The comparative and functional morphology of the bones composing the primate shoulder complex (clavicle, scapula, and humerus) are relatively well studied and have been shown to be adapted to both locomotor style and postural behavior of a given species (Ashton and Oxnard, 1964; Oxnard, 1967; Rodman, 1979; Kimes et al., 1981; Larson, 1993; Gebo and Sargis, 1994; Taylor, 1997; Voisin and Balzeau, 2004; Voisin, 2006). Additionally, both the gross and the fiber architectural characteristics of primate shoulder muscles have been shown to be similarly adapted (Tuttle and Basmajian, 1978; Larson, 1988; Larson and Stern, 1992; Anapol and Gray, 2003; Higurashi et al., 2006; Schmidt and Schilling, 2007; Michilsens et al., 2009). However, there is a surprising lack of comparative studies examining bony articulations of the shoulder joint complex (e.g., glenohumeral, acromioclavicular, and coracoclavicular joints) alongside their associated soft-tissue structures. Given that the motions of the “shoulder” itself occur at these separate joints, a detailed understanding of the comparative, functional, and adaptive morphology of this joint complex may inform our insight into morphological adaptations to both locomotor style and postural behavior. Moreover, an increased insight into the adaptive morphology of the shoulder joint complex in primates may assist our efforts in comprehending the selective forces that drive the evolution of the primate shoulder and the process of its modification from a weight-bearing joint to a relatively weight-free structure that is more closely associated with manipulative functions in Homo.
Primate species are usually broadly assigned to a single locomotor category and to typical postural behaviors (e.g., Napier and Napier, 1994; Fleagle, 1999). However, these often do not describe fully the motions that occur at limb joints because of within-species variation of joint motion resulting from seasonal food availability, the presence of dependent offspring, ontogenetic stages, and so forth. Broad categories of typical locomotor and postural behaviors, however, can be assigned to particular species based upon the frequency of time spent in a given behavior within a 24 hr period. Thus, primate species are generally assigned to one of four broad locomotor categories, based on the frequency of observed locomotor activities: arboreal quadrupedalism, terrestrial quadrupedalism, leaping, and brachiation (Fleagle, 1999; Nowak, 1999). Whereas each of these broad categories can be further subdivided into specific locomotor activities (e.g., Hunt et al., 1996; Thorpe and Crompton, 2006), and they are commonly used as gross descriptors of primate locomotion.
Postural behaviors are recognized as activities performed by an individual where there is no displacement of the individual relative to its surroundings (Rose, 1979). All primates spend more of their time in these behaviors than in locomotor behaviors; thus, postural behaviors may play a great adaptive role in shaping morphology of various limb elements (Rose, 1979; McGraw, 1998).
Among extant primates, prosimians are perhaps the least understood in terms of shoulder adaptations (both osteological and muscular) to locomotor and postural behaviors (Larson, 1993; Fleagle, 1999). However, prosimians (lorises, galagos, lemurs, and tarsiers) consist of species that occupy all locomotor categories except for brachiation, and they practice a wide range of postural behaviors such as vertical clinging, suspension, and palmigrade wrist positioning (Napier and Napier, 1994; Fleagle, 1999). In addition, prosimians are widely considered to be the best extant representation of the stem primates (Cartmill, 1972; Martin, 1990; Fleagle, 1999; Soligo and Martin, 2006; Silcox, 2007). Thus, an increased understanding of the adaptive and functional morphology of shoulder joints across prosimians may aid our efforts at reconstructing the morphotype of the earliest primates and their locomotor and postural behaviors.
The aim of this study is to compare the soft-tissue morphological structures of the glenohumeral, acromioclavicular, and coracoclavicular joints among prosimian species chosen for differences in phylogenetic relationships, locomotor style, and postural behaviors. Whereas the rotator cuff muscles themselves are not intrinsically part of these joints; the presence of their tendons is often cited as a major stabilizer to the glenohumeral joint and are, therefore, examined in this study.
Species Included in This Study
Major locomotor style and postural behaviors of each species used in this study are described here, along with a description of the phylogenetic relationships among the species. All taxonomic designations are based upon Groves (2001).
Galago moholi (Lemuriloriformes : Loriformes : Galagonidae).
This small (140–225 g), nocturnal galago primarily inhabits Acacia thornveld savannas of central and southern Africa and remains in an arboreal setting for the majority of its time. G. moholi is categorized as a vertical clinger and leaper, but also spends some time quadrupedally running along branches in a palmigrade posture (Charles-Dominique, 1977 [referring to both G. senegalensis and G. moholi in “lesser galagos”]; Harcourt and Bearder, 1989). When G. moholi lands from a leap, it lands hindlimbs first, later grabbing the substrate with its hands. This species feeds primarily on exudates and invertebrates and obtains these through a vertical clinging posture (Harcourt and Bearder, 1989).
Eulemur macaco (Lemuriloriformes : Lemuriformes : Lemuroidea : Lemuridae).
These medium-sized (1.0–2.5 kg) lemurs are found in the semideciduous forests of Madagascar and are active both in the trees and on the ground. E. macaco is cathemeral (being active during day and night periods) and is reported to use both terrestrial and arboreal quadrupedal running and suspension by both the forelimbs and hindlimbs in feeding (Colquhoun, 1993, 1998; Mittermeier et al., 2008). This species feeds on a tremendously wide variety of foods, but fruits seem to be the greatest percentage of resources (Mittermeier et al., 2008).
Cheirogaleus medius (Lemuriloriformes : Lemuriformes : Cheirogaleoidea : Cheirogaleidae).
The fat-tailed, dwarf lemur is a small (142–217 g) nocturnal species that is primarily a generalized arboreal quadruped found in the dry secondary forests of Madagascar (Lahann, 2007). C. medius feeds primarily on fruits and is not reported to engage in any clinging or suspensory behavior (Lahann, 2007; Mittermeier et al., 2008).
Tarsius syrichta (Tarsisimiiformes : Tarsiiformes : Tarsiidae).
The Philippine tarsier is an exceptionally small (117–134 g) nocturnal primate that is categorized as a forest-dwelling vertical clinger and leaper (Kappeler, 1991; Dagosto et al., 2001). T. syrichta, like other tarsiers, feeds primarily on invertebrates and is not reported to use any quadrupedal or suspensory behaviors.
Using the above taxa, this study aims to assess the gross morphology of the soft-tissue structures of the prosimian shoulder joint complex (glenoid labrum, tendon of the long head of the biceps brachii muscle, joint capsule of the glenohumeral joint, glenohumeral ligaments, acromioclavicular joint capsule, and coracoclavicular ligament) and to collect weights of the “rotator cuff” muscles (supraspinatus, infraspinatus, teres minor, and subscapularis muscles) to: 1) provide the first morphological and quantitative data on these structures in prosimian species, 2) to compare relative weights of the rotator cuff muscles among taxa with respect to phylogenetic position, locomotor style, and postural behavior, and 3) to compare gross morphology of the joint structure among taxa relative to phylogenetic position, locomotor style, and postural behavior. Whereas the sternoclavicular joint is typically included in the shoulder joint complex, we do not include it in this study because of lack of availability.