Hand and foot morphology maps invasion of terrestrial environments by pterosaurs in the mid-Mesozoic.

Pterosaurs, the first true flying vertebrates, played a crucial role in Mesozoic terrestrial ecosystems. However, our understanding of their ability to move around on the ground and, more broadly, their terrestrial paleoecology remains limited. Here, we demonstrate an unexpectedly high degree of variation in the hands and feet of pterosaurs, comparable with that observed in extant birds. This suggests that pterosaurs were adapted to a remarkably broad range of non-aerial locomotor ecologies. Small, early, long-tailed pterosaurs (non-pterodactyliforms) exhibit extreme modifications in their hand and foot proportions indicative of climbing lifestyles. By contrast, the hands and feet of later, short-tailed pterosaurs (pterodactyliforms) typically exhibit morphologies consistent with more ground-based locomotor ecologies. These changes in proportions correlate with other modifications to pterosaur anatomy, critically, the separation along the midline of the flight membrane (cruropatagium) that linked the hindlimbs, enabling a much more effective locomotory ability on the ground. Together, these changes map a significant event in tetrapod evolution: a mid-Mesozoic colonization of terrestrial environments by short-tailed pterosaurs. This transition to predominantly ground-based locomotor ecologies did not occur as a single event coinciding with the origin of short-tailed forms but evolved independently within each of the four principal radiations: euctenochasmatians, ornithocheiroids, dsungaripteroids, and azhdarchoids. Invasion of terrestrial environments by pterosaurs facilitated the evolution of a wide range of novel feeding ecologies, while the freedom from limitations imposed by climbing permitted an increase in body size, ultimately enabling the evolution of gigantism in multiple lineages.

Human walking biomechanics on sand substrates of varying foot sinking depth.

Our current understanding of human gait is mostly based on studies using hard, level surfaces in a laboratory environment. However, humans navigate a wide range of different substrates every day, which incur varied demands on stability and efficiency. Several studies have shown that when walking on natural compliant substrates there is an increase in energy expenditure. However, these studies report variable changes to other aspects of gait such as muscle activity. Discrepancies between studies exist even within substrate types (e.g. sand), which suggests that relatively 'fine-scale' differences in substrate properties exert quantifiable influences on gait mechanics. In this study, we compare human walking mechanics on a range of sand substrates that vary in overall foot sinking depth. We demonstrate that variation in the overall sinking depth in sand is associated with statistically significant changes in joint angles and spatiotemporal variables in human walking but exerts relatively little influence on pendular energy recovery and muscle activations. Significant correlated changes between gait metrics are frequently recovered, suggesting a degree of coupled or mechanistic interaction in their variation within and across substrates. However, only walking speed (and its associated spatiotemporal variables) correlate frequently with absolute foot sinkage depth within individual sand substrates, but not across them. This suggests a causative relationship between walking speed and foot sinkage depth within individual sand substates is not coupled with systematic changes in joint kinematics and muscle activity in the same way as is observed across sand substrates.

Technical note: A volumetric method for measuring the longitudinal arch of human tracks and feet.

Fossil footprints (i.e., tracks) were believed to document arch anatomical evolution, although our recent work has shown that track arches record foot kinematics instead. Analyses of track arches can thereby inform the evolution of human locomotion, although quantifying this 3-D aspect of track morphology is difficult. Here, we present a volumetric method for measuring the arches of 3-D models of human tracks and feet, using both Autodesk Maya and Blender software. The method involves generation of a 3-D object that represents the space beneath the longitudinal arch, and measurement of that arch object's geometry and spatial orientation. We provide relevant tools and guidance for users to apply this technique to their own data. We present three case studies to demonstrate potential applications. These include, (1) measuring the arches of static and dynamic human feet, (2) comparing the arches of human tracks with the arches of the feet that made them, and (3) direct comparisons of human track and foot arch morphology throughout simulated track formation. The volumetric measurement tool proved robust for measuring 3-D models of human tracks and feet, in static and dynamic contexts. This tool enables researchers to quantitatively compare arches of fossil hominin tracks, in order to derive biomechanical interpretations from them, and/or offers a different approach for quantifying foot morphology in living humans.

New Middle to ?Late Jurassic dinosaur tracksites in the Central High Atlas Mountains, Morocco.

