6
THE CARBONIFEROUS-EARLY PERMIAN: HIGH OXYGEN, FIRES, AND GIANTS

One of the most useful exercises in trying to understand the nature of body plans is to look at their limitations. For example, no echinoderm ever made it into fresh water, let alone land, and the reasons for this are not hard to find: the evolutionary move from salty to fresh water requires extensive modifications of excretory systems and salt regulation. Echinoderms apparently could never produce these changes. Yet another way to chart limitations is not by what environments were exploited (or not) by specific body plans but by asking a deceptively simple question: what is the largest size that a specific lineage attained? Since large size is often a protection against predation, it seems that most animals grow as large as they can. But there are costs to this, and, as we have seen here, one of the most stringent is in assuring that the new, bigger body receives sufficient oxygenation.

What ultimately limits this growth can provide illuminating answers about the biomechanics of animal design. A favorite example of this exercise deals with arthropods. A spate of wonderful science fiction “B” movies from the 1950s (and then sporadically up to the present-day, such as several years ago when giant mosquitoes sucked unto death a bunch of campers) unleashed a striking diversity of giant insects and spiders. And some were gigantic indeed. The ants of Them! were the size of tanks, while the deadly mantis was the size of a 747. Yet



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Out of Thin Air: Dinosaurs, Birds, and Earth’s Ancient Atmosphere 6 THE CARBONIFEROUS-EARLY PERMIAN: HIGH OXYGEN, FIRES, AND GIANTS One of the most useful exercises in trying to understand the nature of body plans is to look at their limitations. For example, no echinoderm ever made it into fresh water, let alone land, and the reasons for this are not hard to find: the evolutionary move from salty to fresh water requires extensive modifications of excretory systems and salt regulation. Echinoderms apparently could never produce these changes. Yet another way to chart limitations is not by what environments were exploited (or not) by specific body plans but by asking a deceptively simple question: what is the largest size that a specific lineage attained? Since large size is often a protection against predation, it seems that most animals grow as large as they can. But there are costs to this, and, as we have seen here, one of the most stringent is in assuring that the new, bigger body receives sufficient oxygenation. What ultimately limits this growth can provide illuminating answers about the biomechanics of animal design. A favorite example of this exercise deals with arthropods. A spate of wonderful science fiction “B” movies from the 1950s (and then sporadically up to the present-day, such as several years ago when giant mosquitoes sucked unto death a bunch of campers) unleashed a striking diversity of giant insects and spiders. And some were gigantic indeed. The ants of Them! were the size of tanks, while the deadly mantis was the size of a 747. Yet

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Out of Thin Air: Dinosaurs, Birds, and Earth’s Ancient Atmosphere we know that insects, with the external body armor typical of arthropods, could never live at such size. Because of scaling properties and strength of the chitin making up the arthropod exoskeleton, a giant ant or preying mantis of even human size would collapse, its walking legs snapping. But there is another aspect of arthropod design that limits size—respiration. Insects, spiders, and scorpions appear to be size-limited by the degree to which oxygen can diffuse into the innermost regions of their bodies. Today, no insect is bigger than about 6 inches in body length (although arthropods in water can be and are bigger, since their weight is buoyed up by the watery medium they exist in). In the past, however, much larger land arthropods than this did exist—during the interval of the highest oxygen in Earth’s history, the subject of this chapter. Here we will explore how the highest oxygen in Earth’s history allowed some of the strangest—and largest—animals ever on Earth. VOYAGE Here is what we might see were we to return to the world of 300 million years ago, when oxygen was at its highest in Earth’s history. The first noticeable characteristic is the color of the sky. It is a polluted yellow-brown, irrespective of weather; only in high winds does the air clear and then soon it muddies again. This is due to smoke from giant fires perpetually raging and new ones set alight with each lightning strike hitting the extensive forests of the temperate and tropical regions. But there is more than soot in the air; there is fine wind-blown dust as well, accumulating as loess, or glacial front deposits. The air is cold over much of the planet, for this is the time of one of the most extensive glaciations in Earth’s history, with ice caps at each pole and continental glaciers reaching icy fingers across the land as they snake downward out of the mountains onto the plains and river valleys. Where there are forests we find unending vistas of conifer-like trees, for the gymnosperms have by now evolved and have swept away many of the earlier dominant plants. No longer do tall but shallow-rooted primitive trees like Lepidodendron dot the landscape. It is much more familiar, or familiar at least to those of us who now live in the high

