close

Вход

Забыли?

вход по аккаунту

?

573

код для вставкиСкачать
JOURNAL OF EXPERIMENTAL ZOOLOGY 284:299–308 (1999)
Hyperplastic Development and Hypertrophic
Growth of Muscle Fibers in the White Seabass
(Atractoscion nobilis)
ANASTASIA MARIA ZIMMERMAN AND MARY SUE LOWERY*
University of San Diego, San Diego, California 92110
ABSTRACT
Because skeletal muscle is the main contributor to body weight in most fish, it is
probable that the size of a fish is limited by the growth of this tissue. Several aspects of both
somatic size and skeletal muscle growth were investigated in white seabass (Atractoscion nobilis).
One hundred and four subjects ranging in size from 1.3–91.8 cm standard length were examined
to discern growth patterns throughout the entire life span of this species. Relationships of somatic
growth were evaluated by weight, length, and age comparisons while muscle growth was assessed
from cross-sectional area measurements of white muscle fibers. The average cross-sectional fiber
area increased from approximately 150 µm2 to 4300 µm2 as the fish increased in size, indicating
that hypertrophy plays an important role in growth. Hyperplastic fiber recruitment accounted for
approximately 93% of muscle growth in recently hatched fish and gradually decreased with fish
length. Although the contribution of hyperplasia declined to less than 1% in the largest subject,
the persistence of hyperplasia at standard lengths equal to or greater than 91.8 cm as observed in
the white seabass has yet to be documented in other fish species. This sustained fiber recruitment
may be responsible for the impressive ultimate standard length of 133 cm (41 kg) that white
seabass are capable of attaining. The white seabass currently represents the largest marine fish
species for which the dynamics of muscle fiber growth have been described. J. Exp. Zool. 284:299–
308, 1999. © 1999 Wiley-Liss, Inc.
Somatic growth is generally viewed as an increase in body size resulting from growth of several if not all of the tissues comprising the
organism. Skeletal muscle tissue represents a significant portion of the mass of most fish, and may
compose between 30–80% of their live weight
(Weatherley and Gill, ’87). Because skeletal
muscle may be the main contributor to body mass
it is probable that the size of a fish is limited by
the growth of this tissue. Investigating muscle
growth is an important focus of study from a biological standpoint as the growth of this tissue may
underlie the overall somatic growth in fish.
Muscle growth is a dynamic process in fish that
begins early in their development and continues
throughout much if not all of their life span. During initial myogenesis several mitotically active
stem cells, referred to as myosatellite cells, fuse together to form individual multinucleated muscle fiber cells (Nag and Nursall, ’72; Campion, ’84;
Schultz, ’89; Matschak and Stickland, ’95). Resulting muscle fibers are the fundamental unit of skeletal muscle tissue, as hundreds to several thousand
fibers collectively form a single muscle mass. Further recruitment of new fibers (hyperplasia) and
enlargement of existing fibers (hypertrophy) within
© 1999 WILEY-LISS, INC.
a muscle mass often continues well past the age
of sexual maturity in fish.
Individual fibers are often classified as being red,
pink, or white based on metabolic and structural
properties. In fish musculature different fiber types
are not intermingled but are separated into either
superficial muscle masses comprised exclusively of
red fibers or deep muscle masses composed entirely
of white fibers. Because deep muscle masses may
comprise more than 90% of the total volume of
muscle tissue in fish (Weatherley and Gill, ’89) it is
probable that increasing body size is due in large
part to growth of white muscle fibers.
Several studies have demonstrated that recently
recruited fibers in fish are relatively small in size
and that these fibers increase in cross-sectional
area through hypertrophic growth(Moss and
LeBlond, ’71; Stickland, ’83; Ennion et al., ’95).
Because hyperplasia is associated with small fibers and hypertrophy is correlated with fibers of
greater dimensions, the size of individual fibers
can therefore be used to assess muscle growth at
*Correspondence to: Mary Sue Lowery, USD Biology Department,
5998 Alcala Park, San Diego, CA 92110. E-mail: slowery@acusd.edu
Received 25 July 1998; Accepted 25 November 1998.
