Summary
Many species of fish show a partial or complete thermal compensation of metabolic rate on acclimation from summer to winter temperatures. In the present study Crucian carp (Carassius carassius L.) were acclimated for two months to either 2° C or 28° C and the effects of temperature acclimation on mitochondrial content and capillary supply to myotomal muscles determined.
Mitochondria occupy 31.4% and 14.7% of slow fibre volume in 2°C- and 28° C-acclimated fish, respectively. Fast muscles of coldbut not warm-acclimated fish show a marked heterogeneity in mitochondrial volume. For example, only 5 % of fast fibres in 28° C-acclimated fish contain 5 % mitochondria compared to 34 % in 2° C-acclimated fish. The mean mitochondrial volume in fast fibres is 6.1 % and 1.6 % for coldand warm-acclimated fish, respectively.
Increases in the mitochondrial compartment with cold acclimation were accompanied by an increase in the capillary supply to both fast (1.4 to 2.9 capillaries/fibre) and slow (2.2 to 4.8 capillaries/fibre) muscles. The percentage of slow fibre surface vascularised is 13.6 in 28° C-acclimated fish and 32.1 in 2° C-acclimated fish. Corresponding values for fast muscle are 2.3 and 6.6 % for warm and cold-acclimated fish, respectively. Maximum hypothetical diffusion distances are reduced by approximately 23–30 % in the muscles of 2° C-compared to 28° C-acclimated fish. However, the capillary surface supplying 1 μ3 of mitochondria is similar at both temperatures.
Factors regulating thermal compensation of aerobic metabolism and the plasticity of fish muscle to environmental change are briefly discussed.
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Altringham JD, Johnston IA (1981) Quantitative histochemical studies on the peripheral innervation of cod (Gadus morhua) fast myotomal muscle fibres. J Comp Physiol 143:123–127
Baldwin KM, Hooker AM, Campbell PJ, Lewis RE (1978) Enzyme changes in neonatal skeletal muscle: effect of thyroid deficiency. Am J Physiol 235:C97-C102
Boddeke R, Slijper EJ, Van Der Stell A (1959) Histological characteristics of the body musculature of fishes in connection with their mode of life. K Ned Ak Wetensch Pro Ser C 62:576–588
Bone Q (1964) Patterns of muscular innervation in the lower chordates. Int Rev Neurobiol 6:99–147
Bone Q (1966) On the function of the two types of myotomal muscle fibre in elasmobranch fish. J Mar Biol Ass UK 46:321–349
Bone Q, Kicenuik J, Jones DR (1978) On the role of the different fibre types in fish myotomes at intermediate swimming speeds. Fish Bull 76:691–699
Bostrom SL, Johansson RG (1972) Enzyme activity patterns in white and red muscles of the eel (Anguilla anguilla) at different developmental stages. Comp Biochem Physiol (B) 42:533–542
Brown MD, Cotter MA, Hudlicka O, Vrbova G (1976) The effects of different patterns of muscle activity on capillary density, mechanical properties and structure of slow and fast rabbit muscles. Pflügers Arch 361:241–250
Cotter M, Hudlicka O, Pette D, Staudte H, Vrbova G (1973) Changes of capillary density and enzyme pattern in fast rabbit muscles during long-term stimulation. J Physiol (Lond) 230:34–35 P
Egginton S, Johnston IA (1981) A morphometric study of regional differences in muscle ultrastructure in the juvenile eel Anguilla anguilla. Cell Tissue Res (in press)
Flood PR (1979) The vascular supply of the three fibre types in the parietal trunk muscle of the Atlantic hagfish (Myxine glutinosa, L.). Microvasc Res 17:55–70
Folkow B, Halicka HD (1968) A comparison between “red” and “white” muscle with respect to blood supply, capillary surface area and oxygen uptake during rest and exercise. Microvasc Res 1:14
