7
THE PERMIAN EXTINCTION AND THE EVOLUTION OF ENDOTHERMY

As the Paleozoic came to a close during the Permian Period, the continents all joined into one large landmass and then, some 250 million years ago, an enormous and devastating mass extinction swept land and sea alike. Estimates vary but a figure of 90 percent of all species on the planet is seen as a reliable estimate of the damage done to world species’ diversity. The event is the Permian extinction. (It has been given a number of more flamboyant sobriquets: The Great Dying, The Mother of All Extinctions, The Day that Life Almost Died.) Prominent victims in the sea included the majority of brachiopods, all trilobites, all reef-building cnidarians, most crinoids, most bryozoans, many mollusks including the majority of ammonoids, and many fish stocks. On land the extinction was equally devastating, causing great reductions in all stocks of plants and animals. The recovery interval for this extinction was long, and survivors inherited an emptied world.

The cause of the extinction remains one of the most vexing and, to many scientists, a still unsolved geological mystery. Controversy thrives as many different hypotheses compete regarding cause. Not all of them can be correct for some are mutually exclusive. What is not contested is the effect that this paramount extinction event had on the history of life. This chapter looks at both topics—the Permian extinction’s real cause and, more importantly, its real effect.



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Out of Thin Air: Dinosaurs, Birds, and Earth’s Ancient Atmosphere 7 THE PERMIAN EXTINCTION AND THE EVOLUTION OF ENDOTHERMY As the Paleozoic came to a close during the Permian Period, the continents all joined into one large landmass and then, some 250 million years ago, an enormous and devastating mass extinction swept land and sea alike. Estimates vary but a figure of 90 percent of all species on the planet is seen as a reliable estimate of the damage done to world species’ diversity. The event is the Permian extinction. (It has been given a number of more flamboyant sobriquets: The Great Dying, The Mother of All Extinctions, The Day that Life Almost Died.) Prominent victims in the sea included the majority of brachiopods, all trilobites, all reef-building cnidarians, most crinoids, most bryozoans, many mollusks including the majority of ammonoids, and many fish stocks. On land the extinction was equally devastating, causing great reductions in all stocks of plants and animals. The recovery interval for this extinction was long, and survivors inherited an emptied world. The cause of the extinction remains one of the most vexing and, to many scientists, a still unsolved geological mystery. Controversy thrives as many different hypotheses compete regarding cause. Not all of them can be correct for some are mutually exclusive. What is not contested is the effect that this paramount extinction event had on the history of life. This chapter looks at both topics—the Permian extinction’s real cause and, more importantly, its real effect.

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Out of Thin Air: Dinosaurs, Birds, and Earth’s Ancient Atmosphere WHAT HAPPENED? The Permian extinction came during the greatest relative drop in oxygen (and was also accompanied by a shorter-term rise in atmospheric carbon dioxide, one of the largest in Earth’s history). Both of these events took place amid the amalgamation of the largest continental landmass and the greatest volcanic event (the flood basalt eruptions left lava fields the size of Alaska). Are all of these things coincidental? That it was catastrophic is undeniable. It is certainly portrayed as the most catastrophic of the five largest mass extinctions of the past 600 million years by virtually every measure by which extinctions are compared: the percent of the fauna dying out and the effect it had on the nature of the planet’s biota. The study of this mass extinction is ongoing. New work on Permian and Triassic strata in the Karoo of South Africa was instigated by the possibility that meteor impact was indeed the primary or contributing cause. Yet in spite of searching for impact, no evidence for impact has been discovered. Major atmospheric and oceanic oxygen-level changes coupled with global warming remain a hypothesis favored here. We will look at how those twin effects radically changed the nature of life on Earth. First, though, let’s go back to a time some 251 million years ago, in the midst of the great Permian extinction. A voyage 251 million years ago would put us at the very end of the Permian Period. Even at the poles there is no ice. The world is hot and desert-like. There is little plant life, so little, in fact, that soil erosion has caused great dune fields of sand to form. The river systems look like those we saw in our Cambrian voyage where there were no meandering rivers, only ephemeral braided streams—the kind of sheetwash and streamflow that today is found at the bottom of glaciers of alluvial fans—places without vegetation, for it is the roots of plants that allow rivers to have bank stability, which is required for meandering rivers. This place is akin to the time before land plants. Harsh, hot winds, filled with grit, only make the atmosphere seem hotter. And hot it is—a place of high carbon dioxide and low oxygen. And it reeks of rotten eggs. Great bubbles of hydrogen sulfide are periodically emerging from the sea and larger lakes, for we will find that both of these are filled with bacteria producing this deadly gas.

