by Peter Ward
From about 475 million years ago, when the aquatic green algae began the numerous evolutionary changes that would allow them to attain nutrients—and most critically reproduce—in the combination of air and soil rather than entirely in water, to about 425 million years ago, when the fossil record shows the beautiful unmistakable remains of the first true vascular plants (those with roots and stems), the necessary changes were slow, step-by-step, and largely invisible to the fossil record. The evolution of these first small spiky and leafless plants to the first plant with true leaves took another 40 million years. But once the first leaves appeared, a great revolution of rapid change was unleashed. By around 370 to 360 million years ago, trees were up to twenty-five feet tall.
It took almost a hundred million years for the invading multicellular plants to change from small marine forms to the world-covering forests that were present by the end of the Devonian period. In one respect these plants had a far more significant effect on the land than the long-reigning microbes did, for the multicellular land-plant invasion utterly changed the nature of landforms and soil. It also changed the transparency of the atmosphere, for as more and more plants spread across the land, the restless sand dunes and dust bowls that had been the unceasing landforms of the Earth until that time were transformed. Roots began to hold the grit and dust of the land in place to a far greater extent than did the land-dwelling bacteria, which, as single cells or even thin sheets would have had little strength; as the primitive plants died and rotted in place, thicker and thicker soil began to form, and the ragged, rocky landscape that had always been Earth began to soften. From space the very air itself would have cleared; for the first time the edges of continents and seas, of large lakes and rivers would have become visible from short and great distances alike.
By the Late Devonian, forests had almost completely covered the land, changing the very way rivers moved across the landscape. And in so doing, plants ultimately caused atmospheric oxygen to climb far above the 21 percent found today, to levels as high as 30 to 35 percent—levels that allowed limbed lungless fish to crawl from the sea and survive the hundreds of thousands of years it would take to evolve an efficient, air-breathing lung. All of this conquest and change caused by land plants depended on a single great anatomical innovation—the evolution of the leaf.
LAND VS. SEA
Animal life emerged from the sea in a series of successive invasions, much like a succession of uncoordinated, ragtag, and poorly equipped and adapted armies might do—a few solders at a time, and most dying in the process. The standard explanation for this particular history is that these invasions took place because animals had finally evolved to a point where conquest of land was possible, with the driver being the presence of unexploited resources, less competition, and less predation (for a while, anyway). 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 allowing them to climb out of the water and conquer the land. But our view is that the first conquest of land by animals took place as soon as atmospheric oxygen rose to levels allowing it.
Let us first look at what was required of both plants and animals to allow terrestrialization, the adaptations allowing life on land. Let us 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 familiar to us still: the green, brown, and red algae that are familiar members of any seashore in our world.5 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 taxa. Much of this history is still disputed, especially with the understanding of how abundant and diverse various groups were in the Proterozoic era, even before the Proterozoic snowball Earth.6 While the press loves anything that includes “oldest,” “largest,” or some other absolute, there is a disconnect between the rapid rate of discovery of the antiquity of land plants, their biological affiliations, and the need to more accurately date them. For instance, in 2010 the discovery of the “oldest” land plants was trumpeted based on new fossil discoveries from Argentina.7 These fossils appear to be related to the common liverwort, and were dated at 472 million years in age. But the error on any such dating from such ancient rock is substantial. And besides, while these are indeed quite ancient “vascular” plants, kinds with complex internal transportation systems, in this case definitions of just what a plant is complicate the story. There were a lot of both body plans and species diversity of photosynthesizing organisms we can call plants well before 472 million years ago. Many paleobiologists suspect that a wide diversity of fungi as well as green photosynthesizing microbes to multicellular plants may have been on land earlier than is now considered, and that even a billion years ago there may have been a surprisingly vigorous and numerous assemblage of what collectively could be called plants, if we throw in lichens, fungi, and sheets of green microbes draping wetter landscapes and swamps.8
It was the green algal group, the Charophyceae, that ultimately gave rise to photosynthetic multicellular land plants that all can agree are true “plants,” the kind of organism being described in most stories about oldest plants. Many obstacles had to be overcome; perhaps first among these was the problem of desiccation. A green alga washing ashore from its underwater habitat quickly degenerates and dies, as it rapidly desiccates in air, for there is no protective coating. But these green algae produce reproductive zygotes that have a resistant cuticle, and this same cuticle may have been used to coat the entire plant in the move onto land. But the evolution of this 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 because there doesn’t appear to be any differentiation in the higher forms. Additionally, this symbiotic relationship 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. One solution is to simply lay 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-lying carpets 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 acquisition of much more light, especially in an ecosystem where there is competition between numerous low-growing plants, and various harder materials were incorporated by early plants to allow first stems and finally tree trunks. Concomitant 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, ensuring 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. If the first terrestrial plants evolved from a small group of predominantly freshwater green algae, as is the most accepted opinion, they certainly did so without a lot of paleontological fanfare or e
vidence in the fossil record. They left behind a very fragmentary fossil record. Unearthing this fossil record (in both the literal and philosophical sense) required detective-like sleuthing of the first order.
