On the Meaning of Alarm Calls: A Review of Functional Reference in Avian Alarm Calling

A long‐standing question in animal communication is whether signals reveal intrinsic properties of the signaller or extrinsic properties of its environment. Alarm calls, one of the most conspicuous components of antipredator behaviour, intuitively would appear to reflect internal states of the signaller. Pioneering research in primates and fowl, however, demonstrated that signallers may produce unique alarm calls during encounters with different types of predators, suggesting that signallers through selective production of alarm calls provide to conspecific receivers information about predators in the environment. In this article, we review evidence for such ‘functional reference’ in the alarm calls of birds based on explicit tests of two criteria proposed in Macedonia & Evans’ (Ethology 93, 1993, 177) influential conceptual framework: (1) that unique alarm calls are given to specific predator categories, and (2) that alarm calls isolated from contextual information elicit antipredator responses from receivers similar to those produced during actual predator encounters. Despite the importance of research on birds in development of the conceptual framework and the ubiquity of alarm calls in birds, evidence for functionally referential alarm calls in this clade is limited to six species. In these species, alarm calls are associated with the type of predator encountered as well as variation in hunting behaviour; with defence of reproductive effort in addition to predators of adults; with age‐related changes in predation risk; and with strong fitness benefits. Our review likely underestimates the occurrence of functional reference in avian alarm calls, as incomplete application and testing of the conceptual framework has limited our understanding. Throughout, therefore, we suggest avian taxa for future studies, as well as additional questions and experimental approaches that would strengthen our understanding of the meaning of functional reference in avian alarm calls.     

Semantic communication in birds: evidence from field research over the past two decades

What do animal signals mean? This is a central question in studies on animal communication. Research into the semantics of animal signals began in 1980, with evidence that alarm calls of a non-human primate designated predators as external referents. These studies have challenged the historical assumption that such referential signaling is a unique feature of human language and produced a paradigm shift in animal communication research. Over the past two decades, an increasing number of field studies have revealed similar complexity in anti-predator communication of birds. The acoustic structures of avian alarm calls show a high degree of variation in pitch, duration, shape, and repetition rate. In addition to such distinct and graded variations, several birds combine discrete types of notes or calls into higher complex sequences. These variations in alarm calls are typically associated with the predator’s attributes, such as predator type and distance, and receivers respond to them with appropriate anti-predator behaviors. Although alarm calls of several bird species, as well as those of monkeys, appear to denote predator attributes, almost nothing is known about the cognitive processes that underlie the production and perception of these signals. In this review, I explore the existing evidence for referential signaling in birds and highlight the importance of the cognitive approach to animal communication research. I hope this review will promote further investigations of alarm-calling behavior in birds and will help enhance our understanding of the ecology and evolution of semantic communication.     

Essay on Contemporary Issues in Ethology: Variation among Mammalian Alarm Call Systems and the Problem of Meaning in Animal Signals

Understanding the information conveyed by animal signals requires studies of both production and perception. It is important to determine the relationship between signal morphology and the circumstances of production, the way signaller behavior varies with motivational state and the role of context in mediating responses to signals. Alarm calls are well-suited to research of this type because they are widespread in birds and mammals and typically evoke unambiguous responses. We review studies of alarm calling in primates and ground-dwelling sciurid rodents, concentrating especially on whether these signal systems may be viewed as ‘functionally referential’, that is, as conveying sufficient information about an event for receivers to select appropriate responses. Comparisons of the physical, behavioral and habitat characteristics of these species suggest that incompatibility of the escape responses required to avoid different classes of predators may have been an important factor in the evolution of functionally referential alarm calls.     

