|
| |
|
|
|
|
||||
| Home Help Feedback Subscriptions Archive Search Table of Contents | ||||
First published online April 18, 2006
Journal of Experimental Biology 209, 1757-1764 (2006)
Published by The Company of Biologists 2006
doi: 10.1242/jeb.02189
Spectral selectivity during phonotaxis: a comparative study in Neoconocephalus (Orthoptera: Tettigoniidae)
Division of Biological Sciences, University of Missouri, Tucker Hall, Columbia, MO, 65211, USA
* Author for correspondence (e-mail: jadz67{at}mizzou.edu)
Accepted 28 February 2006
 |
Summary |
|---|
 TOP Summary IntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Key words: acoustic communication, spectral processing, carrier frequency, call recognition, hearing, phonotaxis, Neoconocephalus
|
Introduction |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
;
Heller, 1988); only a few
groups have narrow-band spectra in audible (e.g.
Suga, 1966;
Bailey, 1970) or ultrasonic
(Morris et al., 1994)
frequency ranges. In the genus Neoconocephalus, most of the call
energy is concentrated in a narrow low-frequency band, with ultrasonic
frequency components at least 20 dB softer than the low-frequency band
(Fig. 1A)
(Greenfield, 1990). The
characteristic frequency (center frequency) of the low-frequency band within
the genus ranges from 7 to 16 kHz
(Greenfield, 1990;
Schul and Patterson, 2003).
Based on measurements of hearing thresholds and the sound transmission
properties of the habitats (tall grasslands and marshes), center frequencies
close to 10 kHz are calculated to be most advantageous in this genus
(Schul and Patterson,
2003).
|
). This frequency is surprisingly low given the disadvantages
of calling at 7 kHz: the hearing sensitivity in N. robustus is about
7 dB lower at 7 kHz than at 10 kHz, and there is no improvement in signal
transmission between 10 kHz and 7 kHz to justify the use of a frequency that
is mismatched with female sensitivity
(Schul and Patterson, 2003). A
potential explanation, however, is that calling in the low-frequency band
provides this species with a `private channel'
(Narins, 1995) that is free of
interfering calls of sympatric congeners. Alternatively, the low-frequency
band may provide female N. robustus with an additional cue for call
recognition beyond the temporal pattern, which is similar to the temporal
pattern of several congeners (Deily and
Schul, 2004).
In tettigoniids, the hearing organ provides fine spectral resolution at the
level of receptor cells (Kalmring et al.,
1978; Römer,
1983). However, at the level of primary auditory interneurons,
this frequency resolution is largely discarded as receptor cells converge on
just a few interneurons with broad spectral sensitivity (e.g.
Schul, 1997;
Stumpner, 1999) (reviewed by
Gerhardt and Huber, 2002).
Accordingly, spectral selectivity of katydids is generally limited to
detecting the absence or presence of energy in broad frequency bands (e.g.
Latimer and Sippel, 1987;
Bailey and Yeoh, 1988;
Dobler et al., 1994;
Jatho, 1995). Preferences
based on fine-scale differences in call spectra (e.g.
Bailey and Yeoh, 1988;
Schul et al., 1998) are most
probably based on differences in the perceived call amplitudes
(Schul, 1999) (reviewed by
Gerhardt and Huber, 2002). The
more detailed spectral processing found in other groups of insects (e.g.
Doolan and Young, 1989;
Fonseca et al., 2000;
Fonseca and Revez, 2002) has
not been described in katydids.
The small spectral difference between N. robustus and most of its congeners in the position of the low-frequency band (7 kHz versus 10 kHz) appears unlikely to be resolved by the spectral selectivity of the ascending pathway in katydids, and thus appears unlikely to serve an important function. However, the disadvantages that the use of the low carrier frequency entails for N. robustus (see above) suggest an adaptive function in this species, possibly for call recognition or masking avoidance. Here, we examine the spectral selectivity in N. robustus and two closely related species with sympatric occurrence (N. nebrascensis and N. bivocatus). We determine the importance of the position of the low-frequency band for female phonotaxis in N. robustus, and explore differences in spectral processing among the three species. Furthermore, we investigate potential mechanisms females may use to discriminate the carrier frequency of N. robustus from the higher carrier frequencies of its congeners.
|
Materials and methods |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
) and Walker
et al. (Walker et al., 1973).
