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Directional hearing of a cicada: biophysical aspects
Abstract
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.
... Cicadas have a highly specialised auditory system ( Fig. 7.3) with a basic structure similar across species (Vogel 1923;Myers 1928;Pringle 1954;Michel 1975;Young and Hill 1977;Doolan and Young 1981;Fonseca 1993Fonseca , 1994Fonseca and Popov 1997). The ears are situated latero-ventrally in the first abdominal segment ( Fig. 7.3a, b). ...
... In cicadas, directional hearing was studied in few species by measuring tympanic membrane vibrations (Fonseca 1993;Fonseca and Popov 1997;Fonseca and Hennig 2004) or auditory nerve activity (Young and Hill 1977;Fonseca 1994;Daws and Hennig 1996;Fonseca and Hennig 2004). Significant directionality occurred both at low frequencies and around the peak of the calling song spectrum, with the exception of C. saundersii males, where no directionality was found (Young and Hill 1977). ...
... Significant directionality occurred both at low frequencies and around the peak of the calling song spectrum, with the exception of C. saundersii males, where no directionality was found (Young and Hill 1977). Experiments with selective and reversible blocking of putative sound inputs to the auditory system (Fonseca 1993;Fonseca and Popov 1997) indicated that in males the sound generating timbal acted as an important input responsible for the directionality at the spectral peak of the song, a frequency that corresponds to the natural resonance of the timbal (e.g. Fonseca 1993;Fonseca and Hennig 2004). ...
Cicadas are iconic insects that use conspicuously loud and often complexly structured stereotyped sound signals for mate attraction. Focusing on acoustic communication, we review the current data to address two major questions: How do males generate specific and intense acoustic signals and how is phonotactic orientation achieved? We first explain the structure of the sound producing apparatus, how the sound is produced and modulated and how the song pattern is generated. We then describe the organisation and the sensitivity of the auditory system. We will highlight the capabilities of the hearing system in frequency and time domains, and deal with the directionality of hearing, which provides the basis for phonotactic orientation. Finally, we focus on behavioural studies and what they have taught us about signal recognition.
... Unless the acoustic impedance of the medium on the inner side of the membrane matches that of the external medium, pressure changes of sound waves reaching the tympanum will have little effect (Yager, 1999). Many members of the order Orthoptera, such as bushcrickets (Michelsen et al., 1994;Rheinlaender et al., 2007), crickets (Michelsen et al., 1994;Mhatre and Balakrishnan, 2008), cicadas (Fonseca, 1993), and grasshoppers (Helversen and Helversen, 1995) possess pressure gradient receivers that allow them to locate conspecifics. For example, male congeners of field crickets, Plebeiogryllus spp., produce acoustic signals that attract potential mates. ...
... The direction of sound has a substantial effect on the amplitude and/or phase of sounds reaching the ears and thus provides directionality (Mhatre and Balakrishnan, 2007). Many members of the order Orthoptera, such as bushcrickets (Michelsen et al., 1994;Rheinlaender et al., 2007), crickets (Michelsen et al., 1994;Mhatre and Balakrishnan, 2008), cicadas (Fonseca, 1993), and grasshoppers (von Helversen and von Helversen, 1995) possess pressure gradient receivers that allow them to phonotactically orient toward conspecifics. Male congeners of field crickets, Plebeiogryllus spp., produce acoustic signals that attract potential mates. ...
... These intraspecific acoustic communication signals are important for sexual behavior and reproduction (Alexander and Moore 1958, Weber et al. 1988, Sanborn and Phillips 1999, Cooley and Marshall 2001, Boulard 2006, Fonseca 2014. Correspondingly, cicadas have a sophisticated hearing system, with one of the largest numbers of auditory sensory cells among the insects (about 1,000 cells) (Huber et al. 1980, Fonseca 1993, Daws and Hennig 1995/96, Fonseca et al. 2000, Strauß and Lakes-Harlan 2009. Clearly, the acoustic signal is the long-range cue for mate finding in most cicada species. ...
Detection of substrate vibrations is an evolutionarily old sensory modality and is important for predator detection as well as for intraspecific communication. In insects, substrate vibrations are detected mainly by scolopidial (chordotonal) sense organs found at different sites in the legs. Among these sense organs, the tibial subgenual organ (SGO) is one of the most sensitive sensors. The neuroanatomy and physiology of vibratory sense organs of cicadas is not well known. Here, we investigated the leg nerve by neuronal tracing and summed nerve recordings. Tracing with Neurobiotin revealed that the cicada Okanagana rimosa (Say) (Hemiptera: Cicadidae) has a femoral chordotonal organ with about 20 sensory cells and a tibial SGO with two sensory cells. Recordings from the leg nerve show that the vibrational response is broadly tuned with a threshold of about 1 m/s2 and a minimum latency of about 6 ms. The vibratory sense of cicadas might be used in predator avoidance and intraspecific communication, although no tuning to the peak frequency of the calling song (9 kHz) could be found.
