Thursday, February 2, 2017

Lips Before Beaks Part I: Why Grow A Beak?

Let's dive right in shall we? Some of my more persistent readers may have caught onto my none too subtle hints that I have been dropping with regards to non-avian theropod lips. Indeed, I first made the proclamation that "I'm coning for you next lizard-lipped theropods" back during my now infamous posts on sabertooth predator oral soft tissue anatomy. While the extent and applicability of soft tissue covering on the various and diverse varieties of sabertoothed predators is still an evolving and contentious issue my main goal - that we at least now have the space to talk about such issues without ridicule - I feel was achieved. I might have the lost the battle for fully sheathed Smilodon but I won the war for a more free, open minded and multifaceted debate for novel soft tissue oral anatomy in all saber toothed predators.

"No one cared who I was until I put on the mask."

What lies behind the keratinized edifice of the beak? What secrets will it betray…

A frequent theme and constant source of needed intellectual dismantling in this blog is the perpetuation of false dichotomies.  Regular readers will note that I have went up against false dichotomies in my various posts on Spinosaurus locomotory methods (belly sliding and bottom punting versus obligate bipedalism/quadrupedalism and ill-equipped swimming) and most recently highlighting naked skin on the face of theropods as a viable alternative to the hemmed in scale/feather extremes. Similar to the feather vs. scale debate the lip debate has become hemmed into two fiefdoms: the croc-like keratinized oral margin and squamate like lizard lips. As I will address in this and subsequent posts the croc-like keratinized lip and lizard lip gestalts likely occurred in some theropods. But far more prevalent - especially on some of the more well known theropods - is a completely different and novel lip design that I will be arguing for.

The "lizard lips" hypothesis rests fairly squarely on the presumption that non-avian theropods had scales on their face right up to the oral margin. However in my last post I attacked this notion, noting that modern aves lack scaled heads and even crocodiles lack scaled heads.  While I do think some theropods had croc-like keratinized oral margins and some basal theropods likely had squamate lizard like lips, regular readers will know that I have been  dressing my theropods in a unique oral fashion for some time now. I want to in fact give this unique theropod lip design - the third option I alluded to earlier - a name, and in typical antediluvian salad fashion the name does poke fun and have a certain mischievous, provocative and subversive appeal: meat curtains.

Kill It With Fire!! Monolophosaurus displaying its meat curtains. credit Duane Nash

Maybe some of my younger readers are naive to the term "meat curtain" but, well, inquiring minds will find out. Let's just say the term "vagina dentata" has brand new and startling meaning: this pussy bites back!! The comparison is apt because in both vaginal lips and theropod lips ; a loose seal was maintained; the tissue was non-muscular; the tissue was tough and elastic; and the tissue was highly enervated and extremely sensitive with blood vessels and nerves. In addition you have the double entendre of "meat curtains"; it was literally curtains to any meat that fell between the lips of theropods. This set up also has some vague similarities to mammalian carnivoran type lips. However, I must stress that I am not implying some sort of muscularity to such lips. The upper lips just sort of hangs there and plops down on top of the droopy lower lip when the jaw is shut. An oral seal is achieved, teeth are obscured, the upper teeth do not cut into the lower lips as would be in a problem in many theropod depictions.

In the rough coronal anatomical schematic above you can see how this lip design works and is consistent with theropod jaw and tooth anatomy. The nutrient foramen on both the dentary and mandible feed and enervate the lip tissue. A certain amount of tooth crossing is implied allowing the diabolical theropod "scissor cut" technique. That theropod teeth did cross past the lower teeth is probable and rarely appreciated in most theropod lip depictions. Indeed the manner in which most theropod lips are depicted would have the upper teeth shred the lower lips and gums. This is not an issue in the above design.

This model of Allosaurus at the Fukui Dinosaur Preferctural Museum of Japan stumbled upon a similar design albeit I would prefer no snarl and less scales:

That the upper teeth went past the lower teeth somewhat is supported by the patently obvious observation that the neuro-vascular foramina on the lower jaw directly correspond to the length of the longest teeth from the upper jaw. The foramina on the lower jaw in fact demarcate the extent to which the upper teeth slid past the lower teeth and rested against the lower jaw. Alternatively the foramina on the upper jaw simply line up along the alveolar margin of the upper jaw.

Giganotosaurus credit OldEarth
What's my name?
The pattern of foramina is very consistent across many lineages of toothed theropods. In the upper jaw foramina come right up against the oral margin. In the lower jaw foramina mirror the extent and interplay of tooth depth from the upper jaw. This pattern is exquisitely brought to light in the below picture from Jaime Headden.

credit Jaime Headden

These foramina are not just haphazardly placed along the jaw as should be expected if they indeed had a croc - like oral margin. No, tissue was growing out from these foramina. In the upper jaw this lippy tissue - possibly fairly rigid and even somewhat keratinized - just sort of hung out draping over the teeth. In the lower jaw the lippy tissue did not form a pocket but instead grew out somewhat laterally and hung inferiorly. This sort of saggy, droopy lower lip allowed the upper lip to just loosely drape over it but also provided great tactical support for feeling, sensing, and reacting to struggling prey in the jaw. The upper and lower lip combined to form an extensive neural net.

Note that the lippy tissue allows substantially more tactile and proprioception than either the lizard lip design or the weird baggy "tooth pocket" design that has recently come into vogue. The nerve pads of felids and sensitive muzzle/lips of canids are especially useful for allowing tactile information for these animals.

This tactile ability of the lips came in handy not just in securing and maintaining prey within in the jaw but also potentially safeguarding the predator from injury. Theropods did not just eat harmless sauropodlets all the time, they bit into some pretty strong, feisty, and retaliatory animals, including other theropods. One of the persistent myths that has become somewhat enshrined in theropod folklore is that theropods could literally run up to large prey and, almost effortlessly, carve out long and deep gouges with minimal contact. The thick hides, nodules, and osteoderms of many dinosaurs argues against such quick and effortless interactions. In order to deliver a devastating bite the prey may have to have been engaged for longer than generally appreciated. Biting such animals was dangerous and large lips could have mitigated risks. Large and tactile lips could have served as an early warning device when the animal within the jaws was tensing for a blow or other damaging movement. Having lips that could sense such movements and struggles better allowed theropods with such lips to react and counter such movements. Or, if the stresses were too strong, abort the bite. Remember many theropods had a good chin but they had glass jaws. They could take could dorsal ventral blows and trauma but a lateral blow could have been devastating.

"What about such floppy lips getting cut up during jaw closures? Wouldn't they get cut to ribbons?"

If you look at slow motion video of dogs biting the upper lips actually don't have to be pulled back by muscular action to prevent teeth biting into lips. Actually what looks to be going on is that the momentum of opening the jaws throws the upper lips up and away from the point of impact. Additionally, even if an accidental bite of the lips occurred such structures are very tough and heal quickly. A non-avian lipped theropod throwing open its jaws and biting would have looked vaguely canid like but still kinda alien looking.


Incidentally I do think lips getting cut up is a big problem in the "tooth pocket" design most notably implemented for T. rex in the game Saurian. What is preventing such a loose, non scaled lower lip from  flopping inwards during the bite and getting penetrated? Scales might offer more structural support but if the face was not scaled? I know komodo dragons are often asserted to feature this "tooth pocket" design but is that what is really going on in that mouth? Do komodo dragon teeth actually slide past one another for a true "scissor bite" or do the upper and lower teeth not really cross during the bite sequence? What is all that gummy tissue doing? (hint I will more into komodo dragons on a future post)

In discussing this novel lip structure I like to discuss the genesis of an idea because that is something I always find interesting. Let's revisit the "Hellhound Rex" picture that started the ball rolling for me:

The image disturbed a lot of people, some really rallied against it. That was the clue that I was onto something... and it is not that I think "this is how rex looked for sure" indeed, the best critique I got was from Jaime Headden who, to paraphrase, told me to concentrate on one or two soft tissue structures instead of such a plethora. Admittedly I did take a "throw a bunch of shit at the wall and see what sticks approach". What I think got underneath a lot of people's skin is one specific part of the oral margin. Something that quite happened by accident but which stimulated a kernel of an idea in my head. In other words, something did stick.

You have seen such morphology before. In fact it is directly reminiscent of the rictus in modern avian theropods. It is the rictus that is most often referred to as the "lip" of modern birds and could it be a sort of evolutionary residue? a relict structure from a formerly lippy pedigree of non-avian theropods? Certainly the picture below suggests that rictus tissue can be co-opted for display purposes. Which also suggests that lippy structures in non-avian theropods could have also been co-opted for display purposes.

Theropods - at least those giving rise to beaked birds - likely once all had lips and the evolutionary residue of a formerly lippy dynasty still persists in modern birds in the rictus at the convergence of the upper and lower jaws.

