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First published online May 8, 2007
Journal of Experimental Biology 210, 1735-1741 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.003194
Larval programming of post-hatch muscle growth and activity in Atlantic salmon (Salmo salar)
The Royal Veterinary College, Royal College Street, London, NW1 0TU, UK
* Author for correspondence (e-mail: nstickland{at}rvc.ac.uk)
Accepted 19 February 2007
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Summary |
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Salmon eggs were incubated at either 10°C or 5°C from fertilization until hatching, then subsequently both groups were reared at 5°C. Fish from both groups were sampled at the eyed stage, 6 and 21 weeks after first feeding, for muscle cellularity analysis and immunocytochemistry. In addition, to try to establish a mechanism for altered growth, the activity of the fish was measured at 3, 6 and 21 weeks after first feeding.
Our results demonstrate that whereas fish incubated at 10°C grow faster, the fish incubated at 5°C show a more sustained period of muscle growth and by 21 weeks are significantly longer, heavier and have more muscle fibres than those fish incubated at a higher temperature. We also demonstrate that fish raised at 5°C show increased food seeking activity throughout development and that this may explain their sustained growth and muscle development.
These results taken together, demonstrate that egg incubation temperature up to hatching in salmon is critical for longer term muscle growth, twinned with increased activity. This is of interest to the aquaculture industry in term of the production of good quality fish protein.
Key words: Salmo salar, muscle cellularity, MRFs, temperature, activity
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Introduction |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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). Salmon is grown and consumed worldwide and because of
increasing consumer demand efforts are made to augment the production of this
species in fisheries. The anatomical part of salmon consumed in human
gastronomy is mostly skeletal muscle fibres. Therefore optimising the
embryonic development and growth of muscle tissue offers considerable
potential for optimising both production yield and meat quality of fish
(Johnston, 1999).
During embryogenesis, muscle development and growth in fish occurs as a
combination of muscle hypertrophy (the increase in size of existing fibres)
and muscle hyperplasia (the recruitment of new muscle fibres) (reviewed by
Koumans and Akster, 1995;
Rowlerson and Veggetti, 2001).
This process continues throughout development into adulthood in most fish
species (Greer-Walker, 1970;
Stickland, 1983;
Weatherley and Gill, 1984;
Weatherley et al., 1988). This
is in contrast to mammals in which hyperplasia stops at around the time of
birth (Campion, 1984;
Goldspink, 1972;
Rayne and Crawford, 1975).
It has long been known that environmental temperature can affect the time
of embryonic development in a variety of animal species
(Krogh, 1914), including the
Atlantic salmon (Salmo salar)
(Hayes et al., 1953). In this
species a warmer incubation temperature, compared to the cooler ambient
temperature, produced bigger but fewer fibres with high myofibrillar content
at the newly hatched stage (Stickland et
al., 1988). The hatched embryos of salmon that were incubated at
the cooler ambient temperature also grew better up to 3 weeks post-hatch when
all juveniles were grown at ambient temperature after hatching
(Nathanailides et al., 1995).
Johnston et al. (Johnston et al.,
2000) also showed that cooler temperature regimes up to first
feeding in Atlantic salmon produced fish that grew better up to 12 weeks
later. Furthermore, it was found that faster growth of salmon juveniles is
achieved by increased muscle fibre hyperplasia
(Higgins and Thorpe, 1990).
Additionally, temperature appears to directly affect the size and the number
of salmon myosatellite cells in vitro with differentiation and fusion
occurring earlier at high temperature
(Matschak and Stickland,
1995). The effects of temperature on muscle growth have also been
demonstrated in many other fish species, such as sea bass
(Ayala et al., 2003;
Ayala et al., 2000) and
Atlantic herring (Johnston et al.,
2001).
Muscle development is controlled by a family of bHLH genes called myogenic
regulatory factors (MRFs), which includes MyoD and myogenin
(Rescan, 2001;
Rudnicki and Jaenisch, 1995;
Rudnicki et al., 1993).
Therefore, a change in time and level of MRF expression with developmental
temperature might constitute a molecular mechanism for the observed changes in
muscle phenotype (Temple et al.,
2001; Wilkes et al.,
2001). In rainbow trout, it was found that egg incubation at
4°C delayed and prolonged expression of MyoD and myogenin in embryos
compared with those reared at 12°C
(Xie et al., 2001).