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Out of Thin Air: Dinosaurs, Birds, and Earth’s Ancient Atmosphere We look closer at the terrestrial world. Where there are copses of vegetation near ponds and water there are herds of the dicynodont Lystrosaurus. They are stolid and lamb-sized, even as adults, but nevertheless are the largest animals on the planet. They are not very active, and all are living at sea level. Almost motionless, they slowly graze on the low vegetation; moving about leaves them breathless. Two kinds of small carnivores harass their young—the small cynodonts, looking much like strange primitive dogs, and graceful, low-slung but active diapsids known as Proterosuchus. They are ambush predators, for the stalking of prey requires locomotion, and while both are capable of rapid bursts of movement to bring down prey, the low oxygen quickly puts them in respiratory debt. What is striking is that other than these few inhabitants there is little else, and the lack of diversity is perhaps the most striking aspect of this world. A paltry few members of the once common dicynodonts such as Dicynodon dodder about, and there is still a last predatory gorgonopsian or two, but these are the last relics of lineages headed to complete extinction. Even insects are rare here and of few varieties, for their kind suffered great losses in the extinction that by this time has been a succession of paroxysms over several million years, and there has still not been an evolutionary burst of new forms. The heat and low oxygen have not relented; in fact, they continue to trend unfavorably. The oxygen content now is even lower than Reconstruction of a gorgonopsian, the largest late Permian predator and also a victim of the Permian extinction. The largest of these top carnivores would have reached 10 feet in length.

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Out of Thin Air: Dinosaurs, Birds, and Earth’s Ancient Atmosphere Reconstructions of a spiny nautiloid cephalopod, left, and crinoid (echinoderm), right, examples of two groups that nearly ended with the Permian extinction. Only a few species of these and most other animals then on Earth survived to seed the ensuing Triassic period. it was 500 million years ago. Things have only gotten worse—and will stay that way for several million years yet. The sight of the ocean is a shock. It is not blue, but a deep purple in color. The surface regions are cloudy with untold numbers of purple and green bacteria, which reflect the presence of larger quantities of the toxic gas hydrogen sulfide than the low-oxygen water can neutralize through oxidation. Oceans and lakes release the surplus hydrogen sulfide gas and thus poison the land organisms. We move into the sea, and here too the world is reminiscent of the time before animals in many ways. The seabed is covered with widespread stromatolites, the layers of bacteria and trapped sediment that were the main kind of earth life from the period of 3.5 billion to 600 million years ago. The rise of animals in the Cambrian Explosion had seemingly put an end to this formerly common kind of life, since the evolution of grazing invertebrates such as limpets and other snails literally ate this kind of life out of existence. But the herbivorous invertebrates have suffered terrible losses in this Permian extinction, and now the stromatolites have been given new reign once more over the bodies of the newly dead. There are different kinds of survivors among the

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Out of Thin Air: Dinosaurs, Birds, and Earth’s Ancient Atmosphere fish and cephalopods, but there are no coral reefs, or trilobites, or most of the echinoderms that were hallmarks of the Paleozoic. Some brachiopods are left, including large numbers of the very primitive lingulids, and there seem to be a number of small flat clams among them. But like the land, the most striking impression is how few in number the various kinds of life are. THE GREATEST OXYGEN CRASH The two major changes in atmospheric content that seem to have driven the Permian extinction were the rapid drop in oxygen and the rapid rise in carbon dioxide. The interval from about 270 to 200 million years ago was exceedingly interesting. It is evident that carbon dioxide had been as low as it is now for some millions of years prior to the Permian extinction—low enough that it may have greatly impacted the nature of the flora. Our current levels of about 350 to 400 ppm carbon dioxide have been present for perhaps 20 million years, and a major finding of the past decade was the realization that this relatively low level compared to prior times in Earth’s history stimulated the evolution of a new photosynthetic pathway. This new kind of photosynthesis, called the C4 pathway, is found in many grasses on our planet. As far as is known, C4 plants did not exist in the Permian and thus the drop of carbon dioxide greatly affected plant life, as shown by the presence of a plant extinction at the time of minimal carbon dioxide levels, at about 305 million years ago. Paleobotanists recognize a mass extinction among plants at this time, with about two-thirds of all plant species known from coal seams going extinct (where, typically, 40-50 distinct plant species can be recovered). While most authors blame this extinction on a drying of the many coal swamps at this time, it seems as likely that the extinction was at least partially caused by the carbon dioxide minimum. The low levels of carbon dioxide certainly affected global temperatures, precipitating, as we have seen, perhaps the most extensive glaciation of the last 500 million years. The rapid rise of carbon dioxide certainly seems to have coincided with the Permian extinction and brought about rapidly warming conditions on Earth.

