Magma rising through the mantle during and after the Archaean formed new continental crust. As with the new oceanic crust, it took time for organisms to establish themselves on this barren, hard, initially steaming surface. Here we explore some of the evidence for the first stages in the process. Are we justified in suggesting that recolonisation rather than step-by-step evolution best accounts for the fossil sequence?

Colonisation in the modern world – ecological succession

Although it is not an exact parallel, we have an analogue in the colonisation of islands formed when lava spews from fissures in the ocean floor. Some, such as Surtsey Island, are very recent and we can observe the sequence of events from the start. Another analogue is the colonisation of existing land after it has been resurfaced by terrestrial eruptions. Small-scale though the eruptions are compared to the cataclysm that caused Earth’s entire crust to be replaced, such cases show that vegetation greens up the land in stages, not all at once.

A typical succession might be: microbes, lichens and mosses, herbaceous plants, and finally shrubs and trees. Depending on climate and the preferences of the other organisms within range, the later stages may never be reached, and successions do not always follow such a pattern. In part the order is determined by rates of growth and generation times; in part it reflects the fact that the later-arriving organisms depend for food on the earlier ones. Each stage builds on and adds to the one before, leading to a mature ecosystem where there is a great variety of species, nutrients are recycled and organisms frequently interact and benefit each other.

The first colonisers – bacteria, microfungi and green algae – form communities on the surface. Later they may be joined by lichens and mosses. Lichens are partnerships of fungi and algae. They release chemicals which, along with fracturing, faulting and weathering processes, break rock into smaller and smaller pieces. Soil bacteria serve the vital role of ‘fixing’ atmospheric nitrogen into compounds which can be utilised by vascular plants, and plant roots and acids further break up the ground. By a process of positive feedback progressively greater depths of rock are converted by microbes, fungi and penetrating roots into fertile soils. In time the activities of invertebrates also play a role. The overall succession is one of increasing energy consumption and increasing biological complexity, but it is an ecological succession, not an evolutionary one. The microbes do not evolve into mosses, or the mosses into ferns. Rather, each group has an independent origin from beyond the area colonised.

The comparison between ecological successions and the order of fossils should not be taken too far, however. In many respects the yet-to-be-vegetated world was different from the modern world. Mountain-building, flash floods and other high-energy processes were continually eroding the mountains and producing ever thickening sheets of sand and mud down slope. With surfaces being so unstable, plants found it hard to get a foothold. In the places where plant fossils were most likely to be preserved – places of rapid deposition – ecological successions could not have occurred, because the surfaces were continually being buried, and therefore one type could not have prepared the ground for another. They could only occur where conditions were quieter and rates of deposition slow enough to enable soils to develop.

It also needs to be borne in mind that new stocks of vegetation were not ‘just round the corner’. In the case of Surtsey Island, vascular plant seeds were mostly transported by birds, arriving, for example, in the gizzards of migrating snow buntings or in the droppings of geese. In the Devonian, however, birds were scarce – they were absent completely from most parts of the world – and many of the plant species that characterise modern ecosystems, including grass, had not yet evolved. On an earth that had been denuded of both fauna and flora, there was no possibility of bringing in relief supplies from somewhere nearby. Ecological systems had to recover from scratch, in an uphill struggle where attempts at recovery were being repeatedly disrupted.

Thus, for some while, plant fossils tended to represent only pioneer species, at the beginning of potential successions. Diversity might slowly have been increasing elsewhere, but paradoxically species that took successions beyond the pioneer stage stood a chance of impressing the fossil record only when a locality that had been stable long enough for them to take root was suddenly overtaken by less stable conditions.

The places where vegetation would most easily have become established were those furthest away from the highlands, such as low-lying plains and deltas. Here the energy of periodic discharges of water from the mountains was mostly dissipated, and the rate of deposition of silts and clays on the margins of ephemeral river channels was slow enough to give vegetation opportunity. The successful plants were those suited to wetland environments, comparatively simple in design. They were not pioneers in the sense of preparing the ground for others to follow. They took root here because they were semi-aquatic plants that did not require mature soils, ‘r-strategists’ that reproduced quickly and proliferated over wide areas.

