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Keywords:

  • locomotion;
  • Pongo;
  • Pan;
  • physiological cross-sectional area;
  • positional behavior

Abstract

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

Eight forelimbs of three orangutans and four chimpanzees were dissected and the muscle mass, fascicle length and physiological cross-sectional area (PCSA) of all forelimb muscles were systematically recorded to explore possible interspecies variation in muscle dimensions. Muscle mass and PCSA were divided by the total mass and total PCSA of the entire forelimb muscles for normalization. The results indicate that the mass and PCSA ratios of the monoarticular elbow flexors (M. brachialis and M. brachioradialis) are significantly larger in orangutans. In contrast, the mass ratios of the biarticular muscles in the upper arm (the short head of M. biceps brachii and the long head of M. triceps brachii) are significantly larger in chimpanzees. For the rotator cuff muscles, the force-generating capacity of M. subscapularis is significantly larger in orangutans, whereas the opposite rotator cuff muscle, M. infraspinatus, is larger in chimpanzees. These differences in forelimb muscle dimensions of the two species may reflect functional specialization for their different positional and locomotor behaviors.


Introduction

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

Orangutans and chimpanzees are generally regarded as adapted to climbing and suspension in an arboreal environment due to their common morphological features associated with suspension, including a broad thorax, dorsally placed scapulae and long forelimbs (Aiello & Dean, 1990; Larson, 1993; Rose, 1993; Fleagle, 1999). However, positional and locomotor behaviors of the two large-bodied great apes are actually known to differ substantially. Orangutans are fundamentally quadrumanous climbers in the rain forest canopy, and they seldom walk on the ground. Indeed, field researchers have suggested that females and young orangutans spend almost all of their lives in trees and never descend to the forest floor (MacKinnon, 1974; Cant, 1987; Delgado & van Schaik, 2000; Thorpe & Crompton, 2005, 2006). Exceptions are the larger male orangutans in Borneo, which spend about 20% of their total travel time on the ground to move between trees (Rodman, 1979). However, chimpanzees travel between feeding trees mainly on the ground by knuckle-walking. Chimpanzees spend nearly 90% of their total travel time on the ground (Doran, 1992), and knuckle-walking accounts for 90% of all locomotor modes (Hunt, 1992). Consequently, the arboreal locomotor repertoire of orangutans is much more versatile than that of chimpanzees (Thorpe & Crompton, 2006). When comparing arboreal locomotion between the two species, in orangutans, the frequency of suspensory locomotion accounts for 39% of traveling and feeding, followed by vertical climbing (25%) and quadrupedal walking (18%) (Thorpe & Crompton, 2006); in chimpanzees, vertical climbing (50%) is the predominant locomotion because they approach food sources from the ground, followed by quadrupedal walking (31%) in trees (Hunt, 1992). In vertical climbing, orangutans exhibit relatively longer cycle duration and longer stride length than African apes (Isler & Thorpe, 2003; Isler, 2005), indicating slow and cautious arboreal climbing in orangutans.

Such marked contrasts in positional and locomotor behaviors between orangutans and chimpanzees are actually reflected in their forelimb skeletal morphology. For instance, the scapula of orangutans possesses a relatively larger infraspinous fossa (Roberts, 1974), a lower angulated spine (Young, 2003, 2008) and a shortened coracoid and acromion (Ciochon & Corruccini, 1977) than that of chimpanzees to allow enhanced shoulder joint mobility. The ulna of orangutans also appears to be longer (Drapeau & Ward, 2007) and has a relatively shorter olecranon process (Drapeau, 2004) for longer reach with full extension of the elbow. The proximal and middle phalanges of orangutans are more curved (Susman, 1979) than those of chimpanzees. These morphological features of orangutans suggest that the orangutan is more specialized for arboreal life. However, it has been suggested that humeral head torsion is relatively larger in chimpanzees, permitting the elbow to rotate on a parasagittal plane (Larson, 1988, 1996). In addition, dorsiflexion of the wrist joint and extension of the metacarpophalangeal joints are mechanically restricted in chimpanzees due to the projected dorsal margin of the distal radius and the heads of the metacarpals (Tuttle, 1967, 1969; Susman, 1979; Richmond & Strait, 2000), implying that the skeletal architecture of the chimpanzee is more specialized for terrestrial knuckle-walking.

Because locomotor capabilities are determined by the structure and function of both skeletal and muscular systems, one could expect that such differences in the positional and locomotor behaviors in orangutans and chimpanzees would also be reflected in their muscle morphology. To date, however, very few reports have described the forelimb muscle morphology of the chimpanzee (Thorpe et al. 1999; Ogihara et al. 2005; Carlson, 2006) and orangutan (Payne, 2001; Oishi et al. 2008), although the muscle morphology of the hindlimb of these species has been more completely described (Thorpe et al. 1999; Payne, 2001; Payne et al. 2006). Recently, we had additional opportunities to dissect several orangutans and chimpanzees. Therefore, this study aimed to provide complete quantitative data on the forelimb muscles of these species. Interspecies variations in the muscle dimensions of orangutans and chimpanzees are then explored, and possible functional relationships with their positional and locomotor behaviors are discussed.