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Out of Thin Air: Dinosaurs, Birds, and Earth’s Ancient Atmosphere northern or southern latitudes where pines and fir trees dominate the forests. Unlike during any of our previous trips, the land is alive with animals and the arthropods, at least, are giants relative to similar species living today. Enormous insects, including dragonflies with nearly yardwide wings, flit about above swampy forests, and even the drier upland areas show a high diversity of both flying and earth-bound insects, intermingled with spiders, scorpions, and millipedes, and many are also giants. But it is the vertebrate life that interests us most, and here too there are giants, at least compared to the very first terrestrial forms of some 40 million years earlier, in the early part of the Carboniferous (but certainly not giant relative to the dinosaurs of the future). In the swamps, giant amphibians, some 10 feet long and massive in girth, lie about like modern-day crocodiles. Land vertebrates, freed from water by the evolution of amniotic eggs, are similarly large. Chief among them is the Sail Back, Dimetrodon, and among its pack scurry smaller reptiles, the eventual rootstocks of turtles, lizards, crocodiles, and dinosaurs. We turn to the oceans, where a huge diversity of fish is immediately noticeable. The largest are the cartilaginous sharks, some with peculiar heads and teeth, but bony fish are there too. Missing are the placoderms and ostracoderms. Chambered cephalopods compete for dominance with the smaller fish, but gone are the enormous straight nautiloids of earlier times. Almost all nautiloids are gone, in fact, replaced by ammonoids—cephalopods with shells that look like that of the living chambered nautilus but showing soft parts more akin to modern squids than the archaic soft parts of the nautilus. Yet as interesting as the active swimmers are, it is the nature of the attached animals that attracts immediate interest. Moving in shallow water above a wide and warm continental shelf we find seemingly endless fields of flowers. But flowers will not appear on Earth for another 200 million years. A closer look shows only the resemblance of these long-stalked animals with petal-like heads to the flowers we know. They are crinoids, or sea lilies, animals banished in our world to the marginal habitats of the less successful. But there is clearly no lack of success here, and the appearance of square miles of these fantastic stalked echinoderms is

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Out of Thin Air: Dinosaurs, Birds, and Earth’s Ancient Atmosphere puzzling. We have seen them before in earlier oceans, but not like this. Virtually alone among echinoderms, crinoids have no respiratory structures, but the oxygen levels of this sea are higher than at any time in Earth’s history, and this change has led to the ascendance of crinoids. They are so abundant that their stony stalks make up the majority of bottom sediment, for most are relatively large for their kind. We pass to a reef habitat, and once again the changes are evident. Sponges have taken the place of corals as the major framework builders of the reef ecosystems. Some of these reefs extend along the shelfslope break for hundreds of miles, a habitat filled with fish and ammonoids among the giant sponges. Large as well are resident brachiopods, with two kinds in abundance: one with spines, the other like a large garbage can sitting among the other reef organisms. Both are huge for their race—testament again to the high oxygen of this world. INSECTS IN THE CARBONIFEROUS-PERMIAN OXYGEN HIGH Oxygen reached extraordinarily high values in the time interval from about 320 million to 260 million years ago, with maximal values occurring near the end of this interval. The Carboniferous Period (in North America subdivided into the Mississippian and Pennsylvanian Periods) and the first half of the subsequent Permian Period (299 million to 251 million years ago) were the times of high oxygen, and the biota of the world at that time left clear evidence of the high oxygen. Insects from that time present the best evidence. The Carboniferous high (and much else as well) was wonderfully described by Nick Lane in his 2002 book, Oxygen. Lane wrote about a fossil dragonfly discovered in 1979 that had a wingspan of some 20 inches. An even larger form with a 30-inch wingspan is known from fossils of this Carboniferous time—a beast aptly named Meganeura, yet another dragonfly (Mega means large). And it was not only the wings that were large. The bodies of these giants were proportionally larger, with a width of as much as an inch and a length of nearly a foot. This is about seagull size and while seagulls are never linked in any sentence with the word “giant,” an insect with a 20-inch wingspan was indeed a veritable giant. In comparison, today’s dragonflies may reach

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Out of Thin Air: Dinosaurs, Birds, and Earth’s Ancient Atmosphere a 6-inch wingspan but far more commonly are much smaller. Other giants of the time included mayflies with 19-inch wingspans, a spider with 18-inch legs, and yard-long (or longer) millipedes and scorpions. A 3-foot-long scorpion could weigh 50 pounds and would be a formidable predator of all land animals, including the amphibians. But as we will see, the amphibians also evolved some giant species of their own. So is it the biomechanics of legs that dictated (or limited) insect size? Apparently not. It is the insect respiratory system that dictates maximum size, it seems. All insects use a system of fine tubes called trachea. Air diffuses into the tissues from these tubes, and air is actively ventilated into the tubes. Either by the insect’s rhythmic expansion and contraction of the abdominal region, or by the insect’s flapping of its wings to create air currents around the tracheal opening, air is pulled into the canals. The tracheal system is fantastically efficient in either case. Flying insects achieve the highest metabolic rates of any animal, and experimental evidence shows that increasing oxygen to higher levels enables dragonflies to produce even higher metabolic rates. These studies showed that dragonflies are both metabolically limited and probably size limited as well by our current 21 percent oxygen levels. Whether or not oxygen levels control arthropod size has been contentious. The best evidence that it does comes from studies of amphipods, small marine arthropods that are widely distributed in our world’s oceans and lakes. Gautier Chapelle and Lloyd Peck examined 2,000 specimens from a wide variety of habitats and discovered that bodies of water with higher dissolved oxygen content had larger amphipods. More direct experiments were conducted by Robert Dudley of Arizona State University, who grew fruit flies in elevated oxygen conditions and discovered that each successive generation was larger than the preceding when raised at 23 percent oxygen. In insects, at least, higher oxygen very quickly promotes larger size. It was not only higher oxygen that allowed the existence of giant dragonflies. The actual air pressure is presumed to have been higher too. Oxygen partial pressures rose but not at the expense of other gases. The total gas pressure was higher than today, and the larger number of gas molecules in the atmosphere would have given more lift to the giants. Gas pressure is a function of the number of molecules in the air.

