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Authors: Steve Jones

BOOK: Darwin's Island
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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.
Often, the special food is produced only when enough ants are around to make it worthwhile. Some trees are even more parsimonious. The whistling thorn of Kenya, which gets its name because the wind howls through its hollow thorns, uses ants to keep hungry giraffes at bay. It gives shelter, but no food, to its resident army. Ants cheat just as much, for some get a meal from the honeydew made by scale insects that feed on sap (and do no good to the tree) while others have little interest in attacking herbivores. Some species are even more selfish, for they castrate their host by chewing off flower buds to ensure that it does not waste its efforts on show, but puts out new and tasty shoots, with their free food instead. The tree fights back with a chemical that keeps the ants off the flowers. Yet another insect destroys its host’s food bodies to dissuade more aggressive ants that might protect the tree but throw off the resident.
The ants gain sugars, based on carbon, from their host - but their corpses and those of their prey provide precious nitrogen to the tree. The shelters have thin walls through which the excretions of the residents, or the remains of their bodies, are picked up by the host tissue. Some acacias take, as a result, nine-tenths of their nitrogen from their insect visitors. It would not be too hard to transform an arboreal ants’ nest into a trap that soaks up nitrogen while giving nothing back.
 
The acacias, like the sundews, are nitrogen hunters that depend on other creatures for help and, with the entry of the ants, make that hungry clan - already diverse - even wider than before. A further look around the botanical world shows that the tactics of acacias or Venus flytraps are feeble when compared with the ingenuity shown by other species. Many plants thrive in what would otherwise be famine conditions thanks to a series of obscure but intimate associations with other creatures in the search for the essential element. They negotiate not with insects - which, as animals, are quite close to plants in evolutionary terms - but with bacteria and fungi around their roots that pull the gas from the air and receive food and shelter in return. That habit is central to the survival of life on earth. It represents a series of evolutionary convergences between minute creatures far less closely related to each other and to their hosts than are insects.
The roots of many plants secrete chemicals that attract bacteria able to transform bound nitrogen into a more digestible product. They then soak up their invaluable wastes. Peas, beans and certain trees have entered into a closer arrangement with specialised ‘nitrogen-fixing’ bacteria that combine nitrogen gas in the air with hydrogen to form ammonia and other compounds which can be soaked up by roots. Many of the insect-eaters and ant-exploiters, with their spectacular adaptations above the ground, also depend on a similar pact with tiny aliens within their roots.
Farmers take advantage of such arrangements when they rotate their cereal crops with legumes such as clover and soybeans, all of which have close relations with nitrogen-fixers. Together, such plants now generate half the nitrogen used on the world’s farms. Without them we would starve. Their bacterial allies make a special enzyme which forces the sullen molecules of the gas into a marriage with the active hydrogen ions made as food is broken down. The reaction consumes a great deal of energy and costs both the bacteria and its host a lot.
Before today’s technical developments in biology, the bacterium involved, and the protein that does the job, looked more or less the same in each of the thousands of species that indulge in the habit. They are not. Just as in the insect-eaters, many unrelated plants, and even more of their minute helpers, have taken up the pastime. DNA shows that bacteria themselves, unimpressive as they might appear, are more diverse as a group than are the two kingdoms of animals and plants put together. The nitrogen-fixers span a good part of the spectrum of bacterial life. They are joined in their helpful habits by fungi, who are themselves more related to ourselves than are bacteria, and by members of a quite distinct group of single-celled beings known as the Archaea that teem in hot springs, deep sea vents and the soil. The sea, too, is itself full of a great variety of gas-fixers, most of them little understood.
Most of the bacteria involved live for most of the time alone. When they come into contact with a root of the right kind, a certain sugar locks into a receptor on its surface. The nitrogen-fixer squeezes its way in and its host’s cells divide to produce a nodule filled with descendants of the invader - a billion or more from a single founder cell. Both parties benefit for the plant provides fuel for the hard chemical work needed to drag the crucial element from the air while the bacteria churn it out in a form that can be used by the other member of the consortium.
The association between the two emerged, in evolutionary terms, not long ago; just after the destruction of the dinosaurs. There was, at about that time, a sudden outburst of carbon dioxide and a spike in temperature, both of which favour plant growth - and meant that a sudden shortage of nitrogen made it worthwhile to enter into the arrangement. It has evolved again and again in distantly related families. Alder trees (but not their close relatives the beeches) have root nodules that contain bacteria better known as the producers of the antibiotic actinomycin. With their help the trees grow on starved soils such as those on dunes or mountains. Tropical ironwoods have the same association as do a few members of the rose and pumpkin families. Liverworts, certain ferns and the giant rhubarb of Brazil all benefit from the ability to use single-celled creatures to soak up the vital gas.
The plants that have come up with that solution are diverse indeed. The creatures that do the work are far more so. The nitrogen-fixers within the roots of beans, clover and their relatives have been widely studied because of their economic importance. Hundreds of different helpers have been pressed into service. Some are tied to a single host - or even to a particular cultivated variety of peas or beans - while others are promiscuous. Under a mask of similarity, the biochemical mechanisms involved, the molecules that signal willingness to enter into an association, the amount of food provided and the rewards paid are diverse indeed.
Like ants on acacias or insects that buzz around a pitcher, the system shows a fine balance between cooperation and conflict. Some bacteria enter their hosts through wounds as a hint that they were once agents of infection (a few are related to known pathogens). Others grow within a membrane that protects them from attack, or make poisons that suppress a host’s ability to fight back. The plants have stayed suspicious of their partners. Now and again a cheat gets in - an invader that produces little of its valuable product but demands free food and shelter. At once the host cuts off supplies, the nodule withers and the fraudster starves.
 
