Dinosaur scales: some thoughts for artists

Turns out that Triceratops horridus had some of the coolest scales of any dinosaur: huge, interlocking tubercles with low bosses and spikes. No other dinosaur has skin like this - at least, not without supporting osteoderms. But what are dinosaur scales actually like, and are we depicting them accurately in our art?

The discovery that many Mesozoic dinosaurs were superfuzzyfilamentouspinyalidocious has been an major influence on contemporary Mesozoic palaeoart. This has affected more than just how we depict the gross appearance of dinosaurian subjects, but also our attitudes to their behaviour, demeanour and place in the Mesozoic world. I've written a fair bit about scientific and artistic attitudes to filamentous dinosaurs and joined choruses arguing that it's important to get these new depictions 'right': we want to see filaments of appropriate morphology, size and distribution in reconstructions of these animals.

In light of this, it's a little peculiar that we have slightly more lax attitudes to how we reconstruct scaly integuments in these animals. We have some truly spectacular skin impressions from scaly dinosaurs which provide a wealth of information about their detailed appearance, and yet many of our reconstructions incorporate little of this data. Instead, we often create 'generically' scaly or wholly speculative integuments. Common issues include rendering of scales of homogenous size and shape across an entire animal, showing little difference in scalation between species, and issues with the size, proportions and shape of individual tubercles. Other times, and most egregiously, some individuals understate just how good the records for scales in certain species are, this seemingly giving license to render a more speculative, but flamboyant body covering. It's not just amateurs making these mistakes and, in the interests of not being a hypocrite, I'll state early on that I'm guilty of some of these issues in my own work.

With this in mind, I want to see out 2015 with a fresh look at four exceptionally interesting samples of dinosaur scales, providing something of a refresher for myself and other about scaly dinosaur integument and food for thought on restoring these animals. The amount of scaly skin we have from dinosaurs means this list could easily comprise 10 or even 20 examples, but for the sake of brevity and detail I'm keeping the count low. The specimens here may be familiar to veterans of dinosaur literature, but I hope to cover them in sufficient detail that much of this information will be new to many readers.

The Carnotaurus holotype skin impressions

Outside of the feathered coelurosaurs, substantial remains of theropod dinosaur skin are pretty rare. There are lots of scraps, many of which are only cautiously referred to Theropoda, but large pieces of skin associated with specific skeletons are very thin on the ground. These circumstances make the extensive scaly skin impressions known from the Late Cretaceous Carnotaurus sasteri type specimen quite special. This specimen is already impressive: described in detail by Bonaparte et al. 1990, it comprises a near complete skeleton missing only parts of the legs and end of the tail. The fact this specimen also preserves a host of skin remains means Carnotaurus is an especially well represented large theropod. Many readers will know the skin remains associated with this specimen makes it quite integral to debates over the ancestral state of dinosaur and theropod skin. As one of the few relatively 'basal' theropods known with decent skin remains, Carnotaurus has quite a bit of sway in discussions about filament development in theropods.

Illustration of the tail base Carnotaurus skin impressions from Bonaparte et al. (1990). The deep grooves in the specimen represent topography of the associated axial skeleton, in this case the haemal arches. Scale bars represent 10 cm.

The skin remains of Carnotaurus are a little patchy, but represent many different parts of the body: the anterior neck, shoulder girdle, mid-torso, and the base of the tail. The skull also bore skin impressions before they were accidentally prepared away. The largest piece of skin covers the tail base, and is figured above. A huge amount of detail can be seen across the various skin pieces. They have a relatively uniform texture, each piece showing a mix of two scale types. The most obvious are the large, 4-5 cm diameter tubercles which protrude slightly from the rest of the skin. Instead of being randomly arranged, these are spaced regularly from each other at roughly 10 cm intervals, separated by large numbers of relatively tiny, 5 mm wide scales. The larger tubercles bear something of a keel, but the smaller structures are quite featureless. Parallel furrows with vertical orientation, perhaps representing creases, are impressed into the mosaic of smaller tubercles, but do not seem to leave an impact on the larger structures. Figures in Bonaparte et al.'s (1990) description suggest that this general skin texture extends right the way around the tail - the reduction in tubercle size and density on the ventral surface commonly seen in artwork is erroneous in this respect.

For artists, the Carnotaurus skin impressions enable us to 'connect the dots' as goes the appearance of this dinosaur's hide. It seems scales were present from skull to tail base, and it doesn't seem much of a stretch to assume most or all of the animal was scaly. There are a few reconstructions of extensively filamentous Carnotaurus out there but, sorry guys, this just doesn't jive with what we know of the skin of this animal. It also seems we shouldn't be drawing Carnotaurus with obvious differences in skin texture across the body - it looks pretty homogenous in the fossils. Also noteworthy is the size of most of the scales. It seems we'd only notice the larger, keeled tubercles and furrows on this animal unless we were standing very close. Those 5 mm tubercles might perhaps register as mottled colouration, but I doubt anyone without superhuman vision could distinguish each scale from afar. Note that Carnotaurus is not unusual in this respect - a lot of dinosaurs had much smaller scales than we show in our illustrations.

