Ryan C. Ridgely

Using CT to Peer into the Past: 3D Visualization of the Brain and Ear Regions of Birds, Crocodiles, and Nonavian Dinosaurs

Until relatively recently, information on the internal skull structures of fossil taxa relied on fortuitous breaks, aggressive removal of rock matrix (Galton 1989, 2001), sectioning with a saw (Osborn 1912), or serial ground thin-sectioning (Stensio 1963), all of which potentially risk damage to the fossil specimen (or even consume it entirely in the case of ground thin-sections). In some cases, casts of internal structures, such as the brain cavity and labyrinth of the inner ear, were preserved as ‘natural endocasts’ by infilling with more resistant matrix (e.g., Newton 1888). In most cases, however, physical endocasts are made after matrix removal by coating internal cavities with latex and then removing the cured replica, referred to as a latex endocast (Radinsky 1968; Jerison 1973; Hopson 1979). The process of making latex endocasts poses further risks to the fossil, and for many fragile specimens, such an approach has been unfeasible.

New Insights Into the Brain, Braincase, and Ear Region of Tyrannosaurs (Dinosauria, Theropoda), with Implications for Sensory Organization and Behavior

The braincase region of tyrannosaurs was investigated to provide insights on anatomical attributes relevant to inferences of sensory biology and behavior. CT scanning focused on three specimens of Tyrannosaurus rex, a juvenile Gorgosaurus, and the controversial Cleveland skull (CMNH 7541). Analysis shows that the cerebral hemispheres were enlarged, but conflicting information on the optic lobes suggests that brain conformation was not fully avian. Previous estimates of olfactory bulb size for T. rex were much too large, but even the corrected sizes are relatively larger than other theropods, suggesting that odor detection was indeed of particular importance to tyrannosaurs. The inner ears show a number of coelurosaurian traits, such as elongate and rounded and rostral, lateral semicircular canals, and incipient twisting of the common crus, which we interpret to be related to enhanced reflexes coordinating rapid eye and head movements. The cochlea is elongate, which, coupled with the finding of extensive tympanic pneumaticity, supports the inference of behavioral emphasis of low‐frequency sounds. Three main groups of sinuses pneumatized the braincase, and there are a number of perhaps systematically relevant differences. Orientation of the endosseous labyrinth reveals that alert head postures of T. rex and Gorgosaurus were somewhat depressed below the horizontal, but the Cleveland skull had a very strongly down‐turned posture. It is concluded that tyrannosaur sensory biology is consistent with their predatory coelurosaurian heritage, with emphasis on relatively quick, coordinated eye and head movements, and probably sensitive low‐frequency hearing; tyrannosaurs apomorphically enhanced their olfactory apparatus. The taxonomic status of the Cleveland skull remains unresolved. Anat Rec, 292:1266–1296, 2009.

The Paranasal Air Sinuses of Predatory and Armored Dinosaurs (Archosauria: Theropoda and Ankylosauria) and Their Contribution to Cephalic Structure

The paranasal air sinuses and nasal cavities were studied along with other cephalic spaces (brain cavity, paratympanic sinuses) in certain dinosaurs via CT scanning and 3D visualization to document the anatomy and examine the contribution of the sinuses to the morphological organization of the head as a whole. Two representatives each of two dinosaur clades are compared: the theropod saurischians Majungasaurus and Tyrannosaurus and the ankylosaurian ornithischians Panoplosaurus and Euoplocephalus. Their extant archosaurian outgroups, birds and crocodilians (exemplified by ostrich and alligator), display a diversity of paranasal sinuses, yet they share only a single homologous antorbital sinus, which in birds has an important subsidiary diverticulum, the suborbital sinus. Both of the theropods had a large antorbital sinus that pneumatized many of the facial and palatal bones as well as a birdlike suborbital sinus. Given that the suborbital sinus interleaves with jaw muscles, the paranasal sinuses of at least some theropods (including birds) were actively ventilated rather than being dead‐air spaces. Although many ankylosaurians have been thought to have had extensive paranasal sinuses, most of the snout is instead (and surprisingly) often occupied by a highly convoluted airway. Digital segmentation, coupled with 3D visualization and analysis, allows the positions of the sinuses to be viewed in place within both the skull and the head and then measured volumetrically. These quantitative data allow the first reliable estimates of dinosaur head mass and an assessment of the potential savings in mass afforded by the sinuses. Anat Rec, 291:1362–1388, 2008.

