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Effects of dietary fatty acid composition on metabolic rate and responses to hypoxia in the European eel (Anguilla anguilla)

Fish Physiology and Biochemistry volume 22, pages 281–296 (2000)Cite this article

Abstract

European eels (Anguilla anguilla, L.) were fed on a commercial diet supplemented either with 15% by dry feed weight of menhaden oil (MO), an oil rich in highly unsaturated fatty acids of the n-3 series (n-3 HUFA), or with 15% by dry feed weight of coconut oil (CO), an oil composed primarily of saturated fatty acids (SFA). Following 90 days of feeding, the mean final masses of eels fed the two different oil supplements were similar, and higher than the mean final mass of a group fed the commercial diet alone. The diets created two distinct phenotypes of eels, distinguished by the fatty acid (FA) composition of their tissue lipids. Eels fed MO had significantly more total n-3 FA and n-3 HUFA in muscle and liver lipids than did eels fed CO, leading to higher n-3/n-6 and eicosapentaenoic acid/arachidonic acid ratios in the MO group. Measurements of O2 uptake (MO2) revealed that the MO group had a significantly lower routine metabolic rate (RMR) than the CO group. When exposed to progressive hypoxia, both groups regulated MO2 at routine normoxic levels until critical water O2 partial pressures that were statistically similar (9.62±1.08 kPa in MO versus 7.57±1.07 kPa in CO), beyond which they showed a reduction in MO2 below RMR. The MO group exhibited a significantly lower MO2 than the CO group throughout hypoxic exposure, but the percentage reductions in MO2 below their relative RMR were equal in both groups. During recovery to normoxia, both groups exhibited an increase in MO2 to rates significantly higher than their RMR. Throughout recovery, MO2 was significantly lower in the MO group compared with the CO group, but the percentage increases in MO2 relative to RMR were equal in both. During progressive hypoxia, neither group exhibited a marked ventilatory reflex response, both showed similar reductions in blood O2 partial pressure and content, and similar increases in plasma lactate. The results indicate that, although the n-3 HUFA-enriched MO group had a significantly lower routine metabolic rate than the CO group, the difference in aerobic metabolism did not influence the European eel's homeostatic regulation of MO2 in hypoxia.

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References

  • Abrami, G., Natiello, F., Bronzi, P., McKenzie, D.J., Bolis L. and Agradi, E. 1992. A comparison of highly unsaturated fatty acid levels in wild and farmed eels (Anguilla anguilla). Comp. Biochem. Physiol. 101B: 79-81.

    Google Scholar 

  • Agnisola, C., McKenzie, D.J., Taylor, E.W., Bolis, C.L. and Tota, B. 1996. Cardiac performance in relation to oxygen supply varies with dietary lipid composition in sturgeon. Am. J. Physiol. 271: R417-R425.

    Google Scholar 

  • Bell, J.G., Dick, J.R., McVicar, A.H., Sargent, J.R. and Thompson, K.D. 1993. Dietary sunflower, linseed and fish oils affect phospholipid fatty acid composition, development of cardiac lesions, phospholipase activity and eicosanoid production in Atlantic salmon (Salmo salar). Prostaglandins, Leukotrienes Essent. Fatty Acids 49: 665-673.

    Google Scholar 

  • Bell, J.G., McVicar, A.H., Park, M. and Sargent, J.R. 1991. High dietary linoleic acid affects fatty acid compositions of individual phospholipids from tissues of Atlantic salmon (Salmo salar): association with stress susceptibility and cardiac lesion. J. Nutr. 121: 1163-1172.

    Google Scholar 

  • Bell, J.G., Tocher, D.R., Farndale, B.M., Cox, D.I., McKinney, R.W. and Sargent, J.R. 1997. The effect of dietary lipid on polyunsaturated fatty acid metabolism in Atlantic salmon undergoing parr-smolt transformation. Lipids 32: 515-525

    Google Scholar 

  • Berg, T. and Steen, J.B. 1965. Physiological mechanisms for aerial respiration in the eel. Comp. Biochem. Physiol. 15: 469-484.

    Google Scholar 

  • Chan, D.K.O and Woo, N.Y.S. 1978. The respiratory metabolism of the Japanese eel, Anguilla japonica: effects of ambient oxygen, temperature, season, body weight and hypophysectomy. Gen. Comp. Endocrinol. 35: 160-168.

    Google Scholar 

  • Cowey, C.B. 1986. The role of nutritional factors in the prevention of peroxidative damage to tissues. Fish. Physiol. Biochem. 2: 171-178.

