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Friday, 28 July 2017

Palaeoartist interview: Johan Egerkrans

Palaeoart has never been a particularly diverse artform. Since the early 1800s most palaeoartists have pursued art attempting to depict fossil animals in realistic ways, with stylistic variation mostly along the spectrum of how obvious our brush strokes and pencil lines are, and how much detail we add. In recent decades we've seen artists deepening their dedication to realism with hyperrealist palaeoart, artworks which look like they've been snapped by high-speed cameras with crisp focuses and ultra-high levels of detail.

But not all palaeoartists are taking this approach. Some take a step away from not only high levels of detail but also realism, producing palaeoart with a more stylised and even abstract bent. Though few in number, the growing roster of ‘stylised’ palaeoartists represent an exciting new frontier for palaeoart. In varying artworks along spectra other than tidiness and detailing, these artists are producing unconventional works recalling pop art, classic western animations, heraldic crests, perspectiveless Medieval art and more. Among the most fascinating aspects of these works is their capacity to maintain respect for scientific credibility even when producing stylised, non-realist art. The forms may be simple or sharply angular, the colours may be garish, but we can still tell what the subjects are, what they are doing, and get a sense of their anatomy.

...which brings us to Johan Egerkrans's Alla tiders dinosaurier. If you like stylised palaeoart, you should check out this book. 
Swedish artist Johan Egerkrans is part of this emerging group of unconventional palaeoartists. Emerging onto the online palaeoart scene only recently, his work has already generated a fanbase and widespread acclaim. It's easy to see the appeal of his creations. Distinctively angular, full of personality and recalling great works of American animation, his digital artworks emphasise and almost caricature the form of fossil animals without undue distortion of their form or disregarding fossil data. Attention to details, anatomy and colours make his work interesting to look at despite it's simplicity compared to traditional modern palaeoart. We're not just seeing generic cartoons of fossil animals, but highly stylised versions of contemporary, scientifically credible palaeoart, informed by a clear appreciation for modern wildlife and the natural world. Notice the pupil colour change between his adult and juvenile Microraptor (below), variable integuments on Gorgosaurus (above), fine attention to animal poses and behaviour, and so on. His use of traditional compositions and poses prevent his work becoming overbearing: in this regard, his work is less intrusive, and even perhaps less cartoony, than some artists employing ‘realistic’ animals in hyper-dynamic poses and compositions.

Egerkrans' parent and offspring Microraptor. Look past the stylisation and this is a pretty accurate take on Microraptor anatomy, right down to the iridescent black plumage. Note the pin feathers and dark pupil on the juvenile - very sensible speculations for juvenile maniraptorans. © Johan Egerkrans.
Each Egerkrans work radiates personality: his animals have real character, and it’s almost impossible not to imagine them taking part in animated vignettes. Several of his works have a strong sense of mischief and dark humour, another rarity among palaeoartworks. I’m particularly tickled by his scene of a capybara running away from terror bird Titanis (below): the bird has a mania that captures real birds at their most frantic and chaotic, while the drab mammal looks overwrought, panicked, but also like it’s going to write a strongly worded letter to the Daily Mail about all this. Comparisons of Egerkrans’ creations to stylised fossil animals rendered for the big screen are inevitable, and mostly leave us wondering what the heck everyone else is doing wrong. Hollywood, give this man a job!

Titanis and capybara star in Hilarious Scene of Violence. Capybara won an Oscar for its eyebrows. © Johan Egerkrans.
Johan was kind enough to send me a copy of his recent book, Alla tiders dinosaurier, which I thoroughly recommend you check out. There’s no English translation at the moment (one might happen at some point) but the artwork speaks volumes alone and the design and print quality is excellent - it's a nice book to have, even if you're unable to read the text. The follow up, Flygödlor och havsmonster, which focuses on marine reptiles and pterosaurs, is due out later this year. Both are published by B Wahlstroms, and can be purchased from Bokus and other Swedish book retailers (sorry, American readers, there are complications around shipping these books to the USA at the moment). You can check out the art of both books on Facebook, Artstation and Johan's blog. If you're Stockholm-based, you can also check out a dinosaur exhibition featuring the Alla tiders dinosaurier work, which is running until the end of September.

Earlier this month I asked Johan if he’d like to chat to me about his art, books and palaeoart philosophy, and he’s taken time out of his schedule to give the following interview. With thanks to him for taking time to respond to my questions, it’s time for me to stop gushing about his work and hand you over to the man himself…

MW. You’re quite new to the palaeoart scene, but have landed an instant fanbase with your highly distinctive artwork. Can you give us some insight into your artistic background and what brought you into restoring dinosaurs, pterosaurs and so on?

JE. Hi Mark! Thanks for having me on the show!

I started out as a concept artist and, like most people in that field it seems, I´ve nursed  a deeply rooted fascination for paleoart since... Well, forever I guess. At the age of four my dad gave me Burian´s seminal art book “Life Before Man” and that was it; I was hooked and filled countless A4 sheets with scribblings of dinosaurs, therapsids, pterosaurs and other extinct beasties. I´ve still got that same cherished tome in my bookshelf, worn and coming apart at the seams.

Fast forward to the early 2000´s when I got my first fulltime job as an illustrator concepting for a small computer game outfit called Idol here in my hometown Stockholm. There I did designs for monsters, robots, spaceships and stuff like that. A high point was when I got to draw a series of - listen to this - demonically possessed cyborg dinosaurs!  That´s about as awesomebro as things can get. Take that Michael Bay!

I was always had a talent for mimicking different art styles, which came in very handy at that job - one month you did a superhero game in a highly stylised Bruce Timm style, another month it was horror inspired by Clive Barker, Frazettaesque fantasy or something completely different. I really got to flex those versatility muscles in that environment.

Anyway, after a couple of years Idol went belly up, as small computer game outfits are wont to do. I became a freelance illustrator and found myself working more and more with children´s books. In 2013 Nordiska väsen/Vaesen was released - a book about creatures from Scandinavian folklore that I wrote and illustrated. That really was a watershed moment, as the book did rather well (still does - it's sold over 40.000 copies in Sweden alone so far). After that success I had a certain amount of freedom and one of the things I wanted to do was to go back to my paleoart roots in some fashion. The first such project was a children´s picture book called My first book of dinosaurs. It was originally intended to be a rather tongue-in-cheek affair and the initial pictures were intentionally tropey (large theropod roaring on cliff, cassowary Oviraptor). I did take care to stay off the beaten path though so, unusually for a book aimed at young children, there wasn't a T. rex or Triceratops in sight - I went with Giganotosaurus and Styracosaurus instead.

Mention the tropes, and they shall appear. Egerkrans' Smilodon bellowing off a cliff (or maybe suffering a major case of lockjaw). It's difficult not to see this as satirising the most traditional means of restoring sabre-toothed cats: the lower jaw stretched so far as to make its tissues near invisible, and the skull arcing upwards to attain more ferociousness. Image © Johan Egerkrans.
Pretty soon my science geek side kicked in - I did more and more research and realised I wanted the reconstructions to have a certain amount of scientific accuracy, even if the book was aimed at toddlers. The cartoony stylised style I had chosen for the book could be tweaked into some something more “serious” while still retaining the whimsy and charm of those first illustrations. My first book of dinosaurs was followed by a another one about Cenozoic beasts and by this time I had gotten wind of the All Yesterdays movement and had started following a bunch of paleoblogs (this one and Tet Zoo among them). This new wave of paleoart and the philosophy behind it appealed to me. My editor and I decided to do a “real” pop science book about dinosaurs which was released as Alla tiders dinosaurier ("Dinosaurs of All Ages") earlier this year. I´m currently racing towards the finish on the follow up about pterosaurs and Mesozoic marine reptiles.

MW. Strongly stylised palaeoart is rare, perhaps because we focus so rigidly on precision and scientific credibility in our reconstructions. Where do you draw the line between style and adherence to science, and are there cases where you’ve thought ‘screw science, this looks cooler!’

JE. My aim, in a way, is to do what Disney animators did in films like The Jungle Book or The Lion King. Now, Shere Khaan might not be realistic per se, but the design is informed by a deep understanding of tiger anatomy, and what tigers are like - their “essence” if you will, with the risk of sounding a tad pretentious. Thus Shere Khaan becomes the tigeriest tiger around as far as I´m concerned. My paleoart sort of tries to do something similar - only with extinct animals (though I´m nowhere near as talented as those old school Disney animators). To capture that “essence” you sometimes got to break the rules a bit. It´s a “know the rules to break the rules” kinda deal.

It´s a bit like caricatures come to think of it. People often find it easier to recognise a celebrity from a (well made) caricature than from a photo because the drawing exaggerates that person's distinguishing features. In a similar way stylisation allows me to focus on what’s distinctive about a certain species/genus and bring that up to front.

Parvicursor, from Alla tiders Dinosaurier, is a great example of Egerkrans' capacity to find the essential elements of form in an extinct animal and project them through a strong visual style. © Johan Egerkrans.
Another advantage is that it allows me to remain vague when we’re uncertain about some feature of an animal's anatomy. Take for instance the recent dispute whether tyrannosaurs had lips or croclike exposed teeth. The simplified style allows me to draw something in-between, should I so wish, and leave it open to interpretation. That doesn’t mean I do this all the time and never takes a stand, but it remains an option.

