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.     

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     

Negative impact of urban noise on sexual receptivity and clutch size in female domestic canaries

In oscines, male song stimulates female reproduction and females are known to adjust both their sexual preferences and their maternal investment according to song quality. Female domestic canaries are especially responsive to wide frequency bandwidth (4 kHz) male songs emitted with a high‐repetition syllable rate and low minimal frequencies (1 kHz). We previously showed that low‐frequency urban noise decreases female sexual responsiveness for these low‐frequency songs (1–5 kHz) through auditory masking. Based on the differential allocation hypothesis, we predicted that urban noise exposure will equally affect female maternal investment. Using a crossover design, we broadcast low‐frequency songs to females either in an overlapping noise condition or in an alternating noise condition. Females decreased both their sexual responsiveness and their clutch size in the overlapping noise treatment relative to the alternative noise treatment. No differences were found concerning egg size or egg composition (yolk and albumen mass, testosterone concentration). Due to our experimental design, we can exclude a general impact of noisy conditions and thereby provide evidence for a detrimental effect through masking on avian courtship and reproductive output. These results suggest that noisy conditions may also affect avian communication in outdoor conditions, which may partly explain field reports on noise‐dependent breeding success and reduced breeding densities at noisy sites.     

Testosterone Induces Sexual Release Quality in the Song of Female Canaries

We tested the sexual responsiveness of female canaries, Serinus canaria, to two sets of different types of female conspecific songs versus an adult male conspecific song. Female songs were either spontaneously emitted (‘S-songs’) or were testosterone-induced (‘T-songs’). Copulation-solicitation displays (CSD) were used as an index of female sexual response. Playbacks were performed several days before and during egg laying, a period of natural sexual responsiveness of the females to song. We demonstrated that the weaker sexual displays of female canaries were recorded to S-songs, thus suggesting that these types of female songs do not contain fully functional sexual releasers. Three T-songs elicited high levels of sexual displays, thus demonstrating that testosterone treatment may induce sexual release quality in the female songs. Study of the phonology of these three T-songs strongly suggested that special song phrases may be good candidates as powerful sexual releasers. To test the sexual value of these female song phrases, we carried out a third experiment, using hybrid songs where each of these special T-song phrase types was included in a well-known heterospecific context. Two phrases elicited high levels of sexual responses in females. Essential features of the male full song, such as broadband rapid frequency modulations and high repetition rate, are retrieved in both female song phrases. Taken together, these data demonstrate that testosterone treatment not only induces a male-like structure in the songs of females, but also induces functionally ‘male-like’ songs. This result allows features of the vocal control network of testosterone-treated females to be compared with those of adult males singing full songs, to distinguish neural correlates of testosterone-dependent full songs. However, because testosterone does not induce functionally male-like songs in all the females, neuroanatomical structure-function correlations need detailed behavioural analysis.     

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.     

Convergent song preferences between female field crickets and acoustically orienting parasitoid flies

Traits that increase the attractiveness of males to femalesoften make them more conspicuous to predators. In the fieldcricket (Gryllus lineaticeps), males are attacked by parasitoidtachinid flies (Ormia ochracea) that locate males through theircalls. Female flies larviposit on crickets and the larvae burrowinto and feed on the cricket, killing the cricket upon emergence.To determine whether traits preferred by females increase amale's risk of attracting a predator, I examined the effectof variation in male singing behavior on mate and predator attraction.Both female crickets and female flies preferred male callingsongs with higher chirp rates, longer chirp durations, and higherchirp amplitudes. In addition, both female crickets and femaleflies preferred male calling songs with higher chirp rates andlonger chirp durations, even when these songs were of loweramplitude. These results suggest that sexual selection by femalechoice will favor the evolution of higher chirp rates and longerchirp durations. However, call types that increase a male'sattractiveness to females also appear to increase a male's riskof attracting parasitoids. Sexual and natural selection appearto have opposing effects on the evolution of male singing behaviorin this species.[Behav Ecol 7: 279-285 (1996)]     

