Directional hearing of a cicada: biophysical aspects

The directional hearing of male and female cicadas of the species Tympanistalna gastrica was investigated by means of laser vibrometry. The results show that the tympanic organs act as pressure difference receivers. This mechanism can produce left-right differences of more than 10 dB. The main acoustic inputs to the inner surfaces of the ears are the tympana, in males supplemented by the timbals, and by the third spiracles in females. In addition the hollow abdomen of males seems to play a minor role. Tympanic membrane input is the source of left-right differences in the tympanic vibration velocity at frequencies below 9 kHz in males and below 15–18 kHz in females. The input via the (contralateral) timbal in males is responsible for a null in vibration velocity appearing between 12 and 14 kHz when the sound is coming from the contralateral direction. The highest energy components of the calling song are found in this frequency range. The mechanical sensitivity of the ears depends upon the sex. At low frequencies males are about 10 dB more sensitive than females.     

Physics of directional hearing in the cricket Gryllus bimaculatus

In the cricket ear, sound acts on the external surface of the tympanum and also reaches the inner surface after travelling in at least three pathways in the tracheal system. We have determined the transmission gain of the three internal sound pathways; that is, the change of amplitude and phase angle from the entrances of the tracheal system to the inner surface of the tympanum. In addition, we have measured the diffraction and time of arrival of sound at the ear and at the three entrances at various directions of sound incidence. By combining these data we have calculated how the total driving force at the tympanum depends on the direction of sound. The results are in reasonable agreement with the directionality of the tympanal vibrations as determined with laser vibrometry.At the frequency of the calling song (4.7 kHz), the direction of the sound has little effect on the amplitudes of the sounds acting on the tympanum, but large effects on their phase angles, especially of the sound waves entering the tracheal system at the contralateral side of the body. The master parameter for causing the directionality of the ear in the forward direction is the sound wave entering the contralateral thoracic spiracle. The phase of this sound component may change by 130–140° with sound direction. The transmission of sound from the contralateral inputs is dominated by a very selective high-pass filter, and large changes in amplitude and phase are seen in the transmitted sounds when the sound frequency changes from 4 to 5 kHz. The directionality is therefore very dependent on sound frequency.The transmission gains vary considerably in different individuals, and much variation was also found in the directional patterns of the ears, especially in the effects of sounds from contralateral directions. However, the directional pattern in the frontal direction is quite robust (at least 5 dB difference between the 330° and 30° directions), so these variations have only little effect on how well the individual animals can approach singing conspecifics.Abbreviations CS contralateral spiracle - CT contralateral tympanum - IS ipsilateral spiracle - IT ipsilateral tympanum - P the vectorial sum of the sounds acting on the tympanum     

Directional sensitivity of wind-sensitive giant interneurons in the cave cricket Troglophilus neglectus.

Unlike the situation in most cockroach and cricket species studied so far, the wind-sensitive cerci of the cave cricket Troglophilus neglectus Krauss (Rhaphidophoridae, Orthoptera) are not oriented parallel to the body axis but perpendicular to it. The effects of this difference on the morphology, and directional sensitivity of cercal giant interneurons (GIs), were investigated. In order to test the hypothesis that the 90 degrees change in cercal orientation causes a corresponding shift in directional sensitivity of GIs, their responses in both the horizontal and vertical planes were tested. One ventral and four dorsal GIs (corresponding to GIs 9-1a and 9-2a, 9-3a, 10-2a, 10-3a of gryllid crickets) were identified. The ventral GI 9-1a of Troglophilus differed somewhat from its cricket homologue in its dendritic arborisation and its directional sensitivity in the horizontal plane. The morphology and horizontal directionality of the dorsal GIs closely resembled that of their counterparts in gryllids. In the vertical plane, the directionality of all GIs tested was similar. They were all excited mainly by wind puffs from the axon-ipsilateral quadrant. The results suggest that directional sensitivity to air currents in the horizontal plane is maintained despite the altered orientation of the cerci. This is presumably due to compensatory modifications in the directional pReferences of the filiform hairs.     

Directional hearing in the barn owl (Tyto alba)

