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Cicadas produce the sound patterns of their songs by
buckling a pair of tymbals in the first abdominal segment
(Pringle, 1954a; Moore and Sawyer, 1966; Reid, 1971; Young
and Bennet-Clark, 1995). The tymbal is a cuticular membrane
whose stiffness depends mainly on the number of ribs it
contains (Popov, 1975) and the amount of embedded resilin
(Young and Bennet-Clark, 1995). Contraction of the large
tymbal muscles causes the tymbal ribs to buckle inwards and
the tymbal then jumps back because of its elasticity. Inward
and outward movements of the tymbal may produce sound.
The sound pulses generated by one tymbal muscle contraction
are defined as a tymbal cycle. Amplitude modulation of tymbal
cycles can be attributed to the action of two systems: the tensor
muscle exerts a force on the tymbal frame and thus modulates
the stress of the tymbal and its resulting sound output (Pringle,
1954a; Simmons and Young, 1978); in addition, the largely
air-filled abdomen may influence sound amplitude as a result
of changes in the radiation or resonance properties of the
cicada body (Pringle, 1954a; Bennet-Clark and Young, 1992;
Fonseca and Popov, 1994).
Current understanding of tensor muscle action comes mostly
from studies in which the tensor muscle was electrically
stimulated and the effect of the muscle contraction on the
amplitude of the sound pulses produced was monitored. Such
experiments suggest that a tonic contraction of the tensor
muscle increases the stiffness of the tymbal (Pringle, 1954a;
Hagiwara, 1956; Simmons and Young, 1978). The higher force
then required to buckle the tymbal results in higher-amplitude
sound pulses with a concurrent change in the timing of the
tymbal sound with respect to the tymbal muscle contraction
(Pringle, 1954b; Simmons and Young, 1978). Overstressing of
the tymbal due to maximum contraction of the tensor muscle
1535
The Journal of Experimental Biology 199, 1535–1544 (1996)
Printed in Great Britain © The Company of Biologists Limited 1996
JEB0296
The effect of tensor muscle contraction on sound
production by the tymbal was investigated in three species
of cicadas (Tettigetta josei, Tettigetta argentata and
Tympanistalna gastrica). All species showed a strict time
correlation between the activity of the tymbal motoneurone
and the discharge of motor units in the tensor nerve during
the calling song. Lesion of the tensor nerve abolished the
amplitude modulation of the calling song, but this
modulation was restored by electrical stimulation of the
tensor nerve or by mechanically pushing the tensor sclerite.
Electrical stimulation of the tensor nerve at frequencies
higher than 30–40 Hz changed the sound amplitude. In Tett.
josei and Tett. argentata there was a gradual increase in
sound amplitude with increasing frequency of tensor nerve
stimulation, while in Tymp. gastrica there was a sudden
reduction in sound amplitude at stimulation frequencies
higher than 30Hz. This contrasting effect in Tymp. gastrica
was due to a bistable tymbal frame. Changes in sound pulse
amplitude were positively correlated with changes in the
time lag measured from tymbal motoneurone stimulation
to the sound pulse. The tensor muscle acted phasically
because electrical stimulation of the tensor nerve during a
time window (0–10ms) before electrical stimulation of the
tymbal motoneurone was most effective in eliciting
amplitude modulations.
In all species, the tensor muscle action visibly changed
the shape of the tymbal. Despite the opposite effects of the
tensor muscle on sound pulse amplitude observed between
Tettigetta and Tympanistalna species, the tensor muscle of
both acts by modulating the shape of the tymbal, which
changes the force required for the tymbal muscle to buckle
the tymbal.
Key words: tymbal, tymbal muscle, sound modulation, cicada,
Tettigetta sp., Tympanistalna gastrica.
Summary
PHASIC ACTION OF THE TENSOR MUSCLE MODULATES THE CALLING SONG IN
CICADAS
P. J. FONSECA1AND R. M. HENNIG2,*
1Departamento de Zoologia e Antropologia da Faculdade de Ciências de Lisboa, Bloco C2, Campo Grande,
1700 Lisboa, Portugal and 2Max-Planck-Institut für Verhaltensphysiologie, D-82319, Seewiesen, Germany
Accepted 25 March 1996
*Present address: Abteilung Verhaltensphysiologie, Institut für Biologie, Humboldt Universität zu Berlin, Invalidenstraße 43, D-10115 Berlin,
Germany.
Introduction
1536
may also cause a reduction in sound amplitude (Hennig et al.
1994). Most of these studies have recorded tensor muscle
activity during the alarm or distress call of the males and only
Weber et al. (1988) have succeeded in recording tensor muscle
activity during calling song production.
Cicadas possess different tymbal types which show rather
distinct tymbal cycles due to their morphology and stiffness
(Popov, 1975). To date, most studies on tensor muscle function
have been concerned with cicadas which produce several
sound pulses in a tymbal cycle due to the sequential buckling
of the tymbal ribs. However, there is a group of cicadas
(Tettigetta and Tympanistalna, Fonseca, 1991; Cicadetta,
Popov, 1975) in which all the tymbal ribs buckle
simultaneously. These cicadas show very fast, large amplitude
modulations in their calling songs (within less than 10ms)
which cannot be accounted for either by a tonic contraction of
the tensor muscle or by a positional change of the abdomen.
