Hearing in tsetse flies? Morphology and mechanics of a putative auditory organ

Tympanal hearing organs are widely used by insects to detect sound pressure. Such ears are relatively uncommon in the order Diptera, having only been reported in two families thus far. This study describes the general anatomical organization and experimentally examines the mechanical resonant properties of an unusual membranous structure situated on the ventral prothorax of the tsetse fly, Glossina morsitans (Diptera: Glossinidae). Anatomically, the prosternal membrane is backed by an air filled chamber and attaches to a pair of sensory chordotonal organs. Mechanically, the membrane shows a broad resonance around 5.3-7.2 kHz. Unlike previously reported dipteran tympana, a directional response to sound was not found in G. morsitans. Collectively, the morphology, the resonant properties and acoustic sensitivity of the tsetse prothorax are consistent with those of the tympanal hearing organs in Ormia sp. and Emblemasoma sp. (Tachinidae and Sarcophagidae). The production of sound by several species of tsetse flies has been repeatedly documented. Yet, clear behavioural evidence for acoustic behaviour is sparse and inconclusive. Together with sound production, the presence of an ear-like structure raises the enticing possibility of auditory communication in tsetse flies and renews interest in the sensory biology of these medically important insects.     

Identification of sound-localization cues in the HRTF of the bat-head model

Animals such as bats and dolphins exhibit impressive echolocation abilities in terms of ranging, resolution and imaging and therefore represent a valuable learning model for the study of spatial hearing and sound source localization leading to a better understanding of the hearing mechanism and further improvement of the existing localization strategies. This study aims to examine and understand the directional characteristics of a sonar receiver modeled upon the bat auditory system via measurements of the head-related transfer function (HRTF) in the horizontal plane. Four different models of the bat head were considered here and used to evaluate acoustic spectral characteristics of the sound received by the bat's ears – a sphere model, a sphere model with a pinna attached (two pinnae of different size were used in this study) and a bat-head cast. The performed HRTF measurements of the bat-head models were further analyzed and compared to identify monaural spectral localization cues in the horizontal plane defined by the bat's head and pinna shape and size. Our study suggests that the acoustical characteristics of a bio-inspired sonar head measured and specified in advance can potentially improve the performance of a receiver. Moreover, the generated auditory models may hold clues for the design of receiver characteristics in ultrasound imaging and navigation systems.     

Directionality of the tympanal vibrations in a cicada: a biophysical analysis

1. Laser vibrometry and acoustic measurements were used to study the biophysics of directional hearing in males and females of a cicada, in which most of the male tympanum is covered by thick, water filled tissue “pads”. 2. In females, the tympanal vibrations are very dependent on the direction of sound incidence in the entire frequency range 1–20 kHz, and especially at the main frequencies of the calling song (3–7 kHz). At frequencies up to 10 kHz, the directionality disappears if the contralateral tympanum, metathoracic spiracle, and folded membrane are blocked with Vaseline. This suggests some pressure-difference receiver properties in the ear. 3. In males, the tympanal vibrations depend on the direction of sound incidence only within narrow frequency bands (around 1.8 kHz and at 6–7 kHz). At frequencies above 10–12 kHz, the directionality appears to be determined by diffraction, and the ear seems to work as a pressure receiver. The peak in directionality at 6–7 kHz disappears when the contralateral timbal, but not the tympanum, is covered. Covering the thin ventral abdominal wall causes the peak around 1.8 kHz to disappear. 4. Most observed tympanal directionalities, except around 1.8 kHz in males, are well predicted from measured transmissions of sound through the body and measured values of sound amplitude and phase at the ears at various directions of sound incidence. Accepted: 18 October 1996     

Spatial processing within the mustache bat echolocation system: possible mechanisms for optimization

