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Shouldering the Burdens of Locomotion and PostureGlenohumeral Joint Structure in Prosimians.

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THE ANATOMICAL RECORD 293:680–691 (2010)
Shouldering the Burdens of Locomotion
and Posture: Glenohumeral Joint
Structure in Prosimians
ADRIAN S. WRIGHT-FITZGERALD,1,2 MARK D. BALCENIUK,3
3,4*
AND ANNE M. BURROWS
1
Department of Health Sciences, Sargent College of Health and Rehabilitation Sciences,
Boston University, Boston, Massachusetts
2
Department of Athletic Training, Duquesne University, Pittsburgh, Pennsylvania
3
Department of Physical Therapy, Duquesne University, Pittsburgh, Pennsylvania
4
Department of Anthropology, University of Pittsburgh, Pittsburgh, Pennsylvania
ABSTRACT
Despite its importance in movement of the upper limb, the soft-tissue
morphology of the shoulder joint complex (the acromioclavicular, coracoclavicular, and glenohumeral joints) across primates is poorly understood. This
study compares soft-tissue morphology of these three shoulder joint components among broad phylogenetic, locomotor, and postural behavior ranges
in prosimian primates. Two adult specimens of Galago moholi (a vertical
clinger and leaper) were dissected for study, along with one adult each of
Cheirogaleus medius (an arboreal quadruped), Eulemur macaco (an arboreal quadruped that also frequently engages in suspensory behavior), and
Tarsius syrichta (a vertical clinger and leaper). Because of their role in glenohumeral joint movement and stabilization, the rotator cuff muscles were
also dissected and weighed among the species. Results showed that muscle
mass of individual components of the rotator cuff musculature may be
adaptive to locomotor and postural behaviors of the taxa in this study. Two
soft-tissue components of the glenohumeral joint, but not the acromioclavicular and coracoclavicular joints, were also considered adaptive. The quadrupedal species, C. medius and E. macaco, both had glenohumeral ligaments
and E. macaco had a relatively deeper glenoid articular surface for the humerus because of the shape of the glenoid labrum. Additionally, this study
noted a lack of a teres minor muscle in G. moholi, C. medius, and E. macaco despite previous studies describing them. A relatively robust teres
minor muscle was found in T. syrichta. Even with the limited sample dissected here, these results suggest that soft-tissue joint morphology itself
may be as adaptive to locomotory and postural styles as osseous morpholC 2010 Wiley-Liss, Inc.
ogy. Anat Rec, 293:680–691, 2010. V
Key words: rotator cuff; shoulder joint; tarsier; Cheirogaleus;
Galago; Tarsius; Eulemur
INTRODUCTION
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). AdditionC 2010 WILEY-LISS, INC.
V
*Correspondence to: Dr. Anne M. Burrows, Department of
Physical 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.21127
Published online in Wiley InterScience (www.interscience.wiley.
com).
PROSIMIAN SHOULDER JOINT MORPHOLOGY
ally, 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 recon-
681
structing 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).
682
WRIGHT-FITZGERALD, BALCENIUK, AND BURROWS
T. syrichta, like other tarsiers, feeds primarily on invertebrates and is not reported to use any quadrupedal or
suspensory behaviors.
Study Aims
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.
MATERIALS AND METHODS
Two adult cadaveric specimens of G. moholi, and one
adult specimen each of C. medius, E. macaco, and T.
syrichta were dissected for study. All specimens were
acquired from Duke Lemur Center/Duke University Primate Center, where they were kept in a seminatural
environment. All animals died of natural causes. After
death, each cadaver was immersed in 10% buffered formalin and stored in this fashion.
All dissections were done on either the right or left
upper limb, depending upon availability and condition,
and were carried out using 2.5x magnifying loupes
except for E. macaco, which was large enough to be dissected without magnifiers. Using microdissection tools,
skin and superficial fascia was excised away from the
shoulder region to reveal the dorsally located rotator
cuff muscles. All other dorsally located musculature
attaching to the scapula around the rotator cuff muscles
was dissected away (i.e., latissimus dorsi, trapezius, and
deltoid muscles). Whereas the latissimus dorsi muscle
was not attached to the scapula in any species used in
this study (Jouffroy, 1962); it was in the general region
of interest and was cleared for an unobstructed view of
the rotator cuff area. Muscle identification followed
Murie and Mivart (1872), Woollard (1925), and Jouffroy
(1962). Once the rotator cuff muscles were located, the
upper limb was disarticulated from the trunk by cutting
through the midpoint of the clavicle with scissors and
cutting connections between the scapula and the rhomboid, latissimus dorsi, serratus anterior, trapezius, pectoralis major, and pectoralis minor muscles. In this
fashion, all rotator cuff muscles plus the teres major
muscles were left attached to the scapula and humerus
(Figs. 1,2).
