Abstract. Introduction REVIEW. K. D Août, 1,2 E. Vereecke, 1,2 K. Schoonaert, 1,2 D. De Clercq, 3 L. Van Elsacker 2 and P. Aerts 1

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1 J. Anat. (2004) 204, pp Blackwell Publishing, Ltd. REVIEW Locomotion in bonobos (Pan paniscus): differences and similarities between bipedal and quadrupedal terrestrial walking, and a comparison with other locomotor modes K. D Août, 1,2 E. Vereecke, 1,2 K. Schoonaert, 1,2 D. De Clercq, 3 L. Van Elsacker 2 and P. Aerts 1 1 Department of Biology, University of Antwerp, Belgium 2 Centre for Research and Conservation, Royal Zoological Society of Antwerp, Belgium 3 Movement and Sport Sciences, Ghent University, Belgium Abstract One of the great ongoing debates in palaeo-anthropology is when, and how, hominids acquired habitual bipedal locomotion. The newly adopted bipedal gait and the ancestral quadrupedal gait are most often considered as very distinct, with each habitual locomotor mode showing corresponding anatomical adaptations. Bonobos (Pan paniscus), along with common chimpanzees (P. troglodytes), are the closest living relatives to humans and their locomotion is valuable for comparison with other primates, and to gain an insight in the acquisition of human bipedalism. Bonobos are habitual quadrupeds, but they also engage in bipedal locomotion, both on terrestrial and in arboreal substrates. In terms of kinematics and dynamics, the contrast between bipedal and quadrupedal walking seems to be more subtle than one might expect. Apart from the trunk being approximately 37 more erect during bipedal locomotion, the leg movements are rather similar. Apart from the heel, plantar pressure distributions show subtle differences between bipedal and quadrupedal locomotion. Regardless, variability is high, and various intermediate forms of locomotion (e.g. tripedal walking) exist both in captivity and in the wild. Moreover, there is overlap between the characteristics of walking and other locomotor modes, as we show with new data of walking on an inclined pole and of vertical squat jumps. We suggest that there is great overlap between the many locomotor modes in bonobos, and that the required polyvalence is reflected in their anatomy. This may hamper the development of one highly specialized gait (i.e. bipedalism), which would constrain performance of the other types of locomotion. Key words bipedalism; bonobos; kinematics; kinetics; pan paniscus; primate locomotion; quadrupedalism. Introduction The acquisition of habitual bipedalism is considered as the most prominent milestone in hominid evolution, and it is used as a hominid identifying mark (see, e.g. Boyd & Silk, 2000). However, it is not trivial to determine the locomotor mode of (pre)hominids because of the lack of (mostly postcranial) remains and, even if they are present, the interpretation of anatomical features. Correspondence Dr Kristiaan D Août, Department of Biology, University of Antwerp, Campus Drie Eiken, Universiteitsplein 1, B-2610 Antwerpen, Belgium. T: +32 (0) ; F: +32 (0) ; E: kristiaan.daout@ua.ac.be Accepted for publication 9 March 2004 Very little direct evidence for the gait of extinct hominids is available (exceptions include the Laetoli footprints; Leakey & Hay, 1979) and therefore analogy with extant species proves essential. Modern humans differ drastically from the early hominids that may have acquired habitual bipedalism (see, e.g. Zihlman, 1984) and therefore the great apes, closest related to hominids (Benton, 1997), and for which both anatomy and gait can be studied, may provide crucial information. All great apes (and some other primates) have been proposed as models for early hominids, often for different reasons. From a phylogenetic point of view, chimpanzees (Pan troglodytes) and bonobos (P. paniscus) are the most obvious species because they are related most closely to humans, and recently it has even been proposed

