Fifty years ago, as a young Forest Entomologist, I visited some of the great balsam fir forests of Canada when they were being attacked by spruce budworm caterpillars. Whole forests were being totally stripped of foliage and nearly all the trees over huge areas were being killed. Only a massive program of aerial spraying with insecticide prevented the death of many more. Some years later I witnessed the same thing happening to plantations of mature pine trees in New Zealand. This time native caterpillars had suddenly found these introduced trees to their taste. There were so many caterpillars eating the needles that, when standing inside the plantation, I was constantly showered with a fine rain of their droppings and could hear them pattering on the forest floor. Some areas needed spraying to save the trees, but most, without being sprayed, subsequently put on new growth that was not attacked. The plantations were again green and healthy, and caterpillars were again few and hard to find.
These two incidents are far from isolated examples. Somewhere in the world there will always be similar attacks taking place. Yet for most of the time, in most places, forests stay green and healthy. 'Why is this so?'
From time to time in many parts of the world, great plagues of locusts will descend, apparently from nowhere, and strip every last vestige of green from the landscape. Mostly, however, locusts are rare and hard to find, like the forest defoliators.
Looking yet further afield, we see that wherever there are plants growing there are all kinds of animals eating them. Everything from large mammals to tiny insects can be seen at all times, and everywhere, spending most of their lives eating plants. And there really are vast numbers of these animals. The huge herds of mammals grazing on African grasslands are a good example. Less obvious, but even more plentiful, are the armies of insects constantly eating every sort of plant. Again, every so often one or other of these herbivores will destroy most or all of their food plants; but for most of the time they do not. On average, herbivores consume only some 7 to 18 per cent of all
the world's plant production. So, as with the forests, most of the world remains green.
In the face of all this, some obvious questions remain: 'Why, then, is the world green? Why do these plant-eating animals not devour all the available plants? And on the relatively infrequent occasions when they do, what has changed so that this can happen?'
The only exception to this picture of general greenness interposed with rare bouts of near-total destruction is when we look at our agricultural and horticultural plantings. Here the situation seems quite different - and much worse. On a regular, indeed constant basis, in all parts of the world, many insects are eating the plants we cultivate for our own use, and in such numbers that they can destroy our crops very quickly. To prevent this happening we must kill the insects first - and keep on doing so - otherwise this multitude of pests would leave precious little for our use. Nevertheless, in spite of our best efforts, each year they consume a significant proportion of our crops before we can harvest them; and continue their depredations whenever we store such produce for future use. These herbivores appear to be behaving like the locusts and budworms during outbreaks, and quite differently from most herbivores in nature. Presumably, too, their ancestors did not behave in this way when feeding upon the wild ancestors of our cultivated plants. Again we must ask: 'What has changed so that this can happen?'
Nobody would dispute that the world is green. Apart from the driest of deserts, or permanent icefields, plants grow on and cover nearly all surfaces of the Earth. They make up some 99.9 per cent of the weight of living things on Earth: only a tiny fraction of life consists of animals. If plants are removed from an area - by anything from fire to a bulldozer - they will quickly recolonise. Witness how soon plants start to grow on volcanic lava flows, or the tenacity with which they invade old buildings and other human constructions, like roads, once we cease to protect and maintain them. Think of some of the ancient cities found buried deep in the jungles of Central and South America. Nor are plants confined to dry land. Myriads of plants, from single-celled plankton to seagrasses and huge kelp, will thrive in water wherever sufficient light penetrates to enable them to photosynthesise.
Why then does the combined impact of all the many animals that feed on plants not make any impression on their number and volume? Why is it that, with the exceptions noted, herbivores seem able to eat no more than a tiny fraction of the huge amount of food that is there for the taking?
The usual answer to this apparent paradox is that before they can eat very much most plant-eating animals are killed by their natural enemies - their predators, parasites and diseases - or they kill each other competing among themselves for access to food or some other resource in short supply. Much of today's research by ecologists, and all of our attempts at biological control of pests of our crops, are based on the first presumption.
When we look closely at this explanation we find that some pretty involved logic has been used to arrive at it. Basically the argument goes like this:
• The great bulk of plants not eaten by herbivores dies and is quickly devoured by decomposers (mostly micro-organisms). These microbes must be limited by their food because they eat all the dead plants. If they did not, dead plants would accumulate and form fossil fuels.
