John A. Nyakatura

Kinematics and Center of Mass Mechanics During Terrestrial Locomotion in Northern Lapwings (Vanellus vanellus, Charadriiformes)

Avian bipedalism is best studied in derived walking/running specialists. Here, we use kinematics and center of mass (CoM) mechanical energy patterns to investigate gait transitions of lapwings-migratory birds that forage on the ground, and therefore may need a trade-off between the functional demands of terrestrial locomotion and long distance flights. The animals ran on a treadmill while high-speed X-ray videos were recorded within the sustainable speed range. Instantaneous CoM mechanics were computed from integrating kinematics and body segment properties. Lapwings exhibit similar locomotor characteristics to specialized walking/running birds, but have less distinct gaits. At slow speeds no clear separation between vaulting (i.e., walking) and bouncing (i.e., running) energy patterns exists. Mechanical energy recovery of non-bouncing gaits correlates poorly with speed and suggests inefficient use of the inverted pendulum mechanism. Speed ranges of gaits overlap considerably, especially those of grounded running, a gait with CoM mechanics indicative of running but without an aerial phase, and aerial phase running, with no preferential gait at most speeds. Compliant limb morphology and grounded running in birds can be regarded as an evolutionary constraint, but lapwings effectively make use of advantages offered by this gait for a great fraction of their speed range. Thus, effective usage of grounded running during terrestrial locomotion is suggested generally to be a part of striding avian bipedalism-even in species not specialized in walking/running locomotion.

Adjustments of global and hindlimb local properties during the terrestrial locomotion of the common quail (Coturnix coturnix)

SUMMARY Previous research has resulted in increasing insight into neuro-mechanical control strategies during perturbed locomotion. In contrast, more general analyses on simple model (template)-related parameters during avian terrestrial locomotion are still rare. Quail kinematic data obtained using X-ray videography combined with ground reaction force measurements were used as a basis to investigate how ‘global’ template and ‘local’ leg joint parameters in this small, predominantly terrestrial bird change with speed and gait. Globally, quail locomotion approximates a spring-like behavior in all investigated gaits. However, ground reaction forces are more vertically oriented, which may help to balance the trunk. At the joint level, practically all the spring-like work was found to occur in the intertarsal joint (ITJ). From walking to grounded running, the local stiffness of the ITJ decreases similarly to the reduction observed in global leg stiffness. Thus, in gaits without aerial phases the quails may modulate ITJ stiffness to regulate global leg stiffness, and therefore gait changes, to a significant degree. At higher speeds both global leg compression and stiffness are increased (the latter to values not significantly different to those obtained during walking). This enables the animals to shorten contact time and to generate aerial phases (running). However, we did not observe a change in the stiffness in the ITJ with a change of gait from grounded running to running. We hypothesize that a more extended leg at touch-down, controlled by the joint angles in the knee and ITJ, has an important influence in the leg stiffness adjustment process during running.

Functional morphology of the muscular sling at the pectoral girdle in tree sloths: convergent morphological solutions to new functional demands?

Recent phylogenetic analyses imply a diphyly of tree sloths and a convergent evolution of their obligatory suspensory locomotion. In mammals the extrinsic shoulder musculature forms a ‘muscular sling’ to support the trunk in quadrupedal postures. In addition, the extrinsic pectoral muscles are responsible for moving the proximal forelimb elements during locomotion. Due to the inverse orientation of the body in regard to the gravitational force, the muscular sling as configured as in pronograde mammals is unsuited to suspend the weight of the thorax in sloths. We here review the muscular topography of the shoulder in Choloepus didactylus and Bradypus variegatus in the light of presumably convergent evolution to adapt to the altered functional demands of the inverse orientation of the body. In addition, we venture to deduce the effect of the shoulder musculature of C. didactylus during locomotion based on previously published 3D kinematic data. Finally, we assess likely convergences in the muscular topography of both extant sloth lineages to test the hypothesis that convergent evolution is reflected by differing morphological solutions to the same functional demands posed by the suspensory posture. Muscular topography of the shoulder in C. didactylus is altered from the plesiomorphic condition of pronograde mammals, whereas the shoulder in B. variegatus more closely resembles the general pattern. Overall kinematics as well as the muscles suitable for pro‐ and retraction of the forelimb were found to be largely comparable to pronograde mammals in C. didactylus. We conclude that most of the peculiar topography of extrinsic forelimb musculature can be attributed to the inverse orientation of the body. These characteristics are often similar in both genera, but we also identified different morphological solutions that evolved to satisfy the new functional demands and are indicative of convergent evolution. We suggest that the shared phylogenetic heritage canalized the spectrum of possible solutions to new functional demands, and digging adaptations of early xenarthrans posed morphological constraints that resulted in similar suspensory postures. The data of this study, including muscle maps, will be helpful to infer locomotor characteristics of fossil sloths.