A lot of paleoart seems rather overworked. I´m hardly the first to voice this opinion but meticulously rendering thousands of  tiny scales in a dinosaur picture doesn't necessarily make said picture more accurate. Sometimes it´s the complete opposite where hyperrealism only serves to create the illusion of scientific accuracy. I tend to prefer sketchier, looser paleoart - by artists like John Conway, Simon Stålenhag and of course Zdeněk Burian - where the emphasis lies on movement, mood and communicating that aforementioned essence of an animal - what it felt like.

My most common “screw-you-science” is probably the eyes. The peepers of my stem-birds are more mobile than they probably were in real life; they move around and look at things in a human, or at least mammalian way. Avian eyes are usually fixed in a perpetual stare which makes them come off as either vexed or insane (or both). That might be precisely what you’re after, but often you’re looking for something different. I almost always give the animals discernible pupils as we humans are geared to interpret that as more affective than-all black eyes. Windows to the soul and all that.

MW. Your reconstructions are full of personality and humour. I find it very easy to project emotion onto your subjects. Is this something you deliberately seek with your work? Do you render each image with an idea about what each animal is thinking?

JE. I´ve always had a flair for characterisation. It just sort of happens no matter what I draw, be it a robot, a dragon or a lone animal hanging about doing nothing. They always end up seeming to be up to something (my subjects often look rather smug for some reason, apparently it´s my go-to emotion). There´s a hint of anthropomorphism but I try not to overdo it. It´s just little things like an eye ridge tweaked to look as if the animal is raising it´s eyebrows or the hint of a smirk at the corner of the mouth. It should only be just enough to help the viewer empathise with the subject.

MW. The colour choices of your artwork are interesting, blending ‘realistic’ animal colour schemes with background hues rarely seen in palaeoart. It works very effectively, creating a strong sense of atmosphere. Can you take us through your approach to choosing animal colouration and blending these with often contrasting backgrounds?

JE. I always start with the animal itself and let their colouration dictate the tones of the background. The aim is to give them striking, simple colour schemes that still comes off as believable. Once the animal is painted I start with the surrounding environment, which on the whole is a rather intuitive and organic process. I play around in Photoshop until I land in something that works.

The colour choices and compositions are highly influenced by animation backgrounds, especially in the way the scenes are framed. There´s a lot of colour theory at work as well - complementary colors (often good old orange and teal) or split complementary colours (like red and blue) in different overlay layers make the animals “pop” from the background. A cool coloured animal will be framed by a warmer environment and vice versa.

Dimorphodon meets a neighbour (notice the keratin crest on the lower jaw of Dimorphodon - most artists miss that). In addition to showing the personality common to Egerkrans' work, this piece also shows the mix of realistic animal colouration with striking, pseudorealistic background colours. In fully realistic art, this might not work, but here, it does. © Johan Egerkrans.
MW. To me, your palaeoartworks recall some of William Stout’s illustrations. Both have a distinctive, non-realist style, interesting colour schemes and emphasis on the animal subjects. Is Stout an influence on your work?

JE. Very much so. I've always loved his work and his approach to paleoart. His creatures have tons of character and the draughtsmanship is sublime. They’re admittedly a bit skeletal at times but they make that up with personality. That I’m partial to Stout is hardly a surprise, as we're both inspired by the same old masters. Even if it's not obvious in my paleoart, a lot of my work takes cues from turn of the century illustrators like Arthur Rackham, Dulac and John Bauer, just like Stout's art.

MW. The work you produce is included in educational books. How do you think style impacts the scientific or educational prospects for palaeoart?

JE. The illustrations are not intended to be photoreal and that´s sort of the point. It´s obvious that they're an interpretation which forces the viewers to do part of the reconstruction in their own heads. That hopefully gets their imagination going which is the ultimate goal - to connect and get people interested. To make science fun.

The chosen style also saves me from meticulously rendering those thousands of tiny scales and retain my sanity, so that´s a huge plus.

MW. Do you ever stray from your signature style? Will we ever see a ‘realistic’ Egerkransian dinosaur?

JE. As I´ve mentioned before I always adapt my technique to the project at hand and this is just one of several styles I utilise. It´d be interesting to do a paleoart project in a more realistic vein, though I think there´ll always be a certain amount of stylisation. I´m not a realist painter and never will be - others have got that down already.

Umoonasaurus and chums. The barnacled fallen trees turns this image from just another Mesozoic marine scene into something much more atmospheric. © Johan Egerkrans.



MW. I’ve seen that you get a lot of scientific feedback on Facebook posts, a source that many palaeoartists – professional and amateur – can be wary of because of misinformation and confrontational internet users. How useful do you find social media to shape your art, and have you encountered much hostility?

JE. I was flabbergasted at how overwhelmingly positive the response was when I posted my first drawings on the Facebooks. Especially from the academic community. There´s been very little hostile or dismissive remarks - in general people seem to take the works seriously, as ‘proper’ paleoart.

The feedback is often extremely helpful - there´s lots of very well informed academics hanging about (you yourself and Darren Naish to mention just a few) and you quickly learn to sift the good advice from the bad or opinionated. I approach the forums as a sort of quick and dirty peer review; I´m not an expert and get things wrong all the time and if there´s something wonky someone is bound to point it out. As the ambition is to be as accurate as possible, within the limitations of the style, I try to surround myself with people who actually truly knows about this stuff. As luck would have it a lot of people I admire have proven to be more than willing to help out with comments, constructive criticism, links to papers and by just being supportive in general.

MW. When are you going to get Hollywood on the phone to make your work into a movie? They already look like they’re stills from some epic animated film about Mesozoic life. And they owe us, frankly, after The Good Dinosaur.

JE. I´m still waiting for them to get the straws out of their noses and give me a call. Bastards.

Guanlong and some sort of impudent Mesozoic mammal. Note how the Guanlong is strikingly and variably coloured, and yet still looks grounded. Bringing bright colours into the Mesozoic doesn't necessarily mean painting entire animals in lurid shades. © Johan Egerkrans.
MW. Finally, where’s the best place to find your art and support your work? And how long do we have to wait until your next book?

JE. You can follow my public facebook account “Johan Egerkrans - Illustrator” where I post about new projects and upcoming events like signings. Then of course there is the Paleoartists Facebook group where I´m pretty active.

I´ve also got a blog at http://johan-egerkrans.blogspot.se/ and an Artstation page https://www.artstation.com/artist/egerkrans.

My books can be bought from www.bokus.com or any other Swedish book retailer. You should be able to order them from there if you live in Europe but it's trickier in the States due to the fickle nature of the U.S. customs. Hopefully Alla tiders Dinosaurier will get an English edition at some point, but nothing's set at the moment.

The next book Flygödlor och havsmonster, about your favourites the pterosaurs (and their marine contemporaries), will be out in Sweden this fall. At some point I´d very much like to do a book about Permian and Mesozoic stem mammals (gorgonopsids are hands down my favourite prehistoric animals), but sadly it is a rather tough sell…  

MW. Johan Egerkrans, thanks very much!


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Friday, 16 June 2017

Revenge of the scaly Tyrannosaurus

Reworked version of my 2012 Tyrannosaurus painting, now in it's third guise. There's something about this painting which recalls reconstructions from 1906 rather than those of 2016.
The skeletal anatomy of Tyrannosaurus rex is probably better known and studied than the skeletons of many living animals, but its soft-tissues - and thus much about its life appearance - are poorly represented by fossil remains. Thus, virtually all of our ideas about muscle bulk, soft-tissue body shape and integument have to be reconstructed by phylogenetic proxy and functional prediction. As with all dinosaurs, we've historically felt pretty confident that Tyrannosaurus was entirely scaly, but relatively recent discoveries of filamented tyrannosauroids in China (Xu et al. 2004, 2012), as well as a growing mountain of fuzzy coelurosaur fossils, point to a different conclusion: that Tyrannosaurus was adorned in simple filaments - hair-like equivalents of feathers. Skin impressions for more derived tyrant species - the tyrannosaurids - have proven rare in fossil record (Hone 2016) and, though rumours have circulated about some, they have largely escaped formal description and publication. In the absence of better evidence, the most parsimonious modern takes on everyone's favourite tyrant have involved a fuzzy covering.

In the recent months two papers have challenged this idea. The first, by Thomas Carr and colleagues (2017), purports to find osteological correlates of scales on the facial anatomy of the tyrannosaurid Daspleteosaurus, which they argue (along with other lines of evidence), to suggest crocodylian-like facial tissues and sensitivity. The second, by Phil Bell et al. (2017), describes scaly skin impressions from multiple postcranial regions of a Tyrannosaurus skeleton, and argues that the distribution of these impressions implies a uniform (or near uniform) covering of scales across the body, without much in the way of fuzz.