Granger HJ, Shepherd AP Jr (1973) Intrinsic microvascular control of tissue oxygen delivery. Microvasc Res 5:49–72
Greer-Walker MG, Emerson L (1978) Sustained swimming speeds and myotomal muscle function in the trout, Salmo gairdneri. J Fish Biol 13:475–481
Hanson RC, Stanley JG (1970) The effects of hypophysectomy and temperature acclimation upon the metabolism of the central mudminnow, Umbra limi (Kirtland). Comp Biochem Physiol 33:871–879
Hazel J (1972) The effect of temperature acclimation upon succinic dehydrogenase activity from the epaxial muscle of the common goldfish (Carassius auratus): lipid reactivation of the soluble enzyme. Comp Biochem Physiol 43 B:863–882
Hazel J, Prosser CL (1974) Molecular mechanisms of temperature compensation in poikilotherms. Physiol Rev 54:620–677
Holloszy JO, Booth FW (1976) Biochemical adaptations to endurance exercise in muscle. An Rev Physiol 38:272–291
Hudson RCL (1973) On the function of the white muscles of teleosts at intermediate swimming speeds. J Exp Biol 58:509–522
Johnston IA (1980) Specialisation of fish muscle. In: Goldspink DF (ed) Development and specialisations of muscle. Soc Exp Biol Seminar Series Symp 7:123–148
Johnston IA (1981a) Quantitative analysis of muscle breakdown during starvation in the marine flatfish Pleuronectes platessa. Cell Tissue Res 214:369–386
Johnston IA (1981b) Physiology of muscle in hatchery raised fish. In: Cowey C (ed) Physiology of salmonid cultivation. Comp Biochem Physiol Supply (in press)
Johnston LA, Bernard L (1981) The effects of acclimation to hypoxia on the capillary supply and mitochondrial content of tench (Tinea tinea) skeletal muscle fibres J. Muscle Res Cell, Motility (In press)
Johnston IA, Lucking M (1978) Temperature induced variation in the distribution of different types of muscle fibre in the goldfish (Carassius carassius L.). J Comp Physiol 124:111–116
Johnston IA, Maitland B (1980) Temperature acclimation in crucian carp, Carassius carassius L., morphometric analyses of muscle fibre ultrastructure. J. Fish Biol 17:113–125
Johnston IA, Moon TW (1980a) Exercise training in the skeletal muscles of brook trout (Salvelinus fontinalis). J Exp Biol 87:177–195
Johnston IA, Moon TW (1980b) Endurance exercise training in the fast and slow muscles of a teleost fish (Pollachius virens). J Comp Physiol 135:147–156
Johnston LA, Moon TW (1981) Fine structure and metabolism of multiply innervated fast muscle fibres in teleost fish. Cell Tissue Res 219:93–109
Johnston IA, Davison W, Goldspink G (1977) Energy metabolism of carp swimming muscles. J Comp Physiol 114:203–216
Jones PL, Sidell BD (1981) Metabolic responses of striped bass (Morone saxatilis) to temperature acclimation. II. Alterations in metabolic carbon sources and distributions of fiber types in locomotory muscles. J Exp Zool (in press)
Kanungo MS, Prosser CL (1959) Physiological and biochemical adaptation of goldfish to cold and warm temperatures-II. Oxygen consumption of liver homogenate; oxygen consumption and oxidative phosphorylation of liver mitochondria. J Cell Comp Physiol 54:265–274
Klicka J (1965) Temperature acclimation in goldfish: lack of evidence for hormonal involvement. Physiol Zool 38:177–189
Kryvi H (1977) Ultrastructure of the different fibre types in axial muscles of the sharks Etmopterus spinax and Galeus melastomus. Cell Tissue Res 184:287–300
Kryvi H, Flood PR, Gulyaev D (1980) The ultrastructure and vascular supply of the different fibre types in the axial muscle of the sturgeon Acipenser stellatus, Pallas. Cell Tissue Res 212:117–126
Lomo T (1976) The role of activity in the control of membrane and contractile properties of skeletal muscle. In: Thesleff S (ed) Motor innervation of skeletal muscle. Academic Press, London, pp 289–321
