The cost of assuming the life history of a host: acoustic startle in the parasitoid fly Ormia ochracea.

In the obligatory reproductive dependence of a parasite on its host, the parasite must trade the benefit of 'outsourcing' functions like reproduction for the risk of assuming hazards associated with the host. In the present study, we report behavioral adaptations of a parasitic fly, Ormia ochracea, that resemble those of its cricket hosts. Ormia females home in on the male cricket's songs and deposit larvae, which burrow into the cricket, feed and emerge to pupate. Because male crickets call at night, gravid female Ormia in search of hosts are subject to bat predation, in much the same way as female crickets are when responding to male song. We show that Ormia has evolved the same evasive behavior as have crickets: an acoustic startle response to bat-like ultrasound that manifests clearly only during flight. Furthermore, like crickets, Ormia has a sharp response boundary between the frequencies of song and bat cries, resembling categorical perception first described in the context of human speech.

Auditory sensitivity of an acoustic parasitoid (Emblemasoma sp., Sarcophagidae, Diptera) and the calling behavior of potential hosts.

Using field broadcasts of model male calling songs, we tested whether Tibicen pruinosa and T. chloromera (Hemiptera: Cicadidae) are candidate hosts for acoustic parasitoid flies. The model calling song of T. pruinosa attracted 90% of the flies (Sarcophagidae: Emblemasoma sp.; all larvapositing females) when broadcast simultaneously with the model T. chloromera song, a phonotactic bias reconfirmed in single song playbacks. In paired broadcasts of model T. pruinosa songs with different relative amplitudes (3 dB or 6 dB), significantly more flies were attracted to the more powerful song, a result consistent with the responses predicted by a model proposed by Forrest and Raspet [1994]. Using intracellular recordings and dye injections, we characterized the sensitivity of auditory units in sound-trapped flies. Intracellular recordings from six auditory units (5 interneurons, 1 afferent) revealed best sensitivity for frequencies near 3-4 kHz, matching the predominant spectral components of the calling songs of both species of cicada. Interestingly, although flies could be attracted to T. pruinosa broadcasts throughout the day, hourly censuses of singing males revealed that calling occurred exclusively at dusk. Furthermore, the duration of the dusk chorus in T. pruinosa was significantly shorter than the midday chorus of the less attractive song of T. chloromera. We propose that the tight temporal aggregation of the dusk chorus time could function to reduce risk from attracted parasitoids.

The development of a biologically-inspired directional microphone for hearing aids.

The development of novel micro-fabrication techniques for producing a directional microphone for hearing aids is here described. The mechanisms underlying both the structure and function of these unusual microphones were originally inspired by the ears of an inconspicuous insect, the parasitoid fly Ormia ochracea. The structure of Ormia's ears inspired new approaches to design directional microphones that are more sensitive and have lower thermal noise than that typical of those using traditional approaches. The mechanisms for directional hearing in this animal are discussed along with the engineering design concepts that they have inspired, because they illustrate how basic research can inspire technology development-translational research. However, to realize the potential of bio-exploitation this microphone diaphragm concept would have been very difficult to realize without the availability of new silicon micro-fabrication technologies. Thus, this report can be viewed as an example of what may be possible with the application of new fabrication methods to microphones. Challenges and opportunities provided by the use of silicon micro-fabrication technology for microphones are discussed.

The unusual visual system of the Strepsiptera: external eye and neuropils.

Adult males of the insect order Strepsiptera are characterized by an unusual visual system that may use design principles from compound as well as simple eyes. The lenses of this eye are unusually large and focus images onto extended retinae. The light-gathering ability of the lens is sufficient to resolve multiple points of an image in each optical unit. We regard each unit as an independent image-forming eye that contributes an inverted partial image. Each partial image is re-inverted by optic chiasmata between the retinae and the lamina, where the complete image could be assembled from the neighboring units. The lamina, medulla and lobula are present, but their organization into cartridges is not clearly discernable. Fluorescent fills, whole-tissue stains, and synaptotagmin immunohistochemistry show that the optic neuropils nevertheless are densely packed, and that several parallel channels within the medulla underlie each of the lenses. The size and shape of the rhabdoms, as well as a relatively slow flicker-fusion frequency could suggest that these eyes evolved through a nocturnal life stage.

