Casey M. Holliday

New Insights Into Dinosaur Jaw Muscle Anatomy

Jaw muscles are key components of the head and critical to testing hypotheses of soft‐tissue homology, skull function, and evolution. Dinosaurs evolved an extraordinary diversity of cranial forms adapted to a variety of feeding behaviors. However, disparate evolutionary transformations in head shape and function among dinosaurs and their living relatives, birds and crocodylians, impair straightforward reconstructions of muscles, and other important cephalic soft tissues. This study presents the osteological correlates and inferred soft tissue anatomy of the jaw muscles and relevant neurovasculature in the temporal region of the dinosaur head. Hypotheses of jaw muscle homology were tested across a broad range archosaur and sauropsid taxa to more accurately infer muscle attachments in the adductor chambers of non‐avian dinosaurs. Many dinosaurs likely possessed m. levator pterygoideus, a trait shared with lepidosaurs but not extant archosaurs. Several major clades of dinosaurs (e.g., Ornithopoda, Ceratopsidae, Sauropoda) eliminated the epipterygoid, thus impacting interpretations of m. pseudotemporalis profundus. M. pseudotemporalis superficialis most likely attached to the caudoventral surface of the laterosphenoid, a trait shared with extant archosaurs. Although mm. adductor mandibulae externus profundus and medialis likely attached to the caudal half of the dorsotemporal fossa and coronoid process, clear osteological correlates separating the individual bellies are rare. Most dinosaur clades possess osteological correlates indicative of a pterygoideus ventralis muscle that attaches to the lateral surface of the mandible, although the muscle may have extended as far as the jugal in some taxa (e.g., hadrosaurs, tyrannosaurs). The cranial and mandibular attachments of mm adductor mandibulae externus superficialis and adductor mandibulae posterior were consistent across all taxa studied. These new data greatly increase the interpretive resolution of head anatomy in dinosaurs and provide the anatomical foundation necessary for future analyses of skull function and evolution in an important vertebrate clade. Anat Rec, 292:1246–1265, 2009.

Diffusible iodine-based contrast-enhanced computed tomography (diceCT) : an emerging tool for rapid, high-resolution, 3-D imaging of metazoan soft tissues.

Morphologists have historically had to rely on destructive procedures to visualize the three‐dimensional (3‐D) anatomy of animals. More recently, however, non‐destructive techniques have come to the forefront. These include X‐ray computed tomography (CT), which has been used most commonly to examine the mineralized, hard‐tissue anatomy of living and fossil metazoans. One relatively new and potentially transformative aspect of current CT‐based research is the use of chemical agents to render visible, and differentiate between, soft‐tissue structures in X‐ray images. Specifically, iodine has emerged as one of the most widely used of these contrast agents among animal morphologists due to its ease of handling, cost effectiveness, and differential affinities for major types of soft tissues. The rapid adoption of iodine‐based contrast agents has resulted in a proliferation of distinct specimen preparations and scanning parameter choices, as well as an increasing variety of imaging hardware and software preferences. Here we provide a critical review of the recent contributions to iodine‐based, contrast‐enhanced CT research to enable researchers just beginning to employ contrast enhancement to make sense of this complex new landscape of methodologies. We provide a detailed summary of recent case studies, assess factors that govern success at each step of the specimen storage, preparation, and imaging processes, and make recommendations for standardizing both techniques and reporting practices. Finally, we discuss potential cutting‐edge applications of diffusible iodine‐based contrast‐enhanced computed tomography (diceCT) and the issues that must still be overcome to facilitate the broader adoption of diceCT going forward.

Cartilaginous epiphyses in extant archosaurs and their implications for reconstructing limb function in dinosaurs.

