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The Search for the Velvet Worm

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New Zealand is a country that beguiles but deceives, for much of it is dressed in false colours. Although there is still some almost untouched forest on the South Island, human hands have transformed much of New Zealand in the service of forestry and sheep.

The story of these islands is one of isolation. Their origins lie within the great and ancient vanished land of Gondwana, from a time when peninsular India, South America, Africa and Australia were united together as a ‘supercontinent’. Something like 100 million years ago the nascent New Zealand separated from its parent, as Gondwana began to fragment progressively into its individual plates. These eventually forged the continents of the southern hemisphere that we would recognise today. Unravelling this story was one of the great achievements of modern science, and it is linked to some of the stories of biological survivors in this book. New Zealand may be just a small part of that story, but its own narrative is geologically complex. To a kernel of old Gondwana rocks, newer rocks have been added piece by piece because the islands have sat in a tectonically active, though isolated zone for millions of years. Volcanoes have made their fiery contribution in ash and lava, other igneous rocks have been intruded into the Alpine range as it grew, and then sediments eroded from the young mountains completed a dynamic rock record. It could be said that the geography of New Zealand has been under constant revision. But animals and plants were also carried onwards into the growing New Zealand from the ancient Gondwana days, a persistent legacy of an old continent bequeathed to a future land. Sometimes the evolutionary signal of an organism betrays a far-distant past in surprising ways.

The ancient coniferous podocarp forests that once covered much of the North Island have all but disappeared. Little patches of it hang on almost by oversight. They are dark and mysterious within; silent, but for melodic tweets from birds high up in the canopy feeding on the little fruits the trees produce. Podocarps are southern hemisphere conifers of several species that make superb and stately trees if they are allowed centuries to grow to maturity. This is too long for a healthy profit. The original forests were felled for their good timber, but were replaced in many areas by quick-growing conifers such as Californian pines deriving from the other hemisphere. Huge areas of the North Island are covered with conifer plantations. Periodically they are felled en masse and then the rolling hills are scenes of devastation, with nothing green left standing but wrecks of stumps and unwanted branches in rough piles everywhere, and small fires smouldering as if shells had exploded not long before. When I drove through such an area I was torn between recollections of battle scenes from World War One, and J. R. R. Tolkien’s descriptions of the ghastly land of Mordor in The Lord of the Rings. I suppose the latter might be more appropriate, since splendid alpine New Zealand has been repeatedly used as the location for the movie version of Tolkien’s saga. The sheep country looks like steep sheep country everywhere, and reminded me of Wales and Scotland, even to the extent of carrying scrubby patches of brilliant yellow-flowered gorse – which, of course, is a troublesome introduction from Europe. There are so many other Europeans on these islands, not just Smiths and Joneses in suburban villas, but oaks, sycamores, elderberries, and implacable ivy. They compete for space with other native trees, including the New Zealand red beech, Nothofagus fusca, with its delightfully delicate little leaves and graceful habit. I could not help feeling that a coarse and unthinking hand has been at work, interfering with the landscape, scrubbing forests out, planting weeds. This is grossly unfair to the New Zealanders, the kindest people on earth.