The Howe Quarry diplodocids

One of the most striking components of the 1999 Walking with Dinosaurs Diplodocus reconstruction was the tall dermal spines adorning the midline of the animal. These structures were not the idle fantasy of sculptors and artists, but actually based sauropod skin fossils from Howe Quarry, a famous Wyoming Jurassic locality. Described by the late palaeoartist Stephen Czerkas in 1992, these finds are frequently discussed by palaeoartists because sauropod skin impressions are extremely rare. The impressions are associated with incomplete skeletons representing animals from 2-3 to 14 m in length, with some skin pieces being exceptionally large at 25 x 75 cm. Unfortunately, Czerkas (1992) did not identify the remains of these animals. Howe Quarry yields at least one named diplodocid, the recently named Kaatedocus siberi, but it remains to be established if these scaled remains represent the same taxon.

The Howe Quarry diplodocid skin can be described as tessellating hexagonal scales with a rough surface, each about 3 cm across. There is no sign of these scales being divided by differently sized scales to form a pattern like those seen in Carnotaurus. The roughened texture of each scale is formed by small (2-3 mm) tubercles dotted across each large scale. As noted by several authors, this morphology is reminiscent of other examples of sauropod hide and seems common to at least Neosauropoda (e.g. Foster and Hunt-Foster 2011; Upchurch et al. 2015). As a rule, sauropods must've been quite rough to the touch.

Illustrations of the Howe Quarry diplodocid spines from Czerkas (1992). Top row, illustrations of specimens as preserved; bottom, interpretative drawings and reconstructed outlines. Scale bars equal 5 cm.

The truly exceptional part of the Howe Quarry diplodocid skin remains are the 14 subconical structures found dotted amongst the sauropod skeletons (above). Some were isolated, but several of these structures were found in connected rows. Perhaps the most significant of these were associated with a skin impressions wrapped around the tail base of one individual. It's from these remains that we can deduce that they were arranged in a row along back of the animal. This might seem like a minor feat, but - as anyone who's attempted to reconstruct stegosaur or titanosaur osteoderm arrangements might attest - being confident about the arrangement of extraneous pieces of dinosaur integument is nothing to be sniffed at. These cones vary quite a bit in size and shape. The largest, estimated at 18 cm tall when complete, seem to stem from the proximal end of the tail, but those of the distal end are smaller. Some cones are quite tall and straight, others blunter and recurved. The tips of all the cones are flattened laterally, but the bottoms more or less round in cross section. As with hexagonal scales on the body, these spines bear small tubercles across their surface. That these were purely comprised of the dermal tissues, and not osteoderms, is confirmed by the total absence of bone from any of the cones. Quite how far these conical structures extended across their owner's bodies cannot be said from the known remains, nor should we feel confident that we have the full spectrum of size or morphological variation of the spines (Czerkas 1992).

The detail and specificity of the Howe Quarry specimens give artists an atypically good insight into the appearance of these sauropods, and remain significant specimens or this reason. But as cool as this all is, the Howe Quarry skin specimens could be more useful. For instance, it is not clear how large each sauropod individual with associated skin remains was, and it's thus not clear how large those spines or scales were in comparison to each specific animal. The range of body lengths for the Howe Quarry specimens (2-3 -14 m) perhaps indicates that the scales of these animals (3 cm across) might be larger against body size than those of most other dinosaurs, but how visible they might be to observers is really dependent on knowing the sizes of the animals concerned. Likewise, the only published illustrations of these unique, interesting remains are pretty basic: it would be neat to get these specimens figured and described in a lot more detail. Hopefully, these details will be forthcoming soon.

The Sternberg/Osborn Edmontosaurus mummy

You can't discuss scaly dinosaurs without mentioning hadrosaurs. Research into hadrosaur skin is only second to that going into the fuzzballs at the other end of the dinosaur tree, there being so many skin impressions from these dinosaurs that we can gauge variation between species, see pathological skin tissues, and reconstruct virtually complete integuments for some taxa. This relative glut of data has spurned investigation into just why hadrosaur skin crops up so often. The exact cause remains elusive (it's seemingly unrelated to the rocks they occur in, nor their palaeoenvironmental or palaeoclimatic preferences), and it is suspected that there is something intrinsic to their skin anatomy which makes it more preservable (Davies 2012).

The amount of data we have for hadrosaur skin is really impressive. Here, in grey, you can see the skin impressions known for several hadrosaurid taxa: A, Brachylophosaurus canadensis; B, Edmontosaurus annectens; C, Gryposaurus notabilis; D, Maiasaura peeblesorum; E, Saurolophus angustirostris; F, Saurolophus osborni; G, Corythosaurus casuarius; H, Lambeosaurus lambei; I, Lambeosaurus magnicristatus; J, Parasaurolophus walkeri. From Bell (2014).

Even among hadrosaurids, Edmontosaurus annectens stands out as having particularly exemplar skin remains. Collectively, we have skin impressions from virtually its entire body (above). One of the most spectacular Edmontosaurus fossils with scaly remains has to be the "Trachodon mummy", discovered by George Sternberg (Charles Sternberg's son) in 1908 and described by Henry Fairfield Osborn in 1912. Osborn lavished attention on the integument of this near complete, fully articulated specimen, of which skin impressions covered the posterior jaws, neck, shoulders, chest, belly and forelimb. This specimen also revealed the presence of a low frill along at least the posterior part of the neck. Osborn's work on this animal stands out as a landmark document on extinct reptile integument, and interested parties really should download this article from the American Museum of Natural History here (NB. this is a 75 Mb download, it coming bundled with historic descriptions of the skulls of Tyrannosaurus and Allosaurus, whatever they are).

