Monkey Calls Research Articles

Vervets revisited: A quantitative analysis of alarm call structure and context specificity.

The alarm calls of vervet monkeys (Chlorocebus pygerythrus) constitute the classic textbook example of semantic communication in nonhuman animals, as vervet monkeys give acoustically distinct calls to different predators and these calls elicit appropriate responses in conspecifics. They also give similar sounding calls in aggressive contexts, however. Despite the central role the vervet alarm calls have played for understanding the evolution of communication, a comprehensive, quantitative analysis of the acoustic structure of these calls was lacking. We used 2-step cluster analysis to identify objective call types and discriminant function analysis to assess context specificity. Alarm calls given in response to leopards, eagles, and snakes could be well distinguished, while the inclusion of calls given in aggressive contexts yielded some overlap, specifically between female calls given to snakes, eagles and during aggression, as well as between male vervet barks (additionally recorded in South Africa) in leopard and aggressive contexts. We suggest that both cognitive appraisal of the situation and internal state contribute to the variation in call usage and structure. While the semantic properties of vervet alarm calls bear little resemblance to human words, the existing acoustic variation, possibly together with additional contextual information, allows listeners to select appropriate responses.

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.

Audio-vocal interaction in single neurons of the monkey ventrolateral prefrontal cortex.

Complex audio-vocal integration systems depend on a strong interconnection between the auditory and the vocal motor system. To gain cognitive control over audio-vocal interaction during vocal motor control, the PFC needs to be involved. Neurons in the ventrolateral PFC (VLPFC) have been shown to separately encode the sensory perceptions and motor production of vocalizations. It is unknown, however, whether single neurons in the PFC reflect audio-vocal interactions. We therefore recorded single-unit activity in the VLPFC of rhesus monkeys (Macaca mulatta) while they produced vocalizations on command or passively listened to monkey calls. We found that 12% of randomly selected neurons in VLPFC modulated their discharge rate in response to acoustic stimulation with species-specific calls. Almost three-fourths of these auditory neurons showed an additional modulation of their discharge rates either before and/or during the monkeys' motor production of vocalization. Based on these audio-vocal interactions, the VLPFC might be well positioned to combine higher order auditory processing with cognitive control of the vocal motor output. Such audio-vocal integration processes in the VLPFC might constitute a precursor for the evolution of complex learned audio-vocal integration systems, ultimately giving rise to human speech.

Functional MRI of the vocalization-processing network in the macaque brain.

Using functional magnetic resonance imaging in awake behaving monkeys we investigated how species-specific vocalizations are represented in auditory and auditory-related regions of the macaque brain. We found clusters of active voxels along the ascending auditory pathway that responded to various types of complex sounds: inferior colliculus (IC), medial geniculate nucleus (MGN), auditory core, belt, and parabelt cortex, and other parts of the superior temporal gyrus (STG) and sulcus (STS). Regions sensitive to monkey calls were most prevalent in the anterior STG, but some clusters were also found in frontal and parietal cortex on the basis of comparisons between responses to calls and environmental sounds. Surprisingly, we found that spectrotemporal control sounds derived from the monkey calls (“scrambled calls”) also activated the parietal and frontal regions. Taken together, our results demonstrate that species-specific vocalizations in rhesus monkeys activate preferentially the auditory ventral stream, and in particular areas of the antero-lateral belt and parabelt.

Rodent ultrasonic vocalizations are bound to active sniffing behavior.

During rodent active behavior, multiple orofacial sensorimotor behaviors, including sniffing and whisking, display rhythmicity in the theta range (~5–10 Hz). During specific behaviors, these rhythmic patterns interlock, such that execution of individual motor programs becomes dependent on the state of the others. Here we performed simultaneous recordings of the respiratory cycle and ultrasonic vocalization emission by adult rats and mice in social settings. We used automated analysis to examine the relationship between breathing patterns and vocalization over long time periods. Rat ultrasonic vocalizations (USVs, “50 kHz”) were emitted within stretches of active sniffing (5–10 Hz) and were largely absent during periods of passive breathing (1–4 Hz). Because ultrasound was tightly linked to the exhalation phase, the sniffing cycle segmented vocal production into discrete calls and imposed its theta rhythmicity on their timing. In turn, calls briefly prolonged exhalations, causing an immediate drop in sniffing rate. Similar results were obtained in mice. Our results show that ultrasonic vocalizations are an integral part of the rhythmic orofacial behavioral ensemble. This complex behavioral program is thus involved not only in active sensing but also in the temporal structuring of social communication signals. Many other social signals of mammals, including monkey calls and human speech, show structure in the theta range. Our work points to a mechanism for such structuring in rodent ultrasonic vocalizations.

