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

Abstract

Vertebrates that eavesdrop on heterospecific alarm calls must distinguish alarms from sounds that can safely be ignored, but the mechanisms for identifying heterospecific alarm calls are poorly understood. While vertebrates learn to identify heterospecific alarms through experience, some can also respond to unfamiliar alarm calls that are acoustically similar to conspecific alarm calls. We used synthetic calls to test the role of specific acoustic properties in alarm call identification by superb fairy-wrens, Malurus cyaneus. Individuals fled more often in response to synthetic calls with peak frequencies closer to those of conspecific calls, even if other acoustic features were dissimilar to that of fairy-wren calls. Further, they then spent more time in cover following calls that had both peak frequencies and frequency modulation rates closer to natural fairy-wren means. Thus, fairy-wrens use similarity in specific acoustic properties to identify alarms and adjust a two-stage antipredator response. Our study reveals how birds respond to heterospecific alarm calls without experience, and, together with previous work using playback of natural calls, shows that both acoustic similarity and learning are important for interspecific eavesdropping. More generally, this study reconciles contrasting views on the importance of alarm signal structure and learning in recognition of heterospecific alarms.

Figure 1.

Spectrograms of call elements. (a) Natural aerial alarm calls from species in three passerine families, including the Maluridae: superb fairy-wren (sufw), white-winged fairy-wren (wwfw), variegated fairy-wren (vafw); Acanthizidae: southern whiteface (stwf), chestnut-rumped thornbill (crtb), brown gerygone (bnge), white-browed scrubwren (wbsw); and Meliphagidae: New Holland honeyeater (nhhe). (b) Synthetic calls used in experiments 2 (4.1 and 11.1 kHz only), 3, 4 and 5. The mean peak frequency (PF, kHz) and mean frequency modulation rate (MR, Hz) is shown next to the natural call of each species [19]. The beginning of each element is aligned with the frequency modulation rate. Some elements are lighter in shade to distinguish calls that overlap. Spectrograms were produced in Raven Pro 1.3 [43] and set to Blackman window function, a temporal grid resolution of 0.295 ms with 94.9% overlap and a frequency grid resolution of 86.1 Hz.

Figure 2.

The results of experiment 2, showing the proportion of fairy-wrens immediately responding to synthetic calls varying in peak frequency (raw data; n = 10 for each column). Natural alarm calls of fairy-wrens (mean peak frequency: 9.1 kHz) and white-browed scrubwrens (mean peak frequency: 7.1 kHz) served as positive controls. Synthetic calls had fairy-wren base properties (see text). Synthetic crimson rosella contact calls, the neutral control, did not elicit any response and are not represented here. Black bars, fleeing; white bars, scanning.

Figure 3.

The results of experiment 3, showing the immediate response of fairy-wrens to synthetic aerial alarm calls varying in both peak frequency (PF) and frequency modulation rate (MR; n = 10 playbacks in each column; raw data shown): (a) the proportion of focal birds fleeing to cover or scanning; and (b) the observed mean (±s.e.) duration (s) the focal bird spent in cover before re-emerging. Natural fairy-wren alarm calls served as a positive control; synthetic calls had fairy-wren base properties (see text). Black bars, fleeing; white bars, scanning.

Figure 4.

The results of experiment 4, showing the immediate response of fairy-wrens to synthetic aerial alarm calls with very low frequency modulation rates (n = 10 for each column; raw data shown): (a) the proportion of focal birds fleeing to cover or scanning; and (b) the mean (±s.e.) duration (s) the focal bird spent in cover before re-emerging. Synthetic calls had fairy-wren base properties (see text). Black bars, fleeing; white bars, scanning.

Figure 5.

The results of experiment 5, showing the immediate response of superb fairy-wrens to natural and synthetic calls with the base properties of New Holland honeyeater alarm calls and varying in peak frequency (n = 12 for each column; raw data shown): (a) the proportion of focal birds fleeing to cover or scanning; and (b) the mean (±s.e.) duration (s) the focal bird spent in cover before re-emerging. Natural crimson rosella contact calls, the neutral control, did not elicit any response and are not shown here. Black bars, fleeing; white bars, scanning.