Metabolic Fuel Utilization During Swimming: Optimizing Nutritional Requirements for Enhanced Performance

  • L. J. Magnoni
  • O. Felip
  • J. Blasco
  • J. V. Planas


Swimming activity is fueled by energy derived from the catabolism of lipids, carbohydrates, or proteins, which ultimately have to be obtained from the diets of fish. This chapter describes changes in the relative use of metabolic fuels available in fish, providing estimates for increasing energy expenditure during different types of swimming conditions. The enzyme AMP-activated protein kinase plays an evolutionarily conserved role during exercise, acting as a fuel gauge in the muscle of fish. Feeding and feed composition may alter swimming performance by changing the cardiovascular capacity and the relative utilization of metabolic fuels. Sustained swimming can enhance the utilization of dietary carbohydrates after a highly digestible carbohydrate-rich meal, sparing the use of protein for muscle growth. Therefore, an optimal diet formulation in combination with an adequate swimming regime may further improve growth rates and feed efficiencies observed in some fish species. Establishing and applying such conditions may imply important advantages for the fish farming industry.


Rainbow Trout Swimming Speed White Muscle Swimming Performance Swimming Activity 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


  1. Alsop DH, Kieffer JD, Wood CM (1999) The effects of temperature and swimming speed on instantaneous fuel use and nitrogenous waste excretion of the Nile tilapia. Physiol Biochem Zool 72:474–483PubMedGoogle Scholar
  2. Alsop DH, Wood CM (1997) The interactive effects of feeding and exercise on oxygen consumption, swimming performance and protein usage in juvenile rainbow trout (Oncorhynchus mykiss). J Exp Biol 200:2337–2346PubMedGoogle Scholar
  3. Anttila K, Jantti M, Mänttäri S (2010) Effects of training on lipid metabolism in swimming muscles of sea trout (Salmo trutta). J Comp Physiol B 180:707–714PubMedGoogle Scholar
  4. Anttila K, Järvilehto M, Mänttäri S (2008) The swimming performance of brown trout and whitefish: the effects of exercise on Ca2+ handling and oxidative capacity of swimming muscles. J Comp Physiol B 178:465–475PubMedGoogle Scholar
  5. Anttila K, Mänttäri S, Järvilehto M (2006) Effects of different training protocols on Ca2+ handling and oxidative capacity in skeletal muscle of Atlantic salmon (Salmo salar L.). J Exp Biol 209:2971–2978PubMedGoogle Scholar
  6. Arzel J, Metailler R, Le Gall P, Guillaume J (1998) Relationship between ration size and dietary protein level varying at the expense of carbohydrate and lipid in triploid brown trout fry, Salmo trutta. Aquaculture 162:259–268Google Scholar
  7. Azevedo PA, van Milgen J, Leeson S, Bureau DP (2005) Comparing efficiency of metabolizable energy utilization by rainbow trout (Oncorhynchus mykiss) and Atlantic salmon (Salmo salar) using factorial and multivariate approaches. J Anim Sci 83:842–851PubMedGoogle Scholar
  8. Babin PJ, Vernier J-M (1989) Plasma lipoproteins in fish. J Lipid Res 30:467–489PubMedGoogle Scholar
  9. Barrett BA, McKeown BA (1988) Sustained exercise increases plasma growth hormone concentrations in two anadromous salmonids. Can J Fish Aquat Sci 45:747–749Google Scholar
  10. Beamish FWH (1974) Apparent specific dynamic action of largemouth bass, Micropterus salmoides. J Fish Res Board Can 31:1763–1769Google Scholar
  11. Beamish FWH (1979) Swimming capacity. In: Hoar WS, Randall DJ (eds) Fish physiology, vol 7. Academic Press, New York, pp 101–187Google Scholar
  12. Beamish FWH, Howlett JC, Medland TE (1989) Impact of diet on metabolism and swimming performance in juvenile lake trout, Salvelinus namaycush. Can J Fish Aquat Sci 46:384–388Google Scholar
  13. Beamish FWH, Medland TE (1986) Protein sparing effects in large rainbow trout, Oncorhynchus mykiss. Aquaculture 55:35–42Google Scholar
  14. Bell JG, Dick JR, McVicar AH, Sargent JR, Thompson KD (1993) Dietary sunflower, linseed and fish oils affect phospholipid fatty acid composition, development of cardiac lesions, phospholipase activity and eicosanoid production in Atlantic salmon (Salmo salar). Prostag Leukotr Ess 49:665–673Google Scholar
  15. Bell JG, McVicar AH, Park MT, Sargent JR (1991) High dietary linoleic acid affects the fatty acid compositions of individual phospholipids from tissues of Atlantic salmon (Salmo salar)—association with stress susceptibility and cardiac lesion. J Nutr 121:1163–1172PubMedGoogle Scholar
  16. Bergot F (1979) Effects of dietary carbohydrates and of their mode of distribution on glycaemia in rainbow trout (Salmo gairdneri R.). Comp Biochem Physiol A 64:543–547Google Scholar
  17. Bernard SF, Reidy SP, Zwingelstein G, Weber J-M (1999) Glycerol and fatty acid kinetics in rainbow trout: effects of endurance swimming. J Exp Biol 202:279–288PubMedGoogle Scholar
