Limb kinematics during locomotion in the two-toed sloth (Choloepus didactylus,Xenarthra) and its implications for the evolution of the sloth locomotor apparatus

In order to gain insight into the function of the extant sloth locomotion and its evolution, we conducted a detailed videoradiographic analysis of two-toed sloth locomotion (Xenarthra: Choloepus didactylus). Both unrestrained as well as steady-state locomotion was analyzed. Spatio-temporal gait parameters, data on interlimb coordination, and limb kinematics are reported. Two-toed sloths displayed great variability in spatio-temporal gait parameters over the observed range of speeds. They increase speed by decreasing the durations of contact and swing phases, as well as by increasing step length. Gait utilization also varies with no strict gait sequence or interlimb timing evident in slow movements, but a tendency to employ diagonal sequence, diagonal couplet gaits in fast movements. In contrast, limb kinematics were highly conserved with respect to ‘normal’ pronograde locomotion. Limb element and joint angles at touch down and lift off, element and joint excursions, and contribution to body progression of individual elements are similar to those reported for non-cursorial mammals of small to medium size. Hands and feet are specialized to maintain firm connection to supports, and do not contribute to step length or progression. In so doing, the tarsometatarsus lost its role as an individual propulsive element during the evolution of suspensory locomotion. Conservative kinematic behavior of the remaining limb elements does not preclude that muscle recruitment and neuromuscular control for limb pro- and retraction are also conserved. The observed kinematic patterns of two-toed sloths improve our understanding of the convergent evolution of quadrupedal suspensory posture and locomotion in the two extant sloth lineages.     

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

Background

Theria (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.

Methods

We 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).

Results

Despite 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.

Conclusions

The 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.     

The Convergent Evolution of Suspensory Posture and Locomotion in Tree Sloths

Recent phylogenetic analyses imply a distant relationship and long separated evolution of two-toed sloths (Choloepus) and three-toed sloths (Bradypus). No known fossil sloth is interpreted to have been suspensory. As a consequence, the suspensory posture and locomotion of the extant genera likely evolved convergently in both lineages, forming a new framework for the analysis of functional aspects of the locomotor apparatus of extant tree sloths. The suspensory posture and locomotion has altered functional demands from the phylogenetically plesiomorphic non-suspensory pronograde situation. Here, anatomical traits that have been argued to be of adaptive significance for quadrupedal suspensory locomotion are reviewed and the evolution of these traits is discussed in light of the new framework. Experimental data are largely limited to Choloepus, but help to deduce functional aspects of the anatomy in Bradypus as well. The most important adaptive traits are hands and feet modified into relatively rigid hook-like appendages, great mobility of all joints proximal to the midcarpal and transverse tarsal joints, relatively long arms with a relatively short scapula, a rounded thorax with a small diameter, a highly mobile sterno-clavicular articulation, and emphasis on powerful flexion in the proximal limb joints via advantageous lever arms. Despite these changes, patterns of limb kinematics remained conservative during the course of evolution in the lineages leading to extant tree sloths, and it is suggested here that this also applies to the pattern of neuromuscular control of limb movements during locomotion. Morphological ‘solutions’ to altered functional demands posed by inversed orientation of the body differ in the two genera of extant tree sloths, thereby corroborating the proposed diphyly. Convergent evolution in tree sloths may be attributed to functional constraints posed by fossorial adaptations in early Xenarthra that canalized sloths to adopt a suspensory posture and locomotion in the arboreal habitat.     

Comparative analysis of methods for estimating arm segment parameters and joint torques from inverse dynamics

