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Friday, 29 April 2016

The lives and times of flying reptiles as told by the fossil record, part 2: Rhamphorhynchus muensteri

Juvenile, subadult and a big, old adult Rhamphorhynchus muensteri forage in a Jurassic lagoon. We know more about the position of this pterosaur in Mesozoic food webs than any other thanks to its excellent fossil record. The floating posture here is based on data from Hone and Henderson (2014).
The Late Jurassic, Solnhofen Formation pterosaur Rhamphorhynchus muensteri is an exceptional flying reptile. We tend to overlook it a bit now - it's been known for almost two centuries, which is long enough to temper enthusiasm for any fossil species - but it's a remarkable animal for a number of reasons. Far from a typical example of the rhamphorhynchid lineage, it's the rhamphorhynchiest of all pterosaurs with a jaw full of large, conical teeth, elongate extensions to its jaw tips, exceptionally long and slender wings, delicate hindlimbs and walking digits, and a long, stiff tail famously adorned with a diamond or triangular shaped vane*. It also arguably has the best fossil record of any pterosaur. It's known from over 100 specimens, many of them being complete, articulated skeletons with at least some three-dimensionality, as well as providing excellent soft-tissues remains. Excepting embryos, we have complete growth series from tiny juveniles to chunky adults with 1.8 m wingspans, and its preservation is such that fine details of bones can be gleaned through careful mechanical or acid preparation. Its osteology is subsequently better known that any other pterosaur. The Cretaceous pterodactyloid Pteranodon might be known from more fossils (>1400), but these flattened, disarticulated remains are nowhere close to the fossil quality of Rhamphorhynchus.

*We see these restored for numerous long tailed pterosaurs, but only Rhamphorhynchus is known, for fact, to have this 'classic' tail vane morphology.

On top of all this, Rhamphorhynchus also provides greater direct insight into its daily behaviour than any other pterosaur. Multiple examples of gut content, coprolites, predator-prey associations and its inclusion in a ball of vomited spittle provide us with insight into what this pterosaur ate, where it was feeding, and what was eating it. In this, a second and concluding foray into the pterosaur palaeoecological record (click here for the first), let's take a look into how this animal slotted into Jurassic ecosystems.

Snap my fish up

What did Rhamphorhynchus eat? At least three specimens suggest that it foraged for fish of various sizes. The most famous example of such a fossil is sometimes referred to as the 'greedy guts Rhamphorhynchus', an animal which swallowed a fish almost as long as its own torso. This specimen represents a smallish individual, first described by Wellnhofer (1975), with a partly articulated, partly digested fish fossil preserved inside the posterior 60% of the rib cage (below). The orientation of the fish tail fin suggests the fish was swallowed head first, and we have to assume that some major distension of the throat occurred when doing so. That pterosaurs were capable of doing this isn't that surprising considering that extant pterosaur relatives - crocodylians and birds - have mobile throats which aid swallowing of big food items. The relative proportions of these gut contents suggests this animal must've bolted its food like these modern archosaurs, a behaviour rare among mammals but known to occur in at least one large, yellow, bipedal primate. This specimen also presents several elongate elements which defy easy explanation: they're suggested as other food items or even bits of preserved gut tissue by various authors (dark grey in the line drawing below).

The fossil, interpretive drawing, and restored reality of Jurassic table manners. Disgraceful.
Line drawing after Wellnhofer (1975).
Fish dietary remains have been reported from two other Rhamphorhynchus specimens. A complete, relatively small fish has been found in the throat region of one specimen, also swallowed head-first, and various scales and bones occur within the rib cage of another (Frey and Tischlinger 2012; Hone et al. 2013). These three specimens do not represent the limit of Rhamphorhynchus gut content, but they are the limit of identifiable examples: some specimens are known with indeterminate bones or massive, disorganised crystal growths in their stomach regions which represent poorly preserved gut matter, but they aren't of much use to us here.

The one, the only, pterosaur coprolite

Of the many questions that keep pterosaur experts up at night - what are they related to? how did they work as functional organisms? how are they related to each other? - none has been greater than what their poop was like. Expelled waste is a common form of fossils in some localities, but remained entirely elusive for flying reptiles until last year when Dave Hone and colleagues (2015) identified the first pterosaur coprolite dropping out of a complete Rhamphorhynchus specimen. Finally, pterosaur workers can sleep easy.

Rhamphorhynchus muensteri specimen with coprolite (cp). From Hone et al. (2015).
The compact shape of these remains and their proximity to the pelvic region suggest that they were expelled from the pterosaur shortly after it settled on the seabed of the Solnhofen lagoon. Some of the coprolite content is pretty indistinct, but one portion preserves thousands of tiny spines, likely indigestible bits of a recent meal. Exactly what they are is difficult to say - you can get a good look here if you'd like to figure them out - but a number of alternatives were considered by Hone et al. (2015). The tentative, albeit still problematic, suggestion is that they represent cephalopod hooklets. This situation is somewhat frustrating, as this coprolite shows that Rhamphorhynchus was not just a fish eater, but doesn't really tell us much else. Still, now that we know what we're looking for, perhaps more pterosaur coprolites might start coming to light.

Fossilised food chains

Several Rhamphorhynchus specimens reveal it was prey to other Jurassic animals. Among the least commonly discussed is a small pellet produced by something like a fish or crocodylomorph which contains several Rhamphorhynchus wing bones (Schweigert et al. 2001). This is a rare example of Rhamphorhynchus from the Nusplingen Limestone, a unit lithologically similar to Solnhofen but slightly older. As is so often the case with such fossils, the identity of the pellet maker remains elusive. My own suspicions are of a piscine origin, as modern crocodylians don't tend to spit out bones (they digest them, only regurgitating hair, feathers and other keratinous tissues that are difficult to break down). That may not have been true for fossil crocs, of course.

Rhamphorhynchus vs. Aspidorhynchus. I guess we should call this one a draw? From Frey and Tischlinger (2012).

Among the most remarkable Rhamphorhynchus fossils are five instances where it is preserved alongside the predatory fish Aspidorhynchus acutirostris, a long-bodied species that is often much larger than its Rhamphorhynhus prey (Frey and Tischlinger 2012; Weber 2013). These fossils are palaeoecologically notable for three reasons. Firstly, large Solnhofen vertebrates are hardly ever associated, and yet we have five instances of this same pterosaur and fish species being found in touching, or near touching, proximity. Secondly, all five are exquisitely preserved - one example includes a 'mummified' pterosaur with wing membranes, and all are completely articulated. Thirdly, the Rhamphorhynchus are invariably positioned around the skull of the fish, as if a specific, repeated behaviour saw these animals preserved together. These particulars make chance association of these animals unlikely and imply Aspidorhynchus sought out Rhamphorhynchus as food, probably hunting live specimens rather than scavenging floating corpses (as indicated by the excellent preservation of the individual pterosaurs). Frey and Tischlinger (2012) provide a plausible scenario for the deaths of these animals: they reason the Aspidorhynchus tackled prey that became entangled in their jaws before accidentally entering the toxic bottom waters of the Solnhofen waterways. In these anoxic depths the tangled pair would die pretty quickly (if the pterosaur wasn't already dead, of course), leaving us with perfectly preserved bungled predatory acts. The icing on the cake of these specimens is that one of these Rhamphorhynchus specimens has already been mentioned here - that individual with a fish in its throat (Frey and Tischlinger 2012). In this specimen at least, we can assume the pterosaur ate a fish shortly before being attacked itself: a rare instance of a fossil food chain.

The bigger picture of Rhamphorhynchus palaeoecology

Collectively, we have 10 specimens of Rhamphorhynchus telling us something about its position in Mesozoic food webs. That's not bad going for a pterosaur, a famously rare type of fossil, and is actually a pretty good palaeoecological record for any fossil vertebrate. 10 specimens is not enough to tell us everything about the lifestyle of a fossil animal, but does allow us to paint a general picture. They show us that Rhamphorhynchus was adapted to foraging on pelagic prey - often small, probably live fish - and that it must have spent a good amount of time in or around water, as it was clearly an attractant to aquatic predators. These specimens gel neatly with general models of Rhamphorhynchus lifestyle interpreted from their functional anatomy. It's generally thought that Rhamphorhynchus was adapted for life along shorelines - basically a Mesozoic gull. It's not uncommon to be suspicious of such claims nowadays, it being realised that the 'Mesozoic seabird equivalent' almost became a trope, or at least a tremendous over-generalisation, of pre-21st century pterosaur science. But in this case, a gull-like lifestyle is a cogent hypothesis based on studies of wing shape, flight style, tooth and jaw apparatus, and limb function (e.g. Wellnhofer 1975; Hazlehurst and Rayner 1992; Witton 2008, 2015; Ösi 2011). Perhaps research on Rhamphorhynchus was involved in creating the stereotype of pterosaurs as Mesozoic seabirds, but we should not regard it as a victims of this stereotyping itself.