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Out of Thin Air: Dinosaurs, Birds, and Earth’s Ancient Atmosphere The rise in carbon dioxide was certainly dramatic. But it was utterly dwarfed by the fall in oxygen, which may have dropped by two-thirds from its high concentration maximum of as much as 35 percent in the early Permian, to perhaps as low as 12 percent in the early Triassic. The cause of the drop is agreed upon: carbon-rich material was no longer buried at the rates it had been in the late Carboniferous and early Permian. At the same time, the burial rate of pyrite-bearing sediment also dropped dramatically. With huge quantities of reduced carbon exposed to the atmosphere, oxidation set in, removing oxygen molecules from the air. But why did this happen? The ultimate cause seems to be related to two events. First, the formation of the supercontinent Pangea was completed about the same time that the oxygen drop occurred. As the continents fused together, many of the sedimentary basins and swamps that had been the site of the rapid and profound burial of plant material that caused the rise of oxygen to the maxima of the Carboniferous-early Permian event were uplifted and thus could no longer serve as traps and reservoirs of reduced carbon. Second, the drop in carbon dioxide that culminated about 300 million years ago may have drastically reduced the amount of plant material through mass extinction of species, which in turn caused a significant reduction of plant biomass. There was less plant life to be deposited, and both of these events conspired to cause the oxygen crash. POSSIBLE CAUSES What is called the Permian extinction is really a series of extinctions, beginning at the end of the Guadaloupian Stage of the Permian Period (about 254 million years ago), with a second and far more severe pulse at the Permian-Triassic boundary itself, dated at about 251 million years ago. This “double extinction” at the end of the Permian has been known for about a decade or more. But now we are finding that even between these larger events there were smaller extinction episodes as well. What caused this pattern? The episode at 251 million years ago is one of the most controversial subjects in modern geological research. There are several scenarios in the controversy, and they are listed below in arbitrary order:

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Out of Thin Air: Dinosaurs, Birds, and Earth’s Ancient Atmosphere The mass extinction was caused by a large-body impact with Earth. Of the many competing hypotheses, the most interesting and controversial is that it was caused by the effects of a large-body impact on Earth some 251 million years ago. This idea is relatively new. The first paper suggesting this cause appeared only after the turn of the millennium, in 2001. This is the most “journalist friendly” of the various scenarios and is a scientific descendant of the Alvarez Impact Hypothesis of 1980, which had been formulated for the end-Cretaceous catastrophe. The major proponents of impact as the cause of the Permian extinction are Luann Becker of the University of California at Santa Barbara and Robert Poreda of the State University of New York, who in the first part of this century announced that “Bucky Balls” claimed to have been found at Permian-Triassic boundaries at several locales around the globe are evidence of large-body impact some 251 million years ago. About a year after this initial report, which was published in the prestigious journal Science and accompanied by worldwide publicity, they announced that they had found the crater as well, a structure named Bedout located near Australia. At that time newly published data on the extinction pattern of marine invertebrates from a stratigraphic section in China indicated that the die-off was sudden and thus consistent with and reminiscent of the pattern of extinction found at the younger Cretaceous-Tertiary boundary sites. But here the historical parallel between the initial Alvarez discovery and subsequent work markedly diverges with what happened following the Becker et al. announcement. In the case of the Cretaceous work, scientists studying stratigraphic sections at many places around the world found the same evidence that the Alvarez group found: the presence of elevated levels of iridium, the presence of glass spherules and the presence of quartz grains marked by shock lamella. All of these are consistent with impact. But the Becker group’s announcement was not followed by paper after paper corroborating their work. No significant iridium was found, no glassy spherules, and a report of shocked quarts (which is consistent with a meteor impact) was later retracted by its author, Greg Retallack of the University of Oregon. The Bucky Ball story was difficult to corroborate as well, as the protocol that isolates these large carbon lattices is not easily done. The

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Out of Thin Air: Dinosaurs, Birds, and Earth’s Ancient Atmosphere one attempt to replicate Becker’s results failed to show any evidence of impact. By 2005 the public and science journalists were the major supporters of the Becker hypothesis, while the working stiff scientists objected—some harshly, which was a response to the tenor of the Becker group and their dogmatic belief in their findings. Carbon dioxide catastrophe. This idea, put forth in the late 1990s by Harvard University’s Andy Knoll and his colleagues, advocated a rapid and massive release of carbon dioxide that was previously locked up in deep-water Permian sediments. Carbon dioxide poisoning, accompanied by high heat brought about by the greenhouse heating effect of the newly released carbon dioxide, was the proposed kill mechanism. This hypothesis, while attractive, was soon shot down by oceanographers who pointed out that the release of carbon dioxide necessary for this scenario was physically impossible. Methane catastrophe. This idea was largely the brainchild of the same Greg Retallack who had mistakenly reported the presence of shocked quartz grains from latest Permian rocks. Retallack noted that carbon isotope values found from most Permian-Triassic boundaries were isotopically so “light” that they could not have been caused by the extinction alone (if all plant life is killed off on a planet, the carbon isotope values go light). But the gas methane is “light,” and a massive release of the stuff would produce the observed isotopic signature. Methane is an even better greenhouse gas than carbon dioxide, so Retallack invoked a sudden heating. At the same time, Retallack suggested that the drop of oxygen already thought to have occurred over the time interval of the Permian extinction happened so fast that land animals died of asphyxia. But Bob Berner dismissed this idea of sudden oxygen drop on scientific grounds. And finally, isotope geochemists even began to question the methane idea, recovering many measures that did not yield the methane signature. They ascribed the very light findings to rocks whose carbon isotope values had been perturbed by later heating and pressure. Heat spike and low oxygen caused by Siberian traps. With the falsification of the methane idea, attention shifted to the simultaneity of the largest flood basalt of the past 600 million years, the Siberian traps, with the Permian extinction. Because the flow from Earth of

