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Glenohumeral Joint Surface Characters and Its Relation to Forelimb Suspensory Behavior in Three Ateline Primates, Ateles, Lagothrix, and Alouatta Miyuki KAGAYA1*

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Glenohumeral Joint Surface Characters and Its Relation to Forelimb Suspensory Behavior in Three Ateline Primates, Ateles, Lagothrix, and Alouatta Miyuki KAGAYA1* ANTHROPOLOGICAL SCIENCE Vol. 115, 17–23, 2007 Glenohumeral joint surface characters and its relation to forelimb suspensory behavior in three ateline primates, 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 primate 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 monkey (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 scapula and humerus 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
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