But we should ask ourselves why Rhamphorhynchus palaeoecology is comparably well-represented in the fossil record. It might be something as simple as preservational conditions, but there are plenty of pterosaur Lagerstätten, some of them containing close relatives of Rhamphorhynchus in reasonable abundance, which provide no information about dietary preferences or interactions with predatory species. Is there something intrinsic to Rhamphorhynchus which makes it special? I find several reasons to wonder if Rhamphorhynchus was an atypically aquatic species, not only flying and feeding above water but actually routinely entering it. Firstly, Rhamphorhynchus has a hatchet-shaped deltopectoral crest (the process on the humerus which anchors the flight muscles), a small (or at least narrow) torso and short legs: these are features which Habib and Cunningham (2010) link to routine and efficient aquatic takeoff. Secondly, tests of pterosaur swimming suggest that Rhamphorhynchus had a pretty stable floating posture - not something that can be said for all pterosaurs (Hone and Henderson 2014). Thirdly, it also has comparably large but delicately constructed feet, which might suit paddling, as well as a slender set of forelimb bones (Witton 2015) which recall the streamlined arm bones of swimming and diving birds (Habib and Ruff 2008). Prolonged bouts of swimming might also account for its general abundance, excellent preservation and all-round good fossil record: being immersed in water puts it a step closer to being preserved than other, less aquatic species. Who knows: perhaps it even dived into Solnhofen's toxic bottom waters on occasion, explaining why so many specimens are excellently preserved? Hmmm.... perhaps this warrants further investigation.

Coming soon: could dinosaurs - gasp - lie down on their sides? My take on the greatest of palaeoart debates.

Rhamphorhynchus is supported by fish; this blog is supported by Patreon

The paintings and words featured here are sponsored by the finest human beings on the planet, those folks who support me at Patreon. Backing my blog for as little as $1 a month helps me churn out researched and detailed articles and paintings to accompany them, and in return you get access to bonus blog content: additional commentary, in-progress views and high-resolution artwork, and even free prints. Accompanying this post, we're going to look at the bigger picture of pterosaur palaeoecology: azhdarchids and Rhamphorhynchus are just two lineages with palaeoecological records - what about the rest of Pterosauria? Sign up to Patreon to join that discussion!


  • Frey, E., & Tischlinger, H. (2012). The Late Jurassic pterosaur Rhamphorhynchus, a frequent victim of the ganoid fish Aspidorhynchus?. PloS one, 7(3), e31945.
  • Habib, M. & Cunningham, J. 2010. Capacity for Water Launch in Anhanguera and Quetzalcoatlus. Acta Geoscientica Sinica. 31, 24-25
  • Habib, M. B., & Ruff, C. B. (2008). The effects of locomotion on the structural characteristics of avian limb bones. Zoological Journal of the Linnean Society, 153(3), 601-624.
  • Hazlehurst, G. A., & Rayner, J. M. (1992). Flight characteristics of Triassic and Jurassic Pterosauria: an appraisal based on wing shape. Paleobiology, 18(04), 447-463.
  • Hone, D. W., Habib, M. B., & Lamanna, M. C. (2013). An annotated and illustrated catalogue of Solnhofen (Upper Jurassic, Germany) pterosaur specimens at Carnegie Museum of Natural History. Annals of Carnegie Museum, 82(2), 165-191.
  • Hone, D. W., & Henderson, D. M. (2014). The posture of floating pterosaurs: Ecological implications for inhabiting marine and freshwater habitats. Palaeogeography, Palaeoclimatology, Palaeoecology, 394, 89-98.
  • Hone, D., Henderson, D. M., Therrien, F., & Habib, M. B. (2015). A specimen of Rhamphorhynchus with soft tissue preservation, stomach contents and a putative coprolite. PeerJ, 3, e1191.
  • Ősi, A. (2011). Feeding‐related characters in basal pterosaurs: implications for jaw mechanism, dental function and diet. Lethaia, 44(2), 136-152.
  • Schweigert, G., Dietl, G. & Wild, R. (2001). Miscellanea aus dem Nusplinger Plattenkalk (Ober-Kimmeridgium, Schwäbische Alb) 3. Ein Speiballen mit Flugsaurierresten. Jahresberichte und Mitteilungen des Oberrheinischen Geologischen Vereines, 83, 357-364
  • Weber, F. (2013). Paléoécologie des ptérosaures 3. Les reptiles volants de Solnhofen, Allemagne. Fossiles. 14. 50-59.
  • Wellnhofer, P. 1975. Die Rhamphorhynchoidea (Pterosauria) der Oberjura-Plattenkalke Süddeutschlands. Palaeontoographica A, 149, 1-30.
  • Witton, M. P. (2008). A new approach to determining pterosaur body mass and its implications for pterosaur flight. Zitteliana, 28, 143-159. 
  • Witton, M. P. (2015). Were early pterosaurs inept terrestrial locomotors? PeerJ, 3, e1018.

Monday, 4 April 2016

Why Protoceratops almost certainly wasn't the inspiration for the griffin legend

Protoceratops, the Late Cretaceous horned dinosaur widely suggested as being the inspiration for the griffin myth. This image shows the lesser seen P. hellenikorhinus, a larger, more ornamented species of Protoceratops than the familiar P. andrewsi.
One thing that everyone 'knows' about the mid-sized, Late Cretaceous Asian horned dinosaur Protoceratops is that it's thought to be a fossil with historical mythical significance. Specifically, it's said to be the origin for the griffin, the lion-bodied, bird-headed chimera that has appeared in art and folklore for thousands of years. You could be forgiven for thinking that this idea is quite old and established because it's mentioned frequently in books, TV shows, and online articles, but it's actually a relatively modern invention. What I'll be calling the 'Protoceratops-griffin hypothesis' was first proposed by Adrienne Mayor and Michael Heaney in the 1993 Folklore paper "Griffins and Arimaspeans" and then developed by Mayor across two editions of the book The First Fossil Hunters: Paleontology in Greek and Roman Times (2001, 2011). These authors were not the first to suggest that the griffin had a basis in ancient interpretations of fossil animals (Mayor and Heaney 1993), but they presented the first argument linking griffins to horned dinosaurs as well as a suite of historic evidence supporting their interpretation. The idea has been praised by several palaeontologists and is celebrated as one of the superior accounts of fossils influencing ancient mythology.

Bird-griffin statue, 7th century BCE. Was Protoceratops the inspiration for this creation? From Mayor and Heaney (1993).
The basic premise of the Protoceratops-griffin hypothesis is straightforward. Tales of Ancient Greek explorers of the 7th century BCE (but first written about in the fifth century BCE) include discussion of vicious, beaked, gold-guarding quadrupedal animals living in deserts to the northeast of Greece. These stories are said to have originated with the Scythians, nomadic peoples who mined gold from central Asia from localities close to the bonebeds of Protoceratops in Mongolia and China. It is reasoned that Scythian nomads saw the weathering skeletons of Protoceratops as they prospected for gold and told others of their existence. The Greeks interpreted these as real-life versions of the griffins they knew of from history and the mythology as we know it was born. The hypothesis argues that specific aspects of griffin anatomy were based directly on these accounts of Protoceratops: the beaked jaws and quadrupedality are obvious, but griffin wings are argued to be Protoceratops neck frills or shoulder blades, taloned hands are thought to reflect Protoceratops claws and so on. As the Greeks continued to hear about these animals, eventually from direct trade with the Scythians in the 7th century BCE, their interest in griffins grew so that they became familiar components of Greek culture. For hundreds of years Greek scholars and artists would continue adding to griffin lore, always referencing the same touchstones of desert settings, of powerful, beaked quadrupedal animals, and gold guarding. Their depictions and stories would be passed through to medieval times and, ultimately, the modern day.