All rotator cuff muscles were detached individually
from their scapular and humeral attachments using
microdissection tools and then blotted dry using a paper
towel (Atzeva et al., 2007). Weights were recorded to the
nearest 0.01 g using a digital Ohaus Analytical Plus
scale.
The acromioclavicular joint was dissected free from
overlying musculature (deltoid and trapezius muscles) so
that the joint capsule was visible. The coracoclavicular
joint/ligament was defined from surrounding fascia and
the subclavius muscle, and the glenohumeral joint capsule was defined both dorsally and ventrally in a similar
fashion. The tendon of the long head of the biceps brachii muscle was followed through the glenohumeral joint
capsule. The joint capsule was opened in all specimens
to view the internal aspect of the glenohumeral joint,
glenoid labrum, glenohumeral ligaments, and termination of the tendon of the long head of the biceps brachii
muscle. The joint capsule was opened by cutting longitudinally through the dorsal surface of the joint capsule
using microdissection tools. Once the joint capsule was
excised, the humeral head was rotated away from the
glenoid fossa of the scapula so that the ventral portion
of the capsule, glenoid labrum, and termination of the
tendon of the long head of the biceps brachii muscle
were visible. The dorsal portion of the capsule was chosen for incision because any glenohumeral ligaments
that were present were expected to be located ventrally
(Standring, 2004). As no comparative data exist for the
presence of the glenohumeral ligament in nonhuman
primates, we use humans as a reference in this study.
Limited sample sizes in this study inhibit the ability
to perform statistical analyses on rotator cuff musculature weights. However, percentage contribution of each
muscle to the entire rotator cuff mass was calculated for
each species to allow comparison. Average adult body
weights were collected from the literature for all taxa
except T. syrichta, where the body weight of the specimen was known, and total rotator cuff muscle mass was
compared to these adult body weight values.
RESULTS
Rotator Cuff Muscles
Figures 1–4 show the rotator cuff musculature of the
four species in this study. All musculature attached in
manners were previously described (e.g., Murie and
Mivart, 1872; Woollard, 1925; Jouffroy, 1962). Whereas
Murie and Mivart (1872), document the presence of a
teres minor muscle in G. crassicaudatus, G. alleni, and
some lorisids and lemurids; this study did not locate this
muscle in any strepsirrhine species (Figs. 1–3). Jouffroy
(1962) describes its distinct, clear presence in all prosimians, but Woollard (1925) describes this muscle in
lemuroids as being only ‘‘feebly’’ present. The teres
minor muscle was clearly distinct in the T. syrichta specimen used in this study (Fig. 4). Only in this specimen,
there was a clear separation between the infraspinatus
muscle and the teres minor muscle; all other species had
muscle fibers arising from the inferior border of the
scapula, as the teres minor muscle is described, but
these fibers were inextricably bound to the infraspinatus
muscle and had no separate tendon of attachment to the
greater tubercle of the humerus (Figs. 1–4).
In general gross appearance, both the supraspinatus
and infraspinatus muscles appeared in all specimens as
robust muscles with unipennate fibers. The teres minor
muscle in T. syrichta was very small and had unipennate fibers. However, the subscapularis muscle in all
PROSIMIAN SHOULDER JOINT MORPHOLOGY
683
Fig. 1. (a) Left upper limb of adult Galago moholi, (b) dorsal view, (c) dorsal view with infraspinatus
muscle visible, and (d) costal view of rotator cuff components.
specimens appeared as a robust multipennate muscle
(Figs. 1–4 for all muscles).
Table 1 and Fig. 5 display the raw weights of individual muscles in the rotator cuff group, and the ratios of
weights of individual rotator cuff muscles to entire muscle mass of the rotator cuff. Whereas there is only one
specimen for each species (except G. moholi), it is apparent that the subscapularis muscle makes up the majority of the rotator cuff muscle mass relative to the
supraspinatus and infraspinatus muscles in all species.