N. robustus and N. bivocatus are considered sibling species
(Walker et al., 1973;
Greenfield, 1990). Preliminary
results of a molecular phylogenetic analysis based on a mitochondrial locus
support this assumption (R. L. Snyder and J. Schul, unpublished data), and
indicate that these species, together with N. nebrascensis and N.
ensiger, form a distinct clade within the genus
Neoconocephalus. The insects were kept at 20–25°C and a light:dark cycle of 14 h:10 h. The females were held for at least 2 weeks after their adult molt before they were used in experiments. Females were tested for up to 5 weeks, during which we detected no changes in their selectivity.
Phonotaxis experiments
We conducted behavioral tests on a walking compensator [Kramer treadmill
(Weber et al., 1981)] in an
anechoic chamber at 25±1°C. In short, the insects were placed on
top of a sphere, free to walk but kept in place by compensatory sphere
rotations, while acoustic signals were presented from loudspeakers located in
the insect's horizontal plane. The intended direction and speed of the animal
were read out from the control circuitry. The experiments were performed in
the dark except for an infrared light used to monitor the movements of the
animal on the sphere. For details see Weber et al.
(Weber et al., 1981) and Schul
(Schul, 1998).
Stimulation
We generated synthetic signals using a custom developed
DA-converter/amplifier system (16 bit resolution, 250 kHz sampling rate). The
signals were attenuated using a computer-controlled attenuator and delivered
via one of two loudspeakers (EAS 10TH400C) mounted at a distance of
150 cm in the horizontal plane of the insect and separated by an angle of
115°. We adjusted signal amplitude using a 1/4'' condenser microphone
(G.R.A.S. 40BF, Holte, Denmark) positioned 1 cm above the top of the sphere,
and a Bruel and Kjaer sound level meter (B&K 2231, Naerum, Denmark). All
sound pressure levels are given as dB peak sound pressure level (SPL; re 20
µPa).
The temporal patterns of the call models used in this study were based on
population mean values determined by Büttner
(Büttner, 2002) at
25°C. All pulses used in the three call models had 0.5 ms rise and fall
times, which are included in the durations of the pulses. Call models of
N. robustus and N. bivocatus were identical to the control
stimuli used by Deily and Schul (Deily and
Schul, 2004).
The temporal pattern for N. robustus (Fig. 1B) consisted of a continuous train of pulses of 3.0 ms duration, separated by silent intervals of 2.0 ms duration (i.e. a single-pulse pattern).
The temporal pattern for N. bivocatus consisted of a continuous train of paired pulses: the duration of these pulses was 2.2 ms and 3.0 ms, with an interval of 2.3 ms in between. These paired pulses were repeated after an interval of 4.0 ms (Fig. 1B). The call models of both N. robustus and N. bivocatus were presented as continuous signals, without a second order time pattern modulating the pulse pattern.
The call model of N. nebrascensis had the same pulse pattern as the N. robustus model (pulse duration of 3.0 ms and interval duration of 2.0 ms). However these pulses were not presented continuously, but grouped into verses of 1000 ms duration, which were repeated after a silent pause of 800 ms.
The calls of N. robustus, N. nebrascensis and N.
bivocatus had similar spectral composition (see Introduction) but
differed in the center frequency of the low-frequency band
(Fig. 1A). The center frequency
was at 7.0 kHz in N. robustus, 10.4 kHz in N. nebrascensis
and 10.1 kHz in N. bivocatus
(Schul and Patterson, 2003).
We used pure tone carriers of 7 kHz (N. robustus) and 10 kHz (N.
nebrascensis and N. bivocatus) with the temporal patterns
described above to construct conspecific call models for each species. This
simplification of both the temporal and spectral structure did not noticeably
reduce the attractiveness of these stimuli relative to natural calls
(Deily and Schul, 2004). These
call models were used as control stimuli throughout this study. We used the
conspecific temporal pattern for each of the three species during all
experiments.
