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.     

The m. caudifemoralis longus and its relationship to caudal autotomy and locomotion in lizards (Reptilia: Sauna)

Although the phenomenon of tail autotomy has traditionally been viewed in a purely adaptive light, functional constraints imposed by the locomotor system appear to have influenced the presence and extent of autotomy in lizards. Them. caudifemoralis longus is an unsegmented hind limb retractor that originates from the caudal vertebrae. It does not participate in autotomy and thus limits the proximal position of autotomic septa. Variation in the extent of the m. caudifemoralis is correlated with locomotor type. The muscle is large and originates from a long series of caudal vertebrae in fast moving lizards with powerful limb retraction, as exemplified by taxa capable of bipedal running. In slower lizards with sprawling postures, such as geckos, the m. caudifemoralis is small and restricted to the first few postsacral vertebrae. Autotomy is typically restricted or absent in the former lizards, while in the latter only the most proximal vertebrae are incapable of autotomy. In the evolution of existing patterns of caudal autotomy, functional demands intrinsic to the tail may be subservient to locomotor constraints imposed on the tail base by the m. caudifemoralis longus .     

Effects of Microhabitat‐Dependent Predation Risk on Vigilance during Intermittent Locomotion in Psammodromus algirus Lizards

Animals should be able to adjust their behavior by tracking changes in predation risk level continuously. Many animals show a pattern of intermittent locomotion with short pauses that may increase detection and vigilance of predators. These locomotor patterns may depend on the microhabitat structure, which affect predation risk levels. We examined in detail in the laboratory the characteristics of spontaneous locomotion, scanning behavior, and the escape performance of Psammodromus algirus lizards moving in two different microhabitats (leaf litter patches and open sand areas). Results showed that in leaf litter, lizards moved at slower speed and had shorter bursts of locomotion both in distance and duration, than in sand substrates. This locomotor pattern allowed lizards to increase scanning rate and total time spent in vigilance behavior. When lizards were forced to flee, they escaped to longer distances and during more time in open sand areas, but lizards were able to attain similar escape speed in the two substrates. Lizards may be able to compensate the cost of moving between different microhabitats with different predation risk by behaviorally changing their locomotor and vigilance patterns. However, complex interactions between the visibility of lizards to predators and the ability of lizards to detect predators, together with the need of attending simultaneously to other conflicting demands, may lead to apparently non‐intuitive solutions in locomotor patterns and the rate of vigilance behavior.     

The relationship between limb morphology, kinematics, and force during running: the evolution of locomotor dynamics in lizards

Terrestrial locomotion occurs via the hierarchical links between morphology, kinematics, force, and center-of-mass mechanics. In a phylogenetically broad sample of seven lizard species, we show that morphological variation drives kinematic variation, which, in turn, drives force variation. Species with short limbs use a short stride–high frequency strategy when running at steady-speed and to change speeds. This link between morphology and kinematics results in relatively small vertical forces during the support phase of the stride cycle. Conversely, species with long limbs use a long stride–low frequency strategy, resulting in large vertical forces during the support phase. In view of these findings, we suggest that limb length may predict locomotor energetics in lizards because energetics are largely determined by vertical forces and stride frequency. Additionally, we propose an energetic trade-off with both long- and short-limbed species paying the most energy to move, whereas intermediate-limbed species move using less energy. Finally, when these traits are mapped onto a lizard phylogeny, we show that locomotor functional morphology exhibits both deep phylogenetic effects and contemporary patterns of evolutionary convergence. Overall, the present study provides a foundation for testing hypotheses regarding the integration and evolution of functional traits in lizards and animals in general.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 97 , 634–651.     

