Jaw gaping in Spinosaurus hinges on modern birds

A north African spinosaurine, with obvious nods to recent work suggesting some of these animals might've had short legs and a semi-aquatic lifestyle. The pterosaurs are azhdarchids, which are known to coexist with some African spinosaurines.

Honestly, I don't intend to cover every new paper which comes out on Spinosaurus. This fourth blog post, covering the third successive paper on this animal since 2014, is not the latest instalment of a stealthily-implemented new blog feature (check out this, this and this for previous non-instalments). Rather, north African spinosaurs are simply 'in' right now, hard to miss on palaeontological social media and the topic of widespread conversation - the dinosaur equivalent of skinny jeans, adult colouring books or whatever ITV runs on a Saturday night nowadays.

The latest paper on these animals is that of Christophe Hendrickx et al. (2016), a piece which provides another interpretation on Moroccan spinosaurine diversity based on isolated quadrate bones. These are elements from the back of the skull which, among other things, articulate with the lower jaw. I don't really want to go into the ins and outs of their primarily descriptive and systematic assessment as the paper is a) a bit of a beast and b) we've spoken a lot about spinosaurine taxonomy of late and I'm desiring fresh topics. It will suffice to summarise that Hendrickx et al. (2016) provide compelling evidence for at least two spinosaurines being present in the Moroccan Kem Kem Beds, one of which is Sigilmassasaurus brevicollis and the other is - in their interpretation - Spinosaurus aegyptiacus. These results are not exactly the same as those presented in the recent Evers et al. (2015) paper, as Hendrickx et al. shuffle and deal north African spinsosaurid fossils among named taxa in another unique way. However, it certainly adds further evidence against the concept of a single spinosaurine species ruling Late Cretaceous north Africa proposed by Ibrahim et al. (2014). And yes, for those interested in scientific responses to the famous quadrupedal Spinosaurus reconstruction publicised in 2014, Hendrickx et al. (2016) specifically comment on the likelihood of it being a chimera of animals from across time and space. There's lots more in the paper - spinosaur skull morphology, body size, ontogeny, loads of illustrations and it's 100% open access - interested parties should definitely check it out.

The pelican-like foraging anatomy of Spinosaurus, as illustrated in Hendricks et al. (2016).

Moving on to fresh, but still spinosaurine-filled waters, let's talk about something more fun - functional morphology that is*! One of the neater parts of the Hendrickx et al. analysis is that they pay a lot of attention to the jaw articulation of spinosaurines, providing detailed descriptions of how it may have influenced jaw operation and prey capture (above). Some readers may be aware that spinosaurids have 'helical' or 'asymmetric' jaw articulations, in which the quadrate condyles force the jaw somewhat outwards as it opens. Hendrickx et al. quantify this, noting that the lateral displacement is somewhere in the region of 20% of the quadrate width when the jaw is opened 45°. This equates to approximately 20 mm of motion on each side of the jaw in a c. 1 m long skull. As a rule, non-avian theropods do not have these helical joints, although they do occur in some pterodactyloid pterosaurs and, perhaps more famously, modern pelicans. Hendrickx et al. (2016) also note that the anterior connection between spinosaurid mandibular rami - the mandibular symphysis - has a fibrous texture indicative of being somewhat loose and flexible, enhancing the pelecanid comparisons further.

*It's OK, my shame about that pun is worse than any punishment you could deliver.

In both the paper and news outlets (example), these perceived similarities between spinosaurid and pelican jaws are being stated as evidence of spinosaurs feeding in a pelican-like fashion, splaying their jaws to enhance food capture and swallow larger prey. Regular readers may recall that Darren Naish and I published research on similar claims for pterosaurs in 2013 (although the paper was not 'officially' published until last year - Witton and Naish 2015), countering suggestions that some pterosaurs fed like pelicans because of their helical quadrate articulations (Averianov 2013). This background made me surprised that another group of fossil animals was being labelled as pelican-like, as much of our discussion on pterosaurs is applicable to non-avian theropods and we're even cited in the Hendrickx et al. paper! I thought it might be of interest to explain some of my reservations about this idea here**.

