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 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.     

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.     

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.     

The use of Artificial Neural Networks to classify primate vocalizations: a pilot study on black lemurs

The identification of the vocal repertoire of a species represents a crucial prerequisite for a correct interpretation of animal behavior. Artificial Neural Networks (ANNs) have been widely used in behavioral sciences, and today are considered a valuable classification tool for reducing the level of subjectivity and allowing replicable results across different studies. However, to date, no studies have applied this tool to nonhuman primate vocalizations. Here, we apply for the first time ANNs, to discriminate the vocal repertoire in a primate species, Eulemur macaco macaco. We designed an automatic procedure to extract both spectral and temporal features from signals, and performed a comparative analysis between a supervised Multilayer Perceptron and two statistical approaches commonly used in primatology (Discriminant Function Analysis and Cluster Analysis), in order to explore pros and cons of these methods in bioacoustic classification. Our results show that ANNs were able to recognize all seven vocal categories previously described (92.5–95.6%) and perform better than either statistical analysis (76.1–88.4%). The results show that ANNs can provide an effective and robust method for automatic classification also in primates, suggesting that neural models can represent a valuable tool to contribute to a better understanding of primate vocal communication. The use of neural networks to identify primate vocalizations and the further development of this approach in studying primate communication are discussed. Am. J. Primatol. 72:337–348, 2010. © 2009 Wiley‐Liss, Inc.     

Song Frequency Does Not Reflect Differences in Body Size among Males in Two Oscine Species

Large animals, having large vocal organs, produce low sound frequencies more efficiently. Accordingly, the frequency of vocalizations is often negatively related to body size across species, and also among individuals of many species, including several non‐oscine birds (non‐songbirds). Little is known about whether song frequency reveals information about body size within oscine species, which are characterized by song learning and large repertoires. We asked whether song frequency is related to body size in two oscines that differ in repertoire size: the dark‐eyed junco (Junco hyemalis) and the serin (Serinus serinus). We also asked whether the extent to which receivers sample repertoires might influence the reliability of their assessment of body size. We found that none of the frequency traits of song that we investigated was related to male body size, nor did more extensive sampling of repertoires lead to any relationship between frequency and body size. Possible reasons for these results are the small range of variation in size within species, or the elaborate vocal physiology of oscines that gives them great control over a wide frequency range. We discuss these results as they relate to female preferences for high‐frequency song that have been previously reported for oscine species.     

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.     

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入,同时为相关研究提供借鉴和参考。     

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.     

Identification of multiple simian immunodeficiency virus (SIV)-specific CTL epitopes in sooty mangabeys with natural and experimentally acquired SIV infection

Host immune responses to SIV infection in sooty mangabeys are likely to be an important determinant of how such nonhuman primate species maintain asymptomatic lentivirus infection. We have previously described two patterns of asymptomatic SIV infection in sooty mangabeys: low viral loads with vigorous SIV-specific CTL activity in SIVmac239-infected sooty mangabeys, and high viral loads with generally weak or absent SIV-specific CTL activity in naturally infected sooty mangabeys. To define the specificity of the CTL response in SIV-infected mangabeys, we characterized CTL epitopes in two naturally infected and three SIVmac239-infected sooty mangabeys. Compared with that in SIVmac239-infected mangabeys, the yield of SIV-specific CTL clones was significantly lower in naturally infected sooty mangabeys. All CTL clones were phenotypically CD3+ CD8+, and lysis was MHC restricted. Seven SIV CTL epitopes were identified in five sooty mangabeys: one in Gag and three each in Nef and Envelope (Env). The CTL epitopes mapped to conserved regions in the SIV genome and were immunodominant. Several similar or identical CTL epitopes were recognized by both naturally infected and SIVmac239-infected mangabeys that shared class I MHC alleles. To our knowledge, this is the first report of SIV-specific CTL epitopes in sooty mangabeys. Longitudinal studies of viral load and sequence variation in CTL epitopes may provide useful information on the role of CTL in control or persistence of SIV infection in sooty mangabeys.     

