How Plant Life Covered the Earth

THE PLANT KINGDOM BEGINS TO COLONIZE THE LAND

ABOUT 18 DECEMBER; ABOUT 965,500 METERS UP THE LINE

We are now almost 97% of the way through our year. Photosynthetic cyanobacteria and green algae have oxygenated the atmosphere and the ocean, although the concentration of oxygen in the atmosphere is not yet up to modern levels. A host of oxygen-using life forms is now undulating and swimming through the ocean. Masses of simple photosynthetic life are there as well, although nothing as exotic and spectacular as the marine animal life of the Cambrian and Ordovician worlds. But a massive transformation of the small planet on which life has originated is at hand. The advent of true plants has arrived. The dry land of that little world is about to be the scene of this transformation. The ones that will transform it have been preceded by various one-celled organisms, including the single-celled algae living on its edges, the first true phototrophs to cling to the land. Multicelled fungi are there, too, nestled in the soil. What will emerge from these simple terrestrial organisms will revolutionize the entire surface of the small planet—and make the evolution of consciousness a greater possibility than it had been before.

The Transition from Water to Land

True land plants are known as embryophytes, eukaryotic, photosynthesizing organisms that go through an embryonic stage, alternate between using sexual and asexual reproduction, and have the ability to synthesize pollen which possesses a durable outer surface, among other traits. Remarkably, they are monophyletic, which means that all of them evolved from a single kind of ancestral organism. Botanists now think that the ancestor from which all land plants evolved was a green algae of the class called Charophyceae. It appears that the first land plants to have diverged from algae were humble liverworts. Recent research has determined that these little plants lived on the eastern shore of Gondwana (in a part of it that is now Argentina) between 473 million and 471 million ybp.¹  How might they have gained a hold there?

The most widespread kind of symbiosis in nature is known as a mycorrhiza. This is the relationship between fungi and plants. In the great majority of such associations, a fungus in the soil latches on to a plant root. The fungus gives the plant mineral nutrients; in most cases, the plant gives the fungus metabolites. It is now thought by certain researchers that roots themselves evolved in order for plants to exploit soil fungi more efficiently.² (In essence, natural selection would have “favored” plants that randomly generated root-like structures.) We must imagine that the soil of the continents in the Ordovician Period’s lower epoch, about 488 million to 472 million ybp, was very poor. Any plants trying to establish themselves in such an environment would have needed considerable assistance. According to a major study, that assistance came from fungi that helped the nascent plant life take in carbon during the process of photosynthesis, acquire phosphorous and nitrogen from the ground, and reproduce more effectively. This symbiosis was so beneficial that those plants that engaged in it flourished, spreading the genomes of the liverworts in which this tendency appeared. The presence of a CO²-rich atmosphere was also beneficial to the new plants.³ Another study has narrowed down the search for the kind of fungi that came to the aid of the liverworts. It appears to have been from the subphylum Mucoromycotina, which existed 475 million ybp, coinciding with the evolution of the simple rootless plants (that nonetheless were able to interact with the fungi that surrounded them).⁴ Of such was the beginning of the world’s grasslands, forests, jungles, and flowers.

What did it take to survive on the dry land? Plants conducted many unconscious “experiments” in land survival. The land of the Ordovician Period provided a variety of microenvironments, and those microenvironments were often filled by plants with unusual body structures, many of which were gone by the end of the Devonian Period, about 359 million ybp.⁵ There were many, many dead-ends, as there always are in the evolution of any life form. A group of major paleobotanists considering the question of dry land survival has concluded:

…it is now apparent that the ability to exist on land is the result of numerous complex interactions that involved the interplay between structural and physiological adaptations in the plants themselves, symbiotic interactions at several levels, and physical and chemical changes in the environment.⁶

Plants were acted upon by the environment, but they also in turn acted upon it. Plants altered the landscape, increased the oxygenation of the atmosphere, extended the carbon and nitrogen cycles into new areas, and in conjunction with the fungi and the microbial life forms, altered the chemical composition of the soil. They occupied environmental niches, but they also created them, in a complex, reciprocal manner. They had begun, unconsciously, not only to conform to the requirements of terrestrial life but to reshape the world to accommodate their needs.