Experiment 1
We tested the effects of both carrier frequency and call amplitude on
attractiveness. The carrier frequency of the call models varied from 5 to 60
kHz. Stimuli were presented at amplitudes of both 68 and 80 dB SPL.
Experiment 2
We tested the effect of an additional high frequency component on the
attractiveness of the call models by adding a second sinusoid to the
conspecific carrier frequencies. Frequencies were chosen as integer multiples
of the carrier frequencies (14, 28 and 42 kHz for N. robustus; 20 and
40 kHz for N. nebrascensis and N. bivocatus). Note that
although up to three high frequency components were tested per species, only
one high frequency component was added to the low-frequency band per trial
stimulus, i.e. for N. nebrascensis, the three stimuli consisted of 10
kHz alone (control), 10 kHz + 20 kHz and 10 kHz + 40 kHz. The absolute
amplitude of the low-frequency component was set for each individual to the
lowest amplitude at which it showed consistent phonotaxis when presented
alone, and was held constant within each series of an individual. Amplitudes
of the low-frequency component ranged from 50 to 56 dB SPL for N.
robustus, 44 to 56 dB SPL for N. nebrascensis and 44 to 62 dB
SPL for N. bivocatus. The amplitude of the high frequency component
was varied between 0 dB and +18 dB relative to the conspecific carrier. We
conducted this experiment at amplitudes close to the behavioral threshold to
detect weak effects of the high frequency component which would be masked by
the strong excitation at higher stimulus amplitudes. Phonotaxis at these
near-threshold amplitudes was comparable to that observed at 68 and 80 dB
SPL.
Experimental protocol
The experimental protocol is described in detail by Schul
(Schul, 1998) and Bush et al.
(Bush et al., 2002). Briefly,
all stimuli were presented twice for approximately 1.5 min each (3 min in
total), with the position of the loudspeaker changed between the two
presentations. At the beginning of each series the control stimulus was
presented, then two or three test stimuli, then another control, etc. Between
stimuli a 1-min period of silence was imposed. Each experimental series lasted
between 30 and 90 min, during which up to nine experimental stimuli (plus four
controls) were presented. We varied the sequence of stimulus presentation
among the individual females tested.
Data analysis
To evaluate the relative response of a female during a test situation, we
calculated a phonotaxis score (Schul,
1998) which included measures for three criteria that describe the
relative strength of phonotaxis: (1) the walking speed relative to the speed
during the control stimulus (describing the locomotion activity elicited); (2)
the vector length, describing the accuracy of orientation; and (3) the
orientation relative to the orientation during the control stimulus.
Phonotaxis scores range from approximately +1 (perfect positive phonotaxis) to
–1 (perfect negative phonotaxis). Phonotaxis scores close to 0 indicate
either no response or random orientation [for details of the data analysis and
calculation of the phonotaxis score see Schul
(Schul, 1998)]. To facilitate
comparison between species and between stimulus intensities, we normalized
phonotaxis scores by setting the phonotaxis score to the control stimulus to
1.
We present all phonotaxis scores as mean ± standard error of the
mean (s.e.m.). Female responses were considered significant if two criteria
were met: (i) the phonotaxis scores were significantly greater [Wilcoxon
paired sample test, P<0.05
(Zar, 1984)] than the
phonotaxis scores obtained from the same females in response to silence; and
(ii) the average response was at least 50% of the response to the model of the
conspecific call. Both criteria agreed for most data points; in the few cases
that only one was significant, the second criterion was usually more stringent
than the first. Therefore, we do not present the results of the Wilcoxon
paired sample tests in the text. Note that the application of significance
criteria and cut-off frequencies (see below) merely emphasize the relative
attractiveness of stimuli and are not meant to classify stimuli as
`recognized' or `not recognized' (for a detailed discussion, see
Bush et al., 2002).
