Walking with ichthyosaurs: the amphibious ichthyosaur hypothesis

Benjamin Waterhouse Hawkin's (1858?) sketch of amphibious marine reptiles, including a large shambling ichthyosaur. Image borrowed from Frank T. Zumbach's Mysterious World.

One of the most charming aspects of mid-19th century palaeoart are those amphibious marine reptiles: depictions of ichthyosaurs and plesiosaurs that hauled themselves onto rocks or beaches to rest, or lunge with open jaws at passers by (above). To modern eyes these images look naive and quaint, a clear reminder of how far our understanding of fossil animals has progressed in the last two centuries.

Of course, art has a habit of imitating life and, a good 150 years after amphibious marine reptiles became unfashionable in palaeoartworks, Ryosuke Motani and colleagues (2014) published a new marine reptile suggested to be capable of locomotion on land as well as in water: the ichthyosauriform Cartorhynchus lenticarpus. This Chinese, Early Triassic species is anatomically remarkable in several respects. Although reminiscent of early ichthyosaurs in overall shape, it has a considerably reduced snout, seems to lack teeth, is just 20 cm from snout to vent despite indications of osteological maturity, and bears enormously long forelimbs. Though unique when first discovered, another, much larger Cartorhynchus-like species has since been found in the same deposits, Sclerocormus parviceps. Together, these animals form a clade at the base of Ichthyosauriformes known as Nasorostra, the 'nose beaks', referring to a defining feature where their nasal bones reach the jaw tip (Jiang et al. 2016).

Holotype specimen of Cartorhynchus lenticarpus. Note the enormous forelimbs with their expansive unossified wrists, indicated by the distal phalanges being well posteriorly displaced from the upper arm bones. From Motani et al. (2014).

The amphibious habits of Cartorhynchus are primarily based on its unusually large forelimbs and small body size, it being reasoned that Cartorhynchus could drag or propel itself over exposed sediments like a mudskipper, turtle or pinniped. I find this idea fascinating: an ichthyosauriform that was at home outside of water? Cartorhynchus certainly deviates from ichthyosaur anatomy and evolutionary trends enough to inspire inquiry about its weird bauplan - if it was not amphibious, it might be doing something else equally unexpected. The amphibious Cartorhynchus hypothesis has received surprisingly little detailed attention online, save for coverage of a 2014 press release and this excellent primer article at Tetrapod Zoology, so there's scope for a closer look at this idea. What is the evidence for amphibious habits in Cartorhynchus, and how does this concept fit models of early ichthyosaur evolution?

The functional basis for an amphibious lifestyle in Cartorhynchus

Motani et al. (2014) present a fairly detailed argument in favour of amphibious habits in Cartorhynchus. The chief lines of evidence are those expansive forelimbs, but it's not just their size that matters: their enormous, unossified carpal regions are also significant. Several early ichthyosauriforms have poorly ossified carpal bones but the unossfied region in Cartorhynchus flippers is proportionally bigger by some margin. This would allow these ordinarily-rigid marine reptile flippers an unusual degree of flexibility and optimise them for terrestrial locomotion. Flipper-based terrestrial motion is surprisingly tricky because its users tend to be suboptimally designed for movement out of water and they almost always have to overcome drag forces acting on the body as well as shove themselves around. Moreover, substrates associated with coasts and waterways tend to be unstable, yielding under pressure and being challenging for even proficient terrestrial animals. These factors mean flippers can easily dig into substrate or slip across it rather than propel their owners about, and it's easy to see why beaching is fatal for so many specialised aquatic species.

Studies (using robot turtles!) suggest that rigid flippers are generally poor at terrestrial locomotion and may even be incapable of moving animals over some surfaces (Mazouchova et al. 2013). A bendy flipper, in contrast, works well, allowing the forelimb to flex before the substrate moves, spreading the weight of the animal over the distal limb and allowing the proximal flipper region to elevate and support the body (Mazouchova et al. 2013; Motani et al. 2014). The unusually expanded flexion zone in Cartorhynchus forelimbs would be well suited to this purpose, and certainly much better at this task than those of other ichthyosaurs. We might note, as an aside, that the lack of flexion zones in other marine reptile flippers, such as those of plesiosaurs, might be good reason to doubt their ability to crawl over land.

Did I mention the robot turtles? There are robot turtles. Supplementary video data from Mazouchova et al. (2013).

