Monkey Alarm Calls Research Articles

Sex differences in the acoustic structure of terrestrial alarm calls in vervet monkeys (Chlorocebus pygerythrus).

The alarm calls of vervet monkeys (Chlorocebus pygerythrus) have been the subject of considerable focus by researchers, owing primarily to the purported referential qualities of different alarm call types. With this focus on reference, acoustic variation among calls elicited by the same range of predators has typically been overlooked. Specifically, at least one type of alarm call-the terrestrial alarm-was described over 50 years ago as being acoustically distinct between males and females-a description that has largely eluded more systematic scrutiny. Here, we provide a quantitative acoustic analysis and comparison of terrestrial alarm calls produced by adult male and female vervet monkeys. We use a random forest model to determine which acoustic variables best distinguish between the calls of males and females, and use an unsupervised clustering technique to objectively determine whether alarms produced by each sex fall into discrete types. We found that the calls of males and females differed most in frequency-based parameters, with male alarms containing more energy at lower frequencies relative to females. Calls produced by males were also of longer duration, and consisted of longer individual call elements relative to female calls. While calls generally fell into clusters associated with either male or female alarms, we found that some fell into atypical clusters given the caller's sex, and that the clusters themselves showed evidence of intergradation. We discuss these results in terms of potential differences in the function of, and motivation for, calling by males and females. We emphasize the need for a more holistic approach to the classification of vocal signals that considers contextual, functional, and structural variation.

Pyow-Hack: Ordered Compositions in Lewis-Skyrms Signaling Games

AbstractThis paper presents a Lewis-Skyrms signaling game that can exhibit a type of compositionality novel to the signaling game literature. The structure of the signaling game is motivated by an analogy to the alarm calls of putty-nosed monkeys (Cercopithecus nictitans). Putty-nosed monkeys display a compositional system of alarm calls with a semantics that is sensitive to the ordering of terms. This sensitivity to the ordering of terms has not been previously modeled with a Lewis-Skyrms signaling game literature. Signaling games are valued for showing how communicative systems can arise with minimal learning tools. Simulation results show that basic (Roth-Erev) reinforcement learning is sufficient for the acquisition of a compositional signaling system sensitive to the ordering of terms.

Aping Language: Historical Perspectives on the Quest for Semantics, Syntax, and Other Rarefied Properties of Human Language in the Communication of Primates and Other Animals.

In 1980, Robert Seyfarth, Dorothy Cheney and Peter Marler published a landmark paper in Science claiming language-like semantic communication in the alarm calls of vervet monkeys. This article and the career research program it spawned for its authors catalyzed countless other studies searching for semantics, and then also syntax and other rarefied properties of language, in the communication systems of non-human primates and other animals. It also helped bolster a parallel tradition of teaching symbolism and syntax in artificial language systems to great apes. Although the search for language rudiments in the communications of primates long predates the vervet alarm call story, it is difficult to overstate the impact of the vervet research, for it fueled field and laboratory research programs for several generations of primatologists and kept busy an equal number of philosophers, linguists, and cognitive scientists debating possible implications for the origins and evolution of language and other vaunted elements of the human condition. Now 40-years on, the original vervet alarm call findings have been revised and claims of semanticity recanted; while other evidence for semantics and syntax in the natural communications of non-humans is sparse and weak. Ultimately, we are forced to conclude that there are simply few substantive precedents in the natural communications of animals for the high-level informational and representational properties of language, nor its complex syntax. This conclusion does not mean primates cannot be taught some version of these elements of language in artificial language systems – in fact, they can. Nor does it mean there is no continuity between the natural communications of animals and humans that could inform the evolution of language – in fact, there is such continuity. It just does not lie in the specialized semantic and syntactic properties of language. In reviewing these matters, I consider why it is that primates do not evince high-level properties of language in their natural communications but why we so readily accepted that they did or should; and what lessons we might draw from that experience. In the process, I also consider why accounts of human-like characteristics in animals can be so irresistibly appealing.