    Google Scholar 

  • Cruz-Neto, A.P., and Steffensen, J.F. 1997. The effects of acute hypoxia and hypercapnia on oxygen consumption of the freshwater European eel. J. Fish Biol. 50: 759-769.

    Google Scholar 

  • Dabrowski, K. 1994. Primitive actinopterygian fish can synthesize ascorbic acid. Experientia 50: 745-748.

    Google Scholar 

  • Egginton, S. 1996. Effect of temperature on optimal substrate for β-oxidation. J. Fish Biol. 49: 753-758.

    Google Scholar 

  • Folch, J., Lees, M. and Sloane-Stanley, G.H. 1957. A simple method for isolation and purification of total lipid from animal tissues. J. Biol. Chem. 226: 497-504.

    Google Scholar 

  • Gerbi, A., Zérouga, M., Debray, M., Durand, G., Chanez, C. and Bourre, J-M. 1994. Effect of fish oil diet on fatty acid composition of phospholipids of brain membranes and on kinetic properties of Na+,K+-ATPase isoenzymes of weaned and adult rats. J. Neurochem. 62: 1560-1569.

    Google Scholar 

  • Henderson, R.J. and Sargent, J.R. 1985. Chain-length specificities of mitochondrial and peroxisomal β-oxidation of fatty acids in livers of rainbow trout (Salmo gairdneri). Comp. Biochem. Physiol. 82B: 79-85.

    Google Scholar 

  • Henderson, R.J. and Tocher, D.R. 1987. The lipid composition and biochemistry of freshwater fish. Prog. Lipid Res. 26: 281-347.

    Google Scholar 

  • Hermesh, O., Kalderon, B. and Bar-Tana, J. 1998. Mitochondrial uncoupling by a long-chain fatty acyl analogue. J. Biol. Chem. 273: 3937-3942.

    Google Scholar 

  • Herreid, C.F. 1980. Hypoxia in invertebrates. Comp. Biochem. Physiol. 67A: 311-319.

    Google Scholar 

  • Hochachka, P.W. and Somero, G.N. 1984. Biochemical Adaptation. Princeton University Press, Princeton.

    Google Scholar 

  • Le Moigne, J., Soulier, P., Peyraud-Waitzenegger, M. and Peyraud, C. 1986. Cutaneous and gill O2 uptake in the European eel (Anguilla anguilla, L.) in relation to ambient Po2, 10-4000 torr. Respir. Physiol. 66: 341-354.

    Google Scholar 

  • Lands, W.E.M. 1991. Biosynthesis of prostaglandins. Ann. Rev. Nutr. 11: 41-60.

    Google Scholar 

  • McKenzie, D.J., Piraccini, G., Agnisola, C., Steffensen, J.F., Bronzi, P., Bolis, C.L., Tota, B. and Taylor, E.W. 1999. The influence of dietary fatty acid composition on the respiratory and cardiovascular physiology of Adriatic sturgeon (Acipenser naccarii): a review. J. Appl. Ichthyol. 15: 265-269.

    Google Scholar 

  • McKenzie, D.J., Piraccini, G., Papini, N., Galli, C., Bronzi, P., Bolis, C.G. and Taylor, E.W. 1997. Oxygen consumption and ventilatory reflex responses are influenced by dietary lipids in sturgeon. Fish Physiol. Biochem. 16: 365-379.

    Google Scholar 

  • McKenzie, D.J., Piraccini, G., Steffensen, J.F., Bolis, C.L., Bronzi, P. and Taylor, E.W. 1995. Effects of diet on spontaneous locomotor activity and oxygen consumption in Adriatic sturgeon (Acipenser naccarii). Fish Physiol. Biochem. 14: 341-355.

    Google Scholar 

  • McKenzie, D.J., Piraccini, G., Taylor, E.W., Steffensen, J.F., Bronzi, P. and Bolis, L. 1994. Effects of dietary lipids on responses to stress in fish. In: High Performance Fish. pp. 40-46. Edited by D.D. MacKinlay. American Fisheries Society, Vancouver.

    Google Scholar 

  • McKenzie, D.J., Serrini, G., Piraccini, G., Bronzi, P. and Bolis, C.L. 1996. Effects of diet on responses to exhaustive exercise in Nile tilapia (Oreochromis niloticus) acclimated to three different temperatures. Comp. Biochem. Physiol. 114A: 43-50

    Google Scholar 

  • Moreau, R., Dabrowski, K., Czesny, S. and Chila, F. 1999. Vitamin C-vitamin E interaction in juvenile lake sturgeon (Acipenser fulvescens R.), a fish able to synthesize ascorbic acid. J. Appl. Ichthyol. 15: 250-257.

