Dynamic plantar pressure distribution during terrestrial locomotion of bonobos (Pan paniscus).код для вставкиСкачать
AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 120:373–383 (2003) Dynamic Plantar Pressure Distribution During Terrestrial Locomotion of Bonobos (Pan paniscus) Evie Vereecke,1* Kristiaan D’Août,1 Dirk De Clercq,2 Linda Van Elsacker,1,3 and Peter Aerts1 1 Department of Biology, University of Antwerp, B-2610 Wilrijk, Antwerp, Belgium Laboratory for Movement and Sport Sciences, Ghent University, B-9000 Ghent, Belgium 3 Royal Zoological Society of Antwerp, B-2018 Antwerp, Belgium 2 KEY WORDS foot function; bipedal/quadrupedal walking; primate locomotion; pedobarography ABSTRACT We collected high-resolution plantar pressure distributions of seven bonobos during terrestrial bipedal and quadrupedal locomotion (N ⫽ 146). Functional foot length, degree of hallux abduction, and total contact time were determined, and plots, showing pressure as a function of time for six different foot regions, were generated. We also studied five adult humans for comparison (N ⫽ 13). Both locomotion types of the bonobo show a large variation in plantar pressure distributions, which could be due to the interference of instantaneous behavior with locomotion and differences in walking speed and body dimensions. The heel and the lateral midfoot typically touch down simultaneously at initial ground contact in bipedal and quadrupedal walking of bonobos, in contrast with the typical heel-strike of human bipedalism. The center of pressure follows a curved course during quadrupedalism, as a consequence of the medial weight transfer during mid-stance. Bipedal locomotion of bonobos is characterized by a more plantar positioning of the feet and by a shorter contact time than during quadrupedal walking, according to a smaller stride and step length at a higher frequency. We observed a varus position of the foot with an abducted hallux, which likely possesses an important sustaining and stabilizing function during terrestrial locomotion. Am J Phys Anthropol 120:373–383, 2003. The acquisition of habitual bipedalism is a puzzling aspect of human evolution and, unsuprisingly, research concerning this topic is quite extensive (e.g., Susman, 1984; Rose, 1991; Susman and Stern, 1991; Senut, 1992; Wood, 1992; Zihlman, 1992; Jablonski and Chaplin, 1993; Benton, 1997). However, these investigations are mainly limited to hominid fossils. We think that a comparative analysis of the locomotion of extant nonhuman primates can give valuable information on the mechanics of bipedalism and add to the interpretation of fossil findings. Since none of the extant apes can be considered as a perfect model for the hominid ancestor, this research requires data from as many relevant ape species as possible (Fleagle, 1979, 1999; Fleagle et al., 1981; Aerts et al., 2000). For several reasons, we chose to focus on the bonobo (Pan paniscus). First of all, bonobos are, together with chimpanzees, our closest living relatives, showing only 1.2% difference in genetic material with Homo sapiens (Chen and Li, 2001). Secondly, bonobos live in the tropical rainforest, a habitat similar to that of the common ancestor (Kano, 1992). It seems reasonable to assume that the bonobo should therefore have a similar morphology as our common ancestor. Analyses of the functional morphology of (pre)hominid fossils and bonobos show that the bonobo likely resembles the common hominoid ancestor and the early hominids more than any other African ape species (Zihlman and Cramer, 1978; Zihlman et al., 1978; McHenry and Corruccini, 1981; Zihlman, 1984; McHenry, 1984; Kano, 1992). Since we study locomotion and functional morphology, it is thus meaningful to use bonobos as a model for the prehominid condition. Thirdly, bonobos quite often engage in bipedal walking, compared to other great apes (up to 8%; Doran, 1989; Susman et al., 1980; Susman, 1984). And lastly, most of the current studies apply to common chimpanzees (e.g., Jenkins, 1972; Bauer, 1977; Kimura et al., 1977, 1983; Kimura, 1985, 1990, 1996; Ishida et al., 1985; Okada, 1985; Li et al., 1996), but data on bonobo locomotion and functional morphology are scarce. With this paper, we hope to add relevant data to our current knowledge of ape locomotion. © 2003 WILEY-LISS, INC. © 2003 Wiley-Liss, Inc. Grant Sponsor: FWO-Flanders; Grant number: G.0209.99; Grant Sponsor: University of Antwerp. *Correspondence to: Evie Vereecke, Laboratory of Functional Morphology, Department of Biology, University of Antwerp, Universiteitsplein 1, B-2610 Wilrijk, Belgium. E-mail: Evie.Vereecke@ua.ac.be Received 24 January 2002; accepted 27 June 2002. DOI 10.1002/ajpa.10163 Published online in Wiley InterScience (www.interscience.wiley. com). 374 E. VEREECKE ET AL. TABLE 1. Origin, sex, year of birth, weight, and number of analyzed sequences of different individuals Number of sequences Qped 1 Individual (origin) Dz (wild) Ki (zoo) He (wild) Ho (wild) Ko (wild) Re (zoo) Un (zoo) Vi (zoo) Zo (zoo) Za (zoo) Total 1 Sex Year of birth F M F F F M F M F M 1971 1983 1978 1978 1982 1990 1993 1994 1999 1999 Bped Weight (kg) 2000 2001 2000 2001 36.3 46.1 37.0 36.7 47.3 34.0 18.5 5.1 5.8 0 14 5 5 7 21 15 8 0 0 75 0 3 2 6 4 11 7 4 0 0 37 0 0 1 12 0 2 0 0 0 0 15 0 2 5 12 0 0 0 0 0 0 19 Wild, born in Democratic Republic of Congo; zoo, born in captivity; Bped, bipedal; Qped, quadrupedal. This paper fits in current research on terrestrial walking of bonobos, with the aim of getting a full insight into their locomotory pattern, with special emphasis on the differences between bipedalism and quadrupedalism. Aerts et al. (2000) dealt with the relations of spatio-temporal gait characteristics and walking speed. It was demonstrated that smaller steps at a higher frequency were used during bipedal walking. Furthermore, the spatio-temporal gait characteristics of bonobos appeared to be highly comparable with those of other extant homininae. In order to get a full understanding of bonobo locomotion, an integrated setup in a zoo environment was constructed to get additional information on groundreaction forces and plantar pressure distributions, together with three-dimensional (3D) video images (D’Août et al., 2001). The segment and joint angles of the hindlimb during terrestrial locomotion of bonobos are described by D’Août et al. (2002). It was found that the major differences between quadrupedalism and bipedalism are situated proximally (trunk, thigh, and hip angles), and that the bipedal walking of bonobos is clearly “bent-hip, bent-knee.” In continuation of those studies, we wanted to focus on dynamic plantar pressure distributions during terrestrial walking of bonobos. So far, only a few studies have collected plantar pressure data of primates. Since the late nineteenth century, when Carlet (1872) and Marey (1873) developed the first method to examine plantar pressures, the techniques for the sampling of plantar pressure profiles have been ameliorated continuously, with