Patterns of axial and appendicular movements during aquatic walking in the salamander Siren lacertina

Most studies of salamander locomotion have focused either on swimming or terrestrial walking, but some salamanders also use limb-based locomotion while submerged under water (aquatic walking). In this study we used video motion analysis to describe the aquatic walking gait of Siren lacertina, an elongate salamander with reduced forelimbs and no hindlimbs. We found that S. lacertina uses a bipedal-undulatory gait, which combines alternating use of the forelimbs with a traveling undulatory wave. Each forelimb is in contact with the substrate for about 50% of the stride cycle and forelimbs have little temporal overlap in contact intervals. We quantified the relative timing and frequency of limb and tail movements and found that, unlike the terrestrial gaits of most salamanders, axial and appendicular movements are decoupled during aquatic walking. We found no significant relationship between stride frequency and aquatic walking velocity, but we did find a statistically significant relationship between tailbeat frequency and aquatic walking velocity, which suggests that aquatic walking speed is mainly modulated by axial movements. By comparing axial wavespeed and distance traveled per tailbeat during swimming (forelimbs not used) and aquatic walking (forelimbs used), we found lower wavespeed and greater distance traveled per tailbeat during aquatic walking. These findings suggest that the reduced forelimbs of S. lacertina contribute to forward propulsion during aquatic walking.     

Neither season nor sex affects the cost of terrestrial locomotion in a circumpolar diving duck: the common eider (Somateria mollissima)

Locomotion accounts for a significant proportion of the energy budget in birds, and selection is likely to act on its economy, particularly where energy conservation is essential for survival. Birds are capable of different forms of locomotion, such as walking/running, swimming, diving and flying, and adaptations for these affect the energetic cost [cost of locomotion (CoL)] and kinematics of terrestrial locomotion. Furthermore, seasonal changes in climate and photoperiod elicit physiological and behavioural adaptations for survival and reproduction, which also influence energy budget. However, little is understood about how this might affect the CoL. Birds are also known to exhibit sex differences in size, behaviour and physiology; however, sex differences in terrestrial locomotion have only been studied in two cursorially adapted galliform species in which males achieved higher maximum speeds, and in one case had a lower mass-specific CoL than females. Here, using respirometry and high-speed video recordings, we sought to determine whether season and sex would affect the CoL and kinematics of a principally aquatic diving bird: the circumpolar common eider (Somateria mollissima). We demonstrate that eiders are only capable of a walking gait and exhibit no seasonal or sex differences in mass-specific CoL or maximum speed. Despite sharing identical limb morphometrics, the birds exhibited subtle sex differences in kinematic parameters linked to the greater body mass of the males. We suggest that their principally aquatic lifestyle accounts for the observed patterns in their locomotor performance. Furthermore, sex differences in the CoL may only be found in birds in which terrestrial locomotion directly influences male reproductive success.     

Posture, gait and the ecological relevance of locomotor costs and energy-saving mechanisms in tetrapods

A reanalysis of locomotor data from functional, energetic, mechanical and ecological perspectives reveals that limb posture has major effects on limb biomechanics, energy-saving mechanisms and the costs of locomotion. Regressions of data coded by posture (crouched vs. erect) reveal nonlinear patterns in metabolic cost, limb muscle mass, effective mechanical advantage, and stride characteristics. In small crouched animals energy savings from spring and pendular mechanisms are inconsequential and thus the metabolic cost of locomotion is driven by muscle activation costs. Stride frequency appears to be the principal functional parameter related to the decreasing cost of locomotion in crouched animals. By contrast, the shift to erect limb postures invoked a series of correlated effects on the metabolic cost of locomotion: effective mechanical advantage increases, relative muscle masses decrease, metapodial limb segments elongate dramatically (as limbs shift from digitigrade to unguligrade designs) and biological springs increase in size and effectiveness. Each of these factors leads to decreases in the metabolic cost of locomotion in erect forms resulting from real and increasing contributions of pendular savings and spring savings. Comparisons of the relative costs and ecological relevance of different gaits reveal that running is cheaper than walking in smaller animals up to the size of dogs but running is more expensive than walking in horses. Animals do not necessarily use their cheapest gaits for their predominant locomotor activity. Therefore, locomotor costs are driven more by ecological relevance than by the need to optimize locomotor economy.     

