Skip to main content
Log in

Seasonal variation of muscle metabolic organization in rainbow trout (Oncorhynchus mykiss)

  • Published:
Fish Physiology and Biochemistry Aims and scope Submit manuscript

Abstract

This study examined how muscle metabolic organization varied during an annual cycle in which rainbow trout (Oncorhynchus mykiss) were held in outdoor holding ponds in which they were exposed to natural changes in temperature (range 0.2 to 15.6°C) and photoperiod. We examined the activities of glycolytic and mitochondrial enzymes in red and white muscle to evaluate whether trout enhance their capacity for lipid and carbohydrate oxidation during cold-acclimization. When assayed at habitat temperature, the enzyme activities generally increased in spring to reach a maximum in summer followed by a decrease in the fall. This led to significantly higher activities at warm than cold periods for all enzymes measured in red muscle and all but one in white muscle. The activities at 10°C provided little evidence for compensatory adjustments of aerobic capacity. Particularly in red muscle, enzyme levels at 10°C were generally lower during cold than warm periods. The variation of enzyme activities throughout the cycle was not due to changes in protein concentration, as the same responses were observed when activities were expressed per g wet mass or per mg protein. Although the aerobic capacity did not increase with cold-acclimatization, the relative capacity for lipid oxidation was higher in winter than in summer trout. In contrast, the relative capacity for aerobic glycolysis was higher in summer than in winter trout. Thus, the metabolic capacities of trout muscle undergo seasonal reorganization.

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.

Similar content being viewed by others

References

  • Bailey, J.R. and Driedzic, W.R. 1993. Influence of low temperature acclimation on fate of metabolic fuels in rainbow trout (Oncorhynchus mykiss) hearts. Can. J. Zool. 71: 2167–2173.

    CAS  Google Scholar 

  • Bates, P.C. and Millward, D.J. 1983. Myofibrillar protein turnover. Biochem. J. 214: 587–592.

    PubMed  CAS  Google Scholar 

  • Blier, P. and Guderley, H. 1988. Metabolic responses to cold acclimation in the swimming musculature of lake whitefish,Coregonus clupeaformis. J. Exp. Zool. 246: 244–252.

    Article  CAS  Google Scholar 

  • Cunjak, R.A. 1988. Physiological consequences of overwintering in streams: the cost of acclimatization? Can. J. Fish. Aquat. Sci. 45: 443–452.

    Article  Google Scholar 

  • Cunjak, R.A. and Power, G. 1987. The feeding and energetics of stream-resident trout in winter. J. Fish Biol. 31: 493–511.

    Article  Google Scholar 

  • Cunjak, R.A., Curry, R.A. and Power, G. 1987. Seasonal energy budget of brook trout in streams: implications of a possible deficit in early winter. Trans. Am. Fish. Soc. 116. 817–828.

    Article  Google Scholar 

  • Dean, J.M. 1969. The metabolism of tissues of thermally acclimated trout (Salmo gairdneri). Comp. Biochem. Physiol. 29: 185–196.

    Article  PubMed  CAS  Google Scholar 

  • Egginton, S. and Sidell, B.D. 1989. Thermal acclimation induces adaptive changes in subcellular structure of fish skeletal muscle. Am. J. Physiol. 256 (Regulatory, Integrative Comp. Physiol. 25): R1–R9.

    PubMed  CAS  Google Scholar 

  • Elliott, J.M. 1991. Tolerance and resistance to thermal stress in juvenile Atlantic salmon,Salmo salar Freshw. Biol. 25: 61–70.

    Article  Google Scholar 

  • Elnageh, K.M. and Gaitonde, M.K. 1988. Effect of a deficiency of thiamine on brain pyruvate dehydrogenase: enzyme assay by three different methods. J. Neurochem. 51: 1482–1489.

    PubMed  CAS  Google Scholar 

  • Guderley, H. 1990. Functional significance of metabolic responses to thermal acclimation in fish muscles. Am. J. Physiol. 259 (Regulatory Integrative Comp. Physiol. 28): R245–R25.

