COPYRIGHT

William Collins

An imprint of HarperCollinsPublishers 1 London Bridge Street London SE1 9GF

WilliamCollinsBooks.com

First published by William Collins Sons & Co. Ltd. and BBC Books:

a division of BBC Enterprises Ltd. in 1979

This eBook edition published by William Collins in 2018

Text © David Attenborough Productions Ltd. 1979, 2018

Photographs © individual copyright holders

The author asserts his moral right to be identified as the author of this work.

Cover Design: Heike Schüssler

Front Cover Photograph © Visuals Unlimited, Inc / Joe McDonald / Getty Images

A catalogue record for this book is available from the British Library.

All rights reserved under International and Pan-American Copyright Conventions. By payment of the required fees, you have been granted the non-exclusive, non-transferable right to access and read the text of this eBook on-screen. No part of this text may be reproduced, transmitted, downloaded, decompiled, reverse engineered, or stored in or introduced into any information storage and retrieval system, in any form or by any means, whether electronic or mechanical, now known or hereinafter invented, without the express written permission of HarperCollins Publishers.

Source ISBN: 9780008294281

Ebook Edition © October 2018 ISBN: 9780008294298

Version: 2018-08-09

CONTENTS

Cover

Title Page

Copyright

Prologue

1 The Infinite Variety

2 Building Bodies

3 The First Forests

4 The Swarming Hordes

5 The Conquest of the Waters

6 The Invasion of the Land

7 A Watertight Skin

8 Lords of the Air

9 Eggs, Pouches and Placentas

10 Theme and Variation

11 The Hunters and the Hunted

12 A Life in the Trees

13 The Compulsive Communicators

Epilogue

Index

Acknowledgements

About the Publisher

Pygmy sunbird (Hedydipna platura) adult male on flower, The Gambia, West Africa.

PROLOGUE

I still recall, with great clarity, the very first time I went to the tropics. Stepping out of the plane and into the muggy, perfumed air of West Africa was like walking into a steam laundry. Moisture hung in the atmosphere so heavily that my skin and shirt were soaked within minutes. A hedge of hibiscus bordered the airport buildings. Sunbirds, glittering with green and blue iridescence, played around it, darting from one scarlet blossom to another, hanging on beating wings as they probed for nectar. Only after I had watched them for some time did I notice, clasping a branch within the hedge, a chameleon, motionless except for its goggling eyes, which swivelled to follow every passing insect. Beside the hedge, I trod on what appeared to be grass. To my astonishment, the leaflets immediately folded themselves flat against the stem, transforming green fronds into apparently bare twigs. It was sensitive mimosa. Beyond lay a ditch covered with floating plants. In the spaces between them, the black water rippled with fish, and over the leaves walked a chestnut-coloured bird, lifting its long-toed feet with the exaggerated care of a man in snowshoes. Wherever I looked, I found a prodigality of pattern and colour for which I was quite unprepared. It was a revelation of the splendour and fecundity of the natural world from which I have never recovered.

Since then, I have managed, one way or another, to get back to the tropics many times. Usually my purpose has been to make a film about some corner of that infinitely varied world. So I have had the luck to find and film rare creatures that few outsiders have seen in the wild, and to gaze on some of the most marvellous spectacles that the wild places of the world have to offer – a tree full of displaying birds of paradise in New Guinea, giant lemurs leaping through the forest of Madagascar, the biggest lizards in the world prowling, like dragons, through the jungle of a tiny island in Indonesia.

Initially, the films we made tried to document the lives of particular animals showing how each found its food, defended itself and courted, and the ways in which it fitted into the community of animals and plants around it. But then the idea formed in my mind that a group of us might make a series of films that portrayed animals in a slightly different way. Our subject would be not only natural history in the sense that those two words are normally used, but the history of nature. We would try to survey the whole animal kingdom and consider each great group of animals in the light of the part it has played in the long drama of life from its beginnings until today. This book originated from the three years of travelling and research that went into the making of those films.

The condensation of three thousand million years of history into three hundred or so pages, and the description of a group of animals containing tens of thousands of species within one chapter, compels vast omissions. My method was to try to perceive the single most significant thread in the history of a group and then concentrate on tracing that, resolutely ignoring other issues, no matter how enticing they may seem.

This, however, risks imposing an appearance of purpose on the animal kingdom that does not exist in reality. Darwin demonstrated that the driving force of evolution comes from the accumulation, over countless generations, of chance genetic changes sifted by the rigours of natural selection. In describing the consequences of this process it is only too easy to use a form of words that suggests that the animals themselves were striving to bring about change in a purposeful way – that fish wanted to climb on to dry land and to modify their fins into legs, that reptiles wished to fly, strove to change their scales into feathers and so ultimately became birds. There is no objective evidence of anything of the kind and I have endeavoured, while describing these processes in a reasonably succinct way, not to use any phrases that might suggest otherwise.

To a surprising degree, nearly all the major events in this history can be told using living animals to represent the ancestral creatures which were the actual protagonists. The lungfish today shows how lungs may have developed; the mouse deer represents the first hoofed mammals that browsed in the forests of fifty million years ago. But misunderstandings can come unless the nature of this impersonation is made quite clear. In rare instances, a living species seems to be identical with one whose remains are fossilised in rocks several hundred million years old. It happens to have occupied a niche in the environment that has existed unchanged for such vast periods of time and suited it so ideally that it had no cause to change. In most cases, however, living species, while they may share essential characters with their ancestors, differ from them in many ways. The lungfish and the mouse deer are fundamentally similar to their ancestors, but they are by no means identical. To underline this distinction each time with a phrase like ‘ancestral forms that closely resemble the living species’ would be unnecessarily clumsy and literal-minded, but that qualifying phrase must be taken as read whenever I have referred to an ancient creature by the name of a living one.

Since this book was first written, science of course has continued to make new discoveries that have illuminated and amplified the history of nature. New species – some living, some fossil – have been discovered that link different groups. Some discoveries have been truly sensational. Perhaps the most dramatic have been those made in China of small dinosaurs with the clearly identifiable remains of feathers covering many parts of their bodies. They have cleared up one of the great and most vehement arguments among evolutionary biologists about the origins of both flight and the birds. Another concerns the very origins of life itself. Fossils have been found not only in Australia but in many other parts of the world, including the Avalon peninsula in northern Canada where a seabed thronged with all kinds of hitherto unknown organisms and dating from around 565 million years ago has been preserved with astounding perfection. All these advances in knowledge and many more will be mentioned in the appropriate places in the text that follows.

Spriggina fossil, leaf-like impression on sandstone, Ediacaran era (575 million years old), Australia.

One whole new branch of science has in recent years spread a great deal of light on the history of life – molecular genetics. Nearly a century after the publication of Darwin’s book on evolution by natural selection, On the Origin of Species, Crick and Watson described the structure of deoxyribonucleic acid – DNA for short – the molecule that carries the genetic blueprint from which another individual animal can be developed. This explained the mechanism by which physical characteristics are passed from one generation to the next.

The first organism to have its version completely deciphered was a small worm. Once that was done, the next great target was to analyse human DNA. That took many years of both international competition and cooperation. Today, however, it is possible to establish genetic identity of a species in a few hours using a piece of apparatus no bigger than a mobile phone. With such knowledge and techniques. all kinds of things can now be deduced – the relationship between individual species, the date in its evolutionary history at which any particular characteristic appeared, and even the precise way in which it did so. So the connections between the various groups that appear in our story can now be determined and statements about ancestry made with real confidence. Such new insights will be described in this new edition in their appropriate places in the pages that follow.

I have used familiar English names rather than scientific Latin ones so that when an animal makes its appearance in this history, it is quickly recognised for what it is. Those who wish to discover more about it in more technical books will find its scientific name in the index. For the most part, I have expressed age in absolute terms of millions of years rather than use the adjectival names of periods coined by classical geology. Lastly, I have made no reference by name to those many scientists whose work has provided the facts and theories on which the following pages are based. This has been done solely to try to maintain clarity in the narrative. I intend no minimisation of the debt owed to them by all of us who take pleasure in watching and thinking about animals. They and their researches have provided us with that most valuable of insights, the ability to perceive the continuity of nature in all its manifestations and to recognise our place within it.

ONE

The Infinite Variety

It is not difficult to discover an unknown animal. Spend a day in the tropical forest of South America, turning over logs, looking beneath bark, sifting through the moist litter of leaves, followed by an evening shining a mercury lamp on a white screen, and one way or another you will collect hundreds of different kinds of small creatures. Moths, caterpillars, spiders, long-nosed bugs, luminous beetles, harmless butterflies disguised as wasps, wasps shaped like ants, sticks that walk, leaves that open wings and fly – the variety will be enormous and one of these creatures is quite likely to be undescribed by science. The difficulty will be to find specialists who know enough about the groups concerned to be able to single out the new one.

No one can say just how many species of animals there are in these greenhouse-humid dimly lit jungles. They contain the richest and the most varied assemblage of animals and plant life to be found anywhere on earth. Not only are there many major categories of creatures – monkeys, rodents, spiders, hummingbirds, butterflies – but most of those types exist in many different forms. There are over forty different species of parrot, over seventy different monkeys, three hundred hummingbirds and tens of thousands of butterflies. If you are not careful, you can even be bitten by a hundred different kinds of mosquito.

Marine iguana (Amblyrhynchus cristatus) underwater, Fernandina Island, Galapagos Islands, Ecuador.

In 1832 a young Englishman, Charles Darwin, twenty-four years old and naturalist on HMS Beagle, a brig sent by the Admiralty in London on a surveying voyage round the world, came to such a forest outside Rio de Janeiro. In one day, in one small area, he collected sixty-eight different species of small beetle. That there should be such a variety of species of one kind of creature astounded him. He had not been searching specially for them so that, as he wrote in his journal, ‘It is sufficient to disturb the composure of an entomologist’s mind to look forward to the future dimensions of a complete catalogue’. The conventional view of his time was that all species were immutable and that each had been individually and separately created by God. At the time, Darwin was far from being an atheist – he had, after all, taken a degree in divinity at Cambridge University – but he was deeply puzzled by this enormous multiplicity of forms.

During the next three years, the Beagle sailed down the east coast of South America, rounded Cape Horn and came north again up the coast of Chile. The expedition then sailed out into the Pacific until, 1,000 kilometres from the mainland, they came to the lonely archipelago of the Galapagos. Here Darwin’s questions about the creation of species recurred, for in these islands he found fresh variety. He was fascinated to discover that the Galapagos animals bore a general resemblance to those he had seen on the mainland, but differed from them in detail. There were cormorants, black, long-necked diving birds like those that fly low along Brazilian rivers, but here in the Galapagos, their wings were so small and with such stunted feathers that they had lost the power of flight. There were iguanas, large lizards with a crest of scales along their backs. Those on the continent climbed trees and ate leaves. Here on the islands, where there was little vegetation, one species fed on seaweed and clung to rocks among the surging waves with unusually long and powerful claws. There were tortoises, very similar to the mainland forms except that these were many times bigger, giants that a man could ride. The British Vice-Governor of the Galapagos told Darwin that even within the archipelago, there was variety: the tortoises on each island were slightly different, so that it was possible to tell which island they came from. Those that lived on relatively well watered islands where there was ground vegetation to be cropped, had a gently curving front edge to their shells just above the neck. But those that came from arid islands and had to crane their necks in order to reach branches of cactus or leaves of trees, had much longer necks and a high peak to the front of their shells that enabled them to stretch their necks almost vertically upwards.

The suspicion grew in Darwin’s mind that species were not fixed forever. Perhaps one could change into another. Maybe, thousands of years ago, birds and reptiles from continental South America had reached the Galapagos, unintentional passengers on the rafts of vegetation that float down the rivers and out to sea. Once there, they had changed, as generation succeeded generation, to suit their new homes until they became their present species.

The differences between them and their mainland cousins were only small, but if such changes had taken place, was it not possible that over many millions of years, the cumulative effects on a dynasty of animals could be so great that they could bring about major transformations? Maybe fish had developed muscular fins and crawled on to land to become amphibians; maybe amphibians in their turn had developed watertight skins and become reptiles; maybe, even, some ape-like creatures had stood upright and become the ancestors of man.

In truth the idea was not a wholly new one. Many others before Darwin had suggested that all life on earth was interrelated. Darwin’s revolutionary insight was to perceive the mechanism that brought these changes about. By doing so he replaced a philosophical speculation with a detailed description of a process, supported by an abundance of evidence, that could be tested and verified; and the reality of evolution could no longer be denied.

Put briefly, his argument was this. All individuals of the same species are not identical. In one clutch of eggs from, for example, a giant tortoise, there will be some hatchlings which, because of their genetic constitution, will develop slightly longer necks than others. In times of drought they will be able to reach leaves and so survive. Their brothers and sisters, with shorter necks, will starve and die. So those best fitted to their surroundings will be selected and be able to transmit their characteristics to their offspring. After a great number of generations, tortoises on the arid islands will have longer necks than those on the watered islands – one species will have given rise to another.

This concept did not become clear in Darwin’s mind until long after he had left the Galapagos. For twenty-five years he painstakingly amassed evidence to support it. Not until 1859, when he was forty-eight years old, did he publish it, and even then he was driven to do so only because another younger naturalist, Alfred Wallace, working in Southeast Asia, had formulated the same idea. He called the book in which he set out his theory in detail, On the Origin of Species by Means of Natural Selection, or the Preservation of Favoured Races in the Struggle for Life.

Since that time, the theory of natural selection has been debated and tested, refined, qualified and elaborated. Later discoveries about genetics, molecular biology, population dynamics and behaviour have given it new dimensions. It remains the key to our understanding of the natural world and it enables us to recognise that life has a long and continuous history during which organisms, both plant and animal, have changed, generation by generation, as they colonised all parts of the world.

There are now two direct sources of evidence for this history. One can be found in the genetic material in the cells of every living organism. The other lies in the archives of the earth, the sedimentary rocks. The vast majority of animals leave no trace of their existence after their passing. Their flesh decays, their shells and their bones become scattered and turn to powder. But very occasionally, one or two individuals out of a population of many thousands have a different fate. A reptile becomes stuck in a swamp and dies. Its body rots but its bones settle into the mud. Dead vegetation drifts to the bottom and covers them. As the centuries pass and more vegetation accumulates, the deposit turns to peat. Changes in sea level may cause the swamp to be flooded and layers of sand to be deposited on top of the peat. Over great periods of time, the peat is compressed and turned to coal. The reptile’s bones still remain within it. The great pressure of the overlying sediments and the mineral-rich solutions that circulate through them cause chemical changes in the calcium phosphate of the bones. Eventually they are turned to stone, but they retain the outward shape that they had in life, albeit sometimes distorted. On occasion, even their detailed cellular structure is preserved so that you can look at sections of them through the microscope and plot the shape of the blood vessels and the nerves that once surrounded them. In rare cases, even the colour of skin or feathers can be detected.

