James H. Fullard

The evolutionary biology of insect hearing

Few areas of science have experienced such a blending of laboratory and field perspectives as the study of hearing. The disciplines of sensory ecology and neuroethology interpret the morphology and physiology of ears in the adaptive context in which this sense organ functions. Insects, with their enormous diversity, are valuable candidates for the study of how tympanal ears have evolved and how they operate today in different habitats.

Ultrasonic hearing in nocturnal butterflies.

Hedylids have ultrasound-sensitive ears on their wings to help them avoid bats.

Interneurones responding to sound in the tobacco budworm mothHeliothis virescens (Noctuidae): morphological and physiological characteristics

Summary1.A group of 7 acoustically activated interneurones has been identified in the central nervous system of the noctuid mothHeliothis virescens. The neurones have their cell bodies and major processes in either the mesoor metathoracic neuromeres of the fused pterothoracic ganglion, and axons contralateral to the cell body (Figs. 1, 2). All neurones except one project via the contralateral connective to at least the prothoracic ganglion.2.The frequency-response characteristics and auditory thresholds for most interneurones were similar to that of the A1 receptor (40–45 dB SPL at 16 kHz) (Fig. 3A). Interneurone intensity-response characteristics were also generally of the sigmoid type displayed by the A1 and A2 receptors (Fig. 3B).3.Each interneurone responded to a tone with a compound EPSP of characteristic shape (Figs. 2, 4, 5). In two neurones with very similar responses, the shapes of the rising and plateau phases of their EPSPs, and the suggestion of a delayed input to one neurone, were sufficient to distinguish them (Fig. 5).4.The subthreshold responses of all identified interneurones considerably outlasted the stimulus duration, but spiking patterns reflected stimulus duration more accurately (Figs. 4, 5, 6). Most neurones responded in a tonic or phasic/tonic manner, suggesting they might be ‘repeater’ type neurones; whereas one local (Fig. 2) and one unidentified interneurone (Fig. 9) responded like ‘pulse-coder’ neurones.5.All responses to sound by identified interneurones were excitatory, and no sound-related IPSPs were seen (Figs. 2, 3, 4). Further, little habituation of the response occurred in any interneurone for stimulus rates up to 20/s (Fig. 7A, B).6.The latency of the EPSP from stimulus onset in several interneurones (501, 503, 504) was in each case equivalent to a synaptic delay of less than 1 ms compared with the response latency of the A1 receptor, suggesting direct connectivity (Table 1). The input-output curves and EPSP of neurone 501 changed in such a way as to suggest a possible additional input from the A2 receptor at higher intensities (Figs. 3 B, 4).7.Electrical stimulation of the tympanal nerve and sound stimulation of the ear evoked a similar EPSP and spike pattern in interneurone 502 (Fig. 8A, B). However, the latency of the EPSP in neurone 502 elicited by electrical stimulation was too long (9 ms) for the connection between neurone 502 and either A1 or A2 receptors to be direct.8.The neuronal morphologies and response characteristics described above provided the basis for a simple model of the neural circuitry mediating the phonotactic response of a moth to a bat call (Fig. 10).

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

SummaryThe 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.

The response of tympanate moths to the echolocation calls of a substrate gleaning bat, Myotis evotis

Summary1.Most studies examining interactions between insectivorous bats and tympanate prey use the echolocation calls of aerially-feeding bats in their analyses. We examined the auditory responses of noctuid (Eurois astricta) and notodontid (Pheosia rimosa) moth to the echolocation call characteristics of a gleaning insectivorous bat, Myotis evotis.2.While gleaning, M. Evotis used short duration (mean ± SD = 0.66 ± 0.28 ms, Table 2), high frequency, FM calls (FM sweep = 80 − 37 kHz) of relatively low intensity (77.3 + 2.9, −4.2 dB SPL). Call peak frequency was 52.2 kHz with most of the energy above 50 kHz (Fig. 1).3.Echolocation was not required for prey detection or capture as calls were emitted during only 50% of hovers and 59% of attacks. When echolocation was used, bats ceased calling 324.7 (±200.4) ms before attacking (Fig. 2), probably using prey-generated sounds to locate fluttering moths. Mean call repetition rate during gleaning attacks was 21.7 (±15.5) calls/s and feeding buzzes were never recorded.4.Eurois astricta and P. rimosa are typical of most tympanate moths having ears with BFs between 20 and 40 kHz (Fig. 3); apparently tuned to the echolocation calls of aerially-feeding bats. The ears of both species respond poorly to the high frequency, short duration, faint stimuli representing the echolocation calls of gleaning M. evotis (Figs. 4–6).5.Our results demonstrate that tympanate moths, and potentially other nocturnal insects, are unable to detect the echolocation calls typical of gleaning bats and thus are particularly susceptible to predation.

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

Abstract 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.

