Extinction of the acoustic startle response in moths endemic to a bat-free habitat

Most moths use ears solely to detect the echolocation calls of hunting, insectivorous bats and evoke evasive flight manoeuvres. This singularity of purpose predicts that this sensoribehavioural network will regress if the selective force that originally maintained it is removed. We tested this with noctuid moths from the islands of Tahiti and Moorea, sites where bats have never existed and where an earlier study demonstrated that the ears of endemic species resemble those of adventives although partially reduced in sensitivity. To determine if these moths still express the anti-bat defensive behaviour of acoustic startle response (ASR) we compared the nocturnal flight times of six endemic to six adventive species in the presence and absence of artificial bat echolocation sounds. Whereas all of the adventive species reduced their flight times when exposed to ultrasound, only one of the six endemic species did so. These differences were significant when tested using a phylogenetically based pairwise comparison and when comparing effect sizes. We conclude that the absence of bats in this habitat has caused the neural circuitry that normally controls the ASR behaviour in bat-exposed moths to become decoupled from the functionally vestigial ears of endemic Tahitian moths.     

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.     

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.     

The auditory system of non-calling grasshoppers (Melanoplinae: Podismini) and the evolutionary regression of their tympanal ears

Reduction of tympanal hearing organs is repeatedly found amongst insects and is associated with weakened selection for hearing. There is also an associated wing reduction, since flight is no longer required to evade bats. Wing reduction may also affect sound production. Here, the auditory system in four silent grasshopper species belonging to the Podismini is investigated. In this group, tympanal ears occur but sound signalling does not. The tympanal organs range from fully developed to remarkably reduced tympana. To evaluate the effects of tympanal regression on neuronal organisation and auditory sensitivity, the size of wings and tympana, sensory thresholds and sensory central projections are compared. Reduced tympanal size correlates with a higher auditory threshold. The threshold curves of all four species are tuned to low frequencies with a maximal sensitivity at 3–5 kHz. Central projections of the tympanal nerve show characteristics known from fully tympanate acridid species, so neural elements for tympanal hearing have been strongly conserved across these species. The results also confirm the correlation between reduction in auditory sensitivity and wing reduction. It is concluded that the auditory sensitivity of all four species may be maintained by stabilising selective forces, such as predation.     

Auditory input to motor neurons of the dorsal longitudinal flight muscles in a noctuid moth (Barathra brassicae L.)

Summary Motor neurons innervating the dorsal longitudinal muscles of a noctuid moth receive synaptic input activated by auditory stimuli. Each ear of a noctuid moth contains two auditory neurons that are sensitive to ultrasound (Fig. 1). The ears function as bat detectors. Five pairs of large motor neurons and three pairs of small motor neurons found in the pterothoracic ganglia innervate the dorsal longitudinal (depressor) muscles of the mesothorax (Figs. 2 to 5). In non-flying preparations the motor neurons receive no oscillatory synaptic input. Synaptic input to a cell resulting from ultrasonic stimulation is consistent and can be either depolarizing or hyperpolarizing (Figs. 6 to 9). Quiescent neurons only rarely fire a spike in response to auditory inputs. Motor neurons in flying preparations receive oscillatory synaptic drive from the flight pattern generator and usually fire a spike for each wingbeat cycle (Figs. 10 to 12). Ultrasonic stimulation can provide augmented synaptic drive causing a neuron to fire two spikes per wingbeat cycle thus increasing flight vigor (Fig. 11). The same stimulus presented on another occasion can also inhibit spiking in the same motor neuron, but the rhythmic drive remains (Fig. 12). Thus, when the flight oscillator is running auditory stimuli can modulate neuronal responses in different ways depending on some unknown state of the nervous system. Sound intensity is the only stimulus parameter essential for activating the auditory pathway to these motor neurons. The intensity must be sufficient to excite two or three auditory neurons. The significance of these responses in relation to avoidance behavior to bats is discussed.     