300
A.M. ZIMMERMAN AND M.S. LOWERY
different life stages. Hyperplastic and hypertrophic growth patterns have been described for
several species of fish representing different taxonomic families which display a broad range of
maximum reported sizes (Weatherley and Gill, ’81,
’84, ’85; Stickland, ’83; Weatherley et al., ’88;
Higgins and Thorpe, ’90; Vegetti et al., ’90;
Rowlerson et al., ’95). The contributions of hyperplasia and hypertrophy appear dependent on both
the species and ultimate somatic size of the fish.
In species of small maximum reported body sizes,
it is generally found that hyperplasia ceases early
in development and most growth after hatching
is attributed to hypertrophy. Conversely, in species capable of attaining large sizes hyperplasia
continues to be an important contributor to muscle
growth into the adult phase. These findings provide strong indications that the overall contribution of hyperplastic growth is responsible for
determining the ultimate attainable size of a fish.
The purpose of this study was to investigate several aspects of somatic and muscle fiber growth in
the white seabass. Somatic growth was evaluated
through weight, length, and age relationships and
muscle growth was investigated by measuring the
cross-sectional area of fibers representative of recently hatched to sexually mature specimens. These
measurements enabled us to assess the contributions of hyperplasia and hypertrophy throughout
the entire life span of this species of fish. We believe our findings provide considerable insight into
the processes that enable white seabass to grow to
their impressive ultimate total length of 1.5 m and
maximum reported weight of 41 kg (Miller and Lea,
’76). This understanding, in addition to its biological interest, has potential value for enhancing applied aquaculture techniques and furthers the
knowledge of hyperplastic and hypertrophic growth
patterns in fish. The white seabass currently represents the largest marine fish species for which
the dynamics of muscle fiber growth have been
discerned.
were established and four fish representative of
each size class were obtained. These fish were
progeny of hatchery-spawns and were raised under similar (if not identical) conditions. Several
larger hatchery-reared subjects of 21.5–50.5 standard length were also obtained for comparison.
White seabass exceeding these sizes are quite rare
in the wild and are prized as hatchery broodstock
fish when caught in southern California. Therefore, in order to investigate extremely large white
seabass, specimens were obtained as hatchery
broodstock mortality occurred, resulting in acquisition of subjects ranging from 56.5 to 91.8 cm
standard length.
MATERIALS AND METHODS
Measurement of fiber size
Subjects
Specimens of white seabass were generously
provided by the Hubbs Sea World Research
Institute’s fish hatchery located in Carlsbad, CA.
Subject selection was based on standard length
(tip of lower jaw to the base of the caudal fin)
since this parameter is a reliable indicator of body
size. Twenty size classes separated by 1-cm divisions ranging from 1.0 to 20.9 cm standard length
Muscle samples
Fish were transferred to the University of San
Diego and upon arrival were sacrificed by an overdose of methanesulfonate salt. Samples of epaxial
white skeletal muscle were extracted from the
right side of each fish at a region directly beneath
and posterior to the first ray of their dorsal fin.
This site was easily located on any size white
seabass and provided the greatest abundance of
skeletal muscle tissue comprised entirely of white
muscle fibers in these fish. The size of each muscle
sample was approximately 0.5 cm in width and
2.0 cm in length although for subjects smaller
than 3.0 cm, muscle samples were inevitably
smaller in accordance with fish length.
Histological techniques
Samples were fixed by immersion in 10% buffered formalin, dehydrated through a graded series of alcohol, and embedded in paraffin. Tissue
blocks were orientated so fibers were cut at a right
angle to their main axis during sectioning. Muscle
sections (5 µm) were stained with haemotoxylin
and eosin and mounted on microscope slides. Resulting sections exhibited a mosaic appearance
and individual fibers were polyhedral in shape as
shown in Fig. 1.
The cross-sectional areas of individual fibers
within each section were determined using an image analysis system consisting of a Leica Q500MC
computer with corresponding image analysis software and a video camera attached to a light microscope. This setup enabled a field of muscle
fibers viewed under the microscope to be projected
onto the computer monitor screen. The area of a
slide representing a single pixel on the monitor
screen was determined through calibration with
MUSCLE FIBER GROWTH IN WHITE SEABASS
301
number of fibers contained in fish measuring 1.7,
7.0, 18.2, 31.4, 73.0, and 88.0 standard length
were determined. The entire body region located
between the first and second dorsal fins of each
fish was sectioned. Depending on the size of the
body cross-section, it was viewed under either a
dissecting microscope or a non-magnified video
camera that was attached to the previously described image analysis system. Using this system
the total surface area of white muscle tissue from
each body section was measured. A small sample
of muscle tissue was subsequently removed from
each section and its corresponding area was also
measured. These samples were processed in the
same manner described for all other muscle
samples and the fiber cross-sections present in
each sample were counted. Because this sum represented a known proportion of the total white
muscle it was possible to extrapolate a realistic
estimate of the total number of fibers present in
each fish.
