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.     

The versatility of graded acoustic measures in classification of predation threats by the tufted titmouse Baeolophus bicolor: exploring a mixed framework for threat communication

Many mammal and bird species respond to predator encounters with alarm vocalizations that generate risk‐appropriate responses in listeners. Two conceptual frameworks are typically applied to the information encoded in alarm calls and to associated anti‐predator behaviors. ‘Functionally referential’ alarm systems encode nominal classes or categories of risk in distinct call types that refer to distinct predation‐risk situations. ‘Risk‐based’ alarms encode graded or ranked threat‐levels by varying the production patterns of the same call types as the urgency of predation threat changes. Recent work suggests that viewing alarm‐response interactions as either referential or risk‐based may oversimplify how animals use information in decision‐making. Specifically, we explore whether graded alarm cues may be useful in classifying risks, supporting a referential decision‐making framework. We presented predator (hawk, owl, cat, snake) and control treatments to captive adult tufted titmice Baeolophus bicolor and recorded their vocalizations, which included ‘chick‐a‐dee’ mobbing calls (composed of chick and D notes), ‘seet’ notes, two types of contact notes (‘chip’, ‘chink’), and song. No single call type was uniquely associated with any treatment and the majority of acoustic measures varied significantly among treatments (46 of 60). The strongest models (ANOVA and classification tree analysis) grouped hawk with cat and owl, and control with snake, and were based on the number or proportion of a) chick and D notes per chick‐a‐dee call, b) chip versus chink notes produced following treatment exposure, and c) the frequency metrics of other note types. We conclude that (1) the predation‐threat information available in complex titmouse alarm calls was largely encoded in graded acoustic measures that were (2) numerous and variable across treatments and (3) could be used singly or in combinations for either ranking or classification of threats. We call attention to the potential use of mixed threat identification strategies, where risk‐based signal information may be used in referential decision‐making contexts.     

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.     

Syntax manipulation changes perception of mobbing call sequences across passerine species

Many 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.     

Semantic Differences in Sifaka (Propithecus verreauxi) Alarm Calls: A Reflection of Genetic or Cultural Variants?

In this study, we compared the usage of alarm calls and anti‐predator strategies between a captive and a wild lemur population. The wild lemur population was studied earlier in Western Madagascar ( Fichtel & Kappeler 2002 ). The captive population was studied in outdoor enclosures of the Duke University Primate Center. Alarm calls and anti‐predator behavior were elicited by conducting experiments with both vocal and visual dummies. We scored the subjects’ immediate behavioral responses, including alarm calls, from video recordings made during the experiments. In principle, both populations have a mixed alarm call system with functionally referential alarm calls for aerial predators and general alarm calls for terrestrial and aerial predators and for situations associated with high arousal, such as group encounters. Although wild and captive sifakas exhibit the same alarm call system and use the same alarm call types, we discovered striking differences in the usage and perception of some of the alarm calls. We argue that these differences indicate either an evolutionary drift in the meaning of these calls or reflect cultural variation. The latter possibility is consistent with our understanding of the ontogeny of call usage and comprehension.     

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.     

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.     

Mobbing behaviour in a passerine community increases with prevalence in predator diet

Mobbing behaviour against predators is well documented but less is known about the factors influencing variation in behavioural response between prey species. We conducted a series of playback experiments to examine how the mobbing responses of prey species differed according to their relative risk of predation by the Eurasian Pygmy Owl Glaucidium passerinum, a predator of passerines. We found that mobbing among 22 passerine prey species was positively correlated with their prevalence in the Pygmy Owl diet. To compare mobbing behaviour between two seasons, we conducted playback experiments during spring (breeding season) and autumn (non‐breeding season). Contrary to previous studies, we found that mobbing intensity was greater during autumn than in spring. Our study shows a differential mobbing response of 22 species to the calls from one predator species and underscores the importance of considering seasonal variation in mobbing behaviour. Mobbing response differences observed among bird species strongly suggest different cooperation behaviour at the community level.     

Which Call Parameters Signal Threat to Conspecifics in White‐Throated Magpie‐Jay Mobbing Calls?

