A path to gigantism: Three-dimensional study of the sauropodomorph limb long bone shape variation in the context of the emergence of the sauropod bauplan.

Sauropodomorph dinosaurs include the largest terrestrial animals that ever lived on Earth. The early representatives of this clade were, however, relatively small and partially to totally bipedal, conversely to the gigantic and quadrupedal sauropods. Although the sauropod bauplan is well defined, notably by the acquisition of columnar limbs, the evolutionary sequence leading to its emergence remains debated. Here, we aim to tackle this evolutionary episode by investigating shape variation in the six limb long bones for the first time using three-dimensional geometric morphometrics. The morphological features of the forelimb zeugopod bones related to the sauropod bauplan tend to appear abruptly, whereas the pattern is more gradual for the hindlimb zeugopod bones. The stylopod bones tend to show the same pattern as their respective zeugopods. The abrupt emergence of the sauropod forelimb questions the locomotor abilities of non-sauropodan sauropodomorphs inferred as quadrupeds. Features characterizing sauropods tend to corroborate a view of their locomotion mainly based on stylopod retraction. An allometric investigation of the shape variation in accordance with size highlight differences in hindlimb bone allometries between the sauropods and the non-sauropodan sauropodomorphs. These differences notably correspond to an unexpected robustness decrease trend in the sauropod hindlimb zeugopod. In addition to forelimb bones that appear to be proportionally more gracile than in non-sauropodan sauropodomorphs, sauropods may have relied on limb architecture and features related to the size increase, rather than general robustness, to deal with the role of weight-bearing.

Osteo-pathological analysis provides evidence for a survived historical ship strike in a Southern Hemisphere fin whale (Balaenoptera physalus).

The life history of a fin whale (Balaenoptera physalus) caught during whaling operations in the 1950s was partly reconstructed. 3D surface models of the bones of the skeleton curated at the Zoological Museum of Hamburg were used for an osteopathological analysis. The skeleton revealed multiple healed fractures of ribs and a scapula. Moreover, the processus spinosi of several vertebrae were deformed and arthrosis was found. Together, the pathological findings provide evidence for large blunt trauma and secondary effects arising from it. Reconstruction of the likely cause of events suggests collision with a ship inflicting the fractures and leading to post traumatic posture damage as indicated by skeletal deformations. The injured bones had fully healed before the fin whale was killed by a whaler in the South Atlantic in 1952. This study is the first in-detail reconstruction of a historical whale-ship collision in the Southern Hemisphere, dating back to the 1940s, and the first documentation of a healed scapula fracture in a fin whale. The skeleton provides evidence for survival of a ship strike by a fin whale with severe injuries causing long-term impairment.

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.

Comparative Three-Dimensional Moment Arm Analysis of the Sauropod Forelimb: Implications for the Transition to a Wide-Gauge Stance in Titanosaurs.

The evolution of extraordinarily large size among Sauropoda was associated with a number of biomechanical adaptations. Changes in muscle moment arms undoubtedly accompanied these adaptations, but since muscles rarely fossilize, our ability to understand them has been restricted. Here, we use three-dimensional (3D) musculoskeletal modeling to reconstruct and quantitatively assess leverage of forelimb muscles in the transition from the narrow-gauge stance of basal sauropods to a wide-gauge stance in titanosaurs. A comparative analysis is conducted on three neosauropods: the narrow-gauge diplodocid Apatosaurus louisae, the intermediate-gauge titanosariform Giraffatitan brancai, and the wide-gauge titanosaur Diamantinasaurus matildae. In this study, moment arm magnitudes and corresponding morphological evidence indicates multiple changes across the narrow-gauge to wide-gauge transition in sauropods. High shoulder adduction was found in Diamantinasaurus, suggesting functional changes for supporting a wider stance and a limb less aligned with ground reaction force. High leverage in shoulder extension of Diamantinasaurus and Giraffatitan is possibly related to the increased use of the forelimb in forward propulsion with an anterior shift in center of mass. In addition, the prominence of the olecranon process in Diamantinasaurus produced high moment arm leverage in elbow flexion and extension, suggesting titanosaurs might have maintained a more flexed forelimb posture and displayed an increased degree of maneuverability. Other results are more variable between taxa but still indicate smaller scale changes. A sensitivity analysis was also conducted to measure the reliability of our models and test specific uncertainties within the modeling process, as well as other uncertainties uncovered during analysis. Anat Rec, 2018. © 2018 Wiley Periodicals, Inc. Anat Rec, 302:794-817, 2019. © 2018 Wiley Periodicals, Inc.