Experimental evidence that titi and saki monkey alarm calls deter an ambush predator

Many animals use alarm calls in intraspecific communication to warn conspecifics of a predator's presence or to elicit coordinated group responses. However, alarm calls may also be aimed directly at the predator to discourage further pursuit. These 'pursuit-deterrent' signals are particularly important in the presence of ambush predators that rely on stealth to hunt prey. Here, we conducted playback experiments over a 16-month period on radiocollared ocelots, Leopardus pardalis, in Peru using audio stimuli of titi monkey (Callicebus toppini) and saki monkey (Pithecia rylandsi) alarm calls, with nonalarm loud calls as controls. We predicted that, if titi and saki alarm calls function as deterrent signals, then ocelots would move away from the sound source and leave the area following exposure to alarms but not following controls. We tracked ocelots via radiotelemetry for 30 min prior to and 30 min following experiments. At 15 min intervals we noted subject location, whether the cat was stationary or moving towards, away from or parallel to the playback area (calculated using a deflection angle) and distance travelled. Results showed a significantly different pattern in response movement between playback trials; ocelots moved away from the sound source in the majority of alarm trials but remained stationary/hidden or moved in a variety of directions following control trials. Ocelots also moved significantly farther following exposure to alarm trials than following exposure to controls. We conclude that ocelots can distinguish alarm calls from other loud calls and are deterred by alarm-calling monkeys. This is the first study to use playbacks on wild predators to test the pursuit-deterrent function of primate alarm calls.

Initiating language in LIDA: Learning the meaning of vervet alarm calls

Abstract This paper initiates language in LIDA by using the Learning Intelligent Decision 1 Agent’s (LIDA) perceptual learning mechanism to suggest how an infant vervet, Chlorocebus pygerthrus, learns the meanings of vervet monkey alarm calls. We consider a multiple meanings approach which includes a feeling-based meaning, an action-based meaning, and a referential meaning. Simulations first test the learning of the meanings of these alarm calls while the infant is physically attached to the mother. The second simulations study the infant’s understanding of these alarm calls while the infant is detached physically from the mother. Our results confirm that a LIDA based agent simulating a vervet infant is capable of learning such multiple meanings. The agent learned in sequence the feeling-based meaning, the action-based meaning, and the referential meaning. The LIDA agent achieved a good understanding of each of these meanings. This work can be seen as a starting step toward modeling the learning of human language in the LIDA cognitive architecture. Such modeling of language use would be a significant addition to the LIDA model.

On the -oo Suffix of Campbell’s Monkeys

Ouattara et al. (2009a,b) make the novel claim that Campbell’s monkey alarm calls demonstrate a simple pattern of linguistic morphology. The authors observe that there are at least two distinct alarm calls (called krak and hok) that are used in two different predatory contexts, and that each may be followed by a low frequency sound (called -oo) that alters the meaning of both calls in predictable ways, allowing contexts with reduced level of threat. In light of these facts, -oo is analyzed as a meaning-bearing, combinatorial unit. However, the claim that a non-human communication system has a combinatorial system (however primitive) is rare in the literature (see x5 for related patterns), and, indeed, is antithetical to certain claims that structural hierarchy is unique to human language (e.g., Bolhuis et al. 2014). Moreover, it has been noted (Schlenker et al. 2014) that there is redundancy between the apparent semantic contribution of -oo and the semantic contribution of a variety of other signal manipulations (e.g. calling rate) that are easiest to explain via non-compositional mechanisms. These facts warrant particular caution when evaluating the pattern as a possible counterexample to generalizations about human language. Thus, in this squib, we examine the compositional hypothesis further. As counterpoint, we consider a class of more conservative hypotheses in which -oo does not itself bear meaning, but instead arises as the side effect of other articulatory processes that noncompositionally affect call meaning. Key to such hypotheses is the premise that -oo is articulatorily parasitic on another phonetic process. A major contribution of this squib is thus phonetic: considering the acoustic properties of -oo, we conclude that complex calls (krakoo and hokoo) are produced with a two pulses of a single breath-group. Critically, the production of these complex calls requires an additional articulatory gesture and thus an increase in articulatory effort. An increase in articulatory effort would not be expected on an analysis in which -oo arises as a phonetic side effect; we accordingly reject these alternate hypotheses, thus strengthening the robustness of the combinatorial analysis.

Fast computation of spatially adaptive kernel estimates

Kernel smoothing of spatial point data can often be improved using an adaptive, spatially varying bandwidth instead of a fixed bandwidth. However, computation with a varying bandwidth is much more demanding, especially when edge correction and bandwidth selection are involved. This paper proposes several new computational methods for adaptive kernel estimation from spatial point pattern data. A key idea is that a variable-bandwidth kernel estimator for d-dimensional spatial data can be represented as a slice of a fixed-bandwidth kernel estimator in $$(d+1)$$ -dimensional scale space, enabling fast computation using Fourier transforms. Edge correction factors have a similar representation. Different values of global bandwidth correspond to different slices of the scale space, so that bandwidth selection is greatly accelerated. Potential applications include estimation of multivariate probability density and spatial or spatiotemporal point process intensity, relative risk, and regression functions. The new methods perform well in simulations and in two real applications concerning the spatial epidemiology of primary biliary cirrhosis and the alarm calls of capuchin monkeys.