Saddleback Galapagos tortoise (Chelonoidis nigra hoodensis) in defensive posture, Espanola Island, Galapagos Islands.

Fossil ammonites (Arnioceras semicostatum), in a sample of rock from the lower Jurassic period (195 to 172 million years ago), Robin Hood’s Bay, Yorkshire, UK.

The most suitable places for fossilisation are in seas and lakes where sedimentary deposits that will become sandstones and limestones are slowly accumulating. On land, where for the most part rocks are not built up by deposition but broken down by erosion, deposits such as sand dunes are only very rarely created and preserved. In consequence, the only land-living organisms likely to be fossilised are those that happen to fall into water. Since this is an exceptional fate for most of them, we are never likely to know from fossil evidence anything approaching the complete range of land-living animals and plants that has existed in the past. Water-living animals, such as fish, molluscs, sea urchins and corals, are much more promising candidates for preservation. Even so, very few of these perished in the exact physical and chemical conditions necessary for fossilisation. Of those that did, only a tiny proportion happen to lie in the rocks that outcrop on the surface of the ground today; and of these few, most will be eroded away and destroyed before they are discovered by fossil hunters. The astonishment is that, in the face of these adverse odds, the fossils that have been collected are so numerous and the record they provide so detailed and coherent.

How can we date them? Since the discovery of radioactivity scientists have realised that rocks have a geological clock within them. Several chemical elements decay with age, producing radioactivity in the process. Potassium turns into argon, uranium into lead, rubidium into strontium. The rate at which this happens can be estimated. So if the proportion of the secondary element to the primary one in a rock is measured, the time at which the original mineral was formed can be calculated. Since there are several such pairs of elements decaying at different speeds, it is possible to make cross-checks.

This technique, which requires extremely sophisticated methods of analysis, will always remain the province of the specialist. But anyone can date many rocks in a relative way by simple logic. If rocks lie in layers, and are not grossly disturbed, then the lower layer must be older than the upper. So we can follow the history of life through the strata and trace the lineages of animals back to their beginnings by going deeper and deeper into the earth’s crust.

Near horizontal layers of sedimentary rock, cut through by the Colorado River, forming the Grand Canyon, USA.

The deepest cleft that exists in the earth’s surface is the Grand Canyon in the western United States. The rocks through which the Colorado River has cut its way still lie roughly horizontally, layer upon layer, red, brown and yellow, sometimes pink in early light, sometimes blue in the shadowed distance. The land is so dry that only isolated juniper trees and low scrub freckle the surface of the cliffs, and the rock strata, some soft, some hard, are clear and stark. Most of them are sandstones or limestones that were laid down at the bottom of the shallow seas that once covered this part of North America. When they are examined closely, breaks in the succession can be detected. These represent times when the land rose, the seas drained away and the seabed became dry so that the deposits that had accumulated on it were eroded away. Subsequently, the land sank again, seas flooded back and deposition restarted. In spite of these gaps, the broad lines of the fossil story remain clear.

A mule will carry you in an easy day’s ride from the rim to the very bottom of the Canyon. The first rocks you pass are already some 200 million years old. There are no remains of mammals or birds in them, but there are traces of reptiles. Close by the side of the trail, you can see a line of tracks crossing the face of a sandstone boulder. They were made by a small four-footed creature, almost certainly a lizard-like reptile, running across a beach. Other rocks, at the same level elsewhere, contain impressions of fern leaves and the wings of insects.

Halfway down the Canyon, you come to 400-million-year-old limestones. There are no signs of reptiles to be found here, but there are the bones of strange armoured fish. An hour or so later – and a hundred million years earlier – the rocks contain no sign of backboned animals of any kind. There are a few shells and worms that have left behind a tracery of trails in what was the muddy seafloor. Three-quarters of the way down, you are still descending through layers of limestone, but now there is no sign of fossilised life whatever. By the late afternoon, you ride at last into the lower gorge where the Colorado River runs green between high rock walls. You are now well over a vertical kilometre below the rim, and the surrounding rocks have been dated to the immense age of 2,000 million years. Here you might hope to find evidence for the very beginnings of life. But there are no organic remains of any kind. The dark fine-grained rocks lie not in horizontal layers like all those above, but are twisted and buckled and riven with veins of pink granite.

Are signs of life absent because these rocks and the limestones directly above are so extremely ancient that all such traces have been crushed from them? Could it be that the first creatures to leave any sign of their existence were as complex as worms and molluscs? For many years these questions puzzled geologists. All over the world, rocks of this antiquity were carefully searched for organic remains. One or two odd shapes were found, but most authorities dismissed these as patterns produced by the physical processes of rock formation that had nothing whatever to do with living organisms. Then during the 1950s, the searchers began to use high-powered microscopes on some particularly enigmatic rocks.

Around 1,600 kilometres northeast of the Grand Canyon, ancient rocks of about the same age as those beside the Colorado River outcrop on the shores of Lake Superior. Some of them contain seams of a fine-grained flint-like substance called chert. This was well known during the nineteenth century because the pioneers used it in their flintlock guns. Here and there, it contains strange white concentric rings a metre or so across. Were these merely eddies in the mud on the bottom of the primeval seas, or could they have been formed by living organisms? No one could be sure and the shapes were given the noncommittal name of stromatolite, a word derived from Greek meaning no more than ‘stony carpet’. But when researchers cut sections of these rings, ground them down into slices so thin that they were translucent and examined them through the microscope, they found, preserved in the chert, the shapes of simple organisms, each no more than one or two hundredths of a millimetre across. Some resembled filaments of algae; others, while they were unmistakably organic, had no parallels with living organisms; and some looked to be identical with the simplest form of life existing today: bacteria.

It seemed almost impossible to many people that such tiny things as microorganisms could have been fossilised at all. That relics of them should have survived for such a vast period of time seemed even more difficult to believe. The solution of silica which had saturated the dead organisms and solidified into chert was clearly as fine-grained and durable a preservative as exists. The discovery of the fossils in the Gunflint Chert stimulated further searches not only in North America but all over the world, and other microfossils were found in cherts in Africa and Australia. Some of these, astonishingly, pre-dated the Gunflint specimens by a billion years, and some scientists now claim to have found fossils from around 4 billion years ago, not long after the formation of the earth. But if we want to consider how life arose, fossils cannot help us, for the origin of life involved the interaction of molecules, which leave no fossil traces. To understand what scientists think happened we have to look back beyond even the earliest microfossils, to a time when the earth was completely lifeless.

In many ways the planet then was radically different from the one we live on today. There were seas, but the way the land masses lay bore no resemblance in either form or distribution to modern continents. Volcanoes were abundant, spewing noxious gases, ash and lava. The atmosphere consisted of swirling clouds of hydrogen, carbon monoxide, ammonia and methane. There was little or no oxygen. This unbreathable mixture allowed ultraviolet rays from the sun to bathe the earth’s surface with an intensity that would be lethal to modern animal life. Electrical storms raged in the clouds, bombarding the land and the sea with lightning.

Laboratory experiments were made in the 1950s to discover what might happen to these particular chemical constituents under such conditions. Such gases, mixed with water vapour, were subjected to electrical discharge and ultraviolet light. After only a week of this treatment complex molecules were found to have formed in the mixture, including sugars, nucleic acids and amino acids, the building blocks of proteins. We now know that such simple organic molecules can be found throughout the universe, including on interstellar bodies such as comets. But amino acids are not life, nor are they even necessary for life to exist. The experiment proved little about the origin of life.

All forms of life that exist today share a common way of transmitting genetic information, of telling cells what to do. It is a molecule called deoxyribonucleic acid, or DNA for short. Its structure gives it two key properties. First, it can act as a blueprint for the manufacture of amino acids; and second, it has the ability to replicate itself. With this substance, molecules had reached the threshold of something quite new. These two characteristics of DNA also characterise even the simplest of living organisms such as bacteria. And bacteria, besides being the simplest form of life we know, are also among the oldest fossils we have discovered.

The ability of DNA to replicate itself is a consequence of its unique structure. It is shaped like two intertwined helices. During cell division, these unzip, splitting the molecule along its length into two separate helices. Each then acts as a template to which other simpler molecules become attached until each has once more become a double helix.

The simple molecules from which the DNA is mainly built are of only four kinds, but they are grouped in trios and arranged in a particular and significant order on the immensely long DNA molecule. This order specifies how the twenty or so different amino acids are arranged in a protein, how much is to be made, in what tissue and when. A length of DNA bearing such information for a protein, or for how a protein should be expressed, is called a gene.

Occasionally, the DNA copying process involved in reproduction may go wrong. A mistake may be made at a single point, or a length of DNA may become temporarily dislocated and be reinserted in the wrong place. The copy is then imperfect and the proteins it will create may be entirely different. Changes in the DNA sequence can also be induced by chemicals or radiation. When this occurred in the first organisms on earth, evolution began, for such hereditary changes, brought about by mutation and errors, are the source of variations from which natural selection can produce evolutionary change.

Because all life shares DNA as the hereditary material, it is possible to compare DNA sequences in different organisms and show how they are related. Such is the progress of technology that it is now also possible to sequence all the DNA in an organism in a matter of hours, using a device the size of a mobile phone. The millions of DNA sequences that have been established, stored in databases and compared show us unequivocally that, just as Darwin predicted, all life on earth shares a common ancestor. Because parts of our DNA accumulate mutations at a constant rate, like a molecular clock, we can use DNA sequences to estimate when two species split apart. In general, genetic and fossil timings agree with each other, although genetic data do sometimes throw up surprises. Using this method we can estimate that the Last Universal Common Ancestor of all life on earth – commonly known as LUCA, and basically a population of simple bacteria – lived around 4 billion years ago. Everything we can see around us can trace its ancestry back to that group of cells.

Such vast periods of time baffle the imagination, but we can form some idea of the relative duration of the major phases of the history of life if we compare the entire span, from these first beginnings until today, with one year. That means that, roughly, each day represents around ten million years. On such a calendar, the Gunflint fossils of algae-like organisms, which seemed so extremely ancient when they were first discovered, are seen to be quite late-comers in the history of life, not appearing until the second week of August. In the Grand Canyon, the oldest worm trails were burrowed through the mud in the second week of November and the first fish appeared in the limestone seas a week later. The little lizard will have scuttled across the beach during the middle of December and humans did not appear until the evening of 31 December.

But we must return to January. The bacteria fed initially on the various carbon compounds that had taken so many millions of years to accumulate in the primordial seas, producing methane as a by-product. Similar bacteria still exist today, all over the planet. And that was all there was, for around five or six months of our year. Then, in the early summer of the year of life, so some time over 2 billion years ago, bacteria developed an amazing biochemical trick. Instead of taking ready-made food from their surroundings, they began to manufacture their own within their cell walls, drawing the energy needed to do so from the sun. This process is called photosynthesis. One of the ingredients required by the earliest form of photosynthesis is hydrogen, a gas that is produced in great quantities during volcanic eruptions.

Conditions very similar to those in which the early photosynthesising bacteria lived can be found today in such volcanic areas as Yellowstone in Wyoming. Here a great mass of molten rock, lying only a thousand metres or so, down in the earth’s crust, heats the rocks on the surface. In places, the ground water is well above boiling point. It rises up channels through the rocks under decreasing pressure until suddenly it flashes into steam and water spouts high into the air as a geyser. Elsewhere, the water wells up into steaming pools. As it trickles away and cools, the salts it gathered from the rocks on its way up, together with those derived from the molten mass far below, are deposited to form rimmed and buttressed basins, surrounded by tiers of terraces. In these scalding mineral-laden waters, bacteria flourish. Some grow into matted filaments and curds, others into thick leathery sheets. Many are brilliantly coloured, their intensity of hue varying during the year as the colonies wax and wane. The names given to these pools hint at the variety of the bacteria and the splendour of the effects they produce – Emerald Pool, Sulphur Cauldron, Beryl Spring, Firehole Falls, Morning Glory Pool and – a particularly rich one with several species of bacteria – Artists’ Paintpots.

Hot spring, its water coloured by bacteria, Yellowstone National Park, Wyoming, USA.

When you wander through this amazing landscape, you can smell sulphurated hydrogen, the unmistakable stench of rotting eggs, produced by the reaction of ground water with the molten rock far beneath. This is the source from which many of the bacteria here obtain their hydrogen, and as long as bacteria were dependent upon volcanic action for it, they could not spread widely. But other forms eventually arose which were able to extract hydrogen from a very much more widespread source – water. This development was to have a profound effect on all life to come, for if hydrogen is extracted from water, the element that remains is oxygen. The organisms that did this are barely more complex in structure than bacteria. They are sometimes called blue-green algae because they appeared to be close relatives of the green algae that are common in ponds, but now we realise they are similar to the ancestors of those algae, and they are referred to as cyanobacteria or, simply, blue-greens. The chemical agent which they contain, making it possible for them to use water in the photosynthetic process, is chlorophyll, which is also possessed by true algae and plants.

Blue-greens are found wherever there is constant moisture. You can often see mats of them, beaded with silver bubbles of oxygen, blanketing the bottoms of ponds. In Shark Bay, on the northwest coast of tropical Australia, they have developed in a particularly spectacular and significant form. Hamelin Pool, one small arm of this vast inlet, has its entrance blocked by a sand bar covered with eel grass. The flow of water in and out of the Pool is so greatly impeded that evaporation under the grilling sun has made the waters very salty indeed. As a result, marine creatures such as molluscs which would normally feed on blue-greens and keep them in check, cannot survive. The blue-greens, therefore, flourish uncropped just as they did when they were the most advanced form of life anywhere in the world. They secrete lime, forming stony cushions near the shores of the Pool and teetering columns at greater depths. Here is the explanation of those mysterious shapes seen in section in the Gunflint Chert. The blue-green pillars of Hamelin Pool are living stromatolites, and the groups of them standing on the sun-dappled seafloor are as close as we may ever get to a scene from the world of 2 billion years ago.