Materials and methods

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

Eight forelimbs of three orangutans and four chimpanzees were dissected. Three adult orangutan specimens (O1, O2 and O3) were obtained for dissection from Yagiyama Zoological Garden, the Primate Research Institute, Kyoto University, and Higashiyama Zoo and Botanical Garden, respectively. Four adult chimpanzee specimens (C1, C2, C3 and C4) were donated to the Primate Research Institute, Kyoto University or the National Science Museum (Tokyo, Japan) from Chausuyama Zoo, Nogeyama Zoo, Yamajiboku and Tama Zoological Park, respectively. General specimen data are presented in Table 1. Two orangutan specimens (O1 and O2) had been preserved in alcohol after death. The chimpanzee specimens were all stored frozen until dissection. The data of the female fresh orangutan specimen (O3) were taken from our previous study (Oishi et al. 2008) and are included here for interspecies comparisons.

Table 1.  General specimen data
 O1O2O3C1C2C3C4
  1. Ppa, Pongo pygmaeus abelii; Ppa*Ppp, Pongo pygmaeus abelii*pygmaeus; Pt, Pan troglodytes. O3 data are cited from a previous study (Oishi et al. 2008). CV, cardiovascular disease; Ge, geromarasmus; ID, infectious disease; DD, digestive disease. 70% alc., 70% alcohol. Upper arm length, distance from greater tubercle to lateral epicondyle of humerus; forearm length, distance from head to styloid process of radius. In C1 the right and left values were averaged.

SpeciesPpa*PppPpa?PpaPtPtPtPt
SexMMFMMMF
Age at death (years)18104027Approx. 35Approx. 2711
Body weight at death (kg)78.648.846.530.2
Cause of deathCVUnknownGeUnknownIDUnknownDD
Preservation70% alc.70% alc.FrozenFrozenFrozenFrozenFrozen
SideRightLeftLeftLeft and rightRightLeftLeft
Upper arm length (cm)38.832.129.627.926.230.826.6
Forearm length (cm)39.831.430.927.725.426.324.8
Total muscle mass of forelimb (g)5677.44948.9752.64008.53127.12918.81946.8

During dissection, the muscles listed in Table 2 were exposed and removed from the forelimb bones. The muscle belly (between the proximal ends of the most proximal and distal ends of the fibers of the muscles) and the external tendon were separated at the belly–tendon junction, and muscle belly mass (= mass) was measured using an electronic balance. Each muscle belly was immersed in 10% formalin and then in water overnight. Muscle fiber length (= fascicle length) was measured at three to six places dissected in varying locations within the muscle belly using calipers, and the mean value was calculated. In fixed specimens (O1 and O2), muscle mass was based on the wet weight of the fixed muscles, which were weighed after immersion in water overnight. The physiological cross-sectional area (PCSA) was calculated by dividing muscle volume by fascicle length. Muscle volume was obtained by dividing muscle mass by muscle density (1.0597 g cm−3) (Mendez & Keys, 1960). The PCSA is proportional to the force-generating capacity of the muscle (Close, 1972; Zajac, 1992; Maclntosh et al. 2006). The pennation angle (the angle between the direction of the muscle fibers and the tendon) was not included in the calculation of PCSA because it was difficult in the two-dimensional muscle model to correctly measure the angle of the three-dimensional fascicle within a muscle. Moreover, the muscle moment arms were not measured in this study because such measurements are technically difficult without an experimental setup as in Payne (2001). For C1, both right and left forelimbs were dissected; hence, the right and left values were averaged to obtain the data listed in Table 2.

Table 2A.  Morphometric data for the muscles of the forelimb in the orangutans
 AbbreviationO1O2O3
Mass (g)PCSA (cm2)FL (cm)Mass (g)PCSA (cm2)FL (cm)Mass (g)PCSA (cm2)FL (cm)
  1. In the orangutan M. extensor indicis was partially separated into two bundles, and inserted into both the second and third digits; M. extensor digiti minimi also consisted of two partially-separated bundles inserted into the fourth and fifth digits; in one orangutan (O3) M. flexor digitorum profundus had a weak bundle as an accessory head, which arose from a capsule in the elbow joint and the coracoid process of the ulna with M. flexor digitorum superficialis. These noted differences are consistent with previous reports (Sonntag, 1924; Sullivan & Osgood, 1927; Oishi et al. 2008). The mass of the fixed specimens (O1 and O2) was based on the wet weight of the fixed muscles, which were weighed after immersion in water overnight. For O3 data see previous study (Oishi et al. 2008). PCSA, physiological cross-sectional area; FL, fascicle length.

