Herbivores have never really enjoyed the popular appeal of their carnivorous cousins. The placid ewe on its pasture and the caterpillar on its leaf inflame fewer hearts than the hunting cheetah or rapacious dragonfly. The herbivorous habit seems dull and undemanding, little more than the conversion of an abundant, immobile food store into animal flesh. The reality is more complex. Recent research portrays herbivory as a subtle trade, but a trade that has left an indelible mark on our surroundings.
Herbivores need all the subtlety they can muster if they are to deal successfully with their diet. As a rule plants are not particularly nutritious, and what resources they do have are extremely well defended. When we take a summer stroll down a country lane, we are entering an evolutionary battlefield in which plants and those who would eat them are locked in combat. According to Valerie Brown and John Lawton, two biologists from Imperial College at Silwood Park in Berkshire, that battle has left its mark on the greenery that surrounds us. They believe that the sizes and shapes of leaves have been influenced by past skirmishes with herbivores.
Botanists have traditionally ascribed the shape of leaves to a range of other influences. A leaf must be both biochemically efficient and able to withstand mechanical forces and other forms of disruption from the environment. Its design can make a huge difference to its physiology. Large leaves, for example, lose heat more slowly than small leaves and, as a result, they may be up to 10 °C warmer than the air around them on a sunny day. Researchers have uncovered a number of correlations between the shapes of leaves and factors such as climate, shade or latitude.
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Evolutionary pressures from herbivores must also have had an impact on the design of foliage, say Brown and Lawton. Plants cannot simply shrug off the loss of their leaves; in one of the researchers’ tests, defoliation of oak trees by caterpillars reduced by a half the number of acorns produced by the trees. Any ploy that reduces attacks from herbivores should be favoured by natural selection.
Brown and Lawton suggest several distinct routes by which herbivores could have influenced the size and shape of leaves. One of the most obvious to the human eye is mimicry: succulent leaves gain protection by mimicking inedible ones, in much the same way as a harmless hover fly dressed in the livery of a short-tempered wasp. Stinging nettles defend themselves with hairs whose forte is the injection of acid into the soft parts of herbivores. Dead-nettles are harmless members of a quite distinct family, but many people are deterred by their appearance and a similar wariness may prevent other mammals from eating them.
Certain vines from New Zealand go one stage further. With their narrow, brown and grey leaves, the young plants resemble dead twigs scattered on the forest floor. This ruse may have helped them avoid the depredations of sharp-sighted moas, the extinct flightless birds whose impact can still be discerned on the flora of New Zealand.
Mimicry may also take a more subtle form. Some researchers have claimed that the ragged leaves of certain plants may be designed to suggest that they have been attacked by herbivores such as caterpillars. One possible practitioner of this ploy is the Swiss cheese plant, that stalwart of living rooms and offices. A herbivore might be deterred from attacking such leaves for several reasons. It might interpret the apparent ‘damage’ as a sign that other herbivores – potential competitors – are already exploiting the leaves. Damaged leaves are also more likely to have switched on their chemical defences, making them a much less attractive target than a leaf in its pristine state.
The chemical defences of plants are highly elaborate, ranging from straightforward poisons such as cyanide to chemicals that mimic the hormones of their assailants and cause physiological mayhem when eaten. Mechanical defences are every bit as elaborate. Leaves may be equipped with hairs which can trap tiny feet or even impale an entire insect. The leaves of yellow wort, a member of the gentian family, surround the stem in such a way that the plant becomes well nigh unscalable by insect predators.
Divided but not conquered
From an insect’s viewpoint, large leaves may provide living space of a higher quality than the same area divided into small leaflets. Small leaves provide fewer calories per package and can only be exploited by insects capable of advanced acrobatics. In a study of British members of the umbellifer family, Lawton and his co-workers found that species with finely divided leaves entertained fewer types of insect herbivores than those with broader, undivided leaves. According to some surveys, trees with small leaves house fewer species of insect than their counterparts with larger leaves. Although more information is badly needed, it seems that a plant has much to gain by acquiring small, narrow or divided leaves, other things being equal.
