Built for speed: strain in the cartilaginous vertebral columns of sharks

In most bony fishes vertebral column strain during locomotion is almost exclusively in the intervertebral joints, and when these joints move there is the potential to store and release strain energy. Since cartilaginous fishes have poorly mineralized vertebral centra, we tested whether the vertebral bodies undergo substantial strain and thus may be sites of energy storage during locomotion. We measured axial strains of the intervertebral joints and vertebrae in vivo and ex vivo to characterize the dynamic behavior of the vertebral column. We used sonomicrometry to directly measure in vivo and in situ strains of intervertebral joints and vertebrae of Squalus acanthias swimming in a flume. For ex vivo measurements, we used a materials testing system to dynamically bend segments of vertebral column at frequencies ranging from 0.25 to 1.00 Hz and a range of physiologically relevant curvatures, which were determined using a kinematic analysis. The vertebral centra of S. acanthias undergo strain during in vivo volitional movements as well as in situ passive movements. Moreover, when isolated segments of vertebral column were tested during mechanical bending, we measured the same magnitudes of strain. These data support our hypothesis that vertebral column strain in lateral bending is not limited to the intervertebral joints. In histological sections, we found that the vertebral column of S. acanthias has an intracentral canal that is open and covered with a velum layer. An open intracentral canal may indicate that the centra are acting as tunics around some sections of a hydrostat, effectively stiffening the vertebral column. These data suggest that the entire vertebral column of sharks, both joints and centra, is mechanically engaged as a dynamic spring during locomotion.     

Kinematics of different types of locomotor movements in the deafferented rat

The kinematics of rat hindlimb movements were assessed and compared pre- and post-deafferentation during swimming, forelimb treadmill locomotion plus hindlimb swimming motion, and walking using all four limbs. All types of locomotion were characterized by an increase in the frequency of locomotor rhythm and reduced amplitude of motion at the hindlimb joints following deafferentation. The reduced change observed in the angle of the coxofemoral joint, indicative of a horizontal component in locomotor motion, was mainly brought about by less marked extension. This would confirm evidence indicating that increased load on the extremities, with its ensuing naturally-occurring afferent outflow, is accompanied by a reduced locomotor motion rate and a rise in the amplitude of the latter due to intensified extension of the limb. The increased forward carriage of the hind limb seen during the transition to four-legged locomotion persisted after deafferentation; this may be considered a sign of coordination amongst the limbs. Deafferentation led to a reduction in the MEG of muscle activity, which was found to be lowest in swimming and highest during walking. The role of the afferent inflow in shaping different types of locomotor motion is evaluated.A. A. Bogomolets Institute of Physiology, Academy of Sciences of the Ukrainian SSR, Kiev. Translated from Neirofiziologiya, Vol. 19, No. 4, pp. 520–525, July–August, 1987.     

Moment arms of the human neck muscles in flexion, bending and rotation

There is a paucity of data available for the moment arms of the muscles of the human neck. The objective of the present study was to measure the moment arms of the major cervical spine muscles in vitro. Experiments were performed on five fresh-frozen human head-neck specimens using a custom-designed robotic spine testing apparatus. The testing apparatus replicated flexion-extension, lateral bending and axial rotation of each individual intervertebral joint in the cervical spine while all other joints were kept immobile. The tendon excursion method was used to measure the moment arms of 30 muscle sub-regions involving 13 major muscles of the neck about all three axes of rotation of each joint for the neutral position of the cervical spine. Significant differences in the moment arm were observed across sub-regions of individual muscles and across the intervertebral joints spanned by each muscle (p<0.05). Overall, muscle moment arms were larger in flexion-extension and lateral bending than in axial rotation, and most muscles had prominent moment arms in at least 2 out of the 3 joint motions investigated. This study emphasizes the importance of detailed representation of a muscle's architecture in prediction of its torque capacity about the individual joints of the cervical spine. The dataset produced may be useful in developing and validating computational models of the human neck.     

