And I, for one, welcome our new wukongopterid pterosaur overlords (to Europe)

Upper Jurassic pterosaur Cuspicephalus scarfi, a species of some uncertain affinity, now confidently restored as a wukongopterid. How come? Read on. If you'd like a print of this image, please head to my print store.

One of the most significant pterosaur discoveries of recent years are the wukongopterids: small, upper Jurassic pterosaurs unknown before 2009 and most familiar in popular circles for Darwinopterus modularis. These pterosaurs are renowned for providing a morphological bridge between the two major stages of pterosaur evolution: the loose group of long-tailed species which dominated the Triassic and Jurassic phases of pterosaur history, and the Pterodactyloidea, short-tailed, large-skulled creatures which represent a second, better known phase of pterosaur evolution.

The manner in which wukongopterids link these groups will be familiar to many. Instead of showing a mosaic of basal and derived characteristics as expected from any species slotting into a evolutionary 'gap', their heads and necks developed a anatomies like those of pterodactyloids while their bodies and limbs retained features typical of earlier pterosaurs (Lü et al. 2010). Wukongopteridae is generally considered the sister taxon to the Pterodactlyoidea, the two forming the clade Monofenestrata after their shared attribute of combined nasal and antorbital openings. To date, all wukongopterids have been recovered from the Middle/Late Jurassic Tiaojishan Formation of China and, thanks to many complete specimens, their anatomy is already quite well known. The number of valid wukongopterid species remains uncertain: at least seven have been named, but some authors suggest these are oversplit to such an extent that they should all be synonymised into one species, D. modularis (Lü et al. 2012). This is yet to be investigated in detail but, if correct, note that wukongopterid posterboy D. modularis does not have nomenclatural priority. At least one other wukongopterid species was named a few months before D. modularis; two were if you take the 2010 paper version of the description as the ‘true’ publication date of D. modularis, not the 2009 online release.

Wukongopterids are not the only pterosaurs shedding light on the origins of the Pterodactyloidea. The recent discovery of another obviously ‘transitional’ taxon, the Late Jurassic, Solnhofen ‘Painten pro-pterodactyloid’ (Tischlinger and Frey 2014), seems to present a step towards pterodactyloid anatomy from that presented by wukongopterids. The only known specimen of this animal, which is privately owned and thus remains nameless, also shows some modularity of evolution with the body and limbs retaining hallmarks of earlier pterosaur evolution, while the skull has developed into something very similar to Jurassic ctenochasmatoids, especially Pterodactylus antiquus.

Monofenestratan pterosaur skulls. A, the wukongopterid Darwinopterus robustodens; B, likely pterodactyloid sister-taxon the ‘Painten Pro-pterodactyloid’; C, ctenochasmatoid Pterodactylus antiquus; D, azhdarchoid Tupuxuara leonardii; E, early dsungaripteroid Germanodactylus rhamphastinus; F, ornithocheiroid Ornithocheirus mesembrinus; G, early dsungaripteroid Germanodactylus cristatus. Scale bars represent 10 mm, except for D and F, which represent 100 mm. Note that neither A or B are pterodactyloids (the rest are), despite the similar skull shapes. Can we identify their skulls as non-pterodactyloidian without the help of postcranial anatomy? From Witton et al. 2015.

A crucial question concerning these new monofenestratan pterosaurs is how we recognise them without evidence of their combined ‘early pterosaur’ bodies and ‘pterodactyloid’ heads and necks. All current diagnoses of these pterosaurs rely on this combination of characteristics and, by necessity, need relatively complete specimens for identification. What can be done with fragmentary specimens, the likes of which comprise most pterosaur fossils? At least two teams of authors have suggested that limb proportions of non-pterodactyloid monofenestratans are characteristic so, as long as sufficient limb material is known, their isolated bodies have some chance of being identified. But what about their strikingly pterodactyloid-like skulls? In isolation, these bear so much resemblance to those of Jurassic pterodactyloids like Germanodactylus and Pterodactylus (above) that referral outside of Pterodactyloidea is unlikely without an associated, 'early-grade' body.

