What pterosaurs tell us about the evolution of feathers

2011 PR image for the 2014 description of Laquintasaura venezuelae, a basal ornithischian from Venezuela. Scales were the requested integument for this reconstruction, but how does that decision hold up today?

For the last two weeks I've been revising an image of the Jurassic ornithischian Laquintasaura venezuelae. The original (above) was produced in 2011, but a request to include it in an upcoming book was impetus to tidy up the art and update the anatomy. One significant question for updating this old piece was whether the animals should stay scaly or receive a coat of filaments. The systematic placement of Laquintasaura isn't certain, but it seems to lack features allying it to major ornithischian clades and, for now, is simply considered a basal member of Ornithischia (Barrett et al. 2014). This puts it in a controversial spot as goes interpretation of dinosaur integument: scales, filaments, or a mix of both?

The origins on filamentous integuments and feathers in reptiles remains an ongoing source of fascination and investigation for palaeontologists. It has been known that filamentous reptilian integuments extend deep into geological time since the 1800s, but research into these structures exploded in the 1990s and 2000s when fossils of many non-avian theropods - seemingly all coelurosaurs - were found adorned with feathers or filamentous feather precursors. Soon after, recovery of quills, filaments and strange, fibrous scales in ornithischians made a reality of once speculative ideas about filaments being widespread across Dinosauria. For years now, palaeontologists have been discussing the possibility that theropod filaments and feathers share ancestry with those of ornithischians. One implication of this is that bodies of dinosaur ancestors would be covered in fuzz instead of, as traditionally supposed, scales. Unravelling this conundrum is of key interest to those attempting to understand ancient reptile evolution and physiology, as well as for artists wanting to know how to credibly restore early dinosaurs. However, integument preservation, and particularly filamentous hide, is rare in the fossil record. Much as we might want to, we currently have insufficient data about the skin of early dinosaurs to address this issue directly.

All is not lost, however: some insight into dinosaur filament evolution can be provided by pterosaurs. Flying reptiles and dinosaurs are largely thought to form a more or less exclusive clade, the Ornithodira, which we now recognise as being characterised by a suite of anatomies - not just hindlimb features, as originally proposed - and commonalities of interpreted anatomy: postcranial pneumaticity, upright postures, elevated metabolisms, and filamentous integument. It's the latter which makes pterosaurs potentially useful to understanding the ancestral state of dinosaur skin. It's a little surprising that it's taken us so long to capitalise on this data, since we've had conclusive evidence of pterosaur filaments (we call them pycnofibres) since the 1970s (Sharov 1971). Suggestions that pycnofibres may have been homologous to dinosaur fuzz arrived much later, in the 2000s, when the evolutionary depth of dinosaurian filaments had become apparent and new discoveries of fuzzy pterosaur fossils were being reported (Czerkas and Ji 2002; Ji and Yuan 2002). Perhaps it was the coincidence of these events, the realisation that filaments were widespread in Pterosauria, and increased confidence in the sister relationship between dinosaurs and pterosaurs which lead to this idea finally being proposed.

Late Jurassic pterosaur Sordes pilosus, described in 1971, was one of the first pterosaurs confirmed to have a filamentous body covering. But are pterosaur filaments tied to those of dinosaurs, or independently evolved?

Studies into pterosaur and dinosaur filament homology remain thin on the ground, and much of what has been said thus far is reliant on gross filament morphology. Earlier this year, a team of researchers (Barrett et al. 2015) tackled the issue of ornithodiran filament evolution quantitatively, estimating the likelihood of homology between theropod, ornithischian and pterosaur integuments via their distribution on the ornithodiran tree. Using 18 different variations in methods, calculations and data values, they predicted the likelihood of ancestral integument states in dinosaurs and ornithodirans: were they scaly, filamentous, or feathered? The result, announced in not only the paper but also a subsequent media release, was that 12 of those 18 assessments suggested scales were ancestral to ornithodirans, and the filaments seen in pterosaurs, ornithischians and theropods were derived independently from a common scaly ancestor.

This conclusion was undoubtedly surprising to some and, indeed, a clear caveat accompanies it: scaly ancestral dinosaurs are "sensitive to the outgroup condition in pterosaurs". Support for ancestrally-scaly ornithodirans relies on the assumption that pterosaur ancestors were also scaly. This condition assumed for 50% of those 18 assessments to account for uncertain ancestral condition for pterosaur integument. In the 9 analyses where pterosaurs were treated as wholly filamentous - and thus consistent with what we see in existing pterosaur fossils - six returned results indicating an ambiguous scaly/filamentous ancestral condition for ornithodirans and dinosaurs, and only 3 supported a wholly scaly interpretation. Of those six 'ambiguous' results, most reported a strong likelihood of ornithodirans being ancestrally filamentous, and many gave dinosaurs a good chance of being ancestrally filamentous too. Moreover, treating pterosaurs as filamentous has knock-on effects through the dinosaur tree: suddenly, there are reasonable, or at least equivocal, chances that ornithichians and saurischians were also ancestrally filamentous. This is a different conclusion to the straighter story of ornithodirans and dinosaurs simply being ancestrally scaly.

