Scared and less noisy: glucocorticoids are associated with alarm call entropy

The nonlinearity and arousal hypothesis predicts that highly aroused mammals will produce nonlinear, noisy vocalizations. We tested this prediction by measuring faecal glucocorticoid metabolites (GCMs) in adult yellow-bellied marmots (Marmota flaviventris), and asking if variation in GCMs was positively correlated with Wiener entropy-a measure of noise. Contrary to our prediction, we found a significant negative relationship: marmots with more faecal GCMs produced calls with less noise than those with lower levels of GCMs. A previous study suggested that glucocorticoids modulate the probability that a marmot will emit a call. This study suggests that, like some other species, calls emitted from highly aroused individuals are less noisy. Glucocorticoids thus play an important, yet underappreciated role, in alarm call production.     

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.     

Golden-marmot Alarm Calls. II. Asymmetrical Production and Perception of Situationally Specific Vocalizations?

Many species produce alarm calls that vary according to situation. An implicit assumption for these species is that production and perception of situationally specific alarm calls is symmetrical: perceivers respond to variation produced by signalers. The companion paper to this one (Blumstein 1995) showed that golden marmots (Marmota caudata aurea) produce variable alarm calls that vary in proportion to the degree of risk the caller perceives. Calls produced in higher-risk situations have fewer notes than calls produced in lower-risk situations. In this study, to determine the salience of the number of notes per call in eliciting different responses in conspecific perceivers, I played back three-note alarm calls, eight-note alarm calls, and the non-alarm vocalization of a local bird to adult golden marmots. Although marmots responded differently to bird calls and alarm calls, vigilance responses to the different alarm calls were similar. Several explanations may account for the apparent insensitivity to alarm-call variation: golden marmots may require additional contextual cues to properly interpret alarm calls, perceptual abilities do not parallel production abilities, or calls may serve a generalized alerting function.     

Eavesdropping on the Neighbourhood: Collared Pika (Ochotona collaris) Responses to Playback Calls of Conspecifics and Heterospecifics

The acoustic environment, composed in part by the vocalizations of sympatric animals, is a major source of information and can be used to fine-tune behavioural decisions. Active assessment of alarm calls within and between mammal species is not fully understood. We explored the behavioural responses of collared pikas to con- and heterospecific vocalizations, in order to determine whether they selectively attend to these calls. Pikas increased their vigilance after playback of alarm calls of heterospecific mammals (marmots and ground squirrels), but responded most strongly to conspecific calls. While responses to playback calls of their own, of neighbours and of a stranger did not differ, pikas did discriminate between individual callers in a habituation-discrimination experiment. The ability to make use of information from different sources in their acoustic environment likely facilitates pikas' behavioural decisions that affect foraging, predator avoidance and nepotism.     

Reliability and the adaptive utility of discrimination among alarm callers

Unlike individually distinctive contact calls, or calls that aid in the recognition of young by their parents, the function or functions of individually distinctive alarm calls is less obvious. We conducted three experiments to study the importance of caller reliability in explaining individual-discriminative abilities in the alarm calls of yellow-bellied marmots (Marmota flaviventris). In our first two experiments, we found that calls from less reliable individuals and calls from individuals calling from a greater simulated distance were more evocative than calls from reliable individuals or nearby callers. These results are consistent with the hypothesis that marmots assess the reliability of callers to help them decide how much time to allocate to independent vigilance. The third experiment demonstrated that the number of callers influenced responsiveness, probably because situations where more than a single caller calls, are those when there is certain to be a predator present. Taken together, the results from all three experiments demonstrate the importance of reliability in explaining individual discrimination abilities in yellow-bellied marmots. Marmots' assessment of reliability acts by influencing the time allocated to individual assessment and thus the time not allocated to other activities.     

Communication of Stimulus Size and Shape in Alarm Calls of Gunnison's Prairie Dogs, Cynomys gunnisoni

Gunnison's prairie dogs ( Cynomys gunnisoni ) emit multiple-note alarm calls to terrestrial predators that vary in acoustic structure according to the eliciting stimulus. The characteristics of the predator that are salient with respect to alarm call variation, however, are poorly understood. Although the behavior of predators has been shown to influence alarm call production in other species of ground-dwelling sciurids, the degree to which sciurid alarm calls describe physical characteristics of predators has not been addressed independently of the effects of variation in predator behavior. The effect of variation in the size and shape of the eliciting stimulus was studied by presenting silhouette models to a colony of prairie dogs and recording the alarm calls that were elicited. Discriminant function analysis on 7 variables measured from spectrograms revealed that the alarm calls differed with respect to silhouette. These results suggest that information with respect to stimulus size and shape is encoded in prairie dog alarm calls.     

