Did tyrannosaurs smile like crocodiles? A discussion of cranial epidermal correlates in tyrannosaurid dinosaurs

Brain 1: "Right, you need an image for your tyrannosaurid facial tissue post."
Brain 2: "OK, here're some Tyrannosaurus rex in a really dark and back-lit scene. Their faces are in shadow, and you can't really see the features."
Brain 1: "This is perfect. After all, only losers want to see the faces of animals in posts about facial tissues."
Brain 2: "Exactly. Hey, since when did I have two brains?"
Brain 3: "Beats me."

Discussing the craniofacial tissues of tyrannosaurid dinosaurs is the palaeointernet equivalent of lighting a match in a straw-filled barn - the slightest spark of opinion spawns a 100-strong comment field about extra-oral tissues, tooth exposure, rictal tissues, facial skin depth and a number of other topics. But despite this keen popular interest, there's been relatively little academic study into tyrannosaurid facial tissues, perhaps because their soft-tissues mostly remain unrepresented in the fossil record. Happily, close examination of tyrant skulls reveals a number of textures and rugosity profiles which were almost certainly created by bone-skin interaction, so we can form some idea of their life appearance even without soft-tissue specimens. The first detailed attempt at interpreting tyrant cranial rugosities was published last year by tyrannosaur expert Thomas Carr and colleagues (Carr et al. 2017 - you might also know Thomas by his super-comprehensive blog Tyrannosauroidea Central). This widely publicised paper proposed a number of hypotheses about the face of Daspletosaurus horneri: that the sides of the jaw were adorned with crocodile-like 'facial scales'; that various scales, dermal armour and cornified sheaths adorned the nasal and orbital region; and that it lacked lips (not explicitly stated in the paper, but restored as such in an illustration and touted in the paper's PR). The idea that tyrannosaurids may have had crocodylian-like facial tissues has since generated a lot of discussion online, some in favour, some against, and as someone increasingly looking at epidermal correlates for palaeoartistic purposes, I thought this topic was worthy of a blog article: are tyrannosaurid jaws really croc-like enough to assume comparable skin types?

(An important caveat before we start this discussion is that the following is based on tyrannosaurids generally, not D. horneri specifically, because the horneri study does not include photographs of its alleged epidermal correlates. The D. horneri paper describes them very well (see Carr et al. 2017, supplementary data), but it's difficult to evaluate them without images of the bone surfaces themselves. Dave "Tyrannosaur Chronicles" Hone needs a shout out here for sharing his expertise and extensive image library of tyrant fossils as I prepared this post - though I have some experience with tyrannosaur bones and their interpretation, this article has been considerably improved by his involvement.)

Tyrannosaurids and crocodylians: face off

An obvious place to begin this discussion is crocodylian facial structure. Crocodylian skulls are so familiar that it's easy to forget how distinctive they are among modern animals, and I don't think it's widely known that their skin plays a significant role in shaping their skull tissues. Crocodylian jaw bones have incredibly high numbers of foramina, with averages of 100 in each major jaw bone (premaxilla, maxilla and dentary) and over 1000 in each bone in some specimens (Morhardt 2009). These openings are the loci around which gnarly ridges and tubercles grow by a process of dermal ossification: tissues from the skin are turned to bone and build up the sculpting on the skull surface (Grigg and Kirshner 2015; de Buffrénil et al. 2015). Simultaneously, the bone immediately surrounding the foramina is resorbed, enhancing the rugosity pattern further and creating that highly distinctive, deeply pitted and grooved crocodylian skull texture (de Buffrénil et al. 2015). This restructuring can be extensive and, over ontogeny, crocodylian snout surface area can increase by as much as 20% (de Buffrénil et al. 2015). That's a major reworking of the superficial bone of the skull, and their skin has a major role in its development.

Skull of a mature American crocodile, Crocodylus acutus, demonstrating that classic crocodylian skull texture. Cropped from public domain Wikimedia image by Daderot.

