by Peter Ward
The oldest fossil land animals all appear to have been small arthropods resembling modern-day spiders, scorpions, mites, isopods, and very primitive insects. It is unclear which of these quite different arthropod groups was first, but being first did not last long, as all of these groups are found in the fossil record in ancient deposits. Identifying these first land animals has necessarily relied on a fossil record that is notoriously inaccurate when it comes to small terrestrial arthropods. All of these groups have very weakly calcified exoskeletons, and thus are rarely preserved as fossils. By the Late Silurian or Early Devonian time intervals, however, or around 400 million years ago, 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 their successful transition from marine animals to successful terrestrial animals. Of all 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 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, as well as taking in oxygen by even their primitive lung structures.
Of the phyla that made it onto land, which included many kinds of arthropods, as well as 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 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 such 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 series of openings in the carapace. This is a passive lung in that there is no current of air “inhaled” into these lungs. And because of this, they are dependent on some minimum oxygen content.
It is well known that 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-O2 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 gills may be more efficient at garnering oxygen than the insect respiratory system, which is composed of tubelike trachea. Like 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.
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 is from late Silurian rocks in Wales, about 420 million years in age, near the end of the Silurian period—and a time when oxygen had already reached very high levels, the highest that had up to that time ever been evolved 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. This deposit has furnished fossils of very early plants, as well as the fossils of small arthropods. Most of these arthropods appear to be related to modern-day mites and springtails, which both eat plant debris and refuse, and thus would have been well adapted to living in the new land communities composed mainly of small, primitive plants. Mites are related to spiders. Springtails, however, are insects, presumably the most ancient of this largest of animal groups now on Earth today. It might be expected that once evolved, insects diversified into the most abundant and diverse of terrestrial animal life in our time. However, this was not the case, and in fact just 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—when oxygen levels had reached modern-day levels, and in fact were on their way up to record levels, which climaxed in the Late Pennsylvanian period of some 310 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 this first development 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, and was surely in no small way aided and abetted by the high levels of atmospheric oxygen.
Insects were also not the first animals on land. 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 freshwater swamps and lakes that they were adapted to and moved onto and then about on land, perhaps scavenging on dead animals such as fish washed up onto beaches. Their gill regions remained wet, and the very high surface area of these gills may have allowed respiration of sorts. They certainly did not have functional lungs, only semi-serviceable gills.
Here is the timetable as we now know it: scorpions onto land about 430 million years ago (MA), but of a kind that may have been still tied to water for reproduction and perhaps even respiration; followed by millipedes at 420 MA, and insects at 410 MA. But common insects did not appear until 330 MA. How does this history relate to the atmospheric oxygen curve?
The newest estimates of atmospheric oxygen levels at this time indicate that a high oxygen peak occurred at about 410 million years ago, followed by a rapid fall, with a rise again from very low levels (12 percent) at the end of the Devonian to the highest levels in Earth history by somewhere in the Permian when it exceeded 30 percent (compared to 21 percent today). 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 (according to paleontologists who study insect diversity) until the rise to near 20 percent in the Mississippian-Pennsylvanian, the time interval from 330 to 310 million years ago—the time of the diversification of winged insects.
The conquest of land by various vertebrate groups was seemingly enabled by a rise in atmospheric oxygen levels during the Ordovician-Silurian time interval. Had that not happened, it is possible that the history and kind of animals that did colonize land might have been much different—or it might never have happened at all; animals might never have colonized land. We also know that following this colonization, animals became seemingly rare, during the subsequent time of low oxygen.
There are three possibilities for this observed pattern of fossil abundances and diversity. First, this seeming pause in the colonization of land is not real at all; it is simply an artifact of a very poor fossil record for the time interval from 400 to about 370 million years ago. Second, the “pause” is real; because of very low oxygen there were ind
eed 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 waves 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 curtain of oxygen. The colonization of land by animals (arthropods, and as we shall see, vertebrates as well) thus took place in two distinct waves: one from 430 to 410 million years ago, the other from 370 onward.
Arthropods are not the only colonists making a new life on land of course. Gastropod mollusks also made the evolutionary leap onto land, but did not make this transition 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. Another group that made shore were 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. But amphibians did not just burst out of the sea. They were the culmination of a long evolutionary history, and before they emerge onto land in our narrative, let us look at the Devonian period, a time long called the Age of Fish. To do this we want to feature one of our favorite field areas, the Devonian-aged Canning Basin of Western Australia, where we two coauthors spent multiple field seasons in one of the most extraordinarily beautiful (if hot!) places on the planet. The Canning Basin preserves the world’s best fossilized barrier reef system. It is as if the Great Barrier Reef were suddenly turned to stone and the water removed. While much of the work to date has been in studying that giant Devonian reef, in fact the rocks deposited in deeper water nearby during the Devonian Period have yielded some of the most extraordinary of all fossil studies that certainly need to be featured in any self-styled “new” history of life.
