Threedimensional Kinematics of Capuchin Monkey Bipedalism

AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 145:147–155 (2011) Three-Dimensional Kinematics of Capuchin Monkey Bipedalism Brigitte Demes* Department of Anatomical Sciences, School of Medicine, Stony Brook University, Stony Brook, NY 11794-8081 KEY WORDS Cebus apella; bipedalism; kinematics ABSTRACT Capuchin monkeys are known to use humans and other animals run, but without a human-like bipedalism when transporting food items and tools. The gait transition. In this respect it resembles avian bipedal bipedal gait of two capuchin monkeys in the laboratory gaits. It remains to be tested whether energy is recovered was studied with three-dimensional kinematics. Capu- through cyclic elastic storage and release as in bipedal chins progress bipedally with a bent-hip, bent-knee gait. birds at higher speeds. Capuchin bipedalism has many The knee collapses into flexion during stance and the hip features in common with the facultative bipedalism of drops in height. The knee is also highly flexed during other primates which is further evidence for restrictions swing to allow the foot which is plantarflexed to clear the on a fully upright striding gait in primates that transition ground. The forefoot makes first contact at touchdown. to bipedalism. It differs from the facultative bipedalism of Stride frequency is high, and stride length and limb other primates in the lack of an extended double-support excursion low. Hind limb retraction is limited, presumably phase and short aerial phases at higher speeds that make to reduce the pitch moment of the forward-leaning trunk. it a run by kinematic definition. This demonstrates that Unlike human bipedalism, the bipedal gait of capuchins is facultative bipedalism of quadrupedal primates need not not a vaulting gait, and energy recovery from pendulum- necessarily be a walking gait. Am J Phys Anthropol like exchanges is unlikely. It extends into speeds at which 145:147–155, 2011. VC 2011 Wiley-Liss, Inc. Capuchin monkeys (genus Cebus) are quadrupeds, but with flexed limbs (so-called bent-hip, bent-knee or BHBK on the ground they often use bipedal gaits in their natural gait: Crompton et al., 1998). 2) Observational and pre- habitats. This has been reported in particular for Cebus liminary data on capuchin monkeys suggest that they libidinosus, the bearded capuchin,1 in the context of food use what seems to be a bipedal running gait, rather and tool transport (Fragaszy et al., 2004; Wright, 2007; than a walk (Demes and O’Neill, 2009). Studies on the Ottoni and Izar, 2008; Liu et al., 2009). At the field site of mechanics of nonhuman primate bipedalism are almost Piauı´ in Brazil, bearded capuchins have been observed exclusively focused on bipedal walking (but see Vereecke transporting palm nuts and hammer stones to anvil sites et al., 2006b), like most of the discussion of the earliest where they crack the nuts. Orthograde activity of Cebus stages of hominid bipedalism is focused on walking and apella has also been reported from other sites (Youlatos, pendulum mechanics. Bipedal running is only invoked 1998; Boinski et al., 2000). Because capuchins switch with at the onset of the genus Homo and associated with ease from quadrupedal to bipedal postures they represent a erect postures, limb elongation, and pelvic reorientation good model species for studying what kind of bipedal gait a (Carrier, 1984; Bramble and Lieberman, 2004; Lieber- quadrupedal primate adopts—a topic of interest to anthro- man et al., 2006; Sockol et al., 2007). Running has not pologists that study the evolution of human bipedalism. been explored as an incipient bipedal gait. While many species of primates opportunistically use I here present spatiotemporal parameters of capuchin bipedal gaits, precious few have been studied using bipedalism derived from 3D kinematics. A parallel study quantitative methods of gait analysis. These are three (Demes and O’Neill, 2009; in preparation) will focus on species of apes (chimpanzees, bonobos, and gibbons) and the dynamics of capuchin bipedalism. The following spe- the Old World monkeys Macaca fuscata and Papio anu- cific questions will be addressed: bis (Reynolds, 1987; Aerts et al., 2000; D’Aouˆ t et al., 2001, 2002; Hirasaki et al., 2004; Vereecke et al., 1. What characterizes the bipedal gait of capuchin 2006a,b; Kimura and Yaguramaki, 2009; Berrillon et al., monkeys? 2010; Ogihara et al., 2010). The capuchin monkey repre- sents an interesting addition to this canon for two rea- sons: 1) It was a study on cebine hip musculature (Stern, Grant sponsor: NSF; Grant number: BCS 0548892. 