The mechanics of sound production in Panacanthus pallicornis (Orthoptera: Tettigoniidae: Conocephalinae): the stridulatory motor patterns
1 Department of Zoology, University of Toronto at Mississauga, 3359
Mississauga Road, Mississauga, Ontario, Canada, L5L 1C6
2 Integrative Behaviour and Neuroscience Group, Department of Life Sciences,
University of Toronto at Scarborough, 1265 Military Trail, Scarborough,
Ontario, Canada, M1C 1A4
* Author for correspondence (e-mail: fmonteal{at}utm.utoronto.ca)
Accepted 27 January 2005
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Summary |
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Key words: sound production, katydid, Panacanthus pallicorni, resonance, stridulatory mechanisms, biomechanics, bush cricket, wing movements, stridulation
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Introduction |
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The mechanism of stridulation in katydids has received less attention
(Bailey, 1970;
Morris and Pipher, 1972
). In
contrast to crickets, katydids include both pure-tone and broadband signals
(although most species produce broadband signals), and the fundamental
frequency, fD, of pure-tone katydid calls can range from
the low audio up to extreme ultrasonic (>100 kHz;
Mason et al., 1991
). Moreover,
katydids produce acoustic signals without the collateral vibration of the two
tegmina, which in katydids are highly asymmetrical. It is unknown whether the
existing model for stridulatory sound production (i.e. the clockwork cricket;
Elliot and Koch, 1985
) applies
to katydids, or whether the same mechanism can also be used to produce
broadband signals. Bailey
(1970
) concluded that the
mirror frame (wing veins surrounding sound radiating membranes) was essential
for pure-tone production in katydids, stating that it behaves as a tuning
fork. Morris and Pipher (1967
)
suggested that the mirror frame vibrates as a cantilever, independent to the
rest of the tegmen. More recently, Bennet-Clark
(2003
) speculated that
pure-tone sound production in katydids was similar to that used by crickets,
i.e. an escapement mechanism.
The genus Panacanthus is a monophyletic group of katydids with
well-resolved phylogenetic relationships and in which a wide range of song
types is represented (Montealegre-Z and
Morris, 2004). In this paper, we investigate the mechanics of
sound production in the katydid Panacanthus pallicornis Walker. In
the phylogeny of Panacanthus this species succeeds P.
cuspidatus, the most basal species in the cladogram. P.
cuspidatus is the only species of the genus producing a pure-tone song
(at 10 kHz), while P. pallicornis produces sustained sound pulses
with a low sharply tuned frequency peak of
5 kHz and also a broad band
frequency range between 15 and 25 kHz (see sound description for more
details). None of the other members of this genus produces sustained sound
pulses or narrow spectral peaks. It thus appears that the evolution of signal
characteristics in this genus has proceeded from a pure-tone ancestral
condition to more broadband sound along the phylogeny
(Montealegre-Z and Morris,
2004
). The song of P. pallicornis appears to be
intermediate between pure-tone and noisy song types. It has a dominant
spectral peak in the audio range below 10 kHz, but also contains strong
broadband components. In this paper we will focus on the characteristics of
the sound produced, the anatomy and some physical properties of the
stridulatory apparatus and the stridulatory motor patterns. We repeat some of
the measurements made on crickets by Bennet-Clark
(2003
) to facilitate
comparisons with that group, and address the question of whether similar
stridulatory mechanisms can account for sound production in both katydids and
crickets.
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Materials and methods |
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Acoustic recordings and analysis
Acoustic recordings in the field
Males of Panacanthus spp. were located by their loud calls. Some
specimens were recorded in the field with audio-limited equipment (120
kHz) using a Sony Walkman WM D6C Professional cassette tape recorder and ECM
909 Sony microphone. Ambient air temperatures were taken using either an Omega
HH23 digital thermometer (Stamford, CT, USA) or an alcohol thermometer.
Acoustic recordings in the laboratory
Specimens were transported to the University of Toronto, Canada, where
their songs were recorded with wide bandwidth equipment (1100 kHz).
These recordings were performed using Brüel & Kjær (B&K,
Nærum, Denmark) equipment: a 1/4'' (Type 4135) condenser microphone
was connected to a sound level meter (Type 2204). Each insect sang from an
individual small cylindrical cage constructed of aluminium screen (mesh size
6/cm), pinned to a base of sound-absorbent material. The output from the sound
level meter went to a Racal instrumentation tape recorder running at 30''
s1 or was digitised (Tucker Davis, System II, Alachua, FL,
USA) at a sampling rate of 100 or 170 kilosamples per second and stored to the
hard disk of a computer. Digitised signals were low-pass filtered at 100 kHz
to avoid aliasing. Sound levels (re 20 µPa) were measured with the 2204
sound level meter (Fast or Impulse/Hold as indicated), usually at a distance
of 10 cmfrom the dorsum of the insect singer. Power spectra and spectrograms
were calculated using DADISP 4.1 (DSP Development Corp., Newton, MA, USA) or
Matlab software (The Mathwords, Natrick, MA, USA). All statistical analyses
were carried out using R software
(www.r-project.org).
Zero-crossing analysis
In order to make detailed comparisons of sound generation, anatomy of the
stridulatory file and wing movements (see below), we analysed songs with the
Zero-crossing module for Canary software (Cornell University, Laboratory of
Ornithology). Zero-crossing v.3 was provided by K. N. Prestwich. Songs were
low-pass filtered with a 7.5 kHz cutoff to isolate the fD.
