Alarm Calls of Marmosets (Callithrix geoffroyi) to Snakes and Perched Raptors

Communication about the presence of predators is an important benefit of group living. Critical information about the nature of danger can be conveyed through referential alarm calls. Raptors pose a significant predatory threat to callitrichid species. Unlike a raptor in flight, a perched raptor cannot attack suddenly at great speed, and it can be monitored from a safe distance. In this sense a perched bird may pose a threat more similar to that of a terrestrial predator such as a snake. Here we compare predatory contexts by addressing these two questions: 1) Do marmosets produce acoustically distinct alarm calls to snake models and perched raptor models? 2) Do the visual responses of the marmosets to the playbacks of perched raptor–elicited calls differ from those given to the playbacks of calls given in response to snakes? We recorded alarm calls from two groups of outdoor-housed Geoffroy’s marmosets (Callithrix geoffroyi) in response to predator models. Later, we played back stimuli created from these recordings to the marmosets and scored their gaze direction. Results show that calls given to models of perched raptors are acoustically distinct from those given to models of snakes. Further, the relative number of upward to downward looks while listening to the playbacks of perched raptor–elicited calls was significantly greater than it was for snake-elicited calls. Reactions to airborne raptors are known to elicit freezing or rapid flight, neither of which occurred in response to our playbacks. Our data suggest a greater complexity in the alarm call repertoire of marmosets than previously demonstrated.     

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 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.     

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.     

Perceptual specificity in the alarm calls of Gunnison's prairie dogs

Gunnison's prairie dogs have a complex alarm communication system. We show that the escape responses of prairie dogs to naturally occurring live predators differed depending upon the species of predator. We also show that playbacks of alarm calls that were elicited originally by the live predators produced the same escape responses as the live predators themselves. The escape responses fell into two qualitatively different categories: running to the burrow and diving inside for hawks and humans, and standing upright outside the burrow for coyotes and dogs. Within these two categories there were differences in response. For hawks, only the prairie dogs that were in the direct flight path of a stooping red-tailed hawk ran to their burrows and dove inside, while for humans and human alarm call playbacks there was a colony-wide running to the burrows and diving inside. For coyotes and coyote alarm call playbacks there was a colony-wide running to the burrows and standing alert at the burrow rims, while for domestic dogs and playbacks of alarm calls for domestic dogs the prairie dogs assumed an alert posture wherever they were feeding, but did not run to their burrows. These responses to both the live predators and to predator-elicited alarm calls suggest that the alarm calls of Gunnison's prairie dogs contain meaningful referential information about the categories of predators that approach a colony of prairie dogs.     

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.     

Playbacks of food-associated calls attract chimpanzees towards known food patches in a captive setting

Food-associated calls have received much research attention due to their potential to refer to discovered food in a word-like manner. Studies have found that in many species, food-associated calls attract receivers to the food patch, suggesting these calls play roles in food sharing, cooperation and competition. Additionally, in various species, these calls play a role that has received much less attention: mediating social interactions among foragers that are already nearby or within the food patch, independently of whether they attract outside foragers. In order to increase understanding of the function of the chimpanzee (Pan troglodytes) food-associated rough grunt, we conducted captive playback studies testing whether rough grunt playbacks attract, repel or have no effect on the proximity of foragers already familiarized with the presence of food. We tested how acoustic playbacks of rough grunts (or control calls) from one of two known, identical feeding sites affected receivers’ approach and feeding behaviors. More often than expected, participants first approached the feeding site from which rough grunts, but not control calls, were broadcast. However, neither condition increased the likelihood that participants fed first from a given site. Our results support the hypothesis that rough grunts elicit an approach response in receivers, while providing no evidence that they repel. In addition, our study provides evidence that receivers may approach rough grunts even if they do not intend to feed. We discuss the information rough grunts may convey to receivers beyond information about discovered food and the potential benefits signalers may gain from this calling behavior.

     

Observational and Experimental Evidence for the Function of Tail Flicking in Eurasian Moorhen Gallinula chloropus

Tail movements such as wagging, flicking or pumping are reported from many bird species but their adaptive functions remain poorly understood. To investigate whether tail flicking functions as an alarm signal, either to predators or neighbouring birds, or as a signal of submission to conspecifics, I observed this behaviour in moorhen in a natural context, and conducted playback experiments using vocalizations of predators, conspecifics and heterospecifics. I found positive relationships between flicking and vigilance and nearest neighbour distance, and negative relationships between flicking and moorhen flock size and total flock size. Moorhen at the edge of a flock flicked at a higher rate. Single moorhen flicked more often compared with individuals in groups, both in single‐ and mixed‐species flocks, and there was a tendency that single moorhen flicked more often than single moorhen within a mixed‐species flock. Moorhen responded differently to conspecific and predator calls. While in both cases vigilance increased, tail flick rate was higher during predator playbacks and lower during conspecific playbacks. Furthermore, moorhen remained rather motionless when conspecific calls were played back, but not during predator calls, and, moorhen resumed to a baseline level of tail flicking more quickly after the playback of conspecific calls. Taken together, the results suggest that flicking may be considered as a honest signal of vigilance directed towards ambushing predators.     

