Part 3 on Dinosaur ‘Lips’: An evo-devo perspective

Why Lips?

One of the things that seems to get lost in the lips discussion is the evolutionary reason for lips. Unfortunately, little seems to be explicitly published on the evolutionary pressures that would favor lips. However, we can glean a few likely reasons why extant lipped taxa have them, and see if these reasons apply to dinosaurs.

Hypotheses I have seen proposed so far in online discussions are:

• Prevent tooth decay/dessication
• Protect teeth from damage

Neither of these are particularly compelling, since it fails to explain loss of lips in crocodiles (crocodiles spend part of their time out of water and are hyper predators that often risk damage to their teeth). It also fails to explain why sem-aquatic lizards (water monitors, marine iquana, etc.) have not lost their lips.

Also, unlike mammals and many lepidosaurs, but similar to crocodiles, dinosaurs repeatedly shed and replaced their teeth. In addition, and unlike crocodiles, most dinosaur species have rows of extra teeth right behind, ready to quickly take the place of any fallen teeth. This would mean there would be even lower evolutionary pressure to evolve or retain lips (if they inherited them from a common ancestor) for purposes of protecting teeth. Furthermore, the gingiva in crocodilians are very tough and thick, similar to what is seen as preserved in a specimen of Camarsaurus and implied by other sauropod isolated tooth rows (Wiersma et al, 2016, 2019; Canudo et al, 2018)..

I think it is more likely that lips in mammals and lepidosaurs evolved due for the following reasons (in order of relative importance):

• in mammals,
  • aiding in the suckling of offspring (lips help form a seal to efficiently consume milk)
  • acquiring & digesting food
    • this would be most important in small insectivores in order to help prevent prey escaping, and in herbivores in manipulating challenging food
    • increased surface area for saliva production would help while chewing food for predigestion (and regurgitation in some species)
  • social signals
• in lepidosaurs,
  • acquiring & digesting food
    • because many species tend to swallow food whole, lips would aid by increasing the surface area of saliva production, enabling easier swallowing and predigestion
  • in venomous species, aid in envenomation
  • display

Interestingly, crocodiles do not generally eat their prey whole nor do they chew, but rather tear off pieces in chunks and then swallow the smaller pieces. As regards lips being a requirement to safeguarding the gums, crocodiles have extensive, toughened gums (Putterill, Soley, 2003). These are so tough that if the teeth are pulled from the skull, the dental row can stay together.

Birds will swallow prey whole, but also have a gizzard that assists in processing food, as well as tearing off pieces of fleshes and then swallowing the smaller pieces whole.

Based on fossils that show the gut contents, some predatory dinosaurs did swallow food whole and coprolites seem to indicate that they also ripped of chunks of flesh and bone, rather than eating their prey whole. This means that there was some evolutionary pressure to acquire lips in terms of oral processing, similar to large lizards (e.g., Komodo dragons).

Overall, it would seem dinosaurs had less pressure to evolve lips, as they seemed to consume prey quickly with relative large mouths and long digestive track, did not need to nurse or suckle young and had high tooth replacement rates.

Why Beaks?

The other interesting topic is, if dinosaurs did have lips, why would they lose or reduce them repeatedly in favor of beaks?

It is commonly assumed that beaks evolved as a weight-saving feature in volant clades. However, tooth loss or reduction occurs repeatedly in favor of beaks in many non-volant archosaur clades:

• shuvosaurs,
• aetosaurs,
• silesaurs,
• therizinosaurs,
• oviraptorids,
• Limusaurus,
• ornithomimosaurs,
• alvarezsaurs,
• in the lower jaw at least once in Ornithischia, and probably multiple times in the upper jaw (since most of the members of the major clades have basal members with some teeth in the premaxillae))

Beaks occur in pterosaurs as well, but occur in both toothed and toothless species (e.g., Rhamphorhynchus).

In addition, a partial beak may occur in Bonitasaura and a tough keratinous covering may occur in rebbachisaurids (e.g. Lavocatisaurus) and Camarasaurus (Wiersma et al, 2016, 2019; Canudo et al, 2018). Particularly interesting is the case of Camarsaurus where some of the external oral structure was preserved, and the authors indicate that the texture is similar to that seen preserved on the plates in Stegosaurus ( Siber and Urs Möckli, 2009). It appears then that beak-like structures or full on bird-like rhampothecae occur in all the major dinosaur clades.

Soft tissue in stegosaur plates, purportedly similar to preserved structures seen in Camarsaurus, source: Siber and Möckli (2009)

Fig. 3 from Wiersma et al, 2016

Fig. 1 from Wiersma et al, 2016, showing preserved keratinous gingiva

Fig. 6 from Wiersma et al, 2016

The beak-like structure seen in some sauropods is said to potentially offer support for the teeth and analyses in beaked theropods show reduction in stress too (see image below).

Reduction in stress to skull in models of Erlikosaurus extent of beak. The more extensive the beak, the smaller the stresses. From Lautenschlager et al (2013)

Scelidosaurus diagram from Norman (2020) – note that the distribution of foramina on the lower jaw has similarities to that in some living birds, the upper jaw foramina have similarities to that seen in both lipped and beaked tetrapods. Norman favors a convergent ‘cheek’ covering the sides of the jaws from an expanded m. levator anguli ors. I personally favor a beak that extended from the premaxilla and predentary backward maybe extending into an expanded gape and rictal flange as seen in condors and flamingos.

Also interesting is, that none of the volant mammalian taxa (e.g., bats and gliding mammals), show any hint of evolving a beak. Bats are second-most speciose clade of extant mammals, and all have teeth.

This repeated evolution of beaks is strange, considering how rarely it occurs outside of Archosauria. None of the lepidosaurian clades (with the exception of the sphenodonts, if you can call what they have a beak) have evolved keratinous beaks, as well as none of the mammals (exception: if you consider the “bill” in the platypus and echidnas to be a beak, although it is still rubbery and somewhat flexible), and possibly only one lissamphibian group (the sirens).

If evolving from lips to beaks was not a barrier to evolution, one would expect it to occur more often in the highly diverse and speciose mammalian and lepidosaurian clades.

A developmental evolutionary constraint?

