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.