Plants faced the challenge of overcoming desiccation. They lived not just on the land but surrounded by air that was often very dry. Their environment was a non-aquatic one in which water was not always available and the drying effects of wind and sun were now fully in play. The evolution of resistance to desiccation was essential, as was the evolution of the ability of plants to anchor themselves in the ground. The ability to resist desiccation and to hold on to the soil were interconnected. The first primitive plants anchored themselves by means of a stem-like structure called a rhizome. The rhizome could help the plant absorb both water and essential nutrients, thus giving the plant a chance to use water sources other than rain and dew. Some plants evolved the ability to survive extreme drying-out. Others evolved the ability to keep themselves hydrated by internal means, a capacity known as homoiohydry.⁷ 

Land plants are divided into two broad categories. The oldest category is the bryophytes, which contains the liverworts (of course), hornworts, and mosses. These plants are found everywhere on the landmasses of the world, even to some extent in Antarctica. They carpet much of the Earth’s surface, and wrap themselves around innumerable objects. They are absolutely essential to the functioning and health of the environment. They create habitats for innumerable other organisms, contribute nutrients to other life forms, and help stabilize soil in the face of heavy rain, among other functions.⁸ But in the plant kingdom, they have quite literally been dwarfed by the members of the second category—the vascular plants, which helped build the entire biosphere itself.

The Evolution of Vascular Plants

The evolution of vascular plants was as significant a development in the history of life as was the evolution of vertebrates in the animal kingdom. Vascular plants are distinguished from the bryophytes by their more complex internal structures. They contain xylem, tissue which transports water and nutrients from the plant’s roots to all other sections. Within the xylem, two kinds of ducts are used for these purposes. There are tubes called xylem vessels, and water-conducting cells called tracheids, the walls of which are composed of cellulose and strengthened by lignin. Vascular plants also possess phloem, which has sieve-like structures that transport the amino acids and sugars produced by photosynthesis (in sources such as a plant’s leaves) to those sections of the plant, such as the roots and the growing tips of leaves, where the sugars and amino acids will be put to use. Units in the phloem called companion cells assist in this process. (The basic physical phenomenon of osmosis drives water through the sieve-like structures.)⁹ It was the evolution of effective systems of water transport that allowed land plants to gain stature, and in some species attain tremendous heights. The xylem that provides both water conduction and rigid structural support in large plants has a more common name—wood.¹⁰ It was water-conducting capacity and the presence of structural strength that ultimately allowed for the evolution of trees, and all the enormous consequences that have come from their existence. It was the evolution of homoiohydric plants that made forest environments possible. In a part of this forest world a group of tree-living mammals were shaped to survive its severe selection pressures. Those tree-living mammals—the primates—gave rise to us. In a sense, because vascular plants came to exist, so did we.

The structures that define vascular plants did not, of course, jump into being in one step. It is now thought that plants with very simple kinds of water-conducting cells had evolved by the late Silurian Period, somewhere between around 423 million and 416 million ybp.¹¹ Whether these were true vascular plants, however, is a matter of some dispute. Researchers working on the evolution of tracheids have looked to what they call a “living fossil”, Huperzia lucidula, for insight into this process. Huperzia is virtually identical to the fossil remains of a species from the Devonian Period. The paleobotanists examining it have concluded that tracheids evolved in a series of steps involving the development of their characteristic type of cell wall, which includes a secondary wall. In their view, the beginning of this process of secondary cell-wall building can be traced to the advent of what is known as autolysis, the breakdown of the cell’s protoplasm in a programmed cell death. This transforms the tracheid into a non-living duct, one which helps provide structural support for the plant as well.¹²

