Respiratory evolution facilitated the origin of pterosaur flight and aerial gigantism

Abstract

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.

Figure 1. Micro-computed tomographic (CT) scans and photograph illustrating external pneumatic openings and typical pneumatic architecture in the ornithocheirid pterosaur Anhanguera santanae (AMNH 22555).

Vertebral (a, b), carpal (c, d), and pelvic (e, f) elements are characterized by the presence of thin cortical bone and large internal cavities (b, d, f). a, b, Mid-cervical (6^th) vertebra in oblique craniolateral (a) and cutaway oblique craniolateral (b) views. Vertebral height = 5 cm. c, d, Left distal syncarpal in proximal (c) and cutaway proximal (d) views. e, dorsal view of block with pelvic elements, sacral vertebrae, and posterior dorsal vertebrae. Black arrows indicate the location of pneumatic foramina on select vertebrae (e) and white arrows indicate both pneumatic foramina and internal pneumatic cavities on pelvic elements (f). Asterisks on (e) delineate the location of the transverse section (dashed blue line) shown in (f). f, Transverse CT scan transect through pelvic block, showing pneumaticity of the sacral neural spine, ilia and left pubis. Note the large pneumatic opening on the surface of the left ilium. Scale bar (c–f) = 1 cm. li, left ilium; Ns, neural spine; Pf, pneumatic foramen; Pz, prezygapophysis; ri, right ilium; rp, right pubis; s3, sacral vertebra 3.

Figure 2. Thoracic and pelvic anatomy of the basal pterosaur Rhamphorhynchus (a–d) and the pterodactyloid Pteranodon (e, f).

a, Rhamphorhynchus muensteri (MB-R. 3633.1-2) showing the location of magnified sections b through d. b, Trunk, showing the location of thoracic and pelvic bones. c, Pelvis, right lateral view, showing the location of the pubis-prepubis joint and the medial prepubic prong. d, Sternal ribs 1 through 7, illustrating the ordered arrangement of sternocostapophyses that act as levers for the intercostal muscles (black arrows). e, Sternum of Pteranodon (YPM 2546), showing fragments of the distal sternal ribs articulating with the costal facets of the sternum. f, Complete sternal rib of Pteranodon (YPM 1175), showing the erose sternal rib margins but ordered distribution of the sternocostapophyses. Scale (a, e) is in centimeters. Abbreviations: F: fragments of distal sternal ribs, Il: ilium, Is: ischium, Pppj: pubic-prepubic joint, Ppu: prepubis, Pu: pubis, Sr: sternal ribs, St: sternum, Vr: vertebral ribs, 1–7, sternal ribs one through seven. Division of Vertebrate Paleontology, YPM 2546 and YPM 1175 (c) 2005 Peabody Museum of Natural History, Yale University, New Haven, Connecticut, USA. All rights reserved.

Figure 3. Models of ventilatory kinematics and the pulmonary air sac system of pterosaurs.

a, Model of ventilatory kinematics in Rhamphorhynchus. Thoracic movement induced by the ventral intercostal musculature results in forward and outward displacement of the distal vertebral and proximal sternal ribs, and ventral displacement of the sternum, upon inspiration (blue arrows and pink outline). In addition, ventral expansion of the abdomen is induced through caudoventral rotation of the prepubis. Ranges of skeletal movement were modelled after those observed in vivo in the avian thorax and the crocodylian pelvis , . Rhamphorhynchus modified from Wellnhofer . b, Model of ventilatory kinematics in Pteranodon wherein the fused anterior vertebral ribs and articulation of the scapulocoracoid with the supraneural plate and anterior sternum limit movement of the anterior sternum, which cannot undergo elliptical rotation. However, the posterior vertebral ribs, sternal ribs, sternum, and prepubis are still capable of anterodorsal-posteroventral excursions facilitating volumetric increases and decreases of the thorax during inspiration-expiration. Pteranodon modified from Bennett . c, d, reconstruction of pulmonary air sac system in the Lower Cretaceous ornithocheirid Anhanguera santanae (AMNH 22555). c, Lateral view showing the inferred position of the lungs (orange), cervical (green) and abdominal air sacs (blue), as predicted on the basis of postcranial skeletal pneumaticity. Thoracic air sacs (shown in grey) are also likely to have been present, but generally do not leave a distinct osteological trace. Humerus and more distal forelimb not shown. d, Dorsal view illustrating the inferred position of subcutaneous diverticular networks (light blue) distally along the wing. The right side depicts a conservative estimate for the size of the airsac network, limiting it to the pre-axial margin of the wing based solely on the presence of pneumatic foramina in closely positioned wing bones. The left side depicts the likely maximal size of an inferred diverticular network, accounting for its inclusion between the dorsal and ventral layers of the wing membrane. Scale = 10 cm. Skeletal reconstruction in c, d modified from Wellnhofer . Abbreviations: as in figure 2, and: Cor: coracoid portion of scapulocoracoid, Ga: gastralia.

Figure 4. The evolution of the respiratory apparatus in pterosaurs.

Tree based on Unwin (2003, 2004), stratigraphic data correct to 2008 (Unwin, unpublished data) and the chronology of Gradstein et al. (2004). Black bars indicate known stratigraphic ranges of the main pterosaur clades, listed at right. Dashed section of bars denotes range extension based on an unverified record. Thick black lines signify a range extension inferred from phylogenetic relationships. Color-filled circles represent occurrences of pneumatization with the following distributions: red = vertebral column; yellow = postaxial pathway in the forelimb; blue = preaxial pathway in the forelimb and in some cases (lonchodectids, Tupuxuara, azhdarchids) a limited presence in the hind limb. Clades in which one or more species reached a wingspan of more than 2.5 metres are shown in underlined dark blue text, and more than 5.0 metres, in caps. A, Basic pterosaurian breathing pump (sternum, vertebral and sternal ribs, gastralia and prepubes): B, notarium. Taxa referred to in the text: 1, Dimorphodon; 2, Eudimorphodon; 3, Rhamphorhynchus; 4, Anhanguera; 5, Pteranodon; 6, Dsungaripterus; 7, Tapejara; 8, Tupuxuara; 9, Quetzalcoatlus.