... They facilitate low-frequency directionality with IIDs of ∼15 dB within the range of the main calling song frequencies, 3-7 kHz (Fonseca and Popov 1994). In males, however, the sound-producing organ (the timbal) also serves as an important (contralateral) acoustic input that enables directional hearing due to its ability to mechanically resonate at the calling song frequency (Fonseca 1993;Fonseca and Popov 1994;Fonseca and Hennig 2004). Figure 3a shows another type of sound receiver, which looks like a classical pressure-difference receiver. ...
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.
... Although the songs of O. striatipes and O. utahensis appear to differ in their temporal patterns, the potential for acoustic interference between the species still exists due to characteristics of the cicada auditory system and the species recognition process. The auditory system of cicadas usually shows a peak sensitivity at the frequency of the species calling song but is sensitive to a wide range of frequencies (Katsuki and Suga 1958, Hagiwara and Ogura 1960, Katsuki 1960, Enger et al. 1969, Popov 1969, Simmons et al. 1971, Young and Hill 1977, Schildberger et al. 1986, Huber et al. 1990; but see Popov et al. 1985, Popov and Sergeeva 1987, Fonseca 1993 for exceptions). In fact, Huber et al. (1990) showed that the auditory system in Magicicada cassinii (Fisher) is more sensitive to the call of M. septendecim (L.) than the auditory system of M. septendecim. ...
Okanagana striatipes and O. utahensis are species synchronous in location of activity and utilization of host plants. They possess similar acoustic behavior. Analysis of calling songs shows that calls overlap in frequency but differ in temporal pattern. Based on characteristics of the cicada auditory system and the species recognition mechanism, the potential for acoustic interference exists. Both species are ectothermic behavioral thermoregulators. Measurements of thermal preference and body temperature during singing show that although thermal preferences are similar, O. utahensis sings at a significantly higher body temperature. Differences in body temperature required to coordinate singing in the 2 species provide a partial temporal separation of acoustic signaling. We suggest the physiological mechanisms that permit synchronous utilization of a habitat by the 2 species are the production of calling songs of different temporal patterns and the presence of different thermal requirements, which may permit and/or facilitate temporal separation of the acoustic environment during the day.
... To modulate the hearing sensitivity the cicadas possibly use their detensor tympani muscles, as was shown by Hennig et. al. (1994b) in some north American cicadas, or induce other modifications on the system, such as changes on the abdomen posture (Fonseca, 1993). ...
... Especially, the maximum membrane vibration response induced by 16 kHz correlates with a sensitive nerve response [16]. Moreover, a match of tympanal vibration maxima obtained at different stimulus frequencies and dominant call frequencies was found in many species, e.g. in frogs [37], cicadas [38] and crickets [39], as well as in locusts [40]. This supports the assumption that the tympanal membranes of M. elongata might show species-specific responses, which amplify reactions to certain call frequencies. ...
Processing of complex signals in the hearing organ remains poorly understood. This paper aims to contribute to this topic by presenting investigations on the mechanical and neuronal response of the hearing organ of the tropical bushcricket species Mecopoda elongata to simple pure tone signals as well as to the conspecific song as a complex acoustic signal. The high-frequency hearing organ of bushcrickets, the crista acustica (CA), is tonotopically tuned to frequencies between about 4 and 70 kHz. Laser Doppler vibrometer measurements revealed a strong and dominant low-frequency-induced motion of the CA when stimulated with either pure tone or complex stimuli. Consequently, the high-frequency distal area of the CA is more strongly deflected by low-frequency-induced waves than by high-frequency-induced waves. This low-frequency dominance will have strong effects on the processing of complex signals. Therefore, we additionally studied the neuronal response of the CA to native and frequency-manipulated chirps. Again, we found a dominant influence of low-frequency components within the conspecific song, indicating that the mechanical vibration pattern highly determines the neuronal response of the sensory cells. Thus, we conclude that the encoding of communication signals is modulated by ear mechanics.
Parasitoid fly (Diptera: Tachinidae: Orminii) demonstrate a remarkable ability to detect the direction of an incident sound stimulus by means of its uniquely structured acoustic sensory organs. In this paper, based on the auditory mechanism of the fly, a nonlinear model that can determine the incident direction of the sound is established. The analytical results are testified by experiments. Directional hearing mechanism of the model as well as effects of mechanical parameters is discussed.
