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First published online December 1, 2006
Journal of Experimental Biology 209, 4923-4937 (2006)
Published by The Company of Biologists 2006
doi: 10.1242/jeb.02608
Generation of extreme ultrasonics in rainforest katydids
1 Integrative Behaviour and Neuroscience Group, Department of Life Sciences,
University of Toronto at Scarborough, 1265 Military Trail, Scarborough,
Ontario, Canada, M1C 1A4
2 Department of Biology, University of Toronto at Mississauga, 3359
Mississauga Road, Mississauga, Ontario, Canada, L5L 1C6
* Author for correspondence: (e-mail: f.montealegre{at}utoronto.ca)
Accepted 19 October 2006
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Key words: Orthoptera, Tettigoniidae, ultrasound, bioacoustics, elastic, stridulation, resilin, katydid
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;
Nelson, 1979); percussion
(Stewart and Maketon, 1991);
stick-and-slip (Patek, 2002);
`tymbalation' (Bennet-Clark,
1999), and the most common method: stridulation. The last three
involve a frequency multiplier by which the slower oscillatory movements of
body parts are converted into the much higher frequency oscillations of
sound-radiating structures (Bennet-Clark,
1995; Michelsen,
1998). Here we present evidence that some katydids (Insecta:
Orthoptera: Tettigoniidae), have evolved to produce signals at high ultrasonic
frequencies by making use of a previously unrecognized form of tegminotegminal
stridulation, one which incorporates something of the elasticity of a
`stick-and-slip' mechanism (Patek,
2002), to create a `compound frequency multiplier'. This mechanism
achieves dramatically higher song frequencies at, paradoxically, lower wing
velocities than those of conventional stridulation.
Most Ensifera (crickets and katydids) generate their predominant sound
components on the closing stroke of the forewings
(Pasquinelly and Busnel, 1954;
Morris and Pipher, 1967;
Heller, 1988;
Otte, 1992). Almost all
cricket spp. call with nearly pure tones of 3-8 kHz
(Leroy, 1966;
Bennet-Clark, 1989;
Otte, 1992). Many species of
katydid also call with pure tones, but over a much wider range of carrier
frequency (Heller, 1995;
Morris et al., 1994). Many
katydid carriers are ultrasonic (Pierce,
1948; Suga, 1966;
Montealegre-Z and Morris,
1999) and some species utilize high, >40 kHz, pure-tone
ultrasonics (Morris et al.,
1994; Montealegre-Z and Mason,
2005).
Stridulation of crickets: escapement
Crickets employ resonant stridulation
(Elsner and Popov, 1978). Each
nearly symmetrical forewing has a tuned forewing radiator
(Nocke, 1971). To avoid
destructive interference, oscillation of the left wing radiator is brought
into phase with that of the right by the `push' of each tooth upon a special
region behind the scraper (Bennet-Clark,
2003). The oscillation of the sound-radiating structures on the
two wings then controls the advance of the scraper along the file in a manner
similar to the escapement mechanism of a clock
(Elliot and Koch, 1985;
Koch et al., 1988) and so
gives a 1:1 relation between each radiated sound wave and each contacted file
tooth (carrier frequency (fc)=tooth impact rate).
Pure-tone stridulation of katydids: non-escapement
For katydids producing pure-tone calls, recent evidence points to important
departures from the mechanism of cricket sound production
(Montealegre-Z and Mason,
2005). These katydids generate sustained wavetrains or trains of
short pure-tone pulses. (These pulses are `sustained' in the sense that like
the pulses of crickets they are kept from decaying by input of additional
energy.) Unlike crickets, strongly asymmetric forewings are almost universal
in katydids (Dumortier, 1963).
Their left forewing appears damped and probably has a reduced role in sound
radiation (Montealegre-Z and Mason,
2005). And advance of the scraper along the katydid file will not
be regulated by sound-radiating oscillations of wing membranes (as in
escapement). Rather the insect must maintain a wing velocity in relation to
file tooth density, independent of the radiator, to achieve the pure tone. In
other words, for a katydid to generate a pure-tone carrier, the wing (or the
scraper) must either pass at constant velocity over uniformly spaced teeth, or
the scraper must change velocity to offset changing tooth density: the time
taken for the scraper to travel from one tooth to the next must be made
constant (Montealegre-Z and Mason,
2005; Prestwich and
O'Sullivan, 2005).
Several species of crickets studied to date, in addition to some katydids
that use pure-tone sounds, have files whose tooth densities gradually decrease
basad. These increments in intertooth distances combine with increments in the
relative velocity of the closing tegmina, to yield a carrier dominated by one
frequency (Montealegre-Z and Mason,
2005; Prestwich and
O'Sullivan, 2005). Here we present data, from katydids producing
such (tonal) calls at extremely high frequencies, indicating that the speed of
wing movement alone cannot account for the tooth impact rate. Our data suggest
a novel stridulatory mechanism in which tooth impact rate is uncoupled from
the wing speed, to allow the production of high-frequency sound by brief
intermittent bursts of high-speed scraper movement.