In his 1997 paper, “The evolution of beaks in reptiles: a proposed evolutionary constraint”, M.S.Y. Lee discusses developmental hurdles to evolving a beak. He primary focuses on the presence of a caruncle early in ontogeny as a requirement for evolving a keratinzed beak. The caruncle occurs in these clades:

Source: M.S.Y. Lee (1997)

Source: M.S.Y. Lee (1997)

Lee proposes the reason why certain clades have caruncles and others don’t is due to the evolution of viviparity. E.g., the caruncle serves as the egg-‘tooth’ (not actually a tooth) in hard-shelled taxa, whereas an actual tooth serves the same purpose in squamates and egg-laying mammals. This might explain why the earliest mammals, monotremes, started to evolve a beak-like structure, whereas no other mammalian clades did. Furthermore, the requirement of having a caruncle to break out of a hard egg-shell is probably one of the most difficult constraints to overcome evolutionary, since it is extremely closely related to successful reproduction.

Supplementary figure from Wang, et al (2017)

We know that dinosaurs had caruncles for their egg-‘teeth’ instead of actual teeth, based on well-preserved titanosaur embryos which show a horn-like structure.

Graphical abstract from Kundra ́t et al. (2020)

The “egg-tooth” seen in dinosaurs, as has been preserved in sauropods, is similar to that seen in crocs and birds and not the kind of egg-tooth (which is an actual, temporary tooth) seen in mammals and squamates, and some evidence for a horn-like structure (García ,2007 ; Kundra ́t et al 2020).

From Wang et al 2017

Interestingly, the beak precursors, caruncles, are absent in both therian mammals and squamates (Hieronymus, Tobin. ,2010). This is highly suggestive that there is come developmental antagonism that prevents beaks from evolving in lineages without it. There is no embryological evidence that I am aware of that lips appear in the embryos of turtles, birds or crocodiles and that beaks evolved from them, which would mean your hypothetical scenario of lips being gradually lost in favor of beaks is with out any basis embryologically or genetically as far as I can tell.

Wang, et al (2017) talks about the beak development in adult Limusaurus from toothed juveniles matches the evolutionary developmental scenario of modern bird beaks, which basically shows that the epidermal cells all become cornified during development.

Supplementary Figure 1 from Kundra ́t et al. (2020)

What is also interesting is there is no precedent for having both lips and beaks, unlike beaks and teeth which occur together in pterosaurs and dinosaurs.

So the question is: does the caruncle also serve as an evolutionary restraint for evolving lips? I don’t think we can answer this right now definitely, and the evidence is mostly circumstantial, but I would tentatively propose the answer is ‘yes’ based on the evidence deduced so far. It would appear that keratinized epidermal layers prevent the evolution of lip-like structures by preventing caruncle ‘egg teeth’.

Summary

My reasoning for the absence of lips in dinosaurs is as follows:

(1) The osteology around the margins of the mouth area in dinosaurs is at least as similar, if not more so, to non-lipped living terrestrial vertebrate taxa than it is in lipped taxa, as well as showing enormous variation within all of those clades that do have lips and beaks (see images below with annotations). This falsifies the hypothesis that there are strong, unamabigous osteological correlates for lips or other extra oral structures.

Aardvark skull – has lips in life

Allosaurus skull

Anteater skull – has lips in life

Maribou stork – no lips, has beak

Merganser skull – beaked

Goose – beaked

Dromaeosaur skull

tyrannosaur skull

Burmese python skull

Tegu Skull

Varanid skull

Chameleon spp skull

Chameleon species skull

(2) all the evidence we do have for extra oral structures happens to be of hard, keratinized structures on the skulls around the oral margins in dinosaurs, and lack of preserved structures indicating lips. Furthermore, we have evidence of repeated evolution of true keratinous beaks in many other dinosaur subclades, and sister groups (e.g., silesaurs, pterosaurs) and other archosaurus (Effigia, Shuvosaurus). That, combined with the evidence from the EPB, suggest that the most parsimonious reconstruction would be lipless dinosaurs with the basal condition being hard, keratinous oral structures that evolved into true beaks in many dinosaur subclades.

(3) Embryologically, there are more similarities to birds and crocs

(4) Little to no adaptive reason to have had lips, since evidence suggests that dinosaurs replaced their teeth multiple times per year, and since dinosaurs had very different feeding mechanisms from lepidosaurs and mammals there is no reason they would have evolved analogous structures. The evidence so far suggests that they had thick, tough gingiva “gums” like that seen in crocodiles. Furthermore, the lips in lepidosaurs are associated with producing various types of non-venomous saliva to aid in prey capture (Zaher, H. et al, 2014), which evolved into venom in several clades of lepidosaurs. In mammals, lips aid in suckling young – which would be a strong evolutionary pressure.

In summary, the difference in life histories, food consumption habits and evolutionary distance in animals we know have lips, along with the osteological data and the preserved fossil oral strucutures we do have for them, weighs heavily against the idea that lips were common in dinosaurs. Of course, new evidence could come to light and be described that shows otherwise, but until then I think this is the best interpretation given the data at hand.

Refs—

PUTTERILL, J.F. & SOLEY, J.T. 2003. General morphology of the oral cavity of the Nile crocodile, Crocodylus niloticus (Laurenti, 1768). I. Palate and gingivae. Onderstepoort Journal of Veterinary Research, 70:281–297

Bertin Thomas J. C., Thivichon-Prince Béatrice, LeBlanc Aaron R. H., Caldwell Michael W., Viriot Laurent 2018. Current Perspectives on Tooth Implantation, Attachment, and Replacement in Amniota . Frontiers in Physiology 9: 1630.

Wiersma, Kayleigh & Sander, Paul. (2016). The dentition of a well-preserved specimen of Camarasaurus sp.: implications for function, tooth replacement, soft part reconstruction, and food intake. PalZ. 10.1007/s12542-016-0332-6.

K. Wiersma, P.M. Sander. THE GRIN OF THE CHESHIRE CAT:

ISOLATED TOOTH ROWS AND OTHER DENTITION EVIDENCE FOR A RHAMPHOTHECA COMBINED WITH TEETH IN EUSAUROPOD DINOSAURS. 2019 SVP Abstract Poster.