A micromachined silicon multielectrode for multiunit recording.

A 16-channel multielectrode was used to record propagating action potentials from multiple units in the ventral nerve cord of the cricket Gryllus bimaculatus. The multielectrode was fabricated using photolithographic and bulk silicon etching techniques. The fabrication differs from standard methods in its use of deep reactive ion etching (DRIE) to form the bulk electrode structure. This technique enables the fabrication of relatively thick (>100 microm), rigid structures whose top surface can have any form of thin film electronics. The multielectrode tested in this paper consists of 16 narrow silicon bridges, 150 microm wide and 350 microm tall, spaced evenly over a centimeter, with passive rectangular gold recording sites on the top surface. The nerve cord was placed perpendicularly across the bridges. In this geometry, the nerve spans a 350 microm deep, 450 microm wide trench between each recording site, permitting adequate isolation of recording sites from each other and a platinum ground plane. Spike templates for eight neurons were formed using principle component analysis and clustering of the concatenated multichannel waveforms. Clean templates were generated from a 40 s recording of stimulus evoked activity. Conduction velocities ranged from 2.59+/-0.05 to 4.99+/-0.12 m/s. Two limitations of extracellular electrode arrays are the resolution of overlapping spikes and relation of discriminated units to known anatomy. The high density, precise positioning, and controlled impedance of recording sites achievable in microfabricated devices such as this one will aid in overcoming these limitations. The rigid devices fabricated using this process offer stable positioning of recording sites over relatively large distances (several millimeters) and are suitable for clamping or squeezing of nerve cords.

Comparison of brain volumes between single and multiple foundresses in the paper wasp Polistes dominulus.

Queens of the paper wasp Polistes dominulus have the option to found nests in spring alone or together with other queens. In the latter case a dominance hierarchy is established among the cofoundresses with the dominant wasp getting the major share of the reproductive output of the nest. The different reproductive strategies of an individual wasp will necessitate different behaviors. We measured the volumes of brain structures as a potential indicator of differential use and elaboration of a number of brain structures. We found a significant increase in the volume of the antennal lobe in members of multiple foundress associations in comparison to single foundresses. The volume of the collar, a substructure of the calyx of the mushroom body, was also significantly larger, especially in the dominant queen of a foundress association. No significant differences between dominant or subordinate wasps in regard to volume of the measured brain substructures were found.

Hyperacute directional hearing in a microscale auditory system.

The physics of sound propagation imposes fundamental constraints on sound localization: for a given frequency, the smaller the receiver, the smaller the available cues. Thus, the creation of nanoscale acoustic microphones with directional sensitivity is very difficult. The fly Ormia ochracea possesses an unusual 'ear' that largely overcomes these physical constraints; attempts to exploit principles derived from O. ochracea for improved hearing aids are now in progress. Here we report that O. ochracea can behaviourally localize a salient sound source with a precision equal to that of humans. Despite its small size and minuscule interaural cues, the fly localizes sound sources to within 2 degrees azimuth. As the fly's eardrums are less than 0.5 mm apart, localization cues are around 50 ns. Directional information is represented in the auditory system by the relative timing of receptor responses in the two ears. Low-jitter, phasic receptor responses are pooled to achieve hyperacute timecoding. These results demonstrate that nanoscale/microscale directional microphones patterned after O. ochracea have the potential for highly accurate directional sensitivity, independent of their size. Notably, in the fly itself this performance is dependent on a newly discovered set of specific coding strategies employed by the nervous system.

Eye stalks or no eye stalks: a structural comparison of pupal development in the stalk-eyed fly Cyrtodiopsis and in Drosophila.

