Body weight Its relation to tissue composition segment distribution and motor function II.код для вставкиСкачать
Body Weight: Its Relation to Tissue Composition, Segment Distribution, and Motor Function 11. DEVELOPMENT OF MACACA MULATTA 1 THEODORE I GRAND Oregon Regonal Przmate Research Center, Beaverton, Oregon 97005 KEY WORDS Anatomy . Development composition Limb segments . Macaca . Musculature . Tissue ABSTRACT The relative composition of skin, muscle, and bone and their distribution patterns throughout the body are given for a series of Macaca mulatta from 141 days conceptual age through adulthood. In terms of percent of total body weight, the musculature of these animals doubles during the first postnatal year whereas bone and skin decrease. Regionally, the muscles of the thighs, back extensors, truncal-forelimb and upper arms increase most markedly. The thighs double and the upper arms increase whereas the trunk, hands, feet, and tail decrease. The biomechanical implications of these changes for motor development are discussed. Body size is a complex variable. The component tissues vary considerably among the adults of many species (Grand, '77). As a result, the notion of size is frequently oversimplified. Weight increases in domestic animals and man from birth to maturity are accompanied by proportional changes in tissues and segments and by a major shift in motor repertoire. In order to examine these phenomena, I applied a method of dissection similar to that used for interspecific comparisons to a series of Macaca mulatta. The baseline for adult Macaca has been established from data in the preceding paper and specimens of this species were available throughout all stages of the life cycle. The same questions could be raised as in the study of adults: differences in tissue composition, limb segment weight, tissue composition of the segments and motor pattern differences of fetus and adult. Not surprisingly, this approach reconsiders many data on body composition gathered by physiologists (Keys and Brozek, '53; Beatty e t al., '67; Young, '701, veterinary anatomists (Palsson, '55; Fowler, '68; Butterfield and Berg, '66; Butterfield and Johnson, '68), human anatomists (Wilmer, '40), and other physical anthropologists (Brozek, '55, '61, '63; Brozek and Keys, '50; Parizkova, '68; Trotter AM. J. PHYS. ANTHROP., 47: 241-248. and Hixon, '74; Trotter et al., '75). The study has blindspots because of its functionallocomotor orientation. Graphic and functional extremes are emphasized. The usual statistical measures of growth and careful group selection could not be applied; curves of growth were not matched. Nevertheless, prenatal rhesus macaques appear to be a homogeneous population in their structural characteristics and resemble prenatal macaques of other species (Grand, unpublished data). METHODOLOGY In table lA, the conceptual age, body weight, sex and anatomical procedure used are listed for the prenatal specimens (from 141 to 155 days). Age at birth averages 166167 days (conceptual age). Postnatal animals are included in table 1B. Nine adult animals were dissected for limb segment analysis only; the specimens are not included in table 1, but the data are given in table 3. The dissection procedure was reported in the earlier paper of this study (Grand, '77). Greater fluid loss occurred in the fetal forms than in postnatal and adult specimens, but this could not be corrected. lPublication No. 827 of t h e Oregun Regiunal Primate Research Cenler, supported in part by Grants RR-00163 from the National Institutes of Health. USPHS 241 242 THEODORE 1. GRAND TABLE 1 Spcimens of Macuca mulutta A. Specimens from 146 to 155 duys (conceptual age: B. Specunens to adulthood A CONCEPTUAL IDENT. No. PRENATAL BPDSTNATAL SEX AGE BDDY WEIGHT (KO) PRESERVATION 7030 t 141 ~ A Y I ,340 FRESH 6830 6117 6127 F