Synthetic Songs Research Articles

Male song quality affects circulating but not yolk steroid concentrations in female canaries (Serinus canaria)

Male song complexity is a sexually selected trait found in many songbirds, including strains of the domestic canary. Studies on several species have shown that male song can affect the hormonal state of females and may also influence concentrations of maternal hormones in the yolk of their eggs. In this study, we show that the level of circulating androgens and oestrogens of female canaries, as measured in faeces, varies with the quality of male song to which they are exposed. The female-perceived quality of male canary song depends on the production of special 'sexy syllables' to which females respond with more sexual displays. Using playback of synthetic song we show that females hearing songs with sexy syllables have higher levels of faecal testosterone than control females hearing songs without them. However, unlike previous studies on the canary, we found no evidence that such females laid eggs with more testosterone (or other steroids) in their egg yolks. We discuss these results in relation to the evolution of male signalling and maternal investment strategies.

Narishige Zoological Science Symposium: From Sensory Reception, Behavior to Brain Functions: Neuroscience in Invertebrates

Cricket calling song is a species-specific signal and plays an important role in species recognition. The role of cricket song as a pre-mating isolation mechanism should be examined in a comparative study of closely related species inhabit sympatrically. On the Japanese Archipelago, three Teleogryllus species have wide distribution areas. T. yezoemma ranges from Hokkaido Island to the Kanto region, T. emma from Hokkaido to the Kyushu region, and T. taiwanemma from south of the Kii Peninsula to the South Asian tropics. The distribution of T. emma overlaps that of T. yezoemma in the north and that of T. taiwanemma in the south. T. yezoemma and T. taiwanemma are allopatric. I compared calling songs of the three species using principal component analysis. Furthermore, three-choice playback experiments using females of the three Teleogryllus species were performed to test whether female crickets can discriminate accurately their conspecific mates on the basis of their calling song. The results showed that the allopatric species (T. yezoemma and T. taiwanemma) have similar songs that females cannot discriminate accurately, whereas the partially sympatric species (T. yezoemma and T. emma, T. emma and T. taiwanemma) have divergent songs that females can distinguish accurately. This empirical evidence suggests that calling song plays an important role as a pre-mating isolation mechanism in three species of Teleogryllus. Furthermore, I performed three-choice playback experiments for females of each species using a synthetic song in order to identify the key feature for mate choice. The results showed that females preferred the song with the conspecific pulse period, while did not show a clear preference for dominant frequency. For pulse number and inter-phrase duration, females showed open-ended preference. These results suggest that pulse period is the key feature for species-specific song recognition. Studies of acoustic animal communication have shown that temporal patterns are more important than frequency parameters for song recognition. Previous neurophysiological studies of other cricket species support these results. In addition, there were differences in female preference shape among the three species. This suggests that even closely related species evaluate key features differently, and consequently calling song diversity could have appeared in the evolutionary process.

Synthesizing bird song

In this work we present an electronic syrinx: an analogical integrator of the equations describing a model for sound production by oscine birds. The model depends on time varying parameters with clear biological interpretation: the air sac pressure and the tension of ventral syringeal muscles. We test the hypothesis that these physiological parameters can be reconstructed from the song. In order to do so, we built two transducers. The input for these transducers is an acoustic signal. The first transducer generates an electric signal that we use to reconstruct the bronchial pressure. The second transducer allows us to reconstruct the syringeal tension (in both cases, for the time intervals where phonation takes place). By driving the electronic syrinx with the output of the transducers we generate synthetic song. Important qualitative features of the acoustic input signal are reproduced by the synthetic song. These devices are especially useful to carry out altered feedback experiences, and applications as biomimetic resources are discussed.

Freedom and Rules: The Acquisition and Reprogramming of a Bird's Learned Song

Canary song is hierarchically structured: Short stereotyped syllables are repeated to form phrases, which in turn are arranged to form songs. This structure occurs even in the songs of young isolates, which suggests that innate rules govern canary song development. However, juveniles that had never heard normal song imitated abnormal synthetic songs with great accuracy, even when the tutor songs lacked phrasing. As the birds matured, imitated songs were reprogrammed to form typical canary phrasing. Thus, imitation and innate song constraints are separate processes that can be segregated in time: freedom in youth, rules in adulthood.

Modulation power and phase spectrum of natural sounds enhance neural encoding performed by single auditory neurons.