What influence do fuzzy pterosaurs have on dinosaur skin evolution? Seemingly, quite a bit. The tree on the left shows integument likelihoods (pie charts) where pterosaurs are considered scaly, tree on the right shows a filamentous analysis.  Modified from Barrett et al. (2015).

Clearly, the crux of all this is the assumption that pterosaur ancestors were scaly: just how defendable is this? Because we know little about pterosaur origins, it's hard to say anything conclusive about the evolution of pterosaur integument with our current fossil record. The stratigraphically oldest pterosaur fossil with pycnofibres is from Middle/Late Jurassic deposits, and thus about 50-60 million years younger than the oldest pterosaur fossils - little help in determining if the first pterosaurs were fuzzy. Ongoing disagreements over pterosaur phylogeny complicate attempts to estimate the appearance of lineages with confirmed pycnofibres. Some schemes (those derived from Kellner 2003 and Unwin 2003) suggest pycnofibres must have appeared by the Triassic, close to or at the base of pterosaur ancestry, but others (e.g. Andres et al. 2010) indicate pycnofibres reliably extend no further than the Lower Jurassic. Of course, such assessments of filament distribution might not even be meaningful at this stage, given that pycnofibres are very rare components of pterosaur fossils. They are nowhere near as common as other soft-tissues, such as wing membranes, and we should probably be cautious about any assessment of their evolutionary pathways until we have more data. Perhaps the only significant observation we can make from our current, limited dataset is that, to date, no pterosaur is known with a scaly body covering, even when regionalised scalation - foot pads - preserves in their fossils (Frey et al. 2003).

A possible pterosaur relative with scaly hide is known: the Triassic archosaur Scleromochlus taylori. Benton (1999) described structures interpreted as thin, transversely orientated scales across the back of multiple specimens of this animal. This might provide vindication of the scaled pterosaur ancestor model, but, again, there are some caveats with this idea. For one, Scleromochlus fossils are not well preserved. The scales are feint sediment impressions, visible only in strong, low angle light, such that that they are only considered 'probable' integument impressions by Benton (1999). Previous workers have interpreted them in a different way (as gastralia). Clearly, the evidence for them being scales could be more compelling, and there's certainly not much to work with if we want to test their identification. Secondly, exactly how Scleromochlus is related to pterosaurs is not precisely agreed. Some workers consider it the sister taxon of Ornithodira, others as a member of the pterosaur branch, and others see it as more closely related to dinosaurs than pterosaurs. That might seem a minor issue, but we've already seen how sensitive models of ornithodiran integument are to changes of single variables at the base of the tree. We would probably need to run many variants of the integument probability calculations to account for all the uncertainty surrounding Scleromochlus. This might give more idea of the range of possible integuments at the base of ornithodiran evolution, but that's not much of an improvement on our current situation.

Was Scleromochlus taylori scaly? Maybe - weakly preserved structures on several specimens seem to suggest so. On this diagram, from Benton (1999), possible transverse scales can be seen on the left and middle specimen.

In all, I feel like we're hitting a bit of a wall here. It seems we just don't know enough, and have too many caveats with the limited data we have, to make even a half convincing best guess on this. Thus, how much weight we put on models of ornithodiran integument using scaly pterosaurs is almost a philosophical issue. From my end, I don't think they should be used to argue for scaly ornithodiran and dinosaurian ancestors, at least not with the same weight as tests made using a filametnous pterosaur lineage. When reconstructing ancestral states, characters objectively observed in fossils have to trump assumed character states, even if we know that our dataset is full of holes. After all, the whole point of attempting to figure out an ancestral state is establishing links between character data we have, so introducing opposing character states seems a little contrary to that objective. To be clear, I'm not saying that running models with scaly pterosaur ancestors is a waste of time. To the contrary, it's a good test of model robustness, and Barrett et al. (2015) certainly demonstrate how sensitive our models of ornithodiran integument evolution are by using this approach. Their hypothetical scaly pterosaurs demonstrate that we really do need more early ornithodiran fossils to understand ornithodiran skin evolution. However, I do not think that results of the scaled pterosaur analyses are as informative as their other assessments, as we have to overlook existing data to consider them equally valid.

With all that said, do pterosaur fossils really help us understand the evolution of dinosaur filaments? Playing the conservative card here, it seems they do not provide super strong evidence for an all-fuzzy Dinosauria, but they certainly make it difficult to defend ideas of entirely scaly dinosaur ancestors. Forcibly arguing for either scales or filaments at the base of Dinosauria seems premature at this stage, and, whatever our personal hunches are, it seems sensible to accept some ambiguity in this situation for now.

I began this article with my Laquintasaura conumdrum: how did that play out when, apparently, I can't make up my mind about this scales and filaments debate? Well, I've argued elsewhere that palaeoart can do no better than illustrate credible interpretations of the past and that, so long as the hypotheses they depict are sound, they're doing OK. When we have conflicting or ambiguous hypotheses, we just have to make a judgement call based on our own opinions, gut feelings and interpretations of existing arguments. With my own leaning being towards data showing that scales may not be ancestral to ornithodirans, but also knowing that some dinosaurs are mosaics of filaments and scales, I decided to partially enfluffen my Laquintasaura, while leaving their snouts, tails and limbs scaly. I'll leave you with the revised image.