For experiment 1, we constructed frequency response functions; each
function had a distinct roll-off towards higher frequencies above the
conspecific call carrier frequency (Figs
2,
3). We fitted a sigmoidal
function to the phonotactic response curve above the conspecific carrier
frequency (see above) of each female by minimizing the sum of the squared
errors. The frequency at which the sigmoid had an amplitude of 50% was defined
as the upper cut-off frequency. We compared median upper cut-off frequencies
between the three species with a Mann-Whitney test, and at different stimulus
intensities within each species using a Wilcoxon paired sample test
(Zar, 1984).
|
|
). We calculated
analysis of variance (ANOVA; General Linear Model) and post-hoc
comparisons using Minitab (Release 14.12.0, Minitab Inc., USA). We used a
significance criterion (
) of 0.05. |
Results |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
|
For frequencies of 20 kHz or higher, mean phonotaxis scores of N. robustus and N. nebrascensis were below 0.1; in N. bivocatus, however, response strength remained above 0.1 for frequencies up to 40 kHz (Fig. 2). Although these responses were not significant, they suggest that frequencies between 20 and 40 kHz were somewhat attractive to N. bivocatus females.
Fig. 3 compares the spectral selectivity of the three species at two stimulus amplitudes, 68 dB SPL and 80 dB SPL. In N. robustus, female selectivity did not change with stimulus amplitude (Fig. 3A); median cut-off frequencies (Table 1) did not differ between 68 dB SPL and 80 dB SPL (Mann–Whitney U-test, P>0.20).
In both N. nebrascensis and N. bivocatus, spectral selectivity changed significantly with stimulus amplitude. Significant responses occurred over a narrower frequency range at 68 dB SPL than at 80 dB SPL in both species (Fig. 3B,C). Accordingly, median upper cut-off frequencies (Table 1) were significantly lower at 68 dB SPL than at 80 dB SPL (Mann–Whitney U-test, P<0.05 for both species).
The amplitude independence of spectral selectivity in N. robustus is a typical signature of `lateral inhibition', i.e. the spectral selectivity seems to be generated by low-frequency excitation and high frequency inhibition. Conversely, changes of spectral selectivity as seen in N. nebrascensis and N. bivocatus suggest that selectivity is generated by excitation only. We tested whether high frequencies have an inhibitory effect on female phonotaxis in the second set of experiments.
Experiment 2
In N. robustus, the inhibitory effect of adding a higher harmonic
to the conspecific carrier frequency of 7 kHz
(Fig. 4A) was highly
significant (ANOVA, P<0.001 for all three frequencies, see
Table 2 for details).
Post-hoc pairwise comparison demonstrated that responses to all
stimuli that include a high frequency component were significantly weaker than
to the control stimulus (Table
2). Females failed to show significant responses to any stimulus
containing a high frequency component, except for 14 kHz at 0 dB relative
amplitude (Fig. 4A).
|
|
In N. nebrascensis, adding either 20 kHz or 40 kHz to the conspecific carrier frequency (10 kHz) had significant effects on female responses (Fig. 4B; ANOVA: 20 kHz, P<0.005; 40 kHz, P<0.002; Table 2). Post-hoc pair-wise comparisons indicated that female responses to stimuli containing either frequency at +12 dB and +18 dB were significantly weaker than to the control stimulus (Tukey test, P<0.05 in all cases). However, all stimuli that included a high frequency component elicited significant responses in N. nebrascensis (Fig. 4B).
In N. bivocatus, adding a higher harmonic to the conspecific carrier frequency of 10 kHz (Fig. 4C) had marginally significant effects (ANOVA: 20 kHz, P<0.05; 40 kHz, P<0.1; Table 2). Post-hoc pairwise comparison to the control stimulus detected a significant reduction in response strength (P<0.05) only for 20 kHz at +12 dB relative amplitude, whereas for all other stimuli with high frequency components these comparisons were not significant (Table 2). All stimuli that included a high frequency component elicited significant responses in N. bivocatus (Fig. 4C).
|
Discussion |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
The female response curves in Figs 2 and 3 were most probably a function of attractiveness of the different frequencies, rather than of their localizability. Analyzing the walking speed alone resulted in the same pattern of response functions as using the phonotaxis score. The walking speed indicates how enthusiastically females respond to a stimulus, independent of the available directional cues (i.e. it is thus influenced only by call attractiveness).
In N. robustus responses decreased steeply toward higher
frequencies, and the upper cut-off frequency of female responses did not
change with stimulus amplitude (Fig.