There is, however, indirect evidence that the tensor muscle
is indeed responsible for the fast and large amplitude
modulations observed in these species (Fonseca, 1991). We
therefore compared the function of the tensor muscle in several
species by recording tensor muscle activity during normal
calling song production and by investigating the effects on the
sound modulation elicited through electrical stimulation of the
tensor nerve. It is shown that the tensor muscle is responsible
for the fast amplitude modulations observed in the calling song
and that the action of the tensor muscle is phasic.
Materials and methods
Animals
The cicada species Tettigetta josei (Boulard), Tettigetta
argentata (Olivier) and Tympanistalna gastrica (Ståhl) were
caught on the southwest coast of Portugal in June 1992. The
animals were kept on a netted feeding plant in a cool room at
10–15°C.
Morphology of the sound-producing structures
Adult cicadas were killed and fixed in a solution modified
after Carnoy for 24h at room temperature (Bock, 1987) and
then preserved in 70% ethanol. Drawings were made from
observations using a Wild M5A stereomicroscope equipped
with a drawing tube, using whole animals as well as
longitudinal and transverse sections of the cicada bodies.
Preparation of the cicadas for nerve recording and electrical
stimulation
A male cicada, with its wings, legs and mouthparts removed,
was waxed to the end of a slender rod (110mm long, 2mm
diameter) attached to a magnetic stand. Two electrodes
(minutien insect pins) were implanted into the head near the
medial edge of the compound eye. The mesosternum was
removed to expose the nerves exiting from the metathoracic
abdominal ganglionic complex (MAC). The abdominal nerves
were cut in order to preclude movements of the abdomen
which might influence sound radiation. Both the tensor nerve
and auditory nerve on one side were lifted on double silver
hook electrodes (diameter 50µm) for recording and electrical
stimulation (Fig. 1). In all three species, the auditory nerve
carries both the auditory receptor fibres and the tymbal
motoneurone. The dissected area was kept moist with insect
Ringer until both nerves had been insulated with a mixture of
Vaseline and mineral oil. The cicada was earthed by a wire
inserted into the mesothoracic leg stump. All experiments were
conducted at room temperature (24±2°C).
Sound monitoring
Hard surfaces close to the animal were covered with sound-
absorbing material (cotton wool and Illbruck Super Waffel
pieces) in order to reduce echoes. The sound generated by the
cicada was monitored using a microphone (Sennheiser MKE-2)
placed approximately 10 cm away from the animal and amplified
using a UHER 4200 tape recorder (the sound pressure measured
with this system was constant within ±3dB in the range
0.5–18kHz). Sound, nerve activity and electrical stimulation
signals were stored on magnetic tape with a DAT recorder
(TEAC 100T).
Electrical stimulation
For brain stimulation, pulsed electrical stimuli (pulse
duration 1 ms; amplitude 1–10V; stimulus frequency 10–60Hz
from a battery-powered stimulus isolation unit) were applied
through the electrodes inserted in the head. Stimulation for
1–2s was in most cases sufficient to elicit singing with a
P. J. FONSECA AND R. M. HENNIG
MAC
TG2
Recording/stimulation
electrodes
Tensor nerve
Tymbal
muscle
Tymbal
frame
Tymbal
plate Tymbal
ribs
Tensor
sclerite
Tensor
muscle
Abd.N. Auditory
nerve
Fig. 1. Schematic drawing of the sound-producing tymbal and the
neuromuscular apparatus investigated by electrical nerve stimulation.
The auditory nerve contains the tymbal motoneurone. Abd.N.,
abdominal nerves; MAC, metathoracic abdominal ganglion complex;
TG2, second thoracic ganglion.
1537Tensor muscle in cicadas
pattern similar to the calling song and starting within a few
seconds to 2min after the stimulation ended. Electrical
stimulation of the auditory and tensor nerves was via insulated
battery units and the double silver hook electrodes (Fig. 1). The
duration of the stimulation pulses was set at 0.5ms and the
frequencies used ranged from 5 to 50Hz (occasionally 100Hz)
for the auditory nerve (tymbal motoneurone) and from 10 to
200Hz for the tensor nerve.
Visual observation of the changes induced in the tymbal and
tymbal frame during electrical stimulation of the tensor
nerve
Tensor muscle contraction was induced by tensor nerve
stimulation, usually at approximately 100Hz. The resulting
morphological changes were observed using a
stereomicroscope (WILD M5A) and noted on a drawing of the
tymbal. The direction of movement (inward or outward) as
well as the magnitude of the displacement (classified as small,
medium or large) was noted.
Mechanical pushing of the tensor sclerite during sound
production
The effect of tensor muscle contraction was simulated by
pushing the tensor sclerite using the smoothed tip of an insect
pin (see Fig. 1). The pin was mounted on a holder and advanced
using a micromanipulator. The effects on the sound pulses were
recorded both during the calling song and during electrical
stimulation of the tymbal motoneurone (i.e. auditory nerve).
