C. G. Farmer

Unidirectional Airflow in the Lungs of Alligators

Alligator Breath Birds have a unidirectional system of airflow within their lungs that has been attributed to the peculiarities of flight. However, Farmer and Sanders (p. 338) provide evidence that this unidirectional and more or less continuous flow of air also occurs through parts of the alligator lung; in contrast to the tidal, biphasic system in mammals. By analyzing lung and tracheal structures, the similarities of the alligator lungs were compared with those of birds. The data suggest that the unusual properties of bird lungs originated before the divergence of the alligator line from the dinosaur or avian line. Crocodilian and bird lungs share patterns of air flow, indicating a common evolutionary origin. The lungs of birds move air in only one direction during both inspiration and expiration through most of the tubular gas-exchanging bronchi (parabronchi), whereas in the lungs of mammals and presumably other vertebrates, air moves tidally into and out of terminal gas-exchange structures, which are cul-de-sacs. Unidirectional flow purportedly depends on bellowslike ventilation by air sacs and may have evolved to meet the high aerobic demands of sustained flight. Here, we show that air flows unidirectionally through parabronchi in the lungs of the American alligator, an amphibious ectotherm without air sacs, which suggests that this pattern dates back to the basal archosaurs of the Triassic and may have been present in their nondinosaur descendants (phytosaurs, aetosaurs, rauisuchians, crocodylomorphs, and pterosaurs) as well as in dinosaurs.

The evolution of pelvic aspiration in archosaurs

Abstract Movements of the pelvic girdle have recently been found to contribute to inspiratory airflow in both crocodilians and birds. Although the mechanisms are quite different in birds and crocodilians, participation of the pelvic girdle in the production of inspiration is rare among vertebrates. This raises the possibility that the pelvic musculoskeletal system may have played a role in the ventilation of basal archosaurs. Judging from the mechanism of pelvic aspiration in crocodilians and the structure of gastralia in basal archosaurs, we suggest that an ischiotruncus muscle pulled the medial aspect of the gastralia caudally, and thereby helped to produce inspiration by increasing the volume of the abdominal cavity. From this basal mechanism, several archosaur lineages appear to have evolved specialized gastralia, pelvic kinesis, and/or pelvic mobility. Kinetic pubes appear to have evolved independently in at least two clades of Crocodylomorpha. This convergence suggests that a diaphragmatic muscle may be basal for Crocodylomorpha. The pelvis of pterosaurs was long, open ventrally, and had prepubic elements that resembled the pubic bones of Recent crocodilians. These characters suggest convergence on the pelvic aspiratory systems of both birds and crocodilians. The derived configuration of the pubis, ischium and gastralia of non-avian theropods appears to have enhanced the basal gastral breathing mechanism. Changes in structure of the pelvic musculoskeletal system that were present in both dromaeosaurs and basal birds may have set the stage for a gradual reduction in the importance of gastral breathing and for the evolution of the pelvic aspiration system of Recent birds. Lastly, the structure of the pelvis of some ornithischians appears to have been permissive of pubic and ischial kinesis. Large platelike prepubic processes evolved three times in Ornithischia. These plates are suggested to have been instrumental in an active expansion of the lateral abdominal wall to produce inspiratory flow. Thus, many of the unique features found in the pelvic girdles of various archosaur groups may be related to the function of lung ventilation rather than to locomotion.

Reproduction: The adaptive significance of endothermy

A central theme raised by Angilletta and Sears is that the energetic cost of endothermy is too enormous to be offset by the benefits that thermogenesis could provide for reproduction. Angilletta and Sears suggest that parents would have been better off producing additional offspring with the energy used for incubation or minimizing their risk of predation by minimizing foraging efforts. However, these views overlook the fact that a defining characteristic of both birds and mammals is high investment in relatively few offspring. The evolution of parental provisioning behaviors is cogent evidence that minimizing foraging efforts and risks of adult predation were not favored over energy expenditure for parental care. Furthermore, the energetic costs of parental feeding of offspring demonstrate that the benefits of parental care can outweigh energetic expenses that exceed by far the cost of endothermy. If the great energetic expense of parental feeding has been favored evolutionarily, it is reasonable to propose that the lesser cost of thermogenesis could be favored for the same reproductive benefit. For example, thermoregulation is expensive for house mice because they are small (26‐44 g), but thermoregulatory costs are not nearly as large as the cost of feeding offspring. When living at 21C, house mice consume approximately 25-fold more food than lava lizards of similar mass living in the field (82.92 and 3.37 kJ d 1 , respectively);

Did lungs and the intracardiac shunt evolve to oxygenate the heart in vertebrates

