In my last post on the issue of recovering the probable structure of extra-oral tissues in dinosaurs, bracketed as they are between crocs and birds, but with lacertilians and other reptiles outside of that grouping, I suggested that one important direction this research must take is that it must account for ornithischians. Specifically, I said that Larry Witmer was correct in his assumption that Leptoceratops gracilis likely had nothing “cheek-like” around its jaws. I attempt here to explain this in more detail.
First, tissues leave marks on bone, especially when they attach to said bone. Keratinous sheets lying close leave dense networks of nutrient grooves on bone, which is normally smooth; the tendons that link muscle to bone leave spiky bone surfaces in small, regular regions and generally in relief of the surrounding cortical surface, due to Sharpey’s fibers; bosses and cornified skin leave rough surfaces with dense foramina penetrating the bone; ligaments leave striae and raised lips with minute rough surfaces; and dental endothelium (or “gum”) leaves smooth bone without irregularities.
When it comes to discussing the option of whether any ornithischian dinosaur had a muscular or nonmuscular flap between upper and lower jaw, it must first be known what tissues were present in the jaw region. I will not speak with authority on this point, as I’ve not undertaken a direct examination of jaws of any variety of ornithischians by which I could say they LACK such markers on them, yet only that so far, no markers have been reported by systematists and paleontologists describing the skulls of dozens upon dozens of diverse hadrosaur, ceratopsian and ankylosaur or stegosaur jaw.
A histological or surficial map has yet to be made of any ornithischian jaw, or even to compare described regions among taxa, instead focusing research on ultrastructure and minute details of particular regions. What I’m covering next is instead partly mechanical and partly based on personal observation, based on what I’ve had the opportunity, with what my mere eyeball has had the opportunity to examine a variety of ornithischian skulls in person or in paper. I am leaving unpublished research out of this.
So, tissue distribution:
It was interesting to me to look for examples where a clear and distinct lamina or ridge exists that separates the lateral surface of the dentary into two faces: a ventrolateral face, and a buccal face. The surficial structure of the buccal face tends to be smooth, but bears large foramina; conversely, the ventrolateral face bears numerous nutrient grooves and appears with a rougher texture. Is this the boundary of a buccal cavity? I argue here that regardless of the presence of sessile, lacertilian-style oral tissues (model A) or a flap of skin (model B), the lateral margin of the tooth row and an extended region of the lateral surface further ventral would be covered in gum tissue, and thus this surface alone might not allow a covering “cheek” analogue. Problematically, not all ornithischians possess a distinct margin between these two faces, so that it may be inferred easily.
In Centrosaurus apertus (following Bell et al., 2009), the margins are distinct, and the faces demarcated by a clear ridge that crosses from the coronoid caudally to essentially merge with the lateral ridge of the predentary. This has other implications, but we won’t get into that here. In Edmontosaurus annectens, rather, the lateral margin of the dentary is more rounded, and the “faces” are far less distinct from one another: the jaw seems smooth all the way down (using Bell et al., 2009, who in turn used an indeterminate lambeosaurine mandible from the Dinosaur Park Formation, meaning it could be all sorts of things).
One thing I noticed (based now largely on discussions with others and thus not my own conclusions, but for which I don’t have a citation handy — if you have the cite, let me know!) is that the presence of a distinct separation of faces may be apparent only as an artifact of rotation of the mandibular ramus about its long axis:
In many ways, the depth of the buccal “cavity” is a product of the rotation of the mandible, and the ventral width relative to the dorsal. And in these taxa, the ventral margin may be thicker than the dorsal, causing rotation to “form” a “buccal ridge.” This ridge then becomes a feature that appears firstly out of rotation, secondly out of morphology (i.e., a lamina develops from an extension of a coronoid process, or caudally from the predentary region). Hadrosaurs, perhaps as a product of the extreme roundness of the lateral surface — nonetheless, bulging outwards — have the most vertical of mandibular rami shown here, followed by ceratopsians which have rotated the ramus lingually by about 15°; ankylosaurians have mandibular rami which are nearly 40° from the vertical, and consequently appear to have the deepest buccal cavity, but these appear to be a factor related not to actual osteological features but to the bone’s orientation. Perhaps a greater clue to the presence of buccal “depth” would be from the lateral margins of the jugal and maxilla, instead: in hadrosaurs, however, this creature is still rounded, and shallow, while in ceratopsians and ankylosaurs a distinct, sharp margin is produced and in the latter forms an overhanging shelf. Does this necessarily force a presence of “cheeks”? No. For certainly, these features also appear in lacertilians.
