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.

Pterosaur body mass estimates from three-dimensional mathematical slicing

“…Birds and pterosaurs are both members of the clade Archosauria (Diapsida) (Benton, 1997), and each would have inherited a similar basic body architecture from a common ancestor. Both birds and pterosaurs show evidence for extensive pneumatization of their axial and appendicular skeletons (Bonde and Christiansen, 2003;Claessens et al, 2009). Birds breathe with a highly efficient, flow-through lung ventilated with a system of abdominal, thoracic, and clavicular air sacs (Proctor and Lynch, 1993), and pterosaurs are interpreted to have had a similar respiratory system (Bonde and Christiansen, 2003;Butler et al, 2009).…”

“…The reduction factor for decreasing the depths and widths with distance was set to 0.55, because the pedes do not become as slender as the distal wing phalanges. The density of the muscled portions of the arms was set at 900 g/liter in light of the hollow nature of the bones, and the evidence for air sacs in the arms (Claessens et al, 2009). The leg density was set at 1000 g/liter.…”

“…The trunk region (pelvic and thoracic) was set to 850 g/liter, and the head and neck were set to 300 g/liter. Although their volumes were not specifically determined, the expectation is that the nasal and oral cavities, and any cranial sinuses, would have been extensive in the skulls of pterosaurs given the high degree of pneumaticity in their skeletons as a whole (Claessens et al, 2009), thus heads were set to a low density. Although there may have been decreases in body and skull density with increasing body size in pterosaurs, direct, reliable evidence of this sort of change is lacking.…”

“…The most parsimonius assumption, given the current state of our knowledge of these animals and their fossil remains, is to assume densities similar to that of birds. The long bony tails of the 'rhamphorhynchoids' had their densities set to 1000 g/liter, whereas those of the more derived pterodactyloids were set to 850 g/liter in light of evidence for more extensive pneumatization (Claessens et al, 2009). The patagial masses were computed by multiplying their volumes by an appropriate density.…”

A pterosaur manus track from Denali National Park, Alaska Range, Alaska, United States

“…The presence of pterosaurs from high-paleolatitude settings (Alaska and New Zealand) is consistent with the implication of Seymour et al (2004) that pterosaurs, as members of the Archosauria, were endothermic. Recently the skeletons of large pterosaurs have been shown to have increased appendicular pneumaticity and this may have aided in thermoregulation (Claessens et al, 2009). The large size of the DENA pterosaur, as a function of thermoregulation capabilities, is expected given the presumed strong seasonality of this ancient northern environment (Brouwers et al, 1987;Parrish et al, 1987;Gangloff, 2000, 2001;Fiorillo, 2004Fiorillo, , 2008aFiorillo, , 2008b.…”