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Bipedal versus Quadrupedal Hind Limb and Foot Kinematics in a Captive Sample of Papio anubis: Setup and Preliminary Results

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Bipedal versus Quadrupedal Hind Limb and Foot Kinematics in a Captive Sample of Papio anubis: Setup and Preliminary Results
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  Bipedal versus Quadrupedal Hind Limband Foot Kinematics in a Captive Sampleof   Papio anubis:  Setup and Preliminary Results Gilles Berillon  &  Guillaume Daver  & Kristiaan D ’ Août  &  Guillaume Nicolas  & Bénédicte de la Villetanet  &  Franck Multon  & Georges Digrandi  &  Guy Dubreuil Received: 20 February 2009 /Accepted: 16 October 2009 / Published online: 1 April 2010 # Springer Science+Business Media, LLC 2010 Abstract  Setups that integrate both kinematics and morpho-functional investigationsof a single sample constitute recent developments in the study of nonhuman primate bipedalisms. We introduce the integrated setup built at the Primatology Station of theFrench National Centre for Scientific Research (CNRS), which allows analysis of both bipedalandquadrupedallocomotioninapopulationof55  –  60captiveolive baboons.Asa first comparison, we present the hind limb kinematics of both locomotor modalities in10 individuals, focusing on the stance phase. The main results are: 1) differences in bipedal and quadrupedal kinematics at the hip, knee, and foot levels; 2) a variety of foot contacts to the ground, mainly of semiplantigrade type, but also of plantigrade type; 3)equal variations between bipedal and quadrupedal foot angles; 4) the kinematics of the Int J Primatol (2010) 31:159  –  180DOI 10.1007/s10764-010-9398-2G. Berillon ( * )UPR 2147 CNRS, Dynamique de l ’ Évolution Humaine, 75014 Paris, Francee-mail: gilles.berillon@evolhum.cnrs.fr G. Daver Département de Préhistoire, Musée de l ’ Homme, Muséum National d ’ Histoire Naturelle, 75116 Paris,FranceK. D ’ Août Functional Morphology, Department of Biology, University of Antwerp, Antwerp, BelgiumK. D ’ Août Centre for Research and Conservation, Royal Zoological Society of Antwerp, Antwerp, BelgiumG. Nicolas :  F. MultonLaboratoire M2S Mouvement, Sport, Santé (Physiologie et Biomécanique) UFR-APS,Université Rennes 2  –   ENS Cachan, Rennes, FranceB. de la Villetanet LAPP, UMR 5199 PACEA, Université Bordeaux 1, Bordeaux, FranceG. Digrandi :  G. DubreuilStation de primatologie, CNRS, Rousset sur Arc, France  foot joints act in coordinated and stereotyped manners, but are triggered differentlyaccording to whether the support is bipedal or quadrupedal. Although very occasionallyrealized, the bipedal walk of olive baboon appears to be a habitual and nonerraticlocomotor modality. Keywords  bipedalism.footstance.hindlimb.integratedsetup.kinematics.olivebaboon.quadrupedalism Introduction Kinematics and the functional morphology of nonhuman primates are 2 researchfields that provide crucial information that can be used to evaluate early hominidlocomotor modes (Coppens and Senut  1991; Crompton and Günther  2004; Franzen et al  . 2003; Ishida  et al.  2006; Kimura  et al.  1996; Meldrum and Hilton 2004; Preuschoft  1970, 1971, 1973; Strasser   et al.  1998; this issue). Kinematicinvestigations regard primates mainly as completely integrated systems anddocument movements quantitatively. Functional morphological analyses often start from anatomical descriptions  —  usually no more than 1 or 2 traits  —   and aim to relatethese to function. For technical reasons, these 2 complementary research fields areusually undertaken separately. Doing so has produced a great deal of valuable data, but correlations among form, function, and locomotor output often remainhypothetical. Because kinematic and kinetic data are still relatively scarce, it isoften difficult to evaluate functional hypotheses deduced from morpho-functionalanalyses, usually performed on cadavers, in light of   in vivo  experimental (motion)data. From a paleoanthropological perspective, Susman and Stern (1991, p. 126)have stated that   “ until we can understand the relationships between structure andfunction in living models, we will never be able to place any confidence in our inferences about fossil forms that are represented by fragmentary and incompleteremains. ”  This holds true also when studying bipedal locomotion, a hot topic in paleoanthropological discussions. Therefore collection of data on both movementsand anatomy will improve our understanding of the process of acquisition of  bipedality in human evolution.Integrated studies of nonhuman primate bipedalism have been developed sincethe late 1990s (Aerts  et al.  2000; D ’ Août   et al.  2001, 2002; Hirasaki  et al.  2004; Nakatsukasa  et al.  1995, 2004, 2006; Ogihara  et al.  2007; Vereecke and Aerts 2008; Vereecke  et al.  2003, 2004, 2005, 2006a, b) and