坝上地区不同海拔农田和恢复半自然生境下尺蛾多样性

为研究生境恢复及地形变化导致的景观异质性对退化景观中生物多样性的影响,于2006和2007年对河北坝上3个不同海拔村庄的农田生境与恢复中的禁牧草地或再造林等半自然生境的尺蛾群落采用灯诱法进行取样调查,比较不同生境的尺蛾多样性.结果表明： 两种生境类型间物种数和个体数存在显著差异、不同海拔村庄物种数也存在显著差异,但不同海拔村庄间个体数差异不显著,不同海拔村庄间以及各村庄内农田和半自然生境稀疏标准化物种数和Fisher α指数无显著差异;非度量多维标度法(NMDS)显示不同海拔的不同生境下尺蛾群落结构显著不同.地形变化导致的景观异质性对坝上地区尺蛾群落组成及多样性影响显著,而无论是恢复中的草地、再造林等半自然生境还是农田生境均是维持尺蛾多样性的重要生境.注重不同地形条件下农田生境和半自然生境景观镶嵌体的保护对维持尺蛾群落γ多样性具有重要意义,但生境恢复能否促进尺蛾群落多样性恢复尚需长期监测.     

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.     

Hearing and evasive behaviour in the greater wax moth, Galleria mellonella (Pyralidae)

Greater wax moths (Galleria mellonella L., Pyraloidea) use ultrasound sensitive ears to detect clicking conspecifics and echolocating bats. Pyralid ears have four sensory cells, A_1?4. The audiogram of G. mellonella has best frequency at 60 kHz with a threshold around 47 dB sound pressure level. A₁ and A₂ have almost equal thresholds in contrast to noctuids and geometrids. A₃ responds at + 12 to + 16 dB relative to the A₁ threshold. The threshold data from the A‐cells give no indication of frequency discrimination in greater wax moths. Tethered greater wax moths respond to ultrasound with short‐latency cessation of flight at + 20 to + 25 dB relative to the A₁ threshold. The behavioural threshold curve parallels the audiogram, thus further corroborating the lack of frequency discrimination. Hence, the distinction between bats and conspecifics is probably based on temporal cues. At a constant duty cycle (percentage of time where sound is on) the pulse repetition rate has no effect on the threshold for flight cessation, but stimulus duration affects both sensory and behavioural thresholds. The maximum integration time is essentially the same: 45 ms for the A₁‐cell and 50–60 ms for the flight cessation response. However, the slopes of the time‐intensity trade‐off functions are very different: ? 2.1 dB per doubling of sound duration for the A₁‐cell threshold, and ? 7.2 dB per doubling of sound duration for the behavioural threshold. The significance of the results for sexual acoustic communication as well as for bat defence is discussed.     

Noctuid moths show neural and behavioural responses to sounds made by some bat-marking rings

Coloured rings are often used for marking bats so that specific individuals can be recognized. We noticed that the rings of mouse-eared bats, Myotis myotis and Myotis blythii, in a combination of one plastic-split and one metallic ring on the same forearm, emitted sounds that were largely ultrasonic each time the rings met in flight. We recorded the ring sounds and the echolocation calls produced by the bats, and played them back to neural preparations of lesser yellow underwing moths, Noctua comes, while making extracellular recordings from the moths' A1 auditory receptors. The peak energy of the ring sounds occurred much closer in frequency to the moth's best auditory frequency (the frequency at which the moth has the lowest auditory threshold) than the peak energy of the calls, for both bat species, and the ring sounds were detected at a threshold 5-6 dB peSPL lower than the calls. Moths performed evasive manoeuvres to playbacks of ring sounds more frequently than they did to control (tape noise) sequences. These neural and behavioural responses imply that certain bats should not be marked with two rings on one wing, as this may make the bat more apparent to tympanate insects, and may therefore reduce its foraging success. Copyright 1999 The Association for the Study of Animal Behaviour.     

Density-dependent melanism in sub-arctic populations of winter moth larvae (Operophtera brumata)

Abstract.  1. The aim of this 4-year observational study was to test for the presence of direct and delayed density-dependent larval melanism in the geometrid moth species Operophtera brumata (winter moth) in northern Norway.
2. Data from many populations with a wide range of population densities in time and space facilitated statistical analyses that could separate the effects of current and past density. The data also included different phases of the 10-year population cycle of this species so that eventual non-linear density effects due to population phase could be detected.
3. The results showed that the prevalence of melanism had a strong positive, linear relation to population density within years, whereas there was no evidence for a delayed effect from the year before or dependency on the phase of the population cycle.
4. In combination, these results limit the range of possible explanations of larval melanism in this outbreaking species. The possible reasons why winter moth larvae might benefit from crowding-induced melanism are discussed.     

