Skip to main content
SpringerLink
Log in

Essential fatty acids influence metabolic rate and tolerance of hypoxia in Dover sole (Solea solea) larvae and juveniles

  • Original Paper
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

Dover sole (Solea solea, Linneaus 1758) were raised from first feeding on brine shrimp (Artemia sp.) with different contents and compositions of the essential fatty acids (EFA) arachidonic acid (ARA, 20:4n − 6); eicosapentaenoic acid (EPA, 20:5n − 3), and docosahexaenoic acid (DHA, 22:6n − 3), and their metabolic rate and tolerance to hypoxia measured prior to and following metamorphosis and settlement. Four dietary Artemia preparations were compared: (1) un-enriched; (2) enriched with a commercial EFA mixture (Easy DHA SELCO Emulsion); (3) enriched with a marine fish oil combination (VEVODAR and Incromega DHA) to provide a high ratio of ARA to DHA, and (4) enriched with these fish oils to provide a low ratio of ARA to DHA. Sole fed un-enriched Artemia were significantly less tolerant to hypoxia than the other dietary groups. Larvae from this group had significantly higher routine metabolic rate (RMR) in normoxia, and significantly higher O2 partial pressure (PO2) thresholds in progressive hypoxia for their regulation of RMR (Pcrit) and for the onset of agitation, respiratory distress and loss of equilibrium. Metamorphosis was associated with an overall decline in RMR and increase in Pcrit, but juveniles fed on un-enriched Artemia still exhibited higher Pcrit and agitation thresholds than the other groups. Sole fed un-enriched Artemia had significantly lower contents of EFA in their tissues, both before and after settlement. Thus, enriching live feeds with EFA has significant effects on the respiratory physiology of sole early life stages and improves their in vivo tolerance to hypoxia. We found no evidence, however, for any effect of the ratio of ARA to DHA.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Bang A, Grønkjær P, Malte H (2004) Individual variation in the rate of oxygen consumption by zebrafish (Danio rerio). J Fish Biol 64:1285–1296

    Article  Google Scholar 

  • Behrens JW, Stahl HJ, Steffensen JF, Glud RN (2007) Oxygen dynamics around buried lesser sandeels, Ammodytes tobianus (Linnaeus 1758): mode of ventilation and oxygen requirements. J Exp Biol 210:1006–1014

    Article  Google Scholar 

  • Bell JG, McEvoy LA, Estevez A, Shields RJ, Sargent JR (2003) Optimising lipid nutrition in first-feeding flatfish larvae. Aquaculture 227:211–220

    Article  CAS  Google Scholar 

  • Bransden MP, Cobcroft JM, Battaglene SC, Morehead DT, Dunstan GA, Nichols PD, Kolkovski S (2005) Dietary 22:6n − 3 alters gut and liver structure and behaviour in larval striped trumpeter (Latris lineata). Aquaculture 243:331–344

    Article  CAS  Google Scholar 

  • Burleson ML, Smatresk NJ, Milsom WK (1992) Afferent inputs associated with cardioventilatory control in fish. In: Hoar WS, Randall DJ (eds) Fish physiology, vol 12B. Academic Press, New York, pp 390–426

    Google Scholar 

  • 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 seabass (Dicentrarchus labrax). J Exp Biol 209:3429–3439

    Article  CAS  Google Scholar 

  • Couturier C, McKenzie DJ, Galois R, Joassard L, Claireaux G (2007) Influence of water viscosity on bioenergetics of the common sole Solea solea: ventilation and metabolism. Mar Biol 152:803–814

    Article  Google Scholar 

  • Cunha I, Conceição LEC, Planas M (2007) Energy allocation and metabolic scope in early turbot, Scophthalmus maximus, larvae. Mar Biol 151:1397–1405

    Article  Google Scholar 

  • Dhert P, Lavens P, Sorgeloos P (1992) Stress evaluation: a tool for quality control of hatchery-produced shrimp and fish fry. Aquacult Eur 17:6–10

    Google Scholar 

  • Duthie GG (1982) The respiratory metabolism of temperature-adapted flatfish at rest and during swimming activity and the use of anaerobic metabolism at moderate swimming speeds. J Exp Biol 97:359–373

    CAS  PubMed  Google Scholar 

  • Finn RN, Rønnestad I, Fyhn HJ (1995a) Respiration, nitrogen and energy metabolism of developing yolk-sac larvae of Atlantic halibut (Hippoglossus hippoglossus L.). Comp Biochem Physiol 111A:647–671

    Article  CAS  Google Scholar 

  • Finn RN, Widdows J, Fyhn HJ (1995b) Calorespirometry of developing embryos and yolk-sac larvae of turbot (Scophthalmus maximus). Mar Biol 122:157–163

    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 

  • Folch J, Lees M, Stanley SGH (1957) A simple method for the isolation of total lipids from animal tissues. J Biol Chem 226:497–509

