Abstract
Eggs from spring spawning stocks of herring (Clupea harengus L.) were fertilized and reared at either 5, 8 or 12°C in 1991 and 1992. The differentiation of myotomal muscle fibres was investigated in relation to the development of other organs and tissues using light and electron microscopy. The gut, notochord, eyes and haemocoel appeared at the same relative point in development between fertilization and hatching at all temperatures. In contrast, the formation of the spinal cord, pronephros, pectoral fin buds and muscle fibres was relatively retarded at 5°C compared with 8 and 12°C. Myogenesis in the presumptive inner muscle mass occurred after 12 to 16 d at 5°C, 7 to 10 d at 8°C and 3.5 to 6 d at 12°C. Myoblasts aligned in orderly rows running from myosept to myosept prior to fusion to form myotubes. Actin and myosin filaments were synthesised throughout the cytoplasm in associated with presumptive Z-lines at the periphery of myotubes and immature muscle fibres. Differentiation of the superficial and inner muscle fibres types of larvae occurred at around the same time. Following this initial period of myogenesis, the number of myotomal muscle fibres remained constant until after hatching, so that increases in muscle bulk in the late embryo were entirely due to fibre hypertrophy. At hatching, the number of superficial muscle fibres present in myotomes just posterior to the yolk-sac was significantly less at 5°C (108±12) than at either 8°C (132±10) or 12°C (140±10) (mean±SD, 12 fish/temperature). In contrast, there were around 280 inner muscle fibres/myotome, comprising 90% of the trunk cross-sectional area, at all three temperatures. Myofibrillargenesis occurred relatively slowly at low temperatures, so that the volume density of myofibrils in the inner muscle fibres of larvae at hatching was significantly less at 5°C (39.2±9.0) than at either 8°C (49.6±8.8) or 12°C (50.2±9.8) (mean ±SD, 20 fibres/temperature from total of 5 fish). Undifferentiated myoblasts remained at hatching to form a population of presumptive myosatellite cells. The number of presumptive myosatellite cells per mm2 cross-sectional area of muscle fibre was more than two times higher at 8°C (1493±335) than at either 5°C (478±102) or 12°C (924±233) (mean±SD, 5 fish/temperature). The results suggest that temperature can influence the commitment of myoblasts to differentiation at a critical stage in embryogenesis, thereby providing a potential mechanism for influencing future growth characteristics.
Similar content being viewed by others
Literature cited
Bailey, K. M., Batty, R. S. (1984). Laboratory study of predation by Aurelia aurita on larvae of cod, flounder, plaice and herring: development and vulnerability to capture. Mar. Biol. 83: 287–291
Ballard, W. W. (1973). Normal embryonic stages for salmonid fishes, based on Salmo gairdneri Richardson and Salvelinus fontinalis (Mitchill). J. exp. Zool. 184: 7–26
Batty, R. S. (1984). Development of swimming movements and musculature of larval harring (Clupea harengus). J. exp. Biol. 110: 217–229
Batty, R. S., Blaxter, J. H. S., Fretwell, K. (1993). Effect of temperature on the escape responses of larval herring, Clupea harengus. Mar. Biol. 115: 523–528
Blaxter, J. H. S. (1968). Rearing herring larvae to metamorphosis and beyond. J. mar. biol. Ass. U.K. 48: 17–28
Blaxter, J. H. S., Hempel, G. (1963). The influence of egg size on herring larvae (Clupea harengus L.). J. Cons. perm. int. Explor. Mer 28: 211–240
Calvo, J., Johnston, I. A. (1992). Influence of rearing temperature on the distribution of muscle fibre types in the turbot Scophthalmus maximus at metamorphosis. J. exp. mar. Biol. Ecol. 161: 45–55
Campion, D. R. (1984). The muscle satellite cell: a review. Int. Rev. Cytol. 87: 225–251
Crockford, T., Johnston, I. A. (1993). Developmental changes in the composition of myofibrillar proteins in the swimming muscles of Atlantic herring, Clupea harengus. Mar. Biol. 115: 15–22
De Silva, C. D. (1974). Development of the respiratory system in herring and plaice larvae. In: Blaxter, J. H. S. (ed.) The early life history of fish. Springer Verlag, Berlin-Heidelberg-New York, p. 465–485
