5
THE SILURIAN-DEVONIAN: HOW AN OXYGEN SPIKE ALLOWED THE FIRST CONQUEST OF LAND

Chapter 4 looked at the world of the Ordovician, a time interval beginning with a wave of extinctions, which ended the Cambrian period some 490 million years ago, and ending with less violence some 450 million years ago. This chapter looks at the next two periods: Silurian (443 million to 416 million years ago) and Devonian (416 million to 359 million years ago). During this time, great reefs grew in the seas; fish began to vie with the cephalopods for dominion in the oceans, while untold numbers of brachiopods covered the warm sea bottoms. Yet for all of the changes in the ocean, it was on land that the greatest transformation took place. For the first time animals began to trek inward from the seashore, breathing through new kinds of lungs as they emerged from their beachheads. They did so in search of new food sources, for a revolution was taking place: the land was greening, and plants, for the first time, rose up from the soil to point green leaves at an enlarging sun. Why did this invasion of the land take place? The old view was that it was about time, nothing more. Here, in this chapter, let’s join those ancient plants and early land animals in breaking new ground. From the middle of the Ordovician Period until the end of the ensuing Silurian Period—a time of 60 million years—atmospheric oxygen uninterruptedly rose 10 percentage points, from a gasping 15 percent to the heady richness of 25 percent of the air—far more



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Out of Thin Air: Dinosaurs, Birds, and Earth’s Ancient Atmosphere 5 THE SILURIAN-DEVONIAN: HOW AN OXYGEN SPIKE ALLOWED THE FIRST CONQUEST OF LAND Chapter 4 looked at the world of the Ordovician, a time interval beginning with a wave of extinctions, which ended the Cambrian period some 490 million years ago, and ending with less violence some 450 million years ago. This chapter looks at the next two periods: Silurian (443 million to 416 million years ago) and Devonian (416 million to 359 million years ago). During this time, great reefs grew in the seas; fish began to vie with the cephalopods for dominion in the oceans, while untold numbers of brachiopods covered the warm sea bottoms. Yet for all of the changes in the ocean, it was on land that the greatest transformation took place. For the first time animals began to trek inward from the seashore, breathing through new kinds of lungs as they emerged from their beachheads. They did so in search of new food sources, for a revolution was taking place: the land was greening, and plants, for the first time, rose up from the soil to point green leaves at an enlarging sun. Why did this invasion of the land take place? The old view was that it was about time, nothing more. Here, in this chapter, let’s join those ancient plants and early land animals in breaking new ground. From the middle of the Ordovician Period until the end of the ensuing Silurian Period—a time of 60 million years—atmospheric oxygen uninterruptedly rose 10 percentage points, from a gasping 15 percent to the heady richness of 25 percent of the air—far more

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Out of Thin Air: Dinosaurs, Birds, and Earth’s Ancient Atmosphere than we have today. The land changed from a place of “thin air” to a world where oxygen was almost a free commodity—which would have been a wonderful and necessary thing for an early insect with a still nearly worthless, newly evolved lung or an early land plant trying to coax oxygen into one of its clumsy, inefficient, newly evolved roots, for while plants above the ground need little oxygen for their leaves, their roots, deep in soil that may have too little oxygen for growth, are another matter. Was this coincidence or cause and effect? In this chapter let’s look at how this great rise in atmospheric air paved the way for the first real colonization of land. TRIP 3 Let’s travel back in time to the last time interval of the Silurian Period, a time some 420 million years ago, to get a snapshot of the middle of this long Silurian-Devonian interval. It has been some 50 million years since our last look at Earth, and the changes that have taken place are nothing short of remarkable. The land is green, and everywhere we see the stems of low plants not only at water’s edge of swamps and lakes but also in uplands. There are true vascular plants, still low in size but now common and diverse: an enormous variety of forms are seen. And they are not alone on the land. Crawling among the plants is a small diversity of insects, also very small in size. They look like today’s springtails and the odious silverfish, and none have wings. Among them are even smaller mites. There are no land-dwelling vertebrates of any kind—yet. We move to a small lake and find it filled with fish. For the first time we see fish with jaws amid the same jawless ostracoderms that were present in the earlier Ordovician. The jawed fish are heavily armored and upon closer examination seem very foreign looking. They are the placoderms, and some have gotten quite large and are destined to become larger yet in the upcoming Devonian Period. They use their jaws to good use, making meals of the algae-eating and jawless ostracoderms. There are a few minnow-like fish that seem to look like the bony fish of our time and perhaps some fish that may become sharks, but these are rare. The bony armor seems like a ludicrous adaptation