Thus, although there is some information on temperature influences of early muscle development and initial growth, we do not know how early thermal history influences longer term growth. We also do not know whether these influence the long term function or activity. The aim of the present study, therefore, was to determine the influence of egg incubation temperature on growth up to 21 weeks post-hatch, with particular reference to the cellular growth of muscle tissue, and the effect on fish activity.
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Materials and methods |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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).
Measurement of fish length and mass
From each temperature regime fish were taken at 6 weeks and 21 weeks after
first feeding and killed by an overdose of the anaesthetic MS-222
(3-aminobenzoic acid ethyl ester; Sigma, Poole, Dorset, UK). At least 20 fish
were photographed for each group and body length was measured. The fish were
blotted dry with filter paper and the body mass was recorded.
Morphometry
White muscle fibres
Five fish from each temperature regime were sacrificed at eyed stage, 6
weeks after first feeding, and 21 weeks after first feeding (i.e. 30 fish in
total). Complete transverse sections were cut from each fish at the level of
the anal vent. The sections were fixed in 3% glutaraldehyde in 0.1 mol
l–1 phosphate buffer (pH 7.2), washed in phosphate buffer,
post-fixed in 1% osmium tetroxide, dehydrated and embedded in TAAB resin
according to the method of Stickland
(Stickland et al., 1988).
Transverse sections of 0.5 µm thickness were obtained using a Reichert
ultramicrotome and stained with 1% Toluidine Blue. Slides were examined using
a Zeiss image analysis system (KS 300, Kontron, Munich, Germany). The
following parameters were quantified: distribution of white fibre
cross-sectional areas, total white muscle cross-sectional area and total white
muscle fibre number from one half of each fish.
Red muscle area
Succinate dehydrogenase staining for oxidative muscle
(Nachlas et al., 1957) was
carried out on frozen transverse sections (20 µm thickness) taken at the
level of the vent. Red muscle area relative to white muscle area was
quantified on a half fish using a Zeiss image analysis system (KS 300,
Kontron, Munich, Germany) on five specimens from each group and stage (6 and
21 weeks after first feeding).
Immunohistochemistry
Immunostaining was carried out using the avidin–biotin (Vector
Laboratories, Burlingame, CA, USA) technique on frozen transverse sections (20
µm thickness) taken at the level of the vent
(Xie et al., 2001). A control
was performed by substituting pre-immunised 5–10% normal goat serum in
PBS for primary antibody. The primary antibodies used were anti-myogenin
polyclonal rabbit IgG (M-225) and anti-MyoD, polyclonal rabbit IgG (M-318)
from Santa Cruz Biotechnology, Inc, Santa Cruz, CA, USA. The secondary
antibody used was polyclonal goat anti-rabbit immunoglobulin from
Dakocytomation, Glostrup, Denmark.
Fish activity
Fish activity was measured using the Linton (AM10530) activity monitor
(Linton Instruments, Diss, UK). The instrument fits over the fish tank and has
two levels of infrared beams which, when broken by movement of fish, register
activity units using the Amonlite software (Linton Instruments;
Fig. 1). Fifteen fish from each
incubation temperature at three different stages (3 weeks after first feeding,
6 weeks after first feeding and 21 weeks after first feeding) were used to
measure the fish activity. The activity of fish was initiated by adding a
pinch of fish pellets to the tank exactly at time 0 and 5 min into the 10 min
experiment for all stages examined. The Amonlite software measures the total
activity, i.e. the total number of beam breaks. The software was set up such
that the total number of beam breaks were recorded every 10 s, therefore a
total of 60 individual measurements were made within the 10 min
experiment.
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Statistical analysis
All statistical analyses were performed using the SPSS 14.0 for Windows
software (Chicago, IL, USA). The data was initially checked for normal
distribution using the `explore' function of the software and no modifications
were necessary. Differences between the two temperatures regimes (namely
5°C and 10°C groups) were analysed using the unpaired Student's
t-test combined with the Levene's test for homogeneity of variances
to determine whether equal variances should be assumed. Results were
considered statistically significant when P<0.05.
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Results |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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Wet mass and length
The average mass of the fish incubated at 10°C was significantly
greater than those incubated at 5°C at 6 weeks after first feeding. By
contrast, at 21 weeks after first feeding, the average mass of the fish
incubated at 5°C was significantly heavier (P<0.001;
Fig. 2A). At 5°C the fish
were significantly longer (P<0.001) than those incubated at
10°C at both 6 and 21 weeks after first feeding
(Fig. 2B).
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Immunohistochemistry
Both MyoD and myogenin immunostaining was localized in the myosepta, in
agreement with the findings of Xie et al.