In G. moholi and C. medius the infraspinatus and supraspinatus make up 23.5% and 30%, respectively, of the
total 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. The
infraspinatus muscle of T. syrichta accounts for roughly
20% of the total rotator cuff mass, and that of E. macaco
makes up 26% of total rotator cuff mass (Fig. 5).
Figures 6,7 display morphology of the acromioclavicular, coracoclavicular, and glenohumeral joints from specimens used in this study. All species had an
acromioclavicular joint capsule that appeared to be
grossly similar to each other and to the acromioclavicular joint capsule of humans (e.g., Standring, 2004).
The coracoclavicular joint was clearly visible in G.
moholi and E. macaco as dense connective tissue
684
WRIGHT-FITZGERALD, BALCENIUK, AND BURROWS
Fig. 2. (a) Right upper limb of adult Tarsius syrichta, (b) dorsal
view, (c) dorsal view with infraspinatus muscle visible, (d) costal view
of rotator cuff components, and (e) dorsal view showing teres minor
muscle (Tminor). Abbreviations: TB ¼ triceps brachii muscle; LD ¼ lat-
issimus dorsi muscle; SA ¼ serratus anterior muscle; IS ¼ infraspinatus muscle; IF ¼ infraspinous fossa; BB ¼ biceps brachii muscle;
TM ¼ teres major muscle.
between the coracoid process of the scapula and the
deep surface of the clavicle (Figs. 6,7). Whereas in
humans it is reported as consisting of two separate ligaments, the trapezoid and conoid ligaments (Standring,
2004); it was observed in this study to be a single united
band of dense connective tissue. There was no visible
dense connective tissue between the coracoid process of
the scapula and the deep surface of the clavicle in either
C. medius or T. syrichta.
The glenohumeral joint capsule and associated structures (tendon of the long head of the biceps brachii muscle, glenoid labrum, and glenohumeral ligaments) were
clearly visible in most specimens (Figs. 6,7). In all species, the posterior portion of the glenohumeral joint capsule was thickened, where it was reinforced by the
tendons of the supraspinatus and infraspinatus muscles
(plus the teres minor muscle in T. syrichta). In C. medius and E. macaco the anterior portion of the joint
685
PROSIMIAN SHOULDER JOINT MORPHOLOGY
Fig. 3. (a) Left upper limb of adult Cheirogaleus medius, (b) dorsal view, and (c) costal view of rotator
cuff components. Abbreviations: LD ¼ latissimus dorsi muscle; Tr ¼ trapezius muscle; SA ¼ serratus
anterior muscle; SS ¼ subscapularis muscle; TM ¼ teres major muscle.
capsule was clearly reinforced on the deep surface by
glenohumeral ligaments (Fig. 6). Two ligaments were
located in each of these species. No such ventrally
located thickenings of the glenohumeral joint capsules
were found in G. moholi or T. syrichta (Fig. 7).
The glenoid labrum appeared to be similar across species as a relatively narrow, continuous band of fibrocartilage attached to the periphery of the glenoid fossa of the
scapula and, rostrally, to the tendon of the long head of
the biceps brachii muscle (Figs. 6,7). Whereas the labrum seems to be similar across these species it appeared
to be relatively more ‘‘cup-like’’ in E. macaco than in
both G. moholi and T. syrichta, where it seems to be relatively ‘‘flatter.’’
The tendon of the long head of the biceps brachii muscle was similar in all species. It traveled through the
intertubercular groove of the humerus, pierced the glenohumeral joint capsule, and attached into the glenoid
labrum and the supraglenoid tubercle of the scapula.
There were no apparent differences among species.
The osteological features of the glenoid fossa, acromion
process, and proximal portion of the humerus have been
well documented in numerous primate taxa (Larson,
1993, for a review) and are not detailed here. However,
it bears mentioning that the coracoid process position
relative to the humeral head varies among taxa in this
study. In E. macaco, the coracoid process covers the majority of the ventral surface of the humeral head (Fig. 7),
a condition that is not seen in any other species in this
study.
