Survivors: The Animals and Plants that Time has Left Behind

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Probably the best-known onychophoran from the Cambrian is called Aysheaia pedunculata. It was named a century ago by the renowned palaeontologist Charles Dolittle Walcott of the Smithsonian Institution, Washington. It occurs in what is probably also the most famous rock formation of that age, the Burgess Shale of British Columbia, Canada. A locality near Mount Field in the Rocky Mountains discovered by Walcott yielded the first known, diverse fossil fauna of ‘soft bodied’ organisms, that is, those lacking hard mineralised shells, which are the kinds that give us ‘regular’ fossils. The Burgess Shale allows us to see something of the whole panoply of marine life at a seminal time – although admittedly it only samples the larger organisms. The fossils are preserved as silvery films on the surface of the black shale, so that they are subtle casts made by fine minerals before the animals could be scavenged or they fell apart. The exact circumstances of their preservation are still being debated, but it is certain that quick burial and protection from normal decay played an important part. Whatever the cause, Aysheaia is preserved in extraordinary detail.

4. Cambrian lobopod fossil Aysheaia pedunculata from the Burgess Shale in the Canadian Rockies, British Columbia.

Comparing Aysheaia with Peripatus reveals that they are of similar size and shape, the former reaching about six cm in length. The fact that differently sized animals of Aysheaia retain the same form as they get larger, implies a simple growth pattern like that of the modern velvet worms. In Aysheaia the fine rings encircling the body are clearly visible, and little prickles are much like the papillae of the living animal; add to that their stumpy conical legs look very alike, and at the tips in the fossil little sickle-like claws can be clearly seen. But there are some differences between this most ancient animal and the creature I helped to dig out of its woody habitat – it would have been astonishing if there were not. Most obviously, there is a pair of gill-like structures on the head end of the fossil. This is hardly surprising since the animal was living under water. There is also no sign of the special slime glands in the fossil. This must have been a later development, which presumably would also have been acquired after the terrestrial invasion. But it would take a hardened sceptic not to believe that these animals were related. Of course in science there are always such sceptics, and the special features of Aysheaia were emphasised by some at the expense of its many similarities to Peripatus, but I believe most students today would accept the onychophoran tag on the Cambrian creature.

The story got interesting when a second, and much more peculiar-looking Burgess Shale species was assigned to the onychophorans. This animal had been named in 1977 Hallucigenia by the Cambridge palaeontologist Simon Conway Morris, but his original description of the fossil was upside down. Hallucigenia carried paired spikes on its back which Conway Morris had originally interpreted as legs (he later acknowledged his error with good grace), while the true legs were more spindly affairs than those of living velvet worms or, indeed, Aysheaia. The spines arose from hardened plates, which had been found separately as fossils in early Cambrian strata, but had been unfathomable up to that time. The mystery was not fully elucidated until much better preserved, soft-bodied fossils began to be found over the last decade or so in strata cropping out around Chengjiang in Yunnan Province in China (these are known as the shales of the Maotianshan Formation). The new fossils were up to ten million years older than the Burgess Shale examples, and have now proved even more diverse. They include at least six animals that can be assigned to the same group as the velvet worms. One of them carries spikes on its back and was an additional species of Hallucigenia, another one (Paucipodia) was an altogether slimmer affair than its distant living relatives, with only nine pairs of slender legs. One fact was now becoming clear: the relatives of the velvet worm were much more varied in the early days. There were lots of them of several distinct kinds, but they did all share those lobe-like legs, often tipped by little claws. An appropriate term for the whole group, both living and fossil, achieved wide currency during the 1990s – they were ‘lobopods’. Thanks to the special preservation of these Cambrian fossils it was possible to see surprisingly varied and delicate lobopod animals in unprecedented detail. Living velvet worms began to seem more of an evolutionary afterthought.

The plot thickened still further at this time, for up in Greenland Dr Graham Budd and his colleagues were finding yet more soft-bodied animals in the early Cambrian Buen Formation. These showed certain similarities to onychophorans, like the rings along the body, but the animal named Kerygmachela by Budd had a pair of grasping appendages at the front and was obviously a hunter capable of grasping prey. The lobopods were clearly going to spring yet more surprises.

The question now arises as to where this curious bunch of animals fits in on the tree of life. I have already described how Cambrian fossil faunas included many kinds of jointed-legged animals or arthropods, such as distant relatives of the horseshoe crab. All these arthropods would have had a tough chitin covering over the body that made the ‘invention’ of hinged joints necessary. Without them, the animals would have been as helpless as a medieval jouster whose articulated armour had rusted into immobility. But with hinges added, arthropods were equipped with a versatile covering that could be recruited to be armour, jaws or toolkit as the occasion demanded. The future walked on spindly legs. Like arthropods, velvet worms and their relatives were, and are, segmented animals. Unlike arthropods they did not have a strong coat made of chitin: no hinges were possible. Their lobopod legs were effective enough in their own plodding way, but they could not be extended into the attenuated pins of a daddy-long-legs. That requires serious mechanical engineering, and the stiffening support of a hard skeleton. On the other hand, some features of internal anatomy seem to be very similar between living onychoporans and arthropods. I could mention the diffuse circulation system and the arrangement of the nerve cords, and some scientists are impressed by the presence of antennae in both kinds of organisms. At least one of the Cambrian lobopods shows evidence of simple eyes. The musculature is differently arranged in lobopods and arthropods, which actually allows the lobopods greater bodily flexibility.

Their fundamental similarities make it likely that Peripatus and arthropods share a common ancestor. The arthropods seem to be more advanced in several respects: the jointed legs could only have been added when the ‘skin’ acquired its hard outer layer, and sophisticated compound eyes like those of Limulus must surely have been a later development. This is another way of saying that lobopods are probably sited on a lower level on the great tree of life, likely to have been around before the arthropods evolved. There are some scientists who would claim that they are the true ancestors of the arthropods, or even that different kinds of lobopod gave rise to different kinds of arthropods. Partly, this depends on the interpretation of the jawed animal Kerygmachela from Greenland that seems to display something of an amalgam of lobopod and arthropod characteristics. Whatever the final interpretation, these recent discoveries of Cambrian fossils provide another case of neat categories of animal classification blurring at the time of the ‘explosive’ phase of animal evolution. The story also takes us back further in time than we have been before.

Recently, additional evidence for the velvet worm’s place on the tree of life has come from the genome of the living species. Ancient fossils do not preserve DNA, which is a large and delicate molecule, readily fracturing into pieces. But by studying the molecules of living survivors from deep branches in the tree of life we are afforded a kind of telescope to see back in time. For the genetic code of DNA records another kind of history, it retains the accumulated narrative of all the changes at the fundamental molecular level that have built up slowly over time. Mutations that have been incorporated in the genome provide a kind of ancient fingerprint. But the code of life is famously huge – which means that the investigator may be obliged to seek out the particular piece of the genome that contains the information he needs. Although, as this is written, more and more organisms are having their entire DNA sequenced, this is still the prerogative of a privileged few – unsurprisingly, those like wheat or influenza that have a particular importance to Homo sapiens. For many organisms, it is more feasible to use a particular chunk of its genetic code to compare with the same chunk from a range of its potential relatives. This might be a particularly suitable gene or series of genes, for example, that do not change too rapidly to be useful through long periods of geological time. Obviously, the chosen gene has to be present in all the organisms under study. Other workers favour sequencing parts of the RNA molecule in the ribosomes that are present in the cells of all living organisms as the centres for protein synthesis. Comparing the similarity of gene sequences is one way assessing how closely (or not) organisms are related to one another. The results can be drawn up as another kind of tree, with branches drawing together the closest related species, and deeper patterns of branching inferred from still more fundamental inherited similarities. This is not as easy as it might sound from this bald description, as various kinds of ‘noise’ can obscure the signal the investigator seeks, and there are always genes that change too fast to retain meaningful signals from deep time. I need hardly add that computer programs have been designed to help out. The technical problems are not part of our story, except in so far as they have produced different ‘trees’ of relationships between organisms since the methods were first developed. Indeed, early attempts sometimes look quaint or improbable. But recent studies seem to have stabilised, and produce trees that appeal to prior knowledge and common sense, mostly by lumping together evidence from many different genes and finding the best fit. These then make a meaningful contribution to the summary trees of evolutionary history like those on our endpapers. The latest molecular analyses to treat the velvet worm and its relatives show interesting results. It places our chosen survivor as the bottom branch of a tree that includes all the arthropods above it – which must therefore have arrived later. Another name appears between the lobopods and the arthropods. This is Tardigrada (water bears), a group of tiny creatures that often live between sand grains and in other cryptic habitats. They are interesting in their own right, but they have but one known fossil, so they will not be described in detail here. Many tiny animals have no fossil record at all, but that does not mean that they did not exist in the past. The important point for us is that the molecular evidence supports the idea that lobopods are a branch even lower on the tree of life than arthropods. Those stumpy legs have walked on and on from a time even before the Cambrian. The very earliest Cambrian strata contain the traces of animals, but not their bodies. This is probably because those early animals lacked readily fossilisable hard parts, and the special conditions required to preserve the slightly younger Chengjiang fossils were not present at this particular time. No matter, for some of the tracks and trails that are preserved as fossils show clearly the traces made by arthropods of normal size digging their way into soft sediments with their numerous paired legs. It is even possible that these could have been tracks left behind by soft-bodied ‘proto’ trilobites since they are similar to tracks made by the same animals higher in the geological column; at the moment we simply do not know. But we now do know that there must have been lobopods on that same sea floor, too, stomping ever onwards. More than that, they must have been present even earlier, before the first arthropods, because both the molecules and the anatomy of the animals tell us that they preceded the jointed-legged organisms. This takes us back into the mysterious world of the Ediacaran, a period whose remains lie above the Precambrian, and below the Cambrian, before the time of abundance and variety of marine life and before the appearance of shells.