Pectoral (lower) and manual (upper) skin remains from the "Trachodon mummy" specimen. Notice the scales extending onto the unguals - these animals did not have nails or claws on their hands. From Osborn (1912).

Osborn's description revealed details of dinosaur skin which were, at that time, poorly known from other animals. He remarked on how thin the skin layer was and the remarkably small size of the scaly tubercles covering the body (1-5 mm). The fineness of the skin resulted in perhaps a third of it being accidentally destroyed during collection - 'dinosaur mummies' were an unknown quantity before this specimen, and collectors had no idea such data was at risk when skeletons were being uncovered. Edmontosaurus skin was a mosaic of larger and smaller tubercles, but their size variation is more continuous the obviously bimodal configurations of other species. The smaller (1-3 mm) tubercles were rounded structures located between larger (5-10 mm) hexagonal ones. Osborn called these 'pavement scales', and noted that they occurred in small (5-10 cm wide) clusters in some areas, such as the neck, inner surface of the arm and belly, but covered entire other parts of the body, such as the side of the chest, lateral surface of the arm and above the hips. The largest pavement scales, about 10 mm wide, occur on the lateral surface of the arm and tail. Both large and small scales occur on the frill (below). Folds, creases and smaller tubercles seem to correspond with intervertebral spaces, likely reflecting where these tissues flexed and creased with neck movement. The actual height of the frill is unknown from this specimen, the free margin being damaged during collection.

Osborn's illustration of the frill of Edmontosaurus. From Osborn (1912).

We could go on as there's so much detail on this specimen, but you're better off just checking out Osborn's description. He certainly provided lots of interesting details for artists: a visual summary of the distribution of larger and smaller scales in a cartoon hadrosaur (below), comments on his collaboration with Charles Knight to produce a 'trachodont' reconstruction in line with his new information on hadrosaur skin (also below), and even speculation on how pigmentation may pertain to the scale pattern. Of further interest is Osborn's comparison of the skin of Edmontosaurus with other hadrosaurs, this noting that the scales of his mummy specimen were a lot smaller than those of other, closely related animals. Other differences in hadrosaur skin texture has become even more apparent in subsequent years.

Left, Osborn's illustration of Edmontosaurus outlining the distribution of large scale clusters, with their size much enhanced for visibility; right, Charles Knight's iconic 1912 painting of the same taxon, an artwork produced in collaboration with Osborn and data from the "Trachodon mummy". From Osborn (1912) and The World of Charles R. Knight.

So, other than the obvious take-home - that we know a heck of a lot about the skin of Edmontosaurus -are there any obvious pointers for artists here? As noted for Carnotaurus above, it's doubtful that we'd be able to define individual scales or the patchy distribution of pavement scales on this large bodied (12-13 m long) species unless we were right next to it. Secondly, of all dinosaurs, surely this is one species to consider off limits to extensive filamentation. I suppose you could argue that filaments filled the few parts of this animal's hide left unrepresented in the fossil record, but that fuzz is going to look like weeds growing through a pavement if you're paying attention to where we know scales were. I also think it's worth paying attention to what Osborn meant by 'frill' along the back of this species: it does not appear to be a narrow, fibrous structure as commonly depicted, but a scaly continuation of adjacent dermal tissues.

The (unpublished) Triceratops superscales

I've saved what I consider to be one of the most interesting and impressive set of scale impressions for last, even though they are represented by specimens which have only currently received only very superficial publication through online news articles. These specimens belong to one of the most familiar and famous dinosaurs of all, the ceratopsid Triceratops horridus, and yet they demonstrate a scale topography completely unlike that of any other dinosaur. Their discovery is a particularly fun curve-ball because we have skin samples from a number of other ceratopsians, none of which are particularly like those now known for Triceratops. I'm reminded about earlier discussions of 'one skin fitting all': it seems ancient dinosaurs really could be just as varied in skin morphology as modern animals.

Huge patch of Triceratops skin, preserved as an internal mould - look at the size of the individual scales! Borrowed from the Rapid City Journal.

These extensive skin impressions were associated with one of the most complete Triceratops specimens ever found, a Wyoming individual known as 'Lane'. This specimen, including its skin, is now on display in the Houston Museum of Natural Science. Without a full description it's a little difficult to give much in the way of specifics about the skin, but published photographs reveal a network of very large (I'm estimating 50-60 mm wide based on the adjacent images) hexagonal tubercles dividing larger tubercles (perhaps c. 100 mm) with central, conical projections. These large scales are sometimes described being as 'nipple-like', for obvious reasons. Divisions between these tightly interlocked scales are marked, and we might have been able to distinguish individual scales on these animals from some distance away. The function of the larger tubercles with their prominences has been the source of much speculation in art - do these structures represent bosses and low spikes, or tubular supports for large, coarse filaments? I must admit to considering the latter unlikely as neither hair or scales in modern animals grow through scales, but instead around them. I'm happy to be wrong on this, though, and both interpretations could be easily tested by looking for apertures at the tip of each prominence. Hopefully these specimens will get a full write up soon, which might provide such details.

Detail of the large tubercles adorning the outside of Triceratops. Also borrowed from the Rapid City Journal.