Steppe Eagle (Aquila nipalensis orientalis) credit Quartl CC3.0

In order to illuminate and bolster this claim that meat curtain, quasi-canid style lips occurred in non-avian predatory theropods I am going to go about it in sort of a round about and non-traditional way.
It relies heavily on the principles of convergence and exaptation - two increasingly robust paleontological concepts. The way and manner to ask and investigate the question of why grow a beak is by investigating the fossil record of the beaked and the non-beaked among terrestrial tetrapods. Upon investigating and then illuminating the patterns encountered then offering explanatory hypotheses on why and how these patterns emerged, answers will start to emerge from the fuzz. As I will argue embedded in the question of why grow a beak? is what type of lip was there before the beak?

Why grow a beak? Go ahead and google search that question - there is a dearth of thought on the subject in both scholarly and popular platforms. But this is the question that needs askingSome lines of thinking might speculate that beaks are just an evolutionary eventuality... that they just happen. I beg to differ. When we take a look at the pattern of beaked and non-beaked among terrestrial tetrapods the patterns are indeed interesting.

The Beak Impoverished Kingdom of Synapsids

Let's start with synapsids - mammals and the various stem mammals. They suck at growing beaks. Let's discount beaked whales of course - not too sure if they have true rhampotheca anyways and we are limiting our discussion to terrestrial tetrapods. I guess it is worth mentioning the platypus and some interesting work on the evolution of its "bill" but again that hardly constitutes the keratinized rhampotheca we are talking about.

So why so beak impoverished, furballs?

I will venture it probably has a lot to do with lactation and suckling - that nested quite deep in mammals and maybe even stem mammals is the ability to form a tight seal on female teats/other organs of "nursing" that was advantageous for such feeding.  This in turn begat a very muscular and evolutionarily flexible oral margin. I'm sure that this idea has been suggested before just not sure where or by whom.

We will revisit mammals upon discussion of other beaked animals but just keep this in mind. When mammals make the transition to herbivory or delicate and precise foraging techniques they pretty much universally invest in more intricate and elaborate oral-facial musculature. Think elephant trunks, tapir noses, or even the prehensile lips of bears.

credit Anna Schultz. CC3.0 Tapirus terrestris flehmen response

Prehensile lips and trunks - these are structures on the opposite spectrum from relatively immobile and non-muscular beaks. Yet both extremes can achieve a lot of the same goals ecologically. Both muscular lips/trunks and non-muscular beaks can do some very dextrous and agile manipulations. Keep this thought in your back pocket.

credit Mojcaj CC3.0

To really come up with a beaked dynasty in synapsids we have to go way back to dicynodonts. These stem mammals are truly beaked but their relatively less derived position also begs the question: Did these stem-mammals even lactate/nurse their young? Seems doubtful or, at the very least, painful. This observation supports the earlier contention I made that muscular mouths/lips/oral margins in synapsids has a lot do with suckling.

edentulous upper mouth pad of domestic cattle. credit Woolshed 1 blog

The roughened and sometimes edentulous oral pad of many mammalian herbivores comes the closest to approximating a beak. But even here not quite a beak.

Over all though the lack of beaks among synapsids - especially derived mammals - is notable but there are good hypothesis to explain the dearth of beaks.

The On Again Off Again Beaked Diapsids

It's really when we get into diapsids that some interesting patterns emerge. Forgive me for using somewhat generalized and familiar names (as i usually do) but this is only for ease of understanding at all levels.

Turtles - always beaked. Probably archosaurs or archosaur cousins. Used to have teeth and beaks but have been eduntulous for some time. However it is worth noting that even after beaks evolved in turtles teeth were not totally lost, this is a concept that I will revisit later on..

Crocodiles - never beaked. Crocodiles figure prominently in the lip debate as well. What is noticeable is that various stem crocs engaged heavily in omnivory/herbivory/insectivory. However unlike the case when theropods became engaged with these lifestyles this move from carnivory to herbivory did not result in beaks for any known crocodyliformes. I will suggest that there is potentially a difference in oral anatomy, i.e. lips the presence or absence there of, that negated a convergence in evolving beaks. Again keep that factoid in your back pocket - crocodiles never evolved beaks even when they switched to an omnivorous/herbivorous diet.

Lizards & Snakes - never beaked. This is an important observation that should not go unstated. Snakes are of course dedicated predators. Lizards on the other hand have experimented with all manner of foodstuffs. However even herbivorous lizards don't grow beaks and become edentulous. They might "tighten" up the keratizined scales around the oral margin but they don't form a true rhampotheca and become edentulous. I will go more into lizards in a bit but the patently true observation that lizards - which by definition have "lizard lips" - never evolved beaks but theropods - asserted to have lizard lips - often evolved beaks.

Sauropods - never beaked. Despite spurious claims of a "beak" in Camarasaurus - which is most likely just highly keratinized scales along the oral margin - there are no beaked sauropods. This is an important observation. Indeed if there is one dynasty of herbivores that begs to have beaks it is sauropods. They live by the motto of bite quickly, don't chew, and swallow so an eduntulous beak would have been perfect for them. Yet in over 140 million years of evolution beaks did not occur in this group and they kept their teeth. That sauropods, like lizards, never grew beaks hints at a commonality in the oral margin in these two groups. Sauropods were, and likely always were, truly lizard lipped with a tight band of scales all the way up to the oral margin.

*Ornithischians - always beaked!! (work in progress)

Pterosaurs - sometimes beaked!! (work in progress)

Crurotarsi - maybe aetosaurs, although might just be a highly keratinized snout? otherwise not much beakyness. (work in progress)

Dinosauromorphs - Did silesaurids have beaks…. hmmm. (work in progress)

*these sections are still works in progress and thinking things through...

"Lizard Lipped" Theropods? Lizards Fail Where Theropods Prevail

Lizard Lips in Theropods a Work of Fiction? Ol' Skool Lizard Lip Carch Shark Cage by Duane Nash

Green Iguana (Iguana iguana) credit Bjørn Christian Tørrissen

The thought dawned on me while driving to work one day. If theropods did indeed have lizard lips we should expect convergence in oral anatomy when dietary changes occur in these respective lineages. In non-avian theropods the transition from a carnivorous diet to an omnivorous-herbivorous diet is commensurate with an increasingly edentulous and beaked oral set up. However when lizards - which by definition are "lizard lipped" i.e. a  somewhat tight, keratinized, and scaled oral margin - transition from a carnivorous or "faunivorous" lifestyle to omnivore and herbivory they never evolve beaks. Never.  Nunca. Not Once. Most obvious are iguana but you have various member of the agamidae such as Uromastyx lizards that are lizard lipped but did not evolve beaks with the advent of ominovry-herbivory. Hell, even the recently discovered fruit eating monitor lizard of the northern Philippines shows no evidence of a beak, and monitor lizard style lips are the style of lip most ascribe to theropods!!

Varanus bitatawa credit ACD CC3.0

Uromastyx acanthinura. credit MAJ Kathleen A. Hoard, U.S. Marine Corpspublic domain
Don't want to leave out the large bodied herbivorous Jim Morrison lizard king from the Eocene: Barbaturex morrisoni.

When faced with a change in diet lizard lipped lizards never evolve beaks. We have to ask ourselves why did non-avian theropods - presumed by many to have lizard lips - always evolve beaks when faced with a similar change in diet? Convergence is a powerful trend in evolution and to not see any degree in convergence between these two lineages when faced with similar adaptive pressures is an observation not to be dismissed.

It is not like theropods dabbled in growing beaks, they fully embraced beaks. Not just avian theropods but Therizinosauria, Oviraptorsauria, Ornithomimosauria, and Elaphrosaurinae. The reason for this convergence in shared oral anatomy - both the reduction and eventual fully edentulous nature of tooth loss and growth of beaks - is tied intimately with diet and feeding anatomy. However the anatomical feature that precipitated this transition in theropods is lips. The question is what did these lips look like?Not the tight fitting, slightly keratinized and scaled lips as we see in lizards. Lips of this sort don't precipitate beaks as shown by the noted absence of beak evolution in lizards.

If we eliminate lizard lips in theropods - at least from those theropods that evolved beaked forms - we are left with meat curtains and croc lips. However no crcodylomorphs evolved beaks and they messed around with all sorts of diets during their long evolutionary tenure. Now I do think that a number of theropods messed around with keratinized croc like oral margins - but among those that evolved into beaked forms I don't think that such an oral margin occurred.

So by eliminating croc-lips and lizard-lips from the ranks of those theropods that evolved beaks what are we left with? meat curtains.

The style of lips that precipitated the evolution of beaks were of a much more looser and pendulous variety - a far cry from the tight fitting shellac of lizards lips. That theropods equipped with such "meat curtains" unanimously replaced them with keratinized rhamphotheca i.e. "beaks" speaks not to the superiority of this lip design with regards to omnivory-herbivory but to the cumbersome and inefficient design of such lips when engaging in such a diet.

