Fish Physiology and Biochemistry

, Volume 21, Issue 3, pp 223–233 | Cite as

Maintenance ration, protein synthesis capacity, plasma insulin and growth of Atlantic salmon (Salmo salar L.) with genetically different trypsin isozymes

  • K. Rungruangsak-Torrissen
  • C.G. Carter
  • A. Sundby
  • A. Berg
  • D.F. Houlihan


Growth was found to be associated with the changes of trypsin activity in the pyloric caecal tissues and the level of plasma insulin in Atlantic salmon (Salmo salar L.). A decrease in trypsin activity accompanied by an increase in plasma insulin was detected one month before an enhanced growth was observed. There were significant relationships between weight specific consumption rate, plasma insulin levels and fish growth. The correlation of weight specific consumption rate was higher with growth rate (R2=0.7, p<0.0001) than with plasma insulin concentration (R2=0.4, p<0.0001).

When the comparison was made between Atlantic salmon carrying and lacking the trypsin variant TRP-2*92, the fish with the variant had lower maintenance ration (p<0.05), higher capacity for protein synthesis in the white muscle (p<0.02), and a greater ability to utilize the feed at a restricted ration than the fish without the variant. In Atlantic salmon lacking the variant, both plasma insulin concentrations and growth rates were significantly lower (p<0.05) in the fish fed 0.5% bw day−1 than those fed 1% bw day−1. Whilst the growth rates of TRP-2*92 salmon fed the different rations became similar one month after similar levels of plasma insulin were observed between them. The TRP-2*92 salmon may be defined as a high protein growth efficiency fish with low protein turnover rate.

Genetic variation in trypsin isozyme pattern affects feed utilization, plasma insulin levels and growth in Atlantic salmon.

Atlantic salmon growth individual feed consumption rate plasma insulin protein synthesis capacity trypsin isozymes 