• Plants, too, must be limited by a shortage of their food (nutrients dissolved in soil water) because hardly any of them are eaten by the herbivores, yet they do not increase without limit.
• Herbivores, however, cannot be limited by their food because they eat so little of it. Nor is there any evidence that weather directly controls the numbers of herbivores; so this leaves only predators, or competition among themselves, to keep their numbers in check. On the rare occasions when they do eat most of their food plants, it must be because they have been 'protected' from their predators by human activity or 'natural events'.
• Finally it follows that because predators are regulating the numbers of their prey, they must, by their own actions, be limiting the amount of their food.
• The conclusion, then, is that all plants and all animals - except herbivores - are short of food, so their numbers cannot expand beyond the limits set by that food. Only herbivores are regulated by their predators, or by competing among themselves for limited resources, at densities below that which their food could support. So the world stays green!
But wait a minute. Why should herbivores be the exception? Might there not be an alternative and simpler - more parsimonious - explanation (a rigorous requirement of all scientific explanations)? What if green plants are not really the good food they seem to us? What if most plants are so nutritionally poor that, even in the absence of predators and competitors, most herbivores starve while eating their fill? Then all this deductive reasoning falls down, and we are left with the proposition that all animals, whether they eat plants or other animals, are limited by their food.
What evidence is there to support this proposition?
First we should ask: 'In what ways might plants, while remaining everywhere abundant, be an inadequate source of food for herbivores?' There are three ways they could do this: they might become too hard to find; become distasteful or poisonous; or become nutritionally so poor that few can survive by eating them.
In the first case, the sort of plants that a particular herbivore can eat could be perfectly palatable and nutritious food, but so scattered and rare that the chance of the herbivore finding one among many other inedible plants is remote. To our eyes many species of plants are widely scattered and hard to find among other sorts of plants. However, this strategy of the plants has been readily countered by herbivores. They have evolved the ability to disperse with great efficiency, and to find their food plants no matter how infrequent and cryptic they may be.
This is particularly well illustrated by many small invertebrates like aphids and mites. Their bodies are so tiny that they will float away on the merest breeze. Many have evolved the behaviour of climbing to the top of a plant and launching themselves from it early in the morning. The air is warming and rising then, so they are quickly carried upwards and may travel great distances before falling from the sky late in the day as the air cools. (Try sitting out in the garden some cool summer evening after a hot day. Before long you will find small winged beasts landing on your clothes and starting to walk about.) For the great majority of these creatures the consequences of dispersing like this are grim. Most individuals will land where there is no suitable food plant, and quickly perish. For the population as a whole, however, the outcome is good; such great numbers are spread, and they become so widely scattered, that every suitable plant will be found. A lucky few of the many will land on the right plant.
I once witnessed a particularly arresting example of this power to find a rare host. I was walking across a large area of recently cleared and ploughed land and came upon a single 25 cm twig of Eucalyptus that had sprouted from a surviving root, and bore but half a dozen leaves. It was hundreds of metres away from any other green thing, and several kilometres from the nearest tree of the same species - a tiny target in the midst of a sea of bare earth. Yet on these few leaves were several 2 mm-long winged females of an insect that will feed on no other species of eucalypt. They were busily laying eggs. Later I was able to observe such females launching themselves into the morning breeze from the plants where they had grown, and catch some of them with a net towed by a light aeroplane 300 m above the land.
When a plant is found in this way it is quickly colonised as the animals multiply, producing enough progeny to devour the plant. Sometimes they do this. Usually, however, very little of the plant is eaten. Why is this so?
A second line of defence open to plants is to produce noxious chemicals so that they are distasteful or poisonous to any animal attempting to eat them. Plants generate a bewildering array of these chemicals. Or they could produce thorns, thick cuticle or hard seed coats to protect themselves from attack. They do this too. Again, however, herbivores have easily evolved counters to these strategies. They detoxify, sequester or simply avoid ingesting such chemicals, and circumvent physical barriers. A good example of the first is the poison 1080, widely used in Australia against introduced rabbits, pigs, foxes, cats and wild dogs. For them it is a deadly poison without antidote. However, it is a natural constituent of some Western Australian plants, and native animals in Western Australia which eat these plants are immune to it. In the eastern states, where 1080 does not occur naturally, these same native animals are not immune.
