Reconstructing locomotor ecology of extinct avialans: a case study of Ichthyornis comparing sternum morphology and skeletal proportions.

Avian skeletal morphology is associated with locomotor function, including flight style, swimming and terrestrial locomotion, and permits informed inferences on locomotion in extinct taxa. The fossil taxon Ichthyornis (Avialae: Ornithurae) has long been regarded as highly aerial, with flight similar to terns or gulls (Laridae), and skeletal features resembling foot-propelled diving adaptations. However, rigorous testing of locomotor hypotheses has yet to be performed on Ichthyornis, despite its notable phylogenetic position as one of the most crownward stem birds. We analysed separate datasets of three-dimensional sternal shape (geometric morphometrics) and skeletal proportions (linear measurements across the skeleton), to examine how well these data types predict locomotor traits in Neornithes. We then used this information to infer locomotor capabilities of Ichthyornis. We find strong support for both soaring and foot-propelled swimming capabilities in Ichthyornis. Further, sternal shape and skeletal proportions provide complementary information on avian locomotion: skeletal proportions allow better predictions of the capacity for flight, whereas sternal shape predicts variation in more specific locomotor abilities such as soaring, foot-propelled swimming and escape burst flight. These results have important implications for future studies of extinct avialan ecology and underscore the importance of closely considering sternum morphology in investigations of fossil bird locomotion.

Modern three-dimensional digital methods for studying locomotor biomechanics in tetrapods.

Here, we review the modern interface of three-dimensional (3D) empirical (e.g. motion capture) and theoretical (e.g. modelling and simulation) approaches to the study of terrestrial locomotion using appendages in tetrapod vertebrates. These tools span a spectrum from more empirical approaches such as XROMM, to potentially more intermediate approaches such as finite element analysis, to more theoretical approaches such as dynamic musculoskeletal simulations or conceptual models. These methods have much in common beyond the importance of 3D digital technologies, and are powerfully synergistic when integrated, opening a wide range of hypotheses that can be tested. We discuss the pitfalls and challenges of these 3D methods, leading to consideration of the problems and potential in their current and future usage. The tools (hardware and software) and approaches (e.g. methods for using hardware and software) in the 3D analysis of tetrapod locomotion have matured to the point where now we can use this integration to answer questions we could never have tackled 20 years ago, and apply insights gleaned from them to other fields.

Quantitative biomechanical assessment of locomotor capabilities of the stem archosaur Euparkeria capensis.

Birds and crocodylians are the only remaining members of Archosauria (ruling reptiles) and they exhibit major differences in posture and gait, which are polar opposites in terms of locomotor strategies. Their broader lineages (Avemetatarsalia and Pseudosuchia) evolved a multitude of locomotor modes in the Triassic and Jurassic periods, including several occurrences of bipedalism. The exact timings and frequencies of bipedal origins within archosaurs, and thus their ancestral capabilities, are contentious. It is often suggested that archosaurs ancestrally exhibited some form of bipedalism. Euparkeria capensis is a central taxon for the investigation of locomotion in archosaurs due to its phylogenetic position and intermediate skeletal morphology, and is argued to be representative of facultative bipedalism in this group. However, no studies to date have biomechanically tested if bipedality was feasible in Eupakeria. Here, we use musculoskeletal models and static simulations in its hindlimb to test the influences of body posture and muscle parameter estimation methods on locomotor potential. Our analyses show that the resulting negative pitching moments around the centre of mass were prohibitive to sustainable bipedality. We conclude that it is unlikely that Euparkeria was facultatively bipedal, and was probably quadrupedal, rendering the inference of ancestral bipedal abilities in Archosauria unlikely.

Reconstructing Articular Cartilage in the Australopithecus afarensis Hip Joint and the Need for Modeling Six Degrees of Freedom.

