by Dave Goulson
The odd clonal nature of aphid colonies has led to the evolution of some remarkable behaviour. In 1977 the Japanese entomologist Shigeyuki Aoki discovered the existence of soldier aphids, a specialist caste of aphids that exist in some species and defend the colony against predators such as ladybirds. Since Aoki’s initial discovery, soldier castes have been discovered in forty or so species of aphid. Oddly, they seem to be particularly common in gall-forming aphids, species that stimulate their host plant to produce a protective, hollow ball of plant tissue, within which they live and feed in a central cavity (one might imagine that aphids living within a gall have less need of soldiers than those living in the open). These soldiers are larger than their genetically identical sisters, and have exaggerated, powerful forelegs and sharp horns on their heads. The soldiers generally don’t reproduce themselves, instead selflessly devoting their life to defending their sisters. They sit at the edge of the colony, and if a predator such as a lacewing attacks, they rush in to defend their siblings, attempting to grab the predator and impale it on their horns or stab it with their sharp mouthparts.
Even more remarkably, another Japanese scientist named Takema Fukatsu recently discovered that soldier aphids will also act as paramedics to their host plant. If a caterpillar chews a hole in the gall in which the aphid colonies live, a team of soldier aphids gather round the breach and eject their own gooey body fluids into the gap, mixing and kneading them with their legs until they dry and harden into a scab. The aphid’s juices seem to contain an unknown substance that stimulates the plant tissues to grow back neatly over the scar, something that doesn’t happen if no aphids are present. Usually many of the soldiers get stuck in their scab and die, their corpses entombed by the growing plant tissues, but Fukatsu found that their sacrifice was effective: aphid colonies in unrepaired galls were rapidly overrun with predators and wiped out, whereas the vast majority of colonies in repaired galls survived.
Such altruistic behaviour is extremely rare in nature. It has an obvious parallel in ants and bees, where workers are sterile and will often sacrifice their lives in defence of the nest. The reason that these two groups show such behaviour lies in the peculiar patterns of genetic relatedness that both show. In most species of animal (including humans) siblings share 50 per cent of their genes. In evolutionary terms, this means that we should care about our own survival and success twice as much as we care about that of our sisters and brothers. Given the choice between saving our own skin or saving a sibling, we should save ourselves every time. An informative, if rather silly scenario is to imagine what you would do if you were kidnapped, along with an assortment of your relatives, by terrorists. Suppose the terrorists offer you a choice: they will shoot you, or your sibling. Genetically speaking, you should sacrifice your sibling; after all, he or she only carries half of your genes. If the deal offered is a choice between your own life and that of two of your siblings, then in evolutionary terms it makes no difference which choice you make. But if you could save three siblings, then you should take the bullet; together your siblings have 50 per cent more of your genes than you do. Similarly, you should cheerfully sacrifice seven cousins rather than die yourself (cousins each having one-eighth of your genes), but you should willingly give your life to save nine of them.
Of course I’m not suggesting that humans, aphids or bees actually think about it in these terms; but we would expect natural selection to favour individuals with behaviours that approximate to these predictions. If you think that humans, with our capacity for thought and reasoning, have risen above such primitive urges, ask yourself this: who would you be most willing to risk your life for, a close relative or a distant one? Who will you leave money to when you die? Many wills divide up assets so that the bulk goes to the closest relatives, and smaller sums to more distant ones; they reflect patterns of genetic relatedness.
I am perhaps getting a little off the point; aphids and bees don’t make wills, and they do not generally get kidnapped. What they do have is unusually close relatedness between members of groups. In female ants and bees, sisters share 75 per cent of their genes, which makes cooperation and self-sacrifice between them more likely to be worthwhile. Female aphids within a colony share 100 per cent of their genes – they are all identical, which makes it easy to understand why they might risk their lives to defend their sisters. If a soldier aphid can save the life of just one sibling by sacrificing itself, it has broken even. If it can save the whole colony, then in evolutionary terms it has made a very wise move indeed.