the eventual development of pressure mats and pressure sensors in the last few decades. The field of application was mainly restricted to the medical world and to sport sciences. However, the setup used in this study was developed not only for medical goals, but also for acquiring quantitative measurements. Elftman and Manter (1935; see also Elftman, 1944) were the first researchers who made a comparison between human and chimpanzee (Pan troglodytes) bipedalism on the basis of plantar pressure distributions. Recently, Wunderlich (1999, using 16 ⫻ 16 cm pressure mats and sampling at 11 Hz; see also Wunderlich and Ford, 2000) made an extensive comparison between plantar pressure distributions of different primate species, including common chimpanzees. To date no study has focused on the bonobo, despite the notion that this may be an especially interesting model for our common ancestor among the living apes (Coolidge, 1933; Zihlman and Cramer, 1978). In the current study, we focus on the plantar pressure distributions, hallux function, and other pedal characteristics during terrestrial walking of the bonobo. We examine if general roll-off patterns exist for bonobos; what the differences are between bipedal and quadrupedal walking; and how they compare to the human pattern. MATERIALS AND METHODS Ten bonobos are held in seminatural circumstances on the bonobo island of the animal park Planckendael in Muizen, Belgium (Van Elsacker et al., 1993). The data used in this study are taken from seven bonobos of this group (Table 1). No samples were taken from the oldest and the two youngest bonobos. The data were collected during July, August, and September 2000 (47 recording days), and during July, August, September, and October 2001 (36 recording days). A 7-m-long ⫻ 1-m-wide horizontal catwalk was built on the bonobo island, equipped with three force plates and three pressure distribution platforms, two of 0.5 ⫻ 0.4 m (units B and C: 64 ⫻ 64 pressure sensors) and one of 1.0 ⫻ 0.4 m (unit A: 128 ⫻ 64 pressure sensors) in each case. These were built in a concrete construction and covered with a rubber sheet. A reference wall 7-m-long ⫻ 2-m-high was set behind the catwalk, provided with a reference grid. The wall is set vertically along the catwalk, but the lowest 0.4 m is set at an angle of 45° with the catwalk, to offer enough space for the bonobos to move. The three force plates (AMTI, Advanced Mechanical Technology, Inc., excitation voltage 10 V nominal) give us the 3D ground reaction forces Fx, lateral force (towards the waterside); Fy, longitudinal force (towards the island); and Fz, vertical force (downwards). Dynamic plantar pressure measure- PLANTAR PRESSURE OF BONOBOS ment is performed at high temporal and spatial resolution (250-Hz sampling and 16,384 pressure sensors of 0.375 cm2), using three pressure mats (RSscan International) which are secured onto the force plates. The pressures are calibrated online with the ground reaction forces, allowing an accurate pressure sampling, and the three measuring systems are synchronized. Recordings as well as further data processing are carried out by means of Footscan mst software 6.2 and 6.3 (RSscan International). Two S-VHS cameras (50 Hz) were set perpendicular to each other, to record the lateral and frontal view of the catwalk (for more details, see D’ Août et al., 2001). On each recording day, the amplifiers were balanced, the force plates and the pressure mats were calibrated, and the catwalk was checked. Subsequently, the bonobos were released on the island, and they could choose freely how and when to walk over the catwalk. Because they seldom walked bipedally over the catwalk, they were encouraged to do so by throwing them food and giving them plastic casks. This is comparable with the locomotory behavior of wild bonobos, which use bipedalism when carrying food and other objects (Kano, 1992). Since we worked in zoo circumstances, direct contact with the animals was prohibited, which resulted in a relatively small number of bipedal footprints sampled. Each time a bonobo walked (bipedally or quadrupedally) over the catwalk, the force plates and the pressure mats were activated. The lateral and frontal views of the catwalk were simultaneously videotaped. Specific weather conditions that could influence measurements were noted (e.g., rain). For analysis, we selected sequences (N ⫽ 146) where the force output was recorded during whole ground contact and where the pressure profile (or footscan image) showed at least a complete foot. The center of pressure (COP) during contact time was calculated as a function of time for every footscan image. Several measurements were taken on the pressure profiles (Fig. 1a; only for the data collected in 2000, N ⫽ 90): 1) the functional foot length, L, i.e., the distance between the most proximal point of the heel to the most distal point of digit II; 2) the degree of abduction, B, i.e., the angle between the length axis of digit I and digit II; 3) the contact time, t, i.e., the time between initial foot contact and toe-off; and 4) the velocity, v, estimated on the basis of lateral video images if these were available (Table 2a,b). We defined six foot regions on the basis of the functional morphology of the bonobo foot: 1) the heel (H1 and H2, 6.750 cm2), 2) the lateral midfoot (V2, 3.375 cm2), 3) the medial midfoot (V1, 3.375 cm2), 4) the lateral metatarsal heads (M II–V; 13.500 cm2), 5) the lateral toes (T II–V, 13.500 cm2), and 6) the hallux (M I and T I; 6.750 cm2; see Fig. 1b). For every foot region, the average pressure was plotted as a function of time, which was normalized against the duration of ground contact (total duration of stance phase ⫽ 100%). Impulses were calcu- 375 Fig. 1. a: Example of footscan image, recorded by footscan pressure mats, showing maximal pressures under a right bonobo foot during ground contact in a quadrupedal walking sequence. Dotted line in foot illustrates displacement of center of pressure (dot interspace, 4 msec). Two measurements are taken on the profiles, i.e., functional foot length, represented by line L, and degree of abduction, i.e., angle B between length axis of hallux and digit II (line L). b: Footscan image, showing assessment of 14 foot regions: H1, medial heel; H2, lateral heel; V1, medial midfoot; V2, lateral midfoot; M1–M5, metatarsal heads I–V; T1–T5, phalanges I–V. In this example there is no contact of the second and third metatarsal heads, and of the second toe. lated as the time integral of the vertical force (i.e., pressure (N/cm2)* area (cm2)). Relative impulses are the impulses divided by the total impulse under the foot. Relative peak pressures under the metatarsal heads and toes were calculated as maximal pressures normalized for body weight. We processed 13 pressure profiles of five nonpathological, adult humans following the same procedure, for comparison. 