are based on pioneering earlier  research (Crompton  et al.  1996; Elftman 1944; Jenkins 1972; Ishida  et al.  1974;Kimura 1985, 1990; Kimura  et al.  1979; Li  et al. , 1996; Okada 1985; Tardieu  et al. 1993; Yamazaki  et al.  1979). For historical reasons and because of the typicallylimited access to primates, these integrated studies have been developed for only afew species, e.g.,  Hylobates lar  ,  Macaca fuscata ,  Pan paniscus . In addition, theytypically use few individuals and focus on cross-sectional analyses. Despite their limitations, these integrated studies have provided a large amount of srcinal dataand have put human and nonhuman bipedalism into a comparative perspective. Thiscan be illustrated by studies of the transverse midtarsal joint in nonhuman primates.In humans, the stability of the transverse midtarsal joint has been associated with an 160 G. Berillon  et al.  efficient support for bipedal locomotion, whereas the compliant nonhuman primatefoot with a midtarsal break has been associated with inefficient bipedalism (Bojsen-Moller  1979; Elftman and Manter, 1935a, b; Lewis 1989). As a consequence, it is implicit in the paleoanthroplogical literature that a hominid with some degree of compliancy in the midfoot should not be considered an efficient biped (see Ward2002 for a complete review of the literature). Researchers have challenged theanatomical basis of midfoot flexibility in some nonhuman primates (DeSilva 2010;Günther  1989; Vereecke  et al.  2003), and thanks to an integrated analysis, Vereeckeand Aerts (2008) have demonstrated that foot compliance might in fact contributeto a form of propulsion generation in bipedalism in gibbons. This example showshow the analysis of nonhuman-like bipedalism in primates can trigger novelinterpretations of functional anatomy and, as a consequence, provide potentialnew perspectives on bipedalism in early hominids.Our team is currently developing an integrated technical platform that couplesmotion and anatomical analyses of nonhuman primates at the Primatology Station of the French National Centre for Scientific Research (CNRS). We are analyzing boththe kinematics and the anatomy of bipedal vs. quadrupedal locomotion in baboons.We chose baboons because it has been known since the 1970s that they occasionally but spontaneously walk bipedally in the wild (Hunt  1989; Rose 1976, 1977; Wrangham 1980) as well as in captivity (G. Berillon,  pers. obs .). However, thekinematics and kinetics of their bipedal and quadrupedal locomotor behavior are still poorly documented (Ishida  et al.  1974; Okada 1985; Shapiro and Raichlen 2005), as is their type of foot contact to the ground (Meldrum 1991; Schmitt and Larson1995). We aim at filling this gap and have started by describing bipedal kinematicsof the main segments of the body (Berillon  et al  . 2010) and describing an integratedsetup for 3D motion capture and anatomical description. In addition, we present theresults of the first comparative analysis of bipedal vs. quadrupedal walking in olive baboons of a wide age range, focusing on the sagittal kinematics of the hind limband the foot. Materials and Methods General SetupTheCNRSPrimatologyStationinRousset-sur-Arc(France)housesandbreedsbaboonsfor scientific investigations. All individuals receive veterinary monitoring from birth onand undergo annual health checks. This baboon population therefore offers anexceptionally valuable basis for joint and long-term motion analysis and anatomicalinvestigations on nonhuman primates. The baboons at the Primatology Station aremainly housed in groups of several tens of individuals. The groups live in open-air enclosures of which the surface areas span between approximately 150 and 500 m, andwhich are connected to permanent shelters by corridors. We selected the group living inenclosure B2F for our studies because 1) the number of baboons is controlled andmaintained at   ca.  60 individuals, representing all age classes from newborns (5  –  6 births per year) to old adults ( ≤ 18 years old); 2) many individuals spontaneously walk bipedally; 3) the arrangement of the enclosure and its surface area ( ca.  300 m) are Bipedalism vs. Quadrupedalism in Olive Baboons 161  well-suited to the installation of an open-air motion analysis setup within the enclosureand its immediate periphery; and 4) the proximity of the veterinary building, includinga pharmacy, a laboratory, and the X-ray machine (Mobil X ray generator SAXOAPELEM), allows on-the-spot morphological investigations and thus limits stresswhen capturing the individuals. The connection between the enclosure and the indoor structure is controlled by several trapdoors, allowing us to adapt the composition of the sample in the enclosure for 2  –  3 h for specific experiments. Each individual isidentified by a numbered collar that is readable on the video footage.We collect data in 2 ways. First, we have constructed a technical platform toanalyze locomotion in olive baboons within their living environment and throughout ontogeny. It consists of a motion analysis system with high-speed video, force plates,and pressure plates. The motion capture and analysis setup allows for high-frequencyrecordings of baboon locomotion along a horizontal surface and was adapted fromexisting setups (Aerts  et al.  2000; D ’ Août   et al.  2001, 2004; Hirasaki  et al.  2004; Nicolas  et al.  2007; Vereecke  et al  . 