1971, 1975) that has let to a paradigmatic insight into bipedal gaits of nonhuman primates and the earliest *Correspondence to: Brigitte Demes, Department of Anatomical hominin bipeds (Stern and Susman, 1981): With iliac Sciences, School of Medicine, Stony Brook University, Stony Brook, blades facing posteriorly, rather than laterally, the lesser NY 11794-8081. E-mail: [email protected] gluteal muscles aren’t capable of balancing an adduction moment at an extended hip joint during unilateral Received 5 July 2010; accepted 9 December 2010 stance, forcing nonhuman primates to walk bipedally DOI 10.1002/ajpa.21484 1Until recently considered a subspecies of C. apella (Groves, Published online 1 March 2011 in Wiley Online Library 2001). (wileyonlinelibrary.com). VC 2011 WILEY-LISS, INC. 148 B. DEMES Fig. 1. Experimental setup. The animals moved on a runway enclosed by a Lexan tunnel. A food reward is offered to them suspended on a pulley system. 2. How do bipedal capuchins modulate speed? Fig. 2. Stick figure showing marker positions, segment ori- 3. How does the bipedal gait of capuchins compare to entations and angles. their quadrupedal gait? 4. How does the bipedal gait of capuchins compare to other nonhuman primates’ bipedal gaits and to Animals were filmed with three video cameras at 60 human bipedalism? Hz, positioned at angles of 508 to each other to produce a lateral and two oblique views. Prior to recording onto VCRs, video signals from all four cameras were sent METHODS through a time code generator (GL-250, J.C. Labs, La Honda, CA) which superimposed a time stamp on each All procedures were approved by the Institutional Ani- video field. This time stamp was used to synchronize vid- mal Care and Use Committee of Stony Brook University. eos. Selected video clips from the three cameras were Data were collected for two male capuchin monkeys of imported into Peak Motus software v. 5.1.2. (Peak Per- the species Cebus apella, ages 9 and 11 years and weigh- formance Technologies, Englewood, CO, now Vicon, Los ing 3 and 3.1 kg, respectively. They were coaxed to walk Angeles, CA) and markers digitized in three views. Prior bipedally with food rewards offered at a height that to each trial, a calibration object with 35 control points forced them to move on their hind limbs alone (see Fig. with known coordinate distances to each other was 1). The animals adapted bipedal postures immediately placed on the runway and filmed. The control points and without any training in the experimental setup. were digitized in the three camera views in Motus, and Like capuchins in the wild, the captive subjects were the 3D coordinates calculated by the software produced observed using bipedal postures regularly in their home 12 coefficients that were used in the direct linear trans- enclosures when carrying food items or toys. formation algorithm to reconstruct the 3D coordinates of Animals moved on a wooden runway enclosed in a clear the joint markers on the animals as they passed through Lexan tunnel 10.5-m long and 0.7-m wide (Polk, 2001). the calibrated space. Positional data were not condi- Prior to trials, animals were briefly anaesthetized, shaved, tioned (filtered) with the exception of the trunk vertical and outfitted with reflective tape markers over major tilt angle in the frontal plane which was fit to a binomial joints. Postural data are reported here for the hind limb curve with a window of two prior to calculating the and trunk using the following joint markers (see Fig. 2): trunk tilt angle. This absolutely small angle had more tip of acromion (shoulder), tip of greater trochanter (hip), digitizing noise associated with it than any of the other lateral epicondyle (knee), lateral malleolus (ankle), and kinematic variables. The temporal and spatial variables head of 5th metatarsal (metatarsophalangeal joint, MT5). calculated from the coordinate data over time are listed Shoulder and hip markers defined the trunk segment, hip in Table 1. and knee markers the thigh, knee and ankle markers the SPSS 17 (IBM, Chicago, IL) was used for all statistical leg, and ankle and MT5 markers the foot. Hind limb pro- calculations. Standard descriptive statistics were calcu- and retraction angles were calculated as angles of a line lated for postural variables at defined gait events, connecting the hip with MT5 at touchdown and liftoff and namely touchdown (TD), midsupport (MS), and liftoff vertical (see Fig. 2). MT5 was considered the appropriate (LO). Average angles over a stride were calculated for reference point because the animals make first contact the trunk, hip, knee, and ankle angles and the thigh and lift off at the forefoot (see below). Hind limb excursion abduction angle. Relationships of selected gait variables is the sum of pro- and retraction angles. Trunk pitch and with speed were explored using linear regressions. Varia- tilt angles were determined relative to vertical in frontal bles that were found to be significantly correlated with and sagittal planes. See Table 1 for further variable defi- speed were entered into standard multiple regressions nitions. Arm and forearm movement was recorded, but and their importance for speed modulation assessed with not quantified for this study. semipartial correlation statistics.

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