The downside of having lots of cartilage in a long flipper is that they are weaker against bending than a more ossified one, so their utility as a walking limb lessen as the forces involved in moving the body increase. It's here where the small size of Cartorhynchus comes into play. Small size equates to low body masses and smaller forces associated with lifting the body, less structural demand on the flipper, and reduced drag effects from the sliding belly. As is so often the case in evolution, small body size might be an enabler for evolutionary experimentation in Cartorhynchus, allowing it to perform feats that its bigger relatives just couldn't even if they were also equipped with giant, bendy fins.

The tail of Cartorhynchus is incompletely known but it's anatomical and phylogenetic proximity to the completely-known Sclerocormus suggests that its tail was long, flexible, and lacked any sort of fin or fluke (Jiang et al. 2016). A relatively simple tail lessens the risk of it dredging sediment or catching on debris during terrestrial locomotion and its flexibility might have permitted its use as a prop or even propulsive organ: fish such as the Pacific leaping blenny show how a long, bendy tail can be used to powerful effects in semi-terrestrial locomotion (Heish 2010, also below). Combinations of fin and axial motion in land-crawling fish can be surprisingly effective over a range of substrates (Standen et al. 2016) and we might assume similar options were available to Cartorhynchus.

 

Leaping blennies, robot turtles... is this the best blog post ever? From Wikipedia, source: Hsieh (2010).

The torso of Cartorhynchus is also of interest for this hypothesis. In contrast to some other Triassic ichthyosaurs, Cartorhynchus has a broad, stout torso rather than a long, laterally-compressed one (Carrol and Dong 1991). Though a wider torso would impart more drag during terrestrial crawling, it would aid stability when crawling over land. Moreover, torso drag can be lessened by shortening the body overall, giving new significance to the low Cartorhynchus pre-sacral vertebral count of 31 vertebrae, instead of a more typical ichthyosaurian count of 40-80 (Motani et al. 2014). Short, narrow hindlimbs, rather than the broad pelvic flippers of some other early ichthyosaurs, might have further aided drag reduction.

Cartorhynchus in context

It seems there's a prima facie argument for considering Cartorhynchus as equipped with some amphibious features. However, we should not get carried away - a suite of evidence for an aquatic lifestyle suggests it wasn't it a specialist denizen of shallow, partly-exposed habitats, but more of an animal able to exploit two realms. It has pachyostotic bones, true flippers rather than webbed walking limbs, and is adapted for suction-feeding: a mechanism where the combination of a small mouth and a large oral cavity creates a pressure differential during feeding, literally sucking small prey into the mouth if it's opened quickly (Motani et al. 2014). This foraging strategy cannot work outside of water so is strong support for Cartorhynchus foraging in fully aquatic settings.

Cartorhynchus also stems from the Nanlinghu Formation, a mudrock and limestone marine deposit rich in fossils of aquatic reptiles and marine invertebrates: ammonoids, bivalves and conodonts. We might take these data as signs that Cartorhynchus was quite happy in water and maybe spent most of its time there, visiting coastlines and beaches on occassion, rather than living there permanently. We should also regard it as a marine animal, not an inhabitant of rivers or swamps (though it would be extremely cool if one turned up in such deposits!).

Holotype of Hupehsuchus nanchangensis, a marine reptile seemingly more closely related to the ancestor of ichthyosaurs than Cartorhynchus. These guys surely deserve their own blog post and painting at some point. From Carroll and Dong (1991).

The relationships of Cartorhynchus to other marine reptiles is also interesting in light of the amphibious hypothesis. You could be forgiven for interpreting Cartorhynchus as some sort of bridge between ichthyosaurs and terrestrial reptiles, but, no, the nasorostran clade seems to nest above the root of the ichthyosaur line between 'true' ichthyosaurs and the fully marine, ichthyosaur-like hupehsuchians (Motani et al. 2014; Jiang et al. 2016). The ichthyosaur + hupehsuchian clade, Ichthyosauromorpha, may be further allied to another group of marine reptiles, the amphibious thalattosaurs (Motani et al. 2014 - Darren Naish has an excellent overview of this topic here). This surrounds Cartorhynchus with lineages that had taken to water in a significant way and we should conclude that any amphibious adaptations of Cartorhynchus do not represent an ichthyosaurian invasion of the sea, but ichthyosaurs returning to land.

