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Fish muscle: the exceptional case of notothenioids

Fish Physiology and Biochemistry volume 35, pages 43–52 (2009)Cite this article

Abstract

Fish skeletal muscle is an excellent model for studying muscle structure and function, since it has a very well-structured arrangement with different fiber types segregated in the axial and pectoral fin muscles. The morphological and physiological characteristics of the different muscle fiber types have been studied in several teleost species. In fish muscle, fiber number and size varies with the species considered, limiting fish maximum final length due to constraints in metabolites and oxygen diffusion. In this work, we analyze some special characteristics of the skeletal muscle of the suborder Notothenioidei. They experienced an impressive radiation inside Antarctic waters, a stable and cold environment that could account for some of their special characteristics. The number of muscle fibers is very low, 12,700–164,000, in comparison to 550,000–1,200,000 in Salmo salar of similar sizes. The size of the fibers is very large, reaching 600 μm in diameter, while for example Salmo salar of similar sizes have fibers of 220 μm maximum diameter. Evolutionary adjustment in cell cycle length for working at low temperature has been shown in Harpagifer antarcticus (111 h at 0°C), when compared to the closely related sub-Antarctic species Harpagifer bispinis (150 h at 5°C). Maximum muscle fiber number decreases towards the more derived notothenioids, a trend that is more related to phylogeny than to geographical distribution (and hence water temperature), with values as low as 3,600 in Harpagifer bispinis. Mitochondria volume density in slow muscles of notothenioids is very high (reaching 0.56) and since maximal rates of substrate oxidation by mitochondria is not enhanced, at least in demersal notothenioids, volume density is the only means of overcoming thermal constraints on oxidative capacity. In brief, some characteristics of the muscles of notothenioids have an apparent phylogenetic component while others seem to be adaptations to low temperature.

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References

  • Balushkin A (2000) Morphology, classification, and evolution of notothenioid fishes of the Southern Ocean (Notothenioidei, Perciformes). J Ichthyol 40:S74–S109

    Google Scholar 

  • Bargelloni L, Marcato S, Zane L et al (2000) Mitochondrial phylogeny of notothenioids: a molecular approach to Antarctic fish evolution and biogeography. Syst Biol 49:114–129. doi:10.1080/10635150050207429

    Article  PubMed  CAS  Google Scholar 

  • Battram JC, Johnston IA (1991) Muscle growth in the Antartic teleost, Nothothenia neglecta (Nybelin). Antarct Sci 3:29–33. doi:10.1017/S0954102091000068

    Article  Google Scholar 

  • Bone Q (1978) Locomotor muscle. In: Hoar WS, Randall DJ (eds) Fish physiology, vol 7. Academic Press, New York, pp 361–424

    Google Scholar 

  • Boyle KL, Dillaman RM, Kinsey ST (2003) Mitochondrial distribution and glycogen dynamics suggest diffusion constraints in muscle fibers of the blue crab, Callinectes sapidus. J Exp Zoolog A Comp Exp Biol 297:1–16

    PubMed  Google Scholar 

  • Brodeur JC, Peck L, Johnston IA (2002) Feeding increases MyoD and PCNA expression in myogenic progenitor cells of Notothenia coriiceps. J Fish Biol 60:1475–1485

    Article  Google Scholar 

  • Brodeur JC, Calvo J, Clarke A et al (2003a) Myogenic cell cycle duration in Harpagifer species with sub-Antarctic and Antarctic distributions: evidence for cold compensation. J Exp Biol 206:1011–1016. doi:10.1242/jeb.00204

    Article  PubMed  Google Scholar 

  • Brodeur JC, Calvo J, Johnston IA (2003b) Proliferation of myogenic progenitor cells following feeding in the sub-Antarctic notothenioid fish Harpagifer bispinis. J Exp Biol 206:163–169. doi:10.1242/jeb.00052

    Article  PubMed  Google Scholar 

  • Cheng CC, DeVries AL (1991) The role of antifreeze glycopeptides and peptides in the freezing avoidance of cold-water fish. In: Prisco Gd (ed) Life under extreme conditions. Springer, Berlin Heidelberg New York, pp 1–14