Lane's skin impressions suggest that the scales of Triceratops were characteristically coarser, certainly a lot larger and perhaps more sculpted than those of most other dinosaurs. Their overall appearance is very different to the hadrosaur and theropod skin mentioned here, contrasts markedly from the scales known from other ceratopsians, and is rather unexpectedly most similar to the scales of sauropods. It's difficult not to intuitively equate Triceratops skin with that rhinos and armadillos: there's something almost armour-like about those heavy scales and low, projecting bosses. Perhaps this chimes with the unusually solid, reinforced cranial frill we find in this species - was Triceratops something of a horned dinosaur tank? I reckon there's a lot of fun to be had with depicting this animal as looking particularly tough and grizzled, with big skin creases and heavy folds - such a depiction can be seen at the top of this article. It's perhaps worth noting that the actual appearance of Triceratops is not a million miles off the Charles Knight's famous painting of 'Agathaumas' (probably = Triceratops) with its speculative heavy scaling.

Summary time

I hope what's becoming clear here is that we can obtain quite a lot of information from dinosaur skin impressions, and that they show scaly dinosaur species have their own characteristic integuments in the same way that filamentous ones do. There really doesn't seem to be a 'standard' type of dinosaur scale, and even closely related species show some significant variation between them. We have to conclude that those of us hoping to restore these animals accurately really need to pay close attention to these data, considering variation in tubercle size, texture and distribution. I particularly emphasise this for artists who draw every scale: if that's the route you're taking, make sure you're drawing them correctly! Moreover, the specimens outlined here are good reasons to be inventive when skin impressions are lacking. It seems most relatively extensive skin impressions of scaly dinosaurs reveal things like spines, keeled scales, armour-like structures, frilled projections and so on. Mesozoic dinosaur skin must've been as interesting as that of modern reptiles, and we might expect many species to have elaborate structures of some kind.

And that's it for 2015

OK folks, we're done here for this year, but there's plenty more to come in 2016. Weird archosauromorphs, stem mammals, some retropalaeoart and the publication of Recreating an Age of Reptiles will be covered early on. Huge thanks to everyone who's been reading and supporting this blog throughout 2015 - I hope you've enjoyed what I considered to be one of my best blogging years so far. All the best to you all for the festive period, and see you all in 2016!

References

• Bonaparte, J. F., Novas, F. E., & Coria, R. A. (1990). Carnotaurus sastrei Bonaparte, the horned, lightly built carnosaur from the Middle Cretaceous of Patagonia. Contributions in Science. Natural History Museum of Los Angeles County, 416, 1-42.
• Czerkas, S. A. (1992). Discovery of dermal spines reveals a new look for sauropod dinosaurs. Geology, 20(12), 1068-1070.
• Davis, M. (2012). Census of dinosaur skin reveals lithology may not be the most important factor in increased preservation of hadrosaurid skin. Acta Palaeontologica Polonica, 59(3), 601-605.
• Osborn, H. F. (1912). Integument of the iguanodont dinosaur Trachodon. Memoirs of the American Museum of Natural History v. 1

Overexposure of Stegosaurus, but in a good way

Is it just me, or are stegosaurs not quite as popular as they used to be? Stegosaurs are iconic dinosaur species that, like tyrannosaurs and ceratopsids, have been drawn to death by generations of palaeoartists eager to capture their freakishly weird anatomy, but they don't seem to be quite the mainstay of dinosaur pop culture that they used to be. I could be wrong, but it seems that other dinosaur taxa, primarily feathery, near-birdy things, have take a share of the stegosaur limelight. Perhaps stegosaurs, and particularly Stegosaurus, are just a so  familiar now that we've become a bit blasé about them. I know I certainly have, so I've not sketched or painted one in years. It was only in revisiting them for this piece that it struck me how freakin' weird stegosaurs are, even in this world of therizinosaurs, mononykosaurs and four-winged microraptors. The front of their bodies clearly belong to relatively small or medium-sized animals, but evolution thought it would be fun to give them hindquarters borrowed from an large elephant or small sauropod. Supporting the dainty head and neck is a set of seemingly well-engineered but overly-short forelimbs, which force their spinal columns into high, curving arches to span the height discrepancy between each limb set. And then there's the osteoderms, shaped into broad plates or spikes, which sit along their backs and may turn the distal end of the tail into a morning star. Stegosaurs make feathery maniraptorans look positively boring.

For this painting, I wanted to show a stegosaur - specifically the Upper Jurassic Morrison Formation species Stegosaurus stenops - with some real character, looking like it had lived a hard life in an unforgiving climate and surrounded by extreme and frequently dangerous animals. For this reason, I chose a rarely depicted, more or less head on aspect for the painting, thus bringing its tiny head to the fore, allowing us to see its face without forgetting that the body behind it was large and powerful. I imagine that standing next to a big stegosaurs should be like standing next to any big, unfamiliar animal. It may not eat you, but the feeling that we're a small, inferior species, and that the 6 tonne animal next to us has absolute right of way, will never disappear. There also seemed to be a lot that could be done with its appearance. Stegosaurus was a large enough animal that they were probably fairly long-lived, and would accumulate decades of wear-and-tear on their hides. Thus, I depicted his very imperfect skin with an extremely washed-out but high contrast colour scheme, in efforts to enhance his battered appearance. Fossil evidence also came into play with creating a history for this animal, as we have good evidence that stegosaur osteoderms were occasionally subject to extreme damage in life, perhaps because they were bitten by predators or, in the case of their defensive tail spines, winged into the side of assailants with enough force to break their tips (Carpenter et al. 2005). With this in mind, my stegosaur has a number of broken plates along its back, this animal having seen off its fair share of aggressors. At one point, he was also going to be depicted drooling long strands of spittle through heat-stress, but the effect wasn't quite in keeping with his posture, so I took a napkin to his beak and tidied him up (see detail, below).