Nature’s market in nitrogen turns over billions of tons of the element each year, which passes from air to soil, from land to water and from plants to animals and back again in an endless cycle. As is true for all markets the accounts of profit and loss are checked with great care. The struggle for the element is pitiless as is that for water, air or sex, but only now and again is the truth of its dealings exposed in all its brutishness. Plants that eat animals are just one instance among many to show how competitive that business must be and how the most improbable expedients are pressed into service to squeeze the most out of what little is on offer.
Now the global trade in nitrogen has been thrown into turmoil. Farmers pour nitrogenous chemicals on to the soil. They buy it from factories that each year generate a hundred million tons of the stuff from oil, or by extracting the gas from the air. The reaction is carried out with the help of catalysts in boilers held at high temperature and extreme pressure. Without that technology, invented just a century ago, the world would starve. The industry is profligate indeed in its use of power, most of it gained from burning the remains of ancient life. Cars, chimneys and aircraft also pump nitrogen salts into the air. All this means that far more nitrogen is available in useful form than in Victorian days. The amount has doubled in the past century.
To add fertiliser to fields does increase the yield of crops but also changes the economics of their bargain with a living source of nitrogen. First, it alters the balance of profit and loss. After a dose of fertiliser, crops need less help from their tiny assistants and squeeze them out. As a result the amount of the element taken from the air by those useful creatures goes down, so that the overall gain from the added nitrogen is less than it might otherwise be. For the starved soils of Africa such opportunistic behaviour by the plants is a real problem.
In addition, excess nitrate is washed to where it is not wanted, and more is added by acid rain, itself full of salts of the element emitted by exhausts and chimneys. Insectivores, ant-shelterers and bacterial hosts all respond, for now they have a cheaper source of the crucial nutriment than they did before. The rain-fed bogs of New England were once full of pitcher plants that flourished as they sucked up nitrogen from their prey. Their competitors could not manage in such starved places. The acid marshes have been enriched. In those hardest hit - near cities or close to fertilised fields - the insect-eaters have abandoned their carnivorous habits in favour of a conventional life. Other species move in and drive the pitchers and Venus flytraps to extinction, and in Europe the sundew faces the same problem, which means that the insectivores are converging in death, as they did in life.

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