Call Variation in Tufted Titmice (Baeolophus bicolor) in a Distress Context: Potential Sex Differences

Tufted titmice, Baeolophus bicolor, produce calls in the contexts related to threat and approach of, and capture by, a predator. In titmice, these calls transition from the chick‐a‐dee call, used in a wide range of social contexts, to ‘distress’ calls that are produced by birds when captured and held by a predator or human observer. A recent study indicated that titmice modify the note composition of their calls in the presence of such threatening stimuli. Here, we tested whether female and male titmice differed in their calling behavior, as relatively few sex differences have been documented in calls shared by female and male songbirds. Individual titmice were captured in walk‐in treadle traps, and we gradually increased the level of fear or arousal by approaching and finally capturing the bird in the hand. Male titmice produced more chick‐a‐dee calls than females as the level of threat increased, up to the point of capturing the bird in the hand. Furthermore, the note composition of calls produced by males differed from that of calls produced by females. A limitation to our study is that our method did not allow us to rule out the possibility that size or dominance differences, rather than sex, were the main reason for the differences in calling we detected. However, increased size generally was not associated with increased calling. We discuss some possible explanations for variation in distress calling behavior in titmice.     

Distress Calls of a Fast-Flying Bat (Molossus molossus) Provoke Inspection Flights but Not Cooperative Mobbing

Many birds and mammals produce distress calls when captured. Bats often approach speakers playing conspecific distress calls, which has led to the hypothesis that bat distress calls promote cooperative mobbing. An alternative explanation is that approaching bats are selfishly assessing predation risk. Previous playback studies on bat distress calls involved species with highly maneuverable flight, capable of making close passes and tight circles around speakers, which can look like mobbing. We broadcast distress calls recorded from the velvety free-tailed bat, Molossus molossus, a fast-flying aerial-hawker with relatively poor maneuverability. Based on their flight behavior, we predicted that, in response to distress call playbacks, M. molossus would make individual passing inspection flights but would not approach in groups or approach within a meter of the distress call source. By recording responses via ultrasonic recording and infrared video, we found that M. molossus, and to a lesser extent Saccopteryx bilineata, made more flight passes during distress call playbacks compared to noise. However, only the more maneuverable S. bilineata made close approaches to the speaker, and we found no evidence of mobbing in groups. Instead, our findings are consistent with the hypothesis that single bats approached distress calls simply to investigate the situation. These results suggest that approaches by bats to distress calls should not suffice as clear evidence for mobbing.     

Mobbing calls signal predator category in a kin group-living bird species

Many prey species gather together to approach and harass their predators despite the associated risks. While mobbing, prey usually utter calls and previous experiments have demonstrated that mobbing calls can convey information about risk to conspecifics. However, the risk posed by predators also differs between predator categories. The ability to communicate predator category would be adaptive because it would allow other mobbers to adjust their risk taking. I tested this idea in Siberian jays Perisoreus infaustus, a group-living bird species, by exposing jay groups to mounts of three hawk and three owl species of varying risks. Groups immediately approached to mob the mount and uttered up to 14 different call types. Jays gave more calls when mobbing a more dangerous predator and when in the presence of kin. Five call types were predator-category-specific and jays uttered two hawk-specific and three owl-specific call types. Thus, this is one of the first studies to demonstrate that mobbing calls can simultaneously encode information about both predator category and the risk posed by a predator. Since antipredator calls of Siberian jays are known to specifically aim at reducing the risk to relatives, kin-based sociality could be an important factor in facilitating the evolution of predator-category-specific mobbing calls.     

