IN THE ROCKS ABOVE THE TRACES and tracks left by soft-bodied animals, there are tiny tubes. In hand specimen they often show as little more than mottling on the bedding surface of the rock. But where limestone formations are developed at precisely this geological interval, as they are in many parts of the world—in China, Russia and Australia—the rocks can be dissolved in dilute acid and the tubes are recovered from the residue by sieving. Many of them are composed of calcium phosphate, which does not dissolve in the acid. A glance quickly reveals that there are several more shapes than simple tubes—there are coils, and little asymmetrical scales, and twisty shapes looking much like the favourite fried snack the Spanish call churros. There are a few things that are obviously tiny shells. Then there are some little spines, often branched, which are recognizable as the skeletal components of sponges, known as spicules. Tube, shell and spicule are all hard—animals had evidently learned to secrete skeletons. This means that we have passed into the Cambrian period, which is marked for the first time by shells. And most extraordinary of all is that in all the appropriate rock sections around the world, whether they are exposed in the bleak cliffs of Newfoundland, or the hot, dry creeks of Australia, the story is the same. There is a sudden appearance of what palaeontologists call “small shelly fossils” above the Precambrian rocks. Since the earliest fossils include closely similar species throughout widely separated and scattered localities, the conclusion is inescapable: this momentous development of shells happened all over the world within a short time, just a few million years. From now on, for the next 540 million years, the fossil record would become prolific, because hard minerals are routinely preserved. Animals with skeletons appeared for the first time,* and with them the first hints of all the achievements of biological engineering which were to come. In the biosphere size really matters, and large size requires mechanical support. The possibility of the blue whale was implicit in these first humble remains.
The very earliest tube of all is now known to just predate the great diversification at the base of the Cambrian. It is called Cloudina, and its name celebrates Preston E. Cloud, one of the pioneer investigators of this great watershed in the history of life. It is an odd little thing, just a millimetre or two in length. Its mineralized skeleton was probably composed of calcium carbonate (calcite), like most sea shells today. Sheets of such calcite were arranged in stacks rather like those piles of paper cups that are found beside soda fountains. Nobody knows to what living animal Cloudina might be related.
In the rapid diversification of the “small shellies” at the base of the Cambrian there are many other unsolved identities. For example, many different things could live in tubes, and the shapes of the tubes provide no clue as to their identity. As at one of those ghastly parties where everyone is supposed to turn up as Count Dracula, the more effective the disguise the harder it is to recognize who anybody is. Ellis Yochelson, a grizzled and often sagacious mollusc expert at the Smithsonian Institution, in Washington, DC, was fond of saying, “What the hell, call them all worms,” which has some pragmatical advantages, although it does rather beg the biological questions. In some cases the disguises have, in part, been penetrated. It used to be thought that the phosphatic skeleton of many of the early shells was an original feature—and hence that this material (which is related to the material of our own bones) was at a distinct advantage in the genesis of mineralized tissue. Now, after a careful study of the microscopic preservation of the shells, tubes and plates, investigators are convinced that in some cases the phosphate actually replaces an earlier shell, which was likely to have been composed of calcium carbonate, much the commonest shell material among living animals. There were rather more phosphatic shells at the start of the Cambrian than there are now, to be sure, but calcium carbonate was found with similar frequency at the time of the inception of shells. Sponges and certain single-celled animals, like radiolarians, used silica (SiO2) for their skeletons, just as they do today. Curiouser and curiouser, for it seems that all common skeletal materials got going together, synchronously, even though common sense might tell us that they should require different conditions for their secretion by living tissues.
Now there are some more puzzles. It seems possible that the early shelled animals were not as small as the tiny fragments recovered in sieves might suggest. In 1990 a remarkable creature several centimetres long was discovered in the Lower Cambrian rocks of Greenland. This strange Halkieria was composed of literally hundreds of tiny plates arranged in ranks, like chain mail, over its back. Even more extraordinary, there were two additional, very much larger, nearly circular plates positioned at either end of this tessellated oddity. The small plates were totally different in shape from the larger, and there was no reason to associate them until the amazing find was made. The isolated bits—or sclerites—had been discovered many years previously, and had already been given different names. Whatever this odd animal was, it evidently fell to pieces when it died, and in this fashion one individual spawned numerous fossils. The new discovery thus banished several mystery organisms at a stroke, only to generate a single, more obdurate enigma. It also highlighted the possibility that other small shelly fossils might be pieces of something larger. The distinguished Swedish palaeontologist Stefan Bengtson, for example, believes that Halkieria was a mollusc, and records an important stage in the evolution of shells: he thinks they started out as little elements which became fused to form a continuous mineralized covering. One of the most primitive living molluscs, the chiton, is still composed of a small number of rows of plates: Halkieria allegedly recorded an even earlier stage when the rows were more plentiful. It is not an entirely satisfactory answer, because it still does not explain the big plates that Halkieria also carried.