Functionally referential communication in a chimpanzee

The evolutionary origins of the use of speech signals to refer to events or objects in the world have remained obscure. Although functionally referential calls have been described in some monkey species, studies with our closest living relatives, the great apes, have not generated comparable findings. These negative results have been taken to suggest that ape vocalizations are not the product of their otherwise sophisticated mentality and that ape gestural communication is more informative for theories of language evolution. We tested whether chimpanzee rough grunts, which are produced during feeding contexts, functioned as referential signals. Individuals produced acoustically distinct types of "rough grunts" when encountering different foods. In a naturalistic playback experiment, a focal subject was able to use the information conveyed by these calls produced by several group mates to guide his search for food, demonstrating that the different grunt types were meaningful to him. This study provides experimental evidence that our closest living relatives can produce and understand functionally referential calls as part of their natural communication. We suggest that these findings give support to the vocal rather than gestural theories of 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.     

Marmoset (Callithrix geoffroyi) Food-Associated Calls are Functionally Referential

Signals that are functionally referential provide listeners with information about a signaler's external environment, such as the presence of a nearby predator. Just as alarm calls may signal the presence of a predator, food-associated calls may signal the presence of food. To date, however, the only conclusive evidence that conspecifics perceive information about food from food-associated calls comes from a single species, the domestic chicken. Geoffroy's marmosets, small, arboreal New World primates, often emit food-associated calls when finding or consuming food. We presented playbacks of food calls and control sounds to two groups of naturalistically housed marmosets and observed the frequency of food-related behaviors (FRBs) during the 20-min post-playback period. Relative to the control playbacks, food call playbacks elicited an increase in the frequency of two FRBs (foraging and feeding), lasting throughout the post-playback observations. Moreover, the effect of food call playbacks was robust, occurring without regard to the type of food eliciting the food calls, the rate of food calling, or whether the signaler was a member of the receiver's group. To our knowledge, this research is the first to demonstrate that the food-associated calls of a primate species, like the food-associated calls of domestic chickens, meet the perception criterion for functionally referential communication. The results are discussed in light of the affective and cognitive mechanisms that may underlie the responses of receivers to hearing food-associated calls given by marmoset conspecifics.     

The neural circuitry underlying primate calls and human language

There are significant structural and functional differences between primate calls and human speech. In addition, these two forms of vocal communication appear to largely depend on nonhomologous brain structures. However, an analysis of the underlying axonal circuitry of these brain systems suggests that there are significant interrelationships between them, both in functional and in evolutionary terms. Based on both primate neuroanatomical studies and humanin vivo mapping studies it is argued that the ventral prefrontal area is the critical link, both functionally and anatomically between these distinct vocal systems. A model of human brain evolution with respect to language is proposed in which limbic-midbrain vocalization circuits became progressively subordinated to the activity of prefrontal-midbrain and frontalmotor circuits for regulating facial gesture, skilled oral food manipulation, and conditional association learning. Quantitative and developmental data are used to suggest that this resulted from the relative enlargement of prefrontal areas and the consequences this has on the relative proportions of different corticomidbrain and diencephalic-midbrain projections. Although humans exhibit a significantly reduced call repertoire, it is argued that the display-vocalization circuits that play the central role in all other primate communication have neither been eliminated, supplanted nor suppressed by language systems. They have instead become integrated into the more distributed language circuits and play a ubiquitous though subordinate role in all normal language processes.     

Functionally Referential Alarm Calls in Tamarins (Saguinus fuscicollis and Saguinus mystax) – Evidence from Playback Experiments

Studies on primate vocalisation have revealed different types of alarm call systems ranging from graded signals based on response urgency to functionally referential alarm calls that elicit predator‐specific reactions. In addition, alarm call systems that include both highly specific and other more unspecific calls have been reported. There has been consistent discussion on the possible factors leading to the evolution of different alarm call systems, among which is the need of qualitatively different escape strategies. We studied the alarm calls of free‐ranging saddleback and moustached tamarins (Saguinus fuscicollis and Saguinus mystax) in northeast Peru. Both species have predator‐specific alarm calls and show specific non‐vocal reactions. In response to aerial predators, they look upwards and quickly move downwards, while in response to terrestrial predators, they look downwards and sometimes approach the predator. We conducted playback experiments to test if the predator‐specific reactions could be elicited in the absence of the predator by the tamarins’ alarm calls alone. We found that in response to aerial alarm call playbacks the subjects looked significantly longer upwards, and in response to terrestrial alarm call playbacks they looked significantly longer downwards. Thus, the tamarins reacted as if external referents, i.e. information about the predator type or the appropriate reaction, were encoded in the acoustic features of the calls. In addition, we found no differences in the responses of S. fuscicollis and S. mystax whether the alarm call stimulus was produced by a conspecific or a heterospecific caller. Furthermore, it seems that S. fuscicollis terrestrial alarm calls were less specific than either S. mystax terrestrial predator alarms or either species’ aerial predator alarms, but because of the small sample size it is difficult to draw a final conclusion.     

