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Pterosaurs, the flying reptiles of the Mesozoic, often play second fiddle in popularity to theircontemporaries, the dinosaurs. Such treatment conceals the remarkable diversity and biology of thisgroup: not only were pterosaurs the first vertebrates to achieve powered flight, but they also existedfor 160 million years—longer than any other flying vertebrates. Named after the Uzbek mythical dragon‘azhdarkho’, the Azhdarchidae are among the most enigmatic of all pterosaurs. As with most pterosaurs,azhdarchid remains are rare, and their fossil record is largely represented by isolated bones orincomplete skeletons. Despite the collection of azhdarchid fossils over the last 100 years, recognition ofthese pterosaurs as a distinct group was not achieved until relatively recently. It is now clear that theazhdarchids were a highly successful group that probably first appeared in the Early Cretaceous,gradually spreading across the globe until the latest Cretaceous when they, as one of the last remaininggroups of pterosaurs, became extinct. Although most notable for achieving wingspans comparable withlight aircraft, other aspects of azhdarchid morphology and ecology make them not just aberrant animalsbut also unusual pterosaurs.

Azhdarchidae as the last and most derived family toevolve (Fig. 1). Cretaceous forms such as Tapejara andTupuxuara are perhaps the closest related taxa to theazhdarchids, sharing similarities in their toothlessjaws, relatively short wings and subequal limbs.

Fossils explained 53Titans of the skies: azhdarchid pterosaurs

Mark WittonPalaeobiology Research

Group, School of Earth and

Environmental Sciences,

University of Portsmouth,

Portstmouth PO1 3QL, UK.

mark.witton@port.ac.uk

Azhdarchid origins

Some controversy surrounds the ancestry ofpterosaurs, but most agree that they should beincluded within Archosauria, the reptilian group thatincludes crocodiles, dinosaurs and birds. Exactlywhere they fall in this category is still debatedbecause of the highly specialised nature of even themost basal pterosaurs: their highly modified skeletonsleave few clues to their ancestry. The first pterosaurfossils are found in the late Triassic, and these basalgroups are typically characterized by long tails andtoothed jaws. These groups dominated pterosaurevolution until the late Jurassic but ultimately yieldedcontrol of the skies to a diverse group of derived, tail-less pterosaurs: the Pterodactyloidea. This groupdiversified in the Early Cretaceous and includes the

Fig. 1. Relationships of the Pterodactyloidea (based on Unwin2003—see Suggested reading). ‘Basal pterosaurs’ is used here torefer to all pterosaur taxa basal to Pterodactyloidea. Althoughpterosaur systematics are controversial, the Azhdarchidae arefrequently suggested to be the most derived clade withinPterodactyloidea. Basal pterosaurs are represented by the skull ofRhamphorhynchus, Ornithocheiroidea by Coloborhynchus,Ctenochasmatoidea by Gnathostoma, Dsungaripteridae byGermanodactylus, Tapejaridae by Tapejara, and the Azhdarchidae byQuetzalcoatlus.

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The earliest occurrences of azhdarchid fossilsoccur in Lower Cretaceous deposits of China andBrazil, although controversial material from Tanzaniamay extend azhdarchid origins down into the UpperJurassic of Africa. Because the first well-preservedazhdarchid material occurs in geographically distantregions, their location of origin is unclear.Azhdarchids appear to have become more widespreadin the Northern Hemisphere than the Southern, withnumerous finds from Upper Cretaceous rocks acrossAsia, Europe and North America (Fig. 2), but remainsin Australia and New Zealand indicate thatazhdarchids were also present in southern regions byLate Cretaceous times.

Skeletal anatomy

Azhdarchid skeletons possess many features thatclearly distinguish them from other pterosaurs(Fig. 3). Their jaws are straight and elongate (over

2 m long in some species) but possess no teeth.Instead, foramina lining the jaws of some taxaindicate that a bird-like horny beak was present. Theskull is lightened by a large pneumatized foramenknown as the nasoantorbital fenestra (within whichthe nostrils were placed) and reduced jaw muscles.The neck in some taxa is almost twice as long as thehead (making them the longest necks of anypterosaurs); a highly diagnostic feature achievedthrough hyperelongation of the mid-series neckvertebrae. Unlike most other pterosaurs, the neck ofazhdarchids articulates with the underside of thecranium and orientates the long axis of the skull,almost 90° to the shaft of the neck in some species.Structures on the middle-neck vertebrae suggest astiff neck with very limited articulation, whilst thecranial condyle is reduced to a poorly developed,hemispherical structure allowing restrictedmovement of the skull.

