First record of a pterosaur landing trackway

The terrestrial progression of pterosaurs, the flying reptiles of the Mesozoic Era, has been debated for over two centuries. The recent discovery of quadrupedal pterodactyloid pterosaur tracks from Late Jurassic sediments near Crayssac, France, shows that the hindlimbs moved parasagittally, as in mammals, birds and other dinosaurs, and the hypertrophied forelimbs could make tracks both close to the body wall and far outside it. Their manus tracks are unique in form, position and kinematics, which would be expected because the forelimbs were used for flight. Here, we report the first record of a pterosaur landing track, which differs substantially from typical walking trackways. The individual landed on both hind feet in parallel fashion, dragged its toes slightly as it left the track, landed again almost immediately and placed the hindfeet parallel again, then placed its forelimbs on the ground, took another short step with both hindlimbs and adjusted its forelimbs, and then began to walk off normally. The trackway shows that pterosaurs stalled to land, a reflection of their highly developed capacity for flight control and manoeuverability.     

Flight in slow motion: aerodynamics of the pterosaur wing

The flight of pterosaurs and the extreme sizes of some taxa have long perplexed evolutionary biologists. Past reconstructions of flight capability were handicapped by the available aerodynamic data, which was unrepresentative of possible pterosaur wing profiles. I report wind tunnel tests on a range of possible pterosaur wing sections and quantify the likely performance for the first time. These sections have substantially higher profile drag and maximum lift coefficients than those assumed before, suggesting that large pterosaurs were aerodynamically less efficient and could fly more slowly than previously estimated. In order to achieve higher efficiency, the wing bones must be faired, which implies extensive regions of pneumatized tissue. Whether faired or not, the pterosaur wings were adapted to low-speed flight, unsuited to marine style dynamic soaring but adapted for thermal/slope soaring and controlled, low-speed landing. Because their thin-walled bones were susceptible to impact damage, slow flight would have helped to avoid injury and may have contributed to their attaining much larger sizes than fossil or extant birds. The trade-off would have been an extreme vulnerability to strong or turbulent winds both in flight and on the ground, akin to modern-day paragliders.     

Partial mandible of a giant pterosaur from the uppermost Cretaceous (Maastrichtian) of the Hațeg Basin,Romania

We describe and interpret a posterior mandibular symphysis of a very large azhdarchid pterosaur. The specimen LPB (FGGUB ) R.2347 exhibits a series of morphological characters present in both azhdarchid and tapejarid pterosaurs, suggesting a more basal position within the clade Azhdarchidae. This fossil was collected from Maastrichtian continental deposits near V?lioara in the Ha?eg Basin, Romania, but cannot be confidently referred to the contemporaneous giant Hatzegopteryx thambema, also from V?lioara, due to the absence of overlapping skeletal elements. Remarkably, this mandibular symphysis shares a number of features the smaller azhdarchoid Bakonydraco galaczi from the Santonian of Hungary. Additional comparisons with previously described large‐sized azhdarchid mandibles indicate a certain degree of morphological and probably ecological disparity within the group. This specimen represents the largest pterosaur mandible ever found and provides insights into the anatomy of the enigmatic giant pterosaurs.     

The shape of pterosaur evolution: evidence from the fossil record

Abstract Although pterosaurs are a well‐known lineage of Mesozoic flying reptiles, their fossil record and evolutionary dynamics have never been adequately quantified. On the basis of a comprehensive data set of fossil occurrences correlated with taxon‐specific limb measurements, we show that the geological ages of pterosaur specimens closely approximate hypothesized patterns of phylogenetic divergence. Although the fossil record has expanded greatly in recent years, collectorship still approximates a sigmoid curve over time as many more specimens (and thus taxa) still remain undiscovered, yet our data suggest that the pterosaur fossil record is unbiased by sites of exceptional preservation (lagerstätte). This is because as new species are discovered the number of known formations and sites yielding pterosaur fossils has also increased – this would not be expected if the bulk of the record came from just a few exceptional faunas. Pterosaur morphological diversification is, however, strongly age biased: rarefaction analysis shows that peaks of diversity occur in the Late Jurassic and Early Cretaceous correlated with periods of increased limb disparity. In this respect, pterosaurs appear unique amongst flying vertebrates in that their disparity seems to have peaked relatively late in clade history. Comparative analyses also show that there is little evidence that the evolutionary diversification of pterosaurs was in any way constrained by the appearance and radiation of birds.     