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Out of Thin Air: Dinosaurs, Birds, and Earth’s Ancient Atmosphere The oxygen high happened when more and more oxygen molecules entered the atmosphere. But this addition did not cause the number of nitrogen molecules to become reduced—hence, higher atmospheric gas pressure. Why so much oxygen in the air then? In Chapter 2 we saw that oxygen levels are mainly affected by burial rates of reduced carbon and sulfur-bearing minerals like fool’s gold (pyrite). When a great deal of organic matter is buried, oxygen levels go up. If this is true, it must mean that the Carboniferous period, the time of Earth’s highest oxygen content, must have been a time of rapid burial of large volumes of carbon and pyrite, and evidence from the stratigraphic record confirms that this indeed happened—through the formation of coal deposits. We are looking at a long interval of time—70 million years, longer than the time between the last dinosaurs and the present-day—in the 330 to 260 million years of high oxygen. It turns out that 90 percent of Earth’s present-day coal deposits are found in rocks of that interval. The rate of coal burial was thus much higher than during any other time in Earth’s history—600 times higher, in fact, according to Nick Lane in his book Oxygen. But the term “coal burial” is pretty inaccurate. Coal is the remains of ancient wood, and thus we see a time when enormous quantities of fallen wood were rapidly buried and only later through heat and pressure turned to coal. The Carboniferous Period was the time of forest burial on a spectacular scale. The burial of organic material during the Carboniferous was not restricted to land plants. There is much carbon in the oceans tied up in phyto- and zooplankton, the oceanic equivalents of the terrestrial forests, and here too large amounts of organic-rich sediments accumulated on sea bottoms. The ultimate cause of this unique accumulation of carbon, leading to the unique maximum of oxygen levels, was the coincidence of several geological and biological events. First, the continents of the time coalesced into one single large continent by the closing of an ancient Atlantic Ocean. As Europe collided with North America and South America with Africa, a gigantic linear mountain chain arose along the suturing of these continental blocks. On either side of this

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Out of Thin Air: Dinosaurs, Birds, and Earth’s Ancient Atmosphere mountain chain great floodplains arose, and the configuration of the mountains produced a wet climate over much of the planet. Newly evolved trees colonized the vast swamps and the adjoining drying land areas that came into being. Many of these trees would appear fantastic to us in their strangeness, and one of their strangest traits was a very shallow root system. They grew tall and fell over quite easily. There are lots of falling trees in our world but nowhere near the accumulation of carbon. More was at work than a swampy world ideal for plant growth. The forests that came into being some 375 million years ago were composed of the first true trees that used lignin and cellulose for skeletal support. Lignin is a very tough substance, and today it is broken down by a variety of bacteria. But even after nearly 400 million years—which brings us to the modern-day—the bacteria that do this job take their own sweet time. A fallen tree takes many years to “rot,” and some of the harder woods, those with more lignin than the so-called soft woods like cedar and pine, take longer yet. This “rotting” is accomplished by the oxidation of much of the tree’s carbon, so even if the end product is eventually buried, very little reduced carbon makes it into the geological record. Reduced carbon, as we saw in Chapter 2, is carbon that is deposited in the absence of oxygen in a state that is highly reactive when and if it is later exposed to free oxygen. Back in the Carboniferous many, or perhaps all, of the bacteria that decompose wood were not yet present. Trees would fall and not decompose. Eventually sediment would cover the unrotted trees and reduced carbon would be buried in the process. With all of these trees (and the plankton in the seas) producing oxygen through photosynthesis and very little of this new oxygen being used to decompose the rapidly growing and falling forests, oxygen levels began to rise. OXYGEN AND FOREST FIRES The Carboniferous oxygen peak would have had consequences in addition to gigantism. Oxygen is combustible, and the more there is the bigger the fire—it facilitates fuel ignition, and the fuel in question was the huge and global forest of the Coal Age. The Carboniferous Period

