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Authors: Dave Goulson

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I later looked through my undergrad notes to remind myself of the lectures I had received on Wigglesworth's experiments. Sir Vincent Brian Wigglesworth, to give him his full title, was a great pioneer of studies of insect physiology and the hormonal control of moulting and growth; he is one of very few entomologists ever to receive a knighthood. Wigglesworth served in the army during the First World War, before studying natural sciences at Cambridge, where he eventually became a lecturer and professor. Quite early in his career he discovered several of the major hormones found in insects, including the juvenile hormone whose analogues are found in paper made from North American trees. His discoveries were underpinned by macabre experiments that he conducted on bedbugs and their relatives.

To demonstrate the presence of a hormone in the body fluids of insects that controls moulting, he decapitated bugs and joined their headless corpses with short lengths of glass ‘microcapillary' tube – the same type of fine tube that I commonly use to extract nectar from flowers. Once joined in this way, the pair of bugs are strongly reminiscent of a mating couple, except that instead of being tail to tail, they are joined neck to neck. The tubing connects their body fluids, so that any compounds within can flow or diffuse from one body to the other. Although the bugs might reasonably be described as dead at this point, for they have no head or central nervous system (brain), nonetheless they continue to function for many days. As you might imagine, they don't do a great deal – without a head, neither body will decide to go for a walk, and they obviously can't feed. However, their tissues are still alive, they continue to respire and their bodies can moult, shedding their skin and thereby producing the cast skins that I had discovered in Mark's room. Wigglesworth found not only that a decapitated bug could moult, but that if he decapitated a bug that was close to moulting and joined it up with a slightly smaller bug that was nowhere near moulting, then both would moult together. Something was being transferred from the larger to the smaller body, causing it to moult prematurely.

Wigglesworth focused particularly on bedbugs and their relatives, the kissing bugs, and tried joining the different species together. He found that the hormone that controlled moulting was common to both, so that conjoined corpses of the different species also moulted in synchrony. Similar hormones are now known to be found in all insects, although it was many more years before their chemical structures were elucidated.

One of the few positive things to be said for bedbugs is that they do not spread disease. Many biting insects do; most famously, mosquitoes spread malaria and a host of other life-threatening diseases, such as dengue fever and yellow fever. Aphids offer a similar service for plant viruses – between the many types of aphid they spread at least 150 different viruses, many of them very harmful to crops, including such colourfully named diseases as beet mosaic, cherry ringspot, onion yellow dwarf and tomato-spotted wilt. One of the relatively few examples of a true bug that spreads human disease is the kissing bug of South America, the insect that Wigglesworth had imported to conduct his experiments. These large brown insects, about two and a half centimetres long, live in crevices is rural houses and huts. Like bedbugs, they sneak out at night to feed on sleeping humans, where they prefer to feed on the soft, delicate skin of the lips, which is easiest to penetrate. It is from this sinister habit that they get their name. While feeding they often defecate, and inevitably some of their faeces fall into the mouth of their unfortunate sleeping host. Even when the kissing bugs do not feed on the lips, they can infect their unfortunate host, for their bite-marks cause itchy lumps, and the scratching they elicit can lead to the insect's faeces penetrating the wound. The faeces contain virulent spores of
Trypanosoma cruzi
, a single-celled protozoan related to the parasite that causes sleeping sickness in Africa. The South American parasite causes Chagas' disease, an unpleasant chronic illness that is thought currently to infect about eleven million people in Central and South America. Many people suffer no symptoms, but about one-third develop inflammation of the heart and sometimes also the gut, with the heart damage eventually causing death. It seems that Charles Darwin was the unlucky recipient of a kiss from one of these bugs when visiting South America on a stop-off from
The Beagle
's voyage. In his diaries he describes being bitten while exploring near Mendoza in Argentina:

At night I experienced an attack, & it deserves no less a name, of the Benchuca, the great black bug of the Pampas. It is most disgusting to feel soft wingless insects, about an inch long, crawling over ones body; before sucking they are quite thin, but afterwards round & bloated with blood, & in this state they are easily squashed.