The evolution of nonhuman primate loud calls: Acoustic adaptation for long-distance transmission

Many nonhuman primates produce species-typical loud calls used to communicate between and within groups over long distances. Given their observed spacing functions, primate loud calls are likely to show acoustic adaptations to increase their propagation over distance. Here we evaluate the hypothesis that primates emit loud calls at relatively low sound frequencies to minimize their attenuation. We tested this hypothesis within and between species. First, we compared the frequencies of loud calls produced by each species with those of other calls from their vocal repertoires. Second, we investigated the relationship between loud call frequency and home range size across a sample of primate species. Comparisons indicated that primates produce loud calls at lower frequencies than other calls within their vocal repertoires. In addition, a significant negative relationship exists between loud call frequency and home range size among species. The relationship between call frequency and range size holds after controlling for the potentially confounding effects of body size and phylogeny. These results are consistent with the hypothesis that nonhuman primates produce loud calls at relatively low frequencies to facilitate their transmission over long distances.     

Introducing a fourth primate species to an established mixed‐species exhibit of African monkeys

Five red‐capped mangabeys (Cercocebus torquatus) were gradually introduced to an established mixed‐species exhibit containing six black and white colobus, seven mandrills, and six sooty mangabeys. Interspecific interactions were documented throughout the 3‐month introduction period and for an additional 3 months immediately thereafter. In addition, each species' behavior and exhibit use were documented before and after the addition of the fourth species. Minimal interactions were observed between the red‐capped mangabeys and the colobus or mandrills, and neither species was significantly affected by this addition. Many affiliative and aggressive interactions and changes in behavior were documented in the sooty mangabeys. However, this study shows that even closely related allopatric species can coexist in a captive environment, and the animals can benefit from this association. Zoo Biol 23:95–108, 2004. © 2004 Wiley‐Liss, Inc.     

Derived vocalizations of geladas (Theropithecus gelada) and the evolution of vocal complexity in primates

Primates are intensely social and exhibit extreme variation in social structure, making them particularly well suited for uncovering evolutionary connections between sociality and vocal complexity. Although comparative studies find a correlation between social and vocal complexity, the function of large vocal repertoires in more complex societies remains unclear. We compared the vocal complexity found in primates to both mammals in general and human language in particular and found that non-human primates are not unusual in the complexity of their vocal repertoires. To better understand the function of vocal complexity within primates, we compared two closely related primates (chacma baboons and geladas) that differ in their ecology and social structures. A key difference is that gelada males form long-term bonds with the 2-12 females in their harem-like reproductive unit, while chacma males primarily form temporary consortships with females. We identified homologous and non-homologous calls and related the use of the derived non-homologous calls to specific social situations. We found that the socially complex (but ecologically simple) geladas have larger vocal repertoires. Derived vocalizations of geladas were primarily used by leader males in affiliative interactions with 'their' females. The derived calls were frequently used following fights within the unit suggesting that maintaining cross-sex bonds within a reproductive unit contributed to this instance of evolved vocal complexity. Thus, our comparison highlights the utility of using closely related species to better understand the function of vocal complexity.     

Sex differences in the vocal repertoire of adult red‐capped mangabeys (Cercocebus torquatus): a multi‐level acoustic analysis

Sex differences in the vocal behavior of nonhuman primates can take various forms: sex‐specific call types, differential production of shared call types, or sex discrepancy in phonation. Also, a growing literature is evidencing that systematically analyzing the vocal repertoires of primates at the call level might lead to underestimating their communicative abilities. Here, we present an extensive multi‐level analysis of the still unknown vocal repertoire of adult red‐capped mangabeys (Cercocebus torquatus), with a special emphasis on sex differences. We collected recordings from seven adult males and seven adult females housed in captivity. We present a structurally‐based classification of mangabey calls that we cross‐validated by an analysis of the associated contexts of emission. We found 12 sound units (including six sex‐specific) that were concatenated to form eight call types (including four sex‐specific), which were produced either singularly or in sequences composed of one (“repetition”) or several (“combination”) call types. We extracted organizational principles that ruled call composition and calling patterns. This revealed a high degree of potentially meaningful variability in terms of semantics and syntax. Male–female discrepancy in terms of phonation could be related to morphological dimorphism and would enable listeners to behave appropriately according to the sex of the caller. Sex differences in repertoire size, structural gradation, and call usage could reflect specificities of male–female social roles. We discuss the pertinence of these sex differences according to social system and habitat quality. Am. J. Primatol. 72:360–375, 2010. © 2010 Wiley‐Liss, Inc.     