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.     

A New Model for the Evolution of the Pterosaur Wing--with a twist

A new hypothesis for the evolution of the pterosaur wing is presented. It is based on the observation that many aspects of pterosaur non-wing anatomy were present in their non-volant, prolacertiform sister taxa. In pterosaurs alone, metacarpal IV was twisted 90° medially, so the wing digit flexed in the plane of the metacarpus, rather than towards the palm as in other tetrapods. While grappling a tree using manual digits I-III, a pre-pterosaur with this character would have been free to flex and extend digit IV in the plane tangential to the circumference of the tree. The addition of a small dermal extension that opened like a Japanese fan would essentially have completed the development of the proto-wing. Its subsequent increase in size was brought on by selective competition. Successful powered flight would have been possible only after a critical wing size had been achieved.     

A reappraisal of azhdarchid pterosaur functional morphology and paleoecology

Azhdarchid pterosaurs were among the most widespread and successful of pterosaur clades, but their paleoecology remains controversial. Morphological features common to all azhdarchids include a long, shallow rostrum; elongate, cylindrical cervical vertebrae that formed a long and unusually inflexible neck; and proportionally short wings with an abbreviated fourth phalanx. While azhdarchids have been imagined as vulture-like scavengers, sediment probers, swimmers, waders, aerial predators, or stork-like generalists, most recent authors have regarded them as skim-feeders, trawling their lower jaws through water during flight and seizing aquatic prey from the water's surface. Although apparently widely accepted, the skim-feeding model lacks critical support from anatomy and functional morphology. Azhdarchids lack the many cranial specialisations exhibited by extant skim-feeding birds, most notably the laterally compressed lower jaw and shock absorbing apparatus required for this feeding style. Well-preserved azhdarchid skulls are rare, but their rostra and lower jaws appear to have been sub-triangular in cross-section, and thus dissimilar to those of skim-feeders and sediment probers. Taphonomic data indicates that azhdarchids predominately inhabited inland settings, and azhdarchid morphology indicates that they were poorly suited for all proposed lifestyles bar wading and terrestrial foraging. However, azhdarchid footprints show that their feet were relatively small, padded and slender, and thus not well suited for wading. We argue that azhdarchids were stork- or ground hornbill-like generalists, foraging in diverse environments for small animals and carrion. Proficient terrestrial abilities and a relatively inflexible neck are in agreement with this interpretation.     

Evidence for modular evolution in a long-tailed pterosaur with a pterodactyloid skull

The fossil record is a unique source of evidence for important evolutionary phenomena such as transitions between major clades. Frustratingly, relevant fossils are still comparatively rare, most transitions have yet to be documented in detail and the mechanisms that underpin such events, typified by rapid large scale changes and for which microevolutionary processes seem insufficient, are still unclear. A new pterosaur (Mesozoic flying reptile) from the Middle Jurassic of China, Darwinopterus modularis gen. et sp. nov., provides the first insights into a prominent, but poorly understood transition between basal, predominantly long-tailed pterosaurs and the more derived, exclusively short-tailed pterodactyloids. Darwinopterus exhibits a remarkable ‘modular’ combination of characters: the skull and neck are typically pterodactyloid, exhibiting numerous derived character states, while the remainder of the skeleton is almost completely plesiomorphic and identical to that of basal pterosaurs. This pattern supports the idea that modules, tightly integrated complexes of characters with discrete, semi-independent and temporally persistent histories, were the principal focus of natural selection and played a leading role in evolutionary transitions.     

The arboreal leaping theory of the origin of pterosaur flight

Three theories about the origin of flight in pterosaurs have been proposed: 1) the arboreal parachuting theory (passive falling from trees leading to gliding and eventually to powered flight); 2) the cursorial theory (bipedal running and leaping leading directly to powered flight); and 3) the arboreal leaping theory (active leaping between branches and trees leading to powered flight). The available evidence as to the functional morphology of pterosaurs, and in particular their hindlimb, is reviewed and used to test the three theories. Pterosaurs were well suited for arboreality and their hindlimb morphology argues against cursoriality, but supports an arboreal leaping lifestyle for early pterosaurs or their immediate ancestors.     