    PubMed  CAS  Google Scholar 

  • Guderley, H. and Blier, P. 1988. Thermal acclimation in fish: conservative and labile properties of swimming muscle. Can. J. Zool. 66: 1105–1115.

    Article  Google Scholar 

  • Guderley, H. and Foley, L. 1990. Anatomic and metabolic responses to thermal acclimation in the ninespine stickleback,Pungitius pungitius. Fish Physiol. Biochem. 8: 465–473.

    Article  Google Scholar 

  • Guderley, H. and Gawlicka, A. 1992. Qualitative modification of muscle metabolic organization with thermal acclimation of rainbow trout,Oncorhynchus mykiss. Fish Physiol. Biochem. 10: 123–132.

    Article  CAS  Google Scholar 

  • Guderley, H., Lavoie, B.A. and Dubois, N. 1994. The interaction among age, thermal acclimation and growth rate in determining muscle metabolic capacities and tissue masses in the threespine stickleback,Gasterosteus aculeatus. Fish Physiol. Biochem. 13: 419–431.

    Article  CAS  Google Scholar 

  • Hazel, J.R. and Williams, E.E. 1990. The role of alterations in membrane lipid composition in enabling physiological adaptation of organisms to their physical environment. Progr. Lipid Res. 29: 167–227.

    Article  CAS  Google Scholar 

  • Heap, S.P., Watt, P.W. and Goldspink, G. 1985. Consequences of thermal change on the myofibrillar ATPase of five freshwater teleosts. J. Fish Biol. 26: 733–738.

    Article  CAS  Google Scholar 

  • Hinman, L.M. and Blass, J.P. 1981. An NADH-linked spectrophotometric assay for pyruvate dehydrogenase complex in crude tissue homogenates. J. Biol. Chem. 256: 6583–6586.

    PubMed  CAS  Google Scholar 

  • Hodges, T.K. and Leonard, R.T. 1974. Purification of plasma membrane bound adenosine triphosphatase from plant roots. Methods Enzymol. 22: 392–406.

    Article  Google Scholar 

  • Johnson, T.P., Bennett, A.F. and McLister, J.D. 1996. Thermal dependence and acclimation of fast start locomotion and its physiological basis in rainbow trout (Oncorhynchus mykiss). Physiol. Zool. 69: 276–292.

    CAS  Google Scholar 

  • Johnston, I.A. 1993. Phenotypic plasticity of fish muscle to temperature change.In Fish Ecophysiology. pp. 322–340. Edited by C. Rankin and F. Jensen, Chapman and Hall, London.

    Google Scholar 

  • Jones, P.L. and Sidell, B.D. 1982. Metabolic responses of striped bass (Morone saxatilis) to temperature acclimation. Il. Alterations in metabolic carbon sources and distributions of fibre types in locomotory muscle. J. Exp. Zool. 219: 163–171.

    Article  CAS  Google Scholar 

  • Kiessling, A., Storebakken, T., Åsgård, T., Andersson, I.L. and Kiessling, K.-H. 1989. Physiological changes in muscle of rainbow trout fed different ration levels. Aquaculture 79: 293–301.

    Article  Google Scholar 

  • Kleckner, N.W. and Sidell, B.D. 1985. Comparison of maximal activities of enzymes from tissues of thermally acclimated and naturally acclimatized chain pickerel (Esox niger). Physiol. Zool. 58: 18–28.

    CAS  Google Scholar 

  • Loughna, P.T. and Goldspink, G. 1985. Muscle protein synthesis rates during temperature acclimation in a eurythermal (Cyprinus carpio) and a stenothermal (Salmo gairdneri) species of teleost. J. Exp. Biol. 118: 267–276.

    CAS  Google Scholar 

  • McCauley, R.W., Elliott, J.R. and Read, L.A.A. 1977. Influence of acclimation temperature on preferred temperature in the rainbow trout (Salmo gairdneri). Trans. Am. Fish. Soc. 106: 362–365.

    Article  Google Scholar 

  • Milanesi, A.A. and Bird, J.W.C. 1972. Lysosomal enzymes in aquatic species II. Distribution and particle properties of thermally acclimated muscle lysosomes of rainbow trout,Salmo gairdneri. Comp. Biochem. Physiol. 41B: 573–591.

