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The Relationship Between Muscle Growth and the Growth of Different Fiber Types in the Chicken
PHYSIOLOGY AND REPRODUCTION The Relationship Between Muscle Growth and the Growth of Different Fiber Types in the Chicken Y. ONO, H. IWAMOTO, and H. TAKAHARA Laboratory of Functional Anatomy of Domestic Animals, Faculty of Agriculture, Kyushu University 46-06, Fukuoka 812, Japan
1993 Poultry Science 72:568-576
be effective in estimating the degree of participation of these two factors in musIt is well known that in the chicken, cle growth, and indicated that the degree characteristics of the growth and time course for full growth of each muscle are of participation was different among musunique (Iwamoto and Takahara, 1971; cles (or body parts) during early postnatal Iwamoto et al, 1975; Ono et al, 1982). development (Ono et al, 1989). Skeletal muscle fibers are generally Postnatal growth of skeletal muscle is accompanied by growth of individual classified into three types based on the muscle fibers, because the number of activities of myosin adenosine triphosphamuscle fibers does not increase after tase and oxidative enzymes by the hatching (Smith, 1963; Mizuno and histochemical methods of Ashmore and Hikami, 1971). Growth of muscle fibers is Doerr (1971), Peter et al (1972), Khan considered to be controlled by two factors: (1976), and Suzuki et al (1982). These fiber 1) enlargement by an increase diameter, types also have different physiological mainly due to the accumulation of my- properties, such as contraction speed and ofibrils; and 2) elongation due to the energy metabolism (Burke et al, 1971, addition of newly formed sarcomere to the 1973, 1974). The composition of these fiber ends (Williams and Goldspink, 1978). The types differs among muscles and reflects relative growth coefficient was shown to muscle function (Gunn, 1973, 1978). Studies on the relationship between muscle growth and the growth of different fiber types were reported by Davies (1972) Received for publication May 5, 1992. and Swatland (1983). Davies (1972) stated Accepted for publication November 4, 1992. INTRODUCTION
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ABSTRACT A relationship of muscle growth to fiber growth was investigated histochemically and allometrically in the chicken from 1 to 35 wk of age. Muscle fibers were classified into three types (I, IIA, and IIB) based on the reactivities for myosin adenosine triphosphatase and reduced nicotinamide adenine dinucleotide dehydrogenase. Fiber type composition widely varied in the four muscles examined in this study. Longus colli dorsalis contained all three types. The Pectoralis was composed only of IIB fibers. The caudal portion of Femorotibialis medius was made up of Type I and IIA fibers. The caudal Iliotibialis lateralis and the cranial portion of Femorotibialis medius were composed of two types, IIA and IIB. These latter two muscles showed a progressive increase of Type IIA fibers and decrease of Type IIB fibers with advancing age. Two processes controlling muscle growth were elongation and enlargement of muscle fibers. The elongation of muscle fibers stops by 15 wk of age, coincident with the cessation of bone growth. However, the enlargement of muscle fibers, the increase in diameter of muscle fibers, continued until 35 wk of age. The rate of enlargement of muscle fibers varied by muscle and fiber type. In general, greatest growth occurred in Type IIB fibers of hindlirnb muscles. (Key words: chickens, muscle type, muscle growth, fiber type, allometry)
CHICKEN MUSCLE GROWTH AND MUSCLE FIBER GROWTH
569
that Type I fibers rapidly grew in Longissimus muscle of pigs, whereas Swatland (1983) stated that Type IIA and IIB fibers showed a rapid growth in Biceps femoris muscle in growing pigs. It was reported that fiber size and fiber type composition differed between meat-type and egg-type chickens (Aberle et ah, 1979). These results suggest that fiber growth would also differ among different muscles or different fiber types. The present study was designed to investigate the relationships between muscle growth and growth of different fiber types from 1 to 35 wk of age, using four muscles different in location and function.
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fibers were divided into three types according to the classification system of Suzuki et ah (1982), I, IIA, and IIB. These correspond to slow-twitch-oxidative, fasttwitch-oxidative-glycolytic, and fasttwitch-glycolytic fibers, respectively, of Peter et ah (1972). The percentage distribution of fiber types was calculated from the number of each fiber type counted on the photographs, and fiber size was measured at the minimum internal diameter passing through the central axis of the fiber, to avoid possible artificial errors due to oblique sections. Percentage distribution and diameter of each fiber type were subjected to variance analysis and compared using Duncan's multiple range test (Duncan, 1955). MATERIALS AND METHODS In order to estimate the correlations A total of 29 male New Hampshire between muscle growth and muscle fiber chickens were studied (3 to 4 birds per growth, allometric growth coefficients of treatment group) at various ages from 1 to muscle fiber diameter against muscle 35 wk. The birds were killed by exsangui- weight were calculated after natural nation from the cervical arteries under logarithmic transformation in the followdeep anesthesia with sodium pentobarbi- ing three different periods: 1) a whole tone, skinned, and immersed in cold water period from 1 to 35 wk; 2) an earlier halfwith ice. Within 30 min, skeletal muscles period from 1 to 15 wk; 3) and a later halfwere dissected, tendons and adipose tis- period from 15 to 35 wk of age. The sue were removed, and muscles were allometry formula used in the current weighed. The four muscles studied were study was the same as previously 1) cervical muscle, Longus colli dorsalis reported (Ono et ah, 1989): In Y = b In X + (LCD); 2) shoulder girdle muscle, Pectoralis In a, where Y = muscle fiber diameter; X = (PECT); 3) lateral hindlimb muscle, caudal muscle weight; b = growth coefficient; and Iliotibialis lateralis (ITL); and 4) cranial a = constant. The examination of a sighindlimb muscle, Femorotibialis medius nificance of b and of the difference of b (FTM). The latter muscle was divided into from the value .333 was done with two parts, the cranial portion and the Student t test (Snedecor and Cochran, caudal portion (deeper portion close to the 1980). The allometric growth equation between muscle weight and fiber diameter femur). Specimens for histochemical analnot only can estimate the relationships ysis were taken from the central part of between fiber enlargement and increase in the four muscles. Muscle tissues were muscle weight, but also can indirectly rapidly frozen in isopentane solution estimate the relationships between elongacooled with dry ice. Serial cross-sections of tion of muscle fiber and increase in muscle the four muscles, 8 pm thick, were ob- weight. In the expression In Y = b In X + tained and stained for myosin adenosine In a, where Y is fiber diameter and X is triphosphatase (ATPase) (Padykula and muscle weight, In Y corresponds .333 In X, Herman, 1955) after acid (pH 4.3) or because Y corresponds ^/X dimensionally. alkaline (pH 10.5) preincubation (Brooke On the basis of this consideration, when and Kaiser, 1970a,b; Suzuki, 1977), and for diameter and length of muscle fiber grow reduced nicotinamide adenine dinucleo- to an equal degree, relative growth coeffitide dehydrogenase (NADH-DH) (Bur- cient (b) must become .333. If fiber distone, 1962) activities. ameter increases at a higher degree than Regional microscopic photographs were the length, the relative growth coefficient taken of the same muscle regions on serial must result in larger than .333, and vice sections with different staining. Muscle
570
ONO ET AL. TABLE 1. Changes of body weight and muscle weight1
Age (wk) 1 2 5 10 15 20 26 29 35
n
Body weight
4 4 3 3 3 3 3 3 3
82 147 470 1,107 1,753 2,427 2,847 3,127 3,460
Muscle weight2 LCD
PECT
ITL
FTM
ft-)
± ± ± ± ± ± ± ± ±
1 10 27 55 74 50 81 75 40
.16 .32 .96 2.46 3.89 6.06 6.79 8.65 10.0
± ± ± ± ± ± ± ± ±
.01 .04 .08 .10 .20 .45 .37 .76 .7
1.78 4.48 14.3 34.1 62.6 95.6 126 131 165
(SI ± .14 ± .32 ± 1.5 ± 4.1 ± 5.5 ± 4.3 ± 13 ± 15 ± 7
.32 ± .73 ± 2.58 ± 6.99 ± 11.9 ± 18.6 ± 27.6 ± 29.2 ± 39.4 ±
.01 .03 .23 .38 .8 .5 2.1 6.7 3.6
.20 .42 1.84 5.79 9.85 13.2 15.1 17.4 21.4
± ± ± ± ± ± ± ± ±
.01 .02 .14 .63 .75 1.0 1.7 2.3 2.4
1
Values represent the 5c ± SD. LCD = Longus colli dorsalis; PECT Pectoralis; ITL = Iliotibialis lateralis; FTM = Femorotibialis medius.