2 354 Bipedal and quadrupedal terrestrial walking, K. D Août et al. that they should be placed within the genus Homo (Wildman et al. 2003). Of these two species, based on postcranial anatomy and evolutionary history, bonobos are considered to provide the best model, although chimpanzees might be alternative candidates as well (Corruccini & McHenry, 1979). By contrast, orang-utans (Pongo pygmaeus), more distantly related to the hominids (Benton, 1997), show interesting features in their locomotion repertoire that may also have been part of the prehominid s repertoire as well and may therefore also be particularly fruitful study subjects (Crompton et al. 2003). Gorillas (Gorilla gorilla) engage in bipedal postures (for display rather than locomotion) more than other apes and may therefore show more adaptations towards bipedalism and, consequently, be relevant study species. It is clear that no living species is a perfect model or stand-in for the hominid that first acquired habitual bipedalism (assuming that this species could be known). Therefore, a comparative approach studying as many relevant species as possible should be used to shed light on the likelihood of existing hypotheses bearing on the acquisition of habitual bipedalism in hominids, and reveal general principles of hominoid locomotion that are likely to have existed in early hominids as well (see Schmitt, 2003, for an overview). This paper presents a non-exhaustive review of the experimental data known to date on bonobo locomotion, focusing primarily on bipedal walking. Based on the available data (taken from the literature and from unpublished results), we evaluate how bipedal locomotion fits in with the bonobo s overall locomotor repertoire, compare to what extent kinesiological parameters differ between bipedal walking and other locomotor modes, and discuss some implications towards studies of bipedal locomotion in apes and hominids. Bipedal vs. quadrupedal terrestrial walking Spatiotemporal gait characteristics When bonobos walk quadupedally, they typically use a diagonal-sequence walking gait, like other primates, but unlike most quadrupeds, who typically use a lateralsequence walk (Hildebrand, 1967; see Larson, 1998, for details). At high velocities, bonobos will gallop; we have never observed a trot, which may be an unfavourable gait because such a high-stiffness, high-frequency gait would lead to excessively high peak stresses on the limbs (Schmitt, 1995 in Larson, 1998; Schmitt, 1999) or would not allow for an efficient recovery stroke in animals with distally heavy limbs (and resulting high moments of inertia about the hip) (Preuschoft & Günther, 1994; Preuschoft et al. 1996). Quantitative data on galloping bonobos are lacking in the literature. Aerts et al. (2000) compared spatiotemporal gait characteristics between bipedally and quadrupedally walking bonobos (Fig. 1). The duty factor (the fraction of the time for which each foot is on the ground) is similar in both gaits, but the relationship between walking velocity and stride frequency (and hence stride length and step length) differs. In any gait, bonobos increase velocity by increasing both the stride length and the stride frequency, but the slope of these paramaters differs, both when absolute values are used or when the data are made dimensionless using the principle of dynamic similarity (see Alexander, 2004). For a given velocity, bonobos walking bipedally will use shorter steps and strides but a higher stride frequency than when walking quadrupedally. Segment and joint angles Bonobos typically display a bent-hip, bent-knee posture during bipedal locomotion but also during quadrupedal Fig. 1 Gait parameters during bipedal and quadrupedal walking in bonobos (after Aerts et al. 2000). Dimensionless values are presented (see Aerts et al. 2000, for details), with a stride being a full gait cycle. For clarity, only the regression lines through the actual data points are shown.

