Kristiaan D'Août

Human-like external function of the foot, and fully upright gait, confirmed in the 3.66 million year old Laetoli hominin footprints by topographic statistics, experimental footprint-formation and computer simulation

It is commonly held that the major functional features of the human foot (e.g. a functional longitudinal medial arch, lateral to medial force transfer and hallucal (big-toe) push-off) appear only in the last 2 Myr, but functional interpretations of footbones and footprints of early human ancestors (hominins) prior to 2 million years ago (Mya) remain contradictory. Pixel-wise topographical statistical analysis of Laetoli footprint morphology, compared with results from experimental studies of footprint formation; foot-pressure measurements in bipedalism of humans and non-human great apes; and computer simulation techniques, indicate that most of these functional features were already present, albeit less strongly expressed than in ourselves, in the maker of the Laetoli G-1 footprint trail, 3.66 Mya. This finding provides strong support to those previous studies which have interpreted the G-1 prints as generally modern in aspect.

Locomotion in bonobos (Pan paniscus): differences and similarities between bipedal and quadrupedal terrestrial walking, and a comparison with other locomotor modes.

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.

Functional anatomy of the gibbon forelimb: adaptations to a brachiating lifestyle

It has been shown that gibbons are able to brachiate with very low mechanical costs. The conversion of muscle activity into smooth, purposeful movement of the limb depends on the morphometry of muscles and their mechanical action on the skeleton. Despite the gibbons reputation for excellence in brachiation, little information is available regarding either its gross musculoskeletal anatomy or its more detailed muscle–tendon architecture. We provide quantitative anatomical data on the muscle–tendon architecture (muscle mass, physiological cross‐sectional area, fascicle length and tendon length) of the forelimb of four gibbon species, collected by detailed dissections of unfixed cadavers. Data are compared between different gibbon species and with similar published data of non‐brachiating primates such as macaques, chimpanzees and humans. No quantitative differences are found between the studied gibbon species. Both their forelimb anatomy and muscle dimensions are comparable when normalized to the same body mass. Gibbons have shoulder flexors, extensors, rotator muscles and elbow flexors with a high power or work‐generating capacity and their wrist flexors have a high force‐generating capacity. Compared with other primates, the elbow flexors of gibbons are particularly powerful, suggesting that these muscles are particularly important for a brachiating lifestyle. Based on this anatomical study, the shoulder flexors, extensors, rotator muscles, elbow flexors and wrist flexors are expected to contribute the most to brachiation.

Morphological analysis of the hindlimb in apes and humans. II. Moment arms

Flexion/extension moment arms were obtained for the major muscles crossing the hip, knee and ankle joints in the orang‐utan, gibbon, gorilla (Eastern and Western lowland) and bonobo. Moment arms varied with joint motion and were generally longer in proximal limb muscles than distal limb muscles. The shape of the moment arm curves (i.e. the plots of moment arm against joint angle) differed in different hindlimb muscles and in the same muscle in different subjects (both in the same and in different ape species). Most moment arms increased with increasing joint flexion, a finding which may be understood in the context of the employment of flexed postures by most non‐human apes (except orang‐utans) during both terrestrial and arboreal locomotion. When compared with humans, non‐human great apes tended to have muscles better designed for moving the joints through large ranges. This was particularly true of the pedal digital flexors in orang‐utans. In gibbons, the only lesser ape studied here, many of the moment arms measured were relatively short compared with those of great apes. This study was performed on a small sample of apes and thus differences noted here warrant further investigation in larger populations.

Comparative forefoot trabecular bone architecture in extant hominids

The appearance of a forefoot push-off mechanism in the hominin lineage has been difficult to identify, partially because researchers disagree over the use of the external skeletal morphology to differentiate metatarsophalangeal joint functional differences in extant great apes and humans. In this study, we approach the problem by quantifying properties of internal bone architecture that may reflect different loading patterns in metatarsophalangeal joints in humans and great apes. High-resolution x-ray computed tomography data were collected for first and second metatarsal heads of Homo sapiens (n = 26), Pan paniscus (n = 17), Pan troglodytes (n = 19), Gorilla gorilla (n = 16), and Pongo pygmaeus (n = 20). Trabecular bone fabric structure was analyzed in three regions of each metatarsal head. While bone volume fraction did not significantly differentiate human and great ape trabecular bone structure, human metatarsal heads generally show significantly more anisotropic trabecular bone architectures, especially in the dorsal regions compared to the corresponding areas of the great ape metatarsal heads. The differences in anisotropy between humans and great apes support the hypothesis that trabecular architecture in the dorsal regions of the human metatarsals are indicative of a forefoot habitually used for propulsion during gait. This study provides a potential route for predicting forefoot function and gait in fossil hominins from metatarsal head trabecular bone architecture.

The dynamics of hylobatid bipedalism: evidence for an energy-saving mechanism?