Zero-crossing analysis computes the signal frequency cycle-by-cycle by
detecting the timing of zero crossings to compute the reciprocal of the period
of individual cycles of sound production, and is therefore suitable for
pure-tone signals. By low-pass filtering at 7.5 kHz to remove higher frequency
components (Krohn-Hite Model 3382 filter 8 pole LP/HP Butterworth/Bessel;
Brockton, MA, USA) in vivo, we could examine cycle-by-cycle variation
in fD for comparison with the spacing of teeth on the
stridulatory file and the velocity of wing movement during sound production
(see below).
Morphology of the stridulatory apparatus
Mirror morphology and the main areas of activity
We examined the morphology of the mirror and scraper using electron
microscopy. We measured the thickness of various regions of the mirror and
determined the detailed anatomy of the scraper. Parts of the tegmina were
dissected and then embedded in Spur's solution; transverse sections were made
with a microtome, according to the process of
(Di Sant' Agnese and De Mesy Jensen,
1984).
The vibration modes of a membrane have nodal lines or curves that divide
the membrane into areas vibrating with opposite phase
(Fletcher, 1992). In
preliminary experiments, the mirror surface was studied to find its main areas
of activity. The method used was similar to that described by Sismondo
(1979
). Specimens were lightly
anaesthetised in CO2 and a thin layer of talcum powder spread over
the mirror surface. The large size of the specimens allows excitation of the
right tegmen by manually engaging the scraper and pushing it over the left
stridulatory file.
Observations were made under a dissecting microscope: manual excitation of the system generated sound and produced a displacement of powder particles in areas of maximum vibration. Three areas of major activity were detected inside the mirror (areas 1, 3 and 4, Fig. 1). Other regions were chosen to represent parts of the tegmina of different thickness and position relative to the mirror so that we could study in more detail how all parts of the tegmina contribute to sound radiation. These data will be presented in a subsequent paper.
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The stridulatory file
The stridulatory file was studied by scanning electronic microscope (SEM)
using a Hitachi (Tokyo, Japan) electron microscope at the Department of
Zoology, University of Toronto. Analysis of the file morphology was performed
on digitised SEM photographs using the dimension tool of a drawing program
(Corel Draw 10, Corel Inc.). Inter-tooth distances were measured from the edge
of the cusp of one tooth to the cusp of the next one
(Fig. 2). For comparison, we
also made similar measurements of the stridulatory file for other species in
this genus (P. cuspidatus, P. gibbosus, P. varius, P. intensus). Only
single specimens of some of these species were available.
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Stridulatory wing movement recordings
We recorded stridulatory wing movements and associated sound production
from eight males. Sound production was monitored with either a ''
microphone (Larson Davis Laboratories model 2540, Provo, UT, USA) or a B&K
'' microphone type 4939. Wing movements were recorded using an
opto-electronic device (von Helversen and
Elsner, 1977
; Hedwig,
2000
). For recording wing movements, a small piece of reflective
tape (Scotchlite 7610 and 8850 retro-reflective tape manufactured by 3M and
distributed by Motion Lab Systems Inc., Baton Rouge, LA, USA) was placed on
the forewing and its position was monitored with a photodiode. Movements of
the forewing evoke changes in the current of the diode, which were recorded
simultaneously with sound output. Sound and wing-movement signals were
recorded on separate channels of a computer data acquisition board and
analysed using Dadisp or Matlab software (in initial recordings sampling rates
were 250 kHz for sound and 31.25 kHz for wing movements, and 100 kHz for both
in most recordings). The temperature in the room was 23.9±0.85°C.
The reflective tape (1x3 mm) was attached to the left tegmen, in a
manner that allowed movements to be recorded in either dorsal (perpendicular
to the wing surface) or posterior view (in the same plane as body axis). Most
recordings were obtained from the posterior view.
After the specimens had been recorded several times and the wing movements characterised, several teeth of the file were removed using a dentist's turbine drill, whose cutting edges were reduced to 0.1 mm in diameter. Teeth were removed carefully in two or three regions, mainly from the middle portion of the file. A space of several teeth (1030) was left between gaps. This allowed us to associate sound oscillations with tooth-scraper contacts or with jumps of the scraper over several teeth, and also to evaluate the functional parts of the file.
We also recorded wing movements using high-speed video (Redlake Motionscope
PCI1000s, San Diego, CA, USA). The high-speed video system was synchronised
with a computer data acquisition board (National Instruments PCI6023e, Austin,
TX, USA; 16 bit, 200 kHz sampling rate) using Midas software (2000 Xcitex
Inc., Cambridge, MA, USA) for simultaneous recording of sound production. In
some cases the position detector was connected as a third channel, so that
wing movements were simultaneously recorded in two modalities: high-speed
video and photo-response of the diode. Recordings were acquired at 500 or 1000
frames s1 for high-speed video, and a sound sampling rate of
100 or 200 kHz. Specimens were put on an artificial perch and the camera was
aligned and focused directly on the stridulatory field, either dorsal, lateral
from the right side or focusing the file and scraper from the posterior. A
'' microphone (B&K 4939), connected to a B&K Nexus
Amplifier (Type 2690), was directed to the specimen in dorsal view. Data were
analysed frame-by-frame using MIDAS software. These recordings were intended
to study the wing velocity during sound production and to identify the
functional parts of the file.
Experimental manipulation of wing membranes
As a preliminary investigation of the contribution to sound production by
specific regions of the mirror, we recorded songs from five specimens before
and after removal of one or more mirror membranes. Wing membranes were removed
with a fine soldering iron. Specimens were initially recorded in a soundproof
room with intact wings, as described previously. Subsequently area 1 was
removed in three specimens and their songs re-recorded after 48 h. Then the
membrane of area 3 was removed and the specimens were recorded again after
another 48 h. Finally, the membrane of area 4 was removed and the process
repeated. The remaining two specimens were treated in similar way, but instead
of removing parts of the mirror in different steps, areas 1, 3 and 4 were
removed at the same time.