1. The directionality of an echolocation system is determined by the acoustic properties of both the emitter and receiver, i.e., by the radiation pattern of the emitted pulse and the directionally of the external ears. We measured the directionality of the echolocation system of the greater mustache bat (Pteronotus parnellii) at the 30 kHz, 60 kHz and 90 kHz harmonics of its echolocation pulse by summing, at points throughout the frontal sound field, the echo attenuation due to the spread of pulse energy and the attenuation due to the spread of pulse energy and the attenuation due to the directionality of its external ears. The pulse radiation pattern at the 3 harmonics was measured by comparing the output of a microphone moved throughout the frontal sound field against a second reference microphone at the center of the field. External ear directionality at the 3. harmonics was measured by presenting free-field sounds throughout the frontal sound field, and recording the intensity thresholds of cochlear microphonic potentials, and the intensity thresholds of monaural neurons in the inferior colliculus tuned to one of the 3 harmonics. 2. When compared with ear directionality, the echolocation system was found to be more directional for the center of the sound field in several respects. At all harmonics, attenuation of sounds originating in the peripheral part of the field was increased by 10 to 13 dB. Areas of maximum sound intensity contracted toward the center of the field. Also, the isointensity contours of the echolocation system were more radially symmetrical about the center of the field. 3. At 60 kHz, sound intensity along the azimuth within the echolocation system was nearly constant 26 degrees to either side of the center of the field. This suggests that the radiation pattern of the echolocation pulse and the directionality of the external ears complement one another to produce an acoustic environment at the center of the sound field in which stimulus intensity is stabilized to allow more effective analysis of various aspects of the echolocation target. In particular, we suggest that this intensity stabilization may allow the bat to more effectively resolve the interaural intensity differences it uses to localize prey. 4. Predictions of the azimuthal spatial tuning of binaurally sensitive neurons in the inferior colliculus within the echolocation system were compared with their spatial tuning when only ear directionality is considered.(ABSTRACT TRUNCATED AT 400 WORDS)     

The efficiency of artificial wingbeat sounds for capturing midges in black light traps

This study was conducted to develop a new method to control adult Chironomus plumosus (L.) midges (Diptera: Chironomidae) using their acoustic responses to sound + light traps in the field. Trials were conducted from June 10 to June 27, 1996 near the hyper-eutrophic Lake Suwa in central Japan. In cylindrical sound traps, optimal trapping of swarming males occurred at frequencies of 270–300 Hz at 22.5 °C. This effect was significantly enhanced using a sound trap equipped with a black light lamp. The mean number of midges captured by sound + light trap was about 4.5 times the number of midges caught by either light or sound trap alone. In conclusion, the application of audio-frequency sounds combined with attraction to light for chironomid midge control seems to be quite feasible, assuming the availability of a suitable collecting device.     

RECENT BIO ACOUSTIC PUBLICATIONS (mainly 1993)

ABSTRACT

Although much research has been done to describe the degradation of sound signals propagating in natural habitats, the directional cues of sound have so far been neglected. This paper describes a first approach to quantifying the degradation of directional cues in sound propagating parallel to the ground in a grassland habitat of orthopteran insects. A matched pair of probe microphones measured the sound amplitude and phase close to the ears of grasshopper carcasses for 12 evenly spaced directions of sound incidence. The degradation was found to increase with frequency and distance from the sound source and to decrease with distance from the ground. The acoustical data were used to predict how well animals with different auditory systems can determine the direction of the sender. At one position in the habitat, the predictions were compared with the pattern of phonotactic responses of live grasshoppers. Amplitude cues appear to degrade much faster with distance than phase cues. Animals exploiting phase cues may therefore maintain a reasonable directional hearing when the amplitude cues no longer make sense. The pressure-difference-receiver type of ears responds to phase differences, and these ears may be particularly suited to overcoming the degradation of directional cues. This suggests that the possession of such ears may be an adaptation not only to small body size (relative to wavelength), but also to the acoustic properties of the habitat.     

Maps of interaural time difference in the chicken’s brainstem nucleus laminaris

Animals, including humans, use interaural time differences (ITDs) that arise from different sound path lengths to the two ears as a cue of horizontal sound source location. The nature of the neural code for ITD is still controversial. Current models differentiate between two population codes: either a map-like rate-place code of ITD along an array of neurons, consistent with a large body of data in the barn owl, or a population rate code, consistent with data from small mammals. Recently, it was proposed that these different codes reflect optimal coding strategies that depend on head size and sound frequency. The chicken makes an excellent test case of this proposal because its physical prerequisites are similar to small mammals, yet it shares a more recent common ancestry with the owl. We show here that, like in the barn owl, the brainstem nucleus laminaris in mature chickens displayed the major features of a place code of ITD. ITD was topographically represented in the maximal responses of neurons along each isofrequency band, covering approximately the contralateral acoustic hemisphere. Furthermore, the represented ITD range appeared to change with frequency, consistent with a pressure gradient receiver mechanism in the avian middle ear. At very low frequencies, below 400 Hz, maximal neural responses were symmetrically distributed around zero ITD and it remained unclear whether there was a topographic representation. These findings do not agree with the above predictions for optimal coding and thus revive the discussion as to what determines the neural coding strategies for ITDs.     

