Wednesday, December 28, 2011
Crafty Caterpillars Mimic Each Other to Avoid Predators
To protect themselves from hungry predators, caterpillars have evolved a number of defenses. Some caterpillars physically camouflage themselves to look like bird droppings or sticks, while others have developed fake eyes to scare off birds. Some caterpillars even have chemical defenses gained from poisonous plants, which they then broadcast to predators with a bright warning coloration.
Although many adult butterflies employ mimicry — where one species develops warning color patterns similar to another species' — to quickly teach predators which insects to avoid, scientists have observed few definitive cases of caterpillars using this strategy.
"Mimicry in general is one of the best and earliest-studied examples of natural selection, and it can help us learn where evolutionary adaptations come from," University of Florida biologist Keith Willmott said in a statement.
Read more here:
http://www.livescience.com/17647-caterpillar-mimicry-predation.html
Friday, November 5, 2010
Drongos mimic alarm calls to get a free lunch
When a meerkat hears the alarm call, it drops its food and runs for cover thinking there's a predator around, allowing the drongo to get a free lunch.
This is the first time scientists have shown that birds use alarm calls specifically to deceive other species.
'Meerkats have learnt to recognise the alarm calls made by different bird species and flee for cover when they hear them,' says Tom Flower from the University of Cambridge and author of the study, which is published in Proceedings of the Royal Society B.
This latest study suggests that fork-tailed drongos (Dicrurus adsimilis) have exploited the meerkats, using both their own and mimicked alarm calls to scare meerkats when they see them with scorpions or geckos.
Flower was working on meerkats in the Kalahari in southern Africa, when he noticed drongos following them around. He noticed the birds making alarm calls when there were no predators nearby and thought they must be doing it on purpose.
'Drongos are following meerkats and pied-babblers around in the hope of catching their food,' says Flower.
He thought the birds might moderate the number of times they lied to avoid blowing their cover. But this doesn't seem to be the case. 'They just turn up and steal as much food as they can get away with,' Flower says.
The researchers think the birds use a repertoire of alarm calls to keep meerkats on their toes, and to stop the creatures getting suspicious.
'It's like the boy who cried wolf: if drongos use the same call each and every time, meerkats will learn to ignore them, so instead they use different calls,' says Flower.
'Meerkats have to sit up and take note, because they've got too much to lose if they ignore the calls. They could lose their lives,' he adds
Drongos act as sentries for other animals - when they make alarm calls, meerkats and birds called pied-babblers know to run for cover. But if they do it too often, they won't be believed. So, they have to change which alarm call they use to stop meerkats ignoring them.
While scientists know that birds use their own and other birds' alarm calls to alert others to danger, until now, they weren't sure if the calls were used to deceive.
To show that fork-tailed drongos use deceptive alarm calls to get a free lunch, Flower's research had to satisfy three conditions. He had to show that alarm calls are used only in a deceptive context rather than an aggressive context; that true alarm calls made by drongos and other species sound the same as false alarm calls; and that meerkats and pied-babblers run for cover in response to recordings of both false and true alarm calls.
Researchers have suggested a number of possible functions for mimicry, such as that being able to copy other birds might help attract a mate, or that it lets animals communicate with other species. But no-one has shown that having a wide repertoire of calls attracts more females.
Flower's research shows a clear function for vocal mimicry, when before scientists could only speculate. He thinks mimicry is likely to be a fairly simple mechanism, and that drongos work out which calls are most effective by trial and error.
He's now keen to go back to the Kalahari to see how drongos learn to vary their calls.
by Tamera Jones
http://planetearth.nerc.ac.uk/news/story.aspx?id=856
Drongos mimic alarm calls to get a free lunch
When a meerkat hears the alarm call, it drops its food and runs for cover thinking there's a predator around, allowing the drongo to get a free lunch.
This is the first time scientists have shown that birds use alarm calls specifically to deceive other species.
'Meerkats have learnt to recognise the alarm calls made by different bird species and flee for cover when they hear them,' says Tom Flower from the University of Cambridge and author of the study, which is published in Proceedings of the Royal Society B.
This latest study suggests that fork-tailed drongos (Dicrurus adsimilis) have exploited the meerkats, using both their own and mimicked alarm calls to scare meerkats when they see them with scorpions or geckos.
Flower was working on meerkats in the Kalahari in southern Africa, when he noticed drongos following them around. He noticed the birds making alarm calls when there were no predators nearby and thought they must be doing it on purpose.
'Drongos are following meerkats and pied-babblers around in the hope of catching their food,' says Flower.
He thought the birds might moderate the number of times they lied to avoid blowing their cover. But this doesn't seem to be the case. 'They just turn up and steal as much food as they can get away with,' Flower says.
The researchers think the birds use a repertoire of alarm calls to keep meerkats on their toes, and to stop the creatures getting suspicious.
