Song discrimination by male cicadas Cicada barbara lusitanica (Homoptera, Cicadidae)
Departamento de Zoologia e Antropologia and Centro de Biologia Ambiental, Faculdade de Ciências de Lisboa, Bloco C2, Campo Grande, 1749-016 Lisboa, Portugal
* e-mail: pfonseca{at}fc.ul.pt
Accepted 18 February 2002
![]() |
Summary |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Key words: cicada, Cicada barbara lusitanica, song discrimination, temporal pattern, frequency discrimination
![]() |
Introduction |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
The ability to discriminate the conspecific signal from heterospecific
songs has been studied in different insect groups (e.g. crickets:
Popov and Shuvalov, 1977;
Weber et al., 1981
;
grasshoppers: von Helversen and von
Helversen, 1983
; Stumpner and
von Helversen, 1994
). In order to assess the relative importance
of particular song parameters in song discrimination, most studies have used
the phonotactic preference of reproductively receptive females or any other
stereotyped response to a modified or a natural song playback. Both the time
pattern (e.g. Pollack and Hoy,
1979
; Hennig and Weber,
1999
) and the frequency spectrum (e.g.
Popov et al., 1975
;
Oldfield, 1980
) of the signal
have been shown to be involved in species discrimination. In cicadas, however,
few studies have addressed this question, and the relative importance of the
song parameters in species recognition is still poorly known. Some evidence
indicates that the frequency spectrum of the signal carries information about
the species-identity of a calling male
(Doolan and Young, 1989
;
Daws et al., 1997
), whereas the
temporal pattern might reveal the quality of the sender at a short distance
(Doolan and Young, 1989
).
Cicadas have traditionally been difficult to work with in the laboratory,
and female flight phonotaxis has been difficult to observe in some species
(Daws et al., 1997). On the
other hand, male cicadas have been described to respond by calling when
stimulated with the conspecific song
(Villet, 1992
;
Fonseca, 1994
). Cicada
barbara males are such an example and, alternatively, the response of
males towards natural and modified songs can be used to determine the relative
importance of song parameters in song discrimination. This method has proved
reliable for some orthopteran species in which either males or females respond
to a song stimulus by singing a response song
(Skovmand and Pedersen, 1983
).
Similarly, Simmons et al.
(1971
) induced cicada males to
sing by presenting sound stimuli and used this behaviour to investigate song
production and hearing in periodical cicadas.
Hence, we used the stereotyped singing response behaviour of males to
analyse song discrimination in C. barbara. We investigated the
following questions: (i) can C. barbara males discriminate the
conspecific calling signal from the songs of other sympatric cicadas? If so,
(ii) which parameters of the song are involved in song discrimination? We
demonstrate that, in contrast to what is presently known for cicadas
(Doolan and Young, 1989;
Daws et al., 1997
), the
temporal pattern can influence long-range communication. Moreover, the
mechanism underlying the frequency-related behaviour in C. barbara
males differs from what has been described for another cicada species
(Daws et al., 1997
).
![]() |
Materials and methods |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Experimental arrangement
All behavioural experiments were conducted outdoors in a cylindrical cage,
100 cm in diameter and 60 cm high, supported by four legs (60 cm) and covered
with green insect net (Fig. 1).
The structure of the arena was made of iron rods 0.8 cm thick. During the
experiments, stimuli were individually presented by a loudspeaker (Dynaudio
D28/2) positioned 60 cm away from the centre of the arena. A laptop (Toshiba
230 CX) equipped with a Yamaha OPL3-SAx soundboard generated the stimuli,
delivered at a D/A rate of 44 kHz to an amplifier (Phoenix Gold QX 4040)
through a step attenuator, allowing an accurate control of the signal
amplitude. The amplitude of the sound stimulus at the stick was calibrated
with a Radio Shack (catalogue no. 33-2050) sound-level meter.
|
Experimental design
Each male was tested individually under one or two of the five different
behavioural experiments (see Stimulus design). For each experiment, the test
procedure was as follows: individual males were placed on the base of a wooden
stick 60 cm long placed at the centre of the arena, and they immediately
walked upwards. When an animal entered the arena, a sound stimulus was
presented by the loudspeaker and singing activity by a male was taken as a
positive response. The time elapsed from the onset of the playback was
recorded and the stimulus was turned off. A failure to respond during 3 min of
consecutive playback was taken as a negative response. In either case, the
experiment continued with the presentation of a different stimulus after
moving the cicada back to the base of the stick.