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.     

Chimpanzee Alarm Call Production Meets Key Criteria for Intentionality

Determining the intentionality of primate communication is critical to understanding the evolution of human language. Although intentional signalling has been claimed for some great ape gestural signals, comparable evidence is currently lacking for their vocal signals. We presented wild chimpanzees with a python model and found that two of three alarm call types exhibited characteristics previously used to argue for intentionality in gestural communication. These alarm calls were: (i) socially directed and given to the arrival of friends, (ii) associated with visual monitoring of the audience and gaze alternations, and (iii) goal directed, as calling only stopped when recipients were safe from the predator. Our results demonstrate that certain vocalisations of our closest living relatives qualify as intentional signals, in a directly comparable way to many great ape gestures. We conclude that our results undermine a central argument of gestural theories of language evolution and instead support a multimodal origin of human language.     

Functionally Referential Communication in Mammals: The Past,Present and the Future

Whether animal vocalizations have the potential to communicate information regarding ongoing external events or objects has received considerable attention over the last four decades. Such ‘functionally referential signals’ (Macedonia & Evans 1993) have been shown to occur in a range of mammals and bird species and as a consequence have helped us understand the complexities that underlie animal communication, particularly how animals process and perceive their socio‐ecological worlds. Here, we review the existing evidence for functionally referential signals in mammals according to the framework put forward in the seminal Macedonia and Evans review paper. Furthermore, we elucidate the ambiguities regarding the functionally referential framework that have become obvious over the last years. Finally, we highlight new potential areas for investigation within referential signalling. We conclude the functionally referential framework is still informative when interpreting the meaning of animal vocalizations but, based on emerging research, requires further integration with other approaches investigating animal vocal complexity to broaden its applicability.     

The evolution of functionally referential meaning in a structured world

Animal communication systems serve to transfer both motivational information--about the intentions or emotional state of the signaler--and referential information--about external objects. Although most animal calls seem to deal primarily with motivational information, those with a substantial referential component are particularly interesting because they invite comparison with words in human language. We present a game-theoretic model of the evolution of communication in a "structured world", where some situations may be more similar to one another than others, and therefore require similar responses. We find that breaking the symmetry in this way creates the possibility for a diverse array of evolutionarily stable communication systems. When the number of signals is limited, as in alarm calling, the system tends to evolve to group together situations which require similar responses. We use this observation to make some predictions about the situations in which primarily motivational or referential communication systems will evolve.     

Multimodal communication and language origins: integrating gestures and vocalizations

The presence of divergent and independent research traditions in the gestural and vocal domains of primate communication has resulted in major discrepancies in the definition and operationalization of cognitive concepts. However, in recent years, accumulating evidence from behavioural and neurobiological research has shown that both human and non‐human primate communication is inherently multimodal. It is therefore timely to integrate the study of gestural and vocal communication. Herein, we review evidence demonstrating that there is no clear difference between primate gestures and vocalizations in the extent to which they show evidence for the presence of key language properties: intentionality, reference, iconicity and turn‐taking. We also find high overlap in the neurobiological mechanisms producing primate gestures and vocalizations, as well as in ontogenetic flexibility. These findings confirm that human language had multimodal origins. Nonetheless, we note that in great apes, gestures seem to fulfil a carrying (i.e. predominantly informative) role in close‐range communication, whereas the opposite holds for face‐to‐face interactions of humans. This suggests an evolutionary shift in the carrying role from the gestural to the vocal stream, and we explore this transition in the carrying modality. Finally, we suggest that future studies should focus on the links between complex communication, sociality and cooperative tendency to strengthen the study of language origins.     

