Structural biomechanics determine spectral purity of bush-cricket calls

Bush-crickets (Orthoptera: Tettigoniidae) generate sound using tegminal stridulation. Signalling effectiveness is affected by the widely varying acoustic parameters of temporal pattern, frequency and spectral purity (tonality). During stridulation, frequency multiplication occurs as a scraper on one wing scrapes across a file of sclerotized teeth on the other. The frequency with which these tooth–scraper interactions occur, along with radiating wing cell resonant properties, dictates both frequency and tonality in the call. Bush-cricket species produce calls ranging from resonant, tonal calls through to non-resonant, broadband signals. The differences are believed to result from differences in file tooth arrangement and wing radiators, but a systematic test of the structural causes of broadband or tonal calls is lacking. Using phylogenetically controlled structural equation models, we show that parameters of file tooth density and file length are the best-fitting predictors of tonality across 40 bush-cricket species. Features of file morphology constrain the production of spectrally pure signals, but systematic distribution of teeth alone does not explain pure-tone sound production in this family

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 elaborated 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 prothoracic 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 approximately 15 dB and a propagation velocity of 255 m/s, 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 modelling the tracheal acoustic behaviour using the finite element method and real 3D geometries of the tracheae of the bush-cricket Copiphora gorgonensis. Taking into account the thermoviscous acoustic-shell interaction on the propagation of sound, we analyse 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

Tenors not sopranos: Bio-mechanical constraints on calling song frequencies in the Mediterranean field cricket.

Male crickets and their close relatives bush-crickets (Gryllidae and Tettigoniidae, respectively; Orthoptera, Ensifera) attract distant females by producing loud calling songs. In both families, sound is produced by stridulation, the rubbing together of their forewings, whereby the plectrum of one wing is rapidly passed over a serrated file on the opposite wing. The resulting oscillations are amplified by resonating wing regions. A striking difference between Gryllids and Tettigonids lies in wing morphology and composition of song frequency: Crickets produce mostly low-frequency (2-8 kHz), pure tone signals with highly bilaterally symmetric wings, while bush-crickets use asymmetric wings for high-frequency (10-150 kHz) calls. The evolutionary reasons for this acoustic divergence are unknown. Here, we study the wings of actively stridulating male field-crickets (Gryllus bimaculatus) and present vibro-acoustic data suggesting a biophysical restriction to low-frequency song. Using laser Doppler vibrometry and brain-injections of the neuroactivator eserine to elicit singing, we recorded the topography of wing vibrations during active sound production. In freely vibrating wings, each wing region resonated differently. When wings coupled during stridulation, these differences vanished and all wing regions resonated at an identical frequency, that of the narrow-band song (~5 kHz). However, imperfections in wing-coupling caused phase shifts between both resonators, introducing destructive interference with increasing phase differences. The effect of destructive interference (amplitude reduction) was observed to be minimal at the typical low frequency calls of crickets, and by maintaining the vibration phase difference below 80°. We show that, with the imperfect coupling observed, cricket song production with two symmetric resonators becomes acoustically inefficient above ~8 kHz. This evidence reveals a bio-mechanical constraint on the production of high-frequency song whilst using two coupled resonators and provides an explanation as to why crickets, unlike bush-crickets, have not evolved to exploit ultrasonic calling songs

Complex wing motion during stridulation in the katydid Nastonotus foreli (Orthoptera: Tettigoniidae: Pseudophyllinae)

Male Katydids (Orthoptera: Tettigoniidae) rub together their specialised forewings to produce sound, a process known as stridulation. During wing closure, a lobe on the anal margin of the right forewing (a scraper), engages with a teeth-covered file on the left forewing. The movement of the scraper across the file produces vibrations which are amplified by a large wing cell adjacent to the scraper, the mirror. Katydids are known to stridulate with either sustained or interrupted sweeps of the file, generating resonant pure-tone (narrowband frequency) or non-resonant (broadband frequencies) calls. However, some species can conserve some purity in their calls despite incorporating discrete pulses and silent intervals. This mechanism is exhibited by many Pseudophyllinae, such as Nastonotus spp., Cocconotus spp., Triencentrus spp. and Eubliastes spp. This study aims to measure and quantify the mechanics of wing stridulation in Nastonotus foreli, a Neotropical katydid that can produce complex, relatively narrowband calls at ≈20kHz. It was predicted that this species will use a stridulatory mechanism involving elastic energy whereby the scraper bends and flicks along the file in periodic bursts. The calling behaviour and wing mechanics of seven males were studied using a combination of technologies (e.g. micro-scanning laser Doppler vibrometry, advanced microscopy, ultrasound-sensitive equipment and optical motion detectors) to quantify wing mechanics and structure. Analysis of recordings revealed no clear relationship between wing velocity and carrier frequency, and a pronounced distinction between wing velocity and scraper velocity during wing closure, suggesting that the scraper experiences considerable deformation. This is characteristic of the elastic scraper mechanism of stridulation. Curiously, N. foreli might have evolved to employ elastic energy to double the duration of the call, despite possessing muscles that can reach velocities high enough to produce the same frequency without the help of elastic energy

The Ander’s organ: A mechanism for Anti-predator Ultrasound in a Relict Orthopteran