Let's play a little thought experiment: Imagine that you are a putative "lizard lipped" theropod that fits this niche of transitional omnivore-herbivore. As compared to your carnivorous brethren you have to spend a lot more time out and about foraging for food. This diet requires a lot of quick and precise nips and bites. Sometimes you are trying to only eat certain parts of a plant and avoid other parts. Sometimes you are selecting nutritious fruiting bodies or fresh green growth, other times you are precisely picking up fallen fruitifications or seeds off the ground. Since the oral margin you have - your "lips" - is a tight fitting rim of scales there is nothing to really impede this foraging ability. More so than that there is no evolutionary imperative to grow a beak or lose your teeth. In fact your "lizard lips" are already a sort of proto-beak of their own.

Long story short if you were a theropod or a lizard equipped with such an oral anatomy no real evolutionary pressure to tighten and clean up the oral margin - the tight fitting scaled lizard lips do the job just fine. No need to lose your teeth either.

Now contrast this scenario with a putative theropod trending into omnivory-herbivory but instead of giving the animal clean and trim "lizard lips" endow it with the cumbersome and sloppy "meat curtains" lips. Now making all those precise nips, pecks, and bites on small items gets a lot more trickier. Your fully carnivorous brethren have no problem operating with large, drooping lips - a quick and violent bite and snatch is all that is needed. But now you find yourself out and about foraging for a lot longer to get your nutrients. This puts you at risk for predation. Because your lips are big and cumbersome and don't quite form a nice clean cutting edge you find yourself having to bite repeatedly at things. Plucking small seeds and fruits from the ground is sloppy. You can't always make the precise bites on select bits of foliage. All the extra time spent foraging puts you at greater risk from predators.

Faced with such a maladaptive situation the solution is simple: tighten up those fleshy, pendulous lips into a nice trim, neat, and keratinized lippy margin. In other words grow a beak. The exaptation for growing a beak in this scenario is not actually some putative proto-beak or such, no it is the exact opposite, a cumbersome "meat curtain" ill-equipped for precise and repeated bites and pecks. Optimal foraging theory dictates that such an evolutionary change would occur in such animals.

Yes For Limusarus, Herbivory & Beaks, and the Quest for Carotenoids

Now I have been planning to consolidate these ideas for a while now and I knew it was going to be a bit tricky to splice apart how all the different birdy, sort of birdy, weird theropods transitioning into herbivory fit along this gradient from toothy to reduced teeth to edentulous. But then I saw the talk on Limusaurus at SVP 2016 SLC and the subsequent paper came out and it was like a god-send. Limusaurus encapsulated this whole transition from a toothed predator to an edentulous beaked herbivore with gastroliths all nicely wrapped up in one complete ontogenetic package!!

Extreme Ontogenetic Changes in a Ceratosaurian Theropod.

This paper (Wang et. al., 2016) encapsulates in one animal the transition from a carnivorous to a more omnivorous/herbivorous lifestyle. In addition to the growth of a beak and loss of teeth evidence of gastroliths and stable isotopic chemistry provide independent lines of evidence converging on the same conclusion: beaks and the evolution there of are not evolutionary eventualities but are coincident with a transition of carnivorous to herbivorous lifestyles and loss of teeth. This trend is very noticeable in theropods and mention of the seed eating avialian Jeholornis is also warranted as it retains some teeth in immature specimens. Harpymimus too and probably a bunch of others I am forgetting.

Jeholornis credit Matt Martyniuk

As the lippy oral margin gets more keratinized it renders the teeth obsolete furthering the loss of teeth and edentulous condition in omnivorous/herbivorous theropods and ultimately modern birds. That the loss of teeth in theropods transitioning into herbivory is commensurate with a transition into herbivory is bolstered by the retention of teeth in many predatory stem birds/enantiornithines as well as the evolution of "pseudo-teeth" and shredding choannal papillae & serrated tongues in many hunting, fishing, and scavenging birds. Limusaurus and its revelations are so important and, well to put it frankly, startlingly fortuitous in documenting this transition from a predator to a beaked herbivore but in reality there were probably many species that fell upon a gradient of lipped predator to quasi-beaked increasingly keratinized toothed omnivore to fully beaked herbivore. I made some rough illustrations to illustrate this transition:

Stage 1: Fully predatory and fully lipped. Will occasionally augment diet with select fruitifications and stomach contents from herbivore prey for display colors and carotenoids. A diffuse coevolutionary partnership has begun with the propagules of several plants enlisting the aide of such carnivores to help spread seeds (i.e. the rotten flesh/cheese odor of ginkgo fruits). Has undergone evolution of protofeather "dino-fuzz" and has subsequently lost scales on the head and around oral margin. No "lizard lips".

Stage 2. Sexo-social signalling devices have stimulated an increased emphasis on colored display for both skin, osteological, and integumentary display. In turn the increase in dietary plants for carotenoids in the diet to support such color displays has created a shift in foraging patterns. Small animals, insects, and scavenging are still important but hypercarnivory and large game hunting has been supplanted by an increased emphasis on high quality plant material, seeds, fruitifications (i.e. cycad, gingko, podocarp propagules) and other vegetative resources in the quest for carotenoids. Commensurate with this shift into herbivory the loose lips around the oral margin have withdrawn and became more keratinized. Some teeth remain, especially at the jaw dip for both grasping, occasional hunting, and defense but other teeth have been lost. Rictal tissue remains at the juncture of the upper and lower jaws is present and is even important for display. The jaw shortens and becomes deeper.

Stage 3. A fully beaked and fully herbivorous realization. Sexo-social signaling and the quest for carotenoids has finally turned a lipped and predatory theropod into a beaked and herbivorous sexual T. rex. Small animals and occasional scavenging are still opportunistically exploited - especially in growing animals and females - but dedicated herbivory is overwhelmingly important. The pubis has tilted back, gut expanded, gastroliths are present, and adults are completely edentulous.

I think it important to iterate that this is not necessarily a straight line progression and there are lots of room for reversions, deviations, and exceptions to this lipped predator to beaked herbivore transition. How you might choose to slot a particular species in this rough spectrum depends on both the ecology of the animal in question and, as Limusarus suggests, its ontogenetic sequence. For some more thought and reference on beaked, half beaked, beaks and teeth in stem-birds go read Matt Martyniuk's post Theropods That Fit the Bill on DinoGoss.

I think it fair to say that there is no eventuality in evolving beaks; beaks are related to an increased dietary emphasis of herbivory (not flight); and neither the crocodile style oral margin nor the "lizard lips" style oral margin produce beaks as neither herbivorous crocodiles or herbivorous lizards/sauropods produced beaked forms.

The End of Lizard Lipped Theropods? Not So Fast...

Am I suggesting we cast a death knell for lizard lipped theropods? At first I thought yes, but I have recently recast my decision.

What translates a good hypothesis into the realm of theory is that it has predictive power. As I have frequently mentioned in this piece sauropods never grew beaks even though their foraging strategy seems like it should compel them to. Since sauropods are only known to have scales, likely never evolved a full coat of filaments, and therefore never cleared up the scales around and on the face, they likely retained an oral margin not unlike lizards. Sauropods, like lizards never evolved beaks because their oral margin was fine as it was for biting, pecking, and plucking as a herbivore. They also never lost their teeth. Now if we work from that observation and realize that theropods and sauropods are in fact kissing cousins we should presume that at least very close to the base of the theropod and sauropod split - before theropods evolved an integumentary coat and lost the scales on their face - there was in fact a putative lizard lipped theropod. A further prediction for this putative lizard lipped theropod is that if it embarked on a quest for carotenoids for display purposes and transitioned to a more herbivorous diet that it would not actually evolve a beak but instead retain teeth in its jaw. Such an animal would deviate from the trend in all other coelurosaurian "feathered" theropods that evolved beaks and trended into omnivory and herbivory.

Ladies and gentleman such an animal exists and its name is Chilesaurus diegosuarezi.

Chilesaurus credit UNO

Chilesaurus has become somewhat lost in the mire in discussions of herbivory, beaks, and theropods. I will offer it is very important in that it is clearly a theropod that made the transition from carnivore to herbivore but it deviates from the trend of beakyness seen in other more derived theropods that likewise changed dietary ecology. For starters this animal was not new to herbivory, it had a rear pointing pubic bone and expanded gut. Furthermore it occurs exactly where we should expect such early experiments in herbivory to exist mid to late Jurassic suggesting that the earliest transitions to herbivory in theropods may have started in the early Jurassic or even Triassic. Finally, as should be expected for an early off-shoot from lizard lipped theropods this animal did not evolve a beak but retained and expanded large cropping spatulate teeth in the front of the jaw. Just like a lizard - or a sauropod - would.

An enigmatic plant-eating theropod from the Late Jurassic period of Chile

a, Partial right (?) maxilla in lateral view. b, Left premaxilla in medial view. c, Right dentary in lateral view.d, Details of dentary teeth in lingual view. e, Crown of unerupted dentary tooth. f, Detail of the carina of an unerupted…
No beaks on Chilesarus, no sir!!

credit Fernando Novas
Although many of the artistic depictions of Chilesaurus give it proto-beak of sorts I think this is more indicative of convention rather than direct proof of a proto-beak in Chilesaurus.

