Interleukin-1 induces sleep-like behavior and alters call structure in juvenile rhesus macaques

To date, there have been no investigations of the behavioral effects of interleukin-1 (IL-1) in nonhuman primates. In this study the locomotor behavior and vocalizations of juvenile rhesus monkeys were monitored for 45 minutes following intravenous injections of recombinant human IL-1 alpha. In addition, their reaction to a broadcasted recording of infant monkey distress calls was determined 20 minutes after the beginning of each test session. IL-1 induced sleep-like inactivity and significantly diminished the monkey's behavioral and vocal responses to the broadcasted calls. The coo calls uttered by the monkeys following IL-1 treatment also had a longer duration and lower fundamental frequency than calls during the control condition. As several studies have indicated that behavioral effects of IL-1 may be mediated by corticotropin-releasing hormone (CRH), a second group of rhesus monkeys was given injections of CRH. CRH did not alter behavior or call structure at the dose administered. These results extend previous research on the behavioral effects of IL-1 to include the nonhuman primate and provide the first evidence that cytokines can affect vocal communication in rhesus monkeys. © 1995 Wiley-Liss, Inc.     

Food-Associated Calling in Gorillas (Gorilla g. gorilla) in the Wild

Many nonhuman primates produce food-associated vocalizations upon encountering or ingesting particular food. Concerning the great apes, only food-associated vocalizations of chimpanzees (Pan troglodytes) and bonobos (Pan paniscus) have been studied in detail, providing evidence that these vocalizations can be produced flexibly in relation to a variety of factors, such as the quantity and quality of food and/or the type of audience. Only anecdotal evidence exists of eastern (Gorilla beringei) and western gorillas (Gorilla gorilla) producing food-associated vocalizations, termed singing or humming. To enable a better understanding of the context in which these calls are produced, we investigated and compared the vocal behavior of two free-ranging groups of western lowland gorillas (Gorilla g. gorilla) at Mondika, Republic of Congo. Our results show that (a) food-associated call production occurs only during feeding and not in other contexts; (b) calling is not uniformly distributed across age and sex classes; (c) calls are only produced during feeding on specific foods; and (d) normally just one individual gives calls during group feeding sessions, however, certain food types elicit simultaneous calling of two or more individuals. Our findings provide new insight into the vocal abilities of gorillas but also carry larger implications for questions concerning vocal variability among the great apes. Food-associated calls of nonhuman primates have been shown to be flexible in terms of when they are used and who they are directed at, making them interesting vocalizations from the viewpoint of language evolution. Food-associated vocalizations in great apes can offer new opportunities to investigate the phylogenetic development of vocal communication within the primate lineage and can possibly contribute novel insights into the origins of human language.     

Tracking silence: adjusting vocal production to avoid acoustic interference

Organisms that use vocal signals to communicate often modulate their vocalizations to avoid being masked by other sounds in the environment. Although some environmental noise is continuous, both biotic and abiotic noise can be intermittent, or even periodic. Interference from intermittent noise can be avoided if calls are timed to coincide with periods of silence, a capacity that is unambiguously present in insects, amphibians, birds, and humans. Surprisingly, we know virtually nothing about this fundamental capacity in nonhuman primates. Here we show that a New World monkey, the cotton-top tamarin (Saguinus oedipus), can restrict calls to periodic silent intervals in loud white noise. In addition, calls produced during these silent intervals were significantly louder than calls recorded in silent baseline sessions. Finally, average call duration dropped across sessions, indicating that experience with temporally patterned noise caused tamarins to compress their calls. Taken together, these results show that in the presence of a predictable, intermittent environmental noise, cotton-top tamarins are able to modify the duration, timing, and amplitude of their calls to avoid acoustic interference.     

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.     

Born to sing! Song development in a singing primate

In animal vocal communication, the development of adult-like vocalization is fundamental to interact appropriately with conspecifics. However, the factors that guide ontogenetic changes in the acoustic features remain poorly understood. In contrast with a historical view of nonhuman primate vocal production as substantially innate, recent research suggests that inheritance and physiological modification can only explain some of the developmental changes in call structure during growth. A particular case of acoustic communication is the indris’ singing behavior, a peculiar case among Strepsirrhine primates. Thanks to a decade of intense data collection, this work provides the first long-term quantitative analysis on song development in a singing primate. To understand the ontogeny of such a complex vocal output, we investigated juvenile and sub-adult indris’ vocal behavior, and we found that young individuals started participating in the chorus years earlier than previously reported. Our results indicated that spectro-temporal song parameters underwent essential changes during growth. In particular, the age and sex of the emitter influenced the indris’ vocal activity. We found that frequency parameters showed consistent changes across the sexes, but the temporal features showed different developmental trajectories for males and females. Given the low level of morphological sexual dimorphism and the marked differences in vocal behavior, we hypothesize that factors like social influences and auditory feedback may affect songs’ features, resulting in high vocal flexibility in juvenile indris. This trait may be pivotal in a species that engages in choruses with rapid vocal turn-taking.     

