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Tufted capuchin monkeys are known to use both quadrupedalism and bipedalism in their natural environments. Although previous studies have investigated limb kinematics and metabolic costs, their ground reaction forces (GRFs) and center of mass (CoM) mechanics during two and four-legged locomotion are unknown. Here, we determine the hind limb GRFs and CoM energy, work, and power during bipedalism and quadrupedalism over a range of speeds and gaits to investigate the effect of differential limb number on locomotor performance. Our results indicate that capuchin monkeys use a “grounded run” during bipedalism (0.83–1.43 ms−1) and primarily ambling and galloping gaits during quadrupedalism (0.91–6.0 ms−1). CoM energy recoveries are quite low during bipedalism (2–17%), and in general higher during quadrupedalism (4–72%). Consistent with this, hind limb vertical GRFs as well as CoM work, power, and collisional losses are higher in bipedalism than quadrupedalism. The positive CoM work is 2.04 ± 0.40 Jkg−1 m−1 (bipedalism) and 0.70 ± 0.29 Jkg−1 m−1 (quadrupedalism), which is within the range of published values for two and four-legged terrestrial animals. The results of this study confirm that facultative bipedalism in capuchins and other nonhuman primates need not be restricted to a pendulum-like walking gait, but rather can include running, albeit without an aerial phase. Based on these results and similar studies of other facultative bipeds, we suggest that important transitions in the evolution of hominin locomotor performance were the emergences of an obligate, pendulum-like walking gait and a bouncy running gait that included a whole-body aerial phase. Am J Phys Anthropol, 2013. © 2012 Wiley Periodicals, Inc.
Habitual bipedal walking and running is an uncommon mode of locomotion among vertebrates, and practicing these gaits on extended lower limbs and with an upright trunk is unique to humans. Many nonhuman primates use bipedal gaits opportunistically, but they all move on flexed limbs, in a so-called bent-hip, bent-knee (BHBK) gait (reviewed in Demes,2011). Understanding the mechanics of this gait is of considerable interest to anthropologists, since BHBK gait was likely the earliest form of bipedalism in the hominin lineage (Stern and Susman,1981; Stern,2000; but see Latimer and Lovejoy,1989; Lovejoy,2005).
The kinematics and kinetics of human bipedalism have been extensively studied. It is widely accepted that the mechanical principles that are applied in human locomotion are pendulum-like swings in walking and spring-like bounces in running (Cavagna et al.,1976; Cavagna and Kaneko,1977). These two principles are not unique to bipedalism or humans, but are widespread across terrestrial animals (Cavagna et al.,1977; Heglund 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 spring-like gaits, as are the fluctuations in potential and kinetic energy: out-of-phase for the former, in-phase for the latter. These fluctuations in height can be tracked from measured ground reaction forces and have been extensively documented for human locomotion (e.g., Cavagna and Margaria,1966; Cavagna et al.,1976; Cavagna and Kaneko,1977; Donelan et al.,2002a), and the quadrupedal gaits of many animals (e.g., Cavagna et al.,1977; review in Biewener,2006), including three species of primates (Cavagna et al.,1977; Ogihara et al.,2012; O'Neill and Schmitt,2012). Additional studies have tracked CoM mechanics in bipedal birds (Muir etal.,1996; Rubenson et al.,2004; Usherwood et al.,2008), and few CoM data on the bipedal gaits of nonhuman primates have also been reported (Vereecke et al.,2006: gibbon; Ogihara et al.,2007, 2010: Japanese macaque; Kimura, 1996; Kimura and Yaguramaki,2009: chimpanzee).
When humans walk bipedally, the CoM vaults over an extended hind limb like an inverted pendulum. Some hind limb muscles are active only early and late during the stance phase to initiate and decelerate the passive swing and to modulate the transition into the next step (Knutson and Soderberg, 1995). Walking with flexed joints, on the other hand, requires prolonged activity of the antigravity muscles, which prevent the partially flexed joints from collapsing into full flexion during stance phase (Ishida et al.,1985). As muscle contractions consume metabolic energy, BHBK gait is, therefore, likely to be less economical than bipedalism on extended limbs (Crompton et al.,1998). And, indeed, it has been demonstrated that chimpanzee BHBK walking is energetically more costly than human bipedal walking on extended lower limbs (Sockol et al.,2007), and that human BHBK gait is more costly than erect bipedalism (Waters and Lundsford,1985; Duffy et al.,1997; Carey and Crompton,2005).
Although comparisons between erect and flexed bipedal gaits can offer insights into selective advantages of the unique form of bipedalism practiced by humans, a comparison of nonhuman primate quadrupedal and bipedal gaits can offer insights into adaptive scenarios driving the transition in the hominin lineage. Economy of transport is considered an important selection pressure on locomotor modes in many species (Alexander,1989, 2003), and a number of studies on the adaptive value of human bipedalism have focused on the metabolic cost per distance (i.e., net cost of transport [CoT]; Rodman and McHenry,1980; Carrier,1984; Leonard and Robertson,1997; Sockol et al.,2007; Pontzer et al.,2009). Few studies have been performed on the metabolic CoT of primate gaits that could inform such a comparison, and they are not conclusive. The classic study by Taylor and Rowntree (1973) on capuchin monkeys and chimpanzees found that the CoT is not different for their bipedal and quadrupedal gaits. More recently, Sockol et al. (2007) determined CoT for five chimpanzees, and, on average, confirmed the results by Taylor and Rowntree (1973), but when compared individually they found 10% higher costs for bipedal gaits in three of the five animals. The increase in walking CoT from quadrupedalism to bipedalism for Japanese macaques was found to be 30% (Nakatsukasa et al.,2004, 2006).
