Leon P. A. M. Claessens

Basic avian pulmonary design and flow-through ventilation in non-avian theropod dinosaurs

Birds are unique among living vertebrates in possessing pneumaticity of the postcranial skeleton, with invasion of bone by the pulmonary air-sac system. The avian respiratory system includes high-compliance air sacs that ventilate a dorsally fixed, non-expanding parabronchial lung. Caudally positioned abdominal and thoracic air sacs are critical components of the avian aspiration pump, facilitating flow-through ventilation of the lung and near-constant airflow during both inspiration and expiration, highlighting a design optimized for efficient gas exchange. Postcranial skeletal pneumaticity has also been reported in numerous extinct archosaurs including non-avian theropod dinosaurs and Archaeopteryx. However, the relationship between osseous pneumaticity and the evolution of the avian respiratory apparatus has long remained ambiguous. Here we report, on the basis of a comparative analysis of region-specific pneumaticity with extant birds, evidence for cervical and abdominal air-sac systems in non-avian theropods, along with thoracic skeletal prerequisites of an avian-style aspiration pump. The early acquisition of this system among theropods is demonstrated by examination of an exceptional new specimen of Majungatholus atopus, documenting these features in a taxon only distantly related to birds. Taken together, these specializations imply the existence of the basic avian pulmonary Bauplan in basal neotheropods, indicating that flow-through ventilation of the lung is not restricted to birds but is probably a general theropod characteristic.

Respiratory evolution facilitated the origin of pterosaur flight and aerial gigantism.

Pterosaurs, enigmatic extinct Mesozoic reptiles, were the first vertebrates to achieve true flapping flight. Various lines of evidence provide strong support for highly efficient wing design, control, and flight capabilities. However, little is known of the pulmonary system that powered flight in pterosaurs. We investigated the structure and function of the pterosaurian breathing apparatus through a broad scale comparative study of respiratory structure and function in living and extinct archosaurs, using computer-assisted tomographic (CT) scanning of pterosaur and bird skeletal remains, cineradiographic (X-ray film) studies of the skeletal breathing pump in extant birds and alligators, and study of skeletal structure in historic fossil specimens. In this report we present various lines of skeletal evidence that indicate that pterosaurs had a highly effective flow-through respiratory system, capable of sustaining powered flight, predating the appearance of an analogous breathing system in birds by approximately seventy million years. Convergent evolution of gigantism in several Cretaceous pterosaur lineages was made possible through body density reduction by expansion of the pulmonary air sac system throughout the trunk and the distal limb girdle skeleton, highlighting the importance of respiratory adaptations in pterosaur evolution, and the dramatic effect of the release of physical constraints on morphological diversification and evolutionary radiation.

DINOSAUR GASTRALIA; ORIGIN, MORPHOLOGY, AND FUNCTION

Abstract Gastralia are dermal ossifications situated in the ventral abdominal wall. Gastralia may be plesiomorphic for tetrapods, but are only retained in extant Crocodylia and Sphenodon, and possibly as part of the chelonian plastron. In contrast to previously published reports, a similar structural configuration of the gastralia is shared throughout prosauropods and (non-ornithurine) theropods. Within the Prosauropoda and Theropoda, the gastralial system consists of approximately 8 to 21 metameric rows. Each row consists of four bones: two lateral and two medial rods. Gastralia of the cranialmost or caudalmost rows may coalesce, forming a median chevron-shaped gastralium. The lateral gastralia articulate in parallel with the medial gastralia in an elongated groove. The medial gastralia imbricate with contralateral gastralia along the ventral midline, creating a series of cranially directed chevrons. Thus all the gastralia are connected to one another, and operate as a single functional unit. The bones recently identified as sauropod gastralia show no morphological similarities with the gastralia of prosauropods and theropods and are probably sternal elements. No gastralia have been recovered in the Ornithischia. In contrast to the reduction of the gastralia in other amniote groups, theropod gastralia show elaborate modification. The anatomy of the gastralial system indicates a more active function than abdominal support or protection. The gastralia may have affected the shape and volume of the trunk in theropods, and may have functioned as an accessory component of the aspiration pump, increasing tidal volume. Moreover, if the caudal region of the lungs in some theropods had differentiated to form abdominal air-sacs, the gastralia might have ventilated them. Gastralial aspiration may have been linked to the generation of small pressure differences between potential cranial and caudal lung diverticula, which may have been important for the evolution of the unidirectional airflow lung of birds.

The skeletal kinematics of lung ventilation in three basal bird taxa (emu, tinamou, and guinea fowl).