  18. Bilinski E, Jonas RE (1964) Utilization of lipids by fish. II. Fatty acid oxidation by a particulate fraction from lateral line muscle. Can J Biochem Physiol 42:345–352PubMedGoogle Scholar
  19. Blaikie H, Kerr S (1996) Effect of activity level on apparent heat increment in Atlantic cod, Gadus morhua. Can J Fish Aquat Sci 53:2093–2099Google Scholar
  20. Blasco J, Fernández-Borrás J, Marimon I, Requena A (1996) Plasma glucose kinetics and tissue uptake in brown trout in vivo: effect of an intravascular glucose load. J Comp Physiol B 165:534–541Google Scholar
  21. Blasco J, Marimon I, Viaplana I, Fernández-Borrás J (2001) Fate of glucose in tissues of brown trout in vivo: effects of fasting and glucose loading. Fish Physiol Biochem 24:247–258Google Scholar
  22. Bonen A (2009) PGC-1α-induced improvements in skeletal muscle metabolism and insulin sensitivity. Appl Physiol Nutr Metab 34:307–308PubMedGoogle Scholar
  23. Brauge C, Corraze G, Médale F (1995) Effects of dietary levels of carbohydrate and lipid on glucose oxidation and lipogenesis from glucose in rainbow trout, Oncorhynchus mykiss, reared in freshwater or in seawater. Comp Biochem Physiol A 111:117–124Google Scholar
  24. Brauge C, Médale F, Corraze G (1994) Effect of dietary carbohydrate levels on growth, body composition and glycaemia in rainbow trout, Oncorhynchus mykiss, reared in seawater. Aquaculture 123:109–120Google Scholar
  25. Brett JR (1964) The respiratory metabolism and swimming performance of young Sockeye salmon. J Fish Res Board Can 21:1183–1226Google Scholar
  26. Brett JR (1973) Energy expenditure of sockeye salmon, Oncorhynchus nerka, during sustained performance. J Fish Res Board Can 30:1799–1809Google Scholar
  27. Brett JR, Groves TDD (1979) Physiological energetics. In: Hoar WS, Randall DJ, Brett JR (eds) Fish physiology, vol 8. Academic Press, New York, pp 279–352Google Scholar
  28. Bureau DP, Kaushik SJ, Cho CY (2002) Bioenergetics. In: Halver JE, Hardy RW (eds) Fish nutrition. Academic Press, San Diego, pp 1–53Google Scholar
  29. Bushnell PG, Steffensen JF, Schurmann H, Jones DR (1994) Exercise metabolism in two species of cod in Arctic waters. Polar Biol 14:43–48Google Scholar
  30. Clarke A, Johnston NM (1999) Scaling of metabolic rate with body mass and temperature in teleost fish. J Anim Ecol 68:893–905Google Scholar
  31. Company R, Calduch-Giner JA, Kaushik S, Pérez-Sánchez J (1999) Growth performance and adiposity in gilthead sea bream (Sparus aurata): risks and benefits of high energy diets. Aquaculture 171:279–292Google Scholar
  32. Coughlin DJ (2002) Aerobic muscle function during steady swimming in fish. Fish Fisher 3:63–78Google Scholar
  33. Chakraborty SC, Ross LG, Ross B (1992) Specific dynamic action and feeding metabolism in common carp, Cyprinus carpio L. Comp Biochem Physiol A 103:809–815Google Scholar
  34. Charnock JS, McLennan PL, Abeywardena MY (1992) Dietary modulation of lipid metabolism and mechanical performance of the heart. Mol Cell Biochem 116:19–25PubMedGoogle Scholar
  35. Chatelier A, McKenzie DJ, Prinet A, Galois R, Robin J, Zambonino J, Claireaux G (2006) Associations between tissue fatty acid composition and physiological traits of performance and metabolism in the sea bass (Dicentrarchus labrax). J Exp Biol 209:3429–3439PubMedGoogle Scholar
  36. Cho CY, Bureau DP (1995) Determination of the energy requirements of fish with particular reference to salmonids. J Appl Ichthyol 11:141–163Google Scholar
  37. Cho CY, Bureau DP (2001) A review of diet formulation strategies and feeding systems to reduce excretory and feed wastes in aquaculture. Aquacult Res 32:349–360Google Scholar
  38. Cho CY, Hynes JD, Wood KR, Yoshida HK (1994) Development of high-nutrient-dense, low-pollution diets and prediction of aquaculture wastes using biological approaches. Aquaculture 124:293–305Google Scholar
  39. Cho CY, Kaushik SJ (1990) Nutritional energetics in fish: energy and protein utilization in rainbow trout (Salmo gairdneri). World Rev Nutr Diet 61:132–172PubMedGoogle Scholar
  40. Cho CY, Slinger SJ, Bayley HS (1982) Bioenergetics of salmonid fishes: energy intake, expenditure and productivity. Comp Biochem Physiol B 73:25–41Google Scholar
  41. Christiansen JS, Jobling M (1990) The behaviour and the relationship between food intake and growth of juvenile Arctic charr, Salvelinus alpinus L., subjected to sustained exercise. Can J Zool 68:2185–2191Google Scholar
  42. Christiansen JS, Jørgensen EH, Jobling M (1991) Oxygen consumption in relation to sustained exercise and social stress in the Arctic charr (Salvelinus alpinus L.). J Exp Zool 260:149–156Google Scholar
  43. Davison W (1989) Training and its effects on teleost fish. Comp Biochem Physiol A 94:1–10Google Scholar
  44. Davison W (1997) The effects of exercise training on teleost fish, a review of recent literature. Comp Biochem Physiol A 117:67–75Google Scholar
  45. Davison W, Goldspink G (1977) The effect of prolonged exercise on the lateral musculature of the brown trout (Salmo trutta). J Exp Biol 70:1–12Google Scholar