It is now becoming clear that other species of the earliest skeletized animals were merely sclerites belonging to something larger. There are the curious tommotiids, genuinely phosphatic animals with very irregular little plates, but so far nobody has found more than one or two plates hanging together. Sponges are not so arcane because living examples still put their skeletons together from fine struts and rods (spicules). They interlink in much the same way as I described organic molecules bonding to form larger and more complex chemical constructions. When the beams of a bathyscape pick out the inhabitants of the ocean floor in the abyss, a remote world far beyond the reach of any daylight, one of the organisms that does not run away is the glass sponge. They are perforated bags, tethered to the sea floor, and are so called because their spicular skeleton is siliceous, like glass, but spun into a tracery so delicate and subtle that no glass blower could ever imitate it. Many of the spicules are six-rayed. Sponges have chambers within their bodies through which seawater passes, and where any edible particles are removed. The walls of the chambers are lined with cells carrying whip-like flagella, which, as the name implies, beat to encourage currents into the chambers. Individually, these cells look very like free-living protist species, and the sponge is rather a loose association of such cells—forming a kind of proto-tissue. Some sponges will even re-assemble themselves if they are mangled up into tiny pieces. It is scarcely a matter of wonder to find these lowly patchworks of cells among the earliest fossils—but their endurance to the present day is remarkable, not least because you can scarcely distinguish a spicule plucked from a Hyalonema caught in a bathyscape’s lights from a specimen dissolved from a Cambrian rock. Like stromatolites, glass sponges have lived on in corners of the world which have endured with little change. The familiar bath sponge does not have siliceous spicules—it would be an agony to wash with if it did. It is composed instead of a tough organic material, spongin. The prodigious capacity of the internal chambers to hold water has bred the metaphor which links sponges with freeloading, which is rather unfair: they are certainly not parasites.* Worms, toads and dogs have been employed in a similarly derogatory fashion, and so far as I know the first two lead exemplary lives (with the possible exception of the bloated cane toad, although even that creature has its enthusiasts); dogs are no more ignoble than their masters. I notice that in current genre movies the bad guys are cursed with the ultimate insult: “You … slime!” It will be recalled that slime had a crucial part to play in the stabilization of bacterial mats, without which this book would have been very brief. I can only conclude that insults are proportional to the position of the organism on the evolutionary ladder, and have nothing to do with its virtues or failings. The game is given away by the great division between animals with backbones and those without—for who wants to be described as “spineless”?
Among the earliest Cambrian small shells there were a number that were certainly not a mere scrap of something larger. There are several kinds of diminutive molluscs, distant relatives of living snails and clams and slugs. Some of these almost certainly grazed the algae which formed mats, and are implicated in the decline of that quintessentially Precambrian community. There were the earliest brachiopods, another kind of animal enclosed in two shells, which we shall discover again among the rich marine life in ensuing periods of geological time. Brachiopods filtered out small organic particles from the seawater. In Australia there may be the earliest corals, which did likewise.
Just a little bit higher again in the rock sections in Newfoundland, China, Siberia, Morocco, Australia—and many other places—the small shells are succeeded by an even greater variety of larger, skeletized organisms. Most prominent among these are the trilobites. These are arthropods, animals with jointed legs. Spiders, flies, fleas, crabs (both kinds), mites, beetles without end—indeed, almost everything that crawls, stings or scares is an arthropod. They are not exactly primitive organisms in comparison with most of those mentioned previously. They have a fully developed nervous system, a brain of sorts, eyes, limbs, gills, antennae, and some of them hunted. Trilobites are my family. They probably adopted me long before I went to Spitsbergen, when, as a lad armed with optimism and a coal hammer, I tapped along Welsh cliffs and riverbanks in their pursuit.
The three divisions that give these animals their name divide their hard, calcite carapace lengthways into a prominent axis which housed guts and brain, flanked on both sides by flatter lobes. There is a semicircular head region equipped with eyes, which often have a crescentic outline, and backwardly directed spines at its lateral corners. Behind the head a thorax includes a number of articulated segments, thus lending the body a certain flexibility. It is this flexible thorax that gives the trilobites their superficial resemblance to woodlice (also known as slaters, or pillbugs, according to where you were raised). At the hind end there is a tail, often a shield somewhat like the head, which in some species is large, but in primitive species is usually very small. The carapace is composed of calcium carbonate, like those of clams and brachiopods. It is this shell which guarantees the trilobites such an excellent fossil record. For many years they were thought to be the only Cambrian arthropods. In any case they are far and away the most common as fossils, and the shallow Cambrian seas must have been fairly swarming with them. The sad fact is that some of the most important parts of the anatomy of trilobites are hardly ever preserved. These are the limbs, which the overlying calcite carapace served to screen from harm. The limbs themselves were not covered with calcium carbonate, and hence left little that could be routinely preserved in the rocks. Rarely, though, they are found as fossil impressions, and these show that trilobites had many pairs of legs, a pair to each segment, as well as antennae at the front. The limbs are themselves further divided into many small segments, often with bristles between them. If you pick up a small leg of a lobster you can see just the same arrangement of bristles close to joints, which serve to detect movement, and sometimes also to “smell,” because some of the hairs are tipped by sensitive little organs. So if you had scooped up a trilobite in your hand—and some of them would have been sluggish enough to catch easily—you could have turned it on to its back and watched the limbs scrabbling desperately to gain a purchase and scuttle away back into the sea. The eyes were unique, as well as being the oldest visual systems known. They resembled those of flies or lobsters in being compound—that is, composed of many lenses (I have counted up to 3,000 in a single eye). But they were unique in that each lens was a calcite rod. The stuff of common or garden limestone was used to see with—its hardness and durability permitted the preservation of these early eyes. The optical mechanism was not complicated. Each lens was carefully orientated in such a way that one particular crystallographic axis ran along its length. Calcite is a rather complex mineral, but its transparent crystals have this one preferred axis along which light passes in straight lines, unrefracted. Thus, calcite lenses “see” in the direction of their long axes—hence it is possible to reconstruct the fields of view of animals dead for 500 million years or more, the most literal way of seeing into the past. The image produced by the eye was a kind of mosaic.