This is an issue my University of Portsmouth colleagues David Martill, Michael O’Sullivan and I tackled in a new (open access) paper, published today in Contributions to Zoology (Witton et al. 2015). Our interest in this problem is not purely theoretical, this paper picking up questions set down three years ago in the description of Cuspicephalus scarfi, a poorly-known British Jurassic monofenestratan (Martill and Etches 2012). Represented only from a partial skull (below) sharing similarities with both wukongopterids and the pterodactyloid Germanodactylus, Cuspicephalus remained of uncertain affinity when first described (Martill and Etches 2012 – an overview of this paper can be found at Dave Hone’s Archosaur Musings). In the same publication, Martill and Etches remarked that another European Jurassic pterosaur only known from cranial material (jaw tips), Normannognathus wellnhoferi (below), suffered similar problems to Cuspicephalus, its once sensible pterodactyloid identification (Buffetaut et al. 1998) now being questionable with wukongopterids on the scene. Taking the Martill and Etches study as our cue, we decided to take a closer look at the characteristics of non-pterodactyloid monofenestratan crania, and apply our findings to these two poorly-known European pterosaurs.

Jurassic pterosaur fossils aren't all complete skeletons and preserved soft-tissues - most of them look like this. A, MJML K1918, holotype skull of the long-snouted pterosaur Cuspicephalus scarfi Martill and Etches, 2013; B, MGCL 59’583, holotype of Normannognathus wellnhoferi Buffetaut et al., 1998. Scale bars represent 50 mm (A) and 10 mm (B). From Witton et al. 2015. 

I don’t want to rehash our anatomical comparisons in full here – the paper is free for all to read, so you can easily find these details there – but we concluded that yes, wukongopterid skulls are identifiable in isolation - we don't need associated postcrania to identify them. Their skulls are quite generalised in construction and best diagnosed by a combination of 16 character states relating to skull shape, features of the orbit, dentition and cranial crest anatomy, but we also found one character more-or-less unique to the group: an atypically long nasoantorbital fenestra. In exceeding 50% of the jaw length, only two derived Cretaceous pterodactyloid clades (istiodactylids and azhdarchoids) can boast longer nasoantorbital openings than wukongopterids. We also found that the ‘Painten pro-pterodactyloid’ also has its own take on monofenestratan cranial anatomy: like wukongopterids, it is best distinguished via a combination of features, but details of its dentition provide genuine apomorphies.

When applying these findings to our poorly-represented European specimens, we found virtually all evaluable features of Cuspicephalus (13 of 16) matched those of the wukongopterid character complex, it even bearing that especially long nasoantorbital fenestra. By contrast, it differs from the ‘Painten pro-pterodactyloid’ and ‘generic’-looking pterodactyloids such as Germanodactylus quite markedly. I’m happy that, as part of our means of demonstrating this, we managed to get some new details of Germanodactylus cristatus anatomy into the literature. There are specimens of this animal showing really big exoccipital processes (flaring projections anchoring neck muscles at the back of the skull - see illustration, above), but they remain relatively poorly documented. These processes not only have bearings on distinguishing Germanodactylus from Cuspicephalus, but might help resolve disputes about the placement of Germanodactylus among Pterodactyloidea (the relationships of this animal are controversial, but big exoccipitals are only known in dsungaripterid pterosaurs, one of the suggested phylogenetic homes of this taxon). The only feature really distinguishing Cuspicephalus from wukongopterids are some minor details of its anterior tooth placement, which we see as relatively little concern given strong similarities elsewhere and propensity for dental variation among even closely related pterosaurs. We conclude that the close relationship between Cuspicephalus and Darwinopterus suggested by Martill and Etches (2012) is likely, and go further in suggesting Cuspicephalus is a member of Wukongopteridae itself - the first to occur outside of China.

The picture is not so straightforward for Normannognathus however. Most of the characters once used to suggest Normannognathus was related to certain pterodactyloids are now realised as features seen across Monofenestrata, and, in being represented by only jaw tips and one tooth, there's not much to compare with other pterosaurs. A suite of features seen in Normannognathus (including crest height, upturned jaws, dental characteristics and midline jaw grooves) are found in ctenochasmatoid pterodactyloids, and we tentatively suggest it might have some link to this group. However, without more data, it’s hard to be certain exactly where in Monofenestrata this species belongs. Admitting defeat with Normannognathus suggests that our abilities to distinguish types of monofenestratan skulls remain a little limited, even after dedicated study – anything less than a near-complete skull (like the Cuspicepahlus holotype) might prove a challenge to identify.

Cuspicephalus was a relative giant compared to other wukongopterids: that's the second biggest wukongopterid (D. robustodens) on the left. Still, they're not enormous animals overall, as demonstrated by the use of a European robin (Erithacus rubecula) for scale. From Witton et al. 2015.

