THE ANATOMICAL RECORD 293:680–691 (2010)

Shouldering the Burdens of Locomotionand Posture: Glenohumeral Joint

Structure in ProsimiansADRIAN S. WRIGHT-FITZGERALD,1,2 MARK D. BALCENIUK,3

AND ANNE M. BURROWS3,4*

1Department of Health Sciences, Sargent College of Health and Rehabilitation Sciences,Boston University, Boston, Massachusetts

2Department of Athletic Training, Duquesne University, Pittsburgh, Pennsylvania3Department of Physical Therapy, Duquesne University, Pittsburgh, Pennsylvania4Department of Anthropology, University of Pittsburgh, Pittsburgh, Pennsylvania

ABSTRACTDespite its importance in movement of the upper limb, the soft-tissue

morphology of the shoulder joint complex (the acromioclavicular, coracocla-vicular, and glenohumeral joints) across primates is poorly understood. Thisstudy compares soft-tissue morphology of these three shoulder joint compo-nents among broad phylogenetic, locomotor, and postural behavior rangesin prosimian primates. Two adult specimens of Galago moholi (a verticalclinger and leaper) were dissected for study, along with one adult each ofCheirogaleus medius (an arboreal quadruped), Eulemur macaco (an arbo-real quadruped that also frequently engages in suspensory behavior), andTarsius syrichta (a vertical clinger and leaper). Because of their role in gle-nohumeral joint movement and stabilization, the rotator cuff muscles werealso dissected and weighed among the species. Results showed that musclemass of individual components of the rotator cuff musculature may beadaptive to locomotor and postural behaviors of the taxa in this study. Twosoft-tissue components of the glenohumeral joint, but not the acromioclavic-ular and coracoclavicular joints, were also considered adaptive. The quadru-pedal species, C. medius and E. macaco, both had glenohumeral ligamentsand E. macaco had a relatively deeper glenoid articular surface for the hu-merus because of the shape of the glenoid labrum. Additionally, this studynoted a lack of a teres minor muscle in G. moholi, C. medius, and E. mac-aco despite previous studies describing them. A relatively robust teresminor muscle was found in T. syrichta. Even with the limited sample dis-sected here, these results suggest that soft-tissue joint morphology itselfmay be as adaptive to locomotory and postural styles as osseous morphol-ogy. Anat Rec, 293:680–691, 2010. VVC 2010 Wiley-Liss, Inc.

Keywords: rotator cuff; shoulder joint; tarsier; Cheirogaleus;Galago; Tarsius; Eulemur

INTRODUCTION

The comparative and functional morphology of thebones composing the primate shoulder complex (clavicle,scapula, and humerus) are relatively well studied andhave been shown to be adapted to both locomotor styleand postural behavior of a given species (Ashton andOxnard, 1964; Oxnard, 1967; Rodman, 1979; Kimeset al., 1981; Larson, 1993; Gebo and Sargis, 1994; Taylor,1997; Voisin and Balzeau, 2004; Voisin, 2006). Addition-

*Correspondence to: Dr. Anne M. Burrows, Department ofPhysical Therapy, 600 Forbes Avenue, Duquesne University,Pittsburgh, PA 15282. Fax 412.396.4399.E-mail: burrows@duq.edu

Received 7 January 2010; Accepted 11 January 2010

DOI 10.1002/ar.21127Published online in Wiley InterScience (www.interscience.wiley.com).

VVC 2010 WILEY-LISS, INC.

ally, both the gross and the fiber architectural character-istics of primate shoulder muscles have been shown tobe similarly adapted (Tuttle and Basmajian, 1978; Lar-son, 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 sur-prising lack of comparative studies examining bonyarticulations of the shoulder joint complex (e.g., gleno-humeral, acromioclavicular, and coracoclavicular joints)alongside their associated soft-tissue structures. Giventhat the motions of the ‘‘shoulder’’ itself occur at theseseparate joints, a detailed understanding of the compar-ative, functional, and adaptive morphology of this jointcomplex may inform our insight into morphologicaladaptations to both locomotor style and postural behav-ior. Moreover, an increased insight into the adaptivemorphology of the shoulder joint complex in primatesmay assist our efforts in comprehending the selectiveforces that drive the evolution of the primate shoulderand the process of its modification from a weight-bearingjoint to a relatively weight-free structure that is moreclosely associated with manipulative functions in Homo.