A new crested pterosaur from the Early Cretaceous of Spain: the first European tapejarid (Pterodactyloidea: Azhdarchoidea)

Background

The Tapejaridae is a group of unusual toothless pterosaurs characterized by bizarre cranial crests. From a paleoecological point of view, frugivorous feeding habits have often been suggested for one of its included clades, the Tapejarinae. So far, the presence of these intriguing flying reptiles has been unambiguously documented from Early Cretaceous sites in China and Brazil, where pterosaur fossils are less rare and fragmentary than in similarly-aged European strata.

Methodology/Principal Findings

Europejara olcadesorum gen. et sp. nov. is diagnosed by a unique combination of characters including an unusual caudally recurved dentary crest. It represents the oldest known member of Tapejaridae and the oldest known toothless pterosaur. The new taxon documents the earliest stage of the acquisition of this anatomical feature during the evolutionary history of the Pterodactyloidea. This innovation may have been linked to the development of new feeding strategies.

Conclusion/Significance

The discovery of Europejara in the Barremian of the Iberian Peninsula reveals an earlier and broader global distribution of tapejarids, suggesting a Eurasian origin of this group. It adds to the poorly known pterosaur fauna of the Las Hoyas locality and contributes to a better understanding of the paleoecology of this Konservat-Lagerstätte. Finally, the significance of a probable contribution of tapejarine tapejarids to the early angiosperm dispersal is discussed.     

Gargantuavis philoinos: Giant bird or giant pterosaur?

Gargantuavis philoinos was described as a giant terrestrial bird on the basis of various postcranial elements (synsacrum and pelvis, femur) from Late Cretaceous (Campanian-Maastrichtian) localities in Southern France. It has recently been suggested that these remains in fact belong to giant pterosaurs. A detailed comparison between bones referred to Gargantuavis and the corresponding skeletal elements of pterosaurs reveals considerable differences and confirms the avian nature of Gargantuavis. The broad pelvis of Gargantuavis is similar to that of various extinct graviportal terrestrial birds.     

Pterosaur tracks and the terrestrial ability of pterosaurs

Unusual tracks of a quadrupedal animal with a three-digit (occasionally four-digit) manus print and four-digit pes print were first interpreted as those of pterosaurs in the 1950s. In the 1980s these tracks were reinterpreted as crocodilian, but new material shows that the original identification was correct. Two features: evidence for elongate penultimate phalanges in digits two to four of the pes, and manus trackways up to three times the width of pes trackways, can only be attributed to pterosaurs. Recent improvements in understanding of pterosaur anatomy and functional morphology explain remaining difficulties regarding the interpretation of ich-nites such as the orientation of the manus digits and the absence of some expected ichnological features. Pteraichnus and Pteraichnus-like tracks show that, when grounded, some, perhaps all, pterosaurs were plantigrade, quadrupedal, and had a semi-erect stance and gait. This is consistent with some functional interpretations of pterosaur anatomy and resolves a long-running debate regarding the terrestrial ability of this group.     

Respiratory Evolution Facilitated the Origin of Pterosaur Flight and Aerial Gigantism

Pterosaurs, enigmatic extinct Mesozoic reptiles, were the first vertebrates to achieve true flapping flight. Various lines of evidence provide strong support for highly efficient wing design, control, and flight capabilities. However, little is known of the pulmonary system that powered flight in pterosaurs. We investigated the structure and function of the pterosaurian breathing apparatus through a broad scale comparative study of respiratory structure and function in living and extinct archosaurs, using computer-assisted tomographic (CT) scanning of pterosaur and bird skeletal remains, cineradiographic (X-ray film) studies of the skeletal breathing pump in extant birds and alligators, and study of skeletal structure in historic fossil specimens. In this report we present various lines of skeletal evidence that indicate that pterosaurs had a highly effective flow-through respiratory system, capable of sustaining powered flight, predating the appearance of an analogous breathing system in birds by approximately seventy million years. Convergent evolution of gigantism in several Cretaceous pterosaur lineages was made possible through body density reduction by expansion of the pulmonary air sac system throughout the trunk and the distal limb girdle skeleton, highlighting the importance of respiratory adaptations in pterosaur evolution, and the dramatic effect of the release of physical constraints on morphological diversification and evolutionary radiation.     

