Functional anatomy of the gibbon forelimb: adaptations to a brachiating lifestyle

Authors

  • Fana Michilsens,

    1. Laboratory for Functional Morphology, University of Antwerp, Belgium
    2. Centre for Research and Conservation, Royal Zoological Society of Antwerp, Belgium
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  • Evie E. Vereecke,

    1. Laboratory for Functional Morphology, University of Antwerp, Belgium
    2. Department of Human Anatomy and Cell Biology, School of Biomedical Sciences, University of Liverpool, UK
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  • Kristiaan D'Août,

    1. Laboratory for Functional Morphology, University of Antwerp, Belgium
    2. Centre for Research and Conservation, Royal Zoological Society of Antwerp, Belgium
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  • Peter Aerts

    1. Laboratory for Functional Morphology, University of Antwerp, Belgium
    2. Department of Movement and Sport Sciences, University of Ghent, Belgium
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Fana Michilsens, Laboratory for Functional Morphology, University of Antwerp, CDE – Universiteitsplein 1 – 2610 Wilrijk, Belgium. E: fana.michilsens@ua.ac.be

Abstract

It has been shown that gibbons are able to brachiate with very low mechanical costs. The conversion of muscle activity into smooth, purposeful movement of the limb depends on the morphometry of muscles and their mechanical action on the skeleton. Despite the gibbon's reputation for excellence in brachiation, little information is available regarding either its gross musculoskeletal anatomy or its more detailed muscle–tendon architecture. We provide quantitative anatomical data on the muscle–tendon architecture (muscle mass, physiological cross-sectional area, fascicle length and tendon length) of the forelimb of four gibbon species, collected by detailed dissections of unfixed cadavers. Data are compared between different gibbon species and with similar published data of non-brachiating primates such as macaques, chimpanzees and humans. No quantitative differences are found between the studied gibbon species. Both their forelimb anatomy and muscle dimensions are comparable when normalized to the same body mass. Gibbons have shoulder flexors, extensors, rotator muscles and elbow flexors with a high power or work-generating capacity and their wrist flexors have a high force-generating capacity. Compared with other primates, the elbow flexors of gibbons are particularly powerful, suggesting that these muscles are particularly important for a brachiating lifestyle. Based on this anatomical study, the shoulder flexors, extensors, rotator muscles, elbow flexors and wrist flexors are expected to contribute the most to brachiation.

Introduction

Gibbons and siamangs (Fam. Hylobatidae) are skilled brachiators and are known for the dominant use of this locomotor mode during travelling (50–80% of their travelling time) (Fleagle, 1974, 1976; Andrews & Groves, 1976; Carpenter, 1976; Hollihn, 1984; Preuschoft & Demes, 1984; Tuttle, 1986; Takahashi, 1990). The definition of brachiation given by Hollihn (1984) is widely accepted and states that brachiation is ‘bimanual progression along or between overhead structures for a distance of several metres without the intermittent use of other types of positional behaviour and without support by the hind limbs or tail’. According to this definition, the hylobatids are the only true brachiators. Although some work has been done on the anatomical characteristics of brachiators (Tuttle, 1972; Schultz, 1973; Andrews & Groves, 1976; Fleagle, 1979, 1999; Hollihn, 1984; Swartz et al. 1989; Takahashi, 1990; Chan, 2007) and the mechanics of brachiation (Fleagle, 1976; Chang et al. 1997; Bertram et al. 1999; Chang et al. 2000; Bertram & Chang, 2001; Usherwood et al. 2003; Gomes & Ruina, 2005), these studies almost never engaged in extensively linking anatomical findings to observed movements (except some electromyographic studies of specific muscles; Stern et al. 1980; Jungers & Stern, 1981; Susman et al. 1982; Stern & Larson, 2001) and, to our knowledge, no study ever provided functional muscle characteristics [muscle masses, physiological cross-sectional areas (PCSAs) and fascicle lengths (FLs)] of the gibbon forelimb.

The aim of this study was therefore to quantify forelimb muscle architecture in gibbons, discuss the findings in relationship to their locomotor habits and compare them with other primates, more specifically non-brachiators (e.g. humans), semi-brachiators (e.g. Ateles) and so-called ‘modified’ brachiators (e.g. chimpanzees). [Napier & Napier (1967) introduced this term to refer to a form of arboreal locomotion in which the forelimbs play a major role in suspending the body or propelling it through space; this does not make any implications about the amount of time spent moving around in that way or about the biomechanical adaptations towards this locomotor mode.]

Apart from providing a detailed account of the functional anatomy of the gibbon forelimb, such data are a necessary input for biomechanical modelling (inverse and forward dynamics) and computer simulations. As such, they are crucial to advance our knowledge of the biomechanics of brachiation. We do not intend to provide a detailed comparison of functional forelimb anatomy among primates or to provide an extensive interspecific comparison within gibbons. Our primary goal was to provide a general functional analysis of the gibbon forelimb. However, due to the composition of our sample (different species and genera) it was necessary to investigate if interspecific differences in musculature exist. Eventually, we are interested in the distinct anatomical features of gibbons that might help to explain their excellent brachiating skills.

Assessing an animal's functional muscular anatomy can be done by analysing four basic parameters: muscle mass, muscle PCSA, muscle FL and tendon length (TL) (Thorpe et al. 1999). The PCSA gives information about the force-generating capacity of the muscle because a high PCSA is associated with a large number of sarcomeres lying in parallel. The FL, however, reflects the number of sarcomeres lying in series and is proportional to the possibility of the muscle generating force over a wider range of motion and to the shortening velocity of the muscle (it should be kept in mind that the resultant kinematics also depend on muscle fibre type and moment arm) (Thorpe et al. 1999; Payne et al. 2006). Muscles that have equal volumes will have a similar capacity for power generation, as power is force × velocity and is therefore directly related to muscle volume (Zajac, 1992; Payne et al. 2006). As muscle volume is proportional to muscle mass, this parameter gives a first estimate of the power-producing capacity of a muscle. Obviously, the presence of a tendon can also have an important influence on the function of a muscle–tendon unit (MTU) (Anapol & Gray, 2003). Muscles with long tendons, i.e. a high TL : MTU ratio, may be able to contract nearly isometrically (Biewener, 1998; Alexander 2002; Roberts, 2002), leading to a low shortening velocity of the muscle fibres and hence a high force production (due to the force–velocity relationship; Hill, 1953). In addition, long tendons might be able to store elastic strain energy that can be released in a following cycle (Alexander, 2002). A low TL : MTU ratio means that there will be an isotonic contraction in which all shortening will happen in the muscle belly itself. In this case, contraction is possible at a high speed but not at maximal force production because the muscle fibres will typically not be operating at maximal myofilament overlap (Anapol & Gray, 2003).

