Excess posthypoxic oxygen consumption in rainbow trout (Oncorhynchus mykiss): Recovery in normoxia and hypoxia

Canadian Journal of Zoology

Volumn 90, Issue 1, 2012, Pages 1-11

  Svendsen, Jon Christian ^a   Steffensen, John Fleng ^a   Aarestrup, Kim ^b   Frisk, Michael ^a   Etzerodt, Anne ^a   Jyde, Mads ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

HYPOTHESIS TESTING; HYPOXIA; METABOLISM; OXYGEN CONSUMPTION; SALMONID; SATURATION;

ONCORHYNCHUS MYKISS;

EID: 84855381715     PISSN: 00084301     EISSN: 14803283     Source Type: Journal    
DOI: 10.1139/Z11-095     Document Type: Article

References (80)

1. Brett, J.R., and Groves, T.D.D. 1979. Physiological energetics. In Fish physiology. Vol. 8. Bioenergetics and growth. Edited by W.S. Hoar, D.J. Randall, and J.R. Brett. Academic Press, New York. pp. 279-352.
2. Burgetz, I.J., Rojas-Vargas, A., Hinch, S.G., and Randall, D.J. 1998. Initial recruitment of anaerobic metabolism during sub-maximal swimming in rainbow trout (Oncorhynchus mykiss). J. Exp. Biol. 201(19): 2711-2721.
3. Bushnell, P.G., Steffensen, J.F., Schurmann, H., and Jones, D.R. 1994. Exercise metabolism in two species of cod in arctic waters. Polar Biol. 14(1): 43-48. doi:10.1007/BF00240271.
4. Chabot, D., and Claireaux, G. 2008. Environmental hypoxia as a metabolic constraint on fish: the case of Atlantic cod, Gadus morhua. Mar. Pollut. Bull. 57(6-12): 287-294. doi:10.1016/j. marpolbul.2008.04.001.
5. Chabot, D., and Dutil, J.D. 1999. Reduced growth of Atlantic cod in non-lethal hypoxic conditions. J. Fish Biol. 55(3): 472-491. doi:10.1111/j.1095-8649.1999.tb00693.x.
6. Claireaux, G., and Lefrançois, C. 2007. Linking environmental variability and fish performance: integration through the concept of scope for activity. Philos. Trans. R. Soc. Lond. B Biol. Sci. 362(1487): 2031-2041. doi:10.1098/rstb.2007.2099.
7. Claireaux, G., Webber, D.M., Kerr, S.R., and Boutilier, R.G. 1995. Physiology and behaviour of free-swimming Atlantic cod (Gadus morhua) facing fluctuating salinity and oxygenation conditions. J. Exp. Biol. 198(1): 61-69.
8. Claireaux, G., Webber, D.M., Lagardère, J.-P., and Kerr, S.R. 2000. Influence of water temperature and oxygenation on the aerobic metabolic scope of Atlantic cod (Gadus morhua). J. Sea Res. 44(3-4): 257-265. doi:10.1016/S1385-1101(00)00053-8.
9. Claireaux, G., Couturier, C., and Groison, A.L. 2006. Effect of temperature on maximum swimming speed and cost of transport in juvenile European sea bass (Dicentrarchus labrax). J. Exp. Biol. 209(17): 3420-3428. doi:10.1242/jeb.02346.
10. Cook, C.L., and Coughlin, D.J. 2010. Rainbow trout Oncorhynchus mykiss consume less energy when swimming near obstructions. J. Fish Biol. 77(7): 1716-1723. doi:10.1111/j.1095-8649.2010. 02801.x.
11. Cutts, C.J., Metcalfe, N.B., and Taylor, A.C. 2002. Juvenile Atlantic salmon (Salmo salar) with relatively high standard metabolic rates have small metabolic scopes. Funct. Ecol. 16(1): 73-78. doi:10. 1046/j.0269-8463.2001.00603.x.
12. Dalla Via, G.J. 1983. Bacterial respiration and antibiotics in animal respirometry. In Polarographic oxygen sensors. Edited by E. Gnaiger and H. Forstner. Springer-Verlag, New York. pp. 202-218.
13. Davis, R.E. 1962. Daily rhythm in the reaction of fish to light. Science (Washington, D.C.), 137(3528): 430-432. doi:10.1126/science.137.3528.430.
