Prepared for landing: A simple activation strategy scales muscle force to landing height.

Before landing from a jump or fall, animals preactivate muscles to stiffen their limb joints but it is unclear how muscles tune limb stiffness and how collision forcefulness is anticipated. We measured electromyography and force from the lateral gastrocnemius muscle during landings in turkeys, an animal model that allows for direct measurements of muscle force. Many studies of landings in humans and other animals have found the duration of muscle preactivation to be constant, starting approximately 100 ms before impact, irrespective of fall duration. Therefore, we hypothesized a lack of relationship between fall duration (as dictated by drop height), muscle activity onset-time, and force at toe-down. Contrary to our expectations, both muscle activity and force rose from briefly after fall initiation until toe-down. Preactivation duration was proportional to fall height, while the rate of force rise was consistent across drop heights, resulting in force at landing and leg stiffness being proportional to fall height. Onset of muscle activity lagged 22 ± 7 ms (mean ± S.E.M.) from fall initiation, consistent with a reflex response initiation of the force ramp-up. Together, our results suggest that a constant (clock-like) rate of motor unit recruitment, initiated at fall initiation provides a preactivation that is proportional to drop height. The result is a tuning of pre-landing muscle force, providing a limb stiffening that is proportional to impact intensity, possibly without using information about fall distance.

Do salamanders chew? An X-ray reconstruction of moving morphology analysis of ambystomatid intraoral feeding behaviours.

Chewing is widespread across vertebrates, including mammals, lepidosaurs, and ray-finned and cartilaginous fishes, yet common wisdom about one group-amphibians-is that they swallow food whole, without processing. Earlier salamander studies lacked analyses of internal kinematics of the tongue, analyses of muscle function, and sampled few individuals, which may have caused erroneous conclusions. Specifically, without tongue and food kinematics, intraoral behaviours are difficult to disambiguate. We hypothesized that ambystomatid salamanders use diverse intraoral behaviours, including chewing, and tested this hypothesis with biplanar videofluoroscopy, X-ray reconstruction of moving morphology, and fluoromicrometry. We generated musculoskeletal kinematic profiles for intraoral behaviours in Axolotls (Ambystoma mexicanum), including three-dimensional skeletal kinematics associated with feeding, for gape, cranial and pectoral girdle rotations, and tongue translations. We also measured muscle fibre and muscle-tendon unit strains for six muscles involved in generating skull, jaw and tongue kinematics (adductor mandibulae, depressor mandibulae, geniohyoid, sternohyoid, epaxialis and hypaxialis). A principal component analysis recovered statistically significant differences between behaviour cycles, classified based on food movements as either chewing or transport. Thus, our data suggest that ambystomatid salamanders use a previously unrecognized diversity of intraoral behaviours, including chewing. Combined with existing knowledge, our data suggest that chewing is a basal trait for tetrapods and jaw-bearing vertebrates. This article is part of the theme issue 'Food processing and nutritional assimilation in animals'.

Using salamanders as model taxa to understand vertebrate feeding constraints during the late Devonian water-to-land transition.

The vertebrate water-to-land transition and the rise of tetrapods brought about fundamental changes for the groups undergoing these evolutionary changes (i.e. stem and early tetrapods). These groups were forced to adapt to new conditions, including the distinct physical properties of water and air, requiring fundamental changes in anatomy. Nutrition (or feeding) was one of the prime physiological processes these vertebrates had to successfully adjust to change from aquatic to terrestrial life. The basal gnathostome feeding mode involves either jaw prehension or using water flows to aid in ingestion, transportation and food orientation. Meanwhile, processing was limited primarily to simple chewing bites. However, given their comparatively massive and relatively inflexible hyobranchial system (compared to the more muscular tongue of many tetrapods), it remains fraught with speculation how stem and early tetrapods managed to feed in both media. Here, we explore ontogenetic water-to-land transitions of salamanders as functional analogues to model potential changes in the feeding behaviour of stem and early tetrapods. Our data suggest two scenarios for terrestrial feeding in stem and early tetrapods as well as the presence of complex chewing behaviours, including excursions of the jaw in more than one dimension during early developmental stages. Our results demonstrate that terrestrial feeding may have been possible before flexible tongues evolved. This article is part of the theme issue 'Food processing and nutritional assimilation in animals'.

