Audrone R. Biknevicius

The tale of the tail: limb function and locomotor mechanics in Alligator mississippiensis

SUMMARY Crocodilians tow their large muscular tail behind them during terrestrial bouts when they high walk (a walking trot). Analysis of ground reaction forces in the American alligator (Alligator mississippiensis) revealed the consequences of tail-dragging. Individual limb and tail ground reaction force records show that the hindlimbs of Alligator take on a substantial role in body mass support consistent with the more caudal location of its center of mass due to the presence of a particularly heavy tail (representing nearly 28% of total body mass). Furthermore, because the constant drag imposed by the tail is substantial, both fore- and hindlimbs in Alligator have a heightened propulsive role as a means of countering the net braking effect of the tail. Ground reaction forces of the whole body were used to assess how well Alligator was able to utilize mechanical energy-saving mechanisms (inverse pendulum or mass-spring). A high-walking Alligator recovers, on average, about 20% of its mechanical energy by inverse pendulum mechanics. These modest energy recovery levels are likely to be due to a combination of factors that may include low locomotor speed, imprecise coordination of contralateral limbs in the trot, frequent dragging of feet of protracting limbs during swing phase and, possibly, tail dragging.

Whole-body mechanics and gaits in the gray short-tailed opossum Monodelphis domestica: integrating patterns of locomotion in a semi-erect mammal.

SUMMARY Gaits (footfall patterns) and external mechanical energy patterns of the center of mass were quantified in a generalized, semi-erect mammal in order to address three general questions. First, do semi-erect mammals exhibit the walk/run gait transitions that have been proposed as the primitive condition for tetrapods? Second, do small, semi-erect mammals employ the energy-saving pendular and spring-based mechanics used by erect mammals? Third, how well do mechanical locomotor patterns of the center of mass correlate with gaits? Monodelphis domestica utilizes only fast walking and running trot gaits over a fivefold increase in speed, over which we could illicit constant velocity steps, although running trots were their preferred gait. In sustained level locomotion the opossums did not use other walking gaits presumed to be primitive for tetrapods. Across the full range of speeds their trotting gaits exhibited force patterns and in-phase mechanical energy fluctuations that are characteristic of spring-mass mechanics. Thus, opossums appear to prefer trotting gaits with bouncing mechanics for sustained locomotion. Integration of center-of-mass versus footfall perspectives reveals that spring-mass mechanics is associated with both walking trot and running trot gaits. Furthermore, the onset of an aerial phase was not clearly associated with either the walk/run gait transition (50% duty factor) or a change in center-of-mass mechanics. The assumption that energy-saving mechanisms are ubiquitous among mammals is tenuous because small non-cursorial mammals do not appear to use pendular-based mechanics for sustained locomotion and, although they prefer spring-based mechanics, they probably lack clear musculoskeletal spring elements that could store energy during running. Thus, it appears that simply paying for locomotion with muscular work may be the primitive condition for mammals.

Hindlimb function in the alligator: integrating movements, motor patterns, ground reaction forces and bone strain of terrestrial locomotion

SUMMARY Alligator hindlimbs show high torsional loads during terrestrial locomotion, in sharp contrast to the bending or axial compressive loads that predominate in animals that use parasagittal limb movements. The present study integrates new data on hindlimb muscle function with previously obtained data on hindlimb kinematics, motor patterns, ground reaction forces and bone strain in order to (1) assess mechanisms underlying limb bone torsion during non-parasagittal locomotion in alligators and (2) improve understanding of hindlimb dynamics during terrestrial locomotion. Three dynamic stance phase periods were recognized: limb-loading, support-and-propulsion, and limb-unloading phases. Shear stresses due to torsion were maximized during the limb-loading phase, during which the ground reaction force (GRF) and caudofemoralis (CFL) muscles generated opposing moments about the femur. Hindlimb retraction during the subsequent stance-and-propulsion phase involves substantial medial rotation of the femur, powered largely by coordinated action of the GRF and CFL. Several muscles that actively shorten to flex and extend limb joints during stance phase in sprawling and erect quadrupeds act in isometric or even eccentric contraction in alligators, stabilizing the knee and ankle during the support-and-propulsion phase. Motor patterns in alligators reveal the presence of local and temporal segregation of muscle functions during locomotion with muscles that lie side by side dedicated to performing different functions and only one of 16 muscles showing clear bursts of activity during both stance and swing phases. Data from alligators add to other recent discoveries that homologous muscles across quadrupeds often do not move joints the same way as is commonly assumed. Although alligators are commonly considered models for early semi-erect tetrapod locomotion, many aspects of hindlimb kinematics, muscle activity patterns, and femoral loading patterns in alligators appear to be derived in alligators rather than reflecting an ancestral semi-erect condition.