Measurements of the force necessary to buckle the tymbal
inwards both with and without tensor nerve stimulation
The tymbal was loaded with a force by advancing a spring
mounted on a micromanipulator, both with and without an
electrically induced tensor muscle contraction. The tip of the
spring, 100µm in diameter, was placed on the apodeme pit
where the tymbal muscle apodeme attaches (see Fig. 2; Young
and Bennet-Clark, 1995). The force was increased steadily by
advancing the micromanipulator until buckling of the tymbal
occurred, usually accompanied by sound production. The force
was then determined from the micromanipulator reading, which
was compared with a calibration curve constructed using a
balance. A force of 1 mN deformed the spring by about 0.75µm,
which is at least 10 times greater than the observed deformation
of the tymbal plate. The size of the tip of the spring, the position
over the tymbal where the force was applied and the angle of
incidence of this force had to be chosen carefully (see also
Young and Bennet-Clark, 1995). Applying the force in other
positions on the tymbal plate or modifying the angle usually
resulted in no measurable differences between the force applied
before and after tensor muscle contraction.
Data analysis
Data analysis was carried out using a Macintosh computer
equipped with appropriate software (SuperScope). Chart prints
were made on an eight-channel chart recorder (Picker Uniscript
UD210), after transferring the data from the DAT recorder to
a Racal Store 4DS.
Nomenclature
Sound pulses are referred to as IN sound pulses when they
were produced during inward buckling of the tymbal and as
OUT sound pulses when they were produced during outward
movement of the tymbal. The term ‘time lag’ refers to the time
elapsed between electrical stimulation of the tymbal
motoneurone (in the auditory nerve) and the occurrence of the
resulting IN or OUT sound pulse.
Results
Morphology of the sound-producing apparatus
The sound-producing apparatus of the males of Tett. josei
and Tymp. gastrica (Fig. 2) is composed of the tymbals, which
are driven by the powerful tymbal muscles, and the tensor
muscle, which inserts at the anterior tymbal frame (see also
Fig. 1 for a schematic view). A large tracheal air sac lines the
tymbals, the tympana and the folded membranes and exits
through the metathoracic spiracles (Fig. 2B). The wall of the
abdomen is internally lined by a relatively thick layer of tissue
in Tett. josei, but only a thin layer in Tymp. gastrica.
The tymbal of Tett. josei shows a convex region anteriorly
with three long and two short sclerotized ribs and a flatter
tymbal plate posteriorly (Fig. 2A). The two most posterior long
ribs join dorsally whereas the third, more anterior rib is
separated from the two long ones. The tymbal buckles along
the short ribs. The tymbal muscles arise ventrally from the
chitinous Vand insert through a tendinous apodeme on the
dorsal portion of the tymbal plate. From outside, the tymbal
muscle apodeme at the tymbal plate is easily recognized as a
small invagination – the apodeme pit. The tymbal frame has a
relatively large tensor sclerite anteriorly which is surrounded
by a flexible membrane, allowing movement (Fig. 2A). The
stout and strong tensor muscle arises from a sclerotized
metathoracic ridge just ventrally to the tymbal and anteriorly
to the folded membrane and inserts at the tensor sclerite
(Fig. 2B). Visual observations revealed that tensor muscle
contraction moves the whole tensor sclerite inwards, especially
at the anterior edge (arrows in Fig. 2A).
In Tymp. gastrica, the convex tymbal area possesses four
long sclerotized ribs, but no short ones (Fig. 2C). The posterior
two ribs join dorsally. The posterior three ribs are slender in
the medial region of the tymbal, where the tymbal buckles. The
most anterior fourth rib is attached to the tymbal frame. The
tensor sclerite is dorsally and anteriorly, but not ventrally,
surrounded by a flexible membrane. Visual observations
showed that tensor muscle contraction moved the tensor
sclerite inwards, mostly at the anterior and dorsal edge (arrow
in Fig. 2C).
Function of the tensor muscle in Tettigetta josei
The tymbal of Tett. josei produces one IN and one OUT
sound pulse in a tymbal cycle (Fig. 3A). The calling song
1538
consists of echemes, each of which is defined by two
consecutive tymbal muscle contractions (Fig. 3; for details, see
Fonseca, 1991). Pulsed electrical stimulation of the brain
elicited this pattern reliably while recordings from the auditory
nerve containing the tymbal motoneurone and the tensor nerve
were made (Fig. 3A). In an echeme of Tett. josei, the first IN
sound pulse was very soft while the second IN pulse was very
loud. The tymbal motoneurone (large potential in the middle
trace of Fig. 3A) showed two action potentials per echeme
which were accompanied by the activity of several units in the
tensor nerve recording spaced between the tymbal
motoneurone spikes (Fig. 3A). Cutting the tensor nerve
abolished the loud IN sound pulses (Fig. 3B), while electrical
stimulation of the tensor nerve resulted in IN sound pulses of
large amplitude (Fig. 3C). The amplitude of the OUT sound
pulses is not modulated during the calling song (Fig. 3A) and
electrical stimulation of the tensor nerve did not influence the
OUT pulse amplitude (Fig. 3C).
