The relative contribution of acoustic signals versus movement cues in group coordination and collective decision-making.

To benefit from group living, individuals need to maintain cohesion and coordinate their activities. Effective communication thus becomes critical, facilitating rapid coordination of behaviours and reducing consensus costs when group members have differing needs and information. In many bird and mammal species, collective decisions rely on acoustic signals in some contexts but on movement cues in others. Yet, to date, there is no clear conceptual framework that predicts when decisions should evolve to be based on acoustic signals versus movement cues. Here, we first review how acoustic signals and movement cues are used for coordinating activities. We then outline how information masking, discrimination ability (Weber's Law) and encoding limitations, as well as trade-offs between these, can identify which types of collective behaviours likely rely on acoustic signals or movement cues. Specifically, our framework proposes that behaviours involving the timing of events or expression of specific actions should rely more on acoustic signals, whereas decisions involving complex choices with multiple options (e.g. direction and destination) should generally use movement cues because sounds are more vulnerable to information masking and Weber's Law effects. We then discuss potential future avenues of enquiry, including multimodal communication and collective decision-making by mixed-species animal groups. This article is part of the theme issue 'The power of sound: unravelling how acoustic communication shapes group dynamic'.

Social restructuring during harsh environmental conditions promotes cooperative behaviour in a songbird.

Cooperation may emerge from intrinsic factors such as social structure and extrinsic factors such as environmental conditions. Although these factors might reinforce or counteract each other, their interaction remains unexplored in animal populations. Studies on multilevel societies suggest a link between social structure, environmental conditions and individual investment in cooperative behaviours. These societies exhibit flexible social configurations, with stable groups that overlap and associate hierarchically. Structure can be seasonal, with upper-level units appearing only during specific seasons, and lower-level units persisting year-round. This offers an opportunity to investigate how cooperation relates to social structure and environmental conditions. Here, we study the seasonal multilevel society of superb fairy-wrens (Malurus cyaneus), observing individual responses to experimental playback of conspecific distress calls. Individuals engaged more in helping behaviour and less in aggressive/territorial song during the harsher non-breeding season compared to the breeding season. The increase in cooperation was greater for breeding group members than for members of the same community, the upper social unit, comprised of distinct breeding groups in association. Results suggest that the interaction between social structure and environmental conditions drives the seasonal switch in cooperation, supporting the hypothesis that multilevel societies can emerge to increase cooperation during harsh environmental conditions.

Species diversity and interspecific information flow.

Interspecific information flow is known to affect individual fitness, population dynamics and community assembly, but there has been less study of how species diversity affects information flow and thereby ecosystem functioning and services. We address this question by first examining differences among species in the sensitivity, accuracy, transmissibility, detectability and value of the cues and signals they produce, and in how they receive, store and use information derived from heterospecifics. We then review how interspecific information flow occurs in communities, involving a diversity of species and sensory modes, and how this flow can affect ecosystem-level functions, such as decomposition, seed dispersal or algae removal on coral reefs. We highlight evidence that some keystone species are particularly critical as a source of information used by eavesdroppers, and so have a disproportionate effect on information flow. Such keystone species include community informants producing signals, particularly about predation risk, that influence other species' landscapes of fear, and aggregation initiators creating cues or signals about resources. We suggest that the presence of keystone species means that there will likely be a positive relationship in many communities between species diversity and information through a 'sampling effect', in which larger pools of species are more likely to include the keystone species by chance. We then consider whether the number and relative abundance of species, irrespective of the presence of keystone species, matter to interspecific information flow; on this issue, the theory is less developed, and the evidence scant and indirect. Higher diversity could increase the quantity or quality of information that is used by eavesdroppers because redundancy increases the reliability of information or because the species provide complementary information. Alternatively, there could be a lack of a relationship between species diversity and information if there is widespread information parasitism where users are not sources, or if information sourced from heterospecifics is of lower value than that gained personally or sourced from conspecifics. Recent research suggests that species diversity does have information-modulated community and ecosystem consequences, especially in birds, such as the diversity of species at feeders increasing resource exploitation, or the number of imitated species increasing responses to vocal mimics. A first step for future research includes comprehensive observations of information flow among different taxa and habitats. Then studies should investigate whether species diversity influences the cumulative quality or quantity of information at the community level, and consequently ecosystem-level processes. An applied objective is to conserve species in part for their value as sources of information for other species, including for humans.

