Objects of an unnatural lust

When dungflies and houseflies become infected with a certain fungus, strange behaviour can ensue. Malcolm Smith reports Anyone who has had fleas knows how irritating and embarrassing such a parasite can be. The uninvited visitors may even alter the behaviour of their hapless human host: more frequent scratching; dusting with insecticidal powders; maybe even a reluctance to mix with colleagues and friends.

But these are minor changes in behaviour compared with the transformation some hosts endure when parasites overtake them. When a fungus called Entomophthora grows on and inside its dungfly host, the creature becomes paralysed in a bizarre perching position it never adopts naturally.

The fate of the dungflies, however, is as nothing to the effect the fungus of a related species has on the common housefly. This creature has never had a good press. It feeds on just about anything but has a particular fondness for decaying bits of plants and animals. The problem is that traces of wherever it last ate stick to its feet, carrying disease-causing microbes to its next meal, which might be food meant for human consumption.

Nor has its image been improved by the way it has figured in horror films and science fiction. But those flies infected with the fungus meet a fate beyond even the imaginings of Hollywood film-makers: they end up as the objects of necrophiliac lust by their uninfected fellows.

But first the dungflies, whose fate was recently reported in Proceedings of The Royal Society (B. vol 258: 187-193). Dr David Maitland of Leeds University has been studying their death throes, and suggests the fungal parasite uses the flies to give it a better chance of dispersing its spores, and thus to infect ever more flies. He has coined the apt title "enslaver parasites" to describe their highly peculiar actions.

Dr Maitland studied the flies at two Yorkshire locations. At both, healthy yellow dungflies always perched on the upper surfaces of leaves - nettles and thistles are particularly favoured - low down on the plants. They showed no particular preference forthe wind direction they faced, tending in most cases to perch facing outwards on their chosen leaves.

No less than 91 per cent of parasitised dungflies, before they were killed by the fungus, clung to the underside of leaves towards the top of the plant. So they were invariably above the healthy dungflies. What's more, most faced into the centre of the plant, adopting a highly artificial, head-down, abdomen-up position and favouring the plant's down-wind side.

So why the big difference? Dr Maitland reckons that healthy flies perch the way they do because of the need to be vigilant. Such vigilance is required if they are to maintain or defend their own little territory, find mates or avoid predators. Parasitised dungflies clearly are not being vigilant. The position they adopt - hanging beneath leaves, sheltered from rain - seems an ideal one from which fungal spores can disperse from the fungus-filled fly abdomen.

With the fly's rear end up in the air, facing outwards from the plant and down wind, it is difficult to imagine a better position for fungi of the future to begin life. Their deathbed position also involves their wings being spread apart and pressed downtowards the leaf surface. This, Dr Maitland thinks, is to prevent them from getting in the way of any sticky spores forcibly ejected by the fungus from the fly's abdomen.

But why do the fungus-ridden flies perch higher up on plants than their healthy siblings? Dr Maitland suggests it is because the spores can rain down on the healthy flies below, increasing the chances of infecting them and perpetuating the fungus.

The effect a flea has on its host's behaviour is well known and easy to understand. What is truly striking in the tale of the dungfly is how a primitive "plant" such as a fungus can so alter the physiology and behaviour of its host. No one knows the answer to that one.

When the same fungus, or a related species, parasitises the housefly, it does not change its host's perching position. Instead, infected housefly cadavers somehow become highly attractive to sexually active male houseflies. As the males try to mate with the corpses, they pick up a sort of venereal disease and so the fungus has a chance to disperse itself. The attraction of fungus-filled dead flies might be hard to imagine; perhaps some chemical attractant is involved. In the summer large numbers of houseflies succumb to this fungus. So if you see piles of dead houseflies, don't clear them up too quickly; leaving them for a while increases the chances of even more flies being killed - which means less swatting.