From nestling calls to fledgling silence: adaptive timing of change in response to aerial alarm calls

Young birds and mammals are extremely vulnerable to predators and so should benefit from responding to parental alarm calls warning of danger. However, young often respond differently from adults. This difference may reflect: (i) an imperfect stage in the gradual development of adult behaviour or (ii) an adaptation to different vulnerability. Altricial birds provide an excellent model to test for adaptive changes with age in response to alarm calls, because fledglings are vulnerable to a different range of predators than nestlings. For example, a flying hawk is irrelevant to a nestling in a enclosed nest, but is dangerous to that individual once it has left the nest, so we predict that young develop a response to aerial alarm calls to coincide with fledging. Supporting our prediction, recently fledged white-browed scrubwrens, Sericornis frontalis, fell silent immediately after playback of their parents' aerial alarm call, whereas nestlings continued to calling despite hearing the playback. Young scrubwrens are therefore exquisitely adapted to the changing risks faced during development.     

Parental alarm calls suppress nestling vocalization

Evolutionary models suggest that the cost of a signal can ensure its honesty. Empirical studies of nestling begging imply that predator attraction can impose such a cost. However, parents might reduce or abolish this cost by warning young of the presence of danger. We tested, in a controlled field playback experiment, whether alarm calls cause 5-, 8- and 11-day-old nestlings of the white-browed scrubwren, Sericornis frontalis, to suppress vocalization. In this species, nestlings vocalize when parents visit the nest ('begging') and when they are absent ('non-begging'), so we measured effects on both types of vocalization. Playback of parental alarm calls suppressed non-begging vocalization almost completely but only slightly reduced begging calls during a playback of parental feeding calls that followed. The reaction of nestlings was largely independent of age. Our results suggest two reasons why experiments ignoring the role of parents probably overestimate the real cost of nestling vocalizations. Parents can warn young from a distance about the presence of danger and so suppress non-begging vocalizations that might otherwise be overheard, and a parent's presence at the nest presumably indicates when it is safe to beg.     

Effect of alarm calling by male Red‐winged Blackbirds on nestling begging and female provisioning behavior

ABSTRACT Nestling begging and parental provisioning can attract nest predators and reduce reproductive success, so parents and their offspring might be expected to respond adaptively by minimizing predator‐attracting cues when predators threaten nests. Male Red‐winged Blackbirds (Agelaius phoeniceus) are well known for their antipredator alarm calls that contain information about the approach of potential nest predators. We examined the begging behavior of nestlings and the provisioning behavior of females in response to antipredator alarm calls of males to test the adaptive response hypothesis. Playback experiments provided no evidence that alarm calls function to switch off vocal begging; nestlings were equally likely to beg vocally during playback and control periods. Video recordings showed that male alarm calling had no significant effect on inappropriate vocal begging (in the absence of an adult), but significantly reduced the incidence of spontaneous calling (in the absence of begging). Adult females responded to male antipredator alarm calls by delaying their provisioning visits. In addition, although having no significant effect on use of nest‐arriving calls by females, male alarm calling significantly reduced their use of nest‐leaving calls. We conclude that nestling and female Red‐winged Blackbirds respond to male alarm calls in ways that might reduce the risk of predation, but nestlings beg vocally when females arrive to feed them, regardless of male alarm calling, perhaps to avoid a competitive disadvantage with broodmates.     

Begging to differ: scrubwren nestlings beg to alarm calls and vocalize when parents are absent

Nestling birds face a dilemma: they can increase parental provisioning by begging more intensively, but by doing so may also increase their risk of predation. Nestlings could deal with this dilemma by reducing begging intensity after parents have warned them of a nearby predator. We therefore tested experimentally whether nestling scrubwrens, Sericornis frontalis, increase begging intensity with hunger but reduce it after adult alarm calls. Single 5- and 8-day-old nestlings were temporarily taken into the laboratory for playback experiments. Over a 90-min period of food deprivation we simulated parental visits every 10 min by playing back adult feeding calls. Hungrier nestlings begged louder and longer to simulated parental visits, but contrary to expectation did not beg less if they had previously heard playback of alarm calls, and even begged to the alarm calls themselves. The results were similar for both ‘mobbing’ and ‘flee’ alarm calls. Nestlings also gave distinctive calls in the 10-min interval between simulated parental visits, and the number of these calls increased with hunger and after playback of alarm calls. We suggest that nestlings acquire the ability to respond appropriately to alarm calls late in the nestling period and that therefore parents might be selected to avoid alarm calling when defending young nestlings.Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour.      