A common problem in the analyses of upper limb unfettered reaching movements is the estimation of joint torques using inverse dynamics. The inaccuracy in the estimation of joint torques can be caused by the inaccuracy in the acquisition of kinematic variables, body segment parameters (BSPs), and approximation in the biomechanical models. The effect of uncertainty in the estimation of body segment parameters can be especially important in the analysis of movements with high acceleration. A sensitivity analysis was performed to assess the relevance of different sources of inaccuracy in inverse dynamics analysis of a planar arm movement. Eight regression models and one water immersion method for the estimation of BSPs were used to quantify the influence of inertial models on the calculation of joint torques during numerical analysis of unfettered forward arm reaching movements. Thirteen subjects performed 72 forward planar reaches between two targets located on the horizontal plane and aligned with the median plane. Using a planar, double link model for the arm with a floating shoulder, we calculated the normalized joint torque peak and a normalized root mean square (rms) of torque at the shoulder and elbow joints. Statistical analyses quantified the influence of different BSP models on the kinetic variable variance for given uncertainty on the estimation of joint kinematics and biomechanical modeling errors. Our analysis revealed that the choice of BSP estimation method had a particular influence on the normalized rms of joint torques. Moreover, the normalization of kinetic variables to BSPs for a comparison among subjects showed that the interaction between the BSP estimation method and the subject specific somatotype and movement kinematics was a significant source of variance in the kinetic variables. The normalized joint torque peak and the normalized root mean square of joint torque represented valuable parameters to compare the effect of BSP estimation methods on the variance in the population of kinetic variables calculated across a group of subjects with different body types. We found that the variance of the arm segment parameter estimation had more influence on the calculated joint torques than the variance of the kinematics variables. This is due to the low moments of inertia of the upper limb, especially when compared with the leg. Therefore, the results of the inverse dynamics of arm movements are influenced by the choice of BSP estimation method to a greater extent than the results of gait analysis.     

Recent Advances on Variability, Morpho-Functional Adaptations, Dental Terminology, and Evolution of Sloths

The occasion of the Xenarthra Symposium during the ICVM 9 meeting allowed us to reflect on the considerable advances in the knowledge of sloths made by the “X-community” over the past two decades, particularly in such aspects as locomotion, mastication, diet, dental terminology, intraspecific variation, sexual dimorphism, and phylogenetic relationships. These advancements have largely been made possible by the application of cladistic methodology (including DNA analyses) and the discovery of peculiar forms such as Diabolotherium, Thalassocnus, and Pseudoglyptodon in traditionally neglected areas such as the Chilean Andes and the Peruvian Pacific desert coast. Modern tree sloths exhibit an upside-down posture and suspensory locomotion, but the habits of fossil sloths are considerably more diverse and include locomotory modes such as inferred bipedality, quadrupedality, arboreality or semiarboreality, climbing, and an aquatic or semi-aquatic lifestyle in saltwater. Modern tree sloths are generalist browsers, but fossil sloths had browsing, grazing, or mixed feeding dietary habits. Discovery of two important sloth faunas in Brazil (Jacobina) and southern North America (Daytona Beach and Rancho La Brea) have permitted evaluation of the ontogenetic variation in Eremotherium laurillardi and the existence of possible sexual dimorphism in this sloth and in Paramylodon harlani. A new dental terminology applicable to a majority of clades has been developed, facilitating comparisons among taxa. An analysis wherein functional traits were plotted onto a phylogeny of sloths was used to determine patterns of evolutionary change across the clade. These analyses suggest that megatherioid sloths were primitively semiarboreal or possessed climbing adaptations, a feature retained in some members of the family Megalonychidae. Pedolateral stance in the hindfoot is shown to be convergently acquired in Mylodontidae and Megatheria (Nothrotheriidae + Megatheriidae), this feature serving as a synapomorphy of the latter clade. Digging adaptations can only be securely ascribed to scelidotheriine and mylodontine sloths, and the latter are also the only group of grazing sloths, the remainder being general browsers.     

