Direction-of-arrival estimation for acoustic signals based on direction-dependent parameter tuning of a bioinspired binaural coupling system.

Bioinspired methods for sound source localization offer opportunities for resource reduction as well as concurrent performance improvement in contrast to conventional techniques. Usually, sound source localization requires a large number of microphones arranged in irregular geometries, and thus has high resource requirements in terms of space and data processing. Motivated by biology and using digital signal processing methods, an approach that adapts the coupled hearing system of the flyOrmia ochraceawith a minimally distant two-microphone array is presented. Despite its physiology, the fly is able to overcome physical limitations in localizing low-frequency sound sources. By exploiting the filtering effect of the coupling system, the direction-of-arrival of the sound is determined with two microphones at an intermediate distance of 0.06 m. For conventional beamforming algorithms, these physical limitations would result in degraded localization performance. In this work, the bioinspired coupling system is analyzed and subsequently parameterized direction-sensitive for different directions of incidence of the sound. For the parameterization, an optimization method is presented which can be adopted for excitation with plane as well as spherical sound wave propagation. Finally, the method was assessed using simulated and measured data. For 90% of the simulated scenarios, the correct direction of incidence could be determined with an accuracy of less than 1∘despite the use of a minimal distant two-microphone array. The experiments with measured data also resulted in a correct determination of the direction of incidence, which qualifies the bioinspired method for practical use in digital hardware systems.

Reconsidering tympanal-acoustic interactions leads to an improved model of auditory acuity in a parasitoid fly.

Although most binaural organisms locate sound sources using neurological structures to amplify the sounds they hear, some animals use mechanically coupled hearing organs instead. One of these animals, the parasitoid flyOrmia ochracea(O. ochracea), has astoundingly accurate sound localization abilities. It can locate objects in the azimuthal plane with a precision of 2°, equal to that of humans, despite an intertympanal distance of only 0.5 mm, which is less than1/100th of the wavelength of the sound emitted by the crickets that it parasitizes.O. ochraceaaccomplishes this feat via mechanically coupled tympana that interact with incoming acoustic pressure waves to amplify differences in the signals received at the two ears. In 1995, Mileset aldeveloped a model of hearing mechanics inO. ochraceathat represents the tympana as flat, front-facing prosternal membranes, though they lie on a convex surface at an angle from the flies' frontal and transverse planes. The model works well for incoming sound angles less than±30∘but suffers from reduced accuracy (up to 60% error) at higher angles compared to response data acquired fromO. ochraceaspecimens. Despite this limitation, it has been the basis for bio-inspired microphone designs for decades. Here, we present critical improvements to this classic hearing model based on information from three-dimensional reconstructions ofO. ochracea's tympanal organ. We identified the orientation of the tympana with respect to a frontal plane and the azimuthal angle segment between the tympana as morphological features essential to the flies' auditory acuity, and hypothesized a differentiated mechanical response to incoming sound on the ipsi- and contralateral sides that depend on these features. We incorporated spatially-varying model coefficients representing this asymmetric response, making a new quasi-two-dimensional (q2D) model. The q2D model has high accuracy (average errors of under 10%) for all incoming sound angles. This improved biomechanical model may inform the design of new microscale directional microphones and other small-scale acoustic sensor systems.

Behavioral responses of a parasitoid fly to rapidly evolving host signals.

