Abstract
To determine the effects of sustained swimming on the use and fate of dietary nutrients in gilthead sea bream, a group of fish were forced to undertake moderate and sustained swimming (1.5 BL s−1) for 3 weeks and compared with a control group undertaking voluntary activity. The exercise group showed a significant increase in specific growth rate (C: 1.13 ± 0.05; E: 1.32 ± 0.06 % day−1, P < 0.05) with no significant change in food intake (C: 3.56 ± 0.20; E: 3.84 ± 0.03 % of body weight). The addition of 13C-starch and 15N-protein to a single meal of 1 % ration allowed analysis of the fate of both nutrients in several tissues and in their components, 6 and 24 h after force-feeding. In exercised fish improved redistribution of dietary components increased the use of carbohydrates and lipid as fuels. Gilthead sea bream have a considerable capacity for carbohydrate absorption irrespective of swimming conditions, but in trained fish 13C rose in all liver fractions with no changes in store contents. This implies higher nutrient turnover with exercise. Higher retention of dietary protein (higher 15N uptake into white muscle during the entire post-prandial period) was found under sustained exercise, highlighting the protein-sparing effect. The combined effects of a carbohydrate-rich, low-protein diet plus sustained swimming enhanced amino acid retention and also prevented excessive lipid deposition in gilthead sea bream.
Similar content being viewed by others
References
Adams CE, Huntingford FA, Krpal J, Jobling M, Burnett SJ (1995) Exercise, agonistic behavior and food acquisition in Arctic charr Salvelinus alpinus. Environ Biol Fishes 43:213–218
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 162:259–268
Bagatto B, Pelster B, Burggren WW (2001) Growth and metabolism of larval zebrafish: effects of swim training. J Exp Biol 204:4335–4343
Basaran F, Ozbilgin H, Ozbilgin YD (2007) Comparison of the swimming performance of farmed and wild gilthead sea bream, Sparus aurata. Aquacult Res 38:452–456
Beltrán M, Fernández-Borrás J, Médale F, Pérez-Sánchez J, Kaushik S, Blasco J (2009) Natural abundance of 15N and 13C in fish tissues and the use of stable isotopes as dietary protein tracers in rainbow trout and gilthead sea bream. Aquacult Nutr 15:9–18
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 64:543–547
Boesgaard L, Nielsen ME, Rosenkilde P (1993) Moderate exercise decreases plasma cortisol levels in Atlantic salmon (Salmo salar). Comp Biochem Physiol A 106:641–643
Brauge C, Medale F, Corraze G (1994) Effect of dietary carbohydrate levels on growth, body composition and glycaemia in rainbow trout, Oncorhynchus mykiss, reared in seawater. Aquaculture 123:109–120
Brauge C, Corraze G, Médale F (1995) Effect of dietary levels of lipid and carbohydrate on growth-performance, body-composition, nitrogen-excretion and plasma-glucose levels in rainbow trout reared at 8-Degrees-C or 18-Degrees-C. Reprod Nutr Dev 35:277–290
Brauner CJ, Iwama GK, Randall DJ (1994) The effect of short-duration seawater exposure on the swimming performance of wild and hatchery-reared juvenile coho salmon (Oncorhyncus kisutch) during smoltifcation. Can J Fish Aquatic Sci 51:2188–2194
Brown EJ, Bruce M, Pether S, Herbert NA (2011) Do swimming fish always grow fast? Investigating the magnitude and physiological basis of exercise-induced growth in juvenile New Zealand yellowtail kingfish, Seriola lalandi. Fish Physiol Biochem 37:327–336
Caseras A, Metón I, Vives C, Egea M, Fernández F, Baanante IV (2002) Nutritional regulation of glucose-6-phosphatase gene expression in liver of the gilthead sea bream (Sparus aurata). Br J Nutr 88:607–614
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 68:2185–2191
Christiansen JS, Jørgensen EH, Jobling M (1991) Oxygen consumption in relation to sustained exercise and social stress in Arctic charr (Salvelinus alpinus). J Exp Zool 260:149–156
Company R, Calduch-Giner JA, Perez-Sanchez J, Kaushik SJ (1999) Protein sparing effect of dietary lipids in common dentex (Dentex dentex): a comparative study with sea bream (Sparus aurata) and sea bass (Dicentrarchus labrax). Aquat Living Resour 12:23–30