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Out of Thin Air: Dinosaurs, Birds, and Earth’s Ancient Atmosphere for animals depending on mobility and maneuverability, but soon the reason for this armor becomes apparent. A great shadow looms from the turbid water, and a hideous nightmare swims into view. It is clearly some kind of arthropod, coated with the typical arthropodan external skeleton, but its size is staggering. It looks like a giant underwater scorpion and is indeed related to the scorpion clan. Many others swim into view, undulating segmented bodies like human swimmers doing the butterfly, but these animals are propelled through the water by a large horizontal tail. The largest of these creatures, called eurypterids, is 10 feet long. They are the largest animals yet evolved on Earth and one of the most fearsome of any that will ever inhabit the sea. The eurypterids sweep into the slowly moving fish, and their means of attaining food is apparent. Each has a long pair of wicked claws emerging from the head region, and many fish become meals. How could any animal be so large at this time? Up until now animals had been far smaller. We know that the amount of oxygen available to an animal is often a determinant of its final size. A quick measure of atmospheric oxygen tells the story: it is 24 percent compared to our present-day 21 percent. A realization dawns: no giant arthropods like this exist in our time, nor could they, in all probability. These giants are enabled by high oxygen. But this time of oxygen abundance will not last, and by the end of the succeeding Devonian Period oxygen levels will crash to far lower values than today. With this crash, the race of arthropod giants and many, many more animal races will be killed off in one of the greatest of all mass extinctions affecting animals (and plants) on Earth—the Devonian mass extinction of 368 million years ago. But that is still far in the future, over 50 million years in the future. For now the high oxygen of the Silurian has allowed the rise of the first insects on land, the rise of plants on land, and the first age of giants here in fresh waters. We wonder what awaits us in the sea. The changes there are no less dramatic. The shelly marine fauna of sessile marine invertebrates is still in place, but again we remark on the size of things. On a shallow sea bottom we find a pavement of shelled brachiopods, looking much like the clams that also occur in some numbers around them. But these brachiopods are the largest that we have ever seen and, like the eurypterids, the largest of their kind that

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Out of Thin Air: Dinosaurs, Birds, and Earth’s Ancient Atmosphere Earth will ever see. They are pentamerid brachiopods, and, like the eurypterids, their time is short, for the fall of oxygen soon to come will spell their end. The high atmospheric oxygen has translated in this shallow sea bottom to a very high level of dissolved oxygen, and the brachiopod pump gill makes these animals well fit for living in this high-oxygen world and allows this gigantism. We see fish here too, many resembling those of the freshwater lake we visited, but the fish are both outnumbered and dwarfed by an incredible diversity of nautiloid cephalopods. The cephalopods vary in size from tiny to gigantic, some larger even than the eurypterids, and there is a cornucopia of shapes as well. For the cephalopods, too, the high oxygen has translated into enormous size—and this makes good evolutionary sense. (The nineteenth-century paleontologist Edward Cope realized that most lineages of animals become larger through time—and he recognized the reason. Large size lends protection against predation. This generalization now bears his name: Cope’s Rule.) The long, straight cones typical of the first nautiloids are still present, and the biggest of the nautiloids are all straight. But among the cephalopods are all manner of shapes from arcuate, or snail-shaped, to tightly coiled forms not too dissimilar from the living Nautilus of today. We look for the prey of the nautiloids and see a variety of trilobites. When threatened, the trilobites coil up, but the most striking thing about their appearance is that most sport far fewer thoracic segments than were present in their Cambrian and even Ordovician ancestors, and many lineages have become larger as well. With this reduction of segments there has been a vast reduction of gill surface area, but once again, the high-oxygen content of these marine waters has allowed the trilobites this luxury. But they have made a bad bet in doing this, and in many respects this time of higher oxygen is their last hurrah. The great Devonian mass extinction will kill off most, and while a few will survive the catastrophe, they will from that point on, until their final extinction in another mass extinction (the most terrible of all, at the end of the Permian), remain rare and minor elements of the marine world.

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Out of Thin Air: Dinosaurs, Birds, and Earth’s Ancient Atmosphere TERRESTRIALIZATION While numerous innovations took place in the sea during the Silurian and Devonian periods, it is on land that the most important events—at least to us land-living animals—took place. The conquest of land, first by plants and then by a succession of animal phyla, began in the Silurian and Devonian. Why did the conquest of land occur then? The standard view of the history of life is that these events took place because animals had finally evolved to a point where land conquest was possible. In other words, the evolutionary advances in arthropods, mollusks, annelids, and eventually vertebrates—the major animal phyla involved in the conquest of land—had finally and coincidentally arrived at levels of organization that allowed them to climb out from water and conquer the land. An alternative view is that the first conquest of land took place as soon as atmospheric oxygen rose to levels allowing land animal life. Let’s first look at what was required of both plants and animals to allow terrestrialization, the adaptations needed to permit life on land. Let’s begin with plants, for without a food source on land, no animals would have made the effort to gain a terrestrial foothold. By 600 million years ago, plant evolution had resulted in the diversification of many lineages of multicellular plants, some of which are familiar to us still—the green, brown, and red algas, which are members of any seashore in our world. But these were plants that had evolved in seawater. The needs of life—carbon dioxide and nutrients—were easily and readily available to them in the surrounding seawater. Reproduction was also mediated by the liquid environment. The move to land required substantial evolutionary change in the areas of carbon dioxide acquisition, nutrient acquisition, body support, and reproduction. Each required extensive modification to the existing body plans of the fully aquatic plant taxa. It was the green algal group, the Charophyceae, which ultimately gave rise to photosynthetic land plants. Many obstacles had to be overcome. First was the problem of desiccation. Green algae washing ashore from their underwater habitat quickly degenerate in air, for they have no protective coating. But these green algae produce reproductive zygotes that have a resistant cuticle, and this same cuticle may have been