In vivo visceral and skeletal kinematics of lung ventilation was examined using cineradiography in two palaeognaths, the emu (Dromaius novaehollandiae) and the Chilean tinamou (Nothoprocta perdicaria), and a basal neognath, the helmeted guinea fowl (Numida meleagris). Upon inspiration, the thorax expands in all dimensions. The vertebral ribs swing forward and upward, thereby increasing the transverse diameter of the trunk. The consistent location of the parapophysis throughout the dorsal vertebral series, ventral and cranial to the diapophysis, ensures a relatively uniform lateral expansion. An increase in the angle between the vertebral and the sternal ribs causes the sternal ribs to push the sternum ventrally. Owing to the greater length of the caudal sternal ribs, the caudal sternal margin is displaced further ventrally than the cranial sternal margin. When observed in lateral view, sternal movement is not linear, but elliptical. The avian thorax is highly constrained in its movement when compared with crocodylians, the other extant archosaur clade. Birds lack a lumbar region and intermediate ribs. Sternal ribs are completely ossified, and have a bicondylar articulation with the sternum. Considering the importance of pressure differences between cranial and caudal air sac complexes for the generation of unidirectional air flow in the avian lung, it is hypothesized that a decrease in the degrees of freedom of movement of the avian trunk skeleton, greater expansion of the ventrocaudal trunk region, and elliptical sternal movement may represent specific adaptations for fine-tuned control over air flow within the complex avian pulmonary system.

Archosaurian respiration and the pelvic girdle aspiration breathing of crocodyliforms

Birds and crocodylians, the only living archosaurs, are generally believed to employ pelvic girdle movements as a component of their respiratory mechanism. This in turn provides a phylogenetic basis for inferring that extinct archosaurs, including dinosaurs, also used pelvic girdle breathing. I examined lung ventilation through cineradiography (high–speed X–ray filming) and observed that alligators indeed rotate the pubis to increase tidal volume, but did not observe pelvic girdle movement contributing to lung ventilation in guinea fowl, emus or tinamous, despite extensive soft–tissue motion. Re–examination of fossil archosaurs reveals that pubic rotation evolved in basal crocodyliforms and that pelvic girdle breathing is not a general archosaurian mechanism. The appearance of pelvic aspiration in crocodyliforms is a striking example of the ability of amniotes to increase gas exchange or circumvent constraints on respiration through the evolution of novel accessory breathing mechanisms.

A cineradiographic study of lung ventilation in Alligator mississippiensis

The skeletal and visceral kinematics of lung ventilation of the American alligator (Alligator mississippiensis) was examined using cineradiography, pneumotachometry, and intrapulmonary pressure recording. The respiratory pattern of A. mississippiensis is intermittent and diphasic. The inspiratory lung volume is retained during the non-ventilatory period through closure of the glottis. The aspiration pump of A. mississippiensis consists of multiple components: visceral movement, pubic rotation, gastralial movement, and costosternal movement, which vary independently in their contribution to lung ventilation. Vertebral flexion and extension is also observed, and may be a passive artifact of costal displacement. The amount of craniocaudal visceral movement during lung ventilation is variable, and can produce as much as 60% of the tidal volume. Pubic rotation is not directly coupled to visceral movement and contributes a relatively small percentage of the tidal volume, approximately 4% on average, as does vertebral flexion, which contributes less than 3%. Costosternal movement contributes the remaining majority of tidal volume, generally over 40%. The gastralia stiffen the abdominal wall and likely facilitate unified displacement of the abdominal wall. Tripartite ribs facilitate thoracic movement, allowing substantial excursion of the body wall. A relatively abrupt change in position of the vertebral parapophysis in the anterior thorax results in an increase in lateral rib movement in the posterior half of the thorax. The crocodylian aspiration pump appears to consist of a derived pelvic and diaphragmatic breathing pump combined with a basal costosternal and gastralial aspiration pump.

Open data and digital morphology

Over the past two decades, the development of methods for visualizing and analysing specimens digitally, in three and even four dimensions, has transformed the study of living and fossil organisms. However, the initial promise that the widespread application of such methods would facilitate access to the underlying digital data has not been fully achieved. The underlying datasets for many published studies are not readily or freely available, introducing a barrier to verification and reproducibility, and the reuse of data. There is no current agreement or policy on the amount and type of data that should be made available alongside studies that use, and in some cases are wholly reliant on, digital morphology. Here, we propose a set of recommendations for minimum standards and additional best practice for three-dimensional digital data publication, and review the issues around data storage, management and accessibility.