Female recognition of trills in the male calling song of the field cricket,<Emphasis Type="Italic"> Teleogryllus taiwanemma</Emphasis>

The calling song of the field cricket, Teleogryllus taiwanemma, is usually considered to consist of sequences of separate chirps. However, sometimes it comprises a phrase of several chirps in a row, with one long chirp (chirp) and a few short chirps (trills). In this study, I compared the phrase containing only chirps with that containing both chirps and trills by analyzing male songs and conducting playback experiments of male songs to females. The song analyses showed significant differences between chirps and trills for all song parameters except bandwidth. To test whether female preference differed with respect to the two phrases, I performed two-speaker playback experiments. When the same numbers of phrases were presented per unit time, females preferred the song with trills to that without trills. This result may reflect female preference for songs with greater sound density. In subsequent playback experiments, I equalized the total sound duration per unit time (duty cycle) in songs with and without trills. The numbers of females that preferred songs with and without trills did not differ significantly. This suggests that trills can attract females like chirps do, even though the two sounds have different components.     

Increased syllable rate during aggressive singing in a bird with complex and fast song

Sexual signals can comprise traits with multiple functions, and species with extreme phenotypes offer an opportunity to link function with signal evolution. This is the case in the serin Serinus serinus, a songbird with extremely fast syllable rate compared to related finches, and high sound frequency for its body size. Previous work on receiver responses showed that playback of artificially increased syllable rate is avoided and inhibits vocal responses, suggesting it is perceived as aggressive, while, on the contrary, higher sound frequency appears preferred by females. We tested whether senders also change these traits during aggressive singing, with a field playback experiment. Serin males responding aggressively by approaching the playback loudspeaker also increased syllable rate, while males responding less aggressively did not change syllable rate. Together with work on receiver responses, this suggests that aggressive signalling may have been an important selective pressure for the evolution of extremely fast syllable rate in this species. It is noteworthy that aggressive male serins still increase syllable rate, despite of their already elevated natural syllable rate. We found no changes in sound frequency when singing aggressively, which agrees with previous work that instead showed a female preference for high song frequency. We conclude that the evolution of extreme traits in serin song is best explained by multiple functions.     

Male Song Stimulation of Female Reproduction in Canaries: Features Relevant to Sexual Displays are not Relevant to Nest-building or Egg-laying

Recent studies conducted in our laboratory have demonstrated that a special type of song phrase (‘sexy’ phrases) containing bipartite syllables composed of abrupt frequency falls and short silences stimulate female canaries to solicit for copulation. The study was undertaken to determine whether sexy phrases also facilitated other aspects of the reproductive activity of the female canary, namely, nest-building and egg-laying. During the first experiment, we studied the effect of sexy and non-sexy songs on copulation solicitation displays in 1-year-old females without reproductive experience and in mature females with previous reproductive experience. We confirmed that sexy songs elicited more sexual responses than did non-sexy songs in yearlings and in mature females. During the second experiment, we studied the effect of male songs on nest-building activities and egg-laying in 1-year-old inexperienced females, and in mature, experienced females. The songs of conspecific males significantly triggered and increased nest-building behaviour in female canaries whatever their age or reproductive experience. In contrast, song effects on egg-laying were only found in young females. One-year-old inexperienced females exposed to sexy or non-sexy songs laid more eggs and laid earlier than did 1-year-old inexperienced controls; no such differences were observed in mature, experienced females. The efficiency of songs in promoting nest-building or egg-laying appeared to be unrelated to their efficiency in eliciting sexual responses. No difference was found between females exposed to sexy songs and females exposed to non-sexy songs; differences were only found between control and the two groups of song-exposed females. This result demands further experiments in order to determine whether other song phrase types may account for the stimulating effects of male song on female nest-building and egg-laying.     

