Song pattern recognition and an auditory time window in the female bushcricket Ancistrura nigrovittata (Orthoptera: Phaneropteridae)

Mate finding in the phaneropterid bushcricket Ancistrura nigrovittata is achieved by a duet, where the female replies with a short sound to the male song. In experiments with artificial song models we analysed the parameters necessary for eliciting a female response. A verse of the male song consists of a group of 5–9 syllabes which after an interval of about 400 ms is followed by a final syllable. The female response was shown to depend on two processes: (i) recognition of the syllable group as belonging to a conspecific male and (ii) perception of the final syllable as a trigger. Critical parameters for the recognition process are the duration of syllables and syllable pauses, as well as the number of syllables in a group. However, even with an optimal syllable group, the response probability still depends on the interval between the syllable group and the final syllable. The female only responds when the final syllable of the male song occurs within a 250 ms long time window begining approximately 250 ms after the end of the male's syllable group. Her reply consists of a single tick, which follows the male's final syllable with a latency of only 25 ms.     

Diversity of intersegmental auditory neurons in a bush cricket

Various auditory interneurons of the duetting bush cricket Ancistrura nigrovittata with axons ascending to the brain are presented. In this species, more intersegmental sound-activated neurons have been identified than in any other bush cricket so far, among them a new type of ascending neuron with posterior soma in the prothoracic ganglion (AN4). These interneurons show not only morphological differences in the prothoracic ganglion and the brain, but also respond differently to carrier frequencies, intensity and direction. As a set of neurons, they show graded differences for all of these parameters. A response type not described among intersegmental neurons of crickets and other bush crickets so far is found in the AN3 neuron with a tonic response, broad frequency tuning and little directional dependence. All neurons, with the exception of AN3, respond in a relatively similar manner to the temporal patterns of the male song: phasically to high syllable repetitions and rhythmically to low syllable repetitions. The strongest coupling to the temporal pattern is found in TN1. In contrast to behavior the neuronal responses depend little on syllable duration. AN4, AN5 and TN1 respond well to the female song. AN4 (at higher intensities) and TN1 respond well to a complete duet.     

Processing of ultrasound in a bush cricket's brain

The processing and categorization of conspecific and heterospecific acoustic signals is an important task of the central nervous system. In orthopteran species, carrier frequency (besides temporal cues) is one of the major discriminators. In the bush cricket species Ancistrura nigrovittata Brunner von Wattenwyl (Phaneropteridae, Barbitistini), ultrasound has potentially different meanings and may elicit vastly different behaviours depending on the context it is perceived in. In the present study, data are presented of the morphology and neuronal responses of three local brain neurones (LBNs) that respond best to ultrasound. All neurones show dense arborizations in the lateral protocerebrum, where ascending interneurones terminate. The LBN2 and LBN9 neurones are entirely restricted to one side of the brain, whereas LBN5 crosses the midline, thereby linking both hemispheres. The response maxima for LBN2 overlap closely with the peak carrier frequencies found in a species‐specific duet, which consists of sonic (16 kHz, male), as well as ultrasonic (24–28 kHz, female) sound. By contrast, LBN9 responds only to ultrasound in the range of the female reply, whereas the male song induces exceptionally long‐lasting inhibition. The LBN5 neurone shows strongest spike activity to a broad range of ultrasonic frequencies, as long as the pulse duration remains short. All three brain neurones respond to ultrasound in a unique way and may be involved in the shaping of different behavioural outcomes.     

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.     

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.     

Ultrasonic singing by the blue-throated hummingbird: a comparison between production and perception

Blue-throated hummingbirds produce elaborate songs extending into the ultrasonic frequency range, up to 30 kHz. Ultrasonic song elements include harmonics and extensions of audible notes, non-harmonic components of audible syllables, and sounds produced at frequencies above 20 kHz without corresponding hearing range sound. To determine whether ultrasonic song elements function in intraspecific communication, we tested the hearing range of male and female blue-throated hummingbirds. We measured auditory thresholds for tone pips ranging from 1 kHz to 50 kHz using auditory brainstem responses. Neither male nor female blue-throated hummingbirds appear to be able to hear above 7 kHz. No auditory brainstem responses could be detected between 8 and 50 kHz at 90 dB. This high-frequency cutoff is well within the range reported for other species of birds. These results suggest that high-frequency song elements are not used in intraspecific communication. We propose that the restricted hummingbird hearing range may exemplify a phylogenetic constraint.     