Couto A, Enes P, Peres H, Oliva-Teles A (2008) Effect of water temperature and dietary carbohydrate level on growth performance and metabolic utilization of diets in gilthead sea bream (Sparus aurata) juveniles. Comp Biochem Physiol A 151:45–50
Cowey CB, de la Higuera M, Adron JW (1977) The effect of dietary composition and of insulin on gluconeogenesis in rainbow trout (Salmo gairdneri). Br J Nutr 38:385–395
Davison W (1997) The effects of exercise training on teleost fish, a review of recent literature. Comp Biochem Physiol A 117:67–75
Davison W, Goldspink G (1977) The effect of prolonged exercise on the lateral musculature of the brown trout (Salmo trutta). J Exp Biol 70:1–12
Degani G, Viola S, Levanon D (1986) Effects of dietary carbohydrate source on growth and body composition of the European eel (Anguilla anguilla L.). Aquaculture 52:97–104
Enes P, Panserat S, Kaushik S, Oliva-Teles A (2006) Effect of normal and waxy maize starch on growth, food utilization and hepatic glucose metabolism in European sea bass (Dicentrarchus labrax) juveniles. Comp Biochem Physiol A 143:89–96
Enes P, Panserat S, Kaushik S, Oliva-Teles A (2008) Growth performance and metabolic utilization of diets with native and waxy maize starch by gilthead sea bream (Sparus aurata) juveniles. Aquaculture 274:101–108
Enes P, Panserat S, Kaushik S, Oliva-Teles A (2009) Nutritional regulation of hepatic glucose metabolism in fish. Fish Physiol Biochem 35:519–539
Enes P, Peres H, Couto A, Oliva-Teles A (2010) Growth performance and metabolic utilization of diets including starch, dextrin, maltose or glucose as carbohydrate source by gilthead sea bream (Sparus aurata) juveniles. Fish Physiol Biochem 36:903–910
Enes P, Panserat S, Kaushik S, Olive-Teles A (2011) Dietary carbohydrate utilization by European sea bass (Dicentrarchus labrax L.) and Gilthead sea bream (Sparus aurata L.) juveniles. Rev Fish Sci 19:201–215
Farrell AP, Johansen JA, Steffensen JF, Moyes CD, West TG, Suarez RK (1990) Effects of exercise training and coronary ablation on swimming performance, heart size, and cardiac enzymes in rainbow trout, Oncorhynchus mykiss. Can J Zool 68:1174–1179
Felip O, Ibarz A, Fernández-Borràs 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 107:834–844
Folch J, Lees M, Stanley GHS (1957) A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 226:497–509
Fraga F (1956) Determination of glycogen in shellfish with the anthrone reagent (Determinación de glucógeno en moluscos con el reactivo de antrona). Invest Pesq (Spain) 3–69
Gatlin DM III, Barrows FT, Brown P, Dabrowski K, Gaylord TG, Hardy RW, Herman E, Hu G, Krogdahl A, Nelson R, Overturf K, Rust M, Sealey W, Skonberg D, Souza EJ, Stone D, Wilson R, Wurtele E (2007) Expanding the utilization of sustainable plant products in aquafeeds: a review. Aquac Res 38:551–579
Good BCA, Cramer H, Somogy M (1933) The determination of glycogen. J Biol Chem 100–491
Hemre GI, Hansen T (1998) Utilisation of different dietary starch sources and tolerance to glucose loading in Atlantic salmon (Salmo salar), during parr-smolt transformation. Aquaculture 161:145–157
Hemre GI, Lie Ø, Lied E, Lambertsen G (1989) Starch as an energy source in feed for cod (Gadus morhua): digestibility and retention. Aquaculture 80:261–270
Hemre GI, Sandnes K, Lie Ø, Torrissen O, Waagbø R (1995) Carbohydrate nutrition in Atlantic salmon, Salmo salar L., growth and feed utilisation. Aquacult Res 26:149–154
Hemre GI, Mommsen TP, Krogdahl A (2002) Carbohydrates in fish nutrition: effects on growth, glucose metabolism and hepatic enzymes. Aquacult Nutr 8:175–194
Herbert NA, Kadri S, Huntingford FA (2011) A moving light stimulus elicits a sustained swimming response in farmed Atlantic salmon, Salmo salar L. Fish Physiol Biochem 37:317–325
Houlihan DF, Laurent P (1987) Effects of exercise training on the performance, growth, and protein-turnover of rainbow trout (Salmo gairdneri). Can J Fish Aquat Sci 44:1614–1621
Hung SSO, Fynn-Aikins K, Lutes PB, Xu R (1989) Ability of juvenile White sturgeon (Acipenser transmontanus) to utilize different carbohydrate sources. J Nutr 119:727–733
