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):
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.
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.
Gorniak, G. C., Rosenberg, H. I. & Gans, C. 1982. Mastication in the tuatara, Sphenodon punctatus (Reptilia: Rhynchocephalia): Structure and activity of the motor system. Journal of Morphology 171:321-353.
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.
Holliday, C. 2009. New insights into dinosaur jaw muscle anatomy. The Anatomical Record 292:1246-1265.
Sereno, P. C. 2012. Taxonomy, morphology, masticatory function and phylogeny of heterodontosaurid dinosaurs. Zookeys 226:1-225.
Sereno, P. C., Zhao X.-j. & Tan L. 2010. A new psittacosaur from Inner Mongolia and the parrot-like structure and function of the psittacosaur skull. Proceedings of the Royal Society of London, B: Biological Sciences 277:199-209.
Tokita, M. 2004. Morphogenesis of parrot jaw muscles: Understanding the development of an evolutionary novelty. Journal of Morphology 259:69-81.
Zusi, R. L. 1993. Patterns of diversity in the avian skull. pp.391-437 in Hanken & Hall (eds.) The Skull: Patterns of Structural and Systematic Diversity, Vol. 2. (University of Chicago Press, Chicago.)
Very interesting post –some of these ideas came to me also, as I whizzed through Sereno (2012). A few thoughts on this:
(1) as you say, close examination of the bone surfaces would be necessary to confirm muscle attachment sites. On the images provided in Sereno et al (2010) and Sereno (2012), the ventral surface of the maxillary/premaxillary ridge looks more convincing as a muscle origin in Heterodontosaurus than in Psittacosaurus.
(2) if there are muscles in these positions, the names are not good, the parrot connection is superficially attractive but the muscles don’t conform: m. adductor mandibulae externus ventralis is a particular avian muscle, arises as a tendon from the zygomatic process of the squamosal, passes medial to the inferior temporal arch, and fans out onto the mandible. The muscle labelled amev in these two reconstructions does none of this except insert on the mandible. M. pseudomasseter of parrots is also very specific, it develops as a superficial bundle of the external adductor, arises from an ossification ventral to the orbit but separate from the inferior arch, and passes lateral to the arch (Tokita 2004), again not like the muscles labelled.
(3) there is a problem with putting ‘cheek’ adductors in Heterodontosaurus: the large caniniform teeth imply wide jaw opening, as in eutherian and marsupial carnivores. Jaw adductors need to have placement and length sufficient to allow this wide opening, muscles in the ‘cheek’ position are likely to be too short. Mammalian carnivores with big canines have a dorsally curved zygomatic arch to accommodate sufficient fibre length.
(4) in the Psittacosaurus reconstruction, the insertion of ‘pseudomasseter’ medial to ‘amev’ is a bit unlikely: the most superficial parts of the external adductor in sauropsids usually insert as a continuous line on the mandible, like in the parrot in the figure in your post.
(5) turtles also have rhamphothecae, and, interestingly, trionychids have a portion of the external adductor arising from the ventral edge of the jugal, usually named m. zygomaticomandibularis (Werneburg 2011); another bad name, attributed from mammalian anatomy. Although turtles are obviously difficult in their uncertain placement relative to archosaurs, this might have made a better model for a possible superficial muscle from infraorbital region to mandible, even if just analogy and more similar skull shape.
Good luck with your deeper analysis.
Ref: Werneburg, I 2011 The cranial muscles of turtles. Palaeontologia Electronica 14/2: 15A
(Other refs as in your post)
Thanks for the response and kick in the back [I mean this last bit positively!]. I keep forgetting about turtles *grumble* so they tend to pass unremarked far more than they should!
I keep thinking about this: in light of the (as yet unpublished) article coming out of SVP2012 on the subject of postmortem bite marks on Triceratops faces, can we draw any conclusions on “cheek” presence or absence based on the presence/absence of Tyrannosaur bite marks in that region of the skull? I know we should probably wait for the paper but, from the preliminary news coverage: “Scratches on the front of the skull suggest T. rex nibbled nostril-region flesh from the bone. But otherwise the front of a Triceratops offered slim pickings” -Jeff Hecht in this week’s New Scientist. Is it safe to say that, whatever fleshy structures Triceratops had in the buccal region, they weren’t as fleshy as his nostrils? Admittedly this still leaves room for really bad-tasting “cheeks”.
I would also have to wait for the paper. One way to attest where soft-tissues were being pulled from the skull is to check for scratch marks, but this doesn’t necessarily mean there were no non-muscular “cheeks” present in larger ceratopsians. It just may mean that the nostril region — which is huge and probably filled with dense vascular tissue — was MUCH more enticing. An animal may have tried to pry open the jaws of the corpse or produce scratching marks as it maneuvered around the jaw to get at the hyoid muscles and tongue, which would certainly also have been very substantial and nutritious, and that might produce marks around the jaw margins that might otherwise also indicate “cheeks.” I eagerly await Fowler et al’s work as well.
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