Diversity of the Vocal Signals of Concave-Eared Torrent Frogs (Odorrana tormota): Evidence for Individual Signatures

Male concave-eared torrent frogs ( Odorrana tormota ) have an unusually large call repertoire and have been shown to communicate ultrasonically. We investigated the individual specificity of male advertisement calls in order to explore the acoustic bases of individual recognition, which was demonstrated in an accompanying study. Vocalizations of 15 marked males were recorded in the field. A quantitative analysis of the signals revealed eight basic call-types. Two of them (the single- and multi-note long-calls) were investigated in more detail. Long-calls were characterized by pronounced and varying frequency modulation patterns, and abundant occurrence of nonlinear phenomena (NLP), i.e., frequency jumps, subharmonics, biphonations and deterministic chaos. The occurrence of NLP was predictable from the contour of the fundamental frequency in the harmonic segment preceding the onset of the NLP, and this prediction showed individual-specific patterns. Fifteen acoustic variables of the long calls were measured, all of which were significantly different among individuals, except biphonic segment duration. Discriminant function analysis (DFA) showed that 54.6% of the calls could be correctly assigned to individual frogs. The correct classification was above chance level, suggesting that individual specificity of calls underlie the ability of males to behaviorally discriminate the vocal signals of their neighbors from those of strangers, a remarkable feat for a frog species with a diverse vocal repertoire. The DFA classification results were lower than those for other anurans, however. We hypothesize that there is a tradeoff between an increase in the fundamental frequency of vocalizations to avoid masking by low-frequency ambient background noise, and a decrease in individual-specific vocal tract information extractable from the signal.     

Development of social vocalizations in mice

Adult mice are highly vocal animals, with both males and females vocalizing in same sex and cross sex social encounters. Mouse pups are also highly vocal, producing isolation vocalizations when they are cold or removed from the nest. This study examined patterns in the development of pup isolation vocalizations, and compared these to adult vocalizations. In three litters of CBA/CaJ mice, we recorded isolation vocalizations at ages postnatal day 5 (p5), p7, p9, p11, and p13. Adult vocalizations were obtained in a variety of social situations. Altogether, 28,384 discrete vocal signals were recorded using high-frequency-sensitive equipment and analyzed for syllable type, spectral and temporal features, and the temporal sequencing within bouts. We found that pups produced all but one of the 11 syllable types recorded from adults. The proportions of syllable types changed developmentally, but even the youngest pups produced complex syllables with frequency-time variations. When all syllable types were pooled together for analysis, changes in the peak frequency or the duration of syllables were small, although significant, from p5 through p13. However, individual syllable types showed different, large patterns of change over development, requiring analysis of each syllable type separately. Most adult syllables were substantially lower in frequency and shorter in duration. As pups aged, the complexity of vocal bouts increased, with a greater tendency to switch between syllable types. Vocal bouts from older animals, p13 and adult, had significantly more sequential structure than those from younger mice. Overall, these results demonstrate substantial changes in social vocalizations with age. Future studies are required to identify whether these changes result from developmental processes affecting the vocal tract or control of vocalization, or from vocal learning. To provide a tool for further research, we developed a MATLAB program that generates bouts of vocalizations that correspond to mice of different ages.     

Individual Acoustic Variation in Fallow Deer (Dama dama) Common and Harsh Groans: A Source-Filter Theory Perspective

Mammals are able to distinguish conspecifics based on vocal cues, and the acoustic structure of mammal vocalizations is directly affected by the anatomy and action of the vocal apparatus. However, most studies investigating individual patterns in acoustic signals do not consider a vocal production‐based perspective. In this study, we used the source‐filter model of vocal production as a basis for investigating the acoustic variability of fallow deer groans. Using this approach, we quantified the potential of each acoustic component to carry information about individual identity. We also investigated if cues to individual identity carry over among the two groan types we describe: common and harsh groans. Using discriminant function analysis, we found that variables related to the fundamental frequency contour and the minimum frequencies of the highest formants contributed most to the identification of a given common groan. Common groans were individually distinctive with 36.6% (53.6% with stepwise procedure) of groans assigned to the correct individual. This level of discrimination is approximately six times higher than that predicted by chance. In addition, univariate anova s showed significant inter‐individual variation in the minimum formant frequencies when common and harsh groans were combined, suggesting that some information about individuality is shared between groan types. Our results suggest that the sound source and the vocal tract resonances act together to determine groan individuality and that enough variation exists to potentially allow individual recognition based on groans.     

