A micro-geography of fear: learning to eavesdrop on alarm calls of neighbouring heterospecifics

Abstract

Many vertebrates eavesdrop on alarm calls of other species, which is a remarkable ability, given geographical variation in community composition and call diversity within and among species. We used micro-geographical variation in community composition to test whether individuals recognize heterospecific alarm calls by: (i) responding to acoustic features shared among alarm calls; (ii) having innate responses to particular heterospecific calls; or (iii) learning specific alarm calls. We found that superb fairy-wrens (Malurus cyaneus) fled to cover to playback of noisy miner (Manorina melanocephala) aerial predator alarm calls only in locations where miners were present, suggesting that learning rather than acoustic structure determines response. Sites with and without miners were well within the dispersal distance of fairy-wrens, and philopatric males and dispersing females showed the same pattern, so that local genetic adaptation is extremely unlikely. Furthermore, where miners were present, fairy-wrens responded appropriately to different miner calls, implying eavesdropping on their signalling system rather than fleeing from miners themselves. Learned eavesdropping on alarm calls enables individuals to harvest ecologically relevant information from heterospecifics on an astonishingly fine spatial scale. Such phenotypic plasticity is valuable in a changing world, where individuals can be exposed to new species.

Alarming features: birds use specific acoustic properties to identify heterospecific alarm calls

“…This is despite fairy-wrens typically not responding to unfamiliar heterospecific alarm calls with peak frequencies lower than 7 kHz [19], and never responding to 4 kHz synthetic calls with the base properties of superb fairy-wren alarms (experiment 2). Additional evidence for learned recognition by fairy-wrens includes responding to the aerial alarm calls of noisy miners, another honeyeater with low-frequency alarm calls that lack frequency modulation, only in areas where they live closely with noisy miners [22]. Furthermore, fairywrens usually scanned rather than fleeing in response to honeyeater calls played in reverse (ascending frequency rather than descending frequency), even though reversed calls are similar in most acoustic properties, including peak frequency [20].…”

“…We presented 108 calls to 12 fairy-wren groups in Canberra over six weeks in January and February 2011. We made a counterintuitive and therefore strong prediction based on the previous experiments using synthetic calls and our work on learned recognition in fairy-wrens [20,22]. We predicted that as peak frequency increased from a natural honeyeater 4 kHz, fairy-wren responses would first decline but then increase as peak frequencies approached the natural fairy-wren 9 kHz.…”

“…¼ 4.0 + 0.23 kHz), much shorter duration (47.9 + 6.2 ms) and a declining tone with no frequency modulation (5.5 -3.1 kHz) [20]. Honeyeaters are common at the study site, where fairy-wrens respond strongly to honeyeater calls [20,27], almost certainly as a result of learning to recognize that they signal danger [20,22]. We generated synthetic calls with the base properties of honeyeater calls and peak frequencies of 3, 4, 5, 6, 7, 8 and 9 kHz (figure 1), with the 4 kHz version mimicking natural honeyeater calls.…”

Interspecific signalling between mutualists: food-thieving drongos use a cooperative sentinel call to manipulate foraging partners

“…For example, treehoppers provision ants with a carbohydraterich excretion, but also produce vibrational signals to elicit costly defence towards predators [4]. A similar protection benefit has been suggested for the numerous birds and mammals that form mixed-species foraging mutualisms to reduce predation risk [7,[12][13][14]. By eavesdropping on each other's alarm and sentinel calls, group members can reduce their own investment in antipredator vigilance and thereby increase time available for foraging [14][15][16].…”

Learning and signal copying facilitate communication among bird species

“…For example, despite divergence as a result of selection in other contexts, calls might include widely recognizable features [24], meaning calls are 'similar enough' across species for receivers to recognize them [25,26]. However, if divergence is too great for automatic recognition, repeated exposure could allow receivers to learn to associate the calls of other species with an appropriate alarm response [27,28]. Learning requires previous experience and, therefore, time to build up responses to the calls of another species [29], which may cause costly delays in alarm situations.…”