Jaw mechanics of ankylosaurids are limited. The skulls are akinetic, but apparently the mandibles are not (Vickaryous & Rybczynski, 2001), permitting flexibility for each mandibular ramus relative to the other, due to the open joint between each dentary and colateral cotylar sockets on the posterior predentary. This affords the ability of the jaws to engage in a complex array, despite restrictions due to the lingual curvature of the tooth row in all taxa.
One of the trickier issues, as I mentioned in the previous post on this topic, was that some ankylosaurians possess a bony plate lateral to the buccal cavity, a buccal plate, and that this has naturally caused some to suspect this plate affirms a fleshy “cheek” of some sort extended across the plate’s lingual surface. I question this for two reasons, barring any new data that will reveal that it can be accomodated:
1. The presence of an elastic structure of any sort or flexible region of skin lingual to the plate would only be effective around the margins of the plate, and cannot necessarily incorporate it. If it did, the plate would need to be weakly attached to the skin in this area to prevent distortion of the tissue around it. Plates in this region are also unintuitive to the function of the “cheek”: opening and closing would provide the flesh required flexibility, and it can be assumed that dermal plates should form in a region where the skin becomes stiff and requires either reinforcement, or are migrated to protect a point of weakness, but develop elsewhere.
2. “Cheeks” — as they were — are not needed for the ostensible role they are implied to be required for: retaining food within the oral cavity.
Depending on the elasticity of the mandibular tissues, the bolus in the jaw is largely contained. This model does not ensure that no loss of food during oral processing occurs, but this model does consider that virtually all volume of the bolus remains within the jaws. Moreover, the bulk of the material may dump into the floor of the mouth between mandibles. You will notice however that this is based on the absence of a tongue; I’ve not forgotten it, it is merely absent based on lack of data suggesting its size, shape, or possible extent. It should also be notable lizards can process food and often incur slippage out of the sides of the mouth, having nothing in the way of a “cheeky” tissue, yet manage to get along fine, so whether the actual — and likely low — volume of lost food is relevant remains to be seen. How efficient was the food stuffs of particular taxa for their environment, and how long they must feed, and how effective they are in processing those foods? These questions are generally pointed at sauropods; ornithischians less so.
Problematic with this model is in fact the issue of bolus retention, however, depending on the tensility of the extra-oral tissues, and their extent, this can be somewhat mitigated without having to involve novel tissues for which no direct evidence exists. The plate on the side of the jaw, and its suggestion of a full “cheek” is useful in helping resolve this, but not only has it not been preserved in many ankylosaurians, it has been preserved only in some nodosaurids, while not even the fantastic bony preservation of the Gobi Desert has permitted preservation in various Mongolian ankylosaurids and “shamosaurs”. Lack of preservation of a thing, of course, does not mean preservation of that thing’s lack.
