Sensory ecology: echolocation calls are used for communication

Noctule bats locate tree roosts faster by eavesdropping on the echolocation calls of conspecifics. Increasing evidence suggests that echolocation is important not only for orientation and finding prey, but also for communication.     

The communicative potential of bat echolocation pulses

Ecological constraints often shape the echolocation pulses emitted by bat species. Consequently some (but not all) bats emit species-specific echolocation pulses. Because echolocation pulses are often intense and emitted at high rates, they are potential targets for eavesdropping by other bats. Echolocation pulses can also vary within species according to sex, body size, age, social group and geographic location. Whether these features can be recognised by other bats can only be determined reliably by playback experiments, which have shown that echolocation pulses do provide sufficient information for the identification of sex and individual in one species. Playbacks also show that bats can locate conspecifics and heterospecifics at foraging and roost sites by eavesdropping on echolocation pulses. Guilds of echolocating bat species often partition their use of pulse frequencies. Ecology, allometric scaling and phylogeny play roles here, but are not sufficient to explain this partitioning. Evidence is accumulating to support the hypothesis that frequency partitioning evolved to facilitate intraspecific communication. Acoustic character displacement occurs in at least one instance. Future research can relate genetic population structure to regional variation in echolocation pulse features and elucidate those acoustic features that most contribute to discrimination of individuals.     

Social calls used by a leaf-roosting bat to signal location

Social calls in bats have many functions, including mate attraction and maintaining contact during flight. Research suggests that social calls may also be used to transfer information about roosts, but no studies have yet demonstrated that calls are used to actively attract conspecifics to roosting locations. We document the social calls used by Spix''s disc-winged bat (Thyroptera tricolor) to actively recruit group members to roosts. In acoustic trials, we recorded two sets of calls; one from flying individuals termed ‘inquiry calls’, and another from roosting bats termed ‘response calls’. Inquiry calls were emitted by flying bats immediately upon release, and quickly (i.e. 178 ms) elicited production of response calls from roosting individuals. Most flying bats entered the roost when roosting individuals responded, while few bats entered the roost in the absence of a response. We argue that information transfer concerning roost location may facilitate sociality in T. tricolor, given the ephemeral nature of roosting structures used by this species.     

Does Interspecific Eavesdropping Promote Aerial Aggregations in European Pipistrelle Bats During Autumn?

Eavesdropping is a widespread strategy to optimize decision‐making. Bats are interesting models for investigating acoustic information transfer, as they possess a broad vocalization repertoire of echolocation and social calls. Yet, the knowledge of the extent to which eavesdropping plays a role in bat communication is scarce. Here, we examined the vocal and spatial activity patterns of three congeneric bat species (Pipistrellus pipistrellus, P. pygmaeus, P. nathusii, hereafter called pipistrelles) during autumn – their migration and mating season. We hypothesized that pipistrelles utilize information of conspecifics and congenerics to localize stopover sites for mating or other information purposes during migration. We found that bats formed small multispecies aggregations on the wing, suggesting interspecific eavesdropping on feeding buzzes and/or courtship calls could occur among these species. Pipistrelles produced similar proportions of feeding buzzes and social calls at aggregation sites. To test whether pipistrelles respond to the courtship vocalizations of conspecifics and congenerics, we conducted a playback experiment with P. pipistrellus where we presented courtship vocalizations of the three pipistrelle species and as a control, a motif of the noctule bat's song (Nyctalus noctula). Pipistrellus pipistrellus decreased the rate of social calls in response to the broadcast of songs of P. nathusii, yet they tended to increase the rate in response to the playback of their own species. We conclude that interspecific eavesdropping occurs at least between P. pipistrellus and P. nathusii and might thus favour the formation of multispecies aggregations. Our findings provide novel insights into the social behaviour and interspecific communication of a bat community during the season of migration and mating.     