Each behavioural experiment consisted of a predefined set of test stimuli (T) presented in random order. To control for motivational changes, a positive control (PC, the conspecific song at 90 dB sound pressure level (SPL) was always required before and after two consecutive test stimuli. An animal with high motivation would always respond to this positive control; failure to respond to this stimulus would mean that the results from the two previous stimuli were discarded before resuming the series. Thus, the sequence of stimuli was always PC-T-T-PC-T-T-PC and so on, until all the stimuli to be tested were presented. Among the test stimuli there were always blank stimuli in which no sound was presented (NC); these represented a control for possible responses in the absence of sound stimuli and the number of these stimuli equalled the number of intensities tested (e.g. if the stimuli were tested at two different intensities, two NC would be randomly positioned among the T). The positive and negative control responses are not presented in the Results section. They were used to evaluate the motivation of each animal during a test series and not for statistical comparisons with the test stimuli. Animals that did not respond to the PC within 40 s or that responded to the NC within 120 s were not used for analysis.
Stimulus design
Five behavioural experiments were designed to investigate specific
questions related to song discrimination by C. barbara males.
Experiment 1
Are C. barbara males able to discriminate the conspecific song
from the calling songs of other sympatric cicada species? Males were presented
with four test stimuli, consisting of the calling songs of C. barbara,
Tibicina quadrisignata (Hagen), Tettigetta argentata (Olivier)
and Cicada orni L. (Fig.
2). To avoid pseudoreplication problems
(Kroodsma, 1989;
McGregor et al., 1992
),
recordings from four different animals of each species were used. The calling
songs were presented at 70 and 90 dB SPL.
|
Experiment 2
Is song discrimination affected by manipulation of the gross temporal
pattern? The gross temporal pattern of the songs of C. barbara and
C. orni (sympatric and closely related species) were modified while
retaining the characteristic frequency spectrum. The continuous trill of
C. barbara was modified into a train of sound pulses by inserting 120
ms pauses every 64 ms. Pauses of 40-120 ms are found in natural C.
orni calling songs. C. orni song was modified by removing the
pauses between echemes, resulting in a continuous trill signal. Natural
conspecific songs were also used in this experiment to compare the
attractiveness of the modified songs. All stimuli were presented at 70 and 90
dB SPL.
Experiments 3 and 4
Which parameters of the temporal pattern are used by C. barbara
males to discriminate their song from the song of the sister species C.
orni? These experiments were designed to investigate the effect of
varying the sound pulse duration, pause duration and the duty cycle (i.e.
pulse duration/pulse period). In experiment 3, the pause was kept constant at
30 ms while the pulse duration was varied between 30 and 240 ms. In a second
variant of experiment 3, the pause was set to 15 ms while the pulse duration
varied between 15 and 180 ms. By contrast, in experiment 4 the pulse duration
was set at 60 ms, whilst the pause varied between 7.5 and 120 ms. This range
was selected to include pauses that were shorter (7.5 and 15 ms), similar (30
and 60 ms) and larger (120 ms) than the average pause found in most C.
orni songs. The test stimuli were presented at 80 dB SPL in both
experiments.
Experiment 5
Can differences in frequency spectrum be used to improve song
discrimination between two trilled songs? C. barbara males were
presented with six pure-frequency tones (3, 4, 6, 9, 12 and 15 kHz) and the
conspecific calling song. This experiment also allowed us to investigate
frequency discrimination. All test stimuli were presented at 80 dB SPL.
Auditory nerve recordings
Seven cicada males, wings and legs removed, were waxed to a holder by their
pro- and mesonotum with the ventral side facing upwards. The auditory nerves
were exposed by ventral dissection and the preparation was kept moist with
insect Ringer. Each auditory nerve was recorded with a single
Vaseline-insulated tungsten hook. Computer-generated sound stimuli (100 kHz
conversion rate, 12 bit resolution) were delivered at the ipsilateral side as
pure-tone sound pulses (25 ms duration, 5 ms ramps, frequency range 0.5-25
kHz) by a Dynaudio D28/2 loudspeaker. The sound stimulus amplitude was
conditioned by two serially connected computer controlled attenuators. One
allowed compensation for the frequency response of the loudspeaker and the
other delivered the signal in 5 dB steps ranging from 30 to 90 dB SPL
(±0.5 dB). For each frequency and intensity, five stimuli were
presented. A microphone B&K 4135 calibrated with a piston phone (B&K
4220) and placed at the position later occupied by the cicada (22 cm from the
loudspeaker) allowed for adjustments in stimulus intensity and echo control.
