by Steve Jones
Just after the publication of The Origin, Darwin began to work on a botanical lifestyle that, as he soon found, drags a great diversity of unrelated species into a shared set of habits. His interest began in 1860, when he visited Hartfield in Sussex, on the edge of Ashdown Forest, the home of his sister-in-law Sarah Elizabeth Wedgwood (and later the birthplace of Winnie the Pooh). There he saw thousands of sundews - small clumped plants, with a sticky surface that traps insects. Some had as many as thirteen victims on a single leaf. Most of the prey consisted of small flies, but some victims were as large as a butterfly and he was told that the traps could even catch dragonflies. As so many sundews were present, the numbers of insects slaughtered must, he calculated, be prodigious. Each leaf had scores of glands held upright on fine hairs. They exuded shiny globules of liquid even on dry days and entangled any small creature foolish enough to land upon them. The sundew, he found, had feeble roots - evidence that most of its nutrition did indeed come from its gruesome way of life. He brought some specimens back to his greenhouse and began to explore how they did their job. It was the first step in a decade of work that produced a powerful vindication of his claim in The Origin that natural selection could, starting from different places, end up with much the same result.
In 1875, he published a book, Insectivorous Plants, on the subject. It deals not just with sundews but with a variety of such creatures from across the world, some from the area of Roraima itself. Darwin soon found many similarities among the various species that have taken up the habit. A closer look showed that many of their adaptations are also present in the other major kingdom of life. Emma noted in her diary when he was at work on a certain insectivore that ‘I suppose he hopes to end in proving it to be an animal.’ Her husband was so astonished by such parallels that he wrote to a friend that ‘I am frightened and astounded at my results.’ The aesthete John Ruskin said, in contrast, that ‘with these obscene processes and prurient apparitions the gentle and happy scholar of flowers has nothing whatever to do. I am amazed and saddened, more than I can care to say, by finding how much that is abominable may be discovered by an ill-taught curiosity.’ Darwin’s curiosity, ill-taught or not, added another plank to his evolutionary edifice.
Roraima and the flat islands of rock around it are ancient indeed. Its sandstone peak - once part of a wide and barren plain, most of it now eroded away - is almost two billion years old. In the context of its immense history the terrible lizards went not long ago and the humans clustered around its base arrived in an evolutionary yesterday.
Its unique vegetation has been on its rain-soaked flanks for longer than either. The plants have seen the slow passage of time and have changed to match. A third of them evolved upon the mountain’s lonely rocks and are found only there. Their native land is a hungry place. Constant downpours eat at the soil and strip what remains of nutriments, which are tipped down some of the highest waterfalls in the world. Worst of all, the rain washes away the nitrogen that every tree, shrub or flower needs to grow. Sandstone peaks, deserts, dunes, bogs, pine forests, Mediterranean scrublands and more - all are short of that element and each, distinct as it looks, and different as its inhabitants might be, has evolved a set of inhabitants whose battle for existence is focused, in a variety of ways, on the need to find it. The struggle for nitrogen shows - even better than the multitude of ways in which life has taken to the skies - how natural selection can reach the same end with different means in creatures from quite separate parts of the biological universe. Plants, animals, bacteria and fungi are all drawn together in their shared hunger for the element and all have become entangled with each other in the struggle to find it.
The gas itself makes up four-fifths of the air but plants cannot extract it directly. Their growth is often limited by a shortage of the stuff. Many manage by soaking it up from the soil. They forage like hungry animals with their roots, which stretch further and further as the essential item runs short. Below the surface, much of the element is bound into compounds that refuse to give it up.
However adept they may be as foragers, many plants live on soils with so little nitrogen that they cannot survive without help. They are forced into contracts with other creatures that donate the vital element. The natives of Roraima eat insects and soak up the nitrogen in their flesh. The trade is one-way, for the plants kill the animals. Sometimes, in contrast, the treaty seems positive, for both parties appear to gain. In fact, even the several apparently amicable associations in the nitrogen market are based on greed and expedience. The fight for the crucial chemical is fierce and has led to shared adaptations that straddle the whole of life.
