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Behavioral Ecology Vol. 12 No. 3: 308-312
© 2001 International Society for Behavioral Ecology
Bidirectional communication system in katydids: the effect on chorus structure
Department of Cell and Animal Biology, The Hebrew University of Jerusalem, Israel
Address correspondence to E. Tauber, who is now at the Department of Genetics, University of Leicester, University Road, Leicester LE1 7RH, UK. E-mail: et22{at}leicester.ac.uk .
Received 3 July 2000; revised 5 September 2000; accepted 5 September 2000.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Unlike most acoustic systems evolved for pair formation where only males signal, the katydidPhaneroptera nana has a bidirectional communication system where both males and females sing. Despite extensive study on male chorusing behavior in different communication systems, this behavior has rarely been explored in duetting species. I examined how this bidirectional communication system affects the collective pattern of male signaling.P. nana males alternate their songs, and in response to synthetic stimuli delay their calls, according to the phase of stimulation. Pairs of synthetic calls (simulating alternating males) presented to females elicited equal female response, as long as the intercall interval was
200
ms. Thus, male alternation is imposed by the female's responsiveness and may
be interpreted as a "jamming avoidance reaction." Further evidence
suggests that chorus structure is not merely constrained by the female sensory
temporal resolution, but rather is adaptively related to female choice in this
species. Key words: acoustic communication, chorusing, female choice, katydids, male signaling, Phaneroptera nana.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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In many mating communication systems, the senders, usually the males, coordinate their signals. This mass signaling, or chorusing behavior, may take the form of synchronization or alternation (anurans: Gerhardt, 1994
; insects:
Greenfield, 1994). Different
models have been suggested for the evolutionary function of chorusing
behavior. Synchrony may be important for species recognition in cases where
the rate of producing the signal (i.e., the period length) is the character
recognized by the female (Greenfield,
1994), may increase the total attractiveness of the joint signal
by many males (the beacon model; Buck and
Buck, 1978), or may confuse potential predators
(Tuttle and Ryan, 1982).
Conversely, alternation may have evolved either to maximize the transmitting
time of the group (i.e., the collective duty cycle) or to preserve components
of the signal, which are important for female recognition
(Schwartz, 1987). All these
models assume a cooperative function of the chorusing behavior (i.e., a group
advantage).
Recently, it has been suggested that synchrony is an epiphenomenon,
resulting from male competition
(Greenfield and Roizen, 1993;
Snedden and Greenfield, 1998).
In these studies, calling males modulated their rhythm in order to time their
signal slightly ahead of their neighbors' calls. It was shown that females
preferred leading calls, and this behavior was related to the
"precedence effect": a sensory bias in female perception
(Wyttenbach and Hoy, 1993).
Synchrony was shown to be an evolutionarily stable strategy (ESS) for
competing males that have similar calling rates
(Greenfield and Roizen, 1993),
and the same mechanism was also used to explain male alternation.
In contrast to the more common pattern in which mute females approach
calling males, both the male and the female sing in phaneropterine katydid
(Orthoptera: Tettigoniidae) (reviewed by
Heller, 1990). In the present
study I used the bidirectional communication system of Phaneroptera
nana, a common Mediterranean katydid, to explore interactions between
male signals. P. nana males produce approximately 50-ms calls
(chirps), consisting of 2-11 pulses, at approximately 700-ms call period
(Tauber and Cohen, 1997;
Tauber et al., manuscript submitted). Receptive females respond with a short
latency (
60 ms), short duration "click." Studies in other
phaneropterine katydids indicated that the female response had to occur during
a precise interval following the end of the male's call; responses falling
within this interval result in male phonotaxis toward the female
(Dobler et al., 1994;
Heller and von Helversen,
1986; Robinson et al.,
1986; Zimmermann et al.,
1989). I examined how the role reversal and the female
phonoresponse affect the chorus structure in this communication system.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Animals
To study the spatial distribution of P. nana males in the field, I measured the nearest neighbor distances in eight different locations around Jerusalem during July-September 1997 and October 1998. Males were found mostly on Plumbago capensis bushes, singing during evening hours from perches on the upper branches of the vegetation. Singing males were first located using red illumination, and the position of each male was then marked and the insect collected. I measured the horizontal distance between the neighbors. As singing males were found on the upper layer of the vegetation, their spatial distribution was approximately horizontal and two dimensional. I measured the area of each location (i.e., the area of the vegetation patch) and calculated the density of the males in that region.
