Insect Ears Research Articles

Sensing of sound pressure gradients by C. elegans drives phonotaxis behavior

Despite lacking ears, the nematode C.elegans senses airborne sound and engages in phonotaxis behavior, enabling it to locate and avoid sound sources.1 How worms sense sound, however, is not well understood. Here, we report an interesting observation that worms respond only to sounds emitted by small but not large speakers, indicating that they preferentially respond to localized sound sources. Notably, sounds emitted by small speakers form a sharp sound pressure gradient across the worm body, while sounds from large speakers do not, suggesting that worms sense sound pressure gradients rather than absolute sound pressure. Analysis of phonotaxis behavior, sound-evoked skin vibration, and sound-sensitive neuron activities further support this model. We suggest that the ability to sense sound pressure gradients provides a potential mechanism for worms to distinguish sounds generated by their predators, which are typically small animals, from those produced by large animals or background noise. As vertebrate cochlea and some insect ears can also detect sound pressure gradients, our results reveal that sensing of sound pressure gradients may represent a common mechanism in auditory sensation across animal phyla. VIDEO ABSTRACT.

The chemistry of an insect ear: ionic composition of a liquid-filled ear and haemolymphs of Neotropical katydids.

The purpose of this study is to examine and to compare the ionic composition of the haemolymph and the ear fluid of seven species of katydids (Orthoptera: Tettigoniidae) with the aim of providing from a biochemical perspective a preliminary assessment for an insect liquid contained in the auditory organ of katydids with a hearing mechanism reminiscent of that found in vertebrates. A multi-element trace analysis by inductively coupled plasma optical-emission spectrometry was run for 16 elements for the ear liquid of seven species and the haemolymph of six of them. Based on the obtained results, it can be recognized that the ionic composition is variable among the studied insects, but sodium (Na+), potassium (K+), calcium (Ca2+) and magnesium (Mg2+) are the most prominent of the dissolved inorganic cations. However, the ion concentrations between the two fluids are considerably different and the absence or low concentration of Ca2+ is a noticeable feature in the inner ear liquid. A potential relationship between the male courtship song peak frequency and the total ion (Na+, K+, Mg2+ and Ca2+) concentration of the inner ear liquid is also reported.

Metabolic decline in an insect ear: correlative or causative for age-related auditory decline?

One leading hypothesis for why we lose our hearing as we age is a decrease in ear metabolism. However, direct measurements of metabolism across a lifespan in any auditory system are lacking. Even if metabolism does decrease with age, a question remains: is a metabolic decrease a cause of age-related auditory decline or simply correlative? We use an insect, the desert locust Schistocerca gregaria, as a physiologically versatile model to understand how cellular metabolism correlates with age and impacts on age-related auditory decline. We found that auditory organ metabolism decreases with age as measured fluorometrically. Next, we measured the individual auditory organ's metabolic rate and its sound-evoked nerve activity and found no correlation. We found no age-related change in auditory nerve activity, using hook electrode recordings, and in the electrophysiological properties of auditory neurons, using patch-clamp electrophysiology, but transduction channel activity decreased. To further test for a causative role of the metabolic rate in auditory decline, we manipulated metabolism of the auditory organ through diet and cold-rearing but found no difference in sound-evoked nerve activity. We found that although metabolism correlates with age-related auditory decline, it is not causative. Finally, we performed RNA-Seq on the auditory organs of young and old locusts, and whilst we found enrichment for Gene Ontology terms associated with metabolism, we also found enrichment for a number of additional aging GO terms. We hypothesize that age-related hearing loss is dominated by accumulative damage in multiple cell types and multiple processes which outweighs its metabolic decline.

Physiological changes throughout an insect ear due to age and noise - A longitudinal study

SummaryHearing loss is not unique to humans and is experienced by all animals in the face of wild and eclectic differences in ear morphology. Here, we exploited the high throughput and accessible tympanal ear of the desert locust, Schistocerca gregaria to rigorously quantify changes in the auditory system due to noise exposure and age. In this exploratory study, we analyzed tympanal displacements, morphology of the auditory Müller’s organ and measured activity of the auditory nerve, the transduction current, and electrophysiological properties of individual auditory receptors. This work shows that hearing loss manifests as a complex disorder due to differential effects of age and noise on several processes and cell types within the ear. The “middle-aged deafness” pattern of hearing loss found in locusts mirrors that found for humans exposed to noise early in their life suggesting a fundamental interaction of the use of an auditory system (noise) and its aging.

