Interspecific Responses of Ringtailed Lemurs to Playback of Antipredator Alarm Calls Given by Verreaux's Sifakas

The ringtailed lemur, Lemur catta, and Verreaux's sifaka, Propithecus verreauxi verreauxi, are diurnal prosimians living sympatrically in Madagascar. Species-specific alarm calls emitted by each of these two species in response to aerial and terrestrial predators differ acoustically. Behavioural responses of ringtailed lemurs evoked by playbacks of conspecific alarm calls differ when the vocalizations were produced in response to aerial predators as opposed to terrestrial predators. We conducted playback experiments on two populations of ringtailed lemurs, using two types of sifaka alarm calls. One population consisted of free-ranging groups which lived sympatrically with sifakas, the other was a colony group which had no contact with sifakas. The results illustrate that the former group of lemurs can perceive what type of predators the sifaka calls refer to, whereas the latter group was not able to recognize the difference in the calls.     

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.     

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.     

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.     

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.     

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.     

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.     

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.     

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.     

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.     

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.     

Neural correlates of threat perception: neural equivalence of conspecific and heterospecific mobbing calls is learned

Songbird auditory areas (i.e., CMM and NCM) are preferentially activated to playback of conspecific vocalizations relative to heterospecific and arbitrary noise. Here, we asked if the neural response to auditory stimulation is not simply preferential for conspecific vocalizations but also for the information conveyed by the vocalization. Black-capped chickadees use their chick-a-dee mobbing call to recruit conspecifics and other avian species to mob perched predators. Mobbing calls produced in response to smaller, higher-threat predators contain more "D" notes compared to those produced in response to larger, lower-threat predators and thus convey the degree of threat of predators. We specifically asked whether the neural response varies with the degree of threat conveyed by the mobbing calls of chickadees and whether the neural response is the same for actual predator calls that correspond to the degree of threat of the chickadee mobbing calls. Our results demonstrate that, as degree of threat increases in conspecific chickadee mobbing calls, there is a corresponding increase in immediate early gene (IEG) expression in telencephalic auditory areas. We also demonstrate that as the degree of threat increases for the heterospecific predator, there is a corresponding increase in IEG expression in the auditory areas. Furthermore, there was no significant difference in the amount IEG expression between conspecific mobbing calls or heterospecific predator calls that were the same degree of threat. In a second experiment, using hand-reared chickadees without predator experience, we found more IEG expression in response to mobbing calls than corresponding predator calls, indicating that degree of threat is learned. Our results demonstrate that degree of threat corresponds to neural activity in the auditory areas and that threat can be conveyed by different species signals and that these signals must be learned.     

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.     

Ravens adjust their antipredatory responses to con‐ and hetero‐specific alarms to the perceived threat

Heterospecific alarm calls are typically found in situations where multiple species have a common predator. In birds, they are particularly common in mixed mixed‐species flocks. In species with highly developed social and cognitive abilities like corvids, there is the potential for differential responses to heterospecific vs. conspecific calls according to the riskiness of the habitat. We tested the responses of free‐ranging ravens (Corvus corax) to conspecific alarm calls and compared them to heterospecific alarm calls of jackdaws (Corvus monedula). We observed the proportion of ravens leaving the feeding site after the con‐ or hetero‐specific playback was presented in a situation of low threat (wild boar—Sus scrofa enclosure) and high threat of predation (wolf—Canis lupus enclosure). We show that ravens responded to conspecific calls more intensively at the wolves than at the wild boar, but the response to conspecific calls was in both enclosures stronger than to the control (great tit—Parus major song). The response to the heterospecific alarm was also stronger in the wolves’ enclosure, but it did not differ from control in the wild boar enclosure. These findings suggest that ravens are aware of the meaning of the jackdaw alarm calls, but they respond to it only in a situation of high predatory threat (wolves are present). In the wild boar enclosure, the ravens probably consider jackdaws warning against some other predator, very probably harmless to ravens. This interpretation requires further testing, as both enclosures differ also in respect to other parameters like food quality and shelter availability.     