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Out of Thin Air: Dinosaurs, Birds, and Earth’s Ancient Atmosphere such lava is accompanied by a massive release of carbon dioxide into the atmosphere, it was hypothesized that a sudden spike in global temperatures was somehow involved in the extinction. The oxygen drop was also invoked but not the precipitous drop advocated by Retallack. Instead, the heat spike overlay a long-term drop in oxygen, which began long before the extrusion of the Siberian trap basalts. The extinction pattern under such a scenario would show long-term extinction due to the oxygen drop, followed by (and greatly exacerbated by) a sudden rise in global temperatures. This is the idea that I promoted in two papers published in Science in 2005. One showed the extinction pattern of mammal-like reptiles across the Permian boundary in South Africa, the second (published with Ray Huey of the University of Washington) invoked a loss of terrestrial habitat due to the drop in oxygen. As atmospheric oxygen dropped, even moderate altitudes would have had even lower-oxygen content. If oxygen dropped below about 12 percent (the value found by an early version of Berner’s GEOCARB modeling), the only place on Earth where terrestrial animals could live would be at sea-level. By using reconstructions of the Permian world, we then showed that sea-level elevations made up about 50 percent of the Permian land surface. Thus, half the land area would be unavailable for animal life, and the areas that were habitable would be cut off from other habitable areas by even modest altitude. The problem with this hypothesis was that while it readily explained the observed pattern of long-term, elevated extinction during the late Permian, the heat spike did not seem severe enough to cause the observed short-term bump in extinction rates at the boundary itself. The effects of a heat spike could be imagined but not modeled. Hydrogen sulfide poisoning. The final entry into the Permian extinction sweepstakes was put forward in 2004 by Lee Kump and colleagues at Pennsylvania State University, and is considered here to be the winner of the Permian extinction sweepstakes. Kump and his colleagues suggested that the long period of low oxygen seen both in models and by direct evidence in marine sediments themselves would have created conditions in the sea favoring the massive growth of hydrogen sulfide–releasing bacteria, which overwhelm the surface water’s oxygen supply and result in colorful bacterial blooms (hence the sugges-

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Out of Thin Air: Dinosaurs, Birds, and Earth’s Ancient Atmosphere tion of purple oceans). As anyone who has ever taken chemistry lab knows (or anyone who has had to smell rotten eggs in a closed area can attest), hydrogen sulfide is nasty stuff. Many humans have been killed by high concentrations of hydrogen sulfide found around natural gas wells, especially, coincidentally enough, around the town of Permian, Texas. This hypothesis is thus like the oxygen-drop heat-spike idea above but adds on the pulse of poisonous hydrogen sulfide entering the oceans and atmosphere as the kill mechanism at the boundary itself. As this book is being written, scientists are scrambling to confirm this intriguing proposal as an add-on to cause 4 above. As can be imagined, this new hypothesis is despised by the impact camp but is gaining favor among the rest of us working on the Permian extinction problem. Better than any of the other hypotheses, it explains the relatively sudden death at the Permian boundary, a spike of extinction overlaying a much longer-term interval of heightened species extinction. But we can improve on this. A NEW SCENARIO FOR THE PERMIAN EXTINCTION Here is how the Permian extinction might have occurred. First, it was caused by a succession of similar events, some smaller, some larger. The most damaging (to animals and plants) occurred 251 million years ago, but there were others both before and after, or from about 255 million to 248 million years ago. Each event began with heat from greenhouse gases rising into the atmosphere. At the same time, the warming ocean began to favor the growth of sulfur-metabolizing bacteria as oxygen levels dropped. If deep-water hydrogen sulfide concentrations increased beyond a critical threshold during oceanic anoxic intervals (times when the ocean bottom and perhaps even its surface regions lose oxygen), then the oceanic conditions (such as those in the modern Black Sea) separating sulfur-rich deep waters from oxygenated surface waters could have risen abruptly to the ocean surface. The horrific result would be great bubbles of highly poisonous hydrogen sulfide gas rising into the atmosphere. The amount of hydrogen sulfide gas entering the late Permian atmosphere would be more than 2,000 times greater than the small

