Localization of Passerine Seeet and Mobbing Calls by Goshawks and Pygmy Owls

Goshawks and pygmy owls responded to recordings of passerine alarm calls by correctly orienting to their source. The seeet, or “aerial predator” alarm call which is generally assumed to be “non-localizable”, while it elicited fewer responses than did mobbing calls, was nevertheless accurately localized by all birds that did respond. The evolution of alarm calls is discussed in terms of efficient prey communication, following Darwin's “antithesis principle”, rather than predator selection for non-localizability.     

Western Burrowing Owls (Athene cunicularia hypugaea) Eavesdrop on Alarm Calls of Black‐Tailed Prairie Dogs (Cynomys ludovicianus)

Animals sharing a common habitat can indirectly receive information about their environment by observing information exchanges between other animals, a process known as eavesdropping. Animals that use an auditory alarm calling system are an important indirect information source for eavesdropping individuals in their environments. We investigated whether Western burrowing owls (Athene cunicularia hypugaea) nesting on black‐tailed prairie dog (Cynomys ludovicianus) colonies responded to broadcasts of prairie dog alarm calls. Western burrowing owls are closely associated with black‐tailed prairie dogs in Colorado and neighboring states on the Great Plains of the United States. Prairie dog burrows in active colonies can serve as nesting sites for Western burrowing owls, and prairie dogs may act as an alternative prey source for predators, potentially decreasing the burrowing owls' risk of predation through the dilution effect. Burrowing owls nesting on prairie dog colonies may also eavesdrop on prairie dog alarm calls, enhancing their survival and nesting success on prairie dog colonies. We performed broadcast experiments with three different sounds: a prairie dog alarm call, a biological control (cattle mooing), and a non‐biological control (an airplane engine), and characterized burrowing owl responses as either alert or relaxed. For each sound stimulus, we recorded the time to first alert response to broadcast sounds (latency) and also how frequently the target burrowing owl exhibited an alert response within the first ten seconds of the broadcast (intensity). Burrowing owls reacted more quickly to the prairie dog alarm than to the biological control. They significantly increased the intensity of alert behaviors in response to broadcasts of the alarm, but did not show an increased reaction to either the biological or the non‐biological control. Our results suggest that burrowing owls nesting on prairie dog colonies eavesdrop on, and increase their alert behaviors in response to, prairie dog alarm calls.     

Premating Behavior in the Subgenus Limia (Pisces: Poeciliidae): Sexual Selection and the Evolution of Courtship

A three-year field-study of Richardson's ground squirrels was conducted to assess whether alarm calling functions to warn close relatives (“kin selection” hypothesis) or manipulate conspecifics (a “selfish” hypothesis). S. richardsonii had distinct calls for terrestrial and aerial predators, and the responses of squirrels varied appropriately according to the context of calls, implying that calling conveyed correct information concerning the nature of the danger. Alarm calling elicited by naturally occurring encounters with potential predators during 454 h of observation, and by a thrown frisbee in 70 experimental trials, was not equally probable for all age/sex classes. Squirrels were most likely to call when they had offspring or siblings nearby, which is supportive of the hypothesis that alarm calling is maintained by kin selection. Adult males, residing in the vicinity of either their probable progeny or their nonlittermate half-siblings, were the most likely age/sex class to call during the lactation period when young were below ground and were most vulnerable. I conclude that alarm calling by Richardson's ground squirrels is nepotistic rather than manipulative.     

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.     

Auditory Perception of Hawks and Owls for Passerine Alarm Calls

The auditory perception of eight species of raptors was examined to test the hypothesis of Marler (1955) that these avian predators are unable to locate certain songbird alarm calls. In particular, Marler proposed that mobbing calls have characteristics that enhance their locatability and that these characteristics are absent in the high-frequency 'seet' calls given by individual songbirds. To test this hypothesis, the behavioral responses of four species of owls and four species of hawks, housed at two different raptor rehabilitation sites, to tape recorded alarm calls were examined. Each raptor was exposed to a random order of 10 trials of mobbing calls and 10 trials of a seet call. Responses were scored based upon head angle orientations. Hawks and owls responded more often and more accurately to mobbing calls than to seet calls. In general, owls responded to significantly more calls than hawks. The results are consistent with Marler's hypothesis that raptors have difficulty locating passerine seet calls. Nevertheless, future studies should test mobbing calls that vary in their frequency and duration ( Ficken & Popp 1996 ) to determine whether some mobbing calls are more difficult to locate than others.     