For playback experiments, I used insects from a laboratory colony established in 1995 from insects collected at three different localities in Jerusalem. The insects were kept under a 12 h light: 12 h dark photoperiod and at 31°C and 27°C during photophase and scotophase, respectively. The insects were fed on fresh plants (P. capensis) and flaked oats. After the final moult, males and females were kept in two acoustically isolated rooms to prevent mating and to eliminate habituation to the calls of the opposite sex.
Recording and playback experiments
To record signal interaction between the males, I recorded in the
laboratory the calls of five pairs of singing males. Recordings were made in a
sound-proof anechoic chamber (0.6 x 0.4 x 0.3 m) at 27 ±
1°C, under dimmed illumination, during the dark hours. Each male of a pair
was placed into a cylindrical, wire-mesh cage (4 cm diam, 3 cm height), 0.5 m
away from the other. The males were recorded on separate channels, using
Linear-X microphones (model M53, ± 1 dB from 10 Hz-40 kHz), fed to a
Neurocorder (Neuro Data KD-484, up to 44,000 samples/s). Recordings were later
fed to the computer and analyzed using Computerscope software (RC Electronics,
Santa Barbara, California). The timing of a male's call during his neighbor's
cycle was expressed as a phase angle (e.g., complete synchrony = 0 degrees). I
used circular statistics (Batschelet,
1981) to calculate the mean vector and confidence intervals and
used Rayleigh's uniformity test to analyze the distributions of the phase
data.
I tested the response of a singing individual male to his neighbor's call
using synthetic calls produced by the computer. Signals were synthesized using
CoolEdit software (Syntrillium Corp., Phoenix, Arizona) and were transmitted
by a 16-bit sound card (Creative Labs, Inc., model CT2940) installed on a PC.
The synthetic song was made according to the population mean value of each of
the song characters: six pulses of 0.5 ms duration each and a 15-ms gap
between the pulses (Tauber and Pener,
2000). The output was sent to the loudspeaker (Utah Electronics,
model H208 tweeter horn) located 15 cm from the male, via a Revox amplifier
(model 39). Sound pressure levels (SPLs) of the synthetic calls were measured
with a Brüel & Kjaer model 2203 SPL meter
(PEAK setting) fitted with a model 1613 octave filter centered on 16 kHz.
Precise values of absolute SPL of the extremely short P. nana calls
were obtained by calibrating oscilloscope readings of call peak amplitudes
with peak equivalents of 16 kHz continuous sound. Output SPL was 55 dB (0 dB =
20 µPa) at the location of the insect. I recorded the playback stimuli and
male response calls separately and analyzed them as described above. The
synthetic stimuli were presented to each of the singing males in random
intervals, and the actual phase of each stimulus was measured after completion
of the experiments (see below).
To study whether the stimuli affect the rhythm of a calling male, I plotted
phase response curves (PRC; see Sismondo,
1990). For each stimulus I measured the call period (CP), defined
as the interval between two consecutive call onsets, before and immediately
after the stimulus presentation. The prestimulus CP (CP'), defined by
the last cycle before stimulus presentation, served as a reference. The
stimulus phase was calculated as the stimulus delay from the last male's call,
divided by CP'. I calculated the response phase as the change in the CP
during stimulation, divided by CP' (see
Fig. 3 for further
explanation).
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To explore female response to males' signals at various interchirp intervals (ICI), I recorded the acoustic response of females under the same experimental design described above. Pairs of synthetic male calls were repeatedly played at a 1.4/s repetition rate. The ICI was varied to obtain different phase relations between the two songs. The response of each of seven females was tested using ICI of 80, 100, and 200 ms. The playback of the synthetic calls, and the recording of the female response were as described above. The latency of each female's response from the onset of each of the two synthetic call stimuli was measured, and peristimulus histograms were plotted.