F 146 DAYS I FRESH 149 DAYS N 1%DAYS 6963 7014 7018 6739 7045 6676 R 150 DKiS )I 152 DAYS A F 153 DAYS M 1% DRYS 155 DAYS 502 ,328 372 .467 .447 ,w 7 ,2675 ,371 ,966 153 DAYS M w54 F 6393 1 6341; 5053 5545 M fl r: AD I 1376 M AD, =Muscle I B o n e 13 MONTHS 1.7 1.8 FRESH FROZEh I YEARS YEARS AD. FRESH FRESH FRESH FRESH FROZEk FRESH 1.946 FRESH 2,500 2.700 5.500 9,500 11.75 FRESH FRESH FRESh FRESH FRESH =Skin Prenatal Averages Skin: 15.2 To i 1.86 Muscle: 24.6X f 2.66 Bone: 19.9 f 0.69 7030 6830 61 27 6963 7014 7018 6739 7045 6676 I Postnatal Average Skin: 12.6% i3.45 Muscle 43.4 t 4 0 Bone: 14 4 X 2.9 6454 6393 6344 5053 5545 * I378 ,2004 4835 '4993 I0 20 Ja 4.0 Body Weight io $0 Fig. 1 Bar graph-tissue composition of whole body. RESULTS A. Tissue composition in relation to body weight The weights of skin, muscle, and bone and their percentage relations to body weight are given for each specimen in table 2. The bar 70 so% *, specimens reported in Grand ('771 mauh (fie. 1) represents numerically the bilateral cinfigura-tion for each animal. Calculation of mean and standard deviation shows that the promrtions of fetal tissue vary less and differ- significantly from adult tissue proportions. The skin, which in prenatal animals repreV I 243 ANALYSIS OF BODY WEIGHT: DEVELOPMENT OF MACACA TABLE 2 %sue composition ofwhole body. Su: mdiulduals of the bottom row are postnatal animals #7030 Tlrruf Y ~ , l G f i l % 16.4 55.7 S%W TBW 5.7 imt 8.1 HIND TRUHn 2; BOO" WT. (KG) BliCX "T*EI WT.(GN) i. Taw %7 9.8 447 10.2 54,2 20.7 i6Y.5 748.2 19.4 58.6 73.5 WT.IGM) 2 TBk 220 1 1 8 s ~h'r.lGM) ~ 21.3 69.6' 7R o e 2:: 193.7 266,5 68.8 101.9 ?: 14.7 7.7 2a1 .267 447 116963 P6i27 TISSUE 4.G 8.9 187 117.0 166.8 u1.u 52.7 FORE HIND 116830 risPUE 9.5 44.3 20.7 23.4 --- --- 466 371 194.3 587.9 138 2 5 5 10.4 m4 737.1 793.2 2z,7 313.2 1OOR ci :2411.6 219 463.6 u87 7 263 Bow 26,3 14,3 175.0 FORE HINO TRUNI BODY WT, 40.2 152 25 (KG) *, bilateral weight; 56.1 --- li, 38.0 56,5 244,o 2.7 77.5 160 104.5 --- 55 lOk,k 123.8 548.0 95 165.0 198.9 10s 1175 low eshmate. -, weight not taken. sents about 15%TBW, drops to 12.6%TBW in the postnatal series. The postnatal decrease is even greater (to 11.0%TBW) if one unusually fat animal (#4835) is removed. The prenatal musculature yields a mean of about 24.5% TBW; that of the postnatal animals is over 43.0%TBW. The regional changes are discussed below. The mean for the prenatal skeleton is almost 20% TBW, with narrow variability; in the postnatal animals, this drops below 14.5% TBW. Bone weight is more variable after birth, a fact which concurs with data obtained from other species (author's unpublished observations). B. Limb segments in relation to body weight In the prenatal specimens (table 3A1, the hindlimb segments constitute 15.8% of body weight, the forelimbs 11%TBW. The tail averages 1.1% TBW and the trunk and head the remaining 72.1%TBW. The postnatal forms (table 3B) were divided into two groups: (1)animals weighing up to 3 kg, (2) animals weighing over 5 kg. The relative weights of segments were averaged for each of the groups. The lighter, younger animals diverge from the prenatal series. This shift is continued and "completed developmentally" in the fully adult animals. In the heaviest animals, the hindlimbs average 23% TBW, the forelimbs 12.6% TBW. The tail drops in relative weight, so that the head and trunk now constitute 63.7%TBW. A detailed analysis of two representative animals in figure 2 illustrates the complexity of weight distribution and of regional tissue changes. The profiles are similar to those obtained for other prenatal and postnatal specimens. 1. Prenatal M mulatta In a 150-day fetus (#6127) (fig. ZA), each hindlimb represents about 8% TBW, each 244 THEODORE 1. GRAND TABLE 3 Maraca mulatta-segmentation analysis and averages A. Prenalal B. Postnatal-up to three kg C. Postnatal-over five kg A C!