Skip to main content
Log in

Differentiation and growth of muscle in the fish Sparus aurata (L): II. Hyperplastic and hypertrophic growth of lateral muscle from hatching to adult

  • Papers
  • Published:
Journal of Muscle Research & Cell Motility Aims and scope Submit manuscript

Summary

Post-hatching growth of lateral muscle in a teleost fish, Sparus aurata (L) was studied morphometrically to identify and quantify muscle fibre hyperplasia and hypertrophy, and by in vivo nuclear labelling with 5-bromo-deoxyuridine to identify areas of myoblast proliferation. Muscle fibre types were identified principally by myosin ATPase histochemistry and immunostaining, and labelled nuclei were identified at light and electronmicroscope level by immunostaining with a specific monoclonal antibody. Hyperplastic growth was slow at hatching, but then increased to a maximum at the mid-point of larval life. Larval hyperplastic growth occured by apposition of new fibres along proliferation zones, principally just under the lateral line and in the apical regions of the myotome, but also just under the superficial monolayer at intermediate positions. The first of these zones gave rise to slow and pink muscle fibres, in a process which continued through into postlarval life. The other zones added new fibres to the fast-white muscle layer in a process which was exhausted by the end of larval life. Post-larvally, between 60 and 90 days posthatching, a new hyperplastic process started in the fast-white muscle as nuclei proliferated and new muscle fibres were formed throughout the whole layer. This process resulted in a several-fold increase in the number of fast-white fibres over a few weeks, and then waned to very low levels in juveniles. Hyperplasia by apposition continued for some time postlarvally on the deep surface of the superficial monolayer, but at this stage gave rise to slow fibres only. Hypertrophic growth occurred at all ages, but was the dominant mechanism of muscle growth only in the juvenile and adult stages. Mechanisms giving rise to these different growth processes in fish muscle are discussed, and compared with muscle development in higher vertebrates.

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

  • Alessio, G. & Gandolfi, G. (1975) Riproduzione artificiale di Orata, Sparus aurata (L.) (Osteichthyes, Sparidae). IV Sviluppo embrionale e postnatale. Instituto Lombardo (Memorie Sc. Mat.) 26, 95–132.

    Google Scholar 

  • Alfei, L., Colombari, P. T., Cavallo, D., Eleuteri, P. and De Vita, R. (1993) Use of 5′-bromodeoxyuridine immunohistochemistry to examine proliferative activity of fish tissues. Eur. J. Histochem. 37, 183–9.

    Google Scholar 

  • Ashby, P. R., Pincon-Raymond, M. & Harris, A. J. (1993) Regulation of myogenesis in paralysed muscles in the mouse mutants peroneal muscular atrophy and muscular dysgenesis. Dev. Biol. 156, 529–36.

    Google Scholar 

  • Battram, J. C. & Johnston, I. A. (1991) Muscle growth in the Antartic teleost, Notothenia neglecta (Nybelin). Antarctic Sci. 3, 29–33.

    Google Scholar 

  • Brooks, S. & Johnston, I. A. (1993) Influence of development and rearing temperature on the distribution, ultrastructure and myosin sub-unit composition of myotomal muscle-fibre types in the plaice Pleuronectes platessa. Mar. Biol. 117, 501–13.

    Google Scholar 

  • Calvo, J. (1989) Sexual differences in the increase of white muscle fibres in Argentine hake, Merluccius hubbsi, from the San Matias gulf (Argentina). J. Fish Biol. 35, 207–14.

    Google Scholar 

  • Carpenè, E. & Veggetti, A. (1981) Increase in muscle fibres in the lateralis muscle (white portion) of Mugilidae (Pisces, Teleostei). Experientia 37, 191–3.

    Google Scholar 

  • Carpenè, E., Scapolo, P. A., Mascarello, F., Veggetti, A. & Rowlerson, A. (1983) Influenza della temperatura sul ciclo iperplastico annuale del muscolo bianco dei Mugilidi. Atti Soc. Ital. Sci. Vet. 37, 117–18.

    Google Scholar 

  • Dimario, J. X., Fernyak, S. E. & Stockdale, F. E. (1993) Myoblasts transferred to the limbs of embryos are committed to specific type fates. Nature 362, 165–7.

    Google Scholar 

  • Draeger, A., Weeds, A. G. & Fitzsimons, R. B. (1987) Primary, secondary and tertiary myotubes in developing skeletal muscle: a new approach to the analysis of human myogenesis. J. Neurol. Sci. 81, 19–43.