Assessment of hyperplasia and hypertrophy
Fig. 1. White fiber cross-sections from a white seabass of
19.2 cm standard length. Mosaic appearance of muscle section and polyhedral shape of individual fibers are characteristic of all subjects. Bar = 20 µm, the diameter of the largest
fibers considered to be hyperplastic.
a stage micrometer. Using the system software
the sum of pixels contained within an individual
fiber viewed on the monitor screen was determined and converted into the actual cross-sectional area of each fiber. In order to ensure a
significant sample size, the cross-sectional areas
of 500 different muscle fibers were measured for
each fish. Extensive editing of images was often
done to ensure that fibers were viewed individually and free from any debris. Fibers exhibiting
an extremely elongated cross-sectional shape were
not measured as it was presumed that these fibers were not true cross-sections and might exhibit a significantly larger area than if cut at a
right angle.
Estimation of total fiber number
To estimate the total number of fibers present
throughout the life span of the white seabass, the
A new fiber arising through hyperplasia is relatively small in size and through hypertrophic
growth it increases in size. Several researchers
have considered fibers less than 20 µm in diameter to represent fibers recruited by hyperplasia
and those exceeding this diameter to represent
fibers which had subsequently grown by hypertrophy (Stickland, ’83; Weatherley and Gill, ’84;
Weatherley et al., ’88; Rowlerson et al., ’95). Hyperplastic and hypertrophic growth in the white
seabass was similarly assessed using this established 20 µm diameter criterion in order to make
comparisons to other fish species. The conversion
of cross-sectional areas to equivalent diameter values was made according to Weatherley et al. (’84)
using the assumption that individual fiber crosssections are circular. Under this assumption the
cross-sectional area of a fiber is considered to be
equal to that of a circle (πr2). Therefore, fibers exhibiting areas under 314 µm2 can be attributed
to hyperplasia whereas those exceeding 314 µm2
are considered a result of hypertrophic growth.
RESULTS
A total of 52,000 fibers from 104 white seabass
ranging in size from 1.3 to 91.8 cm standard
length were measured. The smallest fish in this
range was a recently hatched specimen whereas
the 91.8 cm fish was relatively close to the 133
cm maximum recorded standard length of this
species. Eighty of these fish consisted of members
302
A.M. ZIMMERMAN AND M.S. LOWERY
from the established 20 size classes (1.0–20.9 cm
SL) that were spawned and reared under similar
conditions at the hatchery facility. The larger fish
had experienced more varied conditions when compared to those of the established size classes. In
addition to their acquisition following mortality,
the largest fish (56.5–91.8 cm SL) were originally
members of a wild population prior to their capture and transfer to the hatchery facility. The biases attributed to these variances could not be
assessed and therefore statistical analysis was
performed only on data collected from subjects
comprising the established size classes. The inclusion of the largest subjects in this study is essential, however, as their results prove to have
important comparative value.
It was not possible to determine the sex of immature specimens and it was presumed that the
ratio of male to female subjects was likely to be
equal. Thomas (’68) demonstrated that the weight
and length relationship of late juveniles and mature white seabass is unaffected by gender. Recently hatched and early juvenile white seabass
used in our investigation probably also exhibit an
unbiased size relationship; therefore, gender was
not considered a factor biasing the results obtained in this investigation. Standard length was
compared to weight, age, total fiber number, average fiber area, and fiber distribution, and the
relative contributions of hyperplasia and hypertrophy were determined.
Body weight and length relationship
The measurements of standard length (SL) to
corresponding body weight are represented in Fig.
2. Their statistical relationship was determined
by calculation of the following regression curve:
(Weight) = 0.038(SL2.707) (r2 = 0.995). The shape
of this curve indicates that the amount of weight
gain associated with increasing length becomes
progressively greater as the fish increase in size.