Plants face immense pressure from insect herbivores. At least half a million species of insects worldwide are thought to feed on living plants and the final tally may be much higher. On the receiving end of their attentions is an annual harvest of plant tissue amounting to around 150 billion tonnes. The chief item on the menu is cellulose, a polymer of glucose, which has the distinction of being the most abundant organic molecule on earth.
Cellulose is at the heart of an age-old mystery about herbivory. Many microbes and fungi degrade cellulose with ease, but similar skills seem beyond most herbivorous insects. Of the few insects that use cellulose as food, the vast majority harness the services of fungi, bacteria, or protists to digest it for them, as do sheep, cattle, horses and a range of other vertebrates. Why have so few insects taken cellulose seriously? And why do they not produce their own cellulose-degrading enzymes? The traditional answer, which focuses on the difficulty of digesting cellulose, is now losing ground to a more radical alternative: cellulose may not be worth digesting.
Cellulose is a major constituent of the cell walls of plants. This means that all the nutritious ingredients of the plant cell – sugars, proteins and other essentials – are packaged in a tough, indigestible box. Most insects that feed on foliage ignore the box completely. Aphids and bugs are content to suck out the cells’ contents using a sharp proboscis, and chewing insects such as caterpillars and grasshoppers simply rip open the box without digesting it. The jaws of grasshoppers are as well equipped for grinding as the molars of a cow. Under the microscope, their tiny ridged mandibles have an uncanny resemblance to bovine teeth, despite a thousandfold difference of scale. These mandibles are powered by huge muscles that can occupy around half the volume of the head, according to Elizabeth Bernays of the University of Arizona. Bernays reports that the size of the head in grasshoppers and caterpillars reflects the toughness of the foliage on which they habitually feed. Tougher food needs larger muscles and hence bigger heads.
The majority of insect herbivores are happy, it seems, to crush plant cells or otherwise winkle out their contents. This observation is important. It suggests that, even when digested, cellulose may not have a great deal to offer an insect. Being made of glucose, cellulose can supply energy, but not nitrogen-containing substances such as the amino acids – the raw materials for proteins – that insects need for growth. Most herbivorous insects are held in check by shortages of nitrogen or water; they already have all the energy they need, according to Michael Martin a biologist at the University of Michigan. The ability to digest cellulose would be about as good for a caterpillar as a regular chocolate ration would be for a three-year-old child.
Yet although the digestion of cellulose may not be particularly profitable for most insects, some have made it their speciality. Nearly 80 such species have now been studied in detail, including several cockroaches, termites and wood-boring beetles. Digesting cellulose may not directly provide them with amino acids, but it does permit them to pursue some spectacular lifestyles – tunnelling through solid timber, say, or subsisting on splinters of wood.
These inventive insects divide into four categories based on their approach to cellulose. The cockroach Cryptocercus punctulatus and several species of termite employ the services of cellulose-digesting protozoa that live in their guts. Other termites and some beetles harbour gut bacteria with similar talents. The third technique involves procuring the necessary digestive enzymes from wood-rotting fungi. Martin and his colleagues Jerome Kukor and David Cowan have found that the grubs of several long-horned beetles, which burrow in rotting wood, consume fungal enzymes with their food. The enzymes continue to function inside the digestive tract, permitting the insects to digest a substantial amount of the cellulose in their unpromising diet.
Let them eat cellulose
A fourth method of digesting cellulose has been adopted by a few advanced termites and one species of cockroach. Although final proof is still lacking, these insects do appear to be capable of producing their own cellulases. Similar claims have also been lodged on behalf of a range of molluscs, including some land snails.
