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.

"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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Celestial Troodon said...

Great post.

One notpick though: the side of the mouth on birds (and mammals as well) is called the commissure, not rictus.

BK said...


Deinocheirus upcoming?

Carliro said...

Definitely very interesting.

In regards to beaks in synapsids it's worth noting that dicynodonts are indeed the only synapsids with beaks. Not even more basal "pelycosaurs" and therapsids - which dabbled into herbivory very frequently - have beaks of any sort.

Personally, I think something very odd was happening to dicynodonts.

Carliro said...

In regards to pterosaurs, beaks probably evolved many times:

- Present in pteranodontids

- Present in nyctosaurids (which are more basal than pteranodontids)

- Present in tapejarids

- Present in thalassodromedids

- Present in neoazhdarchians

- Present in Banguela

- Half-beaks in dsungaripterids, Pterodactylus, rhamphorhynchids and Caviramus (see below)

This is interesting because pterosaurs are often depicted with either keratinised jaws or crocodile-like oral margins, but other than rhamphothecae there's no real discussion on pterosaur oral margins.

I can suppose keratinisation as Caviramus' rhamphothecae occurs in the lower jaw, away from the jaw margin, but still it could just be its lower jaw crest

Duane Nash said...

@Midiaou Diallo thanks for clarification, I think there is a lot of confusing of those two terms. Will clean it up in the future.

@BK Jeong well I have been thinking a lot about dabbling/straining/filtering setting in motion a series of changes that could create a beak.

@Carliro Right?! Dicynodonts are weird. Alien food from some terra forming civilization that sporadically visited primordial earth.

Yeah pterosaurs and their teeth, beaks, are weird and don't seem to fit nicely into a pattern. I mean they seem to have kept their teeth going for a long time and they seem to have invested in some pretty toothy mouths. Then the teeth seem to go bye bye for no really good reason… I do want to look more into filter feeding pterosaurs. If a filter feeding pterosaur reversed course into more of small game - plucking type niche perhaps it would have been easier for it to simply go with a beak?

Unknown said...

First of all, it's nice to see the first thing in a scientific post about beak evolution is in fact a meme...I specifically remember sharing that meme on FaceBook ages ago and you were the first one to like it ;)

Excellent post as always. I've been waiting ages for your post on those "meat curtains" you've been teasing me for quite some time now. And this post is even better than I assumed it was going to be. I have a few questions, but I'll probably get back to you on them sometime soon. Not enough time currently to sit down and have a discussion.

Duane Nash said...

Thanks and the meme was lifted from you posting it Khalil "don't end my life because I relate to memes" Beiting

Andrew Raymond Stück said...

Very interesting article; you make some good points.

Have you heard of trilophosaurs? I literally just found out about these weird archosauromorphs. Not sure if they might factor in to your beak discussion at all.

Matthew Martyniuk said...

It's interesting to note that in both pterosaurs and ornithuromorphs, you have aquatic or water-associated species with generally elongated jaws packed with teeth and beaks on the jaw tips. In both of these lineages you also have frequent toothless spinoff lineages with more extensive beaks. It's hard to look at the beak of Aerodactylus, which is essentially just an extra tooth that happens to be made of keratin, and not ask... why? Just why?

Carliro said...

@Matthew: The origin of pterosaur beaks has been suggested as that in the Banguela paper.

We get to see this process in action in dsungaripteroids, from the "extra tooth" at the jaw end in basal forms to the fully toothless maw in Banguela.

Though, dsungaripteroids are a rather specialised group. I'm also not sure if these "keratin teeth" have been found on taxa like ornithocheroids, for example

Carliro said...

In regards to synapsids I'm also wondering if dicynodont beaks are actual beaks and not something weird like the ungulate jaw pads or tuatara's jaw projection hook.

As true beaks are otherwise attested only in sauropsids, I wonder if scales pay a role in the formation of beaks. Synapsids lack scales, so...

Duane Nash said...

@Andrew thanks, duly noted about trilophosaurs. I am interested in those rearward "chisel" teeth.

@Carliro, interesting about the tuatara jaw projection pseudo beak. I need to investigate Banguela some as well...

Nick Fonseca said...