376 E. VEREECKE ET AL. TABLE 2A. Average (X) and standard deviation (SD) of functional foot length, degree of abduction, and total contact time during quadrupedal terrestrial locomotion Individual N Foot length, X ⫾ SD (10⫺2 m) Abduction, X ⫾ SD (°) Contact time, X ⫾ SD (sec) He Ho Ki Ko Re Un Vi Total 5 5 14 7 21 15 8 75 19.7 ⫾ 1.0 17.4 ⫾ 2.3 17.6 ⫾ 1.1 21.1 ⫾ 0.9 20.5 ⫾ 1.3 19.7 ⫾ 1.1 17.2 ⫾ 1.8 19.3 ⫾ 1.9 29.2 ⫾ 9.9 31.7 ⫾ 13.5 33.4 ⫾ 6.2 41.1 ⫾ 3.0 24.3 ⫾ 6.2 13.9 ⫾ 7.5 52.1 ⫾ 18.7 28.9 ⫾ 14.4 0.895 ⫾ 0.139 0.865 ⫾ 0.448 0.669 ⫾ 0.076 0.847 ⫾ 0.298 0.913 ⫾ 0.189 0.667 ⫾ 0.090 0.607 ⫾ 0.089 0.775 ⫾ 0.217 TABLE 2B. Average (X) and standard deviation (SD) of functional foot length, degree of abduction, and total contact time during bipedal terrestrial locomotion Individual N Foot length X ⫾ SD (10⫺2 m) He Ho Re Total 1 12 2 15 18.0 19.3 ⫾ 2.3 22.2 19.4 ⫾ 2.5 Abduction, X ⫾ SD (°) 28.0 ⫾ 10.8 28.0 ⫾ 10.8 Contact time, X ⫾ SD (sec) 0.528 0.623 ⫾ 0.318 0.274 ⫾ 0.150 0.570 ⫾ 0.310 These human footscan images were collected at the Laboratory for Movement and Sport Sciences, University of Ghent (Ghent, Belgium). Statistical analyses were executed on total contact time, degree of hallux abduction, and relative impulses. We tested for a difference between humans and bonobos and between quadrupedalism and bipedalism in bonobos. The data are not paired, and are normally distributed (Shapiro-Wilks, 0.9 ⬍ W ⬍ 0.95), so we could use the parametric Student’s t-test (Statistica 5.0 for Windows). This t-test was also used to analyze the relative peak pressures under the metatarsals and toes. Furthermore, the Pearson product moment correlation coefficient between degree of hallux abduction and relative peak pressure under the hallux (i.e., maximal pressure/body weight) was calculated from the mean values of all seven animals (Statistica 5.0 for Windows). RESULTS Our results consist of a general description of the plantar pressures of quadrupedal and bipedal walking of bonobos, together with a short description of human bipedalism. The latter does not contain new findings, but we will use this description in our comparison with the collected data of the bonobos. We found that the center of pressure (COP) follows a typical curved course during quadrupedal walking of bonobos (Fig. 2a). This is caused by a footfall pattern in which the heel and lateral midfoot touch down simultaneously at the beginning of the stance phase, followed by an anterior progression of the COP during foot-flat and mid-stance, and by a medial transfer of pressure across the metatarsal heads at heel-off. At toe-off, the lateral toes and/or the hallux leave the substrate last. In almost all cases (67/75) there is an important pressure region under the lateral midfoot, near the tuberosity of the Fig. 2. Examples of footscan images during quadrupedal (a– c) and bipedal walking (d) of bonobos. Plantar pressure profiles in a and d are from a left bonobo foot, those in b and c from a right bonobo foot. During quadrupedal locomotion (a– c), initial contact is made by the heel. Then the center of pressure moves anteriorly towards the metatarsal heads and lateral toes, and eventually bends towards the hallux. During bipedalism (d), initial contact is made by the lateral midfoot and the center of pressure moves eventually towards the hallux. Note the variability in plantar pressure distributions, with a V-curved pattern in b and an almost straight course of center of pressure (indicated by dotted line) in c, in contrast with the general pattern with a curved course of center of pressure, shown in a. metatarsal V head. This region of pressure was even present after the heel left the substrate (heel-off). However, there is high variability of footfall patterns during quadrupedal walking. In some cases (20/75), an almost straight course of the COP was observed, starting from the lateral side of the heel and travelling to metatarsal and digit II (Fig. 2c). Occasionally (5/75), the hallux hits the ground first and/or the COP follows a V-curved course (17/75; Fig. 2b). The order in which the different foot regions, especially the metatarsals and the toes, touch down is also very variable. As a consequence of the varus position of the foot, i.e., the inverted position of the foot with curved toes, there is often no contact from the metatarsal heads II–III and the medial midfoot with the ground (Fig. 3a). The plots of pressure as function of time give following results for quadrupedalism (Fig. 4a). There is generally a marked peak pressure under the heel at initial contact, which is larger than the PLANTAR PRESSURE OF BONOBOS 377 Fig. 3. Examples of roll-off patterns of left foot during quadrupedal (a) and bipedal (b) walking of a bonobo and during human bipedalism (c). Progress in time is indicated in milliseconds above every footscan image. In quadrupedal footprint (a), the heel and lateral midfoot touch down simultaneously, then medial midfoot and lateral toes touch down, and finally the hallux hits the substrate. In the bipedal footprint of the bonobo (b), the heel and hallux hit the ground first, and the foot rolls mediolaterally over the lateral toes. In a typical human footfall (c), initial contact is made by the heel, then the lateral midfoot makes contact with the substrate, and finally the metatarsal heads and toes make touchdown. Toe-off generally occurs through the big toe. peak pressure under the lateral toes at toe-off. On average, the pressure under the hallux is larger than that under the lateral toes during toe-off, although 4 of the 7 individuals are characterized by a pressure under the hallux, which is smaller or equal to the pressure under the lateral toes. The other 3 individuals (Ho, Ko, and Vi) have markedly larger pressure under the hallux than under the lateral toes. Two of those individuals (Ko and Ho) are also characterized by a high degree of abduction of the hallux (Table 4), and therefore we examined whether a high degree of abduction correlates with a higher maximum peak pressure under the hallux. A correlation coefficient between the degree of hallux abduction and the relative peak pressure under the hallux (maximum pressure divided by body weight) was defined, but this was not found to be statistically significant (Pearson product moment correlation coefficient, r ⫽ 0.72, N ⫽ 7, P ⫽ 0.067). The course of the COP seems even more variable during bipedal locomotion. In most cases (10/15), the COP starts at the lateral side, somewhat before the calcaneus, and travels further anteriorly, under the lateral or central part of the foot. Near the metatarsal heads, the COP stagnates and eventually bends off towards the hallux, but we also observed (4/15) a V-curved course of the COP (Fig. 2d). During bipedalism, the hallux usually hits the ground earlier than the lateral toes (Fig. 3b). Fig. 4. Average pressure (N/cm2) for six different foot regions as a function of time (%) during quadrupedal (a) and bipedal (b) walking of bonobos, and during human bipedalism (c). Different foot regions are: H, heel; V1, medial midfoot; V2, lateral