Development of infant baboons' responses to graded bark variants.

We studied the development of infant baboons' (Papio cynocephalus ursinus) responses to conspecific 'barks' in a free-ranging population in the Okavango Delta, Botswana. These barks grade from tonal, harmonically rich calls into calls with a more noisy, harsh structure. Typically, tonal variants are given when the signaller is at risk of losing contact with the group or a particular individual ('contact barks'), whereas harsh variants are given in response to predators ('alarm barks'). We conducted focal observations and playback experiments in which we presented variants of barks recorded from resident adult females. By six months of age, infants reliably discriminated between typical alarm and contact barks and they responded more strongly to intermediate alarm calls than to typical contact barks. Infants of six months and older also recognized their mothers by voice. The ability to discriminate between different call variants developed with increasing age. At two and a half months of age, infants failed to respond at all, whereas at four months they responded irrespective of the call type that was presented. At six months, infants showed adult-like responses by responding strongly to alarm barks but ignoring contact barks. We concluded that infants gradually learn to attach the appropriate meaning to alarm and contact barks.     

Responses of Redfronted Lemurs to Experimentally Modified Alarm Calls: Evidence for Urgency-Based Changes in Call Structure

Abstract The aim of this study was to investigate how information about the affective state is expressed in vocalizations. Alarm calls can serve as model systems with which to study this general question. Therefore, we examined the information content of terrestrial predator alarm calls of redfronted lemurs ( Eulemur fulvus rufus ), group-living Malagasy primates. Redfronted lemurs give specific alarm calls only towards raptors, whereas calls given in response to terrestrial predators (woofs) are also used in other situations characterized by high arousal. Woofs may therefore have the potential to express the perceived risk of a given threat. In order to examine whether different levels of arousal are expressed in call structure, we analysed woofs given during inter-group encounters or in response to playbacks of a barking dog, assuming that animals engaged in inter-group encounters experience higher arousal than during the playbacks of dog barks. A multivariate acoustic analysis revealed that calls given during group encounters were characterized by higher frequencies than calls given in response to playbacks of dog barks. In order to examine whether this change in call structure is salient to conspecifics, we conducted playback experiments with woofs, modified in either amplitude or frequencies. Playbacks of calls with increased frequency or amplitude elicited a longer orienting response, suggesting that different levels of arousal are expressed in call structure and provide meaningful information for listeners. In conclusion, the results of our study indicate that the information about the sender's affective state is expressed in the structure of vocalizations.     

Acoustic structure of alarm calls in Indian sambar (<Emphasis Type="Italic">Rusa unicolor</Emphasis>) and Indian muntjac (<Emphasis Type="Italic">Muntiacus vaginalis</Emphasis>) in South Vietnam

The alarm call acoustic structure and nonlinear vocal phenomena of the Indian sambar (Rusa unicolor) and northern Indian muntjac (Muntiacus vaginalis) have been analyzed in detail as well as their vocal behavior in response to mobbing humans under natural conditions of southern Vietnam. The alarm calls of sambars, tonal barks separated by large intervals, were produced by animals standing on the place and gazing at a potentially dangerous object. Muntjacs flee off in danger and produced a series of dull barks interrupted with short intervals from a distance. The alarm call frequencies were characterized for sambars and muntjacs. The results of our study have been compared with the published data on alarm calls of other Cervidae species.     

Sex recognition in brown skuas: do acoustic signals matter?

Bird vocalisations are often essential for sex recognition, especially in species that show little morphological sex dimorphism. Brown skuas (Catharacta antarctica lonnbergi), which exhibit uniform plumage across both sexes, emit three main calls: the long call, the alarm call and the contact call. We tested the potential for sex recognition in brown skua calls of 42 genetically sexed individuals by analysing 8–12 acoustic parameters in the temporal and frequency domains of each call type. For every call type, we failed to find sex differences in any of the acoustic parameters measured. Stepwise discriminant function analysis (DFA) revealed that sexes cannot be unambiguously classified, with increasing uncertainty of correct classification from contact calls to long calls to alarm calls. Consequently, acoustic signalling is probably not the key mechanism for sex recognition in brown skuas.     

