Segment and Joint Angles of Hind Limb During Bipedal and Quadrupedal Walking of the Bonobo (Pan paniscus)

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1 AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 119:37 51 (2002) Segment and Joint Angles of Hind Limb During Bipedal and Quadrupedal Walking of the Bonobo (Pan paniscus) Kristiaan D Août, 1 * Peter Aerts, 1 Dirk De Clercq, 2 Koen De Meester, 1,2 and Linda Van Elsacker 1,3 1 Department of Biology, University of Antwerp, B-2610 Antwerp, Belgium 2 Laboratory for Movement and Sport Sciences, Ghent University, B-9000 Ghent, Belgium 3 Centre for Research and Conservation, Royal Zoological Society of Antwerp, B-2018 Antwerp, Belgium KEY WORDS bonobo; kinematics; segment angles; joint angles; bipedalism; quadrupedalism; gait analysis ABSTRACT We describe segment angles (trunk, thigh, shank, and foot) and joint angles (hip, knee, and ankle) for the hind limbs of bonobos walking bipedally ( bent-hip bent-knee walking, 17 sequences) and quadrupedally (33 sequences). Data were based on video recordings (50 Hz) of nine subjects in a lateral view, walking at voluntary speed. The major differences between bipedal and quadrupedal walking are found in the trunk, thigh, and hip angles. During bipedal walking, the trunk is approximately more erect than during quadrupedal locomotion, although it is considerably more bent forward than in normal human locomotion. Moreover, during bipedal walking, the hip has a smaller range of motion (by 12 ) and is more extended (by ) than during quadrupedal walking. In general, angle profiles in bonobos are much more variable than in humans. Intralimb phase relationships of subsequent joint angles show that hipknee coordination is similar for bipedal and quadrupedal walking, and resembles the human pattern. The coordination between knee and ankle differs much more from the human pattern. Based on joint angles observed throughout stance phase and on the estimation of functional leg length, an efficient inverted pendulum mechanism is not expected in bonobos. Am J Phys Anthropol 119:37 51, Wiley-Liss, Inc. The phenomenon of bipedal locomotion in apes has received considerable attention (e.g., Aristotle, 4th century BC, 1983 translation; Jouffroy et al., 1990; Tyson, 1699; Elftman and Manter, 1934; Elftman, 1944; Jenkins, 1972, 1974; Kimura, 1985, 1996; Okada, 1985). Studies were often framed in the context of human evolution, since habitual bipedalism is generally considered the key event in the hominization process (e.g., Susman, 1984; Senut, 1992; Wood, 1992; Benton, 1997). Bipedal locomotion in apes is characterized as bent-hip, bentknee. The ancestral type of bipedal locomotion in humans may have been bent-hip, bent-knee (Stern and Susman, 1983), with a locomotor anatomy different from that of modern humans (Zihlman and Cramer, 1978; Zihlman, 1984; Jungers, 1982; Stern and Susman, 1983; Abitbol, 1995) or fully erect as in modern humans (Lovejoy, 1981; Latimer and Lovejoy, 1989; Latimer, 1991; Crompton et al., 1998; Kramer, 1999; Nagano et al., 2001) with modern locomotor anatomy (Lovejoy et al., 1973; Latimer and Lovejoy, 1989). Unfortunately, the origin of human bipedalism remains unresolved, and the position of first fully bipedal hominid, frequently attributed to Australopithecus afarensis (for an overview, see Foley and Elton, 1998), is challenged by recent new fossil findings (Senut et al., 2001; Leakey et al., 2001; Haile-Selassie, 2001). The major hypotheses propose that habitual bipedalism, unique to humans, originates from a terrestrial quadrupedal phase (Jenkins, 1972; Gebo, 1992), or that vertical climbing preceded bipedalism (Prost, 1980; Fleagle et al., 1981). However, numerous other hypotheses exist, e.g., the postural feeding hypothesis (Hunt, 1994, 1996), the food transport hypothesis (Hewes, 1961, 1964), and the aquatic ape theory (Bender et al., 1997). In order to understand the processes and constraints that involved the development of (ultimately habitual) bipedalism, an insight into its dynamics, and into possible ancestral forms, seems crucial. Interpretation of fossil material of apes and hominids is an essential starting point, but this has to be completed with behavioral information and functional morphological studies. The extant great apes, Grant sponsor: FWO-Vlaanderen; Grant number: G ; Grant sponsor: Royal Zoological Society of Antwerp. *Correspondence to: Kristiaan D Août, Laboratory for Functional Morphology, Department of Biology, University of Antwerp, Universiteitsplein 1, B-2610 Wilrijk, Belgium. kristiaan.daout@ua.ac.be Received 29 August 2001; accepted 19 February DOI /ajpa Published online in Wiley InterScience ( com) WILEY-LISS, INC.