midfoot; M, metatarsal heads II–V; T, lateral toes II–V; Hallux, metatarsal I head and digit I. Note apparent peak pressure under the heel in a and c, and absence of such a peak pressure in b. Compare also the relative high pressure under the lateral midfoot, which remains after heel-off (pressure under heel ⬎ 0 N/cm2) in a and b, with the relatively low pressure seen in c, which disappears at heel-off. Graphs of bipedal walking sequences, in which pressure is plotted against time, show a very irregular pattern where every foot region touches the ground during 90 –100% of the total contact time (Fig. 4b). A clear peak pressure under the heel is absent, and the heel occasionally touches down in the second half of the stance phase. Pressure distributions under the heel, medial midfoot, metatarsal heads, and hallux are relatively constant throughout the stance phase. Compared with quadrupedalism, there is a more plantar configuration of the foot during bipedal locomotion. At toe-off there is a pressure under the lateral toes, but a peak pressure under the hallux is absent. The human footfall pattern is rather stereotyped and is characterized by a slightly curved course of 378 E. VEREECKE ET AL. where none of the foot regions was significantly different from the other regions. Finally, we investigated the differences in relative peak pressure under the metatarsals, toes, and digits. The pressure under the fifth metatarsal is significantly higher than under central metatarsals II and III (P ⬎ 0.001 and P ⬍ 0.01, respectively), but did not differ significantly from the first metatarsal (P ⬎ 0.1). The relative peak pressure under the first toe was, however, significantly higher than under the second and fifth toes (P ⬍ 0.01 and P ⬍ 0.05). The relative peak pressure under the second digit is significantly smaller than under the other digits. DISCUSSION Fig. 5. Example of footscan image, showing maximal pressures under a left human foot during ground contact in a bipedal walking sequence. Dotted line in foot illustrates displacement of center of pressure (dot interspace, 4 msec). the COP. This point runs from the heel over the metatarsal II head and towards the hallucal digit (or eventually towards digit II) during stance phase (Fig. 5). At heel-strike only the heel touches down, at foot-flat the lateral midfoot and metatarsal heads touch down, and lastly, the lateral toes and hallux touch down (Fig. 4c). In the second half of the stance phase, the pressure under the metatarsal heads is larger than under the hallux, and this in turn is larger than the pressure under the lateral toes (Fig. 4c). For more detailed descriptions, see Inman et al. (1981), Perry (1992), Aiello and Dean (1996), and Whittle (1996). We executed some statistical analyses (Student’s t-test) to test the significance of hallucal abduction and contact time, in order to get a more quantified image of the different gait types (Table 2a,b). We did not find a significant difference in degree of abduction of the hallux between bipedal and quadrupedal locomotion (P ⬎ 0.1; Table 3). The total contact time of the foot during stance phase, i.e., the time between initial contact and toe-off, is significantly shorter during bipedalism than during quadrupedalism (t ⫽ ⫺3.09, df ⫽ 88, P ⬍ 0.005; Table 3). There is no significant difference in contact time between the bipedalism of bonobos and humans (t ⫽ ⫺0.49, df ⫽ 26, P ⬍ 0.1; Table 3). However, the contact time during quadrupedal locomotion of the bonobo is significantly larger than during human bipedalism (t ⫽ 2.67, df ⫽ 86, P ⬍ 0.01; Table 3). The relative impulses were also statistically tested (Student’s t-test), and there appeared to be no significant difference between bipedalism and quadrupedalism of bonobos and human bipedalism. Within a gait type there were significant differences in regional relative impulses, except for bonobo bipedalism, Our results point to some differences between quadrupedalism and bipedalism of bonobos, and lead to the formulation of some questions that are discussed below. Comparisons between different gait types Despite the highly variable bipedal pattern of the bonobo, we were able to detect some differences between the quadrupedal and bipedal locomotion of bonobos. Moreover, we could make a comparison with the human pedobarographic pattern. The total contact time of the bonobo foot during bipedal walking is significantly smaller than the contact time during quadrupedal walking. This is in accordance with the smaller step length and higher step frequency of bonobo bipedalism, as previously described by Aerts et al. (2000). The relatively constant pressure under the heel, medial midfoot, metatarsal heads, and hallux through stance phase, together with the comparable relative impulses under the foot regions and the absence of a peak pressure under the heel at initial contact, point to a flatter and more plantar configuration of the feet during bipedal bouts. This increases the supporting surface of the foot, and thus likely helps to obtain stability and maintain balance during bipedal locomotion. The plantar pressure distribution of human bipedalism is clearly more stereotyped than that of bonobos. In humans, only the heel touches the ground at heel-strike, followed by the lateral midfoot and forefoot. This is in contrast with the pattern in bonobo walking, where the heel and lateral midfoot typically touch down simultaneously, which is reflected in the distribution of fat tissue over the lateral and back part of the foot sole (the heel pad, personal observations). As a consequence of the presence of a plantar longitudinal arch in the human foot (Aiello and Dean, 1996; Whittle, 1996), there is no contact from the medial midfoot with the substrate (in nonpathological, adult humans). In bonobos, in which a longitudinal arch is absent (personal observations), contact of the medial midfoot is variable, but we never observed a high loading of the medial part of the bonobo foot. 379 PLANTAR PRESSURE OF BONOBOS TABLE 3. Results of Student’s t-test Abduction Q vs. B Contact time Q vs. B Contact time B vs. H Contact time Q vs. H 1 Q B 28.9 ⫾ 14.4 0.775 ⫾ 0.217 28.0 ⫾ 10.8 0.570 ⫾ 0.310 0.570 ⫾ 0.310 0.775 ⫾ 0.217 H T df P 0.613 ⫾ 0.059 0.613 ⫾ 0.059 0.21 ⫺3.09 ⫺0.49 2.67 84 88 26 86 0.83 0.003 0.6 0.009 Q, quadrupedalism, bonobo (N ⫽ 75); B, bipedalism, bonobo (N ⫽ 15); H, human bipedalism (N ⫽ 13). TABLE 4. Average pressure (X), standard deviation (SD), and maximal pressure/body mass (MAX/MASS) under hallux for all individuals during quadrupedal locomotion (N ⫽ 75) Individual He Ho Ki Ko Re Un Vi Total Body mass (kg) Abduction (°) X ⫾ SD (N/cm2) MAX/MASS 46.1 37.0 36.3 36.7 47.3 34.0 18.5 36.6 ⫾ 9.5 29.2 ⫾ 9.9 31.7 ⫾ 13.5 33.4 ⫾ 6.2 41.1 ⫾ 3.0 24.3 ⫾ 6.2 13.9 ⫾ 7.5 52.1 ⫾ 18.7 28.9 ⫾ 14.4 6.02 ⫾ 6.12 23.14 ⫾ 15.15 4.85 ⫾ 5.34 13.10 ⫾ 10.89 5.06 ⫾ 6.23 7.73 ⫾ 5.61 7.35 ⫾ 12.27 9.61 ⫾ 6.59 0.17 0.60 0.32 0.49 0.29 0.22 0.59 0.38 ⫾ 0.18 Variability of plantar pressure distribution in bonobos We