Besides bones, fossil tracks and trackways are important sources of knowledge about dinosaur palaeobiology. Here, we report three new tracksites from two different synclines in the Imilchil area, Central High Atlas, Morocco. The tracks and trackways are preserved in fluvial deposits in different levels of the Isli Formation (Early Bathonian-?Upper Jurassic), and contain impressions made by sauropods, theropods and ornithopods, as well as tracks that might represent bird-like non-avian theropod dinosaurs. In addition to traditional field measurements, three-dimensional digital models of the track sites were created using photogrammetry. These new tracksites add to the rich faunal ichnoassemblage already recorded from the High Atlas Mountains and North Africa, which is considerably richer than the contemporaneous body fossil record, and also provide new data on dinosaurs-substrate interactions.

Hipparion tracks and horses' toes: the evolution of the equid single hoof.

The traditional story of the evolution of the horse (family Equidae) has been in large part about the evolution of their feet. How did modern horses come to have a single toe (digit III), with the hoof bearing a characteristic V-shaped keratinous frog on the sole, and what happened to the other digits? While it has long been known that the proximal portions of digits II and IV are retained as the splint bones, a recent hypothesis suggested that the distal portion of these digits have also been retained as part of the frog, drawing upon the famous Laetoli footprints of the tridactyl (three-toed) equid Hipparion as part of the evidence. We show here that, while there is good anatomical and embryological evidence for the proximal portions of all the accessory digits (i.e. I and V, as well as II and IV) being retained in the feet of modern horses, evidence is lacking for the retention of any distal portions of these digits. There is also good ichnological evidence that many tridactyl equids possessed a frog, and that the frog has been part of the equid foot for much of equid evolutionary history.

Dinosaur trackways from the Upper Cretaceous Nichkesai Formation near Mayluu Suu City, Southern Tien Shan Mountains, north-western Kyrgyzstan.

Trackways provide essential data on the biogeographic distribution, locomotion and behaviour of dinosaurs. Cretaceous dinosaur trackways are abundant in the Americas, Europe, North Africa and East Asia, but are less well documented in Central Asia despite extensive exposure of Cretaceous terrestrial sedimentary rocks in the region. Here we report the presence of bipedal, tridactyl dinosaur trackways near the city of Mayluu Suu, Jalal Abad Oblast, north-western Kyrgyzstan, the first discovery of dinosaur trace fossils within the country. The trackways are situated on a steep slope uncovered by a landslide around the year 2000 in a highly landslide-affected area. Photogrammetry is used to digitally analyse and conserve the trace fossils. We infer a shoreface setting for the trackways based on the locality sedimentology, discuss the identity of the track makers and highlight the potential for future trackway discovery in the area. This discovery contributes vital data to an otherwise sparse record on the spatio-temporal distribution of dinosaurs in Kyrgyzstan, and to the dinosaur trackway record of Central Asia.

Arched footprints preserve the motions of fossil hominin feet.

The longitudinal arch of the human foot is viewed as a pivotal adaptation for bipedal walking and running. Fossil footprints from Laetoli, Tanzania, and Ileret, Kenya, are believed to provide direct evidence of longitudinally arched feet in hominins from the Pliocene and Pleistocene, respectively. We studied the dynamics of track formation using biplanar X-ray, three-dimensional animation and discrete element particle simulation. Here, we demonstrate that longitudinally arched footprints are false indicators of foot anatomy; instead they are generated through a specific pattern of foot kinematics that is characteristic of human walking. Analyses of fossil hominin tracks from Laetoli show only partial evidence of this walking style, with a similar heel strike but a different pattern of propulsion. The earliest known evidence for fully modern human-like bipedal kinematics comes from the early Pleistocene Ileret tracks, which were presumably made by members of the genus Homo. This result signals important differences in the foot kinematics recorded at Laetoli and Ileret and underscores an emerging picture of locomotor diversity within the hominin clade.

Why does the metabolic cost of walking increase on compliant substrates?

