ANTHROPOLOGICAL SCIENCE Vol. 115, 17–23, 2007

Glenohumeral joint surface characters and its relation to forelimb suspensory behavior in three ateline , Ateles, Lagothrix, and Alouatta Miyuki KAGAYA1*

1Laboratory of Physical Anthropology, Department of Zoology, Graduate School of Science, Kyoto University, Kitashirakawa, Oiwake-cho, Sakyo-ku, Kyoto, 606-8502 Japan

Received 9 December 2004; accepted 3 June 2006

Abstract Intergeneric morphological variation of the glenohumeral joint surface was investigated among three ateline genera (Ateles, Lagothrix, Alouatta) and compared with Cebus (an ancestral mor- photype of atelines) and Hylobates (a specialized brachiator) to reveal characters associated with fore- limb suspensory behavior. Seventy-six skeletal specimens were examined, and articular surface curvature was measured by a three-dimensional digitizer. It was found that Ateles exhibits joint fea- tures distinct from the other atelines, but resembles Hylobates in its large breadth–length ratio of the glenoid surface and the humeral head, a relatively spherical humeral head, and a dorsoventrally exten- sive humeral head relative to the glenoid surface. These morphologies are likely to be related to bra- chiation, rather than to climbing behavior. A dorsoventrally extensive glenohumeral joint is interpreted to facilitate an increased stride length during brachiation. Lagothrix was found to show many primitive features that are shared with Alouatta in spite of its forelimb suspensory behavior. This may be related to the less specialized mode of forelimb suspensory behavior in Lagothrix compared with Ateles. Those characters that apparently correspond to dependency on suspensory behavior can be useful in interpreting the positional behavior of extinct taxa.

Key words: glenohumeral joint morphology, atelines, hominoids, forelimb suspensory behavior

Introduction argued that climbing behaviors could account for these traits. On the other hand, Gebo (1996) reported that the Members of the subfamily Atelinae adopt forelimb sus- unique morphological pattern shared by the living apes and pensory behavior to varying degrees, while they overlap in Atelini (atelines except Alouatta, which almost never sus- body size and habitat preferences (Terborgh, 1983; Strier, pends by its forelimbs) could largely be explained by fore- 1992). Among the ateline genera, Ateles stands out in its limb suspension and brachiation. While the study by Gebo high frequency of suspensory behavior, especially brachia- (1996) supports the brachiation hypothesis for the similari- tion, compared with Alouatta and Lagothrix (Cant, 1986; ties between Atelini and hominoid forelimb morphology, Cant et al., 2001, 2003). Ateles shares many features of fore- this claim needs to be further verified. First, Gebo’s (1996) limb and trunk morphology with extant hominoids (Erikson, analysis was largely qualitative with little quantitative and 1963; Andrews and Grove, 1976; Larson, 1998). Multi- statistical analyses for support. Second, he treated Alouatta variate analysis revealed that Ateles has a more hominoid-like as exhibiting a quadrupedal climbing condition ancestral to forelimb morphology than is the case with cercopithecoids atelines, thereby evaluating the presumed derived features of (Ashton et al., 1965, 1971; Corruccini and Ciochon, 1978; Ateles from that perspective. This procedure may lead to Takahashi, 1990; McCrossin et al., 1998; Young, 2003). erroneous evaluations because it neglects the possibility that Although many researchers agree that the shared features Alouatta may be derived in some features, perhaps related to of the forelimb and trunk of Ateles and extant hominoids are its distinctive and deliberate quadrupedalism (Rosenberger related to joint mobility, opinions differ regarding whether and Strier, 1989). such features should be attributed to brachiating or climbing Among the atelines, Lagothrix shows intermediate condi- locomotor behavior (Andrews and Grove, 1976; Sarmiento, tions in its trunk and forelimb morphology, and is considered 1995, 2002; Gebo, 1996). For example, Sarmiento (1995) closest to the morphotype of the last common ancestor of pointed out that many of the shared ateline and hominoid atelines (Erikson, 1963; Rosenberger and Strier, 1989). traits, but not all, are observed in lorisines and sloths, and Lagothrix engages in a significant amount of tail-assisted forelimb suspensory behavior, and shows similar frequen- * Corresponding author. e-mail: [email protected] cies of climbing and leaping as Ateles (Defler, 1999). How- phone: +81-75-7534094; fax: +81-75-7534083 ever, the frequency of forelimb suspensory behavior in Published online 8 August 2006 Lagothrix is about half that of Ateles [11% versus 23% of in J-STAGE (www.jstage.jst.go.jp) DOI: 10.1537/ase.041209 total activity time, respectively (Cant et al., 2001)]. More-