The muscle characteristics mentioned above are linked with the locomotor behaviour of the animal. Previous studies have already pointed to some particular characteristics in the forelimb musculature of highly suspensory primates: large digital flexor muscles (Tuttle, 1972), a large supinator muscle (brachiating compared with non-brachiating species; Tuttle, 1972) and large lattissimus dorsi and teres major muscles (Fleagle, 1979). Thorpe et al. (1999) demonstrated that, because of their arboreal lifestyle, chimpanzees have relatively stronger elbow and wrist flexors than humans and mechanical studies of gibbon brachiation also indicated that the supporting arm is commonly flexed to hoist the body and optimize the arm-swinging movement (Fleagle, 1979; Stern et al. 1980; Jungers & Stern, 1981; Turnquist et al. 1999; Usherwood et al. 2003; Usherwood & Bertram, 2003). Although posture and other habits (e.g. feeding) also influence the general anatomy, it is commonly accepted that the animal's muscle anatomy is largely shaped by its locomotor mode due to the high frequency and high loads involved (and hence strong selective pressure) (Fleagle, 1979). Based on this information and knowing that gibbons are highly arboreal and brachiate for more than 50% of their active time (Fleagle, 1976), we expect that the gibbon forelimb will be characterized by elbow and wrist flexors with a high force-generating capacity (high PCSAs). We also expect that the wrist/digital flexors will be coupled to long tendons, enabling isometric contraction and thus maximal force production while having the opportunity to store strain energy in their tendons. The storage and release of elastic energy can contribute to smaller energy expenditure during the locomotion cycle (cf. running according to the spring-mass model in humans; Cavagna et al. 1977). The shoulder muscles, however, should be capable of acting over a wide range of motion and we therefore expect that the shoulder musculature will be characterized by long FLs. Equally important is stabilization of the shoulder joint in all possible positions and during rapid locomotion with high loads. The shoulder, as an inherently mobile joint, depends largely on the muscles and tendons for its stabilization. The muscles responsible for stabilizing the shoulder are expected to be pennate muscles that run close to the joint with short, firm tendons.

Materials and methods

Subject data

Three adult lar gibbons (Hylobates lar), two pileated gibbons (H. pileatus), two moloch gibbons (H. moloch) and four siamangs (Symphalangus syndactylus) of known age and sex were dissected (Table 1). All specimens died under natural circumstances and showed no obvious musculoskeletal pathology. Cadavers were obtained from the National Museums of Scotland, Edinburgh (NMS) and from the Royal Zoological Society of Antwerp. The specimens were eviscerated during post-mortem examination and kept frozen (–18 °C) until required for the analysis. All dissections were conducted on unfixed material that had been defrosted at room temperature or in the fridge. The body mass of each subject was obtained prior to evisceration and was used for normalization of data (Table 1). For Moloch 2 and Pileated 2, however, no pre-evisceration mass was available. For these specimens it was assumed that the ratio of forelimb muscle mass to total body mass was similar to that of the other specimen of the same species. For each specimen, the right forelimb was used to collect data on muscle architecture, whereas the left forelimb was left intact for further measurements.

Table 1.   Subject data
 Lar 1Lar 2Lar 3Pileated 1Pileated 2Moloch 1Moloch 2Siamang 1Siamang 2Siamang 3Siamang 4
  • M, male; F, female; RZSA, Royal Zoological Society of Antwerp; NMS, National Museum of Scotland; Pld, Planckendael Animal Park, B; P, Paignton Zoo, UK; T, Twycross Zoo, UK; PL, Port Lympe, UK; A, Antwerp Zoo, B.

  • *

    Estimated values.

SexMMFMFMMFFFM
Age at death (years)62621.84124.519Adult32935Adult
Mass (kg)6.310.6 6.55.2 6.7* 5.87.3*12.478.511.5510.1
OriginPldUnknownPldPTPLUnknownATTPL
CollectionRZSANMSRZSANMSNMSNMSNMSRZSANMSNMSNMS

The forelimb musculature of gibbons was compared with other primates for which data were available from the literature. For the evaluation of interspecific variation in origin and insertion, we included atelines (Youlatos, 2000) as an example of semi-brachiators, bonobos (Pan paniscus; Miller, 1952) as ‘modified’ brachiators and macaques (Macaca irus; Kimura & Takai, 1970) and humans (Gray, 1918) as non-brachiators. For the comparison of muscle dimensions, we used common chimpanzees (P. troglodytes; Thorpe et al. 1999) as an example of ‘modified’ brachiators and macaques (M. mulatta and M. fascicularis; Cheng & Scott, 2000) and humans as non-brachiators (Thorpe et al. 1999).

Measurement of forelimb muscle dimensions

During the dissection of each right forelimb, muscles were removed systematically and measurements of muscle mass, MTU, muscle belly and TL were recorded, as well as the origin, insertion and inferred function of each muscle. Masses were measured with an electronic scale (Radwag, Poland) to the nearest 0.1 g and lengths were measured with digital calipers (Mitutoyo, Japan) to the nearest 0.01 mm. Each muscle was then cut along the line of the tendon to determine the arrangement of muscle fascicles. Three separate measurements of muscle FL were recorded from different sections of the muscle belly and a mean value was calculated. A photograph was taken with a digital camera to determine the pennation angle, i.e. the angle between internal tendon and muscle fascicles (to improve accuracy, care was taken to place the camera lens parallel to the plane of the muscle). The TL was measured as comprising both the external and internal portion of the tendon; after this the external tendon was removed to measure the muscle belly mass. When possible, a sample of the external tendon was measured and weighed to determine the tendon cross-sectional area (TCSA) (see below). Note that the specimens obtained from NMS were skinned by a taxidermist of the NMS prior to transportation to our laboratory. As a result, the phalanges were removed and the distal parts of the tendons inserting onto the digits were cut off. The TLs and MTUs of flexor digitorum superficialis (FDS), flexor digitorum profundus (FDP), extensor digitorum communis (EDC), extensor digitorum brevis (EDB), extensor digiti minimi (EDM) and extensor pollicis longus (EPL) of these specimens were therefore omitted from our calculations (see Table 2 for abbreviations of muscle names).

Table 2.   Abbreviations of measured arm muscles
MuscleCode
Abductor pollicis longusAPL
Biceps brachiiB
BrachialisBra
BrachioradialisBR
CoracobrachialisCB
DeltoidD
DorsoepitrochlearisDET
Extensor carpi radialis brevisECRB
Extensor carpi radialis longusECRL
Extensor carpi ulnarisECU
Extensor digiti minimiEDM
Extensor digitorum brevisEDB
Extensor digitorum communisEDC
Extensor pollicis brevisEPB
Extensor pollicis longusEPL
Flexor carpi radialisFCR
Flexor carpi ulnarisFCU
Flexor digitorum profundusFDP
Flexor digitorum superficialisFDS
InfraspinatusIS
Latissimus dorsiLD
Levator scapulaeLS
Palmaris longusPalm
Pars superior seratus anteriorSPSA
Pectoralis majorPmaj
Pectoralis minorPmin
Pronator quadratusPQ
Pronator teresPT
RhomboidRh
Rhomboid minorRmin
Serratus anteriorSerr
SubscapularisSSc
SupinatorSup
SupraspinatusSS
Teres majorTmaj
Teres minorTmin
TrapeziusTrap
Triceps brachiiTr

Calculation of anatomical parameters

The PSCA of the muscle can be estimated as follows:

image((eqn 1))

where m is muscle belly mass (in kg), ρ is muscle density (1.06*103 kg m−3; Mendez & Keys, 1960) and FL is average muscle FL (in m). The PCSA calculated in this way is directly related to the force-generating capacity of all muscle fibres (maximal isometric force or Fmax). However, in pennate muscles, only a component of the fibre force (proportional to the cosine of the pennation angle θ) is transmitted to the tendon. Correction for this effect results in

image((eqn 2))

where θ is the angle of pennation with respect to the line of pull of the muscle. The pennation angle was included in all of our estimates of PCSA, even when angles were small (i.e. close to parallel fibred). To obtain an estimate of Fmax, PCSA (in m2) is multiplied by 0.3 MPa [maximal isometric stress of a vertebrate muscle (Wells, 1965; Medler, 2002); note that gibbon-specific data are not available].

The TCSA was calculated in a similar way as in eqn 1; the tendon sample volume (m3) was determined by dividing tendon sample mass by tendon density (1.12*103 kg m−3; Ker et al. 1988). This value was then divided by tendon sample length to acquire TCSA. The total TL over MTU length was calculated as a relative value of TL. Although both tendons at origin and insertion were measured, only the data of insertion tendons were included in our analysis, due to the small number of muscles with origin tendons.