Songs and the Function of Song Elements in Four Duetting Bushcricket Species (Ensifera, Phaneropteridae, Barbitistes)

The structure of male songs and the timing of female replies with respect to the male songs are described for four species of the palaearctic bushcricket genus Barbitistes (B. constrictus, B. ocskayi, B. serricauda, B. yersini). In a male song, 3 to 16 syllables form a chirp followed by a trigger syllable after a longer interval. The trigger syllable releases a female reply with a latency of 30 to 50 ms in all four species. In B. serricauda songs, there is no clearly separated trigger syllable. Instead, the first syllable of a chirp functions as a trigger syllable. Some B. serricauda males may produce a short female-type syllable just at the moment, when a female would reply. The possible function of such a syllable is acoustical mimicry. When comparing at least two song parameters, each species occupies a specific combination of values. According to the overlap of parameters a close phylogenetic relationship between B. constrictus and B. serricauda and between B. ocskayi and B. yersini is assumed. This interpretation is compared with a hypothesis based on morphological investigations.     

Directional hearing of a cicada: biophysical aspects

The directional hearing of male and female cicadas of the species Tympanistalna gastrica was investigated by means of laser vibrometry. The results show that the tympanic organs act as pressure difference receivers. This mechanism can produce left-right differences of more than 10 dB. The main acoustic inputs to the inner surfaces of the ears are the tympana, in males supplemented by the timbals, and by the third spiracles in females. In addition the hollow abdomen of males seems to play a minor role. Tympanic membrane input is the source of left-right differences in the tympanic vibration velocity at frequencies below 9 kHz in males and below 15–18 kHz in females. The input via the (contralateral) timbal in males is responsible for a null in vibration velocity appearing between 12 and 14 kHz when the sound is coming from the contralateral direction. The highest energy components of the calling song are found in this frequency range. The mechanical sensitivity of the ears depends upon the sex. At low frequencies males are about 10 dB more sensitive than females.     

Seasonality in song behaviour revisited: seasonal and annual variants and invariants in the song of the domesticated canary (Serinus canaria)

The song of the domesticated canary (Serinus canaria) is one of the most widely used models to study the neural correlates of behavioural plasticity and the mechanisms of female mate choice. However, only few studies have described the song behaviour in detail and monitored their changes throughout the year, and these data are restricted to the “Waterslager” strain. Here, we studied the song characteristics of the male common domesticated canary at different times of the year, the spring breeding and autumnal non-breeding season, and monitored the birds' songs up to the following breeding season. During breeding, males have increased plasma levels of testosterone, and songs are on average longer and consist of fewer non-repeated syllable types compared to the non-breeding season. When subsequent seasons are compared, song duration and the proportion of non-repeated syllable types change seasonally but not across years. Repertoire size remains constant throughout seasons although syllable types are exchanged. Syllable carry-over is significantly higher from one breeding season to the next than between the breeding and non-breeding season. Further, the repertoire of the breeding season contains more potentially sexually attractive syllable types than that of the non-breeding season. These data show that overall song structure is retained throughout the year while seasonality occurs in the temporal pattern and in repertoire composition.     

Prolonged response to calling songs by the L3 auditory interneuron in female crickets (Acheta domesticus): possible roles in regulating phonotactic threshold and selectiveness for call carrier frequency

L3, an auditory interneuron in the prothoracic ganglion of female crickets (Acheta domesticus) exhibited two kinds of responses to models of the male's calling song (CS): a previously described, phasically encoded immediate response; a more tonically encoded prolonged response. The onset of the prolonged response required 3-8 sec of stimulation to reach its maximum spiking rate and 6-20 sec to decay once the calling song ceased. It did not encode the syllables of the chirp. The prolonged response was sharply selective for the 4-5 kHz carrier frequency of the male's calling songs and its threshold tuning matched the threshold tuning of phonotaxis, while the immediate response of the same neuron was broadly tuned to a wide range of carrier frequencies. The thresholds for the prolonged response covaried with the changing phonotactic thresholds of 2- and 5-day-old females. Treatment of females with juvenile hormone reduced the thresholds for both phonotaxis and the prolonged response by equivalent amounts. Of the 3 types of responses to CSs provided by the ascending L1 and L3 auditory interneurons, the threshold for L3's prolonged response, on average, best matched the same females phonotactic threshold. The prolonged response was stimulated by inputs from both ears while L3's immediate response was driven only from its axon-ipsilateral ear. The prolonged response was not selective for either the CS's syllable period or chirp rate.     