The use of acoustics in predator evasion is a widely reported phenomenon amongst invertebrate taxa, but the study of ultrasonic anti-predator acoustics is often limited to the prey of bats. Here, we describe the acoustic function and morphology of a unique stridulatory structure in the relict orthopteran Cyphoderris monstrosa (Ensifera, Hagloidea): the Ander’s organ. This species is one of just eight remaining members of the family Prophalangopsidae, a group with a fossil record of over 90 extinct species widespread during the Jurassic. We reveal that the sound produced by this organ has the characteristics of a broadband ultrasonic anti-predator defence, with a peak frequency of 58 ± 15.5 kHz and a bandwidth of 50 kHz (at 10 dB below peak). Evidence from sexual dimorphism, knowledge on hearing capabilities and assessment of local predators, suggest the signal likely targets ground-dwelling predators. Additionally, we reveal a previously undescribed series of cavities underneath the organ that likely function as a mechanism for ultrasound amplification. Morphological structures homologous in both appearance and anatomical location to the Ander’s organ are observed to varying degrees in 4 of the 7 other extant members of this family, with the remaining 3 yet to be assessed. Therefore, we suggest that such structures may either be more widely present in this ancient family than previously assumed, or have evolved to serve a key function in the long-term survival of these few species, allowing them to outlive their extinct counterparts

Wing resonances in a new dead-leaf-mimic katydid (Tettigoniidae: Pterochrozinae) from the Andean cloud forests

Day-camouflaged leaf-mimic katydids Typophyllum spp. have a remarkable way of evading predators as male and female forewings appear as bite-damaged leaves complete with necrotic spots. As in all other katydids, males produce sound signals to attract females by rubbing their forewings together. The biophysical properties of these special leaf-like forewings remain obscure. Here we study the wing mechanics and resonances of Typophyllum spurioculis, a new species of leaf-mimic katydid with a broad distribution in the Andes from Western Ecuador to the middle Central Cordillera in Colombia. This species performs an unusual laterally directed aposematic display, showing orange spots that simulate eyes at the leg base. At night, males are conspicuous by their loud, audible calling songs, which exhibit two spectral peaks at ca. 7 and 12 kHz. Using micro-scanning laser Doppler vibrometry we find the effective sound radiators of the wings (speculae) vibrate with three modes of vibration, two of which include the frequencies observed in the calling song. Remarkably, this resonance is preserved in the parts of the wings mimicking necrotic leaves, which are in theory not specialised for sound production. The eyespot function is discussed

Chamber music: an unusual Helmholtz resonator for song amplification in a Neotropical bush-cricket (Orthoptera, Tettigoniidae)

Animals use sound for communication, with high-amplitude signals being selected for attracting mates or deterring rivals. High amplitudes are attained by employing primary resonators in sound producing structures to amplify the signal (e.g., avian syrinx). Some species actively exploit acoustic properties of natural structures to enhance signal transmission by using these as secondary resonators (e.g., tree-hole frogs). Male bush-crickets produce sound by tegminal stridulation and often use specialised wing areas as primary resonators. Interestingly, Acanthacara acuta, a Neotropical bush-cricket, exhibits an unusual pronotal inflation, forming a chamber covering the wings. It has been suggested that such pronotal chambers enhance amplitude and tuning of the signal by constituting a (secondary) Helmholtz resonator. If true, the intact system – when stimulated sympathetically with broadband sound – should show clear resonance around the song carrier frequency which should be largely independent of pronotum material, and change when the system is destroyed. Using laser Doppler vibrometry on living and preserved specimens, micro computed tomography, 3D printed models, and finite element modelling, we show that the pronotal chamber not only functions as a Helmholtz resonator due to its intact morphology but also resonates at frequencies of the calling song on itself, making song production a three-resonator system

A narrow ear canal reduces sound velocity to create additional acoustic inputs in a micro-scale 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, CO2). Integrating laser Doppler vibrometry, micro-CT scanning, and numerical analysis on precise 3D 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 CO2 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). New research paths, and implication of findings in avian directional hearing are discussed

Auditory mechanics in a bush-cricket: direct evidence of dual sound inputs in the pressure difference receiver

The ear of the bush-cricket Copiphora gorgonensis consists of a system of paired eardrums (tympana) on each foreleg. In these insects, the ear is backed by an air-filled tube, the acoustic trachea (AT), which transfers sound from the prothoracic acoustic spiracle to the internal side of the eardrums. Both surfaces of the eardrums of this auditory system are exposed to sound, making it a directionally sensitive pressure-difference receiver. A key feature of the AT is its capacity to reduce the velocity of sound propagation and alter the acoustic driving forces at the tympanum. The mechanism responsible for reduction in sound velocity in the AT remains elusive, yet it is deemed to depend on adiabatic or isothermal conditions. To investigate the biophysics of such multiple input ears, we used micro-scanning laser Doppler vibrometry and micro-computed X-ray tomography. We measured the velocity of sound propagation in the acoustic trachea, the transmission gains across auditory frequencies, and the time-resolved mechanical dynamics of the tympanal membranes in Copiphora gorgonensis. Tracheal sound transmission generates a gain of ~15 dB SPL, and a propagation velocity of ca. 255 m/s, a ~25% reduction from free field propagation. Modelling tracheal acoustic behaviour that accounts for thermal and viscous effects, we conclude that reduction in sound velocity within the acoustic trachea can be explained, amongst 34 others, by heat exchange between the sound wave and the tracheal walls