Mosses and liverworts

Bacteria, fungi and algae reproduce by means of spores. So do certain plants, such as mosses, lycopsids (clubmosses), horsetails and ferns. Plant spores have very resistant walls and because of their lightness and smallness are easily transported by wind and water; the tough walls are a design feature which protects the spores during transport. Consequently they are not only the best preserved plant remains in old sedimentary rocks but also the first and the most abundant. By contrast, the spores of bacteria, fungi and algae are rarely preserved.

Spores of what are believed to be mosses and liverworts are known from at least the mid Ordovician onwards, less certainly from the Cambrian. Their abundance increases with ascending stratigraphic level, as one would expect if plant fossils were reflecting the progressive recovery of vegetation. The macrofossil record is poor until the Devonian.

Though simpler than most other plant types, mosses and liverworts are intrinsically complex, as is apparent from their life cycle and from their ability to photosynthesise. How these first land plants fit into the evolutionary tree of life is unknown. They each constitute separate lineages and are neither preceded by evolutionary forerunners nor followed by evolutionary successors. Capable of withstanding immense changes in moisture and temperature, mosses and liverworts can survive in habitats inimical to other plants, and are so well-designed for their particular role in ecological systems that they have changed little over time. On the other hand, with almost 19,000 species known today they have become extremely diverse.

Mosses were among the first plants to grow on Surtsey. Within a few years of the first eruption in 1963 they were growing around crevices and holes where steam kept the volcanic rock damp. Nitrogen-binding cyanobacteria were also found around the steam-holes, and by 1970 mosses and lichens were widespread on the bare lava.

The first fungi

Fungi are not plants but multicellular organisms in a kingdom of their own, and their origin is as much an evolutionary mystery as that of the other kingdoms. More than 100,000 species are known. Some are aquatic, the majority terrestrial. They play a vital role as decomposers, recycling organic remains back to the environment in forms that other organisms can assimilate. Nearly all plants depend on symbiotic fungi to help the roots absorb minerals and water from the soil, while the fungi benefit by receiving carbohydrates from the plants. Assuming that they have always been interdependent, one would expect them to appear about the same time in the fossil record.

The oldest traces of fungi are filaments and spores from the Ordovician. These bear a strong resemblance to certain modern species, which form filamentous structures in or among plant roots in order to increase the surface area for absorption. Fungal-looking filaments occur also throughout the Silurian, with some again looking like the structures of extant species. Numerous types of fossil fungi have been observed among the plants of the Rhynie chert of the early Devonian.

The first lichens

Lichens are organisms where fungi live in symbiosis with cyanobacteria or algae. DNA analysis of extant lichens has led to the conclusion that lichens arose independently at least five times! The fossil record of lichens is poor, but cyanobacteria and algae first appeared in the Proterozoic, fungi probably also did, and there is a report of lichen-like fossils dating to the Cambrian. The oldest unequivocal lichen is Spongiophyton minutissimum, a widespread fossil from the early Devonian.

The first vascular plants

Photosynthesis in an aerial environment involves the absorption of carbon dioxide and the emission of oxygen, mediated through pores in the surface of the plant. Since large amounts of water vapour are lost in the process, plants higher than a few centimetres require specialised tissues to draw water from the ground, a requirement which increases as the concentration of carbon dioxide in the atmosphere decreases. In vascular plants these tissues are of two types: xylem, which pipes up water and minerals from the roots to the leaves, and phloem, which distributes sugar and other products of photosynthesis from the leaves to the roots. Xylem also provides stems with rigidity – another requirement if plants are to grow higher than a few centimeters. From an evolutionist viewpoint, the emergence of these tissues is one of the most significant events in the history of land plants. Some mosses also have conducting cells, but these are thought to have originated independently of vascular plants.