After emergence from the puparium, stalk-eyed flies of the family Diopsidae rapidly expand their head capsule so that the eyes and optic lobes are displaced at the ends of stalks that extend from the central head. Because the expansion takes place in only 15 minutes, we are especially interested in ontogenetic modifications that may facilitate such a rapid and dramatic change. To examine the pupal development of the brain, we used Bodian staining in the stalk-eyed fly, Cyrtodiopsis whitei and compared it with development in the fruit fly, Drosophila melanogaster, which serves as a "typical" dipteran example without eye stalks. Early in pupal development, the neuropil organization of the two species is fairly similar. In both species, columns are present in the outer medulla and giant fibers are discernible in the lobula plate. In contrast to D. melanogaster, C. whitei shows a small, neck-like constriction between the optic lobes and the rest of the brain. By 20% of pupal development, the divergence is more apparent, and by 30%, the future eye stalk and optic nerve of C. whitei has started to form. During the remaining 70% of development, the initially thick optic nerve narrows, and becomes gradually elongated, eventually coiling and folding throughout the short eye stalk. Similarly, the cuticle of the surrounding region becomes constricted, slightly elongated, and gradually appears more and more densely corrugated, like an accordion bellows. However, except for the formation of the optic nerve, the dense aggregation of cuticle around it, and a shift in orientation of the neuropils, the developmental programs of the two species are remarkably similar. This suggests that only a few aspects of development have been modified during the course of evolution to generate the stalk-eyed phenotype. At eclosion, the imago of C. whitei goes through a pumping process to inflate the eye stalks to their full length. Measurements of the diameter of the optic nerve before and after the expansion reveal only a small decrease. We propose that the cuticular folding of the eye stalk as well as the coiling of the optic nerve prepare the pupa well for the rapid and dramatic eye-stalk inflation after eclosion.

Auditory symmetry analysis.

The study of biological symmetry continues to be an important and active area of research, yet in the hearing sciences there are no established quantitative methods for measuring auditory asymmetries and dissimilarities in threshold tuning curves (i.e. audiograms). Using a paired design and adopting methods from the analysis of fluctuating asymmetry, we describe methods for auditory researchers interested in delineating auditory asymmetries and comparing tuning curves, behavioral or neural. We illustrate the methods using audiograms of the prothoracic T-cell interneuron in a nocturnal katydid (Neoconocephalus ensiger). The results show that 87-92 % of T-cells had right-minus-left threshold asymmetries no larger than expected from measurement error alone. Thus, apart from small random fluctuating asymmetries, T-cell pairs in N. ensiger showed no sensory bias and were bilaterally symmetrical from 5 to 100 kHz. The sensitivity of the methods for detecting tuning curve dissimilarities was confirmed in a sound lateralization paradigm by comparing the 'symmetry' (i.e. similarity) of T-cell tuning curves measured at 0 degrees stimulation with tuning curves measured at 90 degrees stimulation for the same T-cell. The results show that T-cell thresholds measured frontally (0 degrees ) were significantly higher than those measured laterally (90 degrees ), particularly for ultrasonic frequencies. Statistically, the directional shift (increase) in auditory thresholds was detected as a directional asymmetry in T-cell tuning, whose origin and functional significance to an insect behaving normally are discussed. The paper discusses practical considerations for detecting auditory asymmetries and tuning curve dissimilarities in general, and closes by questioning the relevance of auditory symmetry for sound localization in both vertebrates and insects.

Neuroethology of the katydid T-cell. I. Tuning and responses to pure tones.