Some might consider this surprising evolutionary scenario evidence against the amphibious hypothesis - why would a lineage of marine reptiles start retracing their adaptive steps to become landworthy, when the rest of the group is pressing ahead with more specialised aquatic lifestyles? In response, perhaps we should ask if a potentially amphibious marine reptile is really that surprising. A huge number of vertebrates have transferred between terrestrial and aquatic lifestyles in the last 400 million years, sometimes contrasting with wider adaptive trends taking place in closely related species. Well-understood evolutionary 'transitions' also show that large-scale adaptive phases are often complex with all manner of evolutionary experimentation and dead-end offshoots. We know that bridging aquatic and terrestrial realms can be advantageous to aquatic species - refuge from predators or rough seas, access to food off-limits to other marine species, access to safe habitats for rest or reproduction, etc. - and there's no reason to think ichthyosaurs were incapable of capitalising on these advantages, or immune to their selective draws. With all this in mind, the concept of a marine reptile exploiting semi-exposed habitats isn't really that radical. Maybe the key question here isn't 'why would a marine reptile go rouge and turn landward?' but is 'why aren't we seeing more of this sort of thing?'.

What about Sclerocormus?

A question currently unaddressed in technical literature is whether the other currently known nasorostran, Sclerocormus, might have also bear amphibious hallmarks. It has virtually all the same features that we likened to amphibious adaptations above, the only distinctions being marginally enhanced ossification of the forelimb (though it still retains a comparatively enormous unossified carpal region) and greater size overall (body length of 160 cm, representing an animal about 3.3 times larger than Cartorhynchus). In lieu of a detailed, quantified assessment it's difficult to say whether Sclerocormus was too heavy to pull itself along on land, but we can note that it is not especially big compared to the truly massive aquatic animals we have scampering over beaches today - leatherback turtles, giant pinnipeds, the odd manatee (Motani et al. 2014) and so on. Some of these animals weigh several tonnes and, if they can haul themselves out of water, maybe Sclerocormus could too.

Holotype specimen of the larger nasorostran species, Sclerocormus parviceps. From Jiang et al. (2016).

I find this question particularly interesting given how similar Sclerocormus and Cartorhynchus are in virtually all aspects (above). Is nasorostra a clade of potentially amphibious ichthyosaurs, or are we actually looking at growth stages of one oddball species? Their proportions are near identical, and they are only separated by fine details of anatomy (Jiang et al. 2016). Many proposed differences might be attributable to intraspecific variation, too. For instance, the significance of their slightly different vertebral counts is questioned through populations of living snakes, limbless lizards and fish with variable numbers of axial elements (Tibblin et al. 2016). Individually variable vertebral counts seem common in species with large numbers of axial elements, and this might have been true for ichthyosaurs. Ontogeny and scaling effects could explain other differences, including overall size, greater ossification of the postcranial skeleton, and subtle arrangements of skull bones. It can't be overlooked that these near identical species, unique in morphology in the grand scheme of ichthyosaur evolution, also happen to occur in the same member of the same formation, separated by only 14 m of strata (Jiang et al. 2016). For the time being, the identification of 'adult' skull fusion and textures in Cartorhynchus suggests they aren't the same species, but the marine reptile trait of retaining poorly fused skeletons into adulthood makes identifying adult forms especially tricky, especially with so few specimens to look at (Motani et al. 2014). It also seems worryingly difficult to tease fossil adults from juveniles without histological assessments, even with large sample sizes and good growth series (e.g. Prondvai et al. 2009). Perhaps we're waiting on histological examinations and more specimens to make a call on this.

So, walking with ichthyosaurs?

And finally, a painting: Cartorhynchus goes for a drag around a Triassic lagoon.

Putting all the strands of the amphibious Cartorhynchus hypothesis together, I don't see reason for excessive suspicion about the idea of beach hauling nasorostrans. At the core of the pro-amphibious argument is that Cartorhynchus (and perhaps, by extension, Sclerocormus) has weird anatomy that requires an explanation - it's just too different from other ichthyosauromorphs to pretend it wasn't doing something unusual, maybe even unexpected. Amphibious behaviours are an explanation that seem to chime well with provisional form-function investigations and seem a sensible hypothesis at this time. That said, we should be appropriately cautious in our interpretations of these animals: our understanding of nasorostrans is in its infancy and alternative, currently-unexplored functional hypotheses could explain their anatomy as well, or better, than the amphibious concept in future. Fingers crossed that these animals receive more dedicated functional investgiations in years to come.