Noise constrains heterospecific eavesdropping more than conspecific reception of alarm calls.

Many vertebrates eavesdrop on alarm calls of other species, as well as responding to their own species' calls, but eavesdropping on heterospecific alarm calls might be harder than conspecific reception when environmental conditions make perception or recognition of calls difficult. This could occur because individuals lack hearing specializations for heterospecific calls, have less familiarity with them, or require more details of call structure to identify calls they have learned to recognize. We used a field playback experiment to provide a direct test of whether noise, as an environmental perceptual challenge, reduces response to heterospecific compared to conspecific alarm calls. We broadcast superb fairy-wren (Malurus cyaneus) and white-browed scrubwren (Sericornis frontalis) flee alarm calls to each species with or without simultaneous broadcast of ambient noise. Using two species allows isolation of the challenge of heterospecific eavesdropping independently of any effect of call structure on acoustic masking. As predicted, birds were less likely to flee to heterospecific than conspecific alarm calls during noise. We conclude that eavesdropping was harder in noise, which means that noise could disrupt information on danger in natural eavesdropping webs and so compromise survival. This is particularly significant in a world with increasing anthropogenic noise.

The quality of avian vocal duets can be assessed independently of the spatial separation of signallers.

Interactions among groups are often mediated through signals, including coordinated calls such as duets, and the degree of temporal coordination within a group can affect signal efficacy. However, in addition to intrinsic duet quality, the spatial arrangement of callers also affects the timing of calls. So, can listeners discriminate temporal effects caused by intrinsic duet quality compared to spatial arrangement? Such discrimination would allow assessment of quality of duets produced by a pair, as distinct from transient extrinsic spatial effects. To address this issue, we studied experimentally the influence of intrinsic duet quality and spatial arrangement on the efficacy of Australian magpie-lark (Grallina cyanoleuca) vocal duets. Breeding pairs duet at varying distances from each other and to multiple neighbours. Coordinated duets are more effective territorial signals than uncoordinated duets, but it remains unclear whether listeners can discriminate the effects of quality and spatial arrangement. Our playback experiment showed that any deviation from perfect regularity of partners' notes reduced duet efficacy, but that lack of coordination due to spatial separation (slower tempo and offset of notes) had a lower effect on efficacy than effects due to intrinsic quality (irregularity). Our results therefore provide experimental evidence that the temporal organisation of group vocalisations could signal coalition quality independently of spatial effects.

The evolution of eavesdropping on heterospecific alarm calls: Relevance, reliability, and personal information.

Interceptive eavesdropping on the alarm calls of heterospecifics provides crucial information about predators. Previous research suggests predator discrimination, call relevance, reliability, and reception explain when eavesdropping will evolve. However, there has been no quantitative analysis to scrutinize these principles, or how they interact. We develop a mathematical framework that formalizes the study of the key principles thought to select for eavesdropping. Interceptive eavesdropping appears to be greatly affected by the threat faced by caller and eavesdropper, as well as presence of informational noise affecting the detection of calls and predators. Accordingly, our model uses signal detection theory to examine when selection will favor alarm calling by a sender species and fleeing by an eavesdropping receiver species. We find eavesdropping is most strongly selected when (1) the receiver faces substantial threats, (2) species are ecologically similar, (3) senders often correctly discriminate threats, (4) receivers often correctly perceive calls, and (5) the receiver's personal discrimination of threats is poor. Furthermore, we find (6) that very high predation levels can select against eavesdropping because prey cannot continuously flee and must conserve energy. Reliability of heterospecific calls for identifying threats is thought to be important in selecting for eavesdropping. Consequently, we formally define reliability, showing its connection to specificity and sensitivity, clarifying how these quantities can be measured. We find that high call relevance, due to similar vulnerability to predators between species, strongly favors eavesdropping. This is because senders trade-off false alarms and missed predator detections in a way that is also favorable for the eavesdropper, by producing less of the costlier error. Unexpectedly, highly relevant calls increase the total number of combined errors and so have lower reliability. Expectedly, when noise greatly affects personally gathered cues to threats, but not heterospecific calls or detection of predators, eavesdropping is favored.