    CAS  Google Scholar 

  • Hunt von Herbing I, Boutilier RG (1996) Activity and metabolism of larval Atlantic cod Gadus morhua from Scotian shelf and Newfoundland source populations. Mar Biol 124:607–617

    Article  Google Scholar 

  • Hunt von Herbing I, Gallager SM, Halteman W (2001) Metabolic costs of pursuit and attack in early larval Atlantic cod. Mar Ecol Prog Ser 216:201–212

    Article  Google Scholar 

  • Ishibashi Y, Inoue K, Nakatsukasa H, Ishitani Y, Miyashita S, Murata O (2005) Ontogeny of tolerance to hypoxia and oxygen consumption of larval and juvenile red sea bream, Pagrus major. Aquaculture 244:331–340

    Article  Google Scholar 

  • Koven W, Barr Y, Lutzky S, Ben-Atia I, Weiss R, Harel M, Behrens P, Tandler A (2001) The effect of dietary arachidonic acid (20:4 n − 6) on growth, survival and resistance to handling stress in gilthead seabream (Sparus aurata) larvae. Aquaculture 193:107–122

    Article  CAS  Google Scholar 

  • Lefrançois C, Claireaux G (2003) Influence of ambient oxygenation and temperature on metabolic scope and scope for heart rate in the common sole Solea solea. Mar Ecol Prog Ser 259:273–284

    Article  Google Scholar 

  • Logue JA, Howell BR, Bell JG, Cossins AR (2000) Dietary n − 3 long-chain polyunsaturated fatty acid deprivation, tissue lipid composition, ex vivo prostaglandin production, and stress tolerance in juvenile Dover sole (Solea solea L.). Lipids 35:745–55

    Article  CAS  Google Scholar 

  • Lund I, Steenfeld SJ, Hansen BW (2007) Effect of dietary arachidonic acid, eicosapentaenoic acid and docosahexaenoic acid on survival, growth and pigmentation in larvae of common sole (Solea solea L.). Aquaculture 273:532–544

    Article  CAS  Google Scholar 

  • Macquart-Moulin C (1997) Locomotory responses and tolerance of larval and postlarval sole (Solea solea L.) to low oxygen concentrations. Mar Fresh Behav Physiol 30:55–74

    Article  Google Scholar 

  • McKenzie DJ (2001) Effects of dietary fatty acids on the respiratory and cardiovascular physiology of fish. Comp Biochem Physiol 128:607–621

    Article  CAS  Google Scholar 

  • McKenzie DJ (2005) Effects of dietary fatty acids on the physiology of environmental adaptation in fish. In: Starcke JM, Wang T (eds) Physiological and ecological adaptations to feeding in vertebrates. Science Publishers, Enfield, pp 363–388

    Google Scholar 

  • McKenzie DJ, Piraccini G, Steffensen JF, Bolis CL, Bronzi P, Taylor EW (1995) Effects of diet on spontaneous locomotor activity and oxygen consumption in Adriatic sturgeon (Acipenser naccarii). Fish Physiol Biochem 14:341–355

    Article  CAS  Google Scholar 

  • McKenzie DJ, Piraccini G, Papini N, Galli C, Bronzi P, Bolis CG, Taylor EW (1997) Oxygen consumption and ventilatory reflex responses are influenced by dietary lipids in sturgeon. Fish Physiol Biochem 16:365–379

    Article  CAS  Google Scholar 

  • McKenzie DJ, Piraccini G, Piccolella M, Steffensen JF, Bolis CL, Taylor EW (2000) Effects of dietary fatty acid composition on metabolic rate and responses to hypoxia in the European eel, Anguilla anguilla. Fish Physiol Biochem 22:281–296

    Article  CAS  Google Scholar 

  • McKenzie DJ, Wong S, Randall DJ, Egginton S, Taylor EW, Farrell AP (2004) The effects of sustained exercise and hypoxia on oxygen tensions in the red muscle of rainbow trout. J Exp Biol 207:3629–3637

    Article  CAS  Google Scholar 

  • McKenzie DJ, Pedersen PB, Jokumsen A (2007a) Aspects of respiratory physiology and energetics in rainbow trout families that differ in size-at-age and condition factor. Aquaculture 263:280–294

    Article  Google Scholar 

  • McKenzie DJ, Steffensen JF, Korsmeyer K, Whiteley NM, Bronzi P, Taylor EW (2007b) Swimming alters responses to hypoxia in the Adriatic sturgeon (Acipenser naccarii). J Fish Biol 70:651–658

    Article  CAS  Google Scholar 

  • Morais S, Narciso L, Dores E, Pousao-Ferreira P (2004) Lipid enrichment for Senegalese sole (Solea senegalensis) larvae: effect on larval growth, survival and fatty acid profile. Aquacult Int 12:281–298