All animals fall prey to the vegetable world in the end as their dust returns to dust, but in the starved landscape of the Lost World the vegetation cuts out the middleman and devours the local wildlife directly. Natural selection has tinkered with leaves, roots and other parts to come up with the equivalents of teeth, gullets, stomachs and intestines, to draw the machinery of the botanical world close to that of animals.
Charles Darwin’s book on the insect-eaters sold less well than had Conan Doyle’s fictional lizards but such creatures behave in a way beyond the imagination of the most fanciful novelist. Insectivorous Plants raised biological questions that resonate beyond the universe of the carnivores. At first Darwin doubted the value of his own experiments and wrote to a colleague that ‘I must consult you some time whether my “twaddle” is worth communicating’, but he soon became an enthusiast. His book is a masterful narrative of the ingenuity of existence.
Plants that eat flesh attracted curiosity and hyperbole long before Darwin’s day. They still do, even if the Australian version that feeds on rabbits has yet to be confirmed by science. The sundews of Ashdown Forest have a natural flypaper that holds its victims with a syrupy glue. The leaves curl round to entangle them before they meet a sticky end in its sinister digestive globules. Their secretions give the plant its name; as Henry Lyte wrote in 1578 in his Nievve Herbal: ‘This herbe is of a very strange nature and marvelous: for although that the Sonne do shine hoate, and a long time thereon, yet you shall finde it always moyst and bedewed.’ Insectivorous Plants also includes experiments on the Venus flytrap, which modified some of its leaves into a ‘horrid prison’, and on many other kinds forwarded to Down House from afar.
The insectivore habit has evolved in around a dozen distinct lineages, and Darwin saw most of them. They represent but a small fraction of the quarter of a million kinds of plants with flowers, but their habits, and their origins, are varied indeed. Some of the flesh-eaters are relatives as close as the anteater and the pangolin (long-nosed predators of ants from the Americas and the Old World respectively, the former kin to armadillos and the latter to dogs and cats) but others are as different as an anteater is from an insect-eating lizard or a bird such as the swallow.
The sundew belongs to a group of a hundred or so species whose centre of diversity is in Australia. It has a relative called the butterwort that hunts in the same way. The flypaper habit has evolved on at least five independent occasions, to produce the Australian ‘rainbow plants’, so called because of the sinister sheen of their leaves, and many more. Some kinds are three metres high and some tiny, and they are found across much of the globe, from Alaska to New Zealand. Europe has just three of the hundreds of species known. DNA shows that even the sundew and a very similar species from Portugal have evolved insectivory of their own accord, as each can trace affinity to closer relatives that do not indulge in the pastime.
A second trick remarked on by Darwin is to swing a door shut upon the prey. The most familiar jailer is the Venus flytrap, brought to attention in 1768 as the ‘fly trap sensitive’ by Arthur Dobbs, Governor of North Carolina, who sent the first specimen back to Britain (and was in addition the first person to record the movement of pollen by bees). The botanist William Bartram saw the ‘ludicrous’ plant on his travels through the Carolinas: ‘This wonderful plant seems to be distinguished in the creation,
by the Author of nature, with faculties eminently superior to every other vegetable production … We see here, in this plant, motion and volition.’ The ‘irritable principle in vegetables’ was much commented on even if some denied that any plant would lower itself to prey on an animal. Linnaeus, the great classifier, insisted that the flytrap always let its prisoners go, while others claimed that the insects trapped within were sheltering from frogs. It even became part of legal philosophy. The social theorist Cesare Lombroso, who believed that crime was a biological throwback beyond the control of those responsible, felt that flytraps marked ‘the dawn of criminality’. They ‘establish that premeditation, ambush, killing for greed, and, to a certain extent, decision-making (refusing to kill insects that are too small) are derived completely from histology or the microstructure of organic tissue - and not from an alleged will.’
