Casey M. Holliday

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Vertebrate Functional Morphology & Evolution

 

Cranial kinesis in dinosaurs: intracranial joints, protractor muscles, and their significance for cranial evolution in diapsids.

C. M. Holliday and L. M. Witmer. 2008. Journal of Vertebrate Paleontology 28(4):1073-1088.

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Determining whether or not the skulls of dinosaurs and other reptiles possess grossly movable joints within their skulls (aka cranial kinesis) is major challenge to functional and evolutionary morphologists. For over one hundred years, paleontologists have relied on particular joint morphologies to drive their hypotheses of feeding function and cranial evolution. However, these joint morphologies found in dinosaurs are often present in extant taxa that do not show cranial kinesis, a phenomenon that casts doubt on the ability of researchers to clearly interpret joint function in extinct species. This paper reviewed the evidence supporting inferences of cranial kinesis in dinosaurs including the presence of synovial otic and basal joints, protractor muscles, and permissive kinematic linkages.

Whereas almost all dinosaurs possessed synovial joints and protractor muscles, only a few derived taxa exhibit a breakdown of bony linkages that would facilitate gross intracranial movements. This distribution indicates the structures necessary for cranial kinesis are plesiomorphic for dinosaurs, if not also diapsids as a whole. However, even though an taxon may possess these necessary structures, these features are not necessarily sufficient for positive inferences of kinesis in extinct animals.

The distribution of cranial features also suggests that, because their theropod relatives also possessed protractor muscles and synovial joints, birds exapted these features, to develop the intricate form of cranial kinesis they display.

 

Funded by: National Science Foundation: IBN-0407735, IBN-9601174, IOB-0343744; Contract grant sponsors: The Jurassic Foundation; UCMP Sam Welles Fund; Society of Vertebrate Paleontology; OU Student Enhancement Award; OU Graduate Student Senate; OU Departments of Biological and Biomedical Sciences; Marshall University.

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Figure 1. Major structures associated with cranial kinesis in diapsids. A, schematic of a generalized archosaur indicating hypothesized mobile intracranial joints; B, inset of the skull of the basal sauropod dinosaur Massospondylus carinatus (BP/1/4779) based on CT data, denoting the plane of section in C in left lateral view; C, caudal view of a section through the skull at the plane indicated in B, illustrating the synovial basal and otic joints, as well as other relevant anatomical structures.

Figure 2. Osteological correlates of synovial joints in extant diapsids. Dotted lines indicate the extent of the articular cartilage and fibrous capsule. A, braincase of Iguana iguana, in left lateral view; B, close-up of the basipterygoid process from inset in A, showing the braincase portion of the basal joint; C, left quadrate of I. iguana in left lateral view; D, otic process of the left quadrate of I. iguana in left dorsal oblique view; E, quadrate of Alligator mississippiensis in left lateral view; F, close-up of  the otic process of alligator quadrate from inset in E, showing the quadrate portion of the otic joint; G, A, mississippiensis adductor chamber in left ventrolateral view; H, close-up of the laterosphenoid-postorbital joint from inset in G.

Figure 3. Osteological correlates of synovial joints in fossil dinosaurs. Dotted lines indicate the extent of the articular cartilage and fibrous capsule. A, quadrate of Allosaurus fragilis (UMNH VP 18054 [UUVP 4642]) in left lateral view; B, close-up of the otic process of quadrate from inset in A, showing the quadrate portion of the otic joint; C, close-up of the articular process of the quadrate from inset in A; D, skull of Brachylophosaurus canadensis (MOR 1071) in left lateral view; E, close-up of the otic process of quadrate from inset in D, showing the quadrate portion of the otic joint; F, close-up of the articular process of the quadrate from inset in D; G, braincase of A. fragilis (CM 21703) in left lateral view; H, close-up of the basipterygoid process from inset in G in left lateral view, showing the braincase portion of the basal joint; I, braincase of Edmontosaurus regalis (CMN 2289) in left lateral view; J, close-up of  the basipterygoid process from inset in I in left ventral view, showing the braincase portion of the basal joint.