Podocarp trees are in a sense ‘survivors’ from the time of Gondwana. These trees are found in Australia, New Caledonia, South America, and Sub-Saharan Africa – one or two genera are even in common between New Zealand and the Andes. Gondwana may have split into its separate pieces, but the identity tags of its former inhabitants were not redesigned so easily. These Gondwanan coniferous trees, with their relatively large leaves and bright berries, do have a very special appearance, at least to a European accustomed to pines and firs with their dry-looking cones. A botanist would remind me I should really describe the berries as ‘fleshy peduncles’ because they carry exposed seeds at their tips. On the wet west coast of the South Island near Karamea, I walk into a podocarp forest where dampness rules. Everything that could be is covered in moss, epiphytes or filmy ferns. They clothe the trunks and branches of trees in a creeping, delicate and close-fitting cloak of tiny green leaves. Inconspicuous orchids are there somewhere, perched on branches, sporting small yellowish flowers, the antithesis of tropical showiness. Where light breaks through the canopy, tree ferns erupt like green fountains perched on shaggy stems, adding ebullience to the primeval atmosphere. Little brown birds with bright little eyes – tom-tits New Zealanders call them – pipe tamely from exposed twigs hoping that these clodhopping visitors might disturb insects for their supper. Trunks of the podocarp totara tree soar upwards, while the rimu – the most elegant of its family, with weeping, cypress-like branches – breaks through the canopy like drapes. The wood of this tree is so hard that the heart is still sound for working from trunks lying on the ground years after the outer layers have rotted. The more familiar southern beeches (Nothofagus) are unsuitable for major construction since they rot from the inside out, but they also have a Gondwanan signature, following closely the pattern of the podocarps. I recall that Charles Darwin observed how the natives in Tierra del Fuego ate a curious fungus looking like a cluster of yellow golf balls that grew on southern beech branches. The fungus was named Cyttaria darwinii by Miles Joseph Berkeley, the great nineteenth-century mycologist who worked out the fungal cause of the Irish potato blight. Further species of the same fungus were discovered, but they only grew on southern beeches: fungi can be choosy. The Gondwana legacy even applies to soft, edible fungi that would never stand a chance of being preserved as fossils. Biologists must have their wits about them if they are to understand the complexity of the past.

New Zealand took away its package of Gondwanan plants as the continent broke up. Later, it was colonised by birds, and they evolved in isolation to produce a host of endemic species. Some are almost comical, like the kakapo, a ground parrot of remarkable stupidity (and now a threatened species), and the kea, a mountain parrot of legendary intelligence and a fondness for eating the windscreen wipers of cars exploring the Alps. It is said that keas can be found solving crossword puzzles left behind by tourists. Other birds became intimately involved with perpetuating the podocarp forest by swallowing and distributing their seeds. Some still remain, singing sweet songs high in the canopies of the stately stands that survive. Many scientists believe that at some stage in New Zealand history the sea level rose to a point where mammal species could not endure and breed. Today, it has no endemic terrestrial mammals. Whatever happened, nobody could question the fact that this antipodean island represents the acme of avian evolution in the absence of serious mammalian competitors. The loss of the ability to fly is common – why bother to take to the air when you can safely amble about in the bush? The kiwi is the amiable emblem of the country; a variety of kiwi species show the fecundity of this ground-dwelling option. None is safe for the future. The largest flightless bird that ever lived, the moa, lived in huge numbers in New Zealand. A Brobdingnagian ostrich, it was meat on legs for the first human invaders, who undoubtedly hastened its extinction.* In the Karamea forest I see the dark entrance to cave systems perforating Honeycomb Hill from which dozens of moa bones have been recovered, and marvel at a sudden vision of an island swarming with the giant birds. If only we could turn back the clock. So many New Zealand bird species are either extinct or threatened. The new generation of New Zealanders are almost neurotically aware of what human interference has done to the natural environment. The introduction of the possum from Australia was a particular disaster, since these aggressive vegetarians seem to particularly relish New Zealand tree flowers. They threaten the livelihoods of all the nectar sippers and honey eaters among the bird species. The restocking of offshore islands with native birds in a rat-free, possum-free and cat-free environment seems to be the best option at the moment. It is at best a despairing attempt to store away from further trouble a remarkable history running into millions of years.