Introduction: food processing and nutritional assimilation in animals.

How animals process and absorb nutrients from their food is a fundamental question in biology. Despite the continuity and interaction between intraoral food processing and post-oesophageal nutritional extraction, these topics have largely been studied separately. At present, we lack a synthesis of how pre- and post-oesophageal mechanisms of food processing shape the ability of various taxa to effectively assimilate nutrients from their diet. The aim of this special issue is to catalyse a unification of these distinct approaches as a functional continuum. We highlight questions that derive from this synthesis, as well as technical advances to address these questions. At present, there is also a skew toward vertebrates in studies of feeding form-function mechanics; by including perspectives from researchers working on both vertebrates and invertebrates, we hope to stimulate integrative and comparative research on food processing and nutritional assimilation. Below, we discuss how the papers in this issue contribute to these goals in three areas: championing a functional-comparative approach, quantifying performance and emphasizing the effects of life history, and food substrate and extrinsic factors in current and future studies of oral food processing and nutritional assimilation. This article is part of the theme issue 'Food processing and nutritional assimilation in animals'.

Rhythmic chew cycles with distinct fast and slow phases are ancestral to gnathostomes.

Intra-oral food processing, including chewing, is important for safe swallowing and efficient nutrient assimilation across tetrapods. Gape cycles in tetrapod chewing consist of four phases (fast open and -close, and slow open and -close), with processing mainly occurring during slow close. Basal aquatic-feeding vertebrates also process food intraorally, but whether their chew cycles are partitioned into distinct phases, and how rhythmic their chewing is, remains unknown. Here, we show that chew cycles from sharks to salamanders are as rhythmic as those of mammals, and consist of at least three, and often four phases, with phase distinction occasionally lacking during jaw opening. In fishes and aquatic-feeding salamanders, fast open has the most variable duration, more closely resembling mammals than basal amniotes (lepidosaurs). Across ontogenetically or behaviourally mediated terrestrialization, salamanders show a distinct pattern of the second closing phase (near-contact) being faster than the first, with no clear pattern in partitioning of variability across phases. Our results suggest that distinct fast and slow chew cycle phases are ancestral for jawed vertebrates, followed by a complicated evolutionary history of cycle phase durations and jaw velocities across fishes, basal tetrapods and mammals. These results raise new questions about the mechanical and sensorimotor underpinnings of vertebrate food processing. This article is part of the theme issue 'Food processing and nutritional assimilation in animals'.

Bridging the muscle genome to phenome across multiple biological scales.

Muscle is highly hierarchically organized, with functions shaped by genetically controlled expression of protein ensembles with different isoform profiles at the sarcomere scale. However, it remains unclear how isoform profiles shape whole-muscle performance. We compared two mouse hindlimb muscles, the slow, relatively parallel-fibered soleus and the faster, more pennate-fibered tibialis anterior (TA), across scales: from gene regulation, isoform expression and translation speed, to force-length-velocity-power for intact muscles. Expression of myosin heavy-chain (MHC) isoforms directly corresponded with contraction velocity. The fast-twitch TA with fast MHC isoforms had faster unloaded velocities (actin sliding velocity, Vactin; peak fiber velocity, Vmax) than the slow-twitch soleus. For the soleus, Vactin was biased towards Vactin for purely slow MHC I, despite this muscle's even fast and slow MHC isoform composition. Our multi-scale results clearly identified a consistent and significant dampening in fiber shortening velocities for both muscles, underscoring an indirect correlation between Vactin and fiber Vmax that may be influenced by differences in fiber architecture, along with internal loading due to both passive and active effects. These influences correlate with the increased peak force and power in the slightly more pennate TA, leading to a broader length range of near-optimal force production. Conversely, a greater force-velocity curvature in the near-parallel fibered soleus highlights the fine-tuning by molecular-scale influences including myosin heavy and light chain expression along with whole-muscle characteristics. Our results demonstrate that the individual gene, protein and whole-fiber characteristics do not directly reflect overall muscle performance but that intricate fine-tuning across scales shapes specialized muscle function.

