Calls out of chaos: the adaptive significance of nonlinear phenomena in mammalian vocal production

Recent work on human vocal production demonstrates that certain irregular phenomena seen in human pathological voices and baby crying result from nonlinearities in the vocal production system. Equivalent phenomena are quite common in nonhuman mammal vocal repertoires. In particular, bifurcations and chaos are ubiquitous aspects of the normal adult repertoire in many primate species. Here we argue that these phenomena result from properties inherent in the peripheral production mechanism, which allows individuals to generate highly complex and unpredictable vocalizations without requiring equivalently complex neural control mechanisms. We provide examples from the vocal repertoire of rhesus macaques, Macaca mulatta, and other species illustrating the different classes of nonlinear phenomena, and review the concepts from nonlinear dynamics that explicate these calls. Finally, we discuss the evolutionary significance of nonlinear vocal phenomena. We suggest that nonlinear phenomena may subserve individual recognition and the estimation of size or fluctuating asymmetry from vocalizations. Furthermore, neurally ‘cheap’ unpredictability may serve the valuable adaptive function of making chaotic calls difficult to predict and ignore. While noting that nonlinear phenomena are in some cases probably nonadaptive by-products of the physics of the sound-generating mechanism, we suggest that these functional hypotheses provide at least a partial explanation for the ubiquity of nonlinear calls in nonhuman vocal repertoires.     

Structural Classification of Wild Boar (Sus scrofa) Vocalizations

Determining whether a species' vocal communication system is graded or discrete requires definition of its vocal repertoire. In this context, research on domestic pig (Sus scrofa domesticus) vocalizations, for example, has led to significant advances in our understanding of communicative functions. Despite their close relation to domestic pigs, little is known about wild boar (Sus scrofa) vocalizations. The few existing studies, conducted in the 1970s, relied on visual inspections of spectrograms to quantify acoustic parameters and lacked statistical analysis. Here, we use objective signal processing techniques and advanced statistical approaches to classify 616 calls recorded from semi‐free ranging animals. Based on four spectral and temporal acoustic parameters—quartile Q25, duration, spectral flux, and spectral flatness—extracted from a multivariate analysis, we refine and extend the conclusions drawn from previous work and present a statistically validated classification of the wild boar vocal repertoire into four call types: grunts, grunt‐squeals, squeals, and trumpets. While the majority of calls could be sorted into these categories using objective criteria, we also found evidence supporting a graded interpretation of some wild boar vocalizations as acoustically continuous, with the extremes representing discrete call types. The use of objective criteria based on modern techniques and statistics in respect to acoustic continuity advances our understanding of vocal variation. Integrating our findings with recent studies on domestic pig vocal behavior and emotions, we emphasize the importance of grunt‐squeals for acoustic approaches to animal welfare and underline the need of further research investigating the role of domestication on animal vocal communication.     

Primate vocal communication: a useful tool for understanding human speech and language evolution?

Language is a uniquely human trait, and questions of how and why it evolved have been intriguing scientists for years. Nonhuman primates (primates) are our closest living relatives, and their behavior can be used to estimate the capacities of our extinct ancestors. As humans and many primate species rely on vocalizations as their primary mode of communication, the vocal behavior of primates has been an obvious target for studies investigating the evolutionary roots of human speech and language. By studying the similarities and differences between human and primate vocalizations, comparative research has the potential to clarify the evolutionary processes that shaped human speech and language. This review examines some of the seminal and recent studies that contribute to our knowledge regarding the link between primate calls and human language and speech. We focus on three main aspects of primate vocal behavior: functional reference, call combinations, and vocal learning. Studies in these areas indicate that despite important differences, primate vocal communication exhibits some key features characterizing human language. They also indicate, however, that some critical aspects of speech, such as vocal plasticity, are not shared with our primate cousins. We conclude that comparative research on primate vocal behavior is a very promising tool for deepening our understanding of the evolution of human speech and language, but much is still to be done as many aspects of monkey and ape vocalizations remain largely unexplored.     

Vocal Repertoire of Golden-backed Uakaris (<Emphasis Type="Italic">Cacajao melanocephalus</Emphasis>): Call Structure and Context