DISCUSSION
Rotator Cuff
Primates, relative to other mammals, are noted for
relying primarily on their hindlimbs for propulsion in
nonsuspensory locomotion relative to forelimbs (Larson
et al., 2000; Schmitt and Lemelin, 2002). Thus, morphology of forelimb structures cannot be interpreted strictly
with respect to locomotory function as can be done more
686
WRIGHT-FITZGERALD, BALCENIUK, AND BURROWS
Fig. 4. (a) Right upper limb of adult Eulemur macaco, (b) dorsal view, (c) dorsal view with infraspinatus
muscle visible, and (d) costal view of rotator cuff components. Abbreviations: TR ¼ trapezius muscle;
SS ¼ subscapularis muscle.
heavily with the hindlimb. Instead, primates use the
forelimb at least as much in positional, nonlocomotory
behaviors that would likely be under separate selection.
In this conceptualization of forelimb adaptive function,
morphology of the shoulder joint complex and the rotator
cuff components (musculature and tendons) may reflect
postural and other nonlocomotory behaviors such as food
procurement and food handling more heavily than locomotor behaviors (Larson, 1998; Larson et al., 2000;
Hanna et al., 2006; Stevens, 2008; Wright et al., 2008).
Results from this study reflect these previous findings
regarding forelimb function and adaptive morphology in
primates. Whereas sample sizes in this study are limited, and we can make some cautious inferences in light
of locomotor style and postural behavior for each species
used. Comparison of relative contribution of each rotator
cuff muscle to the entire mass of the rotator cuff group
among species reveals some interesting trends. In all
species the subscapularis muscle makes up the greatest
percentage of the total rotator cuff mass, a pattern seen
687
PROSIMIAN SHOULDER JOINT MORPHOLOGY
TABLE 1. Individual muscle masses (in g) of rotator cuff group components (percentage of each muscle
relative 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 (%)
Galago moholi (200 g)
Cheirogaleus medius (156 g)
Eulemur macaco (2,445 g)
Tarsius syrichta (120 g)
0.16
0.18
1.08
0.08
(30%)
(30%)
(19%)
(20%)
a
Infraspinatus (%)
0.125
0.14
1.52
0.08
(23.5%)
(23%)
(26%)
(20%)
Teres Minor (%)
NA
NA
NA
0.005 (x)*
Subscapularis (%)
0.245
0.29
3.20
0.25
(46.5%)
(%)
(55%)
(60%)
RC%
0.27%
0.39%
0.24%
0.34%
Values for all muscles in this species are the average of two specimens: individual weights of supraspinatus muscle 0.19
and 0.13 g, infraspinatus muscle 0.13 and 0.12 g, subscapularis muscle 0.26 and 0.23 g. ‘‘*’’: The teres minor muscle of
T. 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 and
Bearder, 1989; C. medius: Atzeva et al., 2009: E. macaco: Kappeler, 1991) expect for T. syricha. Body weight for this specimen was known in this study.
a
Fig. 5. Pie charts showing the relative contributions of each individual muscle of the rotator cuff group
to the entire mass of the rotator cuff group in each species. ‘‘*"–In the figure for T. syrichta, the infraspinatus 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.
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 to
previous studies, this study notes the multipennate nature of this muscle relative to the unipennate nature of
the supraspinatus and infraspinatus muscles (and teres
minor muscle in T. syrichta).
In quadrupedal primates, the subscapularis muscle
medially rotates the shoulder and, perhaps more importantly, stabilizes the glenohumeral joint against the
shearing force experienced by the joint capsule during
locomotion (Tuttle and Basmajian, 1978; Larson and
Stern, 1987; Larson, 1993). Based On this observation,
we would have expected to see the relatively greatest
688
WRIGHT-FITZGERALD, BALCENIUK, AND BURROWS
Fig. 6. Shoulder joint complex structures from (top row) Galago
moholi and (bottom row) Tarsius syrichta. Abbreviations: GL ¼ glenoid
labrum; BB ¼ biceps brachii muscle; AC ¼ acromioclavicular; CC ¼
coracoclavicular; 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 brachii muscle tendon.
subscapularis muscle mass in the quadrupedal species,
C. medius and E. macaco. E. macaco did in fact have a
high relative subscapularis muscle mass (55%) but
T. syrichta, a vertical clinger and leaper, had the highest
relative subscapularis muscle mass at 60%. C. medius
had a very low relative subscapularis muscle mass. Larson (1988) found that the subscapularis muscle participated in the free arm movements of gibbons, a
brachiating suspensory species. Thus, the high percentage of the subscapularis muscle in E. macaco in this
results may also reflect their use of suspensory behavior.