**I want to note that I feel a bit awkward writing this commentary in light of recent controversies on palaeontology blogs, so-called 'Post Publication Peer Review' and so on. I hope that it's clear that this article, as with all the writings here, are meant as constructive, well-meaning expressions of opinion from someone with an interest in these topics and experience in a similar research field. My disagreement with the functional analogy proposed by Hendrickx et al. and their PR work is a polite one, and doesn't mean I disrespect them as scientists or want to undermine the significance of their paper.

We should begin by familiarising ourselves with the jaws of some relevant modern birds. Quite a bit of research has been done into pelican jaw anatomy (Schreiber et al. 1975; Meyers and Myers 2005; Field et al. 2011), an unsurprising fact given how awesomely and specifically adapted their jaws are to their unusual foraging method. Researchers have identified a number of adaptations critical to pelicans being able to splay their jaws so widely. They include reduced mineralisation at the middle part of the lower jaw to make a long 'bending zone', and even further reduction of mineral content (down to 20%) adjacent to the mandibular symphysis. This makes a 'hinge' for the mandibular rami to swing outwards on despite the fact there is no articulation or joint in the jaw at this point. The mandibular symphyses are so short that virtually all the jaw length is permitted to splay. At the other end of the jaw, the tongue is similarly reduced so as not to get in the way when the mouth is opened. The connection between the dentary bone (forming the jaw anterior) and the complex of bones of the posterior jaw is long, loosely connected and obliquely oriented so as to aid motion when the mandible spreads outwards. Even the horny tissues of the beak are specialised, being very thin (described as 'skin-like' by some authors) so as not to impede jaw flexion.

Contrastingly, little mention is made of helical jaw joints when talking about pelican foraging strategies. Zusi (1993) mentions that jaw spreading at the joints may be important to this effect, but more recent literature states that the precise mechanic responsible for bowing pelican mandibles is not really understood (Meyers and Myers 2005). Three hypotheses are currently thought viable: forces and weight of water acting on the jaw (known to be only part of the solution, as pelicans can splay their jaws on land too), contraction of muscles in the gular pouch (pulling the chin backwards, pushing the jaw rami out) or twisting of the lower jaw by the pterygoideus jaw musculature (Meyers and Myers 2005 and references therein). I guess it's possible that lateral displacement of the jaws has some role too, but it's interesting that the pelican guys aren't championing it's role as essential to manibular bowing. It's always risky using negative evidence in this way, but it might be telling given how intensively studied pelican skulls are.

Mandibular bowing in modern birds, as illustrated by Zusi (1993). a, herring gull (Larus argentatus) with relaxed and bowed mandibles; b, common potoo (Nyctibius griseus) skull and mandible (arrows show zones of flexion; c, tawny frogmouth (Podargus strigoides), a potoo incapable of mandibular kinesis. Note contrasting morphology between the potoo mandibles - even as a fossil taxon, there would be no doubt that N. griseus was capable of mandibular flexion.

Perhaps a factor in ornithologists not paying much attention to pelican jaw joints is that helical quadrate articulations are not unique to them. In addition to pelicans, pterosaurs and spinosaurids, numerous bird groups are equipped with asymmetric quadrate condyles. These including herons, shoebills, certain hummingbirds and seed-eating songbirds, potoos and others. In all these species, the effect is the same - lateral displacement of the posterior jaws when the mouth is opened. Because these animals have very different diets, foraging strategies and lifestyles, their convergence on a similar jaw anatomy reflects a basic functional requirement: apprehending or swallowing large food (Zusi 1993). However, not all these species bow their anterior mandible regions in a significant way. To perform this trick, many non-pelecanid birds have mandibles with hinged regions (above). Some species, like certain potoos, are remarkable in this regard, perhaps surpassing pelicans in their ability to expand and even twist their throats into wide basins. It is not only specialised taxa which have remarkable lower jaws: the likes of seagulls can also bow their mandibles to an impressive extent. In these birds, a combination of the pull of the pterygoideus muscle and osteological specialisations allow the jaws to bulge sideways and large food items to enter the throat. The message here seems to be that helical jaw joints might have nothing to do with pelican-like jaw bowing, whereas other features - the development of pronounced mandibular hinges and specialised musculature - might be.

