by Colin Tudge
In general, then, trees like all living creatures have a mixed relationship with their own kind, and with all other creatures: part war, part peace, and part uneasy truce. This is true even of the creatures that eat them and cause diseases.
LIFE’S TORMENTS – AND AUTUMN COLOURS
All trees, like all plants, are beleaguered from the time they are seeds to the time they return to the earth by predators and parasites. Predators in this context means big herbivorous animals, from cattle and squirrels to leaf monkeys; and parasites are loosely defined here to include the viruses, bacteria and fungi that are commonly known to cause disease, and all the animals such as worms, insects and mites that burrow into them, and indeed all the insects and other creatures commonly classed as pests. Old-fashioned accounts of ecology tended to pass over the parasites as if they are mere accidents. Yet they are major drivers in all of nature, that may determine the shape and direction of an entire ecosystem. We have seen the role of nematodes in the fig–wasp relationship. More profoundly, the need to avoid parasites may largely explain the huge variety of trees in tropical forest: no tree can afford to be too close to another of the same kind, for fear of infection. More cogently still, it may be that if there were no parasites, there would be no sex, and the transformation of all life would then be absolute. It isn’t simply that creatures would live their lives very differently. Without sex to mix the genes, creatures like us (and oak trees and mushrooms) would not have evolved at all. It seems indeed that we are as we are, and trees are as they are, because our respective ancestors had to cope with disease.
In truth, parasites and other pests do a deal of damage, and trees seem particularly vulnerable because they must stay in the same place for so long – not like annual plants, which metaphorically speaking are here today and gone tomorrow. Most tree diseases pass most of us by most of the time, but everyone in Britain became aware of Dutch elm disease, caused by fungi of the genus Ophiostoma and carried by various bark beetles. Elms had been one of Britain’s most characteristics trees: the ones most likely to persist in hedgerows, where traditional farmers were happy to retain them for shade and as a future source of timber — a casual exercise in agroforestry. Elms feature strongly in the landscape paintings of Constable, from Suffolk, and they also grew so rampantly in the west country that they were known as the ‘Wiltshire weed’. But within about a decade, between the 1970s and 80s, English elms above the size of a small shrub were all but eliminated – one of the most dramatic extinctions in historical times.
Of course all trees suffer from pests and diseases to some extent. The average oak in Britain loses roughly half of its leaves each year to insects. Caterpillars sometimes take virtually all of the first crop of young leaves in spring, whereupon the oak may respond with a second flush in May and June, known as ‘Lammas growth’. (Although Lammas, meaning ‘loaf mass’, is a Christianized pagan festival that falls on 2 August. Hmm.) Periodically we read of threats of various kinds to oaks or chestnuts in Europe and the United States from fungi or viruses or whatever, until it seems we will soon be lucky to have any traditional species at all.
The world’s two most valued tropical hardwoods, teak and mahogany, both have their dedicated pests that beleaguer them in the wild and hugely affect their economy in plantations. Teak suffers primarily from the defoliator moth, Hyblaea puera, whose caterpillars may strip the leaves completely almost every year, soon after they emerge. This leaves the trees gaunt and skeletal – teak trees are often a sad sight – and also means they take much longer to reach harvestable size. Thus traditional plantations in India typically raised teak on an eighty-year cycle. Modern selection and cultivation has brought this down to thirty years. But in Brazil, where the defoliator moth mercifully remains absent (the trees left it behind in their native Asia) the cycle of harvest is down to eighteen years (or so Brazilian foresters are hoping). New research in India on biological control promises to deal with the moth at last, but we have yet to see whether it works. Mahogany is plagued in particular by caterpillars of shoot-borer moths, which burrow into the growing tip and destroy it. The tree does not die, but instead of growing straight and true as a prestige timber tree should, it sends out a mass of branches below the ravaged tip, like a bush. The reasons are as described in Chapter 12: the growing bud normally sends out a hormone (auxin) to suppress such unruly behaviour. With the source of the hormone gone, the lesser buds beneath are given free rein. Many other valuable trees worldwide (the cinnamon plantations come to mind, on Madagascar) have their own particular murrains that are of huge economic importance.
