Tiger moths and the threat of bats: decision-making based on the activity of a single sensory neuron

Echolocating bats and eared moths are a model system of predator–prey interaction within an almost exclusively auditory world. Through selective pressures from aerial-hawking bats, noctuoid moths have evolved simple ears that contain one to two auditory neurons and function to detect bat echolocation calls and initiate defensive flight behaviours. Among these moths, some chemically defended and mimetic tiger moths also produce ultrasonic clicks in response to bat echolocation calls; these defensive signals are effective warning signals and may interfere with bats'' ability to process echoic information. Here, we demonstrate that the activity of a single auditory neuron (the A1 cell) provides sufficient information for the toxic dogbane tiger moth, Cycnia tenera, to decide when to initiate defensive sound production in the face of bats. Thus, despite previous suggestions to the contrary, these moths'' only other auditory neuron, the less sensitive A2 cell, is not necessary for initiating sound production. However, we found a positive linear relationship between combined A1 and A2 activity and the number of clicks the dogbane tiger moth produces.     

Acoustic Aposematism and Evasive Action in Select Chemically Defended Arctiine (Lepidoptera: Erebidae) Species: Nonchalant or Not?

Tiger moths (Erebidae: Arctiinae) have experienced intense selective pressure from echolocating, insectivorous bats for over 65 million years. One outcome has been the evolution of acoustic signals that advertise the presence of toxins sequestered from the moths’ larval host plants, i.e. acoustic aposematism. Little is known about the effectiveness of tiger moth anti-bat sounds in their natural environments. We used multiple infrared cameras to reconstruct bat-moth interactions in three-dimensional (3-D) space to examine how functional sound-producing organs called tymbals affect predation of two chemically defended tiger moth species: Pygarctia roseicapitis (Arctiini) and Cisthene martini (Lithosiini). P. roseicapitis and C. martini with intact tymbals were 1.8 and 1.6 times less likely to be captured by bats relative to those rendered silent. 3-D flight path and acoustic analyses indicated that bats actively avoided capturing sound-producing moths. Clicking behavior differed between the two tiger moth species, with P. roseicapitis responding in an earlier phase of bat attack. Evasive flight behavior in response to bat attacks was markedly different between the two tiger moth species. P. roseicapitis frequently paired evasive dives with aposematic sound production. C. martini were considerably more nonchalant and employed evasion in fewer interactions. Our results show that acoustic aposematism is effective at deterring bat predation in a natural context and that this strategy is likely to be the ancestral function of tymbal organs within the Arctiinae.     

Anti-bat tiger moth sounds: Form and function

The night sky is the venue of an ancient acoustic battle between echolocating bats and their insect prey. Many tiger moths (Lepidoptera: Arctiidae) answer the attack calls of bats with a barrage of high frequency clicks. Some moth species use these clicks for acoustic aposematism and mimicry, and others for sonar jamming, however, most of the work on these defensive functions has been done on individual moth species. We here analyze the diversity of structure in tiger moth sounds from 26 spe-cies collected at three locations in North and South America. A principal components analysis of the anti-bat tiger moth sounds reveals that they vary markedly along three axes: (1) frequency, (2) duty cycle (sound production per unit time) and frequency modulation, and (3) modulation cycle (clicks produced during flexion and relaxation of the sound producing tymbal) structure. Tiger moth species appear to cluster into two distinct groups: one with low duty cycle and few clicks per modulation cycle that supports an acoustic aposematism function, and a second with high duty cycle and many clicks per modulation cycle that is con-sistent with a sonar jamming function. This is the first evidence from a community-level analysis to support multiple functions for tiger moth sounds. We also provide evidence supporting an evolutionary history for the development of these strategies. Further-more, cross-correlation and spectrogram correlation measurements failed to support a "phantom echo" mechanism underlying sonar jamming, and instead point towards echo interference.     

Male courtship ultrasound produced by mesothoracic tymbal organs in the yellow peach moth <Emphasis Type="Italic">Conogethes punctiferalis</Emphasis> (Lepidoptera: Crambidae)

Insect sound-producing apparatuses are mostly classified into two types: file–scraper and tymbal. Structures and locations of these organs are conserved in some phylogenetic groups, e.g., crickets, grasshoppers, and cicadas. However, moths have evolved diversified sound-producing organs, such as wing castanets and proboscis, in addition to the file–scraper and tymbal, in each species. Here we demonstrate that the yellow peach moth Conogethes punctiferalis (Guenée) (Lepidoptera: Crambidae) has developed mesothoracic tymbal organs never reported so far in insects. Tymbals are male specific and used for generating ultrasonic clicks in mating. We found eight to nine striae on the smooth surface of the tymbal membrane, suggesting the production of several clicks by a single buckle of the membrane in association with contraction/relaxation of the mesothoracic muscles. Acoustic data from click sequences support the idea that the series is generated by side-to-side asynchrony with an active/passive half cycle by an inward/outward buckle, and thus in click group (pulse) production, males emit 28 clicks with the right and left tymbals. The click-producing mechanism is similar, but not homologous, to those of other clicking species in five moth families. Thus, moths have acquired tymbal organs through independent and convergent evolution.     