Most aphids don’t have a soldier caste, but instead enlist the help of other animals in defence of their colony. The blackfly colonies on the vetchling and thistles at Chez Nauche are assiduously guarded by ants. The ant workers patrol among the aphids almost as a farmer might watch over a herd of cows; if a hungry ladybird attempts to snaffle an aphid or two for lunch, the ants angrily attack, simultaneously emitting an alarm pheromone that calls more of their sisters to their aid. They will chase and bite the ladybird until it gives up and flies off to try its luck elsewhere. The cow analogy is particularly apt, since the ants are not caring for the aphids out of the kindness of their heart; they milk them for sugary honeydew. This is a good deal for the aphids, as they have more sugar than they need. Plant sap is rich in sugar, but generally quite low in protein, so aphids have to drink a lot to obtain enough protein. This gives them a surplus of sugar, which in the absence of ants they simply excrete; if you have ever parked your car under an aphid-infested tree you will be all too familiar with the sticky spots of honeydew that rain down from the aphids above. Ant–aphid mutualisms of this sort are found all over the world, and some have become more complex. In some species the ants will pick up and move the aphids to another plant if the one they are on starts to die. Other ants take the eggs that many aphids lay in autumn into their nest for the winter, keeping them warm and safe (like cows in a barn) until the spring, when they carry the newly hatched nymphs back out and place them on a suitable plant. At Chez Nauche, yellow meadow ants keep several species of aphids permanently underground in their nests, where the aphids feed on the roots of plants and are milked by the ants.
Of course the care shown by the ants to their aphid charges is entirely selfish. When aphids switch to their winged phase, ants have been seen to rip their wings off to prevent them flying away, just as a farmer might clip the wings of his poultry. When food is scarce in winter the yellow meadow ants consume their aphids, but generally keep enough safe that they can build up their stocks again in spring.
If aphids use sugary sap to buy the aid of ant guards, other true bugs use their plentiful supply of sap to defend themselves in quite a different way. In spring one of the hazards of walking though the long grass in my meadow is that your legs are likely to become liberally splattered with cuckoo spit. Cuckoo spit is not, of course, the spit of a cuckoo, and the origins of this peculiar name are lost in time, although it does appear at about the same time that migratory cuckoos arrive from Africa. In fact it is the frothy secretion of young froghoppers – rather cute, chubby little bugs, which as adults live up to their name by performing astonishing leaps when disturbed.2 As youngsters they are much more sedentary, and spend their time hidden within the centre of their own personal bubble bath, which they excrete from their rear end and whip up as necessary with their hindlegs. The glutinous mass provides excellent protection from almost all predators, including birds, which could easily find the conspicuous white blobs in the meadow, but seem to be unwilling to get their beaks covered in the slimy, bitter-tasting froth in order to pick out the tasty nymphs inside.
True bugs are just one relatively small group of generally inconspicuous insects. Keen gardeners will notice aphids from time to time, and if you are unlucky enough to get a bedbug infestation it will be hard to overlook their presence for long, but otherwise it would be easy to live your whole life in ignorance of these creatures. Some may have seemingly grotesque and unpleasant habits, while others will selfless
ly give their lives to save their sisters. Their headless corpses have played a role in helping us to understand how insect hormones work; and one hungry bug may even have killed Darwin. Yet most true bugs are unstudied and unknown, apart perhaps from a pinned specimen in a museum. We have barely scratched the surface of this topic. What even more fascinating natural history has yet to be discovered among these remarkable insects?