I would be remiss not to mention Incisivorosaurus guathieri. This animal being a coeulerosaur is on the branch that underwent feathering, so it potentially could have had dispensed with scales on the face and lacked true lizard lips. Yet it follows more of the trend we see in Chilesaurus… interesting. More derived oviraptors lost all of their teeth.

Incisivosaurus gauthieri credit Jaime A. Headden
Did Incisivosaurus actually have a beak? Was it just embarking on the process of keratinizing its oral margin? If it was just in the incipient stages of keratinizing that would explain why teeth are still very apparent and important in its feeding ecology and anatomy. The pubic bone was not quite so retracted in Incisivosaurus as compared to Chilesaurus. So Incisivosaurus differed from Chilesaurus in that it was just in the incipient stages of herbivory while Chilesaurus was much further along in its dedication to herbivory. Go further: The Origin of Oviraptorosaurs (Diet in Oviraptorosaurs III)

As I mentioned on my last post it is hard to ascribe hard and fast rules to these things. As soon as you start to press down and announce "Aha that's it!!" exceptions start to arise. Biology is squishy and messy.

But I do think that this approach looking at the beaked and the beak less with respect to ecological imperatives gives a faint signal of likely facial appearance and 'lippiness" emerging through the murk of deep time.

In short my parting thoughts on the lip question in theropods are; basal theropods near the sauropod split likely had lizard lips; spinosaurids, unenlagines, piscivorous & small game hunters, kinked snouted theropods, and abelisaurids theropods of that gestalt may have had partially or even completely keratinized oral margins or perhaps even split the difference i.e. lips on lower jaw & keratin on above jaw for abelisaurids; derived predatorial theropods that had underwent evolution of "proto-feathers" may have lost scales on the face and therefore lost lizard lips and adopted a quasi-canid looking "meat curtain" lip gestalt; these same "meat curtain" theropods underwent evolution of rhampotheca i.e. "beaks" when sexo-social display structures stimulated increased consumption of carotenoids leading to increased herbivory. Beaked theropods survived the K/T extinction, not coincidentally their survivorship has been attributed to an ability peck and forage for seeds and other small food stuffs with their beaks.

What wears a mask of a beak, hides a former lippy pedigree. No one cares about me until I wear the mask.

credit Danielle Dufault

Or.... did some beaked lineages of theropods evolve beaks not through feeding on terrestrial foodstuffs but through dabbling in water for food?

As always there are probably some errors in this post, some stuff I missed... things might change even in the course of writing the next post. Evo-devo stuff is a whole other way of looking at the evolution of beaks & lips that I did not even touch upon. Can a bird be reverse engineered to have lips? What about pterosaurs, they appear to have evolved beaks but not from a lipped condition? and ornithischians?

Upcoming posts in this series will touch upon the promise and peril of inferring too much from komodo dragons; their lip/jaw design; their "gummy" mouth tissue; and some new ideas on their poisonous predatory arsenal; more on the interplay of display pressures stimulating a quest for color building carotenoids; and who knows where else I will go. I don't always know myself. 

Best, Duane


Larson, D.W.; Brown, C.M.; Evans, D.C. (2016) "Dental disparity and ecological stability in bird-like dinosaurs prior to the end Cretaceous extinction. Current Biology V-26 Issue 10 pp1325-1333. DOI:

Theropods That Fit the Bill. Mathew Martyniuk. DinoGoss. January 17, 2011

Novas, F. E.; Salgado, L.; Suárez, M.; Agnolín, F. L.; Ezcurra, M. N. D.; Chimento, N. S. R.; de la Cruz, R.; Isasi, M. P.; Vargas, A. O.; Rubilar-Rogers, D. (2015). "An enigmatic plant-eating theropod from the Late Jurassic period of Chile". Nature522: 331–4. doi:10.1038/nature14307.PMID 25915021.

Wang, S.; Stiegler, J.; Amiot, R.; Wang, X.; Du, G.-H.; Clark, J.M.; Xu, X. (2017)."Extreme Ontogenetic Changes in a Ceratosaurian Theropod" (PDF)Cell Biology27: 1–5.doi:10.1016/j.cub.2016.10.043.

Wednesday, January 11, 2017

Ye Shall Enter the SKINgdom of Heaven by Slaying Infidel Scale Loyalists & Feather Nazis

This post might piss off a few people… including some regular readers of the blog. But if you don't know it already you shouldn't  come here expecting not to be challenged in some ways!! And sometimes we all - including myself - need the piss taken out of us a bit.

credit Hyrotrioskjan aka Joschua Knüppe

The battle of out times - scales versus feathers. I imagine some epic Lord of the Rings battle in middle earth: scale loyalist Orcs massing against feather nazi elves (feather nazi elves lolz). Various banners of the opposing forces drawn up with resounding battle cries and triumphant bellows of warfare. I paint this picture to obviously poke fun at members of both parties and to set a tone of jovial banter. Cuz it is kinda funny when you step back from it and realize 99.999% of people don't really care... Of course I care and so do my readers but I think discussions would be more fruitful if both factions stood down a bit and realized that there are resounding points that both sides make and, as I will highlight in this piece, there are some points and arguments to be made that have largely been circumscribed in the exchange.

But if you find yourself getting heated while reading this just pinch yourself, and then remind yourself that in a world of of growing nationalism, fundamentalism, misinformation campaigns, cyber-attacks, and frank talks of nuclear bombardment what dinosaurs wore for apparel does not really matter much...

The long running scale versus feather argument, largely played out online and largely converging on theropods (especially T. rex) integument has become mired down into two factions.

The pro-scale minions, seemingly on the defeat and defensive suffering wave after wave of feathered theropod discoveries and to top it off ornithischians with filaments. Most damning of all, Yutyrannus a largish tyrannosauroid with abundant feather impressions over large parts of the body. This and other feathered basal tyrannosauroids creating the valid and likely position that more derived tyrannosaurids also sported (some amount of) plumage. Still the pro-scale contingent has reason to remain vocal. Scale or scutes is all we really have for many lineages of dinosaurs; Carnotaurus; derived tyrannosaurids and even T. rex. Scales and scutes certainly have a big role to play in theropod and dinosaur integument and they did so for the duration of the Mesozoic.

credit Chris Masna

Diametrically opposed to the scale loyalists are the self proclaimed (I kid you not there is an actual satirical deviantart group) ... "feather nazis". Theirs is the grand and exciting enfluffening movement where everything from sauropods to ceratopsids is gowned and strutted with honest to goodness flowing manes of insulatory integument. Feathers for all!! Feathers right down to the base of dinosauria!! What was considered overly speculative by many in the 90's has now metastasized into a dogma all of its own. What the feather nazis lack in outright evidence they more than make up for in passion and online advocacy (shaming?).

A more succinct analysis would be that nothing triggers a scale loyalist like a fluffy T. rex and nothing triggers a feather nazi like a JP stylized raptor.

My main beef with both factions is that they have perpetrated a bit of a false dichotomy. Lost in the garbled rhetoric of both parties is a third option that has largely been eschewed, silenced, or simply ignored. That third option is nekkid skin itself. As I will lay out nekkid skin perhaps highly keratinized or fleshy - the most basal, germinal layer of all - on the head and even neck in many cases is a quite defensible option for theropods and perhaps even other dinosaurs. 

But first I must slaughter some feather nazis.

Now my issue with the "feather nazis" is not one of complete disagreement. I think there is good reason to argue feathers or at least stage one quilly type things all the way back to the origin of theropods or more  basally to stem archosaurs. However somewhat embedded in this suggestion is that such insulatory "protofeathers", "dino-fuzz" or "quilly" type structures are wholly and completely superior to "naked" scutes and scales in terms of insulatory potential. Or just negating the potential for thermoregulatory capacity in scaley structures at all and dismissing them as "inferior" or harkening back to more "primitive" gestalts.

I believe that scale loyalists have really missed or conceded an important argument in favor of abundant and diverse scaley type integument in dinosaurs.  S.I.G.I.L. "subdermal interstitial gridded insulatory layer" an idea I suggested here a while back makes the case that scales, scutes, even osteoderms, have important potential for insulatory adaptions. Here I suggested that small pockets underneath the outer layer of skin in naked hided dinosaurs created an insulatory vacuum sealed layer when blood was withdrawn internally, basically the same concept of a thermos or people insulating their house with bubble - wrap. So I am not so sold that naked hided dinosaurs are a bad thing of lacking in insulator capacity even at small sizes or in cold climates. If certain basal prosauropods sported insulatory coats (no evidence yet) or basal ornithischians  that we know did (Kulindadromeus yes!!) S.I.G.I.L. might offer a reason why this coat was lost and basically not needed in more derived forms like hadrosaurs, ceratopsids, ankylosaurids etc. etc. or maybe never there to begin with!!

No, my main beef with the "feather nazis" is not just a certain arrogance and condescension in their ranks but a certain amount of committing "sins of omission". We should always be careful to consider are we making the best argument or are we asserting what we want. And I don't really care if you are asserting what you want but don't pretend not to be!!