The story of the lobopods now disappears. There are no velvet worms or indeed any kind of lobopods in strata of Ediacaran age. There has been no shortage of attempts to find them. Geologists and palaeontologists have been cracking open likely rocks for decades now. The fact is that there are no trilobites, no early horseshoe crabs, nor any old familiar biological friends to be found in Ediacaran age strata. As in The Hunting of the Snark by Lewis Carroll searchers vowed: ‘To seek it with thimbles, to seek it with care; To pursue it with forks and hope’, but to no avail. Even big hammers did not work. Instead a whole series of fossil animals have been recovered which have proved as enigmatic as they are exciting: not snarks but boojums. They are not small – some of them are bigger than a dinner plate – and neither are they uncommon if the searcher goes to the right place. The Ediacaran Period takes its name from the Ediacara Hills in the Flinders Ranges in South Australia where a diverse selection of these remarkable early fossils was first collected. They appear as impressions on fine sandstones, many looking like strange leaves or fronds. Most of them show evidence of divisions or compartments dividing up the body, but they are not simple segments, because they are usually offset from one side of the animal to the other. Similar fossils are now known from more than thirty localities all over the world: from Arctic Russia, Canada, America, Newfoundland, and Great Britain. Everyone agrees that these fossils lacked skeletons, but otherwise the experts disagree on almost everything else. Most of them would now concur that the Ediacaran animals were not obvious ancestors of the animals we know from the Cambrian onwards; they were genuinely inhabitants of a former world that did not survive. It seems only fitting that in a book about survivors I should also go to visit a world that failed to endure. The journey took me back to Newfoundland, where I had spent a year at Memorial University in St John’s when I was a young scientist. So I was travelling into my own past as well as towards a far, far deeper time.

Newfoundland is an island at the tip of eastern Canada and is itself something of a survivor. Built on the fortunes made from codfish on the Grand Banks, it has survived the great crash in the population of its most important crop. It is the textbook case for the effects of over-fishing. In the thirty years I have known the ‘rock’ (as the natives call it) I have watched with bewilderment as fishermen have laid up their boats, and an apparently endless resource has all but disappeared. The codfish has not become extinct, of course, but the decline of this otherwise unfussy fish does prove that nothing in nature can be assumed to be unassailably fecund. High-tech factory ships from outside the island indiscriminately scooping up huge quantities of fish are mostly to blame. The Newfoundlanders, ever resourceful, have now taken to oil. The name of the Come-by-Chance refinery is somehow appropriate to their persistence in the face of setbacks not of their making. The little fishing villages along the coast are known as ‘outports’, and ever since they have been required to eschew the cod, those young outport men who have not gone to Come-by-Chance have left to find work at Churchill Falls, the huge hydroelectric plant in northern Labrador, or even to become hands on the extraction of the Athabasca ‘tar sands’ on the other side of Canada. They are a breezy bunch, despite their peripatetic life, and have an unusual accent: Irish with added stretched vowels, and wheezy interpolations of interjections like ‘Jeez, my son’. The outports are all freshly painted these days, with wooden houses in cheery colours scattered up the hillsides. For the few who stay behind, there is nothing much to do except repaint the picket fences.

The drive south along the Avalon Peninsula from the capital St John’s passes several sheltered coves tucked away inside a coastline of magnificent cliffs. The geology is laid bare all along the rim of this island: the only problem is reaching it. Inland, the opposite is true; an endless forest of short conifers interspersed with scattered birch and aspen trees is interrupted only by shallow lakes called ‘ponds’ hereabouts, which are a legacy of the last ice age; the bedrock is hard to see among the scrub. As we approach the end of the Peninsula the trees get shorter and shorter, planed off by the fierce winds. Finally they crouch against the ground, as if terrified to poke up a twig. Usually the whole of this exposed area is swathed in fog, so the landscape supplies a passable setting for a vampire movie starring Vincent Price. But the day we visit it the weather is clear and sunny, with a few fluffy white clouds in a faultlessly blue sky. My companions are astonished, it was the best day they had seen in the last decade. The warden of the Reserve came from Wales, and remarked ruefully that he had chosen to work in the only place in the world with worse weather than Ffestiniog. One of the Newfoundlanders mumbles to me under his breath that the warden will be betrothed before Christmas. ‘Not a lot of single men around here’, he says, with a wink.

At Mistaken Point, a path leads for a mile across a bleak coastal heath, which is less forbidding examined closely. Berry-bearing plants hidden in the close sward bear blue-black or scarlet fruits, and bright yellow tormentil flowers smile at us along the way. Patches of Sphagnum bog support pitcher plants whose leaves trap flies and mosquitoes to compensate for the poor nutrition offered by the damp wilderness. Even wild roses are tucked into natural hollows. As we approach the sea, grasses take over to make a natural lawn. Fulmars wheel in and out, just to have a look. The path leads onto the cliffs, which are quite comfortable to clamber over in this part of the Avalon Peninsula. The sedimentary rocks of which they are composed form a series of ledges that dip at a gentle angle into the sea, forming steps that we can climb up or down to explore different strata. The rocks are dark in colour, and the more resistant beds have made natural groynes that project out into the ocean. Waves break continuously over the ledges, throwing up foam – and this on a calm day. When winter storms are raging, salt spray must blast all the exposed surfaces. It is not hard to imagine how Mistaken Point got its name. The bones of fifty ships lie offshore, waiting to be fossilised.

Each of the flat surfaces exposed on the ledges is an ancient sea floor. In 1967, a graduate student geologist called S. B. Misra at Memorial University of Newfoundland discovered the most extraordinary organic remains preserved on these stretches of petrified sediment surfaces. Only a year later an account of the finds had been published in the most prestigious scientific journal Nature, jointly with Mike Anderson, also of Memorial University. The rocks were recognised as being late Precambrian in age (this was long before the Ediacaran had been named). There was palpable excitement in the scientific community at finding such large fossils in rocks of this great antiquity, although it was not known at the time just how old they were. Misra subsequently described the original conditions under which the sediments had been deposited. There were some special features about this discovery. First, the fossils could not be safely collected. They were impressions on the exposed surfaces of a very hard but brittle rock, shot through with cracks, and often located in the middle of a great uncompromising slab. The best way to study the remains was to pour a latex solution onto the surface of the rock, allow it to dry – even that might be a challenge with the Atlantic hard by and fog always lurking in damp banks – and then take the hardened cast off to somewhere nice and warm. For scientific description it is usual to have an actual specimen on which to found a scientific name, and this should be kept in perpetuity in a public museum. This was obviously going to pose a problem, unless a public museum was constructed over the cliffs. Second, with such unusual material it is rather hard to know where to begin, since most of the usual biological pointers are absent. How does one describe an enigma, except as ‘enigmatic’? Perhaps it was a combination of these factors that stalled a full account of these remarkable fossils. Anderson took over the material when Misra went back to India, and when I met him in the late 1970s he seemed to be crippled into inaction by these admittedly difficult problems. At the same time, he put his marker down upon the fossils so that nobody else could study them. The result was that most of the Mistaken Point fossils did not receive proper descriptions and the respectability of scientific names for several decades. Guy Narbonne and his colleagues from Queen’s University, Ontario, are making good this omission even now. It is a strange fact about science that until an object or a phenomenon receives a name in some way it does not exist. Names really matter. They retrieve something from an endless chaos of anonymity into a world of lists, inventories, and classification. The next stage is to understand their meaning.

