Survivors: The Animals and Plants that Time has Left Behind
Survivors: The Animals and Plants that Time has Left Behind
Richard Fortey
This ebook edition does not include illustrations.An awe-inspiring journey through the eons and across the globe, in search of visible traces of evolution in the living creatures which have survived from earlier times and whose stories speak to us of seminal events in the history of life.The history of life on Earth is far older – and far odder – than many of us realise. In ‘Survivors’, acclaimed author Richard Fortey traces this history not through fossil records, but in the living stories of organisms that have survived nearly unchanged for hundreds of millions of years and whose existence today affords us tantalising glimpses of landscapes long vanished.For evolution has not obliterated its tracks. Scattered across the globe, strange and marvellous plants and animals have survived virtually unchanged since life first began. They range from humble algal mats dating back almost two billion years to hardy musk oxen, which linger as the last vestiges of Ice Age fauna.Following in Fortey’s questing footsteps, ‘Survivors’ takes us on a fascinating journey to these ancient worlds. On a moonlit beach in Delaware where the horseshoe crab shuffles its way through a violent romance, we catch a glimpse of life 450 million years ago, shortly after it diversified on the ocean floor. Along a stretch of Australian coastline, we bear witness to the sights and sounds that would have greeted a Precambrian dawn. Finally, in the dense rainforests of New Zealand where the secretive velvet worm burrows into the rotting timber of the jungle floor, we marvel at a living fossil which has survived unchanged since before the dissolution of the Gondwana supercontinent.Written with Fortey’s customary sparkle and gusto, this wonderfully engrossing exploration of the world’s oldest flora and fauna brilliantly combines the best science writing about the origins of life with an explorer’s sense of adventure and a poet’s wonder at the natural world. Utterly compelling, eye-opening and awe-inspiring, this is a book for anyone with an interest in evolution, in nature, in the remarkable scope of geological time and our own modest interaction with it – in short, in life itself.
Survivors
The Animals and Plants That Time Has Left Behind
Richard Fortey
Dedication
To my sister, with love
Contents
Cover (#ulink_5fb87965-0f72-59fe-895a-79a47af07b06)
Title Page
Dedication
Prologue
Table of Geological Periods
1 Old Horseshoes
2 The Search for the Velvet Worm
3 Slimy Mounds
4 Life in Hot Water
5 An Inveterate Bunch
6 Greenery
7 Of Fishes and Hellbenders
8 Heat in the Blood
9 Islands, Ice
10 Survivors Against the Odds
Epilogue
Picture Section
Glossary
Picture Credits
Further Reading
Searchable Terms
Acknowledgements
Endpaper
Other Books by Richard Fortey
Copyright
About the Publisher
PROLOGUE
These anomalous forms may almost be called living fossils; they have endured to the present day, from having inhabited a confined area, and from having thus been exposed to less severe competition.
CHARLES DARWIN, The Origin of Species
Evolution has not obliterated its tracks as more advanced animals and plants have appeared through geological time. There are, scattered over the globe, organisms and ecologies which still survive from earlier times. These speak to us of seminal events in the history of life. They range from humble algal mats to hardy musk oxen that linger on in the tundra as last vestiges of the Ice Age. The history of life can be approached through the fossil record; a narrative of forms that have vanished from the earth. But it can also be understood through its survivors, the animals and plants that time has left behind. My intention is to visit these organisms in the field, to take the reader on a journey to the exotic, or even everyday, places where they live. There will be landscapes to evoke, boulders to turn over, seas to paddle in. I shall describe the animals and plants in their natural habitat, and explain why they are important in understanding pivotal points in evolutionary history. So it will be a journey through time, as well as around the globe.
I have always thought of myself as a naturalist first, and a palaeontologist second, although I cannot deny that I have spent most of my life looking at thoroughly dead creatures. This book is something of a departure for me, with the focus switched to living organisms that help reveal the tree of life (see endpapers). I will frequently return to considering fossils to show how my chosen creatures root back into ancient times. I have also broken my usual rules of narrative. The logical place to start is at the beginning, which in this case would mean with the oldest and most primitive organisms. Or I could start with the present and work backwards, as in Richard Dawkins’ The Ancestor’s Tale. Instead, I have opted to start somewhere in the middle. This is not perversity on my part. It seemed appropriate to start my exploration in a place, biologically speaking, that is familiar to me. The ancient horseshoe crabs of Delaware Bay were somehow fitting, not least on account of their trilobite connections. Amid all the concern about climate change and extinction, it is encouraging to begin with an organism whose populations can still be counted in their millions. From this starting point somewhere inside the great and spreading tree of life I can climb upwards to higher twigs if I wish, or maybe even delve downwards to find the trunk. Let us begin to explore.
TABLE OF GEOLOGICAL PERIODS
1
Old Horseshoes
Turn seawards off Route 1, Delaware, and a century rolls away. A small road soon leaves the commercial strip and the fast food joints behind, as it moves onto flat fields and marshland that still supports scattered, pretty villages lined with white-painted picket fences. This is how much of America’s east coast used to be. The Little Creek Inn is a grander building altogether: a large, foursquare, wooden Victorian farmstead on three floors with shutters at the windows and a fine portico, and inside all polished wood and turned banisters. In the spacious drawing room of the Inn, anticipation is buzzing. The hosts, Bob and Carol Thomas, are serving iced tea to a crew of enthusiasts all dedicated to travelling back much further in time than a mere century or so. This is the chance to come face to face with life as it was millions of years ago. Glenn Gauvry, the local expert, is waving around models of an ancient animal. A small TV crew is there to straighten out their facts before they get down to filming. Two young women biologists have travelled from Canada to see for themselves an event that only happens when the conditions are just right in late May. I am there with my notebook and a fluttering heart. All of us are impatient for darkness to fall.
Deep in the night along the shores of Delaware Bay the horseshoe crabs are stirring. The tide is now high and there is no moon. Darkness rules, but even in the feeble starlight the overwhelming flatness of the countryside can be made out, except along the rim of the bay where old sand dunes have built up a levee providing foundations for a scattering of wooden beach houses, which loom against the night sky. A path passes between them onto a sandy beach that stretches away into the darkness in a long gentle arc. The shoreline seems to heave with gentle movements.
First, I notice some very odd sounds. There is a general hollow clattering, a tapping and grinding sound, somewhat like that made by knocking coconut shells together (once used on the radio to imitate horses’ hooves) but altogether less rhythmic, and with a kind of underlying push. Then, as my eyes get used to the darkness, low shelly mounds the size of inverted colanders can be seen slowly pushing and jostling all along the shore and perhaps six metres up onto the sands. Their bumping and clambering together is the source of those tap-tapping percussive sounds. The flash of an infrared torch reveals more details. The head-shield of the horseshoe crab is domed upwards and carries a few weak spines; at its back end a hinge marks a jointed boundary with a second large plate, spiny at the edge, which can flap downwards; and beyond that again projects a stout triangular spike as long as the head, which can waggle up and down. Here at Kitt’s Hummock more crabs are gathered on the mud flats seaward of the sands waiting their turn: strange, green-black, slowly animated lumps. Further offshore again in the shallow seawater tail spikes project briefly above the gentle waves like raised radio antennae and are gone, showing where still more horseshoe crabs vie with one another to get their place on the sand. There are evidently thousands upon thousands of these large animals gathered together in some sort of compulsive collusion.
One horseshoe crab lies upturned on the sand. Its tail spike waggles feebly, quite unable to perform the task of turning the body back over again. Five pairs of legs twitch ineffectually in a vain attempt to achieve the same end. I find it impossible to resist the temptation to right the poor animal. It is easy to grasp it by the edges of the head-shield. Once righted again those spindly legs allow the crab to trundle slowly away. Its behaviour seems at once strangely determined, but also apparently random, like the slow progress of a confused old lady on a Zimmer frame.
Now I see that many of the largest crabs are digging in the sand, their limbs working away beneath the carapace. Some have become almost completely buried, and, although I can detect a kind of deep scrabbling from these animals, they do not seem to be worried by their self-inflicted interment. Other slightly smaller crabs crowd on top of the buried animals. The scrabblers are the females of the species burying their eggs in the sand, while the smaller ones on top are males, competing to fertilise the eggs with their sperm (milt). I realise that there is some kind of order to the apparent mayhem on the beach. A proportion of the horseshoe crabs are paired off, with the lighter male desperately hanging off the tail end of the female, having got a purchase by using his special claspers. However, this right of occupation does not deter other males from having a go at mounting the same burdened female. There is enough of a gap behind the head-shield for some of their interloping milt to have a chance. Much of the clinking noise is a consequence of tussles for dominance. So this gathering of crabs is really an orgy, and an orgy that runs for dozens of miles along the strand, all thickly bordered with scrabbling, lustful animals. As for the poor exhausted females, gravid and overprovided with mates, the moist sand stops their gills drying out, and they may eventually struggle back to the sea when the laying is done – although many do not. Bits and pieces of their carcasses litter the shore.
I have a better chance to scrutinise the horseshoe crabs closely during the day, although most of them have returned to the sea by sunrise. Coastal Delaware is a land of marshes, with gentle wetlands dominated by the reed, Phragmites, and the cries of wading birds always in the wind. The landscape reminds me of the East Anglian coast in England. Creeks wind their ways inland from the sea, and terminate in small picturesque harbours like Leipsic, where a few fishing boats are tied up to stout piers, with white-painted clapperboard houses landward of the stage. Sambo’s is a restaurant with a view of the creek, and well known for its edible crabs, which are consumed on simple tables covered with newspapers. Eating in Sambo’s is an audible experience with everybody bashing lunch out from shells. It is a place of crunching and squishing and little conversation. Some of the shucked piles are prodigious. There is nothing on the menu about horseshoe crabs. The nearby villages of no more than one or two streets include neat little houses dating back to the 1880s, which is ancient by American standards. Delaware car number plates bear the legend ‘The first state’, acknowledging the fact that it was the first to sign up to the Declaration of Independence. Like several other early American states, but unlike the majority, it is tiny. Nowadays, vehicles on the main roads shoot past; but a mile or two from the freeways little has changed from post-colonial days. I warmed to it immediately.
After the crustaceous lunch, a visit to Port Mahon shows a few stragglers still on the beach at midday, providing a chance to get close. A large female’s carapace is about 45 cm across. In the sunlight I can readily see that the creature has nearly semicircular eyes set to either side in the midst of the head-shield, topped by sharp spines, rather like the perky eyebrows I associate with clerics of a certain age. Under high magnification it would be apparent that the eyes are composed of many tiny lenses – they are what are known as compound eyes, similar to those of houseflies or bees. The whole animal is a dull pinkish-to greenish-grey colour, the kind of colour I used to get as a kid when I mixed all my powder paints together. The front of the head-shield is subtly bowed upwards about the middle. The tail (or telson) has a triangular cross section, and it makes a stoutly elegant termination to the animal. The middle part of the body is defined on its top surface as a kind of convex median lobe over about half its length: this is where the muscles that power the legs are lodged. The leading edge of the head-shield is thickened into a prominent marginal rim that is prolonged backwards into short spines; this part of the body needs to be strong to butt into the sands and mud that line the floor of Delaware Bay. On the shore there are several beached crabs lying on their backs, waving their legs at the sky. They bend almost double along their middle hinges, but their best efforts still fail to turn them over (it would be different under water). If they remained on their backs, greater black-backed gulls would soon come along to peck them to pieces. Before setting them aright, I have a chance to see how delicately each of the paired jointed limbs under the head-shield carries a set of pincers at its tip. I am reminded of the manual toolkit owned by the eponymous hero of the movie Edward Scissorhands. They are indeed picky little tools. Nearer the front end of the head-shield, where the carapace is doubled back from the top surface into a blunt point, a very delicate set of pincers at the centre of the animal and close to the mouth, looks just the thing to feed titbits towards the innards. The bases of the legs are really quite stout and equipped with blunt spines that face one another along the midline of the animal: they can be used like nutcrackers to crack shellfish if needs be. I begin to understand how these creatures can grab a living from the waters of Delaware Bay. Behind the legs are a few pairs of flattish flaps that cover up intricately folded book lungs. Like every marine animal the horseshoe crab needs to breathe dissolved oxygen, and as long as this breathing apparatus can be kept moist under its protective covers the crab can survive on land. Hence the female can endure her risky excursion to lay her eggs in the sand. The shore may be an unwelcoming nursery, but might still be preferable to a sea where every cubic metre holds a thousand twitching antennae sensing free food. It is time to turn our crab over to allow it to trundle away. It heaves itself along like a battered tank: slowly and undignified, as if to signal ‘I have survived endless battles, and survival is all’. As it performs its lurching exit to the sea, it leaves a track behind on the muddy sand surface. The paired imprints of the limbs are prominent; even the tips of the pincers leave their doubled marks. And the tail, dragged behind, leaves a groove between, as a child might scribe with a stick clumsily trailed across the strand.
Horseshoe crabs are not really crabs at all; indeed, they are only very distantly related to crabs in so far as both kinds of animals propel themselves through the sea on spindly jointed legs. Animals with useful appendages of this articulated kind are known as arthropods (from the Greek: jointed legs). They are classified together in Phylum Arthropoda, a vast animal group that includes all the living insects, as well as spiders, millipedes, and a host of marine ‘bugs’ of all kinds. Crabs are crustaceans, along with lobsters, shrimps, and woodlice (pillbug to some). Horseshoe crabs are no more crustaceans than are butterflies. They do not have the flexible antennae or ‘feelers’ adapted to sensing the environment that are a common property of Crustacea and insects: these delicate organs both feel and touch, and smell. Instead, in the horseshoe crab the head appendages are modified at the front into a pair of useful pincers, or chelicerae, which I had observed in my stranded animal lying on its back. The significance of this apparently small feature will become apparent. The scientific name of the horseshoe crab is Limulus polyphemus (I shall need to use scientific names throughout this book). By day the beach throngs with feeding wading birds: thousands of them skitter nervously away from human intruders in animated, piping, fluttering waves, always beyond reach. Like most waders, many of them are dressed in shades of brown and grey, but the different statures of several species are obvious even to an inexperienced birdwatcher. Small, short-billed sandpipers throng on short legs; slightly larger pale-bellied sanderlings dash along the water’s edge; taller, long-billed dowitchers elegantly stride among them. The iconic species for the area is the red knot, which has a dramatic cinnamon-coloured belly when in breeding plumage. All wader species – and there are many more in the crowd – are united in rapt attention along the shoreline, pecking and probing incessantly at the ground, like chickens fed in a yard on the best grain. They are undoing the work of all those heaving masses of horseshoe crabs the previous night, gorging on the green, millet-seed-sized eggs the female crabs sought to sequester beneath the sand. For the red knot the eggs provide vital refuelling, as this particular population started its migration near the tip of South America. By the time they arrive in Delaware Bay on their way to the Arctic the birds may have lost half their bodyweight and they are starving. The crab eggs must taste like the best caviar. The birds would not survive without those countless horseshoe crabs performing their spectacular mass mating ritual. These inelegant invertebrates are completely unaware of the gift they are providing to an animal many millions of years their evolutionary junior.
Birds always attract devotees, and naturalists’ concerns for the welfare of the red knot probably accounts in turn for their anxiety about the state of the horseshoe crab population. If that were to fail, then so would the long migration of the attractive waders. A recent census estimated that there could be as many as seventeen million horseshoe crabs in the Delaware Bay area, and that concerns about their decline may have been exaggerated. Since the horseshoe crab has a range that extends along the shore north to Maine and south to the Yucatán Peninsula in Mexico the population is assuredly larger still, although the densest concentration of individuals is probably where I saw the heaving multitudes at Kitt’s Hummock and Pickering Beach. Delaware Bay is also where the mature crabs grow largest at maturity. Since there has, indeed, been a decline in red knot numbers the cause must lie somewhere else in its complex migration story. The weakest link in an ecological chain is always the critical one.
It had always been a dream of mine to see throngs of jostling horseshoe crabs reach the climax of their life cycle. For more than three decades at the Natural History Museum in London I studied fossils of trilobites. This once important group of sea animals went extinct something like 260 million years ago, when the world was a very different place. Trilobites had once swarmed in all the ancient oceans, but now their remains have to be patiently collected by splitting open the rocks that have entombed their shelly remains. Like horseshoe crabs, trilobites are arthropods: animals with jointed legs and all the muscles and tendons tucked inside an exoskeleton. However, unlike horseshoe crabs, trilobites did not survive the mass extinctions that redesigned the biological face of our planet. It is astonishing to learn from unchallenged fossil evidence that relatives of Limulus were contemporaries of trilobites. That nocturnal scrimmage on the beach in Delaware might have happened many millions of years before; I might even have been listening to sounds that had been rehearsed in Palaeozoic times. There were relatives of the horseshoe crabs in the sea long before other arthropods, such as insects and spiders, had ventured onto land, or before crustaceans – shrimps, crabs and lobsters – had taken up the central roles in the ecology of the ocean they enjoy today. So it would not be incorrect to describe the animals thronging along Delaware Bay as primeval. Indeed, many scientists believe that Limulus is the closest living relative of trilobites themselves. Would the head-shield of the giant Cambrian trilobite Paradoxides, a fossil 510 million years old, have felt the same to the touch as the beached Limulus I restored to the sea in eastern America early in the twenty-first century? Like a horseshoe crab, a trilobite would surely have contemplated me through compound eyes set within its head-shield; its eyes are preserved in detail as fossils. Trilobite legs would have scraped against my mammal flesh with just the same spikiness as Limulus. It would have crept and it would have crawled, brother under its external skin to the hordes on Delaware Bay.
1. A Silurian trilobite, Calymene blumenbachii, from the limestone quarries of Dudley, West Midlands, England.
So a visit to Delaware is to me rather like a visit to the holy city of Rome to a Catholic. Naturally, I had to meet the Pope. The Pontiff of horseshoe crabs is Carl Shuster, in his tenth decade still a giant of a man: craggy faced, walking without the aid of a stick, with lively eyes beneath towering eyebrows, memory and curiosity undimmed, and only betraying his years by his deafness. Like all field biologists he wears a coarsely chequered thick shirt and blue jeans, hitched up with a stout belt. He was brought up during the Great Depression, when he had to run a farm, so he is himself a survivor, like the horseshoe crabs to which he has devoted his life. His father was a mathematician who gave succour to penniless intellectuals during the tough years, while young Carl raised asparagus, chickens and strawberries. He brought together all the current knowledge about his favourite animal in his book The American Horseshoe Crab. He is accompanied in Delaware by his former student, a man of boundless enthusiasm, Glenn Gauvry (himself an implausibly youthful sixty years), who coordinates much of the research on Limulus around the Bay area. Those volunteers who help with counting the crabs during their nocturnal orgies receive a handsome little pewter lapel pin as a record of their collaboration in the conservation project. Naturally, the pin features a horseshoe crab. It signifies membership of one of the more exclusive clubs in the world.
Carl Shuster and his colleagues established the biological facts about horseshoe crabs that allow naturalists to understand how they fit into the ecology of the Atlantic coast. Limulus is a typical arthropod in that it must moult in order to grow, shedding its old coat as a kind of pale ghost of its former self, and growing a new and larger external covering. With a little vigilance it is possible to find one of the cast ‘shells’ on the beach: they are almost as light as tissue paper, for the animal recycles what it can. The newly emerged horseshoe crab is capable of moving immediately. In this it has the advantage over other marine arthropods in the area; freshly moulted blue crabs, for example, are virtually motionless until their new ‘shell’ hardens. They often hide away. Younger horseshoes resemble the older ones apart from being a little spinier. The surprisingly tough, but flexible exoskeleton is made of a chitinous material, similar to that forming the wings of beetles. A typical horseshoe crab takes ten years to reach sexual maturity, after which it does not moult again, but heads to the beach for reproduction. Only these mature animals partake in the littoral orgy, which is why one does not see any little limulids scuttling between the adults. They are not demanding animals: a fully mature animal might go for months without eating. When her time comes, a female may well lay 80–100,000 eggs, and enough of these survive the depredations of wading birds to secure the future generations. The greenish eggs are laid in the sand in batches of four to six thousand in spheres about the size of a golf ball; the female makes repeated visits on successive tides to complete her duties. Females can be recognised by the scars left behind by the mounting males: up to fifteen males may have a chance of fertilising the eggs of any female. Nonetheless, only about thirty-three eggs out of a million survive to adulthood. This means that at various stages of its life Limulus provides a lot of food for other animals. Loggerhead turtles are an important predator on the crabs, even when they are adults. Turtles, too, are animals with a long geological history, so they may have had eons to make something nutritious out of horseshoe crabs, which now seem all sinew and horn and little enough meat. The crabs themselves can survive on molluscs and carrion and almost any kind of scraps, but the strong inner parts of the legs can also crush thick shells if needs be. Although they seem to lurch in an ungainly way on land, under water the crabs are more streamlined and can move quite fast, even sculling on their backs. They can easily right themselves if they need to. In short, they are tough, jack-of-all-trades kind of creatures, built to last. They remind me in a way of a Volkswagen Beetle that I once owned (a beetle being another arthropod, of course) that carried on carrying on even though its coach-work was full of rusty holes, its suspension was down almost to the tarmac, and it often fired on only three cylinders.
This analogy particularly came to mind when I saw a badly damaged horseshoe crab still trundling gamely onwards, even with a great hole punched right through its head. Looking over the beach more carefully there seemed to be a lot of these war veterans: lumps out of the thorax, broken tail spikes – clearly, it must take a lot to finish these creatures off. Glenn Gauvry pointed out to me what a great advantage for reproductive success this resilience would furnish. Such endurance is possible because the blood of Limulus polyphemus has exceptional clotting powers; the animal does not bleed to death because its blood coagulates and ‘walls off’ damaged areas. And the blood is blue. Does not the horseshoe crab begin to seem ‘curiouser and curiouser’, as Alice would have said? The blood of Limulus is blue because it is fundamentally different from that flowing in red-blooded creatures, like you and I and the kangaroo. Whereas we have haemoglobin as our oxygen-carrying pigment, which includes the element iron as an indispensable component, the horseshoe crab carries a copper-based molecule called haemocyanin to do a similar job. In nature, copper often comes with such a blue colour tag. The molecular structure of both these vital molecules is now known in detail, as is the way they move oxygen through the tissues, although this is not directly part of our story. But the Limulus narrative would not be complete without exploring the extraordinary coagulating properties of its blood a little further, because this affects the very survival of the species.
This discovery was made in 1956 by Fred Bang of the Marine Biological Laboratory at Woods Hole. He noticed how Limulus blood clotted dramatically when infected by a particular bacterium. Subsequent research showed that the crab’s blood had an extraordinary sensitivity to a vast range of micro-organisms that are found almost everywhere in nature – known as gram-negative bacteria. A few cubic centimetres of seawater may contain hundreds of thousands of these tiny organisms. Since some of these bacteria are also agents of disease in humans, this property was of immediate interest. It seems that a hypersensitivity to microbial enemies helps to protect the crabs in their natural habitat – as soon as the bacteria enter a wound their defences were up. Limulus has a very diffuse blood system compared with ours, with the interior of the animal bathed in blood, and lacking the defined circulation of veins, arteries, and capillaries we are used to in humans and other vertebrates. In horseshoe crabs the job of defending the works of the animal is given to one type of protective cell, the amoebocyte, which contains a mass of granules capable of promoting clotting. When a gram-negative bacterium is in its vicinity an amoebocyte will react by rupturing and then the granules are released. A clot follows and the infection is sealed off. Now we know why dented and holed crabs can totter on regardless. They have had hundreds of millions of years to come up with an effective response to some of their most dangerous and invisible enemies.