(Xie et al., 2001). At 6 and
21 weeks after first feeding, more positive staining of MyoD and myogenin was
found in fish incubated at 5°C (Fig.
7). In control samples (with no primary antibody), no positive
staining was found in the myosepta.
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Fish activity
Total activity of the fish from each temperature regime was measured at
three different stages (3 weeks after first feeding, 6 weeks after first
feeding and 21 weeks after first feeding) using the Linton activity monitor.
Fish reared at 5°C throughout were at least twice as active at 3 weeks,
four times more active at 6 weeks and eight times more active at 21 weeks
after first feeding than the 10°C group (P<0.001 in all
cases). Moreover, the activity of the 5°C group increased twofold from 3
weeks to 6 weeks (P<0.01) and again doubled from 6 weeks to 21
weeks (P<0.001; Fig.
8).
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Discussion |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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).
Muscle growth of Atlantic salmon occurs as a consequence of both hyperplasia
and hypertrophy of muscle fibres. Both mechanisms continue throughout growth
in salmonids (Higgins and Thorpe,
1990; Stickland,
1983). The present study has provided new information on the
longer term growth and activity up to 21 weeks after first feeding of salmon
reared at different incubation temperatures up to hatching.
In Atlantic salmon, high temperature is known to accelerate the rate of
development and growth (Hayes et al.,
1953; Marr, 1966).
In our study also, embryos incubated at 10°C hatched twice as fast as
those incubated at 5°C. At 6 weeks after first feeding, the fish that were
incubated at 10°C tended to be shorter but heavier than the 5°C group.
This shortening in the fish incubated at 10°C may be due to a decrease in
the number of vertebrae formed (Matschak
et al., 1995; Pavlov,
1984). The small difference between the two groups in the length
of fish at 6 weeks became more pronounced by 21 weeks. At 21 weeks fish
incubated at 5°C were also heavier than those incubated at 10°C. This
may be because of larval transformation and shifting from endogenous to
exogenous feeding which appears to significantly change the body mass to
length ratio in the cooler-reared group
(Nathanailides et al., 1995).
At the eyed stage, the number of the white fibres was the same in embryos
reared at both temperatures, this is in agreement with previous reports
(Usher et al., 1994).
At 6 weeks after first feeding, the total white muscle cross-sectional area
was significantly greater in the 10°C group fish, but there was no
difference in the total number of white muscle fibres. One possible
explanation is that the muscle growth of Atlantic salmon and other salmonids
in young stages is dominated by hypertrophy of existing fibres
(Higgins and Thorpe, 1990;
Kiessling et al., 1991;
Weatherley et al., 1980).
However at 21 weeks after first feeding, the total white muscle
cross-sectional area and the number of the white muscle fibres in the fish
incubated at 5°C were almost double that of the 10°C group. At both 6
weeks and 21 weeks after first feeding, there were more fibres in the small
size class in the 5°C incubation group compared with the 10°C group.
Small fibres are almost certainly an indication of new muscle fibre formation
(Stickland, 1983), which would
appear to be taking place predominantly in the 5°C group between 6 and 21
weeks after first feeding. Fig.
5 shows that these small fibres are located throughout the
myotome. The small fibres might contribute to the greater growth of the fish
incubated at 5°C.
It has been reported that cold adaptation increases the proportion of red
muscle in post-larval fish such as goldfish
(Johnston and Lucking, 1978).
However, in salmon it has been reported that temperature had no effect on red
muscle relative area in early embryonic development
(Usher et al., 1994). In our
study, incubation temperature appeared to have no influence on the proportion
of red to white muscle areas at later stages.
MyoD and myogenin in fish are key regulatory factors of muscle formation
(Rescan et al., 1994).
Activity of myogenic precursor cells is important for muscle development and
muscle growth (Grounds, 1991).
New muscle fibre hyperplasia in the post-larval growth of fish requires
myosatellite cells (Johnston et al.,
1995; Johnston et al.,
1998; Rowlerson et al.,
1985; Veggetti et al.,
1990). These cells are usually located between the sarcolemma and
the basal lamina of muscle fibres until they become activated (reviewed by
Koumans and Akster, 1995). Our
results showed staining of MyoD and myogenin in myosepta at 6 weeks and 21
weeks after first feeding, with apparently more of these protein in fish
incubated at 5°C. This is in agreement with studies on rainbow trout at
earlier stages (Xie et al.,
2001). The presence of the MRFs in myosepta is consistent with the
high density of myogenic precursor cells in this region described by Stoiber
and Sanger (Stoiber and Sanger,
1996).