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Out of Thin Air: Dinosaurs, Birds, and Earth’s Ancient Atmosphere may have witnessed the largest forest fires ever to occur on Earth—at least until the dinosaur-killing and forest-igniting Chicxulub asteroid strike (the well known Cretaceous-Tertiary, or “K/T” extinction event) of 65 million years ago. Like so much dealing with the change of oxygen over time, studies on the possibility of megafires provoked by high atmospheric oxygen have been controversial but are becoming much less so as more and more evidence accumulates. Indeed, the forest fire controversy has prompted a major criticism of the theory that oxygen values were different in the past (including higher). It was suggested that ancient forests would not have been able to survive the catastrophic fires, and since we have a long fossil record of the forest, the implication is that catastrophic fires did not take place. Conditions of elevated oxygen, at least theoretically, should generate more rapid rates of flame spreading, and higher-intensity fires and indeed large deposits of fossil charcoal in sedimentary rocks of Mississippian and Pennsylvanian age in North America are evidence that there were forest fires back then—forest fires that were larger, more frequent, and more intense than those of today, although direct comparison suffers from the very different biological makeup of forests then and now. If there were more and more intense forest fires, we would expect to see morphological adaptations to promote fire resistance over time. Plants evolved a series of adaptations collectively known as fire resistance traits, which include thicker bark, deeply imbedded vascular tissue (Cambria), and sheaths of fibrous roots surrounding the stems. So why didn’t the Carboniferous forest burn to the ground? While fires seem to have been more frequent then, the presence of fire-resistant plants and high moisture content both in the plants themselves and in the swampy terrain of large portions of Earth’s surface in the numerous coal swamps limited damage. THE EFFECT OF HIGH OXYGEN ON PLANTS So far we have concentrated on the effects that varying levels of oxygen have on animals. But animal life is itself totally dependent on plant productivity, and we are sure that major perturbations in plant diversity and/or abundance had effects on the animal food chains. Thus, we should look at the effects of varying oxygen levels on plants.

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Out of Thin Air: Dinosaurs, Birds, and Earth’s Ancient Atmosphere Like animals, plants need oxygen for life. Oxygen is taken up within the cells during photorespiration. But the levels are far lower than those needed by animals for the most part, and a second difference is that various parts of terrestrial plants, for instance, have different oxygen needs. Compare the very different environments of underground roots (surrounded by water, both solid and gas, but without light) to leaves (surrounded by gas only, with intermittent light). It is the root system that is most susceptible to damage or cell death from low-oxygen conditions, and it is also the underground environment where such conditions can occur even at times of well-oxygenated air. Roots can be smothered by ground water with low-oxygen values, for instance. What about plants and high-oxygen levels? Here there are far fewer data, but what is known suggests that elevated levels of oxygen are deleterious to plants. Higher levels of oxygen in air lead to increased rates of photorespiration, but a more serious consequence is that with higher oxygen levels there are more toxic hydroxyl radicals that are dangerous to living cells, including all animals. To further test these possibilities, David Beerling of Yale University grew various plants in higher than current oxygen within closed tanks. When oxygen levels were raised to 35 percent (thought to have been the highest levels of all time, occurring in the late Carboniferous or early Permian), net primary productivity (a measure of plant growth) dropped by one-fifth. It may be that the higher oxygen of the Carboniferous-early Permian caused a reduction in plant life to some degree, although this is not observable in the fossil record by any dramatic change or mass extinction during this interval. SLUGGISH EVOLUTION Throughout this book, it is proposed that times of low oxygen in Earth’s history stimulated new kinds of evolution but were also times of low diversity. During high-oxygen times, conversely, diversity is high but the rate of new species formation is low. This hypothesis is based on the proposal that low oxygen forces new experimentation in terms of body plan. This proposal is supported by a new comparison of oxygen levels with data on the rate of new taxon formation. Thus, we should expect to see a very low rate of new species formation during

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Out of Thin Air: Dinosaurs, Birds, and Earth’s Ancient Atmosphere the oxygen high of the Carboniferous-early Permian. Just such a finding has recently been made. In 2005, paleontologist Matthew Powell of Johns Hopkins University compiled voluminous data on the fates of various marine invertebrates during this oxygen high. He discovered very low rates of both origination and extinction. In other words, few new taxa appeared, and those that were already present rarely went extinct. The marine world was composed of an assemblage of virtual living fossils, which are characterized by long ranges (they existed for long periods of time) and produced very few new species. Why did this happen? Powell invoked the presence of the late Paleozoic glaciation as the cause: The Paleozoic history of marine life was interrupted in late Paleozoic time by a conspicuous interval of sluggish diversification and low taxonomic turnover. This unique interval coincided precisely with the late Paleozoic Ice Age. Powell went on to suggest that the cool climate was the cause of this slow interval of evolution. Yet other times of glaciation seem to contradict this. One of the greatest extinctions of all time, that of the Ordovician (the mass extinction discussed in Chapter 4), has been blamed on the glaciation by most experts, and noted paleontologist Steve Stanley has suggested that cooling is a killer and cause of mass extinction. In our different view the sluggish evolution seen during the late Paleozoic is related to the high level of oxygen. So how did all of this relate to the group we belong to and the group most people are interested in—the vertebrates? OXYGEN AND LAND ANIMALS—REPTILES AND THEIR EGGS Conquest of the land by chordates, our lineage, required many major adaptations. The most pressing was a way to reproduce that allowed development of the embryo in an egg out of water. The amphibians of the Pennsylvanian and Permian presumably still laid eggs in water, and thus they could not exploit the resources of land regions that were without lakes or rivers. The evolution of what is termed the amniotic egg solved this, and it was this egg that ensured the existence of a stock of vertebrates now known as reptiles. The evolution of the amniotic