Energetics of swimming of a sea turtle.

Young (mean mass 735 g) green turtles (Chelonia mydas) were able to swim in a water channel at sustained speeds between 0-14 and 0-35 m.s-1. Oxygen consumption at rest was was 0-07 l.kg-1.h-1; at maximum swimming speed oxygen consumption was 3-4 times greater than at rest for a given individual. In comparison with other animals of the same body mass the cost of transport for the green turtle (0.186lO2.kg-1.km-1) is less than that for flying birds but greater than that for fish. From drag measurements it was calculated that the aerobic efficiency of swimming was between 1 and 10%; the higher efficiencies were found at the higher swimming speeds. Based upon the drag calculations for young turtles, it is estimated that adult turtles making the round-trip breeding migration between Brazil and Ascension Island (4800 km) would require the equivalent of about 21% of their body mass in fat stores to account for the energetic cost of swimming.     

Application of the mathematics of coupled oscillator systems to the analysis of the neural control of locomotion.

In many animals, the activities of limb motor neurons are rhythmic during locomotion. In some animals it is known that each limb is innervated by a local control center that resides in a discrete portion of the central nervous system. Each local control center is a biological oscillator. Since each limb moves with the same frequency as each other limb and with regulated phase delay with respect to each other limb, then it follows that the local control centers are coupled to one another. The locomotory pattern generator within the central nervous system is therefore a coupled oscillator system. The mathematics of coupled oscillator systems can assist in the construction of a model of the neural pattern generator. This model can be utilized to formulate testable predictions concerning the neural control of locomotion. Experimental data gathered from organisms in several phylums are consistent with the predictions of the model.     

Optimal shape and motion of undulatory swimming organisms

Undulatory swimming animals exhibit diverse ranges of body shapes and motion patterns and are often considered as having superior locomotory performance. The extent to which morphological traits of swimming animals have evolved owing to primarily locomotion considerations is, however, not clear. To shed some light on that question, we present here the optimal shape and motion of undulatory swimming organisms obtained by optimizing locomotive performance measures within the framework of a combined hydrodynamical, structural and novel muscular model. We develop a muscular model for periodic muscle contraction which provides relevant kinematic and energetic quantities required to describe swimming. Using an evolutionary algorithm, we performed a multi-objective optimization for achieving maximum sustained swimming speed U and minimum cost of transport (COT)--two conflicting locomotive performance measures that have been conjectured as likely to increase fitness for survival. Starting from an initial population of random characteristics, our results show that, for a range of size scales, fish-like body shapes and motion indeed emerge when U and COT are optimized. Inherent boundary-layer-dependent allometric scaling between body mass and kinematic and energetic quantities of the optimal populations is observed. The trade-off between U and COT affects the geometry, kinematics and energetics of swimming organisms. Our results are corroborated by empirical data from swimming animals over nine orders of magnitude in size, supporting the notion that optimizing U and COT could be the driving force of evolution in many species.     