I recently became genuinely interested in this interpretation as part of research into the earliest accounts of palaeoart - if griffin art is indeed of horned dinosaur origin, it might qualify as some of the oldest on record. But reading about the Protoceratops-griffin hypothesis (in Mayor and Heaney 1993; Mayer 2011) did not deliver the proverbial 'nugget of truth' behind the griffin myth I expected based on its fame. My impression was that evidence cited for this hypothesis was generalised to account for as much griffin lore as possible, that several major, obvious questions remained unanswered, and that there was not any attempt to refute other, non-fossiliferous takes on griffin origins. Digging into the primary literature on griffin iconography seemed to confirm my concerns, suggesting that the Protoceratops-griffin hypothesis is unfavourable among archaeologists (e.g. Frankfort 1937; Goldman 1960; Wyatt 2009; Tartaron 2014). Moreover, there are far more parsimonious and well substantiated takes on these creatures which do not rely on fossil data. In the interests of providing a counter-argument to all the 'pro'-Protoceratops-griffin hypothesis media out there, I'm sharing the products of my research here.

The griffin timeline

Perhaps the largest issue with the Protoceratops-griffin hypothesis is the fact it largely ignores griffin lore before the 7th century BCE. Griffin iconography extends deep into human history with one of their best early appearances dating to 4th millennium BCE Susa - an ancient city in what is now Iran (below, Frankfort 1937). Similarly aged or older artefacts from Egypt also show griffin-like forms (Wyatt 2009), and by the 3rd millennium BCE griffins were a regular component of art in many Near Eastern countries. The role of griffins in these communities remains a matter of controversy because we have little or no written explanation of their significance. Nevertheless, they are abundant enough to suggest some importance in these cultures, and modern scholars have attempted to interpret griffin imagery based on religious and cultural practises of these times (e.g. Wyatt 2009).

Line drawing of perhaps the oldest known image of a griffin, from Susa, 4th millennium BCE. From Frankfort (1937).
As noted above, the Protoceratops-griffin hypothesis relies on Greek and central Asian evidence no older than the first century BCE, picking up the griffin story at least 2000 years after it begins in the Near East. How does it account for this older period of griffin history? It's actually quite dismissive. Mayor and Heaney (1993) simply write "...we have no way of knowing what kind of folklore, if any, was attached to these creatures" (p. 41), and a similarly brief discussion is presented by Mayor (2011). What is clearly needed is a link between Protoceratops and the oldest Near Eastern griffin art, especially if these fossils were meant to have directly inspired griffin appearance. To my knowledge, no such link has been presented, and this is a problem: whether we understand them fully or not, these early griffins still provide basic information on where and when griffins entered ancient cultures. Therefore, they must be addressed fully by any attempt to explain griffin origins. As it is, the fact that Near Eastern griffins substantially pre-date any from central Asia is a clear argument against the Protoceratops-griffin hypothesis, and one that really needs an explanation if we're to think this myth has a basis in fossil data.

Taking this point further, overlooking the early history of griffin art also means that the Protoceratops-griffin hypothesis does not engage with current, mainstream interpretations of the spread of griffin culture to Ancient Greece. Griffins are thought to have become popular in Greece during the 'Orientalizing Period', a cultural event occurring around the 7th century BCE when Greek art, technology and literature became heavily influenced by Near Eastern civilizations (Tartaron 2014). Put simply, the uptake of griffins into Greek culture coincides exactly with their sudden interest in the guys who'd been drawing and sculpting griffins for thousands of years. It's easy to understand why this is the preferred explanation for the rise of Grecian interest in griffin imagery. It involves the civilisations known to have depicted these animals before anyone else, fits the dates attributed to Greek and Near Eastern griffin art perfectly, and is easily explained as part of a well-established period of cultural exchange between these peoples. A compelling explanation is needed here to explain why this interpretation is inferior to the far more complex one involving distant peoples, a disjointed chronology and fossil animals found 6000 miles away to the East.

Griffin appearance, variation and the 'need' for exotic fossil anatomy

The Protoceratops-griffin hypothesis also presents a simplified interpretation of griffin iconography. Numerous variants on griffins are found in the ancient world, reflecting differences in anatomy, pose and behaviour. The 'bird-griffin' - the winged lion with an avian head (see images, above and below)- is the type Protoceratops is thought to have inspired, but is just one of many griffin chimeras identified by researchers. Reflecting taxonomy on real animals, the identification of distinctive griffin 'species' varies between researchers, but they are generally thought to include wingless sphinxes (human head on a recumbent lion), bipedally standing winged lions with human heads, winged humans with avian heads, winged lions, long necked 'lion-griffins' (sometimes called 'lion-dragons'), and lions with avian heads, wings and forelimbs (Frankfort 1937; Goldman 1960; Wyatt 2009; Gane 2012). Within these forms are more variation: they may or may not include wings, tails, ears, 'crests' or horns on the snout, manes of hair or feathers, and teeth, as well as differences in neck length, mouth gape and claw size. The animal species used in these chimeras differ too. For instance, there are bird-griffins with eagle, peacock and falcon heads, a variety of big cat species are thought to be used for the body and limbs. Tails may be of either avian or felid identity.

A selection of griffins forms from Goldman (1960). Note variation in tails, faces, neck length and ears.
Both Mayor and Heaney (1993) and Mayor (2011) use different griffin types from a variety of cultures in their argument for the Protoceratops-griffin hypothesis, including wingless forms, lion-griffins/dragons, 'classic' bird griffins, as well as toothed and long necked variants. It's argued that these can be distilled to common elements reminiscent of Protoceratops in size and form despite their (sometimes major) anatomical differences, and that this implies a common origin. Variable interpretation of broken fossils are said to explain some features which differ from genuine Protoceratops anatomy. For instance, the horns and ears of some griffins might reflect misinterpreted broken skulls and neck frills, and wings may also be broken frills or misidentified shoulder blades. Embellishment of stories passed on from distant lands might explain other variations.

However, this homogeneous treatment of griffin imagery is troublesome, for two reasons. Firstly, the disregarding of griffin form shows a somewhat selective approach to evidence gathering, highlighting elements that suit the Protoceratops origin while ignoring those which are problematic. The fact is most griffin artworks do not look like Protoceratops beyond the superficial similarity of being being beaked quadrupeds (see below). Furthermore, griffin art remains differentiated even after Greek and Scythian cultures were known to have been communicative and, in theory, tales of Protoceratops could influence griffin depictions. This homogenising of griffin forms also contradicts modern interpretations of griffin art. Many researchers stress the unique histories, origins and cultural significance of different griffin forms, some authors even directly cautioning about treating these chimeras as interchangeable for fear of obscuring their true meaning and history (e.g. Goldman 1960; Wyatt 2009; Gane 2012). Most scholars simply see griffins as chimeras - creatures invented from components of animals and human individuals for symbolic or literary intent (Wyatt 2009; Gane 2012). As with other chimeras, the difference between griffin types likely reflects efforts to convey information about these creatures or the scenarios they're depicted in. For example, the addition of wings may indicate swiftness or divinity; large, erect ears suggest alertness; claws suggest ferocity and so on. These features were not added randomly to griffin art, and the development of distinctive griffin types can be traced over time (e.g. Goldman 1960). The message from mainstream archaeology seems to be that griffin iconography had complex origins and development within the framework of chimera creation common to ancient cultures, and that generalising their form is probably not the best way to understand them.

Superficial musculature of a lion, illustrated in Goldfinger 2004. The torsos and limbs of detailed griffin art shows the same characteristic muscle groups, specific anatomies and proportions as these cats, suggesting there are not generic quadrupeds but true chimeras of large felids and birds. This can easily be seen in some of the imagery posted below and above.
But is mainstream science correct to interpret the griffin as a traditional chimera of familiar, extant animals, or do we need the exotic, extinct form of a Protoceratops to explain their anatomy? I'm not going to compare this dinosaur with all variants on griffin composition here, but will suggest that the 'classic' bird-griffin clearly does not need Protoceratops. It's obviously composed of an avian head, a lion torso, limbs and tail, with a set of bird wings mounted on the shoulders. There are no especially weird or exotic anatomies that cannot be explained without reference to modern species, and even the oldest renditions of griffins show closely observed details of lion and bird anatomy that make their identification obvious. This is particularly true for the lion elements, where the forefeet often have lion-like thumbs, and large, padded, clawed digits. When griffin tails are not just clumps of feathers, they are long, slender and curve upwards in a very lion-like fashion, and their necks are often adorned with manes. I'm struck at how lion-like the proportions and musculature of the torso and limbs are in most griffin depictions: they are not just generic quadrupeds, but really obviously and specifically referencing big cats (above).

