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Implications for the Evolution of Human Bipedalism AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 150:76–86 (2013) Ground Reaction Forces and Center of Mass Mechanics of Bipedal Capuchin Monkeys: Implications for the Evolution of Human Bipedalism Brigitte Demes and Matthew C. O’Neill Department of Anatomical Sciences, Stony Brook University, Stony Brook, NY 11794 KEY WORDS locomotion; center of mass; bipedalism; quadrupedalism; capuchin monkey ABSTRACT Tufted capuchin monkeys are known to GRFs as well as CoM work, power, and collisional losses use both quadrupedalism and bipedalism in their natural are higher in bipedalism than quadrupedalism. The posi- environments. Although previous studies have investi- tive CoM work is 2.04 6 0.40 Jkg21 m21 (bipedalism) and gated limb kinematics and metabolic costs, their ground 0.70 6 0.29 Jkg21 m21 (quadrupedalism), which is within reaction forces (GRFs) and center of mass (CoM) mechan- the range of published values for two and four-legged ics during two and four-legged locomotion are unknown. terrestrial animals. The results of this study confirm that Here, we determine the hind limb GRFs and CoM energy, facultative bipedalism in capuchins and other nonhuman work, and power during bipedalism and quadrupedalism primates need not be restricted to a pendulum-like walking over a range of speeds and gaits to investigate the effect of gait, but rather can include running, albeit without an aer- differential limb number on locomotor performance. Our ial phase. Based on these results and similar studies of results indicate that capuchin monkeys use a ‘‘grounded other facultative bipeds, we suggest that important transi- run’’ during bipedalism (0.83–1.43 ms21) and primarily tions in the evolution of hominin locomotor performance ambling and galloping gaits during quadrupedalism (0.91– were the emergences of an obligate, pendulum-like walk- 6.0 ms21). CoM energy recoveries are quite low during ing gait and a bouncy running gait that included a whole- bipedalism (2–17%), and in general higher during quadru- body aerial phase. Am J Phys Anthropol 150:76–86, pedalism (4–72%). Consistent with this, hind limb vertical 2013. VC 2012 Wiley Periodicals, Inc. Habitual bipedal walking and running is an uncom- 2012; O’Neill and Schmitt, 2012). Additional studies mon mode of locomotion among vertebrates, and practic- have tracked CoM mechanics in bipedal birds (Muir ing these gaits on extended lower limbs and with an et al., 1996; Rubenson et al., 2004; Usherwood et al., upright trunk is unique to humans. Many nonhuman 2008), and few CoM data on the bipedal gaits of nonhu- primates use bipedal gaits opportunistically, but they all man primates have also been reported (Vereecke et al., move on flexed limbs, in a so-called bent-hip, bent-knee 2006: gibbon; Ogihara et al., 2007, 2010: Japanese maca- (BHBK) gait (reviewed in Demes, 2011). Understanding que; Kimura, 1996; Kimura and Yaguramaki, 2009: the mechanics of this gait is of considerable interest to chimpanzee). anthropologists, since BHBK gait was likely the earliest When humans walk bipedally, the CoM vaults over an form of bipedalism in the hominin lineage (Stern and extended hind limb like an inverted pendulum. Some Susman, 1981; Stern, 2000; but see Latimer and Lovejoy, hind limb muscles are active only early and late during 1989; Lovejoy, 2005). the stance phase to initiate and decelerate the passive The kinematics and kinetics of human bipedalism swing and to modulate the transition into the next step have been extensively studied. It is widely accepted that (Knutson and Soderberg, 1995). Walking with flexed the mechanical principles that are applied in human joints, on the other hand, requires prolonged activity of locomotion are pendulum-like swings in walking and the antigravity muscles, which prevent the partially spring-like bounces in running (Cavagna et al., 1976; flexed joints from collapsing into full flexion during Cavagna and Kaneko, 1977). These two principles are stance phase (Ishida et al., 1985). As muscle contractions not unique to bipedalism or humans, but are widespread consume metabolic energy, BHBK gait is, therefore, across terrestrial animals (Cavagna et al., 1977; Heglund likely to be less economical than bipedalism on extended et al., 1982a; Farley et al., 1993; Dickinson et al., 2000; Biewener, 2003, 2006). Fluctuations in the height of the center of mass (CoM) are different for pendulum- and Grant sponsor: National Science Foundation; Grant number: BCS 0548892. spring-like gaits, as are the fluctuations in potential and kinetic energy: out-of-phase for the former, in-phase for *Correspondence to: Brigitte Demes, Department of Anatomical the latter. These fluctuations in height can be tracked Sciences, Stony Brook University, Health Sciences Center, Stony from measured ground reaction forces and have been Brook, NY 11794-8081, USA. E-mail: [email protected] extensively documented for human locomotion (e.g., Cavagna and Margaria, 1966; Cavagna et al., 1976; Received 26 June 2012; accepted 6 September 