Using your head - cranial steering in pterosaurs.

The vast majority of pterosaurs are characterized by relatively large, elongate heads that are often adorned with large, elaborate crests. Projecting out in front of the body, these large heads and any crests must have had an aerodynamic effect. The working hypothesis of the present study is that these oversized heads were used to control the left-right motions of the body during flight. Using digital models of eight non-pterodactyloids ("rhamphorhyncoids") and ten pterodactyloids, the turning moments associated with the head + neck show a close and consistent correspondence with the rotational inertia of the whole body about a vertical axis in both groups, supporting the idea of a functional relationship. Turning moments come from calculating the lateral area of the head (plus any crests) and determining the associated lift (aerodynamic force) as a function of flight speed, with flight speeds being based on body mass. Rotational inertias were calculated from the three-dimensional mass distribution of the axial body, the limbs, and the flight membranes. The close correlation between turning moment and rotational inertia was used to revise the life restorations of two pterosaurs and to infer relatively lower flight speeds in another two.

Pterosaurs evolved a muscular wing-body junction providing multifaceted flight performance benefits: Advanced aerodynamic smoothing, sophisticated wing root control, and wing force generation.

Pterosaurs were the first vertebrate flyers and lived for over 160 million years. However, aspects of their flight anatomy and flight performance remain unclear. Using laser-stimulated fluorescence, we observed direct soft tissue evidence of a wing root fairing in a pterosaur, a feature that smooths out the wing-body junction, reducing associated drag, as in modern aircraft and flying animals. Unlike bats and birds, the pterosaur wing root fairing was unique in being primarily made of muscle rather than fur or feathers. As a muscular feature, pterosaurs appear to have used their fairing to access further flight performance benefits through sophisticated control of their wing root and contributions to wing elevation and/or anterior wing motion during the flight stroke. This study underscores the value of using new instrumentation to fill knowledge gaps in pterosaur flight anatomy and evolution.

Morphospaces of functionally analogous traits show ecological separation between birds and pterosaurs.

Birds originated and radiated in the presence of another group of flying vertebrates, the pterosaurs. Opinion is divided as to whether birds competitively displaced pterosaurs from small-body size niches or whether the two groups coexisted with little competition. Previous studies of Mesozoic birds and pterosaurs compared measurements of homologous limb bones to test these hypotheses. However, these characters probably reflect differing ancestries rather than ecologies. Here, competition and ecological separation were tested for using multivariate analyses of functionally equivalent morphological characters. As well as using characters from the fore- and hindlimbs, these analyses also included measurements of the lower jaw. The results of this study indicate that pterosaurs had relatively longer jaws, shorter metatarsals and shorter brachial regions compared with birds of similar size. Contrary to the results of previous studies, the distal wing was not important for separating the two clades in morphospace owing to the inclusion of the primary feathers in this unit. The differences found here indicate ecological separation based on differences in size, locomotory features and feeding adaptations. Thus, instead of one group displacing the other, birds and pterosaurs appear to have adopted distinctive ecological strategies throughout their period of coexistence.

Intraspecific variation in the pterosaur Rhamphorhynchus muensteri-implications for flight and socio-sexual signaling.

Pterosaurs were the first powered flying vertebrates, with a fossil record that stretches back to about 230 million years before present. Most species are only known from one to three specimens, which are most often fragmentary. However, Rhamphorhynchus muensteri is known from numerous excellent specimens, including multiple specimens with soft tissue preservation. As such, Rhamphorhynchus muensteri is one of the only pterosaurs amenable to analysis for intraspecific variation. It has been previously predicted that elements directly involved in the flight apparatus, such as those of the forelimb, will be more highly constrained in their proportions than other parts of the skeleton. We investigated the degree of variation seen in elements and body parts of Rhamphorhynchus, which represents the best model system among pterosaurs for testing these expectations of intraspecific variation. We recover evidence for high levels of constraint throughout the appendicular and axial elements (head, neck, torso, tail, forelimbs, hindlimbs), suggesting that all were important for flight. We further find that tail variation increases among the largest specimens, suggesting reduced constraint and/or stronger sexual selection on the tail in more mature individuals.

A preliminary analysis of dental microstructure in Hamipterus (Pterosauria, Pterodactyloidea).