Scraper flexibility and velocity
The scraper of crickets and katydids is a flexible structure
(Bennet-Clark and Bailey, 2002;
Bennet-Clark, 2003;
Montealegre-Z and Mason, 2005;
Prestwich and O'Sullivan,
2005). During its catch and release from each file tooth, it
experiences minor changes in speed
(Prestwich and O'Sullivan,
2005), suggesting a brief bending then spring-back, moving
relative to the rest of the wing. Hence, depending on the compliance and
length of the scraper flexible area (see below), the scraper may move with
velocities different from that of the tegmina (the scraper's driving force).
The work described here concerns katydids that have evolved very high carrier
frequencies whose scraper appears to have been elaborated for greater
flexibility. In a manner comparable to the stick and slip mechanism of spiny
lobsters (Patek, 2001), where
packets of energy are stored by elastic tissue during a stick phase and later
released to contribute to the sound production of a slip phase, we propose
that the bending of the flexible scrapers of these katydid species store
energy that, upon release, propels the scraper with elevated velocity across
file teeth.
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Materials and methods |
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A number of other species were chosen for study, all also exhibiting tonal carrier frequencies. They are intended to represent a wide range of carrier frequencies from the low audio to the high ultrasonic. Their localities and critical features of their stridulation are listed in Table 1. Some were chosen because of the availability of data on song structure, wing closing velocities, tooth density, etc. A few, Phlugis from the Amazon basin of Colombia and an unnamed species of the pseudophylline Myopophyllum from Ecuador, were available as live specimens for high-speed video analysis. Some species were also selected for either their known high ultrasonic carriers or their known low-frequency carriers.
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The unavoidably small sample of Arachnoscelis n. sp. may raise
concern about how typical our measures are of the generating mechanism of this
species. Observations of the generation features of Arachnoscelis n.
sp. recur in the comparative analysis of other species (e.g.
Myopophyllum n. sp.), and our two specimens match each other closely
in their stridulatory behaviour, especially in physical song features relevant
to the hypothesis of scraper-based energy, e.g. mean pulse period for one is
2.42 ms (N=9 calls) and for the other 2.00 ms (N=19 calls).
Confidence is also increased where, in the absence of living specimens,
similar patterns of stridulation show compatible parameters of wing movement
(see Results); also by the fact that the measurements of the sound generator
of both male individuals fit the curve of fc vs
mirror dimension at 
130 kHz
(Montealegre-Z, 2005).
Recordings of sound and wing motion
Sound recordings
The extreme ultrasonic nature of the calls of Arachnoscelis n. sp.
were discovered at night in a hotel room in Cali Colombia, using a hetrodyning
bat detector (U30, Ultra Sound Advice, Wimbledon, London, UK) on the caged
insect. This (1996) specimen was later lab-recorded in Canada, free field,
with a 1/8'' Brüel & Kjær (B&K, Naerum, Denmark)
condenser microphone (type 4138), clamped and directed vertically; microphone
output went to a B&K 2606 amplifier, thence to a Racal (Store-4DS)
instrumentation tape recorder (60'' s-1). Recordings, slowed
8x, were transferred to a computer via a PCMCIA digitizing card
(Ines i616) sampling at 200 kilosamples s-1, high-pass filtered at
2 kHz. A power spectral density Fast Fourier Transform (FFT) obtained with
Matlab (The Mathworks, Natick, MA, USA), was smoothed (Welch) and expressed in
dB, relative to its most intense frequency peak.
For other species where acoustic recordings were available, the methods of
recording and sound analysis are found in the respective literature:
Myopophyllum speciosum, Haenschiella spp. and Drepanoxiphus
(Morris et al., 1994);
Championica walkeri and Eubliastes chlorodictyon
(Montealegre-Z and Morris,
1999); Copiphora rhinoceros
(Morris, 1980);
Panacanthus spp. (Montealegre-Z.
and Morris, 2004;
Montealegre-Z and Mason,
2005); Uchuca haltikos
(Montealegre-Z and Morris,
2003).
The remainder of mentioned species (Metrioptera sphagnorum, Myopophyllum n. sp., Copiphora gracilis and C. cf gracilis, E. aethiops, `nr Loboscelis spp.' and Phlugis sp.) were recorded by the following procedure: the output of a 1/4'' microphone (B&K 4135) on a (B&K 2204) sound level meter was digitized (Tucker Davis, System II, Gainesville FL, USA) at 100 or 170 kilosamples s-1. Analysis of acoustic data utilized DADISP 4.1 (DSP Development Corp., Newton, MA, USA) or Matlab software. The calling songs used in all these analyses were recorded in a sound-attenuating room at the University of Toronto (UT) at Mississauga; the average temperature of this room was 23.5°C.