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

SUMMARY 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 (Eptesicus fuscus) to observe the acoustic encoding of the receptors at this critical time in their defensive behaviour. The B cell is a non-tympanal receptor common to all moths that has been suggested to respond to sound, but we found no evidence of this and suggest that its acoustic responsiveness is an artifact arising from its proprioceptive function. The A1 cell, the most sensitive tympanal receptor in noctuid and arctiid moths and the only auditory receptor in notodontid moths, encodes the attack calls with a bursting firing pattern to a point approximately 150 ms from when the bat would have captured the moth. At this point, the firing of the A1 cell reduces to a non-bursting pattern with longer inter-spike periods, suggesting that the moth may no longer express the erratic flight used to escape very close bats. This may be simply due to the absence of selection pressure on moths for auditory tracking of bat echolocation calls beyond this point. Alternatively, the reduced firing may be due to the acoustic characteristics of attack calls in the terminal phase and an acoustic maneuver used by the bat to facilitate its capture of the moth. Although the role of less sensitive A2 cell remains uncertain in the evasive flight responses of moths it may act as a trigger in eliciting sound production, a close-range anti-bat behaviour in the tiger moth, Cycnia tenera.

Detection of certain African, insectivorous bats by sympatric, tympanate moths

SummaryThe tympanic organs of moths we studied in Zimbabwe responded differentially to the echolocation/hunting signals of sympatric, insectivorous bats. Bats employing very high frequencies (> 110 kHz) and/or low intensity cries tend to be first detected by tympanal preparations at distances considerably less than those with more intense, mid-frequency (20–60 kHz) cries. There appears to be some positive correlation between acoustically inconspicous bats and the amount of auditive prey they feed on although there are theoretical disadvantages in producing highly undetectable orientation cries.

Hunting in unfamiliar space: echolocation in the Indian false vampire bat, Megaderma lyra, when gleaning prey

The literature suggests that in familiar laboratory settings, Indian false vampire bats (Megaderma lyra, family Megadermatidae) locate terrestrial prey with and without emitting echolocation calls in the dark and cease echolocating when simulated moonlit conditions presumably allow the use of vision. More recent laboratory-based research suggests that M. lyra uses echolocation throughout attacks but at emission rates much lower than those of other gleaning bats. We present data from wild-caught bats hunting for and capturing prey in unfamiliar conditions mimicking natural situations. By varying light level and substrate complexity we demonstrated that hunting M. lyra always emit echolocation calls and that emission patterns are the same regardless of light/substrate condition and similar to those of other wild-caught gleaning bats. Therefore, echoic information appears necessary for this species when hunting in unfamiliar situations, while, in the context of past research, echolocation may be supplanted by vision, spatial memory or both in familiar spaces.

Information processing at a central synapse suggests a noise filter in the auditory pathway of the noctuid moth

Summary1.The central projections of the A1 afferent were confirmed via intracellular recording and staining with Lucifer Yellow in the pterothoracic ganglion of the noctuid moths,Agrotis infusa andApamea amputatrix (Fig. 1). Simultaneous recordings of the A1 afferent in the tympanal nerve (extracellularly) and in the pterothoracic ganglion (intracellularly) confirm the identity of the stained receptor as being the A1 cell.2.The major postsynaptic arborizations of interneurone 501 in the pterothoracic ganglion were also demonstrated via intracellular recording and staining (Fig. 2). Simultaneous recordings of the A1 afferent (extracellularly) and neurone 501 (intracellularly) revealed that each A1 spike evokes a constant short latency EPSP in the interneurone (Fig. 2 Bi). Neurone 501 receives only monaural input from the A1 afferent on its soma side as demonstrated by electrical stimulation of each afferent nerve (Fig. 2Bii). EPSPs evoked in neurone 501 by high frequency (100 Hz) electrical stimulation of the afferent nerve did not decrement (Fig. 2Biii). These data are consistent with a monosynaptic input to neurone 501 from the A1 afferent.3.The response of neurone 501 to a sound stimulus presented at an intensity near the upper limit of its linear response range (30 ms, 16 kHz, 80 dB SPL) was a plateau-like depolarization, with tonic spiking activity which continued beyond the end of the tone. The instantaneous spike frequency of the response was as high as 800 Hz, and was maintained at above 600 Hz for the duration of the tone (Fig. 3).4.The relationship between the instantaneous spike frequency in the A1 afferent and that recorded simultaneously in neurone 501 is linear over the entire range of A1 spike frequencies evoked by white noise sound stimuli (Fig. 4). Similarly, the relationship between instantaneous spike frequency in the A1 afferent and the mean depolarization evoked in neurone 501 is also linear for all A1 spike frequencies tested (Fig. 5). No summation of EPSPs occurred for A1 spike frequencies below 100 Hz.5.There is no evidence of either facilitation or depression of EPSPs in neurone 501 as both the overall level of depolarization and the amplitudes of individual EPSPs remained constant at high spike frequencies in the A1 afferent (Fig. 5). When coupled with the lack of inhibition in responses of neurone 501 to A1 afferent input, the data suggest that summation of synaptic events is also linear.6.Individual EPSPs evoked in neurone 501 by the A1 afferent were recorded and their shapes analysed. The results (Fig. 6, Table 1) show the EPSPs to be of uniform amplitude, with fast rise times and time to peak, short half-widths and total duration, and a small decay time. The existence of such fast EPSPs accounts for the dynamics of information transfer at this first synapse of the auditory pathway.7.The threshold and integration characteristics of neurone 501 suggest that its function in the defensive behaviour of the moth may be as a noise filter allowing the moth to distinguish sources of natural, high frequency sound (e.g., singing insects) from the echolocation calls of hunting bats.