Time to take the feather nazis down a peg or two.

For best effect the arguments of the feather nazis should be read in the voice of Gollum. Like Gollum, whose mind was poisoned by the ring and all that it brought,  the feather nazis have also came in possession of an ancient and powerful artifact - the feather - that has likewise poisoned and twisted their mind.

"But, my precious, feathers protect from harmful UV rays..."

This is true. But it is a bit of a half truth. What it is suggesting is that if it was not for feathers naked skin would be burnt to a crisp like extra crispy Kentucky Fried Chicken. This is simply not true and you know what protects from UV the best... melanin found in feathers and skin. You don't really need feathers to shield from UV rays, simply put melanin in your skin (as nekkid skin birds do already) and the problem is solved.

"Yes but feather have unique insulatory properties that keep birds thermally protected from extremes in heat or cold my precious..."

This is true. But again the assumption is that scales or scutes (esp. as I outlined in my S.I.G.I.L. hypothesis) could not do that job aptly too. Scales/scutes are rather unexplored as unique thermoregulatory organs in their own right and need not be assumed as vastly inferior to feathers in terms of insulatory properties in light of the lack of study on them. Especially if we assume a lower middle metabolic rate, scute and scale having dinosaurs might have done just fine… sort of like armadillos (more on xenarthans later).

A BIG problem in feathers covering the totality of large archosaur bodies in hot climates (read large dinosaurs in hot climates) is the issue of heat exchange. If the whole or most of the body is draped in feathers - which have excellent insulatory capacity - and body heat rises too high there is nowhere to shed this excess heat. Except, of course, by allowing for large tracts of scaley or nekkid skin (as modern birds do).

"Precious, you have forgot about the heat shedding abilities of the avian lung system..."

Ah... the coup argument against large tracts of naked skin or scales for large feathered dinosaurs in hot climates. The problem is that the poultry ranchers of California don't agree with you.

A bit ago I taught traffic school and one of the more obscure laws on the books is one concerning objects that can fall out of a moving vehicle and not be considered litter (absolving one of a $1000 fine). Clear water and feathers from live birds.

Spilling Loads and Damage to Highway.
(VC §§23114 and 23115) It is against the lawto operate on the highway a vehicle which is improperly covered, constructed, or loaded so that any part of its contents or load spills, drops, leaks, blows, sifts, or in any other way escapes
from the vehicle. (Exception: clear water or feathers from live birds.)

Turns out that transporting live poultry requires open air containers in order for adequate airflow and avoiding heat stress. In fact a cursory investigation into the issue of heat stress and birds (just google birds overheat) is rife with accounts of heat induced stress and death.The mighty avian lung system might not be the panacea we assumed it was in terms of preventing overheating. Additionally that turkeys and chicken have both avian lungs and fleshy display structures shows that even with both of these adaptations overheating still occurs. Overheating occurs quite a lot in birds actually. So I would not put much merit in this argument to counter abundant and extensive tracts of nekkid skin or scales.

The better bet for being a large feathered archosaur in hot climates is to clear up large tracts of nekkid skin on the face, around the eyes, the neck, even the chest. Get nekkid. Like Lappet-faced vultures. Or marabou storks. Or ground hornbills.

Pelage Loss: For Some But Not All?

There is one important concession that I have never seen feather nazis make. If insulatory apparel goes way back to the base of dinosauria or even earlier then we must presume that it was secondarily lost in some lineages : sauropods, hadrosaurids, ceratopsids are the most commonly cited potential examples of this. However if we presume that they could have lost their plumage then why can't we do the same for large tyrannosaurids? I don't think it is an argument that the pro-scale loyalists have been vocal enough about. I don't myself necessarily agree with it but I also suspect that tyrannosaurids had a heck of a lot of scale coating and nekkid skin on them.

In fact if people are allowed to have the boldness and audacity to depict "feathered" sauropods (and I believe that they should although I don't necessarily think it likely) they should also be allowed the boldness and audacity to depict a giant, perhaps mainly scaled and nekkid skinned maniraptoran that has lost almost all of its plumage. Developmentally it could happen. Personally I doubt it and I think a wooly sauropod and a mainly featherless maniraptoran are long shots, but if we allow speculation to one extreme why not the other? Boy would that trigger the feather nazis.

The Nekkid Skinned Archosaur 

The argument is rather simple and straight forward. More so than that it is bolstered by the patterns we see in living feathered archosaurs. Go read this excellent online summary from an ornithology class on avian integument

Ye shall know it when ye sees it...

What was once completely scaled shall henceforth be completely feathered...
From the tip of the tail to the tip of the noggin' ye shall know only feathers until...
Conditions henceforth arise that necessitate a shedding of select feathers revealing...
a nekkid primordial skin... rippling, oozing, and stimulating with a lustful passion for display!!

Or to put it another way:

1) Scaled theropod evolves feathers. Not just a few feathers, but a full on coat covering the whole body as evo-devo studies suggest. Because feathers and scales are somewhat competitive developmentally what was skin covered with scales now just becomes skin covered with feathers.

2) Later on certain members of this feathered tribe get big or move to hotter climes or both. In order to shed heat, feathers retract from certain areas - the head, feet, the tail. In certain spots that are prone to impact or abrasion against the ground scales reemerge. This is exactly like the "scaled" feet and legs of modern birds. In other areas the feather retract to reveal nekkid skin.

3) And when modern archosaurs shed the feathers on their head, around eyes, the neck... when birds get nekkid they freaking play with that skin in all kinds of weird and wondrous ways. Big time freaks.

4) Bird skin is thin. If you eat some bbq chicken it comes with the skin. If you order some bbq beef it does not come with the skin. So that when feathers are lost one potential way to toughen up skin is to add more layers, wrinkles and weird growth type thingies. Cancerous looking caruncles and tufts of skin, waddles.

helmeted Guinnea fowl. credit Bob CC3.0

Abyssinian ground hornbill. female. credit Jerry Thompson CC2.0

credit Eric Kilby wattled crane CC2.0

A frequent dismissal of this generous endowment of soft tissue display/thermoregulatory structures onto  non-avian theropods is parroted at me as such:

"Such skin display structures are not that widespread in birds, in fact statistically speaking we probably have not even found a dinosaur with such display structures."

Figure 4. Structurally colored ornaments of a sample of the piciform and passeriform birds examined: (A) Selenidera reinwardtii, (B) Ramphastos vitellinus, (C) Ramphastos toco, (D) Neodrepanis coruscans, (E) Philepitta castanea, (F) Myrmeciza ferruginea, (G) Gymnopithys leucapsis, (H) Procnias alba, (I) Perissocephalus tricolor, (J) Dyaphorophyia concreta, (K) Terpsiphone mutata and (L) Leucopsar rothschildi. A,F–J, reproduced with permission from VIREO; B,C,L, reproduced with permission from Kenneth Fink; H, reproduced with permission from Nate Rice; D, reproduced with permission from Steve Zack; K, reproduced with permission from Tom Schulenberg (From: Prum and Torres 2003).

For starters it is a text book case of bad statistics. While it is true that if you measured the prevalence of naked skin/fleshy display structures in modern birds you would find a fairly low percentage - I would hazard less than 5% of birds if not less have such structures - but numbers without analysis and context is meaningless. What you have to do is look at the likely ecology of dinosaurs and find what birds best match. And if you look at the birds that best match dinosaurs in ecology I would pick the ones that are large (for a bird that would be partridge size), mainly terrestrial or at least feed on terrestrial items, and live in temperate to hot climates. I would not put aquatic birds and passerines high up in ecological correspondence but even some passerines and waterfowl sport naked skin structures. Among the birds I would put forth closest to non-avian theropods ratites, galliformes, "vultures", storks, hornbills, cranes and especially ground hornbills as some of the best matches. Once you start looking at the birds that best fit non-avian theropod dinosaurs ecologically and environmentally you start to see that such nekkid, fleshy, and skin derived display/thermoregulatory features are quite common. Nothing is 100% and not all of these birds fit the bill - but a large enough proportion of them do that we should be highly confident that such displays were at least as common in feathered dinosaurs. More common I would argue because non-flighted dinosaurs could afford heavier skin structures while birds have to be a bit more thrifty in terms of such heavy building material. Also, the compacted lifespan of dinosaurs and hyper-competitive sexual politics of dinosaurs would encourage the elaboration of skin derived display structures on both sexes. Also, and most importantly, because they tend to piss off some feather nazis and anything to take the piss out of them.

