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First published online October 5, 2006
Journal of Experimental Biology 209, 4115-4128 (2006)
Published by The Company of Biologists 2006
doi: 10.1242/jeb.02460
Tuning the drum: the mechanical basis for frequency discrimination in a Mediterranean cicada
1 NAMC-CNRS UMR 8620, Bât. 446, Université Paris XI, 91405
Orsay Cedex, France
2 School of Biological Sciences, University of Bristol, Woodland Road,
Bristol, BS8 1UG, UK
* Author for correspondence (e-mail: Jerome.Sueur{at}ibaic.u-psud.fr)
Accepted 25 July 2006
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Key words: biomechanics, hearing, tympanum, travelling wave, frequency discrimination, cicada
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Introduction |
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). The
reception of sound waves is mediated by two types of mechanical systems:
particle velocity receivers, or air pressure receivers. In flies and
mosquitoes, sound is detected using specialised antennae. Working as a simple
harmonic oscillator driven by the velocity of air particles, the antenna
oscillates with sound; this motion then mechanically activates neurones
grouped in a sensory organ, Johnston's organ
(Robert and Göpfert,
2002). Another, better known yet less frequent, way to capture
sound energy is to build a very thin membrane backed by an air space. Due its
low acoustic impedance, a thin and light structure can be easily deflected by
sound pressure (Bennet-Clark,
1984). Such a membrane, or tympanum, operating in vertebrate and
insect auditory systems, is a structurally heterogeneous structure
(Stephen and Bennet-Clark,
1985; Yager, 1999;
Yack, 2004) and the way it is
actuated by incident sound energy has been investigated in only a few systems
(Rodriguez et al., 2005;
Windmill et al., 2005).
Recently, microscanning laser vibrometry experiments have investigated the
patterns of vibration on the tympanal membranes of two grasshopper species
(Locusta migratoria L. and Schistocerca gregaria
Forskål). This analysis revealed the presence of distinct and frequency
specific vibrational waves that can travel in the same time across the
tympanal membrane. Remarkably, the travelling waves reach their peak amplitude
at the tympanal locations where groups of sensory neurones attach
(Windmill et al., 2005).
Documenting that this eardrum does not undergo drum-skin-like motions, these
results also demonstrated the mechanical process by which a complex sound wave
can be decomposed into discrete frequency components.
In cicadas, another insect species with conspicuously well developed
tympanal membranes, the mechanical basis of sound reception has not been
investigated to such a degree. Initially identified by Duges, the cicada
hearing system is located ventrally in the second segment of the abdomen
(Duges, 1838). Vogel described
the structure of the ear in detail (Vogel,
1921; Vogel, 1922;
Vogel, 1923). The auditory
system comprises two major elements: the tympanum and the sensory organ. The
tympanum is a thin membrane of cuticle backed by a tracheal air chamber. The
tympanal membrane (TM) is a heterogeneous structure; it is partially crossed
by a dark, spear-like structure called the tympanal ridge (TR). This ridge is
extended by the tympanal apodeme, a cuticular attachment connecting directly
to the sensory organ. The sensory organ is a typical chordotonal organ
containing multicellular auditory receptors (scolopidia; type I monodynal
receptors). Each scolopidium is composed of five distinct cells: a bipolar
sensory neuron, a cap cell, a scolopale cell, a distal attachment cell and a
proximal attachment cell, the latter attaching to the tympanal apodeme
(Chen, 1958;
Michel, 1975;
Young and Hill, 1977;
Doolan and Young, 1981;
Daws and Hennig, 1996).
