Regular Tet Zoo readers will be familiar with azhdarchid pterosaurs and the debate that’s surrounded their ecology and behaviour. Within recent decades, these remarkable, often gigantic, long-necked, long-billed but proportionally short-winged toothless Cretaceous pterosaurs have been imagined as ‘mega-skimmers’, as heron-like waders, as obligate scavengers of dinosaur carcasses, and even as sandpiper-like littoral foragers.

All of these ideas are highly flawed if not nonsensical, since they’re inconsistent with the anatomy of these pterosaurs and simply fail to take account of (and even credit) the numerous anatomical features that correlate with those lifestyles in extant animals.

Back in 2008, Mark Witton and I argued that azhdarchids possess a suite of anatomical features that make it most likely that they were terrestrial stalkers: that is, that – while they were adept, specialised soarers, great at rapidly covering extraordinary distances – they seemingly foraged on foot in both wooded and open terrestrial environments, walking quadrupedally with an efficient, narrow gait, reaching down with their long necks and bills to grab small animals, bits of carrion and perhaps fruits and other edible bits of plants (Witton & Naish 2008). Azhdarchids don’t have any precise modern analogues, but we suggested that their behaviour and lifestyle most closely resembled that of modern ground hornbills and terrestrial-foraging populations of marabou stork. [Adjacent ground hornbill photo - I really, really love the composition of this image - by Rod Waddington.]

This view of terrestrial stalking azhdarchids receives support from the anatomy and proportions of these animals, from the environments and animal communities in which their remains are preserved, and from trackway evidence (there’s a long, continuous trackway preserved in Upper Cretaceous Korean sediments, seemingly made by a quadrupedally walking azhdarchid*) (Witton & Naish 2008).

* A trackway argued to have been produced by a bipedal giant azhdarchid was recently published. There are some issues with the conclusions of this study. Stay tuned.

If you need a refresher on any of this, check out the articles linked to below – there’s quite a bit on azhdarchids in the Tet Zoo archives, plus the Witton & Naish (2008) paper is open-access and available to all.

The terrestrial stalking hypothesis has been reasonably well received within the pterosaur research community and at least a few of our colleagues have said nice things about it. New data on Romanian azhdarchids supports the view that these were animals of continental environments where they were sharing habitats with dinosaurs and other animals uncontroversially associated with inland, terrestrial places (Vremir et al. 2013). New information on the azhdarchid hand is also consistent with the terrestrial stalking hypothesis, since it indicates specialisation for regular terrestrial walking on firm substrates (Carroll 2013, Carroll et al. 2013). Incidentally, terrestrial stalking azhdarchids were featured in the David Attenborough Flying Monsters 3D documentary and (I believe) the hypothesis also gets credited in the new Walking With Dinosaurs 3D movie… which, of course, is now utterly ruined by the fact that the dinosaurs talk. Good work, guys.

The terrestrial stalking model: challenged!

However, if there’s one thing I’ve learnt about human nature, it’s that people will refuse to give up on poorly supported and even nonsense ideas, even when there’s strong or overwhelming evidence to the contrary. So there are still people supporting the idea of water-trawling azhdarchids and wading azhdarchids and so on. In recent months, two challenges to the terrestrial stalking hypothesis have appeared.

The first (I want to spend as little time as possible on this one) comes from the indefatigable David Peters. Peters challenged our hypothesis by posting a comment at PLoS (that’s right, a 2013 comment on an article published in 2008. Weird): he pointed to his own highly suspect phylogenetic results to support the idea that azhdarchids descended from “petite” “micro-azhdarchids” that, in his view, were most likely waders, and he also challenged the idea that azhdarchids look at all like ground hornbills. Mark and I responded (and then responded again, when he responded to our response): you can read the entire chain of correspondence here.

