by Peter Ward
Septate lungs are not elastic and thus do not naturally contract in size following inhalation. Lung ventilation also varies across groups with the septate lung. Lizards and snakes use rib movement to draw air in, but as we have seen, locomotion in lizards inhibits complete expansion of the lung cavity, and thus lizards do not breathe while moving.
The variety of modifications of the septate lung makes this system more diverse than the alveolar system. For instance, crocodiles have both a septate lung and a diaphragm—an organ not found in the snakes, lizards, or birds. But the crocodile diaphragm is also somewhat different from that in mammals: it is not muscular, but is attached to the liver, and movement of this liver-diaphragm acts like a piston to inflate the lungs, with muscles attaching to the pelvis. The mammalian (including human) diaphragm pulls the liver in just the same way a crocodilian one does, creating a visceral piston, but the way this is accomplished differs in crocs and mammals.
Until recently, the septate lungs of crocodile and alligator lungs were considered relatively primitive and therefore inefficient. But a radical new finding not only makes us reassess the respiratory ability of the extant forms, but also puts an entirely new view on the reptilian success across the Permian extinction and in the Triassic.
The most inefficient way to breathe is the mammalian way: inhalation and exhalation through the same tube into the lungs. The inefficiency comes from the disorder of the gas molecules as one exhalation finishes and one inhalation starts. In any sort of more rapid breathing, there is a chaotic collision of exhaled air trying to get out before inhalation begins—and quite often the same gas molecules, including volumes of air with more CO2 and less O2, are sucked back in. It has long been thought that the crocs have this problem as well. But a study in 2010 showed that in fact the crocodilians use a separate one-way path that is similar to that in birds and dinosaurs. The revelation is that the ancient Permian- and Triassic-aged stem reptiles, the groups ultimately giving rise to the modern crocodiles and birds, and to the extinct dinosaurs, were also more efficient in their breathing than their therapsid (protomammal) contemporaries. They went through the filter of the Permian extinction with two great competitive advantages; they were cold-blooded, and they could extract more oxygen out of the air than a mammal or mammal-like reptile. The deck was stacked against us mammals. We never really had a chance in this most consequential competition for not only survivability but for eventual dominance amid the crisis and chaos of mass extinction. The mammals of the Mesozoic eventually would rarely be larger than rats. Probably highly fearful as rats are as well, surrounded by dinosaurs.
THE AVIAN AIR-SAC SYSTEM
The last kind of lung found in terrestrial vertebrates is a variant on the septate lung. The best example of this kind of lung and its associated respiratory system is found in all birds. The lungs themselves in this system are small and somewhat rigid. Thus bird lungs do not greatly expand and contract as ours do on each breath. But the rib cage is very much involved in respiration, and especially those ribs closest to the pelvic region are very mobile in their connection to the bottom of the sternum, and this mobility is quite important in allowing respiration. But these are not the biggest differences. Very much unlike extant reptiles and mammals, these lungs have appendages added to them known as air sacs, and the resultant system of respiration is highly efficient. Here is why. We mammals (and all other nonavians as well) bring air into our dead-end lungs and then exhale it. Birds have a very different system.
When a bird inspires air, the air goes first into the series of air sacs. It then passes into the lung tissue proper, but in so doing the air passes but one way over the lung, since it is not coming down a trachea but from the attached air sacs. Exhaled air then passes out of the lungs. The one-way flow of air across the lung membranes allows a countercurrent system to be set up: the air passes one direction, and blood in the blood vessels within the lungs passes in the opposite direction. This countercurrent exchange allows for more efficient oxygen extraction and carbon dioxide venting than are possible in dead-end lungs.