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Out of Thin Air: Dinosaurs, Birds, and Earth’s Ancient Atmosphere modern flux (this is the toxic killer coming from volcanoes). Enough would have entered the atmosphere to most likely lead to toxic levels. Moreover, the ozone shield, that layer which protects life from dangerous levels of ultraviolet rays, also would have been destroyed. Indeed, there is evidence that this happened at the end of the Permian, for fossil spores from the extinction interval in Greenland sediments show evidence of the mutation expected from extended exposure to high ultraviolet fluxes attendant on the loss of the ozone layer. Today, we see various holes in the atmosphere, and under them, especially in the Antarctic, the biomass of phytoplankton rapidly decreases. If the base of the food chain is destroyed, it will not be long until the organisms higher up are perturbed as well. The complete loss of our ozone layer has even been invoked as a way to cause a mass extinction if Earth was hit by particles from a nearby supernova, which would also destroy the ozone layer. Finally, an abrupt increase in methane concentrations significantly amplifies greenhouse warming from an associated carbon dioxide buildup and methane levels that would have risen to more than1,000 parts per million (in fact the carbon dioxide level may have risen to 3,000 parts per million). As the nasty hydrogen sulfide goes into the atmosphere, at the same time destroying the ozone layer, greenhouse gases do their work in making the planet hotter. It turns out that the lethality of hydrogen sulfide increases with temperature, based on hideous lab experiments where various animals and plants are exposed to increasing doses of hydrogen in closed chambers. WHY THE PERMIAN EXTINCTION MATTERED Mass extinctions have long been recognized as potent evolutionary events. Two aspects foster evolutionary change. First, the removal of species through extinction opens the way for new species to form to fill the suddenly emptied niches. The more catastrophic the extinction, the greater this effect will be. The second influence is more gradual. If the mass extinction is caused by a long-term environmental change of some sort, species will have an opportunity to try to adapt to the new conditions. But this effect can only take place given

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Out of Thin Air: Dinosaurs, Birds, and Earth’s Ancient Atmosphere groups around at that time has just begun. Part of the reason for this is that there are so few well-preserved skulls known from the latest Permian rocks. In 1998 I began a research project in South Africa that entailed new collecting of fossil skulls from this interval of time. Over several years we found and collected over 130 skulls. Each skull, however, must undergo a slow and expensive job of preparation, and only some years later do new discoveries become available to therapsid experts. Already this is yielding dividends, though. Clearly, there is a downside to endothermy—a very high cost in energy that must be expended. So why did it evolve at all? There is an extensive literature dealing with this question and the what, when, and where questions have been looked at from many different biological angles—save for one. Nowhere is there a discussion of how metabolism and specifically endothermic metabolism would compare to ectothermy in either lower- or higher-oxygen conditions. That will be the slant of this discussion. In one of the latest written reviews on the origin of endothermy, two experienced workers, Willem Hillenius and John Ruben, have perhaps answered this question but inadvertently. They stated: Endothermy is also associated with enhanced stamina and elevated capacity for aerobic metabolism during periods of prolonged activity. They were addressing the ability of warm-blooded animals to conduct prolonged exercise even as they go anaerobic physiologically. Paradoxically, this characteristic of endothermy also allows an animal to do better at lower-oxygen values. This is evidenced by the fact that larger animals with endothermy can live at higher altitudes (and thus lower-oxygen levels) than equally sized ectotherms. Here we can propose that endothermy evolved in response to the lowering oxygen levels of the late Permian and that the primary advantage of animals with this new adaptation was the ability to remain more active and thus they were competitively superior to the ectotherms of the late Permian. This can also be viewed in terms of blood flow and heart rate. As anyone who has ever held a small, scared bird well knows, the heart rate of a small endothermic animal can be astonishingly high, well over 100 beats per minute. This allows blood to circulate through the body more quickly, which would be an advantage when oxygen is low. This

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Out of Thin Air: Dinosaurs, Birds, and Earth’s Ancient Atmosphere is part of the reason that birds can live at higher altitudes than similarly sized lizards. In colder temperatures, such as at night, the ectotherms markedly slow their heart rate—and as a consequence reduce the number of molecules of oxygen reaching the cells. Let’s define a hypothesis based on this idea: Hypothesis 7.2: Endothermy evolved in multiple lineages in response to lowering atmospheric oxygen values of the late Permian and came about concomitant with the evolution of a four-chambered heart, body covering, and in some lineages, nasal turbinals bones. The primary reason for this adaptation was not to maintain constant temperature but to increase efficiency in a low-oxygen environment. The main proposition for the evolution of endothermy is called the aerobic capacity model, which asserts that endothermy evolved to allow elevated levels of sustainable activity and that the increase in resting metabolic rate shown by endotherms was an accidental by-product. The second possibility proposed in the literature is that endothermy came about to allow thermoregulation. This is very close to the aerobic capacity hypothesis, but it differs in suggesting that it was not so much the ability to increase exercise efficiency (although that would have been important, of course) but the more visceral need to survive in a lowering-oxygen atmosphere. It must be remembered that the lineages of animals found in the late Permian had descended from a time of much higher oxygen than in the late Permian or even today. They came from a time when there was so much oxygen in the air that even very inefficient lungs could easily deliver all the oxygen needed for life. Thus, the drop in oxygen may have been even more calamitous to vertebrates than it might otherwise have been. The drop in oxygen at the end of the Permian was profound but slow. It was certainly not fast enough to have been a cause of a sudden die-off at the end of the Permian, as advocated by Oregon paleontologist Greg Retallack. But such a slow change is ideal for evolutionary response to changing and deteriorating environmental conditions. Thus, it seems that the Permian oxygen drop, accompanied by the run-up of global temperatures, stimulated various reptile groups to increase