Laquintasaura venezuelae 2015 edition: basically the same picture, but a bit fluffier, and a bit greener.

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References

• Andres, B., Clark, J. M., & Xing, X. (2010). A new rhamphorhynchid pterosaur from the Upper Jurassic of Xinjiang, China, and the phylogenetic relationships of basal pterosaurs. Journal of Vertebrate Paleontology, 30(1), 163-187.
• Barrett, P. M., Butler, R. J., Mundil, R., Scheyer, T. M., Irmis, R. B., & Sánchez-Villagra, M. R. (2014). A palaeoequatorial ornithischian and new constraints on early dinosaur diversification. Proceedings of the Royal Society of London B: Biological Sciences, 281(1791), 20141147.
• Barrett, P. M., Evans, D. C., & Campione, N. E. (2015). Evolution of dinosaur epidermal structures. Biology letters, 11(6), 20150229.
• Czerkas, S. A., & Ji, Q. I. A. N. G. (2002). A new rhamphorhynchoid with a headcrest and complex integumentary structures. Feathered Dinosaurs and the origin of flight, 1, 15-41.
• Frey, E., Tischlinger, H., Buchy, M. C., & Martill, D. M. (2003). New specimens of Pterosauria (Reptilia) with soft parts with implications for pterosaurian anatomy and locomotion. Geological Society, London, Special Publications, 217(1), 233-266.
• Kellner, A. W. (2003). Pterosaur phylogeny and comments on the evolutionary history of the group. Geological Society, London, Special Publications, 217(1), 105-137.
• Ji Q., & Yuan C. (2002) Discovery of two kinds of protofeathered pterosaurs in the Mesozoic Daohugou Biota in the Ningcheng region and its stratigraphic and biologic significances. Geol. Rev. 48, 221–224.
• Sharov A, G. (1971). New flying reptiles from the Mesozoic of Kazakhstan and Kirghizia. - Transactions of the Paleontological Institute, Akademia Nauk, USSR, Moscow, 130: 104–113 [in Russian].
• Unwin, D. M. (2003). On the phylogeny and evolutionary history of pterosaurs. Geological Society, London, Special Publications, 217(1), 139-190.

Humps, lumps and fatty tissues in dinosaurs, starring Camarasaurus

I like to see fossil animals restored as if they belong in the world they're depicted in. That is, not just as basic, conservative reconstructions of ancient species in an certain landscape, but instead with colours, integument and soft-tissue adaptations suited for their possible lifestyles and the environments they frequented. To this end, last year I published an illustration of the Late Jurassic, North American sauropod Camarasaurus supremus as an species well adapted for life in arid settings. As a common part of the famous Morrison Formation dinosaur fauna, dry conditions would be familiar to Camarasaurus, and especially because it occupied the drier, desert-like southern extent of the Morrison palaeoenvironment. I rendered Camarasaurus as a dinosaurian camel, complete with several common cranial adaptations to resisting dry conditions and, most obviously, a fat hump on its back.

2014 restoration of Camarasaurus supremus, published in Witton (2014). Painted to make a point about palaeoart (as well as plugging the awesomeness of All Yesterdays), here's what the caption read. "Reasoned speculation in palaeoart. The sauropod Camarasaurus supremus depicted with adaptations for living in a very dry environment: enlarged nasal cavities to aid resorption of moisture, sealable nostrils to reduce evaporation, wrinkled skin to enhance heat dissipation, white and tan colouring to resist heat soaking, and a fat hump to store energy. Such features are speculative, but do not contradict any data we have for this taxon, and are consistent with the adaptations of modern desert-dwellers."

I decided to revisit this image this week to boost the sauropod content of Recreating an Age of Reptiles (coming soon, I swear!). In doing so, I decided to conduct some more research into the likely nature of non-avian dinosaur fatty tissues. I wanted to keep the fat store on Camarasaurus, as equivalent structures provide energy and water reserves for many modern desert species, and there's no reason to think that extinct dinosaurs would not have developed fat stores for similar purposes. However, is a camel-like hump really likely in a dinosaur? Can we credibly restore any details of dinosaur fats? These were questions I sought to investigate more thoroughly before jumping into my revisions.

Yo extant diapsids so fat

If we're thinking about how to restore dinosaur fats, we need to investigate what the reptile lineage is capable of when it comes to producing and storing fatty tissues. The composition of diapsid fats is a little different to our mammalian ones, although we share functionally comparable approaches to fatty tissue makeup in many respects, including responses to endothermic demands (Goff and Stenson 1988; Saarela et al. 1991; Azeez et al. 2014). Amniotes, as a whole, have fairly similar approaches and uses for fatty tissues, which is great, because that allows us to make some reasonable inferences about fossil species.