The tensor nerve not only innervates the tensor muscle, but
also the intersegmental dorsal muscles which control lift of the
abdomen (Pringle, 1954a; Simmons and Young, 1978).
Furthermore, the tensor nerve contains a large number of
mechanoreceptor axons from the tensor chordotonal organ
which may provide sensory feedback about tymbal buckling
(Young, 1975). The following controls ensured that the
observed effects were solely due to the contraction of the
tensor muscle. (1) Cutting the tensor nerve between the MAC
and the stimulation electrodes did not affect the changes in
sound-pulse amplitude due to electrical nerve stimulation, and
the timing of the central nervous motor output was unchanged
P. J. FONSECA AND R. M. HENNIG
Echeme
Sound
Tensor nerve
Sound
Sound
20ms
Auditory nerve
(tymbal MN)
Tettigetta josei
A
B
C
Fig. 3. Sound recordings and recordings from the auditory nerve and
the tensor nerve of Tettigetta josei during calling song production
elicited by electrical brain stimulation. The auditory nerve contains
the tymbal motoneurone (MN). (A) During the calling song (upper
trace, sound pulses; IN, filled symbols; OUT, open symbols), the
tymbal motoneurone showed two large action potentials per echeme
(middle trace) which were accompanied by the activity of several
units in the tensor nerve recording (bottom trace). (B) Lesion of the
tensor nerve resulted in a reduction in amplitude of the second IN
pulse, while OUT pulses were less affected. (C) Electrical stimulation
of the tensor nerve at frequencies higher than 100Hz resulted in
uniformly loud IN pulses.
lr
sr
ap
abd
lr
ap
ts
1mm
1mm
1mm
Anterior
ty
ts
A
Tettigetta josei
B
Tettigetta josei
C
Tympanistalna gastrica
Fig. 2. Sound-producing apparatus and tymbals of male Tettigetta josei (A,B) and the tymbal of Tympanistalna gastrica (C). (A,C) External
view of the tymbals. (B) Drawing of the tymbal apparatus and selected structures as revealed by a longitudinal vertical section of a Tett. josei
male with the tymbal muscle removed. The sound-producing apparatus of Tymp. gastrica is rather similar in size and structure to that of Tett.
josei and is therefore omitted here. Anterior is to the left in all drawings. Curved arrows in A and C indicate the direction of movement of the
anterior part of the tensor sclerite. abd, anterior part of the abdominal cavity; ac, auditory capsule; ap, apodeme pit; cv, chitinous V; fm, folded
membrane; lr, long ribs; sp, metathoracic spiracle; sr, short ribs; ti, tymbal; tm, tensor muscle; ts, tensor sclerite; ty, tympanum.
1539Tensor muscle in cicadas
when the tensor nerve was cut distally to the recording
electrodes (see Fig. 1). (2) Mechanical pressure on the sclerite
alone had the same effect on sound-pulse amplitude as
electrical stimulation of the tensor nerve. Thus, contraction of
the tensor muscle alone was responsible for the observed
amplitude modulations.
Electrical stimulation of the tymbal motoneurone and the
tensor nerve (see Fig. 1) showed that the effect of tensor
muscle contraction on the sound-pulse amplitude was gradual
(Fig. 4) and dependent on the frequency of electrical
stimulation. Beginning at a tensor nerve stimulation frequency
of approximately 40Hz, there was an increase in amplitude
mainly of the IN sound pulses, up to frequencies higher than
100Hz (Fig. 4A). The changes in sound amplitude were
accompanied by changes in the time lag between electrical
stimulation and the sound pulse (Fig. 4B). The effect of tensor
muscle contraction was independent of the rate of tymbal
motoneurone stimulation (at 5, 20 or 50Hz). The amplitude
change induced by tensor muscle contraction was greater than
20dB, and the amplitude and time lag of the IN pulses showed
a positive correlation (Fig. 4C). Electrical stimulation of the
tensor nerve had only a small effect on the OUT pulse
amplitude (Fig. 4C). Examination of the relative timing of
tensor nerve and tymbal motoneurone stimulation revealed a
time window (−10 to 0ms) during which a single stimulation
of the tensor nerve strongly affected the IN pulse amplitude
(Fig. 5). The amplitude effect of the time window accounted
for approximately 30% of the maximal amplitude modulation
observed in an individual animal. The time lag between
auditory nerve and tensor nerve stimulation for the results in
Fig. 4A,B had been chosen such that, at low stimulation
frequencies of the tensor nerve, the phasic effect (Fig. 5) was
excluded.
