So, What If Ornithischians Did Have “Cheeks”?

I will not go into too much detail, because I want to work on the analytical part of this more in depth. I started my inquiry into the structure of jaw anatomy in ornithischians roughly about the same time that Witmer and Papp had made their SVP presentation, largely because *gasp* they took away ornithischian cheeks! After I was finished over-reacting to the loss of this beloved imagery[n1], I started thinking about all the reasons why we actually put “cheeks” on these guys in the first place.

Jump forward to 2010 when Paul Sereno, Zhao Xijin and Tan Lin described a new species of psittacosaur, Psittacosaurus gobiensis [n2], and pegged on a shallow fossa on the lateral surface of the maxilla, above the maxillary buccal “fossa” (“mfo” below):

Skull of LH PV2, holotype skull of Psittacosaurus gobiensis. After Sereno, Zhao and Tan, 2010.

Muscle Time

It is a curious fact that of all psittacosaurids, only the type species mongoliensis bears a special antorbital-fossa like depression in this region, with distinct margins and a shelf-like ventral border; it is a possibility that the fossa on the maxilla of other psittacosaurids is instead a remnant of this feature; but also that mongoliensis developed a novel, possibly pneumatic, structure independently of other archosaurs. Sereno et al. argued that this feature may, rather, be a muscle attachment site, and indeed would have supported a muscle not unlike the psittaciform m. pseudomasseter (mPsm) a muscle that divided from the m. adductor mandibular externalis ventralis (mAMEV, a version of the m. adductor mandibulae externalis medius, or mAMEM, which rather than inserting on the dorsal margin of the surangular around the coronoid process as it does in ceratopsians and hadrosaurs, as in lizards and crocodilians (Holliday, 2009), is positioned much further ventrally down the lateral surface of the dentary) and also which originates on the ventrolateral jugal and inserts into the lateral dentary rostral to the insertion of the giant m. pterygoideus ventralis (mPTv), along with the mAMEV. Parrots uniquely exhibit the mPsm among all birds (along with the m. ethmomandibularis, mEM), and may also possess a large, ossified suborbital bone to anchor these muscles, though its expression differs from subgroup to subgroup (Hofer, 1950; Zusi, 1993; Tokita, 2004). Typical mAME muscles originate medial to the jugal bar and extend through the subtemporal foramen formed by the pterygoid, ectopterygoid, quadrate, quadratojugal and jugal bones.

Sereno suggests, rather heretically, that the “premaxilla-maxillary crest” that forms the lateral maxillary-fossa’s dorsal edge and the dentary flange that is characteristic of all psittacosaurids (but also some coronosaurian ceratopsians) formed the origin and insertion points for a “pseudomasseter”-like muscle for the jaw. This is pretty novel, and while I like Sereno’s suggestion (backed up in his “monster” of a monograph on Heterodontosauridae, where he extends the morphology to those little guys), there’s work to be done on whether these structures support muscles, much less match what we have of homologous structures. For extraordinary claims, to paraphrase the late, great Carl Sagan, one must provide extraordinary evidence; Sereno matches odd morphology with extraordinary claims, and it is again to his credit that he’s dumped this within larger, broader works, but less interesting than if he’d presented a paper solely on this topic.

As I said, the same is true of Heterodontosaurus tucki, where Sereno (2012)  reconstructed the mAMEV onto the lateral jugal, beneath the ridge formed by the lateral jugal flange.

Jaw muscle reconstructions in Pionites leucogaster (a), Psittacosaurus gobiensis (b), and Heterodontosaurus tucki (c), after Sereno, 2012. Rhamphothecae in green, muscles in red.

Problematically, mAMEV in this scenario leaves little room for mPTv, which should wrap around the ventral angular and onto the lateral surface beneath the articular joint, and somewhat anterior to it. Sereno correctly notes the function of the surangular ridge as the insertion site for a large m. adductor mandibular externalis superficialis (mAMES), citing Holliday (2009), which arises from the medial surface of the supratemporal bar (squamosal and postorbital). However, Sereno emplaces mAMES onto the lateral surface of these bones, rather than the medial, on the basis of the shallow fossa that surrounds the laterotemporal fossa, including down and along the paroccipital process of the squamosal. Moreover, Sereno also places the m. depressor mandibulae (mDM) onto the lateral surface of the squamosal within this fossa, arguing “the depressor mandibulae in psittacosaurs does not appear to originate on the squamosal posteroventral process or paroccipital process, which in all species of Psittacosaurus terminate laterally as subquadrate processes without hook-shaped ends”; yet it appears that the origin for this muscle is on the posterior surface of the squamosal, on the occipital plate (again, Holliday, 2009, but also Gorniak, et al., 1982 and Haas, 1973), and that previous arguments for the mDM to originate on the opisthotic (often called the exoccipital, exoccipital/opisthotic, or merely “paroccipital”) in any fashion are erroneous — indeed, illustrations often peg the proximal tendon of the mDM as arising from the opisthotic, or the margin where the opisthotic meets the squamosal on the lateral surface of the skull. mDM should never be visible above the ventral end of the paroccipital process of the opisthotic/squamosal in lateral view, and despite reports of this in 2009 and even earlier, Sereno does not correct the proposed myology in 2010, instead reinforcing it in 2012. Perhaps there is confusion, coming from using a parrot skull to model the musculature, as parrots (as in most birds), the cranium is so large the squamosals have been moved largely to face laterally, and lose some of their expression on the occipital plate, which causes the mDM to originate laterally.