Twelve years later in 1968, Bang and his colleague Jack Levin had managed to prepare and extract the active principle ‘Limulus amoebocyte lysate’ (known as LAL) that clots human blood plasma when exposed to gram-negative bacteria. This is an extremely useful substance in medical diagnosis, readily used for the detection and measurement of the poisonous toxins (called endotoxins) belonging to the appropriate bacteria. Poisonous endotoxins are released into the host organism (you, me, or a horseshoe crab) when the bacterial cell wall ruptures. LAL is a highly sensitive chemical able to detect minute quantities of the offending substances. The LAL test is now widely applied, having been sold on to pharmaceutical companies for commercial manufacture. It has to be prepared close to the Limulus populations, but is then exported around the world. This means that there is a tremendous demand for the horseshoe crab’s blue blood. What had saved it from harm for millions of years now made it a desirable commodity.
The influence of this new industry has been the subject of some debate. Carl Shuster told me that recent estimates say that there may be as many as seventeen million adult crabs in the Bay. By 2003, some three million crabs were harvested for the pharmaceutical trade – an unsustainable quantity. The bird people were worried about the fate of the red knot and its fellow waders. Now the number has been reduced, and the technique for obtaining blood has been adapted so that it does not require the animals to be killed: they have become blood donors! Four companies have the right to what is called ‘bleed and release’, and this method has been applied to some 600,000 crabs per annum. Maybe it is possible to get the LAL and not threaten the horseshoe crabs, after all. Meanwhile, some ornithologists are sceptical, and feel that the companies, as beneficiaries of the local species, should put something back into safeguarding the regional marine habitat for the benefit of all parties, crabs included. Given the long time taken for the crabs to reach sexual maturity there is always a lag before the effects of a population slide can be observed when the summer high tide hits the beach. But there are certainly some very vigilant people on the case.
There was another threat to the welfare of the horseshoe crabs. They were harvested in great numbers to use as bait to catch the giant marine snail or whelk, known up and down the Atlantic coast as conch (Busycon). Big, pinkish conch shells are a familiar item in every seaside knick-knack shop; put to the ear they allow the listener to ‘hear the sea’. Roadside stalls sell the shells for a modest price in the small villages around Delaware Bay. The molluscs inside the shells have a loyal following among connoisseurs of seafood. The only time I tried them I found the flesh very tough. A crab split in two is a pungent treat for the big snails, however, and fishermen along the coast from Delaware to New Jersey are well aware of the power of this lure. The US Fisheries Commission limited the number of crabs to be used to 100,000 in New Jersey, and later introduced a moratorium, but some fishermen moved northwards to Massachusetts or even Maine (the northern limit of the crabs’ distribution) to continue their trade. A method of sustainable fishing must be worked out, and there are hopeful signs. On Delaware Bay, for example, the use of a different kind of trap employing mesh bags has cut bait use by 50 per cent. One cannot help feeling that the horseshoe crabs deserve to prosper unhindered. There may seem to be endless crowds of them jostling for a space on the sand, but the example of the American passenger pigeon comes to mind: countless millions of the birds were slaughtered in the nineteenth century until the species finally became officially extinct in 1914. How dreadful to contemplate the thought that an animal that has survived in readily recognisable form from the early days of the dinosaurs might become extinct in the cause of being a special garnish on a plate of fruits de mer. It is fortunate that its blue blood is so valuable.
Limulus polyphemus is not alone. There are three additional, Asian species of living horseshoe crabs, but none of them can be found in anything like the profusion of the North American form. Tachypleus tridentatus has been given protected status in Japan, where it lives on the Seto Inland Sea. Its shallow-water habitat there is under threat, and increasing industrialisation on the Seto Sea seems unlikely to spare it. Various attempts have been made to conserve the crab, but none of them has solved the problem of making this ancient animal at home in the modern world. Nonetheless, it has an important place in Japanese history, as its form is believed to have inspired classical samurai masks, and brave warriors were supposed to be reborn in the guise of horseshoe crabs. The contemporary artist Takeshi Yamada has made a modern interpretation of masks based upon the ancient icon. A related species, Tachypleus gigas, is fairly widespread in eastern Asia. I saw the fourth species, Carcinoscorpius rotundicaudatus, while I was on fieldwork in Thailand more than a decade ago. As its second, species name would indicate to those with a smattering of Latin, this particular type has a rounded tail spike compared with other horseshoe crabs. When I first set eyes upon Tachypleus, the poor crab was in one of those tanks in a restaurant where delicacies are displayed before consumption, along with several sad-eyed fishes and a dying lobster. I was puzzled by what there could possibly be to eat on the horseshoe crab, because I knew from dissecting its American relatives that they are not exactly meaty. If the species in the tank was indeed a relative of trilobites this might be my first and last chance to taste something resembling my own speciality. When the cooked item finally arrived I felt a twinge of conscience, for it transpired that large, yolky eggs hidden under the head-shield provided the delicacy, which was only available while the gravid females came inshore. I felt that I was consuming the next generation just to satisfy my curiosity. The eggs came served in a thin sauce on a mountain of noodles. They had a rather overwhelming rancid-fishy taste; I am not anxious to repeat the experience.
2. A growth series of juvenile Tachypleus tridentatus, the Asian species of horseshoe crab, collected from tide strand lines in Deep Bay estuary, Hong Kong. (The scale is a 15 cm/6 in ruler.)
As for the place of the horseshoe crab in the tree of evolution, the Latin name of the horseshoe crab I saw in southern Thailand might offer a clue. Carcinoscorpius means ‘crab scorpion’, and that is what these curious creatures are: superficially crab-like relatives of the scorpions. They are the most primitive living examples of a great group of arthropods that includes all living spiders and mites as well as scorpions, and several less familiar kinds of animals. This group is referred to as chelicerates, after those special appendages – chelicerae – located on the head-shield, which they all share in one form or another. All the relatives of the horseshoe crab I have mentioned live on land. But the cradle of life was the sea, and Limulus and its relatives take us back to the far, far distant days when the land surface was barren of larger organisms.
In the darkness along Delaware Bay the scratching percussion of the crabs provides an unmusical accompaniment on an imaginary journey backwards in time: to an era well before mammals and flowering plants; a time before the acme of giant reptiles, long before Tyrannosaurus; backwards again through an extinction event 250,000,000 years ago that wiped nine-tenths of life from the earth; and then back still further, before a time of lush coal forests to a stage in the earth’s history when the land was stark and life was cradled in the sea; a time when a myriad trilobites scuttled in the mud alongside the forebears of the horseshoe crabs. The trundling, heaving, inelegant not-so-crabs along Delaware Bay are messengers from deep geological time.
A palaeontologist would naturally want to track the history of the horseshoe crabs back into the distant past. A few years ago I visited the famous quarries in Bavaria, southern Germany, where the Solnhofen Limestone of Jurassic age, 150 million years old, had been excavated. Great opencast pits scour the gently rolling countryside revealing thin slabs of cream-coloured limestone, where each bed represents the former sediment surface. The limestone provides the perfect fine-grained stone for the manufacture of lithographic printing plates; this is still a popular medium with artists today, but had an even greater use in the past for graphic illustration. The Germans called this kind of rock ‘plattenkalk’, which is an appropriate name because if a fossil turns up it will be laid out on the surface of the slab like a fish on a very flat plate; and some of the fossils are, indeed, those of fishes. The most famous fossils from the Solnhofen Limestone are skeletons belonging to the early bird Archaeopteryx lithographica, complete with feathers, but they are very rare – only one turns up in an average decade. Some other fossils are quite abundant, like those of little sea lilies (Saccocoma). The Solnhofen Limestone is thought to have accumulated in a warm lagoon, or a series of lagoons, not far from a biologically diverse land habitat, but with periodic influxes of waters from the sea. From time to time the lagoon became salty enough from evaporation to poison living organisms, and its deeper parts were depleted in oxygen sufficiently to deter scavengers. The result is the outstanding preservation of delicate animals. When sticky mud was exposed, animals could get trapped upon it, such as delicate flying reptiles or dragonflies. Operating together, these special conditions preserved a huge cross section of Jurassic life. One of these animals is a horseshoe crab called Mesolimulus walchi. It really is remarkably similar to our living Limulus polyphemus. At first glance it looks as if it had just wandered in from Delaware. One has to look hard to notice that its marginal spines are longer than in our living blue-bloods, and there are a few other minor differences. Nobody could doubt that this species, too, trundled through the shallows, nor that it carried its eggs under its head-shield. To that showy new upstart – a feathered bird – it may already have seemed archaic.
Up to this point I have avoided describing the horseshoe crab as a ‘living fossil’. This is not only because I am chary about using a phrase that is a paradox and an oxymoron rolled into one, but also because it is a misleading description. Charles Darwin himself was cautious when he introduced the term in the phrase quoted at the start of this book. Despite what I have just said about Mesolimulus it is not exactly the same as Limulus. Consider everything we have learned about our living horseshoe crab. It is woven deeply into an ecology that is utterly different from that in the Jurassic. Millions of birds of many species depend on the horseshoes’ eggs every year, whereas its old relative was probably irrelevant to the life cycle of what is often called ‘the first bird’. Limulus has adapted to many changes of circumstances: new predators, new climates, and now humankind. It is a winner in the lottery of life, and not just because of its long family tree. ‘Living fossil’ seems to imply a negative judgement somehow, as if the poor old organism was just about tottering along on its last legs, having hardly changed in tune with a changing world, awaiting an inevitable end. A similar misplaced judgemental tone is often applied to dinosaurs. ‘We mustn’t be dinosaurs! We must change with the times!’ is a mantra of commerce. The dinosaurs were actually superbly efficient animals, and their extinction was most likely a combination of external factors (a drastic meteorite impact is favoured by many) that had nothing to do either with their virtues or lack of them. They were animals of the wrong size living in the wrong places at the wrong time. Bad luck! Meanwhile, the living fossils trundled on through the crisis because … well, we will come to that.
Modifications are happening at the genomic level all the time. There really is no such thing as ‘no change’; the very flexibility of the DNA molecule is what has kept natural selection on its toes for thousands of millions of years. Nor is change in DNA necessarily related directly to any change in the appearance of an animal. Many mutations accumulate in the large fraction of the genome that apparently does not do much work in the specification of proteins, or initiating developmental changes, or any of the other vital, active stuff. These mutations might well be irrelevant to the kind of changes in shape or colour that indicate the appearance of new species. A living fossil may indeed have accumulated many changes at the molecular level that have not even been expressed in its surface appearance, which is the phenotype that has to face the world. Fluctuations in gene frequency are the stuff of life, but they don’t map one-to-one on skeletons and limbs, which are the usual stuff of fossils. So a little caution in terminology is wise.
There is also a temptation to think of the living fossil as if it were a true, surviving ancestor. When the coelacanth fish was discovered it was presented in the popular press as ‘old fourlegs’ as if it were just about to march onto land on its stumpy fins as a thoroughgoing tetrapod. Not only does this scenario happen to be wrong, but the likelihood of any such ancestor surviving unchanged to the present day through many millions of years is also exceedingly remote. Time, chance, and competition will see to it that change is inevitable. What can be said without demur is that the ancient survivor and its other living – and more evolutionarily advanced – relatives will have shared a common ancestor, and that the features of the living fossil will be closer to those of that ancestor. The discovery of ancient fossils more or less similar to the survivor will date the appearance of the whole animal group to which they belong, and point up the changes that must have happened through geological time along the subsequent branches of the evolutionary tree. The survivors from the early days carry with them a package of information revealing primitive morphology, development, and biochemistry that can illuminate histories that would otherwise be hidden from us. Fossils never preserve blue blood. The ‘living fossils’ may not be the ancestor, but they are survivors carrying a precious legacy of information from distant days and vanished worlds.
Hence Limulus allows us to understand something about deep branches in evolution. It is far from unique. If every descendant species had simply replaced its predecessor, the history of life would be like one of those patients described by Oliver Sacks who live perpetually in the present day, constantly erasing the memories of yesterday. Fortunately, life is not like that. Deep history is all around us. In the life of the planet, the latest model does not always invalidate the tried-and-tested old creature. Groups of organisms that originated long, long ago, in very different worlds, have been able to evolve and adapt alongside their more recent cousins and second cousins. The story of life is almost as much about accommodation as it is about replacement. To look at a living horseshoe crab is to see a portrait of a distant ancestor repainted by time, but with many of its features still unchanged. This book reflects my interest in living survivors from the geological past and what they can tell us about the course of evolution. I have spent the last few years seeking out animals and plants that have helped to illuminate our understanding of the history of life. Wherever possible, I have visited these organisms in their natural habitats; none has proved less than fascinating. Observing how they survive today has allowed me a glimpse of their biology and provided clues about the reasons for their longevity. I have carefully selected the old timers I visited because I wished to understand their biology in depth; I have had passing encounters with several more. A few organisms proved too rare or inaccessible for me to discover personally – the coelacanth comes to mind – and then I have relied on the accounts of others. I shall relate many of these case histories to those of their fossil relatives, which is only to be expected of a palaeontologist. This will illuminate the vital fourth dimension – time. I soon discovered that there were too many potential candidates for inclusion, and I am obliged to mention some of them only briefly. I believe it is better to deal with a smaller number of organisms in detail than swish around vaguely with a broad brush. My specialist friends will probably complain that I have left out their particular favourite beast or weed, and my answer is that these survivors have lasted so long that they will almost certainly still be around for someone else to champion in the future.
Consider scorpions, for example. In some ways they are as impressive as horseshoe crabs as survivors. I have met them several times in my fossil collecting career, usually hiding beneath a log or a rock, for many of them stalk their prey at night and stay out of sight by day. In the Oman desert I once disturbed a huge, black knobbly scorpion that came running at me with its tail-sting erect, while I backed off in the opposite direction, gibbering foolishly. My Omani companions laughed and told me that its sting (in the tail of course) was relatively mild. A few hours later I lifted up a rock slab and nestled beneath it was a small yellowish scorpion with a flattened, side-wound sting. I was about to poke at it with my geological hammer when my companions tugged at my arm. ‘Don’t touch, it’s a real killer!’ The smaller, insignificant-looking creatures can often be the most deadly. The spike on Limulus’ tail and the sting on the scorpion’s are closely related structures, and indeed both animals belong to the same great arachnid group. The scorpion learned the trick of arching over the very end of its body to dart poison into enemy or prey. Encased within an external skeleton (cuticle) that prevents evaporation with outstanding efficiency, the scorpion has been able to live far away from water; some species specialise in surviving in the driest places on earth. Scorpions started out as sub-aqueous creatures like Limulus, and only later did they acquire the skill of living on land. Back in Devonian times, 400 million years ago, their relatives, the sea scorpions (eurypterids) were the largest invertebrate predators ever to have lived, some as long as a man. There are fossils from the Carboniferous age that really do look like living scorpions, at least to the non-specialist. They, too, have faced out extinction events that have blasted greater and more glamorous animals. The scorpion is built into mythology as a sign of the zodiac; it features on Roman mosaics, and in the Bible (1 Kings 12:11): ‘my father hath chastised you with whips, but I will chastise you with scorpions’. So one could argue that the scorpion’s connection to human culture is more pervasive than that of the horseshoe crab. My choice of organisms has been guided by the place they occupy in the tree of life, rather than by their innate charisma or significance in folklore and culture. The horseshoe crabs earn a special place in this natural history because their relatives root down to the beginning of the diversification of animals. The early Permian Palaeolimulus is clearly a horseshoe crab, for all that it predated the great extinction that put paid to most species at the end of the Palaeozoic Era, 250 million years ago. Limulitella is present in 242-million-year-old (Triassic) strata dating after the great trauma, evidence of their survival. Those distinctive tracks left by the tips of the legs, and the trail of the tail, that I observed in Delaware have been found as fossils even in the absence of the body itself. There were horseshoe crabs crawling among the coal swamps of the Carboniferous (Pennsylvanian), a little better segmented perhaps than the beasts on Delaware Bay, but carrying the distinct signature of their ancestry. In 2009 my Canadian colleague, David Rudkin, announced the discovery of the oldest typical horseshoe crab in rocks of Ordovician (approximately 450 million years) age, thus taking these simple arthropods back before all the major extinction events that have rocked the Phanerozoic biosphere. Whatever the magic ingredient for survival is, the horseshoes clearly have it in spades. ‘The meek shall inherit the earth’ may be an appropriate motto for their longevity.
3. Gustav Vigeland’s sculpture of a survivor, the scorpion, Frogner Park, Oslo, Norway.
Let me describe these early days in more detail. I have already remarked that the horseshoe crabs had set out upon their distinctive path before the first land plants had advanced upon harsh and barren shores; although recent discoveries suggest that a few simple plants may have already ventured onto mud flats. These had probably not yet been followed by insects or spiders. There were fishes already, of a primitive cast, but they had no ambitions then to invade the land, although a few species may have nudged into waters that were not fully marine. The seas abounded with trilobites, which occupied every ecological zone from shallow shores to ocean deeps. These prolific arthropods must have been many times more abundant than the early relatives of the horseshoe crabs. They evidently had an advantage at the time. This may have been the evolution of their robust dorsal ‘shell’ of calcite, which allowed them to develop spines, armour and a tough anchor for muscles, as well as an ability to roll up into tight, impregnable balls when threatened. Trilobites soon learned an array of different feeding habits; some were predators, some ate soft mud, others swam in the open seas. They died out some 255 million years ago. By contrast, the relatives of Limulus may have stayed conservatively on the sea floor as scavengers and predators. The horseshoe crabs on Delaware Bay have an exoskeleton of chitin, which is a natural polymer that is quite tough and flexible, although no substitute for stony calcite. But the horseshoe crab has turned what might have been a weakness to advantage by developing an exceptional immune system. Survival in the long term may depend on more subtle features than armour alone.
It is possible to trace the horseshoe crab story still further back, into the Cambrian Period more than 500 million years ago, to a time when many of the major types of animals converge towards their common ancestors. The Cambrian was an interval of unprecedented evolutionary activity and I shall describe its special features in more detail in the next chapter. Early relatives of Limulus have been identified in Cambrian strata, but they include some species that look a little different from their hardy survivors. Some of them also look more like early trilobites, such as Olenellus, a form with a big head-shield surrounded by a narrow rim; one might expect a family resemblance if they are indeed closer to a common origin. There are important differences, too. Where the limbs of trilobites are known, they are similar all along the length of the animal: the paired limbs are each split into a walking leg carrying a comb-like branch near its base that in all likelihood functioned as a gill. They are not subdivided into different ‘packages’ in different parts of the body separating walking and feeding appendages in front from gills behind, as they are in Limulus. To add to this, all trilobites had typical ‘feeler’ antennae near the front of the head, and none had the strange chelicerae. This may not be so important, since having antennae seems to have been a general property of primitive arthropods. It might just be that the trilobites still retain this one characteristic more primitive than Limulus and its allies, but they could yet have descended from a common ancestor. Trilobites are abundant fossils on account of their easily preserved calcite hard parts. Fossils of unmineralised animals are altogether more unusual. Spectacular recent discoveries of fossils of soft-bodied animals preserved within Cambrian rocks have been made in China and Greenland. These have revealed an almost embarrassing variety of undoubted arthropods early in the Cambrian. Some of them might seem to bridge the differences between Limulus and its allies and the trilobites, but for every feature that points one way, there seems to be another that suggests something else. For more than a decade now palaeontologists have argued about how these fossils should be classified, and about the only thing they all agree upon is that the Cambrian threw up many animals with curious combinations of characteristics that were probably winnowed out by subsequent evolution. It is not, perhaps, so surprising that ‘mixed up’ animals lived at this Cambrian time, because all the arthropods were not genetically far apart then – they would have had the subsequent 500 million years to box themselves into more separate evolutionary compartments. In these early days the destiny of one animal to become a crustacean, say, and another a chelicerate was not easy to anticipate.
When scientists are confronted by conundrums of this kind, they usually turn to computers. There are now sophisticated computer programs that deal with the problems of determining relationships between animals. They work by identifying the particular arrangement of the creatures analysed on a branching tree that most succinctly accounts for the features they share with their fellows. The most significant resemblances in morphology should result in organisms being classified together on a single branch. Like so many computer methods, the inner workings of the process are staggering in their complexity, so that for a big problem like analysing the Cambrian arthropods millions of potential arrangements of trees embracing the animals under study will be inspected and rejected. My own appreciation of what goes on inside these machines is thoroughly naïve, and I cannot suppress a vision of thousands of cards being shuffled into piles like a supercharged game of Patience until the answer ‘comes out’. The end product is a diagrammatic tree (technically, a cladogram) that can look enticingly simple. I should add that the way the summary ‘tree of life’ on the endpapers is drawn is not like a cladogram, but it does incorporate the results of many individual cladistic analyses. Like all computer methods, the latter are subject to the familiar caveat of RIRO (Rubbish In Rubbish Out), but the fact that they have been so widely used indicates that they have helped with thorny problems. According to the analyses to date, on balance the trilobites indeed do still classify within a group that also includes the horseshoe crabs. Despite all the confusion of the Cambrian it seems my crusty-shelled friends and the dogged, eternally trundling horseshoe crabs are sisters under the external arthropod skin.
They do share special features. The larva of the horseshoe crab is a pinhead-sized object long known as the ‘trilobite larva’, because it does resemble the tiny larva of many trilobites.
Both kinds of animals grow larger with each moult in similar ways, casting off their old external housing and re-growing larger premises. Then there are the compound eyes. In both trilobites and horseshoe crabs the eyes are included as part of the head-shield, rather than sticking out separately at the front on flexible stalks as they are in the majority of crustaceans. Most of us will have looked a lobster in the eyes before popping him into the pot. The lenses of the trilobites are unique in the animal kingdom, since they are made of the mineral calcite. Hard calcite makes up the hard parts of the trilobite, providing the crusty shield that covers the back of the animal known as the dorsal exoskeleton. Calcite has also been recruited to provide the material for the lenses of the eye – so they have become ‘crystal eyes’ if you will. The individual lenses are minute in many trilobite eyes (they can have several thousand), but each separate lens presumably responded to an external light stimulus, and then an optic nerve conveyed the information to the brain. Eyes with many small lenses are usually thought of as particularly sensitive to movement: a moving image progressively impinges on different lenses within the field of view. Both trilobites and Limulus have eyes that look predominantly sideways, scouting around over the sea floor where they live. Strangely enough, the eye of Limulus has been very intensively studied. Haldan K. Hartline of the University of Pennsylvania used the eye of the horseshoe crab as his experimental material to investigate the physics of animal vision. In the 1930s he was the first scientist able to record the activity of a single optic nerve fibre attached to a lens (ommatidium). Limulus has about a thousand such fibres in the eye, and we might well imagine that trilobite eyes had at least a comparable sensitivity. He later showed how different fibres in the optic nerves respond to light in selectively different ways. This opened up the route to a whole new field of physiology – and earned Hartline the Nobel Prize in 1967. Robert Barlow and his colleagues are now building further on Hartline’s research. They have attached miniature video cameras onto living animals in order to scrutinise exactly where the horseshoe crabs are looking. The eyes seem to exhibit an unsuspected sophistication. There is apparently a natural, or circadian rhythm in the sensitivity of the ocular system, which combines with other dark-adaptive mechanisms so that their sensitivity at night may be as much as a million times more acute than in the daytime. Crabs are particularly attuned to recognising potential mates, which, given the frenetic activity along Delaware Bay, is not altogether surprising. The ability of the Limulus eye to eliminate visual ‘noise’ is quite extraordinary (think of our own faltering attempts to really see very faint stars on a dark night), and Dr Barlow is currently trying to understand how this works right down at the molecular level. It is probably the case that we know as much about the visual system of this ancient arthropod as about that of any other living creature. But the more we know the more we might wonder whether this particular survivor is primitive or just exquisitely adapted. Did the trilobites have blue blood? There is no final proof one way or the other; nor can there ever be with such perishable stuff as blood. However, there are many examples of trilobites that have been severely bitten and yet have survived. They usually show a sealed-off gouge on one side. Even in the early Cambrian there were predators such as the lobster-sized Anomalocaris and its relatives that might have regarded a trilobite as a crunchy snack. Anomalocaris was a strange, but evidently raptorial arthropod with two long grasping arms and a mouth surrounded by plates. In those days of accelerated evolutionary change natural selection would rapidly have favoured any mutation that stopped a wounded trilobite from bleeding to death, and the same would have applied to any of its relatives. Since the circulation system of Limulus, and doubtless of a trilobite, is diffuse compared with our own – it more or less fills the open spaces between the other internal organs – a general clotting agent would have been at a premium. It does seem possible that the alternative way of making blood – the copper route – could have had a very long pedigree, and that the blue ichor’s ability to seal wounds and its sensitivity to infection could have helped both trilobites and horseshoe crabs to survive in a newly vicious world. This is one of those moments when palaeontologists wish they could circumvent the rules of the space-time continuum, and go back and see for themselves. As it is, we have to make do with more or less plausible guesses, in the process trying to persuade our fellow scientists that we have undoubtedly arrived at an entirely logical conclusion. History, of course, does not necessarily have to follow our own human logic, and may have surprises of its own.