It is known that salmon spend much of their time hidden in gravel and are
almost completely inactive before the yolk sac is depleted
(Bams, 1967;
Hansen and Moller, 1985). In
this experiment salmon larvae incubated at high temperature continued to
remain on the gravel after the yolk was depleted, whereas salmon larvae
incubated at 5°C were more often seen swimming up in search of food. We
therefore decided to quantify this activity at various time points.
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One possible explanation for this phenomenon is that, during embryonic
development temperature has an effect on appetite and therefore food search
activity and food intake (Fig.
9). Appetite in fish is driven by a number of factors including
neuropeptide Y which is widely distributed in the central nervous system in a
variety of fish species, including Atlantic salmon
(Vecino and Ekstrom, 1992).
Neuropeptide Y plays a critical role in the control of food intake and body
mass in salmonids (Aldegunde and Mancebo,
2006; Silverstein et al.,
1998), but there are also other factors such as galanin and
grhelin (Lin et al., 2000;
Volkoff et al., 2005). We can
speculate that incubation temperature of 5°C upregulates
appetite-stimulating factors (compared to 10°C incubation), which then
drives greater activity in the search for food. Both the muscle exercise and
increased food intake would also drive faster growth
(Fig. 9).
In conclusion, our results show that incubation temperature up to hatching influences post-hatch growth rate and the cellular mechanism of muscle growth up to 21 weeks after first feeding. In addition, incubation temperature has a very marked effect on post-hatch activity, increasingly so up to 21 weeks post-hatch.
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Acknowledgments |
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|
References |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Aldegunde, M. and Mancebo, M. (2006). Effects of neuropeptide Y on food intake and brain biogenic amines in the rainbow trout (Oncorhynchus mykiss). Peptides 27,719 -727.[CrossRef][Medline]
Ayala, M. D., Lopez-Albors, O., Gil, F., Latorre, R., Vazquez, J. M., Garcia-Alcazar, A., Abellan, E., Ramirez, G. and Moreno, F. (2000). Temperature effect on muscle growth of the axial musculature of the sea bass (Dicentrarchus labrax L.). Anat. Histol. Embryol. 29,235 -241.[CrossRef][Medline]
Ayala, M. D., Lopez Albors, O., Garcia Alcazar, A., Abellan, E., Latorre, R., Vazquez, J. M., Ramirez Zarzosa, G., Martinez, F. and Gil, F. (2003). Effect of two thermal regimes on the muscle growth dynamics of sea bass larvae, Dicentrarchus labrax L. Anat. Histol. Embryol. 32,271 -275.[CrossRef][Medline]
Bams, R. A. (1967). Differences in performance of naturally and artificially propagated Sockeye salmon migrant fry, as measured with swimming and predation tests. J. Fish. Res. Board Can. 24,1117 -1153.
Campion, D. R. (1984). The muscle satellite cell; a review. Int. Rev. Cytol. 87,225 -251.[Medline]
Goldspink, G. (1972). Postembryonic growth and differentiation of striated muscle. In The Structure and Function of Muscle (Vol. 1, 2nd edn) (ed. G. H. Bourne), pp. 179-236. New York: Academic Press.
Greer-Walker, M. (1970). Growth and development of the skeletal muscle fibres of the cod (Gadus morhua L.). J. Cons. Int. Expl. Mer 33,228 -244.
Grounds, M. D. (1991). Towards understanding skeletal muscle regeneration. Pathol. Res. Pract. 187, 1-22.[Medline]
Hansen, T. J. and Moller, D. (1985). Yolk absorption, yolk sac constrictions, mortality and growth during 1st feeding of Atlantic salmon (Salmon salar) incubated on Astro-turf. Can. J. Fish. Aquat. Sci. 42,1073 -1078.
Hayes, F. R., Pelluet, D. and Gorham, E. (1953). Some effects of temperature on the embryonic development of the salmon (Salmo salar). Can. J. Zool. 31, 42-51.
Higgins, P. and 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 -519.
Johnston, I. A. (1999). Muscle development and growth: potential implications for flesh quality in fish. Aquaculture 177,99 -115.[CrossRef]
Johnston, I. A. and Lucking, M. (1978). Temperature induced variation in the distribution of different types of muscle fibre in the goldfish (Carassius auratus). J. Comp. Physiol. 124,111 -116.