The recovery of the fossil record of the earliest complex land plants began with a seminal 1937 paper, and for much of the discussion here, as well as the scientific history, we are indebted to our acerbic but brilliant colleague and friend, David Beerling of the University of Sheffield, who in his revolutionary book The Emerald Planet rather unapologetically complains that his field of Earth history, paleobotany, “gets no respect” in an almost comically Rodney Dangerfield way. But he is totally correct, in the sense that while dinosaurs and dinosaur hunters garner the lions’ (raptors’?) share of scientific interest and glory, in fact, plants remain by far the most important group of organisms on Earth in terms of their effect on the history of life. A book about how our planet changed as a result of the “history” of life should have one chapter about animals and all the rest about plants. In any event, much of our take on the role of plants overtly comes from David’s work, and especially his book.
The history of how land plants took over the terrestrial ecosystems, and in so doing changed the nature of life on Earth because of their effects on global temperature, ocean chemistry, and atmospheric inventory, can start with paleobotanist William Lander. Lander is the scientist who made these first discoveries and found the then-oldest-known land-plant fossil remains in 417-million-year-old rocks in Wales. (At the time these dates were completely unknown. In fact, the absolute age dates that we now use are a fairly new discovery.) While the 417-million-year-old fossils from Wales were thought to be the oldest record of land plants, soon other fossils began to appear in even older rocks, later dated as being 425 million years in age, also found in Wales.
This oldest plant was named as Cooksonia. From these early beginnings, land plants underwent a curiously long and much-delayed evolutionary radiation. Between 425 and 360 million years ago plants underwent their own version of the Cambrian explosion in animals; only this time it was an explosion of plants on land. But the newest view is that for at least 30 million years following the first appearance of land plants, not one of them had leaves. It now looks as if leafy plants were not firmly established until 360 million years ago.
There is indeed a mystery as to why leaves took so long. Even after the first appearance of leaves, it then took another 10 million years until they became widespread and distributed both in diversity and abundance throughout the planet. This extremely long period of time between the appearance of a land plant and that of a land plant with leaves can be compared with the much faster appearance of large and diverse mammals following the extinction of the dinosaurs, 65 million years ago. For the latter, it took no more than 10 million years for the major stocks of land mammals to appear, and appear not only in diversity but also in abundance and large size.
Once again we must look at the role of evo-devo and genes to understand this particular evolutionary history. Plants had to first evolve the genetic tool kit required to assemble leaves, but then they had to be able to use it, and the use seems to have been delayed. The best evidence to date indicates that plants with leaves had the genes necessary to build leaves, but then had to await changes within the environment in which they lived. In this particular case it was not a wait for the rise in oxygen—as it was for animals—but something entirely different: a wait for a drop in atmospheric carbon dioxide, as least according to the latest paleobotanical interpretations of the twenty-first century.
Here again is an example where the modern day can inform past history—our history of life. Experiments on living plants show that they are extremely susceptible to the level of carbon dioxide in which they live. All plants need carbon dioxide to undergo photosynthesis, but to do this, the plant has to absorb carbon dioxide out of the atmosphere around it. If there is a leaf, carbon dioxide has to enter through the otherwise impenetrable outer wall of the leaf. This is done through tiny holes called stomata. But there is a two-way street here. While carbon dioxide can enter through the stomata, water within the plant can also exit through the same holes. A theme that recurs over and over in the evolution of land animals and land plants is that desiccation remains one of the major obstacles to life. In high carbon dioxide settings, there are very few stomata. But when carbon dioxide is reduced, the number of stomata increases.