Singing in the Face of Danger: the Anomalous Type II Vocalization of the Splendid Fairy-Wren

Males of certain species of fairy-wrens (Aves: Maluridae) emit a unique vocalization, the Type II vocalization, in response to the calls of potential predators. We conducted field observations and playback experiments to identify the contexts in which the Type II vocalization is emitted by splendid fairy-wren ( Malurus splendens ) males, and to examine social and genetic factors that influence its occurrence. In field observations and controlled playback experiments, Type II vocalizations were elicited most consistently by calls of the predatory gray butcherbird ( Cracticus torquatus ). Some vocalizations from other avian species also elicited Type II vocalizations, and the majority of these were vocalizations from avian predators. Splendid fairy-wrens are cooperative breeders, and males that responded with Type II vocalizations to playbacks of butcherbird calls tended to be primary rather than secondary males, had larger cloacal protuberances, and were older than those that did not respond. In addition, secondary males that were sons of resident females were more likely than non-sons to respond with a Type II vocalization. In another playback experiment, females responded similarly to the Type I song and Type II vocalizations of their mates. Although the Type II vocalization is emitted primarily in response to predator calls, it is inconsistent with an alarm call explanation. Patterns of reproductive success among Type II calling males suggest that it does not function as an honest signal of male quality. At present, the function of the vocalization remains anomalous, but indirect fitness benefits may play a role in its explanation.     

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.     

Differential Response to Interspecific and Intraspecific Signals Amongst Chickadees

Black‐capped chickadees (Poecile atricapillus) and mountain chickadees (P. gambeli) have a similar vocal repertoire and share many other life history traits; yet, black‐capped chickadees are socially dominant to mountain chickadees where populations overlap. Previous research suggested that in contact zones, both species respond weakly to heterospecific songs during the breeding season, and have suggested minimal interspecific competition. However, both black‐capped and mountain chickadees discriminate between conspecific and heterospecific chick‐a‐dee calls, suggesting attention is paid to interspecific signals. We compared the responses of both black‐capped and mountain chickadees to conspecific and heterospecific chick‐a‐dee calls during the winter, when both species compete for the same food resources. We conducted an aviary playback experiment exposing both species to playback composed of heterospecific and conspecific chick‐a‐dee calls, which had been recorded in the context of finding food sources. Responses from the tested birds were measured by recording vocalizations and behaviour. Black‐capped chickadees responded significantly more to conspecific than to heterospecific stimuli, whereas the subordinate mountain chickadees responded to both mountain and black‐capped chickadee calls. Based upon the reactions to playbacks, our results suggest these two closely related species may differ in their perception of the relative threat associated with intra‐ versus interspecific competitors.     

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.     

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.     

Eavesdropping of an African ground squirrel on the heterospecific alarm calls of a noisy ground-nesting bird

Animals gather information about their environment from a variety of sources to enable adaptive decision-making behaviour. Eavesdropping on heterospecific alarm calls enhances predator avoidance, reduces time spent vigilant and allows for more time on daily activities such as foraging. If the information is relevant and reliable, individuals that respond to heterospecific signals may benefit from a wider range of information at a low marginal cost. The Cape ground squirrel (Xerus inauris) and crowned lapwing (Vanellus chilensis) are ground-dwelling species that are taxonomically distant but share similar predators, habitat and anti-predatory behaviours. We used playback experiments of the alarm calls produced by conspecifics and lapwings to investigate the vigilance responses of adult female Cape ground squirrels. Squirrels responded with greater vigilance to both squirrel and lapwing alarm calls, and no changes of vigilance levels were observed in response to a control sound. However, contrary to our predictions, changes in vigilance and time to relax did not differ between conspecific versus heterospecific playbacks. The results from our study suggest that squirrels perceive lapwing alarm calls as relevant and reliable information and that responding to it could increase their survival.