Vertical clinging and leaping is not associated in the
literature with a high subscapularis muscle mass, high
levels of medial rotation of the shoulder, or with the
need to support the glenohumeral joint capsule.
Although it is possible, the clinging component of this
locomotion category requires medial rotation of the
shoulder to hold onto the substrate with the hands,
which may explain the high relative subscapularis muscle mass in T. syrichta. The other vertical clinger and
leaper used in this study, G. moholi, showed the lowest
relative subscapularis muscle mass. However, G. moholi
is reported to spend some time on the ground bipedally
hopping (Harcourt and Bearder, 1989) whereas T.
syrichta is not reported to engage in this behavior (Gursky, 2007). This difference in locomotion may explain the
differences in relative subscapularis muscle mass
between these two vertical clingers and leapers.
The primate supraspinatus and infraspinatus muscles
also act to stabilize the glenohumeral joint but with
great functional differences otherwise. The infraspinatus
muscle is a lateral rotator of the shoulder joint, an activity important during quadrupedal walking and in suspensory behaviors (Whitehead and Larson, 1994;
Larson, 1995). In this study, E. macaco had the greatest
percentage attributed to infraspinatus muscle (26%).
This may reflect the combination of quadrupedal and
suspensory behavior seen in E. macaco. The supraspinatus muscle in primates does not seem to have a great
active role in locomotion but does stabilize the glenohumeral joint during quadrupedal locomotion, and it is
reported to be important in shoulder elevation during
reaching activities (Tuttle and Basmajian, 1978; Larson
and Stern, 1989, 1992). In this study, both G. moholi
and C. medius had the greatest percentage of supraspinatus muscle mass (30%). Whereas quadrupedal walking
may not involve a great deal of overhead reaching, it
may require stabilization of the glenohumeral joint during progression along terminal branches (Schmitt and
Lemelin, 2002; Schmitt, 2003).
Interestingly, E. macaco had the greatest ratio of total
rotator cuff muscle mass relative to body weight among
PROSIMIAN SHOULDER JOINT MORPHOLOGY
689
Fig. 7. Shoulder joint complex structures from (top row) Cheirogaleus medius and (bottom row) Eulemur macaco. Abbreviations: GF ¼
glenoid fossa; HH ¼ humeral head; SS ¼ subscapularis muscle; AC ¼
acromioclavicular; BB ¼ biceps brachii muscle; TB ¼ triceps brachii
muscle. Unlabeled arrow in (a) is pointing to the acromioclavicular
joint capsule; unlabeled arrows in (b) are pointing to the glenoid labrum; asterisks (*) indicate the position of the glenohumeral ligaments
in (a) and (d).
all species in this study. This species averages in excess
of 2 kg total body mass and is by far the largest animal
in this study. Larson (1988) found that gibbons have a
high participation of the subscapularis muscle in suspension activities. It is possible that E. macaco is using not
only the subscapularis muscle for suspension in a similar manner but, being so large, has a higher relative rotator cuff muscle mass to stabilize the glenohumeral
joint from distraction because of the suspension of its
great body weight.
Finally, this study did not locate any independent
teres 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 aspect of the infraspinatus muscle did appear to be somewhat separated from the remaining portion of the
muscle (Figs. 1, 3, and 4) but this semi-independent portion always attached onto the greater tubercle of the humerus with the tendon of the infraspinatus muscle
rather than separately onto the greater tubercle where
teres 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 a
separate teres minor muscle in galagos and lemurs in
previous studies may be because of individual variation
within these taxa or to phylogenetic factors. Tarsius is
routinely problematic in phylogenetic analyses, being
placed either in Haplorrhini with monkeys and apes or
in Prosimii with lorises and lemurs (Le Gros Clark,
1949; Groves, 2001). All monkeys and apes for which the
rotator cuff has been studied are reported to possess a
distinct teres minor muscle (e.g., Ashton and Oxnard,
1963; Swindler and Wood, 1982). The presence of a distinct teres minor muscle in T. syrichta may be a phylogenetically valuable character in the placement of Tarsius,
possibly strengthening the case for its inclusion with
monkeys and apes with the Haplorrhini.
As a concluding remark to this section, it must be
remembered that almost all studies on primate rotator
cuff 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 Larson, 1994). It is possible that the biomechanical inferences afforded by these previous studies do not apply to
690
WRIGHT-FITZGERALD, BALCENIUK, AND BURROWS
the results of this study. Future studies that concentrate
specifically on prosimians are necessary to definitively
interpret the present results on the rotator cuff muscle
group.