Johnston, I. A., Vieira, V. L. A. and Abercromby, M. (1995). Temperature and myogenesis in embryos of the Atlantic herring Clupea harengus. J. Exp. Biol. 198,1389 -1403.[Medline]
Johnston, I. A., Cole, N. J., Abercromby, M. and Vieira, V. L. A. (1998). Embryonic temperature modulates muscle growth characteristics in larval and juvenile herring. J. Exp. Biol. 201,623 -646.[Medline]
Johnston, I. A., McLay, H. A., Abercromby, M. and Robins, D. (2000). Early thermal experience has different effects on growth and muscle fibre recruitment in spring- and autumn-running Atlantic salmon populations. J. Exp. Biol. 203,2553 -2564.[Abstract]
Johnston, I. A., Vieira, V. L. A. and Temple, G. K. (2001). Functional consequences and population differences in the developmental plasticity of muscle to temperature in Atlantic herring Clupea harengus. Mar. Ecol. Prog. Ser. 213,285 -300.
Kiessling, A., Storebakken, T., Asgard, T. and Kissling, K. H. (1991). Changes in the structure and function of the epaxial muscle of rainbow trout (Oncorhynchus mykiss) in relation to ration and age. I. Growth dynamics. Aquaculture 93,335 -356.[CrossRef]
Koumans, J. T. M. and Akster, H. A. (1995). Myogenic cells in development and growth of fish (review). Comp. Biochem. Physiol. 110A,3 -20.[CrossRef][Medline]
Krogh, A. (1914). On the influence of the temperature on the rate of embryonic development. Z. Allgemeine Physiol. 16,163 -177.
Lin, X., Volkoff, H., Narnaware, Y., Bernier, N. J., Peyon, P. and Peter, R. E. (2000). Brain regulation of feeding behavior and food intake in fish. Comp. Biochem. Physiol. 126A,415 -434.[CrossRef][Medline]
Marr, D. H. (1966). Influence of temperature on the efficiency of growth of salmonid embryos. Nature 212,957 -959.[CrossRef][Medline]
Matschak, T. W. and Stickland, N. C. (1995). The growth of Atlantic salmon (Salmo salar L.) myosatellite cells in culture at two different temperatures. Cell. Mol. Life Sci. 51,260 -266.
Matschak, T. W., Stickland, N. C., Crook, A. R. and Hopcroft, T. (1995). Is physiological hypoxia the driving force behind temperature effects on muscle development in embryonic Atlantic salmon (Salmo salar L.). Differentiation 59, 71-77.[CrossRef]
Matschak, T. W., Stickland, N. C., Mason, P. S. and Crook, A. R. (1997). Oxygen availability and temperature affect embryonic muscle development in Atlantic salmon (Salmo salar L.). Differentiation 61,229 -235.[CrossRef]
Nachlas, M. M., Tsou, K. C., Desouza, E., Cheng, C. S. and Seligman, A. M. (1957). Cytochemical demonstration of succinic dehydrogenase by the use of pnitrophenyl substituted ditetrazolium. J. Histochem. 5,420 -436.[Abstract]
Nathanailides, C., Lopez-Albors, O. and Stickland, N. C. (1995). Influence of prehatch temperature on the development of muscle cellularity in posthatch Atlantic salmon (Salmo salar). Can. J. Fish. Aquat. Sci. 52,675 -680.
Naylor, R. L., Goldburg, R. J., Primavera, J. H., Kautsky, N., Beveridge, M. C., Clay, J., Folke, C., Lubchenco, J., Mooney, H. and Troell, M. (2000). Effect of aquaculture on world fish supplies. Nature 405,1017 -1024.[CrossRef][Medline]
Pavlov, D. (1984). Effect of temperature during early ontogeny of Atlantic salmon, Salmo salar. I. Variability of morphological characters and duration of development under different temperatures. J. Ichtyol. 24, 30-38.
Rayne, J. and Crawford, G. N. C. (1975). Increase in fibre numbers of the rat pterygoid muscles during postnatal growth. J. Anat. 119,347 -357.[Medline]
Rescan, P. Y. (2001). Regulation and functions of myogenic regulatory factors in lower vertebrates. Comp. Biochem. Physiol. 130B,1 -12.[CrossRef][Medline]
Rescan, P. Y., Gauvry, L., Paboeuf, G. and Fauconneau, B. (1994). Identification of a muscle factor related to MyoD in a fish species. Biochim. Biophys. Acta 1218,202 -204.[Medline]
Rowlerson, A. and Veggetti, A. (2001). Muscle Development and Growth: Fish Physiology. Vol.18 . New York: Academic Press.
