What determines the tuning of hearing organs and the frequency of calls? A comparative study in the katydid genus Neoconocephalus (Orthoptera, Tettigoniidae)
Division of Biological Sciences, University of Missouri, 207 Tucker Hall, Columbia, MO 65211, USA
* Author for correspondence (e-mail: schulj{at}missouri.edu)
Accepted 10 October 2002
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Summary |
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Key words: Neoconocephalus, acoustic communication, frequency tuning, bushcricket, hearing threshold, call spectrum, sound transmission
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Introduction |
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Further causes of selection leading to a mismatch in the communication
system could arise in other behavioral contexts, such as predator avoidance.
Many organisms use their hearing organs to detect and avoid acoustically
hunting predators (e.g. bats; Moiseff et
al., 1978; Hoy,
1992
). Also, an organism's communication signals can be targeted
by acoustically orienting predators or parasitoids as a way to localize their
prey or hosts (e.g. Cade,
1975
). Thus, calls and hearing organs might be affected by
selection pressures from potentially conflicting forces. Selection on the
communication system can also be caused by environmental factors. Signal
degradation occurs in most cases during the passage of the signal through the
environment. Masking noise may originate from the environment itself (e.g.
moving water) or be produced by other noisy animals. In addition to these
potential selection pressures, non-selective evolutionary forces (e.g.
mutation, genetic drift) might have a strong impact on the evolution of
communication systems. Furthermore, physical, morphological and physiological
constraints might limit the adaptive evolution of both call production and the
hearing system.
The description of mismatches between signal spectrum and tuning of the
hearing organ in one or a few species usually does not allow one to determine
which evolutionary forces contribute to this phenomenon. The influences of
predation, environment, etc. can usually be estimated at best, and the
interpretation of the signal/sensory system mismatch remains speculative (e.g.
Heller et al., 1997;
Bailey and Römer, 1991
). A
comparative approach that studies several species that are similar in some,
but different in other, potentially important factors for the evolution of the
communication system might allow one to single out the influence of individual
evolutionary forces.
In the present study, we focus on a group of five katydid species of the
genus Neoconocephalus (Orthoptera: Tettigoniidae) with largely
sympatric and synchronic occurrences
(Greenfield, 1990), which
differ significantly in the spectral composition of their calls. We compare
the response properties of the hearing organs (tuning and isointensity
responses) in these five species and quantify the influence of their grassland
habitat on signal propagation. Because of the similar morphologies and
lifestyles and the cohabitation of the five species, the influences of factors
other than communication itself (e.g. by environment or predators) on the
evolution of the communication system should be similar among these five
species.
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Materials and methods |
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Call recordings and analysis
Male calls were recorded in an anechoic chamber at an ambient temperature
of 25°C. The specimens were placed in small screen cages 15 cm in
diameter. A microphone was placed 20 cm dorsal of the calling male. Calls were
recorded with a '' free field microphone (40BF, G.R.A.S.,
Vedbaek, Denmark), amplified (G.R.A.S. 26 AC and 12 AA), high-pass filtered
(1000Hz, KH3202, Krohn Hite, Avon, MA, USA) and digitized using a custom-made
A/D-converter system (16-bit resolution, 250kHz sampling rate). This setup
provided a flat (±1 dB) frequency response in the range from 2kHz to
70kHz.
Amplitude spectra were calculated with a computer program (BatSound 1.0, Pettersson, Uppsala, Sweden) by fast Fourier transformation (FFT; Hamming window, frame length 1024) and averaged over a 1 s section of each call. The spectra of the calls of all species had a narrow-band low-frequency component and broad components of lower amplitude in the ultrasound range (Fig. 1A). In the spectra, we measured the frequency with the highest amplitude and the width of the low-frequency component at -3dB and -10dB amplitude. Q3dB and Q10dB values were calculated as the ratio of center frequency to bandwidth at -3dB and -10dB, respectively.