Among living tetrapods, only some turtles and a couple of geckos show a comparable degree of sharply-defined cranial sculpting (Evans 2008; de Buffrénil et al. 2015) but, among extinct taxa, stem-tetrapods, temnospondyls, parareptiles and many crocodylomorphs present analogous cranial conditions (Witzmann et al. 2010; de Buffrénil et al. 2015). Studies show that temnospondyl skulls developed their sculpting via a similar mechanism of ossifying dermal tissues (Witzmann et al. 2010), perhaps indicating croc-like skin properties in these animals, too. Until recently it was thought that crocodylian facial skin was scaly, but new research shows that it is actually a sheet of toughened skin which cracks through growth, creating a scaly appearance, but not true epidermal scales akin to those seen in lizards (Milinkovitch et al. 2013). Regardless of whatever other conclusions are drawn here, this has to be a minor amendment to Carr et al.'s (2017) interpretation: if tyrannosaurids (or any other extinct animal) have croc-like textures on their jaw bones, we should be visualising tight, tough skin, not epidermal scales.

Juvenile alligator, Alligator mississippiensis, showing virtually crack-free facial skin - it's only adults that develop the extensively cracked, superficially 'scaly' faces. Photo by Joxerra Aihartza, from Wikimedia, FAL 1.3.

Whether tyrannosaurid jaws are truly crocodylian-like is open to question, however. Carr et al, (2017) are clear that they consider tyrants and crocodylians jaws as identical in superficial appearance ("The texture in crocodylians is identical to that of tyrannosaurids, except that the entire face of crocodylians is coarse in texture" - p. 21; Supplementary information to Carr et al. 2017) but I disagree: there are a number of ways in which they differ and, given the link between crocodylian skull development and dermal tissues, these differences may be critical to our considerations of facial anatomy. Many of these contrasts pertain to jaw foramina, which we know are important in defining crocodylian cranial sculpting (de Buffrénil et al. 2015) and may have a deeper relationship with jaw tissue properties (Morhardt et al. 2009; Hieronymus et al. 2009).

Firstly, although tyrannosaurids have elevated numbers of jaw foramina compared to other dinosaurs, their numbers are, on average, significantly lower than those of crocodylians (Morhardt 2009). No tyrannosaurid jaw bone reported by Morhardt (2009) exceeds 81 foramina, which is high for a dinosaur, but still short of the crocodylian average, and well below the 1000+ figure reported for some croc jaws. Interestingly, data in Morhardt (2009) suggests that foramina numbers weakly correlate to jaw size: the longer a jaw is, the more foramina it generally has. This trend is particularly well shown in her tyrannosaurid sample but seems true of other fossil and extant animal groups as well, and might also be reflected in ontogeny (smaller Tyrannosaurus have fewer foramina, on average, than large ones). The cause behind this trend seems to be elusive at present - might it reflect a change in tissue type with age (Morhardt 2009)? does it reflect demands of supplying an absolutely larger jaw with nervous and vascular tissues? - but whatever the reason, it implies that we should consider foramina frequency proportionate to jaw size when analysing rugosity profiles. Under this metric, foramina values in crocodylian jaws are even more impressive as, compared to some extinct animals, their skulls are of middling size. By contrast, the slightly above-average foramina counts of even the largest tyrannosaurines seem less significant because, even with extreme jaw size, they don't attain a value comparable to a much smaller alligator. If we remove size from our consideration by comparing similarly-sized tyrant and croc jaws, we find they are worlds apart in terms of jaw perforation. Indeed, the foramina values of smaller tyrants are nothing special - they are comparable to most other similarly-sized tetrapods (Morhardt 2009). Presumably, this explains why - as many internet conversations have pointed out - tyrannosaurid jaws simply don't have that same obvious, pitted surface as those of crocodylians.

Further differences might be noted in relative foramina sizes. Those foramina occurring high on tyrant snouts - such as at the top of the maxilla - are much smaller than the broader, obviously deep labial foramina paralleling the jaws (Brochu 2003; Carr et al. 2017). In crocodylians however, jaw foramina seem to have a lower size range. Foramina shape and size is an important consideration for facial tissues (Hieronymus et al. 2009) and this might imply different tyrant facial tissues over the side of the snout vs. those at the jawline, whereas the more uniform foramina sizes of crocodylians are entirely consistent with their homogeneous jaw skin.

Schematic drawing of Tyrannosaurus skull FMNH PR2081 (the specimen better known as 'Sue') showing the distribution and (somewhat conservatively) size differences in jaw foramina. This huge skull is said to be one of the most rugose Tyrannosaurus skulls known (Brochu 2003), but it fails to meet the high foramina numbers, sculpting extent and uniform foramina size of mature crocs. Image from Brochu (2003).