Modern birds give us a pretty good idea of what sort of features we're looking for in a pelican-like dinosaur. In doing so, as might already be obvious, they suggest major issues with the pelican-spinosaur analogy. Firstly, we need to acknowledge that helical jaw joints are not a special pelican feature. We could also call spinosaurid mandibular joints 'heron-like', 'potoo-like', or even 'hummingbird-like'. It seems more precise to suggest spinosaurid jaw joints are similar to those of several modern bird lineages and not over-emphasise anything to do with pelicans.

Our mandibular bowing experiments with pterosaurs and pelicans illustrated. Even when stretching the pterosaur jaws beyond the limits of their jaw joints, their area increase was negligible compared to that of a lazy pelican. From Witton and Naish 2015.

Secondly, given how ecologically variable modern birds with helical jaw joints are, and that there is no obvious correlation between asymmetric quadrate condyles and mandibular bowing, we need to treat them as part of a 'functional package' - a recipe of functional elements considered simultaneously to assess their overall effect on behaviour and lifestyle. The attempt here is to see the bigger picture of how such joints work with the rest of the jaw - do they function in a pelican-like fashion? It doesn't seem so. The amount of mandibular movement in spinosaurids is pretty negligible compared to what we see in modern birds. As noted above, quantification of of jaw motion by Hendrickx et al. suggests the lower jaws move only a tiny amount, each jaw splaying 20 mm from a skull approaching 1000 mm long. It's likely this motion would not even be noticeable in life. I'm reminded of the calculations Darren and I predicted for pterosaur jaw expansion (above) where we found pterosaur helical jaw joints boost jaw area, at most, by a few 10s of percent, but anterior jaw bowing in pelicans increases area by hundreds of percent (Witton and Naish 2015). These calculations seem to agree with current research that bowing of the anterior mandible is the most important agent in having widely distending jaws. No spinosaurid jaw yet known has adaptations for anterior mandible motion akin to those of pelicans, or even other birds capable of mandibular bowing. Many readers will know that we can, and have, assessed the kinetic potential of fossil animal skulls, including those of fossil pelicans (Louchart et al. 2011). we should be able to detect bowing mandibles in non-avian dinosaurs and other fossil reptiles, should they occur.

My points here might be countered by the observation that the mandibular symphyses of some spinosaurids are quite fibrous, perhaps indicating a loose and mobile connection between them (Hendrickx et al. 2016). This might be the case, but Hendrickx et al. also note that some spinosaurid symphyses are longer than those of other theropods, thus actually having a greater degree of anterior attachment between each lower jaw. Based on our understanding of modern bird jaws, surely this is the opposite of what we'd expect in an extinct pelican-analogue? Even if I'm wrong on that, a slightly spongy symphysis and helical jaw joints are several functional miles off the flexibility afforded by avian jaws - especially those with the most extreme adaptations for mandibular bowing, like pelicans.

In all, then, I'm not convinced on the idea that spinosaurids were pelican-like in their foraging habits. Rather, the adaptations outlined by Hendrickx et al. suggest a somewhat bird-like ability to increase gape for swallowing slightly larger food than usual. In actuality, spinosaurid jaw functionality contrasts so markedly with that of pelicans that it might be misleading to tout pelicans as spinosaur analogues. After all, the spinosaurid ability to bulge their jaws slightly is not especially pronounced or even rare, whereas what pelicans do is really both those things: an extreme and marked adaptation, and almost unique in nature. I come back to a point I've made about other instances of 'extreme' modern animals being used as analogues for extinct ones: we need to be as thorough as possible in our functional assessments before pointing to highly specialised and extremely adapted modern species as suitable analogues for long dead taxa.

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