A Redescription of Ornithomimus velox Marsh, 1890 (Dinosauria, Theropoda)

ABSTRACT The theropod genus and species Ornithomimus velox was erected based on a partial hind limb recovered from the late Maastrichtian Denver Formation. A partial manus, which likely belonged to the same individual, was also recovered and described in the same paper. Ornithomimus edmontonicus is the only other valid species currently recognized in the genus. The validity of Ornithomimus velox has been questioned due to its fragmentary nature and because the diagnostic features identified when the species was erected are now considered characteristic for the family. The pes and manus of Ornithomimus velox were never fully prepared. In the original description, reconstructed metatarsals were figured, but manual phalanges, although preserved, were not described. Here we describe and reevaluate Ornithomimus velox based upon a new preparation of the specimen. Metacarpal proportions are diagnostic for the genus, with metacarpal I longer than metacarpal II, which in turn is longer than metacarpal III. The pes and manus of Ornithomimus velox are smaller than in the type specimen of Ornithomimus edmontonicus. Ornithomimus velox can be distinguished from Ornithomimus edmontonicus based on the robusticity of the pes. Material previously referred to Ornithomimus velox from the Kaiparowits Formation of Utah is older and morphologically distinct and does not represent the same species. The morphological disparity and temporal separation observed in specimens referred to Ornithomimus edmontonicus suggest that it may represent a species complex. The redescription and diagnosis of Ornithomimus velox provides a new framework to investigate ornithomimid systematics.

A review of the dodo and its ecosystem: insights from a vertebrate concentration Lagerstätte in Mauritius

ABSTRACT The dodo Raphus cucullatus Linnaeus, 1758, an extinct and flightless, giant pigeon endemic to Mauritius, has fascinated people since its discovery, yet has remained surprisingly poorly known. Until the mid-19th century, almost all that was known about the dodo was based on illustrations and written accounts by 17th century mariners, often of questionable accuracy. Furthermore, only a few fragmentary remains of dodos collected prior to the birds extinction exist. Our understanding of the dodos anatomy was substantially enhanced by the discovery in 1865 of subfossil bones in a marsh called the Mare aux Songes, situated in southeastern Mauritius. However, no contextual information was recorded during early excavation efforts, and the majority of excavated material comprised larger dodo bones, almost all of which were unassociated. Here we present a modern interdisciplinary analysis of the Mare aux Songes, a 4200-year-old multitaxic vertebrate concentration Lagerstätte. Our analysis of the deposits at this site provides the first detailed overview of the ecosystem inhabited by the dodo. The interplay of climatic and geological conditions led to the exceptional preservation of the animal and associated plant remains at the Mare aux Songes and provides a window into the past ecosystem of Mauritius. This interdisciplinary research approach provides an ecological framework for the dodo, complementing insights on its anatomy derived from the only associated dodo skeletons known, both of which were collected by Etienne Thirioux and are the primary subject of this memoir. Citation for this article: Rijsdijk, K. F., J. P. Hume, P. G. B. de Louw, H. J. M. Meijer, A. Janoo, E. J. de Boer, L. Steel, J. de Vos, L. G. van der Sluis, H. Hooghiemstra, F. B. V. Florens, C. Baider, T. J. J. Vernimmen, P. Baas, A. H. van Heteren, V. Rupear, G. Beebeejaun, A. Grihault, J. van der Plicht, M. Besselink, J. K. Lubeek, M. Jansen, S. J. Kluiving, H. Hollund, B. Shapiro, M. Collins, M. Buckley, R. M. Jayasena, N. Porch, R. Floore, F. Bunnik, A. Biedlingmaier, J. Leavitt, G. Monfette, A. Kimelblatt, A. Randall, P. Floore, and L. P. A. M. Claessens. 2015. A review of the dodo and its ecosystem: insights from a vertebrate concentration Lagerstätte in Mauritius; pp. 3–20 in L. P. A. M. Claessens, H. J. M. Meijer, J. P. Hume, and K. F. Rijsdijk (eds.), Anatomy of the Dodo (Raphus cucullatus L., 1758): An Osteological Study of the Thirioux Specimens. Society of Vertebrate Paleontology Memoir 15. Journal of Vertebrate Paleontology 35(6, Supplement).

The evolution, development and skeletal identity of the crocodylian pelvis: revisiting a forgotten scientific debate.

Unlike most tetrapods, in extant crocodylians the acetabulum is formed by only two of the three skeletal elements that constitute the pelvis, the ilium, and ischium. This peculiar arrangement is further confused by various observations that suggest the crocodylian pelvis initially develops from four skeletal elements: the ilium, ischium, pubis, and a novel element, the prepubis. According to one popular historical hypothesis, in crocodylians (and many extinct archosaurs), the pubis fuses with the ischium during skeletogenesis, leaving the prepubis as a distinct element, albeit one which is excluded from the acetabulum. Whereas the notion of a distinct prepubic element was once a topic of considerable interest, it has never been properly resolved. Here, we combine data gleaned from a developmental series of Alligator mississippiensis embryos, with a revised interpretation of fossil evidence from numerous outgroups to Crocodylia. We demonstrate that the modern crocodylian pelvis is composed of only three elements: the ilium, ischium, and pubis. The reported fourth pelvic element is an unossified portion of the ischium. Interpretations of pelvic skeletal homology have featured prominently in sauropsid systematics, and the unambiguous identification of the crocodylian pubis provides an important contribution to address larger scale evolutionary questions associated with locomotion and respiration. J. Morphol. , 2012.