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Research Article
Plasticity of muscle fibre number in seawater stages of Atlantic salmon in response to photoperiod manipulation
Ian A. Johnston, Sujatha Manthri, Alisdair Smart, Patrick Campbell, David Nickell, Richard Alderson
Journal of Experimental Biology 2003 206: 3425-3435; doi: 10.1242/jeb.00577
Ian A. Johnston
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Sujatha Manthri
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Alisdair Smart
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Patrick Campbell
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David Nickell
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Richard Alderson
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Article Figures & Tables

Figures

  • Table 1.

    Numbers of fish by treatment and seawater cage that were repeatedly weighed to assess growth performance

    CageAmbient photoperiodCagePhotoperiod manipulatedTotal
    11033145248
    21264130256
    Total229Total275504
    • Fish were weighed on the following dates: (1) 5 April 2000, (2) 31 May, (3) 11 July, (4) 12 July, (5) 21 August, (6) 25 September, (7) 30 October, (8) 8 January 2001, (9) 5 March, (10) 30 April, (11) 17 July and (12) 12 August.

  • Table 2.

    Number of fish sampled by treatment and seawater cage to investigate muscle cellularity

    Ambient photoperiod Photoperiod manipulated
    Sample dateCage 1Cage 2TotalCage 3Cage 4Total
    12 July 20006612000
    31 Aug 20006511448
    2 Nov 2000 4 4 8 3 6 9
    10 Jan 2001 6 6 12 6 6 12
    5 Mar 2001 2 4 6 3 2 5
    4 June 2001 6 5 11 5 5 10
    14 Aug 2001 5 4 9 3 6 9
    • The sample points in italic correspond to the fish used for the analysis in Table 3.

  • Fig. 1.
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    Fig. 1.

    (A) The relationship between log10 body mass and growth period in seawater for the treatment groups of PIT-tagged Atlantic salmon (Salmo salar) studied. Salmon were reared either under ambient photoperiod (cage 1, filled circles; cage 2, filled triangles) or were subjected to 24 h continuous lighting from 1 November 2000 to 18 June 2001 (cage 3, open circles; cage 4, open triangles). (B) The condition factor [(body mass/fork length-3)×100] for the treatment groups of salmon during and shortly after photoperiod manipulation. The symbols and number of fish studied are as in A. The period of continuous lighting in cages 3 and 4 is illustrated by the grey box. Values represent means ± s.e.m. The number of fish sampled from each cage and treatment is shown in Table 1.

  • Fig. 2.
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    Fig. 2.

    The number of fast muscle fibres per trunk cross-section at the level of the first dorsal fin ray in a subset of Atlantic salmon (Salmo salar L.) reared under conditions of extended winter day length (yellow symbols, dashed line; period of continuous lighting shown by yellow box) or at ambient photoperiod (blue symbols, solid line). The broken blue line shows sunrise and sunset (Greenwich Mean Time, GMT) at Fort William, and the green line illustrates daily recordings of sea temperature. The results are means± s.e.m. The number of fish sampled from each cage is shown in Table 2.

  • Table 3.

    Analysis of variance (General Linear Model) with the number of fast muscle fibres (FN) as a dependent variable using the method of sequential sums of squares for tests

    Sourced.f.Seq. SSSeq. MSFP
    Model A
    Treatment13.177×10113.177×101123.190.042
    Growth period (GP)13.093×10113.093×101134.390.0001
    Treatment × GP15.842×10105.842×10106.490.013
    Cage (treatment)22.731×10101.365×10101.520.225
    Error867.727×10108.985×109
    Total911.485×1012
    Model B
    Treatment13.177×10113.177×101126.250.037
    TCA14.181×10114.181×101151.910.0001
    TCA × treatment13.439×10103.439×10104.270.042
    Cage (treatment)22.411×10101.205×10101.500.229
    Error866.911×10118.037×109
    Total911.485×1012
    • d.f., degrees of freedom; Seq. SS, sequential sums of squares; Seq. MS, sequential mean squares; F, variance ratio; P, probability.

  • Fig. 3.
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    Fig. 3.