We examined the neural encoding of synthetic and natural sounds by single neurons in the auditory system of male zebra finches by estimating the mutual information in the time-varying mean firing rate of the neuronal response. Using a novel parametric method for estimating mutual information with limited data, we tested the hypothesis that song and song-like synthetic sounds would be preferentially encoded relative to other complex, but non-song-like synthetic sounds. To test this hypothesis, we designed two synthetic stimuli: synthetic songs that matched the power of spectral-temporal modulations but lacked the modulation phase structure of zebra finch song and noise with uniform band-limited spectral-temporal modulations. By defining neural selectivity as relative mutual information, we found that the auditory system of songbirds showed selectivity for song-like sounds. This selectivity increased in a hierarchical manner along ascending processing stages in the auditory system. Midbrain neurons responded with highest information rates and efficiency to synthetic songs and thus were selective for the spectral-temporal modulations of song. Primary forebrain neurons showed increased information to zebra finch song and synthetic song equally over noise stimuli. Secondary forebrain neurons responded with the highest information to zebra finch song relative to other stimuli and thus were selective for its specific modulation phase relationships. We also assessed the relative contribution of three response properties to this selectivity: (1) spiking reliability, (2) rate distribution entropy, and (3) bandwidth. We found that rate distribution and bandwidth but not reliability were responsible for the higher average information rates found for song-like sounds.

Diversity within a birdsong.

We present a model for the activities of neural circuits in a nucleus found in the brains of songbirds: the robust nucleus of the archistriatum (RA). This is a fore brain song control nucleus responsible for the phasic and precise neural signals driving vocal and respiratory motor neurons during singing. Driving a physical model of the avian vocal organ with the signals generated by the neural model, we produce synthetic songs. This allows us to show that certain connectivity architectures in the RA give rise to a wide range of different vocalizations under simple excitatory instructions.

Calling-song function in male haglids (Orthoptera: Haglidae,Cyphoderris)

We studied the response of males to the singing of nearby male conspecifics in two species of the orthopteran genus Cyphoderris, primitive relatives of crickets and katydids. Lone male Cyphoderris buckelli stridulating in a large cage made a phonotactic approach to a nearby speaker broadcasting conspecific calling song. But in field experiments no phonotaxis to song broadcasts occurred; rather, a significant number of male C. buckelli increased their chirp duty cycle and pulse rate. There was no change in their carrier frequency. Calling male Cyphoderris monstrosa were exposed in the field to (i) playback of a synthetic calling song at a typical conspecific pulse rate, (ii) relayed broadcast of their own call, and (iii) low-frequency audio noise. Call duty cycle decreased significantly in response to the noise, while the pooled song models fell just short of significance. Singing C. buckelli were marked individually and their perches flagged over successive nights. We observed low site fidelity and extensive male displacement. Such behaviour is inconsistent with defense of topographically fixed singing territories and concurs with the absence of fighting in this species. Chirp duty cycle was increased significantly in C. buckelli in response to the singing of nearby conspecifics, but unlike in C. monstrosa, this change in duty cycle plays no role in overt aggression, though it may maintain a male's relative attractiveness to females.

A shot in the dark: the silent quest of a free-flying phonotactic fly.

To reproduce, females of the parasitoid fly Ormia ochracea detect and localise a calling male cricket upon which they deposit their endoparasitic larvae. Calling male crickets are therefore subject to both sexual and natural selection by simultaneously attracting mates and phonotactic parasitoids. The possible strategy of song interruption employed by the cricket host to reduce his attractiveness to acoustic parasitoids was tested in the laboratory by examining the fly's phonotactic quest in response to synthetic cricket songs. Phonotactic flight trajectories were recorded in three dimensions with a stereo infrared video tracking system while the sound stimulus was controlled on-line as a function of the fly's position in space. Within a single flight, three distinct phases could be observed: a take-off phase, a cruising phase, during which course and altitude were rather constant, and a landing phase characterised by a spiralling descent towards the sound source. The flies showed remarkable phonotactic accuracy in darkness; they landed at a mean distance of 8.2 cm from the centre of the loudspeaker after a flight distance of approximately 4 m. The present data illustrate the fly's surprising ability to gauge the direction and distance of a sound source in three dimensions and, subsequently, to find it in darkness and silence.

Characterization of female preference functions for Drosophila montana courtship song and a test of the temperature coupling hypothesis.

