Abstract
Fish growth is strongly influenced by environmental and nutritional factors and changing culture conditions can help optimize it. The importance of early-life experience on the muscle phenotype later in life is well known. Here, we study the effects of 5 weeks of moderate and sustained swimming activity (5 BL s−1) in gilthead sea bream during early development. We analysed growth and body indexes, plasma IGF-I and GH levels, feed conversion, composition [proximate and isotopic (15N/13C)] and metabolic key enzymes (COX, CS, LDH, HOAD, HK, ALAT, ASAT) of white muscle. Moderate and continuous exercise in fingerlings of gilthead sea bream increased plasma IGF-I, whereas it reduced plasma GH. Under these conditions, growth rate improved without any modification to feed intake through an increase in muscle mass and a reduction in mesenteric fat deposits. There were no changes in the content and turnover of muscle proteins and lipid reserves. Glycogen stores were maintained, but glycogen turnover was higher in white muscle of exercised fish. A lower LDH/CS ratio demonstrated an improvement in the aerobic capacity of white muscle, while a reduction in the COX/CS ratio possibly indicated a functional adaptation of mitochondria to adjust to the tissue-specific energy demand and metabolic fuel availability in exercised fish. We discuss the synergistic effects of dietary nutrients and sustained exercise on the different mitochondrial responses.
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Antilla K, Jäntti M, Mänttäri S (2010) Effects of training on lipid metabolism in swimming muscles of sea trout (Salmo trutta). J Comp Physiol B 180:707–714
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 178:465–475
APROMAR (2014) La acuicultura en España 2014. http://www.apromar.es/content/la-acuicultura-en-españa-2014. Accessed 03 Aug 2015
Azuma T, Noda S, Yada T, Ototake M, Nagoya H, Moriyama S, Yamada H, Nakanishi T, Iwata M (2002) Profiles in growth, smoltification, immune function and swimming performance of 1-year-old masu salmon, Oncorhynchus masou masou reared in water flow. Fish Sci 68:1282–1294
Barrett BA, McKeown BA (1988a) Sustained exercise increases plasma growth hormone concentrations in two anadromous salmonids. Can J Fish Aquat Sci 45:747–749
Barrett BA, McKeown BA (1988b) Plasma growth hormone levels in Salmo gairderi: studies on temperature and exercise intensity/duration relationship. Comp Biochem Physiol A 94:791–794
Benedito-Palos L, Saera-Vila A, Calduch-Giner JA, Kaushik S, Pérez-Sánchez J (2007) Combined replacement of fish meal and oil in practical diets for fast growing juveniles of gilthead sea bream (Sparus aurata L.): networking of systemic and local components of GH/IGF axis. Aquaculture 267:199–212
Bermejo-Nogales A, Nederlof M, Benedito-Palos L, Ballester-Lozano GF, Folkedal O, Olsen RE, Sitjà-Bobadilla A, Pérez-Sánchez J (2014) Metabolic and transcriptional responses of gilthead sea bream (Sparus aurata L.) to environmental stress: new insights in fish mitochondrial phenotyping. Gen Comp Endocrinol 205:305–315
Bermejo-Nogales A, Calduch-Giner JA, Pérez-Sánchez J (2015) Unraveling the molecular signatures of oxidative phosphorylation to cope with the nutritionally changing metabolic capabilities of liver and muscle tissues in farmed fish. PLoS One 10(4):e0122889. doi:10.1371/journal.pone.0122889
Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37:911–917
Bradford M (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254
Buckley LJ, Bulow FJ (1987) Techniques for the estimation of RNA, DNA and protein. In: Summerfelt, Hall (eds) Age and growth of fish. Iowa State University Press, Ames, pp 345–357
Calduch-Giner JA, Echasseriau Y, Crespo D, Baron D, Planas JV, Prunet P, Pérez-Sánchez J (2014) Transcriptional assessment by microarray analysis and large-scale amd meta-analysis of the metabolic capacity of cardiac and skeletal muscle tissues to cope with reduced nutrient availability in gilthead sea bream (Sparus aurata L.). Mar Biotechnol 16:423–435
Cho CY, Slinger SJ, Bayley HS (1982) Bioenergetics of salmonid fishes: energy intake, expenditure and productivity. Comp Biochem Physiol B 73:25–41