Modern reptiles generally have lower fatty tissue fractions than mammals because of their lower energy requirements (Birsoy et al. 2013; Azeez et al. 2014). However, this is not to say that they are incapable of storing large quantities of fat, or even putting on weight rapidly. Some reptiles are indeed lean species, but some - most famously certain geckos, but also some iguanas, skinks and snakes - periodically or permanently hold large stores of fat in case of hard times, or to prepare themselves for energy-intensive feats (e.g. reproduction or long distance travel). Reptiles generally sequester fatty deposits within their torsos or in their tails, but some species also store them in their armpits and in fat pockets located at the back of the head. Individuals of many lizard species are considered healthy when these regions are literally bulging with fatty mass. To my knowledge, these masses are not directly supported by the skeleton or other tissues: it is simply the cohesive nature of fatty tissues and dermis which keeps them in place. It is known that some lizards can pack their tissues with fat rapidly when necessary, some experiments finding geckos can increase their body mass by 50% in four days (enough fuel to sustain them for over half a year!) (Mayhew 2013). Indeed, reptiles are so good at packing on fat, and maintaining it, that owners pet reptiles will know that obesity can be a real issue for captive lizards.

What about living dinosaurs? As with other diapsids, birds can rapidly generate fatty tissues in anticipation of stressful periods, and frequently do so before, for instance, migrating (Lindström and Piersma 1993). 10-15% body fat is considered low for a migrating bird, with the bodies of some species comprising 50% fatty tissues before embarking on their travels - seasoned ornithologists recognise birds as positively emaciated when they finish their journeys (Alerstam and Christie 1993). However, birds are not fully reliant on fatty tissues as energy stores, some species routinely using their muscles and organs as fuel sources during long migrations. It seems only their lungs and brains are safeguarded against being turned into energy (Battley et al. 2000): everything is fair game for fuel or other components needed to maintain a functioning body. Avian fatty tissues are, like those of lizards and crocs, deposited within their torsos but, in lieu of large tails, they also store them across the surface of the chest and abdomen. Bird skin has some transparency, and field ornithologists interested in avian fat tissue fractions can determine their extent by simply checking the amount of yellowish fat tissue visible underneath bird feathers (e.g. Rogers 1991).

The dinosaur hump controversy

Is there any direct indication of fatty tissues in Mesozoic dinosaurs? The answer is probably 'no', except for the controversial idea that the elongate dorsal neural spines if some dinosaurs are indicative of a camel-like 'hump' morphology. Spinosaurus, Ouranosaurus and Deinocheirus are key species here, these animals being depicted sometimes as humpbacked creatures. These interpretations are not the sole remit of artists, either: Bailey (1997) proposed that the tall neural spines of certain dinosaurs supported masses of tissue acting as energy stores or heat buffers - in other words, a heap of fat.

I must admit to being very sceptical that neural spine anatomy is linked to fat humps. For one,it seemingly violates what we see in the extant phylogenetic bracket for dinosaurs, where no species (to my knowledge) have substantial fat deposits on their backs. Of course, it might be queried how meaningful phylogenetic bracketing is for this issue. Fatty tissues seem quite pliable in an evolutionary sense, being chucked around animal bodies with ease as lineages adapt to new conditions (Birsoy et al. 2013). It isn't crazy to think that dinosaur bodies are different enough from those of modern diapsids that they could not have their own take on fat distribution, and there are certainly functional constraints on extant diapsid fatty tissues which are unlikely to apply to non-avian dinosaurs. However, that's only speculation, and one which conflicts with a big pool of direct data on this issue.

Another approach might be to look at animals which do have fatty humps on their backs - several types of mammal - to see if their composition is analogous to anything we see in non-avian dinosaurs. What do their humps look like internally?

A collection of animals with humpbacks and sails. Fatty humps are not directly supported by skeletons in modern species including (B) lowland gorillas (Gorilla gorilla), (C) dromedaries (Camelus dromedaries) and (D) white rhinoceros (Ceratotherium simum). Vertebral spines anchor sails in some modern lizards, such as crested chameleons (Trioceros cristatus; E), and withers anchor powerful neck muscles as in American bison (Bison bison; F). Cropped figure from Witton (2014); B–D and F from Goldfinger (2004); E historic x-ray (1896) by Josef Maria Eder.

Turns out that most mammalian humps are akin to those bulging reptile fat masses mentioned above: they tend to exist without internal support or even osteological correlates. Where humps do correlate with bone, they are comprised of powerful musculature, not fat: the shoulder humps of rhinos and bison show this well. These structures might have subcutaneous fat on them, but this is not their primary composition, nor does fat storage seem to be a principle adaptive purpose. In several species, like camels and rhinos, the longest neural spines do not align with soft-tissue humps at all, these actually being located over dorsal vertebrae with smaller neural spines (camels) or short-spined cervical vertebrae (rhinos). Taking our attention away from mammals, and turning to reptiles, we see that elongate neural spines anchor laterally compressed sail-like structures, not masses of fat. It thus seems that we have no modern correlation between fatty humps and skeletons at all, and that there is no link between elongate neural spines and fatty deposits - quite the opposite actually seems true. It was this suite of observations which led to my 2014 humped Camarasaurus image: bizarrely, it is more consistent with modern data (though still extremely speculative) to put a camel-like hump on something without long neural spines, like Camarasaurus, than it is to put one on Spinosaurus, Ouranosaurus or Deinocheirus. Sail-like structures or (at least for the lower regions of the spines) muscle attachment seem more parsimonious interpretations of their strange vertebrae - if we're being scientific (as we should be in palaeoart), we really shouldn't be looking at those tall neural spines and thinking 'fat hump correlate'.