Zero-crossing analysis
Songs were analysed with the Zero-crossing (ZC) module for Canary software
(Laboratory of Ornithology, Cornell University). Zero-crossing (version 5) is
freely available from Dr K. N. Prestwich
(http://www.holycross.edu/departments/biology/kprestwi/ZC).
Zero-crossing v.5 calculates the instantaneous frequency on a cycle-to-cycle
basis. The software module starts counting waves at the first point in the
record where the microphone voltage or sound pressure crosses zero. Two such
crossings later is the start of the second cycle, and so on. Thus, the time
separating three ZC events corresponds to the wave period (P). Since
one cycle has two ZC events, the program calculates P for both half
cycles and then an average P of the wave is calculated; therefore,
1/P is the average frequency of this wave. The ZC program then starts
with the first zero-crossing event of the next cycle and continues its
calculation process until the frequency of each wave has been measured. These
features make the program appropriate for analyzing pure-tone signals
(Bennet-Clark and Bailey, 2002;
Bennet-Clark 2003;
Prestwich and O'Sullivan,
2005). Other details of ZC analysis are provided in the ZC v.5
user's manual, from which the above description of the program's capabilities
has been taken.
Wing motion
Recordings of wing movements were made using high-speed video (HSV)
(Redlake Motionscope PCI1000s, San Diego, CA, USA). This system was
synchronized with a computer data acquisition board (National Instruments
BNC-2110, Austin, TX, USA; 16 bit) using MIDAS software (version 2.0 Xcitex
Inc., Cambridge, MA, USA) for simultaneous recording of sound production.
Recordings were acquired at 1000 frames s-1, and acoustic data
sampled at rates of 200 or 300 kilosamples s-1. Insects were free
on a wooden perch, the camera focused on either the stridulatory field or on
the file and scraper (from posterior aspect). A microphone (B&K), directed
at a specimen for sound recording, 1/8'' (4138) or 1/4'' (4939), fed
either a B&K 2606 amplifier or B&K Nexus (Type 2690). Video recordings
were analysed frame-by-frame, using MIDAS software. From these recordings we
measured the closing wing velocity (CWV) and estimated the length of
file traversed by the scraper during sound production. Only the 2003 specimen
of Arachnoscelis n. sp. was examined by HSV.
Stridulatory file and scraper
Files were sputter-coated with gold and viewed on a Hitachi Scanning
Electronic Microscope at the Department of Zoology, UT. Measurements of file
dimensions were obtained from digitized SEM photographs using the dimension
tool of the drawing program Corel Draw (ver. 11, Corel Inc., Ottowa, ON,
Canada). Inter-tooth distances were measured from the tip of one tooth to the
tip of the next (see Montealegre-Z and
Mason, 2005) and tooth density (TD) was calculated as the number
of teeth divided by the length of the functional region of the file.
The functional scraper of tettigoniids is an acute upturned carina situated
at "the hind margin of the right fore wing"
(Ragge, 1955), shaped to
insert between the file teeth of the left wing. This carina sits at the
extreme margin of the region, posterior to the radial and cubital veins,
modified in males for sound generation. Vein homologies are unclear
(Jost and Shaw, 2006), but the
first vein encountered behind the scraper, has been termed here the third
Anal, following Desutter-Grandcolas
(Desutter-Grandcolas, 2003)
(see Results) and the cuticular region in between (from scraper to A3), is
referred to here for convenience as the `scraper shelf' to suggest its rather
low mass as a projection relative to the sclerotized and thickened third Anal
vein to which it attaches.
This scraper shelf region was examined for at least one specimen of each of
the species listed in Table 1
using both microtome sectioning and electron microscopy. For the microtome,
parts of the tegmina were dissected and then embedded in Spur's solution.
Transverse sections were treated with dibasic staining
(Di Sant' Agnese and De Mesy Jensen,
1984). Samples were mounted on slides, observed and then measured
under a light transmission microscope. For scanning electron microscopic
examination, the right tegmen of a fresh or liquid-preserved specimen was
sectioned across the scraper with a razor blade as indicated
(Montealegre-Z and Mason,
2005) and prepared as above.
Wing and scraper velocities
Strain is created between scraper and file teeth by opposing
muscle-generated shear forces (Josephson,
1985). During wing closure the scraper should move at velocities
comparable to those of the wing, experiencing minor deceleration and
acceleration each time a tooth is contacted and/or the scraper released. This
condition is common in species with relatively short scrapers, which permit
the teeth to be contacted in sequence
(Montealegre-Z, 2005).