Canudo, José,Jose, Carballido, Salgado, Leonardo,Garrido, ,Alberto. 2018/12/01, A new rebbachisaurid sauropod from the Aptian–Albian, Lower Cretaceous Rayoso Formation, Neuquén, Argentina. 63. DOI: 10.4202/app.00524.2018 Acta Palaeontologica Polonica

Hans Jakob Siber and Urs Möckli. The Stegosaurs of the Sauriermuseum Aathal. Sauriermuseum Aathal, June 2009.

Rodolfo A. García (2007) An “egg-tooth”–like structure in titanosaurian sauropod embryos, Journal of Vertebrate Paleontology, 27:1, 247-252

Kundra ́t et al., Specialized Craniofacial Anatomy of a Titanosaurian Embryo from Argentina, Current Biology (2020),

Hieronymus, Tobin. (2010). Homology and Evolution of Avian Compound Rhamphothecae. The Auk. 127. 590-604. 10.1525/auk.2010.09122.

Wang, Shuo & Stiegler, Josef & Wu, Ping & Chuong, Cheng-Ming & Hu, Dongyu & Balanoff, Amy & Zhou, Yachun & Xu, Xing. (2017). Heterochronic truncation of odontogenesis in theropod dinosaurs provides insight into the macroevolution of avian beaks. Proceedings of the National Academy of Sciences. 114. 10.1073/pnas.1708023114.

Lautenschlager, Stephan & Witmer, Lawrence & Altangerel, Perle & Rayfield, Emily. (2013). Edentulism, beaks, and biomechanical innovations in the evolution of theropod dinosaurs. Proceedings of the National Academy of Sciences of the United States of America. 110. 10.1073/pnas.1310711110.

David B Norman, Scelidosaurus harrisonii (Dinosauria: Ornithischia) from the Early Jurassic of Dorset, England: biology and phylogenetic relationships, Zoological Journal of the Linnean Society

Zaher, H., de Oliveira, L., Grazziotin, F.G. et al. Consuming viscous prey: a novel protein-secreting delivery system in neotropical snail-eating snakes. BMC Evol Biol 14, 58 (2014).

Part 2 on dinosaur lips

Red tegu skull. Image credit: Wikipedia user HCA.

Well, it has been a few years (!) since my last post, so time to finally follow-up. Last time, my focus was on reasons why I think the arguments in favor of lips are fairly weak: tooth decay is not a good reason for lips as dinosaurs continuously replaced their lips, other aquatic and semi-aquatic tetrapods have not lost their lips (which raises the question of why crocodiles would have lost theirs, if being aquatic is not the reason), crocodiles  do spend considerable time outside of water and appear to be fine in this regard. Happily, Mark Witton agrees that this “dental enamel dessication hypothosis” is a weak argument in his latest book on paleoart (Witton 2018, p. 118 – 119).

The Foramina Argument Redux

A while ago I attempted to refute the idea that the labial row of forminae on the dentary, maxillae and premaxillae are strongly correlated with lips only, since they also appear in lipless animals such as crocodiles, some turtles and some birds. However, I was unaware of Ashley Morhardt’s unpublished thesis (Morhardt 2009) at the time I wrote that article (in 2012). Since that time, her thesis has been cited as supporting lips for theropods, including by Witton.

However, if you look at table 4 in Morhardt’s thesis, it shows a wide range of foramina counts in taxa with and without lips (the croc taxa sampled have counts ranging from 50 to >1000, for instance, as do the turtle taxa). Morhardt in fact notes this,

“It is interesting to note that there are significant exceptions to the cut-off points listed above for Figures 5 and 6 (mean of 100 foramina and 50 foramina per one craniofacial bone respectively). C. ursinus (Northern Fur Seal)and Z. californianus (California Sea Lion) show very high foramina counts, even more so than crocodylians. This is unexpected, as seals and sea lions exhibit the typical mammalian extra-oral coverings, including lips and cheeks, and the implications of these data are discussed below.”

Also, she goes on to say,

“When considering the Mann-Whitney U test results of this study, it is hard to be confident when determining the extra-oral tissue types of extinct animals (Table 2). In many cases, the results for determining differences among the extant extra-oral tissue types, excepting that of bare (group 0), were complex. Likewise, a great deal of variation for both texture and foramina count was present among birds, and this ruled out the possibility of identifying any reliable or practical beak osteological correlates. Therefore, more must be done in the future to attempt new techniques for identifying tissue types reliably in dinosaurs.” (emphasis mine)

She continues,

“Though tissue type cannot be conclusively identified at this time, paleoartists, medical and scientific illustrators, and reconstruction artists may indeed be able to create more accurate and lifelike depictions of dinosaurs with the use of foramina counts. Based on the findings of this study, it is unlikely that dinosaurs were devoid of an extra-oral tissue. The data suggest that depictions of dinosaurs with crocodylian (bare) features would be considered less likely than other extra-oral possibilities.” (emphasis mine)

Basically,she concludes foramina counts seem to rule out croc-like facial tissue, but do not give a good basis for inferring lips specifically, but favor extra-oral tissues of some sort.

So far, no direct fossil evidence has shown soft tissue structures that would support lips in dinosaurs . That said, no such fossil evidence has arisen that shows that they positively do not have lips. (Here I have in mind a mummified theropod skull which could potentially give details such as these or in finely preserved lagerstatten which has sometimes preserved even internal tissues (such as in Scipionyx).

Therefore, this whole discussion is mostly one based on inferring from indirect evidence, largely based on anatomy, ecology and phylogeny.

However, there are two main areas where I think this indirect evidence strongly suggests – but does not prove – a lipless model for theropods, and indeed all dinosaurs (there has been a recent trend where ‘cheeks’ in ornithischians are replaced by lips by some authors and illustrators):  jaw anatomy (covered in this post) and evolutionary constraints (to be covered in another post).

Jaw Anatomy

Image credit: Murdoch University, via Online Veterinary Anatomy Museum (OVAM) project.

Jaime Headden commented in the last post about Tracy Ford’s publication on theropod lips, and it being one of the few that have actually made it all the way to formal publication in a peer-reviewed journal. I had forgotten about this article, which I was happy to find that I still had a copy of sitting on one of my external hard drives. I am pleased to say that much of what he wrote is still applicable, and has not been adequately addressed by those who favor a lizard-lipped model.