Modelling the complexity of the foot and ankle during human locomotion: the development and validation of a multi-segment foot model using biplanar videoradiography.

We developed and validated a multi-segment foot and ankle model for human walking and running. The model has 6-segments, and 7 degrees of freedom; motion between foot segments were constrained with a single oblique axis to enable triplanar motion [Joint Constrained (JC) model]. The accuracy of the JC model and that of a conventional model using a 6 degrees of freedom approach were assessed by comparison to segment motion determined with biplanar videoradiography. Compared to the 6-DoF model, our JC model demonstrated significantly smaller RMS differences [JC: 2.19° (1.43-2.73); 6-DoF: 3.25° (1.37-5.89)] across walking and running. The JC model is thus capable of more accurate musculoskeletal analyses and is also well suited for predictive simulations.

Next Steps in Integrative Biology: Mapping Interactive Processes Across Levels of Biological Organization.

Emergent biological processes result from complex interactions within and across levels of biological organization, ranging from molecular to environmental dynamics. Powerful theories, database tools, and modeling methods have been designed to characterize network connections within levels, such as those among genes, proteins, biochemicals, cells, organisms, and species. Here, we propose that developing integrative models of organismal function in complex environments can be facilitated by taking advantage of these methods to identify key nodes of communication across levels of organization. Mapping key drivers or connections among levels of organization will provide data and leverage to model potential rule-sets by which organisms respond and adjust to perturbations at any level of biological organization.

Thermal Sensitivity of Axolotl Feeding Behaviors.

Musculoskeletal movement results from muscle contractions, recoil of elastic tendons, aponeuroses, and ligaments, or combinations thereof. Muscular and elastic contributions can vary both across behaviors and with changes in temperature. Skeletal muscles reach peak contraction speed at a temperature optimum with performance declining away from that optimum by approximately 50% per 10°C, following the Q10 principle. Elastic recoil action, however, is less temperature sensitive. We subjected Axolotls (Ambystoma mexicanum) to changes from warm (23°C), via medium (14°C), to cold (6°C) temperature across most of their thermal tolerance range, and recorded jaw kinematics during feeding on crickets. We sought to determine if suction feeding strikes and food processing chews involve elastic mechanisms and, specifically, if muscular versus elastic contribution vary with temperature for gape opening and closing. Measurements of peak and mean speed for gape opening and closing during strikes and chews across temperature treatments were compared with Q10-based predictions. We found that strike gape speed decreased significantly from warm and medium to cold treatments, indicating low thermal robustness, and no performance-enhancement due to elastic recoil. For chews, peak, and mean gape closing speeds, as well as peak gape opening speed, also decreased significantly from warm to cold treatments. However, peak gape opening and closing speeds for chews showed performance-enhancement, consistent with a previously demonstrated presence of elastic action in the Axolotl jaw system. Our results add to a relatively small body of evidence suggesting that elastic recoil plays significant roles in aquatic vertebrate feeding systems, and in cyclic food processing mechanisms.

Protein Source and Muscle Health in Older Adults: A Literature Review.