The study of vocal behavior can reveal important aspects of how and why a species communicates in relation to ecological and social challenges. We here focus on vocal communication in golden-backed uakaris (Cacajao melanocephalus), diurnal, pitheciine monkeys that exhibit fission-fusion social organization and typically inhabit dense forests that limit the potential for visual communication. Moreover, the species spends little time engaged in tactile or olfactory communication, e.g., social grooming and scent marking, respectively. Hence, vocalizations may be very important for the coordination of social organization in these monkeys. We 1) categorized golden-backed uakari vocalizations, 2) ascertained their behavioral context, and 3) investigated whether golden-backed uakari calls can encode information about the signaler. We observed the monkeys during 2 wet seasons in the flooded igapó forest of Jaú National Park, Brazil. We showed that golden-backed uakaris have 9 call types in their vocal repertoire, all distinguishable by ear and from analysis of spectrograms. Some calls, e.g., play-specific calls, were used only in particular behavioral contexts, and by individuals of specific age, whereas others were emitted under a range of situations. The structure of the loud tchó call varied among individuals, and according to behavioral context, i.e., whether individuals were foraging/feeding, traveling, or performing agonistic interactions. This knowledge of the species’ vocal repertoire is valuable for surveying the monkeys acoustically in habitats where visual surveys are difficult.     

Vocal communication as a function of differential rearing experiences inPan paniscus: A preliminary report

There is little evidence of vocal learning in nonhuman primates despite the well-documented abilities found in avian species. We describe the vocal repertoire of five bonobos (Pan paniscus), four of which live in a seminatural environment. The fifth subject, Kanzi, has been reared with humans during the course of language training. The data indicated that the four bonobos living in a seminatural environment exhibit a variety of species-typical vocalizations. In addition to producing all the species-typical vocalization, Kanzi produced four structurally unique vocalizations that were not heard among the other subjects. These data suggest that Kanzi has learned vocalizations that are novel due to his unique rearing experience. Discussion is focused on the flexibility of vocal communication and vocal comprehension inPan paniscus.     

Quantitative tools for comparing animal communication systems: information theory applied to bottlenose dolphin whistle repertoires

Comparative analysis of nonhuman animal communication systems and their complexity, particularly in comparison to human language, has been generally hampered by both a lack of sufficiently extensive data sets and appropriate analytic tools. Information theory measures provide an important quantitative tool for examining and comparing communication systems across species. In this paper we use the original application of information theory, that of statistical examination of a communication system's structure and organization. As an example of the utility of information theory to the analysis of animal communication systems, we applied a series of information theory statistics to a statistically categorized set of bottlenose dolphin Tursiops truncatus, whistle vocalizations. First, we use the first-order entropic relation in a Zipf-type diagram (Zipf 1949 Human Behavior and the Principle of Least Effort) to illustrate the application of temporal statistics as comparative indicators of repertoire complexity, and as possible predictive indicators of acquisition/learning in animal vocal repertoires. Second, we illustrate the need for more extensive temporal data sets when examining the higher entropic orders, indicative of higher levels of internal informational structure, of such vocalizations, which could begin to allow the statistical reconstruction of repertoire organization. Third, we propose using 'communication capacity' as a measure of the degree of temporal structure and complexity of statistical correlation, represented by the values of entropic order, as an objective tool for interspecies comparison of communication complexity. In doing so, we introduce a new comparative measure, the slope of Shannon entropies, and illustrate how it potentially can be used to compare the organizational complexity of vocal repertoires across a diversity of species. Finally, we illustrate the nature and predictive application of these higher-order entropies using a preliminary sample of dolphin whistle vocalizations. The purpose of this preliminary report is to re-examine the original application of information theory to the field of animal communication, illustrate its potential utility as a comparative tool for examining the internal informational structure of animal vocal repertoires and their development, and discuss its relationship to behavioural ecology and evolutionary theory. Copyright 1999 The Association for the Study of Animal Behaviour.     

Vocal Repertoire of Cebus capucinus: Acoustic Structure, Context, and Usage

Researchers studying nonhuman primate vocal repertoires suggest that convergent environmental, social, and motivational factors account for intra- and interspecific vocal variation. We provide a detailed overview of the vocal repertoire of white-faced capuchins, including acoustic analyses and contextual information of vocal production and vocal usage by different age-sex classes in social interactions. The repertoire is a mixture of graded and discrete vocalizations. In addition, there is general support for structural variation in vocalizations with changes in arousal level. We also identified several combined vocalizations, which might represent variable underlying motivations. Lastly, by including data on the social contexts and production of vocalizations by different age-sex classes, we provide preliminary information about the function of vocalizations in social interactions for individuals of different rank, age, and sex. Future studies are necessary to explore the function of combined vocalizations and how the social function of vocalizations relate to their acoustic structure, because social use of vocalizations may play an important role in shaping vocal evolution.     

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.     