Could a scene like that witnessed at the beginning of this chapter been played out by trilobites in deep geological time? It is possible. To see evidence I must take you with me to the small town of Arouca in northern Portugal. It lies at the end of a very winding drive into the hills from the old seafaring city of Porto. The prevalence of hillsides covered with eucalyptus trees in some parts of this landscape can be depressing, as these antipodeans are out of place here; but their contribution to the local economy pushes all ecological niceties to one side. Most go to pulp for paper, for these efficient trees grow faster than native species. So in another sense these eucalypts, too, are natural survivors. Every now and then bush fires flare up uncontrollably, fuelled by the volatile oils of the ‘gum trees’; black swathes along the hillsides record their ugly legacy. In the higher hills, pretty valleys contain ancient mills and farmhouses built of crudely squared-off large blocks of the grey granite that makes up the highest, bare ground in the region. In geological terms, obstinate granite is probably the longest survivor of all. Little has happened to the face of these sensible buildings since medieval times other than a dappling of face-paint provided by lichens. On the bleak granite moors nearby are burial chambers that have seen much of human history pass, but still endure. Since the time of the trilobite, whole mountain ranges comprised of this most persistent stone have been worn away grain by grain by the inexorable forces of erosion, and rendered down to sea level. Life outlasts even mountains, for the greatest survivor of all is DNA.
Arouca must be the only town in the world with a trilobite monument, which is a tall spike sitting a little uneasily in the centre of a roundabout. The small hill town is bidding to achieve European Geopark status, and part of its claim is as the home of giant trilobites, which figure prominently on the monument. To see the real thing I head off to the slate quarries above the town near the little village of Canelas. Mining has been a part of the culture in the region for a long time. The Romans were in the hills seeking gold, and old workings excavated into tough Ordovician sandstones can still be seen atop a local high spot, where a dark and slippery stairway leads down into a ferny crevice. The same sandstones preserve fossils of burrows made by trilobites digging into an ancient sea floor, providing yet another type of treasure. Nowadays, the booty is roofing slate. A mass of Ordovician slates known as the Valongo Formation over-lies the sandstones and runs across country. The slates are nearly black, and split into flat sheets that can be further split again until they make usable roofing slabs. Once prepared this way, they are very durable commodities. The slates are extracted from large quarries by blasting out huge chunks of rock, which are then carried away to a factory for further working. The flat planes along which the slate cleaves also furnish a record of Ordovician sea floors, albeit now turned almost vertically as a result of convulsions of the earth. Every now and then a slab covered with trilobites is discovered. They are, as my Spanish colleagues exclaimed without overstatement ¡espectacular! The fossils often show up pale greyish against their dark background. Under normal circumstances it is a rare event to find trilobites much bigger than a small shoe, but in this locality they are often as big as tureens. The largest trilobite in the world, perhaps a metre in length, may be lurking among unstudied collections, but specimens 70 cm long are already familiar. Not only are they large, they are also numerous. Because whole bedding planes (which represent former sea floors) are extracted, an extensive view of a tragic moment in time is occasionally recovered: it is a fossil graveyard, with bodies laid out at the moment of death, a community of cadavers. A scenario like this could not be extracted by the usual tapping of the geologist’s hammer upon a rock: it requires activity on an industrial scale. Fortunately, the quarry owner is aware of the importance of his slates in exposing a sea floor perhaps 470 million years old; time enough to erode three mountain ranges, granite and all. Many of the trilobites are preserved on site in a private museum that the owner has generously dedicated to conserving these fossil remains. A dozen different species are on display there; to one in thrall to the past like me it is an extraordinary experience to see these grey bodies covering every wall. It has something of the feel of a picture gallery, and I have to remind myself that these were once scuttling animals as intent on their business as any living horseshoe crab.
Many of the large slabs show assemblages of just one species together, and the individuals are all large and of similar size. They are often complete bodies, which suggests they are entire animals that have been killed rather than, say, the ‘cast-offs’ left behind after moulting, when bits and pieces might be expected, arranged higgledy-piggledy. There are examples where the bodies partially overlap. All this is very like the mating congregations of horseshoe crabs along Delaware Bay. Imagine if some catastrophe had killed and preserved the crabs at the height of their nuptials. A volcanic eruption might fit the bill; this would bury and kill the animals at exactly the same time. After eons passed the sediments would have hardened into rock and the crabs would be fossils; compaction of the sediment would also have flattened down the buried beasts. Some fossil specimens would still partly overlap their partners, frozen in the act. The younger animals would have been elsewhere, so they are not represented among the fossils. It is a plausible scenario, even a tempting one. We have to add an extra complication, because something additional had happened to the Portuguese trilobites during their long sojourn in the rock. The whole mass of slates of which they have become a part has been squeezed in a tectonic vice that has twisted some specimens out of true until they look a little lopsided. Others have been stretched somewhat, and as a result claims about the ‘longest ever trilobite’ have to be treated with caution.
A more critical examination of the evidence identifies some important differences between Delaware Bay today and Ordovician Portugal. The most obvious of these is that the giant trilobites were clearly not gathered upon a beach. They were overwhelmed and killed on the sea floor. Local Portuguese geologists believe that the Ordovician animals lived in a marine basin with poor oceanic circulation, so that deeper layers could become stagnant. The congregated trilobites might have been overcome by a phase when oxygen dropped to lethal levels: after all, even trilobites needed to breathe. Such anoxia is not much of a problem in Delaware Bay. The trilobites could still have been gathering for reproductive purposes, of course. They might have even been safer from predators in the deeper basin. But then it makes us uneasy to think of the trilobites depositing their eggs in such an inhospitable place – unless anoxic events were so rare as to have little effect on their long-term survival. Then there is the fact that a number of the slabs seem to show a mixture of species. Could they have been gathered together for some purpose other than mating? Unlike Limulus, a freshly moulted ‘soft shelled’ trilobite would have been vulnerable until it grew a new hard carapace. Maybe these congregations were huddled together for mutual protection away from the prying eyes of predators. With these ambiguities in the picture the case for a direct comparison with the behaviour of modern horseshoes begins to seem weaker. A sceptic would say that it is simple minded to expect similar habits to endure for hundreds of millions of years. Perhaps so, but common problems in nature often come up with comparable solutions, the more so if the organisms concerned are related. Those trilobite examples with marginally overlapping bodies might merit further examination, since they do recall the struggle for mating among the horseshoe crabs, and it is more than a guess that eyes in these animals were particularly attuned to seeking out mates. I still like to think that the crystal eyes of trilobites may have had similar lustful intent.
2
The Search for the Velvet Worm
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.
3
Slimy Mounds
Shark Bay is a long way from anywhere. In Australia, distance soon acquires its own curious rules. Within the suburban strip that lines favoured parts of the coast there are traffic jams and shopping malls like anywhere else, but away from civilisation the outback country stretches onwards forever. Far from the mountainous east, much of the country is flat. No doubt connoisseurs of the horizontal find infinite entertainment in its small variations, but for me a bemused puzzlement sets in after a few hours apparently rehearsing the same piece of landscape numerous times. Time begins to stretch in odd ways. After a snooze, I wake up unsure whether I have been asleep for ten minutes or two hours. Small eucalypts line wandering creeks while sand dunes are covered with scrub, occasional scruffy fences mark obscure ownership, and there are groves of taller gums or isolated she-oaks stocked with the noisy parrots known as galahs. Then the sequence repeats, but not necessarily in the same order. The landscape is utterly distinctive, like that of nowhere else in the world, with a stark beauty under a clear pale blue sky, but it is also relentlessly repetitive. Anyone foolish enough to leave the marked track will find it is easy to get lost. Bush stories are full of sticky ends and grieving widows. I know that maps do not really work in a landscape that repeats like an old tune whistled over and over.
Route 1, running up the west coast of Western Australia towards Shark Bay, seems never to end. The Greyhound bus runs onwards through the dark, with nothing really distinguishing the passage of miles except sporadically a startled kangaroo picked out in the headlights. Occasional vehicles pass the other way, and each one seems something of a surprise. What can they be doing out here? I have to remind myself yet again that I am en route to see one of the holy relics in geology; it will be worth the effort. After countless hours, the Overlander Roadhouse welcomes me – a neon-lit marker set down in the endless landscape; a gas station, with a rudimentary restaurant, a place to loaf about until the next bus arrives. Aboriginal people wait there desultorily for relatives who have been off to Perth or somewhere to make a few dollars. Flies buzz about, with irritating persistence; there must be something else for them to do than endlessly return to drink from the same sweaty brow, or so one would think, but round and round they go. Backpackers loiter, waiting to embark on the next section of an adventure planned in theory, but now measured out in sweat and flies. It is a kind of end-of-the-world place, on nobody’s list of ‘must-sees’, but an essential stopping point before negotiating the wilderness. This is a place where timetables mean something to somebody, a place where I can get the next bus to see the stromatolites. Not far from the Overlander Roadhouse is a place that tells us of the transformation of the very air we breathe, a window opening into remote Precambrian times.
Though the outback may look pristine, in this part of Australia the wildlife has been transformed by human introductions. Feral goats have degraded the natural bush, and cats have culled the nocturnal mammals that were once numerous. The big-eared marsupial bilby, with its back legs like a miniature kangaroo and improbably long tail, is such a charming animal that it has become a kind of mascot for the conservation movement hereabouts. It would indeed be tragic if its only permanent memorial were in one of those perfectly photographed wildlife television programmes. Conservationists in Australia have taken to referring to the ‘Easter bilby’ rather than the ‘Easter bunny’ (bunnies being voracious introductions, too). It is already too late for many small marsupials in the eastern states of the country; their only record now being watercolour drawings made by the early naturalists. These harmless creatures could not outwit intelligent feline and canine hunters, and they failed to survive. Australia is full of poignant paradoxes. This land has many ancient biological survivors yet it is also, much like New Zealand, a place where the extinction of species is still in progress. This is despite the efforts of a generation of Australians many of whom treasure their unique fauna and flora. Almost every town boasts dedicated people concerned with ‘bush regeneration’, and in Western Australia new species of beautiful indigenous plants are still being discovered regularly, even around Perth. It is a very biodiverse region, despite the challenges of the climate, and not yet fully known. While I was there Tropical Cyclone Hubert turned the sky black, and sections of the main road were closed. The species that live in this tough land must be natural survivors to be able to negotiate fluctuations between flood and swelter. That description, of course, also includes feral cats.
Shark Bay is a huge and ragged bite into the profile of the west coast of Australia. It has now become a World Heritage Area, which brings more money and more tourism. Much of the former, and nearly all of the latter, is directed to the beach resort of Monkey Mia where ‘swimming with dolphins’ is on offer. When I flew over the Bay and its clear waters in a light plane, I saw an undulating submarine prairie of sea grass, dark emerald green, broken into banks like meadows. A tenth of the world’s dugongs – 250 kilograms of peaceable herbivorous sea mammal – graze in leisurely fashion upon this luscious expanse, many living to seventy years or more. Juicy fishes doubtless account for the name of the Bay, since they attract fourteen species of sharks, including species like the tiger shark that command respect. From the air I saw how Shark Bay is divided into two large lobes by a median peninsula; the aboriginal name for the Bay is ‘cartharrgudu’ (‘two bays’). The top of the peninsula is now the Francois Peron National Park and a serious attempt is being made to clear this sandy area of feral goats and predators for the benefit of the native fauna and flora. Dirk Hartog Island provides an outer barrier to the Bay, which protects the coast from storms cutting across the Indian Ocean. I never knew before visiting Western Australia that this island was the first landfall for any European. The Dutchman, Dirk Hartog, landed here on 25 October 1616, beating Captain Cook to it by 152 years, and leaving a pewter plate nailed to a post as evidence. That plate is still preserved in the Rijksmuseum, Amsterdam. William Dampier, ‘the buccaneer explorer’, spent a week there in 1699 and gave the Bay the name we use today. The aboriginal fishermen were plying their trade at the time, but there is little evidence of them now. I conclude that it is not only small and shy marsupials that failed to survive.
My quest is for something altogether more recherché than shark or dugong. At the tip of the eastern bay the edge of the sea provides a prospect of life two billion years ago … I am travelling incredibly far back in time. The journey to the old telegraph station at Hamelin Pool takes me through undulating, intensely green scrub interspersed with a few mallee trees, interrupted only occasionally by flat-bottomed depressions carrying scrappy salt-scrub and patches of white gypsum – the aboriginal inhabitants called these clay-pans birridas. I missed the flowering season, and now all the bushes seem to bear black nuts. Next come low dunes made up of startlingly white tiny shells. I crunch my way across the dunes, and beyond lies a very shallow arm of the sea. This is where the stromatolites grow. I am approaching the famous site where living analogues still flourish of the most ancient organic structures on earth. They ought to have disappeared long before the first velvet worm or horseshoe crab, but here they linger on, a marvel of anachronism.
Back at the highway must be the only road-sign in the world that points to ‘STROMATOLITES’, and no geologist or palaeontologist could fail to follow its bidding. Here they are growing by the shore while the sea beyond shines an almost improbable ultramarine. Is this luminous vision the time warp I sought? Some part of me expects the stromatolites to be green, but they prove to be darkish umber brown. I confess I am momentarily disappointed. They comprise flat-topped cushions and low pillars, or even giant mushrooms expanding upwards like plush stools, with sandy gullies between them. They are regularly disposed along a seaboard more than a hundred yards wide; seawards they disappear beneath the barely lapping waters. It is a scene of perfect calm. A little walkway has been built over the strand so that visitors can get close without damaging the organic structures. I touch one of the hummocks. It is actually quite hard (why did I expect it to be soft?) and slimy or tacky to the touch when moist, but almost crispy when dry. In the bright Australian sun it is even a little warm. Now that I get closer I can see other kinds of surfaces along the shore, particularly sloping stretches of dimpled microbial mats, a fruity brown colour, running down to the glittering sea. They make stretches of the shoreline resemble wrinkled skin. Stromatolites growing at the water’s edge look less like cushions and more like knobbly cauliflower heads. The inevitable flies are buzzing about my head, and some antipodean swallows chirrup cheerfully about the platform. I hope they are after my flies.
Up on the shore are some dead stromatolites, left behind by the sea maybe a thousand years ago. By now they have decayed into iron-stained ruins, but where they have broken open they show the internal structure of the cushion-shaped columns. It is clear to me that the columns are layered internally parallel to their top surfaces, rather like filo pastry. They seem to be built up layer by layer – a little like those giant stack pancakes an unwary visitor gets offered in New York for breakfast. The columns were evidently living things, self-made towers. A little museum on the site of the old telegraph office nearby provides more explanation. I peer closely at a stromatolite kept in a glass tank; its enveloping seawater must be refreshed every month. I see that when water covers the column its surface is slightly fuzzy – no doubt, it is still alive. A lack of crisp definition is somehow a proof of metabolism in action, life blurring the edges. Little bubbles fizz upwards off the top in a steady stream, none bigger than a lentil: they are bubbles of oxygen. So the column is evidently more than a brownish crust, it is something altogether more potent and dynamic, and it is breathing out oxygen, the element that babies and bilbies and bunnies all need to stay alive. Everyone has had nightmares about suffocation, when fighting for breath becomes fighting for life, so we all know in our bones how quickly we would perish without oxygen. The exhibition reminds me of the demonstration of nature in action at my very first school, when us kids looked at water-weed in a full glass beaker, and saw the same little bubbles of oxygen rising to the surface. This was the first time I heard the word ‘photosynthesis’.
The survival of the stromatolites on the beach is another measure of their toughness. On the foreshore I see two broad grooves carving their way through the stromatolite grove. These are the persistent traces of a former industry. In the late nineteenth and early twentieth century, camel trains brought bales of wool here to Flagpole Landing. These were then carted off the foreshore to lighters that sailed 190 kilometres to a boat waiting in deep anchorage off Dirk Hartog Island. Then the wool was transported to Fremantle and finally to the United Kingdom for manufacturing. We are fortunate that these activities did not destroy the mounds completely. But it is also a measure of the slow rate of biological activity hereabouts that the old tracks are still visible after a century.
Sea conditions in this part of Shark Bay are quite particular. The shallow seawater evaporates fast under the relentless sun. It is the basis of a salt industry at Useless Loop nearby. The very clear water has an elevated salinity and is very poor in nutrients. Hamelin Pool is backed up behind a sand bar known as Fauré Island, lying about forty-seven kilometres out to sea, so it is almost a lagoon. Only specially adapted or tolerant organisms can survive under these conditions. One of those animals is a little clam called Fragum hamelini, which, as the name implies, is special to this locality. It is so abundant that its snow-white shells, none bigger than a walnut, make up the dunes that line the Bay. After some decades the shells harden into a shelly rock – it would be an exaggeration to call it a limestone. An old quarry above the shore records the employment into which this curious white stone has been pressed. Cut into blocks the size of large bricks it made a serviceable, if hardly robust building stone. Some of the older edifices made of it still stand. The stone was used to build the walls of the Pearler Inn in the town of Denham, eighty kilometres distant. This pub looks as if it were constructed from a mass of white peas. In order to survive the testing conditions in the Bay, Fragum has incorporated photosynthesising algae into its tissues: sunlight is the ultimate source of its food, just as it is for the stromatolites. But Fragum is an evolutionary newcomer, whereas the stromatolites are very, very ancient.
Stromatolites are mounds slowly built up by microscopic organisms, layer by layer. The mounds are not composed of a single organism: they are a whole ecology. The tacky or slimy skin that caps the stromatolites is the living part. This very thin layer is composed mostly of cyanobacteria, organisms that are often called ‘blue greens’ (or, formerly and incorrectly, blue-green algae) on account of their characteristic hue beneath the microscope. This may well explain why I expected the stromatolites to be green. The conditions in Hamelin Pool suit their growth. There are many organisms in nature that like to graze on ‘blue greens’. Think of those finely scalloped trails wandering over moist rocks by the seaside, made by the rasping action of the sea snail’s feeding apparatus as it scrapes away the thin nutritious bacterial layer that paints the rocky surface. This is not inappropriately compared with grazing by herbivores on terrestrial environments. Like grass, the ‘blue greens’ grow back, and the molluscs move on. But these micro-organisms never have the chance to build complex or elaborate structures like mounds or ‘stagshorns’ because the constant assault of herbivores renders their best attempts at architecture futile. Everything is eaten back before it can grow too big. However, in the special, warm world of Hamelin Pool the grazers are kept at bay. No snails sully the sticky surfaces of the stromatolites; the fish there don’t nibble away the ‘blue greens’ for supper; in fact, nothing much ventures into the almost unnaturally limpid seas. Some authorities believe that the very low nutrient levels in the Pool are as important in growing stromatolites as the absence of grazers. Whatever the reason, the simple organisms have it all their own way for once. And when they do, they reconstruct the Precambrian world. This is how life was before marine animals chomped and scraped away ancient biological constructions that had covered much of the sub-aqueous environment since life began. In Shark Bay a prelapsarian age can be restored to view, a time before velvet worms or even vendobionts, or anything that crawled upon its belly in the mud. I have seen dozens of artist’s reconstructions of ancient seascapes that owe a debt to the prospect at Hamelin Pool. So when I saw the living stromatolites I was not unprepared for the experience. However, I recall seeing Picasso’s Guernica for the first time; just because an image is familiar does not diminish the impact of the real thing.
Cyanobacteria are simple organisms that often make long, green and narrow threads with organic walls which can be as thin as a few thousandths of a millimetre, but which often occur in sufficient profusion to make green slime. Other species are tiny round cells that grow by fission – essentially splitting in two, to double up as identical twins. They are ubiquitous. When a glass of water is left in the light on a window ledge, cyanobacteria will usually appear as a green smudge. They have been wrongly called ‘blue-green algae’ in old textbooks, but as we shall see the algae are altogether more complicated organisms. When raindrops wash over rocks in a desert these tiny organisms will soon take advantage of the opportunity to grow, and the rocks will shortly glisten with microscopic life. In the sea, their numbers occasionally erupt into ‘blooms’ of billions of cells that can poison fish, or even humans, if they eat the wrong kind of shellfish too soon after one of these events. In biological jargon the ‘blue greens’ are described as prokaryotes. They are both the smallest and the simplest-looking cells – often no more than a sphere or a sausage – but there are hundreds of different species. They lack an organised nucleus surrounded by a membrane that is present in every cell in what are termed eukaryotes. Every organism that has been mentioned so far in this book (including the author) is a eukaryote, which is another way of saying that our narrative has now arrived back to a simpler way of organising a living entity. Prokaryotes came before eukaryotes in time, which also means that they are closer to the main trunk of the tree of life. So there was a world before eukaryotes where the cyanobacteria were state-of-the-art and where the prospect before us in the shallow waters in one corner of Shark Bay would have been typical of much of the world, rather than a special survivor. I should flag up at this point that this prokaryote– eukaryote division is itself an over-simplification, and this topic will be revisited in the next chapter.
Modern seaweeds are both plants and eukaryotes, to emphasise the point again, and do not build stromatolitic mounds. In Shark Bay, the majority of such ‘advanced’ organisms are discouraged by the low levels of nutrients available there; hence they leave the dominant cyanobacteria to cooperate in making different kinds of mounds. In the typical stromatolite the mode of growth is cumulative. The living ‘skin’ is a thin layer of growing threads matted and twined together. The technical term for it is a ‘biofilm’. The cyanobacterial mats are positively attracted to light and grow upwards. Any blown dust and other fine sedimentary material becomes incorporated in the surface layer and maybe provides the modest nutrient required. The slimy surface layer of the bacterium encourages the precipitation of calcium carbonate from its dissolved state in seawater, thus making a thin ‘crust’. A new living layer grows on top of the one beneath, and may be able to extend a tiny bit further laterally: this is why some of the stromatolite mounds are wider at the top than at the base. Naturally, the ‘blue greens’ are only able to grow in the sunlight that gives them nourishment, and are quiescent at night. Some scientists at the University of California even claim to have recognised daily growth increments. The overall rate of growth is extraordinarily slow, however, and certainly less than 1 mm a year (and possibly as little as 0.3 mm). It has been stated that some of the Hamelin Pool structures could be a thousand years old, that is, they grow more slowly than the slowest-growing conifer on land. The life and death of the wool industry would register as no more than a hand-depth on the height of a stromatolite column. Time can be ticked out in microscopic laminations, and history reduced to a measuring stick made by timekeepers invisible to the naked eye.