Hearing in tiger beetles (Cicindelidae)

ABSTRACT. Tympanic hearing organs (ears) are reported for several tiger beetle (Cicindelidae) species. The paired ears are positioned bilaterally on the first abdominal tergum and consist of cavities covered by thin tympana. When the beetle is not flying the elytra covers its ears and reduces their sensitivity to sound. However, when the beetle is flying, its exposed ears are capable of detecting ultrasonic pulses. Under a microscope, beetles with their elytra artificially raised contract their abdomens in response to ultrasound. Ultrasonic emissions directed toward flying beetles induce them immediately to fly downward and land, a response which probably aids escape from predators, particularly echolocating bats. Other possible uses for the ears are the avoidance of diurnal insect predators and intraspecific communication.     

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.     

Auditory event-related potentials to the apparent auditory image motion

Auditory event-related potentials (ERP) were registered to the dichotically presented white noise stimuli (duration 1500 ms, band 150-1200 Hz). Abrupt or gradual change ofinteraural time difference in the middle of stimuli (750 ms after sound offset) was perceived as an apparent auditory image (AI) instant relocation or motion from the midline to one of the ears. In responses these stimuli two ERPs were observed: one to the sound onset, and second--to the onset of motion or AI relocation. ERPs to AI relocation differed from those to sound onset in longer components latencies (123 ms versus 105 ms for N 1,227 ms versus 190 ms for P2). In responses to AI motion component latencies were even longer (N1: 137 ms, P2: 240 ms); N1 amplitude was greater at sites contralateral to the AI motion direction.     

Out of phase: relevance of the medial septum for directional hearing and phonotaxis in the natural habitat of field crickets

A modified tracheal system is the anatomical basis for a pressure difference receiver in field crickets, where sound has access to the inner and outer side of the tympanum of the ear in the forelegs. A thin septum in the midline of a connecting trachea coupling both ears is regarded to be important in producing frequency-dependent interaural intensity differences (IIDs) for sound localization. However, the fundamental role of the septum in directional hearing has recently been challenged by the finding that the localization ability is ensured even with a perforated septum, at least under controlled laboratory conditions. Here, we investigated the influence of the medial septum on phonotaxis of female Gryllus bimaculatus under natural conditions. Surprisingly, even with a perforated septum, females reliably tracked a male calling song in the field. Although reduced by 5.2 dB, IIDs still averaged at 7.9 dB and provided a reliable proximate basis for the observed behavioural performance of operated females in the field. In contrast, in the closely related species Gryllus campestris the same septum perforation caused a dramatic decline in IIDs over all frequencies tested. We discuss this discrepancy with respect to a difference in the phenotype of their tracheal systems.     

不同抗性小麦品种上麦红吸浆虫幼虫的空间分布型与理论抽样数

【目的】为了解小麦品种抗性对麦红吸浆虫Sitodiplosis mosellana(Géhin)幼虫在麦穗上空间分布型的影响,为科学调查提供合理的抽样依据。【方法】2015年5月采用剥穗调查法对陕西省周至县试验田种植的4个抗虫和4个感虫小麦品种麦红吸浆虫幼虫危害进行调查,应用6种聚集度指标和Iwao M*?m回归法综合分析了幼虫在抗性不同小麦品种上的的空间分布结构。【结果】幼虫在抗、感小麦品种整穗及麦穗上、中、下部位上空间分布型一致,均呈聚集分布,但在抗虫品种上聚集强度大于感虫品种;抗、感小麦品种上分布的基本成分均为个体群,个体间相互吸引。聚集均数λ分析表明,幼虫在抗性较强品种上的聚集主要由小麦穗部化学物质和形态结构等环境因素引起,感虫品种上则由环境因素和成虫的产卵习性共同作用所致。幼虫在抗、感小麦品种上的发生趋势一致,均是上部发生最重,中部次之,下部最轻。根据Iwao回归法中的分布型参数,确立了幼虫在不同虫口密度和允许误差条件下的理论抽样数。【结论】麦红吸浆虫幼虫在抗性不同小麦品种上均呈聚集分布,调查时应根据当地栽培品种平均虫口密度选择适宜的抽样数量。     

Otoacoustic emissions from insect ears: evidence of active hearing?