Because this is Tyrannosaurus, media sites and bloggers have spilled great amounts of ink over these stories. The scientific press has often been far from objective or unbiased. Popular articles have suggested Jurassic World fans might have 'won' the debate over scientists, that science fans are 'due' a return to scaly tyrants after 'losing' Pluto, and that the findings mean 'all is well in the dinosaur world'. The implication is a ridiculous one, like evidence of scalier tyrants is a moral victory rather than a test of a scientific hypothesis. But while the popular press has been celebrating the new papers, members of the palaeoblogosphere have been less enamoured with the findings. Trey the Explainer suggests that Bell et al.'s work doesn't really change what we already knew about tyrant integument, and thus does not invalidate many existing reconstructions. Andrea Cau posits that interpretations of scaly tyrants reflect our prejudices more than science, and that taphonomic factors may explain the absence of filaments. Brian Switek has concerns that the skin patches are too small and spread too widely to give a complete picture of the integument, and echoes concerns about taphonomic interference. The collective response seems to be a defensive one, protecting concepts of filamented tyrannosaurids from a resurgence of a more traditional, scaly model. Would any other dinosaur get this treatment? Perhaps not: as Brian explains in his recent post, this reaction is the T. rex celebrity effect at full bore.

Supermegafluffy Tyrannosaurus, from 2015. They were simpler times.
I've painted many fluffy Tyrannosaurus in the last few years (above) and quite like the idea of everyone's favourite 6 tonne dinosaur bonecrusher being a giant plush toy. However, we also have to concede that our ideas of Tyrannosaurus skin have been largely informed by prediction, not direct data, and that popular, long-held notions are as ripe for scientific revision as any other (lest we forget other famous examples of this - Brontosaurus and Ornithoscelida). Moreover, although some critics are suggesting the papers don't tell us anything new - rumours of scale impressions have been circulating for years - these recent studies give us the first rigorously documented, peer-reviewed glimpse into Tyrannosaurus skin anatomy. This is new, allowing us to form our own opinions on Tyrannosaurus appearance based on actual data, not hearsay. So, rather than putting our gloves up to defend our prior model, I wonder if we should be exploring how this new data might transform our perception of Tyrannosaurus life appearance. That these new studies present conflicting data to our expectations is not grounds to be upset, annoyed or defensive. To the contrary, they allow us to use real data - not predictions - to refine our ideas of tyrannosaurid appearance and evolution. For those of us interested in dinosaurs as real entities, and not movie monsters, that's a good thing.

What, exactly, has been argued about scaly tyrants?

A lot of the popular write ups of these recent papers include errors and misrepresentation, so let's recap what is actually being argued about Tyrannosaurus skin. A common social media reaction to Bell et al.'s work is that they've presented 'a patch' of skin, and are extrapolating from that. We need to debunk that right away: they've not described a single patch, but multiple small patches from the neck (alas, exactly where on the neck isn't reported), the top of the pelvis, and the base of the tail (below). All the samples stem from the 'Wyrex' specimen (HMNS 2006.1743.01). The most extensively represented area is the tail base, which has the largest single piece of fossil skin - 30 cm². The other skin samples are not as large, some being just a few centimetres across. Each patch shows the same skin type: uniform, tiny 'basement scales', each less than 1 mm across (Take note, artists: you would not see Tyrannosaurus scales until you were being eaten by their owner). Similar scale patches, also described by Bell et al. (2017), have been found on the torso and tail regions of other tyrannosaurid species, implying similarly scaled regions in these taxa.

Tyrannosaurus skin patches from the neck, pelvic area and tail of the 'Wyrex' specimen as illustrated by Bell et al. (2017). The scale bars for the scale imagery are 5 mm (b - e) and 10 mm (f-h). These things are tiny, and we can assume the skin of the animal would look smooth or leathery in life.
Some folks are suggesting that the size of these skin patches allows us to dismiss their scaly signal, or that even that they're anomalous, reflecting unusual taphonomic conditions that cloud their significance. I'm unsure about these ideas. Most skin impressions are small patches (even scaly skin gets a rough ride during fossilisation) and the fact they're small doesn't diminish the fact that each records a cluster of scales. We have to assume these are not unusual or 'special' areas on the body but generally indicative of surrounding skin fabrics. The fact that each patch is consistent with regard to scale size and texture hints at them being part of a continuous, unbroken integument, and not isolated scaly pockets in a sea of fluff.

But what about arguments that the scale patches are tissues stripped of filaments before preservation, like so many 'monster' carcasses? Filament/scale combos do have precedent in dinosaurs, being present on the tail of Juravenator and those scales of Kulindadromeus with fibre-like tassels (Chiappe and Göhlich 2010; Godefroit et al. 2014). We know from modern animals that fibrous epidermal structures are especially vulnerable to decay and physical weathering, but is there evidence that this has taken place on the Wyrex Tyannosaurus skin patches? At present, it's hard to say because we have no idea what tyrannosaur skin looks like as it decays. It might be significant, however, that the scale patches look very similar across the Wyrex specimen, and that they resemble other tyrannosaurid skin impressions closely. We might expect some variation if taphonomy was really distorting these specimens in a major way, and we're not seeing that. Moreover, the Wyrex skin impressions, though small, are pretty high-resolution. The scales, and their intervening areas, have sub-millimetre proportions and sharply defined edges. There's no tatty scale margins, no obvious spaces for filament attachment, or linear structures crossing the scales to imply a rogue filament impression. We'll remain uncertain if these are anomalous, taphonomically-altered samples until we find other examples of tyrannosaurid skin, but there's no reason to be unduly suspicious of the the samples we have.

Of course, the adage that 'absence of evidence is not evidence of absence' is always important when dealing with the fossil record, and it applies here as a sensible caveat. However, we shouldn't wield this phrase as a definitive counter-argument to reasonable interpretations of available evidence. Palaeontologists have to work with data, not suspicions or gut feelings, and the data we have does not include, or hint at, the presence of filaments. I'm not arguing that taphonomy isn't worthy of consideration here (indeed, the omission of details about 'Wyrex' taphonomic history is an issue with the Bell et al. 2017 paper) but we must beware the logical fallacies of appealing to probability (i.e. taphonomy could explain the lack of filaments, so it does explain the lack of filaments) or special pleading (excluding Tyrannosaurus from the same logic we would apply to other fossil animals when presented with this data).

Tyrannosaurus skull AMNH 5027 - note the 'hummocky' textures on the side of the snout, above and below the orbit, and atop the rostrum, likely indications of scaly skin. Image in public domain, sourced from Wikipedia.
Carr et al. (2017) present a different form of evidence for scales: osteological correlates. I consider some aspects of their study problematic in that it only looks to crocodylians and birds for comparative tissues, despite the clear value other tetrapods have in deducing facial tissue types (Knoll 2008; Morhardt 2009; Hieronymus et al. 2010); it lacks illustrations of the bone textures correlated to scaly integuments; and the conclusion of tyrants bearing crocodile-like face scales is flawed: crocodylians do not have face scales, but a tight, highly cracked sheet of facial skin - Milinkovitch et al. (2013). Nonetheless, I think Carr et al. (2017) are right in concluding the bony textures of tyrannosaur skulls seem indicative of scaly skin. These findings echo previous interpretations of bosses and rugosities in tyrant skulls (e.g. Brusatte et al. 2012; Sullivan and Xu 2016) and aren't controversial. Scales closely associated with bone either leave a 'hummocky' surface texture, which is seen on tyrant snouts (specifically their maxillae and nasals) or small bosses and hornlets, which are found in all tyrannosaurid skulls above their orbits (lacrimal and postorbital bones) and on their 'cheeks' (jugal bones). Hornlets and bosses represent the locations of specific scales in living reptiles (Hieronymus et al. 2009) and can thus give especially good indications of life appearance (check out chameleon skulls for especially good correlation between skull and scale features). The presence of hummocky bone textures and hornlets is a strong correlate for scales, as they rule out coverings of naked or feathered skin. Such skin types do not alter the underlying bone surface (Hieronymus et al. 2009).

These osteological correlates combine with the skin impressions to collectively show Tyrannosaurus as scaly across much of its face, somewhere on its neck, over the pelvic region and along the tail base (below). So far as we can tell, this picture seems consistent with osteological correlates and skin sampling from wider Tyrannosauridae. That's pretty extensive coverage, ruling out the presence of fibres in places that we know other dinosaurs - including other tyrannosauroids - were fuzzy, and implies that tyrannosaurids were mostly scaly. I'm particularly startled at the scales over the hip region as they curb even the long 'fibre capes' we see in some modern tyrant reconstructions, like the famous Saurian Tyrannosaurus. The fact that the scales occur in places known to be ancestrally filamented for tyrants is also intriguing: Bell et al. (2017) speculate that they may be modified feathers - that is, the same as bird scales - rather than a reversion to lizard or croc scales. Hold that thought, we'll come back to it soon.

Everyone's doing maps of Tyrannosaurus with integument details nowadays, and I want in. Note that this is Tyrannosaurus specific, and does not feature scale data from other tryannosaurids.

What's in the gaps?

