Age Differences in the Response of California Ground Squirrels (Spermophilus beecheyi) to Conspecific Alarm Calls

Juvenile California ground squirrel responses to adult alarm calls and juvenile alarm calling may be modified during development to achieve adult form. Adult conspecific chatter and whistle alarm calls were played back to juvenile and adult ground squirrels at an agricultural field site. In response to chatter playbacks, adults spent more time visually orienting to the environment and less time out of view and in covered habitats than juveniles; the converse was true in response to whistle playbacks. To test the evocativeness of juvenile calling, a subset of adult subjects received juvenile chatter and whistle playbacks. Adults spent less time out of view to juvenile call types than to adult calls, and showed more similar responses to juvenile chatters and whistles than to adult chatters and whistles. Age differences in the ground squirrel's alarm call system may reflect adjustments to changing risks during development.     

Age Differences in the Response of Willow Tits (Parus montanus) to Conspecific Alarm Calls

Predation is an important mortality factor in wintering birds. To counter this, birds produce alarm calls in the presence of predators which serve to warn conspecifics. In social hierarchical bird flocks, adults survive the winter better than juveniles and therefore survival strategies probably vary with social status. This study examined the differential responses to alarm calls by free-living willow tits, Parus montanus, in dominance-structured winter flocks in Finland. To explore the age-dependent differences in response to conspecific alarm calls, a series with three alarm calls was played to focal adults and juveniles while they sat in the middle section of a spruce branch. Immediately after the playback, juvenile willow tits moved more often, flew longer distances and changed branches more often than did adults. Previous mammal studies have shown that juveniles are more likely to flee than adults after hearing conspecific alarm calls. The current study demonstrates that similar age-dependent responses to conspecific alarm calls occur in birds also. These findings reflect an increased vulnerability to predators or lack of experience of young birds.     

Ontogeny of conspecific and heterospecific alarm call recognition in wild Verreaux's sifakas (Propithecus verreauxi verreauxi)

The production of vocalizations in nonhuman primates is predominantly innate, whereas learning influences the usage and comprehension of vocalizations. In this study, I examined the development of alarm call recognition in free-ranging infant Verreaux's sifakas. Specifically, I investigated their ability to recognize conspecific alarm calls as well as those of sympatric redfronted lemurs (Eulemur fulvus rufus) in Kirindy forest, western Madagascar. Both species have functionally referential alarm calls for aerial predators and give general alarm calls for both aerial and general predators and also other kinds of threats, such as intergroup encounters with conspecifics. I conducted playback experiments with members of two birth cohorts (nine and ten individuals) to determine the age at which infant Verreaux's sifakas discriminate between conspecific alarm calls, heterospecific alarm calls, and non-alarm vocalizations (parrot song). Most 3-4 months old infants fled toward adults after hearing any playback stimuli, whereas 4-5-month-old infants did so only after presentation of alarm calls. Moreover, all infants of these age classes showed a longer latency to flee after the parrot song indicating their emerging ability to discriminate between alarm calls and non-alarm stimuli. At an age of about 6 months, infants switched from fleeing toward adults to performing adult-like escape responses after presentation of conspecific and heterospecific alarm calls. Thus, the ability to discriminate between alarm from non-alarm stimuli precedes the appearance of adult-like responses. The transition to adult-like escape behavior was coincident with the physical independence of infants from their mothers.     

Threat-Related Acoustical Differences in Alarm Calls by Wild Bonnet Macaques (Macaca radiata) Elicited by Python and Leopard Models