Multilevel social structure predicts individual helping responses in a songbird.

Multilevel societies are formed when stable groups of individuals spatially overlap and associate preferentially with other groups, producing a hierarchical social structure.1 Once thought to be exclusive to humans and large mammals, these complex societies have recently been described in birds.2,3 However, it remains largely unclear what benefits individuals gain by forming multilevel societies.1 One hypothesis-based on food sharing in hunter-gatherers4-is that multilevel societies facilitate access to a range of cooperative relationships, with individual investment varying across the hierarchical levels of the society. We tested experimentally whether such graded cooperation occurs in the multilevel society of a songbird, the superb fairy-wren (Malurus cyaneus). Specifically, we measured whether responses to playbacks of distress calls-used to recruit help when in extreme danger-varied according to the social level at which the focal individual is connected with the caller. We predicted that anti-predator responses should be highest within breeding groups (the core social unit), intermediate between groups from the same community, and lowest across groups from different communities. Our results confirm that birds exhibit the predicted hierarchical pattern of helping and that, within breeding groups, this pattern is independent of kinship. This pattern of graded helping responses supports the hypothesis that multilevel social structures can sustain stratified cooperative relationships and reveals similarity in cooperation in qualitatively different behaviors-anti-predator behavior and food sharing-in the multilevel societies of songbirds and humans.

Reality and illusion: the assessment of angular separation of multi-modal signallers in a duetting bird.

The spatial distribution of cooperating individuals plays a strategic role in territorial interactions of many group-living animals, and can indicate group cohesion. Vocalizations are commonly used to judge the distribution of signallers, but the spatial resolution of sounds is poor. Many species therefore accompany calls with movement; however, little is known about the role of audio-visual perception in natural interactions. We studied the effect of angular separation on the efficacy of multimodal duets in the Australian magpie-lark, Grallina cyanoleuca. We tested specifically whether conspicuous wing movements, which typically accompany duets, affect responses to auditory angular separation. Multimodal playbacks of duets using robotic models and speakers showed that birds relied primarily on acoustic cues when visual and auditory angular separations were congruent, but used both modalities to judge separation between the signallers when modalities were spatially incongruent. The visual component modified the effect of acoustic separation: robotic models that were apart weakened the response when speakers were together, while models that were together strengthened responses when speakers were apart. Our results show that responses are stronger when signallers are together, and suggest that males were are able to bind information cross-modally on the senders' spatial location, which is consistent with a multisensory illusion.

Higher-order sequences of vocal mimicry performed by male Albert's lyrebirds are socially transmitted and enhance acoustic contrast.

Most studies of acoustic communication focus on short units of vocalization such as songs, yet these units are often hierarchically organized into higher-order sequences and, outside human language, little is known about the drivers of sequence structure. Here, we investigate the organization, transmission and function of vocal sequences sung by male Albert's lyrebirds (Menura alberti), a species renowned for vocal imitations of other species. We quantified the organization of mimetic units into sequences, and examined the extent to which these sequences are repeated within and between individuals and shared among populations. We found that individual males organized their mimetic units into stereotyped sequences. Sequence structures were shared within and to a lesser extent among populations, implying that sequences were socially transmitted. Across the entire species range, mimetic units were sung with immediate variety and a high acoustic contrast between consecutive units, suggesting that sequence structure is a means to enhance receiver perceptions of repertoire complexity. Our results provide evidence that higher-order sequences of vocalizations can be socially transmitted, and that the order of vocal units can be functionally significant. We conclude that, to fully understand vocal behaviours, we must study both the individual vocal units and their higher-order temporal organization.

Differential geographic patterns in song components of male Albert's lyrebirds.

