A Pied Piper of a different kind

“…from street to street he piped advancing, and step for step they followed dancing…” Pied Piper of Hamelin, Robert Browning (1842)

An ant colony is a fortress. Patrolled by dedicated guards ready to die for their cause. They protect the nest’s countless inhabitants, its young, its legacy, its treasure trove of resources. Such a bounty within the fortress walls is a temptation for others, of course. Though any intruder foolish enough to invade or infiltrate the colony unprepared will be detected, tracked down, and ruthlessly taken apart by the defenders. Yet, for those that can survive, and succeed in their trespass, the rewards can be great; access to the ants’ hoarded supplies, shelter within a heavily guarded home, and even the unfortunate ants themselves as a food source, if the invader is so inclined. To achieve this, however, and to safely run the gauntlet of entrance into the depths of the nest, an intruder requires remarkable specialisation. Most intruders, accidental or otherwise, will fail. Only a special set of morphological, behavioural, or chemical specialisations will allow a trespasser to succeed and reap the rewards.

Signals by ant sentries to rally the colony’s defenders involve the use of chemicals. The majority of communication between ants is done in this way, a method that initially can seem strange to us. “While we live in an ‘optical’ universe, with vision as our primary sense and most of our actions driven by eyesight, insects perceive their world mostly on a chemical basis,” explains Dr Andrea Di Giulio, an entomologist based at Roma Tre University. “A male moth looking for a mate, for example, can detect the chemical signal of a female from kilometres away”. For many insects, eyesight simply isn’t involved. In ants, chemical signals are passed on via cuticular hydrocarbons – chemicals present on the surface of all insects – and pheromones, conveying messages that drive ant behaviour and allow these industrious marvels to work in sync, leading to their famous feats of teamwork. One way an intruder could safely negotiate a bustling ant colony is to exploit this chemical form of communication: there are a number of butterflies, spiders, and beetles that produce chemical signals that protect themselves from angry ants within the nest and pass through unharmed.

Perhaps less well known than their chemical chatter, ants also communicate with sound, and these acoustics are thought to play an important role in ant organisation. The sounds are known as stridulations, low frequency chirps produced by scraping an area of the leg (known as the plectrum) against a ridged section of the body (the pars stridens). While not reaching the same volume levels, this method is similar to the way crickets and cicadas produce their extraordinary acoustics. Ants use these chirps for a number of purposes, from mating to requests for assistance, and, alongside their chemical communication, they are essential for the smooth running of the colony. Much like the chemical communication, though, this form of signaling is vulnerable to exploitation by specialists.

Enter, the ant nest beetle, of the Paussus genus. A beetle with a very particular set of skills. A beetle that has adaptations that allow it to take advantage of all that is on offer behind the fortress walls. It is tiny, unassuming, a little smaller the than the queen of the Moroccan Pheidole pallidula ants whose home it invades in the Atlas mountains.

“They are social parasites,” explains Andrea. “Ants are a universal symbol of productivity and industry, and Paussus beetles infiltrate their colonies to take advantage of all their hard work.” But how do these sneaky beetles safely negotiate the fortress? What form of mimicry is allowing them safe passage past legions of ant soldiers- chemical or acoustic? “Early entomologists noticed that Paussus beetles have organs to produce sounds, to stridulate, but noone ever heard these sounds, and no-one looked deeper into their function,” says Andrea.

Until now. The chemical mimicry of Paussus beetles had previously been discovered, an adaptation that allows them immunity from attack when living life amongst ants. But any acoustic talents of the beetles had until recently been overlooked. Alongside any chemical tricks, could this potential to produce sound be part of their survival strategy inside the nest?