The echoes were minimised by lining the Faraday cage and the apparatus close
to the preparation with sound-absorbing material (illsonic).
Stimulus and nerve activity were stored in a DAT tape recorder (TEAC RD-120TE). Off-line analysis of digitised nerve recordings (10 kHz, Data translation DT 2821-F-8 di) was performed with purpose-designed software. For each male, the auditory nerve suprathreshold response was estimated as the average peak amplitude of the summed excitation of the auditory receptors for the five repetitions of each frequency and intensity.
Statistics
All behavioural experiments were conducted in a within-subjects
(repeated-measures) design, i.e. each animal was tested for all the
experimental conditions of a particular test series (see
Ferguson, 1981;
Schweigert, 1994
for details
of this experimental design). When data met the assumptions for inferential
statistics, a one-way or two-way within-subjects analysis of variance (ANOVA)
was performed. Data that could not meet these assumptions were log-transformed
before use in subsequent analysis. A posteriori comparisons of means
were performed using the Tukey HSD test; in this case, only the
P-level for the comparison is presented. In experiments with one
repeated-measures factor with only two levels, a related t-test was
used for statistical comparisons.
The average time taken by individuals to sing following sound stimulation, i.e. the response latency, is expressed as the mean±95 % confidence interval.
![]() |
Results |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Males were clearly able to discriminate the conspecific song (CS) from the calling signals of T. argentata and C. orni, as measured by the time taken to respond to these stimuli (Fig. 2A). Indeed, the CS elicited singing activity significantly faster than did both heterospecific songs (P<0.001, both comparisons). The calling song of T. quadrisignata, very similar in temporal pattern to that of C. barbara, proved as effective as the CS in promoting singing behaviour at both 70 and 90 dB SPL (P>0.05, both comparisons).
Thus, C. barbara males presented a consistent stereotyped behavioural response towards the CS that was statistically different from the behavioural responses towards the songs of two other sympatric cicada species, Cicada orni and T. argentata. This experiment also indicated that pulsed songs (T. argentata, C. orni) were less attractive than trilled songs (C. barbara, T. quadrisignata), suggesting a role of the temporal pattern in song discrimination.
Experiment 2: is song discrimination affected by manipulation of the
gross temporal pattern?
Four stimuli were used: two calling songs (C. barbara and C.
orni) and the same songs but with the gross temporal pattern manipulated
(C. barbara with pauses and C. orni without pauses).
The modified C. barbara song (with pauses) was significantly less attractive than the natural calling song (P<0.001). Moreover, the modified C. orni song (without pauses) proved as attractive as the C. barbara song (P>0.05, Fig. 3). Hence, manipulation of the gross temporal characteristics of C. barbara and C. orni songs significantly affected the attractiveness of both stimuli. Note that the frequency spectrum was not manipulated in either modified song.
|
Experiments 3 and 4: which parameters of the temporal pattern are
used by C. barbara males to discriminate their song from that of the
sister species C. orni?
Manipulation of the gross temporal pattern had a strong effect on song
discrimination. Hence, in the following experiments three parameters of the
temporal pattern (pulse duration, pause duration and duty cycle) were
manipulated and signal discrimination investigated.
In Experiment 3, a constant pause duration (30 ms) and variable pulse duration (30-240 ms) was used (Fig. 4A). No significant differences were observed between stimuli (F4,28=2.5, P>0.05). A stimulus in which a 30 ms pause alternated with a 30 ms sound pulse was as effective in stimulating singing activity as a stimulus with 30 ms pauses alternating with 240 ms pulses, although the duty cycle (DC) had increased from 50% to 89%. Hence, pulse duration and duty cycle do not seem to influence signal discrimination significantly. Similar results were obtained when using constant 15 ms pauses (F4,24=0.7, P>0.05).
|
In Experiment 4, constant pulse duration (60 ms) and variable pause
duration (7.5-120 ms) was used (Fig.
