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.     

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.     

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.     

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.     

Selection for acoustic individuality within the vocal repertoire of wild chimpanzees

Individual primates typically produce acoustically distinct calls. To investigate the factors that facilitate the evolution of individual vocal signatures, we examined two components of the call repertoire of chimpanzees: the pant hoot and pant grunt. Pant hoots are long-distance signals whose recipients can be several hundred meters away, while pant grunts are short-range calls given to conspecifics within close visual range. Given their markedly different contexts of emission, we predicted that natural selection would favor the elaboration of individually distinctive acoustic features in pant hoots compared with pant grunts. Analyses of nine acoustic features revealed that pant hoots are more stereotyped within-individuals and variable between-individuals than pant grunts. These data are consistent with the hypothesis that selection may act to encode varying degrees of individuality in different components of the vocal repertoire of a single species.     

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.     

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.     

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.     

The function and mechanism of vocal accommodation in humans and other primates

The study of non‐human animals, in particular primates, can provide essential insights into language evolution. A critical element of language is vocal production learning, i.e. learning how to produce calls. In contrast to other lineages such as songbirds, vocal production learning of completely new signals is strikingly rare in non‐human primates. An increasing body of research, however, suggests that various species of non‐human primates engage in vocal accommodation and adjust the structure of their calls in response to environmental noise or conspecific vocalizations. To date it is unclear what role vocal accommodation may have played in language evolution, in particular because it summarizes a variety of heterogeneous phenomena which are potentially achieved by different mechanisms. In contrast to non‐human primates, accommodation research in humans has a long tradition in psychology and linguistics. Based on theoretical models from these research traditions, we provide a new framework which allows comparing instances of accommodation across species, and studying them according to their underlying mechanism and ultimate biological function. We found that at the mechanistic level, many cases of accommodation can be explained with an automatic perception–production link, but some instances arguably require higher levels of vocal control. Functionally, both human and non‐human primates use social accommodation to signal social closeness or social distance to a partner or social group. Together, this indicates that not only some vocal control, but also the communicative function of vocal accommodation to signal social closeness and distance must have evolved prior to the emergence of language, rather than being the result of it. Vocal accommodation as found in other primates has thus endowed our ancestors with pre‐adaptations that may have paved the way for language evolution.     

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.     

Cultural transmission of vocalizations in ravens, Corvus corax

As ravens have pronounced learning capabilities, especially in the vocal domain, cultural transmission might be a relevant factor affecting the composition of their vocal repertoires. We investigated how important cultural transmission is in establishing a raven's vocal repertoire and whether there are different pathways of transmission. We studied individually known free-ranging breeding pairs whose vocalizations were recorded during interactions with a caged pair. The mean repertoire size of these vocalizations was 12 call types per individual (from 79 types recorded from 74 individuals), with no difference between the sexes. In 81% of individuals the repertoire was composed entirely of calls also used by other individuals. Analysis of the distribution of call types among individuals regarding sex, partnership and neighbourhood and aspects of the geographical distribution of calls showed that the main pathway of cultural transmission was within the sexes. In addition, transmission occurred between pair partners, as well as between neighbouring and more distant pairs. About 40% of the calls in a raven's repertoire were transmitted within a sex and 10% between pair partners. Any two given birds in the population shared on average 20% (0-77%) of their calls. Cultural transmission within the sexes led to a pronounced sexual dimorphism in vocal behaviour. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.      

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.     

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.