Synopsis
Seasonal changes in blood, liver and muscle substrate (glucose, glycogen and lipid) concentrations and enzyme (pyruvate kinase (PyK), fructose diphosphatase (FDPase), NADP-isocitrate dehydrogenase (ICDH), malic enzyme (ME) and the hexose monophosphate shunt dehydrogenases (HMSD)) activities were assessed in ammocoete and metamorphosing stages of a stream stock of the landlocked sea lamprey, Petromyzon marinus L. In all developmental stages studied, muscle rather than liver tissue served as the main site of carbohydrate and fat storage. Blood glucose and muscle lipid exhibited a positive relationship while liver HMSD and muscle ME activity, a negative relationship, with ammocoete weight. These responses were attributed to a proliferation of red fibers and adipocytes in the ammocoete muscle as the time of metamorphosis approched. Muscle lipid stores of ammocoetes in their last year of larval life increased dramatically during the fall and winter preceding metamorphosis. Changes in tissue enzyme activity of ammocoetes in their last year of larval life indicated that the liver was the site of amino acid incorporation into fat while muscle was the site of lipogenesis from glucose. During the non-trophic period of metamorphosis, stored material was catabolized to provide energy for protein synthesis.
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References cited
Abraham, S., J. Madsen & I.L. Chaikoff. 1964. The influence of glucose on amino acid carbon incorporation into proteins, fatty acids, and carbon dioxide by lactating rat mammary gland slices. J. Biol. Chem. 239: 855–864.
Applegate, V.C. 1950. Natural history of the sea lamprey (Petromyzon marinus) in Michigan. U.S. Fish. Wild. Serv., Spec. Sci. Rep., Fish. Ser. 55: 1–237.
Ballard, F.J., R.W. Hanson & D.S. Kronfeld. 1969. Gluconeogenesis and lipogenesis in tissue from ruminant and nonruminant animals. Fed. Proc. 28: 218–231.
Beamish, F.W.H. 1964. Respiration of fishes with special emphasis on standard oxygen consumption. II. Influence of weight and temperature on respiration of several species. Ca. J. Zool. 42: 177–188.
Beamish, F.W.H. & I.C. Potter. 1972. Timing of changes in the blood, morphology, and behaviour of Petromyzon marinus during metamorphosis. J. Fish. Res. Board Can. 29: 1277–1282.
Beamish, F.W.H., A.J. Niimi & P.F.K.P. Lett. 1975. Bioenergetics of teleost fishes: environmental influences. pp. 187–209. In: L. Bolis, H. P. Maddrell & K. Schmidt-Nielson (ed.), Comparative Physiology — Functional Aspects of Structural Materials. North-Holland Publishing Co, Amsterdam.
Beamish, F.W.H. & I.C. Potter. 1975. The life cycle of the anadromous sea lamprey (Petromyzon marinus L.) in New Brunswick. J. Zool., Lond. 177: 57–72.
Bigelow, H.B. & W.C. Schroeder. 1953. Fishes of the Gulf of Maine. Fishery Bull. U.S. Fish. Wildl. Serv. 53: 1–577.
Boddeke, R., E.J. Slijper & A. Van Der Stelt. 1959. Histological characteristics of the body musculature of fishes in connection with their mode of life. Koninkl. Nederl. Akademie van Wetenschappen, Proc. C. 62: 576–588.
Bucher, T. & G. Pfleiderer. 1955. Pyruvate kinase from muscle. pp. 435–500. In: S.P. Colowick & N.O. Kaplan (ed.), Methods in Enzymology. Vol. I. Preparation and Assay of Enzymes. Academic Press, New York.
Bremer, J. & A.B. Wojtczak. 1972. Factors controlling the rate of fatty acid α-oxidation in rat liver mitochondria. Biochem. Biophys. Acta 280: 515–530.
Brett, J.R. 1964. The respiratory metabolism and swimming performance of young sockeye salmon. J. Fish. Res. Board Can. 21: 1183–1226.
Brett, J.R. & D.A. Higgs. 1970. Effect of temperature on the rate of fatty acid α-oxidation in rat liver mitochondria. Biochem. Biophys. Acta 280: 515–530.
Chavin, W. & J.E. Young. 1970. Factors in the determination of normal serum glucose levels of goldfish, Carassius auratus L. Comp. Biochem. Physiol. 33: 629–653.
Cleland, W.W., V.W. Thompson & R. E. Barden. 1969. Isocitrate dehydrogenase (TPN-specific) from pig heart. pp. 30–33. In: J.M. Lowenstein (ed.), Methods in Enzymology. Vol. XIII. Citric Acid Cycle. Academic Press.
Creaser, C.W. & C.S. Hann. 1929. The food of larval lampreys. Mich. Acad. Sci., Arts & Lett., PAP 10: 433–437.