The tuning and pure-tone physiology of the T-cell prothoracic auditory interneuron were investigated in the nocturnal katydid Neoconocephalus ensiger. The T-cell is extremely sensitive and broadly tuned, particularly to high-frequency ultrasound (>20 kHz). Adult thresholds were lowest and showed their least variability for frequencies ranging from 25 to 80 kHz. The average best threshold of the T-cell in N. ensiger ranged from 28 to 38 dB SPL and the best frequency from 20 to 27 kHz. In females, the T-cell is slightly more sensitive to the range of frequencies encompassing the spectrum of male song. Tuning of the T-cell in non-volant nymphs was comparable with that of adults, and this precocious ultrasound sensitivity supports the view that it has a role in the detection of terrestrial sources of predaceous ultrasound. In adults, T-cell tuning is narrower than that of the whole auditory (tympanic) organ, but only at audio frequencies. Superthreshold physiological experiments revealed that T-cell responses were ultrasound-biased, with intensity/response functions steeper and spike latencies shorter at 20, 30 and 40 kHz than at 5, 10 and 15 kHz. The same was also true for T-cell stimulation at 90 degrees compared with stimulation at 0 degrees within a frequency, which supports early T-cell research showing that excitation of the contralateral ear inhibits ipsilateral T-cell responses. In a temporal summation experiment, the integration time of the T-cell at 40 kHz (integration time constant tau =6.1 ms) was less than half that measured at 15 kHz ( tau =15.0 ms). Moreover, T-cell spiking in response to short-duration pure-tone trains mimicking calling conspecifics (15 kHz) and bat echolocation hunting sequences (40 kHz) revealed that temporal pattern-copying was superior for ultrasonic stimulation. Apparently, T-cell responses are reduced or inhibited by stimulation with audio frequencies, which leads to the prediction that the T-cell will encode conspecific song less well than bat-like frequency-modulated sweeps during acoustic playback. The fact that the T-cell is one of the most sensitive ultrasound neurons in tympanate insects is most consistent with it serving an alarm, warning or escape function in both volant and non-volant katydids (nymphs and adults).

Neuroethology of the katydid T-cell. II. Responses to acoustic playback of conspecific and predatory signals.

Although early work on the tettigoniid T large fiber suggested that it might mediate early-warning and escape behavior in katydids, the majority of research thereafter has focused on the ability of the T-cell to detect, localize and/or discriminate mate-calling song. Interestingly, T-cell responses to conspecific song are rarely examined for more than a few seconds, despite the fact that many katydids sing for minutes or hours at a time. In this paper, the second of a pair examining the physiology of the T-cell in Neoconocephalus ensiger, we recorded T-cell responses using longer-duration playbacks (3 min) of conspecific song (Katydid signal 30 ms syllables, 9-25 kHz bandwidth, 12-15 kHz peak frequency) and two types of bat-like ultrasound, a 10 ms, 80->30 kHz frequency-modulated sweep (Bat 10 signal) and a 30 ms, 80->30 kHz frequency-modulated sweep (Bat 30 signal). Spiking responses were distinctly biased towards the short-duration ultrasonic signal, with more spikes per pulse, at a shorter spike latency and at a higher instantaneous firing frequency to the Bat 10 signal than to the Katydid signal or, surprisingly, to the Bat 30 signal. The ability of the T-cell to encode the temporal pattern of the stimulus was particularly striking. Only for the predatory bat signals did T-cell spiking faithfully copy the stimulus; playbacks of conspecific song resulted in significantly weaker spiking responses, particularly in male katydids. The results demonstrate that responses from the T-cell alone may be sufficient for katydids to discriminate biologically relevant signals pertinent to the phonotactic behavior patterns involved in mate attraction and predator avoidance.

Directionality in the mechanical response to substrate vibration in a treehopper (Hemiptera: Membracidae: Umbonia crassicornis).

The use of substrate vibrations in communication and predator-prey interactions is widespread in arthropods. In many contexts, localization of the vibration source plays an important role. For small species on solid substrates, time and amplitude differences between receptors in different legs may be extremely small, and the mechanisms of vibration localization are unclear. Here we ask whether directional information is contained in the mechanical response of an insect's body to substrate vibration. Our study species was a membracid treehopper (Umbonia crassicornis) that communicates using bending waves in plant stems. We used a bending-wave simulator that allows precise control of the frequency, intensity and direction of the vibrational stimulus. With laser-Doppler vibrometry, we measured points on the substrate and on the insect's thorax and middle leg. Transfer functions showing the response of the body relative to the substrate revealed resonance at lower frequencies and attenuation at higher frequencies. There were two modes of vibration along the body's long axis, a translational and a rotational mode. Furthermore, the transfer functions measured on the body differed substantially depending on whether the stimulus originated in front of or behind the insect. Directional information is thus available in the mechanical response of the body of these insects to substrate vibration. These results suggest a vibration localization mechanism that could function at very small spatial scales.

