Friday, 19 June 2015

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

I must admit some surprise that a number of pterosaur workers consider trackway presence and abundance to correlate with terrestrial competency. This is especially so because it is widely acknowledged that the pterosaur fossil record, and that of early pterosaurs in particular, is generally poor. This is not to say that a deficit of early pterosaur tracks is definitely meaningless, but negative evidence is only significant when all other factors are accounted for. To appreciate the deficit of early pterosaur tracks as significant, we’d ideally want to have a good understanding of pterosaur ecology and behaviour, as well as their abundances in habitats suitable to track making. Neither of these are the case at present. Moreover, the track records of many Mesozoic animals are poor, even those which, on paper, have vastly greater track-making potential than early pterosaurs. Examples include widely distributed, entirely terrestrial clades like certain dinosaurs, crocodylomorphs, and mammaliaforms. Even relatively recent, large bodied terrestrial animals – like ceratopsids and tyrannosaurs – have track occurrences countable on the digits of one hand, despite their increased bulk ensuring that they leave deeper, long-lasting and theoretically more-preservable prints. Needless to say, applying 'pterosaur logic' to these animals - assuming that they avoided making tracks because of terrestrial ineptitude, and were reliant on other means of transportation - leads to some... interesting ideas on other potential forms of locomotion.

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

I’m going to cut to the chase here by pointing out that evidence for sprawling pterosaur hindlimbs is not especially strong – most arguments made to support it are now a little old-school, to the extent that they conflict with modern approaches to assessing limb joint function. There’s been a lot of work done on pterosaur hindlimb posture and it seems all flying reptiles had at least upright hindquarters - let's leave that there. But what about sprawling forelimbs? Certainly some early pterosaurs – specifically rhamphorhynchines, and probably ‘campylognathoidids’ - had to sprawl, because their glenoids (shoulder joints) restricted movement of the humerus below the shoulder itself. Their articular surface allows for plenty of room for movement above the shoulder, and some room for fore-and-aft motion, but a large bony ridge prohibits the forelimb adopting anything like an upright pose. This isn't controversial: several authors have already noticed this.

However, several non-pterodactyloid specimens seem to have rather different glenoid morphologies to those of rhamprhorhynchines and 'campylognathoidids'. Species like Dimorphodon macronyx, and perhaps some wukongopterids, have shoulder girdles which lack that ventrally-restrictive bony stop. Instead, their glenoids which are ventrally open, the articular surfaces wrapping around the underside of the glenoid body to meet the shoulder girdle itself rather than a jut of bone. This morphology is borne out by several three-dimensional Dimorphodon glenoid specimens and is unlikely to represent chance distortion of a glenoid into a more 'open' morphology. These specimens seem to indicate that at least some early pterosaurs were capable of tucking their forelimbs underneath their bodies.

Variation in early pterosaur shoulder girdles. Images on the left shown the shoulder joint of Dimorphodon macronyx - note how the (shaded) articular surface extends to the underside of the glenoid (bottom image, and left photograph) to make a ventrally-open shoulder joint. By contrast, the glenoids of certain other non-pterodactyloids (images top right) have articular surfaces only on the dorsal and lateral glenoid surface: the ventral is blocked by a bony ridge. In this morph, the humerus clearly cannot rotate much beneath the shoulder at all. A schematic of the ranges of motion offered by these two shoulder types is shown at bottom right. From Witton (2015).
It’s not a given, however, that the ability to fully adduct a limb correlates with a habitually upright stance: range of motion alone tells us little about habitual joint postures. Is there anything in early pterosaur anatomy to suggest which forelimb postures these animals preferred? Potentially, yes: the end of their humeri. Recent work on the forelimbs of quadrupedal tetrapods has identified anatomical correlates of routine sprawling and erect postures in elbow skeletons (Fujiwara and Hutchinson 2012). Because these joints have to take the strain of standing, different poses emphasise the development of characteristic muscle groups and their corresponding bony attachment sites. Having positively tested this thoroughly on modern animals, we can start to use it on fossil ones, including pterosaurs. Fujiwara and Hutchinson (2012) have already looked at pterodactyloid humeri and suggest they have all the right features for an upright limb. Ergo, if we see pterodactyloid-like humeral morphologies in earlier pterosaurs, they might have had upright limbs, too.