I have to understand New Zealand’s long history before my search for an animal that has survived from a period even earlier than the first appearance of the horseshoe crabs. My quarry is the velvet worm. This creature will help us climb downwards to a still lower branch of the evolutionary tree. George Gibbs from the University of Wellington is my guide. He knows the secretive ways of these elusive animals. We drive out along Route 1, west of Wellington on the southern edge of the North Island, prior to walking up the Akatara Ridge along a small country track. The whole area was milled in the 1930s and 1940s so the mature podocarp forest has all gone, but there is secondary growth of tree ferns and rimu and Protea in a dense thicket. Some of the common native birds have adapted to the new circumstances. We hear the distinctive whistle and churr of the tui as we park the car. New Zealand birds usually have a distinctive and attractive song, even those that are unspectacular to look at. As we walk up the track I notice another survivor, the lowly herb Lycopodium, growing on the bank, a plant we shall meet again. It is a steady climb, though hardly taxing. Towards the top of the track the landscape opens out into gently rolling, wooded farmland. A scattering of cows and white sheep graze on the cleared, grassy hillsides, and dotted among them are Californian pines. The wind blows through the trees with a sound like the gentle crash of waves. The ‘old homestead’ proves to be an antique wooden building in the bottom of a small hollow surrounded by a circle of ageing pine trees. George locates the bleached remnants of rotten pine logs lying on the ground nearby. For some reason they had not been tidied away after felling, so they have had the opportunity slowly to break down in situ. Selecting one log, it soon becomes apparent that inside its pale exterior the decaying wood is rusty red and fibrous. George starts beating at it with a small mattock brought along especially for the purpose. I cannot help leaning expectantly over his shoulder. Each hack of the instrument beats away ten million years of geological time. Can the velvet worm be hiding inside this curious sarcophagus? Where is its time capsule?

But the first log yields nothing. A second log is soon under attack. It seems softer somehow, more decayed. As the wood splits easily apart tiny white termites are exposed to the air, looking something like pallid ants, almost transparently delicate. They move slowly, as if stunned by being exposed suddenly to bright light: they are creatures of habitual darkness. Their little antennae can be seen waving furiously. Termites are wood eaters hiding deep inside the log, living in chambers they make running along its ‘grain’. We had opened up their secret world. And then we see there’s something else, something caterpillar-like, hiding in the termites’ tunnels. It shrinks away as if it does not want to be seen, or as if light is somehow an embarrassment to it. George coaxes it expertly into full view: it’s the velvet worm!

This is the creature we had come all this way to find: Peripatus novae-zealandiae to give it its scientific name. Because it does not move very fast, it proves relatively easy to catch and bring out into the light. It is indeed about the size of a very large caterpillar, light brownish and with a stripe running down its back. I gingerly touch it and find it soft and giving – if hardly velvety. George soon finds a second worm hiding away inside the log, and then a third; they evidently do not mind one another’s company. They attempt to twist away from us in a most peculiar fashion: they seem to be capable of drastically changing their length. It looks as if they can stretch or squash like concertinas. They are highly flexible, too, and one of them turns into a tight ‘S’ shape with no trouble. ‘That’s not like a caterpillar’, I say to George. He grins back at me, sharing my pleasure in the discovery. They clearly have a front and a back, for at the forward end are a prominent pair of antennae – which lead the way the animals want to flee. Their movement is not worm-like at all, despite their name. It is accomplished by means of little conical stumpy legs on either side of the long body. On the hand these make an oddly prickly-tickly sensation. Velvet worms are clearly very odd invertebrates.

The Peripatus animals evidently live alongside the termites inside rotting pine logs; indeed, they feed on the little insects, pursuing them through the chambers inside, doubtless detecting them with their sensitive ‘feelers’. They trap their prey by means of a sticky slime produced in special glands. Nothing else in nature feeds in exactly the same way. One of George’s students proved that the slime only entraps termites of the right size – not too big to escape, not too small to be uneconomic – after all, slime is protein, and that is expensive for the creatures to make. I try out the feel of it; it is distinctly tacky, and it must be like glue to a termite. Both the velvet worm and the termites shun the sunlight with good reason. They lose water very rapidly through their thin ‘skins’. The velvet worm is little more than a bag of fluid surrounded by a membrane. In bright sun it would soon dry to a crisp. Inside the hermetic and lightless world of a decaying pine tree the relative humidity is nearly always 100 per cent and it is perfectly safe.

Poking about some more in the rotten wood we make another discovery: baby velvet worms. They are only about one centimetre long, and pale in colour, but they seem to be exact small versions of the large ones. I presume they must eat suitably diminutive termites. The worms grow continuously to achieve adult size, blowing up like balloons. The velvet worm actually gives birth to live young, and the ones we saw may have been newly born. This is unusual among invertebrates, and even among vertebrates is only characteristic of mammals (and a few specialised reptiles). The eggs of this particular velvet worm are few in number, and large and yolky, thus allowing for further embryonic development within the female; only three or four young are born at one time. There are two ‘litters’ a year. Since the animals live for three years they only have about twenty offspring, which is an extraordinarily small number when one remembers that most arthropods, for example, lay thousands of eggs: recall our horseshoe crabs. The most prolific velvet worm species produces no more than forty young a year. It seems that Peripatus is an animal with a personality all its own.