Figure 4. Synovial basal joints are widespread among diapsids, as shown by axial (coronal) sections through the orbitotemporal regions of lepidosaurs and dinosaurs. A, Sphenodon punctatus; B, Ctenosaura pectinata; C, Varanus gouldi; D, Heloderma suspectum; E, Python molurus; F, Dryosaurus altus (CM 3392); G, Psittacosaurus mongoliensis (IGM 100/1132); H, Camarasaurus lentus (CM 11338); I, Tyrannosaurus rex (FMNH PR2081); J, Struthio camelus. BE adapted from data from www.digimorph.org.

Figure 5. Basal joint in Diplodocus longus (CM 3452), based on CT data. A, skull in left lateral view depicting location of section; B, caudal view of a section at the plane indicated in A, illustrating the elongated basipterygoid process and synovial basal joint.

Figure 6. Basal joints in ceratopsians. A, skull of Psittacosaurus mongoliensis (IGM 100/1132) in left lateral view based on CT data, depicting the location of the avail (coronal) section in C; B, skull in dorsal view depicting the location of the parasagittal section in D; C, rostral view of a section through orbitotemporal region at the plane indicated in A, illustrating the synovial basal joints; D, parasagittal section of skull in right lateral view at the plane indicated in B, illustrating a medial view of the left basal joint; E, skull of Triceratops horridus in ventral view illustrating its unconstrained basal joints (modified from Hatcher et al., 1907).

Figure 7. Basal joint in Panoplosaurus mirus (ROM 1215). A, skull in left lateral view based on CT data; B, skull in caudoventral view illustrating the basal joints; C, skull in dorsal view depicting the location of the oblique parasagittal section in D; D, left, caudolateral view of the oblique parasagittal section at the plane indicated in C, illustrating the synovial basal joint.

Figure 8. Otic joints in the sauropod Camarasaurus lentus (CM 11338). A, skull based on CT data in left lateral view illustrating the otic (quadratosquamosal) joint and the location of the section in B; B, caudal view of the section at the plane indicated in A, illustrating the otic joints.

Figure 9. Evolutionary history of the morphological correlates of cranial kinesis in amniotes with special emphasis on dinosaurs. Nodes: 1, Tetrapoda; 2, Amniota; 3, Sauropsida; 4, Lepidosauria; 5, Squamata; 6, Archosauria; 7, Dinosauria; 8, Ornithischia; 9, Saurischia 10, Theropoda; 11, Maniraptora.

Figure 10. Braincases of dinosaurs in left lateral view illustrating thw osteological correlates of the levator and protractor pterygoideus muscles and other relevant structures in the adductor chambers. A, Triceratops horridus (MOR 699); B, Brachylophosaurus canadensis (MOR 1071); C, Tyrannosaurus rex (AMNH 5117).

Figure 11. The protractor and levator pterygoideus muscles of Triceratops horridus (AD), Brachylophosaurus canadensis (EH), and Tyrannosaurus rex (IL) illustrating the muscle attachments and generalized angulations. Far left (A, E, I), braincase and palate (translucent) with musculature in left lateral view; Far right (B, F, L), orbitotemporal region in left axial (coronal) section illustrating relevant anatomical structures; left middle (C, G, J), right middle (D, H, K), schematics of general angulations of different bellies of the left-side levator and protractor pterygoideus muscles in lateral and caudal views, respectively. Cylinder, basipterygoid process; grey arrows, mLPt; black arrows, mPPt. Figure 12. Evolution and breakdown of kinematic linkages in the palates in diapsids, using schematic images of elements in left lateral view. A, basal archosaur condition; B, evolution of the avian condition; C, the epipterygoid was eliminated in several archosaur and dinosaur lineages but overlapping scarf joints were not; D, evolution of the palate among lepidosaurs.
 

Figure 13. Skull roof diversity among lepidosaurs and dinosaurs illustrating the position of flexible hinge joints in extant taxa. Nonavian dinosaurs do not possess the cranial architecture and kinematic linkages permitting kinesis. A, Sphenodon punctatus; B, Iguana iguana (an iguanian); C, Gymnophthalmus sp. (a derived scleroglossan); D, Edmontosaurus regalis; E, Camarasaurus lentus; F, Majungasaurus crenatissimus; G, Gorgosaurus libratus; H, Troodon formosus; I, Shuvuuia deserti; J, Eudromia elegans.