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Out of Thin Air: Dinosaurs, Birds, and Earth’s Ancient Atmosphere egg differentiates the reptiles, birds, and mammals from their ancestral group, the amphibians. Before the end of the Mississippian Period, three great stocks of reptiles had diverged from one another to become independent groups: one that gave rise to mammals, a second to turtles, and a third to the other reptilian groups and to the birds. The fossil record shows that there are many individual species making up these three. A relatively rich fossil record has delineated the evolutionary pathway of these groups. It has also required a reevaluation of just what a “reptile” is. As customarily defined, the class Reptilia includes the living turtles, squamates, and crocodiles. Technically, reptiles can now be defined by what they are not: they are amniotes that lack the specialized characters of birds and mammals. The fossil record suggests that the “amniotes” are “monophyletic”—that they have but one common ancestor—rather than suggesting the possibility that amniotic eggs arose independently more than once. Reptiles are considered to be a monophyletic stock that diverged from amphibian ancestors perhaps sometime in the Mississippian Period of more than 320 million years ago. But while genetic evidence of this divergence, obtained by the “molecular clock” analysis technique, can be dated back to as long ago as 340 million years, fossils that are ascribed to the first reptiles (instead of terrestrial amphibians) have been recovered from several localities globally. Fossils of small reptiles named Hylonomus and Paleothyris have been found interred in fossilized tree stumps of early Pennsylvanian age, and it may be that the fossil record of this later appearance is more valid than the assumption of a Mississippian evolution of the group. In either case, these first reptiles were very small—only about 4 to 6 inches long. That these small reptiles laid the first amniotic eggs is still speculation. There are no fossil eggs in the stratigraphic record until the lower Permian, and this single find remains controversial. But the pathway to the amniotic condition probably passed through an amphibian-like egg without a membrane that would reduce desiccation, which laid in moist places on land. It would have been the evolution of a series of membranes surrounding the embryo (the chorion and amnion), covered by either a leathery or a calcareous but porous egg that was required for fully terrestrial reproduction. One possibility seemingly

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Out of Thin Air: Dinosaurs, Birds, and Earth’s Ancient Atmosphere never considered is that these first tetrapods evolved live births, so that the embryos were not born until substantial development within the female had taken place; we would love to know if any animals of this time produced live births, but that is only rarely recorded in the fossil record. One exception is the extraordinary fossil showing a female ichthyosaur of the Jurassic that died giving live birth. We also have no record of eggs laid in water—for instance, frog and salamander eggs are so soft that they are never preserved. Land eggs eventually were produced, and it was here that the level of oxygen must have played a part. There is a huge tradeoff in reproduction for any land animal using an egg-laying strategy. Moisture must be conserved, so the openings of the egg must be few and small. But reducing permeability of the egg to water moving from inside to outside also reduces the movement of oxygen into the egg by diffusion. Without oxygen the egg cannot develop. The first amniotic eggs were probably produced in oxygen levels equal to or even higher than those of today. It may be no accident that the evolution of the first amniote occurred during a time of high oxygen. This leads us to a new hypothesis: Hypothesis 6.1: Reproductive strategy is affected by atmospheric oxygen content, with higher-oxygen contents producing more rapid embryonic development. High oxygen may have allowed amniotic eggs and then live births. Some biologists have suggested that live births could not take place in low oxygen because, at least in mammals, the placenta delivers lower levels of oxygen than are present even in arterial blood in the same mother. But this is for mammals. Reptiles have a very different reproductive anatomy. It may be that low oxygen even favors live birth. Evidence to support this comes from three lines of evidence. First, birds (egg layers) living in high-altitude habitats routinely feed at higher altitudes than the maximum altitude at which they can reproduce. The maximum altitudes of the nests of many mountainous bird species repeatedly show this pattern. The highest nests are at 18,000 feet, and higher than this the embryos will not develop successfully. While at least three factors may be involved in this limit (lowered-oxygen con-

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Out of Thin Air: Dinosaurs, Birds, and Earth’s Ancient Atmosphere tent with altitude, desiccation because of air dryness at altitude, and relatively low temperatures at greater altitude), it may be oxygen content that is most important. Second, recent experiments by John VandenBrooks from Yale University have shown that alligator eggs taken from natural clutches and raised in artificially higher-oxygen levels showed dramatically faster than normal development rates. The embryos grew some 25 percent faster than controls held at normal atmospheric oxygen levels. Increased oxygen clearly influences growth rates, at least in American alligators. Since egg contents are a tasty snack for many predators now, and surely back then, it is in the embryo’s better survival interest to develop and hatch as quickly as possible. Finally, a higher proportion of reptiles at high altitudes use live births than do reptiles at lower altitudes. At this point we can summarize and discuss the variables in land animal reproduction and try to relate these to generalizations about both oxygen levels and temperature. There are two possible strategies, egg laying or live birth. In the egg case, the eggs are either covered with a calcareous shell or a softer, more leathery shell. Today, all birds utilize calcareous eggs, while all living reptiles that lay eggs use the leathery covering. Unfortunately, there is little information about the relative oxygen diffusion rates for leathery, or parchment, eggs compared to calcareous eggs. The utilization of egg laying or live births has important consequences for land animals. The embryos developed by the live birth method are not endangered by temperature change, desiccation, or oxygen deprivation. But the cost is the added volume to the mother, which must invariably make her more vulnerable to predation in addition to making her need more food than would be necessary for herself alone. Egg layers are not burdened with this problem but have the tradeoff of a less safe environment—the interior of an egg outside the body—that leads to enhanced embryonic death rate through predation or lethal conditions of the external environment. The study of oxygen levels and egg morphology or reproductive strategy is in its infancy. Obvious tests include raising eggs at both high-and low-oxygen levels, for both calcareous and leathery eggs. Also, a direct study of fossil eggs themselves would be of great interest. A pre-