In a separate set of experiments (N=4), we modified single tegmina by painting them with liquid latex. This material dried as a layer of latex that adhered to the wing surface and could be removed by simply peeling it away. This allowed us to measure the effect of loading each wing individually in a single specimen. Specimens were recorded before application, with the latex applied to one wing, and again following removal of the latex.
Simulation of tooth-scraper contacts
After the calls and wing movements of intact specimens were recorded, some
specimens were anaesthetised in CO2 and the right or left tegmen
removed. The wing hinge was sealed with bees' wax in order to halt bleeding.
The tegmen was attached to a metallic rod by bees' wax at the position of the
wing hinge (Fig. 3).
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Wing vibrations produced by artificial tooth-scraper contacts (clicks) were recorded for areas 1, 3 and 4. In these experiments, clicks were generated with a dissected file or scraper. Thus the right tegmen was driven via its scraper using an excised file and the left tegmen was driven with a dissected scraper via its file. In both cases fine movements of either the dissected file or scraper were performed with a micromanipulator, in order to control for individual tooth impacts. We took into account the angle of the scraper and file during stridulation as observed in our video recordings of wing movements. The preparation was mounted in a similar way for every experiment.
The reaction of the membrane was transduced by the laser vibrometer. A probe microphone (B&K Type 4138) was placed within 5 mm of the specimen. Alignment of the microphone and laser beam is shown in Fig. 3. The microphone and laser vibrometer signals were digitized and stored in a computer (TDT System II, 100 kHz sampling rate). All experiments were performed on an anti-vibration table. The laser allows for accurate measurements of vibration in specific regions, while the microphone was used to monitor the output song of the particular area studied and all surrounding regions. The three main areas found by particle displacement of talcum powder were studied with laser vibrometry (Fig. 1). The same regions were studied in the left tegmen and three plucks were recorded in each area.
The quality factor Q is a measure of the of the response peak of a
system. Q is given by the ratio between the frequency at peak output
and the bandwidth at half power (Fletcher,
1992; Arya, 1998
;
Bennet-Clark, 1999b
). Systems
with higher values of Q have greater response at the peak frequency,
therefore large amplitudes at resonance and small bandwidth. Systems with low
Q values have lower peak response and broad bandwidth. Resonant
biological systems tend to have small Q values in the range from 1 to
about 30 (Fletcher, 1992
). We
calculated the Q-factor for both forewings based on the recordings
mentioned above, using the method proposed by Bennet-Clark
(1999b
).
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Results |
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Spectrograms were performed for 20 different individuals. From these studies it is clear that each individual produces a complex but consistent spectrum and different individuals produce somewhat different spectra (Fig. 4D). In all individuals there is a portion of the call in which the relative amplitude of higher harmonic peaks in spectrum increases. We refer to this as the harmonic portion of the song. This tends to occur in the middle one quarter to one third of the song; however, there is considerable individual variation in the timing of this harmonic portion (Fig. 4D).
Morphology of the stridulatory apparatus
Anatomy of the right tegmina
As in most tettigoniids, in Panacanthus the left forewing wing
overlaps the right one. The right tegmen has most of the specialised
structures for sound radiation (i.e. the mirror cells, veins and surrounding
areas) and these are located in the dorsal field. Homologous regions can be
identified in both wings, but in the left wing they are thicker. Sound is
generated when a specialized region of the right tegmen (the scraper,
Fig. 5) is pushed across a
specialized vein (the file, Fig.
2) on the under surface of the left tegmen. The teeth of the file
deflect the scraper, causing the right wing to bend until the scraper is
released. This catch-and-release mechanism induces oscillations in the mirror
membranes resulting in the radiation of sound from the tegmina
(Pierce, 1948).
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The mirror of the right tegmina consists of complex cells
(Fig. 1B). There are actually
two major cells. One is a sub-quadrilateral region enclosed by the thick veins
A1 and A1+A2. The mirror, measured from the vein A1 to the distal part of the
frame, is 4.11±0.20 mm in length (N=20). The other region is
an adjacent sub-triangular region bounded by the Cubital veins and A1. This
cell is longitudinally divided by a fine vein and the claval fold
(Desutter-Grandcolas, 2003).
The surface of the sub-quadrilateral is diagonally shallowly depressed; the
depression extends from the left inferior corner to the right superior (Area
1, Fig. 1B, broken white line).
On the left side, this cell is isolated from the rest of the wing by a thicker
vein, formed by the fusion of A2 and A1. The surface of the membrane of the
triangular region is even more complex, presenting a small but deeper
concavity on the region adjacent to A1 (Area 3) and another, larger but
shallower, parallel to the claval fold (Area 4,
Fig. 1B). However, the concave
surfaces of Area 1 and Area 3 form a continuous curvilinear depression that is
interrupted just by a fine vein probably derived from A1
(Fig. 1B, broken line); these
zones differ from the rest of the membrane in their transparency. Another
elongated cell is formed by veins A2 and A3 in the basal portion of the anal
margin; we recognized this cell as Area 7 (Figs
1,
5). Different regions of the
tegmina differ in thickness (Fig.
5B).
The scraper is a very complex structure
(Fig. 5A,B). It is framed by an
extension of vein A4 (Fig. 5A);
its active area of contact is a sharp edge 2.58±0.06 mm in length
(range 2.52.7 mm, N=12) and 35±4.5 µm thick in its
widest part (range 3140, N=3,
Fig. 5B). The sharpest part of
this edge is narrower than the widest part described above; hence the scraper
is triangular in cross-section (Fig.