2
RESULTS Body Weight and Muscle Weight
Body weight and muscle weight are shown in Table 1. The four muscles measured in this study displayed extensively different growth rates. The greatest relative increase of muscle weight during the experimental period was for ITL (123 times), followed by FTM (107 times), PECT (93 times), and LCD (63 times). These values were much larger than that of body weight (42 times) and indicated that the growth of hindlimb muscles was larger than those of the other parts. Fiber Type Distribution
Percentage distribution of each fiber type is shown in Table 2. Although transitional fibers from fast Type II to slow Type I were observed in LCD and caudal FTM during the early developmental stages, these were classified as Type I fibers in the current study. A wide difference in fiber type composition was observed among different muscles. All three types were usually presented in LCD (Figure 1), and the percentage distribution of each type was virtually unchanged through the duration of the study (1 to 35 wk).
The PECT contained only Type IIB fibers throughout the experimental period (Figure 2). The ITL was composed of Type IIA and IIBfibers(Figure 3). The percentage of Type IIB fibers was about four times higher than Type IIA fibers at 1 wk of age. As chickens got older, the number of Type IIA fibers increased, replacing Type IIB fibers. The percentage of both fiber types was not different at 35 wk of age. The two parts of the FTM differed in fiber type composition. The cranial FTM was made up of Type IIA and IIB fibers, whereas the caudal FTM was provided with Type I and IIA fibers (Figure 4). The cranial FTM showed a similar change in the proportional distribution as ITL, indicating a progressive increase of Type IIA and decrease of Type IIB fibers with advancing age. The caudal FTM displayed about a 17% increase in Type I fibers and decrease in Type IIA fibers from 1 to 2 wk of age. After this, no further change was observed in the proportional distribution. These results indicated that LCD and the caudal FTM were red muscles, whereas PECT, ITL, and the cranial FTM were white muscles. Fiber Diameter
The diameter of each fiber type is presented in Table 3. At 1 wk of age, the largest diameter was observed in Type IIA fibers of the caudal FTM, followed by Type I fibers of LCD. These two were significantly larger than the others. The smallest diameter was observed in Type IIB fibers of
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versa. After performing the statistical analysis described above, probability values of P < .05 were considered significant.
571
CHICKEN MUSCLE GROWTH AND MUSCLE FIBER GROWTH
TABLE 2. Changes of the mean percentage distribution of each fiber type of four muscles1 LCD Age
n
I
IIA
ITL
PECT IIB
IIB
IIA
Caudal FTM
IIA
IIB
I
IIA
SEM
20.4b*y 25.A x y 36.0 b ' wx 30.7b." 33.9b-x 37.6b-wx 41.1 b ' w 31.1 b ' x 43.5" 2.01
79.6a-w 74.3a
37.71V 55.1" 58.8a-w 58.9 a ." 61.3a-w 59.2a-w 58.5 a -" 58.4 a -" 58.2" 2.02
62.3 a ' w 44.9X 41.2b-x 41.l b ." 3%.7°* 40.8b-x 41.5b-x 41.6b-x 41.8X 2.02
4.40 3.72 4.12 4.37 4.09 3.95 3.79 3.95 3.96
l°'n)
(wk) 1 2 5 10 15 20 26 29 35 SEM
IIB
Cranial FTM
4 4 3 3 3 3 3 3 3
21. l c 23.3 b ' w 22.0b 18.6b'x 21.2b 20.7b 21.3 b 23.4b-w 20.6b .51
43.9a 46.6a 38.3" 39.9a 39.6a 40.5a 44.4a 48.1 a 42.0a 1.02
35.0b 39.7a 39.7" 41.5 a ' w 39.1 a 38.9a 34.4a 28.5b-x 36.2 ab 1.38
100 100 100 100 100 100 100 100 100 0
21.5 b ' z 34.3b'yz 36.6b'xy 35.9b-xy 39.ib-xy 39.ib-xy 49.6W* 53.9a'w 53.9W 2.29
78.6 a ' w 65.7 a ' wx 63.4a'xy 64.1a-xy 60.9a-xy 60.9a'xy 50.4xy 46.1 b ^ 46.1 z 2.29
a_c
Means in rows within muscles with no common superscripts differ significantly (P < .05). Means in columns with no common superscripts differ significantly (P < .05). !LCD = Longus colli dorsalis; PECT = Pectoralis; ITL = Iliotibialis lateralis; FTM = Femorotibialis tnedius.
w_2
respective muscles at 35 wk of age. Because of higher growth rate of Type IIB fibers than those of the other types, the largest diameter was observed in Type IIB fibers of the cranial FTM, followed by Type IIB fibers of ITL at 35 wk of age. The smallest was shown in Type IIA fibers of LCD. It was generally observed that the diameter of red fibers (Type I or IIA) of red muscles was large at 1 wk of age, whereas at 35 wk of age, white fibers (IIB) of white muscles had large diameter. These results indicate that each fiber shows its own growth course and that the growth of Type IIB fibers was intimately related to high growth rate of hindlimb muscles.
FIGURE 1. Serial sections of Longus colli dorsalis at 35 wk of age. Reduced nicotinamide adenine dinucleotide dehydrogenase activity (a), myosin adenosine triphosphatase activity after acid preincubation (b), and after alkaline preincubation (c). Based on these three activities, three fiber types were classified in this muscle: A) Type I; B) Type IIA; and C) Type IIB. The calibration bar represents 100 jim.
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ITL. The relative increase of fiber diameter calculated during the period from 1 to 35 wk showed a marked difference in the rate of muscle fiber growth after 1 wk of age among muscles and fiber types, particularly large in Type IIB fibers of ITL (7.6 times) and cranial FTM (7.4). The reminders were in the range of 4.4 to 6.6 times. The growth pattern of Type I fibers differed between LCD and caudal FTM after 15 wk of age, which resulted in larger Type I fibers of caudal FTM than those of LCD at 29 wk of age. Type IIA fibers observed in LCD, ITL, and both parts of FTM grew at different rates, and consequently, Type IIA fibers of LCD were smaller than those of the other
572
ONO ET AL.
