Acoustic pattern recognition in a grasshopper: processing in the time or frequency domain?

Males of the grasshopper Chorthippus biguttulus produce songs which consist of the stereotyped and rhythmic iteration of a sound unit (termed syllable) separated by distinct syllable pauses. Virgin females respond to this signal, and to similar artificial signals, with song phrases of their own. In behavioural experiments the response probability of virgin females can be measured with artificial acoustic stimuli. The stimuli consisted of an amplitude modulated noise the envelope of which was altered. We investigated several hypotheses on the mechanisms of conspecific song recognition with special emphasis on the question whether recognition occurs in the frequency domain or in the time domain. (1) Females of Ch. biguttulus required only the first five Fourier components of the envelope function (corresponding to 50 Hz for a fundamental frequency of 10 Hz) to detect the syllable/pause structure. In addition, they detected small gaps within syllables if the signal contained at least ca. 15 Fourier components (corresponding to a frequency of 150 Hz). Further experiments showed that the correct phase information of the Fourier components is necessary for recognition, indicating that pattern recognition is not achieved merely on the basis of band pass filtering. (2) A cross correlation between the signal and an assumed internal template yields only inconsistent predictions of the response probabilities. (3) The recognizer system probably works in the time domain, possibly by direct comparison of adjacent syllable and pause durations. It is not yet clear whether the duration of a syllable is evaluated with respect to the preceding or succeeding pause. We emphasize that the neural recognizer of the grasshopper does not only examine a signal for its similarity to an internal template, but that it also takes into account features that indicate an incorrect signal. This may be a general feature of neuronal pattern recognition systems which have been shaped by natural selection. Received: 4 October 1997 / Accepted in revised form: 26 August 1998     

Song recognition by temporal cues in a group of closely related bushcricket species (genus Tettigonia)

Female phonotaxis of Tettigonia viridissima and T. caudata was investigated on a walking compensator to determine the temporal parameters of the male song used for song recognition, and to compare them with the previously described pulse rate filtering of T. cantans. The T. cantans song is continuous with a ≈30-Hz pulse rate. The T. caudata song has a higher pulse rate (≈40 Hz) and duty cycle than T. cantans and a distinct verse structure. The T. viridissima song is continuous with a double-pulse pattern. While the pulse rate is essential for song recognition in T. cantans, neither pulse rate not verse structure were essential for song recognition in T. caudata: females responded to signals above a minimum duty cycle. T. viridissima females did not require the double-pulse structure, but a single long pulse, equivalent to the duration of the double pulses and interval between them, was effective. Song attractiveness was limited by a minimum duration of the merged double pulse, and by minimum and maximum duration of the interval between them. Pulse rate recognition had little if any importance in either of the species investigated. Thus, the three congeners use different mechanisms for temporal song recognition. Accepted: 18 June 1998     

Acoustic preference functions and sexual selection on the male calling song in the grasshopper Chorthippus biguttulus

Male courtship songs have two functions in species recognition and intraspecific mate choice. Female preference might thus exert different types of selection pressure on male song traits. We used a combination of acoustic mate choice experiments and statistical analyses to examine how traits of the calling songs of male nightingale grasshoppers,Chorthippus biguttulus , are influenced by different sexual selection pressures. We recorded calling songs of males and tested their attractiveness to females in acoustic mate choice experiments. The attractiveness values were a good estimate of the potential male mating success. In experiments with a pair of males, females copulated significantly more often with the male that had the higher attractiveness value. To detect directional, stabilizing, disruptive or correlative selection acting on male song properties we used linear and nonlinear regressions between male song traits and female response behaviour. Three signal traits were revealed to be under directional selection: song loudness, pause to syllable ratio and the mean duration of gaps within syllables. A nonlinear regression testing for correlative selection showed that a fourth song trait, rhythm, in combination with mean gap duration was also important for female mate choice. With these traits and trait combinations we were able to explain 42% of the variance in attractiveness between males. Since we found no evidence for stabilizing selection, but ample evidence for directional selection, we conclude that selection on the traits examined is related to mate choice mainly in the context of intraspecific sexual selection and probably less so in species recognition. Copyright 2003 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.      