Or maybe more robot turtles. Either is good with me.

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References

• Carroll, R. L., & Zhi-Ming, D. (1991). Hupehsuchus, an enigmatic aquatic reptile from the Triassic of China, and the problem of establishing relationships. Philosophical Transactions of the Royal Society of London B: Biological Sciences, 331(1260), 131-153.
• Hsieh, S. T. T. (2010). A locomotor innovation enables water-land transition in a marine fish. PloS one, 5(6), e11197.
• Jiang, D. Y., Motani, R., Huang, J. D., Tintori, A., Hu, Y. C., Rieppel, O., ... & Zhang, R. (2016). A large aberrant stem ichthyosauriform indicating early rise and demise of ichthyosauromorphs in the wake of the end-Permian extinction. Scientific reports, 6, 26372.
• Mazouchova, N., Umbanhowar, P. B., & Goldman, D. I. (2013). Flipper-driven terrestrial locomotion of a sea turtle-inspired robot. Bioinspiration & biomimetics, 8(2), 026007.
• Motani, R., Jiang, D. Y., Chen, G. B., Tintori, A., Rieppel, O., Ji, C., & Huang, J. D. (2015). A basal ichthyosauriform with a short snout from the Lower Triassic of China. Nature, 517(7535), 485-488.
• Prondvai, E., Stein, K., Ősi, A., & Sander, M. P. (2012). Life history of Rhamphorhynchus inferred from bone histology and the diversity of pterosaurian growth strategies. PLoS One, 7(2), e31392.
• Standen, E. M., Du, T. Y., Laroche, P., & Larsson, H. C. (2016). Locomotor flexibility of Polypterus senegalus across various aquatic and terrestrial substrates. Zoology, 119(5), 447-454.
• Tibblin, P., Berggren, H., Nordahl, O., Larsson, P., & Forsman, A. (2016). Causes and consequences of intra-specific variation in vertebral number. Scientific reports, 6, 26372.

New paper: pterosaur palaeoecology, as told by the fossil record

A female Pteranodon tries to explain the new Silverstone et al. (2017) paper on Pteranodon taxonomy to the Cretaceous shark Squalicorax. Unfortunately for her, the sharks quite liked the 'Dawndraco' hypothesis.

Last year I posted a couple of overviews of the better parts of the pterosaur palaeoecological record, discussing what we know was eaten by Rhamphorhynchus and azhdarchid pterosaurs, as well as what species ate them. These reviews were tied to a peer-reviewed paper on the same subject which, at the end of Febuary 2017, was published as part of an upcoming collection of pterosaur papers (Witton 2017). This collection, edited by David Hone, myself, and David Martill, is the proceedings of the Flugsaurier 2015 pterosaur meeting and will, when finished, contain over a dozen new insights into pterosaur research, with an emphasis on their palaeobiology. You can check out the existing content here - keep an eye on that site, as there are more papers to come.

With my paper now out (though sadly not open access, but I will eventually be able to post an unformatted version online next year) I thought it would be a good time to take a holistic look at direct fossil evidence of pterosaur lifestyles. What are some of the most interesting examples of pterosaurs interacting with other species? Which purported interactions stand up to scrutiny, and which ones are a little tenuous? And what do they tell us about the all important Big Picture of pterosaur palaeobiology?

Yes, some pterosaurs may well have been seabird mimics

A number of pterosaur specimens have been reported as being associated with the remains of their last meals. Several of these have been lost, found to be erroneously interpreted, or are simply too poorly preserved to interpret their gut content. However, examples of the Jurassic non-pterodactyloids Rhamphorhynchus and Scaphognathus, the Triassic Eudimorphodon, and the famous Cretaceous taxon Pteranodon show reliable insights into their dietary preferences (below). These are virtually all remains of aquatic animals - mostly fish - preserved in intimate association with pterosaur skeletons, either between their jaws, aligned with their throats or within the torso skeleton. One example of a coprolite is known, though it's difficult to say exactly what it contains.

Pterosaurs and their last meals (shaded grey). A, torso of Eudimorphodon; B-D, various Rhamphorhynchus with gut content and coprolite (C), E, Scaphognathus; F, Ludodactylus; and G, Pteranodon. From Witton (2017).