El-Fiky, N. S., Wieser, W. (1988). Life styles and patterns of development of gills and muscles in larval cyprinid fish (Pisces, Teleostei). Zoomorphology 107: 126–132
Fukuhara, O. (1990). Effect of temperature on yolk utilization, initial growth, and behaviour of unfed marine fish-larvae. Mar. Biol. 106: 169–174
Greer-Walker, M. G. (1970). Growth and development of the skeletal muscle fibres of the cod (Gadus morhua L.). J. Cons. perm. int. Explor. Mer. 33: 228–244
Greer-Walker, M. G., Burd, A. C., Pull, G. A. (1972). The total number of white skeletal muscle fibres in cross section as a character for stock separation in North Sea herring (Clupea harengus L.). J. Cons. perm. int. Explor. Mer 34: 238–243
Hayes, F. R., Pelluet, D., Gorham, E. (1953). Some effects of temperature on the embryonic development of the salmon (Salmo salar). Can. J. Zool. 31: 42–51
Hempel, G. (1979). Early life history of marine fish. The egg stage. University of Washington Press, Seattle and London (Washington Sea Grant Publication)
Hubbs, C. L. (1922). Variations in the number of vertebrae and other meristic characters of fishes correlated with the temperature of water during development. Am. Nat. 56: 360–372
Jones, S. R., Jeffs, T. M. (1991). Near-surface sea temperatures in coastal waters of the North Sea, English Channel and Irish Sea. Ministry of Agriculture, Fisheries and Food, Fisheries Research, Data Report. No. 24. Her Majesty's Stationery Office, London
Karp, G., Dervrill, N. J. (1981). Development. 2nd ed. McGraw-Hill, New York
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: 418–424
Lillie, F. R. (1952). Development of the chick. Henry Holt & Co, New York
Moss, F. P., Leblond, C. P. (1970). Nature of dividing nuclei in skeletal muscle of growing rats. J. Cell Biol. 44: 459–462
Nag, A. C., Nursall, J. R. (1972). Histogenesis of white and red muscle fibres of a fish, Salmo gairdneri. Cytobios 6: 227–246
Popiela, H. (1976). Muscle satellite cells in urodele amphibians: facilitated identification of satellite cells using ruthenium red staining. J. exp. Zool. 198: 57–64
Powell, R. L., Dodson, W. V., Cloud, J. G. (1989). Cultivation and differentiation of satellite cells from skeletal muscle of the rainbow trout Salmo gairdneri. J. exp. Zool. 250: 333–338
Scapolo, P. A., Veggetti, A., Rowlerson, A., Mascarello, F., Carpene, E. (1984). Do the small new fibres of grey mullet arise by fibre splitting? J. Muscle Res. Cell Motil. 5, p. 214
Schmidt, J. (1919). Racial studies in fishes. II. Experimental investigations with Lebistes reticulatus (Peters) Regan. J. Genet. 8: 147–153
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: 253–257
Stockard, C. R. (1921). Deveopmental rate and structural expression: an experimental study of twins, ‘double monsters’ and single deformites, and the interaction among embryonic organs during their origin and development. Am. J. Anat. 28: 115–266
Tåning, A. V. (1952). Experimental study of meristic characters in fishes. Biol. Rev. 27: 169–193
Veggetti, A., Mascarello, F., Scapolo, Rowlerson, A. (1990). Hyperplastic and hypertrophic growth of lateral muscle in Dicentrarchus labrax (L.). Anat. Embryol. 182: 1–10
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: 333–341
Waterman, R. E. (1969). Development of the lateral musculature in the teleost, Brachydanio rerio: a fine structural study. Am. J. Anat. 125: 457–494
Weatherley, A. H., Gill, H. S. (1985). Dynamics of increase in muscle fibers in fishes in relaiion to size and growth. Experientia 41: 353–354
Willemse, J. J., Lieuwma-Noordanus, C. (1984). The generation of new “white” muscle fibres by budding in the lateral musculature of elvers Anguilla anguilla L. during normal development. Experientia 40: 990–992
Author information
Authors and Affiliations
Additional information
Communicated by J. Mauchline, Oban
Correspondence to: I.A. Johnston at Gatty Marine Laboratory
Rights and permissions
About this article
Cite this article
Johnston, I.A. Temperature influences muscle differentiation and the relative timing of organogenesis in herring (Clupea harengus) larvae. Marine Biology 116, 363–379 (1993). https://doi.org/10.1007/BF00350053
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00350053