Adaptive auditory risk assessment in the dogbane tiger moth when pursued by bats

Moths and butterflies flying in search of mates risk detection by numerous aerial predators; under the cover of night, the greatest threat will often be from insectivorous bats. During such encounters, the toxic dogbane tiger moth, Cycnia tenera uses the received intensity, duration and emission pattern of the bat''s echolocation calls to determine when, and how many, defensive ultrasonic clicks to produce in return. These clicks, which constitute an acoustic startle response, act as warning signals against bats in flight. Using an integrated test of stimulus generalization and dishabituation, here we show that C. tenera is able to discriminate between the echolocation calls characteristic of a bat that has only just detected it versus those of a bat actively in pursuit of it. We also show that C. tenera habituates more profoundly to the former stimulus train (‘early attack’) than to the latter (‘late attack’), even though it was initially equally responsive to both stimuli. Matched sensory and behavioural data indicate that reduced responsiveness reflects habituation and is not merely attributable to sensory adaptation or motor fatigue. In search of mates in the face of bats, C. tenera''s ability to discriminate between attacking bats representing different levels of risk, and to habituate less so to those most dangerous, should function as an adaptive cost–benefit trade-off mechanism in nature.     

Dynamics of jamming avoidance in echolocating bats

Animals using active sensing systems such as echolocation or electrolocation may experience interference from the signals of neighbouring conspecifics, which can be offset by a jamming avoidance response (JAR). Here, we report JAR in one echolocating bat (Tadarida teniotis: Molossidae) but not in another (Taphozous perforatus: Emballonuridae) when both flew and foraged with conspecifics. In T. teniotis, JAR consisted of shifts in the dominant frequencies of echolocation calls, enhancing differences among individuals. Larger spectral overlap of signals elicited stronger JAR. Tadarida teniotis showed two types of JAR: (i) for distant conspecifics: a symmetric JAR, with lower- and higher-frequency bats shifting their frequencies downwards and upwards, respectively, on average by the same amount; and (ii) for closer conspecifics: an asymmetric JAR, with only the upper-frequency bat shifting its frequency upwards. In comparison, 'wave-type' weakly electric fishes also shift frequencies of discharges in a JAR, but unlike T. teniotis, the shifts are either symmetric in some species or asymmetric in others. We hypothesize that symmetric JAR in T. teniotis serves to avoid jamming and improve echolocation, whereas asymmetric JAR may aid communication by helping to identify and locate conspecifics, thus minimizing chances of mid-air collisions.     

Context-dependent effects of noise on echolocation pulse characteristics in free-tailed bats

Background noise evokes a similar suite of adaptations in the acoustic structure of communication calls across a diverse range of vertebrates. Echolocating bats may have evolved specialized vocal strategies for echolocating in noise, but also seem to exhibit generic vertebrate responses such as the ubiquitous Lombard response. We wondered how bats balance generic and echolocation-specific vocal responses to noise. To address this question, we first characterized the vocal responses of flying free-tailed bats (Tadarida brasiliensis) to broadband noises varying in amplitude. Secondly, we measured the bats’ responses to band-limited noises that varied in the extent of overlap with their echolocation pulse bandwidth. We hypothesized that the bats’ generic responses to noise would be graded proportionally with noise amplitude, total bandwidth and frequency content, and consequently that more selective responses to band-limited noise such as the jamming avoidance response could be explained by a linear decomposition of the response to broadband noise. Instead, the results showed that both the nature and the magnitude of the vocal responses varied with the acoustic structure of the outgoing pulse as well as non-linearly with noise parameters. We conclude that free-tailed bats utilize separate generic and specialized vocal responses to noise in a context-dependent fashion.     

Can pipistrelles, Pipistrellus pipistrellus (Schreber, 1774) and Pipistrellus pygmaeus (Leach, 1825), foraging in a group, change parameters of their signals?

Echolocation behaviour and the structure of calls of Pipistrellus pygmaeus and Pipistrellus pipistrellus were studied by using a time expansion bat detector. Echolocation signals were recorded in the field in south-eastern Moravia and northern Bohemia (Czech Republic) and in an ad hoc experimental laboratory. For each of the species, multivariate analysis of variance (MANOVA) indicated significant differences in calls produced inside the experimental room and in the open. Paired t -tests and MANOVA were also used to reveal influences of interindividual contacts in each of the cryptic species on the spectral patterns of call variables. Differences were found in the spectral variables of echolocation calls of an individual flying in the room alone and in a group of conspecifics. The possibility that bats use their flexibility to avoid mutual disturbances of echolocation calls was tested. We found that bats flying in a group modify the parameters of their echolocation signals according to the presence of other individuals of the same species. These differences can indicate jamming avoidance and recognition of own echoes. However, they did not change the parameters if individuals of another species were present. Social calls are more numerous when bats fly in a mixed-species group than in a monospecific group.     