Many of these specimens have been known for several decades, and their evidence of aquatic feeding probably played some part in the stereotyping of pterosaurs as seabird analogues (e.g. Wellnhofer 1991). Nowadays, we need to be a little more circumspect about what they tell us. Yes, they do show that some pterosaurs ate fish and other pelagic prey and, along with results from detailed studies into functional morphology, they help portray certain pterosaur species in the 'classic' seabird niche. Rhamphorhynchus, Scaphognathus, Eudimorphodon and Pteranodon have at least some adaptations consistent with foraging for pelagic prey, such as long wings ideal for marine soaring, 'fish-grab' jaws and adaptations for launching from aquatic settings, as well as occurrences in coastal or marine settings. It would be a little odd if these aquatic-adapted species weren't catching aquatic animals from time to time.

But we can't maintain the older view that these specimens, on their own, undermine the increasingly diverse and nuanced takes on pterosaur palaeoecology hinted at by form-function studies, biomechanics, and modern understandings of pterosaur habitats. We have thousands of pterosaur specimens in museums around the world, of which gut content is known from less than a dozen examples, and in four species. That's not even enough to demonstrate the full dietary range of the species in question, let alone tell us about the ecology of all pterosaurs. Indeed, the scarcity of pterosaur gut content agrees with some new predictions of pterosaur lifestyles in that non-aquatic food sources now suggested for pterosaurs - insects, wormy things, fruits, small tetrapods - have limited preservation potential, particularly outside of Lagerstätten. When factored against common agents of taphonomy and preservation, these hypotheses predict empty bellies in many pterosaur fossils, which is what we find virtually all of the time. It is, of course, difficult to be certain of anything concerning negative evidence, but it's nevertheless useful to note this predicted match between modern ideas and fossil data.

A selection of pterosaur foraging traces - beak tip impressions and scrape marks - from Jurassic and Cretaceous sites. The black-filled elements are the feeding traces, dark grey are manus prints, and light grey are footprints. From Witton (2017).

Evidence that not all pterosaurs were obtaining their food out to sea comes in the form of feeding traces - small, paired impressions and scratch marks created by beak tips (above). These were likely formed by pterosaurs wandering over water margins in pursuit of invertebrates and other small prey, much like extant shorebirds and waders. Indeed, if you walk across a mudflat on a falling tide you can find near identical traces made by living avians mimicking this pterosaur strategy. Somewhat frustratingly, the identities of the pterosaurs that made these tracks remain mysterious. That said, in my new paper, I have - finally - formalised a case for a Late Cretaceous Mexican set of tracks and possible feeding traces (panel D, above) having an azhdarchid trace maker.

Pterosaur feeding evidence: the 'close, but no biscuit' specimens

Inferring palaeoecological details from fossils can be tricky, and it is unsurprising that some purported insights into pterosaur diets and lifestyles are contentious. One of these is the famous and perhaps darkly comic circumstances surrounding the holotype skull and mandible of Ludodactylus sibbicki, a Cretaceous, likely fish-eating Brazilian ornithocheirid found with a sharp, pointed leaf between its lower jaw rami (panel F in the image above). Much of the 2003 description of this specimen (Frey et al. 2003) discusses this association and concludes that ingestion of these plant remains led to the death of the pterosaur. According to this story, the pterosaur accidentally scooped up the leaf, having mistaking it for its usual prey, stabbed the plant material on its throat tissues, frayed the end of the leaf trying to work it loose, but starved to death before it could dislodge it.

I must admit a little scepticism about this scenario. This is not because animals getting things stuck in their mouths is implausible, but because the story presented by Frey and colleagues is pretty presumptive. It infers a lot about pterosaur behaviour, foraging strategies, throat tissue strength and so on that we can't confirm at present. Moreover, the hyoid apparatus - the skeletal support for much of the throat and tongue tissue - is preserved lying on top of the leaf, despite the suggestion that the plant matter was deeply imbedded in the throat tissues. How did that work itself loose with the leaf fatally stabbed between the jaws? The answer to that question - as with a lot of questions about this association - would easily fall into speculation and special pleading about all manner of unknown quantities, and thus has little value to understanding fossil animal palaeobiology. Boring and po-faced as it is, I don't think the unusual Ludodactylus holotype provides enough information to tell us much about pterosaur behaviour, or how this unlikely fossil association came to be.