I also thought it might be fun to play with the scaly depiction of stegosaurs a bit, decking the thagomizer out with a set of long, bright filaments. Excellent skin impressions from Morrison stegosaurs (possibly even from Stegosaurus itself, if the assessment of stegosaur taxonomy by Maidment et al. [2008] is correct) reveal that their bodies were covered, probably mostly, in typically archosaurian pebbly scales (Christiansen and Tschopp 2010). This integument is exactly what we would expect from a large ornithischian in a warm climate. As with many dinosaurs, their scales are of variable size across the body, with long rows of large (20 mm wide) scales stretching across the dorsal regions and smaller scales lining the belly (see image, below). By analogy with modern 'naked' mammals however, I wondered if some scaly dinosaurs would retain small regions of fuzziness from their ancestors for specific functions. The bushy tails, ear tufts and eyelashes of naked mammals are good analogues here. In this case, my stegosaur's thagomizer isn't bristly to swat flies as are the hairy tail tips of mammals, but to advertise its spikes to marauding predators, and make them think twice about attempting an attack. Further analogy can be made here with the striking colours of many poisonous or otherwise well defended animals: camouflage is thrown to the wind in favour of making themselves unmistakeable to predators, letting them know to think twice about attacking them. Additional uses for fuzzy thagomizers may be sociosexual display, dusting hard to reach shelves and corners or, perhaps for defensively tickling they way out of hairy situations (hat tip to Spike Ekins and Simon Clabby for the latter).

Stegosaur skin impressions, probably from Stegosaurus, from Christiansen and Tschopp (2010). Top, belly scales, bottom, large scale surrounded by smaller, satellite scales. Scale bars represent 20 mm (top) and 10 mm (bottom).

And speaking of patchy filament distribution, I also gave this guy eyelashes, but you can't really see them in all the shadow I then layered over the top. Eyelashes may seem very odd things to put on dinosaurs, but they are common features of animals that have fuzzy ancestors. Numerous bird species have specially adapted feathers which are functionally analogous to mammal eyelashes, for instance. At least hornbills, secretary birds, seriemas, parrots, roadrunners and ostriches bear them, which serve to  trigger blinking when touched (as in mammals) and, in some species, shade the eye. Eyelashes are also frequently retained in mammals that have mostly or entirely lost their fur: elephants, rhinos, hippos, you, and others. Thus, it seems quite plausible that many dinosaurs and other ornithodirans had eyelash-like filaments, and that some scaly dinosaurs will have held onto them.

Right, that's a reasonably concise post for these parts, and will have to do for now: I need to get going with a big palaeoart project that will, coincidentally, also require some consideration of ornithodiran eyelashes. If I'm allowed, there may even be some bits of it being posted here before any of us are too much older.

References

• Carpenter, K., Sanders, F., McWhinney, L., and Wood, L. 2005. Evidence for predator-prey relationships: Examples for Allosaurus and Stegosaurus. In Carpenter, K. (Ed). The Carnivorous Dinosaurs. Indiana University Press. pp. 325–50.
• Christiansen, N. A., and Tschopp, E. 2010. Exceptional stegosaur integument impressions from the Upper Jurassic Morrison Formation of Wyoming. Swiss Journal of Geosciences, 103, 163-171.
• Maidment, S. C., Norman, D. B., Barrett, P. M., and Upchurch, P. 2008. Systematics and phylogeny of Stegosauria (Dinosauria: Ornithischia). Journal of Systematic Palaeontology, 6, 367-407.

Skin-deep: the 'One Skin Fits All' approach to integument reconstruction in palaeoart

The snowy, chilly plains of Maastrichtian Alaska, where Pachyrhinosaurus perotorum roamed. But were they scaly like other ceratopsids, or covered in protofeathers, as shown here?

So... no pressure here, then. I innocently replaced my festive Facebook profile picture with some detail from the painting above last Sunday (07/01/13) and quickly found a storm (well, gusty conditions) of discussion, 'likings' and shares, with several folks mentioning their anticipation of this post to see what all the fuss is about. The Facebook responses have been interesting and mixed: nods of approval, some head-slapping 'why didn't I think of that', a revelation that Tom Hopp already did this last year and, perhaps more predictably, scepticism from a number of individuals who consider the whole concept very silly indeed. In short, there seems to be a certain amount of expectation in the air about this image, and I wouldn't be surprised if some virtual beer bottles are hurled at me across the Internet should this explanation not prove convincing. Here's hoping I've done my homework properly, then.

