Like the explosive arrival of marine animals in the Cambrian, the mushrooming of plants in the Devonian was a step change. By the end of the period all major types of vascular plants had appeared: lycopods, fern-like plants, horsetails, the extinct progymnosperms and various seed-bearers, all ‘fully formed’ and testifying to ‘rapid, highly divergent increases in complexity’ (Bateman et al. 1998). It was a ‘novelty radiation’ rather than organisms diversifying at comparatively low levels of classification. What emerged fully developed was ‘an extraordinary array of complex organs and tissue systems’ (Kenrick & Crane 1997): specialised sexual organs, stems with an intricate fluid transport mechanism, structural tissues, pores for controlled gas exchange (stomata), leaves and roots of various kinds, diverse spore-bearing organs (sporangia), and seeds.

Since fossils of one type commonly appeared at the same time and in the same place as other types, it is clear that the plants occurred as part of communities. Invertebrates too were components of the fledgling ecosystems. Organisms were not competing with each other in overcrowded environments where only the fittest survived, but living in balance with each other, interdependently. Species diversity was initially low.

The oldest known forest is the Gilboa forest of New York State, dating to the late Middle Devonian. It presents a dramatic contrast to the marshes of earlier times. Although the plants still grew in a water-logged soil, they were proper trees, with tapered pith-filled trunks that rose to an estimated height of 9 metres or more.The tallest of them was the fern-like Eospermatopteris. Their bulbous bases gave them a low centre of gravity, so that they did not need deep roots to give them stability, though they must have had some. There were also smaller trees and shrubs. Invertebrates included centipedes, spiders, mites and bristletails.

The tree habit appeared independently in several other lineages – lycopsids, progymnosperms, Pseudobornia and horsetails – and all but the horsetails achieved this in the interval from Middle to Late Devonian. This puzzling phenomenon, where Nature seems to invent essentially the same feature more than once is called convergence, or parallel evolution. Pervasive in all large-scale phylogenies, amongst all types of organism and in relation to innovations of every degree of complexity, it is one of the strongest kinds of evidence against Darwin’s theory. Another example of convergence is photosynthesis, a highly complex process which occurs not only in plants but also in some bacteria, algae and protists – entirely separate biological kingdoms. Within plants, major innovations such as stomata, sporangia, heterospory (the production of two types of spore), leaves, roots and wood tissues also supposedly each evolved more than once. Indeed leaves had to have evolved at least five times, perhaps many more (Friedman et al. 2004). As Michael Donoghue notes, ‘recent phylogenetic findings are making it increasingly difficult to sustain the traditional view’ whereby the identification of ‘key innovations’ is the way to distinguish new branches in the tree of life. Convergence is evidence that the history of evolution cannot be reduced to a single tree and that the structures in question were products of design, not accident.

Long, foreign-sounding names and complex biology can make the plant world seem very alien. Here we offer a brief guide that may help to open up the jungle a little.

Lycopsids

Lycopsid is the technical name for clubmosses (lycopods) and related forms. The informal name refers to their moss-like appearance, though they are not actually mosses, and to the club-shaped sporophyll clusters at the tips of their tiny branches. (A sporophyll is a leaf which bears the capsule in which spores develop, called a sporangium.) Only a few lycopod genera exist today, and they look diminutive in comparison to their largest forebears.

Lycopsids are distinguishable by their sporophylls and their spirally arranged microphylls (spine-like leaves with just one vein). The oldest known lycopsid is Baragwanathia, which we have already come across in Colonising wetlands. It first appeared in the Late Silurian and survived into the Early Devonian. Its leaves were separate from the sporangia and not fully veined. Another Early Devonian lycopod, Drepanophycus, is almost indistinguishable from the still extant Huperzia lucidula (shining clubmoss) – a rare case of stasis through the group’s entire record.

Within the lycopsids were the Protolepidodendrales, a widespread order whose leaf-tips were forked. Some grew to a height of 50 cm or more. They may have been ancestral to the arborescent (tree-sized) lycopods of the Late Devonian and Carboniferous, although the protolepidodendron that most resembles the lycopods, Zhenglia radiata, from China, belongs to the Early Devonian and is among the earliest representatives of the group.