Sexual Selection and the Psychophysics of Female Choice

Woodland birds of 20 species were captured in mist-nets in winter (September to February) and summer (April—August) and scored for whether or not they made distress calls while being handled. Birds of only two species showed significant tendencies to be consistent in calling or failing to call when recaptured, but most species had weak trends in. the same direction. Some species changed seasonally in the tendency to call, but there was no general pattern. In winter, but not summer, the incidence of calling was correlated across species with an index of the number of conspecifics likely to hear the call, but there was no comparable correlation with variations within species. In the long-tailed tit, calling was associated with struggling, and with eyelid colour, which reflects a bird's mood. This implies that calling may be directed at a captor as well as at flock companions.     

Responses of young black skimmers to high-intensity distress notes

The semi-precocial young of the black skimmer (Rynchops niger) rely on cryptic behaviour to avoid detection by predators. After capture most individuals emit loud distress calls, and chicks crouched nearby often run just seconds after these calls begin. Experimental distress calls significantly increase the likelihood of running, regardless of whether a sibling or non-sibling call is used. Since chicks in close proximity are usually siblings, such distress notes could evolve through kin selection, even if disadvantageous to the caller. On the other hand, such calls may startle and distract a predator, providing the captive with an opportunity to escape.     

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.     

Functional traits determine heterospecific use of risk‐related social information in forest birds of tropical South‐East Asia

In birds and mammals, mobbing calls constitute an important form of social information that can attract numerous sympatric species to localized mobbing aggregations. While such a response is thought to reduce the future predation risk for responding species, there is surprisingly little empirical evidence to support this hypothesis. One way to test the link between predation risk reduction and mobbing attraction involves testing the relationship between species’ attraction to mobbing calls and the functional traits that define their vulnerability to predation risk. Two important traits known to influence prey vulnerability include relative prey‐to‐predator body size ratio and the overlap in space use between predator and prey; in combination, these measures strongly influence prey accessibility, and therefore their vulnerability, to predators. Here, we combine community surveys with behavioral experiments of a diverse bird assemblage in the lowland rainforest of Sumatra to test whether the functional traits of body mass (representing body size) and foraging height (representing space use) can predict species’ attraction to heterospecific mobbing calls. At four forest sites along a gradient of forest degradation, we characterized the resident bird communities using point count and mist‐netting surveys, and determined the species groups attracted to standardized playbacks of mobbing calls produced by five resident bird species of roughly similar body size and foraging height. We found that (1) a large, diverse subcommunity of bird species was attracted to the mobbing calls and (2) responding species (especially the most vigorous respondents) tended to be (a) small (b) mid‐storey foragers (c) with similar trait values as the species producing the mobbing calls. Our findings from the relatively lesser known bird assemblages of tropical Asia add to the growing evidence for the ubiquity of heterospecific information networks in animal communities, and provide empirical support for the long‐standing hypothesis that predation risk reduction is a major benefit of mobbing information networks.     

Long-lasting mobbing of the pied flycatcher increases the risk of nest predation

Mobbing behavior may provide real benefits because mobbing preyindividuals often cause a predator to leave the vicinity. However,mobbing calls of prey can attract acoustically oriented predatorsthus increasing nest predation. Therefore, a real value of mobbingas a type of adaptive behavior may depend on its duration. Inthis experimental study, we tested whether mobbing durationby the pied flycatcher Ficedula hypoleuca, a small hole-nestingpasserine, increases the risk of nest predation. From the topof one nest-box within each of 78 experimental plots, we playedback long calls of pied flycatchers, whereas recordings of shortmobbing calls were played back from the top of another nearbynest-box. The nest-boxes were arranged in pairs, and each ofthem contained a quail Coturnix coturnix egg. Long-call nest-boxeswere depredated by martens Martes martes significantly moreoften than short-call nest-boxes. This predator usually huntsby night and may eavesdrop on the calls of their mobbing preywhile resting nearby during the day. The results of the presentstudy show that long-lasting conspicuous mobbing calls may carrya significant cost for the breeding birds.     