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.     

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.     

Perception of harmonics in the combination long call of cottontop tamarins, Saguinus oedipus

A number of nonhuman primates produce vocalizations with time-varying harmonic structure. Relatively little is known about whether such spectral information plays a role in call type classification. We address this problem by utilizing acoustic analyses and playback experiments on cottontop tamarins‘ combi nation long call, a species-typical vocalization with a characteristic harmonic structure. Specifically, we used habituation-discrimination experiments to test whether particular frequency components, as well as the relationship between components, have an effect on the perception and classification of long calls. In Condition 1, we show that tamarins classify natural and synthetic exemplars of the long call as perceptually similar, thereby allowing us to use synthetics to manipulate components of this signal precisely. In subsequent conditions, we tested the perceptual salience and discriminability of long calls in which we deleted (1) the second harmonic, (2) the fundamental frequency, or (3) all frequencies above the fundamental; we also examined the effects of frequency mistuning by shifting the second harmonic by 1000 Hz. Following habituation to unmanipulated long calls, tamarins did not respond (transferred habituation) to long calls with either a missing fundamental frequency or the second harmonic, but responded (discriminated) to long calls with the upper harmonics eliminated or with the second harmonic mistuned. These studies reveal the importance of harmonic structure in tamarin perception, and highlight the advantages of using synthetic signals for understanding how particular acoustic features drive perceptual classification in nonhuman primates. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

Evidence for Dialects in Three Captive Populations of Common Marmosets (<Emphasis Type="Italic">Callithrix jacchus</Emphasis>)

The vocal repertoires of nonhuman primates have long been thought to be invariable across populations and not to result from vocal learning. However, increasing evidence suggests that learning does influence vocal production in nonhuman primates, and that several species modify the structure of their calls in response to social or environmental influences. Vocal usage learning refers to the process whereby an individual learns in which circumstances to produce a certain call type, whereas vocal production learning refers to the process in which signals get modified as the result of individual experiences. Common marmosets (Callithrix jacchus) show socially mediated vocal plasticity as adults and during vocal development. This propensity to engage in simple forms of vocal production learning (accommodation) should produce population-level differences in call structure. To test this prediction, we compared the vocalizations of three captive populations of common marmosets. We analyzed the acoustic structure of 1337 phee calls, 461 trills, and 3611 food calls and compared them with a permutated discriminant function analysis. We found that all call types differed significantly between the three populations, and 76–98% of the calls were correctly classified. As physical differences in body mass and environmental differences between colonies could not explain the call differences, we conclude that vocal accommodation is the most likely explanation for the differences in call structure. This will allow us to further investigate the role and importance of vocal learning in a species increasingly used to study vocal learning and language evolution.     

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.     

Age- and Sex-Related Variations in Clear Calls of <Emphasis Type="Italic">Papio ursinus</Emphasis>

Changes in vocalizations during ontogeny can in principle be related to three factors: growth, maturation, and experience, i.e., learning. While learning is a prerequisite for the proper development of speech, it hardly appears to play a role in the development of the species-typical vocal behavior of nonhuman primates. Nonetheless, subjects of different age and sex often exhibit prominent variation in the structure of their vocalizations. We investigated ontogenetic changes and the emergence of sex-related differences in the acoustic structure of Chacma baboon (Papio ursinus) clear calls. We recorded the vocalizations emitted by individuals separated from the rest of the group or from particular individuals, in a group of baboons in the Moremi Wildlife Reserve, Botswana. We analyzed calls from 58 baboons of both sexes and all age classes. While the structure of the call appeared to be fixed from birth, call duration, the distribution of energy, and the fundamental frequency of the calls, including modulation, varied with age and sex of the caller. We discuss how body size may explain the variations. Some of the variables exhibited a different profile of variation with age between the sexes, with significant differences becoming apparent around puberty. The emergence of these sexual differences may be explained by the onset of sexual dimorphism in body size and mass. To which degree the hormonal status contributes to variation in the calling remains to be investigated.     