Ultrasound sensitivity in the cricket, Eunemobius carolinus (Gryllidae, Nemobiinae).

Extracellular recordings from the cervical connectives in both long- and short-winged E. carolinus reveal auditory units that are sensitive to frequencies > 15 kHz with best sensitivity at 35 kHz (79 dB SPL threshold). Stimuli in this frequency range also elicit a startle response in long-winged individuals flying on a tether. For single-pulse stimuli, startle and neck connective thresholds decrease with increasing ultrasound duration, consistent with the operation of an exponential integrator with a approximately 32.5-ms time constant. There is evidence for adaptation to long duration pulses (> 20 ms) in the neck connectives, however, as it is more difficult to elicit responses to the later stimuli of a series. For paired-pulse stimuli consisting of 1-ms pulses of 40 kHz, temporal integration was demonstrated for pulse separations < 5 ms. For longer pulse separations, startle thresholds were elevated by 3 dB and appear to be optimally combined. Startle thresholds to 5 ms frequency modulated (FM) sweeps (60-30 kHz) and pure tone pulses (40 kHz) did not differ. The characteristics and sensitivity of this ultrasound-induced startle response did not differ between males and females. As in some other tympanate insects, ultrasound sensitivity in E. carolinus presumably functions in the context of predation from echolocating bats.

The sounds of silence: cessation of singing and song pausing are ultrasound-induced acoustic startle behaviors in the katydid Neoconocephalus ensiger (Orthoptera; Tettigoniidae).

Previous studies of acoustic startle in insects have dealt with behavioral and/or neural mechanisms employed in evading aerially hawking, echolocating bats; however, insects also face terrestrial predators. Here we describe an acoustic startle response of the nocturnal katydid, Neoconocephalus ensiger. Stridulating males disturbed in the field perform obvious antipredatory behaviors--cessation of singing, freezing, jumping, and evasive flight. Under controlled laboratory conditions we found that cessation of singing and song pausing are ultrasound-specific behaviors: when stimulated with pulsed ultrasound (20-100 kHz), but not audio-sound (< 20 kHz), males cease mate calling or insert pauses in their song. A second factor influencing acoustic startle is the phase of stimulation: an acoustic startle response occurs only when the pulse of ultrasound arrives during the window of silence between stridulatory syllables. The average startle threshold and response latency was 70 +/- 5 dB SPL and 34.2 +/- 6.0 ms, respectively. N. ensiger is particularly useful for examining acoustic startle responses of nonflying insects because (1) its calling song is broadband and contains ultrasound, thus the possibility exists of confusion over the biological meaning of ultrasound, and (2) this species shows the classic bat-avoidance response while flying, so a direct comparison between two types of acoustic startle is possible within the same species.

Experience-dependent modification of ultrasound auditory processing in a cricket escape response.

The ultrasound acoustic startle response (ASR) of crickets (Teleogryllus oceanicus) is a defense against echolocating bats. The ASR to a test pulse can be habituated by a train of ultrasound prepulses. We found that this conditioning paradigm modified both the gain and the lateral direction of the startle response. Habituation reduced the slope of the intensity/response relationship but did not alter stimulus threshold, so habituation extended the dynamic range of the ASR to higher stimulus intensities. Prepulses from the side (90 degrees or 270 degrees azimuth) had a priming effect upon the lateral direction of the ASR, increasing the likelihood that test pulses from the front (between -22 degrees and +22 degrees ) would evoke responses towards the same side as prepulse-induced responses. The plasticity revealed by these experiments could alter the efficacy of the ASR as an escape response and might indicate experience-dependent modification of auditory perception. We also examined stimulus control of habituation by prepulse intensity or direction. Only suprathreshold prepulses induced habituation. Prepulses from one side habituated the responses to test pulses from either the ipsilateral or contralateral side, but habituation was strongest for the prepulse-ipsilateral side. We suggest that habituation of the ASR occurs in the brain, after the point in the pathway where the threshold is mediated, and that directional priming results from a second process of plasticity distinct from that underlying habituation. These inferences bring us a step closer to identifying the neural substrates of plasticity in the ASR pathway.