Predicting Achievable Fundamental Frequency Ranges in Vocalization Across Species

Vocal folds are used as sound sources in various species, but it is unknown how vocal fold morphologies are optimized for different acoustic objectives. Here we identify two main variables affecting range of vocal fold vibration frequency, namely vocal fold elongation and tissue fiber stress. A simple vibrating string model is used to predict fundamental frequency ranges across species of different vocal fold sizes. While average fundamental frequency is predominantly determined by vocal fold length (larynx size), range of fundamental frequency is facilitated by (1) laryngeal muscles that control elongation and by (2) nonlinearity in tissue fiber tension. One adaptation that would increase fundamental frequency range is greater freedom in joint rotation or gliding of two cartilages (thyroid and cricoid), so that vocal fold length change is maximized. Alternatively, tissue layers can develop to bear a disproportionate fiber tension (i.e., a ligament with high density collagen fibers), increasing the fundamental frequency range and thereby vocal versatility. The range of fundamental frequency across species is thus not simply one-dimensional, but can be conceptualized as the dependent variable in a multi-dimensional morphospace. In humans, this could allow for variations that could be clinically important for voice therapy and vocal fold repair. Alternative solutions could also have importance in vocal training for singing and other highly-skilled vocalizations.     

Convergence and divergence in Diana monkey vocalizations

Individually distinct vocalizations are widespread among social animals, presumably caused by variation in vocal tract anatomy. A less-explored source of individual variation is due to learned movement patterns of the vocal tract, which can lead to vocal convergence or divergence in social groups. We studied patterns of acoustic similarity in a social call produced by 14 female Diana monkeys (Cercopithecus diana) in two free-ranging groups. Calls showed variability in fundamental frequency contours owing to individual identity and external context. Vocal divergence increased significantly between females during poor visibility and tended to increase in the presence of neighbours. In contrast, vocal convergence increased significantly between females during vocal interactions, because females matched the frequency contour of their own call with another female's preceding call. Our findings demonstrate that these primates have some control over the acoustic fine structure of their most important social vocalization. Vocal convergence and divergence are two opposing processes that enable callers to ensure spatial proximity and social cohesion with other group members.     

Spectrographic Description of Vocalizations in Captive Otolemur garnettii

To advance knowledge of the vocal communication associated with close proximity social interactions in Garnett's greater bush baby (Otolemur garnettii), we measured acoustic and temporal properties of vocalizations from videotaped recordings of captives in two main social contexts: mother-infant interactions and adult male-female pair introductions and reintroductions. We used a real-time sonagraph or software program to display, edit, and analyze vocal waveforms, and to provide wideband and narrowband spectrograms. Vocalization characteristics measured include fundamental frequency (via inspection of harmonics) and spectral features such as formant frequency, intensity, and duration. The vocal repertoire contained 4 major types of vocalizations: 1) barks and complex multiple bark sequences, 2) low frequency flutter/hums and growls, 3) high frequency clicks and spits, and 4) noisy shrieks. We describe several vocalizations for the first time and provide a clear classification of some of them on the basis of call durations (long/short growls). Complex bark sequences, previously described as distant communication calls, were invariant and were not often emitted by individuals when in close proximity. When classified spectrographically, the remaining 3 call types, which occurred when individuals were in close proximity, were less stereotypical, and gradations within call types were apparent. Our results show that although nocturnal and non-gregarious, complex communicatory signals of bush babies constitute a vocal repertoire formerly thought to be characteristic only of diurnal, gregarious primates.     

Acoustic cues to caller identity in lemurs: a case study

This study investigated the acoustic structure of grunt vocalizations in red-bellied lemurs (Eulemur rubriventer) and its potential for individual discrimination. Acoustic analyses were performed on 1,605 grunts recorded from seven lemurs belonging to two captive groups. From the perspective of sound-filter theory, we described the acoustic structure of grunts, measuring two sets of parameters: fundamental frequency characteristics as larynx-related variables and four formant frequencies as filter-related features. Formants were effective in assigning 80.5% of the vocalizations to the correct emitter against 24.9% scored by the model based on larynx-related variables. We concluded that vocal tract resonances might potentially provide conspecifics with individual cues.     

Dialects in southern Rocky Mountain pikas, Ochotona princeps (Lagomorpha)

This work quantifies the geographic variation (dialects) in the vocalizations of southern Rocky Mountain pikas and presents data on the vocal responses of pikas to playback of recorded vocalizations of two dialects. Pika vocalizations were tape-recorded in twenty-six locations in Wyoming, Colorado, Utah and New Mexico. Two dialects (based on duration of note and frequency of fundamental) were found in short calls. One dialect was north of the Colorado River (dialect A), and the other was south of the Colorado River (dialect B). There was seasonal variation in the incidence of vocalizations with a peak of songs in late spring and a peak of short calls in late summer. Results of this study indicate that acoustic characteristics of vocalizations could be a useful taxonomic tool in the genus Ochotona.     