Extinct archosaurs, including many non-avian dinosaurs, exhibit relatively simply shaped condylar regions in their appendicular bones, suggesting potentially large amounts of unpreserved epiphyseal (articular) cartilage. This “lost anatomy” is often underappreciated such that the ends of bones are typically considered to be the joint surfaces, potentially having a major impact on functional interpretation. Extant alligators and birds were used to establish an objective basis for inferences about cartilaginous articular structures in such extinct archosaur clades as non-avian dinosaurs. Limb elements of alligators, ostriches, and other birds were dissected, disarticulated, and defleshed. Lengths and condylar shapes of elements with intact epiphyses were measured. Limbs were subsequently completely skeletonized and the measurements repeated. Removal of cartilaginous condylar regions resulted in statistically significant changes in element length and condylar breadth. Moreover, there was marked loss of those cartilaginous structures responsible for joint architecture and congruence. Compared to alligators, birds showed less dramatic, but still significant changes. Condylar morphologies of dinosaur limb bones suggest that most non-coelurosaurian clades possessed large cartilaginous epiphyses that relied on the maintenance of vascular channels that are otherwise eliminated early in ontogeny in smaller-bodied tetrapods. A sensitivity analysis using cartilage correction factors (CCFs) obtained from extant taxa indicates that whereas the presence of cartilaginous epiphyses only moderately increases estimates of dinosaur height and speed, it has important implications for our ability to infer joint morphology, posture, and the complicated functional movements in the limbs of many extinct archosaurs. Evidence suggests that the sizes of sauropod epiphyseal cartilages surpassed those of alligators, which account for at least 10% of hindlimb length. These data suggest that large cartilaginous epiphyses were widely distributed among non-avian archosaurs and must be considered when making inferences about locomotor functional morphology in fossil taxa.

The epipterygoid of crocodyliforms and its significance for the evolution of the orbitotemporal region of eusuchians

ABSTRACT A broad survey of crocodyliform archosaurs and their outgroups was conducted to explore the evolutionary and morphological patterns of the orbitotemporal region, which is a highly apomorphic but poorly understood portion of the head. Data were gathered on the topological similarity and phylogenetic congruence of the epipterygoid, laterosphenoid, and temporal region as a whole, including relevant osteological correlates and such inferred soft tissues as the trigeminal nerves and jaw musculature. Despite the complete suturing of the palatocranial junction, the epipterygoid remained a consistent cranial element throughout crocodyliform evolution, only to be replaced by the topologically analogous, but developmentally neomorphic lateral bridge of the laterosphenoid during the early evolution of eusuchians. These changes led to a unique morphology of the region surrounding the exit of the trigeminal nerve. Mesoeucrocodylian taxa exhibit a diversity of epipterygoid morphologies including waisted (e.g., Araripesuchus), overlapping (e.g., Sarcosuchus), and isolated (e.g., Goniopholis, Leidyosuchus) forms. The isolated form, in which the epipterygoid is uncoupled from the pterygoid and does not to cover the cavum epiptericum laterally, represents a key transition to the extant condition of loss of the epipterygoid. Changes in the epipterygoid coincide with the migration of M. pseudotemporalis superficialis onto the laterosphenoid outside of the dorsotemporal fossa and the topological change in the intermuscular path of the maxillary nerve, both of which are apomorphies found in extant crocodylians. These data reflect a diverse and potentially homoplastic distribution of orbitotemporal morphologies among mesoeucrocodylians and indicate that the epipterygoid was only recently eliminated in crocodyliform evolution.

Cranial biomechanics of Diplodocus (Dinosauria, Sauropoda): testing hypotheses of feeding behaviour in an extinct megaherbivore

Sauropod dinosaurs were the largest terrestrial herbivores and pushed at the limits of vertebrate biomechanics and physiology. Sauropods exhibit high craniodental diversity in ecosystems where numerous species co-existed, leading to the hypothesis that this biodiversity is linked to niche subdivision driven by ecological specialisation. Here, we quantitatively investigate feeding behaviour hypotheses for the iconic sauropod Diplodocus. Biomechanical modelling, using finite element analysis, was used to examine the performance of the Diplodocus skull. Three feeding behaviours were modelled: muscle-driven static biting, branch stripping and bark stripping. The skull was found to be ‘over engineered’ for static biting, overall experiencing low stress with only the dentition enduring high stress. When branch stripping, the skull, similarly, is under low stress, with little appreciable difference between those models. When simulated for bark stripping, the skull experiences far greater stresses, especially in the teeth and at the jaw joint. Therefore, we refute the bark-stripping hypothesis, while the hypotheses of branch stripping and/or precision biting are both consistent with our findings, showing that branch stripping is a biomechanically plausible feeding behaviour for diplodocids. Interestingly, in all simulations, peak stress is observed in the premaxillary–maxillary ‘lateral plates’, supporting the hypothesis that these structures evolved to dissipate stress induced while feeding. These results lead us to conclude that the aberrant craniodental form of Diplodocus was adapted for food procurement rather than resisting high bite forces.