Finally, the stress in life (SIL) (in MPa) was calculated by dividing Fmax (i.e. PCSA × 0.3 MPa) by TCSA and used as a measurement of the stress in a tendon while the muscle is exerting maximum isometric force, Fmax (Ker et al. 2000).

Interspecific comparison

To allow comparison between specimens of varying size (body mass range, 5.2–12.5 kg) and with other primate species, the data were normalized assuming geometric similarity (cf. Alexander et al. 1981; Thorpe et al. 1999; Payne et al. 2006). Masses were scaled to body mass, lengths to (body mass)1/3 and areas to (body mass)2/3. Muscles were grouped in functional categories, which are given in Table 3. The movements affected by the functional muscle groups of the shoulder are movements of the humerus relative to trunk and are shown in Fig. 1, with flexion/extension taking place in the sagittal plane, abduction/adduction in the frontal plane and endorotation/exorotation in the transversal plane. The functional groups of elbow and wrist muscles follow the classical convention of movements at those joints (flexion/extension and pronation/supination in the elbow and palmarflexion/dorsiflexion and ulnar/radial deviation at the wrist) and the scapular muscles are muscles that affect the movement of the scapula. For each functional muscle group the sum of the separate muscle PCSA and mass was taken to result in one value for each muscle group in each individual. The FL was averaged between the containing muscles of that group. Consequently the values (PCSA, mass and FL) were normalized geometrically to the average bodyweight of our gibbons (see above) and finally an average was taken to result in one PCSA, one muscle mass and one FL value for each functional muscle group in each species.

Table 3.   Functional categories of dissected muscles
ShoulderElbowWristScapular muscles
  • *

    Muscles that were used to compare to chimpanzee, human and macaque data as in Thorpe et al. (1999).

FlexorsFlexorsPalmar flexors 
PmajB*FDS*Trap
DBra*FDP*Serr
BBR*FCU*SPSA
CBPTFCR*Rh
 FCRAPLRmin
 PalmPalmLS
 FDSEPB 
 FCU  
ExtensorsExtensorsDorsal flexors 
TrTr*EDC 
Tmaj ECRL* 
LD ECRB* 
D ECU* 
  EPL 
  EDB* 
  EDM 
AbductorsSupinatorsUlnar deviation 
DBECU 
SSSupFCU 
 BREDM 
AdductorsPronatorsRadial deviation 
PmajPQECRL 
CBPTECRB 
TmajBRAPL 
LD EPL 
  FCR 
Endorotators   
SSc   
Pmaj   
D   
Tmaj   
LD   
Exorotators   
IS   
Tmin   
D   
Figure 1.

 Definition of different shoulder movements.

All measured forelimb muscles were included in the analysis of the gibbon data but, for the comparative analysis (with chimpanzees, macaques and humans), only forelimb muscles that were also measured in Thorpe et al. (1999) were included in the comparison of the different primate species (see Table 3). Primates used for quantitative anatomical comparison were: chimpanzee (Chimp 95 from Thorpe et al. 1999), human (scaled to 50 kg; Thorpe et al. 1999) and macaques (M. mulatta and M. fascicularis; from Cheng & Scott, 2000), all scaled to the average measured gibbon body mass (7.7 kg).

Results

Forelimb muscle anatomy

In general, the forelimb musculature of gibbons has a similar organization as that of other primates and only a couple of differences were observed between the forelimb musculature of gibbons and that of various other primate species with distinct locomotor repertoires. The origin and insertion of all forelimb muscles, together with observed variations, are presented in Appendix B.

Of the observed differences, the most remarkable is that, in gibbons, the short head of the biceps is monoarticular, whereas it is biarticular in most primates. In gibbons, the short head originates from the lesser tubercle of the humerus, whereas it originates from the coracoid process of the scapula in humans (Gray, 1918) and other primates (Miller, 1952; Kimura & Takai 1970; Youlatos 2000). As a result, only the long head of the biceps (originating from the supraglenoid) crosses the glenohumeral joint in gibbons.

Also important to note is that we found no anconeus lateralis muscle in any of our gibbon specimens, leaving the triceps as the only elbow extensor in gibbons.

In addition, some clear variations in origin or insertion were found for brachioradialis (BR), APL, flexor digitorum profundus (FDP) and the supinator muscle (Sup) (Appendix B). The BR originates from the lateral supracondylar ridge but its insertion differs among primates. In humans, and occasionally also in siamangs, it inserts on the styloid process of the radius (Gray, 1918), whereas in bonobos, crab-eating monkeys and (most) siamangs its insertion has shifted proximally on the radial shaft and in other gibbons even to the mid-radius. The APL shows some minor variations in both origin and insertion. The origin varies between the proximal part of the radius and ulna in gibbons, to the middle part in crab-eating monkeys, bonobos and humans. Although the insertion is mostly found on the base of metacarpal 1, it can also insert onto the trapezium (some siamangs and bonobos) or even to the sesamoid bones of the pollex (crab-eating monkeys). For the FDP, we noted substantial interindividual variation (within our gibbon sample) in fusion of the digital tendons and/or muscle bellies, with most variation occurring within the siamangs.

Like monkeys and most apes (Howell & Straus, 1961), gibbons possess a dorso-epitrochlearis muscle that connects the latissimus dorsi to the short head of the biceps. However, in some gibbon specimens this muscle has not only a fleshy insertion on the short head of the biceps but also inserts via a narrow tendon on the medial epicondyle of the humerus, a feature also seen in other non-human primates (bonobos: Miller, 1952; atelines: Youlatos, 2000). In humans, this muscle is reduced to fascia (Kimura & Takai, 1970; Aiello & Dean, 1990).

Within our gibbon sample some individual variation in muscle courses was observed (see above) but we did not find any consistent differences in origin and insertion of forelimb muscles between the genus Symphalangus (siamangs) and Hylobates or between the different gibbon species (Appendix B). [Note that when we mention gibbons in general, we refer to all four measured species, including siamangs.] Overall, muscles in the forearm display a remarkably high degree of fusion of muscle bellies (e.g. FDS, FDP and APL + EPL) as well as tendons (e.g. EDC and EDM + ECU). In addition, shoulder, elbow and wrist muscles are linked, forming a proximo-distal muscle chain comprising LD, DET, B and FCR/Palm (Jungers & Stern, 1980).

Forelimb muscle dimensions

Below, we present the muscle mass, PCSA, FL and tendon characteristics of the forelimb muscles of the four gibbon species studied. Unless stated otherwise, values given are always interspecies mean (i.e. mean of the four species means + SD) and scaled to the average measured body mass of 7.7 kg. The mean values of each muscle for each species can be found in Appendix A.

Muscle mass

The unilateral forelimb muscle mass accounts on average for 8.2 ± 0.8% (mean ± SD) of the average body mass of gibbons, corresponding to ca. 641 g of muscles per forelimb. The greatest part (57 ± 0.5%) of the forelimb muscle mass consists of muscles that cross the shoulder (glenohumeral joint) (Fig. 2). Within these shoulder muscles, 50 ± 1.5% of the muscle mass contributes to extension and 48 ± 1.4% to flexion, indicating that a large part of the muscles in the shoulder are those for lowering and lifting the arm in the sagittal plane (extensors and flexors, respectively). However, most of these muscles also contribute to endorotation (42 ± 0.6%), exorotation (36 ± 2.1%) and adduction (40 ± 1.8%). Only abductor muscles (for lifting the arm in the frontal plane) form a smaller share of the shoulder musculature (18 ± 0.7%). In the elbow and wrist, the flexors are the dominant group (78 ± 2.2% and 81 ± 2.6% of the elbow and wrist muscle masses, respectively) and together they make up more than one-third (35 ± 1.3%) of the total forelimb musculature. A similar forelimb muscle mass distribution is found for each of the four gibbon species.