The million dollar question is what was present between these scaly regions: more scales, or fibres? This is a major point for many respondents to the Carr et al. and Bell et al. papers, as it decides whether we keep our interpretation of Tyrannosaurus as an - at least partly - fuzzy animal. With our scale distribution map as a starting point, several options are available. The first is that fuzz was present in regions not yet represented by skin remains or osteological correlates. This would mostly imply the top of the torso (Bell et al. 2017), but may also be parts of the back of the head, some aspects of the neck (depending on where the neck skin impression came from) and maybe the end of the tail. Over on Twitter, Patrick Murphy has presented a reconstruction which shows what this might look like. I must admit to finding it quite amusing, sort of like T. rex has put on a shawl to visit the opera.

But how dense could these fuzzy patches have been? Bell et al. (2017) suggest that dense fibrous coverings are doubtful, noting that large living mammals avoid patches of thick insulating fibres to aid heat loss. This has not gone down well with some critics, who cite studies of feathers preventing over-heating instead of facilitating it. An oft-cited study in this regard is Dawson and Maloney (2004), who found emu feathers block virtually all solar radiation from the skin, preventing them from overheating in solar exposure that causes similarly-sized hairy mammals to seek shelter.

Feathers: great at blocking solar radiation, also great at trapping body heat. Note how cooking hot these ostriches are on their necks, heads and legs, while the feathers are mostly ambient temperature. This isn't because the body isn't warm, but because the feathers block the heat signature entirely, trapping all that heat around the body. As surface area:volume ratios drop as animals get larger, it stands to reason that the benefits of blocking solar radiation give way to a need shed heat. Image from Wikipedia user Arno / Coen, CC BY-SA 3.0.
Feathers, however, are not magic structures that defy fundamental physical laws of insulation, nor do they liberate animals from the challenges of heat loss at reducing surface area:volume ratios. Beyond a certain size, shedding excess body heat is difficult for any terrestrial animal, and it gets tougher as they get larger. King and Farner (1961, p. 249) described feathers as having "an extremely high insulating value to the feathered surfaces" and a rich literature of studies on modern birds shows that feathers are as effective at trapping body heat as they are blocking solar rays (e.g. King and Farner 1961; Kahl 1963; Philips and Sandborn 1994; Dove et al. 2007). We can almost see them as a little too effective, leading many birds to develop heat-dumping adaptations to circumvent their own insulation, such as highly vascularised, non-feathery body parts as well as a repertoire of postures and behaviours (maximising exposure of unfeathered body parts; flapping wings; urinating on their legs) that aid cooling (e.g. Kahl 1963; Arad et al. 1989; Philips and Sandborn 1994). So yes, feathers are terrific at protecting birds from environmental heat, but that limits their ability to release metabolic heat from their own bodies.

If living birds find feathers a little warm, despite their relatively high surface area to volume ratios, we have to assume a theropod weighing anywhere between 6-14 tonnes is going to find big areas of dense filaments a challenge to thermoregulation too. It is not unreasonable to assume blankets of fibres could be a problem for big tyrants. The counterargument here is that Yutyrannus huali, a largish tyrannosauroid, does have dense fibres everywhere. But Yutyrannnus seems more lithe than Tyrannosaurus - perhaps just 10-25% of its mass, depending on the estimates (Bell et al. 2017) - and lived in a more vegetated, and thus shadier, habitat (Bell et al. 2017). A neat comparison Bell et al. (2017) make along this line uses living rhinos, where hairier species live in shadier settings than the virtually naked ones. In light of this, the reduction of filamented regions, and perhaps lessening their density, is a reasonable inference for animals of the size and habitat of Tyrannosaurus, and would reflect thermoregulatory responses to scaling and shade availability seen in living animals.

Large tyrannosauroids, like Yutyrannus huali, show that dinosaurs weighing perhaps 1.5 tonnes could be covered in feathers. But does this reflect the fact that this animal lived in shadier, vegetated habitats than the tyrannosaurids? This idea isn't silly: adaptation to specific circumstances has a major role to play in shaping animal skin anatomy, and could well explain why some tyrants are fuzzy, and others seem less so. (If you want to see the rest of this picture, check out this Patreon post)
Could Tyrannosaurus have had extremely fine, widely-distributed filaments - perhaps similar to something like elephant hair? This isn't entirely falsified by the new data, although the skin impressions we have show no evidence of such a covering despite preserving tiny integument details. Granted, animal filaments can be extremely fine, and they might be beyond the preservation potential and mechanics of even these high-res impressions. However, if we're arguing for filaments of this size and patchiness then - certainly for artistic purposes - we should concede that the animal would be essentially scaly, in the same way that most rhinos, elephants and hippos are essentially naked (below). From a thermoregulatory perspective, short, sparse filaments could make sense as these have the surprising ability to draw heat from the body in modern elephants, helping them stay cool (Myhrvold et al. 2012). Given the potential for overheating under dense filament coats in giant animals (Bell et al. 2017), I see this as more plausible than a 'cloak' of fibres between our scaly waypoints.

Scaly, minimally-filamented Tyrannosaurus. There's some tufts on the neck, but that's it. Is this model more consistent with the thermoregulatory requirements of a 6-14 tonne animal?
A last interpretation of this new data is that Tyrannosaurus was actually just scaly, with no fibres whatsoever. This is the most contested suggestion made by Bell et al. (2017), but it's not unreasonable with our current knowledge. Existing skin data, representing seven parts of the body if you pool all the distinct skull correlates and postcranial points (add several more if you want to extrapolate scale patches from other tyrants), shows enough scales and consistency in the scalation pattern that uniform scale coverage is not a ridiculous or indefensible concept. I appreciate that some folks will point to regional fuzziness of animals like Kulindadromeus in response, and its sharply defined areas of different integument types, and that's valid point. But we can also point to plenty of dinosaurs with extensive or entirely scaly hides and - if there's any value to linking body size and thermoregulatory regimes - they're a better match to Tyrannosaurus body mass than any known fuzzy species. For the time being, wholly scale models fit our existing data just as reasonably as partly fuzzy ones so, archaic and counter-intuitive as it seems - a scaly Tyrannosaurus is not an unreasonable interpretation for the life appearance of this animal, given our current data.

Beyond Tyrannosaurus: 'unlocking' dinosaur skin constraints

My take-home from these new papers is that our models of Tyrannosaurus skin have not crystallised, but we're a little more constrained in how we can imagine this animal, and have to concede a scalier appearance than many of us thought likely. But the implications of the Bell et al. study go beyond Tyrannosaurus in implying new ways to think about dinosaur skin evolution. With incontrovertibly fuzzy animals lining much of the the tyrannosauroid tree and its root, our scalier Tyrannosaurus gives us one of the best examples of a dinosaur replacing fuzz with scales. This is a far-reaching conclusion for those of us interested in dinosaur life appearance, complicating the already confusing evolutionary pattern of scale and fuzz distribution within the group. Ideas that some dinosaurs could be 'secondarily scaled' are supported by this discovery, and we have to wonder if classically fuzzy lineages - including many other theropod lines - are as tightly locked into fuzz, fibres and feathers as we once thought. Could large dromaeosaurs be a little lighter on fuzz than we imagine? Did Therizinosaurus look less like a giant pigeon and more like a walking Christmas dinner? We don't know, but now have reason to wonder.

Fluffy Tyrannosaurus juveniles, one of the possibilities created by the idea that tyrannosaurs might have avian-like 'dynamic' skin. The recovery of scales in non-scaly clades is not as simple as it might first appear!
Furthermore, the notion that Tyrannosaurus scales could be modified feathers (Bell et al. 2017) opens possibilities about mixes of filaments and scales. It's important to realise that not all scales are alike: 'reptile'' scales' are developmentally and genetically distinct from those we see in birds, which are actually secondarily modified feathers (Chang et al. 2000; Dhouailly 2009). Reptilian skin cannot be forced to grow feathers or filaments (Chang et al. 2000) and is developmentally static: once scales are formed, they're with them for life. Bird skin, however, is far more dynamic, and allows for all manner of ontogenetic and even seasonal variation in scale:feather ratios, changes to feather types, and modification of scale size (Lennerstedt 1975; Stettenheim 2000). If, as suspected, our tyrannosaurid skin samples represent fibrous integument masquerading as a scaly one, is this a sign of a bird-like 'unlocked' skin configuration where epidermal dynamism was possible? If so, Tyannosaurus could have changed appearance considerably with age (fluffy when small, scaly when big - above) or season (reflecting changes in climate or behaviour)? It must be stressed that we don't have any direct insight into these sorts of changes at the moment, and the hypothesis of tyrannosaurid scales being modified feathers needs testing. But the irony - we might have data indicating Tyrannosaurus could change its appearance readily, vindicating debaters on both sides of the scaly and fuzzy debate - is not lost on me. Maybe, just this once, everyone wins?