However, in species where the scraper's width (see Results) and flexibility is
greater, it may move at velocities higher or lower than that of the wing. We
therefore distinguish scraper velocity (SV) from CWV, and
argue below that for katydid species producing pure tones and extreme
ultrasonic frequencies, a modified form of stridulation occurs in which
scraper and wing velocities are intermittently uncoupled (in contrast to the
escapement model). Our hypothesis predicts that SV should be higher
than CWV during sound production in species using extreme ultrasonic
frequencies.
Given tuned wings and continuous contact between file and scraper (basic
assumptions of an escapement mechanism), the oscillation period of radiated
sound corresponds exactly to the time the scraper spends between two teeth. If
inter-tooth distances are known, one can estimate the scraper's instantaneous
speed (the speed required for the scraper to travel between two teeth). We
determined the time spent by the scraper travelling between two teeth
(=P) using zero-crossing (ZC) analysis of recorded songs
(Montealegre-Z, 2005), as the
inverse of the instantaneous song frequency (see details above). These time
values (oscillation periods) are converted to instantaneous scraper velocities
by dividing by the inter-tooth distance for every pair of teeth. Instantaneous
SV can be averaged over the entire song to give a measure that allows
comparison with CWV. ZC analysis can also be used to relate events
associated with scraper behaviour to the waveform
(Prestwich and O'Sullivan,
2005).
We measured CWV from HSV recordings (observed CWV) and compared it with average scraper velocities estimated as described above. This procedure was conducted in those species for which measurements of CWV (based on HSV) were available: P. pallicornis, P. cuspidatus, C. walkeri, Co. cf. gracilis, E. aethiops, M. sphagnorum, `nr Loboscelis spp.', U. haltikos, Myopophyllum n. sp., and Arachnoscelis n. sp. (only the 2003 specimen) (see Table 1).
To evaluate the mechanism of stridulation we compared the frequency of produced sound with the tooth-strike rate (TSR) of the scraper. In a conventional (escapement) stridulatory mechanism, the TSR matches the sound frequency and will be determined by the product of CWV and the number of teeth per unit distance of file (TD). Also, average SV and CWV should be similar and the TSR calculated using either of these should yield similar values that match the sound frequency, fc.
A discrepancy between CWV and average SV may arise if
wing movement during stridulation is discontinuous, as is known to be the case
in many katydids producing nonresonant songs
(Heller, 1988;
Heller and von Helversen,
1993). In this case CWV would be underestimated as the
measured wingstroke duration would include pauses in wing movement.
Alternatively, a difference in CWV and average SV could
arise due to movement of the scraper relative to the wing, such that with
continuous wing movement the scraper alternately bends, while remaining
stationary as the wing moves, then releases to travel over a succession of
file teeth at elevated velocity relative to the wing
(Morris and Pipher, 1972). In
this case, SV being calculated on the periods of successive cycles of
sound production (excluding silent intervals), it would yield a higher value
than CWV.
The songs of all (known) katydid species producing pure tones at high ultrasonic frequencies consist of trains of several pulses produced on a single wing stroke, but with the pulses very short and set apart from each other, typically by silent intervals much longer than the pulses themselves (see below). (For convenience these are referred to here as SSTP: short spaced tonal pulses.) Therefore, to analyse the relationship between TD, CWV, SV and fc, we must (1) distinguish between continuous and discontinuous wing movement and (2) identify in song recordings which cycles of radiated sound correspond to tooth engagements rather than to free oscillation of sound radiating structures. Determining the nature of wing movement (1) will provide the correct time value for calculating wing velocity. Identifying driven oscillations in the recorded sound (2) will indicate the number of file teeth involved in sound production.
Identification of driven oscillations
For trains of pulses, we estimated how many teeth of the file are used (to
make driven oscillations), by summing all the waves (rising and sustained) of
all the pulses in a train. Oscillations, coinciding with the rising and
sustained part of each wave train, are produced when the scraper is driven
along the file to generate radiator oscillations. Free decay follows the
driven portion of the waveform and might occur with both structures still in
contact, or as both structures experience total disengagement
(Bennet-Clark and Bailey, 2002;
Prestwich and O'Sullivan,
2005). Incrementing and sustained regions were determined, based
on ZC analysis of each pulse. For driven oscillations, the instantaneous
frequency should be more or less constant, but when the scraper springs ahead
from its maximum deflection, or stops, a sudden change in the instantaneous
frequency is expected. Oscillations occurring after this change should form
part of the free decay (Montealegre-Z,
2005; Prestwich and
O'Sullivan, 2005).