The information that receivers extract from alarm calls in suricates.

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

Calling at a cost: elevated nestling calling attracts predators to active nests

Begging by nestling birds has been used to test evolutionary models of signalling but theory has outstripped evidence. Eavesdropping predators potentially impose a cost on begging that ensures signal honesty, yet little experimental evidence exists for such a cost at active nests because the use of artificial nests, long playback bouts and absence of parents may have exaggerated costs. We broadcast short periods (1 h) of either nestling vocalizations or background noise at active white-browed scrubwren, Sericornis frontalis, nests. Nestlings called naturally during both treatments, allowing us to test whether elevated calling increases risk, a key but rarely tested assumption of evolutionary models. Predators visited nests exclusively during periods of elevated calling. Furthermore, playbacks affected neither adult visits nor nestling activity, suggesting that calling alone attracted predators. Adults gave alarm calls and nestlings usually called less when predators approached nests. Predation risk to broods is, therefore, likely to fluctuate substantially over short periods of time, depending on nestling hunger and whether adults or young have detected predators. This study confirms a present-day cost of nestling begging, demonstrates that this cost can be incurred over short periods and supports the importance of parent-offspring antipredator strategies in reducing predation risk.     

Crying wolf to a predator: deceptive vocal mimicry by a bird protecting young

Animals often mimic dangerous or toxic species to deter predators; however, mimicry of such species may not always be possible and mimicry of benign species seems unlikely to confer anti-predator benefits. We reveal a system in which a bird mimics the alarm calls of harmless species to fool a predator 40 times its size and protect its offspring against attack. Our experiments revealed that brown thornbills (Acanthiza pusilla) mimic a chorus of other species'' aerial alarm calls, a cue of an Accipiter hawk in flight, when predators attack their nest. The absence of any flying predators in this context implies that these alarms convey deceptive information about the type of danger present. Experiments on the primary nest predators of thornbills, pied currawongs (Strepera graculina), revealed that the predators treat these alarms as if they themselves are threatened by flying hawks, either by scanning the sky for danger or fleeing, confirming a deceptive function. In turn, these distractions delay attack and provide thornbill nestlings with an opportunity to escape. This sophisticated defence strategy exploits the complex web of interactions among multiple species across several trophic levels, and in particular exploits a predator''s ability to eavesdrop on and respond appropriately to heterospecific alarm calls. Our findings demonstrate that prey can fool predators by deceptively mimicking alarm calls of harmless species, suggesting that defensive mimicry could be more widespread because of indirect effects on predators within a web of eavesdropping.     

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.     

Alarm call‐based discrimination between common cuckoo and Eurasian sparrowhawk in a Chinese population of great tits

Morphological resemblance of the common cuckoo Cuculus canorus to the Eurasian sparrowhawk Accipiter nisus has been regarded as an example of predator mimicry. Common hosts could distinguish parasites as the result of coevolution, while rare hosts or non‐hosts may mistake cuckoos for hawks because rare hosts or non‐hosts behave similarly when faced with these two species. Birds usually produce alarm calls in addition to showing behavioral responses when in danger. However, previous studies of identification by rare hosts or non‐hosts of sparrowhawks usually lacked experimental evidence of alarm calls. Great tits Parus major, a rare cuckoo host, perform similar behaviors and usually produce alarm calls in response to sparrowhawks and common cuckoos. Here, we tested whether great tits could distinguish common cuckoo from sparrowhawk based on analysis of their alarm calls and the effects of playback of alarm calls on conspecific behavior. Previous studies showed that great tits have a complex communication system that conveys information about predators, and they could perform different kinds of response behavior to different alarm calls. If great tits have not made the ability to distinguish between common cuckoo and sparrowhawk, then their acoustic responses to these two species and their response behaviors in playback experiments should be similar. Specimens of a common cuckoo (parasite), a sparrowhawk (predator) and an Oriental turtle dove Streptopelia orientalis (harmless control) were used to elicit and subsequently record the response behavior and alarm calls of great tits. There was no significant difference in behavioral response among great tits when exposed to the dummy of cuckoo, sparrowhawk and dove. In contrast, they differed significantly in alarm calls. Great tits produced more notes per call that contained increasing D‐type and decreasing I‐type notes when responding to sparrowhawk as compared to cuckoo or dove. In playback experiments, we found that great tits responded more strongly to great tit hawk than to great tit cuckoo or great tit dove alarm calls. Our study suggests that great tits are able to distinguish sparrowhawks from common cuckoos and convey relevant information in alarm calls by adjusting the number and combinations of notes of a single call type.     