observed a large interindividual variation in plantar pressure distributions of terrestrial walking of bonobos, but within an individual the footfall pattern seems relatively stable, such that it is possible to recognize the individual on the basis of footscan images. When variation within an individual is detected, this can often be ascribed to the occurrence of a different pattern for the left and right foot. For terrestrial quadrupedalism this variability is probably a consequence of oblique walking in bonobos (see also D’ Août et al., 2002). In this type of gait, the trunk is held at an angle to the direction of travel. In combination with overstriding, this results in a foot contact pattern where one foot is placed outside the ispilateral hand, and the other foot is placed inside the ipsilateral hand (i.e., between the two hands). The foot that is placed inside the ipsilateral hand is the inside foot and will show a different contact pattern than the outside foot. Moreover, there seems to be an individual preference for using a particular hindlimb as the inside or outside hindlimb. This description is in accordance with the typical walking gait of other great apes (Gorilla gorilla, Pan troglodytes, and Pongo pygmaeus), as previously described by Hildebrand (1967) and Reynolds (1985). For bonobo bipedalism, the intraindividual variability in pressure patterns may be due to the fact that bipedalism is used only occasionally. Footfall patterns observed during the first weeks of bipedal walking of human toddlers also show high variability (A. Hallemans, personal communication). Besides, the interference of instantaneous behavior with locomotion, as well as the differences in walking speed and body dimensions, could also explain part of the observed variability in the terrestrial walking of bonobos. It is necessary to investigate if the large interindividual variability is inherent to the bipedalism of bonobos or if it is only a consequence of the relatively small sample size. In future research it should be attempted to collect a large data set of bipedal sequences, although in practice this is not a trivial undertaking. We observed an alternative type of foot contact during the bipedal and quadrupedal locomotion of several individuals. We call this the toed-in footfall pattern, because the hallux hits the ground first (pointed to the inside) and the foot rolls mediolaterally over its lateral toes. This pattern was also described for common chimpanzees, but was considered an individual anomaly, since it was only observed in 18% of the quadrupedal steps by one animal and almost exclusively for the outside foot (Wunderlich, 1999). The fact that this kind of foot contact was observed by different researchers in bonobos, as well as in chimpanzees, indicates that this is not an anomaly, but an alternative footfall type, which is preferred to the standard pattern in certain situations. Further research could reveal if this pattern is correlated with a particular (inside or outside) hindlimb during oblique walking. Pressure distribution under the metatarsal heads The quadrupedal footfall pattern of bonobos is generally in accordance with previous descriptions (Langdon, 1986; Wunderlich, 1999) of quadrupedal locomotion of the common chimpanzee, and shows some similarities with the human bipedal pattern. Wunderlich (1999) quantified the pressure distribution under the metatarsal heads and found that the pressure under metatarsal head III was significantly higher than under metatarsal heads II and V, and that the highest pressure always occurs under 380 E. VEREECKE ET AL. metatarsal I (significantly higher than under M II, M IV, and M V). However, if we look at the pressure distribution under the metatarsal heads in our sequences, we observe a totally different pattern, in which the highest pressures are measured under the fifth metatarsal head and IV, and the lowest pressures are measured under metatarsals III and II (Fig. 7). We feel this could be ascribed to the varus position of the foot with curved lateral toes. In this position, the lateral border of the foot (M IV and M V) receives most of the pressure, with a minor loading of the medial metatarsal heads (M II and M III). If we look at peak pressures under the digits (metatarsals and phalanges), the hallux receives the highest pressure and the second digit the lowest (P ⬍ 0.5) of all digits (Fig. 7). For the hallux, 74% of the peak pressure is generated by the phalanges, and only 26% by the first metatarsal head. The relatively low pressure that we observed under the head of metatarsal I is thus combined with a higher loading of the distal hallucal phalanx. These findings point to a predominantly lateral pressure distribution under the foot, with a medial shift towards the hallucal phalanges at the end of stance phase. The apparent differences between our pattern and that described by Wunderlich (1999) cannot be ascribed to differences in the substrate, since both studies used a wooden walkway covered with a rubber sheet. However, because Wunderlich (1999) used small pressure mats (16 ⫻ 16 cm), she composed multiple steps to get the pressure distribution under the whole foot. This might have biased the data, since contact of each foot region is assumed for every step, which is not representative under real conditions. This could explain the description of a more plantar foot posture with high pressures under the third metatarsal. General roll-off pattern for bonobos and humans Toe-off generally occurs through the longest digit, i.e., digit II in bonobos and digit I or II in humans, according to the prediction of the “line of leverage” theory (Morton, 1924; Wunderlich, 1999). Morton (1999) defines a humanoid line of leverage for apes and humans that lies between digit I and II, according to the most distally located metatarsal head. Metatarsal II is, indeed, longest in humans and bonobos, but in all hominoids, except humans, the third proximal phalanx is the longest of all phalanges. This results in a configuration in which the third toe is more distally extended than the other toes. However, this is only the case in a position in which the foot sole is placed flatly on the substrate, as in humans. Bonobos and chimpanzees often use an “inverted” foot posture with curved lateral toes and an abducted hallux, so that the hallux reaches further distally than the lateral toes. This could explain why bonobos often roll-off through the hallux and not through the third digit. We can therefore postulate that both in bonobos and in humans, rolloff occurs through the toe that is most distally located in the applied foot posture. In bonobos, this is variable, and toe-off occurs with digits I, II, or III. In humans this variation is smaller, and toe-off occurs with digits I or II. The speed effect Walking speed influences foot-loading patterns, and it is therefore important to take velocity into account in gait analyses (Rosenbaum et al., 1994). However, considering the