Teres majorTMa189.114.3612.4176.720.188.326.62.1511.7
Teres minorTMi47.76.906.555.310.634.96.81.344.8
Deltoideus, pars clavicularisDC190.516.2011.1169.413.2612.121.32.398.4
Deltoideus, pars acromialisDA398.247.148.0288.033.398.151.16.937.0
Deltoideus, pars scapularisDS104.611.088.9100.211.808.012.91.2110.0
SupraspinatusSp202.433.325.7121.818.716.114.13.813.5
InfraspinatusIf254.325.959.2250.332.157.333.94.776.7
SubscapularisSb449.452.638.1353.857.295.850.710.044.8
Biceps brachii, caput longumBL164.69.2616.8147.610.1613.717.81.719.9
Biceps brachii, caput breveBS110.35.2020.0134.97.3717.320.11.5012.7
Coracobrachialis mediusCoM78.513.675.474.013.505.212.42.594.5
Coracobrachialis longusCoL
BrachialisB412.728.9013.5449.435.7911.857.17.377.3
DorsoepitrochlearisDE50.44.929.765.47.887.85.90.5310.5
Triceps brachii, caput longumTLo172.219.508.3141.816.288.222.32.159.8
Triceps brachii, caput lateraleTLa235.723.049.7179.918.629.125.42.878.3
Triceps brachii, caput medialeTMe325.532.809.4199.623.478.031.74.227.1
AnconeusAL17.15.283.013.16.371.91.00.263.5
BrachioradialisBr379.514.3624.9438.918.9321.961.64.2213.8
Extensor carpi radialis longusECRL46.44.0810.764.84.6213.210.01.367.0
Extensor carpi radialis brevisECRB87.68.749.575.59.507.511.81.925.8
Extensor digitorum 2EDC227.32.3311.126.73.277.75.50.707.5
Extensor digitorum 3EDC332.82.9710.426.93.148.14.10.765.1
Extensor digitorum 4EDC426.72.4010.519.82.527.42.90.485.7
Extensor digitorum 5EDC529.02.5310.818.52.516.98.80.938.9
Extensor indicis 2EI212.21.249.37.40.997.12.60.357.1
Extensor indicis 3EI313.81.598.27.21.155.94.00.586.5
Extensor digiti minimi 4EDM47.60.858.510.41.636.01.80.237.2
Extensor digiti minimi 5EDM58.30.908.710.31.357.22.70.318.3
Extensor carpi ulnarisECU76.59.287.870.812.515.310.71.775.7
SupinatorSpn105.321.944.588.323.023.611.14.182.5
Abductor pollicis longusAPL68.78.337.857.912.634.311.93.133.6
Extensor pollicis longusEPL15.51.648.913.61.747.42.20.375.6
Pronator teres, caput humeralePTh80.412.036.360.710.015.77.41.494.7
Pronator teres, caput ulnarePTu20.54.164.718.64.144.27.31.863.7
Flexor carpi radialisFCR124.112.959.0103.018.355.317.82.766.1
Palmaris longusPL42.84.628.832.45.655.44.10.547.2
Flexor carpi ulnarisFCU118.812.369.184.716.884.713.72.016.4
Flexor digitorum superficialis 2FDS250.57.736.247.712.253.76.50.807.7
Flexor digitorum superficialis 3FDS384.99.358.668.111.475.610.71.079.4
Flexor digitorum superficialis 4FDS471.96.899.857.79.385.85.70.618.9
Flexor digitorum superficialis 5FDS528.63.178.526.54.925.12.80.328.3
Flexor digitorum profundus 2FDP2111.47.3814.270.49.037.416.01.4910.2
Flexor digitorum profundus, caput accessoriumFDPa3.80.418.7
Flexor digitorum profundus 3FDP3132.18.1715.3114.212.518.629.22.4411.3
Flexor digitorum profundus 4FDP4134.37.7716.3102.410.089.618.31.799.6
Flexor digitorum profundus 5FDP583.34.7516.573.57.719.010.21.009.6
Pronator quadratusPQ16.96.672.411.85.022.23.11.222.4
Abductor pollicis brevisAPB13.52.804.515.93.804.02.20.583.6
Flexor pollicis brevisFPB12.73.653.312.23.952.90.90.611.5
Opponens pollicisOP4.01.462.65.91.922.91.00.422.3
Adductor pollicisAP32.26.574.632.07.584.01.20.482.4
Abductor digiti minimiADM13.72.794.617.95.393.12.40.613.7
Flexor digiti minimi brevisFDMB10.01.994.86.01.773.21.10.323.4
Opponens digiti minimiODM6.33.431.76.74.181.50.70.661.0
Dorsal interosseus 1DI139.77.984.739.310.393.66.72.362.7
Dorsal interosseus 2DI221.36.073.321.98.192.54.71.742.6
Dorsal interosseus 3DI315.64.693.113.15.012.51.80.662.5
Dorsal interosseus 4DI416.35.492.815.05.272.72.20.892.4
Palmar interosseus 1PI111.52.654.18.33.342.32.20.653.2
Palmar interosseus 2PI26.01.663.46.52.312.62.00.583.3
Palmar interosseus 3PI39.02.273.75.42.152.31.70.493.2
Lumbricalis 1L16.00.5410.63.50.418.10.60.069.3
Lumbricalis 2L28.60.7810.34.10.468.50.80.0810.0
Lumbricalis 3L36.70.6310.13.70.3310.80.70.079.4
Lumbricalis 4L43.90.3610.32.20.219.90.30.046.6
Table 2B.  Morphometric data for the muscles of the forelimb in the chimpanzees
AbbreviationC1C2C3C4
Mass (g)PCSA (cm2)FL (cm)Mass (g)PCSA (cm2)FL (cm)Mass (g)PCSA (cm2)FL (cm)Mass (g)PCSA (cm2)FL (cm)
  1. In two chimpanzees (C1 and C3) M. pronator teres had a bundle as an ulnar head. One chimpanzee (C3) possessed M. coracobrachialis brevis and M. coracobrachialis longus. The former was inserted into the middle of the humerus and the latter into the medial epicondyle of the humerus. These noted differences are consistent with previous reports (Sullivan & Osgood, 1927). In C1 left and right values were averaged. Muscle name abbreviations are as detailed in Table 2A. PCSA, physiological cross-sectional area; FL, fascicle length.