'It's like the boy who cried wolf: if drongos use the same call each and every time, meerkats will learn to ignore them, so instead they use different calls,' says Flower.
'Meerkats have to sit up and take note, because they've got too much to lose if they ignore the calls. They could lose their lives,' he adds
Drongos act as sentries for other animals - when they make alarm calls, meerkats and birds called pied-babblers know to run for cover. But if they do it too often, they won't be believed. So, they have to change which alarm call they use to stop meerkats ignoring them.
While scientists know that birds use their own and other birds' alarm calls to alert others to danger, until now, they weren't sure if the calls were used to deceive.
To show that fork-tailed drongos use deceptive alarm calls to get a free lunch, Flower's research had to satisfy three conditions. He had to show that alarm calls are used only in a deceptive context rather than an aggressive context; that true alarm calls made by drongos and other species sound the same as false alarm calls; and that meerkats and pied-babblers run for cover in response to recordings of both false and true alarm calls.
Researchers have suggested a number of possible functions for mimicry, such as that being able to copy other birds might help attract a mate, or that it lets animals communicate with other species. But no-one has shown that having a wide repertoire of calls attracts more females.
Flower's research shows a clear function for vocal mimicry, when before scientists could only speculate. He thinks mimicry is likely to be a fairly simple mechanism, and that drongos work out which calls are most effective by trial and error.
He's now keen to go back to the Kalahari to see how drongos learn to vary their calls.
by Tamera Jones
http://planetearth.nerc.ac.uk/news/story.aspx?id=856
Saturday, July 17, 2010
Beetles Use Sex And Subterfuge To Infiltrate Bee Nests
Upon hatching from their sandy burrow, hundreds of these dark-orange beetle larvae, called triungulins, find their way to the tip of the nearest plant stem, where they form wriggling masses, or aggregations, that roughly resemble and likely smell like female Habropoda pallida bees, says lead author Dr. John Hafernik, who with co-author Leslie Saul-Gershenz documented this behavior during the springs of 1992 and 1999 from the California State University Desert Studies Center.
According to the researchers, once the triungulin mass successfully lures a male bee into pseudocopulation, the larvae use pincher-like limbs to attach themselves to the underside of the duped bee. The male then deposits the larvae on to female bees during further mating attempts, a process called venereal transmission. “By first attaching to a male bee, triungulins have access to multiple females and, subsequently, the multiple nests of each female,” says Saul-Gershenz.
Female bees then unwittingly transport these larvae back to their nests while provisioning them with pollen and nectar for their own eggs. “Once inside, the larvae parasitize the nest,” says Hafernik, chair of SF State’s Biology Department. “The provisions that would have produced a bee produce a beetle instead. Bee eggs already in the nest cell are likely eaten by the larvae as well.” Hafernik adds that “while cooperative behavior is common among highly social insects, such as bees and ants, it has never been reported in blister beetles. What’s more, until now, no other insect has been known to use cooperative behavior to mimic other species.”
The researchers believe the aggregations lure males into copulation through a combination of visual and olfactory cues. They noted that triungulin masses position themselves on vegetation much like female bees—perched on the top of a plant stem—and males approach and land on masses and females in the same way. To test for the possibility of olfactory cues, the researchers placed model aggregations near live aggregations that were formed or in the process of forming. “The male bees ignored the models completely but hovered or tried to land on groups of triungulins even before they were formed into a bee-like mass,” says Saul-Gershenz, who is currently studying the chemical cues. “The triungulins are likely emitting a bee-like pheromone to attract males, and another chemical cue to form aggregations.”
During their field survey, the researchers observed the life cycle of 22 masses, noting 98 instances of bees hovering within a few centimeters of a triungulin aggregation and nine instances where bees landed on aggregations. Researchers have long known that many blister beetle species parasitize bee nests, but never made the connection between triungulin aggregations—first reported in 1895—and nest finding.
Aggressive mimicry is not new, but has only been associated with individuals of a species. The Ophrys orchid mimics the appearance and scent of female bees to attract pollinators to its flower, and female bolas spiders attract prey by mimicking the female sex pheromone of the armyworm. Dr. Ronald McGinley of the Smithsonian Institution’s Department of Entomology says the findings raise “exciting questions” for future research. “How do newborn beetle larvae coordinate a collective pilgrimage to individual grass stems? And why is this particular bee species attracted to ‘larval clumps’? Is the attraction visual, chemical or both? We can look forward to these researchers revealing some of these answers in future work.”
http://wildlifenews.co.uk
Saturday, June 19, 2010
Insects That Can't Beat Them Scare Them (Via HerpDigest)
6/14/10 by Sean B. Carroll , New York Times
Imagine that you are a one-half-ounce, two-inch-tall insect-eating bird foraging for dinner on the dimly lighted floor of a Costa Rican rain forest. You come face to face with a pair of beady eyes. Study them for a moment.
If those eyes belonged to a snake, that moment of study would mean that you would be dinner by now.