Stromatolites vary in form according to where they are found on the shore. It is easy for me to see that ones at the edge of the sea are little more than pimply mats. At least to this unschooled observer, some of them superficially do not look very different from some of the mats that covered sediment surfaces in the Precambrian at Mistaken Point. They are made particularly by one of the spherical, or coccoidal types called Entophysalis, and the internal layering is not well developed. Further down the shore in Hamelin Pool the stromatolites that I tentatively touched represent the dominant kind in the intertidal zone, with a typical columnar-cushion shape. This kind of column is constructed particularly by a filamentous cyanobacterium called Schizothrix, which under the microscope is an intense emerald-green colour. It has lots of apparent partitions that make the organism look something like an old-fashioned tube of circular cough sweets. These particular stromatolites are very well laminated internally, so that the mechanism of being built up layer by layer is particularly patent. It has been proved that the cushions ‘lean’ a little to the north, each component filament attracted preferentially to the sun (but on such a minute scale) in this, the southern hemisphere; the god Ra evidently ruled in the prokaryotic shallows. Further out to sea again, to a depth of a little more than three metres, there live the lumpier, bumpier, lobed, and somewhat rounded stromatolites that are a collaboration of many different microbes. These include cyanobacteria of the genera Microcoleus and Phormidium; the latter is another concatenation of delicately segmented threads, while the former comprises microscopic ‘ropes’ made up of bundles of a kind of entwined green spaghetti. The different species collaborate to grow together, like a confederation of medieval guilds, with each tiny specialist contributing to the function of an integrated community. True algae – diatoms – may chip in as part of the community among the deeper water stromatolites, but this group of eukaryotes probably did not evolve until much later. Beneath the surface skin of the growing mound, bacteria of a different kind from cyanobacteria process waste products and can cope with low, or even no oxygen; they are like artisans that moved the dung from the streets of the medieval village and made it a trade. Life encouraged specialised habits and habitats from the first.
Stromatolites are the most ancient organic structures, and their recognition as fossils transformed the way we understood the endurance of life on earth and the evolution of its atmosphere. I admit that viewed with complete impartiality when it comes to visual impact, the Shark Bay mounds are not on a par with the Empire State Building or the pyramid of Cheops. But stromatolites are one of the wonders of the world. Rationalists are not permitted to have shrines, but if they were then Shark Bay, where stromatolites were discovered alive, might be high on the list. Although many more living stromatolites have since been discovered, those in Shark Bay have been most thoroughly studied. From their initial recognition in 1954 the fame of these living stromatolites spread, until by the late 1960s they were finding a place in textbooks. As so often happens in science, the discovery of these living mounds happened just when palaeontologists were making major finds of microscopic fossils in rocks of Precambrian age, opening up debates about the biological history of the earth. The strange creatures of the Ediacaran, like Fractofusus and Charniodiscus, took the record of life back tens of millions of years before the great burst of familiar fossils such as trilobites that appeared in the Cambrian, 542 million years ago. But there remained more than three billion years of the history of life on earth in the Precambrian still to account for. This was the era of the stromatolites.
It is necessary to have a digression on geological time at this point. The age of the earth had been established at close to 4.5 billion years by the time Shark Bay was becoming known to the scientific world. The precision of this figure was largely a consequence of refinements in dating techniques, using the slow radioactive decay of naturally-occurring uranium isotopes into other isotopes of lead: turning rocks into clocks, one could say. The samples collected from the moon by the Apollo Mission were first unpacked on 25 July 1969. I recall the excitement of seeing a small black piece of the earth’s barren satellite when samples from the collection made on the Sea of Tranquillity were distributed to major museums, including the Natural History Museum in London. Like the stromatolites, it was not so much the thing itself; it was what it implied that made it so special. After the moon rocks were dated using the best technology of the day the question of the antiquity of the green planet to which the moon was partnered was finally laid to rest: 4.55 billion (plus or minus 0.05).
The geological time period before the Cambrian was simply known as Precambrian for more than a century – after all, that is what it undoubtedly was, ‘before the Cambrian’. But when this time period was recognised as so vastly long, it became necessary to divide it into several named chunks to help us order events in the earth’s history. The Archaean Era is that part of deep geological time that ends at 2500 million years ago, or 2.5 billion years if you prefer. After this came the Proterozoic Era which, in terms of strata, lies above it and extends to the base of the Cambrian Period 542 million years ago (the Cambrian is the first subdivision of the Palaeozoic Era).
The Ediacaran, the latest addition to the roll call of geological time, begins at 635 million years ago and is slotted into the top of the Proterozoic. The Proterozoic Period covers a very long period, and these days is usually divided into three which used to be known as Lower, Middle and Upper, but are now formally known as Palaeo-, Meso- and Neoproterozoic respectively. The Neoproterozoic begins arbitrarily at 1000 million years ago, and the Mesoproterozoic at 1600 million years ago (1.6 billion), so the Palaeoproterozoic occupies the time period 2.5–1.6 billion years ago. Names really do help us get a grasp on the immensity of geological time, though phrases like ‘Palaeoproterozoic digitate columnar stromatolites’ do not exactly trip off the tongue. But it is as well to get our labelling sorted out.
This modern classification is the end point of a long scientific battle. The intellectual classes had been debating the question of the age of the earth since the Comte de Buffon’s estimate of 75,000 years in 1774 based upon the idea of the planet cooling down from a molten state. Apart from a purblind few who insisted (and indeed still insist) upon a biblical timescale based on totting up the generations mentioned in the Bible – Bishop Ussher’s 4004 BC estimate for the Creation – the time available to ‘evolve’ the earth increased fitfully throughout the early days of geology as a science. The bolder savants soon speculated in more and more millions. The longer time got, the more questions were raised about life’s early days, because of the apparent absence of ‘organic remains’ in Precambrian rocks. Charles Darwin famously fretted about it. Geologists of his time were beginning to explore large areas of the world comprised of Precambrian strata as the rocks of countries such as Canada were mapped for the first time. It was soon evident that sedimentary rocks, much like those found in younger geological formations, were widespread over these ancient lands. The seas were apparently barren in these ancient worlds; seas not so different in their physical properties from those that gave succour to the trilobites and snails that could be so easily collected from younger strata. In 1883 the American palaeontologist James Hall found some intensely layered Precambrian rocks apparently ‘growing’ upwards incrementally from a narrower base to which he gave the name Cryptozoon (‘hidden life’); however, their organic nature still remained controversial. Nonetheless, with the mere application of a scientific name, the biological virginity of the Precambrian had been breached. It was time for the stromatolites to be recognised as organic constructions.
The first time I saw fossil stromatolites in the Precambrian was as an undergraduate at the University of Cambridge, when I took part in an expedition to the Arctic island of Spitsbergen in 1967. My doctoral thesis was to be on rocks of Ordovician age exposed along the cold remote shore of Hinlopen Strait on the eastern side of a northerly peninsula called Ny Friesland. The small boat that took us to our field area dodged between ice floes stained with the droppings of countless seabirds, for the Arctic summer is a brief period of plenty for animals that live off the ocean. On land the scenery was bleak: a succession of cobbled beaches raised above the present sea level, across which the occasional polar bear or Arctic fox wandered in search of a feathered snack. It was not an inviting prospect, although it was to be my home for several months. On the way to reach my Ordovician rocks, and before passing the Cambrian strata that lay beneath them, the boat had to chug past a great thickness of even older Proterozoic limestone and shale, piled up layer on layer. There are few places in the world where a young scientist can cruise through such a momentous stretch of geological time, let alone along an outcrop that has survived so unaltered by subsequent earth movements. These ancient rocks were in almost pristine condition. On one occasion we landed to make a temporary camp and pick up fresh water. I wandered over to the nearby rock outcrop just to have a look. The rocks were not horizontal; instead they had been tipped gently (but less so than the rocks at Mistaken Point). I could easily make out the flat bedding planes breaking up the shore into a series of steps that recorded a succession of former sea floors. The rocks were a mixture. Most were very pale grey, sometimes almost pearly, and hard looking. Others were yellowish, in patches somewhat sugary and brightly tinted. The latter were dolomites, a calcium magnesium carbonate rock that at the present day particularly forms in areas surrounding the more arid tropical regions. The off-white rocks were limestones, that is, made of calcium carbonate in a finely crystalline form. Looking closely, I could now observe that several of the limestone surfaces were finely scored. Many years of erosion had picked out subtle differences in hardness within a single bed of limestone, so that lines even a millimetre or so apart could be clearly discerned. A comparison with layered pastry came to mind. I imagine that a blind man could have read the rock surface like Braille, just by gentle palpation. Where the rock surface was weathered at right angles to the bedding surface, providing a natural cross section, these finely-layered rocks were arranged in a series of undulating columns, widening a little from their base. They were stromatolites, or to be more accurate, sections through stromatolites – with a thousand years or more of slow growth preserved in a fossil grave of fine limestone. Cryptozoon proved to be not so cryptic after all; it was the stony legacy of cyanobacteria. When I followed the stromatolites over onto the bedding plane beyond to get a vision of the ancient sea floor, they converted into balloons or pillows stretching away from me, each one showing the top of a stromatolite head. This was the fossilised version of the view at Shark Bay I was to admire decades later. It was bleached to white limestone by the passage of a thousand million years, perhaps, but it was still recognisable, a picture petrified from a former earth. This was the nearest thing I will ever experience to being in a time machine, even if my appreciation of it were countermanded at once by the shrill cries of Arctic terns above my head: chicks to feed, human business to be done, and the earth has moved on. Nothing remains exactly the same forever.
Had I looked more widely along that unwelcoming shore I would have observed a greater variety of shapes carrying the telltale laminations of stromatolites. I would also have noticed some occasional shiny black patches within them; these are made of chert, a very hard, flinty rock composed of the mineral silica. Andrew Knoll, who is perhaps the doyen of Precambrian palaeontology, visited the same rocks in Spitsbergen a few years later, as he has described in his book Life on a Young Planet. From those cherts he recovered remarkable small fossils, which helped to make his reputation. He also recorded a whole range of different rock types produced by ancient micro-organisms; the most general term for these rocks is ‘microbialites’ which is a term that I trust does not require further explanation. Subtly mottled microbialites can present the appearance of ornamental marble, or the interior of a sponge cake, or the dimpled mats that I saw on Shark Bay; they can all be attributed to the work of bacteria and their relatives. Evidently, ancient microscopic communities did not just manufacture columns, though these do display several different shapes. Over much of the vast compass of Precambrian time it was a dominantly microbial world, and there was nothing to prevent tiny organisms from constructing a variety of edifices.
Stromatolite fossils are not at all rare if the right rocks are explored. It is not surprising that many rocks have been altered by heat or pressure if they have sojourned on the earth for billions of years. The great motor of plate tectonics has been continuously in operation, building mountains and moving continents around. It is a lucky rock that escapes unscathed. Most of those that have successfully dodged being crunched or heated up are found around the edges of the most ancient and stable continental cores often known as ‘shields’. These bits of earth’s crust stabilised early on, and have been pushed around the earth during successive phases of continent building rather like counters being shoved around a draughts board. They survive to play another game. If there are patches of stromatolites preserved upon them, they are handed onwards. Perhaps the Canadian Shield is the best known of these ancient areas, but parts of southern Africa and Western Australia are equally familiar to geologists. However, the list of stromatolite occurrences is much longer than that of ancient shield areas, the rocks Andrew Knoll and I examined in Spitsbergen being a case in point. It is obvious that these strange organic structures were almost ubiquitous at least in the shallower parts of ancient oceans. Cyanobacteria would have needed light to grow, so the particular stromatolitic structures made by them must have been confined to comparatively shallow water. The early Precambrian ocean depths are unknown to us, since ocean floors are consumed in the inexorable slow dance of the plates. But it is more than likely that there, too, were structures made by different bacteria that flourished away from light. After all, life never misses a trick.
Stromatolites are found way back into the Archaean. The oldest ones of all are almost miraculous survivors found on the scraps remaining today of the most ancient continents. Fossils dated at 3.5 billion years old have been found in the Apex Chert in Western Australia,
and in Swaziland. It is hardly possible to imagine such antiquity. I have the same trouble trying to grasp the number of stars in the Milky Way, for the mind soon loses its normal frame of reference when the figures get so large. I can probably do no better than echo the words of the pioneer geologist John Playfair in 1788, when he became convinced of the reality of the vast age of the earth: ‘the mind seemed to grow giddy looking so far into the abyss of time’. Nonetheless, it is important to at least get a feeling for this ‘abyss’, an intuition of its magnitude, because it shows just how long it has taken for life to arrive where it is today. The two stories of life, and the earth itself, have been intimately intertwined for billions of years.
Stromatolites began in the Archaean as relatively simple domes, but later they evolved into a number of different forms. Some of the more distinctive shapes have been dubbed with Latin names, just as if they were organisms in the conventional sense (Pilbaria perplexa and the like). As we have seen, they are actually collaborations between several organisms, so such an approach does not fit in with normal biological procedure. However, it is useful to have a way to refer to different shapes and forms, and some of the names have achieved wide currency. In the far reaches of the Precambrian, stromatolites could grow in a wider range of marine environments than they do now, and this may partly account for some of their different shapes. In deeper or calmer water, for example, it was possible for relatively delicate, branching, even candelabra-like forms to grow. In complete contrast, one of the most distinctive varieties produced massive cone-shaped bodies that could grow to be tens of metres high. These microbial behemoths have received the appropriate name Conophyton (‘cone plant’). They have been memorably described as making outcrops in the field look like a series of rocket launchers placed side by side: they must have taken many centuries, even millennia, to grow. The vocabulary used to describe different kinds of stromatolites gives some indication of their variety of form; they have been compared with fingers, fists, cauliflowers, columns, spindles, trees, mushrooms, kidneys. Given time enough these most simple organisms could produce an art gallery’s worth of shapes. Nature was patently a sculptor from the first. The view from Hamelin Pool was, it now transpires, only a partial glimpse of a richer, but now vanished stromatolitic world.
The controls on stromatolite growth were probably quite simple. The growing surface film was attracted towards the sun, while the supply of calcium carbonate from seawater dictated the dimensions of the layers produced. A group of Australian physicists have developed computer models that ‘grow’ stromatolites by playing around with these simple elements. Conophyton emerges naturally as a shape in response to strong solar attraction; prokaryotic life, it seems, simply could not help building regular structures. Where there’s life there’s architecture. But there is also good evidence that the variety and complexity of stromatolites increased during their extraordinarily long tenure of the earth’s seas. The few kinds of simple domes and cones that dominated their first billion years, during the Archaean, were supplemented by dozens of additional shapes during the Proterozoic, when branched structures and pleated columns on many different scales appeared. The first occurrence of particular stromatolites has even been used broadly to subdivide this long period of time. They probably achieved their greatest variety about a thousand million years ago, but still long before the emergence of large animals, even the strange Ediacaran ones. Many early stromatolites were fully submarine, rather than living between the tides. Their living analogues have been found in the Bahamas near Exuma Island, hidden in marine channels. Here, these large, lumpy columns rising from a lime-mud sea floor probably provide a closer match to many Proterozoic environments than does Shark Bay. The biofilm forming the living skin is known to be a complex microbial community, and much more than just a photosynthesising surface. Several other kinds of bacteria have their homes there, some with the capacity to ‘fix’ nitrogen, like the little nodules harbouring bacteria that grow on the roots of beans and contribute to soil fertility. These kinds of bacteria work at night, when the cyanobacteria are ‘sleeping’. Once again, the mat is a whole ecology, a world measured in millimetres.
As for the fossils of the organisms that made the Precambrian mounds, the apparent absence of which so perplexed Charles Darwin and his contemporaries, well, they were lurking there all the time; it is just that they were very small. The cherts, like those tucked among the limestone rocks on Spitsbergen, held the secret. In some cases such siliceous rocks were formed early enough to petrify the fine threads and other cells making up the ancient biofilm. The process is somewhat analogous to that involved in making artificial resin souvenirs in which butterflies or scorpions are preserved, colour and all, which then lurk on the mantelpiece forever. Silica petrifactions were already well known from higher in the geological column, even preserving tree trunks down to the last cell. Considering that the dimensions of the Precambrian fossils are often measured in a few thousandths of a millimetre, the preservation of their cell walls is remarkable, almost miraculous. However, when very thin sections were made of the right Precambrian cherts they became transparent; these preparations were then examined under the microscope and revealed the unmistakeable imprint of life. The discovery was reported in detail in 1965 by the resplendently named American scientist Elso Sterrenberg Barghoorn Jr based on fossils obtained from the Gunflint Chert, a rock formation exposed along the northern shores of Lake Superior. Barghoorn’s co-author, Stanley Tyler, had previously recognised fossil stromatolites preserved in rather beautiful red jaspers (an iron-rich form of silica). At the edge of the Canadian Shield, the Gunflint Chert was one of those special survivors that had escaped the subsequent adventures of our mobile planet, fortuitously frozen in its own ancient time. At 1.9 billion years old, the fossils of the Gunflint Chert lie well down in the Palaeoproterozoic. Among the organic remains seen in thin sections of the chert, the commonest are probably thin threads not unlike those so abundant in living mats and biofilms. Some of these show the kind of transverse striping that are typical of some ‘blue greens’; interestingly, the threads are narrower than they were later in the Precambrian (and narrower still than they are today). They are accompanied by a range of other tiny organisms, some generalised rod-like bacteria, others more distinctive, like the spherical Eosphaeria with its cell walls apparently divided into compartments, and the enigmatic Gunflintia. Palaeontologists continue to argue about the biological identity of some of these fossils, although it is beyond doubt that ‘blue greens’ were certainly present among them, but the important point is surely that this is an early community, already divided into different biological ‘trades’. The kind of prokaryote collaboration happening today was already happening then. Stromatolites were indeed true survivors.
But back in the 1960s, the fossil search was on! The world was scoured for younger, older, similar or, in particular, new and unnamed Precambrian small fossils. Africa, especially Namibia and Swaziland, was mapped and investigated; Australia, especially Western Australia, was crawled over; the Old World was looked at again, and much of the New World was looked at with new eyes. Precambrian fossils turned out to be very widespread, and new discoveries were nearly always heralded by someone spotting stromatolites in the field, which hinted at what might yet be found at the microscopic scale. Geologists’ boots tramped up wadis in deserts, their hammers whacked at Arctic cliffs, and their hand lenses focused on limestones outcropping deep in the Siberian taiga. These last devoted geologists bore the scars of marauding mosquitoes for weeks. Then by dissolving Precambrian shale in hydrofluoric acid still other microfossils with organic walls were extracted, to be studied in detail on microscope slides. University departments hired staff, and the growth in knowledge was exponential. Many of the famous names in early evolution were students of, or collaborated with, Elso Barghoorn. Andrew Knoll was among them. Bill Schopf, an equally grand figure at the University of California, Los Angeles, is now the elder statesman of the Barghoorn disciples, and did much to push the record of life and its fossils further back, into the Archaean.
Lynn Margulis may be the most luminous name of all those scientists associated with Barghoorn. She espoused and championed an idea that has transformed our way of understanding the history of life. There is a lot of hype in science nowadays, the more so since big claims often result in further research funding. I have never heard anybody announce ‘a minor discovery’ or ‘a modest advance’. I have also become allergic to the media’s phrase ‘the textbooks will have to be rewritten’ since it conjures up an inaccurate vision of textbooks being hurled with a curse into the waste paper basket on a regular basis. Textbooks are rewritten, but most scientific discoveries are passed from one edition to another, since science generally works by piling bricks of knowledge one on another to make a solid edifice. It is very unusual to scrap a whole chapter and start again. However, this does happen on occasion, and one such occasion was when it was claimed that eukaryote cells originated by a kind of piracy. The vital organelles within eukaryotic cells – things like mitochondria and chloroplasts – were originally free-living prokaryotes. The more complex cell was a result of a hijack, whereby former free-living bacteria were summarily tucked away inside the swag bag of a bigger descendant cell. Unlike the human hijack, though, all parties benefited: the scientific term is symbiosis. The formerly ‘free’ bacteria proliferated in their new habitat, sequestered away from harm. The newly enhanced cells took advantage of the novel vital functions tucked away inside them. For example, in plants the captured chloroplasts concentrated photosynthesis into special sites within the safety of a eukaryotic cell. Plants could now prosper using the energy of the sun. By contrast, mitochondria localise the ‘furnaces’ providing the chemical energy for life, which is essential for organisms to feed and grow. Malfunctions in these organelles are usually lethal, so deeply are they embedded in the ‘works’. Variegated varieties of garden plants can have white patches lacking chloroplasts, but such varieties are selected by gardeners for their appearance, not by nature for efficiency. Such an origin for complex cells is called the ‘endosymbiont theory’ – ‘endo’ meaning ‘inside’ symbiosis. Complex cells arose by incorporation of simpler ones, for mutual benefit. It altered our understanding of life’s early history to such an extent that not only had the textbooks to be rewritten, but there also had to be new books to replace the old ones in their entirety. The theory was triumphantly vindicated when the DNA of chloroplasts was investigated and found to be similar to that of free-living photosynthesising prokaryotes. The organelles tucked inside complex cells were, indeed, closely related to free-living, simple prokaryotes. This is the kind of confirmation that most of us can only dream about. It was almost as good as getting into a time machine and travelling back to the Precambrian. The phrase ‘endosymbiotic events’ was soon incorporated into foundation biology classes. Like all science, the story has got much more complicated since the initial insight, as more and more acts of cellular piracy have been detected, but all the complications serve to reveal yet more events deep in geological time.
6. Endosymbiotic/endosymbiont theory: a complex cell ‘in the making’ engulfs a formerly free-living prokaryote, which is then retained as a symbiont rather than being digested. This process happened several times, thereby introducing many more possibilities for life.
I should mention that none of these distinguished scientists conforms to the common preconceptions of the ‘geeky’ white-coated specialist. Bill Schopf is a bon viveur and raconteur, with a very persuasive laugh, and a relentless drive for discovery. Andrew Knoll is the kind of American who makes most of us poor Europeans feel as if we were only given half a ration of energy at birth. He has projects spanning most of the world, and a stable of exceptional students to take the work forward. He manages everything with a kind of urbane good humour and insouciance that defuses any possible resentment at his omniscience. Lynn Margulis is unique. I know of no other professor who would, or indeed could, quote the poet Emily Dickinson at length in a supermarket. As a long-term maverick she is always on the look out for ideas that will provoke and encourage new ideas (and completely undeterred that some of them may well prove to be wrong). Her dress style is equally distinctive, featuring embroidered waistcoats and pleated skirts, as if she were about to take part in a folk festival. She has an intuitive grasp of the important collaborations that makes the world work; not just the ubiquitous and versatile bacteria, but also chemistry, and geology, and politics.
This account of the geological importance of stromatolites and their discoverers has entailed a distraction from the little bubbles that provide the nub of this chapter. Recall the tiny gas beads rising from the top of the stromatolite in its tank, arising from a living biofilm breathing out oxygen. Now combine that scene with the picture I have attempted to paint of the fledgling earth in the Archaean and Proterozoic, where shallow seas and lagoons were covered with stromatolites, some of them gargantuan by recent standards. Imagine thousands and thousands of dimpled miles, exhaling oxygen by day in a thousand billion tiny bubbles, stimulated by the primeval sunshine. Even the slimy surface of the threads had a part to play in mitigating the effects of harmful ultra-violet radiation; we should all be grateful to slime. Now imagine this process continuing for billions of years, six times longer than the history of the velvet worm. The effect was to change the atmosphere, bubble by bubble. The early earth had little or no free oxygen; the ‘blue greens’ changed the air itself. Animals need to breathe oxygen to power their life functions. They could not exist before the slow, relentless preparation of the atmosphere effected by lowlier organisms on the tree of life: no gills, no lungs, no blood blue or red. If some malevolent God were instantly to reverse the work of the stromatolites we should all be gasping on the ground like beached trout within minutes. So we are, in a sense, the children of the sticky mounds.