TMa292.821.6612.8162.711.2113.7149.110.5713.398.57.3212.7
TMi45.18.185.224.74.015.834.16.584.920.53.146.2
DC118.612.109.279.66.5511.567.35.9210.750.95.149.3
DA222.933.976.2225.329.867.1216.432.906.2116.019.085.7
DS88.17.4711.261.54.3913.256.84.4512.138.53.2911.0
Sp113.726.604.177.917.454.2107.522.534.552.613.093.8
If233.230.737.2178.821.457.9180.929.155.9110.316.356.4
Sb303.046.076.2195.527.686.7207.925.647.7154.925.105.8
BL137.810.9511.878.44.9215.0104.46.7514.662.25.6010.5
BS191.114.2212.7139.38.1116.287.24.0620.377.15.8612.4
CoM58.812.154.652.88.086.236.05.835.830.55.355.4
CoL29.34.496.2
B247.928.918.1151.213.9210.3136.111.9610.7106.412.907.8
DE51.25.109.445.43.1813.524.21.8112.622.71.8111.9
TLo155.919.867.4168.613.9611.4180.818.119.492.09.619.0
TLa161.122.876.7143.913.3110.2222.222.359.485.29.848.2
TMe218.635.105.9264.128.678.7132.717.217.3126.916.977.1
AL12.33.183.711.12.893.68.01.884.05.81.503.6
Br151.48.5816.785.23.5522.782.33.4222.778.64.3117.2
ECRL35.44.267.947.13.5412.543.53.8110.818.52.247.8
ECRB38.26.785.339.85.486.945.86.956.223.24.085.4
EDC221.12.637.619.42.009.110.41.178.410.61.377.3
EDC327.02.868.920.01.919.923.82.419.314.81.668.4
EDC423.82.837.922.22.438.614.51.688.110.51.277.8
EDC57.70.997.35.00.509.45.90.717.81.60.198.0
EI24.70.716.212.81.528.04.00.556.83.10.525.7
EI3
EDM4
EDM511.51.706.36.60.966.56.20.926.47.20.986.9
ECU28.15.734.625.94.665.231.06.494.519.03.215.6
Spn73.922.283.164.617.503.549.714.863.236.912.602.8
APL47.411.683.839.29.813.835.17.404.532.38.693.5
EPL7.91.465.27.31.265.53.80.754.85.00.865.4
PTh67.311.865.451.211.144.329.84.346.528.16.713.9
PTu4.30.974.113.13.653.4
FCR99.215.666.096.112.827.150.78.205.847.46.846.5
PL11.02.334.56.61.434.47.91.236.13.00.763.8
FCU74.216.474.374.413.675.167.613.244.836.98.124.3
FDS236.912.872.731.06.974.225.75.034.816.64.273.7
FDS377.412.465.952.85.988.357.66.877.945.07.245.9
FDS433.75.985.237.74.098.757.36.458.430.65.585.2
FDS538.77.434.812.91.996.18.81.276.511.22.594.1
FDP270.710.456.435.03.908.537.64.418.126.63.367.5
FDPa
FDP377.19.038.155.44.8710.756.85.499.847.85.368.4
FDP489.611.787.256.86.138.753.45.459.238.64.967.3
FDP557.09.205.936.04.797.126.53.517.130.04.925.8
PQ12.97.821.614.85.052.810.44.632.18.63.782.1
APB10.13.562.76.41.883.23.11.062.84.01.213.1
FPB6.12.692.11.90.662.72.91.022.71.90.642.8
OP2.01.341.55.11.992.43.41.741.92.91.122.4
AP15.44.583.210.93.183.29.52.633.46.52.043.0
ADM11.64.842.312.84.422.78.32.423.26.62.492.5
FDMB1.60.632.42.50.733.21.50.492.91.80.602.9
ODM3.73.051.13.23.181.03.42.561.22.21.151.8
DI119.78.462.216.87.122.212.55.192.38.13.912.0
DI213.87.101.88.04.671.67.93.142.46.73.321.9
DI39.34.731.97.94.211.85.32.202.34.22.491.6
DI49.35.291.78.03.602.15.51.932.75.52.881.8
PI15.92.582.210.43.502.83.51.083.13.01.292.2
PI25.42.691.96.21.933.03.40.893.63.21.402.1
PI35.82.691.94.32.481.63.01.192.42.21.211.7
L12.50.288.52.50.308.01.70.227.21.50.178.2
L22.20.2010.32.20.2110.12.00.218.71.60.188.7
L32.00.199.90.90.099.21.50.169.11.80.199.0
L41.80.189.51.20.1011.20.50.059.40.80.099.0

The mass of each muscle was divided by the total muscle mass of the forelimb to calculate the mass ratio. The PCSA ratio was also calculated in the same way. The muscle parameters were not normalized by body mass as in Payne (2001) because the body mass was not available for every specimen used in the present study. Each mean fascicle length was normalized by dividing by upper arm length (Table 1) because Drapeau & Ward (2007) indicated that humeral length is fairly conservative in orangutans and chimpanzees, although the ulna of orangutans is relatively longer than that of African apes. The normalized fascicle was calculated as the weighted harmonic mean (i.e. the significance of each individual fascicle length weight by the muscle mass) (Alexander et al. 1981). These normalizations allow comparisons of muscle dimensions between the orangutan and chimpanzee. The significance of differences in the mean mass ratios and PCSA ratios between the two species was examined by the nonparametric U-test (P < 0.05) using SPSS 11.0J (SPSS, Chicago, IL, USA). The coefficient of variation was calculated for each muscle to assess variability.