Influence of different envelope maskers on signal recognition and neuronal representation in the auditory system of a grasshopper

Background

Animals that communicate by sound face the problem that the signals arriving at the receiver often are degraded and masked by noise. Frequency filters in the receiver''s auditory system may improve the signal-to-noise ratio (SNR) by excluding parts of the spectrum which are not occupied by the species-specific signals. This solution, however, is hardly amenable to species that produce broad band signals or have ears with broad frequency tuning. In mammals auditory filters exist that work in the temporal domain of amplitude modulations (AM). Do insects also use this type of filtering?

Principal Findings

Combining behavioural and neurophysiological experiments we investigated whether AM filters may improve the recognition of masked communication signals in grasshoppers. The AM pattern of the sound, its envelope, is crucial for signal recognition in these animals. We degraded the species-specific song by adding random fluctuations to its envelope. Six noise bands were used that differed in their overlap with the spectral content of the song envelope. If AM filters contribute to reduced masking, signal recognition should depend on the degree of overlap between the song envelope spectrum and the noise spectra. Contrary to this prediction, the resistance against signal degradation was the same for five of six masker bands. Most remarkably, the band with the strongest frequency overlap to the natural song envelope (0–100 Hz) impaired acceptance of degraded signals the least. To assess the noise filter capacities of single auditory neurons, the changes of spike trains as a function of the masking level were assessed. Increasing levels of signal degradation in different frequency bands led to similar changes in the spike trains in most neurones.

Conclusions

There is no indication that auditory neurones of grasshoppers are specialized to improve the SNR with respect to the pattern of amplitude modulations.     

Recognition of sex in the acoustic communication of the grasshopper Chorthippus biguttulus (Orthoptera, Acrididae)

Many gomphocerine grasshoppers communicate acoustically: a male's calling song is answered by a female which is approached phonotactically by the male. Signals and recognition mechanisms were investigated in Chorthippus biguttulus with regard to the cues which allow sex discrimination. (1) The stridulatory files on the hindfemur of both sexes are homologous in that they are derived from the same row of bristles, but convergent with respect to the “pegs”. In males the pegs are derived from the bristles, and in females from the wall of the bristle's cup. (2) Male and female songs are generated by similar, probably homologous motor programs, but differ in the duration, intensity, “gappyness” of syllables, risetime of pulses, and the frequency spectra. The hindleg co-ordination during stridulation and the resulting temporal song patterns are less variable in males than in females. (3) For both sexes, recognition of a mate's signal depends on species-specific syllable structure. For males it is essential that the female syllables consist of distinct short pulses, whereas females reject “gappy” syllables. Males strongly prefer “ramped” pulses, females respond to syllables irrespective of steeply or slowly rising ramps. Males react only to the low-frequency component, whereas females prefer spectra containing both, low and high frequency components. Accepted: 20 November 1996     

Sound is involved in multimodal communication of Loxosceles intermedia Mello-Leitão, 1934 (Araneae; Sicariidae)

Signals of different modalities are involved during courtship of the brown spider Loxosceles intermedia. A spine on the pedipalp is rubbed against the grooves on the retrolateral region of the chelicerae producing stridulatory signals, which have a dominant frequency of the airborne component range around 770 Hz for females and around 170 Hz for males. These values are significantly lower for the substrate-borne component. The sound pressure level of stridulatory signals lies below 50 dB and the velocity values below 1 mm/s. The copulation frequency does not depend on the presence of pedipalps in females; however, in males the removal of pedipalps decreases the courtship frequency. During courtship, females vibrate their abdomens after being touched by the courting male, producing tremulatory signals with the dominant frequency below 100 Hz, sound pressure level below 60 dB and velocity below 3 mm/s. This vibration may function as a sign of the akinesia state since it precedes the introduction of the embolus. Cuticular compounds probably determine the recognition of the male by the female. Data from the present study corroborate the generalist nature of L. intermedia in which signals of different modalities are used during courtship.     