Functional Analysis of the Primate Shoulder

Studies of the shoulder girdle are in most cases restricted to morphological comparisons and rarely aim at elucidating function in a strictly biomechanical sense. To fill this gap, we investigated the basic functional conditions that occur in the shoulder joint and shoulder girdle of primates by means of mechanics. Because most of nonhuman primate locomotion is essentially quadrupedal walking—although on very variable substrates—our analysis started with quadrupedal postures. We identified the mechanical situation at the beginning, middle, and end of the load-bearing stance phase by constructing force parallelograms in the shoulder joint and the scapulo-thoracal connection. The resulting postulates concerning muscle activities are in agreement with electromyographical data in the literature. We determined the magnitude and directions of the internal forces and explored mechanically optimal shapes of proximal humerus, scapula, and clavicula using the Finite Element Method. Next we considered mechanical functions other than quadrupedal walking, such as suspension and brachiation. Quadrupedal walking entails muscle activities and joint forces that require a long scapula, the cranial margin of which has about the same length as the axillary margin. Loading of the hand in positions above the head and suspensory behaviors lead to force flows along the axillary margin and so necessitate a scapula with an extended axillary and a shorter cranial margin. In all cases, the facies glenoidalis is nearly normal to the calculated joint forces. In anterior view, terrestrial monkeys chose a direction of the ground reaction force requiring (moderate) activity of the abductors of the shoulder joint, whereas more arboreal monkeys prefer postures that necessitate activity of the adductors of the forelimb even when walking along branches. The same adducting and retracting muscles are recruited in various forms of suspension. As a mechanical consequence, the scapula is in a more frontal, rather than parasagittal, position on the thorax. In both forms of locomotion—quadrupedal walking and suspension—the compression-resistant clavicula contributes to keeping the shoulder complex distant from the rib cage. Future studies should consider the consequences for thorax shape. The morphological specializations of all Hominoidea match the functional requirements of suspensory behavior. The knowledge of mechanical functions allows an improved interpretation of fossils beyond morphological similarity.     

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.     

Locomotion and posture in Lagothrix lagotricha

This long-term study of woolly monkey (Lagothrix) locomotor and postural behaviour employs methods identical to those used during a previous study of the locomotion and posture of two species of Ateles, allowing a detailed comparison between the two genera, which are strong competitors in extensive parts of the Amazon basin and northern Andes. As in Ateles, Lagothrix locomotion can be divided into five patterns, based on limb usage: quadrupedal walking and running, suspensory locomotion, climbing, bipedalism (very rare in wild woolly monkeys) and leaping. Lagothrix differs from Ateles primarily in its greater reliance on quadrupedal locomotion during both travel and feeding and on its de-emphasis of the use of suspensory locomotion as compared to Ateles, while the use of climbing and leaping is roughly equal in the two genera. Lagothrix exhibits more generalised (primitive) locomotive behaviour in accordance with its morphology, in comparison to the more specialised Ateles. The generic differences reflect differences in habitat use and particularly foraging ecology.     

The locomotion of Babakotia radofilai inferred from epiphyseal and diaphyseal morphology of the humerus and femur

Palaeopropithecids, or “sloth lemurs,” are a diverse clade of large‐bodied Malagasy subfossil primates characterized by their inferred suspensory positional behavior. The most recently discovered genus of the palaeopropithecids is Babakotia, and it has been described as more arboreal than Mesopropithecus, but less than Palaeopropithecus. In this article, the within‐bone and between‐bones articular and cross‐sectional diaphyseal proportions of the humerus and femur of Babakotia were compared to extant lemurs, Mesopropithecus and Palaeopropithecus in order to further understand its arboreal adaptations. Additionally, a sample of apes and sloths (Choloepus and Bradypus) are included as functional outgroups composed of suspensory adapted primates and non‐primates. Results show that Babakotia and Mesopropithecus both have high humeral/femoral shaft strength proportions, similar to extant great apes and sloths and indicative of forelimb suspensory behavior, with Babakotia more extreme in this regard. All three subfossil taxa have relatively large femoral heads, also associated with suspension in modern taxa. However, Babakotia and Mesopropithecus (but not Palaeopropithecus) have relatively small femoral head surface area to shaft strength proportions suggesting that hind‐limb positioning in these taxa during climbing and other behaviors was different than in extant great apes, involving less mobility. Knee and humeral articular dimensions relative to shaft strengths are small in Babakotia and Mesopropithecus, similar to those found in modern sloths and divergent from those in extant great apes and lemurs, suggesting more sloth‐like use of these joints during locomotion. Mesopropithecus and Babakotia are more similar to Choloepus in humerofemoral head and length proportions while Palaeopropithecus is more similar to Bradypus. These results provide further evidence of the suspensory adaptations of Babakotia and further highlight similarities to both extant suspensory primates and non‐primate slow arboreal climbers and hangers. J. Morphol. 277:1199–1218, 2016. © 2016 Wiley Periodicals, Inc.     

