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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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    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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    • 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.

    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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    • 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.

    Friday, 14 April 2017

    New paper: pterosaur palaeoecology, as told by the fossil record

    A female Pteranodon tries to explain the new Silverstone et al. (2017) paper on Pteranodon taxonomy to the Cretaceous shark Squalicorax. Unfortunately for her, the sharks quite liked the 'Dawndraco' hypothesis.
    Last year I posted a couple of overviews of the better parts of the pterosaur palaeoecological record, discussing what we know was eaten by Rhamphorhynchus and azhdarchid pterosaurs, as well as what species ate them. These reviews were tied to a peer-reviewed paper on the same subject which, at the end of Febuary 2017, was published as part of an upcoming collection of pterosaur papers (Witton 2017). This collection, edited by David Hone, myself, and David Martill, is the proceedings of the Flugsaurier 2015 pterosaur meeting and will, when finished, contain over a dozen new insights into pterosaur research, with an emphasis on their palaeobiology. You can check out the existing content here - keep an eye on that site, as there are more papers to come.

    With my paper now out (though sadly not open access, but I will eventually be able to post an unformatted version online next year) I thought it would be a good time to take a holistic look at direct fossil evidence of pterosaur lifestyles. What are some of the most interesting examples of pterosaurs interacting with other species? Which purported interactions stand up to scrutiny, and which ones are a little tenuous? And what do they tell us about the all important Big Picture of pterosaur palaeobiology?

    Yes, some pterosaurs may well have been seabird mimics

    A number of pterosaur specimens have been reported as being associated with the remains of their last meals. Several of these have been lost, found to be erroneously interpreted, or are simply too poorly preserved to interpret their gut content. However, examples of the Jurassic non-pterodactyloids Rhamphorhynchus and Scaphognathus, the Triassic Eudimorphodon, and the famous Cretaceous taxon Pteranodon show reliable insights into their dietary preferences (below). These are virtually all remains of aquatic animals - mostly fish - preserved in intimate association with pterosaur skeletons, either between their jaws, aligned with their throats or within the torso skeleton. One example of a coprolite is known, though it's difficult to say exactly what it contains.

    Pterosaurs and their last meals (shaded grey). A, torso of Eudimorphodon; B-D, various Rhamphorhynchus with gut content and coprolite (C), E, Scaphognathus; F, Ludodactylus; and G, Pteranodon. From Witton (2017).
    Many of these specimens have been known for several decades, and their evidence of aquatic feeding probably played some part in the stereotyping of pterosaurs as seabird analogues (e.g. Wellnhofer 1991). Nowadays, we need to be a little more circumspect about what they tell us. Yes, they do show that some pterosaurs ate fish and other pelagic prey and, along with results from detailed studies into functional morphology, they help portray certain pterosaur species in the 'classic' seabird niche. RhamphorhynchusScaphognathusEudimorphodon and Pteranodon have at least some adaptations consistent with foraging for pelagic prey, such as long wings ideal for marine soaring, 'fish-grab' jaws and adaptations for launching from aquatic settings, as well as occurrences in coastal or marine settings. It would be a little odd if these aquatic-adapted species weren't catching aquatic animals from time to time.

    But we can't maintain the older view that these specimens, on their own, undermine the increasingly diverse and nuanced takes on pterosaur palaeoecology hinted at by form-function studies, biomechanics, and modern understandings of pterosaur habitats. We have thousands of pterosaur specimens in museums around the world, of which gut content is known from less than a dozen examples, and in four species. That's not even enough to demonstrate the full dietary range of the species in question, let alone tell us about the ecology of all pterosaurs. Indeed, the scarcity of pterosaur gut content agrees with some new predictions of pterosaur lifestyles in that non-aquatic food sources now suggested for pterosaurs - insects, wormy things, fruits, small tetrapods - have limited preservation potential, particularly outside of Lagerstätten. When factored against common agents of taphonomy and preservation, these hypotheses predict empty bellies in many pterosaur fossils, which is what we find virtually all of the time. It is, of course, difficult to be certain of anything concerning negative evidence, but it's nevertheless useful to note this predicted match between modern ideas and fossil data.

    A selection of pterosaur foraging traces - beak tip impressions and scrape marks - from Jurassic and Cretaceous sites. The black-filled elements are the feeding traces, dark grey are manus prints, and light grey are footprints. From Witton (2017).
    Evidence that not all pterosaurs were obtaining their food out to sea comes in the form of feeding traces - small, paired impressions and scratch marks created by beak tips (above). These were likely formed by pterosaurs wandering over water margins in pursuit of invertebrates and other small prey, much like extant shorebirds and waders. Indeed, if you walk across a mudflat on a falling tide you can find near identical traces made by living avians mimicking this pterosaur strategy. Somewhat frustratingly, the identities of the pterosaurs that made these tracks remain mysterious. That said, in my new paper, I have - finally - formalised a case for a Late Cretaceous Mexican set of tracks and possible feeding traces (panel D, above) having an azhdarchid trace maker.