A notice at the top of the cliffs points the way (a quarter of it had blown away in the last gale) accompanied by a pinned-up sheet of paper instructing visitors to ‘remove footwear before visiting fossil bearing surfaces’. I confess that the idea of taking off one’s boots in a howling squall to safeguard fossils that had survived since the Precambrian had its funny side. In the event we are provided with a pair of rather fetching blue over-socks. Visits to the famous fossils are now strictly supervised, as the site is now part of the Mistaken Point Ecological Reserve, and quite right too. Canadians are strict about protecting their national natural heritage. There is an architect-designed Visitor Centre to explain all to those who have made the trip. I climb down onto the best surface, in my special socks, and it takes a while to identify what to look for, but once they are pointed out the fossils are obvious. Any doubt that they were of organic origin was immediately banished from my mind. The fossils are strewn over the black surface of the gently dipping former sea floor almost as if laid out for the convenience of future inspections: one here, one there. The most conspicuous look like leaves or fronds, and are about the same size as a domestic Aspidistra leaf or some other showy tropical pot plant. They are pleated within, and the closer one looks the more subdivisions inside the ‘leaf’ one begins to see. Such spindle-shaped fossils are the commonest type. There are more than a thousand of them on display under the Newfoundland sky. They were named Fractofusus misrai in 2007, four decades on from their original discovery, thereby commemorating the discoverer in perpetuity in the species name. The name Fractofusus is quite descriptive – the ‘fusus’ part refers to the fusiform (spindle-like) shape of the whole organism, and the ‘Fracto’ part to the fact that it appears to have a fractal structure. Fractals, those intriguing mathematical entities recognised by Dr Benoit Mandelbrot in 1980, are shapes that seem to repeat themselves precisely when the scale is focused down to a smaller level. So, the largest primary divisions within Fractofusus are subdivided into identical-looking smaller frondlets, and those in turn into identical-looking ‘sub-frondlets’, and so on. It seems that these Precambrian organisms favoured this kind of structure; indeed, Martin Brasier of Oxford University has shown rather ingeniously that several of the organisms at Mistaken Point can be understood as a kind of three-dimensional origami played out by folding such fractal objects in different ways. But there are also some frond-like organisms that seem to be attached to the former sea floor by a kind of disc-shaped holdfast. Charniodiscus masoni was perhaps the earliest Ediacaran species to be recognised – from Charnwood Forest in Leicestershire in England, as the generic name should make clear (like Misrai, the species name is after its discoverer). The same ‘frond’ is known from a very large number of Ediacaran localities, including several in the Ediacara Hills themselves, so it is almost totemic for this early and vanished marine world. The disc is thought to have held the organism in place while the frondose part was maintained aloft in the water current. There are several additional forms from Newfoundland that have their counterparts in Leicestershire, but since the latest reconstructions of the later Precambrian world place these areas quite close together geographically this is not as surprising as it may seem at first. Some other oddities are pointed out to me, one is a kind of plate with tumid blobs arranged all over it. It was called informally ‘the pizza’. The name reminded me that in my excitement I had not yet eaten lunch, so there I sat on an Ediacaran sea floor eating a cheese sandwich, looking out to sea on a perfect day while fulmars wheeled past on a light breeze. For a palaeontologist, it doesn’t get much better than this. I realise that whatever we eventually make of these strange fractal beings, it cannot be doubted that there was a lot of conspicuous life in the later Precambrian, but apparently no relatives of velvet worms. These special fossils position a time line in our story; they offer a calibration for evolutionary invention.

I wonder what lucky circumstances account for the preservation of the fossils. After all, they are soft bodied. They could have vanished leaving no trace. My guides tell me that the area now so often coolly fog-bound was volcanically active in those distant days. Periodic ash falls cascaded into the sea and rapidly killed off and buried the Ediacaran fauna. They point out the Charniodiscus bending over in a common direction flattened by the incoming volcanic Armageddon. I should have noticed this before. Each fossil-bearing sea floor is the record of one tragic moment for the Ediacaran animals, though it is no less than a miracle for us intelligent primates. Volcanic rocks have another property in addition to their role as natural undertakers; they yield minerals that can be used to obtain a radiometric age for the eruption. They both write the obituary and record the date. A time label of 565 million years ago has been obtained recently from an ash layer immediately above one of the best fossil-bearing beds. This is more accurate than can be achieved with many younger deposits, because datable volcanic rocks are not commonly interleaved with fossil-rich sedimentary rocks. Given that the best date for the base of the Cambrian Period is 542 million years ago, the Newfoundland rocks are only twenty-three million years older. I use the word ‘only’ advisedly; although this might seem like a long time, it is a short span in the history of the horseshoe crab or velvet worm. Even if we went back twenty-three million years from the present day we would readily recognise a world of mammals, birds, butterflies, and flowers; and our own distant ancestors were already in the trees. But the world of Mistaken Point seems to have nothing to do with the marine world familiar from Cambrian strata, with its arthropods like trilobites, together with molluscs, brachiopods, and echinoderms, ancestors of today’s sea urchins and feather stars, not to forget the distant relatives of velvet worms.

It is no wonder that an attempt to understand the Ediacaran world has attracted the attention of researchers around the globe. Some facts have become quite well established, but there remain many disputes, which is hardly surprising when considering scientific forays into such mysterious and ancient environments. In fact, the stuff of science is disagreement. If there were no disputes there would be no incentive to drive scientists out (without shoes) onto exposed Atlantic shores in order to crouch over cold wet rocks for hours on end. They want to get one step ahead in the race for the truth. However, most specialists do concur that the Ediacaran sea floor was very different from the seabed on the continental shelves today. The surface was coherent, even rubbery, due to a thin-skin veneer composed of bacterial mats. Sediments were almost cling-film wrapped, and holdfasts probably got a good purchase on this kind of surface. There is also a less universal consensus that the reason for this skin-like surface was that a range of burrowing organisms had not yet appeared to churn up the sediment. The sea floor nowadays is often a mass of so-called infaunal animals that live in the silt of the seabed and have a vital role to play in the food chain. Think of the huge flocks of waders that strut around on muddy estuaries when the tide is low, pecking down into the mud – not every dunlin has to rely on horseshoe crab eggs. Little churners and burrowers, especially marine polychaete worms, oxygenate the lower layers of the sediment as they work away. In the absence of such activity, an anaerobic layer soon develops beneath the surface, which can be recognised by the preservation of fine, horizontal layers when the sediments eventually harden into rock. Many Precambrian strata do indeed look like this – though by no means all. Sometimes the more fine-grained sedimentary surfaces betray a wrinkly skin, which is finely puckered, almost like the skin of an elephant, enabling us to visualise the gummy bacterial surface, although the minute organisms that made it are not preserved. These curious sea conditions have been ingeniously invoked to explain the preservation of many Ediacaran soft-bodied fossils. After a sudden overwhelming event – it could be a sudden slurry of sediment or a volcanic ash fall – the organisms are entombed, and a new mat then quickly grows on top of the grave sealing the dead animals in the sediment. Then the reducing conditions that inevitably ensue in the absence of wormy disturbance help to mobilise iron in the sediment in a form that migrates to make a kind of ‘death mask’ around the potential fossils before they have decayed away. The endurance of so many soft-bodied organisms certainly implies a lack of those scavengers that make short work of dead bodies in today’s oceans. As for the texture of the Ediacaran organisms, they may have lacked shells but they seem to have been membranous, possibly even quite tough. Some scientists believe that they were divided into chambers rather like an old-fashioned quilted eiderdown. Their apparently fractal structure is probably a reflection of a particular style of growing, whereby the same set of rules are repeated over and over. It may just be a simple way of growing big. However one looks at them these organisms do seem irredeemably strange.

My visit to Mistaken Point convinced me that it was possible for whole groups of organisms to disappear from the biosphere. There are some scientists who claim that the organisms preserved there – they have been called Vendobionta, among other things – are a kingdom (like Animalia) that has become extinct; a kingdom of ‘quilted’ animals that many of the same scientists also think may have harboured bacteria in their body compartments in some kind of symbiosis. The somewhat younger fossils from the Ediacara Hills in Australia also include a variety of ‘quilted’ organisms, but some of these seem to show a clear front end – a head. One of these, a creature called Spriggina, has been quoted as a kind of soft-bodied trilobite precursor. The more I look at Spriggina, the more I doubt it. The numerous ‘segments’ seem to be out of step on either side of the animal, and the head end looks like a boomerang and not really like the forerunner of a head-shield. In fact, when you examine it impartially it looks more like another apparently quilted and very un-trilobitic animal called Dickinsonia. But there is no question Spriggina is an intriguing animal, and I would love to be proved wrong. An Australian school of palaeontologists identifies soft-bodied ancestors of a few, living types of animals among a group of strange Ediacarans that are not quilted. An odd, radially symmetrical creature called Arkarua is claimed as an ancestral echinoderm, for example; a thing that looks something like a snowshoe called Kimberella has been claimed as a mollusc. Every one of these animals courts controversy. But at least some of these Australian Ediacaran animals, including Kimberella, are symmetrical about a line running along their midriff. This may not seem much, but it does show that below the Cambrian there were animals that could be placed in Bilateria – that is, animals with left and right sides that are mirror images (or bilaterally symmetrical). The common ancestor of arthropods, molluscs, annelid worms, and flatworms, not to mention the ancient relatives of velvet worms, would have been bilaterally symmetrical. We shall return to the interesting questions of the early days of animal evolution.