The second challenge was made by Alexander Averianov in a paper mostly devoted to a discussion of neck mobility in the Central Asian azhdarchid Azhdarcho lancicollis (Averianov 2013). Much of the paper is very interesting, since Averianov postulated the range of motion possible in Azhdarcho’s neck, concluding that – while motion was limited – the neck was probably less stiff and straight than usually thought, there being enough flexibility to allow easy contact of the jaw tips with the ground. There are some issues with his conclusions on neck flexibility, but that's an argument for another time.

Anyway, in the rest of his paper, Averianov (2013) presented three main arguments against the terrestrial stalking hypothesis. He claimed that: (1) azhdarchid fossils might come from continental places, but they’re always associated with sediments deposited in aquatic habitats, and, hence, azhdarchids most likely were aquatic foragers of some sort; (2) claims of strong terrestriality in azhdarchids would require them to inhabit places where big, terrestrial theropods occurred, and this is surely untenable due to the danger these big predators would have presented to a grounded pterosaur; and (3) azhdarchids possess mandibular characters better consistent with the idea that they pulled the lower jaw through the water while in flight, catching prey in a mandibular pouch. In short, Averianov (2013) argued that azhdarchids should be interpreted as water-trawling ‘skimming pelicans’, not as terrestrial stalkers. This is a… novel way of imagining azhdarchids, and (in my and Mark’s opinion) a very odd one.

When your own work is challenged, I consider it good practice to respond in print… unless, that is, that your argument or data really has been trounced. So Mark and I set about producing a response: we didn’t submit it to the same venue as Averianov’s (2013) original paper (Paleontological Journal) because (when possible) we use open access journals. Rather, it was submitted to Acta Palaeontologica Polonica where it’s currently – technically – ‘In press’, and will be regarded as so for several more months yet (Witton & Naish 2013). It actually appeared online back in October but I haven’t had time to write about it until now.

So, what do we say? I don’t want to go into the whole argument in enormous depth, partly because Mark already covered it at his blog back in October and also because, again, you can read the full article yourself… it’s fully open-access. So let’s keep this short (Err.. that didn’t work out so well, sorry).

On the claim that azhdarchid fossils are always associated with sediments deposited in aquatic settings… note to start with that fossils are, across the board and across all taxa, most typically preserved in aquatic sediments. As we say in the paper, this is true of “fossil cattle, giraffes, primates, and perching birds” (Witton & Naish 2013, p. 4): it tells you little to nothing about lifestyle. In any case, Averianov’s generalisation is misleading, since there are azhdarchid fossils from volcanic rocks and even from sediments deposited in deserts. Do these support strong ecological ties to an aquatic lifestyle? No. We think it significant that azhdarchid fossils often come from arid places; in fact, some of the geological locations that yield the highest number and greatest diversity of azhdarchids represent dry, terrestrially exposed environments (Witton & Naish 2013).

Shock horror: you can probably walk around in the Mesozoic without being eaten!!

Averianov’s second point is that azhdarchids would be too vulnerable to terrestrial predation to permit a lifestyle dedicated to terrestrial foraging. Our response to this argument is perhaps the most novel part of our manuscript, since it allowed us to say a lot about Mesozoic ecology and animal behaviour that people don’t say often enough.

For starters, the idea being promoted here is that the Mesozoic was so over-run with rapacious uber-predators that vulnerable animals would surely be snatched up and devoured instantaneously. While environments frequented by big animals are, to a degree, potentially dangerous, the fact is that animals of all sorts – hypothetical time-travelling humans included – could certainly wander about the habitats of the Cretaceous world without being instantly grabbed, disemboweled, consumed, torn limb from limb, or swallowed whole. Predators, even big ones, aren’t on the prowl constantly, they don’t live everywhere, and they might even ignore or avoid unfamiliar, formidable or awkward animals that might otherwise look like potential prey. This goes for the modern world as well as the Cretaceous one.