A related issue concerns a possible link between extra-oral tissues and foramina counts. Morhardt (2009) noted that, as a general rule, extant animals with average foramina counts below 50 in each jaw bone have tooth-covering extra-oral tissues; that those above 50 but below 100 have immobile facial tissues; and only those with 100 or more are reliably excluded from having lips or other means of tooth coverage. Average tyrant jaw foramina counts are well below that upper threshold for exposed teeth so, by this metric, they should have lips, and would not look like bipedal crocodiles. This might match what we're seeing with tyrant foramina size: perhaps those large labial foramina are something to do with nourishing and innervating extra-oral tissues, while those on the side of the snout need only access the overlying skin. There are some complications to Morhardt's data (if anyone is looking for a PhD project, a more extensive follow up would be terrific) but, at face value, her research does not support crocodile-like facial tissues for tyrannosaurids.

Finally, we can observe that the ontogeny of tyrannosaurid skull textures is not at all crocodylian-like. Tyrants do have some sculpting on their jaw bones and, as with most reptiles, these become better defined with maturity (e.g. Evans 2008; de Buffrénil et al. 2015). However, even the most rugose tyrannosaurid skulls do not match the complex and sharply pitted rugosity patterns of mature crocodylians (e.g. Osborn 1912; Carr et al. 1999; 2017; Brochu 2003; Hone et al. 2011). Given that ossifying facial skin is a direct factor in jaw bone sculpting in crocodylians, the lack of comparable development in tyrannosaurids is a blow to the idea that their faces bore the same dermal regime. Histological examination of tyrannosaurid jaw bones for might have further insight here, as the resorption/remodelling pattern might reveal details about bone/dermal interactions (Witzmann et al. 2010; de Buffrénil et al. 2015) but, for now, this inconsistency seems to be a big hole in the idea that tyrannosaurids had crocodylian-grade facial tissues.

Does the tyrannosaurid EPB help here?

Collectively, these points seem to suggest that tyrant jaws are not as croc-like as argued, and that it's not a given that the two groups had similar facial tissues. A counterargument to this is that crocodylians are the best tyrant analogues in their extant phylogenetic bracket (EPB), and thus give us our best, most phylogenetically informed insight into tyrannosaurid faces. Indeed, the croc-snouted tyrant hypothesis was informed primarily by comparisons with taxa from the tyrannosaurid EPB - specifically the skulls of birds and alligators (Carr et al. 2017) and, sure, crocs and tyrannosaurid jaws may not be exactly alike, but they're undeniably more similar to each other than either is to a bird. Might we concede that the comparisons aren't perfect, but that this is simply the best we can do without violating the tyrannosaurid EPB?

Our issue is that, while the EPB is a terrific method for predicting ancient anatomies, it really struggles with the complexity of archosaur facial tissue evolution, perhaps to the extent of being redundant. One major issue is that we can be near certain early archosaurs had neither croc- or bird-like facial tissues because no species representing the earliest phases of archosaur evolution have comparable skin-influenced jaw textures (see Nesbitt et al. 2013, and papers therein). Rather, we only see these features developing in relatively crownward archosaur groups, implying independent development of their respective facial anatomies well after the croc-bird split. This being the case, the common archosaur ancestor must have had a different set of facial tissues, and the facial anatomy of extant archosaurs may tell us little about the faces of Mesozoic dinosaurs.

Like crocodylians, birds have jaws with surface textures shaped by their overlying skin: networks of branching neurovascular canals and oblique foramina underlie cornified sheaths (their beaks). The prominence of such jaw rugosities in living archosaurs allows us to predict the facial condition of fossil archosaurs and stress test the tyrannosaur EPB, and it doesn't seem to hold up well. This skull is a marabou stork (Leptoptilos crumenifer), photo by me.