One thing people tend to overlook in birds is that the fleshy "lipped" area on birds tends to overlay the maxilla which is greatly reduced. The long keratin bill or beak is in actuality an elongated premaxilla. This dovetails well with what is seen in Limusaurus i.e. a beaked premaxilla with lipped maxilla. Maybe GSP's proto-beak isn't so crazy afterall? With regards to beaks in dinosaurs it seems that when they grow a beak they elongate the premaxilla while reducing maxilla length. Even Oviraptorids, and cerotopians did the same thing, reduce the maxilla and extend the premaxilla, and ceratopians went even crazier with the bony rostrum. Being that the lipped area on birds seems to correspond with the maxilla gives some evidence IMO that there was a lip of some kind present on the snout as the basal condition in all dinosaur lineages.

Unknown said...

Alright so time for some questions, and I do apologize since I know you're just gonna repeat yourself. I was a tad bit confused at certain points.

So when and where did meat curtains evolve? It looks as though the whole of Ornithischia evolved beaks so they come from a meat curtained ancestor. Theropoda evolved beaks various times so they too had meat curtains. I would like mention of the possibly beaked Silesaurids, especially since in the latest matrix with Buriolestes and that new Lagosuchid, they turned out to be the most basal Ornithischians. Many of the odd basal Theropods turned out to be basal Saurisichians instead. I'm not saying that it's set in stone this phylogeny, but it's worth great mention. hen we get onto Sauropodomorphs. Regardless of wether or not you include Eoraptor, you still have other carnivorous and omnivorous basal forms like Buriolestes that could easily have meat in this mess of phylogeny I'm confused as to when and where meat curtains evolved. I mean it looks as though it was a basal trait but then you get to derived Sauropodmorphs with their lack of beaks*. What's going on?

*worth mentioning the keratinized mouth area of Bonitasaura and Camarasaurus. Maybe instead of evolving a true beak from their meat curtained ancestors they jsut evolved a beak like structure.

Unknown said...

so what are do you think about the lips of Dilophosaurus? or Coelophysis for that matter? at what stage in theropod evolution do you think the lips loosened, because I'm kinda leaning towards carnosaurs and up

Duane Nash said...

@khalil go back and read the part about Chilesaurus and it's lack of beak and how this supports my notion that lizard like lips were basal to theropods. By evolutionary convergence with herbivorous lizards and sauropods I am inferring that Chilesaurus never grew a beak because it had tight fitting lips i.e. they were not cumbersome for precise nips and bites needed for herbivory. When and how the transition from lizard lips to meat curtains occurred has a lot to do with when feathers replaces scales and then scales were lost off of the oral margin. That is my current thinking.

So I notice several have asked how far this morphology might go back… my current thinking is that the looser, drapier "meat curtain" look is tied into the evolution of feathers and subsequent loss of scales on the head and around the oral margin. Scales in my view kept the oral margin tight and trim, when they were lost it got a lot more baggy. I am sorry if that confounds the situation further - because how far back we take feathers or a full filament coat - is always contested.

Feliforma said...

IIRC, Macelognathus was a Crocodylomorph that had a lower jaw beak but not an upper jaw one.

Duane Nash said...

@Whasit Toya Thanks I knew there had to be a beaked croc somewhere!!

Unknown said...

Well I find it likely that meat curtains were ancestral to Dinosauria because we have beaked Ornithiscia, then Saurischia is a little weird. We have meat curtains basal to Theropoda but it would seem at first it wasn't to Sauropodomorpha. But by looking at what the known fleshy integument of the lips are found in Sauropods I find it likely they were also going along the path of "beaks". But instead of evolving true beaks they evolved the next best thing; a "protobeak". Look at Camarasaurus and Bonitasaurua. They don't have beaks but instead of highly keratinized lips that act just like a beak. Why they would grow a protobeak instead of a full fledged beak beats me, but regardless this still looks like the same case that was going on with all other Dinosaurs that became herbivores. And it just so happens that these are the only two sauropods with known facial integument AND they aren't that closely related so it's likely they have a common ancestor with such a proto beak. Maybe there wasn't a major evolutionary pressure to grow a full fledged beak due to their foraging strategy, and that a proto beak was good enough. No need to expend so much energy in evolving and growing a beak when the job is already done with a proto beak. And onto Chilesaurus, whose to say it also doesn't have a protobeak like the Sauropods? The proto beak is made completely of keratin so unless we find a well preserved face then who's to say it didn't evolve one as well over it's muzzle? I find this very likely seeing as how it looks like both Ornithischia and Saurischia have a meat curtained ancestor. I mean, it's not more likely that the same meat curtains evolved twice over in closely related, giant groups.

