Acoustic mimicry in a predator–prey interaction

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 Mü llerian 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.aposematism ͉ Arctiidae ͉ bats V isual mimicry has played an important role in evolutionary theory (1, 2) since Bates (3) and Müller (4) first proposed that mimics benefit through deception if they are palatable or through spreading the cost of educating predators if they are also noxious. Recent reviews of warning signals and mimicry (5, 6) make no mention of the acoustic domain despite the widespread use of sound as an aposematic signal in animals (7). Decades of anecdotal observations (8-12) have suggested acoustic mimicry among groups ranging from viperid snakes (12) to honey bees and droneflies (9). Perhaps the best studied of these is the purported model/mimic complex involving rattlesnakes and burrowing owls (13).Here, we report definitive experimental evidence for acoustic mimicry. Tiger moths answer the echolocation attack of bats with ultrasonic clicks broadcast from bilateral metathoracic structures called tymbals (Fig. 1) [to view the tymbal in action, see supporting information (SI) Movie 1]. Vigorous debate (14) over the functions of these sounds has produced three non-mutually exclusive hypotheses: startle, jamming, and warning. Although some evidence exists for both startle (15) and jamming (16,17) effects, recent work (18) confirmed one critical assumption of the warning model: naïve big brown bats (Eptesicus fuscus) failed to learn to avoid chemically protected moths unless those moths also provided an acoustic warning. Acoustic aposematism is a defensive strategy that is clearly open to mimicry.We trained naïve, lab-raised bats to hunt tethered moths, on the wing, in view of two high-speed video cameras, allowing three-dimensional visualization of interactions that occurred in fractions of a ...

Tempo and mode of antibat ultrasound production and sonar jamming in the diverse hawkmoth radiation

“…Many tiger moths are chemically defended and they use sounds to warn bats of their toxins (12,13,40). Hawkmoths do not appear to sequester plant toxins in their adult tissues (41), are known to be palatable to birds (42), and we have confirmed they are palatable to bats (Table S1).…”

“…Alternatively, if the moth sounds startle bats, the predators should initially be deterred but habituate over time. If moths are warning bats of distasteful toxins, bats should initially capture and drop moths, then learn to avoid them (12,13). We paired these laboratory experiments with high-throughput behavioral field assays and used genetic Significance Ultrasound production is one of the most sophisticated antibat strategies in nocturnal insects, yet it has never been thoroughly studied in a phylogenetic framework.…”

“…Tiger moths can hear bat echolocation and have paired metathoracic tymbals that beam ultrasonic clicks back at bats (6,7). The sounds that these moths make can startle bats (11), warn them of bad taste (12,13), and jam bat sonar (14)(15)(16). Jamming likely functions to confuse the bat because it interferes with the bat's perception of its own echoes that are reflecting off of its prey (16,17).…”

Biological insight into design against crime

“…Prey gain their greatest selective advantage when predators have already experienced similar signals [22]. Many researchers have investigated the benefits of mimics, which promotes deception if the organisms are palatable or through spreading the cost of educating predators if they are also noxious [25]. Some species use shields, which vary in appearance www.witpress.…”

Crying wolf to a predator: deceptive vocal mimicry by a bird protecting young

“…Mimicry is another classic example of a dishonest signal and is often used by otherwise undefended organisms to deceive predators into misidentifying them as toxic or dangerous species (defensive mimicry [3]). This is generally accomplished by mimicking attributes of dangerous models, including predators themselves, or the aposematic coloration or warning sounds of noxious prey (Batesian mimicry [1,[4][5][6]). However, mimicking dangerous species is not always possible, and it is unknown whether mimicking harmless species can provide protection against predators.…”