Exceptionally for insects, the sensory organ of the tympanal ears of cicadas
contains a high number of auditory receptors, from 600 up to 2100 in each ear,
rivalling or even exceeding the number observed in most lower vertebrates
(Fonseca et al., 2000). The
sensory axons of the mechanoreceptive neurons are grouped to form the auditory
nerve that travels around the ventral edge of the tympanum. Numerous studies
reporting averaged extracellular recordings of compound potentials along the
auditory nerve have shown various degrees of matching between the hearing
frequency range and the frequency spectrum of male calling songs
(Enger et al., 1969;
Simmons et al., 1971;
Popov, 1981;
Huber et al., 1990;
Popov, 1990;
Popov et al., 1991;
Daws and Hennig, 1996). More
accurately, ascending neurons recorded in Magicicada cassini (Fisher)
responded selectively to the frequency of the calling song (1–3 kHz)
while the auditory nerve was sensitive to sound stimulation up to 9 kHz
(Huber et al., 1990). In
addition, intracellular recordings made from eight interneurons of
Tettigetta josei Boulard showed distinct frequency tuning that
covered the conspecific song spectrum and may be involved in the process of
auditory frequency discrimination (Fonseca
et al., 2000).
While mechanisms for frequency discrimination have been intensively studied
at the neuronal level, no work has been undertaken to explore the first stages
of the chain of hearing, in particular the role of the tympanum, in the
conversion of acoustic energy into mechanical energy. A recent study on the
directionality of cicada hearing pointed out that vibrations of the tympanum
seem to differ between the proximal and the distal part of the ridge
(Fonseca and Hennig, 2004). To
test the hypothesis that the mechanics of the cicada tympanum, and more
particularly the TR, provide peripheral processing, and are possibly involved
in frequency discrimination, we experimented with the vibrations of the
tympanum of Cicadatra atra (Olivier), a medium-sized cicada from the
Mediterranean Basin. By measuring the nanometre-scale tympanal vibrations
elicited by both synthetic sounds and playback of sounds recorded in the
field, we observed waves travelling from the tip to the base of the ridge,
where it connects to the tympanal apodeme. Notably, these vibrations have
deflection shapes similar to those described along the basilar membrane of the
mammalian inner ear (von
Békésy, 1960). In effect, these travelling waves
displayed amplitude maxima along the ridge at locations that were frequency
dependent. Corroborating previous work that revealed the processing capacity
of tympanal membranes in locusts (Windmill
et al., 2005), this study documents the eardrum mechanics of
– arguably – one of the most complex insect ears – that of a
cicada. The mechanical response of both male and female eardrums is compared
to the calling song of the male. This study also establishes the complex
mechanics and preneural processing capacity of the tympanum of C.
atra, a structure that, like the eardrum of many other animals, does not
behave at all like the skin of a simple drum.
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Materials and methods |
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). A
Fourier transform with a 43 Hz precision was calculated in the middle of the
four calling songs. An average spectrum was then computed for the four calling
songs.
Animals
Thirteen males and eight females were caught on the same study site
(Fig. 1). Animals were cooled
down to 8–10°C and immediately transferred to Bristol (UK) in an
ice-box. Before measurements, animals were placed at 25–26°C in a
plastic cage (0.53 mx0.22 mx0.22 m) provided with birch branches
(Betula sp.). Both males and females sucked sap from the branches and
males emitted typical calling song bouts, indicating a good general condition.
The wings and the legs were cut back before mechanical measurements. The
operculum and the meracanthus that ventrally cover the tympanal organs, but
are not mechanically linked to them, were also removed. Animals were not
anaesthetized during measurements but were firmly attached to a horizontal
brass bar (6 mm wide, 1 mm thick and 16 mm long) using BLU-TACK
(Bostik-Findley, Stafford, UK). The brass bar was connected to a metal rod
(150 mm long, 8 mm diameter) via a thumbscrew, allowing the animal to
be rotated and tilted into the required position. Only one ear was examined
per animal. Tympanal vibrations were measured using a microscanning laser
Doppler vibrometer (Polytec PSV-300-F; Waldbronn, Germany) with an OFV-056
scanning head. The animal was orientated such that the measuring Doppler
vibrometer could scan the entire tympanum and that the tympanum was
perpendicular to the direction of sound wave propagation. All experiments were
carried out on a vibration isolation table (TMC 784-443-12R, Technical
Manufacturing Corp., Peabody, MA, USA) at room temperature (24–26°C)
and relative humidity of 40–62%. The vibration isolation table with the
animal and the laser vibrometry measurement head were located in a dedicated
acoustic isolation booth (Industrial Acoustics IAC series 1204A, internal
dimensions: length 4.50 m, width 2.25 m, height 1.98 m).
