Listening In

Above: A little blue heron pays close attention as a snowy egret searches for fish. 

Humans have always used espionage and intercepted information to get ahead of rivals. The natural world is rife with animal eavesdroppers too, writes Richard Pallardy

Feb 22nd 2021 

Your favourite fictional character is alone in the woods. Something, or someone, is after them. What tells them that danger is imminent, that they should bolt?

In many a film or TV series the moment is cued by a flock of birds launching from the canopy. If the birds are afraid, you should be too. In our highly urbanised modern era we still recognise that the flight of other animals signifies danger. We maintain the ability to eavesdrop on their behaviour: their squawks of panic, their frantic flight. Conversely, another film trope sees the animals go eerily silent, desperate to evade detection by whatever threat is slouching towards them – and indicating that their human observers ought to do the same.

These are not signals intended for us. The birds don’t care whether we’re devoured by the creature approaching through the trees. We can rely on their calls or their silence as indications of approaching problems and act accordingly. This ‘eavesdropping’ on other species’ communication is an ancient survival technique, one that is found throughout the animal kingdom – even in bacteria and plants. It’s an efficiency in an evolutionary sense: sending signals is expensive; intercepting the signals of other, unrelated species is less so.
 
listeningin whitebelliedgoawaybird SteveGarvieWhite-bellied go away bird (credit Steven Garvie)
 

We certainly do plenty of it within our own species. Eavesdropping is central to criminal justice and national security. Etymologically speaking, the word eavesdropping refers to someone snooping beneath the eaves of a house, listening in on the occupants and suffering the rain sluicing off the roof as a consequence. The Swedish word perhaps better captures this activity as it applies to all species – ‘tjuvvlyssnar’ translates as ‘listen thief’.

Theft is rife in the animal kingdom and information is not immune. A 2015 study found that 74 species of animal had been documented as responding to playback of alarm calls issued by another species. In most cases the eavesdropper benefits while the calling animal gains nothing. Eavesdropping is also known as information parasitism. For the most part animals don’t have time to eliminate the snoops in their lives; they’re busy dealing with more material thefts and assaults. Eavesdropping does not bear the same consequences as it does in humans and may even be mutualistically beneficial.

Take birds that travel in mixed-species flocks. These gatherings are in many ways enormous eavesdropping networks – and are among the best-studied instances of information parasitism. The calls of feeding birds of one species may attract additional species that feed on similar foods.

Some species of tropical antbird (Thamnophilidae) listen for the feeding calls of other species that they can bully out of the way. When larger species signal their discovery of an ant swarm the antbirds ignore them, knowing that they will be the ones that will be deterred by their competitors. Small heron species such as the little blue heron (Egretta caerulea) preferentially congregate around groups of snowy egrets, which flush fish out of the shallows. However, it is not worth following the feeding behaviour of the larger great egret (Ardea alba), which is less likely to flush fish and more likely to attack other birds that get too close.

The greater racket-tailed drongo (Dicrurus paradiseus) is a masterful information thief. It both mimics the calls of other birds, which then move in its direction and flush out insects, and follows the calls of these other birds for the same reason. While this is sometimes met with conflict – flameback woodpeckers (Dinopium) will try to chase them off – it is usually tolerated. The drongo’s announcement of the presence of predators is a worthwhile trade-off.

Solitary spies

In mixed-species flocks, solitary species benefit from the communicative nature of their social counterparts. Different birds use different levels of the canopy, giving them unique vantages from which to spot approaching danger. A loner ground-feeding bird might eavesdrop on the alarm calls of a social bird that feeds near the treetops and thus dodge a potential descending hawk.

Some 30% of American woodland birds use the alarm calls of chickadees, tits and their relatives (Poecile) as reliable indicators of danger. These little birds may seem like unlikely bellwethers, but their social nature and complex communication abilities are invaluable to solitary species and to those that feed at different levels in the canopy. In Africa solitary scimitarbills (Rhinopomastus) flock with southern pied babblers (Turdoides bicolor), which are social and noisy. When scimitarbills flock with babblers they reduce their vigilance by up to 60%. By relying on another species to alert them to danger they are able to devote more time to foraging.

Birds’ acute eyesight, aerial observations, and clamorous communications are incredibly useful to a wide array of other species. For Günther’s dik-dik (Madoqua guentheri), a species of tiny antelope, the calls of the white-bellied go-away-bird (Corythaixoides leucogaster) are key to its survival. Unable to peer above the thickets it prefers, it relies on the bird’s alarm calls as an indication that it is time to flee.

Several species of small lizard in Madagascar known as zonosaurs similarly rely on the calls of the paradise flycatcher (Terpsiphone mutata) to send them scurrying to safety. Koch’s giant day gecko (Phelsuma kochi) shifts its colouration in response to the calls of the same bird. Even black rhinoceroses (Diceros bicornis) read cues from red-billed oxpeckers (Buphagus erythrorynchus), perhaps explaining their tolerance of these birds.