The observed increase in the amplitude and the time lag of
the IN pulse due to electrical stimulation of the tensor nerve
can be interpreted in the following way. Contraction of the
tensor muscle increases the convexity of the tymbal and thus
the tymbal muscle takes more time to overcome the increased
B
C
A
0.2
0.4
0.6
0.8
1.0
0
Normalized IN sound amplitude
14
8
12
10
16
Time lag (ms)
Amplitude
0.8
0
0.2
0.4
0.6
1.0
Normalized sound amplitude
50 100 150 2000
Tensor muscle stimulation frequency (Hz)
0 50 100 150 200
Tymbal muscle
Time lag
Sound Sound
Tymbal muscle
10 15 20 255
Time lag (ms)
OUT
IN
Fig. 4. Electrical stimulation of the tymbal
motoneurone (20Hz) and concomitant electrical
stimulation of the tensor nerve of Tettigetta josei at
frequencies up to 200Hz affects sound pulse
amplitude and time lag. Insets show sound
recordings of a tymbal cycle with electrical
stimulation of the tensor nerve and illustrate how
sound amplitude and time lag were determined for
IN sound pulses (filled symbols). Open symbols
represent OUT sound pulses. (A) Amplitude and (B)
time lag of IN sound pulses increased with
increasing stimulation frequencies of the tensor
nerve. Mean values ± S.D. from five males.
(C) Relationship between sound amplitude and time
lag of IN and OUT sound pulses obtained from one
tensor nerve stimulation series. Amplitudes are
normalized to the amplitude of the loudest IN pulse.
IN (filled symbols), OUT (open symbols); data from
one male.
1540
mechanical resistance of the tymbal, which will produce louder
sound pulses when buckled. Hence, an increase in the force
required to buckle the tymbal is expected. Measurements of
this force were conducted by placing the tip of a spring on the
apodeme pit of the tymbal plate and by advancing the spring
until the tymbal buckled. Without electrical stimulation of the
tensor nerve, a force of 1.0mN was necessary to buckle the
tymbal of Tett. josei (Fig. 6). However, electrical stimulation
of the tensor nerve increased the force which had to be applied
to the apodeme pit in order to buckle the tymbal. This force
changed in the same frequency range of tensor nerve
stimulation as previously recorded for the amplitude and time
lag of the IN pulses (see Fig. 4).
Function of the tensor muscle in Tettigetta argentata
The tymbal cycle in Tett. argentata produces one IN and one
OUT sound pulse (Fig. 7). The calling song differs from that
of Tett. josei in that each echeme is defined by three
consecutive contractions of the tymbal muscles (Fig. 7;
Fonseca, 1991). In contrast to the echemes of Tett. josei, values
of intermediate amplitude were observed (e.g. for the second
IN sound pulse in each echeme, Fig. 7) and the amplitude of
the OUT pulses was also modulated (compare the first and
second OUT pulse in each echeme, Fig. 7). Recordings from
the tensor nerve revealed units which were active just prior to
the first tymbal motoneurone spike, but also at the second
tymbal motoneurone spike (Fig. 7) in an echeme. A set of
experiments identical to those performed on Tett. josei (see
Figs 4, 5) gave similar results, i.e. IN pulse amplitude was
dependent on the frequency of electrical stimulation of the
tensor nerve, a positive relationship existed between time lag
and IN pulse amplitude, and a time window within which a
single tensor stimulation pulse elicited a large effect on the
sound-pulse amplitude was observed. While the principal
mechanism of tensor muscle action appeared to be the same
for both species, some distinct differences were also observed,
probably due to the difference in stiffness of the tymbal: (1) the
OUT pulse amplitude also increased with the frequency of
tensor nerve stimulation, (2) the effective time window was
larger (−25 to +5ms), although the maximal effect was also
observed from −10 to 0ms, and (3) the force necessary to
buckle the tymbal was higher (from 2.2mN without
P. J. FONSECA AND R. M. HENNIG
0.8
0
0.2
0.4
0.6
1.0
Normalized sound amplitude
−25 −20 −15 −10 −505−30
Time difference (ms)
Sound
el.stim. A.N.
el.stim. Te.N.
∆tvar
IN
OUT
Fig. 5. Dependence of amplitude of IN and OUT sound pulses on the
relative timing of tymbal motoneurone (A.N.) and tensor nerve (te.N.)
stimulation (el.stim.) in Tettigetta josei. The inset defines the time
difference (∆tvar) between the two stimulus pulses. Stimulation of
the tensor nerve from 10ms before the tymbal motoneurone
stimulation (shown as negative values) to simultaneous stimulation
(i.e. 0ms) was effective in changing the amplitude. Data points
correspond to single sound pulses from tensor nerve stimulation at
less than 40Hz. Amplitudes are normalized to the amplitude of the
loudest IN pulse under these stimulation conditions. Note that the
highest amplitudes in this diagram correspond to about one-third of
the maximal amplitude modulation. IN, filled symbols; OUT, open
symbols; data from two males.
1.5
0.5
1.0
2.0
Force (mN)
50 100 150 2000
Tensor muscle stimulation frequency (Hz)
Fig. 6. Force required to buckle the tymbal of Tettigetta josei under
different magnitudes of tensor muscle contraction induced by
electrical stimulation. Higher stimulation rates of the tensor nerve
resulted in greater forces. Mean values (filled symbols) calculated
from four tymbals of two males (open symbols) are shown.