Context-specific calls in wild chimpanzees, Pan troglodytes verus: analysis of barks

Context-specific calls, which have a distinct acoustic structure and are selectively produced in specific contexts, are a prerequisite for calls that function referentially. Functionally referential calls, which convey information to conspecifics about objects and events in the external world, have been found in a number of species, notably primates. Evidence of context-specific calls in apes, however, is largely absent. We analysed whether the barks of wild male chimpanzees in the Ta? Forest, Côte d'Ivoire, are context specific. We examined the acoustic structure of barks, and other calls produced in association with barks, in six contexts, using discriminant function analysis. Chimpanzees produced context-specific signals in two ways. First, they produced two acoustically graded bark subtypes, in hunt and snake contexts, respectively. Second, they produced context-specific signal combinations of barks with acoustically different call types or drums. These signal combinations increased specificity levels in three of the six contexts to over 90%, a level similar to the classic vervet monkey, Cercophithecus aethiops, predator alarm calls. Furthermore, specific chimpanzee signals were produced in contexts other than alarm, such as travel and hunting, where the potential benefits of evolving specific calls are less obvious. These signals may convey specific context information to listeners, and thus function referentially; however, to confirm this, analyses of listeners' responses are required. The results show that two strategies for producing context-specific signals seem to have evolved in a species other than humans: chimpanzees produce context-specific bark subtypes and context-specific signal combinations. Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour.      

Factors Affecting Acoustic Variation in Barbary-macaque (Macaca sylvanus) Disturbance Calls

Semi-free-ranging Barbary macaques (Macaca sylvanus) were observed to utter distinctive calls after disturbances in the surroundings (e.g. presence of a predator, occurrence of some unusual phenomenon). These calls differed from calls given in other contexts. Most of these calls were uttered in a serial manner, some of which lasted as long as the corresponding context. The aim of this study was to determine the object-related specificity of calls and variation of acoustic parameters within a call series. The analysis revealed that acoustic features of calls varied among contexts. Within one apparently homogeneous context, both temporal and frequency characteristics shifted gradually. Furthermore, the disturbance calls clearly differed between individuals. To examine the disturbance calls' meaning, playback experiments were conducted in which alarm calls and disturbance calls were presented. After playback of an alarm call, subjects typically showed an escape response, whereas, in response to disturbance calls, they most often scanned the surroundings. Juvenile animals generally showed stronger responses than adults.     

Does Gray Squirrel (Sciurus carolinensis) Response to Heterospecific Alarm Calls Depend on Familiarity or Acoustic Similarity?

In habitats in which multiple species are prey to the same predators, individuals can greatly benefit from recognizing information regarding predators that is provided by other species. Past studies have demonstrated that various mammals respond to familiar heterospecific alarm calls, but whether acoustic similarity to a familiar call can prompt a mammal's recognition of an unfamiliar call has yet to be shown. We presented alarm calls to free‐ranging eastern gray squirrels (Sciurus carolinensis) and recorded behavioral changes in vigilance and antipredatory response. Playbacks included alarm calls of a sympatric bird (American robin, Turdus migratorius), an allopatric bird with a call structure similar to that of the robin (common blackbird, Turdus merula), and an allopatric bird with a distinct call structure (New Holland honeyeater, Phylidonyris novaehollandiae). Squirrels responded significantly more frequently to squirrel alarm calls (positive control) than to robin song (negative control) or honeyeater calls. Squirrel response to robin and blackbird alarm calls was statistically similar to their response to squirrel alarm calls, indicating that squirrels responded to those alarm calls as if they provided information about the presence of predators. However, squirrel response to robin song was not statistically different from response to any of the other avian calls, including the robin and blackbird alarms, suggesting that squirrels neither respond to blackbird alarms as if they clearly signify danger, nor as if they clearly do not signify danger, perhaps reflecting some ambiguity in interpretation of the calls. These results suggest that squirrel responses to alarm calls are generally based on call familiarity, but that acoustic similarity of an unfamiliar allopatric call to a familiar call also can elicit antipredator behavior. The lack of response to honeyeater alarm calls also supports the hypothesis that call recognition by gray squirrels is dependent on familiarity, rather than simply detection of an acoustic feature common to alarm calls across a variety of avian species.     

Barking in domestic dogs: context specificity and individual identification

In this study we sought to determine whether dog barks could be divided into subtypes based on context. We recorded barking from 10 adult dogs, Canis familiaris, of six breeds in three different test situations: (1) a disturbance situation in which a stranger rang the doorbell, (2) an isolation situation in which the dog was locked outside or in a room isolated from its owner and (3) a play situation in which either two dogs or a human and a dog played together. We analysed spectrograms of 4672 barks using macros that took 60 sequential frequency measurements and 60 sequential amplitude measurements along the length of the call. Statistical analyses revealed that barks are graded vocalizations that range from harsh, low-frequency, unmodulated calls to harmonically rich, higher-frequency, modulated calls. The harsh, low-frequency, unmodulated barks were more commonly given in the disturbance situation, and the more tonal, higher-pitch, modulated barks were more commonly given in the isolation and play situations. Disturbance barks were also longer in duration with more rapid repetition than the barks given in other contexts. Discriminant analysis revealed that dog barks can be divided into different subtypes based on context even within individual dogs, and that dogs can be identified by their bark spectrograms despite the context of the bark.     

