On the size and flight diversity of giant pterosaurs, the use of birds as pterosaur analogues and comments on pterosaur flightlessness

The size and flight mechanics of giant pterosaurs have received considerable research interest for the last century but are confused by conflicting interpretations of pterosaur biology and flight capabilities. Avian biomechanical parameters have often been applied to pterosaurs in such research but, due to considerable differences in avian and pterosaur anatomy, have lead to systematic errors interpreting pterosaur flight mechanics. Such assumptions have lead to assertions that giant pterosaurs were extremely lightweight to facilitate flight or, if more realistic masses are assumed, were flightless. Reappraisal of the proportions, scaling and morphology of giant pterosaur fossils suggests that bird and pterosaur wing structure, gross anatomy and launch kinematics are too different to be considered mechanically interchangeable. Conclusions assuming such interchangeability--including those indicating that giant pterosaurs were flightless--are found to be based on inaccurate and poorly supported assumptions of structural scaling and launch kinematics. Pterosaur bone strength and flap-gliding performance demonstrate that giant pterosaur anatomy was capable of generating sufficient lift and thrust for powered flight as well as resisting flight loading stresses. The retention of flight characteristics across giant pterosaur skeletons and their considerable robustness compared to similarly-massed terrestrial animals suggest that giant pterosaurs were not flightless. Moreover, the term 'giant pterosaur' includes at least two radically different forms with very distinct palaeoecological signatures and, accordingly, all but the most basic sweeping conclusions about giant pterosaur flight should be treated with caution. Reappraisal of giant pterosaur material also reveals that the size of the largest pterosaurs, previously suggested to have wingspans up to 13 m and masses up to 544 kg, have been overestimated. Scaling of fragmentary giant pterosaur remains have been misled by distorted fossils or used inappropriate scaling techniques, indicating that 10-11 m wingspans and masses of 200-250 kg are the most reliable upper estimates of known pterosaur size.     

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.     

On Zhejiangopterus and the relationships of pterodactyloid pterosaurs

A summary of recent studies on the interrelationships of pterodactyloid pterosaurs is used as a framework for reassessing the taxonomic status of Zhejiangopterus, a new, long‐necked, Late Cretaceous pterosaur from China that has been assigned to the Nyctosauridae. Characters cited in support of this decision include: a notarium, edentulous jaws, and lack of a cranial crest. However, none of these is diagnostic of the Nyctosauridae. Zhejiangopterus exhibits a number of derived characters (orbit relatively small and located in a low position, posteroventrally facing occiput, features of the humerus and ‘T‐shaped’ cross‐section of wing phalanges two and three) only otherwise found in azhdarchids, thus we propose that Zhejiangopterus be reassigned to the Azhdarchidae.     

ON THE RECONSTRUCTION OF PTEROSAURS AND THEIR MANNER OF FLIGHT, WITH NOTES ON VORTEX WAKES

Classical pterosaur reconstructions are variants on a ‘bat-analogy’, whereby the wing is conceived as a simple membrane with no inherent bending strength, stretched between the arm and leg skeletons. The legs are considered to be splayed out to the sides, as in bats, so that the animal would have to adopt a quadrupedal stance on the ground, supported on its feet and the metacarpo-phalangeal joints. In recent years an alternative ‘bird-analogy’ has come to be generally accepted. This hypothesis, most elements of which are due to Padian (1983 a, b) calls for the animal to stand upright on its legs like a bird. The wings are independent of the legs, as in birds, are stiffened by skeletal fibres in the membrane, and have a very narrow, sharply pointed shape. There are difficulties in reconciling the bird-analogy with the evidence. The long-tailed rhamphorhynchs might conceivably have balanced their weight about their hip joints but this would not have been possible for the short-tailed pterodactyls. The bird pelvis shows modifications which permit bipedal standing in spite of the reduction of the tail, but no equivalent adaptations are seen in pterodactyls. Besides, all known pterosaur pelvises, except that of the giant pterodactyl Pteranodon were open ventrally, which would have precluded the legs from being brought to a parasagittal position, as required for bipedal walking. The notion that the wing was not attached to the legs is based on negative evidence, in that no clear impressions of the inner end of the wing membrane are preserved in the fossils. However one pterodactyl fossil shows a membrane edge approaching the ankle joint. In fossils that are preserved with the wings forward, the legs have been pulled forwards by the ankles. A tendon connecting the ankle to the wing tip is consistent with the evidence. The ‘fibres’ in the wing membranes are actually impressions of surface ridges, with no internal structure, and are better interpreted as surface wrinkles in the skin, caused by contraction of elastic fibres within the membrane. The bird analogy also results in a very unsatisfactory wing from an aerodynamic point of view. The structure of an animal wing is best understood in terms of the type of vortex wake it is adapted to generate. Hummingbirds, and insects capable of economical hovering, have wings that can be inverted on the upstroke, and when hovering, generate a wake consisting of two vortex rings per wingbeat cycle. The span of such wings is fixed, which implies that they create a ‘ladder wake’ in cruising flight, consisting of a pair of undulating wing-tip vortices, joined by a transverse vortex at each transition from downstroke to upstroke and back. Normal birds cannot invert their wings, and so are less efficient in hovering, but they can shorten the wing during the upstroke in cruising flight. This creates a ‘concertina wake’, with no transverse vortices. Hummingbirds show very limited migration performance, compared with normal birds, with the implication that a wing capable of creating a concertina wake is more economical in cruising flight than one creating a ladder wake, and is an essential adaptation for long-distance migration. A revised reconstruction of the pterosaur wing starts from the observations that, contrary to the currently popular bird-analogy, pterosaurs were not bipedal, their wings did not contain stiffening fibres but did contain elastic fibres, and the trailing edge of the membrane was supported by a tendon joining the tip of the wing finger to the ankle. A hypothetical arrangement of elastic fibres, that accounts well for the observed pattern of wrinkles in contracted wings, also allows the planform shape of the wing to be adjusted in much the same way as seen in birds, although using a completely different mechanism. It opens the possibility that pterosaurs could fly with a concertina wake, and thus could have been long-distance migrators like modern birds. Although this hypothetical wing is mechanically somewhat bat-like, it is not a return to the classical bat-analogy. It would not have the high degree of control over profile shape, which gives bats their outstanding manoeuvrability. On the other hand bats do not have the degree of control over their wingspan that is suggested here for pterosaurs, and consequently are not notable for migration performance.     