Sprawling locomotion in the lizard Sceloporus clarkii: the effects of speed on gait, hindlimb kinematics, and axial bending during walking

Although the hindlimb is widely considered to provide the propulsive force in lizard locomotion, no study to date has analysed kinematic patterns of hindlimb movements for more than one stride for a single individual and no study has considered limb and axial kinematics together. In this study, kinematic data from several individuals of the Sceloporus clarkii are used to describe the movement patterns of the axial skeleton and hindlimb at different speeds, to analyse how kinematics change with speed, and to compare and contrast these findings with the inferred effects of speed cited in the literature. Angular limb movements and axial bending patterns (standing wave with nodes on the girdles) did not change with speed. Only the relative speed of retracting the femur and flexing the knee during limb retraction changes with speed. Based on these data and similar results from a recent study of salamanders, it appears that, over a range of speeds involving a walking trot, sprawling vertebrates increase speed by simply retracting the femur relatively faster, thus this simple functional adjustment may be a general mechanism to increase speed in tetrapods. The demonstration that femoral retraction alone is the major speed effector in Sceloporus clarkii lends strong functional support to ecomorphological implications of limb length (and especially femur length and caudifemoralis size) in locomotory ecology and performance in phrynosomatid lizards. It also lends support to inferences about the caudifemoralis muscle as a preadaptation to terrestrial locomotion and as a key innovation in the evolution of bipedalism.     

ALTERNATE PATHWAYS OF BODY SHAPE EVOLUTION TRANSLATE INTO COMMON PATTERNS OF LOCOMOTOR EVOLUTION IN TWO CLADES OF LIZARDS

Body shape has a fundamental impact on organismal function, but it is unknown how functional morphology and locomotor performance and kinematics relate across a diverse array of body shapes. We showed that although patterns of body shape evolution differed considerably between lizards of the Phrynosomatinae and Lerista, patterns of locomotor evolution coincided between clades. Specifically, we found that the phrynosomatines evolved a stocky phenotype through body widening and limb shortening, whereas Lerista evolved elongation through body lengthening and limb shortening. In both clades, relative limb length played a key role in locomotor evolution and kinematic strategies, with long‐limbed species moving faster and taking longer strides. In Lerista, the body axis also influenced locomotor evolution. Similar patterns of locomotor evolution were likely due to constraints on how the body can move. However, these common patterns of locomotor evolution between the two clades resulted in different kinematic strategies and levels of performance among species because of their morphological differences. Furthermore, we found no evidence that distinct body shapes are adaptations to different substrates, as locomotor kinematics did not change on loose or solid substrates. Our findings illustrate the importance of studying kinematics to understand the mechanisms of locomotor evolution and phenotype‐function relationships.     

Selection,Morphological Integration,and Strepsirrhine Locomotor Adaptations

Clades with taxa that have multiple locomotor adaptations represent a direct way to test the relationship between adaptation and integration. If integration is influenced by functional requirements, integration should be most apparent where selection is strongest and less evident where selection has been relaxed. If integration is primarily regulated by genetic constraints, integration should be present irrespective of selection pressures. Here we use patterns of integration in the strepsirrhine fore- and hind limbs as a test case. Strepsirrhine locomotion is relatively well-studied, and there are multiple clades that share different locomotor modes. We found that quadrupeds have greater limb integration than vertical leapers. These results suggest that variation can be expressed if selection for integration is relaxed. However, an unexpected pattern was revealed, in which there appears to be some broader regulatory mechanism controlling overall limb integration. Our tests identified a strong correlation between integration of the forelimb and integration of the hind limb. This broader mechanism may be evidence of the primitive genetic control of limb integration.     

Effect of locomotor approach on feeding kinematics in the green anole (Anolis carolinensis)

Squamates are well-known models for studying to examine locomotor and feeding behaviors in tetrapods, but studies that integrate both behavioral activities remain scarce. Anolis lizards are a classical lineage to study the evolutionary relationships between locomotor behavior and complex structural features of the habitat. Here, we analyzed prey-capture behavior in one representative arboreal predator, Anolis carolinensis, to demonstrate the functional links between locomotor strategies and the kinematics of feeding. A. carolinensis uses two strategies to catch living insects on perches: Head-Up Capture and Jump Capture. In both cases, lizards use lingual prehension to capture the prey and the kinematic patterns of the trophic apparatus are not significantly influenced by the selected strategies. Therefore, to capture one prey type, movements of the trophic structures are highly fixed and A. carolinensis modulates the locomotor pattern to exploit the environment. Predation behavior in A. carolinensis integrates two different behavioral patterns: locomotor plasticity of prey-approach and biomechanical stereotypy of tongue prehension to successfully capture the prey.     

