Mobbing Calls Research Articles

Visual cues of predation risk outweigh acoustic cues: a field experiment in black-capped chickadees.

Foragers rely on various cues to assess predation risk. Information theory predicts that high certainty cues should be valued more than low certainty cues. We measured the latency of black-capped chickadees (Poecile atricapillus) to resume feeding during winter in response to cues that conferred different degrees of certainty about current predation risk: a high certainty visual cue (predator mount) and a lower certainty acoustic cue (conspecific mobbing calls), presented either alone or in combination. As predicted, chickadees took longer to resume feeding after the visual than the acoustic cue, and this effect was greatest under conditions of high starvation risk (i.e. low temperatures). Presenting both cues together produced the same foraging delay as the visual cue alone under low starvation risk, but surprisingly, resulted in lower responses under high starvation risk compared to the visual cue alone. We suggest that this may be due to prey using a form of information updating, whereby differences in the timing of perception of acoustic versus visual cues interacts with energetic constraint to shape perceived risk. Although the sequential perception of cues is likely in a range of decision-making contexts, studies manipulating the order in which cues are perceived are needed to test existing models of multimodal cue integration.

The effect of mobbing vocalizations on risk perception in common mynas (Acridotheres tristis)

Animals emit predator-elicited calls in response to potential predation threats. These vocalizations induce a variety of anti-predator behaviors in conspecific receivers ranging from moving away from predators (alarm calls) to rallying conspecifics to fend them off (mobbing calls). While much is known about the immediate response to alarm calls, less is known about how mobbing calls influence subsequent antipredator decisions. Mobbing calls stimulate harassment of a potential predator. Therefore we predicted that hearing a mobbing call would make animals less likely to immediately flee an approaching threat. To study the potential effect of mobbing vocalizations on risk assessment, we primed common mynas (Acridotheres tristis) with a series of different stimuli and studied the variation in their subsequent decisions to flee an approaching human by quantifying flight initiation distance (FID). We found that although mynas increased their rate of locomotion after hearing mobbing calls, their subsequent decision to flee was not influenced. We also found that an individual’s propensity to move and look explained some variation in FID. This suggests that while mobbing calls do not influence subsequent decisions to flee, they do affect subsequent behavior.

A comparison of sex, morphology, physiology and behavior of black-capped chickadees trapped using two common capture methods.

Many biological studies require the capture of individuals for sampling, for example for measurement of morphological or physiological traits, or for marking individuals for later observations. Capture methods employed often vary both within and between studies, and these differing methods could be more or less effective in capture of different individuals based on their morphology or behavior. If individuals that are prone to capture by the selected method differ with respect to traits of interest, such sampling bias could generate misleading or simply inaccurate results. The selection of capture methods could introduce two different forms of sampling bias, with the individuals that are sampled differing from the population at large or with individuals sampled via one method differing from individuals that could be sampled using a different method. We investigated this latter form of sampling bias by comparing individual birds sampled using two common capture techniques. We caught free-ranging black-capped chickadees (Poecile atricapillus) using walk-in traps baited with seed and mist nets paired with playback of an audio stimulus (conspecific mobbing calls). We measured 18 traits that we expect might vary among birds that are trappable by these differing methods—one that targets birds that are food motivated and potentially less neophobic and another that targets birds that respond readily to a perceived predation risk. We found no differences in the sex, morphology, initial and stress-induced corticosterone concentrations, behavioral response to a novel object, or behavioral response to a predator between individuals captured by these two methods. Individual variation in the behavioral response to a novel object was greater among birds caught by mist nets, suggesting this method might provide a sample that better reflects population-level individual variation. We do not know if the birds caught by these two methods provide a representative sample of the population at large, but can conclude that selection of either of these two common capture methods can similarly sample mean trait values of a population of interest. To accurately assess individual variation, particularly in behavior, mist nets might be preferable.

Nuthatches vary their alarm calls based upon the source of the eavesdropped signals

Animal alarm calls can contain detailed information about a predator’s threat, and heterospecific eavesdropping on these signals creates vast communication networks. While eavesdropping is common, this indirect public information is often less reliable than direct predator observations. Red-breasted nuthatches (Sitta canadensis) eavesdrop on chickadee mobbing calls and vary their behaviour depending on the threat encoded in those calls. Whether nuthatches propagate this indirect information in their own calls remains unknown. Here we test whether nuthatches propagate direct (high and low threat raptor vocalizations) or indirect (high and low threat chickadee mobbing calls) information about predators differently. When receiving direct information, nuthatches vary their mobbing calls to reflect the predator’s threat. However, when nuthatches obtain indirect information, they produce calls with intermediate acoustic features, suggesting a more generic alarm signal. This suggests nuthatches are sensitive to the source and reliability of information and selectively propagate information in their own mobbing calls.