Are there any bigger-picture implications to our paper beyond taxonomy? Accepting that this is not a 'game changing' paper, we've at least started adding depth to our understanding of wukongopterid pterosaurs, which I’m happy about. Because these animals were previously only known from a very restricted pocket of space and time (Callovian/Oxfordian strata of China), their identification in Europe allows us to start appreciating the geographic and temporal range this group. Cuspicepahlus occurs in late-Kimmeridgian stage rocks, inferring that wukongopterids enjoyed at least 5-10 million years of evolutionary history, spread across Jurassic Laurasia.

Moreover, Cuspicephalus gives us an insight into the disparity of wukongopterids. It is the first wukongopterid with really obvious morphological distinction to previously known Chinese species, which are distinguished by such minor details that, as noted above, their taxonomy has been questioned. Cuspicephalus possesses a much longer, lower skull than any Chinese wukongopterid, as well as packing in more teeth at the anterior end of its jaws. It’s difficult to say what that means functionally, although we speculate that greater jaw reach and ability to handle small, slippery prey might be related to these features. Cuspicephalus is also considerably larger than its relatives in China, its skull exceeding 300 mm in length to make it one of the biggest Jurassic pterosaur skulls known. Interestingly, this does not translate into a particularly large animal overall: the heads of wukongopterids are proportionally large, and our wingspan estimate for Cuspicephalus (based on skull/wingspan ratios in other wukongopterids) is a relatively modest 1.2 m. The largest Jurassic pterosaurs span well over 2 m, so it remains moderately sized at best. However, its wingspan is still a lot larger than any other known wukongopterid however, which can be measured as spanning no more than 884 mm.

We're not quite done with Jurassic pterosaurs here yet: several on-going projects on the functionality of these pterosaurs, some of which are in the publication system, should be emerging in a few months. Hopefully, we won't be waiting long for them...

References

• Lü, J., Unwin, D. M., Jin, X., Liu, Y., & Ji, Q. (2010). Evidence for modular evolution in a long-tailed pterosaur with a pterodactyloid skull. Proceedings of the Royal Society B: Biological Sciences, 277: 383–389.
• Lü, J. C., Unwin, D. M., Zhao, B., Gao, C., & Shen, C. (2012). A new rhamphorhynchid (Pterosauria: Rhamphorhynchidae) from the Middle/Upper Jurassic of Qinglong, Hebei Province, China. Zootaxa, 3158, 1-19.
• Martill, D. M., & Etches, S. (2012). A new monofenestratan pterosaur from the Kimmeridge Clay Formation (Kimmeridgian, Upper Jurassic) of Dorset, England. Acta Palaeontologica Polonica, 58(2), 285-294.
• Tischlinger, H. & Frey, E. 2014. Ein neuer Pterosaurier mit Mosaikmerkmalen basaler und pterodactyoider Pterosaurier aus dem Ober-Kimmeridgium von Painen (Oberpfalz, Deutschland) [A new pterosaur with moasic characters of basal and pterodactyloid Pterosauria from the Upper Kimmeridgian of Painten (Upper Palatinate, Germany)]. Archaeopteryx 31, 1-13.
• Witton, M. P., O’Sullivan M., & Martill, D. M. 2015. The relationships of Cuspicephalus scarfi Martill and Etches, 2013 and Normannognathus wellnhoferi Buffetaut et al., 1998 to other monofenestratan pterosaurs. Contributions to Zoology, 84(2), 115-127.

Darwinopterus vs. Bat Out of Hell

Darwinopterus robustodens and his pal, a European robin (Erithacus rubecula). When not posing for artwork, they drive around in a van solving mysteries.

Wukongopterid pterosaurs have been on my mind this week thanks to a near-complete manuscript about them. This required* rendering everyone's favourite wukongopterid Darwinopterus - results above (note that this is D. robustodens, not the more familiar modularis). In the final version he's joined by something else, but you'll have to wait to just what that is. Wukongopteridae is the group of recently discovered Chinese pterosaurs which bridge early pterosaur and pterodactyloid-grades of pterosaur morphology, famously combining head and neck characteristics of the latter with the bodies of the former. They're best known for Darwinopterus modularis, but there's actually now nine(!) taxa known from the same horizon in north-east China, all morphologically very similar and almost certainly oversplit.

*By 'required', what I really mean is that I'm compelled to construct papers with extraneous artwork in them somewhere, because I'm a sucker for punishment.

Illustrations of Darwinopterus and I go way back. I was asked to do press images for two early publications on it: the initial description and assessment of its unusually 'modular' evolution (Lü et al., 2010), and the equally fantastic discovery of its sexual dimorphism and an egg-mother association (Lü et al., 2011a). Below is the first of these images, published in 2009.

