How scaling approaches can reveal fundamental principles in physiology and biomechanics.

Among terrestrial mammals, the largest, the 3 tonne African elephant, is one-million times heavier than the smallest, the 3 g pygmy shrew. Body mass is the most obvious and arguably the most fundamental characteristic of an animal, impacting many important attributes of its life history and biology. Although evolution may guide animals to different sizes, shapes, energetic profiles or ecological niches, it is the laws of physics that limit biological processes and, in turn, affect how animals interact with their environment. Consideration of scaling helps us to understand why elephants are not merely scaled-up shrews, but rather have modified body proportions, posture and locomotor style to mitigate the consequences of their large size. Scaling offers a quantitative lens into how biological features vary compared with predictions based on physical laws. In this Review, we provide an introduction to scaling and its historical context, focusing on two fields that are strongly represented in experimental biology: physiology and biomechanics. We show how scaling has been used to explore metabolic energy use with changes in body size. We discuss the musculoskeletal and biomechanical adaptations that animals use to mitigate the consequences of size, and provide insights into the scaling of mechanical and energetic demands of animal locomotion. For each field, we discuss empirical measurements, fundamental scaling theories and the importance of considering phylogenetic relationships when performing scaling analyses. Finally, we provide forward-looking perspectives focused on improving our understanding of the diversity of form and function in relation to size.

Scaling of fibre area and fibre glycogen concentration in the hindlimb musculature of monitor lizards: implications for locomotor performance with increasing body size.

A considerable biomechanical challenge faces larger terrestrial animals as the demands of body support scale with body mass (Mb), while muscle force capacity is proportional to muscle cross-sectional area, which scales with Mb2/3. How muscles adjust to this challenge might be best understood by examining varanids, which vary by five orders of magnitude in size without substantial changes in posture or body proportions. Muscle mass, fascicle length and physiological cross-sectional area all scale with positive allometry, but it remains unclear, however, how muscles become larger in this clade. Do larger varanids have more muscle fibres, or does individual fibre cross-sectional area (fCSA) increase? It is also unknown if larger animals compensate by increasing the proportion of fast-twitch (higher glycogen concentration) fibres, which can produce higher force per unit area than slow-twitch fibres. We investigated muscle fibre area and glycogen concentration in hindlimb muscles from varanids ranging from 105 g to 40,000 g. We found that fCSA increased with modest positive scaling against body mass (Mb0.197) among all our samples, and ∝Mb0.278 among a subset of our data consisting of never-frozen samples only. The proportion of low-glycogen fibres decreased significantly in some muscles but not others. We compared our results with the scaling of fCSA in different groups. Considering species means, fCSA scaled more steeply in invertebrates (∝Mb0.575), fish (∝Mb0.347) and other reptiles (∝Mb0.308) compared with varanids (∝Mb0.267), which had a slightly higher scaling exponent than birds (∝Mb0.134) and mammals (∝Mb0.122). This suggests that, while fCSA generally increases with body size, the extent of this scaling is taxon specific, and may relate to broad differences in locomotor function, metabolism and habitat between different clades.

Exploring the limits to turning performance with size and shape variation in dogs.

Manoeuvrability, the ability to make rapid changes in direction, is central to animal locomotion. Turning performance may depend on the ability to successfully complete key challenges including: withstanding additional lateral forces, maintaining sufficient friction, lateral leaning during a turn and rotating the body to align with the new heading. We filmed high-speed turning in domestic dogs (Canis lupus familiaris) to quantify turning performance and explore how performance varies with body size and shape. Maximal speed decreased with higher angular velocity, greater centripetal acceleration and smaller turning radii, supporting a force limit for wider turns and a friction limit for sharp turns. Variation in turning ability with size was complex: medium sized dogs produced greater centripetal forces, had relatively higher friction coefficients, and generally aligned the body better with the heading compared with smaller and larger bodied dogs. Body shape also had a complex pattern, with longer forelimbs but shorter hindlimbs being associated with better turning ability. Further, although more crouched forelimbs were associated with an increased ability to realign the body in the direction of movement, more upright hindlimbs were related to greater centripetal and tangential accelerations. Thus, we demonstrate that these biomechanical challenges to turning can vary not only with changes in speed or turning radius, but also with changes in morphology. These results will have significant implications for understanding the link between form and function in locomotory studies, but also in predicting the outcome of predator-prey encounters.

