Signalling through acoustic windows: nightingales avoid interspecific competition by short-term adjustment of song timing

The function of bird song is closely linked to sexual selection through female choice and male–male competition, and thus variation in communication success is likely to have major fitness consequences for a singing male. A crucial constraint on signal transmission is imposed by background noise, which may include songs from other species. I investigated whether singing nightingales (Luscinia megarhynchos) avoid temporal overlap with the songs of other bird species in a playback experiment. I analysed the temporal song patterns of six males, each of which were exposed to songs of other species. The nightingales significantly avoided overlapping their songs with the playback songs, and started singing preferentially during the silent intervals between the heterospecific songs. This timing of song onset produced a greater variability in pause duration compared to the nightingales’ undisturbed solo singing. These findings suggest that birds adjust their song timing to avoid acoustic interference on short temporal scales, and thus are able to improve the efficiency of acoustic communication in complex sonic environments. Moreover, the results indicate that temporal song patterns can be affected by the songs of other species, and thus such influences should be taken into account when studying bird song in the field.     

Antiphonal call timing in marmosets is behaviorally significant: interactive playback experiments

Studies of primate vocal communication systems have generally focused on vocalizations and the information they convey to conspecifics. But the vocalizations are not the only sources of information. Aspects of each species vocal behaviors are likely to be communicatively rich as well. During vocal interactions, for example, the latency delay between the calls could communicate an important message to the signal receiver, such as an interest and willingness to socialize. Here we employed novel, interactive playback software to address this issue in the antiphonal calling behavior of common marmosets. In these experiments, we parametrically varied the latency delay of antiphonal call stimuli and measured its effects on subjects’ resultant vocal behavior. Results showed that marmosets produced successively fewer antiphonal call responses during test conditions with increasing latency delays. Moreover, although subjects produced significantly more antiphonal than spontaneous calls in conditions with antiphonal call timing delays up to 9 s, a longer delay resulted in a significant decline in calling. These data suggest that antiphonal call timing is a salient cue for maintaining antiphonal calling interactions and may be used by marmosets to determine whether a subsequent call is produced in response to or independently of their own.     

Variable asymmetry and resonance in the avian vocal tract: a structural basis for individually distinct vocalizations

The social vocalizations of the oilbird (Steatornis caripensis) frequently have their acoustic energy concentrated into 3 prominent formants which appear to arise from the filter properties of their asymmetrical vocal tract with its bronchial syrinx. The frequency of the second and third formants approximate the predicted fundamental resonances of the unequal left and right cranial portions of each primary bronchus, respectively. Reversibly plugging either bronchus eliminates the corresponding formant. The first formant may arise in the trachea. The degree of vocal tract asymmetry varies between individuals, endowing them with different formant frequencies and providing potential acoustic cues by which individuals of this nocturnal, cave dwelling species may recognize each other in their dark, crowded colonies.     

Selective phonotaxis in <Emphasis Type="Italic">Neoconocephalus nebrascensis</Emphasis> (Orthoptera: Tettigoniidae): call recognition at two temporal scales

The calls of many Orthopteran species are comprised of a simple trill of pulses, the temporal pattern of which is important for call recognition. Male Neoconocephalus nebrascensis produce pulses with a temporal structure typical for the genus. However, they modify this pattern by grouping their pulses into verses, thereby creating a higher order temporal structure. The importance of the pulse pattern and verse structure for call recognition in N. nebrascensis was determined using a walking compensator. Females required the conspecific pulse pattern for call recognition, responding only when the intervals between pulses were short or absent. Females also required the verse structure for call recognition, and recognized the verse structure only when the amplitude modulation depth between verses and pauses exceeded 18 dB. We discuss that the verse recognition mechanism is a derived trait adapted for pre-mating isolation. We hypothesize that the unusually large amplitude modulation required for verse recognition forces males to synchronize their calls in order to preserve an attractive pattern. Call synchrony appears to be the outcome of cooperation, rather than competition, in this species.     