Anatomists have been dissecting and describing birds for centuries. It thus seems odd that an accurate understanding of bird air-sac anatomy did not occur until 2005. Two bird anatomists, Patrick O’Connor and Leon Claessens, injected substantial quantities of fast-jelling plastic into the respiratory systems of many different birds and then carefully dissected the corpses and described the anatomy of the filled cavities, the now plastic-filled air sacs.4 To their surprise, they found that avian air sacs are much more voluminous and complicated than anyone had suspected. For the first time, the real relationship of air sac to bone in pneumatized bone—bones with large cavities in them—could be observed. In the same paper the two authors then compared the anatomy of pneumatized bird bones to pneumatized dinosaur bones. The similarity was remarkable, for there were the same shapes of holes in the same (or homologous) bones.
Those arguing that there was no air-sac system in dinosaurs have not denied that the dinosaur bones had holes in them. They said that the holes were there, all right, but that they were adaptations simply for lightening the bones. But there comes a point when arguing that the similarity is simply coincidence in shape collapses under the weight of too great a coincidence.
In the diagram on page 258, the various air sacs are shown with their communication to the lungs. It is clear that the volume of air sacs far exceeds the volume of the lungs themselves. The air sacs are not involved in removing oxygen; they are an adaptation that allows the countercurrent system to work. There is no question that the greater efficiency of this system compared to all other lungs in vertebrates is related to the two-cycle, countercurrent system produced by the air-sac lung anatomy in birds.
By 2005, the evidence that many dinosaurs had air sacs was overwhelming. Until then, one group of anatomists had vigorously argued that dinosaur lungs were no different than modern crocodile lungs, just large, and that the avian lung,5 with its many auxiliary air sacs as well as a one-way airflow, did not appear until the Cretaceous, some 100 million years ago—and then was found only in birds! That view no longer became tenable. But in 2005 there was still no appreciation of the degree to which atmospheric oxygen levels had changed in the Early Mesozoic, or that such changes might have had any influence at all on the evolution of these various respiratory systems.
The air-sac system is better than the mammalian system. It has been estimated that a bird is 33 percent more efficient in extracting oxygen from air than a mammal at sea level. But at higher altitude this differential increases: a bird at five thousand feet in altitude may be 200 percent more efficient at extracting oxygen than a mammal. This gives the birds a huge advantage over mammals and reptiles living at altitude. And if such a system were present deep in the past, when oxygen even at sea level was lower than we find today at five thousand feet, surely such a design would have been advantageous, perhaps enormously so, to the group that had it in competing or preying on groups that did not.
We know that birds evolved from small bipedal dinosaurs that were of the same lineage as the earliest dinosaurs, a group called saurischians. The first bird skeletons come from the Jurassic (although there is now some controversy about just how “birdlike” the earliest species, such as the famous Archaeopteryx, really were, and we will return to this). But the air sacs attached to bird lungs are soft tissue, and would fossilize only under the most unusual circumstances of preservation. Thus we do not have direct evidence for when the air-sac system came about. But we do have indirect evidence, enough to have stimulated the air-sac-in-dinosaurs group to posit that all saurischian dinosaurs had the same air-sac system, as do modern birds. And like birds they were also warm-blooded. The evidence comes from holes in bones, places where these air sacs may have rested.
All credit for the first to make the audacious suggestion that dinosaurs had a bird launch system goes to Robert Bakker. It had been known since the late 1800s that some dinosaur bones had curious hollow
s in them, just as bird bones do. For decades this discovery was either forgotten or attributed to an adaptation for lightening the massive bones, for many of these bones with holes, later called pneumatic bones, came from the largest land animals of all time, the giant sauropods of the Jurassic and Cretaceous. The pneumatic bones were found mainly in vertebrae. Birds have similar pneumatic vertebrae, and while it can be said that some of the bird bones were light to enhance flying, it was also clear that some of the air sacs attached to bird lungs rested in hollows in bones. Thus, in birds, bone pneumaticity was an adaptation for stashing away the otherwise space-taking air sacs. The bodies of animals are filled with necessary organs, and putting the air sacs in hollowed-out bones make a lot of evolutionary sense. But Bakker made the leap and suggested that the pneumatic bones in his beloved fossil sauropods had evolved for a similar purpose, and were direct evidence that sauropods had and used the air-sac system.