Research shows that higher dietary protein of up to 1.2 g/kgbodyweight/day may help prevent sarcopenia and maintain musculoskeletal health in older individuals. Achieving higher daily dietary protein levels is challenging, particularly for older adults with declining appetites and underlying health conditions. The negative impact of these limitations on aging muscle may be circumvented through the consumption of high-quality sources of protein and/or supplementation. Currently, there is a debate regarding whether source of protein differentially affects musculoskeletal health in older adults. Whey and soy protein have been used as the most common high-quality proteins in recent literature. However, there is growing consumer demand for additional plant-sourced dietary protein options. For example, pea protein is rapidly gaining popularity among consumers, despite little to no research regarding its long-term impact on muscle health. Therefore, the objectives of this review are to: (1) review current literature from the past decade evaluating whether specific source(s) of dietary protein provide maximum benefit to muscle health in older adults; and (2) highlight the need for future research specific to underrepresented plant protein sources, such as pea protein, to then provide clearer messaging surrounding plant-sourced versus animal-sourced protein and their effects on the aging musculoskeletal system.

Effect of muscle stimulation intensity on the heterogeneous function of regions within an architecturally complex muscle.

Skeletal muscle has fiber architectures ranging from simple to complex, alongside variations in fiber-type and neuro-anatomical compartmentalization. However, the functional implications of muscle subdivision into discrete functional units remain poorly understood. The rat medial gastrocnemius has well-characterized regions with distinct architectures and fiber type composition. Here, force-length and force-velocity contractions were performed for two stimulation intensities (supramaximal and submaximal) and for three structural units (whole muscle belly, proximal region, and distal region) to assess the effect of muscle compartmentalization on contractile force-length-velocity relationships and optimal speed for power production. Additionally, fiber strain, fiber rotation, pennation, and architectural gearing were quantified. Our results suggest that the proximal and distal muscle regions have fundamentally different physiological function. During supramaximal activation, the proximal region has shorter (8.4 ± 0.8 mm versus 10.9 ± 0.7 mm) fibers and steeper (28.7 ± 11.0° versus 19.6 ± 6.3°) fiber angles at optimum length, and operates over a larger (17.9 ± 3.8% versus 12.6 ± 2.7%) range of its force-length curve. The proximal region also exhibits larger changes in pennation angle (5.6 ± 2.2°/mm versus 2.4 ± 1.5°/mm muscle shortening) and architectural gearing (1.82 ± 0.53 versus 1.25 ± 0.24), whereas the distal region exhibits greater peak shortening speed (96.0 mm/s versus 81.3 mm/s) and 18-27% greater optimal speed. Overall, similar patterns were observed during submaximal activation. These regional differences in physiological function with respect to the whole muscle highlight how variation in motor recruitment could fundamentally shift regional functional patterns within a single muscle, which likely has important implications for whole muscle force and work output in vivo.NEW & NOTEWORTHY We show that muscle compartmentalization can influence whole muscle contractile properties, with slower-fibered proximal rat medial gastrocnemius undergoing larger changes in pennation angle and architectural gearing, whereas the faster-fibered distal region achieves greater peak and optimal shortening velocity, and power output. Consequently, regional variation in motor recruitment can fundamentally influence functional patterns within a single muscle.

Ontogenetic plasticity in cranial morphology is associated with a change in the food processing behavior in Alpine newts.

BACKGROUND: The feeding apparatus of salamanders consists mainly of the cranium, mandible, teeth, hyobranchial apparatus and the muscles of the cranial region. The morphology of the feeding apparatus in turn determines the boundary conditions for possible food processing (i.e., intraoral mechanical reduction) mechanisms. However, the morphology of the feeding apparatus changes substantially during metamorphosis, prompting the hypothesis that larvae might use a different food processing mechanism than post-metamorphic adults. Salamandrid newts with facultative metamorphosis are suitable for testing this hypothesis as adults with divergent feeding apparatus morphologies often coexist in the same population, share similar body sizes, and feed on overlapping prey spectra. METHODS: We use high-speed videography to quantify the in vivo movements of key anatomical elements during food processing in paedomorphic and metamorphic Alpine newts (Ichthyosaura alpestris). Additionally, we use micro-computed tomography (µCT) to analyze morphological differences in the feeding apparatus of paedomorphic and metamorphic Alpine newts and sort them into late-larval, mid-metamorphic and post-metamorphic morphotypes. RESULTS: Late-larval, mid-metamorphic and post-metamorphic individuals exhibited clear morphological differences in their feeding apparatus. Regardless of the paedomorphic state being externally evident, paedomorphic specimens can conceal different morphotypes (i.e., late-larval and mid-metamorphic morphotypes). Though feeding on the same prey under the same (aquatic) condition, food processing kinematics differed between late-larval, mid-metamorphic and post-metamorphic morphotypes. CONCLUSIONS: The food processing mechanism in the Alpine newt changes along with morphology of the feeding apparatus during ontogeny, from a mandible-based to a tongue-based processing mechanism as the changing morphology of the mandible prevents chewing and the tongue allows enhanced protraction. These results could indicate that early tetrapods, in analogy to salamanders, may have developed new feeding mechanisms in their aquatic environment and that these functional innovations may have later paved the way for terrestrial feeding mechanisms.