Arborescent lycopods differed most notably from Protolepidodendrales in having a bipolar shoot system (with branches growing upward and roots downward) and assuming an erect rather than creeping growth habit. In these respects a Chinese fossil, Longostachys, has something of an intermediate character. Although only 1.5 metres tall, it had a slender trunk that branched at the top to form a crown of narrow branches and terminal cones. At the base it had downward-branching roots. However, it did not have the ‘rootlets’ that in arborescent lycopods grew perpendicularly and radially off the rooting organs, like the hairs of a bottlebrush. The sudden appearance of the rooting system of the arborescent lycopods remains a mystery (Gensel & Berry 2001).

Progymnosperms

Progymnosperms, the earliest-known trees, first appeared in the Middle Devonian and became extinct in the Early Carboniferous. The innovation of a bifacial cambium enabled them to produce wood (secondary xylem) and thereby grow outwards as well as upwards, in the same way as trees do today. Unlike the later-appearing gymnosperms, they reproduced by means of spores, rather than seeds, and evidence for the idea that they gave rise to the gymnosperms is currently weak. Indeed it has yet to be shown that the three orders of progymnosperm were related even to each other.

The best known example, Archaeopteris, was the first modern tree. Being only slightly younger than Eospermatopteris, it was virtually the first tree of any kind. It had an extensive root system, produced leaves, grew to a height of 30 metres or more, and had laterally growing branches. A swelling at the base of the branches formed a supporting collar, while layers of wood dovetailed into the trunk to give additional strength. But in one respect Archaeopteris was not modern, for large woody trunks today are produced only by seed plants. Its spore-system of reproduction meant that it needed to be close to bodies of ponded or flowing water, allowing sperm to swim to the egg.

Diversification led to several species of Archaeopteris. Occurring in large numbers on every continent, they colonised floodplains and coastal areas on a global scale. Along with the much less widespread Eospermatopteris they created the first forests. Forests ceased on this scale in the wake of events causing mass extinctions at the end of the Devonian and did not recur until well into the Carboniferous, when several new woody-tree genera of uncertain affinity appeared.

Arborescent lycopsids

The oldest arborescent lycopods date to the Late Devonian, at which point there were already several genera. These trees produced almost no secondary xylem – that is, wood tissue growing out from the centre so as to increase the girth rather than height. Instead the trunk was filled with pith and strengthened by a thick cortex which extended from the cambium outwards to a bark-like, decay-resistant periderm. Long grassy leaves grew from the trunk, and following leaf-fall the scars on the leaf cushions composed a distinctive geometric pattern. In contrast to the brown, non-photosynthetic stems of modern trees, photosynthesising tissue covered the whole trunk, giving it a green colour, and this super-efficient energy factory enabled lycopod trees to reach full height in just a few years. Only towards the end of their lives did they form lateral branches and put out a leafy crown. Rising like pillars, they were able to grow in great density, up to 800 trees per acre.

The best known lycopod trees are Sigillaria and Lepidodendron, being the major components of the vast Carboniferous swamp forests that ended up as coal seams. Their rooting systems, known as stigmaria, supported these lightly-built trees by splaying out horizontally, and the collapsed state of the fossils (or sediment infill where not collapsed) shows that they were hollow and immersed in water rather than soil. Unlike true roots, the fragile appendages around the stigmaria radiated in every direction. From time to time the rootlets were shed and left scars, just like the leaves, and probably also photosynthesised like the leaves. The stigmaria cannot, as is usually assumed, have been anchored in ‘seat earths’. The clays, sandstones and even limestones that surround their fossilised remains accumulated after their demise.

Most of the arborescent lycopods were extinct by the Late Carboniferous. However, growing alongside them and surviving into the Late Carboniferous itself was a related group of smaller mostly unbranched forms, called the isoetaleans. These appeared about the same time as the arborescent forms, in the Late Devonian. Today the order Isoetales is represented by a single genus, the short, semi-aquatic Isoetes, still retaining morphological, anatomical and developmental features that reflect its origins (Pigg 2001).

Ferns

Under this very broad term six major groups are distinguished: whisk ferns, ophioglossoid ferns, cladoxylopsids, marattioid ferns, leptosporangiate ferns and horsetails. Although the first two groups may be related, relationships among the others remain elusive (Pryer et al. 2004). The current state of play is that ‘relationships among major groups of vascular plants are far less completely understood than claimed by some’ and ferns in the broad sense probably do not constitute a single-ancestor group (Rothwell & Nixon 2006).

The earliest fern-like plants to appear were the cladoxylopsids, in the Middle Devonian, some of which grew to tree height. After most arborescent lycopods went extinct, tree ferns became the dominant group of plants. Some North American coals from the Late Carboniferous consist up to 75% of tree fern remains.

