A comparative study of muscle activity and synergies during walking in baboons and humans.

Bipedal locomotion was a major functional change during hominin evolution, yet, our understanding of this gradual and complex process remains strongly debated. Based on fossil discoveries, it is possible to address functional hypotheses related to bipedal anatomy, however, motor control remains intangible with this approach. Using comparative models which occasionally walk bipedally has proved to be relevant to shed light on the evolutionary transition toward habitual bipedalism. Here, we explored the organization of the neuromuscular control using surface electromyography (sEMG) for six extrinsic muscles in two baboon individuals when they walk quadrupedally and bipedally on the ground. We compared their muscular coordination to five human subjects walking bipedally. We extracted muscle synergies from the sEMG envelopes using the non-negative matrix factorization algorithm which allows decomposing the sEMG data in the linear combination of two non-negative matrixes (muscle weight vectors and activation coefficients). We calculated different parameters to estimate the complexity of the sEMG signals, the duration of the activation of the synergies, and the generalizability of the muscle synergy model across species and walking conditions. We found that the motor control strategy is less complex in baboons when they walk bipedally, with an increased muscular activity and muscle coactivation. When comparing the baboon bipedal and quadrupedal pattern of walking to human bipedalism, we observed that the baboon bipedal pattern of walking is closer to human bipedalism for both baboons, although substantial differences remain. Overall, our findings show that the muscle activity of a non-adapted biped effectively fulfills the basic mechanical requirements (propulsion and balance) for walking bipedally, but substantial refinements are possible to optimize the efficiency of bipedal locomotion. In the evolutionary context of an expanding reliance on bipedal behaviors, even minor morphological alterations, reducing muscle coactivation, could have faced strong selection pressure, ultimately driving bipedal evolution in hominins.

From quadrupedal to bipedal walking 'on the fly': the mechanics of dynamical mode transition in primates.

We investigated how baboons transition from quadrupedal to bipedal walking without any significant interruption in their forward movement (i.e. transition 'on the fly'). Building on basic mechanical principles (momentum only changes when external forces/moments act on the body), insights into possible strategies for such a dynamical mode transition are provided and applied first to the recorded planar kinematics of an example walking sequence (including several continuous quadrupedal, transition and subsequent bipedal steps). Body dynamics are calculated from the kinematics. The strategy used in this worked example boils down to: crouch the hind parts and sprint them underneath the rising body centre of mass. Forward accelerations are not in play. Key characteristics of this transition strategy were extracted: progression speed, hip height, step duration (frequency), foot positioning at touchdown with respect to the hip and the body centre of mass (BCoM), and congruity between the moments of the ground reaction force about the BCoM and the rate of change of the total angular moment. Statistical analyses across the full sample (15 transitions of 10 individuals) confirm this strategy is always used and is shared across individuals. Finally, the costs (in J kg-1 m-1) linked to on the fly transitions were estimated. The costs are approximately double those of both the preceding quadrupedal and subsequent bipedal walking. Given the short duration of the transition as such (<1 s), it is argued that the energetic costs to change walking posture on the fly are negligible when considered in the context of the locomotor repertoire.

The quadrupedal walking gait of the olive baboon, Papio anubis: an exploratory study integrating kinematics and EMG.

Primates exhibit unusual quadrupedal features (e.g. diagonal gaits, compliant walk) compared with other quadrupedal mammals. Their origin and diversification in arboreal habitats have certainly shaped the mechanics of their walking pattern to meet the functional requirements necessary for balance control in unstable and discontinuous environments. In turn, the requirements for mechanical stability probably conflict with mechanical energy exchange. In order to investigate these aspects, we conducted an integrative study on quadrupedal walking in the olive baboon (Papio anubis) at the Primatology station of the CNRS in France. Based on kinematics, we describe the centre of mass mechanics of the normal quadrupedal gait performed on the ground, as well as in different gait and substrate contexts. In addition, we studied the muscular activity of six hindlimb muscles using non-invasive surface probes. Our results show that baboons can rely on an inverted pendulum-like exchange of energy (57% on average, with a maximal observed value of 84%) when walking slowly (<0.9 m s-1) with a tight limb phase (∼55%) on the ground using diagonal sequence gaits. In this context, the muscular activity is similar to that of other quadrupedal mammals, thus reflecting the primary functions of the muscles for limb movement and support. In contrast, walking on a suspended branch generates kinematic and muscular adjustments to ensure better control and to maintain stability. Finally, walking using the lateral sequence gait increases muscular effort and reduces the potential for high recovery rates. The present exploratory study thus supports the assumption that primates are able to make use of an inverted pendulum mechanism on the ground using a diagonal walking gait, yet a different footfall pattern and substrate appear to influence muscular effort and efficiency.