Series elasticity facilitates safe plantar flexor muscle-tendon shock absorption during perturbed human hopping.

In our everyday lives, we negotiate complex and unpredictable environments. Yet, much of our knowledge regarding locomotion has come from studies conducted under steady-state conditions. We have previously shown that humans rely on the ankle joint to absorb energy and recover from perturbations; however, the muscle-tendon unit (MTU) behaviour and motor control strategies that accompany these joint-level responses are not yet understood. In this study, we determined how neuromuscular control and plantar flexor MTU dynamics are modulated to maintain stability during unexpected vertical perturbations. Participants performed steady-state hopping and, at an unknown time, we elicited an unexpected perturbation via rapid removal of a platform. In addition to kinematics and kinetics, we measured gastrocnemius and soleus muscle activations using electromyography and in vivo fascicle dynamics using B-mode ultrasound. Here, we show that an unexpected drop in ground height introduces an automatic phase shift in the timing of plantar flexor muscle activity relative to MTU length changes. This altered timing initiates a cascade of responses including increased MTU and fascicle length changes and increased muscle forces which, when taken together, enables the plantar flexors to effectively dissipate energy. Our results also show another mechanism, whereby increased co-activation of the plantar- and dorsiflexors enables shortening of the plantar flexor fascicles prior to ground contact. This co-activation improves the capacity of the plantar flexors to rapidly absorb energy upon ground contact, and may also aid in the avoidance of potentially damaging muscle strains. Our study provides novel insight into how humans alter their neural control to modulate in vivo muscle-tendon interaction dynamics in response to unexpected perturbations. These data provide essential insight to help guide design of lower-limb assistive devices that can perform within varied and unpredictable environments.

Using a biologically mimicking climbing robot to explore the performance landscape of climbing in lizards.

Locomotion is a key aspect associated with ecologically relevant tasks for many organisms, therefore, survival often depends on their ability to perform well at these tasks. Despite this significance, we have little idea how different performance tasks are weighted when increased performance in one task comes at the cost of decreased performance in another. Additionally, the ability for natural systems to become optimized to perform a specific task can be limited by structural, historic or functional constraints. Climbing lizards provide a good example of these constraints as climbing ability likely requires the optimization of tasks which may conflict with one another such as increasing speed, avoiding falls and reducing the cost of transport (COT). Understanding how modifications to the lizard bauplan can influence these tasks may allow us to understand the relative weighting of different performance objectives among species. Here, we reconstruct multiple performance landscapes of climbing locomotion using a 10 d.f. robot based upon the lizard bauplan, including an actuated spine, shoulders and feet, the latter which interlock with the surface via claws. This design allows us to independently vary speed, foot angles and range of motion (ROM), while simultaneously collecting data on climbed distance, stability and efficiency. We first demonstrate a trade-off between speed and stability, with high speeds resulting in decreased stability and low speeds an increased COT. By varying foot orientation of fore- and hindfeet independently, we found geckos converge on a narrow optimum of foot angles (fore 20°, hind 100°) for both speed and stability, but avoid a secondary wider optimum (fore -20°, hind -50°) highlighting a possible constraint. Modifying the spine and limb ROM revealed a gradient in performance. Evolutionary modifications in movement among extant species over time appear to follow this gradient towards areas which promote speed and efficiency.

The scaling of ground reaction forces and duty factor in monitor lizards: implications for locomotion in sprawling tetrapods.

Geometric scaling predicts a major challenge for legged, terrestrial locomotion. Locomotor support requirements scale identically with body mass (α M1), while force-generation capacity should scale α M2/3 as it depends on muscle cross-sectional area. Mammals compensate with more upright limb postures at larger sizes, but it remains unknown how sprawling tetrapods deal with this challenge. Varanid lizards are an ideal group to address this question because they cover an enormous body size range while maintaining a similar bent-limb posture and body proportions. This study reports the scaling of ground reaction forces and duty factor for varanid lizards ranging from 7 g to 37 kg. Impulses (force×time) (α M0.99-1.34) and peak forces (α M0.73-1.00) scaled higher than expected. Duty factor scaled α M0.04 and was higher for the hindlimb than the forelimb. The proportion of vertical impulse to total impulse increased with body size, and impulses decreased while peak forces increased with speed.