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 68:2185–2191
Christiansen JS, Svendsen YS, Jobling M (1992) The combined effects of stocking density and sustained exercise on the behavior, food intake, and growth of juveniles Arctic charr (Salvelinus alpinus L.). Can J Zool 70:115–122
Claireaux G, Couturier C, Groison AL (2006) Effect of temperature on maximum swimming speed and cost of transport in juvenile European sea bass (Dicentrarchus labrax). J Exp Biol 209:3420–3428
Davison W (1997) Training and its effects on teleost fish. Comp Biochem Physiol A 94:1–10
Enders EC, Boisclair D, Roy AG (2004) Differences in the energetic cost of swimming in turbulent flow between wild, farmed and domesticated juvenile Atlantic salmon Salmo salar. J Fish Biol 65:317
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
Felip O, Blasco J, Ibarz A, Martín-Pérez M, Fernández-Borràs J (2013) 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
Forster IP, 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 62:404–409
Fraga F (1956) Determination of glycogen in shellfish with the anthrone reagent. Investig Pesq 3:69
Gómez-Requeni P, Mingarro M, Calduch-Giner JA, Médale F, Martin SAM, Houlihan DF, Kaushik S, Pérez-Sánchez J (2004) Protein growth performance, amino acid utilisation and somatotropic axis responsiveness to fish meal replacement by plant protein sources in gilthead sea bream (Sparus aurata). Aquaculture 232:493–510
Good BCA, Cramer H, Somogy M (1933) The determination of glycogen. J Biol Chem 100:491
Goolish EM, Adelman IR (1987) Tissue specific cytochrome-oxidase activity in largemouth bass: the metabolic costs of feeding and growth. Physiol Zool 60:454–464
Houlihan DF, Laurent P (1987) Effects of exercise training on the performance, growth, and turnover of rainbow trout (Salmo gairdneri). Can J Fish Aquat Sci 44:1614–1621
Ibarz A, Felip O, Fernández-Borràs J, Martín-Pérez M, Blasco J, Torrella JR (2011) Sustained swimming improves muscle growth and cellularity in gilthead sea bream. J Comp Physiol B 181:209–217
Jobling M, Baardvik BM, Christiansen JS, Jørgensen EH (1993) The effects of prolonged exercise training growth performance and production parameters in fish. Aquac Int 1:95–111
Johnston IA, Moon TW (1980) Exercise training in skeletal muscle of brook trout (Salvelinus fontinalis). J Exp Biol 87:177–194
Johnston IA, Moon TW (1981) Fine structure and metabolism of multiply innervated fast muscle fibers in teleost fish. Cell Tissue Res 219:93–109
Jӧnsson E, Bjӧrnsson BT (2002) Physiological functions of growth hormone in fish with special reference to its influence on behaviour. Fish Sci 68:742–748
Lauff RF, Wood CH (1996) Respiratory gas exchange, nitrogenous waste excretion, and fuel usage during aerobic swimming in juvenile rainbow trout. J Comp Physiol B 166:501–509
LeMoine CMR, Craig PM, Dhekney K, Kim JJ, McClelland GB (2010) Temporal and spatial patterns of gene expression in skeletal muscles in response to swim training in adult zebrafish (Danio rerio). J Comp Physiol B 180:151–160
Magnoni LJ, Felip O, Blasco J, Planas JV (2013) Metabolic fuel utilization during swimming: optimizing nutritional requirements for enhanced performance. In: Palstra AJ, Planas JV (eds) Swimming physiology of fish. Springer, Berlin, pp 203–235
Martínez-Barberá JP, Pendón C, Martí-Palanca H, Calduch-Giner JA, Rodríguez RB, Valdivia MM, Pérez-Sánchez J (1995) The use of recombinant gilthead sea bream (Sparus aurata) growth hormone for radioiodination and standard preparation in radioimmunoassay. Comp Biochem Physiol A 110:335–340
Martín-Pérez M, Fernández-Borràs J, Ibarz A, Felip O, Gutierrez J, Blasco J (2011) Stable isotope analysis combined with metabolic indices discriminates between gilthead sea bream (Sparus aurata) fingerlings produced in various hatcheries. J Agric Food Chem 59:10261–10270
Martín-Pérez M, Fernández-Borràs J, Ibarz A, Millán-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
McClelland GB, Scott GB (2013) Muscle plasticity. In: Evans, Clairbone, Currie (eds) The physiology of fishes. CRC Press, Boca Raton, pp 1–31
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 577:739–751