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Out of Thin Air: Dinosaurs, Birds, and Earth’s Ancient Atmosphere diction is that fossil eggs from times of low oxygen should show more openings than those from times of higher oxygen. OXYGEN AND LAND ANIMALS—REPTILES AND THEIR LOCOMOTION As four-legged vertebrates emerged from their piscine ancestors, many new anatomical challenges had to be overcome. No longer was there water to support the animal’s body; in air, both support and locomotion had to be accomplished by the four legs. An entirely new suite of shoulder and pelvic girdle designs had to evolve, along with the muscles necessary to allow locomotion. Equally daunting was the problem of acquiring sufficient oxygen to allow sustained exercise. Early tetrapods apparently used the same set of muscles for motion and for taking a breath, and they could not do both at the same time. Fish seem to have no problem with sustained exercise or with respiring during activity, suggesting that oxygen is not a limiting factor in daily activity. For land tetrapods this is not the case. The body plan of the earliest land tetrapods provided for a sprawling posture with legs splayed out to the sides of the body trunk. In walking or running with such a body plan, the trunk is twisted first to one side and then to the other in a sinuous fashion. As the left leg moves forward, the right side of the chest and the lungs within are compressed. This is reversed with the next step. The distortion of the chest makes “normal” breathing difficult to impossible—so each breath must be taken between steps. This process makes it impossible for the animal to take a breath when running—modern amphibians and most reptiles cannot run and breathe at the same time (the exceptions including varanids that augment respiration with gular pumping), and it is a good bet that their Paleozoic ancestors were similarly impaired. Because of this there are no reptilian marathoners and not too many long-distance sprinters. This is why reptiles and amphibians are ambush predators. They do not run down their prey. The best of the modern reptiles in terms of running is the Komodo dragon, which will sprint for no more than 30 feet when attacking prey. This is called Carrier’s Constraint, after it discoverer, physiologist David Carrier.

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Out of Thin Air: Dinosaurs, Birds, and Earth’s Ancient Atmosphere The dilemma of not being able to breathe and move rapidly at the same time was a huge obstacle to colonizing land. The first land tetrapods would have been at a great disadvantage to even the land arthropods, such as the scorpions, for the vertebrates would have been slow and would have needed to stop constantly to take a breath. This is why oxygen levels would have been critical. Only under high-oxygen conditions would the first land vertebrates have had any chance of making a successful living on land. One consequence of limited respiration while moving was that the early amphibians and reptiles evolved a three-chambered heart. This kind of heart is found in most modern amphibians and reptiles and is adaptive for creatures that have the problem of inferior respiration while moving. While a lizard is chasing prey it is not breathing, and thus the fourth chamber of the heart, which would be pumping blood to the lungs, is superfluous. The three chambers are used to pump blood throughout the body, but the price that must be paid is that it takes the lizard longer to reoxygenate the blood when activity ceases. One group of reptiles, the mammal-like reptiles or synapsids, either partially or totally solved the reptilian problem of not being able to breathe while running by changing their stance. The synapsids show an evolutionary trend of moving their legs into a position so that they were increasingly under the trunk of the body, rather than splayed out to the side as in modern lizards. This created a more upright posture and removed, or at least greatly decreased, the lung compression that accompanies the sinuous gait of lizards and salamanders. While there was still some splay of the limbs to the sides of the trunk, it was certainly less than in the first tetrapods. With the evolution of the therapsids in the middle Permian, the stance became even more upright. OXYGEN AND LAND ANIMALS—REPTILES AND THEIR THERMOREGULATION Another important variable is the nature of thermoregulation—the possibilities of endothermy (warm-bloodedness), ectothermy (cold-bloodedness), and a third category that is essentially neither of the others and is associated with very large size. Warm-bloodedness

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Out of Thin Air: Dinosaurs, Birds, and Earth’s Ancient Atmosphere (endothermy) allows animals using it to stay at a constant, warm temperature no matter how cold it gets. However, this can work against animals in very hot climates, as it is more difficult to cool off than warm up. Cold-blooded animals match the temperature around them. They are sluggish in the cold. There is a third kind of metabolism, found in animals so big that they are largely unaffected by daily swings in temperature, such as daytime and nighttime. The very large dinosaurs presumably used this system. Other important aspects that might be related to the environmental conditions in which the various clades evolved and then lived include the presence or absence of scales, hair, and feathers. With thermoregulation pathways, the question of whether or not dinosaurs were warm-blooded has been the most discussed and most controversial of all. The fact that each of these characteristics, thermoregulatory systems and body covering, is primarily either physiological or involves body parts that only rarely leave any fossil record (such as fur) is in large part responsible for the controversies. We know that all living mammals and birds are warm-blooded, with the former having hair and the latter feathers, just as we know that all living reptiles are cold-blooded, with no hair or feathers. The status of extinct forms remains controversial. Of interest here is how oxygen concentration primarily and characteristic global temperatures secondarily affected thermoregulation or characteristic body coverings in animal stocks of the past. Let’s look at each of the three stocks in more detail with this overarching question in mind. Diapsids Openings are used to lighten the reptile skull, and their number (or lack of) is a convenient way of differentiating the three major stocks of “reptiles.” Anapsids (ancestors of the turtles) had no major openings in their skulls; synapsids (ancestors of the mammals) had one; and diapsids (dinosaurs, crocodiles, lizards, and snakes) had two. The earliest member of the diapsids is known from the latest Pennsylvanian rocks around 305 million to 300 million years ago, and it was small in size, about 8 inches in total length. From the time of their origins until