14. Diaz, R.J., and Breitburg, D.L. 2009. The hypoxic environment. In Fish physiology. Vol. 27. Hypoxia. Edited by J.G. Richards, A.P. Farrell, and C.J. Brauner. Academic Press, San Diego, Calif. pp. 1-23.
15. Dunn, J.F., and Hochachka, P.W. 1987. Turnover rates of glucose and lactate in rainbow trout during acute hypoxia. Can. J. Zool. 65(5): 1144-1148. doi:10.1139/z87-179.
16. Dupont-Prinet, A., Chatain, B., Grima, L., Vandeputte, M., Claireaux, G., and McKenzie, D. 2010. Physiological mechanisms underlying a trade-off between growth rate and tolerance of feed deprivation in the European sea bass (Dicentrarchus labrax). J. Exp. Biol. 213(7): 1143-1152. doi:10.1242/jeb.037812.
17. Dutil, J.-D., Sylvestre, E.-L., Gamache, L., Larocque, R., and Guderley, H. 2007. Burst and coast use, swimming performance and metabolism of Atlantic cod Gadus morhua in sub-lethal hypoxic conditions. J. Fish Biol. 71(2): 363-375. doi:10.1111/j. 1095-8649.2007.01487.x.
18. Evans, D.O. 1972. Correction for lag in continuous-flow respirometry. Can. J. Fish. Aquat. Sci. 29(8): 1214-1216.
19. Evans, D.O. 1990. Metabolic thermal compensation by rainbow trout: effects on standard metabolic rate and potential usable power. Trans. Am. Fish. Soc. 119(4): 585-600. doi:10.1577/1548-8659 (1990)119<0585:MTCBRT>2.3.CO;2.
20. Evans, D.O. 2007. Effects of hypoxia on scope-for-activity and power capacity of lake trout (Salvelinus namaycush). Can. J. Fish. Aquat. Sci. 64(2): 345-361. doi:10.1139/f07-007.
21. Farrell, A.P. 2007. Cardiorespiratory performance during prolonged swimming tests with salmonids: a perspective on temperature effects and potential analytical pitfalls. Philos. Trans. R. Soc. Lond. B Biol. Sci. 362(1487): 2017-2030. doi:10.1098/rstb.2007. 2111.
22. Farrell, A.P., and Richards, J.G. 2009. Defining hypoxia: an integrative synthesis of the responses of fish to hypoxia. In Fish physiology. Vol. 27. Hypoxia. Edited by J.G. Richards, A.P. Farrell, and C.J. Brauner. Academic Press, San Diego, Calif. pp. 487-503.
23. Fry, F.E.J. 1971. The effects of environmental factors on the physiology of fish. In Fish physiology. Vol. VI. Edited by W.S. Hoar and D.J. Randall. Academic Press, New York. pp. 1-98.
24. Fu, S.-J., Zeng, L.-Q., Li, X.-M., Pang, X., Cao, Z.-D., Peng, J.-L., and Wang, Y.-X. 2009. The behavioural, digestive and metabolic characteristics of fishes with different foraging strategies. J. Exp. Biol. 212(14): 2296-2302. doi:10.1242/jeb.027102.
25. Gowan, C., and Fausch, K.D. 2002. Why do foraging stream salmonids move during summer? Environ. Biol. Fishes, 64(1-3): 139-153. doi:10.1023/A:1016010723609.
26. Grossman, G.D., Rincon, P.A., Farr, M.D., and Ratajczak, R.E., Jr. 2002. A new optimal foraging model predicts habitat use by driftfeeding stream minnows. Ecol. Freshwat. Fish, 11(1): 2-10. doi:10.1034/j.1600-0633.2002.110102.x.
27. Guderley, H., and Pörtner, H.O. 2010. Metabolic power budgeting and adaptive strategies in zoology: examples from scallops and fish. Can. J. Zool. 88(8): 753-763. doi:10.1139/Z10-039.
28. Guensch, G.R., Hardy, T.B., and Addley, R.C. 2001. Examining feeding strategies and position choice of drift-feeding salmonids using an individual-based, mechanistic foraging model. Can. J. Fish. Aquat. Sci. 58(3): 446-457.
29. 1H-NMR in white muscle of the common carp Cyprinus carpio. J. Exp. Biol. 211(20): 3237-3248. doi:10. 1242/jeb.019257.