20ms
Sound
Auditory nerve
Tensor nerve
Echeme Tettigetta argentata
Fig. 7. Sound recordings and recordings from the auditory nerve
containing the tymbal motoneurone and from the tensor nerve of
Tettigetta argentata during calling song production (upper trace,
sound pulses; IN, filled symbols; OUT, open symbols). The tymbal
motoneurone showed three large action potentials per echeme (middle
trace). Several units in the tensor nerve showed a constant activity
pattern per echeme (bottom trace). Recording from a male with only
one tymbal intact.
1541Tensor muscle in cicadas
stimulation of the tensor nerve to 2.6mN at a stimulation
frequency of 100Hz).
Function of the tensor muscle in Tympanistalna gastrica
The tymbal produces one IN and one OUT sound pulse by
buckling during one contraction of the tymbal muscle
(Fig. 8A). In a type 1 echeme of the calling song, the amplitude
of the first IN pulse of both tymbals is high, while all following
OUT and IN pulses are of the same reduced loudness (Fig. 8A;
see Fonseca, 1991, for details of the calling song). Tymp.
gastrica shows three types of echeme, with type 1 being the
most common and typical. Nerve recordings showed that
bursts of several units in the tensor nerve occurred between the
action potentials of the tymbal motoneurone (Fig. 8A). The IN
pulses produced by the tymbal when the tensor muscle was
disabled were always as loud as the first IN pulse in an echeme
(Fig. 8B). The amplitude of the OUT pulses was not affected
by the lesion of the tensor nerve. The same control experiments
for influences other than the tensor muscle were conducted as
in Tett. josei, but again there was no evidence for the action of
any additional system.
In order to study the effect of tensor muscle contraction on
the sound-pulse amplitude, the tymbal motoneurone was
electrically stimulated to elicit a tymbal cycle, while the tensor
nerve was electrically stimulated at different rates from 10 to
200Hz (Fig. 9A,B). Stimulation frequencies of the tensor nerve
lower than 30Hz had no effect on the sound-pulse amplitude
nor on the time lag of the sound pulses, but at frequencies higher
than 30Hz, there was a marked reduction in the amplitude and
the time lag of the IN pulses. Furthermore, the changes to the
IN pulse amplitude and time lag were rather sudden with the
onset of electrical tensor nerve stimulation and affected
virtually the first tymbal cycle during the stimulation. The
amplitude reduction of the IN pulse was approximately 9–12 dB
and intermediate amplitude and time lag values of IN sound
pulses were rarely observed. The OUT pulse amplitude was
essentially unaffected by the tensor nerve stimulation (Fig. 9C).
A sudden change in amplitude of the IN sound pulses was
obvious both in sound recordings during the calling song
(Fig. 8A) and during electrical stimulation of the tensor nerve
(Fig. 9A,B). Examination of the relative timing of activity
between the tymbal motoneurone and tensor nerve stimulation
revealed that there was a time window of approximately 20ms
within which a single electrical stimulus applied to the tensor
nerve could elicit complete modulation of the IN pulse
amplitude (Fig. 10). At the beginning and end of that time
window, tensor contraction was not always effective (Fig. 10).
The mechanical properties of the tymbal of Tymp. gastrica
appear to be similar to those of Tett. josei and Tett. argentata:
quiet pulses are generated by a flattened tymbal, while the time
lag increases when louder pulses are produced due to the
increased convexity of the tymbal. However, tensor muscle
action in Tymp. gastrica results in the opposite effect to that
seen in the two Tettigetta species: contraction of the tensor
muscle induces a reduction in amplitude and time lag rather
than an increase. Consequently, if tensor muscle contraction
induces the tymbal to become more flattened for the production
of quiet sound pulses, less force should be required for the
tymbal muscle to buckle the tymbal. Without electrical
stimulation of the tensor muscle, a force of approximately
0.18mN was required to buckle the tymbal in Tymp. gastrica.
The force decreased only slightly but significantly to
approximately 0.15 mN when the tensor muscle was contracted
(mean from two males, standard deviation was less than
0.01 mN). Visual observation during these force measurements
confirmed that the tymbal always buckled completely.
Morphological examination of the tymbal tensor system in
all three species revealed a comparatively large tensor sclerite
surrounded by membranous tissue which allowed large
movements (Fig. 2A,C). In order to describe the
morphological changes induced by contraction of the tensor
muscle on the tymbal, we observed the tymbal while
contraction of the tensor muscle was induced (Fig. 11). For
Tett. josei (Fig. 11A), the largest movement was observed at
the tensor sclerite (inwards), with smaller movements of the
tymbal plate (outwards), the ventral rib area (outwards) and the
20ms
Sound
Sound
Auditory nerve
Tensor nerve
B
Tympanistalna gastricaA
Fig. 8. Sound recordings and auditory and
tensor nerve recordings during calling song
production from Tympanistalna gastrica
with only one tymbal (upper trace, sound
pulses; IN, filled symbols; OUT, open
symbols). During an echeme (one echeme is
shown in the top trace), the tymbal
motoneurone (large potential in the auditory
nerve recording, middle trace) showed a
series of action potentials which were
accompanied by the activity of several units
in the tensor nerve recording (bottom trace).