Tying all this together

Although we may lack direct evidence of them from fossils, data from extant animals suggests it is sensible to restore dinosaurs with noticeable, prominent fatty tissues, especially if we're reconstructing animals associated with extremes of behaviour, climate or environment. Animals about to undertake migration should look well fed and bulky, and those at the other end might look leaner and less nourished. We certainly have good precedent for restoring desert-dwelling Mesozoic dinosaurs - of which there are many - with energy and water reserves, given that even energy-limited ectothermic diapsids take such precautions, as do some endotherms. We should probably not limit fatty tissues to bulky energy stores, either: as in modern lizards, some extinct reptiles may have housed pockets of fat in prominent places to serve as advertisements of health and virility.

Where should we locate those big energy stores? With no direct indication from fossils, I suggest we err on the side of caution and follow the diapsid condition, principally locating them around the tail base and abdomen. Most Mesozoic dinosaurs had well-developed, powerfully muscled tails, and were thus likely capable of supporting a wad of adipose tissue at the tail base. We could start restoring humps in other places, but it seems sensible to keep speculative anatomy grounded somewhere. Besides, it's not like a fat-tailed dinosaur is boring concept!

Combining all this together, I'll leave you with the completed, revised version of my desert-adapted Camarasaurus image, now with fatty tissues fully consistent to those of modern diapsids. This meant chopping off the back hump (I'm not going to pretend I wasn't disappointed to do that), but it's worth it for a more defensible image. Note that the adult is sporting not only a fat tail, which is meant to represent sustenance for wandering through harsh desert settings, but also a pair of natty fat pockets behind the skull. It looks fairly happy with them.

Camarsaurus supremus, queen of the desert, not a member of Weight Watchers.

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References

• Alerstam, T., & Christie, D. A. (1993). Bird migration. Cambridge University Press.
• Azeez, O. I., Meintjes, R., & Chamunorwa, J. P. (2014). Fat body, fat pad and adipose tissues in invertebrates and vertebrates: the nexus. Lipids Health Dis, 13, 71.
• Bailey, J. B. (1997). Neural spine elongation in dinosaurs: Sailbacks or buffalo-backs?. Journal of Paleontology, 1124-1146.
• Battley, P. F., Piersma, T., Dietz, M. W., Tang, S., Dekinga, A., & Hulsman, K. (2000). Empirical evidence for differential organ reductions during trans–oceanic bird flight. Proceedings of the Royal Society of London B: Biological Sciences, 267(1439), 191-195.
• Birsoy, K., Festuccia, W. T., & Laplante, M. (2013). A comparative perspective on lipid storage in animals. Journal of cell science, 126(7), 1541-1552.
• Goldfinger, E. (2004). Animal Anatomy for Artists: The Elements of Form: The Elements of Form. Oxford University Press.
• Goff, G. P., & Stenson, G. B. (1988). Brown adipose tissue in leatherback sea turtles: a thermogenic organ in an endothermic reptile?. Copeia, 1071-1075.
• Lindström, Å., & Piersma, T. (1993). Mass changes in migrating birds: the evidence for fat and protein storage re-examined. Ibis, 135(1), 70-78.
• Mayhew, W. W. (2013). Biology of desert amphibians and reptiles. In: Brown, G. W. (Ed.). Desert biology: special topics on the physical and biological aspects of arid regions (Vol. 1). Elsevier.
• Rogers, C. M. (1991). An Evaluation of the Method of Estimating Body Fat in Birds by Quantifying Visible Subcutaneous Fat. Journal of Field Ornithology, 349-356.
• Saarela, S., Keith, J. S., Hohtola, E., & Trayhurn, P. (1991). Is the “mammalian” brown fat-specific mitochondrial uncoupling protein present in adipose tissues of birds?. Comparative Biochemistry and Physiology Part B: Comparative Biochemistry, 100(1), 45-49.
• Witton, M. P. (2014). Patterns in Palaeontology: Palaeoart-fossil fantasies or recreating lost reality. Palaeontology Online, 4, 1-14.

The life aquatic with flying reptiles

Pteranodon sternbergi dives for a school of panicked fish. So, what, pterosaurs are super good at swimming now? Read on... Reworked version of an image from Witton (2013). Click here to buy prints of this image (and join my Patreon campaign for a discount!). And yes, I'm calling this animal Pteranodon, not Geosternbergia.

