A Buzz in the Meadow (7 page)

Dragonflies are amazing but primitive insects, and I was thrilled to see them occupy the new pond at Chez Nauche. They have not changed much since the Carboniferous, 320 million years ago, when they were the largest animals in the air. Back then, some species were well over sixty centimetres across, the top aerial predators of their day, and they remained kings of the sky for 100 million years until displaced by the pterosaurs. Dragonflies snatch their prey in mid-air, scooping them up with their forward-curved, spiny legs, which form a basket beneath them as they fly. When hunting they can accelerate to well in excess of fifty kilometres per hour, much faster than most of their hapless prey, which includes flies, bees, wasps, butterflies, damselflies and even other dragonflies. Dragonflies have the largest eyes in the insect world, with up to 30,000 facets, and wrapping entirely around their head so that they can see in all directions at once. Close up, their eyes have a multicoloured iridescence, a little reminiscent of the colours on a compact disc, but with a three-dimensional, almost holographic, effect.

There are many fascinating aspects to the biology of dragonflies. They lay their eggs in fresh water, and their nymphs are themselves voracious predators. They are squat and brown, ugly ducklings that show no signs of the beauty that is to come in adulthood. They feed with a mechanism similar to the gruesome alien in the film of the same name; they are ambush predators, waiting motionless until a small fish or tadpole swims near. Then, in the blink of an eye, their telescopic jaws unfold forward from their face and their prey is punctured by their sharp mandibles and drawn back to be consumed. When fully grown, the nymph climbs out of the water, generally using a reed stem, and the adult bursts out from within, leaving behind a papery brown husk.

The adults are quite long-lived by insect standards, some spending several months on the wing, searching for a mate and laying eggs. Their courtship and mating are peculiar even by the standards of the wonderful world of insect sex. The male dragonfly has a pair of claspers at the tip of his long, thin body, which perfectly fit the base of the neck of the female of his species, but will fit no other. Male dragonflies spend much of their time searching for a female, or guarding a resource – a pond – that they know females need to visit to lay their eggs. If they see a female they will attempt to grab her by the neck, either in mid-air or by waiting until she has perched to lay an egg. They will happily grab newly emerging females who are not yet able to fly, or will attack mating couples, attempting to tear them apart and grab the female for themselves. The females usually try to avoid male attentions, and will take evasive action if they have the chance.

Once a male has captured a female, he will not readily let her go. In many species the male's claspers are armed with spines, which actually stab into the head of the female, making it extremely hard for her to escape or for another male to separate them. Couples may stay locked together for days, flying around in tandem, with the male in front, the female being towed behind by the scruff of the neck. It may sound undignified, but they look rather beautiful together.

Before they can actually mate, there are various logistical problems that they must overcome, and that require the cooperation of both parties. First, the male's testes are positioned near the tip of his body, which is now behind the female's head. Unusually, his penis is tucked up near the front of his abdomen, just behind the wings. If he has any sense, he will have carefully transferred a packet of sperm from the testes to the base of the penis by bending his abdomen double before he grasped hold of the female. If he did not, he is wasting his time. For them to mate, the female has to curve her own abdomen forward and underneath her head, so that her genitalia at the tip come into contact with the male's penis. At this point the couple's bodies form a rough circle or, more precisely, a rather romantic, lopsided heart shape, sometimes known as a mating wheel. Once her reproductive parts are in place, the male uses his penis to scrape out the receptacle in which the female stores sperm, in an attempt to remove all the sperm from any previous suitor. To this end, male dragonflies have penises that, in different species, variously resemble ice-cream scoops or scrubbing brushes. Once this sticky job is complete, the male transfers his own parcel of sperm. Having done so, he hangs on to the female for as long as he can. If he lets go, she is sure to be grabbed by another male and his sperm will then be unceremoniously removed, so if he wishes to have offspring he must hang on until she uses his sperm to fertilise her eggs. So it happens that, for much of the summer, most adult dragonflies are in pairs. They will hunt, sleep and she will lay eggs while locked together. Once she has laid eggs, he can be fairly sure that he has fathered at least some of the offspring.