Social Calls Produced within and near the Roost in Two Species of Tent-Making Bats,Dermanura watsoni and Ectophylla alba

Social animals regularly face the problem of relocating conspecifics when separated. Communication is one of the most important mechanisms facilitating group formation and cohesion. Known as contact calls, signals exchanged between conspecifics that permit group maintenance are widespread across many taxa. Foliage-roosting bats are an excellent model system for studying the evolution of contact calling, as there are opportunities to compare closely related species that exhibit major differences in ecology and behavior. Further, foliage-roosting bats rely on relatively ephemeral roosts, which leads to major challenges in maintaining group cohesion. Here, we report findings on the communication signals produced by two tent-making bats, Dermanura watsoni and Ectophylla alba. We found that both species produced calls in the early morning near the roost that were associated with roostmate recruitment. Calling often ended once other bats arrived at the tent, suggesting that calls may be involved in roostmate recruitment and group formation. The structure and function of these calls are described and future research directions are discussed.     

Eavesdropping on heterospecific alarm calls: from mechanisms to consequences

Animals often gather information from other species by eavesdropping on signals intended for others. We review the extent, benefits, mechanisms, and ecological and evolutionary consequences of eavesdropping on other species' alarm calls. Eavesdropping has been shown experimentally in about 70 vertebrate species, and can entail closely or distantly related species. The benefits of eavesdropping include prompting immediate anti‐predator responses, indirect enhancement of foraging or changed habitat use, and learning about predators. Eavesdropping on heterospecifics can provide more eyes looking for danger, complementary information to that from conspecifics, and potentially information at reduced cost. The response to heterospecific calls can be unlearned or learned. Unlearned responses occur when heterospecific calls have acoustic features similar to that used to recognize conspecific calls, or acoustic properties such as harsh sounds that prompt attention and may allow recognition or facilitate learning. Learning to recognize heterospecific alarm calls is probably essential to allow recognition of the diversity of alarm calls, but the evidence is largely indirect. The value of eavesdropping on different species is affected by problems of signal interception and the relevance of heterospecific alarm calls to the listener. These constraints on eavesdropping will affect how information flows among species and thus affect community function. Some species are ‘keystone’ information producers, while others largely seek information, and these differences probably affect the formation and function of mixed‐species groups. Eavesdroppers might also integrate alarm calls from multiple species to extract relevant and reliable information. Eavesdropping appears to set the stage for the evolution of interspecific deception and communication, and potentially affects communication within species. Overall, we now know that eavesdropping on heterospecific alarm calls is an important source of information for many species across the globe, and there are ample opportunities for research on mechanisms, fitness consequences and implications for community function and signalling evolution.     

Landscape structure influences the use of social information in an insectivorous bat

In anthropogenic landscapes, aerial insectivores are often confronted with variable habitat complexity, which may influence the distribution of prey. Yet, high mobility may allow aerial insectivores to adjust their foraging strategy to different prey distributions. We investigated whether aerial-hunting common noctules Nyctalus noctula adjust their foraging strategy to landscapes with different habitat complexity and assumingly different prey distribution. We hypothesized that the movement behaviour of hunting common noctules and changes of movement behaviour in reaction towards conspecifics would depend on whether they hunt in a structurally poor cropland dominated landscape or a structurally rich forest dominated landscape. We tracked flight paths of common noctules in northeastern Germany using GPS loggers equipped with an ultrasonic microphone that recorded foraging events and presence of conspecifics. Above cropland, common noctules hunted mainly during bouts of highly tortuous and area restricted movements (ARM). Bats switched from straight flight to ARM after encountering conspecifics. In the forested landscape, common noctules hunted both during ARM and during straight flights. The onset of ARM did not correlate with the presence of conspecifics. Common noctules showed a lower feeding rate and encountered more conspecifics above the forested than above the cropland dominated landscape. We conjecture that prey distribution above cropland was patchy and unpredictable, thus making eavesdropping on hunting conspecifics crucial for bats during search for prey patches. In contrast, small scale structural diversity of the forested landscape possibly led to a more homogeneous prey distribution at the landscape scale, thus enabling bats to find sufficient food independent of conspecific presence. This suggests that predators depending on ephemeral prey can increase their foraging success in structurally poor landscapes by using social information provided by conspecifics. Hence, a minimum population density might be obligatory to enable successful foraging in simplified landscapes.     