Vendobionts (or call them what you will) seem to have colonised all the seas of the world before the Cambrian Period. They were the first large organisms, and the younger and more advanced ones were certainly animals. Explaining exactly what they were has taxed the ingenuity of many clever people; but they have in all likelihood vanished from the world (the organisms, I mean, rather than the clever people). Some of the quilted animals that lived in shallow water may, possibly, have housed symbiotic algae or bacteria in their tissues, and basked in the sunshine, like prostrate reef corals. On the other hand, the Mistaken Point fauna appear to have lived in too deep and too turbid an environment for this to be a plausible option. It is perhaps not surprising that such strange creatures have inspired strange explanations. One worker even claimed that the vendobionts were not animals at all, but lichens, the living symbiotic collaboration between fungus and ‘alga’

that coats trees and rocks almost everywhere in the world. Lichens are the ultimate biological survivors in the simplest sense, because they seem to relish hardship and the tough life. However, none of them is adapted to life in the sea. The fact that some lichens have a flat and foliate form, as do the Precambrian ‘spindles’, indicates no more than a broadly similar way of growing over flat surfaces. Life’s history is as full of repetition as it is of endless inventiveness.

The waves surge and retreat from the stacked-up sea floors that once built Mistaken Point. This continually punished land will inevitably succumb to erosion, and the record of ancient life buried by chance so long ago beneath clouds of volcanic ash will be returned to the sea as a billion tiny particles. In the end, only the sea endures, it is the greatest survivor of them all. Even the continents mutate and remake themselves, driven by the internal engines of the earth powering slow but inexorable movements of tectonic plates. Mountain ranges are elevated and then reduced to rubble, but life can outlast mere Himalayas. Peripatus’ relatives once walked upon Gondwana when Africa was united with Australia and the Americas. The memory of

5. Pangaea – where the continents of the world were united as one ‘supercontinent’ 270 million years ago. The southern mass (South America, Africa, India, Antarctica, Australia) is Gondwana.

that vanished geography still lingers under rotting logs, or whispers through the leafy boughs of podocarp forests. Briefly, at least geologically speaking, all the continents were united together in the supercontinent called Pangaea (Greek: ‘all earth’) some 270 million years ago. But that mighty entity, too, was just a phase, just one configuration of the earth’s ever-changing physiognomy. For earlier still there was a time when continents were dispersed once more, making for a geography that looks still odder to our eyes. Science tries to reconstruct this former world map: it is like cutting a jigsaw puzzle into a set of new pieces, and then attempting to refit them into another picture altogether. By the Cambrian Period some 500 million years ago, these scattered continents were naked with their rocks unclothed by plants. The distant relatives of the velvet worm were there, though, living beneath the sea among a host of other creatures: some strange, some familiar. The lobopods were more diverse then than they have ever been since.

The branches of the tree of life were drawing closer to a relatively few common major limbs, but there was still a great variety of crawling, swimming, floating, burrowing creatures. There were livings to be earned: prey to hunt, hideaways to construct, plankton to be filtered, mates to be found. But then we must go back further, still further, into the Ediacaran. The surf at Mistaken Point washes over an even earlier, but alien world, a vanished world of soft-bodied, fractal things. There may have been no predation then, no burrowing, no grazing, no evidence of ‘nature red in tooth and claw’. It was a different biosphere, and its mysteries still elude us. And the fossils of Mistaken Point prove that not everything survived.

The search for the velvet worm leads to unsuspected places and puzzling worlds.

3

Slimy Mounds

Shark Bay is a long way from anywhere. In Australia, distance soon acquires its own curious rules. Within the suburban strip that lines favoured parts of the coast there are traffic jams and shopping malls like anywhere else, but away from civilisation the outback country stretches onwards forever. Far from the mountainous east, much of the country is flat. No doubt connoisseurs of the horizontal find infinite entertainment in its small variations, but for me a bemused puzzlement sets in after a few hours apparently rehearsing the same piece of landscape numerous times. Time begins to stretch in odd ways. After a snooze, I wake up unsure whether I have been asleep for ten minutes or two hours. Small eucalypts line wandering creeks while sand dunes are covered with scrub, occasional scruffy fences mark obscure ownership, and there are groves of taller gums or isolated she-oaks stocked with the noisy parrots known as galahs. Then the sequence repeats, but not necessarily in the same order. The landscape is utterly distinctive, like that of nowhere else in the world, with a stark beauty under a clear pale blue sky, but it is also relentlessly repetitive. Anyone foolish enough to leave the marked track will find it is easy to get lost. Bush stories are full of sticky ends and grieving widows. I know that maps do not really work in a landscape that repeats like an old tune whistled over and over.

Route 1, running up the west coast of Western Australia towards Shark Bay, seems never to end. The Greyhound bus runs onwards through the dark, with nothing really distinguishing the passage of miles except sporadically a startled kangaroo picked out in the headlights. Occasional vehicles pass the other way, and each one seems something of a surprise. What can they be doing out here? I have to remind myself yet again that I am en route to see one of the holy relics in geology; it will be worth the effort. After countless hours, the Overlander Roadhouse welcomes me – a neon-lit marker set down in the endless landscape; a gas station, with a rudimentary restaurant, a place to loaf about until the next bus arrives. Aboriginal people wait there desultorily for relatives who have been off to Perth or somewhere to make a few dollars. Flies buzz about, with irritating persistence; there must be something else for them to do than endlessly return to drink from the same sweaty brow, or so one would think, but round and round they go. Backpackers loiter, waiting to embark on the next section of an adventure planned in theory, but now measured out in sweat and flies. It is a kind of end-of-the-world place, on nobody’s list of ‘must-sees’, but an essential stopping point before negotiating the wilderness. This is a place where timetables mean something to somebody, a place where I can get the next bus to see the stromatolites. Not far from the Overlander Roadhouse is a place that tells us of the transformation of the very air we breathe, a window opening into remote Precambrian times.

Though the outback may look pristine, in this part of Australia the wildlife has been transformed by human introductions. Feral goats have degraded the natural bush, and cats have culled the nocturnal mammals that were once numerous. The big-eared marsupial bilby, with its back legs like a miniature kangaroo and improbably long tail, is such a charming animal that it has become a kind of mascot for the conservation movement hereabouts. It would indeed be tragic if its only permanent memorial were in one of those perfectly photographed wildlife television programmes. Conservationists in Australia have taken to referring to the ‘Easter bilby’ rather than the ‘Easter bunny’ (bunnies being voracious introductions, too). It is already too late for many small marsupials in the eastern states of the country; their only record now being watercolour drawings made by the early naturalists. These harmless creatures could not outwit intelligent feline and canine hunters, and they failed to survive. Australia is full of poignant paradoxes. This land has many ancient biological survivors yet it is also, much like New Zealand, a place where the extinction of species is still in progress. This is despite the efforts of a generation of Australians many of whom treasure their unique fauna and flora. Almost every town boasts dedicated people concerned with ‘bush regeneration’, and in Western Australia new species of beautiful indigenous plants are still being discovered regularly, even around Perth. It is a very biodiverse region, despite the challenges of the climate, and not yet fully known. While I was there Tropical Cyclone Hubert turned the sky black, and sections of the main road were closed. The species that live in this tough land must be natural survivors to be able to negotiate fluctuations between flood and swelter. That description, of course, also includes feral cats.

Shark Bay is a huge and ragged bite into the profile of the west coast of Australia. It has now become a World Heritage Area, which brings more money and more tourism. Much of the former, and nearly all of the latter, is directed to the beach resort of Monkey Mia where ‘swimming with dolphins’ is on offer. When I flew over the Bay and its clear waters in a light plane, I saw an undulating submarine prairie of sea grass, dark emerald green, broken into banks like meadows. A tenth of the world’s dugongs – 250 kilograms of peaceable herbivorous sea mammal – graze in leisurely fashion upon this luscious expanse, many living to seventy years or more. Juicy fishes doubtless account for the name of the Bay, since they attract fourteen species of sharks, including species like the tiger shark that command respect. From the air I saw how Shark Bay is divided into two large lobes by a median peninsula; the aboriginal name for the Bay is ‘cartharrgudu’ (‘two bays’). The top of the peninsula is now the Francois Peron National Park and a serious attempt is being made to clear this sandy area of feral goats and predators for the benefit of the native fauna and flora. Dirk Hartog Island provides an outer barrier to the Bay, which protects the coast from storms cutting across the Indian Ocean. I never knew before visiting Western Australia that this island was the first landfall for any European. The Dutchman, Dirk Hartog, landed here on 25 October 1616, beating Captain Cook to it by 152 years, and leaving a pewter plate nailed to a post as evidence. That plate is still preserved in the Rijksmuseum, Amsterdam. William Dampier, ‘the buccaneer explorer’, spent a week there in 1699 and gave the Bay the name we use today. The aboriginal fishermen were plying their trade at the time, but there is little evidence of them now. I conclude that it is not only small and shy marsupials that failed to survive.