2, Fig. 3A). This
suggests that `lateral inhibition'
(Gerhardt and Huber, 2002;
Hennig et al., 2004) is
involved in generating the spectral selectivity towards higher frequencies;
frequencies below the upper cut-off frequency (10 kHz) have excitatory effect,
while higher frequencies inhibit female responses. Experiment 2 directly
demonstrates the inhibitory effect of frequencies above 10 kHz.
In N. bivocatus spectral selectivity changes significantly with stimulus amplitude (Fig. 3C), and the inhibitory effect of high frequencies during experiment 2 was marginal. This suggests that lateral inhibition plays only a minor role in the spectral selectivity towards higher frequencies in this species. Rather, an excitatory function alone seems to sufficiently explain the selectivity found in experiment 1. The nonsignificant positive responses to frequencies from 20 to 40 kHz (Fig. 2) also indicate that high frequencies have little, if any, inhibitory effect in N. bivocatus.
Results in N. nebrascensis were intermediate between the two other species. High frequencies had a highly significant inhibitory effect during experiment 2, although considerably less than in N. robustus (Table 2, Fig. 4). Frequency selectivity towards higher frequencies changed with stimulus amplitude, albeit less than in N. bivocatus, and there was no positive trend for responses in the frequency range between 20 and 40 kHz as there was for N. bivocatus (Fig. 2). These results suggest that lateral inhibition plays a significant role in spectral selectivity in this species, but to a much lesser extent than in N. robustus.
Our results indicate that the influence of lateral inhibition on the spectral selectivity towards high frequencies differs significantly among the three species: inhibition is weakest in N. bivocatus, somewhat stronger in N. nebrascensis, and by far the strongest in N. robustus. Additionally, the border-frequency between excitation and inhibition was lower in N. robustus (approximately 10 kHz) than in the other two species (approximately 15-18 kHz).
Neuronal processes underlying spectral selectivity
Among tettigoniids high hearing sensitivities occur in the broad range from
below 5 kHz to above 80 kHz [(Kalmring et
al., 1990) in Neoconcocephalus
(Schul and Patterson, 2003)].
Auditory receptor cells project into the prothoracic ganglion where they
converge onto a small number of auditory interneurons, which consequently have
broad spectral selectivity (reviewed by
Stumpner and Helversen, 2001).
Sharpening of spectral selectivity through lateral inhibition occurs most
prominently in one neuron: AN-1 receives excitation from frequencies below 20
kHz, but inhibition from frequencies above 20 kHz
(Schul, 1997;
Stumpner, 1997). Accordingly
AN-1 thresholds increase steeply between 20 and 30 kHz [roll off
>50–60 dB per octave (Schul,
1997; Stumpner,
1997)]. AN-1 is most probably involved in generating the spectral
selectivity observed during phonotaxis in several tettigoniid species
(Schul, 1997;
Stumpner, 1997).
The ascending pathway of Neoconocephalus has not been studied in
detail. However, it is likely that the differences in spectral selectivity
described here result from differences in AN-1 properties among the three
species. The strength of the high-frequency inhibition on AN-1 should vary
dramatically among them, being strongest in N. robustus and weakest
in N. bivocatus. Furthermore, the border between excitation and
inhibition should be shifted towards lower frequencies in N. robustus
compared to the two other species. Among closely related species of the
tettigoniid subfamily Phaneropterinae, differences of AN-1 properties occur in
a similar order of magnitude as suggested by our experiments
(Stumpner, 2002).
The sharp decline in response strength of female N. robustus
between 9 and 12 kHz and the amplitude independence of this decline are
exceptional among ensiferans. In tettigoniids, behavioral tuning is usually
amplitude dependent [N. bivocatus and N. nebrascensis in
this study (Hardt, 1988;
Dobler et al., 1994)];
preferences based on small-scale spectral differences (within frequency ranges
of a few kHz) are overridden by small changes in amplitude
(Bailey and Yeoh, 1988;
Schul et al., 1998). In some
crickets, behavioral tuning does exhibit steep roll-offs (e.g.
Hennig and Weber, 1997).
However, this selectivity is caused by the tuning of the hearing organ, and in
this respect is also amplitude dependent. In contrast, N. robustus
responds to 9 kHz, but not to 12 kHz, largely independent of call
amplitude.