Primate species are usually broadly assigned to a sin-gle 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 occurat limb joints because of within-species variation of jointmotion resulting from seasonal food availability, thepresence of dependent offspring, ontogenetic stages, andso forth. Broad categories of typical locomotor and pos-tural behaviors, however, can be assigned to particularspecies based upon the frequency of time spent in agiven behavior within a 24 hr period. Thus, primate spe-cies are generally assigned to one of four broad locomo-tor categories, based on the frequency of observedlocomotor activities: arboreal quadrupedalism, terrestrialquadrupedalism, leaping, and brachiation (Fleagle, 1999;Nowak, 1999). Whereas each of these broad categoriescan be further subdivided into specific locomotor activ-ities (e.g., Hunt et al., 1996; Thorpe and Crompton,2006), and they are commonly used as gross descriptorsof primate locomotion.

Postural behaviors are recognized as activities per-formed by an individual where there is no displacementof the individual relative to its surroundings (Rose,1979). All primates spend more of their time in thesebehaviors than in locomotor behaviors; thus, posturalbehaviors may play a great adaptive role in shapingmorphology of various limb elements (Rose, 1979;McGraw, 1998).

Among extant primates, prosimians are perhaps theleast understood in terms of shoulder adaptations (bothosteological and muscular) to locomotor and posturalbehaviors (Larson, 1993; Fleagle, 1999). However, prosi-mians (lorises, galagos, lemurs, and tarsiers) consist ofspecies that occupy all locomotor categories except for bra-chiation, and they practice a wide range of postural behav-iors such as vertical clinging, suspension, and palmigradewrist positioning (Napier and Napier, 1994; Fleagle,1999). In addition, prosimians are widely considered to bethe best extant representation of the stem primates (Cart-mill, 1972; Martin, 1990; Fleagle, 1999; Soligo and Mar-tin, 2006; Silcox, 2007). Thus, an increased understandingof the adaptive and functional morphology of shoulderjoints across prosimians may aid our efforts at recon-

structing the morphotype of the earliest primates andtheir locomotor and postural behaviors.

The aim of this study is to compare the soft-tissuemorphological structures of the glenohumeral, acromio-clavicular, and coracoclavicular joints among prosimianspecies chosen for differences in phylogenetic relation-ships, locomotor style, and postural behaviors. Whereasthe rotator cuff muscles themselves are not intrinsicallypart of these joints; the presence of their tendons is oftencited as a major stabilizer to the glenohumeral joint andare, therefore, examined in this study.

Species Included in This Study

Major locomotor style and postural behaviors of eachspecies used in this study are described here, along witha description of the phylogenetic relationships amongthe species. All taxonomic designations are based uponGroves (2001).

Galago moholi (Lemuriloriformes : Loriformes :Galagonidae). This small (140–225 g), nocturnal gal-ago primarily inhabits Acacia thornveld savannas of cen-tral and southern Africa and remains in an arborealsetting for the majority of its time. G. moholi is catego-rized as a vertical clinger and leaper, but also spendssome time quadrupedally running along branches in apalmigrade posture (Charles-Dominique, 1977 [referringto both G. senegalensis and G. moholi in ‘‘lesser gala-gos’’]; Harcourt and Bearder, 1989). When G. moholilands from a leap, it lands hindlimbs first, later grabbingthe substrate with its hands. This species feeds pri-marily on exudates and invertebrates and obtains thesethrough a vertical clinging posture (Harcourt andBearder, 1989).

Eulemur macaco (Lemuriloriformes :Lemuriformes : Lemuroidea : Lemuridae). Thesemedium-sized (1.0–2.5 kg) lemurs are found in the semi-deciduous forests of Madagascar and are active both inthe trees and on the ground. E. macaco is cathemeral(being active during day and night periods) and isreported to use both terrestrial and arboreal quadrupe-dal running and suspension by both the forelimbs andhindlimbs in feeding (Colquhoun, 1993, 1998; Mitterme-ier et al., 2008). This species feeds on a tremendouslywide variety of foods, but fruits seem to be the greatestpercentage of resources (Mittermeier et al., 2008).

Cheirogaleus medius (Lemuriloriformes :Lemuriformes : Cheirogaleoidea : Cheirogalei-dae). The fat-tailed, dwarf lemur is a small (142–217 g)nocturnal species that is primarily a generalized arbo-real quadruped found in the dry secondary forests ofMadagascar (Lahann, 2007). C. medius feeds primarilyon fruits and is not reported to engage in any clinging orsuspensory behavior (Lahann, 2007; Mittermeier et al.,2008).