The First Record of the Pterosaur Ichnogenus Purbeckopus in the Late Berriasian (Early Cretaceous) of Northwest Germany

A hypichnium of a manus imprint (preserved as plaster cast) indicates for the first time the presence of the large pterosaur ichnotaxon Purbeckopus cf. pentadactylus Delair, 1963 in the late Berriasian of northwest Germany. It is only the second record of Purbeckopus globally and the first pterosaur track from Germany. It provides evidence of a very large pterosaur (wingspan c. 6 m) in this area and from this time period not yet represented by skeletal remains. When compared with the English type material, the specimen exhibits some differences that are related mostly to different properties of the substrate on which both were left. These include, in the German track, an impression of the metacarpo-phalangeal joint of the wing finger, normally not present in pterosaur tracks. Also interesting is the rather blunt termination of the deeply impressed digits I–III, indicating rather short and blunt claws, which seem more suitable for walking than for grasping or climbing. The specimens of Purbeckopus in England and Germany occur in different environments: the English locality was situated close to a brackish lagoon, while the German site belongs to a limnic-deltaic system at the margin of a large, freshwater lake.     

The evolution of HoxD-11 expression in the bird wing: insights from Alligator mississippiensis

Background

Comparative morphology identifies the digits of the wing of birds as 1,2 and 3, but they develop at embryological positions that become digits 2, 3 and 4 in other amniotes. A hypothesis to explain this is that a homeotic frame shift of digital identity occurred in the evolution of the bird wing, such that digits 1,2 and 3 are developing from embryological positions 2, 3 and 4. Digit 1 of the mouse is the only digit that shows no late expression of HoxD-11. This is also true for the anterior digit of the bird wing, suggesting this digit is actually a digit 1. If this is the case, we can expect closer relatives of birds to show no HoxD-11 expression only in digit 1. To test this prediction we investigate HoxD-11 expression in crocodilians, the closest living relatives of birds.

Methodology/Principal Findings

Using degenerate primers we cloned a 606 nucleotide fragment of exon 1 of the alligator HoxD-11 gene and used it for whole-mount in-situ detection in alligator embryos. We found that in the pentadactyl forelimbs of alligator, as in the mouse, late expression of HoxD-11 is absent only in digit 1.

Conclusions/Significance

The ancestral condition for amniotes is that late-phase HoxD-11 expression is absent only in digit 1. The biphalangeal morphology and lack of HoxD-11 expression of the anterior digit of the wing is like digit 1 of alligator and mouse, but its embryological position as digit 2 is derived. HoxD-11 expression in alligator is consistent with the hypothesis that both digit morphology as well as HoxD-11 expression are shifted towards posterior in the bird wing.     