Interrelationships Between Muscle Weight and Fiber Diameter The relative growth coefficient and its constant of fiber diameter against muscle weight are presented in Table 4. All relative growth coefficients were significant in three periods (P < .01). During the period from 1 to 35 wk, the growth coefficients were larger than .333 in every fiber type of all muscles, with the exceptions of Type IIB fibers in PECT and Type IIA fibers in the caudal FTM, indicating the valuable contribution of fiber enlargement to muscle growth. A particularly high contribution was shown in Type IIB fibers of hindlimb white muscles. When the allometric analy-
DISCUSSION Postnatal muscle growth in the chicken differs among individual muscles. The most remarkable growth is seen in forelimb muscles from hatching to 1 wk of age (Iwamoto and Takahara, 1971; Iwamoto et al, 1975; Ono et al, 1982). Ono et al. (1989) reported that muscle fibers of forelimb muscles had smaller diameters than those of cervical or hindlimb muscles at the time of hatching. At 1 wk of age, all muscle fibers were the same size. These results indicate that cervical and hindlimb muscles achieve a higher state of growth than forelimb muscles, probably so that the former two muscles can function immedi-
FIGURE 3. Sections of Iliotibialis lateralis at 10 (a) and 35 (b) wk of age showing nicotinamide adenine dinucleotide dehydrogenase activity. This muscle is composed of Type IIA (B) and IIB (C) fibers. The number of Type IIA fibers increased with advancing age. The calibration bar represents 100 /tm.
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sis was performed on each of two periods, from 1 to 15, and from 15 to 35 wk, the relative growth coefficients were apparently larger in the latter. In the former period, the relative growth coefficients did not differ from .333, meaning that muscle growth was obtained by an almost equal degree of the enlargement and elongation of muscle fibers. During the latter period, it became clear that muscle growth was mostly supported by the enlargement of muscle fibers, with the exceptions of Type I fibers of LCD and caudal FTM. Relative FIGURE 2. Section of Pertoralis at 35 wk of age growth coefficients in this period also showing reduced nicotinamide adenine dinucleotide indicated that fiber enlargement was most dehydrogenase activity. This muscle was composed of prominent in Type IIA fibers in every only white (IIB) fibers. The calibration bar represents muscle that contained that fiber type. 100 (jm.
573
CHICKEN MUSCLE GROWTH AND MUSCLE FIBER GROWTH
1 to 2 wk of age appeared to result from the transformation between these two types, as stated by Suzuki and Cassens (1980). The PECT, ITL, and cranial FTM are white muscles with only or predominantly Type IIB fibers. Suzuki (1978) reported that the chicken PECT contained some Type IIA fibers in addition to predominant Type IIB fibers based on NADH-DH reactivity, except for the deepest region where three fiber types were recognized. In the current study, however, any fibers with high NADH-DH reactivity equivalent for typical IIA fibers were not seen (Figure 4). George and Berger (1966) reported that PECT in wild birds was exclusively composed of red fibers. Therefore, loss of flight may be related to the fact that chicken PECT is composed of only white fibers (Type IIB).
B
©
o FIGURE 4. Serial sections of cranial (a and b) and caudal (c and d) Femorotibialis medius at 35 wk of age. Reduced nicotinamide adenine dinucleotide dehydrogenase (a and c), and acid (pH 4.3) preincubated myosin adenosine triphosphatase (b and d) activities. The former was composed of red Type IIA (B) and white Type IIB (C) fibers, whereas the latter was made up of only red Type I (A) and IIA (B) fibers. The calibration bar represents 100 am.
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ately after hatching (e.g., moving or feeding). Forelimb muscles do not need to function quite so well at the time of hatching. The remarkable growth of forelimb muscles during the 1st wk is considered to compensate for the delay of growth at the time of hatching (Ono et ah, 1989). Therefore, it seems reasonable to place 1 wk of age as the baseline of muscle growth. Based on this concept, the high rate of hindlimb muscle growth, as shown in the current study, would be significant for chicken muscle (meat) production. According to the fiber type composition, the muscles used in this study can be divided into two groups: red muscle and white muscle. The LCD and caudal FTM are red muscles in which red fibers (Type I and IIA) predominate or are the only fibers. The change in the distribution of Type I and IIA fibers in caudal FTM from
b74
ONO ET AL. TABLE 3. Changes of the mean diameter of
PECT
Age
n
I
(wk) 1 2 5 10 15 20 26 29 35 SEM
4 4 3 3 3 3 3 3 3
12.6a<" 10.&X&K lo.^d-y 16.7abc,wi2.6d,w 12.4dA 26.9ab-v 20.9C-V 2i.4c,w 37.8 a ' u 30.1 b - u 29.4b,v 41.5»'t 28.7 b ." 29.ib,v 56.3».s 40.6«*,t 39.7d,u 53.5bcd,s43.le,t 44.0 e '' 54,7cd^ 47.6
IIB
IIB
Caudal FTM
Cranial FTM
ITL HA
HA
IIB
IIB
I
IIA
10.9b.x 16.0bc-w 27.8a
13.1^ 18.6a5bcd/s 58.3 bc ' s 62.2 bc ' s 3.34
Pooled SEM
, ^
(IttOl)
10.1bcd,z 17.7ab,y 23.2bc,x 30.2 b ' w 38.3 ab ' v 47.1b,uv 51.9cd,tu SS^-' 62.1^ 3.31
9.4cd-y 9.3d-y d
11.8
14.2^A
20.7C-X 29.5b-w 31.5b-w 40.3 d ' v 48.0de-u 53.3«i.' 61.8cd,s 3.32
25.6ab-w 38.7a-v 40.1*
9.5cd-y io.3 bcd 'y 12.6d-x 15.2 b ^ 20.6C-W 26.2ab-w 29.2b,v 4i.4a,v 36.8 b ' u 45.7a-" 46.5b<* 60.1a<* 52.6 bcd ' t 67.8as<' 57.4^ es.^* 62.9abc-s 76.03*8 3.63 4.45
.23 .43 .64 .96 1.66 1.39 1.48 1.35 1.56
a_e
Means in rows with no common superscripts differ significantly (P < .05). Means in columns with no common superscripts differ significantly (P < .05). *LCD = Longus colli dorsalis; PECT = Pectoralis; ITL = Iliotibialis lateralis; FTM = Femorotibialis medius. s_z
obviously larger than red muscle fibers at 35 wk of age. In particular, the enlargement of Type IIB fibers in ITL and cranial FTM was remarkable. It is suggested that this high growth rate of Type IIB fibers was responsible for the high growth rate of these two muscles. Aberle et al. (1979) and Iwamoto et al. (1984) pointed out that broiler chickens with excellent capability of muscle deposition have more numerous and larger Type IIB fibers than layer or crossbred chickens. On the other hand, Ashmore et al. (1972) described that the transformation of small Type IIA to large Type IIB fibers was promoted by selection
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The ITL and cranial FTM are composed of Type IIA and IIB fibers in which Type IIB fibers predominate. These two muscles showed a marked similarity in the pattern of the increase of Type IIA fibers with advancing age. This result indicates that the activity of oxidative enzymes located in mitochondria is elevated with growth. Enlargement as well as elongation of muscle fibers is important for muscle growth. In general, fiber diameter of red muscles was larger than that of white muscles at 1 wk of age. However, white muscle fibers increased in diameter more rapidly after 1 wk of age, and they became
TABLE 4. Relative growth coefficients of muscle1 fiber diameters to the muscle weight after natural logarithmic transformation in the three different periods LCD Period
I
HA
PECT
IIB
1 to 35 wk Growth coefficient .372* .380* .380* Constant 3.252 3.014 3.015 1 to 15 wk Growth coefficient .385 .349 .349 Constant 3.256 2.992 2.992 IE u
i.~ lyj
ITL
Cauc lal FTM
Cranial FTM
.370 2.173
.381* .403** 2.632 2.767
.392* .411** 2.838 3.022
.389** .314 3.061 3.128
.349 2.210
.355 2.637
.338 2.813
.382 3.008
.392 3.063
.295 3.119
.481* 1.652
.565** .485** 2.051 2.492
.706** .628 2.014 2.434
.287 3.349
.446* 2.777
.418 2.768
IIB
HA
IIA
IIB
IIA
I
IIB
-3C . . . 1 . ULJ rv r*
Growth coefficient .295 Constant 3.389
.604* .598* 2.572 2.585
!LCD = Longus colli dorsalis; PECT = Pectoralis; ITLIliotibialis lateralis; FTM = Femorotibialis medius. 'Significantly different from .333 (P < .05). '•Significantly different from .333 (P < .01).