Behavioral responses to conspecific mobbing calls are predator‐specific in great tits (Parus major)

When facing a predator, animals need to perform an appropriate antipredator behavior such as escaping or mobbing to prevent predation. Many bird species exhibit distinct mobbing behaviors and vocalizations once a predator has been detected. In some species, mobbing calls transmit information about predator type, size, and threat, which can be assessed by conspecifics. We recently found that great tits (Parus major) produce longer D calls with more elements and longer intervals between elements when confronted with a sparrowhawk, a high‐threat predator, in comparison to calls produced in front of a less‐threatening tawny owl. In the present study, we conducted a playback experiment to investigate if these differences in mobbing calls elicit different behavioral responses in adult great tits. We found tits to have a longer latency time and to keep a greater distance to the speaker when sparrowhawk mobbing calls were broadcast. This suggests that tits are capable of decoding information about predator threat in conspecific mobbing calls. We further found a tendency for males to approach faster and closer than females, which indicates that males are willing to take higher risks in a mobbing context than females.     

Predator‐Associated Vocalizations in North American Red Squirrels (Tamiasciurus hudsonicus): To Whom are Alarm Calls Addressed and How do They Function?

Alarm vocalizations produced by prey species encountering predators can serve a variety of functions. North American red squirrels are a small-bodied mammal popularly known for producing loud, conspicuous alarm calls, but functional accounts of calling in this species are few and contradictory. We conducted research over a 3-yr period on a sample of 47 marked red squirrels in the foothills of the Canadian Rockies. We recorded the production of alarm calls during encounters with natural predators and in a series of simulated predator experiments. We tested for variation in call production patterns consistent with three traditional hypotheses concerning the conspecific warning functions of alarm calling: namely that they serve as warnings to kin, to potential mates, or to territorial neighbors with which callers have an established relationship. Patterns of calling did not provide clear support for any of these hypothesized functions. We consider several possible qualifications to our results. We also consider the possibility that conspicuous calls given by red squirrels during encounters with predators are directed at the predators themselves and function to announce their detection and possibly deter them. This possibility is consistent with additional life-history features of red squirrels including that they are a relatively solitary and territorial, food-hoarding species that produces the same conspicuous vocalizations in response to other squirrels intruding on their territory to steal cones. An important corollary of this account is that red squirrel alarm calls probably do not entail referentially specific messages about different types of predator, as proposed previously.     

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.     

Response of Captive Raptors to Avian Mobbing Calls: the Roles of Mobber Size and Raptor Experience

The ‘move on’ hypothesis for avian mobbing proposes that mobbing induces stress in potential predators, thereby provoking them into moving elsewhere. We tested whether mobbing is stress inducing by subjecting captive owls, hawks, and falcons to the mobbing calls of four species of co‐occurring passerine birds that vary considerably in body size. Test subjects comprised 15 individuals of seven species of birds of prey that were housed at a wildlife rehabilitation center in northwestern Pennsylvania, USA. Playback treatments included mobbing calls of the black‐capped chickadee (Poecile atricapillus), blue‐headed vireo (Vireo solitarius), blue jay (Cyanocitta cristata), and American crow (Corvus brachyrhynchos), which vary in size from 12 g (chickadee) to 500 g (crow). A non‐mobbing vocalization (song of the black‐capped chickadee) was included in the playback treatments as a control. Playback treatment produced pronounced effects on three behavioral indicators of probable stress: head orientation toward the playback speaker, raising of feathers or spreading of wings, and changing of perch positions. Test subjects responded more vigorously to mobbing calls of the large passerines (jays and crows) than to those of the smaller passerines (chickadees and vireos). In addition, raptors that had entered the rehabilitation facility as adults generally responded more vigorously to the mobbing calls of jays and crows than did naive individuals that had entered the facility as fledglings or young juveniles. Our results are therefore consistent with the ‘move on’ hypothesis and suggest (1) that the mobbing calls of large passerines are more effective in provoking stress and altering the behavior of potential predators than are the mobbing calls of small passerines and (2) that a raptor's previous experience with mobbing in the wild can exaggerate the strength of its response, particularly to the mobbing calls of large passerines.     