And about the whole feather and scale thing, in your last post you talked about how the norm was for Archosaurs to have a bald face, or rather a face devoid of scales. Crocodiles, Birds and Ceratosaurs show that the head is rarely if ever covered in scales, so meat curtains turning into beaks via the loss of scales for feathers isn't as likely, when scales are rarely the norm on the face; therefor the scales would rarely be in the way of evolving meat curtains, then evolving into a beak since there's plenty of room because of the lack of scales. In fact, the only scaley faces I can think of come from Dinsoaurs like Hadrosaurs that already possessed a beak. This also coincides with the fact that feathers (including the very basal and basic structures) are likely to be basal farther than we think. Afterall, feathers (and pycnofibers) are found throughout Avemetatarsalia, and the very basal structures like Pycnofibers and the things found on Sinosauropteryx and some of the structures on Kulindadromeus are incredibly similar to near identical. AND, the "scales" of Dinosaurs aern't even reptilian scales; they're in fact highly modified feathers. Matthew Martinyiuk has talked about this before:
And a neat little blog has also covered this and it's implications on the feathers and other structures of Kulindadromeus, and all other Dinosaurs:
So feathers are most likely basal to all of these groups. And if not true feathers, than at least most of these groups independently evolved fiborous integument very early into their evolution.

And if meat curtains weren't present in more basal forms like Dilophosaurus, then how could they properly cover up their teeth? I mean, the neuro-vascular foramin is pretty high up compared to those long saber teeth. Unless of course the teeth were partially exposed, in which case it can work out. It'd be incredibly odd and hard to have lizard lips when you're teeth go so far down the jaw line.

Duane Nash said...

Yeah I know that has been suggested before that the "scales" of dinosaurs are feathers that have been developmentally hijacked. Probably true in some cases, especially scutes in theropod tarsals. But far from proven and certainly not proven in all dinosaurs, hadrosaurs for instance did not have scuty tarsals. What can only be known for sure is that scales and feathers are somewhat competitive developmentally. We don't actually know what came first scutes or feathers. For me it is still up in the air and far too presumptive for anyone to make a definite call and when and how widespread feathers or feather like integument arose and how widespread that origin was. For that reason I am not going to be too hasty in advancing when and where "meat curtains" first evolved. I am just happy if people consider that lip design a possibility at this point.

Good mention on Bonitasaura, still very suggestive that beaks or even beak like growths were not very widespread in sauropods. Sure vaguely beak like they would look in some forms, but the jaws of herbivorous lizards are very beaklike too.

I would not be surprised if ornithischians evolved from a lippy omnivorous ancestor. What is interesting to me is that ornithischians kept their back teeth while theropods lost them in the transition to herbivory. I suspect that this is due to the "scissor cut" shearing bite of theropods while ornithischians likely always had some ability to grind their back teeth together.

On Dilophosaurus I think it had partially exposed croc like design towards the front but more fleshy lips towards the rear. I want to draw Dilophosuarus or its much more bad ass cousin Sinosaurus soon.

Beetle Boy said...

Another very good post!

Off-topic, but do you plan on doing anything about oviraptorids and/or therizinosaurids. Two of my personal favourite theropod groups, and I think there's quite a lot of potential in therizinosaurids in particular for speculation.

Anonymous said...

About therizinosaurids, I don't believe they lost their teeth, yet we know some of them have beaks, too.

Unknown said...

Very insightful reply Duane. Keep note that reticula, aka the most common scales in non avian Dinosaurs, are most likely to be highly modified feathers. As is said in Matthew Martinyiuk's post and the paper on integument evolution he quoted.

Why do you say it had croc like open teeth in the front and more fleshy in the back? What first came to mind was a vaguely blood hound look. It could easily cover the teeth completely (though I still find it likely the teeth were in some way partially exposed). Though I do like the look you mention with a croc like snout. It looks nice and I suppose it could have its benefits.