Airport noise disturbs foraging behavior of Japanese pipistrelle bats

The expansion of anthropogenic noise poses an emerging threat to the survival and reproductive success of various organisms. Previous investigations have focused on the detrimental effects of anthropogenic noise on the foraging behavior in some terrestrial and aquatic animals. Nevertheless, the role of airport noise in impairing foraging activities of most wild animals has been neglected. Here, we aimed to assess whether foraging behavior in free‐living Japanese pipistrelle bats (Pipistrellus abramus) can be disturbed by airport noise. We used audio recording to monitor foraging activities of bats at 11 sites around the runway of a municipal airport. We quantified noise level and spectra, aircraft activity, habitat type, nightly temperature, wind speed, and moon phase for each site. The analysis revealed that noise level and aircraft activity were significant negative predictors for the number of bat passes and feeding buzzes around the runway, even after controlling for the effects of other environmental factors. There was no marked spectral overlap between bat echolocation pulses and airport noise in the presence and absence of low‐flying aircraft. The spectro‐temporal parameters of echolocation vocalizations emitted by bats were dependent on noise level, aircraft activity, and habitat type. These results provide correlative evidence that airport noise can reduce foraging activities of wild pipistrelle bats. Our findings add to the current knowledge of adverse impacts of airport noise on foraging bats in artificial ecosystems and provide a basis for further research on the mechanisms behind noise pollution near airports.     

Rapid jamming avoidance in biosonar

The sonar systems of bats and dolphins are in many ways superior to man-made sonar and radar systems, and considerable effort has been devoted to understanding the signal-processing strategies underlying these capabilities. A major feature determining the efficiency of sonar systems is the sensitivity to noise and jamming signals. Previous studies indicated that echolocating bats may adjust their signal structure to avoid jamming ('jamming avoidance response'; JAR). However, these studies relied on behavioural correlations and not controlled experiments. Here, we provide the first experimental evidence for JAR in bats. We presented bats (Tadarida brasiliensis) with 'playback stimuli' consisting of recorded echolocation calls at one of six frequencies. The bats exhibited a JAR by shifting their call frequency away from the presented playback frequency. When the approaching bats were challenged by an abrupt change in the playback stimulus, they responded by shifting their call frequencies upwards, away from the playback. Interestingly, even bats initially calling below the playback's frequency shifted their frequencies upwards, 'jumping' over the playback frequency. These spectral shifts in the bats' calls occurred often within less than 200 ms, in the first echolocation call emitted after the stimulus switch-suggesting that rapid jamming avoidance is important for the bat.     

菲菊头蝠回声定位声波频率的性二态有利于性别识别

许多动物的叫声频率呈现性二态现象。蝙蝠夜间活动,主要利用声音信号导航空间、追踪猎物、传递交流信息。本研究选择成体菲菊头蝠作为研究对象,检验回声定位声波频率性二态是否有利于性别识别。研究发现,菲菊头蝠回声定位声波频率参数具有显著性别差异。播放白噪音、雄性回声定位声波及雌性回声定位声波期间,实验个体的反应叫声数量依次递减。播放白噪音、雌性回声定位声波及雄性回声定位声波后,实验个体的反应叫声数量依次递增。白噪音诱导反应叫声强度高于回声定位声波诱导反应叫声强度。研究结果表明,菲菊头蝠回声定位声波的频率参数编码发声者性别信息,有利于种群内部的性别识别。本研究暗示,回声定位声波可能在蝙蝠配偶选择中扮演一定作用。     

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.     