Many insect herbivores are not only immune to harmful substances in their food plants - they have become addicted to them. They need them as cues before they will attack a plant. Cabbage white butterflies are like this. They will only lay eggs and their caterpillars will only feed upon brassica plants - cabbages, cauliflowers, brussels sprouts, etc. - which contain specific toxins; those which give these plants their characteristic 'mustard' taste. Others have gone a step further, and have incorporated toxic chemicals from their food plant into their own bodies to deter attacks by their predators. The wanderer butterfly does this. Its caterpillars accumulate alkaloids from the milkweed plants on which they feed and these make the body of the adult butterfly highly distasteful to any bird which attempts to eat it. Most learn to avoid them altogether. Those that do attack them quickly spit them out and then avoid others of the same kind.
One consequence of countering these deterrent chemicals is that the herbivores that are successful at doing so are usually - like the butterflies mentioned above - specialists, each feeding on only one species of plant. So the plant has been successful in limiting the number of species which are able to use it as food, but not the number of individuals of an adapted species.
So having, by whichever means, neutralised this second ploy of the plants, adapted herbivores have the potential to eat out their food plants. But mostly they do not. Why not?
The third way plants might avoid attack, even though they are abundant, easy to find, palatable and non-toxic, is to simply be inadequate food for the herbivores. They would do this if they lacked any one nutrient that animals must have in order to grow and breed. What is more, no animal could evolve a counter-stratagem to the absence of an essential nutrient. However, the common biochemistry of life precludes a plant from doing this; the chemicals needed to grow a plant are the same as those needed to grow an animal.
On the other hand, a plant could evolve to the point where an essential nutrient in its tissues is so dilute that a herbivore could not eat enough of the plant before perishing from malnutrition. Alternatively (because plants, too, must deliver nutrients into their new growth and their reproductive organs) the plant could limit the time that an essential nutrient is concentrated in its growing tissues or flowers and fruit. Then, while a herbivore may thrive by eating those tissues, it will be able to do so for only a short time. Soon it would again be reduced to consuming poor quality food.
As I shall discuss in this book, there is widespread evidence that plants have evolved both of these latter strategies.
Not surprisingly, then, we find that herbivores have, as they have with the other tactics, evolved a whole suite of structural, physiological, behavioural and life history adaptations to counter this dilution of their food. Nevertheless, once again, they rarely eat very much of the available plants. Why not?
Because, in spite of these adaptations, the third strategy has been relatively successful; for most of the time herbivores do not get enough good food. Specifically, their young seldom get food of sufficient quality to enable them to survive, let alone to grow. Those few that do grow to adults can then usually, but not always, get enough to maintain themselves. Only rarely and spasmodically, however, is their food nutritious enough, for long enough, to allow them to breed, and their new offspring to grow.
It would seem then, that if you are a herbivore, you can evolve ways to find plants trying to hide from you and you can counter or avoid poisons they produce to deter or kill you. But, having done so, there is little more you can do if you are then confronted with not being able to get enough basic nutrients from your food, no matter how much of it you eat.
So, the answer to the question 'Why does the world stay green?' is not the most widely espoused, and apparently obvious one: 'Because most animals that eat plants are eaten by other animals before they can eat the plants, or are prevented from eating them by other animals also trying to eat the same plants.' Rather it is one which is not intuitively obvious: 'Most herbivores starve while eating their fill of plants which look (to us) to be perfectly good food, but are actually quite inadequate food.' A universal feature of the life of all herbivores which illustrates this, and which is in stark contrast to that of carnivores, is the time they spend eating, the volume of food they consume, and the consequent volume of faeces they produce. They spend the greater part of their lives eating, constantly processing large amounts of poor quality food in order to extract sufficient nutrition from it.
To be more specific, plants are poor food for herbivores because they are mostly carbohydrate, and contain insufficient nitrogen for the production and growth of young herbivores. Furthermore, it is not just any old nitrogen that is in short supply. It is the nitrogen in quickly and readily absorbed amino acids that are essential for building new body protein. These amino acids are so dilute in plants for most of the time that herbivores are constantly striving to get enough of them. As a result they can produce few viable young, and most of those they do produce soon starve. And they will die whether or not others of their own - or any other - kind are trying to eat the same food.