The arrival of the blue-greens marked a point of no return in the history of life. In ways we do not fully understand, the oxygen they produced eventually accumulated over the millennia to form the kind of oxygen-rich atmosphere that we know today. Our lives, and those of all other animals, depend on it. We need it not only to breathe but to protect us. Oxygen in the atmosphere forms a screen, the ozone layer, which cuts off most of the ultraviolet rays of the sun.

Life remained at this stage of development for a vast period. Then, around 2 billion years ago one single-celled life form found itself trapped inside another, in an entirely chance encounter. You can find examples of the kind of organisms it eventually produced in almost any patch of fresh water.

A drop from a pond, viewed through a microscope, swarms with tiny organisms, some spinning, some crawling, some whizzing across the field of vision like rockets. As a group they are often called the protozoa, or protists – the name means ‘first animals’, although they are now seen as a very disparate group, not all of which have any affinity with animals. They are all single cells, yet within their cell walls they contain much more complex structures than any bacterium possesses. One central packet, the nucleus, is full of DNA. This appears to be the organising force of the cell. Elongated bodies, the mitochondria, provide energy by burning oxygen in much the same way as many bacteria do. Many cells have a thrashing tail attached to them and this resembles a filamentous bacterium called a spirochete. Some also contain chloroplasts, packets of chlorophyll which, like blue-greens, use the energy of sunlight to assemble complex molecules as food for the cell. Each of these tiny organisms thus appears to be a committee of simpler ones. This, in effect, is what they are. The mitochondria are the descendants of the single-celled organism that was trapped some 2 billion years ago, say in June in the year of life, while the chloroplasts are descended from a trapped blue-green.

Protozoans reproduce by splitting into two, as bacteria do, but their internal structure is much more complex and their division, not surprisingly, is consequently an elaborate business. Most of the separate structures, the members of the committee, themselves split. Indeed, the mitochondria and chloroplasts, each with their own DNA as befits their origins as separate organisms, often do so independently of the division of the main cell. The DNA within the nucleus replicates in a particularly complex manner which ensures that all its genes are copied and that each daughter cell receives a complete duplicate set. There are, however, several other methods of reproduction practised by various protozoans on occasions. The details vary. The essential feature of all the techniques is that a shuffling of genes is involved. In some cases this takes place when two cells join up and exchange genes before breaking apart and then undergoing cell division some time later. In other cases, cells normally contain two complete sets of genes which, after shuffling, divide to make new cells with only one set. These cells are of two types – a large comparatively immobile one, and a smaller active one, driven by a flagellum. The first is called an egg and the second a sperm – for this is the dawning of sex. When the two types unite in a new amalgamated cell the genes are once again in two sets but in new combinations with genes from not just one parent but two. This may well be a unique combination which will produce a slightly different organism with new characteristics. Since the evolution of sex increased the possibilities of genetic variation, it also greatly accelerated the rate at which evolution could proceed as organisms encountered new environments.

Ciliated protozoan (Paramecium multimicronucleatum), scanning electron micrograph (SEM).

There are tens of thousands of species of protozoans. Some are covered by a coat of flailing threads or cilia, which with a coordinated beat drive the creature through the water. Others, including the amoeba, move by bulging out fingers from the main body and then flowing into them. Many of those that live in the sea secrete shells with the most elaborate structure of silica or calcium carbonate. These are among the most exquisite objects that the microscope-carrying explorer will ever encounter. Some resemble minuscule snail shells, some ornate vases and bottles. The most delicate of all are of shining translucent silica, concentric spheres transfixed by needles, gothic helmets, rococo belfries and spiked space capsules. The inhabitants of these shells extend long threads through pores with which they trap particles of food.

Other protists feed in a different way, photosynthesising with the aid of their packets of chlorophyll. These can be regarded as plants; the remainder of the group, which feed on them, as animals. The distinction between the two at this level, however, does not have as much meaning as such labelling might suggest, for there are many species that can use both methods of feeding at different times.

Some protists are just large enough to see with the naked eye. With a little practice, the creeping grey speck of jelly which is an amoeba can be picked out in a drop of pond water. But there is a limit to the growth of a single-celled creature, for as size increases, the chemical processes inside the cell become difficult and inefficient. Size, however, can be achieved in a different way – by grouping cells together in an organised colony.

One species that has done this is volvox, a hollow sphere, almost the size of a pinhead, constructed from a large number of cells, each with a flagellum. The striking thing about these units is that they are virtually the same as other single cells that swim by themselves and have separate existences. The constituent cells of volvox, however, are coordinated, for all the flagella around the sphere beat in an organised way and drive the tiny ball in a particular direction.

This kind of coordination between constituent cells in a colony was taken a stage further, probably between 800 and 1,000 million years ago – some time in October in our calendar – when sponges appeared. Sponges can grow to a very considerable size. Some species form soft shapeless lumps on the seafloor two metres or so across. Their surfaces are covered with tiny pores through which water is drawn into the body by flagella, and then expelled through larger vents. The sponge feeds by filtering particles from this stream of water passing through its body. The colonial bonds between its constituents are very loose. Individual cells may crawl about over the surface of the sponge like amoebae. If two sponges of the same species are growing close to one another, they may, as they grow, come into contact and eventually merge into one huge organism. If a sponge is forced through a fine gauze sieve so that it is broken down into separate cells, these will eventually reorganise themselves into a new sponge, each kind of cell finding its appropriate place within the body. Most remarkably of all, if you take two sponges of the same species and treat them both in this extreme way and then mix cells from the two, they will reconstitute themselves into a single mixed-parentage entity.

Massive barrel sponge (Xestospongia testudinaria) and diver. Tubbataha Reef National Marine Park, Palawan, Philippines.

Some sponges produce a soft, flexible substance around their cells which supports the whole organism. This, when the cells themselves have been killed by boiling and washed away, is what we use in our baths. Other sponges secrete tiny needles, called spicules, either of calcium carbonate or silica, which mesh together to form a scaffold in which the cells are set. How one cell orientates itself and produces its spicule so that it fits perfectly into the overall design is totally unknown. When you look at a complex sponge skeleton such as that made of silica spicules which is known as Venus’ flower basket, the imagination is baffled. How could quasi-independent microscopic cells collaborate to secrete a million glassy splinters and construct such an intricate and beautiful lattice? We do not know. But even though sponges can produce such miraculous complexities as this, they are not like other animals. They have no nervous system, no muscle fibres. The simplest creatures to possess these physical characteristics are the jellyfish and their relatives.

A typical jellyfish is a saucer fringed with stinging tentacles. This form is called a medusa after the unfortunate woman in a Greek myth who was loved by the god of the sea and as a result had her hair changed by a jealous goddess into snakes. Jellyfish are constructed from two layers of cells. The jelly which separates them gives the organism a degree of rigidity needed to withstand the buffeting of the sea. They are quite complex creatures. Their cells, unlike those of the sponge, are incapable of independent survival. Some are modified to transmit electric impulses and are linked into a network which amounts to a primitive nervous system; others are able to contract in length and so can be considered as simple muscles. There are also stinging cells with coiled threads inside them, the unique possessions of the jellyfish tribe. When food or an enemy comes near, the cell discharges the thread, which is armed with spines like a miniature harpoon and often loaded with poison. It is these cells in the tentacles that will sting you if you unluckily brush against a jellyfish when swimming.

Jellyfish reproduce by releasing eggs and sperm into the sea. The fertilised egg does not develop into another jellyfish directly but becomes a free-swimming creature quite different from its parents. It eventually settles down on the bottom of the sea and grows into a tiny flower-like organism called a polyp. In some species, this sprouts, through branching twigs, into other polyps. They filter-feed with the aid of tiny beating cilia. Eventually, the polyps bud in a different way and produce miniature medusae which detach themselves and wriggle away to take up the swimming life once more.

Portugese man o’war (Physalia physalis) split level showing float and tentacles, Indo-pacific.

This alternation of form between generations has allowed all kinds of variations within the group. The true jellyfish spend most of their time as free-floating medusae with only the minimum period fixed to the rocks. Others, like the sea anemones, do the reverse. For all their adult lives they are solitary polyps, glued to the rock, their tentacles waving in the water ready to trap prey that may touch them. Yet a third kind are colonies of polyps but ones that have, confusingly, given up their attachment to the sea bottom and sail free like medusae. The Portuguese man o’war is one of these. Chains of polyps dangle from a float filled with gas. Each chain has a specialised function. One kind produces reproductive cells; another absorbs sustenance from captured prey; another, heavily armed with particularly virulent stinging cells, trails behind the colony for up to fifty metres, paralysing any fish that blunder into it.

It seems an obvious assumption that these relatively simple organisms appeared very early in the history of animal life, but for a long time there was no proof that they actually did so. Hard evidence could only come from the rocks. Even if microorganisms can be preserved in chert, it is difficult to believe that a creature as large but as fragile and insubstantial as a jellyfish could retain its shape long enough to be fossilised. But in the 1940s some geologists noticed very odd shapes in the ancient Ediacara Sandstones of the Flinders Ranges in southern Australia. These rocks, now thought to be about 650 million years old, were believed to be completely unfossiliferous. Judging from the size of the sand grains of which they are composed and the ripple marks on the surface of their bedding planes, they had once formed a sandy beach. Very occasionally, flower-like impressions were detected on them, some the size of a buttercup, some as big as a rose. Could these be the marks left by jellyfish stranded on the beach, baked in the sun and then covered by a wash of fine sand by the next tide? Eventually enough of these shapes were collected and studied for it to be undeniable that this is just what they must be.

Since then, other assemblages of living organisms of this extreme age have been discovered in many parts of the world – the Charnwood Forest in the heart of England, Namib Desert in southwest Africa, on the flanks of the Ural Mountains and the shores of the White Sea in Russia. But the most impressive and richest of all these discoveries have been made on the Avalon peninsula in Newfoundland. There the rocks, which are around 565 million years old, are exposed in dramatic cliffs. The strata have been tilted and folded, as one might expect in deposits of such extreme age, but not so severely that they have destroyed or even seriously distorted the fossils they contain. These are so abundant that in places it is impossible to walk over the exposed surface of a layer without treading on examples that any museum in the world would regard as one of its greatest treasures. They have been preserved in extraordinary perfection, seemingly by falls of volcanic ash from nearby volcanoes which buried them almost instantaneously, so creating what have been called death masks. There is a rich variety of shapes that are still being catalogued – spindles, fronds, discs, mats, plumes and combs, by far the richest record of any of the communities that flourished in the seas of the world during this extremely ancient period. Many seem to be unrelated to anything alive today and may perhaps be regarded as evolution’s failed experiments. One or two, however, bear at least a superficial resemblance to living marine creatures called sea pens that are still common today.

The name sea pen was given them when people wrote with quills, and very apt it must have seemed, for not only are they shaped like feathers but their skeleton is flexible and horny. They grow sticking up vertically on sandy seafloors, some only a few centimetres long, some half as tall as a man. At night they are particularly spectacular for they glow with a bright purple luminescence, and if you touch them, ghostly waves of light pulsate along their slowly writhing arms.

Sea pens are also called soft corals. Stony corals, their relatives, often grow alongside them and they too are colonial creatures. Their history is not as ancient as that of the sea pens, but once they had appeared, they flourished in immense numbers. An organism that produces a skeleton of stone and lives in an environment where deposits of ooze and sand are being laid down is an ideal subject for fossilisation. Huge thicknesses of limestone in many parts of the world consist almost entirely of coral remains and they provide a detailed chronicle of the development of the group.

The coral polyps secrete their skeletons from their bases. Each is connected with its neighbours by strands that extend laterally. As the colony develops, new polyps form, often on these connecting sections, and their skeletons grow over and stifle earlier polyps. So the limestone the colony builds is riddled with tiny cells where polyps once lived. The living ones form only a thin layer on the surface. Each species of coral has its own pattern of budding and so erects its own characteristic monument.

Corals are very demanding in their environmental requirements. Water that is muddy or fresh will kill them. Most will not grow at depths beyond the reach of sunlight for they are dependent upon single-celled algae that grow within their bodies. The algae photosynthesise food for themselves and in the process absorb carbon dioxide from the water. This assists the corals in the building of their skeletons, and releases oxygen which helps the corals respire.

The first time you dive on a coral reef is an experience never to be forgotten. The sensation of moving freely in three dimensions in the clear sunlit water that corals favour is, in itself, a bewitching and other-worldly one. But there is nothing on land that can prepare you for the profusion of shapes and colours of the corals themselves. There are domes, branches and fans, antlers delicately tipped with blue, clusters of thin pipes that are blood red. Some seem flower-like, yet when you touch them they have the incongruous scratch of stone. Often different coral species grow beside one another, mingled with sea pens arching above and beds of anemones that wave long tentacles in the current. Sometimes you swim over great meadows that consist entirely of one kind of coral; sometimes in deeper water, you discover a coral tower hung with fans and sponges that extends beyond your sight into depths of darkest blue.

Purple sea pen (Virgularia gustaviana) on sandy sea bed. Rinca, Indonesia.

But if you swim only during the day, you will hardly ever see the organisms that have created this astounding scene. At night, with a torch in your hand, you will find the coral transformed. The sharp outlines of the colonies are now misted with opalescence. Millions of tiny polyps have emerged from their limestone cells to stretch out their minuscule arms and grope for food.

Coral polyps are each only a few millimetres across, but, working together in colonies, they have produced the greatest animal constructions the world had seen long before humans appeared. The Great Barrier Reef, running parallel to the eastern coast of Australia for over 1,600 kilometres can be seen from the moon. So if, some 500 million years ago, astronauts from some other planet passed near the earth, they could easily have noticed in its blue seas a few new and mysterious turquoise shapes; and from them they might have guessed that complex life on earth had really started.

Table corals (Acropora spp.) on remote reef. Komodo National Park, Indonesia.

TWO

Building Bodies

The Great Barrier Reef swarms with life. The tides surging through the coral heads charge the water with oxygen and the tropical sun warms it and fills it with light. All the main kinds of sea animals seem to flourish here. Phosphorescent purple eyes peer out from beneath shells; black sea urchins swivel their spines as they slowly perambulate on needle tip; starfish of an intense blue spangle the sand; and patterned rosettes unfurl from holes in the smooth surface of coral. Dive down through the pellucid water and turn a boulder. A flat ribbon, striped yellow and scarlet, dances gracefully away and an emerald green brittle star careers over the sand to find a new hiding place.