Whisk ferns have no fossil record. Because of their simple body plans (for example, no roots, and highly reduced leaves), they were long thought to be related to some of the earliest vascular plants, such as Rhynia. However, most experts now believe that they derive from more complex ferns that did once have roots. They are an example of evolution proceeding in the reverse direction, being ‘advanced’ in time but comparatively simple in form. The similarity with the earliest vascular plants, while thought-provoking, is fortuitous. Ophioglossoid ferns go back no further than the earliest Cenozoic.

Although only recently identified as such, the most famous of the cladoxylopsids is the tree whose stumps thronged the fossilised Gilboa forest, Eospermatopteris. It photosynthesised through fronds that spread out from the crown like a feather-duster. As the trunk grew upwards, the branches dropped off and the outer tissues of the trunk remodelled themselves into longitudinal strands, so that the branch scars gradually disappeared. Present-day cycads and palms – which, however, are seed plants (see below) – have a similar structure.

The marattioid ferns first appeared in the Middle Carboniferous with later species reaching heights of up to 8 metres. Unlike most arborescent plants, they did not produce secondary xylem. Instead, the trunk was encased by a dense mantle of intertwining roots. The extant representatives of this group are ‘living fossils’ in the sense that they have changed little since that time.

The leptosporangiate ferns are the most diverse of the fern groups. Of the dozens of families classified, one – the polypods – accounts for about 60% of the 11,000 present-day species, testifying to an extraordinary burst of diversification from the Cretaceous onwards (though this is less anomalous in relation to the timescale of recolonisation theory ,which lengthens towards the present). Leptosporangiate ferns first arose in the Early Carboniferous and soon after diversified to give rise to roughly six distinct lineages, none of which are easily traceable to present-day ferns.

Horsetails are characterised by their grooved, jointed, hollow stems, whorls of highly ‘reduced’ leaves at the joints, extensive underground rhizomes, and sporangium-bearing stalks that cluster into cone-like ‘strobili’. The oldest horsetails (Archaeocalamites) go back to the Late Devonian. Represented today by just one genus, the group climaxed in abundance and diversity in the Late Carboniferous, when they grew as tall as trees. Like the arborescent lycopods but unlike Archaeopteris, they produced secondary tissue only on the inside of the cambium. Modern horsetails are diminutive by comparison with their forebears.

As with the other ‘ferns’, there are earlier plants (such as Sphenophyllum, Hyenia, Pseudobornia) that although hinting at a relationship with the horsetails have so far resisted attempts to classify them within an orderly evolutionary scheme. The Late Devonian plant Pseudobornia reached heights of up to 20 metres.

Seed plants (‘gymnosperms’)

Seed plants include both the gymnosperms – plants with naked seeds – and the angiosperms, the ‘flowering plants’, whose seeds are enclosed within a carpel. Angiosperms did not appear on the scene until the Cretaceous, long after the gymnosperms, and their origin continues to be the ‘abominable mystery’ that it was for Darwin. The lateness of their appearance is also something of a mystery for recolonisation theory.

Seeds consist of an embryonic plant and a store of food, surrounded by a protective coat. The advantage of this mode of propagation is that the fertilisation process preceding development of the embryo takes place through wind pollination rather than via water, and less surface water is required after seed dispersal for the plant to germinate. The food store enables the embryo to establish itself in its new environment without external resources initially, following which nutrients and water can be procured from the soil.

These advantages allowed seed plants to colonise a wider range of environments than the vascular sporing plants. While gymnosperms in the Palaeozoic seem to have mostly preferred the wetter parts of the landscape, like the other types of plant, they also spread into drier and higher-altitude locations. The photograph shows one of the giant trees recovered from Lower Carboniferous sandstones near Edinburgh, now on display outside the Natural History Museum in London. These trees had been plucked from their inland environment, transported by strong currents and buried where the sediments, now settling, fanned into the sea.

Gymnosperms are no longer thought to correspond to a group traceable to a common ancestor (the first seed plant) from which all such organisms arose. The evolutionary pattern has proved altogether more complicated.

The oldest known seed plant is Runcaria, from the Middle Devonian. It displayed ‘a highly derived morphology compared to that of sporangia in progymnosperms’ and was ‘already complex’ (Gerrienne et al. 2004), indicating that seed plants must have originated considerably earlier than the time the so-called progymnosperms first appeared. This is also the implication of the Late Devonian seed plants found at Elkins, West Virginia, and Taffs Well, near Cardiff, which reveal greater complexity and variation than was to be expected at this stage in seed-plant evolution.

