by Steve Jones
What woke the sundew up was nitrogen. Urine (presumably the great naturalist’s own) did the job, while tea did not. Ammonium carbonate - sal volatile, its ammonia used to stimulate fainting Victorian ladies - contains that essential nutriment and elicited a response almost at once, even when diluted. Just a twenty-millionth of a grain of nitrogen salts in solution - less than a thousandth of a milligram - was enough to stir the sundew’s interest.
The Venus flytrap solved the hunter’s problem with quite a different set of tricks. Its prison doors slam shut within a tenth of a second of being touched - which means that it makes among the fastest of all plant movements. As soon as the prey arrives it disturbs the sensitive hairs that cover the trap. A wave of electrical activity passes across the surface at around ten centimetres a second. The wall of each modified leaf, with its two hinged parts, has cells kept full of liquid at high pressure and the flytrap uses its feeble powers to pump them up, with many hours of effort needed to reset the snare each time it has been used. The trap wall is curved outwards when open, and inwards when shut, with a fine balance between the two stable states. A squeeze with the fingers causes it to snap shut in the same way as a pea pod pops open. The elastic energy stored in the curved shell of an open trap is released in a sudden rush and it slams closed.
The flytrap’s trigger - which evolved down quite a different path from that of the sundew - gives further hints about how information from outside is translated into action. Darwin found that it was as alert to a sudden touch as was the gland of its sticky fellow carnivore, but responded less to prolonged pressure. Two or three quick taps within thirty seconds of each other, rather than just one, were needed to spring it, perhaps to avoid disturbance by wind-blown grains of dust. Rain had no effect.
The pitcher plants had evolved another ingenious way to catch their prey. Many befuddle the insects with signals that draw them to a promise of food or sex but in fact deliver death. Certain pitchers have a nectar-laden ‘spoon’ near the mouth while others generate motifs that are irresistible to bees and other insects, such as dark centres with stripes that radiate out and look rather like flowers. Some have backward-pointing hairs within the pitfall to prevent escape. The cobra lily has a guileful way with its victims, for its walls are decorated with clear patches that persuade the flies to stay and beat against a window until they drown rather than flying upwards to gain freedom. Once they have fallen into the liquid their fate is sealed for it contains a syrup from which escape is impossible.
The slippery wax that covers the inner surface of many pitfalls and causes insects to plunge to their doom has revealed its secrets. It has two layers. The lower section is made of stiff foam, while the upper consists of a sheet of loosely attached and brittle plates. These break off and clog the prey’s hooked feet, which then skid on the foam below. Other species keep their surface moist with a series of fine ridges that trap water or nectar and cause any insect that lands to aquaplane into the void below. As a result, certain kinds can catch their quarry only in rainy weather. At other times an insect can sit happily on the rim. That, perhaps, lulls it into a false sense of confidence when it comes for food until, one day, it falls to its doom.
To trap a fly is just the first step to sucking out its goodness. The animal must be digested and its nitrogen absorbed. Once again, the insect-eaters use different means to achieve a common end. As they do, they seem, once again, to approach the habits of animals. A sundew leaf with a series of tentacles all pointing towards an item of food led Charles Darwin to ‘imagine that we were looking at a lowly organised animal seizing prey with its arms’. Soon the whole leaf closed up to make a ‘temporary stomach’ that smothered the prey as each hair pumped out digestive droplets, the ‘dew’ that gave the plant its name. By a ‘curious sort of rolling movement’, rather like that of the human intestine, the unfortunate victim was propelled towards the centre, where more hairs awaited. As it expired, the secretion changed from a mere glue to an acid liquid. The sticky fluid could, he found, digest living material of many kinds.
The magic liquid was pumped out from the base of each hair. There were marked changes in the internal structure of each cell as they prepared to make the digestive juice, with the accumulation of masses of purple matter after a dose of meat. The sundews were a first hint that cells can communicate with each other, for a colour change could be tracked as the message spread across the leaf. The agitation spread just as in animal nerves, although nerves act faster and show no visible changes as they do their work.