It should be noted before I continue that the lizard-model is the only one that I have seen proposed, either in informal discussion on the DML, blogs or abstracts or in the few published papers. There have been no serious comparison with mammals lips, as far as I am aware, likely due to their greater phylogenetic distance  from theropods than lepidosaurs and the unique mammalian facial anatomy which includes many muscles in the lips – different from the largely muscle-less lips of lepidosaurs.

Ford (1997) makes this clear when he says, “Lizards do not have lip per se. Lizards do not have the facial muscles to move their lips that mammals do, so the lips of lizards do not move.” Note this is contrary to what Gregory S. Paul states in his book Predatory Dinosaurs of the World (p. 97 of the Touchstone edition), “As for the lip bands, these were like those of lizards, and were supplied with blood vessels and nerves via numerous small openings (foramina). These lips could be lifted to bare the teeth in a threatening gesture, or lowered to help cover the teeth when the mouth was closed. Restorations that show theropods with naked croclike teeth are very much in error.” Unfortunately, neither author provides a direct citation for either of these statements. So which is it – did lizards have labial muscles with which they could at least slightly move their ‘lips’, or not?

Happily, one of the citations in Ford (1997) does directly address this topic, and quite succinctly. Oelrich’s (1956) description of the head anatomy of Ctenosaura pectinata states (p. 110), “The lips are thin immobile boundaries of the oral fissure. The inferior lips are firmly attached to the paired maxillae. They are bounded externally by supralabial, infralabial, rostral, and mental scales.” (emphasis mine) No labial muscles are noted in his description of the oral cavity. To  be fair, I did notice that Paul corrects this in his Princeton Field Guide (2010, p. 25), stating “the mouth is sealed and the teeth covered by nonmuscular lips when closed”. Note however that the quadratomaxillary ligament and levator angularis oris muscle do connect the mundplatt (this is the ‘cheek’-like subtriangular structure of connective tissue seen in extant lepidosaurs,  as well as in aves and crocodilians when the jaw is open).

The fact that lepidosaurian ‘lips’ are immobile is relevant to this discussion because of the difference in lizard and dinosaur jaw anatomy. I have mentioned this before in passing, but Ford’s (1997) analysis makes this strikingly clear. Unlike in lepidosaurs, where the teeth in the upper jaw stop before going past the foramina (which do supply blood and nerve vessels to the ‘lips’) when the jaw is shut, this is not true in theropods. All non-avian toothed theropods have a significant under-bite in which the upper teeth slide past the the line of labial foramina on the upper dentary.

Varanus sp. Image credit: Meghan Kelley and Katie Sagarin (http://borbl426-526.blogspot.com/2014/02/laboratory-5-lepidosauria-serpentes.html)

Note how in the above picture, when the jaw is shut, the teeth do not go past the foramina.

Savannah monitor skull x-ray. Image credit: Casey Holiday lab. (http://web.missouri.edu/~hollidayca/3DAnatomy/lizard_symphyses_AnatRec.htm, note that web link does not appear to work anymore).

Tegu skull x-ray, jaw shut. Image credit: Casey Holiday lab. (http://web.missouri.edu/~hollidayca/3DAnatomy/lizard_symphyses_AnatRec.htm, note that web link does not appear to work anymore).

It is instructive to see these animals with their heads in vivo:

Savannah monitor. Image credit: Kodie Hayes, Nanjemoy MD, USA  (from exo-terra.com)

Tegu. Image credit: Wildlife and Nature Travel Inc. (http://wantexpeditions.com/getpage.php?pg=tripimg&tid=93&subgal=Pouso%20Alegre%20II)

As can be seen here, the upper ‘lip’ stops right at or slightly below the upper teeth/above the lower teeth. It is then met by the lower ‘lip’ (Kochva, 1978).

Image credit: Elezar Kochva.

However, it is notable that this is not how theropod ‘lips’ in particular are portrayed. Time and time again in paleoart, theropod ‘lips’ are shown stopping at the border of the premaxillae and maxillae. In lateral view, when their jaws are open, the teeth are shown exposed (see nearly every toothed theropod illustrated in Paul’s (2010 & 2016) Princeton book).

Golden tegu head lateral view. Image credit: Stock photo from Alamy.com: http://l7.alamy.com/zooms/9d05034a0c2047209352e76ca1464703/gold-tegu-tupinambis-teguixin-whiptail-family-teiidae-amazon-rainforest-ew8egc.jpg

Besides Paul, even the new crop of All Yesterdays-inspired paleoartists (who are otherwise excellent), can’t help but show theropod teeth when the skull is open in lateral view (with the exception of John Conway). I can’t help but think that is another paleo-meme gone awry.  This does not occur in lizards and does not make much anatomical sense, especially considering what the ‘lips’ were supposed to be for. In the words of Matt Martyniuk (http://dinogoss.blogspot.com/), “You’re doing it wrong”! (Yes, even he sometimes gets things wrong: https://upload.wikimedia.org/wikipedia/commons/archive/8/87/20131122151918!Tyrannosaurus_rex_mmartyniuk.png)  If you absolutely must give your theropods lips, at least do it in a way that is semi-plausible anatomically.

Interestingly, even from non-lateral views, it is sometimes hard to see the teeth in lizards, as the teeth are largely covered by the labial glands:

Tegu, with mouth open head-on. Image credit: Miguel César.

So if you are showing ‘lipped’-theropods with highly visible teeth in your illustrations, closed or open, that is very unlikely to be correct. As can bee seen in the image of the tegu with its jaws open, the labial glands are nearly flush with the teeth.

In a few lizard species, the teeth are sometimes visible. In particular, the butterfly lizards, genus Leiolepis, have large ‘fangs’ that are visible when the mouth is open:

Image credit: Dr. Jessie Maisano, Digimorph (Note that the nutrient foramina are below the fangs on the lower jaw, not being overlapped by the teeth)

Image credit: Getty Images stock photo, Paul Starosta

Hydrosaurus also has teeth that are visible when open, in the lower jaw, and barely visible in the upper jaw:

Image credit: Matthew DeRuyter/Cameron Siler

However, these species appear to be the exception, rather than the rule.