Anti‐Predator Behaviour in a Nocturnal Primate,the Grey Mouse Lemur (Microcebus murinus)

Although one‐third of all primates are nocturnal, their anti‐predator behaviour has rarely been studied. Because of their small body size, in combination with their solitary and nocturnal life style, it has been suggested that they mainly rely on crypsis to evade predators. However, recent studies revealed that nocturnal primates are not generally cryptic and that they exhibit predator‐specific escape strategies as well as alarm calls. In order to add to this new body of research, we studied anti‐predator strategies of nocturnal grey mouse lemurs experimentally. In order to elicit anti‐predator behaviour and alarm calls, we conducted experiments with a carnivore‐, snake‐ and raptor model. We also conducted playback experiments with mouse lemur alarm calls to characterize their function. In response to predator models, they exhibited a combination of anti‐predator strategies: in response to carnivore and snake models, mouse lemurs monitored the predator, probably to assess the potential risk that emanates from the predator. In response to raptor models they behaved cryptically and exhibited freezing behaviour. All mouse lemurs, except one individual, did not alarm call in response to predator models. In addition, during playback experiments with alarm calls, recorded during real predator encounters, mouse lemurs did not emit alarm calls nor did they show any escape behaviour. Thus, as in other nocturnal primates/mammals, mouse lemurs do not seem to rely on routinely warning of conspecifics against nearby predators.     

Inter- and Intraspecific Variation in the Acoustic Habitats of Three Marmot Species

Closely related species often have remarkably different vocalizations. Some of the variation in acoustic structure may result from species adapting their calls to maximize transmission through their acoustic environments. We document the relative magnitude of inter- and intraspecific variation in acoustic transmission properties of the habitats of three closely related marmot species to study the relative importance that the acoustic environment may have played in selecting for species-specific marmot alarm calls. We used spectrogram correlation to quantify the degree to which pure tones and alarm calls changed as they were broadcast through marmot home ranges to describe the acoustic habitats of golden (M. candata aurea), yellow-bellied (M. flaviventris), and alpine (M. marmota L.) marmots. Species lived in quantifiably different acoustic habitats. One analysis partitioned variation between species and between marmot social groups (nested within species). We found significant interspecific variation in the acoustic transmission fidelity of the three species' habitats and insignificant intraspecific variation between social groups. Further analysis of a larger sample of alarm calls broadcast through golden marmot social groups found significant intraspecific variation. Interspecific variation greater than intraspecific variation suggests that variable acoustic habitats may be responsible for at least some of the interspecific variation in alarm call structure. This is the first study to use spectrogram correlation to describe habitat acoustics. We discuss aspects of the method that may be useful for others seeking to quantify habitat acoustics.     

Wild chimpanzees inform ignorant group members of danger

The ability to recognize other individuals' mental states-their knowledge and beliefs, for example-is a fundamental part of human cognition and may be unique to our species. Tests of a "theory of mind" in animals have yielded conflicting results. Some nonhuman primates can read others' intentions and know what others see, but they may not understand that, in others, perception can lead to knowledge. Using an alarm-call-based field experiment, we show that chimpanzees were more likely to alarm call in response to a snake in the presence of unaware group members than in the presence of aware group members, suggesting that they recognize knowledge and ignorance in others. We monitored the behavior of 33 individuals to a model viper placed on their projected travel path. Alarm calls were significantly more common if the caller was with group members who had either not seen the snake or had not been present when alarm calls were emitted. Other factors, such as own arousal, perceived risk, or risk to receivers, did not significantly explain the likelihood of calling, although they did affect the call rates. Our results suggest that chimpanzees monitor the information available to other chimpanzees and control vocal production to selectively inform them.     

