Effects of routine handling and tagging procedures on physiological stress responses in juvenile Chinook salmon. Progressive Fish-Culturist 1998, 60:81-87.
83. Sink T D, Strange R J, Sawyers R E. Clove oil used at lower concentrations is less effective than MS-222 at reducing cortisol stress responses in anesthetized rainbow trout. North American Journal of Fisheries Management 2007, 27:156-161.
84. Skjervold P O, Fjæra S O, Østby P B, Einen O. Live-chilling and crowding stress before slaughter of Atlantic salmon (Salmo salar). Aquaculture 2001, 192:265-280.
85. Sloman K A, Metcalfe N B, Taylor A C, Gilmour K M. Plasma cortisol concentrations before and after social stress in rainbow trout and brown trout. Physiological and Biochemical Zoology 2001, 74:383-389.
86. Smith M E, Kane A S, Popper A N. Noise-induced stress response and hearing loss in goldfish (Carassius auratus). Journal of Experimental Biology 2004, 207:427-435.
87. Stone D A J, Gaylord T G, Johansen K A, Overturf K, Sealey W M, Hardy R W. Evaluation of the effects of repeated fecal collection by manual stripping on the plasma cortisol levels, TNF-α gene expression, and digestibility and availability of nutrients from hydrolyzed poultry and egg meal by rainbow trout, Oncorhynchus mykiss (Walbaum). Aquaculture 2008, 275:250-259.
88. Stratholt M L, Donaldson E M, Liley N R. Stress induced elevation of plasma cortisol in adult female coho salmon (Oncorhynchus kisutch), is reflected in egg cortisol content, but does not appear to affect early development. Aquaculture 1997, 158:141-153.
89. Sumpter J P, Pickering A D, Pottinger T G. Stress-induced elevation of plasma α-MSH and endorphin in the brown trout, Salmo trutta L. General and Comparative Endocrinology 1985, 59:252-265.
90. Tanck M W T, Booms G H R, Eding E H, Bonga S E W, Komen J. Cold shocks: a stressor for common carp. Journal of Fish Biology 2000, 57:881-894.
91. Tanck M W T, Claes T, Bovenhuis H, Komen J. Exploring the genetic background of stress using isogenic progenies of common carp selected for high or low stress-related cortisol response. Aquaculture 2002, 204:419-434.
92. Thomas P M, Pankhurst N W, Bremner H A. The effect of stress and exercise on post-mortem biochemistry of Atlantic salmon and rainbow trout. Journal of Fish Biology 1999, 54:1177-1196.
93. Trenzado C E, Carrick T R, Pottinger T G. Divergence of endocrine and metabolic responses to stress in two rainbow trout lines selected for differing cortisol responsiveness to stress. General and Comparative Endocrinology 2003, 133:332-340.
94. Van Dijk P L M, Van Den Thillart G E E J M, Bonga S E W. Is there a synergistic effect between steady-state exercise and water acidification in carp? Journal of Fish Biology 1993, 42:673-681.
95. Vianen G J, Van den Thillart G E E J M, Van Kampen M, Van Heel T I, Steffens A B. Plasma lactate and stress hormones in common carp (Cyprinus carpio) and rainbow trout (Oncorhynchus mykiss) during stepwise decreasing oxygen levels. Netherlands Journal of Zoology 2001, 51:33-50.
96. Vijayan M M, Moon T W. The stress response and the plasma disappearance of corticosteroid and glucose in a marine teleost, the sea raven. Canadian Journal of Zoology 1994, 72:379-386.
97. Wagner E, Arndt R, Hilton B. Physiological stress responses, egg survival and sperm motility for rainbow trout broodstock anesthetized with clove oil, tricaine methanesulfonate or carbon dioxide. Aquaculture 2002, 211:353-366.
98. Waring C P, Stagg R M, Poxton M G. The effects of handling on flounder (Platichthys flesus L.) and Atlantic salmon (Salmo salar L.). Journal of Fish Biology 1992, 41:131-144.
99. Weber E D, Borthwick S M, Helfrich L A. Plasma cortisol stress response of juvenile Chinook salmon to passage through Archimedes lifts and a Hidrostal pump. North American Journal of Fisheries Management 2002, 22:563-570.
100. Weber G M, Silverstein J T. Evaluation of a stress response for use in a selective breeding program for improved growth and disease resistance in rainbow trout. North American Journal of Aquaculture 2007, 69:69-79.
101. Wendelaar Bonga S E. The stress response in fish. Physiological Reviews 1997, 77:591-625.
102. Wikelski M, Cooke S J. Conservation physiology. TRENDS in Ecology and Evolution 2006, 21:38-46.
103. Winberg S, Lepage O. Elevation of brain 5-HT activity, POMC expression, and plasma cortisol in socially subordinate rainbow trout. American Journal of Physiology 1998, 43:R645-R654.
104. Wingfield J C. Comparative endocrinology, environment and global change. General and Comparative Endocrinology 2008, 157:207-216.
105. Yin Z, Lam T J, Sin Y M. The effects of crowding stress on the non-specific immune response in fancy carp (Cyprinus carpio L.). Fish & Shellfish Immunology 1995, 5:519-529.
106. Young J L, Bornik Z B, Marcotte M L, Charlie K N, Wagner G N, Hinch S G, Cooke S J. Integrating physiology and life history to improve fisheries management and conservation. Fish and Fisheries 2006, 7:262-283.