Bakker’s larger purpose was to try to add further evidence that dinosaurs were warm-blooded rather than make any claim about this being an adaptation to low oxygen. Birds, with their enormous energy and oxygen demands related to flying, were thought to have evolved the air-sac system as a way of satisfying the metabolic demands of their endothermy.
Following Bakker, other dinosaur workers took up the call, and the specific case of air sacs being present in sauropods was made by paleontologist and dinosaur specialist Matt Wedel in 2003, while similar arguments for bipedal species were made at about the same time by dinosaur specialist Greg Paul. In 2002 he suggested that the first of the so-called archosaurs, the primitive late Permian through early Triassic reptilian group (that we have called archosauromorphs), which would eventually give rise to crocodiles, dinosaurs, and birds, had air sacs. Examples of this group, which included the quadruped form Proterosuchus (described above as one of the earliest Triassic archosaurs), would have had a reptilian septate lung. Inspiration may have been aided by a primitive abdominal pump-diaphragm system (more primitive, perhaps, than this system as found today in modern crocodiles). What was unknown at the time, however, was that the crocodiles and their ilk back then had a far better respiratory system than was then agreed upon, thanks to their innovation of making air move one way through the respiratory system.
This discovery did not take place until 2010, and certainly affects our view of the relative evolutionary fitness of crocodiles, dinosaurs, and mammals. In fact, all of the Triassic reptiles seemed to have been better “breathers” than we mammals.
Successively, however, the evolution of the air-sac system may have fairly rapidly progressed in the lineage leading to dinosaurs at least. Alas (for them, anyway), the crocodiles ceased major innovation to their respiratory system with the newly evolved flow-through anatomy; they never experimented with pneumaticity in bones, and air sacs.
By the time the first true dinosaur is seen in the Middle Triassic, there may have been part of the air-sac system in place. The most primitive theropods from this time (the first dinosaurs) do not show bone pneumatization; the lung itself may have become inflexible and relatively smaller, both characteristics of extant bird lungs. With the Jurassic forms such as Allosaurus, the air-sac system may have been essentially complete but still much different from the bird system, modified as it has been for flying (for even the modern-day flightless birds came from fliers in the deep past) with large thoracic and abdominal air sacs.
By the time Archaeopteryx had evolved in the middle part of the Jurassic, there may have been a great diversity of respiratory types among the dinosaurs, some with pneumatized bones and some without. There also may have been a great deal of convergent evolution going on. For instance, the extensive pneumatization in the large sauropods studied with such care by Wedel may have arisen somewhat independently from the system found in the bipedal saurischians.
A final note about air sacs: While universal in saurischian dinosaurs, there is still no evidence of air sacs in the other giant dinosaur group, the ornithischian dinosaurs, including the well-known duckbills, iguanodons, and horned ceratopsian dinosaurs—not coincidentally (for three groups) all from the Cretaceous, not the Jurassic. The lack of an air-sac system in this group meshes well with their distribution in time. During the Jurassic times of very low oxygen they were minor elements of the fauna. It was not until the great oxygen rise of the Late Jurassic through the Cretaceous that this second great group of dinosaurs became common.
Perhaps the earliest dinosaurs were something like lions: sleeping twenty hours a day to conserve energy as dictated by the low oxygen, but when hunting, doing so actively, more actively than any of their competitors, which would have included the nondinosaur archosaurs (such as the early crocodiles), the cynodonts, and the first true mammals. All they needed to be was better than the rest. All evidence suggests that they were.
Metabolic complexes may have been far more diverse than our simple subdivision into endothermy and ectothermy. While modern birds, reptiles, and mammals are put into one of these two categories, there are, in fact, many kinds of organisms that can generate heat in their bodies without external heat sources. These include large flying insects, some fish, large snakes, and large lizards. Such animals are endotherms, but not in the mammalian or avian sense. There may have been many kinds of metabolism in the great variety of dinosaurs that existed.