Ontogeny of limb force distribution in squirrel monkeys (Saimiri boliviensis): insights into the mechanical bases of primate hind limb dominance

The distribution of peak vertical forces between the forelimbs and the hind limbs is one of the key traits distinguishing primate quadrupedal locomotion from that of other mammals. Whereas most mammals generate greater peak vertical forelimb forces, primates generate greater peak vertical hind limb forces. At the ultimate level, hind limb dominance in limb force distribution is typically interpreted as an adaptation to facilitate fine-branch arboreality. However, the proximate biomechanical bases for primate limb force distribution remain controversial. Three models have been previously proposed. The Center of Mass (COM) Position model attributes primates’ unique mode of limb loading to differences in the position of the whole-body COM relative to the hands and feet. The Active Weight Shift model asserts that primates actively redistribute body weight to their hind limbs by pitching the trunk up via the activation of hind limb retractor muscles. Finally, the Limb Compliance model argues that primates selectively mitigate forelimb forces by maintaining a compliant forelimb and a flat shoulder trajectory. Here, a detailed dataset of ontogenetic changes in morphology and locomotor mechanics in Bolivian squirrel monkeys (Saimiri boliviensis) was employed as a model system to evaluate each of these proposed models in turn. Over the first 10 months of life, squirrel monkeys transitioned from forelimb dominant infants to hind limb dominant juveniles, a change that was precipitated by decreases in peak vertical forelimb forces and increases in peak vertical hind limb forces. Results provided some support for all three of the models, although the COM Position and Active Weight Shift models were most strongly supported by the data. Overall, this study suggests that primates may use a variety of biomechanical strategies to achieve hind limb dominance in limb force distribution.     

Architectural Properties of Sloth Forelimb Muscles (Pilosa: Bradypodidae)

Tree sloths have reduced skeletal muscle mass, and yet they are able to perform suspensory behaviors that require both strength and fatigue resistance to suspend their body mass for extended periods of time. The muscle architecture of sloths is hypothesized to be modified in ways that will enhance force production to compensate for this reduction in limb muscle mass. Our objective is to test this hypothesis by quantifying architecture properties in the forelimb musculature of the brown-throated three-toed sloth (Bradypus variegatus: N = 4). We evaluated architecture from 52 forelimb muscles by measuring muscle moment arm (r _m), muscle mass (MM), belly length (ML), fascicle length (L_F), pennation angle (θ), and physiological cross-sectional area (PCSA), and these metrics were used to estimate isometric force, joint torque, and power. Overall, the musculature becomes progressively more pennate from the extrinsic to intrinsic regions of the forelimb, and the flexors are more well developed than the extensors as predicted. However, most muscles are indicative of a mechanical design for fast joint rotational velocity instead of large joint torque (i.e., strength), although certain large, parallel-fibered shoulder (e.g., m. latissimus dorsi) and elbow (e.g., m. brachioradialis) flexors are capable of producing appreciable torques by having elongated moment arms. This type of functional tradeoff between joint rotational velocity and mechanical advantage is further exemplified by muscle gearing in Bradypus that pairs synergistic muscles with opposing L_F/r _m ratios in each functional group. These properties are suggested to facilitate the slow, controlled movements in sloths. In addition, the carpal/digital flexors have variable architectural properties, but their collective PCSA and joint torque indicates the capability for maintaining grip force and carpal stability while distributing load from the manus to the shoulder. The observed specializations provide a basis for understanding sustained suspension in sloths.     