Great tits encode contextual information in their food and mobbing calls.

The calling behaviour of Paridae species (i.e. titmice, tits and chickadees) in a predator-related context is well-studied. Parid species are known to alter call types, note composition or call duration according to predation risk. However, how these species encode information about a non-threatening context, such as food sources, has been subject to only few studies. Studies in Carolina chickadees (Poecile carolinensis) have shown that this species alters the ratio of C and D notes to encode information about the presence of food and/or the flight behaviour of the signaller. This suggests that parids also use graded signals to encode information about non-predatory contexts. No study to date has directly compared the calls of a feeding context with those of a predation (i.e. mobbing) context. Hence, the aim of this study was to compare the calling behaviour of these two situations in great tits (Parus major). Calls uttered at a feeder were recorded, analysed and compared with calls uttered in front of taxidermy mounts of sparrowhawks (Accipiter nisus). In the food context, great tits reduced the number of D notes and increased the number of B, C and E notes compared with the mobbing context. Furthermore, tits produced calls with longer D notes and shorter intervals between D notes than in the mobbing context. This indicates that great tits use two mechanisms of graded signals (i.e. note type and acoustic structure of D calls) to inform conspecifics about the nature of a situation.

The Effect of Pine Forest Structure on Bird-Mobbing Behavior: From Individual Response to Community Composition

Pine-forest bird communities are affected by the forest structure and the density and composition of its understory vegetation. In this study, we focused on the combined effects of vegetation structure and caller identity on the mobbing behavior of birds in breeding and non-breeding seasons. We examined the effect of the understory structure and the density of three types of conifer forest habitats on bird behavior by broadcasting three different types of mobbing calls: Those of two all-year resident species in the state Israel (Sardinian warbler Sylvia melanocephala Gmelin and great tit Parus major L.) and one European species (coal tit Periparus ater L.), which is absent from these habitats. The mobbing call attracted 689 birds of 17 species, which represented 31% to 95% of the forest bird species that we detected in point counts at the same study plots. Bird reactions to mobbing calls were affected by the status and season, depending on forest type. Our results show that responses were stronger in forests with developed understory in comparison to forests with no understory, especially in winter. The highest number of responders and highest species richness of responders were observed in winter. P. major calls generated more interspecific than intraspecific responses, whereas S. melanocephala calls generated equal levels of inter- and intraspecific reactions. Both species generated different response patterns across the three forest habitat types. The response level of responders is higher when the mobbing calls are issued by local species rather than the P. ater. In winter, the response of non-resident species was higher than of resident species. Based on these results, we encourage the managers to maintain well-established understory vegetation, with special attention to the shrubs layer, to promote species diversity and rich behavioral responses of birds in the conifer forests in the eastern Mediterranean region.

The role of associative learning process on the response of fledgling great tits (Parus major) to mobbing calls.

When they detect a predator, many species emit anti-predator vocalizations. In some cases, they emit mobbing calls, which are associated with the caller approaching and harassing the predator while attracting others to join it. Surprisingly, although mobbing has been widely reported in adults of numerous species, there has been no test of the role of learning in mobbing call recognition, especially during ontogeny. Here, we exposed wild great tit (Parus major) nestlings to playbacks of an unthreatening novel sound either associated with conspecific mobbing calls (experimental treatment) or with another unthreatening novel sound (control treatment). We then tested them as nestlings and fledglings to see how they respond to the novel sound compared to conspecific mobbing calls. Results revealed that fledglings in the experimental treatment behaved similarly to conspecific mobbing calls and the novel sound associated with conspecific mobbing calls. Because mobbing efficiency is often linked to interspecific communication, associative learning should be used by heterospecifics as mobbing calls recognition mechanism. Regardless of treatment during the nestling phase, fledglings always were sensitive to the playback of conspecific mobbing calls. However, fledglings from the control group were more likely to approach the loudspeaker than those from the experimental group when mobbing calls were played suggesting that overexposure during the nestling phase altered mobbing learning. Overall, these results suggest that learning could play a role in the recognition of calls, like heterospecific mobbing calls, when paired with conspecific mobbing, and that mobbing is perceived as a threatening stimulus from a very young age.