Tarsius syrichta (Tarsisimiiformes :Tarsiiformes : Tarsiidae). The Philippine tarsier isan exceptionally small (117–134 g) nocturnal primatethat is categorized as a forest-dwelling vertical clingerand leaper (Kappeler, 1991; Dagosto et al., 2001).

PROSIMIAN SHOULDER JOINT MORPHOLOGY 681

T. syrichta, like other tarsiers, feeds primarily on inver-tebrates and is not reported to use any quadrupedal orsuspensory behaviors.

Study Aims

Using the above taxa, this study aims to assess thegross morphology of the soft-tissue structures of the pro-simian shoulder joint complex (glenoid labrum, tendon ofthe long head of the biceps brachii muscle, joint capsuleof the glenohumeral joint, glenohumeral ligaments, acro-mioclavicular joint capsule, and coracoclavicular liga-ment) and to collect weights of the ‘‘rotator cuff ’’muscles (supraspinatus, infraspinatus, teres minor, andsubscapularis muscles) to: 1) provide the first morpho-logical and quantitative data on these structures in pro-simian species, 2) to compare relative weights of therotator cuff muscles among taxa with respect to phyloge-netic position, locomotor style, and postural behavior,and 3) to compare gross morphology of the joint struc-ture among taxa relative to phylogenetic position, loco-motor style, and postural behavior. Whereas thesternoclavicular joint is typically included in theshoulder joint complex, we do not include it in this studybecause of lack of availability.

MATERIALS AND METHODS

Two adult cadaveric specimens of G. moholi, and oneadult specimen each of C. medius, E. macaco, and T.syrichta were dissected for study. All specimens wereacquired from Duke Lemur Center/Duke University Pri-mate Center, where they were kept in a seminaturalenvironment. All animals died of natural causes. Afterdeath, each cadaver was immersed in 10% buffered for-malin and stored in this fashion.

All dissections were done on either the right or leftupper limb, depending upon availability and condition,and were carried out using 2.5x magnifying loupesexcept for E. macaco, which was large enough to be dis-sected without magnifiers. Using microdissection tools,skin and superficial fascia was excised away from theshoulder region to reveal the dorsally located rotatorcuff muscles. All other dorsally located musculatureattaching to the scapula around the rotator cuff muscleswas dissected away (i.e., latissimus dorsi, trapezius, anddeltoid muscles). Whereas the latissimus dorsi musclewas not attached to the scapula in any species used inthis study (Jouffroy, 1962); it was in the general regionof interest and was cleared for an unobstructed view ofthe rotator cuff area. Muscle identification followedMurie and Mivart (1872), Woollard (1925), and Jouffroy(1962). Once the rotator cuff muscles were located, theupper limb was disarticulated from the trunk by cuttingthrough the midpoint of the clavicle with scissors andcutting connections between the scapula and the rhom-boid, latissimus dorsi, serratus anterior, trapezius, pec-toralis major, and pectoralis minor muscles. In thisfashion, all rotator cuff muscles plus the teres majormuscles were left attached to the scapula and humerus(Figs. 1,2).

All rotator cuff muscles were detached individuallyfrom their scapular and humeral attachments usingmicrodissection tools and then blotted dry using a papertowel (Atzeva et al., 2007). Weights were recorded to the

nearest 0.01 g using a digital Ohaus Analytical Plusscale.

The acromioclavicular joint was dissected free fromoverlying musculature (deltoid and trapezius muscles) sothat the joint capsule was visible. The coracoclavicularjoint/ligament was defined from surrounding fascia andthe subclavius muscle, and the glenohumeral joint cap-sule was defined both dorsally and ventrally in a similarfashion. The tendon of the long head of the biceps bra-chii muscle was followed through the glenohumeral jointcapsule. The joint capsule was opened in all specimensto view the internal aspect of the glenohumeral joint,glenoid labrum, glenohumeral ligaments, and termina-tion of the tendon of the long head of the biceps brachiimuscle. The joint capsule was opened by cutting longitu-dinally through the dorsal surface of the joint capsuleusing microdissection tools. Once the joint capsule wasexcised, the humeral head was rotated away from theglenoid fossa of the scapula so that the ventral portionof the capsule, glenoid labrum, and termination of thetendon of the long head of the biceps brachii musclewere visible. The dorsal portion of the capsule was cho-sen for incision because any glenohumeral ligamentsthat were present were expected to be located ventrally(Standring, 2004). As no comparative data exist for thepresence of the glenohumeral ligament in nonhumanprimates, we use humans as a reference in this study.

