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The Art of Eavesdropping: Nature’s Silent Sniffers, Watchers and Listeners

The views expressed are those of the author and are not necessarily those of Scientific American.


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Typically we think of eavesdropping as a human endeavor. Individually we all do it to a certain degree. Call it social listening, if you will. Sometimes we can’t help but overhear a conversation. Other times we might deliberately try to listen in on what someone else is saying. I remember as a kid putting a cup up against the door to try and hear what was going on behind closed doors. Collectively as nations we eavesdrop on a massive scale, in times of peace and war. Currently, the military spends a considerable amount of money on ‘electronic intelligence’, so much so that there is an entire center devoted to eavesdropping: Menwith Hill in North Yorkshire.

We certainly did not invent this strategy of watching or listening in on others. Like most things, we’ve copied it from nature. Eavesdropping is ubiquitous across the animal kingdom. Whenever substantial time or resources are devoted to an activity there is usually a payoff to be found. This got me wondering, what is the payoff for eavesdropping?

Several advantages immediately come to mind. For example, perhaps you can increase your access to resources. One way to do this would be to avoid wasting time going after resources that someone else has already used up. This is frequently observed among competitors searching for similar resources. When one thinks of fierce competitors, two stingless bee species may not be the first thing that comes to mind.

Nevertheless, between two species of Trigona, the largest genus of stingless bees, Trigona hyalinata is able to increase its foraging efficiency (spend less energy/time looking for food) by avoiding visiting food sources that have been potentially depleted by the other species Trigona spinipes. Both species use pheremone (odor) trails to recruit others of their own species, but it appears that T. hyalinata detects and avoids the trails left by T. spinipes in order to not waste time on unprofitable resources.

Conversely, intercepting someone else’s signal could lead you to resources you might otherwise not know about, or would have to spend a considerable amount of time discovering on your own. Blatant thievery via eavesdropping is a common practice among animals, particularly among food-storing species.

Many rodents and birds store, or cache, their food. In general, if you have to store your food, it seems like a good idea to remember where you put it. Therefore we can predict that animals that put food in different locations will, at the very least, have superb spatial memory. Because of this, some animals also have the ability to find where others put their food, resulting in pilfering rates that can exceed 30%. This stealing is not limited to one’s own species, but often includes thievery between species that coexist in the same area.

The idea is obvious. Why not supplement your own stockpile and strike a blow to your competitor all in one fell swoop? Of course if you are the smaller of the two you might be able to hide your food in places that a larger competitor can’t get to and simultaneously steal their stash. For many rodents, it does seem as though the little guy does better in the robbing department. Pocket mice steal more from kangaroo rats than vice versa, yellow pine chipmunks find more of the larger golden-mantled ground squirrel’s cache sites, and the least chipmunk helps itself to more of the eastern chipmunks hidden food. The more interesting question, however, is how do these robbers find these caches?

In some cases, particularly rodents, it is frequently through smell. Unlike in the bee example, this would not really qualify as eavesdropping since the cacher is not deliberately leaving a scent for others to find. Instead it is tantamount to a kind of random search, except that there are some environmental cues giving you a hint. In most case then, you would be better off looking for food on your own rather than randomly searching around for where someone else hid their reserves. Unless, of course, you could somehow learn where they hid the food. In such situations, the would-be thief does eavesdrop by waiting and watching to see where the cacher plans to hide its food. This is widespread in the corvids, a group that includes ravens, pinyon jays, and the champion of cachers, the Clark’s nutcracker.

Ravens, known for their communication, problem solving abilities, and tool use, can add another specialty to their list: criminal mastermind. Since any reasonable individual would protect their stash, it would be advantageous to delay stealing someone else’s food so that you don’t have to engage in a direct confrontation (e.g., robbing the house when no one is home). Direct confrontation is costly unless you are dominant in some way, like the Somali warlords who sit and wait to intercept aid rations. A safer strategy for the majority of us is tactical deception.

