Formant Frequencies are Acoustic Cues to Caller Discrimination and are a Weak Indicator of the Body Size of Corncrake Males

Source–filter theory assumes that calls are generated by a vocal source and are subsequently filtered by the vocal tract. The air in the vocal tract vibrates preferentially at certain resonant frequencies, called formants. Formant frequencies can be a good indicator of the caller's characteristics, such as sex, age, body size or individual identity. Although source–filter theory was originally proposed for mammals, formants are also observed in birds, and some bird species have been shown to perceive formants. In this study, we evaluated the hypotheses that formant frequencies (1) are an indicator of body size and (2) can be used for individual discrimination by a nocturnal bird species, the corncrake (Crex crex). We analysed calls of 104 males from Poland and the Czech Republic. Linear regression models showed that the males with a longer head (including the bill length) had a significantly lower formant dispersion and lower fourth and fifth formant frequencies. However, we found no significant relationships between body weight and any filter‐related acoustic measurement. The formant frequencies had smaller within‐ than between‐individual coefficients of variation. This characteristic of the formant frequencies implies a high potential for individual coding. A discriminant function analysis correctly assigned 94.8% of the calls to the caller based on formants from second to fifth. Our results indicated that the formant frequencies are a weak indicator of the body size of the sender in the corncrake. However, even weak dependence between body size and acoustic properties of signal may be important in natural selection process. Alternatively, such a weak dependence may be observed, because receivers ignore the acoustical, formant‐based cues of body size. Simultaneously, the formants might potentially provide acoustic cues to individual discrimination and could be used to census and monitoring tasks.     

Vocal Tract Morphology Determines Species-Specific Features in Vocal Signals of Lemurs (Eulemur)

The source-filter theory describes vocal production as a two-stage process involving the generation of a sound source, with its own spectral structure, which is then filtered by the resonant properties of the vocal tract. This theory has been successfully applied to the study of animal vocal signals since the 1990s. As an extension, models reproducing vocal tract resonance can be used to reproduce formant patterns and to understand the role of vocal tract filtering in nonhuman vocalizations. We studied three congeneric lemur species —Eulemur fulvus, E. macaco, E. rubriventer— using morphological measurements to build computational models of the vocal tract to estimate formants, and acoustic analysis to measure formants from natural calls. We focused on call types emitted through the nose, without apparent articulation. On the basis of anatomical measurements, we modeled the vocal tract of each species as a series of concatenated tubes, with a cross-sectional area that changed along the tract to approximate the morphology of the larynx, the nasopharyngeal cavity, the nasal chambers, and the nostrils. For each species, we calculated the resonance frequencies in 2500 randomly generated vocal tracts, in which we simulated intraspecific length and size variation. Formant location and spacing showed significant species-specific differences determined by the length of the vocal tract. We then measured formants of a set of nasal vocalizations (“grunts”) recorded from captive lemurs of the same species. We found species-specific differences in the natural calls. This is the first evidence that morphology of the vocal tract is relevant in generating filter-related acoustic cues that potentially provide receivers with information about the species of the emitter.     

Red deer stags use formants as assessment cues during intrasexual agonistic interactions

While vocal tract resonances or formants are key acoustic parameters that define differences between phonemes in human speech, little is known about their function in animal communication. Here, we used playback experiments to present red deer stags with re-synthesized vocalizations in which formant frequencies were systematically altered to simulate callers of different body sizes. In response to stimuli where lower formants indicated callers with longer vocal tracts, stags were more attentive, replied with more roars and extended their vocal tracts further in these replies. Our results indicate that mammals other than humans use formants in vital vocal exchanges and can adjust their own formant frequencies in relation to those that they hear.     