Ultimately, what this means is that in theropods there would be no room for the labial glands in the lower jaw, as the upper margin of the lower jaw (including the nutrient foramina) is *inside* the upper jaw:

Image credit: Tracy Ford (1997, fig.6a & b).

The jaw anatomy of theropods in this sense is very similar to extant crocodilians, where the upper and lower jaws close tightly together, and the lower jaw fits neatly inside the upper jaw

What this means is that the labial anatomy of theropod dinosaurs (as well as sauropods) is in stark contrast to the anatomy of lizards. When they closed their jaws, unlike in lizards, the upper third of the surangular would be under and inside of the upper jaw. The upper and lower jaw closed together fairly tightly (even when accounting for muscles and other tissues which Ford leaves out of his illustrations), meaning there would not be much room for labial glands on the lower law in any case. This also has the additional affect that the teeth in the lower jaw would not really even need lips, as they wouldn’t be exposed when the jaw was closed. If there was no lower lip and only an upper lip (a condition which is far as I know would be unique among tetrapods), there would be no oral seal, meaning the upper lip would dry out, which would cause the problem that the lips are hypothesized to solve! Of course, that may now be irrelevant since the enamel dessication hypothesis doesn’t seem to have much merit (see references to Witton 2018 earlier).

Image credit: Tracy Ford (1997, fig.10c).

In order to have lower jaws that would work, saurischians would have had to have mammalian cheeks & lips, that drooped well below the jaws:

Image credit: madaboutgreys via Getty Images

This is where the reality that lizard lips are immobile and fixed to the jaw via glands and scales, something I mentioned earlier, becomes a problem for the lips hypothesis. Dinosaurs are usually proposed to have lizard-like lips, not the complex mammalian lips that are attached via muscles and can be moved and where theses issues of anatomy could be probably worked around. Mammalian lips have generally not been proposed for dinosaurs for good reason: disparate anatomy and evolutionary relationships rule out these derived structures having been present in dinosaurs. In fact, mammal and lizard lips are not anatomically similar, and are likely convergent structures and not homologues. Witton (2018) claims that the assumption should be that lips should be the default assumption since amphibians, lepidosaurs and mammals all have lips. (Witton [2018, p. 123] claims that amphibians also have lips, but I haven’t had any success in finding literature discussing these structures, and photos showing amphibians with jaws open online do not clearly show any separate extra oral structures other than gums that are flush with the jaw line.) The problem with this argument is that it is not clear that the structures are in fact homologous.

(Side note, the skulls of amphibians don’t have formina that resemble lizards. Example:

Source: Acorn Naturalists (https://www.acornnaturalists.com/salamander-giant-skull-replica.html) Andrias davidianus

Now, you may be thinking, “Aha! So maybe saurischians didn’t have lips, but what about ornithischians? They have teeth that occlude like mammals and some lizards, which wouldn’t cause the problems aforementioned. Couldn’t they have had lips?” This brings us to another point, and why I think it is likely that all dinosaurs were lip-less: evolutionary reasons and developmental constraints. We should try to explain why lepidosaurs and mammals are lipped first, and then see if the evolutionary reasons are applicable to dinosaurs, along with any restraints that might prevent them from evolving them. Are the lips of mammals and lepidosaurs, and possibly lissamphibians, even homologous stuctures? If they aren’t homologous, then an evolutionary argument can’t be made that they would have retained them, and a reason for having them would need to be put forward instead.

References:

Ford, Tracy L. Did theropods have lips? Southwest Paleontological Symposium  – Proceedings, 1997. Southwest Paleontological Society and Mesa Southwest Museum.

Kochva, Elazar . 2. Oral Glands of the Reptilia in Gans, Carl, and Gans, Kyoko A., eds. (1978). Biology of the Reptilia. Volume 8. Physiology B. Academic Press, London and New York. xiii + 782 pp. Published 15 December 1978.

Morhardt, Ashley. DINOSAUR SMILES: DO THE TEXTURE AND MORPHOLOGY OF THEPREMAXILLA, MAXILLA, AND DENTARY BONES OF SAUROPSIDS PROVIDE OSTEOLOGICAL CORRELATES FOR INFERRING EXTRA-ORAL STRUCTURES RELIABLY IN DINOSAURS? Masters Thesis. Unpublished. 2009. Western Illinois University. 48 pp.

Oelrich, Thomas M. The Anatomy of the Head of Ctenosaura pectinata (Iguanidae). MISCELLANEOUS PUBLICATIONS MUSEUM OF ZOOLOGY, UNIVERSITY OF MICHIGAN, NO. 94. ANN ARBOR MUSEUM OF ZOOLOGY, UNIVERSITY OF MICHIGAN. March 21, 1956.

Paul, Gregory S. Predatory Dinosaurs of the World – A Complete Illustrated Guide. New York Academy of Sciences. A Touchstone Book. Simon & Schuster, Inc. 1989. 464 pp.

—. The Princeton Field Guide to Dinosaurs.Princeton University Press. 2010. 320 pp.

Witton, Mark P. The Palaeoartist’s Handbook: Recreating prehistoric animals in art. Crowood. 2018. 224 pp.

Reports of the death of lipless theropods are greatly exaggerated (part 1)

A while ago (over 4 years! Where does the time go?), I wrote a journal on why I didn’t think theropods had lips, at my deviantArt website (http://palaeozoologist.deviantart.com/journal/Theropod-lips-I-don-t-think-so-288659080).  That post generated a number of comments, both in favor of my hypothesis and against.

My attention had been directed to a new abstract was recently published by a commenter on my journal regarding this and I wanted to discuss it. Presented at the 4th Annual Meeting, 2016, Canadian Society of Vertebrate Palaeontology, in it the authors favor giving theropod lips. When I first read it, I thought, “They have a pretty good case, looks like I am wrong, and will need to start drawing theropods with lips again.” However, upon re-reading it, I am not so sure.