% SiDXl SEGMENT WT, IGRI SEGniui 6117 S E ~ E NW T i, Wi, (LM !?I) P L 5,7 11.1 12.3 ... ... .~. 1.9 10.J 25.5 25.6 18.2 31.0 54.6 nn~,,. FORE*PII UWER A R V FOOT CALF r ~:GH TAIL l c ~ vWT, (KG) 10.0 24.0 27.1 18.2 30.4 53.5 11.1 ‘I , ’: 6.5 ‘I , 3 6.8 7.1 7.3 6.’: 7.3 12.0” 6.1 ----- 3,4 3.0 8.7 8.2 6.9 8.6 L.6 15,/ 32 4.b 2.9 L.li 25,? 67 R 86 6 7l.i K 6 2 SiGMEVT 41.4 93,l 3 2 ,0 26.6 91.3 :ae.o 553.0 52.7 ... 7.5 8.1 nr L 50.2 253 2 391.9 382,t 471 257 6 YY.5 K76 S ~ i n ~ tUT, lr (GY: AVERAGE 1 T?il 6.0 10.7 10.4 9.5 ]‘.I 19.7 5 4 24.2 61.1 85.0 44.1 86.1 194,7 2..4 46.5 190.3 282.4 81.9 212.0 b83.2 59.3 8.27 57.2 223 8 267.7 86.0 232.5 619.5 87.0 9.5 ~1378 (69) 886.5 43,3 141 ? 715 r 97 1 240 2 569 3 214,6 R 51.0 262.4 261.0 45 1 6 ‘ 4 199, L 7 c 6.13 23 7 37.5 52.5 161.3 52.0 235.0 87.3 193.F 483 7 73.0 24,s 67 1 83.: 183.b 19.4 :&l; 50 14 2 3 4 5.3 60.2 YilL5 S~GnrhlrU T , 5.2 8.. 8.9 7,: 5.3 20.2 131,u 175,b 552.3 5.8 4.8 14.0 33.0 139,m 410.8 26.11 pjp9 SEGMENTW T , (LM) 59.0 70.2 34.6 70.2 16.7 28.0 53.9 128.3 212. 0 66.5 55 L 18.9 55.2 68.’: 34.4 68 3 163.2 1’19.2 17.0 15,s 41.7 53.5 34.7 125.4 185.9 65.3 164, : Q Sl27 SLBIIENT Wi, !GM) 918 3 88.7 11.35 SElElENT ki. lBW :GK 69.6 0.6 304.7 24 33 1.1 27 7.7 0.7 333 3 124.5 323 1 915 1 78.5 I:, 75 , weight not taken, *, low estimate forelimb about 6% TBW. Almost 72% TBW is concentrated in head and trunk. The skeleton is 11%TBW; the viscera, heart, and brain, 40%; the truncal muscular components, 15%; and the back extensor muscles 2.6%. Bone increases and muscle decreases distally in both hindlimb and forelimb. In the hindlimb, bone is over 18%of thigh weight, and 43%of foot weight. Muscle is 48%of thigh weight, but 14.5%in the foot (table 4). 2. Postnatal M mulatta In the adult (#5053) in figure 2B, the hindlimbs constitute almost 25% TBW; the thigh “increases” to 8%TBW and the foot “drops” t o 1.2% TBW. The tail “drops” to 0.5% TBW. Muscle increases considerably in each segment, but both bone and skin are relatively reduced. The musculature in the thigh constitutes 80% of its weight. Muscle increases in the calf and foot (table 4). A similar shift occurs in the forelimb. Two changes should be noted: first, the upper arm segment increases in percent of total body weight, whereas the hand decreases; second, the muscular proportions in each segment rise while bone and skin are usually lowered (table 4). The adult trunk and the viscera relatively 245 ANALYSIS OF BODY WEIGHT: DEVELOPMENT OF MACACA X TBW X TBW 2 2 0 Slun 37 I Muscle 0Bane 23 23 19 13 A 6'27 B 5053 I 58 L l50doys TAIL HINDLIMBS 051 2 4 8 I TRUNK 62 I FORE- 100% TBW Adult Fig. 2 Segment figures-segments and tissue composition A. #6127-150 days (conceptual age). B. #5053--adult male decrease by 10% TBW (fig. 31, and the skin and truncal skeleton decrease somewhat. Each group of muscles (particularly the truncal-forelimb and back extensors) increases; the back extensors, for example, constitute 5% TBW. Thus, in adulthood the entire trunk is reorganized in relative weight, and musculature is the dominant component. C. Segment variability The variability of the prenatal segments and tissue components is somewhat narrow (fig. 3). Hand, foot, and thigh are significantly different from those of the postnatal sample. As expected, the segments of younger animals (1-3kg) are intermediate between those of the prenatal and adult forms; with increased body weight, the foot and hand decrease and the thigh doubles in percent TBW. The growth curves are clearest here. The calf increases and the tail decreases in percent of weight, but both segments are more variable than those previously mentioned. TABLE 4 T u su e composition of segments of #6127 and #5053 _._ ..3 'l.4 1.6 159 53.7 21.9 1.3 14.9 552 21.8 13.7 22.2 10.4 70.7 17.7 31.2 16.7 41.7 12.C Y.1 13s 34.6 282 37.5 45.5 103 80.6 '1.8 1.1 1 5 0,8 7 0 3.81 65 2.5 I.! '1.0 23 2.c 1.0 3,o 1 L1.l 13i 5 21, 7 8R.6 21.9 481 18.2 565,' lZ4 465 26.7 112 0 29.0 14.5 43.5 122 74.0 13.2 41 1 8.9 I! 8 9.6 68.3 21.6 55 4 10 j 19 1 25 3 29.9 29.2 38.7 246 THEODORE I. GRAND 90: . ... .. . . .. 