The evolution of vocal alarm communication in rodents

On encountering a predator, many species emit potentially riskyvocalizations known as alarm calls. We evaluated the relativeimportance of two adaptive hypotheses on the evolution of calling:(1) communicating to predators, which may function by deterringpursuit and hence increasing individual survival, and (2) analternative nepotistic hypothesis for alarm calling wherebycallers obtain direct and indirect fitness by warning relatives.Focusing on 209 species of rodents, we found significant associationsbetween diurnality and alarm calling, living socially and alarmcalling, and diurnality and sociality. Diurnality, however,accounted for nearly three times as much variation in whetheror not a species alarm called than did sociality. Phylogenetictests revealed that the evolution of diurnality preceded theevolution of alarm calling, and that the evolutions of diurnalityand sociality were unrelated. Our results are consistent withthe hypothesis that alarm communication evolved to communicateto predators. If so, then nepotistic benefits, although importantfor the maintenance of alarm calling in some rodents, may berelatively less important in its evolution.     

Male monkeys remember which group members have given alarm calls

Primates give alarm calls in response to the presence of predators. In some species, such as the Thomas langur (Presbytis thomasi), males only emit alarm calls if there is an audience. An unanswered question is whether the audience's behaviour influences how long the male will continue his alarm calling. We tested three hypotheses that might explain the alarm calling duration of male Thomas langurs: the fatigue, group size and group member behaviour hypotheses. Fatigue and group size did not influence male alarm calling duration. We found that males only ceased calling shortly after all individuals in his group had given at least one alarm call. This shows that males keep track of and thus remember which group members have called.     

The effect of body size and habitat on the evolution of alarm vocalizations in rodents

When confronted with a predator, many mammalian species emit vocalizations known as alarm calls. Vocal structure variation results from the interactive effects of different selective pressures and constraints affecting their production, transmission, and detection. Body size is an important morphological constraint influencing the lowest frequencies that an organism can produce. The acoustic environment influences signal degradation; low frequencies should be favoured in dense forests compared to more open habitats (i.e. the ‘acoustic adaptation hypothesis’). Such hypotheses have been mainly examined in birds, whereas the proximate and ultimate factors affecting vocalizations in nonprimate mammals have received less attention. In the present study, we investigated the relationships between the frequency of alarm calls, body mass, and habitat in 65 species of rodents. Although we found the expected negative relationship between call frequency and body mass, we found no significant differences in acoustic characteristics between closed and open‐habitat species. The results of the present study show that the acoustic frequencies of alarm calls can provide reliable information about the size of a sender in this taxonomic group, although they generally do not support the acoustic adaptation hypothesis.     

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.     

Effect of conspecific alarm calls in the parental behaviour of nesting southern house wrens

Alarm calls are usually used to signal the presence of a threat to members of the same species and have been studied broadly in social foraging species. We analysed the effects of conspecific alarm calls on the parental behaviour of a territorial species, the southern house wrens (Troglodytes aedon musculus), during nestling stage. We compared the parental response of adults feeding 9–11-day-old nestlings when faced with conspecific alarm calls and with a control non-sympatric species’ song broadcast from a neighbouring territory. We measured the time required by parents to return to the nest (latency) when exposed to the stimuli and estimated parent’s nest visitation rate and mean visit duration. Parents took longer to resume parental activities when we broadcast a conspecific alarm call, but they did not modify their nest visitation rate or the mean visit duration. Heterospecific songs did not seem to affect parental behaviour. Our results suggest that nesting southern house wrens can use alarm calls uttered from neighbouring territories to assess the presence of a threat and adjust their parental behaviour accordingly.     

The response of adult orang-utans to flanged male long calls: inferences about their function

Flanged male orang-utans emit loud vocalizations called long calls. In this study, we examined the correlates of variation in long-calling rates among flanged male Sumatran orang-utans, as well as the ranging responses of adult females and flanged males to these long calls. Males that gave calls more often were more likely to approach calls by others. Results bolster a female attraction function of long calls. Flanged males did not significantly avoid or approach long calls. However, males called more when alone than when guarding a female mate, and adult females significantly approached long calls, especially those of the dominant male, and did so regardless of their reproductive state, allowing them to remain within earshot of calling males. The possible selective advantages of this response include avoidance of harassment and infanticide by males. These findings confirm the existence of some form of social organization above the mother-infant unit.     

