EVERYTHING was going to plan for the male cicada looking for love. High in his tree in the dry bush country of eastern Australia, he started his serenade. First he gave a bright chirruping prelude, then urr-chip, urr-chip, urr-chip. Right on cue came an answering click. Each time the cicada repeated his urr-chip, there was that click again. His luck was in: a female was signalling her interest. The cicada began to move slowly towards the source of the clicks, singing as he went. The closer he got, the louder the clicks, and soon he could make out a telltale trembling among the leaves. Sure of his target now, he made his final move.
Quick as a flash, a pair of long, green legs darted out and clasped him in a tight embrace. In another instant, a powerful pair of insect jaws clamped around his head. What had gone wrong? His song was perfect, the response exactly right and dead on cue. But the cicada had been deceived. Those come-hither clicks were not the love call of a female cicada but a con trick executed by a voracious predator in search of a meal.
When husband-and- wife cicada experts Dave Marshall and Kathy Hill of the University of Connecticut at Storrs first heard this insect duet they too were taken in. They study cicadas belonging to the Cicadettini tribe, a group in which males and females locate each other with a characteristic call-and-response routine. Recently they have focused their attention on Australia, where there are hundreds of species of these duetting cicadas, most undescribed and many still to be discovered. To their expert ears, what they were hearing was the call-and-response of Kobonga oxleyi. "When we homed in on the clicks, we expected to see a small, black cicada," says Hill. "Instead, we found a giant green-and-white katydid."
Hill and Marshall had stumbled across something extraordinary. The spotted predatory katydid, Chlorobalius leucoviridis, a species of bush cricket common across the arid interior of Australia, has a unique talent. It snares male cicadas by imitating the female response to their songs, making it the first known example of acoustic aggressive mimicry.
Most examples of mimicry are a form of defence. Innumerable insects camouflage themselves as leaves, flowers or twigs, or pose as unpalatable species to escape predators. Aggressive mimicry is more malevolent: this time it is the predator that fools its prey, luring victims with the false promise of food or sex. The most famous examples are bolas spiders, which produce fake female-moth pheromones, and predaceous female fireflies, which mimic flashing females of other species (see "Love-lights and perfumed nights").
To mimicry based on smell and sight, we can now add sound. For Hill and Marshall, the siren call of the katydid is exciting for another reason too: it may help explain why cicada songs are so diverse and evolve so quickly.
Male cicadas are famous for their singing, with choruses often reaching deafening volumes. Their songs consist of a rapid series of clicks generated by tymbals - a pair of ribbed, membranous organs on the sides of the abdomen. Only males have tymbals and, in general, males sing and females approach them silently. Female Cicadettini, though, are not so mute. As the male sings they chip in at intervals with loud clicks, produced by a sharp flick of their wings. "The male turns towards the sound and uses it to locate the female," says Marshall. "When it gets close it also looks for the movement of the flicking wings."
The males of each species have a unique song which enables the female cicadas to recognise one of their own. Some songs consist of simple patterns of pulsed clicks, others are much more complex, with a longish "prelude" leading into the call-and-response phase. The sound of a female wing-flick is short and nondescript, however, and so for the male, recognition hinges on timing. Embedded in every song are cues, elements of the song that the female must reply to accurately and promptly to attract a mate.
For those familiar with the songs of duetting cicadas, it is pretty easy to identify cues. They are generally made up of a short and comparatively loud burst of clicks that ends abruptly. "Even if you've never heard the species before, you can usually pick out the cues," says Marshall.
All in the timing
That has proved a boon for the biologists. They have found that one of the best ways to collect specimens is to call males down from their trees with well-timed snaps of the fingers. It takes skill: female cicadas respond to cues within 70 milliseconds, sometimes less than half that time. "Males respond to our finger snaps if we can follow the cue within around 100 milliseconds, " says Marshall. "It's easier if there's a rhythmic pattern to the song so you can anticipate where the clicks come. It takes practice but we've gotten quite good at it."
In 2005, Hill and Marshall joined up with the Australian Museum's cicada expert Max Moulds for a collecting trip in Queensland. One night, they camped near the small town of Cunnamulla. "I happened to wake up very early and heard a cicada singing," recalls Hill. "It was a species that was proving difficult to collect so I went out with my net." Then she heard what sounded like the clicking of a female. "I could see the little black male getting closer and closer to the source of the clicks. Then when it was about 20 centimetres away it abruptly flew away to another tree."
Hill couldn't find either cicada, but a few hours later she heard another male singing and two females clicking in reply. By now Marshall was up and about and after recording the duet, the pair homed in on one of the clicking females. "Then I saw what was making the clicks - a fierce-looking katydid," says Hill. "I rushed back to the tree where I heard the clicking female earlier and found another katydid, about 10 centimetres long and brilliantly camouflaged."
The recording of the duet revealed how accurate the katydid's impersonation had been. Its click was brief and acoustically nondescript, with a broad spectrum of frequencies - just like a female cicada's - and each click followed a cue from the male with an average delay of 58 milliseconds. Like a female cicada, the katydid also provided a visual clue to its whereabouts, though instead of flicking its wings, the katydid flexed its legs with a jerky bounce.
Hill and Marshall suspected that the clicks were part of a predatory strategy and it didn't take long to confirm this. Later that day they pitched their tent, put the katydids from Cunnamulla inside and released a succession of male cicadas into the makeshift lab. "Max agonised over this. It was hard work collecting specimens and now we wanted to feed some to the katydids - so we only used ones he was willing to sacrifice," says Marshall. When the first cicada began to sing, a katydid quickly replied. The cicada moved closer. And closer. Suddenly the katydid grabbed it with its forelegs and subdued it by biting off part of its head, before eating everything but the indigestible forewings. Five kills later and there was no doubt they had been right.