Is “Pishing” Tantamount to Mobbing? Black-Capped Chickadees Respond Similarly to Human Pishing and Conspecific Mobbing Calls in Rural and Suburban Forests

Poecile atricapillus (Black-capped Chickadee) mobbing calls elicit mobbing events in which birds drive away a predator. Human birders simulate these calls by “pishing” (vocalizing mobbing calls) to coerce birds into view. We investigated whether pishing is as salient as natural mobbing calls, and whether birds respond differently in suburban forest fragments than in intact forests. Using experimental playbacks, we broadcast mobbing calls and pishing calls in suburban forest patches and intact forests and measured Chickadee response. We found that Chickadees had significantly stronger responses to mobbing calls than to alarm calls used as a positive control, but pishing call response was not significantly different than mobbing or control alarm call responses. We also saw no difference in number of Chickadees responding between suburban fragments and intact forests, but we did see a difference in areas with denser vegetation. These findings show that pishing may be less urgent than Chickadee mobbing calls but may still contribute to stress and energetic demands on birds.

Supplemental feeding may reduce responsiveness of Black-capped Chickadees (Poecile atricapillus) to avian mobbing calls during gap-crossing experiments

Deforestation creates gaps in forest habitat, which can limit the movements of many avian species. Increased predation risk associated with crossing open habitats is often considered the primary impediment to crossing gaps. However, other factors such as energetic reserves may also influence these decisions. We conducted playback experiments before and after supplemental feeding of Black-capped Chickadees (Poecile atricapillus (Linnaeus, 1766)) to investigate how energetic reserves influenced gap-crossing decisions. Black-capped Chickadees were less likely to respond to playbacks, whether conducted within forests or across gaps, after supplemental feeding. This suggests that energetic reserves may have less influence on gap-crossing decisions than on the willingness of birds to respond to mobbing calls in general. We recommend that future studies investigating gap-crossing decisions using playbacks account for differences in resource availability among sampling locations, especially when making comparisons across discrete habitats.

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.

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.

Syntax manipulation changes perception of mobbing call sequences across passerine species

AbstractMany species approach predators to harass them and drive them away. Both the intensity of this antipredator strategy and its success are positively related to the size of the group that carries out this mobbing. To recruit individuals to the mob, members of prey species produce mobbing calls. In some songbirds—the Japanese tit, Parus minor, and the southern pied babbler, Turdoides bicolor—mobbing calls are structurally complex and it has been suggested that they convey information by means of compositional syntax, when meaningful items are combined into larger units. These two species combine alert and recruitment calls into an alert and recruitment sequence when attracting conspecifics to cooperate in mobbing a predator. Whether this rudimentary, two‐call, compositional structure is used by other bird species in mobbing calls and how it can alter the ability of heterospecifics to adequately recognize mobbing calls is not well understood. Heterospecifics’ responses to mobs are critical to the success of the mobbing strategy, so it is of great importance to understand whether and how syntax influences these responses. To address these questions, we conducted two playback experiments. Firstly, we investigated whether the great tit, Parus major, extracts different meanings from different individual motifs (i.e., component calls), and from combined motifs in both natural and artificially reversed order. We found that great tits extract different meanings from the two motifs involved in mobbing calls and that they also discriminate for motif order reversal in the mobbing call sequence. Secondly, we investigated whether heterospecifics (the coal tit, Periparus ater, and the common chaffinch, Fringilla coelebs) are sensitive to syntax alteration of great tit mobbing calls. While chaffinches did not respond to great tit mobbing calls, coal tits were sensitive to mobbing call sequence reversal although they did not react in the same way as conspecific subjects. Overall, whereas our results indicate that tits are sensitive to call reversal, this is not to say that tits actually use compositional syntax to increase the information content.