Walking on compliant substrates requires more energy than walking on hard substrates but the biomechanical factors that contribute to this increase are debated. Previous studies suggest various causative mechanical factors, including disruption to pendular energy recovery, increased muscle work, decreased muscle efficiency and increased gait variability. We test each of these hypotheses simultaneously by collecting a large kinematic and kinetic dataset of human walking on foams of differing thickness. This allowed us to systematically characterize changes in gait with substrate compliance, and, by combining data with mechanical substrate testing, drive the very first subject-specific computer simulations of human locomotion on compliant substrates to estimate the internal kinetic demands on the musculoskeletal system. Negative changes to pendular energy exchange or ankle mechanics are not supported by our analyses. Instead we find that the mechanistic causes of increased energetic costs on compliant substrates are more complex than captured by any single previous hypothesis. We present a model in which elevated activity and mechanical work by muscles crossing the hip and knee are required to support the changes in joint (greater excursion and maximum flexion) and spatio-temporal kinematics (longer stride lengths, stride times and stance times, and duty factors) on compliant substrates.

A machine learning approach for the discrimination of theropod and ornithischian dinosaur tracks.

Fossil tracks are important palaeobiological data sources. The quantitative analysis of their shape, however, has been hampered by their high variability and lack of discrete margins and landmarks. We here present the first approach using deep convolutional neural networks (DCNNs) to study fossil tracks, overcoming the limitations of previous statistical approaches. We employ a DCNN to discriminate between theropod and ornithischian dinosaur tracks based on a total of 1372 outline silhouettes. The DCNN consistently outperformed human experts on an independent test set. We also used the DCNN to classify tracks of a large tridactyl trackmaker from Lark Quarry, Australia, the identity of which has been subject to intense debate. The presented approach can only be considered a first step towards the wider application of machine learning in fossil track research, which is not limited to classification problems. Current limitations, such as the subjectivity and information loss inherent in interpretive outlines, may be overcome in the future by training neural networks on three-dimensional models directly, though this will require an increased uptake in digitization among workers in the field.

What is Stance Phase On Deformable Substrates?

The stance phase of walking is when forces are applied to the environment to support, propel, and maneuver the body. Unlike solid surfaces, deformable substrates yield under load, allowing the foot to sink to varying degrees. For bipedal birds and their dinosaurian ancestors, a shared response to walking on these substrates has been identified in the looping path the digits follow underground. Because a volume of substrate preserves a 3-D record of stance phase in the form of footprints or tracks, understanding how the bipedal stride cycle relates to this looping motion is critical for building a track-based framework for the study of walking in extinct taxa. Here we used biplanar X-ray imaging to record and analyze 161 stance phases from 81 trials of three Helmeted Guineafowl (Numida meleagris) walking on radiolucent substrates of different consistency (solid, dry granular, firm to semi-liquid muds). Across all substrates, the feet sank to a range of depths up to 78% of hip height. With increasing substrate hydration, the majority of foot motion shifted from above to below ground. Walking kinematics sampled across all stride cycles revealed six sequential gait-based events originating from both feet, conserved throughout the spectrum of substrate consistencies during normal alternating walking. On all substrates that yielded, five sub-phases of gait were drawn out in space and formed a loop of varying shape. We describe the two-footed coordination and weight distribution that likely contributed to the observed looping patterns of an individual foot. Given such complex subsurface foot motion during normal alternating walking and some atypical walking behaviors, we discuss the definition of "stance phase" on deformable substrates. We also discuss implications of the gait-based origins of subsurface looping on the interpretation of locomotory information preserved in fossil dinosaur tracks.

A new method to calculate limb phase from trackways reveals gaits of sauropod dinosaurs.

Limb phase, the timing of the footfalls in quadrupedal locomotion that describes common gaits such as the trot and the pace gait,1,2 is widely believed to be difficult or even impossible to estimate for extinct tetrapods.3-5 We here present a fundamentally new approach that allows for estimating limb phase based on variation patterns in long trackways. The approach is tested on trackways of modern mammals, where the estimates generally correspond well with the actually employed limb phase. We then estimate limb phases of giant wide-gauged sauropod dinosaurs based on three long trackways from the Lower Cretaceous of Arkansas, US.6,7 Gait selection at the largest body sizes is of considerable interest given the lack of modern analogs. Contrary to previous assumptions,8,9 our estimates suggest lateral sequence diagonal couplet walks, in which the footfalls of the diagonal limb pairs (e.g., right hind and left fore) are more closely related in time than those of the same side of the body (e.g., right hind and right fore). Such a gait selection allows for efficient walking while maintaining diagonal limb support throughout the step cycle, which is important for a giant, wide-gauged trackmaker.10 Estimations of limb phase may help to constrain other gait parameters, body size and shape, and, finally, potential trackmaker taxa.

