Excess post-hypoxic oxygen consumption is independent from lactate accumulation in two cyprinid fishes

Comparative Biochemistry and Physiology - A Molecular and Integrative Physiology

Volumn 165, Issue 1, 2013, Pages 54-60

  Genz, J ^a   Jyde, M B ^b   Svendsen, J C ^c,d,e   Steffensen, J F ^d   Ramlov H ^b  

^a UNIVERSITY OF MANITOBA   (Canada)

^b ROSKILDE UNIVERSITY   (Denmark)

^c TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

^d UNIVERSITY OF COPENHAGEN   (Denmark)

^e FRESHWATER INSTITUTE   (Canada)

Author keywords

Anaerobic metabolism; Anoxia; Common carp; Crucian carp

Indexed keywords

LACTIC ACID;

ANAEROBIC METABOLISM; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANOXIA; ARTICLE; CARP; FAST MUSCLE; GOLDFISH; HYPOXIA; NONHUMAN; OXYGEN CONSUMPTION; PLASMA; RESPIROMETRY;

EID: 84875034673     PISSN: 10956433     EISSN: 15314332     Source Type: Journal    
DOI: 10.1016/j.cbpa.2013.02.002     Document Type: Article

References (55)

1. Behrens J., Steffensen J. The effect of hypoxia on behavioural and physiological aspects of lesser sandeel, Ammodytes tobianus (Linnaeus, 1785). Mar. Biol. 2007, 150:1365-1377.
2. Bickler P.E., Buck L.T. Hypoxia tolerance in reptiles, amphibians, and fishes: life with variable oxygen availability. Annu. Rev. Physiol. 2007, 69:145-170.
3. Brett J.R. The respiratory metabolism and swimming performance of young sockeye salmon. J. Fish. Res. Board Can. 1964, 21:1183-1226.
4. Bushnell P.G., Steffensen J.F., Schurmann H., Jones D.R. Exercise metabolism in two species of cod in arctic waters. Polar Biol. 1994, 14:43-48.
5. Campbell H.A., Fraser K.P.P., Bishop C.M., Peck L.S., Egginton S. Hibernation in an Antarctic fish: on ice for winter. PLoS One 2008, 3:e1743.
6. Dalla Via J., Van den Thillart G., Cattani O., de Zwaan A. Influence of long-term hypoxia exposure on the energy metabolism of Solea solea. 11. Intermediary metabolism in blood, liver and muscle. Mar. Ecol. Prog. Ser. 1994, 111:17-27.
7. Dalla Via J., van den Thillart G., Cattani O., Cortesi P. Environmental versus functional hypoxia/anoxia in sole Solea solea: the lactate paradox revisited. Mar. Ecol. Prog. Ser. 1997, 154:79-90.
8. Farrell A.P., Richards J.G. Defining hypoxia: an integrative synthesis of the responses of fish to hypoxia. Fish Physiol. 2009, 27:487-503.
9. Hallman T.M., Rojas-Vargas A.C., Jones D.R., Richards J.G. Differential recovery from exercise and hypoxia exposure measured using 31P- and 1H-NMR in white muscle of the common carp Cyprinus carpio. J. Exp. Biol. 2008, 211:3237-3248.
10. Hochachka P.W. Defense strategies against hypoxia and hypothermia. Science 1986, 231:234-241.
11. Hochachka P.W., Mommsen T.P. Protons and anaerobiosis. Science 1983, 219:1391.
12. Holopainen I.J., Hyvärinen H. Ecology and physiology of crucian carp [Carassius carassius (L.)] in small Finnish ponds with anoxic conditions in winter. Verh. Int. Ver. Theor. Angew. Limnol. 1985, 22:2566-2570.
13. Holopainen I.J., Hyvärinen H., Piironen J. Anaerobic wintering of crucian carp (Carassius carassius L.) - II. Metabolic products. Comp. Biochem. Physiol. A: Physiol. 1986, 83:239-242.
14. Hyvärinen H., Holopainen I.J., Piironen J. Anaerobic wintering of crucian carp (Carassius carassius L.) I. Annual dynamics of glycogen reserves in nature. Comp. Biochem. Physiol. A: Physiol. 1985, 82:797-803.
15. Johnston I.A., Bernard L.M. Utilization of the ethanol pathway in carp following exposure to anoxia. J. Exp. Biol. 1983, 104:73-78.
16. Jordan A.D., Steffensen J.F. Effects of ration size and hypoxia on specific dynamic action in the cod. Physiol. Biochem. Zool. 2007, 80:178-185.