Cephalic influences on a defensive behaviour in the dogbane tiger moth, Cycnia tenera

ABSTRACT. The dogbane tiger moth ( Cycnia tenera Hübner; Arctiidae) responds to ultrasonic, artificial bat echolocation signals by emitting stereotyped trains of high-frequency, rapidly repeated clicks. By comparing this response in intact and headless moths, the role of protocerebral auditory inter-neurones suggested by other studies was examined. Individual moths were tested intact and decapitated, and their response differences analysed. Response latency and threshold (dB) did not alter with the removal of the head but response duration and responsiveness to stimulus trains were significantly reduced in headless moths. These data are interpreted as suggesting the existence of a reflex arc connecting the moth's tympanic organ (ear) with its sound-producing structure (tymbal), and as providing preliminary evidence that the role of higher-order interneurones is primarily that of response reinforcement.     

Double meaning of courtship song in a moth

Males use courtship signals to inform a conspecific female of their presence and/or quality, or, alternatively, to ‘cheat’ females by imitating the cues of a prey or predator. These signals have the single function of advertising for mating. Here, we show the dual functions of the courtship song in the yellow peach moth, Conogethes punctiferalis, whose males generate a series of short pulses and a subsequent long pulse in a song bout. Repulsive short pulses mimic the echolocation calls of sympatric horseshoe bats and disrupt the approach of male rivals to a female. The attractive long pulse does not mimic bat calls and specifically induces mate acceptance in the female, who raises her wings to facilitate copulation. These results demonstrate that moths can evolve both attractive acoustic signals and repulsive ones from cues that were originally used to identify predators and non-predators, because the bat-like sounds disrupt rivals, and also support a hypothesis of signal evolution via receiver bias in moth acoustic communication that was driven by the initial evolution of hearing to perceive echolocating bat predators.     

Listening for bats: pulse repetition rate as a cue for a defensive behavior inCycnia tenera (Lepidoptera:Arctiidae)

Summary The tympanate, arctiid moth,Cycnia tenera responds to pulsed, 30 kHz acoustic stimuli resembling bat echolocation signals by emitting trains of clicks. This phonoresponse was used to determine that this moth is maximally sensitive to stimulus pulse repetition rates of 30–50 pulses/s, rates typically emitted by bats shortly before they close with their targets. At rates both above and below this optimum moths exhibit higher thresholds and reduced responsiveness. These data suggest thatC. tenera is capable of using the repetition rate emitted by an approaching bat as a cue in determining the relative proximity of the bat. The use of repetition rate information should allow this moth both an unambiguous indication of a bat at very close range as well as the ability to distinguish sources of nocturnal, high-frequency sounds not emitted by predators.     

To females of a noctuid moth,male courtship songs are nothing more than bat echolocation calls

It has been proposed that intraspecific ultrasonic communication observed in some moths evolved, through sexual selection, subsequent to the development of ears sensitive to echolocation calls of insectivorous bats. Given this scenario, the receiver bias model of signal evolution argues that acoustic communication in moths should have evolved through the exploitation of receivers'' sensory bias towards bat ultrasound. We tested this model using a noctuid moth Spodoptera litura, males of which were recently found to produce courtship ultrasound. We first investigated the mechanism of sound production in the male moth, and subsequently the role of the sound with reference to the female''s ability to discriminate male courtship songs from bat calls. We found that males have sex-specific tymbals for ultrasound emission, and that the broadcast of either male songs or simulated bat calls equally increased the acceptance of muted males by the female. It was concluded that females of this moth do not distinguish between male songs and bat calls, supporting the idea that acoustic communication in this moth evolved through a sensory exploitation process.     