Jorgensen EH, Jobling M (1993) The effects of exercise on growth, food utilization and osmoregulatory capacity of juvenile Atlantic salmon, Salmo salar. Aquaculture 116:233–246
Kaushik SJ, Oliva-Teles A (1985) Effect of digestible energy on nitrogen and energy balance in rainbow trout. Aquaculture 50:89–101
Kaushik SJ, Seiliez I (2010) Protein and amino acid nutrition and metabolism in fish: current knowledge and future needs. Aquacult Res 41:322–332
Kirchner S, Kaushik S, Panserat S (2003) Low protein intake is associated with reduced hepatic gluconeogenic enzyme expression in rainbow trout (Oncorhynchus mykiss). J Nutr 133:2561–2564
Lenas DS, Triantafillou DJ, Chatziantoniou S, Nathanailides C (2011) Fatty acid profile of wild and farmed gilthead sea bream (Sparus aurata). J Verbrauch Lebensm 6:435–440
Magnoni L, Weber JM (2007) Endurance swimming activates trout lipoprotein lipase: plasma lipids as a fuel for muscle. J Exp Biol 210:4016–4023
Martin-Perez M, Fernández-Borràs J, Ibarz A, Millan-Cubillo A, Felip O, de Oliveira E, Blasco J (2012) New insights into fish swimming: a proteomic and isotopic approach in gilthead sea bream. J Proteome Res 11:3533–3547
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 55:476–488
Metón I, Mediavilla D, Caseras A, Canto E, Fernández F, Baanante IV (1999) Effect of diet composition and ration size on key enzyme activities of glycolysis–gluconeogenesis, the pentose phosphate pathway and amino acid metabolism in liver of gilthead sea bream (Sparus aurata). Br J Nutr 82:223–232
Metón I, Caseras A, Fernández F, Baanante IV (2000) 6-Phosphofructo-2-kinase/fructose-2,6-biphosphatase gene expression is regulated by diet composition and ration size in liver of gilthead sea bream, Sparus aurata. Biochim Biophys Acta 1491:220–228
Metón I, Caseras A, Fernández F, Baanante IV (2004) Molecular cloning of hepatic glucose-6-phosphatase catalytic subunit from gilthead sea bream (Sparus aurata): response of its mRNA levels and glucokinase expression to refeeding and diet composition. Comp Biochem Physiol B 138:145–153
Milligan CL, Girard SS (1993) Lactate metabolism in rainbow trout. J Exp Biol 180:175–193
Moon TW (2001) Glucose intolerance in teleost fish: fact or fiction? Comp Biochem Physiol B 129:243–249
Morrison DJ, Preston T, Bron JE, Hemderson RJ, Cooper K, Strachan F, Bell JG (2007) Authenticating production origin of Gilthead sea bream (Sparus aurata) by chemical and isotopic fingerprinting. Lipids 42:537–545
Nahhas R, Jones NV, Goldspink G (1982) Some aspects of sustained training of rainbow trout, Salmo gairdneri Richardson. J Fish Biol 20:351–358
Ozório ROA (2008) Swimming activity and non-protein energy (NPE) metabolism in fish. Curr Nutr Food Sci 4:282–289
Palstra AP, Planas JV (2011) Fish under exercise. Fish Physiol Biochem 37:259–272
Panserat S, Kaushik S (2002) Régulation nutritionelle du métabolisme glucidique chez les poissons: exemple de la truite arc-en-ciel (Oncorhynchus mykiss), faible utilisatrice des glucides alimentaires. INRA Prod Anim 15:109–117
Panserat S, Médale F, Blin C, Brèque J, Vachot C, Plagnes-Juan E, Gomes E, Krishnamoorthy R, Kaushik S (2000) Hepatic glucokinase is induced by dietary carbohydrates in rainbow trout, gilthead seabream and common carp. Am J Physiol Regul Integr Comp Physiol 278:1164–1170
Panserat S, Hortopan GA, Plagnes-Juan E, Kolditz C, Lansard M, Skiba-Cassy S, Esquerré D, Geurden I, Médale F, Kaushik S, Corraze G (2009) Differential gene expression after total replacement of dietary fish meal and fish oil by plant products in rainbow trout (Oncorhynchus mykiss) liver. Aquaculture 294:123–131
Papoutsoglou ES, Lyndon AR (2005) Effect of incubation temperature on carbohydrate digestion in important teleosts for aquaculture. Aquac Res 36:1252–1264
Peres H, Oliva-Teles A (2002) Utilization of raw and gelatinized starch by European sea bass (Dicentrarchus labrax) juveniles. Aquaculture 205:287–299
Peres H, Gonçalves P, Oliva-Teles A (1999) Glucose tolerance in Gilthead sea bream (Sparus aurata) and European seabass (Dicentrarchus labrax). Aquaculture 179:415–423