Avoiding predators at night: antipredator strategies in red-tailed sportive lemurs (Lepilemur ruficaudatus)

Although about one-third of all primate species are nocturnal, their antipredator behavior has rarely been studied directly. Crypsis and a solitary lifestyle have traditionally been considered to be the main adaptive antipredator strategies of nocturnal primates. However, a number of recent studies have revealed that nocturnal primates are not as cryptic and solitary as previously suggested. Thus, the antipredator strategies available for diurnal primates that rely on early detection and warning of approaching predators may also be available to nocturnal species. In order to shed additional light on the antipredator strategies of nocturnal primates, I studied pair-living red-tailed sportive lemurs (Lepilemur ruficaudatus) in Western Madagascar. In an experimental field study I exposed adult sportive lemurs that lived in pairs and had offspring to playbacks of vocalizations of their main aerial and terrestrial predators, as well as to their own mobbing calls (barks) given in response to disturbances at their tree holes. I documented the subjects' immediate behavioral responses, including alarm calls, during the first minute following a playback. The sportive lemurs did not give alarm calls in response to predator call playbacks or to playbacks with barks. Other behavioral responses, such as gaze and escape directions, corresponded to the hunting strategies of the two classes of predators, suggesting that the corresponding vocalizations were correctly categorized. In response to barks, they scanned the ground and fled. Because barks do not indicate any specific threats, they are presumably general alarm calls. Thus, sportive lemurs do not rely on early warning of acoustically simulated predators; rather, they show adaptive escape strategies and use general alarm calls that are primarily directed toward the predator but may also serve to warn kin and pair-partners.     

Predation increases acoustic complexity in primate alarm calls

According to most accounts, alarm calling in non-human primates is a biologically hardwired behaviour with signallers having little control over the acoustic structure of their calls. In this study, we compared the alarm calling behaviour of two adjacent populations of Diana monkeys at Taï forest (Ivory Coast) and Tiwai Island (Sierra Leone), which differ significantly in predation pressure. At Taï, monkeys regularly interact with two major predators, crowned eagles and leopards, while at Tiwai, monkeys are only hunted by crowned eagles. We monitored the alarm call responses of adult male Diana monkeys to acoustic predator models. We found no site-specific differences in the types of calls given to eagles, leopards and general disturbances, but there were consistent differences in how callers assembled calls into sequences. At Tiwai, males responded to leopards and general disturbances in the same way, while at Taï, males discriminated by giving call sequences that differed in the number of component calls. Responses to eagles were identical at both sites. We concluded that Diana monkeys are predisposed to use their repertoire in context-specific ways, but that ontogenetic experience determines how individual calls are assembled into meaningful sequences.     

Alarm Calling and Implications for Risk Perception in a Desert Baboon Population

Patterns of alarm calling and their implications for perceived predation risk were explored among adult baboons Papio cynocephalus ursinus in four social groups differing in both size and composition (22–55 members with one to six adult males) in a desert population. Data were collected in a field experiment where alarm calls were elicited from baboons under similar conditions of risk in response to the approach of a potential predator, a human observer. The results show that females call more frequently than males in most groups. In addition, the median calling rate of females shows an exponential increase in smaller groups. These patterns suggest that females in small groups may perceive the highest risk in this population. Nevertheless, there was no clear tendency for either sex to be the first to call. The observer approaches were also used to evaluate the influence of group size on the ease of detection of 1. the baboons by the observer; and 2. the observer by the baboons. Group size did not appear to affect detection distances for either subject, although the probability that baboons were more likely to perform alarm calls before the observer had detected them increased in smaller groups.     

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.     

The information that receivers extract from alarm calls in suricates.

Field observations and acoustic analyses have shown that suricate (Suricata suricatta) alarm calls vary in their acoustic structure depending on predator type. In this study, we tested whether receivers respond appropriately when hearing a call in the absence of a predator. Although the only way for suricates to escape from predators is to retreat to boltholes, responses to playbacks could be divided into distinct categories. The subjects responded differently to alarm calls given in response to aerial or terrestrial predators and to recruitment calls emitted in response to snakes and deposits on the ground. Suricates also showed rather distinct responses to low, medium and high urgency aerial calls. Differences in the responses were less obvious for different levels of urgency in the terrestrial and recruitment calls. Suricate receivers thus gain information about both the predator type and level of urgency from the acoustic structures of their calls.     