A second major issue is evidence that living archosaur faces don't reflect tissues known from their fossil cousins. In addition to tight facial dermis and cornified sheaths, a plethora of fossil evidence show that fossil archosaurs had faces with epidermal scales, projecting skin tissues (e.g. pterosaur crests) armoured dermis, and cornified pads (Frey et al. 2003; Hieronymus 2009; Hieronymus et al. 2009; Carr et al. 2017). These go well beyond the anatomical range implied by the EPB and show that fossil archosaur faces sometimes had more in common with non-archosaurs than their closest extant relatives. We must remember that the EPB is a predictive method which should be applied where no other data is forthcoming: in this case, we have enough fossil data to show that our EPB predictions are problematic, and that we can't rely on it for insight into tyrannosaurid faces. I'm hardly the first to suggest EPB approaches don't help discussion of non-avian dinosaur faces (e.g. Vickaryous et al. 2001; Knoll 2008), but these points are worth repeating in this context: I don't think the EPB is a compelling supporting argument for a croc-faced tyrannosaurid.

So, if not croc-like, what might be happening here?

If croc-skinned tyrant snouts are problematic, what are our other options? Our discussion above really only pertains to the maxillary region of tyrannosaurid snouts and, for the rest of the skull, I think Carr et al. (2017) nailed it: what I've seen of tyrannosaurid skulls suggests the orbital region and skull roofs were covered in cornified sheaths, armoured dermis and large scales. There seems to be quite a bit of variation in these tissues, with some taxa having more defined scale correlates over the nasals than others, as well as differences in elaborations of the hornlets above the eye. In all likelihood, different tyrant species would be highly recognisable in life by the development of scales, armour and horn across the top of their faces. These armoured tissues are entirely consistent with what we understand of tyrannosaurid behaviour: if you were being routinely bitten about the face by another tyrannosaur, you'd want some protection too (see opening image).

Dorsal view of the snout of a red river hog (Potamochoerus porcus). These pitted, grooved bone textures are fairly widespread across tetrapod skulls and don't seem to correlate to any one skin type, but might indicate the presence of tough, well-cornified skin (these hogs wrestle with their faces, so need protected snouts). Note the projecting rugosities on the side of the snout and on the ascending maxillary projection - these anchor vast skin projections in life. Red river hog skulls are awesome. Photo by me.

But what of that maxillary portion of the snout - the lateral region suggested as being crocodile-like? The surfaces of tyrannosaurid maxillae are pretty complex with a hierarchy of rugosity profiles (Carr et al. 2017). Very obvious features include many pits and short, branching neurovascular grooves: these might not necessarily indicate of particular tissue type in themselves, but are often associated with a well-cornified, tough epidermis (above). The high number of foramina in tyrant maxillae implies immobile facial tissues (Morhardt 2009), which I guess we probably expected in a reptile anyway.

Holotype maxilla of Zhuchengtyrannus magnus: check out that network of elliptical depressions bordered by raised regions. Note how they terminate about a few centimetres above the line of labial foramina - we'll come back to this in a moment. From Hone et al. (2011).

Underlying these pits and grooves are a series of large, elliptical shallow depressions surrounded by low ridges (above). These vertically-aligned structures are found in many tryannosaurids and are especially obvious in large tyrannosaurines like Tyrannosaurus, Tarbosaurus and Zhuchengtyrannus. You can see them easily in museum mounts, even from across the room. Some taxa have single rows of these structures below the antorbital fenestra (Tyrannosaurus), but others have tessellating networks of depressions and ridges that extend to the top of the maxilla (Tarbosaurus), terminating beneath the scaly region overlying the nasal bone. They're unusual structures which are almost certainly epidermal in origin: they're in a place where epidermal correlates often form; are more pronounced in mature individuals; are regularly and consistently arranged across the surface of the skull; and are not associated with any pneumatic or neurovascular openings. They broadly recall the 'hummocky' rugosity profile seen under epidermal scales (Hieronymus et al. 2009) and, if so, the convex, ridged areas probably underlay vertically aligned scales, or rows of scales. Some tyrant skulls, such as the especially rugose Tyrannosaurus skull AMNH 5027, have especially sharp and rugose ridges which, to me, recall the facial ridges of certain iguanine lizards: specifically, anoles, chameleons and basilisks. These are often quite rugose and sculpted, but smoother, more tyrannosaurid-like conditions exist in a number of species (I'm thinking of things like helmeted basilisks and smooth chameleons). Prominent, ornamental rows of relatively large and often colourful scales overly these structures in these iguanines and I wonder if the same was true for tyrants. Alternative hypotheses, such as scales sitting in the depressions between the ridges, aren't consistent with the relationship between scales and bone in living species, and there's no indication that other tissue types (e.g. cornified sheaths, armoured dermis) were present in these areas, so I think the ornamental ridge hypothesis is sensible (or, at least, not outrageously daft given the available data). I must admit to liking this hypothetical juxtaposition of fancy ornamental scales around the mouth and tough, reinforced tissues over the snout: perhaps tyrannosaurs weren't just big biting machines, but liked to look nice, too.