2 38 K. D AOÛT ETAL. the closest relatives to humans, are the most relevant species to be studied because of phylogenetical (e.g., Chen and Li, 2001) and morphological (e.g., Zihlman and Cramer, 1978) affinities with early hominids. In this context, it should be stressed that no single species can be seen as a perfect model for early hominids. Moreover, there is considerable debate on human phylogeny (for overviews, see Wood, 2000; Wood and Richmond, 2000; Balter, 2001a,b) and on the species that first engaged in habitual bipedalism (see above). Therefore, one has to adopt a comparative approach and study as many species as possible (Aerts et al., 2000). In this context, the bonobo (Pan paniscus) is the species that may contribute most to our insights for various reasons. From a comparative kinesiological point of view, it is important that the bonobo resembles A. afarensis more closely, in morphological terms, than any other species (Zihlman and Cramer, 1978; Aiello and Dean, 1990). Field research reports that bonobos engage in bipedal walking in various contexts, i.e., food carrying and wading through streams (Kano, 1992). Of all apes, most kinesiological information is available for chimpanzees (Aerts et al., 2000), but gorillas (Tuttle et al., 1975, 1979; Doran, 1997) and orangutans (Tuttle and Beck, 1972; Shapiro and Jungers, 1994; Schmitt and Larson, 1995; Payne, 2001) have also been studied. In bonobos, kinesiological studies up to now are limited to Tuttle et al. (1991, 1992; footprint shape), Aerts et al. (2000; spatio-temporal gait characteristics of bipedal and quadrupedal walking), and Isler (in press; vertical climbing). In terms of spatio-temporal gait characteristics (step length, stride length, stride frequency, duty factor), walking in bonobos closely resembles walking in chimpanzees, and even humans. For any particular speed of bonobos, bipedal walking uses higer stride frequencies and lower stride lengths than quadrupedal walking (Aerts et al., 2000). The duty factor (i.e., time of ground contact of a foot relative to total cycle time) is similar during bipedal and quadrupedal walking, and does not seem to be significantly higher during vertical climbing (Isler, in press). Still, essential aspects of bonobo locomotion, and ape locomotion in general, need clarification. Is there an energy-saving mechanism in bipedal walking, as there is in humans ( inverted pendulum paradigm, e.g., Cavagna et al., 1977; Alexander, 1991)? To what extent is the bipedalism of apes comparable to that of modern humans (or early hominids)? Our aim here is to add to the kinesiological knowledge of bonobo walking by analyzing segment and joint angles. Such an analysis will provide a better understanding of the gait mechanism itself, and will allow for comparison with other primates and humans. Moreover, the results can help provide insight into the factors underlying the acquisition of habitual, erect bipedalism during human evolution. TABLE 1. Overview of individual data for bonobos studied 1 Bipedal sequences Quadrupedal sequences Range speed (m/sec) and range, dimensionless speed Average speed (m/sec) and average dimensionless speed (means std) Range speed (m/sec) and range, dimensionless speed N Average speed (m/sec) and average dimensionless speed (means std) N Distance from heel to hip (m) Age (years, months) Born in wild/captivity Sex Mass (kg) Individual number/code 1 (De) Wild Male y (Dz) Wild Female y (He) Wild Female y (Ho) Wild Female y (Ki) Captive Male y7m (Lu) Captive Male y (Re) Captive Male y 10 m (Un) Captive Female y 7 m (Vi) Captive Male 5.6 2y2m y, years; m, months.

3 BIPEDAL AND QUADRUPEDAL WALKING IN BONOBOS 39 MATERIALS AND METHODS Nine bonobos (see Table 1 for relevant details) were videotaped (Panasonic F-15 S-VHS camera, 50 fields sec 1 ) in lateral view while walking bipedally and quadrupedally in their outdoor exhibit (see Van Elsacker et al., 1993) in the Wild Animal Park of Planckendael, Belgium. A reference wall with horizontal and vertical gridlines interspaced 0.5 m was placed perpendicular to the axis of the camera. The animals walked between this wall and a water moat (see also Aerts et al., 2000). In order to promote natural behavior and to comply with the practical and ethical priorities of the Animal Park of Planckendael, the animals were not trained in any sense and were unmarked. From the video footage, 17 bipedal sequences and 33 quadrupedal sequences were retained for further analysis. Selected sequences had to contain walking, perpendicular to the camera and at a steady speed. The latter condition was assessed by means of a linear regression of the horizontal hip displacement against time; R 2 values of this regression, i.e., estimates for the linearity of this relation (i.e., constancy of speed), were above 0.97 in all selected sequences. Selected sequences were digitized field by field, using a NAC-1000 XY-coordinator connected to a Panasonic S-VHS video recorder (type AG-7350) and custom-written software. The following points were digitized from one body side: neck (dorsal side), hip (estimated position of the acetabulum), knee (frontal side), heel (posterodorsal edge), and tip of the distalmost toe. Positions of digitized points were converted to absolute values (in m), using the grid on the reference wall and parallel chalk lines on the ground, allowing for scaling differences due to differences in distance between camera and subject (see also Aerts et al., 2000). From the scaled data, four segment angles (trunk, thigh, shank, and foot) and three joint angles (hip, knee, and ankle) were calculated using basic trigonometry. We defined segment angles as the angle, in degrees, between the horizontal and the segment concerned, measured from the frontal side. Joint angles were defined as the angle enclosed by two adjacent segments, so that greater angles mean extension (hip, knee) or plantarflexion (ankle) of the joint, and smaller angles mean flexion (hip, knee) or dorsiflexion (ankle) of the joint (see Fig. 1). The raw angle data were digitally filtered, using a fourth-order zero phase-shift digital Butterworth filter (Winter, 1990) set at a cutoff frequency of five times the cycle frequency (resulting in cutoff frequencies from Hz). For differentiation, a fourth-order central difference was calculated (Biewener and Full, 1992). In addition to the angle data, we calculated absolute speed by