The postcranial skeleton of Australopithecus afarensis (AL 288-1) exhibits clear adaptations for bipedality, although there is some debate as to the efficiency and frequency of such upright movement. Some researchers argue that AL 288-1 walked with an erect limb like modern humans do, whilst others advocate for a "bent-hip bent-knee" (BHBK) gait, although in recent years the general consensus favors erect bipedalism. To date, no quantitative method has addressed the articulation of the AL 288-1 hip joint, nor its range of motion (ROM) with consideration for joint spacing, used as a proxy for the thickness of the articular cartilage present within the joint spacing which can affect how a joint moves. Here, we employed ROM mapping methods to estimate the joint spacing of AL 288-1's hip joint in comparison to a modern human and chimpanzee. Nine simulations assessed different joint spacing and tested the range of joint congruency (i.e., ranging from a closely packed socket to loosely packed). We further evaluated the sphericity of the femoral head and whether three rotational degrees of freedom (DOFs) sufficiently captures the full ROM or if translational DOFs must be included. With both setups, we found that the AL 288-1 hip was unlikely to be highly congruent (as it is in modern humans) because this would severely restrict hip rotational movement and would severely limit the capability for both bipedality and even arboreal locomotion. Rather, the hip was more cartilaginous than it is in the modern humans, permitting the hip to rotate into positions necessitated by both terrestrial and arboreal movements. Rotational-only simulations found that AL 288-1 was unable to extend the hip like modern humans, forcing the specimen to employ a BHBK style of walking, thus contradicting 40+ years of previous research into the locomotory capabilities of AL 288-1. Therefore, we advocate that differences in the sphericity of the AL 288-1 femoral head with that of a modern human necessitates all six DOFs to be included in which AL 288-1 could osteologically extend the hip to facilitate a human-like gait.

A Guide to Inverse Kinematic Marker-Guided Rotoscoping Using IK Solvers.

X-ray Reconstruction of Moving Morphology (XROMM) permits researchers to see beneath the skin, usually to see musculoskeletal movements. These movements can be tracked and later used to provide information regarding the mechanics of movement. Here, we discuss "IK marker-guided rotoscoping"-a method that combines inverse kinematic solvers with that of traditional scientific rotoscoping methods to quickly and efficiently overlay 3D bone geometries with the X-ray shadows from XROMM data. We use a case study of three Nile crocodiles' (Crocodylus niloticus) forelimbs and hindlimbs to evaluate this method. Within these limbs, different marker configurations were used: some configurations had six markers, others had five markers, and all forelimb data only had three markers. To evaluate IK marker-guided rotoscoping, we systematically remove markers in the six-marker configuration and then test the magnitudes of deviation in translations and rotations of the rigged setup with fewer markers versus those of the six-marker configuration. We establish that IK marker-guided rotoscoping is a suitable method for "salvaging" data that may have too few markers.

La reconstruction par rayons X de la morphologie en mouvement (XROMM) permet aux chercheurs d'observer les structures internes d'un organisme en mouvement, notamment au niveau musculo-squelettique. Ces mouvements peuvent être suivis à l'aide de marqueurs, renseignant ainsi sur la mécanique des mouvements de l'organisme étudié. Nous présentons ici la méthode  'IK marker-guided rotoscoping' qui combine des solveurs de cinématique inverse (IK) et des méthodes de rotoscopie scientifique pour superposer efficacement et de manière fiable des os en 3D avec les données obtenues par XROMM. Afin d'estimer la précision de cette méthode, nous l'avons appliquée sur un échantillon composé de membres antérieurs et postérieurs de trois crocodiles du Nil (Crocodylus niloticus) en utilisant trois configurations différentes : certaines comprenaient six marqueurs, d'autres cinq, tandis que toutes les configurations sur le membre antérieur comprenaient trois marqueurs. Nous avons ensuite retiré des marqueurs dans toutes les configurations comprenant six marqueurs afin de vérifier si cette différence avait un impact sur les mouvements de translations et de rotations obtenus respectivement avec ces deux configurations. Nous démontrons ainsi qu'il est possible d'étudier des données incomplètes, et donc n'offrant que très peu de marqueurs, en utilisant la méthode 'IK marker-guided rotoscoping'.(by Romain Pintore).

Three-dimensional polygonal muscle modelling and line of action estimation in living and extinct taxa.