Sketch of a juvenile Protoceratops andrewsi skull, right lateral view.

It should be stressed that much of this contrasts with the anatomy of Protoceratops. I need to be careful that I don't set up a straw man here - after all, it's likely we know far more about Protoceratops than anyone who lived thousands of years ago, and the hypothetical passing of tales about Protoceratops from central Asia to eastern Europe is an incredibly long game of Chinese whispers. However, if the Protoceratops-griffin hypothesis is to be accepted it needs to pass some basic anatomical tests, even if they are very simple. Let's start with the head. Immediately obvious is that there is nothing projecting rearwards from the posterior head region of most griffins, whereas all Protoceratops (even very small juveniles) have some sort of frill extending posterodorsally from the back of the skull (above). The ears and crests of griffins, explained as being the broken frills of Protoceratops fossils, are structures which project upwards from the head, not backwards. If we must give these structures a basis in reality, we can look to the ornamental head feathers of birds for the crests (remember that the heads of some elaborate birds, like peacocks, are used in some griffin art) and any number of common mammal species for the ears. These are surely simpler alternatives than the broken skull bones of dinosaur fossils occurring thousands of miles away. It is often suggested that griffin wings might be mistaken interpretations of the Protoceratops frill, but the wings are clearly set on the shoulders in most reconstructions and behind lion-like neck manes in some imagery. Moreover, as noted above, not all griffins have wings. Protoceratops is also not toothless, its densely packed cheek teeth being obvious in even weathered skulls. The majority of griffin images show a fully toothless beak far more like that of a bird than a ceratopsian dinosaur.
Scott Hartmans's skeletal reconstruction of Protoceratops andrewsi. Borrowed from the excellent Scott Hartman's Skeletal
Protoceratops also does not have lion-like hands or feet, nor any raptorial claws (above). Ceratopsians had relatively stout, blunt claws, and the hands of early taxa like Protoceratops are not especially big. I'm not sure anyone - even folks living thousands of years ago - has ever looked at Protoceratops and been amazed by its powerful limbs or ferocious talons, whereas these are striking characteristics of big cats. Finally, the tail of Protoceratops is proportionally deep, seemingly incapable of significant dorsal curvature, and not at all like that of a lion. So beyond being beaked animals with four legs, there's no striking similarity between Protoceratops and bird-griffins. Once we start considering the variance in griffin art - the long necks, manes, feathers and so forth - even more differences become apparent. In light of this, and the fact that living animal anatomies can easily account for all elements of ancient griffin depictions, there seems no need to invoke Protoceratops as a part of griffin anatomy. The mainstream view of griffins being simple chimeras of living animals has to be considered a far simpler and better supported interpretation of their form.

Written accounts of griffin behaviour, and the development of griffin lore

Even if Protoceratops did not inform the raw appearance of griffins, could it be referenced in written accounts of griffin appearance and behaviour, such as their desert-living, parental care and gold-guarding habits? It's perhaps these accounts which provide the best evidence for the Protoceratops-griffin hypothesis, as it's these which indicate the deserts of central Asia as the griffin's home and their association with gold. It's worth summarising some details of the first griffin accounts here as their nature and propagation is important. Please check out Phillips (1955), Bowra (1956), Mayor and Heaney (1993) and Mayor (2011) for more details.

Much of Greek griffin lore is derived from stories of the Greek poet Aristeas, who travelled through Asia in c. 675 BCE. His adventures and travels are first recorded in texts from 460-450 BCE (Mayor and Heaney 1993) and were so influential that they continued to be referenced well into the Common Era. However, it's worth stressing that these stories are semi-mythical tales of a semi-mythical man: Aristeas was a real chap, but he is described as seeing and doing things which are combinations of real and fantastic phenomena. Scholars still discuss the realities behind the locations, events, creatures, and peoples Aristeas encountered, and even ancient Greek authors, such as Herodotus, did not believe everything Aristeas was said to have seen and done (Phillips 1955, Bowra 1956). Among the earliest accounts of Aristeas' travels is the tragedy Prometheus Bound, a tale involving gods, titans, gorgons and other monsters. Here, griffins and other creatures were suggested to live to the far north-east of Greece in a desolate desert setting where nomadic barbarians (the Scythians) also hunted for gold. Other documents from the fifth century BCE, also influenced by tales of Aristeas, tell of griffins guarding the gold sought by men and other beasts. Griffin burrows were mentioned by Pliny the Elder's Naturalis Historia, written in 77 CE, as well as by Pausanias in 170 CE. These authors, again citing Aristeas, described how griffins were engaged in a constant war with a race of one-eyed men, the Arimaspi (Bowra 1956). Later accounts, penned in 200 CE, provide specifics of griffin anatomy and behaviour. They include the familiar accounts of their far eastern habitation of mountains and deserts, as well as new information: their membranous wings (considered useless for flight), the extent of their feathering, the colouration of different body parts, the fiery look in their eyes, the fact that men cannot best adult individuals but can capture their offspring, their nesting behaviour and parental nature, and how miners prospect for gold at night to avoid upsetting them.

Line drawing of a bird-griffin with offspring from Mayor (2011). The original hammered bronze relief dates to 7th Century BCE, Greece. Note the extremely lion-like torso, including strands of hair dangling from the mane. The original has texturing around the neck to further demonstrate the presence of long, shaggy hair.
These stories are the start of griffin lore as we know it today, as medieval scholars continued these basic elements in their griffin legends and we've maintained them until modern times. But do these stories strengthen the idea that Protoceratops is the 'real' griffin? Again, there are problems. For starters, the major early account of griffins are - at best - semi-mythical stories containing numerous imagined beasts and supernatural phenomena. Why we should consider griffins to have any more basis in reality than the gods, monsters or strange human races also mentioned in these stories? If griffins are based on actual phenomena, do we need to seek rationales for these other creatures, too? Secondly, these texts echo griffin art in providing no anatomical details specifically reminiscent of Protoceratops. Indeed, many of their embellishments (feathers, colours, wing membranes etc.) are clearly not based on anything to do with horned dinosaur fossils. These accounts also blatantly refer to living animals, not fossil (or even simply dead) ones, and their descriptions of griffin wars with one eyed men, the vulnerability of their offspring to human capture and so on fit better with fantastical yarns than accounts of fossil creatures. Mayor (2011) suggests that the some griffin behaviour identified in these texts supports Protoceratops as the griffin source, such as their parenting skills (see image, above). These might marry up nicely with the well-known occurrence of nests and juvenile Protoceratops alongside older individuals, but parental care is easily observable for many animals, including the mammals and birds that comprise the griffin chimera. There is no need to invoke a 'third party' fossil species to explain this behaviour in griffins when thousands of modern species could have provided the same inspiration. This trait is just not specific enough to implicate Protoceratops as being referenced in griffin lore.

Protoceratops localities (red) superimposed onto the map of ancient central Asian trade routes and alluvial gold sites presented in Mayor and Haeney (1993). Note the scale bar, bottom right, which represents 200 miles, and the distance between Protoceratops sites and gold deposits (black stars). Protoceratops locality information from Fastovsky et al. (1997) and Lambert et al. (2001).
What of the gold guarding, behaviour, though? This is a specific trait that cannot be casually dismissed for being common among living animals. Mayor and Heaney (1993) and Mayor (2011) identify a wealth of alluvial gold deposits that may well be the real inspirations of the gold described in griffin tales and found that some ancient trade routes do bisect central Asian Cretaceous dinosaur beds (see map, above). An argument for Scythian people at least seeing Protoceratops is starting to look compelling, but, again, closer scrutiny reveals complications. Mayor and Heaney (1993) and Mayor (2011) show maps with Cretaceous fossil sites right the way across central Asia, giving the impression that Scythian miners and traders would've been falling over fossils wherever they went. But we're not just after any old Cretaceous fossils: we're specifically after Protoceratops. Both species of this dinosaur only occur in a few select localities in the southernmost region of Mongolia and adjacent to the China/Mongolia border (Fastovsky et al. 1997; Lambert et al. 2001). Those ancient trade routes and mining sites need to approach these specific sites if we're to bring Protoceratops into this story. Comparing modern Protoceratops localities with the maps in Mayor and Heaney (1993) and Mayor (2011) shows that these dinosaurs occur several hundred kilometres east from the nearest alluvial gold deposits, and even further away from the most productive regions (above). The identified ancient gold sites are mostly west or southwest of the Altai Mountains, suggesting ancient folks would only encounter Protoceratops fossils if they travelled hundreds of kilometres away from these productive areas, and seemingly towards increasingly unproductive terrain.