In a different set of experiments, I tested the female response toward long
trains of calls (>2 s). Each of seven females was presented with a
synthetic song that was constructed of effective pulse duration (0.5 ms) and
interpulse intervals (15 ms; Tauber and
Pener, 2000). This long stimulus simulated males calling one right
after the other, without delaying their call. The playback of the synthetic
calls and the recording of the female response were as described above.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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P. nana males sing for 6-8 h starting at dusk from their perches. There were 4-10 singing males in each location, depending on the size of the vegetation patch (mean ± SD 7.5 ± 0.9 per 7-12 m2). Figure 1 presents the nearest-neighbor distance distribution. The mean distance was 1.57 ± 0.96 m (mean ± SD, n = 52), and the range was 0.34-4.63 m. These observations indicated that male spacing in the field allows for song detection of (nearest) neighbors in P. nana (for auditory thresholds see Tauber and Pener, 2000
).
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Recordings of pairs of P. nana males showed that males tend to
alternate their calls with those of their neighbors and that their calls
rarely overlap (Figure 2). The
phase angle between the calls was 182.50° ± 7.81° (grand mean
vector ± circular SE). The 95% confidence intervals were
167.18°-197.80°. The distribution of the phase angles was not uniform,
and a Rayleigh test (Batschelet,
1981) indicated significant evidence for a preferred phase angle
in each of the five pairs of males that was tested (Rayleigh test, p
<.05 in all five tests).
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The playback experiments, in which the free-run calling of individual males
was perturbed by a single synthetic call
(Figure 3A), showed that males
presumably modulate their rhythm to control the phase between their own and
their neighbors' calls. The phase response curve
(Figure 3B) showed that P.
nana males responded to the stimulus by a transient change of the CP, and
this change depended on the stimulus phase. Although there was scatter in
males' response, the slope of the linear regression was significantly
different from zero in each of the tested males (n = 12 males,
p <.05 in all tests). The average regression slope across males
was also significant different from zero (one-sample t test,
t = 4.35, p <.01). The slope of the linear regression was
consistent with the observed alternation and is comparable to other
alternating-call insects (Greenfield,
1994).
Figure 4 shows the female's response to pairs of synthetic songs simulating calls of alternating males. When the interchirp interval (ICI) was 80 ms, females respond with one click to the leading synthetic song. When an ICI of 100 ms was presented, females responded with the same latency as before, but occasionally emitted an additional click, presumably directed toward the second (following) synthetic call. When the interval between the leading and the following calls was extended to 200 ms, all females equally responded to both calls. The effect of extending the ICI on the female response toward the second call was highly significant (Friedman statistic: 11.57, n = 7 females, p <.001). In two additional cases, females emitted only one response, which according to its long latency, was presumably directed to the second stimulus.
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Figure 5 shows a female
response to long trains of calls that were constructed of effective pulse
duration and interpulse intervals (Tauber
and Pener, 2000). The female responded during the onset of the
song and then was silent as long as the stimulus continued. When 100-ms pauses
were introduced, the female emitted an additional response during the onset of
the next synthetic call. Similar results were observed in six additional
females. Thus, females are actively inhibited during the on-going sound.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Bidirectional communication systems where both sexes call, producing a duet, have been evolved in different groups of animals. In insects, duetting functions mainly for localization (e.g., Heller, 1990
) and possibly for
mate selection (see Greenfield and Roizen,
1993). In birds and primates duetting is mostly a postmating
behavior, serving functions such as territorial defense and strengthening the
pair bond (e.g., Geissmann,
1999; Langmore,
1998).
Chorusing behavior, where males coordinated their calls, was extensively
studied in different phylogenetic groups; however, it has rarely been explored
in duetting species (but see Galliart and
Shaw, 1991; Bailey and Field,
2000). The duetting in P. nana involves a role reversal:
females signal their mate choice with an acoustic response, and males will
approach the female if they receive a female answer within a defined,
species-specific time window after their call
(Dobler et al., 1994;
Heller and Helversen, 1986;
Robinson et al., 1986;
Zimmermann et al., 1989).
These characteristics of this bidirectional communication system have a unique
effect on the structure of males' chorus.
The results of the present study indicate that P. nana males
modulate their rhythm in response to the call of other males (Figures
2 and
3). This implies that P.
nana males perceive and process two different auditory inputs, which
result in two different behavioral responses: (1) female calls initiate
phonotaxis of the male toward the female (Tauber et al., manuscript
submitted), and (2) conspecific-male call, which induces a call delay. Because
the signals of the male and the female differ both in the frequency domain and
in the temporal structure (Tauber and
Pener, 2000), both types of call characters may be used by the
sensory system of the males to differentiate between conspecific males and
females.