CHICKEN MUSCLE GROWTH AND MUSCLE FIBER GROWTH
In conclusion, it is clear from the present data that muscle fiber growth differs among muscles, fiber types, and developmental stages. It is suggested that Type IIB fibers play an important role in further increasing muscle deposition, as
reflected by the remarkable growth in this fiber type in muscles with a high growth rate. REFERENCES Aberle, F. D., P. B. Addis, and R. N. Soffner, 1979. Fiber types in skeletal muscles of broiler- and layer type chickens. Poultry Sci. 58:1210-1212. Ashmore, C. R., and L. Doerr, 1971. Postnatal development of fiber types in normal and dystrophic skeletal muscle of the chick. Exp. Neurol. 30:431-446. Ashmore, C. R., G. Tompkins, and L. Doerr, 1972. Postnatal development of muscle fiber types in domestic animals. J. Anim. Sci. 34:37-41. Brooke, M. H., and K. K. Kaiser, 1970a. Three 'myosin adenosine triphosphatase' systems: the nature of their pH lability and sulfhydryl dependence. J. Histochem. Cytochem. 18: 670-672. Brooke, M. H., and K. K. Kaiser, 1970b. Muscle fibre types: how many and what kind? Arch. Neurol. 23:369-379. Burke, R. E., D. N. Levine, M. Salcman, and P. Tsairis, 1974. Motor units in cat soleus muscle: physiological, histochemical and morphological characteristics. J. Physiol. 238:503-514. Burke, R. E., D. N. Levine, P. Tsairis, and F. E. Zajac, 1973. Physiological types and histochemical profiles in motor units of the cat gastrocnemius. J. Physiol. 234:723-748. Burke, R. E., D. N. Levine, F. E. Zajac, P. Tsairis, and W. K. Eegel, 1971. Histochemical profiles of three physiologically defined types of motor units in cat gastrocnemius muscle. Science 174: 709-712. Burstone, M. S., 1962. Enzyme Histochemistry. Academic Press, London, England. Davies, A. S., 1972. Postnatal changes in the histochemical fibre types of porcine skeletal muscle. J. Anat. 113:213-240. Duncan, D. B., 1955. Multiple range and multiple F tests. Biometrics 11:1-42. George, J. G., and A. J. Berger, 1966. Avian Myology. Academic Press, New York, NY. Gunn, H. M., 1973. Histochemical differences in the skeletal muscles of different breeds of horses and dogs. J. Anat. 114:303.(Abstr.) Gunn, H. M., 1978. Differences in the histochemical properties of skeletal muscles of different breeds of horses and dogs. J. Anat. 127:615-634. Iwamoto, H., S. Morita, Y. Ono, H. Takahara, H. Higashiuwatoko, T. Kukimoto, and S. Gotoh, 1984. A study on the fiber composition of breast and thigh muscles in satumadori crossbred broilers. Jpn. J. Zootech. Sci. 55:87-94. Iwamoto, H., and H. Takahara, 1971. Fundamental studies on the meat production of the domestic fowl. V. Comparison of postnatal growth of individual muscle and its sexual differences. Sci. Bull. Fac. Agric. Kyushu Univ. 25:191-199. Iwamoto, H., H. Takahara, and M. Okamoto, 1975. Fundamental studies on the meat production of the domestic fowl. VII. Postnatal growth of skeletal muscle in some body parts of barred
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for increased meat yield in domestic mammals, with the consequent increase in number and size of Type IIB fibers. These reports and the results of the present experiment suggest that Type IIB fibers would play an important role in the further increase of muscle production. This suggestion is also supported by the relative growth coefficients from 1 to 35 wk in the current study, in which Type IIB fibers of hindlimb muscles with high growth rate showed the largest values. Muscle fiber length seems to have an intimate correlation with bone length. Increase in fiber length ceases by 15 wk of age when bone growth is completed in chickens (Iwamoto and Takahara, 1971; Iwamoto et al, 1975). It is hypothesized that the relationship of muscle growth and muscle fiber growth would be different before and after 15 wk of age. Growth coefficients obtained from these two periods indicated that muscle fiber growth was attained by both enlargement and elongation up to 15 wk; however after this stage, enlargement became the main factor. Growth coefficients of Type I fibers were smaller in the latter period than in the former period, suggesting that Type I fibers matured earlier. On the other hand, Type IIA and IIB fibers matured later; particularly the enlargement of Type IIA fibers, which was remarkable in every muscle. Sexual maturation in the chicken begins around 20 wk of age (Ono et al, 1979), the latter period is coincident with this period. In this period, it is observed that a remarkable growth of hindlimb muscle occurs in the intact cock, but not in the castrated cock (Ono et al, 1982). At the same time, a marked development of Type IIA fibers and fiber type transformation from Type IIB to Type IIA fibers occur in the cock during sexual maturation, resulting in remarkable growth of hindlimb muscles (Ono et al, 1983). In the current study, the marked enlargement of Type IIA fibers was also observed during the later period (15 to 35 wk).
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ONO ET AL. histochemical techniques. J. Histochem. Cytochem. 3:161-169. Peter, J. B., R. J. Barnard, V. R. Edgerton, C. A. Gillespie, and K. E. Stempel, 1972. Metabolic profiles of three fiber types of skeletal muscle in guinea pigs and rabbits. Biochemistry 11: 2627-2633. Smith, J. H., 1963. Relation of body size to muscle cell size and number in the chicken. Poultry Sci. 42: 283-290. Snedecor, G., and W. G. Cochran, 1980. Statistical Methods. The Iowa University Press, Ames, LA. Suzuki, A., 1977. A comparative histochemical study of the masseter muscle of the cattle, sheep, swine, dog, guinea pig and rat. Histochemistry 51:121-131. Suzuki, A., 1978. Histochemistry of the chicken skeletal muscles. II. Distribution and diameter of three fiber types. Tohoku J. Agric. Res. 29:38-43. Suzuki, A., and R. G. Cassens, 1980. A histochemical study of myofiber types in muscle of the growing pig. J. Anim. Sci. 51:1449-1461. Suzuki, A., T. Tsuchiya, and H. Tamate, 1982. Histochemical properties of myofiber types in thigh muscles of the chicken. Acta Histochem. Cytochem. 15:362-371. Swatland, H. J., 1983. Aerobic activity in the axis of growing myofibers in the porcine biceps femoris. J. Anim. Sci. 56:1324-1328. Williams, P., and G. Goldspink, 1978. Changes in sarcomere length and physiological properties in immobilized muscle. J. Anat. 127:459-468.