Flight performance, echolocation and foraging behaviour in noctule bats Nyctalus noctula

The noctule Nyctulus noctula (Schreber, 1774) is a relatively large (c. 25 g) insectivorous bat which catches insects on the wing (by aerial hawking). Emergence at a maternity roost was earliest relative to sunset when females were lactating, and bats may then have risked predation by flying at higher light levels during a period of high energy demand. Flight performance was quantified by using stereophotogrammetry. At feeding sites bats flew at 6.0 ± 2.1 m/s. This was faster than predicted minimum power speed (V _mp), and either between V _mp and maximum range speed (V _mr), or close to their predicted V _mr, depending on which aerodynamic model of flight power requirements was used. The echolocation behaviour of noctules is flexible. Long duration, low frequency calls (c. 20 kHz) with little frequency modulation were emitted while cruising, but at foraging sites the calls became more frequency-modulated. As the noctule is traditionally thought of as using low frequency echolocation, it was expected to receive weak echoes from small targets and therefore to specialize in eating large insect prey. Although the bats ate mainly beetles, large numbers of small dipterans were also eaten. The noctule is probably able to detect such small items because, when foraging, its calls become broadband and sweep from high frequencies. Higher harmonics are also present, and these may assist in the detection of small prey. In noctules, as in many bats, there appears to be a 1:1 link between wingbeat and call production during the search phase of foraging.     

Calls in the Forest: A Comparative Approach to How Bats Find Tree Cavities

Although tree cavities are a particularly critical resource for forest bats, how bats search for and find new roosts is still poorly known. Building on a recent study on the sensory basis of roost finding in the noctule (Ruczynski et al. 2007), here we take a comparative approach to how bats find roosts. We tested the hypothesis that species' flight abilities and echolocation call characteristics play important roles in how well and by which cues bats find new tree roosts. We used the very manoeuvrable, faintly echolocating brown long-eared bat ( Plecotus auritus ) and the less manoeuvrable, louder Daubenton's bat ( Myotis daubentonii ) as study species. The species are sympatric in European temperate forests and both roost in tree cavities. We trained bats in short-term captivity to find entrances to tree cavities and experimentally manipulated the sensory cues available to them. In both species, cue type influenced the search time for successful cavity detection. Visual, olfactory and temperature cues did not improve the bats' performance over the performance by echolocation alone. Eavesdropping on conspecific echolocation calls played back from inside the cavity decreased search time in Daubenton's bat ( M. daubentonii ), underlining the double function of echolocation signals – orientation and communication. This was not so in the brown long-eared bat ( P. auritus ) that has low call amplitudes. The highly manoeuvrable P. auritus found cavities typically from flight and the less manoeuvrable M. daubentonii found more entrances during crawling. Comparison with the noctule data from Ruczyński et al. (2007) indicates that manoeuvrability predicts the mode of cavity search. It further highlights the importance of call amplitude for eavesdropping and cavity detection in bats.     

Bat echolocation calls facilitate social communication

Bat echolocation is primarily used for orientation and foraging but also holds great potential for social communication. The communicative function of echolocation calls is still largely unstudied, especially in the wild. Eavesdropping on vocal signatures encoding social information in echolocation calls has not, to our knowledge, been studied in free-living bats so far. We analysed echolocation calls of the polygynous bat Saccopteryx bilineata and found pronounced vocal signatures encoding sex and individual identity. We showed experimentally that free-living males discriminate approaching male and female conspecifics solely based on their echolocation calls. Males always produced aggressive vocalizations when hearing male echolocation calls and courtship vocalizations when hearing female echolocation calls; hence, they responded with complex social vocalizations in the appropriate social context. Our study demonstrates that social information encoded in bat echolocation calls plays a crucial and hitherto underestimated role for eavesdropping conspecifics and thus facilitates social communication in a highly mobile nocturnal mammal.     