Pterosaur humeri in anterior view, showing variation in distal humeral shape in non-pterodactyloids (A–F) and pterodactyloids (G–I). A-B, Dimorphodon macronyx; C, Archaeoistiodactylus linglongtaensis (a likely wukongopterd); D, Rhamphorhynchus muensteri; E-F, Dorygnathus banthensis; G, Pteranodon sp; H, Montanazhdarcho minor; I, Dsungaripterus weii. Note how Dimorphodon and Archaeoistiodactylus are far more pterodactyloid like in humeral morphology than Rhamphorhynchus or Dorygnathus: does this implicate erect limbs in some early pterosaur species? Scale bars represent 10 mm, except for G and H, which equal 50 mm. From Witton (2015).
As with shoulder anatomy, it turns out there some potentially significant variation here. Rhamphorhynchines and (probably) 'campylognathoidids' - taxa seemingly confined to sprawling - have humeri which are quite different from those of pterodactyloids. Their elbows are very narrow, being little wider than the condyles necessary to articulate the forearm. This fits well with the predictions of Fujiwara and Hutchinson, because we would expect pterosaurs confined to sprawling to have different anatomy to tall-standing pterodactyloids. Dimorphodon and wukongopterids - those pterosaurs with less restrictive shoulder joints - have a different elbow anatomy however: a distal humerus which is broadly expanded beyond the margins of the forearm articulations. In virtually all details, these humeri have distal ends very similar to what we see in pterodactyloids and, all else being equal, that might imply a similar loading regime at their elbows. We might take this an an indication that upright postures were adopted regularly in these non-pterodactyloids, which marries nicely with observations made about their ability to tuck their forelimbs under their bodies. The idea that Dimorphodon and wukongopterids were also sprawlers is less parsimonious because we have to explain why some early pterosaur humeri don’t resemble those of obligate sprawlers, but instead look so similar to those of pterosaurs we’re confident had erect forelimbs.

This observation might be quite significant for considerations of terrestrial abilities in early pterosaurs. Sprawling postures are not as restrictive to locomotion as some pterosaur literature suggests (sprawling does not limit its users to slow crawling, and is actually quite useful for certain habits, like climbing or accelerating quickly), but there might be something to the idea that upright locomotion is better for sustained, active terrestrial habits. Indications that the likes of Dimorphodon and wukongopterids were capable of walking on fully erect limbs, without impedance from their uropatagia, suggest they have greater terrestrial potential than previously anticipated. Perhaps our views on the likely habits of non-pterodactyloids might benefit from further research.

Further indications of terrestriality?

The possibility that some early pterosaurs had erect forelimbs is only one indication that these taxa may have been more terrestrially adept than we’ve previously considered. I think our views on these animals have been biased by the familiarity of taxa like Rhamphorhynchus: these sprawling, slender-limbed species with oversize forelimbs don’t look like the hottest terrestrial locomotors in town (see Dorygnathus illustration, below), and this perception may have bled into our consideration of non-pterodactyloids as a whole. In actuality, taxa like Dimorphodon, Preondactylus, anurognathids and others have pretty chunky, proportionate limbs: we could take their wing fingers away and they still look capable of looking after themselves using terrestrial locomotion alone. Several authors have noted features indicative of strong running and leaping abilities in early pterosaur hindlimbs, and this might apply to their forelimbs too.

It’s also intriguing to note that some features found in pterosaur digits – sesamoids immediately above and behind their claws – are only otherwise found in terrestrial reptiles (lots of squamates and one fossil stem-turtle, Proganochelys). No-one seems to know exactly what function these antungual sesamoids perform, but I've speculated that they are related to claw contact with hard surfaces. Sesamoids seem to mostly offer two functions: enhancing joint leverage or protecting tendons from extremes of motion. Claws routinely deflected backwards by contact with substrata might necessitate a bony element in the tendon to ensure nutrient flow to the tendon is maintained, or else to facilitate better leverage when actively hyperextending claws to prevent claw blunting. It's difficult to think what else a sesamoid above and behind a claw can really help with, especially given their occurrence in animals as different as pterosaurs, lizards and a stem-turtle. I'm not the first to suggest pterosaurs could retract their claws (Frey et al. 2003), and some sort of hyperextension would explain the large digital articular surfaces seen in pterosaurs with antungual sesamoids compared to those lacking them. Again, there is clearly need for more research here, but the take-home is that this anatomical aspect of non-pterodactyloids is only mirrored in terrestrial animals, and might present another feature signifying greater terrestriality than expected in early pterosaurs.