Monitoring muscle over three orders of magnitude: Widespread positive allometry among locomotor and body support musculature in the pectoral girdle of varanid lizards (Varanidae).

There is a functional trade-off in the design of skeletal muscle. Muscle strength depends on the number of muscle fibers in parallel, while shortening velocity and operational distance depend on fascicle length, leading to a trade-off between the maximum force a muscle can produce and its ability to change length and contract rapidly. This trade-off becomes even more pronounced as animals increase in size because muscle strength scales with area (length2 ) while body mass scales with volume (length3 ). In order to understand this muscle trade-off and how animals deal with the biomechanical consequences of size, we investigated muscle properties in the pectoral girdle of varanid lizards. Varanids are an ideal group to study the scaling of muscle properties because they retain similar body proportions and posture across five orders of magnitude in body mass and are highly active, terrestrially adapted reptiles. We measured muscle mass, physiological cross-sectional area, fascicle length, proximal and distal tendon lengths, and proximal and distal moment arms for 27 pectoral girdle muscles in 13 individuals across 8 species ranging from 64 g to 40 kg. Standard and phylogenetically informed reduced major axis regression was used to investigate how muscle architecture properties scale with body size. Allometric growth was widespread for muscle mass (scaling exponent >1), physiological cross-sectional area (scaling exponent >0.66), but not tendon length (scaling exponent >0.33). Positive allometry for muscle mass was universal among muscles responsible for translating the trunk forward and flexing the elbow, and nearly universal among humeral protractors and wrist flexors. Positive allometry for PCSA was also common among trunk translators and humeral protractors, though less so than muscle mass. Positive scaling for fascicle length was not widespread, but common among humeral protractors. A higher proportion of pectoral girdle muscles scaled with positive allometry than our previous work showed for the pelvic girdle, suggesting that the center of mass may move cranially with body size in varanids, or that the pectoral girdle may assume a more dominant role in locomotion in larger species. Scaling exponents for physiological cross-sectional area among muscles primarily associated with propulsion or with a dual role were generally higher than those associated primarily with support against gravity, suggesting that locomotor demands have at least an equal influence on muscle architecture as body support. Overall, these results suggest that larger varanids compensate for the increased biomechanical demands of locomotion and body support at higher body sizes by developing larger pectoral muscles with higher physiological cross-sectional areas. The isometric scaling rates for fascicle length among locomotion-oriented pectoral girdle muscles suggest that larger varanids may be forced to use shorter stride lengths, but this problem may be circumvented by increases in limb excursion afforded by the sliding coracosternal joint.

Where Have All the Giants Gone? How Animals Deal with the Problem of Size.

The survival of both the hunter and the hunted often comes down to speed. Yet how fast an animal can run is intricately linked to its size, such that the fastest animals are not the biggest nor the smallest. The ability to maintain high speeds is dependent on the body's capacity to withstand the high stresses involved with locomotion. Yet even when standing still, scaling principles would suggest that the mechanical stress an animal feels will increase in greater demand than its body can support. So if big animals want to be fast, they must find solutions to overcome these high stresses. This article explores the ways in which extant animals mitigate size-related increases in musculoskeletal stress in an effort to help understand where all the giants have gone.

Not all urban landscapes are the same: interactions between urban land use and stress in a large herbivorous mammal.