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.     

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.     

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.     

Interspecies semantic communication in two forest primates

West African Diana monkeys (Cercopithecus diana) and Campbell's monkeys (Cercopithecus campbelli) frequently form mixed-species associations. Males of both species produce acoustically distinct alarm calls to crowned eagles (Stephanoaetus coronalus) and leopards (Panthera pardus), two of their main predators. Field playback experiments were conducted to investigate whether Diana monkeys respond to Campbell's alarm calls and whether they understand the calls' semantic content. Diana monkeys responded to playback of Campbell's leopard or eagle alarm calls as though the original predator were present. In a second experiment, Diana monkeys were primed with either Campbell's eagle or leopard alarm calls and then subsequently probed with the vocalizations of a crowned eagle or a leopard. Results showed that monkeys used the semantic information conveyed by the Campbell's alarm calls to predict the presence of a predator. The data are consistent with the hypothesis that non-human primates are able to use acoustic signals of diverse origin as labels for underlying mental representations.     

Experimental study of alarm calls of the oriental tit (Parus minor) toward different predators and reactions they induce in nestlings

Anti-predatory strategies of birds are diverse and may include predator-specific alarm calls. For example, oriental tit (Parus minor) parents can distinguish snakes from other predators and produce snake-specific referential vocalizations ("jar" call) when a snake poses a threat to their nest. The “jar” call has a very specific function to induce fledging of nestlings close to fledging age. This reaction ensures nestlings' survival in natural encounters with snakes that are capable of entering nest cavities and kill entire broods. Sciurid rodents, like chipmunks, may pose a similar threat to cavity-nesting birds. We explored the hypothesis that parents use the fledging-inducing alarm vocalizations in this situation, because chipmunks, like snakes, can kill the brood upon entering the nest cavity. We compared alarm calls of parents toward two predators (chipmunk and snake) who pose a similar threat to the nestlings in a nest cavity, and toward an avian predator (Eurasian jay) who cannot enter nest cavities and poses no threat to the nestlings in a nest. Our results show that the vocal responses of oriental tits were different among the three predators. This suggests that the acoustic properties of vocal responses to predators are different between predators of a similar hunting strategy (nest-cavity entering). The playback of recorded vocal responses of parents to chipmunks did not trigger the fledging of old nestlings, whereas the vocalizations toward a snake did, as shown by earlier studies. Our study suggests that the vocal response of parents does not carry information about the ability of predators to enter the nest cavity and confirms the special status of alarm calls triggered by snakes.     

Vocal development in vervet monkeys

Observations and playback experiments were used to study the development of grunts and alarm calls among free-ranging vervet monkeys. Results indicate that the production of vocalizations, their use in appropriate circumstances, and the response to the vocalizations of others emerge gradually during an individual's first 4 years. Particularly in the case of grunts, different acoustic components develop at different rates. Immatures respond appropriately to the calls of others before they produce appropriate vocalizations themselves. Finally, immature vocal development may be aided by cues received from adults. If an infant gives an alarm call to a genuine predator (as opposed to a non-predator), adults respond more strongly. When infants hear a playback of an alarm, they are more likely to respond appropriately if they first look at an adult.     

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.     

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.     

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

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

Learning fine-tunes a specific response of nestlings to the parental alarm calls of their own species

Parent birds often give alarm calls when a predator approaches their nest. However, it is not clear whether these alarms function to warn nestlings, nor is it known whether nestling responses are species-specific. The parental alarms of reed warblers, Acrocephalus scirpaceus ("churr"), dunnocks, Prunella modularis ("tseep"), and robins, Erithacus rubecula ("seee") are very different. Playback experiments revealed that nestlings of all three species ceased begging only in response to conspecific alarm calls. These differences between species in response are not simply a product of differences in raising environment, because when newly hatched dunnocks and robins were cross-fostered to nests of the other two species, they did not develop a response to their foster species' alarms. Instead, they still responded specifically to their own species' alarms. However, their response was less strong than that of nestlings raised normally by their own species. We suggest that, as in song development, a neural template enables nestlings to recognize features of their own species' signals from a background of irrelevant sounds, but learning then fine-tunes the response to reduce recognition errors.     

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.