Figure 2.

 Relative muscle mass distribution in an average gibbon forelimb. (Note that because of biarticular muscles, the total adds up to more than 100%.)

Physiological cross-sectional area

The deltoid (D) has on average the largest PCSA (10.67 ± 2.28 cm2) and hence the highest force-producing capacity of all forelimb muscles (Fmax = 326 N), followed by the triceps (8.48 ± 1.17 cm2) and the flexor digitorum profundus and superficialis muscles (FDP, 8.19 ± 1.85 cm2; FDS, 7.41 ± 1.48 cm2). The pectoralis major, latissimus dorsi and biceps are exceptionally large in pileated gibbons compared with other gibbons, whereas lar gibbons have larger trapezius, deltoid and supinator muscles (see Appendix A for values). It is also remarkable that both lar and pileated gibbons have relatively larger deeper digital flexors (lar: FDP, 10.15 cm2, FDS, 6.68 cm2; pileated: FDP, 9.19 cm2, FDS, 5.71 cm2), whereas moloch gibbons and siamangs have relatively larger superficial digital flexors (moloch: FDP, 5.98 cm2, FDS, 8.93 cm2; siamang: FDP, 7.45 cm2, FDS, 8.33 cm2). Of the total PCSA of all forelimb muscles, 51% (53.94 cm2) is situated in the shoulder musculature, 38% (40.09 cm2) is situated in the elbow, 27% (28.48 cm2) in the wrist musculature and 9% (6.04 cm2) is formed by the scapular muscles. Although there is some variation among gibbon species, the general pattern is the same (Fig. 3a). The PCSA of the functional muscle groups shows that the elbow and wrist musculature have a clear dominance for flexion (flexors constitute 71% of the elbow musculature and 81% of the wrist musculature) (Fig. 3a). In the shoulder, the extensors are the group with the largest PCSA (27.31 cm or 50% of the shoulder musculature), closely followed by the endorotators (24.56 cm2 or 43 ± 4%), flexors (23.2 cm2 or 40 ± 3%) and exorotators (19.54 cm2 or 36 ± 4%). Both abductors and adductors form a smaller part of the total shoulder PCSA (13.73 cm2 or 25 ± 2% and 13.08 cm2 or 24 ± 4%, respectively).

Figure 3.

 (a) Total physiological cross-sectional area (PCSA), (b) average fascicle length and (c) average tendon length [relative to muscle–tendon unit (MTU)] of each functional muscle group of the forelimb averaged for each of the four measured gibbon species and normalized to the average measured gibbon weight. Error bars show mean + SD. [In (c) only those muscles are used that have insertion tendons.]

Fascicle length

On average, the latissimus dorsi (LD) has the longest muscle fascicles (mean FL, 138.46 ± 11.24 mm). [See Appendix A for values of separate muscles for each species.] The elbow supinators (FL, 66.50 mm), scapular muscles (FL, 63.53 mm) and shoulder adductors (FL, 80.10 mm) all have long muscle fascicles (Fig. 3b). In the wrist, the FL is low compared with more proximally located forelimb muscles. Although some minor differences were observed, the overall pattern of the FL of the functional muscle groups is similar across the four gibbon species.

Tendon length and stress in life

Tendons are prominent in most muscles of the gibbon forelimb but are particularly extensive in muscles crossing the wrist joint. Figure 3cshows the relative (insertion) TL (TL : MTU) for each functional muscle group. Only muscles for which tendon data are available are included; data of FDS, FDP, EDC, EDB, EDM and EPL tendons are omitted as these tendons were incomplete in most of our specimens (see Materials and methods). The longest tendons (relative to muscle belly length) are found in the muscles that cross the wrist muscles, in particular in the flexor and ulnar and radial deviator groups (Fig. 3c). The shoulder muscles, especially the adductors, have the shortest tendons.

The SIL, an estimate of the stress in a tendon while the muscle is exerting maximum isometric stress (Ker et al. 2000), is largest for the tendons of the elbow and wrist/digital flexors (B and FDS) (Fig. 4). Lar gibbons also have a particularly high SIL for tendons of the EPL, EPB and APL, whereas pileated gibbons have high SILs in the tendons of FCR and EDB. For most tendons, siamangs have relatively lower SIL values; however, it should be noted that this parameter presents substantial inter- and intraspecific variation.

Figure 4.

 Average stress in life (SIL) for those muscles that have insertion tendons and for which the tendon cross-sectional area (TCSA) could be determined for each of the four measured gibbon species and normalized to the average measured gibbon weight.

Discussion

Are there anatomical adaptations to a brachiating lifestyle?

In this study, gibbons, as specialized brachiators, were compared with ‘modified’ brachiators (bonobo and chimpanzee), New World semi-brachiators (atelines) and non-brachiators (crab-eating monkeys, humans and macaques). Although the locomotor anatomy of gibbons is qualitatively similar to the anatomy of great apes (Swindler & Wood, 1973), the highly suspensory mode of locomotion of gibbons has contributed to some specialized anatomical features (e.g. well-developed scapular spine, long forearms relative to both humerus and body size, and radii that are thicker sagittally than transversely) (Takahashi, 1990). Other features are, to some extent, also found in atelines (e.g. axially elongated scapulae and curvature of the clavicle) (Takahashi, 1990; Voisin, 2006) because they also frequently arm-swing, although in a different way to gibbons (assisted by the prehensile tail).

A remarkable difference between gibbons and other primates is the site of origin of the short head of the biceps brachii. Whereas it originates on the coracoid process of the scapula in most primates, the short head of the biceps originates from the lesser tubercle of the humerus in gibbons. Therefore, whereas in most primates both the long head and the short head of the biceps run over the shoulder, giving the entire muscle a biarticular function (crossing shoulder and elbow joint), in gibbons only the long head crosses the shoulder and thus works biarticularly, whereas the short head works only at the elbow. Because of this, the biceps brachii in gibbons might have a reduced flexion capacity in the shoulder, as only the long head can work at shoulder level, although this apparently reduced capacity could be compensated by an increase in PCSA of the biceps in gibbons compared with other primates. Moreover, despite the fact that Miller (1932) proclaims that there can be doubling of one of the heads of the biceps in gibbons and ‘modified’ brachiators, we observed two biceps heads in all of our gibbon specimens and in one siamang specimen (Siamang 1) the biceps was not two-headed but rather fused to a single muscle head. Fusion of arm muscles was frequently observed in our gibbon specimens. Fusion mainly occurred within and between the muscle bellies of FDS and FDP and between the muscle bellies of APL and EPL. The different tendons of EDC showed fusion as well as the tendons of EDM with the tendons of ECU. We also observed two muscle chains running from the shoulder to the digital muscles, as described by Jungers & Stern (1980). The dorsal muscle chain is formed by fusion of the latissimus dorsi, dorso-epitrochlearis, biceps short head (Bsh) and flexor digitorum superficialis (FDS), whereas the ventral chain consists of the pectoralis major, Bsh and FDS. These chains have long been thought to have a force-transmitting function from shoulder to fingertips (Andrews & Groves, 1976) but have been shown by Jungers & Stern (1980) to be only a morphological consequence of the rearrangement of the origin of the short head of the biceps. Although the flexion function of the biceps at the shoulder is probably reduced by the shift in origin of the Bsh, the leverage for elbow flexion is improved due to an increased insertion area (coracoid process vs. lesser tubercle and midshaft humerus; Jungers & Stern, 1980). This is advantageous for brachiation, where the arms are used to hoist the body by extending the arm at the shoulder and flexing it at the elbow. Although those chains do not seem to have an obvious force conductive function from proximal to distal, or show phasic simultaneity during brachiation (electromyographic study of Jungers & Stern, 1980), it is possible that the fusion of muscle bellies and tendons in the forearm contributes to an increased concerted action of different muscles (fusion can be seen as two muscles working together as one more powerful muscle). However, it might lead to less accurate finger movements, and hence manipulation skills, due to the loss of separate muscle activation. These less accurate movements (personal observation, but see Prime & Ford, 2006) may also be a consequence of the fact that gibbons do not have separate digital extensors like macaques (all digits separately) and bonobos (to digits 1, 2 and 5) (Miller, 1952; Kimura & Takai, 1970) but gibbons do have an EDM to the fifth phalanx, an APL to the thumb and an EDB that can have tendons to digits 2–4 (Appendix B). Therefore, they will have no problem in moving their little finger or thumb separately but the three middle fingers will move mostly simultaneously. Another muscle that is missing in gibbons is the anconeus lateralis muscle [absent in all of our specimens but Gibbs et al. (2002) mention the presence of this muscle in gibbons], a prominent elbow extensor (part of the triceps complex) that is present in humans and bonobos and also in macaques (Gray, 1918; Miller, 1952; Kimura & Takai, 1970). Therefore, although gibbons have multiple elbow flexors (biceps, brachialis and brachioradialis), only the triceps works as an extensor of the elbow and even though the triceps has one of the largest PCSAs, it is not able to match the PCSA of its antagonists, the elbow flexors.