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Richard Fortey
This ebook edition does not include illustrations.An awe-inspiring journey through the eons and across the globe, in search of visible traces of evolution in the living creatures which have survived from earlier times and whose stories speak to us of seminal events in the history of life.The history of life on Earth is far older – and far odder – than many of us realise. In ‘Survivors’, acclaimed author Richard Fortey traces this history not through fossil records, but in the living stories of organisms that have survived nearly unchanged for hundreds of millions of years and whose existence today affords us tantalising glimpses of landscapes long vanished.For evolution has not obliterated its tracks. Scattered across the globe, strange and marvellous plants and animals have survived virtually unchanged since life first began. They range from humble algal mats dating back almost two billion years to hardy musk oxen, which linger as the last vestiges of Ice Age fauna.Following in Fortey’s questing footsteps, ‘Survivors’ takes us on a fascinating journey to these ancient worlds. On a moonlit beach in Delaware where the horseshoe crab shuffles its way through a violent romance, we catch a glimpse of life 450 million years ago, shortly after it diversified on the ocean floor. Along a stretch of Australian coastline, we bear witness to the sights and sounds that would have greeted a Precambrian dawn. Finally, in the dense rainforests of New Zealand where the secretive velvet worm burrows into the rotting timber of the jungle floor, we marvel at a living fossil which has survived unchanged since before the dissolution of the Gondwana supercontinent.Written with Fortey’s customary sparkle and gusto, this wonderfully engrossing exploration of the world’s oldest flora and fauna brilliantly combines the best science writing about the origins of life with an explorer’s sense of adventure and a poet’s wonder at the natural world. Utterly compelling, eye-opening and awe-inspiring, this is a book for anyone with an interest in evolution, in nature, in the remarkable scope of geological time and our own modest interaction with it – in short, in life itself.
Survivors
The Animals and Plants That Time Has Left Behind
Richard Fortey
Dedication
To my sister, with love
Contents
Cover (#ulink_5fb87965-0f72-59fe-895a-79a47af07b06)
Title Page
Dedication
Prologue
Table of Geological Periods
1 Old Horseshoes
2 The Search for the Velvet Worm
3 Slimy Mounds
4 Life in Hot Water
5 An Inveterate Bunch
6 Greenery
7 Of Fishes and Hellbenders
8 Heat in the Blood
9 Islands, Ice
10 Survivors Against the Odds
Epilogue
Picture Section
Glossary
Picture Credits
Further Reading
Searchable Terms
Acknowledgements
Endpaper
Other Books by Richard Fortey
Copyright
About the Publisher
PROLOGUE
These anomalous forms may almost be called living fossils; they have endured to the present day, from having inhabited a confined area, and from having thus been exposed to less severe competition.
CHARLES DARWIN, The Origin of Species
Evolution has not obliterated its tracks as more advanced animals and plants have appeared through geological time. There are, scattered over the globe, organisms and ecologies which still survive from earlier times. These speak to us of seminal events in the history of life. They range from humble algal mats to hardy musk oxen that linger on in the tundra as last vestiges of the Ice Age. The history of life can be approached through the fossil record; a narrative of forms that have vanished from the earth. But it can also be understood through its survivors, the animals and plants that time has left behind. My intention is to visit these organisms in the field, to take the reader on a journey to the exotic, or even everyday, places where they live. There will be landscapes to evoke, boulders to turn over, seas to paddle in. I shall describe the animals and plants in their natural habitat, and explain why they are important in understanding pivotal points in evolutionary history. So it will be a journey through time, as well as around the globe.
I have always thought of myself as a naturalist first, and a palaeontologist second, although I cannot deny that I have spent most of my life looking at thoroughly dead creatures. This book is something of a departure for me, with the focus switched to living organisms that help reveal the tree of life (see endpapers). I will frequently return to considering fossils to show how my chosen creatures root back into ancient times. I have also broken my usual rules of narrative. The logical place to start is at the beginning, which in this case would mean with the oldest and most primitive organisms. Or I could start with the present and work backwards, as in Richard Dawkins’ The Ancestor’s Tale. Instead, I have opted to start somewhere in the middle. This is not perversity on my part. It seemed appropriate to start my exploration in a place, biologically speaking, that is familiar to me. The ancient horseshoe crabs of Delaware Bay were somehow fitting, not least on account of their trilobite connections. Amid all the concern about climate change and extinction, it is encouraging to begin with an organism whose populations can still be counted in their millions. From this starting point somewhere inside the great and spreading tree of life I can climb upwards to higher twigs if I wish, or maybe even delve downwards to find the trunk. Let us begin to explore.
TABLE OF GEOLOGICAL PERIODS
1
Old Horseshoes
Turn seawards off Route 1, Delaware, and a century rolls away. A small road soon leaves the commercial strip and the fast food joints behind, as it moves onto flat fields and marshland that still supports scattered, pretty villages lined with white-painted picket fences. This is how much of America’s east coast used to be. The Little Creek Inn is a grander building altogether: a large, foursquare, wooden Victorian farmstead on three floors with shutters at the windows and a fine portico, and inside all polished wood and turned banisters. In the spacious drawing room of the Inn, anticipation is buzzing. The hosts, Bob and Carol Thomas, are serving iced tea to a crew of enthusiasts all dedicated to travelling back much further in time than a mere century or so. This is the chance to come face to face with life as it was millions of years ago. Glenn Gauvry, the local expert, is waving around models of an ancient animal. A small TV crew is there to straighten out their facts before they get down to filming. Two young women biologists have travelled from Canada to see for themselves an event that only happens when the conditions are just right in late May. I am there with my notebook and a fluttering heart. All of us are impatient for darkness to fall.
Deep in the night along the shores of Delaware Bay the horseshoe crabs are stirring. The tide is now high and there is no moon. Darkness rules, but even in the feeble starlight the overwhelming flatness of the countryside can be made out, except along the rim of the bay where old sand dunes have built up a levee providing foundations for a scattering of wooden beach houses, which loom against the night sky. A path passes between them onto a sandy beach that stretches away into the darkness in a long gentle arc. The shoreline seems to heave with gentle movements.
First, I notice some very odd sounds. There is a general hollow clattering, a tapping and grinding sound, somewhat like that made by knocking coconut shells together (once used on the radio to imitate horses’ hooves) but altogether less rhythmic, and with a kind of underlying push. Then, as my eyes get used to the darkness, low shelly mounds the size of inverted colanders can be seen slowly pushing and jostling all along the shore and perhaps six metres up onto the sands. Their bumping and clambering together is the source of those tap-tapping percussive sounds. The flash of an infrared torch reveals more details. The head-shield of the horseshoe crab is domed upwards and carries a few weak spines; at its back end a hinge marks a jointed boundary with a second large plate, spiny at the edge, which can flap downwards; and beyond that again projects a stout triangular spike as long as the head, which can waggle up and down. Here at Kitt’s Hummock more crabs are gathered on the mud flats seaward of the sands waiting their turn: strange, green-black, slowly animated lumps. Further offshore again in the shallow seawater tail spikes project briefly above the gentle waves like raised radio antennae and are gone, showing where still more horseshoe crabs vie with one another to get their place on the sand. There are evidently thousands upon thousands of these large animals gathered together in some sort of compulsive collusion.
One horseshoe crab lies upturned on the sand. Its tail spike waggles feebly, quite unable to perform the task of turning the body back over again. Five pairs of legs twitch ineffectually in a vain attempt to achieve the same end. I find it impossible to resist the temptation to right the poor animal. It is easy to grasp it by the edges of the head-shield. Once righted again those spindly legs allow the crab to trundle slowly away. Its behaviour seems at once strangely determined, but also apparently random, like the slow progress of a confused old lady on a Zimmer frame.
Now I see that many of the largest crabs are digging in the sand, their limbs working away beneath the carapace. Some have become almost completely buried, and, although I can detect a kind of deep scrabbling from these animals, they do not seem to be worried by their self-inflicted interment. Other slightly smaller crabs crowd on top of the buried animals. The scrabblers are the females of the species burying their eggs in the sand, while the smaller ones on top are males, competing to fertilise the eggs with their sperm (milt). I realise that there is some kind of order to the apparent mayhem on the beach. A proportion of the horseshoe crabs are paired off, with the lighter male desperately hanging off the tail end of the female, having got a purchase by using his special claspers. However, this right of occupation does not deter other males from having a go at mounting the same burdened female. There is enough of a gap behind the head-shield for some of their interloping milt to have a chance. Much of the clinking noise is a consequence of tussles for dominance. So this gathering of crabs is really an orgy, and an orgy that runs for dozens of miles along the strand, all thickly bordered with scrabbling, lustful animals. As for the poor exhausted females, gravid and overprovided with mates, the moist sand stops their gills drying out, and they may eventually struggle back to the sea when the laying is done – although many do not. Bits and pieces of their carcasses litter the shore.
I have a better chance to scrutinise the horseshoe crabs closely during the day, although most of them have returned to the sea by sunrise. Coastal Delaware is a land of marshes, with gentle wetlands dominated by the reed, Phragmites, and the cries of wading birds always in the wind. The landscape reminds me of the East Anglian coast in England. Creeks wind their ways inland from the sea, and terminate in small picturesque harbours like Leipsic, where a few fishing boats are tied up to stout piers, with white-painted clapperboard houses landward of the stage. Sambo’s is a restaurant with a view of the creek, and well known for its edible crabs, which are consumed on simple tables covered with newspapers. Eating in Sambo’s is an audible experience with everybody bashing lunch out from shells. It is a place of crunching and squishing and little conversation. Some of the shucked piles are prodigious. There is nothing on the menu about horseshoe crabs. The nearby villages of no more than one or two streets include neat little houses dating back to the 1880s, which is ancient by American standards. Delaware car number plates bear the legend ‘The first state’, acknowledging the fact that it was the first to sign up to the Declaration of Independence. Like several other early American states, but unlike the majority, it is tiny. Nowadays, vehicles on the main roads shoot past; but a mile or two from the freeways little has changed from post-colonial days. I warmed to it immediately.
After the crustaceous lunch, a visit to Port Mahon shows a few stragglers still on the beach at midday, providing a chance to get close. A large female’s carapace is about 45 cm across. In the sunlight I can readily see that the creature has nearly semicircular eyes set to either side in the midst of the head-shield, topped by sharp spines, rather like the perky eyebrows I associate with clerics of a certain age. Under high magnification it would be apparent that the eyes are composed of many tiny lenses – they are what are known as compound eyes, similar to those of houseflies or bees. The whole animal is a dull pinkish-to greenish-grey colour, the kind of colour I used to get as a kid when I mixed all my powder paints together. The front of the head-shield is subtly bowed upwards about the middle. The tail (or telson) has a triangular cross section, and it makes a stoutly elegant termination to the animal. The middle part of the body is defined on its top surface as a kind of convex median lobe over about half its length: this is where the muscles that power the legs are lodged. The leading edge of the head-shield is thickened into a prominent marginal rim that is prolonged backwards into short spines; this part of the body needs to be strong to butt into the sands and mud that line the floor of Delaware Bay. On the shore there are several beached crabs lying on their backs, waving their legs at the sky. They bend almost double along their middle hinges, but their best efforts still fail to turn them over (it would be different under water). If they remained on their backs, greater black-backed gulls would soon come along to peck them to pieces. Before setting them aright, I have a chance to see how delicately each of the paired jointed limbs under the head-shield carries a set of pincers at its tip. I am reminded of the manual toolkit owned by the eponymous hero of the movie Edward Scissorhands. They are indeed picky little tools. Nearer the front end of the head-shield, where the carapace is doubled back from the top surface into a blunt point, a very delicate set of pincers at the centre of the animal and close to the mouth, looks just the thing to feed titbits towards the innards. The bases of the legs are really quite stout and equipped with blunt spines that face one another along the midline of the animal: they can be used like nutcrackers to crack shellfish if needs be. I begin to understand how these creatures can grab a living from the waters of Delaware Bay. Behind the legs are a few pairs of flattish flaps that cover up intricately folded book lungs. Like every marine animal the horseshoe crab needs to breathe dissolved oxygen, and as long as this breathing apparatus can be kept moist under its protective covers the crab can survive on land. Hence the female can endure her risky excursion to lay her eggs in the sand. The shore may be an unwelcoming nursery, but might still be preferable to a sea where every cubic metre holds a thousand twitching antennae sensing free food. It is time to turn our crab over to allow it to trundle away. It heaves itself along like a battered tank: slowly and undignified, as if to signal ‘I have survived endless battles, and survival is all’. As it performs its lurching exit to the sea, it leaves a track behind on the muddy sand surface. The paired imprints of the limbs are prominent; even the tips of the pincers leave their doubled marks. And the tail, dragged behind, leaves a groove between, as a child might scribe with a stick clumsily trailed across the strand.
Horseshoe crabs are not really crabs at all; indeed, they are only very distantly related to crabs in so far as both kinds of animals propel themselves through the sea on spindly jointed legs. Animals with useful appendages of this articulated kind are known as arthropods (from the Greek: jointed legs). They are classified together in Phylum Arthropoda, a vast animal group that includes all the living insects, as well as spiders, millipedes, and a host of marine ‘bugs’ of all kinds. Crabs are crustaceans, along with lobsters, shrimps, and woodlice (pillbug to some). Horseshoe crabs are no more crustaceans than are butterflies. They do not have the flexible antennae or ‘feelers’ adapted to sensing the environment that are a common property of Crustacea and insects: these delicate organs both feel and touch, and smell. Instead, in the horseshoe crab the head appendages are modified at the front into a pair of useful pincers, or chelicerae, which I had observed in my stranded animal lying on its back. The significance of this apparently small feature will become apparent. The scientific name of the horseshoe crab is Limulus polyphemus (I shall need to use scientific names throughout this book). By day the beach throngs with feeding wading birds: thousands of them skitter nervously away from human intruders in animated, piping, fluttering waves, always beyond reach. Like most waders, many of them are dressed in shades of brown and grey, but the different statures of several species are obvious even to an inexperienced birdwatcher. Small, short-billed sandpipers throng on short legs; slightly larger pale-bellied sanderlings dash along the water’s edge; taller, long-billed dowitchers elegantly stride among them. The iconic species for the area is the red knot, which has a dramatic cinnamon-coloured belly when in breeding plumage. All wader species – and there are many more in the crowd – are united in rapt attention along the shoreline, pecking and probing incessantly at the ground, like chickens fed in a yard on the best grain. They are undoing the work of all those heaving masses of horseshoe crabs the previous night, gorging on the green, millet-seed-sized eggs the female crabs sought to sequester beneath the sand. For the red knot the eggs provide vital refuelling, as this particular population started its migration near the tip of South America. By the time they arrive in Delaware Bay on their way to the Arctic the birds may have lost half their bodyweight and they are starving. The crab eggs must taste like the best caviar. The birds would not survive without those countless horseshoe crabs performing their spectacular mass mating ritual. These inelegant invertebrates are completely unaware of the gift they are providing to an animal many millions of years their evolutionary junior.
Birds always attract devotees, and naturalists’ concerns for the welfare of the red knot probably accounts in turn for their anxiety about the state of the horseshoe crab population. If that were to fail, then so would the long migration of the attractive waders. A recent census estimated that there could be as many as seventeen million horseshoe crabs in the Delaware Bay area, and that concerns about their decline may have been exaggerated. Since the horseshoe crab has a range that extends along the shore north to Maine and south to the Yucatán Peninsula in Mexico the population is assuredly larger still, although the densest concentration of individuals is probably where I saw the heaving multitudes at Kitt’s Hummock and Pickering Beach. Delaware Bay is also where the mature crabs grow largest at maturity. Since there has, indeed, been a decline in red knot numbers the cause must lie somewhere else in its complex migration story. The weakest link in an ecological chain is always the critical one.
It had always been a dream of mine to see throngs of jostling horseshoe crabs reach the climax of their life cycle. For more than three decades at the Natural History Museum in London I studied fossils of trilobites. This once important group of sea animals went extinct something like 260 million years ago, when the world was a very different place. Trilobites had once swarmed in all the ancient oceans, but now their remains have to be patiently collected by splitting open the rocks that have entombed their shelly remains. Like horseshoe crabs, trilobites are arthropods: animals with jointed legs and all the muscles and tendons tucked inside an exoskeleton. However, unlike horseshoe crabs, trilobites did not survive the mass extinctions that redesigned the biological face of our planet. It is astonishing to learn from unchallenged fossil evidence that relatives of Limulus were contemporaries of trilobites. That nocturnal scrimmage on the beach in Delaware might have happened many millions of years before; I might even have been listening to sounds that had been rehearsed in Palaeozoic times. There were relatives of the horseshoe crabs in the sea long before other arthropods, such as insects and spiders, had ventured onto land, or before crustaceans – shrimps, crabs and lobsters – had taken up the central roles in the ecology of the ocean they enjoy today. So it would not be incorrect to describe the animals thronging along Delaware Bay as primeval. Indeed, many scientists believe that Limulus is the closest living relative of trilobites themselves. Would the head-shield of the giant Cambrian trilobite Paradoxides, a fossil 510 million years old, have felt the same to the touch as the beached Limulus I restored to the sea in eastern America early in the twenty-first century? Like a horseshoe crab, a trilobite would surely have contemplated me through compound eyes set within its head-shield; its eyes are preserved in detail as fossils. Trilobite legs would have scraped against my mammal flesh with just the same spikiness as Limulus. It would have crept and it would have crawled, brother under its external skin to the hordes on Delaware Bay.
1. A Silurian trilobite, Calymene blumenbachii, from the limestone quarries of Dudley, West Midlands, England.
So a visit to Delaware is to me rather like a visit to the holy city of Rome to a Catholic. Naturally, I had to meet the Pope. The Pontiff of horseshoe crabs is Carl Shuster, in his tenth decade still a giant of a man: craggy faced, walking without the aid of a stick, with lively eyes beneath towering eyebrows, memory and curiosity undimmed, and only betraying his years by his deafness. Like all field biologists he wears a coarsely chequered thick shirt and blue jeans, hitched up with a stout belt. He was brought up during the Great Depression, when he had to run a farm, so he is himself a survivor, like the horseshoe crabs to which he has devoted his life. His father was a mathematician who gave succour to penniless intellectuals during the tough years, while young Carl raised asparagus, chickens and strawberries. He brought together all the current knowledge about his favourite animal in his book The American Horseshoe Crab. He is accompanied in Delaware by his former student, a man of boundless enthusiasm, Glenn Gauvry (himself an implausibly youthful sixty years), who coordinates much of the research on Limulus around the Bay area. Those volunteers who help with counting the crabs during their nocturnal orgies receive a handsome little pewter lapel pin as a record of their collaboration in the conservation project. Naturally, the pin features a horseshoe crab. It signifies membership of one of the more exclusive clubs in the world.
Carl Shuster and his colleagues established the biological facts about horseshoe crabs that allow naturalists to understand how they fit into the ecology of the Atlantic coast. Limulus is a typical arthropod in that it must moult in order to grow, shedding its old coat as a kind of pale ghost of its former self, and growing a new and larger external covering. With a little vigilance it is possible to find one of the cast ‘shells’ on the beach: they are almost as light as tissue paper, for the animal recycles what it can. The newly emerged horseshoe crab is capable of moving immediately. In this it has the advantage over other marine arthropods in the area; freshly moulted blue crabs, for example, are virtually motionless until their new ‘shell’ hardens. They often hide away. Younger horseshoes resemble the older ones apart from being a little spinier. The surprisingly tough, but flexible exoskeleton is made of a chitinous material, similar to that forming the wings of beetles. A typical horseshoe crab takes ten years to reach sexual maturity, after which it does not moult again, but heads to the beach for reproduction. Only these mature animals partake in the littoral orgy, which is why one does not see any little limulids scuttling between the adults. They are not demanding animals: a fully mature animal might go for months without eating. When her time comes, a female may well lay 80–100,000 eggs, and enough of these survive the depredations of wading birds to secure the future generations. The greenish eggs are laid in the sand in batches of four to six thousand in spheres about the size of a golf ball; the female makes repeated visits on successive tides to complete her duties. Females can be recognised by the scars left behind by the mounting males: up to fifteen males may have a chance of fertilising the eggs of any female. Nonetheless, only about thirty-three eggs out of a million survive to adulthood. This means that at various stages of its life Limulus provides a lot of food for other animals. Loggerhead turtles are an important predator on the crabs, even when they are adults. Turtles, too, are animals with a long geological history, so they may have had eons to make something nutritious out of horseshoe crabs, which now seem all sinew and horn and little enough meat. The crabs themselves can survive on molluscs and carrion and almost any kind of scraps, but the strong inner parts of the legs can also crush thick shells if needs be. Although they seem to lurch in an ungainly way on land, under water the crabs are more streamlined and can move quite fast, even sculling on their backs. They can easily right themselves if they need to. In short, they are tough, jack-of-all-trades kind of creatures, built to last. They remind me in a way of a Volkswagen Beetle that I once owned (a beetle being another arthropod, of course) that carried on carrying on even though its coach-work was full of rusty holes, its suspension was down almost to the tarmac, and it often fired on only three cylinders.
This analogy particularly came to mind when I saw a badly damaged horseshoe crab still trundling gamely onwards, even with a great hole punched right through its head. Looking over the beach more carefully there seemed to be a lot of these war veterans: lumps out of the thorax, broken tail spikes – clearly, it must take a lot to finish these creatures off. Glenn Gauvry pointed out to me what a great advantage for reproductive success this resilience would furnish. Such endurance is possible because the blood of Limulus polyphemus has exceptional clotting powers; the animal does not bleed to death because its blood coagulates and ‘walls off’ damaged areas. And the blood is blue. Does not the horseshoe crab begin to seem ‘curiouser and curiouser’, as Alice would have said? The blood of Limulus is blue because it is fundamentally different from that flowing in red-blooded creatures, like you and I and the kangaroo. Whereas we have haemoglobin as our oxygen-carrying pigment, which includes the element iron as an indispensable component, the horseshoe crab carries a copper-based molecule called haemocyanin to do a similar job. In nature, copper often comes with such a blue colour tag. The molecular structure of both these vital molecules is now known in detail, as is the way they move oxygen through the tissues, although this is not directly part of our story. But the Limulus narrative would not be complete without exploring the extraordinary coagulating properties of its blood a little further, because this affects the very survival of the species.
This discovery was made in 1956 by Fred Bang of the Marine Biological Laboratory at Woods Hole. He noticed how Limulus blood clotted dramatically when infected by a particular bacterium. Subsequent research showed that the crab’s blood had an extraordinary sensitivity to a vast range of micro-organisms that are found almost everywhere in nature – known as gram-negative bacteria. A few cubic centimetres of seawater may contain hundreds of thousands of these tiny organisms. Since some of these bacteria are also agents of disease in humans, this property was of immediate interest. It seems that a hypersensitivity to microbial enemies helps to protect the crabs in their natural habitat – as soon as the bacteria enter a wound their defences were up. Limulus has a very diffuse blood system compared with ours, with the interior of the animal bathed in blood, and lacking the defined circulation of veins, arteries, and capillaries we are used to in humans and other vertebrates. In horseshoe crabs the job of defending the works of the animal is given to one type of protective cell, the amoebocyte, which contains a mass of granules capable of promoting clotting. When a gram-negative bacterium is in its vicinity an amoebocyte will react by rupturing and then the granules are released. A clot follows and the infection is sealed off. Now we know why dented and holed crabs can totter on regardless. They have had hundreds of millions of years to come up with an effective response to some of their most dangerous and invisible enemies.
Twelve years later in 1968, Bang and his colleague Jack Levin had managed to prepare and extract the active principle ‘Limulus amoebocyte lysate’ (known as LAL) that clots human blood plasma when exposed to gram-negative bacteria. This is an extremely useful substance in medical diagnosis, readily used for the detection and measurement of the poisonous toxins (called endotoxins) belonging to the appropriate bacteria. Poisonous endotoxins are released into the host organism (you, me, or a horseshoe crab) when the bacterial cell wall ruptures. LAL is a highly sensitive chemical able to detect minute quantities of the offending substances. The LAL test is now widely applied, having been sold on to pharmaceutical companies for commercial manufacture. It has to be prepared close to the Limulus populations, but is then exported around the world. This means that there is a tremendous demand for the horseshoe crab’s blue blood. What had saved it from harm for millions of years now made it a desirable commodity.
The influence of this new industry has been the subject of some debate. Carl Shuster told me that recent estimates say that there may be as many as seventeen million adult crabs in the Bay. By 2003, some three million crabs were harvested for the pharmaceutical trade – an unsustainable quantity. The bird people were worried about the fate of the red knot and its fellow waders. Now the number has been reduced, and the technique for obtaining blood has been adapted so that it does not require the animals to be killed: they have become blood donors! Four companies have the right to what is called ‘bleed and release’, and this method has been applied to some 600,000 crabs per annum. Maybe it is possible to get the LAL and not threaten the horseshoe crabs, after all. Meanwhile, some ornithologists are sceptical, and feel that the companies, as beneficiaries of the local species, should put something back into safeguarding the regional marine habitat for the benefit of all parties, crabs included. Given the long time taken for the crabs to reach sexual maturity there is always a lag before the effects of a population slide can be observed when the summer high tide hits the beach. But there are certainly some very vigilant people on the case.