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Out of Thin Air: Dinosaurs, Birds, and Earth’s Ancient Atmosphere used to coat the entire plant in the move onto land. But the evolution of the cuticle, which protected the liquid-filled plant cells inside, created a new problem: it cut off ready access to carbon dioxide. In the ocean, carbon in dissolved carbon dioxide was simply absorbed across the cell wall. So to accomplish this in the newly evolved land plant, many small holes, called stomata, evolved as tiny portals for the entry of gaseous carbon dioxide. The plant body must be anchored in place, and early land plants were probably anchored by fungal symbionts. Additionally, the symbiotic relationship between plants and fungi would provide for a means through which water could be recovered from the soil. Moving onto land also created the problem of support. Plants need large surface areas facing sunlight so that their chloroplast receive enough energy through light to run the photosynthetic reactions necessary for plant life. One solution is to simply lie flat on the ground, and the very first land plants probably did this. This kind of solution is still used by mosses, which grow as flat carpets lying over soil. A visit to the Ordovician land probably would have been a visit to a moss world, where the world’s tallest “tree” was all of a quarter-inch tall. But this is a very limiting solution. Growing upright enables the acquisition of much more light, especially in an ecosystem where there is competition between numerous low-growing plants, and harder material was incorporated by early plants to allow first stems and finally tree trunks. Concomitant with the evolution of stems would have been the evolution of a transport system from the newly evolved roots up to the newly evolved leaves. Finally, reproductive bodies that could withstand periods of desiccation evolved, enabling reproduction in the terrestrial environment. With these innovations the colonization of land by plants was ensured, and with the formation of vast new amounts of organic carbon on land for the first time, animals were quick to follow. New resources spur new evolution. As with plants, a major problem facing any would-be terrestrial animal colonist is water loss. All living cells require liquid within them, and living in water does not create any sort of desiccation problem. But living on land requires a tough coat to hold water in. The problem is that solutions that allow a reduction in surface desiccation are an-

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Out of Thin Air: Dinosaurs, Birds, and Earth’s Ancient Atmosphere tagonistic to the needs of a respiratory membrane. So—to build an external coating that resists desiccation and then suffocate? Or build a surface respiratory structure that allows the diffusion of oxygen into the body but risk desiccation through this same structure? This dilemma had to be overcome by any land conqueror, and it was apparently so difficult that only a very small number of animal phyla ever accomplished the move from water to land. Some of the largest and most important of current marine phyla certainly never made it: there are no terrestrial sponges, cnidarians, brachiopods, bryozoans, or echinoderms, among many others, for instance. Identification of the first land animals has relied on a fossil record that is notoriously inaccurate when it comes to small terrestrial arthropods. The oldest fossils of land animals all appear to be small spiders, scorpions, or very primitive insects dating back to between 420 million and 410 million years ago—right about the transition from the Silurian to the Devonian. All of these animals, however, have very weakly calcified exoskeletons and are rarely preserved. By the late Silurian or early Devonian, however, the rise of land plants also brought ashore the vanguards of the animal invasion, and it is clear that multiple lines of arthropods independently evolved respiratory systems capable of dealing with air. The respiratory systems in today’s scorpions and spiders provide a key to understanding the transition of arthropods from marine animals to successful terrestrial animals. Of all body structures required to make this crucial jump, none was more important than respiratory structures. It also seems apparent that the earliest lungs used by the pioneering arthropods would have been transitional structures nowhere near as efficient as the respiratory structures in later species. But in a very high-oxygen atmosphere, air can diffuse across the body wall of very small land animals—and the first land animals all seemed to be small—and can enter the body through even the primitive lung structures. Of the phyla that made it onto land—the arthropods, mollusks, annelids, and chordates (along with some very small animals such as nematodes)—the arthropods were preevolved to succeed, for their all-encompassing skeletal box was already fashioned to provide protection from desiccation. But they still had to overcome the problem of