  46. Daxboeck C (1982) Effect of coronary artery ablation on exercise performance in Salmo gairdneri. Can J Zool 60:375–381Google Scholar
  47. de Lange P, Moreno M, Silvestri E, Lombardi A, Goglia F, Lanni A (2007) Fuel economy in food-deprived skeletal muscle: signaling pathways and regulatory mechanisms. FASEB J 21:3431–3441PubMedGoogle Scholar
  48. Dewar H, Graham J (1994) Studies of tropical tuna swimming performance in a large water tunnel: energetics. J Exp Biol 192:13–31PubMedGoogle Scholar
  49. Dobson GP, Hochachka PW (1987) Role of glycolysis in adenylate depletion and repletion during work and recovery in teleost white muscle. J Exp Biol 129:125–140PubMedGoogle Scholar
  50. Dobson GP, Parkhouse WS, Hochachka PW (1987) Regulation of anaerobic ATP-generating pathways in trout fast-twitch skeletal muscle. Am J Physiol Regul Integr Comp Physiol 253:R186–R194Google Scholar
  51. Driedzic WR, Hochachka PW (1976) Control of energy metabolism in fish white muscle. Am J Physiol 230:579–582PubMedGoogle Scholar
  52. Driedzic WR, Hochachka PW (1978) Metabolism in fish during exercise. In: Hoar WS, Randall DJ (eds) Fish physiology, vol 7. Academic Press, New York, pp 503–543Google Scholar
  53. East P, Magnan P (1987) The effect of locomotor activity on the growth of brook charr, Salvelinus fontinalis Mitchill. Can J Zool 65:843–846Google Scholar
  54. Farrell AP, Johansen JA, Steffensen JF, Moyes CD, West TG, Suarez RK (1990) Effects of exercise training and coronary artery ablation on swimming performance, heart size, and cardiac enzymes in rainbow trout, Oncorhynchus mykiss. Can J Zool 68:1174–1179Google Scholar
  55. Farrell AP, Johansen JA, Suarez RK (1991) Effects of exercise-training on cardiac performance and muscle enzymes in rainbow trout, Oncorhynchus mykiss. Fish Physiol Biochem 9:303–312Google Scholar
  56. Farrell AP, Thorarensen H, Axelsson M, Crocker CE, Gamperl AK, Cech JJ Jr (2001) Gut blood flow in fish during exercise and severe hypercapnia. Comp Biochem Physiol A 128:549–561Google Scholar
  57. Felip O, Ibarz A, Fernández-Borrás J, Beltrán M, Martín-Pérez M, Planas JV, Blasco J (2012) Tracing metabolic routes of dietary carbohydrate and protein in rainbow trout (Oncorhynchus mykiss) using stable isotopes ([13C]starch and [15N]protein): effects of gelatinisation of starches and sustained swimming. Br J Nutr 107:834–844PubMedGoogle Scholar
  58. Fitzgibbon QP, Baudinette RV, Musgrove RJ, Seymour RS (2008) Routine metabolic rate of southern bluefin tuna (Thunnus maccoyii). Comp Biochem Physiol A 150:231–238Google Scholar
  59. Forster I, Ogata H (1996) Growth and whole-body lipid content of juvenile red sea bream reared under different conditions of exercise training and dietary lipid. Fish Sci 62:404–409Google Scholar
  60. Frøyland L, Lie Ø, Berge RK (2000) Mitochondrial and peroxisomal beta-oxidation capacities in various tissues from Atlantic salmon, Salmo salar. Aquacult Nutr 6:85–89Google Scholar
  61. Fu SJ, Xie XJ, Cao ZD (2005) Effect of dietary composition on specific dynamic action in southern catfish, Silurus meridionalis. Aquacult Res 36:1384–1390Google Scholar
  62. Fu SJ, Zeng LQ, Li XM, Pang X, Cao ZD, Peng JL, Wang YX (2009) The behavioural, digestive and metabolic characteristics of fishes with different foraging strategies. J Exp Biol 212:2296–2302PubMedGoogle Scholar
  63. Furnell DJ (1987) Partitioning of locomotor and feeding metabolism in sablefish (Anoplopoma fimbria). Can J Zool 65:486–489Google Scholar
  64. Furuichi M, Yone Y (1981) Change of blood sugar and plasma insulin levels of fishes in glucose tolerance test. Bull Jpn Soc Sci Fish 47:761–764Google Scholar
  65. Gatlin DM, Barrows FT, Brown P, Dabrowski K, Gaylord TG, Hardy RW, Herman E, Hu G, Krogdahl Å, Nelson R, Overturf K, Rust M, Sealey W, Skonberg D, J Souza E, Stone D, Wilson R, Wurtele E (2007) Expanding the utilization of sustainable plant products in aquafeeds: a review. Aquacult Res 38:551–579Google Scholar
  66. Gatlin DM, Poe WE, Wilson RP (1986) Protein and energy requirements of fingerling channel catfish for maintenance and maximum growth. J Nutr 116:2121–2131PubMedGoogle Scholar
  67. Glencross BD, Clarke SM, Buchanan JG, Carter CG, van Barneveld RJ (2002) Temporal growth patterns of farmed juvenile southern bluefin tuna, Thunnus maccoyii (Castelnau) fed moist pellets. J World Aquacult Soc 33:138–145Google Scholar
  68. Goolish EM (1991) Aerobic and anaerobic scaling in fish. Biol Rev 66:33–56Google Scholar
  69. Gregory TR, Wood CM (1999) The effects of chronic plasma cortisol elevation on the feeding behaviour, growth, competitive ability, and swimming performance of juvenile rainbow trout. Physiol Biochem Zool 72:286–294PubMedGoogle Scholar
  70. Haman F, Weber J-M (1996) Continuous tracer infusion to measure in vivo metabolite turnover rates in trout. J Exp Biol 199:1157–1162PubMedGoogle Scholar