3 Bipedal and quadrupedal terrestrial walking, K. D Août et al. 355 Fig. 2 Joint angles during bipedal and quadrupedal walking in bonobos (after D Août et al. 2002). The angles are defined as the enclosed angle in the sagittal plane between the segments that form the considered joint (i.e. full flexion = 0, full extension = 180 ). The foot is modelled as one segment from the posteroventral edge of the heel bone to the distalmost toe. Fig. 3 Example vertical ground-reaction force profiles from a bonobo walking bipedally (A), a bonobo walking quadrupedally (B), a bonobo walking over a 30 inclined pole (C) (K. Schoonaert et al., unpublished data) and a human (D, after Farley & Ferris, 1998). For comparison, all forces are scaled to 100% peak force. locomotion. D Août et al. (2002) quantified the hip, knee and ankle angle throughout the stride for both gait types. Time plots of these joint angles have similar shapes (Fig. 2). During the greater part of stance phase, the hip extends, but it may already begin to flex at the end of stance phase, when the heel is lifted but the forefoot remains in contact with the ground. The knee flexes considerably throughout stance, most importantly at initial contact and shortly before swing phase. The foot is placed quite flat on to the substrate in bonobos (see below), and thus the ankle first flexes and then extends during stance, but the latter not as fast as during the human push-off. In general, remarkably few significant differences were found between the angle values of bipedal and quadrupedal walking at selected phases of the stride. On average, the trunk is held 37 more erect during bipedal walking than during quadrupedal walking. Consequently, the hip angle is larger (i.e. more extended) throughout the stride (Fig. 2). Selected angle values of the thigh, shank and foot, and the resulting knee and ankle angles, do not differ significantly between bipedal and quadrupedal walking (D Août et al. 2002). Kinetics Figure 3 shows sample vertical ground reaction forces of bonobos (Schoonaert et al. 2003). Although variability appears to be higher than in human walking, it is consistently single-humped. A double-humped profile, as seen for human walking (but not running), is not observed, but a sharp peak corresponding with heel impact is frequently observed. From this, we conclude that bonobos do not use an inverted pendulum -type gait, as further confirmed by the very low vertical oscillations of the body s centre of mass during both bipedal and quadrupedal walking (D Août et al. 2001; Schoonaert et al. 2003). Pedobarography Vereecke et al. (2003) compared plantar pressures for bipedally and quadrupedally walking bonobos (Fig. 4).

4 356 Bipedal and quadrupedal terrestrial walking, K. D Août et al. the substrate first) back to the heel region and then forwards. Quantitative analyses of selected zones under the foot indicate a clear difference in peak pressures under the heel, which is much higher in quadrupedal than in bipedal walking. However, relative impulses of all selected zones under the foot (including the heel) are not significantly different between both gait types, and load is carried by the whole foot throughout almost the whole stance phase. Gait asymmetry Fig. 4 Time course of plantar pressure under selected zones of the bonobo foot while walking bipedally and quadrupedally (data from Vereecke et al. 2003). All profiles are normalized to 100% contact time. The general foot roll-off pattern, shown by the path and time course of the centre of pressure (COP) under the feet, is very variable during both bipedal and quadrupedal bouts. In most cases, initial contact is made almost simultaneously by the heel and the lateral midfoot. The COP then travels forward, typically following a curved course along the lateral rays and moving medially at the end of stance. Alternative patterns may vary from an almost straight COP course from the heel to the second digit, to a V-curved course in which the COP travels from the hallux (which may occasionally hit It has already been established that quadrupedally walking primates often overstride, placing their feet in front of the ipsilateral hand (for an overview, see Larson, 1998). This allows them to use long strides and correspondingly low stride frequencies for a given velocity, which in turn may reduce internal work (Raichlen, 2003). Furthermore, and unlike most other mammals, primates typically use a diagonal sequence/diagonal couplets quadrupedal walk, in which diagonal limbs move as a pair (Hildebrand, 1967). Both of these features are typically (but not always) found in bonobo quadrupedal sequences. As in other primates, an overstriding foot may be placed medially of the ipsilateral hand ( inside foot ) or laterally of the ipsilateral hand ( outside foot ), and this possibly has an important effect as to the spatial (a)symmetry of the gait. We have analysed quadrupedal walks of bonobos, focusing on left right differences of the walk. Preliminary data (D Août et al. 2003) strongly suggest that individuals use both ( inside and outside ) foot placements, but that they have an individual preference for one type. Furthermore, an inside foot, being placed more medially and thus closer to the vertical projection of the body s centre of mass, can be expected to carry more load than an outside foot. Our tentative data for six quadrupedal sequences (of one adult female and two adult males) confirm this and, moreover, show higher vertical ground reaction peak forces for the inside foot. Plantar pressure recordings suggest a flatter placement of inside feet than outside feet, with a more laterally travelling centre of pressure and a more abducted hallux. The way in which the foot is placed during quadrupedal walking also influences the orientation of the body with respect to the overall direction of progression: the body will be positioned obliquely, e.g. when the left foot is inside, the longitudinal body axis will be shifted (the animal will look ) to the right.