    Google Scholar 

  • Cornelison D, Wold B (1997) Single-cell analysis of regulatory gene expression in quiescent and activated mouse skeletal muscle satellite cells. Dev Biol 191:270–283. doi:10.1006/dbio.1997.8721

    Article  PubMed  CAS  Google Scholar 

  • Cossins AR, Friedlander MJ, Prosser CL (1977) Correlations between behavioral temperature adaptations of goldfish and the viscosity and fatty acid composition of their synaptic membranes. J Comp Physiol [A] 120:109. doi:10.1007/BF00619309

    Article  CAS  Google Scholar 

  • Davison W, MacDonald JA (1985) A histochemical study of the swimming musculature of Antartic fish. NZ J Zool 12:473–483

    Google Scholar 

  • Devincenti CV, Díaz AO, Garcïa AM et al (2008) Pectoral fins of Micropogonias furnieri: a histochemical and ultrastructural study. Fish Physiol Biochem. doi:10.1007/s10695-008-9216-3

  • Dunn JF, Archer SD, Johnston IA (1989) Muscle fibre types and metabolism in post-larval and adult stages of Notothenoid fish. Polar Biol 9:213–223. doi:10.1007/BF00263769

    Article  Google Scholar 

  • Eastman JT (1993) Antarctic fish biology: evolution in an unique environment. Academic Press, New York

    Google Scholar 

  • Eastman JT (2005) The nature of the diversity of Antarctic fishes. Polar Biol 28:93–107. doi:10.1007/s00300-004-0667-4

    Article  Google Scholar 

  • Eastman JT, De Vries AL (1982) Buoyancy studies of Notothenioid fishes in McMurdo Sound, Antractica. Copeia 2:385–393. doi:10.2307/1444619

    Article  Google Scholar 

  • Eastman JT, Eakin R (2000) An updated species list for notothenioid fish (Perciformes; Notothenioidei), with comments on Antarctic species. Arch Fisch Meeresforsch 48:11–20

    Google Scholar 

  • Eastman JT, McCune A (2000) Fishes on the Antarctic continental shelf: evolution of a marine species flock? J Fish Biol 57:84–102

    Google Scholar 

  • Eastman JT, Sidell BD (2002) Measurements of buoyancy for some Antarctic notothenioid fishes from the South Shetland Islands. Polar Biol 25:753–760

    Google Scholar 

  • Egginton S, Sidell BD (1989) Thermal acclimation induces adaptive changes in subcellular structure of fish skeletal muscle. Am J Physiol 256:1–9

    Google Scholar 

  • Fernández DA (2000) Caracterización histoquimica, distribución y crecimiento de las fibras musculares en Nototenidos subantárticos. Análisis inicial de dos factores relacionados con la natación: flotabilidad y temperatura. Biology Department. Universidad de Buenos Aires, Buenos Aires

    Google Scholar 

  • Fernández DA, Calvo J, Johnston IA (1999) Characterisation of the swimming muscles of two sub-Antarctic Notothenioids. Sci Mar 201:477–484

    Article  Google Scholar 

  • Fernández DA, Calvo J, Franklin CE et al (2000) Muscle fibre types and size distribution in sub-antarctic notothenioid fishes. J Fish Biol 56:1295–1311. doi:10.1111/j.1095-8649.2000.tb02144.x

    Article  Google Scholar 

  • Fernández DA, Calvo J, Wakeling JM et al (2002) Escape performance in the sub-Antarctic notothenioid fish Eleginops maclovinus. Polar Biol 25:914–920

    Google Scholar 

  • Gauvry L, Ennion S, Ettelaie C et al (2000) Characterisation of red and white muscle myosin heavy chain gene coding sequences from Antarctic and tropical fish. Comp Biochem Physiol B 127:575–588. doi:10.1016/S0305-0491(00)00286-8

    Article  PubMed  CAS  Google Scholar 

  • Guderley H (2004) Metabolic responses to low temperature in fish muscle. Biol Rev Camb Philos Soc 79:409–427. doi:10.1017/S1464793103006328