The painting in question shows a family of the Alaskan centrosaurine Pachyrhinosaurus perotorum, a species notable for its existence in rather chilly, latest Cretaceous climates at palaeolatitudes of 80-90°. It differs from other pictures of this species by having its Muskox Quotient upped by 500%, replacing the scaly hides of more traditional Pachyrhinosaurus reconstructions with a blanket of fuzz analogous to the fuzzy, unkempt feathers of modern ratites. Fuzzy polar dinosaurs are not unusual in palaeoart nowadays and they result in animals that look immediately more at home in icy, subfreezing climates than their scaly brethren. This image, however, directly contradicts what most folks will say we know about horned dinosaur integument. Some comments on Facebook have already wheeled this argument out: known ceratopsian integuments were predominately scaly, so the concept of a shaggy pachyrhinosaur is nonsense, right? Well, I'm going to argue here that it's not, or at least not a concept that is easily dismissed. Before we go any further, it's worth stressing that I'm not presenting this image as the new 'standard' for Pachyrhinosaurus perotorum: I don't know of any new evidence that confirms the shaggy hides shown here, be it soft-tissue remains of ceratopsids or a new interpretation of dinosaur evolution that suggests super-fuzzy ornithischians were common. Nor, for that matter, do I have the heads up on research indicating that latest Cretaceous Alaskan palaeoclimates were much lower than expected. Instead, across four points, I'm going to argue that, based on what we know of dinosaur evolution, the responses of modern animals to their environments, and - importantly - the vast gulf of unknown data regarding dinosaur appearance, that this concept is as plausible as our scaly variants and, in some respects, may be more plausible. On the way, I'm going to suggest that, as with some other considerations in palaeoart, we may be too conservative when it comes to depicting animal integuments, because we focus too much on their evolutionary relationships without considering their likely adaptations to habitats and lifestyles. Hmm... this is all starting to sound very All Yesterdays, isn't it? That's not a coincidence.

1) Ornithischians were fuzzy, and some were probably fuzzier than others.
First up, the least controversial pin in this case. Thanks to Tianyulong and the early ceratopsian Psittacosaurus, we know that ornithischians were covered in more than just scales, the former being covered in filamentous structures akin to early feathers and the latter possessing long quills (Mayr et al. 2002; Zheng et al. 2009) Accordingly, it's now fairly fashionable, and by no means unreasonable, to restore even large ceratopsids with at least a smattering of quills across their bodies like those seen on Psittacosaurus, reflecting a relict integument from an earlier phase of their evolutionary history. It naturally follows that we should expect some taxa to have been more densely adorned with filaments and quills than others, just as fur and feathers are of variable densities in modern species. Accordingly, while a shaggy pachyrhinosaur is certainly at the 'extreme' end of our predictions for an ornithischian integument, it does not directly contradict anything we know regarding dinosaur evolution. Ceratopsids probably had the appropriate genetic blueprints to produce a shaggy animal, so long as the right conditions promoted its expression. There is a question of how appropriate it is to cover a ceratopsid in shaggy integumentary structures however, in light of preserved skin impressions of other ceratopsids. How likely is it that any horned dinosaurs were fuzzy?



Fossil integument of Chasmosaurus belli. From Sternberg 1925.

2) Is the extrapolation of preserved integuments to other species that reliable, really?
Skin impressions and the remains of other integumentary structures are Holy Grails to palaeoartists, and we use them extensively in restoring extinct animals. Through phylogenetic bracketing, or use of their basic phylogenetic proxy when less data is available, we stretch these remains over entire clades so that the known integument of one species becomes the norm for an entire group - what I'll call 'One Skin Fits All' approach. Thus, because we have scaly skin impressions for three ceratopsids - Centrosaurus, Triceratops and Chasmosaurus (see image, above, of the latter. From Sternberg 1925), it's assumed that scales were common to the entire clade. There's nothing necessarily wrong with this assessment and, one may argue, it's the most parsimonious way to interpret this data. A stick in the mud, however, is that another dataset, the diversity of integuments in modern animals, suggests that integuments can vary wildly within groups, and that we could be vastly underestimating the integumentary variation in extinct animals.

Consider the different varieties of fluff, fur, feathers, hair, bristles and other fuzzes in a group of modern animals and then think how a future palaeoartist would reconstruct all varieties of that group if they only had access to only one or two examples of integument. Perhaps all reconstructions of bovids would have woolly coats like those of sheep, or, conversely, the sparse, almost naked skin like a water buffalo? We may deck all primates out in the long capes of colobus monkeys, all pigs with boar-like fur, or cover every inch of birds with feathers. We know such approaches are wrong because these groups demonstrably show variation in the distribution, length and structure of their varying integuments, and yet we maintain a One Skin Fits All' approach to fossil clades. We can't even play the 'extremely close relationship card' in this game as the likes of woolly mammoths, and the fuzzy Sumatran and woolly rhinos, show vastly different integuments to their closest, naked relatives.

One could counter this point by arguing that the relative abundance of scaly remains in certain dinosaur lineages suggest that most, if not all members of that clan were scaly. Perhaps, but we should consider both the sample sizes here and the taphonomic window through which fossils are passed to the modern day. We have, at best, skin impressions from a handful of species compared to the group diversity, so statistical support for the 'One Skin Fits All' approach is low. Moreover, which types of skin are more likely to be preserved? Taphonomic observations on modern animals suggest that fur and feathers are easily removed from carcasses by biological or physical processes, so their preservation potential in ancient animals is low outside of fossil Lagerstätten. Is it a coincidence that the only skin impressions we find outside of Lagerstätten are scaly, leathery hides? I don't have the answer to that question, but it's worth chewing over.