Pendular mechanics and the kinematics and energetics of brachiating locomotion

Because brachiating locomotion is characterized by a pattern of swinging movements, brachiation has often been analogized to pendular motion, and aspects of the mechanics of pendular systems have been used to provide insight into both energetic and structural design aspects of this locomotor mode. However, there are several limitations to this approach. First, the motions of brachiating animals only approximate pendular motion, and therefore the energetics of these two systems are only roughly comparable. Second, the kinematic similarity between brachiation and pendular motion will be maximal at only one velocity, and the correspondence will be even less at greater or lesser speeds. Third, all forms of terrestrial locomotion that involve the use of limbs incorporate elements of pendular systems, and therefore brachiation is not unusual in this respect. Finally, it has been suggested that the mechanics of pendular motion will constrain the maximum attainable body size of brachiating animals and that this mechanical situation explains the lack of brachiating primates of greater than 30-kg body size; the present analysis provides evidence that the constraints on body size are far less strict than previously indicated and that extrinsic factors such as the geometry of the forest environment are more likely to dictate maximum body size for brachiators.     

Comparative aspects of gait, scaling and mechanics in mammals.

In phylogenetically based systematics, Mammalia is the nomenclatural term which designates the clade stemming from the most recent common ancestry of monotremes and theria [, Sys. Biol. 43 (1994) 497]. Considering that locomotor performance is a prevalent function to provide the necessary conditions to survive and transmit genes, it may be questioned if the diverse types of locomotion exhibited by extant mammals could have played a role in their evolution, or have only followed it. We may look after the structural and behavioural features which are involved in mammal locomotion compared to other tetrapods and test if they fit with the proposed phylogeny. Several factors may be checked: scaling effect in relation to gravitational constraints; geometrical distribution of masses in the body, and relative mechanical role of the limbs in the production of the external forces necessary to forward motion. Classically, it was thought that the fastest gaits used by terrestrial mammals were based upon a unique kind of limb motion co-ordination, called asymmetrical gaits, which in turn may be thought to be related to a peculiar neuronal wiring. Kinematic analysis brings an insight to this topic. Is the search for an ancestral mammalian locomotor pattern judicious? Notice the small size of many of the first mammals and their probable locomotor plasticity. (relation between grain size of the elements within the substrate and the organism scale). At a small size, the gravitational constraint is less important, and the distinction between terrestrial and arboreal has probably no sense when the limbs are the principal motor elements. There remains the importance of the geometrical distribution of body elements, the proportions of the limbs and of the head-neck complex, the tail merely as an appendix, a set of factors which may have generated the frame of constraints within which diverse locomotor modes have evolved.     

Sexual dimorphism in traits related to locomotion: ontogenetic patterns of variation in Podarcis wall lizards

Sexual dimorphism in body size and shape in animals is normally linked to sexual selection mechanisms that modify the morphological properties of each sex. However, sexual dimorphism of ecologically relevant traits may be amplified by natural selection and result in the ecological segregation of both sexes. In the present study, we investigated patterns of sexual dimorphism of morphological traits relevant for locomotion in two lacertid lizards, Podarcis bocagei and Podarcis carbonelli, aiming to identify ontogenetic sources of variation. We analysed trunk and limb variation in relation to total body size, as well as the covariation of different traits, aiming to shed light on the proximate causation of adult sexual dimorphism. We find that, although immatures are generally monomorphic, adult females have a longer trunk, and adult males have longer fore and hind limbs. Both sexes differ substantially with respect to their growth trajectories and relationships between traits, whereas, in some cases, there are signs of morphological constraints delimiting the observed patterns. Because of the direct connection between limb size/shape and locomotor performance, which is relevant both for habitat use and escape from predators, the observed patterns of sexual dimorphism are expected to translate into ecological differences between both sexes. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 99 , 530–543.     