Evolution of olfaction in non-avian theropod dinosaurs and birds

Little is known about the olfactory capabilities of extinct basal (non-neornithine) birds or the evolutionary changes in olfaction that occurred from non-avian theropods through modern birds. Although modern birds are known to have diverse olfactory capabilities, olfaction is generally considered to have declined during avian evolution as visual and vestibular sensory enhancements occurred in association with flight. To test the hypothesis that olfaction diminished through avian evolution, we assessed relative olfactory bulb size, here used as a neuroanatomical proxy for olfactory capabilities, in 157 species of non-avian theropods, fossil birds and living birds. We show that relative olfactory bulb size increased during non-avian maniraptoriform evolution, remained stable across the non-avian theropod/bird transition, and increased during basal bird and early neornithine evolution. From early neornithines through a major part of neornithine evolution, the relative size of the olfactory bulbs remained stable before decreasing in derived neoavian clades. Our results show that, rather than decreasing, the importance of olfaction actually increased during early bird evolution, representing a previously unrecognized sensory enhancement. The relatively larger olfactory bulbs of earliest neornithines, compared with those of basal birds, may have endowed neornithines with improved olfaction for more effective foraging or navigation skills, which in turn may have been a factor allowing them to survive the end-Cretaceous mass extinction.

The evolution of mammal-like crocodyliforms in the Cretaceous Period of Gondwana

Fossil crocodyliforms discovered in recent years have revealed a level of morphological and ecological diversity not exhibited by extant members of the group. This diversity is particularly notable among taxa of the Cretaceous Period (144–65 million years ago) recovered from former Gondwanan landmasses. Here we report the discovery of a new species of Cretaceous notosuchian crocodyliform from the Rukwa Rift Basin of southwestern Tanzania. This small-bodied form deviates significantly from more typical crocodyliform craniodental morphologies, having a short, broad skull, robust lower jaw, and a dentition with relatively few teeth that nonetheless show marked heterodonty. The presence of morphologically complex, complementary upper and lower molariform teeth suggests a degree of crown–crown contact during jaw adduction that is unmatched among known crocodyliforms, paralleling the level of occlusal complexity seen in mammals and their extinct relatives. The presence of another small-bodied mammal-like crocodyliform in the Cretaceous of Gondwana indicates that notosuchians probably filled niches and inhabited ecomorphospace that were otherwise occupied by mammals on northern continents.

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.

Endocranial Anatomy of Lambeosaurine Hadrosaurids (Dinosauria: Ornithischia): A Sensorineural Perspective on Cranial Crest Function

Brain and nasal cavity endocasts of four corythosaurian lambeosaurines (Dinosauria: Ornithischia) were investigated to test hypotheses of cranial crest function related to sensorineural systems. Endocasts were generated through computed tomography and three‐dimensional rendering and visualization software. The sample comprises a range of ontogenetic stages from the taxa Lambeosaurus, Corythosaurus, and Hypacrosaurus. Results show that the morphology of brain endocasts differs little from that of hadrosaurines. The strikingly convoluted nasal vestibule of Hypacrosaurus altispinus, when interpreted in the context of lambeosaurine phylogeny, suggests selective pressure for nasal cavity function independent from changes in the external shape of the crest and associated visual display function. The plesiomorphically small olfactory bulbs and apparently small olfactory region of the nasal cavity argues against the hypothesis that increased olfactory acuity played a causal role in crest evolution. The elongate cochlea of the inner ear reveals that hearing in lambeosaurines emphasized low frequencies consistent with the hypothesized low‐frequency calls made by the crests under the resonation model of crest function. The brain is relatively large in lambeosaurines compared with many other large dinosaurs, and the cerebrum is relatively larger than that of all non‐hadrosaurian ornithischians and large theropods, but compares favorably with hadrosaurine hadrosaurids as well as some maniraptoran theropods. It is concluded that the large brains of lambeosaurines are consistent with the range of social behaviors inferred when the crest is interpreted as an intraspecific signaling structure. Anat Rec, 292:1315–1337, 2009.