5B,C). As the file teeth are triangular in profile (see below),
the triangular shape of the scraper allows it to fit between adjacent teeth on
the stridulatory file despite variation in inter-tooth spacing. The scraper
active area is easily distinguishable because it is strongly sclerotized and
darkened. There is a space of 1.56 mm between the scraper edge and the robust
vein A1+A2 that surrounds the mirror. Dividing this space there is a thick
vein formed by a branch or an extension of A3. As a result of this division,
this complex region comprises two cells: one close and almost perpendicular to
the mirror plane (100°), formed by a thick mass of soft tissue and
elastic cuticle (thick membrane in Fig.
5A,B); the other adjacent to vein A1+A2, is the subsclerotized
Area 7. Microtome sections reveal that the scraper is dorsally connected to
the rest of the tegmen by a layer of elastic cuticle. Another layer, which
seems not to be directly connected to the scraper but partially isolated, is
positioned ventrally. There is a gap between this area and the scraper,
because the cuticle beneath is not continuous; this gap is covered with soft
tissue (Fig. 5C). Both dorsal
and ventral layers of cuticle are connected basally, i.e. they are part of
same region (the thick membrane) that bifurcates to form the dorsal and
ventral layers. The scraper morphology differs from that of crickets, and this
model seems widespread in Tettigoniidae
(Anstee, 1971
;
Montealegre-Z and Morris,
2003
; F.M.-Z, unpublished), suggesting that it might operate
differently (see Bennet-Clark,
2003
).
The stridulatory file in Tettigoniidae has traditionally thought to be a
modification of the vein Cu2 or cubital posterior
(Ragge, 1955;
Desutter-Grandcolas, 1995
).
However, more recent studies suggest that the stridulatory file originated
from the vein A1 (Desutter-Grandcolas,
2003
); our description is based on the latter wing venation
nomenclature. In the ventral part of the right tegmen, the vein A1 does
conserve some features of a stridulatory file, although it is dramatically
shorter and narrower than its counterpart in the left wing (the functional
stridulatory file).
Anatomy of the left tegmina
Like most tettigoniids, P. pallicornis is unable to switch wing
overlap as the two tegmina are highly asymmetrical
(Fig. 1A). The most important
component of the left wing for sound production is the stridulatory file,
through which the wings are excited during stridulation.
The stridulatory file of P. pallicornis is 6.47±0.09 mm in
length (N=16, mean ± S.D.). It is laterally curved
(Fig. 2D), and dorsoventrally
arcuate. The number of teeth varies from 210253 (N=16). In
profile, teeth are laterally compressed, but the engagement side (distal part)
is vertical with respect to the horizontal base; its contra-lateral side is
more obtuse (Fig. 2). When seen
in lateral view, this asymmetry gives a triangular aspect to every tooth, so
that teeth present a steep face to the scraper during the engagement. The file
is massive, therefore it seems mechanically unlikely that tooth-scraper
interactions and vibrations of the rudimentary left mirror (F. Montealegre-Z
and A. C. Mason, manuscript in preparation) generate bending vibrations of the
file at the frequencies radiated by the tegmina with sufficient amplitude to
release the scraper during each oscillation, as suggested for the escapement
mechanism of crickets (Bennet-Clark,
1999a,
2003
).
There is an overall trend for teeth to be more widely spaced towards the
end of the file (Figs 2A,
6A), but spacing is highly
variable. Average inter-tooth distance increases over the anal approximately
one fifth of the file length, then stabilises and decreases slightly in the
last basal one fifth or one quarter. Half of the total number of teeth are
concentrated in the anal third of the file, i.e. where the teeth are engaged
at the beginning of sound production (Fig.
6B). In this portion of the file, teeth occur at an average
density of 46 teeth mm1, while in the basal two thirds
of the file, teeth occur at an average density of 29 teeth
mm1. Thus, the file presents regional differences in
inter-tooth spacing at the anal and basal ends
(Fig. 6A). The tooth spacing
seems to be less consistent than that of gryllids studied as models of
pure-tone generators (Bennet-Clark,
2003
). Comparison of the file-tooth spacing among several
Panacanthus species (Fig.
6C) shows a range of patterns and variability in tooth spacing.
Panacanthus cuspidatus and P. pallicornis have the most
regular distribution of file teeth, and a pattern of increased tooth spacing
along the length of the file. In P. gibbosus, P. intensus and P.
varius, tooth spacing is less regular and inter-tooth distances are
greatest in the middle portion of the file. Details of file structure and
sound analysis of these species can be found in Montealegre-Z and Morris
(2004
).
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Both tegmina have the common feature of having the costal and apical fields made of a very flexible soft tissue. This ductile region extends towards the distal portion of both wings. Another remarkable feature of both forewings is that the radial field is very swollen, giving the tegmina a globular contour in this region. The radial field is completely isolated from the costal field by the veins R and M. When the insect is singing, the costal fields of both tegmina remain attached to the abdominal pleura and these swollen portions and stridulatory field form a chamber.
Identification of main areas of vibration
We used observations of particle vibration over the mirror to identify
maximal tegminal areas, but for the purposes of this paper we did not attempt
to quantify the relative vibration of different wing regions. Quantitative
vibration measurements of both tegmina were made using a laser vibrometer, but
these results will be presented in a subsequent paper. Areas 1, 3 and 4
presented the major displacement of talcum powder particles. Area 1 vibrated
with greater amplitude than 3 and 4, where particle movement was reduced.
Particles move from these areas and tend to accumulate outside of the mirror,
on a sharp depression between Area 6 and the posterior part of the mirror
frame (Fig. 1B). Areas 3 and 4
are concave regions that are more transparent than the rest of the thicker
surrounding membrane in which they are embedded. These regions show strong
phase independence during particle displacement. Phase independence was first
observed under a stereomicroscope and confirmed with laser vibrometry (data
not included in this paper).