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Tympanal nerve recordings
The animals were anesthetized by brief exposure to CO2 and fixed
ventral side up on a free-standing metal holder with a waxresin
mixture. The forelegs were fixed on a wire holder, perpendicular to the body
axis, in a natural position. The cuticle covering the entrance of the tympanal
nerve into the prothoracic ganglion was removed, and exposed tissue was
covered with saline. A silver wire, inserted into the abdomen, served as the
indifferent electrode.
Experiments took place in an anechoic chamber (1.2mx1.2mx0.7m) at 24-26°C. Whole nerve recordings were obtained using electrolytically sharpened tungsten hook-electrodes (diameter 50-70µm) placed at the entrance of the tympanic nerve into the prothoracic ganglion. The recording site was covered with silicone-grease (Baysilone) in order to prevent drying of the nerve. The recorded signals were amplified using a custom-made amplifier, band-pass filtered (120-4000Hz, Krohn Hite 3342) and digitized (12-bit A/D converter, 10kHz sampling rate).
The stimuli were delivered via one loudspeaker (Technics 10TH400C)
located 70 cm from the preparation, perpendicular to the body axis of the
animal. The stimuli were generated using a computer and a 16-bit DA-converter
system (sampling rate 250kHz). The signals were amplified and their amplitude
manipulated by a computer-controlled attenuator in steps of 3dB. The
amplitudes of the signals were calibrated at the position of the insect using
a B&K 2231 sound level meter (Bruel and Kjaer, Naerum, Denmark) and a
'' free field microphone (G.R.A.S. 40BF). Sound measurements were
obtained on the preparation site with no animal present. Signal amplitudes are
given in dB peak SPL (re 2x10-1 Pa), which is, for sine
waves, 3dB above the respective root-mean-square (rms) value. At the recording
site, slight echoic influences were unavoidable, but these influences did not
alter the intensity or the envelope of the signals by more than
±1dB.
Thresholds were determined for sinusoids in the range of 4 kHz to 80 kHz (1 kHz steps from 4 kHz to 10 kHz; 2 kHz steps from 10 kHz to 20 kHz; 5 kHz steps from 20 kHz to 50 kHz; 10 kHz steps from 50 kHz to 80 kHz). Stimuli had a trapezoid-shaped envelope with a rise and fall time of 1 ms and a 10 ms plateau time. Each frequency was played back at 20 different amplitude attenuations in steps of 3 dB (total amplitude range 57 dB). The stimulus protocol included the playback of `no stimulus' (i.e. a digital stimulus consisting only of zeros) at the same attenuation settings as the other stimuli. These stimuli provided the baseline for the threshold determination and controlled for the noise generated by the amplifiers and the computer-controlled attenuator. Absolute stimulus amplitudes for each frequency were set so that the lowest amplitude tested was well below threshold. All stimulus combinations were presented 25 times: all frequency/amplitude combinations, including the `no stimulus', were presented once, and then the whole sequence was repeated 25 times. This procedure guaranteed almost simultaneous measurement of all stimulus combinations, thus excluding effects due to changes in recording quality. During each repeat of the stimulus sequence, each frequency was presented from low to high amplitudes, and the frequencies were sorted from low to high. A pause of 350 ms was kept between different amplitudes of the same frequency; between frequencies, a pause of 3500 ms was kept. Because the main purpose of these experiments was to determine the hearing thresholds, the non-random presentation of stimulus intensities should have no impact on the results, because the presentation at threshold level was preceded by below-threshold stimulation. Also, all frequencies were treated identically, so that possible influences of the preceding stimulation would affect all frequencies in the same way.
Analysis of neurophysiological data
The digitized recordings of 15-25 responses of each stimulus/amplitude
combination were averaged. We excluded stimulation cycles from the analysis
when amplitude disturbances (e.g. due to movements of the insect) occurred or
when the amplitude of the recordings diminished. Averaged responses well above
threshold resembled damped oscillations (see
Fig. 5A), the peak-to-peak
amplitude of which was measured for each stimulus combination.
