Odd-nosed monkey scapular morphology converges on that of arm-swinging apes

Abstract

Odd-nosed monkeys ‘arm-swing’ more frequently than other colobines. They are therefore somewhat behaviorally analogous to atelines and apes. Scapular morphology regularly reflects locomotor mode, with both arm-swinging and climbing anthropoids showing similar characteristics, especially a mediolaterally narrow blade and cranially angled spine and glenoid. However, these traits are not expressed uniformly among anthropoids. Therefore, behavioral convergences in the odd-nosed taxa of Nasalis, Pygathrix, and Rhinopithecus with hominoids may not have resulted in similar structural convergences. We therefore used a broad sample of anthropoids to test how closely odd-nosed monkey scapulae resemble those of other arm-swinging primates. We used principal component analyses on size-corrected linear metrics and angles that reflect scapular size and shape in a broad sample of anthropoids. As in previous studies, our first component separated terrestrial and above-branch quadrupeds from clambering and arm-swinging taxa. On this axis, odd-nosed monkeys were closer than other colobines to modern apes and Ateles. All three odd-nosed genera retain glenoid orientations that are more typical of other colobines, but Pygathrix and Rhinopithecus are closer to hominoids than to other Asian colobines in mediolateral blade breadth, spine angle, and glenoid position. This suggests that scapular morphology of Pygathrix may reflect a significant reliance on arm-swinging and that the morphology of Rhinopithecus may reflect more reliance on general climbing. As ‘arm-swinging’ features are also found in taxa that only rarely arm-swing, we hypothesize that these features are also adaptive for scrambling and bridging in larger bodied anthropoids that use the fine-branch component of their arboreal niches.

Introduction

Throughout much of the twentieth century, hominoids were almost universally classified as ‘brachiators’ (Avis, 1962, Napier, 1963, Napier and Napier, 1967), and features associated with brachiation were argued to represent the ancestral state for hominoid postcranial morphology and arboreal locomotion (Keith, 1923, Gregory, 1930, Tuttle, 1975; but see Straus, 1949). These ‘brachiating’ features included an elongated clavicle and antebrachium, an especially mobile shoulder with a dorsally placed scapula, an abbreviated olecranon allowing increased extension, a mobile wrist (usually with ‘ulnar withdrawal’ or midcarpal rotation; Jenkins, 1981, Lovejoy et al., 2009a), elongated metacarpals and manual phalanges, a broadened thorax, and a reduced lumbar column (both in element number and in centrum craniocaudal height; e.g., Schultz, 1930, Erikson, 1963, Ashton and Oxnard, 1964, Andrews and Groves, 1976, Jungers and Stern, 1984, Larson, 1993, Ward, 1993, Gebo, 1996). There is now new and considerable evidence that many of these features evolved in parallel (Larson, 1998; Lovejoy et al., 2009a, Lovejoy et al., 2009b, Hammond et al., 2013, Reno, 2014, Alba et al., 2015, Ward, 2015, Arias-Martorell, 2019; but see Gebo, 1996, Young, 2003), not only in hominoids but also in some New World monkeys and Old World monkeys (see below).

Of equal importance is that classifying both great and lesser apes simply as ‘brachiators’ does not sufficiently capture extant hominoid locomotor diversity. Hylobatids are unarguably ‘true brachiators’ (Fleagle, 1976, Fleagle, 1980). In fact, they are alone adapted to ‘ricochetal arm-swinging,’ a form of rapid bimanual suspension that includes an aerial phase (Jungers and Stern, 1984, Swartz, 1989, Hunt et al., 1996, Bertram and Chang, 2001, Usherwood and Bertram, 2003, Bertram, 2004). We refer to ‘arm-swinging’ here as bimanual progression without an aerial phase. The orangutan's ‘orthograde clamber’ (Hunt et al., 1996) is a unique form of locomotion, which not only includes arm-swinging but also involves hind limb grasping and stabilization in various orientations (Thorpe and Crompton, 2006, Thorpe et al., 2009). This ‘quadrumanous climbing’ differs greatly from the arm-swinging of gibbons, in part because of its much greater body mass and unique phylogenetic history.

The arboreal locomotion of extant African apes differs dramatically from that of these other hominoids. Chimpanzees and gorillas regularly knuckle-walk when terrestrial and engage in a mixture of vertical climbing and scrambling when arboreal, the former being required to navigate and exploit resources achievable only by terrestrial travel (Hunt, 1992, Remis, 1995, Doran, 1996, Doran, 1997). Knuckle-walking is therefore likely an adaptation to the combination of large body mass and the need to access diversely distributed feeding patches (Simpson et al., 2018). In fact, chimpanzees practice arm-swinging infrequently, and it is only rarely seen in adult gorillas (Hunt, 1992, Remis, 1995, Doran, 1996, Doran, 1997). Knuckle-walking is very likely a specialized form of quadrupedal travel in which many of the typical mechanisms of energy dissipation of ground collision forces have been compromised by specializations of the forelimb for vertical climbing and scrambling. The African apes are the only primates with conical upper thoraces, in contrast to hominins, gibbons, and orangutans (Haile-Selassie et al., 2010, Simpson et al., 2018). This hypothesis has been criticized by Thompson et al. (2018), but their data were obtained from subadult apes, who could not experience the same force magnitudes as adults, and macaques (which do not knuckle-walk), and of course, electromyographic data cannot reflect the passive stretching of tendons and the spring effects of ligaments which are primary energy transducers.