Limited condition dependence of male acoustic signals in the grasshopper Chorthippus biguttulus

In many animal species, male acoustic signals serve to attract a mate and therefore often play a major role for male mating success. Male body condition is likely to be correlated with male acoustic signal traits, which signal male quality and provide choosy females indirect benefits. Environmental factors such as food quantity or quality can influence male body condition and therefore possibly lead to condition-dependent changes in the attractiveness of acoustic signals. Here, we test whether stressing food plants influences acoustic signal traits of males via condition-dependent expression of these traits. We examined four male song characteristics, which are vital for mate choice in females of the grasshopper Chorthippus biguttulus. Only one of the examined acoustic traits, loudness, was significantly altered by changing body condition because of drought- and moisture-related stress of food plants. No condition dependence could be observed for syllable to pause ratio, gap duration within syllables, and onset accentuation. We suggest that food plant stress and therefore food plant quality led to shifts in loudness of male grasshopper songs via body condition changes. The other three examined acoustic traits of males do not reflect male body condition induced by food plant quality.     

The effect of vibratory disturbance on sexual behaviour of the southern green stink bug Nezara viridula (Heteroptera, Pentatomidae)

The effect of vibratory disturbance on sexual behaviour and substrate-borne sound communication of the southern green stink bug, Nezara viridula L. was studied. Disturbance signals do not change the time N. viridula males need to locate the source of vibratory signals, but decrease the number of males responding with the calling and courtship song to calling females. Female N. viridula proceed calling during stimulation with disturbance signals but some of them change the song rhythm by skipping one or more signal intervals or emitting the repelling signals. The number of females which change the dominant frequency of the calling song decreases proportionally with increasing differences between the dominant frequency of the disturbance signals and the emitted female calling song. Variation of the song dominant frequency probably serves females to avoid interference by increasing the signal to noise ratio. Signal duration and repetition rate do not change significantly when the female is stimulated with the disturbance signals. This indicates that frequency shift by calling females is the main strategy for reducing interference by competitive signalers in N. viridula vibrational communication.     

A neural network-based analysis of acoustic courtship signals and female responses in <Emphasis Type="Italic">Chorthippus biguttulus</Emphasis> grasshoppers

In many animal species, male acoustic courtship signals are evaluated by females for mate choice. At the behavioural level, this phenomenon has been well studied. However, although several song characteristics have been determined to affect the attractiveness of a given song, the mechanisms of the evaluation process remain largely unclear. Here, we present a simple neural network model for analysing and evaluating courtship songs of Chorthippus biguttulus males in real-time. The model achieves a high predictive power of the attractiveness of artificial songs as assigned by real Chorthippus biguttulus females: about 87% of the variance can be explained. It also allows us to determine the relative contribution of different song characteristics to overall attractiveness and how each of the song components influences female responsiveness. In general, the obtained results closely match those of empirical studies. Therefore, our model may be used to obtain a first estimate of male song attractiveness and may thus complement actual testing of female responsiveness in the laboratory. In addition, the model allows including and testing novel song parameters to generate new hypotheses for further experimental studies. The supplemental material of this article contains the article’s data in an active, re-usable format.     

Walking in Fourier’s space: algorithms for the computation of periodicities in song patterns by the cricket Gryllus bimaculatus

Is discrimination of the envelope of an acoustic signal based on spectral or temporal computations? To investigate this question for the cricket Gryllus bimaculatus, pattern envelopes were constructed by the addition of several sine waves and modified by systematic phase changes. The phonotactic response of female crickets towards such sinusoidal but also rectangular pulse patterns was quantified on a locomotion compensator. Envelope patterns that exhibited a modulation frequency of 25 Hz as the dominant frequency were attractive and although changes of phase modified the temporal pattern, the values of attractiveness remained unaffected. Removal of the 25-Hz component reduced the phonotactic scores. Patterns in which other frequency components exhibited a larger amplitude than the 25-Hz component were less attractive. However, the combination of an unattractive pulse period with the attractive modulation frequency of 25 Hz in a pattern revealed that such stimuli were unattractive despite the presence of the 25-Hz component. A comparison of the attractiveness of all patterns revealed that female crickets evaluated the duration of pulse period over a wide range of duty cycles. The combined evidence showed that pattern envelopes were processed in the time- and not in the spectral domain.     

