Skip to main content

Advertisement

Log in

Energy allocation and metabolic scope in early turbot, Scophthalmus maximus, larvae

  • Research Article
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

Early stages of marine fish larvae are characterized by fast growth while having a limited aerobic scope and an immature digestive system. In order to understand this apparent paradox, the study of energy allocation is a major necessity. Components of the energy budget of turbot (Scophthalmus maximus) larvae were determined during initial development (days 4–12) and the complete energy allocation budget is presented. It was observed that food absorption efficiency increased from 32 to 51% during the studied period, and so did the energy available for growth and metabolic purposes. The relative amount of energy for maintenance decreased from 71 to 36% of energy channelled to metabolism. Gross growth efficiency increased from 20 to 26% of ingested energy, and net growth efficiency decreased from 66 to 52% of assimilated energy. Reduction of net growth efficiency is the reflex of a higher metabolic rate in older larvae, due to increased costs of activity and growth. Evidence, indicating that metabolic scope of early turbot larva is unable to accommodate simultaneously high levels of growth and activity was found. Alternative strategies to accommodate the costs of growth and activity exist in turbot larvae, and may result in a trade-off between fast growth and viability. As larvae grow, the various physiological processes described get more efficient, and the metabolic scope increases.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Blight EG, Dyer WJ (1959) A rapid method for total lipid extraction and purification. Can J Biochem 37:911–917

    Google Scholar 

  • Brett JR, Glass R (1973) Metabolic rates and critical swimming speeds of sockeye salmon (Oncorhynchus nerka) in relation to size and temperature. J Fish Res bd Can 30:379–387

    Article  Google Scholar 

  • Brett JR, Groves TDD (1979) Physiological energetics. In: Hoar WS, Randall DJ, Brett JR (eds) Fish physiology, vol 8. Academic, New York, pp 279–352

    Google Scholar 

  • Cahu CL, Zambonino Infante JL (2001) Substitution of live food by formulated diets in marine fish larvae. Aquaculture 200:161–180

    Article  Google Scholar 

  • Cho CY, Slinger SJ, Bayley HS (1982) Bioenergetics of salmonid fishes: energy intake, expenditure and productivity. Comp Biochem Physiol B 73:25–41

    Article  Google Scholar 

  • Conceição LEC (1997) Growth in early life stages of fishes: an explanatory model. Ph.D. Thesis, Wageningen Agricultural University, The Netherlands

  • Conceição LEC, Houlihan DF, Verreth JAJ (1997a) Fast growth, protein turnover and costs of protein metabolism in yolk-sac larvae of the African catfish Clarias gariepinus. Fish Physiol Biochem 16:291–302

    Article  Google Scholar 

  • Conceição LEC, van der Meeren T, Verreth JAJ, Evjen MS, Houlihan DF, Fyhn HJ (1997b) Amino acid metabolism and protein turnover in larval turbot Scophthalmus maximus fed natural zooplankton or Artemia. Mar Biol 129:255–265

    Article  Google Scholar 

  • Conceição LEC, Dersjant-Li Y, Verreth JAJ (1998) Cost of growth in larval and juvenile African catfish (Clarias gariepinus) in relation to growth rate, food intake and oxygen consumption. Aquaculture 161:95–106

    Article  Google Scholar 

  • Cousin JCB, Baudin-Laurencin F (1985) Morphogenese de l’appareil digestif et de la vessie gazeuse du turbot, Scophthalmus maximus L. Aquaculture 47:305–319

    Article  Google Scholar 

  • Cunha I, Planas M (1995) Ingestion rates of turbot larvae (Scophthalmus maximus) using different sized live prey. ICES Mar Sci Symp 201:16–20

    Google Scholar 

  • Cunha I, Planas M (2003) Use of multivariate analysis to assess the nutritional condition of fish larvae from nucleic acids and protein content. Biol Bull 204:339–349

    Article  CAS  Google Scholar 

  • Elliot JM, Davison W (1975) Energy equivalents of oxygen consumption in animal energetics. Oecologia 19:195–201

    Article  Google Scholar 

  • Finn RN, Fyhn HJ, Henderson RJ, Evjen MS (1996) The sequence of catabolic substrate oxidation and enthalpy balance of developing embryos and yolk-sac larvae of turbot (Scophthalmus maximus L). Comp Biochem Physiol A 115:133–151

    Article  Google Scholar 

  • Finn RN, Ronnestad I, Meeren T, Fyhn HJ (2002) Fuel and metabolic scaling during the early life stages of Atlantic cod Gadus morhua. Mar Ecol Prog Ser 243:217–234

    Article  Google Scholar 

  • Finn RN, Rønnestad I (2003) The effect of acute changes in temperature and light on the aerobic metabolism of embryos and yolk-sac larvae of turbot (Scophthalmus maximus). Can J Fish Acuat Sci 60:1324–1331