Gibbon muscle dimensions: the key to efficient brachiation?

Our results clearly indicate that there is a proximal to distal distribution of muscle mass in the gibbon forelimb (Fig. 2), with the heaviest muscle groups near the body and long tendons running to the fingers. Although all primates (and even most mammals) show this kind of muscle distribution, the pattern is exaggerated in gibbons as they are the only ones that have a long forearm relative to both humerus and body size (Takahashi, 1990), resulting in forearm muscles with high relative TLs (high TL : MTU ratios) (Fig. 3c). This distribution is advantageous for brachiating in two ways: on the one hand, because of the low distal muscle mass and the long (fore)arm, the non-supporting arm can swing fairly quickly and with little power input back up to the next handgrip because the segment centre of mass (COM) lies near the body (cf. cursorial mammals). On the other hand, the pendulum effect of the body during contact with the overhead support can be enhanced because muscle mass is centred near the body (and away from the pivot point, i.e. the hand). Gibbons are also capable of moving their COM closer to, or further from, the handgrip to enhance the pendulum effect (affecting swing speed and velocity of the body). They flex or extend their elbows and lift their legs to shift the COM. The further away that the COM is from the pivot point, the slower the swing movement will be but the gibbons will then be able to reach further and consequently the velocity of the body moving forward will be higher. In this way, the COM follows the pattern of a pendulum and mechanical energy recovery is possible (Bertram et al. 1999; Bertram & Chang, 2001; Usherwood et al. 2003). The muscles that seem most suitable for this action are, based on muscle masses and PCSAs, the shoulder muscles, elbow flexors and wrist/digital flexors. The deltoid, in particular, provides a significant advantage during brachiation, having the largest PCSA and contributing to different movements of the humerus (abduction and flexion/extension).

From the muscle mass results, we can conclude that shoulder muscle masses are almost equally distributed over the functional groups. Only abductor muscles (i.e. D and SS) have a much lower mass, hence shoulder abductors are the shoulder muscles with the lowest capacity for power production and this seems to be the case in all gibbon species studied. For brachiation, arm abductors do not seem very important (at least not for powerful arm motion) as arm motion predominantly occurs in the sagittal plane and in a suspensory position the arm is fully abducted under the influence of gravity. However, the abductors might be important in reaching for overhead supports that are not necessarily placed in the sagittal plane of the body and therefore have to be able to act quickly and accurately but can be less powerful. In the elbow and wrist, we find a clear dominance of flexor muscle groups. Even though the triceps muscle has one of the highest individual PCSAs, it is small compared with the large elbow flexor group. It is the only elbow extensor in gibbons (m. anconeus lateralis is not present in gibbons) and its function as an elbow extensor is consequently not negligible. However, during brachiation (overhead support) the elbow can be extended passively under the influence of gravitation and active/powerful elbow extension is probably only necessary for movements such as climbing or reaching for food. During brachiation, the triceps muscle will probably primarily act at the shoulder.

In suspension, e.g. during brachiation, the arms undergo tension forces instead of compressive forces as occurring in quadrupedal locomotion. Although there is also some compression in the joints due to muscle contraction, the muscles have to be able to work primarily against these gravitational forces to move the body up and forward. Therefore, flexor muscles in the elbow and wrist (working against gravity) will have to be developed more than extensor muscles (working with gravity). In the shoulder, however, we expect extensor muscles (pull arm back and body up in the sagittal plane) and adductor muscles to be more developed. Figure 3a shows that wrist and digital flexors, elbow flexors and shoulder extensors, rotators and flexors are capable of producing large forces. Rotator muscles in the shoulder might be important to stabilize the body during brachiation and prevent it from swinging mediolaterally rather than forward. These muscles might also be necessary in reaching (e.g. to reach for branches or food).

Of course PCSA and mass are not the only parameters that can predict the capabilities of a muscle. Although FL is included in the calculation of PCSA, it is an important factor on its own that can give information about the range of motion in which a muscle can produce force and the velocity at which it can contract. The latter is also affected by the fibre type distribution of the muscle and eventually the muscle moment arm also influences the speed of movement. Gibbon wrist and digital flexors have relatively low FLs (Fig. 3b), meaning that they might not be able to work over a large range of motion or contract very fast, although they are fairly strong.

Figure 5 shows the FL (average for the functional muscle group) and PCSA (sum of the muscle PCSA in each functional group) of the functional muscle groups. Note that the characteristics given below are relative parameters that hold within our gibbon sample only. The most powerful muscles (large PCSA and long FL) are found in the top right corner and include shoulder flexors, extensors, rotators and elbow flexors. In the bottom right corner, we find muscles with a large range of motion and capacity for fast contraction but with little force (long FL and small PCSA). These muscles are shoulder adductors, elbow extensors, pronators and supinators and muscles of the scapula. These muscles are not necessary to provide high forces (e.g. elbow extensors work with gravity) but will be able to work over a wide range of joint angles and at high contraction speed. The relatively low PCSA of the shoulder adductors might be due to the fact that brachiation mainly occurs in the sagittal plane. In addition, in a suspensory position (i.e. the arm raised above the body), it is possible to achieve adduction of the arm by combined extension and endorotation. The adductors are probably more important in other movements, such as climbing or reaching for food or branches, or for stabilizing the shoulder. The wrist (and digital) flexors are found in the top left corner, meaning that they can produce a lot of force but have a small range of motion (low power). The other muscles that work at the wrist, as well as the shoulder abductors and elbow extensors, have a low FL and PCSA, and are probably less important for brachiation. They might have a stabilizing function and/or contribute to other less powerful and more precise movements, such as reaching for food, manipulation and grooming.

Figure 5.

 Fascicle length (FL) against physiological cross-sectional area (PCSA) for each functional muscle group of the four measured gibbon species. This indicates the actions to which the muscle groups are best suited.