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plymouth rock chicken. Sci. Bull. Fac. Agric. Kyushu Univ. 30:119-136. Khan, M. A., 1976. Histochemical characteristics of vertebrate striated muscle: A review. Prog. Histochem. Cytochem. 8(4):l-48. Mizuno, T., and Y. Hikami, 1971. Comparison of muscle growth between meat-type and egg-type chickens. Jpn. J. Zootech. Sci. 42:526-532. Ono, Y., H. Iwamoto, and H. Takahara, 1982. Studies on the growth of skeletal muscle of capon, n. Effects of castration on muscle weights in different body parts and individual muscle weights. Sci. Bull. Fac. Agric. Kyushu Univ. 37: 23-30. Ono, Y., H. Iwamoto, and H. Takahara, 1983. Histochemical studies on the effects of androgen on the fiber composition of M. biceps femoris in cocks. Jpn. J. Zootech. Sci. 54:453-459. Ono, Y., H. Iwamoto, and H. Takahara, 1989. Allometry of body weight, skeletal muscle weight and muscle fiber diameter in the chick. Jpn. J. Zootech. Sci. 60:958-964. Ono, Y., H. Iwamoto, H. Takahara, and M. Okamoto, 1979. Studies on the growth of skeletal muscle of capon. I. Effect of castration on the weights of skeletal muscle, abdominal fat, intermuscular fat, skin, bone and viscera. Sci. Bull. Fac. Agric. Kyushu Univ. 34:39-46. Padykula, H. A., and E. Herman, 1955. Factors affecting the activity of adenosine triphosphatase and other phosphatases as measured by
1993 Poultry Science 72:568-576
be effective in estimating the degree of participation of these two factors in musIt is well known that in the chicken, cle growth, and indicated that the degree characteristics of the growth and time course for full growth of each muscle are of participation was different among musunique (Iwamoto and Takahara, 1971; cles (or body parts) during early postnatal Iwamoto et al, 1975; Ono et al, 1982). development (Ono et al, 1989). Skeletal muscle fibers are generally Postnatal growth of skeletal muscle is accompanied by growth of individual classified into three types based on the muscle fibers, because the number of activities of myosin adenosine triphosphamuscle fibers does not increase after tase and oxidative enzymes by the hatching (Smith, 1963; Mizuno and histochemical methods of Ashmore and Hikami, 1971). Growth of muscle fibers is Doerr (1971), Peter et al (1972), Khan considered to be controlled by two factors: (1976), and Suzuki et al (1982). These fiber 1) enlargement by an increase diameter, types also have different physiological mainly due to the accumulation of my- properties, such as contraction speed and ofibrils; and 2) elongation due to the energy metabolism (Burke et al, 1971, addition of newly formed sarcomere to the 1973, 1974). The composition of these fiber ends (Williams and Goldspink, 1978). The types differs among muscles and reflects relative growth coefficient was shown to muscle function (Gunn, 1973, 1978). Studies on the relationship between muscle growth and the growth of different fiber types were reported by Davies (1972) Received for publication May 5, 1992. and Swatland (1983). Davies (1972) stated Accepted for publication November 4, 1992. INTRODUCTION
568
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ABSTRACT A relationship of muscle growth to fiber growth was investigated histochemically and allometrically in the chicken from 1 to 35 wk of age. Muscle fibers were classified into three types (I, IIA, and IIB) based on the reactivities for myosin adenosine triphosphatase and reduced nicotinamide adenine dinucleotide dehydrogenase. Fiber type composition widely varied in the four muscles examined in this study. Longus colli dorsalis contained all three types. The Pectoralis was composed only of IIB fibers. The caudal portion of Femorotibialis medius was made up of Type I and IIA fibers. The caudal Iliotibialis lateralis and the cranial portion of Femorotibialis medius were composed of two types, IIA and IIB. These latter two muscles showed a progressive increase of Type IIA fibers and decrease of Type IIB fibers with advancing age. Two processes controlling muscle growth were elongation and enlargement of muscle fibers. The elongation of muscle fibers stops by 15 wk of age, coincident with the cessation of bone growth. However, the enlargement of muscle fibers, the increase in diameter of muscle fibers, continued until 35 wk of age. The rate of enlargement of muscle fibers varied by muscle and fiber type. In general, greatest growth occurred in Type IIB fibers of hindlirnb muscles. (Key words: chickens, muscle type, muscle growth, fiber type, allometry)
CHICKEN MUSCLE GROWTH AND MUSCLE FIBER GROWTH
569
that Type I fibers rapidly grew in Longissimus muscle of pigs, whereas Swatland (1983) stated that Type IIA and IIB fibers showed a rapid growth in Biceps femoris muscle in growing pigs. It was reported that fiber size and fiber type composition differed between meat-type and egg-type chickens (Aberle et ah, 1979). These results suggest that fiber growth would also differ among different muscles or different fiber types. The present study was designed to investigate the relationships between muscle growth and growth of different fiber types from 1 to 35 wk of age, using four muscles different in location and function.
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fibers were divided into three types according to the classification system of Suzuki et ah (1982), I, IIA, and IIB. These correspond to slow-twitch-oxidative, fasttwitch-oxidative-glycolytic, and fasttwitch-glycolytic fibers, respectively, of Peter et ah (1972). The percentage distribution of fiber types was calculated from the number of each fiber type counted on the photographs, and fiber size was measured at the minimum internal diameter passing through the central axis of the fiber, to avoid possible artificial errors due to oblique sections. Percentage distribution and diameter of each fiber type were subjected to variance analysis and compared using Duncan's multiple range test (Duncan, 1955). MATERIALS AND METHODS In order to estimate the correlations A total of 29 male New Hampshire between muscle growth and muscle fiber chickens were studied (3 to 4 birds per growth, allometric growth coefficients of treatment group) at various ages from 1 to muscle fiber diameter against muscle 35 wk. The birds were killed by exsangui- weight were calculated after natural nation from the cervical arteries under logarithmic transformation in the followdeep anesthesia with sodium pentobarbi- ing three different periods: 1) a whole tone, skinned, and immersed in cold water period from 1 to 35 wk; 2) an earlier halfwith ice. Within 30 min, skeletal muscles period from 1 to 15 wk; 3) and a later halfwere dissected, tendons and adipose tis- period from 15 to 35 wk of age. The sue were removed, and muscles were allometry formula used in the current weighed. The four muscles studied were study was the same as previously 1) cervical muscle, Longus colli dorsalis reported (Ono et ah, 1989): In Y = b In X + (LCD); 2) shoulder girdle muscle, Pectoralis In a, where Y = muscle fiber diameter; X = (PECT); 3) lateral hindlimb muscle, caudal muscle weight; b = growth coefficient; and Iliotibialis lateralis (ITL); and 4) cranial a = constant. The examination of a sighindlimb muscle, Femorotibialis medius nificance of b and of the difference of b (FTM). The latter muscle was divided into from the value .333 was done with two parts, the cranial portion and the Student t test (Snedecor and Cochran, caudal portion (deeper portion close to the 1980). The allometric growth equation between muscle weight and fiber diameter femur). Specimens for histochemical analnot only can estimate the relationships ysis were taken from the central part of between fiber enlargement and increase in the four muscles. Muscle tissues were muscle weight, but also can indirectly rapidly frozen in isopentane solution estimate the relationships between elongacooled with dry ice. Serial cross-sections of tion of muscle fiber and increase in muscle the four muscles, 8 pm thick, were ob- weight. In the expression In Y = b In X + tained and stained for myosin adenosine In a, where Y is fiber diameter and X is triphosphatase (ATPase) (Padykula and muscle weight, In Y corresponds .333 In X, Herman, 1955) after acid (pH 4.3) or because Y corresponds ^/X dimensionally. alkaline (pH 10.5) preincubation (Brooke On the basis of this consideration, when and Kaiser, 1970a,b; Suzuki, 1977), and for diameter and length of muscle fiber grow reduced nicotinamide adenine dinucleo- to an equal degree, relative growth coeffitide dehydrogenase (NADH-DH) (Bur- cient (b) must become .333. If fiber distone, 1962) activities. ameter increases at a higher degree than Regional microscopic photographs were the length, the relative growth coefficient taken of the same muscle regions on serial must result in larger than .333, and vice sections with different staining. Muscle
570
ONO ET AL. TABLE 1. Changes of body weight and muscle weight1
Age (wk) 1 2 5 10 15 20 26 29 35
n
Body weight
4 4 3 3 3 3 3 3 3
82 147 470 1,107 1,753 2,427 2,847 3,127 3,460
Muscle weight2 LCD
PECT
ITL
FTM
ft-)
± ± ± ± ± ± ± ± ±
1 10 27 55 74 50 81 75 40
.16 .32 .96 2.46 3.89 6.06 6.79 8.65 10.0
± ± ± ± ± ± ± ± ±
.01 .04 .08 .10 .20 .45 .37 .76 .7
1.78 4.48 14.3 34.1 62.6 95.6 126 131 165
(SI ± .14 ± .32 ± 1.5 ± 4.1 ± 5.5 ± 4.3 ± 13 ± 15 ± 7
.32 ± .73 ± 2.58 ± 6.99 ± 11.9 ± 18.6 ± 27.6 ± 29.2 ± 39.4 ±
.01 .03 .23 .38 .8 .5 2.1 6.7 3.6
.20 .42 1.84 5.79 9.85 13.2 15.1 17.4 21.4
± ± ± ± ± ± ± ± ±
.01 .02 .14 .63 .75 1.0 1.7 2.3 2.4
1
Values represent the 5c ± SD. LCD = Longus colli dorsalis; PECT Pectoralis; ITL = Iliotibialis lateralis; FTM = Femorotibialis medius.