The toothed members of Pterosauria display an extremely wide range of tooth morphologies that supported a variety of feeding habits. Histological studies on the teeth of different pterosaur clades are potentially valuable in understanding the development of their tooth diversity. In this study, we used histological sections and scanning electron microscopy to describe and interpret the tooth microstructure of Hamipterus (Pterodactyloidea). Our analysis is based on seven teeth of Hamipterus (six isolated and one from a skull) from the Lower Cretaceous collected in Hami, China. Our results show that the enamel on the tooth crown is thin (~25 µm) in Hamipterus and covers only approximately half of the tooth crown. This thin enamel of the Hamipterus tooth makes it vulnerable and often becomes damaged during taphonomic and diagenetic processes. The radicular pulp inside the conical-shaped root shows a spindle space with a small foramen at the bottom, while the coronal pulp shows a small tunnel (100-140 µm in diameter). We estimate that the small teeth of Hamipterus likely took approximately 80 days to form. Furthermore, the tooth has Andresen lines, which represent 7-15 days period. For stable articulation of the tooth in the alveolus, the thick cellular cementum is concentrated on the lingual side of the root. The acellular cementum (~40 µm thick) layer runs from the root to the partial tooth crown.

How did extinct giant birds and pterosaurs fly? A comprehensive modeling approach to evaluate soaring performance.

The largest extinct volant birds (Pelagornis sandersi and Argentavis magnificens) and pterosaurs (Pteranodon and Quetzalcoatlus) are thought to have used wind-dependent soaring flight, similar to modern large birds. There are 2 types of soaring: thermal soaring, used by condors and frigatebirds, which involves the use of updrafts to ascend and then glide horizontally; and dynamic soaring, used by albatrosses, which involves the use of wind speed differences with height above the sea surface. Previous studies have suggested that P. sandersi used dynamic soaring, while A. magnificens and Quetzalcoatlus used thermal soaring. For Pteranodon, there is debate over whether they used dynamic or thermal soaring. However, the performance and wind speed requirements of dynamic and thermal soaring for these species have not yet been quantified comprehensively. We quantified these values using aerodynamic models and compared them with that of extant birds. For dynamic soaring, we quantified maximum travel speeds and maximum upwind speeds. For thermal soaring, we quantified the animal's sinking speed circling at a given radius and how far it could glide losing a given height. Our results confirmed those from previous studies that A. magnificens and Pteranodon used thermal soaring. Conversely, the results for P. sandersi and Quetzalcoatlus were contrary to those from previous studies. P. sandersi used thermal soaring, and Quetzalcoatlus had a poor ability both in dynamic and thermal soaring. Our results demonstrate the need for comprehensive assessments of performance and required wind conditions when estimating soaring styles of extinct flying species.

Deep evolutionary diversification of semicircular canals in archosaurs.

Living archosaurs (birds and crocodylians) have disparate locomotor strategies that evolved since their divergence ∼250 mya. Little is known about the early evolution of the sensory structures that are coupled with these changes, mostly due to limited sampling of early fossils on key stem lineages. In particular, the morphology of the semicircular canals (SCCs) of the endosseous labyrinth has a long-hypothesized relationship with locomotion. Here, we analyze SCC shapes and sizes of living and extinct archosaurs encompassing diverse locomotor habits, including bipedal, semi-aquatic, and flying taxa. We test form-function hypotheses of the SCCs and chronicle their evolution during deep archosaurian divergences. We find that SCC shape is statistically associated with both flight and bipedalism. However, this shape variation is small and is more likely explained by changes in braincase geometry than by locomotor changes. We demonstrate high disparity of both shape and size among stem-archosaurs and a deep divergence of SCC morphologies at the bird-crocodylian split. Stem-crocodylians exhibit diverse morphologies, including aspects also present in birds and distinct from other reptiles. Therefore, extant crocodylian SCC morphologies do not reflect retention of a "primitive" reptilian condition. Key aspects of bird SCC morphology that hitherto were interpreted as flight related, including large SCC size and enhanced sensitivity, appeared early on the bird stem-lineage in non-flying dinosaur precursors. Taken together, our results indicate a deep divergence of SCC traits at the bird-crocodylian split and that living archosaurs evolved from an early radiation with high sensory diversity. VIDEO ABSTRACT.

New anatomical information on Dsungaripterus weii Young, 1964 with focus on the palatal region.