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In order to determine the threshold for the different frequencies, we first calculated the mean and S.E.M. for the peak-to-peak amplitudes of the recordings obtained during the 20 presentations of `no-stimulus'. This mean, plus 2 S.E.M., was used as the threshold criterion. Then, an intensity/response function was constructed for each frequency using the measured amplitudes of the averaged responses. These functions were smoothed by calculating the gliding mean over three values. Starting at the lowest stimulus intensity, we searched the smoothed curve for the stimulus intensity in which the response amplitude increased above the threshold criterion determined from the `no-stimulus' recording. By linear interpolation of the steepness of the intensity/response function at this point, the threshold was determined to a resolution of 1 dB.
The intensity/response functions that were constructed for each frequency
were also used to compare the response magnitudes at certain levels above
threshold (+9 dB, +18 dB, +27 dB and +36 dB) between different frequencies.
Response magnitudes were measured as the peak-to-peak amplitude of the
averaged responses. This amplitude is mainly determined by the number of cells
responding and the level of synchronization
(Pollack and Faulkes, 1998;
Schul, 1999
). To compare the
level of synchronization among different stimuli, we measured the breadth of
the first peak in the averaged recording
(Pollack and Faulkes, 1998
;
see Fig. 5).
Sound transmission in the field
The attenuation of the sound frequencies from 5 kHz to 40 kHz during
transmission was measured through vegetation typical for the biotope of
Neoconocephalus. Measurements took place in Rock Bridge State Park in
Columbia, MO, USA. The field site was a grassland with tall stalks (2.0-2.5 m)
and a dense understory of grass blades (0.75-1.0 m). The vegetation was
uniform in the range of our experiment. Males of all five species studied were
heard calling at this site. Measurements were made during the calling season
of Neoconocephalus, in early September 2001 from 17:00 h to 21:00 h,
immediately before the calling activity of Neoconocephalus began.
Stimulus-playback was performed with the same setup and identical signals
as in the neurophysiological experiment detailed above. The loudspeaker was
placed at the upper edge of the understory at a height of 85 cm. We normally
found calling males at similar positions in the vegetation. The sound was
recorded at several distances from the stimulus (1 m, 2 m, 5 m, 10 m and 20m)
with a " free-field microphone (G.R.A.S. 40AG) placed at 1.5 m
height in the vegetation. The signals were also recorded at a distance of 17
cm without any vegetation between loudspeaker and microphone. During all
recordings, the microphone and loudspeaker were on axis to each other.
The recorded signals were amplified (G.R.A.S. 26AC and 12AA), high-pass filtered (1000 Hz, Krohn Hite 3202) and recorded with a Pioneer D-C88 DAT recorder (sampling rate 96 kHz, frequency response up to 40 kHz). We also recorded a calibration signal (94 dB SPL, 1000 Hz, Bruel & Kjaer 4231) with the same gain settings as the recordings for each frequency, to allow the comparison of absolute signal amplitudes among the recordings at different distances. The signals were later digitized (250 kHz sampling rate, 16-bit resolution) and 50 repeats of each frequency were averaged to improve the signal-to-noise ratio. The averaged recordings were then filtered with a digital band-pass filter (bandwidth 2 kHz, CoolEdit 2000, Syntrillum Software) that was centered around each stimulus frequency, to further eliminate noise from the stimuli. We then measured the rms amplitude for the 10 ms plateau of each stimulus recorded at the six distances.
For each frequency, we plotted attenuation vs distance and calculated the best-fit curve for attenuation using the formula: y=a*x+b*log(x)+c. In this function, the term b*log(x) represents the spherical attenuation, and the term a*x includes atmospheric attenuation and attenuation due to reflection, absorption and diffraction by the vegetation (`excess attenuation'). The best-fit functions, which for all frequencies had r2 values of above 0.9, were used for further analysis. Excess attenuation was calculated as the difference between the best-fit curves and the theoretical curve calculated for spherical attenuation alone (6 dB per double distance; see Fig. 7).