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Mechanical measurements
Cicada ears are made of two main components: a tympanum and a sensory
organ. The ears are symmetrically located in the second segment of the
abdomen. Female ears are smaller than male ears
(Fig. 2). The tympanum is a
thin membrane partly crossed by a dark spear-like structure called the
tympanal ridge (TR). This latter is extended by the tympanal apodeme, a
cuticular attachment inside the sensory organ where the auditory receptors
(scolopidia) are attached. The vibrations of the tympanum were studied
following the same general procedure used in a previous study on migratory
locusts (Windmill et al.,
2005). The vibrations of the whole tympanum, of a focused area
along the ridge and of a 35-point line along the ridge were examined in
response to four different acoustic stimulations. The first stimulus consisted
of a frequency modulated signal (duration=80 ms) sweeping at similar intensity
all frequencies from 1 kHz to 30 kHz. The second stimulus was a typical C.
atra calling song (duration=5 s, frequency range=1–22.05 kHz). This
allowed observation of the response of the tympanum to a natural signal. The
third stimulus was a short click, a square pulse (duration 186 µs, output
frequency bandwidth: 1–30 kHz) synthesized by the Polytec PSV300 sound
generator. This stimulus was used to estimate, in the time domain, the first
mode of vibration of the 35 scan points positioned along the ridge. The fourth
stimulus consisted of a pure-tone signal increasing and then decreasing in
amplitude from 1 mPa to 30 mPa sound pressure, i.e. from 34 dB to 63.5 dB
SPL re 20 µPa (duration=10 s, frequency=11.7 kHz). This last
stimulus provided a test for the potential non-linearity of the ridge in
response to signals of different intensity. A non-linearity in the response
might suggest an active process of audition.
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).
As described in detail elsewhere
(Windmill et al., 2005), the
tympanal and ridge vibrations were analysed by simultaneous recording of the
vibration velocity of the tympanum and the SPL adjacent to the tympanum. The
laser vibrometer allowed accurate measurement (laser positioning 
1 µm)
of the topography of tympanal motion in the amplitude, time and frequency
domains, in a contact-free way and without requiring the use of a reflective
medium on TM. SPL was measured using a 1/8 inch (3.2 mm) precision
pressure microphone (Bruel and Kjaer, 4138; Nærum, Denmark) and
preamplifier (Bruel and Kjaer, 2633). The microphone has a linear response in
the measured frequency range. The microphone's sensitivity was calibrated
using a Bruel and Kjaer sound level calibrator (4231, calibration at 1 kHz, 94
dB SPL). The microphone was positioned 10 mm from the tympanum,
with its diaphragm parallel to the sound direction, thus maximizing the
response. A calibrated stimulus sound level, at the tympanum, of 0.14 Pa (77
dB SPL) was used throughout these experiments.
Evaluation of tympanum response
Analyses of the tympanum velocity, U, and SPL were
carried out by the vibrometer's control PC. The laser signals resulting from
the FM sweep and natural sound stimuli were simultaneously sampled at 102.4
kHz. Sets of 15 data windows of 80 ms duration were acquired and averaged for
each point across the membrane. Using an FFT (Fast Fourier Transform) with a
rectangular window, which weights all sample points equally, a frequency
spectrum was produced for each signal with a resolution of 12.5 Hz. The laser
and microphone signals were then used to calculate different quantities, such
as gain and phase responses. By combining the results from all the points
scanned, oscillation profiles and animations of tympanal deflections were
generated for specific frequencies.
