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.     

The acoustic structure of suricates'' alarm calls varies with predator type and the level of response urgency.

The variation in the acoustic structure of alarm calls appears to convey information about the level of response urgency in some species, while in others it seems to denote the type of predator. While theoretical models and studies on species with functionally referential calls have emphasized that any animal signal considered to have an external referent also includes motivational content, to our knowledge, no empirical study has been able to show this. In this paper, I present an example of a graded alarm call system that combines referential information and also information on the level of urgency. Acoustically different alarm calls in the social mongoose Suricata suricatta are given in response to different predator types, but their call structure also varies depending on the level of urgency. Low urgency calls tend to be harmonic across all predator types, while high urgency calls are noisier. There was less evidence for consistency in the acoustic parameters assigned to particular predator types across different levels of urgency. This suggests that, while suricates convey information about the level of urgency along a general rule, the referential information about each category of predator type is not encoded in an obvious way.     

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.     

Interspecific Semantic Alarm Call Recognition in the Solitary Sahamalaza Sportive Lemur,Lepilemur sahamalazensis

As alarm calls indicate the presence of predators, the correct interpretation of alarm calls, including those of other species, is essential for predator avoidance. Conversely, communication calls of other species might indicate the perceived absence of a predator and hence allow a reduction in vigilance. This “eavesdropping” was demonstrated in birds and mammals, including lemur species. Interspecific communication between taxonomic groups has so far been reported in some reptiles and mammals, including three primate species. So far, neither semantic nor interspecific communication has been tested in a solitary and nocturnal lemur species. The aim of this study was to investigate if the nocturnal and solitary Sahamalaza sportive lemur, Lepilemur sahamalazensis, is able to access semantic information of sympatric species. During the day, this species faces the risk of falling prey to aerial and terrestrial predators and therefore shows high levels of vigilance. We presented alarm calls of the crested coua, the Madagascar magpie-robin and aerial, terrestrial and agitation alarm calls of the blue-eyed black lemur to 19 individual Sahamalaza sportive lemurs resting in tree holes. Songs of both bird species’ and contact calls of the blue-eyed black lemur were used as a control. After alarm calls of crested coua, Madagascar magpie-robin and aerial alarm of the blue-eyed black lemur, the lemurs scanned up and their vigilance increased significantly. After presentation of terrestrial alarm and agitation calls of the blue-eyed black lemur, the animals did not show significant changes in scanning direction or in the duration of vigilance. Sportive lemur vigilance decreased after playbacks of songs of the bird species and contact calls of blue-eyed black lemurs. Our results indicate that the Sahamalaza sportive lemur is capable of using information on predator presence as well as predator type of different sympatric species, using their referential signals to detect predators early, and that the lemurs’ reactions are based on experience and learning.     

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.     

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.     

Alarm calls of the Southern House Wren Troglodytes musculus: variation with nesting stage and predator model

Alarm calls given by parents when risk is detected during nesting may be considered a form of parental defense. We analyzed variations in callings of breeding pairs of the Southern House Wren Troglodytes musculus during the nesting cycle and when faced with different predator models. Nesting birds were exposed to stuffed models at different nesting stages (early and late during incubation, and nests with younger and older nestlings). Nests were also exposed to different predator models where the calling response of breeding adults and acoustic structure variations of the calls were analyzed. The presence of a predator model increased the parents’ alarm calls along the nesting stage. This result supports the hypothesis that the higher the nest reproductive value, the higher the nest defense performed by the Southern House Wren. However, it also supports the notion that alarm calls could be used by parents to silence nestlings and reduce their detectability. Alarm calls also varied according to the predator model presented. We suggest that alarm calls variations of Southern House Wrens could encode information about the kind of predator and the risk envisaged through variations of call rates.     

