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.

The extinct nonavian dinosaur Tyrannosaurus rex, considered one of the hardest biting animals ever, is often hypothesized to have exhibited cranial kinesis, or, mobility of cranial joints relative to the braincase. Cranial kinesis in T. rex is a biomechanical paradox in that forcefully biting tetrapods usually possess rigid skulls instead of skulls with movable joints. We tested the biomechanical performance of a tyrannosaur skull using a series of static positions mimicking possible excursions of the palate to evaluate Postural Kinetic Competency in Tyrannosaurus. A functional extant phylogenetic bracket was employed using taxa, which exhibit measurable palatal excursions: Psittacus erithacus (fore–aft movement) and Gekko gecko (mediolateral movement). Static finite element models of Psittacus, Gekko, and Tyrannosaurus were constructed and tested with different palatal postures using anatomically informed material properties, loaded with muscle forces derived from dissection, phylogenetic bracketing, and a sensitivity analysis of muscle architecture and tested in orthal biting simulations using element strain as a proxy for model performance. Extant species models showed lower strains in naturally occurring postures compared to alternatives. We found that fore–aft and neutral models of Tyrannosaurus experienced lower overall strains than mediolaterally shifted models. Protractor muscles dampened palatal strains, while occipital constraints increased strains about palatocranial joints compared to jaw joint constraints. These loading behaviors suggest that even small excursions can strain elements beyond structural failure. Thus, these postural tests of kinesis, along with the robusticity of other cranial features, suggest that the skull of Tyrannosaurus was functionally akinetic. Anat Rec, 303:999–1017, 2020. © 2019 Wiley Periodicals, Inc.

Numerous vertebrates exhibit cranial kinesis, or movement between bones of the skull and mandible other than at the jaw joint. Many kinetic species possess a particular suite of features to accomplish this movement, including flexible cranial joints and protractor musculature. Whereas the musculoskeletal anatomy of these kinetic systems is well understood, how these joints are biomechanically loaded, how different soft tissues affect joint loading and kinetic capacity, and how the protractor musculature loads the skull remain poorly understood. Here, we present a finite element model of the savannah monitor, Varanus exanthematicus, a modestly kinetic lizard, to better elucidate the roles of soft tissue in mobile joints and protractor musculature in cranial loading. We describe the 3D resultants of jaw muscles and the histology of palatobasal, otic and jaw joints. We tested the effects of joint tissue type, bite point and muscle load to evaluate the biomechanical role of muscles on the palate and braincase. We found that the jaw muscles have significant mediolateral components that can impart stability across palatocranial joints. Articular tissues affect the magnitude of strains experienced around the palatobasal and otic joints. Without protractor muscle loading, the palate, quadrate and braincase experience higher strains, suggesting this muscle helps insulate the braincase and palatoquadrate from high loads. We found that the cross-sectional properties of the bones of V. exanthematicus are well suited for performing under torsional loads. These findings suggest that torsional loading regimes may have played a more important role in the evolution of cranial kinesis in lepidosaurs than previously appreciated.

Comparing patterns of performance and kinematics across behavior, development and phylogeny is crucial to understand the evolution of complex musculoskeletal systems such as the feeding apparatus. However, conveying 3D spatial data of muscle orientation throughout a feeding cycle, ontogenetic pathway or phylogenetic lineage is essential to understanding the function and evolution of the skull in vertebrates. Here, we detail the use of ternary plots for displaying and comparing the 3D orientation of muscle data. First, we illustrate changes in 3D jaw muscle resultants during jaw closing taxa the American alligator (Alligator mississippiensis). Second, we show changes in 3D muscle resultants of jaw muscles across an ontogenetic series of alligators. Third, we compare 3D resultants of jaw muscles of avian-line dinosaurs, including extant (Struthio camelus, Gallus gallus, Psittacus erithacus) and extinct (Tyrannosaurus rex) species to outline the reorganization of jaw muscles that occurred along the line to modern birds. Finally, we compare 3D resultants of jaw muscles of the hard-biting species in our sample (A. mississippiensis, T. rex, P. erithacus) to illustrate how disparate jaw muscle resultants are employed in convergent behaviors in archosaurs. Our findings show that these visualizations of 3D components of jaw muscles are immensely helpful towards identifying patterns of cranial performance, growth and diversity. These tools will prove useful for testing other hypotheses in functional morphology, comparative biomechanics, ecomorphology and organismal evolution.

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For many animals, touch is one of the most crucial senses, as it allows an animal to assess its surroundings, develop properly, and socialize. Remote touch is an essential part of avian survival, as it allows some families of birds to identify prey through changes in pressure. Some birds possess a sensitive bill tip organ filled with a large number of mechanoreceptors to perform remote touch sensation. This implies that they possess a complex trigeminal nerve system. The trigeminal nerve has three divisions (ophthalmic, V1; maxillary, V2; and mandibular, V3) that supply somatosensory information from the face and head. Birds from the families Apterygidae, Scolopacidae, Anatidae, Threskiornithidae, and Psittacidae are known to have a sensitive bill tip organ supplied by the trigeminal nerve, whereas other birds use vision, hearing, and other touch to identify prey, potentially resulting in less overall dependence on the trigeminal nerve. Here, we created nerve maps of birds from a range of orders including Anseriformes, Gruiformes, Pelecaniformes, Strigiformes, Accipitriformes, and Passeriformes. We find that species with a remote touch organ possess more observable nerve fiber bundles associated with the maxillary and mandibular trigeminal nerve divisions than species not possessing a remote touch organ. Our results indicate that birds with foraging or prey capture techniques not relying on mechanoreception through the bill possess maxillary and mandibular divisions of the trigeminal nerve that are less robust as they enter the beak.