Can the integration hypothesis account for language evolution?

Abstract In a recent series of papers, Shigeru Miyagawa and colleagues propose an Integration Hypothesis for language evolution (Miyagawa, 2016; Miyagawa, Ojima, Berwick, & Okanoya, 2014, 2013; Nobrega & Miyagawa, 2015). This model suggests an ‘emergent’ view of language evolution in which two primitive systems, both occurring in animal communication, were integrated abruptly in our recent ancestors to form language as we know it. The proposed pre-existing systems are an ‘E’ system, for ‘expressive’, which occurs in learned birdsong, and an ‘L’ system, for ‘lexical’, which is said to have its origins in monkey alarm calls. What is distinctive about our hominin ancestors is that they alone attained the ability to ‘merge’ signals, so forming both words and syntax immediately via the integration of the L-system and the E-system. This view thus differs from much current work on the evolution of language, which suggests the gradual development of syntactic language from a pre-linguistic protolanguage. Here, I argue against the Integration Hypothesis, proposing that the two putative systems in animal communication do not have the requisite properties to form the basis for language. Conversely, the gradualist view of language evolution is well able to explain how grammatical and functional elements in language develop, uniquely in humans.

Primate vocal production and the riddle of language evolution

Trying to uncover the roots of human speech and language has been the premier motivation to study the signalling behaviour of nonhuman primates for several decades. Focussing on the question of whether we find evidence for linguistic reference in the production of nonhuman primate vocalizations, I will first discuss how the criteria used to diagnose referential signalling have changed over time, and will then turn to the paradigmatic case of semantic communication in animals, the alarm calls of vervet monkeys, Chlorocebus pygerythrus. A recent in-depth analysis of the original material revealed that, while the alarm calls could be well distinguished, calls of similar structure were also used in within- and between-group aggression. This finding is difficult to reconcile with the idea that calls denote objects in the environment. Furthermore, nonhuman primates show only minimal signs of vocal production learning, one key prerequisite for conventionalized and symbolic communication. In addition, the structure of calls in different populations or closely related species is highly conserved. In conclusion, any continuity between nonhuman primate and human communication appears to be found at the level of the processing of signals. Why and how the ancestors of our own species one day began to talk to each other continues to be an enigma. Future research should focus on changes in the neural structure supporting volitional control over vocalizations, the gene networks associated with vocal production, and the developmental processes involved in the integration of production and perception of vocalizations.

Pyow-hack revisited: Two analyses of Putty-nosed monkey alarm calls

Male Putty-nosed monkeys have two main alarm calls, pyows and hacks. While pyows have a broad distribution suggestive of a general call, hacks are often indicative of eagles. In a series of articles, Arnold and Zuberbühler showed that Putty-nosed monkeys sometimes produce distinct pyow-hack sequences made of a small number of pyows followed by a small number of hacks; and that these are predictive of group movement. Arnold and Zuberbühler claimed that pyow-hack sequences are syntactically combinatorial but not semantically compositional because their meaning cannot be derived from the meanings of their component parts. We compare two theories of this phenomenon. One formalizes and modifies the non-compositional theory. The other presents a semantically compositional alternative based on weak meanings for pyow (‘general alarm’) and hack (‘non-ground movement’), combined with pragmatic principles of competition; a crucial one is an ‘Urgency Principle’ whereby calls that provide information about the nature/location of a threat must come before calls that do not. Semantically, pyow-hack sequences are compatible with any kind of situation involving (moving) aerial predators or (arboreal) movement of the monkeys themselves. But in the former case, hacks provide information about the location of a threat, and hence should appear at the beginning of sequences. As a result, pyow-hack sequences can only be used for non-threat-related situations involving movement, hence a possible inference that they involve group movement. Without adjudicating the debate, we argue that a formal analysis can help clarify competing theories and derive new predictions that might decide between them.

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.

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.

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.

Monkey's alarm calls reveal predator location

Monkey's alarm calls reveal predator location

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.