Temporal population code of concurrent vocal signals in the auditory midbrain

Unique patterns of spike activity across neuron populations have been implicated in the coding of complex sensory stimuli. Delineating the patterns of neural activity in response to varying stimulus parameters and their relationships to the tuning characteristics of individual neurons is essential to ascertaining the nature of population coding within the brain. Here, we address these points in the midbrain coding of concurrent vocal signals of a sound-producing fish, the plainfin midshipman. Midshipman produce multiharmonic vocalizations which frequently overlap to produce beats. We used multivariate statistical analysis from single-unit recordings across multiple animals to assess the presence of a temporal population code. Our results show that distinct patterns of temporal activity emerge among midbrain neurons in response to concurrent signals that vary in their difference frequency. These patterns can serve to code beat difference frequencies. The patterns directly result from the differential temporal coding of difference frequency by individual neurons. Difference frequency encoding, based on temporal patterns of activity, could permit the segregation of concurrent vocal signals on time scales shorter than codes requiring averaging. Given the ubiquity across vertebrates of auditory midbrain tuning to the temporal structure of acoustic signals, a similar temporal population code is likely present in other species.     

THE GENETIC BASIS OF ZEBRA FINCH VOCALIZATIONS

Animal vocalizations play an important role in individual recognition, kin recognition, species recognition, and sexual selection. Despite much work in these fields done on birds virtually nothing is known about the heritability of vocal traits in birds. Here, we study a captive population of more than 800 zebra finches ( Taeniopygia guttata ) with regard to the quantitative genetics of call and song characteristics. We find very high heritabilities in nonlearned female call traits and considerably lower heritabilities in male call and song traits, which are learned from a tutor and hence show much greater environmental variance than innate vocalizations. In both sexes, we found significant heritabilities in several traits such as mean frequency and measures of timbre, which reflect morphological characteristics of the vocal tract. These traits also showed significant genetic correlations with body size, as well as positive genetic correlations between the sexes, supporting a scenario of honest signaling of body size through genetic pleiotropy ("index signal"). In contrast to such morphology-related voice characteristics, classical song features such as repertoire size or song length showed very low heritabilities. Hence, these traits that are often suspected to be sexually selected would hardly respond to current directional selection.     

Individual and geographical variation in display behaviour of male harbour seals in Scotland

Studying variations in behaviour at the individual or population level enables insight into the reproductive strategies within a species. We examined individual and geographical variation in the vocal and dive behaviour of male harbour seals, Phoca vitulina, which is associated with aquatic mating. This display behaviour was recorded in the Moray Firth, Scotland, from July 1994 to 1997, and in Orkney, Scotland, during July 1998. One vocalization type was apparent in the Moray Firth and two in Orkney. Time parameters (total and pulse duration) varied between males in the population in the Moray Firth. We used both frequency and time parameters in a discriminant analysis, which showed that 73.2% of individual male vocalizations could be correctly classified; 94.6% of male vocalizations from the Moray Firth and Orkney could be correctly classified according to their geographical areas. Therefore, vocal variation was greater between geographical areas than between individuals. No individual variation was apparent between dive and surface interval durations. However, individuals varied significantly in the percentage of short surface intervals. Male harbour seals showed substantial variability in the parameters affecting their vocal and dive behaviour during the mating season. We suggest that these variations may be indicative of adaptations to varying environmental challenges influencing the reproductive strategies of discrete populations. Copyright 2000 The Association for the Study of Animal Behaviour.     

Mother-young recognition in an ungulate hider species: a unidirectional process

Parent-offspring recognition is usually crucial for survival of young. In mammals, olfaction often only permits identification at short range, and vocalizations are important at longer distances. Following and hiding antipredator strategies found in newborn mammals may also affect parental recognition mechanisms. We investigated mother-offspring recognition in fallow deer, an ungulate hider species. We analyzed the structure of adult female and fawn contact calls to determine whether they are individually distinctive and tested for mother-offspring recognition. Only females (and not fawns) have individualized vocalizations, with the fundamental frequency as the most distinctive parameter. Playback experiments showed that fawns can distinguish the calls of their mothers from those of other females, but mothers could not discriminate their own and alien fawn calls. Thus, the vocal identification process is unidirectional. In followers, mother-offspring acoustic recognition is mutual, and therefore the different antipredator strategies of newborn mammals may have shaped the modalities of parent-offspring acoustic recognition.     