Sensitive hearing organs often employ nonlinear mechanical sound processing which generates distortion-product otoacoustic emissions (DPOAE). Such emissions are also recordable from tympanal organs of insects. In vertebrates (including humans), otoacoustic emissions are considered by-products of active sound amplification through specialized sensory receptor cells in the inner ear. Force generated by these cells primarily augments the displacement amplitude of the basilar membrane and thus increases auditory sensitivity. As in vertebrates, the emissions from insect ears are based on nonlinear mechanical properties of the sense organ. Apparently, to achieve maximum sensitivity, convergent evolutionary principles have been realized in the micromechanics of these hearing organs-although vertebrates and insects possess quite different types of receptor cells in their ears. Just as in vertebrates, otoacoustic emissions from insects ears are vulnerable and depend on an intact metabolism, but so far in tympanal organs, it is not clear if auditory nonlinearity is achieved by active motility of the sensory neurons or if passive cellular characteristics cause the nonlinear behavior. In the antennal ears of flies and mosquitoes, however, active vibrations of the flagellum have been demonstrated. Our review concentrates on experiments studying the tympanal organs of grasshoppers and moths; we show that their otoacoustic emissions are produced in a frequency-specific way and can be modified by electrical stimulation of the sensory cells. Even the simple ears of notodontid moths produce distinct emissions, although they have just one auditory neuron. At present it is still uncertain, both in vertebrates and in insects, if the nonlinear amplification so essential for sensitive sound processing is primarily due to motility of the somata of specialized sensory cells or to active movement of their (stereo-)cilia. We anticipate that further experiments with the relatively simple ears of insects will help answer these questions.     

Mechanical signatures of transducer gating in the Drosophila ear

Hearing relies on dedicated mechanotransducer channels that convert sound-induced vibrations into electrical signals [1]. Linking this transduction to identified proteins has proven difficult because of the scarcity of native auditory transducers and their tight functional integration into ears [2-4]. We describe an in vivo paradigm for the noninvasive study of auditory transduction. By investigating displacement responses of the Drosophila sound receiver, we identify mechanical signatures that are consistent with a direct mechanotransducer gating in the fly's ear. These signatures include a nonlinear compliance that correlates with electrical nerve responses, shifts with adaptation, and conforms to the gating-spring model of vertebrate auditory transduction. Analyzing this gating compliance in terms of the gating-spring model reveals striking parallels between the transducer mechanisms for hearing in vertebrates and flies. Our findings provide first insights into the mechanical workings of invertebrate mechanotransducer channels and set the stage for using Drosophila to specifically search for, and probe the roles of, auditory transducer components.     

Mechanical properties of the frog ear: vibration measurements under free- and closed-field acoustic conditions

The acoustically induced motion of the eardrum of the frog was measured by an incoherent optical technique. When free-field sound stimulation was used, the eardrum vibration had a band-pass characteristic with maximum amplitude at 1-2.5 kHz. However, when the sound was presented in a closed-field acoustic coupler the response was low-pass (cut-off frequency about 2.5 kHz). We demonstrate that the motion is the result of the mechanical properties of the eardrum and the sound pressure acting upon it. The net pressure is due to a combination of sound incident directly on the front of the drum and of sound conducted to the rear via internal (resonant) pathways. The frog ear therefore acts as a pressure-gradient receiver at low frequency and a pressure receiver at high frequency. A model is proposed and analysed in terms of its electrical analogue. This model accounts for both our own experimental observations and those of previous studies.     