Separate localization of sound recognizing and sound producing neural mechanisms in a grasshopper

Summary In the two acridid speciesChorthippus parallelus andCh. montanus, the sound template by which females recognize male song varies with temperature, as does the song itself. At relatively high temperatures the females respond best to simulated songs with high syllable frequencies, and at lower temperatures songs with lower syllable frequencies are preferred.The temperature around the supraesophageal and metathoracic ganglia of female grasshoppers was monitored by implanted thermocouples, and either the head or the thorax was warmed selectively while the animal was free to move (within the imits of the wires). Then simulations of the conspecific song varying in syllable frequency corresponding to different song temperatures were presented, and the stridulatory responses of the animals were observed.The results were as follows. 1. Song recognition (in particular, the position of the peak of the response curve) depended on the temperature of the head. 2. The rate of stridulatory hindleg movement was determined by the temperature of the thoracic ganglia.This result provides strong evidence against the genetic coupling hypothesis.     

Is female preference for male repertoires due to sensory bias?

There are several possible explanations for the female preference for male repertoires in birds. These males are older, and have better territories; thus there are functional reasons for females to prefer these males. However, there is an alternative explanation; females may habituate less quickly to song repertoires than single songs. I tested whether females have a non-functional, sensory bias for male song repertoires, by testing female preference for a repertoire in zebra finches (Taenopygia guttata), a species in which males possess a single stereotyped song. Females chose between a male repertoire of four different phrases created from the song phrase of one individual and that of one of those phrases repeated four times (natural zebra finch song). Females were also given a choice between the above repertoire and a song made from the phrases of four related males (''family'' stimulus). I tested female preference by training females to press a button for presentation of a song stimulus, and counting the number of button presses. Females preferred the song repertoire to a single phrase song, and did not differentiate between the repertoire and song phrases from four males. Evidence from the Estrildidae indicates that having a single song is the ancestral state for zebra finches, so the preference is not ancestral.     

Directional female preference for an exaggerated male trait in canary (Serinus canaria) song

Motor constraints on vocal production impose a trade-off between trill rate and frequency bandwidth within birdsong. We tested whether domesticated canary (Serinus canaria) females, reared either in acoustic isolation or in aviary conditions, had a preference for broad bandwidth songs with artificially increased syllable rates. The copulation solicitation display (CSD) was used as an index of female preference. As predicted, both naive and experienced females were especially responsive to syllables with a broad bandwidth emitted at an artificially increased rate. Female preference for supernormal stimuli provide support for the honest-signalling hypothesis and our results are consistent with recent findings indicating that production of song phrases maximizing both bandwidth and syllable rate may be a reliable indicator of male physical or behavioural qualities. We suggest that female preference for vocal emissions, which simultaneously maximize these two parameters, could be a widespread pattern within songbirds.     

Species Recognition by Song in the Veery (Catharus fuscescens: Aves)

Territorial male veeries (Catharus fuscescens) were presented with three series of reorganised songs to determine the functional properties of song structure. Songs consist of three parts: a low frequency initial phrase, a higher frequency middle phrase, and again a lower frequency end phrase. The latter two consist of vibrato syllables. Three series of experiments were performed, using various combinations of song syllables. In Series I, songs consisted of repetitions of a single syllable, one from each part of the song. Veeries responded to syllables from the middle and end phrases as to normal songs, both in localisation and in vocal responses. However, they showed little localisation and vocalisation responses to the introductory syllables. In Series II and III, veeries responded significantly more to songs in which syllables from the middle and end phrases were presented in proper sequence, rather than not. The minimum requirements for intraspecific recognition were determined in relation to the number and order of syllables in the song.     

Female Preferences for Male Song Characters in the Bush-Cricket Isophya camptoxypha (Orthoptera, Tettigonioidea)

Female preferences for two male song characters (duration of syllables [DS], syllable repetition period [SRP]) have been studied in Isophya camptoxypha, an Eastern European duetting bush-cricket. Songs with modified DS or SRP were presented to virgin females and their response songs were recorded and counted. Female preference functions were unimodal for both characters. But while in the case of SRP the obtained female preference function reached its maximum at the mean value of that character, in the case of DS females preferred modified songs with a DS slightly higher than the natural range of that character. A comparison between the obtained preference functions and the DS and SRP values measured in sympatric Isophya species (with similar song structure) suggests that the two examined characters and female preferences for them may be effective components of the species-specific mate recognition system of I. camptoxypha. Moreover DS values may also convey information about the quality of the singing male.     