Context-dependent vocal mimicry in a passerine bird

How do birds select the sounds they mimic, and in what contexts do they use vocal mimicry? Some birds show a preference for mimicking other species' alarm notes, especially in situations when they appear to be alarmed. Yet no study has demonstrated that birds change the call types they mimic with changing contexts. We found that greater racket-tailed drongos (Dicrurus paradiseus) in the rainforest of Sri Lanka mimic the calls of predators and the alarm-associated calls of other species more often than would be expected from the frequency of these sounds in the acoustic environment. Drongos include this alarm-associated mimicry in their own alarm vocalizations, while incorporating other species' songs and contact calls in their own songs. Drongos show an additional level of context specificity by mimicking other species' ground predator-specific call types when mobbing. We suggest that drongos learn other species' calls and their contexts while interacting with these species in mixed flocks. The drongos' behaviour demonstrates that alarm-associated calls can have learned components, and that birds can learn the appropriate usage of calls that encode different types of information.     

Alarm calls modulate the spatial structure of a breeding owl community

Animals should continuously assess the threat of predation. Alarm calls inform on predation risk and are often used as cues to shape behavioural responses in birds and mammals. Hitherto, however, the ecological consequences of alarm calls in terms of organization of animal communities have been neglected. Here, we show experimentally that calls of a resident nocturnal raptor, the little owl Athene noctua, triggered a response in terms of breeding habitat selection and investment in current reproduction in conspecifics and heterospecifics. Little owls preferred to settle in territories where calls of conspecifics, irrespective of their type (i.e. alarm versus contact calls), were broadcasted, indicating that either conspecific attraction exists or calls are interpreted as foreign calls, eliciting settlement as a mode of defence against competitors. Also, we found that little owls seemed to invest more in current reproduction in safe territories as revealed by conspecific calls. Innovatively, we reported that a second owl species, the migratory scops owl Otus scops, preferred to breed in safe territories as indicated by little owls' calls. These results evidence that the emission of alarm calls may have, apart from well-known behavioural effects, ecological consequences in natural communities by inducing species-specific biases in breeding habitat selection. This study demonstrates a previously unsuspected informative role of avian alarm calls which may modulate the spatial structure of species within communities.     

A micro-geography of fear: learning to eavesdrop on alarm calls of neighbouring heterospecifics

Many vertebrates eavesdrop on alarm calls of other species, which is a remarkable ability, given geographical variation in community composition and call diversity within and among species. We used micro-geographical variation in community composition to test whether individuals recognize heterospecific alarm calls by: (i) responding to acoustic features shared among alarm calls; (ii) having innate responses to particular heterospecific calls; or (iii) learning specific alarm calls. We found that superb fairy-wrens (Malurus cyaneus) fled to cover to playback of noisy miner (Manorina melanocephala) aerial predator alarm calls only in locations where miners were present, suggesting that learning rather than acoustic structure determines response. Sites with and without miners were well within the dispersal distance of fairy-wrens, and philopatric males and dispersing females showed the same pattern, so that local genetic adaptation is extremely unlikely. Furthermore, where miners were present, fairy-wrens responded appropriately to different miner calls, implying eavesdropping on their signalling system rather than fleeing from miners themselves. Learned eavesdropping on alarm calls enables individuals to harvest ecologically relevant information from heterospecifics on an astonishingly fine spatial scale. Such phenotypic plasticity is valuable in a changing world, where individuals can be exposed to new species.     

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.     

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.     

Situational Specificity in Alpine-marmot Alarm Communication

We studied the degree to which alpine marmot (Marmota marmota L.) alarm calls function as communication about specific external stimuli. Alpine marmots emit variable alarm calls when they encounter humans, dogs, and several species of aerial predators. The first part of the study involved observations and manipulations designed to document contextual variation in alarm calls. Alarm calls varied along several acoustic parameters, but only along one that we examined, the number of notes per call, was significantly correlated with the type of external stimulus. Marmots were more likely to emit single-note alarm calls as their first or only call in response to an aerial stimulus, and multiple-note alarm calls when first calling to a terrestrial stimulus. This relationship was not without exceptions; there was considerable variation in the number of notes they emitted to both aerial and terrestrial stimuli, and a single stimulus type — humans — elicited a wide range of acoustic responses. The second part of the study involved playing back three types of alarm calls to marmots and observing their responses. Marmots did not have overtly different responses to the three types of played-back alarm calls. Our results are consistent with the hypotheses that: 1. Alarm calls do not refer to specific external stimuli; 2. Alarm calls function to communicate the degree of risk a caller experiences; and 3. Alarm calls require additional contextual cues to be properly interpreted by conspecifics.     