dividing stride length with stride duration. Dimensionless walking speed was calculated as the square root of the Froude number, based on Fig. 1. Definitions of segment and joint angles. Segment angles are relative to horizontal plane; joint angles are enclosed angles between two segments. the principle of dynamic similarity, using the following formula: Dimensionless speed v2 g l, with v, absolute speed; g, gravity; and l, length from knee to heel. The latter length was used because it was least sensitive to digitization errors on unmarked subjects. Knee and heel were easily detectable, and the knee-heel segment is proportional to hind-limb length (for details, see Aerts et al., 2000). Stance time (i.e., ground contact of foot concerned) and total stride time (i.e., stance time swing time) were calculated as well. A stride was defined as starting at initial ground contact of a foot and ending at the subsequent initial ground contact of the same foot; stride length was the distance traveled during one such cycle (Alexander 1977a,b). In order to generate mean angle profiles (e.g., mean bipedal and mean quadrupedal profiles), the following procedure was followed: 1) The absolute time axes (in seconds) of the selected strides were converted to a fraction of total stride duration. 2) These data sets were run through an interpolation routine that converted all data sets to comprise exactly 41 data points, irrespective of initial number of data points. Thus, each stride was described at

4 40 K. D AOÛT ETAL. TABLE 2A. Averaged minimal angles (MIN), maximal angles (MAX), and observed range of motion (RANGE) for pooled data of all individuals (degrees; mean standard deviation) 1 Bipedal Quadrupedal Difference if significant P-value Trunk MIN MAX RANGE Thigh MIN MAX RANGE Shank MIN MAX RANGE Foot MIN MAX RANGE Hip MIN MAX RANGE Knee MIN MAX RANGE Ankle MIN MAX RANGE P-values for ANCOVA analyses are given; significantly different means, after Bonferroni correction (Sokal and Rohlf, 1995), are underlined. intervals of 2.5% of stride duration. 3) Per new data point, the mean was calculated for all sequences. 4) In the same way, standard deviations were calculated per mean to give an impression of the variation around angle curves. 5) In order to quantify the overall variation of angle curves, a coefficient of variation (CV) was calculated per mean angle curve, using the following formula: N i i 1 CV N 100/ max min ), with N the number of strides, i the stride number, 1 the standard deviation of stride i, and max and min the maximal and minimal values found during the mean angle curve, respectively. This CV is basically the standard error for the mean angle curve, as a percentage, scaled to the mean range of movement of the angle considered. In addition to the construction of mean angle curves, we selected some landmark points on these curves to allow for statistical testing of these points between bipedal and quadrupedal sequences. Four landmark points were selected: minimal (MIN) and maximal angles (MAX) found during each individual stride, angle at initial contact of the foot (IC), and angle at toe-off (TO). Furthermore, the observed range of motion (RANGE) was calculated as the TABLE 2B. Averaged angles at initial contact (IC) and toe-off (TO) for pooled data of all individuals (degrees; mean standard deviation) 1 Bipedal Quadrupedal Difference if significant P-value Trunk IC TO Thigh IC TO Shank IC TO Foot IC TO Hip IC TO Knee IC TO Ankle IC TO P-values for ANCOVA analyses are given; significantly different means, after Bonferroni correction (Sokal and Rohlf, 1995), are underlined. absolute difference between MIN and MAX. These five variables were tested using MANCOVA (Statistica 5.0). In a first design, we used gait type (bipedal or quadrupedal) and sex (male or female) as independent variables, the seven (joint and segment) angles as dependent variables, and dimensionless speed as a covariate. Such a test was run for each of the five data sets (four landmark points and RANGE). In all five data sets, there was a significant (P 0.05) general effect of gait type. Moreover, in all data sets but one (MIN), there was a significant (P 0.05) general effect of sex. However, in four data sets (MAX, RANGE, IC, and TO), there was no interaction between sex and gait type (P ranging from In the data set MIN, there was a significant interaction (P 0.032). Thus, in most cases there is a sex effect, but this does not interact with the gait-type effect, the subject of this study. Therefore, a second (ANCOVA) design was used, in which we used gait type as independent variable, the seven angles as dependent variables, and dimensionless speed as a covariate. These core results are summarized in Table 2A (MIN, MAX, and RANGE) and Table 2B (IC and TO). Differences between mean bipedal and mean quadrupedal landmarks were considered significant at P values below In a few cases, significant differences became nonsignificant after Bonferroni correction (see Tabe 2A,B). In order to compare our data with modern humans, the mean joint angles (N 19) and standard deviations in Winter (1991, his Table 3.32(b)) were used. We converted the original angle data to our angle definitions (Fig. 1). We also calculated the CV as defined above. The data set of Winter (1991)

5 BIPEDAL AND QUADRUPEDAL WALKING IN BONOBOS 41 Fig. 2. Sample joint angle profiles, bipedal (A) and quadrupedal (B), of a single individual walking at a similar speed. In A, landmark points MIN, MAX, IC, and TO, used for statistical analysis (see Materials and Methods), are indicated as an example. reports a duty factor of 0.6 for humans walking at natural cadence. RESULTS Table 1 gives an overview of the individuals studied, along with observed absolute and relative speeds. All sequences, both bipedal and quadrupedal, involve walking at an unrestrained, self-selected speed. For details on the descriptive kinematic variables (speed, step length, stride length, stride frequency, and duty factor) of walking in bonobos, refer to Aerts et al. (2000). Figure 2 shows an example of the joint angles studied (hip, knee, and ankle), as a function of time, of the hind limb of a single bonobo (individual 4 in Table 1), walking bipedally and quadrupedally at a similar speed (1.356 and m/sec, respectively; dimensionless speed, and 0.842, respectively). The X-axis shows one stride, starting with initial contact (i.e., with