A case of spontaneous acquisition of a human sound by an orangutan

The capacity of nonhuman primates to actively modify the acoustic structure of existing sounds or vocalizations in their repertoire appears limited. Several studies have reported population or community differences in the acoustical structure of nonhuman primate long distance calls and have suggested vocal learning as a mechanism for explaining such variation. In addition, recent studies on great apes have indicated that there are repertoire differences between populations. Some populations have sounds in their repertoire that others have not. These differences have also been suggested to be the result of vocal learning. On yet another level great apes can, after extensive human training, also learn some species atypical vocalizations. Here we show a new aspect of great ape vocal learning by providing data that an orangutan has spontaneously (without any training) acquired a human whistle and can modulate the duration and number of whistles to copy a human model. This might indicate that the learning capacities of great apes in the auditory domain might be more flexible than hitherto assumed. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Vocal communication of tonkean macaques in confined environments

Vocal recordings of one semi-free-ranging group and one captive group of Tonkean macaques (Macaca tonkeana) were used to establish the vocal repertoire of the species. Only the alpha male of the groups uttered a very distinctive loud call. Localization variants of coo calls were found. Alarm calls given by this species were acoustically similar to those by Japanese, rhesus, and long-tailed macaques (M. fuscata, M. mulatta, andM. fascicularis). Adult females uttered a specific variant of vocalizations during sexual morphological changes. The repertoire of agonistic vocalizations was more variable than that of any other macaque species investigated. These characteristics were discussed with reference to previous studies on vocalizations of macaque species.     

The use of Vocalizations of the Sambirano Mouse Lemur (<Emphasis Type="Italic">Microcebus sambiranensis</Emphasis>) in an Acoustic Survey of Habitat Preference

Primate vocalizations convey a variety of information to conspecifics. The acoustic traits of these vocalizations are an effective vocal fingerprint to discriminate between sibling species for taxonomic diagnosis. However, the vocal behavior of nocturnal primates has been poorly studied and there are few studies of their vocal repertoires. We compiled a vocal repertoire for the Endangered Sambirano mouse lemur, Microcebus sambiranensis, an unstudied nocturnal primate of northwestern Madagascar, and compared the acoustic properties of one of their call types to those of M. murinus and M. rufus. We recorded vocalizations from radio-collared individuals using handheld recorders over 3 months. We also conducted an acoustic survey to measure the vocal activity of M. sambiranensis in four forest habitat types at the study site. We identified and classified five vocalization types in M. sambiranensis. The vocal repertoires of the three Microcebus species contain very similar call types but have different acoustic properties, with one loud call type, the whistle, having significantly different acoustic properties between species. Our acoustic survey detected more calls of M. sambiranensis in secondary forest, riparian forest, and forest edge habitats, suggesting that individuals may prefer these habitat types over primary forest. Our results suggest interspecific differences in the vocal repertoire of mouse lemurs, and that these differences can be used to investigate habitat preference via acoustic surveys.     

Automated identification and clustering of subunits within delphinid vocalizations

Tonal vocalizations or whistles produced by many species of delphinids range from simple tones to complex frequency contours. Whistle structure varies in duration, frequency, and composition between delphinid species, as well as between populations and individuals. Categorization of whistles may be improved by decomposition of complex calls into simpler subunits, much like the use of phonemes in classification of human speech. We identify a potential whistle decomposition scheme and normalization process to facilitate comparison of whistle subunits derived from tonal vocalizations of bottlenose dolphins (Tursiops truncatus), spinner dolphins (Stenella longirostris), and short‐beaked common dolphins (Delphinus delphis). Network analysis is then used to compare subunits within the vocal corpus of each species. By processing whistles through a series of steps including segmentation, normalization, and dynamic time warping, we are able to automatically cluster selected subunits by shape, regardless of differences in absolute frequency or moderate differences in duration. Using the clustered subunits, we demonstrate a preliminary species classification scheme based on rates of subunit occurrence in vocal repertoires. This provides a potential mechanism for comparing the structure of complex vocalizations within and between species.     

非人灵长类声音通讯的研究进展

声音通讯是非人灵长类研究一个重要的研究领域,有助于了解非人灵长类的社会行为、个体关系、行为进化和社会演化等,甚至对探究人类语言起源和进化等方面也具有十分重要的意义.本文通过对非人灵长类声音通讯的研究内容、影响因素和研究方法等进行了梳理,探讨非人灵长类声音通讯研究的前景和展望,旨在进一步推动国内非人灵长类声音通讯研究的深...     