Large male Kori Bustard. Gular Display but no nekkid flesh. An important exception to the trend
credit David Berkowitz C2.0

In fairness there are notable exceptions to this large, terrestrial bird with naked skin/fleshy faced pattern. Biology is after all notoriously squishy and as soon as you push down on something and proclaim "this is the answer" exceptions start to arise. Kori bustards are fully feathered and siriemas only have a little eye patch of naked skin. Cranes don't have loads of fleshy skin derived facial structures but they are highly migratory (remember skin weighs more than feather) and principally temperate.  Far be it to me to insist on fleshy faced, skin display structures on all theropods even maniraptorans - I don't really see that this issue is as clear cut as even I would like it to be. Herons are another group that doesn't fit the trends as they have fully feathered necks and faces. However in their case they need to use rapid neck strikes to catch prey and skin weighs more than feathers so better to keep the feathers for display. Certainly smallish microraptorines types likely had fully feathered faces, or species that lived in cool temperate climes (i.e. Liaoning). But gigantic oviraptorines, dromies, ornithomimids, tyrant lizards, therizinosaurs, megaraptors and other largish coulurosaurs I would really hedge my bets towards such  gnarly skin & flesh derived facial and forequarter display/thermoregulatory structures as fairly common. How far back you want to take such skin derived structures depends somewhat on how far back you want to take feathers in theropods. In other words the evolution of feathers begets naked skin derived structures.

The other point lost entirely on some is that I don't have to speculate about nekkid skin and derived structures - we already have proof.

Pelecanimimus polyodon. How come nobody talks about Pelecanimimus anymore? This is a basal ornithomimosaur and therefore a coelurosaur and therefore feathered. The soft tissue preserved around the head and neck as interpreted by the authors is very telling. No scales present. No feathers present. Instead impressions revealing wrinkles (possibly desiccated caruncles?) of skin lacking integumentary structures i.e. no feathers or scales. A soft tissue crest or flange of skin or keratin on the back of the head. A "pelican like" gular pouch. Just as I would predict and just as we should expect for a good number of feathered dinosaurs in hot climates. Soft tissue structures and nekkid skin. Also Edmontosaurus.

*update Darren Naish (see comment) let me know Pelecanimimus soft tissue interpretations are a bit of a wash. What did I say about taking the piss out everyone (including myself)? Maybe the wiki page needs an update too...

credit Cristian-Milia

Of course if an ornithomimid the size of Pelecanimimus is showing a tendency to clear up feathers for nekkid skin and display structures you can imagine how far Deinocheirus could have taken things...

Let's not to forget to feed the rumor mill. If you dig deep enough there are some accounts of nekkid facial skin on tyrannosaurids and ol' sexy rexy himself. Now I don't want ol' Rexy to dominate this discussion but there are consistent rumors of "plucked chicken" looking skin, bits of skin with reduced scalation and completely naked skin. Feather nazis should rejoice at the notion of naked skin because  as I highlighted earlier naked skin implies it was once feathered and there is likely reduced feathering somewhere on the body. But the sheer amount of retrieved "gila-monster" like scalation does suggest that scales were an important and potentially widespread ectodermal covering for tyrannosaurids. Probably more widespread than in the secondarily evolved scalation of modern birds.

I and a few other artists and thinkers that are increasingly embracing nekkid skin on the head & forequarters of theropods are a threat to both the scale loyalists and some feather nazis. I put scale loyalists in a frenzy because this look completely alters the iconic typography of how a theropod head "should" look - primarily portrayed as a tightly adhering scaled shellac over the theropod skull. And I know I really get under the skin of feather nazis because I argue - based on what modern birds do - that the attractive, graceful, and highly feathered facial countenance as depicted in many non-avian theropods is substantially different than what they have become beholden to.

Some feather nazis deserve to be put in their place a bit because some are guilty of the same crimes that they charge the scale loyalists with. What am I saying? Feather nazis often charge the scale loyalists with being emotionally and culturally clinging to an old outdated 90's nostalgia - the T. rex and raptor of Jurassic Park fame. However from my point of view when I advocate abundant fleshy and skin display features in theropods - inspired by birds of course - who do I get the most push back from? Feather nazis. Why? Even though nekkid skin presupposes a fully feathered ancestral state once you go the path of nekkid skin then you pretty much have to go the path of outrageous skin derived structures. And this completely ruins the fully feathered and attractive plumage depicted on the head of most feathered dinosaurs and calls into question how ubiquitous the "ground hawk" look was for dromies. Feather nazis don't like me for primarily the same reason scale loyalists don't like feather nazis. I call into question a certain look that they have grown fond of. Feather nazis can't outright dismiss me based on an adherence to past interpretations as they can do with the scale loyalists.

Confounding the situation is that many paleoartists give theropods a veneer of feathery type insulation but capitulate to the scale loyalists by giving theropods a scaly head. Why do they do this? If you look at what modern birds do when they lose the feathers on the head all you are left with is naked, not scaly, skin.

So far I have taken it a bit easy on the scale loyalists. That is gonna change.

(best read in an awesome - bro voice, whatever that means to you)

"But, yeah, hey man what about like Carnotaurus it had like scales like top to bottom man. Fully bruh."

Ahh I'm glad we get to talk about Carnotaurus. And it was literally shellacked with scales, scutes, nodules galore. Not a feather to be found. Carnotaurus is indeed the clarion call for scale loyalists  and they should not budge from what it tells us - just as feather nazis should not budge from what Yutyrannus tell us. What I really want to talk about is the face of Carnotaurus because, let's be real, that's what we really care about right? The question I ask is did Carnotaurus - and by extension other abelisaurids - actually have a scaly face?

Yeah I am actually serious when I say this. Carnotaurus may have not had a scaly face, it may have indeed had a croc face.

Skin sections (left) indicate that cracks correspond to epidermal bulges that reach the stiff underlying tissues. Immunohistochemnistry (right) indicates increased cell proliferation (green) within the skin grooves corresponding to cracks. Abbreviations: primary (pc) and secondary (sc) cracks (ep, epidermis, de, dermis, bo, bone tissue). from Milinkovitch 2013

Check out this nice summary piece,  croccrack, showing that the assumed scales on the heads of crocs are actually cracked skin that forms embryologically from the underlying bone pressing against it.

Now, I am not one to lean to fully on the extant phylogenetic bracket to infer soft tissues, and I won't start now, but one of the interesting observations is that no living archosaurs have scaly faces. Birds don't although the wood stork comes close with a highly keratinized face. And crocs actually do not have scaly faces, they have a very tight fitting skin that cracks and creases along defined planes of stress embryologically creating the illusion of very irregular scales. Yep, that was something that really threw me for a loop when I first came across that info on Jaime Headden's blog. But it is true, crocs have scales everywhere else on the body but not on the head. Could this have something to do with better use of ISO's on the snout and head... possibly. Stay posted on that thought.

CC3.0 credit A Stranger in the Alps

It is one of those frustrating aspects of paleontology that the holotype of Carnotaurus supposedly contained remnants of the facial skin but they were prepared away... gripes!!

"Originally, the right side of the skull also was covered with large patches of skin - this was not recognized when the skull was prepared and these patches were accidentally destroyed." wiki citing Czerkas 1997

However there are at least some descriptions available of what the facial skin of Carnotaurus looked like which included bits from the lower left jaw and right side of the head:

"Scalation was similar across different body parts with the exception of the head, which apparently showed a different, irregular pattern of scales." wiki citing Donald F. Glut Carnotosaurus: Dinosaurs 3rd edition

Our first clue is that the "scales" of the head were described as "different" from the rest of the body. Hmmm why would that occur? Does the scalation on a monitor lizard head differ substantially from the rest of the body scales? Our second clue is that the scales of the head were described as "irregular"... where have we heard that descriptor before? Oh yeah, the "scales" on the heads of crocs (actually cracks in scaleless skin) are also described as "irregular". Our third clue is that the skull of both crocodiles and abelisaurids are highly rugose, bumpy, and just gnarly looking. The tight fitting skin that covered the skull was equally keratinized, rugose and just gnarly looking. Our fourth clue has to do with why - adaptationally - would crocodiles lose scales on the head? It might have something to do with allowing better transmission of data to those integumentary sensory organs on the head of crocs. Forgive me for lacking a reference but I thing I came across the suggestion of that idea on Mark Witton's blog once... need further info. Regardless I think it worth further investigation.

Remember when it was common sense that crocs had scaly heads? Why, if we for so long assumed that, is it not a definite possibility that the first impulse when confronted with the preserved facial integument of Carnotaurus could the researchers have not made a similar mistake?

Fucking rad, right? Much props to J.W. Kirby for this Aucasaurus with a keratinized but non-scaly head

J.W. Kirby was nice enough to lend his talents for this depiction of an Aucasaurus with a keratinized mug. I think it works exceptionally well and does a good job of splitting the difference between a wood stork and a croc. Visit his deviantart: KirbyniferousRegret

Am I suggesting that abelisaurids lost the scales on their face to enact ISO's? Nope, although the idea of subaquatic abelisaurids has been toyed with, the swarm of data points towards terrestrial. So I don't think that they had ISO's but I do think that they had especially tactile faces. They had tough faces for sure - highly keratinized - but they also had tactile and sensitive regions, especially along the oral margin i.e. the lips. And I would suggest that they had such tactile lips to better react and position themselves with regard to prolonged and dangerous engagements with prey. Their teeth, their jaws their whole predatory apparatus was set up to bite onto and hold onto prey - not slice through it like the vast majority of other theropods. Dispensing with scales on the head allowed for a more tactile and also tough and keratinized predatorial and cranial adaptation to flourish. And also face biting.