Female mate preferences are a major cause of diversity and elaboration in male sexual traits. Here we characterize the shape of female preference functions for pulse length and carrier frequency of the courtship song of Drosophila montana by fitting both parametric and nonparametric functions to the incidence of female receptive gestures to synthetic song. Preference functions for both traits are strongly directional. That for pulse length is linear and favors short pulses, whereas that for carrier frequency is stabilizing in shape, but would exert directional preferences favoring males with high carrier frequency. The preference for carrier frequency has probably evolved under sexual selection, but reasons for the preference for short pulses are less apparent. We also examine the effect of ambient temperature on the carrier frequency of male song and on the preference function for carrier frequency. For many similar acoustic communication systems, temperature coupling, a compensatory effect of temperature on preference functions, is thought to maintain coordination between preferences and signals. However, although the carrier frequency of D. montana song is highly dependent on environmental temperature, there is no temperature coupling of the female preference function. We suggest that temperature coupling may often arise due to a common effect of temperature on song and preference, rather than be an advantageous characteristic whose function is to maintain coordination in temperature-affected communication systems.

Song recognition in female bushcrickets Phaneroptera nana.

Unlike most acoustic systems evolved for pair formation, in which only males signal, in many species of phaneropterine bushcrickets both sexes sing, producing a duet. We used the duetting species Phaneroptera nana as a model to explore the cues in the male's song that elicit the female's phonoresponse. Different synthetic male songs (chirps containing 2-6 pulses) were presented to Ph. nana females, and their acoustic responses were recorded. The threshold of the female response is lowest at 16 kHz (best frequency), coinciding with the dominant frequency of the male song. The specific amplitude pattern of consecutive pulses in the song of the male is not a critical factor in his signal. That is, songs with both a normal and a reversed order of pulses equally elicit a female response. By systematically deleting pulses from the synthetic male chirp, we found that at least two pulses are needed to elicit a female reply. Under no-choice conditions, increasing the number of pulses did not result in a higher probability of response and did not change the latency of the response; i.e. two pulses are necessary and sufficient to elicit a female response. The range of pulse duration that elicits a female response is 0.2-25 ms, and the inter-pulse silent interval ranges from 5 to 30 ms.

Drosophila song as a species-specific mating signal and the behavioural importance of Kyriacou & Hall cycles in D. melanogaster song

‘Species-specific’ mating signals may not make a significant contribution to sexual isolation if differences between species are not matched by narrowly tuned differences in female preferences. The courtship song of the melanogaster species group of Drosophila has been studied by several researchers as a potential factor in sexual isolation, but there are few clear demonstrations that species differences are behaviourally significant. We played synthetic song with typical pulse interval parameters for D.melanogaster, D.simulans orD.sechellia to D.melanogaster or D.simulans females in the presence of mute males. Females mated most quickly when stimulated by song typical of their own species, confirming that song can influence sexual isolation between these species. This effect was greater in D.melanogaster than D.simulans, which correlates with reduced variability in mean interpulse interval within D.melanogaster. We also examined the role of ‘Kyriacou & Hall cycles’ (periodic cycling of mean interpulse intervals) in D.melanogaster. Contrary to some predictions, the presence of the Kyriacou & Hall cycle was more important in increasing mating speed than the increased variability of interpulse intervals that is inevitably present in song containing a cycle. The large stimulatory effect of cycles on mating speed is curious, given that the periodicity of cycles would probably be difficult for females to detect during courtship in field conditions.

Female preference for fly song: playback experiments confirm the targets of sexual selection

The courtship song ofDrosophilais thought to be involved in sexual selection and species recognition. Because of the mating system of flies, however, directly demonstrating that song influences female preference is difficult. The majority of previous studies have used an experimental design that potentially confounds male and female reactions to song. InD.montana, correlational evidence has suggested that males that produce short sound pulses consisting of a high number of sound cycles (i.e. a high carrier frequency) have a higher mating success than other males. In this study, we played synthetic song that varied in pulse length and carrier frequency to individual females in the laboratory, both alone and in the presence of mute males. We scored female preference via an acceptance posture, ‘wing spreading’, which the females of this species usually display prior to mounting by a male. Females responded to synthetic song in the absence of males. The presence of mute males significantly increased their overall responsiveness, but the relative effectiveness of the songs did not change, eliminating male reaction to song as a possible confounding factor in the results. The interaction between pulse length and carrier frequency determined the discrimination between song types, with females responding most readily to song consisting of short pulses with a high carrier frequency. Thus, direct examination of female preferences supports the previous studies of male mating success, and confirms female song preference as a likely determinant of male mating success.