Filtering of temporal parameters of the calling song by cricket females of two closely related species: a behavioral analysis

The phonotactic response of cricket females was investigated on a locomotion compensator to determine the temporal parameters of the male's calling song which are important for species recognition. Two sympatric species (Teleogryllus commodus, T. oceanicus) that show different syllable periods in the chirp and trill parts of their calling songs were used. By their responses T. commodus females exhibited two temporal filters for syllable periods, which were tuned to the species-specific syllable periods occurring during chirp and trill. For song recognition both filters had to be activated and for both a minimum number of three to five consecutive syllable periods was necessary. In contrast, T. oceanicus females showed only one sharply tuned filter corresponding to the chirp part of the male's calling song. This filter was sufficient for calling song recognition. Syllable periods of the trill part also influenced calling song recognition, but these played only a minor role. Carrier frequency was also important for positive phonotaxis. Calling song recognition by T. commodus females is largely based on central nervous processing, while for T. oceanicus both peripheral frequency filtering and central temporal filtering is important. Accepted: 17 January 1997     

The structure and function of songs emitted by southern green stink bugs from Brazil, Florida, Italy and Slovenia

Nezara viridula (L.) (Pentatomidae: Heteroptera) from Brazil, Florida, Italy and Slovenia, communicate by vibratory songs associated with long‐range calling and close‐range courting, rivalry and repelling. Each song is composed of spectrally and temporally different units. Spectrally different pulses of duration less than 300 ms are present in the male calling song. The female calling song is characterized by pulse trains composed of pulses shorter than 150 ms and pulse trains composed of a longer (> 700 ms) and shorter (< 250 ms) pulse. Shorter and longer pulses have different spectral characteristics. The male and female courtship songs are characterized by fusion of shorter (< 150 ms) pulses into a pulse train usually followed by a shorter (< 200 ms) postpulse in the case of the male courtship song. The female repelling song is a several seconds long vibration of irregular temporal structure. The short (< 400 ms) male rival song pulses are frequency modulated. The dominant frequency peaks of the songs investigated lie between 70 and 130 Hz. The dominant frequency and the microstructure of song spectra show no population specificity. The average duration varies more in calling than in courtship songs. The repetition time varies extensively in songs of different populations. Normal communication followed by copulation was observed between mates from Slovenia and Brazil and between mates from Florida and Italy. The potential role of different temporal and spectral parameters for species recognition and mate location is discussed in view of the expected distortion of the characteristic signal structure during transmission through plants.     

Temporal resolution for calling song signals by female crickets, <Emphasis Type="Italic">Gryllus bimaculatus</Emphasis>

A behavioural gap detection paradigm was used to determine the temporal resolution for song patterns by female crickets, Gryllus bimaculatus. For stimuli with a modulation depth of 100% the critical gap duration was 6–8 ms. A reduction of the modulation depth of gaps to 50% led either to an increase or a decrease of the critical gap duration. In the latter case, the critical gap duration dropped to 3–4 ms indicating a higher sensitivity of auditory processing. The response curve for variation of pulse period was not limited by temporal resolution. However, the reduced response to stimuli with a high duty cycle, and thus short pause durations, was in accordance with the limits of temporal resolution. The critical duration of masking pulses inserted into pauses was 4–6 ms. An analysis of the songs of males revealed that gaps (5.8 ms) and masking pulses (6.9 ms) were at detectable time scales for the auditory pathway of female crickets. However, most of the observed temporal variation of song patterns was tolerated by females. Critical cues such as pulse period and pulse duty cycle provided little basis for inter-individual selection by females.     