Auditory sensitivity and ecological relevance: the functional audiogram as modelled by the bat detecting moth ear

Auditory sensitivity has often been measured by identifying neural threshold in real-time (online) which can introduce bias in the audiograms that are produced. We tested this by recording auditory nerve activity of the notodontid moth Nadata gibbosa elicited by bat-like ultrasound and analysing the response offline. We compared this audiogram with a published online audiogram showing that the bias introduced can result in a difference in the audiogram shape. In the second part of our study we compared offline audiograms using spike number as threshold with others that used spike period and stimulus/spike latency, variables that have been suggested as providing behaviourally functional criteria. These comparisons reveal that functional audiograms are more flatly tuned than simple spike audiograms. The shapes of behavioural audiograms are discussed in the context of the selection pressure that maintains their shape, bat predation. Finally, we make predictions on the distance from bats at which notodontid moths use negative phonotaxis or the acoustic startle response.     

Nocturnal activity positively correlated with auditory sensitivity in noctuoid moths

We investigated the relationship between predator detection threshold and antipredator behaviour in noctuoid moths. Moths with ears sensitive to the echolocation calls of insectivorous bats use avoidance manoeuvres in flight to evade these predators. Earless moths generally fly less than eared species as a primary defence against predation by bats. For eared moths, however, there is interspecific variation in auditory sensitivity. At the species level, and when controlling for shared evolutionary history, nocturnal flight time and auditory sensitivity were positively correlated in moths, a relationship that most likely reflects selection pressure from aerial-hawking bats. We suggest that species-specific differences in the detection of predator cues are important but often overlooked factors in the evolution and maintenance of antipredator behaviour.     

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.     

Gleaning bat echolocation calls do not elicit antipredator behaviour in the Pacific field cricket, <Emphasis Type="Italic">Teleogryllus oceanicus</Emphasis> (Orthoptera: Gryllidae)

Bats that glean prey (capture them from surfaces) produce relatively inconspicuous echolocation calls compared to aerially foraging bats and could therefore be difficult predators to detect, even for insects with ultrasound sensitive ears. In the cricket Teleogryllus oceanicus, an auditory interneuron (AN2) responsive to ultrasound is known to elicit turning behaviour, but only when the cricket is in flight. Turning would not save a cricket from a gleaning bat so we tested the hypothesis that AN2 elicits more appropriate antipredator behaviours when crickets are on the ground. The echolocation calls of Nyctophilus geoffroyi, a sympatric gleaning bat, were broadcast to singing male and walking female T. oceanicus. Males did not cease singing and females did not pause walking more than usual in response to the bat calls up to intensities of 82 dB peSPL. Extracellular recordings from the cervical connective revealed that the echolocation calls elicited AN2 action potentials at high firing rates, indicating that the crickets could hear these stimuli. AN2 appears to elicit antipredator behaviour only in flight, and we discuss possible reasons for this context-dependent function.     

Neuroethology of ultrasonic hearing in nocturnal butterflies (Hedyloidea)

Nocturnal Hedyloidea butterflies possess ultrasound-sensitive ears that mediate evasive flight maneuvers. Tympanal ear morphology, auditory physiology and behavioural responses to ultrasound are described for Macrosoma heliconiaria, and evidence for hearing is described for eight other hedylid species. The ear is formed by modifications of the cubital and subcostal veins at the forewing base, where the thin (1–3 μm), ovoid (520 × 220 μm) tympanal membrane occurs in a cavity. The ear is innervated by nerve IIN1c, with three chordotonal organs attaching to separate regions of the tympanal membrane. Extracellular recordings from IIN1c reveal sensory responses to ultrasonic (>20 kHz), but not low frequency (<10 kHz) sounds. Hearing is broadly tuned to frequencies between 40 and 80 kHz, with best thresholds around 60 dB SPL. Free flying butterflies exposed to ultrasound exhibit a variety of evasive maneuvers, characterized by sudden and unpredictable changes in direction, increased velocity, and durations of ∼500 ms. Hedylid hearing is compared to that of several other insects that have independently evolved ears for the same purpose-bat detection. Hedylid hearing may also represent an interesting example of evolutionary divergence, since we demonstrate that the ears are homologous to low frequency ears in some diurnal Nymphalidae butterflies.     

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.     