A mathematical model of hind-limb control in cats when walking backward

The “walking backward” mode was achieved within a single model of cat hind-limb locomotion with the balance maintenance only due to a change in the controlling actions (in addition to the “forward walking” mode). The skeletal part of the model contains the spine, pelvis, and two limbs consisting of the thigh, shin, and foot. The hip joint and spine mount in the thoracic region have three degrees of freedom; the knee and ankle joints have one degree of freedom. The pelvis is rigidly connected to the spine. Control is performed by model muscles (flexors and extensors of the thigh, shin, and foot). The muscle activation is performed by the effects that are typical for motoneurons that control the muscles. The feet in the support phase touch the treadmill, which moves at a constant speed. The model qualitatively reproduces multiple characteristics of feline movements during forward and backward walking (supporting its validity).     

Segmental Kinematic Coupling of the Human Spinal Column during Locomotion

As one of the most important daily motor activities, human locomotion has been investigated intensively in recent decades. The locomotor functions and mechanics of human lower limbs have become relatively well understood. However, so far our understanding of the motions and functional contributions of the human spine during locomotion is still very poor and simultaneous in-vivo limb and spinal column motion data are scarce. The objective of this study is to investigate the delicate in-vivo kinematic coupling between different functional regions of the human spinal column during locomotion as a stepping stone to explore the locomotor function of the human spine complex. A novel infrared reflective marker cluster system was constrncted using stereophotogrammetry techniques to record the 3D in-vivo geometric shape of the spinal column and the segmental position and orientation of each functional spinal region simultaneously. Gait measurements of normal walking were conducted. The preliminary results show that the spinal column shape changes periodically in the frontal plane during locomotion. The segmental motions of different spinal functional regions appear to be strongly coupled, indicating some synergistic strategy may be employed by the human spinal column to facilitate locomotion. In contrast to traditional medical imaging-based methods, the proposed technique can be used to investigate the dynamic characteristics of the spinal column, hence providing more insight into the functional biomechanics of the human spine.     

The tri-segmented limbs of therian mammals: kinematics, dynamics, and self-stabilization--a review

The evolution of therian mammals is to a large degree marked by changes in their motion systems. One of the decisive transitions has been from the sprawled, bi-segmented to the parasagittal, tri-segmented limb. Here, we review aspects of the tri-segmented limb in locomotion which have been elucidated in our research groups in the last 10 years. First, we report the kinematics of the tri-segmented therian limb from mouse to elephant in order to explore general principles of the therian limb configuration and locomotion. Torques will be reported from a previous paper (Witte et al., 2002. J Exp Biol 205:1339-1353) for a better understanding of the anti-gravity work of all limb joints. The stability of a limb in z-configuration will be explained and its advantage with respect to other potential solutions from modeling will be discussed. Finally, we describe how the emerging concept of self-stability can be explained for a tri-segmented leg template and how it affects the design of the musculoskeletal system and the operation of legs during locomotion. While locomotion has been considered as mainly a control problem in various disciplines, we stress the necessity to reduce control as much as possible. Central control can be cheap if the limbs are "intelligent" by means of their design. Gravity-induced movements and self-stability seem to be energy-saving mechanisms.     

A videofluoroscopy-based tracking algorithm for quantifying the time course of human intervertebral displacements

The motions of individual intervertebral joints can affect spine motion, injury risk, deterioration, pain, treatment strategies, and clinical outcomes. Since standard kinematic methods do not provide precise time-course details about individual vertebrae and intervertebral motions, information that could be useful for scientific advancement and clinical assessment, we developed an iterative template matching algorithm to obtain this data from videofluoroscopy images. To assess the bias of our approach, vertebrae in an intact porcine spine were tracked and compared to the motions of high-contrast markers. To estimate precision under clinical conditions, motions of three human cervical spines were tracked independently ten times and vertebral and intervertebral motions associated with individual trials were compared to corresponding averages. Both tests produced errors in intervertebral angular and shear displacements no greater than 0.4° and 0.055 mm, respectively. When applied to two patient cases, aberrant intervertebral motions in the cervical spine were typically found to correlate with patient-specific anatomical features such as disc height loss and osteophytes. The case studies suggest that intervertebral kinematic time-course data could have value in clinical assessments, lead to broader understanding of how specific anatomical features influence joint motions, and in due course inform clinical treatments.     