© 2006 The Anthropological Society of Nippon 17 18 M. KAGAYA ANTHROPOLOGICAL SCIENCE over, most modes of brachiating locomotion in Lagothrix are half-stride (non-consecutive) brachiation (Cant et al., 2003). Alouatta seldom suspends itself using its forelimb(s) and, compared with Ateles and Lagothrix, more exclusively pre- fers above-branch quadrupedal locomotor modes (Mendel, 1976; Schön Ybarra and Schön, 1987; Gebo, 1992). In the present study, I undertook a quantitative compari- son of the forelimb morphology of Ateles, Lagothrix, and Alouatta with the specific aim of detecting derived charac- teristics related to forelimb suspensory behavior. In addition to the three ateline genera, Cebus and Hylobates were included in the analysis as outgroups. Cebus is a generalized arboreal quadruped (Gebo, 1992), with forelimb myology considered to be primitive in platyrrhines (Dunlap et al., 1985) and a prehensile tail like atelines (Garber and Rehg, 1999). Here, Cebus was considered to represent the morpho- type ancestral to atelines. Hylobates was included in the present study because of its high dependence on forelimb suspensory behavior, especially brachiation (Fleagle, 1976). Because scapular movement is limited to slight rotation and tilting in the brachiating spider (Jenkins et al., 1978), movement at the glenohumeral joint is critical in forelimb suspensory locomotion. Thus, the present study focuses on the structure of the glenohumeral joint. Relative curvature and extensiveness of the scapular glenoid and humeral head articular surfaces were compared separately and in relation to each other.