Some New World monkeys (e.g., Ateles, Brachyteles, and Lagothrix) and Old World monkeys (e.g., Pygathrix, see below) also regularly use arm-swinging. In both Ateles and Pygathrix, the behavior is largely similar to that of gibbons, especially with respect to shoulder and elbow kinematics, although there is less morphological and kinematic homogeneity of the wrist among these taxa (Byron et al., 2017). Among monkeys, a true ‘brachiator’ phenotype is largely observed only in Ateles, which exhibits a relatively broad thorax and narrow scapula with cranially oriented glenoid and scapular spine. These features render them postcranially more similar to hominoids than to the phylogenetically related Lagothrix (Andrews and Groves, 1976, Larson, 1998). Ateles uses arm-swinging more commonly than Lagothrix (∼25% in the former vs. <15% in the latter; Mittermeier, 1978, Cant, 1986, Cant et al., 2001). Ateles and Lagothrix are also unusual in that they rely frequently on horizontal body postures made possible by their prehensile tails (Turnquist et al., 1999).

Odd-nosed monkeys are a monophyletic group of Asian colobines (e.g., Sterner et al., 2006, Ting et al., 2008, Liedigk et al., 2012) that exhibit more diverse locomotor behavior than other African or Asian colobines. Douc monkeys (Pygathrix) in captivity engage in relatively frequent bouts of arm-swinging (∼20–55%; Byron and Covert, 2004, Workman and Covert, 2005, Wright et al., 2008). Snub-nosed monkeys (Rhinopithecus) perform this behavior as juveniles, but are mainly terrestrially quadrupedal as adults. When arboreal, snub-nosed monkeys are reported to use general quadrupedal walking, climbing, leaping, and occasional arm-swinging (Wu, 1993, Su and Jablonski, 2009, Zhu et al., 2015). Proboscis monkey (Nasalis) locomotion is less well documented, but arm-swinging has been observed (Hollihn, 1984, Su and Jablonski, 2009). The sister taxon to the proboscis monkey, the pig-tailed snub-nosed monkey of Sumatra (Simias), is also less well studied behaviorally and is poorly represented in museum collections. Its locomotor habit is considered to differ from that of other odd-nosed monkeys and from that of its sister genus Nasalis (Su and Jablonski, 2009). Because of a lack of sufficient sample size, Simias will not be further discussed here.

Some characteristics of Pygathrix converge on those of arm-swinging hominoids. Douc monkeys exhibit higher intermembral and brachial indices, longer clavicles, a narrower scapula with an elongated and more cranially oriented acromion, and a shorter olecranon than other Old World monkeys. However, Pygathrix wrist morphology differs somewhat dramatically from that of hominoids (Su and Jablonski, 2009, Bailey et al., 2017). Similarly, wrist kinematics during arm-swinging in Pygathrix contrasts with those of Ateles and Hylobates, whereas those of the shoulder and elbow are more comparable with these taxa (Byron et al., 2017).

Scapular morphology can substantially reflect locomotor mode (Fig. 1). Extensive multivariate studies have positioned anthropoid taxa along a continuum from above-branch and/or terrestrial quadrupeds to clambering/brachiating species (Ashton et al., 1965a, Oxnard, 1967, Young, 2008, Selby and Lovejoy, 2017). Features common to primates specialized for climbing, clambering, and/or arm-swinging include a mediolaterally narrow blade, a cranially oriented spine and acromion, and a cranially oriented and positioned glenoid (Fig. 1; Ashton and Oxnard, 1964, Ashton et al., 1965b, Andrews and Groves, 1976, Green and Alemseged, 2012, Green, 2013, Green et al., 2016, Selby and Lovejoy, 2017). However, the morphology of arm-swinging and climbing anthropoids is not uniform, particularly with respect to their spine and glenoid angles (Young, 2008, Green et al., 2016, Selby and Lovejoy, 2017). Therefore, it is predicted that odd-nosed monkeys are also likely to vary in these features as well. Furthermore, we anticipate that their scapular characteristics should be more similar in shape to those of hominoids or atelids than to those of other colobines.

These expectations are supported by the literature. Pygathrix does appear to be intermediate to colobines and gibbons in scapular morphology (Bailey et al., 2017). Gibbons have an especially mediolaterally narrow scapula and highly angled scapular spine, which is consistent with their being unusual distinctiveness among anthropoids in using of ricochetal arm-swinging. Pygathrix and other odd-nosed monkeys have been shown to have narrow scapulae relative to those of other cercopithecines (Su and Jablonski, 2009, Byron et al., 2017). However, a narrow scapula alone is not necessarily indicative of suspensory behaviors (Larson, 2015, Selby and Lovejoy, 2017). Pygathrix, like Ateles and Lagothrix, engage in both above-branch quadrupedalism and arm-swinging to varying degrees. Our goal here is to determine if there are morphological convergences in scapular form among odd-nosed monkeys (Pygathrix, Nasalis, and Rhinopithecus) and other arm-swinging hominoids and atelids compared with other anthropoids that practice different modes of locomotion.