Summing up time

Let's tie this all together. A lot of ambiguity remains about the skin of Tyrannosaurus and its relatives, and it's not wise to hold any opinion about their life appearance too strongly at present. However, unduly downplaying the creep of scaly evidence into the tyrannosaurid fossil record isn't useful or logical. The skull skin correlates and fossil skin patches show that scales were present in numerous, widely-distributed parts of the body, and - until we see evidence to the contrary - this is good reason to assume scalier Tyrannosaurus than we might be used to. And yes, this does mean that some of our favourite, fluffier interpretations are now directly contradicted by fossil data, and consigned to our ever growing book of historic, discredited reconstructions. But this is always a possibility in palaeontology: our views of these animals are only ever hypotheses based on a sparse, biased fossil record, and every new discovery risks overturning someone's favourite concept. The fact we're able to move on from these reconstructions is positive, as it means we're a little less uncertain about the past, and a little closer to the truth.

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References

    • Bell, P. R., Campione, N. E., Persons, W. S., Currie, P. J., Larson, P. L., Tanke, D. H., & Bakker, R. T. (2017). Tyrannosauroid integument reveals conflicting patterns of gigantism and feather evolution. Biology Letters, 13(6), 20170092.
    • Brusatte, S. L., Carr, T. D., & Norell, M. A. (2012). The osteology of Alioramus, a gracile and long-snouted tyrannosaurid (Dinosauria: Theropoda) from the Late Cretaceous of Mongolia.
    • 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.
    • Chang, C., Wu, P., Baker, R. E., Maini, P. K., Alibardi, L., & Chuong, C. M. (2009). Reptile scale paradigm: Evo-Devo, pattern formation and regeneration. The International journal of developmental biology, 53(5-6), 813.
    • Chiappe, L. M., & Göhlich, U. B. (2010). Anatomy of Juravenator starki (Theropoda: Coelurosauria) from the Late Jurassic of Germany. Neues Jahrbuch für Geologie und Paläontologie-Abhandlungen, 258(3), 257-296.
    • Dawson, T. J., & Maloney, S. K. (2004). Fur versus feathers: the different roles of red kangaroo fur and emu feathers in thermoregulation in the Australian arid zone. Australian Mammalogy, 26(2), 145-151.
    • Dhouailly, D. (2009). A new scenario for the evolutionary origin of hair, feather, and avian scales. Journal of anatomy, 214(4), 587-606.
    • Dove, C. J., Rijke, A. M., Wang, X., & Andrews, L. S. (2007). Infrared analysis of contour feathers: the conservation of body heat radiation in birds. Journal of Thermal Biology, 32(1), 42-46.
    • Godefroit, P., Sinitsa, S. M., Dhouailly, D., Bolotsky, Y. L., Sizov, A. V., McNamara, M. E., ... & Spagna, P. (2014). A Jurassic ornithischian dinosaur from Siberia with both feathers and scales. Science, 345(6195), 451-455.
    • 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. (2016). The Tyrannosaur Chronicles: The Biology of the Tyrant Dinosaurs. Bloomsbury Publishing.
    • Kahl Jr, M. P. (1963). Thermoregulation in the wood stork, with special reference to the role of the legs. Physiological Zoology, 36(2), 141-151.
    • King, J. R., & Farner, D. S. (1961). Energy metabolism, thermoregulation and body temperature. Biology and comparative physiology of birds, 2, 215-288.
    • Knoll, F. (2008). Buccal soft anatomy in Lesothosaurus (Dinosauria: Ornithischia). Neues Jahrbuch für Geologie und Paläontologie-Abhandlungen, 248(3), 355-364.
    • Lennerstedt, I. (1975). Seasonal variation in foot papillae of wood pigeon, pheasant and house sparrow. Comparative Biochemistry and Physiology Part A: Physiology, 51(3), 511-520.
    • 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? (Doctoral dissertation, Western Illinois University).
    • Myhrvold, C. L., Stone, H. A., & Bou-Zeid, E. (2012). What is the use of elephant hair?. PloS one, 7(10), e47018.
    • Phillips, P. K., & Sanborn, A. F. (1994). An infrared, thermographic study of surface temperature in three ratites: ostrich, emu and double-wattled cassowary. Journal of Thermal Biology, 19(6), 423-430.
    • Stettenheim, P. R. (2000). The Integumentary Morphology of Modern Birds—An Overview 1. American Zoologist, 40(4), 461-477.
    • Sullivan, C., & Xu, X. (2017). Morphological diversity and evolution of the jugal in dinosaurs. The Anatomical Record, 300(1), 30-48.
    • Xu, X., Norell, M. A., Kuang, X., Wang, X., Zhao, Q., & Jia, C. (2004). Basal tyrannosauroids from China and evidence for protofeathers in tyrannosauroids. Nature, 431(7009), 680-684.
    • Xu, X., Wang, K., Zhang, K., Ma, Q., Xing, L., Sullivan, C., ... & Wang, S. (2012). A gigantic feathered dinosaur from the Lower Cretaceous of China. Nature, 484(7392), 92-95.

    Wednesday, 31 May 2017

    Armoured theropod faces, rhino horns and pterosaur skin crests: how artists can predict elaborate skin structures in fossil animals

    Abelisaurid Kryptops palaios recieves some TLC in Early Cretaceous Niger, while duck-faced Anatosuchus minor sneaks out of the water. But what's with the swollen, bulging look to the abelisaur's face? (Concept by Chidumebi Browne. Award yourself an extra biscuit if you spot the homage to one of my palaeoart heroes in this scene.)
    A hot topic in modern palaeoart circles is the relationship between bone surface texture and soft-tissues. Specifically, artists are interested in what bone textures mean for skin composition and thickness, and whether it tells us anything about epidermal structures such as scales, feathers or hair. The idea that bone texture has a relationship to skin anatomy is not new, and palaeontologists have been linking details of fossil bones to beaks, horns, feathers and so on for many decades. Recent research on this matter is much more detailed and informed than previous efforts however, and uses careful comparisons of bone structure (both external and internal) in fossil and living species to make detailed predictions about the life appearance of long-extinct animals. Tobin Hieronymus and other individuals from the Witmer Lab (University of Ohio) have made some especially valuable contributions to this field, and their work adds to a growing literature that palaeoartists should consult to make credible restorations of past species. Palaeoart is long past the stage where we can doodle a rough outline around a skeleton and call it a day - more than ever, production of truly credible palaeoartwork is only possible after careful and thorough research.

    One of the most interesting aspects of this recent work concerns a skin type that we rarely discuss for ancient animals: dense, stiff dermal tissues that forms thick armour in animals like hippos, mouse deer and pigs; and epidermal projections, such as horns and crests, in rhinos and birds. We might assume that these soft-tissue structures would leave little trace on bone and that we're ignorant of their presence in fossil animals until specimens preserving soft-tissues show us otherwise. However, this is not so. Work by Hieronymus (2009) and Hieronymus et al. (2006, 2009) shows that we can identify the presence of skin armour and epidermal projections without soft-tissue preservation. This has significant implications for how we might restore fossil animals, and artists should be on the lookout for features evidencing these structures when researching their reconstructions.

    Reinforcing skin to make armour and skin projections

    Before we get to the fossil examples, it will help to know how skin is armoured and epidermal projections are reinforced without the aid of bony material. For armoured skin, white rhinoceros hide provides a well-studied example. Here, the dermis is reinforced with densely packed collagen fibres criss-crossing one another in three perpendicular planes (Shadwick et al. 1992). This structure differs markedly from typical reptilian and mammalian skin (Hieronymus et al. 2010) and has correspondingly different skin mechanics. Not only is it considerably stiffer and highly resistant to tearing, but under compression it is stronger than cartilage (Shadwick 1992). White rhinoceros skin is, on average, 25 mm thick (though their belly skin is about half that measurement) and it serves them well at resisting damage during intraspecific bouts or when on the wrong end of a predatory act. Similar skin has convergently evolved in pigs, hippos, mouse deer and seals, these being species that engage in biting and stabbing fights and having obvious need for protective tissues.

    Indian rhinoceros skin in all it's supercollagenous glory. Note the thick folding but otherwise sparse wrinkling, a consequence of poor elasticity in this skin type. From Wikimedia user Sanjay ach, CC BY-SA 3.0.
    Soft-tissue crests, horns and other projecting structures can also be made of expanded, dense dermis (seen in comb ducks), or reflect enhancement of another skin tissue: the epidermis (Hieronymus et al. 2006, 2009). These epidermal elements anchor to underlying dermis and are formed of dense keratin matrices, producing ultra-tough cornified tissue not dissimilar in composition to beaks, claws, horn sheaths or baleen (Hieronymus et al. 2006). Some skin projections can incorporate non-keratinised components as well - rhino horns, for instance, have mineral and melanin components as additional stiffening agents (Hieronymus et al. 2006) - and the degree of keratinisation can vary, depending on the functional demands of the projection. The crests of white pelicans are a well-known example of these structures, and are noteworthy for their ephemeral nature. Unlike most epidermal outgrowths, pelicans shed and regrow these structures annually. That's food for thought for not only palaeoartists, but also those of us wondering if soft-tissue crests have significance to taxonomy. Would a fossil pelican with a rostral crest be considered a different species to one without? Quite possibly.