Retraction of the mobile descended larynx during groaning enables fallow bucks (Dama dama) to lower their formant frequencies

A permanently descended larynx is found in humans and several other species of mammals. In addition to this, the larynx of species such as fallow deer is mobile and in males it can be retracted during vocalization. The most likely explanation for the lowered retractable larynx in mammals is that it serves to exaggerate perceived body size (size exaggeration hypothesis) by decreasing the formant frequencies of calls. In this study, we quantified for the first time the elongation of the vocal tract in fallow bucks during vocalization. We also measured the effect of this vocal tract length (VTL) increase on formant frequencies (vocal tract resonances) and formant dispersion (spacing of formants). Our results show that fallow bucks increase their VTL on average by 52% during vocalization. This elongation resulted in strongly lowered formant frequencies and decreased formant dispersion. There were minimal changes to formants 1 and 2 (−0.91 and +1.9%, respectively) during vocal tract elongation, whereas formants 3, 4 and 5 decreased substantially: 18.9, 10.3 and 13.6%, respectively. Formant dispersion decreased by 12.4%. Formants are prominent in deer vocalizations and are used by males to gain information on the competitive abilities of signallers. It remains to be seen whether females also use the information that formants contain for assessing male quality before mating.     

Visualizing Sound Emission of Elephant Vocalizations: Evidence for Two Rumble Production Types

Recent comparative data reveal that formant frequencies are cues to body size in animals, due to a close relationship between formant frequency spacing, vocal tract length and overall body size. Accordingly, intriguing morphological adaptations to elongate the vocal tract in order to lower formants occur in several species, with the size exaggeration hypothesis being proposed to justify most of these observations. While the elephant trunk is strongly implicated to account for the low formants of elephant rumbles, it is unknown whether elephants emit these vocalizations exclusively through the trunk, or whether the mouth is also involved in rumble production. In this study we used a sound visualization method (an acoustic camera) to record rumbles of five captive African elephants during spatial separation and subsequent bonding situations. Our results showed that the female elephants in our analysis produced two distinct types of rumble vocalizations based on vocal path differences: a nasally- and an orally-emitted rumble. Interestingly, nasal rumbles predominated during contact calling, whereas oral rumbles were mainly produced in bonding situations. In addition, nasal and oral rumbles varied considerably in their acoustic structure. In particular, the values of the first two formants reflected the estimated lengths of the vocal paths, corresponding to a vocal tract length of around 2 meters for nasal, and around 0.7 meters for oral rumbles. These results suggest that African elephants may be switching vocal paths to actively vary vocal tract length (with considerable variation in formants) according to context, and call for further research investigating the function of formant modulation in elephant vocalizations. Furthermore, by confirming the use of the elephant trunk in long distance rumble production, our findings provide an explanation for the extremely low formants in these calls, and may also indicate that formant lowering functions to increase call propagation distances in this species''.     

Age Differences in the Responses to Adult and Juvenile Alarm Calls by Bonnet Macaques (Macaca radiata)

This study examined the differential responses to alarm calls from juvenile and adult wild bonnet macaques ( Macaca radiata ) in two parks in southern India. Field studies of several mammalian species have reported that the alarm vocalizations of immature individuals are often treated by perceivers as less provocative than those of adults. This study documents such differences in response using field-recorded playbacks of juvenile and adult alarm vocalizations. To validate the use of playback vocalizations as proxies of natural calls, we compared the responses of bonnet macaques to playbacks of alarm vocalizations with responses engendered by natural alarm vocalizations. We found that the frequency of flight, latency to flee, and the frequency of scanning to vocalization playbacks and natural vocalizations were comparable, thus supporting the use of playbacks to compare the effects of adult and juvenile calls. Our results showed that adult alarm calls were more provocative than juvenile alarm calls, inducing greater frequencies of flight with faster reaction times. Conversely, juvenile alarm calls were more likely to engender scanning by adults, a result interpreted as reflecting the lack of reliability of juvenile calls. Finally, we found age differences in flight behavior to juvenile alarm calls and to playbacks of motorcycle engine sounds, with juveniles and subadults more likely to flee than adults after hearing such sounds. These findings might reflect an increased vulnerability to predators or a lack of experience in young bonnet macaques.     