Although spectral selectivity in N. robustus appears to have
attained a `new quality' among tettigoniids in steepness and amplitude
independence, it is instead most probably based on quantitative changes in the
sensory system: high frequency inhibition on AN-1 shifted towards lower
frequencies, and its synaptic weighting increased (see above). The spectral
selectivity of N. robustus is most probably the result of evolution
from less selective ancestors. Given that 7 kHz is less suited than 10 kHz for
long range communication in Neoconocephalus
(Schul and Patterson, 2003),
the question arises: What evolutionary forces caused the shift in call
frequency and call processing in N. robustus?
Evolutionary influences on call spectrum
The three species studied here are probably sibling species (see Materials
and methods); each species' call features one characteristic that
distinguishes it from the calls of the other two species: In N.
bivocatus and N. nebrascensis these are temporal characters
(double-pulse pattern in N. bivocatus and verse structure in N.
nebrascensis), while in N. robustus the center frequency is
shifted significantly below 9 kHz
(Büttner, 2002;
Schul and Patterson, 2003).
These three call characteristics (double-pulses, verse structure, and center
frequency below 9 kHz) are uncommon in this genus: of 23 described calls, 18
have single-pulse pattern, 17 are continuous
(Greenfield, 1990), and most
species' calls are limited to frequencies above 9 kHz
(Schul and Patterson, 2003;
Greenfield, 1990). This
pattern suggests that within the clade containing N. robustus, N.
nebrascensis and N. bivocatus, the ancestral call consisted of a
continuous single-pulse temporal pattern and a center-frequency of about 10
kHz. The `unique`characteristic in each species' call are therefore probably
derived call traits.
In both N. nebrascensis and N. bivocatus, the derived
temporal characteristics provide cues for the females to recognize their
conspecific calls: N. bivocatus females recognize the double pulse
rate of approximately 87 Hz (Deily and
Schul, 2004), and N. nebrascensis females require a
distinct verse structure (J.A.D. and J.S., our unpublished data). Neither of
these two species shows significant phonotaxis to signals with the temporal
pattern of its congeners; i.e. their species-specific temporal call pattern
ensures species isolation. By contrast, the presence or absence of these
derived temporal characteristics is not a reliable cue for female N.
robustus, which show significant phonotaxis to the temporal pattern of at
least one congener (N. bivocatus,
Fig. 5). Thus, temporal pattern
recognition is insufficient for N. robustus to avoid mismatings.
Furthermore, temporal selectivity in N. robustus could not be higher
without rejecting the conspecific temporal pattern
(Deily and Schul, 2004).
However, in this species, the spectral difference provides a more reliable cue
for species recognition, especially when combined with the temporal cues
(Fig. 5).
|
Ancestors of N. robustus most probably had the same temporal call
pattern (and the same temporal call recognition mechanism) as N.
robustus, but a higher center frequency. After the appearance of species
with derived temporal patterns, the temporal call recognition of this
ancestral population would not have enabled reliable rejection of the `new'
calls. Thus, selection would have favored any traits that reduced the risk of
hybridization. Because temporal selectivity could not be sharpened enough to
reject the new temporal pattern (see above) we suggest that a lower call
frequency evolved in response to the appearance of new call patterns. Thus a
reinforcement-like process (Dobzhansky,
1937) could have gradually shifted the call center frequency
towards lower frequencies and concomitantly sharpened spectral selectivity in
N. robustus.
Hearing sensitivity of N. robustus females is considerably lower
at 7 kHz than at 10 kHz and therefore the shift to the lower call center
frequency resulted in a reduction of communication distance
(Schul and Patterson, 2003).
Also, as the ears of tettigoniids usually function as pressure receivers
rather than pressure gradient receivers, 7 kHz probably provides less
peripheral directionality than 10 kHz
(Gerhardt and Huber, 2002).