Results

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

The measured muscle mass, PCSA and fascicle length of all forelimb muscles are presented in Table 2. For each individual, mean ratios (± standard deviation) of measured to species-average muscle mass, PCSA and fascicle length were computed for comparisons. The mean ratios of muscle mass were 1.50 (± 0.18), 1.28 (± 0.18) and 0.22 (± 0.09) for O1, O2 and O3, respectively, and 1.33 (± 0.26), 1.09 (± 0.25), 0.91 (± 0.21) and 0.67 (± 0.13) for C1, C2, C3 and C4, respectively, suggesting that, in both species, male muscles were absolutely larger than those of females (O3 and C4) and the muscles of O3 were particularly small. The mean PCSA ratios were 1.30 (± 0.21), 1.44 (± 0.21) and 0.25 (± 0.10) for O1, O2 and O3, respectively, and 1.44 (± 0.27), 0.99 (± 0.23), 0.85 (± 0.22) and 0.71 (± 0.14) for C1, C2, C3 and C4, respectively, showing similar tendencies as those for muscle mass. The mean fascicle length ratios were 1.18 (± 0.11), 0.92 (± 0.14) and 0.90 (± 0.16) for O1, O2 and O3, respectively, and 0.91 (± 0.10), 1.08 (± 0.10), 1.07 (± 0.11) and 0.94 (± 0.11) for C1, C2, C3 and C4, respectively. Unlike mass and PCSA, both species showed a small degree of sex-related variation in fascicle length.

Comparisons of the mean mass and PCSA ratios in the orangutans and chimpanzees are presented in Table 3. The means of the coefficients of variation were 0.21 and 0.24 for the mass ratios and PCSA ratios, respectively, in the orangutan and 0.21 and 0.23, respectively, in the chimpanzee, indicating that some inter-individual differences actually exist in both species.

Table 3.  Comparisons of forelimb mass and physiological cross-sectional area (PCSA) ratios between the orangutan and chimpanzee
 Mass ratio (%)PCSA ratio (%)FL/upper arm length
Orangutan (SD)Chimpanzee (SD)Orangutan (SD)Chimpanzee (SD)Orangutan (SD)Chimpanzee (SD)
  1. Mass ratios and PCSA ratios were calculated as a subtotal of the constituent muscles of muscle groups and normalized fascicle as weighted harmonic mean (Alexander et al. 1981). Standard deviations (SD) are shown in parentheses. Underline indicates statistically significant larger value (P < 0.05). FL, fascicle length. Muscle name abbreviations are as detailed in Table 2A.