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Out of Thin Air: Dinosaurs, Birds, and Earth’s Ancient Atmosphere their efficiency of oxygen uptake through the evolution of endothermy and by changes in the nasal area of the skull. Soft-part and physiological responses may have taken place as well, such as increasing the number of red blood cells in the body by increasing red-blood-cell-forming bone marrow. The most obvious change would have been in the lungs and circulatory system, and evolution of the four-chambered heart probably happened at this time. But in how many lineages? THE FOUR-CHAMBERED HEART Both the avian and mammalian hearts have four chambers: two auricles and two ventricles. Many other land tetrapod lineages, including many reptiles and all amphibians, use a three-chambered heart. This difference affects the relationship between oxygenated blood coming back to the heart from the lungs and venous blood returning to the heart from elsewhere in the body. The latter is depleted of its oxygen content. In the four-chambered system, there is never mixing of these two blood groups. But in the three-chambered heart, mixing can take place, and this would seem to reduce the efficiency and oxygen-carrying capacity of this kind of respiratory system. Because the four-chambered heart is associated with endotherms of high metabolic activity, it has long been argued that a perfect separation of bloods was selected for in animals that had higher metabolic activity levels, such as endotherms. Recently, this traditional view has been cleverly questioned by a group of Australian biologists led by Roger Seymour. They have pointed out that some snakes are capable of keeping oxygenated and nonoxygenated bloods separated even though they have a three-chambered heart. Instead, they argue, the four-chambered heart evolved for allowing elevated blood pressure rather than blood itself. Four-chambered hearts are larger than the hearts of ectotherms, and high blood pressure seems to be associated with endothermy. Again, it must be assumed that this (and all other work about respiration discussed to date) was argued in the context of present-day oxygen levels, since this is never brought up. Seymour and his group pointed out that the activity levels of endotherms require more oxygen getting to various parts of the body faster than in ectotherms. Perhaps

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Out of Thin Air: Dinosaurs, Birds, and Earth’s Ancient Atmosphere it was not so much natural selection for greater activity that drove this respiratory system improvement but the critically low, late Permian oxygen levels. Even with ectothermy, the latest Permian therapsids may have been like human mountain climbers. THE ARGUMENTS OVER DINOSAUR ENDOTHERMY One of the most enduring scientific debates of the past two decades has been about the metabolism of dinosaurs. Were they endotherms, ectotherms, or so massive that neither applied? The arguments have gone back and forth, based on evidence as disparate as bone structure, oxygen isotopes from dinosaur fossils, and reputed predator-prey ratios. Here it is proposed that endothermy originated as an adaptation to low atmospheric oxygen. If that was the case, endothermy should have evolved in multiple lineages near the end of the Permian. We have seen that such evidence exists for the late Permian therapsids, the lineage leading to mammals. But what of the other groups of Permian reptiles, the diapsids and anapsids? There is no evidence one way or another about anapsids, but this is not the case for the other large reptilian group, the diapsids (or archosaurs)—ancestors of crocodiles, dinosaurs, and many other lineages. Until recently most arguments about this lineage have rested on evidence from the modern crocodile group. It is generally agreed that crocodiles are archosaurs belonging to a lineage dating back to the late Permian. According to most phylogenies, this Permian group was also ancestral to the dinosaur-avian lineage and that the fundamental split into separate crocodile and dinosauravian lineages took place in the middle to late Triassic. Therefore, late Permian and early Triassic archosaurs were ancestors to both later lineages. So when might endothermy have evolved, if it did at all? The large number of extant crocodiles are all ectotherms, and because of this it has been theorized that if endothermy evolved anywhere in the archosaur lineages other than in birds it did so only in the dinosaurs. According to this phylogeny, then, endothermy evolved after the crocodile-like lineage split off from the dinosaur-bird lineage. This former group, known as the crurotarsans, evolved into a number of very successful and common taxa of the middle to late Triassic, including the crocodile-like phytosaurs, the wholly terrestrial aetosaurs,