limitations of working in a zoo environment, it was not possible to make an extensive study of the effect of speed on plantar pressure distributions. To get an impression of the influence of speed, we analyzed the relationship between contact time and peak pressure for each foot region for two individuals. We used contact time as a measure of speed, since we did not dispose of walking speed data for all sequences. The graphs did not show a consistent pattern in which peak pressures increased with decreasing contact time. We think that it is beneficial to look at the speed effect in more depth, and we plan to do so in future research with more suitable data. Are bonobos plantigrade? There have been numerous discussions about whether or not the terrestrial locomotion of the African great apes is plantigrade. According to Morton (1922, 1924), only humans are truly plantigrade, while Keith (1929) believed that all apes are plantigrade. Tuttle (1970) described chimpanzees and gorillas as basically plantigrade. Gebo (1992, 1993) saw plantigradism as a synapomorphy of the African great apes and humans, associated with a terrestrial way of life. Gebo (1997, 1993) assumed that this points to a stage of terrestrial quadrupedalism in the evolution of human bipedalism (contra Prost, 1980). However, Meldrum (1993) claimed that heel contact is common in many primates, and that plantigrady is a primitive condition. It is obvious that we need some clarity on this subject. The main problem is the lack of a clear-cut definition of the term “plantigrady.” Schmitt and Larson (1995) offered a valuable contribution to this topic. Schmitt and Larson (1995) gave a comprehensive overview of the recent debates on heel contact and plantigrady. The patterns of heel contact of 30 primate species were analyzed and classified in three distinct categories, namely: 1) digitigrade; 2) semiplantigrade; and 3) plantigrade. They defined plantigrade, as “a foot position in which there is a complete heel contact with the substrate at some point during support phase of locomotion,” and make a division into “heel-strike” and “mid-foot/heel” plantigrady. If we follow this definition, we should classify the bonobo as “heel-strike plantigrade,” since P. paniscus shows a clear heel-strike at initial ground contact. However, the bonobo foot is placed on the PLANTAR PRESSURE OF BONOBOS substrate in a somewhat different configuration than in humans. Elftman and Manter (1935) demonstrated that the initial foot contact of common chimpanzees (Pan troglodytes), where heel and lateral midfoot touch down simultaneously, is different from the typical human heel-strike, where only the heel touches down (at least in 75% of cases; Kerr et al., 1983; Aerts and De Clercq, 1993; De Clercq et al., 1994). This is also the most striking difference that we observed in this study between the footfall patterns of humans and bonobos. In the beginning of the twentieth century it was observed that apes possess an inverted position of the foot during climbing, whereas humans show an eversion of the foot during bipedalism (Wood-Jones, 1916, in Wunderlich, 1999; p. 10). The inversion that is found in primates during climbing is retained during terrestrial locomotion, and has been called the varus position of the foot. We observed, indeed, that bonobos walk with “inverted” feet. In this position, the lateral toes are curved, letting the weight rest on the dorsal surface of the middle and distal phalanges (instead of on the plantar side of the distal phalanges). Some individuals (Ko and Vi) have also been noticed to place the feet completely flat on the ground with extended toes, in which the distal phalanges touch the ground with their plantar surfaces, similar to the human condition. Within the clear definition of plantigrady given by Schmitt and Larson (1995), we feel that it is confusing to classify the great apes, and thus bonobos, in the same group as humans as being “heel-strike plantigrade,” since there is a clear difference between their foot positions. Plantigrady is a foot position in which the plantar surface of the foot is in contact with the substrate; hence the term, which is not typically the case in the great apes. Due to the inversion of the foot of bonobos, and other great apes, it is mainly the lateral side of the foot which is frequently in contact with the substrate. We should be able to make a distinction between those different foot positions, which is not possible with the current definitions. In fact, the term “plantigrady” only fully describes the human foot position, but regarding the prevailing definitions, it would certainly be confusing to restrict the term “plantigrade” to the human condition. Instead, we suggest dividing the existing term “heel-strike plantigrady” into an inverted type for the foot position of the great apes, and a full-contact type for humans. The “fullcontact” heel-strike plantigrady of the human foot is an apparent specialization to habitual bipedalism, and therefore an apomorphy of the homininae. Heel strike, and not “plantigrady” per se, may be a synapomorphy for the great apes, and is probably related to increased terrestrial habitat use. What is the function of the hallux in terrestrial locomotion of the bonobo? In our study, we did not find significantly greater abduction of the hallux during bipedalism. However, 381 Fig. 6. Hatched, shaded, and dotted bars show mean relative impulses under six foot regions for, respectively, quadrupedal walking of bonobos, bipedal walking of bonobos, and human bipedalism. Vertical lines indicate standard deviations. H heel; V1, medial midfoot; V2, lateral midfoot; M, metatarsal heads (II–V); T, lateral toes (II–V); Hallux, M1 ⫹ T1; Qped, bonobo quadrupedalism; Bped, bonobo bipedalism; Human human bipedalism. this was observed in the field during arboreal bipedal locomotion of bonobos (Susman et al., 1980), and concerned walking over a large branch (⬎20 cm). We used a flat substrate in our setup, which may offer greater stability than a round branch. So it seems that abduction of the hallux is less necessary during terrestrial bipedalism, because other mechanisms, e.g., a more plantar position of the foot, are likely sufficient to keep balance. Nevertheless, some researchers (e.g., Meldrum, 1991; Wunderlich, 1999) have postulated that the hallux has a negligible function in the terrestrial locomotion of primates, because they observed a large variation in degree of abduction of the hallux. We found, indeed, high variation in degree of abduction (Table 4), especially between individuals, but also between the left and the right foot of the same individual (“inner” and “outer” foot). There does not seem to be a correlation between degree of abduction and age or body mass, because a high degree of abduction of the hallux has been observed both in juveniles and in adults. Despite this high variation, the hallux might possess an important sustaining and stabilizing function, since there is an