Abstract Variation in signals often encodes additional information beyond that provided by the main signal. Many species communicate degree of threat using such signal variation. However, multiple signal parameters often covary with threat level, and it is unclear whether receivers are using variation along one or more parameters when assessing threat level. White-throated magpie-jays ( Calocitta formosa ) vary several call parameters when mobbing, and here I report on an experiment testing whether such variation contains information used by conspecific receivers, and which parameters are salient to receivers. I collected data on natural mobbing sequences in two threat contexts and found that mobbing calls were highly variable in both length and inter-call interval, but on average, both parameters were shorter in high threat contexts, while call frequency did not differ. To determine how jays respond to such between-context variation, I conducted a playback experiment in which call length and inter-call interval were independently varied in a factorial design. This is one of the first studies to my knowledge to deconstruct and independently test covarying signal parameters in an anti-predator signaling system. Magpie-jays responded more often to treatments with either short call lengths or short inter-call intervals, in concordance with the natural calling data. However, the two parameters did not appear to act independently; responses were not additive, and short calls at short inter-call intervals elicited no stronger of a response than short calls at long intervals or long calls at short intervals. Receivers can use either parameter when assessing threat level. These data demonstrate that mobbing can signal threat level, that call length and call rate are redundant, and that receivers need not use both to determine whether to approach.     

Distress Calls of Birds in a Neotropical Cloud Forest1

Distress calls are loud, harsh calls given by some species of birds when they are captured by a predator or handled by humans. We recorded the frequency of distress calls and struggling behavior in 40 species of birds captured in mist nets during the dry season in a Costa Rica cloud forest. We tested the following hypotheses proposed to explain the function of distress calls: (1) calling for help from kin or reciprocal altruists; (2) warning kin; (3) eliciting mobbing behavior; (4) startling the predator; and (5) distracting the predator through attraction of additional predators. Our results did not support the calling‐for‐help, warning kin, or mobbing hypotheses. Indeed, genera that regularly occurred with kin or in flocks were not more likely to call than non‐flocking genera. There was no relationship between calling frequency and struggling behavior as predicted by the predator startle hypothesis. Genera of larger birds tended to call more than smaller birds, providing some support for both the predator distraction hypothesis and predator startle hypotheses. Calls of higher amplitude may be more effective in startling the predator. Distress calls of larger birds may also travel greater distances than those of smaller birds, supporting the predator manipulation hypothesis, but this requires further testing.     

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

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

Is mobbing altruistic or selfish behaviour?

The hypotheses that try to explain mobbing behaviour can be divided into three main classes: altruistic behaviour, parental care and selfish behaviour. To try to distinguish between these hypotheses, I presented 12 Arabian babblers,Turdoides squamiceps , with a snake model, both alone and together with another babbler. Seven components of mobbing were compared in the two situations. Single babblers that were exposed to a snake model carried out mobbing-like behaviour. Mobbing in the absence of an audience or additional participants shows that it is basically a selfish behaviour, and suggests that it is an antipredator behaviour. No difference was found between males and females, and mobbing by two participants together was more intensive than mobbing by each of them on its own. These findings support the prey-predator communication hypothesis. However, the different hypotheses explaining mobbing are not exclusive, and this study does not exclude other hypotheses as secondary explanations. Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour.      

Facultative response to a kleptoparasite by the cooperatively breeding pied babbler

In many cases of interspecific kleptoparasitism, hosts developdefensive behaviors to minimize the impact of kleptoparasites.Because vigilance and defensive behaviors are often costly,selection should favor hosts that adjust the amount of investmentneeded to minimize losses to kleptoparasitism. However, examplesof such facultative responses are rare. Here, we investigatethe response of cooperatively breeding pied babblers (Turdoidesbicolor) to the drongo (Dicrurus adsimilis), an avian kleptoparasitethat regularly follows pied babbler groups, often giving alarmcalls to alert the group to predators but also occasionallygiving false alarm calls in order to steal food items. We showthat pied babbler response to drongos varies markedly accordingto babbler group size. In small groups, where there are fewindividuals available to act as sentinels, babblers sentinelless when a drongo is present and respond strongly to drongoalarm calls. However, in large groups, where there are manyindividuals available to participate in predator vigilance,babblers sentinel more often when a drongo is present, rarelyrespond to drongo alarm calls, and aggressively displace drongos,with a consequent decline in the number of successful kleptoparasitismevents. This behavior represent a facultative response to akleptoparasite according to the costs versus benefits of toleratingtheir presence.     