    Article  PubMed  Google Scholar 

  • Harrison P, Nicol CJM, Johnston IA (1987) Gross morphology, fibre composition and mechanical properties of pectoral fin muscles in the Antartic teleost Notothenia neglecta Nybelin. Proceedings of the V Congress of European Ichthyology, Stockholm, pp 459–465

  • Hazel JR, Williams EE (1990) The role of alterations in membrane lipid composition in enabling physiological adaptation of organisms to their physical environment. Prog Lipid Res 29:167–227. doi:10.1016/0163-7827(90)90002-3

    Article  PubMed  CAS  Google Scholar 

  • Hollway G, Currie P (2005) Vertebrate myotome development. Birth Defects Res C Embryo Today 75:172–179. doi:10.1002/bdrc.20046

    Article  PubMed  CAS  Google Scholar 

  • Jobling M (1995) Fish bioenergetics. Chapman & Hall, London

    Google Scholar 

  • Johnston IA (1981) Structure and function of fish muscle. Symp Zool Soc Lond 48:71–113

    CAS  Google Scholar 

  • Johnston IA (1982) Capillarisation, oxygen diffusion distances and mitochondrial content of carp muscles following acclimation to summer and winter temperatures. Cell Tissue Res 222:325–337. doi:10.1007/BF00213216

    Article  PubMed  CAS  Google Scholar 

  • Johnston IA (1987) Respiratory characteristics of muscle fibres in a fish (Chaenocephalus aceratus) that lacks haem pigments. J Exp Biol 133:415–428

    PubMed  CAS  Google Scholar 

  • Johnston IA (1993) Temperature influences muscle differentiation and the relative timing of organogenesis in herring (Clupea harengus) larvae. Mar Biol (Berlin) 116:363–379. doi:10.1007/BF00350053

    Article  Google Scholar 

  • Johnston IA (2003) Muscle metabolism and growth in Antarctic fishes (suborder Notothenioidei): evolution in a cold environment. Comp Biochem Physiol B Biochem Mol Biol 136:701–713. doi:10.1016/S1096-4959(03)00258-6

    Article  PubMed  Google Scholar 

  • Johnston IA, Patterson S, Ward W et al (1974) The histochemical demonstration of myofibrillar adenosine triphosphatase activity in fish muscle. Can J Zool 52:871–877. doi:10.1139/z74-118

    Article  PubMed  CAS  Google Scholar 

  • Johnston IA, Camm JP, White M (1988) Specialisations of swimming muscles in the pelagic Antarctic fish Pleuragramma antarcticum. Mar Biol 100:3–12. doi:10.1007/BF00392949

    Article  Google Scholar 

  • Johnston IA, Calvo J, Guderley H et al (1998) Latitudinal variation in the abundance and oxidative capacities of muscle mitochondria in perciform fishes. J Exp Biol 201:1–12

    PubMed  CAS  Google Scholar 

  • Johnston I, Vieira VL, Fernandez DA et al (2003a) Muscle growth in Polar fish: a study of Harpagifer species with sub-Antarctic and Antarctic distributions. Fish Sci 68:1023–1028

    Google Scholar 

  • Johnston IA, Fernández DA, Calvo J et al (2003b) Reduction in muscle fibre number during the adaptive radiation of notothenioid fishes: a phylogenetic perspective. J Exp Biol 206:2595–2609. doi:10.1242/jeb.00474

    Article  PubMed  Google Scholar 

  • Johnston IA, Abercromby M, Vieira VL et al (2004) Rapid evolution of muscle fibre number in post-glacial populations of Arctic charr Salvelinus alpinus. J Exp Biol 207:4343–4360. doi:10.1242/jeb.01292

    Article  PubMed  Google Scholar 

  • Kinsey ST, Pathi P, Hardy KM et al (2005) Does intracellular metabolite diffusion limit post-contractile recovery in burst locomotor muscle? J Exp Biol 208:2641–2652. doi:10.1242/jeb.01686