Tying this all together

A 'traditional' view of a non-pterodactyloid standing posture: Dorygnathus banthensis with sprawling forelimbs. How the development of this feature fits into pterosaur evolution remains to be seen: earlier pterosaurs (both stratigraphically and phylogenetically) may have stood quite differently. Prints of this image are available.
It's noteworthy that features proposed as potentially signifying terrestriality in early pterosaurs are not neatly mappable to any current concept of non-pterodactyloid phylogeny. Even comparatively simple models of early pterosaur evolution show complex changes in shoulder girdle morphs, humeral anatomy and and limb robustness as we trace evolutionary pathways up the tree. Nevertheless, the potential for upright postures, running behaviours and other features of proficient terrestriality seem deeply rooted in Pterosauria because some of the oldest, 'most basal' pterosaurs possess such indicative anatomy. A lot of what is said here complements ideas already in pterosaur literature. To use a well-studied example, there are lots of hints that the Lower Jurassic Dimorphodon was terrestrially adapted: it seems proportionally heavy to the extent of impeding flight potential, has been strongly suggested to have a diet of insects and small vertebrates, and has a suite of features suited to climbing (see the previous post). Combine these with the possibility of erect limbs, subcursorial limb proportions, robust extremities and so on, and we've got a pretty good argument for Dimorphodon being terrestrially competent, and maybe even adapted for a primarily terrestrial existence. It's hard to think of a lifestyle more opposing to traditional interpretations of non-pterodactyloid palaeobiology than that, but a multitude of disparate research projects seem to be collectively pointing that way.

In all, my point for writing this synthesis paper is to demonstrate how little we've really looked into the terrestrial prospects of early pterosaur species. If even basic variation in their limb arthrology remain poorly studied, how can we claim to understand their terrestrial prospects or plug our models into our Big Picture of Pterosaur Evolution? Even if everything I've said here ends up being challenged, I hope at least this new paper stimulates some detailed research into this rather poorly explored area of pterosaurology. Until that happens, my suggestion is that we avoid blanket-statements about the terrestrial prospects of non-pterodactyloids.

Those interested in early pterosaur funky morph might be interested to know that I'm talking about the flight performance of Dimorphodon at Flugsaurier 2015. Registration is open until 30th June, so get your interest registered quickly!


  • Butler, R. J., Benson, R. B., & Barrett, P. M. (2013). Pterosaur diversity: Untangling the influence of sampling biases, Lagerstätten, and genuine biodiversity signals. Palaeogeography, Palaeoclimatology, Palaeoecology, 372, 78-87.
  • 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.
  • Fujiwara, S. I., & Hutchinson, J. R. (2012). Elbow joint adductor moment arm as an indicator of forelimb posture in extinct quadrupedal tetrapods. Proceedings of the Royal Society of London B: Biological Sciences, 279(1738), 2561-2570.
  • Ősi, A. (2011). Feeding‐related characters in basal pterosaurs: implications for jaw mechanism, dental function and diet. Lethaia, 44(2), 136-152.
  • Unwin, D. M. (2005) The pterosaurs from deep time. Pi Press.
  • Uwnin, D. M., & Bakhurina, N. (1994). Sordes pilosus and the nature of the pterosaur flight apparatus. Nature, 371(6492), 62-64.
  • Witton, M. P. (2015). Were early pterosaurs inept terrestrial locomotors? PeerJ 3:e1018; DOI 10.7717/peerj.1018


  1. infinitely cool. Methinks an animated reconstruction in witton look is called for

    "In light this, suggestions that this organ 'shackled' their hindlimbs seem a bit odd."
    In light OF this...

    1. Thanks for the typo spot - proof reading remains something of a personal Achilles heel.

      An animated, erect-limbed Dimorphodon would be awesome!

  2. That’s why we find so many flightless Pterosaur & Bat species?

  3. "sprawling does not limit its users to slow crawling, and is actually quite useful for certain habits, like climbing or accelerating quickly"

    I can appreciate how sprawling rather than having limbs tucked under would help with climbing, but why would it enable quick acceleration? That's not obvious to me.

    1. Possibly more torque with propulsion points more proximal to the nosy mass? Example think about how much easier it is to hold a weight close to your chest or side than it is to hold it up with your arm outstretched. The same physical principle would apply to accelerating. Moles have short and robust limbs for power rather than gracile limbs, like a rabbit for example.

  4. Excellent summary of a very interesting paper. Possible other advantages to an enhance terrestrial lifestyle in addition to ones you mentioned may be; burrowing and shelter seeking, egg deposition/burying, better access to water and aquatic food sources, and general reduction in the expenditure of energy since flight or more specifically launching into fight is very energy consuming.