Looking a little more closely at the velvet worm, the first thing to notice is that the body seems to be made out of many rings that encircle the body, even the legs and antennae. They remind me of the Michelin Man, supreme advertising logo of the famous tyre company, all dressed up in his bands of rubber. It is this distinctive structure that accounts for the body’s elastic properties. Muscles circle the body cavity inside the skin. Then it is obvious that this is a segmented animal rather like a trilobite, with lots of similar units repeated along the length of the body. Each body segment carries a pair of those stumpy legs. Among living species of velvet worms the number of segments varies quite widely, but, biologically speaking, that is only a matter of tacking on extra identical units, and does not require massive tinkering at the genetic level. To prove this, there is even one velvet worm species that can have between twenty-nine and forty-three body segments. The short, stumpy legs propel the animal along by working in sequence in waves, a common feature among segmented animals. From the side, it looks as if one leg hands on a motion to its neighbour progressively in a common direction. Forward movement would obviously not be possible if legs pushed forwards entirely at random; cooperation is required. The legs remind me of the limbs of a child’s stuffed toy, rather like those belonging to Piglet as illustrated by E. H. Shepard in The House at Pooh Corner, but they work well enough to catch up with termites. After all, one does not need a Maserati to overtake a donkey. Looking more closely at the surface of the ‘skin’ each of the body rings carries a line of protuberances, giving the external surface a knobbly appearance, especially on its upper side – these are known as papillae (they may have even smaller secondary papillae upon them). The patterns of the papillae vary between velvet worm species, as does the overall colour. There is one magnificently blue species elsewhere in New Zealand.

The head of Peripatus is most obviously identified by its pair of antennae. But close to the front on the underside is the mouth, which is provided with sickle-like jaws to either side, each equipped with a pair of blades at the tip that are produced by a local thickening of the skin, or cuticle. They are simple but efficient shredders. The ducts for the slime glands open at the side of the head. There are no eyes. As for the legs, they are little more than stumpy projections off the body equipped with muscles internally to swing them backwards and forwards. Their feet carry two sickle-shaped claws at their tips, which are much like the jaws in structure; this may indeed provide a clue to the evolutionary origins of the more specialised jaw. Males and females are similar, except that the former are usually a little smaller and are less common.

Inside they are pretty simple, too. The major part of the body is taken up with the stomach, which runs along the length of the animal to the anus at the end. Between the gut and the mouth there is a short oesophagus and a muscular pharynx, which is used for initial food processing. Oxygen absorption is achieved through tiny tubes inside the body called tracheae that have their apertures located in depressions between the papillae. There are no special gills or lungs because animals of this size can get all the oxygen they need through thinned parts of the cuticle. The heart is another simple tube, positioned at the top of the body above the stomach. The rest of the vascular system is much as in the horseshoe crab Limulus, distributed rather diffusely through the internal cavity. Peripatus gets rid of its waste products by means of nephridia, kidney-like organs, located in the legs along with small excretory openings. The nerve cord is a double structure running along most of the length of the animal, with cross connections that make it look somewhat like a ladder: nerves extend from this into the segments and limbs. A larger ganglion in the head is all that this basic creature can display as a brain.

Simple though it may be, the velvet worm functions perfectly well. For a moving animal, there is quite a short list of vital functions: sensory equipment to find a source of food and tools to help eat it; a method of locomotion; a way to breathe and distribute oxygen to internal organs; a system of waste disposal; a reliable way to propagate the species. Peripatus would be the kind of creature one might put together from a ‘how to make an animal’ kit, except that like almost everything else in nature it has some tricks all its own – its gluey trap, its ability to produce little peripati by live birth. It is a simple creature in many features, specialised in other subtle ways; but it is also another old timer, a messenger from the distant past.

