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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References

• Bennett, S. C. (2007). A second specimen of the pterosaur Anurognathus ammoni. Paläontologische Zeitschrift, 81(4), 376-398.
• Buffetaut, E., Martill, D., & Escuillié, F. (2004). Pterosaurs as part of a spinosaur diet. Nature, 430(6995), 33-33.
• Dalla Vecchia, F. M., Muscio, G., & Wild, R. (1989). Pterosaur remains in a gastric pellet from the Upper Triassic (Norian) of Rio Seazza valley (Udine, Italy). Gortania, 10(1988), 121-132.
• Frey, E., Martill, D. M., & Buchy, M. C. (2003). A new crested ornithocheirid from the Lower Cretaceous of northeastern Brazil and the unusual death of an unusual pterosaur. Geological Society, London, Special Publications, 217(1), 55-63.
• Holgado, B., Dalla Vecchia, F. M., Fortuny, J., Bernardini, F., & Tuniz, C. (2015). A reappraisal of the purported gastric pellet with pterosaurian bones from the Upper Triassic of Italy. PloS one, 10(11), e0141275.
• Martin-Silverstone, E., Glasier, J. R. N., Acorn, J. H., Mohr, S. & Currie, P. J. (2017). Reassesment of Dawndraco kanzai Kellner, 2010 and reassignment of the type specimen to Pteranodon sternbergi Harksen, 1966. Vertebrate Anatomy Morphology Palaeontology, 3, 47–59.
• Tischlinger, H. (2001). Bemerkungen zur Insekten-Taphonomie der Solnhofen Plattenkalke. Archaeopteryx, 19, 29-44.
• Wellnhofer, P. (1991). The illustrated encyclopedia of pterosaurs. Salamander Books.
• Witton, M. P. (2013). Pterosaurs: natural history, evolution, anatomy. Princeton University Press.
• Witton, M. P. (2017). Pterosaurs in Mesozoic food webs: a review of fossil evidence. Geological Society, London, Special Publications, 455, SP455-3.