I have referred several times to the commonly held belief that animals do not outgrow their environment because they compete among themselves for limited resources and the successful ones kill their competitors, or exclude them from access to the resources, so that they die anyway. But this belief is not tenable. Why?
There is no doubting that competition is a reality in nature. It is constantly observable and all-pervasive. And in this world it could not be otherwise. Once the first entities on earth (presumably simple DNA-like chemical structures) reached a stage of complexity where they could use other, simpler, chemicals in the environment to build copies of themselves, competition became inevitable. Why? - because, sooner or later, the supply of the least abundant of those elements which are essential for the building of new 'bodies' would run out. Once that happened only those better than others at gaining access to this now limiting resource would be able to make any more copies of themselves. And in doing so they would prevent others from using the resource. The unsuccessful ones would eventually disintegrate - 'die' - or be dismantled - 'eaten' - by the survivors which could then use their prey's released chemicals to build more of their own structures.
Since that presumed time competition has been a major force driving the evolution of more and more complex organisms over billions of years. Only those inheriting some attribute that made them better competitors survived to pass on their genes - or precursor genes - via new copies of themselves.
Much could be said about the role of competition in today's populations, but here I need make only two points. First, yes, it is vitally important in moulding the way in which plants and animals continue to evolve, because it decides which few of the many attempting to use limited resources survive. Whenever there is not enough for all, only those best adapted to out-compete their conspecifics survive and breed. Second, and of major importance to what this book is all about, no, competition does not decide how many individuals in a population survive. That is decided by the supply of the resource in short supply. Whether there are 1000 or 20 competing, if there is enough for only 10, then only 10 will survive. Competition is a consequence not a cause.
But what about the predators?
This leaves us with the other factor said to be preventing herbivores eating all the plants: predation. Predators are believed to be such efficient regulators of their herbivorous prey that they keep their numbers below the level that the available food could support. Yet this is not so. They are themselves limited by a shortage of their food. But not because they reduce the number of herbivores by eating so many of them. Their capacity to produce and raise young is constrained by their inability to catch enough of what seems, superficially to us, an abundance of readily available prey.
What, you may ask, is the evidence for all this? How can I justify such sweeping statements?
The rest of this book is devoted to explaining some of the evidence. It tells about many varied and fascinating ways in which herbivores have evolved to improve their access to the limiting nitrogen in their food, and how their predators fail to live up to their reputation as efficient killers. It also describes how some forms of competition have evolved that not only do not reduce the numbers that survive, but increase them. They do this by the highly inequitable allocation of what resources are available to just a few, thus ensuring a more efficient use of those resources. And, finally, it relates how it is the weather which is ultimately responsible for how much food there is, and so for how many animals there are.
Nitrogen - the key limiting factor
I should first explain why it is nitrogen, and not some other essential chemical - or energy - in food that is the key limiting factor.
Organised life on Earth is based upon four elements: hydrogen, carbon, oxygen and nitrogen, and it is fuelled by energy from the sun.
Many biologists believe, and base their research on the assumption, that what limits the growth of organisms is the supply of energy that they can access - from photosynthesis for plants; from plants for herbivores; from other animals for carnivores. The supply of solar energy is, however, to all intents and purposes, continuous and unlimited. Yet only a very small fraction of it is ever incorporated into plants and animals; most of it is re-radiated back to space as heat. Much less than 10 per cent of the energy reaching the Earth is incorporated into plants by photosynthesis. Only about one-thousandth of that is converted to herbivores, and the loss continues as herbivores are converted to carnivores, and so on, until only the original chemicals are left. If energy were the first to be limiting, would so much go unused? And would the little that is trapped be so wantonly wasted? For example, the evolution of warm-blooded animals would have been a very improbable event had the energy needed for their thermoregulation been in short supply. Similarly the large investment in energy required for long-distance migration by many birds is unlikely to have evolved if it were hard to come by.