Pterosaur specimens with complete and well-preserved palatal region are rare. Here we describe new and previously collected specimens of the pterodactyloid pterosaur Dsungaripterus weii that are three-dimensionally preserved and provide new anatomical information for this species. Among the unique features is a lateral process of the pterygoid divided into two parts: an anterior thin, parabolic arc shaped element that separates the secondary subtemporal and the subtemporal fenestrae, followed by a dorsoventrally flattened portion that is directed inside the subtemporal fenestrae. The interpterygoid fenestrae join forming an irregular oval shape with two symmetrical posterior notches and a smooth anterior margin. Among all pterosaurs where the palate is known, the posterior configuration of the palate of D. weii is similar to some azhdarchoids, which is consistent with the suggested phylogenetic position of the Dsungaripteridae as closely related to the Azhdarchoidea. Furthermore, we identify symmetrical grooves on the lateral surface of the upper and lower jaws, that likely represent the impression of the edge of a keratinous sheath that would cover the upturned toothless rostrum during foraging activity, most likely consisting of hard elements, as has been previously assumed. Wear facets on the teeth also support this feeding mode.

The first pterosaur basihyal, shedding light on the evolution and function of pterosaur hyoid apparatuses.

The pterosaur is the first known vertebrate clade to achieve powered flight. Its hyoid apparatus shows a simplification similar to that of birds, although samples of the apparatus are rare, limiting the ability to make an accurate determination. In this study we reveal a new pterosaur specimen, including the first definite basihyal. Through the comparison of pterosaur hyoids, a trend has been discovered for the shortened hyoid relative to the length of the skull, indicating a diminished role of lingual retraction during the evolution of the pterosaur. The new material, possibly from a gallodactylid Gladocephaloideus, represents one of the least effective lingual retractions in all pterosaurs. Based on the structure of an elongated ceratobranchial and retroarticular process on mandibles, the function of the Y-shaped istiodactylid tongue bone is similar to those of scavenger crows rather than chameleons, which is consistent with the interpretation of the scavenging behavior of this taxon. More fossil samples are needed for further study on the function of other pterosaur hyoids.

The Early Origin of Feathers.

Feathers have long been regarded as the innovation that drove the success of birds. However, feathers have been reported from close dinosaurian relatives of birds, and now from ornithischian dinosaurs and pterosaurs, the cousins of dinosaurs. Incomplete preservation makes these reports controversial. If true, these findings shift the origin of feathers back 80 million years before the origin of birds. Gene regulatory networks show the deep homology of scales, feathers, and hairs. Hair and feathers likely evolved in the Early Triassic ancestors of mammals and birds, at a time when synapsids and archosaurs show independent evidence of higher metabolic rates (erect gait and endothermy), as part of a major resetting of terrestrial ecosystems following the devastating end-Permian mass extinction.

Neck biomechanics indicate that giant Transylvanian azhdarchid pterosaurs were short-necked arch predators.

Azhdarchid pterosaurs include the largest animals to ever take to the skies with some species exceeding 10 metres in wingspan and 220 kg in mass. Associated skeletons show that azhdarchids were long-necked, long-jawed predators that combined a wing planform suited for soaring with limb adaptations indicative of quadrupedal terrestrial foraging. The postcranial proportions of the group have been regarded as uniform overall, irrespective of their overall size, notwithstanding suggestions that minor variation may have been present. Here, we discuss a recently discovered giant azhdarchid neck vertebra referable to Hatzegopteryx from the Maastrichtian Sebes Formation of the Transylvanian Basin, Romania, which shows how some azhdarchids departed markedly from conventional views on their proportions. This vertebra, which we consider a cervical VII, is 240 mm long as preserved and almost as wide. Among azhdarchid cervicals, it is remarkable for the thickness of its cortex (4-6 mm along its ventral wall) and robust proportions. By comparing its dimensions to other giant azhdarchid cervicals and to the more completely known necks of smaller taxa, we argue that Hatzegopteryx had a proportionally short, stocky neck highly resistant to torsion and compression. This specimen is one of several hinting at greater disparity within Azhdarchidae than previously considered, but is the first to demonstrate such proportional differences within giant taxa. On the assumption that other aspects of Hatzegopteryx functional anatomy were similar to those of other azhdarchids, and with reference to the absence of large terrestrial predators in the Maastrichtian of Transylvania, we suggest that this pterosaur played a dominant predatory role among the unusual palaeofauna of ancient Hateg.

Earliest filter-feeding pterosaur from the Jurassic of China and ecological evolution of Pterodactyloidea.

Pterosaurs were a unique clade of flying reptiles that were contemporaries of dinosaurs in Mesozoic ecosystems. The Pterodactyloidea as the most species-diverse group of pterosaurs dominated the sky during Cretaceous time, but earlier phases of their evolution remain poorly known. Here, we describe a 160 Ma filter-feeding pterosaur from western Liaoning, China, representing the geologically oldest record of the Ctenochasmatidae, a group of exclusive filter feeders characterized by an elongated snout and numerous fine teeth. The new pterosaur took the lead of a major ecological transition in pterosaur evolution from fish-catching to filter-feeding adaptation, prior to the Tithonian (145-152 Ma) diversification of the Ctenochasmatidae. Our research shows that the rise of ctenochasmatid pterosaurs was followed by the burst of eco-morphological divergence of other pterodactyloid clades, which involved a wide range of feeding adaptations that considerably altered the terrestrial ecosystems of the Cretaceous world.