30. Herbert, N.A., Skjæraasen, J.E., Nilsen, T., Salvanes, A.G.V., and Steffensen, J.F. 2011. The hypoxia avoidance behaviour of juvenile Atlantic cod (Gadus morhua L.) depends on the provision and pressure level of an O2 refuge. Mar. Biol. (Berl.), 158(4): 737-746. doi:10.1007/s00227-010-1601-7.
31. Herskin, J. 1999. Effects of social and visual contact on the oxygen consumption of juvenile sea bass measured by computerized intermittent respirometry. J. Fish Biol. 55(5): 1075-1085. doi:10. 1111/j.1095-8649.1999.tb00742.x.
32. Jones, E.A., Lucey, K.S., and Ellerby, D.J. 2007. Efficiency of labriform swimming in the bluegill sunfish (Lepomis macrochirus). J. Exp. Biol. 210(19): 3422-3429. doi:10.1242/jeb. 005744.
33. Jordan, A.D., and Steffensen, J.F. 2007. Effects of ration size and hypoxia on specific dynamic action in the cod. Physiol. Biochem. Zool. 80(2): 178-185. doi:10.1086/510565.
34. Jorgensen, S.J., Klimley, A.P., and Muhlia-Melo, A.F. 2009. Scalloped hammerhead shark Sphyrna lewini, utilizes deep-water, hypoxic zone in the Gulf of California. J. Fish Biol. 74(7): 1682-1687. doi:10.1111/j.1095-8649.2009.02230.x.
35. Killen, S.S., Costa, I., Brown, J.A., and Gamperl, A.K. 2007. Little left in the tank: metabolic scaling in marine teleosts and its implications for aerobic scope. Proc. R. Soc. Lond. B Biol. Sci. 274(1608): 431-438. doi:10.1098/rspb.2006.3741.
36. Lee, C.G., Farrell, A.P., Lotto, A., Hinch, S.G., and Healey, M.C. 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): 3253-3260. doi:10.1242/jeb.00548.
37. Luecke, C., and Teuscher, D. 1994. Habitat selection by lacustrine rainbow trout (Oncorhynchus mykiss) within gradients of temperature, oxygen, and food availability. In Theory and application in fish feeding ecology. Vol. 18. Edited by D.J. Stouder, K.L. Fresh, and R.J. Feller. University of South Carolina Press, Columbia. pp. 134-149.
38. Mandic, M., Lau, G.Y., Nijjar, M.M.S., and Richards, J.G. 2008. Metabolic recovery in goldfish: a comparison of recovery from severe hypoxia exposure and exhaustive exercise. Comp. Biochem. Physiol. C Toxicol. Pharmacol. 148(4): 332-338.
39. Marvin, D.E., Jr., and Burton, D.T. 1973. Cardiac and respiratory responses of rainbow trout, bluegills and brown bullhead catfish during rapid hypoxia and recovery under normoxic conditions. Comp. Biochem. Physiol. A Physiol. 46(4): 755-765. doi:10. 1016/0300-9629(73)90127-8.
40. Matthews, K.R., and Berg, N.H. 1997. Rainbow trout responses to water temperature and dissolved oxygen stress in two southern California stream pools. J. Fish Biol. 50(1): 50-67. doi:10.1111/j. 1095-8649.1997.tb01339.x.
41. Maxime, V., Pichavant, K., Boeuf, G., and Nonnotte, G. 2000. Effects of hypoxia on respiratory physiology of turbot, Scophthalmus maximum. Fish Physiol. Biochem. 22(1): 51-59. doi:10.1023/ A:1007829214826.
42. McKenzie, D.J., Pedersen, P.B., and Jokumsen, A. 2007. Aspects of respiratory physiology and energetics in rainbow trout (Oncorhynchus mykiss) families with different size-at-age and condition factor. Aquaculture, 263(1-4): 280-294. doi:10.1016/j. aquaculture.2006.10.022.
43. Milligan, C.L. 1996. Metabolic recovery from exhaustive exercise in rainbow trout. Comp. Biochem. Physiol. A Physiol. 113(1): 51-60. doi:10.1016/0300-9629(95)02060-8.
44. Milligan, C.L., Hooke, G.B., and Johnson, C. 2000. Sustained swimming at low velocity following a bout of exhaustive exercise enhances metabolic recovery in rainbow trout. J. Exp. Biol. 203(5): 921-926.
45. Neuenfeldt, S., Andersen, K.H., and Hinrichsen, H.-H. 2009. Some Atlantic cod Gadus morhua in the Baltic Sea visit hypoxic water briefly but often. J. Fish Biol. 75(1): 290-294. doi:10.1111/j.1095-8649.2009.02281.x.