The function of food-associated calls in white-faced capuchin monkeys, Cebus capucinus, from the perspective of the signaller

In many species, call recipients respond to food-associated calls by approaching the signaller. For this reason, most studies of food-associated calls focus on the benefits to a signaller of attracting a particular audience to a food source. Although call recipients respond as if they have been informed about the location of a food source, it is not necessarily the case that the primary function of food-associated calls is to inform others. I combined naturalistic observations and food placement experiments to investigate the environmental and social influences on call production in white-faced capuchin monkeys to assess other possible functions of food-associated calls. Individuals did not call under the circumstances predicted by an information-sharing hypothesis. The quantity of food and the age-sex composition of the audience did not influence call production, but food type did. Individuals produced more food-associated calls when they discovered fruit compared with insects or eggs. Results of observations of social interactions after food discovery indicated another possible function of food-associated calls. Individuals who called when they discovered food were less likely to be approached by others who were in visual contact than individuals who remained silent. Individuals who did not call when they discovered food were more likely to call subsequently if a higher-ranking, as opposed to a lower-ranking, animal approached them. Furthermore, individuals who called when approached by higher-ranking animals were less likely to receive aggression than individuals who did not call. Therefore, food-associated calls may function to announce food ownership, thereby decreasing aggression from other individuals.     

The versatility of graded acoustic measures in classification of predation threats by the tufted titmouse Baeolophus bicolor: exploring a mixed framework for threat communication

Many mammal and bird species respond to predator encounters with alarm vocalizations that generate risk‐appropriate responses in listeners. Two conceptual frameworks are typically applied to the information encoded in alarm calls and to associated anti‐predator behaviors. ‘Functionally referential’ alarm systems encode nominal classes or categories of risk in distinct call types that refer to distinct predation‐risk situations. ‘Risk‐based’ alarms encode graded or ranked threat‐levels by varying the production patterns of the same call types as the urgency of predation threat changes. Recent work suggests that viewing alarm‐response interactions as either referential or risk‐based may oversimplify how animals use information in decision‐making. Specifically, we explore whether graded alarm cues may be useful in classifying risks, supporting a referential decision‐making framework. We presented predator (hawk, owl, cat, snake) and control treatments to captive adult tufted titmice Baeolophus bicolor and recorded their vocalizations, which included ‘chick‐a‐dee’ mobbing calls (composed of chick and D notes), ‘seet’ notes, two types of contact notes (‘chip’, ‘chink’), and song. No single call type was uniquely associated with any treatment and the majority of acoustic measures varied significantly among treatments (46 of 60). The strongest models (ANOVA and classification tree analysis) grouped hawk with cat and owl, and control with snake, and were based on the number or proportion of a) chick and D notes per chick‐a‐dee call, b) chip versus chink notes produced following treatment exposure, and c) the frequency metrics of other note types. We conclude that (1) the predation‐threat information available in complex titmouse alarm calls was largely encoded in graded acoustic measures that were (2) numerous and variable across treatments and (3) could be used singly or in combinations for either ranking or classification of threats. We call attention to the potential use of mixed threat identification strategies, where risk‐based signal information may be used in referential decision‐making contexts.     

Responses to natural and synthetic phee calls by common marmosets (Callithrix jacchus)

Captive adult common marmosets (Callithrix jacchus) produce whistlelike “phee” calls in two contexts: in the home cage, where phee calls may function as part of territorial marking behavior, and when separated from social companions, where phee calls may function to reunite conspecifics. Natural and synthesized calls representing the acoustic structure of male and female calls in each context were presented to adult marmosets in a playback paradigm. Marmosets demonstrated discriminative abilities according to the context of the call and the caller's sex. Vocal and behavioral responses indicated increased vigilance and territorial behavior, following playbacks of naturally produced calls as well as synthetic calls. All animals scanned more frequently following produced calls as well as synthetic calls. All animals scanned more frequently following natural home cage as well as isolation calls, but only increased contact behavior (trills) in response to home cage calls. The responses were dimorphic according to the sex of the caller, where adult males scanned more following male calls, and adult females were more aggressive following male and female calls. The differential behavioral responses to playbacks of marmoset phee calls suggest a biological relevance to subtle differences found in the acoustic parameters of the phee call. © 1994 Wiley-Liss, Inc.