How the pterosaur got its wings.

Throughout the evolutionary history of life, only three vertebrate lineages took to the air by acquiring a body plan suitable for powered flight: birds, bats, and pterosaurs. Because pterosaurs were the earliest vertebrate lineage capable of powered flight and included the largest volant animal in the history of the earth, understanding how they evolved their flight apparatus, the wing, is an important issue in evolutionary biology. Herein, I speculate on the potential basis of pterosaur wing evolution using recent advances in the developmental biology of flying and non-flying vertebrates. The most significant morphological features of pterosaur wings are: (i) a disproportionately elongated fourth finger, and (ii) a wing membrane called the brachiopatagium, which stretches from the posterior surface of the arm and elongated fourth finger to the anterior surface of the leg. At limb-forming stages of pterosaur embryos, the zone of polarizing activity (ZPA) cells, from which the fourth finger eventually differentiates, could up-regulate, restrict, and prolong expression of 5'-located Homeobox D (Hoxd) genes (e.g. Hoxd11, Hoxd12, and Hoxd13) around the ZPA through pterosaur-specific exploitation of sonic hedgehog (SHH) signalling. 5'Hoxd genes could then influence downstream bone morphogenetic protein (BMP) signalling to facilitate chondrocyte proliferation in long bones. Potential expression of Fgf10 and Tbx3 in the primordium of the brachiopatagium formed posterior to the forelimb bud might also facilitate elongation of the phalanges of the fourth finger. To establish the flight-adapted musculoskeletal morphology shared by all volant vertebrates, pterosaurs probably underwent regulatory changes in the expression of genes controlling forelimb and pectoral girdle musculoskeletal development (e.g. Tbx5), as well as certain changes in the mode of cell-cell interactions between muscular and connective tissues in the early phase of their evolution. Developmental data now accumulating for extant vertebrate taxa could be helpful in understanding the cellular and molecular mechanisms of body-plan evolution in extinct vertebrates as well as extant vertebrates with unique morphology whose embryonic materials are hard to obtain.

Were early pterosaurs inept terrestrial locomotors?

Pterodactyloid pterosaurs are widely interpreted as terrestrially competent, erect-limbed quadrupeds, but the terrestrial capabilities of non-pterodactyloids are largely thought to have been poor. This is commonly justified by the absence of a non-pterodactyloid footprint record, suggestions that the expansive uropatagia common to early pterosaurs would restrict hindlimb motion in walking or running, and the presence of sprawling forelimbs in some species. Here, these arguments are re-visited and mostly found problematic. Restriction of limb mobility is not a problem faced by extant animals with extensive fight membranes, including species which routinely utilise terrestrial locomotion. The absence of non-pterodactyloid footprints is not necessarily tied to functional or biomechanical constraints. As with other fully terrestrial clades with poor ichnological records, biases in behaviour, preservation, sampling and interpretation likely contribute to the deficit of early pterosaur ichnites. Suggestions that non-pterodactyloids have slender, mechanically weak limbs are demonstrably countered by the proportionally long and robust limbs of many Triassic and Jurassic species. Novel assessments of pterosaur forelimb anatomies conflict with notions that all non-pterodactyloids were obligated to sprawling forelimb postures. Sprawling forelimbs seem appropriate for species with ventrally-restricted glenoid articulations (seemingly occurring in rhamphorhynchines and campylognathoidids). However, some early pterosaurs, such as Dimorphodon macronyx and wukongopterids, have glenoid arthrologies which are not ventrally restricted, and their distal humeri resemble those of pterodactyloids. It seems fully erect forelimb stances were possible in these pterosaurs, and may be probable given proposed correlation between pterodactyloid-like distal humeral morphology and forces incurred through erect forelimb postures. Further indications of terrestrial habits include antungual sesamoids, which occur in the manus and pes anatomy of many early pterosaur species, and only occur elsewhere in terrestrial reptiles, possibly developing through frequent interactions of large claws with firm substrates. It is argued that characteristics possibly associated with terrestriality are deeply nested within Pterosauria and not restricted to Pterodactyloidea as previously thought, and that pterodactyloid-like levels of terrestrial competency may have been possible in at least some early pterosaurs.