First published online August 25, 2003
Plasticity of muscle fibre number in seawater stages of Atlantic salmon in response to photoperiod manipulation
Ian A. Johnston1,*,
Sujatha Manthri1,
Alisdair Smart2,
Patrick Campbell3,
David Nickell4 and
Richard Alderson3
1 Gatty Marine Laboratory, School of Biology, University of St Andrews, St
Andrews, Fife, KY16 8LB, UK,
2 Marine Harvest Scotland Ltd, Craigcrook Castle, Edinburgh, EH4 3TU,
UK,
3 BioMar Ltd, North Shore Road, Grangemouth Docks, Grangemouth, FK3 8UL,
UK
4 Roche Vitamins Ltd, Heanor, Derbyshire, DE75 7SG, UK
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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)x100] 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.
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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.
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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.
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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.
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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.
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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).
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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.
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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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© The Company of Biologists Ltd 2003