Deslorelin acetate implant induces transient sterility and behavior changes in male olive baboon (Papio anubis): A case study.

This case study evaluates the effects of a 4.7 mg deslorelin acetate implant on one male olive baboon (Papio anubis). Implantation induces transient azoospermia after which the subject was able to conceive again. Behavior was also impacted with a decrease in our proxies of aggressiveness and sexual arousal.

Compliant legs enable lizards to maintain high running speeds on complex terrains.

Substrate variations are likely to constrain animal performance in natural environments, as running over complex terrains challenges the dynamic stability of the body differently in each step. Yet, being able to negotiate complex terrains at top speed is a strong advantage for animals that have to deal with predators and evasive prey. Little is known on how animals negotiate such terrain variability at high speed. We investigated this in fast-running Acanthodactylus boskianus lizards, by measuring their 3D kinematics using four synchronised high-speed video cameras (325 Hz) on an adaptable racetrack. This racetrack was covered with four different substrates, representing increasing levels of terrain complexity. We found that the lizards deal with this complexity gradient by gradually adopting more erect parasagittal leg postures. Legs in a more-erect position are more compliant and are therefore highly adjustable on complex terrains. Additionally, the lizards stabilise their head, which facilitates vestibular and visual perception. Together, compliant legs and head stabilisation enable the lizards to minimise movements of the body centre of mass, even when running on highly irregular terrains. This suggests that the head and the centre of mass are the priority targets for running on uneven terrains. As a result, running performance (mean forward speed) decreases only slightly, and only on the most challenging substrate under investigation.

The body center of mass in primates: Is it more caudal than in other quadrupedal mammals?

OBJECTIVES: Whole body center of mass (BCoM) position values are lacking for a comparative sample of primates. Therefore, it still remains unknown whether the BCoM in primates is more posteriorly located than in other mammals. The aim of the present report is to provide data for a large sample of primate species and to compare the position of the BCoM in primates to non-primate mammals. MATERIALS AND METHODS: We collected morphometrics on eight primate species belonging to various families: Hylobatidae (Nomascus grabriellae, Nomascus Siki), Cercopithecidae (Cercopithecus roloway, Cercopithecus lhoesti, Colobus guereza, Trachypithecus francoisi), Cebidae (Sapajus xanthosternos), and Atelidae (Ateles fusciceps). Using a geometric model, we assessed the position of the BCoM in a natural quadrupedal posture and in a control posture. To complete our comparative sample with a wider range of morphotypes, we added the data available in the literature for hominoids (Pan paniscus, Pan troglodytes, Gorilla gorilla, Pongo pygmaeus, Hylobates lar) and another cercopithecoid species (Papio anubis). We also evaluated the phylogenetic signal of the position of the BCoM in primates. RESULTS: The variation in the position of the BCoM in primates is very large, ranging from 40% of the distance between the hip and the shoulder in Ateles fusciceps to 63% in Hylobates lar. We observed a strong phylogenetic signal for this trait: hominoid species, as well as the baboon, have a cranial BCoM relative to the midline between the hip and the shoulder, arboreal cercopithecoids and the spider monkey have a caudal BCoM, and the capuchin monkey has a BCoM positioned at mid-trunk. The variation observed in non-primate quadrupedal mammals lies inside the variation range of primates, from 51% in Felis catus to 63% in Canis familiaris. DISCUSSION: The BCoM of primates is not more posteriorly located than in other quadrupedal mammals; however, there is a substantial range of variation in primates, from caudal (in arboreal quadrupeds) to cranial (in hominoids and terrestrial quadrupeds) positions. This variation is related to a phylogenetic model that suggests stabilizing selection for this trait. It seems that the BCoM position mostly depends of the size of the appendicular system (i.e., limbs) and the tail. Therefore, it may also reflect a general trend in quadrupedal mammals with arboreal species exhibiting a caudal BCoM and terrestrial species exhibiting a cranial BCoM. These results are discussed in the context of the locomotor evolution of primates including locomotor habits and gait mechanics. We also propose a new "passive" mechanism for the explanation of the particular weight support pattern observed in primates with tails.