Whether or not pterosaurs could swim, or how well they could swim, is a recurrent discussion among those interested in flying reptiles. For the most part, palaeontologists have seemed happy to assume that pterosaurs were aquatically capable, at least long enough to permit their escape from water, because so many pterosaur fossils occur in coastal or marine sediments. Moreover, some long-known specimens show evidence of pterosaurs feeding on aquatic prey. Odds are that pteroaurs would end up in water some of the time, even if only by accident, so it makes sense that they could at least keep themselves afloat for a while. Plus, virtually all tetrapods can swim one way or another, including bats and bird species which, on first principles, seem ill-suited to aquatic locomotion. Pterosaurs might be a bit strange, but they'd have to be very strange not to be capable of at least limited aquatic locomotion.

Proof that pterosaur workers of old thought swimming was possible: Bramwell and Whitfield's (1974) landmark paper on Pteranodon flight depicts one attempting to take off from water.

In recent years, pterosaur researchers have taken a more in depth look at pterosaur swimming, with three main lines of inquiry offering perspectives on how, and how well, pterosaurs took to water. The first concerns pterosaur swim tracks, scratch marks made in upper Jurassic sediments of North America made by pterosaurs paddling across a shallow lake. First described by Lockley and Wright (2003), these tracks record pterosaur feet scraping narrow gouges into sediment, sometimes with toe pad impressions, as buoyant pterosaurs propelled themselves over lake margins. At least locally, such tracks are not rare: Lockley and Wright (2003) report bedding planes covered with hundreds of parallel scratch marks attributed to swimming pterosaurs. Toe pad impressions are only seen occasionally, suggesting that most of these track makers were more or less entirely supported by water, only the very tips of their toes scraping the lake bed. Notably absent altogether from the same slabs are imprints from pterosaur forelimbs. Neither wingtips or walking fingers left impressions when these pterosaurs were swimming or punting about. This helps us work out what these swimming pterosaurs might have looked like, as well as how they propelled themselves: their arms must been held higher than their legs, and at least some of their locomotion was achieved through peddling feet. Quite what this means for mysterious 'manus only' pterosaur tracks (pterosaur track sites where only hand impressions are recorded) is a discussion for another day.

Select examples of pterosaur swim tracks from the Jurassic Summerville (A) and Sundance (B) formations, North America. There are many more examples of tracks like this - some bedding planes are covered in them. Traced illustrations from Lockley and Wright (2003), published in Witton (2013).

Pterosaur swim tracks provide a compelling answer to the basic question over whether pterosaurs could swim at all: clearly, some could, and swim track abundance suggests this behaviour was not unusual, in at least some species. But were all pterosaurs equally adept at swimming, and what - beyond relative positions of the limbs - was their likely floating posture? We have typically assumed that floating pterosaurs might look a bit like floating birds, sitting high on the water surface with their heads well clear of the anything wet. To test this, Hone and Henderson (2014) threw sophisticated, 3D virtual models of pterosaurs into buckets of digital water to see how they floated. These models had variable density for major body components, so account for the distribution of airsacs throughout pterosaur bodies. Some readers may be familiar with Don Henderson's digital water experiments concerning other species: we've seen sauropods and giraffes given the same treatment to understand their floating mechanics (Henderson 2004; Henderson and Naish 2010; and yes, that reads 'giraffes': as explained here, no-one really knows how well they swim!). The Hone and Henderson study included multiple pterosaur species, and grounded itself with convincingly replicating the floating postures of birds (as, indeed, other Henderson studies have done with the floating postures of other extant animals).

How did pterosaurs fare? Although they assumed a stable floating posture, it was not quite as expected. As explained by Dave Hone at The Guardian, pterosaurs were incapable of assuming a bird-like pose when floating. Playing around with postures and body component densities made little difference: the digital pterosaurs consistently floated with their heads close to, or somewhat submerged, in water. Crucially, their nostrils always ended up close to the digital water line, suggesting that anything but a motionless pterosaur in the calmest water was going to be struggling for a clear airway. The problem, it seems, is that pterosaurs are very front heavy. Pterosaurs combine large heads, necks and shoulders with comparatively slender hindquarters so that, even accounting for their pneumatic features and denser hindlimbs, they consistently pitch forward when floating. This condition is more pronounced in pterodactyloids than other pterosaurs, but the general problem applies across the group.

So, sorry, 2013 Ornithocheirus-as-a-bird-like-floater-image-that-I-have-a-little-soft-spot-for, you're out of date.

Does the inability for pterosaurs to float like birds make them unlikely to enter water? To answer that, we might need to think about bird anatomy for just a minute. Because we see swimming birds so often, we don't think their floatation skills are especially remarkable, but they actually are. Bird anatomy is ideal for stable, effortless floating: not only are their necks and heads smaller than those of pterosaurs, but their heavy shoulder regions are counterbalanced by large, strongly muscled legs. This, of course, is a reflection of the hindlimb-dominated launch strategies employed by birds. The only reason their legs are so large and heavy is because of the demands of bipedal launch. Other tetrapod fliers, like pterosaurs, launch using different strategies have no need for heavy hindquarters, which means they overbalance easily in water. Bird bodies are thus exapted for floating, their comparatively large, well-balanced and pneumatised torsos providing stable, lightweight platforms to rest on water. Birds are so good at floating that they can be entirely passive when doing so, their heads sufficiently clear to avoid issues with respiration and light enough that they can move them around freely without overbalancing. This is taken to extreme in aquatic birds like swans and ducks, which perform much of their daily activities on water surfaces. They're essentially flying barges, alighting on water to collect food with lightweight, crane-like necks and heads. The next time you see a floating swan, consider that you're looking at an evolutionary champion as goes floating and foraging from the water-surface.