    Atlantic salmon (Salmo salar L.) reared under conditions of ambient photoperiod (closed circles, solid line; combined cages 1 and 2) or continuous lighting from 1 November 2000 to 18 June 2001 (open circles, broken line; combined cages 3 and 4). (A) The relationship between the number of fibres and the total cross-sectional area (TCA) of fast myotomal muscle at the level of the first dorsal fin ray. The arrows join common sample points. (B) The relationship between the densities of fast muscle fibres (fibres mm-2 cross-sectional area) and the growth period in seawater. The results are means ± s.e.m. The number of fish sampled from each cage is shown in Table 2.

  • Fig. 4.
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    Fig. 4.

    The mean probability density function (pdf) of fibre diameter in the fast muscle of Atlantic salmon in June 2001 at the end of the period of photoperiod manipulation. Ambient photoperiod (solid line; N=10) and 24 h continuous lighting regime (dashed line; N=10). The dotted line represents the average probability of the combined population, and the grey shaded area represents 100 bootstrap estimates of the probability density. Areas where the mean pdf of the ambient and photoperiod-manipulated treatments fall outside the shaded area provide a graphical representation of the parts of the distribution that are significantly different. The position of data points is shown on the abscissa.

  • Fig. 5.
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    Fig. 5.

    The mean rate of hypertrophy of fast muscle fibres between successive sample points plotted against seawater growth for the ambient (solid circles) and photoperiod-manipulated (open circles) fish. The period of continuous lighting in the photoperiod manipulated treatment is illustrated by the grey box. The rate of hypertrophy has been plotted at the midpoint of the time period over which it was calculated. Hypertrophy was calculated as the mean of the difference between the observed fibre diameter and the mean of the fibre diameter in the preceding sample.

  • Fig. 6.
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    Fig. 6.

    The number of myonuclei in single muscle fibre segments of 1 cm length in relation to muscle fibre diameter for the 4 June sample (see Table 1) for the ambient (closed circles) and photoperiod-manipulated treatment (open circles). First-order linear regressions were fitted to the data with the following equations. For the ambient photoperiod: myonuclei number=288.6+14.4(fibre diameter) (r2=0.80; ANOVA: F1,159=627.2, P<0.001). For the manipulated photoperiod: myonuclei number=1258.1+12.4(fibre diameter) (r2=0.34; ANOVA: F1,230=118.4, P<0.001).

  • Fig. 7.
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    Fig. 7.

    The density of c-met immuno-positive cells per mm2 fast muscle cross-sectional area for the ambient (closed circles) and photoperiod-manipulated treatment (open circles). Values represent means± s.e.m. for six fish per treatment group.

  • Fig. 8.
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    Fig. 8.

    Working hypothesis to explain the cellular basis of the results obtained. Myogenic stem cells (red nuclei) are derived from a pleuripotent stem cell (yellow nuclei) population at an earlier stage in ontogeny. The myogenic stem cells are assumed to undergo an asymmetric division to regenerate the stem cell and produce a daughter cell (orange) capable of a limited number of further divisions before terminal differentiation. Relative to ambient winter photoperiod (illustrated in A), the cells committed to differentiation (orange) undergo more divisions and/or have a shorter cell cycle time than similar cells in the continuous light treatment (illustrated in B), resulting in a higher standing population of c-met immuno-positive cells (see Fig. 7), a higher content of myonuclei (see Fig. 6) and a higher fibre number (Fig. 2).

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Research Article
Plasticity of muscle fibre number in seawater stages of Atlantic salmon in response to photoperiod manipulation
Ian A. Johnston, Sujatha Manthri, Alisdair Smart, Patrick Campbell, David Nickell, Richard Alderson
Journal of Experimental Biology 2003 206: 3425-3435; doi: 10.1242/jeb.00577
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Research Article
Plasticity of muscle fibre number in seawater stages of Atlantic salmon in response to photoperiod manipulation
Ian A. Johnston, Sujatha Manthri, Alisdair Smart, Patrick Campbell, David Nickell, Richard Alderson
Journal of Experimental Biology 2003 206: 3425-3435; doi: 10.1242/jeb.00577

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