The variety at first seems bewildering, but leaving aside primitive creatures like jellyfish and corals which we have already described, and the much more advanced backboned fish, nearly all can be allocated to one of three main types: shelled animals, like clams, cowries and sea snails; radially symmetrical creatures, like starfish and sea urchins; and elongated animals with segmented bodies varying from wriggling bristle worms to shrimps and lobsters.

The principles on which these three kinds of bodies are built are so fundamentally different that it is difficult to believe that they can be related to one another except right at the very roots of the evolutionary tree. The fossil record bears this out. All three groups, being sea-dwellers, have left behind abundant remains, and the details of their separate dynastic fortunes can be traced through the rocks for hundreds of millions of years. The walls of the Grand Canyon show that animals without backbones, invertebrates, came into existence long before the vertebrates such as fish. But just below the layer of gently folded limestones that contain the earliest of the invertebrate fossils, the strata change radically. Here the rocks are highly contorted. They had once formed mountains. These were eroded and eventually covered with the sea that deposited the limestone now lying above them. The episode occupied many millions of years and during all that time there were no deposits. As a consequence, this junction in the rocks represents a huge gap in the record. To trace the invertebrate lines back to their origins, we must find another site where rocks were not only deposited continuously throughout this critical period, but have survived in a relatively undistorted condition.

Such places are few, but one lies in the Atlas Mountains of Morocco. The bare hills behind Agadir in the west are built of blue limestones so hard that they ring under the fossil hunter’s hammer. The beds of rock are slightly tilted but otherwise undistorted by earth movements. On the crest of the passes, the rocks yield fossils. They are not very many, but if you look hard enough you can collect quite a range of species. All fossils found anywhere in the world in rocks of this age can be placed in one or other of those three main groups we identified on the reef. There are tiny shells, the size of your little fingernail, called brachiopods; radially symmetrical organisms looking like stalked flowers called crinoids; and trilobites, segmented creatures that resemble woodlice.

The limestones at the top of the Moroccan succession are about 560 million years old. Beneath them lie more layers extending downwards for thousands of metres, seemingly unchanged in character. In them, surely, must be evidence about the origins of those three great invertebrate groups.

But it is not so. As you clamber down the mountainside over the strata, the fossils suddenly disappear. The limestone seems to be exactly the same as that at the head of the pass, so the seas in which it was laid down must surely have been very similar to those that produced fossiliferous rocks. There are no signs of a revolutionary change in physical conditions. It is simply that at one time the ooze covering the seafloor contained shells of animals – and before that it did not.

This abrupt beginning to the fossil record is not just a Moroccan phenomenon, though you can see it here more vividly than in most places. It occurs in almost all the rocks of this age throughout the world. The microfossils from the cherts of Lake Superior and South Africa show that life had started long, long before. In the theoretical year of life, shelled animals do not appear until early November. So the bulk of life’s history is undocumented in the rocks. Only at this late date, about 600 million years ago, did several separate groups of organisms begin to leave records of any abundance by secreting shells. Why this sudden change should have come about, we do not know. Perhaps before this time the seas were not at the right temperature or did not have the chemical composition to favour the deposition of the calcium carbonate from which most marine shells and skeletons are constructed. Whatever the reason, we have to look elsewhere for evidence of the origins of the invertebrates.

A living crinoid: the great west indian sea lily (Cenocrinus asterius), 180–250 metres depth, Caribbean.

Flatworm (Maiazoon orsaki) Raja Ampat, Irian Jaya, Indonesia, Pacific Ocean.

We can find some living clues back on the reef. Fluttering over the coral heads, hiding in the crevices or clinging to the underside of rocks, are flat leaf-shaped worms. Like jellyfish, they have only one opening to their gut through which they both take in food and eject waste. They have no gills and breathe directly through their skin. Their underside is covered with cilia which by beating enable them to glide slowly over surfaces. Their front end has a mouth below and a few light-sensitive spots above so that the animal can be said to have the beginnings of a head. These flatworms are the simplest creatures to show signs of such a thing.

Eye-spots, to be of any use, must be linked to muscles so that the animal can react to what it senses. In flatworms all that exists is a simple network of nerve fibres. There are a few thickenings in some of them, but these can hardly be described as brains. Yet the flatworms can learn the kind of things that would help even this simplest of animals to survive, such as avoiding a particularly dangerous place or remembering where food can be found.

Today we know of some 3,000 species of flatworm in the world. Most are tiny and water-living. You can find freshwater ones in most streams simply by dropping a piece of raw meat or liver into the water. If the underwater vegetation is thick, flatworms are likely to glide out in some numbers and settle on the bait. In humid tropical forests, the ground is usually moist enough for some species to live on land, and many are likely to appear, undulating on the mucus that they secrete from their undersides. One of these species grows to a length of about 60 centimetres. Other flatworms have taken to the parasitic life and live unseen within the bodies of other animals – including us.

Liver flukes still retain the typical flatworm form. Tapeworms are also members of the group, though they look very different, for after burying their heads in the walls of their host’s gut, they bud off egg-bearing sections from their tail end. These segments remain attached while they mature, eventually forming a chain that may be as much as 10 metres long. The whole creature, as a result, looks as though it is divided into segments, but in fact these separate living packets of eggs are quite different from the permanent internal compartments of a truly segmented creature like an earthworm.

Flatworms are very simple creatures. Members of one free-swimming group lack a gut altogether and look very like the tiny free-swimming coral organisms before they settle down to a sedentary life. So there is little difficulty in believing those researchers who conclude from a study of the detailed structure of both adult and larva that the flatworms are descended from simpler organisms like corals and jellyfish.

During the period when these first marine invertebrates were evolving, between 600 and 1,000 million years ago, erosion of the continents was producing great expanses of mud and sand on the seabed around the continental margins. This environment must have contained abundant food in the form of organic detritus falling from the waters above as the single-celled organisms that floated in the surface waters died and drifted downwards. It also offered concealment and protection for any creature that lived within it. The flatworm shape, however, is not suited to burrowing. A tubular form is much more effective, and eventually worms with such a shape appeared. Some became active burrowers, tunnelling through the mud in search of food particles. Others lived half buried with their front end above the sediment. Cilia around their mouths created a current of water and from it they filtered their food.

Some of these creatures lived in a protective tube. In time, the shape of the top of this was modified into a collar with slits in it. This improved the flow of water over the tentacles. Further modification and mineralisation eventually produced a two-part protective shell around the front end. These were the first brachiopods, including Lingulella, an example of a species that has existed virtually unchanged for hundreds of millions of years.

The front end of a brachiopod is really quite complicated. Within the shell, it has a mouth surrounded by a group of tentacles. They are covered with beating cilia which create a current in the water. Any food particles in it are caught by the tentacles and then passed by them down to the mouth. While doing this, the tentacles perform another and important function, for the water brings with it dissolved oxygen which the animal needs in order to respire. The tentacles absorb it and so, in effect, they become gills. The shell enclosing the tentacles not only gives protection to these soft delicate structures, but concentrates the water into a steady stream so that it flows more effectively over them.

The brachiopods elaborated this design considerably over the next million years or so. One group developed a hole at the hinge end of one of the valves through which the worm-like stalk emerged to fasten the animal into the mud. This gave the shell the look of an upside-down Aladdin oil lamp, with the stalk as the wick, and so the group as a whole gained the name of lamp shell. The tentacles within the shell eventually became so enlarged that they had to be supported by delicate spirals of limestone.

There are other shelled worms to be found alongside the brachiopods in these ancient rocks. In one kind the elaborated worm did not attach itself to the seafloor but continued to crawl about and secreted a small conical tent of shell under which it could huddle when in danger. This was the ancestor of the most successful group of all these shelled worms, the molluscs, and it too has a living representative, a tiny organism called Neopilina, which was dredged up in 1952 from the depths of the Pacific. Today there are about 80,000 different species of molluscs with about as many again known from their fossils. You can find some of them in your garden; they are the snails and the slugs.

Brachiopods (Glottidia albida).

The lower part of the molluscan body is called the foot. Its owner moves itself about by protruding the foot from the shell and rippling its undersurface. Many species carry a small disc of shell on the side of it which, when the foot is retracted into the shell, forms a close-fitting lid to the entrance. The upper surface of the body is formed by a thin sheet that cloaks the internal organs and is appropriately called the mantle. In a cavity between the mantle and the central part of the body, most species have gills which are continually bathed by a current of oxygen-bearing water, sucked in at one end of the cavity and expelled at the other.

The shell is secreted by the upper surface of the mantle. One whole group of molluscs has single shells. The limpet, like Neopilina, produces shell at an equal rate right round the circumference of the mantle and so builds a simple pyramid. In other species, the front of the mantle secretes faster than the rear and creates a shell in a flat spiral, like a watch spring. In yet others, maximum production comes from one side so that the shell develops a twist and becomes a turret. The cowrie concentrates its secretion along the sides of the mantle, forming a shell like a loosely clenched fist. From the slit along the bottom, it protrudes not only its foot but two sections of its mantle which in life may extend over each flank of the shell and meet at the top. These lay down the marvellously patterned and polished surface characteristic of cowries.

Blue limpet (Patella coerulea), showing underside.

The single-shelled molluscs feed not with tentacles within the shell like the brachiopods but with a radula, a ribbon-shaped tongue, covered with rasping teeth. Some use it to scrape algae from the rocks. Whelks have developed a radula on a stalk which they can extend beyond the shell and use to bore into the shells of other molluscs. Through the holes they have drilled, they poke the tip of the radula and suck out the flesh of their victim. Cone shells also have a stalked radula but have modified it into a kind of gun. They slyly extend it towards their prey – a worm or even a fish – and then discharge a tiny glassy harpoon from the end. While the tethered victim struggles, they inject a venom so virulent that it kills a fish instantly and can even be lethal to human beings. They then haul the prey back to the shell and slowly engulf it.

A heavy shell must be something of a handicap when actively hunting, and some carnivorous molluscs have taken to a faster if riskier life by doing without it altogether and reverting to the lifestyle of their flatworm-like ancestors. These are the sea slugs (nudibranchs) and they are among the most beautiful and highly coloured of all invertebrates in the sea. Their long soft bodies are covered on the upper side with waving tentacles of the most delicate colours, banded, striped and patterned in many shades. Though they lack a shell, they are not entirely defenceless, for some have acquired secondhand weapons. These species float near the surface of the water on their feathery extended tentacles and hunt jellyfish. As the sea slug slowly eats its way into its drifting helpless prey, the stinging cells of the victim are taken into its gut, complete and unsprung. Eventually these migrate within the sea slug’s tissues and are concentrated in the tentacles on its back. There they give just the same protection to their new owners as they did to the jellyfish that developed them.

Other molluscs, such as mussels and clams, have shells divided into two valves lke those of a brachiopod and thus are known as bivalves. These creatures are much less mobile. The foot is reduced to a protrusion that they use to pull themselves down into the sand. For the most part, they are filter feeders, lying with valves agape, sucking water in through one end of the mantle cavity and squirting it out through a tubular siphon at the other. Since they do not need to move, great size is no disadvantage. Giant clams on the reef may grow to be a metre long. They lie embedded in the coral, their mantles fully exposed, a zigzag of brilliant green flesh spotted with black, which pulsates gently as water is pumped through it. They can certainly be quite big enough for a diver to put his foot into, but he would have to be very incautious indeed to get trapped. Powerful though the clam’s muscles are, it cannot slam its valves shut. It can only heave them slowly together, and that gives plenty of notice of its intentions. What is more, even when the valves of a really large specimen are fully closed, they only meet at the spikes on the edge. The gaps between them are so big that if you plunge your arm through into the mantle, the clam is quite unable to grip it – though the experiment is a little less unnerving if it is tried first with a thick stick.

Some filter feeders like the scallops do manage to travel – by convulsively clapping their valves together and so making curving leaps through the water. By and large, however, adult bivalves live rather static lives and the spreading of the species into distant parts of the seabed is carried out by the young. The molluscan egg develops into a larva, a minuscule animated globule striped with a band of cilia, which is swept far and wide by ocean currents. Then, after several weeks, it changes its shape, grows a shell and settles down. The drifting phase of its life puts it at the mercy of all kinds of hungry animals, from other stationary filter feeders to fish, so in order that its species can survive, a mollusc must produce great numbers of eggs. And indeed it does. One individual may discharge as many as 400 million.

One branch of the molluscs, very early in the group’s history, found a way of becoming highly mobile and yet retaining the protection of a large and heavy shell – they developed gas-filled flotation tanks. The first such creature appeared about 500 million years ago. Its flat-coiled shell was not completely filled with flesh as is that of a snail, but had its hind end walled off to form a gas chamber. As the animal grew, new chambers were added to provide sufficient buoyancy for the increasing weight. This creature was the nautilus, and we can get an accurate idea of how it and its family lived because a few nautilus species, just like Lingulella and Neopilina, have survived to the present day.

A nudibranch (Eubranchus tricolor) on the seabed of a Scottish loch.

One of these species, the pearly nautilus, grows to about 20 centimetres across. A tube runs from the back of the body chamber into the flotation tanks at the rear so that the animal can flood them and adjust its buoyancy to float at whatever level it wishes. The nautilus feeds not only on carrion but on living creatures such as crabs. It moves by jet propulsion, squirting water through a siphon in a variation of the current-creating technique developed by its filter-feeding relatives. It searches for its prey with the help of small stalked eyes and tentacles that are sensitive to taste. Its molluscan foot has become divided into some ninety long grasping tentacles which it uses to grapple with its prey. In the centre of them it has a horny beak, shaped like that of a parrot and capable of delivering a lethal, shell-cracking bite.

About 400 million years ago, after some 100 million years of evolution, the nautiluses gave rise to a variant group with many more flotation chambers to each shell, the ammonites. These became much more successful than their nautilus relatives, and today their fossilised shells can be found lying so thickly that they form solid bands in the rocks. Those of some species grew as big as lorry wheels. When you find one of these giants embedded in the honey-coloured limestones of central England or the hard blue rocks of Dorset, you might think that such immense creatures could do little but lumber massively across the seabed. But where erosion has removed the outer shell, the elegant curving walls of the flotation chambers that are revealed remind you that these creatures may well have been virtually weightless in water and able, like the nautilus, to jet-propel themselves at some speed through the water.

About 100 million years ago, the ammonite dynasty began to dwindle. Perhaps there were ecological changes that affected their egg-laying habits. Maybe new predators had appeared. At any rate, many species died out. Other lines gave rise to forms in which the shells were loosely coiled or almost straight. One group took the same path as the sea slugs did in more recent times and lost their shells altogether. Eventually all the shelled forms except the pearly nautilus disappeared. But some shell-less ones survived and became the most sophisticated and intelligent of all the molluscs, the squids and cuttlefish and the octopus. These are the cephalopods.