Wild and urban bonnet macaques (Macaca radiata) were studied in southern India to record alarm calls during presentations of realistic models of spotted and dark leopards (Panthera pardus) and an Indian python (Python molurus). Recordings of alarm calls were made from members of four forest troops at feeding stations who observed brief and prolonged presentations of fully exposed spotted and dark leopard morphs and partially concealed views of the spotted morph. Four different forest troops were presented a slowly moving python near feeding stations. Two predator‐inexperienced urban troops from the city of Bangalore were presented either the spotted leopard morph briefly or the python. Analyses of alarm calls revealed differences in acoustic structure, such as a lower harmonic to noise ratio, which can be interpreted as reflecting the level of perceived threat rather than predator type. Noisy alarm calls likely indicate high states of physiological arousal that might provide eavesdropping troop members with information useful for assessing the urgency of the predatory threat. Lack of alarm‐call distinctiveness characterizing predator type is complemented by explicit contextual information in which alarm calling to leopards never occurred on the ground whereas nearly all initial python‐elicited alarm calls were made by individuals on the ground monitoring the python. The alarm calls of Bangalore monkeys distinguished the leopard and python models, with the latter engendering the noisiest calls and immediate flight to trees. Such flight is unnecessary with the python and suggests that, without appropriate experience with pythons, bonnet macaques adopt less predator specific refuge‐seeking behavior.     

Red Squirrels (Sciurus vulgaris) Respond to Alarm Calls of Eurasian Jays (Garrulus glandarius)

Recognition of heterospecific (interspecific) alarm calls has been demonstrated in birds and mammals, but bird–mammal interactions have rarely been studied. Here, I tested the hypothesis that red squirrels (Sciurus vulgaris) are able to recognize alarm calls of a sympatric bird species, the Eurasian jay (Garrulus glandarius), and respond adequately with anti‐predator behaviour. Both animals are preyed upon by the same predators. To test whether squirrels would react to heterospecific alarm calls, I recorded squirrels behaviour during playbacks of jay alarm calls, control playbacks (territorial songs of sympatric songbirds) and during silence. Differences between the control treatment (songbirds) and silence were not significant. Seven of the 13 squirrels responded with escape after broadcasting alarm calls of jays. Further, squirrels spent less time in the patch, expressed a higher vigilance, and showed more rapid head and body movements. These results suggest that squirrels recognize heterospecific alarm vocalizations of jays and discriminate them from equally loud non‐threatening sounds.     

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.     

Wild fledgling tits do not mob in response to conspecific or heterospecific mobbing calls

Mobbing, where birds harass a predator through a combination of vocalizations and stereotyped behaviours, is an effective anti-predator behaviour for many species. Mobbing may be particularly important for juveniles, as these individuals are often more vulnerable than adults. Although the component behaviours of mobbing are often considered to be un-learned, there are few confirmatory data, and the developmental trajectory of mobbing is unknown. In this study, we tested whether conspecific or heterospecific mobbing calls initiated mobbing behaviour in juvenile Blue Tits Cyanistes caeruleus. We located wild adult and recently fledged juvenile Blue Tits and presented them with playback recordings of adult conspecific (Blue Tit) and heterospecific (Great Tit Parus major) mobbing alarm calls. Although adult birds readily mob in response to these types of playbacks, juveniles did not exhibit characteristic mobbing behaviour. Some juveniles did, however, exhibit individual components of mobbing behaviour found in mobbing, despite not producing adult-like mobbing behaviour in response to either conspecific or heterospecific playback. These results suggest that, although birds might be capable of mobbing as juveniles, the associations between the non-vocal stereotyped mobbing behaviours and mobbing calls may be learned.     

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.     

A mutual understanding? Interspecific responses by birds to each other's aerial alarm calls

Individuals are likely to benefit from responding to the alarmsignals of other species with similar predators, and mutualinterspecific responses to aerial (hawk) alarms are thoughtto be common in birds, in part because similarity in alarm callstructure among species might facilitate detection or interpretation.However, there has been no test of whether interspecific responsesto aerial alarm calls can involve mutual responses between speciesand only incomplete tests of the response of any species tosuch heterospecific alarms. We describe the aerial alarm callsof white-browed scrubwrens (Sericornis frontalis) and superbfairy-wrens (Malurus cyaneus) and use a playback experimentto test for mutual responses to each other's aerial alarm calls.The 2 species occur in similar habitats and can co-occur inmixed-species flocks during the nonbreeding season. The aerialalarm calls of both species are high pitched (7 kHz) and rapidlyfrequency-modulated calls but are distinct in frequency measuresand only the scrubwren's call had 2 parallel sounds. Both speciesfled to cover after playback of either their own or the otherspecies' alarm calls but never to control sounds. The responseto either species' alarm was almost invariant in both speciesin an experiment at high natural amplitude, but there was aslightly lower response to heterospecific compared with conspecificalarms when playbacks were at the mean natural amplitude. Ourresults demonstrate, after at least 50 years of interest inthe subject, that there can be mutual responses to aerial alarmcalls between species.     