This also present a further complication to the Protoceratops-griffin hypothesis: are Protoceratops localities likely to contain gold when they're so far away from the alluvial gold sites? Both Mayor and Heaney (1993) and Mayor (2011) argue that desert storms may have transported nuggets of gold to Protoceratops localities, and that seeing these transported nuggets alongside Protoceratops fossils may account for the gold-guarding element of the griffin mythos. This is something we can test because the geology of Protoceratops sites is well documented and understood. Assuming the same basic meteorological processes occur today as thousands of years ago, we should see evidence of windswept gold in the Protoceratops bonebeds. But as far as I'm aware, no gold has been reported from these sites, either as surface debris or as buried elements. Moreover, although the possibility of wind transportation is not excluded entirely, no gold is mentioned by the palaeontologists with Mongolian field experience interviewed by Mayor and Heaney (1993) or Mayor (2011). All this considered, the evidence for it seems the link between Protoceratops and gold deposits is not as strong as it first seems.

Finally, it's worth noting that the Greek accounts of griffins may no longer be the only texts on these creatures from the first century BCE. Gane (2012) discusses Babylonian and Neo-Assyrian literature which is tentatively thought to describe another take on griffin lore. They provide a very different interpretation of griffins, where they are divine guardians against evil spirits and possibly associated with funerary rites. This sounds little like the idea that they were desert-dwelling, gold-hoarding wild animals, and of course suggests no obvious link to fossil animals of China and Mongolia. The implication here is that the Greek stories are only one set of lore about griffins. They are more familiar to us because of their transition to the post-classical period, but they might not be the only, or even the original interpretation of these creatures. Thus, even if Protoceratops is something to do with the griffin - which is far from clear - it is likely only involved in one component of griffin folklore. This seems to echo points made above about the griffin is a very old and complex concept, and how interpretations of its origins are blurred by multiculturalism.

So... is Protoceratops the basis of the griffin myth?

Before we answer that, here's a quick summary of the main issues outlined here:
  • Near Eastern griffin culture seems to occur thousands of years before we have evidence for it in central Asia, suggesting Protoceratops anatomy could not be referenced in any way by the original griffin artists.
  • Griffin anatomies, in all their variants, are best and entirely explained as chimeras of extant animals. There is no need to invoke any exotic fossil anatomies in their design.
  • Griffin iconography, and perhaps written legends, are sufficiently varied to suggest a complex set of origins and legends for these creatures.
  • Ancient Greek writings seem to lack compelling references to Protoceratops, and aspects of appearance and behaviour they discuss clearly indicate they were not informed by fossilised animals. Several details of these accounts suggest they must be talking about imaginary creatures.
  • Protoceratops fossils are found hundreds of kilometres from ancient Scythian gold mines, undermining the suggestion they might be the source of griffin gold guarding lore. There is no indication that these dinosaur fossils are associated with gold.
With all this said, it seems invoking Protoceratops to the griffin myth is nothing but a complication for griffin origins. Data has to be selected to fit this model and then worked around, rather than with, existing ideas on griffin origins that better account for its history, cultural diversity and spread among ancient peoples. So, in short, no, I can't see any reason to think Protoceratops has anything to do with griffin lore, and entirely understand the mainstream view of it as a chimeric animal cooked up by ancient cultures of the Near East. Interestingly, none of the recent papers on griffin lore and imagery I looked at in preparation for this article mention the Protoceratops-griffin hypothesis, and it's surprisingly challenging to find much mention of it in any peer-reviewed literature. This is despite its 23 year vintage and wide popularity among educators, media outlets and some palaeontologists. it clearly has not been adopted as readily by archaeologists as by those of us interested in dinosaur science. I suspect this idea has found greater mileage among the palaeontologically minded because it presents an interesting and seemingly reasonable story, but that also one that sufficiently straddles disciplines and knowledge bases to discourage further research from people mainly interested in extinct species. Given the lack of commentary on this idea from archaeological quarters, I'm genuinely curious to know what those with this sort of background make of this idea.

This Protoceratops article and painting has origins at Patreon

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  • Bowra, C. M. (1956). A Fragment of the Arimaspea. The Classical Quarterly, 6(1/2), 1-10.
  • Fastovsky, D. E., Badamgarav, D., Ishimoto, H., Watabe, M., & Weishampel, D. B. (1997). The paleoenvironments of Tugrikin-Shireh (Gobi Desert, Mongolia) and aspects of the taphonomy and paleoecology of Protoceratops (Dinosauria: Ornithishichia). Palaios, 59-70.
  • Frankfort, H. (1937). Notes on the Cretan griffin. The Annual of the British School at Athens, 37, 106-122.
  • Gane, C. E. (2012). Composite Beings in Neo-Babylonian Art (Doctoral dissertation, University of California, Berkeley).
  • Goldfinger, E. (2004). Animal Anatomy for Artists: The Elements of Form: The Elements of Form. Oxford University Press, USA.
  • Goldman, B. (1960). The development of the lion-griffin. American Journal of Archaeology, 64(4), 319-328.
  • Lambert, O., Godefroit, P., Li, H., Shang, C. Y., & Dong, Z. M. (2001). A new species of Protoceratops (Dinosauria, Neoceratopsia) from the Late Cretaceous of Inner Mongolia (PR China). Bulletin-Institut royal des sciences naturelles de Belgique. Sciences de la Terre, 71, 5-28.
  • Mayor, A. (2001). The first fossil hunters: paleontology in Greek and Roman times. Princeton University Press. (First edition)
  • Mayor, A. (2011). The first fossil hunters: paleontology in Greek and Roman times. Princeton University Press. (Second edition)
  • Mayor, A., & Heaney, M. (1993). Griffins and Arimaspeans. Folklore, 104(1-2), 40-66.
  • Phillips, E. D. (1955). The legend of Aristeas: fact and fancy in early Greek notions of East Russia, Siberia, and Inner Asia. Artibus Asiae, 18(2), 161-177.
  • Tartaron, T. F. (2014). Cross-Cultural Interaction in the Greek World: Culture Contact Issues and Theories. In Encyclopedia of Global Archaeology (pp. 1804-1821). Springer New York.
  • Wyatt, N. (2009). Grasping the Griffin: Identifying and Characterizing the Griffin in Egyptian and West Semitic Tradition. Journal of Ancient Egyptian Interconnections, 1(1), 29-39.

    Friday, 25 March 2016

    The lives and times of flying reptiles as told by the fossil record, part 1: azhdarchid pterosaurs

    The undignified end to the life of a large (6m wingspan) azhdarchid: being squabbled over by Saurornitholestes and other local ruffians. We know a scene like this must have occurred at least once thanks to an azhdarchid fossil discussed below, and a growing number of specimens are providing similar insights into the place of azhdarchids in Mesozoic food webs.

    Discussions of the lifestyles of fossil animals primarily centre around their functional morphology - the use of comparative anatomy and biomechanical calculations to assess their anatomical suitability to certain habits and behaviours. We use these approaches to deduce their likely diets, locomotory strategies, likely interactions with ancient environments and other organisms, and so on. But despite the widespread and proven utility of these techniques, it's widely regarded that these approaches can only provide probabilities and hypotheses about fossil habits. They allow us to predict, but not necessarily know how ancient animals functioned in their respective ecosystems. For the latter, we rely on fossils to provide us with direct records of animal habits - gut content, evidence of animals attacking and ingesting each other, trace evidence of foraging strategies and so on. For vertebrates, these fossils are very rare - hence our general reliance on functional anatomy - and single examples of palaeoecologically-significant fossils can provide crucial insights into ancient lifestyles and ecosystems.