Materials and Methods Materials The following skeletal specimens were examined: 13 Ateles (A. paniscus, A. belzebuth, and A. geoffroyi), 10 Lagothrix (L. lagotricha and L. sp.), 13 Alouatta (A. caraya, A. seniculus and A. sp.), 22 Cebus (C. apella, C. albifrons, C. Figure 1. Measurements of the glenoid cavity and the humeral capucinus, and C. sp.), and 18 Hylobates (H. lar, H. agilis, head (right side). L2/L1, L5/L1, and R2/R1 correspond to glenoid indices H. klossii, H. hoolock, and H. sp.). These specimens include 1, 2, and 3, respectively; L4/L3 and R4/R3 to humeral head indices 4 both captive and free-ranging individuals. They are housed and 5, respectively; and R3/R1, R4/R2, A3/A1, and A4/A2 to gleno- in the Primate Research Institute, Kyoto University; the humeral indices 6 to 9, respectively. Japan Monkey Centre; and the Department of Anatomy, Dokkyo University School of Medicine. All the specimens are adults whose epiphyses at the Since anatomical orientation of the and humeral head and the coracoid process are fused. Individuals differs between living hominoids and quadrupedal non-homi- with pathological conditions were excluded. Specimens noid primates, in this study the directional terminology used were not grouped by sex. Since intrageneric variation in for hominoids was adopted (i.e. the glenoid faces laterally) positional behavior is considered to be minor in atelines (Figure 1). For example, the long axis of the glenoid articu- (Mittermeier, 1978), morphological analyses were con- lar surface and its perpendicular breadth are considered to ducted at the generic level. Since known body sizes of ate- correspond with the craniocaudal and dorsoventral direc- line genera and Hylobates overlap largely within 6 to 8 kg tions, respectively. (Strier, 1992; Smith and Jungers, 1997), size-adjustment of Linear lengths (L1 to L4) were measured to the nearest morphological data was not conducted. 0.01 mm by sliding calipers. Radii of curvature (R1 to R4), arc lengths A1 and A2, and central angles (θ1, θ2) were mea- Measurements sured on plaster replicas made from dental silicone molds Measurements were taken on the right side when possible. (PROVIL, Heraeus Kulzer, Inc.). These replicas were placed Seventeen variables were taken on the humerus and scapula with the articular surfaces facing upwards, and digitized (Figure 1). Linear (L1 to L4) and arc (A3 and A4) measure- with a probe-type three-dimensional scanner (PICZA, ments correspond to the conventional osteometric protocol Roland DG, Corp.) at a high resolution (0.05 mm) mesh. The of Martin (Knußmann, 1988). Angular variables (θ1 to θ4) graphical software 3D-Rugle2 (Medic Engineering, Inc.) follow Ziemer (1978), and measurements L5, A1, A2, and R1 was used to process the three-dimensional data. The cranio- to R4 were defined in this study. caudal profile of the glenoid was measured along the long Vol. 115, 2007 ATELINE GLENOHUMERAL JOINT CHARACTERS 19 axis of the glenoid. The dorsoventral profile was measured Scapular glenoid cavity at the maximum breadth of the glenoid and orthogonal to the The relative breadth of the glenoid (index 1) exhibits large plane of the craniocaudal profile. Craniocaudal and dorso- intergeneric variation in the atelines. Ateles has a signifi- ventral profiles corresponding to those of the glenoid were cantly higher value than the other atelines, nearly equal to used on the humeral head. Articular profiles were approxi- that of Hylobates. Alouatta has a significantly lower value mated as arcs defined by the two terminal points and the (narrow glenoid relative to height) than the other genera. mid-point. Radii of curvature (R1 to R4), arc lengths (A1, A2), The position of the maximum glenoid breadth (index 2) in and central angles (θ1, θ2) were computed for each defined Hylobates is almost at the midpoint of the craniocaudal arc. Three-dimensional data of the humeral head were used length of the glenoid. The same dimension is positioned only to obtain the radii of curvature (R3, R4). Since it was more caudally in Ateles and Lagothrix, and even more so in difficult to digitize its inferior articular surface border (the Alouatta and Cebus. Thus, although the breadth–length ratio globular humeral head obscures the border), arc lengths of is equivalent (index 1), the glenoid of Ateles tapers cranially the humeral head (A3, A4) were measured manually with a relative to that of Hylobates. tape measure. Central angles of the humeral head (θ3, θ4) The orthogonal radius of curvature ratio (index 3) exhibits were calculated from the arc lengths and radii. Measurement large individual