    Google Scholar 

  • Feldman, J. L. & Stockdale, F. E. (1992) Temporal appearance of satellite cells during myogenesis. Dev. Biol. 153, 217–26.

    Google Scholar 

  • Gratzner, H. G. (1982) Monoclonal antibody to 5-Bromo- and 5-iododeoxyuridine: a new reagent for detection of DNA replication. Science 218, 474–5.

    Google Scholar 

  • Gratzner, H. G., Leif, R. C., Ingram, D. J. & Castro, A. (1975) The use of antibody specific for bromodeoxyuridine for the immunofluorescent determination of DNA replication in single cells and chromosomes. Exp. Cell Res. 95, 88–94.

    Google Scholar 

  • Higgins, P. J. & Thorpe, J. E. (1990) Hyperplasia and hypertrophy in the growth of skeletal muscle in juvenile Atlantic salmon, Salmo salar L. J. Fish Biol. 37, 505–19.

    Google Scholar 

  • Johnston, I. A. (1993) Temperature influences muscle differentiation and the relative timing of organogenesis in herring (Clupea harengus) larvae. Mar. Biol. 116, 369–79.

    Google Scholar 

  • Johnston, I. A. (1994) Development and plasticity of fish muscle with growth. Bas. Appl. Myol. 4, 353–68.

    Google Scholar 

  • Kiessling, A., Storebakken, T., Asgard, T. & Kiessling, K.-H. (1991) Changes in the structure and function of the epaxial muscle of rainbow trout (Oncorhychus mykiss) in relation to ration and age I. Growth dynamics. Aquaculture 93, 335–56.

    Google Scholar 

  • Koumans, J. T. M. & Akster, H. A. (1995) Myogenic cells in development and growth of fish. Comp. Biochem. Physiol. 110A, 3–20.

    Google Scholar 

  • Koumans, J. T. M., Akster, H. A., Dulos, G. J. & Osse, J. W. M. (1990) Myosatellite cells of Cyprinus carpio (Teleostei) in vitro: isolation, recognition and differentiation. Cell Tiss. Res. 261, 173–81.

    Google Scholar 

  • Koumans, J. T. M., Akster, H. A., Booms, G. H. R., Lemmens, C. J. J. & Osse, J. W. M. (1991) Numbers of myosatellite cells in white axial muscle of growing fish: Cyprinus carpio L. (Teleostei). Am. J. Anat. 192, 418–24.

    Google Scholar 

  • Koumans, J. T. M., Akster, H. A., Booms, G. H. R. & Osse, J. W. M. (1993) Growth of carp (Cyprinus carpio) white axial muscle; hyperplasia and hypertrophy in relation to the myonucleus/sarcoplasm ratio and the occurrence of different subclasses of myogenic cells. J. Fish Biol. 43, 69–80.

    Google Scholar 

  • Mascarello, F., Stecchini, M. L., Rowlerson, A. & Ballocchi, E. (1992) Tertiary myotubes in postnatal growing pig muscle detected by their myosin isoform composition. J. Anim. Sci. 70, 1806–13.

    Google Scholar 

  • Mascarello, F., Rowlerson, A., Radaelli, G., Scapolo, P. A. & Veggetti, A. (1995) Differentiation and growth of muscle in Sparus aurata (L) (Osteichthyes, Sparidae): I. Myosin expression and organisation of fibre types in lateral muscle from hatching to adult. J. Muscle Res. Cell Motil. 16, 213–22.

    Google Scholar 

  • NATHANAILIDES, C., LOPEZ-ALBORS, O. & STICKLAND, N. C. (1995) Influence of pre-hatch temperature on the development of muscle cellularity in post-hatch Atlantic salmon (Salmo salar L.). Can. J. Fish. Aquat. Sci., in press.

  • Ontell, M. & Kozeka, K. (1984) The organogenesis of murine striated muscle: a cytoarchitectural study. Am. J. Antl. 171, 133–48.

    Google Scholar 

  • Patterson, J. M. & Zakon, H. H. (1993) Bromodeoxyuridine labelling reveals a class of satellite-like cells within the electric organ. J. Neurobiol, 24, 660–74.

    Google Scholar 

  • Powell, R. L., Dodson, M. V. & Cloud, J. G. (1989) Cultivation and differentiation of satellite cells from skeletal muscle of the rainbow trout Salmo gairdneri. J. Exp. Zool. 250, 333–8.