Wing movements
Sound emission coincides with the entire course of tegminal closure (Figs
7,
8). Both wings are raised above
the body to an angle of about 45° (viewed laterally and taking the wing's
resting position as 0°). If viewed dorsally, when the scraper begins to
contact the first teeth of the file, each wing is opened at a maximum of
27° (from a resting position). Viewed from the posterior, in the same
action each wing is lifted about 49° from the horizontal plane of the
body. A small change in amplitude of the wing-movement signal occurs during
the closing movement as the scraper first contacts the file of teeth
(Fig. 7B). The pattern of
stridulation involves a single opening and closing stroke without pause, and a
single type of phonatome. The total opening and closing of the forewings
(phonatome period) lasts 120 ms, and the effective time for sound
production varies from approximately 4060 ms (N=10).
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High-speed video and opto-electronic recordings show that during sound
generation (closing stroke), the entire length of the stridulatory file is
used and the velocity of the scraper gradually increases (Figs
7,
8). The velocity of the closing
stroke was calculated by measuring the displacement of a specific point on the
wing every five frames (i.e. over time intervals of 5 ms for 1000 frames
s1 or 10 for 500 frames s1). This
measurement was repeated for about eight consecutive stages during a single
wing-stoke (N=3 specimens). The average velocity of the scraper
movement along the file is 120 mm s1. Wing velocity
data calculated by taking the derivative of the position sensor signal give
higher resolution (Fig. 8) and
indicate variation in velocity over the course of a single wing cycle, but
still show an overall increase over the course of a wing-stroke. The wing
velocity abruptly, but briefly, increases when the pulse is complete and the
scraper disengages from the file before the forewings recover their resting
position.
The engagement of the scraper can be studied precisely from these
recordings. The active contact area of the scraper changes during one closing
stroke, as described for the cricket Teleogryllus oceanicus
(Bennet-Clark, 2003). The first
teeth of the file are contacted by the distal part of the scraper; then the
contact area is gradually shifting to the anterior mesal portion during the
closing stroke. That is, there is a moderate but detectable relative movement
of file and scraper perpendicular to the direction of wing closing (data not
shown).
Recordings using the opto-electric position sensor show that high frequency
`ripples' in the position signal are detectable when sound and wing movements
are shown at full resolution, corresponding to the sound-radiating
oscillations of wing membranes likely generated by tooth impacts
(Fig. 8C). This is consistent
with previous observations indicating that tooth contacts occur at a frequency
similar to the calling song frequency
(Suga, 1966;
Koch et al., 1988
;
Hedwig, 2000
).
Manipulation of wing membranes
Removal of mirror membranes of the right wing
After removal of Area 1, there was no change either in the song envelope or
in the spectrum. A minor reduction in intensity was noticed in all cases,
especially at frequencies between 15 and 25 kHz, similar to the observations
of Morris and Pipher (1967)
and Keuper et al. (1988
).
Removal of regions 3 and 4 resulted in a reduction of the relative power of
fD and a significant increase in the frequencies of
spectral peaks (Fig. 9,
Table 1). Increments in
frequency, after removal of mirror regions, have also been reported in other
katydids (Morris and Pipher,
1967
; Keuper et al.,
1988
) and are consistent with a decrease in the mass component of
a resonant system (Arya, 1998
).
In some specimens (previously recorded intact) we excised all regions at once
and results were similar. Fundamental and harmonic components increased in
frequency and the relative power of the fundamental decreased after ablation
of Areas 3 and 4.
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Loading of wings with latex
When the left tegmen was loaded, the overall characteristics of the song
were not changed, but there was a decrease in frequencies in the harmonic
segment of the pulse (paired Wilcoxon test P<0.029,
Fig. 10A,B, Table 2), as well as a decrease
in the amplitude of the call. These results are consistent with increased
damping in a resonant system (Arya,
1998). The original spectral properties of the song were restored
following removal of the latex (Fig.
10C). When the right tegmen was loaded, the harmonic segment of
the pulse no longer occurred (Fig.
10D).
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|
Removal of file teeth
Recordings of specimens in which two or three groups of teeth were removed
(separated by a segment of intact teeth) corroborated our results showing a
one-to-one correspondence between file teeth and cycles of the fundamental
song frequency. Gaps in the song corresponded to the segments of missing
teeth, and the number of cycles generated in the intervening segment matched
the number intact teeth between the regions of ablation
(Fig. 11A,C). Removal of file
teeth had little effect on the overall spectrum of the song. But a comparison
of the spectrograms and wing movements from the same individual before and
after ablation of file teeth showed differences in the spectral quality of the
sound produced, as well as the obvious changes in the time-domain
(Fig. 11). The harmonic
segment of the song was not produced after removal of file teeth, and the
velocity of wing movement was erratic and did not show a clear acceleration
towards the end of the pulse as in the intact song
(Fig. 11B,D).
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Zero-crossing analysis, wing velocity and sound quality
Zero-crossing analysis indicates that the fD is quite
constant over the course of a single pulse, particularly during the harmonic
portion of the call. There is no `glissando' as observed in crickets
(Simmons and Ritchie, 1996;
Bennet-Clark and Bailey, 2002
;
Bennet-Clark, 2003
) and in some
katydids (Bailey and Broughton,
1970
). The frequency is more or less constant as the pulse
progresses, regardless of increments in inter-tooth distances, except on the
anal and basal ends of the file, where tooth distribution is different (Figs
6,
12). For one specimen we were
able to obtain complete measurements of the inter-tooth distances for the
stridulatory file, as well as sound and simultaneous optical recordings of
wing movement. Using cycle-by-cycle frequency measurements and file tooth
spacing, we calculated the instantaneous velocity of wing movement over the
course of an entire wing stroke that would be predicted if each cycle of the
fD of sound output corresponded with a single impact of
file and scraper, as in crickets (Elliot
and Koch, 1985
). In other words, using the actual sound output and
file morphology, we calculated the wing closing velocity that would be
required to maintain regular phasing of tooth impact with respect to
sound-radiating oscillations of the wings. We compared this `ideal'
wing-velocity trace with the measured wing velocity data derived from optical
recordings of wing movement (Fig.