variation (see S.D. values in Table 1). There L5 was obtained by processing the three-dimensional data is a tendency for the more suspensory taxa to have a smaller and quantifying the length of the cranial portion of the gle- craniocaudal central angle (angle 1); Alouatta and Cebus noid, measured as the projected distance between the cra- have a more concave glenoid surface with larger craniocau- nial-most glenoid point and the axis of maximum glenoid dal central angle values. Intergeneric differences in the dorso- breadth in the plane that passes through the cranial tip and ventral central angle (angle 2) are obscured by individual two caudal points of the glenoid rim. variation. Nine indices and four angles were used to compare the joint morphologies. The glenoid variables exam- Humeral head ined were: index 1 (breadth–length ratio, L2/L1); index 2 The relative breadth of the humeral head (index 4) in (maximum breadth level, L5/L1); index 3 (orthogonal radius Ateles is remarkably large among atelines, with an average of curvature ratio, R2/R1); angle 1 (craniocaudal central value close to unity, as in Hylobates. Lagothrix, on the other angle, θ1); and angle 2 (dorsoventral central angle, θ2). The hand, has a narrow humeral head relative to its length, which humeral head variables were: index 4 (breadth–length ratio, is a characteristic shared with Alouatta and Cebus. L4/L3); index 5 (orthogonal radius of curvature ratio, R4/R3); The orthogonal radius of curvature ratio (index 5) is high angle 3 (craniocaudal central angle, θ3); and angle 4 (dorso- in Ateles and Hylobates. In these taxa, the humeral head ventral central angle, θ4). The glenohumeral joint variables approximates a part of a spherical surface (similarly curved were: index 6 (craniocaudal radius of curvature ratio, R3/R1); in both craniocaudal and dorsoventral directions). In index 7 (dorsoventral radius of curvature ratio, R4/R2); index Lagothrix, Alouatta, and Cebus, the humeral head exhibits a 8 (craniocaudal articular length ratio, A3/A1); and index 9 radius of curvature in the dorsoventral axis that is shorter (dorsoventral articular length ratio, A4/A2). than that in the craniocaudal axis. Indices 1 and 4 are conventional descriptions of projected The craniocaudal central angle (angle 3) exhibits large articular shape (e.g. Fleagle and Simons, 1982; Larson, individual variation. The dorsoventral central angle (angle 1998). Index 2 was used to describe the craniocaudal posi- 4) distinguishes between taxa more clearly. In particular, a tion of the maximum breadth of the glenoid articular surface. dorsoventrally convex articular surface characterizes the Indices 3 and 5 reflect the degree to which an articular sur- humeral head of Hylobates. The central angles of Ateles are face has equal radii of curvature along the two orthogonal the most similar in the two orthogonal directions (angles 3 profiles. If the value is close to unity, an articular surface and 4) among all the taxa. forms part of a more spherical surface. Central angles 1 to 4 were used to compare the degree of concavity or convexity Glenoid-humeral head relation of articular surfaces. Indices 6 and 7 were devised to evalu- Ateles and Lagothrix exhibit a significantly low congru- ate congruency in the radii of curvature between the humeral ency of the articular surface curvatures (radius of curvature) and glenoid joint surfaces. Indices 8 and 9 were examined to in the craniocaudal direction (index 6) compared with evaluate the extensiveness of the humeral head relative to Alouatta and Cebus. This incongruency is highest in the glenoid surface. A larger value indicates a potentially Hylobates. Concerning congruency in the dorsoventral direc- greater range of joint motion. tion (index 7), individual variation was large and no clear Differences between the five genera were tested by the trends were found. least significant difference (LSD) multiple comparison tests The arc length ratio between the glenohumeral joint sur- using the software STATISTICA (StatSoft, Inc.). faces shows no significant difference in the craniocaudal direction (index 8). However the arc length ratio in the dorso- Results ventral direction (index 9) is high in Ateles, and particularly high in Hylobates. Among the other genera, Lagothrix is not Table 1 summarizes the results. Table 2 lists P-values of distinguishable from Cebus and Alouatta. the LSD tests. In both tables, the taxa are ordered by fre- Table 3 summarizes the characters that differentiate the quency of forelimb suspensory locomotion. three ateline genera. 20 M. KAGAYA ANTHROPOLOGICAL SCIENCE