Urbanization significantly impacts the health and viability of wildlife populations yet it is not well understood how urban landscapes differ from non-urban landscapes with regard to their effects on wildlife. This study investigated the physiological response of eastern grey kangaroos (Macropus giganteus) to land use at a landscape scale. Using fecal glucocorticoid metabolites (FGM) we compared stress levels of kangaroo populations in urban and non-urban environments. We modeled FGM concentrations from 24 kangaroo populations against land use (urban or non-urban) and other anthropogenic and environmental factors, using a linear modeling approach. We found that land use was a significant predictor of FGM concentrations in eastern grey kangaroos with significant differences in concentrations between urban and non-urban populations. However, the direction of the relationship differed between northern and southern regions of Australia. In the northern study sites, kangaroos in urban areas had significantly higher FGM levels than their non-urban counterparts. In contrast, in southern sites, where kangaroos occur in high densities in many urban areas, urban kangaroos had lower FGM concentrations than non-urban kangaroos. Rainfall and temperature were also significant predictors of FGM and the direction of the relationship was consistent across both regions. These results are consistent with the contrasting abundance and persistence of kangaroo populations within the urban matrix between the two study regions. In the northern region many populations have declined over the last two decades and are fragmented, also occurring at lower densities than in southern sites. Our study indicates that it is the characteristics of urban environments, rather than the urban environment per se, which determines the extent of impacts of urbanization on kangaroos. This research provides insights into how the design of urban landscapes can influence large mammal populations.

Quantifying koala locomotion strategies: implications for the evolution of arborealism in marsupials.

The morphology and locomotor performance of a species can determine their inherent fitness within a habitat type. Koalas have an unusual morphology for marsupials, with several key adaptations suggested to increase stability in arboreal environments. We quantified the kinematics of their movement over ground and along narrow arboreal trackways to determine the extent to which their locomotion resembled that of primates, occupying similar niches, or basal marsupials from which they evolved. On the ground, the locomotion of koalas resembled a combination of marsupial behaviours and primate-like mechanics. For example, their fastest strides were bounding type gaits with a top speed of 2.78 m s-1 (mean 1.20 m s-1), resembling marsupials, while the relatively longer stride length was reflective of primate locomotion. Speed was increased using equal modification of stride length and frequency. On narrow substrates, koalas took longer but slower strides (mean 0.42 m s-1), adopting diagonally coupled gaits including both lateral and diagonal sequence gaits, the latter being a strategy distinctive among arboreal primates. The use of diagonally coupled gaits in the arboreal environment is likely only possible because of the unique gripping hand morphology of both the fore and hind feet of koalas. These results suggest that during ground locomotion, they use marsupial-like strategies but alternate to primate-like strategies when moving amongst branches, maximising stability in these environments. The locomotion strategies of koalas provide key insights into an independent evolutionary branch for an arboreal specialist, highlighting how locomotor strategies can convergently evolve between distant lineages.

Moving in complex environments: a biomechanical analysis of locomotion on inclined and narrow substrates.

Characterisation of an organism's performance in different habitats provides insight into the conditions that allow it to survive and reproduce. In recent years, the northern quoll (Dasyurus hallucatus) - a medium-sized semi-arboreal marsupial native to northern Australia - has undergone significant population declines within open forest, woodland and riparian habitats, but less so in rocky areas. To help understand this decline, we quantified the biomechanical performance of wild northern quolls as they ran up inclined narrow (13 mm pole) and inclined wide (90 mm platform) substrates. We predicted that quolls may possess biomechanical adaptations to increase stability on narrow surfaces, which are more common in rocky habitats. Our results showed that quolls have some biomechanical characteristics consistent with a stability advantage on narrow surfaces. This includes the coupled use of limb pairs, as indicated via a decrease in footfall time, and an ability to produce corrective torques to counteract the toppling moments commonly encountered during gait on narrow surfaces. However, speed was constrained on narrow surfaces, and quolls did not adopt diagonal sequence gaits, unlike true arboreal specialists such as primates. In comparison with key predators, such as cats and dogs, northern quolls appear inferior in terrestrial environments but have a stability advantage at higher speeds on narrow supports. This may partially explain the heterogeneous declines in northern quoll populations among various habitats on mainland Australia.

Extreme positive allometry of animal adhesive pads and the size limits of adhesion-based climbing.

