by Peter Ward
The first tetrapod bone fossils are not known until rocks about 360 million years in age, so the transition was in this interval between 400 and 360 MA. A rapid drop in oxygen characterizes this interval, and the first tetrapod fossils come from a time that shows minimal oxygen on the Berner curve. It is likely, however, that the actual transition from fish to amphibian must have happened much earlier, nearer the time of the Devonian high-oxygen peak but still in a period of dropping oxygen.
Most of our understanding about these crucial events comes from only a few localities, with the outcrops in Greenland being the most prolific in tetrapod remains. Although the genus Ichthyostega is given pride of place in most texts 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 Ichthyostega, Acanthostega, and Hynerpeton.
Of these, Ichthyostega was the most renowned—until Tiktaalik, that is. Yet the new notoriety of Tiktaalik is a bit misplaced. It was a fish. Ichthyostega was something else. An amphibian, 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 had well-developed legs, but it also had a fish-like tail. Later that further study showed that this inhabitant from 363 million years 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 that was soon after the devastating Late Devonian mass extinction, whose cause was most certainly a drop in atmospheric oxygen 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. But the success of Ichthyostega and its brethren was short-lived: the fossil record shows that within a few million years after its first appearance, it and the other pioneering tetrapods disappeared.
The appearance of Ichthyostega and its late Devonian brethren poses crucial questions. If these were indeed the first terrestrial vertebrates, why wasn’t there a succeeding “adaptive radiation” of their descendants? But this did not happen. Instead there is a long gap before more amphibians appear. This gap has perplexed generations of paleontologists. In fact it came to be known as Romer’s gap, after the early twentieth-century paleontologist Alfred Romer, who first brought attention to the mysterious gap between the first wave of vertebrates invading the land and the second. In fact, the expected evolutionary radiation of amphibians did not take place until about 340 to 330 million years ago, making Romer’s gap at least 30 million years in length.
A 2004 summary by John Long and Malcolm Gordon similarly interpreted the tetrapods living in the 370- to 355-million-year-old interval, the time of a great oxygen drop, as entirely aquatic, essentially fish with legs, even though some of them had lost gills. Respiration was by gulping air in the manner of many current fish, and oxygen absorption through the skin. They were not amphibians as we know them today—species that can live for their entire adult lives on land. And it appears that none of the Devonian tetrapods had any sort of tadpole stage.
The long interval supposedly without amphibians was “plugged” in 2003 by Jenny Clack. While looking through old museum collections she came upon a fossil misinterpreted as a fully aquatic fish, but which she showed to be a tetrapod with five toes and the skeletal architecture that would have allowed land life. This fossil was given a new name, Pederpes, and it lived long after Tiktaalik. It indeed may have been the first true amphibian, and it did come from the time interval between 354 and 344 million years ago known as Romer’s gap. But like so much about the past, sometimes fossils raise more questions than answers. It does tell us that somewhere in the middle of Romer’s gap, a tetrapod did evolve the legs necessary for land life. However, it is still not known if it could breathe air or whether it could even emerge from the water for even for a few minutes.
Alfred Romer thought that the evolution of the first amphibians came about because of the effect of oxygen. Romer considered that lungfish or their Devonian equivalents were trapped in small pools that would seasonally desiccate. He thought that the lack of oxygen brought about by natural processes in these pools, as well as the drying, was the evolutionary impetus for the evolution of lungs—the amphibians-in-waiting were forced out of the pools and into the 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. It may be that the transitional forms had both gills and primitive lungs.
The transition from aquatic tetrapods such as Ichthyostega or, more probably, Pederpes, passed through the Tiktaalik grade of fish organization and involved changes in the wrists, ankle, 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. Yet a great radiation of new amphibian species, which would be expected soon after the evolution of a respiratory system that could breathe air, not water, and limbs that could move a heavy body across land, did not occur until 340 to 330 million years ago. But when it did finally take 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.
The evidence at hand suggests that the evolution of the amphibian grade of organization, essentially a fish that came on land, may have taken place twice, or even three times, the first being some 400 million years ago as evidenced by the Valentia footprints as well as the Tiktaalik fossil discovery, and the second some 360 million years ago, and the last some 350 million years ago. 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. In fact, we now know that over a hundred different kinds of modern fish use air breathing (as well as gills) of some sort. Air breathing has evolved independently in as many as sixty-eight 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 tetrapod lineages, but one that was evolving back into a fully aquatic lifestyle, forced off the land by its primitive lungs and the dropping oxygen levels of the Late Devonian.
Artist rendition of Tiktaalik, created for the Animal Planet program Animal Armageddon. (Art by Alfonse de la Torre in conjunction with Peter Ward, used with permission from Digital Ranch Productions, Rob Kirk)
It has long been assumed that the first amphibians were freshwater forms, and indeed this has been a major question in the history of life: was the route to land through freshwater first, or did some organisms evolve directly from salt water to air? However, new research has shown that early lobe-finned fish and lungfish—the immediate ancestors of the first tetrapods—were most often marine forms. Similarly, paleontologist Michel Laurin has noted several classical Carboniferous-aged localities that have yielded early amphibians and that have long been considered to represent freshwater deposits may in fact have been either marine or near marine deposits, such as intertidal or lagoonal environments. However, it seems equally sure that the famous Tiktaalik and some early amphibians such as Ichthyostega and Acanthostega have been interpreted as freshwater forms. It is thus likely that these first amphibians and near amphibians inhabited a wide variety of environments: salt water, freshwater, and terrestrial environments in the Late Paleozoic. T
his brings up an interesting point. Modern amphibians are intolerant of salt water; their skin, which takes in oxygen when immersed in water, cannot deal with the salt. This must be a trait evolved much later in their history.