D'Adamo, A.F. & D.E. Haft. 1965. An alternate pathway of α-ketoglutarate catabolism in the isolated, perfused rat liver. J. Biol. Chem. 240: 613–617.
Draper, N.R. & H. Smith. 1966. Applied regression analysis. John Wiley and Sons, Inc., London. 407 pp.
Farmer, G.J., F.W.H. Beamish & G.A. Robinson. 1975. Food consumption of the adult landlocked sea lamprey, Petromyzon marinus L. Comp. Physiol. Biochem. 50A: 753–757.
Folch, J., M. Lees & C.H. Sloane Stanley. 1957. A simple method for the isolation and purification of total lipids from animal tissues. J. Biol. Chem. 226: 497–509.
Fry, F.E.G, & P.W. Hochachka. 1970. Fish. pp. 79–134. In: G. C. Whittow. (ed.), Comparative Physiology of Thermoregulation. Vol. I. Invertebrates and Nonmammalian Vertebrates. Academic Press, New York.
Gage, S.H. 1928. The lampreys of New York State — life history and economics. Biological survey of the Oswega River System. Rep. N.Y. St. Conserv. Dept. 17 (Suppl.): 158–191.
George, J.C. 1962. A histophysiological study of the red and white muscles of the mackerel. Am. Midl. Nat. 68: 487–494.
George, J.C. & F.W.H. Beamish. 1974. Haemocytology of the supra-neural myeloid body in the sea lamprey during several phases of life cycle. Can. J. Zool. 52: 1585–1589.
Glaser, L. & D.H. Brown. 1955. Purification and properties of d-glucose-6-phosphate dehydrogenase. J. Biol. Chem. 216: 67–79.
Hardisty, M.W. 1961. The growth of larval lampreys. J. Anim. Ecol. 30: 357–371.
Hardisty, M.W. & I.C. Potter. 1971. The behaviour, ecology and growth of larval lampreys. In: M.W. Hardisty & I.C. Potter (ed.), The Biology of Lampreys 1: pp. 85–125. Academic Press, London.
Harper, H.A. 1975. Review of physiological chemistry. Lange Medical Publ., Los Altos, California. 570 pp.
Hill, B.J. & I.C. Potter. 1970. Oxygen consumption in ammocoetes of the lamprey Ichthyomyzon hubbsi Raney, J. Exp. Biol. 53: 47–57.
Hsu, R.Y. & H.A. Lardy. 1969. Malic enzyme. pp. 230–235. In: J.M. Lowenstein (ed.). Methods in Enzymology. Vol. XIII. Citric Acid Cycle. Academic Press.
Kuz'mina, V.V. & L.P. Zhilina. 1973. The ratio of glycogen concentrations in the liver and muscles of some freshwater teleost fishes. J. Ichthyol. 13: 623–627.
Leach, W.J. 1939. The endostyle and thyroid gland of the brook lamprey, Ichthyomyzon fossor. J. Morphol. 65: 549–605.
Leach, W.J. 1940. Occurrence and life history of the northern brook lamprey, Ichthyomyzon fossor, in Indiana. Copeia 1940: 21–34.
Leibson, L.G. 1972. Features of the metabolism and its endocrine regulation in fish with different motor activities. J. Evol. Biochem. Physiol. 8: 248–255.
Leveille, G.A. 1970. Adipose tissue metabolism: Influence of periodicity of eating and diet composition. Fed. Proc. 29: 1294–1301.
Lo, S., J.C. Russell & A.W. Taylor. 1970. Determination of glycogen in small tissue samples. J. Applied Physiol. 28: 234–236.
Low, D.R., 1972. Variations in body composition of pre-adult landlocked sea lamprey, Petromyzon marinus L. in relation to size and season. M. Sc. Thesis, University of Guelph, Canada. 78 pp.
Lowe, D.R., F.W.H. Beamish & I.C. Potter. 1973. Changes in the proximate body composition of the landlocked sea lamprey, Petromyzon marinus L. during larval life and metamorphosis. J. Fish. Biol. 5: 673–682.
Lowry, O.H., W.J. Rosebrough, A.L. Farr & R.J. Randall. 1951. Protein measurement with the folin phenol reagent. J. Biol. Chem. 193: 265–271.
Manion, P.J. 1967. Diatoms as food of larval sea lampreys in a small tributary of Northern Lake Michigan. Trans. Am. Fish. Soc. 96: 224–226.
Manion, P.J. & T.M. Stauffer. 1970. Metamorphosis of the landlocked sea lamprey, Petromyzon marinus. J. Fish. Res. Board Can. 27: 1735–1746.
Moore, J.W. 1972. Food, food selection, and consumption by larval sea lamprey, Petromyzon marinus Linnaeus, and american brook lamprey, Lampetra lamottenii (LeSueur). M.Sc. Thesis, University of Guelph, Canada. 359 pp.