Tracy Ford suggested an odd compromise:
Are both of these mechanisms possible? Yes, and certainly I think they are more likely than one in which a full fleshy “cheek” is present. There are, of course, possibilities (I say, waffling) that some ornithischians had developed a fleshy “cheek,” almost certainly one not comprised of muscle, while others did not. Ornithischia is a complex clade, and its backbone was a series of lineages all based on small, bipedal taxa with jaws full of teeth and no real distinct inset of the jaws that might even suggest a “cheek,” yet has produced three clades all convergent on the lingually-rotated mandibular ramus: thyreophorans, in which ankylosaurs (and especially ankylosaurids) have gone leagues beyond the condition seen in Scelidosaurus harrisonii or stegosaurians; ceratopsians; and iguanodontians. Yet desite this convergence, the relative buccal cavity to the oral cavity width doesn’t seem to have increased by much in a given lineage. While Coombs (1978) shows how Sauropelta edwardsorum had remarkably inset maxillary tooth rows, this inset variation hasn’t been strongly tested, and we are left wondering if the inset really did remain stable across Ornithischia when it becomes this inset. No matter; another thing for researchers to look into.
However, I would like to indicate that, as with a variety of herbivorous lizards, including those with relatively complex jaw movements but somewhat akinetic skulls (as with Uromastyx hardwickii; Throckmorton, 1978, Schwenk, 2000), many herbivorous ornithischian dinosaurs also appear to have akinetic or largely akinetic skulls and complexly mobile mandibles (Holliday & Witmer, 2008, but notably – hadrosaurids: Cuthbertson et al., 2012; ankylosaurids: Vickaryous & Rybczynski, 2001; and ceratopsians: Haas, 1955). If the lack of a “cheek” is no limit to the diverse but herbivorous diet of uromastyx lizards, it should be no issue for larger herbivores.
Here, I present four variable reconstructions of the head of Panoplosaurus mirus as it might appear in life, with sessile, lacertilian-style “lips;” a fleshy, boneless “cheek”; a fleshy “cheek” in which the bone plate has been placed and anchored to the mandible; and finally, following Tracy Ford’s idea, one in which the bony plate operates as an extension of the mandibular extra-oral tissues and not as part of a “cheek.” I leave it to the reader to consider which option is best, fitting sense or the data.
Bell, P. R., Snively, E. & Shychoski, L. 2009. A comparison of the jaw mechanics in hadrosaurid and ceratopsid dinosaurs using Finite Element Analysis. The Anatomical Record 292(9):1338-1351.
Coombs, W. P., Jr. 1978. The families of the ornithischian dinosaur order Ankylosauria. Palaeontology 21:143-170.
Cuthbertson, R. S., Tirabasso, A., Rybczynski, N. & Holmes, R. B. 2012. Kinetic limitations of intracranial joints in Brachylophosaurus canadensis and Edmontosaurus regalis (Dinosauria: Hadrosauridae), and their implications for the chewing mechanics of hadrosaurids. The Anatomical Record 295(6):968-979.
Haas, G. 1955. The jaw musculature in Protoceratops and in other ceratopsians. American Museum Novitates 1729:1-24. [PDF]
Holliday, C. M. & Witmer, L. M. 2008. Cranial kinesis in dinosaurs: Intracranial joints, protractor muscles, and their significance for cranial evolution and function in diapsids. Journal of Vertebrate Paleontology 28(4):1073-1088. [PDF]
Rybczynski, N. & Vickaryous, M. K. 2001. Evidence of complex jaw movement in the Late Cretaceous ankylosaurid Euoplocephalus tutus (Dinosauria: Thyreophora). pp.299-317 in Carpenter (ed.) The Armored Dinosaurs. (Indiana University Press, Bloomington & Indiana.)
Schwenk, K. 2000. Feeding in lepidosaurs. pp.175–291 in Schwenk (ed.) Feeding: Form, Function, and Evolution in Vertebrates. (Academic Press, New York.)
Throckmorton, G. S. 1976. Oral food processing in two herbivorous lizards, Iguana iguana (Iguanidae) and Uromastyx aegyptius (Agamidae). Journal of Morphology 148:363-390.
Witmer, L. M. & Ridgely, R. c. 2008. The paranasal air sinuses of predatory and armored dinosaurs (Archosauria: Theropoda and Ankylosauria) and their contribution to cephalic structure. The Anatomical Record 291(11):1362-1388. [PDF]