  71. Haman F, Zwingelstein G, Weber J-M (1997) Effects of hypoxia and low temperature on substrate fluxes in fish: plasma metabolite concentrations are misleading. Am J Physiol Regul Integr Comp Physiol 273:R2046–R2054Google Scholar
  72. Hammer C (1994) Effects of endurance swimming on the growth of 0- and 1- age group of whiting, Merlangius merlangus, Gadidae. Arch Fish Mar Res 42:105–122Google Scholar
  73. Hammer C (1995) Fatigue and exercise tests with fish. Comp Biochem Physiol A 112:1–20Google Scholar
  74. Hardie D, Sakamoto K (2006) AMPK: a key sensor of fuel and energy status in skeletal muscle. Physiology 21:48–60PubMedGoogle Scholar
  75. Hardie DG, Hawley SA, Scott JW (2006) AMP-activated protein kinase: development of the energy sensor concept. J Physiol 574:7–15PubMedGoogle Scholar
  76. Harpaz S (2005) L-Carnitine and its attributed functions in fish culture and nutrition: a review. Aquaculture 249:3–21Google Scholar
  77. Hemre GI, Mommsen TP, Krogdahl A (2002) Carbohydrates in fish nutrition: effects on growth, glucose metabolism and hepatic enzymes. Aquacult Nutr 8:175–194Google Scholar
  78. Henderson RJ, Sargent JR (1985) Chain-length specificities of mitochondrial and peroxisomal β-oxidation of fatty acids in livers of rainbow trout (Salmo gairdneri). Comp Biochem Physiol B 82:79–85PubMedGoogle Scholar
  79. Hinch SG, Rand PS (1998) Swim speeds and energy use of upriver migrating sockeye salmon (Oncorhynchus nerka): role of local environment and fish characteristics. Can J Fish Aquat Sci 55:1821–1831Google Scholar
  80. Hock CE, Beck LD, Bodine RC, Reibel DK (1990) Influence of dietary fatty acids on myocardial ischemia and reperfusion. Am J Physiol Heart Circ Physiol 259:H1518–H1526Google Scholar
  81. Hochachka PW, Matheson GO (1992) Regulating ATP turnover rates over broad dynamic work ranges in skeletal muscles. J Appl Physiol 73:1697–1703PubMedGoogle Scholar
  82. Houlihan DF, Carter CG, McCarthy ID (1995) Protein synthesis in fish. In: Hochachka PW, Mommsen TP (eds) Metabolic Biochemistry, vol 4., Biochemistry and molecular biology of fishesElsevier Science, Amsterdam, pp 191–220Google Scholar
  83. Houlihan DF, Laurent P (1987) Effects of exercise training on the protein turnover of rainbow trout (Salmo gairdneri). Can J Fish Aquat Sci 44:1614–1621Google Scholar
  84. Ibarz A, Felip O, Fernández-Borrás J, Martín-Pérez M, Blasco J, Torrella J (2011) Sustained swimming improves muscle growth and cellularity in gilthead sea bream. J Comp Physiol B 181:209–217PubMedGoogle Scholar
  85. Jessen N, Goodyear LJ (2005) Contraction signaling to glucose transport in skeletal muscle. J Appl Physiol 99:330–337PubMedGoogle Scholar
  86. Jibb LA, Richards JG (2008) AMP-activated protein kinase activity during metabolic rate depression in the hypoxic goldfish, Carassius auratus. J Exp Biol 211:3111–3122PubMedGoogle Scholar
  87. Jobling M (1981) The influences of feeding on the metabolic rate of fishes: a short review. J Fish Biol 18:385–400Google Scholar
  88. Jobling M (1983) Towards an explanation of specific dynamic action (SDA). J Fish Biol 23:549–555Google Scholar
  89. Jobling M, Baardvik BM, Christiansen JS, Jørgensen EH (1993a) The effects of prolonged exercise training on growth performance and production parameters in fish. Aquacult Int 1:95–111Google Scholar
  90. Jobling M, Jørgensen EH, Arnesen AM, Ringø E (1993b) Feeding, growth and environmental requirements of Arctic charr: a review of aquaculture potential. Aquacult Int 1:20–46Google Scholar
  91. Johnston IA, Moon TW (1980) Endurance exercise training in the fast and slow muscles of a teleost fish (Pollachius virens). J Comp Physiol B 135:147–156Google Scholar
  92. Jones DR (1982) Anaerobic exercise in teleost fish. Can J Zool 60:1131–1134Google Scholar
  93. Jørgensen EH, Jobling M (1993) The effects of exercise on growth, food utilisation and osmoregulatory capacity of juvenile Atlantic salmon, Salmo salar. Aquaculture 116:233–246Google Scholar
  94. Jorgensen SB, Richter EA, Wojtaszewski JFP (2006) Role of AMPK in skeletal muscle metabolic regulation and adaptation in relation to exercise. J Physiol 574:17–31PubMedGoogle Scholar
  95. Jourdan-Pineau H, Dupont-Prinet A, Claireaux G, McKenzie DJ (2010) An investigation of metabolic prioritization in the European sea bass, Dicentrarchus labrax. Physiol Biochem Zool 83:68–77PubMedGoogle Scholar
  96. Kaushik SJ (2002) European sea bass Dicentrarchus labrax. In: Webster CD, Lim C (eds) Nutrient requirements and feeding of finfish for aquaculture. CABI Publishing, Wallingford, pp 28–39Google Scholar
  97. Kaushik SJ, Médale F (1994) Energy requirements, utilization and dietary supply to salmonids. Aquaculture 124:81–97Google Scholar
  98. Kaushik SJ, Oliva-Teles A (1985) Effect of digestible energy on nitrogen and energy balance in rainbow trout. Aquaculture 50:89–101Google Scholar