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Out of Thin Air: Dinosaurs, Birds, and Earth’s Ancient Atmosphere respiration. As we have seen, the outer skeleton of arthropods required the evolution of extensive and large gills on most segments to ensure survival in the low-oxygen Cambrian world (where most arthropod higher taxa are first seen in the fossil record). But external gills will not work in air. The solution among the first terrestrial arthropods, spiders and scorpions, was to produce a new kind of respiratory structure called a book lung, named after the resemblance of the inner parts of this lung to the pages of a book. A series of flat plates within the body have blood flowing between the leaves. Air enters the book lungs through a set of openings in the carapace. The book lung is a passive lung in that there is no current of air “inhaled.” And because they have a passive lung, animals with book lungs depend on some minimum oxygen content. Surprisingly, no experiments have yet been done to see how low they can go. Some very small spiders are blown by winds at high altitudes and have been dubbed “aerial plankton.” This would seemingly argue that the book lung system in spiders is capable of extracting sufficient oxygen in low-oxygen environments. But these spiders are invariably very small in size, so small that an appreciable fraction of their respiratory needs may be satisfied by passive diffusion across the body. Larger-bodied spiders are dependent on the book lungs. Book lungs may be more efficient at garnering oxygen than the insect respiratory system, which is composed of tube-like trachea. Like the respiratory systems of spiders and scorpions, the insect system is passive in that there is little or no pumping, although recent studies on insects suggest that some slight pumping may indeed be occurring but at very low pressures. The book lung system of the arachnids has a much higher surface area than does the insect system and thus should work at lower atmospheric oxygen concentrations. Understanding the when of this first colonization of land is hampered by the small size and poorly fossilizable nature of the earliest scorpions and spiders. Present-day scorpions are more mineralized than spiders, and not surprisingly, have a better fossil record. The earliest evidence of animal fragments on land is from late Silurian rocks in Wales, about 420 million years in age, near the end of the Silurian Period—a time when oxygen had already reached very high levels, the

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Out of Thin Air: Dinosaurs, Birds, and Earth’s Ancient Atmosphere highest that until then had ever been present on Earth. These early fossils are rare and of low diversity, but identifications have been made: most of the material seems to have come from fossil millipedes. A far richer assemblage is known from the famous Rhynie Chert of Scotland, which has been dated at 410 million years in age. The Rhynie Chert deposit has furnished fossils of very early plants, and from these cherts, small fossil arthropods are known as well. The arthropods are mites and springtails, which both eat plant debris and refuse. Mites are related to spiders and are very small in size. Springtails, however, are insects, presumably the most ancient of this largest of animal groups on Earth today. While it might be expected that once they evolved, insects diversified into common elements of the early Devonian fauna, just as they make up the most common element of terrestrial animal life in our time, actually the opposite appears to be true. According to paleoentomologists, insects remained rare and marginal members of the land fauna until nearly the end of the Mississippian Period, some 330 million years ago. Insect flight also occurred well after the first appearance of the group, with undoubted flying insects occurring commonly in the record some 330 million years ago. Soon after the first development of insect flight, the insects undertook a fantastic evolutionary surge of new species, mainly flying forms. This was a classic “adaptive radiation,” where a new morphological breakthrough allows colonization of new ecological niches. But that radiation also took place at the oxygen high 330 million years ago near the end of the Mississippian Period—when oxygen levels had reached modern-day levels and in fact were on their way up to record levels that climaxed in the late Pennsylvanian Period of some 310 million years ago—and was surely in no small way aided and abetted by the high levels of atmospheric oxygen. So were insects the first animals on land? Surely not, according to those who study early terrestrial animal life. That accolade may go to scorpions. In mid-Silurian time, some 430 million years ago, a lineage of proto-scorpions with water gills crawled out of the water and moved about on land, perhaps scavenging on dead animals washed up on beaches. Their gill regions remained wet though, and the very high surface area of these gills may have allowed air respiration of sorts. So

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Out of Thin Air: Dinosaurs, Birds, and Earth’s Ancient Atmosphere Reconstruction of the early terrestrial arthropod Archaeognatha, a flightless true insect. we see a timetable: scorpions out first at 430 million years ago but of a kind that may have been still tied to water for reproduction and perhaps even respiration, followed by millipedes at 420 million years ago, and insects at 410. But common insects did not appear until 330 million years ago. How does this history relate to the atmospheric oxygen curve? The Berner curve for this time interval (shown at the start of this chapter) indicates that the end of the Silurian was a time when oxygen had already reached very high levels—the highest that until then had ever been evolved on Earth—with a high-oxygen peak at about 410 million years ago, followed by a rapid fall, with a rise again from very low levels of perhaps 12 percent at the end of the Devonian (359 million years ago) to the highest levels in Earth’s history by somewhere in the Permian (299 to 251 million years ago). The Rhynie Chert, which yielded the first abundant insect/arachnid fauna, is right at the oxygen maximum in the Devonian. Insects are then rare in the record until the near 20 percent oxygen in the Mississippian-Pennsylvanian, the time interval from 330 million to 310 million years ago—the time of the diversification of winged insects. The correspondence to the Berner curve is remarkable. Let’s formalize this relationship between oxygen levels and the first arthropod land life: Hypothesis 5.1: The conquest of land by vertebrate groups was enabled by a rise in atmospheric oxygen levels during the Silurian time interval. Had atmospheric oxygen levels not risen, animals might never have colonized land.

