Moth Hearing, Defense, and Communication

Spangler, Hayward G.

doi:10.1146/annurev.en.33.010188.000423

Cited by 117 publications

(70 citation statements)

References 57 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…As the bat pups learned to fly and began to hunt, they were trained to capture tethered moths by using a commercially available pyralid moth, Galleria mellonella. Male G. mellonella use ultrasound in sexual communication when not flying, but they do not acoustically respond to bat attack (28). To eliminate any insectborne ultrasound from the naïve bat pups' environment, however, only female moths were used for training and experimentation.…”

Section: Methodsmentioning

confidence: 99%

Acoustic mimicry in a predator–prey interaction

Barber

Conner

2007

Proc. Natl. Acad. Sci. U.S.A.

110

105

View full text Add to dashboard Cite

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 ...

show abstract

Section: Methodsmentioning

confidence: 99%

Acoustic mimicry in a predator–prey interaction

Barber

Conner

2007

Proc. Natl. Acad. Sci. U.S.A.

110

105

View full text Add to dashboard Cite

show abstract

“…The most intensively studied of these are the two-celled ears of owlet moths (Noctuidae) (for reviews, see Roeder, 1967Roeder, , 1974Spangler, 1988;Hoy and Robert, 1996;Fullard, 1998) and in a series of classic papers, Roeder and his colleagues described the physiological responses of the noctuid A1 and A2 auditory cells as well as the apparently non-auditory B-cell. They proposed that noctuids respond to the approach of bats with a bimodal defensive flight behaviour determined by the closeness of the bat as perceived by the moth (Roeder, 1962(Roeder, , 1964(Roeder, , 1974.…”

mentioning

confidence: 99%

Auditory encoding during the last moment of a moth's life

Fullard

Dawson

Jacobs

2003

Journal of Experimental Biology

View full text Add to dashboard Cite

Many insects hear the ultrasonic echolocation calls of hunting insectivorous bats in time to allow them to escape predation (Hoy and Robert, 1996;Miller and Surlykke, 2001) and the ears of moths are amongst the most neurologically simple, containing up to four auditory receptors. The most intensively studied of these are the two-celled ears of owlet moths (Noctuidae) (for reviews, see Roeder, 1967Roeder, , 1974Spangler, 1988;Hoy and Robert, 1996;Fullard, 1998) and in a series of classic papers, Roeder and his colleagues described the physiological responses of the noctuid A1 and A2 auditory cells as well as the apparently non-auditory B-cell. They proposed that noctuids respond to the approach of bats with a bimodal defensive flight behaviour determined by the closeness of the bat as perceived by the moth (Roeder, 1962(Roeder, , 1964(Roeder, , 1974. Aerially foraging bats emit intense echolocation calls as they hunt and use a series of acoustic stages leading to prey capture (Griffin, 1958): (1) search, (2) approach, (3) tracking (Kick and Simmons, 1984), (4) terminal buzz (I) and (5) terminal buzz (II) (Surlykke and Moss, 2000). According to Roeder's (1974) model, the first stage (far-bat) of a flying moth's anti-bat response occurs when it directionally detects a distant bat in its search mode (i.e. emitting relatively faint and slowly repeated echolocation calls) with the most sensitive receptor, the A1 cell. Theoretically, the responses of the A1 cell then evoke controlled, directional flight that takes the moth away from the bat before the bat has detected the echo of the moth. The moth's second defensive mode (near-bat) occurs when it detects a close bat (i.e. emitting relatively intense and rapidly repeated echolocation calls). These sounds activate both the A1 cell and the less sensitive receptor, A2 cell, evoking erratic, non-directional flight as a 'last-ditch', anti-bat flight maneuver. In addition to the A2 cell, Lechtenberg (1971) suggested that the third noctuid receptor, the B cell, considered by earlier authors to be non-auditory (Roeder and Treat, 1957;Treat and Roeder, 1959), might identify the characteristic calls of the terminal stage of the bat's attack to evoke a sustained near-bat response in an escaping moth. The A2 cell has also been implicated in the activation of another near-bat defence, sound-production in the dogbane tiger moth, Cycnia tenera (Fullard, 1992;Dawson and Fullard, 1995). As a way of testing the bimodal theory, Roeder (1974) suggested observing the anti-bat behaviour of prominent moths (Notodontidae) whose ears each contain only the A1 receptor cell, and the subsequent study by Surlykke (1984) challenged the theory that near-bat The simple auditory system of noctuoid moths has long been a model for anti-predator studies in neuroethology, although these ears have rarely been experimentally stimulated by the sounds they would encounter from naturally attacking bats. We exposed the ears of five noctuoid moth species to the pre-recorded echolocation calls of an attacking bat...

show abstract

“…While bats emit highintensity ultrasonic pulses and use echoes to locate and track flying prey, some Arctiid moths can direct ultrasonic clicks back at the echolocating bat. The function of these clicks remains unclear; they may serve either to warn the bat that the moth is distasteful (Spangler 1988) or to jam its echolocating system (Fullard et al 1979), or perhaps both (Ratcliffe and Fullard 2005). In more general terms, the remarkable diversity in insect ears suggests that predator-prey interactions between bats and insects have played a key role in the evolution of insect auditory systems (Hoy and Robert 1996).…”

Section: Future Challenges Taking the Lab To The Fieldmentioning

confidence: 99%