Biomechanical models and simulations of musculoskeletal function rely on accurate muscle parameters, such as muscle masses and lines of action, to estimate force production potential and moment arms. These parameters are often obtained through destructive techniques (i.e., dissection) in living taxa, frequently hindering the measurement of other relevant parameters from a single individual, thus making it necessary to combine multiple specimens and/or sources. Estimating these parameters in extinct taxa is even more challenging as soft tissues are rarely preserved in fossil taxa and the skeletal remains contain relatively little information about the size or exact path of a muscle. Here we describe a new protocol that facilitates the estimation of missing muscle parameters (i.e., muscle volume and path) for extant and extinct taxa. We created three-dimensional volumetric reconstructions for the hindlimb muscles of the extant Nile crocodile and extinct stem-archosaur Euparkeria, and the shoulder muscles of an extant gorilla to demonstrate the broad applicability of this methodology across living and extinct animal clades. Additionally, our method can be combined with surface geometry data digitally captured during dissection, thus facilitating downstream analyses. We evaluated the estimated muscle masses against physical measurements to test their accuracy in estimating missing parameters. Our estimated muscle masses generally compare favourably with segmented iodine-stained muscles and almost all fall within or close to the range of observed muscle masses, thus indicating that our estimates are reliable and the resulting lines of action calculated sufficiently accurately. This method has potential for diverse applications in evolutionary morphology and biomechanics.

Musculoskeletal modelling of the Nile crocodile (Crocodylus niloticus) hindlimb: Effects of limb posture on leverage during terrestrial locomotion.

We developed a three-dimensional, computational biomechanical model of a juvenile Nile crocodile (Crocodylus niloticus) pelvis and hindlimb, composed of 47 pelvic limb muscles, to investigate muscle function. We tested whether crocodiles, which are known to use a variety of limb postures during movement, use limb orientations (joint angles) that optimise the moment arms (leverages) or moment-generating capacities of their muscles during different limb postures ranging from a high walk to a sprawling motion. We also describe the three-dimensional (3D) kinematics of the crocodylian hindlimb during terrestrial locomotion across an instrumented walkway and a treadmill captured via X-ray Reconstruction of Moving Morphology (biplanar fluoroscopy; 'XROMM'). We reconstructed the 3D positions and orientations of each of the hindlimb bones and used dissection data for muscle lines of action to reconstruct a focal, subject-specific 3D musculoskeletal model. Motion data for different styles of walking (a high, crouched, bended and two types of sprawling motion) were fed into the 3D model to identify whether any joints adopted near-optimal poses for leverage across each of the behaviours. We found that (1) the hip adductors and knee extensors had their largest leverages during sprawling postures and (2) more erect postures typically involved greater peak moment arms about the hip (flexion-extension), knee (flexion) and metatarsophalangeal (flexion) joints. The results did not fully support the hypothesis that optimal poses are present during different locomotory behaviours because the peak capacities were not always reached around mid-stance phase. Furthermore, we obtained few clear trends for isometric moment-generating capacities. Therefore, perhaps peak muscular leverage in Nile crocodiles is instead reached either in early/late stance or possibly during swing phase or other locomotory behaviours that were not studied here, such as non-terrestrial movement. Alternatively, our findings could reflect a trade-off between having to execute different postures, meaning that hindlimb muscle leverage is not optimised for any singular posture or behaviour. Our model, however, provides a comprehensive set of 3D estimates of muscle actions in extant crocodiles which can form a basis for investigating muscle function in extinct archosaurs.

3D hindlimb joint mobility of the stem-archosaur Euparkeria capensis with implications for postural evolution within Archosauria.

Triassic archosaurs and stem-archosaurs show a remarkable disparity in their ankle and pelvis morphologies. However, the implications of these different morphologies for specific functions are still poorly understood. Here, we present the first quantitative analysis into the locomotor abilities of a stem-archosaur applying 3D modelling techniques. µCT scans of multiple specimens of Euparkeria capensis enabled the reconstruction and three-dimensional articulation of the hindlimb. The joint mobility of the hindlimb was quantified in 3D to address previous qualitative hypotheses regarding the stance of Euparkeria. Our range of motion analysis implies the potential for an erect posture, consistent with the hip morphology, allowing the femur to be fully adducted to position the feet beneath the body. A fully sprawling pose appears unlikely but a wide range of hip abduction remained feasible-the hip appears quite mobile. The oblique mesotarsal ankle joint in Euparkeria implies, however, a more abducted hindlimb. This is consistent with a mosaic of ancestral and derived osteological characters in the hindlimb, and might suggest a moderately adducted posture for Euparkeria. Our results support a single origin of a pillar-erect hip morphology, ancestral to Eucrocopoda that preceded later development of a hinge-like ankle joint and a more erect hindlimb posture.