My quest is for something altogether more recherché than shark or dugong. At the tip of the eastern bay the edge of the sea provides a prospect of life two billion years ago … I am travelling incredibly far back in time. The journey to the old telegraph station at Hamelin Pool takes me through undulating, intensely green scrub interspersed with a few mallee trees, interrupted only occasionally by flat-bottomed depressions carrying scrappy salt-scrub and patches of white gypsum – the aboriginal inhabitants called these clay-pans birridas. I missed the flowering season, and now all the bushes seem to bear black nuts. Next come low dunes made up of startlingly white tiny shells. I crunch my way across the dunes, and beyond lies a very shallow arm of the sea. This is where the stromatolites grow. I am approaching the famous site where living analogues still flourish of the most ancient organic structures on earth. They ought to have disappeared long before the first velvet worm or horseshoe crab, but here they linger on, a marvel of anachronism.

Back at the highway must be the only road-sign in the world that points to ‘STROMATOLITES’, and no geologist or palaeontologist could fail to follow its bidding. Here they are growing by the shore while the sea beyond shines an almost improbable ultramarine. Is this luminous vision the time warp I sought? Some part of me expects the stromatolites to be green, but they prove to be darkish umber brown. I confess I am momentarily disappointed. They comprise flat-topped cushions and low pillars, or even giant mushrooms expanding upwards like plush stools, with sandy gullies between them. They are regularly disposed along a seaboard more than a hundred yards wide; seawards they disappear beneath the barely lapping waters. It is a scene of perfect calm. A little walkway has been built over the strand so that visitors can get close without damaging the organic structures. I touch one of the hummocks. It is actually quite hard (why did I expect it to be soft?) and slimy or tacky to the touch when moist, but almost crispy when dry. In the bright Australian sun it is even a little warm. Now that I get closer I can see other kinds of surfaces along the shore, particularly sloping stretches of dimpled microbial mats, a fruity brown colour, running down to the glittering sea. They make stretches of the shoreline resemble wrinkled skin. Stromatolites growing at the water’s edge look less like cushions and more like knobbly cauliflower heads. The inevitable flies are buzzing about my head, and some antipodean swallows chirrup cheerfully about the platform. I hope they are after my flies.

Up on the shore are some dead stromatolites, left behind by the sea maybe a thousand years ago. By now they have decayed into iron-stained ruins, but where they have broken open they show the internal structure of the cushion-shaped columns. It is clear to me that the columns are layered internally parallel to their top surfaces, rather like filo pastry. They seem to be built up layer by layer – a little like those giant stack pancakes an unwary visitor gets offered in New York for breakfast. The columns were evidently living things, self-made towers. A little museum on the site of the old telegraph office nearby provides more explanation. I peer closely at a stromatolite kept in a glass tank; its enveloping seawater must be refreshed every month. I see that when water covers the column its surface is slightly fuzzy – no doubt, it is still alive. A lack of crisp definition is somehow a proof of metabolism in action, life blurring the edges. Little bubbles fizz upwards off the top in a steady stream, none bigger than a lentil: they are bubbles of oxygen. So the column is evidently more than a brownish crust, it is something altogether more potent and dynamic, and it is breathing out oxygen, the element that babies and bilbies and bunnies all need to stay alive. Everyone has had nightmares about suffocation, when fighting for breath becomes fighting for life, so we all know in our bones how quickly we would perish without oxygen. The exhibition reminds me of the demonstration of nature in action at my very first school, when us kids looked at water-weed in a full glass beaker, and saw the same little bubbles of oxygen rising to the surface. This was the first time I heard the word ‘photosynthesis’.

The survival of the stromatolites on the beach is another measure of their toughness. On the foreshore I see two broad grooves carving their way through the stromatolite grove. These are the persistent traces of a former industry. In the late nineteenth and early twentieth century, camel trains brought bales of wool here to Flagpole Landing. These were then carted off the foreshore to lighters that sailed 190 kilometres to a boat waiting in deep anchorage off Dirk Hartog Island. Then the wool was transported to Fremantle and finally to the United Kingdom for manufacturing. We are fortunate that these activities did not destroy the mounds completely. But it is also a measure of the slow rate of biological activity hereabouts that the old tracks are still visible after a century.

Sea conditions in this part of Shark Bay are quite particular. The shallow seawater evaporates fast under the relentless sun. It is the basis of a salt industry at Useless Loop nearby. The very clear water has an elevated salinity and is very poor in nutrients. Hamelin Pool is backed up behind a sand bar known as Fauré Island, lying about forty-seven kilometres out to sea, so it is almost a lagoon. Only specially adapted or tolerant organisms can survive under these conditions. One of those animals is a little clam called Fragum hamelini, which, as the name implies, is special to this locality. It is so abundant that its snow-white shells, none bigger than a walnut, make up the dunes that line the Bay. After some decades the shells harden into a shelly rock – it would be an exaggeration to call it a limestone. An old quarry above the shore records the employment into which this curious white stone has been pressed. Cut into blocks the size of large bricks it made a serviceable, if hardly robust building stone. Some of the older edifices made of it still stand. The stone was used to build the walls of the Pearler Inn in the town of Denham, eighty kilometres distant. This pub looks as if it were constructed from a mass of white peas. In order to survive the testing conditions in the Bay, Fragum has incorporated photosynthesising algae into its tissues: sunlight is the ultimate source of its food, just as it is for the stromatolites. But Fragum is an evolutionary newcomer, whereas the stromatolites are very, very ancient.

Stromatolites are mounds slowly built up by microscopic organisms, layer by layer. The mounds are not composed of a single organism: they are a whole ecology. The tacky or slimy skin that caps the stromatolites is the living part. This very thin layer is composed mostly of cyanobacteria, organisms that are often called ‘blue greens’ (or, formerly and incorrectly, blue-green algae) on account of their characteristic hue beneath the microscope. This may well explain why I expected the stromatolites to be green. The conditions in Hamelin Pool suit their growth. There are many organisms in nature that like to graze on ‘blue greens’. Think of those finely scalloped trails wandering over moist rocks by the seaside, made by the rasping action of the sea snail’s feeding apparatus as it scrapes away the thin nutritious bacterial layer that paints the rocky surface. This is not inappropriately compared with grazing by herbivores on terrestrial environments. Like grass, the ‘blue greens’ grow back, and the molluscs move on. But these micro-organisms never have the chance to build complex or elaborate structures like mounds or ‘stagshorns’ because the constant assault of herbivores renders their best attempts at architecture futile. Everything is eaten back before it can grow too big. However, in the special, warm world of Hamelin Pool the grazers are kept at bay. No snails sully the sticky surfaces of the stromatolites; the fish there don’t nibble away the ‘blue greens’ for supper; in fact, nothing much ventures into the almost unnaturally limpid seas. Some authorities believe that the very low nutrient levels in the Pool are as important in growing stromatolites as the absence of grazers. Whatever the reason, the simple organisms have it all their own way for once. And when they do, they reconstruct the Precambrian world. This is how life was before marine animals chomped and scraped away ancient biological constructions that had covered much of the sub-aqueous environment since life began. In Shark Bay a prelapsarian age can be restored to view, a time before velvet worms or even vendobionts, or anything that crawled upon its belly in the mud. I have seen dozens of artist’s reconstructions of ancient seascapes that owe a debt to the prospect at Hamelin Pool. So when I saw the living stromatolites I was not unprepared for the experience. However, I recall seeing Picasso’s Guernica for the first time; just because an image is familiar does not diminish the impact of the real thing.

Cyanobacteria are simple organisms that often make long, green and narrow threads with organic walls which can be as thin as a few thousandths of a millimetre, but which often occur in sufficient profusion to make green slime. Other species are tiny round cells that grow by fission – essentially splitting in two, to double up as identical twins. They are ubiquitous. When a glass of water is left in the light on a window ledge, cyanobacteria will usually appear as a green smudge. They have been wrongly called ‘blue-green algae’ in old textbooks, but as we shall see the algae are altogether more complicated organisms. When raindrops wash over rocks in a desert these tiny organisms will soon take advantage of the opportunity to grow, and the rocks will shortly glisten with microscopic life. In the sea, their numbers occasionally erupt into ‘blooms’ of billions of cells that can poison fish, or even humans, if they eat the wrong kind of shellfish too soon after one of these events. In biological jargon the ‘blue greens’ are described as prokaryotes. They are both the smallest and the simplest-looking cells – often no more than a sphere or a sausage – but there are hundreds of different species. They lack an organised nucleus surrounded by a membrane that is present in every cell in what are termed eukaryotes. Every organism that has been mentioned so far in this book (including the author) is a eukaryote, which is another way of saying that our narrative has now arrived back to a simpler way of organising a living entity. Prokaryotes came before eukaryotes in time, which also means that they are closer to the main trunk of the tree of life. So there was a world before eukaryotes where the cyanobacteria were state-of-the-art and where the prospect before us in the shallow waters in one corner of Shark Bay would have been typical of much of the world, rather than a special survivor. I should flag up at this point that this prokaryote– eukaryote division is itself an over-simplification, and this topic will be revisited in the next chapter.