A method for estimating CWV in the absence of living specimens
For some species of interest, living specimens were unavailable for HSV
recordings (Co. rhinoceros, Co. gracilis, E. chlorodyction,
Haenschiella spp., Drepanoxiphus sp., M. speciosum, see
Table 1). Unable to obtain
direct measurements of their CWV, we derived an estimate of overall
wing speed (estimated CWV, Table
1) under the assumptions of a conventional escapement mechanism as
follows. The duration of sound production in a single wing stroke defined the
total time of wing movement. For a one-to-one correspondence between radiated
sound waves and tooth engagements by the scraper, the total number of driven
oscillations produced on a single wing stroke [that is, the number of sound
waves excluding the free decay at the end of within-closure pulses or of the
song (Montealegre-Z, 2005;
Prestwich and O'Sullivan,
2005)] is equivalent to the number of file teeth involved. Using
anatomical data from preserved specimens to obtain the distance represented by
this number of file teeth, we estimated CWV as this distance divided
by the duration of sound production.
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For the 19 species we analysed data on CWV and song frequency
(fc) by cluster analysis, using partitioning around
medoids (PAM) (Kaufman and Rousseeuw,
1990; Struyf et al.,
1997). We analysed the relationship between song frequency and
closing wing velocity by ANCOVA with wing velocity as a continuous variable
and group membership (high vs low frequency) as a categorical
variable. In addition, a similar analysis was performed using the product of
file tooth density and wing speed (=average TSR) as the continuous
variable. The purpose of this analysis was not to address questions on the
evolution of stridulatory mechanisms. Our goal, rather, was to identify
species in which the relationship between wing velocity and sound frequency is
inconsistent with a sustained-pulse mechanism. All statistical analyses were
done using R software (v2.0.1,
www.r-project.org).
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). The forewings are quite reduced and used only for calling
(Fig. 1A,
Fig. 2); brachyptery is
characteristic of the genus Arachnoscelis
(Nickle, 2002).
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Peak amplitudes achieved in early pulses increment, diminishing in later ones (Fig. 1B), and in mid-train a number of pulses in succession may peak uniformly. Each pulse lasts about 120 µs (Fig. 1C); pulse period was 2.42 ms for the 1996 specimen, 2.00 ms for the 2003 specimen. There are about 7 waves in each pulse (driven oscillations) before decay begins. Pulses recur at an average rate of 588 s-1. Output energy in the 1996 specimen was centred at 122.9 kHz, and for the 2003 specimen it was 128.6 kHz (Fig. 1D). There was no energy below 100 kHz in the spectrum of either specimen.
As determined using ZC analysis (Fig.
1E) for Arachnoscelis n. sp., near pulse onset there was
a slight increment in the instantaneous frequency coincident with the first
few waves. Instantaneous frequency then decreases as the pulse progresses
until it jumps up rapidly again as (presumably) scraper disengagement occurs
(Prestwich and O'Sullivan,
2005).
Songs of the 2003 specimen, recorded by HSV, gave a CWV of 12.8 mm s-1. This is an average velocity over the whole closing interval; one that assumes continuous wing movement. The frame rate of the HSV (1 frame ms-1) is too slow relative to the duration of the sound pulses (120 µs) to reveal wing behaviour during pulses, but the silent interpulse intervals (2.15 ms and 1.83 ms, means for 1996 and 2003 specimens, respectively) were long enough to allow detection of wing movement in these intervals. Comparing wing velocities measured between successive frames, those intervals that included sound outputs gave a lower CWV (Fig. 2); only intervals without pulse production (silent intervals) over the course of a single wing stroke, gave maximal wing velocities. These results suggest that wing displacement in this species only occurs when pulses are not being generated. In some cases, sound pulses occurred with no detectable displacement of the tegmina (Fig. 2B).
The file of Arachnoscelis n. sp. bears approximately 70 teeth
within a 0.70 mm length a TD=100 teeth mm-1
(Table 1,
Fig. 3). The total distance
moved by the scraper along the file during a single wingstroke was 0.35-0.40
mm (for the 2003 specimen), but there is evidence that the complete file might
also be used for sound production, allowing longer pulse trains (see below).
If this insect used a grylloid escapement mechanism, i.e. with a 1:1
relationship between tegminal oscillator and tooth contact rate, then to
produce a 129 kHz sound pulse, the scraper would have had to contact teeth at
the rate of 129 000 s-1 at a velocity of 1161 mm
s-1 (see Table 1 for
tooth spacing, TS). But in fact the HSV-measured (overall) CWV,
however, was only 12.8 mm s-1. If the scraper and right tegmen
moved as a single unit (i.e. no relative movement of scraper and
SV=CWV), this is an order of magnitude slower than the
necessary SV to meet teeth at a rate of 129 000 s-1. In
one specimen of Arachnoscelis n. sp. the total number of driven
oscillations in the song was nearly equal to the number of file teeth (64
waves vs 67 file teeth). In songs from the specimen recorded with
HSV, the scraper of Arachnoscelis n. sp. contacted no more than 35-40
teeth, all in the basal half of the file (Figs
2,
3).