important pressure region under the hallux during stance phase. To get an idea of the propulsive function of the hallux of bonobos compared to humans, we calculated relative impulses from the regional pressure data and, as expected, the relative impulse under the bonobo hallux is smaller than under the human hallux, and is also smaller than under the lateral toes of the bonobo, although none of these differences are statistically significant (Fig. 6). In humans, propulsion at toe-off is thus mainly generated by the hallux, whereas in bonobos, propulsion is primarly generated by the lateral toes. It seems likely that the propulsive function of the hallux is less crucial during bonobo walking than during human (habitual) bipedalism, where the hallux generates high forces at toe-off. 382 E. VEREECKE ET AL. balance during bipedalism. In both gait types, the heel and lateral midfoot typically touch down simultaneously at initial contact, and a midtarsal break is present. The foot position can be categorized as inverted heel-strike plantigrady, and the hallux has an important stabilizing and sustaining function. The observed variability of the collected plantar pressure profiles may be due to the interference of instantaneous behavior with locomotion, and differences in walking speed and body mass. ACKNOWLEDGMENTS Fig. 7. Bar-chart shows relative peak pressure (peak pressure/body weight, N/cm2kg) under digits during quadrupedal walking of bonobos (N ⫽ 61). Shaded bars represent relative peak pressures measured under toes (T). Hatched bars represent relative peak pressures measured under metatarsal heads (M). D1– D5, digits I–V (and D ⫽ M ⫹ T). Which joint causes the midtarsal break during terrestrial locomotion? A midtarsal break occurs as a consequence of a flexible midfoot. Due to this considerable flexibility, the heel can be lifted before the midfoot leaves the ground. This is only occasionally seen in humans (e.g., in basketball players; M. Lafortune, Nike Inc., personal communication), but has repeatedly been described for primates (Elftman and Manter, 1935; Aiello and Dean, 1996; Wunderlich, 1999, D’ Août el al., 2002). In our study, we observed a distinct pressure region under the lateral midfoot on the plantar pressure profiles of bonobo feet, which remains present after heel-off. The bonobo foot thus clearly possesses a midtarsal break. Nevertheless, it is still unclear which tarsal joint causes this midtarsal break. Classically, the calcaneo-cuboid joint is assumed to be responsible for this apparent flexibility of the midfoot (Elftman and Manter, 1935; Susman, 1983). However, personal observations of the foot skeleton of an adult male bonobo, together with the interpretation of plantar pressure distributions of bonobos, point in the direction of the cuboid-metatarsal V joint (see also D’ Août et al., in press). In the latter, the range of motion appears to be markedly larger than in the calcaneo-cuboid joint. Further morphological research on ape feet should bring more clarity. CONCLUSIONS Analysis of plantar pressure distributions, collected during terrestrial locomotion of the bonobo, points to some differences between bipedal and quadrupedal walking. Quadrupedalism has a curved course of the center of pressure, caused by a medial weight transfer during mid-stance. Bipedal walking has a more irregular course of the center of pressure and is characterized by a significantly smaller contact time, according to a smaller step length at higher frequency. Additionally, the feet are more plantar-positioned to maintain We thank the Royal Zoological Society of Antwerp and the Planckendael staff for allowing us to work with the bonobos, and in particular the bonobo keepers for their cooperation. Dr. Clark S. Larsen and two anonymous reviewers provided constructive comments on an earlier version of the manuscript. This research was supported by FWO-Flanders (project G.0209.99, to P.A., D.D.C., and L.V.E.) and by the University of Antwerp (Dehousse mandate to E.V.). We also thank the Flemish Government for structural support throught the Centre for Research and Conservation (Royal Zoological Society of Antwerp). LITERATURE CITED Aerts P, Declerq D. 1993. Deformation characteristics of the heel region of the shod foot during a simulated heel strike: the effect of varying midsole hardness. J Sport Sci 11:449 – 461. Aerts P, Van Damme R, Van Elsacker L, Duchêne V. 2000. Spatio-temporal gait characteristics of the hind-limb cycles during voluntary bipedal and quadrupedal walking in bonobos (Pan paniscus). Am J Phys Anthropol 111:503–517. Aiello L, Dean C. 1996. An introduction to human evolutionary anatomy. London: Academic Press. Bauer HR. 1977. Chimpanzee bipedal locomotion in the Gombe National Park, East Africa. Primates 18:913–921. Benton MJ. 1997. Vertebrate palaeontology, 2nd ed. London: Chapman and Hall. Carlet G. 1872. Sur la locomotion humaine. Ann Sci Nat Ser 5:1–92. Chen F-C, Li W-H. 2001. Genomic divergences between humans and other hominoids and the effective population size of the common ancestor of humans and chimpanzees. Am J Hum Genet 68:444 – 456. Coolidge HJ. 1933. Pan paniscus: pygmy chimpanzee from south of the Congo River. Am J Phys Anthropol 18:1–57. D’Août K, Aerts P, De Clercq D, Schoonaert K, Vereecke E, Van Elsacker L. 2001. Studying bonobo (Pan paniscus) locomotion using an integrated setup in a zoo environment: preliminary results. Primatology 4:191–206. D’Août K, Aerts P, De Clercq D, De Meester K, Van Elsacker L. In press. Segment and joint angles of the hindlimb during bipedal and quadrupedal walking of the bonobo (Pan paniscus). Am J Phys Anthropol 119:37–51. De Clercq D, Aerts P, Kunnen M. 1994. The mechanical characteristics of the human heel pad during foot strike in running: an in vivo cineradiographic study. J Biomech 27:10:1213–1222. Doran DM. 1989. Chimpanzee and pygmy chimpanzee positional behavior: the influence of environment, body size, morphology, and ontogeny on locomotion and posture. Ph.D. thesis, State University of New York, Stony Brook. Elftman H. 1944. The bipedal walking of the chimpanzee. Mammalogy 25:67–71. Elftman H, Manter J. 1935. Chimpanzee and human feet in bipedal walking. Am J Phys Anthropol 20:69 –79. Fleagle JG. 1979. Primate positional behavior and anatomy: naturalistic and experimental approaches. In: Morbeck ME, Preuschoft H, Gomberg N, editors. Environment, behavior and PLANTAR PRESSURE OF BONOBOS morphology: dynamic interactions in primates. New York: Gustav Fischer. p 313–325. Fleagle JG. 1999. Primate adaptation and evolution. New York: Academic Press. Fleagle JG, Stern JT, Jungers WL, Susman RL, Vangor AK, Wells JP. 1981. Climbing: a biomechanical link with brachiation and with bipedalism. Symp Zool Soc Lond 48:359 –375. Gebo DL. 1992. Plantigrady and foot adaptation in African apes: implications for hominid origins. Am J Phys Anthropol 89:29–58. Gebo DL. 1993. A reply to Dr. Meldrum. Am J Phys Anthropol 91:382–385. Hildebrand M. 1967. Symmetrical