Animals eavesdrop on signals and cues generated by prey, predators, hosts, parasites, competing species, and conspecifics, and the conspicuousness of sexual signals makes them particularly susceptible. Yet, when sexual signals evolve, most attention is paid to impacts on intended receivers (potential mates) rather than fitness consequences for eavesdroppers. Using the rapidly evolving interaction between the Pacific field cricket, Teleogryllus oceanicus, and the parasitoid fly, Ormia ochracea, we asked how parasitoids initially respond to novel changes in host signals. We recently discovered a novel sexual signal, purring song, in Hawaiian populations of T. oceanicus that appears to have evolved because it protects the cricket from the parasitoid while still allowing males to attract female crickets for mating. In Hawaii, there are no known alternative hosts for the parasitoid, so we would expect flies to be under selection to detect and attend to the new purring song. We used complementary field and laboratory phonotaxis experiments to test fly responses to purring songs that varied in many dimensions, as well as to ancestral song. We found that flies strongly prefer ancestral song over purring songs in both the field and the lab, but we caught more flies to purring songs in the field than reported in previous work, indicating that flies may be exerting some selective pressure on the novel song. When played at realistic amplitudes, we found no preferences-flies responded equally to all purrs that varied in frequency, broadbandedness, and temporal measures. However, our lab experiment did reveal the first evidence of preference for purring song amplitude, as flies were more attracted to purrs played at amplitudes greater than naturally occurring purring songs. As purring becomes more common throughout Hawaii, flies that can use purring song to locate hosts should be favored by selection and increase in frequency.

A High-Precision Algorithm for DOA Estimation Using a Long-Baseline Array Based on the Hearing Mechanism of the Ormia Ochracea.

Inspired by the Ormia Ochracea hearing mechanism, a new direction of arrival estimation using multiple antenna arrays has been considered in spatially colored noise fields. This parasitoid insect can locate s cricket's position accurately using the small distance between its ears, far beyond the standard array with the same aperture. This phenomenon can be understood as a mechanical coupled structure existing between the Ormia ears. The amplitude and phase differences between the received signals are amplified by the mechanical coupling, which is functionally equivalent to a longer baseline. In this paper, we regard this coupled structure as a multi-input multi-output filter, where coupling exists between each pair of array elements. Then, an iterative direction-finding algorithm based on fourth-order cumulants with fully coupled array is presented. In this manner, the orientation of the mainlobe can direct at the incident angle. Hence, the direction-finding accuracy can be improved in all possible incident angles. We derive the Cramér-Rao lower bound for our proposed algorithm and validate its performance based on simulations. Our proposed DOA estimation algorithm is superior to the existing biologically inspired direction-finding and fourth-order cumulants-based estimation algorithms.

Mathematical Analysis and Micro-Spacing Implementation of Acoustic Sensor Based on Bio-Inspired Intermembrane Bridge Structure.

A biomimetic study on the auditory localization mechanism of Ormia ochracea was performed to improve the localization ability of small acoustic systems. We also present a microscale implementation of an acoustic localization device inspired by the auditory organ of the parasitic O. ochracea. The device consists of a pair of circular membranes coupled together with an elastic beam. The coupling serves to amplify the difference in magnitude and phase between the two membranes' responses as the incident angle of the sound changes, allowing directional information to be deduced from the coupled device response. The research results show that the intermembrane bridge structure improves the sound source localization and directional weak acoustic signal acquisition of sound detectors. The recognition rate of the phase difference and amplitude ratio was greatly improved. The theoretical resolution of the incident angle of the sound source can reach 2° at a phase difference recognition rate of 5°. The sound source's optimal identification frequency range for the coupling device based on the intermembrane bridge bionic structure is 300 Hz to 1500 Hz.

Immunogenetic and tolerance strategies against a novel parasitoid of wild field crickets.

Among the parasites of insects, endoparasitoids impose a costly challenge to host defenses because they use their host's body for the development and maturation of their eggs or larvae, and ultimately kill the host. Tachinid flies are highly specialized acoustically orienting parasitoids, with first instar mobile larvae that burrow into the host's body to feed. We investigated the possibility that Teleogryllus oceanicus field crickets employ postinfestation strategies to maximize survival when infested with the larvae of the parasitoid fly Ormia ochracea. Using crickets from the Hawaiian Islands of Kauai, where the parasitoid is present, and crickets from the Cook Islands (Mangaia), where the parasitoid is absent, we evaluated fitness consequences of infestation by comparing feeding behavior, reproductive capacity, and survival of males experimentally infested with O. ochracea larvae. We also evaluated mechanisms underlying host responses by comparing gene expression in crickets infested with fly larvae for different lengths of time with that of uninfested control crickets. We observed weak population differences in fitness (spermatophore production) and survival (total survival time postinfestation). These responses generally did not show an interaction between population and the number of larva hosts carried or by host body condition. Gene expression patterns also revealed population differences in response to infestation, but we did not find evidence for consistent differences in genes associated with immunity or stress response. One possibility is that any postinfestation evolved resistance does not involve genes associated with these particular functional categories. More likely, these results suggest that coevolution with the fly does not strongly select for either postinfestation resistance or tolerance of parasitoid larvae in male crickets.