    As you might expect, such fossils are particularly rare for pterosaurs. Flying reptiles were not prone to fossilisation at the best of times and this - through simple probability - dramatically lowers their chance of forming fossils with palaeoecological significance. As recently as the 1990s some authors lamented the lack of these fossils and tried to ascribe some significance to their rarity. But renewed interest in pterosaur science, an increased rate of discovery of flying reptile remains and greater alertness for details on fossil specimens has seen our sample size of palaeoecologically-significant pterosaur specimens grow considerably in the last few years. These records have been augmented more in some taxa than others so that our record of pterosaur palaeoecology is looking increasingly patchy: some groups now now have a half-dozen or more of these fossils to their names, others have none at all. There's probably no real significance to this other than the habits and anatomy of some pterosaurs being more suited to recording these fossils than others.

    I thought it might be fun to take a look at two pterosaur taxa with increasingly good palaeoecological records. In an upcoming post, we'll look at the really quite excellent palaeoecological data for the Jurassic pterosaur Rhamphorhynchus muensteri, but today I want to discuss the palaeoecology of azhdarchids. That's right: the lifestyles of these sometimes giant, sometimes long necked, always edentulous, and increasingly famous flying reptiles are not only predicted by functional morphology, but can be deduced somewhat from fossils too. Thanks to a number of specimens discovered in recent decades we have an idea what happened to azhdarchids when they died, what sort of animals they must have encountered in day to day life, and maybe even how they foraged.

    Meeting the (teeth of the) neighbours

    The majority of the azhdarchid palaeoecological record pertains to specimens showing which animals ate them, their teeth and puncture marks being left on azhdarchid bones, or else azhdarchid remnants being found in the torsos of other animals as gut content. One of the most famous of these fossils is an incomplete azhdarchid skeleton from the upper Cretaceous Dinosaur Park Formation of Canada. This fossil is noteworthy for not only being one of the most substantial pterosaur fossils from Canada, but also for the tooth gouges and embedded dinosaur tooth found at the distal end of the tibia (Currie and Jacobsen 1995). The tooth belongs to the 2 m long dromaeosaur Saurornitholestes langstoni, and the size and provenance of the gouges indicate they were probably made by the same species, perhaps the same individual. The size discrepancy between the pterosaur and dinosaur here is pretty dramatic. Check out the size of the tibia of the (c. 6 m wingspan) pterosaur compared to the embedded tooth:

    Immature azhdarchid tibia from the Dinosaur Park Formation of Alberta, Canada, with an embedded dromaeosaur tooth (arrowed). Note the size of the pterosaur remains compared to those of the dinosaur. Image by Liz Martin-Silverstone, borrowed from her Twitter account.
    This is not the only known occasion of a dromaeosaur interacting with an azhdarchid. Recently Dave Hone and colleagues (2012) described an articulated Velociraptor mongoliensis specimen from Tugrikin Shireh (Gobi Desert, Mongolia) with fragmentary remains of an azhdarchid pterosaur in its gut (below). That this reflects true gut content, and not just chance association of pterosaur bones with those of a dinosaur, is indicated by the articulation of the specimen and location of the pterosaur remains within an envelope of dorsal ribs. It's presumed that the dinosaur was eating bits of pterosaur bone with meat attached, not just swallowing chunks of bone.

    A Velociraptor mongoliensis chest cavity with pterosaur remains, probably belonging to an azhdarchid, as gut content. Black arrows show pterosaur bone, white arrow indicates a pathological rib. Borrowed from Dave Hone's Archosaur Musings.
    Crocodyliforms are also thought to have consumed azhdarchids. Possible puncture wounds from these reptiles are found on the holotype specimen of the Eurazhdarcho langendorfensis, from the upper Cretaceous Sebeş Formation of Transylvania (Vremir et al. 2013). Round bite marks and crushing are found on the cervical vertebrae (below) and distal metacarpal IV of this specimen. In this instance the azhdarchid was unlikely to have been receiving selective treatment by the local reptile fauna, as crocodyliform biting traces are common to many bones from this formation (Vremir et al. 2013).

    Holotype cervical vertebrae III and IV of Eurazhdarcho langendorfensis, with possible crocodyliform tooth marks outlined and arrowed. From Vremir et al. (2013).

    Azhdarchid bones as an insect hotel?

    A further possible record of azhdarchid consumption pertains to strange oval punctures at the back of a Quetzalcoatlus sp. skull (Kellner and Langston 1996). These may record tooth marks, although there is no obvious indication as to what animal might have made them. A rather different take on them was suggested by Kellner et al. (2010), who noted that insect borings had been found the same Quetzalcoatlus material. Kellner et al. suggest that these borings were described by Kellner and Langston (1996) but, to my knowledge, this suggestion is an error as I can find no mention of insect borings in the 1996 paper. I assume this comment provides a different interpretation of the skull punctures, but it might not. I'd really like to know more about this, as there are as yet no confirmed cases of pterosaur bones being utilised by insects. I wonder if this is a simple mistake, or might pertain to details of as-yet undescribed portions of Quetzalcoatlus anatomy?

    An azhdarchid foraging trace?

    Pterosaur foraging traces are known from a number of Jurassic and Cretaceous tracksites (Lockley and Wright 2003). Most look very similar to those known for birds - paired impressions made in the substrate surfaces by beaks pecking at the ground. Interested parties need only check out the mudflats frequented by wading birds to see analogous traces left by modern fliers. Sometimes we find longer scrapes or gouges made by pterosaur beaks sweeping low across sediments, too. These are sometimes interpreted as tail drags, but it's difficult to envisage sensible scenarios where short-tailed pterodactyloid pterosaurs - those thought to have been creating the pterosaur tracks we know of - randomly sweep their tails across the ground.

    Such a beak scrape might be known preserved alongside a possible azhdarchid track from the Late Cretaceous (Campanian) Cerro del Pueblo Formation of North Mexico (Rodriguez-de la Rosa 2003). This track comprises one well-preserved footprint and a series of handprints, alongside several sharp, linear gouges. Other tracks from this locality - known as the El Pelillal tracksite - include turtles, crocodylomorphs, theropods and mammal-like creatures, and the sedimentary setting is considered a shallow, freshwater environment. When described, these pterosaur prints were considered to represent the generic pterodactyloid trace Pteraichnus (Rodriguez-de la Rosa 2003), but the footprint bears little similarity to the broad, triangular-shaped impressions of this ichnotaxon (below). In my 2013 book I argued that the narrow form, pronounced heel impression and short, blunt toes of this print much more reminiscent of Haenamichnus, a trace thought with good reason to represent the footfalls of azhdarchids (below, Hwang et al. 2002; Witton 2013). The age of the specimen is further indication of an azhdarchid identity, the Campanian being a stage of the Mesozoic where azhdarchids seem to largely dominate pterosaur evolution.
    The El Pelillal pterosaur trace described by Rodriguez-de la Rosa (2003), argued here and elsewhere to represent an azhdarchid trace (Haenamichnus) rather than a generic pterosaur track (Pteraichnus) - see for yourself in the inset. Illustrations after Rodriguez-de la Rosa 2003 and Hwang et al. 2002.
    If this is an azhdarchid track, could the sediment gouges represent marks made by the same animal? The original 2003 description provides little commentary little on these marks, but, to be fair, we only really started discussing pterosaur foraging traces in the early 2000s and prospects of terrestrial foraging were considered poor to non-existent by most workers at that time. Perhaps the concept of pterosaur foraging traces were just not on the radar for many researchers in 2003. In any case, these gauges do look similar to marks thought to record sweeping pterosaur beaks at other track sites (Lockley and Wright 2003), so the El Palillal gouges might indeed represent similar phenomena. If this is the case, this specimen might have some important implications for how we interpret azhdarchid pterosaur habits. Speaking of which...

    What these fossils might indicate about azhdarchid pterosaur palaeobiology

    What we have here is the start of a fossil dataset on azhdarchid palaeoecology, comprising several indications of which animals ate them, possible indications of animals using their remains for shelter, and possible trace evidence of a foraging azhdarchid. The data is currently of a small sample size - only five specimens in total - but already offers several points of interest those wanting to understand azhdarchid habits. 