Table 1. Intergeneric comparison of the glenoid cavity and humeral head metrics Definition Hylobates Ateles Lagothrix Alouatta Cebus Glenoid

Index 1 Breadth–length ratio (L2/L1) 0.76 0.74 0.66 0.59 0.66 0.06 0.04 0.04 0.04 0.04 (18) (12) (10) (13) (22) Index 2 Maximum breadth level (L5/L1) 0.58 0.64 0.67 0.73 0.70 0.05 0.02 0.04 0.04 0.02 (9)(7)(7)(9)(11) Index 3 Orthogonal radius of curvature ratio (R2/R1) 0.90 0.85 0.92 1.01 1.09 0.15 0.09 0.14 0.18 0.14 (9) (12) (8) (9) (10) Angle 1 Craniocaudal central angle (θ1) 48.4 56.5 68.8 79.5 78.3 7.4 6.5 7.2 5.4 8.0 (9)(13)(8)(9)(11) Angle 2 Dorsoventral central angle (θ2) 39.4 47.7 44.3 46.3 43.4 4.7 4.9 7.9 8.1 5.2 (9) (12) (8) (9) (10) Humeral head

Index 4 Breadth–length ratio (L4/L3) 0.97 0.96 0.84 0.82 0.87 0.03 0.04 0.05 0.04 0.04 (18) (12) (10) (13) (20) Index 5 Orthogonal radius of curvature ratio (R4/R3) 0.96 0.95 0.88 0.88 0.91 0.03 0.05 0.05 0.04 0.02 (14) (10) (9) (10) (10) Angle 3 Craniocaudal central angle (θ3) 157.0 162.9 169.0 174.4 175.8 5.3 5.8 9.1 11.1 7.8 (14) (10) (9) (10) (10) Angle 4 Dorsoventral central angle (θ4) 192.5 164.8 149.8 134.9 139.6 11.9 9.1 4.8 9.5 7.0 (13) (10) (9) (10) (10) Glenoid–humeral head relation

Index 6 Craniocaudal radius of curvature ratio (R3/R1) 0.63 0.72 0.76 0.92 0.88 0.07 0.05 0.08 0.04 0.05 (7) (10) (7) (6) (9) Index 7 Dorsoventral radius of curvature ratio (R4/R2) 0.71 0.80 0.73 0.84 0.76 0.12 0.08 0.11 0.06 0.10 (7) (10) (7) (6) (9) Index 8 Craniocaudal articular length ratio (A3/A1) 1.85 1.78 1.68 1.75 1.82 0.11 0.12 0.10 0.09 0.13 (9)(8)(7)(9)(11) Index 9 Dorsoventral articular breadth ratio (A4/A2) 3.27 2.80 2.44 2.37 2.40 0.61 0.41 0.13 0.32 0.24 (9) (11) (8) (9) (10) See Figure 1 for measurement definitions. Values are mean (top), standard deviation (middle), and sample size (bottom, in parentheses).

Discussion climbing hypothesis offered by Sarmiento (1995) for the morphological similarities between the of Ateles The present study quantitatively confirms a number of and hominoids, but rather emphasizes forelimb suspensory purported distinctions between the glenohumeral joint mor- behavior as the specific basis for such similarities. It also phologies of Ateles and Lagothrix. Features that characterize contrasts in part with the interpretations offered by Gebo Ateles are a relatively broad glenoid and humeral head, and (1996) and Larson (1998). Gebo (1996) related most of the a more spherically curved humeral head surface (indices 1, derived traits of Ateles to brachiation and forelimb suspen- 4, 5). Ateles does not differ significantly from the specialized sion, as is suggested in the present study. However, he brachiator Hylobates in these traits, while Lagothrix is simi- adopted a more generalized functional interpretation for the lar to the other quadrupedal platyrrhines. Thus, at least these globular humeral head by associating this character to three features of Ateles are likely to be derived, and conse- climbing, bridging, and brachiation, citing shared similari- quently, likely attributable to a high dependence on forelimb ties with the globular humeral head of lorisines. Larson suspensory behavior. (1998) reported overlap between some humeral head shape The above conclusion does not support the generalized indices of hominoids and cercopithecoids. Nevertheless, the Vol. 115, 2007 ATELINE GLENOHUMERAL JOINT CHARACTERS 21

Table 2. P-values of the LSD multiple comparison tests between genera Hylobates Ateles Lagothrix Alouatta Glenoid

Index 1 Breadth–length ratio (L2/L1) Ateles 0.358 Lagothrix 0.000 0.000 Alouatta 0.000 0.000 0.000 Cebus 0.000 0.000 0.816 0.000

Index 2 Maximum breadth level (L5/L1) Ateles 0.000 Lagothrix 0.000 0.174 Alouatta 0.000 0.000 0.002 Cebus 0.000 0.000 0.065 0.085

Index 3 Orthogonal radius of curvature ratio (R2/R1) Ateles 0.414 Lagothrix 0.771 0.273 Alouatta 0.120 0.015 0.219 Cebus 0.006 0.000 0.016 0.212