One would think that high levels of carbon dioxide would be the most optimal condition for any land plant. In terms of this physiology, in fact this is true. However, we know that carbon dioxide is one of the principal greenhouse gases. Times of high carbon dioxide are times of high heat on the surface of the Earth.
Plants have an exquisite signaling system, allowing fully grown and mature leaves to communicate with leaves just undergoing first growth and development. The larger leaves inform the smaller about the optimal number of stomata to produce for the environmental conditions they are all living in. If we go back in time to observe the levels of carbon dioxide in the atmosphere when land plants first began their evolutionary rise, over 400 million years ago, we see a period of extremely high carbon dioxide levels—and thus an extremely warm planet. So warm, in fact, that heat itself may have been a major brake on plant evolution and ecological success. The same stomata that let carbon dioxide in also allow the removal of water from the inside of the plant—and it is this process that actually cools the plant.
A little desiccation cools a plant, but a lot kills it, and as in so much, success comes from balance. In a very hot climate, a lot of cooling is needed. But in a high-CO2 atmosphere, a plant needs very few stomata to handle its carbon dioxide needs. Yet the same number of stomata necessary for “ingestion” or carbon dioxide into the body of the plant might be too few to allow cooling—especially if the stomata are located on a large, flat surface—like a leaf. In such a case, a large leaf with few stomata will cause overheating to the point of death. This is the newest view of why it took so long for leaves to evolve. The genetic tool kit necessary to make them was in place. But the atmosphere had so much CO2 in it that plants did not dare build leaves.
The new early twenty-first-century work of David Beerling and others suggests that it took a drop in carbon dioxide before leaves could be viable at all. Before this time any leaf would be a death sentence for the plant. Thus it was that it was only after 40 million years following the first appearance of Cooksonia that leaves as well as better internal plumbing systems within the plant (including new and deeper boring roots) first appeared. This latter, the ability to send roots to ever-greater depths, had two advantages for plants. First, deeper roots provided more stability. Second, deeper rooting gave greater access to both soil nutrients and water. The first plants have extremely shallow rooting systems. But once leaves evolved, roots also began to change and evolve to go ever deeper into the soil.
By the Devonian period, we see the evidence of roots that extended downward for as much as three feet. The new, deeper roots vastly increased the weathering of rocks beneath these early plants. As more plants lived in the soil, more and more of them died, adding organic material to the soil. At the same time, ever-deeper penetration by roots vastly increased both mechanical and chemical weathering of rocks beneath. This had important consequences for the makeup of the atmosphere as well as the temperature of the Earth.
We have seen that perhaps the most important driver removing carbon dioxide from the atmosphere is the weathering of silicate rocks, the granites, and sedimentary and metamorphic rocks with a granite-like chemical composition, a rock type rich in the element silicon. The reaction of chemically weathered silicate rocks on land is such that molecules of carbon dioxide are removed from the atmosphere. This is called the biotic enhancement of weathering, and it would have been taking place as soon as tree-rich forests began covering the land, about 380 to 360 million years ago. As roots went deeper into silicate rocks beneath, the granite and compositionally grani
te-like rocks of the continents began to weather much more quickly than the time before forests, and this caused carbon dioxide levels to plunge, and plunge quickly.
The lowering carbon dioxide levels allowed ice to appear on the continents, first only at the highest latitudes, but eventually at ever-lower latitudes. But the juggernaut of evolution favored taller trees, and with taller trees came deeper roots. Plants became taller, roots went deeper, and the planet became ever colder. The evolution of land plants with their ever-deeper rooting in fact plunged the planet into one of the longest-running ice ages ever in Earth history, one that began in the Carboniferous period. But before this happened, the world would have been warm, lush, and rich in plant-friendly levels of carbon dioxide. In short, the continents, newly green with vascular plants, would have been like a gigantic, stocked, but customer-free grocery store. Free food, if only you can get into the store. Or in this case, out of the sea and onto land—to stay.
THE FIRST LAND ANIMALS
The major problem facing any would-be terrestrial animal colonist was water loss. All living cells require liquid within them, and living in water does not provide 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 antagonistic to the needs of a respiratory membrane. So here we are twixt the devil and the deep blue sea: build an external coating that resists desiccation, an advantage, but at the same time risk death from suffocation. The alternative was to evolve a surface respiratory structure that allowed the diffusion of oxygen into the body, but caused increased risk of 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, plant, and protozoan 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.