Why have so many insects employed the services of microbes in the war on cellulose instead of evolving their own cellulases? Martin’s answer turns the spotlight on the many other functions performed by microbes in insect guts, such as fixation of atmospheric nitrogen, or synthesis of essential amino acids, fatty acids and vitamins. Martin thinks that such associations could have been the starting point for the evolution of cellulose digestion. An omnivorous insect with an industrious gut flora could have been invaded by microbes capable of degrading cellulose. At first those microbes would have made little difference to the insect, which was no doubt amply supplied with carbohydrates before they appeared. Once they were installed, the insect would have been able to switch to a new lifestyle, fuelled by cellulose.
But to the majority of herbivores, cellulose is merely an unavoidable nuisance that lies between them and the worthwhile parts of a plant. Why have they not adopted the more radical alternative of abandoning herbivory, going green and making their own sugars by photosynthesis – in the time-honoured manner of plants? The question is not as nonsensical as it sounds. Plants themselves originated when primitive cells took to harbouring photosynthetic microbes. Lichens are symbiotic associations between a fungus and an alga, in which the alga provides nutrient to the fungus. Some animals make a similar trade: they harbour photosynthetic algae within their tissues and reap the rewards of their guests’ industry.
Making maltose
Among these ingenious creatures are many unicellular forms, such as amoebae and species of paramecium, as well as sponges, corals, sea anemones, and a select group of flatworms, sea squirts and molluscs – notably the giant clams, which cultivate photosynthetic dinoflagellates in their blood vessels. In many cases, especially among the lowlier animals, the algae actually live inside their host’s cells. For example, algae of a species of Chlorella live inside the cells of freshwater hydra, where they carry out photosynthesis and pump out sugar in the form of maltose. Each cell has around 20 Chlorella in residence.
Why is this felicitous arrangement so rare among animals? There are several reasons, according to David Smith of the University of Edinburgh. For one thing, the gains may not be as great as they first appear. Many animals obtain a rather unwholesome food supply from their internal symbionts. With Chlorella, whose only product is maltose, the effect has been likened to eating junk food. Symbiodinium, a marine dinoflagellate associated with corals and giant clams, produces a wider range of products, including glycerol, fatty acids and the amino acid alanine, but such a diet is by no means balanced. It is significant that very few animals with photosynthetic symbionts give up eating for themselves.
Any animal that harbours symbionts must evolve special mechanisms for controlling its guests and for persuading them to release the products of photosynthesis. It must encourage them to prosper but prevent them from reproducing too quickly, or it may be overwhelmed. According to research by Smith and Angela Douglas, some symbionts may grow 10 times faster once freed from the influence of their hosts. Another high cost arises from the need to expose symbionts to light. Loitering in the light and displaying a large area of green tissue is an invitation to predators.
Animals that play host to symbiotic algae must also invest in a mechanism for passing them on to their progeny. Working at the University of California, Irvine, Richard Campbell has pieced together the method by which green hydra ensure that their eggs start life with algae in residence. Hydra are made up of two layers of cells separated by a jelly-like layer called the mesolamella. Cells of the inner layer contain the algae, while the outer layer produces the growing egg. Before the algae can be engulfed by the egg, they must be released from their normal home and persuaded to cross the no-man’s-land of the mesolamella. Their journey is made possible by the degeneration of a layer of muscle that would normally stand in their path. When a young hydra is born, it already carries its green guests – but only as the result of a most complex piece of manipulation.
An even more extraordinary approach to symbiosis has been adopted by Elysia viridis and its relatives. Elysia is a marine slug-like mollusc, which lives around the coasts of Europe and feeds on the seaweed Codium fragile. Elysia is as well camouflaged on its food plant as it could be, because it gets its green complexion by hijacking the plant’s chloro-plasts – the organelles that carry out photosynthesis. In an audacious manoeuvre, Elysia cuts open the cells of its host plant, sucks out the chloroplasts and then stores them unharmed inside the cells of its digestive system, where they carry on working for at least a week and possibly much longer. Flaps at the sides of its body increase its surface area and make it an ideal absorber of light. One researcher’s reaction on seeing Elysia for the first time was: ‘Oh look, leaves that crawl!’