Limited sample sizes in this study inhibit the abilityto perform statistical analyses on rotator cuff muscula-ture weights. However, percentage contribution of eachmuscle to the entire rotator cuff mass was calculated foreach species to allow comparison. Average adult bodyweights were collected from the literature for all taxaexcept T. syrichta, where the body weight of the speci-men was known, and total rotator cuff muscle mass wascompared to these adult body weight values.

RESULTSRotator Cuff Muscles

Figures 1–4 show the rotator cuff musculature of thefour species in this study. All musculature attached inmanners were previously described (e.g., Murie andMivart, 1872; Woollard, 1925; Jouffroy, 1962). WhereasMurie and Mivart (1872), document the presence of ateres minor muscle in G. crassicaudatus, G. alleni, andsome lorisids and lemurids; this study did not locate thismuscle in any strepsirrhine species (Figs. 1–3). Jouffroy(1962) describes its distinct, clear presence in all prosi-mians, but Woollard (1925) describes this muscle inlemuroids as being only ‘‘feebly’’ present. The teresminor muscle was clearly distinct in the T. syrichta spec-imen used in this study (Fig. 4). Only in this specimen,there was a clear separation between the infraspinatusmuscle and the teres minor muscle; all other species hadmuscle fibers arising from the inferior border of thescapula, as the teres minor muscle is described, butthese fibers were inextricably bound to the infraspinatusmuscle and had no separate tendon of attachment to thegreater tubercle of the humerus (Figs. 1–4).

In general gross appearance, both the supraspinatusand infraspinatus muscles appeared in all specimens asrobust muscles with unipennate fibers. The teres minormuscle in T. syrichta was very small and had unipen-nate fibers. However, the subscapularis muscle in all

682 WRIGHT-FITZGERALD, BALCENIUK, AND BURROWS

specimens appeared as a robust multipennate muscle(Figs. 1–4 for all muscles).

Table 1 and Fig. 5 display the raw weights of individ-ual muscles in the rotator cuff group, and the ratios ofweights of individual rotator cuff muscles to entire mus-cle mass of the rotator cuff. Whereas there is only onespecimen for each species (except G. moholi), it is appa-rent that the subscapularis muscle makes up the major-ity of the rotator cuff muscle mass relative to thesupraspinatus and infraspinatus muscles in all species.In G. moholi and C. medius the infraspinatus and supra-spinatus make up 23.5% and 30%, respectively, of thetotal muscle mass of the rotator cuff. In both T. syrichta

and E. macaco the supraspinatus muscle makes up� 20% of the total mass of the rotator cuff group. Theinfraspinatus muscle of T. syrichta accounts for roughly20% of the total rotator cuff mass, and that of E. macacomakes up 26% of total rotator cuff mass (Fig. 5).

Figures 6,7 display morphology of the acromioclavicu-lar, coracoclavicular, and glenohumeral joints from speci-mens used in this study. All species had anacromioclavicular joint capsule that appeared to begrossly similar to each other and to the acromioclavicu-lar joint capsule of humans (e.g., Standring, 2004).

The coracoclavicular joint was clearly visible in G.moholi and E. macaco as dense connective tissue

Fig. 1. (a) Left upper limb of adult Galago moholi, (b) dorsal view, (c) dorsal view with infraspinatusmuscle visible, and (d) costal view of rotator cuff components.

PROSIMIAN SHOULDER JOINT MORPHOLOGY 683

between the coracoid process of the scapula and thedeep surface of the clavicle (Figs. 6,7). Whereas inhumans it is reported as consisting of two separate liga-ments, the trapezoid and conoid ligaments (Standring,2004); it was observed in this study to be a single unitedband of dense connective tissue. There was no visibledense connective tissue between the coracoid process ofthe scapula and the deep surface of the clavicle in eitherC. medius or T. syrichta.