Geographic variation in bird song has received much attention in evolutionary studies, yet few consider components within songs that may be subject to different constraints and follow different evolutionary trajectories. Here, we quantify patterns of geographic variation in the socially transmitted "whistle" song of Albert's lyrebirds (Menura alberti), an oscine passerine renowned for its remarkable vocal abilities. Albert's lyrebirds are confined to narrow stretches of suitable habitat in Australia, allowing us to map likely paths of cultural transmission using a species distribution model and least cost paths. We use quantitative methods to divide the songs into three components present in all study populations: the introductory elements, the song body, and the final element. We compare geographic separation between populations with variation in these components as well as the full song. All populations were distinguishable by song, and songs varied according to the geographic distance between populations. However, within songs, only the introductory elements and song body could be used to distinguish among populations. The song body and final element changed with distance, but the introductory elements varied independently of geographic separation. These differing geographic patterns of within-song variation are unexpected, given that the whistle song components are always produced in the same sequence and may be perceived as a temporally discrete unit. Knowledge of such spatial patterns of within-song variation enables further work to determine possible selective pressures and constraints acting on each song component and provides spatially explicit targets for preserving cultural diversity. As such, our study highlights the importance for science and conservation of investigating spatial patterns within seemingly discrete behavioral traits at multiple levels of organization.

Male lyrebirds create a complex acoustic illusion of a mobbing flock during courtship and copulation.

Darwin argued that females' "taste for the beautiful" drives the evolution of male extravagance,1 but sexual selection theory also predicts that extravagant ornaments can arise from sexual conflict and deception.2,3 The sensory trap hypothesis posits that elaborate sexual signals can evolve via antagonistic coevolution whereby one sex uses deceptive mimicry to manipulate the opposite sex into mating.3 Here, the success of deceptive mimicry depends on whether it matches the receiver's percept of the model,4 and so has little in common with concepts of aesthetic judgement and 'beauty.'1,5-9 We report that during their song and dance displays,10 male superb lyrebirds (Menura novaehollandiae) create an elaborate acoustic illusion of a mixed-species mobbing flock. Acoustic analysis showed that males mimicked the mobbing alarm calls of multiple species calling together, enhancing the illusion by also vocally imitating the wingbeats of small birds. A playback experiment confirmed that this illusion was sufficient to fool avian receivers. Furthermore, males produced this mimicry only (1) when females attempted to exit male display arenas, and (2) during the lyrebirds' unusually long copulation, suggesting that the mimicry aims to prevent females from prematurely terminating these crucial sexual interactions. Such deceptive behavior by males should select for perceptual acuity in females, prompting an inter-sexual co-evolutionary arms race between male mimetic accuracy and discrimination by females. In this way the elaboration of the complex avian vocalizations we call 'song' could be driven by sexual conflict, rather than a female's preference for male extravagance.

Discriminating between similar alarm calls of contrasting function.

In a pioneering study of signal design, Marler (Marler 1955 Nature176, 6-8. (doi:10.1038/176006a0); Marler 1957 Behaviour11, 13-37. (doi:10.1163/156853956X00066)) argued that the contrasting acoustic design of hawk (seet) and mobbing alarm calls of European passerines reflected their contrasting function. Hawk alarms were high-frequency tones, warning conspecifics to flee but making localization difficult for predators, while mobbing calls were broadband and harsh, allowing easy localization and approach. Contrasting signal features are also consistent with signal detection theory. Discriminating these calls quickly is critical for survival, because hawk alarms require immediate escape. These signals should therefore be selected to be easy to discriminate, reducing the trade-off between immediate fleeing to hawk alarms and unnecessary fleeing to mobbing alarms. Despite these expectations, hawk and mobbing alarm calls of superb fairy-wrens, Malurus cyaneus, are surprisingly similar, raising the question of discriminability without contextual cues. We synthesized these calls on computer, made intermediates and used playbacks to test whether calls can be discriminated acoustically, and if so by what features. We found that birds used multiple acoustic features when discriminating calls, allowing fast discrimination despite overlap in individual parameters. We speculate that the similarity of fairy-wren alarm calls could enhance detectability of both signals, while multiple subtle acoustic differences reduce a trade-off with discriminability. This article is part of the theme issue 'Signal detection theory in recognition systems: from evolving models to experimental tests'.

Speedy revelations: how alarm calls can convey rapid, reliable information about urgent danger.