We can definitely say that vascular plants existed in the early Devonian Period (from around 416 million to about 397 million ybp). The time from the appearance of the first liverworts to the evolution of vascular plants was therefore perhaps 60-70 million years—less than two days on our condensed calendar of the Universe’s history. To oversimplify the matter, the evolution of diverse and increasingly complex vascular plants was brought about by combinations of distinct features brought together in certain ancestral species. These features were in their rudimentary forms, and through reproductive success and speciation, became more elaborated and widespread. (We will discuss the reproductive strategies of vascular plants below.) The formation of root systems, the construction of xylem, the development of leaves, the formation of branches, all started out in the simplest ways.¹³ But in combination they proved to be a powerful synergy. From the standpoint of natural selection, they worked. Do we know the entire story? Not by any means. The most basic feature of vascular plants, water-conducting cells, may even have evolved several times in distinct regions of the Earth. We cannot yet really say. We have a fossil specimen that combines features of both the bryophytes and vascular plants.¹⁴ The full story of how the relatively simple plants gave rise to the relatively more complex ones is still being elucidated. But we do have our resources.

Just as the animal kingdom has areas that are fossil treasure troves, so too does the plant kingdom. One of the greatest collections of fossil plant life is located in Scotland. Known as the Rhynie Chert (named after the village closest to it), it contains a wonderful collection of fossil plants from the Early Devonian Period. The fossils of the Rhynie Chert are extraordinarily well preserved, owing to the unusual physical circumstances of the area in ancient times. These fossils give us a picture of the earliest vascular plants and their environment matched by few other sites. The authors of a study on fossil plants have described this world:

The tallest plants were slightly short of knee height, and most were much smaller…Like fossils from elsewhere, those from the Rhynie Chert document a world of miniature plants with bifurcating, stick-like stems. Most were leafless, but some bore minute hairs and one had short scale-like leaves. Plants grew in dense clumps, an aspect of growth that probably helped to support an upright posture for their thin stems.¹⁵

Not terribly impressive by modern standards, perhaps, but the authors make a highly salient observation about the challenges faced by plant life compared to those faced by the first animal life on land. Animals migrating to the land had body structures deeply shaped by the long evolution of marine life. One could see that they were arthropods or vertebrates, for example. The transition to land represented a modification of pre-existing forms. But land plants, in effect, built entirely new forms, creating types of photosynthetic life for which there were no precedents in the aquatic world. It could, in fact, be contended that plants weren’t so much colonizing the land as they were colonizing the air, pushing themselves upward into it a way that no other life form had before.¹⁶ Seen from this perspective, it is perhaps understandable that the earliest vascular plants were humble, simple organisms. They were a true evolutionary novelty.

The Expansion of Plant Life in the Devonian Period

Just as animal life underwent a major expansion in the Cambrian Period, so did plant life in the Devonian. Over a period from about 400 million to 360 million ybp, the number of plant species exploded. The tallest plants at the end of this time were 40 times taller than the tallest plants at the beginning of it. The soils of the world were becoming something we would recognize, and genuine forests had come into existence. (See below.) Moreover, plants themselves were more structurally complex. The dominant types of plants in the Devonian Period were clubmosses (plants that aren’t actually mosses at all), which are relatives of ferns and conifers, and horsetails, which are plants with large numbers of bristly, thin branches. Paleobotanists estimate that perhaps 50% of all Devonian plant life belonged to these two categories or their related species.¹⁷