Multiple acoustic features underlie vocal signal recognition in tamarins: antiphonal calling experiments

We examine which acoustic features are relevant for recognition of the cotton-top tamarin (Saguinus oedipus) combination long-call. This vocalization, emitted by both males and females, functions in maintaining group cohesion, territory defense and mate attraction. Using the tamarins natural antiphonal vocal response to hearing a combination long-call as the primary measure of recognition, we presented subjects with synthetic exemplars of combination long-calls in which we manipulated across one of three acoustic dimensions: frequency, time and amplitude. Results indicated that although acoustic features in the frequency and time domains are important for combination long-call recognition, the changes in amplitude within and between syllables are not. Furthermore, while the fundamental frequency appears to be the used to encode information about the frequency contour, the temporal information is derived from the harmonics. Overall, these results suggest that tamarins use a specific suite of acoustic features for combination long-call recognition.Abbreviations CLC combination long-call - F0 fundamental frequency - JND just noticeable difference - JMD just meaningful difference - IPI inter-pulse interval     

Peripheral encoding of behaviorally relevant acoustic signals in a vocal fish: single tones

The midshipman fish, Porichthys notatus, generates acoustic signals for intraspecific communication. Nesting males produce long-duration “hums” which attract gravid females and can be effectively mimicked by pure tones. In this study we examine the encoding of tonal signals by the midshipman peripheral auditory system. Single-unit recordings were made from afferents innervating the sacculus while presenting sounds via an underwater loudspeaker. Units were characterized by iso-intensity spike rate and vector strength of synchronization curves, as well as by peri-stimulus time histograms. Additionally, response-intensity curves and responses to long-duration (up to 10 s) stimuli were obtained. As has been seen in other teleosts, afferents had highly variable activity profiles. Excitatory frequencies ranged from 60 to over 300 Hz with most units responding best around 70 or 140 Hz. Thresholds at 90 Hz ranged from 95 to 145 dB re 1 μPa. Strong synchronization provided a robust temporal code of frequency, comparable to that described for goldfish. Spike rate showed varying degrees of adaptation but high rates were generally maintained even for 10-s stimuli. The midshipman peripheral auditory system is well suited to encoding conspecific communication signals, but nonetheless shares many response patterns with the auditory system of other teleosts. Accepted: 10 February 1999     

Visual and acoustic communication in non-human animals: a comparison

The visual and auditory systems are two major sensory modalities employed in communication. Although communication in these two sensory modalities can serve analogous functions and evolve in response to similar selection forces, the two systems also operate under different constraints imposed by the environment and the degree to which these sensory modalities are recruited for non-communication functions. Also, the research traditions in each tend to differ, with studies of mechanisms of acoustic communication tending to take a more reductionist tack often concentrating on single signal parameters, and studies of visual communication tending to be more concerned with multivariate signal arrays in natural environments and higher level processing of such signals. Each research tradition would benefit by being more expansive in its approach.     

Discrimination of jittered sonar echoes by the echolocating bat,Eptesicus fuscus: The shape of target images in echolocation

1. Behavioral experiments with jittering echoes examined acoustic images of sonar targets in the echolocating bat, Eptesicus fuscus, along the echo delay or target range axis. Echo phase, amplitude, bandwidth, and signal-to-noise ratio were manipulated to assess the underlying auditory processes for image formation. 2. Fine delay acuity is about 10 ns. Calibration and control procedures indicate that this represents temporal acuity rather than spectral discrimination. Jitter discrimination curves change in phase when the phase of one jittering echo is shifted by 180 degrees relative to the other, showing that echo phase is involved in delay estimation. At an echo detectability index of about 36 dB, fine acuity is 40 ns, which is approximately as predicted for the delay accuracy of an ideal receiver. 3. Compound performance curves for 0 degrees and 180 degrees phase conditions match the crosscorrelation function of the echoes. The locations of both 0 degrees and 180 degrees phase peaks in the performance curves shift along the time axis by an amount that matches neural amplitude-latency trading in Eptesicus, confirming a temporal basis for jitter discrimination.     