Traditional wisdom of the evolution of lungs in fishes is that lungs arose when gill ventilation was hindered by an aquatic habitat that was low in oxygen. This scenario has been buttressed primarily by a proposed correlation between extant air-breathing fishes and hypoxic habitats, as well as by the fact that early vertebrate fossils were found in sediments believed to indicate a semi-arid environment. There are problems with this scenario, yet it retains a dominant influence on how the evolution of aerial respiration is viewed. This paper presents a new hypothesis for lung evolution that is more consistent with the fossil record and physiology of extant animals than the traditional scenario; I propose that lungs evolved to supply the heart with oxygen. The primitive vertebrate heart was spongy in architecture and devoid of coronary support, obtaining oxygen from luminal blood. By supplying oxygen to this tissue, lungs may have been important in ancient fishes for sustaining activity, regardless of environment. Furthermore, this function for lungs may have influenced cardiovascular adaptations of tetrapods because their divided cardiovascular system isolates the right side of the heart from pulmonary oxygen. I propose that three innovations compensate for this isolation: In extant amphibians oxygen-rich blood from cutaneous and buccal respiration enters the right side of the heart; in chelonians and lepidosaurs the intracardiac shunt washes oxygen-rich blood into the right side of the heart; in mammals, birds, and perhaps in crocodilians, support of the heart by coronary vasculature eliminates this problem.

On the origin of avian air sacs.

For many vertebrates the lung is the largest and lightest organ in the body cavity and for these reasons can greatly affect an organisms shape, density, and its distribution of mass; characters that are important to locomotion. In this paper non-respiratory functions of the lung are considered along with data on the respiratory capacities and gas exchange abilities of birds and crocodilians to infer the evolutionary history of the respiratory systems of dinosaurs, including birds. From a quadrupedal ancestry theropod dinosaurs evolved a bipedal posture. Bipedalism is an impressive balancing act, especially for tall animals with massive heads. During this transition selection for good balance and agility may have helped shape pulmonary morphology. Respiratory adaptations arising for bipedalism are suggested to include a reduction in costal ventilation and the use of cuirassal ventilation with a caudad expansion of the lung into the dorsal abdominal cavity. The evolution of volant animals from bipeds required yet again a major reorganization in body form. With this transition avian air sacs may have been favored because they enhanced balance and agility in flight. Finally, I propose that these hypotheses can be tested by examining the importance of the air sacs to balance and agility in extant animals and that these data will enhance our understanding of the evolution of the respiratory system in archosaurs.

The Right‐to‐Left Shunt of Crocodilians Serves Digestion

All amniotes except birds and mammals have the ability to shunt blood past the lungs, but the physiological function of this ability is poorly understood. We studied the role of the shunt in digestion in juvenile American alligators in the following ways. First, we characterized the shunt in fasting and postprandial animals and found that blood was shunted past the lungs during digestion. Second, we disabled the shunt by surgically sealing the left aortic orifice in one group of animals, and we performed a sham surgery in another. We then compared postprandial rates of gastric acid secretion at body temperatures of 19° and 27°C and rates of digestion of bone at 27°C. Twelve hours after eating, maximal rates of gastric acid secretion when measured at 19° and 27°C were significantly less in the disabled group than in sham‐operated animals. Twenty‐four hours postprandial, a significant decrease was found at 27°C but not at 19°C. For the first half of digestion, dissolution of cortical bone was significantly slower in the disabled animals. These data suggest the right‐to‐left shunt serves to retain carbon dioxide in the body so that it can be used by the gastrointestinal system. We hypothesize that the foramen of Panizza functions to enrich with oxygen blood that is destined for the gastrointestinal system to power proton pumps and other energy‐demanding processes of digestion and that the right‐to‐left shunt serves to provide carbon dioxide to gastrointestinal organs besides the stomach, such as the pancreas, spleen, upper small intestine, and liver.

Unidirectional pulmonary airflow patterns in the savannah monitor lizard

The unidirectional airflow patterns in the lungs of birds have long been considered a unique and specialized trait associated with the oxygen demands of flying, their endothermic metabolism and unusual pulmonary architecture. However, the discovery of similar flow patterns in the lungs of crocodilians indicates that this character is probably ancestral for all archosaurs—the group that includes extant birds and crocodilians as well as their extinct relatives, such as pterosaurs and dinosaurs. Unidirectional flow in birds results from aerodynamic valves, rather than from sphincters or other physical mechanisms, and similar aerodynamic valves seem to be present in crocodilians. The anatomical and developmental similarities in the primary and secondary bronchi of birds and crocodilians suggest that these structures and airflow patterns may be homologous. The origin of this pattern is at least as old as the split between crocodilians and birds, which occurred in the Triassic period. Alternatively, this pattern of flow may be even older; this hypothesis can be tested by investigating patterns of airflow in members of the outgroup to birds and crocodilians, the Lepidosauromorpha (tuatara, lizards and snakes). Here we demonstrate region-specific unidirectional airflow in the lungs of the savannah monitor lizard (Varanus exanthematicus). The presence of unidirectional flow in the lungs of V. exanthematicus thus gives rise to two possible evolutionary scenarios: either unidirectional airflow evolved independently in archosaurs and monitor lizards, or these flow patterns are homologous in archosaurs and V. exanthematicus, having evolved only once in ancestral diapsids (the clade encompassing snakes, lizards, crocodilians and birds). If unidirectional airflow is plesiomorphic for Diapsida, this respiratory character can be reconstructed for extinct diapsids, and evolved in a small ectothermic tetrapod during the Palaeozoic era at least a hundred million years before the origin of birds.