With all this in mind, I wonder if applying the fossil integuments of one species to all its relatives, even close ones, is a questionable practise. I'm not saying that skin impressions are useless and that we should pay them no attention, but we should remember that they only highlight possibilities and perhaps some degree of probability for integumentary structures in a related species. They may well also have no bearing whatsoever on the appearance of their relatives. We're dealing with a great amount of unknown data when reconstructing ancient integuments, and we know how complex this issue is through modern species. When applying this thought to horned dinosaurs, we can say that the scaly skin impressions we have for a few species demonstrate that some bore scales, but we cannot rule out the possibility that others were covered in entirely different structures, like the quills and fuzz that seem deeply rooted in dinosaur ancestry. It does seem likely that many centrosaurines heads, including Pachyrhinosaurus, bore heavily keratinised scales and pads (Hieronymus et al. 2009), but, of course, this doesn't tell us much about the rest of the body. The majority of skin in Pachyrhinosaurus could be scaly, fuzzy, or anywhere inbetween. Without skin impressions to directly tell us the integument of specific species, there's no way to be sure. We need to be careful that we do not afflict ourselves with palaeoartistic phyloblindness here, by only considering these animals as denizens of cladograms and evolutionary hypotheses. Phylogenies may tell us what is possible for integument reconstructions, but other factors may help us decide is more probable.

3) Phylogeny is far from the only factor controlling integument, and can be readily overruled
It's funny to think that, for all the time we spend looking at the phylogenies of extinct animals, we're often missing much about the raw power that drove their evolution: adaptation. This is probably because we're lacking so much anatomical detail in their fossils that their responses to even broad environmental changes are largely undetectable, so understanding why they change through time is not always as certain as how. Nevertheless, we can be sure that different environments drove modification to the anatomy of extinct lineages on small and large scales, and integuments were likely to be one of the most affected tissues. Animal integuments are critical interfaces between body and environment, and have to be appropriately adapted for given habitats. This is a readily observable phenomenon in modern animals, because their integuments reflect all sorts of environmental factors including sun exposure, temperature, local vegetation types, water availability, parasite prevalence, and their local predators. Presumably, this is why such variation in integument exists in even closely related species. But we frequently reconstruct fossil species as if they all live in the same place. Sedimentological and isotope data reveals that closely related ancient species sometimes lived in starkly contrasting settings, but because we frequently take the 'One Skin Fits All' approach, our animals look very similar, irrespective of the requirements of their habitats.

Hot Fuzz: a reference to the condensing breath of the animal, the controversial concept depicted here, or just an excuse for a bad pun? Whatever: it's an excuse to link to this clip from Hot Fuzz: Best. Granny. Kick. Ever.

Behaviour may also have an effect on integument. Sun-shy, non-aggressive and cursorial animals may well bear thinner integuments than slower, frequently exposed or bad-tempered species, for instance. Morphology, too, will have an influence, with larger animals having lessened needs for insulation or being capable of carrying heavier, armoured hides. These are all things palaeoartists should be considering when reconstructing extinct animals: they should look adapted to the lifestyles we predict for them, rather than being based on phylogenetic hypotheses alone. Perhaps some desert-living dinosaurs had elephant-like, deeply wrinkled skin to help heat dissipation, while smaller desert-dwellers had extremely short feathers, or none at all, to prevent overheating. Maybe large theropods had heavy scales on their faces to defend themselves during bouts of head biting. We don't know for sure, but we can be certain that these species had to be appropriately adapted for wherever and however they lived. In short, we need to be wary reconstructing our ancient species by cladogram alone, and realise that integuments, and soft-tissue anatomies in general, should reflect a combination of phylogenetic data and possible adaptations to habitats and lifestyles. This, undoubtedly, involves some of the 'informed speculation' that has been discussed so much with All Yesterdays, but the results are more consistent with our knowledge of modern animals and evolution generally, and arguably producing a more convincing look into the ancient world ('convincing' is the right word here: I'm not sure we're ever going to get 'accurate' results in this game). In fact, after mulling this over for some time, I find the typical and conservative, 'One Skin Fits All' approach much harder to defend than the more open minded, environmentally-influenced reconstructions argued for here.

Bringing this back to our fuzzy pachyrhinosaurs, we again have to question the how applicable the currently available ceratopsid skin impressions are to this Alaskan species. The scaly hides of Chasmosaurus, Centrosaurus and Triceratops represent animals living in more southerly regions than Pachyrhinosaurus, which were at least temperate to subtropical in climate. The former two taxa also lived somewhat before Pachyrhinosaurus, when global temperatures were, on average, a little warmer. These sub-arctic coastal plains encountered by Pachyrhinosaurus perotorum, by contrast, were much cooler, and sometimes genuinely cold. Accordingly, the selection pressures on integument may have been very different for P. perotorum compared to these warm-climate ceratopsids, and we have to wonder how suitable the skin impressions of Chasmosaurus et al. are for reconstructions of Pachyrhinosaurus. We wouldn't, after all, expect the integument of a yak to resemble that of a African buffalo, or consider the fur of a lithe gazelle a suitable model for mountain goat fur. With this philosophy in mind, the question of shaggy pachyrhinosaurs shifts focus from arguments about the cladograms and the skin impressions of their relatives, and on to whether or not Late Cretaceous Alaska was cold enough to promote the development of an extreme integument adaptation in a large dinosaur species.