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Stridulation by a single specimen of Phlugis sp. was analysed by
HSV. Each of this specimen's calls was composed of a train of just two
discrete pulses (Montealegre-Z,
2005). A pattern of forewing movement was observed very like that
of Arachnoscelis n. sp. To generate its 48-kHz pulses on the basis of
a driven resonant mechanism would require a tooth contact rate of 48 000
s-1, but by the measured CWV the rate of tooth contact
would be 4140 s-1 (Table
1). There was an obvious acceleration of this insect's wings,
increasing CWV to 40 mm s-1 before the first pulse
was produced. During the production of the first pulse, CWV decreased
dramatically to almost zero, then there was a short wing displacement
elevating CWV to 52 mm s-1 in the next (silent) interval.
The second pulse was produced and CWV decreased again to almost zero.
It is possible that during the production of a pulse in both
Arachnoscelis n. sp. and Phlugis n. sp. a short displacement
of the wing occurs, but due to the small size of specimens and resolution of
our HSV system, these were imperceptible.
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22 kHz. Calls of this pseudophylline involve 11-12 regularly repeated
sinusoidal pulses at each tegminal closure. CWV measured for the
frame interval just before the fourth pulse of the train was 129.3 mm
s-1, increasing in the subsequent frame, which incorporates the
third pulse, to 166.1 mm s-1
(Fig. 5); the same relative
velocity changes are shown occurring in conjunction with the last pulse of the
train. Just as with Myopophyllum n. sp., E. aethiops shows
an increased speed of tegminal movement as there is an emission of each pulse
and a depressed speed when no pulse is involved in the pair of frames that
form the basis of a velocity measure.
During a closure, the average velocity of the wing of E. aethiops
is 151 mm s-1 (Table
1). If this velocity were maintained throughout closure, given the
insect's observed tooth density, a carrier would be produced of 7701 Hz,
only about one-third the 22 000 Hz carrier observed. The observed carrier
can be achieved only by a scraper velocity of about 440 mm s-1,
occurring within each of the pulses to augment the lower speed of the
wing.
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), but in no instance did the number of driven oscillations
exceed the number of available teeth.
Cluster analysis
Cluster analysis assigned each species to one of two groups based on the
relationship between CWV and fc. The procedure
generated two groups, corresponding to species with song frequencies above and
below roughly 35 kHz. ANCOVA analysis with frequency group as categorical and
CWV as continuous variables showed significant effects of both group
membership and CWV, as well as a significant interaction
(Fig. 8A). In the low-frequency
group there was a significant positive relationship between song frequency and
CWV (F=13.8, P=0.005), whereas in the
high-frequency group, CWV decreased with increasing song frequency,
though this relationship was not significant (F=1.55,
P=0.259).
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Because TSR depends on both CWV and tooth spacing (density), we also repeated the ANCOVA using the product of CWV and TD as the continuous variable. Overall results were similar to the previous analysis, with significant main effects and interaction (Fig. 8B). In this analysis, however, linear regression of song frequency with average TSR was significant in both groups, with a slope of unity for the low-frequency group (F=39.36, P<<0.001) consistent with the conventional model of resonant stridulation. In the high-frequency group, average TSR (product of CWV and TD) decreased steeply with increasing song frequency (F=9.81, P=0.02).
Consideration of their CWV, TD and fc indicates that for all eight species in the high frequency group (all species exhibiting SSTP), a 1:1 relationship between tegminal oscillator and tooth-contact rate, the relationship essential for an sustained pure tone pulse, is not achievable with the observed or estimated closing wing velocity (Table 1, Fig. 8). All these species are closing their wings at speeds far below that necessary to account for the SV inherent in their high frequency carriers. To account for the high carrier and its short wavelength on a tooth per wave basis requires some other mechanism. We believe the likely basis, one consistent with the SSTP form of all these calls, involves a special mechanical contribution from the scraper.
Comparisons of scraper morphology
Certain morphological characteristics are peculiar to the scrapers of
species in the high frequency group. Males producing these extremely high
carriers with relatively low CWVs had a more extensively developed
region of thin cuticle (`scraper shelf') between the scraper proper and the
third anal vein. The vein itself was greatly thickened and relatively more
massive than in species of the lower frequency group.
Scraper sections for Panacanthus pallicornis and nr Loboscelis sp. 1 are illustrated (Fig. 9A); they show a lesser development of their scraper shelf area, suggesting a lesser deformability of the scraper shelf relative to that of the two high frequency group species (Fig. 9B). For both Arachnoscelis n. sp. and Myopophyllum n. sp. transverse sections of the scraper shelf (Fig. 9B) show this region to be extremely thin and much more extensive, appearing to constitute a highly deformable region.
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Discussion |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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). These
observations lead us to propose a role for `uncoupled' scraper behaviour and
elasticity to achieve high ultrasonic rates of pure-tone generation: the
proposed mechanism is illustrated in Fig.