These disadvantages of the derived center frequency in N. robustus
support our view that N. robustus was `pushed' by congeners to the
lower center frequency, rather than that the low center frequency provides an
advantage in itself such as a `private' communication channel free of masking
signals. Owing to the strong inhibitory effect of higher frequencies on female
phonotaxis, calls of congeners should inhibit phonotaxis in N.
robustus and therefore interfere with intraspecific communication in this
species. The adaptive value of the spectral selectivity of N.
robustus seems not to be interference avoidance, but rather species
isolation.
|
Acknowledgments |
|---|
|
References |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Bailey, W. J. (1970). The mechanics of
stridulation in bush crickets (Tettigonioidea, Orthoptera). I. The tegminal
generator. J. Exp. Biol.
52,495
-505.
Bailey, W. J. and Yeoh, P. B. (1988). Female phonotaxis and frequency discrimination in the bushcricket Requena verticalis. Physiol. Entomol. 13,363 -372.
Bush, S. L., Gerhardt, H. C. and Schul, J. (2002). Pattern recognition and call preferences in treefrogs (Anura: Hylidae): a quantitative analysis using a no-choice paradigm. Anim. Behav. 63,7 -14.[CrossRef]
Büttner, U. K. (2002). Charakterisierung der Gesänge von fünf in Missouri (USA) heimischen Neoconocephalus-Arten (Orthoptera, Tettigoniidae). Diploma Thesis, University of Erlangen, Germany.
Deily, J. A. and Schul, J. S. (2004).
Recognition of calls with exceptionally fast pulse rates: female phonotaxis in
the genus Neoconocephalus (Orthoptera: Tettigoniidae). J.
Exp. Biol. 207,3523
-3529.
Dobler, S., Stumpner, A. and Heller, K. G. (1994). Sex-specific spectral tuning for the partner's song in the duetting bushcricket Ancistrura nigrovittata (Orthoptera: Phaneropteridae). J. Comp. Physiol. A 175,303 -310.
Dobzhansky, T. (1937). Genetics and the Origin of Species. New York: Columbia University Press.
Doolan, J. M. and Young, D. (1989). Relative
importance of song parameters during flight phonotaxis and courtship in the
bladder cicada Cystosoma saundersii. J. Exp. Biol.
141,113
-131.
Fonseca, P. J. and Revez, M. A. (2002). Song
discrimination by male cicadas Cicada barbara lusitanica (Homoptera,
Cicadidae). J. Exp. Biol.
205,1285
-1292.
Fonseca, P. J., Münch, D. and Hennig, R. M. (2000). How cicadas interpret acoustic signals. Nature 405,297 -298.[CrossRef][Medline]
Froeschner, R. C. (1954). The grasshoppers and other Orthoptera of Iowa. Iowa St. Coll. J. Sci. 29,163 -354.
Gerhardt, H. C. and Huber, F. (2002). Acoustic Communication in Insects and Anurans. Chicago, IL: University of Chicago Press.
Greenfield, M. D. (1990). Evolution of acoustic communication in the genus Neoconocephalus: discontinuous songs, synchrony, and interspecific interactions. In The Tettigoniidae: Biology, Systematics and Evolution (ed. W. J. Bailey and D. C. F. Rentz), pp. 71-97. Heidelberg: Springer.
Hardt, M. (1988). Zur Phonotaxis von Laubheuschrecken: eine vergleichende verhaltensphysiologische und neurophysiologisch/neuroanatomische Untersuchung. PhD thesis, Bochum, Germany.
Heller, K.-G. (1988). Die Biologie der Europäischen Laubheuschrecken. Weikersheim, Germany: Verlag J. Margraf.
Hennig, R. M. and Weber, T. (1997). Filtering of temporal parameters of the calling song by cricket females of two closely related species: a behavioral analysis. J. Comp. Physiol. A 180,621 -630.[CrossRef]
Hennig, R. M., Franz, A. and Stumpner, A. (2004). Processing of auditory information in insects. Microsc. Res. Tech. 63,351 -374.[CrossRef][Medline]
Jatho, M. (1995). Untersuchungen zur Schallproduktion und zum phonotaktischen Verhalten von Laubheuschrecken (Orthoptera: Tettigoniidae). PhD thesis, Philipps University, Marburg, Germany.