    Pterosaur feeding evidence: the 'close, but no biscuit' specimens

    Inferring palaeoecological details from fossils can be tricky, and it is unsurprising that some purported insights into pterosaur diets and lifestyles are contentious. One of these is the famous and perhaps darkly comic circumstances surrounding the holotype skull and mandible of Ludodactylus sibbicki, a Cretaceous, likely fish-eating Brazilian ornithocheirid found with a sharp, pointed leaf between its lower jaw rami (panel F in the image above). Much of the 2003 description of this specimen (Frey et al. 2003) discusses this association and concludes that ingestion of these plant remains led to the death of the pterosaur. According to this story, the pterosaur accidentally scooped up the leaf, having mistaking it for its usual prey, stabbed the plant material on its throat tissues, frayed the end of the leaf trying to work it loose, but starved to death before it could dislodge it.

    I must admit a little scepticism about this scenario. This is not because animals getting things stuck in their mouths is implausible, but because the story presented by Frey and colleagues is pretty presumptive. It infers a lot about pterosaur behaviour, foraging strategies, throat tissue strength and so on that we can't confirm at present. Moreover, the hyoid apparatus - the skeletal support for much of the throat and tongue tissue - is preserved lying on top of the leaf, despite the suggestion that the plant matter was deeply imbedded in the throat tissues. How did that work itself loose with the leaf fatally stabbed between the jaws? The answer to that question - as with a lot of questions about this association - would easily fall into speculation and special pleading about all manner of unknown quantities, and thus has little value to understanding fossil animal palaeobiology. Boring and po-faced as it is, I don't think the unusual Ludodactylus holotype provides enough information to tell us much about pterosaur behaviour, or how this unlikely fossil association came to be.

    A similar observation might be made about insect specimens - a dragonfly and lacewing - from the Jurassic Solnhofen Limestone that have torn wings, allegedly from a pterosaur attack (Tischlinger 2000). The logic goes that these otherwise perfectly preserved insects cannot have been attacked by aquatic predators, or else they would have been eaten after their wings were damaged. Failed attack from an airborne predator that would not pursue the injured insects into water is suggested as more likely. Solnhofen deposits do hold pterosaurs that were almost certainly aerial insect hawkers - such as Anurognathus (below, see Bennett 2007 and Witton 2013) - and these might be ideal perpetrators in this scenario.

    Anurognathus ammoni was an insect-hawking pterosaur that lived over the Solnhofen lagoon. Has it left feeding traces on fossil insect wings after a failed attack?
     As with Ludodactylus, this set of circumstances is quite elaborate to base purely on damaged insect wings. The extent of their wing damage is considerably greater than we might expect under general 'wear and tear' and foul play was probably involved, but whether it was a pterosaur, a conspecific, or even those disregarded aquatic predators is difficult to say. I appreciate the logic that aquatic predators would eat disabled insects after a failed strike, but animals are not predictable, logic-driven machines: they make mistakes, strike at things they have no intention of eating, get bored, distracted and so on. In all, other than the fact that these insects were almost certainly attacked by something, it might be difficult to say anything more substantial about their final moments.

    Pterosaurs vs. dinosaurs, crocodyliforms and... the revenge of the fish

    The fossil record gives us an insight on the question "did pterosaurs taste good?", and that answer seems to be "yes". Bite marks, embedded teeth and vomited pterosaur remains indicate that dinosaurs, crocodyliforms and fish all ate pterosaur flesh, at least on occasion (below). Among the more impressive examples of these interactions is a spinosaurid tooth, likely from the Brazilian spinosaurine Irritator challengeri, embedded in the cervical vertebra of an ornithocheirid (Buffetaut et al. 2004). Alas, no other evidence of their interaction was evident on the specimen (a series of pterosaur vertebrae) and it's not possible to ascertain much about circumstances that brought these species together.
    Evidence of many, many things that ate pterosaurs. A, ornithocheirid cervical vertebrae with embedded spinosaurid tooth; B, azhdarchid tibia with tooth gouges and embedded dromaeosaur tooth; C, ornithocheiroid wing metacarpal with unidentified puncture marks; D, Quetzalcoatlus sp. skull with puncture marks; E, Eurazhdarcho langendorfensis cervical vertebrae with crocodyliform puncture marks; F, Pteranodon sp. cervical vertebra with intimately associated Cretoxyrhina mantelli tooth; G, Velociraptor mongoliensis torso with possible azhdarchid pterosaur gut content; H, probable fish gut regurgitate including Rhamphorhynchus bones; I, associated Rhamphorhynchus muensteri and Aspidorhynchus acutirostris skeletons. Images drawn and borrowed from many sources - see Witton 2017 for details.
    The fossil record's most common purveyors of pterosaur murder, however, are not dinosaurs or crocodyliforms, but fish. Apparently out for revenge after learning of all that fishy pterosaur gut content, we've got evidence of fish eating and spitting out pterosaurs, of pterosaurs getting entangled with piscine predators, and even fish bite marks on pterosaur bones. A lot of these pertain to specimens of Rhamphorhynchus and you can read more about them in this post - some of the specimens are exceptional and there's lots to say about them. One of the more famous examples of piscine-pterosaur consumption -  an Italian, Triassic pellet composed of alleged pterosaur bones (Dalla Vecchia et al. 1989) - has recently been reappraised. It's now more reliably interpreted as vomit ball made of bones from the tanystropheid Langobardisaurus (Holgado et al. 2015).