The relics of the cuttlefish’s ancestral shell can be found deep within it. This is the flat leaf of powdery chalk, the cuttlebone, that is often washed up on the seashore. The octopus has no trace of a shell even within the flesh of its body, but one species, the argonaut, secretes from one of its arms a marvellous paper-thin version shaped very like a nautilus shell but without chambers, which it uses not as a home for itself but as a delicate floating chalice in which to lay its eggs.

The squid and cuttlefish have many fewer tentacles than the nautilus – only ten – and the octopus, as its name makes obvious, has only eight. Of the three creatures, the squids are much the more mobile and have lateral fins running along their flanks which undulate and so propel the animal through the water. All cephalopods can, like the nautilus, use jet propulsion on occasion.

Several nautilus (Nautilus pompilius) on a coral reef at night, Pacific.

Cephalopod eyes are very elaborate. In some ways they are even better than our own, for a squid can distinguish polarised light, which we cannot do, and their retinas have a finer structure, which means, almost certainly, that they can distinguish finer detail than we can. To deal with the signals produced by these sense organs they have considerable brains and very quick reactions.

Some squids grow to an immense size. The aptly named colossal squid lives in the seas around Antarctica. It can reach nearly 100 kilos in weight and measure six metres from the end of its body to the tip of its outstretched tentacles. Its rival for the claim to be the largest species of all is the giant squid. The biggest so far discovered have in fact been slightly smaller and substantially lighter. Although there are records of even larger specimens of this species, it seems that these were not accurate. Nevertheless, we are unlikely to have discovered the biggest individuals of either species, so the record may yet be broken. The eyes of these huge cephalopods are even larger than might be expected. The biggest recorded were 27 centimetres across and are the largest known eyes of any kind of animal, five times bigger, for example, than those of the blue whale. Why the squid should have such gigantic eyes is a mystery.

It could be, however, that they need extremely sensitive eyes to detect the presence of their great enemy – the sperm whale. Squid beaks are often found in the stomachs of sperm whales, and their heads often carry circular scars with diameters that match a squid’s suckers. So there seems little doubt that squids and whales regularly fight in the dark depths of the ocean. Maybe the squids’ huge eyes help them to detect the presence of the only animal big enough to hunt them.

The intelligence of all the cephalopods – octopus, squid and cuttlefish – is well known. Octopus have been observed disguising themselves from an approaching enemy by covering themselves with shells or picking up two halves of a coconut and hiding within. Many species in all three groups have an extraordinary ability to change their colour and shape. They can camouflage themselves by matching almost any environment and also signal to one another with patterns and shapes that sweep across their bodies. A female squid has even been filmed signalling to a male lying alongside her that she is not ready to mate, while at the same time displaying a pattern on the other side of her body to summon another male. Octopus and squid, two of the most advanced animals in the ocean which least resemble human beings, are among the few, it seems, that can rival mammals in their intellectual abilities.

But what of the second great category of animals without backbones, the one represented in ancient rocks by the flower-like crinoids? As these are traced upwards through the rocks, they become more elaborate and their fundamental structure becomes clearer. Each has a central body, the calyx, rising from a stem like the seedhead of a poppy. From this sprout five arms which, in some species, branch repeatedly. The surface of the calyx is made up of closely fitting plates of calcium carbonate, as are the stems and branches. Lying in the rocks, the stems look like broken necklaces, their individual beads sometimes scattered, sometimes still in loose snaking columns, as though their thread had only just snapped. Occasionally gigantic specimens are found with stems 20 metres long. These creatures, like the ammonites, have had their day, but a few species, sometimes called sea lilies, still survive in the ocean depths.

Bigfin squid (Sepioteuthis lessoniana) hovering in open water above a coral reef at night. Dampier Strait, Raja Ampat, West Papua, Indonesia. Tropical West Pacific Ocean.

Crinoid (feather star, centre) on a gorgonian (sea fan, red) with a Dendronephthya soft coral in the background, Andaman Sea, Thailand.

Sea lilies show that the calcium carbonate plates, in life, are embedded just under the skin. This gives their surface a curious prickly feel. In other families, related to the crinoids, the skin has spines and needles attached to it so the creatures are known as echinoderms, ‘spiny-skins’. The basic module on which the echinoderm body is built has a fivefold symmetry. The plates on the calyx are pentagons. Five arms extend from it, and all the internal organs occur in groups of five. Their bodies work by a unique exploitation of hydrostatic principles. Tube feet, each a thin tube ending in a sucker and kept firm by the pressure of water within, wave and curl in rows along the arms. The water for this system circulates quite separately from that in the body cavity. It is drawn through a pore into a channel surrounding the mouth and circulated throughout the body and into the myriads of tube feet. When a drifting particle of food touches an arm, tube feet fasten on to it and pass it on from one to another until it reaches the gutter that runs down the upper surface of the arm to the mouth at the centre.

Tube feet of a red cushion sea star (Oreaster reticulatus), Singer Island, Florida.

Though stalked sea lilies were the most abundant crinoid in fossil times, the commonest forms today are the feather stars. Instead of stalks, they have a cluster of curling roots with which they attach themselves to coral or rocks. In places on the Great Barrier Reef, they swarm in huge numbers, covering the floor of the tidal pools with a tufted coarse carpet of brown. When disturbed, however, they can suddenly swim away, writhing their five limbs like Catherine wheels.

The fivefold symmetry and the hydrostatically operated tube feet are such distinctive characteristics that they make other echinoderms very easy to recognise. The starfish and their more sprightly cousins, the brittle stars, both possess them. These creatures appear to be crinoids that have neither stalk nor rootlets and are lying in an inverted position with their mouths on the ground and their five arms outstretched. Sea urchins too are obviously related. They seem to have curled their arms up from the mouth as five ribs and then connected them by more plates to form a sphere.

The sausage-like sea cucumbers that sprawl on sandy patches in the reef are also echinoderms, although in most species their shelly internal skeletons are reduced to tiny structures beneath the skin. Most lie neither face up nor face down, but on their sides. At one end there is an opening called the anus, though the term is not completely appropriate for the animal uses it not only for excretion but also for breathing, sucking water gently in and out over tubules just inside the body. The mouth, placed at the other end, is surrounded by tube feet that have become enlarged into short tentacles. These fumble about in the sand or mud. Particles adhere to them and the sea cucumber slowly curls them back into its mouth and sucks them clean with its fleshy lips.

One highly specialised deep-sea sea cucumber, called a sea-pig, lives in the mud of the deep seabed at depths of up to 5,000 metres. They are rotund little creatures about 15 centimetres long and have large tube-like structures on their underside with which they rootle about in the mud. They have been filmed in the deep sea, assembled in herds, perhaps for reproduction or attracted by the smell of a new source of food drifting down from the surface.

If you pick up a sea cucumber, do so with care, for they have an extravagant way of defending themselves. They simply extrude their internal organs. A slow but unstoppable flood of sticky tubules pours out of the anus, fastening your fingers together in an adhesive tangle of threads. When an inquisitive fish or crab provokes them to such action, it finds itself struggling in a mesh of filaments while the sea cucumber slowly inches itself away on the tube feet that protrude from its underside. Over the next few weeks it will slowly grow itself a new set of entrails.

The echinoderms may seem, from a human point of view, to be a blind alley of no particular importance. Were we to imagine that life was purposive, that everything was part of a planned progression due to culminate in the appearance of the human species or some other creature that might rival us in dominating the world, then the echinoderms could be dismissed as of no consequence. But such trends are clearer in the minds of people than they are in the rocks. The echinoderms appeared early in the history of life. Their hydrostatic mechanisms proved a serviceable and effective basis for building a variety of bodies, but were not susceptible in the end to spectacular development. In the areas that suit them, they are still highly successful. A starfish on the reef can crawl across a clam, fasten its tube feet on either side of its gape and slowly wrench the valves apart to feed on the flesh within. The crown-of-thorns starfish occasionally proliferates to plague proportions and devastates great areas of coral. Crinoids are brought up in trawls from the deep sea several thousand at a time. If it is improbable that any further major developments will come from this stock, it is also unlikely, on the evidence of the last 600 million years, that the group will disappear as long as life remains possible at all in the seas of the world.

Panamic cushion sea stars (Pentaceraster cumingi) group on seafloor, Galapagos Islands.

The third category of creatures on the reef contains those with segmented bodies. In this instance, we do have fossil evidence of even earlier forms than the trilobites found in the Moroccan hills. The Ediacaran deposits in Australia which contain the remains of jellyfish and sea pens also preserve impressions of segmented worms. One species, a 5-centimentre-long animal named Spriggina after Reg Spriggs who first discovered the Ediacara fossils, has a crescent-shaped head and up to forty segments, fringed on either side by leg-like projections. What exactly it was, nobody can agree. No legs have been identified, but this may be a limitation in the process of fossilisation. Some scientists think it may represent a completely extinct group. One widely accepted possibility is that it was a kind of annelid worm related to the bristle worms that are so common on a reef and the earthworms that you can find in your garden.

Annelids have grooves encircling their body that correspond to the internal walls that divide its interior into separate compartments. Each of these is equipped with its own set of organs. On the exterior and on either side, there are leg-like projections sometimes equipped with bristles, and another pair of feathery appendages through which oxygen is absorbed. Within its body, each segment has a pair of tubes opening to the exterior from which waste is secreted. A gut, a large blood vessel and a nerve cord run from front to end through all the segments, linking and coordinating them.

Fossils can only tell us so much. Even the exceptionally well-preserved remains of Ediacara offer no clue about the connection between the segmented worms and the other early groups. However, there is one further category of evidence to be looked at – the larvae. The segmented worms have spherical larvae with a belt of cilia round their middles and a long tuft on top. These are almost identical to the larva of some molluscs, a strong indication that back in time the two groups sprang from common stock. The echinoderms, on the other hand, have a larva that is quite different, with a twist to its structure and winding bands of cilia around it. This group must have separated from the ancestral flatworms at a very early stage indeed, long before the split between the molluscs and the segmented worms. Geneticists, analysing the DNA of each of these groups, now confirm these deductions and reveal that there are two major groupings of bilaterally symmetrical animals. Octopus, crabs and flatworms form one group, while echinoderms, tunicates and all the backboned animals make up the other.

Segmentation may have developed as a way of enabling worms to increase their efficiency as burrowers in mud. A line of separate limbs down each side is clearly a very effective structure for this purpose and it could have been acquired by repeating the simple body unit to form a chain. The change must have taken place long before Ediacaran times, for when those rocks were deposited the fundamental invertebrate divisions were already established The Ediacaran fossils, in Australia where they were first discovered and in Britain, Newfoundland, Namibia and Siberia, now confirm these deductions. Thereafter their history remains virtually invisible for a 100 million years. Only after this vast span do we reach the period, 600 million years ago, represented by the Moroccan deposits and others throughout the world. By that time many organisms had, as we have seen, developed shells from which we can deduce their existence and shape, but not much more.

However, there is one exceptional fossil site dating from only a little later than those of Ediacara that provides far more detailed information about the bodies of animals than can come from mere shells. In the Rocky Mountains of British Columbia, the Burgess Pass crosses a ridge between two high snowy peaks. Close to its crest lies an outcrop of particularly fine-grained shales, and in these have been discovered some of the most perfectly preserved fossils in the world. The shales were laid down about 530 million years ago, close to the beginning of the Cambrian period in a basin of the seafloor at a depth of about 150 metres. It must have been sheltered by a submarine ridge, for there were no currents to disturb the fine sediments on the floor or to bring down oxygenated water from nearer the surface. Few animals lived in those dark stagnant waters. There are no signs of tracks or burrows. Once in a while, however, mud from the ridge above slipped down in a turbid cloud, carrying with it all kinds of small creatures, and dumped them there. Since there was neither oxygen to fuel the processes of decay nor any scavenging animals to feed on the bodies and destroy them, many of the tiny carcasses remained complete as the settling mud particles slowly entombed them, preserving even their softest body parts. Eventually the entire deposit became consolidated into shale. Earth movements elevated and folded great areas of these marine deposits during the building of the Rocky Mountains. Many parts of them were distorted and crushed until most traces of life in them were obliterated. But miraculously, this one small patch survived virtually undamaged.

Velvet worm (Peripatus novaezealandiae). Velvet worms are known as ‘living fossils’, having remained the same for approximately 570 million years.

The range of creatures it contains is far wider than that found in rocks of a similar age at any other site so far discovered. There are the jellyfish that Ediacara would lead us to expect. There are echinoderms, brachiopods, primitive molluscs and half a dozen species of segmented worms – further representatives of the lineage that stretches from the beaches of Ediacara to the Barrier Reef of today.

There are also several creatures which were rather more mysterious. Among the most abundant of these was a strange segmented creature with what seemed to be a line of legs on its underside. It looked rather like a shrimp, though mysteriously none of the species had a head. It was given the name Anomalorcaris: strange shrimp. There were also small disc-shaped fossils marked with lines radiating from its centre that looked somewhat like a tiny slice of pineapple, which was initially thought to be some kind of jellyfish. Perhaps strangest of all, there was an elongated segmented animal that appeared to have seven pairs of spiny stilt-like legs, and seven flexible tentacles along its back, each ending in a tiny mouth. It seemed so strange as to be almost nightmarish, and the researcher who studied it accordingly called it Hallucigenia.

Subsequent work, however, showed that these oddities were not the founder members of some wholly unsuspected animal groups. A very exceptional specimen of Anomalocaris showed that the ‘strange shrimps’ were not complete animals but just the forelimbs belonging to a much bigger creature that used them to grab its prey. And the pineapple slice was eventually shown to have in its centre minute teeth. It was a mouth that belonged to the same animal as the tentacles. Both these pieces of Anomalorcaris’ body apparently had a more heavily strengthened exoskeleton and so regularly became separated from the animal’s more easily decayed body. As for Hallucigenia, further research on other specimens showed that it had been reconstructed in an upside-down position. The spindly legs were in fact protective dorsal spines, and what had been considered tentacles were in reality its legs. It is now thought that it may be the first known member of a strange group called the lobopods which today includes odd little creatures called velvet worms.

The great variety of creatures in the Burgess Shales is a reminder of how incomplete our knowledge of all fossil faunas actually is. The ancient seas contained many more kinds of animals than we can ever know. In this one site, conditions allowed a uniquely large proportion to be preserved, but even this is only a hint of what must have once existed.