Functionally referential signals: A promising paradigm whose time has passed

Finding the evolutionary origins of human language in the communication systems of our closest living relatives has, for the last several decades, been a major goal of many in the field of animal communication generally and primate communication specifically. 1 - 4 The so‐called “functionally referential” signals have long been considered promising in this regard, with apparent parallels with the semantic communication that characterizes language. The once‐prominent idea that functionally referential signals are word‐like, in that they are arbitrary sounds that refer to phenomena external to the caller, has largely been abandoned. 5 However, the idea that these signals may offer the strongest link between primate communication and human language remains widespread, primarily due to the fact the behavior of receivers indicates that such signals enable them to make very specific inferences about their physical or social environment. Here we review the concept of functional reference and discuss modern perspectives that indicate that, although the sophistication of receivers provides some continuity between nonhuman primate and human cognition, this continuity is not unique to functionally referential signals. In fact, because functionally referential signals are, by definition, produced only in specific contexts, receivers are less dependent on the integration of contextual cues with signal features to determine an appropriate response. The processing of functionally referential signals is therefore likely to entail simpler cognitive operations than does that of less context‐specific signals. While studies of functional reference have been important in highlighting the relatively sophisticated processes that underlie receiver behavior, we believe that the continued focus on context‐specific calls detracts from the potentially more complex processes underlying responses to more unspecific calls. In this sense, we argue that the concept of functional reference, while historically important for the field, has outlived its usefulness and become a red herring in the pursuit of the links between primate communication and human language. © 2012 Wiley Periodicals, Inc.     

Communication in bottlenose dolphins: 50 years of signature whistle research

Bottlenose dolphins (Tursiops truncatus) produce individually distinctive signature whistles that broadcast the identity of the caller. Unlike voice cues that affect all calls of an animal, signature whistles are distinct whistle types carrying identity information in their frequency modulation pattern. Signature whistle development is influenced by vocal production learning. Animals use a whistle from their environment as a model, but modify it, and thus invent a novel signal. Dolphins also copy signature whistles of others, effectively addressing the whistle owner. This copying occurs at low rates and the resulting copies are recognizable as such by parameter variations in the copy. Captive dolphins can learn to associate novel whistles with objects and use these whistles to report on the presence or absence of the object. If applied to signature whistles, this ability would make the signature whistle a rare example of a learned referential signal in animals. Here, we review the history of signature whistle research, covering definitions, acoustic features, information content, contextual use, developmental aspects, and species comparisons with mammals and birds. We show how these signals stand out amongst recognition calls in animals and how they contribute to our understanding of complexity in animal communication.     

Localization of Passerine Seeet and Mobbing Calls by Goshawks and Pygmy Owls

Goshawks and pygmy owls responded to recordings of passerine alarm calls by correctly orienting to their source. The seeet, or “aerial predator” alarm call which is generally assumed to be “non-localizable”, while it elicited fewer responses than did mobbing calls, was nevertheless accurately localized by all birds that did respond. The evolution of alarm calls is discussed in terms of efficient prey communication, following Darwin's “antithesis principle”, rather than predator selection for non-localizability.     

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.     

Bird calls: just emotional displays or something more?

Two widely held assumptions about the sounds of birds and other animals are (1) they are impulsive and involuntary, and cannot be controlled, and (2) they are based only on emotion, apparently because the stimuli eliciting them are thought to be very generalized. The validity of these assumptions has been tested in studies of the alarm calling and food calling behavior of domestic chickens. Videotapes of aerial and ground predators–a hawk overhead and a raccoon on the ground–were effective in eliciting the two major classes of alarm calls. The frequency of aerial alarm calling was strongly affected by presence or absence of a companion, while other aspects of antipredator behavior were unchanged. This so-called "audience effect" on calling is not found with the ground predator call, apparently because this call is addressed to the predator as well as companions. The rules for audience effects are different again with food calling. Evidently calling is not completely impulsive, but can be controlled. By varying the attributes of digitized video images of predators we have shown that stimuli eliciting the aerial predator alarm call are quite specific, encoding different information than the ground predator call. Playback experiments demonstrate that another chicken can decode this information, and react adaptively. Although emotion is undoubtedly involved in bird calling, we conclude that simple emotion-based models of bird calls are inadequate as the sole basis for explaining the vocal behavior of birds.     

Bird calls: just emotional displays or something more?