Tendon function: efficient force production vs. a product of optimal mass distribution

The gibbon's elbow and wrist flexors are characterized by a relatively high SIL (Fig. 4). A high SIL was found for Bra and B and for most wrist flexors (i.e. FDS, FDP, FCR, Palm and APL), surpassing the average SIL of mammalian tendons (13 MPa; Ker et al. 1988). The high SIL of the tendons of these muscles is due to the combination of a high PCSA, and hence strength, and a relatively low TCSA, which will result in substantial tendon stretch, thus creating the possibility for storage of elastic strain energy. The B and Bra muscles, however, do not have long tendons and it seems unlikely that their high SIL represents a capacity for energy storage in the tendon. The wrist flexors, however, have relatively long tendons, which are generally more compliant, meaning that the muscle will be able to contract nearly isometrically, leading to a more economical force production (Biewener, 1998; Alexander, 2002; Roberts, 2002). Although the long tendons might be merely a by-product of optimal mass distribution in the forelimb (muscle bellies as proximal to the body as possible), the high forces generated by the muscles (high PCSA) might also be able to stretch the long, compliant tendons, allowing energy-saving via storage and recoil of elastic energy. However, it should be noted that there is a lot of interindividual and interspecific variation in the SIL values. As the muscle PCSA does not show much variation, this must be because of the TCSA. Although care was taken when assessing the tendon mass and length (to calculate TCSA), it is possible that this variation occurs due to a measuring error rather than representing actual biological variation.

What muscle capacities are unique to gibbons?

For the wrist and digital muscle masses and PCSAs (Figs 6a, 7a), we do not see much difference between the non-human primate species. However, if we look at the ratio of wrist flexors to wrist extensors (Fig. 6b for mass; Fig. 7b for PCSA), there seems to be a decreasing share of flexors and an increasing share of extensors from specialized (wrist flexor mass and PCSA both ±80%) over ‘modified’ brachiators (wrist flexor mass 73% and PSCA 69%) to non-brachiators (wrist flexor mass 67% and PCSA 63%). For the elbow muscles this is even more obvious, with the quadrupeds and bipeds (macaques and humans) clearly having a greater share of extensors (elbow extensor mass 52–58% and PCSA 65–76%) in comparison to gibbons, whose elbow flexors are relatively larger and stronger (elbow flexor mass 69–75% and PCSA 55–65%). Chimpanzees, as ‘modified’ brachiators, lie somewhere in between (elbow flexor mass 57% and PCSA 50%). For the FLs (Fig. 8) of the elbow flexors we find similar results (decreasing FL of elbow flexors from specialized over ‘modified’ to non-brachiators), suggesting that gibbons do not only have stronger elbow flexors but that these muscles will also have a wider range of motion and possibly a higher contraction speed (more power; although this will also depend on the fibre type of the muscle) (Fig. 8). Moreover, for all studied primate species, the elbow flexors seem to have a higher FL compared with the elbow extensors, concluding that, in general, elbow flexors are more suitable for a wide range of motion and have a faster contraction capacity than elbow extensors. In the wrist and digital muscles, no clear differences in FL between species or between antagonistic muscle groups are found. This suggests once again that these muscles are not tightly linked to the specific locomotor mode of gibbons, i.e. brachiation. It is most likely that this similarity in FLs of the muscles of the wrist of different primates reflects adaptation to locomotion in the same, arboreal habitat, where grasping is important (low FL and high PCSA of wrist/digital flexors). Note that the values for macaques are optimal FLs, which are measured FLs normalized to the optimal sarcomere length of macaques. Unfortunately, data of wrist and digital muscles of strictly quadrupedal, terrestrial primates were unavailable, limiting an extensive interspecific comparison. Cheng & Scott (2000) did provide some masses and PCSAs of the shoulder muscles, allowing us to compare LD and Tmaj across primates with different locomotor specializations. The statement of Fleagle (1979) that both latissimus dorsi and teres major should be particularly large in brachiating species is not supported by our results. The normalized values of LD and Tmaj muscle mass and PCSA give similar results for specialized, modified and non-brachiating primates, indicating that these muscles are not specifically linked to brachiation but rather adapted for a large range of movements (e.g. climbing, grasping and reaching) occurring in these different primates. It should also be noted that for a thorough anatomical comparison of several primate species, it is important to take phylogenetic effects into account (closely related species can have similar anatomy regardless of their differences in locomotion habits or habitat). However, as our primary goal was to provide a quantitative analysis of the functional anatomy of the gibbon forelimb, rather than a detailed interspecific comparison of primate forelimb anatomy, we only present a rough comparative analysis mainly as a framework for our data. We can conclude from our analysis that the high proportion of elbow flexor muscles in gibbons is linked to their unique locomotor mode, i.e. brachiation.

Figure 6.

 Muscle mass comparison with non-specialized brachiators. Functional muscle groups contain only those muscles used by Thorpe et al. (1999). Chimpanzee and human data from Thorpe et al. (1999) and macaque data from Cheng & Scott (2000). All data are normalized to the measured average gibbon weight (7.7 kg). (a) Summed-up values and (b) proportional values (relative to total elbow or total wrist muscle mass, respectively).

Figure 7.

 Muscle physiological cross-sectional area (PCSA) comparison with non-specialized brachiators. Functional muscle groups contain only those muscles used by Thorpe et al. (1999). Chimpanzee and human data from Thorpe et al. (1999) and macaque data from Cheng & Scott (2000). All data are normalized to the measured average gibbon weight (7.7 kg). (a) Summed-up values and (b) proportional values (relative to total elbow or total wrist PCSA, respectively).

Figure 8.

 Average fascicle length (FL) comparison with non-specialized brachiators. Functional muscle groups contain only those muscles used by Thorpe et al. (1999). Chimpanzee and human data from Thorpe et al. (1999) and macaque data from Cheng & Scott (2000). All data are normalized to the measured average gibbon weight (7.7 kg).

Conclusion

This study presents detailed anatomical data of the forelimb musculature of four gibbon species (H. lar, H. moloch, H. pileatus and S. syndactylus). No substantial differences in forelimb anatomy were found between the different gibbon species and muscle dimensions are comparable when normalized to the same body mass. This is an important finding as it allows us to generalize the anatomy of ‘the gibbon’ and provides the opportunity to extrapolate published work on brachiating lar gibbons to other species.

Overall, gibbons have shoulder flexors, extensors, rotator muscles and elbow flexors with a high power or work-generating capacity. In addition, elbow flexor tendons have a high SIL, pointing to a possible energy storage capacity. Wrist flexors have a high force-generating capacity but seem restricted to a small range of motion (low FL). The wrist flexor tendons have a high SIL and a high FL : MTU ratio, giving them the capacity to store and release strain energy in their tendons, although this might also be merely a by-product of an optimal mass distribution and long forearm length. The shoulder flexors, extensors, rotator muscles, elbow flexors and wrist flexors are expected to contribute the most in brachiation and especially the elbow flexors of gibbons are more powerful, compared with those of non-specialized brachiators. Although brachiation on a horizontal and fixed substrate might require little energy input, these muscles will be necessary to actively regulate the movement of the body COM and maintain the most energetically effective path when brachiating on compliant, varying and unpredictable substrates.

Acknowledgements

This study was supported by a research grant to F.M. from the University of Antwerp and the Fund for Scientific Research, Flanders (Belgium). Structural support was provided by the Centre for Research and Conservation of the Royal Zoological Society of Antwerp. We also thank the Royal Zoological Society of Antwerp and NMS for provision of gibbon cadavers and the Royal Society International Joint Project for travel funding.