    American white pelican with rostral crest, photographed by Travis Barfield. Photo from Wikimedia.
    When either of these skin types overgrow bone, they leave clear traces on the bone surface texture and histology. The best places to look for these markers are animal skulls, as they are generally not separated from skin by layers of muscle and fat like postcranial bones, and they tend to be body parts that animals adorn with horns, crests and other epidermal outgrowths. Particularly good sites to check for skin-derived markers are the bones forming the cheek, those around the orbit, and along the forehead and snout, as these regions generally have the closest relationship between bone and skin.

    Collagen-dense armoured dermis leaves relatively coarse (1-2 mm) rugose projections of bone beneath it, often of sufficient extent that they are discernible in photographs. You can readily see them on rhino skulls, for instance, as well as around the jaw tips of hippos and the rostral bosses of red river hogs. They have a corresponding histological signature, too: patches of obliquely-orientated metaplastically ossified dermal collagen fibres (Hieronymus 2009; Hieronymus et al. 2009). These patches of rugose bone cover large areas of the skull, and, in hippos, they even wrap into the mouth, betraying the presence of soft-tissue armour inside the jaws. This is something for palaeoartists to note as it shows dense, armoured skin can grow around complex structures, like gums and teeth, and also allows for lip-like structures that sheath teeth (so no, these tissues are not excuses for toothy prehistoric artwork). I assume the stiffness of armoured skin explains why the 'canine pocket' in the hippo upper jaw does not collapse when gaping, despite their lack of skeletal reinforcement.

    Business end of a hippopotomus skull - note the rugose textures around the end of the snout, characteristic of collagen-dense armoured skin. Cropped detail from a CC BY-SA 3.0 photo by Wikimedia user ContinentalEurope. From Wikimedia.
    Similarly coarse rugose projections or spicules exist underneath epidermally-derived horns and crests, but with an important distinction to those underlying armoured skin. Rather than leaving uniform patches, these structures leave ring-like rugosities that outline the circumference of the projecting structure. This is true for massive projections, like rhino horns, and also more delicate ones, like pelican crests (Hieronymus 2009; Hieronymus et al. 2009). It's thought that stresses inflicted on projecting structures explain their ring-shaped 'footprint'. Virtually any load placed on a crest or horn is transmitted to base of the opposing side, meaning the edges of these structures experience the greatest loading in life. It makes sense, therefore, that the outline of the structures have the deepest developmental scarring (Hieronymus 2009). A boss or other elevated bony region is sometimes associated with epidermal structures too, but this is not universal. Ring rugosities do not tell us much about the exact morphology of projecting structures but they do reveal something about the extent of the base and - from the size of the rugosities and spicules - we can predict the size of the compositional fibres. If we assume that bigger structures need larger fibres for reinforcement, which seems borne out in modern animals - rugosity dimensions might give us some clue of overall structure size (Hieronymus 2009). 

    Where can we find these structures in the fossil record?

    Spoilers: in species like this guy. Mmm... abelisaur fresh... 
    Turning our attention to extinct creatures, these bony correlates are robust enough to withstand fossilisation and we can look for hints of thick, armoured skin or epidermal projections in any specimen with reasonable preservation. The skulls of fossil rhinocerotids are an obvious place to seek such structures and the results are quite fascinating. Evidence of dense, armoured skin appears in taxa from c. 40 million years ago, while their horns are a more recent development, from about 20 million years ago (Hieronymus 2009). The development of large tusks, rather than horns, seems to have spurred the development of skin armour in ancient, hornless rhinos, and we can note parallel correlations between large teeth and armoured skin in other lineages. When animals are routinely slashing, ripping and biting one another, armoured skin seems to be a common adaptive response (Hieronymus 2009).

    Majungasaurus crenatissimus skull, showing extent of bone texture related to armoured skin (blue) and tough cornified skin (purple). Skull drawn from Sampson and Witmer (2007); distribution of bone textures after Hieronymus (2009).
    It's not just mammals that get in on this act. The top and front of the skull of the abelisaurid theropod, Majungasaurus crenatissimus, matches osteological and histological criteria for dermal armour, and this is good reason to restore this species with thick, collagen-reinforced skin over its snout and braincase region (Hieronymus 2009). Adjacent skull areas - the sides of the jaws, the roof of the mouth, the orbital and cheek regions  - also show hints of a gnarly skin covering, these being marked with a bone texture characterised by deep pits and grooves. Among modern animals, this seems best correlated with thick, highly keratinised skin, such as cornified pads or beaks (Heironymus 2009; Hieronymus et al. 2009). When considered with the correlate for dermal armour, these textures suggest the face and oral cavity of Majungasaurus was covered in deep, reinforced skin tissue, and we have to wonder how much of the underlying skull structure was obvious in life. Abelisaurids are well known for their gnarly, pitted skull bones (e.g. Sereno et al. 2004), and it's likely that thick facial skin occurred in other members of the group (Hieronymus 2009). These are animals that science encourages artistic speculation with: what would the armoured face of an abelisaur look like? I've taken a punt at this concept with the Kryptops painting accompanying this post, but I'm sure there are other configurations that could be explored. It would be remiss not to mention that armoured skin on theropod faces aligns well with face-biting antagonistic behaviour predicted from their pathological bones (Tanke and Currie 1998; Hieronymus 2009), and that this again chimes with biting behaviour driving evolution of armoured skin.

    Evidence of epidermal structures are common in a paleaoart mainstay: pterosaurs. By now, most of us will be familiar with the idea that many pterosaurs had soft-tissue headcrests thanks to well-publicised exceptionally preserved fossils (e.g. Bennett 2002; Frey et al. 2003), but can we predict them in species represented by bones alone? Thanks to bone textures, we can. Soft-tissue crests grow over low bars of bone projecting from pterosaur snouts, often with expanded anterior regions (Bennett 2002). Fine, curving striations and spicules are discernible on the top of these projections, contrasting with the smooth bone forming the base of the bony crest and the rest of the pterosaur skull. These rugosities mostly project vertically, or somewhat anteriorly at the front of the base structure. It is difficult to know if these rugose regions have a ring-like distribution given the flattened nature of most pterosaur fossils, but their presence around the top of a projecting bone bar implies a ring-distribution. Collectively, these components meet predictions for epidermal projections and their distribution points to a tall, narrow structure - a crest - rather than a horn or boss. We would likely see this as the most parsimonious take on pterosaur crest bases even without exceptional fossil preservation so, wherever you see these features on pterosaur skulls, it is reasonable to assume a large, prominent crest. I stress that you do not these features in all crested pterosaurs: some bony crests are completely smooth, and have no evidence for extensive soft-tissue elaboration. This is mainly seen in the ornithocheiroids (the group that includes taxa like Anhanguera, Pteranodon and Nyctosaurus).

    Darwinopterus robustodens as a case study for pterosaur striated crests, and what they mean for soft-tissues. Yes, they were that daft - don't feel you need to be conservative when restoring them!
    We are fortunate to have pterosaur specimens with preserved soft-tissues to help us gauge the size and shape of their crests. They are generally rounded, with the deepest portion posteriorly, and their size seems correlated with bony crest development (coarser rugosities and taller crests seem to indicate larger crests). Their crests were generally large, even in animals with modestly developed bony supports (Czerkas and Ji 2002), and they can grow to many times the area of the skull in species with strongly developed crest rugosities (Campos and Kellner 1997; Frey et al. 2003). Don't hold back when drawing these things, chaps: they were nuts (see diagram, above).

    Applications to other species, and potential pitfalls

    There are surely other animals that we could discuss with these features, but I think our point is made by now: with careful observation and comparison to modern species, we can detect the presence of body profile-altering skin structures in fossil animals, and these features should be on the radar of anyone trying to restore fossil tetrapods credibly. It should be stressed how phylogenetically widespread the examples given in this post are: as if it needs saying - pterosaurs, rhinos, abelisaurids, deer and so on are not closely related, and yet they share basic aspects of bone texture and histology related to skin structure. The take-home here is that skin is a highly plastic, adaptable tissue that we need to be especially open-minded about reconstructing. It is naive to assume fossil animals will only have skin types common to their closest extant relatives.

    There are some caveats and pitfalls to be aware of about predicting tough dermis and epidermal projections. For example, there are a few cases where skin elaborations lack osteological correlates. Warthog warts, for instance, are prominent, permanent and conspicuous skin structures, but they leave no trace on the underlying bone. Likewise, the presence of armoured skin becomes difficult to predict beyond the skull because postcranial bones tend to be buried under other soft-tissues. We know from living animals that collagen-dense skin can be regionalised (mouse deer, for instance, tend to localise it on their dorsum and rumps - Dubost and Terrade 1970), so evidence of cranial armour is only a partial indicator for armouring across the body.

    Cuspicephalus scarfi regrets sporting a hunk of tall, cornified cranial epidermis on a windy day.
    Detection of bone rugosity type is also an issue, at least in cases where we are unable to see fossil material first-hand. Yes, the rugosities and structures discussed here can be seen in photos, but not always. Moreover, unless the photo is especially clear, it's easy to confuse them with other types of bone surface rugosity, of which there are several, all with different soft-tissue correlates (Hieronymus et al. 2009). So, before going nuts with armour, crests and horns on a fossil animal because they seem to have a rough surface somewhere on their skull, check out specimen descriptions, high-res photos, histological studies, quiz those consultants, and make sure the criteria for these elaborate skin structures are met.