Three-dimensional kinematic analysis of the pectoral girdle during upside-down locomotion of two-toed sloths (Choloepus didactylus, Linné 1758).

BackgroundTheria (marsupials and placental mammals) are characterized by a highly mobile pectoral girdle in which the scapula has been shown to be an important propulsive element during locomotion. Shoulder function and kinematics are highly conservative during locomotion within quadrupedal therian mammals. In order to gain insight into the functional morphology and evolution of the pectoral girdle of the two-toed sloth we here analyze the anatomy and the three-dimensional (3D) pattern of shoulder kinematics during quadrupedal suspensory (upside-down) locomotion.MethodsWe use scientific rotoscoping, a new, non-invasive, markerless approach for x-ray reconstruction of moving morphology (XROMM), to quantify in vivo the 3D movements of all constituent skeletal elements of the shoulder girdle. Additionally we use histologic staining to analyze the configuration of the sterno-clavicular articulation (SCA).ResultsDespite the inverse orientation of the body towards gravity, sloths display a 3D kinematic pattern and an orientation of the scapula relative to the thorax similar to pronograde claviculate mammalian species that differs from that of aclaviculate as well as brachiating mammals. Reduction of the relative length of the scapula alters its displacing effect on limb excursions. The configuration of the SCA maximizes mobility at this joint and demonstrates a tensile loading regime between thorax and limbs.ConclusionsThe morphological characteristics of the scapula and the SCA allow maximal mobility of the forelimb to facilitate effective locomotion within a discontinuous habitat. These evolutionary changes associated with the adoption of the suspensory posture emphasized humeral influence on forelimb motion, but allowed the retention of the plesiomorphic 3D kinematic pattern.

Soft tissue influence on ex vivo mobility in the hip of Iguana: comparison with in vivo movement and its bearing on joint motion of fossil sprawling tetrapods.

The reconstruction of a joints maximum range of mobility (ROM) often is a first step when trying to understand the locomotion of fossil tetrapods. But previous studies suggest that the ROM of a joint is restricted by soft tissues surrounding the joint. To expand the limited informative value of ROM studies for the reconstruction of a fossil species’ locomotor characteristics, it is moreover necessary to better understand the relationship of ex vivo ROM with the actual in vivo joint movement. To gain insight into the relationship between ex vivo mobility and in vivo movement, we systematically tested for the influence of soft tissues on joint ROM in the hip of the modern lizard Iguana iguana. Then, we compared the ex vivo mobility to in vivo kinematics of the hip joint in the same specimens using X‐ray sequences of steady‐state treadmill locomotion previously recorded. With stepwise removal of soft tissues and a repeated‐measurement protocol, we show that soft tissues surrounding the hip joint considerably limit ROM, highlighting the problems when joint ROM is deduced from bare bones only. We found the integument to have the largest effect on the range of long‐axis rotation, pro‐ and retraction. Importantly, during locomotion the iguana used only a fragment of the ROM that was measured in our least restrictive dissection situation (i.e. pelvis and femur only conjoined by ligaments), demonstrating the discrepancy between hip joint ROM and actual in vivo movement. Our study emphasizes the necessity for caution when attempting to reconstruct joint ROM or even locomotor kinematics from fossil bones only, as actual in vivo movement cannot be deduced directly from any condition of cadaver mobility in Iguana and likely in other tetrapods.

On vision in birds: coordination of head-bobbing and gait stabilises vertical head position in quail

IntroductionHead-bobbing in birds is a conspicuous behaviour related to vision comprising a hold phase and a thrust phase. The timing of these phases has been shown in many birds, including quail, to be coordinated with footfall during locomotion. We were interested in the biomechanics behind this phenomenon. During terrestrial locomotion in birds, the trunk is subjected to gait-specific vertical oscillations. Without compensation, these vertical oscillations conflict with the demands of vision (i.e., a vertically stable head position). We tested the hypothesis that the coordination between head-bobbing and trunk movement is a means of reconciling the conflicting demands of vision and locomotion which should thus vary according to gait.ResultsSignificant differences in the timing of head-bobbing were found between gaits. The thrust phase was initiated just prior to the double support phase in walking (vaulting) trials, whereas in running (bouncing) trials, thrust started around midstance. Altering the timing of head-trunk-coordination in simulations showed that the timing naturally favoured by birds minimizes the vertical displacement of the head. When using a bouncing gait the timing of head bobbing had a compensatory effect on the fluctuation of the potential energy of the bird’s centre of mass.ConclusionThe results are consistent with expectations based on the vertical trunk fluctuations observed in biomechanical models of vaulting and bouncing locomotion. The timing of the head-bobbing behaviour naturally favoured by quail benefits vision during vaulting and bouncing gaits and potentially helps reducing the mechanical cost associated with head bobbing when using a bouncing gait.