Appendices

Table AppendixA.   Averaged and normalized (to average body mass of 7.7 kg) data for each muscle and each of the four measured gibbon species
MuscleLarPileated
Mass (g)PCSA (mm2)FL (mm)TL : MTUMass (g)PCSA (mm2)FL (mm)TL : MTU
Pmaj49.823921070.2860.125621020.17
Pmin5.1560580.275.0655860.19
LD59.003681490.2566.954931290.21
Trap33.5952162 26.4435770 
Serr19.4320990 18.2819688 
Rh13.2822857 13.3724851 
Rmin3.00   3.577247 
LS7.388874 4.254796 
SPSA7.72   6.5513945 
D57.64135237 57.53974550.56
Tmaj20.2322487 20.0524977 
Tmin4.74124370.25    
SS11.79300300.5115.50361380.56
IS15.56328410.6017.14355410.63
SSc31.53736350.4528.10539500.52
DET9.05110540.6011.3320551 
B66.42581950.3571.55794850.61
CB6.54160360.278.4519441 
Bra36.57451690.3945.89601660.35
Tr51.06911470.6543.19833490.69
BR9.72751070.4613.95154810.44
ECRL4.5972510.825.0876500.81
ECRB5.11117340.845.47126350.82
FCR8.86274330.6713.31300390.73
FCU5.95152320.849.06265310.83
Palm3.5689350.843.18131210.79
PT8.37298231.006.41271220.61
FDS 239.96668470.8343.8357177 
FDS 3   0.79    
FDS 4   0.87    
FDS 5   0.86    
FDP 139.001015360.8843.5191945 
FDP 2        
FDP 3        
FDP 4        
FDP 5        
PQ0.91   1.23   
EDC9.7019041 12.5323346 
EDB2.929428 2.697531 
EDM0.5213540.830.933523 
ECU4.21108270.834.2379410.85
Sup8.115886 7.42   
EPL1.4554270.881.725427 
EPB2.33121240.771.6760210.91
APL5.64167250.893.3588310.92
MuscleMolochSiamang
Mass (g)PCSA (mm2)FL (mm)TL : MTUMass (g)PCSA (mm2)FL (mm)TL : MTU
Pmaj41.883411160.2743.04443940.30
Pmin5.0563730.265.4383620.28
LD49.323601280.2365.394331470.31
Trap26.3638267 27.95461580.18
Serr14.1116183 20.1519999 
Rh10.8520750 10.9119653 
Rmin        
LS3.734778 4.464790 
SPSA4.1010837 6.0712248 
D43.28818540.6859.661128460.51
Tmaj14.43278500.3518.72253700.36
Tmin4.73122350.515.19104430.35
SS9.76376220.4510.48285340.55
IS13.09336340.6416.68401370.65
SSc22.26607360.5231.65668390.58
DET7.8515249 10.04135730.69
B52.55476940.5555.68525970.38
CB5.0311239 7.99170450.38
Bra31.80571640.3550.79618790.42
Tr37.00957390.6640.99690610.71
BR8.85100770.6413.89149890.64
ECRL3.6764450.845.0878570.83
ECRB2.4950420.825.09116320.85
FCR7.41180340.6810.55276350.71
FCU5.69186280.807.03233280.86
Palm2.7472330.842.8073300.85
PT6.59225250.597.76339200.56
FDS 245.7689342 37.41833380.84
FDS 3       0.86
FDS 4       0.86
FDS 5       0.84
FDP 130.9259841 37.19745420.81
FDP 2       0.98
FDP 3       0.82
FDP 4       0.73
FDP 5       0.83
PQ1.44  0.391.178215 
EDC6.7120327 9.74156420.78
EDB2.146927 3.1385280.85
EDM0.421919 1.1626380.82
ECU2.66102200.843.3887290.84
Sup7.4526426 8.10290240.64
EPL1.223031 1.3437280.86
EPB1.2744250.731.5859270.78
APL3.23110270.904.94146250.84
Table AppendixB.   Overview of dissected muscles with origin and insertion
MuscleSpeciesOriginInsertion
  1. Variations in muscle course found in separate individuals or species are indicated (var = variation; LH =  long head; SH = short head; latH = lateral head; MH = medial head; I/O = interosseous; MC = metacarpals; D = digits; T = thoracic; C = cervical; MB = muscle belly) (crab-eating monkey: Kimura & Takai, 1970; bonobo: Miller, 1952; atelines: Youlatos, 2000).