    That final point seems particularly relevant given the modern palaeoart fashion of speculating about fossil animal appearance. Long-time readers will know that I'm an advocate of this practise, but science of the kind discussed here puts an onus on artists to be careful when adorning extinct animals with elaborate skin structures. Yes, there are loopholes which can justify these outlandish reconstructions if we want to find them, but consider that some speculative structures included in modern palaeoartworks would be expected to leave osseous markers if they were present. Maybe this is a case where absence of evidence is actually evidence of absence and, if we cannot find these correlates, we should assume those structures were not present in our subject species.

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    References

    • Bennett, S. C. (2002). Soft tissue preservation of the cranial crest of the pterosaur Germanodactylus from Solnhofen. Journal of Vertebrate Paleontology, 22, 43-48.
    • Campos, D.A. & Kellner, A.W.A. (1997). Short note on the first occurrence of Tapejaridae in the Crato Member (Aptian), Santana Formation, Araripe Basin, Northeast Brazil. Anais da Academia Brasileira Ciências, 69, 83–87.
    • Czerkas, S. A., & Ji, Q. I. A. N. G. (2002). A new rhamphorhynchoid with a headcrest and complex integumentary structures. Feathered Dinosaurs and the Origin of Flight, 1, 15-41.
    • Dubost, G., & Terrade, R. (1970). La transformation de la peau des Tragulidae en bouclier protecteur. Mammalia, 34, 505-513.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, 233-266.
    • Hieronymus, T. L. (2009). Osteological Correlates of Cephalic Skin Structures in Amniota: Documenting the Evolution of Display and Feeding Structures with Fossil Data (Doctoral dissertation, Ohio University).
    • Hieronymus, T. L., Witmer, L. M., & Ridgely, R. C. (2006). Structure of white rhinoceros (Ceratotherium simum) horn investigated by X‐ray computed tomography and histology with implications for growth and external form. Journal of Morphology, 267, 1172-1176.
    • 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, 1370-1396.
    • Sampson, S. D., & Witmer, L. M. (2007). Craniofacial anatomy of Majungasaurus crenatissimus (Theropoda: Abelisauridae) from the late Cretaceous of Madagascar. Journal of Vertebrate Paleontology, 27, 32-102.
    • Sereno, P. C., Wilson, J. A., & Conrad, J. L. (2004). New dinosaurs link southern landmasses in the Mid–Cretaceous. Proceedings of the Royal Society of London B: Biological Sciences, 271, 1325-1330. 
    • Shadwick, R. E., Russell, A. P., & Lauff, R. F. (1992). The structure and mechanical design of rhinoceros dermal armour. Philosophical Transactions of the Royal Society of London B: Biological Sciences, 337, 419-428.
    • Tanke, D. H., & Currie, P. J. (1998). Head-biting behavior in theropod dinosaurs: paleopathological evidence. Gaia, 15, 167-184.

    Thursday, 27 April 2017

    Walking with ichthyosaurs: the amphibious ichthyosaur hypothesis

    Benjamin Waterhouse Hawkin's (1858?) sketch of amphibious marine reptiles, including a large shambling ichthyosaur. Image borrowed from Frank T. Zumbach's Mysterious World.
    One of the most charming aspects of mid-19th century palaeoart are those amphibious marine reptiles: depictions of ichthyosaurs and plesiosaurs that hauled themselves onto rocks or beaches to rest, or lunge with open jaws at passers by (above). To modern eyes these images look naive and quaint, a clear reminder of how far our understanding of fossil animals has progressed in the last two centuries.

    Of course, art has a habit of imitating life and, a good 150 years after amphibious marine reptiles became unfashionable in palaeoartworks, Ryosuke Motani and colleagues (2014) published a new marine reptile suggested to be capable of locomotion on land as well as in water: the ichthyosauriform Cartorhynchus lenticarpus. This Chinese, Early Triassic species is anatomically remarkable in several respects. Although reminiscent of early ichthyosaurs in overall shape, it has a considerably reduced snout, seems to lack teeth, is just 20 cm from snout to vent despite indications of osteological maturity, and bears enormously long forelimbs. Though unique when first discovered, another, much larger Cartorhynchus-like species has since been found in the same deposits, Sclerocormus parviceps. Together, these animals form a clade at the base of Ichthyosauriformes known as Nasorostra, the 'nose beaks', referring to a defining feature where their nasal bones reach the jaw tip (Jiang et al. 2016).

    Holotype specimen of Cartorhynchus lenticarpus. Note the enormous forelimbs with their expansive unossified wrists, indicated by the distal phalanges being well posteriorly displaced from the upper arm bones. From Motani et al. (2014).
    The amphibious habits of Cartorhynchus are primarily based on its unusually large forelimbs and small body size, it being reasoned that Cartorhynchus could drag or propel itself over exposed sediments like a mudskipper, turtle or pinniped. I find this idea fascinating: an ichthyosauriform that was at home outside of water? Cartorhynchus certainly deviates from ichthyosaur anatomy and evolutionary trends enough to inspire inquiry about its weird bauplan - if it was not amphibious, it might be doing something else equally unexpected. The amphibious Cartorhynchus hypothesis has received surprisingly little detailed attention online, save for coverage of a 2014 press release and this excellent primer article at Tetrapod Zoology, so there's scope for a closer look at this idea. What is the evidence for amphibious habits in Cartorhynchus, and how does this concept fit models of early ichthyosaur evolution?

    The functional basis for an amphibious lifestyle in Cartorhynchus

    Motani et al. (2014) present a fairly detailed argument in favour of amphibious habits in Cartorhynchus. The chief lines of evidence are those expansive forelimbs, but it's not just their size that matters: their enormous, unossified carpal regions are also significant. Several early ichthyosauriforms have poorly ossified carpal bones but the unossfied region in Cartorhynchus flippers is proportionally bigger by some margin. This would allow these ordinarily-rigid marine reptile flippers an unusual degree of flexibility and optimise them for terrestrial locomotion. Flipper-based terrestrial motion is surprisingly tricky because its users tend to be suboptimally designed for movement out of water and they almost always have to overcome drag forces acting on the body as well as shove themselves around. Moreover, substrates associated with coasts and waterways tend to be unstable, yielding under pressure and being challenging for even proficient terrestrial animals. These factors mean flippers can easily dig into substrate or slip across it rather than propel their owners about, and it's easy to see why beaching is fatal for so many specialised aquatic species.

    Studies (using robot turtles!) suggest that rigid flippers are generally poor at terrestrial locomotion and may even be incapable of moving animals over some surfaces (Mazouchova et al. 2013). A bendy flipper, in contrast, works well, allowing the forelimb to flex before the substrate moves, spreading the weight of the animal over the distal limb and allowing the proximal flipper region to elevate and support the body (Mazouchova et al. 2013; Motani et al. 2014). The unusually expanded flexion zone in Cartorhynchus forelimbs would be well suited to this purpose, and certainly much better at this task than those of other ichthyosaurs. We might note, as an aside, that the lack of flexion zones in other marine reptile flippers, such as those of plesiosaurs, might be good reason to doubt their ability to crawl over land.

    video
    Did I mention the robot turtles? There are robot turtles. Supplementary video data from Mazouchova et al. (2013).

    The downside of having lots of cartilage in a long flipper is that they are weaker against bending than a more ossified one, so their utility as a walking limb lessen as the forces involved in moving the body increase. It's here where the small size of Cartorhynchus comes into play. Small size equates to low body masses and smaller forces associated with lifting the body, less structural demand on the flipper, and reduced drag effects from the sliding belly. As is so often the case in evolution, small body size might be an enabler for evolutionary experimentation in Cartorhynchus, allowing it to perform feats that its bigger relatives just couldn't even if they were also equipped with giant, bendy fins.

    The tail of Cartorhynchus is incompletely known but it's anatomical and phylogenetic proximity to the completely-known Sclerocormus suggests that its tail was long, flexible, and lacked any sort of fin or fluke (Jiang et al. 2016). A relatively simple tail lessens the risk of it dredging sediment or catching on debris during terrestrial locomotion and its flexibility might have permitted its use as a prop or even propulsive organ: fish such as the Pacific leaping blenny show how a long, bendy tail can be used to powerful effects in semi-terrestrial locomotion (Heish 2010, also below). Combinations of fin and axial motion in land-crawling fish can be surprisingly effective over a range of substrates (Standen et al. 2016) and we might assume similar options were available to Cartorhynchus.

     
    Leaping blennies, robot turtles... is this the best blog post ever? From Wikipedia, source: Hsieh (2010).