What does this mean for pterosaurs? Their inability to float like birds probably rules out some behaviours, such as prolonged bouts of sitting on water to rest or forage. However, most swimming animals - even those which routinely travel or forage in water - also can't float like birds. Indeed, predicted pterosaur floating postures are actually pretty consistent with those of other non-avian tetrapods. We might therefore surmise that pterosaur floating abilities are not atypically bad, but simply not at the 'advanced' avian level. As with most tetrapods, pterosaurs might have been quite happy in water, the caveat being that it would never be a passive, restful act. Water-borne pterosaurs were likely either were there for a reason (e.g. finding food, moving through an environment) or, if they had no business there, sought to escape it as soon as possible.

This brings us to the third string of recent work on aquatic pterosaur habits: the biomechanics of entering and exiting water. Earlier this year I discussed pterosaur water launch at some length, so will only provide a brief summary here. Calculations by pterosaur biomechanicists Michael Habib and Jim Cunningham (2010) suggest that pterosaur quadrupedal launching also works on water, albeit in a modified, and slightly more energy intensive form. For some pterosaurs, the effort needed to escape water necessitates a series of hops across the water/air interface to escape surface tension and build up velocity, but some - like the big, powerful azhdarchids - could hulk smash water powerfully enough to escape in one go.

Ornithocheiroid Ornithocheirus simus achieves launch velocity from a coastal sea. Prints of this painting are available from my shop.

Pterosaur water launch becomes especially relevant to our discussion of aquatic habits when we consider the adaptations it imposed on pterosaur anatomy. Certain pterosaurs - ornithocheirids, pteranodontids, rhamphorhynchids - possess features which are unusual among pterosaurs until viewed in light of aquatic launching. Reconfiguring the shoulder muscles to optimise for aquatic launches favours warped or hatchet-shaped deltopectoral crests (the flange on the humerus which anchors flight muscle), robust shoulders, reduced hindlimbs and broad wing joints: most or all of these characters occur in these lineages (Habib and Cunningham 2010). Other pterosaurs - like the aforementioned azhdarchids - seem capable of water launching without these features, suggesting they are not strictly essential for water launch. We might therefore consider some pterosaurs as specifically adapated for aquatic takeoff, implying that some taxa were routinely entering aquatic realms rather than just casually dropping in, or suffering the odd accident.

As with terrestrially-based pterosaurs, it seems takeoff strains put a cap on the maximum size of aquatic-adapted forms. In his Flugsaurier 2015 talk, Mike Habib explained how animals larger than Pteranodon (biggest wingspans around 5-6 m) would struggle with water launching. The largest ornithocheiroids (8-9 m wingpan, c. 160kg in mass) seem to require significant energetic investment and space to take off from water, to the extent that entering aquatic settings resulted in a net loss of energy unless food was particularly plentiful (Habib 2015). This is not to say water launching was impossible for very large or giant pterosaurs, but that the energy demands make it an unlikely routine behaviour. Pterosaur aficionados will note that this size constraint is lower than those proposed for terrestrial launchers (Habib 2013): as might be expected, this reflects the complexity of launching from a fluid substrate instead of hard ground.

Nevertheless, most pterosaurs were not operating at those enormous proportions, and so could theoretically enter water with less concern. Intriguingly, early calculations suggest that some pterosaurs were well-suited to rapid water entry. Qualitative assessments of Pteranodon anatomy indicate that it might be capable of performing shallow dives because, in general construction, it is no less robust than diving birds like pelicans (Bennett 2001; note this is not advocating pelican-like feeding for Pteranodon per se, but simply that Pteranodon anatomy was robust enough to dive into water from a flighted position). Mike's Flugsaurier 2015 talk suggested that this observation is borne out in some basic assessments of skeletal strength. Diving actions would not exceed safety factors of the Pteranodon skeleton, and its streamlined head and air sacs anterior to the torso would aid force dissipation as the animal penetrated the water surface. I must admit to finding the concept of diving Pteranodon quite appealing. Pteranodon skulls are especially streamlined and pointy compared to many other marine pterosaurs (not the least because they lack teeth and anterior crests), and we know that at least some individuals predated relatively tiny fish (Bennett 2001) which may have been difficult to snag during flight. Thus, some sort of shallow diving to get Pteranodon into water where it can pursue prey makes sense to me (as depicted above, see Witton 2013 for more discussion of this concept).

Pteranodon sp. jaw specimen AMNH 5098. That mass of random crap between the manidibular rami is a heap of small, half-digested fish vertebrae. Scale bar represents 100 mm.