AMNH 5027 is just riddled with interesting surface textures that probably relate to epidermal features. To my reckoning, in addition to those depression/ridge pairings on the maxilla, the dorsal region of the lacrimal bears coarse projecting rugosity (armoured dermis); the top of the premaxilla and postorbital has a series of coarse hummocks (probable scales); and the ascending processes of the postorbital, lacrimal and maxilla are covered in a dense, anastomising network of neurovascular foramina (cornified sheath). What a neat looking animal Tyrannosaurus must've been - my take on this data is seen in the paintings accompanying this post. Image from Osborn (1912), in public domain.

Significantly, I can't find any tyrannosaurid skulls where these possible scale correlates extend right to the base of the maxilla (see photos, above). Rather, they terminate a few centimetres above the line of labial foramina, and this might have bearing on ongoing discussions about dinosaur lips. Scleroglossan lizards (the group that includes geckos, skinks, varanoids and amphisbaenians) frequently have osteoderms on their faces which cover their snouts (including the maxillae) except for a region around the labial foramina, which is smooth. This seems to relate to the presence of lip tissues displacing the scales from the skull and prohibiting formation of a epidermal correlate adjacent to the toothrow. Their maxillary juxtaposition of epidermal correlates is the same configuration that we see in tyrannosaurids as well as a number of other non-avian dinosaurs with maxillary epidermal correlates (e,g, pachycephalosaurids, ankylosaurids, some ceratopsids) and this has to be regarded consistent with hypotheses of extra-oral 'lips' in tyrannosaurids and other dinosaurs. If we add this to the evidence from foramina counts (Morhardt 2009, also see above) as well as other arguments for extra-oral tissues the case for crocodylian-like exposed teeth is looking increasingly doubtful. I must admit to thinking that proponents of exposed dinosaur teeth really need to start making better cases for this idea: most ways we can slice this particular debate suggests that extra-oral tissues are looking likely (and no, the common argument that their teeth were too big to be sheathed isn't valid: it's simply a speculation based on incredulity, not actual data from dinosaur skulls).

So...

To sum up this long, detail-heavy post:

1. Crocodylian skull textures are basically built by their skin, and we should expect any prehistoric animal with croc-like facial tissues to have a croc-like cranial rugosity profile. What we see in tyrannosaurs is a little croc-like, but only superficially. Differences between croc and tyrant skull tissues may be more significant than their similarities and seem to contradict the notion of croc-like facial tissues in tyrannosaurids.
2. Attempts to ground discussions of dinosaur facial tissue in the EPB are problematic: a great deal of what we know about archosaur facial tissue refutes what the EPB predicts. Basic comparative anatomy, framed by a wide phylogenetic bracket, might be the way forward for understanding dinosaur faces.
3. Tyrant faces - as largely predicted by Carr et al. (2017) - seem to have been adorned with scales, cornified sheaths and armoured dermis, but their jaw regions may have been covered in vertical (perhaps ornamental?) bands of epidermal scales, not croc-like skin. Distribution of epidermal correlates around the jaws of tyrannosaurids (and other dinosaurs) is suspiciously reminiscent of many lizard skulls, and may favour a lipped condition.

Tyrannosaurus rex portrait, based on my take of epidermal correlates of the AMNH 5027 skull. No, you tell it that its ornamental ridges look a bit silly.

Perhaps unsurprisingly, I couldn't research and write all this without wanting to draw my take on tyrannosaur facial anatomy. I'll leave you with my take on the face of AMNH 5027 (above): I'm sure it'll need modifications as more details on tyrannosaurid faces come to light, but I won't pretend it wasn't neat to draw a Tyrannosaurus based on relatively objective reading of available data. Palaeoart is at it's most exciting when we join dots between data rather than, as is so often the case, largely imagine huge swathes of our subject species. The duelling Tyrannosaurus that welcomed you to the post are based on the same model.