Patterns of mechanical energy change in tetrapod gait: pendula, springs and work

Kinematic and center of mass (CoM) mechanical variables used to define terrestrial gaits are compared for various tetrapod species. Kinematic variables (limb phase, duty factor) provide important timing information regarding the neural control and limb coordination of various gaits. Whereas, mechanical variables (potential and kinetic energy relative phase, %Recovery, %Congruity) provide insight into the underlying mechanisms that minimize muscle work and the metabolic cost of locomotion, and also influence neural control strategies. Two basic mechanisms identified by Cavagna et al. (1977. Am J Physiol 233:R243-R261) are used broadly by various bipedal and quadrupedal species. During walking, animals exchange CoM potential energy (PE) with kinetic energy (KE) via an inverted pendulum mechanism to reduce muscle work. During the stance period of running (including trotting, hopping and galloping) gaits, animals convert PE and KE into elastic strain energy in spring elements of the limbs and trunk and regain this energy later during limb support. The bouncing motion of the body on the support limb(s) is well represented by a simple mass-spring system. Limb spring compliance allows the storage and return of elastic energy to reduce muscle work. These two distinct patterns of CoM mechanical energy exchange are fairly well correlated with kinematic distinctions of limb movement patterns associated with gait change. However, in some cases such correlations can be misleading. When running (or trotting) at low speeds many animals lack an aerial period and have limb duty factors that exceed 0.5. Rather than interpreting this as a change of gait, the underlying mechanics of the body's CoM motion indicate no fundamental change in limb movement pattern or CoM dynamics has occurred. Nevertheless, the idealized, distinctive patterns of CoM energy fluctuation predicted by an inverted pendulum for walking and a bouncing mass spring for running are often not clear cut, especially for less cursorial species. When the kinematic and mechanical patterns of a broader diversity of quadrupeds and bipeds are compared, more complex patterns emerge, indicating that some animals may combine walking and running mechanics at intermediate speeds or at very large size. These models also ignore energy costs that are likely associated with the opposing action of limbs that have overlapping support times during walking. A recent model of terrestrial gait (Ruina et al., 2005. J Theor Biol, in press) that treats limb contact with the ground in terms of collisional energy loss indicates that considerable CoM energy can be conserved simply by matching the path of CoM motion perpendicular to limb ground force. This model, coupled with the earlier ones of pendular exchange during walking and mass-spring elastic energy savings during running, provides compelling argument for the view that the legged locomotion of quadrupeds and other terrestrial animals has generally evolved to minimize muscle work during steady level movement.     

Scale Effects between Body Size and Limb Design in Quadrupedal Mammals

Recently the metabolic cost of swinging the limbs has been found to be much greater than previously thought, raising the possibility that limb rotational inertia influences the energetics of locomotion. Larger mammals have a lower mass-specific cost of transport than smaller mammals. The scaling of the mass-specific cost of transport is partly explained by decreasing stride frequency with increasing body size; however, it is unknown if limb rotational inertia also influences the mass-specific cost of transport. Limb length and inertial properties – limb mass, center of mass (COM) position, moment of inertia, radius of gyration, and natural frequency – were measured in 44 species of terrestrial mammals, spanning eight taxonomic orders. Limb length increases disproportionately with body mass via positive allometry (length ∝ body mass^0.40); the positive allometry of limb length may help explain the scaling of the metabolic cost of transport. When scaled against body mass, forelimb inertial properties, apart from mass, scale with positive allometry. Fore- and hindlimb mass scale according to geometric similarity (limb mass ∝ body mass^1.0), as do the remaining hindlimb inertial properties. The positive allometry of limb length is largely the result of absolute differences in limb inertial properties between mammalian subgroups. Though likely detrimental to locomotor costs in large mammals, scale effects in limb inertial properties appear to be concomitant with scale effects in sensorimotor control and locomotor ability in terrestrial mammals. Across mammals, the forelimb''s potential for angular acceleration scales according to geometric similarity, whereas the hindlimb''s potential for angular acceleration scales with positive allometry.     

Locomotion in hatchling leatherback turtles Dermochelys coriacea

Hatchling leatherback turtles can only swim forwards, and employ synchronized beating of the forelimbs whether swimming slowly or quickly. The hind limbs make no contribution to propulsion. Effectively, the hatchlings have two swimming speeds; subsurface and fast (30 cm s^-1) or surfaced and slow (8 cm s^-1). Intermediate velocities are transitory; the hatchlings were never seen to rest without movement, nor did they exhibit gliding of the type seen in green turtles. During fast ('vigorous') swimming, power is developed on both the upstroke and downstroke of the limb cycle. During slow swimming, power is only developed during the upstroke—a consequence of the orientation of the axis of limb beat which is opposite in direction to that of cheloniid sea turtles. Terrestrial locomotion is laboured and features an unstable gait which involves simultaneous movement of all four limbs and forward overbalancing during each limb cycle.     