As with all pterosaurs, the torso is short (perhapsless than half the length of the skull) but stronglyfused to anchor the flight muscles of the arms andlegs. The wings comprise a short but powerfully builthumerus, with the radius and ulna leading to a long,robust metacarpal which in turn supports a relativelyreduced wing finger. This finger supported the mainflight membrane; a thin but responsive organ alsoattached to the forearm, torso and leg. In allpterosaurs the wing area is increased throughadditional membranes supported between the pteroid(a long bony shaft projecting from the wrist) andshoulder, with a third set of membranes between thetail and hindlimbs. When grounded, azhdarchidswalked on the distal end of their wing metacarpal(further supported by three small digits) and, becauseof unusually long hindlimbs, may have held their

Fig. 2. Reported occurrences ofazhdarchid fossils across theglobe.

Fig. 3. Restoration of theskeleton of Quetzalcoatlus, alarge azhdarchid from Texas.

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body almost parallel with the ground whilst standingand walking. This contrasts with other largepterosaurs that had disproportionately long forelimbs,forcing the body into a more erect posture whilstwalking and perhaps limiting their terrestrialcapability. Such limb disproportions are not seen inazhdarchids however, suggesting a terrestrialprowess better than most pterosaurs.

The largest flying animals ever?

Many pterosaurs grew to sizes far in excess of anyliving birds, but no other pterosaur group obtainedgigantic size as frequently as the azhdarchids. Earlyforms held modest wingspans of 2.5 m, but their sizeincreased steadily throughout the Cretaceous untilthey had the largest wingspans of any flyingvertebrates (Fig. 4). Their size was the cause of someconfusion in the early twentieth century: anextremely elongate neck-vertebra discovered inJordan in the 1920s (now known to belong to theazhdarchid Arambourgiania) was originally thoughtto be a pterosaur wing element, such was its size andpeculiar features. It was not until the 1970s and thediscovery of more complete azhdarchid material inUpper Cretaceous deposits of Texas that the true sizeof the azhdarchids was appreciated. These sedimentsyielded three azhdarchid individuals belonging to thegenus Quetzalcoatlus, with one, despite itsfragmentary nature, clearly enormous. Initialestimates gave this giant a wingspan of somewherebetween 11 and 21 m, but an improvedunderstanding of azhdarchid anatomy now favoursthe lower estimate. When standing, the shoulder ofQuetzalcoatlus would have stood some 2.5 m off theground—a height comparable with a mature Asianelephant. The discovery of Quetzalcoatlus promptedsome aeronautical engineers to state that the genus

represented the largest flying creature possible.However, and very likely to the dissatisfaction ofaeronautical engineers everywhere, new discoveriesin Europe and a reappraisal of fossil material of thegenus Arambourgiania hint at forms with wingspansof 12 m or more. Equally, the probability offossilization indicates that the azhdarchid individualsknown to palaeontologists are very likely to be ofaverage sizes: truly enormous, freakishly bigindividuals have almost no chance of entering thefossil record but are very likely to have existed in thesame way that giant individuals are seen in modernanimal populations. Being so much larger than allother known flying animals, it seems quite plausiblethat the azhdarchids were indeed the largest fliers ofall time.

Despite their enormous size, azhdarchids possesstypical pterosaur features of hollow and extremelythin-walled bones. An extensive pneumatic systemand thin bone histology makes azhdarchid skeletonsdeceptively lightweight and, although establishingpterosaur mass is controversial to the point wheresome workers claim it impossible, most workers agreethat even the largest azhdarchids would had weighedrelatively little. Estimates for Quetzalcoatlus with a 10–11 m wingspan range from 70 to 250 kg, but it is

Fig. 5. Azhdarchid wingconfiguration (demonstrated byQuetzalcoatlus—bottom left)compared to Pteranodon(bottom right). The shorter,broader wings of the azhdarchidare more akin to the staticallysoaring Andean condor (top left)than the dynamically soaringwandering albatross (top right).