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  1. Ablett, R.F., Sinnhuber, R.O., Holmes, R.M. and Selivonchick, D.P. 1981. The effect of prolonged administration of bovine insulin in rainbow trout (Salmo gairdneri R.). Gen. Comp. Endocrinol. 43: 211–217.Google Scholar
  2. Almås, B., Pryme, I.F., Vedeler, A. and Hesketh, J.E. 1992. Insulin: Signal transmission and short term effects on the cytoskeleton and protein synthesis. Int. J. Biochem. 24: 183–191.Google Scholar
  3. Ashford, A.J. and Pain, V.M. 1986. Effect of diabetes on the rates of synthesis and degradation of ribosomes in rat muscle and liver in vivo. J. Biol. Chem. 261: 4059–4065.Google Scholar
  4. Austreng, E., Storebakken, T. and Åsgård, T. 1987. Growth rate estimates for cultured Atlantic salmon and rainbow trout. Aquaculture 60: 157–160.Google Scholar
  5. Bassompierre, M., Ostenfeld, T.H., McLean, E. and Rungruangsak-Torrissen, K. 1998. In vitro protein digestion, and growth of Atlantic salmon with different trypsin isozymes. Aquacult. Int. 6: 47–56.Google Scholar
  6. Carter, C.G., Houlihan, D.F., Buchanan, B. and Mitchell, A.I. 1993. Protein-nitrogen flux and protein growth efficiency of individual Atlantic salmon (Salmo salar L.). Fish Physiol. Biochem. 12: 305–315.Google Scholar
  7. Carter, C.G., Houlihan, D.F., Buchanan, B. and Mitchell, A.I. 1994. Growth and feed utilization efficiencies of seawater Atlantic salmon, Salmo salar L., fed a diet containing supplementary enzymes. Aquacult. Fish. Managem. 25: 37–46.Google Scholar
  8. Hesketh, J.E. and Campbell, G.P. 1987. Effects of insulin, pertussis toxin and cholera toxin on protein synthesis and diacylglycerol production in 3T3 fibroblasts: evidence for a G-protein mediated activation of phospholipase C in the insulin signal mechanism. BioSci. Rep. 7: 533–543.Google Scholar
  9. Hesketh, J.E., Campbell, G.P. and Reeds, P.J. 1986. Rapid response of protein synthesis to insulin in 3T3 cells: effects of protein kinase C depletion and differences from the response to serum repletion. BioSci. Rep. 6: 797–804.Google Scholar
  10. Houde, D.E. and Schekter, R.C. 1981. Growth rate, rations and cohort consumption of marine fish larvae in relation to prey concentration. Rapp. P.-V. Reun. Cons. Int. Explor. Mer 178: 441–453.Google Scholar
  11. Houlihan, D.F., McMillan, D.N. and Laurent, P. 1986. Growth rates, protein synthesis, and protein degradation rates in rainbow trout: Effects of body size. Physiol. Zool. 59: 482–493.Google Scholar
  12. Houlihan, D.F., Hall, S.J., Gray, C. and Nobel, B.S. 1988. Growth rates and protein turnover in cod, Gadus morhua. Can. J. Fish. Aquat. Sci. 45: 951–964.Google Scholar
  13. Ince, B.W. and Thorpe, A. 1978. The effects of insulin on plasma amino acid levels in the Northern pike, Esox lucius L. J. Fish Biol. 12: 503–506.Google Scholar
  14. Inui, Y., Arai, S. and Yokote, M. 1975. Gluconeogenesis in the eel. VI. Effects of hepatectomy, alloxan and mammalian insulin on the behaviour of plasma amino acids. Bull. Jap. Soc. Sci. Fish. 41: 1105–1111.Google Scholar
  15. Lowry, H.O., Rosebrough, N.J., Farr, A.L. and Randall, R.J. 1951. Protein measurement with Folin phenol reagent. J. Biol. Chem. 193: 265–275.Google Scholar
  16. Machado, C.R., Garofalo, M.A.R., Roselino, J.E.C., Kettelhut, I.C. and Migliorini, R.H. 1988. Effects of starvation, refeeding, and insulin on energy-linked metabolic processes in catfish (Rhamdia hilarii) adapted to a carbohydrate-rich diet. Gen. Comp. Endocrinol. 71: 429–437.Google Scholar
  17. McCarthy, I.D., Houlihan, D.F., Carter, C:G. and Moutou, K.A. 1993. Variation in individual food consumption rates of fish and its implications for the study of fish nutrition and physiology. Proc. Nutr. Soc. 52: 427–436.Google Scholar
  18. Plisetskaya, E.M., Dickhoff, W.W., Paquette, T.L. and Gorbman, A. 1986. The assay of salmon insulin by homologous radioimmunoassay. Fish Physiol. Biochem. 1: 37–43.Google Scholar
  19. Pringle, G.M., Houlihan, D.F., Callanan, K.R., Mitchell, A.I., Raynard, R.S. and Houghton, G.H. 1992. Digestive enzyme levels and histopathology of pancreas disease in farmed Atlantic salmon (Salmo salar). Comp. Biochem. Physiol. 102A: 759–768.Google Scholar
  20. Rungruangsak, K. and Utne, F. 1981. Effect of different acidified wet feeds on protease activities in the digestive tract and on growth rate of rainbow trout (Salmo gairdneri Richardson). Aquaculture 22: 67–79.Google Scholar
  21. Rungruangsak-Torrissen, K. 1993. Trypsin isozyme TRP-2(92): a growth marker in Atlantic salmon (Salmo salar L.) and its effect on digestion and absorption of dietary protein. Doctor philos. Thesis, University of Bergen, Norway.Google Scholar
  22. Rungruangsak-Torrissen, K., Pringle, G.M., Moss, R. and Houlihan, D.F. 1998. Effects of varying rearing temperatures on expression of different trypsin isozymes, feed conversion efficiency and growth in Atlantic salmon (Salmo salar L.). Fish Physiol. Biochem. 19:247–255.Google Scholar
  23. Schacterle, G.R. and Pollock, R.L. 1973. A simplified method for the quantitative assay of small amounts of protein in biologic material. Analyt. Biochem. 51: 654–655.Google Scholar
  24. Sundby, A., Eliassen, K., Refstie, T. and Plisetskaya, E.M. 1991a. Plasma levels of insulin, glucagon and glucagon-like peptide in salmonids of different weights. Fish Physiol. Biochem. 9: 223–230.Google Scholar
  25. Sundby, A., Eliassen, K.A., Blom, A.K. and Åsgård, T. 1991b. Plasma insulin, glucagon, glucagon-like peptide and glucose levels in response to feeding, starvation and life long restricted feed ration in salmonids. Fish Physiol. Biochem. 9: 253–259.Google Scholar
  26. Torrissen, K.R. 1984. Characterization of proteases in the digestive tract of Atlantic salmon (Salmo salar) in comparison with Rainbow trout (Salmo gairdneri). Comp. Biochem. Physiol. 77B: 669–674.Google Scholar
  27. Torrissen, K.R. 1987. Genetic variation of trypsin-like isozymes correlated to fish size of Atlantic salmon (Salmo salar). Aquaculture 62: 1–10.Google Scholar
  28. Torrissen, K.R. 1991. Genetic variation in growth rate of Atlantic salmon with different trypsin-like isozyme patterns. Aquaculture 93: 299–312.Google Scholar
  29. Torrissen, K.R. and Shearer, K.D. 1992. Protein digestion, growth and food conversion in Atlantic salmon and Arctic charr with different trypsin-like isozyme patterns. J. Fish Biol. 41: 409–415.Google Scholar
  30. Torrissen, K.R., Lied, E. and Espe, M. 1994. Differences in digestion and absorption of dietary protein in Atlantic salmon (Salmo salar) with genetically different trypsin isozymes. J. Fish Biol. 45: 1087–1104.Google Scholar
  31. Torrissen, K.R., Lied, E. and Espe, M. 1995. Differences in utilization of dietary proteins with varying degrees of partial prehydrolysis in Atlantic salmon (Salmo salar L.) with genetically different trypsin isozymes. In Biopolymers and Bioproducts: Structure, Function and Applications. pp. 432–442. Edited by J. Svasti, V. Rimphanitchayakit, A. Tassanakajorn, P. Pongsawasdi, B. Sonthayanon, K. Packdibamrung, S. Soontaros, T. Limpaseni, P. Wilairat, J. Boonjawat and S. Kamolsiripichaiporn. Proc. 11th FAOBMB Symp., Samakkhisan Public Company Limited, Bangkok.Google Scholar
  32. Torrissen, K.R., Male, R. and Nævdal, G. 1993. Trypsin isozymes in Atlantic salmon, Salmo salar L.: studies of heredity, egg quality and effect on growth of three different populations. Aquacult. Fish. Managem. 24: 407–415.Google Scholar

Copyright information

© Kluwer Academic Publishers 1999

Authors and Affiliations

  • K. Rungruangsak-Torrissen
    • 1
  • C.G. Carter
    • 2
  • A. Sundby
    • 3
  • A. Berg
    • 1
  • D.F. Houlihan
    • 2
  1. 1.Matre Aquaculture Research Station, Department of AquacultureInstitute of Marine ResearchMatredalNorway (Phone
  2. 2.Department of ZoologyUniversity of AberdeenAberdeenUK
  3. 3.Department of BiochemistryPhysiology and Nutrition, Norwegian School of Veterinary ScienceOsloNorway

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