46. Niimi, A.J. 1978. Lag adjustment between estimated and actual physiological responses conducted in flow-through systems. Can. J. Fish. Aquat. Sci. 35(9): 1265-1269.
47. Nonnotte, G., Maxime, V., Truchot, J.P., Williot, P., and Peyraud, C. 1993. Respiratory responses to progressive ambient hypoxia in the sturgeon, Acipenser baeri. Respir. Physiol. 91(1): 71-82. doi:10. 1016/0034-5687(93)90090-W.
48. Norin, T., and Malte, H. 2011. Repeatability of standard metabolic rate, active metabolic rate and aerobic scope in young brown trout during a period of moderate food availability. J. Exp. Biol. 214(10): 1668-1675. doi:10.1242/jeb.054205.
49. Ott, M.E., Heisler, N., and Ultsch, G.R. 1980. A re-evaluation of the relationship between temperature and the critical oxygen tension in freshwater fishes. Comp. Biochem. Physiol. A Physiol. 67(3): 337-340. doi:10.1016/S0300-9629(80)80005-3.
50. Pichavant, K., Person-Le-Ruyet, J., Le Bayon, N., Severe, A., Le Roux, A., and Boeuf, G. 2001. Comparative effects of long-term hypoxia on growth, feeding and oxygen consumption in juvenile turbot and European sea bass. J. Fish Biol. 59(4): 875-883. doi:10. 1111/j.1095-8649.2001.tb00158.x.
51. Pollock, M.S., Clarke, L.M.J., and Dubé, M.G. 2007. The effects of hypoxia on fishes: from ecological relevance to physiological effects. Environ. Rev. 15: 1-14. doi:10.1139/a06-006.
52. Priede, I.G. 1977. Natural selection for energetic efficiency and the relationship between activity level and mortality. Nature (London), 267(5612): 610-611. doi:10.1038/267610a0.
53. Priede, I.G. 1985. Metabolic scope in fishes. In Fish energetics: new perspectives. Edited by P. Tytler and P. Calow. Croom-Helm, London. pp. 33-64.
54. Rahel, F.J., and Nutzman, J.W. 1994. Foraging in a lethal environment: fish predation in hypoxic waters of a stratified lake. Ecology, 75(5): 1246-1253. doi:10.2307/1937450.
55. Rao, G.M.M. 1968. Oxygen consumption of rainbow trout (Salmo gairdneri) in relation to activity and salinity. Can. J. Zool. 46(4): 781-786. doi:10.1139/z68-108.
56. Reidy, S.P., Nelson, J.A., Tang, Y., and Kerr, S.R. 1995. Postexercise metabolic rate in Atlantic cod and its dependence upon the method of exhaustion. J. Fish Biol. 47(3): 377-386. doi:10. 1111/j.1095-8649.1995.tb01907.x.
57. Reidy, S.P., Kerr, S.R., and Nelson, J.A. 2000. Aerobic and anaerobic swimming performance of individual Atlantic cod. J. Exp. Biol. 203(2): 347-357.
58. Richards, J.G. 2009. Metabolic and molecular responses of fish to hypoxia. In Fish physiology. Vol. 27. Hypoxia. Edited by J.G. Richards, A.P. Farrell, and C.J. Brauner. Academic Press, San Diego, Calif. pp. 443-485.
59. Richards, J.G. 2011. Physiological, behavioral and biochemical adaptations of intertidal fishes to hypoxia. J. Exp. Biol. 214(2): 191-199. doi:10.1242/jeb.047951.
60. Ross, L.G., and McKinney, R.W. 1988. Respiratory cycles in Oreochromis niloticus (L.), measured using a six-channel microcomputer-operated respirometer. Comp. Biochem. Physiol. A Physiol. 89(4): 637-643. doi:10.1016/0300-9629(88)90846-8.
61. Scarabello, M., Heigenhauser, G.J.F., and Wood, C.M. 1991. The oxygen debt hypothesis in juvenile rainbow trout after exhaustive exercise. Respir. Physiol. 84(2): 245-259. doi:10.1016/0034-5687 (91)90121-X.
62. Schurmann, H., and Steffensen, J.F. 1997. Effects of temperature, hypoxia and activity on the metabolism of juvenile cod. J. Fish Biol. 50(6): 1166-1180.