SKELETAL ALLOMETRY AND INTERLIMB SCALING PATTERNS IN MUSTELID CARNIVORANS

To address the effects of an evolutionary increase in body size on long bone skeletal allometry, scaling patterns relating body mass, bone length, limb length, midshaft diameters, and cross‐sectional properties of the humerus and femur were analyzed for four species of scansorial mustelids. Humeral and, to a lesser extent, femoral allometry is consistent with expectations of elastic similarity: bone and limb length scale with negative allometry on body mass while bone robusticity (cross‐sectional parameters against bone length) scales with strong positive allometry. Differences between fore‐ and hindlimb scaling patterns, however, are observed, with size‐dependent increases in forelimb length and humeral strength and robusticity exceeding those of the hindlimb and femur. It is hypothesized that this greater fore‐ than hindlimb lengthening results in postural modifications that serve to straighten the hindlimb of larger bodied scansorial mustelids relative to smaller mustelids. Straightening of hindlimb joints would more precisely align the long axis of the femur with peak (vertical) ground reaction forces, thereby accounting for the reduction in relative bending stresses acting on the femur compared to the humerus. J. Morphol. 235:121–134, 1998.

Ontogeny of feeding function in the gray short-tailed opossum Monodelphis domestica: empirical support for the constrained model of jaw biomechanics

SUMMARY The constrained model of masticatory function enables specific predictions of bite force potentials in skulls of differing craniodental configurations. In this study, empirical support for the constrained model is provided using maximum voluntary bite force data along Region I and II of the jaws of gray short-tailed opossums Monodelphis domestica. Then, growth series of M. domestica are used to assess how bite force potential changes with growth by evaluating craniodental changes using longitudinal sets of dorsoventral radiographs and by assessing maximal bite force potential at the Region I-II boundary of the jaw in juveniles (aged 70-80 days) and adults. Our findings show that, while juveniles and adults alike enclose at least three molariform teeth within Region II (the area of highest bite force potential along the jaw), age-dependent elongation of the masticatory muscle resultant lever arm and narrowing of the palate relative to jaw length especially enhance the mechanical advantage of the adductor muscle resultant in adults. While maximal bite forces at the Region I-II boundary are absolutely greater in adults, these bite forces scale isometrically with body mass, which suggests that mass-specific forces exerted by jaw adductor muscles of larger (adult) opossums are disproportionately smaller than those exerted by smaller (juvenile) opossums.

Effects of early-stage aging on locomotor dynamics and hindlimb muscle force production in the rat

SUMMARY Attenuation of locomotor function is common in many species of animals as they age. Dysfunctions may emerge from a constellation of age-related impairments, including increased joint stiffness, reduced ability to repair muscle tissue, and decreasing fine motor control capabilities. Any or all of these factors may contribute to gait abnormalities and substantially limit an animals speed and mobility. In this study we examined the effects of aging on whole-animal locomotor performance and hindlimb muscle mechanics in young adult rats aged 6–8 months and ‘early aged’ 24-month-old rats (Rattus norvegicus, Fischer 344 × Brown Norway crosses). Analyses of gaits and kinematics demonstrated that aged rats moved significantly more slowly, sustained longer hindlimb support durations, moved with a greater proportion of asymmetrical gaits, were more plantigrade, and moved with a more kyphotic spinal posture than the young rats. Additionally, the external mechanical energy profiles of the aged animals were variable across trials, whereas the younger rats moved predominantly with bouncing mechanics. In situ analyses of the ankle extensor/plantar flexor muscle group (soleus, plantaris, and medial and lateral gastrocnemii) revealed reduced maximum force generation with aging, despite minimal changes in muscle mass. The weakened muscles were implicated in the degradation of hindfoot posture, as well as variability in center-of-mass mechanics. These results demonstrate that the early stages of aging have consequences for whole-body performance, even before age-related loss of muscle mass begins.