2
RESULTS Body Weight and Muscle Weight
Body weight and muscle weight are shown in Table 1. The four muscles measured in this study displayed extensively different growth rates. The greatest relative increase of muscle weight during the experimental period was for ITL (123 times), followed by FTM (107 times), PECT (93 times), and LCD (63 times). These values were much larger than that of body weight (42 times) and indicated that the growth of hindlimb muscles was larger than those of the other parts. Fiber Type Distribution
Percentage distribution of each fiber type is shown in Table 2. Although transitional fibers from fast Type II to slow Type I were observed in LCD and caudal FTM during the early developmental stages, these were classified as Type I fibers in the current study. A wide difference in fiber type composition was observed among different muscles. All three types were usually presented in LCD (Figure 1), and the percentage distribution of each type was virtually unchanged through the duration of the study (1 to 35 wk).
The PECT contained only Type IIB fibers throughout the experimental period (Figure 2). The ITL was composed of Type IIA and IIBfibers(Figure 3). The percentage of Type IIB fibers was about four times higher than Type IIA fibers at 1 wk of age. As chickens got older, the number of Type IIA fibers increased, replacing Type IIB fibers. The percentage of both fiber types was not different at 35 wk of age. The two parts of the FTM differed in fiber type composition. The cranial FTM was made up of Type IIA and IIB fibers, whereas the caudal FTM was provided with Type I and IIA fibers (Figure 4). The cranial FTM showed a similar change in the proportional distribution as ITL, indicating a progressive increase of Type IIA and decrease of Type IIB fibers with advancing age. The caudal FTM displayed about a 17% increase in Type I fibers and decrease in Type IIA fibers from 1 to 2 wk of age. After this, no further change was observed in the proportional distribution. These results indicated that LCD and the caudal FTM were red muscles, whereas PECT, ITL, and the cranial FTM were white muscles. Fiber Diameter
The diameter of each fiber type is presented in Table 3. At 1 wk of age, the largest diameter was observed in Type IIA fibers of the caudal FTM, followed by Type I fibers of LCD. These two were significantly larger than the others. The smallest diameter was observed in Type IIB fibers of
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versa. After performing the statistical analysis described above, probability values of P < .05 were considered significant.
571
CHICKEN MUSCLE GROWTH AND MUSCLE FIBER GROWTH
TABLE 2. Changes of the mean percentage distribution of each fiber type of four muscles1 LCD Age
n
I
IIA
ITL
PECT IIB
IIB
IIA
Caudal FTM
IIA
IIB
I
IIA
SEM
20.4b*y 25.A x y 36.0 b ' wx 30.7b." 33.9b-x 37.6b-wx 41.1 b ' w 31.1 b ' x 43.5" 2.01
79.6a-w 74.3a
37.71V 55.1" 58.8a-w 58.9 a ." 61.3a-w 59.2a-w 58.5 a -" 58.4 a -" 58.2" 2.02
62.3 a ' w 44.9X 41.2b-x 41.l b ." 3%.7°* 40.8b-x 41.5b-x 41.6b-x 41.8X 2.02
4.40 3.72 4.12 4.37 4.09 3.95 3.79 3.95 3.96
l°'n)
(wk) 1 2 5 10 15 20 26 29 35 SEM
IIB
Cranial FTM
4 4 3 3 3 3 3 3 3
21. l c 23.3 b ' w 22.0b 18.6b'x 21.2b 20.7b 21.3 b 23.4b-w 20.6b .51
43.9a 46.6a 38.3" 39.9a 39.6a 40.5a 44.4a 48.1 a 42.0a 1.02
35.0b 39.7a 39.7" 41.5 a ' w 39.1 a 38.9a 34.4a 28.5b-x 36.2 ab 1.38
100 100 100 100 100 100 100 100 100 0
21.5 b ' z 34.3b'yz 36.6b'xy 35.9b-xy 39.ib-xy 39.ib-xy 49.6W* 53.9a'w 53.9W 2.29
78.6 a ' w 65.7 a ' wx 63.4a'xy 64.1a-xy 60.9a-xy 60.9a'xy 50.4xy 46.1 b ^ 46.1 z 2.29
a_c
Means in rows within muscles with no common superscripts differ significantly (P < .05). Means in columns with no common superscripts differ significantly (P < .05). !LCD = Longus colli dorsalis; PECT = Pectoralis; ITL = Iliotibialis lateralis; FTM = Femorotibialis tnedius.
w_2
respective muscles at 35 wk of age. Because of higher growth rate of Type IIB fibers than those of the other types, the largest diameter was observed in Type IIB fibers of the cranial FTM, followed by Type IIB fibers of ITL at 35 wk of age. The smallest was shown in Type IIA fibers of LCD. It was generally observed that the diameter of red fibers (Type I or IIA) of red muscles was large at 1 wk of age, whereas at 35 wk of age, white fibers (IIB) of white muscles had large diameter. These results indicate that each fiber shows its own growth course and that the growth of Type IIB fibers was intimately related to high growth rate of hindlimb muscles.
FIGURE 1. Serial sections of Longus colli dorsalis at 35 wk of age. Reduced nicotinamide adenine dinucleotide dehydrogenase activity (a), myosin adenosine triphosphatase activity after acid preincubation (b), and after alkaline preincubation (c). Based on these three activities, three fiber types were classified in this muscle: A) Type I; B) Type IIA; and C) Type IIB. The calibration bar represents 100 jim.
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ITL. The relative increase of fiber diameter calculated during the period from 1 to 35 wk showed a marked difference in the rate of muscle fiber growth after 1 wk of age among muscles and fiber types, particularly large in Type IIB fibers of ITL (7.6 times) and cranial FTM (7.4). The reminders were in the range of 4.4 to 6.6 times. The growth pattern of Type I fibers differed between LCD and caudal FTM after 15 wk of age, which resulted in larger Type I fibers of caudal FTM than those of LCD at 29 wk of age. Type IIA fibers observed in LCD, ITL, and both parts of FTM grew at different rates, and consequently, Type IIA fibers of LCD were smaller than those of the other
572
ONO ET AL.