Fig. 4. Size ranges ofazhdarchids. The fragmentaryremains of many giantazhdarchids (such asArambourgiania) mean thattheir sizes can only be estimatedbased on more completematerial from other azhdarchidtaxa. In the case ofArambourgiania, wingspans of11–13 m are predicted; thelargest estimate is figured here.

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probable that the latter figure is far too high. A figurebetween 70 and 85 kg conforms more to ourunderstanding of pterosaur anatomy and flightdynamics, but more data regarding pterosaur softtissues is needed before these figures can be verified.

In the air

As seems to be the case with many fossil groups,palaeontologists did not portray an attractive pictureof pterosaurs for much of the twentieth century.Pterosaur aerodynamics were particularly criticised,with flight modelling of large pterosaurs during the1970s casting doubts over their flight capabilities. Itwas thought that take-off was particularly difficult,with either a headwind or a long drop from a cliffedge required to become airborne. It was evensuggested that if conditions were too adverse thepterosaurs would have to remain grounded as theirclumsy flight capability would not have withstood theflight stresses of blustery conditions. This attitude hasnow changed to one more understanding of thishighly successful and diverse group: evidence fromnumerous pterosaur fossils indicates that manyspecies had a hair-like integument covering theirbodies, necks and skulls, perhaps suggesting thatpterosaurs controlled their core body temperatures ina manner similar to all modern actively flyinganimals (birds, bats and flying insects possessmethods of temperature regulation). This possibilityhas led to thoughts that pterosaurs were active,powerfully flying creatures able to become airborneregardless of weather or topographical conditions.Because of their size many azhdarchids probablyrequired a brief run-up to assist with take-off, as seenin larger species of modern birds. Such locomotionwas probably possible: pterosaur trackways indicatethat pterosaurs may have been competent terrestrialanimals, with both quadrupedal galloping and bipedalrunning possibly used during take-off. Althoughheadwinds, slopes and cliffs may have assistedazhdarchids in becoming airborne, it seems unlikelythat they would be mandatory for take-off.

Many large pterosaurs are thought to have beendynamic soarers akin to modern gulls and albatross,

manipulating air currents to travel with minimalexpenditure of energy on flapping, but severalfeatures of azhdarchid skeletons indicate that theirmethod of flight may have been different. Because thepterosaur wing incorporates both sets of limbs in itsconstruction, an idea of wing shape or aspect ratio(AR = wingspan2/wing area) can be ascertainedthrough relative limb lengths (Fig. 5). Most largepterosaurs had disproportionately long forelimbscompared to their hindlimbs and consequently havelong, narrow wings (high aspect ratio). However,azhdarchids have relatively long hind limbs andtruncated distal components of the wing finger,resulting in relatively short and broad wings (lowaspect ratio).

This low aspect ratio has implications for otherbasic flight calculations. Wing loading (WL = mass/wing area) is indicative of flying style: high wingloading is typical of faster flight whereas low wingloading suggests a gentler pace. Generally, estimatesof pterosaur wing loading are lower than flyingvertebrates of equivalent dimensions, although thereare no modern flying animals large enough tocompare the biggest azhdarchids against. Because oftheir broad wings azhdarchids have lower wingloading values than other large pterosaurs,suggesting that azhdarchids may have flownrelatively slowly. Although smaller forms may havebeen capable of powered, flapping flight, the energyrequirements for flapping flight in larger azhdarchidsprobably excluded the largest forms from this activity.

The position of the shoulder joint (glenoid) is alsounusual in azhdarchids. It is neither in the ‘top-decker’ configuration seen in ornithocheiroidpterosaurs or the ‘bottom-decker’ condition knownfrom tapejarid pterosaurs, but instead forms a ‘middledecker’ construction with the glenoid positionedhalfway up the shoulder girdle (Fig. 6). ‘Top-decker’pterosaurs carried their centre of gravity beneath thewings for stable flight (akin to a modern cargo plane)whereas ‘bottom-deckers’ acted more like fighterplanes with the wings below the centre of gravity,making for a less stable but more manoeuvrableconfiguration. As such, the unique ‘middle-decker’system of azhdarchids may have been a compromise

Fig. 6. Shoulder and wingstructures in pterosaurs (basedon Frey et al. 2003—seeSuggested reading). The stable‘top-decker’ configuration withthe centre of gravity (indicatedby crosses) below the wings(top) seen in ornithocheiroidpterosaurs; the characteristicazhdarchid ‘middle-decker’configuration with the centre ofgravity between the wings; andthe unstable ‘bottom-decker’configuration seen in tapejaridpterosaurs with the centre ofgravity above the wings.