Song pattern recognition in the grasshopper Chorthippus biguttulus: the mechanism of syllable onset and offset detection

The male song of the duetting grasshopper Chorthippus biguttulus consists of syllables alternating with noisy pauses. The syllable-pause structure is important for song recognition by the female. Using playback experiments we investigated the mechanism by which intensity modulations within the song pattern are used to detect syllable onsets and offsets. We varied the relative onset level (level of the syllable beginning relative to the noisy pause) and the relative offset level (level of the noisy pause relative to the syllable end) independently in different experiments. For all females, an increase in intensity defining the syllable onset was necessary to evoke responses. Syllable offset cues were not always necessary: some females responded to continuous noise stimuli wherein only syllable onsets were marked by short pulses of high intensity. Those females that did not require syllable offset cues did not, however, lack a functional pause detection mechanism, since their responses to model songs containing silent pauses were restricted to a given range of pause durations. We propose that syllable-pause detection involves two independent processes: (1) syllable onset detection by a phasic neuronal unit that can be re-activated only after a short pause, and (2) the rejection of unacceptably long pauses by a second unit.     

Changes in the Frequency Structure of a Mating Call Decrease Its Attractiveness to Females in the Cricket Frog Acris crepitans blanchardi

In many species, females often prefer male signals that are more complex than in nature or beyond the range of calls naturally produced by conspecific males in spectral, temporal and amplitude features. In this study we examined both the ability of females to recognize signals outside the normal range of spectral frequency variation seen in male advertisement calls, and the influence of increasing call complexity by adding spectral components to enhance the attractiveness of a male advertisement call in the cricket frog Acris crepitans blanchardi, while keeping its amplitude constant. We used two different natural male call groups and created the following synthetic call groups: with a dominant frequency at 3500 Hz, i.e. at the normal dominant frequency with a frequency band within the sensitivity range of the inner ear basilar papilla; with a dominant frequency at 700 Hz, i.e. outside the normal range of variation and with a frequency band outside the sensitivity range of the basilar papilla but within the range of the amphibian papilla; with two dominant frequencies, one at 700 Hz and another at 3500 Hz, stimulating the basilar and amphibian papilla simultaneously. In double choice experiments we tested all combinations of the three call groups, and we tested the 3500 Hz call groups against the same natural call groups. Additionally, we tested the 700 Hz call groups against white noise to see whether these signals are meaningful in mate choice. Females preferred 3500 Hz call groups over all other call groups. The synthetic call group was as attractive to females as the same natural call group. The 700 Hz call group was not meaningful in mate choice. The combined (700 Hz + 3500 Hz) call group was significantly less attractive to females than the 3500 Hz call group. Thus, making a call more spectrally complex without increasing its overall amplitude decreases its attractiveness to cricket frog females.     

Variance in female responses to the fine structure of male song in the field cricket, Gryllus integer

Although female mating preferences are a focus of current controversy,little detailed information exists on female preferences withinnatural populations. In the field cricket Gryllus integer, malecalls attract sexually receptive females, and females preferentiallymove toward male calls with longer calling bouts (periods ofcalling containing no pause greater than 0.10 s in real time).This study investigated female preferences for other variablesof the male song, including syllable period, chirp pause, andnumber of syllables per chirp. Male song was measured in thefield to determine mean values for each variable in nature.Female preferences were determined using a locomotor-compensatordevice, on which females ran in response to sequential playbacksof synthesized male song. Mean female preferences correspondedroughly to mean male song variables. Nonetheless, females variedgreatly in their responses to synthesized calls differing insyllable period, syllable number, and chirp pause. Moreover,individual females who were more selective for any one variablealso tended to be more selective for others. These results showthat females may differ from one another in their mating preferencesand degrees of selectivity, even within a single population.     