For much of his later life he suffered from a range of symptoms that were never diagnosed, but which approximate to those caused by Chagas' disease – the disease was discovered by Carlos Chagas some thirty years after Darwin's death. Some have suggested that Darwin was simply a chronic hypochondriac, the condition perhaps brought on by worry at the prospect of publishing his theory of evolution by natural selection, but it may be that the poor chap was genuinely suffering from a life-threatening illness.
1
There have been moves to test Darwin's remains for DNA fragments of the parasite, but the authorities of Westminster Abbey, where he lies entombed, have so far refused permission.

If bedbugs and kissing bugs sound as if they are best given a wide berth, their cousins the African bat bugs are arguably more gruesome still. These creatures closely resemble bedbugs, but inhabit caves in East Africa, where they feast upon the blood of bats, being active in the daytime when the bats are asleep. In a wonderful irony, they have South American cousins that suck the blood of vampire bats. The mating habits of the African bat bug are perhaps amongst the most barbaric yet discovered in the animal kingdom, and should perhaps cause human females to reflect that, no matter how clumsy their lover, matters could be much worse. The penis of the African bat bug is not dissimilar to its mouthparts – a sharp, pointed tube. Instead of inserting this into the genital opening of the female in the conventional manner, the male bat bug simply grabs the female and stabs his penis through her body wall, injecting his sperm directly into her body cavity, from where it swims to fertilise her eggs. Females are forced to mate many times in their lives, and so can accumulate considerable tissue damage from the multiple stabbings. To make matters worse the male's penis is far from clean – personal hygiene not being a high priority in the bat bug – and so it introduces bacteria into her body, which can lead to infection and death.

In an attempt to combat this, female bat bugs have evolved a fake ‘genital opening', a funnel on their back that tries to guide the sharp penis of the male into a cluster of immune cells, which mop up the bacteria. Females still sometimes get stabbed elsewhere, but the damage is reduced.

This sordid story has a further twist. As in many animals, the males are not terribly discriminating in their courtship. They frequently grab and stab other males, causing them considerable damage in the process. As a result, some males have also evolved a fake genital opening to try and minimise the damage, but this in turn makes them look a little more like females and so increases the frequency with which other males try to mate with them. It seems there is no escape for either male or female bat bugs from the damaging sexual depredations of the males of the species.

In marked contrast to the degenerate bat bugs, some true bugs eschew sex altogether for much of the year. Some of the flowers in the meadow – notably including white campions, creeping thistles and meadow vetchling – are commonly attacked by blackfly, sap-sucking aphids. In chapter twelve we will look at why most animals have both males and females and reproduce sexually. Aphids are one of the interesting exceptions, at least during the summer months. The clusters of blackfly on thistles are predominantly wingless females. They plug themselves into the phloem, the network of tubes that transports sugar-rich sap around the plant, and then rarely move again unless they are attacked or the plant dies. They squirt out youngsters at a prodigious pace (up to twelve per day) and these are genetically identical copies of themselves – a process known as parthenogenesis. If sheep could do this, it would have saved scientists the enormous effort and expense that went into producing Dolly (the first artificially cloned mammal). The offspring walk a few millimetres from their mum, plug themselves in and repeat the process. In some aphid species, offspring have their own young already developing inside them as they are born, recalling Russian nesting dolls that are packed one inside the other. Hence one aphid quickly becomes thousands, all identical females descended from a single individual. They sacrifice the advantages associated with sexual reproduction – the mixing of genes – for extremely rapid reproduction.

Only when summer ends and they find themselves under heavy attack from predators, or the plant starts to weaken under the load of aphids, do they change strategy. When this happens, they start to produce both males and females; and what is more, these offspring have wings. They fly away, mate (and so jumble up their genes once more) and start fresh colonies. In autumn they tend to set up their new colonies on woody plants in the hedgerows, where they can survive the winter in relative safety.

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.

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