4B). Significant differences were found between stimuli as the
pause duration was varied (F4,16=44.9,
P<0.001). The efficiency of a stimulus with a 60 ms sound pulse
duration decreased significantly as the pause duration in the song approached
the range found in C. orni songs (40-120 ms). Experiment 3
demonstrated that both the duty cycle and the pulse duration were not
correlated with the response latency, suggesting that duty cycle variation is
unlikely to be responsible for the effects observed in Experiment 4. Rather,
C. barbara males respond preferentially to continuous songs or to
signals with short periodic pauses (15 ms).
The previous experiments demonstrate that C. barbara males
discriminate continuous trills from pulsed songs (if pulses 30 ms). Using
this temporal cue alone, however, is not sufficient to discriminate the
conspecific song from the songs of some sympatric species (e.g. Tibicina
quadrisignata, Fig. 2B).
Hence, we further investigated if differences in the frequency spectrum might
be used as a complementary cue for species discrimination.
Experiment 5: can differences in frequency spectrum be used to
improve song discrimination between two trilled songs?
Both C. barbara and T. quadrisignata songs are continuous
trills, but the former has a main frequency spectrum peak around 6 kHz whereas
the latter is centred around 9 kHz (Fig.
2B). Hence, spectrum differences might be used to help
discriminate between these signals. We investigated if (i) significant
differences in response could be observed between different frequencies and
(ii) if certain frequencies alone could be sufficient to elicit singing
behaviour as well as the conspecific song
(Fig. 5).
|
Significant differences in the response latency were observed between frequencies (F6, 78=24.2, P<0.001), with C. barbara males discriminating tones differing by 1-2 kHz (e.g. 3 versus 4 kHz, P<0.01; 4 versus 6 kHz, P<0.01). The most effective tones were 6 and 9 kHz, but males could not significantly discriminate between these stimuli (P>0.05). On the other hand, only the 6 kHz tone induced singing behaviour as rapidly as the conspecific song (P>0.05).
Thus, although C. barbara males responded better to some frequencies than to others, the small differences in the response latency between the 6 and 9 kHz tones indicate that these are unlikely to enhance song discrimination significantly between C. barbara and T. quadrisignata songs.
Auditory nerve recordings
C. barbara males were more stimulated to sing by some frequencies
than others. Importantly, the previous experiment also demonstrated that
cicadas were able to discriminate frequencies differing by only 1 kHz (e.g. 3
versus 4 kHz). To investigate if this discrimination could be
attributed to differences in overall excitation of the auditory system,
frequency-dependent excitation at the auditory nerve (AN) was measured in
seven males (Fig. 6). The
frequencies 3 kH and 4 kHz induced the largest but similar levels of AN
excitation at the three intensities tested. This demonstrated that the
frequency discrimination observed in the behavioural experiments between 3 and
4 kHz (Fig. 5) cannot be
explained by differences in overall auditory afferent excitation. Moreover,
although 6 kHz was the most effective tone in behavioural experiments
(Fig. 5), the AN excitation
induced by this frequency was lower than the excitation at 3 and 4 kHz, both
at 70 and 80 dB SPL. Above 8 kHz, AN excitation decreased even further.
|
![]() |
Discussion |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
We have demonstrated that specific manipulation of the gross temporal
pattern of the song significantly affected song discrimination. Indeed,
experiments in which pauses were introduced into the conspecific song revealed
that C. barbara males stopped responding when these pauses exceeded
30 ms (see Fig. 4B), a pause
approaching what can be found in the song of the closely related species
C. orni. Hence, the acoustic system of C. barbara clearly
uses the gross temporal song structure for long-range communication, a feature
common to other insects (molecrickets:
Ulagaraj and Walker, 1975;
crickets: Pollack and Hoy,
1979
; grasshoppers: von
Helversen and von Helversen, 1994
). Still, and unlike the present
findings, Doolan and Young
(1989
) reported that long-range
song recognition by tethered flying Cystosoma saundersii females was
not affected by gross manipulation of the song structure. A near ninefold
increase in the pause separating individual pulses had no significant effect
on female steering preferences. However, in the cicada Cystosoma
saundersii the frequency spectrum of the song could be used as a
sufficient cue for species recognition since, to our knowledge, there are no
other sympatric insect species using the same frequency channel (800 Hz).
Thus, evolutionary pressure to develop a long-range recognition system
sensitive to the temporal properties of the signal might not have
occurred.