The auditory threshold of Cyclochila australasiae, recorded in the whole auditory nerve, is lowest at 3.5 kHz. The roll-off between 4 and 8 kHz is very steep, with thresholds above 96 dB at 8 kHz and higher. The auditory curve is more sharply tuned in males than in females. Experimental manipulations designed to alter the mechanical properties of the accessory structures of the auditory system, and also the auditory organ, suggest that the observed tuned auditory response is not due to resonance of the abdominal air sac, the tympana, the tympanal apodeme, or the auditory organ. The tensor nerve of Cyclochila australasiae responds to acoustic stimuli with a summed response similar to that seen in the auditory nerve. This response probably originates at the tymbal and tensor chordotonal organs, and is independent of the auditory nerve response. The threshold of the tensor nerve response is 15 to 20 dB less sensitive than that of the auditory nerve, but is similarly tuned to 3.5 kHz. The tuning of the auditory threshold of Cyclochila australasiae appears to be due to intrinsic properties common to the scolopidia of the auditory organ and those of the tymbal and tensor chordotonal organs.
Earlier chapters in this volume emphasize the many variations in form and function that play out in the auditory system of
insects. As pointed out in Chapter 1, the diverse developmental origins of insectan hearing organs lead to an assortment of
tympanal ears. In comparison with the singular origin and location of the vertebrate ears, insectan hearing organs present
a bewildering diversity of form and location. These differences stand in contrast to the similarity of the behavioral tasks
that are subserved by the auditory system in both vertebrates and insects. It is fascinating to the comparative physiologist
to observe the dynamic interplay between the convergence of behavioral function and the divergence of form in the auditory
systems of vertebrates and insects. The morphological diversity of insectan auditory systems is very well suited to the comparative
study of auditory function, through its biomechanics, transduction mechanisms, or neural processing capabilities. Our understanding
of the evolutionary adaptive process certainly benefits from study of the variation and diversity of forms.
Periodical cicadas, Magicicada septendecim and M. cassini, occupy the same habitat and the males’ singing overlaps, often forming a chorus, which in M. cassini is synchronized. The calling songs of the males differ in their sound frequency spectra and in the temporal pattern. Playback of conspecific calling songs in the field initiated singing in both species. In M. cassini the initial tick part of the song stimulated males to synchronize their songs with the chorus; the final buzz part attracted preferably females by flight phonotaxis.
For efficient acoustic communication precise concordance between the properties of sound signals of emitters and those of the auditory system of receivers is necessary. An extremely important parameter, the communication range, directly depends on it. So, for any species this concordance is highly “desirable”. Sound-producing and sound-receiving systems have different morphological substrate, are controlled by different genes and matching between them is established by natural selection as the result of a complicated game of different selection forces fitting the animal as a whole to definite environment. The degree of concordance between hearing and sound production vary greatly in different animals and is dependent on the presence or absence of forces working against it.
The neuromuscular mechanism of sound-production in cicadas has been elucidated by a detailed anatomical and physiological study of Platypleura capitata (Oliv.) and by the analysis of magnetic tape recordings of the song of eight other species in Ceylon. In all cases the song consists of a succession of pulses, the repetition frequency being between 120 and 600/sec. Each pulse is composed of a damped train of sound waves whose frequency is determined by the natural period of vibration of the tymbals. A pulse of sound is emitted when the tymbal suddenly buckles or is restored to its resting position by its natural elasticity; in the song of some species both movements are effective. The tymbal muscles, which are responsible for the buckling, have a myogenic rhythm of activity, initiated, but only slightly controlled in frequency, by impulses in the single nerve fibre supplying each muscle. The two tymbals normally act together. The curvature of the tymbals can be increased by the contraction of accessory muscles, the chief of which are the tensor muscles. This increases the volume of sound emitted at each click and lowers the pulse repetition frequency; the abdomen is raised from the opercula by contraction of the tensor muscles. The tracheal air sacs form a cavity which is approximately resonant to the frequency of tymbal vibration and can be varied in size by expansion of the abdomen. Cicada songs, to the human ear, appear to be of great variety. The differences arise largely from the properties of the mammalian cochlea as a frequency analyser; the degree of coherence of phase between pulses, which is probably without significance to the insect, is of great importance in determining the quality of the sound to a human observer. The songs of three species which resemble respectively a bell, a musical phrase and a strident chatter are analysed from high-speed oscillograms, and the difference in quality of sound is explained by reference to the wave-forms. Some species emit a regular succession of pulses. Others have a slow pattern to their song, produced by the co-ordinated nervous excitation of three functional groups of muscles: (a) wthe tymbal muscles, producing the sound; (b) the tensor muscles, controlling the amplitude and pulse repetition frequency; (c) the muscles controlling the resonance of the air sacs. Of the nine species recorded in Ceylon, those belonging to the genus Platypleura produce their pattern by using (b) and (c), the tymbal muscle being in continuous rhythmic activity; those of the genus Terpnosia use mainly (a) to interrupt the continuity of emission of sound pulses, with some accompanying change in amplitude and pulse frequency. The remaining species use all three muscle groups, but different patterns of co-ordination produce great differences in song. In one species (Platypleura octoguttata) a distinct courtship song was recorded from a male in close proximity to a female; this ends with attempted copulation. Preliminary electrophysiological experiments show that the chordotonal sensilla associated with the tympana are extremely sensitive to high-pitched sounds. When the song of another cicada is played back through a loudspeaker the impulse pattern in the auditory nerve corresponds to the pulse modulation envelope, with some after-discharge, as in other insect ‘ears’ (Pumphrey, 1940). The function of the song is to assemble the local population of a cicada species (males and females) into a small group. It remains to be determined whether it is the main intersexual stimulus in mating behaviour.