In his book Supernature Lyall Watson regarded the trilobite eye as too sophisticated for its age, a precocious structure in advance of its appropriate use. On the contrary, it is as clear as calcite that the eyes were needed: acuteness of vision was necessary either for seeing the approach of hunters or to pursue prey. The tracks of Cambrian trilobites have been seen converging upon a worm trail—and only the trilobite emerges after the engagement. It was certainly not the worm that was doing the hunting. It seems that even one geological second after the appearance of Cambrian skeletons there also arose something recognizably like a modern marine ecology, with hunters and hunted, grazers and filterers. Stefan Bengtson has even recognized what look like the borings of predators into the very first shells belonging to Cloudina. Far from being a precocious luxury, the trilobite eye was a piece of equipment necessary to cope with a hostile world. Thus it was that the world of Ediacara and the Precambrian passed away, and another great step across a threshold in the history of life was taken, never to be retraced. Cellularity had become a food chain, gobbling began, and voracity has never gone away. If there were a point in history at which Tennyson’s famous phrase “Nature, red in tooth and claw” could be said first to apply, this was it, not the age of the dinosaurs—still less that of mammals. Perhaps the first predation happened as the result of an erstwhile cooperation that went awry: the biographical details are not recorded. The era of photosynthetic passivity and peaceful coexistence among bacteria and algae had passed from the Earth, and the hierarchy of power has never subsequently been forgotten.
It would be misleading to claim that the appearance of mineralized skeletons was the crucial event which reconstructed the living world; for this is only part of the story, although an important part. After all, most marine animals do not have hard skeletons, even today, and these creatures are just as important in the ecology as those that do. In a few places there are special geological sites where we get a fuller insight into what was living in the Cambrian. These are places where shells are accompanied by impressions of soft-bodied animals, often preserved in miraculous detail. Dolf Seilacher called these special rock beds Konservat Lagerstätten, a pompous-sounding term which has none the less passed into general scientific usage. And the most famous of these is without doubt the Burgess Shale.
High in the Canadian Rockies of British Columbia, in the Yoho National Park on the flanks of Mount Stephen, there is a small excavation on a steep hillside. A modest apron of spoil reveals the quarrying activities of several generations of palaeontologists. It is a hard march uphill all the way from the town of Field, and it is cold until well into summer, and frequently inhospitable even then. The site was first made famous in the late nineteenth and early twentieth century by Charles Doolittle Walcott, a man with as inappropriate a middle name as could be devised. Walcott did almost everything. He described Cambrian fossils from all around the world, including China (if placed side by side his books must stretch to a yard of shelf space); he was a considerable administrator; and he discovered the Burgess Shale. The apocryphal tale has it that his mule lost a shoe at the critical spot, but he was already prospecting these mountains for their ancient, middle Cambrian spoils, so any intervention by serendipity was mediated by design. Walcott noticed something glistening on the surface of a black slab of shale; only when the light struck the bedding surface from a particular direction did the remarkable fossils display themselves. They are revealed as flattened, silvery films, which glisten momentarily when the light is exactly right—otherwise they are dark black on slightly lighter black, and very hard to see. Walcott was quick to appreciate the importance of what he had found, which was nothing less than a completely preserved biota of larger organisms from the Cambrian. The animals had been buried so fast in their entombing sediment that their soft tissues had, for once, escaped decay. He traced the mother lode up the hillside, which is how the quarry came to be opened. Hundreds and hundreds of specimens were later collected, and stored in the US National Museum in Washington, DC. Walcott thought the world might be sceptical of the reality of his astounding discovery, and as a precaution he sent batches of specimens to other museums around the world so that the curators there, too, could be dumbfounded. He could spare a few specimens, because some of the species were not at all rare. When I made a visit to the site (which is now rigorously protected) I was able to find specimens of Walcott’s delicate “lace crab” Marrella* after a few minutes’ searching among the slabs lying on the slopes. Clearly, they were common enough to throw away.
The black shales preserved all the limbs and the delicate antennae of a trilobite, Olenoides. It preserved sponges and seaweeds and brachiopods and jellyfish. It preserved one Charnia-like survivor from the Ediacaran days. It preserved an array of worm-like animals, some of them readily recognized as belonging to living groups like annelids and priapulids, but also others which were much more puzzling, and possibly allied to the early Cambrian Halkieria. It preserved at least one animal much like the laboratory Amphioxus, a creature which used to be dissected by biology students seeking to learn the rudiments of organization in animals with a dorsal nerve cord like our own; from an anthropocentric viewpoint this little Pikaia might be the most significant animal of them all. But most spectacularly it preserved arthropods—the jointed-legged animals of which trilobites had once been regarded as almost the sole Cambrian exemplars. How wrong that idea was. For on the dark shales there was a fishmonger’s slabful of arthropods: big ones and small ones, blind ones and sighted ones, some with grasping claws, others with spiny legs, twenty-six or more different kinds. Of these, Marrella, a dainty, feathery creature with no real carapace, was much the commonest—but it was known from nowhere else. The sea must have teemed with these little swimming creatures of which there was no hint from other rocks. Finally, there were bizarre enigmas, animals which seemed to resist classification in any of the biological filing cabinets into which zoologists were accustomed to tuck away the animals they recognized. The very names of these animals spoke of arcane mysteries unsolved: Hallucigenia and Anomalocaris. How would these perverse and paradoxical Cambrian curiosities fit into the story of life? Anomalocaris was a large predator the size of a lobster with two great, spiny leading arms and a mouth surrounded by an apparently unique circlet of plates. As for Hallucigenia, it seemed to be a gut topped by wiggly tubes propped up on spikes. Had Edward Lear seen it he might have considered that it needed no embellishment; it was quite nonsensical enough as it was. A true glimpse into the Cambrian seas permitted an appreciation of how partial was the view from skeletons alone; how much richer the world had been, and how much less predictable.