The glenohumeral joint capsule and associated struc-tures (tendon of the long head of the biceps brachii mus-cle, glenoid labrum, and glenohumeral ligaments) wereclearly visible in most specimens (Figs. 6,7). In all spe-cies, the posterior portion of the glenohumeral joint cap-sule was thickened, where it was reinforced by thetendons of the supraspinatus and infraspinatus muscles(plus the teres minor muscle in T. syrichta). In C. med-ius and E. macaco the anterior portion of the joint

Fig. 2. (a) Right upper limb of adult Tarsius syrichta, (b) dorsalview, (c) dorsal view with infraspinatus muscle visible, (d) costal viewof rotator cuff components, and (e) dorsal view showing teres minormuscle (Tminor). Abbreviations: TB ¼ triceps brachii muscle; LD ¼ lat-

issimus dorsi muscle; SA ¼ serratus anterior muscle; IS ¼ infraspina-tus muscle; IF ¼ infraspinous fossa; BB ¼ biceps brachii muscle;TM ¼ teres major muscle.

684 WRIGHT-FITZGERALD, BALCENIUK, AND BURROWS

capsule was clearly reinforced on the deep surface byglenohumeral ligaments (Fig. 6). Two ligaments werelocated in each of these species. No such ventrallylocated thickenings of the glenohumeral joint capsuleswere found in G. moholi or T. syrichta (Fig. 7).

The glenoid labrum appeared to be similar across spe-cies as a relatively narrow, continuous band of fibrocarti-lage attached to the periphery of the glenoid fossa of thescapula and, rostrally, to the tendon of the long head ofthe biceps brachii muscle (Figs. 6,7). Whereas the lab-rum seems to be similar across these species it appearedto be relatively more ‘‘cup-like’’ in E. macaco than inboth G. moholi and T. syrichta, where it seems to be rel-atively ‘‘flatter.’’

The tendon of the long head of the biceps brachii mus-cle was similar in all species. It traveled through theintertubercular groove of the humerus, pierced the gle-nohumeral joint capsule, and attached into the glenoidlabrum and the supraglenoid tubercle of the scapula.There were no apparent differences among species.

The osteological features of the glenoid fossa, acromionprocess, and proximal portion of the humerus have beenwell documented in numerous primate taxa (Larson,1993, for a review) and are not detailed here. However,it bears mentioning that the coracoid process positionrelative to the humeral head varies among taxa in thisstudy. In E. macaco, the coracoid process covers the ma-jority of the ventral surface of the humeral head (Fig. 7),a condition that is not seen in any other species in thisstudy.

DISCUSSIONRotator Cuff

Primates, relative to other mammals, are noted forrelying primarily on their hindlimbs for propulsion innonsuspensory locomotion relative to forelimbs (Larsonet al., 2000; Schmitt and Lemelin, 2002). Thus, morphol-ogy of forelimb structures cannot be interpreted strictlywith respect to locomotory function as can be done more

Fig. 3. (a) Left upper limb of adult Cheirogaleus medius, (b) dorsal view, and (c) costal view of rotatorcuff components. Abbreviations: LD ¼ latissimus dorsi muscle; Tr ¼ trapezius muscle; SA ¼ serratusanterior muscle; SS ¼ subscapularis muscle; TM ¼ teres major muscle.

PROSIMIAN SHOULDER JOINT MORPHOLOGY 685

heavily with the hindlimb. Instead, primates use theforelimb at least as much in positional, nonlocomotorybehaviors that would likely be under separate selection.In this conceptualization of forelimb adaptive function,morphology of the shoulder joint complex and the rotatorcuff components (musculature and tendons) may reflectpostural and other nonlocomotory behaviors such as foodprocurement and food handling more heavily than loco-motor behaviors (Larson, 1998; Larson et al., 2000;Hanna et al., 2006; Stevens, 2008; Wright et al., 2008).

Results from this study reflect these previous findingsregarding forelimb function and adaptive morphology inprimates. Whereas sample sizes in this study are lim-ited, and we can make some cautious inferences in lightof locomotor style and postural behavior for each speciesused. Comparison of relative contribution of each rotatorcuff muscle to the entire mass of the rotator cuff groupamong species reveals some interesting trends. In allspecies the subscapularis muscle makes up the greatestpercentage of the total rotator cuff mass, a pattern seen

Fig. 4. (a) Right upper limb of adult Eulemur macaco, (b) dorsal view, (c) dorsal view with infraspinatusmuscle visible, and (d) costal view of rotator cuff components. Abbreviations: TR ¼ trapezius muscle;SS ¼ subscapularis muscle.