Modern seaweeds are both plants and eukaryotes, to emphasise the point again, and do not build stromatolitic mounds. In Shark Bay, the majority of such ‘advanced’ organisms are discouraged by the low levels of nutrients available there; hence they leave the dominant cyanobacteria to cooperate in making different kinds of mounds. In the typical stromatolite the mode of growth is cumulative. The living ‘skin’ is a thin layer of growing threads matted and twined together. The technical term for it is a ‘biofilm’. The cyanobacterial mats are positively attracted to light and grow upwards. Any blown dust and other fine sedimentary material becomes incorporated in the surface layer and maybe provides the modest nutrient required. The slimy surface layer of the bacterium encourages the precipitation of calcium carbonate from its dissolved state in seawater, thus making a thin ‘crust’. A new living layer grows on top of the one beneath, and may be able to extend a tiny bit further laterally: this is why some of the stromatolite mounds are wider at the top than at the base. Naturally, the ‘blue greens’ are only able to grow in the sunlight that gives them nourishment, and are quiescent at night. Some scientists at the University of California even claim to have recognised daily growth increments. The overall rate of growth is extraordinarily slow, however, and certainly less than 1 mm a year (and possibly as little as 0.3 mm). It has been stated that some of the Hamelin Pool structures could be a thousand years old, that is, they grow more slowly than the slowest-growing conifer on land. The life and death of the wool industry would register as no more than a hand-depth on the height of a stromatolite column. Time can be ticked out in microscopic laminations, and history reduced to a measuring stick made by timekeepers invisible to the naked eye.

Stromatolites vary in form according to where they are found on the shore. It is easy for me to see that ones at the edge of the sea are little more than pimply mats. At least to this unschooled observer, some of them superficially do not look very different from some of the mats that covered sediment surfaces in the Precambrian at Mistaken Point. They are made particularly by one of the spherical, or coccoidal types called Entophysalis, and the internal layering is not well developed. Further down the shore in Hamelin Pool the stromatolites that I tentatively touched represent the dominant kind in the intertidal zone, with a typical columnar-cushion shape. This kind of column is constructed particularly by a filamentous cyanobacterium called Schizothrix, which under the microscope is an intense emerald-green colour. It has lots of apparent partitions that make the organism look something like an old-fashioned tube of circular cough sweets. These particular stromatolites are very well laminated internally, so that the mechanism of being built up layer by layer is particularly patent. It has been proved that the cushions ‘lean’ a little to the north, each component filament attracted preferentially to the sun (but on such a minute scale) in this, the southern hemisphere; the god Ra evidently ruled in the prokaryotic shallows. Further out to sea again, to a depth of a little more than three metres, there live the lumpier, bumpier, lobed, and somewhat rounded stromatolites that are a collaboration of many different microbes. These include cyanobacteria of the genera Microcoleus and Phormidium; the latter is another concatenation of delicately segmented threads, while the former comprises microscopic ‘ropes’ made up of bundles of a kind of entwined green spaghetti. The different species collaborate to grow together, like a confederation of medieval guilds, with each tiny specialist contributing to the function of an integrated community. True algae – diatoms – may chip in as part of the community among the deeper water stromatolites, but this group of eukaryotes probably did not evolve until much later. Beneath the surface skin of the growing mound, bacteria of a different kind from cyanobacteria process waste products and can cope with low, or even no oxygen; they are like artisans that moved the dung from the streets of the medieval village and made it a trade. Life encouraged specialised habits and habitats from the first.

Stromatolites are the most ancient organic structures, and their recognition as fossils transformed the way we understood the endurance of life on earth and the evolution of its atmosphere. I admit that viewed with complete impartiality when it comes to visual impact, the Shark Bay mounds are not on a par with the Empire State Building or the pyramid of Cheops. But stromatolites are one of the wonders of the world. Rationalists are not permitted to have shrines, but if they were then Shark Bay, where stromatolites were discovered alive, might be high on the list. Although many more living stromatolites have since been discovered, those in Shark Bay have been most thoroughly studied. From their initial recognition in 1954 the fame of these living stromatolites spread, until by the late 1960s they were finding a place in textbooks. As so often happens in science, the discovery of these living mounds happened just when palaeontologists were making major finds of microscopic fossils in rocks of Precambrian age, opening up debates about the biological history of the earth. The strange creatures of the Ediacaran, like Fractofusus and Charniodiscus, took the record of life back tens of millions of years before the great burst of familiar fossils such as trilobites that appeared in the Cambrian, 542 million years ago. But there remained more than three billion years of the history of life on earth in the Precambrian still to account for. This was the era of the stromatolites.

It is necessary to have a digression on geological time at this point. The age of the earth had been established at close to 4.5 billion years by the time Shark Bay was becoming known to the scientific world. The precision of this figure was largely a consequence of refinements in dating techniques, using the slow radioactive decay of naturally-occurring uranium isotopes into other isotopes of lead: turning rocks into clocks, one could say. The samples collected from the moon by the Apollo Mission were first unpacked on 25 July 1969. I recall the excitement of seeing a small black piece of the earth’s barren satellite when samples from the collection made on the Sea of Tranquillity were distributed to major museums, including the Natural History Museum in London. Like the stromatolites, it was not so much the thing itself; it was what it implied that made it so special. After the moon rocks were dated using the best technology of the day the question of the antiquity of the green planet to which the moon was partnered was finally laid to rest: 4.55 billion (plus or minus 0.05).

The geological time period before the Cambrian was simply known as Precambrian for more than a century – after all, that is what it undoubtedly was, ‘before the Cambrian’. But when this time period was recognised as so vastly long, it became necessary to divide it into several named chunks to help us order events in the earth’s history. The Archaean Era is that part of deep geological time that ends at 2500 million years ago, or 2.5 billion years if you prefer. After this came the Proterozoic Era which, in terms of strata, lies above it and extends to the base of the Cambrian Period 542 million years ago (the Cambrian is the first subdivision of the Palaeozoic Era).

The Ediacaran, the latest addition to the roll call of geological time, begins at 635 million years ago and is slotted into the top of the Proterozoic. The Proterozoic Period covers a very long period, and these days is usually divided into three which used to be known as Lower, Middle and Upper, but are now formally known as Palaeo-, Meso- and Neoproterozoic respectively. The Neoproterozoic begins arbitrarily at 1000 million years ago, and the Mesoproterozoic at 1600 million years ago (1.6 billion), so the Palaeoproterozoic occupies the time period 2.5–1.6 billion years ago. Names really do help us get a grasp on the immensity of geological time, though phrases like ‘Palaeoproterozoic digitate columnar stromatolites’ do not exactly trip off the tongue. But it is as well to get our labelling sorted out.

This modern classification is the end point of a long scientific battle. The intellectual classes had been debating the question of the age of the earth since the Comte de Buffon’s estimate of 75,000 years in 1774 based upon the idea of the planet cooling down from a molten state. Apart from a purblind few who insisted (and indeed still insist) upon a biblical timescale based on totting up the generations mentioned in the Bible – Bishop Ussher’s 4004 BC estimate for the Creation – the time available to ‘evolve’ the earth increased fitfully throughout the early days of geology as a science. The bolder savants soon speculated in more and more millions. The longer time got, the more questions were raised about life’s early days, because of the apparent absence of ‘organic remains’ in Precambrian rocks. Charles Darwin famously fretted about it. Geologists of his time were beginning to explore large areas of the world comprised of Precambrian strata as the rocks of countries such as Canada were mapped for the first time. It was soon evident that sedimentary rocks, much like those found in younger geological formations, were widespread over these ancient lands. The seas were apparently barren in these ancient worlds; seas not so different in their physical properties from those that gave succour to the trilobites and snails that could be so easily collected from younger strata. In 1883 the American palaeontologist James Hall found some intensely layered Precambrian rocks apparently ‘growing’ upwards incrementally from a narrower base to which he gave the name Cryptozoon (‘hidden life’); however, their organic nature still remained controversial. Nonetheless, with the mere application of a scientific name, the biological virginity of the Precambrian had been breached. It was time for the stromatolites to be recognised as organic constructions.