I am copying the text of the abstract since it is relatively short:

(Oral Presentation)
Dental anatomy and skull length to tooth size ratios support the hypothesis that theropod dinosaurs had lips
Robert.R. Reisz1, D. Larson2
1Department of Biology, University of Toronto Mississauga, 3359 Mississauga Road,
Mississauga, Ontario, L5L 1C6, robert.reisz@utoronto.ca
2Department of Ecology and Evolutionary Biology, University of Toronto, 100 Queen’s
Park, Toronto, Ontario, M5S 2C6, Canada, derek.larson@mail.utoronto.ca

Two competing hypotheses, whether the large teeth of theropod dinosaurs were
exposed or covered by peri-oral tissues or lips when the mouth was closed, are tested
using phylogenetic bracketing, dental anatomy and development, and regression analysesusing skull length to tooth size ratios.
Two different anatomical patterns can be discerned in reptiles. In crocodiles, the
closest extant, toothed relatives of theropod dinosaurs, about ¼ of the tooth is covered by gingiva, but there are no lips, and the crowns are exposed permanently. In contrast, in extant squamates, a more distant reptilian relative to dinosaurs, teeth are covered by lips when the mouth is closed, and there is extensive gingiva. Phylogenetic bracketing, in the absence of evidence from birds and from fossils would tend to support the hypothesis that the large teeth of theropod dinosaurs would be exposed when the mouth is closed, although there is little reason to suggest that the same was the case for the small teeth of other dinosaurs, like the cheek teeth of ornithischians.

Dental anatomy and development offer a different perspective. As the hardest
vertebrate tissue, enamel has a low water content (Zheng et al. 2013), and is hydrated and maintained by glandular secretions in the mouth. We propose that this requirement of hydration is not possible to maintain if the tooth is exposed permanently. We tested this by examining the exposed teeth of terrestrial mammals (tusks), modified teeth that evolved independently in several mammal clades.

Histological thin sections show that tusks in mammals do not have enamel. At the initial stages of development, some enamel may be formed, but soon after eruption the enamel is worn away, and may be replaced by cementum. This suggests that the large teeth of theropod dinosaurs, all known to have well preserved and maintained enamel, even with specialized ziphodonty (Brink et al. 2015), were not exposed permanently, but covered by reptilian lips similar to those found in squamates.

Similarly, ordinary least squares regression analyses of skull lengths to tooth sizes
in varanid lizards and theropod dinosaurs of various sizes indicate that the teeth of
theropod dinosaurs conform to the same pattern as varanid lizards. This provides strong added support to the hypothesis that theropod dinosaurs had lip-covered teeth, as teeth in theropod dinosaurs are no larger than would be expected in a similarly sized varanid lizard. This conclusion has wider implications, suggesting that this may be the primitive condition for all terrestrial vertebrates, allowing us to test whether the large, tusk-like structures of some basal ornithischians (Weishample and Witmer 1990), or the large canine-like teeth of terrestrial vertebrates (Brink et al. 2015) were exposed or not.

Finally, we propose that the lip-covered dental pattern is primitive for terrestrial
vertebrates, and that of crocodilians is a derived condition related to their secondary
aquatic or semiaquatic adaptations. It should be noted that terrestrial stem crocodilians (Clark et al. 2001) have a dental anatomy very similar to that of theropod dinosaurs, and likely had lips too.

 

Since it is an abstract only, and the actual data hasn’t been published, I can only comment on problems with I see with how they frame the hypothesis and test it.

In the third paragraph they posit that enamel needs to be adequately hydrated to be maintained, and that this would not be possible with permanently exposed lips. They appeal to histological evidence in mammalian tusks that show that the teeth are covered in cementum, not enamel, and thus dinosaurs must have had lips.

There are several problems with this.

(A) Mammalian tusks are very specialized structures and are not used like other teeth. Mammals that have tusks tend to use them in specialized tasks such as rooting through dirt, fighting (as in elephants) or digging (see warthog image below).

Why would we expect animals engaged in such specialized behavoiors to be histologically similar to theropods? I am not aware of any theropod that is hypothesized to have used it jaws (and thus teeth) in similar behaviors. Of course if an animals is using it’s teeth in ways that are being constantly abraded by rough dirt and clashing, I would expect the enamel to be replaced by cementum. I don’t think this is a good behavioral analogy to theropods at all, and thus is a very weak argument in support of lips.

(B) Having teeth that are partially exposed some of the time (for extended periods) and then completely submerged in water on a repeated basis would actually be worse.  Crocodiles spend a significant time sunbathing in order to modulate their internal temperature as they are ectothermic:

If hydration of the enamel were a problem, one would actually expect crocodiles to retain their lips. Anyone who has had to repeatedly wash their hands over an extended period of time knows how repeated washing and drying chaps the skin. For animals that are semiaquatic, one would think if lips were needed in order to protect the enamel, lips would be retained in order to avoid extremes of being dehydrated to being completely saturated.

(C) In addition to the problems with analogous behavior between theropods and tusked mamals, there is another problem: Mammals are, by-and-large, diphyodont, whereas theropods (as well as crocodiles) are polyphyodont. What this means is that most mammals only have two sets of teeth, the deciduous set (aka primary or “baby teeth” in humans), followed by the permanent set. Theropods, on the other hand, continuously shed their teeth throughout their lives. This rate varies, but appears to have been equivalent to modern day crocodiles (http://www.ncbi.nlm.nih.gov/pmc/articles/PMC26184/), about 1 to 2 a year. In at least some sauropods, they replaced their teeth every one to two months (http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0069235).

Unlike squamates whose teeth are directly fused implanted to the jawbone (i.e., no tooth sockets; this can take the form of acrodonty or pleurodonty – the latter in which they are fused or ankylosed to the jaw bone; see Jaime’s comments below on my choice of terminology, as well as my response), theropods and crocodiles also share in having in their dental anatomy tooth sockets (alveoli). What this means is that there is already a replacement tooth right behind when a tooth is lost and can quickly be replaced.

So theropods have the best of both worlds, continuous (see comment below) repeated replacement of their teeth as in squamates, as well as having tooth sockets like mammals.

I would hypothesize that this would enable theropods to overcome any concerns of eroding enamel.

(D) Other semi-aquatic and aquatic toothed animals have not lost their lips, or extraoral seals. If you looked at aquatic and semi-aquatic squamates, such as sea snakes, marine iguanas and and some lizards (such as the Chinese Alligator Lizard, see below), none have lost their lips:

 

Sea snake:

Marine iguana:

Anaconda:

And a nice short video of a water monitor (Varanus mertensi):

 

So I don’t understand what the evolutionary reasons would be for crocodiles to lose their lips, since all other extant toothed reptiles that are aquatic or semi-aquatic have not lost their lips.