Peripheral frequency mis-match in the primitive ensiferan Cyphoderris monstrosa (Orthoptera: Haglidae).

Peripheral auditory frequency tuning in the ensiferan insect Cyphoderris monstrosa (Orthoptera: Haglidae) was examined by comparing tympanal vibrations and primary auditory receptor responses. In this species there is a mis-match between the frequency of maximal auditory sensitivity and the frequency content of the species' acoustic signals. The mis-match is not a function of the mechanical properties of the tympanum, but is evident at the level of primary receptors. There are two classes of primary receptors: low-tuned and broadly tuned. Differences in the absolute sensitivity of the two receptor types at the male song frequency would allow the auditory system to discriminate intraspecific signals from sounds containing lower frequencies. Comparisons of tympanal and receptor tuning indicated that the sensitivity of the broadly tuned receptors did not differ from that of the tympanum, while low-tuned receptors had significantly narrower frequency tuning. The results suggest that the limited specialization for the encoding of intraspecific signals in the auditory system of C. monstrosa is a primitive rather than a degenerate condition. The limited specialization of C. monstrosa may reflect the evolutionary origin of communication-related hearing from a generalized precursor through the addition of peripheral adaptations (tympana, additional receptors) to enhance frequency sensitivity and discrimination.

Tympanal hearing in the sarcophagid parasitoid fly Emblemasoma sp.: the biomechanics of directional hearing.

In Diptera, tympanal hearing has evolved at least twice in flies that belong to two different families, the tachinids and the sarcophagids. Common to these flies is their parasitoid reproductive strategy, both relying on the acoustic detection and localization of their hosts, singing insects, by means of tympanal hearing organs. In the present study, the external anatomy of the unusual hearing organs of the sarcophagid fly Emblemasoma sp. is described. The sarcophagid ears bear numerous anatomical similarities with those of ormiine tachinids: they are located on the ventral prosternum and possess a pair of scolopidial mechanoreceptive sense organs. A striking difference, however, resides in the lack of a well-defined presternum in the sarcophagid tympanal system. Instead, a deep longitudinal fold, the tympanal fold, spans both hemilateral tympanal membranes across the midline of the animal. Measured using laser Doppler vibrometry, the tympanal mechanical response in the sound field reveals asymmetrical deflection shapes that differ from those of tachinids. Lacking a central fulcrum, the sarcophagid tympanal complex presents different vibrational modes that also result in interaural coupling. The evolutionarily convergent, yet distinct, solutions used by these two small auditory systems to extract directional cues from the sound field and the role of tympanal coupling in this process are discussed.

Visual system of the stalk-eyed fly, Cyrtodiopsis quinqueguttata (Diopsidae, Diptera): an anatomical investigation of unusual eyes.