Bridging the Gap Between Mammal and Insect Ears – A Comparative and Evolutionary View of Sound-Reception

Insects must wonder why mammals have ears only in their head and why they evolved only one common principle of ear design—the cochlea. Ears independently evolved at least 19 times in different insect groups and therefore can be found in completely different body parts. The morphologies and functional characteristics of insect ears are as wildly diverse as the ecological niches they exploit. In both, insects and mammals, hearing organs are constrained by the same biophysical principles and their respective molecular processes for mechanotransduction are thought to share a common evolutionary origin. Due to this, comparative knowledge of hearing across animal phyla provides crucial insight into fundamental processes of auditory transduction, especially at the biomechanical and molecular level. This review will start by comparing hearing between insects and mammals in an evolutionary context. It will then discuss current findings about sound reception will help to bridge the gap between both research fields.

Turnover and activity-dependent transcriptional control of NompC in the Drosophila ear

SummaryAcross their lives, biological sensors maintain near-constant functional outputs despite countless exogenous and endogenous perturbations. This sensory homeostasis is the product of multiple dynamic equilibria, the breakdown of which contributes to age-related decline. The mechanisms of homeostatic maintenance, however, are still poorly understood. The ears of vertebrates and insects are characterized by exquisite sensitivities but also by marked functional vulnerabilities. Being under the permanent load of thermal and acoustic noise, auditory transducer channels exemplify the homeostatic challenge. We show that (1) NompC-dependent mechanotransducers in the ear of the fruit fly Drosophila melanogaster undergo continual replacement with estimated turnover times of 9.1 hr; (2) a de novo synthesis of NompC can restore transducer function in the adult ears of congenitally hearing-impaired flies; (3) key components of the auditory transduction chain, including NompC, are under activity-dependent transcriptional control, likely forming a transducer-operated mechanosensory gain control system that extends beyond hearing organs.

A narrow ear canal reduces sound velocity to create additional acoustic inputs in a microscale insect ear

Located in the forelegs, katydid ears are unique among arthropods in having outer, middle, and inner components, analogous to the mammalian ear. Unlike mammals, sound is received externally via two tympanic membranes in each ear and internally via a narrow ear canal (EC) derived from the respiratory tracheal system. Inside the EC, sound travels slower than in free air, causing temporal and pressure differences between external and internal inputs. The delay was suspected to arise as a consequence of the narrowing EC geometry. If true, a reduction in sound velocity should persist independently of the gas composition in the EC (e.g., air, [Formula: see text]). Integrating laser Doppler vibrometry, microcomputed tomography, and numerical analysis on precise three-dimensional geometries of each experimental animal EC, we demonstrate that the narrowing radius of the EC is the main factor reducing sound velocity. Both experimental and numerical data also show that sound velocity is reduced further when excess [Formula: see text] fills the EC. Likewise, the EC bifurcates at the tympanal level (one branch for each tympanic membrane), creating two additional narrow internal sound paths and imposing different sound velocities for each tympanic membrane. Therefore, external and internal inputs total to four sound paths for each ear (only one for the human ear). Research paths and implication of findings in avian directional hearing are discussed.

Turnover and Activity-Dependent Transcriptional Control of NompC (=TRPN1) in the <i>Drosophila</i> Ear

Across their lives, biological sensors maintain a near-constant functional output despite a plethora of exogenous and endogenous perturbations. This sensory homeostasis is the product of multiple dynamic equilibria, the breakdown of which contributes to age-dependent sensory decline. The molecular mechanisms of homeostatic maintenance, however, are still poorly understood. The ears of vertebrates and insects are characterised by exquisite sensitivities but also marked functional vulnerabilities. Being under the permanent load of both thermal and acoustic noise, auditory transducer channels are prime examples for the homeostatic challenge. We show that (i) NompC-dependent mechanotransducers in the ear of the fruit fly Drosophila melanogaster undergo a continual turnover with estimated half-lives of ≈ 3h; (ii) a de novo synthesis of NompC can restore transducer function in the adult ears of congenitally deafened flies; (iii) key components of the auditory transduction chain, including NompC, are under activity-dependent transcriptional control, likely forming a transducer-operated gain control system.