13). The wing velocity required to match cycle-by-cycle frequency
with the timing of tooth impacts is also quite stable, whereas the actual wing
velocity accelerates over the course of sound production (Figs
7,
13B). There is a discrepancy
between the expected and calculated velocities; initially, the actual wing
velocity (Fig. 13, blue line)
is lower but approaches the predicted velocity (green line) near the strongly
harmonic region of the pulse and tends to become more erratic towards the end
of the pulse, sometimes oscillating around an average velocity similar to the
predicted velocity (Fig. 13C).
In general, both (measured) wing velocity and cycle-by-cycle sound frequency
were more variable during non-harmonic portions of the call.
|
|
Simulation of tooth-scraper contacts
The excitation produced by simulations of tooth-scraper contacts was
analysed on the three areas of vibration in the right tegmen and on the
homologous areas of the left. The purpose of these recordings was to measure
directly the natural frequency of wing vibrations, fo.
Clicks generated by single toothscraper interactions show a single
abrupt build up and a gradual free decay in each case
(Fig. 14B,C). In the original
recordings, there was a strong component at very low frequencies
(306.7±69.7 Hz, N=7). We suspected that this represented
oscillation of the entire tegmen around its attachment point, i.e. as a
cantilever. We calculated the frequency of vibration for a wing attached to
one end moving as a cantilever (Morris and
Pipher, 1967) using published values for Young's modulus
(Fletcher, 1992
). A wing with
the physical characteristic of that of P. pallicornis would move with
frequencies between 227 and 300 Hz when glued from its hinge to a rigid rod.
We concluded that these low frequencies are the result of the movement of the
tegmina from the tip of the rod to the tegminal apex, and not of the normal
vibration of the mirror and adjacent zones. In the data presented here, this
`whole-wing oscillation' component has been removed by high-pass filtering
(600 Hz cutoff).
|
Simulation of tooth scraper contacts was simultaneously measured with a
probe microphone and with a laser vibrometer. Both measures gave similar
values for fo of the wings
(Fig. 14A). In all cases, the
fo was significantly lower for the left tegmen (mean
± S.D., 4311±235 Hz, N=4) than for the right
tegmen (mean ± S.D., 5101±472 Hz, N=4),
which was close the fD of the song (mean ±
S.D., 5050±173 Hz, N=4). The free vibration of the
right tegmen was moderately lower or higher than the frequency of the calling
song, while that of the left was always lower. Lower free vibration of the
left tegmina, in relation to the species calling song, might have occurred
because of changes in the resonant properties of isolated wings. The
interaction between file and scraper might add mass and stiffness to the
system, as suggested by Bennet-Clark
(2003). Conversely, the mean
values of Q did not differ significantly for both tegmina, i.e.
17.2±5.2 for the left wing and 16.2±8.9 for the right
(F=1.01, P=0.32, N=5). Other aspects of the
physical properties of both wings will be presented in a subsequent paper.
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Discussion |
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---|
Cycle-by-cycle analysis showed that the fD is
relatively constant and does not show the glissando effect observed in
crickets (Leroy, 1966;
Simmons and Ritchie, 1996
;
Bennet-Clark, 2003
). There is,
nevertheless, variation in spectral quality within a pulse. Spectrograms of
individual calls show that a segment of each pulse has a more prominent
harmonic structure while other portions of the same pulse are noisier. The
portion of the call having a more sustained and pure-tone structure varies
between individuals, but is consistent within individuals and corresponds to
periods of stable or accelerating velocity of wing movement during the closing
stroke, and in which the wing velocity matches the inter-tooth distances
allowing regular phasing of tooth-scraper impacts with respect to the sound
waveform (Figs 6,
12,
13). This suggests that
resonance is the main factor setting the fD, but that the
arrangement of file teeth has a strong effect on the quality of tegminal
oscillation, and that tooth impact rate is not strictly regulated during the
course of a stridulatory wing stroke, as it is in crickets. In crickets the
scraper is released by vibrations of the file and other regions of both
tegmina at the fD
(Koch et al., 1988
;
Bennet-Clark and Bailey,
2002
). This model requires a very flexible file that controls
movement of the scraper from tooth to tooth. In crickets the stridulatory file
is believed to act as a spring, releasing the file as it bends upward with
each oscillation of the wing (Bennet-Clark,
2003
). P. pallicornis and its congeners, as well as
several other katydid species, possess a very rigid and massive file. The
amplitude of vibration of the file itself tends to decrease continuously over
the course of a stridulatory wing stroke (F. Montealegre-Z and A. C. Mason, in
preparation). In other words, the stridulatory file in crickets appears to
bend with the tegminal oscillations, consistent with its being located on a
wing that forms part of the sound radiator, whereas the file in P.
pallicornis shows little evidence of bending and is located on the
thicker left tegmen, which does have a major role in sound radiation (F.