While all corvids are known for their ridiculously fantastic spatial memory, ravens also watch where a competitor hides their food, wait a while, and then raid the cache after the individual doing the hiding leaves the area. Unlike other corvids that hide thousands of seeds over long periods of time (and also remember the location of where others hid their food), ravens hide valuable food on a more short-term basis. As a result, the one doing the watching tries to do so undetected, and the one doing the hiding tries to obfuscate the location of its treasure. As expected, countermeasures develop on both sides, much like the jamming and interception tactics developed by competing military operations. Overall, this ‘arms race’ for discovering information and preventing detection seen in ravens gives rise to one of the few examples of strategic or tactical deception in a nonprimate.

Certainly the value of a limiting resource like food lends itself to behavior such as eavesdropping, but what about other valuable resources? For a lot of animals out there, finding a mate involves a hard, long, drawn out battle. The fiddler crab has a lovely courtship approach. You have probably seen them along beaches or inter-tidal areas around salt marshes. The easiest way to recognize them is by the males, who have one large fiddle-shaped claw.

Sometimes these crab look like they are waving at you with their one big claw. Indeed the males are waving, not really at you, but at the females. This show-stopping waving action is designed to get the attention of, and impress, the female. Females are attracted to the rate at which a male is waving his claw, and faster is better. While it may get her attention, it also acts like a beacon to other males competing for her affections.

A recent study by Milner and colleagues found that male fiddler crabs eavesdrop on each other. If a male spots another male beginning to wave, he too starts waving. In addition, the eavesdropping male waves at a rate similar to the male who is in complete visual contact with the female. Thus, fiddler crab males use the signal of rivals to increase their chances of getting noticed by females. Similarly, male bush crickets will eavesdrop on a dueting pair and attempt to intercept the female, while the Broadley’s painted reed frog takes its cue, as in the case with fiddler crabs, from the calling of other males to determine when a female is around.

So far all of the examples have focused on avoiding depleted resources or gaining access to resources through clandestine means. In many more cases, and possibly more similar to what we, as humans do, eavesdropping is used to detect a potential threat. For example, in animal communication systems, alarm calls, once emitted, move into the ‘public domain’ creating an opportunity for others to intercept the call.

The challenge here is that to benefit from heterospecific alarm calls an eavesdropping species has to be able to interpret or decode the information sent out by the other species. In doing so, a species can garner several advantages, including 1) not having to spend their time watching for predators since they have a heterospecific sentinel system and 2) not having to produce their own alarm call, thereby revealing their location to the predator.

Of course for eavesdropping to evolve in a community, you need two species at risk from the same predator and one of the species must produce an alarm call. This form of threat eavesdropping has been documented in a wide range of species, including mammals, birds and lizards. It is especialy common in mixed-species groups of birds and social primates.

For instance, the superb fairy-wren likes to feed on the forest floor. This is a dangerous place to be. In some places superb fairy-wrens share the habitat with the noisy miner, a bird that forages in the canopy. Noisy miners are so named for their proclivity to be feisty and, well, noisy. They routinely attack, or mob, potential predators such as hawks. In addition to mobbing, they emit two different alarm calls, one when a raptor is in flight and one when the predator is perched or on the ground. Superb fairy-wrens have learned what the two alarm calls mean and by eavesdropping on noisy miners, they have a personal alarm system letting them know when its time to get out of dodge.

Aside from potential threats, eavesdropping might let you better discriminate between friend and foe, particularly if there is dishonesty afoot. In this way, being a ‘silent’ bystander can have a strong influence on your future willingness to cooperate. We can easily see how this is advantageous from a military perspective. Nations may appear to be allies, but eavesdropping can reveal divided loyalties. At a smaller scale, social eavesdropping can give individuals important information regarding their status or the willingness of others to share or be altruistic.

For example, little blue penguin males produce a ‘triumph’ display when they win a conflict against another male. When other males hear this call, not only are they less likely to instigate a fight with the winner, but they also have a stress reaction in response to all the fuss. This is similar to what was found in humans, where eavesdropping influenced the perceptions of dominance rank among men.

On the flip side, indirect evidence gained via eavesdropping can assist an individual in detecting cooperating versus cheating individuals. Sparrow males are aggressive with their neighbors until territories have been established. Once mating is underway it behooves both males to spare their energy and fight against strangers and not each other. Strategically this makes sense, but also sets up the potential for one male to not hold up his end of the bargain.