17. Killen S.S., Costa I., Brown J.A., Gamperl A.K. Little left in the tank: metabolic scaling in marine teleosts and its implications for aerobic scope. Proc. R. Soc. B 2007, 274:431-438.
18. Lin C., Wu H., Tjeerdema R., Viant M. Evaluation of metabolite extraction strategies from tissue samples using NMR metabolomics. Metabolomics 2007, 3:55-67.
19. Mandic M., Lau G.Y., Nijjar M.M.S., Richards J.G. Metabolic recovery in goldfish: a comparison of recovery from severe hypoxia exposure and exhaustive exercise. Comp. Biochem. Physiol. C 2008, 148:332-338.
20. Maxime V., Pichavant K., Boeuf G., Nonnotte G. Effects of hypoxia on respiratory physiology of turbot, Scophthalmus maximus. Fish Physiol. Biochem. 2000, 22:51-59.
21. Muusze B., Marcon J., van den Thillart G., Almeida-Val V. Hypoxia tolerance of Amazon fish: respirometry and energy metabolism of the cichlid Astronotus Ocellatus. Comp. Biochem. Physiol. A 1998, 120:151-156.
22. Nilsson G. A comparative study of aldehyde dehydrogenase and alcohol dehydrogenase activities in crucian carp and three other vertebrates: apparent adaptations to ethanol production. J. Comp. Physiol. B 1988, 158:479-485.
23. Nilsson G.E. Long-term anoxia in crucian carp: changes in the levels of amino acid and monoamine neurotransmitters in the brain, catecholamines in chromaffin tissue, and liver glycogen. J. Exp. Biol. 1990, 150:295-320.
24. Nilsson G.E. Surviving anoxia with the brain turned on. News Physiol. Sci. 2001, 16:217-221.
25. Nilsson G.E., Renshaw G.M.C. Hypoxic survival strategies in two fishes: extreme anoxia tolerance in the North European crucian carp and natural hypoxic preconditioning in a coral-reef shark. J. Exp. Biol. 2004, 207:3131-3139.
26. Peake S.J., Farrell A.P. Fatigue is a behavioural response in respirometer-confined smallmouth bass. J. Fish Biol. 2006, 68:1742-1755.
27. Pichavant K., Maxime V., Thebault M.T., Ollivier H., Garnier J.P., Bousquet B., Diouris M., Boeuf G., Nonnotte G. Effects of hypoxia and subsequent recovery on turbot Scophthalmus maximus: hormonal changes and anaerobic metabolism. Mar. Ecol. Prog. Ser. 2002, 225:275-285.
28. Piironen J., Holopainen I.J. A note on seasonality in anoxia tolerance of Crucian carp (Carassius carassius (L)) in the laboratory. Ann. Zool. Fenn. 1986, 23:335-338.
29. Richards J.G., Heigenhauser G.J.F., Wood C.M. Glycogen phosphorylase and pyruvate dehydrogenase transformation in white muscle of trout during high-intensity exercise. Am. J. Physiol. Reg. Int. Comp. Physiol. 2002, 282:R828-R836.
30. Scarabello M., Heigenhauser G.J.F., Wood C.M. The oxygen debt hypothesis in juvenile rainbow trout after exhaustive exercise. Respir. Physiol. 1991, 84:245-259.
31. Schurmann H., Steffensen J.F. Effects of temperature, hypoxia and activity on the metabolism of juvenile Atlantic cod. J. Fish Biol. 1997, 50:1166-1180.
32. Shoubridge E.A., Hochachka P.W. Ethanol: Novel end product of vertebrate anaerobic metabolism. Science 1980, 209:308-309.
33. Stecyk J.A.W., Farrell A.P. Cardiorespiratory responses of the common carp (Cyprinus carpio) to severe hypoxia at three acclimation temperatures. J. Exp. Biol. 2002, 205:759-768.
34. Stecyk J.A.W., Stenslökken K.O., Farrell A.P., Nilsson G.E. Maintained cardiac pumping in anoxic crucian carp. Science 2004, 306:77.
35. Steffensen J. Some errors in respirometry of aquatic breathers: how to avoid and correct for them. Fish Physiol. Biochem. 1989, 6:49-59.
36. Steffensen J.F., Johansen K., Bushnell P.G. An automated swimming respirometer. Comp. Biochem. Physiol. A: Physiol. 1984, 79:437-440.
37. Svendsen J.C., Tudorache C., Jordan A.D., Steffensen J.F., Aarestrup K., Domenici P. Partition of aerobic and anaerobic swimming costs related to gait transitions in a labriform swimmer. J. Exp. Biol. 2010, 213:2177-2183.