Plasticity of Alarm-call Response Development in Belding's Ground Squirrels (Spermophilus beldingi, Sciuridae)

Plasticity in the alarm-call responses of Belding's ground squirrels ( Spermophilus beldingi ) may function to prepare young to respond appropriately to calls according to the predator environment and habitat in which the young develop. To examine the extent to which antipredator responses are sensitive to early rearing environments, we studied the development of behavioural responses to playbacks of alarm calls and non-alarm calls in free-living juveniles and captive juveniles housed in large outdoor enclosures. Compared with same-aged, free-living juveniles, captive juveniles were more likely to show an observable response to playbacks, exhibited more exaggerated initial responses (e.g. enter a burrow vs. freeze), and remained alert longer following playbacks. The influence of rearing history on antipredator responses was limited to responses to auditory stimuli, as the two groups of juveniles reacted similarly to fast-moving visual stimuli. The responses of free-living juveniles appeared to be more discriminating than responses of captive juveniles, particularly following playbacks of calls associated with less immediate threats.
The responses of captive and free-living mothers were similar, indicating a developmental component to the juvenile response differences observed here. Free-living juveniles developed a discrimination among alarm and non-alarm calls sooner than captive young. Response differences were evident within 1 wk of first emergence from natal burrows and persisted at least 4 wk, at around the age of natal dispersal. This suggests that early rearing history has an enduring effect on response repertoires, which may be adaptive if animals continue to inhabit the predator environment in which they developed.     

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.     

Behavioral responses to species-specific warning calls in infant squirrel monkeys reared in social isolation

Six infant squirrel monkeys were reared in social isolation. They responded differentially to playbacks of two species-specific alarm calls. The reaction to the alarm peep, the warning call to bird predators, was a prompt flight to the mother surrogate and essentially resembled the respective behavior of mother-reared infants. The responses to yapping, the alarm call to terrestrial predators, were less clear-cut and habituated soon. However, when yapping was played back in connection with the presentation of a reference object, both subjects tested in this way clearly avoided the object and preferred contact with the mother surrogate while they thoroughly explored an object presented with a control tone. From this it can be concluded that the perception of both alarm calls is innate. In addition, the method of behavior-contingent playback of vocalizations simulates the learning process by which the visual perception of terrestrial predators of the habitat is acquired.     

Adult Richardson's Ground Squirrels (Spermophilus richardsonii) Ignore Rate Changes in Juvenile Alarm Calls: Age‐Differential Response Urgency Perception?

Juvenile Richardson's ground squirrels (RGS; Spermophilus richardsonii) communicate response urgency by modulating the rate of syllable production in repetitive alarm calls, although longer call bouts do not promote more pronounced or longer‐lasting (tonic) vigilance in juvenile call recipients. We exposed free‐living adult RGS to playbacks of alarm calls differing in rate and length to determine whether adult receivers respond to the same alarm parameters as juveniles. Adult squirrels did not respond differentially to differences in call rate or length, suggesting that adult RGS do not attend to call rate as do juveniles. This difference in response may be attributable to a developmental change in the perceptual mechanisms by which individuals extract information regarding response urgency, but could also be a product of adult receivers devaluing information encoded in alarm calls emitted by relatively inexperienced juvenile signalers.     