The first time I saw fossil stromatolites in the Precambrian was as an undergraduate at the University of Cambridge, when I took part in an expedition to the Arctic island of Spitsbergen in 1967. My doctoral thesis was to be on rocks of Ordovician age exposed along the cold remote shore of Hinlopen Strait on the eastern side of a northerly peninsula called Ny Friesland. The small boat that took us to our field area dodged between ice floes stained with the droppings of countless seabirds, for the Arctic summer is a brief period of plenty for animals that live off the ocean. On land the scenery was bleak: a succession of cobbled beaches raised above the present sea level, across which the occasional polar bear or Arctic fox wandered in search of a feathered snack. It was not an inviting prospect, although it was to be my home for several months. On the way to reach my Ordovician rocks, and before passing the Cambrian strata that lay beneath them, the boat had to chug past a great thickness of even older Proterozoic limestone and shale, piled up layer on layer. There are few places in the world where a young scientist can cruise through such a momentous stretch of geological time, let alone along an outcrop that has survived so unaltered by subsequent earth movements. These ancient rocks were in almost pristine condition. On one occasion we landed to make a temporary camp and pick up fresh water. I wandered over to the nearby rock outcrop just to have a look. The rocks were not horizontal; instead they had been tipped gently (but less so than the rocks at Mistaken Point). I could easily make out the flat bedding planes breaking up the shore into a series of steps that recorded a succession of former sea floors. The rocks were a mixture. Most were very pale grey, sometimes almost pearly, and hard looking. Others were yellowish, in patches somewhat sugary and brightly tinted. The latter were dolomites, a calcium magnesium carbonate rock that at the present day particularly forms in areas surrounding the more arid tropical regions. The off-white rocks were limestones, that is, made of calcium carbonate in a finely crystalline form. Looking closely, I could now observe that several of the limestone surfaces were finely scored. Many years of erosion had picked out subtle differences in hardness within a single bed of limestone, so that lines even a millimetre or so apart could be clearly discerned. A comparison with layered pastry came to mind. I imagine that a blind man could have read the rock surface like Braille, just by gentle palpation. Where the rock surface was weathered at right angles to the bedding surface, providing a natural cross section, these finely-layered rocks were arranged in a series of undulating columns, widening a little from their base. They were stromatolites, or to be more accurate, sections through stromatolites – with a thousand years or more of slow growth preserved in a fossil grave of fine limestone. Cryptozoon proved to be not so cryptic after all; it was the stony legacy of cyanobacteria. When I followed the stromatolites over onto the bedding plane beyond to get a vision of the ancient sea floor, they converted into balloons or pillows stretching away from me, each one showing the top of a stromatolite head. This was the fossilised version of the view at Shark Bay I was to admire decades later. It was bleached to white limestone by the passage of a thousand million years, perhaps, but it was still recognisable, a picture petrified from a former earth. This was the nearest thing I will ever experience to being in a time machine, even if my appreciation of it were countermanded at once by the shrill cries of Arctic terns above my head: chicks to feed, human business to be done, and the earth has moved on. Nothing remains exactly the same forever.

Had I looked more widely along that unwelcoming shore I would have observed a greater variety of shapes carrying the telltale laminations of stromatolites. I would also have noticed some occasional shiny black patches within them; these are made of chert, a very hard, flinty rock composed of the mineral silica. Andrew Knoll, who is perhaps the doyen of Precambrian palaeontology, visited the same rocks in Spitsbergen a few years later, as he has described in his book Life on a Young Planet. From those cherts he recovered remarkable small fossils, which helped to make his reputation. He also recorded a whole range of different rock types produced by ancient micro-organisms; the most general term for these rocks is ‘microbialites’ which is a term that I trust does not require further explanation. Subtly mottled microbialites can present the appearance of ornamental marble, or the interior of a sponge cake, or the dimpled mats that I saw on Shark Bay; they can all be attributed to the work of bacteria and their relatives. Evidently, ancient microscopic communities did not just manufacture columns, though these do display several different shapes. Over much of the vast compass of Precambrian time it was a dominantly microbial world, and there was nothing to prevent tiny organisms from constructing a variety of edifices.

Stromatolite fossils are not at all rare if the right rocks are explored. It is not surprising that many rocks have been altered by heat or pressure if they have sojourned on the earth for billions of years. The great motor of plate tectonics has been continuously in operation, building mountains and moving continents around. It is a lucky rock that escapes unscathed. Most of those that have successfully dodged being crunched or heated up are found around the edges of the most ancient and stable continental cores often known as ‘shields’. These bits of earth’s crust stabilised early on, and have been pushed around the earth during successive phases of continent building rather like counters being shoved around a draughts board. They survive to play another game. If there are patches of stromatolites preserved upon them, they are handed onwards. Perhaps the Canadian Shield is the best known of these ancient areas, but parts of southern Africa and Western Australia are equally familiar to geologists. However, the list of stromatolite occurrences is much longer than that of ancient shield areas, the rocks Andrew Knoll and I examined in Spitsbergen being a case in point. It is obvious that these strange organic structures were almost ubiquitous at least in the shallower parts of ancient oceans. Cyanobacteria would have needed light to grow, so the particular stromatolitic structures made by them must have been confined to comparatively shallow water. The early Precambrian ocean depths are unknown to us, since ocean floors are consumed in the inexorable slow dance of the plates. But it is more than likely that there, too, were structures made by different bacteria that flourished away from light. After all, life never misses a trick.

Stromatolites are found way back into the Archaean. The oldest ones of all are almost miraculous survivors found on the scraps remaining today of the most ancient continents. Fossils dated at 3.5 billion years old have been found in the Apex Chert in Western Australia,

and in Swaziland. It is hardly possible to imagine such antiquity. I have the same trouble trying to grasp the number of stars in the Milky Way, for the mind soon loses its normal frame of reference when the figures get so large. I can probably do no better than echo the words of the pioneer geologist John Playfair in 1788, when he became convinced of the reality of the vast age of the earth: ‘the mind seemed to grow giddy looking so far into the abyss of time’. Nonetheless, it is important to at least get a feeling for this ‘abyss’, an intuition of its magnitude, because it shows just how long it has taken for life to arrive where it is today. The two stories of life, and the earth itself, have been intimately intertwined for billions of years.

Stromatolites began in the Archaean as relatively simple domes, but later they evolved into a number of different forms. Some of the more distinctive shapes have been dubbed with Latin names, just as if they were organisms in the conventional sense (Pilbaria perplexa and the like). As we have seen, they are actually collaborations between several organisms, so such an approach does not fit in with normal biological procedure. However, it is useful to have a way to refer to different shapes and forms, and some of the names have achieved wide currency. In the far reaches of the Precambrian, stromatolites could grow in a wider range of marine environments than they do now, and this may partly account for some of their different shapes. In deeper or calmer water, for example, it was possible for relatively delicate, branching, even candelabra-like forms to grow. In complete contrast, one of the most distinctive varieties produced massive cone-shaped bodies that could grow to be tens of metres high. These microbial behemoths have received the appropriate name Conophyton (‘cone plant’). They have been memorably described as making outcrops in the field look like a series of rocket launchers placed side by side: they must have taken many centuries, even millennia, to grow. The vocabulary used to describe different kinds of stromatolites gives some indication of their variety of form; they have been compared with fingers, fists, cauliflowers, columns, spindles, trees, mushrooms, kidneys. Given time enough these most simple organisms could produce an art gallery’s worth of shapes. Nature was patently a sculptor from the first. The view from Hamelin Pool was, it now transpires, only a partial glimpse of a richer, but now vanished stromatolitic world.

The controls on stromatolite growth were probably quite simple. The growing surface film was attracted towards the sun, while the supply of calcium carbonate from seawater dictated the dimensions of the layers produced. A group of Australian physicists have developed computer models that ‘grow’ stromatolites by playing around with these simple elements. Conophyton emerges naturally as a shape in response to strong solar attraction; prokaryotic life, it seems, simply could not help building regular structures. Where there’s life there’s architecture. But there is also good evidence that the variety and complexity of stromatolites increased during their extraordinarily long tenure of the earth’s seas. The few kinds of simple domes and cones that dominated their first billion years, during the Archaean, were supplemented by dozens of additional shapes during the Proterozoic, when branched structures and pleated columns on many different scales appeared. The first occurrence of particular stromatolites has even been used broadly to subdivide this long period of time. They probably achieved their greatest variety about a thousand million years ago, but still long before the emergence of large animals, even the strange Ediacaran ones. Many early stromatolites were fully submarine, rather than living between the tides. Their living analogues have been found in the Bahamas near Exuma Island, hidden in marine channels. Here, these large, lumpy columns rising from a lime-mud sea floor probably provide a closer match to many Proterozoic environments than does Shark Bay. The biofilm forming the living skin is known to be a complex microbial community, and much more than just a photosynthesising surface. Several other kinds of bacteria have their homes there, some with the capacity to ‘fix’ nitrogen, like the little nodules harbouring bacteria that grow on the roots of beans and contribute to soil fertility. These kinds of bacteria work at night, when the cyanobacteria are ‘sleeping’. Once again, the mat is a whole ecology, a world measured in millimetres.