The integration hypothesis of human language evolution and the nature of contemporary languages.

How human language arose is a mystery in the evolution of Homo sapiens. Miyagawa et al. (2013) put forward a proposal, which we will call the Integration Hypothesis of human language evolution, that holds that human language is composed of two components, E for expressive, and L for lexical. Each component has an antecedent in nature: E as found, for example, in birdsong, and L in, for example, the alarm calls of monkeys. E and L integrated uniquely in humans to give rise to language. A challenge to the Integration Hypothesis is that while these non-human systems are finite-state in nature, human language is known to require characterization by a non-finite state grammar. Our claim is that E and L, taken separately, are in fact finite-state; when a grammatical process crosses the boundary between E and L, it gives rise to the non-finite state character of human language. We provide empirical evidence for the Integration Hypothesis by showing that certain processes found in contemporary languages that have been characterized as non-finite state in nature can in fact be shown to be finite-state. We also speculate on how human language actually arose in evolution through the lens of the Integration Hypothesis.

The function of loud calls in black howler monkeys (Alouatta pigra): food, mate, or infant defense?

Loud calling (i.e., howling) is the single most distinctive behavioral attribute of the social system of howler monkeys (Alouatta spp.), yet no general consensus exists regarding its main function. During a 28-month study of five groups of black howler monkeys (Alouatta pigra) at Palenque National Park, Mexico, we examined whether howling mainly functioned in the defense of food resources, mates, or infants vulnerable to infanticide. We recorded 602 howling bouts. Howling occurred more frequently when monkeys were feeding, particularly on fruits, and less frequently when they were resting than would be expected by chance. Furthermore, howling was concentrated in areas of the home range in which major feeding sites were located. Howling did not occur more frequently when vulnerable infants or potentially fertile females were present versus absent, nor did the howling rate increase with an increasing number of vulnerable infants or potentially fertile females in the group. Howling bouts lasted on average 14.4 ± SE 0.5 min, and call duration was not influenced by the presence of vulnerable infants or potentially fertile females. The duration of spontaneous calls, however, was positively correlated to the percentage of feeding time in the vicinity of howling locations. In addition, vocal displays lasted longer when neighboring groups and extragroup males were within visual contact compared with spontaneous calls and calls in response to nearby calls in which there was no visual contact between callers. Our findings suggest that loud calls in black howler monkeys are multifunctional, but most frequently occur in the defense of major feeding sites. These calls also may function in the defense of infants and mates during encounters with extragroup males.

Vocal behavior of black‐fronted titi monkeys (Callicebus nigrifrons): Acoustic properties and behavioral contexts of loud calls

Loud calls can be heard over long distances due to their high amplitude and low frequency. These calls are commonly used for both within- and between-group communication in many bird and primate species. In the Neotropics, mated pairs of socially monogamous titi monkeys (genus Callicebus) emit conspicuous, coordinated loud calls. These vocalizations appear to play a role in territorial defense, a hypothesis derived from studies of only three of the 31 recognized Callicebus species. Here, we describe the acoustic properties and organization of the loud calls of black-fronted titi monkeys (Callicebus nigrifrons). We compare the behavioral and ecological contexts associated with these vocalizations to investigate their role in within- and between-group communication, resource defense, and mate defense. Black-fronted titi monkeys create loud calls by combining a finite number of syllables to form more complex phrases, which are assembled to compose long sequences of loud calls. Bioacoustic features distinguish the loud calls used in different contexts, involving communication within- and between-groups. We found support for the hypothesis that vocalizations used for between-group communication are cooperative displays used by the mated pair and other group members to regulate access to important food resources, such as fruits. On the other hand, we only found weak support for the mate defense hypothesis.

Living in a landscape of fear: the impact of predation, resource availability and habitat structure on primate range use

Spatial variation in predation risk generates a ‘landscape of fear’, with prey animals modifying their distribution and behaviour in response to this variable predation risk. In systems comprising multiple predators and prey species, a key challenge is distinguishing the independent effects of different predator guilds on prey responses. We exploited the acoustically distinct alarm calls of samango monkeys, Cercopithecus mitis erythrarchus, to create a predator-specific landscape of fear from eagles to assess its impact on space use within mixed regressive–spatial regressive models incorporating data on resource distribution and structural characteristics of the environment. The landscape of fear from eagles was the most significant determinant of samango range use, with no effect of resource availability. The monkeys also selected areas of their range with higher canopies and higher understory visibility, behaviour consistent with further minimizing risk of predation. These results contrast with those of vervet monkeys, Chlorocebus aethiops pygerythrus, at the same site for which the landscapes of fear from leopards and baboons were the most significant determinants of space use. While highlighting that predation risk is a key driver of primate behaviour in this population, the landscapes of fear experienced by samango monkeys and vervet monkeys appear to differ despite exposure to identical predator guilds. This emphasizes the importance of distinguishing between the risk effects of different predators in understanding prey ecology, but also that closely related prey species may respond to these predator-specific risks in different ways.