Crouched posture and high fulcrum, a principle in the locomotion of small mammals: The example of the rock hyrax (Procavia capensis) (Mammalia: Hyracoidea)

The cineradiographic study of the locomotion of the rock hyrax (Procavia capensis) and the functional interpretation of its locomotory system, reveals that the main action of proximal segments is combined with flexed position and low movements of limb joints. This observation can be applied to the locomotion of other small mammals. In the forelimb, scapular rotation and translation account for more than 60% of step length. Effective shoulder joint movements are mostly restricted to less than 20°, and elbow movements range mainly between 20°-50°. The detachment of the shoulder girdle of therian mammals from the axial skeleton, and development of a supraspinous fossa, are correlated with movements at a high scapular fulcrum. Movements at such a high fulcrum are in interdependency with a crouched posture. Only flexed limbs can act as shock absorbers and prevent vertical changes in the center of gravity. Basic differences in forelimb movements exist between larger primates (humeral retraction) and smaller mammals (scapula retraction). In the hyrax, propulsion is due mainly to hip joint movements in symmetrical gaits, but sagittal lumbar spine movements play the dominant role at in-phase gaits. Joint and muscular anatomy, especially of the shoulder region, are discussed in view of the kinematic data.     

The equine neck and its function during movement and locomotion

During both locomotion and body movements at stance, the head and neck of the horse are a major craniocaudal and lateral balancing mechanism employing input from the visual, vestibular and proprioceptive systems. The function of the equine neck has recently become the focus of several research groups; this is probably also feeding on an increase of interest in the equine neck in equestrian sports, with a controversial discussion of specific neck positions such as maximum head and neck flexion. The aim of this review is to offer an overview of new findings on the structures and functions of the equine neck, illustrating their interplay. The movement of the neck is based on intervertebral motion, but it is also an integral part of locomotion; this is illustrated by the different neck conformations in the breeds of horses used for various types of work. The considerable effect of the neck movement and posture onto the whole trunk and even the limbs is transmitted via bony, ligamentous and muscular structures. Also, the fact that the neck position can easily be influenced by the rider and/or by the employment of training aids makes it an important avenue for training of new movements of the neck as well as the whole horse. Additionally, the neck position also affects the cervical spinal cord as well as the roots of the spinal nerves; besides the commonly encountered long-term neurological effects of cervical vertebral disorders, short-term changes of neural and muscular function have also been identified in the maximum flexion of the cranial neck and head position. During locomotion, the neck stores elastic energy within the passive tissues such as ligaments, joint capsules and fasciae. For adequate stabilisation, additional muscle activity is necessary; this is learned and requires constant muscle training as it is essential to prevent excessive wear and tear on the vertebral joints and also repetitive or single trauma to the spinal nerves and the spinal cord. The capability for this stabilisation decreases with age in the majority of horses due to changes in muscle tissue, muscle coordination and consequently muscle strength.     

Effect of a pedicle-screw-based motion preservation system on lumbar spine biomechanics: A probabilistic finite element study with subsequent sensitivity analysis