Nor have aquatic and semi aquatic mammals:

Elephant seal (female):

Otter:

Orca:

(Quick side note on whales: while whales no longer have muscular movable lips, they have retained the oral seal, and when the mouth is closed, the teeth are invisible).

It’s therefore not clear why crocodiles would lose their lips,  and stating that is because of their aquatic or predatory habits is falsified by the above examples. It is also interesting to note that some of the most derived members of the Trionychia (soft-shelled turtles) have lost (or nearly lost) their beaks (external premaxillary, maxillary and dentary rhampotheca, see Jaime’s comments and my response below; they have retained an internal palatine and tomian rhampotheca) and have actually independently evolved fleshy lip-like structures, and are aquatic:

Note that this really is an independent evolution, as the most basal members of crown Trionychia, such as Carettochelys , still have beaks, whereas derived members, such as Carettochelys Pelodiscus, have lost or nearly lost their beaks and replaced with lips (see cladogram from Wikipedia below). Turtles have interesting implications with regards to phylogenetic bracketing and the biological restrictions on lips, teeth and beaks. In the second part of this article, I want to discuss these evolutionary developmental reasons that, in my view, also suggest no lips – and not just for theropods, but likely for all dinosaurs.

The Incredibly Shrinking Dreadnoughtus

Dreadnoughtus was just described this past September by Lacovara et al. (2014). As per usual, both the paper and the media played up the size of Dreadnoughtus, with CNN in particular declaring on its website that it was “perhaps the biggest creature to ever walk the planet.” *Doublefacepalm* This should not be surprising for those who have followed science journalism covering paleontology, as nearly all gigantic sauropods that have been published in recent memory have had initial size estimates far higher than they likely were. For instance, “Seismosaurus”, Supersaurus, Argentinosaurus, Futalognksaurus, Puertasaurus – to name a few – were all declared to be the “biggest” at the time of their discovery but are now considered to be far smaller than initially reported. Only one of these, Argentinosaurus, may still be considered a contender for the biggest, although it too has had its size estimates reduced. Dreadnoughtus, however, is a particularly egregious example. In the paper, the mass was estimated at 59.3 tonnes, with the length estimated at 26 meters. However, doing my own skeletal reconstruction (see above) based on the 3D model in the supplementary material, I get a significantly different estimate.

My own mass estimate is about 29.2 tonnes, and the length estimate of 21.2 meters. In terms of mass, that is nearly a 50% difference! And the length estimate is still a difference of 18.5%. To get some perspective, that is like saying a person who is actually 5 ft 11 and 180 lbs is 7 ft tall and 360 lbs – a mighty big difference. Now, how did I get my estimate, and why is it so different? I got my estimate in a different way than the authors. I used a technique called Graphic Double Integration (GDI). I will go into detail this method and defend my reconstruction in future posts. For now, I want discuss my skepticism of the methods they used.

They used a mass regression model to predict the size based on methods in Campione & Evans (2012). Campione & Evans (2012) went to great lengths to rebut the slew of criticisms that have been made against these models in the past. Interestingly enough, the mass estimates they get for Giraffatitan and Diplodocus are quite close to mass estimates that I get using the GDI technique for both taxa. They estimate a mass of 26.8 tonnes – 44.7 tonnes for Giraffatitan, with a mean of 35.7 tonnes. A GDI estimate I did for Giraffatitan off of a figure by Greg Paul gave me an estimated mass of approximately 32.8 tonnes, which is quite close to the mean and right within the predicted range. Similarly, for Diplodocus I get a mass of about 10.5 tonnes, and they get a mean mass of 10.9 tonnes, with a range of 8.2 – 13.6 tonnes. Note that these mass ranges for both taxa are +/- ~25%. Applying the same range to Dreadnoughtus gives a range of 40.5 – 67.2 tonnes. The lower end of this range is closer to my estimate, but it is still off by about 25% – a significant difference.

So why is my estimate in this case so much lower than the equations used by Campione & Evans (2012)? One thing to note before I go on is that I think the similarity between my previous GDI estimates and how close they are to the regression method is possibly misleading. We are only working from a sample of 2, meaning the sample size is too small to draw any conclusions from this, it would be good to compare GDIs of the other taxa and compare them. For now, we are not able to do this. The real reason I suspect for this discrepancy is twofold: (1) the regression model is hit-and-miss when it comes to predicting masses in living taxa for which we already know the masses and (2) is that there is good reason to think that Dreadnoughtus is an outlier, and therefore would not be accurately predicted by the regression equation model.

How accurate are the regression equations when applied to living taxa?

In regards to the first point, I took the 2nd regression equation from Campione and Evans (2012) and used it to predict the masses of the living taxa. Doing this, I found that for over a third of the taxa the predicted mean mass that was +/-30% or greater from the observed living mass of the taxa. This is a significant problem, because it shows that for a significant portion of living taxa, the regression model produces a poor fit when predicting masses. In addition, 35 of the 255 taxa had predicted mean masses that were +/-50% from the observed mass, which is nearly 1 in 7 taxa. From this data, it should be clear that while the majority of the taxa have reasonable mass predictions, enough fall out of a range that I would consider reasonable to suggest that, used alone, the regression equations may not be sufficiently robust to predict masses of extinct animals. At the very least, another independent method should be used to give a check on mass estimates. I would suggest that a relatively easy method to do this would be GDI techniques.

Is Dreadnoughtus an outlier?

In regards to the second point, I suspect Dreadnoughtus may be an outlier (being in the range of masses of by more than +/- 50%) because the referred limb bones of Futalognkosaurus are very similar in size to Dreadnoughtus in terms of length. While femur length is a poor indicator of overall size and mass, in other comparable measurements (cervical vertebra size, pelvis size, etc.), it appears that Futalognkosaurus is quite similar in size in general to Dreadnoughtus. Futalognkosaurus was found by Benson et al. (2014) to have a mass of about 38.1 tonnes, which is not too different than my GDI estimate for Dreadnoughtus (although it should be noted that my GDI mass estimate for Futalognkosaurus is considerably lower than these estimates – that said, I consider my Futalognkosaurus reconstruction to be out of date in a number ways). Another reason why Dreadnoughtus is probably an outlier, and therefore not predicted well by the regression equations, is that in statistics there is the danger of extrapolation. This refers to using statistical models to predict values out of the range of the sample data. In this case, while Campione & Evans (2012) do an admirable job of trying to rebut criticism of this, I don’t think they do a very effective job.