Evaluation of ridge area response
Similarly, the ridge area vibrations induced with FM sweep and natural
signals were reconstructed. More particularly, the frequency corresponding to
a zero phase was measured for the vibration of each point of the 35 points
line scanned along the ridge. This value obtained using the FM sweep stimulus
indicates the frequency at which the tympanal point's velocity was maximal,
corresponding to the resonant frequency at that position. We then obtained an
estimation of the frequency sensitivity along from the apex (X) to
the base (Y) of the ridge. In addition, the tympanum ridge velocity
resulting from the broadcast of short clicks was recorded at a sampling
frequency of 102.4 kHz for a time period of 1 ms. The vibrational response
frequency was measured by the zero-crossing method.
We described the travelling waves running through the ridge area by three
main characteristics (Robles and Ruggero,
2001). We estimated the travel time between two locations
(
t), the wave velocity (Vwave) and the
wavelength (Lwave), following:
 | (1) |
is phase
difference between the two locations, and x is the distance
between the two locations.
Data reliability
The data reliability was estimated by means of magnitude-squared coherence
(C) functions between the laser and microphone signals following:
 | (2) |
Statistics
Differences between male and female were tested using the non-parametric
Wilocoxon test and differences between different driving frequencies were
tested using the Kruskal–Wallis test. All statistics and graphics were
processed using the base package of the software `R'
(R Development Core Team,
2004).
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Frequency composition of the calling song
The calling song of C. atra consisted of a continuous buzz
repeated at irregular intervals. In the frequency domain, the main energy of
the signal was situated between 6 and 17 kHz with 50% of the energy
concentrated between 9.1 and 11.3 kHz (Fig.
3). The dominant frequency was at 10.23±0.78 kHz
(n=200, N=4 males). There was no frequency modulation but a
fast amplitude modulation at a rate of about 1000 Hz due to the pulsed
structure of the signal. This introduced small secondary peaks every 1000 Hz
around the dominant frequency.
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When stimulated with the male calling song, male and female TMs showed deflection shapes similar to those measured using frequency modulated chirps (Fig. 7). The same relationship was observed between localization of maximal deflection points and driving frequency. Finally, measurements done post-mortem immediately following an injection of ethanol showed the same results (data not shown).
Vibrations of the tympanal ridge in response to FM sweep frequency
The phase response along the TR whilst stimulating with FM sweep sound
shows an increasing phase lag as a function of stimulus frequency
(Fig. 8). This phase lag is
substantial, exceeding the phase lag expected for the displacement response of
a simple oscillator (maximum of –90° at frequencies above
resonance). Lag increases as a function of frequency; at higher frequencies,
such as 20 kHz, the phase lag reaches –300° for females and nearly
–900° for males. The envelope of the wave in motion along the ridge
becomes apparent when the response is displayed for every 10° of phase
angle in the full oscillation cycle (Fig.
9). At a frequency of 10 kHz, the deflection envelope of TR is
thus shown every 2.78 µs. The magnitude of the displacement envelopes is
about four times higher for males than for females (displacement gain at 10
kHz: 5.84 µm Pa–1 for males; 1.34 µm
Pa–1 for females). In addition, the frequency response of
female TR differs from that of the male. Deflections of maximum magnitude are
observed at 15 kHz for females, and 10 kHz for males. In other words, 15 and
10 kHz constitute the TR's mechanical `best frequencies'. In effect, the
deflection envelopes vary with the stimulus frequency, with deflection maxima
occurring at different positions along the ridge. In the male, the measured
deflection envelopes reveal that high frequencies deflect the apex of the
ridge more than its base. This relationship between driving frequency and
position along the ridge is less pronounced for females, where the maximum
deflections driven by 5 and 20 kHz sound stimuli occur at similar locations
along the ridge. Topographical positions for 5, 10 and 15 kHz are arranged in
ascending order from the apex to the base of the ridge.
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The differences in TR response with driving frequency were further assessed by computing the frequency spectrum at each of the 35 measurement points taken along the ridge (Fig. 2). Each point on the membrane can indeed be considered as an oscillator, like a mass-spring resonating system. These spectral responses were plotted as 2D density plots, in which the abscissa is the length along the TR (Fig. 10). This place spectrogram clearly shows a decrease in frequency from apex to base, the female's `best frequency' being overall higher than the male's.