Behavioral responses to species-specific warning calls in infant squirrel monkeys reared in social isolation

Six infant squirrel monkeys were reared in social isolation. They responded differentially to playbacks of two species-specific alarm calls. The reaction to the alarm peep, the warning call to bird predators, was a prompt flight to the mother surrogate and essentially resembled the respective behavior of mother-reared infants. The responses to yapping, the alarm call to terrestrial predators, were less clear-cut and habituated soon. However, when yapping was played back in connection with the presentation of a reference object, both subjects tested in this way clearly avoided the object and preferred contact with the mother surrogate while they thoroughly explored an object presented with a control tone. From this it can be concluded that the perception of both alarm calls is innate. In addition, the method of behavior-contingent playback of vocalizations simulates the learning process by which the visual perception of terrestrial predators of the habitat is acquired.     

Free-Ranging Male Koalas Use Size-Related Variation in Formant Frequencies to Assess Rival Males

Although the use of formant frequencies in nonhuman animal vocal communication systems has received considerable recent interest, only a few studies have examined the importance of these acoustic cues to body size during intra-sexual competition between males. Here we used playback experiments to present free-ranging male koalas with re-synthesised bellow vocalisations in which the formants were shifted to simulate either a large or a small adult male. We found that male looking responses did not differ according to the size variant condition played back. In contrast, male koalas produced longer bellows and spent more time bellowing when they were presented with playbacks simulating larger rivals. In addition, males were significantly slower to respond to this class of playback stimuli than they were to bellows simulating small males. Our results indicate that male koalas invest more effort into their vocal responses when they are presented with bellows that have lower formants indicative of larger rivals, but also show that males are slower to engage in vocal exchanges with larger males that represent more dangerous rivals. By demonstrating that male koalas use formants to assess rivals during the breeding season we have provided evidence that male-male competition constitutes an important selection pressure for broadcasting and attending to size-related formant information in this species. Further empirical studies should investigate the extent to which the use of formants during intra-sexual competition is widespread throughout mammals.     

Are men better than women at acoustic size judgements?

Formants are important phonetic elements of human speech that are also used by humans and non-human mammals to assess the body size of potential mates and rivals. As a consequence, it has been suggested that formant perception, which is crucial for speech perception, may have evolved through sexual selection. Somewhat surprisingly, though, no previous studies have examined whether sexes differ in their ability to use formants for size evaluation. Here, we investigated whether men and women differ in their ability to use the formant frequency spacing of synthetic vocal stimuli to make auditory size judgements over a wide range of fundamental frequencies (the main determinant of vocal pitch). Our results reveal that men are significantly better than women at comparing the apparent size of stimuli, and that lower pitch improves the ability of both men and women to perform these acoustic size judgements. These findings constitute the first demonstration of a sex difference in formant perception, and lend support to the idea that acoustic size normalization, a crucial prerequisite for speech perception, may have been sexually selected through male competition. We also provide the first evidence that vocalizations with relatively low pitch improve the perception of size-related formant information.     

Bee Threat Elicits Alarm Call in African Elephants

Unlike the smaller and more vulnerable mammals, African elephants have relatively few predators that threaten their survival. The sound of disturbed African honeybees Apis meliffera scutellata causes African elephants Loxodonta africana to retreat and produce warning vocalizations that lead other elephants to join the flight. In our first experiment, audio playbacks of bee sounds induced elephants to retreat and elicited more head-shaking and dusting, reactive behaviors that may prevent bee stings, compared to white noise control playbacks. Most importantly, elephants produced distinctive “rumble” vocalizations in response to bee sounds. These rumbles exhibited an upward shift in the second formant location, which implies active vocal tract modulation, compared to rumbles made in response to white noise playbacks. In a second experiment, audio playbacks of these rumbles produced in response to bees elicited increased headshaking, and further and faster retreat behavior in other elephants, compared to control rumble playbacks with lower second formant frequencies. These responses to the bee rumble stimuli occurred in the absence of any bees or bee sounds. This suggests that these elephant rumbles may function as referential signals, in which a formant frequency shift alerts nearby elephants about an external threat, in this case, the threat of bees.     