gaits of primates. Am J Phys Anthropol 26:119 –130. Inman VT, Ralston HJ, Todd F. 1981. Human walking, Baltimore: Williams & Wilkins. Ishida H, Kumakura H, Kondo S. 1985. Primate bipedalism and quadrupedalism: comparative electromyography. In: Kondo S, Ishida H, Kimura T, Okada M, Yamazaki N, Prost JH, editors. Primate morphophysiology, locomotor analysis and human bipedalism. Tokyo: University of Tokyo Press. p 59 –79. Jablonski NG, Chaplin G. 1993. Origin of habitual terrestrial bipedalism in the ancestor of the Hominidae. J Hum Evol 24:259 –280. Jenkins FA. 1972. Chimpanzee bipedalism: cineradiographic analysis and implications for the evolution of gait. Science 178:877– 879. Kano T. 1992. The last ape: pygmy chimpanzee behavior and ecology. Stanford, CA: Stanford University Press. p 123–125. Keith A. 1929. The history of the human foot and its bearing on orthopaedic practice. J Bone Joint Surg 11:10 –32. Kerr BA, Beauchamp L, Fisher V, Neil R. 1983. Footstrike patterns in distance running. In: Nigg B, Kerr BA, editors. Biomechanical aspects of sport shoes and playing surfaces. Calgary: University Press. p 135–143. Kimura T. 1985. Bipedal and quadrupedal walking of primates: comparative dynamics. In: Kondo S, Ishida H, Kimura T, Okada M, Yamazaki N, Prost JH, editors. Primate morphophysiology, locomotor analysis and human bipedalism. Tokyo: University of Tokyo Press. p 81–104. Kimura T. 1990. Voluntary bipedal walking of infant chimpanzees. In: Jouffroy FK, Stack MH, Niemitz C, editors. Gravity, posture and locomotion in primates. Florence: II Sedicesimo. p 237–251. Kimura T. 1996. Centre of gravity of the body during the ontogeny of chimpanzee bipedal walking. Folia Primatol (Basel) 66: 126 –136. Kimura T, Okada M, Ishida H. 1977. Dynamics of primate bipedal walking as viewed from the force of foot. Primates 18:137–147. Kimura T, Okada M, Yamazaki N, Ishida H. 1983. Speed of the bipedal gaits of man and nonhuman primates. Ann Sci Nat Zool Paris 5:145–158. Langdon JH. 1986. Functional morphology of the Miocene hominoid foot. New York: Karger. Li Y, Crompton RH, Alexander RMN, Günther MM, Wang WJ. 1996. Characteristics of ground reaction forces in normal and chimpanzee-like bipedal walking by humans. Folia Primatol (Basel) 66:137–159. Marey M. 1873. De la locomotion terrestre chez les bipedes et quadrupedes. J Anat Physiol 9:42. McHenry HM. 1984. The common ancestor. A study of the postcranium of Pan paniscus, Australopithecus and other hominoids. In: Susman RL, editor. The pygmy chimpanzee. Evolutionary biology and behavior. New York: Plenum Press. p 201–224. McHenry HM, Corruccini RS. 1981. Pan paniscus and human evolution. Am J Phys Anthropol 54:355–367. Meldrum DJ. 1991. Kinematics of the Cercopithecine foot on arboreal and terrestrial substrates with implications for the interpretation of hominid terrestrial adaptations. Am J Phys Anthropol 84:273–290. Meldrum DJ. 1993. On plantigrady and quadrupedalism. Am J Phys Anthropol 91:379 –385. Morton DJ. 1922. Evolution of the human foot I. Am J Phys Anthropol 5:305–336. 383 Morton DJ. 1924. Evolution of the human foot II. Am J Phys Anthropol 7:1–52. Okada M. 1985. Primate bipedal walking: coparative kinematics. In: Kondo S, Ishida H, Kimura T, Okada M, Yamazaki N, Prost JH, editors. Primate morphophysiology, locomotor analysis and human bipedalism. Tokyo: University of Tokyo Press. p 47–58. Perry J. 1992. Gait analysis: normal and pathological function. Thorofare, NJ: Slack. Prost JH. 1980. Origin of bipedalism. Am J Phys Anthropol 52: 175–189. Reynolds TR. 1985. Stresses on the limbs of quadrupedals primates. Am J Phys Anthropol 67:351–362. Rose MD. 1991. The process of bipedalization in hominids. In: Coppens Y, Senut B, editors. Origine(s) de la bipédie chez les hominidés (Cahiers de Paléanthropologie). Paris: Editions du CNRS. p 37– 48. Rosenbaum D, Hautman S, Gold M, Claes L. 1994. Effects of walking speed on plantar pressure patterns and hindfoot angular motion. Gait Posture 2:191–197. Schmitt D, Larson SG. 1995. Heel contact as a function of substrate type and speed in primates. Am J Phys Anthropol 96:39–50. Senut B. 1992. New ideas on the origins of hominid locomotion. In: Nishida T, McGrew WC, Marker P, Pickford M, de Waal FBM, editors. Topics in primatology. Volume I: human origins. Tokyo: University of Tokyo Press. p 393– 407. Susman RL. 1983. Evolution of the human foot: evidence from Plio-Pleistocene hominids. Foot Ankle 3:365–376. Susman RL. 1984. The locomotor behavior of Pan paniscus in the Lomako forest. In: Susman RL, editor. The pygmy chimpanzee. Evolutionary biology and behavior. New York: Plenum. p 369 – 393. Susman RL, Badrian NL, Badrian AJ. 1980. Locomotor behavior of Pan paniscus in Zaire. Am J Phys Anthropol 53:69 – 80. Susman RL, Stern JT Jr. 1991. Locomotor behavior of early hominids: epistemology and fossil evidence. In: Coppens Y, Senut B, editors. Origine(s) de la bipédie chez les hominidés (Cahiers de Paléanthropologie). Paris: Editions du CNRS. p 121–131. Tuttle RH. 1970. Postural, propulsive and prehensile capabilities in the cheiridia of chimpanzees and other great apes. Chimpanzee 2:167–253. Van Elsacker L, Claes G, Melens W, Struyf K, Vervaecke H, Walraven V. 1993. New outdoor exhibit for a bonobo group at Planckendael: design and introduction procedures. In: Daman FJ, editor. Bonobo tidings, jubilee volume on the occasion of the 150th anniversary of the Royal Zoological Society of Antwerp. Antwerp: Royal Zoological Society of Antwerp. p 35– 47. Whittle MW. 1996. Basic sciences. Gait analysis, an introduction. 2nd ed. Oxford: Butterworth-Heinemann. Wood BA. 1992. Evolution of australopithecines. In: Jones S, Martin R, Pilbeam D, editors. The Cambridge encyclopedia of human evolution. Cambridge: Cambridge University Press. p 231–240. Wunderlich RE. 1999. Pedal form and plantar pressure distribution in anthropoid primates. Ph.D. thesis. Ann Arbor, MI: Bell & Howell (UMI Dissertation Services). Wunderlich RE, Ford KR. 2000. Plantar pressure distribution during bipedal and quadrupedal walking in the chimpanzee (Pan troglodytes). Proceedings of EMED Scientific Meeting, 2– 6 August 2000. p 19. Zihlman AL. 1984. Body build and tissue composition in Pan paniscus and Pan troglodytes, with comparison to other hominoids. In: Susman RL, editor. The pygmy chimpanzee. Evolutionary biology and behavior. New York: Plenum Press. p 179–200. Zihlman AL. 1992. The emergence of human locomotion: the evolutionary background and environmental context. In: Nishida T, McGrew WC, Marker P, Pickford M, de Waal FBM, editors. Topics in primatology. Volume 1: human origins. Tokyo: University of Tokyo Press. p 409 – 442. Zihlman AL, Cramer DL. 1978. Skeletal differences between pygmy (Pan paniscus) and common chimpanzees (Pan troglodytes). Folia Primatol (BaseI) 29:86 –94. Zihlman AL, Cronin JE, Cramer DL, Sarich VM. 1978. Pygmy chimpanzee as a possible prototype for the common ancestor of humans, chimpanzees and gorillas. Nature 275:744 –746.