    Firstly, these occurrences show azhdarchids interacting with animals known to have existed in inland habitats. Several of the involved animals are entirely terrestrial, and the most aquatically adapted species yet known to have accosted an azhdarchid bone is a crocodyliform. Given that the latter group is a primarily freshwater lineage (and, indeed, the crocodyliforms in question lived in a freshwater deposit), this data is not inconsistent with this model. As regular readers may appreciate, an 'inland' palaeoecological signature is consistent with the 'terrestrial stalker' mode of azhdarchid life proposed in by myself and Darren Naish in 2008 (see below, also Witton and Naish 2008, 2015), where we argued that azhdarchids were not aquatic or marine adapted species, but much more at home in woodlands and plains, picking up small game with their oversize beaks. I see these palaeoecologically-relevant fossils as a test of this idea, and am happy to see that - so far - they are consistent with the model we proposed. 

    Azhdarchid terrestrial stalking, the infographic. From Witton and Naish 2015.
    Secondly, if we do indeed have an azhdarchid foraging trace, proposals that azhdarchids can reach the ground with their jaw tips to feed are vindicated. Darren and I initially encountered some resistance to our 2008 'terrestrial stalker' proposal because some peers thought the azhdarchid neck would not permit the jaws to reach the ground. We argued that the jaw is so long that only minimal neck motion, or even just a bit of forelimb flexion, would see the jaws reaching the ground without problem. Azhdarchid beak scrapes would indicate that this was indeed the case and put this minor debate to rest. 

    Thirdly, the terrestrial stalker model might predict the presence of beak scrapes alongside azhdarchid footprints. After all, azhdarchids looking for or striking at prey may sometimes have held their jaw tips close to the ground - modern animals track prey in this fashion, after all. The potential existence of beak marks with the El Pallilal track may be 'smoking gun' evidence of azhdarchids foraging on the ground in the manner proposed in 2008. I stress that the El Pallilal tracks need re-examination to confirm these ideas, but, if I'm correct, these traces augment the 'terrestrial stalker' argument considerably.

    One question I expect will be asked about these fossils will be whether they tell us much about azhdarchid susceptibility to predation. This is something which has been discussed at a technical level (see this blog post for details), but I'm not sure these specimens help us understand it further. My issue is that, although various ideas have been published on the likelihood of certain azhdarchid fossils representing scavenging or predation (mainly involving relative masses of the animals involved), I'm not sure we can account for the many factors behind the circumstances recorded in these remains. Those azhdarchids outlined above were certainly dead, or near death, when being chewed on as their bones show no signs of healing from the inflicted damage, but a number of scenarios could account for this. We know that modern predatory events are influenced by the health of the animals involved, the skills and behaviour of different predatory species and individuals, and circumstances of time and place. These are difficult to account for with those bitten and chewed azhdarchid fossils we currently have, so I prefer to have no opinion on these matters and focus on the significance of things we can say more positively.

    OK, that's all for now. In the next, and concluding part of this series we'll see what the fossil record tells us about the rhamphorhynchiest pterosaur of all, Rhamphorhynchus muensteri

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    • Currie, P. J., & Jacobsen, A. R. (1995). An azhdarchid pterosaur eaten by a velociraptorine theropod. Canadian Journal of Earth Sciences, 32(7), 922-925.
    • Hone, D., Tsuihiji, T., Watabe, M., & Tsogtbaatr, K. (2012). Pterosaurs as a food source for small dromaeosaurs. Palaeogeography, Palaeoclimatology, Palaeoecology, 331, 27-30.
    • Hwang, K. G., Huh, M., Lockley, M. G., Unwin, D. M., & Wright, J. L. (2002). New pterosaur tracks (Pteraichnidae) from the Late Cretaceous Uhangri Formation, southwestern Korea. Geological Magazine, 139(04), 421-435.
    • Kellner, A. W., & Langston Jr, W. (1996). Cranial remains of Quetzalcoatlus (Pterosauria, Azhdarchidae) from Late Cretaceous sediments of Big Bend National Park, Texas. Journal of Vertebrate Paleontology, 16(2), 222-231.
    • Kellner, A. W., Rich, T. H., Costa, F. R., Vickers-Rich, P., Kear, B. P., Walters, M., & Kool, L. (2010). New isolated pterodactyloid bones from the Albian Toolebuc Formation (western Queensland, Australia) with comments on the Australian pterosaur fauna. Alcheringa, 34(3), 219-230.
    • Lockley, M. G., & Wright, J. L. (2003). Pterosaur swim tracks and other ichnological evidence of behaviour and ecology. Geological Society, London, Special Publications, 217(1), 297-313.
    • Rodriguez-de la Rosa, R. A. (2003). Pterosaur tracks from the latest Campanian Cerro del Pueblo Formation of southeastern Coahuila, Mexico. Geological Society, London, Special Publications, 217(1), 275-282.
    • Vremir, M., Kellner, A. W., Naish, D., & Dyke, G. J. (2013). A new azhdarchid pterosaur from the Late Cretaceous of the Transylvanian Basin, Romania: implications for azhdarchid diversity and distribution. PLoS One, 8(1), e54268.
    • Witton, M. P. (2013). Pterosaurs: natural history, evolution, anatomy. Princeton University Press.
    • Witton, M. P., & Naish, D. (2008). A reappraisal of azhdarchid pterosaur functional morphology and paleoecology. PLoS One, 3(5), e2271.
    • Witton, M. P., & Naish, D. (2015). Azhdarchid pterosaurs: water-trawling pelican mimics or “terrestrial stalkers”?. Acta Palaeontologica Polonica, 60(3), 651-660.

    Monday, 14 March 2016

    The magnificent Caviramus, an early example of an anatomically 'extreme' pterosaur

    The Carnian/Norian Swiss pterosaur Caviramus schesaplanensis, one of the earliest species to take pterosaur anatomy to strange new places. Anyone else want to make puns about 'Cave-iramus' with this picture? No? Anyone...?
    What happens when you take the innate weirdness of the Triassic Period - the evolutionary equivalent of the late 1960s in terms of experimentation, weirdness and tragic ends to interesting lineages - and multiply it by a pterosaur? One answer is the marvellously strange Late Triassic flying reptile Caviramus schesaplanensis. This animal is a relative newcomer to the pterosaur roster, first being described in 2006 based on an incomplete lower jaw from Switzerland (Fröbisch and Fröbisch 2006), before better material in the form of an incomplete skeleton turned up a few years later* (Stecher 2008). Several cranial and dental features indicate Caviramus had kinship with other European pterosaurs such as Eudimorphodon and Campylognathoides, but that it was a rather distinctive animal compared to even close relatives. This 1.35 m wingspan animal had a chunky skull, large crests on both upper and lower jaws, densely packed and gnarly teeth, long, slender wings and a robust, lengthy set of hindlimbs (Stecher 2008). Several of these features are 'extreme' variants of pterosaur anatomy common to other Triassic animals, and others represent the most pronounced development of anatomical traits of any pterosaur. They mean that, even a decade after the first remains of this animal were published, Caviramus still gives us a lot to think about as goes its life appearance, lifestyle and functional anatomy.

    *This skeleton was described as the holotype of a new genus and species, Raeticodactylus filisurensis, but a number of recent workers have shown it to be very likely congeneric, if not entirely synonymous, with C. schesaplanensis. I'm treating the two as the same taxon here.

    Fossil material referred to Caviramus. Above, the holotype jaw of Caviramus schesaplanensis, below, the incomplete holotype skeleton of "Raeticodactylus filisurensis", a taxon now considered by most to be Caviramus and perhaps even Caviramus schesaplanensis itself. From Fröbisch and Fröbisch (2006) and Stecher (2008).
    One atypical aspect of Caviramus is the cranial crest. Sure, pterosaur headcrests are really not uncommon (it's perhaps fair to say seems crestless species are more unusual than crested ones) but they remain fairly rare in the Triassic and, even compared to much later pterosaurs, Caviramus is pretty well endowed in the crest department. Rather than the low midline ridge typical of many pterosaur bony crests, this structure projects rudely from the front of the snout to reach well above the rest of the skull. We don't see anything like this again in the pterosaur record until the lower Cretaceous, when the famously elaborate tapejarids adopted a similar configuration. As with these pterosaurs, it's likely a soft-tissue component extended the Caviramus crest tissues in some way. The posterior crest border of the only known Caviramus skull is badly preserved, but the lateral crest surfaces have the same fibrous textures as pterosaurs known to have large soft-tissue crest components, such as Pterodactylus and Tupandactylus. The most parsimonious interpretation of this is that Caviramus had a big soft-tissue crest too, and - if the bony crest portion is indicative of the soft-tissue extent, as seems apparent from some pterosaur fossils - it might have been quite a spectacularly adorned animal. Caviramus seems to represent one of the first experiments with this sort of outlandish headgear, there being only one other Triassic species which could rival it for crest development (Austriadactylus cristatus - see Dalla Vecchia et al. 2002) .