The Burgess Shales also contain superbly preserved examples of trilobites like those in the Moroccan limestones. Their body armour was constructed partly of calcium carbonate and strengthened by a horny substance called chitin, a material that forms the external skeletons of insects. But chitin, unlike skin, does not expand, so any animal with such an external chitinous skeleton has to shed it regularly if it is to grow – as indeed insects do today. Many of the trilobite fossils we find are in fact these empty suits of armour. Sometimes they are concentrated in great drifts, having been sorted by sea currents, as shells sometimes are when they are swept up on beaches today. The underwater avalanches in the Burgess Shales Basin, however, swept down not just discarded armour but living trilobites and buried them. Mud particles filtered into the animals’ bodies and preserved the finest details of their anatomy. So in them we can still see the paired jointed legs that are attached to each body segment, the feathery gill associated with each leg, two feelers at the front of the head, and the gut running the entire length of the body. Even the muscle fibres along the back, which enabled the animal to roll itself up into a ball, are still recognisable in some exceptional specimens.

Trilobites, as far as we know, were the first creatures on earth to develop high-definition eyes. They are mosaics, a cluster of separate components, each with its own lens of crystalline calcite orientated in the precise position in which it transmits light most efficiently, much like the eyes of today’s insects. One eye may contain 15,000 elements, and would have given its owner an almost hemispherical field of view. Late in the dynasty, some species developed an even more sophisticated kind of eye and one that has never been paralleled by any other animal. Here the components are fewer but larger. Their lenses are much thicker and it is thought that these species lived where there was little light and needed thick lenses to collect and concentrate what light there was. However, the optical properties of a simple calcite lens in contact with water are such that it transmits light in a diffused way and cannot bring it to a sharply focused point. To do this, a two-part lens is needed which has a waved surface at the junction between its two elements. And this is exactly what these trilobites evolved. The lower element of the double lens was formed by chitin and the surface between the two conforms to the mathematical principle that human scientists did not discover until 300 years ago when they tried to correct the spherical aberration of lenses in their newly invented telescopes.

As the trilobites spread through the seas of the world, they diversified into a great number of species. Many seem to have lived on the seafloor, chomping their way through mud. Some colonised the deep seas where there was little light and lost their eyes altogether. Others, to judge from the shape of their limbs, may well have paddled about, legs uppermost, scanning the seafloor below with their large eyes.

In due course, as creatures of many kinds and varying ancestries came to live on the bottom of the seas, the trilobites lost their supremacy. Two hundred and fifty million years ago, their dynasty came to an end. One relation alone survives, the horseshoe crab. It’s a misleading name for it is not a crab and only half its shell bears any resemblance to a horseshoe. Measuring 30 centimetres or so across, it is many times bigger than most known trilobites and its armour no longer shows any signs of segmentation. Its front section is a huge domed shield, on the front of which are two bean-shaped compound eyes. A roughly rectangular plate, hinged to the back of the shield, carries a sharp spike of a tail. But beneath its shell, the animal’s segmentation is clear. It has several pairs of jointed legs with pincers on the end, and behind these there are plate-like gills, large and flat like the leaves of a book.

Tower-eyed trilobite (Erbenochile erbeni) from the Timrahrhart Formation, Morocco.

Horseshoe crab (Limulus polyphemus) group spawning at high tide at sunset, Cape May, New Jersey.

Horseshoe crabs are seldom seen, for they live at considerable depths. Some inhabit Southeast Asian waters, others are found in the seas along the North Atlantic coast of America. Every spring, they migrate towards the coast. Then on three successive nights, when the moon is full and the tides are high, hundreds of thousands emerge from the sea. The females, their huge shells glinting in the moonlight, move towards the shore, dragging smaller males behind them. Sometimes four or five males, in their anxiety to reach a female, cling to one another and form a chain. As she reaches the edge of the water, the female half buries herself in the sand. There she sheds her eggs and the males release sperm. For kilometre after kilometre along the dark beaches, the living tide of horseshoe crabs is so thick that they form a continuous strip, like a causeway of giant cobbles. The breakers sometimes overturn them and they lie in the sand, with their legs waving, their stiff tails slowly swivelling, in an effort to lever themselves right side up. Many fail and are abandoned by the receding tide to die as thousands more swim in the shallows, pressing forward to take their turn.

This scene must have been enacted every spring for several hundred million years. When it began, the land was without life of any kind, and on such beaches the eggs were safe from sea-dwelling marauders. Perhaps this is why the horseshoe crabs developed the habit. Today beaches are not quite so safe, for hordes of gulls and small wading birds congregate to share the prodigious feast. But many of the fertilised eggs remain buried deep among the sand grains where they will stay for a month until, once more, high water reaches this part of the beach, stirring the sand and releasing the larvae to swim freely in the sea.

Although the trilobites were so successful, they were by no means the only armoured creatures to develop from the segmented worms. So did a group that must have been among the most alarming of all marine monsters – the sea scorpions, called scientifically the Eurypterids. Some grew to a length of two metres and were the largest arthropods ever known to have existed. However, in spite of their appearance and huge claws, many of them were filter feeders. Presumably, their fearsome claws were used in fights between one another rather than in subduing prey. Like the trilobites, they disappeared at the end of the Permian period.

One group related to the trilobites did however survive and today is extremely successful. They differed in one seemingly trivial but nonetheless diagnostic characteristic. They have not one but two pairs of antennae on their heads. They lived alongside the trilobites, comparatively unobtrusively for hundreds of millions of years, and then, when the trilobite dynasty came to an end, it was they who took over. They are the crustaceans. Today there are about 35,000 species of crustacean – seven times as many as there are of birds. Most prowl among the rocks and reefs – crabs, shrimps, prawns and lobsters. Some – the barnacles – have taken up a static life. Others – the krill which forms the food of whales – swim in vast shoals.

Robber crab (Birgus latro) climbing coconut tree, Aldabra Seychelles.

An external skeleton is highly versatile; it serves the tiny water flea as well as it does the giant Japanese spider crab that measures over three metres from claw to claw. Each crustacean species modifies the shape of its many paired legs for particular purposes. Those at the front may become pincers or claws; those in the middle, paddles, walking legs or tweezers. Some have feathery branches, gills through which oxygen is absorbed from the water. Others develop attachments so that they can carry eggs.

The limbs, which are tubular and jointed, are operated by internal muscles. These extend from the end of one section, along its length, to a prong from the next section which projects across the joint. When the muscle contracts between these two attachment points, the limb hinges. Such joints can only move in one plane, but crustaceans deal with that limitation by grouping two or three on a limb, sometimes close together, each working in a different plane so that the free end of the limb can move in a complete circle.

The external shell, however, gives the crustaceans the same problem as it gave the trilobites. It will not expand, and since it completely encloses their bodies, the only way they can grow is to shed it periodically. As the time for the moult approaches, the animal absorbs much of the calcium carbonate from its shell into its blood. It secretes a new, soft and wrinkled skin beneath the shell. The outgrown armour splits at the back and the animal pulls itself out, leaving the shell more or less complete, like a translucent ghost of its former self. Now, because the animal’s skin is soft, it must hide, but it grows fast and swells its body by absorbing water and stretching out the wrinkles of its new carapace. Gradually this hardens so the animal can again venture into a hostile world.

The hermit crab partly avoids this complicated and hazardous process by having a shell-less hind part and protecting it with a discarded mollusc shell, slipping into a new one in a minute or so whenever it has the need.

The external skeleton has one incidental quality which has had momentous results. Mechanically, it works almost as well on land as it does in water, so that, providing a creature can find a way of breathing, there is little to prevent it walking straight out of the sea and up the beach. Many crustaceans, indeed, have done so – sand shrimps and beach hoppers stay quite close to the sea; and pill bugs and penny sows have colonised moist ground throughout the land.

The most spectacular of all these land-living crustaceans is the robber crab. It is found on islands in the Indian Ocean and the western parts of the Pacific. At the back of its main carapace, at the junction with the first segment of its abdomen, there is an opening to an air chamber lined with moist puckered skin through which the animal absorbs oxygen. This monster is so big it can embrace the trunk of a palm tree between its outstretched legs. It climbs with ease, and once in the palm’s crest, cuts down with its gigantic pincers the young coconuts on which it feeds. It has to return to the sea to lay its eggs, but otherwise it is entirely at home on land.

Other descendants of the marine invertebrates have also left the water. Among the molluscs there are the snails and the shell-less slugs, but these emerged from water relatively recently in the group’s history. The first to make the move to land were probably descendants of the segmented worms, the millipedes. Their droppings have been found fossilised in the rocks of Shropshire. They were followed by pioneers which recent DNA studies show to have been crustaceans. And some of these made such a success of life in their new surroundings that they eventually gave rise to the most numerous and diverse group of all land animals – the insects.

THREE

The First Forests

There are few more barren places on earth than the plains surrounding a volcano in the aftermath of its eruption. Black tides of lava lie spilt over its flanks like slag from a furnace. Their momentum has gone but they still creak, and boulders still tumble as the flow settles. Steam hisses between the blocks of lava, caking the mouths of the vents with yellow sulphur. Pools of liquid mud, grey, yellow or blue, boiled by the subsiding heat from far below, bubble creamily. Otherwise all is still. No bush grows to give shelter from the scouring wind; no speck of green relieves the black surface of the empty ash plains.

This desolate landscape has been that of much of the earth for the greater part of its history. The first volcanoes to appear on the surface of the cooling planet erupted on a far greater scale than any that we know today, building entire mountain ranges of lava and ash. Over the millennia, the wind and rain destroyed them. Their rocks weathered and turned to clay and mud. Streams transported the debris, particle by particle, and strewed it over the seafloor beyond the margins of the land. As the deposits accumulated, they compacted into shales and sandstone.

Lava cactus (Brachycereus nesioticus) growing in lava field, coast of Fernandina, Galapagos Islands.

The continents were not stationary. They drifted slowly over the earth’s surface, driven by the convection currents moving deep in the earth’s mantle. When they collided, the sedimentary deposits around them were squeezed and rucked up to form new mountain ranges. As the geological cycles repeated themselves for some three thousand million years, and the volcanoes exploded and spent themselves, the land remained barren. In the sea, however, life burgeoned.

Some marine algae no doubt managed to live on the edges of the seas, rimming the beaches and boulders with green, but they could not have spread far beyond the splash zone, for they would have dried out and died. Then between 450 and 500 million years ago, some forms developed a waxy covering, a cuticle, which warded off desiccation. Even this, however, did not totally emancipate them from water. They could not leave it because their reproductive processes depended on it.

Algae reproduce themselves in two ways – by straightforward asexual division and by the sexual method, which is of great importance in the the evolutionary process. Sex cells will only develop further if they meet each other and fuse in pairs. To make these journeys and achieve these meetings, they need water.

This problem still besets the most primitive land plants living today – both the flat, moist-skinned ones known as liverworts, and the filamentous ones covered with green scales, the mosses. They use these two methods of reproduction, sexual and asexual, in alternate generations. The familiar green moss is the generation which produces the sex cells. Each large egg remains attached to the top of the stem, while the smaller microscopic sperms are released into water and wriggle their way up to fertilise it. The egg then germinates while still attached to the parent plant and produces the next asexual generation – a thin stem with, at its tip, a hollow capsule. In this, great numbers of grain-like spores are produced. When the atmosphere becomes dry, the capsule wall expands until it suddenly snaps apart, throwing the spores into the air to be distributed by the wind. Those that land on a suitably moist site then develop into new plants.

Moss filaments have no rigidity. Some kinds achieve a modest height by packing closely together in cushions and so giving one another support, but their soft, permeable, water-filled cells do not provide enough strength to enable individual stems to stand upright. Plants like these are very likely to have been among the earliest forms to colonise the moist margins of the land, but so far no fossil relics of undoubted mosses have been discovered from this early period.

The first land plants we have indentified, dating from over 400 million years ago, are simple leafless branching strands which occur as filaments of carbon in the rocks of central Wales and in some cherts in Scotland. Like mosses, they had no roots, but when their stems are carefully prepared and examined under the microscope, they are seen to contain structures that no moss possesses – long, thick-walled cells that must have conducted water up the stem. These structures gave them strength and enabled them to stand several centimetres tall. That may not sound very imposing, but it represented a major advance in life’s colonisation of the land.

Apple moss (Bartrimia pomiformis) with spore capsules, Inverness-shire, Scotland, UK.

Endive Pellia liverwort (Pellia endiviifolia) in centre growing through common liverwort (Marchantia polymorpha), the latter bearing cups containing gemmae (used in asexual reproduction). Lathkill Dale, Peak District National Park, Derbyshire, UK.

Such plants, together with primitive mosses and liverworts, formed green tangled carpets, miniature forests that spread inland from the edges of estuaries and rivers, and into these crept the first animal colonists from the sea. They were segmented creatures, ancestors of today’s millipedes, well suited by their chitinous armour to movement on land. At first they doubtless kept close to the edge of the water, but wherever there was moss there was both moisture and vegetable debris and spores to eat. With the land to themselves, these pioneering creatures flourished. Their name millipede, ‘thousand legs’, is something of an overstatement. No species alive today has many more than two hundred legs, and some have as few as eight. Nevertheless, some of them grew to magnificent dimensions. One of them was two metres long and must have had a devastating effect on the plants as it browsed its way through the wet green bogs. It was, after all, as long as a cow.

The external skeleton inherited from their water-living forebears needed few modifications for life on land, but the millipedes did have to acquire a different method of breathing. The feathery gill attached to a stalk alongside the leg that had served their aquatic relatives, the crustaceans, would not work in air. In its place, the millipedes developed a system of breathing tubes, the tracheae. Each tube begins at an opening on the flank of the shell and then branches internally into a fine network that leads ultimately to all the organs and tissues of the body, the tips even entering individual specialised cells called tracheoles that deliver gaseous oxygen to the surrounding tissues and also absorb waste.

Reproduction out of water, however, posed problems for the millipedes. Their marine ancestors had relied, like the algae, on water to enable their sperm to reach their eggs. On land the solution was an obvious one – male and female, being well able to move about, must meet and transfer the sperm directly from one to the other. This is exactly what millipedes do. Both sexes house their reproductive cells in glands close to the base of the second pair of legs. When the male meets the female in the mating season, the two intertwine. The male reaches forward with his seventh leg, collects a bundle of sperm from his sex gland and then clambers alongside the female until the bundle is beside her sexual pouch and she is able to take it in. The process looks rather laborious but at least it is not dangerous. Millipedes are entirely vegetarian. Fiercer invertebrates, which came to the moss jungles to prey on this grazing population of millipedes, could not indulge in such trusting relationships.