Semantic communication in vervet monkeys and other animals

The research field of semantic communication in animals was initiated by the study on alarm calls of vervet monkeys, Chlorocebus pygerythrus (then known as Cercopithecus aethiops) by Seyfarth, Cheney and Marler (Animal Behaviour, 1980, 28, 1070–1094). Based on observations of alarm call production and playback experiments in the natural habitat of the monkeys, Seyfarth, Cheney and Marler provided evidence that the alarm calls designated predators as external referents and conveyed sufficient information to listeners to make distinct adaptive responses in the absence of the stimulus. Their interpretation that ‘these calls show semantic properties, potentially based on the formation of internal perceptual concepts’ contrasted with the existing consensus of the time, which saw animal signals as ‘affective’, providing information only about the internal motivational state of the signaller and/or the signaller's likely behaviour. This study, particularly its semantic approach, was hugely influential in revitalizing the discussion of what animal calls ‘mean’, specifically how they are interpreted in the minds of the animals, and ultimately acted as the impetus for the construction of the ‘functionally referential’ framework in animal communication. Although this semantic approach has been criticized in terms of anthropomorphizing animal communication, understanding the underlying cognitive mechanisms is a crucial component of deconstructing animal communication systems and hence we can greatly profit from such a research trajectory. Applying linguistic concepts to animal vocal communication has opened up an enormous research field regarding the continuity between animal vocalizations and human language, integrating different disciplines including animal behaviour, comparative psychology, neurobiology, linguistics and philosophy.

Voice discrimination in four primates

One accepted function of vocalisations is to convey information about the signaller, such as its age–sex class, motivation, or relationship with the recipient. Yet, in natural habitats individuals not only interact with conspecifics but also with members of other species. This is well documented for African forest monkeys, which form semi-permanent mixed-species groups that can persist for decades. Although members of such groups interact with each other on a daily basis, both physically and vocally, it is currently unknown whether they can discriminate familiar and unfamiliar voices of heterospecific group members. We addressed this question with playbacks on monkey species known to form polyspecific associations in the wild: red-capped mangabeys, Campbell's monkeys and Guereza colobus monkeys. We tested subjects’ discrimination abilities of contact calls of familiar and unfamiliar female De Brazza monkeys. When pooling all species, subjects looked more often towards the speaker when hearing contact calls of unfamiliar than familiar callers. When testing De Brazza monkeys with their own calls, we found the same effect with the longest gaze durations after hearing unfamiliar voices. This suggests that primates can discriminate, not only between familiar and unfamiliar voices of conspecifics, but also between familiar and unfamiliar voices of heterospecifics living within a close proximity.

The Emergence of Hierarchical Structure in Human Language

We propose a novel account for the emergence of human language syntax. Like many evolutionary innovations, language arose from the adventitious combination of two pre-existing, simpler systems that had been evolved for other functional tasks. The first system, Type E(xpression), is found in birdsong, where the same song marks territory, mating availability, and similar “expressive” functions. The second system, Type L(exical), has been suggestively found in non-human primate calls and in honeybee waggle dances, where it demarcates predicates with one or more “arguments,” such as combinations of calls in monkeys or compass headings set to sun position in honeybees. We show that human language syntax is composed of two layers that parallel these two independently evolved systems: an “E” layer resembling the Type E system of birdsong and an “L” layer providing words. The existence of the “E” and “L” layers can be confirmed using standard linguistic methodology. Each layer, E and L, when considered separately, is characterizable as a finite state system, as observed in several non-human species. When the two systems are put together they interact, yielding the unbounded, non-finite state, hierarchical structure that serves as the hallmark of full-fledged human language syntax. In this way, we account for the appearance of a novel function, language, within a conventional Darwinian framework, along with its apparently unique emergence in a single species.