Segmental morphometrics of bonobos (Pan paniscus): are they really different from chimpanzees (Pan troglodytes)?

The inertial properties of body segments reflect performance and locomotor habits in primates. While Pan paniscus is generally described as more gracile, lighter in body mass, and as having relatively longer and heavier hindlimbs than Pan troglodytes, both species exhibit very similar patterns of (quadrupedal and bipedal) kinematics, but show slightly different locomotor repertoires. We used a geometric model to estimate the inertial properties for all body segments (i.e. head, trunk, upper and lower arms, hand, thigh, shank and foot) using external length and diameter measurements of 12 anaesthetized bonobos (eight adults and four immatures). We also calculated whole limb inertial properties. When we compared absolute and relative segment morphometric and inertial variables between bonobos and chimpanzees, we found that adult bonobos are significantly lighter than adult chimpanzees. The bonobo is also shorter in head length, upper and lower arm lengths, and foot length, and is generally lighter in most absolute segment mass values (except head and hand). In contrast, the bonobo has a longer trunk. When scaled relative to body mass, most differences disappear between the two species. Only the longer trunk and the shorter head of the bonobo remain apparent, as well as the lighter thigh compared with the chimpanzee. We found similar values of natural pendular periods of the limbs in both species, despite differences in absolute limb lengths, masses, mass centres (for the hindlimb) and moments of inertia. While our data contradict the commonly accepted view that bonobos have relatively longer and heavier hindlimbs than chimpanzees, they are consistent with the observed similarities in the quadrupedal and bipedal kinematics between these species. The morphological differences between both species are more subtle than those previously described from postcranial osteological materials.

Behavioral implications of ontogenetic changes in intrinsic hand and foot proportions in olive baboons (Papio Anubis).

OBJECTIVES: Relatively long digits are considered to enhance grasping performance in primates. We tested whether growth-related changes in intrinsic hand and foot proportions may have behavioral implications for growing animals, by examining whether ontogenetic changes in digital proportions are related to variation in voluntary grasping behaviors in baboons. MATERIALS AND METHODS: Longitudinal morphological and behavioral data were collected on 6 captive olive baboons (Papio anubis) as they aged from 5 to 22 months. The length of digits and metapodials, measured from radiographs, were used to calculate phalangeal indices (i.e., PIs: summed length of non-distal phalanges relative to corresponding metapodial length). We also examined the allometric scaling of digital bones relative to body mass. We observed baboon positional behaviors over a 15-day period following the radiographic sessions, quantifying the frequency of forelimb and hindlimb grasping behaviors. RESULTS: PIs for all digits declined during growth, a result of the differential scaling of metapodials (which scaled to body mass with isometry) versus phalanges (which scaled with negative allometry). The incidence of forelimb and hindlimb grasping behaviors declined with age. Though we found no relationship between forelimb grasping and hand proportions, the incidence of hindlimb grasping was directly correlated with postaxial digit PIs. DISCUSSION: Only changes in the intrinsic proportions of the pedal digits are associated with variation in grasping activity in growing baboons. This finding accords previous biomechanical and neuroanatomical studies showing distinct functional roles for the hands and feet during primate locomotion, and has important implications for reconstructing primate locomotor evolution.

Segmental morphometrics of the olive baboon (Papio anubis): a longitudinal study from birth to adulthood.