50 .. . . 40 1 u - .. .. . :I 22 L 2oL2 I S 3 4 5 6 7’ B’ 9 ’ 10 ! I1 ’ I2 ’ Ekdy Weight [kgs) 1 2 3 4 5 8 7 8 9 1 0 112 Body Weight ( k g s l Fig 3 Segment variation compared w i t h body weight DISCUSSION At any stage of life, bone, muscle, and skin together constitute 60 to 70% of body weight; and from birth to maturity, these tissues are responsible for the motor repertoire. (Paradoxically, the remaining 30 to 40% [viscera, heart, brain, larger glands1 have received far greater attention. See Spector, ’56 for a review.) The prenatal form undergoes dramatic segmental redistribution of weight as well as alteration of tissue and organ ratios to achieve adult form and composition. To examine the fate of the “locomotor tissues and segments,” I framed certain questions that had been applied to the adults of various species: How does the composition of these tissues change from prenatal through postnatal development? How are the tissues distributed to the limb segments and how does the distribution change? How are these changes related to locomotor demands? The tissues in the prenatal macaque are almost equal in weight (skin 15%,bone 20% muscle 24%TBW), but during the first year they begin to diverge considerably (skin 12%, bone 15%, muscle 43%). Although time of maturity varied, Palsson (’55) and Fowler (’68) found these shifts in various birds and mammals, and Wilmer (‘40) found a similar shift in man. In rhesus macaques, the decrease in the relative weight of skin can be explained in two ways: (1)the skin is a protective covering which does not need to keep pace with an increasingly independent motor life; (2) volume and weight increase by the cube whereas surface area and skin covering increase only by a square (Thompson, ’69). Muscular development is most important because the motor patterns of early postnatal life change with locomotor independence. The survival mode of the newborn is clinging to the mot her; therefore, truncal coordination and fore- and hindlimb propulsive thrust are minimized. The hands and feet are heavy; the thigh, upper arm, and back are low in muscle. ANALYSIS OF BODY WEIGHT: DEVELOPMENT OF MACACA Increasing maturity, however, is directly associated with muscle and with whole body activity. Muscle develops in thigh, back extensor and upper arm. As a result, the thigh and upper arm segments increase relatively, the hands and feet decrease. The tissue shift brings about two other phenomena. First, the hands and feet become relatively lighter, forearms and calves become slightly heavier, thighs and upper arm segments much heavier. The centers of mass of fore- and hindlimbs are elevated. Recovery motions may require less effort in the older animals. The limbs, however, increase in absolute weight. These weight increases go directly into limb musculature, and the trunk becomes relatively lighter. A second developmental process is change of density. Although the water content of the body drops, this is complicated by tissue and organ changes. The viscera, less dense than the musculoskeletal apparatus, become lighter. The limb bones become more dense and muscle volume increases. The precision of other methods (ash weight or calcium content of bone, dry weight of muscle) is required to trace these changes (Mitchell e t al., '45; Rathbun and Pace, '45; Morales et al., '45; Pace and Rathbun, '45; Brody, '45). An apparent difference between the results of this study and those of Trotter and Hexon ('74) and Trotter et al. ('75) is traced to procedure. This study demonstrates that the wet weight of