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Results |
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The low-frequency components of the five species have Q3 dB values between 4.5 and 6 and Q10 dB values of approximately 2.5 (Table 1). The low-frequency band of all species except N. robustus was fairly symmetrical around the peak amplitude. In N. robustus, a secondary peak was present in all individual call spectra (see Fig. 1C), which resulted in the asymmetrical position of the -10 dB band relative to the peak frequency.
Hearing thresholds
Hearing thresholds were determined independently for males and females of
all species. Fig. 3 shows the
mean threshold curves for males and females of the five
Neoconocephalus species. We found highest sensitivity for all five
species in the range from 16 kHz to 20 kHz, with absolute thresholds of
approximately 30 dB SPL. The absolute sensitivity was similar in all five
species, with a tendency for larger species to be more sensitive
(Table 1). There were no
significant differences between the threshold curves obtained in males and
females in any of the five species. There was a non-significant tendency for
females to be slightly more sensitive than their male counterparts, except for
N. robustus, where females were slightly less sensitive. This again
reflects differences in body size, with males of all species being smaller in
our sample than the females, except for N. robustus, where the males
were larger than the females. The shape and general tuning of males and
females were similar in all five species studied here (but see
Faure and Hoy, 2000b for
sex-specific differences in the tuning of an auditory interneuron in N.
ensiger). Therefore, for comparison of the tuning among the five species,
we pooled the data for males and females of each species.
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The relative spectral sensitivity of the five species is compared in Fig. 4. The tuning of the five species was similar, with highest sensitivities occurring in the range of 16-20 kHz. Threshold values remained low for frequencies down to 9 kHz. Below 9 kHz, the steepness of the roll-off of the threshold curve increased to 20-25 dB octave-1 in all species. For frequencies above 20 kHz, the roll-off was approximately 8-10 dB octave-1 in all species tested. The main difference among the hearing thresholds of the five species is the increase of thresholds from the best frequencies at 16-20 kHz down to 9 kHz. In N. robustus and N. bivocatus, the increase of threshold in this range is less than 3 dB, while in N. ensiger, the threshold at 9 kHz was 8 dB higher than at 18 kHz. N. nebrascensis and N. retusus were intermediate, with threshold increases of 5-6 dB between 18 kHz and 9 kHz.
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Comparing the tuning of the auditory thresholds with the dominant frequencies of the calls revealed a mismatch between calls and hearing in all five species. This was most apparent in N. robustus, where hearing sensitivity at the dominant call frequency (7 kHz) was 9 dB lower than at the best frequency of the threshold curve (18 kHz). In N. nebrascensis, sensitivity at the dominant call frequency (10 kHz) was 7 dB lower than at 18 kHz. In the other three species, the mismatch was less pronounced, with reduced sensitivity at their respective call frequency of 4-5 dB (N. retusus and N. ensiger) or 3 dB (N. bivocatus). Given the distinct differences in dominant call frequency among the five Neoconocephalus species, the tuning of hearing thresholds did not seem to reflect these differences in the calls.
Above-threshold responses
The averaged responses obtained from the tympanic nerve recordings
resembled damped oscillations (Fig.
5A). The response magnitudes, measured as peak-to-peak amplitudes
of the averaged recordings, increased with stimulus intensity. For stimulus
frequencies up to 30 kHz, this increase was linear up to 30 dB above
threshold; above this intensity, response magnitude began to saturate
(Fig. 5B). For higher stimulus
frequencies (40-70 kHz), the increase of response magnitude was similar to
that of lower frequencies up to 24 dB above threshold. At higher intensities,
the steepness of the intensity/response function for these high frequencies
increased and continued to rise at the higher rate up to the highest
intensities tested (Fig. 5B).