Overview of Risk Factors and Strategies for Management of Insect-Derived Ear Injury and Aflatoxin Accumulation for Maize Grown in Subtropical Areas of North America

Abstract Pest and disease risk factors causing maize yield and kernel quality issues in subtropical areas of North America (between 35°N and 23.5°N latitude) are reviewed: preharvest Aspergillus flavus (Link) (Deuteromycetes: Moniliales) infection and propagation in maize ears and ear injury principally caused by Helicoverpa zea (Boddie) and Spodoptera frugiperda (J. E. Smith) (Lepidoptera: Noctuidae). Risk is affected by potentially interacting factors of maize genetics, ear feeding with insects, fungal inoculum and growth, and weather (rainfall, temperature, and humidity). This review gives special attention to integration of the most efficient pest and disease management strategy combinations and the potential interaction of insect ear feeding and A. flavus occurrence. Management strategies reviewed include maximizing partial genetic resistance to A. flavus and selection of appropriate hybrids for the area, biological control of A. flavus using non-aflatoxigenic strains, avoiding pests and diseases using cultural practices like early planting, and reducing H. zea and S. frugiperda ear injury using Bt transgenes. Understanding the combined influences and identifying combined management approaches may lead to reduced aflatoxin risk and maintaining yield. This review focuses on subtropical areas of North America because the amount of maize produced in warm environments within or similar to subtropical maize production areas is likely to increase due to projected increases in demand for maize and predicted increases in temperature may increase pest and disease risk.

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.

The Role of the Mechanotransduction Ion Channel Candidate Nanchung-Inactive in Auditory Transduction in an Insect Ear.

Insect auditory receivers provide an excellent comparative resource to understand general principles of auditory transduction, but analysis of the electrophysiological properties of the auditory neurons has been hampered by their tiny size and inaccessibility. Here we pioneer patch-clamp recordings from the auditory neurons of Müller's organ of the desert locust Schistocerca gregaria to characterize dendritic spikes, axonal spikes, and the transduction current. We demonstrate that dendritic spikes, elicited by sound stimuli, trigger axonal spikes, and that both types are sodium and voltage dependent and blocked by TTX. Spontaneous discrete depolarizations summate upon acoustic stimulation to produce a graded transduction potential that in turn elicits the dendritic spikes. The transduction current of Group III neurons of Müller's organ, which are broadly tuned to 3 kHz, is blocked by three ion channel blockers (FM1-43, streptomycin, and 2-APB) that are known to block mechanotransduction channels. We investigated the contribution of the candidate mechanotransduction ion channel Nanchung-Inactive—which is expressed in Müller's organ—to the transduction current. A specific agonist of Nanchung-Inactive, pymetrozine, eliminates the sound-evoked transduction current while inducing a tonic depolarizing current of comparable amplitude. The Nanchung-Inactive ion channels, therefore, have the required conductance to carry the entire transduction current, and sound stimulation appears not to open any additional channels. The application of three mechanotransduction ion channel blockers prevented the pymetrozine-induced depolarizing current. This implies that either Nanchung-Inactive is, or forms part of, the mechanotransduction ion channel or it amplifies a relatively small current (<30 pA) produced by another mechanotransduction ion channel such as NompC.SIGNIFICANCE STATEMENT The mechanically activated ion channel underpinning hearing is not known. We have pioneered intracellular patch-clamp recordings from locust auditory neurons to unravel the role of the candidate mechanotransduction ion channel Nanchung-Inactive in auditory transduction in insects.

Biologically inspired acoustic sensors: From insect ears to miniature microphones

Taking inspiration from insect ears to develop an acoustic device is not new. Research to take inspiration from the highly directional, sub-wavelength, Ormia ochracea fly’s ear to produce miniature directional microphones is well-known. Since the 1990s, researchers have tried to implement Ormia based micro-electro-mechanical systems devices, typically using standard silicon or similar microfabrication. Much of this time has been spent trying to circumvent the fact that Ormia evolved to hear one specific frequency, that of a calling cricket, and so is not a broadband system as you would require for an audio microphone. Further, building a silicon system inspired by the mechanics of insect ears leads to various compromises. This talk will discuss ongoing work at the University of Strathclyde on silicon microfabrication of acoustic devices inspired by the Ormia system. It will focus on efforts to create MEMS microphones designed with multiple resonance frequencies in the human vocal range. It will also descr...

Insect ear biomechanics: Passive and active processes that can inspire acoustic sensors

Biological systems provide an incredible wealth of archetypes that have emerged through evolutionary processes. Hearing organs are a good example of how different solutions, and adaptions, across different animal taxa, can often converge to solve similar sensory problems. Hearing has evolved independently multiple times across the insects, and the diversity of these biological solutions therefore provides a wealth of inspiration for the creation of novel acoustic sensors. Some biological solutions can be considered as purely passive mechanical constructs that accomplish some processing of the incoming sound. This talk will consider examples of this, including the frequency discrimination of the locust ear, and the directionality and wideband response of different moth ears. Several insects also display active hearing processes, whereby energy is used to actively change the hearing response, bearing some similarity to the processes found in the mammalian inner ear. This talk will thus discuss how some moths actively tune their ear, and how the mosquito ear actively utilizes gain and compression. Finally, the talk will discuss some examples of different acoustic sensors from the University of Strathclyde that take inspiration from these passive and active biological processes.