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Out of Thin Air: Dinosaurs, Birds, and Earth’s Ancient Atmosphere But we know that, following this colonization, animals became seemingly rare during the time of low oxygen. There are three possibilities. First, this seeming pause in the colonization of land was not real at all—it is simply an artifact of a very poor fossil record for the time interval from 400 million to about 370 million years ago. Second, the pause was real—that because of very low oxygen there were indeed very few arthropods, and especially insects, on land. But the few that survived were able to diversify into a wave of new forms when oxygen again rose, some 30 million years later. Third, the first wave of attackers coming from the sea as part of the invasion of land were wiped out in the oxygen fall. Yes, here and there, a few survivors held out. But the second wave was just that—coming from new stocks of invaders, again swarming onto the land under a new curtain of oxygen. Which of these three possibilities is the correct one? The answer now seems clear. As I wrote this book, it seemed that both land arthropods and land vertebrates showed the same pattern, which could not simply be a coincidence. With help from three colleagues—Robert Berner, Conrad Labandeira (the world’s foremost expert on early land arthropods), and Michel Laurin (who provided data on early land vertebrates)—I wrote a scientific paper suggesting the two-part colonization. Let’s formalize this as part of our revisionist history: Hypothesis: 5.2 The colonization of land by animals (arthropods and, as we shall see, vertebrates as well) took place in two distinct waves: one from 430-410 million years ago, the other from 370 onward. Arthropods were not the only colonists to make a new life on land, of course. Gastropod mollusks also made the evolutionary leap onto land but not until the Pennsylvanian (thus they were part of the second wave), when oxygen levels were even higher than at any time during the first wave. The very inefficient gastropod lung required this high oxygen, especially in the transitional phase, when the first lungs in these formally aquatic animals were being formed. Another group that made it ashore was horseshoe crabs, at about the same time that the mollusks landed. But these are minor colonists compared to the group that most concerns this history of life—our group—the vertebrates.

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Out of Thin Air: Dinosaurs, Birds, and Earth’s Ancient Atmosphere THE EVOLUTION OF TERRESTRIAL VERTEBRATES Let’s now turn our attention to the evolution of the first amphibians, the vertebrate group that first colonized the land, or partially did. The fossil record has given us a fair understanding of both the species involved in this transition and the time. A group of Devonian Period bony fish known as Rhipidistians appear to have been the ancestors of the first amphibians. These fish were dominant predators, and most or all appear to have been fresh water animals. This in itself is interesting and suggests that the bridge to land was first through freshwater. The same may have been true for the arthropods as well. The Rhipidistians were seemingly preadapted to evolving limbs capable of providing locomotion on land by having fleshy lobes on their fins. The still-living coelacanth provides a glorious example of both a living fossil and a model for envisioning the kind of animal that did give rise to the amphibians. But another group of lobe-finned fish, the lungfish, also is useful in understanding the transition, not in terms of locomotion but in the all-important transition from gill to lung. The best limbs in the world were of no use if the amphibian-in-waiting could not breathe. There were thus two lineages of lobe-finned fishes, the crossopterygians (of which the coelacanth is a member) and the lungfish. There is controversy about which of these groups was the real ancestor of the amphibians. Whichever it was, there is a record of the first “tetrapods,” animals with four legs, in the latter part of the Devonian, meaning that the crucial transition from a fish with lobed fins and gills to an animal with four legs took place prior to that time. But when? And just how terrestrial were those first tetrapods? Could they walk on land? More importantly, could they breathe in air without the help of water-breathing gills as well? Both genetic information and the fossil record are of use here. But in some ways we are very hampered. Not until we somehow find the earliest tetrapods with fossil soft parts preserved will we be able to answer the respiration question. Happily we have extant representatives of the crossopterygians and lung fish, and some relatively primitive amphibians. Geneticist Blair Hedges has compared their genetic codes in an effort to discover the time that fish and amphibians diverged. The “molecular clock” discov-

