© 2018. Published by The Company of Biologists Ltd | Journal of Experimental Biology (2018) 221, jeb170910. doi:10.1242/jeb.170910 RESEARCH ARTICLE Hand pressures during arboreal locomotion in captive bonobos (Pan paniscus) Diana S. Samuel1, Sandra Nauwelaerts2,3, Jeroen M. G. Stevens3,4 and Tracy L. Kivell1,5,* ABSTRACT of both manipulation and locomotion. Although there has been much Evolution of the human hand has undergone a transition from use research into the potential changes in manipulative abilities during locomotion to use primarily for manipulation. Previous throughout human evolution, from both morphological (e.g. comparative morphological and biomechanical studies have Napier, 1955; Marzke, 1997; Marzke et al., 1999; Skinner et al., focused on potential changes in manipulative abilities during 2015) and biomechanical (e.g. Marzke et al., 1998; Rolian et al., human hand evolution, but few have focused on functional signals 2011; Williams et al., 2012; Key and Dunmore, 2014) perspectives, for arboreal locomotion. Here, we provide this comparative context comparatively little research has been done that may help us infer though the first analysis of hand loading in captive bonobos during how our ancestors may have used their hands for arboreal arboreal locomotion. We quantify pressure experienced by the locomotion, particularly climbing and suspension. Many fossil fingers, palm and thumb in bonobos during vertical locomotion, hominins show features of the hand (e.g. curved fingers) and upper suspension and arboreal knuckle-walking. The results show that limb (e.g. superiorly oriented shoulder joint) (e.g. Stern, 2000; pressure experienced by the fingers is significantly higher during Larson, 2007; Churchill et al., 2013; Kivell et al., 2011, 2015; Kivell, knuckle-walking compared with similar pressures experienced by the 2015) that suggest arboreal locomotion may still have been an fingers and palm during suspensory and vertical locomotion. Peak important selective pressure on the hominin postcranium (for a pressure is most often experienced at or around the third digit in all review, see Rose, 1991; Ward, 2002; Niemitz, 2010). More locomotor modes. Pressure quantified for the thumb is either very low information about the biomechanics and, in particular, the loads or absent, despite the thumb making contact with the substrate during experienced by the hand during arboreal locomotion in our closest all suspensory and vertical locomotor trials. Unlike chimpanzees, living relatives, the African apes, will help us to interpret the potential bonobos do not show a rolling pattern of digit contact with the functional significance of variation in hand morphology that we see substrate during arboreal knuckle-walking – instead, we found that among fossil hominins. To gain this insight, we measured pressures digits 3 and 4 typically touch down first and digit 5 almost always experienced by the hand during vertical locomotion, suspension and Pan paniscus made contact with the substrate. These results have implications for arboreal knuckle-walking in captive bonobos ( ). interpreting extant and fossilized hand morphology; we expect Bonobos, in addition to their close genetic relationship with bonobo (and chimpanzee) bony morphology to primarily reflect the humans (Prüfer et al., 2012), show greater stasis in their anatomy biomechanical loading of knuckle-walking, while functional signals for compared with chimpanzees and thus are arguably a better extant ape arboreal locomotion in fossil hominins are most likely to appear in model for understanding human evolution (Diogo et al., 2017a,b). the fingers, particularly digit 3, and least likely to appear in the Bonobo locomotion has been studied in a variety of ways, in morphology of the thumb. both the wild and captivity. Early work on locomotion in the wild highlighted greater arboreality in bonobos compared with KEY WORDS: Force, Biomechanics, African apes, Vertical climbing, chimpanzees (Alison and Badrian, 1977; MacKinnon, 1978), Suspension, Knuckle-walking particularly suspension, leaping and bipedal locomotion in the trees (Susman et al., 1980). Doran (1992, 1993) later confirmed INTRODUCTION these initial impressions with more detailed comparative studies, The human hand is unique among primate hands in its enhanced noting that bonobos used more arboreal quadrupedalism, ability to precisely and forcefully manipulate objects (e.g. Napier, particularly palmigrade quadrupedalism, suspension and leaping 1955; Marzke, 1997, 2013). However, understanding how these compared with chimpanzees (Susman, 1984; Doran, 1993). With abilities evolved requires a better understanding of what fossil human regards to hand use during arboreal locomotion, only chimpanzee (hominin) ancestors may have been doing with their hands, in terms hand postures have been studied in the wild, highlighting the use of power grips, involving the palm and thumb, and hook grips, using the fingers only, on differently sized substrates during suspension 1Animal Postcranial Evolution (APE) Lab, Skeletal Biology Research Centre, School of Anthropology and Conservation, University of Kent, Canterbury CT2 7NR, UK. (Hunt, 1991; Marzke and Wullstein, 1996) and vertical climbing 2Laboratory for Functional Morphology, Department of Biology, University of (Hunt, 1991; Neufuss et al., 2017b). Antwerp, Universiteitsplein 1, 2610 Wilrijk, Belgium. 