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 55:1208–1219
Mingarro M, Vega-Rubín de Celis S, Astola A, Pendón C, Valdivia MM, Pérez-Sánchez J (2002) Endocrine mediators of seasonal growth in gilthead sea bream (Sparus aurata): the growth hormone and somatolactin paradigm. Gen Comp Endocrinol 128:102–111
Morash AJ, Vanderveken M, McClelland GB (2014) Muscle metabolic remodeling in response to endurance exercise in salmonids. Front Physiol. doi:10.3389/fphys.00452
Nielsen ME, Boesgaard L, Sweeting RM, McKeown BA, Rosenkilde P (1994) Plasma levels of lactate, potassium, glucose, cortisol, growth-hormone and triiodo-l-thyrinine in rainbow trout (Oncorhynchus mykiss) during exercise at various levels for 24 h. Can J Zool 72:1643–1647
Pelletier D, Guderley H, Dutil JD (1993) Does the aerobic capacity of fish muscle change with growth rates? Fish Physiol Biochem 2:83–93
Pérez-Sánchez J, Le Bail PY (1999) Growth hormone axis as marker of nutritional status and growth performance in fish. Aquaculture 177:117–128
Pérez-Sánchez J, Weil C, Le Bail PY (1992) Effects of human insulin-like growth factor-I on release of growth hormone by rainbow trout, Oncorhynchus mykiss, pituitary cells. J Exp Zool 262:287–290
Reindl KM, Sheridan MA (2012) Peripheral regulation of the growth hormone-insulin-like growth factor system in fish and other vertebrates. Comp Biochem Physiol A 163:231–245
Sánchez-Gurmaches J, Cruz-García L, Ibarz A, Fernández-Borrás J, Blasco J, Gutiérrez J, Navarro I (2013) Insulin, IGF-I, and muscle MAPK pathway responses after sustained exercise and their contribution to growth and lipid metabolism regulation in gilthead sea bream. Domest Anim Endocrinol 45:145–153
Scott GR, Johnston IA (2012) Temperature during embryonic development has persistent effects on thermal acclimation capacity in zebrafish. Proc Natl Acad Sci USA 109:14247–14252
Shimizu M, Swanson P, Fukada H, Dickhoff W (2000) Comparison of extraction methods and assay validation for salmon insulin-like growth factor-I using commercially available components. Gen Comp Endocrinol 119:26–36
Srere PA (1969) Citrate synthase. In: Lowenstein, Kaplan, Colowick (eds) Methods of enzymology, vol 13. Academic Press, New York, pp 3–5
Steinhausen MF, Steffensen JF, Andersen NG (2010) The effects of swimming pattern on the energy use of gilthead seabream (Sparus aurata L.). Mar Freshw Behav Physiol 43:227–241
Tørud B, Hillestad M (2004) “Hjerterapporten”. Rapport om hjerteliderser hos laks of regnbueorret. http://www.fiskerifond.no/files/projects/attach/hjerterapporten.pdf
Vega-Rubin de Celis S, Gómez-Requeni P, Pérez-Sánchez J (2004) Production and characterization of recombinantly derived peptides and antibodies for accurate determinations of somatolactin, growth hormone and insulin-like growth factor-I in European sea bass (Dicentrarchus labrax). Gen Comp Endocrinol 139:266–277
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
The authors would like to thank Carlos Mazorra from Tinamenor S. L. and the personnel from the facilities at the School of Biology for the maintenance of the fish. We thank Pilar Teixidor and Pilar Rubio from the “Centre Científic i Tecnològic” (CCIT-UB) for valuable help during isotopic analyses. A.M.C and E.J.V. are supported by a predoctoral fellowship from the “Ministerio de Ciencia e Innovación” (MICINN) and A.M.P. by a fellowship from the University of Barcelona (APIF-2012). This study was supported by the projects from the MICINN AGL2012-39768, and the “Xarxa de Refèrencia d’R+D+I en Aqüicultura” and the SGR2009-00402 from the “Generalitat de Catalunya”. The English version has been corrected by the Language Advisory Service of the University of Barcelona.
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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.
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Blasco, J., Moya, A., Millán-Cubillo, A. et al. Growth-promoting effects of sustained swimming in fingerlings of gilthead sea bream (Sparus aurata L.). J Comp Physiol B 185, 859–868 (2015). https://doi.org/10.1007/s00360-015-0933-5
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DOI: https://doi.org/10.1007/s00360-015-0933-5