There was another threat to the welfare of the horseshoe crabs. They were harvested in great numbers to use as bait to catch the giant marine snail or whelk, known up and down the Atlantic coast as conch (Busycon). Big, pinkish conch shells are a familiar item in every seaside knick-knack shop; put to the ear they allow the listener to ‘hear the sea’. Roadside stalls sell the shells for a modest price in the small villages around Delaware Bay. The molluscs inside the shells have a loyal following among connoisseurs of seafood. The only time I tried them I found the flesh very tough. A crab split in two is a pungent treat for the big snails, however, and fishermen along the coast from Delaware to New Jersey are well aware of the power of this lure. The US Fisheries Commission limited the number of crabs to be used to 100,000 in New Jersey, and later introduced a moratorium, but some fishermen moved northwards to Massachusetts or even Maine (the northern limit of the crabs’ distribution) to continue their trade. A method of sustainable fishing must be worked out, and there are hopeful signs. On Delaware Bay, for example, the use of a different kind of trap employing mesh bags has cut bait use by 50 per cent. One cannot help feeling that the horseshoe crabs deserve to prosper unhindered. There may seem to be endless crowds of them jostling for a space on the sand, but the example of the American passenger pigeon comes to mind: countless millions of the birds were slaughtered in the nineteenth century until the species finally became officially extinct in 1914. How dreadful to contemplate the thought that an animal that has survived in readily recognisable form from the early days of the dinosaurs might become extinct in the cause of being a special garnish on a plate of fruits de mer. It is fortunate that its blue blood is so valuable.
Limulus polyphemus is not alone. There are three additional, Asian species of living horseshoe crabs, but none of them can be found in anything like the profusion of the North American form. Tachypleus tridentatus has been given protected status in Japan, where it lives on the Seto Inland Sea. Its shallow-water habitat there is under threat, and increasing industrialisation on the Seto Sea seems unlikely to spare it. Various attempts have been made to conserve the crab, but none of them has solved the problem of making this ancient animal at home in the modern world. Nonetheless, it has an important place in Japanese history, as its form is believed to have inspired classical samurai masks, and brave warriors were supposed to be reborn in the guise of horseshoe crabs. The contemporary artist Takeshi Yamada has made a modern interpretation of masks based upon the ancient icon. A related species, Tachypleus gigas, is fairly widespread in eastern Asia. I saw the fourth species, Carcinoscorpius rotundicaudatus, while I was on fieldwork in Thailand more than a decade ago. As its second, species name would indicate to those with a smattering of Latin, this particular type has a rounded tail spike compared with other horseshoe crabs. When I first set eyes upon Tachypleus, the poor crab was in one of those tanks in a restaurant where delicacies are displayed before consumption, along with several sad-eyed fishes and a dying lobster. I was puzzled by what there could possibly be to eat on the horseshoe crab, because I knew from dissecting its American relatives that they are not exactly meaty. If the species in the tank was indeed a relative of trilobites this might be my first and last chance to taste something resembling my own speciality. When the cooked item finally arrived I felt a twinge of conscience, for it transpired that large, yolky eggs hidden under the head-shield provided the delicacy, which was only available while the gravid females came inshore. I felt that I was consuming the next generation just to satisfy my curiosity. The eggs came served in a thin sauce on a mountain of noodles. They had a rather overwhelming rancid-fishy taste; I am not anxious to repeat the experience.
2. A growth series of juvenile Tachypleus tridentatus, the Asian species of horseshoe crab, collected from tide strand lines in Deep Bay estuary, Hong Kong. (The scale is a 15 cm/6 in ruler.)
As for the place of the horseshoe crab in the tree of evolution, the Latin name of the horseshoe crab I saw in southern Thailand might offer a clue. Carcinoscorpius means ‘crab scorpion’, and that is what these curious creatures are: superficially crab-like relatives of the scorpions. They are the most primitive living examples of a great group of arthropods that includes all living spiders and mites as well as scorpions, and several less familiar kinds of animals. This group is referred to as chelicerates, after those special appendages – chelicerae – located on the head-shield, which they all share in one form or another. All the relatives of the horseshoe crab I have mentioned live on land. But the cradle of life was the sea, and Limulus and its relatives take us back to the far, far distant days when the land surface was barren of larger organisms.
In the darkness along Delaware Bay the scratching percussion of the crabs provides an unmusical accompaniment on an imaginary journey backwards in time: to an era well before mammals and flowering plants; a time before the acme of giant reptiles, long before Tyrannosaurus; backwards again through an extinction event 250,000,000 years ago that wiped nine-tenths of life from the earth; and then back still further, before a time of lush coal forests to a stage in the earth’s history when the land was stark and life was cradled in the sea; a time when a myriad trilobites scuttled in the mud alongside the forebears of the horseshoe crabs. The trundling, heaving, inelegant not-so-crabs along Delaware Bay are messengers from deep geological time.
A palaeontologist would naturally want to track the history of the horseshoe crabs back into the distant past. A few years ago I visited the famous quarries in Bavaria, southern Germany, where the Solnhofen Limestone of Jurassic age, 150 million years old, had been excavated. Great opencast pits scour the gently rolling countryside revealing thin slabs of cream-coloured limestone, where each bed represents the former sediment surface. The limestone provides the perfect fine-grained stone for the manufacture of lithographic printing plates; this is still a popular medium with artists today, but had an even greater use in the past for graphic illustration. The Germans called this kind of rock ‘plattenkalk’, which is an appropriate name because if a fossil turns up it will be laid out on the surface of the slab like a fish on a very flat plate; and some of the fossils are, indeed, those of fishes. The most famous fossils from the Solnhofen Limestone are skeletons belonging to the early bird Archaeopteryx lithographica, complete with feathers, but they are very rare – only one turns up in an average decade. Some other fossils are quite abundant, like those of little sea lilies (Saccocoma). The Solnhofen Limestone is thought to have accumulated in a warm lagoon, or a series of lagoons, not far from a biologically diverse land habitat, but with periodic influxes of waters from the sea. From time to time the lagoon became salty enough from evaporation to poison living organisms, and its deeper parts were depleted in oxygen sufficiently to deter scavengers. The result is the outstanding preservation of delicate animals. When sticky mud was exposed, animals could get trapped upon it, such as delicate flying reptiles or dragonflies. Operating together, these special conditions preserved a huge cross section of Jurassic life. One of these animals is a horseshoe crab called Mesolimulus walchi. It really is remarkably similar to our living Limulus polyphemus. At first glance it looks as if it had just wandered in from Delaware. One has to look hard to notice that its marginal spines are longer than in our living blue-bloods, and there are a few other minor differences. Nobody could doubt that this species, too, trundled through the shallows, nor that it carried its eggs under its head-shield. To that showy new upstart – a feathered bird – it may already have seemed archaic.
Up to this point I have avoided describing the horseshoe crab as a ‘living fossil’. This is not only because I am chary about using a phrase that is a paradox and an oxymoron rolled into one, but also because it is a misleading description. Charles Darwin himself was cautious when he introduced the term in the phrase quoted at the start of this book. Despite what I have just said about Mesolimulus it is not exactly the same as Limulus. Consider everything we have learned about our living horseshoe crab. It is woven deeply into an ecology that is utterly different from that in the Jurassic. Millions of birds of many species depend on the horseshoes’ eggs every year, whereas its old relative was probably irrelevant to the life cycle of what is often called ‘the first bird’. Limulus has adapted to many changes of circumstances: new predators, new climates, and now humankind. It is a winner in the lottery of life, and not just because of its long family tree. ‘Living fossil’ seems to imply a negative judgement somehow, as if the poor old organism was just about tottering along on its last legs, having hardly changed in tune with a changing world, awaiting an inevitable end. A similar misplaced judgemental tone is often applied to dinosaurs. ‘We mustn’t be dinosaurs! We must change with the times!’ is a mantra of commerce. The dinosaurs were actually superbly efficient animals, and their extinction was most likely a combination of external factors (a drastic meteorite impact is favoured by many) that had nothing to do either with their virtues or lack of them. They were animals of the wrong size living in the wrong places at the wrong time. Bad luck! Meanwhile, the living fossils trundled on through the crisis because … well, we will come to that.
Modifications are happening at the genomic level all the time. There really is no such thing as ‘no change’; the very flexibility of the DNA molecule is what has kept natural selection on its toes for thousands of millions of years. Nor is change in DNA necessarily related directly to any change in the appearance of an animal. Many mutations accumulate in the large fraction of the genome that apparently does not do much work in the specification of proteins, or initiating developmental changes, or any of the other vital, active stuff. These mutations might well be irrelevant to the kind of changes in shape or colour that indicate the appearance of new species. A living fossil may indeed have accumulated many changes at the molecular level that have not even been expressed in its surface appearance, which is the phenotype that has to face the world. Fluctuations in gene frequency are the stuff of life, but they don’t map one-to-one on skeletons and limbs, which are the usual stuff of fossils. So a little caution in terminology is wise.
There is also a temptation to think of the living fossil as if it were a true, surviving ancestor. When the coelacanth fish was discovered it was presented in the popular press as ‘old fourlegs’ as if it were just about to march onto land on its stumpy fins as a thoroughgoing tetrapod. Not only does this scenario happen to be wrong, but the likelihood of any such ancestor surviving unchanged to the present day through many millions of years is also exceedingly remote. Time, chance, and competition will see to it that change is inevitable. What can be said without demur is that the ancient survivor and its other living – and more evolutionarily advanced – relatives will have shared a common ancestor, and that the features of the living fossil will be closer to those of that ancestor. The discovery of ancient fossils more or less similar to the survivor will date the appearance of the whole animal group to which they belong, and point up the changes that must have happened through geological time along the subsequent branches of the evolutionary tree. The survivors from the early days carry with them a package of information revealing primitive morphology, development, and biochemistry that can illuminate histories that would otherwise be hidden from us. Fossils never preserve blue blood. The ‘living fossils’ may not be the ancestor, but they are survivors carrying a precious legacy of information from distant days and vanished worlds.
Hence Limulus allows us to understand something about deep branches in evolution. It is far from unique. If every descendant species had simply replaced its predecessor, the history of life would be like one of those patients described by Oliver Sacks who live perpetually in the present day, constantly erasing the memories of yesterday. Fortunately, life is not like that. Deep history is all around us. In the life of the planet, the latest model does not always invalidate the tried-and-tested old creature. Groups of organisms that originated long, long ago, in very different worlds, have been able to evolve and adapt alongside their more recent cousins and second cousins. The story of life is almost as much about accommodation as it is about replacement. To look at a living horseshoe crab is to see a portrait of a distant ancestor repainted by time, but with many of its features still unchanged. This book reflects my interest in living survivors from the geological past and what they can tell us about the course of evolution. I have spent the last few years seeking out animals and plants that have helped to illuminate our understanding of the history of life. Wherever possible, I have visited these organisms in their natural habitats; none has proved less than fascinating. Observing how they survive today has allowed me a glimpse of their biology and provided clues about the reasons for their longevity. I have carefully selected the old timers I visited because I wished to understand their biology in depth; I have had passing encounters with several more. A few organisms proved too rare or inaccessible for me to discover personally – the coelacanth comes to mind – and then I have relied on the accounts of others. I shall relate many of these case histories to those of their fossil relatives, which is only to be expected of a palaeontologist. This will illuminate the vital fourth dimension – time. I soon discovered that there were too many potential candidates for inclusion, and I am obliged to mention some of them only briefly. I believe it is better to deal with a smaller number of organisms in detail than swish around vaguely with a broad brush. My specialist friends will probably complain that I have left out their particular favourite beast or weed, and my answer is that these survivors have lasted so long that they will almost certainly still be around for someone else to champion in the future.
Consider scorpions, for example. In some ways they are as impressive as horseshoe crabs as survivors. I have met them several times in my fossil collecting career, usually hiding beneath a log or a rock, for many of them stalk their prey at night and stay out of sight by day. In the Oman desert I once disturbed a huge, black knobbly scorpion that came running at me with its tail-sting erect, while I backed off in the opposite direction, gibbering foolishly. My Omani companions laughed and told me that its sting (in the tail of course) was relatively mild. A few hours later I lifted up a rock slab and nestled beneath it was a small yellowish scorpion with a flattened, side-wound sting. I was about to poke at it with my geological hammer when my companions tugged at my arm. ‘Don’t touch, it’s a real killer!’ The smaller, insignificant-looking creatures can often be the most deadly. The spike on Limulus’ tail and the sting on the scorpion’s are closely related structures, and indeed both animals belong to the same great arachnid group. The scorpion learned the trick of arching over the very end of its body to dart poison into enemy or prey. Encased within an external skeleton (cuticle) that prevents evaporation with outstanding efficiency, the scorpion has been able to live far away from water; some species specialise in surviving in the driest places on earth. Scorpions started out as sub-aqueous creatures like Limulus, and only later did they acquire the skill of living on land. Back in Devonian times, 400 million years ago, their relatives, the sea scorpions (eurypterids) were the largest invertebrate predators ever to have lived, some as long as a man. There are fossils from the Carboniferous age that really do look like living scorpions, at least to the non-specialist. They, too, have faced out extinction events that have blasted greater and more glamorous animals. The scorpion is built into mythology as a sign of the zodiac; it features on Roman mosaics, and in the Bible (1 Kings 12:11): ‘my father hath chastised you with whips, but I will chastise you with scorpions’. So one could argue that the scorpion’s connection to human culture is more pervasive than that of the horseshoe crab. My choice of organisms has been guided by the place they occupy in the tree of life, rather than by their innate charisma or significance in folklore and culture. The horseshoe crabs earn a special place in this natural history because their relatives root down to the beginning of the diversification of animals. The early Permian Palaeolimulus is clearly a horseshoe crab, for all that it predated the great extinction that put paid to most species at the end of the Palaeozoic Era, 250 million years ago. Limulitella is present in 242-million-year-old (Triassic) strata dating after the great trauma, evidence of their survival. Those distinctive tracks left by the tips of the legs, and the trail of the tail, that I observed in Delaware have been found as fossils even in the absence of the body itself. There were horseshoe crabs crawling among the coal swamps of the Carboniferous (Pennsylvanian), a little better segmented perhaps than the beasts on Delaware Bay, but carrying the distinct signature of their ancestry. In 2009 my Canadian colleague, David Rudkin, announced the discovery of the oldest typical horseshoe crab in rocks of Ordovician (approximately 450 million years) age, thus taking these simple arthropods back before all the major extinction events that have rocked the Phanerozoic biosphere. Whatever the magic ingredient for survival is, the horseshoes clearly have it in spades. ‘The meek shall inherit the earth’ may be an appropriate motto for their longevity.
3. Gustav Vigeland’s sculpture of a survivor, the scorpion, Frogner Park, Oslo, Norway.
Let me describe these early days in more detail. I have already remarked that the horseshoe crabs had set out upon their distinctive path before the first land plants had advanced upon harsh and barren shores; although recent discoveries suggest that a few simple plants may have already ventured onto mud flats. These had probably not yet been followed by insects or spiders. There were fishes already, of a primitive cast, but they had no ambitions then to invade the land, although a few species may have nudged into waters that were not fully marine. The seas abounded with trilobites, which occupied every ecological zone from shallow shores to ocean deeps. These prolific arthropods must have been many times more abundant than the early relatives of the horseshoe crabs. They evidently had an advantage at the time. This may have been the evolution of their robust dorsal ‘shell’ of calcite, which allowed them to develop spines, armour and a tough anchor for muscles, as well as an ability to roll up into tight, impregnable balls when threatened. Trilobites soon learned an array of different feeding habits; some were predators, some ate soft mud, others swam in the open seas. They died out some 255 million years ago. By contrast, the relatives of Limulus may have stayed conservatively on the sea floor as scavengers and predators. The horseshoe crabs on Delaware Bay have an exoskeleton of chitin, which is a natural polymer that is quite tough and flexible, although no substitute for stony calcite. But the horseshoe crab has turned what might have been a weakness to advantage by developing an exceptional immune system. Survival in the long term may depend on more subtle features than armour alone.
It is possible to trace the horseshoe crab story still further back, into the Cambrian Period more than 500 million years ago, to a time when many of the major types of animals converge towards their common ancestors. The Cambrian was an interval of unprecedented evolutionary activity and I shall describe its special features in more detail in the next chapter. Early relatives of Limulus have been identified in Cambrian strata, but they include some species that look a little different from their hardy survivors. Some of them also look more like early trilobites, such as Olenellus, a form with a big head-shield surrounded by a narrow rim; one might expect a family resemblance if they are indeed closer to a common origin. There are important differences, too. Where the limbs of trilobites are known, they are similar all along the length of the animal: the paired limbs are each split into a walking leg carrying a comb-like branch near its base that in all likelihood functioned as a gill. They are not subdivided into different ‘packages’ in different parts of the body separating walking and feeding appendages in front from gills behind, as they are in Limulus. To add to this, all trilobites had typical ‘feeler’ antennae near the front of the head, and none had the strange chelicerae. This may not be so important, since having antennae seems to have been a general property of primitive arthropods. It might just be that the trilobites still retain this one characteristic more primitive than Limulus and its allies, but they could yet have descended from a common ancestor. Trilobites are abundant fossils on account of their easily preserved calcite hard parts. Fossils of unmineralised animals are altogether more unusual. Spectacular recent discoveries of fossils of soft-bodied animals preserved within Cambrian rocks have been made in China and Greenland. These have revealed an almost embarrassing variety of undoubted arthropods early in the Cambrian. Some of them might seem to bridge the differences between Limulus and its allies and the trilobites, but for every feature that points one way, there seems to be another that suggests something else. For more than a decade now palaeontologists have argued about how these fossils should be classified, and about the only thing they all agree upon is that the Cambrian threw up many animals with curious combinations of characteristics that were probably winnowed out by subsequent evolution. It is not, perhaps, so surprising that ‘mixed up’ animals lived at this Cambrian time, because all the arthropods were not genetically far apart then – they would have had the subsequent 500 million years to box themselves into more separate evolutionary compartments. In these early days the destiny of one animal to become a crustacean, say, and another a chelicerate was not easy to anticipate.
When scientists are confronted by conundrums of this kind, they usually turn to computers. There are now sophisticated computer programs that deal with the problems of determining relationships between animals. They work by identifying the particular arrangement of the creatures analysed on a branching tree that most succinctly accounts for the features they share with their fellows. The most significant resemblances in morphology should result in organisms being classified together on a single branch. Like so many computer methods, the inner workings of the process are staggering in their complexity, so that for a big problem like analysing the Cambrian arthropods millions of potential arrangements of trees embracing the animals under study will be inspected and rejected. My own appreciation of what goes on inside these machines is thoroughly naïve, and I cannot suppress a vision of thousands of cards being shuffled into piles like a supercharged game of Patience until the answer ‘comes out’. The end product is a diagrammatic tree (technically, a cladogram) that can look enticingly simple. I should add that the way the summary ‘tree of life’ on the endpapers is drawn is not like a cladogram, but it does incorporate the results of many individual cladistic analyses. Like all computer methods, the latter are subject to the familiar caveat of RIRO (Rubbish In Rubbish Out), but the fact that they have been so widely used indicates that they have helped with thorny problems. According to the analyses to date, on balance the trilobites indeed do still classify within a group that also includes the horseshoe crabs. Despite all the confusion of the Cambrian it seems my crusty-shelled friends and the dogged, eternally trundling horseshoe crabs are sisters under the external arthropod skin.
They do share special features. The larva of the horseshoe crab is a pinhead-sized object long known as the ‘trilobite larva’, because it does resemble the tiny larva of many trilobites.
Both kinds of animals grow larger with each moult in similar ways, casting off their old external housing and re-growing larger premises. Then there are the compound eyes. In both trilobites and horseshoe crabs the eyes are included as part of the head-shield, rather than sticking out separately at the front on flexible stalks as they are in the majority of crustaceans. Most of us will have looked a lobster in the eyes before popping him into the pot. The lenses of the trilobites are unique in the animal kingdom, since they are made of the mineral calcite. Hard calcite makes up the hard parts of the trilobite, providing the crusty shield that covers the back of the animal known as the dorsal exoskeleton. Calcite has also been recruited to provide the material for the lenses of the eye – so they have become ‘crystal eyes’ if you will. The individual lenses are minute in many trilobite eyes (they can have several thousand), but each separate lens presumably responded to an external light stimulus, and then an optic nerve conveyed the information to the brain. Eyes with many small lenses are usually thought of as particularly sensitive to movement: a moving image progressively impinges on different lenses within the field of view. Both trilobites and Limulus have eyes that look predominantly sideways, scouting around over the sea floor where they live. Strangely enough, the eye of Limulus has been very intensively studied. Haldan K. Hartline of the University of Pennsylvania used the eye of the horseshoe crab as his experimental material to investigate the physics of animal vision. In the 1930s he was the first scientist able to record the activity of a single optic nerve fibre attached to a lens (ommatidium). Limulus has about a thousand such fibres in the eye, and we might well imagine that trilobite eyes had at least a comparable sensitivity. He later showed how different fibres in the optic nerves respond to light in selectively different ways. This opened up the route to a whole new field of physiology – and earned Hartline the Nobel Prize in 1967. Robert Barlow and his colleagues are now building further on Hartline’s research. They have attached miniature video cameras onto living animals in order to scrutinise exactly where the horseshoe crabs are looking. The eyes seem to exhibit an unsuspected sophistication. There is apparently a natural, or circadian rhythm in the sensitivity of the ocular system, which combines with other dark-adaptive mechanisms so that their sensitivity at night may be as much as a million times more acute than in the daytime. Crabs are particularly attuned to recognising potential mates, which, given the frenetic activity along Delaware Bay, is not altogether surprising. The ability of the Limulus eye to eliminate visual ‘noise’ is quite extraordinary (think of our own faltering attempts to really see very faint stars on a dark night), and Dr Barlow is currently trying to understand how this works right down at the molecular level. It is probably the case that we know as much about the visual system of this ancient arthropod as about that of any other living creature. But the more we know the more we might wonder whether this particular survivor is primitive or just exquisitely adapted. Did the trilobites have blue blood? There is no final proof one way or the other; nor can there ever be with such perishable stuff as blood. However, there are many examples of trilobites that have been severely bitten and yet have survived. They usually show a sealed-off gouge on one side. Even in the early Cambrian there were predators such as the lobster-sized Anomalocaris and its relatives that might have regarded a trilobite as a crunchy snack. Anomalocaris was a strange, but evidently raptorial arthropod with two long grasping arms and a mouth surrounded by plates. In those days of accelerated evolutionary change natural selection would rapidly have favoured any mutation that stopped a wounded trilobite from bleeding to death, and the same would have applied to any of its relatives. Since the circulation system of Limulus, and doubtless of a trilobite, is diffuse compared with our own – it more or less fills the open spaces between the other internal organs – a general clotting agent would have been at a premium. It does seem possible that the alternative way of making blood – the copper route – could have had a very long pedigree, and that the blue ichor’s ability to seal wounds and its sensitivity to infection could have helped both trilobites and horseshoe crabs to survive in a newly vicious world. This is one of those moments when palaeontologists wish they could circumvent the rules of the space-time continuum, and go back and see for themselves. As it is, we have to make do with more or less plausible guesses, in the process trying to persuade our fellow scientists that we have undoubtedly arrived at an entirely logical conclusion. History, of course, does not necessarily have to follow our own human logic, and may have surprises of its own.