Songs of Holcostethus strictus (Fabricius): a different repertoire among landbugs (Heteroptera: Pentatomidae)

Songs emitted during mating by male and female Holcostethus strictus were recorded as substrate vibrations. Spectra of the vibrational signals have a dominant frequency peak between 100 and 260 Hz and in this respect reflect the general characteristic of the family Pentatomidae. Songs of H. strictus differ from the song repertoire of the southern green stink bug Nezara viridula (L.) (Pentatomidae) in many respects. The female calling and courtship songs differ in echeme and phrase duration. The male calling song is composed of spectrally different subunits. The male courtship song is characterised by three types of spectrally and temporally different echemes. The male copulatory song is composed of echemes of two types, which constitute a phrase of less regular temporal structure. In H. strictus, males start to sing first and female songs are less complex than in N. viridula. The female calling song is evoked by male calling and does not trigger male response. The female and male courtship song phrases are superimposed on one another and we have not observed any obvious regularity in their exchange. The possible role of different songs in H. strictus is discussed and compared with that in other pentatomide landbug species.     

Temporal processing of vibratory communication signals at the level of ascending interneurons in Nezara viridula (Hemiptera: Pentatomidae)

During mating, males and females of N. viridula (Heteroptera: Pentatomidae) produce sex- and species-specific calling and courtship substrate-borne vibratory signals, grouped into songs. Recognition and localization of these signals are fundamental for successful mating. The recognition is mainly based on the temporal pattern, i.e. the amplitude modulation, while the frequency spectrum of the signals usually only plays a minor role. We examined the temporal selectivity for vibratory signals in four types of ascending vibratory interneurons in N. viridula. Using intracellular recording and labelling technique, we analyzed the neurons' responses to 30 pulse duration/interval duration (PD/ID) combinations. Two response arrays were created for each neuron type, showing the intensity of the responses either as time-averaged spike counts or as peak instantaneous spike rates. The mean spike rate response arrays showed preference of the neurons for short PDs (below 600 ms) and no selectivity towards interval duration; while the peak spike rate response arrays exhibited either short PD/long ID selectivity or no selectivity at all. The long PD/short ID combinations elicited the weakest responses in all neurons tested. No response arrays showed the receiver preference for either constant period or duty cycle. The vibratory song pattern selectivity matched the PD of N. viridula male vibratory signals, thus pointing to temporal filtering for the conspecific vibratory signals already at level of the ascending interneurons. In some neurons the responses elicited by the vibratory stimuli were followed by distinct, regular oscillations of the membrane potential. The distance between the oscillation peaks matched the temporal structure of the male calling song, indicating a possible resonance based mechanism for signal recognition.     

The Effect of Age on a Sexually Selected Acoustic Display

Models of sexual selection suggest that females should prefer to mate with older males because old age is evidence of heritable high viability. In a longitudinal analysis, we demonstrate that male field crickets (Gryllus campestris) alter their calling song with age. Carrier frequency, a calling song character related to growing condition and the main song component under female preference, changed towards higher sexual attractiveness with age. Body mass decreased slightly with age, while chirp rate, an indicator of current condition, remained stable. By choosing males singing at a low frequency, female field crickets would base their mate choice decision on a sexual trait that indicates superior growing conditions as juvenile and on viability, i.e. enhanced current condition as adult.     

Exploring the hidden landscape of female preferences for complex signals

A major challenge in evolutionary biology is explaining the origins of complex phenotypic diversity. In animal communication, complex signals may evolve from simpler signals because novel signal elements exploit preexisting biases in receivers’ sensory systems. Investigating the shape of female preference functions for novel signal characteristics is a powerful, but underutilized, method to describe the adaptive landscape potentially guiding complex signal evolution. We measured female preference functions for characteristics of acoustic appendages added to male calling songs in the grasshopper Chorthippus biguttulus, which naturally produces only simple songs. We discovered both hidden preferences for and biases against novel complex songs, and identified rules governing song attractiveness based on multiple characteristics of both the base song and appendage. The appendage's temporal position and duration were especially important: long appendages preceding the song often made songs less attractive, while following appendages were neutral or weakly attractive. Appendages had stronger effects on songs of shorter duration, but did not restore the attractiveness of very unattractive songs. We conclude that sensory biases favor, within predictable limits, the evolution of complex songs in grasshoppers. The function‐valued approach is an important tool in determining the generality of these limits in other taxa and signaling modalities.