10 for Arachnoscelis sp. n. [That elastic energy residing
in the scraper might contribute to stridulation was first suggested
(Morris and Pipher, 1972) to
explain ultrasonic pure-tone pulses made by the katydid Metrioptera
sphagnorum in its ultrasonic mode.]
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This interpretation of how Arachnoscelis n. sp. sings is supported
by observed variation in the instantaneous frequency of its single pulses
(Fig. 1E). During the pulse
onset, there is an increment in the instantaneous frequency for the first few
waves (Fig. 1E), which suggests
a higher velocity of the scraper at its release. Instantaneous frequency
decreases as the pulse progresses and the scraper loses velocity. If the total
number of driven oscillations involved in one closing stroke are added, one
obtains a number of cycles represented in individual tooth contacts. The
region of the file actually used holds 40 teeth (specimen 2003); thus
teeth are likely not skipped and all teeth over the functional file region are
struck by the successive movements of the scraper. But this technique might
vary and perhaps few teeth might be skipped when the wing moves during the
silent interval.
Applying a lock-step (coupled) view of wing and scraper movement to the mechanism involved in SSTP singers, the wing (and the scraper) must stop, and remain so over the silent interpulse interval. Sound can only occur when there is wing displacement. Our HSV analyses of Arachnoscelis n. sp. show changes in wing position in two successive frames within a silent interval in the song: so something other than wing movement must be responsible for the generated sound, the scraper being the only feasible candidate.
In a decoupled view, for SSTP species the scraper would move, `atop' the wing movement, to make each pulse of the train. The bending scraper should also have an effect on the general closing velocity of the wing: during the interval when it is lodged and bending, storing deformation energy, it should cause the wing velocity to drop. Then during the emission of the pulse, when the scraper pushes ahead along the file at a velocity (necessary to achieve the high tooth contact rate of the ultrasonic carrier) higher than that of the overall wing movement, the scraper should contribute to an increase in wing velocity.
A decoupled mechanism predicts that for species where the wing moves continuously during closure, its velocity, established by two consecutive frames in advance of a pulse, should decline (the wings being slowed by having to bend the scraper) and then increase between two frames that bracket (include) the making of a pulse (because some of the deformation energy is given back to the wing speed). Exactly these velocity changes are shown in Fig. 4 (Myopophyllum n. sp.): 94.9 mm s-1 at a point just before a pulse begins, increases to 141.7 as the pulse is over, that is, the velocity of the wing is increased coincident with the making of the pulse; 141.7 then drops to 81.7 mm s-1 during the time taken to make the next frame that includes no sound, that is, the velocity of the wing decreases under the effect of bending the scraper lobe. A similar mechanism is used by E. aethiops (Fig. 5).
Though consistent with the decoupling of the scraper and wing these arguments about velocity do not apply in the same way to Arachnoscelis n. sp. In this species the HVR indicates the wings are brought to a complete halt, not just a slowing, after storing the energy for the 129 kHz pulse. In fact it is possible that at these slow speeds the insect triggers the dislodgement of the scraper as an independent motor act by slightly changing the shear forces between the wings that are keeping the scraper bent.
Stridulation in other high frequency SSTP singers
In our comparison of the songs of 19 species of katydids, the ANCOVA
separates out a group of very high carrier frequency singers, all making
forewing closures by SSTP and all showing very low tegminal closing
velocities.
Males of the first 12 species listed in
Table 1 sing in the range of
5-45 kHz and exhibit CWV of 120-300 mm s-1 (excluding
M. sphagnorum and E. aethiops, see below). Among these
species, CWV and SV are equal and the scraper makes an
uninterrupted passage along the file, contacting consecutive teeth in a long
series. For the remaining seven species, carriers range upward from 48
(Phlugis) to 129 kHz (Arachnoscelis n. sp.) but closing wing
velocity is lower, in some cases dramatically: 13-140 mm s-1. In
these latter species, CWV no longer equates to SV. Lower
CWV is least in evidence in the two species of Myopophyllum,
probably because these two largest species have more muscular mass, allowing
them to achieve higher velocities.
The seven high-frequency species of Table 1 share the production of a train of relatively short sound pulses, corresponding to a single closing file-run. As explained above, this pulse train is likely the signature of scraper-stored elastic energy. The scraper is apparently making a series of tooth lodgements along the file, each associated with scraper bending, and a succession of increased scraper velocities is achieved over very short durations. The work done by the scraper during each pulse occurs in a shorter time than could be managed by wing muscle alone and so will be at a higher power. In these species, scraper movement by wing muscle contraction is no longer the limiting determinant of scraper kinetic energy. The additional elastic energy brings us up to the necessary tooth-impact rates for the high ultrasonic frequencies. Slower overall closing wing velocities can maximise SV and so the distances travelled by the scraper for each elastic energy input, thus making lengthened pulses.
