Pterosaurs: Flying Reptiles of the Mesozoic Darren Naish University of Southampton

Pterosaurs: winged diapsid reples of the Mesozoic, membranous wings supported by super-enlarged 4th finger. Toothed & toothless species.

Known since late 1700s; ‘Ptero-dactyle’ named by George Cuvier in 1809.

The wing Main spar supported by super-enlarged, thickened 4th finger and associated 4th metacarpal with roller-like distal end. Unique, rod-like bone at the wrist - the pteroid – controls posion and shape of membrane between shoulder and wrist. Three small, clawed fingers in most (but not all) species.

Pteroid is somemes incredibly long: in , more than 50% length of radius Pterosaurs in popular mythology: typically called ‘pterodactyls’, they are scaly, dull-coloured, bat-winged monsters with prehensile feet Pterosaurs: not scaly, but hairy Sordes Exceponal show that pterosaur bodies were covered in hair-like fibres known as pycnofibres. Best known for Sordes from Central Asia, but pycnofibres now known from numerous , Jurassic and Species from across the family tree. Pterosaurs had fuzzy coats, probably for insulaon.

Fibres on top of skull of Sordes

Fibres on side of body of anurognathid The extent of the main part of the wing membrane has been controversial Distal part universally agree to be narrow and slender (= high-aspect), but proximal part argued to be broad, and to incorporate some/all hindlimb, by some, and narrow and aaching to body by others. Fossils show that brachiopatagium did aach to hindlimb, being most extensive in non- pterodactyloids.

Brachiopatagium aaching to bia in Cretaceous azhdarchoid

Brachiopatagium aaching to ankle (perhaps to long 5th toe) in Jurassic rhamphorhynchid Sordes Pterosaur wing membranes were internally complex The ‘darkwing’ specimen, examined under UV light, reveals the presence of a massive, looping blood vessel system, a layer of subparallel supporng fibres, and a layer with a mesh-like network of connected ssue strands.

These features suggest that (while thin) the membrane was robust, internally supported, perhaps used in thermoregulaon (or even respiraon). Frey, E., Tischlinger, H., Buchy, M.-C. & Marll, D. M. 2003. New specimens of Pterosauria (Replia) with so parts with implicaons for pterosaurian anatomy and locomoon. In Buffetaut, E. & Mazin, J.-M. (eds) Evoluon and Palaeobiology of Pterosaurs. Geological Society Special Publicaon 217. The Geological Society of London, pp. 233-266. Skeletal pneumacity: pterosaurs, like birds and other saurischian dinosaurs, had pneumac bones. Air-filled sacs connected to the lungs were distributed throughout the body, and occupied most of the skeleton. Demonstrated by pneumac foramina and hollow bones. Pneumac foramina (pf) and hollow bones here illustrated for ornithocheiroid . So-ssue pneumacity: when skeletal pneumacity is present, a series of air-filled sacs connected (by tubes called divercula) to the lungs are also present. Pterosaurs had air-sacs throughout the body cavity, also extending along the length of wing and wing-finger.

Distribuon of air-sacs in Cretaceous ornithocheiroid Anhanguera

Pneumacity present in earliest pterosaurs: was it a primive feature for the group, shared with dinosaurs? Or did it evolve independently? This remains unknown and controversial. What are pterosaurs? They are undoubted members of Neodiapsida, and almost certainly members of Archosauromorpha. But where within this clade do their affinies lie? Sll somewhat controversial. Hypothesis 1. Pterosaurs are crown-archosaurs (they have an antorbital fenestra), and share a list of characters with dinosaurs (hinge-like ankle, long neck): there is a pterosaur + dinosaur clade within crown-Archosauria. Hypothesis 2, 3 and 4. Pterosaurs are only convergently similar to dinosaurs, are outside of crown-Archosauria, and (1) are protorosaurs, (2) are close to drepanosaurs, or (3) are close to Archosauria, but not part of it.