Fig. 2. Relationship between standard length (SL) and corresponding weight (W) for white seabass comprising the 20
established size classes. The relationship was fitted using an
exponential curve: (W) = 0.038(SL2.707) (n = 80, r2 = 0.995).
Total fiber number
The total number of fibers contained within fish
of 1.7, 7.0, 18.2, 31.4, 73.0, and 88.0 cm standard
length are shown in Fig. 4. These results clearly
indicate that the white seabass develop new fibers
during much of their lives. However, because of the
low sample number, it is not possible to determine
whether recruitment continues throughout their
entire size range or if a plateau of relatively constant fiber numbers occurs.
Average fiber area
Age and length relationship
The age of each fish was calculated as the time
elapsed from the date at which it was spawned
until the date at which it was sacrificed. Standard length plotted against age is shown in Fig.
3. The statistical relationship existing between
these variables was calculated utilizing a linear
regression analysis and was determined to be: (SL)
= 0.075(Age) – 0.055 with an r2 value of 0.947.
The increase of standard length with age indicates
that these subjects were in a state of growth.
The average fiber area was found to increase
linearly with the length of the fish (Fig. 5). Regression analysis determined r2 = 0.828 for the following relationship: (Average fiber area) = 98.617
+ 28.714 (SL). This increasing fiber area indicates
that hypertrophy is an important contributor to
overall muscle growth. Although only the established size classes (1.0–20.9 cm SL) were included
in our statistical analysis, the data obtained from
the larger fish appear to follow similar trends as
shown in Table 1.
MUSCLE FIBER GROWTH IN WHITE SEABASS
Fig. 3. Relationship between age and standard length (SL)
for white seabass comprising the 20 established size classes.
The solid line was fitted using a linear regression: (SL) =
0.075(Age) – 0.055 (n = 80, r2 = 0.947).
303
Fig. 4. Relationship between total fiber number and standard length for white seabass. The solid line represents the
following linear regression: (Total fiber number) = 8283(SL)
– 25764 (n = 6, r2 = 0.941).
Range of fiber area
The dynamics of fiber growth are perhaps best
illustrated by investigating the distribution of fiber area in relation to standard length. The series of histograms shown in Fig. 6 depicts the
relative percentage of fiber area in relation to increasing standard length. The 20 established size
classes are consolidated into the first four histograms and the remaining four histograms reflect
groupings of the larger subjects into classes each
spanning a range of 20 cm in standard length.
Hyperplasia and hypertrophy
The relative contribution of hyperplasia in relation to standard length of the established size
classes is illustrated in Fig. 7. The percentage
of fibers exhibiting hyperplastic growth for the
entire range of standard lengths is shown in
Table 2. Hyperplasia appears to be the dominant growth process in recently hatched white
seabass and although this type of growth decreases as these fish increase in size it remains
an important contributor well into their adult
phase. The decrease of fibers associated with
hyperplasia coincides with a proportional increase
of fibers attributed to hypertrophic growth. Hypertrophy of existing fibers may make a larger
contribution to overall muscle growth as hypertrophic fibers account for a progressively greater
percentage of overall total fiber volume as the
white seabass increase in size.
DISCUSSION
Origin of recruited fibers
The total number of fibers comprising individual
white seabass was found to increase with increasing body size (Fig. 4) indicating that white seabass
develop new fibers during much if not all of their
lives. Considerable evidence indicates that small
recruited fibers originate from the differentiation
of myosatellite cells (Nag and Nursall, ’72; Campion, ’84; Schultz, ’89; White and Esser, ’89;
Veggetti, ’90). It has been suggested, however, that
increasing fiber number may result from the splitting of existing fibers. Although fiber splitting has
been demonstrated in the eel, Anguilla anguilla
304
A.M. ZIMMERMAN AND M.S. LOWERY
Fig. 5. Relationship between average fiber area and standard length of white seabass. Each point is an average calculated from 500 individual fibers from each of 80 subjects. The
illustrated line represents the following linear regression: (Average fiber area) = 28.714(SL) + 99.617 (r2 = 0.828).