Two widely held assumptions about the sounds of birds and other animals are (1) they are impulsive and involuntary, and cannot be controlled, and (2) they are based only on emotion, apparently because the stimuli eliciting them are thought to be very generalized. The validity of these assumptions has been tested in studies of the alarm calling and food calling behavior of domestic chickens. Videotapes of aerial and ground predators–a hawk overhead and a raccoon on the ground–were effective in eliciting the two major classes of alarm calls. The frequency of aerial alarm calling was strongly affected by presence or absence of a companion, while other aspects of antipredator behavior were unchanged. This so-called "audience effect" on calling is not found with the ground predator call, apparently because this call is addressed to the predator as well as companions. The rules for audience effects are different again with food calling. Evidently calling is not completely impulsive, but can be controlled. By varying the attributes of digitized video images of predators we have shown that stimuli eliciting the aerial predator alarm call are quite specific, encoding different information than the ground predator call. Playback experiments demonstrate that another chicken can decode this information, and react adaptively. Although emotion is undoubtedly involved in bird calling, we conclude that simple emotion-based models of bird calls are inadequate as the sole basis for explaining the vocal behavior of birds.     

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 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.     

Characteristics of arctic ground squirrel alarm calls

Summary Arctic ground squirrels, Citellus undulatus, produce six distinctly different sounds. Each of these sounds may represent a signal in itself, but combinations of these acoustic elements or repetition of a single element produce additional signals. Several of these signals serve as alarm calls. One sound element consists of a short (0.05 sec) broad frequency chat while another is a longer (0.16 to 0.25 sec) descending narrow frequency whistle. Squirrels utter three-note chatter calls when approached by a ground predator, and a series of five or more chatters, which fade in intensity, is given upon the close approach of a ground predator as the squirrel escapes into a burrow. A single whistle, which resembles the alarm call of some birds, is given upon the approach of an aerial predator. This call is repeated at approximately six to eight second intervals if the predator alights near a squirrel and remains nearby.     

Semantic Differences in Sifaka (Propithecus verreauxi) Alarm Calls: A Reflection of Genetic or Cultural Variants?

In this study, we compared the usage of alarm calls and anti‐predator strategies between a captive and a wild lemur population. The wild lemur population was studied earlier in Western Madagascar ( Fichtel & Kappeler 2002 ). The captive population was studied in outdoor enclosures of the Duke University Primate Center. Alarm calls and anti‐predator behavior were elicited by conducting experiments with both vocal and visual dummies. We scored the subjects’ immediate behavioral responses, including alarm calls, from video recordings made during the experiments. In principle, both populations have a mixed alarm call system with functionally referential alarm calls for aerial predators and general alarm calls for terrestrial and aerial predators and for situations associated with high arousal, such as group encounters. Although wild and captive sifakas exhibit the same alarm call system and use the same alarm call types, we discovered striking differences in the usage and perception of some of the alarm calls. We argue that these differences indicate either an evolutionary drift in the meaning of these calls or reflect cultural variation. The latter possibility is consistent with our understanding of the ontogeny of call usage and comprehension.     

Eavesdropping on heterospecific alarm calls: from mechanisms to consequences

Animals often gather information from other species by eavesdropping on signals intended for others. We review the extent, benefits, mechanisms, and ecological and evolutionary consequences of eavesdropping on other species' alarm calls. Eavesdropping has been shown experimentally in about 70 vertebrate species, and can entail closely or distantly related species. The benefits of eavesdropping include prompting immediate anti‐predator responses, indirect enhancement of foraging or changed habitat use, and learning about predators. Eavesdropping on heterospecifics can provide more eyes looking for danger, complementary information to that from conspecifics, and potentially information at reduced cost. The response to heterospecific calls can be unlearned or learned. Unlearned responses occur when heterospecific calls have acoustic features similar to that used to recognize conspecific calls, or acoustic properties such as harsh sounds that prompt attention and may allow recognition or facilitate learning. Learning to recognize heterospecific alarm calls is probably essential to allow recognition of the diversity of alarm calls, but the evidence is largely indirect. The value of eavesdropping on different species is affected by problems of signal interception and the relevance of heterospecific alarm calls to the listener. These constraints on eavesdropping will affect how information flows among species and thus affect community function. Some species are ‘keystone’ information producers, while others largely seek information, and these differences probably affect the formation and function of mixed‐species groups. Eavesdroppers might also integrate alarm calls from multiple species to extract relevant and reliable information. Eavesdropping appears to set the stage for the evolution of interspecific deception and communication, and potentially affects communication within species. Overall, we now know that eavesdropping on heterospecific alarm calls is an important source of information for many species across the globe, and there are ample opportunities for research on mechanisms, fitness consequences and implications for community function and signalling evolution.     