Flexibility of intraoral food processing in the salamandrid newt Triturus carnifex: effects of environment and prey type.

Intraoral food processing mechanisms are known for all major vertebrate groups, but the form and function of systems used to crush, grind or puncture food items can differ substantially between and within groups. Most vertebrates display flexible mechanisms of intraoral food processing with respect to different environmental conditions or food types. It has recently been shown that newts use cyclical loop-motions of the tongue to rasp prey against the palatal dentition. However, it remains unknown whether newts can adjust their food processing behavior in response to different food types or environmental conditions. Newts are interesting models for studying the functional adaptation to different conditions because of their unique and flexible lifestyle: they seasonally change between aquatic and terrestrial habitats, adapt their prey-capture mode to the respective environment, and consume diverse food types with different mechanical properties. Using X-ray high-speed recordings, anatomical investigations, behavioral analyses and mechanical property measurements, we tested the effects of the medium in which feeding occurs (water/air) and the food type (maggot, earthworm, cricket) on the processing behavior in Triturus carnifex We discovered that food processing, by contrast to prey capture, differed only slightly between aquatic and terrestrial habitats. However, newts adjusted the number of processing cycles to different prey types: while maggots were processed extensively, earthworm pieces were barely processed at all. We conclude that, in addition to food mechanical properties, sensory feedback such as smell and taste appear to induce flexible processing responses, while the medium in which feeding occurs appears to have less of an effect.

Added mass in rat plantaris muscle causes a reduction in mechanical work.

Most of what we know about whole muscle behaviour comes from experiments on single fibres or small muscles that are scaled up in size without considering the effects of the additional muscle mass. Previous modelling studies have shown that tissue inertia acts to slow the rate of force development and maximum velocity of muscle during shortening contractions and decreases the work and power per cycle during cyclic contractions; however, these results have not yet been confirmed by experiments on living tissue. Therefore, in this study we conducted in situ work-loop experiments on rat plantaris muscle to determine the effects of increasing the mass of muscle on mechanical work during cyclic contractions. We additionally simulated these experimental contractions using a mass-enhanced Hill-type model to validate our previous modelling work. We found that greater added mass resulted in lower mechanical work per cycle relative to the unloaded trials in which no mass was added to the muscle (P=0.041 for both 85 and 123% increases in muscle mass). We additionally found that greater strain resulted in lower work per cycle relative to unloaded trials at the same strain to control for length change and velocity effects on the work output, possibly due to greater accelerations of the muscle mass at higher strains. These results confirm that tissue mass reduces muscle mechanical work at larger muscle sizes, and that this effect is likely amplified for lower activations.

Post-activation muscle potentiation and its relevance to cyclical behaviours.