This increased steepness of high frequencies at high intensities could be
caused either by an increased number of neurons responding or by a higher
spike synchronization (Pollack and
Faulkes, 1998). To distinguish between these possibilities, we
measured the breadth of the first spike in the compound action potential
(Fig. 5C). The width did not
vary systematically over stimulus intensity at both 12 kHz and 50 kHz nor did
it differ significantly between high and low frequencies. This indicates that
spike synchronization remains constant over the intensity range tested.
To compare the intensity/response functions in the complete frequency range tested, in Fig. 6 we show iso-intensity responses (relative to threshold) for all five species. For stimulus intensities of 9 dB, 18 dB and 27 dB above threshold, the response magnitudes did not vary systematically with frequency, indicating similar intensity/response functions for the frequency range between 5 kHz and 80 kHz up to 27 dB above threshold. An additional increase of stimulus intensity to 36 dB above threshold revealed a strong, non-linear increase of response amplitudes for ultrasonic frequencies between 35 kHz and 70 kHz, while below 30 kHz, the response magnitudes increase at the same, or lower, rate than at lower stimulus intensities. We found the same general pattern of above-threshold response magnitudes in all five species tested (Fig. 6).
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Transmission in the field
We measured the attenuation during the transmission through a typical
biotope of Neoconocephalus for sinusoidal stimuli in the range of 5
kHz to 40 kHz. As expected (Keuper and
Kühne, 1983), the attenuation of high frequencies was much
more severe than for lower frequencies
(Fig. 7): at frequencies below
10 kHz, attenuation was only little more than spreading loss (-6 dB per double
distance), while at 40 kHz, the excess attenuation (i.e. attenuation
additional to the spreading loss) was more than 60 dB at 20 m distance. The
excess attenuation is plotted against frequency in
Fig. 8. In the range from 5 kHz
to 9 kHz, excess attenuation was hardly recognizable (below 4 dB at 20 m
distance) and did not increase with frequency. For frequencies above 9 kHz,
excess attenuation increased with increasing frequency
(Fig. 8). Thus, the grassland
vegetation of the Neoconocephalus biotope acted like a low-pass
filter by not significantly affecting frequencies below 10 kHz but
increasingly dampening higher frequencies. This is in contrast to measurements
in habitats with shrubs and trees, where excess attenuation increases linearly
with frequency from at least 5 kHz to 40 kHz
(Römer and Lewald,
1992
).
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`Effectiveness' of frequencies for communication
The effectiveness of a signal frequency during communication, i.e. how
effectively the signal stimulates the receiver's sensory system, is determined
by the sensitivity of the receiver and the transmission properties of the
biotope. We calculated the theoretical effectiveness of call frequencies in
the range of 6-18 kHz, assuming that calls were produced with an amplitude of
110 dB SPL at 20 cm distance, which is approximately the amplitude of male
calls of the five species (U. Büttner and J. Schul, unpublished
observations). Using the hearing thresholds
(Fig. 3) and the transmission
functions through the biotope (Figs
7,
8), we calculated the amplitude
at which a female would perceive the call (i.e. its amplitude above the
hearing threshold) over distance. At 18 kHz (the frequency of highest hearing
sensitivity), this perceived amplitude is high at short distances but declines
rapidly as the distance increases (Fig.
9). The perceived amplitude of lower frequencies (e.g. 9 kHz;
Fig. 9) is lower at short
distances because of higher hearing thresholds. But the decline of perceived
amplitude of lower frequencies (e.g. 9 kHz;
Fig. 9) with increasing
distance is less steep than at 18 kHz because of the lower excess attenuation.
The two amplitude functions cross at a `break-even' distance (arrow in
Fig. 9): at shorter distances,
the higher frequency is perceived as louder by the female; at longer
distances, the lower frequency has a higher perceived amplitude.