Integration of biplanar X-ray, three-dimensional animation and particle simulation reveals details of human 'track ontogeny'.

The emergence of bipedalism had profound effects on human evolutionary history, but the evolution of locomotor patterns within the hominin clade remains poorly understood. Fossil tracks record in vivo behaviours of extinct hominins, and they offer great potential to reveal locomotor patterns at various times and places across the human fossil record. However, there is no consensus on how to interpret anatomical or biomechanical patterns from tracks due to limited knowledge of the complex foot-substrate interactions through which they are produced. Here, we implement engineering-based methods to understand human track formation with the ultimate goal of unlocking invaluable information on hominin locomotion from fossil tracks. We first developed biplanar X-ray and three-dimensional animation techniques that permit visualization of subsurface foot motion as tracks are produced, and that allow for direct comparisons of foot kinematics to final track morphology. We then applied the discrete element method to accurately simulate the process of human track formation, allowing for direct study of human track ontogeny. This window lets us observe how specific anatomical and/or kinematic variables shape human track morphology, and it offers a new avenue for robust hypothesis testing in order to infer patterns of foot anatomy and motion from fossil hominin tracks.

Virtual and augmented reality: New tools for visualizing, analyzing, and communicating complex morphology.

Virtual and augmented reality (VR/AR) are new technologies with the power to revolutionize the study of morphology. Modern imaging approaches such as computed tomography, laser scanning, and photogrammetry have opened up a new digital world, enabling researchers to share and analyze morphological data electronically and in great detail. Because this digital data exists on a computer screen, however, it can remain difficult to understand and unintuitive to interact with. VR/AR technologies bridge the analog-to-digital divide by presenting 3D data to users in a very similar way to how they would interact with actual anatomy, while also providing a more immersive experience and greater possibilities for exploration. This manuscript describes VR/AR hardware, software, and techniques, and is designed to give practicing morphologists and educators a primer on using these technologies in their research, pedagogy, and communication to a wide variety of audiences. We also include a series of case studies from the presentations and workshop given at the 2019 International Congress of Vertebrate Morphology, and suggest best practices for the use of VR/AR in comparative morphology.

Evolutionary versatility of the avian neck.

Bird necks display unparalleled levels of morphological diversity compared to other vertebrates, yet it is unclear what factors have structured this variation. Using three-dimensional geometric morphometrics and multivariate statistics, we show that the avian cervical column is a hierarchical morpho-functional appendage, with varying magnitudes of ecologically driven osteological variation at different scales of organization. Contrary to expectations given the widely varying ecological functions of necks in different species, we find that regional modularity of the avian neck is highly conserved, with an overall structural blueprint that is significantly altered only by the most mechanically demanding ecological functions. Nevertheless, the morphologies of vertebrae within subregions of the neck show more prominent signals of adaptation to ecological pressures. We also find that both neck length allometry and the nature of neck elongation in birds are different from other vertebrates. In contrast with mammals, neck length scales isometrically with head mass and, contrary to previous work, we show that neck elongation in birds is achieved predominantly by increasing vertebral lengths rather than counts. Birds therefore possess a cervical spine that may be unique in its versatility among extant vertebrates, one that, since the origin of flight, has adapted to function as a surrogate forelimb in varied ecological niches.

It's in the loop: shared sub-surface foot kinematics in birds and other dinosaurs shed light on a new dimension of fossil track diversity.

The feet of ground-dwelling birds retain many features of their dinosaurian ancestry. Experiments with living species offer insights into the complex interplay among anatomy, kinematics and substrate during the formation of Mesozoic footprints. However, a key aspect of the track-making process, sub-surface foot movement, is hindered by substrate opacity. Here, we use biplanar X-rays to image guineafowl walking through radiolucent substrates of different consistency (solid, dry granular, firm to semi-liquid muds). Despite substantial kinematic variation, the foot consistently moves in a looping pattern below ground. As the foot sinks and then withdraws, the claws of the three main toes create entry and exit paths in different locations. Sampling these paths at incremental horizons captures two-dimensional features just as fossil tracks do, allowing depth-based zones to be characterized by the presence and relative position of digit impressions. Examination of deep, penetrative tracks from the Early Jurassic confirms that bipeds had an equivalent looping response to soft substrates approximately 200 Ma. Our integration of extant and extinct evidence demonstrates the influence of substrate properties on sinking depth and sub-surface foot motion, both of which are significant sources of track variation in the fossil record of dinosaurs.