Advertising individual identity by mother and adolescent contact calls in Siberian wapiti Cervus elaphus sibiricus

Individualistic contact calls facilitate mother‐offspring reunion after separation. However, in many mammals, both the acoustic structure and individuality of contact calls differ between mother and young. In contrast, in Siberian wapiti Cervus elaphus sibiricus, contact calls are similar in the acoustics between mother and young, whereas effects of this similarity on vocal individuality were not investigated. In this study, we analyzed acoustic differences between closed‐mouth (nasal) and open‐mouth (oral) contact calls and examined individuality of the most usual oral calls of 19 Siberian wapiti (9 hinds and 10 5–6‐month adolescents) emitted in response to mother‐offspring separation. In the oral calls, the values of frequency and power variables were higher than in the nasal calls. Calls of hinds and adolescents did not differ by the maximum fundamental frequency and duration, whereas the peak frequency was higher in the young. Discriminant function analysis (DFA) based on 11 acoustic variables of oral calls accurately classified to individual 92.5% of hind calls and 96.9% of adolescent calls (chi‐square test for differences between hinds and adolescents, p = 0.19). Variables mainly contributing to vocal identity (duration, start, and maximum fundamental frequency) were the same in calls of mothers and adolescents. We conclude that similarities in the acoustics calls of mothers and adolescents mean that they do not differ in their potential for encoding individual identity, suggesting a mutual process of mother‐offspring vocal recognition in Siberian wapiti.     

Acoustic variation of pant hoot calls by male chimpanzees: a playback experiment

Pant hoots, a type of long-distance calls of chimpanzees (Pan troglodytes), were played back to two male chimpanzees in a group of seven captive individuals to determine if chimpanzees would modify those vocalizations in response to strange males. Subjects emitted pant hoots with higher rates of delivery, shorter duration of buildup, and lower minimum fundamental frequency of climax when they were presented with pant hoots of strangers than when they produced the calls spontaneously. Considering the direction of acoustical change, we concluded that the rate of delivery, duration of buildup, and minimum frequency of climax might be associated with the underlying emotional states of the callers rather than call matching. Individual difference between two subject males was significant in minimum frequency and duration of climax and in average frequency of call, which appears to reflect differences of the caller's age and social status. These results suggest that different acoustic variables relate to within- and interindividual differences of these vocalizations. Received: March 7, 2000 / Accepted: May 8, 2000     

Call Learning in Black-capped Chickadees (Parus atricapillus): The Role of Experience in the Development of ‘Chick-A-Dee’ Calls

The role of learning in the development of bird vocalizations other than territorial song is not well studied. The well-known role of direct imitation in the development of territorial song potentially masks the effects of other processes in the development of vocal behaviour. The ‘chick-a-dee’ call of black-capped chickadees is a good system in which to investigate more subtle developmental processes because this call is composed of a small number of distinctive note types. These note types may be classified objectively based on a simple set of acoustic variables, allowing for a quantitative assessment of vocal learning. We raised four groups of black-capped chickadees under different degrees of social and acoustic isolation. We then used a multivariate analysis of the acoustic structure of the introductory call notes (‘A-’ ‘B-’ and ‘C-notes’) to determine how similar the notes produced by these hand-reared birds were to the notes of wild birds. Hand-reared chickadees with greater exposure to normal phonology produced notes of all three note types that were more similar to those of wild birds. Regardless of experience, however, all birds produced A-notes that fell within the normal range of those produced by wild birds. By contrast, the development of normal B- and C-notes appears to be more dependent upon experience. These data suggest that learning may play a different role in the development of different phonological units within one vocalization. Our results also illustrate the importance of considering processes other than simple imitation in the development of avian vocalizations.     

Acoustic characteristics and variations in grunt vocalizations in the oyster toadfish <Emphasis Type="Italic">Opsanus tau</Emphasis>

Acoustic communication is critical for reproductive success in the oyster toadfish Opsanus tau. While previous studies have examined the acoustic characteristics, behavioral context, geographical variation, and seasonality of advertisement boatwhistle sound production, there is limited information on the grunt or other non-advertisement vocalizations in this species. This study continuously monitored sound production in toadfish maintained in an outdoor habitat for four months to identify and characterize grunt vocalizations, compare them with boatwhistles, and test for relationships between the incidence of grunt vocalizations, sound characteristics and environmental parameters. Oyster toadfish produced grunts in response to handling, and spontaneous single (70% of all grunts), doublet (10%), and trains of grunts (20%) throughout the May to September study period. Grunt types varied in pulse structure, duration, and frequency components, and were shorter and of lower fundamental frequency than the pulse repetition rate of boatwhistles. Higher water temperatures were correlated with a greater number of grunt emissions, higher fundamental frequencies, and shorter sound durations. The number of grunts per day was also positively correlated with daylength and maximum tidal amplitude differences (previously entrained) associated with full and new moons, thus providing the first demonstration of semilunar vocalization rhythms in the oyster toadfish. These data provide new information on the acoustic repertoire and the environmental factors correlated with sound production in the toadfish, and have important implications for seasonal acoustic communication in this model vocal fish.     