Ah, 2009. Shrink wrapping, relatively light integuments and very low soft-tissue crests were still in fashion. Fun fact: Darwinopterus was referred to as 'Frank' before it was given a binomial, a nod to it being a Frankenstein's Creature-like mash of body parts.

Looking back on Darwinopterus 2009, I'm not enormously happy with it. This in itself isn't that unusual. Artists often look back with dissatisfaction with older works, but this has an additional reason for dissatisfaction: I never really agreed with the notion of Darwinopterus as an aerial-hawker of flying tetrapods, and I think this comes across in its execution. I outlined my basic concerns with this idea in Pterosaurs (Witton 2013):

Given that wukongopterids have provided an insight into macroevolutionary processes, filled a gap in pterosaur phylogeny, and present a very unique pterosaur bauplan, expectations may be high that their proposed foraging strategies will also be rather amazing. Fittingly, some have proposed that wukongopterids were pterosaur top guns, their newly evolved long necks and oversize heads being used to prey upon dinosaurs, other pterosaurs, and even gliding mammals in midair (Lü et al. 2010). Such acts would be rather remarkable because, with even a generous mass estimate, the biggest Tiaojishan wukongopterids would not weigh much over 300 g (extrapolating data from Witton 2008), which is about the same as a modern feral pigeon.

At that size, tackling squirrel- sized mammals or crow-sized dinosaurs on the wing would be a feat earning praise from even the hardiest modern raptors, and wukongopterid skeletons would have to be brimming with offensive weaponry for this purpose. Vertebrate-hawking birds are renowned for their talons, incredibly strong feet, robust skulls, and powerful beaks (e.g., Hertel 1995; Fowler et al. 2009), while bats that subdue large vertebrates in flight are also armed with formidable teeth and powerful jaws (Ibáñez et al. 2001). These adaptations provide the means to immobilize their prey quickly and efficiently, and are obvious advantages for animals grappling with large prey while in “flight. Vertebrate hawkers are also powerful fliers that can chase down their quarry and, once immobilized, carry the prey to a safe spot to eat. Pterosaurian equivalents would therefore require equally powerful “flight musculature to permit the same tasks. Unfortunately for the Darwinopterus raptor hypothesis, wukongopterids do not possess any of these requirements. None of their appendages bear the chunky digits and talons ideal for subduing large aerial prey items, and their long, comparatively delicate skulls and unimpressive teeth are ill suited to this task. Nor, for that matter, do they have the expanded shoulder regions indicative of the powerful “flight muscles needed to chase and eventually carry their prey. With this in mind, raptorial pursuits look doubtful for wukongopterids.

Witton (2013), p. 141-142.

There's a lot more that could have been said about this, but you get the idea: Darwinopterus and chums were small (jackdaw-sized - see image at the top of the post), delicately built animals for which aerial predation seems counter-intuitive and unlikely. I'm not the only person saying this, either: Lü et al. (2011b) and Sullivan et al. (2014) also raise points against the aerial hawking idea. We could go so far as to to label wukongopterid aerial hawking as another example of an 'extreme' palaeoecology based on cherry picked characteristics rather than considering a full suite of functional data.

So, on reflection, we probably started on the wrong foot but, hey, what can you do? Working as an artist is quite different to being involved in research: ultimately, you're a guy with a paintbrush being told to illustrate someone else's idea, even if you don't necessarily agree with it (also see Csotonyi and White 2014). With the notion of aerial predation being raised in the paper, specifically as a possible explanation for the development of pterodactyloid head and neck features Lü et al. (2010), it was an obvious choice for the image. But we didn't help matters by walking into some of the cheesiest, silliest things stereotypes of palaeoart, primarily because we were trying to make a small, fairly inoffensive animal look like a skydiving, dinosaur-eating-badass. We tried several different takes on this, varying aerial and terrestrial prey, and compositions which upped the voracity, such as this:

You'll need to make your own whooshing jet fighter noises and 'pew pew' laser sounds.

Eventually death-from-above was decided over death from sideways. But a key issue to tackle was that that the proposed prey for Darwinopterus was the same size as the predator itself (Sullivan et al. 2014 go into this more), and it's obvious that Darwinopterus is not a fighting, wrestling creature. To make the image work at all we had to play liberally with animal sizes: the maniraptoran (loosely based on Anchiornis in the final version) is tiny, and the Darwinopterus is a huge, ferocious juggernaut. I'm not the only artist who used this trick: the disappointing pterosaur documentary Flying Monsters 3D also had their Darwinopterus plundering undersized theropods. After we tinkered with reality, we then started piling on the cheese: the maniraptoran was made more reptilian-looking, it's head twisted to stare into the Maw of Destiny and, of course, it's mouth open to 'NOOOOOO!!!' it's impending fate. The result is 'Meat Loaf palaeoart', the sort which resembles the worst kind of rock album covers more than nature.