Montealegre-Z and A. C. Mason, in preparation). Oscillation of the file in
this species, its congeners and most katydids, should therefore not be
sufficient to control the scraper movement during the closing stroke. The
massiveness and rigid nature of the file and complex scraper anatomy suggest
that sound production is governed by the mechanics of the scraper as it moves
along a passive file. It should be noted, however, that the escapement
mechanism of crickets does not strictly require the degree of flexibility in
the file that is usually assumed. Oscillations of the scraper-bearing wing
alone could dislodge the scraper from file teeth by a mechanism analogous to
what we propose here (see also Bennet-Clark,
1989
,
1999a
).
The mechanics of the scraper
Fig. 15 outlines the
mechanism we propose for the regulation of movements of the scraper during
stridulation in P. pallicornis. When the scraper is released from a
tooth, it accelerates forward until it strikes a subsequent tooth. This impact
is associated with the emission of high frequency sound (red asterisk,
Fig. 15B, see
Bennet-Clark and Bailey,
2002). Likely the complete scraper region from the vein A3 to A1
(or A1+A2) bends upward (Fig.
15A,B). During this action, the thick membrane reduces its extent
(i.e. extends downward) and will force the adjacent elastic cuticle to
strongly bend towards the right side (if seen from the posterior), acquiring a
maximum distortion just as it is released
(Fig. 15C). At this point, the
gap between the opposing and adjacent cuticles is also maximal, and all the
intervening material of this region is stretched
(Fig. 15C). The resulting
deflection of the tegmen constitutes a half-cycle of sound-radiating
oscillation (
0.11 ms; see red wave in
Fig. 15B,C). While this
partial cycle occurs, the wings continue to move past each other and oblige
the scraper to dislodge (Fig.
15C), creating a second high-frequency click sound upon its
release (blue asterisk in Fig.
15D). Elasticity of the system, due to the bifurcation of the
cuticle in this region, will cause the scraper to return to equilibrium during
the next 0.11 ms, while it travels to and contacts the next tooth, completing
the cycle of sound-radiating oscillation. The cycle repeats when the scraper
contacts the next tooth (Fig.
15E). Some of the energy released by each impact will be absorbed
when the adjacent cuticle flexes right. The rest of the energy should be
dispersed during the distortion of the scraper region in the form of
sound-radiating vibration to the rest of the tegmina, primarily radiated by
the mirror of the right tegmen and to a lesser extent by the mirror of the
left (F. Montealegre-Z and A. C. Mason, manuscript in preparation). Put
simply, the time required by the scraper to hit a tooth and travel between two
adjacent teeth corresponds to the period of the sound cycle (
0.22 ms). To
produce a pure frequency, a consistent interval of 0.22 ms is required between
tooth contacts, and the scraper must increase its velocity as the wings'
closing stroke progresses because file teeth are more separated at the basal
end of the file (see Fig. 5A).
Our data are consistent with this. Wing velocity also gradually increases
during the production of a sound pulse (see Figs
11B,
13B,C), which predicts that
tooth impacts will be stronger as the closing stroke progresses. This is
consistent with observations that the sound pulse increases in amplitude
towards the end. Sound amplitude decreases again in the last one quarter of
the pulse, corresponding to decreasing inter-tooth distances in the last one
fifth or one quarter of the file length
(Fig. 5A). These observations
were confirmed with our high-speed video recordings; the complete file is used
during stridulation and wing velocity increases over the course of a
wing-stroke, but decreases at the very end
(Fig. 8D).
|
File morphology
File morphology may strongly affect the sound generation
(Morris and Pipher, 1972;
Walker and Carlysle, 1975
;
Montealegre-Z and Morris,
1999
; Morris and
Montealegre-Z, 2001
). Bailey and Broughton
(1970
) showed that when the
tooth-scraper contact rate and the natural frequency of the tegmina match,
sound energy is greatest and the wave form most pure. We have evidence that
average tooth-contact rate in P. pallicornis matches
fD of the radiated sound. We also show, however, that
there is a significant overall increment from the anal to the basal of the
file in inter-tooth distance, and that inter-tooth distances do not increase
continuously but in an erratic fashion. These discontinuous changes in
distances among teeth along the file will result in irregular phasing of
tooth-contact with tegminal oscillation, inducing non-fD
components, causing changes in the amplitude of the fD
(compared to what it would have been), and in the sharpness of high
frequencies (harmonics) of the spectrum. In stridulatory files of pure-tone
singers (e.g. those of most crickets and P. cuspidatus), the inter
tooth distances increase systematically from the anal to the basal portion of
the file (Fig. 6; see also
Bennet-Clark, 2003
), an
arrangement that favours a constant tooth strike (and in turn a constant
frequency) as the closing velocity increases
(Fig. 15). However, for P.
pallicornis, inter-tooth distances tend to increase more erratically than
systematically, and this may account for some of the variability in the call
spectra. Bennet-Clark (1970) observed that the file-tooth arrangement
resembled the instantaneous amplitude of sound pulses in the mole crickets he
studied. Increments in inter-tooth distances corresponded with increments in
amplitude in the pulse. We found a similar pattern in P. pallicornis.
Increments in inter-tooth space may generate stronger high frequency
transients during engagement and release of the scraper (Bennet Clark and
Bailey, 2002) due to corresponding increments in velocity.
Nevertheless, there is a net increase in the inter-tooth space towards the
basal end of the file. Consequently, the tooth-contact rate is maintained
close to resonant frequency of the tegmina (5 kHz; Figs
12,
15). Notably, this pattern of
increasing tooth spacing was similar in P. cuspidatus and P.
pallicornis, the only species in the genus that produce sustained sound
pulses, with P. cuspidatus having the most pure-tone song
(Montealegre-Z and Morris,
2004
). The other species we examined, which produce transient
pulse trains, show most variable tooth spacing with largest inter-tooth
distances in the middle of the file (Fig.
6C).
