New paper: walking with early pterosaurs

Non-pterodactyloids like Dimorphodon macronyx are meant to be slow, sprawling terrestrial locomotors. So what's up with this image of one running with erect limbs? Read on... Prints of this image are available.

Readers interested in flying reptiles will know that a recent, major paradigm shift in our understanding of these animals concerns their terrestrial locomotion. In short, perceptions of pterosaurs as awkward, clumsy terrestrial creatures have been overturned to models of upright, proficient walkers and runners. This reinterpretation is founded on a substantial amount of evidence from skeletal anatomy, trackway data, as well as reconstructions of muscle kinematics, and underpinned recent proposals of terrestrial foraging in some pterosaurs (most famously of course, the azhdarchids - read this for an overview of their research history) - famously stark departures from classic views of pterosaur palaeobiology. However, it is really only pterodactyloids, that group of Jurassic-Cretaceous pterosaurs which contains the majority of pterosaur diversity, that much of this work on terrestriality really applies to. It seems all pterosaur tracks are actually pterodactyloid tracks; most 3D fossils we've used to understand limb joints and motion are pterodactyloid fossils, and most detailed discussions of step cycles, stride lengths and so on are based on pterodactyloid proportions.

Non-pterodactyloids are considered somewhat differently. Our views on early pterosaur walking and running are less researched and more controversial than those of pterodactyloids, and we've seen several ideas on this topic emerge since the 1980s. These include non-pterodactyloids as bird-like bipeds (briefly discussed here); as slow and terrestrially ineffective lizard-like quadrupeds; as quadrupeds which were adept climbers; or quadrupeds with sprawling forelimbs but erect hindlimbs, which had to run bipedally. From these, the notion of early pterosaurs as particularly laboured terrestrial locomotors has emerged dominant. In several cases, this perception has been important when interpreting pterosaur history and biology: how early pterosaurs foraged, their roles in Mesozoic ecosystems, and patterns in their fossil record have all factored in the terrestrial ineptitude of the first flying reptiles (e.g. Unwin 2005; Ősi 2011; Butler et al. 2013). There are three core assumptions forming the foundation of non-pterodactyloid terrestrial incompetency:

1. The broad, hindlimb-spanning membrane (uropatagium) of early pterosaurs 'shackled' their hindlimbs, preventing anything but slow, shuffling gaits
2. The absence of pterosaur tracks before the Middle Jurassic demonstrates that these animals rarely walked, allegedly because they were so awful at it
3. The sprawled limbs of pterosaurs made quadrupedal terrestrial locomotion slow and difficult. 

Pterodactyloids, with their fully erect limbs and split uropatagia, freed themselves from these constraints and 'terrestrialised' the group, leading to the formation of a track record which roughly corresponds to the earliest occurrences of pterodactyloid remains.

All this sounds fine, until the realisation hits that many of these assumptions are on somewhat shaky logical ground. Indeed, available data and well-known specimens can be used to undermine them to the extent that we might want to reconsider the whole 'terrestrially inept non-pterodactyloid' concept. In a new paper, published this week in PeerJ, I've attempted to do just that, outlining how we probably know a lot less about the terrestrial prospects of non-pterodactyloids than some suggest, and that some of our chief assumptions about these animals may very well be incorrect. Being a PeerJ paper means you can read the whole thing for yourself, for free (along with the review history) but let's summarise the main points here, tackling each of the points raised above in turn.

1. Large hindlimb membranes ‘shackled’ early pterosaur legs

Pterosaur and bat uropatagia compared. A, tracing of Sordes pilosus fossil, showing one of our best known uropatagia specimens; B, reconstruction of Rhamphorhynchus skeleton, mapped out with likely membrane distributions for non-pterodactyloids; C, terrestrially-competent vampire species Desmodus rotundus, complete with uropatagium rather like that of non-pterodactyloids. From Witton (2015).

Notions that the proportionally large hindlimb membrane of early pterosaurs (above) would impede terrestrial locomotion are not based on much in the way of detailed analysis of pterosaur soft-tissues. It really is just the size of the membrane, and the fact it was anchored extensively across the leg and fifth toes, which suggests it impeded terrestrial activity. Evidence that this membrane was particularly stiff or unyielding has not been presented, unlike other parts of pterosaur wings, which seem to have been stiffened and reinforced by long fibres. To the contrary, several workers have suggested that pterosaur uropatagia were probably as elastic as other membrane tissues close to the pterosaur body (Unwin and Bakhurina 1994) – those which were flexible enough to permit huge strides and running behaviours recorded in pterosaur trackways. In light of this, suggestions that this organ 'shackled' their hindlimbs seem a bit odd.

Moreover, there are plenty of modern animals with analogous uropatagial structures which locomote terrestrially without problem – examples include several bats with terrestrial capabilities described as being ‘rodent-like’. Many of them even make habits of grounded foraging, digging, crevice-crawling, running, climbing and other complex behaviours. All this occurs without their membranes being damaged, snagged or being otherwise restricting locomotion. Much of this is aided, it seems, by uropatagia being elastic, shrinking away when their limbs are not in flight configuration. Of course, there are some animals with large hindlimb membranes which aren’t particularly hot on the ground, but zoologists have labelled aspects of limb strength and myology as more important here than membrane size. This seems to be a second complication for the idea that large uropatagia were problematic for walking in the way suggested by some pterosaur workers. In concert with what we know of pterosaur membrane anatomy, I'm left wondering what, if any, deleterious effect non-pterodactyloid hindlimb membranes had on their terrestrial prospects.

2. Trackways = terrestrial proficiency

Revised locomotion in tyrant dinosaurs, ceratopsids and mammaliaforms, brought to you by the 'no footprints = terrestrial competency' hypothesis.

Of course, no-one thinks the lack of footprints in these groups is anything to do with terrestrial competency. The fossil record is full of strange quirks reflecting a secret recipe of ancient animal behaviours, taphonomy, sampling, interpretation, and plain serendipity, so scare track data may have no significance at all. Or it might. We don't know, because we can't account for all variables. But that doesn't matter, because what we can do is use available data - that of limb functionality - to draw conclusions about the terrestrial prospects of these groups. That has to trump an absent track record, because we cannot test the significance of our conclusions on a negative dataset. Until we know more about early pterosaur functionality, ascribing the absence of a footprint record to their terrestrial capacity is probably getting ahead of ourselves, and puts the approach of pterosaur researchers at odds with other branches of vertebrate palaeontology.

3.All non-pterodactyloids had sprawling forelimbs

Tying this all together