Nonlinearities in Meerkat Alarm Calls Prevent Receivers from Habituating

Despite the fact that nonlinearities are present in the calls of a number of different species, their adaptive function has received little empirical investigation. Previous studies have demonstrated that playbacks of nonlinear calls evoke a more extreme behavioural response and lead to an increase in responsiveness compared with control playbacks without nonlinearities. Consequently, it has been suggested that nonlinearities might prevent receivers from habituating, by increasing the unpredictability of the call (‘unpredictability hypothesis’). In this study, we tested the unpredictability hypothesis, specifically whether nonlinearities prevent receivers from habituating, by means of a playback experiment using meerkat (Suricata suricatta) alarm calls. We found that in meerkats, playbacks of naturally occurring nonlinear alarm calls take longer to habituate to than alarm calls without any nonlinear intrusions. These data provide important empirical support for the hypothesis that nonlinearities are not just an irrelevant by‐product of the vocal production system, but indeed function adaptively.     

Responses of Redfronted Lemurs to Experimentally Modified Alarm Calls: Evidence for Urgency-Based Changes in Call Structure

Abstract The aim of this study was to investigate how information about the affective state is expressed in vocalizations. Alarm calls can serve as model systems with which to study this general question. Therefore, we examined the information content of terrestrial predator alarm calls of redfronted lemurs ( Eulemur fulvus rufus ), group-living Malagasy primates. Redfronted lemurs give specific alarm calls only towards raptors, whereas calls given in response to terrestrial predators (woofs) are also used in other situations characterized by high arousal. Woofs may therefore have the potential to express the perceived risk of a given threat. In order to examine whether different levels of arousal are expressed in call structure, we analysed woofs given during inter-group encounters or in response to playbacks of a barking dog, assuming that animals engaged in inter-group encounters experience higher arousal than during the playbacks of dog barks. A multivariate acoustic analysis revealed that calls given during group encounters were characterized by higher frequencies than calls given in response to playbacks of dog barks. In order to examine whether this change in call structure is salient to conspecifics, we conducted playback experiments with woofs, modified in either amplitude or frequencies. Playbacks of calls with increased frequency or amplitude elicited a longer orienting response, suggesting that different levels of arousal are expressed in call structure and provide meaningful information for listeners. In conclusion, the results of our study indicate that the information about the sender's affective state is expressed in the structure of vocalizations.     

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.     

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.     

Vocal-tract filtering by lingual articulation in a parrot

Human speech and bird vocalization are complex communicative behaviors with notable similarities in development and underlying mechanisms. However, there is an important difference between humans and birds in the way vocal complexity is generally produced. Human speech originates from independent modulatory actions of a sound source, e.g., the vibrating vocal folds, and an acoustic filter, formed by the resonances of the vocal tract (formants). Modulation in bird vocalization, in contrast, is thought to originate predominantly from the sound source, whereas the role of the resonance filter is only subsidiary in emphasizing the complex time-frequency patterns of the source (e.g., but see ). However, it has been suggested that, analogous to human speech production, tongue movements observed in parrot vocalizations modulate formant characteristics independently from the vocal source. As yet, direct evidence of such a causal relationship is lacking. In five Monk parakeets, Myiopsitta monachus, we replaced the vocal source, the syrinx, with a small speaker that generated a broad-band sound, and we measured the effects of tongue placement on the sound emitted from the beak. The results show that tongue movements cause significant frequency changes in two formants and cause amplitude changes in all four formants present between 0.5 and 10 kHz. We suggest that lingual articulation may thus in part explain the well-known ability of parrots to mimic human speech, and, even more intriguingly, may also underlie a speech-like formant system in natural parrot vocalizations.     

Of Ducklings and Turing Machines: Interactive Playbacks Enhance Subsequent Responsiveness to Conspecific Calls

Distress calls of mallard ducklings consist of a highly stereotyped series of notes. When two ducklings are simultaneously separated from the brood, they characteristically call in alternation. Each bird inhibits its calls while the other is vocalizing, thus preventing masking and facilitating localization by the hen. I examined whether exposure of ducklings to calls presented in a naturalistic alternating pattern affected subsequent responsiveness to them. Individual ducklings were exposed to either 40 s or 80 s of computer-controlled distress call playbacks, using an algorithm that mimicked the behavior of another duckling. Calls were presented only when the subject was silent and ended as soon as it began to vocalize. Each of these ducklings was paired with a ‘yoked’ control. Birds in these control groups experienced exactly the same pattern of playbacks as the ‘interactive’ birds, but the stimuli had no consistent relationship to their own vocal behavior. When the same calls were played back 24 h later, in a fixed pattern that was independent of the ducklings' behavior, birds that had received 80 s of prior interactive exposure were significantly more responsive than both their yoked controls and birds receiving only 40 s of such playbacks. This result suggests that interactive vocal experience, characteristic of natural communication, affects the subsequent perceptual sensitivity of ducklings.     