You may wonder why the female would be willing to mate after being grabbed by a male without courtship, and after trying to evade him and reject his advances. The answer is presumably that she has to mate with someone. Having done her best to escape, she has established that this particular male must be fairly fast and strong, and so hopefully her sons will inherit his vigour.

There is something of a puzzle as to why dragonflies have evolved such a bizarre and complex way of mating. The explanation may be that it came about as a means of avoiding being eaten by their intended mate. In most mammals, males tend to be bigger and stronger than females; they need to be able to fight for access to females. Hence male red deer, the stags, are much more powerful and have much larger antlers than the females. In contrast, in insects it is generally the females that are larger; the bigger the female, the more eggs she can produce, whereas in males high mobility (to find mates) is usually more important than size. Hence natural selection has favoured voluptuous females and skinny, nippy males.
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As a result, sex in many predatory insects and also spiders is fraught with danger for the male of the species, for the females are often the larger and more powerful sex. Male dragonflies have largely overcome this problem by swooping on the object of their desire from above and behind; once he has firmly grasped her by the neck, he is safe from her powerful legs and jaws.

Male mantises have not yet come up with an entirely adequate solution to this problem. It may be that mantises evolved relatively more recently, about 100 million years ago, and so have had less time to come up with an answer than the dragonflies. The female mantis is considerably bigger and stronger than the male, so she is readily able to overpower and eat him, should she prefer a snack to sex. For the amorous male, gauging the mood of his potential mate as accurately as possible could not be more important; it is a matter of life or death.

It has long been known that female mantises commonly eat their mate during the act of copulation – the famous French entomologist Jean-Henri Fabre described this in the 1800s. Some have argued that it is an essential part of mating. Indeed, once the male's head has been removed – this is usually the first body part that the female consumes – his mating seems to become more enthusiastic, his body pumping vigorously. Of course his body might as well give it everything at this point, as it isn't going anywhere afterwards. Indeed, the male often doesn't get as far as copulating before he loses his head. Bizarrely, the male can still successfully initiate copulation
after
his head had been removed. In a series of odd experiments carried out by K.D. Roeder of Tufts University, Massachusetts, in the 1930s he demonstrated that successful mating can in fact take place when neither partner has a head, though perhaps this is of little relevance to what happens in nature.

It has been suggested that it may be in the male's interests to be consumed during copulation, for he is providing a large meal to his partner that may enable her to produce more of his offspring. However, this is only likely to be so if his chances of finding another female and mating again are slim; otherwise he is giving up all chance of mating again for the benefit of providing one meal to his current partner. Males of most animals are not so self-sacrificing.
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Some years ago I had the chance to study this for myself. I had gone on a cheap package holiday with my wife to Gambia, a country with an immense diversity of wildlife. The area around our hotel was almost dripping with mantises of various species, and their large egg masses, known as oothecae, were stuck all over various ornamental shrubs and could even be found on the walls of the hotel. I'd always been intrigued by the mating habits of mantises, and this seemed like an ideal opportunity to get hold of enough to do some experiments. I brought some oothecae back with me, and in the dingy basement of the biology building at the University of Southampton I set about rearing them.

Many of the oothecae produced only tiny parasitic wasps, the females armed with enormous ovipositors far longer than their bodies. These they clearly use to stab into fresh oothecae, laying their eggs deep inside, where they hatch and consume the eggs of the mantis. I pickled them in alcohol, and to this day have not got round to checking whether they belong to a species known to science. Fortunately some oothecae had escaped the depredations of the wasps, and dozens of tiny mantis nymphs emerged from these. Rearing mantises is problematic, as they are enthusiastic cannibals from day one. If they are housed together, a group of a dozen small mantises quickly becomes one bigger mantis, so they each have to be housed and fed individually, on fruit flies to start with, moving on to house flies and then small crickets. Luckily one of our technical staff, a shambling bear of a man called Keith, absolutely loved mantises and gave me heaps of help. Eventually, after an awful lot of work, we had several hundred splendid adult mantises, each about ten centimetres long. We kept them for another week or so to make sure they were mature, and then I began my experiments.