Animals that eavesdrop are selective about who they listen to to avoid false alarms. Zebras (genus Equus) are attentive to the changes in posture of giraffes when they see an approaching lion (Panthera leo). They are less likely to pay attention to the alarms of impala (Aepyceros melampus), which are preyed on by lions but also by smaller predators that pose no threat to zebras. Similarly, two tiny Australian birds, superb fairy-wrens (Malurus cyaneus) and white-browed scrubwrens (Sericornis frontalis), flee when they hear the alarm calls of the larger New Holland honeyeaters (Phylidonyris novaehollandiae), but the honeyeaters are less likely to react to the calls of the smaller species, which often shriek at the sight of creatures that pose no threat to them.

Some animals respond not to alarm calls, but to silence. Male túngara frogs (Engystomops pustulosus) will stop calling when a quorum of other males, even those of other species, stop calling, usually in response to a predatory bat overhead. This is not much different to a hush falling over a crowded room – most of the people there aren’t reacting directly to the distraction itself, but to the change in activity of those around them. The silence is an indicator that something important is happening.

listening in Gunthers dikdikGunther's dik-dik relies on less 'verticallly challenged' species to help it stay alert to predators in the distance. 
 

Whispers, secrets and lies

In human spycraft misdirection is a key strategy. We put out faulty information in the hopes of sending the enemy off on a wild goose chase or perhaps catching them in the act. Animals, too, know they are being spied upon and will work this to their advantage.

The birds that serve as sentinels in mixed-species flocks exploit the panicked responses to their alarm calls. While in many cases these calls are genuine signifiers of an approaching predator, birds such as fork-tailed drongos (Dicrurus adsimilis) and bluish-slate antshrikes (Thamnomanes schistogynus) will also issue false alarms that allow them to snap up food that has been abandoned by their panicked freeloading followers.

The effects of eavesdropping have entirely altered the habits of some animals. In forests frequented by bats, katydids issue shorter mating calls, believed to be an adaptation to the bats’ use of these calls to locate and devour them. Some species of katydid and cricket have actually shifted their calls from strings to percussion. Instead of stridulating, males thump the substrate – producing vibrations more targeted to female katydids and less easily detected by bats.

The arms race analogy is perhaps overused in discussing evolution, but it is particularly appropriate to the neotropical brown stink bug. Both males and females of the species drum their songs into the trees they inhabit in the hopes of keeping their trysts discreet. But parasitoid wasps have managed to tap into these tap-dancing duets. The females inadvertently signal the location of their eggs, which are injected with the wasp’s own progeny.

Somewhat more successfully, many species of bird modulate their mating and conflict calls to avoid attracting both predators and potential rivals. Birds such as the common blackbird (Turdus merula) and European robin (Erithacus rubecula) reduce their calls to much softer twittering when in close proximity to a mate or a territorial invader. These shorter songs are less likely to attract further rivals or predators that may see two posturing males as an easy meal.

Innate or learned?

Whether eavesdropping behaviour is innate or learned appears to depend on the species. There seems to be something tonally fundamental to these frightened cries and Australian birds have been observed reacting with urgency to the calls of North American species that they have never encountered.

In some cases, though, it does seem to be learned through experience – for example, in animals that only respond to the alarm calls of others where their ranges overlap. Such is the case with bonnet macaques (Macaca radiata) and two species of langur (Trachypithecus johnii and Semnopithecus entellus) that in some places share territory. And some species of antbirds that respond to one another’s calls on the mainland fail to do so on outlying islands where one or the other species is absent. This aptitude for learning in birds has been demonstrated even more clearly with a simple experiment. Researchers found that superb fairy wrens learned to associate a novel alarm call with a fake hawk gliding overhead in just two days.

The attentiveness of our animal cousins testifies eloquently to the sophistication of their communication networks. The twittering of the birds or the calling of the crickets in the evening may seem like simple, unidirectional messages. But the fact that these messages are intercepted is exactly due to their complexity. They signify danger or safety, availability or territoriality. Deep in our brains we know this already. We still know that when danger is imminent the birds take flight.

Richard Pallardy is a writer, researcher and editor with a particular interest in zoology, botany, evolution and conservation

Sources / further reading
1) Goodale, E. et al. Mixed-Species Groups of Animals Behavior: Community Structure, and Conservation 107–114 (Elsevier Science, 2017).
2) Haff, T. M. & Magrath, R. D. Learning to listen? Nestling response to heterospecific alarm calls. An. Behav. 84(6), 1401–1410 (2012).
3) Koob, G. (ed.) et al. Encyclopedia of Behavioral Neuroscience, 274 (Elsevier Science, 2010).
4) Magrath, R. D. et al. Eavesdropping on heterospecific alarm calls: from mechanisms to consequences. Biol. Rev. 90, 560–586 (2015).
5) Magrath, R. D. et al. Wild birds learn to eavesdrop on heterospecific alarm calls. Curr. Bio. 25(15), 2047–2050 (2015).
6) Ridley, A. R. et al. The ecological benefits of interceptive eavesdropping. Funct. Ecol. 28(1), 197–205 (2014).
7) Schmitt, M. H. et al. Zebra reduce predation risk in mixed-species herds by eavesdropping on cues from giraffe. Behav. Ecol. 27(4), 1073–1077 (2016).
8) Stevens, M. Sensory Ecology, Behaviour, and Evolution (OUP Oxford, 2013).