38. Svendsen J.C., Steffensen J.F., Aarestrup K., Frisk M., Etzerodt A., Jyde M. Excess post hypoxic oxygen consumption in rainbow trout Oncorhynchus mykiss: recovery in normoxia and hypoxia. Can. J. Zool. 2012, 90:1-11.
39. van den Thillart G., van Waarde A. The role of metabolic acidosis in the buffering of ATP by phosphagen stores in fish: an in vivo NMR study. Surviving Hypoxia: Mechanisms of Control and Adaptation 1993, 237-252. CRC Press. P.W. Hochachka, P.L. Lutz, T. Sick, M. Rosenthal, G. van den Thillart (Eds.).
40. van den Thillart G., Verbeek R. Anoxia-induced oxygen debt of goldfish (Carassius auratus L.). Physiol. Zool. 1991, 64:525-540.
41. 2 excretion rates and anoxia tolerance at 20, 10 and 5°C. Comp. Biochem. Physiol. A: Physiol. 1983, 76:295-300.
42. van der Linden A., Verhoye M., Nilsson G.E. Does anoxia induce cell swelling in carp brains? In vivo MRI measurements in crucian carp and common carp. J. Neurophysiol. 2001, 85:125-133.
43. van Ginneken V., van den Thillart G. Metabolic depression in fish measured by direct calorimetry: a review. Thermochim. Acta 2009, 483:1-7.
44. van Ginneken V., van den Thillart G., Addink A., Erkelens C. Fish muscle energy metabolism measured during hypoxia and recovery: an in vivo 31P-NMR study. Am. J. Physiol. Reg. Int. Comp. Physiol. 1995, 268:R1178-R1187.
45. van Ginneken V., Nieveen M., Van Eersel R., Van den Thillart G., Addink A. Neurotransmitter levels and energy status in brain of fish species with and without the survival strategy of metabolic depression. Comp. Biochem. Physiol. A 1996, 114:189-196.
46. van Ginneken V., Boot R., Murk T., van den Thillart G., Balm P. Blood plasma substrates and muscle lactic-acid response after exhaustive exercise in common carp and trout: indications for a limited lactate-shuttle. Anim. Biol. 2004, 54:119-130.
47. van Ginneken V.J.T., Snelderwaard P., van der Linden A., van der Reijden R., van den Thillart G., Kramer K. Coupling of heart rate with metabolic depression in fish: a radiotelemetric and calorimetric study. Thermochim. Acta 2004, 414:1-10.
48. van Raaij M.T.M., Pit D.S.S., Balm P.H.M., Anton B., van den Thillart G. Behavioral strategy and the physiological stress response in rainbow trout exposed to severe hypoxia. Horm. Behav. 1996, 30:85-92.
49. van Waarde A., van den Thillart G., Erkelens C., Addink A., Lugtenburg J. Functional coupling of glycolysis and phosphocreatine utilization in anoxic fish muscle. An in vivo 31P NMR study. J. Biol. Chem. 1990, 265:914-923.
50. Vianen G.J., Thillart G.E.E.J., 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. Neth. J. Zool. 2001, 51:33-50.
51. Viant M.R., Rosenblum E.S., Tjeerdema R.S. NMR-based metabolomics: a powerful approach for characterizing the effects of environmental stressors on organism health. Environ. Sci. Technol. 2003, 37:4982-4989.
52. Virani N.A., Rees B.B. Oxygen consumption, blood lactate and inter-individual variation in the gulf killifish, Fundulus grandis, during hypoxia and recovery. Comp. Biochem. Physiol. A 2000, 126:397-405.
53. Wilkie M.P., Pamenter M.E., Alkabie S., Carapic D., Shin D.S.H., Buck L.T. Evidence of anoxia-induced channel arrest in the brain of the goldfish (Carassius auratus). Comp. Biochem. Physiol. C 2008, 148:355-362.
54. Wissing J., Zebe E. The anaerobic metabolism of the bitterling Rhodeus amarus (cyprinidaf, teleostei). Comp. Biochem. Physiol. B 1988, 89:299-303.
55. Zhou B.S., Wu R.S.S., Randall D.J., Lam P.K.S., Ip Y.K., Chew S.F. Metabolic adjustments in the common carp during prolonged hypoxia. J. Fish Biol. 2000, 57:1160-1171.