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between stability and manoeuvrability.Although many of these characters make

azhdarchids unique amongst pterosaurs, they doconform to some types of extant birds. Azhdarchidsmay have not been dynamic soarers like gulls, buttheir wing loading and aspect ratios indicate thatthey may have been static soarers akin to modernvultures and storks. These birds manipulate thermalupdrafts to gain high altitude, then slowly glide to thenext thermal column. The increased manoeuvrabilityoffered by the ‘middle-decker’ shoulder configurationmay have enabled large azhdarchids to control theirposition within thermals more efficiently. As suchupdrafts are not generated readily on open water, itseems unlikely that large azhdarchids were capable oflong-distance migration over bodies of water assuggested by some authors—if azhdarchids didperform long, trans-continental migrations, theyprobably did so over land. The unusual abundance ofazhdarchid remains in continental deposits maysupport this notion; most large pterosaur remains arepreserved in open marine or coastal sediments,implying a different environmental preference forazhdarchids. Because of their lower masses and lowerenergy requirements to achieve flapping flight,smaller azhdarchids may have been capable offlapping flight as well as soaring.

Feeding habits

The majority of pterosaur fossils are found in marineor coastal sediments, ranging from near-shorelagoons to shallow seaways. Although someazhdarchids are found in such settings, most arefound in lucustrine deposits and, when found inmarine deposits, azhdarchids are often associatedwith material derived from continental settings suchas plants or dinosaur fossils. This strongly suggests amore land-based ecology for azhdarchids than otherpterosaurs: from palaeoenvironmental analysis ofazhdarchid bearing sediments, it seems thatazhdarchids like Quetzalcoatlus inhabited aridenvironments with few large bodies of water, whilstothers such as Zhejiangopterus occupied woodedsettings crossed with small rivers and streams.

Some controversy has surrounded the ecologicalsignificance of the apparent azhdarchid preference forterrestrial environments, particularly concerningtheir feeding habits. Because of its unusual habitatand in situ association with numerous sauropoddinosaur remains, Quetzalcoatlus has been suggestedto be a scavenger of large dinosaur carcasses. Otherworkers have argued that, because of the richness oftrace fossils and burrows in the Quetzalcoatlushorizon, large azhdarchids probed for invertebrateinfauna. Both these suggestions ignore the long, rigid

neck of azhdarchids; modern avian scavengers andprobers have flexible necks able to probe deep intocarcasses or investigate narrow burrows, suggestingthat these lifestyles are not viable for azhdarchids.Most authors currently cite aerial fishing as the mostlikely method of azhdarchid feeding, plucking fish andother pelagic organisms from bodies of water byeither dip feeding or skimming. However, thestructure of the neck also makes these interpretationsproblematic. Modern birds that partake in dip feedinghave short, flexible necks capable of curving ventrallyto minimize drag and resistance when submergingtheir jaws into the water during feeding. The neckalso articulates with the skull at an angle slightlybelow horizontal, facing the long-axis of the skullessentially forwards. The long, stiff necks and stronglydownturned skulls of azhdarchids bear littleresemblance to their analogues in modern dip-feedersand would surely impair their ability to feed in thismanner. Skim-feeding like that seen in the modernbird Rhyncops is also unlikely; although laterallycompressed, the mandibles of azhdarchids do notshow the extreme degree of lateral compression seenin modern skimmers; nor do they possess thehorizontally orientated skulls or short, strong neck ofskimming animals.

A model for azhdarchid feeding that complies morewith their anatomy is that azhdarchids acted in asimilar manner to some modern storks, obtainingmost of their food when foraging terrestrially orwading (Fig. 7). Such a lifestyle explains manyotherwise problematic anatomical features ofazhdarchid skeletons. The relatively long hindlimbsposition the torso sub-horizontally, extending theneck forward along a horizontal plane, holding theskull close to the ground. With a sub-horizontallyheld neck and ventrally-orientated occipital condylethe head is naturally directed downwards, a useful

Fig. 7. A Quetzalcoatlus seizesan unwary crocodile in aCretaceous swamp. Whetherazhdarchids fed in this manner iscontroversial, but many aspectsof their skeleton imply thatwading was certainly a potentialfeeding option.