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.

Gating of Acoustic Transducer Channels Is Shaped by Biomechanical Filter Processes

Mechanoelectrical transduction of acoustic signals is the fundamental process for hearing in all ears across the animal kingdom. Here, we performed in vivo laser-vibrometric and electrophysiological measurements at the transduction site in an insect ear (Mecopoda elongata) to relate the biomechanical tonotopy along the hearing organ to the frequency tuning of the corresponding sensory cells. Our mechanical and electrophysiological map revealed a biomechanical filter process that considerably sharpens the neuronal response. We demonstrate that the channel gating, which acts on chordotonal stretch receptor neurons, is based on a mechanical directionality of the sound-induced motion. Further, anatomical studies of the transduction site support our finding of a stimulus-relevant tilt. In conclusion, we were able to show, in an insect ear, that directionality of channel gating considerably sharpens the neuronal frequency selectivity at the peripheral level and have identified a mechanism that enhances frequency discrimination in tonotopically organized ears.

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.

Active amplification in insect ears: mechanics, models and molecules.

Active amplification in auditory systems is a unique and sophisticated mechanism that expends energy in amplifying the mechanical input to the auditory system, to increase its sensitivity and acuity. Although known for decades from vertebrates, active auditory amplification was only discovered in insects relatively recently. It was first discovered from two dipterans, mosquitoes and flies, who hear with their light and compliant antennae; only recently has it been observed in the stiffer and heavier tympanal ears of an orthopteran. The discovery of active amplification in two distinct insect lineages with independently evolved ears, suggests that the trait may be ancestral, and other insects may possess it as well. This opens up extensive research possibilities in the field of acoustic communication, not just in auditory biophysics, but also in behaviour and neurobiology. The scope of this review is to establish benchmarks for identifying the presence of active amplification in an auditory system and to review the evidence we currently have from different insect ears. I also review some of the models that have been posited to explain the mechanism, both from vertebrates and insects and then review the current mechanical, neurobiological and genetic evidence for each of these models.

Prestin is an anion transporter dispensable for mechanical feedback amplification in Drosophila hearing.

In mammals, the membrane-based protein Prestin confers unique electromotile properties to cochlear outer hair cells, which contribute to the cochlear amplifier. Like mammals, the ears of insects, such as those of Drosophila melanogaster, mechanically amplify sound stimuli and have also been reported to express Prestin homologs. To determine whether the D. melanogaster Prestin homolog (dpres) is required for auditory amplification, we generated and analyzed dpres mutant flies. We found that dpres is robustly expressed in the fly’s antennal ear. However, dpres mutant flies show normal auditory nerve responses, and intact non-linear amplification. Thus we conclude that, in D. melanogaster, auditory amplification is independent of Prestin. This finding resonates with prior phylogenetic analyses, which suggest that the derived motor function of mammalian Prestin replaced, or amended, an ancestral transport function. Indeed, we show that dpres encodes a functional anion transporter. Interestingly, the acquired new motor function in the phylogenetic lineage leading to birds and mammals coincides with loss of the mechanotransducer channel NompC (=TRPN1), which has been shown to be required for auditory amplification in flies. The advent of Prestin (or loss of NompC, respectively) may thus mark an evolutionary transition from a transducer-based to a Prestin-based mechanism of auditory amplification.Electronic supplementary materialThe online version of this article (doi:10.1007/s00359-014-0960-9) contains supplementary material, which is available to authorized users.

Selective forces on origin, adaptation and reduction of tympanal ears in insects.

Insect ears evolved many times independently. As a consequence, a striking diversity exists in the location, construction and behavioural implementation of ears. In this review, we first summarise what is known about the evolutionary origin of ears and the presumed precursor organs in the various insect groups. Thereafter, we focus on selective forces for making and keeping an ear: we discuss detecting and localising predators and conspecifics, including establishing new "private" channels for intraspecific communication. More advanced aspects involve judging the distance of conspecifics, or assessing individual quality from songs which makes auditory processing a means for exerting sexual selection on mating partners. We try to identify negative selective forces, mainly in the context of energy expenditure for developing and keeping an ear, but also in conjunction with acoustic communication, which incorporates risks like eavesdropping by predators and parasitoids. We then discuss balancing pressures, which might oppose optimising an ear for a specific task (when it serves different functions, for example). Subsequently, we describe various scenarios that might have led to a reduction or complete loss of ears in evolution. Finally, we describe cases of sex differences in ears and potential reasons for their appearance.

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.