I wanted to watch exactly what happened during courtship, and to see whether cannibalism only occurred when the female was hungry. I also wanted to see whether cannibalism was reduced when mating took place in a spacious environment with lots of twigs and cover for the male, rather than in a bare cage. I spent many happy hours watching my mantises, aided by a succession of undergraduate project students.

Typically, and understandably, the male mantises tended to approach the females extremely slowly. Mantises can move almost imperceptibly by swaying gently, as if they are a frond of vegetation being wafted by the breeze. The impression is helped by their camouflage; most species are green or brown, so that they blend in well with the vegetation in which they live. A few tropical species are spectacularly beautiful, being pink or white to match the exotic orchids on which they wait to catch prey. The French species found in my meadow is a vivid, glossy green, the colour of wet summer grass; my Gambian mantises were a twiggy brown. With each tiny sway the mantis moves slightly more forward than back, and so edges towards its target: often prey, sometimes a mate.

When courting, the males proved to have two distinct strategies. Some attempted a front-on approach, edging more and more slowly towards the female, the closer they got. When they were just out of reach of her powerful forelegs, they started to display. The exact display varies from species to species; mine engaged in something akin to belly-dancing, with the male gyrating his abdomen, curling it forwards and backwards, wiggling it from side to side, and sometimes managing both at once. The female watched, inscrutable. Or at least so it seemed to me, but presumably the males were watching her to see if she was impressed. What kind of mood was she in? Did she look amorous, or peckish? If he felt the moment was right, he would pause, crouch and in a single bound would leap on to her back, pivoting in mid-air as he did so, like a vaulter at the Olympics.

Other males approached the females from behind. In this case a male would typically approach slowly at first, but – in marked contrast to males approaching from the front – he would accelerate as he got closer, sprinting the last few centimetres and then hurling himself on to the female. So far as I could tell, these females had no idea he was there until rudely mounted from behind.

Once on the female's back via either strategy, a male is not within easy reach of the female's forelegs, but he is not safe. She invariably struggles when he first lands on her, presumably weighing up her options. If he is lucky, she may decide to accept his attentions. If not and she continues to struggle, it is only a matter of moments before her superior strength prevails and he becomes dinner. This might occur if the female decides that the male is of inferior quality – an extreme form of rejection – or it might be just because he caught her at a bad time. Sometimes she lets him mate, but then decides that she needs a snack halfway through and that is when, typically, she bites off his head.

The results of our studies were pretty clear. At no point could we discern any sign that the male was a willing victim of cannibalism. Their approaches to females were cautious, and after mating they would either leap off and run for it or edge discreetly off her back, keeping well away from her front end. When confined with a female in a simple, undecorated cage, the males were much more likely to be consumed, usually without mating, than when there were plentiful twigs and leaves. When confined with a hungry female, their chances were not great. But when the female was well fed and they were confined together in a twig-filled cage, rates of cannibalism were very low, with males surviving more than 90 per cent of matings. I have since repeated this with French mantises from my meadow, and these Gallic lovers show no more signs of wishing to be eaten by their partners than did their Gambian counterparts. None of this tells us for sure how common sexual cannibalism is in nature, but it suggests that it may be nowhere near as common as once supposed.

Sex in insects is fraught with conflict. A meadow in summer is a seething mass of sexual adverts, courting couples, brutal rejections, conquests and copulation, a mad rush to reproduce and ensure there are offspring to carry on the line when the season ends. The song of the birds and crickets, the flash of a butterfly's wing, the swarming of dance flies on a summer's eve – all are driven by the evolutionary imperative of reproduction. However, as we shall see in chapter twelve, sexual intrigue is not confined just to animals.