Predator guild does not influence orangutan alarm call rates and combinations

Monkey alarm calls have shown that in the primate clade, combinatorial rules in acoustic communication are not exclusive to humans. A recent hypothesis suggests that the number of different call combinations in monkeys increases with increased number of predator species. However, the existence of combinatorial rules in great ape alarm calls remains largely unstudied, despite its obvious relevance to ideas about the evolution of human speech. In this paper, we examine the potential use of combinatorial rules in the alarm calls of the only Asian great ape: the orangutan. Alarm calls in orangutans are composed of syllables (with either one or two distinct elements), which in turn are organized into sequences. Tigers and clouded leopards are predators for Sumatran orangutans, but in Borneo, tigers are extinct. Thus, orangutans make a suitable great ape model to assess alarm call composition in relation to the size of the predator guild. We exposed orangutans on both islands to a tiger and control model. Response compositionality was analyzed at two levels (i.e., syllable and syllable sequences) between models and populations. Results were corroborated using information theory algorithms. We made specific, directed predictions for the variation expected if orangutans used combinatorial rules. None of these predictions were met, indicating that monkey alarm call combinatorial rules do not have direct homologues in orangutans. If these results are replicated in other great apes, this indicates that predation did not drive selection towards ever more combinatorial rules in the human lineage.

Graded or discrete? A quantitative analysis of Campbell's monkey alarm calls

A standard way of describing the vocal behaviour of nonhuman primates is to classify the vocal repertoire as either graded or discrete. We analysed a large database of calls given by adult males of a primate considered a typical example for discrete vocal behaviour, the forest-dwelling Campbell's monkeys, Cercopithecus campbelli. We recorded vocal responses from several dozen individuals to their main predators, crowned eagles and leopards. Using cluster analysis techniques, we found two main call types, which were modified further by optional affixation of an inflexible vocal structure. It was possible to force the four call types into eight subtypes, with various degrees of gradedness. When taking context into account, we found that acoustically discrete and nonaffixed calls tended to be given right after discovering a predator, while acoustically graded and affixed calls were given during later parts of a predator encounter and to nonpredatory disturbances. In sum, our results suggest that classifications of primate vocal repertoires as either discrete or graded are likely to be meaningless, as communicatively relevant acoustic variation can be present within seemingly discrete call types.

Evidence for semantic communication in titi monkey alarm calls

Black-fronted titi monkeys, Callicebus nigrifrons , produce acoustically distinct vocalizations in response to several predator species. Compared to other primates, the calls are remarkably quiet, high-pitched and structurally simple, suggesting that they may not function uniquely as predator-specific warning calls. To address this, we investigated whether conspecifics were able to respond to these calls in adaptive ways, by playing back call series originally given to a perched raptor (caracara) and terrestrial predatory mammals (oncilla and tayra). Monkeys responded strongly and in predator-specific ways. Specifically, listeners preferentially looked upwards when hearing raptor-related calls, and towards the presumed caller when hearing terrestrial predator-related calls. Locomotor responses were generally uncommon, but if they occurred then they were always in the expected direction. We concluded that black-fronted titi monkeys discriminated between calls given to different predators on the basis of their acoustic features and were able to make inferences about the type or likely location of the predator.

From Monkey Alarm Calls to Human Language: How Simulations Can Fill the Gap

Observations of alarm calling behavior in putty-nosed monkeys are suggestive of a link with human language evolution. However, as is often the case in studies of animal behavior and cognition, competing theories are underdetermined by the available data. We argue that computational modeling, and in particular the use of individual-based simulations, is an effective way to reduce the size of the pool of candidate explanations. Simulation achieves this both through the classification of evolutionary trajectories as either plausible or implausible, and by putting lower bounds on the cognitive complexity required to perform particular behaviors. A case is made for using both of these strategies to understand the extent to which the alarm calls of putty-nosed monkeys are likely to be a good model for human language evolution.

Campbell's monkeys use affixation to alter call meaning.

Human language has evolved on a biological substrate with phylogenetic roots deep in the primate lineage. Here, we describe a functional analogy to a common morphological process in human speech, affixation, in the alarm calls of free-ranging adult Campbell's monkeys (Cercopithecus campbelli campbelli). We found that male alarm calls are composed of an acoustically variable stem, which can be followed by an acoustically invariable suffix. Using long-term observations and predator simulation experiments, we show that suffixation in this species functions to broaden the calls' meaning by transforming a highly specific eagle alarm to a general arboreal disturbance call or by transforming a highly specific leopard alarm call to a general alert call. We concluded that, when referring to specific external events, non-human primates can generate meaningful acoustic variation during call production that is functionally equivalent to suffixation in human language.