The linear dimensions and inertial characteristics of the body are important in locomotion and they change considerably during the ontogeny of animals, including humans. This longitudinal and ontogenetic study has produced the largest dataset to date of segmental morphometrics in a Catarrhini species, the olive baboon. The objectives of the study were to quantify the changes in body linear and inertial dimensions and to explore their (theoretical) mechanical significance for locomotion. We took full-body measurements of captive individuals at regular intervals. Altogether, 14 females and 16 males were followed over a 7-year period, i.e. from infancy to adulthood. Our results show that individual patterns of growth are very consistent and follow the general growth pattern previously described in olive baboons. Furthermore, we obtained similar growth curve structures for segment lengths and masses, although the respective time scales were slightly different. The most significant changes in body morphometrics occurred during the first 2 years of life and concerned the distal parts of the body. Females and males were similar in size and shape at birth. The rate and duration of growth produced substantial size-related differences throughout ontogeny, while body shapes remained very similar between the sexes. We also observed significant age-related variations in limb composition, with a proximal shift of the centre of mass within the limbs, mainly due to changes in mass distribution and in the length of distal segments. Finally, we observed what we hypothesize to be 'early biomechanical optimization' of the limbs for quadrupedal walking. This is due to a high degree of convergence between the limbs' natural pendular periods in infants, which may facilitate the onset of quadrupedal walking. Furthermore, the mechanical significance of the morphological changes observed in growing baboons may be related to changing functional demands with the onset of autonomous (quadrupedal) locomotion. From a wider perspective, these data provide unique insights into questions surrounding both the processes of locomotor development in primates and how these processes might evolve.

The origin of bipedality as the result of a developmental by-product: The case study of the olive baboon (Papio anubis).

In this paper, we point to the importance of considering infancy in the emergence of new locomotor modes during evolution, and particularly when considering bipedal walking. Indeed, because infant primates commonly exhibit a more diverse posturo-locomotor repertoire than adults, the developmental processes of locomotion represent an important source of variation upon which natural selection may act. We have had the opportunity to follow the development of locomotion in captive individuals of a committed quadrupedal primate, the olive baboon (Papio anubis). We observed six infants at two different stages of their development. In total, we were able to analyze the temporal parameters of 65 bipedal steps, as well as their behavioral components. Our results show that while the basic temporal aspects of the bipedal walking gait (i.e., duty factor, dimensionless frequency, and hind lag) do not change during development, the baboon is able to significantly improve the coordination pattern between hind limbs. This probably influences the bout duration of spontaneous bipedal walking. During the same developmental stage, the interlimb coordination in quadrupedal walking is improved and the proportion of quadrupedal behaviors increases significantly. Therefore, the quadrupedal pattern of primates does not impede the developmental acquisition of bipedal behaviors. This may suggest that the same basic mechanism is responsible for controlling bipedal and quadrupedal locomotion, i.e., that in non-human primates, the neural networks for quadrupedal locomotion are also employed to perform (occasional) bipedal walking. In this context, a secondary locomotor mode (e.g., bipedalism) experienced during infancy as a by-product of locomotor development may lead to evolutionary novelties when under appropriate selective pressures.

Bipedality from locomotor autonomy to adulthood in captive olive baboon (Papio anubis): Cross-sectional follow-up and first insight into the impact of body mass distribution.

OBJECTIVE: Despite that the biomechanics of standing and walking bipedally has been extensively studied in nonhuman primates, the morphological features that may constrain, or facilitate, the control of balance and thus of the spontaneous occurrence of bipedal behavior are poorly known. We aim to test the relationship between body mass distribution and bipedal behavior using a nonhuman primate species, the olive baboon, Papio anubis, raised in captivity. MATERIALS AND METHODS: We collected quantitative data on the frequency and duration of bipedalism together with morphometrics on a sample of 22 individuals. We used ontogenetic changes as a natural experiment that provides insights into the impact of morphology. Specifically we focus on 1) quantifying how body mass distribution changes from infancy to adulthood in baboons; and 2) whether the different patterns of mass distribution influence the behavioral variables, i.e., a) the frequency and b) the duration of bouts of bipedal behavior realized in different activity contexts. RESULTS: With regard to assisted bipedal behaviors, the duration and frequency of bouts of standing, contrary to walking, are significantly related to age. With regard to unassisted bipedal behaviors, no correlation to age is observed; the bout duration of walking is strongly correlated to body mass and mass distribution, contrary to the frequency of walking as well as the bout duration and frequency of bipedal standing. DISCUSSION: Our results suggest a close relationship between the pattern of mass distribution and the mechanism of balance control in the spontaneous bipedal walking of baboons. The mechanical effects of the pattern of mass distribution on the ability to perform bipedally in extant nonhuman primates are discussed in the context of the evolution toward habitual bipedalism.