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adaptation for large animals feeding at ground level.The elongate skull positions the jaw tips close to

feeding level, whilst the peculiar stiffness of the neckmay have served to minimize the energyrequirements to hold the head in feeding position.The length of the neck may have allowed azhdarchidsto extend their feeding range into areas where theycould otherwise not reach—such as the deeperwaters of rivers or lakes. It is not inconceivable toimagine azhdarchids standing in shallow water oralong riverbanks with open jaws suspended in thewater column, snagging fish and other forms as theyswam between the jaws or perhaps even collectingprey whilst walking across plains and woodlands. Thestraight nature of azhdarchid beak morphologysuggests that they did not specialize in one food itemand, as with storks, a vast range of small vertebratesmay have been eaten. More work is needed beforeany of these hypotheses can be verified but, on atheoretical level at least, the latter idea seems mostsatisfactory.

A dying breed?

The azhdarchids are among some of the lastpterosaurs known. It seems that pterosaur diversitydeclined towards the end of the Mesozoic and, by thelatest Cretaceous, only the azhdarchids remained inany abundance (a few other pterosaur lineages mayhave been present at this time, but their remains arerare). It has been suggested that the apparent declineof pterosaurs may merely be a taphonomic artefact,perhaps instigated by a shift of pterosaur habit frommarine environments towards continental settings.These environments are less likely to be preserved inthe geological record and do not provide manysettings conducive to fossilization, possibly hiding trueLate Cretaceous pterosaur diversity. Thedisappearance of azhdarchids from the fossil record atthe end of the Mesozoic is often attributed to theirsize: larger animals are more prone to extinctionthrough slower rates of reproduction and higherenergy requirements.

The extinction of the azhdarchids and pterosaursmay be attributed to competition from birds, a groupwhich appear to have gradually replaced pterosaursin a variety of roles throughout the Cretaceous. Asthe continental environments that the azhdarchids

had apparently become well adapted-to changed atthe termination of the Mesozoic it appears thatbirds—and not azhdarchids—possessed the necessarydiversity and numbers to progress into the Tertiary.No flying animals before or since the azhdarchidshave managed to capture their size or grandeur;although we now only have fossils as evidence oftheir presence, they clearly demonstrate thatazhdarchids must have been fantastic sights tobehold.

Suggestions for further reading

Chatterjee, S. & Templin, R.J. 2003. Posture,Locomotion and Palaeoecology of the Pterosaurs.Geological Society of America Special Publication,v.376, pp.1–64.

Kellner, A.W.A. & Langston, W. Jr. 1996. Cranialremains of Quetzalcoatlus (Pterosauria,Azhdarchidae) from Late Cretaceous sediments ofBig Bend National Park. Journal of VertebratePaleontology, v.16, pp.222–231.

Langston, W. Jr. 1981. Pterosaurs. Scientific American,v.244, pp.92–102.

Frey, E., Buchy, M.-C. & Martill, D.M. 2003. Middle-and bottom-decker Cretaceous pterosaurs: uniquedesigns in active flying vertebrates. In: Buffetaut,E. & Mazin, J.-M. (eds), Evolution and Palaeobiologyof Pterosaurs. Geological Society SpecialPublication, v.217, pp.267–274.

Martill, D.M. & Frey, E. 1998. Discovery of theholotype of the giant pterosaur Titanopteryxphiladelphiae Arambourg 1959, and the status ofArambourgiania and Quetzalcoatlus. Neues Jahrbuchfür Geologie und Paläontologie, Abhandlungen, v.207,pp.57–76.

Ösi, A., Weishampel, D.B. & Jianu, C.M. 2005. Firstevidence of azhdarchid pterosaurs from the LateCretaceous of Hungary. Acta PalaeontologicaPolonica, v.50, pp.777–787.

Unwin, D.M. 2003. On the phylogeny andevolutionary history of pterosaurs. In: Buffetaut, E.and Mazin, J. M. (eds), Evolution and Palaeobiology ofPterosaurs, Geological Society Special Publication,v.217, pp.139–190.

Unwin, D.M. 2005. The Pterosaurs from Deep Time. PiPress, New York.