63. Steffensen, J.F. 1989. Some errors in respirometry of aquatic breathers: how to avoid and correct for them. Fish Physiol. Biochem. 6(1): 49-59. doi:10.1007/BF02995809.
64. Steffensen, J.F. 2002. Metabolic cold adaptation of polar fish based on measurements of aerobic oxygen consumption: fact or artefact? Artefact! Comp. Biochem. Physiol. A Mol. Integr. Physiol. 132(4): 789-795. doi:10.1016/S1095-6433(02)00048-X.
65. Steffensen, J.F., Johansen, K., and Bushnell, P.G. 1984. An automated swimming respirometer. Comp. Biochem. Physiol. A Physiol. 79(3): 437-440. doi:10.1016/0300-9629(84)90541-3.
66. Steffensen, J.F., Schurmann, H., and Bushnell, P.G. 1994. Oxygen consumption in four species of teleosts from Greenland: no evidence of metabolic cold adaptation. Polar Biol. 14(1): 49-54. doi:10.1007/BF00240272.
67. Svendsen, J.C., Tudorache, C., Jordan, A.D., Steffensen, J.F., Aarestrup, K., and Domenici, P. 2010. Partition of aerobic and anaerobic swimming costs related to gait transitions in a labriform swimmer. J. Exp. Biol. 213(13): 2177-2183. doi:10.1242/jeb. 041368.
68. Tang, Y., and Boutilier, R.G. 1991. White muscle intracellular acid-base and lactate status following exhaustive exercise: a comparison between freshwater- and sea water- adapted rainbow trout. J. Exp. Biol. 156(1): 153-171.
69. van den Thillart, G., and Verbeek, R. 1991. Anoxia-induced oxygen debt of goldfish (Carassius auratus L.). Physiol. Zool. 64(2): 525-540.
70. 2 levels for aerobic and anaerobic metabolism. Mar. Ecol. Prog. Ser. 104(1): 109-117. doi:10.3354/meps104109.
71. van Ginneken, V., van den Thillart, G., Addink, A., and Erkelens, C. 1995. Fish muscle energy metabolism measured during hypoxia and recovery: an in vivo 31P-NMR study. Am. J. Physiol. 268(5): R1178-R1187.
72. Vianen, G.J., van den Thillart, G.E.E.J.M., van Kampen, M., van Heel, T.I., and Steffens, A.B. 2001. Plasma lactate and stress hormones in common carp (Cyprinus carpio) and rainbow trout (Oncorhynchus mykiss) during stepwise decreasing oxygen levels. Neth. J. Zool. 51(1): 33-50.
73. Virani, N., and Rees, B. 2000. Oxygen consumption, blood lactate and inter-individual variation in the gulf killifish, Fundulus grandis, during hypoxia and recovery. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 126(3): 397-405. doi:10.1016/S1095-6433 (00)00219-1.
74. Vornanen, M., Stecyk, J.A.W., and Nilsson, G.E. 2009. The anoxiatolerant crucian carp (Carassius carassius L.). In Fish physiology. Vol. 27. Hypoxia. Edited by J.G. Richards, A.P. Farrell, and C.J. Brauner. Academic Press, San Diego, Calif. pp. 397-441.
75. Water Management Branch. 1997. Ambient water quality criteria for dissolved oxygen. Ministry of Environment, Lands and Parks, Government of British Columbia, Victoria. Available from http://www.env.gov.bc.ca/wat/wq/BCguidelines/do/ [assessed 9 July 2011].
76. Webb, P.W. 1971. The swimming energetics of trout. II. Oxygen consumption and swimming efficiency. J. Exp. Biol. 55(2): 521-540.
77. Wells, M.G.R. 2009. Blood-gas transport and haemoglobin function: adaptations for functional and environmental hypoxia. In Fish physiology. Vol. 27. Hypoxia. Edited by J.G. Richards, A.P. Farrell, and C.J. Brauner. Academic Press, San Diego, Calif. pp. 255-299.
78. Wieser, W. 1985. Developmental and metabolic constraints of the scope for activity in young rainbow trout (Salmo gairdneri). J. Exp. Biol. 118(1): 133-142.
79. Wu, R.S.S. 2002. Hypoxia: from molecular responses to ecosystem responses. Mar. Pollut. Bull. 45(1-12): 35-45. doi:10.1016/S0025-326X(02)00061-9.
80. Zar, J.H. 1984. Biostatistical analysis. Prentice-Hall, Inc., Englewood Cliffs, N.J.