Shoulder protractors
 DC3.2 (0.33)2.6 (0.27)2.3 (0.34)1.7 (0.21)0.32 (0.052)0.37 (0.048)
 Co1.5 (0.13)1.7 (0.34)2.3 (0.14)2.1 (0.38)0.15 (0.011)0.20 (0.029)
 Subtotal4.7 (0.22)4.3 (0.17)4.6 (0.41)3.9 (0.32)0.23 (0.029)0.27 (0.036)
Shoulder retractors
 TMa3.5 (0.13)5.7 (1.09)2.5 (0.59)2.9 (0.48)0.32 (0.069)0.47 (0.038)
 TMi1.0 (0.15)1.0 (0.17)1.4 (0.27)1.3 (0.32)0.16 (0.008)0.20 (0.034)
 DS1.9 (0.15)2.0 (0.12)1.6 (0.42)1.2 (0.07)0.27 (0.058)0.43 (0.053)
 Subtotal6.3 (0.37)8.7 (1.27)5.5 (1.16)5.3 (0.70)0.27 (0.043)0.40 (0.048)
Shoulder abductor
 DA6.5 (0.64)6.5 (0.91)6.5 (1.34)7.0 (1.24)0.23 (0.024)0.23 (0.031)
Rotator cuffs
 Sp2.6 (0.86)2.9 (0.52)4.0 (1.39)4.8 (0.73)0.15 (0.037)0.15 (0.008)
 If4.7 (0.33)5.8 (0.24)4.6 (0.37)5.9 (1.13)0.23 (0.006)0.25 (0.046)
 Sb7.3 (0.60)7.2 (0.73)9.0 (0.24)7.4 (0.84)0.18 (0.023)0.24 (0.018)
 Subtotal14.6 (1.42)16.0 (1.09)17.6 (0.99)18.1 (1.55)0.19 (0.016)0.22 (0.021)
Biarticular elbow extensors
 TLo3.0 (0.08)5.1 (0.98)2.6 (0.64)3.7 (0.68)0.27 (0.059)0.34 (0.072)
 DE1.0 (0.28)1.2 (0.26)0.8 (0.37)0.7 (0.17)0.28 (0.062)0.43 (0.074)
 Subtotal4.0 (0.22)6.2 (0.87)3.3 (1.13)4.4 (0.56)0.27 (0.059)0.35 (0.073)
Biarticular elbow flexors
 BL2.8 (0.33)3.2 (0.47)1.6 (0.02)1.7 (0.30)0.40 (0.056)0.47 (0.078)
 BS2.4 (0.44)4.0 (0.78)1.1 (0.26)1.9 (0.56)0.49 (0.058)0.55(0.103)
 Subtotal5.2 (0.45)7.2 (0.70)2.7 (0.27)3.5 (0.62)0.44 (0.052)0.50 (0.082)
Monoarticular elbow extensors
 TLa3.7 (0.40)5.2 (1.65)3.1 (0.64)4.1 (1.18)0.27 (0.020)0.31 (0.062)
 TMe4.7 (0.93)6.2 (1.68)4.4 (1.00)5.8 (1.09)0.24 (0.006)0.26 (0.052)
 AL0.2 (0.09)0.3 (0.03)0.7 (0.41)0.6 (0.11)0.09 (0.029)0.13 (0.004)
 Subtotal8.6 (1.37)11.7 (1.57)8.4 (1.63)10.4 (0.68)0.24 (0.011)0.27 (0.049)
Monoarticular elbow flexors
 B8.0 (0.97)5.3 (0.69)5.7 (1.00)3.9 (0.79)0.32 (0.065)0.33 (0.049)
 Br7.9 (1.12)3.3 (0.66)3.1 (0.76)1.2 (0.32)0.60 (0.115)0.71 (0.117)
 Subtotal15.9 (2.00)8.6 (1.29)8.8 (1.75)5.1 (1.10)0.42 (0.079)0.42 (0.057)
Wrist extensors
 ECRL1.2 (0.29)1.2 (0.34)0.9 (0.32)0.8 (0.13)0.31 (0.093)0.35 (0.090)
 ECRB1.5 (0.02)1.2 (0.25)1.6 (0.17)1.4 (0.28)0.22 (0.026)0.21 (0.032)
 ECU1.4 (0.05)0.9 (0.16)1.7 (0.21)1.2 (0.32)0.19 (0.018)0.18 (0.030)
 Subtotal4.1 (0.34)3.3 (0.68)4.2 (0.48)3.5 (0.72)0.22 (0.016)0.24 (0.042)
Wrist flexors
 FCR2.2 (0.14)2.4 (0.55)2.5 (0.35)2.6 (0.46)0.20 (0.034)0.23 (0.035)
 PL0.6 (0.11)0.2 (0.06)0.7 (0.20)0.3 (0.06)0.21 (0.039)0.17 (0.023)
 FCU1.9 (0.20)2.1 (0.28)2.2 (0.40)3.1 (0.39)0.20 (0.046)0.17 (0.020)
 Subtotal4.7 (0.29)4.8 (0.61)5.4 (0.82)6.0 (0.69)0.20 (0.038)0.19 (0.025)
Digital II–V extensors
 EDC2.2 (0.51)2.0 (0.11)2.0 (0.51)1.6 (0.08)0.25 (0.022)0.30 (0.031)
 EI0.5 (0.30)0.2 (0.14)0.6 (0.27)0.2 (0.12)0.22 (0.015)0.24 (0.043)
 EDM0.4 (0.16)0.3 (0.07)0.4 (0.11)0.3 (0.04)0.23 (0.031)0.23 (0.023)
 Subtotal3.2 (0.94)2.4 (0.22)3.0 (0.85)2.1 (0.18)0.24 (0.017)0.29 (0.029)
Digital II–V flexors
 FDS3.9 (0.39)4.9 (0.46)4.4 (1.68)5.7 (0.97)0.22 (0.070)0.21 (0.042)
 FDP8.6 (1.55)6.6 (0.83)5.8 (0.99)5.7 (0.95)0.34 (0.065)0.28 (0.037)
 Subtotal12.4 (1.20)11.5 (1.10)10.2 (1.66)11.5 (1.90)0.28 (0.062)0.25 (0.039)
Pollicis extensors
 APL1.3 (0.22)1.3 (0.23)2.1 (0.75)2.3 (0.49)0.15 (0.042)0.14 (0.006)
 EPL0.3 (0.01)0.2 (0.06)0.3 (0.04)0.3 (0.05)0.22 (0.024)0.19 (0.024)
 Subtotal1.6 (0.23)1.5 (0.27)2.4 (0.79)2.6 (0.53)0.16 (0.040)0.14 (0.005)
Pronators
 PT1.8 (0.17)1.6 (0.16)2.7 (0.45)2.3 (0.32)0.15 (0.013)0.17 (0.017)
 PQ0.3 (0.09)0.4 (0.07)1.0 (0.20)1.3 (0.04)0.07 (0.010)0.08 (0.021)
 Subtotal2.1 (0.26)2.0 (0.15)3.7 (0.63)3.6 (0.32)0.13 (0.009)0.13 (0.010)
Supinator
 Spn1.7 (0.20)1.9 (0.15)3.7 (0.14)4.1 (0.31)0.10 (0.017)0.11 (0.014)
Thenar muscles
 APB0.3 (0.04)0.2 (0.06)0.5 (0.06)0.4 (0.13)0.12 (0.003)0.11 (0.016)
 FPB0.2 (0.06)0.1 (0.04)0.6 (0.03)0.3 (0.12)0.07 (0.022)0.09 (0.013)
 OP0.1 (0.03)0.1 (0.05)0.3 (0.07)0.4 (0.12)0.08 (0.011)0.07 (0.020)
 AP0.5 (0.26)0.3 (0.03)0.9 (0.40)0.7 (0.05)0.11 (0.023)0.12 (0.005)
 Subtotal1.1 (0.31)0.8 (0.08)2.4 (0.38)1.8 (0.17)0.10 (0.016)0.10 (0.011)
Hypothenar muscles
 ADM0.3 (0.06)0.3 (0.06)0.6 (0.20)0.8 (0.19)0.11 (0.014)0.10 (0.011)
 FDMB0.2 (0.03)0.1 (0.03)0.3 (0.03)0.2 (0.05)0.11 (0.012)0.10 (0.016)
 ODM0.1 (0.02)0.1 (0.01)0.6 (0.04)0.6 (0.18)0.04 (0.007)0.05 (0.015)
 Subtotal0.6 (0.05)0.5 (0.08)1.5 (0.21)1.6 (0.32)0.08 (0.005)0.08 (0.009)
Interossei
 DI10.8 (0.10)0.5 (0.06)1.7 (0.43)1.5 (0.21)0.11 (0.016)0.08 (0.005)
 DI20.5 (0.13)0.3 (0.05)1.3 (0.30)1.1 (0.17)0.08 (0.004)0.07 (0.007)
 DI30.3 (0.02)0.2 (0.03)0.7 (0.10)0.8 (0.20)0.08 (0.005)0.07 (0.006)
 DI40.3 (0.01)0.2 (0.04)0.9 (0.06)0.8 (0.21)0.08 (0.006)0.07 (0.012)
 PI10.2 (0.06)0.2 (0.10)0.5 (0.08)0.5 (0.26)0.10 (0.020)0.09 (0.014)
 PI20.2 (0.09)0.2 (0.04)0.4 (0.13)0.4 (0.12)0.09 (0.016)0.09 (0.025)
 PI30.2 (0.06)0.1 (0.02)0.4 (0.06)0.4 (0.13)0.09 (0.018)0.07 (0.007)
 Subtotal2.4 (0.39)1.7 (0.23)5.9 (0.83)5.5 (1.14)0.09 (0.003)0.08 (0.006)
Lumbricales
 L10.1 (0.02)0.1 (0.01)0.1 (0.02)0.1 (0.01)0.28 (0.031)0.29 (0.037)
 L20.1 (0.03)0.1 (0.01)0.1 (0.03)0.1 (0.01)0.29 (0.041)0.34 (0.046)
 L30.1 (0.02)0.1 (0.03)0.07 (0.03)0.04 (0.02)0.30 (0.038)0.34 (0.028)
 L40.05 (0.02)0.04 (0.01)0.04 (0.01)0.02 (0.01)0.26 (0.043)0.35 (0.053)
 Subtotal0.3 (0.09)0.2 (0.04)0.3 (0.09)0.2 (0.03)0.29 (0.020)0.32 (0.036)