    Article  CAS  Google Scholar 

  • Miranda, E.J. and Hazel, J.R. 1996. Temperature-induced changes in the transbilayer distribution of phosphatidylethanolamine in mitoplasts of rainbow trout (Oncorhynchus mykiss) liver. J. Exp. Zool. 274: 23–32.

    Article  CAS  Google Scholar 

  • Newsholme, E.A. and Paul, J.M. 1983. The use ofin vitro enzyme activities to indicate the changes in metabolic pathways during acclimatisation.In Cellular Acclimatisation to Environmental Changes. pp. 81–101. Edited by A.R. Cossins and P. Sheterline, Cambridge University Press, London.

    Google Scholar 

  • Penney, R.K. and Goldspink, G. 1981. Short term temperature acclimation in myofibrillar ATPase of a stenothermSalmo gairdneri Richardson and an eurythermCarassius auratus. J. Fish Biol. 18: 715–721.

    Article  CAS  Google Scholar 

  • Ricker, W.E. 1980. Calculs et interprétation des statistiques biologiques des populations de poissons. Bull. Rish. Res. Bd. Canada 191F: 409 pp.

  • Sänger, A.M. 1993. Limits to the acclimatation of fish muscle. Rev. Fish Biol. Fish. 3: 1–15.

    Article  Google Scholar 

  • Scherrer, B. 1984. Biostatistique. Gaëtan Morin, Chicoutimi Québec.

    Google Scholar 

  • Segner, H. and Braunbeck, T. 1990. Adaptive changes of liver composition and structure in golden ide during winter acclimatization. J. Exp. Zool. 255: 171–185.

    Article  Google Scholar 

  • Smith, P.K., Krohn, R.I., Hermanson, G.T., Mallia, A.K., Gartner, F.H., Provenzano, M.D., Fujimoto, E.K., Goeke, N.M., Olson, B.J. and Klenk, D.C. 1985. Measurement of protein using bicinchoninic acid. Anal. Biochem. 150: 76–85.

    Article  PubMed  CAS  Google Scholar 

  • Somero, G.N. and Childress, J.J. 1990. Scaling of ATP-supplying enzymes, myofibrillar proteins and buffering capacity in fish muscle: relationship to locomotory habit. J. Exp. Biol. 149: 319–333.

    CAS  Google Scholar 

  • Taylor, S.E., Egginton, S., Taylor, E. 1996. Seasonal temperature acclimatisation of rainbow trout: cardiovascular and morphometric influences on maximal sustainable exercise level. J. Exp. Biol. 199: 835–845.

    PubMed  Google Scholar 

  • van Bohemen, Ch.G., Lambert, J.G.D. and Peute, J. 1981. Annual changes in plasma and liver in relation to vitellogenesis in the female rainbow trout,Salmo gairdneri. Gen. Comp. Endocrinol. 44: 94–107.

    Article  PubMed  Google Scholar 

  • van den Thillart, G. and Smit, H. 1984. Carbohydrate metabolism of goldfish (Carassius auratus L.). Effects of long term hypoxia-acclimation on enzyme patterns of red muscle, white muscle and liver. J. Comp. Physiol. 154B: 477–486.

    Google Scholar 

  • Vézina, D. and Guderley, H. 1991. Anatomic and enzymatic responses of the three-spined stickleback,Gasterosteus aculeatus, to thermal acclimation and acclimatization. J. Exp. Zool. 258: 277–287.

    Article  Google Scholar 

  • Voss, B. 1985. Effects of temperature on activity of pyruvate dehydrogenase in liver mitochondria of rainbow trout (Salmo gairdneri). J. Therm. Biol. 10: 131–135.

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Thibault, M., Blier, P.U. & Guderley, H. Seasonal variation of muscle metabolic organization in rainbow trout (Oncorhynchus mykiss). Fish Physiol Biochem 16, 139–155 (1997). https://doi.org/10.1007/BF00004671

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00004671

Keywords

Navigation