Dinosaurs were not alone on the Jurassic stage, for our own ancestors were present, at very small size, as were other land animals and sea animals, including turtles on land and in the sea, as well as long-necked plesiosaurs and crocodiles. But the dinosaurs were certainly dominant on land. While at first it seems that there were many, many kinds of dinosaur body shapes, in fact there were really but three. All three shared a common characteristic with birds and mammals: a fully upright posture. The three kinds of dinosaurs were bipeds, short-necked quadrupeds, and long-necked quadrupeds. Each had a different time of origin and time of maximum abundance. Five distinct and successive assemblages of dinosaurian “morphotypes” (body plans) seem apparent to us. They are as follows:
1. Late Triassic. The earliest dinosaurs appeared in the last third of the Triassic but remained for their first 15 million years at low diversity. The majority of forms were bipedal, carnivorous saurischians. Toward the end of the period, quadrupedal saurischians (sauropods) evolved. Ornithischians diverged from the saurischians before the end of the Triassic but made up a very small percentage of dinosaur species and individuals. For much of the Triassic, dinosaur size is small, from one to three meters, and the earliest ornithischians (such as Pisanosaurus) were meter-long bipeds that had a new jaw system specialized for slicing plants. In the latest Triassic the first substantial radiation of dinosaurs occurs. It takes place among saurischians, with the evolution of both more and larger bipedal carnivores, and the first gigantism among early sauropods (such as Plateosaurus of the Late Triassic).
2. Early to mid Jurassic. Saurischian bipeds and long-necked quadrupeds dominated faunas. During this time, however, the ornithischians, while remaining small in size and few in number, diversify into the major stocks that will ultimately dominate dinosaur diversity in the Cretaceous. These stocks include the appearance of heavily armored forms (such as the thyreophorans). These are quadrupeds, and include the first stegosaurs of the middle part of the Jurassic. A second group is the unarmored neornischians (which include ornithopods—hypsilophodontids, iguanodons, and duckbills—and marginocephalians—the ceratopsians, which do not appear until the Cretaceous—and bone-headed pachycephalans). But it is the sauropods that are most evident in numbers. They split into two groups in the latest Triassic, the prosauropods and true sauropods, and in the early and middle Jurassic the prosauropods were far more diverse than sauropods, but went extinct in middle Jurassic time, leading to a vast radiation of sauropods into the Late Jurassic.
The bipedal saurischians also showed diversity and success in the early and middle Jurassic. In latest Triassic time they had split into two groups (the ceratos
aurs and tetanurans). The ceratosaurs dominated the early Jurassic, but by middle Jurassic time the tetanurans increased in number at the expense of the ceratosaurs. They too split in two, the two groups being the ceratosauroids and the coelophysids. The latter group eventually produced the most famous dinosaur of all: the late Cretaceous Tyrannosaurus rex, although its middle Jurassic members were considerably smaller. Their most important development in the Jurassic was the evolution of the stock that gave rise to birds.
3. Late Jurassic. This was the time of the giants. The largest sauropods come from late Jurassic rocks, and their dominance continues into the early part of the Cretaceous. Keeping pace with this large size were the saurischian carnivores, with giants such as Allosaurus typical. Thus the most notable aspect of this interval was the appearance of sizes far larger than in the early and middle Jurassic. And this was not only among the saurischians. During the late Jurassic the armored ornithischians also increased in size, most notably among the heavily armored stegosaurs. The diversification of ornithischians at this time with the appearance of stegosaurs, ankylosaurs, nodosaurs, camptosaurs, and hypsilophontids radically changes the complexion of the dinosaur assemblages.
4. Early to middle Cretaceous. While the dominants for the early part of this interval remained large sauropods, as the Cretaceous progressed a major shift occurred: ornithischians increased in diversity and abundance until they outnumbered saurischians. Sauropods become increasingly rare as many sauropod genera go extinct at the end of the Jurassic.