Response properties of the prothoracic AN2 auditory interneurone to model calling songs in the cricket Gryllus bimaculatus

Sound processing properties for calling song (CS) models, as described for the prothoracic L3 auditory neurone in Acheta domesticus, are investigated for the homologous auditory neurone 2 (AN2) in female Gryllus bimaculatus De Geer. AN2 of G. bimaculatus responds selectively to the syllable period (SP) of models of a male CS. The selectiveness of this response parallels the selectivity of phonotaxis females perform in response to the same SPs. Both, the responses of AN2 and female behaviour show clear interindividual variability. The SP‐selective responses of AN2 result from an SP‐dependent reduction in the spiking to subsequent syllables of the model CSs, measured as the percentage decrement. This SP‐dependent response does not primarily result from inbuilt properties of the AN2 membrane. Rather, it is dependent on inhibitory input to the AN2. However, clear inhibitory postsynaptic potentials in dendritic recordings of the AN2 are not encountered. This immediate response of AN2 to CSs is followed by an increased rate of tonic firing between stimulus CSs, which is termed the prolonged response, and is dependent on the carrier frequencies that make up the male CSs. With stimulation on the contralateral side of the soma of AN2s, more than 50% of AN2s exhibit a prolonged response. However, with stimulation from the ipsilateral side of the soma, most AN2s exhibit a prolonged response. The prolonged response of AN2 at 5 kHz may be even more sensitive than the immediate response. Thus, the AN2 neurone could provide a basis for phonotaxis that is selective for both the SPs and the carrier frequencies of potentially attractive calling songs.     

Neuronal basis for spectral song discrimination in the bushcricket Tettigonia cantans

Previous experiments demonstrated that in choice situations female Tettigonia cantans prefer signals with the conspecific spectrum over signals with the spectrum of the sibling species T. viridissima, whose signals lack the T. cantans-typical 8-kHz component but are otherwise identical in spectral composition. The underlying neuronal mechanisms were investigated using whole-nerve recordings of the tympanal nerve. Hearing thresholds did not differ significantly between the species in the range between 7 and 25 kHz. The responses of the tympanic nerve at 30 dB above threshold did, however, differ significantly between the species. While in T. viridissima response amplitudes did not differ between 7 and 12 kHz, in T. cantans responses at 8 kHz were significantly larger than at 10 and 12 kHz. Since possible influences of axonal diameters on response magnitudes were excluded, these results indicate that in T. cantans more receptor cells are tuned to 8 kHz than to 10–12 kHz, while in T. viridissima tuning of receptor cells is more evenly distributed. The higher response magnitude in T. cantans at 8 kHz than at 10–12 kHz is equivalent to an amplitude difference of 3.8–7 dB, which agrees well with previous behavioural estimates. Accepted: 13 January 1999     

Tympanic and extratympanic sound transmission in the leopard frog

Summary The inner ear of the leopard frog,Rana pipiens, receives sound via two separate pathways: the tympanic-columellar pathway and an extratympanic route. The relative efficiency of the two pathways was investigated. Laser interferometry measurements of tympanic vibration induced by free-field acoustic stimulation reveal a broadly tuned response with maximal vibration at 800 and 1500 Hz. Vibrational amplitude falls off rapidly above and below these frequencies so that above 2 kHz and below 300 Hz tympanic vibration is severely reduced. Electrophysiological measurements of the thresholds of single eighth cranial nerve fibers from both the amphibian and basilar papillae in response to pure tones were made in such a way that the relative efficiency of tympanic and extratympanic transmission could be assessed for each fiber. Thresholds for the two routes are very similar up to 1.0 kHz, above which tympanic transmission eventually becomes more efficient by 15–20 dB. By varying the relative phase of the two modes of stimulation, a reduction of the eighth nerve response can be achieved. When considered together, the measurements of tympanic vibration and the measurements of tympanic and extratympanic transmission thresholds suggest that under normal conditions in this species (1) below 300 Hz extratympanic sound transmission is the main source of inner ear stimulation; (2) for most of the basilar papilla frequency range (i.e., above 1.2 kHz) tympanic transmission is more important; and (3) both routes contribute to the stimulation of amphibian papilla fibers tuned between those points. Thus acoustic excitation of the an uran's inner ear depends on a complex interac tion between tympanic and extratympanic sound transmission.Abbreviations dB SPL decibels sound pressure level re: 20 N/ m² - AP amphibian papilla - BP basilar papilla - BEF best excitatory frequency     

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.     