EMG of chimpanzee shoulder muscles during knuckle-walking: problems of terrestrial locomotion in a suspensory adapted primate

By most accounts, the upper limb of the chimpanzee is primarily adapted to suspensory postures and locomotion. In order to determine how the derived morphology of the chimpanzee forelimb has affected the form of quadrupedal locomotion displayed by these animals, electromyographic activity patterns of 10 shoulder muscles during knuckle-walking in two chimpanzee subjects were analysed and compared to data on the opossum and cat taken from the literature. Telemetered electromyography coupled with simultaneous video recording was employed in order to study unfettered locomotion in the chimpanzee subjects.
Chimpanzees are characterized by a quadrupedal gait in which the hind limb overstrides the ipsilateral forelimb. Forelimb position in the plane of abduction/adduction is significantly affected by whether the hind limb passes inside or outside its ipsilateral forelimb. The degree of abduction adduction of the forelimb, in turn, influences many of the muscle activity patterns. That is, some muscles would be more frequently or less frequently active, depending on whether the arm was relatively abducted or adducted during a stride. Thus, there can be no single motor programme that generates the step cycle in chimpanzees.
While there are some parallels between muscle recruitment patterns for chimpanzee, opossum and cat quadrupedalism, the results of this study also indicate that many aspects of muscle use in chimpanzees have been significantly influenced by factors related to increased mobility of the upper limb. Finally, this study has revealed that moving the arm forward during swing phase of knuckle-walking is not a simple product of muscular elTort. and that other mechanisms must be involved. However, it is unclear at present exactly what these mechanisms may be.     

Bipedalism and quadrupedalism in Megatheriurn: an attempt at biomechanical reconstruction

Biomechanical reconstruction is increasingly being applied to the study of the mode of life of fossil animals. Different footprints from the fossil mammal Megatherium sp., the giant ground sloth, seem to indicate that it was able to use either bipedal or quadrupedal locomotion. By means of the estimation of the body mass of the type of the species Megatherium americanum , and using the published tracks, different mechanical parameters, such as speed, Froude number, indicators of athletic ability and bending and resistance moments of the vertebral column were calculated in both bipedal and quadrupedal conditions. Results on leg parameters are not conclusive as to the kind of locomotion to which Megatherium sp. was better adapted, but the calculations on the moments of resistance of the vertebral column and on the bending moment at breaking of the femur seem to indicate that Megatherium sp. presented adaptations to bipedalism. MEGATHERIUM, mammals, legs, vertebral column, locomotion, biomechanics, reconstruction .     

Comparisons of Suspensory Behaviors Among <Emphasis Type="Italic">Pygathrix cinerea</Emphasis>, <Emphasis Type="Italic">P. nemaeus</Emphasis>, and <Emphasis Type="Italic">Nomascus leucogenys</Emphasis> in Cuc Phuong National Park,Vietnam

In our study at the Endangered Primate Rescue Center of Cuc Phuong National Park, Vietnam, we aimed first to assemble a positional behavioral profile of captive gray-shanked (Pygathrix cinerea) and red-shanked (P. nemaeus) doucs that relates to the use of forelimb suspensory postures and arm-swinging locomotion. The profile is of interest because researchers have documented that red-shanked doucs more frequently use suspensory postures and locomotions than other colobines do. We confirmed that red-shanked doucs commonly use suspensory positional behaviors and also that gray-shanked doucs use suspensory behaviors at similar or even higher frequencies than those of red-shanked doucs. Our second goal was to assemble a preliminary kinematic profile of suspensory locomotion in Pygathrix within the context of the arm-swinging locomotion exhibited by northern white-cheeked gibbons, Nomascus leucogenys. Mean forelimb angles at initial contact and release of arm-swinging behaviors were remarkably consistent among gibbons and doucs despite the fact that gibbons typically used more continuous brachiation. Doucs also exhibit a greater range of forelimb angles than gibbons do. In addition, trunk orientation tends to be less vertical at initial contact for doucs than for gibbons, perhaps owing to the frequent use of quadrupedal sequences directly before or after forelimb suspension. Our behavioral and kinematic analyses add to the emerging realization that Pygathrix is capable of, and frequently expresses, a range of suspensory positional behaviors, including brachiation.     