Pedicle-screw-based motion preservation systems are often used to support a slightly degenerated disc. Such implants are intended to reduce intradiscal pressure and facet joints forces, while having a minimal effect on the motion patterns.In a probabilistic finite element study with subsequent sensitivity analysis, the effects of 10 input parameters, such as elastic modulus and diameter of the elastic rod, distraction of the segment, level of bridged segments, etc. on the output parameters intervertebral rotations, intradiscal pressures, and facet joint forces were determined. A validated finite element model of the lumbar spine was employed. Probabilistic studies were performed for seven loading cases: upright standing, flexion, extension, left and right lateral bending and left and right axial rotation.The simulations show that intervertebral rotation angles, intradiscal pressures and facet joint forces are in most cases reduced by a motion preservation system. The influence on intradiscal pressure is small, except in extension. For many input parameter combinations, the values for intervertebral rotations and facet joint forces are very low, which indicates that the implant is too stiff in these cases. The output parameters are affected most by the following input parameters: loading case, elastic modulus and diameter of the elastic rod, distraction of the segment, and angular rigidity of the connection between screws and rod.The designated functions of a motion preservation system can best be achieved when the longitudinal rod has a low stiffness, and when the connection between rod and pedicle screws is rigid.     

Relationship between lordosis and the position of the centre of reaction of the spinal disc

Whenever we stand upright in apparent static equilibrium, we are, in fact, continuously making minor adjustments in order to maintain our balance. For each intervertebral joint, a point must exist at which all moments applied to the joint are continually and dynamically balanced. This point, known as the centre of reaction, is a mathematical invention necessary to perform analyses of spinal motion, but which need not be associated with any real anatomical structure.As the spine flexes and extends, this centre is expected to move; where it moves and the rationale for its motion is worthy of enquiry. In this paper, we propose that the centre of reaction remains confined to the nucleus of the disc, but only if one simple but crucial assumption is made; that the motion of the spine and control of its musculature maintain a minimum and equal stress at each intervertebral joint. This is a simple hypothesis which imposes a very specific relationship between lordosis and the centre of reaction. We investigate this relationship and its consequences on the teaching of lifting.The impossibility of designing experiments adequately to verify this hypothesis prevents in vivo verification, and, therefore, the model's verification must be made through the inferred consequences. For example, the capability of correctly predicting physiological responses of the musculoskeletal system is an indication of the validity of a model; however, this is not universally accepted. In this particular case, additional experimental data are available in the form of the locus of the centre of rotation of a vertebra vis-à-vis its lower neighbour as the spine flexes and extends.It is instructive to compare the predicted locus of the centre of reaction to experimentally determined locus of the centre of rotation; more than just coincidental similarities are found.     

Three-dimensional static modeling of the lumbar spine

This paper presents three-dimensional static modeling of the human lumbar spine to be used in the formation of anatomically-correct movement patterns for a fully cable-actuated robotic lumbar spine which can mimic in vivo human lumbar spine movements to provide better hands-on training for medical students. The mathematical model incorporates five lumbar vertebrae between the first lumbar vertebra and the sacrum, with dimensions of an average adult human spine. The vertebrae are connected to each other by elastic elements, torsional springs and a spherical joint located at the inferoposterior corner in the mid-sagittal plane of the vertebral body. Elastic elements represent the ligaments that surround the facet joints and the torsional springs represent the collective effect of intervertebral disc which plays a major role in balancing torsional load during upper body motion and the remaining ligaments that support the spinal column. The elastic elements and torsional springs are considered to be nonlinear. The nonlinear stiffness constants for six motion types were solved using a multiobjective optimization technique. The quantitative comparison between the angles of rotations predicted by the proposed model and in the experimental data confirmed that the model yields angles of rotation close to the experimental data. The main contribution is that the new model can be used for all motions while the experimental data was only obtained at discrete measurement points.     

Function of the spine

In spite of the considerable effort which has been invested in attempts to understand the mechanism of human spines, substantial controversy remains, particularly in connection with assumptions which have to be made by those engaged in biological modelling.The hypothesis presented here is that the living joint has stress sensors driving a feedback mechanism, an arrangement which could react to imposed loads by modifying muscular action in such a way as to minimize stress at the joints and therefore the risk of injury. A theory of this kind gives an image of the spine not in terms of a spatial picture, as would a CAT scan, but in terms of stresses, forces and moments acting at the intervertebral joints. Calculations show that the erectores spinae alone cannot support more than about 50 kg; there must be some other mechanism to explain man's ability substantially to exceed that load.It is suggested that the interaction between the erectores spinae and the abdominals are of fundamental importance in the function of the spine; how they are co-ordinated during the lifting of weights is examined in detail. The theory resulting from this hypothesis is used to relate spinal injury and an injured subject's posture and behaviour.A mathematical formulation permits an objective evaluation of the spine, and a procedure for determining an automatic diagnosis of lumbar spine disabilities is proposed.     