    Article  PubMed  CAS  Google Scholar 

  • Kinsey ST, Hardy KM, Locke BR (2007) The long and winding road: influences of intracellular metabolite diffusion on cellular organization and metabolism in skeletal muscle. J Exp Biol 210:3505–3512. doi:10.1242/jeb.000331

    Article  PubMed  CAS  Google Scholar 

  • Londraville RL, Sidell BD (1990) Ultrastructure of aerobic muscle in Antarctic fishes may contribute to maintenance of diffusive fluxes. J Exp Biol 150:205–220

    Google Scholar 

  • Mommsen TP (2001) Paradigms of growth in fish. Comp Biochem Physiol B Biochem Mol Biol 129:207–219. doi:10.1016/S1096-4959(01)00312-8

    Article  PubMed  CAS  Google Scholar 

  • Near TJ (2004) Estimating divergence times of notothenioid fishes using a fossil-calibrated molecular clock. Antarct Sci 16:37–44. doi:10.1017/S0954102004001798

    Article  Google Scholar 

  • Near TJ, Pesavento JJ, Cheng C-HC (2004) Phylogenetic investigations of Antarctic notothenioid fishes (Perciformes: Notothenioidei) using complete gene sequences of the mitochondrial encoded 16S rRNA. Mol Phylogenet Evol 32:881–891. doi:10.1016/j.ympev.2004.01.002

    Article  PubMed  CAS  Google Scholar 

  • Near TJ, Kendrick BJ, William Detrich H et al (2007) Confirmation of neutral buoyancy in Aethotaxis mitopteryx DeWitt (Notothenioidei: Nototheniidae). Polar Biol 30:443–447. doi:10.1007/s00300-006-0201-y

    Article  Google Scholar 

  • Nyack AC, Locke BR, Valencia A et al (2007) Scaling of postcontractile phosphocreatine recovery in fish white muscle: effect of intracellular diffusion. Am J Physiol Regul Integr Comp Physiol 292:R2077–R2088. doi:10.1152/ajpregu.00467.2006

    PubMed  CAS  Google Scholar 

  • Patterson SE, Mook LB, Devoto SH (2007) Growth in the larval zebrafish pectoral fin and trunk musculature. Dev Dyn 237:307–315. doi:10.1002/dvdy.21400

    Article  Google Scholar 

  • Richardson MK, Allen SP, Wright GM et al (1998) Somite number and vertebrate evolution. Development 125:151–160

    PubMed  CAS  Google Scholar 

  • Rolfe DF, Brand MD (1996) Contribution of mitochondrial proton leak to skeletal muscle respiration and to standard metabolic rate. Am J Physiol 271:C1380–C1389

    PubMed  CAS  Google Scholar 

  • Rolfe DF, Newman JM, Buckingham JA et al (1999) Contribution of mitochondrial proton leak to respiration rate in working skeletal muscle and liver and to SMR. Am J Physiol 276:C692–C699

    PubMed  CAS  Google Scholar 

  • Rowlerson A, Veggetti A (2001) Cellular mechanisms of post-embryonic growth in aquaculture especies. In: Johnston IA (ed) Muscle development and growth. Academic Press, San Diego

    Google Scholar 

  • Rowlerson A, Scapolo P, Mascarello E et al (1985) Comparative study of myosins present in the lateral muscle of some fish: species variations in myosin isoforms and their distribution in red, pink and white muscle. J Muscle Res Cell Motil 6:601–640. doi:10.1007/BF00711917

    Article  PubMed  CAS  Google Scholar 

  • Sanger AM, Davison W, Egginton S (2005) Muscle fine structure reflects ecotype in two nototheniids. J Fish Biol 66:1371–1386. doi:10.1111/j.0022-1112.2005.00689.x

    Article  Google Scholar 

  • Sidell BD, Hazel JR (1987) Temperature affects the diffusion of small molecules through cytosol of fish muscle. J Exp Zool 129:191–203

    CAS  Google Scholar 

  • Smialowska E, Kilarski W (1981) Histological analysis of fibres in myotomes of Antarctic fish (Admiralty Bay, King George Islands, South Shetland Islands) I. Comparative analysis of muscle fibre sizes. Pol Polar Res 2:109–129