1 This article is a US Government work and, as such, in the public domain in the United States of America.

     

Mobbing calls signal predator category in a kin group-living bird species

Many prey species gather together to approach and harass their predators despite the associated risks. While mobbing, prey usually utter calls and previous experiments have demonstrated that mobbing calls can convey information about risk to conspecifics. However, the risk posed by predators also differs between predator categories. The ability to communicate predator category would be adaptive because it would allow other mobbers to adjust their risk taking. I tested this idea in Siberian jays Perisoreus infaustus, a group-living bird species, by exposing jay groups to mounts of three hawk and three owl species of varying risks. Groups immediately approached to mob the mount and uttered up to 14 different call types. Jays gave more calls when mobbing a more dangerous predator and when in the presence of kin. Five call types were predator-category-specific and jays uttered two hawk-specific and three owl-specific call types. Thus, this is one of the first studies to demonstrate that mobbing calls can simultaneously encode information about both predator category and the risk posed by a predator. Since antipredator calls of Siberian jays are known to specifically aim at reducing the risk to relatives, kin-based sociality could be an important factor in facilitating the evolution of predator-category-specific mobbing 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.     

Acoustic Analysis and Contextual Description of Food-Associated Calls in White-Faced Capuchin Monkeys (Cebus capucinus)

Since early studies of primates that identified vocalizations that attracted others to a food source, the assumed function of food-associated calls has been to inform others of the presence of food. The label food-associated calls and its implied function has led to a focus in research on many species of the costs/benefits for the signaler and recipient of informing others about the presence of food; however, without clearly identifying the calls contextually or acoustically, it is unclear if calls are specific to a feeding context and thus whether calls provide specific information about the presence of food. If calls occur exclusively in the context of feeding, information about individual identity would allow listeners to decide whether or not to approach a calling individual. I conducted acoustic and contextual analyses on food-associated calls in white-faced capuchins. I identified the calls as distinct vocalizations that occur almost exclusively in a feeding context. Discriminant function analyses demonstrate that information about caller sex and identity are encoded in the calls. Therefore, there is the potential for individuals to use acoustic information when responding to food-associated calls; however, playback experiments are necessary to test more explicitly the hypothesis that recipients are able to recognize the calls of specific individuals.     

Individual distinctiveness in the mobbing call of a cooperative bird, the noisy miner Manorina melanocephala

Individual differentiation is usually advantageous in maximising the fitness benefits of interactions with conspecifics. In social species, where intraspecific interactions are frequent, this is likely to be particularly important. Indeed, some form of differentiation underpins most hypotheses proposed to account for cooperative behaviour in birds. The auditory modality is a likely candidate for this function, particularly for species where individuals are widely spaced and in dense vegetation. In this study, we examined the acoustic structure of a distinctive mobbing signal, the 'chur' call, of the cooperatively breeding noisy miner Manorina melanocephala . Using 250  calls from 25 individuals, a combination of spectrographic-based measurement of call parameters, cross-correlation and multi-dimensional scaling was used to test for systematic individual differences in call structure. Strong differences between individuals were observed in all measures, indicating that this call encodes sufficient information to facilitate individual differentiation. We then conducted a series of field playbacks to test the effect of the behaviour on conspecifics. Results demonstrated that the call, in isolation, has a clear attractant effect. Given that chur calls are synonymous with the characteristic cooperative mobbing behaviour of this species, these findings suggest they are likely to have an important function in coordinating complex social behaviour.     

Traffic noise differentially impacts call types in a Japanese treefrog (Buergeria japonica)