The modern study of the Burgess Shale was led by Professor Whittington, who held Marr’s position as Woodwardian Professor at Cambridge University during the 1970s. It was Harry Whittington who made the first identifications of the Ordovician trilobites from Spitsbergen, observations which were instrumental in determining my own future. He described a number of the Burgess animals, in the most painstaking way, and guided the research students who studied Anomalocaris and Hallucigenia and the varied coterie of Burgess Shale arthropods. He and his students prepared an inventory of Cambrian anatomy which was like having a dredge plunge down into the hidden seas of 520 million years ago. Teasing details out with a pin by gently flaking off little pieces of the covering rock, preparing drawings of every limb under a camera lucida, testing reconstructions until they made sense in three dimensions—this is slow and laborious work. But it meant that Burgess animals are now known nearly as well as animals dredged from the deeps only yesterday.
What did these animals contribute to our understanding of evolution? What was their place in the story of life? Lying so close to the beginnings of the record of complex animals they almost certainly hold some special message, if only we could read it. Harry Whittington had noticed how curious the Burgess arthropods were. They did not seem to him to display the kind of anatomy appropriate to ancestors of living arthropods—they were altogether too peculiar. His natural caution made him reluctant to interpret more than one or two as close relatives of anything more familiar. Gradually, an idea took root in the 1980s that perhaps the Burgess Shale revealed not ancestors (as Walcott may have believed), but designs long vanished from the world. The reconstructions of the remarkable animals Hallucigenia and Anomalocaris seemed to set the seal on this speculation. These animals did not look like anything figured in zoology textbooks.
The greatest division of animal life is into different phyla (singular phylum): Mollusca are one phylum, arthropods another, jellyfish and allies another, brachiopods another, and so on. The record of nearly all these phyla begins with dramatic suddenness at or near the base of the Cambrian, like a curtain suddenly being pulled aside to reveal a drama in the middle of the first act. Perhaps, so the speculation went, in the Cambrian there were dramas undreamed of, phyla uncharted, a richness beyond compare. Hallucigenia must be one of these vanished designs, Anomalocaris another; several other Burgess creatures were lined up for the honour of being experiments in life that failed. There is something romantic in the notion of a “lost world” of strange creatures shuffling over the sea floor. Some, possibly favoured by no more than good luck, would survive and prosper to populate the hundreds of millions of years that followed. Others, the unlucky ones, survive only as misty shadows on the surface of shale slabs prised from a Canadian mountainside, and, but for the chance stumble of Walcott’s mule, might have remained unknown for ever, unrecorded might-have-beens. One thinks of Thomas Gray’s rumination on obscurity in Elegy in a Country Churchyard: “Some mute inglorious Milton here may rest.” Mute and obscure indeed were these mysterious fossils. How could they be made to speak of their identity?
At this point Stephen Jay Gould entered the Cambrian charivari. In 1989 he published a book explaining the Burgess Shale to the world. Wonderful Life became a bestseller and did much to promulgate the excitement of investigating the past. It also broadcast the notion of an unparalleled variety of body designs in the Cambrian: his narrative took the former students of Harry Whittington, Derek Briggs and Simon Conway Morris as the heroes in a detective story, the dénouement being nothing less than a new picture of the tree of life. The Burgess fossils, as he deciphered them, meant that this most familiar metaphor of descent should be turned upside down: the tree of life had been viewed in the past as a kind of bush that branched ever outwards and upwards. Now that tree could be inverted. In order to retain the comfortable arboreal comparison the image of a Christmas tree was substituted—a tree wider at the base and thinning upwards. More designs had been present in the early days near the base of the tree. The sudden bushing-out above the “trunk” of common descent portrayed the evolutionary explosion at the base of the Cambrian into a panoply of unrivalled variety. Subsequent history has involved a thinning of this early wealth of designs, so that only a handful continued to evolve to populate the world as it is today. If it were possible to replay history, chance alone would have “weeded out” a different set of animals, and the living world would be utterly different today. The course of life was not inevitable. If one of the silvery streaks on a Burgess slab had not failed, its history would have been neither mute, nor inglorious. It is an idea that is easily grasped and readily explained, and was championed in virtuoso style by Gould.