In the perpetual struggle between high-speed predators and their prey, individuals need to react in the blink of an eye to avoid capture. Alarm calls that warn of danger therefore need to do so sufficiently rapidly that listeners can escape in time. Paradoxically, many species produce more elements in their alarm calls when signalling about more immediate danger, thereby increasing the reliability of transmission of critical information but taking longer to convey the urgent message. We found that New Holland honeyeaters, Phylidonyris novaehollandiae, incorporated more elements in alarm calls given to more dangerous predators, but video analysis revealed that listeners responded in 100 ms, after only the first element. Consistent with this rapid response, the acoustic structure of the first element varied according to the danger, and playbacks confirmed that birds need hear only the first element to assess risk. However, birds hid for longer and were more likely to flee, after calls with more elements. The dual mechanisms of varying both element structure and number may provide a widespread solution to signalling rapidly and reliably about immediate danger.

Personal information about danger trumps social information from avian alarm calls.

Information about predators can mean the difference between life and death, but prey face the challenge of integrating personal information about predators with social information from the alarm calls of others. This challenge might even affect the structure of interspecific information networks: species vary in response to alarm calls, potentially because different foraging ecologies constrain the acquisition of personal information. However, the hypothesis that constrained personal information explains a greater response to alarm calls has not been experimentally tested. We used a within-species test to compare the antipredator responses of New Holland honeyeaters, Phylidonyris novaehollandiae, during contrasting foraging behaviour. Compared with perched birds, which hawk for insects and have a broad view, those foraging on flowers were slower to spot gliding model predators, showing that foraging behaviour can affect predator detection. Furthermore, nectar-foraging birds were more likely to flee to alarm call playbacks. Birds also assessed social information relevance: more distant calls, and those from another species, prompted fewer flights and slower reaction times. Overall, birds made flexible decisions about danger by integrating personal and social information, while weighing information relevance. These findings support the idea that a strategic balance of personal and social information could affect community function.

Birds Learn Socially to Recognize Heterospecific Alarm Calls by Acoustic Association.

Animals in natural communities gain information from members of other species facing similar ecological challenges [1-5], including many vertebrates that recognize the alarm calls of heterospecifics vulnerable to the same predators [6]. Learning is critical in explaining this widespread recognition [7-13], but there has been no test of the role of social learning in alarm-call recognition, despite the fact that it is predicted to be important in this context [14, 15]. We show experimentally that wild superb fairy-wrens, Malurus cyaneus, learn socially to recognize new alarm calls and can do so through the previously undemonstrated mechanism of acoustic-acoustic association of unfamiliar with known alarm calls. Birds were trained in the absence of any predator by broadcasting unfamiliar sounds, to which they did not originally flee, in combination with a chorus of conspecific and heterospecific aerial alarm calls (typically given to hawks in flight). The fairy-wrens responded to the new sounds after training, usually by fleeing to cover, and responded equally as strongly in repeated tests over a week. Control playbacks showed that the response was not due simply to greater wariness. Fairy-wrens therefore learnt to associate new calls with known alarm calls, without having to see the callers or a predator. This acoustic-acoustic association mechanism of social learning could result in the rapid spread of alarm-call recognition in natural communities, even when callers or predators are difficult to observe. Moreover, this mechanism offers potential for use in conservation by enhancing training of captive-bred individuals before release into the wild.

Sounds of Modified Flight Feathers Reliably Signal Danger in a Pigeon.

In his book on sexual selection, Darwin [1] devoted equal space to non-vocal and vocal communication in birds. Since then, vocal communication has become a model for studies of neurobiology, learning, communication, evolution, and conservation [2, 3]. In contrast, non-vocal "instrumental music," as Darwin called it, has only recently become subject to sustained inquiry [4, 5]. In particular, outstanding work reveals how feathers, often highly modified, produce distinctive sounds [6-9], and suggests that these sounds have evolved at least 70 times, in many orders [10]. It remains to be shown, however, that such sounds are signals used in communication. Here we show that crested pigeons (Ochyphaps lophotes) signal alarm with specially modified wing feathers. We used video and feather-removal experiments to demonstrate that the highly modified 8th primary wing feather (P8) produces a distinct note during each downstroke. The sound changes with wingbeat frequency, so that birds fleeing danger produce wing sounds with a higher tempo. Critically, a playback experiment revealed that only if P8 is present does the sound of escape flight signal danger. Our results therefore indicate, nearly 150 years after Darwin's book, that modified feathers can be used for non-vocal communication, and they reveal an intrinsically reliable alarm signal.