The role of pressure difference reception in the directional hearing of budgerigars (Melopsittacus undulatus)

In many birds, the middle ears are connected through an air-filled interaural pathway. Sound transmission through this pathway may improve directional hearing. However, attempts to demonstrate such a mechanism have produced conflicting results. One reason is that some species of birds develop a lower static air pressure in the middle ears when anaesthetized, which reduces eardrum vibrations. In anaesthetized budgerigars with vented interaural air spaces and presumed normal eardrum vibrations, we find that sound propagating through the interaural pathway considerably improves cues to the directional hearing. The directional cues in the received sound combined with amplitude gain and time delay of sound propagating through the interaural pathway quantitatively account for the observed dependence of eardrum vibration on direction of sound incidence. Interaural sound propagation is responsible for most of the frontal gradient of eardrum vibration (i.e. when a sound source is moved from a small contralateral angle to the same ipsilateral angle). Our study confirms that at low frequencies the interaural sound propagation may cause vibrations of the eardrum to differ much in time, thus providing a possible cue for directional hearing. The acoustically effective size of the head of our birds (diameter 28 mm) is much larger than expected from the dimensions of the skull, so apparently the feathers on the head have a considerable acoustical effect.Dedicated to Professor Franz Huber on the occasion of his 80th birthday.     

The diets of two high-flying bats from Africa

The diets of two fast-flying, aerial-hawking bats from north-east Africa (Ethiopia) were investigated by means of faecal analysis. Otomops martiensseni (Molossidae; c. 35 g body mass), which is remarkably specialized morphologically with very long, narrow wings and large ears, and which uses low frequency echolocation (10kHz), feeds almost exclusively (97% by volume) on moths, mostly of large species. The smaller (20 g) Taphozous perforatus (Emballonuridae) also has long, narrow wings but short ears and is less morphologically extreme than Otomops. It feeds on moths (56%), but also on many other insect groups such as Isoptera (14%). Coleoptera (10o%), Orthoptera (8%), as well as Hemiptera, Neuroptera, Hymenoptera and Diptera. Otomops martiensseni , in particular, appears to be a highly specialized moth predator.     

Responses of mosquitoes and German cockroaches to ultrasound emitted from a random ultrasonic generating device

The repellency of ultrasound to females of two species of mosquitoes, Anopheles quadrimaculatus Say and Anopheles gambiae Giles (Diptera: Culicidae), and male and female German cockroaches, Blattella germanica (L.) (Blattodea: Blattellidae), was evaluated under laboratory conditions using a random ultrasonic device developed at Kansas State University. This device produces ultrasound in the 20–100 kHz frequency range and random sound patterns at any frequency range. Under the particular settings described in the paper, this ultrasonic device produced sound pressure levels from 91 to 101, 91 to 102, and 90 to 100 dB at the top, bottom, and side panels of the test chamber, respectively (0 dB = 20 micropascals). Sound pressure levels recorded at the center of the top, bottom, and side panels were higher than those recorded at the panel edges. Ultrasound from the random ultrasonic device failed to repel mosquitoes and German cockroaches at the different frequency ranges evaluated. Our results confirm previous findings with commercial devices producing constant sound patterns that ultrasound in general is not a promising tool for repelling mosquitoes and cockroaches.     

The Auditory Mechanics of the Outer Ear of the Bush Cricket: A Numerical Approach

Bush crickets have tympanal ears located in the forelegs. Their ears are elaborate, as they have outer-, middle-, and inner-ear components. The outer ear comprises an air-filled tube derived from the respiratory trachea, the acoustic trachea (AT), which transfers sound from the mesothoracic acoustic spiracle to the internal side of the ear drums in the legs. A key feature of the AT is its capacity to reduce the velocity of sound propagation and alter the acoustic driving forces of the tympanum (the ear drum), producing differences in sound pressure and time between the left and right sides, therefore aiding the directional hearing of the animal. It has been demonstrated experimentally that the tracheal sound transmission generates a gain of ∼15 dB and a propagation velocity of 255 ms⁻¹, an approximately 25% reduction from free-field propagation. However, the mechanism responsible for this change in sound pressure level and velocity remains elusive. In this study, we investigate the mechanical processes behind the sound pressure gain in the AT by numerically modeling the tracheal acoustic behavior using the finite-element method and real three-dimensional geometries of the tracheae of the bush cricket Copiphora gorgonensis. Taking into account the thermoviscous acoustic-shell interaction on the propagation of sound, we analyze the effects of the horn-shaped domain, material properties of the tracheal wall, and the thermal processes on the change in sound pressure level in the AT. Through the numerical results obtained, it is discerned that the tracheal geometry is the main factor contributing to the observed pressure gain.