Wood Stork. credit Sandy Sharkey/Great Backyard Bird Count

So if you want to draw abelisaur heads a nice informed speculative venture would be to look at crocs and wood storks for inspiration and add some tough but tactile lips and thickened gums!! I am actually converging on a perception that the upper lips of abelisaurids were very keratinized and did not hang low - almost on the path to lipless crocs. I think, however that the lower lips did hang laterally and inferior with a nice big keratinized gummy mess leading up to the teeth. Go bold and add some flesh antlers and outgroths off the cranial crest as suggested by the vessels on the top of the skull of Rugops!!

While we are on the subject of cranial scale reduction, keratinized skin, croc heads, and rugose skulls it is also interesting to wonder if the rugose skulls of other theropods that lived a very facial - tactile existence such as spinosaurids, unenlagines, other theropods and even pachecephalosaurids and some ceratopsids - may have dispensed with scales and opted for keratinized facial halos. Lots of potential candidates there.

I have some other things to say about scales and the potential loss of scales on the heads of theropods but I'm gonna save than for upcoming posts. Just know that I am not done with you yet "lizard-lipped" theropods...

Scale Loyalists Should Not Simply Concede Kulindadromeus or Psittacosaurus

Another issue I take with scale loyalists is that they simply seem to concede animals like Kulindadromeus and to a lesser extent other quilly ornithischians and possibly Concavenator to the feather nazi hordes in their blitzkrieg conquest. Don't stand down scale loyalists these animals have important stories to tell about scales too!!

credit Tomopteryx CC4.0 Kulindadromeus

Kulindadromeus is the best example so I will talk about this little Siberian maverick the most. Somewhat lost in the excitement about this ornithischian with I think 3(?!) different types of filamentous coverings is that it also had a diversity of scaley type coverings. I think 2 or 3 types of scale coatings. That is an important point not to be conceded by the scale loyalists. Think about where these scales were located. On the tail, the hands, the feet. The areas most liable for temperature oscillations. Scales do have an important story to tell and it likely has a lot to do with thermoregulation and scales remained very important for the duration of dinosaur history.

Psittacosaurus soft tissue reconstruction credit:Vinther et al. - 3D Camouflage in an Ornithischian Dinosaur, Current Biology (2016), CC4.0

The quilly Psittacosaurus was pretty small, lived in a cool climate, could have probably grown a coat of insulating filaments. Certainly other similarly sized maniraptoran herbivores and omnivores in the same environment grew a full coat of feathers. So why not Psittacosaurus? We can rule out preservational bias as an argument so often posited for why feathers are "not preserved" as the Xixian beds preserve feathers/filaments well. This is a dilemma that feather nazis simply ignore by pretty much not addressing it or talking around it. It was scaled and those scales may have provided good enough thermoregulatory benefit that a more extensive filamentous coat was not needed.

An important thought to keep in mind with rear gut fermenting dinosaurian herbivores is that they walk around with big compost bins in their gut. Like compost does, rear gut fermentators release heat. This constant slow burn of heat could have allowed for a more reduced and basal insulatory apparel - scales dominating and perhaps in some instances supplanting filamentous coatings. If we look at scales as basically solar panels such animals could have further supplanted their heating costs by stealing and hoarding energy from the sun and environment. Muscular activity, solar panel scales, rearward heat creating fermentation, blood flow and perhaps a rather low and thrifty basal metabolic furnace could have all combined to create an especially energy thrifty and efficient design. An extensive plumage not really called for. This exceptionally thrifty design would have also begat exceptional ability to dedicate food resources to growth as opposed to heating the furnace, in line with the noted size of many dinosaurian herbivores.

Filaments and feathers may not so much as replaced scales but augmented them in some instances, especially in herbivorous dinosaurs.

Xenarthran Dinosaur: The Further Back You Go, the More Complex Things May Get

I want to end this piece by pointing out where I think we might be heading. We might be heading into a  zone of less certainty than more certainty with regard to integumentary structures in not just theropods but dinosaurs as a whole as well as other beasties like various stem-mammals of the synapsid gestalt that have also been receiving interest as goes soft tissue reconstruction. Now I realize that some might not take much solace in this. But I think that we should really begin to expect the unexpected. Before I let you know why I suspect that the integumentary patterns we might infer based on extant relatives might be a little too conservative let me post this abstract to a rather practical and succinct paper.


In zoology it is well known that birds are characterized by the presence of feathers, and mammals by hairs. Another common point of view is that avian scales are directly related to reptilian scales. As a skin embryologist, I have been fascinated by the problem of regionalization of skin appendages in amniotes throughout my scientific life. Here I have collected the arguments that result from classical experimental embryology, from the modern molecular biology era, and from the recent discovery of new fossils. These arguments shape my view that avian ectoderm is primarily programmed toward forming feathers, and mammalian ectoderm toward forming hairs. The other ectoderm derivatives – scales in birds, glands in mammals, or cornea in both classes – can become feathers or hairs through metaplastic process, and appear to have a negative regulatory mechanism over this basic program. How this program is altered remains, in most part, to be determined. However, it is clear that the regulation of the Wnt/beta-catenin pathway is a critical hub. The level of beta-catenin is crucial for feather and hair formation, as its down-regulation appears to be linked with the formation of avian scales in chick, and cutaneous glands in mice. Furthermore, its inhibition leads to the formation of nude skin and is required for that of corneal epithelium. Here I propose a new theory, to be further considered and tested when we have new information from genomic studies. With this theory, I suggest that the alpha-keratinized hairs from living synapsids may have evolved from the hypothetical glandular integument of the first amniotes, which may have presented similarities with common day terrestrial amphibians. Concerning feathers, they may have evolved independently of squamate scales, each originating from the hypothetical roughened beta-keratinized integument of the first sauropsids. The avian overlapping scales, which cover the feet in some bird species, may have developed later in evolution, being secondarily derived from feathers.

Danielle Dhouailly, A new scenario for the evolutionary origin of hair, feather, and avian scale. Journal of Anatomy April 20, 2009

Another important read is this blog post from "feathers" on the big, "feathers" on the small but feathers for dinosaurs one and all? by Jura it is a little dated but still packed with some good info, as well as good comment section and further links.

Now, in several points in this piece I have referred to nekkid skin as the basal or germinal layer - that when scales or fur or feathers are lost what remains is pure skin. This study confirms that "inhibition (of the Wnt/beta-caratin pathway) leads to the formation of nude skin and is required for that of corneal epithelium." Which is pretty much what I have been suggesting happened quite a lot in dinosaurs that were formerly completely feathered but then - for a multiplicity of reasons - lost such feather coatings on parts of the head and potentially forequarters.

A more interesting bit of info from this abstract is the notion that - read modern - mammals and birds have ectoderm primarily programmed to grow feathers and fur respectively. Again, I want to reiterate that this is how modern bird and mammal skin appears to be programmed. But let us not assume that more basal (read extinct) forms were as hemmed in developmentally to form such structures. I first came across this notion in the above Jura post on the topic (feathers for one and all?) and there Jura  referred to as a basic rule of thumb in the comments section: the regulatory pathways, the developmental constraints may have been a lot more lax and prone to slippage, reversions, and wholesale jumbled set ups than what the more modern derived and somewhat set in stone representatives would suggest. A lot more play. A lot more complexity. And a lot less certainty for anyone trying to arbitrate what is accepted and reasonable in paleoartistic representations.

Pink Fairy Armadillo. credit cliff1066 C3.0

*Update 1/22/17. I too hastily made the following comparison and it erroneous. I still think it worthwhile to consider more basal members of dinosaur lineages may have had a diversity of integumentary features - as Kulindadromeus suggests - but as several commentators pointed out the analogy is wrong. I will leave it up as is because I think it important to document things I get right and things I get wrong.

Consider xenarthrans - the strange and alluring mammals that include the extinct glyptodonts and giant grounds sloths, as well as armadillos, sloths, anteaters, probably some other weird ones too I am forgetting. I don't like to use the term "living fossil" but I think it fair to call these mammals the least derived or most basal among extant mammals. The most basal mammals but also the most diverse in terms of integumentary structures. Think about the weird scutes of armadillos and glyptodonts, the coarse hairs of anteaters, the osteoderm studded skin of giant ground sloths. Now in light of what was discussed in the last paragraph where I made the point that the most derived members of clades are "locked into" defined developmental pathways for respective integumentary structures. For extant birds this is feathers for mammals it is fur. But if you go further back into more basal forms in each group it is very probable that there was a  lot more developmental wiggle room, a lot more play, and a lot less capacity to fully predict what was going on in terms of how much, where, and what type of integumentary structures were going on. Consider monotremes, also very basal and also diverse in terms of integumentary types. Pangolins and aardvarks as well.

