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RESEARCH ARTICLE Mechanical Filtering for Narrow-Band Hearing in the Weta

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RESEARCH ARTICLE Mechanical Filtering for Narrow-Band Hearing in the Weta 778 The Journal of Experimental Biology 214, 778-785 © 2011. Published by The Company of Biologists Ltd doi:10.1242/jeb.050187 RESEARCH ARTICLE Mechanical filtering for narrow-band hearing in the weta Kathryn Lomas1, Fernando Montealegre-Z2,*, Stuart Parsons1, Larry H. Field3 and Daniel Robert2 1University of Auckland, School of Biological Sciences, Private Bag 92019, Auckland 1142, New Zealand, 2School of Biological Sciences, University of Bristol, Woodland Road, Bristol BS8 1UG, UK and 3School of Biological Sciences, University of Canterbury, Edward Percival Field Station, The Esplanade, Kaikoura 7300, New Zealand *Author for correspondence ([email protected]) Accepted 22 November 2010 SUMMARY This paper constitutes a major attempt to associate tympanic deflections with the mechanoreceptor organ location in an acoustic insect. The New Zealand tree weta (Hemideina thoracica) has tympanal ears located on each of the prothoracic tibiae. The tympana exhibit a sclerotized oval plate, membranous processes bulging out from the tibial cuticle and many loosely suspended ripples. We used microscanning laser Doppler vibrometry to determine how such a tympanal membrane vibrates in response to sound and whether the sclerotized region plays a role in hearing. The tympanum displays a single resonance at the calling frequency of the male, an unusual example of an insect tympana acting as a narrow bandpass filter. Both tympana resonate in phase with the stimulus and with each other. Histological sections show that the tympanal area is divided into two distinct regions, as in other ensiferans. An oval plate lies in the middle of a thickened region and is surrounded by a transparent and uniformly thin region. It is hinged dorsally to the tympanal rim and thus resembles the model of a ‘hinged flap’. The thickened region appears to act as a damping mass on the oscillation of the thin region, and vibration displacement is reduced in this area. The thinner area vibrates with higher amplitude, inducing mechanical pressure on the dorsal area adjacent to the crista acustica. We present a new model showing how the thickened region might confer a mechanical gain onto the activation of the crista acustica sensory neurons during the sound-induced oscillations. Supplementary material available online at http://jeb.biologists.org/cgi/content/full/214/5/778/DC1 Key words: weta, laser vibrometry, ensiferan ear, tympanum vibration, mechanical tuning. INTRODUCTION thicker membrane than the Tettigoniidae (Ball and Field, 1981; The auditory systems of insects are typically adapted to be most Bangert et al., 1998). A further difference is that the tympanum of sensitive to sounds that are significant for survival and/or tree weta does not appear to be taut, and conspicuous ripples radiate reproductive success. Such sounds include conspecific signals and out from a sclerotized thickened area (Ball and Field, 1981), referred incidental noises generated by predators and/or prey. The range of here to as the inner plate. The tettigoniid tympanum tends to be frequencies detectable by insect species can be relatively broad (Hill taut, as are those of most other insects. Given the size and thickness and Oldfield, 1981; Hoy et al., 1982; Mhatre et al., 2009; Yager of the weta tympanal membranes, they might be expected to have and Hoy, 1986) or quite narrow (Field et al., 1980; Mason, 1991) low responsiveness for the transmission of sound waves (Beranek, (present study). The ultimate reasons favouring broad or narrow 1954). frequency selectivity and the biophysical and neural mechanisms Although it has been established that tree weta hear well [peak subtending such selectivity are still only partially understood. It is sensitivity 2–3kHz, threshold at 34dB sound pressure level (SPL)] remarkable that insects with narrow-band intraspecific (Field et al., 1980), it is still unclear how sound is transduced given communication signals (such as field crickets) do not necessarily the suggested large compliance of the tympanal membrane. A model display narrow-band tuning in their auditory or mechanical that may apply to this system has been described by Bangert et al. sensitivity. (Bangert et al., 1998) for the tettigoniids. Their hinge-door model The endemic tree weta of New Zealand (Orthoptera, Ensifera, describes equally sized membranes, both moving in anti-phase to Anostostomatidae, genus Hemideina) has typical ensiferan each other. Sound pressure in the underlying tracheal chambers prothoracic tibial ears. Superficially, the morphology and anatomy pushes out the inner plates of the tympana (acting as hinged flaps), of their ears resembles the relatively well-known