Non‐Redundant Social Information Use in Avian Flocks with Multisensory Stimuli

Animals generally live in multisensory worlds; however, our understanding of multisensory perception is rather limited, despite its relevance for explaining the mechanisms behind social interactions, such as collective detection while foraging in groups. We tested how multisensory stimuli affected the antipredator behavior of dark‐eyed juncos (Junco hyemalis) using alarm calls as an auditory signal and flushing behavior as a visual cue. We varied the degree of risk within the group by manipulating the number of group mates alarm calling and/or flushing using robotic birds. We assumed that alarm calling and flushing were redundant stimuli and predicted that they could generate one of three types of responses (enhancement, equivalence, or antagonism) depending on the mechanism of multisensory perception. We set up an artificial flock with three robotic juncos surrounding a live junco and controlled for multiple confounding factors (e.g., identity of the focal, body mass, food deprivation time). We found that the degree of alarm of live juncos increased when at least one robot flushed. However, the time it took the live individuals to react to the robots' behavior increased, rather than decreased, with at least one alarm call. This could be the result of an orienting response or sensory overload, as live juncos increased scanning behavior after being exposed solely to alarm calls. Contrary to some theoretical assumptions, alarm calling and flushing behavior elicited independent unimodal responses, suggesting that they are non‐redundant stimuli and that together they could reduce the occurrence of false alarms and facilitate flock cohesion.     

Monotony and the Information Content of Richardson's Ground Squirrel (Spermophilus richardsonii) Repeated calls: Tonic Communication or Signal Certainty?

The repetition of elements within an alarm signal is commonly thought to ensure that receivers have detected that signal, or to promote residual vigilance in light of the dangerous circumstances prompting the signal's initial production (tonic communication). Beyond alerting others and maintaining that state of alertness, however, repetitive signal elements may be parsed so as to encode information about the nature of potential threats. To determine how call length and variation in intersyllable latency might prove informative in the repetitive alarm vocalizations of Richardson's ground squirrels (Spermophilus richardsonii), we conducted a field‐based playback experiment quantifying antipredator responses to manipulated alarm calls. Free‐living juvenile squirrels were exposed to playbacks of 12 syllable (long) and six syllable (short) calls with a constant (monotonous) or changing (variable) call rate. The length of calls had no significant effect on the behaviour of call recipients during and immediately after call production; however, call recipients showed greater vigilance after the playback of monotonous calls than after variable calls. The absence of a call length effect is not consistent with tonic communication in the strict sense; rather, enhanced responsiveness to monotonous relative to variable calls suggests that multiple syllables, and the emergent patterns of intersyllable latency, communicate information about response urgency or the distance to a predatory threat. Only monotonous calls convey those aspects with any certainty on the part of the signaller and hence are selectively attended to by receivers.     

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.     

Age Differences in the Responses to Adult and Juvenile Alarm Calls by Bonnet Macaques (Macaca radiata)

This study examined the differential responses to alarm calls from juvenile and adult wild bonnet macaques ( Macaca radiata ) in two parks in southern India. Field studies of several mammalian species have reported that the alarm vocalizations of immature individuals are often treated by perceivers as less provocative than those of adults. This study documents such differences in response using field-recorded playbacks of juvenile and adult alarm vocalizations. To validate the use of playback vocalizations as proxies of natural calls, we compared the responses of bonnet macaques to playbacks of alarm vocalizations with responses engendered by natural alarm vocalizations. We found that the frequency of flight, latency to flee, and the frequency of scanning to vocalization playbacks and natural vocalizations were comparable, thus supporting the use of playbacks to compare the effects of adult and juvenile calls. Our results showed that adult alarm calls were more provocative than juvenile alarm calls, inducing greater frequencies of flight with faster reaction times. Conversely, juvenile alarm calls were more likely to engender scanning by adults, a result interpreted as reflecting the lack of reliability of juvenile calls. Finally, we found age differences in flight behavior to juvenile alarm calls and to playbacks of motorcycle engine sounds, with juveniles and subadults more likely to flee than adults after hearing such sounds. These findings might reflect an increased vulnerability to predators or a lack of experience in young bonnet macaques.     

Acoustic Behaviour of Birds and Mammals in the Predator Context; I. Factors Affecting the Structure of Alarm Signals. II. The Functional Significance and Evolution of Alarm Signals

I. 7 vocalizations emitted in the predator context are defined in terms of their function. The physical and physiological constraints on the evolution of the physical structure of alarm calls with respect to detectability and localizability are discussed. Detection of various calls depends on signal amplitude, environmental attenuation, signal-to-noise ratio, discrimination of the receiver against background noise, and absolute auditory sensitivity of the receiver. The combined effect of these factors is discussed for an exemplary predator-prey system, in which the hearing of both, predator and prey is known. Localizability of an alarm call is determined by its frequency, bandwidth, and possibly its amplitude relative to the auditory threshold of the receiver. Crude differentiation between localizable and non-localizable signals is not possible, and localizability of particular sounds varies between species. In some cases the question of detectability may render the problem of localizability unimportant. Besides detectability and localizability, other factors such as the acoustic background formed by the alarm calls of sympatric species and by the species' own repertoire of calls are discussed. II. Requisite conditions and available evidence for the evolution of alarm calls through individual selection and kin selection are described. Five types of alarm calls are discussed individually:

• 1 The occurrence of mobbing calls indicates that a major function of these calls is predator deterrence (“move on”), although the calls also alert other prey and promote cultural transmission of the predator's characteristics.
• 2 Alarm calls associated with evasive actions of the prey cause the predator to give up the hunt or diminish its hunting success by warning other prey, which only in some cases are closely related to the caller.
• 3 Distress calls of a seized prey either attract other prey which then mob the predator, or attract other predators, which presumably attack the first predator. In both cases the chances to escape are enhanced because the predator's attention is diverted.
• 4 Defence calls are used to threaten a predator. These calls often mimic sounds of other predators.
• 5 Distraction calls may enhance the effect of distraction display.

Although the different functions of various alarm calls are treated individually, certain of the calls may have more than one function and may be employed in nonpredator contexts as well.     

No need to shout: Effect of signal loudness on sibling communication in barn owls Tyto alba

In animal communication, signal loudness is often ignored and seldom measured. We used a playback experiment to examine the role of vocal loudness (i.e., sound pressure level) in sibling to sibling communication of nestling barn owls Tyto alba. In this species, siblings vocally negotiate among each other for priority access to parental food resources. Call rate and call duration play key roles in this vocal communication system, with the most vocal nestlings deterring their siblings from competing for access to the food item next delivered by parents. Here, we broadcast calls at different loudness levels and call rate to live nestlings. The loudness of playback calls did not affect owlets' investment in call rate, call duration or call loudness. The rate at which playback calls were broadcast affected owlets' call rate but did not influence their response in terms of loudness. This suggests that selection for producing loud signals may be weak in this species, as loud calls may attract predators. Moreover, given that owlets do not overlap their calls and that they communicate to nearby siblings in the silence of the night, loud signals may not be necessary to convey reliable information about food need.     

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.     

Bird calls: just emotional displays or something more?

Two widely held assumptions about the sounds of birds and other animals are (1) they are impulsive and involuntary, and cannot be controlled, and (2) they are based only on emotion, apparently because the stimuli eliciting them are thought to be very generalized. The validity of these assumptions has been tested in studies of the alarm calling and food calling behavior of domestic chickens. Videotapes of aerial and ground predators–a hawk overhead and a raccoon on the ground–were effective in eliciting the two major classes of alarm calls. The frequency of aerial alarm calling was strongly affected by presence or absence of a companion, while other aspects of antipredator behavior were unchanged. This so-called "audience effect" on calling is not found with the ground predator call, apparently because this call is addressed to the predator as well as companions. The rules for audience effects are different again with food calling. Evidently calling is not completely impulsive, but can be controlled. By varying the attributes of digitized video images of predators we have shown that stimuli eliciting the aerial predator alarm call are quite specific, encoding different information than the ground predator call. Playback experiments demonstrate that another chicken can decode this information, and react adaptively. Although emotion is undoubtedly involved in bird calling, we conclude that simple emotion-based models of bird calls are inadequate as the sole basis for explaining the vocal behavior of birds.     

Bird calls: just emotional displays or something more?

Two widely held assumptions about the sounds of birds and other animals are (1) they are impulsive and involuntary, and cannot be controlled, and (2) they are based only on emotion, apparently because the stimuli eliciting them are thought to be very generalized. The validity of these assumptions has been tested in studies of the alarm calling and food calling behavior of domestic chickens. Videotapes of aerial and ground predators–a hawk overhead and a raccoon on the ground–were effective in eliciting the two major classes of alarm calls. The frequency of aerial alarm calling was strongly affected by presence or absence of a companion, while other aspects of antipredator behavior were unchanged. This so-called "audience effect" on calling is not found with the ground predator call, apparently because this call is addressed to the predator as well as companions. The rules for audience effects are different again with food calling. Evidently calling is not completely impulsive, but can be controlled. By varying the attributes of digitized video images of predators we have shown that stimuli eliciting the aerial predator alarm call are quite specific, encoding different information than the ground predator call. Playback experiments demonstrate that another chicken can decode this information, and react adaptively. Although emotion is undoubtedly involved in bird calling, we conclude that simple emotion-based models of bird calls are inadequate as the sole basis for explaining the vocal behavior of birds.