Lower rotational inertia and larger leg muscles indicate more rapid turns in tyrannosaurids than in other large theropods.

SYNOPSIS: Tyrannosaurid dinosaurs had large preserved leg muscle attachments and low rotational inertia relative to their body mass, indicating that they could turn more quickly than other large theropods. METHODS: To compare turning capability in theropods, we regressed agility estimates against body mass, incorporating superellipse-based modeled mass, centers of mass, and rotational inertia (mass moment of inertia). Muscle force relative to body mass is a direct correlate of agility in humans, and torque gives potential angular acceleration. Agility scores therefore include rotational inertia values divided by proxies for (1) muscle force (ilium area and estimates of m. caudofemoralis longus cross-section), and (2) musculoskeletal torque. Phylogenetic ANCOVA (phylANCOVA) allow assessment of differences in agility between tyrannosaurids and non-tyrannosaurid theropods (accounting for both ontogeny and phylogeny). We applied conditional error probabilities a(p) to stringently test the null hypothesis of equal agility. RESULTS: Tyrannosaurids consistently have agility index magnitudes twice those of allosauroids and some other theropods of equivalent mass, turning the body with both legs planted or pivoting over a stance leg. PhylANCOVA demonstrates definitively greater agilities in tyrannosaurids, and phylogeny explains nearly all covariance. Mass property results are consistent with those of other studies based on skeletal mounts, and between different figure-based methods (our main mathematical slicing procedures, lofted 3D computer models, and simplified graphical double integration). IMPLICATIONS: The capacity for relatively rapid turns in tyrannosaurids is ecologically intriguing in light of their monopolization of large (>400 kg), toothed dinosaurian predator niches in their habitats.

Pathological survey on Temnodontosaurus from the Early Jurassic of southern Germany.

Paleopathologies document skeletal damage in extinct organisms and can be used to infer the causes of injury, as well as aspects of related biology, ecology and behavior. To date, few studies have been undertaken on Jurassic marine reptiles, while ichthyosaur pathologies in particular have never been systematically evaluated. Here we survey 41 specimens of the apex predator ichthyosaur Temnodontosaurus from the Early Jurassic of southern Germany in order to document the range and absolute frequency of pathologies observed in this taxon as a function of the number of specimens examined. According to our analysis, most observed pathologies in Temnodontosaurus are force-induced traumas with signs of healing, possibly inflicted during aggressive interactions with conspecifics. When the material is preserved, broken ribs are correlated in most of the cases with traumas elsewhere in the skeleton such as cranial injuries. The range of cranial pathologies in Temnodontosaurus is similar to those reported for extinct cetaceans and mosasaurs, which were interpreted as traces of aggressive encounters. Nevertheless, Temnodontosaurus differs from these other marine amniotes in the absence of pathologies in the vertebral column, consistent with the pattern previously documented in ichthyosaurs. We did not detect any instances of avascular necrosis in Temnodontosaurus from southern Germany, which may reflect a shallow diving life style. This study is intended to provide baseline data for the various types of observed pathologies in large ichthyosaurs occupying the 'apex predator' niche, and potentially clarifies aspects of species-specific behavior relative to other ichthyosaurs and marine amniotes.

Three-Dimensional Musculoskeletal Modeling of the Sauropodomorph Hind Limb: The Effect of Postural Change on Muscle Leverage.