To tie this together, our understanding of pterosaurian aquatic locomotion has moved on a lot in just over a decade. While it would be remiss to pretend we have anything more than a basic understanding of their aquatic skills, we nevertheless have some basic hypotheses in place for further work: footprints tell us pterosaurs did swim; digital models give us some idea of likely floating postures and constraints on behaviour; and biomechanical studies hint at anatomical parameters suited to aquatic locomotion. This allows us to start asking more refined questions: which species regularly entered water, and why? How did they propel themselves? Were any pterosaurs specifically adapted for aquatic lifestyles? There are several projects in the works which have bearing on these questions, and those interested in pterosaur lifestyles will definitely want to keep an eye out for them.

This post was brought to you by Patreon

If you've enjoyed this post, and would like to see more original artwork and articles on cool fossil animals, please consider contributing to my Patreon campaign. For as little as $1 a month you can help keep this enterprise ticking over, and you'll get access to exclusive content, discount print prices and other rewards for your troubles. A huge thanks to those who have signed on in my first week of Patreon - your support is really appreciated and encouraging.

References

• Bennett, S. C. (2001). The osteology and functional morphology of the Late Cretaceous pterosaur Pteranodon Part I. General description of osteology. Palaeontographica Abteilung A, 1-112.
• Bramwell, C. D., & Whitfield, G. R. (1974). Biomechanics of Pteranodon. Philosophical Transactions of the Royal Society B: Biological Sciences, 267(890), 503-581.
• Habib, M. (2013). Constraining the air giants: limits on size in flying animals as an example of constraint-based biomechanical theories of form. Biological Theory, 8(3), 245-252.
• Habib, M. 2015. Size limits of marine pterosaurs and energetic considerations of plunge versus pluck feeding. Flugsaurier 2015 Portsmouth, Abstract Volume, 24-25.
• Habib, M. B., & Cunningham, J. (2010). Capacity for water launch in Anhanguera and Quetzalcoatlus. Acta Geoscientica Sinica, 31, 24-25.
• Henderson, D. M. (2004). Tipsy punters: sauropod dinosaur pneumaticity, buoyancy and aquatic habits. Proceedings of the Royal Society of London B: Biological Sciences, 271(Suppl 4), S180-S183.
• Henderson, D. M., & Naish, D. (2010). Predicting the buoyancy, equilibrium and potential swimming ability of giraffes by computational analysis. Journal of theoretical biology, 265(2), 151-159.
• 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.
• 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.
• Witton, M. P. (2013). Pterosaurs: Natural History, Evolution, Anatomy. Princeton University Press.

Announcing my Patreon page

Scleromochlus taylori, because a hustling palaeoartist needs mascots. The full painting can be seen at my Patreon page, and you can read more about this fantastic little animal here.

Regular readers may have noticed I've been making a bit of an effort to make a living from my art this year, setting up a print store and producing a palaeoart book which will be arriving in the next month or so. I really appreciate the enthusiasm and interest I've received about these projects but, like many artists, I find that selling specialised merchandise only goes so far when it comes to making a living. My situation has got to the point where I need to justify the time put into these projects instead of, you know, getting a proper job or something. I like doing what I do, and get the feeling that people enjoy my output, so I'm looking for ways to make my artwork and writing sustainable for the long run.

To that end, I've hopped on the Patreon bandwagon. Patreon, for those unfamiliar with it, is a site which allows followers of artists to pledge money in support of their creative output. The idea is to provide creative types with reliable income which, in other respects, can be otherwise difficult to source through online media - especially if that media is highly specialised (which I think we can all agree applies to palaeontology-based content).

Through my Patreon page, you can support my work with donations whenever I produce a new piece of artwork and/or article. Even small donations - as little as $1 per work - are appreciated, and you can cap the number of pledges you make per month so budgets are not exceeded. There's no obligation to maintain pledges over time, and you can change or stop your contribution whenever you like. Whatever your pledge, the ultimate pay off is that I can invest more time and effort into my output, which means more varied, interesting and higher quality content. As a bonus, I'm also offering reward packages to say thanks to those supporting my work. They include access to exclusive content (previews of upcoming work), access to print-quality artwork files for non-commercial use, prints, books, and commissions. The full break down is thus:


Pledge $1.00 or more per artwork and/or article

• Access to exclusive Patreon content 

Pledge $5.00 or more per artwork and/or article

• Access to exclusive Patreon content

• One small print (up to 8x10") of your choosing each year

Pledge $15.00 or more per artwork and/or article

• Access to exclusive Patreon content

• One small print (up to 8x10") of your choosing each year

• Access to a library of web-resolution artworks for free use (with attribution)

• Access to print-quality artwork files, allowing you to print your own copies for personal use

Pledge $30.00 or more per artwork and/or article

• Access to exclusive Patreon content

• One small print (up to 8x10") of your choosing each year

• Access to a library of web-resolution artworks for free use (with attribution)

• Access to print-quality artwork files, allowing you to print your own copies for personal use

• Signed copy of my upcoming book Recreating an Age of Reptiles (eta. October 2015)

• Your own commission - I'll paint a fossil species of your choosing, you'll get a high-quality digital file for (non-commercial) use, and a signed print

That's pretty much the nuts and bolts of this plan - further details can be found at my Patreon page. A few individuals have already signed up - huge thanks to them - and, if you like what I do, please consider joining them.