The idea of replaying life stories was rehearsed in Frank Capra’s 1946 movie It’s a Wonderful Life, which gave Gould his title. A short story by Ray Bradbury—not mentioned by Gould—provides an exact illustration of his case. The story described how marksmen of the future return to the geological past to hunt dinosaurs. These trophy hunters are strictly forbidden to disturb history and so rules are fixed such that only moribund dinosaurs may be killed; in this way nothing will interfere with the subsequent unravelling of history. But one member of the shooting party steps off the protective walkway and treads on an insect. When they return to their present time the hunting party is met by a race of giant ants.…
If palaeontology has a priesthood, then Steve Gould is the pontiff. The Burgess Shale, however, was one case where he has, I think, been fallible. The excitement of the ideas being promulgated was so seductive that he simply passed over the real evidence presented by the Burgess fossils. This in no way diminishes their importance. Part of his misinterpretation was the result of following those researchers who took Whittington’s doubts about the relationships of the more curious animals and inflated them into claims about hitherto unknown animal phyla, complete with appropriately mysterious names. More thorough examination showed that they were less radically different in organization than an initial appraisal had suggested. Hallucigenia—the typical example of a “weird wonder”—turned out to have been interpreted upside down! The wiggly organs on its back proved to be, somewhat more prosaically, mere legs; a second set of legs was discovered when the fossil was appropriately excavated, and the animal was rapidly reinterpreted as a stumpy-legged creature with spikes on its back. Some other discoveries from China made in the late 1980s showed that animals of this kind were widespread in the Cambrian, and were probably related to a curious group of living stumpy-legged animals, the velvet worms (Onychophora), which now survive under rotting logs in many places in the southern hemisphere. These primitive animals had long been regarded as occupying a lowly place in the hierarchy of life; indeed, many writers had indicated that they might represent a kind of proto-arthropodan organization—just the kind of bug, in fact, that you might have expected to discover crawling around in the Cambrian seas. It is now becoming clearer that the velvet worms were much more varied and diverse in the Cambrian—they had more designs and were more disparate then than they are today. Spiky forms no longer survive, for example. This was no different from a discovery that Simon Conway Morris had made in 1980 about another obscure group of living “worms,” the priapulids, which were much more varied in the Burgess Shale than in our seas now. This is an important and exciting finding: we could no more predict what kinds of velvet worms were living in the Cambrian than we could infer the shapes of dinosaurs from thought alone. Only the fossils could chart the story. Hallucigenia was no hallucination, but rather a vision. So, too, with Anomalocaris. To those like myself who had studied arthropods its grasping arms always spoke of that great, versatile ragbag of jointed-legged designs. It now seems that they, too, were widespread. Anomalocarids have been found on Kangaroo Island in South Australia, in early Cambrian rocks—even older than the Burgess Shale. Their compound eyes and limb forms make more sense as an arthropod than anything else, but one that was already highly specialized as a hunter (6 FOOT SHRIMP RULED ANCIENT WORLD, as one of the tabloids put it). One could not have predicted Anomalocaris’ existence, of course, without the wonderful insights provided by special fossil preservations, but no purpose is served by assigning it to a phylum unknown. One may still marvel at the fecundity of nature without making wild assertions about every fossil belonging to a different world.
Many of the other arthropods, too, seemed less strange when they were interpreted through what they shared with other, known arthropods, rather than being celebrated only for their peculiarities. None was as strange as a present-day barnacle, nor as grotesque as a queen termite. To be sure, there remain many problematic animals, but their problems seem more to do with how they are assembled than with doubts about common ancestry. The jointed limbs of arthropods are arranged in different ways, often having different functions, rather like an articulated tool kit. Some have grasping claws, others fine hairs for grooming, others again spines for filtering. It is no coincidence that some of our attempts at mechanical robots clank around on spindly legs, with different arms for different jobs. Exactly how the tools are kitted out and in what order they were assembled is what understanding these Cambrian animals is truly about. In the process of early animal evolution, many viable, but to our eyes odd-looking creatures came into being and thrived. We need to know about these animals in order to gain some idea of the richness of the history of life. It remains true that if—but what a big if (to re-use Darwin’s phrase about life’s genesis)—one rather than another of these animals had survived, then the subsequent course of history would have been different: the consequences of an early branch would have been a different tree, ultimately in a different forest. If there was ever a claim that evolutionary history would slavishly replay itself if it could somehow be restarted, I have never come across it. No doubt crucial crossroads were decided on a turn of chance. And no doubt a different turn would have had quite different consequences.
These somewhat arcane arguments are of crucial importance. Any history of life is torn between portraying the narrative of successive species as orderly, almost a logical progression, and as something trawled from mighty disorder and upheaval from which chance alone plucks survivors. There is no question of the rapidity of the change we see at the base of the Cambrian. It was a time when animals could be constructed in ways unknown before or since, perhaps because their genetics were more flexible than at any other time in history. But many Cambrian animals actually do make more sense in the light both of what came after them and of what is still alive today, particularly when compared with the puzzling Ediacara animals. Despite the claims of the “new phylum” enthusiasts (one book claims at least 100 Cambrian phyla which did not survive) there are relatively few Cambrian designs which are wholly unfamiliar to us. Many, like Hallucigenia, elaborate in unexpected and inventive ways upon a ground plan which we already know, rather like improvisations upon an underlying musical theme that we can only recognize if we listen very carefully.