(Willemse and Van den Berg, ’78), and suggested in
the gray mullet, Mugil capito (Scapolo et al., ’84),
the preponderance of evidence discounts fiber
splitting as the probable mechanism for increasing fiber number in most fish (Greer-Walker, ’70;
Stickland, ’83; Weatherley and Gill, ’84; Powell et
al., ’89; Koumans et al., ’90, ’93a,b, ’94; Koumans
and Akster, ’95; Matschak and Stickland, ’95). Furthermore, in some species small fibers have been
shown to contain unique embryonic myosin isoforms, supporting a new origin of the small fibers
rather than formation by splitting of existing fiFig. 6. Distribution of fiber area in relation to increasing
standard length. Each histogram represents a consolidation
of size classes as indicated in the upper right corner. The
first four histograms (1.0–20.9 cm) each reflect measurements
from 20 different fish and 10,000 individual fibers. The remaining histograms are representations of the following: 5
fish and 2500 fibers (21.0–39.9 cm); 7 fish and 3500 fibers
(40.0–59.9 cm); 10 fish and 5000 fibers (60.0–79.9 cm) and 2
fish and 1000 fibers (80.0–91.8 cm).
MUSCLE FIBER GROWTH IN WHITE SEABASS
305
TABLE 1. Weight, age and average fiber area of larger
white seabass subjects1
SL
(cm)
No. of
fish
Weight
(g)
Age2
(days)
Fiber area
(µm2)
21.0–29.9
30.0–39.9
40.0–49.9
50.0–59.9
60.0–69.9
70.0–79.9
80.0–89.9
90.0–99.9
3
2
5
2
3
7
1
1
199 ± 83
607
1,741 ± 206
2,459
3,406 ± 503
4,653 ± 1,182
7,140
8,270
254 ± 7
410
464 ± 0
Unknown3
Unknown3
Unknown3
Unknown3
Unknown3
813 ± 74
1,393
1,152 ± 137
1,027
1,601 ± 114
1,561 ± 446
2,518
4,315
Values stated as means ± standard deviation where possible.
Age calculated as time elapsed from spawn until sacrifice.
3
Fish that were once members of wild populations.
1
2
bers (Ennion et al., ’95; Rowlerson et al., ’97).
Small fibers recruited in the white seabass are
considered to have originated from myosatellite
cells and not by fiber splitting. This conclusion is
in agreement with results from other investigated
fish species and is further supported by our discovery of myosatellite cells in the white seabass
(unpublished data).
Fiber distribution
The average fiber area was found to increase
with standard length (Fig. 5) with individual
fish often comprised of fibers exhibiting a wide
range of areas. This range of fiber area was responsible for the mosaic appearance of muscle
sections (Fig. 1). Histograms, shown in Fig. 6,
clearly indicate that the distribution of fiber
area varies considerably with length. In the
smallest fish (1.0–5.0 cm SL), fibers are initially
confined to a small range between 10 and 1,130
µm2 with a high percentage exhibiting areas
under 200 µm 2. As the subjects increase in
length this range becomes progressively broader
and in the largest fish (91.8 cm SL) the range
of fiber sizes was found to extend between 168
and 10,730 µm2. This wide range of fiber sizes
in each class indicates that at every length investigated, both hyperplastic development and
hypertrophic growth occur.
Hyperplastic and hypertrophic growth
Hyperplasia is the dominant growth process in
recently hatched white seabass and gradually decreases as these fish increase in size (Fig. 7 and
Table 2). In the smallest size class (1.0–1.9 cm
SL) approximately 93% of their fibers are considered to be in a state of hyperplastic growth
whereas the contribution of hyperplasia in the
Fig. 7. Relative percentage of hyperplastic fibers in relation to standard length (SL) of white seabass comprising the
20 established size classes. The illustrated curve represents
the best fit between these variables: (% of hyperplastic fibers) = 98.67e–0.0603(SL) (n = 80, r2 = 0.84).
largest specimen (91.8 cm SL) was found to have
decreased to 0.8%. This finding that the relative
contribution of hyperplasia is greatest early in the
life of the white seabass and decreases with standard length is in agreement with skeletal muscle
growth patterns reported in other species (Stickland, ’83; Weatherley and Gill, ’84, ’85; Weatherley
TABLE 2. Hyperplastic fibers from white seabass
of all size classes1
SL
(cm)
1.0–5.9
6.0–10.9
11.0–15.9
16.0–20.9
21.0–39.9
40.0–59.9
60.0–79.9
80.0–91.3
1
2
No. of
fish
No. of fibers
measured
Relative %
hyperplastic fibers2
20
20
20
20
5
7
10
2
10,000
10,000
10,000
10,000
2,500
3,500
5,000
1,000
82 ± 9
59 ± 9
44 ± 6
33 ± 8
22 ± 10
20 ± 7
9±5
1
Hyperplastic fibers are those <314 µm2.