the heel in most cases). Similar plots were made for segment angles, and for all sequences studied. We used two main approaches to analyze these plots. The first approach consisted of a statistical analysis (ANCOVA) of five variables deduced from these plots: MIN, MAX, and RANGE, which depict the minimal and maximal values (and the resulting range of motion) found on average during a stride, and IC and TO, which depict the angles at the instant of initial contact and toe-off, respectively (see Materials and Methods and Fig. 2). The former three variables are relevant because they describe the total angular excursion found during a stride; the latter two are relevant because they describe posture at the instants relevant for locomotion. Results of the analysis are found in Table 2A (for MIN, MAX, and RANGE) and in Table 2B (for IC and TO). Significant differences between bipedal and quadrupedal walking are almost exclusively limited to proximal angles, i.e., the segment angles of trunk and thigh and, as a result, the hip joint angle. For these angles, nearly all of the five variables (MIN, MAX, RANGE, IC, and TO) are significantly different between bipedal and quadrupedal walking (see Table 2A,B for details). These results indicate that during bipedal walking, the trunk is held more erect (by approximately ; see Table 2A,B), the hip is more extended (by approximately ; see Table 2A,B), and the hip has a smaller range of motion (by 11.8 ; see Table 2A) than during quadrupedal walking. Apart from these angles, the only significant difference between bipedal and quadrupedal walking is found in the knee at toe-off (but not at initial contact or at the three other variables measured). Apparently, the difference in thigh angle at toe-off is not only reflected in the hip (proximal end of the thigh) but also, to some extent, in the knee (distal end of the thigh). In a second approach to angular data analysis, we pooled similar plots (i.e., same segment or joint angle, and same locomotion type) by averaging the plots and calculating a coefficient of variation (CV) for each pooled set of plots (see Materials and Methods). In this way, we could establish to what extent angle profiles are stereotyped in bonobos, and describe the average bonobo angle profile at voluntary speeds. Segment angles Figure 3 shows the segment angles for both bipedal and quadrupedal walking. Despite the significant differerence in trunk angle between bipedal and quadrupedal sequences (Table 2A,B, Fig. 3A,B), the trunk remains quite stable in both cases, com-

6 42 K. D AOÛT ETAL. Fig. 3. Segment angles for bipedally (A, C, E, G) and quadrupedally (B, D, F, H) walking bonobos. See Figure 1 for angle definitions. Angle profiles show average values (middle line) and angles standard deviation (top and bottom lines). Vertical lines indicate instant of toe-off (middle line) and toe-off standard deviation (left and right lines). pared to the other segments studied (note that the observed range of motion in the trunk does not differ significantly between bipedal and quadrupedal walking; Table 2A). The maximal value (i.e., most erect posture) occurs in both cases around initial contact, and the minimal value (on average, 13 less

7 BIPEDAL AND QUADRUPEDAL WALKING IN BONOBOS 43 TABLE 3. Coefficients of variation and mean standard deviations for angle profiles of segment and joint angles in bonobos walking bipedally and quadrupedaly, and for bipedally walking normal human subjects Bonobo bipedal Bonobo quadrupedal Human bipedal CV Mean std CV Mean std CV Mean std Segment angles trunk thigh shank foot Joint angles hip knee ankle in bipedal sequences and 16 less in quadrupedal sequences; Table 2A) occurs just prior to (bipedal sequences) or at the instant of (quadrupedal sequences) toe-off. In absolute terms, the trunk angle has the smallest mean standard deviation of all angles studied in bonobos (Table 3, Fig. 3B), but it is the most variable of all when accounting for the small movement range (CV 30.35% and 13.94% for bipedal and quadrupedal walking, respectively; see Table 3. Variability is evenly spread throughout the cycle during quadrupedal walking, but during bipedal walking, the swing phase is more variable than the stance phase. The general pattern of the three leg segment angles (Fig. 3), as a function of time (standardized to cycle duration), is very similar for bipedal and quadrupedal walking. At initial foot contact, leg position is almost identical. During stance phase, the thigh retracts from anterversion towards almost vertical, the shank rotates from slightly anteversed towards almost horizontal, and the foot rotates from horizontal to almost vertical. During swing phase, the three leg segments are reoriented towards the initial contact position. The range of motion of the thigh is much larger than that of the trunk, and more so during quadrupedal locomotion (59 ) than during bipedal locomotion (47 ; see Table 2A and Fig. 3C,D). Nevertheless, in both cases the profile is similar: the thigh angle remains approximately constant at the beginning of stance phase (for 10 20% of stride duration), and then decreases and starts to increase shortly before toe-off. During swing phase, the thigh angle continues to increase (i.e., the swinging forward of the thigh). Strikingly, the thigh never gets vertical (angle smaller than 90 ) during bipedal walking, or does so only to a limited extent, during quadrupedal walking. In both gait types, variability in thigh angle throughout the cycle is evenly spread. The CV is 7.03% for bipedal walking and 3.34% for quadrupedal walking, both being the highest value of any segment angle apart from the trunk angle. For shank angles (Fig. 3E,F), the plots of bipedal and quadrupedal sequences are even more similar. The shank angle is maximal at initial contact and immediately starts to decrease, until toe-off. The resemblance between bipedal and quadrupedal walking remains valid for the foot angle (Fig. 3G,H). None of the landmark points from the plots differ significantly between bipedal and quadrupedal walking (Table 2A,B) and the profiles as a whole are also similar, though it should be mentioned that the greatest variation is found in this case, and most of all during quadrupedal walking. Immediately before or at the instant of ground contact, the foot angle is maximal. The angle decreases slowly until approximately 35 (i.e., approximately