Summary The acoustical properties of the external ear of the barn owl (Tyto alba) were studied by measuring sound pressure in the ear canal and outer ear cavity. Under normal conditions, pressure amplification by the external ear reaches about 20 dB between 3–9 kHz but decreases sharply above 10 kHz. The acoustic gain curve of the outer ear cavity alone is close to that of a finite-length exponential horn between 1.2–13 kHz with maximum gain reaching 20 dB between 5–9 kHz. Pressure gain by the facial ruff produces a maximum of 12 dB between 5–8 kHz and decreases rapidly above 9 kHz.The directional sensitivity of the external ear was obtained from pressure measurements in the ear canal. Directivity of the major lobe is explained, to a first approximation, by the sound diffraction properties of a circular aperture. Aperture size is based on the average radius (30 mm) of the open face of the ruff. Above 5 kHz, the external ear becomes highly directional and there is a 26° disparity in elevation between the acoustic axis of the left and right ear. In azimuth, directivity patterns are relocated closer to the midline as frequency increases and the acoustic axis moves at a rate of 20°/octave between 2–13 kHz. Movement of the axis can be explained, to a first approximation, by the acoustical diffraction properties of an obliquely truncated horn, due to the asymmetrical shape of the outer ear cavity.The directional sensitivity of the barn owl ear was studied by recording cochlear microphonic (CM) potentials from the round window membrane. Between 3–9 kHz, CM directivity patterns are clearly different to the directivity patterns of the external ear; CM directionality is abruptly lost above 10 kHz. Above 5 kHz, CM directivity patterns are characterized by an elongated major lobe containing the CM axis, forming a tilted band of high amplitude but low directionality (CM axial plane), closely bordered by minima or nulls. The highest directionality is found in theCM directional plane, approximately perpendicular to the CM axial plane. The left and right ear axial planes are symmetrical about the interaural midline (tilted 12° to the right of the midline of the head) and inclined by an average of 60° to the left and right respectively. In azimuth, the CM axis moves towards the midline at a rate of 37°/octave as frequency increases from 2–9 kHz, crossing into contralateral space near 7 kHz. In the CM directional plane, the directivity of the major lobe suggests that a pressure gradient may occur at the TM. The region of frontal space mapped by movement of the CM axis in azimuth closely matches the angle of sound incidence which would be expected to produce the maximum driving pressure at the TM. It is suggested that acoustical interference at the TM results from sound transmission through the interaural canal and therefore the ear is inherently directional. It is proposed that ear directionality in the barn owl may be explained by the combined effect of sound diffraction by the outer ear cavity and a pressure gradient at the TM.Abbreviations CM cochlear microphonic - RMS root mean square - SPL sound pressure level - TM tympanic membrane     

Hyperacute directional hearing and phonotactic steering in the cricket (Gryllus bimaculatus deGeer)

Background

Auditory 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 Findings

Here 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.

Conclusions

Our 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.     

Directional hearing in the gray tree frog Hyla versicolor: Eardrum vibrations and phonotaxis

1. We used laser vibrometry to study the vibrational frequency response of the eardrum of female gray tree frogs for different positions of the sound source in three-dimensional space. Furthermore, we studied the accuracy of 3-D phonotaxis in the same species for sounds with different frequency contents. 2. The directionality of the eardrum was most pronounced in a narrow frequency range between 1.3 and 1.8 kHz. 3. The average 3-D, horizontal and vertical jump error angles for phonotactic approaches with a sound similar to the natural advertisement call (1.1 and 2.2 kHz frequency components) were 23 degrees, 19 degrees and 12 degrees, respectively. 4. 3-D jump error angle distributions for the 1.4 + 2.2 kHz, 1.0 kHz and 2.0 kHz sounds were not significantly different from that for the 1.1 + 2.2 kHz sound. 5. The average 3-D jump error angle for the 1.4 kHz sound was 36 degrees, and the distribution was significantly different from that for the 1.1 + 2.2 kHz sound. Hence, phonotactic accuracy was poorer in the frequency range of maximum eardrum directionality. 6. Head scanning was not observed and is apparently unnecessary for accurate sound localization in three-dimensional space. 7. Changes in overall sound pressure level experienced by the frog during phonotactic approaches are not an important cue for sound localization.     

Directional hearing of cod (Gadus morhua) under approximate free field conditions

Summary The cod,Gadus morhua L., can hear the direction of a sound source of 75 Hz in the transversal plane. At the experimental site in the middle of a fjord, local depth 35 m, the sound sources were situated at radial distances of 4 to 5.3 m from the subject in its netting cage. Both in two-alternative and four alternative choice experiments, in which an acoustic discrimination of separate similar sound sources was required, reward conditioning yielded positive results. The bearing of the sound source was decisive for the discrimination and not the identity of the sound sources used (intensity or timbre deviations). If the reverberation characteristics of the fjord at the receiving point were strongly dependent on the spatial position of the source, the results of the choice experiments might represent a demonstration of pseudo-directional hearing. However, from acoustic measurements of the time averages of the sound parameters such an anisotropy for sources with different bearing was not apparent (Fig. 5). Furthermore, in a well-trained cod, in which the pars inferior of only one single labyrinth was put out of function by surgery, the discrimination of the bearing of the sound sources was abolished but not the detection of sound as such (see Table 5). Detection of the direction of the sound therefore seems to be a function of the labyrinths and not of the lateral line system (directionalhearing). Estimates are given of the minimal angle that can be distinguished (about 22° for a 50% detectability likelihood; Fig. 6), and of the minimal acoustic level necessary for acoustic orientation (about — 13 dB re 1 bar; see Fig. 9). Finally an extension to an existing detection model of directional hearing is proposed. It receives empirical support in the next paper (Schuijf and Buwalda, 1975).Professor S. Dijkgraaf's readiness to develop the necessary operations and perform them in Norway in 1971 and 1972 is gratefully acknowledged. I thank Mr. G. Aase, Mr. K. Olsen and Dr. G. Sætersdal, Fiskeridirektoratets Havforskningsinstitutt (Bergen, Norway), for offering facilities to continue Kjell Olsen's study on directional responses of cod to sound. The contributions and the enormous efforts of my former student companions Drs M. A. van Arkel and Drs. M. E. Siemelink were decisive for success in the field. Guests from Utrecht supported the project in different directions, especially in constructing. I am grateful to Drs. R. J. A. Buwalda, Prof. S. Dijkgraaf, Drs. E. Meelis (statistics), Dr. F. J. Verheijen and Ir. D. W. van Wulfften Palthe (acoustics), all of whom made valuable comments on various aspects of the paper, and to Drs. J. W. Baretta for his aid enabling a quick start in 1971. The Netherlands Organization for the Advancement of Pure Research (Z.W.O.) for this study financed two journies to Norway and one to Scotland.     

