The Evolution of Endothermy in Terrestrial Vertebrates: Who? When? Why?

Abstract

Avian and mammalian endothermy results from elevated rates of resting, or routine, metabolism and enables these animals to maintain high and stable body temperatures in the face of variable ambient temperatures. Endothermy is also associated with enhanced stamina and elevated capacity for aerobic metabolism during periods of prolonged activity. These attributes of birds and mammals have greatly contributed to their widespread distribution and ecological success. Unfortunately, since few anatomical/physiological attributes linked to endothermy are preserved in fossils, the origin of endothermy among the ancestors of mammals and birds has long remained obscure. Two recent approaches provide new insight into the metabolic physiology of extinct forms. One addresses chronic (resting) metabolic rates and emphasizes the presence of nasal respiratory turbinates in virtually all extant endotherms. These structures are associated with recovery of respiratory heat and moisture in animals with high resting metabolic rates. The fossil record of nonmammalian synapsids suggests that at least two Late Permian lineages possessed incipient respiratory turbinates. In contrast, these structures appear to have been absent in dinosaurs and nonornithurine birds. Instead, nasal morphology suggests that in the avian lineage, respiratory turbinates first appeared in Cretaceous ornithurines. The other approach addresses the capacity for maximal aerobic activity and examines lung structure and ventilatory mechanisms. There is no positive evidence to support the reconstruction of a derived, avian-like parabronchial lung/air sac system in dinosaurs or nonornithurine birds. Dinosaur lungs were likely heterogenous, multicameral septate lungs with conventional, tidal ventilation, although evidence from some theropods suggests that at least this group may have had a hepatic piston mechanism of supplementary lung ventilation. This suggests that dinosaurs and nonornithurine birds generally lacked the capacity for high, avian-like levels of sustained activity, although the aerobic capacity of theropods may have exceeded that of extant ectotherms. The avian parabronchial lung/air sac system appears to be an attribute limited to ornithurine birds.

Dinosaur Energetics: Setting the Bounds on Feasible Physiologies and Ecologies

“…Respiratory turbinates appeared fairly early in the therapsid lineage (Laass et al 2011) but amongst dinosaurs the first clear indication is not until the Cretaceous ornithurine (that is, crown group) birds. Furthermore the scaling of nasal passage cross-sectional area suggests that there was no room to house respiratory turbinates in dinosaurs (Hillenius and Ruben 2004;but see Witmer 2001).…”

Giants on the landscape: modelling the abundance of megaherbivorous dinosaurs of the Morrison Formation (Late Jurassic, western USA)

“…Dinosaurian metabolic physiology has been a controversial topic (Russell 1965;Ostrom 1970;Bakker 1971Bakker , 1972Spotila et al 1973;Thomas and Olson 1980;Weaver 1983;Farlow 1990;Paladino et al 1990;Paul 1991Paul , 1994Paul , 1998Paul , 2001Barrick and Showers 1994Farlow et al 1995;Ruben 1995;Barrick et al 1996;Ruben et al 1996;Reid 1997;Horner et al 1999Horner et al , 2000O'Connor and Dodson 1999;Seebacher et al 1999;Fricke and Rogers 2000;Seymour and Lillywhite 2000;Burness et al 2001;Jones and Ruben 2001;Schweitzer and Marshall 2001;McNab 2002McNab , 2009bShowers et al 2002;Seebacher 2003;Chinsamy and Hillenius 2004;Hillenius and Ruben 2004a;Padian and Horner 2004;Seymour et al 2004;Chinsamy-Turan 2005;Amiot et al 2006;Gillooly et al 2006;Grellet-Tinner 2006;Sander and Andrassy 2006;…”

Cardio‐pulmonary anatomy in theropod dinosaurs: Implications from extant archosaurs

“…Blood oxygen carrying capacities, blood oxygen affinity and tissue mitochondrial volumes are characters of the soft tissue and have not been described in any fossilized remains. Nasal respiratory turbinates, which are respiratory water and heat conserving mechanisms associated with elevated avian and mammalian rates of pulmonary ventilation have been discussed at length in other publications (Ruben et al, 1996;Ruben et al, 2003;Hillenius and Ruben, 2004a) and are unknown in any theropod remains. However, there exists further evidence in the skeletal and soft tissue remains of theropod dinosaurs that provides insight to their respiratory apparatus and their bird-like or crocodilian-like aerobic capacities.…”

“…3;Hillenius and Ruben, 2004a). At the sternocostal joint, the sternal ribs are distally expanded into two fossae that articulate with the thickened, dorsally oriented posterolateral border of the sternum which bears two paired articular convexities (i.e., internal and external condyles, Zimmer, 1935;Fig.…”

“…Contractions of several intercostal and trunk muscles during inspiration increase the intracostal angle at the joint, rotating the ribs cranially and forcing the sternum ventrally (Fig. 4;Zimmer, 1935;Fedde, 1987;Hillenius and Ruben, 2004a;Codd et al, 2005). Distal coracoids form a saddle joint with the coracoid sulcus of the cranial sternum and the coracoids act as a strut during inhalation: when the sternum is depressed, the caudal end moves further ventrally than the cranial end ( Fig.…”