Grouping in auditory temporal perception and vocal production is mutually adapted: the case of wriggling calls of mice

Auditory Gestalt perception by grouping of species-specific vocalizations to a perceptual stream with a defined meaning is typical for human speech perception but has not been studied in non-human mammals so far. Here we use synthesized models of vocalizations (series of wriggling calls) of mouse pups (Mus domesticus) and show that their mothers perceive the call series as a meaningful Gestalt for the release of instinctive maternal behavior, if the inter-call intervals have durations of 100–400 ms. Shorter or longer inter-call intervals significantly reduce the maternal responsiveness. We also show that series of natural wriggling calls have inter-call intervals mainly in the range of 100–400 ms. Thus, series of natural wriggling calls of pups match the time-domain auditory filters of their mothers in order to be optimally perceived and recognized. A similar time window exists for the production of human speech and the perception of series of sounds by humans. Neural mechanisms for setting the boundaries of the time window are discussed.     

At the interface of the auditory and vocal motor systems: NIf and its role in vocal processing,production and learning

Communication between auditory and vocal motor nuclei is essential for vocal learning. In songbirds, the nucleus interfacialis of the nidopallium (NIf) is part of a sensorimotor loop, along with auditory nucleus avalanche (Av) and song system nucleus HVC, that links the auditory and song systems. Most of the auditory information comes through this sensorimotor loop, with the projection from NIf to HVC representing the largest single source of auditory information to the song system. In addition to providing the majority of HVC’s auditory input, NIf is also the primary driver of spontaneous activity and premotor-like bursting during sleep in HVC. Like HVC and RA, two nuclei critical for song learning and production, NIf exhibits behavioral-state dependent auditory responses and strong motor bursts that precede song output. NIf also exhibits extended periods of fast gamma oscillations following vocal production. Based on the converging evidence from studies of physiology and functional connectivity it would be reasonable to expect NIf to play an important role in the learning, maintenance, and production of song. Surprisingly, however, lesions of NIf in adult zebra finches have no effect on song production or maintenance. Only the plastic song produced by juvenile zebra finches during the sensorimotor phase of song learning is affected by NIf lesions. In this review, we carefully examine what is known about NIf at the anatomical, physiological, and behavioral levels. We reexamine conclusions drawn from previous studies in the light of our current understanding of the song system, and establish what can be said with certainty about NIf’s involvement in song learning, maintenance, and production. Finally, we review recent theories of song learning integrating possible roles for NIf within these frameworks and suggest possible parallels between NIf and sensorimotor areas that form part of the neural circuitry for speech processing in humans.     

Explosive vocal activity for attracting human attention is related to domestication in silver fox

Domestication affects behavioral and vocal responses, involved in communication with humans; in particular, those that attract human attention. In this study, we found that silver foxes of Tame strain, experimentally domesticated for a few tenses of generation, displayed bursts of vocal activity during the first minute after appearance of an unfamiliar human, that faded quickly during the remaining time of the test, when the experimenter stayed passively before the cage. Distinctively, foxes of Aggressive strain, artificially selected for tenses of generation for aggressive behavior toward humans, and the control group of Unselected for behavior silver foxes kept steady levels of vocal activity for the duration of the tests. We found also that Aggressive foxes vocalized for a larger proportion of time than Unselected foxes for all 5 min of the test. We discuss the obtained data in relation to proposal effects of domestication on mechanisms directed to involving people into human-animal interactions and structural similarity between human laughter and vocalization of Tame foxes.     

Lung mediated auditory contrast enhancement improves the Signal-to-noise ratio for communication in frogs

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Acoustic communication in the Kittiwake <Emphasis Type=Italic>Rissa tridactyla</Emphasis>: potential cues for sexual and individual signatures in long calls

Sex and individual recognition systems vary among species and can have various functions in different contexts. In order to determine the basis of identification by voice in the Kittiwake (Rissa tridactyla), the greeting calls of 32 individuals (18 males and 14 females) were recorded in May–June 2004 on the Kittiwake colony of Hornøya island (Barents sea) and analysed. On the basis of coefficient of variation calculations and discriminant analyses, we show (1) that calls are sexually dimorphic and that the dimorphism is mainly based on the value of the fundamental frequency, and (2) that calls are individually distinct, individuality being due to a complex of temporal and frequency parameters located in different parts of the signal. This coding strategy is discussed in the context of the colonial breeding habitat of the species.     