half of stance phase), and then decreases more rapidly until shortly after toe-off. Then the foot angle rapidly increases again. The considerable angular movement of the whole foot during the entire stance phase is unexpected. Since our foot angles are calculated from the positions of the ankle and the toes, most likely the angular movement results from the heel being lifted during stance phase, while the midfoot and forefoot remain in contact with the ground surface (see Discussion). Joint angles The joint angles result from the segment angles of the neighboring segments and are shown in Figure 4, along with similar data for humans from literature (transformed from Winter, 1991). The hip is significantly more flexed during quadrupedal walking than during bipedal walking (by approximately ; see Table 2A,B), and the observed range of motion is 11.8 greater in quadrupedal walking (range, 53.1 ) than in bipedal walking (range, 41.3 ; see Table 2A). Nevertheless, the general pattern is similar, and comparable to the pattern in humans (Fig. 4A,C). At initial contact, the hip angle is much greater during bipedal walking (i.e., ) than during quadrupedal walking (i.e., 72.1 ), but in any case much smaller than in humans, where the hip angle at initial contact is approximately 160 and increases to approximately 180 at the end of stance phase. In bonobos, the hip extends to a maximum at the end of stance phase of, on average, only during bipedal, and during quadrupedal walking (Table 2A). The knee angle profiles of bonobos walking bipedally and quadrupedally are very similar (Fig. 4D,E), but differ from humans (Fig. 4F). Following initial contact, at a knee angle of approximately (compared to almost 180 in humans), there is knee flexion, by approximately 30, until

8 44 K. D AOÛT ETAL. Fig. 4. Joint angles for bipedally (A, D, G) and quadrupedally (B, E, H) walking bonobos and for humans walking at natural cadence (C, F, I). See Figure 1 for angle definitions. Angle profiles show average values (middle line) and angles standard deviation (top and bottom lines). Vertical lines indicate instant of toe-off (middle line) and, for bonobo data, toe-off standard deviation (left and right lines). Human data are recalculated from Winter (1991). approximately 20% of stride duration. The knee angle then changes little for approximately 20 30% of stride duration, which is in contrast to the human pattern where the knee angle increases (i.e., extension) at this stage. At the end of stance phase, the knee flexes (but the hip and ankle extend; Fig. 4A C,G I) in all cases, and reaches a minimum during swing phase. Ankle angles are also similar for bipedal and quadrupedal walking. At initial contact, the angle is approximately (Table 2B, Fig. 4G,H), as in humans (Fig. 4I). Then it soon decreases (i.e., dorsiflexion) to (see Table 2A) at 35 40% of stride duration. Plantarflexion then starts and continues until approximately toe-off. In humans, the ankle angle remains more stable during most of stance phase, and changes more sharply around maximal plantarflexion just after toe-off. Angle-angle plots In order to assess intralimb coordination, we constructed angle-angle plots of the hip and knee and of the knee and ankle (Fig. 5). The coordination between hip and knee is similar for both gait types in bonobos, and compares very well with humans (Fig. 5A C). After initial contact, a first phase of knee flexion with a relatively stable hip angle is observed (until approximately 20% of stride duration), followed by a phase of hip extension with a relatively stable knee angle until approximately 40 50% of stride duration. In humans, the knee angle increases considerably during this phase of hip extension. Next follows the major knee flexion, during which the hip first extends and then starts to flex. Then follows knee extension (during swing phase), accompanied by further flexion of the hip until just before initial contact.

9 BIPEDAL AND QUADRUPEDAL WALKING IN BONOBOS 45 Fig. 5. Phase diagrams for hip and knee relationship of bipedally walking bonobos (A), quadrupedally walking bonobos (B), and humans (C), and for knee and ankle relationship of bipedally walking bonobos (D), quadrupedally walking bonobos (E), and humans (F). Black dot on curve marks initial contact of foot; white dot marks toe-off. Arrow shows direction in which diagrams are to be read. Human diagrams are based on angle data in Winter (1991). Only mean angle profiles (as in Fig. 4) are used to construct phase diagrams. The coordination between knee and ankle is quite similar for bipedal and quadrupedal bonobos (Fig. 5D,E), but differs from humans (Fig. 5F). In bonobos, both knee and ankle angles decrease following initial contact until approximately 35% of stride duration. Then a phase of dorsiflexion follows until slightly after toe-off, while the knee keeps on flexing. Finally, during most of the swing phase, the knee extends while the ankle first dorsiflexes, and then plantarflexes. During bipedal walking, maximal dorsiflexion during swing phase is small, but during quadrupedal walking it reaches almost the same value as observed during stance phase. The kneeankle coordination in humans differs from bonobos (Fig. 5D F); movement in both joints occurs mainly from the end of stance phase with knee flexion and ankle plantarflexion until after toe-off, and continues during swing phase, with mainly knee extension (to almost 180 ) and ankle dorsiflexion. When comparing overall knee-ankle phase plots (Fig. 5D F), a pattern may be discerned in which the left loop gets gradually larger from bipedal bonobos, over quadrupedal bonobos, to humans. DISCUSSION Comparison of bonobo joint and segment angles with literature data on common chimpanzees, bonobos, and humans Okada (1985) published segment and joint angles from one chimpanzee (Pan troglodytes), one blackhanded gibbon (Hylobates agilis), one sacred baboon (Papio hamydrias), two Japanese macaques (Macaca fuscata), two spider monkeys (Ateles geoffroyi), and one human. Although these data are limited to one subject in most cases, and angle patterns are only given for the hip and knee of one bipedal trial of three species (man, chimpanzee, and baboon), they were obtained in a similar way to our methods, and can thus be used for comparison. Okada (1985) obtained several trials and described considerable variation between them (e.g., due to speed effects).