The supply of the four basic chemicals, on the other hand, is not unlimited. However, carbon, hydrogen and oxygen are all very abundant and readily available. There seems little prospect they could run out. Nitrogen is equally abundant - but 99.95 per cent of it is inert gas in the atmosphere, and so unavailable to plants and animals. The remaining 0.05 per cent of the nitrogen on earth is combined with other chemicals, but half of this is in inorganic form and essentially unavailable to animals. The other half of that half of 1 per cent of all the world's nitrogen is in organic form. But 95 per cent of that is present as dead material in litter and soil or (mostly) as particulate and dissolved matter in the oceans. So, in contrast to the other three essential components of living things, nitrogen is in very short supply. And what little is available tends to be thinly spread in the environment. There is a relative, rather than an absolute shortage of it. Not surprisingly then, it is most often the first essential nutrient to become limiting for the growth and reproduction of both plants and animals.
Because of the inherited biochemistry of all life, nitrogen is required as a nutrient second only to carbon. It is the key component of amino acids from which proteins are built. And no organism - plant, animal or microbe - can survive or grow without a supply of nitrogen for the synthesis of proteins. Carbon, on the other hand, is greatly in excess of nitrogen in all living tissues. The ratio of carbon to nitrogen in the amino acids basic to all life varies from 1:1 to 2:1, while at the other extreme, in woody tissues of plants, this ratio reaches 1000:1.
Plants, of course, are the primary producers. Only they can fix energy from the sun. Animals must eat plants (or other animals) to obtain the energy to fuel their metabolism. Equally importantly, plants alone can incorporate inorganic nitrogen from the environment into organic forms that animals can then use to build their body proteins.
Plants must obtain all their nitrogen in solution from the soil, and all agricultural practice (including the use of manufactured fertilisers) attests to its acute shortage. Nature also illustrates this for us. The little carnivorous sundew or venus flytrap plants grow in soils with too little nitrogen to support normal plant growth and reproduction. They can survive and reproduce in such habitats only because they have evolved the capacity to catch and digest insects, thus supplementing the otherwise limiting supply of nitrogen with animal protein. But even then they are struggling. Feed them with more insects than they can catch naturally and they grow bigger and produce more flowers and seeds than those plants left to get by on whatever they can catch for themselves. Feed them with artificial nitrogen fertiliser and they can grow and reproduce without access to insect prey.
It is not hard to see, then, why a lack of nitrogen looms largest for herbivores, why it must be of equal or greater concern to the animals that depend on the plants for their food. Plants absorb nitrogen as ammonium or nitrate. Animals cannot do this. They must have ready-made amino acids manufactured by the plants.
For a start, however, herbivores are confronted with a food composed largely of carbon. Plants have used the great surplus of carbon in their environment for structural purposes, husbanding their scarce nitrogen to make protoplasm. As a consequence, most of the body of a plant is built of cellulose and lignin, both carbon-based. Animals cannot digest these tissues. So what nitrogen there is in the food of a herbivore is either locked away within indigestible cell walls, or is thinly and unevenly spread through the body of the plant. At best they can eat pollen or seeds, getting a food containing about 7 per cent nitrogen. At worst a diet of wood or xylem sap yields as little as 0.1 per cent nitrogen. Growing leaves will provide about 5 per cent. Animal tissues comprise around 15 per cent nitrogen, so they are mostly starting from well behind the eight ball.
But this is not the end of it. Much of the limited nitrogen that is present in the food of herbivores is in complex structural forms that require the expenditure of time and energy to break them down into the amino acids which the animals' digestive systems can absorb. It is only when the plant is transporting nitrogen as soluble amino acids to and from growing, reproductive and storage tissues that it is readily available. And all this is exacerbated by the fact that animals need much more nitrogen than do plants. Their structural materials are based on protein not carbohydrate.
Then animals have a third problem. Not only is nitrogen scarce in their diet, with much of it requiring expenditure of considerable energy before it can be absorbed, they cannot use all that they do absorb. The metabolic chemistry of all animals is such that in the process of converting nitrogen into body tissues, some must be excreted as metabolic waste.
And as I said earlier, carnivores, too, suffer from a relative shortage of nitrogenous food - but in a different way. While every individual animal that carnivores can capture is a rich source of useable nitrogen, for most of the time they just cannot catch enough of them, often enough, to meet minimal requirements for reproduction and growth. While to our eyes there may seem an abundance of prey just waiting to be caught and eaten by the carnivores, this is not so. Mostly the only prey predators can catch are the very young, the very old, the sick, the wounded or the momentarily incautious or just plain unlucky. As a consequence it is failure to breed on the part of females and early death from starvation of most neonates that limits the numbers of carnivores, just as surely as it does for herbivores.