For instance, in their data set the largest animal they have data for is Loxodonta africana, at about 6.4 tonnes. This is in comparison to masses of many sauropods which easily out classing this, as even the rather light Diplodocus is at least 50% heavier than this. The predicted mass of Giraffatitan being over 450% heavier than the heaviest taxon in the sample. Therefore, there is good reason to be skeptical of extrapolating animals much larger than the sample the regression equations are based on.

For fun, here is what a 52 tonne Dreadnoughtus looks like with the soft-tissues of my skeletal increased by 50% on the torso and 25% on the neck:

And here is a screen shot of the calculation:

Me thinks that is not very likely.

Up next: A GDI mass estimate for Dreadnoughtus.

References:

Benson, R. B. J., Campione, N. E., Carrano, M. T., Mannion, P. D., Sullivan, C., Upchurch, P. & Evans, D. C. Rates of dinosaur body mass evolution indicate 170 million years of sustained ecological innovation on the avian stem lineage. PLoS Biol. 12, e1001853 (2014).

Campione, N. E. & Evans, D. C. A universal scaling relationship between body mass and proximal limb bone dimensions in quadrupedal terrestrial tetrapods. BMC Biol. 10, 1–22 (2012).

Lacovara, K.J. et al. A Gigantic, Exceptionally Complete Titanosaurian Sauropod Dinosaur from Southern Patagonia, Argentina. Sci. Rep. 4, 6196; DOI:10.1038/srep06196 (2014).

Introduction

First of all, welcome to my blog. I’m Zach Armstrong, “The Palaeozoographer”. I got tired of trying to “blog” via DeviantArt’s journal feature (see my DeviantArt page here: http://palaeozoologist.deviantart.com), so I will probably move all of my longer thoughts here. Hopefully, it will be easier to blog, and I can do it more often. Plus, here, anybody can comment, whereas only people signed up on DeviantArt can comment there. Therefore, the discussions will be more open and included a greater diversity of commenters. I will tend to blog about dinosaurs and my own palaeozoography (aka, “paleoart”), however I will likely cover more broad topics than that from time to time.

What is a “Palaeozoographer”?

Simply put, a paleozoographer is someone who illustrates fossil animals, either as life restorations or as reconstructions of the actual fossil material. I derive it from the term “zoography”, the primary definition of which is “the branch of zoology concerned with animal description.” However, the secondary usage is more analogous to what I have in mind, “pictorial art in general, but especially that which shows animals.” So, in this case, “palaeozoography” is the “branch of zoology concerned with the description of extinct animals in pictorial art in general, but especially that which shows extinct animals.”

This word is not technically a neologism of my own invention, as a quick Google search as of today (January 17, 2015), shows only 45 results (“paleozoography” showing 44 results), so it is not in common usage. The actual term “paleozoographer” or “palaeozoographer” shows only 8 and 24 results in a Google search as of today. Therefore, since it is not in common usage, I feel is OK to appropriate it for my own use.

Why not “paleoartist”?

For sure, “paleoartist” is a much better known term, as is the term “paleoart”, but as has been pointed out by others, it is not actually the best formed word. As constructed, it should mean “ancient art”, presumably referring to art produced by ancient people, such as cave art, etc. I also toyed with the idea of “paleobiographer” (which would be more inclusive of all ancient life, including plants), but that sounds like someone who does ancient biographies.

John Conway has attempted to co-opt the word “paleontography” in place of “paleoart”, however the definition and current usage of that is primarily the “description of fossil remains”, or more simply as “descriptive paleontology”. Also, “paleontography” is slightly more used, which Google showing about 8,300 hits. That said, paleontography has not yet caught on either. I doubt the term “palaeozoographer” and “palaeozoography” will catch on either (too long and clunky), but no matter because I like, being more unique than the other terms available. I am acutely aware that I am being animal-centric here, leaving out those who portray paleobotany, etc. I suppose they will have to stick with the more generic “paleontography”.

So, what will this blog be about?

While palaeozoography encompasses a vast number of extinct animals, I will largely focus on dinosaurs in my own art. Therefore, most of the topics I cover will be dinosaur-related. That said, I don’t intend this to be simply a dinosaur art blog, or even simply a dinosaur science blog, but I hope to cover a wide range of topics of all sorts. That said, both dinosaurs and dinosaur art will be a major if not primary focus of this blog. I am not sure how often I will blog, considering I have been very fickle with posting anything on my DeviantArt page, I can’t promise I will be very prolific. My goal, however, is to blog at least once a week, even if just a short post.

Who am I?

I’m a hobbyist artist, with little formal artistic or scientific training. I, of course, took art and science classes in college, and am deeply interested in both, but do not have an art or science degree. I have an Associate of Arts degree in Liberal Arts with a Mathematics Emphasis from Normandale Community College and an Associate of Arts degree in Accounting from Hennepin Technical College. By day, I work as a pension benefits analyst. My previous work experience includes being a college math tutor for 2 and 1/2 years as well as an IT/Accounting Technician for a year. I have been drawing dinosaurs for a long time, 15+ years, and have had a presence on DeviantArt with my current account for about 4 years as of present, with a shorter stint on there of about 2 years with another account.

Ending remarks

My hope is that this blog will bring further attention and add a new perspective to the intersection of science and art. Reactions, in-depth comments, and criticism are very much encouraged, but my hope is to always keep the discourse intelligent and civil. I reserve the right to censor or, in extreme cases, remove comments that do not adhere to a reasonable person’s definition of civil discourse, especially if comments include graphic language, threats or hate speech. Please strive to be kind to others, even if you intensely disagree with their views.

Hope to see you here!

-Zach

A piece of palaeozoography – an Alamosaurus strolling along, by yours truly.