Deceptive vocal duets and multimodal display in a songbird.

Many group-living animals cooperatively signal to defend resources, but what stops deceptive signalling to competitors about coalition strength? Cooperative-signalling species include mated pairs of birds that sing duets to defend their territory. Individuals of these species sometimes sing 'pseudo-duets' by mimicking their partner's contribution, but it is unknown if these songs are deceptive, or why duets are normally reliable. We studied pseudo-duets in Australian magpie-larks, Grallina cyanoleuca, and tested whether multimodal signalling constrains deception. Magpie-larks give antiphonal duets coordinated with a visual display, with each sex typically choosing a different song type within the duet. Individuals produced pseudo-duets almost exclusively during nesting when partners were apart, but the two song types were used in sequence rather than antiphonally. Strikingly, birds hid and gave no visual displays, implying deceptive suppression of information. Acoustic playbacks showed that pseudo-duets provoked the same response from residents as true duets, regardless of whether they were sequential or antiphonal, and stronger response than that to true duets consisting of a single song type. By contrast, experiments with robot models showed that songs accompanied by movements of two birds prompted stronger responses than songs accompanied by movements of one bird, irrespective of the number of song types or singers. We conclude that magpie-larks used deceptive pseudo-duets when partners were apart, and suppressed the visual display to maintain the subterfuge. We suggest that the visual component of many species' duets provides the most reliable information about the number of signallers and may have evolved to maintain honesty in duet communication.

Bright birds are cautious: seasonally conspicuous plumage prompts risk avoidance by male superb fairy-wrens.

Increased predation risk is considered a cost of having conspicuous colours, affecting the anti-predator behaviour of colourful animals. However, this is difficult to test, as individual factors often covary with colour and behaviour. We used alarm call playback and behavioural observations to assess whether individual birds adjust their response to risk according to their plumage colour. Male superb fairy-wrens (Malurus cyaneus) change from a dull brown to conspicuous blue plumage each year, allowing the behaviour of different coloured birds to be compared while controlling for within-individual effects. Because the timing of colour change varies among males, blue and brown birds can also be compared at the same time of year, controlling for seasonal effects on behaviour. While blue, fairy-wrens fled more often in response to alarm calls, and took longer to emerge from cover. Blue fairy-wrens also spent more time foraging in cover and being vigilant. Group members appeared to benefit from the presence of blue males, as they reduced their response to alarms, and allocated less time to sentinel behaviour when a blue male was close by. We suggest that fairy-wrens perceive themselves to be at a higher risk of predation while in conspicuous plumage and adjust their behaviour accordingly.

Wild birds learn to eavesdrop on heterospecific alarm calls.

Many vertebrates gain critical information about danger by eavesdropping on other species' alarm calls [1], providing an excellent context in which to study information flow among species in animal communities [2-4]. A fundamental but unresolved question is how individuals recognize other species' alarm calls. Although individuals respond to heterospecific calls that are acoustically similar to their own, alarms vary greatly among species, and eavesdropping probably also requires learning [1]. Surprisingly, however, we lack studies demonstrating such learning. Here, we show experimentally that individual wild superb fairy-wrens, Malurus cyaneus, can learn to recognize previously unfamiliar alarm calls. We trained individuals by broadcasting unfamiliar sounds while simultaneously presenting gliding predatory birds. Fairy-wrens in the experiment originally ignored these sounds, but most fled in response to the sounds after two days' training. The learned response was not due to increased responsiveness in general or to sensitization following repeated exposure and was independent of sound structure. Learning can therefore help explain the taxonomic diversity of eavesdropping and the refining of behavior to suit the local community. In combination with previous work on unfamiliar predator recognition (e.g., [5]), our results imply rapid spread of anti-predator behavior within wild populations and suggest methods for training captive-bred animals before release into the wild [6]. A remaining challenge is to assess the importance and consequences of direct association of unfamiliar sounds with predators, compared with social learning-such as associating unfamiliar sounds with conspecific alarms.