The experiment also showed that katydids could attract several species of cicada with markedly different songs. Their versatility as mimics became even more evident as the expedition progressed and the biologists added more cicadas to their live collection. As they drove along, every so often one of their specimens started to sing - and the katydids would reply. "When we realised how broad the katydid's abilities were, we began to play them songs from our computer archive using my laptop," says Marshall. The katydids responded to more than two dozen songs with beautifully timed responses. "They even got it right when the cicadas were from New Zealand and North America, whose songs they could never encounter."
Versatile virtuosos
By 2008, Marshall and Hill had recorded more than 30 minutes of cicada-katydid duets. The songs varied from very simple with just one sort of cue to the virtuoso, with long introductory passages followed by complex cueing sections. Cues ranged from a simple isolated "tick" to a passage lasting nearly 2 seconds (see diagram). None of this seemed to faze the katydids. They could respond correctly to 22 of the 26 species tested, and for 18 of these, they got it right more than 90 per cent of the time (PloS ONE, DOI: 10.1371/journal. pone.0004185
"Their versatility is impressive," says Marshall. "But the katydid isn't quite as clever as it looks." Female cicadas must recognise their suitor's song in its entirety even though they reply only to specific cues. Katydids don't mind which species they eat and so the distinctive phrasing and embellishments are irrelevant: they need only recognise the male's cues. As long as they click after a brief phrase that ends abruptly they are likely to attract one male or another. "It's evolved a mechanism based on the application of a few general rules. That's what makes it so versatile, but it also means it's unlikely to get it right all the time," says Marshall. As he and Hill discovered on their Australian road trips, captive katydids will sometimes respond to almost any short, sharp sound - the click of two coins or even the sound of a car's indicator signal. "They aren't perfect, but they don't need to be."
Captive katydids respond to almost any short, sharp sound, like the click of two coins or even the sound of a car's indicator.
Many questions remain to be answered about how the spotted katydid evolved to become an aggressive mimic. Like cicadas, katydids are singing insects, so they have many of the requisites for acoustic mimicry - noisemaking structures, hearing organs and a brain that can interpret patterns of sound. Some katydids sing courtship duets too, with the males trilling and females clicking in reply. Yet the spotted katydid's mimicry isn't just a modification of an existing courtship song. If that were the case, you would expect them to duet - and this species doesn't seem to. You would also expect male spotted katydid songs to include recognisable cues, which they don't. And you would expect only female katydids to click to cicadas - yet both male and female katydids capture cicadas in this way. Hill and Marshall suggest that unlike the firefly Photuris, which has adapted its normal courtship signals to trick males of closely related species, the katydid's mimicry may have evolved purely for predatory purposes.
Musical arms race
For cicada biologists, these discoveries may help answer an entirely different question. There's something about the courtship songs of singing insects that has bugged entomologists for many years. What drives their evolution and why do they change so rapidly? Sexual characteristics are usually relatively stable. "If a male sings something too different, the female won't recognise him and he loses out," says Marshall. "Yet cicada songs change unexpectedly fast and are often the first sign that populations are diverging into new species." For newly evolved species that live in the same place there's an obvious explanation: the songs must diverge to allow mate recognition. Another force for change could be female choice, where picky females encourage males to change their tune. "If the male's song was any indicator of his quality as a mate, that might explain why some songs change so rapidly, but female cicadas don't seem at all choosy," says Marshall.
Marshall and Hill suspect that in the case of Cicadettini cicadas, predation could be one of the forces driving change, as they engage in a sort of musical arms race to outwit spotted katydids. "Some songs are very complex with short phrases that look like cues. Katydids click after them - but female cicadas never do," says Hill. "These could be false cues to trick the katydid into giving itself away." As katydids cotton on to the false cues, then the cicadas must lay more traps to keep one step ahead of their predators, speeding the rate of song evolution and perhaps explaining why some songs are so extraordinarily complex.
This is not the only way to expose imposters. Some species seem more wary of poorly timed finger clicks. "They may have more stringent criteria for the exact sound of the click and its timing," says Marshall. One species that could be growing wise to the katydid clicks is Kobonga oxleyi, the little black cicada that led to the discovery of acoustic aggressive mimicry. And that could account for the behaviour of the very first one that Hill heard duetting with a katydid - the one that got away.
Love-lights and perfumed nights
Most forms of mimicry are defensive and help potential prey avoid predators. Aggressive mimicry is where predators draw prey closer with the promise of a mate or with fake food - as in the case of the angler fish's lure, or the pink worm-like tongue of the alligator snapping turtle. The most sophisticated aggressive mimics attract victims by exploiting their courtship signals.
Among the most famous are the bolas spiders (Mastophora species), the females of which attract male moths by producing a whiff of female moth pheromones. These extraordinary spiders capture their prey with the aid of a sticky ball on the end of a filament - the arachnid equivalent of a South American gaucho's bolas. When prey comes within reach, the spider swings the ball - and if it hits the insect it sticks. To ensure prey comes close enough, the spiders emit a stream of volatile chemicals that includes compounds present in moth pheromones. Most of these spiders capture moths of a single species, but M. hutchinsoni alters the perfume as the night wears on, attracting one moth species early in the evening and another a few hours later.
An even more versatile mimic is the voracious female Photuris firefly, which attracts males of other species by replying to their courtship flashes. Male fireflies signal to prospective mates with a species-specific pattern of light flashes and females reply with flashes that vary both in their length and the delay between signal and response - yet Photuris can mimic as many as 11 species. The ultimate imposter, though, is the male Photuris. In a bid to attract a female's attention, it has taken to mimicking the flashes of her prey - sensibly switching to its own courtship signals once he gets dangerously close.
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