A new non-pterodactyloid pterosaur from the Late Jurassic of southern Germany

Background

The ‘Solnhofen Limestone’ beds of the Southern Franconian Alb, Bavaria, southern Germany, have for centuries yielded important pterosaur specimens, most notably of the genera Pterodactylus and Rhamphorhynchus. Here we describe a new genus of non-pterodactyloid pterosaur based on an extremely well preserved fossil of a young juvenile: Bellubrunnus rothgaengeri (gen. et sp. nov.).

Methodology/Principal Findings

The specimen was examined firsthand by all authors. Additional investigation and photography under UV light to reveal details of the bones not easily seen under normal lighting regimes was completed.

Conclusions/Significance

This taxon heralds from a newly explored locality that is older than the classic Solnhofen beds. While similar to Rhamphorhynchus, the new taxon differs in the number of teeth, shape of the humerus and femur, and limb proportions. Unlike other derived non-pterodacytyloids, Bellubrunnus lacks elongate chevrons and zygapophyses in the tail, and unlike all other known pterosaurs, the wingtips are curved anteriorly, potentially giving it a unique flight profile.     

Air Space Proportion in Pterosaur Limb Bones Using Computed Tomography and Its Implications for Previous Estimates of Pneumaticity

Air Space Proportion (ASP) is a measure of how much air is present within a bone, which allows for a quantifiable comparison of pneumaticity between specimens and species. Measured from zero to one, higher ASP means more air and less bone. Conventionally, it is estimated from measurements of the internal and external bone diameter, or by analyzing cross-sections. To date, the only pterosaur ASP study has been carried out by visual inspection of sectioned bones within matrix. Here, computed tomography (CT) scans are used to calculate ASP in a small sample of pterosaur wing bones (mainly phalanges) and to assess how the values change throughout the bone. These results show higher ASPs than previous pterosaur pneumaticity studies, and more significantly, higher ASP values in the heads of wing bones than the shaft. This suggests that pneumaticity has been underestimated previously in pterosaurs, birds, and other archosaurs when shaft cross-sections are used to estimate ASP. Furthermore, ASP in pterosaurs is higher than those found in birds and most sauropod dinosaurs, giving them among the highest ASP values of animals studied so far, supporting the view that pterosaurs were some of the most pneumatized animals to have lived. The high degree of pneumaticity found in pterosaurs is proposed to be a response to the wing bone bending stiffness requirements of flight rather than a means to reduce mass, as is often suggested. Mass reduction may be a secondary result of pneumaticity that subsequently aids flight.     

Avian Cerebellar Floccular Fossa Size Is Not a Proxy for Flying Ability in Birds

Extinct animal behavior has often been inferred from qualitative assessments of relative brain region size in fossil endocranial casts. For instance, flight capability in pterosaurs and early birds has been inferred from the relative size of the cerebellar flocculus, which in life protrudes from the lateral surface of the cerebellum. A primary role of the flocculus is to integrate sensory information about head rotation and translation to stabilize visual gaze via the vestibulo-occular reflex (VOR). Because gaze stabilization is a critical aspect of flight, some authors have suggested that the flocculus is enlarged in flying species. Whether this can be further extended to a floccular expansion in highly maneuverable flying species or floccular reduction in flightless species is unknown. Here, we used micro computed-tomography to reconstruct “virtual” endocranial casts of 60 extant bird species, to extract the same level of anatomical information offered by fossils. Volumes of the floccular fossa and entire brain cavity were measured and these values correlated with four indices of flying behavior. Although a weak positive relationship was found between floccular fossa size and brachial index, no significant relationship was found between floccular fossa size and any other flight mode classification. These findings could be the result of the bony endocranium inaccurately reflecting the size of the neural flocculus, but might also reflect the importance of the flocculus for all modes of locomotion in birds. We therefore conclude that the relative size of the flocculus of endocranial casts is an unreliable predictor of locomotor behavior in extinct birds, and probably also pterosaurs and non-avian dinosaurs.     