Mechanics of torque generation during quadrupedal arboreal locomotion

Quadrupedal animals moving on arboreal substrates face unique challenges to maintain stability. The torque generated by the limbs around the long axis of a branch during locomotion may clarify how the animals remain stable on arboreal supports. We sought to determine what strategy gray short-tailed opossums (Monodelphis domestica) use to exert torque and avoid toppling. The opossums moved across a branch trackway about half the diameter of their bodies. Part of the trackway was instrumented to measure substrate reaction forces and torque around the long axis of the branch. Kinematic analysis was used to estimate the center of pressure of the manus and pes; from center of pressure and vertical and mediolateral forces, the torque generated by substrate reaction forces versus muscular effort could be determined. Forelimbs generated significantly greater torque than hindlimbs, which is probably explained by the greater weight-bearing role of the forelimbs. Fore- and hindlimbs generated torque in opposite directions because contralateral fore- and hindlimbs typically contacted the branch. Torque generated by muscular effort, however, was often in the same direction in both fore- and hindlimbs. The muscle-generated torque is likely the result of mediolateral movement of the center of mass caused by mediolateral undulation of the torso. These results bear an important implication for the study of arboreal locomotion: center of mass dynamics are at least as important as static positions. M. domestica is a good representative for a primitive mammal, and comparisons with arboreal specialists will shed light on how proficient arboreal locomotion evolved.     

Locomotion Generation and Motion Library Design for an Anguilliform Robotic Fish

In this paper, modeling, locomotion generation, motion library design and path planning for a real prototype of an Anguilliform robotic fish are presented. The robotic fish consists of four links and three joints, and the driving forces are the torques applied to the joints. Considering kinematic constraints and hydrodynamic forces, Lagrangian formulation is used to obtain the dynamic model of the fish. Using this model, three major locomotion patterns of Anguilliform fish, including forward locomotion, backward locomotion and turning locomotion are investigated. It is found that the fish exhibits different locomotion patterns by giving different reference joint angles, such as adding reversed phase difference, or adding deflections to the original reference angles. The results are validated by both simulations and experiments. Furthermore, the relations among the speed of the fish, angular frequency, undulation amplitude, phase difference, as well as the relationship between the turning radius and deflection angle are investigated. These relations provide an elaborated motion library that can be used for motion planning of the robotic fish.     

Hopping and swimming in the leopard frog,Rana pipiens: I. Step cycles and kinematics

This study presents a model for the step cycle patterns used during both hopping and swimming by the leopard frog, Rana pipiens. The two behaviors are essentially similar in movement pattern and in the ways they are modified from quadrupedal gaits. In hopping, there is marked hind limb extension throughout stance. The swing begins with a suspension equivalent to the leap that occurs in a galloping or bounding quadruped. Following suspension, as the frog descends from the apex of its leap, the hind limbs remain posterior and in line with the spine while they flex. Near the end of flexion, there is a rapid downward rotation of the hindquarters to bring the hind feet underneath the body. This movement utilizes the planted forelimb as a pivot. A similar pattern of movement occurs in swimming; the stance (propulsion) phase involves extension at all hind limb joints. The swing (recovery) phase begins with the hind feet fully extended and includes a protracted gliding phase, equivalent to the suspension in the hop. The hind limb then recovers to its initial position during a flexion phase. Since there is no landing and the hind limbs remain lateral rather than ventral to the pelvis, less flexion occurs in the spine or the limb joints. In both behaviors, the extensor muscles of hip (M. semimembranosus), knee (M. cruralis), and ankle (M. plantaris longus) achieve their longest lengths, when they likely can produce near maximal force, at the beginning of extension. All three muscles shorten during extension, but, because they are multiple-joint muscles, the amount of shortening is relatively small (≈ 15%). Hopping and swimming in frogs are comparable asymmetrical gaits with the same relative contact intervals (25% of stride). The step cycles in both gaits are modified from quadrupedal locomotion in the same ways: by 1) loss of knee and ankle extension toward the ground prior to landing (or end of flexion in swimming), 2) loss of a yield phase on landing (or end of flexion in swimming), and 3) inclusion of extended suspensions in both gaits. © 1996 Wiley-Liss, Inc.     