Now, this is an area of needed study but in light of the basal nature of these animals and the breadth of integumentary structures that they evince I doubt it merely a coincidence that we see this congruence. That pangolins, monotremes, and xenarthrans showcase more diversity in integumentary structures than more derived and numerous ungulates, carnivorans, and rodentia combined is something to think about...

This notion that using highly derived extant relatives to ascribe dogmatic rules to their extinct relatives should not sit too well with both feather nazis or scale loyalists. And you know I like it when both sides of the divide get befuddled. That creates fertile living and creative space to speculate to truly bizarre and jarring amalgamations of quills, feathers, scales, scutes, keratinized skin, wattles, caruncles, frills, dewlaps, and other structures.

In fact we don't have to speculate. Kulindadromeus spells it right out for us being fairly basal and hosting a diversity of scutes, overlapping scales, and various types of filaments. Later ornithischians may have largely dispensed with pelage and just as derived modern birds and mammals are locked into a pathway of fur or hair more derived ornithischians became more and more locked into a developmental pathway of scales. You simply don't see derived ungulates with lumps of osteoderms in their skin do you? And while the maybe - maybe not ulnar quill nodes of Concavenator get most of the attention for that fantastic beast less widely reported is the unexpected diversity and size of large scales preserved with the body. The Mesozoic may have been rife with complex amalgamations of scaly, scutey, quilly, nekkid skinned, and feathery beasties. Enough to confound dogmatists on both sides of the aisle.

Its not about "the enfluffening" or the return of the retrosaur it is about the advent of the weirdening and we have been in it for a while now.

In summary both scale loyalists and feather nazis bring important points to the table but their rigidity sometimes veers into dogmatism.

Naked skin on many formerly fully feathered theropods is a thing, as evinced by Pelacinimimus. The reasons for clearing up naked skin on theropods (extinct and extant) is not fully understood, doubtless multifaceted, and as shown by species such as Kori Bustards and Siriemas not a 100% mandate or law. But it was a trend that was certainly common. The evolution of naked headed theropods depends in large part on how far back fully feathered dinosaurs goes. Whether or not tyrannosaurids sported naked skinned heads is up for grabs but a distinct possibility. Especially considering the tactile nature of their skulls, feathered pedigree, and several anecdotal records of scaleless or almost scaleless hide as remarked by several researchers (Phil Currie & Paul Sereno).

Because bird skin is so thin we should expect that when feathering is lost it should thicken up with wattles, caruncles, fleshy outgrowths, keratinized bits, and other diverse features we see in living naked faced birds. Expandable gular pouches, snoods, crests, and other features were also likely widespread. I would venture that these features are relatively more common in feathered non-avian dinosaurs than flight capable birds because 1) skin weighs more than feathers so flighted animals will tend to be a bit more thrifty with such features compared to grounded animals 2) the hyper competitive, hyper condensed mating politics of dinosaurs would stimulate outrageous, expensive, and elaborate features. Dinosaurs - unlike sea turtles, crocodilians, and long lived monogamous birds species - simply did not have multiple decades to make their reproductive mark. Instead the stakes were high to make their mark when they could and for many species had much less than a decade of good potential mating years. For large and combative males this opportunity may have been substantially less.

Abelisaurids - and by extension perhaps spinosaurids, unenlagines and several other rugose skulled dinosaurs - may have dispensed with scales on the head partially or completely and sported a tight fitting shellac of keratinized skin. Convergent in design with crocodilians and wood storks such a design would offer durability and protection while potentially allowing sensitivity for animals that explored their world largely through their heads.

Much to the consternation of both scale loyalists and feather nazis the more basal we go in many dinosaurian groups the more anarchic and varied might be the integumentary structures. In derived forms feathers or scales seem to predominate the ectoderm in various lineages. In maniraptorans it is feathers, while in ceratopsids, hadrosaurids, and abelisaurids it is scales. However in more basal forms of each group we might expect a veritable riot of weird, diverse, and unexpected integumentary coverings. This prediction is met by the rich and varied ectodermal topography of Kulindadromeus, the potential for both quills and diverse scales & scutes in Concavenator, quills and scales in many ornithischians, and the noted diversity of outgrowths in many basal mammal families today such as xenarthrans.

In short there is a lot to learn. Both scale loyalists and feather nazis have their role to play but I think we might be converging on a world where both sides are too dogmatic and that nekkid skin has a role to play in this as well. As well as keratinized skin. And funky jumbled up, mish-mashed piles of xenarthran like dinosaurs with piles of scutes, filaments, quills and other things galore. For those that like precise laws and set in stone didactic guidelines on how to depict dinosaurs - especially earlier more basal forms in which the developmental pathways were not yet established rigidily - probably not a pleasant time for you right now. And people of such mind sets will probably find greater and greater consternation at the sight of increasingly odd and bizarre dinosaur reconstructions. SUX2BU.

Ok, ok are you still with me? Have I done a good of enough job in triggering scale loyalists and feather nazis? Ok time to trigger myself a bit and it is the consistent critique I always get from some quarters regarding fleshy, hangy things or big lips jutting off the faces of theropods - especially toothy ones. triggrd

"But precious, such features would get snipped right off?!?"

I'm triggrd.
And this is my final word on this.

1) Don't underestimate how tough and flexible skin can be. Chewing on the wattles of a theropod could have been like chewing on a flat tire. You won't really hurt it and you might compromise your position allowing for a more devastating counter strike to the back of the neck, throat, or belly/cloaca.

I really like the thickness, elasticity, and well toughness in J.W. Kirby's depiction of SANTAnaraptor below... they look like tough chew toys that would stretch out and cause frustration to anything that bit into them.

SANTANAraptor  credit J.W. Kirby
2) Critiques of soft tissue display/thermoregulatory structures on toothy theropods should familiarize themselves with the the "handicap" hypothesis of social-sexual signaling structures. In order for a signal to be true and just it must impart a cost on the signaler. That the signal actually imposes some maladaptive traits on the signaler is actually a good thing. Such signals represent the "conspicuous consumption" of the animal kingdom. They also should be expected in animals in which the stakes are high reproductively. And the stakes were definitely high reproductively in dinosaurs. They did not have several decades to make their mark in the Darwinian sweepstakes but only several years. In the largest and most combative large theropods how many years would you expect a large male to reign supreme? 2-3 years? Dinosaur sexual politics was a wild and wooly world, not for the feign of heart.

Also don't be carnivore biased. If you can accept fleshy, hangy wattles, dewlaps on ornithischians, herbivorous theropods, and sauropodomorphs but not on predatory theropods you are being biased. The giant beaks of ornithischians, ceratopsids, the powerful beak and jaws of an oviraptor, a macronarian are not to be trifled. These animals could easily rip your limbs from their sockets and could do the same to any fleshy display device. Should we eschew such devices on all dinosaurs then? - clearly not. In fact Edmontosaurus and Pelacinimimus prove that they had them!!

3) Male bull elephant seals and hooded seals engage in epic biting battle yet maintain fleshy, vulnerable facial outgrowths. Elephant seals form huge colonies... at least some maniraptorans did too. Male elephant seals have a severely limited time to get to the top of the social heap and mate. Theropods - indeed probably all dinosaurs - did not live as long as crocodiles so they were likely under the gun to achieve mating success at any cost. Male southern elephant seals are the largest mammalian carnivoran of all time. Now that is not stated enough in my opinion. The largest mammalian carnivoran of all time is not from the Eocene, Miocene, or early Pleistocene but living with us on earth right now. And it engages in absolutely vicious face biting prolonged skirmishes. And it has the size, strength, and tusks to do some real damage. Just like theropods did. Yet this animal - colony forming, combative, multi-ton largest carnivore ever - it has big, fleshy pendulous display structures right there on the tip of it's face. And you know that sometimes it gets ripped into, indeed it is a bit of a liability in fights but to be a true signal, to evince handicap, to resonate intimidating sounds and visually stimulate opponents - evolution has eclipsed these liabilities and favored large, fleshy pendulous things on the face of an animal that should rightly have them yanked right off. But it has them anyways and most likely did toothy theropods.

And finally - inb4 criticism - highly perceptive and critical reader will have detected what I have done here. By highlighting the need of scale loyalists to look at insulatory and thermal potential in scaley dinosaurs and by suggesting nekkid skin as a kinda proxy for a formerly fully feathered condition, I have deftly played both sides of the aisle and bolstered my claims of 1) S.I.G.I.L. i.e. insulation without feathers and 2) a fairly common evolution of facial nekkid skin and nekkid skin structures in feathered theropods. Duane you self serving bastard!!

Bwa, Ha, Ha, Ha (evil cackle from bowels of paleo - dungeon) stroking my pet cat. "You don't know my paleo super - powers!!"

Scale Loyalists and Feather Nazis recant and end your evil ways and you may yet enter the SKINgdom of Heaven!!


"A Long habit of not thinking a thing wrong, gives it a superficial appearance of being right, and raises at first a formidable outcry in defense of custom". Thomas Paine

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