Do aggressive signals evolve towards higher reliability or lower costs of assessment?

It has been suggested that the evolution of signals must be a wasteful process for the signaller, aimed at the maximization of signal honesty. However, the reliability of communication depends not only on the costs paid by signallers but also on the costs paid by receivers during assessment, and less attention has been given to the interaction between these two types of costs during the evolution of signalling systems. A signaller and receiver may accept some level of signal dishonesty by choosing signals that are cheaper in terms of assessment but that are stabilized with less reliable mechanisms. I studied the potential trade‐off between signal reliability and the costs of signal assessment in the corncrake (Crex crex). I found that the birds prefer signals that are less costly regarding assessment rather than more reliable. Despite the fact that the fundamental frequency of calls was a strong predictor of male size, it was ignored by receivers unless they could directly compare signal variants. My data revealed a response advantage of costly signals when comparison between calls differing with fundamental frequencies is fast and straightforward, whereas cheap signalling is preferred in natural conditions. These data might improve our understanding of the influence of receivers on signal design because they support the hypothesis that fully honest signalling systems may be prone to dishonesty based on the effects of receiver costs and be replaced by signals that are cheaper in production and reception but more susceptible to cheating.     

Language, Handedness, and Primate Brains: Did the Australopithecines Sign?

Evidence from comparative primate neuroanatomy, archaeology, and studies of vocalization systems of nonhuman primates suggests that human vocal language has a long evolutionary history and that there is continuity between our early primate ancestors' call systems and human speech. Old World monkeys exhibit cerebral asymmetries similar to those that appear related to human language. If arboreal monkeylike ancestors of humans were also characterized by cerebral asymmetry, then the fundamental asymmetry that forms the neurological substrate for human language may have been established through selection for simple "discrete" call systems in an arboreal habitat and would have occurred much longer ago than previously thought. The eventual shift from an arboreal to a terrestrial habitat was accompanied by increased complexity ("gradation") of vocal communication systems. The archaeological record of tools suggests that communication systems became still more complex under the selective pressures that led to bipedalism and that language had been selected for by the time that bipedalism was achieved. Contrary to the gestural hypothesis, right-handedness (which could not have preceded freeing of the hands) succeeded speech and may have been due to selective pressures for increased complexity of communication, causing a Field Effect upon the brain. [australopithecine, cerebral asymmetry, language, primate brains, right-handedness]     

Heterospecific recognition of referential alarm calls in two species of lemur

ABSTRACT

Alarm vocalizations are a common feature of the mammalian antipredator response. The meaning and function of these calls vary between species, with some species using calls to reference-specific categories of predators. Species can also use more than just the calls of conspecifics to detect threat, ‘eavesdropping’ on other species’ signalling to avoid predation. However, the evidence to date for both referential signalling and eavesdropping within primates is limited. We investigated two sympatric populations of wild lemur, the Coquerel’s sifaka Propithecus coquereli and the common brown lemur Eulemur fulvus, presenting them with playbacks of predator calls, conspecific alarm calls and heterospecific lemur alarm calls, and recorded their behavioural responses following the playbacks. Results suggest that the Coquerel’s sifaka may have functionally referential alarm calls with high specificity for aerial predators, but there was no evidence for any referential nature of the other call investigated. Brown lemurs appear to have a mixed alarm system, with one call being specific with respect to aerial predators. The other call investigated appeared to reference terrestrial predators. However, it was also used in other contexts, so does not meet the criteria for functional reference. Both species showed evidence for heterospecific alarm call recognition, with both the Coquerel’s sifaka and the brown lemurs responding appropriately to heterospecific aerial alarm calls.     