Dietary variation and food hardness in sooty mangabeys (Cercocebus atys): Implications for fallback foods and dental adaptation

We present information on food hardness and monthly dietary changes in female sooty mangabeys (Cercocebus atys) in Tai Forest, Ivory Coast to reassess the hypothesis that thick molar enamel is parsimoniously interpreted as a response to consumption of hard foods during fallback periods. We demonstrate that the diet of sooty mangabeys varies seasonally, but that one food—Sacoglottis gabonensis—is the most frequently consumed food every month and year round. This food is the hardest item in the sooty diet. Given that this species has among the thickest enamel within the primate order, a plausible conclusion is that thick enamel in this taxon evolved not in response to seasonally critical function or fallback foods, but rather to the habitual, year round processing of a mechanically protected foodstuff. These data serve as a caution against de rigueur interpretations that reliance on fallback foods during lean periods primarily explains the evolution of thick enamel in primates. Am J Phys Anthropol 154:413–423, 2014. © 2014 Wiley Periodicals, Inc.     

Detection of intracellular signal transduction molecules in PBMC from rhesus macaques and sooty mangabeys

Abstract: One of the manifestations of human HIV-1 and nonhuman primate SIV infection that lead to disease is reasoned to be secondary to generalized T-cell dysfunction. The molecular mechanisms associated with the T-cell dysfunction remain to be elucidated. To address this issue, we sought to utilize the nonhuman primate model to study intracellular signaling events in cells from disease-susceptible rhesus macaques and disease-resistant sooty mangabeys. Because relatively little is known about these events in nonhuman primates, our laboratory defined optimal conditions, reagents, and assays for the study of signal transduction events in cells from nonhuman primates. The protein phosphorylation patterns in the two monkeys exhibited quantitative, qualitative, and kinetic differences. Antibodies to Stat6 detected a unique band in macaque cell lysates. This band is markedly decreased human cell lysates and never seen in mangabey cell lysates. Detection of various other intracellular signaling proteins is also described.     

Vocal production in nonhuman primates: Acoustics,physiology, and functional constraints on “honest” advertisement

The physiological mechanisms and acoustic principles underlying sound production in primates are important for analyzing and synthesizing primate vocalizations, for determining the range of calls that are physically producible, and for understanding primate communication in the broader comparative context of what is known about communication in other vertebrates. In this paper we discuss what is known about vocal production in nonhuman primates, relying heavily on models from speech and musical acoustics. We first describe the role of the lungs and larynx in generating the sound source, and then discuss the effects of the supralaryngeal vocal tract in modifying this source. We conclude that more research is needed to resolve several important questions about the acoustics of primate calls, including the nature of the vocal tract's contribution to call production. Nonetheless, enough is known to explore the implications of call acoustics for the evolution of primate communication. In particular, we discuss how anatomy and physiology may provide constraints resulting in “honest” acoustic indicators of body size. © 1995 Wiley-Liss, Inc.     

Chimpanzees Differentially Produce Novel Vocalizations to Capture the Attention of a Human

Chimpanzees produce numerous species-atypical signals when raised in captivity. Here we report contextual elements of the use of two captivity-specific vocal signals, the "raspberry" and the extended grunt. Results demonstrate that these vocalizations are not elicited by the presence of food; rather the data suggest that these vocalizations function as attention-getting signals. These findings demonstrate a heretofore underappreciated category of animal signals: novel signals invented in novel environmental circumstances. The invention and use of species-atypical signals, considered in relation to group differences in signaling repertoires in apes in their natural habitats, may index a generative capacity in these hominoid species without obvious corollary in other primate species.     

Vocal Repertoire and Its Behavioral Contexts in the Pied Tamarin, <Emphasis Type="Italic">Saguinus bicolor</Emphasis>

The study of animal sound signals can be useful in assisting conservation strategies. Understanding the vocal repertoires of endangered species and the behavioral contexts in which they are given is relevant for monitoring protocols, such as those based on automated sound recordings. The pied tamarin (Saguinus bicolor) is at risk of extinction because of deforestation and urban growth in its restricted geographic range. Between 2012 and 2015 we studied the vocal repertoire of the species and the contexts in which different signals are emitted. We made focal recordings of eight free-living groups, two rescued individuals, and one temporarily captive group of pied tamarins in Manaus, central Brazilian Amazonia. From the 766 sounds analyzed we identified 12 distinct signals within the range of 2–11 kHz. Most signals were emitted during resting or locomotion. Less frequently emitted signals were associated with intergroup agonistic interactions, foraging, and infant-exclusive vocalizations. These results increased the known vocal repertoire of the pied tamarin providing more reliable baseline data for monitoring the species by means of automated or focal sound recordings.