Male dominance and immunocompetence in a field cricket

Female preference for dominant males has been found in manyspecies, and it is generally thought that winners of male-malecompetition are of superior quality. Success in contests probablydepends on male condition and overall health. Thus, femalescould avoid infection and gain genetic benefits in terms ofmore viable offspring by mating with dominant males. In thepresent study, we tested whether dominant males of the Mediterraneanfield cricket, Gryllus bimaculatus, had higher immunocompetencethan did their subordinates in experimental trials. We foundthat dominant males had better immune defense, as indicatedby significantly higher encapsulation rate and lytic activity,than did subordinate males of the same size. Dominant maleswere also more successful in obtaining matings, but this wasmeasured nonindependently of dominance status. Our results suggestthat a male's dominance status and success in fights may indicatehis immunocompetence to females.     

Seminal fluid affects sperm viability in a cricket

Recent studies have suggested that males may vary the quality of their ejaculates in response to sperm competition, although the mechanisms by which they do so remain unclear. The viability of sperm is an important aspect of ejaculate quality that determines competitive fertilization success in the field cricket Teleogryllus oceanicus. Using in vitro mixtures of sperm and seminal fluid from pairs of male crickets, we show that seminal fluid can affect the viability of sperm in this species. We found that males who invest greatly in the viability of their own sperm can enhance the viability of rival sperm, providing the opportunity for males to exploit the investments in sperm competition made by their rivals. Transitive effects of seminal fluids across the ejaculates of different males are expected to have important implications for the dynamics of male investments in sperm competition.     

The quantitative genetics of growth in a field cricket

Because of its relationship with both development time and adult size, the rate of growth in determinately growing organisms is an important aspect of their life histories. We reared sixty-nine families of Gryllus pennsylvanicus derived from a natural population and found significant genetic variation in growth rate as estimated by the slope of linearized growth trajectories. We found no evidence for a genetic tradeoff between rate of growth and survival, nor rate of growth and fecundity. In principle, adult size may be determined both by the rate of growth and the time taken by the nymphs to develop. Our data indicate that variation in adult size is explained by variation in growth rate, not by variation in development time. We conclude with a discussion of the plausible explanations for the presence of genetic variation in growth rate in this natural population.     

Condition dependence of female choosiness in a field cricket

Females generally choose mates that produce the loudest, brightest or most elaborate sexual displays, and these costly male displays are predicted to be condition dependent. However, mate choice itself is a costly behaviour also expected to be condition dependent. Male fall field crickets, Gryllus pennsylvanicus, produce a conspicuous long‐distance calling song that attracts females and is condition dependent. In this study, we tested the condition dependence of female preferences (preference function and choosiness) for male calling effort in G. pennsylvanicus. We manipulated female condition by raising crickets from hatching on either a low‐ or high‐quality diet. In a series of two‐speaker phonotaxis trials, both low‐ and high‐condition females preferred playbacks reflecting greater calling effort. However, relative to low‐condition females, high‐condition females took significantly longer to make a choice, were more likely to fail to choose within the time allotted for a phonotaxis trial and significantly increased their latency to choose over the course of multiple trials. We discuss these results with respect to the possibility that female G. pennsylvanicus may be foraging for direct benefits when they choose their mates.     

Diversity of intersegmental auditory neurons in a bush cricket

Various auditory interneurons of the duetting bush cricket Ancistrura nigrovittata with axons ascending to the brain are presented. In this species, more intersegmental sound-activated neurons have been identified than in any other bush cricket so far, among them a new type of ascending neuron with posterior soma in the prothoracic ganglion (AN4). These interneurons show not only morphological differences in the prothoracic ganglion and the brain, but also respond differently to carrier frequencies, intensity and direction. As a set of neurons, they show graded differences for all of these parameters. A response type not described among intersegmental neurons of crickets and other bush crickets so far is found in the AN3 neuron with a tonic response, broad frequency tuning and little directional dependence. All neurons, with the exception of AN3, respond in a relatively similar manner to the temporal patterns of the male song: phasically to high syllable repetitions and rhythmically to low syllable repetitions. The strongest coupling to the temporal pattern is found in TN1. In contrast to behavior the neuronal responses depend little on syllable duration. AN4, AN5 and TN1 respond well to the female song. AN4 (at higher intensities) and TN1 respond well to a complete duet.