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Out of Thin Air: Dinosaurs, Birds, and Earth’s Ancient Atmosphere eries seem to roughly match the fossil record. The split of the amphibian stocks from their ray-finned ancestors (in this case the lobe fins) is dated at 450 million years ago, or at about the transition from the Ordovician Period to the Silurian Period. But this may have simply been the evolution of the stock of fish from which the amphibians ultimately came, not the amphibians themselves. Paleontologist Robert Carroll, whose specialty is the transition of fish to amphibians, considers that a fish genus known as Osteolepis is the best candidate for the last fish ancestor of the first amphibian, and this fish genus did not appear until the early to middle part of the Devonian, or, that is, this final fish ancestor did not appear before about 400 million years ago. However, the first land-dwelling amphibians may have evolved 10 million years before this time, based on tantalizing evidence from footprints recently found in Ireland. A set of footprints from Valentia, Ireland, has been interpreted as the oldest record of limbed animals leaving footprints. But were these footprint makers really on land—or were they water-breathing fish that had evolved four legs to gently pad across the muddy bottom of ponds, as suggested by amphibian expert Michel Laurin in a letter to me in 2006? There are no skeletons associated with this track way, which is composed of about 150 individual footprints of an animal walking across ancient mud dragging a thick tail. This find has set off intense debate, since it predates the first undoubted tetrapod bones by 32 million years! The footprints were found at a time interval when oxygen levels either approached or exceeded current levels, and it is at this same time that the fossil record of insects, recounted above, yielded the first specimens of terrestrial insects and arachnids. Thus, just as high oxygen aided the transition from water to land in insects, so too might it have allowed evolution of a first vertebrate land dweller. The first tetrapod bone fossils are not known until their appearance in rocks of about 360 million years in age, so the transition from fish to amphibians was in this interval between 400 million and 360 million years ago. A rapid drop in oxygen characterizes this interval, and the first tetrapod fossils come from a time that shows oxygen minima on the Berner curve. It is likely, however, that the actual transition from fish to amphibians must have happened much earlier, nearer

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Out of Thin Air: Dinosaurs, Birds, and Earth’s Ancient Atmosphere the time of the Devonian high-oxygen peak but still in a period of dropping oxygen. This scenario fits the proposal that the times of low, or lowering oxygen, stimulated the most consequential evolutionary changes—the formation of new body plans, which the first tetrapod most assuredly was. Most of our understanding about the transition from fish to amphibians comes from only a few localities, with the outcrops in Greenland being the most prolific in tetrapod remains. Although the genus Ichythostega is given pride of place in most discussions of animal evolution as being first, actually a different genus, named Ventastega, was first, at about 363 million years ago, followed in several million years by a modest radiation that included Ichythostega, Acanthostega, and Hynerpeton. Are these forms legged fish or fishy amphibians? They are certainly transitional and difficult to categorize. Of these, Ichthyostega is the most renowned. Its bones were first recovered in the 1930s, but they were fragmentary, and it was not until the 1950s that detailed examination led to a reconstruction of the entire skeleton. The animal certainly had well-developed legs, but it also had a fish-like tail. Nevertheless, the legs led to its coronation as the first four-legged land animal. It was only later that further study showed that this inhabitant from so long ago was probably incapable of walking on land. Newer studies of its foot and ankle seemed to suggest that it could not have supported its body without the flotation aid of being immersed in water. The strata enclosing Ichthyostega and the other primitive tetrapods from Greenland came from a time interval soon after the devastating late Devonian mass extinction, whose cause was most certainly an atmospheric oxygen drop that created widespread anoxia in the seas. The appearance of Ichthyostega and its brethren may have been instigated by this extinction, since evolutionary novelty often follows mass extinction in response to filling empty ecological niches (the traditional view)—and since it was a time of lower oxygen (the view here). And, as postulated in this book, while periods of low oxygen seem to correlate well with times of low organism diversity, just the opposite seems true of the process bringing about radical breakthroughs in body plans: while times of low oxygen may have few spe-