Organismal functions are size-dependent whenever body surfaces supply body volumes. Larger organisms can develop strongly folded internal surfaces for enhanced diffusion, but in many cases areas cannot be folded so that their enlargement is constrained by anatomy, presenting a problem for larger animals. Here, we study the allometry of adhesive pad area in 225 climbing animal species, covering more than seven orders of magnitude in weight. Across all taxa, adhesive pad area showed extreme positive allometry and scaled with weight, implying a 200-fold increase of relative pad area from mites to geckos. However, allometric scaling coefficients for pad area systematically decreased with taxonomic level and were close to isometry when evolutionary history was accounted for, indicating that the substantial anatomical changes required to achieve this increase in relative pad area are limited by phylogenetic constraints. Using a comparative phylogenetic approach, we found that the departure from isometry is almost exclusively caused by large differences in size-corrected pad area between arthropods and vertebrates. To mitigate the expected decrease of weight-specific adhesion within closely related taxa where pad area scaled close to isometry, data for several taxa suggest that the pads' adhesive strength increased for larger animals. The combination of adjustments in relative pad area for distantly related taxa and changes in adhesive strength for closely related groups helps explain how climbing with adhesive pads has evolved in animals varying over seven orders of magnitude in body weight. Our results illustrate the size limits of adhesion-based climbing, with profound implications for large-scale bio-inspired adhesives.

Surface friction alters the agility of a small Australian marsupial.

Movement speed can underpin an animal's probability of success in ecological tasks. Prey often use agility to outmanoeuvre predators; however, faster speeds increase inertia and reduce agility. Agility is also constrained by grip, as the foot must have sufficient friction with the ground to apply the forces required for turning. Consequently, ground surface should affect optimum turning speed. We tested the speed-agility trade-off in buff-footed antechinus (Antechinus mysticus) on two different surfaces. Antechinus used slower turning speeds over smaller turning radii on both surfaces, as predicted by the speed-agility trade-off. Slipping was 64% more likely on the low-friction surface, and had a higher probability of occurring the faster the antechinus were running before the turn. However, antechinus compensated for differences in surface friction by using slower pre-turn speeds as their amount of experience on the low-friction surface increased, which consequently reduced their probability of slipping. Conversely, on the high-friction surface, antechinus used faster pre-turn speeds in later trials, which had no effect on their probability of slipping. Overall, antechinus used larger turning radii (0.733±0.062 versus 0.576±0.051 m) and slower pre-turn (1.595±0.058 versus 2.174±0.050 m s-1) and turning speeds (1.649±0.061 versus 2.01±0.054 m s-1) on the low-friction surface. Our results demonstrate the interactive effect of surface friction and the speed-agility trade-off on speed choice. To predict wild animals' movement speeds, future studies should examine the interactions between biomechanical trade-offs and terrain, and quantify the costs of motor mistakes in different ecological activities.

The effects of cracks on the quantification of the cancellous bone fabric tensor in fossil and archaeological specimens: a simulation study.

Cancellous bone is very sensitive to its prevailing mechanical environment, and study of its architecture has previously aided interpretations of locomotor biomechanics in extinct animals or archaeological populations. However, quantification of architectural features may be compromised by poor preservation in fossil and archaeological specimens, such as post mortem cracking or fracturing. In this study, the effects of post mortem cracks on the quantification of cancellous bone fabric were investigated through the simulation of cracks in otherwise undamaged modern bone samples. The effect on both scalar (degree of fabric anisotropy, fabric elongation index) and vector (principal fabric directions) variables was assessed through comparing the results of architectural analyses of cracked vs. non-cracked samples. Error was found to decrease as the relative size of the crack decreased, and as the orientation of the crack approached the orientation of the primary fabric direction. However, even in the best-case scenario simulated, error remained substantial, with at least 18% of simulations showing a > 10% error when scalar variables were considered, and at least 6.7% of simulations showing a > 10° error when vector variables were considered. As a 10% (scalar) or 10° (vector) difference is probably too large for reliable interpretation of a fossil or archaeological specimen, these results suggest that cracks should be avoided if possible when analysing cancellous bone architecture in such specimens.

How to build your dragon: scaling of muscle architecture from the world's smallest to the world's largest monitor lizard.