Chasing sounds

Prior work with Wright and others demonstrated that rhesus monkeys recognized the relative relationships of notes in common melodies. As an extension of tests of pattern similarities, tamarins were habituated to 3-sound unit patterns in an AAB or ABB form that were human phonemes, piano notes, or monkey calls. The subjects were tested with novel sounds in each category constructed either to match the prior pattern or to violate the prior habituated pattern. The monkeys attended significantly more to a violation of their habituated pattern to a new pattern when human phonemes were used, and there was a trend difference in attention toward pattern violations with melodies. Monkey call patterns generated a variety of behavioral responses, were less likely to show habituation, and did not generate a strong attention reaction to changes in the patterns. Monkeys can extract abstract rules and patterns from auditory stimuli but the stimuli, by their nature, may generate competing responses which block processing of abstract regularities.

Processing of vocalizations in humans and monkeys: A comparative fMRI study

Humans and many other animals use acoustical signals to mediate social interactions with conspecifics. The evolution of sound-based communication is still poorly understood and its neural correlates have only recently begun to be investigated. In the present study, we applied functional MRI to humans and macaque monkeys listening to identical stimuli in order to compare the cortical networks involved in the processing of vocalizations. At the first stages of auditory processing, both species showed similar fMRI activity maps within and around the lateral sulcus (the Sylvian fissure in humans). Monkeys showed remarkably similar responses to monkey calls and to human vocal sounds (speech or otherwise), mainly in the lateral sulcus and the adjacent superior temporal gyrus (STG). In contrast, a preference for human vocalizations and especially for speech was observed in the human STG and superior temporal sulcus (STS). The STS and Broca's region were especially responsive to intelligible utterances. The evolution of the language faculty in humans appears to have recruited most of the STS. It may be that in monkeys, a much simpler repertoire of vocalizations requires less involvement of this temporal territory.

Predator and non-predator long-distance calls in Guereza colobus monkeys

East African Guereza colobus monkey males are known for their conspicuous roaring behaviour; a spectacle that can dominate the predawn hours of African forests. Recent research has shown that these monkeys also produce roars during daytime hours in response to predators. While roars to leopards and eagles differ in how roaring phrases are assembled into sequences, there are no obvious structural differences between predawn roars and roars to eagles. Although recipients could use daytime information to disambiguate between the two contexts, this may be a risky strategy because eagles can be active before dawn. We carried out acoustic analyses, which showed that the duration of the first roaring phrase was significantly longer in predawn roars compared to eagle roars. Furthermore, the initial call repetition rate was faster in response to eagle roars compared to predawn roars. Apart from these two differences, all other acoustic characteristics were identical between the two contexts. Although these monkeys exhibit some of the most basic vocal behaviour found in non-human primates, callers are able to provide reliable contextual information by varying the duration and assemblage of individual vocal units. Playback experiments are needed to confirm whether recipients relate these acoustic differences to different contexts.

Social learning of vocal structure in a nonhuman primate?

BackgroundNon-human primate communication is thought to be fundamentally different from human speech, mainly due to vast differences in vocal control. The lack of these abilities in non-human primates is especially striking if compared to some marine mammals and bird species, which has generated somewhat of an evolutionary conundrum. What are the biological roots and underlying evolutionary pressures of the human ability to voluntarily control sound production and learn the vocal utterances of others? One hypothesis is that this capacity has evolved gradually in humans from an ancestral stage that resembled the vocal behavior of modern primates. Support for this has come from studies that have documented limited vocal flexibility and convergence in different primate species, typically in calls used during social interactions. The mechanisms underlying these patterns, however, are currently unknown. Specifically, it has been difficult to rule out explanations based on genetic relatedness, suggesting that such vocal flexibility may not be the result of social learning.ResultsTo address this point, we compared the degree of acoustic similarity of contact calls in free-ranging Campbell's monkeys as a function of their social bonds and genetic relatedness. We calculated three different indices to compare the similarities between the calls' frequency contours, the duration of grooming interactions and the microsatellite-based genetic relatedness between partners. We found a significantly positive relation between bond strength and acoustic similarity that was independent of genetic relatedness.ConclusionGenetic factors determine the general species-specific call repertoire of a primate species, while social factors can influence the fine structure of some the call types. The finding is in line with the more general hypothesis that human speech has evolved gradually from earlier primate-like vocal communication.

Structure and contexts in the long distance calls of Alouatta clamitans and Alouatta belzebul.

The structure of the long range calls of howler monkeys, primates of the genus Alouatta, is scarcely understood in relation to the functions they assume. Records of Alouatta clamitans and Alouatta belzebul long distance calls were obtained at different Brazilian sites. The long distance calls of both species are low‐frequency, harsh, loud sounds, uttered in sequences that may last several minutes. There is wide gradation both within and between call categories. The structure of roars and barks seems to serve different roles: barks function as graded signals of alarm, roars as resource holding potential signals used in resource defense. Observations in A. clamitans give support to such hypotheses. Roar use and structure have the most marked differences between these species. A dawn chorus of roaring was observed only for A. belzebul, which probably has a more spontaneous emission of roars, while A. clamitans use roars mainly in intergroup encounters. The structural divergence between the long range calls of these species may reflect species–typical adaptations. The presence of both brief and continuous roars in both species, but not in the most basal Alouatta palliata can bring cues to loud calling evolution in howlers. [Work supported by CNPq, FAPESP, IF/SP, FURB, CEPESBI, IBAMA/PB, and Fazenda Pacatuba.]