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Out of Thin Air: Dinosaurs, Birds, and Earth’s Ancient Atmosphere cies, they seem to show high disparity—the number of different body plans. Such was the case during the Cambrian Explosion, a time of relatively low species-level diversity but of many kinds of body plans relative to the number of species. So too with the interval of time from 365 million to perhaps 360 million years ago, with many new evolutionary experiments being tried out. Ichthyostega was one of these, and, judging from its geological record, a not too successful one. The fossil record shows that soon after its first appearance, it and the other pioneering tetrapods disappeared. But were Ichthyostega and the two or three allied forms found with it even land-dwelling organisms? The bones of this first amphibian have been reexamined in detail by Cambridge paleontologist Jenny Clack. What she and other anatomists discovered was unexpected. Taken together, the anatomy of Ichthyostega does not seem appropriate for life on land: Ichthyostega would have been very inefficient on land, if it could walk in air at all. This creature was pretty much a fish with legs, rather than an amphibian in the sense of how we know them today. And if it were the first amphibian, we would expect this great evolutionary breakthrough to be soon followed by an adaptive radiation, the rapid proliferation of new species using the breakthrough morphology. But this did not happen. There was a long gap before more amphibians appeared. This gap has perplexed generations of paleontologists and it came to be known as Romer’s Gap, after the early twentieth-century paleontologist Alfred Romer, who first brought attention to it. The expected evolutionary radiation of amphibians did not take place until about 340 million to 330 million years ago, making Romer’s Gap at least 20 million years in length. This radiation took place at a time when oxygen had again risen to, or above, present-day levels, and that did not happen until later than 355 million years ago. A 2004 summary by John Long and Malcolm Gordon similarly interpreted the tetrapods living 370 million to 355 million years ago, the time of a great oxygen drop, as entirely aquatic—essentially fish with legs—even though some of them had lost gills. Respiration took place by gulping air, in the manner of many current fish, and by oxygen absorption through the skin. None were amphibians as we know them today, species that can live their entire adult lives on land. And it ap-

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Out of Thin Air: Dinosaurs, Birds, and Earth’s Ancient Atmosphere pears that none of the Devonian tetrapods had any sort of tadpole stage; they went directly from egg to land dweller without a water-breathing larval stage. PLUGGING ROMER’S GAP? The long interval supposedly without amphibians was “plugged” in 2003 by Jenny Clack with great media fanfare. While looking through old museum collections she came upon a fossil long thought to have been a fish. But more detailed examination showed it to be a tetrapod and, more than that, it was an animal with five toes and the skeletal architecture that would have allowed land life. More importantly, it was within the mysterious Romer’s Gap. The popular press reports of this finding, which was named Perdepes, would have us believe that Romer’s Gap was filled. Hardly. Perdepes may indeed have been the first true amphibian, and it did come from an interval of time within the gap: the fossil comes from the time interval between 354 million and 344 million years ago. But here is where reality sometimes escapes the news. Dating sedimentary rocks is devilishly hard. And more so for non-marine deposits. Perdepes was not an amphibian living the 10 million years from 354 to 344 million years ago. Instead, it is an admittedly (by its discoverer) short-ranging genus living sometime in that interval. Perdepes does not plug the gap—it is a small boat sailing in a vast sea of time. It does tell us that somewhere in the middle of Romer’s Gap a tetrapod did evolve the legs necessary for land life. But did it breathe air? Could it live entirely emerged from the water, even for a few minutes? That we do not know. So let’s demystify the gap, as alluded to earlier in this chapter. Alfred Romer thought that evolution of the first amphibians came about because of the effect of oxygen. But the pathway may not have been that supposed by Romer, who considered that lungfish or their Devonian equivalents were trapped in small pools that would seasonally dry up. In his view the lack of oxygen brought about by natural processes in these pools, and the drying, was the evolutionary impetus for the evolution of lungs. His idea was that seasonally drying swamps spurred the jump to land or smaller freshwater ponds or lakes. Accord-

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Out of Thin Air: Dinosaurs, Birds, and Earth’s Ancient Atmosphere ing to this idea, then, the amphibians-in-waiting were forced out of these pools and into air. Gradually, those animals that could survive the times of emersion from water had an advantage. These fish still had gills, but the gills themselves allowed some adsorption of oxygen. The problem was that the gills quickly dried out. By evolving ever-tighter and water-resistant pockets around the gills, the transition from gill to lung was under way. But a gill is still an evagination, even if in a pocket. There had to be a complete inversion of this system, for a lung is a series of sacs, whereas a gill is a series of protuberances. It may be that the transitional forms had both gills and primitive lungs. The transition from aquatic tetrapods such as Ichthyostega or, more probably, Perdepes, involved changes in the wrists, ankles, backbone, and other portions of the axial skeleton that facilitate breathing and locomotion. Rib cages are important to house lungs, while the demands of supporting a heavy body in air, as compared to the near flotation of the same body in water, required extensive changes to the shoulder girdle, pelvic region, and the soft tissues that integrated them. The first forms that had made all of these changes can be thought of as the first terrestrial amphibians and the Perdepes, found in rocks younger than 355 million years in age, may indeed have been the first of all, according to Long and Gordon. But there may be a continuation of the gap after Perdepes. The great radiation of new amphibian species did not occur until 340 million to 330 million years ago. But when it finally took off, it did so in spectacular fashion, and by the end of the Mississippian Period (some 318 million years ago) there were numerous amphibians from localities all over the world. Let’s reexamine the radiation of amphibian species in the context of atmospheric oxygen levels. A gill is very inefficient when it must act as a lung, and a primitive lung must evolve through many steps before the complex and high surface area surface of internal pockets, all vascularized, with concomitant changes to the circulatory system, is effected. While all these respiratory and circulatory changes are happening, the respiratory system in the stock leading to amphibians would have been less efficient at delivering oxygen than either a gill in water or the complex lung in air that would later be evolved. The high-oxygen peak in the early Devonian would have provided the extra oxy-