The “English Mozart,” George Frederick Pinto, was born in Lambeth, London, in 1786. Samuel Wesley said of him: “Greater musical Genius has not been known … England would have had the honour of producing a second Mozart.” Like Wolfgang Amadeus he had astonishing natural ability. As was the fashion among prodigies, he had already performed brilliantly in public by the time he was eleven years old, and over the next few years he composed piano and violin sonatas of remarkable maturity. His songs have been likened to those of the young Schubert. He was celebrated by his contemporaries, who had every expectation of his future greatness. Sadly, he was to disappoint those expectations, for he died before his twenty-second birthday. He has become a peripheral figure in musical history, neither mute nor inglorious, to be sure, but none the less a might-have-been. The historian can only speculate about the course musical development might have taken had Pinto lived longer, but one cannot say that because his potential was that of a Mozart, his place in history deserves to be the same. Mozart’s stature is the result of what he did rather than of what he was. Our judgement is inevitably coloured by historical perspective—how can it be otherwise? But, equally, we should recognize that those who listened in awe to the “English Mozart” as the eighteenth century drew to a close were not mistaken when they surmised a glorious future for the handsome prodigy playing the piano so brilliantly. But for the attentions of a cruel bacterium it could well have been so. Heard again today, Pinto’s brief contribution fits into the context of the music of its time, just as Mozart’s followed from Joseph Haydn’s example. Poor Pinto might be compared with a Cambrian animal that was destined to produce just a handful of descendants: it could well have been many more, but for a brief stroke of fate. While chance—mere random luck—may have picked off this animal rather than that one, there was also a kind of orderliness, because each animal was adapted after its own lights to life in the Cambrian sea, just as music belongs recognizably to its age regardless of the individuality of the genius who wrote it.
With predators like Anomalocaris swimming around (to say nothing of old-fashioned jellyfish) there was no room for limping, maladapted and vulnerable morsels even at this early stage in metazoan history. But crawling over the Cambrian muds there were also creatures which fill in for us some of the gaps between groups of animals that later seem widely separated. These are hybrids between trilobites and crustaceans, between clams and snails, not so much a gallery of missing links as a pot-pourri testifying to common ancestry, survivors of a mutable age. The later weeding-out of early forms served incidentally to separate the surviving animals more distinctly, but, in the Cambrian, categories were still blurred. There was no question of Lear-like chimeras spanning plant and animal, but there were mixed-up molluscs and ambiguous arthropods. The velvet worms alive now, like Peripatus, are all terrestrial animals, but Aysheaia, which included their Cambrian relatives, were marine animals equipped with gills. You would expect a marine relative of a Peripatus to have gills. Whittington’s uncertainty about how to classify these animals came about not merely because of their strangeness, but because of their ambiguity, their previously unknown assembly of characteristics. Gould’s mistake was to accord them a status they did not deserve because of these same novel combinations of features. The importance of the Cambrian fossils is not as a pot-pourri of zoological strangeness but rather as a key to understanding the state of the animal world close to its birth. There could hardly be a more important insight.
I have dwelt upon this question of the Cambrian evolutionary “explosion” because it is probably the most significant threshold to be crossed since the first organic molecules joined together to polymerize the first molecular chains. This is where leisureliness disappeared from our story. The animals that evolved in the Cambrian would have crawled over one another to be first to mate, evading the attention of predators on the way. Competition was introduced into ecology: these animals led exciting lives, vying with one another, sculpted for fitness. By contrast, the mat-formers which populated the endless stretches of Precambrian time, and even the Ediacara fauna, may have led lives almost devoid of incident. When this changed, it changed for ever. Indeed, competitiveness still governs all biological life: “Getting and spending, we lay waste our powers.” And all getting is at some other creature’s expense.
As to the different interpretations of the meaning of the Cambrian fossils, they furnish an object lesson in the relativity of truth. Flann O’Brien, one of the greatest Irish writers of the twentieth century, created a natural philosopher, De Selby, who elaborated alternative theories of an atomic nature. He proposed, for example, that darkness was not, as convention has it, an absence of light, but in reality a progressive accumulation of coal-black particles, so that night fell by a kind of blizzard of accreted blackness. As almost everything can be described as particulate in modern physics, De Selby’s conceit in turning a mirror on to light and dark has a certain attractiveness. Such philosophical ambiguity is appropriate to the question of the meaning of Cambrian animal designs, which can be regarded as strangely unfamiliar or strangely familiar, according to the way in which they are considered. It all depends what you mean by familiarity and oddity.
There remain several Cambrian animals which have defied all attempts to relate them to something more familiar. For example, Opabinia from the Burgess Shale had a number of eyes, and peculiar appendages; some of the animals which carried plates all over were neither sponge nor worm, and may, possibly, represent a large group of organisms of which there is no known close relative. But there is no question that the uniqueness of the Cambrian designs has been exaggerated by those with eyes for novelty rather than commonality of descent. To be sure, the Cambrian was a peculiar world, but a recognizable one for all that. There were as many links as enigmas.
There are a few palaeontologists who are as eccentric as Opabinia, and one wishes there were more. Usually, eccentricity is within the bounds of academic variation (quite a generous allowance, admittedly)—absent-mindedness, odd expressions or manners of speech, tramp-like garments worn for decades, etc. etc. There are a few who transcend such mundane bounds to become legendary figures. Dr. Rousseau H. Flower was an eccentric in the grand manner. He was an authority on nautiloids—the living pearly nautilus is the last representative of a formerly diverse group of marine animals distantly related to the octopus, whose straight or coiled shells are often found in rocks of Ordovician and younger age. From the 1960s until the 1980s he lived in New Mexico, although he came originally from New York. Possibly as a consequence of his removal he became more western than the westerners. He always wore hand-tooled cowboy boots with elaborate curlicues in the stitching, and a hat and jacket to match. He was very short-sighted, and tended to stumble along in the purposeful way adopted by the cartoon character Mr. Magoo, while mumbling vigorously to himself. When some particularly appealing idea occurred to him he would stop and cry out “aha!” with a kind of surprised enthusiasm, as if he had just recognized an old and valued friend. In the field he carried a bull-whip, and was known to lash outcrops that refused to yield up their share of nautiloids. He was even said to try the same trick with a six-shooter, but his approximate aim reduced bystanders to gibbering terror. He was an inveterate smoker, which was eventually to lead to the emphysema that killed him. When I shared a hotel room with him, I recall him emerging from the shower with a bent cigarette still clenched between his teeth, and dripping sadly on to the floor. Yet he was also a masterly cello player—indeed, he could play the Dvorák concerto, the Mount Everest of cello concert works. For all his eccentricity, Rousseau Flower led a productive and satisfactory life. Perhaps his example should be remembered as we contemplate the alleged eccentricities of animals long extinct, for they, too, would have been capable of living successfully on the sea floors of their own vanished worlds. Our own perceptions are schooled in what we know, and are not lightly converted to imagine life in the Cambrian or before.