Hierarchical Auditory Processing Directed Rostrally along the Monkey's Supratemporal Plane

Connectional anatomical evidence suggests that the auditory core, containing the tonotopic areas A1, R, and RT, constitutes the first stage of auditory cortical processing, with feedforward projections from core outward, first to the surrounding auditory belt and then to the parabelt. Connectional evidence also raises the possibility that the core itself is serially organized, with feedforward projections from A1 to R and with additional projections, although of unknown feed direction, from R to RT. We hypothesized that area RT together with more rostral parts of the supratemporal plane (rSTP) form the anterior extension of a rostrally directed stimulus quality processing stream originating in the auditory core area A1. Here, we analyzed auditory responses of single neurons in three different sectors distributed caudorostrally along the supratemporal plane (STP): sector I, mainly area A1; sector II, mainly area RT; and sector III, principally RTp (the rostrotemporal polar area), including cortex located 3 mm from the temporal tip. Mean onset latency of excitation responses and stimulus selectivity to monkey calls and other sounds, both simple and complex, increased progressively from sector I to III. Also, whereas cells in sector I responded with significantly higher firing rates to the "other" sounds than to monkey calls, those in sectors II and III responded at the same rate to both stimulus types. The pattern of results supports the proposal that the STP contains a rostrally directed, hierarchically organized auditory processing stream, with gradually increasing stimulus selectivity, and that this stream extends from the primary auditory area to the temporal pole.

Optical Brain Imaging Reveals General Auditory and Language-Specific Processing in Early Infant Development

This study uses near-infrared spectroscopy in young infants in order to elucidate the nature of functional cerebral processing for speech. Previous imaging studies of infants' speech perception revealed left-lateralized responses to native language. However, it is unclear if these activations were due to language per se rather than to some low-level acoustic correlate of spoken language. Here we compare native (L1) and non-native (L2) languages with 3 different nonspeech conditions including emotional voices, monkey calls, and phase scrambled sounds that provide more stringent controls. Hemodynamic responses to these stimuli were measured in the temporal areas of Japanese 4 month-olds. The results show clear left-lateralized responses to speech, prominently to L1, as opposed to various activation patterns in the nonspeech conditions. Furthermore, implementing a new analysis method designed for infants, we discovered a slower hemodynamic time course in awake infants. Our results are largely explained by signal-driven auditory processing. However, stronger activations to L1 than to L2 indicate a language-specific neural factor that modulates these responses. This study is the first to discover a significantly higher sensitivity to L1 in 4 month-olds and reveals a neural precursor of the functional specialization for the higher cognitive network.

Production and perception of situationally variable alarm calls in wild tufted capuchin monkeys (Cebus apella nigritus)

Many mammalian and avian species produce conspicuous vocalizations upon encountering a predator, but vary their calling based on risk urgency and/or predator type. Calls falling into the latter category are termed “functionally referential” if they also elicit predator-appropriate reactions in listeners. Functionally referential alarm calling has been well documented in a number of Old World monkeys and lemurs, but evidence among Neotropical primates is limited. This study investigates the alarm call system of tufted capuchin monkeys (Cebus apella nigritus) by examining responses to predator and snake decoys encountered at various distances (reflecting differences in risk urgency). Observations in natural situations were conducted to determine if predator-associated calls were given in additional contexts. Results indicate the use of three call types. “Barks” are elicited exclusively by aerial threats, but the call most commonly given to terrestrial threats (the “hiccup”) is given in nonpredatory contexts. The rate in which this latter call is produced reflects risk urgency. Playbacks of these two call types indicate that each elicits appropriate antipredator behaviors. The third call type, the “peep,” seems to be specific to terrestrial threats, but it is unknown if the call elicits predator-specific responses. “Barks” are thus functionally referential aerial predator calls, while “hiccups” are better seen as generalized disturbance calls which reflect risk urgency. Further evidence is needed to draw conclusions regarding the “peep.” These results add to the evidence that functionally referential aerial predator alarm calls are ubiquitous in primates, but that noncatarrhine primates use generalized disturbance calls in response to terrestrial threats.