Suffixation influences receivers' behaviour in non-human primates

Compared to humans, non-human primates have very little control over their vocal production. Nonetheless, some primates produce various call combinations, which may partially offset their lack of acoustic flexibility. A relevant example is male Campbell''s monkeys (Cercopithecus campbelli), which give one call type (‘Krak’) to leopards, while the suffixed version of the same call stem (‘Krak-oo’) is given to unspecific danger. To test whether recipients attend to this suffixation pattern, we carried out a playback experiment in which we broadcast naturally and artificially modified suffixed and unsuffixed ‘Krak’ calls of male Campbell''s monkeys to 42 wild groups of Diana monkeys (Cercopithecus diana diana). The two species form mixed-species groups and respond to each other''s vocalizations. We analysed the vocal response of male and female Diana monkeys and overall found significantly stronger vocal responses to unsuffixed (leopard) than suffixed (unspecific danger) calls. Although the acoustic structure of the ‘Krak’ stem of the calls has some additional effects, subject responses were mainly determined by the presence or the absence of the suffix. This study indicates that suffixation is an evolved function in primate communication in contexts where adaptive responses are particularly important.     

Age- and sex-dependent contact call usage in Japanese macaques

The question of the flexibility of nonhuman primate vocal communication remains open today, especially due to early evidence of innately guided vocal production. However, socially determined flexibility can be found when the debate is moved from vocal structure to vocal usage. While increasing evidence shows that the audience quality influences the vocal behaviour of nonhuman primates, the impact of the caller’s characteristics has been far less studied. Here, we tested the influence of an individual’s sex and age on the usage style of contact calls. We recorded contact calls of male and female Japanese macaques and compared the vocal usage styles of approximately 1-year-old juveniles with those of adults at various ages. We found, first, important differences in call usage style between juveniles and adults, the latter forming temporally ruled vocal exchanges respecting an interindividual turntaking principle. Moreover, sex differences were substantial in adults but nonexistent in juveniles. Finally, age continued to influence female vocal behaviour during adulthood, whereas dominance rank explained differences between adult males. Two nonexclusive mechanisms can explain this phenomenon, that is, a socially guided development of the appropriate form of calling versus an emotional maturation to control call emission, opening new lines of research on nonhuman primate vocal development of appropriate usages.     

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.     

Calling at the highway: The spatiotemporal constraint of road noise on Pacific chorus frog communication

Loss of acoustic habitat due to anthropogenic noise is a key environmental stressor for vocal amphibian species, a taxonomic group that is experiencing global population declines. The Pacific chorus frog (Pseudacris regilla) is the most common vocal species of the Pacific Northwest and can occupy human‐dominated habitat types, including agricultural and urban wetlands. This species is exposed to anthropogenic noise, which can interfere with vocalizations during the breeding season. We hypothesized that Pacific chorus frogs would alter the spatial and temporal structure of their breeding vocalizations in response to road noise, a widespread anthropogenic stressor. We compared Pacific chorus frog call structure and ambient road noise levels along a gradient of road noise exposures in the Willamette Valley, Oregon, USA. We used both passive acoustic monitoring and directional recordings to determine source level (i.e., amplitude or volume), dominant frequency (i.e., pitch), call duration, and call rate of individual frogs and to quantify ambient road noise levels. Pacific chorus frogs were unable to change their vocalizations to compensate for road noise. A model of the active space and time (“spatiotemporal communication”) over which a Pacific chorus frog vocalization could be heard revealed that in high‐noise habitats, spatiotemporal communication was drastically reduced for an individual. This may have implications for the reproductive success of this species, which relies on specific call repertoires to portray relative fitness and attract mates. Using the acoustic call parameters defined by this study (frequency, source level, call rate, and call duration), we developed a simplified model of acoustic communication space–time for this species. This model can be used in combination with models that determine the insertion loss for various acoustic barriers to define the impact of anthropogenic noise on the radius of communication in threatened species. Additionally, this model can be applied to other vocal taxonomic groups provided the necessary acoustic parameters are determined, including the frequency parameters and perception thresholds. Reduction in acoustic habitat by anthropogenic noise may emerge as a compounding environmental stressor for an already sensitive taxonomic group.     

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.     

Efficiency of coding in macaque vocal communication

A key characteristic of human language efficiency is that more frequently used words tend to be shorter in length—the ‘law of brevity’. To date, no test of this relationship between frequency of use and length has been carried out on non-human animal vocal communication. We show here that the vocal repertoire of the Formosan macaque (Macaca cyclopis) conforms to the pattern predicted by the law of brevity, with an inverse relationship found between call duration and rate of utterance. This finding provides evidence for coding efficiency in the vocal communication system of this species, and indicates commonality in the basic structure of the coding system between human language and vocal communication in this non-human primate.     

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.