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, 104 (22), 9331-4

Acoustic Mimicry in a Predator-Prey Interaction

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Acoustic Mimicry in a Predator-Prey Interaction

Jesse R Barber et al. Proc Natl Acad Sci U S A.

Abstract

Mimicry of visual warning signals is one of the keystone concepts in evolutionary biology and has received substantial research attention. By comparison, acoustic mimicry has never been rigorously tested. Visualizing bat-moth interactions with high-speed, infrared videography, we provide empirical evidence for acoustic mimicry in the ultrasonic warning sounds that tiger moths produce in response to echolocating bats. Two species of sound-producing tiger moths were offered successively to naïve, free-flying red and big brown bats. Noctuid and pyralid moth controls were also offered each night. All bats quickly learned to avoid the noxious tiger moths first offered to them, associating the warning sounds with bad taste. They then avoided the second sound-producing species regardless of whether it was chemically protected or not, verifying both Müllerian and Batesian mimicry in the acoustic modality. A subset of the red bats subsequently discovered the palatability of the Batesian mimic, demonstrating the powerful selective force these predators exert on mimetic resemblance. Given these results and the widespread presence of tiger moth species and other sound-producing insects that respond with ultrasonic clicks to bat attack, acoustic mimicry complexes are likely common components of the acoustic landscape.

Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1.
Fig. 1.
Tiger moth acoustic mimicry complex. (A) Scanning electron micrographs of the tiger moths' sound-producing structures (tymbals) used in this study. Some scales were removed for clarity. (Reference bars: 1 mm.) (B) Example spectrograms (kilohertz × time) and power spectra (kilohertz × amplitude) of each species call. See ref. for species averages. Note that each call comprises two groups of clicks. The first group is produced as the tymbal is actively pulled inward along the striated band. The second group is produced as the tymbal passively returns to its resting state (see SI Movie 1). (C) A C. tenera tiger moth responding to an L. borealis echolocation attack. Notice that the tiger moth calls start just after the third echolocation cry. The moth calls appear to be different from B because of overlap created by asynchronous activity between the paired tymbals.
Fig. 2.
Fig. 2.
Müllerian mimicry comparison. Black lines are E. fuscus (n = 5), and red lines are L. borealis (n = 2). Solid lines graph the percentage of tiger moths captured. Dashed lines chart the percentage of noctuid novelty controls captured. See Materials and Methods for details. Vertical dotted lines indicate tiger moth changes illustrated below the figure. Beside each moth's image are oscillogram (time × relative amplitude) traces of its call. (Scale bars: 10 msec.) Asterisks above day 5 indicate statistical significance when comparing day 1 with 5, and those above day 11 specify a significant difference between days 10 and 11. Data are mean ± SD. It is important to note that the low percentage of moths captured on night 1, in both Müllerian (this figure) and Batesian (Fig. 3) comparisons, was due both to an initial startle response in which the first sound-producing moth was often avoided and to frequent one-trial learning of the aposematic signal.
Fig. 3.
Fig. 3.
Batesian mimicry comparison. See Fig. 2 legend for graph details. (A) All bats used in the Batesian contrast (E. fuscus, n = 3; L. borealis, n = 7). The vertical dotted line indicates a tiger moth change from C. tenera to E. egle. (B) Bats that were deceived by the Batesian mimic (E. fuscus, n = 3; L. borealis, n = 4). Vertical dotted lines indicate tiger moth changes from C. tenera to E. egle and then to E. egle with tymbals ablated. (C) Three L. borealis that discovered the Batesian mimic, graphed individually. Vertical dotted lines indicate tiger moth changes illustrated below the panel. Data are means ± SD.

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