The last decades has seen an increasing interest in the sound communication of insects. Much information has been accumulated in “classical” fields, such as the anatomy of sound-producing and sound-receiving structures, the analysis of sounds, acoustic behavior, and hexing. This chapter concentrates on the biophysical aspects of sound communication. Both the sound-producing mechanisms and the sound-receiving structures have evolved independently in a number of insects. The main problem of bioengineering in insect sound communication is that of matching the impedances of the sound transmitter, the medium, and the sound receptor. This problem is similar to the impedance matching of electrical equipment: For the transmission to be efficient, the output impedance of the sender should be low, compared with the input impedance of the receiver. In sound emission, the mechanical impedance of the transmitter (the vibrating parts of the insect) should be low, compared with that of the air (the radiation impedance). In sound reception, the impedance of the air should be low, compared with that of the sound-receiving structure. The frequency range of insect sounds is limited, mainly by the impedance problem because the radiation impedance depends very much upon the size of the object relative to the wavelength of sound.
.1An account is given of the anatomy of the organs of sound production and reception in Tettigarcta tomentosa and T. crinita, primitive cicadas from Australia.1This genus provides a link between the Cercopids and true cicadas and makes it possible to suggest detailed homologies for the muscles and other structures concerned in sound-production. It is concluded, contrary to Pringle (1954), that the tymbals and tymbal muscles of cicadas are developments of the first abdominal segment.1The evolution of inter-sexual sound signalling in the Homoptera Auchenorrhyncha is discussed in general terms. It is suggested that the system may have originated from movements made during copulation and evolved through a stage involving pulse vibrations.
The tympanic organ of the Cicadidae is situated on the abdominal ventral side stretching inside a cuticular capsule, which is formed as an irregular cone-shaped protuberance on both sides of the second abdominal segment. Near the hearing capsule lies the drum in a cavity spanned perpendicularly with regard to the longitudinal axis of the animal. The drum forms a narrow and flat process reaching in the hearing capsule. The tympanic organ is attached to this cuticular body. On the other side the organ is fixed at the integument of the distal part of the hearing capsule. There are two protuberances, to which the scolopidia are fastened.
The tympanic organ consists of about 1300 scolopidia each composed of the following distinct cells: the sense cell, which distally bears the cilium, the proximal attachment cell, the scolopale cell, the cap cell, and a distal attachment cell. Proximal and distal attachment cells mediate the attachment of the organ at the epidermal cells of the cuticle. Numerous folds and much desmosomes associated with microtubules fasten the cells at each other so that the organ is spanned very tightly between the two cuticular bodies.
The auditory organ of Cystosoma saundersii consists of 2000-2200 scolopidia arranged in two groups, a dorsal and a ventral group. The dorsal group contains scolopidia orientated along the longitudinal axis of the organ while the ventral group contains scolopidia aligned at right angles to these. On the basis of current theories of sensory transduction, it is possible that these groups may have different intensity characteristics. The cellular composition of an individual scolopidium was described at the electron microscope level and was found to be similar to that occurring in most other chordotonal organs. Slight differences in fine structure were observed in the structure of the scolopale, the mass and position of the ciliary dilatation and the ciliary root. Differences in these parameters may influence the adequate stimulus needed for a chordotonal organ. The fine structure of proximal and distal attachments of the scolopidia to the cuticle is similar to that of muscle attachments observed in insects, crustaceans and arachnids. The central projections of the auditory nerve within the thoracic ganglia are similar to those described for the periodical cicadas.