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Out of Thin Air: Dinosaurs, Birds, and Earth’s Ancient Atmosphere and the carnivorous rauisuchians. Endothermy evolved somewhere on the other great branch, known as archosaurs, the lineage leading to dinosaurs and birds. We know that birds are warm-blooded, and in recent decades there has been a great deal of research and speculation as to whether the ancestors of birds, the saurischian dinosaurs, were themselves endothermic. Several camps of dinosaur specialists have formed around this fundamental question about dinosaur metabolism. One group that includes Jack Horner, Robert Bakker, and A. de Riqules argue that dinosaurs were endotherms. More recently, however, a new faction has come forward suggesting that dinosaurs and even the earliest birds were all ectoderms and that endothermy in birds did not arise until at least the Cretaceous Period. Recently a new hypothesis has been put forward by the same group that argued that late Permian archosaurs had a four-chambered heart and were at least primitively endothermic. This idea has arisen from recognition that, like the contemporaneous therapsids, the late Permian and early Triassic archosaurs had a more upright posture with legs beneath the body, rather than sprawled to the side in lizard-like fashion. The skeletons of both groups suggest an active life style of high mobility. In this model, all the basal archosaurs had warm blood. But later, perhaps in the middle Triassic, the crocodile and crocodile-like lineages returned to a largely aquatic life style, and re-evolved ectothermy, while maintaining the crocodilian four-chambered heart. The argument here is that ectothermy was thus secondarily re-evolved in this lineage for a simple reason: ectothermy aids diving by enabling the animal to stay underwater longer. By reducing oxygen uptake, an aquatic predator can remain underwater longer than can a similarly sized endotherm. Large size also favors diving and breath holding. For every order of magnitude body mass increases, diving time is doubled. Another adaptation to diving is blood “shunting,” where oxygenated blood is mixed with less oxygenated blood during dives. This latter view fits well with the history of the archosaurs. Modern crocodiles have four-chambered hearts, a trait associated with endothermy. Additionally, crocodiles came from ancestors that had an upright rather than sprawling posture. This upright posture is found today only in endotherms. While the major radiation of the early archosaurs took place in the

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Out of Thin Air: Dinosaurs, Birds, and Earth’s Ancient Atmosphere Reconstruction of the common herbivorous therapsid Diictodon, a victim of the Permian extinction. The degree of its “mammalness” can only be determined now by characteristics that rarely fossilize, such as hair and internal organs. Triassic, they were present in late Permian strata. The oldest Triassic member of the group is Proterosuchus from the Karoo of South Africa. Its appearance coincides with the oxygen minimum, and it might be the first of its lineage to have been endothermic. RESPIRATORY ADAPTATIONS IN LATE PERMIAN-EARLY TRIASSIC THERAPSIDS As we have seen above, the Permian extinction has been proposed as a time of lowering oxygen. This hypothesis stimulated paleontologist Ken Angelyck of Berkeley to look at various therapsid fossils from the late Permian and lower Triassic to see if there were any anatomical adaptations to lowering oxygen, either long-term or short-term. He examined the skull of every known taxon of therapsid in the latest Permian and early Triassic in various museum collections and came up with a fascinating result. While he could find no short-term changes, the size of the nasal passages and the size of the secondary palate area showed significant increases in size from the late Permian into the lower Triassic. This anatomical change is consistent with and supports

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Out of Thin Air: Dinosaurs, Birds, and Earth’s Ancient Atmosphere the hypothesis of long-term atmospheric oxygen reduction across the Permian-Triassic time interval. HABITABLE LAND AREA AT THE END OF THE PERMIAN A last aspect of the Permian extinction relates to altitude and oxygen. Just as oxygen content diminishes with increasing altitude in our world, so too would a change in altitude during any time in the past act in analogous fashion. But with the rise or drop in oxygen levels, paleoaltitude and its effects on the distribution of organisms would greatly change. Mountain ranges in our world often are barriers to gene exchange, producing different biota on either side of the range. At the end of the Permian just living at sea level would have been equivalent today to breathing at 15,000 feet, a height greater than that found atop Mount Rainer in Washington State. Thus even low altitudes during the Permian would have exacerbated this, so that even a modest set of hills would have isolated all but the most low-oxygen-tolerant animals. The result would be a world composed of numerous endemic centers hugging the sea-level coastlines. The high plateaus of many continents may have been without animal life save for the most altitude tolerant. This goes against expectation based on continental position. Because the continents 250 million years ago were all merged into one gigantic supercontinent (named Pangea), we would expect a world where there were very few terrestrial biotic provinces, since animals would be able to walk from one side of the continent to the other without an Atlantic Ocean in the way. But altitude became the new barrier to migration, and new studies of various vertebrate faunas appear to show a world of many separate biotic provinces, at least on land. The work of Roger Smith and myself in the Karoo desert, of Mike Benton in Russia, of Christian Sidor in Niger, and of Roger Smith in Madagascar showed that each of these separate localities had distinct and largely nonoverlapping faunas, as predicted by the Huey and Ward model of altitude. This can be formalized as follows: Hypothesis 7.3: During times of low oxygen, altitude creates barriers to migration and gene flow. Low-oxygen times there-