How to climb a tree: lizards accelerate faster,but pause more,when escaping on vertical surfaces

Many species of lizards effectively traverse both two and three‐dimensional habitats. However, few studies have examined maximum locomotor performance on different inclines. Do maximum acceleration and velocity differ on a level and inclined surface? Do lizards pause more on an inclined surface? To address these questions, Sceloporus woodi lizards (N = 12) were run in the laboratory on a level trackway and a vertical tree trunk. This species is known to frequently utilize both vertical and horizontal aspects of its habitat. Average maximum acceleration on the vertical surface exceeded that on the level surface, although average maximum velocity exhibited the opposite pattern. The average number of pauses during level locomotion was lower compared to vertical locomotion. In addition, the average location of the first pause on the level surface was 0.51 m, which is farther than the average for vertical locomotion where the first pause was at 0.35 m. The combination of performance and pause data suggests that the relative lack of pausing during level locomotion allows individuals to reach higher maximum velocities on level surfaces because they accelerate over greater distances. The increased pausing when moving vertically could be a result of high energetic demands of vertical locomotion, or greater microhabitat complexity as a result of branching and/or refuges. The faster acceleration exhibited during vertical locomotion by S. woodi likely offsets the frequent pauses. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 102 , 83–90.     

The Effect of Speed on the Hindlimb Kinematics of the Reeves' Butterfly Lizard,Leiolepis reevesii(Agamidae)

We recorded locomotor performance of Reeves' butterfly lizards(Leiolepis reevesii) on a racetrack and to describe hindlimb kinematic patterns and to evaluate the effect of speed on hindlimb kinematics. The studied lizards predominantly used quadrupedal locomotion at relatively low speeds, but ran bipedally with a digitigrade posture at high speeds. Speed was positively correlated with both stride length and stride frequency, and was negatively correlated with duty factor. Lizards modulated speed probably by a combination of changing frequency and amplitude of limb movements. Within the range of standardized speeds from 50 to 150 cm/s, speed effects on 28 out of a total of 56 kinematic variables were significant. The hip height at footfall increased as speed increased, whereas the amplitude of vertical oscillations of the hip did not vary with speed. The total longitudinal and dorsoventral movements relative to the hip varied with speed for all parts of the limb that were distal to the knee, whereas the lateral movements did not. The knee and ankle angle at footfall varied with speed, but did not at the end of stance. The degree of pelvis rotation during the entire stride cycle did not vary with speed. Our results suggest that pelvic rotation and femoral protraction/retraction have a minor role in modulating speed in L. reevesii.     

Tuataras and salamanders show that walking and running mechanics are ancient features of tetrapod locomotion

The lumbering locomotor behaviours of tuataras and salamanders are the best examples of quadrupedal locomotion of early terrestrial vertebrates. We show they use the same walking (out-of-phase) and running (in-phase) patterns of external mechanical energy fluctuations of the centre-of-mass known in fast moving (cursorial) animals. Thus, walking and running centre-of-mass mechanics have been a feature of tetrapods since quadrupedal locomotion emerged over 400 million years ago. When walking, these sprawling animals save external mechanical energy with the same pendular effectiveness observed in cursorial animals. However, unlike cursorial animals (that change footfall patterns and mechanics with speed), tuataras and salamanders use only diagonal couplet gaits and indifferently change from walking to running mechanics with no significant change in total mechanical energy. Thus, the change from walking to running is not related to speed and the advantage of walking versus running is unclear. Furthermore, lumbering mechanics in primitive tetrapods is reflected in having total mechanical energy driven by potential energy (rather than kinetic energy as in cursorial animals) and relative centre-of-mass displacements an order of magnitude greater than cursorial animals. Thus, large vertical displacements associated with lumbering locomotion in primitive tetrapods may preclude their ability to increase speed.     