Discrimination of degraded conspecific song in zebra finches (Taeniopygia guttata)

Thresholds for detecting degraded conspecific songs in zebra finches were measured using operant conditioning. A parametric representation of song obtained by decomposing natural songs using a bank of frequency filters served as a model for synthetic songs. Degraded songs were produced by progressively changing the instantaneous relative phase across adjoining frequency bands. Control songs preserving original phase relationships have generated neural responses in the avian forebrain nucleus HVC that are indistinguishable from responses to natural versions of the bird’s own song (BOS). Our thresholds showed that birds were very sensitive to modifications in BOS, giving results very similar to those obtained from neural recordings in HVC. Moreover, our bird thresholds were similar to those obtained for humans tested with the same task. Unlike electrophysiological results, however, behavioral thresholds for discriminating changes in song were not selective for an individual’s own song, nor for the song played forwards or backwards. These results suggest that precise temporal information present in the relative phase of any complex sound is preserved in both high level general auditory areas as well as in areas specialized for detecting particular songs. [Work supported by NIH.]

Courtship songs ofDrosophila pseudoobscuraandD. persimilis: analysis of variation

Differences inDrosophilacourtship song elements are thought to confer species sexual isolation because of the low levels of variation within species, the large differences often seen between closely related species, and the results of experiments using synthetic songs in two species groups. In this study, we reanalyse the courtship song elements ofD.pseudoobscuraandD.persimilis. We confirmed the differences between these species in high-rate repetition song interpulse interval (IPI) and intrapulse frequency and in the amount of low-rate repetition song produced. We found that both X-chromosome and autosomal loci contribute to the differences betweenD.pseudoobscuraandD.persimilisin their IPI and intrapulse frequency. No association was detected between IPI and hybrid male mating success to females of either species, although frequency was associated with mating success toD.persimilisfemales. Additionally, we found evidence of IPI periodicity in the song ofD.persimilis, demonstrated differences in mean IPI betweenD.pseudoobscurapopulations, and showed a significant influence of temperature on IPI and intrapulse frequency. Such environmental effects may have obscured tests for population differentiation in courtship song parameters in other species, and we suggest the possibility that differences betweenDrosophilaspecies in mean courtship song IPI might only rarely affect their sexual isolation.

Temporal and Spectral Sensitivity of Complex Auditory Neurons in the Nucleus HVc of Male Zebra Finches

Complex vocalizations, such as human speech and birdsong, are characterized by their elaborate spectral and temporal structure. Because auditory neurons of the zebra finch forebrain nucleus HVc respond extremely selectively to a particular complex sound, the bird's own song (BOS), we analyzed the spectral and temporal requirements of these neurons by measuring their responses to systematically degraded versions of the BOS. These synthetic songs were based exclusively on the set of amplitude envelopes obtained from a decomposition of the original sound into frequency bands and preserved the acoustical structure present in the original song with varying degrees of spectral versus temporal resolution, which depended on the width of the frequency bands. Although both excessive temporal or spectral degradation eliminated responses, HVc neurons responded well to degraded synthetic songs with time-frequency resolutions of approximately 5 msec or 200 Hz. By comparing this neuronal time-frequency tuning with the time-frequency scales that best represented the acoustical structure in zebra finch song, we concluded that HVc neurons are more sensitive to temporal than to spectral cues. Furthermore, neuronal responses to synthetic songs were indistinguishable from those to the original BOS only when the amplitude envelopes of these songs were represented with 98% accuracy. That level of precision was equivalent to preserving the relative time-varying phase across frequency bands with resolutions finer than 2 msec. Spectral and temporal information are well known to be extracted by the peripheral auditory system, but this study demonstrates how precisely these cues must be preserved for the full response of high-level auditory neurons sensitive to learned vocalizations.

The influence of female age on phonotaxis during single and multiple song presentations in the field cricket,Gryllus integer (Orthoptera: Gryllidae)

The influence of age on variation in female phonontaxis in the field cricket,Gryllus integer, was investigated using a Kugel treadmill-type device. Synthetic male calling songs, with different pulse rates, were presented in both single-stimulus and three-stimulus designs. Females were either 11–14 or 25–28 days postecdysis. Females varied in motivation, or the degree of reproductive effort they exhibited, but only in single-stimulus trials: older females achieved higher scores than younger females. Females varied in selectivity, or the extent to which they discriminated among potential mates, in both presentation designs. All females discriminated against atypical pulse rates. In multiple-stimulus trials with normal range pulse rates, younger females were discriminatory; older females were not. Mated females showed reduced phonotaxis and selectivity irrespective of mating interval.

FEMALE CHOICE FOR AN INDICATOR OF MALE SIZE IN THE SONG OF THE BLACK-HORNED TREE CRICKET, OECANTHUS NIGRICORNIS (ORTHOPTERA: GRYLLIDAE: OECANTHINAE).