P. nana females do not answer males' calls that are too closely
spaced ( 200 ms; Figure 4).
Thus, P. nana males have to delay their call at least 200 ms after
their neighbor's call to ensure a female response to their own call. This
minimal delay, which is less than half of the call period, leads to sequential
calling (alternation, in case of n = 2) of several neighboring males.
The synthetic calls in the playback experiments were emitted from the same
direction (speaker) and at the same intensity. This represents a highly
simplified simulation. In the field, females are exposed to calls coming from
different directions and at different intensities, which may result in a
different temporal resolution of the female (cf.
Römer and
Krusch, 2000). Still, the results indicate that the chorus
structure of the male relates to the female's responsiveness.
The minimal interval between males' calls, imposed by the timing of the
responses of the females, is not merely a result of a sensory constraint
(e.g., a refractory period in the female's neural circuitry or a physiological
fatigue). This was demonstrated by presenting a long train of acceptable
pulses and gaps (Figure 5), simulating multiple males calling one after the other. Females did not respond
even for trains longer than 5 s. A silent pause of > 100 ms was necessary
to reinitiate female response. Thus, females are actively inhibited by the
on-going sound. What is the function of this inhibition? A previous study in
P. nana (Tauber and Cohen,
1997; Tauber et al., manuscript submitted) demonstrated a female
choice: females preferred to answer specific males and ignored others.
Nonpreferred males apparently do not approach the female. The alternating
pattern of the calls of the males, reported here, allows the females to direct
their response toward a specific, preferred male. In the analogous signaling
system in fireflies, the males engaged in synchrony (reviewed by
Buck, 1988). While female
choice may exist in some species (Branham
and Greenfield, 1996), male synchrony may prevent it in practice,
and invite various forms of interloping of neighboring males
(Buck, 1988).
In the more common communication systems in insects or anurans (i.e.,
females approach a calling male), the best strategy for a male is to time his
call slightly before his neighbors (e.g.,
Greenfield and Roizen, 1993).
In this way, males enhance their own call and mask the following males;
masking is achieved either directly, by overlapping the "tail" of
their chirp with that of their neighbors, or indirectly, through the
precedence effect affecting the female sensory system. In the communication
system of P. nana, this strategy is apparently not adaptive. The male
has to terminate his call before the call of his neighbors, since the female
response has to be received by the male in a defined time window
(Heller, 1990). Thus,
alternation in this bidirectional communication system ensures that calling
males will be detected by the females and female response will be detected by
the males.
A recent study in another phaneropterine katydid,Elephantodeta
nobilis (Bailey and Field,
2000), indicates a different type of acoustic interaction between
males. In E. nobilis, noncalling males often use satellite tactics,
inserting a short call within the alpha male's chirp, to attract the female.
Interestingly, E. nobilis also differ from P. nana in their
phonotaxis pattern; the task of searching and approaching inE.
nobilis is carried out by the females. Because E. nobilis males
are stationary, they do not need to detect the female answer. This, in turn,
may have allowed for these acoustic satellite interactions to evolve.
In contrast to synchrony, the number of alternating males in a chorus is
limited. The species call period (CP) and call duration (CD) present an upper
limit to the number of males that can effectively alternate with each other
(approximately CP/CD). In P. nana, with CP about 700 ms, CD about 70
ms, the intercall interval of 200, imposed by the female, sets an upper
limit for the number of males that can effectively alternate with each other
(i.e., 2-3 males). Because males usually aggregate in higher numbers, males
probably interact with their closest neighbors and ignore others. This kind of
selective attention was reported both in anurans
(Narins, 1992) and in insects
(Snedden et al., 1998;
Römer and
Krusch, 2000).
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ACKNOWLEDGEMENTS |
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I am grateful to D. Cohen, M. P. Pener, T. Keasar, and D. Eberl for comments on the manuscript and to M. D. Greenfield for discussions and helpful advice during this study. This study was supported by the Charles E. Smith Family Laboratory for Collaborative Research in Psychobiology, The Hebrew University of Jerusalem.
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REFERENCES |
|---|
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
|---|
Bailey WJ, Field G, 2000. Acoustic satellite behaviour in the Australian bushcricket Elephantodeta nobilis (Phaneropterinae, Tettigoniidae, Orthoptera) Anim Behav 59: 361-369.[ISI][Medline]
Batschelet E, 1981. Circular statistics in biology. London: Academic Press.