JOHN LONG AND THE GOGO FORMATION FISH
While common in salt water to freshwater and all salinities in between, in fact fish fossilize all too rarely. It usually takes a low oxygen sea bottom where a dead fish is rapidly buried for an entire fish to be preserved. Scavengers are all too efficient at tearing fish corpses apart. But here and there beautiful fish fossils can be preserved. Sometimes they appear in two-dimensional form, as from the Eocene-aged Green River shale of Colorado, perhaps the place where more fish fossils have been found than in any other locality. But other fish parts, especially big fish skulls, are sometimes preserved in large round balls of rock called concretions. These cannonball-like objects are often found in sedimentary rocks, and they can contain the most beautifully preserved of fossils. Such preservation is found in strata from northern Ohio of Devonian age, where gigantic fish skulls have been found for a century, including the skull of one of the iconic monsters, an ancient fish called Dunkleosteas, lately featured in the usually cheesy Discovery Channel programs about ancient predators. But such preservation is also found in a curiously named rock formation called the Gogo Formation, the same age rocks (but deeper water equivalents) of our own Devonian Age research. Among these cannonball concretions are some of the most important fossils ever found. They give us a window of the platform from which our amphibian ancestors ultimately emerged. To understand the conquest of land we first have to know the Devonian world of fish in all its diversity and complexity. In recent years Australian paleontologist John Long, a professor at Flinders University in Adelaide, Australia (but also with a long professional stint at the Los Angeles County Museum of Natural History), has taken new high-resolution-scanning technology to make breakthrough discoveries about the ancestry of all modern fish, as well as the lineages in deep time that are in our own DNA.
Long is a rarity in Australian academics in having a successful and thriving career in science outreach, and is the author of numerous books. But Long’s “day job” has shown us that the evolution, morphology, diversity, and ecology of Devonian age fish was far more complex than is now portrayed in textbooks. By pioneering the use of imaging technology such as CT scanning, which bombards fossils with energy sufficient to produce 3-D slices of the fossils, Long has literally looked into the heads of the various fish groups.
The four “traditional” fish groups—today represented by lampreys and hagfish; sharks; the most diverse, the “bony” fish; and an entirely extinct group, the placoderms (the first jawed fish)—are far more complicated in all aspects than they have been long portrayed. Long’s major discoveries from his field expeditions to the Gogo fossil sites included the first complete skull of one of the first bony fish, named Gogonasus, which showed that this species had large spiracles, or holes, previously unknown in fish on top of its head. But the most surprising discovery—beyond demonstrating a hitherto unknown diversity of other kinds of early fish, including new types of lungfish (closely related to the fish that ultimately crawled onto land) as well as strange fish called arthrodires—was the discovery of the first Devonian fishes showing embryos inside them. This latter discovery was the first time that reproduction by internal fertilization was demonstrated, as well as the oldest evidence for vertebrate viviparity yet discovered. One of his specimens was the only known fossil to show a mineralized umbilical structure linked to the unborn embryo. Long used his new high-tech methods to remarkably preserve 3-D muscle tissues, nerve cells, and microcapillaries, all new kinds of detail from fossil fish. But most important for understanding the move onto land, his soft tissue discoveries gave entirely new insight into how a fish could evolve ancestors that could walk—even upright on two legs.
THE EVOLUTION OF TERRESTRIAL VERTEBRATES
The transition of our own group from purely aquatic organisms to true terrestrial inhabitants began with the evolution of the first amphibians. The fossil record has given us a fair understanding of both the species involved in this transition and the time it happened. A group of Devonian period bony fish known as rhipidistians appears to have been the ancestors of the first amphibians. These fish were dominant predators, and most or all appear to have been freshwater 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 are 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 are 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.
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 in this transition, considers a fish genus known as Osteolepis 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 before about 400 million years ago.
The first land-dwelling amphibians may have evolved at this time, based on tantalizing evidence from footprints found in Ireland. A set of footprints from Valentia has been interpreted as being the oldest record of limbed animals leaving footprints, dated at about 400 million years in age. But there are no skeletons associated with this trackway, which is composed of about 150 individual footprints of an animal walking across ancient mud dragging a thick tail. This find has set off debate, since it predates the first undoubted tetrapod bon
es by 32 million years. Interestingly, however, the trackway dates to 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 the 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 uncertainty about the age of the first vertebrate footprints on land was slightly alleviated by a discovery made in 2010, of a second set of tracks that was discovered to be 395 million years in age. They were preserved in marine sediments of the southern coast of (now) Poland. They were made during the Middle Devonian period. The tracks, some of which show digits, are thus 18 million years older than the oldest-known tetrapod body fossils. Additionally, the tracks show that the animal was capable of a type of arm and leg motion that would have been impossible in the more fish-like tetrapods and near tetrapods, such as the aforementioned Tiktaalik and its probable descendant, Acanthostega.
The animal that produced the tracks was large for the time: some estimates peg it at more than eight feet long. Perhaps this creature and its ilk were scavengers on the tidal flats, feeding on washed-up marine animals stranded by the tide, or the numerous land arthropods, including scorpions and spiders.