bone drops in relative % TBW; the other studies show that the dry, fat-free skeleton increases in % TBW up t o six years. I am describing living tissues and live weight whereas they are characterizing changes in body chemistry and tissue density. Nevertheless, the functional framework presented here is another approach to body decomposition or somatolysis (Brozek, '63), which reinforces earlier findings that tissue features distinguish newborn from adult, and that the components of body weight must be separated a t different stages of development. Further, it demonstrates that selection operates upon the components of size and upon survival skills of each stage of life: the motor requirements of the clinging newborn contrast to those of the independent juvenile and adult, in whom climbing skill, acceleration, and endurance are enhanced by truncal coordination and integration of forelimb and hindlimb motions. The ratios of skin, muscle, and bone and their distribution throughout 247 the body illustrate how the adult form is the resultant of many selective forces. ACKNOWLEDGMENTS This study has extended over several years and many people have cooperated with me: Alan Rogers of the University of Oregon Medical School and Paul Miller of the Oregon Regional Primate Research Center have obtained my nonprimate specimens (mixed breed dogs, racing greyhounds, cats, jack rabbits); Nicholas Smythe (Smithsonian Tropical Research Institute), Gary Dawson, and John Eisenberg (National Zoological Park) obtained my South American specimens; Margaret Rarss, Adrienne Zihlman, Patricia Ladd, Robert Kuehn, and William Montagna have reread critically several drafts of each section of the paper; Rose Mary Bocek and Clarissa Beatty have read over and commented upon this paper; discussions with William Hunter and Charles Wood have been important. The ORPRC staff was helpful throughout research and preparation, particularly Steve Estvanik and Ingrid Palm for mathematical and statistical evaluation, and Joel Ito and Kathleen Kerr for the evolution of the tables and figures. Sheila Alderman, Joyce Hodges, Barbara Renstrom, and Karen Anderson brought order t o the remaining chaos with their typing and retyping of successive stages of the entire manuscript and its tables. LITERATURE CITED Beatty, C. H.. G. M. Basinger and R. M. Bocek 1967 Differentiation of red and white fibers in muscle from fetal. neonatal, and infant rhesus monkeys. J . Histochem. Cytochern., 15: 93-103. Brody, S. 1945 Bioenergetics and Growth. Rcinhold Publishing Company. New York, 1023 pp. Brozek, J. 1955 Role of anthropology in the study of body composition: toward a synthesis of methods. In: Dynamic Anthropometry. Roy Waldo Miner, ed. Ann. N. Y. Acad. Sci., 63: 491-504. 1961 Body composition. 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Interspecific comparisons. Am. J. Phys. Anthrop., 47:211240. Keys, A,, and J. Brozek 1953 Body fat in adult man. Physiol. Rev.. 33: 245-325. Mitchell, H. H.. T. S. Hamilton. F. R. Steggerda and 11. W. Bean 1945 The chemical composition of the adult human body and its bearing on the biochemistry of growth. J . Bid. Chem., 158: 625-637. Morales, M. F., E. N. Rathbun. R. E. Smith and N. Pace 1Y45 Studies on body composition 11. Theoretical considerations regarding the major body tissue components. with suggestions for application to man. J. Biol. (:hem.. 158: 677.684. Pace. N.. and E. N. Rathbun 1945 Studies on body cumpusition. 111. The body water and chemically combined nitrogen content in relation to fat content. J. Biul. Chem., 158: 685-691. Palsson. H. 1955 Conformation and body composition. In: Progress in the Physiology of Farm Animals. Vol. 2. John Hamnrond. ed. Butterworths, London. pp. 430-542. Parizkovd, J . 1968 Body composition and physical fitness. 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