Unknown said...

This was um, something alright. I am a very new reader to your blog posts, and I must say, I am extremely pissed off, but in the best way. I'm mad at myself, and the world, for what has been instilled into my brain and other paleo fans. I am pissed that you have challenged what has been so widely accepted as fact. Honestly, reading these made me feel like an idiot. Projects such as Saurian show their dinosaurs in such a familiar way, that many do not challenge them or oppose them, because they do not stray from what we know and what we have come to accept. Eagle-like dromaeosaurs, lizard-lipped theropods, all of these things have become such the norm, that when someone like you comes in to challenge it, and you bring such a good arguement, I cannot help but to be pissed. So, it the end, I say to you, thanks. Thanks for pissing me and so many other dinosaur fans off. And I am not being sarcastic. I mean what I am saying. These blog posts challenge us to think so outside of the box, and realize that much of what we consider fact is just conveniently appealing speculation. I look forward to future blog posts to come.

Duane Nash said...

@wolf of comely Thanks Wolf of Comedy, love the name by the way. I am glad you are getting something from my posts and you seem open to new ideas. I don't think Saurian is all that bad and like their depictions a lot over all, so I don't want people to construe I am singling them out or such. Paleontology is just so interesting in that it blends science, culture, speculation, creativity all stitched together in a kind of emotional jig-saw puzzle of "paleoart".

@khalil Indeed I think the crux of the problem is what came first the reticula or the feather? I don't think it is resolved either way. That for me makes it hard to decisively pick a side and leave it some what open to peoples own preference at this point. It is interesting to think if stem mammals went through a similar transition of a more scaled like lizard lip oral margin to something more like what we see in modern carnivorans and if this transition was linked to the growth of hair and loss of scales.

Unknown said...

@Duane Nash no problem. Btw, love the beard

SbS said...

One theme amongst fleshy lipped creatures is incisiform premaxillary teeth as in Tyrannosaurs whose scraping tissue off (as evidenced) of fallen prey is very useful.

Nick Fonseca said...

I was just at the zoo and ended up watching the Tiliqua Rugosa AKA Shingleback Lizard AKA Blue-tongued skink. One decided to have a snack and I was able to see the mouth in action. What I found interesting outside of the creepy blue-black tongue, was that the "lips" were laid out similar to how you lay out the lips in your dinosaur representations. the lower "lip" is beveled in toward the tooth row and the upper "lip" overlapped the bevel. The main difference was the scales. In addition, the upper lip was fairly flexible. It was squishing and bending while it took bites of its lettuce. The scales didn't seem to keep the upper lip from moving around from the force of the bite. It reminded me of the image of the wolf biting the watermelon. I thought you might find the anecdote interesting.

Unknown said...

There's been a new and extremely relevant fossil discovery- a new species of Daspletosaurus found with preserved skull textures, largely identical to that of modern crocodilians. So it does appear to have had an extremely sensitive face- just without the associated fleshy structures on top. (Note- it sounds similar to the rumours of the original Carnotaurus fossil having had crocodile-esque facial tissue destroyed during preparation.)

Between this, the Camarasaurus fossil-

and the uniquity of beaks in ornithischians, I'd suggest that keratinous or partially-keratinous oral tissue was basal to dinosaurs or even archosaurs as a whole, and that the drastic differences between bird and crocodile facial structures is because the existing crocodile-esque sensory structures were lost in the probably-basally-granivorous neornithenes.

Unknown said...

Amendment- probably archosaurs as a whole, seeing as even toothed pterosaurs such as Pterodactylus seem to have keratin structures on their jaw tips.

Anonymous said...


Duane Nash said...

@Eurypterid Whoooa pump the brakes!! They did not actually find preserved facial integument, they inferred it from their comparisons - check the supplementary info in the paper. A croc like facial integument has been argued before by Tracy L. Ford. WHile I find some theropods (spinosaurids & other spinosaur mimics like unenlagines) may have went this route I doubt it for tyrannosaurids and most theropods. I go over it in my new post:

c said...

there was an unbeaked chicken of the 19th century which looked a lot like your theropods. C.M. Kosemen shows it here:

Duane Nash said...

Thanks that's a weird chicken. That book I want!!

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