Frequency Invariant Beamforming for a Small-Sized Bi-Cone Acoustic Vector-Sensor Array.

In this work, we design a small-sized bi-cone acoustic vector-sensor array (BCAVSA) and propose a frequency invariant beamforming method for the BCAVSA, inspired by the Ormia ochracea's coupling ears and harmonic nesting. First, we design a BCAVSA using several sets of cylindrical acoustic vector-sensor arrays (AVSAs), which are used as a guide to construct the constant beamwidth beamformer. Due to the mechanical coupling system of the Ormia ochracea's two ears, the phase and amplitude differences of acoustic signals at the bilateral tympanal membranes are magnified. To obtain a virtual BCAVSA with larger interelement distances, we then extend the coupling magnified system into the BCAVSA by deriving the expression of the coupling magnified matrix for the BCAVSA and providing the selecting method of coupled parameters for fitting the underwater signal frequency. Finally, the frequency invariant beamforming method is developed to acquire the constant beamwidth pattern in the three-dimensional plane by deriving several sets of the frequency weighted coefficients for the different cylindrical AVSAs. Simulation results show that this method achieves a narrower mainlobe width compared to the original BCAVSA. This method has lower sidelobes and a narrower mainlobe width compared to the coupling magnified bi-cone pressure sensor array.

Background noise disrupts host-parasitoid interactions.

The soundscape serves as a backdrop for acoustic signals dispatched within and among species, spanning mate attraction to parasite host detection. Elevated background sound levels from human-made and natural sources may interfere with the reception of acoustic signals and alter species interactions and whole ecological communities. We investigated whether background noise influences the ability of the obligate parasitoid Ormia ochracea to locate its host, the variable field cricket (Gryllus lineaticeps). As O. ochracea use auditory cues to locate their hosts, we hypothesized that higher background noise levels would mask or distract flies from cricket calls and result in a decreased ability to detect and navigate to hosts. We used a field manipulation where fly traps baited with playback of male cricket advertisement calls were exposed to a gradient of experimental traffic and ocean surf noise. We found that increases in noise amplitude caused a significant decline in O. ochracea caught, suggesting that background noise can influence parasitoid-host interactions and potentially benefit hosts. As human-caused sensory pollution increases globally, soundscapes may influence the evolution of tightly co-evolved host-parasitoid relationships. Future work should investigate whether female cricket phonotaxis towards males is similarly affected by noise levels.

A Biomimetic Miniaturized Microphone Array for Sound Direction Finding Applications Based on a Phase-Enhanced Electrical Coupling Network.

In this research, we proposed a miniaturized two-element sensor array inspired by Ormia Ochracea for sound direction finding applications. In contrast to the convectional approach of using mechanical coupling structures for enlarging the intensity differences, we exploited an electrical coupling network circuit composed of lumped elements to enhance the phase differences and extract the optimized output power for good signal-to-noise ratio. The separation distance between two sensors could be reduced from 0.5 wavelength to 0.1 wavelength 3.43 mm at the operation frequency of 10 kHz) for determining the angle of arrivals. The main advantages of the proposed device include low power losses, flexible designs, and wide operation bandwidths. A prototype was designed, fabricated, and experiments examined within a sound anechoic chamber. It was demonstrated that the proposed device had a phase enhancement of 110 ∘ at the incident angle of 90 ∘ and the normalized power level of -2.16 dB at both output ports. The received power levels of our device were 3 dB higher than those of the transformer-type direction-finding system. In addition, our proposed device could operate in the frequency range from 8 kHz to 12 kHz with a tunable capacitor. The research results are expected to be beneficial for the compact sonar or radar systems.

How spatial release from masking may fail to function in a highly directional auditory system.

