Marine Biology

, Volume 154, Issue 6, pp 1041–1051 | Cite as

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

  • D. J. McKenzie
  • I. Lund
  • P. B. Pedersen
Original Paper


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, 22:6− 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.


Essential Fatty Acid Dietary Group Early Life Stage Hypoxia Tolerance Routine Metabolic Rate 
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.



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.


  1. Bang A, Grønkjær P, Malte H (2004) Individual variation in the rate of oxygen consumption by zebrafish (Danio rerio). J Fish Biol 64:1285–1296CrossRefGoogle Scholar
  2. 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 210:1006–1014CrossRefGoogle Scholar
  3. Bell JG, McEvoy LA, Estevez A, Shields RJ, Sargent JR (2003) Optimising lipid nutrition in first-feeding flatfish larvae. Aquaculture 227:211–220CrossRefGoogle Scholar
  4. 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 243:331–344CrossRefGoogle Scholar
  5. 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 390–426Google Scholar
  6. 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 209:3429–3439CrossRefGoogle Scholar
  7. 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 152:803–814CrossRefGoogle Scholar
  8. Cunha I, Conceição LEC, Planas M (2007) Energy allocation and metabolic scope in early turbot, Scophthalmus maximus, larvae. Mar Biol 151:1397–1405CrossRefGoogle Scholar
  9. Dhert P, Lavens P, Sorgeloos P (1992) Stress evaluation: a tool for quality control of hatchery-produced shrimp and fish fry. Aquacult Eur 17:6–10Google Scholar
  10. 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 97:359–373PubMedGoogle Scholar
  11. 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:647–671CrossRefGoogle Scholar
  12. Finn RN, Widdows J, Fyhn HJ (1995b) Calorespirometry of developing embryos and yolk-sac larvae of turbot (Scophthalmus maximus). Mar Biol 122:157–163CrossRefGoogle Scholar
  13. 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 243:217–234CrossRefGoogle Scholar
  14. Folch J, Lees M, Stanley SGH (1957) A simple method for the isolation of total lipids from animal tissues. J Biol Chem 226:497–509Google Scholar
  15. 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 124:607–617CrossRefGoogle Scholar
  16. Hunt von Herbing I, Gallager SM, Halteman W (2001) Metabolic costs of pursuit and attack in early larval Atlantic cod. Mar Ecol Prog Ser 216:201–212CrossRefGoogle Scholar
  17. 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 244:331–340CrossRefGoogle Scholar
  18. 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 193:107–122CrossRefGoogle Scholar
  19. 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 259:273–284CrossRefGoogle Scholar
  20. 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 35:745–55CrossRefGoogle Scholar
  21. 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 273:532–544CrossRefGoogle Scholar
  22. Macquart-Moulin C (1997) Locomotory responses and tolerance of larval and postlarval sole (Solea solea L.) to low oxygen concentrations. Mar Fresh Behav Physiol 30:55–74CrossRefGoogle Scholar
  23. McKenzie DJ (2001) Effects of dietary fatty acids on the respiratory and cardiovascular physiology of fish. Comp Biochem Physiol 128:607–621CrossRefGoogle Scholar
  24. 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 363–388Google Scholar
  25. 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 14:341–355CrossRefGoogle Scholar
  26. 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 16:365–379CrossRefGoogle Scholar
  27. 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 22:281–296CrossRefGoogle Scholar
  28. 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 207:3629–3637CrossRefGoogle Scholar
  29. 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 263:280–294CrossRefGoogle Scholar
  30. 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 70:651–658CrossRefGoogle Scholar
  31. 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 12:281–298CrossRefGoogle Scholar
  32. Nonnotte G, Kirsch R (1978) Cutaneous respiration in seven seawater teleosts. Respir Physiol 35:111–118CrossRefGoogle Scholar
  33. 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 204:2175–2183PubMedGoogle Scholar
  34. 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 170:113–125Google Scholar
  35. 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 201:1763–1769PubMedGoogle Scholar
  36. Salhi M, Hernandez-Cruz CM, Bessonart M, Izquierdo MS, Fernandez-Palacios H (1999) Effect of different polar lipid levels and different − 3 HUFA content in polar lipids on gut and liver histological structure of gilthead seabream (Sparus aurata) larvae. Aquaculture 179:253–263CrossRefGoogle Scholar
  37. Sargent J, Bell G, McEvoy L, Tocher D, Estevez A (1999a) Recent developments in the essential fatty acid nutrition of fish. Aquaculture 177:191–199CrossRefGoogle Scholar
  38. 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 179:217–229CrossRefGoogle Scholar
  39. Steffensen JF (1989) Some errors in the respirometry of water breathers: how to avoid and correct for them. Fish Physiol Biochem 6:49–59CrossRefGoogle Scholar
  40. 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 237–248Google Scholar
  41. 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 179:231–239CrossRefGoogle Scholar
  42. 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 104:109–117CrossRefGoogle Scholar
  43. 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 202:2869–2876PubMedGoogle Scholar
  44. Wieser W (1995) Review article: energetics of fish larvae, the smallest vertebrates. Acta Physiol Scand 154:279–290CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  1. 1.Danish Institute for Fisheries Research (DIFRES)Danish Technical UniversityHirtshalsDenmark
  2. 2.Institut des Sciences de l’Evolution de Montpellier (UMR 5554 CNRS-Université de Montpellier 2)SèteFrance

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