Sereno makes novel use of the ventral process of the jugal, a feature in Heterodontosaurus tucki, but similar to some features in hadrosaurids. Indeed, it is one of those odd features that once placed heterodontosaurids close to euornithopods, but no explanatory function has been satisfactory for the presence of a ventral circular emargination of the subtemporal bar (quadratojugal/jugal), especially when the posterior process of the jugal is so elongated and deep, but very, very thin and rather blade like. So Sereno’s use of it for Heterodontosauridae, and indeed for Psittacosaurus spp. is useful, but there the support ends. Several problems with this model call several aspects of the myology into question, but it raises a new possibility.

Is it Possible for Ornithischians to Have a Pseudomasseter-like Muscle?

This is no simple question. While parrots have this novel musculature, along with the m. ethmomandibularis (mEM), a muscle suite rostral to the typical adductor muscles (PT and AME complexes) also occurs in mammals, in which the muscle group m. masseter (mM) extends from the ventral zygomatic (jugal) to the lateral mandibular (dentary) bones. These muscles, divided into rostral and caudal segments, with deep and superficial layers, form the primary mandibular adductors, along with the m. temporalis (mT). Muscle homologies between sauropsidans (“reptiles”) and mammals is not of use here, merely functional novelties. And in this, the mM forms a correspondence with the mPsm of parrots, and thus a basis on which to form arguments about tissue structure parallel to the jaw, and lateral to the oral cavity in which food is processed. And that’s what we’re going for. But I’d really rather not answer this question; it is not that I do not think I can answer it (I do think I can, with the right examination, for instance looking at the bone structure microscopically to see if there are traces of entheses, where tendons and ligaments attach to bones, or through tracking nutrient and nerve foramina in these regions, which would be explained only through muscle innervation/nutriation), but that I think we need to heed [a variation of] Doyle’s famous aphorism: Eliminate the impossible, then we can uphold whatever it is we have left. (Yes, yes, that’s not what he actually says; I’m paraphrasing.) That is, if I cannot eliminate it, even if due to incomparability, then that becomes a functional hypothesis to run on. With paleo, of course, it is more difficult to eliminate all possibilities, so there will result many potential possibles from which to work with.

And it is this that I wish to build on. And I’ll do this with this: I’ve identified four functional modules that relate to ornithischian “cheeks”, which form a matrix of about 15 variations of “cheeked” ornithischians (the first is the “cheekless” model, which and some of you readers may be aware is the null hypothesis — that is, it is the model from which the others must be compared, and is the one that reflects the basic, “cheekless” state of virtually all other Sauropsida; all other models represent variations attempting to consider what features, reasonable to assume or found in living species, that produce “cheeks” that may be used by Ornithischia). These models of these four modules, each testable explicitly in some fashion, but potentially not against the preserved fossil record, will allow a more direct framework on which to discuss the evolution and likelihood of what, if anything, exists outside the buccal regions of ornithischian jaws.

But… I’m not going to do that now. Or even soon. I want to put this model through an actual analytical wringer. I am posting this now to drum up some dialog on the subject. I want to potentially publish this work, and rather than simply plug it out here — a tact I am going to be refraining from for a while — I am withholding my current thoughts to allow myself time to examine these models, potentially add to them, and work on what it is I need to do to test these models against the null. I would like to stress, however, that the cheekless model is the null: other models must overcome that, and what it can allow us to solve the problems of ornithischian mastication (such as the idea that food falls out without cheeks) … only after the null is disproven should these models be taken as more likely, more reasonable, more actual.

[n1] Not unlike many reactions to the loss of Pluto as a “true” planet, though I accepted that purely nomenclatural re-designation with a good deal of aplomb.
[n2] There is somewhat of an abundance of species, many considered valid, referred to the taxon Psittacosaurus. At current count, that’s mongoliensis (which includes as synonyms Protiguanodon mongoliense, and Psittacosaurus osborni, tingi, and guyangensis), sinensis (including youngi), xinjiangensis, meileyingensis, neimongoliensis, ordosensis, mazongshanensis, sibiricus, lujiatunensis, major, gobiensis; the species sattayaraki has been questioned for its extreme morphology and likely juvenility (which also sunk tingi and youngi). Various analyses have groups several of these into discrete arrangements, and there has been some push from paleontologists and lay persons alike to consider spliting these into discrete “genera.” The description of Psittacosaurus-like taxa such as Chaoyangsaurus youngi and Hongshanosaurus houi has conversely also suggested merely lumping these taxa in with other species referred to Psittacosaurus. Nonetheless, Psittacosaurus as a clade remains one of the most speciose taxa without subclades above the included species.

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Haas, G. 1973. Muscles of the jaws and associated structures in the Rhynchocephalia and Squamata. pp.285-490 in Gans & Parsons (eds.) Biology of the Reptilia, Vol 4. (Academic Press, New York & London.)
Hofer, H. 1950. Zur Morphologie der Kiefermuskulatur der Vögel [On the morphology of the jaw muscles of birds]. Zoologische Jahrbücher, Abteilung für Anatomie und Ontogenie der Tiere [Zoological Journal of the Department of Animal Anatomy and Ontogeny] 70:427–556.
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