Sex-specific spectral tuning for the partner's song in the duetting bushcricket Ancistrura nigrovittata (Orthoptera: Phaneropteridae)

The song of the male bushcricket Ancistrura nigrovittata consists of a sequence of verses. Each verse comprises a syllable group, plus, after about 400 ms a single syllable serving as a trigger for the female response song. The carrier frequency of the male song spectrum peaks at around 15 kHz, while the female song peaks at around 27 kHz. The thresholds of female responses to models of male songs are lowest for song frequencies between 12 and 16 kHz and therefore correspond to the male song spectrum. The threshold curve of the female response to the trigger syllable at different frequencies has the same shape as the tuning for the syllable group. Phonotactic thresholds of male Ancistrura nigrovittata to synthetic female responses at different frequencies are lowest between 24 and 28 kHz and thereby correspond to the female song spectrum and clearly differ from female response thresholds. Activity of the tympanic fibre bundle of both sexes is most sensitive between 15 and 35 kHz and therefore not specifically tuned to the partner's song. Individual behavioural thresholds have their minimum within 10 dB of the values of tympanic thresholds.     

Behavioral sterility of hybrid males in acoustically communicating grasshoppers (Acrididae,Gomphocerinae)

The effectiveness of hybridization barriers determines whether two species remain reproductively isolated when their populations come into contact. We investigated acoustic mating signals and associated leg movements responsible for song creation of hybrids between the grasshopper species Chorthippus biguttulus and C. brunneus to study whether and how songs of male hybrids contribute to reproductive isolation between these sympatrically occurring species. Songs of F1, F2, and backcross hybrids were intermediate between those of both parental species in terms phrase number and duration. In contrast, species-specific syllable structure within phrases was largely lost in hybrids and was produced, if at all, in an irregular and imperfect manner. These divergences in inheritance of different song parameters are likely the result of incompatibility of neuronal networks that control stridulatory leg movements in hybrids. It is highly probable that songs of hybrid males are unattractive to females of either parental species because they are intermediate in terms of phrase duration and lack a clear syllable structure. Males of various hybrid types (F1, F2, and backcrosses) are behaviorally sterile because their songs fail to attract mates.     

The effect of temperature on the temporal structure of the vibratory courtship signals of a spider (Cupiennius salei Keys.)

We studied the effect of ambient temperature (13°C–34°C) on the vibratory courtship communication of the wandering spider Cupiennius salei.

1. Male vibratory signals. The durations of most signal parameters decreased linearly with increasing temperature. The number of syllables in one series, and that of pulses in one syllable did not change with temperature, however. The ratios of the durations of a series and interseries, and of a syllable and a sequence (duty cycle) remained largely unchanged by temperature as well.
2. Female vibratory response. The duration of the female response to the male vibration decreased with increasing temperature whereas the female response rate remained roughly constant between 13°C and 25°C. Females exposed to different temperatures favored male signals recorded in the same temperature range. To compensate for temperature dependent changes of male vibrations the female may therefore rely on the adjustment of her receiving system and/or temperature invariant signal parameters. Among these the duty cycle is considered particularly important.
3. Temporal relationship. The onset of the female response often occurred at the supposed onset of a male syllable, had the male continued to signal after completing the series. This synchronization may be advantageous in a noisy environment.

     

Responses to features of the calling song by ascending auditory interneurones in the cricket Gryllus campestris