Angle 1 Craniocaudal central angle (θ1) Ateles 0.010 Lagothrix 0.000 0.000 Alouatta 0.000 0.000 0.003 Cebus 0.000 0.000 0.005 0.721

Angle 2 Dorsoventral central angle (θ2) Ateles 0.004 Lagothrix 0.104 0.240 Alouatta 0.022 0.608 0.518 Cebus 0.159 0.113 0.755 0.317 Humeral head

Index 4 Breadth–length ratio (L4/L3) Ateles 0.264 Lagothrix 0.000 0.000 Alouatta 0.000 0.000 0.150 Cebus 0.000 0.000 0.060 0.000

Index 5 Orthogonal radius of curvature ratio (R4/R3) Ateles 0.885 Lagothrix 0.000 0.000 Alouatta 0.000 0.000 0.887 Cebus 0.006 0.015 0.032 0.040

Angle 3 Craniocaudal central angle (θ3) Ateles 0.076 Lagothrix 0.000 0.099 Alouatta 0.000 0.002 0.137 Cebus 0.000 0.001 0.064 0.692

Angle 4 Dorsoventral central angle (θ4) Ateles 0.000 Lagothrix 0.000 0.001 Alouatta 0.000 0.000 0.001 Cebus 0.000 0.000 0.018 0.256 Glenoid–humeral head relation

Index 6 Craniocaudal radius of curvature ratio (R3/R1) Ateles 0.004 Lagothrix 0.000 0.148 Alouatta 0.000 0.000 0.000 Cebus 0.000 0.000 0.000 0.153

Index 7 Dorsoventral radius of curvature ratio (R4/R2) Ateles 0.058 Lagothrix 0.615 0.167 Alouatta 0.015 0.378 0.045 Cebus 0.287 0.366 0.590 0.103 22 M. KAGAYA ANTHROPOLOGICAL SCIENCE

Table 2. (continued) Hylobates Ateles Lagothrix Alouatta

Index 8 Craniocaudal articular length ratio (A3/A1) Ateles 0.246 Lagothrix 0.006 0.095 Alouatta 0.064 0.507 0.272 Cebus 0.557 0.514 0.018 0.168

Index 9 Dorsoventral articular breadth ratio (A4/A2) Ateles 0.006 Lagothrix 0.000 0.042 Alouatta 0.000 0.013 0.689 Cebus 0.000 0.017 0.827 0.843

Table 3. Glenohumeral characters in the three atelines Ateles Lagothrix Alouatta Broad glenoid (index 1) +−− − Broad humeral head (index 4) +−− Spherical humeral head (index 5) +−− Dorsoventrally large potential joint movement (index 9) +−− Craniocaudally less concave glenoid (angle 1) +±− Dorsoventrally more convex humeral head (angle 4) +±− Craniocaudally large curvature discrepancy (index 6) ++− +, characters present; −, characters absent; ±, characters intermediate. State of Alouatta for index 1 is represented by − −, which is considered derived (see text).