Three groups of these predatory creatures still survive today – centipedes, scorpions and spiders. Like their prey, they are members of the segmented group of animals, though the degree to which they have retained divisions in their bodies varies considerably. The centipedes are as clearly and extensively segmented as their close relatives the millipedes. The scorpions show divisions only in their long tails; and most spiders have completely lost all signs of segmentation, except for a few Southeast Asian species which retain clearly recognisable relics of their segmented past.

The scorpions that live today have not only fearsome-looking claws but a large venom gland drooping from the end of a long thin tail with a sharp curving sting. Their copulations cannot be the somewhat hit-and-miss gropings practised by the millipedes. Approaching such an aggressive and powerful creature is a dangerous enterprise even if the move is made by another individual of the same species and its intentions are purely sexual. There is a real risk of it being regarded not as a mate but a meal. So scorpion mating demands, for the first time among the animals that have appeared so far in this history, the ritualised safeguards and placations of courtship.

The male scorpion approaches the female with great wariness. Suddenly he grabs her pincers with his. Thus linked, with her weapons neutralised, the pair begin to dance. Backwards and forwards they move with their tails held upright, sometimes even intertwined. After some time, their shuffling steps have cleared the dancing ground of much of its debris. The male then extrudes a packet of sperm from the genital opening beneath his thorax and deposits it on the ground. Still grasping the female by the claws, he jerks and heaves her forward until her sexual opening, also on her underside, is brought directly above the sperm packet. She takes it up, the partners disengage and then go their separate ways. The eggs eventually hatch inside the mother’s pouch, the young crawl out and clamber up on to her back. There they stay for about a fortnight until they have completed their first moult and can fend for themselves.

Mediterranean/European scorpion (Buthus occitanus) stinging a spider (Amourobius sp.).

Spiders, too, must be extremely cautious in their courtship. Matters are made even more hazardous for the male because he is nearly always smaller than the female. And he prepares for his encounter with his mate long before he meets her. He spins a tiny triangle of silk a few millimetres in length and deposits a drop of sperm on to it from the gland that lies underneath his body. He then sucks it into the hollow first joint of his pedipalp, a special limb at the front of his body. Now he is ready.

The courtships of spiders are beguilingly various and ingenious. Jumping spiders and wolf spiders hunt primarily by sight and have excellent eyes. The courting male, consequently, relies on visual signals to make the female aware of his presence and his purpose. His pedipalps are brightly coloured and patterned, and as soon as he sights a female, he begins to signal with them in a kind of manic semaphore. Nocturnal spiders, on the other hand, depend largely on an extremely delicate sense of touch to find their prey. When they meet one another, they gingerly caress each other’s long legs, and only after a great deal of hesitation do they come to closer quarters. Web-making spiders are sensitive to the vibrations on their silken threads that tell them when a victim has blundered into the web. So when the male of such a species approaches a female hanging, large and menacing, on her web, or lurking hidden beside it, he signals to her by twanging the threads at one side in a special and meaningful way which he trusts the female will recognise. Other species put their faith in bribery. The male catches an insect and carefully parcels it up in silk. Holding this in front of him, he cautiously approaches the female and presents it to her. While she is occupied in examining the gift, he quickly scuttles over her and ties her to the ground with bonds of silk. Only then does he risk an embrace.

All these techniques lead to the same conclusion. The male, having survived every danger, places his pedipalp close to the female’s genital opening, squirts out the sperm and then hastily retreats. It has to be recorded that in spite of all his precautions he sometimes fails to make his getaway in time and the female eats him after all. But in terms of the transmission of his genes, the male’s disaster is of limited consequence: he lost his life after, not before, he had completed his purpose.

While the early segmented animals were perfecting their adaptations for living on land and away from moisture, the plants were also changing. Neither the mosses nor the other early forms had true roots. Their short upright stems sprang from a horizontal one of a similar character lying along the ground or just below it. This construction served well enough in moist surroundings, but in many parts of the world the only permanent water supply lies below the ground. To tap that requires roots that probe deep between the particles of the soil and can absorb the film of water that clings to them in all except the most arid environments. Three groups of plants appeared that possessed such structures, and all three have descendants that have survived without much change: club mosses, which resemble mosses but have stiffer stems; horsetails, which grow in waste patches and ditches and have stems encircled at intervals with rings of needle-like leaves; and ferns.

Wolf spiders (Pardosa sp.), male (right) waving palps in courtship display, Derbyshire, UK.

The ferns, early in their history, had developed a special protein to protect themselves from damage by ultraviolet light, something that had not been a problem for their ancestors since they lived in water where such wavelengths could not reach them. This substance now slowly changed into a material called lignin. This is the basis of wood, and it gave them the rigidity needed to grow tall. So a new kind of competition developed between plants.

All green plants depend on light to power the chemical processes by which they use simple elements to synthesise their body substances. So if a plant does not grow tall, it risks being overshadowed by its neighbours and condemned to shade where, starved of light, it might die. So these early groups used the newly acquired strength of their stems to grow very tall indeed. They became trees. The club mosses and horsetails were still, for the most part, swamp-dwellers, and there they now stood in dense ranks, thirty metres tall, some with woody trunks two metres in diameter. The compacted remains of their stems and leaves today form coal. The great thicknesses of the seams are impressive evidence of the abundance and persistence of the early forests. Other species of both these groups also spread farther inland and there mingled with ferns. These had developed true leaves, large spreading structures with which to collect as much light as possible. They grew tall with curving trunks, like the tree ferns that still thrive in tropical rainforests.

Wood horsetails (Equistetum sylvaticum) Columbia River, Gorge National Scenic Area, Oregon, USA.

The height of these first forests must have caused considerable problems for their animal inhabitants. Once, there had been a superabundance of leaves and spores close to the ground. Now the soaring trunks had raised this source of food high in the sky, creating a dense canopy that cut out much of the light. The floor of these forests was, at best, only sparsely vegetated and great areas may have been entirely without any living leaves. Some of the multi-legged vegetarians found their fodder by clambering up the trunks.

There may have been another factor that induced these creatures to leave the ground. About this time, animals of a completely new kind joined the invertebrates on the land. They had backbones and four legs and wet skins. They were the first amphibians and they too were carnivorous. A description of their origins and fate will have to wait until we have followed the development of the invertebrates to its climax, but their presence at this stage must be mentioned if the scene in these first jungles is not to be misrepresented.

Virtually all of the new-style invertebrate families still survive. Among the most numerous are the bristletails and springtails. Although they are little known and infrequently seen, they are enormously abundant. There is hardly a spadeful of soil or leaf litter anywhere in the world that does not contain some of them. Indeed, the springtails, or collembola, are probably the most abundant arthropods on the planet. Most are only a few millimetres long. Of those new families, only one is commonly noticed – the silverfish that glides smoothly across cellar floors or is occasionally discovered making a meal of the dried glue in the bindings of books. Its body is clearly segmented but it has very many fewer divisions than the millipede. It has a well-defined head with compound eyes and antennae; a thorax bearing three pairs of legs, the result of fusing together three segments; and a segmented abdomen which, while it no longer carries limbs on each segment, retains little stumps as signs that it once possessed them. Three thin filaments trail from its rear end. It breathes like the millipedes by means of tracheae, and it reproduces in a manner reminiscent of those early land invertebrates, the scorpions. The male silverfish deposits a bundle of sperm on the ground and then, one way or another, he entices the female to walk over it. When that happens, she is stimulated to take it up into her own sexual pouch.

There are several thousand different species of bristletails and collembola. They vary considerably in their anatomy and, as is often the case when considering the simpler members of a big group, it is sometimes difficult to decide whether a particular characteristic represents a truly primitive survival or one that has become secondarily reduced to suit a particular way of life. The silverfish, for example, has compound eyes but other members of the group are blind. All lack wings. Some even lack tracheae and breathe through their chitinous skeleton which is particularly thin and permeable. Is this because they never had them or because they have lost them?

Marine springtail/bristletail (Petrobius maritimus) adult resting on stones, Lough Muree, County Clare, Ireland.

Many such debatable questions raised by the anatomy of these creatures still wait universally agreed answers. However, they all have six legs and tripartite bodies and these characteristics clearly link them to that great and varied group of land invertebrates, the insects. They appeared many millions of years after the earlier groups were well established. Geneticists have now shown that collembolla, as well as the insects, including the silverfish, are all closely related to one particular group of water-living crustaceans, the remipedia (the name means ‘oar-foot’), which today are found only in the pools and streams of caves.

The primitive insects must have found some of their food by climbing the trunks of the early tree ferns and horsetails. The ascent was doubtless relatively easy. The climb down, involving long detours over the upward-pointing leaf-bases, may have been very much more laborious and time-consuming. Whether or not the prevalence of such obstacles had anything to do with the next developments, we cannot be sure. It is certain, however, that some of these primitive insects did develop a much swifter and less laborious method of getting down. They flew.

We have no direct evidence of how they achieved flight, but the living silverfish provides a clue. On the back of its thorax it has two flap-like sideways extensions of the chitinous shell that look as though they might be the rudiments of wings. The early wings may not have served initially for flight. Insects, like all animals, are greatly affected by body temperature. The warmer they are, the quicker the energy-producing chemical reactions of their body can proceed and the more active they can be. If their blood were to be circulated through thin flaps extending laterally from the back, they could certainly warm themselves very effectively and quickly in the sunshine. If, furthermore, these flaps had muscles at their base, they could be tilted to face squarely to the sun’s rays. Insect wings do originate as flaps on the back and they do, initially, have blood flowing in their veins, so such a theory seems very plausible.

However this may be, insects with wings appeared some 350 million years ago. The earliest so far discovered are dragonflies. There were several species, most about the size of those living today. But for the dragonflies as for millipedes and other groups that have pioneered a new environment, the absence of competition allowed some early forms to develop to an enormous size, and dragonflies eventually appeared with a wingspan of 70 centimetres, the largest insects ever to exist. When the air became more thickly populated, such extravagant forms disappeared.

Living dragonflies have two pairs of wings which have simple joints to them: they can only move up and down and cannot be folded back. Even so, they are highly accomplished flyers, shooting over the surface of a pond in a blur of gauzy wings at up to 30 kph. At such speeds, they need accurate sense organs if they are to avoid damaging collisions. A tuft of hair on the front of the body helps them to check that their motion through the air is straight, but their primary navigational guidance comes from huge mosaic eyes on either side of the head, which provide superbly accurate and detailed vision.

Because of this dependence on sight, most dragonflies do not fly at night, although there are some that migrate vast distances over the oceans, flying from India to Africa and stopping off at the islands of the Maldives along the way. All are daytime hunters, flying with their six legs crooked in front of them to form a tiny basket in which they catch smaller insects. That fact alone makes it clear that they must have been preceded into the air by other herbivorous forms which, judging from the primitive nature of their anatomy, were probably related to cockroaches, grasshoppers, locusts and crickets.

The presence of these large populations of insects, whirring and buzzing through the air of the ancient forests, was eventually to play an extremely important part in a revolution that was taking place among the plants.

The early trees, like their predecessors, the mosses and liverworts, existed in two alternating forms, a sexual generation and an asexual one. Their greater height posed no problem for spore dispersal: if anything it was a help, since up in the treetops spores were more easily caught by the wind and carried away. The distribution of sex cells, however, was a different matter. Hitherto, it had been achieved by the male cells swimming through water, a process which demanded that the sexual generation be small and live close to the ground. That of ferns, club mosses and horsetails still is. The spores of these plants develop into a thin filmy plant called the thallus which looks not unlike a liverwort and releases its sex cells from its underside where there is permanent moisture. After its eggs have been fertilised, they grow into tall plants like the previous spore-producing generation.

On the ground, the thallus is clearly vulnerable. It is easily grazed by animals; if it dries out it dies; and the very success of the asexual generation with their arching fronds cuts it off from life-giving light. Many advantages would follow if it too could grow tall, but this would require a new technique for getting the male cell to the female.

There were two mechanisms available – the ancient, rather hazardous and capricious method that distributed spores, the wind; and the newly arrived messenger service, the flying insects, which were now regularly moving from tree to tree, feeding on the leaves and the spores. Plants took advantage of both mechanisms. About 350 million years ago, some appeared in which the sexual generation no longer grew flat on the ground, but up in the crowns of the trees. One group among these plants, the cycads, survives today and shows the development at a particularly dramatic stage.

Cycads look superficially like ferns, with long coarse feathery fronds. Some individuals produce tiny spores of the ancient type that can be distributed by the wind. Others develop much larger ones. These are not blown away but remain attached to the parent. There they develop the equivalent of the thallus, a special kind of conical structure within which eggs eventually appear. When a wind-blown spore – which now can be called pollen – lands on an egg-bearing cone, it germinates, not into a filmy thallus for which there is now no need, but into a long tube which burrows its way down into the female cone. The process takes several months. Eventually, when the tube is complete, a sperm cell is produced from the end of the tube. It is a majestic ciliated sphere, the largest known sperm of any organism, plant or animal, so big that a single one is visible to the naked eye. Slowly it makes its way down the tube. When it reaches the bottom, it enters a small drop of water that has been secreted by the surrounding tissues of the cone. There it swims, slowly spinning, driven by its cilia, as it re-enacts in miniature the journeys made through the primordial seas by the sperm cells of its algal ancestors. Only after several days does it fuse with the egg and so complete the long process of fertilisation.

Another group of plants adopting a similar strategy to the cycads arose at about the same time. These were the conifers – pines, larches, cedars, firs and their relations. They too rely on the wind to distribute their pollen. Unlike the cycads, they produce both pollen and egg-bearing cones on the same tree. The process of fertilisation in a pine takes even longer. The pollen tube requires a whole year to grow down and reach the egg, but once there, it contacts the egg cell directly, and the male cell, after descending the tube, does not tarry in a drop of water but fuses directly with the egg. The conifers have at last eliminated water as a transport medium for their sexual processes.

Common hawker dragonfly (Aeshna juncea) on Brackish Moss National Nature Reserve, County Armagh, Northern Ireland.