    Multiple aspects of the Caviramus jaw are of interest. It was probably a powerful biter, and perhaps regularly consumed relatively tough prey such as invertebrates with thick exoskeletons or fish with hard scales. Such a diet is indicated by its blunted and worn tooth tips, and the enamel of the anterior teeth being strongly rugose - some readers may recall from a recent article that these features also occur in other specialists of hard prey, such as the giant, turtle-eating Cretaceous crocodylian Deinosuchus. Caviramus dentition is morphologically complicated and, again, indicates some specialisation. As with many Triassic pterosaurs, the teeth are differentiated into large, curving anterior fangs at the jaw tips and complicated, multicusped teeth behind these. These posterior teeth are so numerous and tightly packed that they actually sit obliquely in the jaw, overlapping one another to form a continuous, 'megaserrated' cutting surface. The depression of the jaw joint (another atypical feature for a pterosaur, and one that won't reappear until later in pterosaur evolution) permitted these teeth to occlude simultaneously rather than gradually, as occurs in animals with jaw joints level with the toothrow. Areas of Caviramus jaw muscle attachment are large, including a broadly expanded posterior lower jaw. The mandible and skull are not, as with some pterosaurs, delicately built from slender struts but comprised of deep bars and robust bone junctions. Cross sections of the Caviramus holotype jaw indicate that some cavities were present in the cranial skeleton, but that bone volumes were superior in at least some places. This was clearly an skull capable of delivering and withstanding forceful bites, and its configuration recalls some dinosaur species which are sometimes considered to be omnivorous (e.g. many small ornithischians). Maybe it was equipped with powerful jaws so that it could tackle a wide range of tough foods, including nutritious plant matter.

    Cross section through the posterior (specifically, coronoid) section of the Caviramus holotype jaw. Grey shading represents bone, white indicates hollow regions. From Fröbisch and Fröbisch (2006).
    This strong skull and dental apparatus seems odd compared to the Caviramus humerus. This bone is about as long as expected for a pterosaur of this kind, but is distinctive for being very, very slender. Usually, pterosaur humeri are the most robust elements in the limb skeleton, but that of Caviramus is no wider than the more distal wing elements. So proportionally different is this bone that the shoulder and upper arm were probably much more slender in life than those of other pterosaurs. Quite what this means for Caviramus locomotion has not been looked into yet, and any attempt to assess this will be frustrated by the only known Caviramus humerus being somewhat imperfectly preserved. Still, it's known in enough detail to at least permit some basic comments.

    One obvious question concerns what this humerus means for quadrupedal launch potential in this animal. A core basis to this hypothesis is that pterosaur humeri are much stronger than their femora (Habib 2008) but - going on a basic assessment of bone shape here - this is not obviously the case for Caviramus. We should not automatically default to assuming Caviramus was a bipedal launcher however, as it is small enough to not need atypically strengthened limb elements for launch. The limb bones of volant animals are expected to start showing strong signals of a launch strategy once their body mass hits 2 kg (i.e. it's above this mass where the humerus or femur strength starts to become disproportionately strong compared to the other limb elements - see Habib 2008 for details) but, at only 1.35 metres across the wings, Caviramus probably only massed a little over one kilo. I'm sure Caviramus did have a preference for a particular launch strategy (I'm not aware of any animals which can readily flip between quadrupedal and bipedal launch, except under special circumstances), but its size means we might need dedicated investigation to know which was more likely. Given that all other pterosaurs seem to be quad-launchers, my suggestion is to assume this as the null hypothesis for now until we have reason to assume otherwise.

    Caviramus schesaplanensis skeletal reconstruction, somewhat updated from the original version in Witton (2013). Unknown elements based on Campylognathoides liassicus (see Padian 2008).
    The slenderness of the Caviramus humerus might have impacted flight once airborne, too. Caviramus joins pterosaurs like Eudimorphodon and Campylognathoides in having very long wings, but lacks the stocky, probably powerfully muscled humeri of these species. These might have enabled Eudimorphodon et al. to be forceful fliers capable of rapid flapping, elevated speeds and high agility. But the delicately constructed humerus supporting a long distal wing in Caviramus might have curbed any potential for being a powerful flapper or aerial acrobat - its humerus would have been far more vulnerable to bending than those of other pterosaurs. This is not to say that it was purely restricted to gliding, however. Studies of avian wing construction show that their humeri do not have to be enormously strong to permit flapping flight (indeed, their humeral strength seems to scale more or less isometrically with body size - Witton and Habib 2010) and the fact Caviramus has a large deltopectoral crest to anchor flight musculature is a good indication it was an active flier. We might conclude that its long, slender wing bones were suited to soaring flight with limited flapping - long winged seabirds like gulls, albatross and terns might be a good modern flight analogue.

    Readers familiar with the Caviramus illustration in my 2013 book Pterosaurs: Natural History, Evolution, Anatomy might note that the 2016 Caviramus (above) is rather differently posed. There's good reason for this - read on...
    It's not only flight that this unusual humerus might have impacted: it might have imposed some restrictions for life on the ground. I don't think we should assume it was so slender that it was incapable of supporting the animal - again, we're not dealing with an enormously heavy species here - but its slenderness might have impacted how the limb functioned when grounded. Specifically, the apparent absence of an expanded elbow region suggests it had sprawling forelimbs. As noted above, the Caviramus humerus is a little imperfectly preserved in places, the distal end being the poorest bit, but the proximal ulna confirms that the elbow joint was not broad. Slender elbows have been interpreted as a signature of sprawling forelimbs in some pterosaurs, for two reasons (Witton 2015, also see this blog post). Firstly, they suggest that musculature operating the wrist was fairly reduced (remember that wrist action is controlled by muscles anchored around the elbow - see Fujiwara and Hutchinson 2012). This reflects both the stresses encountered when standing in a sprawling pose and practicalities of terrestrial locomotion. Walking animals need to clear their feet or hands from the ground when moving, and animals with erect limbs have to do this by collapsing limb joints to reduce the effective length of the limb. Sprawling animals can use motion of the upper limb bone (humerus or femur) to elevate the entire limb, and can therefore take steps without needing to collapse the distal joints. Secondly, slender pterosaur elbows seem to correlate with shoulder joints that prevent depression of the humerus below the horizontal, a bony stop at the base of the shoulder precluding adoption of erect forelimb poses in these species. Given what we see in other pterosaurs, then, we might assume Caviramus elbow morphology indicates it had sprawling forelimbs, although we really need better fossil material to verify this. As in all other pterosaurs, details of the femoral morphology indicate that the hindlimbs were likely held erect. The legs are long enough that even with a highly crouched forelimb the animal still looks very 'leggy', and, in spite of its sprawled forelimbs, it might have been a fast, sprightly terrestrial animal. I imagine long-legged, skinny-limbed Caviramus scuttling about the place might give some people the creeps if it were alive today - if there was ever a pterosaur that might indirectly trigger arachnophobia, it's this one.

    Collectively, these points suggest Caviramus represents one of the oldest deviations from what might be considered a 'standard' pterosaur bauplan and perhaps one of the first developments of anatomical 'extremes' in the group, at least as goes skull and wing anatomy. What makes this remarkable is that Caviramus lived so soon after the pterosaurs evolved in the first place - it seems to have wasted no time in pushing the pterosaur skeleton to weird new places. Unfortunately, it's currently difficult to say how successful these experiments were. The Triassic pterosaur record is extremely poor, particularly outside of Europe, and it is difficult to provide any meaningful evaluation of the abundance or longevity of lineages from this period. In a broad sense, however, it might be significant that we don't find Caviramus-like humeri or jaws in the better understood pterosaur faunas of the Jurassic or Cretaceous. Maybe Caviramus represents a configuration that was unsuited to life beyond conditions of the Triassic or, alternatively, perhaps the more 'typical' anatomies of other pterosaurs were just more adaptable in the long run. Whatever the reality here, Caviramus is a good example of how diverse and adaptable pterosaur anatomy can be and how much we have to learn about the early history of this group.

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