In vivo three-dimensional intervertebral kinematics of the subaxial cervical spine during seated axial rotation and lateral bending via a fluoroscopy-to-CT registration approach

Accurate measurement of the coupled intervertebral motions is helpful for understanding the etiology and diagnosis of relevant diseases, and for assessing the subsequent treatment. No study has reported the in vivo, dynamic and three-dimensional (3D) intervertebral motion of the cervical spine during active axial rotation (AR) and lateral bending (LB) in the sitting position. The current study fills the gap by measuring the coupled intervertebral motions of the subaxial cervical spine in ten asymptomatic young adults in an upright sitting position during active head LB and AR using a volumetric model-based 2D-to-3D registration method via biplane fluoroscopy. Subject-specific models of the individual vertebrae were derived from each subject’s CT data and were registered to the fluoroscopic images for determining the 3D poses of the subaxial vertebrae that were used to obtain the intervertebral kinematics. The averaged ranges of motion to one side (ROM) during AR at C3/C4, C4/C5, C5/C6, and C6/C7 were 4.2°, 4.6°, 3.0° and 1.3°, respectively. The corresponding values were 6.4°, 5.2°, 6.1° and 6.1° during LB. Intervertebral LB (ILB) played an important role in both AR and LB tasks of the cervical spine, experiencing greater ROM than intervertebral AR (IAR) (ratio of coupled motion (IAR/ILB): 0.23–0.75 in LB, 0.34–0.95 in AR). Compared to the AR task, the ranges of ILB during the LB task were significantly greater at C5/6 (p=0.008) and C6/7 (p=0.001) but the range of IAR was significantly smaller at C4/5 (p=0.02), leading to significantly smaller ratios of coupled motions at C4/5 (p=0.0013), C5/6 (p<0.001) and C6/7 (p=0.0037). The observed coupling characteristics of the intervertebral kinematics were different from those in previous studies under discrete static conditions in a supine position without weight-bearing, suggesting that the testing conditions likely affect the kinematics of the subaxial cervical spine. While C1 and C2 were not included owing to technical limitations, the current results nonetheless provide baseline data of the intervertebral motion of the subaxial cervical spine in asymptomatic young subjects under physiological conditions, which may be helpful for further investigations into spine biomechanics.     

Validation of single-segment and three-segment spinal models used to represent lumbar flexion

Changes in spinal posture between the erect and flexed positions were calculated using angular measurements from lateral photographs and radiographs of ten adult male subjects. For photographic measurements, the thoracolumbar vertebral column was modelled as either a single segment or as three segments. In the three-segment model, there was a non-significant correlation between the decrease in lumbar concavity and intervertebral motion. In addition, there was a non-significant negative correlation between the increase in thoracic convexity and lumbar motion determined radiographically. In the single-segment model, the decrease in angulation between the thoracolumbar spine and pelvis was a good representation of lumbar spine flexion as determined by the mean lumbar intervertebral angular change. Therefore, modelling the thoracolumbar vertebral column as a single segment allowed better estimation of lumbar intervertebral angular change during flexion than a three-segment model. The results indicate that large range dynamic motion of the lumbar vertebral column can be represented using photographic analysis of the positions of three easily identified anatomical landmarks: the anterior superior iliac spine, posterior superior iliac spine and the spinous process of the first thoracic vertebra.     