The calling song of male crickets, including Oecanthus nigricornis (Walker), attracts females for mating and provides a model system of sexual communication. We give the first conclusive identification of a feature of cricket song that is both attractive to females and indicates a phenotypic feature (body size) that determines male mating success and female reproductive benefits. We do this by first testing for correlations between song characteristics and aspects of male phenotype that are hypothesized to indicate male quality. We show that song is a reliable indicator of male size and male age, and that large male size is associated with increased female fecundity. We then use playbacks of synthetic songs that mimic natural variation in song parameters to study song preferences and we compare preferences under different presentation regimes to determine whether choices are based on relative song quality or some fixed criterion. Females show a preference for the lower frequency songs produced by large males, but only during simultaneous playbacks. Thus female choice is based on the relative quality of calls that can be sampled simultaneously. These results provide strong support for the hypothesis that females use variation in calling song to assess male mate quality.

The Introduction, Establishment, and Spread ofOrmia depletain Florida

Abstract Ormia depleta (Wiedemann) (Diptera: Tachinidae), native to Brazil, is a parasitoid of some Scapteriscus species (Orthoptera: Gryllotalpidae). It was first cultured in a laboratory in Florida in 1987. Releases of O. depleta were made against Scapteriscus mole crickets in all regions of Florida beginning in 1988. Establishment of populations was achieved at some, but not all, of the release sites. The two earliest-established populations were monitored using traps employing synthetic calling song of male Scapteriscus mole crickets, to which gravid female flies are attracted. Additionally, progeny of the released flies were trapped between 1988 and 1993 in 32 peninsular counties, including 15 counties in which no releases had been made. The most parsimonious explanation of the pathways of spread of the current population was inferred from trapping surveys, and this yielded the probable year of colonization for peninsular counties. Reports in successive years by golf course superintendents of damage by mole crickets showed that counties with O. depleta populations had significantly less damage than did yet-uncolonized counties.

Frequency as a releaser in the courtship song of two crickets, Gryllus bimaculatus (de Geer) and Teleogryllus oceanicus: a neuroethological analysis.

1. The courtship behavior of male field crickets, Gryllus bimaculatus (De Geer) and Teleogryllus oceanicus, is a complex, multimodal behavioral act that involves acoustic signals (a courtship song; Fig. 1A, B). The dominant frequency is 4.5 kHz for T. oceanicus song (Fig. 1A) and 13.5 kHz for G. bimaculatus (Fig. 1B). 2. When courting males are deprived of their courtship song by wing amputation, their courtship success declines markedly but is restored when courting is accompanied by tape-recordings of their courtship songs or a synthetic courtship song with only the dominant frequency of the natural song; other naturally occurring frequency components are ineffective for restoring mating success (Figs. 4, 5). 3. It has been suggested that an identified auditory interneuron, AN2, plays a critical role in courtship success. Chronic recordings of AN2 in an intact, tethered female show that AN2's response to the natural courtship song and synthesized songs at 4.5 and 13.5 kHz is similar in T. oceanicus. By contrast, in G. bimaculatus, AN2's response to the natural courtship song and synthesized song at 13.5 kHz, but not at 4.5 kHz, is similar (Fig. 2,3). 4. In behavioral experiments, playback of a 30 kHz synthetic courtship song in G. bimaculatus does not restore courtship success, yet this same stimulus elicits as strong a response from AN2 as does the normal courtship song (Fig. 6). Thus, contrary to earlier work by others, we conclude AN2 is not, by itself, a critical neural link in the courtship behavior of these two species of crickets.

Use of a Sound Trap to Inoculate Steinernema scapterisci (Rhabditida: Steinernematidae) into Pest Mole Cricket Populations (Orthoptera: Gryllotalpidae)

We report on a novel method to disseminate an entomopathogenic nematode, Steinernema scapterisci Nguyen & Smart, planned to capitalize on the potential of the nematode as a classical, inoculative biological control agent. Scapteriscus mole crickets were attracted to synthetic mole cricket song and thus exposed to up to 1.5 million infective-stage S. scapterisci during the spring and early summer mole cricket flight season for 2 consecutive years. Releases were made on 28 Florida golf courses and one sod farm. The nematode was established by exposing attracted mole cricket adults to infective-stage juvenile S. scapterisci held in moist sand (seven sites) and in damp upholstery foam (2 sites). Based on capture of nematode-infected mole crickets at least three months after release, S. scapterisci was established on eight of the golf courses and the sod farm.