PART II
The Rich Tapestry of Life
The lives of the myriad creatures of the meadow are, as we have seen, fascinatingly varied, sometimes unexpected and often unknown. However, the greater mystery is how they all fit together. No creature lives in isolation – all are interlinked one way or another in a dynamic web of interactions that we are only just beginning to explore. The bedrock of meadow life is the plants, which capture energy from the sun and transform it into food that ultimately supports more or less everything else. The plants themselves compete for space, light, water, nutrients and pollinators, have mutualistic relationships with bacteria and fungi, and are attacked by diseases, parasites and herbivores. What determines how many species there are? What happens if species are lost, or new ones invade? Why are some animals and plants rare, while others are common? How many species are necessary to maintain healthy soils, and to ensure adequate pollination? More often than not we do not have answers to these questions.
Here I will explore some of the ways in which the creatures and flowers of the meadow interact with one another, focusing particularly on pollination, a process that underlies much of the diversity of both plant and insect life on Earth. Pollination might seem to be a simple, harmonious activity – bees buzzing from flower to flower, drinking nectar and carrying pollen – but look closely and a web of deception, competition and robbery is revealed. It is these interactions between species that form the rich tapestry of life.
CHAPTER TEN
Hothouse Flowers
15 September 2011. Run: 38 mins 50 secs. People: 4 – hunters with shotguns under their arms and slaughter on their minds. Dogs: 5 – I armed myself with a stick before passing the spaniel’s house, which seemed to deter attack. Butterfly species: 9, all rather tired, as summer comes to an end. I glimpsed a hoopoe in the hamlet of Le Breuil, using its long, downcurved beak to probe for insects in a cowpat on the road through. They are common enough, but I can never fail to get excited by this splendid clown of a bird with bright-orange, black and white markings and a foolish crest of feathers. It headed off in characteristic swooping, woodpecker-like flight when it saw me.
There is endless and wonderful variety in the structure of flowers, and I would encourage anyone who has never taken the time to look at them carefully to do so. Although we spend much energy in growing pretty flowers in our gardens, and expend considerable sums on buying cut flowers for our loved ones, the pleasing forms of flowers are not for our benefit. Their complex shapes and fabulous colours are the culmination of 130 million years or so of co-evolution between pollinators and plants. Each flower is both an advert and a trading platform. The purpose of flowers is to attract pollinators – generally insects – and then to persuade them to carry pollen grains to another flower of the same species, but on a different plant, in exchange for rewards. This is no simple matter, for there are many other flowers of the same and different species, all competing for the attention of pollinators. There are also many different types of pollinator. At Chez Nauche there are a dozen or more species of bumblebee, honeybees, probably in excess of fifty species of solitary bee (I am still trying to identify many of them), numerous butterflies, moths, beetles, hoverflies, and so on. In more exotic climes pollinators may also include bats, lizards, various birds such as parrots and hummingbirds, even mammals.1 Each pollinator has a different shape, size and tongue length, and some are only active at certain times of the day or night, or at particular times of the year. For example, some solitary bees are only on the wing for a few weeks; the hairy-footed flower bee, Anthophora plumipes, appears in March or April and is gone by May.
From a pollinator’s perspective, there may be a plethora of flowers in a meadow. How does it choose which ones to visit, and in what order? Does it go for the commonest, tallest, largest, prettiest or most fragrant ones? It also has somehow to take into account what all the other pollinators might be doing, for if they all make the same choice, then they will all end up fighting over the same flowers, which would not be productive for any of them. For bees it is particularly important to maximise the amount of food they gather, for this directly determines the number of offspring they can rear. From the plant’s perspective, which insects should it try to attract? Each varies in its abundance, size, speed and effectiveness as a pollinator. Should it expend lots of resources on big, brightly coloured petals to advertise its presence, but then have few resources left to provide rewards for its pollinators, or will insects see through such unfounded marketing hype? It may be better to pour resources into providing rich rewards and spend little on advertising, relying on discerning, intelligent insects to discover its worth. There is no one answer, and the meadow at Chez Nauche is packed with different flowers, each of which has adopted a slightly different approach. A meadow filled with flowers and busy insects is a complex web of interactions, which shifts through the seasons as different flowers come into bloom and different suites of insect pollinators come and go.