Spatial release from masking (SRM) occurs when spatial separation between a signal and masker decreases masked thresholds. The mechanically-coupled ears of Ormia ochracea are specialized for hyperacute directional hearing, but the possible role of SRM, or whether such specializations exhibit limitations for sound source segregation, is unknown. We recorded phonotaxis to a cricket song masked by band-limited noise. With a masker, response thresholds increased and localization was diverted away from the signal and masker. Increased separation from 6° to 90° did not decrease response thresholds or improve localization accuracy, thus SRM does not operate in this range of spatial separations. Tympanal vibrations and auditory nerve responses reveal that localization errors were consistent with changes in peripheral coding of signal location and flies localized towards the ear with better signal detection. Our results demonstrate that, in a mechanically coupled auditory system, specialization for directional hearing does not contribute to source segregation.

Parasitoid infestation changes female mating preferences.

Females often adjust their mating preference to environmental and social conditions. This plasticity of preference can be adaptive for females and can have important consequences for the evolution of male traits. While predation and parasitism are widespread, their effects on female preferences have rarely been investigated. Females of the cricket Gryllus lineaticeps are parasitized by the parasitoid fly Ormia ochracea. Infestation with fly larvae substantially reduces female life span and thus reproductive opportunities of the cricket. Both female G. lineaticeps and flies orient to male song and both prefer male songs with faster chirp rates to songs with slower chirp rates. We tested the effect of parasitic infestation on female responsiveness to male song and female chirp rate preferences. The proportion of individuals responding to male songs did not differ between infested and control females. Control females preferred intermediate chirp rates to slow chirp rates and did not discriminate between fast and intermediate chirp rates. In contrast, infested females showed no preferences in the choice trials, indicating reduced chirp rate selectivity. This plasticity in female preferences may be adaptive; parasitized females may have a higher probability of reproducing before they are killed by the parasitoids if they are less selective (i.e. there will be a larger pool of males considered acceptable). The change in preferences suggests relaxed selection on male chirp rate during times of parasitism.

Eavesdropping parasitoids do not cause the evolution of less conspicuous signalling behaviour in a field cricket.

Males of many species produce conspicuous mating signals to attract females, but these signals can also attract eavesdropping predators and parasites. Males are thus expected to evolve signalling behaviours that balance the sexual selection benefits and the natural selection costs. In the variable field cricket, Gryllus lineaticeps, males sing to attract females, but these songs also attract the lethal parasitoid fly Ormia ochracea. The flies use male crickets as hosts for their larvae, primarily search for hosts during a 2 h period following sunset and prefer the same song types as female crickets. We tested whether males from high-risk populations reduce the risk of parasitism by singing less frequently or by shifting their singing activity to a time of the night when the risk of parasitism is low. We compared male singing activity and its temporal pattern between six high-risk and six low-risk populations that were reared in a common environment. There was no effect of parasitism risk on either total male singing activity or the temporal pattern of male singing activity. Males from high-risk populations thus sang as frequently as males from low-risk populations. These results suggest that sexual selection on male singing behaviour may be substantially stronger in high-risk populations than in low-risk populations. It is possible that other traits may have evolved to reduce parasitism risk without compromising mate attraction.

CALLING SONGS OF FIELD CRICKETS (TELEOGRYLLUS OCEANICUS) WITH AND WITHOUT PHONOTACTIC PARASITOID INFECTION.

The field cricket Teleogryllus oceanicus has been introduced to Hawaii, where it is parasitized by an acoustically orienting parasitoid fly, Ormia ochracea. Previous work showed that call parameters from parasitized populations differ from those in unparasitized populations in a direction expected if selection by flies is occurring. Here we examined songs of males collected in the field and compare calling song characters of crickets later found to harbor parasitoid larvae with those of males free of parasitoids. The two groups differ significantly in several song characteristics, particularly the trill-like long chirp given at the beginning of each song. Males with longer long chirps containing shorter interpulse intervals are more likely to be parasitized, suggesting that the flies find such males more attractive. Depending on the traits females prefer, sexual selection may oppose natural selection in altering T. oceanicus song in parasitized populations.