Diopsid flies have eye stalks up to a centimeter in length, displacing the retina laterally from the rest of the head. This bizarre condition, called hypercephaly, is rare, but has evolved independently among several insect orders and is most common in flies (Diptera). Earlier studies of geometrical optics and behavior have led to various hypotheses about possible adaptive advantages of eye stalks, such as enhanced stereoscopic vision while other hypothesis suggest that eye stalks are an outcome of sexual selection. Here, we focus on how these curious distortions of head/eye morphology are accompanied by changes in the neural organization of the visual system of Cyrtodiopsis quinqueguttata. Histological examinations reveal that the optic lobes, lamina (La), medulla (Me), lobula (Lo), and lobula plate (LP) are contained entirely within the fly's eye bulbs, which are located at the distal ends of the eye stalks. We report that the organization of the peripheral visual system (La and Me) is similar to that of other Diptera (e.g., Musca and Drosophila), but deeper visual areas (Lo and LP) have been more strongly modified. For example, in both the lobula and lobula plate, fewer but larger giant collector neurons are found. The most pronounced difference is the reduction in the number of wide-field vertical cells of the lobula plate, where there are only four relatively large fibers, as opposed to 11 in Musca. The "fewer but larger" neural organization may enhance the conduction velocities of these cells, but may result in a loss of spatial resolution. At the base of the eye bulb, axon bundles collect and form a long optic nerve that extends the length of the eye stalk. We suggest that this organization of the diopsid visual system provides evidence for the costs of possessing long eye stalks.

Hearing in mole crickets (Orthoptera: Gryllotalpidae) at sonic and ultrasonic frequencies.

We have studied auditory responses in two species of mole cricket (Scapteriscus borellii and S. abbreviatus) to determine (1) whether they show sensitivity to ultrasound, (2) whether their hearing (at both low and high frequencies) is based on the same neural circuitry as that of true crickets, and (3) whether ultrasound sensitivity in different mole cricket species varies with their ability to fly. S. borellii are sensitive to ultrasonic frequencies. There is evidence of a segregation of frequency bands in prothoracic auditory neurons. There are two pairs of omega neurons (ONs) with similar morphology to ON1 of true crickets. The two pairs of ONs differ in tuning. One pair has two sensitivity peaks: at the frequency of the calling song of this species (3 kHz), and in the ultrasonic range (25 kHz). The other pair lacks the high-frequency sensitivity and responds exclusively to frequencies in the range of the species song. These two types are not morphologically distinguishable. In S. abbreviatus, only one class of ON was found. S. abbreviatus ONs are narrowly tuned to the frequency of the species' calls. A T-neuron had the best ultrasonic frequency sensitivity in S. borellii. This cell showed a broad tuning to ultrasonic frequencies and was inhibited by low-frequency stimuli. A morphologically similar neuron was also recorded in S. abbreviatus, but lacked the high-frequency sensitivity peak of that in S. borellii. We also assessed the responses of flying S. borellii to ultrasound using field playbacks to free-flying animals. The attractiveness of broadcast calling song was diminished by the addition of an ultrasound signal, indicating that S. borellii avoid high-frequency sound. The results indicate that mole crickets process low-frequency auditory stimuli using mechanisms similar to those of true crickets. They show a negative behavioural response to high-frequency stimuli, as do true crickets, but the organization of ultrasound-sensitive auditory circuitry in mole crickets differs from that of true crickets.

Spatial acuity of ultrasound hearing in flying crickets.

The minimum audible angle is the smallest angular separation at which two sounds are perceived as coming from distinct sources. To determine the spatial acuity of hearing in crickets, we measured minimum audible angles at various locations in azimuth and elevation. Crickets (Teleogryllus oceanicus) were able to discriminate between sources separated by 11.25 degrees (1/32 of a circle) in azimuth directly ahead of them; acuity declined to 45 degrees in azimuth for sound sources 90 degrees to the side and then improved to 33.75 degrees at the rear. Crickets were also able to discriminate between sources separated in elevation, although acuity was much poorer, ranging from 45 degrees at the front and rear of the animal to 90 degrees below the animal. A habituation-dishabituation test was used to test discrimination. This involved presenting a train of ultrasound pulses from one location, habituating the cricket's escape response. This train was followed by a test pulse of ultrasound from another location, after which a final pulse was presented from the original source. If the test pulse was discriminated from the habituating pulses, then the response to the final pulse was dishabituated. To determine the minimum audible angle, we repeated such tests while moving the two sound sources closer together until dishabituation no longer occurred.