4) Late Cretaceous Alaska: a struggle for any tourist board
Although nowhere near as bleak as our modern Alaska, the dinosaur faunas inhabiting the northern reaches of latest Cretaceous Alaska would have experienced fairly grim weather for much of the time, perhaps akin to that experienced by modern animals living on the northwest coast of Canada or the more depressing parts of Scotland. In a recent review based on palaeobotanical data from the Cretaceous Arctic, Spicer and Herman (2010) suggested that uppermost Cretaceous Alaska experienced mean average temperatures around 6°C, with summer months attaining a comfortable 14.5°C, but winter months dropping to an average of -2°C. The Pachyrhinosaurus perotorum-bearing Prince Creek Formation may have been a little cooler than other parts of the Late Cretaceous arctic circle, with a mean average temperature between 2.5-5°C. Winter lasts a long time at 80-90° latitude, with 5 of darkness bracketed by 2 months of twilight. A permanent cloud cap over the Late Cretaceous Arctic (detected by the oversize nature of the fossil plant leaves from Cretaceous Alaskan localities) acted as a atmospheric blanket for the region, prohibiting temperatures from plummeting below freezing low for long period. The lowest temperatures - perhaps -10°C - may not have lasted more than a few weeks. Evidence for deep freezes is absent however, with neither the sedimentological or palaeobotanical record indicating nothing more severe than week-long frosts and light freezes. Despite this, rain and snow were probably common, with relative humidity averaging about 80% and even the driest months of the year experiencing over 180 mm of rain. The collective three wettest months, by contrast, collected almost 800 mm. (To put this in perspective, rain-soaked England has an average annual rainfall of 854 mm, according to the UK Met Office [via Wikipedia]). Such a climate was capable of supporting a rich array of plantlife, and evergreen taiga-like forests were common, as were swamps, rivers and other bodies of water. Such conditions seem fairly common right the way through Late Cretaceous Alaska, with conditions a full 8° south of the Prince Creek Formation seeming similarly cold and wet. I should add that this consideration of ancient Alaska  isn't particularly controversial, the palaeobotanical data mentioned here matching palaeoclimate models based on isotope records, animal distribution and sedimentology.

So the Prince Creek palaeoenviroment wasn't exactly an ideal holiday spot, but was it 'extreme' enough to promote the evolution of an fuzzy coat in a 1.5-2 tonne dinosaur species? Given the dense furs we see in large mammals found in similar climates, I think it's certainly a possibility. It would certainly be far weirder if polar dinosaurs of the Late Cretaceous didn't respond to their climate somehow, and a thick coat of protofeathers is one possible adaptation to their cool, wet habitat. A layer of insulating fat would be another (cue an image of some tubby pachyrhinosaurs). Of course, the picture may be different if these animals hibernated or migrated in and out of Alaska annually, enjoying the brief mild period before heading south to escape the winter. The latter is perhaps the most widely discussed concept, but direct evidence for such migrations in Alaskan dinosaurs is as sparse as evidence for their fluffy integuments or fat layers. In the concept proposed here, the protofeather coat may have acted as an insulator against the cold, prevented wind, rain and snow from hitting the naked skin of the animal, or both. The latter function would benefit from the coat being thick and fluffy, but this may not have lead to overheating even in a big animal like Pachyrhinosaurus: the ragged, loose coats of hot-climate adapted ratites appear similarly thick and massive without overheating their owners. Perhaps the concept of shaggy coats in these Alaskan dinosaurs doesn't seem so as implausible as it may first appear, then.

To bring this more-mammoth-than-intended essay to a close, then, I again stress that I'm not saying 'this is what Pachyrhinosaurus looked like!', but attempting to present it as a product of both its phylogenetic history, its environment and habits, and not simply reconstructed via a cladogram. I think there's a lot of scope for these sorts of palaeoartistic renditions, even it does mean more reliance on the 'informed speculation' principle of All Yesterdays. Of course, this whole argument flows back to the core idea behind the All Yesterdays movement: the conservative, 'One Skin Fits All' approach to integument reconstruction is just as likely to be wrong as our more speculative concepts, but at least the use of informed speculation lines the reconstruction up with our knowledge of modern animal diversity.

References

• Hieronymus, T. L., Witmer, L. M., Tanke, D. H. and Currie, P. J. 2009. The facial integument of centrosaurine ceratopsids: morphological and histological correlates of novel skin structures. Anatomical Record, 292, 1370–1396.
• Mayr, G., Peters, D. S., Plodowski, G. and Vogel, O. 2002. Bristle-like integumentary structures at the tail of the horned dinosaur Psittacosaurus. Naturwissenschaften 89, 361–365.
• Spicer, R. A. and Herman, A. B. 2010. The Late Cretaceous environment of the Arctic: A quantitative reassessment based on plant fossils. Palaeogeography, Palaeoclimatology, Palaeoecology, 295, 423–442.
• Sternberg, C. 1925. Integument of Chasmosaurus belli. The Canadian Field-Naturalist, 39, 108-1 10.
• Zheng, X., You, H., Xu, X. and Dong, Z. 2009. An Early Cretaceous heterodontosaurid dinosaur with filamentous integumentary structures. Nature, 458, 333–336.