In other words, how can males determine if they should trust the truce reached? We have a saying that your ‘reputation’ precedes you and means everything, and it seems the same is true for sparrows. A given male will observe how his neighbor interacts with his neighbor’s neighbor. If he determines, through eavesdropping, that his neighbor is defecting from the peace treaty, he too will choose an aggressive strategy since he has observed, indirectly, that his neighbor is untrustworthy.

As with people, it has been reported that chimpanzees, client fish, and dogs may monitor interactions between two individuals to assess which individual is more altruistic and willing to cooperate. Though in the case of dogs, they can monitor the interaction between a pair of humans! Marshall-Pescini and colleagues examined whether, through social eavesdropping, dogs monitor, comprehend, and adjust their behavior when observing interactions between two people. Previous work had revealed that dogs console the loser in third-party interaction and also can tell if a person will make a good play partner based on watching that person interact with another dog. In this study dogs first observed a human begging for food from another human. The ‘selfish’ human gave no food to the ‘begging’ human, while the ‘generous’ human freely shared his/her food with the human asking for food.

The dogs were observed for their tendency to gaze at each of the players, and then tested to see if they preferentially approached the ‘selfish’ or ‘generous’ person in search of sausage. In the experimental group, dogs wasted no time with the ‘selfish human’. The dogs not only approached the generous food-sharer more frequently, but also interacted with them for significantly more time. Given that the humans were strangers, dogs used eavesdropping on a third-party interaction to gain valuable information about the likelihood that a particular person would share food with him or her. Not only do dogs have a better sense of smell than us, but also seem to be smarter about reading human behavior and intention than we sometimes are!

From the pheremone trails of stingless bees to the broadscale electronic surveillance undertaken by militaries around the world, it is clear that accessing information, particularly by indirect means via eavesdropping has adaptive benefits. The listener can avoid depleted resources, access additional resources, garner extra protection against predators, and determine their social status. In other social settings, both within and between species (e.g., humans-dog), where the interactions among indivduals are observed, assessing ones tendency to share, cooperate, or be fair may not only benefit the listener or observer, but could potentially discourage selfish behavior. On the other hand, countermeasures flourish in the presence of eavesdropping, so maybe all that listening just promotes more sophosticated deception.

Resources:

Akçay, C., Reed, V.A., Campbell, S.E., Templeton, C.N., Beecher, M.D. 2010. Indirect reciprocity: song sparrows distrust aggressive neighbours based on Eavesdropping. Animal Behaviour 80: 1041-1047. (doi:10.1016/j.anbehav.2010.09.009)

Bshary, R. & Grutter, A. S. 2006. Image scoring and cooperation in a cleaner fish mutualism. Nature, 441, 975-978.

Bugnyar, T. and Kotroschal, K. 2002. Observational learning and the raiding of food caches in ravens, Corvus corax: is it ‘tactical’ deception? Animal Behaviour 634:185-195. (doi:10.1006/anbe.2002.3056)

Dally, J. M., Clayton, N. S., & Emery, N. J. (2006). The behaviour and evolution of cache protection and pilferage. Animal Behaviour, 72, 13–23. (doi:10.1016/j.anbehav.2005.08.020)

Earley, R.L. 2010. Social eavesdropping and the evolution of conditional cooperation cheating strategies. Phil Trans R Soc B 365:2675-2686. (doi:10.1098/rstb.2010.0147)

Grodzinski, U. and Clayton, N.S. 2010. Problems faced by food-caching corvids and the evolution of cognitive solutions. Phil Trans R Soc B 365:977-987. (doi:10.1098/rstb.2009.0210)

Jones, B.C., DeBruine, L.M., Little, A.C., Watkins, C.D., Feinberg, D.R. 2011. ‘Eavesdropping’ and perceived male dominance rank in humans. Animal Behaviour 81:1203-1208. (doi:10.1016/j.anbehav.2011.03.003)

Leaver, L. A., L. Hopewell, C. Caldwell, and L. Mallarky. 2007. Audience effects on food caching in grey squirrels (Sciurus carolinensis): evidence for pilferage avoidance strategies. Animal Cognition 10:23–27.