10 46 K. D AOÛT ETAL. The chimpanzee bipedal hip angle pattern (Okada, 1985, p. 51) resembles the bonobo pattern (Fig. 4A) very closely. Okada (1985) also showed hip-knee plots (phase diagrams) of the six species studied. For the chimpanzee, Okada (1985, p. 52) described different patterns for bipedal and quadrupedal walking (phase diagrams as in Fig. 5), where the quadrupedal pattern resembles human bipedalism more closely (a trend he also observed in the other species studied). This difference between bipedal and quadrupedal walking in bonobos is subtle in our study (compare Fig. 5A,B), but we used data of 50 sequences, whereas Okada (1985) only showed one sample sequence per gait type. Given the large variation observed in both bonobo and chimpanzee walking, it may be that the difference between quadrupedal and bipedal walking in the chimpanzee (found by Okada, 1985) is not significant but complies with natural variation. Still, the quadrupedal phase plot (Fig. 5E) resembles the human plot (Fig. 5F) more closely than does the bipedal plot (Fig. 5D). The knee angle plot in chimpanzees, like that of the hip (Okada, 1985), resembles that of bonobos closely. Jenkins (1972) found, in two juvenile chimpanzees, that the knee does not usually pass beneath the hip joint during bipedalism. In bonobos, this is also the case (thigh angle greater than 90 ; see Fig. 3C), and even during quadrupedalism the knee is rarely smaller than 90 (Fig. 3D). Significant femoral extension posterior to the hip joint has only been found in a chimpanzee with a modified bipedal gait due to forelimb paralysis (Bauer, 1977). Isler (in press) described hip and knee angles during vertical climbing in bonobos. The active range of motion of both joint during vertical climbing is considerably larger than during walking (i.e., hip, approximately from ; knee, approximately from ). The major difference is in the minimal hip angle, which is smaller (more flexed hip) than found, on average, for bonobo walking, either bipedally or quadrupedally (Table 2A,B). The maximal hip angle (approximately 135 ) during vertical climbing correponds well with our average of during bipedal walking (Table 2A). Maximal flexion of the knee is more pronounced, by approximately 10, in vertical climbing (Isler, in press) than in either bipedal or quadrupedal walking (Table 2A). Overall, hip and knee angles do not seem to be dramatically different between vertical climbing and walking in bonobos. Variation in segment and joint angle curves of walking bonobos The variation of angle plots we observe in bonobos is larger than in humans (e.g., Winter, 1991). We see three main possible sources of variation in the angle curves, i.e., variation due to an individual effect, variation due to sex, variation due to a speed effect, and variation due to oblique walking. Other sources of variation may be present as well. Fig. 6. Knee-angle profile for all quadrupedal sequences of individual 4 (solid lines; see Table 1 for individual details), compared to profile for all individuals combined (as in Fig. 4D). Note that standard deviation for individual 4 is almost as large as for all eight individuals (see Discussion for details). Since our data do not pertain to many individuals, and moreover the number of sequences studied per individual is very variable (from 1 12), the effect of individual variation can best be estimated by comparing a selected variable in one individual with the data from all individuals. As an example, we compare knee angle during quadrupedal locomotion in all 33 sequences with those sequences of individual 4, for which the most (12) sequences are available. The resulting graph (Fig. 6) shows that not all sequences of individual 4 group together, but rather they vary and occupy most of the range found for all sequences. The CV of the 12 sequences of individual 4 (3.26; mean std, 0.148) is almost as great as of all 33 sequences (3.63; mean std, 0.226). We conclude that individual effects are likely small, which agrees with the observation that all individuals behave similarly when scaled properly, i.e., following the principle of dynamic similarity (Aerts et al., 2000). Our analysis (see Materials and Methods) revealed that the angle profiles of the 5 males differed significantly from the 4 females studied in bipedal and quadrupedal walking. Since this sex effect did not show statistical interaction with the speed effect (i.e. the subject of this paper), we did not focus on this effect. Moreover, we cannot pinpoint whether this truly is a sex effect. Possibly this difference is due to the fact that our male and female groups differ in several other respects than sex, e.g., mean age, weight, or length. Nevertheless, the sex effect is puzzling and merits future attention. Bonobos, like other apes (e.g., Leigh, 1995), show sexual dimorphism with respect to body morphology, although dimorphism may be limited to body weight only (Cramer and Zihlman, 1978), and bonobos may be the least sexually dimorphic of the great apes. Lee (2001) found that even chimpanzees (Pan troglodytes), more sexually dimorphic than bonobos, are less dimorphic than gorillas (Gorilla gorilla) and modern humans. Aerts et al. (2000) found a significant decrease in duty factor, from approximately 0.75 to 0.6, with