686 WRIGHT-FITZGERALD, BALCENIUK, AND BURROWS

among many comparative primate studies (Inman et al.,1944; Ashton and Oxnard, 1963; Anapol and Gray, 2003;Hirugashi et al., 2006; Potau et al., 2009). Similar toprevious studies, this study notes the multipennate na-ture of this muscle relative to the unipennate nature ofthe supraspinatus and infraspinatus muscles (and teresminor muscle in T. syrichta).

In quadrupedal primates, the subscapularis musclemedially rotates the shoulder and, perhaps more impor-tantly, stabilizes the glenohumeral joint against theshearing force experienced by the joint capsule duringlocomotion (Tuttle and Basmajian, 1978; Larson andStern, 1987; Larson, 1993). Based On this observation,we would have expected to see the relatively greatest

TABLE 1. Individual muscle masses (in g) of rotator cuff group components (percentage of each musclerelative to entire mass of the rotator cuff muscle group) and percentage of total body weight of the species

accounted for by the rotator cuff mass (RC%)

Species Supraspinatus (%) Infraspinatus (%) Teres Minor (%) Subscapularis (%) RC%

Galago moholi (200 g) 0.16 (30%)a 0.125 (23.5%) NA 0.245 (46.5%) 0.27%Cheirogaleus medius (156 g) 0.18 (30%) 0.14 (23%) NA 0.29 (%) 0.39%Eulemur macaco (2,445 g) 1.08 (19%) 1.52 (26%) NA 3.20 (55%) 0.24%Tarsius syrichta (120 g) 0.08 (20%) 0.08 (20%) 0.005 (x)* 0.25 (60%) 0.34%aValues for all muscles in this species are the average of two specimens: individual weights of supraspinatus muscle �0.19and 0.13 g, infraspinatus muscle �0.13 and 0.12 g, subscapularis muscle �0.26 and 0.23 g. ‘‘*’’: The teres minor muscle ofT. syrichta was so small that it accounts for close to 0% of the total mass of the rotator cuff muscle group (sec also Fig.5).Values in parentheses beside the species name are adult body weight pulled from the literature (G. moholi: Harcount andBearder, 1989; C. medius: Atzeva et al., 2009: E. macaco: Kappeler, 1991) expect for T. syricha. Body weight for this speci-men was known in this study.

Fig. 5. Pie charts showing the relative contributions of each individual muscle of the rotator cuff groupto the entire mass of the rotator cuff group in each species. ‘‘*"–In the figure for T. syrichta, the infraspina-tus muscle is shown as making up 20.5% of the total mass of the rotator cuff group for this species.Here, the diminutive teres minor muscle has been grouped with the infraspinatus muscle component.

PROSIMIAN SHOULDER JOINT MORPHOLOGY 687

subscapularis muscle mass in the quadrupedal species,C. medius and E. macaco. E. macaco did in fact have ahigh relative subscapularis muscle mass (55%) butT. syrichta, a vertical clinger and leaper, had the highestrelative subscapularis muscle mass at 60%. C. mediushad a very low relative subscapularis muscle mass. Lar-son (1988) found that the subscapularis muscle partici-pated in the free arm movements of gibbons, abrachiating suspensory species. Thus, the high percent-age of the subscapularis muscle in E. macaco in thisresults may also reflect their use of suspensory behavior.

Vertical clinging and leaping is not associated in theliterature with a high subscapularis muscle mass, highlevels of medial rotation of the shoulder, or with theneed to support the glenohumeral joint capsule.Although it is possible, the clinging component of thislocomotion category requires medial rotation of theshoulder to hold onto the substrate with the hands,which may explain the high relative subscapularis mus-cle mass in T. syrichta. The other vertical clinger andleaper used in this study, G. moholi, showed the lowestrelative subscapularis muscle mass. However, G. moholiis reported to spend some time on the ground bipedallyhopping (Harcourt and Bearder, 1989) whereas T.syrichta is not reported to engage in this behavior (Gur-sky, 2007). This difference in locomotion may explain the

differences in relative subscapularis muscle massbetween these two vertical clingers and leapers.