Interrelationships Between Muscle Weight and Fiber Diameter The relative growth coefficient and its constant of fiber diameter against muscle weight are presented in Table 4. All relative growth coefficients were significant in three periods (P < .01). During the period from 1 to 35 wk, the growth coefficients were larger than .333 in every fiber type of all muscles, with the exceptions of Type IIB fibers in PECT and Type IIA fibers in the caudal FTM, indicating the valuable contribution of fiber enlargement to muscle growth. A particularly high contribution was shown in Type IIB fibers of hindlimb white muscles. When the allometric analy-
DISCUSSION Postnatal muscle growth in the chicken differs among individual muscles. The most remarkable growth is seen in forelimb muscles from hatching to 1 wk of age (Iwamoto and Takahara, 1971; Iwamoto et al, 1975; Ono et al, 1982). Ono et al. (1989) reported that muscle fibers of forelimb muscles had smaller diameters than those of cervical or hindlimb muscles at the time of hatching. At 1 wk of age, all muscle fibers were the same size. These results indicate that cervical and hindlimb muscles achieve a higher state of growth than forelimb muscles, probably so that the former two muscles can function immedi-
FIGURE 3. Sections of Iliotibialis lateralis at 10 (a) and 35 (b) wk of age showing nicotinamide adenine dinucleotide dehydrogenase activity. This muscle is composed of Type IIA (B) and IIB (C) fibers. The number of Type IIA fibers increased with advancing age. The calibration bar represents 100 /tm.
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sis was performed on each of two periods, from 1 to 15, and from 15 to 35 wk, the relative growth coefficients were apparently larger in the latter. In the former period, the relative growth coefficients did not differ from .333, meaning that muscle growth was obtained by an almost equal degree of the enlargement and elongation of muscle fibers. During the latter period, it became clear that muscle growth was mostly supported by the enlargement of muscle fibers, with the exceptions of Type I fibers of LCD and caudal FTM. Relative FIGURE 2. Section of Pertoralis at 35 wk of age growth coefficients in this period also showing reduced nicotinamide adenine dinucleotide indicated that fiber enlargement was most dehydrogenase activity. This muscle was composed of prominent in Type IIA fibers in every only white (IIB) fibers. The calibration bar represents muscle that contained that fiber type. 100 (jm.
573
CHICKEN MUSCLE GROWTH AND MUSCLE FIBER GROWTH
1 to 2 wk of age appeared to result from the transformation between these two types, as stated by Suzuki and Cassens (1980). The PECT, ITL, and cranial FTM are white muscles with only or predominantly Type IIB fibers. Suzuki (1978) reported that the chicken PECT contained some Type IIA fibers in addition to predominant Type IIB fibers based on NADH-DH reactivity, except for the deepest region where three fiber types were recognized. In the current study, however, any fibers with high NADH-DH reactivity equivalent for typical IIA fibers were not seen (Figure 4). George and Berger (1966) reported that PECT in wild birds was exclusively composed of red fibers. Therefore, loss of flight may be related to the fact that chicken PECT is composed of only white fibers (Type IIB).
B
©
o FIGURE 4. Serial sections of cranial (a and b) and caudal (c and d) Femorotibialis medius at 35 wk of age. Reduced nicotinamide adenine dinucleotide dehydrogenase (a and c), and acid (pH 4.3) preincubated myosin adenosine triphosphatase (b and d) activities. The former was composed of red Type IIA (B) and white Type IIB (C) fibers, whereas the latter was made up of only red Type I (A) and IIA (B) fibers. The calibration bar represents 100 am.
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ately after hatching (e.g., moving or feeding). Forelimb muscles do not need to function quite so well at the time of hatching. The remarkable growth of forelimb muscles during the 1st wk is considered to compensate for the delay of growth at the time of hatching (Ono et ah, 1989). Therefore, it seems reasonable to place 1 wk of age as the baseline of muscle growth. Based on this concept, the high rate of hindlimb muscle growth, as shown in the current study, would be significant for chicken muscle (meat) production. According to the fiber type composition, the muscles used in this study can be divided into two groups: red muscle and white muscle. The LCD and caudal FTM are red muscles in which red fibers (Type I and IIA) predominate or are the only fibers. The change in the distribution of Type I and IIA fibers in caudal FTM from
b74
ONO ET AL. TABLE 3. Changes of the mean diameter of
PECT
Age
n
I
(wk) 1 2 5 10 15 20 26 29 35 SEM
4 4 3 3 3 3 3 3 3
12.6a<" 10.&X&K lo.^d-y 16.7abc,wi2.6d,w 12.4dA 26.9ab-v 20.9C-V 2i.4c,w 37.8 a ' u 30.1 b - u 29.4b,v 41.5»'t 28.7 b ." 29.ib,v 56.3».s 40.6«*,t 39.7d,u 53.5bcd,s43.le,t 44.0 e '' 54,7cd^ 47.6
IIB
IIB
Caudal FTM
Cranial FTM
ITL HA
HA
IIB
IIB
I
IIA
10.9b.x 16.0bc-w 27.8a
13.1^ 18.6a
Pooled SEM
, ^
(IttOl)
10.1bcd,z 17.7ab,y 23.2bc,x 30.2 b ' w 38.3 ab ' v 47.1b,uv 51.9cd,tu SS^-' 62.1^ 3.31
9.4cd-y 9.3d-y d
11.8
14.2^A
20.7C-X 29.5b-w 31.5b-w 40.3 d ' v 48.0de-u 53.3«i.' 61.8cd,s 3.32
25.6ab-w 38.7a-v 40.1*
9.5cd-y io.3 bcd 'y 12.6d-x 15.2 b ^ 20.6C-W 26.2ab-w 29.2b,v 4i.4a,v 36.8 b ' u 45.7a-" 46.5b<* 60.1a<* 52.6 bcd ' t 67.8as<' 57.4^ es.^* 62.9abc-s 76.03*8 3.63 4.45
.23 .43 .64 .96 1.66 1.39 1.48 1.35 1.56
a_e
Means in rows with no common superscripts differ significantly (P < .05). Means in columns with no common superscripts differ significantly (P < .05). *LCD = Longus colli dorsalis; PECT = Pectoralis; ITL = Iliotibialis lateralis; FTM = Femorotibialis medius. s_z
obviously larger than red muscle fibers at 35 wk of age. In particular, the enlargement of Type IIB fibers in ITL and cranial FTM was remarkable. It is suggested that this high growth rate of Type IIB fibers was responsible for the high growth rate of these two muscles. Aberle et al. (1979) and Iwamoto et al. (1984) pointed out that broiler chickens with excellent capability of muscle deposition have more numerous and larger Type IIB fibers than layer or crossbred chickens. On the other hand, Ashmore et al. (1972) described that the transformation of small Type IIA to large Type IIB fibers was promoted by selection
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The ITL and cranial FTM are composed of Type IIA and IIB fibers in which Type IIB fibers predominate. These two muscles showed a marked similarity in the pattern of the increase of Type IIA fibers with advancing age. This result indicates that the activity of oxidative enzymes located in mitochondria is elevated with growth. Enlargement as well as elongation of muscle fibers is important for muscle growth. In general, fiber diameter of red muscles was larger than that of white muscles at 1 wk of age. However, white muscle fibers increased in diameter more rapidly after 1 wk of age, and they became
TABLE 4. Relative growth coefficients of muscle1 fiber diameters to the muscle weight after natural logarithmic transformation in the three different periods LCD Period
I
HA
PECT
IIB
1 to 35 wk Growth coefficient .372* .380* .380* Constant 3.252 3.014 3.015 1 to 15 wk Growth coefficient .385 .349 .349 Constant 3.256 2.992 2.992 IE u
i.~ lyj
ITL
Cauc lal FTM
Cranial FTM
.370 2.173
.381* .403** 2.632 2.767
.392* .411** 2.838 3.022
.389** .314 3.061 3.128
.349 2.210
.355 2.637
.338 2.813
.382 3.008
.392 3.063
.295 3.119
.481* 1.652
.565** .485** 2.051 2.492
.706** .628 2.014 2.434
.287 3.349
.446* 2.777
.418 2.768
IIB
HA
IIA
IIB
IIA
I
IIB
-3C . . . 1 . ULJ rv r*
Growth coefficient .295 Constant 3.389
.604* .598* 2.572 2.585
!LCD = Longus colli dorsalis; PECT = Pectoralis; ITLIliotibialis lateralis; FTM = Femorotibialis medius. 'Significantly different from .333 (P < .05). '•Significantly different from .333 (P < .01).