5 Bipedal and quadrupedal terrestrial walking, K. D Août et al. 357 We found that the oblique positioning of the trunk is not only typical for quadrupedal walking, but also for bipedal walking and that here, too, some kinesiological left/right differences are found in our bipedal sequences. For instance, when the body is rotated to the left with respect to the walking direction, the right foot will be leading and the left foot may strike not much anteriorly of the right foot, staying closely under the body s centre of mass. In this respect, the leading foot may be functionally comparable with an outside foot during quadrupedal walk, and the trailing foot to the inside foot, carrying more load. Although our preliminary data clearly suggest that left/right differences in foot function are systematic and that they are similar for bipedal and quadrupedal bouts, more quantitative data are clearly required. They are not trivial to collect because, as variability in bonobo gait is high, study sequences should ideally consist of at least two consecutive strides of a single walking sequence, each with documented groundreaction forces and plantar pressure data. Terrestrial walking vs. other locomotor modes Terrestrial locomotion Although research on terrestrially walking bonobos (and other apes) has typically contrasted bipedal with quadrupedal locomotion, and indeed found differences (see above), it should be stressed that the discrete subdivision between both gait types may only reflect extremes in a continuous range of terrestrial walking styles, in which different walking styles fade into each other. Figure 5 illustrates this point by showing some locomotor postures during untrained walking of bonobos. Typical quadrupedal and bipedal postures are shown in panels 1 and 5, respectively. Panels 2 4 illustrate alternative locomotor modes. In a range from typical knuckle walking to bipedal walking, we may observe tripedal walking (panel 2), very crouched bipedal walking with an occasional hand ground contact (panel 3) and crouched bipedal walking (panel 4). Intermediate locomotor modes are observed less frequently than the typical extremes, but are not anomalous. For example, Susman (1984) and Kano (1992) describe tripedal locomotion in wild bonobos, and it has also been observed in chimpanzees (Kelly, 2001). This overview is not exhaustive, but illustrates that the clear-cut subdivision between bipedal and quadrupedal walking in apes may be somewhat artificial. Although quantitative data are lacking for the intermediate gaits, we presume gait parameters may change in a continuous fashion. Observations on bipedal walking and terrestrial locomotion in the wild and in captivity Bipedal walking and other terrestrial locomotion types in wild bonobos have been described in three sites in the Democratic Republic of Congo. The observations suggest that the locomotor types, as found in captivity, reflect natural behaviour. In Wamba, a wet and densely forested site but with sugarcane fields to facilitate observations, apart from arboreal locomotion such as brachiation and climbing, the habituated bonobos engage in several forms of terrestrial locomotion: either quadrupedalism (knuckle walking), bipedalism (sometimes over a distance of 20 m or more), as well as tripedal walking (Kano, 1992). In Lomako, which is also wet and densely forested, terrestrial locomotion also included bipedal walking (Susman et al. 1980) and tripedal walking (Susman, 1984; Doran, 1993). Recent observations from Lukuru, a dry forest/ savanna mosaic habitat, report frequent bipedal walking through Fig. 5 Example body postures during terrestrial walking. Note that there is a continuum from left to right, with A being a typical quadrupedal knuckle-walking posture and E a typical bipedal bent-hip, bent-knee posture. B illustrates tripedal walking.