SUMMARY When gibbons travel through the forest canopy, brachiation is alternated with short bipedal bouts over horizontal boughs. We know, from previous research, that brachiation is a very efficient locomotor mode that makes use of a pendulum-like exchange of energy, but to date, nothing is known about the dynamics of hylobatid bipedalism. We wondered if gibbons also make use of an efficient gait mechanism during bipedal locomotion. To investigate this, we calculated oscillations of the centre of mass (COM), energy fluctuations, recovery rates and power outputs from the 3D ground reaction forces. These ground reaction forces were collected during spontaneous bipedal locomotion of four untrained white-handed gibbons (Hylobates lar) over an instrumented walkway (with an AMTI force plate). Excursions of the COM are relatively large during hylobatid bipedalism and the fluctuations of potential and kinetic energy are largely in-phase. Together with the low inverted pendulum recovery rates, this points to a spring-mass mechanism during bipedal locomotion. Although the well-developed Achilles tendon of gibbons seems to be a good candidate for the storage and recoil of elastic energy, this is not supported by kinematical data of the ankle joint. Instead, we suggest that the knee extensor muscle tendon unit functions as an energy-saving mechanism during hylobatid bipedalism, but detailed anatomical data is needed to confirm this suggestion. At low speeds gibbons use either pendular or spring mechanics, but a clear gait transition as seen in most quadrupedal mammals is absent. At moderate to high velocities, gibbons use a bouncing gait, generally without aerial phases. This supports the view that aerial phases are not a prerequisite for spring-mass mechanics and reinforces the claim that duty factor alone should not be used to distinguish between a walk and run.

Functional analysis of the foot and ankle myology of gibbons and bonobos

This study investigates the foot and ankle myology of gibbons and bonobos, and compares it with the human foot. Gibbons and bonobos are both highly arboreal species, yet they have a different locomotor behaviour. Gibbon locomotion is almost exclusively arboreal and is characterized by speed and mobility, whereas bonobo locomotion entails some terrestrial knuckle‐walking and both mobility and stability are important. We examine if these differences in locomotion are reflected in their foot myology. Therefore, we have executed detailed dissections of the lower hind limb of two bonobo and three gibbon cadavers. We took several measurements on the isolated muscles (mass, length, physiological cross sectional area, etc.) and calculated the relative muscle masses and belly lengths of the major muscle groups to make interspecific comparisons. An extensive description of all foot and ankle muscles is given and differences between gibbons, bonobos and humans are discussed. No major differences were found between the foot and ankle musculature of both apes; however, marked differences were found between the ape and human foot. The human foot is specialized for solely one type of locomotion, whereas ape feet are extremely adaptable to a wide variety of locomotor modes. Apart from providing interesting anatomical data, this study can also be helpful for the interpretation of fossil (pre)hominids.

Pressure Distribution Patterns under the Feet of New Walkers: The First Two Months of Independent Walking

In order to describe foot function during the first weeks of independent walking, spatio-temporal pressure distribution patterns were measured. These data give detailed information about roll-off of the foot, by determining the course of the center of pressure, and about load bearing, by calculating relative vertical impulses under the feet. During those first weeks of independent walking, roll-off is very unstable. Although infants can occasionally perform a mature roll-off, a consistent pattern has not yet developed and there is instability. To improve stability the entire plantar surface area contributes to load bearing – first, because a larger contact area will improve stability, and second, because a forward shifting of the load allows more muscular control to compensate for minor imbalances under the foot.

The evolution of compliance in the human lateral mid-foot

Fossil evidence for longitudinal arches in the foot is frequently used to constrain the origins of terrestrial bipedality in human ancestors. This approach rests on the prevailing concept that human feet are unique in functioning with a relatively stiff lateral mid-foot, lacking the significant flexion and high plantar pressures present in non-human apes. This paradigm has stood for more than 70 years but has yet to be tested objectively with quantitative data. Herein, we show that plantar pressure records with elevated lateral mid-foot pressures occur frequently in healthy, habitually shod humans, with magnitudes in some individuals approaching absolute maxima across the foot. Furthermore, the same astonishing pressure range is present in bonobos and the orangutan (the most arboreal great ape), yielding overlap with human pressures. Thus, while the mean tendency of habitual mechanics of the mid-foot in healthy humans is indeed consistent with the traditional concept of the lateral mid-foot as a relatively rigid or stabilized structure, it is clear that lateral arch stabilization in humans is not obligate and is often transient. These findings suggest a level of detachment between foot stiffness during gait and osteological structure, hence fossilized bone morphology by itself may only provide a crude indication of mid-foot function in extinct hominins. Evidence for thick plantar tissues in Ardipithecus ramidus suggests that a human-like combination of active and passive modulation of foot compliance by soft tissues extends back into an arboreal context, supporting an arboreal origin of hominin bipedalism in compressive orthogrady. We propose that the musculoskeletal conformation of the modern human mid-foot evolved under selection for a functionally tuneable, rather than obligatory stiff structure.

Functional adaptations in the forelimb muscles of non-human great apes

The maximum capability of a muscle can be estimated from simple measurements of muscle architecture such as muscle belly mass, fascicle length and physiological cross‐sectional area. While the hindlimb anatomy of the non‐human apes has been studied in some detail, a comparative study of the forelimb architecture across a number of species has never been undertaken. Here we present data from chimpanzees, bonobos, gorillas and an orangutan to ascertain if, and where, there are functional differences relating to their different locomotor repertoires and habitat usage. We employed a combination of analyses including allometric scaling and ancovas to explore the data, as the sample size was relatively small and heterogeneous (specimens of different sizes, ages and sex). Overall, subject to possible unidentified, confounding factors such as age effects, it appears that the non‐human great apes in this sample (the largest assembled to date) do not vary greatly across different muscle architecture parameters, even though they perform different locomotor behaviours at different frequencies. Therefore, it currently appears that the time spent performing a particular behaviour does not necessarily impose a dominating selective influence on the soft‐tissue portion of the musculoskeletal system; rather, the overall consistency of muscle architectural properties both between and within the Asian and African apes strengthens the case for the hypothesis of a possible ancient shared evolutionary origin for orthogrady under compressive and/or suspensory loading in the great apes.