  99. Kaushik SJ, Seiliez I (2010) Protein and amino acid nutrition and metabolism in fish: current knowledge and future needs. Aquacult Res 41:322–332Google Scholar
  100. Kieffer JD, Alsop D, Wood CM (1998) A respirometric analysis of fuel use during aerobic swimming at different temperatures in rainbow trout (Oncorhynchus mykiss). J Exp Biol 201:3123–3133PubMedGoogle Scholar
  101. Kiessling A, Higgs DA, Dosanjh BS, Eales JE (1994) Influence of sustained exercise at two ration levels on growth and thyroid function of all-female chinook salmon (Oncorhynchus tshawytscha) in seawater. Can J Fish Aquat Sci 51:1975–1984Google Scholar
  102. Kiessling A, Lindahal-Kiessling K, Kiessling KH (2004) Energy utilization and metabolism in spawning migrating Early Stuart sockeye salmon (Oncorhynchus nerka): the migratory paradox. Can J Fish Aquat Sci 61:425–465Google Scholar
  103. Kiessling KH, Kiessling A (1993) Selective utilization of fatty acids in rainbow trout (Oncorhynchus mykiss Walbaum) red muscle mitochondria. Can J Zool 71:248–251Google Scholar
  104. Lau G, Richards J (2011) AMP-activated protein kinase plays a role in initiating metabolic rate suppression in goldfish hepatocytes. J Comp Physiol B 181:927–939PubMedGoogle Scholar
  105. Lauff RF, Wood CM (1996a) Respiratory gas exchange, nitrogenous waste excretion, and fuel usage during aerobic swimming in juvenile rainbow trout. J Comp Physiol B 166:501–509Google Scholar
  106. Lauff RF, Wood CM (1996b) Respiratory gas exchange, nitrogenous waste excretion, and fuel usage during starvation in juvenile rainbow trout, Oncorhynchus mykiss. J Comp Physiol B 165:542–551PubMedGoogle Scholar
  107. Lauff RF, Wood CM (1997) Effects of training on respiratory gas exchange, nitrogenous waste excretion, and fuel usage during aerobic swimming in juvenile rainbow trout (Oncorhyncus mykiss). Can J Fish Aquat Sci 54:566–571Google Scholar
  108. LeGrow SM, Beamish FWH (1986) Influence of dietary protein and lipid on apparent heat increment of rainbow trout, Salmo gairdneri. Can J Fish Aquat Sci 43:19–25Google Scholar
  109. Li XM, Cao ZD, Fu SJ (2010) The effect of exercise training on the metabolic interaction between feeding and locomotion in the juvenile southern catfish (Silurus meridionalis Chen). J Exp Zool A 313:557–563Google Scholar
  110. Lucas MC, Priede IG (1992) Utilization of metabolic scope in relation to feeding and activity by individual and grouped zebrafish, Brachydanio rerio (Hamilton-Buchanan). J Fish Biol 41:175–190Google Scholar
  111. Luna-Acosta A, Lefrancois C, Millot S, Chatain B, Bagout ML (2011) Physiological response in different strains of sea bass (Dicentrarchus labrax): swimming and aerobic metabolic capacities. Aquaculture 317:162–167Google Scholar
  112. Lupatsch I, Kissil GW, Sklan D, Pfeffer E (1998) Energy and protein requirements for maintenance and growth in gilthead seabream (Sparus aurata L.). Aquacult Nutr 4:165–173Google Scholar
  113. MacLean PS, Zheng D, Jones JP, Olson AL, Dohm GL (2002) Exercise-induced transcription of the muscle glucose transporter (GLUT4) gene. Biochem Biophys Res Commun 292:409–414PubMedGoogle Scholar
  114. Magnoni L, Vaillancourt E, Weber JM (2008) High resting triacylglycerol turnover of rainbow trout exceeds the energy requirements of endurance swimming. Am J Physiol Regul Integr Comp Physiol 295:R309–R315PubMedGoogle Scholar
  115. Magnoni L, Weber JM (2007) Endurance swimming activates trout lipoprotein lipase: plasma lipids as a fuel for muscle. J Exp Biol 210:4016–4023PubMedGoogle Scholar
  116. Magnoni LJ, Patterson DA, Farrell AP, Weber JM (2006) Effects of long-distance migration on circulating lipids of sockeye salmon (Oncorhynchus nerka). Can J Fish Aquat Sci 63:1822–1829Google Scholar
  117. Magnoni LM, Vraskou Y, Palstra AP, Planas JV (2012) AMP-activated protein kinase plays an important evolutionary conserved role in the regulation of glucose metabolism in fish skeletal muscle cells. PLoS ONE 7:e31219PubMedGoogle Scholar
  118. Masumoto T (2002) Yellowtail, Seriola quinqueradiata. In: Webster CD, Lim C (eds) Nutrient requirements and feeding of finfish for aquaculture. CABI Publishing, Wallingford, pp 131–146Google Scholar
  119. McClelland GB, Craig PM, Dhekney K, Dipardo S (2006) Temperature- and exercise-induced gene expression and metabolic enzyme changes in skeletal muscle of adult zebrafish (Danio rerio). J Physiol 577:739–751PubMedGoogle Scholar
  120. McCue MD (2010) Starvation physiology: reviewing the different strategies animals use to survive a common challenge. Comp Biochem Physiol A 156:1–18Google Scholar
  121. McDonald DG, Milligan CL, McFarlane WJ, Croke S, Currie S, Hooke B, Angus RB, Tufts BL, Davidson K (1998) Condition and performance of juvenile Atlantic salmon (Salmo salar): effects of rearing practices on hatchery fish and comparison with wild fish. Can J Fish Aquat Sci 55:1208–1219Google Scholar