Kalmring, K., Lewis, B. and Eichendorf, A. (1978). The physiological characteristics of the primary sensory neurons of the complex tibial organ of Decticus verrucivorus L. (Orthoptera, Tettigonioidea). J. Comp. Physiol. 127,109 -121.[CrossRef]
Kalmring, K., Schröder, J., Rössler, W. and Bailey, W. J. (1990). Resolution of time and frequency patterns in the tympanal organs of Tettigoniids. II. Its basis at the single receptor level. Zool. Jb. Physiol. 94,203 -215.
Latimer, W. and Sippel, M. (1987). Acoustic cues for female choice and male competition in Tettigonia cantans.Anim. Behav. 35,887 -900.[CrossRef]
Morris, G. K., Mason, A. C. and Wall, P. (1994). High ultrasonic and tremulation signals in neotropical katydids (Orthoptera: Tettigoniidae). J. Zool. Lond. 233,129 -163.
Narins, P. (1995). Frog communication. Sci. Am. 273,62 -67.
Römer, H. (1983). Tonotopic organization of the auditory neuropile in the bushcricket Tettigonia viridissima.Nature 306,60 -62.[CrossRef]
Schul, J. (1997). Neuronal basis of phonotactic behaviour in Tettigonia viridissima: processing of behaviourally relevant signals by auditory afferents and thoracic interneurons. J. Comp. Physiol. A 180,573 -583.[CrossRef]
Schul, J. (1998). Song recognition by temporal cues in a group of closely related bushcricket species (Genus Tettigonia). J. Comp. Physiol. A 183,401 -410.[CrossRef]
Schul, J. (1999). Neuronal basis for spectral song discrimination in the bushcricket Tettigonia cantans. J. Comp. Physiol. A 184,457 -461.[CrossRef]
Schul, J. and Patterson, A. C. (2003). What
determines the tuning of hearing organs and the frequency of calls? A
comparative study in the katydid genus Neoconocephalus (Orthoptera,
Tettigoniidae). J. Exp. Biol.
206,141
-152.
Schul, J., Helversen, O. V. and Weber, T. (1998). Selective phonotaxis in Tettigonia cantans and T. viridissima in song recognition and discrimination. J. Comp. Physiol. A 182,687 -694.[CrossRef]
Stumpner, A. (1997). An auditory interneurone tuned to the male song frequency in the duetting bushcricket Ancistrura nigrovittata (Orthoptera, Phaneropteridae). J. Exp. Biol. 200,1089 -1101.[Abstract]
Stumpner, A. (1999). An interneurone of unusual morphology is tuned to the female song frequency in the bushcricket Ancistrura nigrovittata (Orthoptera, Phaneropteridae). J. Exp. Biol. 202,2071 -2081.[Abstract]
Stumpner, A. (2002). A species-specific frequency filter through specific inhibition, not specific excitation. J. Comp. Physiol. A 188,239 -248.[Medline]
Stumpner, A. and Helversen, D. V. (2001). Evolution and function of auditory systems in insects. Naturwissenschaften 88,159 -170.[CrossRef][Medline]
Suga, N. (1966). Ultrasonic production and its reception in some neotropical Tettigoniidae. J. Insect Physiol. 12,1039 -1050.[CrossRef][Medline]
Walker, T. J., Whitesell, J. J. and Alexander, R. D. (1973). The robust conehead: two widespread sibling species (Orthoptera: Tettigoniidae: Neoconocephalus "robustus"). Ohio J. Sci. 73,321 -330.
Weber, T., Thorson, J. and Huber, F. (1981). Auditory behaviour of the cricket. I. Dynamics of compensated walking and discrimination paradigms on the Kramer treadmill. J. Comp. Physiol. 141,215 -232.[CrossRef]
Zar, J. H. (1984). Biostatistical Analysis. London: Prentice Hall.
CiteULike 
Complore 
Connotea 
Del.icio.us 
Digg 
Reddit 
Technorati 
Twitter What's this?
This article has been cited by other articles:
|
|
 |
|
  J. D. Triblehorn and J. Schul Sensory-Encoding Differences Contribute to Species-Specific Call Recognition Mechanisms J Neurophysiol, September 1, 2009; 102(3): 1348 - 1357. [Abstract] [Full Text] [PDF]
|
|
| |||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