11 BIPEDAL AND QUADRUPEDAL WALKING IN BONOBOS 47 increasing speed over the range of walking speeds observed (see Figs. 3, 4). Since the angle profiles have close relationships with the moment of initail contact and toe-off, it can be assumed that at least some angle profiles will shift with speed. For example, the ankle angle during bipedal walking (Fig. 4) has a clear local maximum (i.e., plantar flexion) near toe-off. Thus, this maximum occurs sooner in the cycle at earlier toef-off, i.e., at smaller duty factors of higher speeds. The speed effect likely plays a less important role in human studies, where, in most cases, speed is either imposed upon the study subject or natural cadence is studied. Our bonobo data, in contrast, range from m/sec (dimensionless speeds from , respectively). Since in humans, the duty factor also changes significantly with speed (Nilsson and Thorstensson, 1987; Minetti and Alexander, 1997; Zatsiorsky et al., 1994), the above rationale for bonobos presumably holds true, although this has, to our knowledge, not been tested explicitly. Larson and Stern (1987) and Demes et al. (1994) described oblique walking in chimpanzees (Pan troglodytes), where the overstriding feet can either be places medial to the ipsilateral hand ( inside foot) or outside the ipsilateral hand ( outside foot). We did not differentiate between inside and outside foot placements because, due to the very dark bonobo fur, we could not clearly see the placement for all sequences analyzed. Moreover, differentiation would decrease the number of degrees of freedom in statistical analysis. Nevertheless, slight differences in angle profiles due to oblique walking may be present, since they have been found in chimpanzee ground reaction forces (Demes et al., 1994) and in electromyographic recordings of shoulder muscles (Larson and Stern, 1987). Apart from the above-mentioned effects, there are likely other sources of variation; Kimura et al. (1983) also found that walking in apes is much more variable than in humans. Tardieu (1991) and Tardieu et al. (1993) suggested that chimpanzees (Pan troglodytes) have a rope walker gait in which segment kinematics are variable, to dynamically adjust the linearity of the trajectory. The same may hold true for bonobos. Up to now, we cannot pinpoint all sources of variation, but they may include behavioral factors or subtle differences in soil surface. We conclude that there is a stereotyped angle profile for bonobos, but it is much more variable than in humans. The CV we calculated gives an indication of overall variation per angle considered. It should, however, be mentioned that our CV is scaled to the range of motion observed, and thus, for an equal absolute variation, angles moving little will have the higher CV. How bent is bent-hip, bent-knee walking? The joint angles of hip and knee operate in ranges far from a completely stretched position (i.e., 180 ). On average, the hip extends to a maximal value of 138 during bipedal locomotion, and to 116 during quadrupedal locomotion. Interestingly, the movement range of the hip is approximately 12 smaller during bipedal than during quadrupedal locomotion. This corresponds with the observed smaller strides in bonobo bipedalism (Aerts et al., 2000). A similar trend for smaller angular excrusions and stride lengths was found for quadrupedal primates in general (Reynolds, 1987). The knee extends to a maximum of approximately 133 in both gait types (Table 2). In any gait, this differs strongly from the human pattern, in which the hip and knee both approach 180 (i.e., completely stretched) in a stride (Fig. 4C). Thus, kinematically, bipedal and quadrupedal walking in bonobos both show the same type of bent-hip, bent-knee walking. The difference in the hip is attributed to the more bent posture during quadrupedal walking, although even during bipedal walking, the trunk remains bent forwards by approximately 20 (Fig. 3A). Distal angles (knee and ankle) differ remarkably little. Comparison of bonobo bipedal walking with human walking We find higher CVs in bonobos than in the human data of Winter (1991), but this can be expected, given the wide range of speeds in this study, in contrast to the human data that are all from walking at preferred speed. Apart from this higher variation (see above and Kimura et al., 1983) and the general similarity of the general pattern, some differences are found. First, in the bonobo, the trunk remains bent forwards, by approximately 20 (Fig. 3A), even during bipedal locomotion. Second, the hip and knees remain considerably flexed throughout the cycle in both bipedal and quadrupedal walk (Elftman (1944) also noticed, in bipedally and quadrupedally walking chimpanzees, that the flexion of the knee continues longer than it does in man). Third, the phase relationship between the knee and ankle differs considerably (Fig. 5D F). Fourth, one striking aspect of bonobo locomotion, not found in humans, is in the foot movement throughout stance phase (Fig. 3G H). Since we calculated foot angle from the ankle and toe position, it follows that the heel is being lifted relative to the toe tips throughout stance. We argue that this phenomenon results from the presence of a midtarsal break in the ape foot that has a large amplitude, in contrast to humans. To test this idea, we videotaped the foot, in detail, during a typical bonobo stride (Fig. 7). It can be clearly seen in Figure 7 that there is indeed a marked midtarsal break. It is unclear, however, where this break occurs on an osteological level. It may either be at the calcaneo-cuboid joint, as suggested by Susman (1983), or at the cuboid-metatarsal (tarsometatarsal) joint. Future research is needed to elucidate the exact foot function in the bonobo, and to compare its function with that of the unique human foot (Meldrum, 1991).