Subtle variations in mobbing calls are predator-specific in great tits (Parus major)

Many species are known to use vocalizations to recruit con- and heterospecifics to mobbing events. In birds, the vocalizations of the Family Paridae (titmice, tits and chickadees) are well-studied and have been shown to recruit conspecifics and encode information about predation risk. Species use the number of elements within a call, call frequency or call type to encode information. We conducted a study with great tits (Parus major) in the field where we presented taxidermy mounts of two predators of different threat levels (tawny owl, Strix aluco, and sparrowhawk, Accipiter nisus) and compared the mobbing calls of these two contexts. We hypothesized, based on results of studies in other paridae species, that tits vary the number or type of elements of a call according to predatory context. We found great tits to vary the number of D elements and the interval between those elements. Great tits produced significantly longer D calls with more elements and longer intervals between elements when confronted with a sparrowhawk (high-threat) compared to a tawny owl (low-threat) mount. Furthermore, birds produced more D calls towards the high-threat predator. This suggests that the basic D calls are varied depending on threat intensity.

Seasonal variation in mobbing behaviour of passerine birds

When they detect a predator, many birds exhibit mobbing behaviour and produce mobbing calls that quickly draw other prey against the predator. This anti-predator strategy often involves several species and, therefore, implies heterospecific communication. As fledging and nestling stages could be particularly targeted by predators, a high mobbing intensity is to be expected during the breeding season. While recognizing other species’ mobbing calls is critical to setting up this behaviour, to date, we have no information about the perception of these calls with regard to the season. Here, we used playbacks of mobbing calls to study the variation in response of the Great Tit (Parus major) and the Blue Tit (Cyanistes caeruleus) exposed to the mobbing calls of two heterospecific species, the Eurasian Nuthatch (Sitta europaea), and the Eurasian Wren (Troglodytes troglodytes). To investigate mobbing response seasonality, we conducted playback experiments during spring (breeding season) and autumn (non-breeding season). Contrary to most previous studies, we found that mobbing intensity was greater in autumn than in spring. Additionally, although neither Nuthatch nor Wren is related to the Tit family, we found that both Tit species responded more to the former than the latter species. At the heterospecific communication level, this study demonstrates a previously unsuspected level of complexity in the use of mobbing calls.

Birds orient their heads appropriately in response to functionally referential alarm calls of heterospecifics

Vertebrate alarm calls signal danger and often encode graded or categorical information about predator proximity or type. In addition to allowing communication with conspecifics, alarm calls are a valuable source of information for eavesdropping heterospecifics. However, although eavesdropping has been experimentally demonstrated in over 70 species, we know little about exactly what information eavesdroppers gain from heterospecific alarm calls. Here, we investigated whether Australian magpies, Cracticus tibicen, extract relevant information about the type of threat from functionally referential alarm calls given by noisy miners, Manorina melanocephala. Miner aerial alarm calls signal a predator in flight, whereas mobbing calls signal a terrestrial or perched predator. We therefore tested whether magpies gain information on the elevation of expected danger. We first confirmed, by measuring bill angles on video, that magpie head orientation changes appropriately with differences in the elevation of a conspicuous moving object. We then conducted a field experiment that measured magpie bill angle in response to playback of miner aerial and mobbing alarm calls. The maximum and mean bill angles were higher in response to aerial than to mobbing calls, suggesting that magpies use information from miner alarms to search visually at appropriate elevations for the specific type of danger. Magpies were also vigilant for longer after aerial alarm calls that followed mobbing calls, implying perception of an escalating threat level. Our work shows that individuals can gain information on the type or location of danger from heterospecific alarm calls, which is likely to increase the effectiveness of antipredator responses.

The low-frequency acoustic structure of mobbing calls differs across habitat types in three passerine families

The acoustic adaptation hypothesis predicts that animals should adaptively respond to the transmission properties of the habitat in which they communicate. Although there have been many tests of the acoustic adaptation hypothesis with birdsong, there have been very few tests with different types of bird vocalizations. Here I tested the predictions of the acoustic adaptation hypothesis with avian mobbing calls produced in closed, open and urban habitats in three families of passerine birds. I also controlled for body size and phylogeny since these are known to influence acoustic characteristics of vocalizations. I found that body size was important in duration and frequency measurements of mobbing call acoustic structure. Phylogeny explained acoustic variation in only some acoustic variables measured. I also found only the two low-frequency measurements to differ across habitats. First, 5% frequency (a measurement of low-frequency energy distribution) differed between species classified as occurring in predominately open or closed habitats, with species classified as closed having lower 5% frequency than species classified as open. This finding supports the prediction that species in closed habitats will have lower low frequencies than species in open habitats. Additionally, I found that species classified as urban had a lower minimum frequency. This is in direct opposition to the prediction of the acoustic adaptation hypothesis and previous findings for birdsong, where species appear to shift lower minimum frequencies upward, likely to avoid masking by anthropogenic noise. To confirm this finding, I also measured low frequency using power spectra with an amplitude threshold (i.e. threshold method) and confirmed the same result: species classified as urban had lower minimum frequencies than species classified as open or closed.