Apparent density patterns in subchondral bone of the sloth and anteater forelimb

Vertebrate morphologists often are interested in inferring limb-loading patterns in animals characterized by different locomotor repertoires. Because bone apparent density (i.e. mass per unit volume of bone inclusive of porosities) is a determinant of compressive strength, and thus indicative of compressive loading, recent comparative studies in primates have proposed a structure-function relationship between apparent density of subchondral bone and locomotor behaviours that vary in compressive loading. If such patterns are found in other mammals, then these relationships would be strengthened further. Here, we examine the distal radius of suspensory sloths that generally load their forelimbs (FLs) in tension and of quadrupedal anteaters that generally load their FLs in compression. Computed tomography osteoabsorptiometry was used to visualize the patterns in subchondral apparent density. Suspensory sloths exhibit relatively smaller areas of high apparent density than quadrupedal anteaters. This locomotor-based pattern is analogous to the pattern observed in suspensory and quadrupedal primates. Similarity between xenarthran and primate trends suggests broad-scale applicability for analysing subchondral bone apparent density and supports the idea that bone functionally alters its material properties in response to locomotor behaviours.     

On the organizing role of nonmuscular forces during performance of a giant circle in gymnastics

Five elite gymnasts performed giant circles on the high bar under different conditions of loading (without and with 6-kg loads attached to the shoulders, waist or ankles). Comparing the gymnasts' kinematic pattern of movement with that of a triple-pendulum moving under the sole influence of nonmuscular forces revealed qualitative similarities, including the adoption of an arched position during the downswing and a piked position during the upswing. The structuring role of nonmuscular forces in the organization of movement was further reinforced by the results of an inverse dynamics analysis, assessing the contributions of gravitational, inertial and muscular components to the net joint torques. Adding loads at the level of the shoulders, waist or ankles systematically influenced movement kinematics and net joint torques. However, with the loads attached at the level of the shoulders or waist, the load-induced changes in gravitational and inertial torques provided the required increase in net joint torque, thereby allowing the muscular torques to remain unchanged. With the loads attached at the level of the ankles, this was no longer the case and the gymnasts increased the muscular torques at the shoulder and hip joints. Together, these results demonstrate that expert gymnasts skillfully exploit the operative nonmuscular forces, employing muscle force only in the capacity of complementary forces needed to perform the task.     

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.     

Kinetic chain of overarm throwing in terms of joint rotations revealed by induced acceleration analysis

This study investigated how baseball players generate large angular velocity at each joint by coordinating the joint torque and velocity-dependent torque during overarm throwing. Using a four-segment model (i.e., trunk, upper arm, forearm, and hand) that has 13 degrees of freedom, we conducted the induced acceleration analysis to determine the accelerations induced by these torques by multiplying the inverse of the system inertia matrix to the torque vectors. We found that the proximal joint motions (i.e., trunk forward motion, trunk leftward rotation, and shoulder internal rotation) were mainly accelerated by the joint torques at their own joints, whereas the distal joint motions (i.e., elbow extension and wrist flexion) were mainly accelerated by the velocity-dependent torques. We further examined which segment motion is the source of the velocity-dependent torque acting on the elbow and wrist accelerations. The results showed that the angular velocities of the trunk and upper arm produced the velocity-dependent torque for initial elbow extension acceleration. As a result, the elbow joint angular velocity increased, and concurrently, the forearm angular velocity relative to the ground also increased. The forearm angular velocity subsequently accelerated the elbow extension and wrist flexion. It also accelerated the shoulder internal rotation during the short period around the ball-release time. These results indicate that baseball players accelerate the distal elbow and wrist joint rotations by utilizing the velocity-dependent torque that is originally produced by the proximal trunk and shoulder joint torques in the early phase.     

The dynamics of quadrupedal locomotion

This paper presents a dynamical analysis of quadrupedal locomotion, with specific reference to an adult Nubian goat. Measurements of ground reaction forces and limb motion are used to assess variations in intersegmental forces, joint moments, and instantaneous power for three discernible gaits: walking, running, and jumping. In each case, inertial effects of the torso are shown to dominate to the extent that lower-extremity contributions may be considered negligible. Footforces generated by the forelimbs exceed those exerted by the hindlimbs; and, in general, ground reactions increase with speed. The shoulder and hip dominate mechanical energy production during walking, while the knee plays a more significant role in running. In both cases, however, the elbow absorbs energy, and by so doing functions primarily as a damping (control) element. As opposed to either walking or running, jumping requires total horizontal retardation of the body's center of mass. In this instance, generating the necessary vertical thrust amounts to energy absorption at all joints of the lower extremities.     

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.