Development of echolocation and communication vocalizations in the big brown bat, <Emphasis Type="Italic">Eptesicus fuscus</Emphasis>

Big brown bats form large maternity colonies of up to 200 mothers and their pups. If pups are separated from their mothers, they can locate each other using vocalizations. The goal of this study was to systematically characterize the development of echolocation and communication calls from birth through adulthood to determine whether they develop from a common precursor at the same or different rates, or whether both types are present initially. Three females and their six pups were isolated from our captive breeding colony. We recorded vocal activity from postnatal day 1 to 35, both when the pups were isolated and when they were reunited with their mothers. At birth, pups exclusively emitted isolation calls, with a fundamental frequency range <20 kHz, and duration >30 ms. By the middle of week 1, different types of vocalizations began to emerge. Starting in week 2, pups in the presence of their mothers emitted sounds that resembled adult communication vocalizations, with a lower frequency range and longer durations than isolation calls or echolocation signals. During weeks 2 and 3, these vocalizations were extremely heterogeneous, suggesting that the pups went through a babbling stage before establishing a repertoire of stereotyped adult vocalizations around week 4. By week 4, vocalizations emitted when pups were alone were identical to adult echolocation signals. Echolocation and communication signals both appear to develop from the isolation call, diverging during week 2 and continuing to develop at different rates for several weeks until the adult vocal repertoire is established.     

Vocal individual discrimination in Japanese monkeys

The present study determines which features of the coo call are used by Japanese monkeys Macaca fuscata for vocal individual discrimination. First, two female Japanese monkeys were trained to discriminate conspecific individuals vocally, using an operant conditioning. Using as stimuli three unknown individuals with 30 calls per individual, the two monkeys succeeded in discriminating new call exemplars from the three stimulus individuals. A discriminant analysis performed on calls used as stimuli indicated that start frequency of the fundamental and call duration were variables that can differentiate individuals efficiently. Then, playbacks of acoustically modified signals were used to indicate which vocal features are used by monkeys for the individual discrimination. Stimuli signals containing modified pitch or duration, or filtered so as to keep only the fundamental component, were tested. Results indicated that Japanese monkeys use multiple acoustical cues to perform vocal individual discrimination, including at least pitch, call duration, and harmonics. However, harmonics seem to be less important for discrimination than pitch and call duration.     

Using Shannon entropy on measuring the individual variability in the Rufous-bellied thrush Turdus rufiventris vocal communication

We applied the information theory concepts to notes repertoire characteristics combined with temporal parameters of the Rufous-bellied thrush Turdus rufiventris song, using this particular case to test a new method of analysing quantitatively complex animal communication systems. Like most Turdus thrushes, Rufous-bellied thrushes are remarkable for their long, varied and melodious songs. For the analysis of the species repertoire, we used recordings of 44 individuals from 24 localities covering its full geographical range. We measured the repertoire size, note duration and rhythm (frequency of note utterance), and combined these parameters with the Shannon entropy values calculated for each individual. Although individuals maintain species-specific recognition capacity, we find a large variation between their song parameters and show that the information theory can be useful to analyse large and varied animal vocal repertoires. We are introducing two new parameters, temporal average entropy (E(t)) and utterance frequency average entropy (E(f)), for measuring such communication systems.     

Vocal signature in capybara,Hydrochoerus hydrochaeris

Social groups of capybaras are stable and cohesive. The species’ vocal communication is complex and mediates social interaction. The click call is emitted in a variety of contexts by animals from all age groups, but differs among groups; its attributed function is to keep contact among animals. To evaluate the presence of individual characteristics in the click call of capybaras, we recorded the vocalizations emitted spontaneously by six adults kept either solitary or in groups. We selected and measured the acoustic parameters of 300 click call phrases, 50 per individual. The parameters were submitted to a discriminant function analysis that revealed a classification accuracy of 76.8 %. A General Linear Model analysis revealed significant differences among the six individuals, and post hoc results showed that differences between a given pair were different from those of any other pair. The acoustic parameters that most contributed to discriminate the individual calls were click interval duration and click duration, suggesting that temporal parameters are more important than frequency parameters for individuals’ discrimination. The findings of individual characteristics in the click calls indicate that these vocalizations can be used as vocal signatures during social interactions.