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Finally, the travelling wave across the TR was characterised for different driving frequencies. For 9 males and 6 females, the travel time and phase difference across the ridge were estimated, as well as the wave velocity and the wavelength between the apex and the base (Fig. 12). For both males and females, the phase difference increases with the driving frequency (from 112.0±29.5° to 515.0±104.6° for males, P<0.001; 138.3±51.0° to 394.3±147.0° for females, P<0.05). There was no significant difference between males and females (P=0.388). This corresponds to a decrease of the wavelength with increasing driving frequency for both sexes (from 1.62±0.47 mm to 0.34±0.17 mm for males, P<0.001; from 1.35±0.39 mm to 0.49±0.20 mm for females, P<0.05), with again no significant difference between them (P=0.388). The travel time was significantly constant for males (between 57.04±12.28 µs and 71.53±13.72 µs, P=0.365) and females (between 52.44±18.33 µs and 76.85±28.34 µs, P=0.715). There was no significant difference between males and females (P=0.314). This directly implies a constant wave velocity for males (between 6.87±1.22 m s–1 and 8.68±1.92 m s–1, P=0.365) and females (between 6.76±1.94 m s–1 and 10.00±3.59 m s–1, P=0.715) without significant differences between sexes (P=0.314).
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;
Fonseca and Popov, 1997;
Fonseca and Hennig, 2004).
Hence, while several important biophysical aspects of cicada audition have
been studied, most notably directional hearing, the mechanical response of the
tympanal membrane has remained elusive. Using a microscanning laser vibrometer
and sound playback, we have measured and analysed the tympanal mechanics in
the Mediterranean cicada C. atra. The results show that: (1) TM
vibrations scale linearly with sound level, (2) a travelling wave propagates
across the TM and more particularly across the TR, (3) this travelling wave
varies in relation to the driving frequency, and (4) there are obvious
differences between male and female TM vibrations. These results highlight the
mechanical behaviour of the tympanum of an insect ear. Phenomenologically, the
presence of a travelling wave suggests a peripheral mechanism supporting
frequency discrimination.
Tympanal mechanics
When acoustically stimulated, the TM of C. atra vibrates in a
complex way that is unlike the conventional resonant modes of a homogenous
drum skin. In males, the peripheral part of the TM, in particular the TR area,
vibrates substantially more than the central tympanal area. In both males and
females, the TR undergoes vibrations carried by a wave running from its apex
to its base. This wave fulfils the three criteria of a travelling wave
(von Békésy,
1960; Robles and Ruggero,
2001): (1) the magnitude of the oscillation shows an increasing
phase lag along the propagating medium, (2) displacement magnitudes have an
asymmetric envelope where the wave is seen to compress, (3) the wave is
passive, resulting from the mechanical characteristics of the propagating
medium. The travelling wave observed in C. atra can be compared to
some extent with the travelling wave occurring in locust and vertebrate ears
[see summary of travelling wave velocity and wavelength in different taxa
(Windmill et al., 2005)]. As
in the locust, but in contrast to vertebrates, the travelling wave velocity
seems to be constant in cicadas. The lengths of the travelling waves are
shorter in cicadas than in locusts, but show similar values to those of
vertebrates (from 0.3 to 1.6 mm). Differences between locusts and cicadas
might be due to the shorter length of the TR (around 1 mm) compared to the
span of the locust tympanum (around 1.8 mm). In cicadas, as in vertebrates and
locusts, the wavelength decreases with increasing forcing frequency. Yet, one
important biophysical implementation distinguishes the travelling waves
observed in cicadas and locusts to those reported for vertebrates. The medium
of propagation and its surroundings are very different: both sides of insect
tympana are directly in contact with air whereas the basilar membrane is set
between two fluid filled cavities (the scalae media and tympani)
(Olson, 1999;
Robles and Ruggero, 2001). In
locusts and vertebrates, the membrane is directly connected to groups of
neurons that project towards central neural pathways. In cicadas, the TM is
not directly in contact with mechanosensory nerve cells but through an
apodemal prolongation of the TR. It is plausible to postulate that travelling
waves are transmitted from the TR to the apodeme.