The relationships between CoM mechanics and metabolic costs are quite complex (e.g., Heglund et al.,1982a, b; Taylor,1994). CoM mechanics can provide a measure of the minimal mechanical work required during the support phase of a stride, and, by extension, provide some insight into the demands placed on the muscles that rely on metabolic energy gained from aerobic oxidation. Numerous studies have indicated that the metabolic cost of transport (CoT) are set by the mechanical demands of the support phase of a stride (e.g., Farley and McMahon,1992; Taylor,1994; Donelan et al.,2002a, b; Griffin et al.,2003; Pontzer,2007; Soo and Donelan,2010), with limb swing accounting for a much smaller fraction of metabolic cost (Marsh et al.,2004; Rubenson and Marsh,2009; Umberger,2010). The use of a pendulum-like walking gait and a bouncing running gait appears to reduce the mechanical demands on the CoM during stance (Srinivasan and Ruina,2006; Srinivasan,2011), and this should also decrease CoT. However, the exact relationship between mechanics and energetics remains elusive. Note that the use of “bouncing” mechanics does not necessarily imply elastic storage and subsequent release of passive energy in tendons and connective tissue, but, as per definition by Srinivasan and Ruina (2006), includes the shortening and lengthening of “pseudo-elastic” leg springs.
CoM mechanical energy fluctuations for the bipedal gaits of nonhuman primates have been shown to be much more in-phase than for human walking, and, consequently, recovery of mechanical energy (i.e., the exchange between these two forms of mechanical energy) is lower. For gibbons, Vereecke et al. (2006) reported recovery rates of less than 25% for the majority of bipedal strides collected, but including a few slow strides that have peak recoveries of 60 to 70%, similar to those found for human walking. Kimura (1996) and Kimura and Yaguramaki (2009) found highly variable recovery rates for chimpanzees, infants through adults. The lowest values are below 10%, the highest over 60%. Adult chimpanzees averaged 30%. Japanese macaques were reported to have vertical displacements of the CoM that differ from those of humans (Ogihara et al.,2007), and in-phase hip height (CoM proxy) fluctuations (Hirasaki et al.,2004). In a more recent paper, Ogihara et al. (2010) reported highly variable percent recoveries for bipedal Japanese macaques, ranging from 5.5 to 61.8%. Low recovery rates of 27% were found for human BHBK walking (Wang et al.,2003). CoM data for primate quadrupedal gaits are rare (Cavagna et al.,1977; Ogihara et al.,2012; O'Neill and Schmitt,2012). They are not directly comparable to the bipedal data as species and/or methods differ.
We here add ground reaction force data collected for bipedal and quadrupedal gaits of tufted capuchin monkeys and evaluate whether their CoM mechanics is fundamentally different. Capuchin monkeys are arboreal quadrupeds, but in more open habitats tufted capuchins come to the ground frequently, and terrestrially they adopt bipedal gaits in the context of transport and tool use (Fragaszy et al.,2004; Ottoni and Izar,2008; Liu et al.,2009). Because of this facultative use of bipedalism in their natural environments, they are an interesting species to study. In addition, they are one of only three nonhuman primate species for which CoT data for both quadrupedal and bipedal gaits are available (Taylor and Rowntree,1973), thus allowing a comparison of CoM work and CoT across speed and gaits. Capuchin monkeys can also be easily enticed to walk on two legs (Demes,2011), and their bipedal as well as quadrupedal locomotor kinematics have been documented (Wallace and Demes,2008; Carlson and Demes,2010; Demes,2011).
In addition to the classic CoM calculations pioneered by Cavagna (1975), we also explore CoM mechanics using a more contemporary approach based on collision mechanics (Ruina et al.,2005; Lee et al.,2011; O'Neill and Schmitt,2012). The mechanical work performed on the CoM includes the work required to redirect its path over the course of a stride. The amount of work depends on the angle between the CoM velocity and the GRF vectors. Large discrepancies from orthogonality increase the amount of work lost per stride. Gaits using pendulum-like mechanics tend to have smaller angular discrepancies than faster spring-like gaits, although these spring-like gaits could benefit from larger collision forces for tensing springs and storing passive elastic energy. Like the classic Cavagna approach, collision calculations only address the mechanical CoT. Mathematical models have shown that increasing the number of limbs in contact with the ground in a stride smoothes the down-to-up transition by decreasing the collisional angle of each limb contact (Smith and Berkemeyer,1997; Ruina et al.,2005). It is expected then, based on collisional accounting alone, that the mechanical CoT would be lower in quadrupedalism than in bipedalism at similar speeds.
Ground reaction forces for bipedal and quadrupedal gaits were recorded to test the following hypotheses:
Peak vertical GRF magnitudes are different for capuchin bipedalism and quadrupedalism.
Hind limb vertical GRF curves are different for capuchin and human bipedalism.
CoM mechanics are different for capuchin bipedalism and quadrupedalism.
CoM mechanics are different for capuchin and human bipedalism.
The lack of a difference in CoT between capuchin bipedalism and quadrupedalism (Taylor and Rowntree,1973
) is reflected in CoM work per distance for these two locomotor modes.
Testing these hypotheses contributes to an understanding of the mechanical challenges of transitioning from a quadrupedal to a bipedal gait and possible energetic consequences of such a transition. Our study is the first that documents CoM mechanics for primate bipedalism and quadrupedalism using the same subjects and applying identical methods.