  122. McGoogan BB, Gatlin DMI (1998) Metabolic requirements of red drum, Sciaenops ocellatus, for protein and energy based on weight gain and body composition. J Nutr 128:123–129PubMedGoogle Scholar
  123. McKenzie DJ (2001) Effects of dietary fatty acids on the respiratory and cardiovascular physiology of fish. Comp Biochem Physiol A 128:605–619Google Scholar
  124. McKenzie DJ, Higgs DA, Dosanjh B, Deacon G, Randall DJ (1998) Dietary lipid composition influences swimming performance in Atlantic salmon (Salmo salar) in seawater. Fish Physiol Biochem 19:111–122Google Scholar
  125. McKenzie DJ, Pedersen P, Jokumsen A (2007) Aspects of respiratory physiology and energetics in rainbow trout (Oncorhynchus mykiss) families with different size-at-age and condition factor. Aquaculture 263:280–294Google Scholar
  126. Merrill GF, Kurth EJ, Hardie DG, Winder WW (1997) AICA riboside increases AMP-activated protein kinase, fatty acid oxidation, and glucose uptake in rat muscle. Am J Physiol Endocrinol Metab 273:E1107–E1112Google Scholar
  127. Milligan CL (1996) Metabolic recovery from exhaustive exercise in rainbow trout. Comp Biochem Physiol A 113:51–60Google Scholar
  128. Milligan CL, Girard SS (1993) Lactate metabolism in rainbow trout. J Exp Biol 180:175–193Google Scholar
  129. Mommsen TP, French CJ, Hochachka PW (1980) Sites and patterns of protein and amino acid utilization during the spawning migration of salmon. Can J Zool 58:1785–1799Google Scholar
  130. Moon TW (2001) Glucose intolerance in teleost fish: fact or fiction? Comp Biochem Physiol B 129:243–249PubMedGoogle Scholar
  131. Morash AJ, Bureau DP, McClelland GB (2009) Effects of dietary fatty acid composition on the regulation of carnitine palmitoyltransferase (CPT) I in rainbow trout (Oncorhynchus mykiss). Comp Biochem Physiol B 152:85–93PubMedGoogle Scholar
  132. Moyes CD, Buck LT, Hochachka PW, Suarez RK (1989) Oxidative propierties of the carp red muscle and white muscle. J Exp Biol 143:321–331PubMedGoogle Scholar
  133. Moyes CD, West TG (1995) Exercise metabolism of fish. In: Hochachka PW, Mommsen TP (eds) Metabolic biochemistry, vol 4., Biochemistry and molecular biology of fishesElsevier Science, Amsterdam, pp 368–392Google Scholar
  134. Muir BS, Niimi AJ (1972) Oxygen consumption of the euryhaline fish Aholehole (Kuhlia sandvicensis) with reference to salinity, swimming, and food consumption. J Fish Res Board Can 29:67–77Google Scholar
  135. Ohta M, Watanabe T (1996) Energy requirement for maintenance of body weight and activity, and for maximum growth in rainbow trout. Fish Sci 62:737–744Google Scholar
  136. Omlin T, Weber J-M (2010) Hypoxia stimulates lactate disposal in rainbow trout. J Exp Biol 213:3802–3809PubMedGoogle Scholar
  137. Otha M, Watanabe T (1996) Dietary energy budgets in carp. Fish Sci 62:745–753Google Scholar
  138. Ozório RODA (2008) Swimming activity and non-protein energy (NPE) metabolism in fish. Curr Nutr Food Sci 4:282–289Google Scholar
  139. Ozório RODA, Andrade C, Timóteo VMFA, da Conceição LEC, Valente LMP (2009) Effects of feeding levels on growth response, body composition, and energy expenditure in blackspot seabream, Pagellus bogaraveo, juveniles. J World Aquacult Soc 40:95–103Google Scholar
  140. Ozório RODA, Van Ginneken VJT, Bessa RJB, Verstegen MWA, Verreth JAJ, Huisman EA (2010) Effects of exercise on L-carnitine and lipid metabolism in African catfish (Clarias gariepinus) fed different dietary L-carnitine and lipid levels. Br J Nutr 103:1139–1150PubMedGoogle Scholar
  141. Palstra A, van den Thillart G (2010) Swimming physiology of European silver eels (Anguilla anguilla L.): energetic costs and effects on sexual maturation and reproduction. Fish Physiol Biochem 36:297–322PubMedGoogle Scholar
  142. Pang X, Cao ZD, Fu SJ (2011) The effects of temperature on metabolic interaction between digestion and locomotion in juveniles of three cyprinid fish (Carassius auratus, Cyprinus carpio and Spinibarbus sinensis). Comp Biochem Physiol A 159:253–260Google Scholar
  143. Pang X, Cao ZD, Peng JL, Fu SJ (2010) The effects of feeding on the swimming performance and metabolic response of juvenile southern catfish, Silurus meridionalis, acclimated at different temperatures. Comp Biochem Physiol A 155:253–258Google Scholar
  144. Panserat S, Skiba-Cassy S, Seiliez I, Lansard M, Plagnes-Juan E, Vachot C, Aguirre P, Larroquet L, Chavernac G, Medale F, Corraze G, Kaushik S, Moon TW (2009) Metformin improves postprandial glucose homeostasis in rainbow trout fed dietary carbohydrates: a link with the induction of hepatic lipogenic capacities? Am J Physiol Regul Integr Comp Physiol 297:R707–R715PubMedGoogle Scholar
  145. Peres H, Goncalves P, Oliva-Teles A (1999) Glucose tolerance in gilthead seabream (Sparus aurata) and European seabass (Dicentrarchus labrax). Aquaculture 179:415–423Google Scholar
  146. Peres H, Oliva-Teles A (1999) Effect of dietary lipid level on growth performance and feed utilization by European sea bass juveniles (Dicentrarchus labrax). Aquaculture 179:325–334Google Scholar