Trees, like all living creatures, contrive in various ways to make life difficult for their parasites. Commonly, tree leaves are low in nutrients: the parasite has to work prodigiously hard simply to get enough to eat. All trees present physical barriers to would-be predators and parasites, including thick waxy cuticles on their leaves that inhibit the entry of fungi or bacteria, while deciduous trees plug the scars left by their falling leaves with cork, like Elastoplast. Finally, trees are fabulous chemists. In addition to the proteins, fats, carbohydrates and other materials they need to synthesize for the everyday tasks of staying alive, they also turn out a huge range of recondite molecules known as ‘secondary metabolites’. Clearly these are not essential for day-to-day living. Some trees produce some kinds of secondary metabolites, and some produce other kinds, and some seem to produce very little at all. In times gone past botanists wrote them off as waste or by-products: things the tree produced apparently through carelessness. That is how plants might have produced them first of all, in the deep evolutionary past. Now it is clear that secondary metabolites play many vital roles in the life of the plant – and paramount among them is the repulsion or destruction of would-be predators and pests.
But although pests and predators clearly do cause huge problems, the relationship between trees and their tormentors is not a simple battle. The subtleties are far from understood – the research is difficult, and most studies so far have focused on the pests of herbaceous crop plants, which are easier to work with than trees, and offer quicker financial returns. But already we can see that between trees and their parasites there is the same counterpoise of antagonism and collaboration – war, peace, and uneasy truce – that we find in all ecology. Over time we can discern co-evolution, as each player in each relationship adapts more and more minutely to the other. When the relationship is antagonistic, this co-evolution becomes an arms race, with predators or parasites and prey each upping the ante as the centuries pass. When it is cooperative, the relationship tends to become more intricate with time, until the various players become totally interdependent. The little that is so far known about trees and their parasites already reveals relationships of endless subtlety.
Upping the ante is the first sign of an arms race. So it is that many trees have spines and prickles. But spines and prickles (like cuticles and corky plugs for leaf scars, and all the secondary metabolites) require a lot of energy to produce. So we find that in various ways, trees contrive to be minimalist. Thus as we noted earlier, many species of palm that live in continental forests where predators abound are spiked as fiercely as a medieval prison, while related types, on islands free from abuse, are spikeless. So we find too that the leaves of holly are spiny on the lower branches, where they might be browsed by deer and cattle, but tend to be spineless higher up. In general, a plant that can do without spikes and such adornments has energy to spare for other things, like rapid growth – and in a competitive world, other things being equal, it doesn’t pay to waste energy on things that are not necessary.
In their secondary metabolites, too, we see on the one hand a continuous upping of the ante – the trees becoming more toxic, the predators and parasites evolving new ways to cope – but also the constant need, on both sides, to economize.
Among the commonest of the secondary metabolites – very evident in oaks, for example – are the tannins. Tannins bind with the proteins of animals
and in various ways disrupt their feeding – and are used for tanning leather, making it tougher and more waterproof, which is where they got their name. Heartwood rich in tannins is evidently less prone to rot than wood without tannins – although, of course, old oaks tend eventually be hollow; and in truth (for nothing is simple) trees that are only partly hollowed (but not so much that they fall apart) may be stronger than those that are still solid, just as an iron pipe may be stronger than a solid rod. Cattle, deer and apes are among the creatures known to be put off their feed by too many tannins but rodents and rabbits have joined the arms race and have adapted to them. They produce an amino acid (proline) in their saliva which binds with tannins and blocks their activity. Other mammals are attracted to the astringency of tannins – and so it is that human beings like tea, and tannin-rich red wines. But then, for mammals at least, tannins are not all bad. Evidently they block the chemical signals that cause blood vessels to contract. Red wine is known to protect against heart disease – and this may be in part because the tannins help to dilate the coronary blood vessels that feed the wall of the heart. Tea, a cardiologist now assures me, has the same effect; pleasing news indeed.