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Out of Thin Air: Dinosaurs, Birds, and Earth’s Ancient Atmosphere the beginning of the fall of oxygen, which probably began in earnest some 260 million years ago, in the middle and late part of the Permian period, the diapsids did little in the way of diversification or specialization. They remained small and lizard-like. They gave no indication that they would be the ancestors of the largest land animals ever to appear on Earth, in the form of the Mesozoic dinosaurs. If the time of highest oxygen stimulated insects to their greatest size, the same cannot be said of the diapsids. The most pressing question is whether or not this group was warm-blooded. Anapsids The lineage that ultimately gave rise to turtles was very successful during the late Pennsylvanian but less so into the Permian. Anapsids did evolve into giant forms, including cotylosaurs and the even larger pareiosaurs. These were armored giants, surely slow moving and herbivores that lived right until the end of the Permian. Other anapsids were small and more lizard-like. It is very likely that the gigantic size of the earlier Permian anapsids was allowed by high oxygen. All modern anapsids use ectothermy; they are cold-blooded. Presumably the ancient forms used this system as well, but that is still controversial. Synapsids The third group of amniotes from this time, the synapsids, or mammal-like reptiles, are known in their most primitive form from Pennsylvanian rocks, and these ancestors of mammals had a lizard-like small shape and mode of life in all probability. It is assumed that these early synapsids were cold-blooded. They in turn gave rise to two great and largely temporally successive stocks, the pelycosaurs (or finbacks, like the early Permian Dimetrodon) and their successors, the therapsids (the lineage giving rise to mammals). It is this latter group that is also called the mammal-like reptiles. Unlike the diapsids, the synapsids diversified during the oxygen high and at its peak became the largest of all land vertebrates. In the

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Out of Thin Air: Dinosaurs, Birds, and Earth’s Ancient Atmosphere Reconstruction of the synapsid reptile Dimetrodon. The large fin was probably for thermoregulation, and thus is evidence that this group was not warm-blooded. latter part of the Pennsylvanian the pelycosaurs probably looked and acted like the large monitor lizards or iguanas of today. By the end of the Pennsylvanian some attained the size of today’s Komodo dragon, and they may have been fearsome predators. By the beginning of the Permian Period, some 300 million years ago, the pelycosaurs made up at least 70 percent of the land vertebrate fauna. And they diversified in terms of feeding as well; three groups were found: fish eaters, meat eaters, and the first large herbivores. Both predators and prey (for this group evolved both predatory and herbivorous species) could attain a size of 12 feet in length, and some, such as Dimetrodon, had a large sail on its back that would have made it appear even larger. The sail present on both carnivores and herbivores of the late Pennsylvanian and early Permian is a vital clue to the metabolism of the pelycosaurs: it was a device used to rapidly heat the animal in the morning hours. By positioning the sail so as to catch the morning sun, both predators and prey could warm their large bodies quickly, allowing rapid movement. The animal that first attained warm internal temperature would have been the winner in the game of predation or escape, and hence natural selection would have promoted these sails. But the larger clue from the presence of sails is that during the oxygen high, the ancestors of the mammals had not yet evolved warm-bloodedness. So when did warm-bloodedness first appear? That revolutionary breakthrough must have happened among the successors to the pelycosaurs, the therapsids. We must note as well that the late Pennsylva-