The flytrap - and just a single species is known - lives in nitrogen-poor swamps in the Carolinas, its native home. It was given the erroneous Latin tag of Dionaea muscipula (which means ‘mouse-eater’ rather than ‘fly-eater’ as intended). Its popular name among the colonists was ‘tipitiwitchet’, then a slang term for female genitalia, because of its supposed resemblance to that organ, (although to avoid vulgarity Thomas Jefferson used the label ‘Aphrodite’s mousetrap’ when he added his specimen to his collection). Each bears up to a dozen traps, each made of a much-modified leaf. Darwin himself considered the creature to be ‘one of the most wonderful in the world’. Its trap closed on its prey with spines that interlocked like the teeth of a rat-trap, rather than gluing them to its leaves, but its sensitivity reminded him of the sundew’s quite different strategy.
Just two snap-traps are known: the Venus flytrap itself, and the so-called waterwheel plant (again just a single species, but found scattered across the world) which does the same under water, on a smaller scale.
Other freshwater flesh-eaters use another method: a lobster pot, a snare with a one-way entrance valve. A separate group, found both on land and in fresh water, has tiny capsules or bladders that, when touched, suck in prey with irresistible force.
The bladderworts, as they are called, have hundreds of species, found everywhere except in Antarctica. They prime their trap by pumping water out across its wall. Another kind found on moist rocks in South America and parts of Africa specialises in single-celled animals, protozoa that swim into tiny slits in its specialised underground leaves. It shows a microscopic kind of carnivory and Darwin had speculated that it was indeed a meat-eater, although he had no idea of its food.
The insect-killers of Roraima use a different trick, a pitfall based on rolled leaves with margins sealed together. The fatal ambush is covered with a slippery glaze and decorated with a nectar bait. The sixteen species known from that peak are relatives of heathers and their mountain allies. Some are a metre tall, some tiny. Other pitcher plants of the New and Old Worlds and of Australia also use rolled-up leaves to snare their prey and some are big enough to take mice. They come from quite a different section of the botanical kingdom. Their capital is in the New World, which has more of those baleful creatures than anywhere else. The cobra lily of the western United States has a mouth said to resemble that of a snake. It feasts on ants. Others among its kin have a flared cover that shelters the jaws of the trap and keeps water out. A different group with the same general appearance, the monkey cups from around the Indian Ocean, make their pitfalls as structures that spring from a leaf ’s mid-rib and are held at the end of a long tendril. They get their taxonomic name, Nepenthes, from the restorative drug given to Helen of Troy. Linnaeus was impressed by them: ‘What botanist would not be filled with admiration if, after a long journey, he should find this wonderful plant. In his astonishment, past ills would be forgotten when beholding this admirable work of the Creator!’ Yet another pitcher is found in Western Australia. Its traps look rather like old shoes and the plant is unrelated to any of the other pitfall-makers.
DNA reveals some unexpected affinities among the pitchers, for the Old World kinds are in fact more related to sundews and Venus flytraps than they are to their New World equivalents. In addition they are quite close to a group of non-carnivorous lianas of tropical forests, and find more relatives in a larger class that includes rhubarbs, spinach and beet.
An even more distinct group, the bromeliads - relatives of the pineapple and in quite a different subdivision of the kingdom from the other green carnivores - also make leafy containers that fill with water. They live in the tropical forests of the Americas. There may be more than a hundred thousand in every hectare, most of them stuck to trees. The vessels made by their fused leaves generate a huge series of tiny lakes, in which a variety of creatures find a home. At first the bromeliads appear benign, for they lack the digestive enzymes found in the other pitfalls. Tadpoles, insect larvae, twenty-five-millimetre-long salamanders and tiny crabs all live in the liquid within. In truth, they have a darker side. Each watery island is full of conflict, and their proprietors gain nitrogen from the corpses of the creatures that are killed there and are broken down by bacteria. One kind has already taken a step to true carnivory with digestive enzymes of its own.