% values stated as means ± standard deviation where possible.
306
A.M. ZIMMERMAN AND M.S. LOWERY
et al., ’88; Higgins and Thorpe, ’90; Veggetti et
al., ’90; Rowlerson et al., ’95). However, several previous investigations found not only that hyperplasia decreased with standard length but also that
once the fish reached a certain size hyperplastic
growth ceased completely (Weatherley et al., ’80b,
’88; Stickland, ’83; Weatherley and Gill, ’84; Kundu
and Mansuri, ’90, ’92). The persistence of hyperplasia at standard lengths equal to or greater than
91.8 cm as observed in the white seabass has yet
to be documented in other species.
In perhaps the most extensive study of this sort
of growth, Weatherley and his colleagues (Weatherley et al., ’79, ’80a, ’80b, ’88; Weatherley and Gill,
’81, ’84, ’85, ’89) investigated hyperplasia in 10 distantly related fish species from three orders and
five families. The maximum reported sizes exhibited by these ten species ranged from 10 to 165
cm total length although the largest subjects they
examined ranged between 65.0 and 69.9 cm. In
these investigations hyperplasia was found to cease
in these fish at lengths which were approximately
44% of the ultimate total length of each species.
According to their relationship hyperplasia in the
white seabass is predicted to cease at 66.0 cm total length (57.7 cm SL). This was not the case in
our investigation as we found white seabass to
clearly exhibit hyperplasia at sizes greater than
57.7 cm standard length. In fact, hyperplasia persisted well past this predicted value within the
next largest size class (60.0–79.9 cm SL) where
9% of these fibers were scored as hyperplastic
(Table 2). The occurrence of hyperplasia was not
concentrated in the lower range of this size class,
rather hyperplastic fibers were evenly distributed
between 60.0 and 79.9 cm standard length. Four
hyperplastic fibers ranging in size from 168 to 305
µm2 were also documented within the 500 fibers
measured from the largest white seabass (91.3 cm
SL) indicating that hyperplasia occurs at every
length examined in this investigation.
Our data clearly indicate that white seabass retain their hyperplastic ability far beyond that
which has been documented in other species. In
fact, the occurrence of hyperplastic fibers in our
largest subject indicates that white seabass exhibit hyperplasia at lengths which are 74% of their
ultimate size. Even with a conservative approach
that considers 79.9 cm as the largest size with
substantial hyperplasia, white seabass exhibit hyperplasia at 61% of their ultimate size. Either percentage is substantially greater than the 44%
which would be predicted using Weatherley’s relationship. There are several possible reasons for
this discrepancy, perhaps the most intriguing of
which is that white seabass may have uniquely
retained the ability to recruit muscle fibers
throughout their entire lives. It is also plausible
that the white seabass may lose their hyperplastic ability at lengths greater than those observed
in our study.
When making comparisons between these types
of investigations one should consider that the histological methods utilized, although similar, are
not completely uniform. Variation in the fixatives
and subsequent processing of muscle samples is
likely to produce size differences in the resulting
fiber cross-sections. These differences are often a
result of variation in shrinkage imparted to both
fibers and their surrounding connective tissue during fixation (Bourne, ’72). Fiber shrinkage was observed in the white seabass tissue; however, since
each sample was processed in the same manner,
the extent of this shrinkage was considered to be
consistent. This artifact of fiber shrinkage was
similarly addressed in several of the previously
cited studies although it was never quantified.
Therefore, it is not possible to determine if the
white seabass fibers endured a greater or lesser
degree of shrinkage that might lead to either an
over- or underestimation of hyperplasia when compared to previous studies. It is for this reason that
direct numerical comparisons between investigations may be problematic. Nevertheless, although
the accuracy of numerical comparisons may be
uncertain, it is reasonable to draw reliable conclusions by comparing overall trends between different investigations.