Pectoralis majorGibbonsRibs 1–6, lateral half of clavicle, small part of sternumWith broad tendon (ca. 4 cm), to bicipital groove running over biceps LH tendon
Var lar: lateral 2/3rd of clavicleVar S3 and lar: second slip attaches to biceps SH tendon; fusion with deltoid
BonoboIdem gibbon but ribs 1–7Greater tubercle of humerus
AtelinesIdem gibbon but of clavicleIdem gibbon
Pectoralis minorGibbonsLateral part ribs 2, 3 and 4Coracoid process of scapula
Var lar: ribs 2–5Var S3 and lar: also lateral part of clavicle
BonoboIdem gibbonIdem gibbon
TrapeziusGibbonsCervical and thoracic vertebrae (spinous processes)Lateral third of clavicle, scapular spine, acromion
BonoboIdem gibbonIdem gibbon
Latissimus dorsiGibbonsLower 6 thoracic vertebrae, iliac crest, lower 4 ribsWith broad tendon to bicipital groove
Var lar: iliac crest not in all specimenVar lar: Tmaj fused with LD at insertion
BonoboLower 5 thoracic vertebrae, lumbar and sacral vertebra, iliac crest and lower 5 ribsIdem gibbon
AtelinesIdem with some variation depending on speciesIdem gibbon
SubclaviusGibbonsCartilage of 1st ribDorsolateral part clavicle
Var S3: 1st and 2nd rib; var lar: 2nd and 3rd rib
BonoboIdem gibbonIdem gibbon
Serratus anteriorGibbonsFrom 2nd to 10th ribsMedial border and inferior angle of scapula
BonoboFrom 1st to 10th ribsSuperior angle and vertebral border and inferior angle
Pars superior of serratus anteriorGibbonsSuperior angle and medial border of scapulaRib 2–3
Var lar: ribs 1–3
RhomboidGibbonsSpinous processes of T2–T5Medial border and inferior angle of scapula
Var lar: T1–T5Var S1: also scapular spine
BonoboC3 to T6Idem gibbon
Levator scapulaeGibbonsTransverse processes of C1–4Superior angle of scapula
BonoboIdem gibbonIdem gibbon
DeltoidGibbonsLateral 2/3 of scapular spine, acromion process, lateral third of clavicleLateral border of proximal humerus
Var S3, S4 and lar: aponeurosis covers IS
Var lar: lateral 1/2 of scapular spine
BonoboIdem gibbonIdem gibbon
AtelinesIdem gibbonIdem gibbon
Teres majorGibbonsInferior angle of scapulaBicipital groove of humerus var S4 and lar: on tendon of LD
Var lar: also lower third lateral border scapula
BonoboIdem gibbon plus lower half of axilliary border scapulaLesser tubercle of humerus
Teres minorGibbonsLower lateral border of scapulaGreater tubercle of humerus (post-lateral neck)
Var lar: middle of lateral border of scapula
BonoboAxilliary borderIdem gibbon
SubscapularisGibbonsSubscapular fossaLesser tubercle of humerus
Var S1: also lower border scapulaVar S1 and lar: with tendon to humerus head, with muscle fibres to humerus neck
BonoboIdem gibbonIdem gibbon
SupraspinatusGibbonsSupraspinous fossaSuperior part of greater tubercle of humerus
BonoboIdem gibbonIdem gibbon
AtelinesIdem gibbonIdem gibbon
InfraspinatusGibbonsInfraspinous fossaMiddle part of greater tubercle of humerus
BonoboIdem gibbonIdem gibbon
DorsoepitrochlearisGibbonsFrom LD tendon, near insertionFused with head of biceps SH, thin tendon-like aponeurosis to medial condyle
Crab-eating monkeyIdem gibbonIdem gibbon
BonoboIdem gibbonIdem gibbon
AtelinesIdem gibbonIdem gibbon
CoracobrachialisGibbonsCoracoid process of scapulaProximal third of medial surface of humerus
Crab-eating monkey2 parts: profundus and medialMiddle of humerus
BonoboIdem gibbonMiddle of humerus
TricepsGibbonsLH: superior lateral border scapula (infraglenoid)Olecranon process of ulna
LatH: prox-post part of humerusVar S1 and lar: part of tendon of origin runs over aponeurosis at insertion Tmaj
MH: post and middle part of humerus (sulcus n. radialis between LatH and MH)
Crab-eating monkeyIdem gibbonIdem gibbon
BonoboIdem gibbonIdem gibbon
BicepsGibbonsLH: supraglenoid tubercleTendon to radial tuberosity, muscle fibres (SH) to superficial flexors and fascia
SH: lesser tubercle of humerus
Var S1: not clearly 2-headed, only insertion on lesser tubercle found
Crab-eating monkeySH: processus coracoideus of scapulaIdem gibbon
BonoboSH: coracoidIdem gibbon
AtelinesSH: coracoidIdem gibbon
BrachialisGibbonsDistal 1/2 of anterior surface of humerusProximal part of ulna (2 cm→3.5 cm; tuberositas ulnae)
Var S1: distal 2/3 of anterior surface of humerus
Crab-eating monkeyIdem gibbonIdem gibbon
BonoboIdem gibbonIdem gibbon
AtelinesIdem gibbonUlnar shaft
BrachioradialisGibbonsLateral supracondylar ridgeMiddle of radius
Var S1 and S3: radius head (styloid process)
Var S4: distal part radius
Crab-eating monkeyIdem gibbonDistal part radius
BonoboIdem gibbonDistal part radius
PalmarisGibbonsMedial epicondyle of humerusPalmar aponeurosis
Crab-eating monkeyIdem gibbonIdem gibbon
BonoboIdem gibbonTransverse carpal ligament
Extensor digitorum communisGibbonsLateral epicondyle of humerus2nd phalanx of D2–4
Var S1: tendon at originVar S1: tendons all fused
Var lar: D2–5
Crab-eating monkeyIdem gibbon and fascia antebrachia2nd and 3rd phalanges D2–5
BonoboIdem gibbon2nd and 3rd phalanges D2–5
Extensor carpi ulnarisGibbonsProximal third of ulna and lateral epicondyle humerusLateral side base 5th metacarpal
Crab-eating monkeyLateral epicondyleIdem gibbon
BonoboIdem gibbonIdem gibbon
Extensor carpi radialis longusGibbonsLateral supracondylar ridge humerusBase of 1st and 2nd metacarpal
Var lar: 2 tendons at insertion
Crab-eating monkeyIdem gibbon2nd metacarpal
BonoboIdem gibbon2nd metacarpal
Extensor carpi radialis brevisGibbonsLateral epicondyle humerusBase of 2nd and 3rd metacarpal
Var S1: also belly EDCVar S4: only 2nd; var lar: only 3rd
Crab-eating monkeyIdem gibbon3rd metacarpal
BonoboIdem gibbon3rd metacarpal
Extensor digiti minimiGibbonsLateral epicondyle of humerusDorsal aponeurosis (middle phalanx) of D5
Var S1and lar: also middle part ulnaVar S1 tendon fused with ECU tendon
2 tendons at insertion (fused)
Var lar: fused with EDC but tendon runs in own tendon sheet
Extensor digitorum brevisGibbonsDistal 2/3 of ulnaSplitting at wrist into two
Var lar: middle of ulnaPart 1: base prox phalanx of D2
Part 2: to base of prox phalanx of D3/D4
Var S1 and lar: base prox phalang D2–4 and extensor sheet phalanges (sometimes only D2–3)
Var S2: tendon fused with tendon EDC
Extensor pollicis longusGibbonsProximal 1/4 of ulnaTerminal phalanx of pollex (dorsal side)
Crab-eating monkeyIdem gibbonIdem gibbon
BonoboMiddle 1/3rd ulnaIdem gibbon
Extensor pollicis brevisGibbonsProximal medial part of radius and I/O membraneDorsal side 1st metacarpal
Var S1: proximal 1/2 and also prox ulnaVar S1: scaphoid-trapezium (= APL?)
Var lar: middle 1/3Var S3 and lar: med part base MC1; also in lar fused with APL
BonoboAbsent
Abductor pollicis longusGibbonsProximal 1/3 of ulna and radius, prox to EPBMedial side base of MC1
Var S1: proximal half of ulna and radiusVar S2: 1 muscle belly with 2 tendons (1 very thin)→2 insertions on same bone: trapezium
Var S: trapezium (only 1 tendon)
Crab-eating monkeyMiddle 3/5 ulna, proximal 2/3 radius and I/O membraneMetacarpal and sesamoid bone
BonoboMiddle 3/5 ulna, proximal 2/3 radius and I/O membraneIdem gibbon and trapezium
Flexor digitorum superficialisGibbonsD2: proximal part of ulnaFour tendons to both sides of middle phalanges D2–5
D3: lateral border of radius
D4: medial epicondyle of humerus
D5: proximal half of ulna
Var S1: D2: prox 1/2 ulna and heads D4 and D5 fused
Crab-eating monkeyMedial epicondyl humerusIdem gibbon
BonoboD2: coronoidIdem gibbon
Atelines2 distinct heads both from medial humeral epicondyleFive tendons to both sides of middle phalanges D1–5
Flexor digitorum profundusGibbonsMedial, middle 2/3 surface of radius, prox ulna, anterior surface and lateral border of ulnaBase distal phalanges D1–5
Var S1: middle 1/3 radius and I/O membraneVar S1: D1–2 and D4–5 tendons fused, D4–5 and D2–3 fused MB, D1 has separate MB
Var lar: medial epicondyleVar S3: D1–2 share MB + tendon, D3 biggest tendon + separate MB, D4 has multiple small tendons and shares MB with D5
Crab-eating monkeyIdem gibbonIdem gibbon
BonoboIdem gibbonIdem gibbon
AtelinesIdem gibbon and medial epicondyle but ateles additional humeral headIdem gibbon
Flexor carpi radialisGibbonsMedial epicondyle humerus idemPalmar side base of MC2
Var lar: also from PT
Crab-eating monkeyIdem gibbonIdem gibbon
BonoboIdem gibbonIdem gibbon
Flexor carpi ulnarisGibbonsProximal 2/3 ulna with oleocranon processPisiform bone
Crab-eating monkey2 heads: one same as gibbon and one medial epicondyle humerusIdem gibbon
BonoboMedial epicondyle and lateral ulnaIdem gibbon and base of 5th metacarpal
SupinatorGibbonsLateral epicondyle of humerusProximal posterior side radius
Var lar: proximal 1/3 radius and radial tuberosityVar lar: proximal side ulna
Crab-eating monkeyIdem gibbonProx ulna
BonoboIdem gibbonIdem gibbon
AtelinesIdem gibbonIdem gibbon
Pronator teresGibbonsMedial epicondyle of humerusProximal lateral border of radius, often fused with FDS
Crab-eating monkeyIdem gibbonIdem gibbon
BonoboIdem gibbon plus coronoid processusMiddle third of radius
AtelinesIdem gibbonRadial shaft
Pronator quadratusGibbonsAnterior distal 1/4 of ulna (I/O side)Anterior distal 1/4 of radius (I/O side)
Crab-eating monkeyIdem gibbonIdem gibbon
BonoboIdem gibbonIdem gibbon
AtelinesUlnar shaftRadial shaft

Ancillary