Other meat-eaters, unknown in the nineteenth century, are bizarre indeed. Certain soil fungi devour nematodes, worm-like creatures far larger than themselves, with a lasso that snaps shut within a tenth of a second, strangles the animal and gives the predator a rich source of food. Others do the same job with a sticky pad, while the familiar and tasty inkcap mushroom puts out spiked and lethal balls that puncture its prey and allow the fungal spores to grow within it. A hundred and fifty fungi that snack on flesh are known and there is a whole world of hunting mushrooms ready to be discovered.
Wherever they sit in the botanical world, a hard life in a hungry place has pushed every flesh-eater towards a similar set of expedients. Like cactuses they succeed where others fail, in their case because of a shortage of food rather than of water. The cost of success is specialisation. Their habit can be expensive and their way of life fragile, for traps cost a lot and force a reduction in the investment in roots or leaves. Insectivores often find it hard to cohabit with other species, which means that vast areas are carpeted by them alone. In addition, they are forced to seek open sunlight, for their leaves are too feeble to cope with shade, and do best in places where fires sweep through and wipe out the opposition.
The insect-eating package is sometimes lost when conditions change. Some are committed to it. The Venus flytrap is itself trapped into its narrow way of life, for it gains around three-quarters of its nitrogen from insects. The cobra lily is not far behind, and the snares of both those species are elaborate and hard to build. Other plants are more adaptable in their ways. Almost all the carnivores have some chlorophyll, the stuff that makes leaves green, but often no more than half that found in normal species. They gain some energy from the sun, albeit at reduced efficiency. The sundew and many of its fellows have reduced roots as not much food is available in their native swamps, but they can soak up a little. Radioactively labelled nitrogen shows that up to half of the nitrogen taken up by a typical individual comes from soil rather than from flesh.
For most insectivores, the prey are more important in the summer when they are abundant - and a large part of what they provide goes to make flowers, expensive as they are. The bladderwort makes traps only at the height of that season, when insects are common and the time has come for sex. The pitchers of New England make more traps in the bogs with least nitrogen, but put effort into ordinary leaves when the water contains more of that mineral. Pitchers make two kinds of leaves, either modified to make a trap or large and flat to soak up sunshine. When nitrogen is added, the plants make more of the latter, for a shortage of the element no longer limits their growth. Others, too, play the mineral market. The sundew produces less slime than normal when given a decent dose of fertiliser. All this suggests that carnivory is a luxury that is abandoned whenever a cheaper source of nitrogen becomes availab
le. That has happened many times, for DNA shows that several vegetarians have evolved from carnivore ancestors. Certain pitchers from Borneo now soak up nutrition from dead leaves or from bird excrement that falls into their flasks instead of from insects.
The first botanical carnivores evolved long ago. A famous fossil bed at Yixian, in north-east China, from around a hundred and twenty-five million years before the present, yields dinosaurs with feathers - together with a small pitcher quite similar to those of today, with lures to attract its prey and glands ready to soak up their remains. The bed dates from a time close to that of the origin of flowers themselves. A tree of relatedness of that entire group based on DNA suggests that perhaps the sticky traps evolved first, while pitfalls and snap-traps came later - which, if true, pushes the habit even further into the past. Even the nematode-eating fungi have left a hundred-million-year-old fossil, trapped in amber in a French quarry.
Our insight into that motley set of unrelated creatures was transformed by Charles Darwin, who raised - and answered - biological questions that resonate far beyond their own narrow universe. He began a systematic survey of how the various members caught their prey, digested it and absorbed its goodness. The results, he wrote, were ‘highly remarkable’.
First, he found that sundews grew far better when fed with insects than when starved, although they could survive for a time on a vegetarian diet. Their sensitivity was impressive. Even a tiny gnat with its ‘excessively delicate feet’ was enough to set off a reaction. A gland moved within ten seconds of the arrival of a meal. The impulse to do so soon spread through a whole leaf. Within an hour, a mass of tentacles began to bend towards the prey. The trap moved faster on warm days but light and dark made no difference. The tentacles had no sense of smell for an object had to touch the surface to induce the effect, but they could taste, for they held on to pieces of meat for longer than to bits of glass, cork or hair. Water, tea and sherry did not excite them and neither did a firm prod with a twig, but even a minute particle of living material led to some response.