    Lesser known, but pretty darned awesome examples of fishes eating pterosaurs are Pteranodon specimens that found themselves at the wrong end of Cretaceous sharks. Several Pteranodon bones reveal bite marks and even embedded teeth from two genera of sharks, the 2-3 m long 'crow shark' Squalicorax and the larger, 6 m long 'ginsu shark', Cretoxyrhina. The former seems to have eaten Pteranodon flesh on several occasions, while evidence of the latter is only currently known from a tooth closely associated with a cervical vertebra (panel F, above). Further work on the latter specimen is currently underway.

     Feeding traces from these sharks are common in Western Interior Seaway fossils and those of Squalicorax are particularly abundant and taxonomically indiscriminate. Given that even giant marine reptiles are among the species consumed by this mid-sized shark, it's often assumed that this animal was a scavenger, biting into whatever free meat floated about America's continental sea. However, it is less certain that Pteranodon was scavenged by Squalicorax, as even a 2 m long specimen would vastly outweigh the largest Pteranodon. It is not inconceivable that an unwary Pteranodon could be grabbed and killed by a stealthy Squalicorax, though I stress this scenario is no better supported than the shark simply chancing across a Pteranodon carcass. Whatever the scenario, it's somewhat grounding to think of a weird extinct creature like a pterosaur being devoured by a fairly conventional-looking shark. It's a reminder, perhaps, that Mesozoic life was not a pantomime of exotic, giant reptiles and weirdo evolutionary experiments, and that much of our modern ecosystem was in place many millions of years ago.

    The big picture

    Looking at the pterosaur palaeoecological record holistically, what patterns emerge? If we look at where the record focuses phylogenetically (below), it's obvious that our records are significantly biased towards certain taxa - Pteranodon, Rhamphorhynchus, and azhdarchids. Even their close relatives, with similar anatomy and adaptations, preservational conditions and so on, don't get much of a look in. There's a few data points scattered here and there, but tumbleweeds run though the palaeoecological data stores for the majority of the group.

    Attempting to make sense of the pterosaur palaeoecological record in a holistic way mainly shows how paltry this record remains. It's improved a lot in recent years, but we await evidence of diet and consumer-consumed relationships in virtually all major pterosaur clades. The images at the bottom of this figure are takes on known examples of pterosaur ecology: Rhamphorhynchus ingesting fish, and azhdarchids being devoured by dromaeosaurs. From Witton (2017).
    We wouldn't be scientists if we didn't ask ourselves why this is. I don't think it's simply a sampling issue. The pterosaur record is not great, but we are talking about several thousand specimens now - enough that we might start looking at what we don't have as well as what we do. So why does Rhamphorhynchus show 10 palaeoecologically-relevant fossils, but other Solnhofen species only preserve one confirmed piece of gut content? Why do azhdarchids, which are never found in sites of exception preservation and are generally only known from bits and pieces, have a better record than those lineages which are abundant, represented by dozens of complete skeletons, and often found in sites of exceptional preservation? Interestingly, there's no obvious correlation between factors like abundance, preservation quality and palaeoecological data. Several lineages - the ctenochasmatoids (wading pterodactyloids), the rhamphorhynchids (excluding Rhamphorhynchus) and ornithocheiroids (excluding Pteranodon) - have everything going for them in terms of abundant fossils, occurrences in sites of exceptional preservation, and yet they turn up very little in the way of gut content, or evidence of being consumed by other Mesozoic animals.

    My take on all this is that there must other factors at play here. We don't get evidence of pterosaur palaeoecology just by throwing more fossils, or better quality fossils, into the mix. I'm sure these factors have some role, but perhaps only in concert with special traits of certain pterosaur groups - maybe behaviours and anatomies - that allow them to have good records. We might have a good record of azhdarchids being consumed by dinosaurs and crocs, for instance, because their bones are often quite big and allow predators to bite them without destroying them. Perhaps we have good palaeoecological insights for Rhamphorhynchus and Pternanodon because of their habits and behaviour - both have strong aquatic adaptations (see this blog post for ideas on that), and there is a bias towards preservation of aquatic animals in the fossil record. Perhaps this aids preservation of not only palaeoecological data, but also explains why these taxa are our most abundant pterosaurs (>100 Rhamphorhynchus fossils are known, >1000 Pteranodon).

    The pterosaur palaeoecological record, then, is perhaps in a transformative state. Though vastly improved over its condition a few decades ago, it requires further augmentation to provide us with significant insights into pterosaur lifestyles, and to explain its biased nature. However, we should not be too pessimistic about the insight it offers into pterosaur palaeobiology: it still provides useful datapoints that can shape our interpretation of flying reptile ecology for several species. Cliched as it is, the take-home message of this project is that any palaeoecologically-relevant pterosaur fossils are worth putting on record. We still have a lot to learn about how these animals lived and behaved, and direct insights are the most reliable ways to do that.

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