BACKGROUND: The functional design of skeletal muscles is shaped by conflicting selective pressures between support and propulsion, which becomes even more important as animals get larger. If larger animals were geometrically scaled up versions of smaller animals, increases in body size would cause an increase in musculoskeletal stress, a result of the greater scaling of mass in comparison to area. In large animals these stresses would come dangerously close to points of failure. By examining the architecture of 22 hindlimb muscles in 27 individuals from 9 species of varanid lizards ranging from the tiny 7.6 g Varanus brevicauda to the giant 40 kg Varanus komodoensis, we present a comprehensive dataset on the scaling of musculoskeletal architecture in monitor lizards (varanids), providing information about the phylogenetic constraints and adaptations of locomotor muscles in sprawling tetrapods. RESULTS: Scaling results for muscle mass, pennation and physiological cross-sectional area (PCSA), all suggest that larger varanids increase the relative force-generating capacity of femur adductors, knee flexors and ankle plantarflexors, with scaling exponents greater than geometric similarity predicts. Thus varanids mitigate the size-related increases in stress by increasing muscle mass and PCSA rather than adopting a more upright posture with size as is shown in other animals. As well as the scaling effects of muscle properties with body mass, the variation in muscle architecture with changes in hindlimb posture were also prominent. Within varanids, posture varies with habitat preference. Climbing lizards display a sprawling posture while terrestrial lizards display a more upright posture. Sprawling species required larger PCSAs and muscle masses in femur retractors, knee flexors, and ankle plantarflexors in order to support the body. CONCLUSIONS: Both size and posture-related muscle changes all suggest an increased role in support over propulsion, leading to a decrease in locomotor performance which has previously been shown with increases in size. These estimates suggest the giant Pleistocene varanid lizard (Varanus megalania priscus) would likely not have been able to outrun early humans with which it co-habitated the Australian landmass with.

The private life of echidnas: using accelerometry and GPS to examine field biomechanics and assess the ecological impact of a widespread, semi-fossorial monotreme.

The short-beaked echidna (Tachyglossus aculeatus) is a monotreme and therefore provides a unique combination of phylogenetic history, morphological differentiation and ecological specialisation for a mammal. The echidna has a unique appendicular skeleton, a highly specialised myrmecophagous lifestyle and a mode of locomotion that is neither typically mammalian nor reptilian, but has aspects of both lineages. We therefore were interested in the interactions of locomotor biomechanics, ecology and movements for wild, free-living short-beaked echidnas. To assess locomotion in its complex natural environment, we attached both GPS and accelerometer loggers to the back of echidnas in both spring and summer. We found that the locomotor biomechanics of echidnas is unique, with lower stride length and stride frequency than reported for similar-sized mammals. Speed modulation is primarily accomplished through changes in stride frequency, with a mean of 1.39 Hz and a maximum of 2.31 Hz. Daily activity period was linked to ambient air temperature, which restricted daytime activity during the hotter summer months. Echidnas had longer activity periods and longer digging bouts in spring compared with summer. In summer, echidnas had higher walking speeds than in spring, perhaps because of the shorter time suitable for activity. Echidnas spent, on average, 12% of their time digging, which indicates their potential to excavate up to 204 m3 of soil a year. This information highlights the important contribution towards ecosystem health, via bioturbation, of this widespread Australian monotreme.

Morphology and burrowing energetics of semi-fossorial skinks (Liopholis spp.).

Burrowing is an important form of locomotion in reptiles, but no study has examined the energetic cost of burrowing for reptiles. This is significant because burrowing is the most energetically expensive mode of locomotion undertaken by animals and many burrowing species therefore show specialisations for their subterranean lifestyle. We examined the effect of temperature and substrate characteristics (coarse sand or fine sand) on the net energetic cost of burrowing (NCOB) and burrowing rate in two species of the Egernia group of skinks (Liopholis striata and Liopholis inornata) compared with other burrowing animals. We further tested for morphological specialisations among burrowing species by comparing the relationship between body shape and retreat preference in Egernia group skinks. For L. striata and L. inornata, NCOB is 350 times more expensive than the predicted cost of pedestrian terrestrial locomotion. Temperature had a positive effect on burrowing rate for both species, and a negative effect on NCOB for L. striata but not L. inornata. Both NCOB and burrowing rate were independent of substrate type. Burrows constructed by skinks had a smaller cross-sectional area than those constructed by mammals of comparable mass, and NCOB of skinks was lower than that of mammals of similar mass. After accounting for body size, retreat preference was significantly correlated with body shape in Egernia group skinks. Species of Egernia group skinks that use burrows for retreats have narrower bodies and shorter front limbs than other species. We conclude that the morphological specialisations of burrowing skinks allow them to construct relatively narrow burrows, thereby reducing NCOB and the total cost of constructing their burrow retreats.