2012 Cavagna and Kaneko, 1977; Donelan et al., 2002a), and the quadrupedal gaits of many animals (e.g., Cavagna DOI 10.1002/ajpa.22176 et al., 1977; review in Biewener, 2006), including three Published online 2 November 2012 in Wiley Online Library species of primates (Cavagna et al., 1977; Ogihara et al., (wileyonlinelibrary.com). VC 2012 WILEY PERIODICALS, INC. DYNAMICS OF CAPUCHIN MONKEY BIPEDALISM 77 limbs (Crompton et al., 1998). And, indeed, it has been walking. Kimura (1996) and Kimura and Yaguramaki demonstrated that chimpanzee BHBK walking is ener- (2009) found highly variable recovery rates for chimpan- getically more costly than human bipedal walking on zees, infants through adults. The lowest values are below extended lower limbs (Sockol et al., 2007), and that 10%, the highest over 60%. Adult chimpanzees averaged human BHBK gait is more costly than erect bipedalism 30%. Japanese macaques were reported to have vertical (Waters and Lundsford, 1985; Duffy et al., 1997; Carey displacements of the CoM that differ from those of and Crompton, 2005). humans (Ogihara et al., 2007), and in-phase hip height Although comparisons between erect and flexed (CoM proxy) fluctuations (Hirasaki et al., 2004). In a bipedal gaits can offer insights into selective advantages more recent paper, Ogihara et al. (2010) reported highly of the unique form of bipedalism practiced by humans, a variable percent recoveries for bipedal Japanese maca- comparison of nonhuman primate quadrupedal and ques, ranging from 5.5 to 61.8%. Low recovery rates of bipedal gaits can offer insights into adaptive scenarios 27% were found for human BHBK walking (Wang et al., driving the transition in the hominin lineage. Economy 2003). CoM data for primate quadrupedal gaits are rare of transport is considered an important selection pres- (Cavagna et al., 1977; Ogihara et al., 2012; O’Neill and sure on locomotor modes in many species (Alexander, Schmitt, 2012). They are not directly comparable to the 1989, 2003), and a number of studies on the adaptive bipedal data as species and/or methods differ. value of human bipedalism have focused on the meta- We here add ground reaction force data collected for bolic cost per distance (i.e., net cost of transport [CoT]; bipedal and quadrupedal gaits of tufted capuchin monkeys Rodman and McHenry, 1980; Carrier, 1984; Leonard and and evaluate whether their CoM mechanics is fundamen- Robertson, 1997; Sockol et al., 2007; Pontzer et al., tally different. Capuchin monkeys are arboreal quadru- 2009). Few studies have been performed on the meta- peds, but in more open habitats tufted capuchins come to bolic CoT of primate gaits that could inform such a com- the ground frequently, and terrestrially they adopt bipedal parison, and they are not conclusive. The classic study gaits in the context of transport and tool use (Fragaszy by Taylor and Rowntree (1973) on capuchin monkeys et al., 2004; Ottoni and Izar, 2008; Liu et al., 2009). and chimpanzees found that the CoT is not different for Because of this facultative use of bipedalism in their natu- their bipedal and quadrupedal gaits. More recently, ral environments, they are an interesting species to study. Sockol et al. (2007) determined CoT for five chimpan- In addition, they are one of only three nonhuman primate zees, and, on average, confirmed the results by Taylor species for which CoT data for both quadrupedal and and Rowntree (1973), but when compared individually bipedal gaits are available (Taylor and Rowntree, 1973), they found 10% higher costs for bipedal gaits in three of thus allowing a comparison of CoM work and CoT across the five animals. The increase in walking CoT from speed and gaits. Capuchin monkeys can also be easily quadrupedalism to bipedalism for Japanese macaques enticed to walk on two legs (Demes, 2011), and their was found to be 30% (Nakatsukasa et al., 2004, 2006). bipedal as well as quadrupedal locomotor kinematics have The relationships between CoM mechanics and meta- been documented (Wallace and Demes, 2008; Carlson and bolic costs are quite complex (e.g., Heglund et al., Demes, 2010; Demes, 2011). 1982a,b; Taylor, 1994). CoM mechanics can provide a In addition to the classic CoM calculations pioneered measure of the minimal mechanical work required during by Cavagna (1975), we also explore CoM mechanics the support phase of a stride, and, by extension, provide using a more contemporary approach based on collision some insight into the demands placed on the muscles that mechanics (Ruina et al., 2005; Lee et al., 2011; O’Neill rely on metabolic energy gained from aerobic oxidation. and Schmitt, 2012). The mechanical work performed on Numerous studies have indicated that the metabolic cost the CoM includes the work required to redirect its path of transport (CoT) are set by the mechanical demands of over the course of a stride. The amount of work depends the support phase of a stride (e.g., Farley and McMahon, on the angle between the CoM velocity and the GRF vec- 1992; Taylor, 1994; Donelan et al., 2002a,b; Griffin et al., tors.
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