In summary, colonization of the land came in two steps, each corresponding with a time of high oxygen. The time in between, the time of the Devonian mass extinction through the so-called Romer’s gap, had little animal life on land. Thus Romer’s gap should be expanded in concept to include arthropods as well as chordates.9 It finally ended in the Carboniferous period (split in two in America, where we call it the Mississippian and Pennsylvanian periods), when oxygen levels rose in spectacular fashion, and in the last intervals of Carboniferous and then continuing into the successive Permian period, when the oxygen levels finally topped out at nearly 32 to 35 percent, creating a unique interval in Earth history. A time of giants.
CHAPTER XI
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The Age of Arthropods: 350–300 MA
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A staple of Hollywood in the immediate post–World War II interval, the dawn of the nuclear age, was the “giant-creature-produced-by-A-bomb-radiation” movie. Sometimes these monsters were examples of some kind of giant extinct life, often thawed out of some 70-million-year-old glacier. More often they were a familiar insect, scorpion, or spider of giant size. While easy to dismiss as “unscientific,” these movie monsters do let us pose a legitimate question about the maximum size that can be obtained by any given animal body plan. Since large size is often a protection against predation, it seems that most animals grow as large as they can. What ultimately limits the size of animals? In the case of terrestrial arthropods (spiders, scorpions, millipedes, centipedes, and insects among a few other more minor groups) it is clear that two aspects of the arthropod body plan limited and still limit them from attaining large mammal-like size.
One of these is the exoskeleton. Because of scaling properties and strength of the material called chitin, the hard-part material that makes up most of the arthropod exoskeleton, a giant ant, spider, scorpion, or mantis of even human size would collapse, its walking legs snapping. The second aspect of arthropod design that limits size is respiration. Insects, spiders, and scorpions appear to be limited in size by the degree to which oxygen can diffuse into the innermost regions of their body. Today, no insect is bigger than about six inches in body length. In the past, however, much larger forms than this did exist, during the interval of the highest oxygen in Earth history.
THE CARBONIFEROUS-PERMIAN OXYGEN HIGH
While the various specialists modeling past atmospheric composition differ in values, their respective models suggest for past time intervals that there is unanimous agreement that oxygen reached extraordinarily high values in the time interval from about 320 to 260 million years ago, with maximal values occurring near the end of this interval. The Carboniferous period (again in North America subdivided into the Mississippian and Pennsylvanian periods) and the first half of the subsequent Permian period were the times of high oxygen, and the biota of the world at that time has left clear evidence of the high oxygen. Insects from the time present the best evidence.
The Carboniferous oxygen high (and much else as well) was well described by Nick Lane in his 2002 book Oxygen.1 In a chapter titled “The Bolsover Dragonfly,” Lane wrote about a fossil dragonfly discovered in 1979 that had a wingspan of some twenty inches. An even larger form, with a thirty-inch wingspan, is also known from fossils of this Carboniferous time, a beast aptly named Meganeura, yet another dragonfly. It was not only the wings that were large. The bodies of these giants were also 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 twenty-inch wingspan was indeed a veritable giant. In comparison, today’s dragonflies may reach four inches in wingspan, but more commonly are smaller. Other giants of the time included mayflies with nineteen-inch wingspans, a spider with eighteen-inch legs, and two-yard-long (or longer) millipedes and scorpions. A three-foot-long scorpion could weigh fifty 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.
In the case of insects, it is the nature and efficiency of the insect respiratory system in extracting oxygen and getting it into the most interior recesses of its body that dictates maximum size. All insects use a system of fine tubes, called trachea. Air actively ventilated into the tubes where it then diffused into the tissues. Air is pulled into the canals either by rhythmically expanding and contracting the abdominal region or by using the flapping of wings to create air currents around the tracheal opening. The tracheal system is thus made more 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 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. Gauthier Chapelle and Lloyd Peck examined two thousand 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.2
It was not only higher oxygen that allowed the existence of giant dragonflies. The actual air pressure is presumed to have been higher as well. 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. There was clearly more oxygen in the air than now. The question is why.
Earlier we saw that oxygen levels are affected mainly 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 the Earth’s highest oxygen content, must have been a time of rapid burial of large volumes of carbon and pyrite, and the 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 330–260-million-years-old time of high oxygen. It turns out that 90 percent of the Earth’s coal deposits are found in rocks of that interval. The rate of coal burial was much higher than any other time in Earth history—six hundred 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 buildup of carbon, leading to the unique maximum of oxygen levels, was the coincidence of several geological and biological events that culminated in the vast carbon deposit accumulations. 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 gig
antic linear mountain chain arose along the suturing of these continental blocks.
On either side of this mountain chain great floodplains arose, and the configuration of the mountains also produced a wet climate over much of the Earth. Newly evolved trees colonized the vast swamps and their 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. And 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, the bacteria that do this job take their own sweet time.3 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.
Decomposition of trees is accomplished by 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. Back in the Carboniferous, many or perhaps all of the bacteria that decompose wood were not yet present,4 with the key to this the seeming inability of microbes to break down the main structural component of wood, the material lignin. Trees would fall and not decompose back then. Eventually sediment would cover the undecomposed trees, and reduced carbon was 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.