Insects in general are put off by tannins – but, as part of the arms race, some at least have evolved ways of coping. Leaves tend to focus first on growth, and only then have energy to spare to create physical defences and secondary metabolites; so pests such as the moths whose caterpillars feed on oaks commonly focus on the youngest leaves. Deciduous trees in turn seek to outwit the moths by producing their springtime leaves with tremendous speed. Thus the buds of oaks seem to unfold before your eyes. Still, though, the moths are liable to win because they have already laid their eggs on the oak’s buds. The caterpillars emerge just before the leaves, and so are lying in wait. How the eggs know when exactly to hatch, is unknown. Do they simply respond to the same climatic signals as the oak buds do? Or do they pick up some chemical signal from the oak itself?
Many trees and other plants produce secondary metabolites known as ‘terpenes’ that are specifically insecticidal. Among the best known terpenes are the pyrethroids, which human beings have extracted in particular from African daisies of the genus Chrysanthemum (which is not the same as the ‘chrysanthemums’ of the florist), and adapted as commercial insecticides. Pines, firs, and many other conifers harbour similar agents in their resin ducts. Of course, it is expensive for the tree to produce such chemical agents. But the conifers economize by not producing more than they really need: at least, when they are attacked by bark beetles they produce more terpenes in response.
The terpenes also include the ‘limonoids’ found in citrus fruits: the skins of oranges and lemons also repel insect predators. The most powerful insect repellent known is also a limoinoid: this is ‘azadirachtin’ – produced by the all-purpose medicinal neem tree, Azadirachta indica. Azidarachtin will repel insects in astonishingly low concentrations (fifty parts per billion) and also has other toxic effects – yet it has no toxicity to speak of in mammals. So, like the pyrethroids, it is favoured as a commercial insecticide (and modern politics being what it is, the neem tree is now the cause of international disputes).
All the chemical agents cited so far tend to stay within the plant that produces it. But many others are ‘volatile’, meaning that they rapidly evaporate and float off in the wind. Some of these volatiles, particularly those known as ‘essential fatty acids’, are highly scented. Hence the fragrance of sage, mint, basil, and other such relatives of teak. Hence, too, the powerful medicinal niff of the eucalyptus. Chemical repellents that are not volatile have no effect until the predator has taken its first bite – but the volatile ones warn insects and other creatures to stay away before they attack: a more sophisticated measure altogether. But, as with tannin, these essential oils often prove agreeable in small quantities, and human beings, ever opportunist, extract the oils of eucalypts (and many other plants) for perfumes and medicines – simply by boiling them up and then distilling the oil.
Then again, a few specialist animals, equally opportunist, have developed ways of coping with such repellents. Thus the essential oils of eucalypts are toxic to most animals (in their raw state) – but koalas are equipped with a huge extension of the gut (the caecum) which is packed with symbiotic bacteria, and these detoxify all the noxious compounds in eucalypt leaves. Very few other creatures can cope with eucalypts, which is one reason why the trees are so successful. Because koalas can cope they have the entire run of Australia’s host of eucalypts (600 species or so) almost (though not quite) to themselves. Indeed, koalas will eat very little else, and usually nothing else at all, except eucalypts – and different populations of koalas typically confine themselves to just one or a few eucalypt species, and reject others. Very few mammals are anything like so specialized. Pandas munch almost exclusively on bamboo but they will eat many other things besides if given half a chance, from omelettes to roast pork. But creatures that specialize in eating toxic tree leaves pay a price. Brains are particularly susceptible to toxins. Koalas, like the leaf-eating monkeys and the peculiar leaf-eating Amazonian birds known as hoatzins, have smaller brains than their more omnivorous relatives. Even the best friends of the koala have little praise for its intellect.