Some insects choose a generalist strategy, flitting readily between different types of flowers. Others specialise, and have often evolved particular structures to help them deal with particular types of plants; in particular, some bees have evolved long tongues to help them gather the nectar in deep flowers that many other insects cannot reach. This approach limits their flower choices, for long tongues are unwieldy for feeding on shallow flowers, but it also cuts down the competition to only those other insects with long tongues. Correspondingly, some flowers are generalists, aiming to attract any old pollinator they can – the hogweed growing along hedge banks and the wild carrot that flourishes in the open meadow are good examples. They do not hide their rewards, but display them within easy reach on a broad, flat platform of tiny white flowers, each a shallow dish of nectar with pollen on offer on short stamens above. The rewards can easily be gathered without any special apparatus; such flowers tend to attract a broad variety of flies, beetles and short-tongued bees. The advantage of this approach is that the flowers are likely to get lots of insect visits, but there is a downside: their visitors will themselves tend to be generalists, and so they are likely to flit off to a different flower species for their next drink of nectar. Pollen transfer between different plant species is of no use to either the donor or the recipient. In fact the female part, the stigma, can become clogged up with pollen if too much arrives from a different flower species, leaving no room for the correct pollen, should it subsequently be delivered.
Much of the strategy adopted by a particular flower species can be discerned by close examination of its structure. Almost all flowers are constructed of essentially the same parts, though they may differ wildly in shape, size and colour between species. The most obvious parts are usually the brightly coloured petals, designed to attract pollinators from far and wide. Flowers that are aiming to attract bees are often yellow or purple, since these are the colours to which a bee’s eyes are most sensitive. The petals of bee-pollinated flowers often have nectar guides in ultraviolet, invisible to us without special equipment, but obvious to bees, which lead them to the rewards. In some bee-pollinated flowers, such as clovers, foxgloves and dead-nettles, the petals form a deep tube with the nectar at the bottom, so that only long-tongued bees can reach it. Often these flowers have bilateral symmetry (rather than the radial symmetry found in the majority of flowers), a design that seems to be inherently appealing to bees.
Many flowers target bees because they are the most assiduous and hard-working of pollinators, driven by the need to feed their young, but some plants aim to attract other insects. Butterfly-pollinated flowers t
end to be pink or red, although there are few of these in Europe. Moth-pollinated flowers, such as white campions, tend to be white so that they can be seen more easily in the dark, and they typically have a strong scent; honeysuckle is another example, which clambers up the small elms and blackthorns along the drive at Chez Nauche, and is a favourite for growing up garden trellises because of its evening fragrance. Fly-pollinated flowers are often bowl- or plate-like – think of the yellow dish of buttercups, or the white platform provided by meadowsweet and elder flowers. In these, the nectar is readily available to sip, even for insects with short tongues. Some fascinating fly-pollinated plants stink of rotting meat to attract carrion flies, though fortunately there are no such plants in my meadow.2
Although the petals are often the most obvious part of a flower, the design of the rest of the structure is equally important to its success. Inside the petals – or sometimes protruding from them, where they will contact approaching pollinators – are the male and female parts. Often the sexual parts are hidden so that only pollinators of the correct shape and size can find them. Meadow clary, a wild relative of garden salvias, has anthers hidden amongst the upper petals in its purple flower, and a nifty mechanism whereby the action of a bee probing the nectaries activates a lever, causing the anthers to swing down and place pollen precisely on the thorax of the insect, just behind its head. There was no meadow clary in my meadow until recently, for it has heavy seeds and so takes a very long time to recolonise suitable areas, but I collected some seeds locally and sprinkled them into the grass, and I now have a handful of these lovely plants coming through. I can never resist plucking a slender grass stem and gently inserting it into the mouth of the flower, mimicking the action of a bee and causing the anthers to swing gracefully down.