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Out of Thin Air: Dinosaurs, Birds, and Earth’s Ancient Atmosphere Reconstructions of the earliest known tetrapods, Tiktaalik (left) and Acanthostega (right), shows how the transition from fish to amphibians took place. In spite of their limbs, both of these were probably fully aquatic and unable to climb onto land because of inadequate (for land life) respiratory and locomotory systems. gen necessary to make this system work, as would have the high oxygen of the latter parts of the Mississippian and Pennsylvanian of 330 million to 300 million years ago. The Berner curve starting this chapter suggests that there was a great drop in oxygen near the end of the Devonian and coincident with this is the Devonian mass extinction, one of the five most severe mass extinctions in Earth’s history. While investigators have been searching for clues to this extinction for decades and have invoked causes ranging from an asteroid impact to climate change, it is not known for sure what the causes of the Devonian mass extinction were. Ammonite workers have long known that at this time the oceans showed a marked change to low-oxygen conditions. The extinction took place over about 2 million years, from 370 to 368 million years ago, at a time when the Berner curve shows a very low level of atmospheric oxygen of about 12 to 14 percent. Here is where the new terrestrial arthropod data from Conrad Labandeira and the new land vertebrate range data from Michel Laurin can help solve the mystery of “Romer’s Gap,” and support the hypothesis presented below that the animal conquest of land happened in two initial phases separated by a time of low oxygen. The figure from our paper is shown here:

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Out of Thin Air: Dinosaurs, Birds, and Earth’s Ancient Atmosphere The black lines mark the geological ranges of arthropods and vertebrates during the crucial time when land animals first invaded the land. The grey shaded region is the time known as Romer’s Gap. These data indicate that the conquest of land was made up of two separate events, with the first largely a failure.

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Out of Thin Air: Dinosaurs, Birds, and Earth’s Ancient Atmosphere Ichthyostega, long thought to mark the appearance of the first land vertebrate, may have been far more fish-like than first thought, and the fact that it lost its gills is not evidence of a fully terrestrial habitat. Long and Gordon point out that today there is a large diversity (over a hundred different kinds) of air-breathing fish. Air breathing has evolved independently in as many as 68 kinds of these extant fish, showing how readily this adaptation can take place. Ichthyostega may not even have been on the line leading to the rest of the tetrapod lineages but may have been on a line that was evolving back into a fully aquatic life style, forced off the land by its primitive lungs and the dropping oxygen levels of the late Devonian. It may even be a descendent of the first true tetrapods, perhaps evidenced by the Valentia footprints of the early Devonian. But while there is doubt that the Valentia footprints came from the first land tetrapod, there is no doubt that the first really diverse land animal fauna, dominated by air-breathing arthropods, appear in the fossil record coincident with the early Devonian oxygen high. This high was followed by a low-oxygen period, when Ichthyostega appeared and then quickly disappeared. Following the extinction of the Ichthyostega, the world had to wait until oxygen again increased before land could be conquered. Let’s thus formalize this view: Hypothesis 5.3: Colonization of the land came in two steps, each corresponding with a time of high oxygen: the first invasion was from 410 million to 400 million years ago and was followed by a second one, beginning from 370 million years ago, that dramatically increased the diversity of land animals with the oxygen high of 330 million to 300 million years ago. The time in between the time of the Devonian mass extinction through the so-called Romer’s Gap had little animal life on land. Romer’s Gap should be expanded in concept to include arthropods and chordates.

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Out of Thin Air: Dinosaurs, Birds, and Earth’s Ancient Atmosphere A comparison of oxygen levels with the diversity of arthropods and limbed vertebrates during the interval of time shown in the previous figure. The far left column, which portrays the number of new terrestrial arthropod orders over the time interval from 450 million to 290 million years ago shows that during the time from 380 million to 350 million years ago, a time interval encompassing Romer’s Gap, there were no new orders. This time interval also coincides with either dropping- or low-oxygen values. THE TIME OF GIANTS Romer’s Gap ended in the Carboniferous Period (split in two in America, where we call it the Mississippian and Pennsylvanian Periods), and its European name comes from the fact that the majority of coal now found on Earth dates from this time. During this time oxygen levels rose in spectacular fashion, and in the last intervals of the Carboniferous and continuing into the successive Permian Period, oxygen levels finally topped out at nearly 35 percent, creating a unique interval in Earth’s history, the subject of the next chapter.

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