Specialists are sll arguing over these compeng hypotheses and pterosaur affinies have yet to be resolved A quick history of pterosaurs Pterosaurs appear in Late Triassic, persist to end of Late Cretaceous. All early pterosaurs (non-pterodactyloids or “rhamphorhynchoids”) are small predators of small . Pterodactyloids evolved in Middle Jurassic: possessed combined nostril + antorbital fenestra (termed nasoantorbital fenestra or NAOF). Evolve giant size (wingspans of c 10 m) and several lineages evolve toothlessness. Pterodactyloids dominate Cretaceous: include oceanic, fish-eang ornithocheiroids, strongly terrestrial dsungaripteroids and azhdarchoids. Only ornithocheiroids and azhdarchoids persist to very end of Late Cretaceous. A quick history of pterosaurs Pterosaurs appear in Late Triassic, persist to end of Late Cretaceous. All early pterosaurs (non-pterodactyloids or “rhamphorhynchoids”) are small predators of small animals. Pterodactyloids evolved in Middle Jurassic: possessed combined nostril + antorbital fenestra (termed nasoantorbital fenestra or NAOF). Evolve giant size (wingspans of c 10 m) and several lineages evolve toothlessness. Pterodactyloids dominate Cretaceous: include oceanic, fish-eang ornithocheiroids, strongly terrestrial dsungaripteroids and azhdarchoids. Only ornithocheiroids and azhdarchoids persist to very end of Late Cretaceous. Non-pterodactyloids (= ‘rhamphorhynchoids’) mostly Triassic and Jurassic, but some lineages persisted into Cretaceous. Generally small (wingspans less than 1 m), generally long-tailed. Short metacarpus, long 5th toes. Curved claws suggest good at climbing. Short hindlimbs. Probably poor terrestrial abilies.

Anurognathids: ny size, wide mouths, flexible interphalangeal joints in wing finger ds: long, deep skulls, anterior Unusual in being short-tailed. fang-like teeth. Late Triassic - Early Jurassic. Several Triassic pterosaur taxa (grouped together in Campylognathoididae) are strong heterodont. They have conical anterior teeth suited for grabbing mnd mulcusped posterior teeth suited for slicing or cung. Oen extensive tooth wear.

Raecodactylus Upper Triassic, Switzerland. Deep anterior part of mandible, massive nasal horn.

Best known form: from Italy.

Austriadactylus, Late Triassic Austria

Eudimorphodon cheek tooth

Austriadactylus teeth from (A) premaxilla, (C-D) maxilla & (D-E) posterior part of lower jaw Rhamphorhynchids include taxa with slender jaws and slim, anteriorly poinng teeth (like Rhamphorhynchus) as well as taxa with deeper jaws and vercally implanted teeth (like ).

Rhamphorhynchus-like teeth look good for grabbing fish: this confirmed by stomach contents.

But what were scaphognathines doing? Darwinopterus: an evoluonary intermediate between rhamphorhynchids and pterodactyloids? Long tail, long 5th toe, short metacarpus (like a rhamphorhynchid), but long neck, confluent NAOF like a pterodactyloid. non-pterodactyloid

Darwinopterus

Modular evoluon in the origins of pterodactyloids? Darwinopterus suggests that the evoluonary transion from non- pterodactyloids to pterodactyloids occurred in ‘modular’ form (with different parts of the body evolved at different rates). pterodactyloid

Skull and neck module seemingly Lü, J., Unwin, D. M., Jin, X., Liu, Y. & Ji, Q. 2009. Evidence for became of pterodactyloid modular evoluon in a long-tailed pterosaur with a character before the rest of the pterodactyloid skull. Proceedings of the Royal Society B 277, body did. Why? 383-389. Pterodactyloids Evolved during Middle Jurassic from Darwinopterus-like ancestor. NAOF, long & slender pteroid, substanally elongate metacarpal IV, short tail, pedal digit V strongly reduced or absent. Ornithocheiroids Toothed and toothless, long-jawed pterodactyloids, some with long, fang-like array of teeth at jaw ps probably used for grabbing prey from water. Very small, weakly muscled hindlegs and feet. Strongly specialised for soaring; members of several lineages (ds, nyctosaurids) wholly marine. Pteranodon (and kin): best known ornithocheiroids. Long, gently upcurved, toothless jaws, variable cranial crest. Preserved in Upper Cretaceous marine deposits of American seaway. Marine animals, albatross or frigatebird-like lifestyle. Giant, antler-like crests in Nyctosaurus Suggested by some experts to have formed a windsail-like structure that provided some sort of aerodynamic advantage… Giant, antler-like crests in Nyctosaurus Suggested by some experts to have formed a windsail-like structure that provided some sort of aerodynamic advantage…

… but this idea is problemac. Actual shape of bony crest not ‘windsail-like’ at all (it has long posterior spar), bone texture not right for the support of so- ssue membrane, and aerodynamics unlikely to work anyway. Why all the crazy head-crests? Bony crests at the jaw ps, above the snout, and on the braincase were common in pterosaurs… ornithocheirid ornithocheiroid

tapejarid thalassodromid azhdarchoid azhdarchoid

nyctosaurid ornithocheiroid

dsungaripterid dsungaripteroid pteranodond ornithocheiroid

Exceponally preserved specimens show that so-ssue extensions grew on top of some of these bony crests and made them much larger. And some kinds without bony crests (e.g., Pterodactylus) had so- ssue crests that we wouldn’t know about were it not for exceponal so-ssue preservaon. Male Darwinopterus Big cranial crest (also fused pelvis).