We confirmed that the muscle dimensions of the forelimb were essentially similar in both species, as shown in Table 3. However, the statistical analyses showed that there were some significant differences in the mass and PCSA ratios between the orangutans and chimpanzees. The mass and PCSA ratios of the elbow flexors (M. brachialis and M. brachioradialis) were larger in the orangutans, indicating that the orangutans are equipped with larger monoarticular elbow flexors (Table 3). In contrast, the mass ratios of the biarticular muscles in the upper arm (the short head of M. biceps brachii and long head of M. triceps brachii) and M. teres major were larger in the chimpanzees. For the rotator cuff muscles, the PCSA ratio of M. subscapularis was significantly larger in the orangutans, whereas that of M. infraspinatus was larger in the chimpanzees. The PCSA ratios of the wrist and digital II–V extensors tended to be larger in the orangutans, whereas those of the flexors were larger in the chimpanzees, although they were not significantly different. In the intrinsic hand muscles, the mass ratios of the interosseous muscles and the PCSA ratios of the lumbrical muscles were significantly larger in the orangutans.

When the fascicle length was normalized by the upper arm length, the fascicles of the shoulder retractor and digital II–V extensor muscles were longer in the chimpanzees, whereas those of the interosseous muscle were longer in the orangutans (Table 3). Although the differences between the two species were not significant, the digital II–V flexors were slightly longer in the orangutans than in the chimpanzees.

Discussion

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

The present study presents the complete set of muscle parameters for both the orangutan and chimpanzee based on multiple individuals, allowing comparative evaluation of the biomechanical capacity of the forelimb muscles in the two species. In our previous report on the orangutan's muscle dimensions based on a single individual (O3) (Oishi et al. 2008), we suggested that orangutans tend to possess larger PCSA (i.e. force-generating capacity) in the elbow flexors, notably M. brachioradialis, and smaller PCSA in the wrist and the digital II–V flexor muscles than chimpanzees. In this study, such tendencies were confirmed in a larger number of specimens (Table 3).

As preliminarily suggested by our previous study (Oishi et al. 2008) and clearly confirmed by the present study, the monoarticular elbow flexor muscles, M. brachialis and M. brachioradialis, were much larger in the orangutans than in the chimpanzees (Table 3). This tendency was also observed by Payne (2001). We attributed this morphological specialization to arboreal locomotion, such as vertical climbing, and torso-orthograde suspensory locomotion because the elbow flexors are important for weight suspension and progression in trees (see Oishi et al. 2008). In particular, Thorpe & Crompton (2006) suggested, based on their complete orangutan positional behavior dataset, that it is the presence of pronograde suspensory posture and locomotion that distinguishes the orangutan from the African apes. Such differences in locomotion might be functionally aligned to the above morphological specialization in the elbow muscles.

Furthermore, the present study demonstrated that the brachial biarticular muscles, namely the long head of M. triceps brachii and the short head of M. biceps brachii, had relatively smaller mass ratios in the orangutans than in the chimpanzees (Table 3). Electromyographic studies of forelimb muscles during knuckle-walking in chimpanzees suggested that the M. triceps brachii is active during the stance phase to retract the humerus while maintaining the elbow joint in extension for vaulting the body over it (Tuttle et al. 1983). Although this activity was reported to be modest during horizontal knuckle-walking in an experimental setting, the activity tended to be much increased in the natural environments, as the electromyographic activity increases when the chimpanzees walk up and down a slope (Tuttle et al. 1983). Therefore, the large M. triceps brachii seems to enhance terrestrial locomotion in the chimpanzee, which actually travels more frequently on the ground.

