Deep reptilian evolutionary roots of a major avian respiratory adaptation.

Vertebral ribs of the anterior thorax in extant birds bear bony prongs called uncinate processes, which improve the mechanical advantage of mm. appendicocostales to move air through the immobile lung and pneumatic air sacs. Among non-avian archosaurs, broad, cartilaginous uncinate processes are present in extant crocodylians, and likely have a ventilatory function. Preserved ossified or calcified uncinate processes are known in several non-avian dinosaurs. However, whether other fossil archosaurs possessed cartilaginous uncinate processes has been unclear. Here, we establish osteological correlates for uncinate attachment to vertebral ribs in extant archosaurs, with which we inferred the presence of uncinate processes in at least 19 fossil archosaur taxa. An ancestral state reconstruction based on the infer distribution suggests that cartilaginous uncinate processes were plesiomorphically present in Dinosauria and arguably in Archosauria, indicating that uncinate processes, and presumably their ventilatory function, have a deep evolutionary history extending back well beyond the origin of birds.

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.

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.

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.

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.

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.

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.

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.