A similar observation might be made about insect specimens - a dragonfly and lacewing - from the Jurassic Solnhofen Limestone that have torn wings, allegedly from a pterosaur attack (Tischlinger 2000). The logic goes that these otherwise perfectly preserved insects cannot have been attacked by aquatic predators, or else they would have been eaten after their wings were damaged. Failed attack from an airborne predator that would not pursue the injured insects into water is suggested as more likely. Solnhofen deposits do hold pterosaurs that were almost certainly aerial insect hawkers - such as Anurognathus (below, see Bennett 2007 and Witton 2013) - and these might be ideal perpetrators in this scenario.

Anurognathus ammoni was an insect-hawking pterosaur that lived over the Solnhofen lagoon. Has it left feeding traces on fossil insect wings after a failed attack?

 As with Ludodactylus, this set of circumstances is quite elaborate to base purely on damaged insect wings. The extent of their wing damage is considerably greater than we might expect under general 'wear and tear' and foul play was probably involved, but whether it was a pterosaur, a conspecific, or even those disregarded aquatic predators is difficult to say. I appreciate the logic that aquatic predators would eat disabled insects after a failed strike, but animals are not predictable, logic-driven machines: they make mistakes, strike at things they have no intention of eating, get bored, distracted and so on. In all, other than the fact that these insects were almost certainly attacked by something, it might be difficult to say anything more substantial about their final moments.

Pterosaurs vs. dinosaurs, crocodyliforms and... the revenge of the fish

The fossil record gives us an insight on the question "did pterosaurs taste good?", and that answer seems to be "yes". Bite marks, embedded teeth and vomited pterosaur remains indicate that dinosaurs, crocodyliforms and fish all ate pterosaur flesh, at least on occasion (below). Among the more impressive examples of these interactions is a spinosaurid tooth, likely from the Brazilian spinosaurine Irritator challengeri, embedded in the cervical vertebra of an ornithocheirid (Buffetaut et al. 2004). Alas, no other evidence of their interaction was evident on the specimen (a series of pterosaur vertebrae) and it's not possible to ascertain much about circumstances that brought these species together.

Evidence of many, many things that ate pterosaurs. A, ornithocheirid cervical vertebrae with embedded spinosaurid tooth; B, azhdarchid tibia with tooth gouges and embedded dromaeosaur tooth; C, ornithocheiroid wing metacarpal with unidentified puncture marks; D, Quetzalcoatlus sp. skull with puncture marks; E, Eurazhdarcho langendorfensis cervical vertebrae with crocodyliform puncture marks; F, Pteranodon sp. cervical vertebra with intimately associated Cretoxyrhina mantelli tooth; G, Velociraptor mongoliensis torso with possible azhdarchid pterosaur gut content; H, probable fish gut regurgitate including Rhamphorhynchus bones; I, associated Rhamphorhynchus muensteri and Aspidorhynchus acutirostris skeletons. Images drawn and borrowed from many sources - see Witton 2017 for details.

The fossil record's most common purveyors of pterosaur murder, however, are not dinosaurs or crocodyliforms, but fish. Apparently out for revenge after learning of all that fishy pterosaur gut content, we've got evidence of fish eating and spitting out pterosaurs, of pterosaurs getting entangled with piscine predators, and even fish bite marks on pterosaur bones. A lot of these pertain to specimens of Rhamphorhynchus and you can read more about them in this post - some of the specimens are exceptional and there's lots to say about them. One of the more famous examples of piscine-pterosaur consumption -  an Italian, Triassic pellet composed of alleged pterosaur bones (Dalla Vecchia et al. 1989) - has recently been reappraised. It's now more reliably interpreted as vomit ball made of bones from the tanystropheid Langobardisaurus (Holgado et al. 2015).

Lesser known, but pretty darned awesome examples of fishes eating pterosaurs are Pteranodon specimens that found themselves at the wrong end of Cretaceous sharks. Several Pteranodon bones reveal bite marks and even embedded teeth from two genera of sharks, the 2-3 m long 'crow shark' Squalicorax and the larger, 6 m long 'ginsu shark', Cretoxyrhina. The former seems to have eaten Pteranodon flesh on several occasions, while evidence of the latter is only currently known from a tooth closely associated with a cervical vertebra (panel F, above). Further work on the latter specimen is currently underway.