Hyperplasia facilitates ultimate size
Previous research has shown that species of fish
that experience long periods of hyperplasia reach
larger body sizes than those that grow primarily
through hypertrophy (Weatherley et al., ’80b, ’88;
Stickland, ’83; Weatherley and Gill, ’84, ’85, ’89;
Calvo, ’89; Kundu and Mansuri, ’90, ’92; Veggetti
et al., ’90; Battram and Johnson, ’91; Koumans et
al., ’93b; Rowlerson et al., ’95). The findings of
the current investigation are in agreement with
this trend, as hyperplasia was found to persist
well into the adult phases of the white seabass, a
species that attains a relatively large ultimate
size. Considerable evidence therefore suggests
that fiber recruitment holds the main role in determining the ultimate size of a fish.
This phenomenon of hyperplasia facilitating ultimate size can be explained by considering the
metabolic exchange processes of individual fibers.
MUSCLE FIBER GROWTH IN WHITE SEABASS
During hyperplasia the individual muscle fiber is
small in size, thereby creating a high surface-tovolume ratio that facilitates processes such as
amino acid assimilation and metabolic removal of
cellular waste products. Hypertrophic growth begins as existing fibers are augmented in size, leading to a decrease in their surface-to-volume ratio.
As hypertrophy continues, an increasingly inefficient and potentially unfavorable situation develops as a result of this decreasing surface area
which causes a limiting of metabolic exchange.
Weatherley et al. (’88) proposed that beyond a
critical fiber size the continuation of hypertrophic
growth would result in impairing metabolic exchange. According to their hypothesis the ultimate
size to which a fish could grow would correlate
with the attainment of this final critical size by
all comprising fibers. Weatherley (’90) suggests
that the critical fiber diameter at which surface
area becomes limiting ranges from 120 to 270 µm
in fish. The largest white seabass fiber measured
in our investigation corresponds to a 117 µm diameter and was found in the largest subject (91.8
cm SL). It is probable that white seabass exceeding 91.8 cm standard length would have fibers that
had grown to the metabolically restrictive sizes indicated by Weatherley (’90). The prolonged hyperplasia and lack of a restrictive maximum fiber size
throughout most of the life span observed in the
white seabass is likely to delay the onset of impaired
metabolic exchange in these fish. It is therefore reasonable to conclude that this prolonged hyperplastic growth is responsible for enabling this species
of fish to grow to their impressive ultimate size.
LITERATURE CITED
Battram J, Johnston I. 1991. Muscle growth in the Antarctic
teleost, Notothenia neglecta (Nybelin). Antarct Sci 3:29–33.
Bourne G. 1972. The structure and function of muscle. New
York: Academic Press.
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 35:207–214.
Campion D. 1984. The muscle satellite cell: a review. Int Rev
Cytol 87:225–247.
Ennion S, Gauvry L, Butterworth P, Goldspink G. 1995.
Small-diameter white myotomal muscle fibers associated
with growth hyperplasia in the carp (Cyprinus carpio) express a distinct myosin heavy chain gene. J Exp Biol
198:1603–1611.
Greer-Walker M. 1970. Growth and development of the skeletal muscle fibres of the cod (Gadus morhua L.). J Cons Int
Explor Mer 33:228–244.
Higgins P, Thorpe J. 1990. Hyperplasia and hypertrophy in
the growth of skeletal muscle in juvenile Atlantic salmon,
Salmo salar L. J Fish Biol 37:505–519.
Koumans J, Akster H. 1995. Myogenic cells in development
and growth of fish. Comp Biochem Physiol 100:3–20.
307
Koumans J, Akster H, Dulos G, Osse J. 1990. Myosatellite
cells of Cyprinus carpio (Teleosteri) in vitro: isolation, recognition and differentiation. Cell Tissue Res 261:173–181.
Koumans J, Akster H, Booms R, Osse J. 1993a. 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.
Koumans J, Akster H, Booms R, Osse J. 1993b. Influence of
fish size on proliferation and differentiation of cultured
myosatellite cells of white axial muscle of carp (Cyprinus
carpio L.). Differentiation 53:1–6.
Koumans J, Akster H, Witkam A, Osse J. 1994. Numbers of
muscle nuclei and myosatellite cell nuclei in red and white
axial muscle during growth of the carp (Cyprinus carpio). J
Fish Biol 44:391–408.
Kundu R. 1991. Muscle fibre diameter and its relationship
with body shape and size in some marine fish. J Curr Biosci
8:53–61.