Another group that has not lived up to expectations is the ‘seed ferns’. These used to be considered transitional between ferns and seed plants, but are now recognised to be a very heterogeneous group, with relationships among themselves no clearer than their overall relationship to non-seed-fern plants. The earliest seed ferns were the lyginopterids, mostly liana-like plants and vines from the Late Devonian. Others, appearing in the Carboniferous and Permian, were erect trees. Seed ferns finally became extinct in the Eocene.

Other distinct seed-plant groups without obvious ancestry include the cordaites, cycads and conifers. These emerged in the Late Carboniferous. Some cordaites were shrubs; others reached tree height, with narrow parallel-veined leaves up to 1 metre long. They died out at the end of the Palaeozoic. The cycads and conifers are of course more familiar, having descendants in the modern world.

Novelties galore

Why is it, then, that we talk about the ‘Cambrian Explosion’ but not about a ‘Devonian Explosion’? The main reason is that the Cambrian was when nearly all animal phyla first appeared and, in modern classification, there are many more animal phyla than plant phyla. Most animal phyla consist of marine forms of life, some include creatures that began in the sea and subsequently colonised the land and/or fresh water (such as snails), and others include creatures that are merely presumed to have colonised the land from the sea. For example, most terrestrial invertebrates are classified within the single phylum arthropods. If one sees things from this point of view, then the Cambrian Explosion, when the first arthropods appeared, will seem far more radical, far more ‘explosive’.

However, it is not entirely correct to say that the basic body plans of organisms are all at the phylum level. The question of what is, in the context of evolution, a basic body plan is one that has to be inferred empirically, case by case. As is clear from the arthropod and vertebrate phyla, it cannot be determined simply by agreeing that the basic body plan is a certain hierarchic level in a scheme that begins with species and continues by grouping species indefinitely into higher and higher levels, on the assumption that all species are related. In the context of Darwinian evolution there can be no ‘basic body plans’: degrees of difference should increase gradually over time, not be so great, so early, that already at the beginning of the macrofossil record they were at phylum level. Darwinian evolution should be a story of continual improvisation, not of variations on fundamental designs that were presented to natural selection at the outset.

Once we recognise that some basic body plans may be marked by gaps at a lower level of classification, so that there may not have been any evolutionary transition between the progymnosperms (so called) and the gymnosperms, or between some unknown arthropod and the earliest millipede, or between Tiktaalik and the earliest tetrapod, it will become apparent that organisms appeared on land just as suddenly in the Devonian as they did in nearshore marine environments in the Cambrian. It was a ‘novelty radiation’, where new biological types appeared, not by evolution from organisms visible earlier in the fossil record, but from off-stage, where they were previously too few and too sparse to be fossilised.

The order in which plants made themselves known in the fossil record was the order of ecological succession:

It was a reflection of the fact that, little by little, plants were being given more time to establish themselves in the same spot and develop vertically tiered communities. It was not mega-evolution Darwin-style.

New habitats

The increasing diversity of plants reflected the increasing availability of diverse habitats. Owing to the declining rate of radioactivity (the main driver of plate tectonics), geological processes such as sea-level change, volcanism and mountain-building were slowing down, and environments – drainage-systems particularly – were gradually becoming more stable, allowing a variety of pre-existing plant types to begin exploiting them. Diversification within those plant types partitioned the landscape into ever smaller ecological niches. Channel-dissected mudflats close to the sea began to fill with lycopsids and fern-like plants. Floodplains further inland became sufficiently stable for trees such as Archaeopteris to proliferate and reach maturity. Opportunist species of seed ferns spread from these various wetlands to exploit areas of greater stress and variability.

Plants created new habitats as well as simply colonising them. Increasingly penetrative root systems helped to break up rocks and develop soils, which in turn promoted the growth of a greater range of plants. Vegetation helped to stabilise land surfaces by reducing erosion. Forest canopies moderated humidity and temperature, allowing smaller plants to grow beneath them and providing shade for a variety of invertebrates. They also produced copious amounts of spores and leaf litter, which were an important source of food for the invertebrates and provided material for the decomposing activities of microbes and fungi. Soils enriched by herbivores and decomposers enabled the growth of other plant types, and other invertebrates preyed on the herbivores. In time a complex detritus-based food web began to develop, supporting in the drier parts of the forests insects, mites, spiders, myriapods and the like, in the wetter parts tetrapods, molluscs, eurypterids and shallow-water fish.

See also Recolonisation and plant fossil order