On the other hand, for C. barbara the temporal pattern alone was
not sufficient for correct discrimination between all heterospecific sympatric
cicadas, since some also have continuous songs (e.g. T.
quadrisignata). We initially hypothesised that differences in the
frequency spectrum could enhance discrimination in such cases. Indeed, the
frequency content of a song was demonstrated to be important for species
recognition in various insect groups
(Popov et al., 1975;
Ulagaraj and Walker, 1975
;
Bailey et al., 1990
). However,
although the main spectral peaks of C. barbara and T.
quadrisignata differ by approximately 3 kHz, these differences were not
observed to enhance song discrimination significantly.
Thus, the song recognition system present in C. barbara males is
able to discriminate songs that differ significantly in the gross temporal
pattern. This clearly reflected the ability to discriminate stimuli on the
basis of the pause duration (Fig.
4B). A high-pass filter, possibly based on its temporal summation
properties, may be responsible for the discrimination ability described here
(Weber and Thorson, 1989;
Stumpner et al., 1991
;
von Helversen and von Helversen,
1994
). If present in females, such a recognition system would
allow for efficient behavioural discrimination between C. barbara and
C. orni males.
Frequency-dependent behaviour: preferential attraction for particular
frequencies due to the tuned auditory system or active choice based on fine
frequency analysis?
C. barbara males demonstrated a behavioural preference for
specific frequencies (Fig. 5).
This behaviour is thought to be possible in cicadas through at least two
mechanisms: (i) a tuned peripheral auditory system that allows only some
frequencies to excite the central nervous system (CNS)
(Daws et al., 1997) and (ii)
active choice based on fine frequency analysis in the CNS
(Fonseca et al., 2000
).
Daws et al. (1997) have
shown that female frequency-selective phonotaxis in the bladder cicada
Cystosoma saundersii was associated with the strength of the auditory
system's response to an acoustic signal. At a defined sound intensity,
frequencies that evoked a stronger auditory excitation were more attractive
than frequencies causing a weaker excitation. Hence, the attractiveness of a
particular sound frequency in C. saundersii reflected the tuning
curve of the auditory system, as obtained by auditory nerve recordings. A
similar mechanism has been suggested for other insect species
(Ulagaraj and Walker, 1975
;
Huber, 1983
;
Bailey et al., 1990
;
Pollack and El-Feghaly,
1993
).
In contrast, our results indicate that there is no correlation between the
behavioural response and auditory excitation in C. barbara males.
Indeed, the 3 and 4 kHz tones induced similar peripheral auditory responses
but a significantly different behaviour, as measured by the response latency
(Figs 5 and
6). In the same way, there was
a sevenfold difference in AN excitation between 4 and 12 kHz at 80 dB, but
both tones were similarly effective in the behavioural experiments. Thus, the
frequency-dependent behaviour observed in C. barbara males is not a
consequence of differential excitation of the tuned peripheral auditory system
(see also 3 versus 6 kHz, Figs
5 and
6). Rather, this behaviour
seems to involve fine frequency analysis in the central nervous system (CNS),
which has been physiologically demonstrated in another cicada species
(Tettigetta josei; Fonseca et al.,
2000). Indeed, frequencies that induced similar responses at the
auditory nerve were discriminated in behavioural experiments. Moreover, the
most attractive frequency was 6 kHz. This frequency corresponds to the main
spectral peak of the calling song but induces a weaker peripheral excitation
than other frequencies (e.g. 3 and 4 kHz). If the frequency information was
instead processed through an intensity-dependent system, as is believed to
occur in C. saundersii (Daws et
al., 1997
), C. barbara males would present a preference
for frequencies with a sound intensity well below the highest energy peak of
the song (3 kHz, -12 dB). This would result in a `behavioural mismatch' that
would be an important constraint for long-range communication. Interestingly,
males of Magicicada cassini presented a behavioural response to
pure-frequency tones (Simmons et al.,
1971
) that is not correlated with the auditory tuning curve, as
measured by the summed response of the receptors
(Huber et al., 1990
). Indeed,
despite having the majority of the receptor cells more excited at 2 kHz than
at 6 kHz, in behavioural experiments the males responded significantly better
to the tone corresponding to the spectral peak of the calling song (5-6 kHz).
This suggests that, as in C. barbara males, in M. cassini
the frequency-related behaviour involves a mechanism different from that
described for Cystosoma saundersii but similar to Cicada
barbara.
Several insect species have a fine frequency resolution in the peripheral
auditory system, with ears sensitive to a broad range of sound frequencies and
with different receptor cells encoding different frequencies
(Schildberger et al., 1989).