    Google Scholar 

  • Romanello, M. G., Scapolo, P. A., Luprano, S. & Mascarello, F. (1987) Post-larval growth in the lateral white muscle of the eel, Anguilla anguilla. J. Fish Biol. 30, 161–72.

    Google Scholar 

  • Scapolo, P. A., Veggetti, A., Mascarello, F. & Romanello, M. G. (1988) Developmental transitions of myosin isoforms and organisation of the lateral muscle in the teleost Dicentrarchus labrax (L). Anat. Embryol. 178, 287–95.

    Google Scholar 

  • Stickland, N. C. (1983) Growth and development of muscle fibres in the rainbow trout (Salmo gairdneri). J. Anat. 137, 323–33.

    Google Scholar 

  • Stickland, N. C., White, R. N., Mescall, P. E., Crook, A. R. & Thorpe, J. E. (1988) The effect of temperature on myogenesis in embryonic development of the Atlantic salmon (Salmo salar L.). Anat. Embryol. 178, 253–7.

    Google Scholar 

  • Stockdale, F. E. (1992) Myogenic cell lineages. Dev. Biol. 154, 284–98.

    Google Scholar 

  • Talesara, C. L. & Urfi, A. J. (1987) A histophysiological study of muscle differentiation and growth in the common carp, Cyprinus carpio Var. communis. J. Fish Biol. 31, 45–54.

    Google Scholar 

  • Van Raamsdonk, W., Mos, W., Smit-Onel, M. J., Van Der Laarse, W. J. & Fehres, R. (1983) The development of the spinal motor column in relation to the myotomal muscle fibers in the Zebrafish (Brachydanio rerio). Anat. Embryol. 167, 125–39.

    Google Scholar 

  • Veggetti, A., Mascarello, F., Scapolo, P. A. & Rowlerson, A. (1990) Hyperplastic and hypertrophic growth of lateral muscle in Dicentrarchus labrax (L.): an ultrastructural and morphometric study. Anat. Embryol. 182, 1–10.

    Google Scholar 

  • Veggetti, A., Mascarello, F., Scapolo, P. A., Rowlerson, A. & Candia Carnevali, M. D. (1993) Muscle growth and myosin isoform transitions during development of a small teleost fish, Poecilia reticulata (Peters) (Atherinifornes, Poeciliidae): a histochemical, immunohistochemical, ultrastructural and morphometric study. Anat. Embryol. 187, 353–61.

    Google Scholar 

  • Vieira, V. L. A. & Johnston, I. A. (1992) Influence of temperature on muscle-fibre development in larvae of the herring Clupea harengus. Mar. Biol. 112, 333–41.

    Google Scholar 

  • Weatherley, A. H., Gill, H. S. & Rogers, S. C. (1979) Growth dynamics of muscle fibres, dry weight, and condition in relation to somatic growth rate in yearling rainbow trout (Salmo gairdneri). Can. J. Zool. 57, 2385–92.

    Google Scholar 

  • Weatherley, A. H. & Gill, H. S. (1981) Characteristics of mosaic muscle growth in rainbow trout Salmo gairdneri. Experientia 37, 1102–3.

    Google Scholar 

  • Weatherley, A. H. & Gill, H. S. (1984) Growth dynamics of white myotomal muscle fibres in the bluntnose minnow, Pimephales notatus Rafinesque, and comparison with rainbow trout, Salmo gairdneri Richardson. J. Fish Biol. 25, 13–24.

    Google Scholar 

  • Weatherley, A. H., Gill, H. S. & Lobo, A. F. (1988) Recruitment and maximal diameter of axial muscle fibres in teleosts and their relationship to somatic growth and ultimate size. J. Fish Biol. 33, 851–9.

    Google Scholar 

  • Wilson, S. J., McEwan, J. C., Sheard, P. W. & Harris, A. J. (1992) Early stages of myogenesis in a large mammal: formation of successive generations of myotubes in sheep tibialis cranialis muscle. J. Muscle Res. Cell Motil. 13, 534–50.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Rowlerson, A., Mascarello, F., Radaelli, G. et al. Differentiation and growth of muscle in the fish Sparus aurata (L): II. Hyperplastic and hypertrophic growth of lateral muscle from hatching to adult. J Muscle Res Cell Motil 16, 223–236 (1995). https://doi.org/10.1007/BF00121131

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00121131

Keywords

Navigation