Feeding is a complex behavior that all tetrapods engage in on a regular basis to procure energy and survive. The reptilian feeding apparatus includes many types of feeding behaviors including multiple methods of engaging cranial kinesis, the ability to move one portion of the skull in relation to another portion of the skull. Understanding the underlying mechanisms of cranial kinesis enabled feeding mechanism is integral to understanding avian feeding behaviors, strategies, and ecology. Chapter 1 introduces how the feeding apparatus of reptiles is modified during the evolution of birds from dinosaur and reptile relatives. During this introductory chapter I lay the foundation for our knowledge of avian feeding and its evolution and describe the musculoskeletal environment of the avian feeding apparatus, which becomes the main focus of the rest of this project. Chapter 2 explores the diversity of jaw muscle resultants across a sample of birds, dinosaurs and other reptiles using ternary plots. Jaw musculature orientations are altered across ontogeny, behavior, and evolution. I use ternary plots to investigate the diversity of jaw muscle orientations across the ontogeny and feeding behaviors of alligators and through evolution in the dinosaur to bird lineage. Additionally, I use ternary plots to show how diverse organisms use different muscles to produce high bite forces. Chapter 3 introduces and demonstrates the use of postural modeling to investigate the feeding apparatus at a specific instant of a feeding behavior. I investigate the kinetic capability of 3 taxa using this method. I use my postural modeling method to validate postural models of known behaviors in extant taxa first. I then evaluate the kinetic capabilities of an extinct animal, Tyrannosaurus rex. Finally, Chapter 4 investigates the diversity of the feeding apparatus across parrots, a lineage of morphologically comparable birds with distinctive ecological roles. The biomechanical requirements of similar functional morphology used for diverse feeding behaviors are analyzed here. I use statistical and finite element analyses to describe the biomechanical environment of the feeding apparatus in parrots. I analyze stress and strain dissipation as well as geometric properties of bone mechanics that enable parrots to engage in cranial kinesis. I use a phylogenetic tree informed by molecular phylogenies to plot and compare ancestral reconstructions of characters of the feeding apparatus in parrots. My findings using these methods describe the diversity of the musculoskeletal systems of diverse parrots. The data gathered from the studies described here form the foundation of a better understanding of the biomechanics of the avian feeding apparatus. The findings described here will be used in future studies to describe the underlying mechanisms that govern diverse feeding behaviors.

Sauropsids, unlike mammals, possess an intramandibular joint (IMJ) separating the dentary and postdentary bones, with different lineages either rigidifying (turtles & crocodilians) or maintaining compliance (lepidosaurs & birds) about the joint. IMJ construction and its role on mandibular performance is unclear, impeding our understanding of its function in extinct animals with extreme feeding behaviors like Tyrannosaurus rex. Sauropsids like T. rex pose a particular biomechanical paradox; feeding traces, coprolites, and their robust crania and teeth indicate that they regularly bit through and ingested bone, but their dorsoventrally‐tall and mediolaterally‐thin hemimandibles, IMJ, and patent mandibular symphyses suggest their mandibles were ill‐suited for bone‐crushing bites. Extant sauropsids also exhibit wrapping intramandibularis (mIRA) and pterygoideus ventralis (mPTv) muscles, whose effect on mandibular performance and interaction with the IMJ are unknown. Here we model the effect of the IMJ, symphyseal tissue properties, and wrapping muscle orientation on T. rex mandible biomechanical performance in order to give insight into the biomechanical constraints faced by sauropsids, and the link between their mandibular form and function. Joint tissue histology, gross dissection, and iodine contrast data of extant sauropsids were performed to inform model tissue properties, IMJ construction and muscle orientation. We imported a 3D STL model of the T. rex “STAN” and modeled the IMJ by differing material properties of modeled joint tissues to test the influence of linkage materials on mandibular performance. Muscles were mapped onto the model, and their corresponding muscle moments calculated from area centroids, muscle architecture, and volumes. Wrapping mIRA and mPTv muscles were simulated by directing their force vectors to appropriately positioned dummy points using extant sauropsids as a guide. The mandible was then constrained at the jaw joint and in a series of points along the tooth row from rostral to caudal, simulating both unilateral and bilateral bites. We find that while strains are quite high (>6000 µstrains) about the intramandibular joint, mediolateral bending stresses and strain are markedly reduced by the prearticular, which exhibits greater strain than the surrounding bone. Our results suggest the prearticular of T. rex acted as a strain sink to counteract bending about the IMJ and thereby rigidifying the mandible during feeding. We hypothesize that differences in IMJ articulation and prearticular construction may differentially facilitate or impede prearticular streptognathy, and thus intramandibular kinesis about the IMJ, in sauropsids. Forthcoming models will simulate other theropods within and without Tyrannosauridae to test this hypothesis.