Can skeletal surface area predict in vivo foot surface area?

The surface area of feet in contact with the ground is a key morphological feature that influences animal locomotion. Underfoot pressures (and consequently stresses experienced by the foot), as well as stability of an animal during locomotion, depend on the size and shape of this area. Here we tested whether the area of a skeletal foot could predict in vivo soft tissue foot surface area. Computed tomography scans of 29 extant tetrapods (covering mammals, reptiles, birds and amphibians) were used to produce models of both the soft tissues and the bones of their feet. Soft tissue models were oriented to a horizontal plane, and their outlines projected onto a surface to produce two-dimensional silhouettes. Silhouettes of skeletal models were generated either from bones in CT pose or with all autopodial bones aligned to the horizontal plane. Areas of these projections were calculated using alpha shapes (mathematical tight-fitting outline). Underfoot area of soft tissue was approximately 1.67 times that of skeletal tissue area (~ 2 times for manus, ~ 1.6 times for pes, if analysed separately). This relationship between skeletal foot area and soft tissue area, while variable in some of our study taxa, could provide information about the size of the organisms responsible for fossil trackways, suggest what size of tracks might be expected from potential trackmakers known only from skeletal remains, and aid in soft tissue reconstruction of skeletal remains for biomechanical modelling.

The importance of muscle architecture in biomechanical reconstructions of extinct animals: a case study using Tyrannosaurus rex.

Functional reconstructions of extinct animals represent a crucial step towards understanding palaeocological interactions, selective pressures and macroevolutionary patterns in the fossil record. In recent years, computational approaches have revolutionised the field of 'evolutionary biomechanics' and have, in general, resulted in convergence of quantitative estimates of performance on increasingly narrow ranges for well studied taxa. Studies of body mass and locomotor performance of Tyrannosaurus rex - arguably the most intensively studied extinct animal - typify this pattern, with numerous independent studies predicting similar body masses and maximum locomotor speeds for this animal. In stark contrast to this trend, recent estimates of maximum bite force in T. rex vary considerably (> 50%) despite use of similar quantitative methodologies. Herein we demonstrate that the mechanistic causes of these disparate predictions are indicative of important and underappreciated limiting factors in biomechanical reconstructions of extinct organisms. Detailed comparison of previous models of T. rex bite force reveals that estimations of muscle fibre lengths and architecture are the principal source of disagreement between studies, and therefore that these parameters represents the greatest source of uncertainty in these reconstructions, and potentially therefore extinct animals generally. To address the issue of fibre length and architecture estimation in extinct animals we present data tabulated from the literature of muscle architecture from over 1100 muscles measured in extant terrestrial animals. Application of this dataset in a reanalysis of T. rex bite force emphasises the need for more data on jaw musculature from living carnivorous animals, alongside increased sophistication of modelling approaches. In the latter respect we predict that implementing limits on skeletal loading into musculoskeletal models will narrow predictions for T. rex bite force by excluding higher-end estimates.

An 8.5 m long ammonite drag mark from the Upper Jurassic Solnhofen Lithographic Limestones, Germany.

Trackways and tracemakers preserved together in the fossil record are rare. However, the co-occurrence of a drag mark, together with the dead animal that produced it, is exceptional. Here, we describe an 8.5 m long ammonite drag mark complete with the preserved ammonite shell (Subplanites rueppellianus) at its end. Previously recorded examples preserve ammonites with drag marks of < 1 m. The specimen was recovered from a quarry near Solnhofen, southern Germany. The drag mark consists of continuous parallel ridges and furrows produced by the ribs of the ammonite shell as it drifted just above the sediment surface, and does not reflect behaviour of the living animal.

Open data and digital morphology.

Over the past two decades, the development of methods for visualizing and analysing specimens digitally, in three and even four dimensions, has transformed the study of living and fossil organisms. However, the initial promise that the widespread application of such methods would facilitate access to the underlying digital data has not been fully achieved. The underlying datasets for many published studies are not readily or freely available, introducing a barrier to verification and reproducibility, and the reuse of data. There is no current agreement or policy on the amount and type of data that should be made available alongside studies that use, and in some cases are wholly reliant on, digital morphology. Here, we propose a set of recommendations for minimum standards and additional best practice for three-dimensional digital data publication, and review the issues around data storage, management and accessibility.