Female greater wax moths reduce sexual display behavior in relation to the potential risk of predation by echolocating bats

Female greater wax moths Galleria mellonella display by wing fanning in response to bursts of ultrasonic calls produced bymales. The temporal and spectral characteristics of these callsshow some similarities with the echolocation calls of batsthat emit frequency-modulated (FM) signals. Female G. mellonellatherefore need to distinguish between the attractive signalsof male conspecifics, which may lead to mating opportunities,and similar sounds made by predatory bats. We therefore predictedthat (1) females would display in response to playbacks of male calls; (2) females would not display in response to playbacksof the calls of echolocating bats (we used the calls of Daubenton'sbat Myotis daubentonii as representative of a typical FM echolocatingbat); and (3) when presented with male calls and bat callsduring the same time block, females would display more whenperceived predation risk was lower. We manipulated predationrisk in two ways. First, we varied the intensity of bat callsto represent a nearby (high risk) or distant (low risk) bat.Second, we played back calls of bats searching for prey (lowrisk) and attacking prey (high risk). All predictions weresupported, suggesting that female G. mellonella are able todistinguish conspecific male mating calls from bat calls, andthat they modify display rate in relation to predation risk.The mechanism (s) by which the moths separate the calls ofbat and moth must involve temporal cues. Bat and moth signalsdiffer considerably in duration, and differences in durationcould be encoded by the moth's nervous system and used in discrimination.     

Impact of predation by a cave-dwelling bat, Rhinolophus ferrumequinum, on the diapausing population of a troglophilic moth, Goniocraspidum preyeri

The predation pressure of the greater horseshoe bat, Rhinolophus ferrumequinum, on the diapausing population of the noctuid moth, Goniocraspidum preyeri, was examined at an abandoned mine in central Japan. These bats did not prey on the moths in summer. The number of moths preyed on was largest in March. More than 60% of the diapausing moths were eaten by only three or four bats, which accounted for over 90% of all the moth deaths. This moth was an important source of food at the end of the hibernating period when the bat had already used most of its stored subcutaneous fat. The predation on G. preyeri may have raised the overwintering success rate of R. ferrumequinum.     

Keeping up with bats: dynamic auditory tuning in a moth

Many night-flying insects evolved ultrasound sensitive ears in response to acoustic predation by echolocating bats . Noctuid moths are most sensitive to frequencies at 20-40 kHz , the lower range of bat ultrasound . This may disadvantage the moth because noctuid-hunting bats in particular echolocate at higher frequencies shortly before prey capture and thus improve their echolocation and reduce their acoustic conspicuousness . Yet, moth hearing is not simple; the ear's nonlinear dynamic response shifts its mechanical sensitivity up to high frequencies. Dependent on incident sound intensity, the moth's ear mechanically tunes up and anticipates the high frequencies used by hunting bats. Surprisingly, this tuning is hysteretic, keeping the ear tuned up for the bat's possible return. A mathematical model is constructed for predicting a linear relationship between the ear's mechanical stiffness and sound intensity. This nonlinear mechanical response is a parametric amplitude dependence that may constitute a feature common to other sensory systems. Adding another twist to the coevolutionary arms race between moths and bats, these results reveal unexpected sophistication in one of the simplest ears known and a novel perspective for interpreting bat echolocation calls.     

Numerical and Functional Responses of Forest Bats to a Major Insect Pest in Pine Plantations

Global change is expected to modify the frequency and magnitude of defoliating insect outbreaks in forest ecosystems. Bats are increasingly acknowledged as effective biocontrol agents for pest insect populations. However, a better understanding is required of whether and how bat communities contribute to the resilience of forests to man- and climate-driven biotic disturbances. We studied the responses of forest insectivorous bats to a major pine defoliator, the pine processionary moth pityocampa, which is currently expanding its range in response to global warming. We used pheromone traps and ultrasound bat recorders to estimate the abundance and activity of moths and predatory bats along the edge of infested pine stands. We used synthetic pheromone to evaluate the effects of experimentally increased moth availability on bat foraging activity. We also evaluated the top-down regulation of moth population by estimating T. pityocampa larval colonies abundance on the same edges the following winter. We observed a close spatio-temporal matching between emergent moths and foraging bats, with bat activity significantly increasing with moth abundance. The foraging activity of some bat species was significantly higher near pheromone lures, i.e. in areas of expected increased prey availability. Furthermore moth reproductive success significantly decreased with increasing bat activity during the flight period of adult moths. These findings suggest that bats, at least in condition of low prey density, exhibit numerical and functional responses to a specific and abundant prey, which may ultimately result in an effective top-down regulation of the population of the prey. These observations are consistent with bats being useful agents for the biocontrol of insect pest populations in plantation forests.     