Lichtenberg, E., Hrncir, M., Turatti, I.C., and Nieh, C. 2011. Olfactory eavesdropping between two competing stingless bee species. Behavioral Ecology and Sociobiology 65:763-774(doi:10.1007/s00265-010-1080-3)

Magrath, R.D. and Bennett, T.H. 2012. A micro-geography of fear: learning to eavesdrop on alarm calls of neighboring heterospecifics. Proc Royal Soc B 279:902-909. (doi:10.1098/rspb.2011.1362)

Marshall-Pescini, S. Passalacqua, C., Ferrario, A., Valsecchi, P., Prato-Previde, E. 2011. Social eavesdropping in the domestic dog. Animal Behaviour 81:1177-1183. (doi:10.1016/j.anbehav.2011.02.029)

Milner, R.N.C., Jennions. M.D., Backwell, P.R.Y. 2010. Eavesdropping in crabs: an agency for lady detection. Biology Letters 6:755-757. (doi:10.1098/rsbl.2010.0384)

Mouterde, S.C., Duganzich, D.M., Molles, L.E., Helps, S., Helps, F., Waas, J.R. 2010. Triumph displays inform eavesdropping little blue penguins of new dominance asymmetries. Animal Behaviour 83:605-611. (doi:10.1016/j.anbehav.2011.11.032)

Penner, J.L. and Davenport, L.D. 2011. A comparative study of cachin and pilfering behavior in two species, least chipmunks (Tamias minimus) and eastern chipmunks (Tamias striatus). Journal of Comparative Psychology, 125:375-384. (doi:10.1037/a0024562)

Subiaul, F., Vonk, J., Okamoto-Barth, S. & Barth, J. 2008. Do chimpanzees learn reputation by observation? Evidence from direct and indirect experience with generous and selfish strangers. Animal Cognition, 11, 611e623. Vander Wall, S. B., & Jenkins, S. H. (2003). Reciprocal pilferage and the evolution of food-hoarding behavior. Behavioral Ecology, 14, 656–667.

Images:

1. Raven by National Park Service at Wikimedia commons; 2. Fiddler crab by Ianaré Sévi at Wikimedia commons; 3. Superb fairy-wren by Cas Liber at Wikimedia commons.

 

Jennifer Verdolin About the Author: Jennifer Verdolin is a behavioral ecologist studying social and mating behavior. Her work has been featured in Science News and on National Public Radio. She is a postdoctoral researcher at the National Evolutionary Synthesis Center in Durham, NC. She is a co-author of Prairie dogs: Communication and community in an animal society (Harvard University Press), and is writing a new book on animal and human behavior. Follow on Twitter @JVerdolin.

The views expressed are those of the author and are not necessarily those of Scientific American.






Comments 3 Comments

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  1. 1. Alison Hill 10:45 am 05/11/2012

    I love the unique way the writer makes correlations between human and animal behavior, making it interesting and entertaining. This is a fascinating exploration of how animals utilize a strategy we think of as innately human to advance themselves. I will now view my fellow creatures a little differently. Thank you for this post!

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  2. 2. JadeMins 6:36 pm 05/11/2012

    I have a Dawn & Dusk (with occasional forays during the day) seed feeding on my footpath; Mr & Mrs Peewee (Magpie Lark) are the “telegraphers” to Cockatoos, peaceful doves, turtle doves, sparrows & noisy miners (often feeding in a mixed group); they (being the “other” species) differentiate between “food is here” & “Hooded Butcherbird is around” calls … I’ve noticed this before in 3 different locations over periods of 5 yrs or more in each. Sydney (NSW), SW Darling Downs & now in Cairns (Qld far north)covering various other mixed visitor groups & various other raptors. Mr & Mrs Peewee seem to be THE callers to listen to wherever you are ^_~

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  3. 3. Jerzy v. 3.0. 7:45 pm 05/11/2012

    Actually, many naturalists know that eavesdropping bird calls is a good way to see birds of prey, owls and carnivores. Also “pishing” is a method used by birdwatchers who mimic alarm call of tits/chickadees to see birds coming to investigate the call.

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