Female phonotaxis and frequency discrimination in the bushcricket Requena verticalis

ABSTRACT. The male bushcricket, Requena verticalis , calls with a signal containing two predominant frequencies, 16 kHz and 28 kHz. A synthesized call, made from a template of the natural call, was played to females under conditions of a two-speaker trial on a flat arena. Orientation pathways to a speaker emitting only a 16 kHz signal were more circuitous than the pathways made by females orientating to a speaker emitting only a 28 kHz signal. Females preferred a signal with both carrier frequency peaks present within the song to a signal with only a 16 kHz or 28 kHz carrier frequency, when the signal containing a double peak was kept at equivalent absolute intensity to that with a single peak. Females chose signals containing a more powerful high frequency peak over a signal in which both peaks were balanced. For the higher peak, they were able to differentiate between frequencies with a separation of 8 kHz but not of 4 kHz. They were unable to differentiate between frequencies with a separation up to 8 kHz in the lower peak when one frequency was held at 16 kHz; however, when this frequency was held at 18 kHz, females were able to distinguish between frequencies with a difference of 4 kHz. ( N.B. 18 kHz is 2 kHz above the mean value for this frequency within the natural population.) We conclude that females are choosing males on the amount of power in the higher frequency range of their song and that this may be equivalent to a close calling male in the field.     

Sound production in some triatomine bugs

ABSTRACT. Adults of five species of Triatominae were found to stridulate when handled: Triatoma protracta, T. lenti, T. infestans, Panstrongylus megistus and Dipetalogaster maximus. All five larval stages of D. maximus were also found to stridulate. Stridulation is caused by the tip of the reflexed proboscis rubbing along the transversely ridged prosternal groove. Each syllable of the resulting song is produced by a single antero-posterior movement of the proboscis and contains 80–150 intrasyllabic spikes, each corresponding to the striking of a single ridge in the prosternal groove. Analysis of tape recordings of the songs showed that all species have a broad frequency band without well-defined maxima, extending into the ultrasonic with frequencies of up to 50–100 kHz. The lowest frequency produced by each species is consistent with the repetition rate of the striking of prosternal ridges by the proboscis. No behavioural response to the replayed song was detected, but when the song was replayed to female P. megistus the frequency of action potentials within the antennal nerve correlated well with the intrasyllabic spike frequency of the replayed song. Possible microphonic artefacts were not, however, excluded. Possible functions of the song are discussed.     

Middle-ear development

Laser interferometry was used to measure umbo velocity in the developing BALB/c mouse middle ear at 133 pure-tone frequencies between 2.0 kHz and 40.0 kHz, all at a constant 100 dB sound pressure level. Umbo velocities increased with age across the entire frequency range, and reached adult-like levels by about 19 days between 2.0 and 22.0 kHz. Velocities at 28.0 and 34.0 kHz took 27 and 52 days respectively to reach adult-like levels.A simple middle-ear model utilizing compliance, resistance, and inertia elements matched the general trends of our velocity results and provided an indication of the anatomical basis for the growth in umbo velocity. The model suggested that velocity development at the lowest frequencies may be attributed to increases in tympanic membrane compliance. The model also indicated that both the frictional resistance of the middle ear and the inertia of the tympanic membrane and ossicles decreased during the growth period.At frequencies below 20.0 kHz, age-related increases in umbo velocity coincided with improvements in Nj₁ thresholds recorded from the round window and evoked potential thresholds obtained from the cochlear nucleus. These results indicated that the functional development of the middle-ear plays a major role in the development of hearing in the mouse.Portions of this work were presented at the Fifteenth Meeting of the Association for Research in Otolaryngology