What path did the information take as it travelled through the leaf? Various vessels traverse it, but tentacles close to and distant from such channels behaved in the same way. The best that Darwin could come up with was that the motor impulse involves the passage of chemicals of some kind but what these were he had no idea.
In those days all that was known about nerve transmission was that it involved what he called an ‘invisible molecular change that is sent from one end of the nerve to the other’, but there was no evidence of what that might be. His experiments with poisons on sundews provided a hint of what later became a central truth of cell biology. Some, from arsenic to strychnine, were as pernicious to plants as to ourselves, while others, cobra venom included, were not. Morphine and alcohol, with their noticeable actions on the human nervous system, left the sundews indifferent - but salts of potassium and of sodium had opposed effects, for the former caused the leaf to move while the latter was fatal. That observation presaged the later discovery that a balance between the two elements on either side of the cell membrane is behind the electrical activity of both plant and animal cells, nerves included.
The flytrap with its need for a double tap before closing must, in some sense, remember the first before it responds to the second. It was suggested to Darwin by Burdon Sanderson, Professor of Physiology at University College London, that a chemical or electrical mechanism was involved. He was the first to find that - just as in animal muscles when they contract - the voltage altered when it snapped shut. A complicated long-chained sugar causes the prison walls to close when applied in minute quantities to the leaf. It builds up at speed after the trap is touched, but is broken down almost as fast. Only if the second tap arrives in time does it reach a concentration high enough to trigger off a response. The memory molecule - which is what it is - activates channels in the cell membrane that transmit sodium and potassium ions. As it does, it generates an electrical signal that fires off the poised cells. As in nerves and muscles, the movement of calcium ions is also involved. The ambush can also be induced to snap shut with human chemical messengers such as adrenaline and certain other nerve-transmitters, which are themselves molecules that work by reaching a threshold.
Concerned as ever with the state of his own intestines, Darwin turned again for advice about the sundew’s digestive juice to Burdon Sanderson. Its power to break down protein had long been known. The sticky secretion of butterwort was once used to make ‘ropy milk’, a sort of yoghurt in which the milk was curdled under the influence of its digestive enzymes. Herbalists still insist that the substance is useful against tuberculosis, asthma, intestinal pain and the chapped udders of cows (in the Netherlands it was once popular as a hair pomade).
The two scientists established that the exudate contained a series of organic acids related to vinegar, together with an enzyme. When both were present - but not when just acid or enzyme alone was available - insect flesh was broken down. The sundew stomach, if such it could be called, hence showed close parallels in its actions to our own, which itself contains both acids and enzymes. That, Charles Darwin felt, was a ‘new and wonderful fact in physiology’, for it brought the plant and animal kingdoms together.
The digestive enzymes of the insect-eaters have now revealed more of their secrets. Our own gastric talents are limited in comparison with theirs, for the plants cope with a diet that would give us all dyspepsia. Vincent Holt’s neglected 1885 work Why Not Eat Insects? contained recipes fo
r nutritious dishes such as larves des guêpes frites au rayon (wasp grubs fried in their nests). Some people do indeed eat larvae - in the Far East silkworms are popular - but some of Holt’s suggestions, such as phalènes à l’hottentot (moths in butter) and cerfs-volants à la gru gru (stag beetles on toast), would be indigestible indeed. The Vietnamese who feast on water-beetles or scorpions have to throw away the tough outer shells as impossible to manage. Their botanical relatives can afford to be less fastidious, for their enzymes can break down all the prey has to offer, the hard coat included.
The insectivores use, as do our own intestines, a cocktail of chemicals, each of which digests a particular foodstuff. Sundews have an enzyme that cuts up nucleic acids, while pitchers - which can hold three litres of digestive fluid - have half a dozen distinct kinds that attack proteins, nucleic acids and other substances, together with a special protein that breaks down the insect skeleton. The Venus flytrap has equivalents of its own (and if a leaf overeats it may die from indigestion), as do almost all the other botanical carnivores.