The primate supraspinatus and infraspinatus musclesalso act to stabilize the glenohumeral joint but withgreat functional differences otherwise. The infraspinatusmuscle is a lateral rotator of the shoulder joint, an activ-ity important during quadrupedal walking and in sus-pensory behaviors (Whitehead and Larson, 1994;Larson, 1995). In this study, E. macaco had the greatestpercentage attributed to infraspinatus muscle (26%).This may reflect the combination of quadrupedal andsuspensory behavior seen in E. macaco. The supraspina-tus muscle in primates does not seem to have a greatactive role in locomotion but does stabilize the gleno-humeral joint during quadrupedal locomotion, and it isreported to be important in shoulder elevation duringreaching activities (Tuttle and Basmajian, 1978; Larsonand Stern, 1989, 1992). In this study, both G. moholiand C. medius had the greatest percentage of supraspi-natus muscle mass (30%). Whereas quadrupedal walkingmay not involve a great deal of overhead reaching, itmay require stabilization of the glenohumeral joint dur-ing progression along terminal branches (Schmitt andLemelin, 2002; Schmitt, 2003).

Interestingly, E. macaco had the greatest ratio of totalrotator cuff muscle mass relative to body weight among

Fig. 6. Shoulder joint complex structures from (top row) Galagomoholi and (bottom row) Tarsius syrichta. Abbreviations: GL ¼ glenoidlabrum; BB ¼ biceps brachii muscle; AC ¼ acromioclavicular; CC ¼coracoclavicular; GF ¼ glenoid fossa; GH ¼ glenohumeral; SS ¼ sub-

scapularis muscle; HH ¼ humeral head. Unlabeled arrow at bottom of(a) is pointing to the distal portion of the long head of the biceps bra-chii muscle tendon.

688 WRIGHT-FITZGERALD, BALCENIUK, AND BURROWS

all species in this study. This species averages in excessof 2 kg total body mass and is by far the largest animalin this study. Larson (1988) found that gibbons have ahigh participation of the subscapularis muscle in suspen-sion activities. It is possible that E. macaco is using notonly the subscapularis muscle for suspension in a simi-lar manner but, being so large, has a higher relative ro-tator cuff muscle mass to stabilize the glenohumeraljoint from distraction because of the suspension of itsgreat body weight.

Finally, this study did not locate any independentteres minor muscle in any species except for T. syrichta,contrary to previous reports (e.g., Murie and Mivart,1872; Jouffroy, 1962). In this study, the more caudal as-pect of the infraspinatus muscle did appear to be some-what separated from the remaining portion of themuscle (Figs. 1, 3, and 4) but this semi-independent por-tion always attached onto the greater tubercle of the hu-merus with the tendon of the infraspinatus musclerather than separately onto the greater tubercle whereteres minor is reported to insert in related taxa(e.g.,Swindler and Wood, 1982). Thus, this cannot be

considered a separate teres minor muscle. Findings of aseparate teres minor muscle in galagos and lemurs inprevious studies may be because of individual variationwithin these taxa or to phylogenetic factors. Tarsius isroutinely problematic in phylogenetic analyses, beingplaced either in Haplorrhini with monkeys and apes orin Prosimii with lorises and lemurs (Le Gros Clark,1949; Groves, 2001). All monkeys and apes for which therotator cuff has been studied are reported to possess adistinct teres minor muscle (e.g., Ashton and Oxnard,1963; Swindler and Wood, 1982). The presence of a dis-tinct teres minor muscle in T. syrichta may be a phyloge-netically valuable character in the placement of Tarsius,possibly strengthening the case for its inclusion withmonkeys and apes with the Haplorrhini.

As a concluding remark to this section, it must beremembered that almost all studies on primate rotatorcuff function and gait have been done on anthropoids,not on prosimians (e.g., Tuttle and Basmajian, 1978;Larson and Stern, 1987, 1989, 1992; Whitehead and Lar-son, 1994). It is possible that the biomechanical infer-ences afforded by these previous studies do not apply to

Fig. 7. Shoulder joint complex structures from (top row) Cheiroga-leus medius and (bottom row) Eulemur macaco. Abbreviations: GF ¼glenoid fossa; HH ¼ humeral head; SS ¼ subscapularis muscle; AC ¼acromioclavicular; BB ¼ biceps brachii muscle; TB ¼ triceps brachii

muscle. Unlabeled arrow in (a) is pointing to the acromioclavicularjoint capsule; unlabeled arrows in (b) are pointing to the glenoid lab-rum; asterisks (*) indicate the position of the glenohumeral ligamentsin (a) and (d).