Effect of body mass distribution on the ontogeny of positional behaviors in non-human primates: Longitudinal follow-up of infant captive olive baboons (Papio anubis).

The diversity of primates' positional capabilities is unique among mammals. Indeed, they exhibit a daily repertoire composed of various locomotor and postural modes that may be linked to their particular morphological pattern. Because ontogeny undergoes parallel behavioral and morphological modifications, it may be useful to investigate the biomechanical consequences of the changing body shape. We, therefore, collected accurate quantitative and longitudinal data on positional behaviors, body mass distribution patterns, activities, and environment on a sample of six infant olive baboons, Papio anubis. These baboons are kept at the Primatology Station of the CNRS, France, where they live within the same social group. Individual behaviors were quantified using the focal sampling method. The body mass distribution was estimated according to a geometric model based on direct external measurements. Multivariate analysis enabled us to analyze the interactions between the data. Our results show that body mass distribution changes together with the ontogenetic changes in positional behaviors. At an early age, individuals have distally heavy segment masses in the limbs and an important fraction of the behavioral repertoire involves efficient grasping abilities. At the end of infancy, the same individuals have relatively more mass in proximal segments of the limbs and the proportion of quadrupedal walking is significantly higher while other climbing and suspensory behaviors decreased substantially. The present study experimentally confirms the association between body mass distribution and the positional repertoire of primates. These relationships, when interpreted in the context of basic biomechanical concepts, may improve our understanding of primate locomotion. We discuss further the implications of these functional relationships when modeling the evolutionary pathway of primates. Am. J. Primatol. 78:1201-1221, 2016. © 2016 Wiley Periodicals, Inc.

Vertical climbing in free-ranging bonobos: An exploratory study integrating locomotor performance and substrate compliance.

OBJECTIVES: Ecological factors and body size shape animal movement and adaptation. Large primates such as bonobos excel in navigating the demanding substrates of arboreal habitats. However, current approaches lack comprehensive assessment of climbing performance in free-ranging individuals, limiting our understanding of locomotor adaptations. This study aims to explore climbing performance in free-ranging bonobos and how substrate properties affect their behavior. METHODS: We collected data on the climbing performance of habituated bonobos, Pan paniscus, in the Bolobo Territory, Democratic Republic of Congo. We analyzed 46 climbing bouts (12 ascents, 34 descents) while moving on vertical substrates of varying diameter and compliance levels. This study assessed the average speed, peak acceleration, resting postures, and transitions between climbing and other locomotor modes. RESULTS: During climbing sequences and transitions, bonobos mitigate speed variations. They also exhibit regular pauses during climbing and show higher speeds during descent in contrast to their ascent. Regarding the influence of substrate properties, bonobos exhibit higher speed when ascending on thin and slightly flexible substrates, while they appear to achieve higher speeds when descending on large and stiff substrates, by using a "fire-pole slide" submode. DISCUSSION: Bonobos demonstrate remarkable abilities for negotiating vertical substrates and substrate properties influence their performance. Our results support the idea that bonobos adopt a behavioral strategy that aligns with the notion of minimizing costs. Overall, the adoption of high velocities and the use of low-cost resting postures may reduce muscle fatigue. These aspects could represent important targets of selection to ensure ecological efficiency in bonobos.

Bipedal behaviour in olive baboons: infants versus adults in a captive environment.

The olive baboon is described as a committed quadrupedal primate. However, available data show that they actually use a variety of locomotor and postural modes. Bipedalism is observed occasionally but spontaneously in captivity and in the wild. As observed in other Catarrhini, immature baboons appear to be more bipedal than adults: this study aims to provide the necessary quantitative data to support this hypothesis, as none has been available so far. The locomotor and postural repertoire was quantified for two age classes: infants beginning to forage independently, and adults. Our results show that infants appear to have a wider repertoire than adults, and bipedal postures and locomotion in infants, although infrequent, appear to distinguish them clearly from adults. In captivity, behavioural context and morphology are the two main factors that could explain age-related positional differences, given a constant ecological context.

Development of bipedal walking in olive baboons, Papio anubis: A kinematic analysis.