Cones of the Eastern Cape giant cycad, or bread tree (Encephalartos altensteinii). Present day cycads are survivors of a group dating back 300 million years. Most families died out during the Cretaceous period, 80 million years ago. Cycads are of great evolutionary interest due to their reproductive system, considered to be the forerunner of flowering plants. The cones are the reproductive structures and can be male or female, producing seeds to form new plants.

They have also developed one further refinement. The fertilised egg remains in the cone for one more year. Rich food supplies are laid down within its cells and waterproof coats are wrapped round it. Eventually, more than two years after fertilisation began, the cone dries and becomes woody. Its segments open, and out drop the fertilised fully provisioned eggs – seeds – which if necessary can wait for years before moisture penetrates them and stimulates them to spring to life.

By any standards, the conifers are a great success. Today, they constitute about a third of the forests of the world. The biggest living organism of any kind is a conifer, the giant redwood of California, which grows to 100 metres in height. Another conifer, the bristle-cone pine, which grows in the dry mountains of the southwestern United States, has one of the longest life-spans of any individual organism. The age of trees can easily be calculated if they grow in an environment where there are distinct seasons. In summer, when there is plenty of sunshine and moisture, they grow quickly and produce large wood cells; in winter, when growth is slow, the cells are smaller and the wood consequently more dense. This produces annual rings in the trunk. Counting those in the bristle-cone pine establishes that some of these gnarled and twisted trees germinated over five thousand years ago at a time when people in the Middle East were just beginning to invent writing, and the trees have remained alive throughout the entire duration of civilisation.

Conifers protect their trunks from mechanical damage and insect attack with a special gummy substance, resin. When it first flows from a wound it is runny, but the more liquid part of it, turpentine, quickly evaporates, leaving a sticky lump which seals the wound very effectively. It also, incidentally, acts as a trap. Any insect touching it becomes inextricably stuck and very often buried as more resin flows around it. Such lumps have proved to be the most perfect fossilising medium of all. They survive as pieces of amber and contain ancient insects in their translucent golden depths. When the amber is carefully sectioned, it is possible, through the microscope, to see mouthparts, scales and hairs with as much clarity as if the insect had become entangled in the resin only the day before. Scientists have even been able to distinguish tiny parasitic insects, mites, clinging to the legs of the bigger ones. Extracting the DNA from a blood-sucking arthropod seems likely to remain science fiction, however. Even attempts to do so from insects trapped in copal, the modern equivalent of amber only a few decades old, have all met with failure.

The oldest pieces of amber so far discovered date from around 230 million years ago, a long time after the conifers and the flying insects first appeared, but they contain a huge range of creatures, including representatives of all the major insect groups that we know today. Even in the earliest specimens, each type has already developed its own characteristic way of exploiting that major insect invention, flight.

Ancient bristlecone pine in winter, near Wheeler Peak in Great Basin National Park, Nevada, USA.

The dragonflies beat their two wings synchronously, with the front pair raised while the rear pair are lowered. This, however, creates very considerable physiological complexities. Their wings do not normally come into contact, but even so there are problems when the dragonfly executes sharp turns. Then the fore- and hindwings, bending under the additional stress of the turn, beat against one another, making an audible rattle that you can easily hear as you sit watching them make their circuits over a pond.

The later insect groups seem to have found that flight was more efficiently achieved with just one pair of beating membranes. Bees and wasps, flying ants and sawflies all hitch their fore- and hindwings together with hooks to make, in effect, a single surface. Butterfly wings overlap. Hawkmoths, which are among the swiftest insect flyers, capable of speeds of 50 kph, have reduced their hindwings very considerably in size and latched them on to the long narrow forewings with a curved bristle. Beetles use their forewings for a different purpose altogether. These creatures are the heavy armoured tanks of the insect world and they spend a great deal of their time on the ground, barging their way through the vegetable litter, scrabbling in the soil or gnawing into wood. Such activities could easily damage delicate wings. The beetles protect theirs by turning the front pair into stiff thick covers which fit neatly over the top of the abdomen. The wings are stowed beneath, carefully and ingeniously folded. The wing veins have sprung joints in them. When the wing covers are lifted, the joints unlock and the wings spring open. As the beetle lumbers into the air, the stiff wing covers are usually held out to the side, a posture that inevitably hampers efficient flight. Flower beetles, however, have managed to deal with this problem. They have notches at the sides of the wing covers near the hinges so that the covers can be replaced over the abdomen, leaving the wings extended and beating.

The most accomplished aeronauts of all are the flies. They use only their forewings for flight. The hindwings are reduced to tiny knobs. All flies possess these little structures but they are particularly noticeable in the crane flies, the daddy-long-legs, in which the knobs are placed on the ends of stalks so that they look like the heads of drumsticks. When the fly is in the air, these organs which are jointed to the thorax in the same way as wings, oscillate up and down a hundred or more times a second. They act partly as stabilisers, like gyroscopes, and partly as sense organs presumably telling the fly of the attitude of its body in the air and the direction in which it is moving. Information about its speed comes from its antennae, which vibrate as the air flows over them.

Flies are capable of beating their wings at speeds up to an astonishing 1,000 beats a second. Some flies no longer use muscles directly attached to the bases of the wings. Instead they vibrate the whole thorax, a cylinder constructed of strong pliable chitin, making it click in and out like a bulging metal tin. The thorax is coupled to the wings by an ingenious structure at the wing base, and its contractions cause them to beat up and down.

Longhorn beetle (Cerambycidae) in flight Rookery Wood, Sussex, England, UK, July.

The insects were the first creatures to colonise the air, and for over a 100 million years it was theirs alone. But their lives were not without hazards. Their ancient adversaries, the spiders, never developed wings, but they did not allow their insect prey to escape totally. They set traps of silk across the flyways between the branches and so continued to take toll of the insect population.

Plants now began to turn the flying skills of the insects to their own advantage. Their reliance on the wind for the distribution of their reproductive cells was always haphazard and expensive in biological terms. Spores do not require fertilisation and they will develop wherever they fall, provided the ground is sufficiently moist and fertile. Even so, the vast majority of them, from such a plant as a fern, fail to find the right conditions and die. The chances of survival for a wind-blown pollen grain are very much smaller still, for their requirements are even more precise and restricted. They can only develop and become effective if they happen to land on a female cone. So the pine tree has to produce pollen in gigantic quantities. A single small male cone produces several million grains, and if you tap one in spring, they fall out in such numbers that they create a golden cloud. A whole pine forest produces so much pollen that ponds become covered with curds of it – and all of it wasted.

Insects could provide a much more efficient transport system. If properly encouraged, they could carry the small amount of pollen necessary for fertilisation and place it on the exact spot in the female part of the plant where it was required. This courier service would be most economically operated if both pollen and egg were placed close together on the plant. The insects would then be able to make both deliveries and collections during the same call. And so developed the flower.

Some of the earliest and simplest of these marvellous devices so far identified are those produced by the magnolias. They appeared about a 100 million years ago. The eggs are clustered in the centre, each protected by a green coat with a receptive spike on the top called a stigma, on which the pollen must be placed if the eggs are to be fertilised. Grouped around the eggs are many stamens producing pollen. In order to bring these organs to the notice of the insects, the whole structure is surrounded by brightly coloured modified leaves, the petals.

Beetles had fed on the pollen of cycads and they were among the first to transfer their attentions to the early flowers such as those of magnolias and waterlilies. As they moved from one to another, they collected meals of pollen and paid for them by becoming covered in excess pollen which they involuntarily delivered to the next flower they visited.

Saucer Magnolia (Magnolia x soulangeana) tree in full flower against blue sky. Stourhead gardens, Wiltshire, UK, April.

Meadow in flower, with cork oaks (Quercus suber) in the background, Beja, Portugal.

One danger of having both eggs and pollen in the same structure is that the plant may pollinate itself, thereby preventing cross-fertilisation, the very purpose of all these complexities. This possibility is avoided in the magnolia, as in many plants, by having eggs and pollen that develop at different times. Magnolia stigmas will accept pollen as soon as the flower opens. Its own stamens, however, do not produce their pollen until later, by which time its eggs are likely to have been cross-fertilised by exploring insects.

The appearance of flowers transformed the face of the world. The green forest now flared with colour as the plants advertised the delights and rewards they had on offer. The first flowers were open to all that cared to alight on them. No specialised organs were required in order to reach the centre of the magnolia flower or the waterlily, no particular skill was needed to gather the pollen from the loaded stamens. Such blooms attracted several kinds of insects – bees as well as beetles. But a variety of visitors is not an unmitigated advantage, for they themselves are also likely to visit several kinds of unspecialised flowers. Pollen of one species deposited in flowers of another is pollen wasted. So throughout the evolution of the flowering plants, there has been a tendency for particular flowers and particular insects to develop together, each catering specifically for the other’s requirements and tastes.

Right from the times of the giant horsetails and ferns, insects had been accustomed to visiting the tops of trees to gather spores as food. Pollen was an almost identical diet and it still remains a most important prize. Bees collect it in capacious baskets on their thighs and take it back to their hives for immediate consumption or for turning into pollen bread which is an essential food for their developing young. Some plants, among them species of myrtle, produce two kinds of pollen, one that fertilises their flowers, and another of a particularly tasty kind that has no value except as food.

Other flowers developed a completely new bribe, nectar. The only purpose of this sweet liquid is to please insects so greatly that they devote all possible time during the flowering season to collecting it. With this the plants recruited a whole new regiment of messengers, particularly bees, flies and butterflies.

These prizes of pollen and nectar have to be advertised. The bright colours of flowers make them conspicuous from considerable distances. As the insect approaches, it is provided with markings on the petals which indicate the exact placing of the rewards they seek. Some flowers intensify their colours towards the centre or introduce another shade altogether – as do forget-me-nots, hollyhocks, bindweed. Others are marked with lines and spots like an airfield to show the insect where to land and in which direction to taxi – foxgloves, violets and rhododendrons. There are more of these signals on flowers than we may realise. Many insects can perceive colours of the spectrum that are invisible to us. If we photograph what seem to be plain flowers in ultraviolet light, we can see many more such markings on the petals.

Bee orchid (Ophrys apifera) in flower. Dorset, UK, June.

Scent is also a major lure. In most cases, the perfumes that insects find attractive, such as those produced by lavender, roses, and honeysuckle, please us as well. But this is not always the case. Some flies are attracted to rotting flesh as a food for themselves and their maggots. Flowers that enlist them as pollinators must cater for their tastes and produce a similar smell, and they often do so with an accuracy and pungency far beyond the endurance of the human nose. The maggot-bearing Stapelia from southern Africa has flowers that reek dreadfully of carrion but it also reinforces its appeal to flies with wrinkled brown petals covered with hairs that look like the decaying skin of a dead animal. To complete the illusion, the plant generates heat that mimics the warmth produced by corruption. The whole effect is so convincing that flies transporting Stapelia’s pollen not only visit flower after flower, but even complete the activity for which they visit real carrion – laying their eggs on the flower just as they do in a carcass. When these hatch, the maggots find that they are not provided with a meal of rotting meat but only an inedible petal. They die from starvation, but the Stapelia has been fertilised.

Perhaps the most bizarre imitations of all are those of some orchids that attract insects by sexual impersonation. One produces a flower that closely resembles the form of a female wasp complete with eyes, antennae and wings and even gives off the odour of a female wasp in mating condition. Male wasps, deceived, attempt to copulate with it. As they do so, they deposit a load of pollen within the orchid flower and immediately afterwards receive a fresh batch to carry to the next false female. The extent of this mimicry can be far greater than mere physical resemblance. The orchid’s flowers are covered with waxes that correspond to an extraordinary degree to the sex-specific pheromones that cover the female wasp and which are just as attractive. These orchids produce no nectar. The reward they provide for their insect pollinators is not sex, but its illusion.

Sometimes insects are disinclined to collect pollen, preferring nectar, and will bypass the plant’s strategies and become nectar thieves, biting their way through the flowers from the outside and inserting their proboscis into the nectar source without getting covered in pollen. Then the flowers have to have devices to force their pollen on the insect. Some blooms have become obstacle courses during which their visitors are pummelled by stamens and bombarded with pollen before they are able to leave. Broom flowers are so constructed that if, for example a bee, lands, the stamens, packed under tension inside a sealed capsule of petals, shoot out and strike the underside of the bee, covering its furry abdomen with pollen. The bucket orchid from Central America drugs its visitors. Bees clamber into its throat and sip a nectar so intoxicating that after they have taken only a little they begin to stagger about. The surface of the flower is particularly slippery. The bees lose their foothold and fall into a small bucket of liquid. The only way out of this is up a spout. As the inebriated insect totters up, it has to wriggle beneath an overhanging rod which showers it with pollen.

Rafflesia flower (Rafflesia keithii) in Gunung Gading National Park, Borneo, Sarawak, Malaysia.

Sometimes plant and insect become totally dependent one upon the other. The yucca grows in Central America. It has a rosette of spear-shaped leaves from the centre of which rises a mast bearing cream-coloured flowers. These attract a small moth with a specially curved proboscis that enables it to gather pollen from the yucca stamens. It moulds the pollen into a ball and then carries it off to another yucca flower. First it goes to the bottom of the flower, pierces the base of the ovary with its ovipositor and lays several eggs on some of the ovules that lie within. Then it climbs back up to the top of the stigma rising from the ovary and rams the pollen ball into the top. The plant has now been fertilised and in due course all the ovules in the chamber at the base will swell into seeds. Those that carry the moth’s eggs will grow particularly large and be eaten by the young caterpillars. The rest will propagate the yucca. If the moth were to become extinct, the yuccas would never set seed. If the yuccas disappeared, the moth’s caterpillars could not develop. Each species is inextricably in the debt of the other.

One further debt is clear. Flowers, exquisitely perfumed and graced with a multitude of colours and shapes, bloomed long before humans appeared on the earth. They evolved in order to appeal not to us but to insects. Had butterflies been colour-blind and bees without a delicate sense of smell, we would have been denied some of the greatest delights that the natural world has to offer.

FOUR

The Swarming Hordes

By any standards, the insect body must be reckoned the most successful of all the solutions to the problems of living on the surface of the earth. Insects swarm in deserts as well as forests; they swim below water and crawl in deep caves in perpetual darkness. They fly over the high peaks of the Himalayas and exist in surprising numbers on the permanent icecaps of the Poles. One fly makes its home in pools of crude oil welling up from the ground; another lives in steaming-hot volcanic springs. Some deliberately seek high concentrations of brine and others regularly withstand being frozen solid. They excavate homes for themselves in the skins of animals and burrow long winding tunnels within the thickness of a leaf.

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