In summary, first it is plants that are struggling to gain access to enough of the scarce available nitrogen in this world to support their reproduction and growth. In turn, the animals that eat plants are similarly striving to get enough of it. Finally the carnivores which eat the herbivores are struggling to gain access to enough animal protein to support their breeding and the raising of their young. So both herbivores and their predators are struggling to survive in an environment that is passively hostile and inadequate.
I said that herbivores have evolved a huge range of adaptations to improve their access to the limited amount of useable nitrogen in their food. To survive - as individuals and as species - they have had to evolve to cope with what was aptly referred to by a wise old scientist in an earlier generation as 'this universal nitrogen hunger'. However, before I discuss in more detail some of these examples, let's first have a look, in general terms, at what form these adaptations might take. I can identify six ways.
1 Herbivores could selectively feed on those parts of the plants which are richest in amino acids and synchronise their breeding and the raising of their young with times when the plants provide the greatest amount and concentration of these.
2 They might increase the concentration of this soluble nitrogen and prolong, in various ways, the time it is available in the plants.
3 They could eat more food more quickly, and extract, absorb and digest the available amino acids in that food more efficiently.
4 They could enlist the help of micro-organisms to break down components of their food which they cannot digest, and produce essential amino acids they are unable to synthesise themselves. Then they could devour their microbial 'helpers'.
5 They might supplement the limited amount of nitrogen in their food plants by eating other animals.
6 They could apportion and concentrate the limited amount of good food in their environment to a selected few individuals at the expense of the many.
Many of the tactics incorporated in these strategies have in fact been adopted by both vertebrate and invertebrate herbivores, young and old, male and female. Yet, in spite of all these adaptations, the chances are still very slim that any one individual will get enough good food to survive for long. Most young animals die either shortly after conception or birth. And this is why animals produce so many young. They must produce what appears to be a wasteful surplus of offspring to make sure that enough lucky ones find enough food to survive and replace them. Else their species would become extinct.
As an aside here, I should perhaps point out that the usual belief is the reverse of this statement. Most biology students are taught, and most educated people accept, that the remorseless struggle for existence in nature follows because organisms produce too many offspring. If they all survived, numbers would increase exponentially and the world would quickly be flooded with them. So the young must struggle against each other to survive - and most don't. But rather the reverse is true. No organism produces too many offspring. All produce so many young simply because each individual must struggle for existence. Surviving on this earth is, and always has been, especially for the very young, a struggle - a chancy business. The huge 'surplus' of young that all organisms produce is the universal illustration of this. The capacity to produce so many young did not evolve to provide a struggle for existence as a vehicle for evolution. It evolved because the only populations which persist on earth are those which produce sufficient offspring to ensure that at least enough of these gain access to sufficient food to survive and replace their parents.
And as we shall see at the end of the book, it is this universal great capacity to reproduce which permits sudden and huge explosions in numbers of animals when changed conditions in the habitat alleviate the usually chronic shortage of food so that many more young survive and grow to maturity.
Furthermore, those that die need not have been actively killed by a predator or out-competed by others of their own or another species. Most die because they fail to ever gain a foothold. For most animals the 'struggle for existence' is not a tooth and claw business. It is a lonely struggle to live in an inadequate world. They die young, and their passing is solitary, passive and unnoticed.
Those best adapted to the habitat of the moment - or just plain lucky to be at the right place at the right time - survive. Those that, for whatever reason, do not gain access to enough resources to survive, die - they are selected against. Natural selection is not a matter of'the survival of the fittest'. As a Dutch colleague of mine famously states, it is 'the non-survival of the non-fit'. This being so, many must be produced to ensure some survive.
In our modern Western societies this harsh reality of the death of most young is largely forgotten: we have virtually eliminated such deaths from our own population. But for our early ancestors - and even for those of only one hundred years ago - it was commonplace, as it still is today for many peoples of the developing world. In the natural world it is, and always has been, the universal rule.
The chapters that follow highlight some of the myriad ways within the six general strategies I listed, that herbivores have evolved to increase their access to enough nitrogen to enable them to produce sufficient viable young to persist on earth. These in turn constantly illustrate why, in spite of their best efforts, herbivores for most of the time just cannot eat enough plants to prevent the world from remaining green.
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