The occurrence of trains of pulses within single wing closures is not
limited to these extreme high-frequency singers. Some species, e.g.
Metrioptera sphagnorum and E. aethiops, present cases where
elastic energy and low CWV are used to generate moderately high
pure-tone ultrasonic frequencies. Shorter transient pulses can also be
produced during wing closures, e.g. Cocconotini (Monteleagre-Z and Morris,
1999). Other species with nonresonant, broadband spectra, e.g. Pterophylla
camellifolia (Montealegre-Z and
Morris, 1999), stridulate with a scraper-file mechanism differing
from the one presented here, but also yielding pulse trains of short,
rapid-decay, transient pulses).
The distinctive post-scraper morphology of the high frequency species group
might help to predict SSTP structure for species with unknown songs. It is
also possible that this region will prove to be specialized in terms of its
elastic properties. For example, that it might incorporate resilin
(Andersen and Weis-Fogh, 1964;
Neff et al., 2000;
Vincent and Wegst, 2004;
Elvin et al., 2005). This
needs to be examined in future work.
Selective forces for extreme ultrasonics
The song of Arachnoscelis n. sp. is the highest pure-tone call
carrier presently known, surpassing the previous highest, that of another
katydid, Haenschiella spp., at 106 kHz
(Morris et al., 1994).
[Another extreme carrier, but not a pure tone, is that of the pyralid moth
Corcyra cephalonica: the dominant peak in the moth's broad-band
spectrum is 125 kHz (Spangler,
1987).]
What selective forces might have favoured the evolution of these very
high-frequency generators? Because ultrasonics lose energy more rapidly with
distance, especially in humid air
(Griffin, 1971;
Römer and Lewald, 1992;
Römer, 1993), it seems
questionable they would aid in enticing distant females. Using such
frequencies a caller limits his reach and (possibly) increases his cost. Two
other hypotheses seem more plausible. (1) Enhanced directionality. At such
short wavelengths body diffraction (normally not of importance) may become
significant even for a very small insect and so enhance close-range
localization mechanisms. For instance, the wavelength of the
Arachnoscelis n. sp. song is 2.7 mm, while this insect's body
diameter is 3.5 mm; this disparity is sufficient to cause scattering of
sound by body diffraction (Mason et al.,
1991; Morris et al.,
1994; Mason and Bailey,
1998). (2) Eavesdropping avoidance. The heightened attenuation of
these frequencies may in itself be adaptive in confining male to female
transmission to a more intimate range, avoiding the attention of
ultrasound-detecting insectivorous bats
(Belwood and Morris, 1987;
Belwood, 1990).
The extreme short wavelengths of these tropical katydids might also be an
adaptation to improve radiation efficiency. Sound radiation efficiency is
nearly zero at very low frequencies, when the wavelength is long compared with
radiator diameter, rises to a maximum when the sound wavelength is comparable
with the diameter, and then declines again more slowly
(Fletcher, 1992). In practice
the radiation resistance of a dipole acoustic source in a baffle increases to
that of the surrounding air as the source radius rises to 1/4 wavelength
(Fletcher, 1992;
Bennet-Clark, 1998). The
quarter wavelengths involved here approximate the diameters of their radiators
(Montealegre-Z, 2005). A
benefit of evolving in this fashion may have been improved sound radiation
through reduced short-circuiting and better coupling of the impedance of the
mirror membranes to the surrounding air mass
(Bennet-Clark, 1989;
Bennet-Clark, 1998).
Conclusion
In evolving to a higher carrier, some tettigoniid species have increased
either TD or CWV, or both, while still contacting one tooth per sound
radiating cycle (Montealegre-Z,
2005). In these species, SV and CWV remain
equivalent as the scraper moves exactly in tandem with the wing. A few other
species have to some degree separated SV from CWV and
incorporated elastic energy into the generating process. Measuring
CWV, file morphology and instantaneous frequency of pulse
oscillations allows one to distinguish between these two species groups and to
make predictions about the stridulatory mechanism a katydid, cricket or grig
is using.
The rate at which an animal can do work (apply force through a distance) is
normally limited by how fast muscles can contract. But deformed cuticle can
return the work that went into its deformation much faster than a working
muscle. Elastic energy is used by some arthropods to achieve powerful movement
in this way. So for example, in the jump of a leafhopper or flea
(Bennet-Clark and Lucey, 1967;
Burrows, 2003;
Krasnov et al., 2004),
deformed cuticle provides power. In Arachnoscelis n. sp. and other
species using extreme ultrasonic means, the paradox of high-frequency output
by low-velocity wing movement can be resolved by invoking a mechanism that
utilizes the power capability of elastic energy stored in cuticle.
)
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Acknowledgments |
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