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Out of Thin Air: Dinosaurs, Birds, and Earth’s Ancient Atmosphere nian and early Permian, while a time of oxygen high, was a period of temperature low. There was a great glaciation during this interval and much of the polar regions of both hemispheres would have been covered in ice, both continental and sea ice. The transition from the pelycosaurs to the therapsids is poorly known because of few fossiliferous deposits of the critical age. The gap in our knowledge of the synapsid fossil record extends from perhaps 285 million years ago to around 270 million years ago with some few exceptions in two main regions, the Russian area around the Ural Mountains and the Karoo region of South Africa. The record in the Karoo begins with glacial deposits perhaps as much as 270 million years in age, and then there is a continuous record right into the Jurassic (199 million to 145 million years ago), giving an unparalleled understanding of this lineage of animals. The therapsids split into two groups, a dominantly carnivorous group and an herbivorous group. By about 260 million years ago the ice was gone in South Africa, but we can assume that the relatively high latitude of this part of the supercontinent Pangea (about 60 degrees South latitude) remained cool. It was still a time of high oxygen, certainly higher than now, but that was changing. As the Permian period progressed, oxygen levels dropped. Seemingly two great radiations of therapsids occurred, among both carnivores and herbivores. From perhaps 270 million to 260 million years ago the dominant land animals were the dinocephalians, and these great bulky beasts reached astounding size, not dinosaur-sized but certainly exceeding the size of any land mammal today save, perhaps, the elephant, and some of the largest of the dinocephalians certainly must have weighed as much as elephants. Moschops, for instance, a common genus from South Africa, was 10 feet in length, with an enormous head and front legs longer than the back. This was an enormous animal, the biggest yet on the Earth. But it was graceless in construction, being bulky, and surely awkward. No fast running here, or any deep thoughts, if the tiny size of its brain case is any indication. It was hunted by a group of nearly equally-sized carnivores, also lumbering and slow in all probability. The dinocephalians and their carnivore predators were hit by a great extinction, still very poorly understood, of some 260 million

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Out of Thin Air: Dinosaurs, Birds, and Earth’s Ancient Atmosphere years ago, the same time, it turns out, that oxygen levels began to plummet. The immediate successors in terrestrial dominance of the dinocephalians, the dicynodonts, were the dominant herbivores of the time from 260 million to 250 million years ago. They in turn were almost eliminated from the planet in the Permian extinction, which will be described in more detail in the next chapter. The dicynodonts were hunted by three groups of carnivores, all therapsids: the gorgonopsians, which died out at the end of the Permian; the slightly more diverse therocephalians; and the cynodonts, which ultimately evolved into mammals during the Triassic. We will return to these groups—and their horrific fate—in more detail in the next chapter. OXYGEN AND LAND ANIMALS—REPTILES AND THEIR SIZE The rise of atmospheric oxygen to unprecedented values of over 30 percent in the Carboniferous-early Permian was accompanied by the evolution of insects of unprecedented size. The giant dragonflies and others of the late Carboniferous through the early Permian were the largest insects in Earth’s history. Perhaps it is just coincidence but most specialists agree that the high oxygen would have enabled insects to grow larger, since the insect’s respiratory system requires diffusion of oxygen through tubes into the interior of the body and in times of higher oxygen, more of this vital gas could penetrate into ever-larger-bodied insects. So if insects got larger as oxygen raised, what about vertebrates? New data acquired by French anatomist Michel Laurin can be used to test this question. Indeed, it does seem that body size in various late Paleozoic reptilian lineages do track oxygen levels. Laurin’s published data were compared to the oxygen levels given in the Berner curves (like so much discovered while writing this book, this information is simultaneously being published in the scientific literature). Laurin looked at a sample of animals from the anapsids and synapsids. He used a measure of body length and a measure of skull size to evaluate animal size, for specific time horizons between the late Mississippian and the end of the Permian, from about 320 million years ago until about 250 million years ago. Then I did a simple regression analysis of mean size and oxygen levels. Indeed, mean skull size closely

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Out of Thin Air: Dinosaurs, Birds, and Earth’s Ancient Atmosphere tracks oxygen levels, increasing and decreasing in close correspondence with atmospheric oxygen levels for the time periods for which size data is available. As oxygen levels rose in the late Carboniferous, so too did the size of the reptiles increase and, as oxygen began to drop in the mid-Permian, we see size beginning to trend downward. Thus, like insects, it appears that at least these groups of land vertebrates changed size in response to the oxygen available at any given time. The mammal-like reptiles also seem to show this trend (according to vertebrate paleontologist Christian Sidor of the University of Washington), although the quantitative data (measured in the way that Laurin measured the sizes of earlier land vertebrates) are not yet available. Nevertheless, it is clear that the largest therapsids of all time, the dinocephalians of the middle Permian, evolved at the peak of oxygen abundance. As oxygen began to drop in the mid-Permian, successive taxa assigned to various therapsid groups and, most importantly, the dicynodonts, showed a trend toward smaller skull sizes. While some relatively large forms still lived in the latest Permian—the genus Dicynodon and even the carnivorous gorgonopsians come to mind—by this time many of the dicynodonts were smaller. The latest Permian taxa, Cistecephalus, Diictodon, and a few others, were very small. The late Permian-early Triassic genus Lystrosaurus is smaller in the Triassic than it is in the Permian, and the various cynodonts of the late Permian and early Triassic are all small in size. There are a few giants in the Triassic—Kannemeyeria and Tritylodon are examples—but in general the therapsids of the Triassic are much smaller than those of the Permian. A recent paper by University of Washington paleontologist Christian Sidor has confirmed the drop in size of Triassic forms compared to their Permian ancestors. Thus, once again, we see there is a strong correlation between terrestrial animal size and oxygen levels, in this case from the latest Permian into the Triassic. In high oxygen tetrapods grew large, and then they grew smaller as oxygen levels diminished. We have come to a time of about 260 million years ago. It was the end of the long Paleozoic Era, and in the last 10 million years of its nearly 300-million-year-long history all hell would break loose—literally, as the next chapter shall recount.

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