Sanchez-Muros MJ, Garcia-Rejon L, Lupianez JA, De la Higuera M (1996) Long-term nutricional effects on the primary liver and kidney metabolism in rainbow trout (Oncorhynchus mykiss). Adaptive response of glucose-6-phosphate dehydrogenase activity to high carbohydrate/low-protein and high-fat/non-carbohydrate diets. Aquacult Nutr 2:193–200
Santinha JM, Medale F, Corraze G, Gomes EFS (1999) Effects of the dietary protein: lipid ratio on growth and nutrient utilization in gilthead seabream (Sparus aurata L.). Aquacult Nutr 5:147–156
Saravanan S, Schrama JW, Figueiredo-Silva AC, Kaushik SJ, Verreth JAJ et al (2012) Constraints on energy intake in fish: the link between diet composition, energy metabolism, and energy intake in rainbow trout. PLoS ONE 7(4):e34743. doi:10.1371/journal.pone.0034743
Steinhausen MF, Steffensen JF, Andersen NG (2010) The effects of swimming pattern on the energy use of gilthead sea bream (Sparus aurata L.). Mar Freshwater Behav Physiol 43:227–241
Stephan G, Dreanno C, Guiollaume J, Arzel J (1996) Incidence of different amounts of proteins, lipids and carbohydrates in diets on the muscle lipid composition in the turbot (Scophthalmus maximus). Ichthyophysiol Acta 19:11–30
Stone DAJ (2003) Dietary carbohydrate utilization by fish. Rev Fish Sci 11:337–369
Stone DAJ, Allan GL, Anderson AJ (2003) Carbohydrate utilization by juvenile silver perch, Bidyanus bidyanus (Mitchell). III. The protein-sparing effect of wheat starch-based carbohydrates. Aquacult Res 34:123–134
Tacon AGJ, Marc M, Turchini GM, De Silva SS (2010) Responsible aquaculture and trophic level implications to global fish supply. Rev Fish Sci 18:94–105
Totland GK, Kryvi H, Jødestøl KA, Christiansen EN, Tangerås A, Slinde E (1987) Growth and composition of the swimming muscle of adult Atlantic salmon (Salmo salar L.) during long-term sustained swimming. Aquaculture 66:299–313
Venou B, Alexis MN, Fountoulaki E, Nengas I, Apostolopoulou M, Castritsi-Cathariou I (2003) Effect of extrusion of wheat and corn on gilthead sea bream (Sparus aurata) growth, nutrient utilization efficiency, rates of gastric evacuation and digestive enzyme activities. Aquaculture 225:207–223
Vergara JM, López-Calero G, Robaina L, Caballero MJ, Montero D, Izquierdo MS, Aksnes A (1999) Growth, feed utilization and body lipid content of gilthead seabream (Sparus aurata) fed increasing lipid levels and fish meals of different quality. Aquaculture 179:35–44
Vincent RE (1960) Some influences of domestication upon three stocks of brook trout (Salvelinus fontinalis). Trans Am Fisheries Soc 89:3–14
Watanabe T (2002) Strategies for further development of aquatic feeds. Fish Sci 68:242–252
Werner W, Rey HG, Wielinger H (1970) On the properties of a new chromogen for the determination of glucose in blood according to the GOD/POD-method. Z Analyt Chem 252:224
Wilson RP (1994) Utilization of dietary carbohydrate by fish. Aquaculture 124:67–80
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 66:1100–1105
Acknowledgments
We thank Pilar Teixidor and Pilar Rubio from the “Centre Científic i Tecnològic” (CCIT-UB) for their valuable help during isotopic analyses. This study was supported by a grant from the Spanish government (AGL2009-12427). O. Felip and M. Martín-Pérez received fellowships from FPI-2007 and FI-2007 of the Spanish government and the Catalan government, respectively. The English version was corrected by the Language Advisory Service of the University of Barcelona.
Conflict of interest
The authors declare that they have no conflict of interest.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by G. Heldmaier.
The experiments complied with the Guidelines of the European Union Council (86/609/EU), the Spanish Government (RD 1201/2005) and the University of Barcelona (specific ethics approval number for the protocol was CEEA-96/09) for the use of laboratory animals.
Rights and permissions
About this article
Cite this article
Felip, O., Blasco, J., Ibarz, A. et al. Beneficial effects of sustained activity on the use of dietary protein and carbohydrate traced with stable isotopes 15N and 13C in gilthead sea bream (Sparus aurata). J Comp Physiol B 183, 223–234 (2013). https://doi.org/10.1007/s00360-012-0703-6
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00360-012-0703-6