The face, however, is not a snake's, but the chrysalis of a skipper butterfly. An uncanny resemblance - but, as it turns out, not a unique disguise.
In one area of Costa Rica alone, a team of researchers led by Daniel H. Janzen and Winnie Hallwachs of the University of Pennsylvania and John M. Burns of the Smithsonian National Museum of Natural History have discovered hundreds of species of moths and butterflies whose caterpillars or chrysalises display false eye and face patterns that mimic those of snakes, lizards or other animals. In a study published this week in The Proceedings of the National Academy of Sciences, they propose that this plethora of counterfeit patterns has evolved to exploit birds' innate instinct to avoid potential predators.
The idea is a fresh twist on the well-established phenomenon of mimicry among animals. First described by the British explorer Henry Walter Bates in the 1860s (the subject of my column on Feb. 16), the original insight was that harmless, edible species could gain protection from predators by resembling distasteful, noxious species.
Bates assumed that for this mechanism to work, the potential predators had to learn which prey in their range were to be avoided. And the potential prey - say, a large, colorful adult butterfly - must closely resemble the inedible species it mimics.
But when it comes to a deadly encounter with another species, there may be no second chances, no opportunity for learning. Hence, natural selection would favor instant recognition, and hard-wired rapid responses, in a close encounter with potential danger. Harmless creatures that evolved some general resemblance to the variety of creature features to be avoided (eyes, scale patterns) would then gain some protection.
Dr. Janzen and colleagues have cataloged a delightful assortment of striking false eye patterns on the front and rear ends of caterpillars and the front ends of chrysalises.
Their bounty and insights are the product of a dedicated, and somewhat accidental, long-term study of the denizens of the Área de Conservación Guanacaste, or A.C.G., in northwestern Costa Rica.
It began in 1978, when Dr. Janzen broke some ribs falling into a ravine while conducting field studies in the region. The road to the hospital was too rough to navigate, so he wrapped his sore rib cage and confined himself to a chair for a month.
Unable to explore the rain forest, he soon went a bit stir-crazy. The field station had only two hours of electricity each night, and just enough power to run a 25-watt light bulb. Fortunately for Dr. Janzen, that was a bumper year for moths, which were attracted to the light. So he passed the time building a moth collection.
When he recovered enough to wander back into the rain forest, he discovered that it was also a bumper year for caterpillars. The challenge was to identify which of the many different kinds of caterpillars belonged to which species of moths or butterflies. Now 71, he told me from his field station 32 years later that "my private insanity was to find all of the species before I die."
To accomplish his goal, he had to set up a system of collecting the caterpillars, photographing each of them, raising them into adults, then identifying each of the species, at least half of which had not been described previously. He started by himself, then was joined by his wife, Dr. Hallwachs, an expert on rodents and now caterpillars. The operation continues to this day, 365 days a year, with the help of 33 trained Costa Rican assistants.
In an area of about 77 square miles, more than 450,000 caterpillars have been studied. As of a few years ago, the team had identified more than 12,000 species. That number ballooned to 15,000 species when the team discovered, through the use of DNA typing, or "bar coding," that many of the species were actually made up of multiple distinct species, as many as 11 in one case. The total number of species in just this one region equals that of all of the moths and butterflies species of North America.
With caterpillars and chrysalises coming into the station at the rate of more than one hundred a day, Dr. Janzen began to discern a trend. In species belonging to many different groups, he saw caterpillars or chrysalises that bore all sorts of paired eyelike markings of various color schemes, with round or slit pupils. The variety of patterns suggested that the bugs do not have to match exactly the appearance of any particular predator for the ruse to work.
Moreover, the distinct behavior of many caterpillars when handled underscored that the whole game was to startle the many species of insect-eating birds that foraged in the dry, cloud and rain forests of the conservation area. Some eye patterns became visible only when the caterpillars were molested and expanded part of their body, and some large specimens wriggled and rattled like snakes.
Dr. Janzen and his colleagues estimate that a typical foraging bird might encounter tens to hundreds of false-eyed bugs each day. It is unlikely that a bird encountering such a spectrum of patterns could learn to discern which specific ones were safe and which were not, especially when one mistake would mean its demise. It would be better to leave suspicious items alone and to quickly move on.
For two centuries, naturalists have sought to catalog and make sense of the dazzling diversity of life, particularly as found in the tropics. Often, new insights have come from asking very simple questions, like "Why does this small caterpillar look like a snake on one end?"
But the answer to such questions requires finding many more creatures and understanding where and how they live. And that requires a special breed of human willing to live far from the comforts of home and eager to look at 450,000 bugs for 32 years.
http://www.nytimes.com/slideshow/2010/06/11/science/20100615-creatures.html?ref=science
for slide show of insects trying to look like snakes.
Wednesday, September 30, 2009
Monster insect mimic lures prey with siren song
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.
Monster insect mimic lures prey with siren song
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.