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.     

Effects of avian mobbing on roost use and diet of powerful owls,Ninox strenua

We observed the species and numbers of mobbing birds and their effects on a large, nocturnal, bird-eating predator, the powerful owl, together with the pattern of owl predation on mobbing and non-mobbing species. Owls were mobbed on 35 occasions by seven of 44 species of forest birds at a site composed of open forest (88% by area) and rainforest (12%). The majority of bouts involved individuals of a single species, although mixed groups were observed on nine occasions. Regular mobbers were between 4 and 26% of the owls’ body weight. Owls abandoned their daytime roosts during 20% of bouts and responded by calling or actively monitoring mobbers during 54% of bouts. Mobbing appeared to explain why owls roosted in rainforest significantly more often than expected by its availability, mobbing being significantly less frequent in rainforest than in open forest. Only one mobbing species regularly occupied rainforest and the canopy of roosts in rainforest was denser than that in open forest, thus reducing the chances of an owl being detected by potential mobbers. Twelve species of forest birds were within the range of prey size of the powerful owl (75–800 g): six were mobbers and six non-mobbers. The frequency of owl predation on non-mobbers was 8.75 times that on mobbers. The species in this study took a high risk by mobbing a very large predator, but benefited by greatly reducing their chances of predation.     

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.     

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.     

No evidence of eavesdropping on heterospecific alarm calls by captive zebra finches recently descended from wild birds

Alarm calls are vocalisations animals give in response to predators which mainly function to alert conspecifics of danger. Studies show that numerous species eavesdrop on heterospecific calls to gain information about predator presence. Responding to heterospecific calls may be a learned or innate response, determined by whether the response occurs with or without prior exposure to the call. In this study, we investigated the presence of eavesdropping behaviour in zebra finches Taeniopygia guttata. This species is not known to possess a distinct alarm call to warn adult conspecifics of a threat, and could be relying on alarm calls of nearby heterospecifics for predator information. We used a playback experiment to expose captive zebra finches to three heterospecific sounds: an unfamiliar alarm call (from the chestnut‐rumped thornbill Acanthiza uropygialis), a familiar alarm call, and a familiar control (both from the noisy miner Manorina melanocephala). These calls were chosen to test if the birds had learnt to distinguish between the function of the two familiar calls, and if the acoustic properties of the unfamiliar alarm indicated presence of a threat to the finches. Our results showed that in response to the thornbill alarm, the birds reduced the rate of production of short calls. However, this decrease was also seen when considering both short and distance calls in response to the control sound. An increase in latency to call was also seen after the control stimulus when compared to the miner alarm. The time spent scanning increased in response to all three stimuli, but this did not differ between stimuli. There were no significant differences when considering the stimulus by time interaction for any of the three vigilance measures. Overall, no strong evidence was found to indicate that the captive zebra finches were responding to the heterospecific alarm stimuli with anti‐predator behaviour.     

Acoustic preferences and localization performance of blood-sucking flies (Corethrella Coquillett) to tungara frog calls

Mating signals that increase attractiveness of males to femalescan also increase conspicuousness of the signaler to predatorsand parasites. We investigated the acoustic preference of speciesof blood-sucking flies of the genus Corethrella (Diptera: Corethrellidae),which eavesdrop on the sexual advertisement signals of túngarafrogs (Physalaemus pustulosus). Male frogs of this species facultativelyproduce 2 types of mating calls: simple (whines alone) and complex(whines and chucks). We tested the acoustic preference of theflies and their ability to locate their host when the frogsproduce simple or complex calls. The flies exhibited phonotaxisto both types of calls but were preferentially attracted tocomplex calls. We show that acoustic information alone is sufficientfor the flies' accurate localization of calling frogs. Complexcalls, however, were not approached at closer distance or withdecreased landing error (i.e., proportion of landings outsidethe target) than simple calls, suggesting that call structuredoes not influence localization performance. Female túngarafrogs and frog-eating bats (Trachops cirrhosus) also prefercomplex to simple túngara frog calls. Thus, intendedand unintended receivers with different ear morphologies exhibitthe same preference for a specific túngara frog calltype. This result is discussed in the context of the evolutionof call attractiveness in a communication network.