2006a, b). Second, we conduct noninvasive morphological investigations (weighing, external measurements, radiography) of allindividuals of the population.We make morphological investigations on anesthetized individuals duringscheduled captures. These consist of external measurements, measurements of joint mobility, weighing, and osteoarticular observations based on X-ray imaging.Captures are conducted every 3 mo under veterinary control, and are the only formof physical interaction allowed with the baboons in the enclosure. We capture the baboons individually using a restraining nest box. We then transfer the capturedindividual to a cage to receive general anesthesia via intramuscular injection of Imalgène (10  –  15 mg/kg). Anesthesia lasts  ≤ 30 min, the time required to make theexternal measurements and radiographs, to develop the films, and to weigh theindividuals. We perform additional anatomical investigations  —  dissections, inertial properties, 3D imaging, etc.  —   on cadavers when available.In conclusion, our research facilities enable us to monitor quantitatively themorphological, functional, and behavioral development, i.e., in a longitudinal studyapproach of each individual in the enclosure with limited stress for the subjects. Our experiments have been approved by the Regional Ethics Committee for animalexperimentation of the Midi-Pyrénées Region (Letter MP/01/15/02/08, datedFebruary 20, 2008).MaterialsTo date, we have recorded 320 quadrupedal gait sequences. These were performed by all of the individuals >6 mo old, sometimes several times and in some cases at several stages of ontogeny. In addition, we recorded 90 bipedal gait sequences performed by young individuals (6 mo  –  6 yr old) in several stages of ontogeny. For this initial comparison of bipedal and quadrupedal kinematics, we selected 10  Papioanubis  for which we recorded both bipedal and quadrupedal locomotion at equivalent stages in their development, which allows us to limit the effect of individual variation when comparing the characteristics of bipedal and quadrupedalgaits. We give general information on these 10 individuals in Table I; ages rangedfrom 0.55 to 5.39 yr and masses from 2.7 kg to 15.2 kg. 162 G. Berillon  et al.  Methods The Motion Capture Setup  The motion capture setup is based on a multicamerahigh-speed video recording system. The recording zone is in the southeastern part of the open-air enclosure B2F (Fig. 1). To guide the baboons along a regular path, we built an elevated, horizontal walkway around which we set up the video cameras.The walkway (podium) is a concrete structure, 80 cm wide, 30 cm high, and 5 mlong, with ramps at each end to maintain continuity with the ground in the enclosure.The walkway runs east to west, parallel to and 3 m away from the southern edge of the enclosure. Two free spaces are supplied for force plates and pressure pads(FootScan).We mounted 4 high-speed digital video cameras (Basler 602fc) outside the fenceon tripods and swivel arms. We equipped each camera with a C-Mount manual lens(8  –  48 mm F/1.0). We use the three cameras located in the southern part of theobservation area for 3D motion capture within a 2 m-wide field: 1 camera ishorizontally oriented, perpendicular to the long axis of the walkway, at a distance of 3.5 m from the center of the recording field and at a height of 40 cm above the top of the walkway; 2 cameras are obliquely oriented on either side of the previous camera, ca.  2.5 m away from it, at a height of 1.40 m above the top of the walkway and4.5 m distant from the centre of the recording field. The fourth camera is placedopposite to the first camera, perpendicular to the long axis of the walkway, at a Table I  Composition of bipedal (2P) and quadrupedal (4P) samples used in the study Name Identification tag Code Sex Gait Age (yr) Mass (kg)Chris 854 V792BA M 2P 0.67 2.94P 0.55 2.7Chantal 139 V908I F 2P 1.09 4.14P 1.09 4.1Babar 632 V916F M 2P 1.58 5.44P 1.88 6.1Alf 643 V894G M 2P 2.38 7.14P 2.39 7.1Vinci 568 V896F M 2P 3.14 8.34P 3.27 8.5Voltarelle 604 V915F F 2P 3.28 7.34P 3.12 7.1Vernie 638 V903D F 2P 3.28 6.34P 3.15 6.1Victoire 406 V896E F 2P 3.82 10.34P 3.63 9.9Volga 411 V916D F 2P 3.95 12.54P 4.09 12.5Tassadite 606 V893E F 2P 5.39 15.24P 5.09 14.5Bipedalism vs. Quadrupedalism in Olive Baboons 163
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