    Google Scholar 

  • Stellabotte F, Devoto SH (2007) The teleost dermomyotome. Dev Dyn 236:2432. doi:10.1002/dvdy.21253

    Article  PubMed  CAS  Google Scholar 

  • Stellabotte F, Dobbs-McAuliffe B, Fernández DA et al (2007) Dynamic somite cell rearrangements lead to distinct waves of myotome growth. Development 134:1253–1257. doi:10.1242/dev.000067

    Article  PubMed  CAS  Google Scholar 

  • Stoiber W, Sanger AM (1996) An electron microscopic investigation into the possible source of new muscle fibres in teleost fish. Anat Embryol (Berl) 194:569–579. doi:10.1007/BF00187470

    CAS  Google Scholar 

  • Stoiber W, Haslett JR, Goldschmid A et al (1998) Patterns of superficial fibre formation in the European pearlfish (Rutilus frisii meidingeri) provide a general template for slow muscle development in teleost fish. Anat Embryol 197:485–496. doi:10.1007/s004290050159

    Article  PubMed  CAS  Google Scholar 

  • Tyler S, Sidell BD (1984) Changes in motochondrial disribution and diffusion distances in muscle of goldfish upon acclimation to warm and cold temperature. J Exp Zool 232:1–9. doi:10.1002/jez.1402320102

    Article  Google Scholar 

  • van Raamsdonk W (1982) Differentiation of the muscle fiber types in the teleost Brachydanio rerio, the zebrafish. Anat Embryol 164:51–62. doi:10.1007/BF00301878

    Article  PubMed  Google Scholar 

  • Wakeling JM, Johnston IA (1998) Muscle power output limits fast-start performance in fish. J Exp Biol 201:1505–1526

    PubMed  CAS  Google Scholar 

  • Wakeling JM, Cole NJ, Kemp K et al (2000) The biomechanics and evolutionary significance of thermal acclimation in the common carp Cyprinus carpio. Am J Physiol Regul Integr Comp Physiol 279:657–665

    Google Scholar 

  • Walesby NJ, Johnston IA (1980) Fibre types in locomotory muscles of an antarctic teleost Notothenia rosii. Cell Tissue Res 208:143–164. doi:10.1007/BF00234180

    Article  PubMed  CAS  Google Scholar 

  • Walworth NC (2000) Cell-cycle checkpoint kinases: checking in on the cell cycle. Curr Opin Cell Biol 12:697–704. doi:10.1016/S0955-0674(00)00154-X

    Article  PubMed  CAS  Google Scholar 

  • Wilson R, Franklin C, Davison W et al (2001) Stenotherms at sub-zero temperature: thermal dependence of swimming performance in Antarctic fish. J Comp Physiol [B] 171:263–269. doi:10.1007/s003600000172

    CAS  Google Scholar 

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Acknowledgments

We would like to thank CONICET, Agencia de Investigación Científica y Tecnológica (SeCyT), Fundación Antorchas and the European Union for funding previous projects on muscle of notothenioids. We would also like to thank present and past members of the laboratory of Ecophysiology at CADIC for collaboration in these projects. Sandy Becker and Sheryl Macnie helped to improve the English of the manuscript. Comments from two anonymous referees have helped greately to improve the manuscript.

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  1. Austral Center for Scientific Research (CADIC-CONICET), 200 B. Houssay, CC 92 CADIC, 9410, Ushuaia, Tierra del Fuego, Argentina

    Daniel A. Fernández & Jorge Calvo

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  1. Daniel A. Fernández
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  2. Jorge Calvo
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Correspondence to Daniel A. Fernández.

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Fernández, D.A., Calvo, J. Fish muscle: the exceptional case of notothenioids. Fish Physiol Biochem 35, 43–52 (2009). https://doi.org/10.1007/s10695-008-9282-6

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Keywords

  • Fish muscle
  • Muscle growth
  • Fiber size
  • Notothenioids
  • Temperature

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