Dynamic similarity and the peculiar allometry of maximum running speed.

Animal performance fundamentally influences behaviour, ecology, and evolution. It typically varies monotonously with size. A notable exception is maximum running speed; the fastest animals are of intermediate size. Here we show that this peculiar allometry results from the competition between two musculoskeletal constraints: the kinetic energy capacity, which dominates in small animals, and the work capacity, which reigns supreme in large animals. The ratio of both capacities defines the physiological similarity index Γ, a dimensionless number akin to the Reynolds number in fluid mechanics. The scaling of Γ indicates a transition from a dominance of muscle forces to a dominance of inertial forces as animals grow in size; its magnitude defines conditions of "dynamic similarity" that enable comparison and estimates of locomotor performance across extant and extinct animals; and the physical parameters that define it highlight opportunities for adaptations in musculoskeletal "design" that depart from the eternal null hypothesis of geometric similarity. The physiological similarity index challenges the Froude number as prevailing dynamic similarity condition, reveals that the differential growth of muscle and weight forces central to classic scaling theory is of secondary importance for the majority of terrestrial animals, and suggests avenues for comparative analyses of locomotor systems.

Lizard tricks: overcoming conflicting requirements of speed versus climbing ability by altering biomechanics of the lizard stride.

Adaptations promoting greater performance in one habitat are thought to reduce performance in others. However, there are many examples of animals in which, despite habitat differences, such predicted differences in performance do not occur. One such example is the relationship between locomotory performance to habitat for varanid lizards. To explain the lack of difference in locomotor performance we examined detailed observations of the kinematics of each lizard's stride. Differences in kinematics were greatest between climbing and non-climbing species. For terrestrial lizards, the kinematics indicated that increased femur adduction, femur rotation and ankle angle all contributed positively to changes in stride length, but they were constrained for climbing species, probably because of biomechanical restrictions on the centre of mass height (to increase stability on vertical surfaces). Despite climbing species having restricted stride length, no differences have been previously reported in sprint speed between climbing and non-climbing varanids. This is best explained by climbing varanids using an alternative speed modulation strategy of varying stride frequency to avoid the potential trade-off of speed versus stability on vertical surfaces. Thus, by measuring the relevant biomechanics for lizard strides, we have shown how kinematic differences among species can mask performance differences typically associated with habitat variation.

Multilevel dynamic adjustments of geckos (Hemidactylus frenatus) climbing vertically: head-up versus head-down.

Many climbing animals use direction-dependent adhesives to attach to vertical or inclined surfaces. These structures adhere when activated via a pull but detach when pushed. Therefore, a challenge arises when a change in climbing direction causes external forces such as gravity to change its acting orientation upon the lizard. To investigate how specialized climbers adjust, we studied kinematics and dynamics of six Hemidactylus frenatus geckos climbing head-up and head-down a vertical racetrack. We found that limbs functionally swap their adhesive role: feet above the centre of mass (COM) generated adhesive forces, feet below the COM compressive forces, both equal in magnitude across directions. To investigate how lizards perform this swap, despite the constraint of their direction-dependent adhesives, we analysed kinematic adjustments across multiple smaller levels of hierarchy: limbs, feet and toes. All levels contributed: the hindfoot angle was reoriented realigning the adhesive structure, the hindlimb centre range of motion was further protracted and the hindfoot toe spreading was reduced. Notably, all three variables were adjustments of hindlimbs, suggesting that they make a more flexible contribution in upward versus downward climbing, while forelimbs may be anatomically or functionally constrained. The relevance of multilevel dynamic adjustments might inform the development of performant gaits for legged climbing robots.