  147. Peres H, Oliva-Teles A (2001) Effect of dietary protein and lipid level on metabolic utilization of diets by European sea bass (Dicentrarchus labrax) juveniles. Fish Physiol Biochem 25:269–275Google Scholar
  148. Petersen LH, Gamperl AK (2010) Effect of acute and chronic hypoxia on the swimming performance, metabolic capacity and cardiac function of Atlantic cod (Gadus morhua). J Exp Biol 213:808–819PubMedGoogle Scholar
  149. Polakof S, Panserat S, Craig PM, Martyres DJ, Plagnes-Juan E, Savari S, Aris-Brosou S, Moon TW (2011) The metabolic consequences of hepatic AMP-kinase phosphorylation in rainbow trout. PLoS ONE 6:e20228PubMedGoogle Scholar
  150. Rasmussen RS, Ostenfeld TH, McLean E (2000) Growth and feed utilisation of rainbow trout subjected to changes in feed lipid concentrations. Aquacult Int 8:531–542Google Scholar
  151. Regan MD, Kuchel LJ, Huang SSY, Higgs DA, Wang J, Schulte PM, Brauner CJ (2010) The effect of dietary fish oil and poultry fat replacement with canola oil on swimming performance and metabolic response to hypoxia in stream type spring Chinook salmon parr. Aquaculture 308:183–189Google Scholar
  152. Richards JG, Heigenhauser GJF, Wood CM (2002a) Glycogen phosphorylase and pyruvate dehydrogenase transformation in white muscle of trout during high-intensity exercise. Am J Physiol Regul Integr Comp Physiol 282:R828–R836PubMedGoogle Scholar
  153. Richards JG, Heigenhauser GJF, Wood CM (2002b) Lipid oxidation fuels recovery from exhaustive exercise in white muscle of rainbow trout. Am J Physiol Regul Integr Comp Physiol 282:R89–R99PubMedGoogle Scholar
  154. Richards JG, Mercado AJ, Clayton CA, Heigenhauser GJF, Wood CM (2002c) Substrate utilization during graded exercise in rainbow trout. J Exp Biol 205:2067–2077PubMedGoogle Scholar
  155. Ross LG, McKinney RW, Cardwell SK, Fullarton JG, Roberts SEJ, Ross B (1992) The effects of dietary protein content, lipid content and ration level on oxygen consumption and specific dynamic action in Oreochromis niloticus L. Comp Biochem Physiol A 103:573–578Google Scholar
  156. Roy D, Marette A (1996) Exercise induces the translocation of GLUT4 to transverse tubules from an intracellular pool in rat skeletal muscle. Biochem Biophys Res Commun 223:147–152PubMedGoogle Scholar
  157. Scarabello M, Heigenhauser GJF, Wood CM (1992) Gas exchange, metabolite status and excess post-exercise oxygen consumption after repetitive bouts of exhaustive exercise in juvenile rainbow trout. J Exp Biol 167:155–169PubMedGoogle Scholar
  158. Schalles JF, Wissing TE (1976) Effects of dry pellet diets on the metabolic rate of bluegill (Lepomis macrochirus). J Fish Res Board Can 33:2443–2449Google Scholar
  159. Shanghavi DS, Weber J-M (1999) Effects of sustained swimming on hepatic glucose production of rainbow trout. J Exp Biol 202:2161–2166PubMedGoogle Scholar
  160. Sheridan MA (1988) Lipid dynamics in fish: aspects of absorption, transportation, deposition and mobilization. Comp Biochem Physiol B 90:679–690PubMedGoogle Scholar
  161. Smith RW, Houlihan DF (1995) Protein synthesis and oxygen consumption in fish cells. J Comp Physiol B 165:93–101Google Scholar
  162. Standen EM, Hinch SG, Healey MC, Farrell AP (2002) Energetic costs of migration through the Fraser River Canyon, British Columbia, in adult pink (Oncorhynchus gorbuscha) and sockeye (Oncorhynchus nerka) salmon as assessed by EMG telemetry. Can J Fish Aquat Sci 59:1809–1818Google Scholar
  163. Stenslokken K-O, Ellefsen S, Stecyk JAW, Dahl MB, Nilsson GE, Vaage J (2008) Differential regulation of AMP-activated kinase and AKT kinase in response to oxygen availability in crucian carp (Carassius carassius). Am J Physiol Regul Integr Comp Physiol 295:R1803–R1814PubMedGoogle Scholar
  164. Stone DAJ (2003) Dietary carbohydrate utilization by fish. Rev Fish Sci 11:337–369Google Scholar
  165. Tandler A, Beamish FWH (1980) Specific dynamic action and diet in largemouth bass, Micropterus salmoides (Lacepede). J Nutr 110:750–764PubMedGoogle Scholar
  166. Thorarensen H, Farrell AP (2006) Postprandial intestinal blood flow, metabolic rates, and exercise in Chinook salmon (Oncorhynchus tshawytscha). Physiol Biochem Zool 79:688–694PubMedGoogle Scholar
  167. Tocher DR (2003) Metabolism and functions of lipids and fatty acids in teleost fish. Rev Fish Sci 11:107–184Google Scholar
  168. Totland GK, Kryvi H, Jødestøl KA, Christiansen EN, Tangeras A, Slinde E (1987) Growth and composition of the swimming muscle of adult Atlantic salmon (Salmo salar L.) during long-term sustained swimming. Aquaculture 66:299–313Google Scholar
  169. Towler MC, Hardie DG (2007) AMP-activated protein kinase in metabolic control and insulin signaling. Circ Res 100:328–341PubMedGoogle Scholar
  170. Van den Thillart G (1986) Energy metabolism of swimming trout (Salmo gairdneri). J Comp Physiol B 156:511–520Google Scholar