Interspecific responses to distress calls in bats (Chiroptera: Vespertilionidae): a function for convergence in call design?

Distress calls were recorded from three sympatric species of pipistrelle bat (Pipistrellus nathusii, P. pipistrellus and P. pygmaeus) in England and Northern Ireland. At foraging sites, we conducted playback experiments, consisting of experimental distress call sequences from each species and control sequences of random noise and sound recorded with no bats present. We measured response by simultaneously recording ultrasound during playbacks and counting the echolocation pulses above a predetermined threshold which were then identified to species. All three species responded to each other's calls. The number of recorded echolocation pulses of all species increased eight-fold, on average, during the playback of distress call sequences compared with the playback of ultrasonic noise, and four-fold compared with the playback of silence. In a separate playback experiment, the number of echolocation pulses of P. pygmaeus increased 14-fold during the playback of distress calls of four endemic species of bat from Madagascar (Emballonura atrata, Myotis goudoti, Miniopterus majori and M. manavi) compared with the playback of silence. This increased response might have been caused by the high calling rates of the Malagasy species. Distress calls of P. nathusii, P. pipistrellus and P. pygmaeus were structurally convergent, consisting of a series of downward-sweeping, frequency-modulated elements of short duration and high intensity with a relatively strong harmonic content. Selection may favour convergence in the structure of distress calls among bat species, if attracting heterospecifics increases the chance of repelling predators by mobbing.     

Cost of mobbing call to breeding pied flycatcher, Ficedula hypoleuca

Mobbing signals advertise the location of a stalking predatorto all prey in an area and recruit them into the inspectionaggregation. Such behavior usually causes the predator to moveto another area. However, mobbing calls could be eavesdroppedby other predators. Because the predation cost of mobbing callsis poorly known, we investigated whether the vocalizations ofthe mobbing pied flycatcher, Ficedula hypoleuca, a small holenesting passerine, increase the risk of nest predation. We usedmobbing calls of pied flycatchers to examine if they could lurepredators such as the marten, Martes martes. This predator usuallyhunts by night and may locate its mobbing prey while restingnearby during the day. Within each of 56 experimental plots,from the top of one nest-box we played back mobbing sounds ofpied flycatchers, whereas blank tapes were played from the topof another nest-box. The trials with mobbing calls were carriedout before sunset. We put pieces of recently abandoned nestsof pied flycatchers and a quail, Coturnix coturnix, egg intoeach of the nest-boxes. Nest-boxes with playbacks of mobbingcalls were depredated by martens significantly more than werenest-boxes with blank tapes. The results of the present studyindicate that repeated conspicuous mobbing calls may carry asignificant cost for birds during the breeding season.     

Cooperatively breeding Arabian babblers call differently when mobbing in different predator-induced situations

Cooperatively breeding Arabian babblers (Turdoides squamiceps) havea repertoire of different calls that they use in predator-induced contexts.We investigated their vocal mobbing behavior in two different predator-inducedsituations. We presented territorial groups of babblers a perched,stuffed owl representing an avian predator and a cat representinga ground predator. Babblers approached in both situations andmobbed the predators with the same two call types. In both predator-inducedsituations their first call was a short, metallic-sounding "tzwick."In response to the cat, babblers continued to primarily usetzwicks. However, in continued response to the owl, the babblersprimarily used long trills. The experiments indicate that differencesin use of two common call types during mobbing provide informationon differences in predator-induced situations, although no calltype per se identified a specific situation. The experiments suggestthat the short tzwicks indicate a higher risk or urgency thantrills and that combinations of both call types may providegraded information about differences in predator-induced situations.The relatively stable groups of these cooperative breeders mighthave favored evolution for using different calls in differentmobbing situations.     

The evolution of vocal alarm communication in rodents

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

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.     

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.     

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.