Interaction torque contributes to planar reaching at slow speed

Background

How the central nervous system (CNS) organizes the joint dynamics for multi-joint movement is a complex problem, because of the passive interaction among segmental movements. Previous studies have demonstrated that the CNS predictively compensates for interaction torque (INT) which is arising from the movement of the adjacent joints. However, most of these studies have mainly examined quick movements, presumably because the current belief is that the effects of INT are not significant at slow speeds. The functional contribution of INT for multijoint movements performed in various speeds is still unclear. The purpose of this study was to examine the contribution of INT to a planer reaching in a wide range of motion speeds for healthy subjects.

Methods

Subjects performed reaching movements toward five targets under three different speed conditions. Joint position data were recorded using a 3-D motion analysis device (50 Hz). Torque components, muscle torque (MUS), interaction torque (INT), gravity torque (G), and net torque (NET) were calculated by solving the dynamic equations for the shoulder and elbow. NET at a joint which produces the joint kinematics will be an algebraic sum of torque components; NET = MUS - G - INT. Dynamic muscle torque (DMUS = MUS-G) was also calculated. Contributions of INT impulse and DMUS impulse to NET impulse were examined.

Results

The relative contribution of INT to NET was not dependent on speed for both joints at every target. INT was additive (same direction) to DMUS at the shoulder joint, while in the elbow DMUS counteracted (opposed to) INT. The trajectory of reach was linear and two-joint movements were coordinated with a specific combination at each target, regardless of motion speed. However, DMUS at the elbow was opposed to the direction of elbow movement, and its magnitude varied from trial to trial in order to compensate for the variability of INT.

Conclusion

Interaction torque was important at slow speeds. Muscle torques at the two joints were not directly related to each other to produce coordinated joint movement during a reach. These results support Bernstein's idea that coordinated movement is not completely determined by motor command in multi-joint motion. Based on the data presented in this study and the work of others, a model for the connection between joint torques (muscle and passive torques including interaction torque) and joint coordination is proposed.     

Bridging “Romer’s Gap”: Limb Mechanics of an Extant Belly-Dragging Lizard Inform Debate on Tetrapod Locomotion During the Early Carboniferous

Devonian stem tetrapods are thought to have used ‘crutching’ on land, a belly-dragging form of synchronous forelimb action-powered locomotion. During the Early Carboniferous, early tetrapods underwent rapid radiation, and the terrestrial locomotion of crown-group node tetrapods is believed to have been hindlimb-powered and ‘raised’, involving symmetrical gaits similar to those used by modern salamanders. The fossil record over this period of evolutionary transition is remarkably poor (Romer’s Gap), but we hypothesize a phase of belly-dragging sprawling locomotion combined with symmetrical gaits. Since belly-dragging sprawling locomotion has differing functional demands from ‘raised’ sprawling locomotion, we studied the limb mechanics of the extant belly-dragging blue-tongued skink. We used X-ray reconstruction of moving morphology to quantify the three-dimensional kinematic components, and simultaneously recorded single limb substrate reaction forces (SRF) in order to calculate SRF moment arms and the external moments acting on the proximal limb joints. In the hindlimbs, stylopodal long-axis rotation is more emphasized than in the forelimbs, and much greater vertical and propulsive forces are exerted. The SRF moment arm acting on the shoulder is at a local minimum at the instant of peak force. The hindlimbs display patterns that more closely resemble ‘raised’ sprawling species. External moment at the shoulder of the skink is smaller than in ‘raised’ sprawlers. We propose an evolutionary scenario in which the locomotor mechanics of belly-dragging early tetrapods were gradually modified towards hindlimb-powered, raised terrestrial locomotion with symmetrical gait. In accordance with the view that limb evolution was an exaptation for terrestrial locomotion, the kinematic pattern of the limbs for the generation of propulsion preceded, in our scenario, the evolution of permanent body weight support.