For plants and people alike digestion is followed by absorption. The insectivores have refined their abilities to soak up a meaty soup, but at a price, for the leaves of conventional plants are, in the main, quite impermeable because of the need to conserve water. A creature that feeds through its leaves cannot safeguard itself in that way. The sundew has large pores in a generally waterproof skin that allow its insect broth into the digestive cells. In pitchers, the whole interior surface is thin or is scattered with holes that allow water to pass. The carnivores then face a dilemma, for as they suck in the liquid remains of their feasts across a porous leaf surface they are at risk of fluid loss from the same place. As a result, many are restricted to wet places.
Such plants have to make many other compromises. First, they face a conflict between sex and starvation. They eat insects but are also pollinated by them. To reduce the chance of error, flowers and traps open at different times, or on different parts of their parent’s anatomy, or attract a separate set of visitors. Even so, the carnivores often devour their winged Cupids by mistake or, perhaps, because they are more valuable as a source of nitrogen than as a sexual aid.
What struck Darwin most of all about his insect-eaters - and he did experiments on the underwater kinds as well as those on land - was that all of them built their specialised machinery by picking up and using talents already found in species with more orthodox habits. They were a wonderful example of how evolution could make do and mend. Natural selection often scavenged its raw material from whatever was available rather than being forced to wait for what it needed to emerge anew.
Varied as the insect-eaters are, and distinct as their traps and their means of digestion and absorption might be, carnivory has always been cobbled together from pre-existing structures. All the species studied at Down House, and the many more now known, have modified the banal talents of their ancestors to reach their present state. All roots make mucus, and sundews themselves are related to tamarisks and knotweeds, which make lots of the stuff to get rid of salt or to fight off insects. Most plants are attacked by insects and some have evolved defences such as glue-covered hairs, or spines that can, when needed, be used for aggressive ends. The familiar blue Plumbago is notorious for its sticky flowers that trap its enemies and save it from attack. Many flowers close upon a pollinator before they release it and - as a hint of how the flytrap evolved its remarkable talent - plenty of plants can move their leaves or seed-pods, some at speed. The pitchers had less to do to develop a trap, for leaves fuse for many reasons and a variety of mutations in crops such as maize cause once-independent leaves to bond together.
Digestion, too, has its echoes in the more innocent parts of the botanical world. Some wild geraniums are covered in a secretion that can break down and absorb proteins placed upon their leaves. They are ‘proto-carnivores’, poised on the edge of that habit but not yet committed to it. Other parts of the digestive tool-kit are also lying about, ready to be used. Seeds and many leaves secrete enzymes to protect themselves against attack. Those of certain insectivores resemble others that, in most species, are found only within the cell, proof that the leap towards carnivory did not involve some novel chemical but just a talent to pump one out. The sundew enzyme that cuts up nucleic acids (a material abundant in insect cells) looks rather like those secreted by all plants after damage. That, too, was hijacked. In the same way, the enzyme used to chew up the hard outer husk of an insect is close to those made by other plants when placed under stress.
Most leaves can absorb some molecules, small and sometimes large, through their surfaces. Darwin himself found that even species that never eat insects, such as Primulas, could transfer nitrogen-rich nutriments like ammonium carbonate across their leaves. His observation led in time to the idea of ‘foliar feeding’. Instead of adding fertiliser to soil, where it can be washed away or rendered useless through chemical change, the hope was to spray it on to leaves, whence it would enter. In alkaline places there can be plenty of iron and manganese - both needed for healthy growth - but they are bound into soil compounds that will not release them. For some organic gardeners the idea has become almost a cult, but it gives real benefit only when rare nutriments are in short supply. Some places lack zinc, or copper, or boron, all needed in minute amounts. A quick spray does a lot to help. The technique is of no use for nitrogen, which is needed in large quantities, for leaves are too small to soak enough up.