present analysis of the atelines supports the interpretation Ateles, namely a large discrepancy in the craniocaudal radii that these traits are probably related to specialization in fore- of the glenoid and humeral head articular surfaces (index 6; limb suspensory behavior. Table 3), it shares more features with the non-brachiating The comparison of the central angles of the articular sur- Alouatta and Cebus (indices 4, 5, 9; Table 3). The rather faces shows a gradational difference among the atelines, primitive joint morphology seen in Lagothrix seems to cor- with Lagothrix occupying an intermediate position. Ateles respond to its more generalized positional repertoire (Cant et has a humeral head which is convex dorsoventrally (angle 4) al., 2003). Since Lagothrix often exhibits pronograde pos- and a glenoid which is relatively flat craniocaudally (angle ture even in forelimb swing with assistance of tail and/or 1). These trends are less striking in Lagothrix. However, the pedal grasp (Cant et al., 2003), its primitive glenohumeral craniocaudally confined glenoid in Ateles does not contrib- joint morphology may be related to a smaller degree of ute to an expanded range of movement, as judged from the mobility in comparison with the more suspensory Ateles. relative extent of the humeral head (index 8). In contrast, in Most traits of Alouatta are shared by Cebus. However, the dorsoventral direction, the extensive humeral head of Alouatta evidently is specialized in one feature, the dorso- Ateles relative to the glenoid is notable (index 9). This differ- ventrally narrow glenoid surface (index 1); the value of this ence between the humeral head and glenoid is weaker in index in Alouatta is extremely low among anthropoids [see Lagothrix, and not significantly different from the Cebus Figure 12 of MacLatchy et al. (2000)]. This supports the and Alouatta conditions. case of Rosenberger and Strier (1989), who cautioned The dorsoventral direction corresponds to the direction of against uncritically considering Alouatta as representing the progression in brachiating Ateles, whose scapular blades are primitive ateline morphotype. situated relatively dorsal on the thoracic wall (Jenkins et al., Most Oligocene and Miocene fossil catarrhines, for 1978). Ateles has a longer stride during forelimb suspended instance Aegyptopithecus and Pliopithecus, exhibit a mosaic progression than Lagothrix, even after standardization by of ateline and Cebus-like forelimb features (Fleagle and forelimb length (Turnquist et al., 1999). Thus, the above- Simons, 1982; Rose, 1989, 1993, 1996). Although the described glenohumeral joint features of Ateles may provide present study shows that there is little distinction in gleno- an increase in the fore–aft range of forelimb movement, con- humeral joint morphology between the non-specialized tributing to a longer stride length during brachiation. brachiator (Lagothrix) and arboreal quadrupeds, some Because of the relatively cranial orientation of the glenoid in inferences are possible regarding forelimb suspensory posi- suspensory monkeys and apes (Gebo, 1996), a craniocau- tional behavior in fossils. For example, morphological fea- dally elongated glenohumeral joint may not be necessary for tures pronounced in Ateles (indices 1, 4, 5, 9) may indicate a forelimb mobility in this direction, in contrast to the situa- rather specialized forelimb suspensory behavior. Features tion with dimensions in the dorsoventral direction. shared by Lagothrix and Ateles (index 6) may simply be While Lagothrix shares only one character state with indicators of the capability for forelimb suspensory behav- Vol. 115, 2007 ATELINE GLENOHUMERAL JOINT CHARACTERS 23 ior. Features that appear to be intermediate in Lagothrix American Journal of Physical Anthropology, 110: 325–339. (angles 1, 4) may be suggestive of relative intensity of fore- Gebo D.L. (1992) Locomotor and postural behavior in Alouatta limb suspensory behavior. Although atelines are phylogenet- palliata and Cebus capucinus. American Journal of Primatol- ogy, 26: 277–290. ically distant from hominoids, phylogenetically controlled Gebo D.L. (1996) Climbing, brachiation, and terrestrial quadrupe- comparisons, like that of the present study, enable the con- dalism: historical precursors of hominid . Ameri- struction of a framework for the functional interpretation of can Journal of Physical Anthropology, 101: 55–92. extant and extinct primate morphology. Jenkins F.A. Jr., Dombrowski P.J., and Gordon E.P. (1978) Analy- sis of the shoulder in brachiating spider monkeys. American Journal of Physical Anthropology, 48: 65–76. Acknowledgments Knußmann R. (1988) Anthropologie. Handbuch der verglei- chenden Biologie des Menschen. Gustav Fischer Verlag, I am indebted to Professor Hidemi Ishida, Dr Masato Stuttgart. Nakatsukasa and Dr Naomichi Ogihara for providing Larson S.G. (1998) Parallel evolution in the hominoid trunk and insightful and constructive comments. I am grateful to Dr forelimb. Evolutionary Anthropology, 6: 87–99. Harumoto Gunji, Japan Monkey Centre; Dr Masaki MacLatchy L., Gebo D., Kityo R., and Pilbeam D. 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