Our measurements reveal clear differences between male and female TM
vibrations. Female TMs show lower amplitude vibrations but sensitivity to
higher frequencies. There are notable differences in size, shape and
iridescence (material thickness) between male and female tympana. These
differences are likely to generate variations in key mechanical properties of
the tympanum, such as bulk and local stiffness and damping, and Poisson ratio
of the TM, which all contribute to vibrational behaviour. Such properties are
unknown for cicadas, as they are for all other insect auditory systems.
Interestingly, it has been shown in other cicada species that the TM also acts
as radiating surface during sound emission
(Young, 1990). The enlarged
and translucent central area of the TM, only present in males, which is now
revealed to vibrate very little compared to the TR in C. atra, may
also play a role in sound production. The cicada TM is a complex structure,
allegedly serving, at least, the dual function of capturing sound energy from
the acoustic pressure field and dissipating the large acoustic pressure
generated by the animal's tymbal organ
(Young, 1990). Different parts
of the tympanal membrane may thus have distinct and specialised roles within
that multifunctional scheme.
Frequency analysis
While many insect species show frequency tuning, few of them seem to be
endowed with frequency discrimination. Frequency tuning, as the enhanced
sensitivity to a particular frequency band, is usually situated around the
dominant (or carrier) frequency of the relevant signal. This process has been
shown to involve low-pass, high-pass or band-pass neuronal filtering
(Hennig et al., 2004).
Auditory nerve recordings in cicadas have shown typical V-shape tuning curves
(Enger et al., 1969;
Simmons et al., 1971;
Popov, 1981;
Huber et al., 1990;
Popov, 1990;
Popov et al., 1991;
Daws and Hennig, 1996). It is
shown in the present study that the female tympanum vibrates maximally at
frequencies corresponding to the song's dominant frequencies. The males seem
to be slightly detuned to their own song. Therefore, and different to that
which has been put forward for the tympanum of the Australian cicada
Cyclochila australasiae (Donovan)
(Daws and Hennig, 1996), a
mechanical frequency tuning through tympanal resonance is present prior to
neuronal filtering.
Frequency discrimination implies that the receiving system is able to
distinguish one frequency from another, whether present successively or
simultaneously. While there is physiological evidence in insects for a fine
frequency resolution at the level of receptor cells, only gross frequency
discrimination has been behaviourally documented, and this only in very few
species (Pollack and Imaizumi,
1999; Stumpner and von
Helversen, 2001; Gerhardt and
Huber, 2002; Hennig et al.,
2004; Wyttenbach and Farris,
2004). Our data support the idea that cicadas could perform
peripheral spectral processing with a resolution higher than most insects. As
shown here, the pattern of TR vibrations varies with driving frequency. The
vibrational wave travelling along the TR displays envelope peaks near the apex
for high frequency tones and near the base for low frequencies. Also, the
resonance frequency of the TM linearly decreases from the apex to the base of
the TR (9.8 kHz–3.8 kHz for males; 13.7 kHz–5.7 kHz for females).
Furthermore, the wavelength of the travelling wave decreases with the
wavelength of the sound stimulus.
Altogether, these observations indicate that the TR can act as a frequency
analyser between at least 4 kHz and 10 kHz for males and between 6 and 14 kHz
for females, decomposing a sound wave in its different frequency components.
This decomposition could be transmitted to the apodeme where the auditory
receptor neurones are attached. It is, however, difficult to estimate the
resolution of the frequency decomposition from the mechanical data presented
here; but it is certain to exceed that of the locust, which encompasses four
frequency components (Michelsen,
1968; Michelsen,
1971; Römer,
1976).