Andrea and his team investigated. The first obstacle of many was actually finding the elusive beetles. “They are not easy to find!” says Andrea. “The beetles are less than half a centimeter long and live hidden deep in the nests of a specific species of ant.” Days and days were spent in the searing heat of Morocco’s remote places, tracking down nests of the relevant ant species, then toppling stones, and digging through the fortresses hoping for any sign of Paussus. And, of course, not helped by the fearless, indignant ants, swarming up the researcher’s limbs to defend their homes. Only a small percentage of ant colonies have been parasitised, and even when a colony has been, the beetles aren’t easily spotted within the maze of tunnels. “After many frustrating searches, we finally found a place where we could collect a good number of specimens – a memorable day!” Beetles successfully collected, the team was ready to tackle the second obstacle: the challenge of actually hearing the Paussus beetles’ mystery acoustic repertoire. “Recording the sounds was also not an easy task. We used very sophisticated apparatus to hear and record the Paussus beetles, and you can imagine our emotions when we were finally able to listen to these recordings – after all, we were the first humans to hear these songs!” Three distinct songs were identified and recorded, rather than the single, simple sound that the researchers were expecting.

The next piece of the puzzle was to identify how the songs benefit the beetle. Did it somehow work with the chemical mimicry to make the beetle’s life within the nest easier? While thousands of examples of chemical mimicry have been documented, only once before had any form of acoustic mimicry been recorded: deep within the brood chambers of some ant nests, larvae of the Maculinea butterfly are pampered and preened by attentive workers. The larvae of the Maculinea stridulates to mimic the sounds of the colony’s queen, essentially posing as ant royalty and making the most of the benefits this social status brings.

Within the forbidding ant colonies of the Atlas mountains, could the Paussus beetle be mimicking sounds in its own attempts to be treated like a queen? Initial analysis of sound waves suggested striking similarities between the stridulations of the beetle and Phiedole ant communications. Workers, soldiers, and queens – the three castes of the ant species – all generate a different sound. The three beetle songs recorded appeared to accurately mimic the pulse and intensity of these caste-specific sounds, and the team were starting to really believe that there was more to come from this enigmatic beetle.

To test the reactions of ants to the signals, the researchers buried a miniature speaker in shallow sand, and within the same chamber placed Phiedole ants. From the hidden speaker came the sounds of the Paussus’ stridulation songs, and the researchers found themselves captivated by the ant behaviour they subsequently observed. Instead of aggression, racing towards the alien sounds to attack, the ants investigated the noise. The pattern of their antennae waving was one they use only when detecting fellow ants, and they surprised the observers even more by starting to dig towards the sound – a behaviour that likely indicates a rescue attempt of a fellow ant in trouble. “Our basic hypothesis was that Paussus beetles use sounds alongside chemicals to fool ants,” says Andrea. “But we could never imagine that these beetles have a repertoire of different sounds that mimic those of the various ant castes: the workers, the soldiers and the queen.”

These beetles were capable of seductive songs, mimicking each ant caste, suited to different situations and needs. While its chemical signals allow it to safely enter a nest without fearing attack, its acoustics can then enhance its life within. Copying the queen, the beetle can elevate its social status to that of royalty, in turn soliciting more effective care, and gain free run of the entire colony. Paussus eggs will be laid, and, once hatched, their young are fed by willing ant workers as if they were their own. As the beetles reach adulthood, their hoodwinked hosts will still pamper them, and they will respond to the ants’ hospitality by feeding on ant larvae, perhaps using a particular stridulation to be instantly forgiven for such behaviour.

“Our finding is the only known case of an invertebrate with a complex repertoire of acoustic signals to mimic the different sounds produced by another animal. This discovery has important implications for our understanding of co-evolutionary processes in host-parasites relationships,” explains Andrea. “The more we investigate the acoustic world of insects living with ants, the clearer it becomes that this pathway actually represents an overlooked route of host colony infiltration for the thousand of species of social parasites living at the expense of ants.” The relationship between beetle and ant is a fascinating one, a social parasite integrating completely within the ant colony, turning a forbidding fortress into a comfortable home, fooling its industrious hosts first with chemical mimicry and then with complex acoustic mimicry to ensure all its needs are catered for, and in many cases, living like a queen.

The above article was originally featured in Biosphere Magazine.

Image credit: Andrea Di Giulio, Roma Tre University.

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