For instance, crickets have a tonotopic organisation of the auditory organ
with different fine-tuned receptor cells
(Oldfield et al., 1986
),
allowing a fine frequency discrimination at the periphery. However, the
resolution allowed by the insect ear is frequently reduced within the CNS. In
crickets, the frequency resolution at the periphery is pooled in the CNS
through two parallel channels, one centred at 5 kHz and used for acoustic
communication (Schildberger,
1994
) and the other a broad-band channel important for the
detection of echolocation calls of bats
(Nolen and Hoy, 1984
). Hence,
in cricket species only a categorical perception of frequencies seems to take
place in the brain (Wyttenbach et al.,
1996
).
Cicadas are also likely to have a high frequency resolution at the
periphery, with up to 2000 receptor cells in each ear. However, recently it
was demonstrated that a good frequency resolution is maintained in the CNS
(Fonseca et al., 2000). At
least eight ascending interneurons in Tettigetta josei are tuned to
different frequencies with Q10dB values similar to most lower
vertebrates (where Q is a measure of frequency tuning and can be derived from
a neuron's tuning curve; Q10dB corresponds to the quotient between
the frequency at which a neuron shows the lowest threshold and the bandwidth
at 10 dB above that threshold), providing that cicada with a capacity for fine
frequency resolution in the brain that is remarkably high for insects. Here,
we showed that individual C. barbara males can discriminate
frequencies that differ by 1-2 kHz (see 3-6 kHz,
Fig. 5). Thus, this behavioural
data similarly indicates that cicadas have fine representation of frequencies
in the CNS.
![]() |
Acknowledgments |
---|
![]() |
References |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Bailey, W.J., Cunningham, R.J. and Lebel, L. (1990). Song power, spectral distribution and female phonotaxis in the bushcricket Requena verticalis (Tettigoniidae: Orthoptera): active female choice or passive attraction. Anim. Behav. 40,33 -42.
Daws, A. G., Hennig, R. M. and Young, D. (1997). Phonotaxis in the cicadas Cystosoma saundersii and Cyclochila australasiae. Bioacoustics 7, 173-188.
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.
Ferguson, G. A. (1981). Statistical Analysis in Psychology and Education. McGraw-Hill, Japan.
Fonseca, P. J. (1994). Acoustic Communication in Cicadas (Homoptera, Cicadoidea): Sound Production and Sound Reception. PhD thesis, University of Lisbon.
Fonseca, P. J., Münch, D. and Hennig, R. M. (2000). How cicadas interpret acoustic signals. Nature 405,297 -298.[Medline]
Helversen, D. von and Helversen, O. von (1983). Species recognition and acoustic localisation in acridid grasshoppers: a behavioural approach. In Neuroethology and Behavioural Physiology (ed. F. Huber and H. Mark1), pp.95 -107. Heidelberg: Springer-Verlag.
Helversen, O. von and Helversen, D. von (1994). Forces driving coevolution of song and song recognition in grasshoppers. In Neural Basis of Behavioural Adaptations (ed. K. Schildberger and N. Elsner), pp. 253-284. New York: Gustav Fischer Verlag.
Hennig, R. M. and Weber, T. (1999). Pattern recognition in crickets (Teleogryllus). In Proceedings of the 1st Göttingen Conference of the German Neuroscience Society 1999, vol. 1 (ed. N. Elsner and U. Eysel), pp. 344. Stuttgart, New York: Georg Thieme Verlag.
Huber, F. (1983). Neural correlates of orthopteran and cicada phonotaxis. In Neuroethology and Behavioural Physiology (ed. F. Huber and H. Mark1), pp.108 -135. Heidelberg: Springer.
Huber, F., Kleindienst, H. U., Moore T. E., Schildberger, K. and Weber, T. (1990). Acoustic communication in periodical cicadas: neuronal responses to songs of sympatric species. In Sensory Systems and Communication in Arthropods (ed. F. G. Gribakin, K. Wiese and A. V. Popov), pp.217 -228. Basel: Birkhäuser Verlag.
Kroodsma, D. E. (1989). Suggested experimental designs for song playbacks. Anim. Behav. 37,600 -609.
McGregor, P. K., Catchpole, C. K., Dabelsteen, T., Falls, J. B., Fusani, L., Gerhardt, H. C., Gilbert, F., Horn, A. G., Klump, G. M., Kroodsma, D. E. et al. (1992). Design of playback experiments: the Thornbridge Hall Nato ARW consensus. In Playback and Studies of Animal Communication (ed. P. K. McGregor), pp.1 -9. New York: Plenum Press.