There remains the question of timing. It is true that the biological world changed, and changed utterly, between Ediacara and the Cambrian. This is only about 15 million years, at the most, according to recent estimates from radiometric dates. The appearance of skeletons certainly happened over a shorter time-period again. There can be little doubt that one change followed upon another in a chain reaction, as the sequence of rocks in Newfoundland or Siberia relate with the simple clarity of a folk story. The first predators appeared, and with them protective skeletons in their victims; which prompted better predators, which in turn gave an advantage to animals with thicker shells, and so on and so on, in a kind of arms race. But we also know that soft-bodied animals proliferated as fossils or traces at exactly the same time: hence the Cambrian threshold was marked not just by the acquisition of shells, although that surely was a part of it. Now a whole array of animals like those of the Burgess Shale have been found among the earliest rocks of the Cambrian at Chengjiang, in China, and at Sirius Passet, in Greenland, so it seems that the differentiation of the designs of animals must have been even earlier, and its progeny more widespread. I recently examined a PhD thesis written about the Greenland arthropods. The author was convinced that there were a variety of Peripatus relatives which were variously in the process of transforming themselves into more familiar arthropods. And yet how can it be that all this variety arose apparently instantly at the base of the Cambrian? We know that some of these animals are more primitive than others, just as surely as we know that living Peripatus is more primitive than a living butterfly. In short, there must inevitably have been a history of descent which is not recorded along the windy shores of the Rock, or in the tundra along the banks of the Lena river in Siberia. Marrella and trilobites and Anomalocaris and all the rest must have had a prior common ancestry to account for what they share, as inevitably as we and the chimpanzee share a previous history because we can use our thumbs in a similar way. Wehere, then, were these ancestors? Why were they apparently invisible?
There seems only one way out of this paradox: the late Precambrian ancestors of the arthropods, molluscs and all the rest were very small—a few millimetres long at most. It was only when the “small shellies” acquired shells that they became visible. At the same time they became large enough to leave their footprints or their tracks and trails. Maybe some of the small animals lived as part of the plankton, where larvae of many groups of animals live today. Most of these are virtually invisible in the fossil record. Lest this seem like special pleading, it can be shown that even among living groups of animals the most primitive species are often very diminutive. The most primitive insects are tiny, wingless springtails, for example; there are curious, primitive little worm-like molluscs called aplacophorans; even shrews are both the smallest and possibly the most primitive of mammals. Small is not only beautiful, but often durable.
The explosion in Cambrian diversity of life may have been the result of an increase in size from small ancestors. Much of the hard, evolutionary groundwork may have happened in the late Precambrian. The apparently magical curtain that was drawn aside in the Cambrian to reveal a wealth of life displayed the point in the drama when the actors suddenly donned their costumes to become visible to the audience. The work backstage in the Precambrian, the rehearsals abandoned, the writing and rewriting, are forgotten in the sudden drama of illumination as the curtain rises. Maybe the costumes—shells, for example—appeared as a result of increase in size: after all, stature requires support. A tiny organism can be supported by its own turgor, and requires neither struts nor enclosure by hard shells. Shells do many things besides offer protection; they enclose a chamber for feeding; they allow for life inside sediments on the sea floor without choking vital parts; they provide privacy for housing the organs of sexual reproduction. All this may have come about as a by-product, a chance gift, after the appearance of shells for entirely different, protective reasons. As with the discovery of fermentation, with its intoxicating primary products, it was a bonus to find that wine also tasted good, and provided a drink immune from those poisonous bacteria that infect unsafe water. The latter properties could scarcely have been the prime mover for the original innovation, but the connoisseur would doubtless claim that taste was its most durable consequence, especially when he is well into the second bottle. These originally incidental advantages became the main reason for further development and sophistication as wines competed to tickle the palate, until the thousands of châteaux, vineyards, and haciendas we know today had come to fruition. It is always tempting to describe such changes in a thoroughly purposive way; in the Cambrian instance, it would be as if a shell was an advantage waiting for its moment in time, and the animal schemed to exploit its various properties. This is to confuse purpose with effect. But there is no question that novel interactions between animals, including competition and predation, prompted the explosive proliferation of life in the Cambrian, even if the generation of fundamentally different designs had happened in animals of small size over tens of millions of years previously. There was a chain reaction, unstoppable once started, a bacchanalia of zoological inventiveness, which has never been matched again. This is the point in my biography when those forces which are still supposed to energize human economies first made themselves felt in the economy of Nature itself.
