IT STARTED with a ping. Martha Weiss鈥檚 lab was quiet. She was alone, except for her caterpillars. Then she distinctly heard a ping.
Weiss, a biologist at Georgetown University in Washington DC, was studying the larvae of the silver-spotted skipper, Epargyreus clarus, a butterfly common in the US. The yellowy-green caterpillars have black heads with big orange eyespots to warn off would-be predators. As the caterpillars grow they make themselves a series of increasingly spacious shelters by clipping and folding or rolling a piece of leaf and stitching the flap in place with silk. They spend most of their time inside, emerging briefly each day to feed.
Weiss kept her caterpillars in plastic shoeboxes for easy observation. 鈥淎nd in the evenings, every now and then I heard a ping,鈥� she says. It wasn鈥檛 hard to trace the source: it was the sound of a small, soft pellet striking plastic. 鈥淭he caterpillars were sticking their rear ends out of the back door of their shelters and firing,鈥� says Weiss. The pellets blasted out like little black bullets. If Weiss took the lid off the box, the pellets would fly over the rim and out of sight.
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Weiss was intrigued. Was this normal behaviour or were just a few caterpillars super poopers? To find out she lined up larvae on sheets of white paper and waited. 鈥淭he faecal pellets don鈥檛 bounce or roll, so there鈥檚 no dispute about how far they can shoot,鈥� says Weiss. The average range achieved by the flying faeces was 19 times the length of the larva鈥檚 body. The best shot, by a 4-centimetre long caterpillar, was 153 centimetres 鈥� 38 times its body length. The human equivalent would be 76 metres, or about 12 houses farther down the street. Pellets travel at speeds of 1.3 metres a second or more. 鈥淥ne moment you see a pellet hovering on the caterpillar鈥檚 anus, then it鈥檚 gone. It goes so fast, you don鈥檛 see it shoot away,鈥� says Weiss.
There was no doubt about it. Silver-spotted skipper caterpillars are frass-flingers. They fire their faeces 鈥� or frass, as entomologists call it 鈥� amazing distances. But why, Weiss wondered, do they eject it so far and so fast? The puzzle has converted Weiss from ecologist to faecologist 鈥� a field that she says is ripe for study. 鈥淭here are thousands of studies on the intake end 鈥� foraging and predation and so on 鈥� but very little about the other end,鈥� she says. 鈥淧eople tend to find it a little unsavoury.鈥�
Yet, as Weiss points out, the way an animal defecates can have important consequences for its survival. Natural selection has played a part in shaping defecation behaviour just as it has foraging behaviour. The nestlings of some birds, for instance, produce neatly packaged sacs of faeces which their parents can pick up and remove from the nest, perhaps to keep the nest clean and healthy or to avoid attracting the attention of predators. Some beetles take the opposite approach, deterring their enemies by carrying their toxic waste around on their backs.
In many lepidoptera, natural selection has led to the development of an extraordinarily explosive waste-disposal system. Weiss discovered that the phenomenon occurs in 17 unrelated families of moths and butterflies. Within each family, species that live in shelters tend to be flingers while free-roving caterpillars and stem borers are not. The phenomenon has evolved independently several times, which suggests that it is evolution鈥檚 answer to a problem all these animals share 鈥� a stay-at-home lifestyle.
Staying in one place has a number of drawbacks. But which of them was the driving force that led to projectile poo? Weiss decided to test out the possibilities on her silver-spotted skippers. First she looked at simple hygiene. The warm, moist interior of a leaf shelter filled with faeces would make a fine breeding ground for pathogens that could be lethal to a growing caterpillar. But when Weiss compared caterpillars that had their boxes cleaned daily with ones where the frass was left until they reached pupation, there was no difference in survival between the two groups.
Hygiene obviously wasn鈥檛 the answer. So what about lack of space? Between hatching and pupation the average skipper caterpillar builds five shelters to accommodate its growing body. If dung piled up, it would crowd out the caterpillar, forcing it to leave sooner and build another shelter. The more often a caterpillar relocates, the more energy it uses up on construction work and the less it has left for growth.
This idea was more difficult to test because the caterpillars are so fastidious. If Weiss pushed a faecal pellet into the shelter, the occupant either headbutted it out or carried it out in its jaws. So instead she used pieces of paper or leaf, stuffing shelters until only half the living space remained. Deprived of room to move, caterpillars left and started to build new homes. But even if larvae were forced to build a new shelter every two or three days, they still grew at the normal rate and reached pupation in the usual time. The crowding theory didn鈥檛 seem to stand up either.
There was one strong contender left. Perhaps the odour of ordure inside a shelter would attract predators. Parasitic wasps that lay their eggs in developing larvae are known to respond to chemical cues from frass. Might predators of caterpillars that live in shelters do the same? To put this to the test Weiss placed leaf shelters inside a cage with a colony of predatory Polistes wasps. Some shelters had frass tucked inside, others contained fake frass 鈥� odour-free black glass beads. The wasps took a keener interest in frassy shelters.
Next Weiss tried 鈥渓ive鈥� tests, offering individual wasps a choice of shelters with larvae inside. This time, she left a pile of frass or glass beads on the adjacent leaf, as close as she could get without prompting the caterpillar to clean it up. The wasps found and dispatched the caterpillars next to the frass with ruthless efficiency. In 17 trials, only three of these caterpillars survived longer than five minutes, while 14 of the larvae in clean shelters survived (Ecology Letters, vol 6, p 361). 鈥淚 suggest that some ancestral skipper evolved flinging as a way of getting rid of cues that attract predators,鈥� says Weiss.
This might explain why skippers get rid of their waste 鈥� but why bother to send the stuff any further than the edge of the leaf, where it will drop off into the void? Why, in short, do they have such excessive firepower? As it happened, Weiss wasn鈥檛 the only researcher taking an interest in fast-flying faeces. In Canada, at the University of Western Ontario, zoologist Stanley Caveney was investigating the firing mechanism in the related Brazilian skipper, Calpodes ethlius, and his studies may hold the key.
In the run-up to defecation, Brazilian skippers pump blood into the rearmost compartment of their abdomen, pushing the faecal pellet along the rectum. As the pellet emerges, a toothed piece of cuticle called the anal comb swings down and clips over a swollen ring in the rectal wall, preventing the pellet from falling out. When the compartment is fully pressurised, the comb flips free of the ring, and a hard skeletal plate above the anus slams down onto the back end of the pellet, firing it off like a tiddlywink (Journal of Experimental Biology, vol 201, p 121).
The ability to raise blood pressure in the rearmost part of the body is common in many caterpillars. It may have evolved as a means of pushing out faeces the normal way or as a mechanism for improving the uptake of oxygen by ensuring blood cells come into close contact with breathing tubes. When a pile of poo became a potentially lethal liability, evolution simply hijacked an existing bit of insect physiology and added the anal comb to make the most of it. Instead of acquiring an effective waste disposal system, caterpillars ended up with something quite spectacular.