6 358 Bipedal and quadrupedal terrestrial walking, K. D Août et al. Fig. 6 Hip angle during during terrestrial bipedal and guadrupedal walking, climbing on a 30 inclined pole, vertical climbing (after Isler, 2003) and vertical jumping (M. Scholz et al., unpublished data). Definition of angles as in Fig. 2. The jumping curve is an average of five high sequences of one individual, and the plot goes from maximal flexion (corresponding well with the start of jumping) to toe-off. Fig. 7 Knee angle during during terrestrial bipedal and guadrupedal walking, climbing on a 30 inclined pole, vertical climbing (after Isler, 2003) and vertical jumping (M. Scholz et al., unpublished data). Definition of angles as in Fig. 2. The jumping curve is an average of five high sequences of one individual, and the plot goes from maximal flexion (corresponding well with the start of jumping) to toe-off. open short-grass plains, along roadsides and in shallow pools (Thompson, 2002). In the wild, unaided, bipedal walking bouts represent as low as 0.3% of terrestrial travel (Doran, 1993), but bipedalism apparently decreased when habituation increased (Susman, 1984; Doran, 1993), so it may be more frequent than direct observations in the wild suggest. Observations of captive bonobo populations vary widely. Unsupported bipedal locomotion may occupy less than 0.01% of the total time budget (calculated from Dielentheis et al. 1996). In our work on the population of the Wild Animal Park of Planckendael (Belgium), high frequencies of bipedal walking (as a percentage of bipedal plus quadrupedal locomotion bouts) were found, ranging from 3.9% for spontaneous bouts to 18.9% when abundant food is supplied (Duchêne, 1997; see also Videan & McGrew, 2001, 2002). during bipedal walking than during climbing. Isler (2002) describes that bonobo climbing is more versatile than, for instance, gorilla climbing. Vertical jumping Jumping is a specific type of locomotion in which bonobos frequently engage both in arboreal and in terrestrial settings (our personal observations). During vertical jumping, bonobos will start from a deeply crouched resting position in which the hip is considerably more flexed (i.e. to a joint angle of approximately 20 ) than during any other gait type studied. At the end of the push-off phase, the hip is even slightly more extended than in bipedal walking (Fig. 6). A similar pattern holds true for the knee and thus, for both joints, the range of motion of vertical jumping encompasses completely that of all other locomotor types studied. Arboreal locomotion Isler (2002, 2003) examined the kinematics of vertical climbing along a rope in bonobos, and Schoonaert et al. (2003) studied climbing on an instrumented pole with a slope of 30. Joint angle curves, compared with terrestrial locomotion, are shown in Figs 6 and 7. In general, climbing on a 30 inclined pole shows more resemblance to quadrupedal terrestrial locomotion than to bipedal locomotion (Lauwers, 2003). This appears not to hold true for vertical climbing (Isler, 2002). Thus far, all studies indicate that hip extension is larger Locomotion and anatomy It has been long established that the overall morphology of P. paniscus is generalized, more so than for the common chimpanzee (Coolidge, 1933). Data on limb length and weight distribution and tissue composition (Zihlman, 1984) confirm this, and suggest that from a morphological point of view, P. paniscus most closely resembles the common Pan hominid ancestor. More detailed anatomy and morphometry of the locomotor apparatus has been carried out recently (Payne & Crompton, 2001; Payne, 2001), and helps

7 Bipedal and quadrupedal terrestrial walking, K. D Août et al. 359 explain anatomical adaptations towards locomotion. Compared with the habitually bipedal modern humans, bonobo anatomy was found to be more generalistic and indicative of an arboreal lifestyle. The relatively small moment arms about the hindlimb joints, along with relatively long fascicles, show that mobility is favoured at the expense of tension production. Among African apes, the bonobo resembles modern humans better in this respect (Payne, 2001), but less so than the highly arboreal orang-utan (Pongo pygmaeus), so this characteristic is not necessarily an adaptation for bipedalism per se. Discussion and conclusions Bipedal locomotion in bonobos is highly variable and in many kinesiological characteristics significant differences from quadrupedal walking and from other locomotor modes are found. Should this lead to the conclusion that bonobo bipedal locomotion is an exceptional gait type with unique features? In fact, two major arguments challenge this statement, as outlined below. First, the