Know thine enemy: fighting fish gather information from observing conspecific interactions

Many of the signals that animals use to communicate transmit relatively large distances and therefore encompass several potential signallers and receivers. This observation challenges the common characterization of animal communication systems as consisting of one signaller and one receiver. Furthermore, it suggests that the evolution of communication behaviour must be considered as occurring in the context of communication networks rather than dyads. Although considerations of selection pressures acting upon signallers in the context of communication networks have rarely been expressed in such terms, it has been noted that many signals exchanged during aggressive interactions will transmit far further than required for information transfer between the individuals directly involved, suggesting that these signals have been designed to be received by other, more distant, individuals. Here we consider the potential for receivers in communication networks to gather information, one aspect of which has been termed eavesdropping. We show that male Betta splendens monitor aggressive interactions between neighbouring conspecifics and use the information on relative fighting ability in subsequent aggressive interactions with the males they have observed.     

Calling under pressure: short-finned pilot whales make social calls during deep foraging dives

Toothed whales rely on sound to echolocate prey and communicate with conspecifics, but little is known about how extreme pressure affects pneumatic sound production in deep-diving species with a limited air supply. The short-finned pilot whale (Globicephala macrorhynchus) is a highly social species among the deep-diving toothed whales, in which individuals socialize at the surface but leave their social group in pursuit of prey at depths of up to 1000 m. To investigate if these animals communicate acoustically at depth and test whether hydrostatic pressure affects communication signals, acoustic DTAGs logging sound, depth and orientation were attached to 12 pilot whales. Tagged whales produced tonal calls during deep foraging dives at depths of up to 800 m. Mean call output and duration decreased with depth despite the increased distance to conspecifics at the surface. This shows that the energy content of calls is lower at depths where lungs are collapsed and where the air volume available for sound generation is limited by ambient pressure. Frequency content was unaffected, providing a possible cue for group or species identification of diving whales. Social calls may be important to maintain social ties for foraging animals, but may be impacted adversely by vessel noise.     

Social Organization of a Maternity Group in the Noctule Bat,Nyctalus noctula (Chiroptera: Vespertilionidae)

Social organization of a captive group of noctule bats, N. noctula, was studied by frequent censuses of bats at roost sites during one summer season. Numerous nonrandom associations as measured by information indices of similarity (Kullback 1959; Semkin 1972; Zakharov et al. 1987) were found between related and unrelated individuals. The social group structure revealed by multidimensional scaling analysis was affected first of all by the history of group formation, and also by bat age and sex. Spatial bonds were in general stronger between related than unrelated bats. However, nearly all closest associations observed were formed by at best distantly related bats; family membership influenced the socio-spatial positions of noctules far less than the above-mentioned variables did. It is suggested that emergence and persistence of nonrandom associations is mainly due to individual attainment of a certain level of comfort in company of familiar conspecifics whose behaviour is predictable, and thus reduction of aggression within a group. Other benefits of stable associations would be derived from this primary function.     

Eavesdropping by Bats: The Influence of Echolocation Call Design and Foraging Strategy

We used playback presentations to free-flying bats of 3 species to assess the influence of echolocation call design and foraging strategy on the role of echolocation calls in communication. Near feeding sites over water, Myotis lucifugus and M. yumanensis responded positively only to echolocation calls of conspecifics. Near roosts, these bats did not respond before young of the year became volant, and after this responded to presentations of echolocation calls of similar and dissimilar design. At feeding sites Lasiurus borealis responded only to echolocation calls of conspecifics and particularly to “feeding buzzes”. While Myotis, particularly subadults, appear to use the echolocation calls of conspecifics to locate feeding sites, L. borealis appears to use the calls of a foraging neighbour attacking prey to identify opportunities for ‘stealing’ food.     