CHICKEN MUSCLE GROWTH AND MUSCLE FIBER GROWTH
In conclusion, it is clear from the present data that muscle fiber growth differs among muscles, fiber types, and developmental stages. It is suggested that Type IIB fibers play an important role in further increasing muscle deposition, as
reflected by the remarkable growth in this fiber type in muscles with a high growth rate. REFERENCES Aberle, F. D., P. B. Addis, and R. N. Soffner, 1979. Fiber types in skeletal muscles of broiler- and layer type chickens. Poultry Sci. 58:1210-1212. Ashmore, C. R., and L. Doerr, 1971. Postnatal development of fiber types in normal and dystrophic skeletal muscle of the chick. Exp. Neurol. 30:431-446. Ashmore, C. R., G. Tompkins, and L. Doerr, 1972. Postnatal development of muscle fiber types in domestic animals. J. Anim. Sci. 34:37-41. Brooke, M. H., and K. K. Kaiser, 1970a. Three 'myosin adenosine triphosphatase' systems: the nature of their pH lability and sulfhydryl dependence. J. Histochem. Cytochem. 18: 670-672. Brooke, M. H., and K. K. Kaiser, 1970b. Muscle fibre types: how many and what kind? Arch. Neurol. 23:369-379. Burke, R. E., D. N. Levine, M. Salcman, and P. Tsairis, 1974. Motor units in cat soleus muscle: physiological, histochemical and morphological characteristics. J. Physiol. 238:503-514. Burke, R. E., D. N. Levine, P. Tsairis, and F. E. Zajac, 1973. Physiological types and histochemical profiles in motor units of the cat gastrocnemius. J. Physiol. 234:723-748. Burke, R. E., D. N. Levine, F. E. Zajac, P. Tsairis, and W. K. Eegel, 1971. Histochemical profiles of three physiologically defined types of motor units in cat gastrocnemius muscle. Science 174: 709-712. Burstone, M. S., 1962. Enzyme Histochemistry. Academic Press, London, England. Davies, A. S., 1972. Postnatal changes in the histochemical fibre types of porcine skeletal muscle. J. Anat. 113:213-240. Duncan, D. B., 1955. Multiple range and multiple F tests. Biometrics 11:1-42. George, J. G., and A. J. Berger, 1966. Avian Myology. Academic Press, New York, NY. Gunn, H. M., 1973. Histochemical differences in the skeletal muscles of different breeds of horses and dogs. J. Anat. 114:303.(Abstr.) Gunn, H. M., 1978. Differences in the histochemical properties of skeletal muscles of different breeds of horses and dogs. J. Anat. 127:615-634. Iwamoto, H., S. Morita, Y. Ono, H. Takahara, H. Higashiuwatoko, T. Kukimoto, and S. Gotoh, 1984. A study on the fiber composition of breast and thigh muscles in satumadori crossbred broilers. Jpn. J. Zootech. Sci. 55:87-94. Iwamoto, H., and H. Takahara, 1971. Fundamental studies on the meat production of the domestic fowl. V. Comparison of postnatal growth of individual muscle and its sexual differences. Sci. Bull. Fac. Agric. Kyushu Univ. 25:191-199. Iwamoto, H., H. Takahara, and M. Okamoto, 1975. Fundamental studies on the meat production of the domestic fowl. VII. Postnatal growth of skeletal muscle in some body parts of barred
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for increased meat yield in domestic mammals, with the consequent increase in number and size of Type IIB fibers. These reports and the results of the present experiment suggest that Type IIB fibers would play an important role in the further increase of muscle production. This suggestion is also supported by the relative growth coefficients from 1 to 35 wk in the current study, in which Type IIB fibers of hindlimb muscles with high growth rate showed the largest values. Muscle fiber length seems to have an intimate correlation with bone length. Increase in fiber length ceases by 15 wk of age when bone growth is completed in chickens (Iwamoto and Takahara, 1971; Iwamoto et al, 1975). It is hypothesized that the relationship of muscle growth and muscle fiber growth would be different before and after 15 wk of age. Growth coefficients obtained from these two periods indicated that muscle fiber growth was attained by both enlargement and elongation up to 15 wk; however after this stage, enlargement became the main factor. Growth coefficients of Type I fibers were smaller in the latter period than in the former period, suggesting that Type I fibers matured earlier. On the other hand, Type IIA and IIB fibers matured later; particularly the enlargement of Type IIA fibers, which was remarkable in every muscle. Sexual maturation in the chicken begins around 20 wk of age (Ono et al, 1979), the latter period is coincident with this period. In this period, it is observed that a remarkable growth of hindlimb muscle occurs in the intact cock, but not in the castrated cock (Ono et al, 1982). At the same time, a marked development of Type IIA fibers and fiber type transformation from Type IIB to Type IIA fibers occur in the cock during sexual maturation, resulting in remarkable growth of hindlimb muscles (Ono et al, 1983). In the current study, the marked enlargement of Type IIA fibers was also observed during the later period (15 to 35 wk).
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plymouth rock chicken. Sci. Bull. Fac. Agric. Kyushu Univ. 30:119-136. Khan, M. A., 1976. Histochemical characteristics of vertebrate striated muscle: A review. Prog. Histochem. Cytochem. 8(4):l-48. Mizuno, T., and Y. Hikami, 1971. Comparison of muscle growth between meat-type and egg-type chickens. Jpn. J. Zootech. Sci. 42:526-532. Ono, Y., H. Iwamoto, and H. Takahara, 1982. Studies on the growth of skeletal muscle of capon, n. Effects of castration on muscle weights in different body parts and individual muscle weights. Sci. Bull. Fac. Agric. Kyushu Univ. 37: 23-30. Ono, Y., H. Iwamoto, and H. Takahara, 1983. Histochemical studies on the effects of androgen on the fiber composition of M. biceps femoris in cocks. Jpn. J. Zootech. Sci. 54:453-459. Ono, Y., H. Iwamoto, and H. Takahara, 1989. Allometry of body weight, skeletal muscle weight and muscle fiber diameter in the chick. Jpn. J. Zootech. Sci. 60:958-964. Ono, Y., H. Iwamoto, H. Takahara, and M. Okamoto, 1979. Studies on the growth of skeletal muscle of capon. I. Effect of castration on the weights of skeletal muscle, abdominal fat, intermuscular fat, skin, bone and viscera. Sci. Bull. Fac. Agric. Kyushu Univ. 34:39-46. Padykula, H. A., and E. Herman, 1955. Factors affecting the activity of adenosine triphosphatase and other phosphatases as measured by