Cranial osteology of a juvenile specimen of Tarbosaurus bataar (Theropoda, Tyrannosauridae) from the Nemegt Formation (Upper Cretaceous) of Bugin Tsav, Mongolia

ABSTRACT A juvenile skull of the tyrannosaurid Tarbosaurus bataar found in the Bugjn Tsav locality in the Mongolian Gobi Desert is described. With a total length of 290 mm, the present specimen represents one of the smallest skulls known for this species. Not surprisingly, it shows various characteristics common to juvenile tyrannosaurids, such as the rostral margin of the maxillary fenestra not reaching that of the external antorbital fenestra and the postorbital lacking the cornual process. The nasal bears a small lacrimal process, which disappears in adults. Lacking some of the morphological characteristics that are adapted for bearing great feeding forces in adult individuals, this juvenile specimen suggests that T. bataar would have changed its dietary niches during ontogeny. The numbers of alveoli in the maxilla (13) and dentary (14 and 15) are the same as those in adults, suggesting that they do not change onto genetically in T. bataar and thus are not consistent with the hypothesis that the numbers of alveoli decreases ontogenetically in tyrannosaurids.

Breathing Life Into Dinosaurs: Tackling Challenges of Soft‐Tissue Restoration and Nasal Airflow in Extinct Species

The nasal region plays a key role in sensory, thermal, and respiratory physiology, but exploring its evolution is hampered by a lack of preservation of soft‐tissue structures in extinct vertebrates. As a test case, we investigated members of the “bony‐headed” ornithischian dinosaur clade Pachycephalosauridae (particularly Stegoceras validum) because of their small body size (which mitigated allometric concerns) and their tendency to preserve nasal soft tissues within their hypermineralized skulls. Hypermineralization directly preserved portions of the olfactory turbinates along with an internal nasal ridge that we regard as potentially an osteological correlate for respiratory conchae. Fossil specimens were CT‐scanned, and nasal cavities were segmented and restored. Soft‐tissue reconstruction of the nasal capsule was functionally tested in a virtual environment using computational fluid dynamics by running air through multiple models differing in nasal soft‐tissue conformation: a bony‐bounded model (i.e., skull without soft tissue) and then models with soft tissues added, such as a paranasal septum, a scrolled concha, a branched concha, and a model combining the paranasal septum with a concha. Deviations in fluid flow in comparison to a phylogenetically constrained sample of extant diapsids were used as indicators of missing soft tissue. Models that restored aspects of airflow found in extant diapsids, such as appreciable airflow in the olfactory chamber, were judged as more likely. The model with a branched concha produced airflow patterns closest to those of extant diapsids. These results from both paleontological observation and airflow modeling indicate that S. validum and other pachycephalosaurids could have had both olfactory and respiratory conchae. Although respiratory conchae have been linked to endothermy, such conclusions require caution in that our re‐evaluation of the reptilian nasal apparatus indicates that respiratory conchae may be more widespread than originally thought, and other functions, such as selective brain temperature regulation, could be important. Anat Rec, 297:2148–2186, 2014.

Neurocranial Osteology and Neuroanatomy of a Late Cretaceous Titanosaurian Sauropod from Spain (Ampelosaurus sp.)

Titanosaurians were a flourishing group of sauropod dinosaurs during Cretaceous times. Fossils of titanosaurians have been found on all continents and their remains are abundant in a number of Late Cretaceous sites. Nonetheless, the cranial anatomy of titanosaurians is still very poorly known. The Spanish latest Cretaceous locality of “Lo Hueco” yielded a relatively well preserved, titanosaurian braincase, which shares a number of phylogenetically restricted characters with Ampelosaurus atacis from France such as a flat occipital region. However, it appears to differ from A. atacis in some traits such as the greater degree of dorsoventral compression and the presence of proatlas facets. The specimen is, therefore, provisionally identified as Ampelosaurus sp. It was CT scanned, and 3D renderings of the cranial endocast and inner-ear system were generated. Our investigation highlights that, although titanosaurs were derived sauropods with a successful evolutionary history, they present a remarkably modest level of paleoneurological organization. Compared with the condition in the basal titanosauriform Giraffatitan brancai, the labyrinth of Ampelosaurus sp. shows a reduced morphology. The latter feature is possibly related to a restricted range of head-turning movements.