It's a jungle out there

There's an arms race in the animal kingdom: hosts and their parasites fight a constant battle for survival. Take the cuckoo. It seems to be winning, reports Laura Spinney. For now...
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Picture the scene: a nest inhabited by a mummy bird, a daddy bird, a chirruping baby bird and an egg. This image of domestic bliss lasts until the egg hatches and a psychopath suddenly appears: a cuckoo chick that will quickly grow to six times the size of either "parent" and have an appetite to match. It will murder its foster siblings in cold blood, hoisting them on to the small of its back and climbing backwards up the nest to tip them out, and then it will work its parents to exhaustion through its constant demands for food.

Cuckoos are the most notorious brood parasites, but other birds practise similar dirty tricks. African honeyguides, for instance, stab the offspring of their host with a special bill hook. Fish do it too: the cuckoo catfish of East Africa's Lake Tanganyika smuggles its eggs in among those of another species, a mouth-brooding cichlid, and, inside that teeming mouth, the cuckoo fry repay their host's hospitality by eating its own fry. And, among insects, a related phenomenon called social parasitism is rife. The shameless cuckoo bumblebee queen simply hijacks a ready-made colony for her own ends.

Researchers are interested in brood parasitism partly because it reveals the fragile economy of the nest or family unit - the delicate balance between the expandable hunger of the brood and the finite resources of food and parental energy - but also because it epitomises the evolutionary arms race. Here are two species locked in a sort of deadly embrace, each constantly trying to outwit the other and yet at the same time ensure their own long-term survival.

"What quite a few birds do is that they have a fatal sibling competition, where somebody in the nest has to starve in order to make the budget work out," says Douglas Mock of the University of Oklahoma, who studies "siblicide" in egrets. "If you study birds that are all close genetic relatives, as I do, then the great puzzle is, why are they killing each other? Conversely, if you're studying cuckoos, which are unrelated to anybody else in the nest, then the question is, why do they ever spare anybody?"

There is, in fact, a spectrum of behaviour that comes under the label of brood parasitism. The European cuckoo slays all its adopted nestmates, while the brown-headed cowbird of North America reprieves one or two. Rebecca Kilner, an evolutionary biologist in the University of Cambridge's department of zoology, has been studying the different strategies and thinks she may have found a possible explanation for this variation.

The European cuckoo never builds its own home, but lays its eggs in the nest of several host species, including the reed warbler. As soon as the female reed warbler has laid her first egg, the cuckoo swoops in, removes it, deposits her own, and makes her getaway. The heist takes 10 seconds from start to finish. The cuckoo egg looks almost identical to the reed warbler egg, though it is slightly larger, and the cuckoo hatches first. With devastating efficiency, it then goes about securing its orphanhood, using the piggyback method to evict the other eggs.

Any resemblance between cuckoo and reed warbler ends at the egg stage. Yet, as Kilner explains: "The parents slave away, bringing food for a chick that looks nothing like their own." Other researchers have shown that a cuckoo chick's rate of calling is faster than that of a reed warbler, that it equates to the call of four reed warblers, and that the cuckoo receives the ration of four reed warbler chicks. In other words, it behaves selfishly - but not quite as selfishly as you might expect.

The cuckoo actually struggles to get that ration, says Kilner. And evidence suggests that among parasitic bird species that occasionally build their own nests, those that are reared in "foreign" nests grow more slowly than their home-grown counterparts. Given that they share no genes with their adopted nestmates, and given how clever they are at duping their hosts, why don't those parasites go all out for selfishness and grow as fast as they can?

The reason, says Kilner, is that the host parent seems to have a built-in safety check: it determines its rate of provisioning not only by the chicks' calls, but also by the expanse of brightly coloured flesh on display from their gaping throats. Kilner demonstrated this in an experiment in which she counted the food loads that reed warbler parents brought per hour to broods of either two or four chicks, both with and without the additional calls of another brood that was broadcast through tiny speakers attached to the nests. The parents brought more food when both the gape and vocal cues increased - that is, when the brood size genuinely increased - rather than when just the vocal cue was enhanced.

"Parents use exactly the same rules for the cuckoo as for their own offspring, and the cuckoo tunes into these rules," she says. "That explains why it doesn't command vastly high provisioning rates, because it creates a signalling problem by evicting the other chicks from the nest." It compensates to a degree with its accelerated call, but even so there is an upper limit on how much it can manipulate the parental effort.

Enter the brown-headed cowbird, which also exploits a variety of host species. Kilner reviewed the literature on cowbirds, and found that their presence was most lethal to their nestmates when those nestmates were small, probably because their small size made them more vulnerable to starvation in the company of a large beggar. But mortality was also higher among cowbirds when those other nestlings were small. In fact, cowbirds did best when their fellow nestlings were of intermediate size, and one or two of them survived. Kilner suspects that the combined gape of three mouths persuades the host parent to bring more food, of which the cowbird then commandeers the lion's share. And she has preliminary evidence from manipulations of cowbird and host-nestling combinations that this explanation is correct.

The different strategies of brood parasites may have evolved to suit different species in different ecological niches, with different incidence rates of parasitism. But far from being static, the relationship between host and parasite is dynamic and continues to evolve. In Europe, the reed warbler occasionally rejects a cuckoo egg, but once the egg has hatched it happily feeds the resulting behemoth. By contrast, the Australian host of another cuckoo is more discerning when it comes to its chicks. Kilner's field observations in Australia have revealed that the female superb fairy-wren abandons her nest in 40 per cent of cases of parasitism by the Horsfield's bronze-cuckoo, after the lone cuckoo nestling has hatched, yet she never makes the mistake of abandoning her own brood.

Kilner believes that the short breeding season in northern Europe has a lot to do with it. "Northern European birds don't have very many opportunities to learn either what their eggs look like or what chicks look like," she says. "The birds in Australia live much longer, and they can get three or four breeding attempts out of a breeding season. That means they can afford to spread their learning over many reproductive attempts."

In turn, though, the cuckoo has raised its game. When she and her colleagues analysed the call of the Horsfield's bronze-cuckoo, and compared it to that of another cuckoo that rarely invades the superb fairy-wren's nest - the shining bronze-cuckoo - they found that the Horsfield's call resembled the wren's far more closely.

So the arms race escalates, but there is one cuckoo in Japan that may be able to declare victory - at least for now. It has patches on the underside of its wings, the colour of which closely resembles that of the gaping throat of its host's nestlings. By flashing these patches at the parent, and issuing its deceptive call, it can persuade the parent to feed it ad libitum, without the assistance of other nestlings. It can, in fact, behave perfectly selfishly. What will its prospective hosts, the losers in the game, come up with next to counter this ingenious ploy? Watch this space.