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Out of Thin Air: Dinosaurs, Birds, and Earth’s Ancient Atmosphere fore should have many separate biotic provinces, at least on land. The opposite occurs during high-oxygen times: there will be relatively few biotic provinces and a worldwide fauna. The drop in oxygen did more than make mountain ranges barriers to migration. It made most areas higher than 3,000 feet uninhabitable during the late Permian-Triassic time interval. Huey and I recognized that there might be a further effect on life’s history: it may have contributed to the Permian and Triassic mass extinctions. We called this “altitudinal compression.” The removal of habitat because of altitudinal compression would have caused species from highlands to migrate toward sea level or die out. Doing so would have increased competition for space and resources and perhaps would have introduced new predators, parasites, or diseases in the previously populated lowlands, causing some number of species to go extinct. We calculated that by the end of the Permian more than 50 percent of the planet’s land surface would no longer have been habitable because of altitudinal compression. There may even have been extinction caused by the effects modeled long ago by Robert MacArthur and E. O. Wilson in their Theory of Island Biogeography. These two scientists noted that diversity is related to habitat area and that species died out when islands or reserves of some sort became smaller. Altitudinal compression would accomplish the same by making the continental landmasses functionally lower in terms of usable area. THE FATE OF PLANTS While plants probably were not overtly affected by the gradual drop in oxygen during the latter half of the Permian period, the concomitant rise in temperature coupled with poisonous hydrogen sulfide in the air surely got their attention. Plant species today are highly sensitive to temperature, both high and low, and will migrate to follow their required temperature ranges during climate change intervals. (Unlike mobile animals, which can move into shelter from freezing winds or find shade in blazing heat, plants must just sit there rooted and take it.) The Permian shows two trends—a change in the kind of flora during the period and a substantial extinction of plants at the end.

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Out of Thin Air: Dinosaurs, Birds, and Earth’s Ancient Atmosphere Tree ferns, seed ferns, and even some of the more archaic plants from the coal ages, such as lycopsids, characterized the cool climate of the early Permian. But as time progressed, conifers, ginkgos, cycads, and other seed plants replaced these floras. This change seems to reflect adaptations to heating and drying, the two climatic trends of the latter part of the Permian. So how severe was the heating? In a study published in 2002, University of Chicago paleobotanist Peter McAllister Rees compiled lists of fossil plant recoveries from around the world during the Permian. This was a Herculean effort of data collections, but its payoff was substantial. Rees showed that during the latter part of the Permian there was a marked shift of high-diversity floras toward higher latitudes—just the sort of pattern that would be expected by a slow but significant global warming. Eventually the tropical latitudes became too hot for most plants, and there would have been giant regions of the globe essentially barren of plant life at the end of the Permian. This change culminated with the extinction itself. While the death toll varies from place to place, well over half of plant species may have gone extinct, and in the southern hemisphere the total extinction of what has been called the Glossopteris flora (glossopterids were a type of woody seed fern that formed forests akin to conifer forests but were lower-growing forms) seemingly all went extinct. Another curious aspect of the extinction has been the finding of abundant fossils, presumably from fungi at the Permian-Triassic boundary itself, and so global and pervasive is this layer that it has been used for correlation of the boundary. While it was eventually found that this so-called fungal layer was in reality several layers rich in fungal and algae remains, its presence is further evidence that the catastrophic plant extinction that killed plants did not faze them, and with plants gone, the low-growing fungi and algae had no competition for light and nutrients. RESULTS OF THE PERMIAN EXTINCTION While intense controversy still exists about the cause or causes of the Permian extinction, on one aspect of that time interval there is agree-

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Out of Thin Air: Dinosaurs, Birds, and Earth’s Ancient Atmosphere ment: in the aftermath of the extinction, ecosystems were profoundly affected, and extinction recovery was long delayed. It is this latter evidence that readily distinguishes the Permian extinction from the later Cretaceous-Tertiary event. While both caused more than half of the species on Earth to disappear, the world recovered relatively quickly after the Cretaceous-Tertiary event. As we have seen above, while some earth scientists believe that the Permian and the Cretaceous-Tertiary events were caused by a large-body impact on Earth, it seems as if the environmental conditions causing the Permian extinction persisted for millions of years after the onset of the extinction. It was not until the middle Triassic, some 245 million years ago, that some semblance of recovery seems to have been under way. These results would be expected if some part of the Permian mass extinction were directly or indirectly caused by the reduction in oxygen at the end of the Permian period. The newest Berner curves show that oxygen stayed low into the Triassic, and there is even some indication that oxygen levels did not bottom out and begin rising until near the end of the lower Triassic, which might account for the long delay in recovery. This evidence suggests that the environmental events that produced the extinction persisted. If so, and if animals were capable of any sort of adaptation in the face of these deleterious conditions, we would predict that the Triassic would show a host of new species not only in response to the many empty ecological niches brought about by the mass extinction but also in response to the longer-term environmental affects of the prolonged extinction event itself. This is the pattern observed for the Triassic—the world was refilled with many species that looked and acted like some of those that were going extinct (therefore an ecological replacement), but there also appeared to be a host of novel creatures, especially on land. The next chapter postulates that many of the new species evolved to counter the continued low-oxygen conditions continuing right into the Jurassic, a period of more than 50 million years. The Triassic was truly the crossroads of animals adapted to two different worlds, one of higher oxygen and one of lower.

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Out of Thin Air: Dinosaurs, Birds, and Earth’s Ancient Atmosphere