Muscle can experience post-activation potentiation (PAP), a temporary increase in force and rate of force development, when contractions are closely timed; therefore, cyclical behaviours are likely affected by PAP, as succeeding contraction cycles can lead to potentiation over several subsequent cycles. Here, we examined PAP during in situ cyclical contractions of the mallard lateral gastrocnemius (LG). Surface swimming, a cyclical behaviour, was mimicked with work-loops using in vivo LG length change and stimulation parameters. Tests were performed at mallards' preferred cycle frequency as well as at lower and higher frequencies. Like muscles from mammals, anurans and arthropods, the mallard LG exhibited PAP with increases in peak force, average force rate and net work. Staircase potentiation occurred over two or more work-loop cycles, resulting in gradual increases in PAP. The number of cycles needed to reach maximum work varied with cycle frequency, requiring more cycles at higher cycle frequencies. PAP occurred under in vivo-like stimulation parameters, suggesting a potentially important role of PAP in animal locomotion, especially in cyclical behaviours.

Elastic recoil action amplifies jaw closing speed in an aquatic feeding salamander.

Tendon springs often influence locomotion by amplifying the speed and power of limb joint rotation. However, less is known about elastic recoil action in feeding systems, particularly for small aquatic animals. Here, we ask if elastic recoil amplifies the speed of gape closing during aquatic food processing in the Axolotl (Ambystoma mexicanum). We measure activation of the adductor mandibulae externus via electromyography and strain of the jaw adductor muscle-tendon unit (MTU), and gape kinematics via fluoromicrometry. The muscle is pre-activated coincident with gape opening, which causes MTU stretch. Activation lasts significantly shorter for fish than cricket processing, and muscle shortening during MTU lengthening yields significantly greater elastic strain for cricket processing. The speed of MTU shortening, which dictates the speed of gape closing is 2.5-4.4 times greater than the speed of the initial shortening of the muscle fascicles for fish and cricket gape cycles, respectively. These data demonstrate a clear role for elastic recoil, which may be unexpected for a MTU in a feeding system of a small, aquatic animal. Amplification of jaw-closing speed resulting from elastic recoil likely confers ecological advantages in reducing prey escape risks during food processing in a dense and viscous fluid environment.

Skeletal Muscle Shape Change in Relation to Varying Force Requirements Across Locomotor Conditions.

Contractions of skeletal muscles to generate in vivo movement involve dynamic changes in contractile and elastic tissue strains that likely interact to influence the force and work of a muscle. However, studies of the in vivo dynamics of skeletal muscle and tendon strains remain largely limited to bipedal animals, and rarely cover the broad spectra of movement requirements met by muscles that operate as motors, struts, or brakes across the various gaits that animals commonly use and conditions they encounter. Using high-speed bi-planar fluoromicrometry, we analyze in vivo strains within the rat medial gastrocnemius (MG) across a range of gait and slope conditions. These conditions require changes in muscle force ranging from decline walk (low) to incline gallop (high). Measurements are made from implanted (0.5-0.8 mm) tantalum spheres marking MG mid-belly width, mid-belly thickness, as well as strains of distal fascicles, the muscle belly, and the Achilles tendon. During stance, as the muscle contracts, muscle force increases linearly with respect to gait-slope combinations, and both shortening and lengthening fiber strains increase from approximately 5 to 15% resting length. Contractile change in muscle thickness (thickness strain) decreases (r 2 = 0.86; p = 0.001); whereas, the change in muscle width (width strain) increases (r 2 = 0.88; p = 0.001) and tendon strain increases (r 2 = 0.77; p = 0.015). Our results demonstrate force-dependency of contractile and tendinous tissue strains with compensatory changes in shape for a key locomotor muscle in the hind limb of a small quadruped. These dynamic changes are linked to the ability of a muscle to tune its force and work output as requirements change with locomotor speed and environmental conditions.

The Reliability of Foot and Ankle Bone and Joint Kinematics Measured With Biplanar Videoradiography and Manual Scientific Rotoscoping.