Free body analysis, beam mechanics, and finite element modeling of the mandible of Alligator mississippiensis

The mechanical behavior of mammalian mandibles is well‐studied, but a comprehensive biomechanical analysis (incorporating detailed muscle architecture, accurate material properties, and three‐dimensional mechanical behavior) of an extant archosaur mandible has never been carried out. This makes it unclear how closely models of extant and extinct archosaur mandibles reflect reality and prevents comparisons of structure–function relationships in mammalian and archosaur mandibles. We tested hypotheses regarding the mechanical behavior of the mandible of Alligator mississippiensis by analyzing reaction forces and bending, shear, and torsional stress regimes in six models of varying complexity. Models included free body analysis using basic lever arm mechanics, 2D and 3D beam models, and three high‐resolution finite element models of the Alligator mandible, incorporating, respectively, isotropic bone without sutures, anisotropic bone with sutures, and anisotropic bone with sutures and contact between the mandible and the pterygoid flange. Compared with the beam models, the Alligator finite element models exhibited less spatial variability in dorsoventral bending and sagittal shear stress, as well as lower peak values for these stresses, suggesting that Alligator mandibular morphology is in part designed to reduce these stresses during biting. However, the Alligator models exhibited greater variability in the distribution of mediolateral and torsional stresses than the beam models. Incorporating anisotropic bone material properties and sutures into the model reduced dorsoventral and torsional stresses within the mandible, but led to elevated mediolateral stresses. These mediolateral stresses were mitigated by the addition of a pterygoid‐mandibular contact, suggesting important contributions from, and trade‐offs between, material properties and external constraints in Alligator mandible design. Our results suggest that beam modeling does not accurately represent the mechanical behavior of the Alligator mandible, including important performance metrics such as magnitude and orientation of reaction forces, and mediolateral bending and torsional stress distributions. J.Morphol. 2011.

A 3D interactive model and atlas of the jaw musculature of Alligator mississippiensis.

Modern imaging and dissemination methods enable morphologists to share complex, three-dimensional (3D) data in ways not previously possible. Here we present a 3D interactive model of the jaw musculature of the American Alligator (Alligator mississippiensis). Alligator and crocodylian jaw musculature is notoriously challenging to inspect and interpret because of the derived nature of the feeding apparatus. Using Iodine-contrast enhanced microCT imaging, a segmented model of jaw muscles, trigeminal nerve, brain and skull are presented as a cross-sectional atlas and 3D, interactive pdf of the rendered model. Modern 3D dissemination methods like this 3D Alligator hold great potential for morphologists to share anatomical information to scientists, educators, and the public in an easily downloadable format.

The impact of bone and suture material properties on mandibular function in Alligator mississippiensis: testing theoretical phenotypes with finite element analysis.