(B) Lesion of the tensor nerve resulted in an
increase in the IN sound amplitude
throughout the calling song, although OUT
sound amplitude was unaffected.
1542
dorsal rib area (inwards). The posterior medial rib area moved
outwards, whereas the anterior medial rib area moved inwards.
The schematic cross section of the tymbal summarizes these
observations (Fig. 11A).
In Tymp. gastrica (Fig. 11B), the largest movement was
observed for the tensor sclerite, which moved inwards,
especially at its dorsal posterior edge where the tensor muscle
inserts. Other movements of the tymbal plate and the ventral
and dorsal rib areas were small and directed inwards
(Fig. 11B). The ventral edge of the tensor sclerite is connected
to the tymbal frame and therefore the ventral mobility is
reduced. Contraction of the tensor muscle will pull the tensor
sclerite inwards, but also push down the ventral part of the
tymbal frame (Fig. 11B). The mechanical construction of the
tymbal frame is bistable and will only change if the force
exerted by the tensor muscle via its sclerite is above a certain
mechanical threshold. This particular mechanical construction
of the tymbal frame reverses the ‘normal’ action of the tensor
muscle and, at the same time, introduces a bistability to the
frame, which reduces the likelihood of intermediate amplitudes
of IN sound pulses.
Discussion
The tensor muscle has a pivotal role in the production of the
species-specific signal of the cicada species investigated. The
fast and large amplitude modulations of the calling songs are
achieved firstly by a phasic component in the action of the
tensor muscle and secondly by the buckling mechanism of the
tymbal and by the mechanical construction of the tymbal frame,
which allow fast modulations of the shape of the tymbal.
Principal action of the tensor muscle
The tymbal muscle contracts, causing the tymbal to buckle.
This produces sound, and the tensor muscle modulates the
sound amplitude by changing the tension of the tymbal via the
P. J. FONSECA AND R. M. HENNIG
B
C
A
0.2
0.4
0.6
0.8
1.0
0
Normalized IN sound amplitude
20
15
10
25
Time lag (ms)
Amplitude
0.8
0
0.2
0.4
0.6
1.0
Normalized sound amplitude
50 100 150 2000
Tensor muscle stimulation frequency (Hz)
0 50 100 150 200
Tymbal muscle
Time lag
Sound Sound
Tymbal muscle
15 20 25 3010
Time lag (ms)
IN, tensor muscle on
IN, tensor muscle off
OUT, tensor muscle on
OUT, tensor muscle off
Fig. 9. Effects of electrical stimulation of the
tymbal motoneurone of Tympanistalna gastrica
(20Hz) and concomitant electrical stimulation
of the tensor nerve at frequencies up to 200Hz.
Insets show sound recordings of a tymbal cycle
with electrical stimulation of the tensor nerve
and illustrate how sound amplitude and time lag
were determined for IN sound pulses (filled
symbols). OUT, open symbols. (A) There was a
sudden reduction of the IN sound pulse
amplitude at stimulation frequencies higher than
30Hz. (B) The time lag from stimulation of the
tymbal motoneurone to the IN sound pulses
decreased sharply at stimulation frequencies
higher than 30Hz (mean values ± S.D. from five
males). (C) Relationship between amplitude and
time lag from electrical stimulation of the tymbal
motoneurone for IN and OUT pulses from a
tensor nerve stimulation series. Amplitudes are
normalized to the amplitude of the loudest IN
pulse. The amplitude and time lag values
decreased with electrical stimulation of the
tensor nerve. IN (filled symbols), OUT (open
symbols); data from one male.
1543Tensor muscle in cicadas
tymbal frame. Hence, the shape of the tymbal relates to the
force that is required to buckle it and, via the force produced
by the tymbal muscle, also relates to the amplitude and time
lag of the sound pulse. Thus, it is the construction of the tymbal
frame which determines the effect of tensor muscle
contraction: an increase in convexity in Tett. josei and Tett.
argentata, but a decrease in Tymp. gastrica. Such opposite
effects of tensor muscle action have been reported previously
for other species (an increase in amplitude by Pringle, 1954a;
Hagiwara, 1956; Simmons and Young, 1978; a decrease in
amplitude by Weber et al. 1988; Hennig et al. 1994). In these
cases, however, the mechanism is likely to be less dependent
on the construction of the tymbal frame. The range of
amplitude modulation described previously differs greatly
from the effects observed here: less than 6dB (Pringle, 1954a;
Hagiwara, 1956; Simmons and Young, 1978; Weber et al.