An attempt to reconstruct the lifestyle of confuciusornithids (Aves,Confuciusornithiformes)

The lifestyle of some representatives of the family Confuciusornithidae is reconstructed based on the analysis of osteological data, horn structures, and taphonomy. Confuciusornithids, which resemble extant Phaethon in general appearance, fed on fish, catching them from the surface layer of freshwater lakes. They rested and probably nested in trees growing near the basin. When moving in the tree canopy, they used the second digit of the wing, free from an alula and equipped with a well-developed claw. Unable to take off from the ground, they used the fourth digit of the forearm, which was free from feathers, for climbing tree trunks. A pair of elongated caudal feathers (rectrices) were probably used to attract mates.     

On wing disparity and morphological variation of the Santana Group pterosaurs

Pterosaurs were widely spread throughout the Mesozoic Era, populating the whole world. Among this great diversity, two groups are commonly found in Brazil: the Anhangueridae and Tapejaridae. These can be mainly identified by cranial synapomorphies. However, because of the fragility of the pterosaur skeleton and rarity of the fossilisation process, the fossils found are usually incomplete, which hampers a proper taxonomic identification of the specimens. The specific proportions of these two groups of pterosaurs were obtained from bibliographic data and measurements of specimens. Eight Anhangueridae-like and seven Tapejaridae were used: Anhanguera piscator, Anhanguera santanae, Anhanguera spielbergi, Araripesaurus castilhoi, Barbosania gracilisrostris and three Anhangueridae sp. indet.; Sinopterus dongi, Tapejara wellnhoferi and five Tapejaridae sp. indet. We find that proportions of the humerus, wing metacarpal, first phalanx of the wing digit, femur and tibia are sufficient to identify partial remains of Araripe pterosaurs. A principal component analysis shows that each clade has different, non-overlapping scores in the studied ratios and these can be used with precision. Specific bone ratios for fast identification of anhanguerids and tapejarids are given, opening a broader way to diagnostic fragmentary bones.     

Discovery of a Rare Pterosaur Bone Bed in a Cretaceous Desert with Insights on Ontogeny and Behavior of Flying Reptiles

A pterosaur bone bed with at least 47 individuals (wing spans: 0.65–2.35 m) of a new species is reported from southern Brazil from an interdunal lake deposit of a Cretaceous desert, shedding new light on several biological aspects of those flying reptiles. The material represents a new pterosaur, Caiuajara dobruskii gen. et sp. nov., that is the southermost occurrence of the edentulous clade Tapejaridae (Tapejarinae, Pterodactyloidea) recovered so far. Caiuajara dobruskii differs from all other members of this clade in several cranial features, including the presence of a ventral sagittal bony expansion projected inside the nasoantorbital fenestra, which is formed by the premaxillae; and features of the lower jaw, like a marked rounded depression in the occlusal concavity of the dentary. Ontogenetic variation of Caiuajara dobruskii is mainly reflected in the size and inclination of the premaxillary crest, changing from small and inclined (∼115°) in juveniles to large and steep (∼90°) in adults. No particular ontogenetic features are observed in postcranial elements. The available information suggests that this species was gregarious, living in colonies, and most likely precocial, being able to fly at a very young age, which might have been a general trend for at least derived pterosaurs.     

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.     

Bambi and Sp8 Expression Mark Digit Tips and Their Absence Shows That Chick Wing Digits 2 and 3 Are Truncated

An often overlooked aspect of digit development is the special nature of the terminal phalanx, a specialized structure with characteristics distinct from other phalanges, for example the presence of ectodermal derivatives such as nails and claws. Here, we describe the unique ossification pattern of distal phalanges and characteristic gene expression in the digit tips of chick and duck embryos. Our results show that the distal phalanx of chick wing digit 1 is a genuine tip with a characteristic ossification pattern and expression of Bambi and Sp8; however, the terminal phalanx of digits 2* and 3 is not a genuine tip, and these are therefore truncated digits. Bambi and Sp8 expression in the chick wing provides a direct molecular assessment of digit identity changes after experimental manipulations of digit primordia. In contrast, digits 1 and 2 of the duck wing both possess true tips. Although chick wing-tip development was not rescued by application of Fgf8, this treatment induced the development of extra phalanges. Grafting experiments show that competence for tip formation, including nails, is latent in the interdigital tissue. Our results deepen understanding of the mechanisms of digit tip formation, highlighting its developmental autonomy and modular nature, with implications for digit reduction or loss during evolution. * Numbering of wing digits is 1, 2, 3 from anterior to posterior.     

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.     

Climate,isolation and intraspecific competition affect morphological traits in an endangered steppe bird,the Dupont’s Lark Chersophilus duponti

Capsule: We assess biometric variation in the threatened Dupont’s Lark along a wide fraction of its distribution area analysing the largest data set for this bird species available to date, comprising a 28-year period and including birds captured in Spain, Morocco and Tunisia.