differences between gait characteristics of bipedal locomotion and other gaits are often more subtle than one might expect (and drastically different from walking in modern humans). For example, the angular displacements of leg joint and segments are remarkably similar and the differences that are found (most importantly, the greater hip extension) can be attributed to the more erect position of the trunk during typical bipedal locomotion (D Août et al. 2002). However, even greater hip extension is found during jumping. Pedobarographic records show overlap between bipedal and quadrupedal walking, and the only striking difference is the higher impact of the heel during quadrupedal locomotion. Other differences, if present, are quite subtle and, in general, foot roll-off during both gait types follows similar (albeit variable) patterns (see Vereecke et al. 2003). Secondly, and importantly, although bipedalism is easily defined as a locomotor mode in which only the hindlimbs interact with the substrate, this may be an oversimplification. Ou personal observations under seminatural circumstances (see Fig. 5) demonstrate that bipedal sequences cover a range from typical bipedal bouts to very crouched bouts. Although quantitative data on such sequences are lacking, it is likely that their characteristics would be different and may be closer to (or overlapping with) other locomotor modes. As such, different locomotor modes blend into each other to form a continuum. Interestingly, various forms of terrestrial locomotion, including tripedal locomotion as an intermediate form between bipedal and quadrupedal locomotion, are observed quite regularly in captivity but also in the wild. The variability both within and between gait types in bonobos correpsonds well with anatomical findings. Apes in general, and bonobos in particular, show anatomical features that favour manoeuvrability and versatility (see above). Clearly, more data are required. Specifically, we need (1) a more profound insight into ape locomotion including as much non-invasive methods as possible (e.g. inverse dynamics), (2) quantitative data of more locomotor modes (e.g. climbing at different angles and brachiation) in a wide range of hominoid species and (3) a better knowledge of locomotor behaviour and kinesiology in the wild. So, although our understanding of bonobo or ape locomotion is far from complete, what can the available data reviewed here tell us regarding bipedalism in this species and more generally about apes and possibly hominids? Because of the variability of bipedalism, its overlap with other locomotor modes and the associated polyvalent anatomy, we suggest that the ability for terrestrial bipedalism may be a mere free bonus locomotor mode and, in other words, unspecialized, bonobo- or ape-like terrestrial bipedalism may not be that difficult to accomplish. In this respect, recent data confirm statements made by Zihlman (1984): Given the morphology and behavioral abilities of pygmy chimpanzees, it is no longer necessary to hypothesize an unusual gait in order to characterize the locomotor pattern of early hominids, and that: The possible existence of an ape ancestor like P. paniscus suggests no great morphological leap from the quadrupedal ape ancestor to hominids, and perhaps less of a behavioral leap than previously thought, as well as Isler s view that: In a hypothetical light-weighted ancestral hominoid, a corresponding flexibility could have opened ways to new locomotor behaviours such as frequent or habitual bipedalism (Isler, 2003). Terrestrial bipedalism in bonobos (or bent-hip, bentknee locomotion in general) is clearly not as specialized and efficient as in modern humans (see, e.g. Crompton

8 360 Bipedal and quadrupedal terrestrial walking, K. D Août et al. et al. 1998). It is likely that such specialization would constrain other, more frequently used, locomotor modes, such as the various arboreal locomotor styles. Although frequencies of natural bipedal locomotion are low, injured bonobos are capable of sustained bipedal locomotion (Van Lawick-Goodall, 1968; Bauer, 1977, in Zihlman, 1984) and it was recently found in a wild population of common chimpanzees that they also may engage in bipedalism very frequently under certain ecological conditions (Stanford, 2002). Generalizing the bonobo findings to palaeo-anthropological interpretations, we suggest that care should be taken when assessing locomotor abilities realting to fossil findings: even if clear adaptations for bipedalism are absent, bipedalism may have been a significant (but probably not habitual) part of their locomotion repertoire. 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