Selective Eavesdropping Behaviour in Three Neotropical Bat Species

Knowledge of interspecies information transfer in mammals is scarce compared with other taxa. We investigated whether eavesdropping on echolocation calls of bats may be used by sympatric bats with similar feeding ecology. We performed playback experiments with three free‐ranging neotropical bat species, broadcasting search phase calls or feeding buzzes of conspecifics and heterospecifics belonging either to the same or to another bat family. Both the greater fishing bat Noctilio leporinus and the lesser bulldog bat Noctilio albiventris (Noctilionidae) reacted with repeated approaches in response to playbacks of search phase calls and feeding buzzes from conspecifics and also to congeneric feeding buzzes. Noctilio leporinus also were attracted by search phase calls from its sister species N. albiventris. In contrast, the sac‐winged bat Saccopteryx bilineata (Emballonuridae) did not react to any playback sequences presented. Our results support the existence of eavesdropping behaviour for both species of Noctilio. We suggest that information transfer via eavesdropping may depend mainly on species‐specific traits, including foraging style and social behaviour (territoriality, group foraging), and on distribution and density of prey. Call design had only a minor influence on the reaction.     

Experimental evidence for group hunting via eavesdropping in echolocating bats

Group foraging has been suggested as an important factor for the evolution of sociality. However, visual cues are predominantly used to gain information about group members'' foraging success in diurnally foraging animals such as birds, where group foraging has been studied most intensively. By contrast, nocturnal animals, such as bats, would have to rely on other cues or signals to coordinate foraging. We investigated the role of echolocation calls as inadvertently produced cues for social foraging in the insectivorous bat Noctilio albiventris. Females of this species live in small groups, forage over water bodies for swarming insects and have an extremely short daily activity period. We predicted and confirmed that (i) free-ranging bats are attracted by playbacks of echolocation calls produced during prey capture, and that (ii) bats of the same social unit forage together to benefit from passive information transfer via the change in group members'' echolocation calls upon finding prey. Network analysis of high-resolution automated radio telemetry confirmed that group members flew within the predicted maximum hearing distance 94±6 per cent of the time. Thus, echolocation calls also serve as intraspecific communication cues. Sociality appears to allow for more effective group foraging strategies via eavesdropping on acoustical cues of group members in nocturnal mammals.     

Sound amplification by means of a horn-like roosting structure in Spix's disc-winged bat

While sound is a signal modality widely used by many animals, it is very susceptible to attenuation, hampering effective long-distance communication. A strategy to minimize sound attenuation that has been historically used by humans is to use acoustic horns; to date, no other animal is known to use a similar structure to increase sound intensity. Here, we describe how the use of a roosting structure that resembles an acoustic horn (the tapered tubes that form when new leaves of plants such as Heliconia or Calathea species start to unfurl) increases sound amplification of the incoming and outgoing social calls used by Spix''s disc-winged bat (Thyroptera tricolor) to locate roosts and group members. Our results indicate that incoming calls are significantly amplified as a result of sound waves being increasingly compressed as they move into the narrow end of the leaf. Outgoing calls were faintly amplified, probably as a result of increased sound directionality. Both types of call, however, experienced significant sound distortion, which might explain the patterns of signal recognition previously observed in behavioural experiments. Our study provides the first evidence of the potential role that a roost can play in facilitating acoustic communication in bats.     