Moore, J.W. & F.W.H. Beamish. 1973. Food of larval sea lamprey (Petromyzon marinus) and american brook lamprey (Lampetra lamottei). J. Fish, Res. Board Can. 30: 7–15.
Moore, J.W. & I.C. Potter. 1976a. A laboratory study on the feeding of larvae of the brook lamprey Lampetra planeri (Bloch). J. Animal Ecol. 45: 81–90.
Moore, J.W. & I.C. Potter. 1976b. Aspects of feeding and lipid deposition and utilization in the lampreys, Lampetra fluviatilis (L.) and Lampetra planeri (Bloch). J. Anim. Ecol. 45: 699–712.
Nagai, M. & S. Ikeda. 1971a. Carbohydrate metabolism in fish. I. Effects of starvation and dietary composition on the blood glucose and the hepatopancreatic glycogen and lipid contents in carp. Bull. Jap. Soc. Sci. Fish. 37: 404–409.
Nagai, M. & S. Ikeda . 1971b. Carbohydrate metabolism in fish. II. Effect of dietary composition on metabolism of glucose6–14C in carp. Bull. Jap. Soc. Sci. Fish. 37: 410–414.
Nagai, M. & S. Ikeda. 1972. Carbohydrate metabolism in fish. III. Effect of dietary composition on metabolism of glucose-U-14 C in carp. Bull. Jap. Soc. Sci. Fish. 38: 137–143.
Nie, N.H., C.H. Hull, J.G. Jenkins, K. Steinbrenner & D.H. Bent. 1975. Statistical package for the social sciences. McGraw-Hill Book Co., New York. 675 pp.
Peters, A. & B. Mackay. 1961. The structure and innervation of the myotomes of the lamprey. J. Anat. 95: 575–585.
Plisetskaya, E.M. 1968. Brain and heart glycogen content in some vertebrates and effect of insulin. Endocrinol. Exper. 2: 251–262.
Plisetskaya, E.M. & V.V. Kuz'mina. 1971. Glycemia level in the organs of cyclostomes and fishes. J. Ichthyol. 11: 948–958.
Plisetskaya, E.M. & V.V. Kuz'mina. 1972. Glycogen content in organs of Agnatha (Cyclostomata) and Fish (Pisces). J. Ichthyol. 12: 297–306.
Pontremoli, S. 1966. Fructose-1, 6-diphosphatase: I-rabbit liver (crystalline) pp. 625–631. In: Methods in enzymology. Vol. IX — Carbohydrate metabolism.
Rovainen, C.M., G.E. Lemcoe & A. Peterson. 1971. Structure and chemistry of glucose-producing cells in meningeal tissue of the lamprey. Brain Research. 30: 99–118.
Rovainen, C.M., O.H. Lowry & J.V. Passoneau. 1969. Levels of metabolites and production of glucose in the lamprey brain. J. Neurochem. 16: 1451–1458.
Saifer, A. & S. Gerstenfeld. 1958. The photometric microdetermination of blood glucose with glucose oxidase. J. Lab. Clin. Med. 51: 448–460.
Schroll, F. 1959. Zur Ernährungsbiologie der steirischen Ammocoeten Lampetra planeri (Bloch) und Eudontomyzon danfordi (Regan). Int. Rev. Ges. Hydrobiol. 44: 395–428.
Shul'man, G.E. 1974. Life cycles of fish-physiology and biochemistry. John Wiley and Sons, Inc., New York. 258 pp.
Taylor, B.J.R. 1965. The analysis of polymodal frequency distributions. J. Anim. Ecol. 34: 445–452.
Taylor, W.M. & M.L. Halperin. 1975. Effect of glutamate on, the control of fatty-acid synthesis in white adipose tissue of the rat. Eur. J. Biochem. 53: 411–418.
Tepperman, J. & H.M. Tepperman. 1970. Gluconeogenesis, lipogenesis and the Sherrington metaphor. Fed. Proc. 29: 1284–1293.
Washko, M.E. & E. W. Rice. 1961. Determination of glucose by an improved enzymatic procedure. Clin. Chem: 7: 542–545.
Wigley, R.L. 1959. Life history of the sea lamprey of Cayuga Lake, New York. U.S. Fish Wildl. Serv., Fish. Bull. 154 (59): 561–617.
Youson, J.H. 1970. Observations on the opisthonephric kidney of the sea lamprey of the Great Lakes, Petromyzon marinus L., at various stages during the life cycle. Can. J. Zool. 48: 1313–1316.
Zaragoza-Hermans, N.M. 1973. Studies on the metabolic effect induced in the rat by a high-fat diet. Eur. J. Biochem. 38: 170–179.
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O'Boyle, R.N., Beamish, F.W.H. Growth and intermediary metabolism of larval and metamorphosing stages of the landlocked sea lamprey, Petromyzon marinus L. Environ Biol Fish 2, 103–120 (1977). https://doi.org/10.1007/BF00005366
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DOI: https://doi.org/10.1007/BF00005366