OBJECTIVE: Although extant nonhuman primates are not habitual bipeds, they are able to walk bipedally from an early age. In humans, children improve their walking skills through developmental processes and learning experience. In nonhuman primates, infants do not routinely experience bipedalism and their musculoskeletal system gradually specializes for other locomotor modes. The aim of this study is to explore the development of occasional bipedal walking in olive baboon and to test whether the postural adjustments change with age. MATERIALS AND METHODS: We collected kinematics and spatiotemporal parameters of bipedal gait in an ontogenetic sample of 24 baboons. Data were collected at the primatology station of the CNRS (France) and a total of 47 bipedal strides were extracted for the present analysis. RESULTS: Adults and adolescents walk bipedally in the same way, and the average kinematic pattern is similar across the age-classes. Infants walk bipedally with longer duty factor, they present larger movement amplitude of the thigh and the amplitude of the knee joint decreases with speed. In contrast, older baboons increase the amplitude of the knee and ankle joints with speed. DISCUSSION: In a non-adapted biped, the postural adjustments of bipedal walking vary with age. In infant baboons, the balance requirements are likely to be higher and these are solved by adopting a "blocking strategy". In older baboons, the postural adjustments are focused on the lower limb and the movements increase with speed. These results may echo, in some respects, the developmental sequence of the intersegmental coordination described in the ontogeny of human locomotion.

Balancing costs and benefits in primates: ecological and palaeoanthropological views.

Maintaining the balance between costs and benefits is challenging for species living in complex and dynamic socio-ecological environments, such as primates, but also crucial for shaping life history, reproductive and feeding strategies. Indeed, individuals must decide to invest time and energy to obtain food, services and partners, with little direct feedback on the success of their investments. Whereas decision-making relies heavily upon cognition in humans, the extent to which it also involves cognition in other species, based on their environmental constraints, has remained a challenging question. Building mental representations relating behaviours and their long-term outcome could be critical for other primates, but there are actually very little data relating cognition to real socio-ecological challenges in extant and extinct primates. Here, we review available data illustrating how specific cognitive processes enable(d) modern primates and extinct hominins to manage multiple resources (e.g. food, partners) and to organize their behaviour in space and time, both at the individual and at the group level. We particularly focus on how they overcome fluctuating and competing demands, and select courses of action corresponding to the best possible packages of potential costs and benefits in reproductive and foraging contexts. This article is part of the theme issue 'Existence and prevalence of economic behaviours among non-human primates'.

Small vertebrates running on uneven terrain: a biomechanical study of two differently specialised lacertid lizards.

While running, small animals frequently encounter large terrain variations relative to their body size, therefore, terrain variations impose important functional demands on small animals. Nonetheless, we have previously observed in lizards that running specialists can maintain a surprisingly good running performance on very uneven terrains. The relatively large terrain variations are offset by their capacity for leg adjustability that ensures a 'smooth ride' of the centre of mass (CoM). The question as to how the effect of an uneven terrain on running performance and locomotor costs differs between species exhibiting diverse body build and locomotor specializations remains. We hypothesise that specialized runners with long hind limbs can cross uneven terrain more efficiently than specialized climbers with a dorso-ventrally flattened body and equally short fore and hind limbs. This study reports 3D kinematics using high-speed videos (325 Hz) to investigate leg adjustability and CoM movements in two lacertid lizards (Acanthodactylus boskianus, running specialist; Podarcis muralis, climbing specialist). We investigated these parameters while the animals were running on a level surface and over a custom-made uneven terrain. We analysed the CoM dynamics, we evaluated the fluctuations of the positive and negative mechanical energy, and we estimated the overall cost of transport. Firstly, the results reveal that the climbers ran at lower speeds on flat level terrain but had the same cost of transport as the runners. Secondly, contrary to the running specialists, the speed was lower and the energy expenditure higher in the climbing specialists while running on uneven terrain. While leg movements adjust to the substrates' variations and enhance the stability of the CoM in the running specialist, this is not the case in the climbing specialist. Although their legs are kept more extended, the amplitude of movement does not change, resulting in an increase of the movement of the CoM and a decrease in locomotor efficiency. These results are discussed in light of the respective (micro-)habitat of these species and suggest that energy economy can also be an important factor for small vertebrates.