Mule deer (Odocoileus hemionus) respond to yellow‐bellied marmot (Marmota flaviventris) alarm calls

Individuals may obtain valuable information about the presence of predators by listening to heterospecific alarm signals. Most playback studies have demonstrated that similarly sized and taxonomically related species may respond to the calls of each other, but less work has been carried out to define these factors influence responsiveness to alarm signals. In theory, individuals should respond to calls from any species that provide information about the presence of important predators, regardless of body size or taxonomic relationship. However, size is often associated with vulnerability. Coyotes (Canis latrans) in the Rocky Mountains prey upon both mule deer (Odocoileus hemionus) and yellow‐bellied marmots (Marmota flaviventris), which differ considerably in size, alarm vocalizations, and antipredator behavior. We conducted a playback experiment to see whether deer discriminated between marmot alarm calls and the non‐alarm song of a common sympatric bird. We found that deer increased vigilance significantly more after hearing broadcast marmot alarm calls compared with the bird song. Interestingly, deer that were studied within 0.5 km of homes showed significantly greater discrimination than those studied farther from humans. Our results suggest relative size differences do not prevent interspecific communication and that common predators should generally drive the evolution of the ability to learn to respond to meaningful risk cues. As long as two species share a predator, it should benefit the other to respond to its alarm calls.     

Alarm calls elicit predator-specific physiological responses

Glucocorticoids regulate glucose concentrations and responses to unpredictable events, while also modulating cognition. Juvenile Belding''s ground squirrels (Urocitellus beldingi) learn to respond to whistle and trill alarm calls, warning of aerial and terrestrial predators, respectively, shortly after emerging from natal burrows at one month of age. Alarm calls can cause physiological reactions and arousal, and this arousal, coupled with watching adult responses, might help juveniles learn associations between calls and behavioural responses. I studied whether young show differential cortisol responses to alarm and non-alarm calls, using playbacks of U. beldingi whistles, trills, squeals (a conspecific control vocalization) and silent controls. Trills elicited very high cortisol responses, and, using an individual''s response to the silent control as baseline, only their response to a trill was significantly higher than baseline. This cortisol increase would provide glucose for extended vigilance and escape efforts, which is appropriate for evading terrestrial predators which hunt for long periods. Although whistles do not elicit a cortisol response, previous research has shown that they do result in bradycardia, which enhances attention and information processing. This is a novel demonstration of two physiological responses to two alarm calls, each appropriate to the threats represented by the calls.     

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.     

Adaptive differences in response to two types of parental alarm call in altricial nestlings

Vertebrate alarm calls can contain information about the type of predator and the degree of danger, but young animals often respond to alarm calls differently from adults. The distinct behaviour of young may reflect an imperfect stage in the gradual development of the adult response, or a response adapted to specific risks faced by young. In this study, we tested whether nestling white-browed scrubwrens, Sericornis frontalis, responded to different alarm calls according to their specific risks of predation. As predators on the ground pose a danger to scrubwren nestlings, whereas flying predators do not, we predicted that they would respond to ground alarm calls but not to aerial alarm calls. In a field playback experiment, we tested the response of young to aerial and ground alarm calls, each presented in a shorter (less urgent) and longer (more urgent) form. We found that both 5- and 11-day-old nestlings responded to ground alarm calls, and did so more strongly to the more urgent playback. By contrast, the response to aerial alarm calls started to develop only towards the end of the nestling stage. Thus, scrubwren nestlings can distinguish between different types of alarm calls and react more strongly to calls warning of a predator posing greater danger, appropriate to the nestling stage of development. Furthermore, they use the length of ground alarm calls as an indicator of the degree of danger.     

Is Alarm Calling Risky? Marmots Avoid Calling from Risky Places

Alarm calling is common in many species. A prevalent assumption is that calling puts the vocalizing individual at increased risk of predation. If calling is indeed costly, we need special explanations for its evolution and maintenance. In some, but not all species, callers vocalize away from safety and thus may be exposed to an increased risk of predation. However, for species that emit bouts with one or a few calls, it is often difficult to identify the caller and find the precise location where a call was produced. We analyzed the spatial dynamics of yellow-bellied marmot (Marmota flaviventris) alarm calling using an acoustic localization system to determine the location from which calls were emitted. Marmots almost always called from positions close to the safety of their burrows, and, if they produced more than one alarm call, tended to end their calling bouts closer to safety than they started them. These results suggest that for this species, potential increased predation risk from alarm calling is greatly mitigated and indeed calling may have limited predation costs.