Allometry of the limb long bones of insectivores and rodents

In an attempt to investigate the relationships between allometry and locomotory adaptations, we studied the long limb bones of 45 species of insectivores and rodents. Animals ranged from a few grams to about 50 kilograms. Diameter and length of the bones and body mass (when known) were recorded. Regressions of diameter to length, diameter to body mass, and length to body mass were calculated by the least-squares and Model II, or major axis, methods. The results obtained do not agree with the predictions of either the theory of geometric similarity or the theory of elastic similarity. The discrepancies could be due to the fact that animals studied exhibit various modes of locomotion. Moreover, the allometric relationships of the different locomotor patterns are better reflected in insectivores and rodents than in other groups of mammals. The use of a single regression analysis seems to be inadequate when the sample includes a large range of body sizes.     

Functional differentiation of trailing and leading forelimbs during locomotion on the ground and on a horizontal branch in the European red squirrel (Sciurus vulgaris, Rodentia)

Mammalian locomotion is characterized by the frequent use of in-phase gaits in which the footfalls of the left and right fore- or hindlimbs are unevenly spaced in time. Although previous studies have identified a functional differentiation between the first limb (trailing limb) and the second limb (leading limb) to touch the ground during terrestrial locomotion, the influence of a horizontal branch on limb function has never been explored. To determine the functional differences between trailing and leading forelimbs during locomotion on the ground and on a horizontal branch, X-ray motion analysis and force measurements were carried out in two European red squirrels (Sciurus vulgaris, Rodentia). The differences observed between trailing and leading forelimbs were minimal during terrestrial locomotion, where both limbs fulfill two functions and go through a shock-absorbing phase followed by a generating phase. During locomotion on a horizontal branch, European red squirrels reduce speed and all substrate reaction forces transmitted may be due to the reduction of vertical oscillation of the center of mass. Further adjustments during locomotion on a horizontal branch differ significantly between trailing and leading forelimbs and include limb flexion, lead intervals, limb protraction and vertical displacement of the scapular pivot. Consequently, trailing and leading forelimbs perform different functions. Trailing forelimbs function primarily as shock-absorbing elements, whereas leading forelimbs are characterized by a high level of stiffness. This functional differentiation indicates that European red squirrels ‘test’ the substrate for stability with the trailing forelimb, while the leading forelimb responds to or counteracts swinging or snapping branches.     

Sensory-evoked turning locomotion in red-eared turtles: kinematic analysis and electromyography

We examined the limb kinematics and motor patterns that underlie sensory-evoked turning locomotion in red-eared turtles. Intact animals were held by a band-clamp in a water-filled tank. Turn-swimming was evoked by slowly rotating turtles to the right or left via a motor connected to the shaft of the band-clamp. Animals executed sustained forward turn-swimming against the direction of the imposed rotation. We recorded video of turn-swimming and computer-analyzed the limb and head movements. In a subset of turtles, we also recorded electromyograms from identified limb muscles. Turning exhibited a stereotyped pattern of (1) coordinated forward swimming in the hindlimb and forelimb on the outer side of the turn, (2) back-paddling in the hindlimb on the inner side, (3) a nearly stationary, “braking” forelimb on the inner side, and (4) neck bending toward the direction of the turn. Reversing the rotation caused animals to switch the direction of their turns and the asymmetric pattern of right and left limb activities. Preliminary evidence suggested that vestibular inputs were sufficient to drive the behavior. Sensory-evoked turning may provide a useful experimental platform to examine the brainstem commands and spinal neural networks that underlie the activation and switching of different locomotor forms.     

Manual digital pressures during knuckle‐walking in chimpanzees (Pan troglodytes)

Considerable attention has been given to hand morphology and function associated with knuckle‐walking in the African apes because of the implications they have for the evolution of bipedalism in early hominins. Knuckle‐walking is associated with a unique suite of musculoskeletal features of the wrist and hand, and numerous studies have hypothesized that these anatomical features are associated with the dynamics of load distribution across the digits during knuckle‐walking. We collected dynamic digital pressures on two chimpanzees during terrestrial and simulated arboreal locomotion. Comparisons were made across substrates, limb positions, hand positions, and age categories. Peak digital pressures were similar on the pole and on the ground but were distributed differently across the digits on each substrate. In young animals, pressure was equally high on digits 2–4 on the ground but higher on digits 3 and 4 on the pole. Older animals experience higher pressures on digits 2 and 3 on the ground. Hand posture (palm‐in vs. palm‐back) influenced the distribution and timing of peak pressures. Age‐related increases in body mass also result in higher overall pressures and increased variation across the digital row. In chimpanzees, digit 5 typically bears relatively little load regardless of hand position or substrate. These are the first quantitative data on digital pressures during knuckle‐walking in hominoids, and they afford the opportunity to develop hypotheses about variation among hominoids and biomechanical models of wrist and forearm loading. Am J Phys Anthropol 2009. © 2009 Wiley‐Liss, Inc.     