    Article  Google Scholar 

  • Fry FEJ (1947) Effects of environment on animal activity. Publs Ont Fish Res Lab 55:5–62

    Google Scholar 

  • Fyhn HJ (1989) First-feeding of marine fish larvae: are the amino acids the source of energy? Aquaculture 80:111–120

    Article  Google Scholar 

  • Fyhn HJ (1990) Energy production in marine fish larvae with enphasis to FAA as potential fuel. In: Mellinger J (ed) Animal nutrition and transport processes, 1. Nutrition in wild and domestic animal. Comp Physiol Basel Karger 5:176–192

  • Giguère LA, Côté B, St-Pierre JF (1988) Metabolic rates scale isometrically in larval fishes. Mar Ecol Prog Ser 50:13–19

    Article  Google Scholar 

  • Glass NR (1969) Discussion of calculation of power functions with specifical reference to respiratory metabolism. J Fish Res bd Can 26:2643–2650

    Article  Google Scholar 

  • Gnaiger E (1983) Calculation on energetics and biochemical equivalents of respirometry oxygen consumption. In: Gnaiger E, Forstner H (eds) Polarographic oxygen sensors. Springer, Berlin Heidelberg New York, pp 337–345

  • Gnaiger E, Kemp RB (1990) Anaerobic metabolism in aerobic mammalian cells: information from the ratio of calorimetric heat flux and respirometric oxygen flux. Biochem Biophys Acta 1016:328–332

    CAS  PubMed  Google Scholar 

  • Govoni JJ, Boehlert GW, Watanabe Y (1986) The physiology of digestion in fish larvae. Environ Biol Fish 16:59–77

    Article  Google Scholar 

  • Higgs DM, Fuiman LA (1996) Ontogeny of visual and mechanosensory structure and function in Atlantic menhaden Brevoortia tyrannus. J Exp Biol 199:2619–2629

    CAS  PubMed  Google Scholar 

  • Houde ED (1987) Early life dynamic and recruitment variability. Am Fish Soc Symp 2:17–29

    Google Scholar 

  • Houlihan DF, Pannevis M, Heba H (1993) Protein synthesis in juvenile tilapia (Oreochromis mossambicus). J World Aquacult Soc 24:145–161

    Article  Google Scholar 

  • Houlihan DF, Pedersen BH, Steffensen JF, Brenchin J (1995) Protein synthesis growth and energetics in larval hearring (Clupea harengus) at different feeding regimes. Fish Physiol Biochem 14:195–208

    Article  CAS  Google Scholar 

  • Kiørboe T (1989) Growth in fish larvae, are they particularly efficient? Rapp P-v Reun Cons int Expl Mer 191:383–389

    Google Scholar 

  • Kiørboe T, Munk P, Richardson K (1987) Respiration and growth of larval herring Clupea harengus: relation between specific dynamic action and growth efficiency. Mar Ecol Prog Ser 40:1–10

    Article  Google Scholar 

  • Kiørboe T, Møhlenberg F (1987) Partitioning of oxygen consumption between maintenace and growth in developing herring Clupea harengus (L.) embryos. J Exp Mar Biol Ecol 111:99–108

    Article  Google Scholar 

  • Lowry OH, Rosenbrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the folin fenol reagent. J Biol Chem 193:265–275

    CAS  Google Scholar 

  • Lucas MC, Priede JC (1992) Utilization of metabolic scope in relation to feeding and activity by individual and grouped zebrafish, Brachydanio rerio (Hamilton-Buchanan). J Fish Biol 41:175–190

    Article  Google Scholar 

  • Miller TJ, Crowder LB, Rice JA, Marschall EA (1988) Larval size and recruitment mechanisms in fishes: towards a conceptual framework. Can J Fish Aquat Sci 45:1657–1670

    Article  Google Scholar 

  • Morais S, Koven W, Rønnestad I, Dinis MT, Conceição LEC (2005) Dietary protein/lipid ratio and lipid nature affects fatty acid absorption and metabolism in a teleost larva. Br J Nutr 93:813–820

    Article  CAS  Google Scholar 

  • Munilla-Morán R, Stark JR (1989) Protein digestion in early turbot larvae, Scophthalmus maximus L. Aquaculture 81:315–372

    Article  Google Scholar 

  • Munilla-Morán R, Stark JR, Barbour A (1990) The role of exogenous enzymes in digestion in cultured turbot larvae. Aquaculture 88:337–350

    Article  Google Scholar 

  • Oikawa S, Itazawa Y (1984) Allometric relationship between tissue respiration and body mass in carp. Comp Biochem Physiol A 77:415–418