Another point: most time we see Mesozoic predation events discussed or illustrated, it’s allosauroids taking on giant sauropods, tyrannosaurids fighting adult ceratopsians, and so on. People don’t make the point enough that predatory theropods – even the giant tyrannosaurids that Averianov had in mind – likely preferred cute little baby animals (Hone & Rauhut 2010) to big, gnarly, difficult-to-kill adult ones. So, not only were giant theropods not a constant, ubiquitous menace, we should also keep in mind the fact that they would have gone for easy, lazy meals whenever possible.

Azhdarchids: quite capable in a fight, thank you very much

And it’s important to note that azhdarchids were far from flimsy and helpless, as Averianov (2013) implied in his argument. The big ones really were big (shoulder heights of 2.5 m or so, head height of 4 m), had robust skulls and huge, pointed rostra more than 1 m long, and would have superficially recalled giant storks – a group of animals that are more than capable of defending themselves against big animals (witness the cases of Jabiru vs tapir, Jabiru vs human zookeeper, Marabou vs human child) (Witton & Naish 2013). [Adjacent photo by Nino Barbieri.]

Mark produced this excellent illustration (from Witton & Naish 2013) to show how a giant azhdarchid would compare to a giant theropod. Hopefully you get the point that we’re trying to make: even the biggest, badassest, hungriest Tyrannosaurus is (we not unreasonably assume) going to thing twice about tackling that azhdarchid, and it might well decide not to do so at all. Furthermore, some azhdarchids were the biggest predators in their ecosystems anyway – the biggest theropod living alongside Hatzegopteryx from Romania is Balaur, and it somehow seems doubtful that this 2-m-long maniraptoran was any kind of danger to the azhdarchid.

In short, Averianov’s (2013) contention that azhdarchids would have been too vulnerable to terrestrial predators to permit a terrestrial stalking lifestyle is highly arguable, and probably flat out wrong. Averianov (2013) also said that an azhdarchid would be unable to get quickly into flight when rapid escape was needed. Obviously, this ignores recent work on quadrupedal launching (Habib 2008, 2013, Witton and Habib 2010), all of which shows that azhdarchids could actually launch immediately into flight from a quadrupedal standing start.

Azhdarchids: water-trawling pelican-skimmer hybrids? Err, no

Finally, Averianov (2013) also contested the terrestrial stalking hypothesis by proposing that azhdarchids used their lower jaws as ‘scoop nets’: he specifically suggested that the form of azhdarchid jaw joints allowed these animals to expand the halves of the lower jaw outwards and then use the whole lower jaw (plus a throat sac) as a fish-catching scoop, employed in flight. In other words, he proposed that azhdarchids combined both a pelican-like use of the lower jaw with a Rynchops-like skimming habit. Hm.

We see quite a few problems with this proposal. Put simply, the form of the azhdarchid lower jaw is absolutely inconsistent with the idea of notable outward movement of the halves of the lower jaw, the very long mandibular (inflexible) symphysis would have incurred enormous drag if the lower jaw was trawled through the water, there’s no good reason to think that a throat sac was present (Witton & Naish 2013), and the whole idea of skim-feeding in pterosaurs is essentially untenable for functional and energetic reasons (Zusi 1962, Humphries et al. 2007, Witton & Naish 2008). For the full, detailed argument (we worked out the mandible and throat volume of both large and small azhdarchids and did other fancy calculations), do see the paper… did I mention that it’s open access?

Terrestrial stalking: support from multiple lines of evidence

The whole idea of terrestrial stalking azhdarchids can be considered multi-layered: Mark and I developed the hypothesis as we first saw a consistent pattern emerging from the form of azhdarchid skulls, proximal forelimb bones, wing-fingers, proximal hindlimb bones and feet, and from their overall, ‘pseudo-ungulate’ proportions (Witton & Naish 2008, 2013).