Its more recent history is not very different from that of the podocarp trees. Peripatus and its relatives number about two hundred living species (placed together in Phylum Onychophora, informally known as ‘onychophorans’).* They also have a distribution over the areas that once formed Gondwana: Australia, New Zealand, South Africa, South America and Assam (India). There are also velvet worms in Irian Jaya and New Guinea, where it is very likely that further species still remain to be discovered in mountainous and inaccessible areas. All of them carry the long memory of the vanished supercontinent as they tramp their unadventurous way on their stubby legs. Velvet worms had once wandered over Gondwana but, like the podocarps and southern beeches, new species arose on the separate pieces of the progressively fragmented continent; for evolution does not stand still. I could have gone in search of the velvet worm in any one of these other regions. The New Zealand species I happened to pursue is particularly interesting because it has developed a relationship with a special kind of termite that is regarded as the most primitive of its kind (of the Family Kalotermitidae), among which most individuals finish up as flying insects. The other termites are noted for their extraordinary caste system, with specialist workers and soldiers that never change their roles. It seems possible that a whole primitive ecology was transferred to New Zealand when Gondwana broke up, and there it endured, virtually unchanged, encased in logs. But something did change. I found Peripatus inside a pine log belonging to a species that was not native to New Zealand, so at some recent date the velvet worm must have followed its termite prey into a new habitat. You can teach old worms new tricks.

Since the velvet worm has a body as soft as dough it is most unlikely to be preserved as a fossil. Shells and bones leave behind their hard evidence, but can we expect a shy, soft package of flesh to do the same? Even the Solnhofen Limestone fails to preserve a single fossil of a Peripatus. Fortunately, there is one example preserved in Cretaceous amber from Burma (Myanmar), perhaps 100 million years old, a contemporary of the dinosaurs. Amber preserves the most evanescent of creatures: flies, beetles, even mushrooms. This fossil species is very like the living Peripatus and there is no question that it lived in a similar fashion. It provides the proof that velvet worms of modern type were alive at the break-up of the Gondwana supercontinent – which is good to know although we might infer it anyway from their distribution today. But we want to go back much further than this, 200 million years earlier. A remarkably preserved impression from the Carboniferous called Helenodora tells us that in the swamps of the coal measures, distant relatives of the velvet worm – but still eminently recognisable – were wandering their deliberate way through the damp undergrowth. Their contemporaries at this stage in the evolution of life were inelegant amphibians and very early reptiles, accompanied by the first flying insects. The velvet worm was terrestrial then, just as it is now. It may even have developed its special slimy-gluey glands, although at this early date it must have fed on something other than termites: for these insects were not even a twinkle in the eye of evolution in the Carboniferous. The velvet worm is beginning to look at least as ancient as the horseshoe crab. The velvet worm likewise survived the great extinction at the end of the Permian, and then it slid through the major event that secured the removal of the dinosaurs from our planet; like Limulus’ ancestors, Peripatus is made of sterner stuff, not to be seen off by mere global catastrophes. But now there comes a surprise. When we go back yet another 200 million years all the way to the Cambrian Period, to the time of ‘explosive’ evolution at the beginning of complex animal life, there, too, were relatives of velvet worms – they prove to be more common as fossils in Cambrian rocks than they are in rocks laid down in later geological periods. They began their history under the sea, in the cradle of life, like everything else. And they proved to be survivors. They shared their early world with trilobites, and the first relatives of horseshoe crabs, and the distant ancestors of scorpions. So much in biology seems to converge back more than 500 million years ago to the Cambrian ancient sea floor. The ancestors of the velvet worms were yet another kind of animal that later moved onto land – and this happened at least 300 million years ago. Because of their rarity as fossils it is not possible to say whether velvet worms got onto land before or after scorpions; we shall probably never know. Unlike scorpions, they needed to stay in wet, or at least humid environments, but just like those venomous arachnids none of their close relatives managed to survive to the present day beneath the sea. For Peripatus and its relatives going on land was arriving at some sort of haven.

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.

Survivors: The Animals and Plants that Time has Left Behind

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