As the sole surviving members of Archosauria, crocodilians and birds are the best extant models for reconstructing the soft tissue anatomy and physiological state of their extinct relatives. However, for features that are disparate in these terminal taxa, it is difficult to infer their evolutionary history in extinct archosaurs, a problem compounded by the lack of a fossil record for many of these features. The interesting questions of the origin of endothermy, aerobic capacity, and the evolution of the avian respiratory system have been particularly troublesome in this regard and addressing these questions necessitates the use of extant phylogenetic bracketing (EPB) (Witmer, 1995), functional morphological studies (Perry and Sander, 2004), and theoretical models (e.g., Perry et al., 2009). Reconstructing these characters would be greatly aided by unambiguous osteological correlates; however, these have proved illusive. Pneumaticity, or the invasion of bone by air cavities, is a good example of a tempting but equivocal correlate of pulmonary form and function. Pneumaticity is very common in birds, and in the postcranial skeleton, it is caused by diverticula of the respiratory system (e.g., Duncker, 1971; O'Connor, 2004, 2006). Importantly, specific regions of the avian skeleton are pneumatized by distinct parts of the respiratory system; for example, the cervical air sacs typically invade the cervical vertebrae, although this is not a universal feature (e.g., O'Connor, 2004, 2006). Furthermore, the evidence of pneumaticity is preserved in the fossil record, and so this character might provide excellent insight into the unpreserved soft anatomy of the respiratory system (e.g., O'Connor and Claessens, 2005, O'Connor, 2006; Wedel, 2006, 2009). This would be especially interesting if the presence of air sacs was linked to other pulmonary features, such as unidirectional airflow through tubular gas-exchange structures (parabronchi). On the other hand, the use of fossil evidence of pneumaticity to reconstruct respiratory anatomy has been criticized because pneumaticity plays no known role in respiration or gas exchange, and the preponderance of the data indicates its function is lightening the skeleton to aid flight or reduce rotational inertia (Farmer, 2006). In this view, the fact that cervical air sacs pneumatize the cervical vertebrae is simply a consequence of proximity; this part of the respiratory system is nearest at hand, and, therefore, cervical pneumaticity may provide more information about the need to reduce rotational inertia of the neck than it does about the presence or topography of air sacs or about patterns of air flow or gas exchange (Farmer, 2006). Thus, while pneumaticity is consistent with the presence of air sacs, it is not necessarily evidence for air sacs, and additional data are required to shore up or refute hypotheses of bird-like respiratory systems in extinct archosaurs.
Skeletal evidence of a minimally dorsoventrally compressible thorax in fossil taxa might be functionally correlated with two distinct features of the extant avian respiratory system: 1) that the lungs do not change volume significantly with respiration, and 2) the blood-gas barrier (BGB) is extraordinarily thin and the air capillaries are very small in diameter (Duncker, 1971; Perry, 1989; Maina, 2005; Maina and West, 2005). These features are functionally related and place special demands on the axial skeleton. The relationship of the transverse processes of the thoracic vertebrae and the widely separated rib capitula restrict the axis for rib motion (Zimmer, 1935; Duncker, 1971). Ventrally, the lungs are bounded by the horizontal septum (also known as the diaphragm or the pulmonary aponeurosis), which attaches laterally a little dorsal to the intercostal joints and medially to either hypapophyses or a median perpendicular septum that extends ventrally from narrow high vertebral bodies, so that the enclosed space, the cavum pulmonale, undergoes minimal volume changes during breathing and the volume changes that do occur are largely in the ventrolateral portions (Duncker, 1971). The construction of the thorax, therefore, limits the amount of movement of the lung, particularly in the dorsomedial regions, where most of the tubular gas-exchange structures, the parabronchi, are located. The near constant volume of the cavum pulmonale is believed to reduce the mechanical stress on the pulmonary capillaries and enable selection for a very thin, but fragile, blood-gas barrier and very small diameter air capillaries, as they never collapse and therefore require to be reinflated. Until recently, it was thought that, among extant animals, unidirectional airflow was also unique to birds, but the discovery of this character in alligators suggests that it was indeed plesiomorphic for Archosauria (Farmer and Sanders, 2010). Thus, it is necessary to revise what is meant by the phrase “avian-style” features. A constant volume lung might be a true avian synapomorphy, or it may have been present in less derived archosaurs. Here, we analyze the axial skeleton of a phylogenetically broad range of archosaurs to gain insight into the evolution of the rigidity in the thoracic skeleton that is expected to be functionally correlated with the evolution of a lung with near constant volume.
Both the avian and crocodilian respiratory systems are highly derived and modified relative to the pulmonary morphology of lizards and other squamates (e.g., Perry, 1998; Maina, 2002). They are also correspondingly associated with specific anatomical adaptations on the axial skeleton, particularly the vertebral and rib morphology. Based on comparisons between the axial skeleton of extinct archosaurs and their living relatives, revised hypotheses on their pulmonary anatomy and functional morphology can be generated and tested.