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 far from exact, a modern analogue may be seen in the colonisation of islands that form when lava spews out from fissures in the ocean floor. Some, such as Surtsey Island, have formed so recently that we can observe the sequence of events from the start. Another parallel might be the colonisation of existing land that is resurfaced following terrestrial eruptions. Small-scale though such 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, though the process can certainly be rapid.

A typical succession would be: first microbes, then lichens and mosses, then grasses and ferns, then herbaceous plants, finally shrubs and trees. Depending on climate and the preferences of the organisms within range of the new environment, 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 species diversity is high, nutrients are recycled and many of the organisms interact and benefit from each other.

Communities of bacteria, microfungi and green algae form crusts that grow on or just below the surface. Soon they may be joined by lichens (fungi and algae in symbiosis) and by mosses. Lichens release chemicals which, along with various non-biological processes, serve to break up the rock, and in the later stages soil bacteria serve the vital role of ‘fixing’ atmospheric nitrogen into compounds which vascular plants then utilise. Thus continually 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.

Suggestive though the modern analogues are, caution should be exercised when applying them to the fossil record. In many respects the world after the cataclysm would have been unlike our own. It was ‘a world of rocky screes, mudflows and flash floods’ (Falcon-Lang 2005). Mountain-building and other high-energy processes were continually eroding the mountains and producing ever thickening sheets of sand and mud on lower-lying ground. Land surfaces were rarely stable for long, and plants would have found it difficult to get a foothold. Ecological successions could not have occurred in the places where plant fossils were most likely to be preserved – where deposition was rapid – because surfaces here were continually being buried. One type could not have prepared the ground for another. They could only occur on an altogether wider scale, and in places where conditions were quieter and rates of deposition slow enough to enable soils to develop. For some while fossils would have tended to represent only the pioneer species, at the beginning of potential successions. Diversity might have been increasing elsewhere, but it would have had a chance of impressing the fossil record only when a place that had previously enjoyed stability long enough to progress beyond the pioneer stage was overtaken by suddenly 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 would have been 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 protecting the spores during transport. Consequently they are not only the best preserved plant remains in Palaeozoic sediments 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 precursors 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.

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 every other kingdom. 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 other organisms can assimilate. Nearly all plants depend on symbiotic fungi to help the roots of the plants 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 (hyphae) and spores from the Ordovician. These bear a strong resemblance to certain modern species, which form filamentous structures (mycorrhizae) 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 hyphae of extant species. Numerous types of fossil fungi, including mycorrhizae, 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. An analysis of DNA sequences 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 centimeters 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 not expect it to give rise to 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 the creative power was something else. In this instance we are talking about superb design. ‘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 is fully six orders of magnitude greater than that of non-vascular plants.

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 may already have been in place by the mid Silurian, when the earliest vascular plant, Cooksonia, appeared. Cooksonia was small (less than 10 cm high), simple in appearance, and 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 also unclear. These 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 showed, 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. 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). 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.