The explanation that the level of oxygen had reached a critical level for the respiration of large animals has a pleasing continuity with the role of humble, inconspicuous photosynthesizers, which had transformed the atmosphere through the previous vast stretches of geological time—the slime time. Oxygen may have increased to a point where it was sufficient to supply a protective ozone layer high in the atmosphere, which served to shield vulnerable animal tissues from harmful solar radiation; shells may have offered additional protection, another unpredictable benefit of this innovation. But geologists have discovered evidence for several further interesting events that happened close to the base of the Cambrian. This was when seas advanced over the continents to leave a rich sedimentary record—in some parts of the world (as in many areas in Scandinavia) this sea flooded a landscape which was already ancient and eroded. In such areas there was no opportunity for any geological record of the critical interval of time until the sea had made its inroads. The diversification of life may have accompanied the flooding as continental shelves, rich in nutrients, became available to the new and larger fauna, literally a feast of opportunities waiting to be exploited.
Then there were changes in the quantity of that vital nutrient, phosphate, in the ancient oceans. My companion in Australian fieldwork, John Shergold, had become interested in the abundance of latest Precambrian and Cambrian phosphate deposits, which are commercially important as a source of fertilizer and industrial chemicals. He took me to the mine at Mount Isa, almost exactly in the middle of Australia. Like all open-cast mines it has a blatant obtrusiveness which sits ill in the surrounding landscape, a hole where none should be. There is always a temporary feel about mines, which is often justified by their busting soon after booming. But it became clear to me at once how the Cambrian sea had flooded over Precambrian Australia, bringing with it dark, shaly rocks black with little nodules of phosphate; the same seas teemed with tiny, swimming trilobites, which must have clouded the water in their abundance. This was no struggling ecology, poised on the brink of things; rather, this was a cornucopia of biological activity. Comparable Cambrian deposits are known around the world. Clearly something had stimulated the production of these phosphates, and John Shergold would like to link this curious phenomenon with the appearance of many phosphate-shelled animals at more or less the same time. Today, an abundant source of phosphate still produces bumper harvests in the sea; in places where seawater charged with dissolved phosphate wells up to the surface, as it does off the western coast of South America, for example, there are limpets as big as soup plates. The whole guano industry is founded upon phosphate excreted by millions of seabirds, and derived ultimately from the recycled deeps. Perhaps the Cambrian enrichment was powered by phosphate, catalysed and accelerated by a rejuvenated ocean circulation system. Others have sought to turn the same argument completely on its head, claiming that it was the breakthrough in deposition of minerals made by animals and plants at the end of the Proterozoic which served to trap more phosphate, which could then be readily preserved in the rock record. They point to the fact that most geologically younger phosphate deposits are closely associated with biological agents, as in the case of guano.
Momentous events in the history of life were evidently inextricably bound to events in the world, and vice versa. Life and environment comprise one linked system, they have an umbilical connection. It is impossible to talk about a breakthrough in the story of organisms without looking at what was happening in the seas around, or at how the continents were distributed and what this might have done to the circulation of wind and water. Life itself created the conditions under which further life could thrive, and thus began the complex interdependencies that are the stuff of ecology.
I can imagine standing upon a Cambrian shore in the evening, much as I stood on the shore at Spitsbergen and wondered about the biography of life for the first time. The sea lapping at my feet would look and feel much the same. Where the sea meets the land there is a patch of slightly sticky, rounded stromatolite pillows, survivors from the vast groves of the Precambrian. The wind is whistling across the red plains behind me, where nothing visible lives, and I can feel the sharp sting of wind-blown sand on the back of my legs. But in the muddy sand at my feet I can see worm casts, little curled wiggles that look familiar. I can see trails of dimpled impressions left by the scuttling of crustacean-like animals. On the strand line a whole range of shells glistens—washed up by the last storm, I suppose—some of them mother-of-pearl, others darkly shining, made of calcium phosphate. At the edge of the sea a dead sponge washes back and forth in the waves, tumbling over and over in the foam. There are heaps of seaweed, red and brown, and several stranded jellyfish, one, partly submerged, still feebly pulsing. Apart from the whistle of the breeze and the crash and suck of the breakers, it is completely silent, and nothing cries in the wind. I wade out into a rock pool. In the clear water I can see several creatures which could fit into the palm of my hand crawling or gliding very slowly along the bottom. Some of them carry an armour of plates on their backs. I can recognize a chiton, but others are unfamiliar. In the sand there are shy tube-worms. A trilobite the size of a crab has caught one of them and is shredding it with its limbs. Another one crawls across my foot, and I can feel the tickle of its numerous legs on my bare flesh—but wait, it is not a trilobite, but a different kind of arthropod with eyes on stalks at the front and delicate grasping “hands.” Now that I look out to sea I can see a swarm of similar arthropods sculling together in the bright surface water—and can that dark shape with glistening eyes be Anomalocaris in pursuit? Yes, for the top of its body briefly breaks the surface, and I can glimpse its fierce arms for an instant. Where the water breaks it shines luminously for a while in the dying light—the seawater must be full of light-producing plankton—and I have to imagine millions more microscopic organisms in the shimmering sea.
* The technical term for this phenomenon is “biomineralization.”
* A pedantic reader might insist that the sponge Cliona effectively is a parasite, since it bores into and weakens the shells of the clams it colonizes—often fatally.
* Walcott was clearly taking no chances. Marrella was named for Johnny Marr, the Woodwardian Professor at the University of Cambridge, the senior position in palaeontology in Britain. However, he named various other species from the Burgess Shale after his family, of which Sidneya inexpectans is the most charming.