1988; Hennig et al. 1994) compared with 10–20dB in the
present study. It is quite conceivable that these differences are
related to the buckling mechanism of the tymbal: Popov (1975)
distinguished tymbals with fewer than four ribs which buckle
virtually synchronously to produce one IN and one OUT sound
pulse and tymbals with more than four ribs which buckle
sequentially so that each rib produces one sound pulse with the
OUT pulse being quite quiet. Intermediate types where the ribs
buckle sequentially, but with a very short delay, such that the
pulses fuse also occur. It appears that only tymbals of the first
type show a strong amplitude modulation caused by the tensor
muscle and that this modulatory range may also be related to
the stiffness of the tymbal itself. Tymbals which produce one
IN and one OUT sound pulse are considered to be rather stiff
(see Fig. 6; Popov, 1975). However, force measurements
showed that the tymbal of Tymp. gastrica is quite soft. As yet,
it is not possible to compare the results of the force
measurements of the tymbal as a measure of its stiffness, but
comparative research directed towards both a morphological
0.8
0
0.2
0.4
0.6
1.0
Normalized sound amplitude
−20 −15 −10 −5051015−25
Time difference (ms)
OUT
IN
el.stim. Te.N.
Sound
el.stim. A.N.
∆tvar
A
Tymbal plate Tymbal plate
Tensor sclerite
Tensor
sclerite Tensor
sclerite
Tymbal
plate Tymbal
plate
Ribs Outward
Outward
Inward
No tensor contraction No tensor contraction
Tensor contraction Tensor contraction
Inward
Ribs
Tensor sclerite
Ribs Ribs
ATettigetta josei Tympanistalna gastrica
Fig. 10. Dependence of the amplitude of IN sound pulses on the
relative timing of tymbal motoneurone (A.N.) and tensor nerve
(Te.N.) stimulation (el.stim.) in Tympanistalna gastrica. Electrical
stimulation of the tensor nerve from 15 ms before to 5ms after tymbal
motoneurone stimulation abruptly changed the sound pulse amplitude.
Amplitudes are normalized to the amplitude of the loudest IN pulse.
IN, filled symbols; OUT, open symbols; data from two males. The
inset defines the time difference (∆tvar) between the two stimulus
pulses.
Fig. 11. Perspectively flattened view of the
tymbal of Tettigetta josei (A) and Tympanistalna
gastrica (B) and the areas on the tymbal which
show inward (open arrows) or outward (filled
arrows) movements resulting from the
contraction of the tensor muscle. The anterior of
the male is to the left. In Tymp. gastrica, there
was also a joint-like movement in the tymbal
frame ventral to the tensor sclerite indicated by a
dot and two arrows pointing in opposite
directions. Schematic cross sections through the
medial region of a tymbal (perpendicular to the
ribs) are presented below the tymbals. The
observed movements due to contraction of the
tensor muscle are shown.
1544
and a functional description of the tymbal will certainly allow
a much better understanding of the principles and variations of
sound production in cicadas.
Speed of action by the tensor muscle
The phasic contraction and fast effect of the tensor muscle
observed here are in sharp contrast to the known tonic action
of the tensor muscle (Pringle, 1954a; Hagiwara, 1956;
Simmons and Young, 1978; Weber et al. 1988; Hennig et al.
1994). However, the action of the tensor muscle described here
is not only phasic but also tonic for two reasons. First, the
phasic action accounts for only 30% of the amplitude
modulation in both Tettigetta species. In order to obtain the full
range of amplitude modulation in these species, the tensor
muscle had to be activated at frequencies higher than 50Hz.
Second, even though the tensor muscle action is very fast,
values of intermediate amplitude are observed both in our
stimulation experiments and in the calling song of the
Tettigetta species (Figs 4, 5, 7; Fonseca, 1991). In
Tympanistalna gastrica, the mechanical construction of the
tymbal frame enhances the fast effect of tensor muscle action.
An important prerequisite for such a fast action [10–20ms
compared with 0.5s (Hennig et al. 1994) to 2s (Simmons and
Young, 1978)] seems to be the increased mobility of the tensor
sclerite due to the soft membrane (Fig. 2A,C). However, there
are other modifications necessary for such an effect: most
importantly, the timing of tensor muscle activity with respect
to tymbal muscle activity becomes crucial in order to produce
the species-specific signal. Notably, the change in time lag of
the sound pulse due to the change in the convexity of the
tymbal is rather large, i.e. approximately 30% of the
contraction period of one tymbal muscle during the calling
song (Tett. josei, Figs 3, 4; Tymp. gastrica, Figs 8, 9). While
in many cicadas the tensor muscle enables the male to increase
the sound level of the mate-attracting signal in an unspecific
manner, tensor muscle activity in Tettigetta and Tympanistalna
species contributes much to the species-specificity of the
signal. Besides the peripheral modifications in the morphology
and mechanical properties of the tymbal and tymbal frame,
changes in muscle physiology from a slow- to a fast-
contracting muscle and changes in the fine tuning of central
nervous coordination, must have taken an important place in
generating the specific calling song of these cicadas.
We thank F. Huber for his support of this work and for his
comments on the manuscript. We would like to thank T. Weber
and T. E. Moore for stimulating discussions about our data, B.
Ronacher for critically reading the manuscript and H. Bamberg
for technical support. We also thank two anonymous referees
for their critical comments on an earlier version of the
manuscript. We gratefully acknowledge Brüel and Kjaer
Portugal for the loan of equipment for measuring the acoustic
conditions of our apparatus.
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P. J. FONSECA AND R. M. HENNIG