    Article  CAS  Google Scholar 

  • Nonnotte G, Kirsch R (1978) Cutaneous respiration in seven seawater teleosts. Respir Physiol 35:111–118

    Article  CAS  Google Scholar 

  • Parra G, Yúfera M (2001) Comparative energetics during early development of two marine fish species, Solea senegalensis (Kaup) and Sparus aurata (L.). J Exp Biol 204:2175–2183

    CAS  PubMed  Google Scholar 

  • Randall DJ, McKenzie DJ, Abrami G, Bondiolotti GP, Natiello F, Bronzi P, Bolis L, Agradi E (1992) Effects of diet on responses to hypoxia in the sturgeon (Acipenser naccarii). J Exp Biol 170:113–125

    Google Scholar 

  • Rombough PJ (1998) Partitioning of oxygen uptake between the gills and skin in fish larvae: a novel method for estimating cutaneous oxygen uptake. J Exp Biol 201:1763–1769

    CAS  PubMed  Google Scholar 

  • Salhi M, Hernandez-Cruz CM, Bessonart M, Izquierdo MS, Fernandez-Palacios H (1999) Effect of different polar lipid levels and different n − 3 HUFA content in polar lipids on gut and liver histological structure of gilthead seabream (Sparus aurata) larvae. Aquaculture 179:253–263

    Article  CAS  Google Scholar 

  • Sargent J, Bell G, McEvoy L, Tocher D, Estevez A (1999a) Recent developments in the essential fatty acid nutrition of fish. Aquaculture 177:191–199

    Article  CAS  Google Scholar 

  • Sargent JR, Bell JG, McEvoy LA, Estevez A, Bell MV, Henderson RJ, Tocher DR (1999b) Lipid nutrition of marine fish during early development: current status and future directions. Aquaculture 179:217–229

    Article  CAS  Google Scholar 

  • Steffensen JF (1989) Some errors in the respirometry of water breathers: how to avoid and correct for them. Fish Physiol Biochem 6:49–59

    Article  CAS  Google Scholar 

  • Steffensen JF (2007) Oxygen consumption of fish exposed to hypoxia: Are they all oxyregulators or are any oxyconformers ? In: Brauner CJ, Suvajdzic K, Nilsson G, Randall DJ (eds) Fish physiology, fish toxicology and fisheries management: Proceedings of the 9th international symposium. Ecosystem Research Division publication EPA/600/R-07/010. United States Environmental Protection Agency, Athens, Georgia, pp 237–248

    Google Scholar 

  • Tago A, Yamamoto Y, Teshima S, Kanazawa A (1999) Effects of 1, 2-di-20:5-phosphatidylcholine (PC) and 1, 2-di-22:6-PC on growth and stress tolerance of Japanese flounder (Paralichthys olivaceus) larvae. Aquaculture 179:231–239

    Article  CAS  Google Scholar 

  • van den Thillart G, Dalla Via J, Vitali G, Cortesi P (1994) Influence of long-term hypoxia exposure on the energy metabolism of Solea solea. I. Critical O2 levels for aerobic and anaerobic metabolism. Mar Ecol Prog Ser 104:109–117

    Article  Google Scholar 

  • Weltzien F, Døving KB, Carr WES (1999) Avoidance reaction of yolk-sac larvae of the inland silverside Menidia beryllina (Atherinidae) to hypoxia. J Exp Biol 202:2869–2876

    PubMed  Google Scholar 

  • Wieser W (1995) Review article: energetics of fish larvae, the smallest vertebrates. Acta Physiol Scand 154:279–290

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors are grateful to Professor Thomas Kiørboe for the loan of the infrared video equipment. This research was partially funded by the Danish Directorate for Food Fisheries and Agri Business. Ivar Lund was supported by a DIFRES PhD fellowship. This is ISEM publication 2008-037.

Author information

Authors and Affiliations

  1. Danish Institute for Fisheries Research (DIFRES), Danish Technical University, The North Sea Centre, 9850, Hirtshals, Denmark

    D. J. McKenzie, I. Lund & P. B. Pedersen

  2. Institut des Sciences de l’Evolution de Montpellier (UMR 5554 CNRS-Université de Montpellier 2), Station Méditerranéenne de l’Environnement Littoral, 1, quai de la Daurade, 34200, Sète, France

    D. J. McKenzie

Authors
  1. D. J. McKenzie
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. I. Lund
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. P. B. Pedersen
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to D. J. McKenzie.

Additional information

Communicated by H. O. Pörtner.

Rights and permissions

Reprints and permissions

About this article

Cite this article

McKenzie, D.J., Lund, I. & Pedersen, P.B. Essential fatty acids influence metabolic rate and tolerance of hypoxia in Dover sole (Solea solea) larvae and juveniles. Mar Biol 154, 1041–1051 (2008). https://doi.org/10.1007/s00227-008-0998-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-008-0998-8

Keywords

Search

Navigation