Early Cretaceous (Berriasian) birds and pterosaurs from the Cornet bauxite mine,Romania

Abstract: We revisit a small but extremely significant collection of bird and pterosaur bones from the Lower Cretaceous (Berriasian) of western Romania. These fossils were collected in the late 1970s and early 1980s from a Lower Cretaceous (Berriasian) conglomerate lens deep in a bauxite mine at Cornet, close to the city of Oradea, Romania, and they caused a sensation when first described. Some fossils were initially ascribed to the early bird genus Archaeopteryx as well as to the modern clade Neornithes, an astonishing avian assemblage if correct. Described pterosaurs include dsungaripterids and a cervical vertebra that is likely the oldest azhdarchid pterosaur known from Europe and perhaps the world. Not only does the Cornet azhdarchid support an Eurasian origin for this clade, it is also significant because of its size: it is one of the smallest representatives of this pterosaur clade yet reported. Aside from their phylogenetic affinities, these unique Romanian fossils are also important because of their age; in particular, very few birds are known globally from the earliest Cretaceous. Re‐examination of collections in Oradea confirms the presence of both birds and pterosaurs in the Cornet bauxite: although the fragmentary bird remains are mostly indeterminate, one record of a hesperornithiform is confirmed. There is no evidence for Archaeopteryx at the Cornet site while the two supposed neornithines (Palaeocursornis biharicus Kessler and Jurcsák and Eurolimnornis corneti Kessler and Jurcsák) are based on undiagnostic remains and are here regarded as nomina dubia.     

Did pterosaurs feed by skimming? Physical modelling and anatomical evaluation of an unusual feeding method

Similarities between the anatomies of living organisms are often used to draw conclusions regarding the ecology and behaviour of extinct animals. Several pterosaur taxa are postulated to have been skim-feeders based largely on supposed convergences of their jaw anatomy with that of the modern skimming bird, Rynchops spp. Using physical and mathematical models of Rynchops bills and pterosaur jaws, we show that skimming is considerably more energetically costly than previously thought for Rynchops and that pterosaurs weighing more than one kilogram would not have been able to skim at all. Furthermore, anatomical comparisons between the highly specialised skull of Rynchops and those of postulated skimming pterosaurs suggest that even smaller forms were poorly adapted for skim-feeding. Our results refute the hypothesis that some pterosaurs commonly used skimming as a foraging method and illustrate the pitfalls involved in extrapolating from limited morphological convergence.     

Do different disparity proxies converge on a common signal? Insights from the cranial morphometrics and evolutionary history of Pterosauria (Diapsida: Archosauria)

Disparity, or morphological diversity, is often quantified by evolutionary biologists investigating the macroevolutionary history of clades over geological timescales. Disparity is typically quantified using proxies for morphology, such as measurements, discrete anatomical characters, or geometric morphometrics. If different proxies produce differing results, then the accurate quantification of disparity in deep time may be problematic. However, despite this, few studies have attempted to examine disparity of a single clade using multiple morphological proxies. Here, as a case study for this question, we examine the disparity of the volant Mesozoic fossil reptile clade Pterosauria, an intensively studied group that achieved substantial morphological, ecological and taxonomic diversity during their 145+ million-year evolutionary history. We characterize broadscale patterns of cranial morphological disparity for pterosaurs for the first time using landmark-based geometric morphometrics and make comparisons to calculations of pterosaur disparity based on alternative metrics. Landmark-based disparity calculations suggest that monofenestratan pterosaurs were more diverse cranially than basal non-monofenestratan pterosaurs (at least when the aberrant anurognathids are excluded), and that peak cranial disparity may have occurred in the Early Cretaceous, relatively late in pterosaur evolution. Significantly, our cranial disparity results are broadly congruent with those based on whole skeleton discrete character and limb proportion data sets, indicating that these divergent approaches document a consistent pattern of pterosaur morphological evolution. Therefore, pterosaurs provide an exemplar case demonstrating that different proxies for morphological form can converge on the same disparity signal, which is encouraging because often only one such proxy is available for extinct clades represented by fossils. Furthermore, mapping phylogeny into cranial morphospace demonstrates that pterosaur cranial morphology is significantly correlated with, and potentially constrained by, phylogenetic relationships.     

A possible pterosaur manus track from the Late Cretaceous of Alberta

An isolated track from the latest Campanian–Maastrichtian Wapiti Formation (Alberta) is tentatively identified as a pterosaur manus print. The basic digital formula (digit I < digit II < digit III) is consistent with the plesiomorphic condition in pterosaurs. The track measures 25.5 cm in length, making it the largest putative pterosaur manus print (estimated wingspan 7.7 m) from North America. Although precise chronostratigraphic data are lacking, sedimentary evidence indicates the track comes from a mid‐ to late Campanian fluvial deposits that accumulated approximately 400 km from the closest shoreline within a high‐latitude (65°N) setting.