  171. Van der Meulen T, Schipper H, van den Boogaart JGM, Huising MO, Kranenbarg S, van Leeuwen JL (2006) Endurance exercise differentially stimulates heart and axial muscle development in zebrafish (Danio rerio). Am J Physiol Regul Integr Comp Physiol 291:R1040–R1048PubMedGoogle Scholar
  172. van Ginneken VJT, van den Thillart GEEJM (2000) Physiology: Eel fat stores are enough to reach the Sargasso. Nature 403:156–157PubMedGoogle Scholar
  173. Videler JJ (1993) Fish swimming. Chapman and Hall, LondonGoogle Scholar
  174. Von Herbing IH, White L (2002) The effects of body mass and feeding on metabolic rate in small juvenile Atlantic cod. J Fish Biol 61:945–958Google Scholar
  175. Wagner GN, Balfry SK, Higgs DA, Lall SP, Farrell AP (2004) Dietary fatty acid composition affects the repeat swimming performance of Atlantic salmon in seawater. Comp Biochem Physiol A 137:567–576Google Scholar
  176. Walton MJ, Cowey CB (1982) Aspects of intermediary metabolism in salmonid fish. Comp Biochem Physiol B 73:59–79Google Scholar
  177. Wang Y, Heigenhauser GJ, Wood CM (1994) Integrated responses to exhaustive exercise and recovery in rainbow trout white muscle: acid-base, phosphogen, carbohydrate, lipid, ammonia, fluid volume and electrolyte metabolism. J Exp Biol 195:227–258PubMedGoogle Scholar
  178. Watanabe T (2002) Strategies for further development of aquatic feeds. Fish Sci 68:242–252Google Scholar
  179. Weber J-M (2011) Metabolic fuels: regulating fluxes to select mix. J Exp Biol 214:286–294PubMedGoogle Scholar
  180. Weber J-M, Brill RW, Hochachka PW (1986) Mammalian metabolite flux rates in a teleost: lactate and glucose turnover in tuna. Am J Physiol Regul Integr Comp Physiol 250:R452–R458Google Scholar
  181. Weber J-M, Haman F (2004) Oxidative fuel selection: adjusting mix and flux to stay alive. In: Morris S, Vosloo A (eds) Animals and Environments. International congress series, vol 1275. Elsevier, Amsterdam, pp 22–31Google Scholar
  182. Weber J-M, Zwingelstein G (1995) Circulatory substrate fluxes and their regulation. In: Hochachka PW, Mommsen TP (eds) Metabolic biochemistry, vol 4. Biochemistry and molecular biology of fishes Elsevier, Amsterdam, pp 15–32Google Scholar
  183. West TG, Arthur PG, Suarez RK, Doll CJ, Hochachka PW (1993) In vivo utilization of glucose by heart and locomotory muscles of exercising rainbow trout (Oncorhynchus mykiss). J Exp Biol 177:63–79Google Scholar
  184. Wilson CM, Friesen EN, Higgs DA, Farrell AP (2007) The effect of dietary lipid and protein source on the swimming performance, recovery ability and oxygen consumption of Atlantic salmon (Salmo salar). Aquaculture 273:687–699Google Scholar
  185. Wilson RP (1994) Utilization of dietary carbohydrate by fish. Aquaculture 124:67–80Google Scholar
  186. Winder W, Holmes B, Rubink D, Jensen E, Chen M, Holloszy J (2000) Activation of AMP-activated protein kinase increases mitochondrial enzymes in skeletal muscle. J Appl Physiol 88:2219–2226PubMedGoogle Scholar
  187. Wood CM (1991) Acid-base and ion balance, metabolism, and their interactions, after exhaustive exercise in fish. J Exp Biol 160:285–308Google Scholar
  188. Wood CM (2001) Influence of feeding, exercise and temperature on nitrogen metabolism and excretion. In: Wright P, Anderson P (eds) Nitrogen excretion. Academic Press, London, pp 201–238Google Scholar
  189. Woodward JJ, Smith LS (1985) Exercise training and the stress response in rainbow trout, Salmo gairdneri Richardson. J Fish Biol 26:435–447Google Scholar
  190. Yogata H, Oku H (2000) The effects of swimming exercise on growth and whole-body protein and fat contents of fed and unfed fingerling yellowtail. Fish Sci 66:1100–1105Google Scholar
  191. Young PS, Cech JJ (1993) Improved growth, swimming performance, and muscular development in exercised-conditioned young-of-the-year striped bass (Morone saxatilis). Aquat Sci 50:703–707Google Scholar
  192. Young PS, Cech JJ (1994) Effects of different exercise conditioning velocities on the energy reserves and swimming responses in young-of-the-year striped bass (Morone saxatilis). Can J Fish Aquat Sci 51:1528–1534Google Scholar
  193. Zhou G, Myers R, Li Y, Chen Y, Shen X, Fenyk-Melody J, Wu M, Ventre J, Doebber T, Fujii N, Musi N, Hirshman MF, Goodyear LJ, Moller DE (2001) Role of AMP-activated protein kinase in mechanism of metformin action. J Clin Invest 108:1167–1174PubMedGoogle Scholar
  194. Zong H, Ren J, Young L, Pypaert M, Mu J, Birnbaum M, Shulman G (2002) AMP kinase is required for mitochondrial biogenesis in skeletal muscle in response to chronic energy deprivation. Proc Natl Acad Sci U S A 99:15983–15987PubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • L. J. Magnoni
    • 1
    • 2
  • O. Felip
    • 1
  • J. Blasco
    • 1
  • J. V. Planas
    • 1
    • 2
  1. 1.Departament de Fisiologia i Immunologia, Facultat de BiologiaUniversitat de BarcelonaBarcelonaSpain
  2. 2.Institut de Biomedicina de la Universitat de Barcelona (IBUB)BarcelonaSpain

Personalised recommendations