Testing social learning of anti-predator responses in juvenile jackdaws: the importance of accounting for levels of agitation.

Social learning is often assumed to help young animals respond appropriately to potential threats in the environment. We brought wild, juvenile jackdaws briefly into captivity to test whether short exposures to conspecific vocalizations are sufficient to promote anti-predator learning. Individuals were presented with one of two models—a stuffed fox representing a genuine threat, or a toy elephant simulating a novel predator. Following an initial baseline presentation, juveniles were trained by pairing models with either adult mobbing calls, indicating danger, or contact calls suggesting no danger. In a final test phase with no playbacks, birds appeared to have habituated to the elephant, regardless of training, but responses to the fox remained high throughout, suggesting juveniles already recognized it as a predator before the experiment began. Training with mobbing calls did seem to generate elevated escape responses, but this was likely to be a carry-over effect of the playback in the previous trial. Overall, we found little evidence for social learning. Instead, individuals' responses were mainly driven by their level of agitation immediately preceding each presentation. These results highlight the importance of accounting for agitation in studies of anti-predator learning, and whenever animals are held in captivity for short periods.

Mobbing calls: a signal transcending species boundaries

When they detect a predator, some prey exhibit mobbing behaviour and produce mobbing calls that quickly draw a mixed conspecific and heterospecific group against the predator. While the efficiency of this strategy is often linked to interspecific communication, it raises the question of how animals recognize these signals as mobbing calls. It is usually suggested that associative learning about a predator when heterospecific mobbing calls are heard plays a crucial role in communication among species. Alternatively, phylogenetic conservation or evolutionary convergence could also explain this communication process. To determine whether prior experience is required to express a mobbing response, we conducted playback experiments with four European passerine species: great tit, Parus major, blue tit, Cyanistes caeruleus, coal tit, Periparus ater, and common chaffinch, Fringilla coelebs. The aim of the study was to examine whether they would respond to the mobbing signals of several North American passerines. As expected, because natural selection might shape a strong response to conspecific mobbing calls, our focal species reacted more strongly towards their own mobbing calls than towards those of American species. Nevertheless, for the three European species of tit, prior experience of heterospecific mobbing calls was not required to elicit a response. Additionally, for great tit and chaffinch, we found that acoustic similarity could explain behavioural responses to allopatric species. In contrast, such similarity was probably not the main mechanism underlying the response for the other two European species. Heterospecific response to mobbing calls probably involved many different mechanisms. Further studies focusing on each of these should allow us to understand their relative contribution to heterospecific communication.

A comparative study of how British tits encode predator threat in their mobbing calls

Many species use antipredator vocalizations to signal information about potential predators, including the level of threat posed by a particular predator. It is not clear, however, why only some prey species do this. Because they use multiple mechanisms to encode threat-specific information about predators, North American Paridae species have been a particularly useful model for studying antipredator signals. Paridae as a group are also useful for examining phylogenetic conservation of vocal signals because all of these species (at least those studied previously) employ similar ways of encoding information about predator threat. To test whether the ways in which predator threat information is encoded (here measured by a bird's vocal output) are conserved across a family with similar vocalizations, we used taxidermy mounts to simulate low- and high-threat predators to induce mobbing in six species across five genera of British Paridae. We found that, like North American species, British tits all increased their call rate in response to predators compared with nonthreatening control mounts, but they all varied in the number and types of additional ways they encoded this information. Some species (blue and willow tits) used all four ways to differentiate between different threat predators, while others used only two (crested tits), one (great and coal tits) or none at all (willow tits). The variation in the way each species encoded predator threat information in their calls was not explained by phylogenetic relatedness or by variation in life history. To better understand patterns of information encoding across related species, we suggest that playback experiments to determine how encoded information is used by conspecifics and heterospecifics might provide insights about why some species encode information about predator threat in multiple ways.

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.