Symmetrical gaits and center of mass mechanics in small-bodied, primitive mammals

Widely accepted relationships between gaits (footfall patterns) and center of mass mechanics have been formulated from observations for cursorial mammals. However, sparse data on smaller or more generalized forms suggest a fundamentally different relationship. This study explores locomotor dynamics in one eutherian and five metatherian (marsupials) mammals-all small-bodied (<2 kg) with generalized body plans that utilize symmetrical gaits. Across our sample, trials conforming to vaulting mechanics occurred least frequently (<10% of all trials) while bouncing mechanics was obtained most commonly (60%); the remaining trials represented mixed mechanics. Contrary to the common situation in large mammals, there was no evidence for discrete gait switching within symmetrical gaits as speed increased. This was in part due to the common practice of grounded running. The adaptive advantage of different patterns of center-of-mass motion and their putative energy savings remain questionable in small-bodied mammals.

Abdominal muscle and epipubic bone function during locomotion in Australian possums: Insights to basal mammalian conditions and eutherian-like tendencies in Trichosurus

Mammals have four hypaxial muscle layers that wrap around the abdomen between the pelvis, ribcage, and spine. However, the marsupials have epipubic bones extending anteriorly into the ventral hypaxial layers with two additional muscles extending to the ventral midline and femur. Comparisons of South American marsupials to basal eutherians have shown that all of the abdominal hypaxials are active bilaterally in resting ventilation. However, during locomotion marsupials employ an asymmetrical pattern of activity as the hypaxial muscles form a crosscouplet linkage that uses the epipubic bone as a lever to provide long‐axis support of the body between diagonal limb couplets during each step. In basal eutherians, this system shifts off the femur and epipubic bones (which are lost) resulting in a shoulder to pelvis linkage associated with shifts in both the positions and activity patterns of the pectineus and rectus abdominis muscles during locomotion. In this study, we present data on hypaxial function in two species (Pseudocheirus peregrinus and Trichosurus vulpecula) representing the two major radiations of possums in Australia: the Pseudocheiridae (within the Petauroidea) and the Phalangeridae. Patterns of gait, motor activity, and morphology in these two Australian species were compared with previous work to examine the generality of 1) the crosscouplet lever system as the basal condition for the Marsupialia and 2) several traits hypothesized to be common to all mammals (hypaxial tonus during resting ventilation, ventilation to step synchrony during locomotion, and bilateral transversus abdominis activity during locomotor expiration). Our results validate the presence of the crosscouplet pattern and basic epipubic bone lever system in Australian possums and confirm the generality of basal mammalian patterns. However, several novelties discovered in Trichosurus, reveal that it exhibits an evolutionary transition to intermediate eutherian‐like morphological and motor patterns paralleling many other unique features of this species. J. Morphol., 2010.

A comparative study of single-leg ground reaction forces in running lizards.

The role of different limbs in supporting and propelling the body has been studied in many species with animals appearing to have either similarity in limb function or differential limb function. Differential hindlimb versus forelimb function has been proposed as a general feature of running with a sprawling posture and as benefiting sprawled postured animals by enhancing maneuvering and minimizing joint moments. Yet only a few species have been studied and thus the generality of differential limb function in running animals with sprawled postures is unknown. We measured the limb lengths of seven species of lizard and their single-limb three-dimensional ground reaction forces during high-speed running. We found that all species relied on the hindlimb for producing accelerative forces. Braking forces were forelimb dominated in four species and equally distributed between limbs in the other three. Vertical forces were dominated by the hindlimb in three species and equally distributed between the forelimb and hindlimb in the other four. Medial forces were dominated by the hindlimb in four species and equally distributed in the other three, with all Iguanians exhibiting hindlimb-biased medial forces. Relative hindlimb to forelimb length of each species was related to variation in hindlimb versus forelimb medial forces; species with relatively longer hindlimbs compared with forelimbs exhibited medial forces that were more biased towards the hindlimbs. These results suggest that the function of individual limbs in lizards varies across species with only a single general pattern (hindlimb-dominated accelerative force) being present.

Structured variability of steady-speed locomotion in rats

By examining key locomotor parameters during terrestrial locomotion on a substrate without irregularities, we show that rats frequently accelerate and decelerate between two consecutive steps while maintaining an overall steady speed and that the touchdown order of contralateral limbs significantly influences those speed adjustments. The latter highly correlates with significant adjustments in relative forelimb protraction at touchdown and hindlimb extension at lift-off. We conclude that this remarkable level of variability in limb coordination would clearly be advantageous for the functional flexibility needed during terrestrial locomotion on much more irregular (rough) natural terrain. In addition, its occurrence on a substrate lacking irregularities suggests that much of stable, terrestrial steady-speed locomotion in rats is mechanically controlled.