Kundu R, Mansuri A. 1990. Growth dynamics of myotomal
muscle fibers in a carangid, Caranx malabaricus. J Fish
Biol 36:21–27.
Kundu R, Mansuri A. 1992. Growth of pectoral muscle fibres
in relation to somatic growth in some marine fishes. Neth
J Zool 42:595–606.
Matschak T, Stickland N. 1995. The growth of Atlantic salmon
(Salmo salar L.) myosatellite cells in culture at two different temperatures. Experientia 51:260–266.
Miller D, Lea R. 1976. Guide to the coastal marine fishes of
California. CA Dept. of Fish and Game: Fish Bulletin
157:154.
Moss F, LeBlond C 1971. Satellite cells as the source of nuclei in muscles of growing rats. Anat Rec 170:421–436.
Nag A, Nursall J. 1972. Histogenesis of white and red muscle
fibres of trunk muscles of a fish Salmo gairdneri. Cytobios
6:227–246.
Powell R, Dodson M, Cloud J. 1989. Cultivation and differentiation of satellite cells from skeletal muscle of the rainbow trout Salmo gairdneri. J Exp Zool 250:333–338.
Rowlerson A, Mascarello F, Radaelli G, Veggetti A. 1995. 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.
Rowlerson A, Radaelli G, Mascarello F, Veggetti A. 1997. Regeneration of skeletal muscle in two teleost fish: Sparus
aurata and Brachydanio rerio. Cell Tissue Res 289: 311–322.
Scapolo P, Veggetti A, Rowlerson A, Mascarello F, Carpené E.
1984. Do the small new fibres of grey mullet white muscle
arise by fibre splitting? J Muscle Res Cell Motil 5:214.
Schultz E. 1989. Satellite cell behavior during skeletal muscle
growth and regeneration. Med Sci Sports Exerc 21:81–187.
Stickland N. 1983. Growth and development of muscle fibres
in the rainbow trout (Salmo gairdneri). J Anat 137:323–333.
Thomas J. 1968. Management of the white seabass in California waters. CA Dept. of Fish and Game. Fish Bulletin
142:1–35.
Veggetti A, Mascarello F, Scapolo P, Rowlerson A. 1990. Hyperplastic and hypertrophic growth of lateral muscle in
Dicentrarchus labrax (L): an ultrastructural and morphometric study. Anat Embryol 182:1–10.
Weatherley A. 1990. Approaches to understanding fish growth.
Trans Am Fish Soc 119:662–672.
Weatherley A, Gill H. 1981. Characteristics of mosaic muscle
growth in rainbow trout Salmo gairdneri. Experientia
37:102–1103.
308
A.M. ZIMMERMAN AND M.S. LOWERY
Weatherley A, Gill H. 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.
Weatherley A, Gill H. 1985. Dynamics of increase in muscle
fibers in fishes in relation to size and growth. Experientia
41:353–354.
Weatherley A, Gill H. 1987. Biology of fish growth. San Diego, CA: Academic Press.
Weatherley A, Gill H. 1989. The role of muscle in determining growth and size in teleost fish. Experientia 45:875–878.
Weatherley A, Gill H, Rogers S. 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 57:2385–2392.
Weatherley A, Gill H, Rogers S. 1980a. Growth dynamics of
mosaic muscle fibres in fingerling rainbow trout (Salmo
gairdneri) in relation to somatic growth rate. Can J Zool
58:1535–1541.
Weatherley A, Gill H, Rogers S. 1980b. The relationship between mosaic muscle fibres and size in rainbow trout (Salmo
gairdneri). J Fish Biol 17:603–610.
Weatherley A, Gill H, Lobo A. 1988. Recruitment and maximal diameter of axial muscle fibres in teleosts and their
relationship to somatic growth and ultimate size. J Fish
Biol 33:851–859.
White T, Esser K. 1989. Satellite cell and growth factor involvement in skeletal muscle growth. Med Sci Sports Exerc
21:158–164,
Willemse J, Van den Berg P. 1978. Growth of striated muscle
fibres in the m. lateralis of the European eel Anguilla
anguilla (L.) (Pisces, Teleostei). J Anat 125:447–460.
Документ
Категория
Без категории
Просмотров
2
Размер файла
365 Кб
Теги
573
1/--страниц
Пожаловаться на содержимое документа