tympanal ear of causing stretching of the crista acustica (CA). the Tettigoniidae and the lesser-known ear of the Haglidae (Mason, The anatomical observations of Ball and Field (Ball and Field, 1991). All three groups have two equally sized tympana located on 1981) and the model proposed by Bangert et al. (Bangert et al., each prothoracic tibia. Comparison between the better-known 1998) together suggest a functional arrangement – to be tested in Tettigoniidae and the tree weta shows that they also have similar the weta – that would rely on a putatively similar hinge-like underlying tracheal chambers (tympanal vesicles) and associated mechanical response. To document the mechanics of the weta receptor organs. However, a marked difference exists in the size tympanal system with sufficient accuracy and evaluate its function and thickness of the tympanal membranes, with weta having a larger, in hearing, we undertook a renewed morphological and physiological THE JOURNAL OF EXPERIMENTAL BIOLOGY Hearing in the weta 779 study and performed high-resolution vibration analysis. The weta spontaneous rate, plus one deviation in two out of three recordings. tympanum displays a tuned mechanical response that is distinct from The spontaneous rate was determined from recordings 0–5ms pre- that of a homogenous membrane. Tympanal deflection shapes reveal stimulus. Thresholds were confirmed using the headphone method non-symmetrical patterns introduced by the presence of the stiff described by Autrum (Autrum, 1941). inner plate. The auditory function of this unusually thick, loosely Stimuli presented were 40ms tones, decreasing in intensity, with suspended and heterogeneous tympanal membrane is discussed in 0.4ms rise and fall times, produced with a TDT RA6 processor in the context of the acoustic communication of the weta. 1kHz increments between 1 and 60kHz. Stimuli were presented ipsilateral to the recorded nerve in random order. Amplitude was MATERIALS AND METHODS measured by recording tones at position of preparation using a Animals 0.25inch condenser microphone (Brüel & Kjær 4939, Nærum, Adult male and female Hemideina thoracia (White 1846) were Denmark) and calibrating with a Brüel & Kjær acoustical calibrator collected from around Auckland, New Zealand, in October 2008. (type 421; 90dB SPL at 1000Hz). Animals were kept in a 1ϫ1ϫ1m enclosure and provided with a diet of New Zealand native plant material. Mechanical measurements Thirty-two H. thoracica were transported to the University of Bristol, Tympanal morphology UK, where the biomechanical experiments were carried out. Once To examine the morphological characteristics of the tympana, in the UK, animals were placed in plastic boxes and provided with examinations were carried out at the University of Auckland, New a substitute diet of apple and carrot with some lettuce. The Zealand. The two tympana are known as the anterior tympanic temperature was kept at an optimal range for weta (10–20°C). The membrane (ATM) and the posterior tympanic membrane (PTM). experiments did not commence until 1week after the animals arrived, The surface structure of each tympanum was examined by scanning allowing them to acclimatise to their new environment. electron microscopy (SEM). Specimens were prepared by removing Movement of the animals was restricted during laser scans by the forelegs and preserving them in 90% ethanol. They were then firmly attaching the meso-thoracic, meta-thoracic and dorsal side mounted on stubs, dried in a critical point dryer and gold-coated of the thorax to a horizontal brass plate (6ϫ1ϫ16mm) using liquid before being scanned using an environmental scanning electron latex (Magnacraft, Midhurst, UK). The brass plate was connected microscope (FEI Quanta 200 F, FEI, Hillsboro, OR, USA). SEM to a metal rod (150mm long, 8mm diameter) via a thumbscrew, images were digitised using FEI’s standard hardware and software. allowing the preparation to be rotated and tilted into a position where Details of the tympanum structure and thickness were studied the tympanum was perpendicular to the laser beam. Blu-Tack® using transverse and longitudinal sections under a 10ϫ light (Bostik-Findley, Stafford, UK) was wrapped around the rod to microscope. Four tibia were removed and immediately fixed in minimise residual resonant vibrations of the tethering system. The Bouin’s medium overnight, then transferred to cold 10% sucrose forelegs of the animal were secured to a wooden perch that placed (in Millonig’s buffer) for 2h (4°C), transferred to cold 30% sucrose them in a natural standing posture. Animals were not anaesthetised (in Millonig’s buffer) and kept at 4°C until they sank to the bottom during measurements. However, in some cases it was necessary to of the vials (Field, 1993). Specimens were embedded in optimal further restrict movement of the animals. To achieve this, an
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