It was at the end of this period of expansion that large leaves evolved, although all of the details by which this happened are not yet fully known. Leaves are basically modified branches. They don’t require an entirely new kind of body plan. In effect, leaves are a form of webbing that develops between these modified branches. The large leaves we see on so many plants are called megaphylls, and their evolution was particularly significant. Microphylls—very small leaves—were widespread in the plant kingdom long before megaphylls. Vascular plants had already existed for 40 million years before the general appearance of large leaves. (It appears that leaves evolved independently in a number of different plant groups.) Plants had long had the capacity to produce large leaves, but they had not done so. Why did they begin to appear? An interesting hypothesis about their emergence is that leaf evolution was, in large part, a response to reduced levels of CO² in the atmosphere, levels which declined perhaps as much as 90% in the late Devonian. This decline apparently triggered the latent capacity of plants to form large leaves. One particular study shows that leaf sizes increased 25 fold as the carbon dioxide in the atmosphere diminished. As this CO² decline occurred, the number and density of stomata (surface pores) on vascular plants increased dramatically. Stomata on plants are critically important. They keep plants from overheating (with is fatal to them, of course) by facilitating evaporative cooling. As large leaves began to appear, even though they intercepted much more solar energy, they radiated heat efficiently enough to keep plants in the safe temperature zone. The plentiful stomata of the leaves also served as highly efficient ways of gathering carbon dioxide for photosynthesis, a tremendous advantage in an era when CO² was no longer abundant. All of this was accompanied by the co-evolution of deeper  roots and improved vascular systems, which served to support high rates of transpiration.¹⁸

The evolution of megaphylls was a major event in the history of plants, and indeed the history of life on Earth itself. Leafy plants now unconsciously battled each other for sunlight, and their canopies broadened to take more of it in. Effective cooling mechanisms allowed plants to colonize very warm territories. Leafy plants with deep root systems had a major impact on soil composition. Leafy plants were efficient carbon sinks, removing carbon from the atmosphere, thus lowering average temperatures, and triggering a period of glaciation that waxed and waned across different sections of Gondwana, the most dramatic episodes of which were from 310 million to 290 million ybp, between the Carboniferous and Permian Periods. Levels of oxygen in the atmosphere increased as well, which would greatly facilitate the spread of another life form beginning to make itself felt on the planet—animals. In short, leafy plants were involved in several major feedback loops that had a major impact on every aspect of the planet’s life.¹⁹

The First Forests

The earliest class of vascular plants was the lycopsids, of which the club mosses are the most prominent modern representatives. In the Middle Devonian (around 397 million to 385 million ybp) some of the lycopsids were arborescent (tree-like), with heights ranging from 3 meters to as high as 9 meters. Yet, the groves of these plants were not really true forests, inasmuch as the vegetation lacked deep roots and large leaves, the importance of which we have just examined. The first genuine forests emerged in the Late Devonian, and were filled with trees from the genus  Archaeopteris. These trees were more than 20 meters in height, with abundant, fern-like leaves that undoubtedly created large areas of dense shade, a relatively new feature of life. Such shady areas would have shielded the life forms within them from the Sun’s ultraviolet rays, and would have moderated temperatures as well. A whole new habitat, without precedent on the Earth, was being created: the forest biome. Archaeopteris forests came to dominate lowlands and coastal environments over a huge stretch of territory.²⁰

By spreading so widely, Archaeopteris had a major effect. Because of its deep root system, it helped create new soil at a much faster rate than had been possible before. Ancient forests of these trees generated huge amounts of organic waste products, creating a haven for microbes and invertebrate animals. Archaeopteris almost certainly had an impact on streams, stabilizing their banks and strongly influencing their flow patterns. The spread of forests also caused changes in marine environments, as organic matter in great quantities flowed into the ocean via the rivers and streams. The deposition of this matter may have influenced the Devonian Extinction.²¹ (See below) Archaeopteris did not survive the end of the Devonian Period. But its place as the first genuine tree makes its evolution a milestone, and its impact is still felt.