The biomechanical constraints for life at massive size can be directly observed in the evolutionary history of sauropodomorph dinosaurs. Members of this lineage underwent a number of major postural transitions as they increased in size from relatively small bipedal dinosaurs to massive titanosaurs that include the largest terrestrial animals of all time. To better understand the impact of gigantic size on the biomechanics of sauropods, we used three-dimensional musculoskeletal modeling to investigate how hind limb musculature was affected, first by the development of a quadrupedal stance from a bipedal one, and later in the transition from a narrow-gauge to a wide-gauge stance. Muscle moment arms were measured in four sauropodomorph taxa: the bipedal basal sauropodomorph Plateosaurus engelhardti, the narrow-gauge diplodocid Diplodocus carnegii, the titanosauriform Giraffatitan brancai, and the wide-gauge titanosaur Diamantinasaurus matildae. In Plateosaurus, low moment arm leverage in the hip extensors and knee flexors and extensors was observed suggesting high-velocity movement for fast locomotion. A reduction in hip extensor leverage in Diamantinasaurus was found which suggests a reduced role for the hind limb in forward propulsion in titanosaurs. An increase in overall hip adductor leverage and leverage of adductors 1 and 2 in Diamantinasaurus, compared with other taxa studied, might relate to the development of a wide-gauge stance. High knee flexor-extensor leverage in Giraffatitan but not Diamantinasaurus partially refutes the idea that broader femoral condyles in titanosauriforms increased knee torque production capabilities. Sauropodomorph postural changes clearly had an impact on the function and leverage of hind limb muscles. Anat Rec, 301:2145-2163, 2018. © 2018 Wiley Periodicals, Inc.

Biology of the sauropod dinosaurs: the evolution of gigantism.

The herbivorous sauropod dinosaurs of the Jurassic and Cretaceous periods were the largest terrestrial animals ever, surpassing the largest herbivorous mammals by an order of magnitude in body mass. Several evolutionary lineages among Sauropoda produced giants with body masses in excess of 50 metric tonnes by conservative estimates. With body mass increase driven by the selective advantages of large body size, animal lineages will increase in body size until they reach the limit determined by the interplay of bauplan, biology, and resource availability. There is no evidence, however, that resource availability and global physicochemical parameters were different enough in the Mesozoic to have led to sauropod gigantism. We review the biology of sauropod dinosaurs in detail and posit that sauropod gigantism was made possible by a specific combination of plesiomorphic characters (phylogenetic heritage) and evolutionary innovations at different levels which triggered a remarkable evolutionary cascade. Of these key innovations, the most important probably was the very long neck, the most conspicuous feature of the sauropod bauplan. Compared to other herbivores, the long neck allowed more efficient food uptake than in other large herbivores by covering a much larger feeding envelope and making food accessible that was out of the reach of other herbivores. Sauropods thus must have been able to take up more energy from their environment than other herbivores. The long neck, in turn, could only evolve because of the small head and the extensive pneumatization of the sauropod axial skeleton, lightening the neck. The small head was possible because food was ingested without mastication. Both mastication and a gastric mill would have limited food uptake rate. Scaling relationships between gastrointestinal tract size and basal metabolic rate (BMR) suggest that sauropods compensated for the lack of particle reduction with long retention times, even at high uptake rates. The extensive pneumatization of the axial skeleton resulted from the evolution of an avian-style respiratory system, presumably at the base of Saurischia. An avian-style respiratory system would also have lowered the cost of breathing, reduced specific gravity, and may have been important in removing excess body heat. Another crucial innovation inherited from basal dinosaurs was a high BMR. This is required for fueling the high growth rate necessary for a multi-tonne animal to survive to reproductive maturity. The retention of the plesiomorphic oviparous mode of reproduction appears to have been critical as well, allowing much faster population recovery than in megaherbivore mammals. Sauropods produced numerous but small offspring each season while land mammals show a negative correlation of reproductive output to body size. This permitted lower population densities in sauropods than in megaherbivore mammals but larger individuals. Our work on sauropod dinosaurs thus informs us about evolutionary limits to body size in other groups of herbivorous terrestrial tetrapods. Ectothermic reptiles are strongly limited by their low BMR, remaining small. Mammals are limited by their extensive mastication and their vivipary, while ornithsichian dinosaurs were only limited by their extensive mastication, having greater average body sizes than mammals.