Joint Structure
This study provides the first comparative data on the
soft-tissue structures of the glenohumeral, acromioclavicular, and coracoclavicular joints in primates. Whereas
previous studies have demonstrated that osseous morphology of the scapula, clavicle, and proximal part of the
humerus is adaptive to locomotory and postural styles;
this study found mixed results in the adaptive soft-tissue
morphology of the shoulder joint complex.
The capsules of the acromioclavicular joint were without apparent variation among species, and the structure
of this joint was very similar to that seen in humans
(e.g., Standring, 2004). Differing locomotor and postural
behaviors (arboreal quadrupedalism, suspension, and
leaping) and phylogenetic position did not appear to be
associated with variation in this joint.
The coracoclavicular joint was noted only in G. moholi
and E. macaco in this study. In these species the coracoclavicular ligament was observed as a single band of
dense connective tissue, unlike the condition in humans
where it consists of two separate bands, the trapezoid
and conoid ligaments (Standring, 2004). G. moholi and
E. macaco practice very different locomotor and postural
behaviors and are phylogenetically divergent. The apparent lack of this ligament in C. medius and T. syrichta
in this study cannot be explained at this time, and we
have no reason to believe that our dissection methods
failed to locate an existing structure. The coracoclavicular ligament in humans prevents excessive rotation of
the clavicle away from the scapula (Standring, 2004),
but its function in nonhuman primates is uncertain. If it
acts similarly in nonhuman primates, its apparently
unique presence in one leaper and one quadruped to the
exclusion of the other leaper and quadruped is mysterious. An increased sample size may help to answer this
question.
The glenohumeral joint capsule did vary both among
species and among locomotor/postural behaviors. Dorsally, the capsule was similar among species and was reinforced by tendons of the supraspinatus and
infraspinatus muscles (and of the teres minor muscle in
T. syrichta). Ventrally, it was reinforced by the tendon of
the subscapularis muscle. Additionally, glenohumeral
ligaments were located in the two quadrupedal species,
C. medius and E. macaco, and may act as joint stabilizers. These ligaments were not found in the clinging
and leaping species, G. moholi and T. syrichta. Leaping
in these species involves landing with the hindlimb first
and using the forelimbs primarily in ‘‘clinging’’ and procuring insects for food. Glenohumeral joint stabilization
on the ventral surface may not be as important in vertical clinging and leaping activities as in quadrupedal
activities where there is a great amount of shearing
force on the joint capsule (Tuttle and Basmajian, 1978;
Larson and Stern, 1987; Larson, 1993).
The course and attachment of the tendon from the
long head of the biceps brachii muscle did not vary
among species and appeared to be similar to human
morphology. As in humans, it may be adapted for stabi-
lizing the position of the humeral head in overhead
activities (Standring, 2004).
Lastly, the glenoid labrum appeared to vary among
the species from this study. In E. macaco the labrum
appeared to be more ‘‘cup-like,’’ creating a deeper articulating site for the humeral head than in G. moholi, T.
syrichta, and C. medius (Figs. 6,7). Such a deeper articulating surface may increase the stability of the glenohumeral joint during activities that would distract the
humeral head from the glenoid fossa such as suspensory
behavior (e.g., Roberts, 1974).
CONCLUSIONS
Overall, this study found that individual muscle mass
of the rotator cuff muscle components in the prosimian
species used are generally reflective of locomotor and
postural behavior. However, the nonosseous components
of the shoulder joint complex present a mixed bag of
both adaptive and nonadaptive morphologies. This may
be due to the limited sample size in this study, but it
may also indicate that soft-tissue joint structures are
highly conserved throughout phylogeny and are not subjected to evolutionary selection in the same manner as
osseous characters. Future studies using expanded primate taxa with larger sample sizes should be carried out
to further explore the question of adaptive morphology
of the primate shoulder joint complex.
ACKNOWLEDGMENTS
The authors wish to thank Jason Organ for his kind
invitation to submit this article. The authors thank the
two reviewers for their comments that greatly enhanced
the quality of this manuscript. The authors also wish to
thank Leanne Nash and Tim Smith for useful discussion
on drafts of this manuscript. This is Duke Lemur Center
publication # 1166.
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