The Seed Plants Emerge

Botanists call plant reproduction by means of seeds the Seed Habit. It took many millions of years to evolve. The earliest method by which plants reproduced, including the earliest vascular plants, was by disseminating spores. The most primitive method by which this is done is known as homospory, where spores of a single size are spread. A more advanced method, which was used by such plants as Archaeopteris, is called heterospory, wherein two distinct sizes of spore are released by the plant, each of which develops into a gametophyte (a phase of a plant’s growth) that produces either sperm or eggs. But genuine seeds, and seed-bearing plants, did not emerge in the Plant Kingdom until well into the Devonian Period. There is disagreement among paleobotanists about the epoch within the Devonian in which this happened. There are researchers who believe that some plants had established the seed habit by about 385 million ybp at the latest, in the Middle epoch.²² Other scientists place it in the Late Devonian, which ended about 360 million ybp.²³ The different estimates lie in differing interpretations of the fossil record. At either date, it was a momentous development. A seed is a large spore, a megaspore, surrounded by a seed coat. The seeds are stored and nourished in different ways within the two great categories of seed-bearing plants. In the gymnosperms, which include, among others, all the conifers, the seeds are in clusters on the outside of the plant (the pine cone being the most famous example). The megaspore is nourished by an internal structure. There are fewer than 1,000 gymnosperm species in the world²⁴, although gymnosperms are found in vast numbers across much of the planet. The other great plant category is the angiosperms, which now number more than 250,000 species and have become the dominant form of plant life on Earth. In angiosperms a structure called the endosperm nourishes the plant embryo. The reproductive structures in angiosperms are found in their most conspicuous feature—their flowers. The seeds that result from the pollination process are spread in certain angiosperms by another innovation—fruit.

The evolution of the seed habit was the result, as were so many developments in the history of life, of the coming together of a number of different processes that emerged at widely divergent times. Such processes as the evolution of integument (seed coat), methods by which pollen could be captured efficiently, and modifications of the gametophytes characteristic of seed plants took many centuries to develop.²⁵ The gymnosperms are far and away the older of the two seed plant groups. The earliest appearance and phylogeny of the angiosperms is being explored. It now appears that a group of plants scientists have labeled ANITA for convenience (Amborella, Nymphaeales and Illiciales-Trimeniaceae-Austrobaileya) lies at the base of all angiosperms.²⁶ Amborella can be traced back at least as far as 130 million years, and perhaps it is millions of years older. But there is a more than 200 million year gap between the evolution of the gymnosperms and the emergence of the angiosperms. The full story of the evolution of the flowering plants has not yet been elucidated. The earliest gymnosperms were probably present when the first vertebrates began to pull themselves up onto the land. The angiosperms lay far in the future, more than five days away on our condensed calendar.

The Late Devonian Mass Extinction

One of the immense extinction events that have periodically so affected the course of life on Earth occurred at the end of the Devonian. In this extinction the primary life forms affected were marine. Many hypotheses about its causes have been put forward. Several researchers have attributed it to a severe episode of global cooling, one which would have been devastating to coral reefs and tropical fish species. Some have argued that glaciation was the trigger for this cooling, but the timing of the glaciation events in that period of prehistory indicates that they were probably not the direct cause. The sharp reduction in CO² in the world atmosphere (see above) has been implicated by some in this cooling. There are scientists who argue, however, that the decline in carbon dioxide levels was so gradual, taking millions of years to reach their lowest point, that they would not have been sudden enough to trigger an extinction brought on by severe cooling. Severe fluctuations in climate between warmer and cooler periods have been investigated as well, fluctuations attributed to such causes as tectonic activity. But there is no consensus on the issue of climate change as the sole triggering event.