The role of vocal self-stimulation in female responses to males: implications for state-reading

As research neurobiologists, we pursue specific questions, and the answers rendered are also correspondingly specific. Our goal, however, is to understand an entire system or the whole organism. To that end, it is not only useful, but sometimes also necessary, that we periodically reappraise a body of specific data in light of current knowledge of the field at large. In this spirit, the present paper reviews my work on the neural and hormonal mechanisms underlying the reproductive system of ring doves and others' studies of songbirds. By integrating these fields I then advance the concept that inherent in the avian breeding system is the mechanism of "state-reading" (a term fashioned after "mindreading", which was coined by cognitive neuroscientists). State-reading helps to coordinate a sequence of endocrine and behavioral events to realize a desired objective, in this case, successful reproduction.     

Seasonal variation in avian auditory evoked responses to tones: a comparative analysis of Carolina chickadees,tufted titmice,and white-breasted nuthatches

We tested for seasonal plasticity of the peripheral auditory system of three North American members of the Sylvioidea: Carolina chickadees (Poecile carolinensis), tufted titmice (Baeolophus bicolor), and white-breasted nuthatches (Sitta carolinensis). We measured three classes of auditory evoked responses (AER) to tone stimuli: sustained receptor/neural responses to pure-tone condensation waveforms, the frequency-following response (FFR), and the earliest peak of the AER to stimulus onset (tone onset response). Seasonal changes were detected in all classes of AERs in chickadees and nuthatches. Seasonal changes in titmice were restricted to the tone onset response. Interestingly, changes detected in chickadees (and to a lesser extent in titmice) were generally in an opposite direction to changes seen in nuthatches, with chickadees exhibiting greater amplitude AER responses in the spring than in winter, and nuthatches exhibiting greater amplitude AER responses in winter than in spring. In addition, the seasonal differences in the sustained responses tended to be broad-band in the chickadees but restricted to a narrower frequency range in nuthatches. In contrast, seasonal differences in the onset response were over a broader frequency range in titmice than in chickadees and nuthatches. We discuss some possible mechanistic and functional explanations for these seasonal changes.     

Mother is not like mother: Concurrent pregnancy reduces lactating guinea pigs’ responsiveness to pup calls

Offspring signalling can serve to communicate need to the parents and thus influence parental readiness to provide care. Offspring stimuli that affect parental care have been investigated extensively. Yet much less is known about the mechanisms leading to a decline in maternal motivation when conflicts of provisioning current and future offspring may arise. Here we tested responses by pregnant and non-pregnant female guinea pigs (Cavia aperea f. porcellus) to playback of pup calls during their period of lactation for dependent offspring. Most concurrently pregnant and lactating females did not respond to pup calls, whereas non-pregnant lactating females responded strongly. Our findings expand on previous studies by showing that female behavioural responsiveness to pup stimuli is strongly reduced by concurrent pregnancy and lactation. These instantaneous measurements of female responsiveness to young show more directly than standard measures like nursing performance or time to weaning how female motivation to care for current offspring is diminished by simultaneous gestation.     

Instant messages vs. speech: hormones and why we still need to hear each other

Human speech evidently conveys an adaptive advantage, given its apparently rapid dissemination through the ancient world and global use today. As such, speech must be capable of altering human biology in a positive way, possibly through those neuroendocrine mechanisms responsible for strengthening the social bonds between individuals. Indeed, speech between trusted individuals is capable of reducing levels of salivary cortisol, often considered a biomarker of stress, and increasing levels of urinary oxytocin, a hormone involved in the formation and maintenance of positive relationships. It is not clear, however, whether it is the uniquely human grammar, syntax, content and/or choice of words that causes these physiological changes, or whether the prosodic elements of speech, which are present in the vocal cues of many other species, are responsible. In order to tease apart these elements of human communication, we examined the hormonal responses of female children who instant messaged their mothers after undergoing a stressor. We discovered that unlike children interacting with their mothers in person or over the phone, girls who instant messaged did not release oxytocin; instead, these participants showed levels of salivary cortisol as high as control subjects who did not interact with their parents at all. We conclude that the comforting sound of a familiar voice is responsible for the hormonal differences observed and, hence, that similar differences may be seen in other species using vocal cues to communicate.