Müller W (1976) Subsarcolemmal mitochondria and capillarization of soleus muscle fibres in young rats subjected to an endurance training. A morphometric study. Cell Tissue Res 174:367–389
Nicol CJM, Johnston IA (1981) Energy metabolism of fastand slow-twitch muscle in the rat: thyroid hormone induced changes. J Comp Physiol 142:465–472
Pette D (1980) Plasticity of muscle. Walter de Gruyter&Co, Berlin New York, pp 685
Precht H (1958) Concepts of the temperature adaptation of unchanging reaction systems of cold blooded animals. In: Prosser CL (ed) Physiological adaptation. Washington DC: Am Physiol Soc, pp 50–78
Prosser CL (1973) Comparative animal physiology. WB Saunders, Philadelphia
Shaklee JB, Christiansen JA, Sidell BD, Prosser CL, Whitt GS (1977) Molecular aspects of temperature acclimation in fish: contributions of changes in enzymatic activities and isoenzyme patterns to metabolic reorganisation in the green sunfish. J Exp Zool 201:1–20
Sidell B (1977) Turnover of cytochrome c in skeletal muscle of green sunfish (Lepomis cyanellus R.) during thermal acclimation. J Exp Zool 169:233–250
Sidell BD (1980) Responses of goldfish (Carassius auratus L.) muscle to acclimation temperature: alterations in biochemistry and proportions of different fiber types. Physiol Zool 53:98–107
Smit H, Van den Berg RJ, Kijn-den Hartog I (1974) Some experiments on thermal acclimation in the goldfish (Carassius auratus L.). Neth J Zool 24:32–49
Somero GN (1978) Temperature adaptations of enzymes: Biological optimization through structurefunction compromises. An Rev Ecol Syst 9:1–29
Stevens ED (1979) The effect of temperature on tail beat frequency of fish swimming at constant velocity. Can J Zool 57:1628–1635
Thillart, Vanden G, Modderkolk J (1978) The effect of acclimation temperature on the activation energies of state III respiration and on the unsaturation of membrane lipids of goldfish mitochondria. Biochim Biophys Acta 510:38–51
Vrbova G (1980) Innervation and differentiation of muscle fibres. In: Goldspink DF (ed) Development and specialization of muscle. Soc Exp Biol Seminar Series Symp 7:37–50
Walesby NJ, Johnston IA (1980a) Fibre types in the locomotory muscles of an Antarctic teleost, Notothenia rossii: A histochemical, ultrastructural and biochemical study. Cell Tissue Res 208:143–164
Walesby NJ, Johnston IA (1980b) Temperature acclimation in brook trout muscle: adenine nucleotide concentrations, phosphorylation state and adenylate energy charge. J Comp Physiol 139:127–133
Weibel ER (1967) Stereological techniques for electron microscopic morphometry. In: Hayat HA (ed) Principles and techniques of electron microscopy. Van Nostrand Reinhold Comp, New York, Vol III
Wilson TL (1977) Interrelations between pH and temperature for the catalytic rate of the M4 isozyme of lactate dehydrogenase (EC.1.1.1.27) from goldfish (Carassius auratus L.). Arch Biochem Biophys 179:378–390
Winder WW, Baldwin KM, Terjung RL, Holloszy JO (1975) Effects of thyroid hormone administration on skeletal muscle mitochondria. Am J Physiol 228:1341–1345
Wokoma A, Johnston IA (1981) Lactate production at high sustainable cruising speeds in rainbow trout (Salmo gairdneri Richardson). J Exp Biol 90:361–364
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Johnston, I.A. Capillarisation, oxygen diffusion distances and mitochondrial content of carp muscles following acclimation to summer and winter temperatures. Cell Tissue Res. 222, 325–337 (1982). https://doi.org/10.1007/BF00213216
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DOI: https://doi.org/10.1007/BF00213216