Bat-deafness in day-flying moths (Lepidoptera, Notodontidae, Dioptinae)

Assuming that bat-detection is the primary function of moth ears, the ears of moths that are no longer exposed to bats should be deaf to echolocation call frequencies. To test this, we compared the auditory threshold curves of 7 species of Venezuelan day-flying moths (Notodontidae: Dioptinae) to those of 12 sympatric species of nocturnal moths (Notodontidae: Dudusinae, Noctuidae and Arctiidae). Whereas 2 dioptines (Josia turgida, Zunacetha annulata) revealed normal ears, 2 (J. radians, J. gopala) had reduced hearing at bat-specific frequencies (20–80 kHz) and the remaining 3 (Thirmida discinota, Polypoetes circumfumata and Xenorma cytheris) revealed pronounced to complete levels of high-frequency deafness. Although the bat-deaf ears of dioptines could function in other purposes (e.g., social communication), the poor sensitivities of these species even at their best frequencies suggest that these moths represent a state of advanced auditory degeneration brought about by their diurnal life history. The phylogeny of the Notodontidae further suggests that this deafness is a derived (apomorphic) condition and not a retention of a primitive (pleisiomorphic), insensitive state. Accepted: 1 May 1997     

Developmental changes in the expression level of connexin36 in the rat retina

Many noctuid moth species perceive ultrasound via tympanic ears that are located at the metathorax. Whereas the neural processing of auditory information is well studied at the peripheral and first synaptic level, little is known about the features characterizing higher order sound-sensitive neurons in the moth brain. During intracellular recordings from the lateral protocerebrum in the brain of three noctuid moth species, Heliothis virescens, Helicoverpa armigera and Helicoverpa assulta, we found an assembly of neurons responding to transient sound pulses of broad bandwidth. The majority of the auditory neurons ascended from the ventral cord and ramified densely within the anterior region of the ventro-lateral protocerebrum. The physiological and morphological characteristics of these auditory neurons were similar. We detected one additional sound-sensitive neuron, a brain interneuron with its soma positioned near the calyces of mushroom bodies and with numerous neuronal processes in the ventro-lateral protocerebrum. Mass-staining of ventral-cord neurons supported the assumption that the ventro-lateral region of the moth brain was the main target for the auditory projections ascending from the ventral cord.     

Moth hearing on the Faeroe Islands, an area without bats

ABSTRACT. The ultrasound-sensitive ears found in several families of moths are believed to be part of a predator (bat) specific defence strategy; the moth's evasive responses, elicited by the calls of bats, reduce its chances of being caught. Bats have never been found on the Faeroe Islands, whereas moths migrated there before the last Ice Age, and have since been isolated from areas with bats. For this reason, the hearing characteristics of moths from the Faeroes are investigated in this study. All noctuid moths caught there have functional ears sensitive to ultrasound. Audiograms are determined for thirty-two individuals of four noctuid species: Cerapteryx gramminis L., Apamea crenata Hūfn., Apamea maillardi Gey. and Diarsia mendica F. The auditory characteristics of the moths from the Faeroes resemble those of moths from other temperate zones where bats are abundant. The audiograms revealed best frequencies between 20 and 45 kHz, relatively broad turnings (Q_10dB around 1), and thresholds of 35–50 dB SPL at the best frequency. The fact that the moths on the Faeroes possess such sensitive ears is explained by the large time spans which might be required for reduction of a character which is not directly opposed by a selection pressure.     

Echolocation behavior of the Japanese horseshoe bat in pursuit of fluttering prey

Echolocation sounds of Rhinolophus ferrumequinum nippon as they approached a fluttering moth (Goniocraspidum pryeri) were investigated using an on-board telemetry microphone (Telemike). In 40?% of the successful moth-capture flights, the moth exhibited distinctive evasive flight behavior, but the bat pursued the moth by following its flight path. When the distance to the moth was approximately 3-4?m, the bats increased the duration of the pulses to 65-95?ms, which is 2-3 times longer than those during landing flight (30-40?ms). The mean of 5.8 long pulses were emitted before the final buzz phase of moth capture, without strengthening the sound pressure level. The mean duration of long pulses (79.9?±?7.9?ms) corresponded to three times the fluttering period of G. pryeri (26.5?×?3?=?79.5?ms). These findings indicate that the bats adjust the pulse duration to increase the number of temporal repetitions of fluttering information rather than to produce more intense sonar sounds to receive fine insect echoes. The bats exhibited Doppler-shift compensation for echoes returning from large static objects ahead, but not for echoes from target moths, even though the bats were focused on capturing the moths. Furthermore, the echoes of the Telemike recordings from target moths showed spectral glints of approximately 1-1.5?kHz caused by the fluttering of the moths but not amplitude glints because of the highly acoustical attenuation of ultrasound in the air, suggesting that spectral information may be more robust than amplitude information in echoes during moth capturing flight.