白腹管鼻蝠成体交流声波多样性

小蝙蝠亚目即通常所说的蝙蝠,是哺乳动物中群居程度最高的类群之一,主要依靠声学信号在黑暗环境中进行交流并维持社群结构,很多蝙蝠种类的交流声波具有极高的多样性,但是目前关于特定种类蝙蝠交流声波的研究还比较缺乏。我们通过录制白腹管鼻蝠(Murina leucogaster)成体的声波,深入研究其交流声波声谱特征,根据交流声波在声谱图上的形状对声波类型进行初步划分,并利用主成分分析(PCA)和判别分析(DFAs)进行验证。结果表明,其交流声波在声谱结构上具有较高多样性,分为16种不同的音节类型,其中包括13种简单音节和3种组合音节,大多数音节都具有多谐波结构。简单音节可分为9种调频音节、2种准恒频音节和2种噪音,组合音节由简单音节无间隔地组合而成。第一谐波最大频率、第一谐波带宽、持续时间为与调频音节类型相关的主要参数。本研究结果为今后进一步开展研究蝙蝠发声行为的行为学意义和声波交流的神经生理学机制方面的研究奠定了基础。     

A comparison of individual distinctiveness in three vocalizations of the dwarf mongoose (Helogale parvula)

Individual specificity can be found in the vocalizations of many avian and mammalian species. However, it is often difficult to determine whether these vocal cues to identity rise from “unselected” individual differences in vocal morphology or whether they have been accentuated by selection for the purposes of advertising caller identity. By comparing the level of acoustic individuality of different vocalizations within the repertoire of a single species, it is possible to ascertain whether selection for individual recognition has modified the vocal cues to identity in particular contexts. We used discriminant function analyses to determine the level of accuracy with which calls could be classified to the correct individual caller, for three dwarf mongoose (Helogale parvula) vocalizations: contact, snake, and isolation calls. These calls were similar in acoustic structure but divergent in context and function. We found that all three call types showed individual specificity but levels varied with call type (increasing from snake to contact to isolation call). The individual distinctiveness of each call type appeared to be directly related to the degree of benefit that signalers were likely to accrue from advertising their identity within that call context. We conclude that dwarf mongoose signalers have undergone selection to facilitate vocal individual recognition, particularly in relation to the species’ isolation call.     

Unusual repertoire of vocalizations in adult BTBR T+tf/J mice during three types of social encounters

BTBR T+tf/J (BTBR) is an inbred mouse strain that displays social deficits and repetitive behaviors analogous to the first and third diagnostic symptoms of autism. We previously reported an unusual pattern of ultrasonic vocalizations in BTBR pups that may represent a behavioral homolog to the second diagnostic symptom of autism, impaired communication. This study investigated the social and vocal repertoire in adult BTBR mice, to evaluate the role of ultrasonic vocalizations in multiple social situations at the adult stage of development. Three different social contexts were considered: male–female, male–male (resident–intruder) and female–female interactions. Behavioral responses and ultrasonic vocalizations were recorded for BTBR and for the highly social control strain C57BL/6J (B6). No episodes of overt fighting or mating were observed during the short durations of the three different experimental encounters. BTBR displayed lower levels of vocalizations and social investigation in all three social contexts as compared with B6. In addition, the correlation analyses between social investigation and ultrasonic vocalization emission rate showed that in B6 mice, the two variables were positively correlated in all the three different social settings, whereas in BTBR mice, the positive correlation was significant only in the male–female interactions. These findings strongly support the value of simultaneously recording two aspects of the mouse social repertoire: social motivation and bioacoustic communication. Moreover, our findings in adults are consistent with previous results in pups, showing an unusual vocal repertoire in BTBR as compared with B6.     

Individuality in the vocalizations of infant and adult coppery titi monkeys (Plecturocebus cupreus)

As social animals, many primates use acoustic communication to maintain relationships. Vocal individuality has been documented in a diverse range of primate species and call types, many of which have presumably different functions. Auditory recognition of one's neighbors may confer a selective advantage if identifying conspecifics decreases the need to participate in costly territorial behaviors. Alternatively, vocal individuality may be nonadaptive and the result of a unique combination of genetics and environment. Pair-bonded primates, in particular, often participate in coordinated vocal duets that can be heard over long distances by neighboring conspecifics. In contrast to adult calls, infant vocalizations are short-range and used for intragroup communication. Here, we provide two separate but complementary analyses of vocal individuality in distinct call types of coppery titi monkeys (Plecturocebus cupreus) to test whether individuality occurs in call types from animals of different age classes with presumably different functions. We analyzed 600 trill vocalizations from 30 infants and 169 pulse-chirp duet vocalizations from 30 adult titi monkeys. We predicted that duet contributions would exhibit a higher degree of individuality than infant trills, given their assumed function for long-distance, intergroup communication. We estimated 7 features from infant trills and 16 features from spectrograms of adult pulse-chirps, then used discriminant function analysis with leave-one-out cross-validation to classify individuals. We correctly classified infants with 48% accuracy and adults with 83% accuracy. To further investigate variance in call features, we used a multivariate variance components model to estimate variance partitioning in features across two levels: within- and between-individuals. Between-individual variance was the most important source of variance for all features in adults, and three of four features in infants. We show that pulse-chirps of adult titi monkey duets are individually distinct, and infant trills are less individually distinct, which may be due to the different functions of the vocalizations.