Enjoy monthly insights into palaeoart and fossil animal biology? Support this blog for $1 a month and get free stuff!

This blog is sponsored through Patreon, the site where you can help online content creators make a living. If you enjoy my content, please consider donating $1 a month to help fund my work. $1 might seem a meaningless amount, but if every reader pitched that amount I could work on these articles and their artwork full time. In return, you'll get access to my exclusive Patreon content: regular updates on research papers, books and paintings, including numerous advance previews of two palaeoart-heavy books (one of which is the first ever comprehensive guide to palaeoart processes). Plus, you get free stuff - prints, high quality images for printing, books, competitions - as my way of thanking you for your support. As always, huge thanks to everyone who already sponsors my work!

References

• Brochu, C. A. (2003). Osteology of Tyrannosaurus rex: insights from a nearly complete skeleton and high-resolution computed tomographic analysis of the skull. Journal of Vertebrate Paleontology, 22, 1-138.
• Carr, T. D. (1999). Craniofacial ontogeny in Tyrannosauridae (Dinosauria, Coelurosauria). Journal of vertebrate Paleontology, 19(3), 497-520.
• Carr, T. D., Varricchio, D. J., Sedlmayr, J. C., Roberts, E. M., & Moore, J. R. (2017). A new tyrannosaur with evidence for anagenesis and crocodile-like facial sensory system. Scientific reports, 7, 44942.
• De Buffrénil, V., Clarac, F., Fau, M., Martin, S., Martin, B., Pellé, E., & Laurin, M. (2015). Differentiation and growth of bone ornamentation in vertebrates: a comparative histological study among the Crocodylomorpha. Journal of morphology, 276(4), 425-445.
• Evans, S. E. (2008). The skull of lizards and tuatara. Biology of the Reptilia, 20, 1-347.
• Grigg, G. (2015). Biology and evolution of crocodylians. Csiro Publishing.
• Hieronymus, T. L. (2009). Osteological correlates of cephalic skin structures in amniota: Documenting the evolution of display and feeding structures with fossil data. Ohio University.
• Hieronymus, T. L., Witmer, L. M., Tanke, D. H., & Currie, P. J. (2009). The facial integument of centrosaurine ceratopsids: morphological and histological correlates of novel skin structures. The Anatomical Record, 292(9), 1370-1396.
• Hone, D. W., Wang, K., Sullivan, C., Zhao, X., Chen, S., Li, D., ... & Xu, X. (2011). A new, large tyrannosaurine theropod from the Upper Cretaceous of China. Cretaceous Research, 32(4), 495-503.
• 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.
• Knoll, F. (2008). Buccal soft anatomy in Lesothosaurus (Dinosauria: Ornithischia). Neues Jahrbuch für Geologie und Paläontologie-Abhandlungen, 248(3), 355-364.
• Milinkovitch, M. C., Manukyan, L., Debry, A., Di-Poï, N., Martin, S., Singh, D., ... & Zwicker, M. (2013). Crocodile head scales are not developmental units but emerge from physical cracking. Science, 339(6115), 78-81.
• Morhardt, A. C. (2009). Dinosaur smiles: Do the texture and morphology of the premaxilla, maxilla, and dentary bones of sauropsids provide osteological correlates for inferring extra-oral structures reliably in dinosaurs?. Western Illinois University.
• Nesbitt, S. J., Desojo, J. B., & Irmis, R. B. (2013). Anatomy, phylogeny and palaeobiology of early archosaurs and their kin. Geological Society, London, Special Publications, 379(1).
• Osborn, H. F. (1912). Crania of Tyrannosaurus and Allosaurus; Integument of the iguanodont dinosaur Trachodon. Memoirs of the AMNH; new ser., v. 1, pt. 1-2.
• Vickaryous, M. K., A. P. Russell, and P. J. Currie. (2001). Cranial ornamentation of ankylosaurs (Ornithischia: Thyreophora): reappraisal of developmental hypotheses. In K. Carpenter (ed). The Armored Dinosaurs. 318–340. Indiana University Press.
• Witzmann, F., Scholz, H., Mueller, J., & Kardjilov, N. (2010). Sculpture and vascularization of dermal bones, and the implications for the physiology of basal tetrapods. Zoological Journal of the Linnean Society, 160(2), 302-340.