Branham MA, Greenfield MD, 1996. Flashing males win mate success. Nature 381: 745-746.[Medline]
Buck J, 1988. Synchronous rhythmic flashing of fireflies II. Q Rev Biol 63: 265-289.[Medline]
Buck J, Buck E, 1978. Toward a functional interpretation of synchronous flashing by fireflies. Am Nat 112: 471-492.
Dobler S, Heller K-G, von Helversen O, 1994. Song pattern recognition and an auditory time window in the female bushcricket Ancistrura nigrovittata (Orthoptera: Phaneropteridae). J Comp Physiol A 175: 67-74.
Galliart PL, Shaw KC, 1991. Effect of intermale distance and female presence on the nature of chorusing by paired Amblycorypha parvipennis (Orhtoptera: Tettigoniidae). Fla Entomol 74: 559-569.
Geissmann T, 1999. Duet songs of the siamang, Hylobates syndactylus: II. Testing the pair-bonding hypothesis during a partner exchange. Behaviour 136: 1005-1039.
Gerhardt HC, 1994. The evolution of vocalization in frogs and toads. Annu Rev Ecol Syst 25: 293-324.[ISI]
Greenfield MD, 1994. Synchronous and alternating choruses in insects and anurans: common mechanisms and diverse functions. Am Zool 34: 605-615.
Greenfield MD, Roizen I, 1993. Katydid synchronous chorusing is an evolutionarily stable outcome of female choice. Nature 364: 618-620.
Heller K-G, 1990. Evolution of song pattern in East Mediterranean Phaneropterinae: constraints by the communication system. In: The Tettigoniidae (Bailey WJ, Rentz DCF, eds). Bathurst, Australia: Crawford House Press; 130-151.
Heller K-G, von Helversen D, 1986. Acoustic communication in phaneropterid bushcrickets: species-specific delay of female stridulatory response and matching male sensory time window. Behav Ecol Sociobiol 18: 189-198.
Langmore NE, 1998. Functions of duet and solo songs of female birds. Trends Ecol Evol 13: 136-140.
Narins MP, 1992. Evolution of anuran chorus behavior: neural and behavioral constraints. Am Nat 139: S90-S104.
Robinson D, Rheinlaender J, Hartley JC, 1986. Temporal parameters of male-female sound communication in Leptophyes punctatissima. Physiol Entomol 11: 317-323.
Römer H, Krusch M, 2000. A gain-control mechanism for processing of chorus sounds in the afferent auditory pathway of the bushcricket Tettigonia viridissima (Orthoptera; Tettigoniidae). J Comp Physiol A 186: 181-191.[Medline]
Schwartz JJ, 1987. The function of call alternation in anuran amphibians: a test of three hypotheses. Evolution 41: 461-471.
Sismondo E, 1990. Synchronous, alternating, and
phase-locked stridulation by a tropical katydid. Science
249: 55-58.
Snedden WA, Greenfield MD, 1998. Females prefer leading males: relative call timing and sexual selection in katydid chorus. Anim Behav 56: 1091-1098.[ISI][Medline]
Snedden WA, Greenfield MD, Jang Y, 1998. Mechanisms of selective attention in grasshoppers choruses: who listens to whom? Behav Ecol Sociobiol 43: 59-66.
Tauber E, Cohen D, 1997. Acoustic communication and duet singing in the bush cricket Phaneroptera nana. [abstract] Isr J Zool 43: 117-118.
Tauber E, Pener MP, 2000. Song recognition in female bushcrickets Phaneroptera nana. J Exp Biol 203: 597-603.[Abstract]
Tuttle MD, Ryan MJ, 1982. The role of synchronized calling, ambient light, and ambient noise, in anti-bat-predator behavior of a tree frog. Behav Ecol Sociobiol 11: 125-131.
Wyttenbach RA, Hoy RR, 1993. Demonstration of the precedence effect in an insect. J Acoust Soc Am 94: 777-784.[ISI][Medline]
Zimmermann U, Rheinlaender J, Robinson D, 1989. Cues for male phonotaxis in the duetting bushcricket Leptophyes punctatissima. J Comp Physiol A 164: 621-628.
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