More and more investigators are looking to anoxia, a severe reduction in oceanic oxygen levels (as is suspected in the case of the Cambrian extinction) as the major trigger.²⁷ Recent research has attempted to incorporate the reduction of CO² and the cooling effect it helped promote into a broader framework that includes the massive changes brought about by the evolution of large trees, and the spread of forests to upland areas that had not until that time had any major plant life. In this hypothesis, trees, by generating much more soil than had existed before, caused the land to be a more efficient absorber of carbon dioxide. Coupled with this, trees and other vegetation were producing huge amounts of nutrient runoff, which flooded into the coastal waters. As a result of this runoff, eutrophication—a condition in which excessive amounts of nutrients build up in a body of water—caused algal blooms to spread in the ocean, which in turn caused anoxia and with the anoxia a mass extinction of marine life living in the shallow seas that lay on top of the continental shelves. The formation of black shales, sedimentary rock with a high organic materials content (which still exists along what were once the margins of the Devonian continental landmasses) is indicative of this anoxia.²⁸ This hypothesis seems to be highly plausible, and it takes into account a wide range of synergistically-interacting variables.

It should be noted that there were smaller extinction episodes in the Devonian prior to the major one late in the period. It should also be emphasized that these extinctions caused a prolonged crisis, lasting perhaps 20-25 million years. The loss of marine biodiversity was severe: some 20% of all animal families, and 70-80% of all species. Marine life in shallow areas was devastated, and it is thought that corals never fully recovered from this event.²⁹

The Geography and Climate of the Earth in the Silurian and Devonian Periods

In the Silurian the vast majority of the world’s land was south of the Equator, and there were oceans of considerable size between the major landmasses. In the early Devonian the majority of the world’s land still lay south of the Equator. Gondwana still encompassed the lion’s share of the landmasses, although a continent geologists have dubbed Euramerica had formed. The land of the world was beginning a long process of consolidation, and the oceans between landmasses were closing up gradually. By the late Devonian the consolidation of the world’s landmasses was well under way. There was an extensive ice sheet in the far south of the world.³⁰ Certain researchers now think the Early Devonian was a very warm period, with temperatures of 30 degrees Celsius (around 86 degrees Fahrenheit) the global average. The evidence they have examined seems to indicate a reduction of temperature in the Middle Devonian, then a rebound of warmer temperatures by 375 million ybp. The temperature of the world’s surface water was decreasing by the end of the period.³¹ As we have seen, a major atmospheric cooling was setting in at the end of the Devonian, with ice sheets the result, rather than the cause, of this phenomenon.

The Significance of Plant Life’s Radiation

The evolution of true plants and the radiation of plant life across the world’s landmasses from the Late Silurian through the Devonian Periods was of the utmost significance. As we have seen, the entire world atmosphere was altered, as oxygen levels rose significantly and carbon dioxide levels declined. The effect on the world’s sea life proved to be destructive. New habitats were formed, soil was created, the carbon and nitrogen cycles vastly expanded, and evolution driven in all kinds of new directions. All of this is well-documented. Plants also brought a new phenomenon to the land: fire, as trees were ignited by such causes as lightning strikes. Rivers and streams were altered in their courses and impeded by dense concentrations of vegetation. The whole balance of forces on the world’s surface was being altered. The plants were laying the foundation of the biosphere as we know it.

While the plants were establishing themselves, another revolution was underway. Driven perhaps by brutal competition for resources in the ocean, some animal life forms began making tentative, brief forays on to the shorelines of the ancient continents. There was no guarantee anything would come of these first probes. But enough animals succeeded in surviving and adapting to the land to establish animal life for all time outside the ocean. Many of these animals found shelter and sustenance in the environments being created by the Plant Kingdom. It is to the story of these first land animals that we now turn. Their story eventually became an early chapter in another one: ours.

1.  C. V. Rubinstein, P. Gerrienne, G. S. de la Puente, R. A. Astini, P. Steemans, “Early Middle Ordovician evidence for land plants in Argentina (eastern Gondwana)”,  in New Phytologist, 20 August 2010

2.  Mycorrhizal Associations: The Web Resource http://mycorrhizas.info/index.html

3.  Humphreys, Claire P., Peter J. Franks, Mark Rees, Martin I. Bidartondo,  Jonathan R. Leake, and David J. Beerling , “Mutualistic mycorrhiza-like symbiosis in the most ancient group of land plants” in Nature Communications, November 2010

4.  Bidartondo, Martin I., David J. Read, James M. Trappe, Vincent Merckx, Roberto Ligrone and Jeffrey

G. Duckett, “The dawn of symbiosis between plants and fungi” in Biology Letters, 9 March 2011

5.  Taylor, Thomas N., Edith L. Taylor, Michael Krings, Paleobotany: The Biology and Evolution of Fossil Plants, “The Move to the Land”*

6.  Paleobotany, “The Move to the Land”

7.  Paleobotany, “The Move to the Land”

8.  LiToL: Assembling the Liverwort Tree of Life located at:

http://www.biology.duke.edu/bryology/LiToL/index.html

9.  Kimball, http://users.rcn.com/jkimball.ma.ultranet/BiologyPages/P/PlantTissues.html#Xylem

10. Map of Life - "Secondary xylem (wood) in vascular plants" http://www.mapoflife.org/topics/topic_453_Secondary-xylem-(wood)-in-vascular-plants/

11. Paleobotany, “Early Land Plants with Conducting Tissue”

12. Friedman, William E., and  Martha E. Cook, “The origin and early evolution of tracheids in

vascular plants: integration of palaeobotanical and neobotanical data” in Philosophical Transactions of the Royal Society, pp. 857-868, 2000; Pallardy, Stephen G., and Theodore Thomas Kozlowski, Physiology of Woody Plants, pp. 62-63.

13.  Paleobotany, “Early Land Plants with Conducting Tissue”

14.  Paleobotany, “Early Land Plants with Conducting Tissue”

15.  Kenrick, Paul and Paul Davis, Fossil Plants, pp. 23-25

16.  Kenrick and Davis, pp. 28-29

17.  Kenrick and Davis, pp. 32-35

18.  Beerling, David J.,  “Leaf Evolution: Gases, Genes and Geochemistry” in Annals of Botany, September 2005

19.  Beerling

20. “The First Forests” from Devonian Times, http://www.devoniantimes.org/opportunity/forests.html; Paleobotany, “Progymnosperms”.

21.  Devonian Times

22.  Paleobotany, “Origin and Evolution of The Seed Habit”.

23.  Devonian Times, “Early Seed Plants (lyginopterids)”

24.  The Gymnosperm Database, http://www.conifers.org/zz/gymnosperms.php

25.  Paleobotany, “Origin and Evolution of The Seed Habit”

26.  Yin-Long Qiu, Jungho Lee, Fabiana Bernasconi-Quadroni, Douglas E. Soltis, Pamela S. Soltis, Michael Zanis, Elizabeth A. Zimmer, Zhiduan Chen, Vincent Savolainen & Mark W. Chase “The earliest angiosperms: evidence from mitochondrial, plastid and nuclear genomes” from Nature, 25 November 1999

27.  McGhee, George R., The Late Devonian Mass Extinction: the Frasnian/Famennian Crisis, pp. 132-156

28.  Algeo, Thomas J., and  Stephen E. Scheckler,  “Terrestrial-marine teleconnections in the Devonian: links between the evolution of land plants, weathering processes, and marine anoxic events” in Philosophical Transactions of the Royal Society, 1998

29.  Devonian Times, “Late Devonian Mass Extinctions”

30.  Paleomap Project, http://www.scotese.com/earth.htm

31.  Joachimski, M.M. S. Breisig, W. Buggisch, J.A. Talent, R. Mawson, M. Gereke, J.R. Morrow, J. Day, K. Weddige, “Devonian climate and reef evolution: Insights from oxygen isotopes in apatite” in Earth and Planetary Science Letters, Volume 284, 15 July 2009

*The book Paleobotany is a Kindle edition that is unfortunately not paginated, nor is there an index which indicates pages of the original text in which specific information is located. I can only provide chapter locations in the notes.