ABSTRACT. In female Gryllus campestris L., three functional types of ascending auditory intemeurones have been studied by recording from them extracellularly in the split cervical connectives using suction electrodes. Type 1 neurones are characterized by an optimal sensitivity to the carrier frequency of the species calling song (4–5 kHz). They copy the syllable and pause structure of the call at all intensities. The patterned spike discharge is observable at least 8 dB above absolute threshold. With suprathreshold stimulation, the neurones exhibit maximal responses (number of spikes/chirp) around the carrier frequency. The intensity response curves are approximately linear in the range of 40–90 dB SPL. The envelope of each syllable is reflected by a corresponding change in the firing rate, and syllable periods of 24ms and longer are resolved. This type can be considered as a neural correlate for phonotactic behaviour of the female where the syllable period has been found to be the most important temporal parameter. Type 2 neurones are most sensitive in the range of 4–6 and 11–13 kHz. They copy the syllable and pause structure of the species calling song at low and moderate intensities. However, the spikes invade the intersyllable pauses, when stimulated with the calling song at higher intensities (above 85 dB). This is particularly apparent at the onset of a chirp series. The slope of the intensity—response curve mimics that of type 1 units. The neurones cannot follow syllable periods shorter than 32 ms. Type 3 neurones differ from types 1 and 2 by a rather broad-band sensitivity in the range of 3–16 kHz, and in copying the chirp as a whole. Even at low stimulus intensities, the intersyllable pauses are filled with spikes, and information about the syllable—pause structure is lost. Stimulation with suprathreshold intensities gives rise to a rather uniform, broad-band response without distinctive peaks. The intensity—response curve is characterized by a higher absolute threshold, and by the reduction in the response magnitude starting above 70–80 dB. These units are not suitable for copying the calling song temporal structure in detail, but would indicate the chirping rhythm. Their strong response in the range of the species courtship song carrier frequency make them suitable to copy the courtship song.     

The Development of Local Song Preferences in Female Cowbirds (Molothrus ater): Flock Living Stimulates Learning

We carried out two experiments across 2 yr on song perception in female cowbirds (Molothrus ater). In the first experiment, juvenile and adult female brown‐headed cowbirds, living in same‐sex flocks in outdoor aviaries, were periodically tutored with recordings of local male cowbirds’ songs. In the spring, four adult male cowbirds were placed with half of the females for a 12‐d period. We then tested song preferences of all females by measuring copulation solicitation displays during the breeding season. We found that the females exposed only to tape‐tutor songs preferred those songs to those of the unfamiliar males used as companions and that the females allowed to interact with males preferred their songs over the familiar tape‐tutor songs. These data establish the modifiability of female cowbirds’ song preferences at the level of local song. In a second experiment, we studied the playback responses of juvenile females, hand‐reared from the egg, who were tape‐tutored only in the spring in the presence or absence of adult females. There were no differences between the responses of juveniles housed with or without adult females and the hand‐reared juveniles were significantly less responsive to song than adult females. Adult females responded more to familiar songs than to the unfamiliar songs: juvenile females made no such distinction. Taken as a whole, these data are the first to document that female cowbirds’ song preferences for local song can be reshaped by post‐natal experience. These data complement recent study in cowbirds and other species showing that socially more complex contexts reveal plasticity in female song preferences that are not apparent when learning opportunities are constrained by impoverished laboratory settings.     

Versatility and Stereotypy of Free-Tailed Bat Songs

In mammals, complex songs are uncommon and few studies have examined song composition or the order of elements in songs, particularly with respect to regional and individual variation. In this study we examine how syllables and phrases are ordered and combined, ie “syntax”, of the song of Tadarida brasiliensis, the Brazilian free-tailed bat. Specifically, we test whether phrase and song composition differ among individuals and between two regions, we determine variability across renditions within individuals, and test whether phrases are randomly ordered and combined. We report three major findings. First, song phrases were highly stereotyped across two regions, so much so that some songs from the two colonies were almost indistinguishable. All males produced songs with the same four types of syllables and the same three types of phrases. Second, we found that although song construction was similar across regions, the number of syllables within phrases, and the number and order of phrases in songs varied greatly within and among individuals. Last, we determined that phrase order, although diverse, deviated from random models. We found broad scale phrase-order rules and certain higher order combinations that were highly preferred. We conclude that free-tailed bat songs are composed of highly stereotyped phrases hierarchically organized by a common set of syntactical rules. However, within global species-specific patterns, songs male free-tailed bats dynamically vary syllable number, phrase order, and phrase repetitions across song renditions.