Think I'm being daft comparing palaeoart to cheesy hard rock album covers? How many depictions of extinct animals have the exact same pose as the titular bat here? See links below for more examples. From Wikipedia.

The result isn't awful, but I think I've had more successful collaborations with the same authors, just because this doesn't feel realistic at all. From the science to the composition, the whole thing just seems 'forced'. Don't get me wrong: I'm sure Darwinopterus could be terrifying instruments of mortality to the right prey (probably terrestrial invertebrates according to Lü et al. 2011b and Witton 2013), and I'm not belittling the drama or viciousness which can occur in the lives of small animals. But life - thank God - doesn't look like the cover of a Meat Loaf album. There are some fossil animals that can - just about - pull off Meat Loaf palaeoart, but it's just not possible to turn small, fluffy, unthreatening animals into monsters. When we do, they're more liable to look goofy than impressive. Despite this, we do it all the time. I understand why we do - it's exciting and marketable, and feeds into expectation that Deep Time as a monster-filled fantasy realm - but it also reinforces the perception that palaeoart is unsophisticated and aimed at children. But there may be another way.

Palaeontologists: next time you have a new, diminutive animal you want illustrated, forget the monster: play the cute card. The chubby little Darwinopterus at the top of this post intuitively seems closer to the reality of this animal than Darwinopterus 2009: AwesomeoSuperKiller. It's proportions, fluffiness and posture are all accurate, and it only looks cute because, well, it probably was: it's a small fuzzball with an oversize head and mischievous grin. If the Internet's obsession with cats and baby sloths has taught us anything, it's that cute sells better than violence. Indeed, this image is one of the most popular things I've ever put on Facebook, and (at time of writing) it was posted less than a day ago. The great thing about the cute card is that everyone wins: the artwork should promote research just as well or better than it's Meat Loaf variant, because it appeals to wider demographics. The artist gets to render an animal in a more realistic light without jumping through hoops to monsterise it, and the world gets a new picture to 'coo' at. A few folks might even start to appreciate extinct animals in ways they never could when they're always shown screaming and fighting.

And if nothing else, it will mean we'll never have to discuss Meat Loaf album covers here again.

May God have mercy on us all. (Wikipedia)

References

• Csotonyi, J. & White, S. (2014). The Paleoart of Julius Csotonyi: Dinosaurs, Sabre Tooths and Beyond. Titan Books, London.
• Fowler, D. W., Freedman, E. A., & Scannella, J. B. (2009). Predatory functional morphology in raptors: interdigital variation in talon size is related to prey restraint and immobilisation technique. PloS one, 4(11), e7999.
• Hertel, F. (1995). Ecomorphological indicators of feeding behavior in recent and fossil raptors. Auk, 112(4), 890-903.
• Ibáñez, C., Juste, J., García-Mudarra, J. L., & Agirre-Mendi, P. T. (2001). Bat predation on nocturnally migrating birds. Proceedings of the National Academy of Sciences, 98(17), 9700-9702.
• Lü, J., Unwin, D. M., Jin, X., Liu, Y., & Ji, Q. (2010). Evidence for modular evolution in a long-tailed pterosaur with a pterodactyloid skull. Proceedings of the Royal Society B: Biological Sciences, 277(1680), 383-389.
• Lü, J., Unwin, D. M., Deeming, D. C., Jin, X., Liu, Y., & Ji, Q. (2011a). An egg-adult association, gender, and reproduction in pterosaurs. Science, 331(6015), 321-324.
• Lü, J., Xu, L., Chang, H., & Zhang, X. (2011b). A new darwinopterid pterosaur from the Middle Jurassic of western Liaoning, northeastern China and its ecological implications. Acta Geologica Sinica‐English Edition, 85(3), 507-514.
• Sullivan, C., Wang, Y., Hone, D. W., Wang, Y., Xu, X., & Zhang, F. (2014). The vertebrates of the Jurassic Daohugou Biota of northeastern China. Journal of Vertebrate Paleontology, 34(2), 243-280.
• Witton, M. P. (2008). A new approach to determining pterosaur body mass and its implications for pterosaur flight. Zitteliana, 143-158.
• Witton, M. P. (2013). Pterosaurs: Natural History, Evolution, Anatomy. Princeton University Press.