PROSIMIAN SHOULDER JOINT MORPHOLOGY 689

the results of this study. Future studies that concentratespecifically on prosimians are necessary to definitivelyinterpret the present results on the rotator cuff musclegroup.

Joint Structure

This study provides the first comparative data on thesoft-tissue structures of the glenohumeral, acromiocla-vicular, and coracoclavicular joints in primates. Whereasprevious studies have demonstrated that osseous mor-phology of the scapula, clavicle, and proximal part of thehumerus is adaptive to locomotory and postural styles;this study found mixed results in the adaptive soft-tissuemorphology of the shoulder joint complex.

The capsules of the acromioclavicular joint were with-out apparent variation among species, and the structureof this joint was very similar to that seen in humans(e.g., Standring, 2004). Differing locomotor and posturalbehaviors (arboreal quadrupedalism, suspension, andleaping) and phylogenetic position did not appear to beassociated with variation in this joint.

The coracoclavicular joint was noted only in G. moholiand E. macaco in this study. In these species the coraco-clavicular ligament was observed as a single band ofdense connective tissue, unlike the condition in humanswhere it consists of two separate bands, the trapezoidand conoid ligaments (Standring, 2004). G. moholi andE. macaco practice very different locomotor and posturalbehaviors and are phylogenetically divergent. The appa-rent lack of this ligament in C. medius and T. syrichtain this study cannot be explained at this time, and wehave no reason to believe that our dissection methodsfailed to locate an existing structure. The coracoclavicu-lar ligament in humans prevents excessive rotation ofthe clavicle away from the scapula (Standring, 2004),but its function in nonhuman primates is uncertain. If itacts similarly in nonhuman primates, its apparentlyunique presence in one leaper and one quadruped to theexclusion of the other leaper and quadruped is mysteri-ous. An increased sample size may help to answer thisquestion.

The glenohumeral joint capsule did vary both amongspecies and among locomotor/postural behaviors. Dor-sally, the capsule was similar among species and was re-inforced by tendons of the supraspinatus andinfraspinatus muscles (and of the teres minor muscle inT. syrichta). Ventrally, it was reinforced by the tendon ofthe subscapularis muscle. Additionally, glenohumeralligaments were located in the two quadrupedal species,C. medius and E. macaco, and may act as joint stabil-izers. These ligaments were not found in the clingingand leaping species, G. moholi and T. syrichta. Leapingin these species involves landing with the hindlimb firstand using the forelimbs primarily in ‘‘clinging’’ and pro-curing insects for food. Glenohumeral joint stabilizationon the ventral surface may not be as important in verti-cal clinging and leaping activities as in quadrupedalactivities where there is a great amount of shearingforce on the joint capsule (Tuttle and Basmajian, 1978;Larson and Stern, 1987; Larson, 1993).

The course and attachment of the tendon from thelong head of the biceps brachii muscle did not varyamong species and appeared to be similar to humanmorphology. As in humans, it may be adapted for stabi-

lizing the position of the humeral head in overheadactivities (Standring, 2004).

Lastly, the glenoid labrum appeared to vary amongthe species from this study. In E. macaco the labrumappeared to be more ‘‘cup-like,’’ creating a deeper articu-lating site for the humeral head than in G. moholi, T.syrichta, and C. medius (Figs. 6,7). Such a deeper articu-lating surface may increase the stability of the gleno-humeral joint during activities that would distract thehumeral head from the glenoid fossa such as suspensorybehavior (e.g., Roberts, 1974).

CONCLUSIONS

Overall, this study found that individual muscle massof the rotator cuff muscle components in the prosimianspecies used are generally reflective of locomotor andpostural behavior. However, the nonosseous componentsof the shoulder joint complex present a mixed bag ofboth adaptive and nonadaptive morphologies. This maybe due to the limited sample size in this study, but itmay also indicate that soft-tissue joint structures arehighly conserved throughout phylogeny and are not sub-jected to evolutionary selection in the same manner asosseous characters. Future studies using expanded pri-mate taxa with larger sample sizes should be carried outto further explore the question of adaptive morphologyof the primate shoulder joint complex.

ACKNOWLEDGMENTS

The authors wish to thank Jason Organ for his kindinvitation to submit this article. The authors thank thetwo reviewers for their comments that greatly enhancedthe quality of this manuscript. The authors also wish tothank Leanne Nash and Tim Smith for useful discussionon drafts of this manuscript. This is Duke Lemur Centerpublication # 1166.

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