Aims: To analyse Dupont’s Lark morphology evaluating five potential sources of divergence: (I) sexual dimorphism, (II) macro-regional differences, (III) climate, (IV) isolation and (V) intraspecific competition.

Methods: Multivariate analysis was used to summarize biometric data. Sexual dimorphism and macro-regional divergence were assessed by generalized linear mixed models. Climate, isolation and intraspecific competition effects on phenotype were explored by means of model averaging.

Results: Sexes differed in wing shape suggesting a sexual selection pressure on males for aerial displays. Males showed longer bills after controlling for body size. We found an increasing Spain?Conclusion: We found convincing results for wing morphology variation in relation to intrasexual competition, as males seem to be subjected to a sexual selection pressure for aerial display and this adaptation strengthens when intraspecific competition increases. We also found solid support for Allen’s rule, with results suggesting that bill size plays an important role in the bird’s thermoregulation, which does not occur in the case of tarsus. Although Bergmann’s rule is not supported in relation to minimum annual temperature, we found a relationship with thermal conditions in the breeding season, as well as water availability.     

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.     

Three‐dimensional geometry of a pterosaur wing skeleton,and its implications for aerial and terrestrial locomotion

This study reports on the three‐dimensional spatial arrangement and movements of the skeleton of Anhanguera santanae (Pterodactyloidea: Ornithocheiridae), determined using exceptionally well‐preserved uncrushed fossil material, and a rigid‐body method for analysing the joints of extinct animals. The geometric results of this analysis suggest that the ornithocheirids were inherently unstable in pitch and yaw. As a result, pitch control would probably have been brought about by direct adjustment of the angle of attack of the wing, by raising or lowering the trailing edge from the root using the legs if, as is indicated in soft‐tissue specimens of a number of unrelated pterosaur species, the legs were attached to the main wing membrane, or by using long‐axis rotations at the shoulder or wrist to raise and lower the trailing edge from the wingtip. An analysis of the three‐dimensional morphology of the wrist lends support to the idea that the pteroid – a long, slender wrist bone unique to pterosaurs that supported a membranous forewing – was directed forwards in flight, not towards the body. As a result, the forewing could have fulfilled the function of an air‐brake and high‐lift device, and may also have had an important role in pitch, yaw, and roll control. The joint analysis is consistent with a semi‐erect quadrupedal model of terrestrial locomotion in the ornithocheirids. © 2008 The Linnean Society of London, Zoological Journal of the Linnean Society, 2008, 154 , 27–69.     

New models for the wing extension in pterosaurs

All powered flying animals have to face the same energetic problems: operating the wings during steady flight with muscles that require constant energy input and neural control to work. Accordingly the extant flying vertebrates have apparently found very similar solutions to parts of these issues – the biomechanical automatism built in their skeletal, muscular and connective tissue system. Based on these extant analogues (birds and bats) two new models are presented here for the mechanism of the distal wing extension in pterosaurs, an extinct group of flying vertebrates. The elongate fourth finger which solely supported their extensive flight membrane was a long lever arm that experienced significant loads and for which a reduction in muscle mass through automatisation would have been strongly beneficial. In the first model we hypothesize the presence of a propatagial ligament or ligamentous system which, as a result of the elbow extension, automatically performs and maintains the extension of the wing finger during flight and prohibits the hyperextension of the elbow. The second model has a co-operating bird-like propatagial ligamentous system and bat-like tendinous extensor muscle system on the forearm of the hypothetical pterosaur. Both models provide strong benefits to an animal with powered flight: (1) reduction of muscles and weight in the distal wing; (2) prevention of hyper extension of the elbow against drag; (3) automating wing extension and thereby reducing metabolic costs required to operate the pterosaurian locomotor apparatus. These models, although hypothetical, fit with the existing fossil evidence and lay down a basis for further biomechanical and/or aerodynamical investigations.     

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.     

Constraints on the wing morphology of pterosaurs

Animals that fly must be able to do so over a huge range of aerodynamic conditions, determined by weather, wind speed and the nature of their environment. No single parameter can be used to determine-let alone measure-optimum flight performance as it relates to wing shape. Reconstructing the wings of the extinct pterosaurs has therefore proved especially problematic: these Mesozoic flying reptiles had a soft-tissue membranous flight surface that is rarely preserved in the fossil record. Here, we review basic mechanical and aerodynamic constraints that influenced the wing shape of pterosaurs, and, building on this, present a series of theoretical modelling results. These results allow us to predict the most likely wing shapes that could have been employed by these ancient reptiles, and further show that a combination of anterior sweep and a reflexed proximal wing section provides an aerodynamically balanced and efficient theoretical pterosaur wing shape, with clear benefits for their flight stability.