Kinematics of the Coordination of Pointing during Locomotion

In natural motor behaviour arm movements, such as pointing or reaching, often need to be coordinated with locomotion. The underlying coordination patterns are largely unexplored, and require the integration of both rhythmic and discrete movement primitives. For the systematic and controlled study of such coordination patterns we have developed a paradigm that combines locomotion on a treadmill with time-controlled pointing to targets in the three-dimensional space, exploiting a virtual reality setup. Participants had to walk at a constant velocity on a treadmill. Synchronized with specific foot events, visual target stimuli were presented that appeared at different spatial locations in front of them. Participants were asked to reach these stimuli within a short time interval after a “go” signal. We analysed the variability patterns of the most relevant joint angles, as well as the time coupling between the time of pointing and different critical timing events in the foot movements. In addition, we applied a new technique for the extraction of movement primitives from kinematic data based on anechoic demixing. We found a modification of the walking pattern as consequence of the arm movement, as well as a modulation of the duration of the reaching movement in dependence of specific foot events. The extraction of kinematic movement primitives from the joint angle trajectories exploiting the new algorithm revealed the existence of two distinct main components accounting, respectively, for the rhythmic and discrete components of the coordinated movement pattern. Summarizing, our study shows a reciprocal pattern of influences between the coordination patterns of reaching and walking. This pattern might be explained by the dynamic interactions between central pattern generators that initiate rhythmic and discrete movements of the lower and upper limbs, and biomechanical factors such as the dynamic gait stability.     

Artificial neural network model for the generation of muscle activation patterns for human locomotion.

Skilled locomotor behaviour requires information from various levels within the central nervous system (CNS). Mathematical models have permitted researchers to simulate various mechanisms in order to understand the organization of the locomotor control system. While it is difficult to adequately characterize the numerous inputs to the locomotor control system, an alternative strategy may be to use a kinematic movement plan to represent the complex inputs to the locomotor control system based on the possibility that the CNS may plan movements at a kinematic level. We propose the use of artificial neural network (ANN) models to represent the transformation of a kinematic plan into the necessary motor patterns. Essentially, kinematic representation of the actual limb movement was used as the input to an ANN model which generated the EMG activity of 8 muscles of the lower limb and trunk. Data from a wide variety of gait conditions was necessary to develop a robust model that could accommodate various environmental conditions encountered during everyday activity. A total of 120 walking strides representing normal walking and ten conditions where the normal gait was modified in terms of cadence, stride length, stance width or required foot clearance. The final network was assessed on its ability to predict the EMG activity on individual walking trials as well as its ability to represent the general activation pattern of a particular gait condition. The predicted EMG patterns closely matched those recorded experimentally, exhibiting the appropriate magnitude and temporal phasing required for each modification. Only 2 of the 96 muscle/gait conditions had RMS errors above 0.10, only 5 muscle/gait conditions exhibited correlations below 0.80 (most were above 0.90) and only 25 muscle/gait conditions deviated outside the normal range of muscle activity for more than 25% of the gait cycle. These results indicate the ability of single network ANNs to represent the transformation between a kinematic movement plan and the necessary muscle activations for normal steady state locomotion but they were also able to generate muscle activation patterns for conditions requiring changes in walking speed, foot placement and foot clearance. The abilities of this type of network have implications towards both the fundamental understanding of the control of locomotion and practical realizations of artificial control systems for use in rehabilitation medicine.     

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.     

An analytical estimation of the energy cost for legged locomotion

Legged locomotion requires the determination of a number of parameters such as stride period, stride length, order of leg movements, leg trajectory, etc. How are these parameters determined? It has been reported that the locomotor patterns of many legged animals exhibit common characteristics, which suggests that there exists a basic strategy for legged locomotion. In this study we derive an equation to estimate the cost of transport for legged locomotion and examine a criterion of the minimization of the transport cost as a candidate of the strategy. The obtained optimal locomotor pattern that minimizes the cost suitably represents many characteristics of the pattern observed in legged animals. This suggests that the locomotor pattern of legged animals is well optimized with regard to the energetic cost. The result also suggests that the existence of specific gait patterns and the phase transition between them could be the result due to optimization; they are induced by the change in the distribution of ground reaction forces for each leg during locomotion.