    The torso of Cartorhynchus is also of interest for this hypothesis. In contrast to some other Triassic ichthyosaurs, Cartorhynchus has a broad, stout torso rather than a long, laterally-compressed one (Carrol and Dong 1991). Though a wider torso would impart more drag during terrestrial crawling, it would aid stability when crawling over land. Moreover, torso drag can be lessened by shortening the body overall, giving new significance to the low Cartorhynchus pre-sacral vertebral count of 31 vertebrae, instead of a more typical ichthyosaurian count of 40-80 (Motani et al. 2014). Short, narrow hindlimbs, rather than the broad pelvic flippers of some other early ichthyosaurs, might have further aided drag reduction.

    Cartorhynchus in context

    It seems there's a prima facie argument for considering Cartorhynchus as equipped with some amphibious features. However, we should not get carried away - a suite of evidence for an aquatic lifestyle suggests it wasn't it a specialist denizen of shallow, partly-exposed habitats, but more of an animal able to exploit two realms. It has pachyostotic bones, true flippers rather than webbed walking limbs, and is adapted for suction-feeding: a mechanism where the combination of a small mouth and a large oral cavity creates a pressure differential during feeding, literally sucking small prey into the mouth if it's opened quickly (Motani et al. 2014). This foraging strategy cannot work outside of water so is strong support for Cartorhynchus foraging in fully aquatic settings.

    Cartorhynchus also stems from the Nanlinghu Formation, a mudrock and limestone marine deposit rich in fossils of aquatic reptiles and marine invertebrates: ammonoids, bivalves and conodonts. We might take these data as signs that Cartorhynchus was quite happy in water and maybe spent most of its time there, visiting coastlines and beaches on occassion, rather than living there permanently. We should also regard it as a marine animal, not an inhabitant of rivers or swamps (though it would be extremely cool if one turned up in such deposits!).

    Holotype of Hupehsuchus nanchangensis, a marine reptile seemingly more closely related to the ancestor of ichthyosaurs than Cartorhynchus. These guys surely deserve their own blog post and painting at some point. From Carroll and Dong (1991).
    The relationships of Cartorhynchus to other marine reptiles is also interesting in light of the amphibious hypothesis. You could be forgiven for interpreting Cartorhynchus as some sort of bridge between ichthyosaurs and terrestrial reptiles, but, no, the nasorostran clade seems to nest above the root of the ichthyosaur line between 'true' ichthyosaurs and the fully marine, ichthyosaur-like hupehsuchians (Motani et al. 2014; Jiang et al. 2016). The ichthyosaur + hupehsuchian clade, Ichthyosauromorpha, may be further allied to another group of marine reptiles, the amphibious thalattosaurs (Motani et al. 2014 - Darren Naish has an excellent overview of this topic here). This surrounds Cartorhynchus with lineages that had taken to water in a significant way and we should conclude that any amphibious adaptations of Cartorhynchus do not represent an ichthyosaurian invasion of the sea, but ichthyosaurs returning to land.

    Some might consider this surprising evolutionary scenario evidence against the amphibious hypothesis - why would a lineage of marine reptiles start retracing their adaptive steps to become landworthy, when the rest of the group is pressing ahead with more specialised aquatic lifestyles? In response, perhaps we should ask if a potentially amphibious marine reptile is really that surprising. A huge number of vertebrates have transferred between terrestrial and aquatic lifestyles in the last 400 million years, sometimes contrasting with wider adaptive trends taking place in closely related species. Well-understood evolutionary 'transitions' also show that large-scale adaptive phases are often complex with all manner of evolutionary experimentation and dead-end offshoots. We know that bridging aquatic and terrestrial realms can be advantageous to aquatic species - refuge from predators or rough seas, access to food off-limits to other marine species, access to safe habitats for rest or reproduction, etc. - and there's no reason to think ichthyosaurs were incapable of capitalising on these advantages, or immune to their selective draws. With all this in mind, the concept of a marine reptile exploiting semi-exposed habitats isn't really that radical. Maybe the key question here isn't 'why would a marine reptile go rouge and turn landward?' but is 'why aren't we seeing more of this sort of thing?'.

    What about Sclerocormus?

    A question currently unaddressed in technical literature is whether the other currently known nasorostran, Sclerocormus, might have also bear amphibious hallmarks. It has virtually all the same features that we likened to amphibious adaptations above, the only distinctions being marginally enhanced ossification of the forelimb (though it still retains a comparatively enormous unossified carpal region) and greater size overall (body length of 160 cm, representing an animal about 3.3 times larger than Cartorhynchus). In lieu of a detailed, quantified assessment it's difficult to say whether Sclerocormus was too heavy to pull itself along on land, but we can note that it is not especially big compared to the truly massive aquatic animals we have scampering over beaches today - leatherback turtles, giant pinnipeds, the odd manatee (Motani et al. 2014) and so on. Some of these animals weigh several tonnes and, if they can haul themselves out of water, maybe Sclerocormus could too.

    Holotype specimen of the larger nasorostran species, Sclerocormus parviceps. From Jiang et al. (2016).
    I find this question particularly interesting given how similar Sclerocormus and Cartorhynchus are in virtually all aspects (above). Is nasorostra a clade of potentially amphibious ichthyosaurs, or are we actually looking at growth stages of one oddball species? Their proportions are near identical, and they are only separated by fine details of anatomy (Jiang et al. 2016). Many proposed differences might be attributable to intraspecific variation, too. For instance, the significance of their slightly different vertebral counts is questioned through populations of living snakes, limbless lizards and fish with variable numbers of axial elements (Tibblin et al. 2016). Individually variable vertebral counts seem common in species with large numbers of axial elements, and this might have been true for ichthyosaurs. Ontogeny and scaling effects could explain other differences, including overall size, greater ossification of the postcranial skeleton, and subtle arrangements of skull bones. It can't be overlooked that these near identical species, unique in morphology in the grand scheme of ichthyosaur evolution, also happen to occur in the same member of the same formation, separated by only 14 m of strata (Jiang et al. 2016). For the time being, the identification of 'adult' skull fusion and textures in Cartorhynchus suggests they aren't the same species, but the marine reptile trait of retaining poorly fused skeletons into adulthood makes identifying adult forms especially tricky, especially with so few specimens to look at (Motani et al. 2014). It also seems worryingly difficult to tease fossil adults from juveniles without histological assessments, even with large sample sizes and good growth series (e.g. Prondvai et al. 2009). Perhaps we're waiting on histological examinations and more specimens to make a call on this.

    So, walking with ichthyosaurs?

    And finally, a painting: Cartorhynchus goes for a drag around a Triassic lagoon.
    Putting all the strands of the amphibious Cartorhynchus hypothesis together, I don't see reason for excessive suspicion about the idea of beach hauling nasorostrans. At the core of the pro-amphibious argument is that Cartorhynchus (and perhaps, by extension, Sclerocormus) has weird anatomy that requires an explanation - it's just too different from other ichthyosauromorphs to pretend it wasn't doing something unusual, maybe even unexpected. Amphibious behaviours are an explanation that seem to chime well with provisional form-function investigations and seem a sensible hypothesis at this time. That said, we should be appropriately cautious in our interpretations of these animals: our understanding of nasorostrans is in its infancy and alternative, currently-unexplored functional hypotheses could explain their anatomy as well, or better, than the amphibious concept in future. Fingers crossed that these animals receive more dedicated functional investgiations in years to come.

    Or maybe more robot turtles. Either is good with me.

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    References

    • Carroll, R. L., & Zhi-Ming, D. (1991). Hupehsuchus, an enigmatic aquatic reptile from the Triassic of China, and the problem of establishing relationships. Philosophical Transactions of the Royal Society of London B: Biological Sciences, 331(1260), 131-153.
    • Hsieh, S. T. T. (2010). A locomotor innovation enables water-land transition in a marine fish. PloS one, 5(6), e11197.
    • Jiang, D. Y., Motani, R., Huang, J. D., Tintori, A., Hu, Y. C., Rieppel, O., ... & Zhang, R. (2016). A large aberrant stem ichthyosauriform indicating early rise and demise of ichthyosauromorphs in the wake of the end-Permian extinction. Scientific reports, 6, 26372.
    • Mazouchova, N., Umbanhowar, P. B., & Goldman, D. I. (2013). Flipper-driven terrestrial locomotion of a sea turtle-inspired robot. Bioinspiration & biomimetics, 8(2), 026007.
    • Motani, R., Jiang, D. Y., Chen, G. B., Tintori, A., Rieppel, O., Ji, C., & Huang, J. D. (2015). A basal ichthyosauriform with a short snout from the Lower Triassic of China. Nature, 517(7535), 485-488.
    • Prondvai, E., Stein, K., Ősi, A., & Sander, M. P. (2012). Life history of Rhamphorhynchus inferred from bone histology and the diversity of pterosaurian growth strategies. PLoS One, 7(2), e31392.
    • Standen, E. M., Du, T. Y., Laroche, P., & Larsson, H. C. (2016). Locomotor flexibility of Polypterus senegalus across various aquatic and terrestrial substrates. Zoology, 119(5), 447-454.
    • Tibblin, P., Berggren, H., Nordahl, O., Larsson, P., & Forsman, A. (2016). Causes and consequences of intra-specific variation in vertebral number. Scientific reports, 6, 26372.