Adaptive auditory risk assessment in the dogbane tiger moth when pursued by bats

Moths and butterflies flying in search of mates risk detection by numerous aerial predators; under the cover of night, the greatest threat will often be from insectivorous bats. During such encounters, the toxic dogbane tiger moth, Cycnia tenera uses the received intensity, duration and emission pattern of the bat''s echolocation calls to determine when, and how many, defensive ultrasonic clicks to produce in return. These clicks, which constitute an acoustic startle response, act as warning signals against bats in flight. Using an integrated test of stimulus generalization and dishabituation, here we show that C. tenera is able to discriminate between the echolocation calls characteristic of a bat that has only just detected it versus those of a bat actively in pursuit of it. We also show that C. tenera habituates more profoundly to the former stimulus train (‘early attack’) than to the latter (‘late attack’), even though it was initially equally responsive to both stimuli. Matched sensory and behavioural data indicate that reduced responsiveness reflects habituation and is not merely attributable to sensory adaptation or motor fatigue. In search of mates in the face of bats, C. tenera''s ability to discriminate between attacking bats representing different levels of risk, and to habituate less so to those most dangerous, should function as an adaptive cost–benefit trade-off mechanism in nature.     

Moth wing scales slightly increase the absorbance of bat echolocation calls

Coevolutionary arms races between predators and prey can lead to a diverse range of foraging and defense strategies, such as countermeasures between nocturnal insects and echolocating bats. Here, we show how the fine structure of wing scales may help moths by slightly increasing sound absorbance at frequencies typically used in bat echolocation. Using four widespread species of moths and butterflies, we found that moth scales are composed of honeycomb-like hollows similar to sound-absorbing material, but these were absent from butterfly scales. Micro-reverberation chamber experiments revealed that moth wings were more absorbent at the frequencies emitted by many echolocating bats (40-60 kHz) than butterfly wings. Furthermore, moth wings lost absorbance at these frequencies when scales were removed, which suggests that some moths have evolved stealth tactics to reduce their conspicuousness to echolocating bats. Although the benefits to moths are relatively small in terms of reducing their target strengths, scales may nonetheless confer survival advantages by reducing the detection distances of moths by bats by 5-6%.     

Support for the allotonic frequency hypothesis in an insectivorous bat community

The allotonic frequency hypothesis proposes that certain insectivorous bat species can prey upon moths that can hear bat echolocation calls by using echolocation frequencies outside the sensitivity range of moth ears. The hypothesis predicts that the peak frequencies of bat echolocation calls are correlated with the incidence of moths in the diets of these bats. The aim of this study was to test this prediction on a bat community dominated by bats using low duty cycle echolocation calls, i.e. aerial foraging, insectivorous species using frequency modulated calls. The community consisted of nine species, two molossids, Sauromys petrophillus and Tadarida aegyptiaca, five vespertilionids, Eptesicus capensis, Eptesicus hottentotus, Miniopteris schreibersii, Myotis tricolor, and Myotis lesueuri, one rhinolophid, Rhinolophus clivosus, and one nycterid, Nycteris thebaica. The insect fauna in the habitat used by the bat community was suited to the testing of the allotonic frequency hypothesis because more than 90% of the moths comprising the insect fauna were tympanate. These included Pyralidae (3.8%), Geometridae (44.9%), Notodontidae (3.8%), Arctiidae (4.6%), Lymantriidae (0.8%) and Noctuidae (32.4%). As predicted, peak echolocation frequency was correlated with the incidence of moths in the diets of these nine species (r=0.98, df=7, P<0.01). Furthermore, multivariate analysis revealed that echolocation frequency (t=9.91, n=129, P<0.001) was a better predictor of diet than forearm length (t=5.51, n=129, P<0.001) or wing area (t=-3.41, n=129, P<0.001). This suggests that the selection pressure exerted by moth hearing might have acted directly on call frequency and secondarily on body size and wing morphology, as part of the same adaptive complex. It is unlikely that dietary differences were due to temporal and spatial differences in the availability of prey because the pattern of differences in skull morphology of the nine species supported our dietary analyses. The skull morphology of a bat represents a historical record of the kind of diet it has become adapted to over its evolutionary history. These results suggest that prey defences may mediate other factors structuring bat communities, e.g. competition. Competition may be reduced for those species of bats that can circumvent prey defences.     

Auditory sensitivity of Hawaiian moths (Lepidoptera: Noctuidae) and selective predation by the Hawaiian hoary bat (Chiroptera: Lasiurus cinereus semotus).