Cost of mobbing call to breeding pied flycatcher, Ficedula hypoleuca

Mobbing signals advertise the location of a stalking predatorto all prey in an area and recruit them into the inspectionaggregation. Such behavior usually causes the predator to moveto another area. However, mobbing calls could be eavesdroppedby other predators. Because the predation cost of mobbing callsis poorly known, we investigated whether the vocalizations ofthe mobbing pied flycatcher, Ficedula hypoleuca, a small holenesting passerine, increase the risk of nest predation. We usedmobbing calls of pied flycatchers to examine if they could lurepredators such as the marten, Martes martes. This predator usuallyhunts by night and may locate its mobbing prey while restingnearby during the day. Within each of 56 experimental plots,from the top of one nest-box we played back mobbing sounds ofpied flycatchers, whereas blank tapes were played from the topof another nest-box. The trials with mobbing calls were carriedout before sunset. We put pieces of recently abandoned nestsof pied flycatchers and a quail, Coturnix coturnix, egg intoeach of the nest-boxes. Nest-boxes with playbacks of mobbingcalls were depredated by martens significantly more than werenest-boxes with blank tapes. The results of the present studyindicate that repeated conspicuous mobbing calls may carry asignificant cost for birds during the breeding season.     

Vocal-tract resonances as indexical cues in rhesus monkeys

Vocal-tract resonances (or formants) are acoustic signatures in the voice and are related to the shape and length of the vocal tract. Formants play an important role in human communication, helping us not only to distinguish several different speech sounds [1], but also to extract important information related to the physical characteristics of the speaker, so-called indexical cues. How did formants come to play such an important role in human vocal communication? One hypothesis suggests that the ancestral role of formant perception--a role that might be present in extant nonhuman primates--was to provide indexical cues [2-5]. Although formants are present in the acoustic structure of vowel-like calls of monkeys [3-8] and implicated in the discrimination of call types [8-10], it is not known whether they use this feature to extract indexical cues. Here, we investigate whether rhesus monkeys can use the formant structure in their "coo" calls to assess the age-related body size of conspecifics. Using a preferential-looking paradigm [11, 12] and synthetic coo calls in which formant structure simulated an adult/large- or juvenile/small-sounding individual, we demonstrate that untrained monkeys attend to formant cues and link large-sounding coos to large faces and small-sounding coos to small faces-in essence, they can, like humans [13], use formants as indicators of age-related body size.     

Dual Function of Chip Calls Depending on Changing Call Rate Related to Risk Level in Territorial Pairs of White‐Eared Ground‐Sparrows

Different mechanisms have been proposed for encoding information into vocalizations: variation of frequency or temporal characteristics, variation in the rate of vocalization production, and use of different vocalization types. We analyze the effect of rate variation on the dual function of chip calls (contact and alarm) produced by White‐eared Ground‐sparrows (Melozone leucotis). We conducted an acoustic playback experiment where we played back 1 min of four chip call rates (12, 36, 60, 84 calls/min). We measured the response of territorial pairs using behavioral responses, and fine structural features of calls produced in response to those playbacks. White‐eared Ground‐sparrows showed more intense behavioral responses to higher than lower call rate playbacks. Both individuals of the pair approached the source of the playback stimulus faster, produced the first vocalization faster, produced more vocalizations, and spent more time close to the stimulus in higher call rate than in lower call rate playbacks. Frequency and duration characteristics of calls (chip and tseet) were similar in response to all call rate playbacks. Our playback experiment elicited different intensity of behavioral responses, suggesting that risk‐based information is encoded in call rate. Our results suggest that variation in the rate of chip call production serves a dual function in this species; calls are used at lower rates for pair contact and at higher rates for alarm/mobbing signals.