Behavioural implications
How do these results contribute to understanding the acoustic behaviour of
cicadas? Females are tuned to the male calling song and thus they may show
frequency tuning, as has been proposed for other cicada species
(Daws et al., 1997;
Fonseca and Revez, 2002;
Sueur and Aubin, 2002). This
probably ensures a species-specific recognition process. Frequency tuning can
indeed ensure premating isolation from species calling in other frequency
ranges [like Lyristes plebejus (Scopoli), Cicada orni L.,
Tettigetta argentata (Olivier), Tibicicina garricola
Boulard, T. corsica fairmairei (Boulard), T. tomentosa
(Olivier)]. If females were also able to resolve fine frequency differences
based not only on mechanical but also on neuronal mechanisms, they might be
able to distinguish different conspecific calling songs in the background
noise produced by other species with partially overlapping spectra (like
T. c. fairmairei). Male spectral sensitivity seems to be shifted
towards lower frequencies, implying some detuning. Because males produce
intense signals [76–78 dB at 1 m
(Boulard, 1992)], there is a
risk of overdriving their own hearing system. To be slightly out-of-tune might
reduce self-deafening risks, while still allowing the ability to listen to
competitors when not calling. Injuries might also be reduced by a mechanical
modification of TM tension. As already observed in other species
(Pringle, 1954;
Hennig et al., 1994;
Yang et al., 1998), C.
atra is able to fold its TM during sound production under the action of a
tympanal muscle (data not shown).
The capacity for frequency analysis may have an important function in
females in the context of male competition. Because, in their natural
environment, males call in the vicinity of each other and actively compete for
the acoustic space, females can hear several of them at the same time. Such
competition results in the notoriously loud cacophony (at least to the human
ear) of male songs. This situation makes a scheme of sexual selection by
female choice plausible in C. atra. To our best knowledge, sexual
selection exerted through preference of sound frequency has been clearly
documented and tested in a few Orthopteran species, but never in cicadas
(Gerhardt and Huber, 2002).
Differences between males in the frequency composition of their calling have
still to be precisely documented. However, tympanum mechanics combined with
higher-level processes of frequency discrimination (auditory neurons,
interneurons, brain neurons) might provide the basis for mating choice in
female cicadas.
In addition, it may be crucial for both sexes to localise nearby singing
males. Males need to know where their competitors are, and females, being the
searching sex during pair formation, need to accurately localise and identify
suitable courting males. The assessment of the distance to a sound source is
usually based on the degradation of the signal's frequency composition
(Naguib and Wiley, 2001).
Sound propagation in air is frequency-dependent, greater attenuation affecting
the higher frequencies contained in a signal. Spectral composition then varies
with the distance between the emitter and the receiver. The capacity for
frequency analysis may then help cicadas in estimating the distance to a sound
source. It has been proposed that such a mechanism is at work in bushcrickets
living in a highly scattering environment
(Römer and Bailey, 1986;
Römer, 1987). In this
conjecture, male hearing tuned to lower frequencies, yet encompassing their
own song, would enhance their sensitivity to distant acoustic competitors.
The apparent remarkable capacity of cicadas to process frequency
information (Fonseca et al.,
2000) needs to be further investigated, from the mechanical and
physiological responses of the auditory system, to the behavioural and
psychophysical capacity to respond to, and discriminate between, male songs of
different qualities.
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Acknowledgments |
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Footnotes |
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References |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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Bennet-Clark, H. C. (1984). Insect hearing: acoustics and transduction. In Insect Communication:12th Symposium of the Royal Entomological Society of London (ed. T. Lewis), pp.49 -82. London: Academic Press.
Boulard, M. (1992). Identité et bio-écologie de Cicadatra atra (Olivier, 1790), la cigale noire, in Gallia Primordia Patria. EPHE Biol. Evol. Insectes 5,55 -86.
Chen, C. (1958). Studies of the tympanal and sound-production organs of a cicada Cryptotympana pustulata Fabr. Acta Entomol. Sin. 8,361 -370.
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