However, what is enigmatic is that M. biceps brachii, the antagonistic muscle of M. triceps brachii, was also relatively larger in the chimpanzees, despite the fact that its synergistic muscles, M. brachialis and M. brachioradialis (Tuttle et al. 1983; Tuttle & Cortright, 1988), were larger in the orangutans (Table 3). The explanation for this is obscure but it might be linked to a difference in the speed of movements. For example, when apes climb vertically, they lift the body load by simultaneous shoulder retraction and elbow flexion (Tuttle et al. 1983; Larson & Stern, 1986). In such circumstances, the shortening velocity of M. biceps brachii is lower than that of the elbow flexors because of the concurrent joint movements. The force-generating capacity of a muscle is known to be affected by its shortening velocity; the faster the shortening velocity, the lower the force that it can exert (Nigg & Herzog, 1999). Therefore, the biarticular muscle is more capable of generating force in such movements due to the force–velocity relationship, especially when the movements are fast (van Ingen-Schenau et al. 1990). A monoarticular muscle could be less effective in this regard but joints can be actuated independently. Locomotion of the chimpanzees seems to be quite fast both on the ground and in arboreal settings, whereas that of the orangutans is known to be very slow and cautious (Isler, 2005). This difference in the speed of locomotion might be functionally linked to the difference in the ratio between the mono- and biarticular elbow flexor muscles between the orangutans and chimpanzees. However, it has recently been pointed out that orangutans are actually capable of fast and acrobatic locomotion, despite the fact that they are generally considered cautious, slow climbers (Thorpe & Crompton, 2006). Furthermore, biarticular muscles are also considered to be functionally important for generating favorable energy transfer among the segments by producing moments around the two joints simultaneously, especially in explosive movements such as jumping (e.g. Gregoire et al. 1984; van Soest et al, 1993), and favorable endpoint force that is different from corresponding uniarticular muscles (e.g. Hof, 2001; Ogihara et al. 2009). The actions of biarticular muscles are complex and perplexing. Further biomechanical studies are needed to better clarify the functional meaning of this difference in muscle dimensions.

Another interesting finding of the present study is that the force-generating capacity of M. subscapularis was significantly larger in orangutans, whereas the opposite rotator cuff muscle, M. infraspinatus, was larger in chimpanzees (Table 3). As a consequence, the PCSA ratio of the M. subscapularis is more balanced with the PCSA ratios of M. infraspinatus and M. supraspinatus in orangutans but the latter are much greater in chimpanzees. Electromyographic data by Larson & Stern (1986, 1987) showed that the three rotator cuff muscles are all active during vertical climbing in the chimpanzee (M. subscapularis is highly active in the support phase, and M. infraspinatus and M. supraspinatus are active in the swing phase) but, during knuckle-walking, M. subscapularis is not significantly active, although the other two muscles are. Therefore, the morphology of the rotator cuff muscles also seems to be functionally specialized for terrestrial adaptation in the chimpanzee.

In our previous work, we suggested that the fascicles of the wrist and the digital II–V flexor muscles were longer in the orangutans, resulting in relatively small PCSA ratios (Oishi et al. 2008). Although the same tendency was observed in the present study, the differences in the fascicle lengths normalized by the upper arm length of these muscle groups between the two species were not significant (Table 3). These findings indicate that our previous suggestion was not supported by a larger number of cases due to considerable individual variability. The present study demonstrated that multiple individuals must be studied to compare patterns of muscle dimensions among different species, despite the fact that such opportunities are usually very limited.

In this study, the mass and PCSA ratios were compared to clarify interspecies variations in the forelimb muscle morphology between orangutans and chimpanzees; however, the mass and PCSA of each muscle were not normalized by body mass and (body mass)0.667, respectively, assuming a geometric similarity as in other similar studies (e.g. Thorpe et al. 1999; Payne, 2001; Carlson, 2006; Payne et al. 2006). The main reason for this was that body mass was not available for every specimen used but another reason was that the body mass of the same skeletal dimension could be highly variable due to such factors as obesity, aging and nutritional status and may not be always suitable as a baseline. However, our interspecies comparisons based on the ratios certainly do not allow one to determine which muscles are absolutely larger in orangutans and vice versa when corrected for body size. For example, our data do not suggest that the brachial biarticular muscles are absolutely smaller in the orangutan than in the chimpanzee of the same body weight. Comparing muscle parameters of two different animals is difficult. Care must be taken in the interpretation of the present results and comparisons with other data.

Conclusions

The present study presented a complete dataset on the forelimb musculature of the orangutan and chimpanzee based on careful dissection of eight forelimbs of three orangutans and four chimpanzees. We found that the mass and PCSA ratios of the elbow flexors were significantly larger in the orangutans. In contrast, the mass ratios of the biarticular muscles in the upper arm were significantly larger in the chimpanzees. For the rotator cuff muscles, the force-generating capacity of M. subscapularis was significantly larger in the orangutans, whereas the opposite rotator cuff muscle, M. infraspinatus, was larger in the chimpanzees. These results provide important insights for understanding the function of the forelimb musculature and its relationship to locomotion in orangutans and chimpanzees.

Acknowledgements

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

The authors would like to thank Dr S. Kawada of the Department of Zoology, National Science Museum, and all the staff of Tama Zoological Park, Nogeyama Zoo, Higashiyama Zoo and Botanical Gardens, Chausuyama Zoo, Yagiyama Zoological Garden, Yamajiboku and the Primate Research Institute of Kyoto University for kindly allowing us to dissect the specimens. The authors also thank Dr N. Kuze for providing us with useful information on positional behavior in orangutans. This study was partly supported by the Cooperation Research Program of the Primate Research Institute, Kyoto University, the JSPS core-to-core program HOPE and a Grant-in-Aid for Scientific Research on Priority Areas ‘Emergence of Adaptive Motor Function through Interaction between Body, Brain and Environment’ from the Japanese Ministry of Education, Culture, Sports, Science and Technology.

References

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References