The intricate motion of the small bones of the feet are critical for its diverse function. Accurately measuring the 3-dimensional (3D) motion of these bones has attracted much attention over the years and until recently, was limited to invasive techniques or quantification of functional segments using multi-segment foot models. Biplanar videoradiography and model-based scientific rotoscoping offers an exciting alternative that allows us to focus on the intricate motion of individual bones in the foot. However, scientific rotoscoping, the process of rotating and translating a 3D bone model so that it aligns with the captured x-ray images, is either semi- or completely manual and it is unknown how much human error affects tracking results. Thus, the aim of this study was to quantify the inter- and intra-operator reliability of manually rotoscoping in vivo bone motion of the tibia, talus, and calcaneus during running. Three-dimensional CT bone volumes and high-speed biplanar videoradiography images of the foot were acquired on six participants. The six-degree-of-freedom motions of the tibia, talus, and calcaneus were determined using a manual markerless registration algorithm. Two operators performed the tracking, and additionally, the first operator re-tracked all bones, to test for intra-operator effects. Mean RMS errors were 1.86 mm and 1.90° for intra-operator comparisons and 2.30 mm and 2.60° for inter-operator comparisons across all bones and planes. The moderate to strong similarity values indicate that tracking bones and joint kinematics between sessions and operators is reliable for running. These errors are likely acceptable for defining gross joint angles. However, this magnitude of error may limit the capacity to perform advanced analyses of joint interactions, particularly those that require precise (sub-millimeter) estimates of bone position and orientation. Optimizing the view and image quality of the biplanar videoradiography system as well as the automated tracking algorithms for rotoscoping bones in the foot are required to reduce these errors and the time burden associated with the manual processing.

A salamander that chews using complex, three-dimensional mandible movements.

Most non-mammal tetrapods have a hinge-like jaw operation restricted to vertical opening and closing movements. Many mammal jaw joints, by contrast, operate in more complex, three-dimensional (3D) ways, involving not only vertical but also propalinal (rostro-caudal) and transverse (lateral) movements. Data on intraoral food processing in lissamphibians and sauropsids has prompted a generally accepted view that these groups mostly swallow food unreduced, and that in those cases where lissamphibians and sauropsids chew, they mostly use simple vertical jaw movements for food processing. The exception to this generally accepted view is the occurrence of some propalinal chewing in sauropsids. We combined 3D kinematics and morphological analyses from biplanar high-speed video fluoroscopy and micro-computed tomography to determine how the paedomorphic salamander Siren intermedia treats captured food. We discovered not only that S. intermedia uses intraoral food processing but also that the elaborated morphology of its jaw joint facilitates mandibular motions in all three planes, resulting in complex 3D chewing. Thus, our data challenge the commonly held view that complex 3D chewing movements are exclusive to mammals, by suggesting that such mechanisms might have evolved early in the tetrapod evolution.

Modulation of Flight Muscle Recruitment and Wing Rotation Enables Hummingbirds to Mitigate Aerial Roll Perturbations.

Both biological and artificial fliers must contend with aerial perturbations that are ubiquitous in the outdoor environment. Flapping fliers are generally least stable but also most maneuverable around the roll axis, yet our knowledge of roll control in biological fliers remains limited. Hummingbirds are suitable models for linking aerodynamic perturbations to flight control strategies, as these small, powerful fliers are capable of remaining airborne even in adverse wind conditions. We challenged hummingbirds to fly within a steady, longitudinally (streamwise) oriented vortex that imposed a continuous roll perturbation, measured wing kinematics and neuromotor activation of the flight muscles with synchronized high-speed video and electromyography and used computational fluid dynamics (CFD) to estimate the aerodynamic forces generated by observed wing motions. Hummingbirds responded to the perturbation with bilateral differences in activation of the main flight muscles while maintaining symmetry in most major aspects of wing motion, including stroke amplitude, stroke plane angle, and flapping frequency. Hummingbirds did display consistent bilateral differences in subtler wing kinematic traits, including wing rotation and elevation. CFD modeling revealed that asymmetric wing rotation was critical for attenuating the effects of the perturbation. The birds also augmented flight stabilization by adjusting body and tail posture to expose greater surface area to upwash than to the undesirable downwash. Our results provide insight into the remarkable capacity of hummingbirds to maintain flight control, as well as bio-inspiration for simple yet effective control strategies that could allow robotic fliers to contend with unfamiliar and challenging real-world aerial conditions.