Legumes (Fabaceae) are among the most accomplished chemists of all. Many produce soap-like ‘saponins’ which interfere with animal digestion. Many produce ‘flavones’, some of which are strong insecticides – and again have been exploited commercially. Legumes often produce agents that limit the oestrogen hormones of mammals, so that sheep grazing on legume-rich pastures often become infertile. I know of no direct evidence of such activity in leguminous trees, but it would be very surprising if there were none. Many leguminous trees secrete similar flavones into the soil – not to kill insects, but to help establish good relations with the nitrogen-fixing bacteria that they seek to entice into their roots. Complex chemicals in general are versatile. Any one molecule, with or without further chemical adjustment, might kill one group of creatures and attract others.
Flavones impinge directly upon our senses, did we but know it. Among them is anthocyanin, the material which, in a myriad slightly different chemical forms, provides plants with a broad palate of pigments, all red, but ranging from gentle tints through the brightest scarlet to maroons and purples. Flowers and fruits are often red, of course – but so too, surprisingly often, are leaves. In particular, the young shoots of tropical trees are often red – as are, in the autumn, the dying leaves of many a temperate tree, perhaps most famously the maples that are the piece de resistance in the glorious autumn colours of New England, one of the greatest natural shows on earth.
Anthocyanin is not produced gratuitously, it seems. It is a ‘secondary metabolite’ to be sure, but it is no mere accident. Chemically, it is expensive to produce. So why is it produced in young tree shoots (especially in the tropics) and in dying leaves (especially in temperate countries)? What do the two have in common?
New work based both in the US and in New Zealand shows beyond reasonable doubt that anthocyanin is protective. In particular it is an antioxidant. Creatures like us and trees need oxygen of course, in constant supply, to stay alive. We need to burn sugars to provide ourselves with energy. But oxygen does such a good job on sugars because it is so lively, and we admit it to our bodies at our peril. Left unchaperoned, oxygen gives rise to a whole range of ‘free radicals’ that destroy our flesh and corrupt our DNA – and do the same in trees. Any creature that aspires to live where there is oxygen (anywhere, in fact, that is not some murky swamp) must equip itself with anti-oxidants, to keep oxygen (or, rather, the radicals it gives rise to) under wraps. In people, these anti-oxidants include many a vitamin, including C and E. In plants, they include some enzymes, and the agents known as phenolics. And they include anthocyanin.
Trees, like all creatures, are most vulnerable to attack by oxygen radicals when under stress. Young leaves, before they have all their chemical and physica
l defences in place, are tender. High in tropical trees, exposed to the fiercest sun and sometimes short of water, young leaves are extremely vulnerable. Extra anthocyanin protects them.
But why should dying leaves produce such expensive stuff? Why should they be protected when their number is already up? Precisely because the state of dormancy that temperate trees enter in the autumn is not a simple shutting down. Before they pack up for the winter, deciduous trees withdraw as much nutrient as possible from their leaves. Chlorophyll, the principal protein, is broken down, the nitrogen it contains carefully drawn back into the body of the tree, to nourish next year’s growth. But the breaking down is stressful. It opens the leaf to attack by oxygen radicals before the work is complete. So (modern theory has it) trees such as maple produce anthocyanins to keep the oxygen in check, and allow the withdrawal of chlorophyll to proceed in good order.
We might ask, of course, why all deciduous plants don’t do as the maple does; why most of them are not bright red in autumn. The general evolutionary answer would be that nothing is for nothing. Anthocyanin helps the maple to sort out its problems – but it is expensive. Other trees may simply find that it is more trouble to produce anthocyanins in the autumn, than to endure a little damage. Or they may simply not have got around to producing anthocyanins in autumn, for not every species does everything that is theoretically possible.
The general notion that anthocyanin is actively protective fits neatly with a whole range of otherwise bizarre observations from other trees (and other plants) in many different circumstances. Thus it is that when insects bite the horopito tree Pseudowintera colorata of New Zealand the wound turns red: an outpouring of protective anthocyanin. It also fits the common observation that New England’s autumn colours are most spectacular when the weather is cold, or has been so. It’s then, after all, that the trees are under greatest stress. Horopito is a relative of winter’s bark, in the Winteraceae.