Acoustic noise from automobile traffic impedes communication between signaling animals. To overcome the acoustic interference imposed by anthropogenic noise, species across taxa adjust their signaling behavior to increase signal saliency. As most of the spectral energy of anthropogenic noise is concentrated at low acoustic frequencies, species with lower frequency signals are expected to be more affected. Thus, species with low-frequency signals are under stronger pressure to adjust their signaling behaviors to avoid auditory masking than species with higher frequency signals. Similarly, for a species with multiple types of signals that differ in spectral characteristics, different signal types are expected to be differentially masked. We investigate how the different call types of a Japanese stream breeding treefrog (Buergeria japonica) are affected by automobile traffic noise. Male B. japonica produce two call types that differ in their spectral elements, a Type I call with lower dominant frequency and a Type II call with higher dominant frequency. In response to acoustic playbacks of traffic noise, B. japonica reduced the duration of their Type I calls, but not Type II calls. In addition, B. japonica increased the call effort of their Type I calls and decreased the call effort of their Type II calls. This result contrasts with prior studies in other taxa, which suggest that signalers may switch to higher frequency signal types in response to traffic noise. Furthermore, the increase in Type I call effort was only a short-term response to noise, while reduced Type II call effort persisted after the playbacks had ended. Overall, such differential effects on signal types suggest that some social functions will be disrupted more than others. By considering the effects of anthropogenic noise across multiple signal types, these results provide a more in-depth understanding of the behavioral impacts of anthropogenic noise within a species.     

Behavioural response evoked by conspecific distress calls in two neotropical treefrogs

Anurans emit distress calls when attacked by predators as a defensive mechanism. As distress calls may trigger antipredator behaviour even in individuals that are not under attack, we tested whether this defensive behaviour induced behavioural changes in neighbouring conspecifics. We compared the behavioural responses of two species of Neotropical hylid frogs (genus Boana) to conspecific distress calls and white noise. Individuals of both species interrupted their vocal activity and decreased call rate after hearing the distress call. Natural variation on signal intensity calibrated among the nearest neighbours did not influence the response and we did not observe negative phonotaxis after any acoustic stimulus. Despite the fact that many predators are acoustically oriented, we could not determine if such response (reduced call rate) was induced by risk assessment or by the masking effect on advertisement calls. Boana faber responded similarly to white noise and distress calls, while B. bischoffi responded more intensely to distress calls. Duration of silence after playbacks in B. faber was longer than B. bischoffi. We suggest that, if the signals are interpreted as a risk cue by neighbouring conspecifics, each species may be preyed upon by different predators, as they may have led to distinct defensive strategies and different responses to distress calls. If risk assessment information is included in distress calls, it triggers behavioural responses only in the nearest neighbours, as we did not observe responses on the vocal activity of the interspecific chorus. Our results add relevant data about acoustic communication and interpretations by anurans, highlighting the importance of considering cues within common and widespread 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.     

Antiphonal call timing in marmosets is behaviorally significant: interactive playback experiments

Studies of primate vocal communication systems have generally focused on vocalizations and the information they convey to conspecifics. But the vocalizations are not the only sources of information. Aspects of each species vocal behaviors are likely to be communicatively rich as well. During vocal interactions, for example, the latency delay between the calls could communicate an important message to the signal receiver, such as an interest and willingness to socialize. Here we employed novel, interactive playback software to address this issue in the antiphonal calling behavior of common marmosets. In these experiments, we parametrically varied the latency delay of antiphonal call stimuli and measured its effects on subjects’ resultant vocal behavior. Results showed that marmosets produced successively fewer antiphonal call responses during test conditions with increasing latency delays. Moreover, although subjects produced significantly more antiphonal than spontaneous calls in conditions with antiphonal call timing delays up to 9 s, a longer delay resulted in a significant decline in calling. These data suggest that antiphonal call timing is a salient cue for maintaining antiphonal calling interactions and may be used by marmosets to determine whether a subsequent call is produced in response to or independently of their own.     

Variation in and Meaning of Alarm Calls in a Social Desert Rodent Rhombomys opimus

The great gerbil (Rhombomys opimus), a social rodent that lives in family groups, emits three different alarm vocalizations in the presence of predators: a rhythmic call; a faster more intense call; and a single whistle. We tested the hypothesis that the alarm calls communicate risk of predation. We quantified the relationship between predator distance and type of alarm call via human approaches to gerbils. We also tested responses of focal adults in family groups to playback broadcasts of the different calls and controls of bird song and tape noise. Results showed that alarm calls were related to distance from a predator. Gerbils gave the rhythmic call when the predator was farthest away, the more intense call as the predator moved closer; and a short whistle when startled by a close approach of the predator. Gerbils stopped feeding and stood vigilant in a frozen alert posture in response to playbacks of all three alarm calls. They decreased non‐vigilant behavior to the alarm vocalizations more than to the controls and decreased non‐vigilant behavior significantly more in response to the intense alarm and whistle compared with the rhythmic alarm. We conclude that one function of gerbil alarm calls is to communicate response urgency to family members. The rhythmic alarm communicates danger at a distance, whereas the intense alarm and whistle signal the close approach of a predator.