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Accordingly, we calculated the break-even distances for frequencies between 7 kHz and 14 kHz, relative to an 18 kHz signal, for all five species (Fig. 10). For all five species, this distance was short in the range from 9 kHz to 14 kHz: for N. robustus and N. bivocatus, it was below 1 m; for the other three species, it ranged between 1 m and 2.3 m. Below 9 kHz, the break-even distance increased sharply in all five species. This increase is due to the increasing hearing thresholds of all species below 9 kHz (Figs 3, 4) and the fact that the transmission properties of the biotope do not change for frequencies below 9 kHz (Fig. 8). At frequencies above 9 kHz, the higher hearing thresholds compared with 18 kHz (Figs 3, 4) are offset at short distances by the higher excess attenuation at the higher frequency (Fig. 8).
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Discussion |
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Influences on the tuning of the hearing organ
Crickets and katydids (tettigoniids) use their auditory sensory system
mainly in two behavioral contexts: acoustic communication and bat avoidance.
Thus, selective pressure for high hearing sensitivity stems from two signal
classes with different spectral properties: conspecific communication signals
and bat echolocation calls. In most crickets, auditory sensitivity is high in
two frequency ranges (Pollack and
Imaizumi, 1999): the frequency of the calling songs (usually 3-9
kHz) and the frequency range of many bat echolocation calls (25-60 kHz;
Fenton et al., 1998
). Many
katydid species have calls with broad band spectra or with several distinct
frequency bands, which commonly extend from 10 kHz to 60 kHz
(Heller, 1988
). Hearing
sensitivity in such species usually has a broad frequency range of highest
sensitivity, comprising both the frequency range of their communication
signals and bat echolocation calls (e.g.
Kalmring et al., 1990
).
The communication signals of Neoconcephalus are more
`cricket-like' than `katydid-like' in that the main energy component of the
call is in a narrow low-frequency band and only minor ultrasound components
are present in the calls (Fig.
1; Greenfield,
1990; Libersat and Hoy,
1991
). The low amplitude of these ultrasound components and the
high intraspecific variability suggest little, if any, importance for
communication; if they were important for female phonotaxis, i.e. if they
would make a call more attractive or better localizable, sexual selection
theory would predict a pronounced ultrasound component in male calls (similar
to most other katydid species) and also lower variability within male calls of
each species for this trait (Anderson,
1994
). Therefore, it is most likely that the pronounced
low-frequency component of male calls is mainly, if not exclusively, used for
communication between males and females.
Surprisingly, in all five species of Neoconocephalus, the
frequency range of highest sensitivity of the hearing organ was not tuned to
either communication signals or to bat echolocation calls but to an
intermediate frequency range around 18 kHz
(Fig. 4). This mismatched
tuning could nevertheless be a by-product of the above-mentioned selective
pressures in combination with the limitations caused by the biophysics of the
hearing mechanism. In crickets, the high, narrow-band selectivity in the
low-frequency range is due to the transmission properties of the tracheal
system, which constitutes the main sound input for the hearing system
(Michelsen et al., 1994). In
katydids, the acoustic trachea acts as a finite exponential horn, which has
high-pass rather than band-pass characteristics
(Hoffmann and Jatho, 1995
).
The cut-off frequency of the exponential horn largely determines the
low-frequency roll-off of hearing thresholds. Towards high frequencies, the
gain of the exponential horn remains high, and the decrease in sensitivity
towards high frequency is probably due to the mechanical properties of the
receptor organ itself. This mechanism leads to a broad frequency range of high
sensitivity rather than to a W-shaped threshold curve, as found in crickets.
In Neoconocephalus, we found evidence for special adaptations to
hearing bats (see below), which suggest a strong selective pressure for high
sensitivity in the ultrasonic frequency range. The acoustic trachea of the
katydid hearing system, with its broad frequency range of high gain, probably
prevents the evolution of a sensitivity maximum of 40-50 kHz, but the
sensitivity in this range can be increased by an increase of the overall
sensitivity. In conclusion, we suggest that the tuning of the five
Neoconocephalus species is the consequence of selection for high
sensitivity in the frequency range of the conspecific signals (7-15 kHz) and
of bat echolocation calls (30-60 kHz). Highest sensitivity around 18 kHz is
probably a consequence of selection for high sensitivity in the two adjacent
frequency ranges.