    Article  Google Scholar 

  • Osse JWM, van den Boogaart JGM (1995) Fish larvae, development, allometric growth, and the aquatic environment. ICES Mar Sci Symp 201:21–34

    Google Scholar 

  • Pankhurst PM, Butler P (1996) Development of the sensory organs in the greenback flounder, Rhombosolea tapirina. Mar Freshw Behav Physiol 28:55–73

    Article  Google Scholar 

  • Peterson I, Wroblewski JS (1984) Mortality rate of fish in the pelagic ecosystem. Can J Fish Aquat Sci 41:1117–1120

    Article  Google Scholar 

  • Post JR, Lee JA (1996) Metabolic ontogeny of teleost fishes. Can J Fish Aquat Sci 53:910–923

    Article  Google Scholar 

  • Ricker WE (1979) Growth rate models. In: Hoar WS, Randall DJ, Brett JR (eds) Fish physiology, vol 8. Academic, London, pp 677–707

  • Rombough PJ (1994) Energy partitioning during fish development: additive and compensatory allocation of energy to support growth? Funct Ecol 8:178–186

    Article  Google Scholar 

  • Rønnestad I, Conceição LEC (2005) Aspects of protein and amino acids digestion and utilization by marine fish larvae. In: Starck JM, Wang T (eds) Physiological and ecological adaptations to feeding in vertebrates. Science Publishers, Enfield, New Hampshire, USA

  • Rønnestad I, Fyhn HJ, Gravningen K (1992) The importance of free amino acids to the energy metabolism of eggs and larvae of turbot (Scophthalmus maximus). Mar Biol 114:517–525

    Article  Google Scholar 

  • Rønnestad I, Thorsen A, Finn RN (1999) Fish larval nutrition: a review of recent advances in the roles of amino acids. Aquaculture 177:201–216

    Article  Google Scholar 

  • Salgado-Alvarez XA (1993) Mecanismos de transporte e balance bioxeoquímico de nitroxeno na Ria de Vigo. Ph.D thesis, University, Santiago de Compostela, Spain

  • Schmidt-Nielsen K (1984) Scaling. Why is animal size so important?. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Segner H, Storch V, Reinecker M, Kloas W, Hanke W (1993) A tabular overview of organogenesis in larval turbot (Scophthalmus maximus L.). ICES Mar Sci Symp 201:35–39

    Google Scholar 

  • Strickland JD, Parsons TR (1968) A practical handbook of seawater analysis. Bull Fish Res bd Can 167, 311p

  • Weihs D (1980) Energetic significance of changes in swimming modes durind growth of larval anchovy, Engraulis mordax. Fish Bull USA 77:597–604

    Google Scholar 

  • Wieser W (1985) Developmental and metabolic constraints of the scope for activity in young rainbow trout (Salmo gairdnerii). J Exp Biol 18:133–142

    Google Scholar 

  • Wieser W (1994) Cost of growth in cells and organisms: general rules and comparative aspects. Biol Rev 68:1–33

    Article  Google Scholar 

  • Wieser W, Forstner H, Medgyesy N, Hinterleitner S (1988) To switch or not to switch: partitioning of energy between growth and activity in larval cyprinids (Cyprinidae:Teleostei). Funct Ecol 2:499–507

    Article  Google Scholar 

  • Wieser W, Kaufmann R (1998) A note on interactions between temperature, viscosity, body size and swimming energetics in fish larvae. J Exp Biol 201:1369–1372

    PubMed  Google Scholar 

  • Yamashita Y, Bailey KM (1989) A laboratory study of the bioenergetics of larval walleye pollock, Theragra chalcogramma. Fish Bull 87:525–536

    Google Scholar 

Download references

Acknowledgments

This study was financially supported by the Comisión Interministerial de Ciencia y Tecnología (CICYT, Spain) under Project AGF 185/92. Isabel Cunha was supported by a doctoral fellowship from FCT–Program Praxis XXI–BD/3489/94. We would like to thank to E. Gomes, Animal Nutrition Laboratory, ICBAS, Porto, for the use of the calorimetric bomb; to M. López and J. Quiñones, ASM soft and Escuela de Peritos, Vigo, for the automation of the respirometric data capture, and finally; to J. Salgado-Alvarez and M.J. Pasó, Oceanography Laboratory, IIM, CSIC, Vigo, for the analysis of nitrogen compounds.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to I. Cunha.

Additional information

Communicated by S.A. Poulet, Roscoff.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Cunha, I., Conceição, L.E.C. & Planas, M. Energy allocation and metabolic scope in early turbot, Scophthalmus maximus, larvae. Mar Biol 151, 1397–1405 (2007). https://doi.org/10.1007/s00227-006-0576-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-006-0576-x

Keywords

Navigation