Female Darwinopterus No cranial crest (also flexible pelvis)… and egg.

Darwinopterus: females are uncrested, males are crested. So, sexual dimorphism in crest form is present in some pterosaurs. But in others, both sexes similarly crested: evidence for mutual sexual selecon? Ctenochasmatoids: long-jawed waders Pterodactyloid clade with rotated occipital region, oen numerous teeth used in capture of small aquac prey. with c.1000 bristle-like teeth for suspension-feeding Pterodactylus

Pterodaustro

Gnathosaurus

Ctenochasma Azhdarchoids Short-skulls and long-skulled, toothless pterodactyloids, oen found in terrestrial sengs. Proporonally short wing-fingers, long or very long neck vertebrae.

Dsungaripteroids tapejarid azhdarchoid Early Cretaceous forms look specialised for durophagy (= shell-crushing), with upturned jaw ps, stout teeth fused to jaw bones. Stout limb bones suggesng strong terrestrial adaptaon. azhdarchid azhdarchoid Azhdarchid azhdarchoids: largest flying animals of all me Largest forms () have wingspans 10-11 m. Skull along c. 2.5-3 m. Wing shape suggests Giraffa stac soaring, though occasional flapping 3 m at shoulder Quetzalcoatlus permied. Despite highly pneumac Mass 2000 kg 2.5 m at shoulder skeleton, sll heavy (partly due to massive Esmated mass 250 kg muscles). Mass 250 kg…. or more?

Long, toothless jaws, long, fairly sff, straight neck, proficient terrestrial abilies (demonstrated by tracks)…

… what did these pterosaurs do for a living? Azhdarchids have been imagined as shorebird-like probers, as vulture-like scavengers, as marine ‘mega- skimmers’…. Numerous pterosaurs have been interpreted as Mesozoic analogues of skimmers, but this ignores the numerous specialisaons skimmers have for their lifestyle. ….. as marine ‘dip-feeders’, as analogues of stabbling herons, as grabbing storks…

Dip-feeding frigatebird ….. as marine ‘dip-feeders’, as analogues of stabbling herons, as grabbing storks…

Dip-feeding frigatebird

Ground hornbill

Numerous lines of evidence show that azhdarchids were ‘terrestrial stalkers’, like ground hornbills Short, broad wings suited for stac soaring, elongate forearms and hindlimbs, small, well-padded feet and narrow, parasagial gait indicate that azhdarchids were animals of terrestrial environments, well adapted for quadrupedal terrestrial locomoon.

Wion, M. P. & Naish, D. 2008. A reappraisal of azhdarchid pterosaur funconal morphology and paleoecology. PLoS ONE 3(5): e2271. doi:10.1371/journal.pone. 0002271 How did pterosaurs take off? ‘Over-designed’ forelimb bones and evidence for massive pectoral musculature indicates that pterosaurs were quadrupedal launchers that pushed off from the ground in a vaulng leap....

Pterosaurs were thus very different from birds, virtually all of which are hindlimb launchers. Could launch in limited spaces (no run-up needed), and even from water. How did pterosaurs take off? ‘Over-designed’ forelimb bones and evidence for massive pectoral musculature indicates that pterosaurs were quadrupedal launchers that pushed off from the ground in a vaulng leap....

Pterosaurs were thus very different from birds, virtually all of which are hindlimb launchers. Could launch in limited spaces (no run-up needed), and even from water. Could this unique technique have any praccal applicaon? “The concept we have in mind resembles a suit more than a plane - as Mike put it on Twier, "think Batman x Iron Man" - alluding to concepts of the cra being controlled by a person strapped within the chassis, sort of like wearing a mul-million dollar pterosaur costume.” – Mark Wion, 2014

rendering by Mark Wion We’ve looked at… -- pterosaur anatomy & anatomical diversity -- the controversy over pterosaur affinies -- pterosaur history, the difference between pterodactyloids and non-pterodactyloids -- pterosaur diversity as goes lifestyles & feeding behaviours