Nolen, T. G. and Hoy, R. R. (1984). Initiation of behaviour by single neurons: the role of behavioral context. Science 226,992 -994.[Medline]
Oldfield, B. P. (1980). Accuracy of orientation in female crickets, Teleogryllus oceanicus (Gryllidae): dependence on song spectrum. J. Comp. Physiol. A 141, 93-99.
Oldfield, B. P., Kleindienst, H. U. and Huber. F. (1986). Physiology and tonotopic organisation of auditory receptors in the cricket Gryllus bimaculatus DeGeer. J. Comp. Physiol. A 159,457 -464.[Medline]
Perdeck, A. C. (1957). The isolating value of specific song patterns in two sibling species of grasshoppers (Chorthippus brunneus Thunberg and Ch. biguttulus L.). Behaviour 12,1 -75.
Pollack, G. S. and Hoy, R. R. (1979). Temporal pattern as a cue for species-specific calling song recognition in crickets. Science 204,429 -432.
Pollack, G. S. and El-Feghaly, E. (1993). Calling song recognition in the cricket Teleogryllus oceanicus: comparison of the effects of stimulus intensity and sound spectrum on selectivity for temporal pattern. J. Comp. Physiol. A 171,759 -765.
Popov, A. V., Shuvalov, V. F., Svetlogorskaya, I. D. and Markovich, A. M. (1974). Acoustic behavior and auditory system in insects. In Mechanoreception (ed. J. Schwartzkopff), pp. 281-306. Opladen: Westdentscher Verlag.
Popov, A. V., Shuvalov, V. F. and Markovich, A. M. (1975). The spectrum of the calling song signals, phonotaxis, and the auditory system in the cricket Gryllus bimaculatus. J. Evol. Biochem. Physiol. 11,398 -404.
Popov, A. V. and Shuvalov, V. F. (1977). Phonotactic behaviour of crickets. J. Comp. Physiol. A 119,111 -126.
Schildberger, K., Huber, F. and Wohlers, D. W. (1989). Central Auditory Pathway: Neuronal Correlates of Phonotactic Behavior. In Cricket Behaviour and Neurobiology (ed. F. Huber, T. Moore and W. Loher), pp.423 -458. Ithaca, London: Cornell University Press.
Schildberger, K. (1994). The auditory pathway of crickets: Adaptations for intraspecific acoustic communication. In Neural Basis of Behavioural Adaptations (ed. K. Schildberger and N. Elsner), pp. 209-225. New York: Gustav Fischer Verlag.
Schweigert, W. A. (1994). Research Methods and Statistics for Psychology. California: Brooks/Cole.
Simmons, J. A., Wever, E. G. and Pylka, J. M. (1971). Periodical cicada: sound production and hearing. Science 171,212 -213.[Medline]
Skovmand, O. and Pedersen, S. B. (1983). Song recognition and song pattern in a shorthorned grasshopper. J. Comp. Physiol. A 153,393 -401.
Stumpner, A., Ronacher, B. and Helversen, O. von (1991). Auditory interneurons in the metathoracic ganglion of the grasshopper Chorthippus biguttulus. II Processing of temporal patterns of the song of the male. J. Exp. Biol. 158,411 -430.
Stumpner, A. and Helversen, O. von (1994). Song production and song recognition in a group of sibling grasshopper species (Chortippus dorsatus, Ch. dichrous and Ch. loratus: Orthoptera, Acrididae). Bioacoustics 6, 1-23.
Ulagaraj, S. M. and Walker, T. J. (1975). Response of flying mole crickets to three parameters of synthetic songs broadcast outdoors. Nature 253,530 -532.
Villet, M. (1992). Responses of free-living cicadas (Homoptera: Cicadidae) to broadcasts of cicada songs. J. ent. Soc. Sth. Afr. 55,93 -97.
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.
Weber, T. and Thorson, J. (1989). Phonotactic behaviour of walking crickets. In Cricket Behaviour and Neurobiology (ed. F. Huber, T. Moore and W. Loher), pp.310 -339. Ithaca: Cornell University Press.
Wyttenbach, R. A., May, M. L. and Hoy, R. R. (1996). Categorical perception of sound frequency by crickets. Science 273,1542 -1544.[Abstract]
Related articles in JEB: