Insect Hearing Research Articles

Review of the applications of principles of insect hearing to microscale acoustic engineering challenges.

When looking for novel, simple, and energy-efficient solutions to engineering problems, nature has proved to be an incredibly valuable source of inspiration. The development of acoustic sensors has been a prolific field for bioinspired solutions. With a diverse array of evolutionary approaches to the problem of hearing at small scales (some widely different to the traditional concept of 'ear'), insects in particular have served as a starting point for several designs. From locusts to moths, through crickets and mosquitoes among many others, the mechanisms found in nature to deal with small-scale acoustic detection and the engineering solutions they have inspired are reviewed. The present article is comprised of three main sections corresponding to the principal problems faced by insects, namely frequency discrimination, which is addressed by tonotopy, whether performed by a specific organ or directly on the tympana; directionality, with solutions including diverse adaptations to tympanal structure; and detection of weak signals, through what is known as active hearing. The three aforementioned problems concern tiny animals as much as human-manufactured microphones and have therefore been widely investigated. Even though bioinspired systems may not always provide perfect performance, they are sure to give us solutions with clever use of resources and minimal post-processing, being serious contenders for the best alternative depending on the requisites of the problem.

Auditory mechanics in the grig ( Cyphoderris monstrosa ): tympanal travelling waves and frequency discrimination as a precursor to inner ear tonotopy

Ensiferan orthopterans offer a key study system for acoustic communication and the process of insect hearing. Cyphoderris monstrosa (Hagloidea) belongs to a relict ensiferan family and is often used for evolutionary comparisons between bushcrickets (Tettigoniidae) and their ancestors. Understanding how this species processes sound is therefore vital to reconstructing the evolutionary history of ensiferan hearing. Previous investigations have found a mismatch in the ear of this species, whereby neurophysiological and tympanal tuning does not match the conspecific communication frequency. However, the role of the whole tympanum in signal reception remains unknown. Using laser Doppler vibrometry, we show that the tympana are tonotopic, with higher frequencies being received more distally. The tympana use two key modalities to mechanically separate sounds into two auditory receptor populations. Frequencies below approximately 8 kHz generate a basic resonant mode in the proximal end of the tympanum, whereas frequencies above approximately 8 kHz generate travelling waves in the distal region. Micro-CT imaging of the ear and the presented data suggest that this tonotopy of the tympana drive the tonotopic mechanotransduction of the crista acustica (CA). This mechanism represents a functional intermediate between simple tuned tympana and the complex tonotopy of the bushcricket CA.

Within host acoustic signal preference of frog‐biting mosquitoes (Diptera: Culicidae) and midges (Diptera: Corethrellidae) on Iriomote Island, Japan

AbstractHaematophagous insects can rely on specialized host‐seeking behaviors to locate hosts. Some frog‐biting flies, for example, eavesdrop on the conspicuous acoustic signals produced by male frogs and toads. Using such auditory cues to locate a host imposes an additional challenge: how to recognize appropriate sounds when different frog species produce calls with varying acoustic properties. The limited knowledge of antennal hearing in dipteran insects hinders our ability to understand how eavesdropping flies detect and recognize frog calls. Behavioral studies suggest that frog‐biting flies use broad acoustic templates to detect and recognize their victims. Here, we use within‐species call variation to examine the acoustic preferences in frog‐biting flies. Specifically, we examine the attraction of frog‐biting mosquitoes (Uranotaenia spp.) and midges (Corethrella nippon) to the calls of a Japanese treefrog, the Ryukyu Kajika frog (Buergeria japonica), on Iriomote Island, Japan. Male Ryukyu Kajika frogs produce two call types. While both calls have a high frequency peak (3 kHz), the first call type (Type I) also contains a lower frequency peak (1.8 kHz) absent in the second call type (Type II). Using field phonotaxis experiments we found that Type I calls are more attractive to both frog‐biting mosquitoes and midges. Thus, our results suggest that the frog‐biting Nematoceran flies in this community are biased towards the acoustic properties of Type I calls. We discuss this finding in the context of the evolution of antennal hearing in flies.

What Does an Insect Hear? Reassessing the Role of Hearing in Predator Avoidance with Insights from Vertebrate Prey.

Insects have a diversity of hearing organs known to function in a variety of contexts, including reproduction, locating food, and defense. While the role of hearing in predator avoidance has been extensively researched over the past several decades, this research has focused on the detection of one type of predator-echolocating bats. Here we reassess the role of hearing in antipredator defense by considering how insects use their ears to detect and avoid the wide range of predators that consume them. To identify the types of sounds that could be relevant to insect prey, we first review the topic of hearing-mediated predator avoidance in vertebrates. Sounds used by vertebrate prey to assess predation risk include incidental sound cues (e.g., flight sounds, rustling vegetation, and splashing) produced by an approaching predator or another escaping prey, as well as communication signals produced by a predator (e.g., echolocation calls, songs) or nonpredator (e.g., alarm calls). We then review what is known, and what is not known, about such sounds made by the main predators and parasitoids of insects (i.e., birds, bats, terrestrial vertebrates, and invertebrates) and how insects respond to them. Three key insights emerged from our review. First, there is a lack of information on how both vertebrate and insect prey use passive sound cues produced by predators to avoid being captured. Second, while there are numerous examples of vertebrate prey eavesdropping on the calls and songs of predators and nonpredators to assess risk, there are currently no such examples for eared insect prey. Third, the hearing sensitivity of many insects, including those with ears considered to be dedicated to detecting bats or mates, overlaps with both sound cues and signals generated by nonbat predators. Sounds of particular relevance to insect prey include the flight sounds and calls of insectivorous birds, the flight sounds of insect predators and parasitoids, and rustling vegetation sounds of birds and terrestrial predators. We conclude that research on the role of insect hearing in predator avoidance has been disproportionally focused on bat-detection, and that acoustically-mediated responses to other predators may have been overlooked because the responses of prey may be subtle (e.g., ceasing activity, increasing vigilance). We recommend that researchers expand their testing of hearing-mediated risk assessment in insects by considering the wide range of sounds generated by predators, and the varied responses exhibited by prey to these sounds.

Directional hearing in insects: biophysical, physiological and ecological challenges.

Sound localisation is a fundamental attribute of the way that animals perceive their external world. It enables them to locate mates or prey, determine the direction from which a predator is approaching and initiate adaptive behaviours. Evidence from different biological disciplines that has accumulated over the last two decades indicates how small insects with body sizes much smaller than the wavelength of the sound of interest achieve a localisation performance that is similar to that of mammals. This Review starts by describing the distinction between tympanal ears (as in grasshoppers, crickets, cicadas, moths or mantids) and flagellar ears (specifically antennae in mosquitoes and fruit flies). The challenges faced by insects when receiving directional cues differ depending on whether they have tympanal or flagellar years, because the latter respond to the particle velocity component (a vector quantity) of the sound field, whereas the former respond to the pressure component (a scalar quantity). Insects have evolved sophisticated biophysical solutions to meet these challenges, which provide binaural cues for directional hearing. The physiological challenge is to reliably encode these cues in the neuronal activity of the afferent auditory system, a non-trivial problem in particular for those insect systems composed of only few nerve cells which exhibit a considerable amount of intrinsic and extrinsic response variability. To provide an integrative view of directional hearing, I complement the description of these biophysical and physiological solutions by presenting findings on localisation in real-world situations, including evidence for localisation in the vertical plane.

Comparative micromechanics of bushcricket ears with and without a specialized auditory fovea region in the crista acustica.

In some insects and vertebrate species, the specific enlargement of sensory cell epithelium facilitates the perception of particular behaviourally relevant signals. The insect auditory fovea in the ear of the bushcricket Ancylecha fenestrata (Tettigoniidae: Phaneropterinae) is an example of such an expansion of sensory epithelium. Bushcricket ears developed in convergent evolution anatomical and functional similarities to mammal ears, such as travelling waves and auditory foveae, to process information by sound. As in vertebrate ears, sound induces a motion of this insect hearing organ (crista acustica), which can be characterized by its amplitude and phase response. However, detailed micromechanics in this bushcricket ear with an auditory fovea are yet unknown. Here, we fill this gap in knowledge for bushcricket, by analysing and comparing the ear micromechanics in Ancylecha fenestrata and a bushcricket species without auditory fovea (Mecopoda elongata, Tettigoniidae: Mecopodinae) using laser-Doppler vibrometry. We found that the increased size of the crista acustica, expanded by a foveal region in A. fenestrata, leads to higher mechanical amplitudes and longer phase delays in A. fenestrata male ears. Furthermore, area under curve analyses of the organ oscillations reveal that more sensory units are activated by the same stimuli in the males of the auditory fovea-possessing species A. fenestrata. The measured increase of phase delay in the region of the auditory fovea supports the conclusion that tilting of the transduction site is important for the effective opening of the involved transduction channels. Our detailed analysis of sound-induced micromechanics in this bushcricket ear demonstrates that an increase of sensory epithelium with foveal characteristics can enhance signal detection and may also improve the neuronal encoding.

Awesome ears: The weird world of insect hearing

Evolution made insect ears many times over, resulting in a dazzling variety of forms found in spots all over the body. Biologists are digging deep into some of those ears to figure out how and why they came to be.

Functional basis of the sexual dimorphism in the auditory fovea of the duetting bushcricket Ancylecha fenestrata.

From mammals to insects, acoustic communication is in many species crucial for successful reproduction. In the duetting bushcricket Ancylecha fenestrata, the mutual acoustic communication between males and females is asymmetrical. We investigated how those signalling disparities are reflected by sexual dimorphism of their ears. Both sexes have tympanic ears in their forelegs, but male ears possess a significantly longer crista acustica containing 35% more scolopidia. With more sensory cells to cover a similar hearing range, the male hearing organ shows a significantly expanded auditory fovea that is tuned to the dominant frequency of the female reply to facilitate phonotactic mate finding. This sex-specific auditory fovea is demonstrated in the mechanical and neuronal responses along the tonotopically organized crista acustica by laservibrometric and electrophysiological frequency mapping, respectively. Morphometric analysis of the crista acustica revealed an interrupted gradient in organ height solely within this auditory fovea region, whereas all other anatomical parameters decrease continuously from proximal to distal. Combining behavioural, anatomical, biomechanical and neurophysiological information, we demonstrate evidence of a pronounced auditory fovea as a sex-specific adaptation of an insect hearing organ for intraspecific acoustic communication.

Morphological basis for a tonotopic design of an insect ear.

The tonotopically organized hearing organs of bushcrickets provide the opportunity for a detailed correlation of morphological and structural properties within hearing organs that are needed to establish tonotopic gradients. In the present study of a tonotopic insect hearing organ, we combine mechanical measurements of sound-induced hearing organ motion and detailed anatomical investigations to explore the anatomical basis of tonotopy. We compare mechanical data of frequency responses along the auditory organ to several anatomical parameters. Low frequency responses are related to larger organ and cap cell size in the proximal part of the hearing organ while in the distal part of the organ, small organ and cap cell size is related to high-frequency representation. However, the correlation between organ and cap cell size with continuous frequency representation along the organ is not very tight. Instead, the height of the organ and the corresponding length of the sensory dendrites are best correlated to tonotopic frequency representation. The sensory dendrite contains a ciliary root with a pronounced cross-banding of electron-dense material that should be important for the stiffness of the dendrite. The geometry of surrounding structures like the hemolymph channel and the acoustic trachea as well as the extension of the tectorial membrane are not correlated to the tonotopy. We provide evidence that tonotopy in the bushcricket hearing organ may depend on the size of ciliary structures. In particular, the ciliary root of the sensory cells is a likely cellular basis of tonotopy.

Directional hearing in insects with internally coupled ears.

Compared to all other hearing animals, insects are the smallest ones, both in absolute terms and in relation to the wavelength of most biologically relevant sounds. The ears of insects can be located at almost any possible body part, such as wings, legs, mouthparts, thorax or abdomen. The interaural distances are generally so small that cues for directional hearing such as interaural time and intensity differences (IITs and IIDs) are also incredibly small, so that the small body size should be a strong constraint for directional hearing. Yet, when tested in behavioral essays for the precision of sound source localization, some species demonstrate hyperacuity in directional hearing and can track a sound source deviating from the midline by only [Formula: see text]-[Formula: see text]. They can do so by using internally coupled ears, where sound pressure can act on both sides of a tympanic membrane. Here we describe their varying anatomy and mode of operation for some insect groups, with a special focus on crickets, exhibiting probably one of the most sophisticated of all internally coupled ears in the animal kingdom.

Hearing in Insects.

Insect hearing has independently evolved multiple times in the context of intraspecific communication and predator detection by transforming proprioceptive organs into ears. Research over the past decade, ranging from the biophysics of sound reception to molecular aspects of auditory transduction to the neuronal mechanisms of auditory signal processing, has greatly advanced our understanding of how insects hear. Apart from evolutionary innovations that seem unique to insect hearing, parallels between insect and vertebrate auditory systems have been uncovered, and the auditory sensory cells of insects and vertebrates turned out to be evolutionarily related. This review summarizes our current understanding of insect hearing. It also discusses recent advances in insect auditory research, which have put forward insect auditory systems for studying biological aspects that extend beyond hearing, such as cilium function, neuronal signal computation, and sensory system evolution.

Computational themes of peripheral processing in the auditory pathway of insects.

Hearing in insects serves to gain information in the context of mate finding, predator avoidance or host localization. For these goals, the auditory pathways of insects represent the computational substrate for object recognition and localization. Before these higher level computations can be executed in more central parts of the nervous system, the signals need to be preprocessed in the auditory periphery. Here, we review peripheral preprocessing along four computational themes rather than discussing specific physiological mechanisms: (1) control of sensitivity by adaptation, (2) recoding of amplitude modulations of an acoustic signal into a labeled-line code (3) frequency processing and (4) conditioning for binaural processing. Along these lines, we review evidence for canonical computations carried out in the peripheral auditory pathway and show that despite the vast diversity of insect hearing, signal processing is governed by common computational motifs and principles.

From microseconds to seconds and minutes-time computation in insect hearing.

The computation of time in the auditory system of insects is of relevance at rather different time scales, covering a large range from microseconds to several minutes. At the one end of this range, only a few microseconds of interaural time differences are available for directional hearing, due to the small distance between the ears, usually considered too small to be processed reliably by simple nervous systems. Synapses of interneurons in the afferent auditory pathway are, however, very sensitive to a time difference of only 1–2 ms provided by the latency shift of afferent activity with changing sound direction. At a much larger time scale of several tens of milliseconds to seconds, time processing is important in the context species recognition, but also for those insects where males produce acoustic signals within choruses, and the temporal relationship between song elements strongly deviates from a random distribution. In these situations, some species exhibit a more or less strict phase relationship of song elements, based on phase response properties of their song oscillator. Here we review evidence on how this may influence mate choice decisions. In the same dimension of some tens of milliseconds we find species of katydids with a duetting communication scheme, where one sex only performs phonotaxis to the other sex if the acoustic response falls within a very short time window after its own call. Such time windows show some features unique to insects, and although its neuronal implementation is unknown so far, the similarity with time processing for target range detection in bat echolocation will be discussed. Finally, the time scale being processed must be extended into the range of many minutes, since some acoustic insects produce singing bouts lasting quite long, and female preferences may be based on total signaling time.

Useless hearing in male Emblemasoma auditrix (Diptera, Sarcophagidae)--a case of intralocus sexual conflict during evolution of a complex sense organ?

Sensory modalities typically are important for both sexes, although sex-specific functional adaptations may occur frequently. This is true for hearing as well. Consequently, distinct behavioural functions were identified for the different insect hearing systems. Here we describe a first case, where a trait of an evolutionary novelty and a highly specialized hearing organ is adaptive in only one sex. The main function of hearing of the parasitoid fly Emblemasoma auditrix is to locate the host, males of the cicada species Okanagana rimosa, by their calling song. This task is performed by female flies, which deposit larvae into the host. We show that male E. auditrix possess a hearing sense as well. The morphology of the tympanal organ of male E. auditrix is rather similar to the female ear, which is 8% broader than the male ear. In both sexes the physiological hearing threshold is tuned to 5 kHz. Behavioural tests show that males are able to orient towards the host calling song, although phonotaxis often is incomplete. However, despite extensive observations in the field and substantial knowledge of the biology of E. auditrix, no potentially adaptive function of the male auditory sense has been identified. This unique hearing system might represent an intralocus sexual conflict, as the complex sense organ and the behavioural relevant neuronal network is adaptive for only one sex. The correlated evolution of the sense organ in both sexes might impose substantial constraints on the sensory properties of the ear. Similar constraints, although hidden, might also apply to other sensory systems in which behavioural functions differ between sexes.

Insect Hearing: Active Amplification in Tympanal Ears

A new study identifies an active process that resembles the mammalian cochlear amplifier in the tympanal hearing organ of a tree cricket.

If a bird flies in the forest, does an insect hear it?

Birds are major predators of many eared insects including moths, butterflies, crickets and cicadas. We provide evidence supporting the hypothesis that insect ears can function as 'bird detectors'. First, we show that birds produce flight sounds while foraging. Eastern phoebes (Sayornis phoebe) and chickadees (Poecile atricapillus) generate broadband sounds composed of distinct repetitive elements (approx. 18 and 20 Hz, respectively) that correspond to cyclic wing beating. We estimate that insects can detect an approaching bird from distances of at least 2.5 m, based on insect hearing thresholds and sound level measurements of bird flight. Second, we show that insects with both high and low frequency hearing can hear bird flight sounds. Auditory nerve cells of noctuid moths (Trichoplusia ni) and nymphalid butterflies (Morpho peleides) responded in a bursting pattern to playbacks of an attacking bird. This is the first study to demonstrate that foraging birds generate flight sound cues that are detectable by eared insects. Whether insects exploit these sound cues, and alternatively, if birds have evolved sound-reducing foraging tactics to render them acoustically 'cryptic' to their prey, are tantalizing questions worthy of further investigation.

Discovery of a lipid synthesising organ in the auditory system of an insect.

Weta possess typical Ensifera ears. Each ear comprises three functional parts: two equally sized tympanal membranes, an underlying system of modified tracheal chambers, and the auditory sensory organ, the crista acustica. This organ sits within an enclosed fluid-filled channel–previously presumed to be hemolymph. The role this channel plays in insect hearing is unknown. We discovered that the fluid within the channel is not actually hemolymph, but a medium composed principally of lipid from a new class. Three-dimensional imaging of this lipid channel revealed a previously undescribed tissue structure within the channel, which we refer to as the olivarius organ. Investigations into the function of the olivarius reveal de novo lipid synthesis indicating that it is producing these lipids in situ from acetate. The auditory role of this lipid channel was investigated using Laser Doppler vibrometry of the tympanal membrane, which shows that the displacement of the membrane is significantly increased when the lipid is removed from the auditory system. Neural sensitivity of the system, however, decreased upon removal of the lipid–a surprising result considering that in a typical auditory system both the mechanical and auditory sensitivity are positively correlated. These two results coupled with 3D modelling of the auditory system lead us to hypothesize a model for weta audition, relying strongly on the presence of the lipid channel. This is the first instance of lipids being associated with an auditory system outside of the Odentocete cetaceans, demonstrating convergence for the use of lipids in hearing.

Ultra high frequency hearing in a moth

Ultra high frequency hearing in a moth

Hyperacute Directional Hearing and Phonotactic Steering in the Cricket (Gryllus bimaculatus deGeer)

BackgroundAuditory mate or prey localisation is central to the lifestyle of many animals and requires precise directional hearing. However, when the incident angle of sound approaches 0° azimuth, interaural time and intensity differences gradually vanish. This poses a demanding challenge to animals especially when interaural distances are small. To cope with these limitations imposed by the laws of acoustics, crickets employ a frequency tuned peripheral hearing system. Although this enhances auditory directionality the actual precision of directional hearing and phonotactic steering has never been studied in the behaviourally important frontal range.Principal FindingsHere we analysed the directionality of phonotaxis in female crickets (Gryllus bimaculatus) walking on an open-loop trackball system by measuring their steering accuracy towards male calling song presented at frontal angles of incidence. Within the range of ±30°, females reliably discriminated the side of acoustic stimulation, even when the sound source deviated by only 1° from the animal's length axis. Moreover, for angles of sound incidence between 1° and 6° the females precisely walked towards the sound source. Measuring the tympanic membrane oscillations of the front leg ears with a laser vibrometer revealed between 0° and 30° a linear increasing function of interaural amplitude differences with a slope of 0.4 dB/°. Auditory nerve recordings closely reflected these bilateral differences in afferent response latency and intensity that provide the physiological basis for precise auditory steering.ConclusionsOur experiments demonstrate that an insect hearing system based on a frequency-tuned pressure difference receiver achieves directional hyperacuity which easily rivals best directional hearing in mammals and birds. Moreover, this directional accuracy of the cricket's hearing system is reflected in the animal's phonotactic motor response.

Antennal hearing in insects – New findings, new questions

Mosquitoes, certain Drosophila species, and honey bees use Johnston’s organ in their antennae to detect the wing-beat sounds of conspecifics. Recent studies on these insects have provided novel insights into the intricacies of insect hearing and sound communication, with main discoveries including transduction and amplification mechanisms as known from vertebrate hearing, functional and molecular diversifications of mechanosensory cells, and complex mating duets that challenge the frequency-limits of insect antennal ears. This review discusses these recent advances and outlines potential avenues for future research.