 Feeding traces from these sharks are common in Western Interior Seaway fossils and those of Squalicorax are particularly abundant and taxonomically indiscriminate. Given that even giant marine reptiles are among the species consumed by this mid-sized shark, it's often assumed that this animal was a scavenger, biting into whatever free meat floated about America's continental sea. However, it is less certain that Pteranodon was scavenged by Squalicorax, as even a 2 m long specimen would vastly outweigh the largest Pteranodon. It is not inconceivable that an unwary Pteranodon could be grabbed and killed by a stealthy Squalicorax, though I stress this scenario is no better supported than the shark simply chancing across a Pteranodon carcass. Whatever the scenario, it's somewhat grounding to think of a weird extinct creature like a pterosaur being devoured by a fairly conventional-looking shark. It's a reminder, perhaps, that Mesozoic life was not a pantomime of exotic, giant reptiles and weirdo evolutionary experiments, and that much of our modern ecosystem was in place many millions of years ago.

The big picture

Looking at the pterosaur palaeoecological record holistically, what patterns emerge? If we look at where the record focuses phylogenetically (below), it's obvious that our records are significantly biased towards certain taxa - Pteranodon, Rhamphorhynchus, and azhdarchids. Even their close relatives, with similar anatomy and adaptations, preservational conditions and so on, don't get much of a look in. There's a few data points scattered here and there, but tumbleweeds run though the palaeoecological data stores for the majority of the group.

Attempting to make sense of the pterosaur palaeoecological record in a holistic way mainly shows how paltry this record remains. It's improved a lot in recent years, but we await evidence of diet and consumer-consumed relationships in virtually all major pterosaur clades. The images at the bottom of this figure are takes on known examples of pterosaur ecology: Rhamphorhynchus ingesting fish, and azhdarchids being devoured by dromaeosaurs. From Witton (2017).

We wouldn't be scientists if we didn't ask ourselves why this is. I don't think it's simply a sampling issue. The pterosaur record is not great, but we are talking about several thousand specimens now - enough that we might start looking at what we don't have as well as what we do. So why does Rhamphorhynchus show 10 palaeoecologically-relevant fossils, but other Solnhofen species only preserve one confirmed piece of gut content? Why do azhdarchids, which are never found in sites of exception preservation and are generally only known from bits and pieces, have a better record than those lineages which are abundant, represented by dozens of complete skeletons, and often found in sites of exceptional preservation? Interestingly, there's no obvious correlation between factors like abundance, preservation quality and palaeoecological data. Several lineages - the ctenochasmatoids (wading pterodactyloids), the rhamphorhynchids (excluding Rhamphorhynchus) and ornithocheiroids (excluding Pteranodon) - have everything going for them in terms of abundant fossils, occurrences in sites of exceptional preservation, and yet they turn up very little in the way of gut content, or evidence of being consumed by other Mesozoic animals.

My take on all this is that there must other factors at play here. We don't get evidence of pterosaur palaeoecology just by throwing more fossils, or better quality fossils, into the mix. I'm sure these factors have some role, but perhaps only in concert with special traits of certain pterosaur groups - maybe behaviours and anatomies - that allow them to have good records. We might have a good record of azhdarchids being consumed by dinosaurs and crocs, for instance, because their bones are often quite big and allow predators to bite them without destroying them. Perhaps we have good palaeoecological insights for Rhamphorhynchus and Pternanodon because of their habits and behaviour - both have strong aquatic adaptations (see this blog post for ideas on that), and there is a bias towards preservation of aquatic animals in the fossil record. Perhaps this aids preservation of not only palaeoecological data, but also explains why these taxa are our most abundant pterosaurs (>100 Rhamphorhynchus fossils are known, >1000 Pteranodon).

The pterosaur palaeoecological record, then, is perhaps in a transformative state. Though vastly improved over its condition a few decades ago, it requires further augmentation to provide us with significant insights into pterosaur lifestyles, and to explain its biased nature. However, we should not be too pessimistic about the insight it offers into pterosaur palaeobiology: it still provides useful datapoints that can shape our interpretation of flying reptile ecology for several species. Cliched as it is, the take-home message of this project is that any palaeoecologically-relevant pterosaur fossils are worth putting on record. We still have a lot to learn about how these animals lived and behaved, and direct insights are the most reliable ways to do that.

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