Rowlerson, A., Scapolo, P. A., Mascarello, F., Carpene, E. and Veggetti, A. (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.[CrossRef][Medline]
Rudnicki, M. A. and Jaenisch, R. (1995). The MyoD family of transcription factors and skeletal myogenesis. BioEssays 17,203 -209.[CrossRef][Medline]
Rudnicki, M. A., Schnegelsberg, P. N., Stead, R. H., Braun, T., Arnold, H. H. and Jaenisch, R. (1993). MyoD or Myf-5 is required for the formation of skeletal muscle. Cell 75,1351 -1359.[CrossRef][Medline]
Silverstein, J. T., Breininger, J., Baskin, D. G. and Plisetskaya, E. M. (1998). Neuropeptide Y-like gene expression in the salmon brain increases with fasting. Gen. Comp. Endocrinol. 110,157 -165.[CrossRef][Medline]
Stickland, N. C. (1983). Growth and development of muscle fibres in the rainbow trout (Salmo gairdneri). J. Anat. 137,323 -333.[Medline]
Stickland, N. C., White, R. N., Mescall, P. E., Crook, A. R. and 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.[CrossRef][Medline]
Stoiber, W. and Sanger, A. M. (1996). An electron microscopic investigation into the possible source of new muscle fibres in teleost fish. Anat. Embryol. 194,569 -579.[Medline]
Temple, G. K., Cole, N. J. and Johnston, I. A.
(2001). Embryonic temperature and the relative timing of
muscle-specific genes during development in herring (Clupea harengus
L.). J. Exp. Biol. 204,3629
-3637.
Usher, M. L., Stickland, N. C. and Thorpe, J. E. (1994). Muscle development in Atlantic salmon (Salmo salar) embryos and the effect of temperature on muscle cellularity. J. Fish Biol. 44,953 -964.[CrossRef]
Vecino, E. and Ekstrom, P. (1992). Colocalization of neuropeptide Y (NPY)-like and FMRFamide-like immunoreactivities in the brain of the Atlantic salmon (Salmo salar). Cell Tissue Res. 270,435 -442.[CrossRef][Medline]
Veggetti, A., Mascarello, F., Scapolo, P. A. and Rowlerson, A. (1990). Hyperplastic and hypertrophic growth of lateral muscle in Dicentrarchus labrax (L.). An ultrastructural and morphometric study. Anat. Embryol. 182, 1-10.[Medline]
Volkoff, H., Canosa, L. F., Unniappan, S., Cerda-Reverter, J. M., Bernier, N. J., Kelly, S. P. and Peter, R. E. (2005). Neuropeptides and the control of food intake in fish. Gen. Comp. Endocrinol. 142,3 -19.[CrossRef][Medline]
Weatherley, A. H. and Gill, H. S. (1984). Growth dynamic of white myotomal muscle fibres in the bluntnose minnov Pimephales notatus rafinesque and comparison with rainbow trout Salmo gairdneri Richardson. J. Fish Biol. 25, 13-24.[CrossRef]
Weatherley, A. H., Gill, H. S. and Rogers, S. C. (1980). The relationship between mosaic muscle fibres and size in rainbow trout (Salmo gairdneri). J. Fish Biol. 17,603 -610.[CrossRef]
Weatherley, A. H., Gill, H. S. and Lobo, A. F. (1988). Recruitment and maximal diameter of axial muscle fibre in teleost and their relationship to somatic growth and ultimate size. J. Fish Biol. 33,851 -859.[CrossRef]
Wilkes, D., Xie, S. Q., Stickland, N. C., Alami-Durante, H., Kentouri, M., Sterioti, A., Koumoundouros, G., Fauconneau, B. and Goldspink, G. (2001). Temperature and myogenic factor transcript levels during early development determines muscle growth potential in rainbow trout (Oncorhynchus mykiss) and sea bass (Dicentrarchus labrax). J. Exp. Biol. 204,2763 -2771.[Medline]
Xie, S. Q., Mason, P. S., Wilkes, D., Goldspink, G., Fauconneau, B. and Stickland, N. C. (2001). Lower environmental temperature delays and prolongs myogenic regulatory factor expression and muscle differentiation in rainbow trout (Onchrhynchus mykiss) embryos. Differentiation 68,106 -114.[CrossRef][Medline]
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