Evidence for social role in a dolphin social network

Social animals have to take into consideration the behaviour of conspecifics when making decisions to go by their daily lives. These decisions affect their fitness and there is therefore an evolutionary pressure to try making the right choices. In many instances individuals will make their own choices and the behaviour of the group will be a democratic integration of everyone’s decision. However, in some instances it can be advantageous to follow the choice of a few individuals in the group if they have more information regarding the situation that has arisen. Here I provide early evidence that decisions about shifts in activity states in a population of bottlenose dolphin follow such a decision-making process. This unshared consensus is mediated by a non-vocal signal, which can be communicated globally within the dolphin school. These signals are emitted by individuals that tend to have more information about the behaviour of potential competitors because of their position in the social network. I hypothesise that this decision-making process emerged from the social structure of the population and the need to maintain mixed-sex schools.     

Effects of Eavesdropping on Subsequent Signalling Behaviours in Male Canaries

Signalling interactions could provide information for an observing third party. This behaviour has been labelled as eavesdropping. Studies on eavesdropping in birds have concerned only few species and have mainly been conducted in the wild. Our experiment was designed to evaluate the effects of eavesdropping on subsequent interactions in male canaries in a controlled laboratory context. The experiment had two stages: a presentation stage and a test stage. During the presentation stage, subjects heard three different interaction types: an alternating interaction, an overlapping interaction or two song sequences presented separately one after the other, i.e. without interaction. Then during the test stage, subjects were allowed to listen to the songs previously heard separately. We noted calls emitted by subjects during the two stages. During the presentation stage, responses of male canaries did not differ according to the type of interaction they could hear. During the test stage, we found a clear effect of the song status on the calls emitted by subjects. They emitted less calls during the songs of the winner than during all other songs. Surprisingly, subjects also produced intermediate responses by emitting fewer calls during the second song previously heard during the presentation phase, and during the song of the looser when compared to the three other songs. Our results show that male canaries obtain information on the relative threat from an overlapping interaction whereas an alternating interaction does not seem to provide any kind of relative information on singers' status. In following encounters, the higher the potential threat of a singer was, the less the subjects emitted calls, probably to avoid the more serious rival. This inhibiting effect is discussed.     

Social communication in bats

Bats represent one of the most diverse mammalian orders, not only in terms of species numbers, but also in their ecology and life histories. Many species are known to use ephemeral and/or unpredictable resources that require substantial investment to find and defend, and also engage in social interactions, thus requiring significant levels of social coordination. To accomplish these tasks, bats must be able to communicate; there is now substantial evidence that demonstrates the complexity of bat communication and the varied ways in which bats solve some of the problems associated with their unique life histories. However, while the study of communication in bats is rapidly growing, it still lags behind other taxa. Here we provide a comprehensive overview of communication in bats, from the reasons why they communicate to the diversity and application of different signal modalities. The most widespread form of communication is the transmission of a signaller's characteristics, such as species identity, sex, individual identity, group membership, social status and body condition, and because many species of bats can rely little on vision due to their nocturnal lifestyles, it is assumed that sound and olfaction are particularly important signalling modes. For example, research suggests that secretions from specialized glands, often in combination with urine and saliva, are responsible for species recognition in several species. These olfactory signals may also convey information about sex and colony membership. Olfaction may be used in combination with sound, particularly in species that emit constant frequency (CF) echolocation calls, to recognize conspecifics from heterospecifics, yet their simple structure and high frequency do not allow much information of individual identity to be conveyed over long distances. By contrast, social calls may encode a larger number of cues of individual identity, and their lower frequencies increase their range of detection. Social calls are also known to deter predators, repel competitors from foraging patches, attract group mates to roost sites, coordinate foraging activities, and are used during courtship. In addition to sound, visual displays such as wing flapping or hovering may be used during courtship, and swarming around roost sites may serve as a visual cue of roost location. However, visual communication in bats still remains a poorly studied signal modality. Finally, the most common form of tactile communication known in bats is social grooming, which may be used to signal reproductive condition, but also to facilitate and strengthen cooperative interactions. Overall, this review demonstrates the rapid advances made in the study of bat social communication during recent years, and also identifies topics that require further study, particularly those that may allow us to understand adaptation to rapidly changing environmental conditions.