No evidence of eavesdropping on heterospecific alarm calls by captive zebra finches recently descended from wild birds

Alarm calls are vocalisations animals give in response to predators which mainly function to alert conspecifics of danger. Studies show that numerous species eavesdrop on heterospecific calls to gain information about predator presence. Responding to heterospecific calls may be a learned or innate response, determined by whether the response occurs with or without prior exposure to the call. In this study, we investigated the presence of eavesdropping behaviour in zebra finches Taeniopygia guttata. This species is not known to possess a distinct alarm call to warn adult conspecifics of a threat, and could be relying on alarm calls of nearby heterospecifics for predator information. We used a playback experiment to expose captive zebra finches to three heterospecific sounds: an unfamiliar alarm call (from the chestnut‐rumped thornbill Acanthiza uropygialis), a familiar alarm call, and a familiar control (both from the noisy miner Manorina melanocephala). These calls were chosen to test if the birds had learnt to distinguish between the function of the two familiar calls, and if the acoustic properties of the unfamiliar alarm indicated presence of a threat to the finches. Our results showed that in response to the thornbill alarm, the birds reduced the rate of production of short calls. However, this decrease was also seen when considering both short and distance calls in response to the control sound. An increase in latency to call was also seen after the control stimulus when compared to the miner alarm. The time spent scanning increased in response to all three stimuli, but this did not differ between stimuli. There were no significant differences when considering the stimulus by time interaction for any of the three vigilance measures. Overall, no strong evidence was found to indicate that the captive zebra finches were responding to the heterospecific alarm stimuli with anti‐predator behaviour.     

Alarm call discrimination in a social rodent: adult but not juvenile degu calls induce high vigilance

Many social animals develop vocal communications to send and receive information efficiently in a group. In alarm communication, call recipients in a social group evaluate alarm calls, enhancing their probability of survival in the face of predatory threats. Calls from naïve and younger group members might be less evocative, in terms of rendering group members vigilant, than calls from more experienced adults because adults are generally more reliable. It remains uncertain, however, what acoustic characteristics render an alarm call reliable. Here, we report that adult degus, Octodon degus (Rodentia, Octodontidae), produced an alarm with a frequency-modulated (FM) syllable, accompanied by low bandwidth and entropy, to evoke a high-vigilance response amongst receivers. Unlike adults, subadult degus did not emit the FM syllable in the warning context, and their call without the FM syllable evoked less vigilance than the adult alarm. We suggest that the FM structure of the adult-produced syllable serves as the primary feature characterizing a reliable alarm call. Our results are consistent with those found in other social rodents, e.g., ground squirrels and gerbils, also produce FM alarm calls in high-urgency situations supports the importance of the FM syllable in alarm communication.     

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.     

Situational Specificity in Alpine-marmot Alarm Communication

We studied the degree to which alpine marmot (Marmota marmota L.) alarm calls function as communication about specific external stimuli. Alpine marmots emit variable alarm calls when they encounter humans, dogs, and several species of aerial predators. The first part of the study involved observations and manipulations designed to document contextual variation in alarm calls. Alarm calls varied along several acoustic parameters, but only along one that we examined, the number of notes per call, was significantly correlated with the type of external stimulus. Marmots were more likely to emit single-note alarm calls as their first or only call in response to an aerial stimulus, and multiple-note alarm calls when first calling to a terrestrial stimulus. This relationship was not without exceptions; there was considerable variation in the number of notes they emitted to both aerial and terrestrial stimuli, and a single stimulus type — humans — elicited a wide range of acoustic responses. The second part of the study involved playing back three types of alarm calls to marmots and observing their responses. Marmots did not have overtly different responses to the three types of played-back alarm calls. Our results are consistent with the hypotheses that: 1. Alarm calls do not refer to specific external stimuli; 2. Alarm calls function to communicate the degree of risk a caller experiences; and 3. Alarm calls require additional contextual cues to be properly interpreted by conspecifics.     

Dual Function of Chip Calls Depending on Changing Call Rate Related to Risk Level in Territorial Pairs of White‐Eared Ground‐Sparrows

Different mechanisms have been proposed for encoding information into vocalizations: variation of frequency or temporal characteristics, variation in the rate of vocalization production, and use of different vocalization types. We analyze the effect of rate variation on the dual function of chip calls (contact and alarm) produced by White‐eared Ground‐sparrows (Melozone leucotis). We conducted an acoustic playback experiment where we played back 1 min of four chip call rates (12, 36, 60, 84 calls/min). We measured the response of territorial pairs using behavioral responses, and fine structural features of calls produced in response to those playbacks. White‐eared Ground‐sparrows showed more intense behavioral responses to higher than lower call rate playbacks. Both individuals of the pair approached the source of the playback stimulus faster, produced the first vocalization faster, produced more vocalizations, and spent more time close to the stimulus in higher call rate than in lower call rate playbacks. Frequency and duration characteristics of calls (chip and tseet) were similar in response to all call rate playbacks. Our playback experiment elicited different intensity of behavioral responses, suggesting that risk‐based information is encoded in call rate. Our results suggest that variation in the rate of chip call production serves a dual function in this species; calls are used at lower rates for pair contact and at higher rates for alarm/mobbing signals.     

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.