Planar covariation of limb elevation angles during bipedal locomotion in common quails ( Coturnix coturnix )

In human bipedal walking, temporal changes in the elevation angle of the thigh, shank and foot segments covary to form a regular loop within a single plane in three-dimensional space. In this study, we quantified the planar covariation of limb elevation angles during bipedal locomotion in common quails to test whether the degree of planarity and the orientation of the covariance plane differ between birds, humans and Japanese macaques as reported in published accounts. Five quails locomoted on a treadmill and were recorded by a lateral X-ray fluoroscopy. The elevation angle of the thigh, shank and foot segments relative to the vertical axis was calculated and compared with published data on human and macaque bipedal locomotion. The results showed that the planar covariation applied to quail bipedal locomotion and planarity was stronger in quails than in humans. The orientation of the covariation plane in quails differed from that in humans, and was more similar to the orientation of the covariation plane in macaques. Although human walking is characterized by vaulting mechanics of the body center of mass, quails and macaques utilize spring-like running mechanics even though the duty factor is >0.5. Therefore, differences in the stance leg mechanics between quails and humans may underlie the difference in the orientation of the covariation plane. The planar covariation of inter-segmental coordination has evolved independently in both avian and human locomotion, despite the different mechanical constraints.

Automated approximation of center of mass position in X-ray sequences of animal locomotion.

A crucial aspect of comparative biomechanical research is the center of mass (CoM) estimation in animal locomotion scenarios. Important applications include the parameter estimation of locomotion models, the discrimination of gaits, or the calculation of mechanical work during locomotion. Several methods exist to approximate the CoM position, e.g. force-plate-based approaches, kinematic approaches, or the reaction board method. However, they all share the drawback of not being suitable for large scale studies, as detailed initial conditions from kinematics are required (force-plates), manual interaction is necessary (kinematic approach), or only static settings can be analyzed (reaction board). For the increasingly popular case of X-ray-based animal locomotion analysis, we present an alternative approach for CoM estimation which overcomes these shortcomings. The main idea is to only use the recorded X-ray images, and to map each pixel to the mass of matter it represents. As a consequence, our approach is surgically noninvasive, independent of animal species and locomotion characteristics, and neither requires prior knowledge nor any kind of user interaction. To assess the quality of our approach, we conducted a comparison to highly accurate reaction board experiments for lapwing and rat cadavers, and achieved an average accuracy of 2.6mm (less than 2% of the animal body length). We additionally verified the practical applicability of the algorithm by comparison to a previously published CoM study which is based on the kinematic method, yielding comparable results.

Multi-view active appearance models for the X-ray based analysis of avian bipedal locomotion

Many fields of research in biology, motion science and robotics depend on the understanding of animal locomotion. Therefore, numerous experiments are performed using high-speed biplanar x-ray acquisition systems which record sequences of walking animals. Until now, the evaluation of these sequences is a very time-consuming task, as human experts have to manually annotate anatomical landmarks in the images. Therefore, an automation of this task at a minimum level of user interaction is worthwhile. However, many difficulties in the data--such as x-ray occlusions or anatomical ambiguities--drastically complicate this problem and require the use of global models. Active Appearance Models (AAMs) are known to be capable of dealing with occlusions, but have problems with ambiguities. We therefore analyze the application of multi-view AAMs in the scenario stated above and show that they can effectively handle uncertainties which can not be dealt with using single-view models. Furthermore, preliminary studies on the tracking performance of human experts indicate that the errors of multi-view AAMs are in the same order of magnitude as in the case of manual tracking.

Ichnology of an Extant Belly-Dragging Lizard—Analogies to Early Reptile Locomotion?

A recently described Erpetopus trackway bearing unusual claw and belly-drag marks ostensibly indicates an obligatory sprawled posture and belly-walk in the locomotion of small captorhinids. Here, the ichnology of the blue-tongued skink (Tiliqua scincoides) is investigated in order to identify features of a trackway produced by a lizard in continuous belly-walk. Comparisons between T. scincoides and Erpetopus tracks tested whether the locomotory pattern observed for T. scincoides resembles that of small captorhinid track makers. Characteristic features of the T. scincoides track include: (1) a belly-dragging mark, (2) claw scratch marks produced during the early stance phase, and (3) claw drag marks produced by the forelimb during the swing phase. Trackway parameters did not correlate with track maker velocity, rendering inference of velocity for belly-dragging track makers problematic. This result was probably caused by increased substrate influence on locomotor speed because of belly contact with the ground. The track characteristics of T. scincoides match those recently described for Erpetopus and thus corroborate the notion of a similar pattern of locomotion for small captorhinids.