John A. Ruben

Endothermy and activity in vertebrates.

Resting and maximal levels of oxygen consumption of endothermic vertebrates exceed those of ectotherms by an average of five- to tenfold. Endotherms have a much broader range of activity that can be sustained by this augmented aerobic metabolism. Ectotherms are more reliant upon, and limited by, anaerobic metabolism during activity. A principal factor in the evolution of endothermy was the increase in aerobic capacities to support sustained activity.

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

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.

The metabolic status of some Late Cretaceous dinosaurs

Analysis of the nasal region in fossils of three theropod dinosaurs (Nanotyrannus, Ornithomimus, and Dromaeosaurus) and one ornithischian dinosaur (Hypacrosaurus) showed that their metabolic rates were significantly lower than metabolic rates in modern birds and mammals. In extant endotherms and ectotherms, the cross-sectional area of the nasal passage scales approximately with increasing body mass M at M0.72. However, the cross-sectional area of nasal passages in endotherms is approximately four times that of ectotherms. The dinosaurs studied here have narrow nasal passages that are consistent with low lung ventilation rates and the absence of respiratory turbinates.

Cursoriality in bipedal archosaurs

Modern birds have markedly foreshortened tails and their body mass is centred anteriorly, near the wings. To provide stability during powered flight, the avian centre of mass is far from the pelvis, which poses potential balance problems for cursorial birds. To compensate, avians adapted to running maintain the femur subhorizontally, with its distal end situated anteriorly, close to the animals centre of mass; stride generation stems largely from parasagittal rotation of the lower leg about the knee joint. In contrast, bipedal dinosaurs had a centre of mass near the hip joint and rotated the entire hindlimb during stride generation. Here we show that these contrasting styles of cursoriality are tightly linked to longer relative total hindlimb length in cursorial birds than in bipedal dinosaurs. Surprisingly, Caudipteryx , described as a theropod dinosaur, possessed an anterior centre of mass and hindlimb proportions resembling those of cursorial birds. Accordingly, Caudipteryx probably used a running mechanism more similar to that of modern cursorial birds than to that of all other bipedal dinosaurs. These observations provide valuable clues about cursoriality in Caudipteryx , but may also have implications for interpreting the locomotory status of its ancestors.

Respiratory and Reproductive Paleophysiology of Dinosaurs and Early Birds

In terms of their diversity and longevity, dinosaurs and birds were/are surely among the most successful of terrestrial vertebrates. Unfortunately, interpreting many aspects of the biology of dinosaurs and the earliest of the birds presents formidable challenges because they are known only from fossils. Nevertheless, a variety of attributes of these taxa can be inferred by identification of shared anatomical structures whose presence is causally linked to specialized functions in living reptiles, birds, and mammals. Studies such as these demonstrate that although dinosaurs and early birds were likely to have been homeothermic, the absence of nasal respiratory turbinates in these animals indicates that they were likely to have maintained reptile‐like (ectothermic) metabolic rates during periods of rest or routine activity. Nevertheless, given the metabolic capacities of some extant reptiles during periods of elevated activity, early birds were probably capable of powered flight. Similarly, had, for example, theropod dinosaurs possessed aerobic metabolic capacities and habits equivalent to those of some large, modern tropical latitude lizards (e.g., Varanus), they may well have maintained significant home ranges and actively pursued and killed large prey. Additionally, this scenario of active, although ectothermic, theropod dinosaurs seems reinforced by the likely utilization of crocodilian‐like, diaphragm breathing in this group. Finally, persistent in vivo burial of their nests and apparent lack of egg turning suggests that clutch incubation by dinosaurs was more reptile‐ than birdlike. Contrary to previous suggestions, there is little if any reliable evidence that some dinosaur young may have been helpless and nestbound (altricial) at hatching.

Selective Factors Associated with the Origin of Fur and Feathers1

Abstract Conventional wisdom notwithstanding, fur and feathers are unlikely to have arisen in direct association with elevated metabolic rates in early mammals, birds, or their ancestors. A complete insulative fur coat probably appeared first in the earliest mammals long after mammalian ancestors (therapsids) had attained mammalian, or near-mammalian, metabolic rates. The evolution of feathers was unlinked to the evolution of modern avian metabolic rates since early, fully flighted birds (i.e., Archaeopteryx) retained an ectothermic metabolic status. Recent claims of “feathered dinosaurs” should be regarded with caution.

REPTILIAN PHYSIOLOGY AND THE FLIGHT CAPACITY OF ARCHAEOPTERYX

Current scenarios frequently interpret the Late Jurassic bird Archaeopteryx as having had an avian‐type physiology and as having been capable of flapping flight, but only from “the trees downward.” It putatively lacked capacity for takeoff and powered flight from the ground upward.

THE EVOLUTION OF BONE

Vertebrates are practically unique among the Metazoa in their possession of a skeleton made from calcium phosphate rather than calcium carbonate. Interpretation of the origin of a phosphatic skeleton in early vertebrates has previously centered primarily on systemic requirements for phosphate and/or calcium storage or excretion. These interpretations afford no anatomical or physiological advantage(s) that would not have been equally valuable to many invertebrates.

Some correlates of cranial and cervical morphology with predatory modes in snakes

Dissection of the cervical and basicranial regions in three species of snakes indicates that compared to Crotalus viridis and Lichanura roseofusca, Masticophis flagellum possesses relatively high numbers of compound axial muscle insertions on the atlas‐axis and vertebrae numbers 3‐5. It is suggested that the condition in Masticophis facilitates its vertical‐neck‐horizontal‐head foraging posture and has allowed axial muscles inserting on the dorsocaudal braincase in this snake to generate vertical and lateral head movements more effectively.

Getting Warmer, Getting Colder: Reconstructing Crocodylomorph Physiology

Seymour et al. (2004) deserve credit for a provocative article. The question they raise—why crocodilians have a four-chambered heart when other reptiles get along with just three—is valid and interesting, and it deserves far more attention than it has thus far received. However, their suggestion that crocodilians once had endothermic ancestors and reverted back to ectothermy when they invaded aquatic niches is less than compelling for a number of reasons. Seymour et al. actually deal with two separate questions: What was the metabolic status of the early crocodylomorphs? and What selective factors might account for the attributes of modern crocodilians and the transformation that distinguishes this lineage from the ancestral forms? With regard to the first question, they argue not merely that crocodilian biology was modified from that of their Triassic and Early Jurassic ancestors but explicitly that these ancestors had attained full endothermic status. Unfortunately, they provide no compelling evidence that endothermy was in fact present in the ancestral forms. The authors point to the agile body sizes, delicate bones, and erect, possibly bipedal gait of early crocodylomorphs as evidence of a terrestrial, cursorial lifestyle and then postulate that “upright stance and the capacity for highly active, terrestrial behavior are characteristic of endotherms” (p. 1054). However, as the authors themselves acknowledge, attributes such as posture, gait, and bone structure are not compelling evidence of endothermy (in addition to the reviews cited by the authors, see also Farlow 1990; Farlow et al. 1995; Ruben 1995; Chinsamy and Hillenius 2004; Hillenius and Ruben 2004). Early croco-