Could a scene like that witnessed at the beginning of this chapter been played out by trilobites in deep geological time? It is possible. To see evidence I must take you with me to the small town of Arouca in northern Portugal. It lies at the end of a very winding drive into the hills from the old seafaring city of Porto. The prevalence of hillsides covered with eucalyptus trees in some parts of this landscape can be depressing, as these antipodeans are out of place here; but their contribution to the local economy pushes all ecological niceties to one side. Most go to pulp for paper, for these efficient trees grow faster than native species. So in another sense these eucalypts, too, are natural survivors. Every now and then bush fires flare up uncontrollably, fuelled by the volatile oils of the ‘gum trees’; black swathes along the hillsides record their ugly legacy. In the higher hills, pretty valleys contain ancient mills and farmhouses built of crudely squared-off large blocks of the grey granite that makes up the highest, bare ground in the region. In geological terms, obstinate granite is probably the longest survivor of all. Little has happened to the face of these sensible buildings since medieval times other than a dappling of face-paint provided by lichens. On the bleak granite moors nearby are burial chambers that have seen much of human history pass, but still endure. Since the time of the trilobite, whole mountain ranges comprised of this most persistent stone have been worn away grain by grain by the inexorable forces of erosion, and rendered down to sea level. Life outlasts even mountains, for the greatest survivor of all is DNA.
Arouca must be the only town in the world with a trilobite monument, which is a tall spike sitting a little uneasily in the centre of a roundabout. The small hill town is bidding to achieve European Geopark status, and part of its claim is as the home of giant trilobites, which figure prominently on the monument. To see the real thing I head off to the slate quarries above the town near the little village of Canelas. Mining has been a part of the culture in the region for a long time. The Romans were in the hills seeking gold, and old workings excavated into tough Ordovician sandstones can still be seen atop a local high spot, where a dark and slippery stairway leads down into a ferny crevice. The same sandstones preserve fossils of burrows made by trilobites digging into an ancient sea floor, providing yet another type of treasure. Nowadays, the booty is roofing slate. A mass of Ordovician slates known as the Valongo Formation over-lies the sandstones and runs across country. The slates are nearly black, and split into flat sheets that can be further split again until they make usable roofing slabs. Once prepared this way, they are very durable commodities. The slates are extracted from large quarries by blasting out huge chunks of rock, which are then carried away to a factory for further working. The flat planes along which the slate cleaves also furnish a record of Ordovician sea floors, albeit now turned almost vertically as a result of convulsions of the earth. Every now and then a slab covered with trilobites is discovered. They are, as my Spanish colleagues exclaimed without overstatement ¡espectacular! The fossils often show up pale greyish against their dark background. Under normal circumstances it is a rare event to find trilobites much bigger than a small shoe, but in this locality they are often as big as tureens. The largest trilobite in the world, perhaps a metre in length, may be lurking among unstudied collections, but specimens 70 cm long are already familiar. Not only are they large, they are also numerous. Because whole bedding planes (which represent former sea floors) are extracted, an extensive view of a tragic moment in time is occasionally recovered: it is a fossil graveyard, with bodies laid out at the moment of death, a community of cadavers. A scenario like this could not be extracted by the usual tapping of the geologist’s hammer upon a rock: it requires activity on an industrial scale. Fortunately, the quarry owner is aware of the importance of his slates in exposing a sea floor perhaps 470 million years old; time enough to erode three mountain ranges, granite and all. Many of the trilobites are preserved on site in a private museum that the owner has generously dedicated to conserving these fossil remains. A dozen different species are on display there; to one in thrall to the past like me it is an extraordinary experience to see these grey bodies covering every wall. It has something of the feel of a picture gallery, and I have to remind myself that these were once scuttling animals as intent on their business as any living horseshoe crab.
Many of the large slabs show assemblages of just one species together, and the individuals are all large and of similar size. They are often complete bodies, which suggests they are entire animals that have been killed rather than, say, the ‘cast-offs’ left behind after moulting, when bits and pieces might be expected, arranged higgledy-piggledy. There are examples where the bodies partially overlap. All this is very like the mating congregations of horseshoe crabs along Delaware Bay. Imagine if some catastrophe had killed and preserved the crabs at the height of their nuptials. A volcanic eruption might fit the bill; this would bury and kill the animals at exactly the same time. After eons passed the sediments would have hardened into rock and the crabs would be fossils; compaction of the sediment would also have flattened down the buried beasts. Some fossil specimens would still partly overlap their partners, frozen in the act. The younger animals would have been elsewhere, so they are not represented among the fossils. It is a plausible scenario, even a tempting one. We have to add an extra complication, because something additional had happened to the Portuguese trilobites during their long sojourn in the rock. The whole mass of slates of which they have become a part has been squeezed in a tectonic vice that has twisted some specimens out of true until they look a little lopsided. Others have been stretched somewhat, and as a result claims about the ‘longest ever trilobite’ have to be treated with caution.
A more critical examination of the evidence identifies some important differences between Delaware Bay today and Ordovician Portugal. The most obvious of these is that the giant trilobites were clearly not gathered upon a beach. They were overwhelmed and killed on the sea floor. Local Portuguese geologists believe that the Ordovician animals lived in a marine basin with poor oceanic circulation, so that deeper layers could become stagnant. The congregated trilobites might have been overcome by a phase when oxygen dropped to lethal levels: after all, even trilobites needed to breathe. Such anoxia is not much of a problem in Delaware Bay. The trilobites could still have been gathering for reproductive purposes, of course. They might have even been safer from predators in the deeper basin. But then it makes us uneasy to think of the trilobites depositing their eggs in such an inhospitable place – unless anoxic events were so rare as to have little effect on their long-term survival. Then there is the fact that a number of the slabs seem to show a mixture of species. Could they have been gathered together for some purpose other than mating? Unlike Limulus, a freshly moulted ‘soft shelled’ trilobite would have been vulnerable until it grew a new hard carapace. Maybe these congregations were huddled together for mutual protection away from the prying eyes of predators. With these ambiguities in the picture the case for a direct comparison with the behaviour of modern horseshoes begins to seem weaker. A sceptic would say that it is simple minded to expect similar habits to endure for hundreds of millions of years. Perhaps so, but common problems in nature often come up with comparable solutions, the more so if the organisms concerned are related. Those trilobite examples with marginally overlapping bodies might merit further examination, since they do recall the struggle for mating among the horseshoe crabs, and it is more than a guess that eyes in these animals were particularly attuned to seeking out mates. I still like to think that the crystal eyes of trilobites may have had similar lustful intent.
2
The Search for the Velvet Worm
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.
3
Slimy Mounds
Shark Bay is a long way from anywhere. In Australia, distance soon acquires its own curious rules. Within the suburban strip that lines favoured parts of the coast there are traffic jams and shopping malls like anywhere else, but away from civilisation the outback country stretches onwards forever. Far from the mountainous east, much of the country is flat. No doubt connoisseurs of the horizontal find infinite entertainment in its small variations, but for me a bemused puzzlement sets in after a few hours apparently rehearsing the same piece of landscape numerous times. Time begins to stretch in odd ways. After a snooze, I wake up unsure whether I have been asleep for ten minutes or two hours. Small eucalypts line wandering creeks while sand dunes are covered with scrub, occasional scruffy fences mark obscure ownership, and there are groves of taller gums or isolated she-oaks stocked with the noisy parrots known as galahs. Then the sequence repeats, but not necessarily in the same order. The landscape is utterly distinctive, like that of nowhere else in the world, with a stark beauty under a clear pale blue sky, but it is also relentlessly repetitive. Anyone foolish enough to leave the marked track will find it is easy to get lost. Bush stories are full of sticky ends and grieving widows. I know that maps do not really work in a landscape that repeats like an old tune whistled over and over.
Route 1, running up the west coast of Western Australia towards Shark Bay, seems never to end. The Greyhound bus runs onwards through the dark, with nothing really distinguishing the passage of miles except sporadically a startled kangaroo picked out in the headlights. Occasional vehicles pass the other way, and each one seems something of a surprise. What can they be doing out here? I have to remind myself yet again that I am en route to see one of the holy relics in geology; it will be worth the effort. After countless hours, the Overlander Roadhouse welcomes me – a neon-lit marker set down in the endless landscape; a gas station, with a rudimentary restaurant, a place to loaf about until the next bus arrives. Aboriginal people wait there desultorily for relatives who have been off to Perth or somewhere to make a few dollars. Flies buzz about, with irritating persistence; there must be something else for them to do than endlessly return to drink from the same sweaty brow, or so one would think, but round and round they go. Backpackers loiter, waiting to embark on the next section of an adventure planned in theory, but now measured out in sweat and flies. It is a kind of end-of-the-world place, on nobody’s list of ‘must-sees’, but an essential stopping point before negotiating the wilderness. This is a place where timetables mean something to somebody, a place where I can get the next bus to see the stromatolites. Not far from the Overlander Roadhouse is a place that tells us of the transformation of the very air we breathe, a window opening into remote Precambrian times.
Though the outback may look pristine, in this part of Australia the wildlife has been transformed by human introductions. Feral goats have degraded the natural bush, and cats have culled the nocturnal mammals that were once numerous. The big-eared marsupial bilby, with its back legs like a miniature kangaroo and improbably long tail, is such a charming animal that it has become a kind of mascot for the conservation movement hereabouts. It would indeed be tragic if its only permanent memorial were in one of those perfectly photographed wildlife television programmes. Conservationists in Australia have taken to referring to the ‘Easter bilby’ rather than the ‘Easter bunny’ (bunnies being voracious introductions, too). It is already too late for many small marsupials in the eastern states of the country; their only record now being watercolour drawings made by the early naturalists. These harmless creatures could not outwit intelligent feline and canine hunters, and they failed to survive. Australia is full of poignant paradoxes. This land has many ancient biological survivors yet it is also, much like New Zealand, a place where the extinction of species is still in progress. This is despite the efforts of a generation of Australians many of whom treasure their unique fauna and flora. Almost every town boasts dedicated people concerned with ‘bush regeneration’, and in Western Australia new species of beautiful indigenous plants are still being discovered regularly, even around Perth. It is a very biodiverse region, despite the challenges of the climate, and not yet fully known. While I was there Tropical Cyclone Hubert turned the sky black, and sections of the main road were closed. The species that live in this tough land must be natural survivors to be able to negotiate fluctuations between flood and swelter. That description, of course, also includes feral cats.
Shark Bay is a huge and ragged bite into the profile of the west coast of Australia. It has now become a World Heritage Area, which brings more money and more tourism. Much of the former, and nearly all of the latter, is directed to the beach resort of Monkey Mia where ‘swimming with dolphins’ is on offer. When I flew over the Bay and its clear waters in a light plane, I saw an undulating submarine prairie of sea grass, dark emerald green, broken into banks like meadows. A tenth of the world’s dugongs – 250 kilograms of peaceable herbivorous sea mammal – graze in leisurely fashion upon this luscious expanse, many living to seventy years or more. Juicy fishes doubtless account for the name of the Bay, since they attract fourteen species of sharks, including species like the tiger shark that command respect. From the air I saw how Shark Bay is divided into two large lobes by a median peninsula; the aboriginal name for the Bay is ‘cartharrgudu’ (‘two bays’). The top of the peninsula is now the Francois Peron National Park and a serious attempt is being made to clear this sandy area of feral goats and predators for the benefit of the native fauna and flora. Dirk Hartog Island provides an outer barrier to the Bay, which protects the coast from storms cutting across the Indian Ocean. I never knew before visiting Western Australia that this island was the first landfall for any European. The Dutchman, Dirk Hartog, landed here on 25 October 1616, beating Captain Cook to it by 152 years, and leaving a pewter plate nailed to a post as evidence. That plate is still preserved in the Rijksmuseum, Amsterdam. William Dampier, ‘the buccaneer explorer’, spent a week there in 1699 and gave the Bay the name we use today. The aboriginal fishermen were plying their trade at the time, but there is little evidence of them now. I conclude that it is not only small and shy marsupials that failed to survive.
My quest is for something altogether more recherché than shark or dugong. At the tip of the eastern bay the edge of the sea provides a prospect of life two billion years ago … I am travelling incredibly far back in time. The journey to the old telegraph station at Hamelin Pool takes me through undulating, intensely green scrub interspersed with a few mallee trees, interrupted only occasionally by flat-bottomed depressions carrying scrappy salt-scrub and patches of white gypsum – the aboriginal inhabitants called these clay-pans birridas. I missed the flowering season, and now all the bushes seem to bear black nuts. Next come low dunes made up of startlingly white tiny shells. I crunch my way across the dunes, and beyond lies a very shallow arm of the sea. This is where the stromatolites grow. I am approaching the famous site where living analogues still flourish of the most ancient organic structures on earth. They ought to have disappeared long before the first velvet worm or horseshoe crab, but here they linger on, a marvel of anachronism.
Back at the highway must be the only road-sign in the world that points to ‘STROMATOLITES’, and no geologist or palaeontologist could fail to follow its bidding. Here they are growing by the shore while the sea beyond shines an almost improbable ultramarine. Is this luminous vision the time warp I sought? Some part of me expects the stromatolites to be green, but they prove to be darkish umber brown. I confess I am momentarily disappointed. They comprise flat-topped cushions and low pillars, or even giant mushrooms expanding upwards like plush stools, with sandy gullies between them. They are regularly disposed along a seaboard more than a hundred yards wide; seawards they disappear beneath the barely lapping waters. It is a scene of perfect calm. A little walkway has been built over the strand so that visitors can get close without damaging the organic structures. I touch one of the hummocks. It is actually quite hard (why did I expect it to be soft?) and slimy or tacky to the touch when moist, but almost crispy when dry. In the bright Australian sun it is even a little warm. Now that I get closer I can see other kinds of surfaces along the shore, particularly sloping stretches of dimpled microbial mats, a fruity brown colour, running down to the glittering sea. They make stretches of the shoreline resemble wrinkled skin. Stromatolites growing at the water’s edge look less like cushions and more like knobbly cauliflower heads. The inevitable flies are buzzing about my head, and some antipodean swallows chirrup cheerfully about the platform. I hope they are after my flies.
Up on the shore are some dead stromatolites, left behind by the sea maybe a thousand years ago. By now they have decayed into iron-stained ruins, but where they have broken open they show the internal structure of the cushion-shaped columns. It is clear to me that the columns are layered internally parallel to their top surfaces, rather like filo pastry. They seem to be built up layer by layer – a little like those giant stack pancakes an unwary visitor gets offered in New York for breakfast. The columns were evidently living things, self-made towers. A little museum on the site of the old telegraph office nearby provides more explanation. I peer closely at a stromatolite kept in a glass tank; its enveloping seawater must be refreshed every month. I see that when water covers the column its surface is slightly fuzzy – no doubt, it is still alive. A lack of crisp definition is somehow a proof of metabolism in action, life blurring the edges. Little bubbles fizz upwards off the top in a steady stream, none bigger than a lentil: they are bubbles of oxygen. So the column is evidently more than a brownish crust, it is something altogether more potent and dynamic, and it is breathing out oxygen, the element that babies and bilbies and bunnies all need to stay alive. Everyone has had nightmares about suffocation, when fighting for breath becomes fighting for life, so we all know in our bones how quickly we would perish without oxygen. The exhibition reminds me of the demonstration of nature in action at my very first school, when us kids looked at water-weed in a full glass beaker, and saw the same little bubbles of oxygen rising to the surface. This was the first time I heard the word ‘photosynthesis’.
The survival of the stromatolites on the beach is another measure of their toughness. On the foreshore I see two broad grooves carving their way through the stromatolite grove. These are the persistent traces of a former industry. In the late nineteenth and early twentieth century, camel trains brought bales of wool here to Flagpole Landing. These were then carted off the foreshore to lighters that sailed 190 kilometres to a boat waiting in deep anchorage off Dirk Hartog Island. Then the wool was transported to Fremantle and finally to the United Kingdom for manufacturing. We are fortunate that these activities did not destroy the mounds completely. But it is also a measure of the slow rate of biological activity hereabouts that the old tracks are still visible after a century.
Sea conditions in this part of Shark Bay are quite particular. The shallow seawater evaporates fast under the relentless sun. It is the basis of a salt industry at Useless Loop nearby. The very clear water has an elevated salinity and is very poor in nutrients. Hamelin Pool is backed up behind a sand bar known as Fauré Island, lying about forty-seven kilometres out to sea, so it is almost a lagoon. Only specially adapted or tolerant organisms can survive under these conditions. One of those animals is a little clam called Fragum hamelini, which, as the name implies, is special to this locality. It is so abundant that its snow-white shells, none bigger than a walnut, make up the dunes that line the Bay. After some decades the shells harden into a shelly rock – it would be an exaggeration to call it a limestone. An old quarry above the shore records the employment into which this curious white stone has been pressed. Cut into blocks the size of large bricks it made a serviceable, if hardly robust building stone. Some of the older edifices made of it still stand. The stone was used to build the walls of the Pearler Inn in the town of Denham, eighty kilometres distant. This pub looks as if it were constructed from a mass of white peas. In order to survive the testing conditions in the Bay, Fragum has incorporated photosynthesising algae into its tissues: sunlight is the ultimate source of its food, just as it is for the stromatolites. But Fragum is an evolutionary newcomer, whereas the stromatolites are very, very ancient.
Stromatolites are mounds slowly built up by microscopic organisms, layer by layer. The mounds are not composed of a single organism: they are a whole ecology. The tacky or slimy skin that caps the stromatolites is the living part. This very thin layer is composed mostly of cyanobacteria, organisms that are often called ‘blue greens’ (or, formerly and incorrectly, blue-green algae) on account of their characteristic hue beneath the microscope. This may well explain why I expected the stromatolites to be green. The conditions in Hamelin Pool suit their growth. There are many organisms in nature that like to graze on ‘blue greens’. Think of those finely scalloped trails wandering over moist rocks by the seaside, made by the rasping action of the sea snail’s feeding apparatus as it scrapes away the thin nutritious bacterial layer that paints the rocky surface. This is not inappropriately compared with grazing by herbivores on terrestrial environments. Like grass, the ‘blue greens’ grow back, and the molluscs move on. But these micro-organisms never have the chance to build complex or elaborate structures like mounds or ‘stagshorns’ because the constant assault of herbivores renders their best attempts at architecture futile. Everything is eaten back before it can grow too big. However, in the special, warm world of Hamelin Pool the grazers are kept at bay. No snails sully the sticky surfaces of the stromatolites; the fish there don’t nibble away the ‘blue greens’ for supper; in fact, nothing much ventures into the almost unnaturally limpid seas. Some authorities believe that the very low nutrient levels in the Pool are as important in growing stromatolites as the absence of grazers. Whatever the reason, the simple organisms have it all their own way for once. And when they do, they reconstruct the Precambrian world. This is how life was before marine animals chomped and scraped away ancient biological constructions that had covered much of the sub-aqueous environment since life began. In Shark Bay a prelapsarian age can be restored to view, a time before velvet worms or even vendobionts, or anything that crawled upon its belly in the mud. I have seen dozens of artist’s reconstructions of ancient seascapes that owe a debt to the prospect at Hamelin Pool. So when I saw the living stromatolites I was not unprepared for the experience. However, I recall seeing Picasso’s Guernica for the first time; just because an image is familiar does not diminish the impact of the real thing.
Cyanobacteria are simple organisms that often make long, green and narrow threads with organic walls which can be as thin as a few thousandths of a millimetre, but which often occur in sufficient profusion to make green slime. Other species are tiny round cells that grow by fission – essentially splitting in two, to double up as identical twins. They are ubiquitous. When a glass of water is left in the light on a window ledge, cyanobacteria will usually appear as a green smudge. They have been wrongly called ‘blue-green algae’ in old textbooks, but as we shall see the algae are altogether more complicated organisms. When raindrops wash over rocks in a desert these tiny organisms will soon take advantage of the opportunity to grow, and the rocks will shortly glisten with microscopic life. In the sea, their numbers occasionally erupt into ‘blooms’ of billions of cells that can poison fish, or even humans, if they eat the wrong kind of shellfish too soon after one of these events. In biological jargon the ‘blue greens’ are described as prokaryotes. They are both the smallest and the simplest-looking cells – often no more than a sphere or a sausage – but there are hundreds of different species. They lack an organised nucleus surrounded by a membrane that is present in every cell in what are termed eukaryotes. Every organism that has been mentioned so far in this book (including the author) is a eukaryote, which is another way of saying that our narrative has now arrived back to a simpler way of organising a living entity. Prokaryotes came before eukaryotes in time, which also means that they are closer to the main trunk of the tree of life. So there was a world before eukaryotes where the cyanobacteria were state-of-the-art and where the prospect before us in the shallow waters in one corner of Shark Bay would have been typical of much of the world, rather than a special survivor. I should flag up at this point that this prokaryote– eukaryote division is itself an over-simplification, and this topic will be revisited in the next chapter.
Modern seaweeds are both plants and eukaryotes, to emphasise the point again, and do not build stromatolitic mounds. In Shark Bay, the majority of such ‘advanced’ organisms are discouraged by the low levels of nutrients available there; hence they leave the dominant cyanobacteria to cooperate in making different kinds of mounds. In the typical stromatolite the mode of growth is cumulative. The living ‘skin’ is a thin layer of growing threads matted and twined together. The technical term for it is a ‘biofilm’. The cyanobacterial mats are positively attracted to light and grow upwards. Any blown dust and other fine sedimentary material becomes incorporated in the surface layer and maybe provides the modest nutrient required. The slimy surface layer of the bacterium encourages the precipitation of calcium carbonate from its dissolved state in seawater, thus making a thin ‘crust’. A new living layer grows on top of the one beneath, and may be able to extend a tiny bit further laterally: this is why some of the stromatolite mounds are wider at the top than at the base. Naturally, the ‘blue greens’ are only able to grow in the sunlight that gives them nourishment, and are quiescent at night. Some scientists at the University of California even claim to have recognised daily growth increments. The overall rate of growth is extraordinarily slow, however, and certainly less than 1 mm a year (and possibly as little as 0.3 mm). It has been stated that some of the Hamelin Pool structures could be a thousand years old, that is, they grow more slowly than the slowest-growing conifer on land. The life and death of the wool industry would register as no more than a hand-depth on the height of a stromatolite column. Time can be ticked out in microscopic laminations, and history reduced to a measuring stick made by timekeepers invisible to the naked eye.
Stromatolites vary in form according to where they are found on the shore. It is easy for me to see that ones at the edge of the sea are little more than pimply mats. At least to this unschooled observer, some of them superficially do not look very different from some of the mats that covered sediment surfaces in the Precambrian at Mistaken Point. They are made particularly by one of the spherical, or coccoidal types called Entophysalis, and the internal layering is not well developed. Further down the shore in Hamelin Pool the stromatolites that I tentatively touched represent the dominant kind in the intertidal zone, with a typical columnar-cushion shape. This kind of column is constructed particularly by a filamentous cyanobacterium called Schizothrix, which under the microscope is an intense emerald-green colour. It has lots of apparent partitions that make the organism look something like an old-fashioned tube of circular cough sweets. These particular stromatolites are very well laminated internally, so that the mechanism of being built up layer by layer is particularly patent. It has been proved that the cushions ‘lean’ a little to the north, each component filament attracted preferentially to the sun (but on such a minute scale) in this, the southern hemisphere; the god Ra evidently ruled in the prokaryotic shallows. Further out to sea again, to a depth of a little more than three metres, there live the lumpier, bumpier, lobed, and somewhat rounded stromatolites that are a collaboration of many different microbes. These include cyanobacteria of the genera Microcoleus and Phormidium; the latter is another concatenation of delicately segmented threads, while the former comprises microscopic ‘ropes’ made up of bundles of a kind of entwined green spaghetti. The different species collaborate to grow together, like a confederation of medieval guilds, with each tiny specialist contributing to the function of an integrated community. True algae – diatoms – may chip in as part of the community among the deeper water stromatolites, but this group of eukaryotes probably did not evolve until much later. Beneath the surface skin of the growing mound, bacteria of a different kind from cyanobacteria process waste products and can cope with low, or even no oxygen; they are like artisans that moved the dung from the streets of the medieval village and made it a trade. Life encouraged specialised habits and habitats from the first.