    Google Scholar 

  • Paige, J.A., Liao, R.L., Hajjar, R.J., Foisy, R.L., Cory, C.R., O'Brien, P.J. and Gwathmey, J.K. 1996. Effect of a high omega-3 fatty acid diet on cardiac contractile performance in Oncorhynchus mykiss. Cardiovascular Res. 31: 249-262.

    Google Scholar 

  • Piquet, M.A., Fontaine, E., Sibille, B., Filippi, C., Keriel, C. and Leverve, X.M. 1996. Uncoupling effect of polyunsaturated fatty acid deficiency in isolated rat hepatocytes: Effect on glycerol metabolism. Biochem. J. 317: 667-674.

    Google Scholar 

  • Randall, D.J. 1982. The control of respiration and circulation in fish during exercise and hypoxia. J. Exp. Biol. 100: 275-285.

    Google Scholar 

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

    Google Scholar 

  • Rolfe, D.F.S. and Brown, G.C. 1997. Cellular energy utilisation and the molecular origin of standard metabolic rate in mammals. Physiol. Rev. 77: 731-758.

    Google Scholar 

  • Rowley, A.F., Knight, J., Lloyd-Evans, P., Holland, J.W. and Vickers, P.J. 1995. Eicosanoids and their role in immune modulation in fish. Fish Shellfish Immunol. 5: 549-567.

    Google Scholar 

  • Sidell, B.D. and Driedzic, W.R. 1985. Relationship between cardiac energy metabolism and cardiac work demand in fishes. In: Circulation, Respiration and Metabolism. pp. 381-401. Edited by R. Gilles. Springer-Verlag, Berlin.

    Google Scholar 

  • Smatresk, N.J. 1990. Chemoreceptor modulation of the endogenous respiratory rhythm in vertebrates. Am. J. Physiol. 228: R116-R125.

    Google Scholar 

  • Soivio, A., Westman, K. and Nyholm, K. 1972. Improved method of dorsal aortic catheterisation: haematological variables followed for three weeks in rainbow trout (Salmo gairdneri). Finnish Fish Res. 1: 11-21.

    Google Scholar 

  • Steffensen, J.F., Bushnell, P.G., Schurmann, H. 1994. Oxygen consumption in four species of teleosts from Greenland: no evidence of metabolic cold adaptation. Polar Biol. 14: 49-54.

    Google Scholar 

  • Tucker, V.A. 1967. Method for oxygen content and dissociation curves on microliter blood samples. J. Appl. Physiol. 23: 410-414.

    Google Scholar 

  • Ushio, H., Ohishima, T., Koizumi, C., Visuthi, V., Kiron, V. and Watanabe, T. 1997. Effect of dietary fatty acids on Ca2+-ATPase activity of the sarcoplasmic reticulum of Rainbow trout skeletal muscle. Comp. Biochem. Physiol. 118B: 681-691.

    Google Scholar 

  • Watanabe, T. 1982. Lipid nutrition in fish. Comp. Biochem. Physiol. 73B: 3-15.

    Google Scholar 

  • Wolf, K. 1963. Physiological salines for freshwater teleosts. Prog. Fish Cult. 25: 135-140.

    Google Scholar 

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Authors and Affiliations

  1. School of Biosciences, University of Birmingham, Birmingham, B15 2TT, UK

    D.J. McKenzie & E.W. Taylor

  2. Institute of Pharmacological Sciences, University of Milan, via Balzaretti, 9, 20133, Milano, Italy

    G. Piraccini, M. Piccolella & C.L. Bolis

  3. University of Copenhagen, Strandpromenaden 5, DK-3000, Helsingør, Denmark

    J.F. Steffensen

Authors
  1. D.J. McKenzie
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  2. G. Piraccini
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  3. M. Piccolella
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  4. J.F. Steffensen
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  5. C.L. Bolis
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  6. E.W. Taylor
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McKenzie, D., Piraccini, G., Piccolella, M. et al. Effects of dietary fatty acid composition on metabolic rate and responses to hypoxia in the European eel (Anguilla anguilla). Fish Physiology and Biochemistry 22, 281–296 (2000). https://doi.org/10.1023/A:1007865327923

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  • DOI: https://doi.org/10.1023/A:1007865327923

  • blood O2 content
  • menhaden oil
  • n-3 fatty acids
  • O2 uptake
  • plasma lactate
  • tissue lipids
  • ventilation

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