How muscles accommodate movement in different physical environments: aquatic vs. terrestrial locomotion in vertebrates.

Representatives of nearly all vertebrate classes are capable of coordinated movement through aquatic and terrestrial environments. Though there are good data from a variety of species on basic patterns of muscle recruitment during locomotion in a single environment, we know much less about how vertebrates use the same musculoskeletal structures to accommodate locomotion in physically distinct environments. To address this issue, we have gathered data from a broad range of vertebrates that move successfully through water and across land, including eels, toads, turtles and rats. Using high-speed video in combination with electromyography and sonomicrometry, we have quantified and compared the activity and strain of individual muscles and the movements they generate during aquatic vs. terrestrial locomotion. In each focal species, transitions in environment consistently elicit alterations in motor output by major locomotor muscles, including changes in the intensity and duration of muscle activity and shifts in the timing of activity with respect to muscle length change. In many cases, these alterations likely change the functional roles played by muscles between aquatic and terrestrial locomotion. Thus, a variety of forms of motor plasticity appear to underlie the ability of many species to move successfully through different physical environments and produce diverse behaviors in nature.     

Forward dynamic simulation of bipedal walking in the Japanese macaque: investigation of causal relationships among limb kinematics, speed, and energetics of bipedal locomotion in a nonhuman primate

Japanese macaques that have been trained for monkey performances exhibit a remarkable ability to walk bipedally. In this study, we dynamically reconstructed bipedal walking of the Japanese macaque to investigate causal relationships among limb kinematics, speed, and energetics, with a view to understanding the mechanisms underlying the evolution of human bipedalism. We constructed a two-dimensional macaque musculoskeletal model consisting of nine rigid links and eight principal muscles. To generate locomotion, we used a trajectory-tracking control law, the reference trajectories of which were obtained experimentally. Using this framework, we evaluated the effects of changes in cycle duration and gait kinematics on locomotor efficiency. The energetic cost of locomotion was estimated based on the calculation of mechanical energy generated by muscles. Our results demonstrated that the mass-specific metabolic cost of transport decreased as speed increased in bipedal walking of the Japanese macaque. Furthermore, the cost of transport in bipedal walking was reduced when vertical displacement of the hip joint was virtually modified in the simulation to be more humanlike. Human vertical fluctuations in the body's center of mass actually contributed to energy savings via an inverted pendulum mechanism.     

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.     

Thermal influence on metabolic rates and a bioenergetic budget for Notophthalmus viridescens from southwestern Massachusetts

Notophthalmus viridescens has been reported to overwinter on land in southwestern Massachusetts, whereas these newts hibernate in water in southwestern Ohio. Aquatic and terrestrial metabolic rates of newts from Massachusetts were measured at different exercise speeds and acclimation temperatures in order to better understand their seasonal energetic budgets. Oxygen uptake at 25°C increased with increased swimming and walking speeds and reached a plateau at speeds of 60 and 90 cm/min, whereas at 5°C, oxygen consumption linearly increased with swimming speeds. Aerobic transport costs of the newts thus decreased with increased locomotor speeds at 25°C but remained unchanged when the newts were exercised in water at 5°C. Anaerobic metabolic rates of the newts on land were little affected by acclimation temperature but also increased linearly with walking speeds at both 5°C and 25°C. Anaerobiosis contributed most of the energy for the locomotion of the newts. These newts stored an average of 12 mg lipd/g body mass, which could apparently support their survival at 5°C for 46 days without food on land but only for 18 days in water. These calculations, based on measured metabolic rates and energy reserves, support field observations of red-spotted newts hibernating on land in Massachusetts.