Adaptations to hearing bats
The intensity/response functions of all five Neoconocephalus
species showed a peculiarity at ultrasonic frequencies between 35 kHz and 70
kHz; for stimulus intensities higher than 25-30 dB above threshold, the
intensity response function was more than twice as steep than that at lower
stimulus amplitudes (Fig. 5).
Iso-intensity functions of call responses were flat for lower stimulus
intensities (9-27 dB; Fig. 6)
in the complete frequency range tested, indicating that similar numbers of
receptor cells contribute to the compound action potential at each stimulus
frequency. This, in turn, suggests that best frequencies of individual
receptor cells are evenly distributed along the tuning curve of the whole
hearing organ (Pollack and Faulkes,
1998; Schul,
1999
), as was found for several katydid species (e.g.
Kalmring et al., 1990
;
Römer, 1983
; but see
Stölting and Stumpner,
1998
). The increase in the slope of the intensity response
function at high intensities in the ultrasonic range cannot be attributed to
an increased spike synchronization, because the width of the compound action
potential remains constant. Rather, the increased slope is explained by an
increased number of cells responding, i.e. a second receptor cell population
begins responding to ultrasonic stimuli. This receptor cell population could
either be a group of receptors tuned to ultrasonic frequencies, but with 25-30
dB higher thresholds, or could be cells tuned to lower frequencies with a
secondary sensitivity maximum at the higher frequencies. In crickets, most
receptor cells tuned to ultrasonic frequencies have such secondary sensitivity
maxima at lower frequencies close to the carrier frequency of the calling song
(Imaizumi and Pollack, 1999
),
whereas threshold curves described for katydid receptor cells do not show such
secondary peaks. Stölting and Stumpner
(1998
) demonstrate that
receptor cells of the intermediate organ may have high frequency auditory
tuning with thresholds that are 25 dB higher than that of receptor cells in
the crista acoustica, the major hearing organ in katydids. Thus, receptor
cells of the intermediate organ could be the second receptor cell population
responding to ultrasonic stimuli. Our whole nerve recordings do not allow us
to decide between the two possibilities; single cell recordings of auditory
receptor cells are required to answer this question.
The presence of a second group of receptor cells responding to ultrasound
with 25-30 dB higher thresholds is reminiscent of the auditory system in some
moths (Roeder, 1967). The ear
of the noctuid moth is comprised of only two receptor cells (A1 and A2). A1
and A2 have nearly identical tuning curves, but the A2 cell is approximately
20 dB less sensitive than the A1 cell
(Roeder, 1967
). Noctuid moths
show graded responses to bat calls: negative phonotaxis at low echolocation
call intensities, and erratic flight maneuvers at high intensities. The switch
between these behaviors is probably related to the intensity range fractioning
provided by the A1 and A2 receptors (reviewed in
Yager, 1999
).
The approximate threshold of the second receptor cell population at 40 kHz
described here is in the range of 70-75 dB SPL. A bat echolocation call
reaching an insect as large as Neoconocephalus with this amplitude
would probably produce an echo that the bat would be able to hear, thus
indicating an immediate danger for the insect
(Schulze and Schul, 2001). Bat
avoidance behaviors have been described in N. ensiger both during
flight (Libersat and Hoy,
1991
) and calling (Faure and
Hoy, 2000a
), and thresholds in both situations were at 70-75 dB
SPL. The correlation between behavioral and neuronal thresholds suggests that
the second receptor cell population determines the behavioral threshold for
bat-avoidance behavior in Neoconocephalus. Therefore, we interpret
its presence as an adaptation for predator detection.