Pulmonary anatomy in the Nile crocodile and the evolution of unidirectional airflow in Archosauria

The lungs of birds have long been known to move air in only one direction during both inspiration and expiration through most of the tubular gas-exchanging bronchi (parabronchi). Recently a similar pattern of airflow has been observed in American alligators, a sister taxon to birds. The pattern of flow appears to be due to the arrangement of the primary and secondary bronchi, which, via their branching angles, generate inspiratory and expiratory aerodynamic valves. Both the anatomical similarity of the avian and alligator lung and the similarity in the patterns of airflow raise the possibility that these features are plesiomorphic for Archosauria and therefore did not evolve in response to selection for flapping flight or an endothermic metabolism, as has been generally assumed. To further test the hypothesis that unidirectional airflow is ancestral for Archosauria, we measured airflow in the lungs of the Nile crocodile (Crocodylus niloticus). As in birds and alligators, air flows cranially to caudally in the cervical ventral bronchus, and caudally to cranially in the dorsobronchi in the lungs of Nile crocodiles. We also visualized the gross anatomy of the primary, secondary and tertiary pulmonary bronchi of C. niloticus using computed tomography (CT) and microCT. The cervical ventral bronchus, cranial dorsobronchi and cranial medial bronchi display similar characteristics to their proposed homologues in the alligator, while there is considerable variation in the tertiary and caudal group bronchi. Our data indicate that the aspects of the crocodilian bronchial tree that maintain the aerodynamic valves and thus generate unidirectional airflow, are ancestral for Archosauria.

Structure and function of the esophagus of the American alligator (Alligator mississippiensis)

SUMMARY Esophageal structure and function were studied in juvenile American alligators (Alligator mississippiensis). The anatomy of alligators differs from humans in several important aspects: the crocodilian esophagus is more muscular and is composed entirely of smooth muscle. Functionally, the crocodilian esophagus is similar to that of mammals, but alligators have peak esophageal peristaltic pressures that are 2–3-fold greater than pressures in the human esophagus. As is found in humans, the incidence of esophageal reflux increased in postprandial animals compared with the fasting state. We observed a large increase in pressure in the lower esophageal sphincter (LES) during ventilation that ranged from 200% to 3000% of the pressures measured during apnea. These pressure changes appear to be intrinsic to the LES. Alligators lack a mammalian-type diaphragm; thus, there is no crural diaphragmatic contribution to LES pressure. These features recommend the alligator as a useful model for the study of regulation of the LES.

New insight into the evolution of the vertebrate respiratory system and the discovery of unidirectional airflow in iguana lungs

Significance The avian respiratory system appears strikingly distinct from all other animals. Purported key innovations underpinning avian patterns of airflow are an enclosed intrapulmonary bronchus, intercameral perforations, heterogeneous parenchyma; these traits allegedly coevolved with separation of the cardiac ventricle into right and left sides and are presumed to have been favored by selection because they facilitate high activity metabolisms. In contradistinction to these prevailing theories, here we show that unidirectional flow is present in the lungs of the green iguana, an ectothermic animal with low aerobic capacity, no intrapulmonary bronchus, and no intercameral perforations. This discovery indicates a transformation in our understanding of the evolution of the vertebrate respiratory system is needed. The generally accepted framework for the evolution of a key feature of the avian respiratory system, unidirectional airflow, is that it is an adaptation for efficiency of gas exchange and expanded aerobic capacities, and therefore it has historically been viewed as important to the ability of birds to fly and to maintain an endothermic metabolism. This pattern of flow has been presumed to arise from specific features of the respiratory system, such as an enclosed intrapulmonary bronchus and parabronchi. Here we show unidirectional airflow in the green iguana, a lizard with a strikingly different natural history from that of birds and lacking these anatomical features. This discovery indicates a paradigm shift is needed. The selective drivers of the trait, its date of origin, and the fundamental aerodynamic mechanisms by which unidirectional flow arises must be reassessed to be congruent with the natural history of this lineage. Unidirectional flow may serve functions other than expanded aerobic capacity; it may have been present in the ancestral diapsid; and it can occur in structurally simple lungs.