12 48 K. D AOÛT ETAL. Fig. 7. Sample video sequence, showing foot rolloff during quadrupedal walking in a bonobo. Total contact time in this example is 800 msec. 0 msec, initial contact; 100 msec, lateral margin of the foot in contact; 260 msec, foot flat; 320 msec, start of heel lift; 600 msec, maximal flexion of the midfoot (forefoot has contact; arrowhead indicates midtarsal break; 720 msec, final phase prior to toe-off (at 800 msec in this sequence). Mechanical constraints on fully erect bipedalism Berge (1994) noted that apes are unable to simultaneously extend the knee and hip. We found this also to be the case in a fresh bonobo cadaver, although both joints can be completely stretched individually (personal observation), as observed frequently during normal behavior (personal observation). Other mechanical problems that may constrain fully erect bipedalism in bonobos are due to the inclined position of the pelvic girdle along with the shape of the spine, which is convex-curved and not S-haped as in humans (Aiello and Dean, 1990; Preuschoft et al., 1979). Erect bipedalism is likely to cause high stresses at the level of the pelvic girdle and spine. Indeed, an abnormal deformation of the spine, among other changes, was observed in a chimpanzee that walked predominantly bipedally due to forelimb paralysis (Bauer, 1977) and in Japanese macaques (Macaca fuscata) trained for bipedalism (Preuschoft et al., 1988). The mechanism of bipedal locomotion Humans walk with an energy-efficient inverted pendulum mechanism (e.g., Cavagna et al., 1977; Alexander, 1991). It is not known whether early hominids had this mechanism or not. Kimura (1996) argued that an extension of the hind limb is one of the bases for energy economy in human bipedalism. Since bonobos might be a good study species for helping to understand early hominid (e.g., Australopithecus afarensis) locomotion, we should see whether this inverted pendulum is still possible, despite a bent-hip, bent-knee mechanism that, in itself, is likely to be less efficient than a straightlegged mechanism. Abitbol (1995) suggested that the erect posture in A. afarensis (AL 288-1) must have been unlike that of modern humans. An inverted-pendulum mechanism, in which kinematic and potential energy is cyclically exchanged, is characterized by the center of mass (COM) being highest during single stance phase, as in humans. Kimura (1991) reported that, in chimpanzees (Pan troglodytes), this is also the case for individuals aged 2 years and over. At younger ages, the COM is highest during double stance (i.e., at the beginning and at the end of a stance phase of a single foot), as it is found in macaques of all ages. The COM trajectory in chimpanzees and man, during bipedalism, is found to be essentially the same (Kimura, 1990a,b, 1996; Yamazaki et al., 1979), although quantitative differences may be important (Tardieu, 1991; Tardieu et al., 1993). One prerequisite for an inverted-pendulum mechanism is that the total body COM pivots over a stiff segment (i.e., the distance between this COM and the center of pressure of the stance foot should be constant; cf. Lee and Farley, 1998). This would be the case if joint-angle changes during stance phase were very small. This study shows that individual angles change considerably during stance. However, combined movements of different joints (some flexing while others extend) are possible, obscuring functional leg length. For an estimation of functional leg length, we calculated distance from hipto-heel of a typical bipedal sequence (Fig. 8). During stance, we saw functional leg length decreased by

13 BIPEDAL AND QUADRUPEDAL WALKING IN BONOBOS 49 26% (from 30.7 to 22.6 cm), but this mostly at the end of stance phase (which may be less important, since the contralateral leg is now being loaded). The midtarsal break (Fig. 7), however, might compensate for some of this functional leg length decrease (measured by hip-heel distance alone). To check this, we calculated heel lift (Fig. 8), and added this to the hip-heel distance (Fig. 8) as an estimate, for an adult individual. Heel lift during stance reached a maximum just prior to toe-off of 10.7 cm. The combined result was that functional leg length only decreased by approximately 14% during stance (from 31.8 to 27.2 cm), but the initial pattern (until midstance) stayed almost exactly the same. The major difference was at end of stance, where the functional leg length was substantially increased due to heel lift (the first part of heel lift is a result of the midtarsal break). In humans, Kerrigan et al. (2000) found that heel rise between foot-flat and toe-off had a considerable role in decreasing the vertical displacement of the center of mass. Because of the flexion of the hip and knee throughout stance, and because we estimated functional leg length to decrease significantly during stance, we suggest that an efficient inverted-pendulum mechanism is not likely to be present in bonobos, although some energy may be exchanged. The relative inefficiency of bipedal locomotion in bonobos, we presume (and suggested for Australopithecus afarensis; Crompton et al., 1998; Nagano et al., 2001), does not necessarily mean it is less efficient than quadrupedal locomotion. Taylor and Rowntree (1973) found that chimpanzees (Pan troglodytes) running on a treadmill consumed the same amount of metabolic energy in both gait types, and Roberts et al. (1998a,b) showed that, in general, quadrupeds and bipeds consume nearly the same amount of energy to run, despite considerable differences in morphology, running mechanics, and muscle physiology (Roberts et al., 1998b). Fig. 8. Estimation of functional leg length for typical sequence of adult bonobo walking bipedally. A: Joint angles, for comparison. B: Estimate of functional leg length (upper trace) consists of distance of hip to heel (dashed line), plus elevation of heel above ground (lower trace). Note that heel lift increases the functional leg length estimate at the end of stance phase (pushoff), but that the initial decrease due to knee flexion is almost unchanged. ACKNOWLEDGMENTS We thank the Planckendael staff, and in particular the bonobo keepers, for their cooperation in the bonobo research. Sandra Nauwelaerts, Anthony Herrel, and Raoul Van Damme (University of Antwerp) and Jos Van Renterghem (University of Ghent) helped with data analysis. We also thank Karin Isler (University of Zürich) for sharing her manuscript before publication, and for fruitful discussions. Dr. C.S. Larsen and two anonymous reviewers provided constructive comments on an earlier version of the manuscript. This study was supported by project G of the FWO-Vlaanderen (to P.A., D.D.C., and L.V.E.). We also thank the Flemish Government for structural support through the Centre for Research and Conservation (Royal Zoological Society of Antwerp). LITERATURE CITED Abitbol MM Lateral view of Australopithecus afarensis: primitive aspects of bipedal positional behavior in the earliest hominids. J Hum Evol 28: Aert P, Van Damme R, Van Elsacker L, Duchêne V Spatiotemporal gait characteristics of the hind-limb cycles during voluntary bipedal and quadrupedal walking in bonobos (Pan paniscus). Am J Phys Anthropol 111: Aiello L, Dean C An introduction to human evolutionary anatomy. London: Adademic Press. Alexander RMN. 1977a. Terrestrial locomotion. 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