Why do males not call at the frequency of highest female
sensitivity?
The amplitude of a male call is probably the single most important factor
determining its overall attractiveness. Call amplitude was found to be the
most important factor for intraspecific female choice
(Arak et al., 1990); with all
other parameters equal, amplitude differences of as little as 1-2 dB have been
reported to reliably cause female preferences for the louder signal (e.g.
Römer et al., 1998
).
Therefore, selection should favor male call frequencies that are perceived by
females as the loudest. Which call frequency is optimal for the male depends
on the tuning of the female hearing system and the sound-transmission
properties of the biotope. In the case of the Neoconocephalus species
studied here, females are most sensitive for frequencies around 18 kHz
(Fig. 4). However, sounds are
best transmitted through grasslands at lower frequencies; excess attenuation
is lowest for frequencies below 10 kHz and increases with increasing
frequencies above 10 kHz. Therefore, at short distances, when the transmission
through the biotope has only little effect, a call frequency of 18 kHz would
be optimal. At longer distances, beyond the break-even distance
(Fig. 10), call frequencies of
9-10 kHz seem ideal. The relevant distance for female choice is as long or
longer than half the nearest neighbor distance of calling males, because
females must choose (for the latest) when they are sitting between two calling
males.
Male Neoconocephalus are usually spaced 3-10 m apart (J. Schul, unpublished observation). Therefore, female phonotaxis should usually take place at considerably longer distances than at the break-even distances. Thus, the optimal call frequency for males of all five Neoconocephalus species is 9-10 kHz. Males of two species (N. bivocatus and N. nebrascensis) call at this frequency, while two species (N. retusus and N. ensiger) call at considerably higher frequencies (approximately 15 kHz) and N. robustus calls at lower frequencies (approximately 7 kHz).
At this point, we can only speculate as to which factors might be
responsible for these discrepancies between the call frequency and the
predicted optimal frequency in three of the five species. N. retusus
and N. ensiger, which both call above the predicted optimal
frequency, are the smallest of the five species
(Table 1). A physiological
constraint such as body size could hinder the evolution of lower call
frequencies in two ways. First, males might be too small to produce the lower
frequency effectively; i.e. they would lose more in absolute call amplitude
than they would gain in improved transmission (reviewed in
Bennet-Clark, 1998). Second,
the females might be too small to generate enough sound shadow to localize the
lower call frequency effectively; because katydid ears function as pressure
receivers (Michelsen et al.,
1994
), directional information is derived from intensity
differences between the sound entrances of both ears. These intensity
differences are caused by diffraction on the insect's body, which strongly
depends on body size (Michelsen,
1994
). As N. retusus and N. ensiger are the
smallest of the five species, their body size might be too small to generate
sufficient directional information at the optimal call frequency of 9-10 kHz.
In this case, their call frequency of 15 kHz would be a trade-off between
attractiveness for and localizability by the females. Such size constraints
would not explain the situation in N. robustus, where males call at 7
kHz rather than at 10 kHz. A possible explanation here could be the need for
this species to signal in a `private channel'
(Narins, 1995
) to avoid
masking of their signals by signals of other noisy animals.
Concluding remarks
Although the five species of Neoconocephalus studied here differ
considerably in the spectral composition of their calls, the tuning properties
of their hearing systems are very similar. The tuning of the hearing system
seems to be largely determined by the influence of factors such as bat
detection and the morphology of the hearing system. The call frequency is not
strongly influenced by the tuning of the hearing organ due to constraints
imposed by the transmission properties of the biotope: the high pass
characteristics of the grassland habitat favor call frequencies of 10 kHz for
all species. Thus, the mismatch between call frequencies and tuning of the
hearing systems seems to be mainly a consequence of bat predation, which
favors high sensitivity at ultrasonic frequencies, and the low pass
transmission properties of the biotope, which favor a call frequency lower
than the best frequency of the hearing organ.
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