The sedimentological, geographical and environmental context of the azhdarchid fossil record adds strong additional support to our model, and trackway evidence adds soft tissue and postural data as further support (Witton & Naish 2008, 2013). Furthermore, azhdarchids lack the anatomical features you expect for the various other lifestyles that have been proposed for the group – they lack any and all features associated with skim-feeding, with sediment-probing, and with wading, for example. So, if somebody seriously wants to overturn the terrestrial stalking model, they have to come up with a model that better explains the several lines of evidence that we marshalled together. Thus far, that hasn’t happened.

As we approach the end of December, I begin to look back at all the stuff that happened during the year. 2013 wasn’t bad as goes my output on azhdarchids and their relatives, the azhdarchoids. Together with colleagues, I described the new Romanian azhdarchid Eurazhdarcho (Vremir et al. 2013), the small, Isle of Wight tapejarid-like Vectidraco (Naish et al. 2013), and of course published the paper on azhdarchid lifestyle and ecology that you’ve just been reading about. But, alas, there are several other projects that both Mark and I (with co-authors) presented at meetings, and which we simply weren’t able to get finished and published. They will appear eventually. If only we weren’t so lazy. Oh yeah: Mark also published a giant BOOK on pterosaurs. Ah yeah, about that...

For previous Tet Zoo articles on azhdarchids on other azhdarchoid pterosaurs, see...

Refs - -

Averianov, A. O. 2013. Reconstruction of the neck of Azhdarcho lancicollis and lifestyle of azhdarchids (Pterosauria, Azhdarchidae). Paleontological Journal 47, 203-209.

Carroll, N. 2013. Functional morphology of the azhdarchid manus. Journal of Vertebrate Paleontology 33, Supplement to Issue 3, 102A.

Carroll, N. R., Poust, A. W. and Varricchio, D. J. 2013. A third azhdarchid pterosaur from the Two Medicine Formation (Campanian) of Montana. In: Sayão, J. M., Costa, F. R., Bantim, R. A. M. & Kellner, A. W. A. International Symposium on Pterosaurs, Rio Ptero 2013, Short Communications. Universidad Federal do Rio de Janeiro: pp 40-42.

Habib, M. B. 2008.Comparative evidence for quadrupedal launch in pterosaurs. Zitteliana B28, 161-168.

- . 2013. Constraining the air giants: limits on size in flying animals as an example of constraint-based biomechanical theories of form. Biological Theory. doi: 10.1007/s13752-013-0118-y

Hone, D. W. & Rauhut, O. W. 2010. Feeding behaviour and bone utilization by theropod dinosaurs. Lethaia 43, 232-244.

Humphries, S., Bonser, R. H., Witton, M. P. & Martill, D. M. 2007. Did pterosaurs feed by skimming? Physical modelling and anatomical evaluation of an unusual feeding method. PLoS Biology 5: e204.

Naish, D., Simpson, M. I. & Dyke, G. J. 2013. A new small-bodied azhdarchoid pterosaur from the Lower Cretaceous of England and its implications for pterosaur anatomy, diversity and phylogeny. PLoS ONE 8: e58451.

Vremir, M., Kellner, A. W. A., Naish, D. & Dyke, G. J. 2013. A new azhdarchid pterosaur from the Late Cretaceous of the Transylvanian Basin, Romania: implications for azhdarchid diversity and distribution. PLoS ONE 8: e54268.

Witton, M. P. & Habib, M. B. 2010. On the size and flight diversity of giant pterosaurs, the use of birds as pterosaur analogues and comments on pterosaur flightlessness. PLoS ONE 5: e13982.

- . & Naish, D. 2008. A reappraisal of azhdarchid pterosaur functional morphology and paleoecology. PLoS ONE 3: e2271.

- . & Naish, D. 2013. Azhdarchid pterosaurs: water-trawling pelican mimics or “terrestrial stalkers”? Acta Palaeontologica Polonica doi:

Zusi, R. L. 1962. Structural adaptations of the head and neck in the black skimmer. Publications of the Nuttall Ornithological Club 3, 1-101.