The communicative content of the common marmoset phee call during antiphonal calling

Vocalizations are a dominant means of communication for numerous species, including nonhuman primates. These acoustic signals are encoded with a rich array of information available to signal receivers that can be used to guide species‐typical behaviors. In this study, we examined the communicative content of common marmoset phee calls, the species‐typical long distance contact call, during antiphonal calling. This call type has a relatively stereotyped acoustic structure, consisting of a series of long tonal pulses. Analyses revealed that calls could be reliably classified based on the individual identity and social group of the caller. Our analyses did not, however, correctly classify phee calls recorded under different social contexts, although differences were evident along individual acoustic parameters. Further tests of antiphonal calling interactions showed that spontaneously produced phee calls differ from antiphonal phee calls in their peak and end frequency, which may be functionally significant. Overall, this study shows that the marmoset phee call has a rich communicative content encoded in its acoustic structure available to conspecifics during antiphonal calling exchanges. Am. J. Primatol. 72:974–980, 2010. © 2010 Wiley‐Liss, Inc.     

Motivation before meaning: motivational information encoded in meerkat alarm calls develops earlier than referential information

In contrast to historical assumptions about the affective nature of animal vocalizations, it is now clear that many vertebrates are capable of producing specific alarm calls in response to different predators, calls that provide information that goes beyond the motivational state of a caller. However, although these calls function referentially, it does not mean that they are devoid of motivational content. Studies on meerkats (Suricata suricatta) directly support this conclusion. The acoustic structure of their alarm calls simultaneously encodes information that is both motivational (level of urgency) and referential (predator specific). In this study, we investigated whether alarm calls of young meerkats undergo developmental modification and whether the motivational or the referential aspect of calls changes more over time. We found that, based on their acoustic structure, calls of young showed a high correct assignment to low- and high-urgency contexts but, in contrast to adults, low assignment to specific predator types. However, the discrimination among predator types was better in high-urgency than in low-urgency contexts. Our results suggest that acoustic features related to level of urgency are expressed earlier than those related to predator-specific information and may support the idea that referential calls evolve from motivational signals.     

Individual and Contextual Variation in Thomas Langur Male Loud Calls

Individual and contextual differences in male loud calls of wild Thomas langurs (Presbytis thomasi) were studied in northern Sumatra, Indonesia. Loud calls were given in the following contexts: morning calls, vocal responses to other groups, between‐group encounter calls and alarm calls. Loud call spectrograms were analysed for a large number of variables. With discriminant analyses, 14 variables were found to be important in distinguishing individuals and contexts. Loud calls were assigned to the correct individual in 95.6% of the cases (91.8% with ‘leave‐one‐out’ validation) and to the correct context in 52.2% of the cases (39.0% with ‘leave‐one‐out’ validation). Further analyses with two‐way anova s showed significant differences in both temporal and frequency variables between individuals and contexts. Loud calls seemed to differ between the contexts in functionally meaningful ways, relating to the distance of the intended receivers and to the urgency of the message. Observation showed that females in the caller's group collected infants more often in the between‐group encounter context and in the alarm call context than in the vocal exchange context. These differential responses suggest that the monkeys also perceive the measurable differences in loud call characteristics between the various contexts.     

Dogs' gaze following is tuned to human communicative signals

Recent evidence suggests that preverbal infants' gaze following can be triggered only if an actor's head turn is preceded by the expression of communicative intent [1]. Such connectedness between ostensive and referential signals may be uniquely human, enabling infants to effectively respond to referential communication directed to them. In the light of increasing evidence of dogs' social communicative skills [2], an intriguing question is whether dogs' responsiveness to human directional gestures [3] is associated with the situational context in an infant-like manner. Borrowing a method used in infant studies [1], dogs watched video presentations of a human actor turning toward one of two objects, and their eye-gaze patterns were recorded with an eye tracker. Results show a higher tendency of gaze following in dogs when the human's head turning was preceded by the expression of communicative intent (direct gaze, addressing). This is the first evidence to show that (1) eye-tracking techniques can be used for studying dogs' social skills and (2) the exploitation of human gaze cues depends on the communicatively relevant pattern of ostensive and referential signals in dogs. Our findings give further support to the existence of a functionally infant-analog social competence in this species.