As for the fossils of the organisms that made the Precambrian mounds, the apparent absence of which so perplexed Charles Darwin and his contemporaries, well, they were lurking there all the time; it is just that they were very small. The cherts, like those tucked among the limestone rocks on Spitsbergen, held the secret. In some cases such siliceous rocks were formed early enough to petrify the fine threads and other cells making up the ancient biofilm. The process is somewhat analogous to that involved in making artificial resin souvenirs in which butterflies or scorpions are preserved, colour and all, which then lurk on the mantelpiece forever. Silica petrifactions were already well known from higher in the geological column, even preserving tree trunks down to the last cell. Considering that the dimensions of the Precambrian fossils are often measured in a few thousandths of a millimetre, the preservation of their cell walls is remarkable, almost miraculous. However, when very thin sections were made of the right Precambrian cherts they became transparent; these preparations were then examined under the microscope and revealed the unmistakeable imprint of life. The discovery was reported in detail in 1965 by the resplendently named American scientist Elso Sterrenberg Barghoorn Jr based on fossils obtained from the Gunflint Chert, a rock formation exposed along the northern shores of Lake Superior. Barghoorn’s co-author, Stanley Tyler, had previously recognised fossil stromatolites preserved in rather beautiful red jaspers (an iron-rich form of silica). At the edge of the Canadian Shield, the Gunflint Chert was one of those special survivors that had escaped the subsequent adventures of our mobile planet, fortuitously frozen in its own ancient time. At 1.9 billion years old, the fossils of the Gunflint Chert lie well down in the Palaeoproterozoic. Among the organic remains seen in thin sections of the chert, the commonest are probably thin threads not unlike those so abundant in living mats and biofilms. Some of these show the kind of transverse striping that are typical of some ‘blue greens’; interestingly, the threads are narrower than they were later in the Precambrian (and narrower still than they are today). They are accompanied by a range of other tiny organisms, some generalised rod-like bacteria, others more distinctive, like the spherical Eosphaeria with its cell walls apparently divided into compartments, and the enigmatic Gunflintia. Palaeontologists continue to argue about the biological identity of some of these fossils, although it is beyond doubt that ‘blue greens’ were certainly present among them, but the important point is surely that this is an early community, already divided into different biological ‘trades’. The kind of prokaryote collaboration happening today was already happening then. Stromatolites were indeed true survivors.

But back in the 1960s, the fossil search was on! The world was scoured for younger, older, similar or, in particular, new and unnamed Precambrian small fossils. Africa, especially Namibia and Swaziland, was mapped and investigated; Australia, especially Western Australia, was crawled over; the Old World was looked at again, and much of the New World was looked at with new eyes. Precambrian fossils turned out to be very widespread, and new discoveries were nearly always heralded by someone spotting stromatolites in the field, which hinted at what might yet be found at the microscopic scale. Geologists’ boots tramped up wadis in deserts, their hammers whacked at Arctic cliffs, and their hand lenses focused on limestones outcropping deep in the Siberian taiga. These last devoted geologists bore the scars of marauding mosquitoes for weeks. Then by dissolving Precambrian shale in hydrofluoric acid still other microfossils with organic walls were extracted, to be studied in detail on microscope slides. University departments hired staff, and the growth in knowledge was exponential. Many of the famous names in early evolution were students of, or collaborated with, Elso Barghoorn. Andrew Knoll was among them. Bill Schopf, an equally grand figure at the University of California, Los Angeles, is now the elder statesman of the Barghoorn disciples, and did much to push the record of life and its fossils further back, into the Archaean.

Lynn Margulis may be the most luminous name of all those scientists associated with Barghoorn. She espoused and championed an idea that has transformed our way of understanding the history of life. There is a lot of hype in science nowadays, the more so since big claims often result in further research funding. I have never heard anybody announce ‘a minor discovery’ or ‘a modest advance’. I have also become allergic to the media’s phrase ‘the textbooks will have to be rewritten’ since it conjures up an inaccurate vision of textbooks being hurled with a curse into the waste paper basket on a regular basis. Textbooks are rewritten, but most scientific discoveries are passed from one edition to another, since science generally works by piling bricks of knowledge one on another to make a solid edifice. It is very unusual to scrap a whole chapter and start again. However, this does happen on occasion, and one such occasion was when it was claimed that eukaryote cells originated by a kind of piracy. The vital organelles within eukaryotic cells – things like mitochondria and chloroplasts – were originally free-living prokaryotes. The more complex cell was a result of a hijack, whereby former free-living bacteria were summarily tucked away inside the swag bag of a bigger descendant cell. Unlike the human hijack, though, all parties benefited: the scientific term is symbiosis. The formerly ‘free’ bacteria proliferated in their new habitat, sequestered away from harm. The newly enhanced cells took advantage of the novel vital functions tucked away inside them. For example, in plants the captured chloroplasts concentrated photosynthesis into special sites within the safety of a eukaryotic cell. Plants could now prosper using the energy of the sun. By contrast, mitochondria localise the ‘furnaces’ providing the chemical energy for life, which is essential for organisms to feed and grow. Malfunctions in these organelles are usually lethal, so deeply are they embedded in the ‘works’. Variegated varieties of garden plants can have white patches lacking chloroplasts, but such varieties are selected by gardeners for their appearance, not by nature for efficiency. Such an origin for complex cells is called the ‘endosymbiont theory’ – ‘endo’ meaning ‘inside’ symbiosis. Complex cells arose by incorporation of simpler ones, for mutual benefit. It altered our understanding of life’s early history to such an extent that not only had the textbooks to be rewritten, but there also had to be new books to replace the old ones in their entirety. The theory was triumphantly vindicated when the DNA of chloroplasts was investigated and found to be similar to that of free-living photosynthesising prokaryotes. The organelles tucked inside complex cells were, indeed, closely related to free-living, simple prokaryotes. This is the kind of confirmation that most of us can only dream about. It was almost as good as getting into a time machine and travelling back to the Precambrian. The phrase ‘endosymbiotic events’ was soon incorporated into foundation biology classes. Like all science, the story has got much more complicated since the initial insight, as more and more acts of cellular piracy have been detected, but all the complications serve to reveal yet more events deep in geological time.

6. Endosymbiotic/endosymbiont theory: a complex cell ‘in the making’ engulfs a formerly free-living prokaryote, which is then retained as a symbiont rather than being digested. This process happened several times, thereby introducing many more possibilities for life.

I should mention that none of these distinguished scientists conforms to the common preconceptions of the ‘geeky’ white-coated specialist. Bill Schopf is a bon viveur and raconteur, with a very persuasive laugh, and a relentless drive for discovery. Andrew Knoll is the kind of American who makes most of us poor Europeans feel as if we were only given half a ration of energy at birth. He has projects spanning most of the world, and a stable of exceptional students to take the work forward. He manages everything with a kind of urbane good humour and insouciance that defuses any possible resentment at his omniscience. Lynn Margulis is unique. I know of no other professor who would, or indeed could, quote the poet Emily Dickinson at length in a supermarket. As a long-term maverick she is always on the look out for ideas that will provoke and encourage new ideas (and completely undeterred that some of them may well prove to be wrong). Her dress style is equally distinctive, featuring embroidered waistcoats and pleated skirts, as if she were about to take part in a folk festival. She has an intuitive grasp of the important collaborations that makes the world work; not just the ubiquitous and versatile bacteria, but also chemistry, and geology, and politics.

This account of the geological importance of stromatolites and their discoverers has entailed a distraction from the little bubbles that provide the nub of this chapter. Recall the tiny gas beads rising from the top of the stromatolite in its tank, arising from a living biofilm breathing out oxygen. Now combine that scene with the picture I have attempted to paint of the fledgling earth in the Archaean and Proterozoic, where shallow seas and lagoons were covered with stromatolites, some of them gargantuan by recent standards. Imagine thousands and thousands of dimpled miles, exhaling oxygen by day in a thousand billion tiny bubbles, stimulated by the primeval sunshine. Even the slimy surface of the threads had a part to play in mitigating the effects of harmful ultra-violet radiation; we should all be grateful to slime. Now imagine this process continuing for billions of years, six times longer than the history of the velvet worm. The effect was to change the atmosphere, bubble by bubble. The early earth had little or no free oxygen; the ‘blue greens’ changed the air itself. Animals need to breathe oxygen to power their life functions. They could not exist before the slow, relentless preparation of the atmosphere effected by lowlier organisms on the tree of life: no gills, no lungs, no blood blue or red. If some malevolent God were instantly to reverse the work of the stromatolites we should all be gasping on the ground like beached trout within minutes. So we are, in a sense, the children of the sticky mounds.