How natural selection acting on genetic mutations leads to new designs is far from clear, and assuming it did, one would expect it to give rise to no more than adequate design. The characteristics of distinctly good design, such as energy efficiency or ingenuity in the solution of a given problem, are evidence that intelligent creative power was responsible. In this instance the design is superb. ‘It is difficult to imagine a cheaper process for driving the transpiration stream’, writes John Sperry. The automatic coupling between evaporation at the plant surface and the negative pressure achieved by capillary forces in the cell walls produces the driving force almost free of charge. Xylem conductivity per area exceeds that of non-vascular plants by six orders of magnitude.

The minimum requirement for such a system is a genetic program that causes the death of the cells lining the conduits and the manufacture and deployment of a substance (lignin) to strengthen the cell walls against collapse. These innovations were already in place by the late Ordovician, when vascular plants begin to leave rare traces in the form of characteristic spores – there are even reports of spores going back to the Cambrian. Yet the oldest known whole vascular plant, Cooksonia, did not appear until the mid Silurian. Presumably, the processes of erosion and deposition in their vicinity were now less destructive. Cooksonia was small (less than 10 cm high), simple in appearance, and like the spores initially rare. By the end of the period (supposedly millions of years later) it was globally widespread, though still rare, and comprised at least five species.

The relationship of Cooksonia to the later vascular plants is as little understood as the origin of the whole group. This later vegetation included zosterophytes (from the Greek word for garland, describing the successively arranged sporangia, and the Greek word for plant, phyton), rhyniophytes (named after the Scottish village of Rhynie), trimerophytes (so named because of their multiple branching, as illustrated by Psilophyton below) and lycopods (referring to the resemblance of some branch tips to a wolf’s paw). Most did not have leaves and roots, but the lycopod Baragwanathia had leaves (as do mosses), and all of them branched upwards off horizontally growing stems called rhizomes, which anchored the plants. In other respects they differed markedly from each other, notably in the design of their conducting walls, which were more complex and various than with extant plants. Since these diverse groups all appeared about the same time (late Silurian-early Devonian), a shared ancestry seems unlikely. The zosterophytes, rhyniophytes and trimerophytes died out in the course of the Devonian and left no descendants. A few lycopod species exist today, though much diminished both in size and diversity.

Baragwanathia, the earliest examples of which come from Australia, is especially problematic because it is taller and more ‘advanced’ than its fossilised contemporaries. Other anomalously early appearances include vascular plant fossils from Late Silurian deposits on Bathurst Island, Canada (Kotyk et al 2002), and Early Devonian deposits around Gaspé Bay, Canada. In the latter case, the plants achieved a stature of 2–3 metres and, as in-situ root traces show, were capable of rooting to a depth of nearly 1 metre (Elick et al 1998).

Because of these and many other discoveries the ‘somewhat simplistic’ picture of plant evolution has had to change (Edwards & Richardson 2004). Simplicity of outward form masks complexity at the cellular level. Almost from the moment they appear, vascular plants are diverse, making it difficult to see how, invisible to the fossil record, they might all have arisen from a single vascular plant ancestor. The gap between vascular plants and non-vascular plants such as the mosses and liverworts is even larger, as is the gap between all land plants and their closest presumed relatives, the green algae (Kenrick 2000). By contrast, the time gaps between them (all being attested from as early as the Ordovician) are comparatively small. Mega-evolution simply is not an appropriate inference to draw.

What Diane Edwards says about the assemblages of the Anglo-Welsh Basin is in fact true of all the sites where early plant fossils are found:

While it is recognized that the assemblages provide the most complete and extensive record of the history of vascular plants in a restricted geographical area during the time interval, it seems likely that major evolutionary innovation occurred elsewhere.

‘Major evolutionary innovation’ always occurs off camera. What we actually see is organisms that have already been ‘innovated’ – one might say, created – parachuting in from somewhere else, colonising virgin territory.