Elysia acquires at least a third of the sugar made by its symbiotic chloroplasts, and so gains substantially from its unusual behaviour. If kept in a dark aquarium, it loses weight. Yet the symbiosis is in some ways an imperfect affair. Elysia must continually replenish its stock of chloroplasts because they begin to run down as soon as they are removed from their normal surroundings. This reflects the fact that chloroplasts depend on the plant cell for many of the materials they need. However, research by Smith and others has demonstrated that the Codium’s chloro-plasts are relatively hard wearing. They resist mechanical and osmotic shocks, and run down at a more sedate pace than chloroplasts from a land plant such as spinach.
Why have land animals such as caterpillars and bugs not adopted Elysia’s strategy? Part of the answer may be that the chloroplasts of land plants are less well suited to such liaisons than are those of Codium, which are robust enough to survive being transferred from plant to animal and long-lived enough to be worth coopting. Elysia’s way of life may simply not be open to caterpillars and other land animals.
Aping trees
What is true of the caterpillar applies with even greater force to large, active, warm-blooded animals like ourselves, as biologists such as Peter Moore of King’s College, London, have pointed out. Imagine a green man, similar to the leafy figure of legend who appears in pub signs and church carvings. A rough calculation confirms that despite being green, he would still need three square meals a day.
An adult human exposes a surface area of about one square metre when sunbathing, enough to intercept about 150 kilojoules of solar energy in a day in Britain. If our green man were as efficient as the best plants, he could expect to harness a daily total of around 3.8 kilojoules, or about 0.5 per cent of his daily energy requirement of around 600 kilojoules. To improve on this miserable figure, he would need a huge surface area and a complex infrastructure for transporting gases and water to his voluminous, busy tissues. He would be obliged to spend all day lying in the sun – and all for a diet of sugar. He would doubtless come to look suspiciously like a tree. Herbivory may have its hardships, but photosynthesis is best left to the plants.
Stephen Young is a freelance science writer based in Wales. This article is based on a meeting held at the Royal Society ‘The evolutionary interaction of animals and plants’, held on 27 and 28 February 1991.
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In search of the earliest plant eaters
By about 400 million years ago, plant life had colonised the land and created an environment fit for terrestrial animals such as insects and other arthropods. By providing shelter and moist surroundings, the plants paved the way for the great radiations of the insect lineage. The insects repaid the plants by eating them. Researchers such as Bill Chaloner, Andrew Scott and Jonathan Stephenson at Royal Holloway and Bedford New College, University of London, are trying to reconstruct the earliest stages in the development of herbivory on land.
Some of the most informative fossils come from the Rhynie Chert site near Aberdeen. The fossils, which are about 400 million years old, include primitive plants with stems the size of a pencil, some of which have been damaged and then partly repaired as if by a wound reaction similar to that of modern plants. The damage could have been caused by some of the arthropods that lived at that period, but the identity of the perpetrators is unknown. Many of the earliest known land arthropods are predators, such as centipedes and arachnids, and the key herbivores still await discovery.
However, circumstantial evidence suggests that some of the arachnids already discovered may have been plant eaters. Chaloner points to a trigonotarbid arachnid, the largest arthropod fossil found so far at Rhynie Chert. The structure of its mouth, he says, is such that the spider would have been capable of biting plant tissue. Like all the Rhynie Chert spiders, it was found sheltering inside fossilised spore-bearing structures called sporangia. But this alone is not proof of herbivory. Some critics say that the fossil spiders make poor candidates for the earliest herbivores as modern spiders generally do not eat plants.
Better evidence has been gleaned from fossilised faeces, which contain plant spores, but it can be difficult to connect the faeces to their original owners. Some fossilised seeds show clear signs of holes where marauding herbivores could have gained entry.
By the Upper Carboniferous (about 300 million years ago) the fossil record includes leaves that appear to have been nibbled at the edges – perhaps by insects. The evidence becomes clearer with time. Fossilised plant tissues from the Cretaceous , about 100 million years ago, provide particularly compelling testimony. Chewed leaves, with bite marks at the centre as well as the margin, confirm that the insect herbivores were going from strength to strength.