Resonance of the tegmina
In this section, we discuss the roles of the right and left tegmina in the
sound radiation, leaving aside those structures responsible for the initial
generation of tegminal vibrations (i.e. the file and scraper). Bennet Clark
(1999a) discusses the general principles of resonant vibration as they relate
to sound production by insects. Our results indicate that sound radiation in
P. pallicornis is based on resonant vibration of the tegmina.
Similarly to previous work (Broughton,
1964; Morris and Pipher,
1967
; Bailey, 1970
;
Keuper et al., 1988
), our
findings show that sound radiation is primarily a function of the right
tegmen. Furthermore, the function of membranes of the mirror appears to be
amplification rather than tuning. Removal of mirror membranes caused only a
small increase in the output frequency, consistent with a decrease in the mass
element of a resonator (Arya,
1998
), as well as a decrease in output amplitude. It has been
proposed that the mirror frame acts as a cantilever whose frequency is
directly proportional to the fD of the calling song
(Morris and Pipher, 1967
;
Bailey, 1970
;
Sales and Pye, 1974
). Based on
this argument, we estimated the frequency of vibration of the mirror of P.
pallicornis, which has a span of about 4.1 mm. Morris and Pipher's fig.
12 (Morris and Pipher, 1967
)
and Bailey's fig. 8 (Bailey,
1970
) indicate a frequency of vibration of the mirror frame of
P. pallicornis of nearly 5 kHz, which corresponds to the
fD of the calling song. This supports previous findings
that the tuning of tettigoniid tegminal resonators resides, in part, in the
structure of the veins surrounding the mirror, rather than the mirror itself
(Broughton, 1964
;
Morris and Pipher, 1967
;
Bailey and Broughton,
1970
).
The natural vibration frequency fo differed for the two
tegmina, being higher for the right than for the left tegmen. The
fo of the right tegmen matched the fD
of the calling song close. Differences in tuning of the two forewings is not
rare in Orthoptera; similar results were presented by Bennet-Clark
(2003) for the cricket T.
oceanicus. Bennet-Clark concluded that the fo of the
file-bearing tegmen, which is always lower when compared with the
contra-lateral wing, might increase during the interaction of both forewings,
as stiffness is added to the system. During the interaction both wings
compensate for optimal values of fo, generating the
fD of the calling song.
The primary role of the left tegmen appears to be to provide damping.
Loading of the left tegmen resulted in decreased amplitude and frequency of
output, as predicted for an increase in the damping coefficient in a forced
resonant system (Arya, 1998).
In addition to reduced amplitude and a shift of the resonance peak to lower
frequencies, increased damping in a forced resonator also results in a
broadening of the relationship between output amplitude and driving frequency;
this effect is described by the quality factor, or Q value. For
high-Q systems, damping is light and there is a dramatic increase in
vibration amplitude when the driving frequency matches the resonant frequency.
But this resonance peak is narrowly tuned and the driving frequency must match
the resonant frequency very closely to maintain this output. In
lower-Q, more heavily damped systems, there is a broader relationship
between output amplitude and driving frequency such that variation in the
driving frequency causes more gradual changes in vibration amplitude. In other
words, a more strongly damped system can be driven over a broader range of
frequencies than a more lightly-damped, higher Q system. In many
mechanical systems, where consistent operation is required, damping serves to
eliminate undesirable peaks in vibration due to varying frequencies of input
energy. In insect sound production, resonance is usually discussed as a
strategy for maximizing output power at the expense of bandwidth
(Michelsen and Nocke, 1974
),
or regulating output frequency
(Bennet-Clark, 1999a
). Our
results suggest that katydids producing broadband acoustic signals, such as
P. pallicornis, may also make use of resonant vibration of sound
radiating structures to improve output efficiency by opting for a more or less
low-Q resonator with a wider bandwidth
(Fig. 14).
The quality of sound output in P. pallicornis depends on matching the timing of tooth-scraper impacts to the frequency of sound produced. Males accelerate their wings during stridulation, generating a frequency sweep of tooth-scraper impact rates. A broader resonance in tegminal vibration should allow a greater portion of the wing-stroke (i.e. a greater range of tooth-scraper impact rates) to result in efficient sound generation than would be possible with a narrower resonance, given the irregularity of the driving force. Therefore, P. pallicornis song may reflect a trade-off between output amplitude and the duration of the song over which a clear frequency structure can be maintained in the absence of a mechanism to directly regulate the tooth-strike rate (such as the escapement mechanism of crickets).
Conclusion
Our results show that the escapement mechanism of the `clockwork cricket'
(Elliot and Koch, 1985;
Bennet-Clark and Bailey, 2002
)
is probably not at work in katydids, even those that produce pure-tone songs.
Sound production in P. pallicornis does rely on the tuned vibration
of tegminal resonators. The excitation of tegminal vibration, however, relies
on a more variable mechanism than the precisely regulated escapement of
crickets. A rigid file and a scraper mounted on a flexible joint allow
stridulatory wing movements to occur at a range of different speeds.
Engagement with file teeth will displace the scraper by deflecting it around
its flexible joint. The subsequent release will allow the scraper to spring
back to its natural position and, combined with continued wing movement, will
result in an impact between the scraper and the next file tooth. This impact
will induce vibrations in the tegmina. When the wing velocity is such that
successive tooth impacts occur at an interval that matches the natural
vibration frequency of the tegmina, resonant vibration will build up in the
wing. By sweeping their wings over a range of velocities during stridulation,
P. pallicornis males, in the absence of a mechanism that specifically
matches the rate of tooth impacts with tegminal vibration cycles, are able to
produce a complex song spectrum that includes a resonant portion when wing
velocity and tooth spacing coincide with the natural mode of tegminal
vibration.
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Acknowledgments |
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