Stromatolites are the most ancient organic structures, and their recognition as fossils transformed the way we understood the endurance of life on earth and the evolution of its atmosphere. I admit that viewed with complete impartiality when it comes to visual impact, the Shark Bay mounds are not on a par with the Empire State Building or the pyramid of Cheops. But stromatolites are one of the wonders of the world. Rationalists are not permitted to have shrines, but if they were then Shark Bay, where stromatolites were discovered alive, might be high on the list. Although many more living stromatolites have since been discovered, those in Shark Bay have been most thoroughly studied. From their initial recognition in 1954 the fame of these living stromatolites spread, until by the late 1960s they were finding a place in textbooks. As so often happens in science, the discovery of these living mounds happened just when palaeontologists were making major finds of microscopic fossils in rocks of Precambrian age, opening up debates about the biological history of the earth. The strange creatures of the Ediacaran, like Fractofusus and Charniodiscus, took the record of life back tens of millions of years before the great burst of familiar fossils such as trilobites that appeared in the Cambrian, 542 million years ago. But there remained more than three billion years of the history of life on earth in the Precambrian still to account for. This was the era of the stromatolites.
It is necessary to have a digression on geological time at this point. The age of the earth had been established at close to 4.5 billion years by the time Shark Bay was becoming known to the scientific world. The precision of this figure was largely a consequence of refinements in dating techniques, using the slow radioactive decay of naturally-occurring uranium isotopes into other isotopes of lead: turning rocks into clocks, one could say. The samples collected from the moon by the Apollo Mission were first unpacked on 25 July 1969. I recall the excitement of seeing a small black piece of the earth’s barren satellite when samples from the collection made on the Sea of Tranquillity were distributed to major museums, including the Natural History Museum in London. Like the stromatolites, it was not so much the thing itself; it was what it implied that made it so special. After the moon rocks were dated using the best technology of the day the question of the antiquity of the green planet to which the moon was partnered was finally laid to rest: 4.55 billion (plus or minus 0.05).
The geological time period before the Cambrian was simply known as Precambrian for more than a century – after all, that is what it undoubtedly was, ‘before the Cambrian’. But when this time period was recognised as so vastly long, it became necessary to divide it into several named chunks to help us order events in the earth’s history. The Archaean Era is that part of deep geological time that ends at 2500 million years ago, or 2.5 billion years if you prefer. After this came the Proterozoic Era which, in terms of strata, lies above it and extends to the base of the Cambrian Period 542 million years ago (the Cambrian is the first subdivision of the Palaeozoic Era).
The Ediacaran, the latest addition to the roll call of geological time, begins at 635 million years ago and is slotted into the top of the Proterozoic. The Proterozoic Period covers a very long period, and these days is usually divided into three which used to be known as Lower, Middle and Upper, but are now formally known as Palaeo-, Meso- and Neoproterozoic respectively. The Neoproterozoic begins arbitrarily at 1000 million years ago, and the Mesoproterozoic at 1600 million years ago (1.6 billion), so the Palaeoproterozoic occupies the time period 2.5–1.6 billion years ago. Names really do help us get a grasp on the immensity of geological time, though phrases like ‘Palaeoproterozoic digitate columnar stromatolites’ do not exactly trip off the tongue. But it is as well to get our labelling sorted out.
This modern classification is the end point of a long scientific battle. The intellectual classes had been debating the question of the age of the earth since the Comte de Buffon’s estimate of 75,000 years in 1774 based upon the idea of the planet cooling down from a molten state. Apart from a purblind few who insisted (and indeed still insist) upon a biblical timescale based on totting up the generations mentioned in the Bible – Bishop Ussher’s 4004 BC estimate for the Creation – the time available to ‘evolve’ the earth increased fitfully throughout the early days of geology as a science. The bolder savants soon speculated in more and more millions. The longer time got, the more questions were raised about life’s early days, because of the apparent absence of ‘organic remains’ in Precambrian rocks. Charles Darwin famously fretted about it. Geologists of his time were beginning to explore large areas of the world comprised of Precambrian strata as the rocks of countries such as Canada were mapped for the first time. It was soon evident that sedimentary rocks, much like those found in younger geological formations, were widespread over these ancient lands. The seas were apparently barren in these ancient worlds; seas not so different in their physical properties from those that gave succour to the trilobites and snails that could be so easily collected from younger strata. In 1883 the American palaeontologist James Hall found some intensely layered Precambrian rocks apparently ‘growing’ upwards incrementally from a narrower base to which he gave the name Cryptozoon (‘hidden life’); however, their organic nature still remained controversial. Nonetheless, with the mere application of a scientific name, the biological virginity of the Precambrian had been breached. It was time for the stromatolites to be recognised as organic constructions.
The first time I saw fossil stromatolites in the Precambrian was as an undergraduate at the University of Cambridge, when I took part in an expedition to the Arctic island of Spitsbergen in 1967. My doctoral thesis was to be on rocks of Ordovician age exposed along the cold remote shore of Hinlopen Strait on the eastern side of a northerly peninsula called Ny Friesland. The small boat that took us to our field area dodged between ice floes stained with the droppings of countless seabirds, for the Arctic summer is a brief period of plenty for animals that live off the ocean. On land the scenery was bleak: a succession of cobbled beaches raised above the present sea level, across which the occasional polar bear or Arctic fox wandered in search of a feathered snack. It was not an inviting prospect, although it was to be my home for several months. On the way to reach my Ordovician rocks, and before passing the Cambrian strata that lay beneath them, the boat had to chug past a great thickness of even older Proterozoic limestone and shale, piled up layer on layer. There are few places in the world where a young scientist can cruise through such a momentous stretch of geological time, let alone along an outcrop that has survived so unaltered by subsequent earth movements. These ancient rocks were in almost pristine condition. On one occasion we landed to make a temporary camp and pick up fresh water. I wandered over to the nearby rock outcrop just to have a look. The rocks were not horizontal; instead they had been tipped gently (but less so than the rocks at Mistaken Point). I could easily make out the flat bedding planes breaking up the shore into a series of steps that recorded a succession of former sea floors. The rocks were a mixture. Most were very pale grey, sometimes almost pearly, and hard looking. Others were yellowish, in patches somewhat sugary and brightly tinted. The latter were dolomites, a calcium magnesium carbonate rock that at the present day particularly forms in areas surrounding the more arid tropical regions. The off-white rocks were limestones, that is, made of calcium carbonate in a finely crystalline form. Looking closely, I could now observe that several of the limestone surfaces were finely scored. Many years of erosion had picked out subtle differences in hardness within a single bed of limestone, so that lines even a millimetre or so apart could be clearly discerned. A comparison with layered pastry came to mind. I imagine that a blind man could have read the rock surface like Braille, just by gentle palpation. Where the rock surface was weathered at right angles to the bedding surface, providing a natural cross section, these finely-layered rocks were arranged in a series of undulating columns, widening a little from their base. They were stromatolites, or to be more accurate, sections through stromatolites – with a thousand years or more of slow growth preserved in a fossil grave of fine limestone. Cryptozoon proved to be not so cryptic after all; it was the stony legacy of cyanobacteria. When I followed the stromatolites over onto the bedding plane beyond to get a vision of the ancient sea floor, they converted into balloons or pillows stretching away from me, each one showing the top of a stromatolite head. This was the fossilised version of the view at Shark Bay I was to admire decades later. It was bleached to white limestone by the passage of a thousand million years, perhaps, but it was still recognisable, a picture petrified from a former earth. This was the nearest thing I will ever experience to being in a time machine, even if my appreciation of it were countermanded at once by the shrill cries of Arctic terns above my head: chicks to feed, human business to be done, and the earth has moved on. Nothing remains exactly the same forever.
Had I looked more widely along that unwelcoming shore I would have observed a greater variety of shapes carrying the telltale laminations of stromatolites. I would also have noticed some occasional shiny black patches within them; these are made of chert, a very hard, flinty rock composed of the mineral silica. Andrew Knoll, who is perhaps the doyen of Precambrian palaeontology, visited the same rocks in Spitsbergen a few years later, as he has described in his book Life on a Young Planet. From those cherts he recovered remarkable small fossils, which helped to make his reputation. He also recorded a whole range of different rock types produced by ancient micro-organisms; the most general term for these rocks is ‘microbialites’ which is a term that I trust does not require further explanation. Subtly mottled microbialites can present the appearance of ornamental marble, or the interior of a sponge cake, or the dimpled mats that I saw on Shark Bay; they can all be attributed to the work of bacteria and their relatives. Evidently, ancient microscopic communities did not just manufacture columns, though these do display several different shapes. Over much of the vast compass of Precambrian time it was a dominantly microbial world, and there was nothing to prevent tiny organisms from constructing a variety of edifices.
Stromatolite fossils are not at all rare if the right rocks are explored. It is not surprising that many rocks have been altered by heat or pressure if they have sojourned on the earth for billions of years. The great motor of plate tectonics has been continuously in operation, building mountains and moving continents around. It is a lucky rock that escapes unscathed. Most of those that have successfully dodged being crunched or heated up are found around the edges of the most ancient and stable continental cores often known as ‘shields’. These bits of earth’s crust stabilised early on, and have been pushed around the earth during successive phases of continent building rather like counters being shoved around a draughts board. They survive to play another game. If there are patches of stromatolites preserved upon them, they are handed onwards. Perhaps the Canadian Shield is the best known of these ancient areas, but parts of southern Africa and Western Australia are equally familiar to geologists. However, the list of stromatolite occurrences is much longer than that of ancient shield areas, the rocks Andrew Knoll and I examined in Spitsbergen being a case in point. It is obvious that these strange organic structures were almost ubiquitous at least in the shallower parts of ancient oceans. Cyanobacteria would have needed light to grow, so the particular stromatolitic structures made by them must have been confined to comparatively shallow water. The early Precambrian ocean depths are unknown to us, since ocean floors are consumed in the inexorable slow dance of the plates. But it is more than likely that there, too, were structures made by different bacteria that flourished away from light. After all, life never misses a trick.
Stromatolites are found way back into the Archaean. The oldest ones of all are almost miraculous survivors found on the scraps remaining today of the most ancient continents. Fossils dated at 3.5 billion years old have been found in the Apex Chert in Western Australia,
and in Swaziland. It is hardly possible to imagine such antiquity. I have the same trouble trying to grasp the number of stars in the Milky Way, for the mind soon loses its normal frame of reference when the figures get so large. I can probably do no better than echo the words of the pioneer geologist John Playfair in 1788, when he became convinced of the reality of the vast age of the earth: ‘the mind seemed to grow giddy looking so far into the abyss of time’. Nonetheless, it is important to at least get a feeling for this ‘abyss’, an intuition of its magnitude, because it shows just how long it has taken for life to arrive where it is today. The two stories of life, and the earth itself, have been intimately intertwined for billions of years.
Stromatolites began in the Archaean as relatively simple domes, but later they evolved into a number of different forms. Some of the more distinctive shapes have been dubbed with Latin names, just as if they were organisms in the conventional sense (Pilbaria perplexa and the like). As we have seen, they are actually collaborations between several organisms, so such an approach does not fit in with normal biological procedure. However, it is useful to have a way to refer to different shapes and forms, and some of the names have achieved wide currency. In the far reaches of the Precambrian, stromatolites could grow in a wider range of marine environments than they do now, and this may partly account for some of their different shapes. In deeper or calmer water, for example, it was possible for relatively delicate, branching, even candelabra-like forms to grow. In complete contrast, one of the most distinctive varieties produced massive cone-shaped bodies that could grow to be tens of metres high. These microbial behemoths have received the appropriate name Conophyton (‘cone plant’). They have been memorably described as making outcrops in the field look like a series of rocket launchers placed side by side: they must have taken many centuries, even millennia, to grow. The vocabulary used to describe different kinds of stromatolites gives some indication of their variety of form; they have been compared with fingers, fists, cauliflowers, columns, spindles, trees, mushrooms, kidneys. Given time enough these most simple organisms could produce an art gallery’s worth of shapes. Nature was patently a sculptor from the first. The view from Hamelin Pool was, it now transpires, only a partial glimpse of a richer, but now vanished stromatolitic world.
The controls on stromatolite growth were probably quite simple. The growing surface film was attracted towards the sun, while the supply of calcium carbonate from seawater dictated the dimensions of the layers produced. A group of Australian physicists have developed computer models that ‘grow’ stromatolites by playing around with these simple elements. Conophyton emerges naturally as a shape in response to strong solar attraction; prokaryotic life, it seems, simply could not help building regular structures. Where there’s life there’s architecture. But there is also good evidence that the variety and complexity of stromatolites increased during their extraordinarily long tenure of the earth’s seas. The few kinds of simple domes and cones that dominated their first billion years, during the Archaean, were supplemented by dozens of additional shapes during the Proterozoic, when branched structures and pleated columns on many different scales appeared. The first occurrence of particular stromatolites has even been used broadly to subdivide this long period of time. They probably achieved their greatest variety about a thousand million years ago, but still long before the emergence of large animals, even the strange Ediacaran ones. Many early stromatolites were fully submarine, rather than living between the tides. Their living analogues have been found in the Bahamas near Exuma Island, hidden in marine channels. Here, these large, lumpy columns rising from a lime-mud sea floor probably provide a closer match to many Proterozoic environments than does Shark Bay. The biofilm forming the living skin is known to be a complex microbial community, and much more than just a photosynthesising surface. Several other kinds of bacteria have their homes there, some with the capacity to ‘fix’ nitrogen, like the little nodules harbouring bacteria that grow on the roots of beans and contribute to soil fertility. These kinds of bacteria work at night, when the cyanobacteria are ‘sleeping’. Once again, the mat is a whole ecology, a world measured in millimetres.
As for the fossils of the organisms that made the Precambrian mounds, the apparent absence of which so perplexed Charles Darwin and his contemporaries, well, they were lurking there all the time; it is just that they were very small. The cherts, like those tucked among the limestone rocks on Spitsbergen, held the secret. In some cases such siliceous rocks were formed early enough to petrify the fine threads and other cells making up the ancient biofilm. The process is somewhat analogous to that involved in making artificial resin souvenirs in which butterflies or scorpions are preserved, colour and all, which then lurk on the mantelpiece forever. Silica petrifactions were already well known from higher in the geological column, even preserving tree trunks down to the last cell. Considering that the dimensions of the Precambrian fossils are often measured in a few thousandths of a millimetre, the preservation of their cell walls is remarkable, almost miraculous. However, when very thin sections were made of the right Precambrian cherts they became transparent; these preparations were then examined under the microscope and revealed the unmistakeable imprint of life. The discovery was reported in detail in 1965 by the resplendently named American scientist Elso Sterrenberg Barghoorn Jr based on fossils obtained from the Gunflint Chert, a rock formation exposed along the northern shores of Lake Superior. Barghoorn’s co-author, Stanley Tyler, had previously recognised fossil stromatolites preserved in rather beautiful red jaspers (an iron-rich form of silica). At the edge of the Canadian Shield, the Gunflint Chert was one of those special survivors that had escaped the subsequent adventures of our mobile planet, fortuitously frozen in its own ancient time. At 1.9 billion years old, the fossils of the Gunflint Chert lie well down in the Palaeoproterozoic. Among the organic remains seen in thin sections of the chert, the commonest are probably thin threads not unlike those so abundant in living mats and biofilms. Some of these show the kind of transverse striping that are typical of some ‘blue greens’; interestingly, the threads are narrower than they were later in the Precambrian (and narrower still than they are today). They are accompanied by a range of other tiny organisms, some generalised rod-like bacteria, others more distinctive, like the spherical Eosphaeria with its cell walls apparently divided into compartments, and the enigmatic Gunflintia. Palaeontologists continue to argue about the biological identity of some of these fossils, although it is beyond doubt that ‘blue greens’ were certainly present among them, but the important point is surely that this is an early community, already divided into different biological ‘trades’. The kind of prokaryote collaboration happening today was already happening then. Stromatolites were indeed true survivors.
But back in the 1960s, the fossil search was on! The world was scoured for younger, older, similar or, in particular, new and unnamed Precambrian small fossils. Africa, especially Namibia and Swaziland, was mapped and investigated; Australia, especially Western Australia, was crawled over; the Old World was looked at again, and much of the New World was looked at with new eyes. Precambrian fossils turned out to be very widespread, and new discoveries were nearly always heralded by someone spotting stromatolites in the field, which hinted at what might yet be found at the microscopic scale. Geologists’ boots tramped up wadis in deserts, their hammers whacked at Arctic cliffs, and their hand lenses focused on limestones outcropping deep in the Siberian taiga. These last devoted geologists bore the scars of marauding mosquitoes for weeks. Then by dissolving Precambrian shale in hydrofluoric acid still other microfossils with organic walls were extracted, to be studied in detail on microscope slides. University departments hired staff, and the growth in knowledge was exponential. Many of the famous names in early evolution were students of, or collaborated with, Elso Barghoorn. Andrew Knoll was among them. Bill Schopf, an equally grand figure at the University of California, Los Angeles, is now the elder statesman of the Barghoorn disciples, and did much to push the record of life and its fossils further back, into the Archaean.
Lynn Margulis may be the most luminous name of all those scientists associated with Barghoorn. She espoused and championed an idea that has transformed our way of understanding the history of life. There is a lot of hype in science nowadays, the more so since big claims often result in further research funding. I have never heard anybody announce ‘a minor discovery’ or ‘a modest advance’. I have also become allergic to the media’s phrase ‘the textbooks will have to be rewritten’ since it conjures up an inaccurate vision of textbooks being hurled with a curse into the waste paper basket on a regular basis. Textbooks are rewritten, but most scientific discoveries are passed from one edition to another, since science generally works by piling bricks of knowledge one on another to make a solid edifice. It is very unusual to scrap a whole chapter and start again. However, this does happen on occasion, and one such occasion was when it was claimed that eukaryote cells originated by a kind of piracy. The vital organelles within eukaryotic cells – things like mitochondria and chloroplasts – were originally free-living prokaryotes. The more complex cell was a result of a hijack, whereby former free-living bacteria were summarily tucked away inside the swag bag of a bigger descendant cell. Unlike the human hijack, though, all parties benefited: the scientific term is symbiosis. The formerly ‘free’ bacteria proliferated in their new habitat, sequestered away from harm. The newly enhanced cells took advantage of the novel vital functions tucked away inside them. For example, in plants the captured chloroplasts concentrated photosynthesis into special sites within the safety of a eukaryotic cell. Plants could now prosper using the energy of the sun. By contrast, mitochondria localise the ‘furnaces’ providing the chemical energy for life, which is essential for organisms to feed and grow. Malfunctions in these organelles are usually lethal, so deeply are they embedded in the ‘works’. Variegated varieties of garden plants can have white patches lacking chloroplasts, but such varieties are selected by gardeners for their appearance, not by nature for efficiency. Such an origin for complex cells is called the ‘endosymbiont theory’ – ‘endo’ meaning ‘inside’ symbiosis. Complex cells arose by incorporation of simpler ones, for mutual benefit. It altered our understanding of life’s early history to such an extent that not only had the textbooks to be rewritten, but there also had to be new books to replace the old ones in their entirety. The theory was triumphantly vindicated when the DNA of chloroplasts was investigated and found to be similar to that of free-living photosynthesising prokaryotes. The organelles tucked inside complex cells were, indeed, closely related to free-living, simple prokaryotes. This is the kind of confirmation that most of us can only dream about. It was almost as good as getting into a time machine and travelling back to the Precambrian. The phrase ‘endosymbiotic events’ was soon incorporated into foundation biology classes. Like all science, the story has got much more complicated since the initial insight, as more and more acts of cellular piracy have been detected, but all the complications serve to reveal yet more events deep in geological time.
6. Endosymbiotic/endosymbiont theory: a complex cell ‘in the making’ engulfs a formerly free-living prokaryote, which is then retained as a symbiont rather than being digested. This process happened several times, thereby introducing many more possibilities for life.
I should mention that none of these distinguished scientists conforms to the common preconceptions of the ‘geeky’ white-coated specialist. Bill Schopf is a bon viveur and raconteur, with a very persuasive laugh, and a relentless drive for discovery. Andrew Knoll is the kind of American who makes most of us poor Europeans feel as if we were only given half a ration of energy at birth. He has projects spanning most of the world, and a stable of exceptional students to take the work forward. He manages everything with a kind of urbane good humour and insouciance that defuses any possible resentment at his omniscience. Lynn Margulis is unique. I know of no other professor who would, or indeed could, quote the poet Emily Dickinson at length in a supermarket. As a long-term maverick she is always on the look out for ideas that will provoke and encourage new ideas (and completely undeterred that some of them may well prove to be wrong). Her dress style is equally distinctive, featuring embroidered waistcoats and pleated skirts, as if she were about to take part in a folk festival. She has an intuitive grasp of the important collaborations that makes the world work; not just the ubiquitous and versatile bacteria, but also chemistry, and geology, and politics.
This account of the geological importance of stromatolites and their discoverers has entailed a distraction from the little bubbles that provide the nub of this chapter. Recall the tiny gas beads rising from the top of the stromatolite in its tank, arising from a living biofilm breathing out oxygen. Now combine that scene with the picture I have attempted to paint of the fledgling earth in the Archaean and Proterozoic, where shallow seas and lagoons were covered with stromatolites, some of them gargantuan by recent standards. Imagine thousands and thousands of dimpled miles, exhaling oxygen by day in a thousand billion tiny bubbles, stimulated by the primeval sunshine. Even the slimy surface of the threads had a part to play in mitigating the effects of harmful ultra-violet radiation; we should all be grateful to slime. Now imagine this process continuing for billions of years, six times longer than the history of the velvet worm. The effect was to change the atmosphere, bubble by bubble. The early earth had little or no free oxygen; the ‘blue greens’ changed the air itself. Animals need to breathe oxygen to power their life functions. They could not exist before the slow, relentless preparation of the atmosphere effected by lowlier organisms on the tree of life: no gills, no lungs, no blood blue or red. If some malevolent God were instantly to reverse the work of the stromatolites we should all be gasping on the ground like beached trout within minutes. So we are, in a sense, the children of the sticky mounds.
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Richard Fortey
Тип: электронная книга
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Издательство: HarperCollins
Дата публикации: 28.04.2024
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О книге: This ebook edition does not include illustrations.An awe-inspiring journey through the eons and across the globe, in search of visible traces of evolution in the living creatures which have survived from earlier times and whose stories speak to us of seminal events in the history of life.The history of life on Earth is far older – and far odder – than many of us realise. In ‘Survivors’, acclaimed author Richard Fortey traces this history not through fossil records, but in the living stories of organisms that have survived nearly unchanged for hundreds of millions of years and whose existence today affords us tantalising glimpses of landscapes long vanished.For evolution has not obliterated its tracks. Scattered across the globe, strange and marvellous plants and animals have survived virtually unchanged since life first began. They range from humble algal mats dating back almost two billion years to hardy musk oxen, which linger as the last vestiges of Ice Age fauna.Following in Fortey’s questing footsteps, ‘Survivors’ takes us on a fascinating journey to these ancient worlds. On a moonlit beach in Delaware where the horseshoe crab shuffles its way through a violent romance, we catch a glimpse of life 450 million years ago, shortly after it diversified on the ocean floor. Along a stretch of Australian coastline, we bear witness to the sights and sounds that would have greeted a Precambrian dawn. Finally, in the dense rainforests of New Zealand where the secretive velvet worm burrows into the rotting timber of the jungle floor, we marvel at a living fossil which has survived unchanged since before the dissolution of the Gondwana supercontinent.Written with Fortey’s customary sparkle and gusto, this wonderfully engrossing exploration of the world’s oldest flora and fauna brilliantly combines the best science writing about the origins of life with an explorer’s sense of adventure and a poet’s wonder at the natural world. Utterly compelling, eye-opening and awe-inspiring, this is a book for anyone with an interest in evolution, in nature, in the remarkable scope of geological time and our own modest interaction with it – in short, in life itself.