Carnivory is just a further step - a case of the biter bit - in the endless battle between the insects and their vegetable prey. Each of their tactics is in use somewhere else, for a different reason. All that evolution had to do was to put the package together. The end result can be achieved in quite different ways, each of which works reasonably well.
The relationship between a carnivore and its prey shows a clear divergence of interest. Even so, their conflict can sometimes shade into what looks like cooperation. Many insect-eaters depend on third parties to help them. The North American pitfall known as the Virgin Mary’s Socks (from its purple colour and the footwear of the Pope) has no digestive enzymes of its own and depends on bacteria to do the job. A South African species that, at first sight, looks like a typical carnivore has sticky hairs that trap insects - but it gains goodness at second hand. A bug makes its home upon the leaves and feeds upon the corpses, and its excreta feed its host.
The struggle for existence between fly-trapper and fly is easy to observe. It is a microcosm of nature red in leaf and glue. Some insects, in contrast, live not as prey for plants, but - like the South African bug - in apparent harmony with them. Certain ants, too, defend their hosts against attack - a talent known to the fourth-century Chinese, who put their nests into lemon trees. As is true for the insect-eaters, the tie between the two kingdoms has prompted the evolution of some remarkable organs, each of which has emerged, like a snap-trap or a flypaper, from a distinct part of the plant’s anatomy. A celebrated passage from The Origin reads: ‘If it could be proved that any part of the structure of any one species had been formed for the exclusive good of another species, it would annihilate my theory, for such could not have been produced through natural selection.’ The helpful ants might appear to be such a threat, but they support the idea of evolution and do not annihilate it. On the way they hint at how insectivory began, for they pay a good part of their rent not with aggression, but with nitrogen. They add a whole group of new members to the grand botanical convergence that faces the fertiliser problem.
Thomas Belt was an engineer and naturalist who spent five years in charge of a gold mine in Central America. Darwin called Belt’s 1874 book A Naturalist in Nicaragua ‘the best of all natural history journals’. It notes how some trees in the Acacia family have fallen into an association with certain ants, who protect them against grazing insects and mammals. As Belt saw, the balance of advantage is delicate indeed.
The total mass of ants in a patch of Amazon jungle is four times that
of all its mammals, birds, reptiles and amphibians put together. Certain plants, there and elsewhere, have put them to work. Many tropical trees have hollow thorns which shelter the vicious insects, together with small structures filled with sweet and sticky material. Both parties benefit, for any creature that dares to browse on the tree is attacked and the ant gets a free meal. If its garrison is killed off with insecticides the tree is attacked by grazers at ten times the previous rate. The helpers also prune back branches of nearby trees that shade their host, and clean up the ground around its trunk, reducing competition for food. Some ants even poison nearby plants as they inject formic acid into the leaves. That then allows their own host to flourish on patches of cleared ground known to the locals as ‘devil’s gardens’ and thought to be cultivated by an evil and cloven-hoofed spirit. In return the insects feed on secretions from the acacia’s leaves and feed their young from what Darwin called its ‘wonderful food bodies’. They also gain protection by laying eggs inside the hollow thorns.
More than a hundred distinct groups of tropical trees, and forty families of ants, have entered into such an alliance. The habit has evolved many times and - like insectivory - has enabled natural selection to pick up a diversity of parts for use in a novel way. The shelters are based on thorns, on hollow stems or on rolled-up leaves, or on special pouches made on the surface of the leaf. Once again, evolution makes do and mends, as it must.
The details of the liaison give proof of Darwin’s insistence that natural selection allows nobody a free lunch. At first sight, the bond between ant and trees is based on a shared dedication to a common end. In fact, each tries to get the most out of the arrangement while putting the least possible in. Their tactics hint at how the tie between the botanical carnivores and their prey may have begun.