The More the Scarier: Adult Richardson's Ground Squirrels (Spermophilus richardsonii) Assess Response Urgency Via the Number of Alarm Signallers

Richardson’s ground squirrels (RGS) produce alarm calls that warn conspecifics of potential predators. We presented free‐living adult and juvenile RGS with playbacks of repetitive alarm calls from one vs. two juvenile callers broadcast sequentially through two spatially separated loudspeakers. Adult RGS spent a greater proportion of time vigilant in response to two vs. one calling squirrel, whereas juvenile RGS did not respond differentially to two vs. one caller. Apparently then, the relative inexperience of juvenile RGS with alarm calls and the context in which such calls are emitted precludes their enumeration of alarm callers. Taken together with our earlier finding that adult but not juvenile RGS ignore information regarding response urgency encoded in the rate of juvenile produced repetitive calls, our present results suggest a developmental shift in response‐urgency perception. Adult RGS selectively extract information regarding response urgency via discrimination of the number of callers, ignoring less reliable information encoded in the rate of repetitive calls issued by inexperienced juvenile signallers.     

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.     

Bee Threat Elicits Alarm Call in African Elephants

Unlike the smaller and more vulnerable mammals, African elephants have relatively few predators that threaten their survival. The sound of disturbed African honeybees Apis meliffera scutellata causes African elephants Loxodonta africana to retreat and produce warning vocalizations that lead other elephants to join the flight. In our first experiment, audio playbacks of bee sounds induced elephants to retreat and elicited more head-shaking and dusting, reactive behaviors that may prevent bee stings, compared to white noise control playbacks. Most importantly, elephants produced distinctive “rumble” vocalizations in response to bee sounds. These rumbles exhibited an upward shift in the second formant location, which implies active vocal tract modulation, compared to rumbles made in response to white noise playbacks. In a second experiment, audio playbacks of these rumbles produced in response to bees elicited increased headshaking, and further and faster retreat behavior in other elephants, compared to control rumble playbacks with lower second formant frequencies. These responses to the bee rumble stimuli occurred in the absence of any bees or bee sounds. This suggests that these elephant rumbles may function as referential signals, in which a formant frequency shift alerts nearby elephants about an external threat, in this case, the threat of bees.     

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.     

Alarm responses are maintained during captive rearing in chicks of endangered kaki

The maintenance of species-specific behavioural repertoires and traditions is an important but often implicit goal of conservation efforts. When captive rearing is used as a conservation practice, it becomes critical to address its possible implications for the social and behavioural traits of developing individuals. In particular, animals must retain or acquire many of their behavioural abilities to increase the likelihood of survival upon release into the wild. This study investigated the behavioural development of critically endangered kaki (black stilt: Himantopus novaezelandiae ) chicks reared without live adult conspecifics. The captive rearing programme included playbacks of adult kaki alarm calls during cleaning and handling of precocial chicks housed as groups. We used videotaped observations and playback experiments to address the following questions: do kaki chicks respond differentially to (1) familiar versus unfamiliar adult kaki alarm calls and (2) conspecific alarm versus heterospecific control vocalizations. Adult-naïve kaki chicks exhibited a varied behavioural repertoire over their early development. In multivariate analyses, when age was statistically controlled, chicks showed responses to familiar and unfamiliar alarm calls that were similar in magnitude. In contrast, following conspecific alarm calls chicks had longer average latencies to resume pre-playback activities than following heterospecific vocalizations. Although the generality of these conclusions is limited by experimental constraints stemming from working with an endangered species, the findings suggest that current management techniques produce captive-reared kaki for release into the wild that possess many of the behavioural and auditory recognition skills that are required for survival.     

Perception of Vocal Tract Resonances by Whooping Cranes Grus americana

Although formants (vocal tract resonances) can often be observed in avian vocalizations, and several bird species have been shown to perceive formants in human speech sounds, no studies have examined formant perception in birds' own species-specific calls. We used playbacks of computer-synthesized crane calls in a modified habituation—dishabituation paradigm to test for formant perception in whooping cranes ( Grus americana ). After habituating birds to recordings of natural contact calls, we played a synthesized replica of one of the habituating stimuli as a control to ensure that the synthesizer worked adequately; birds dishabituated in only one of 13 cases. Then, we played the same call with its formant frequencies shifted. The birds dishabituated to the formant-shifted calls in 10 out of 12 playbacks. These data suggest that cranes perceive and attend to changes in formant frequencies in their own species-specific vocalizations, and are consistent with the hypothesis that formants can provide acoustic cues to individuality and body size.     

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.