The islands of Hawai'i offer a unique opportunity for studying the auditory ecology of moths and bats since this habitat has a single species of bat, the Hawaiian hoary bat (Lasiurus cinereus semotus), which exerts the entire predatory selection pressure on the ears of sympatric moths. I compared the moth wings discarded by foraging bats with the number of surviving moths on the island of Kaua'i and concluded that the endemic noctuid Haliophyle euclidias is more heavily preyed upon than similar-sized endemic (e.g. Agrotis diplosticta) and adventive (Agrotis ipsilon and Pseudaletia unipuncta) species. Electrophysiological examinations indicated that, compared with species less preyed upon, H. euclidias has lower auditory sensitivities to the bat's social and echolocation calls, which will result in shorter detection distances of the bat. The poor ears of H. euclidias suggest that this moth coevolved with the bat using non-auditory defences that resulted in auditory degeneration. This moth now suffers higher predation because it is drawn away from its normal habitat by the man-made lights that are exploited by the bat.     

The role of prey-generated sounds,vision, and echolocation in prey localization by the African batCardioderma cor (Megadermatidae)

Summary Cardioderma cor responded with head movements and flight toward speakers broadcasting calls of frogs and crickets which contained only sonic frequencies. Unlike the frog-eating bat,Trachops cirrhosus, they did not make contact with the speakers. Prey movements that generated sonic and ultrasonic sounds were both sufficient and necessary for the bats to localize and capture prey. Prey dragged across a glass sheet with a thin layer of water did not generate sounds and bats did not attempt to capture these prey, even with the availability of visual and echolocation cues. There was no evidence for the use of visual cues while hunting; bats did not localize prey more readily in light than darkness. Prey were presented such that their movements initially generated sounds, but then the prey moved onto the water layer of the glass sheet and sounds were eliminated. The bats emitted echolocation signals while hunting in this situation; however, the information from these signals was not utilized. The bats landed at the site that prey last made sound. These results demonstrate the importance of passive hearing for prey localization in this bat, and further suggest that when preygenerated sounds and echolocation signals offer conflicting information the bat's behavior is guided by the former.     

Prey pursuit strategy of Japanese horseshoe bats during an in-flight target-selection task

The prey pursuit behavior of Japanese horseshoe bats (Rhinolophus ferrumequinum nippon) was investigated by tasking bats during flight with choosing between two tethered fluttering moths. Echolocation pulses were recorded using a telemetry microphone mounted on the bat combined with a 17-channel horizontal microphone array to measure pulse directions. Flight paths of the bat and moths were monitored using two high-speed video cameras. Acoustical measurements of returning echoes from fluttering moths were first collected using an ultrasonic loudspeaker, turning the head direction of the moth relative to the loudspeaker from 0° (front) to 180° (back) in the horizontal plane. The amount of acoustical glints caused by moth fluttering varied with the sound direction, reaching a maximum at 70°–100° in the horizontal plane. In the flight experiment, moths chosen by the bat fluttered within or moved across these angles relative to the bat’s pulse direction, which would cause maximum dynamic changes in the frequency and amplitude of acoustical glints during flight. These results suggest that echoes with acoustical glints containing the strongest frequency and amplitude modulations appear to attract bats for prey selection.     

High duty cycle pulses suppress orientation flights of crambid moths

Bat-and-moth is a good model system for understanding predator–prey interactions resulting from interspecific coevolution. Night-flying insects have been under predation pressure from echolocating bats for 65 Myr, pressuring vulnerable moths to evolve ultrasound detection and evasive maneuvers as counter tactics. Past studies of defensive behaviors against attacking bats have been biased toward noctuoid moth responses to short duration pulses of low-duty-cycle (LDC) bat calls. Depending on the region, however, moths have been exposed to predation pressure from high-duty-cycle (HDC) bats as well. Here, we reveal that long duration pulse of the sympatric HDC bat (e.g., greater horseshoe bat) is easily detected by the auditory nerve of Japanese crambid moths (yellow peach moth and Asian corn borer) and suppress both mate-finding flights of virgin males and host-finding flights of mated females. The hearing sensitivities for the duration of pulse stimuli significantly dropped non-linearly in both the two moth species as the pulse duration shortened. These hearing properties support the energy integrator model; however, the threshold reduction per doubling the duration has slightly larger than those of other moth species hitherto reported. And also, Asian corn borer showed a lower auditory sensitivity and a lower flight suppression to short duration pulse than yellow peach moth did. Therefore, flight disruption of moth might be more frequently achieved by the pulse structure of HDC calls. The combination of long pulses and inter-pulse intervals, which moths can readily continue detecting, will be useful for repelling moth pests.