Acoustic Behaviour of Birds and Mammals in the Predator Context; I. Factors Affecting the Structure of Alarm Signals. II. The Functional Significance and Evolution of Alarm Signals

I. 7 vocalizations emitted in the predator context are defined in terms of their function. The physical and physiological constraints on the evolution of the physical structure of alarm calls with respect to detectability and localizability are discussed. Detection of various calls depends on signal amplitude, environmental attenuation, signal-to-noise ratio, discrimination of the receiver against background noise, and absolute auditory sensitivity of the receiver. The combined effect of these factors is discussed for an exemplary predator-prey system, in which the hearing of both, predator and prey is known. Localizability of an alarm call is determined by its frequency, bandwidth, and possibly its amplitude relative to the auditory threshold of the receiver. Crude differentiation between localizable and non-localizable signals is not possible, and localizability of particular sounds varies between species. In some cases the question of detectability may render the problem of localizability unimportant. Besides detectability and localizability, other factors such as the acoustic background formed by the alarm calls of sympatric species and by the species' own repertoire of calls are discussed. II. Requisite conditions and available evidence for the evolution of alarm calls through individual selection and kin selection are described. Five types of alarm calls are discussed individually:

• 1 The occurrence of mobbing calls indicates that a major function of these calls is predator deterrence (“move on”), although the calls also alert other prey and promote cultural transmission of the predator's characteristics.
• 2 Alarm calls associated with evasive actions of the prey cause the predator to give up the hunt or diminish its hunting success by warning other prey, which only in some cases are closely related to the caller.
• 3 Distress calls of a seized prey either attract other prey which then mob the predator, or attract other predators, which presumably attack the first predator. In both cases the chances to escape are enhanced because the predator's attention is diverted.
• 4 Defence calls are used to threaten a predator. These calls often mimic sounds of other predators.
• 5 Distraction calls may enhance the effect of distraction display.

Although the different functions of various alarm calls are treated individually, certain of the calls may have more than one function and may be employed in nonpredator contexts as well.     

Referential labelling in Diana monkeys

Animal semantic communication has received considerable theoretical and empirical attention because of its relevance to human language. Advances have been made by studies of alarm-call behaviour in nonhumans. In monkeys, for example, there is evidence that recipients have a fairly sophisticated understanding of a call's meaning; that is, the predator type usually associated with a certain alarm call. Little is known, however, about the mental mechanisms that drive call production in nonhuman primates. In some nonprimate species, it has been found that signallers do not respond to a predator's physical features but instead seem to respond to its relative threat or direction of attack. In these species, therefore, alarm calls do not denote different predator categories but simply reflect different types or levels of danger. Because different predator categories typically impose different types and degrees of threat it is entirely possible that nonhuman primates also respond to threat rather than a predator's category. This study examined how wild Diana monkeys, Cercopithecus diana, of the Ta? forest, Ivory Coast, label predation events. By altering playback stimuli and the position of a concealed speaker, I investigated whether Diana monkeys respond with acoustically different alarm calls depending on a predator's (1) distance (close versus far), (2) elevation (above versus below), or (3) category (eagle versus leopard). Analysis of male and female alarm-call behaviour showed that Diana monkeys consistently responded to predator category regardless of immediate threat or direction of attack. Data further suggested that, in addition to predator category, monkeys' alarm calls might also convey information about the predator's distance. Copyright 2000 The Association for the Study of Animal Behaviour.