The functional effects of bone and suture stiffness were considered here using finite element models representing three different theoretical phenotypes of an Alligator mississippiensis mandible. The models were loaded using force estimates derived from muscle architecture in dissected specimens, constrained at the 18th and 19th teeth in the upper jaw and 19th tooth of the lower jaw, as well as at the quadrate‐articular joint. Stiffness was varied systematically in each theoretical phenotype. The three theoretical phenotypes included: (i) linear elastic isotropic bone of varying stiffness and no sutures; (ii) linear elastic orthotropic bone of varying stiffness with no sutures; and (iii) linear elastic isotropic bone of a constant stiffness with varying suture stiffness. Variation in the isotropic material properties of bone primarily resulted in changes in the magnitude of principal strain. By comparison, variation in the orthotropic material properties of bone and isotropic material properties of sutures resulted in: a greater number of bricks becoming either more compressive or more tensile, changing between being either dominantly compressive or tensile, and having larger changes in the orientation of maximum principal strain. These data indicate that variation in these model properties resulted in changes to the strain regime of the model, highlighting the importance of using biologically verified material properties when modeling vertebrate bones. When bones were compared within each set, the response of each to changing material properties varied. In two of the 12 bones in the mandible, varied material properties within sutures resulted in a decrease in the magnitude of principal strain in bricks adjacent to the bone/suture interface and decreases in stored elastic energy. The varied response of the mandibular bones to changes in suture stiffness highlights the importance of defining the appropriate functional unit when addressing relationships of performance and morphology.

Ontogeny of the Alligator Cartilago Transiliens and Its Significance for Sauropsid Jaw Muscle Evolution

The cartilago transiliens is a fibrocartilaginous structure within the jaw muscles of crocodylians. The cartilago transiliens slides between the pterygoid buttress and coronoid region of the lower jaw and connects two muscles historically identified as m. pseudotemporalis superficialis and m. intramandibularis. However, the position of cartilago transiliens, and its anatomical similarities to tendon organs suggest the structure may be a sesamoid linking a single muscle. Incompressible sesamoids often form inside tendons that wrap around bone. However, such structures rarely ossify in reptiles and have thus far received scant attention. We tested the hypothesis that the cartilago transiliens is a sesamoid developed within in one muscle by investigating its structure in an ontogenetic series of Alligator mississippiensis using dissection, 3D imaging, and polarizing and standard light microscopy. In all animals studied, the cartilago transiliens receives collagen fibers and tendon insertions from its two main muscular attachments. However, whereas collagen fibers were continuous within the cartilaginous nodule of younger animals, such continuity decreased in older animals, where the fibrocartilaginous core grew to displace the fibrous region. Whereas several neighboring muscles attached to the fibrous capsule in older individuals, only two muscles had significant contributions to the structure in young animals. Our results indicate that the cartilago transiliens is likely a sesamoid formed within a single muscle (i.e., m. pseudotemporalis superficialis) as it wraps around the pterygoid buttress. This tendon organ is ubiquitous among fossil crocodyliforms indicating it is a relatively ancient, conserved structure associated with the development of the large pterygoid flanges in this clade. Finally, these findings indicate that similar tendon organs exist among potentially homologous muscle groups in birds and turtles, thus impacting inferences of jaw muscle homology and evolution in sauropsids in general.

A new eusuchian crocodyliform with novel cranial integument and its significance for the origin and evolution of Crocodylia.

Crocodyliforms were one of the most successful groups of Mesozoic tetrapods, radiating into terrestrial, semiaquatic and marine environments, while occupying numerous trophic niches, including carnivorous, insectivorous, herbivorous, and piscivorous species. Among these taxa were the enigmatic, poorly represented flat-headed crocodyliforms from the late Cretaceous of northern Africa. Here we report a new, giant crocodyliform from the early Late Cretaceous (Cenomanian) Kem Kem Formation of Morocco. Represented by a partial braincase, the taxon has an extremely long, flat skull with large jaw and craniocervical muscles. The skull roof is ridged and ornamented with a broad, rough boss surrounded by significant vascular impressions, likely forming an integumentary structure unique among crocodyliforms. Size estimates using endocranial volume indicate the specimen was very large. The taxon possesses robust laterosphenoids with laterally oriented capitate processes and isolated epipterygoids, features allying it with derived eusuchians. Phylogenetic analysis finds the taxon to be a derived eusuchian and sister taxon to Aegyptosuchus, a poorly understood, early Late Cretaceous taxon from the Bahariya formation. This clade forms the sister clade of crown-group Crocodylia, making these taxa the earliest eusuchian crocodyliforms known from Africa. These results shift phylogenetic and biogeographical hypotheses on the origin of modern crocodylians towards the circum-Tethyean region and provide important new data on eusuchian morphology and evolution.