3Centre for Research and Conservation (CRC), Royal Zoological Society of Antwerp, Koningin Astridplein Unlike most natural environments, captive environments can 20-26, 2018 Antwerp, Belgium. 4Behavioral Ecology and Ecophysiology group, provide a venue for experimental studies that utilize specialist Department of Biology, University of Antwerp, Universiteitsplein 1, 2610 Wilrijk, equipment to obtain biomechanical information, such as three- Belgium. 5Department of Human Evolution, Max Planck Institute for Evolutionary Anthropology, Deutscher Platz 6, Leipzig 04103, Germany. dimensional kinematics, substrate reaction forces or hand/foot pressures, that are crucial to gaining a full understanding of *Author for correspondence ([email protected]) locomotor biomechanics in primates and the potential selective T.L.K., 0000-0001-5087-0897 pressures on the skeletal morphology (Vereecke and Wunderlich, 2016, and references therein). Among the captive biomechanical Received 22 September 2017; Accepted 5 March 2018 studies that include bonobos or chimpanzees, most analyse Journal of Experimental Biology 1 RESEARCH ARTICLE Journal of Experimental Biology (2018) 221, jeb170910. doi:10.1242/jeb.170910 terrestrial locomotion, often with a focus on the hindlimb (e.g. 1992; Doran, 1993; Crompton et al., 2010) and may also have been Kimura et al., 1979; Demes et al., 1994; Aerts et al., 2000; D’Août critical behaviours in the evolution of early hominin ancestors (e.g. et al., 2001, 2002, 2004; Vereecke et al., 2003, 2004; Li et al., 2004; Rose, 1991; Schmitt, 2003). To fill this gap, we measured pressures Sockol et al., 2007; Raichlen et al., 2009). Some of this research has experienced by the bonobo hand (divided into regions of the palm, revealed that chimpanzees (bonobos have not yet been studied), like fingers and thumb) during three modes of arboreal locomotion: most primates, are distinct from many other mammals in having vertical locomotor behaviours, suspension and knuckle-walking. lower or equal vertical forces on the forelimbs and hindlimbs We tested four hypotheses, based on previous studies of hand use (Kimura et al., 1979; Demes et al., 1994; Li et al., 2004). and posture during arboreal locomotion in bonobos, or great apes in Comparatively few studies have investigated the biomechanics of general, and pressure analyses of chimpanzee arboreal knuckle- arboreal locomotion, especially vertical climbing or suspension walking (Wunderlich and Jungers, 2009). (1) Hand postures used (Isler, 2002, 2005; Nakano et al., 2006; Wunderlich and Jungers, during arboreal locomotion will be similar to those described 2009; Schoonaert et al., 2016; Wunderlich and Ischinger, 2017), previously in chimpanzees during suspension and climbing (Hunt, probably in part because of the inherent logistical challenges 1991; Marzke and Wullstein, 1996; Neufuss et al., 2017b) and associated with collecting such data compared with terrestrial arboreal knuckle-walking (Wunderlich and Jungers, 2009). (2a) substrates. In Isler’s (2002, 2005) investigation of gait parameters Pressure experienced by the palm and fingers will be similar within (e.g. stride length, duty factor) and kinematics of the forelimbs and both vertical locomotion and suspension as both regions of the hand hindlimbs during vertical climbing, she found that vertical climbing are generally used to grasp the substrate during these locomotor in bonobos was highly variable in terms of gait parameters, but that behaviours (Hunt, 1991). (2b) In contrast, pressure experienced by joint angles were similar to those of gorillas. Bonobo gait the thumb will be significantly lower than that experienced by the parameters have been further studied during terrestrial locomotion palm or fingers because of the thumb’s short length relative to that (Aerts et al., 2000) and, only recently, during arboreal knuckle- of the fingers, small musculature (Tuttle, 1969; Marzke et al., 1999) walking and climbing on a variety of different inclines (Schoonaert and the general assumption that the function of the thumb is limited et al., 2016). However, to our knowledge, substrate