Different Auditory Feedback Control for Echolocation and Communication in Horseshoe Bats

Auditory feedback from the animal''s own voice is essential during bat echolocation: to optimize signal detection, bats continuously adjust various call parameters in response to changing echo signals. Auditory feedback seems also necessary for controlling many bat communication calls, although it remains unclear how auditory feedback control differs in echolocation and communication. We tackled this question by analyzing echolocation and communication in greater horseshoe bats, whose echolocation pulses are dominated by a constant frequency component that matches the frequency range they hear best. To maintain echoes within this “auditory fovea”, horseshoe bats constantly adjust their echolocation call frequency depending on the frequency of the returning echo signal. This Doppler-shift compensation (DSC) behavior represents one of the most precise forms of sensory-motor feedback known. We examined the variability of echolocation pulses emitted at rest (resting frequencies, RFs) and one type of communication signal which resembles an echolocation pulse but is much shorter (short constant frequency communication calls, SCFs) and produced only during social interactions. We found that while RFs varied from day to day, corroborating earlier studies in other constant frequency bats, SCF-frequencies remained unchanged. In addition, RFs overlapped for some bats whereas SCF-frequencies were always distinctly different. This indicates that auditory feedback during echolocation changed with varying RFs but remained constant or may have been absent during emission of SCF calls for communication. This fundamentally different feedback mechanism for echolocation and communication may have enabled these bats to use SCF calls for individual recognition whereas they adjusted RF calls to accommodate the daily shifts of their auditory fovea.     

Female big brown bats, Eptesicus fuscus, recognize sex from a caller's echolocation signals

The echolocation calls of bats function in prey capture and navigation but are not commonly regarded as communicative signals. However, because bats' echolocation calls show patterns of variability, they may transmit information about a bat, such as its age, individual identity or sex. For echolocation calls to function in this manner, variation in calls must be reliably linked to the characteristics of the bat, as has been shown in a number of studies. However, few studies have asked whether bats respond to this variation. We tested whether female big brown bats can identify the sex of an unfamiliar bat from playbacks of its echolocation calls. Playback consisted of a 30-s preplayback period, a 60-s playback period of either male or female echolocation calls, and a 30-s postplayback period. In the playback and postplayback periods the vocalization rates of female bats changed significantly relative to the preplayback period depending on the sex of the playback stimulus, indicating that they could determine sex from the echolocation calls. These findings support the possibility that echolocation calls play a role in communication in big brown bats.     

Understanding signal design during the pursuit of aerial insects by echolocating bats: tools and applications

Bats are among the few predators that can exploit the large quantities of aerial insects active at night. They do this by using echolocation to detect, localize, and classify targets in the dark. Echolocation calls are shaped by natural selection to match ecological challenges. For example, bats flying in open habitats typically emit calls of long duration, with long pulse intervals, shallow frequency modulation, and containing low frequencies-all these are adaptations for long-range detection. As obstacles or prey are approached, call structure changes in predictable ways for several reasons: calls become shorter, thereby reducing overlap between pulse and echo, and calls change in shape in ways that minimize localization errors. At the same time, such changes are believed to support recognition of objects. Echolocation and flight are closely synchronized: we have monitored both features simultaneously by using stereo photogrammetry and videogrammetry, and by acoustic tracking of flight paths. These methods have allowed us to quantify the intensity of signals used by free-living bats, and illustrate systematic changes in signal design in relation to obstacle proximity. We show how signals emitted by aerial feeding bats can be among the most intense airborne sounds in nature. Wideband ambiguity functions developed in the processing of signals produce two-dimensional functions showing trade-offs between resolution of time and velocity, and illustrate costs and benefits associated with Doppler sensitivity and range resolution in echolocation. Remarkably, bats that emit broadband calls can adjust signal design so that Doppler-related overestimation of range compensates for underestimation of range caused by the bat's movement in flight. We show the potential of our methods for understanding interactions between echolocating bats and those prey that have evolved ears that detect bat calls.     

Ethanol ingestion affects flight performance and echolocation in Egyptian fruit bats

Ethanol, a potential toxin for vertebrates, is present in all fleshy fruits and its content increases as the fruit ripens. Previously, we found that the marginal value of food for Egyptian fruit bats, Rousettus aegyptiacus, decreases when its ethanol content exceeds 1%. Therefore, we hypothesized that, if ingested, food containing >1% ethanol is toxic to these bats, probably causing inebriation that will affect flight and echolocation skills. We tested this hypothesis by flying Egyptian fruit bats in an indoor corridor and found that after ingesting ethanol-rich food bats flew significantly slower than when fed ethanol-free food. Also, the ingestion of ethanol significantly affected several variables of the bats’ echolocation calls and behavior. We concluded that ethanol can be toxic to fruit bats; not only does it reduce the marginal value of food, but it also has negative physiological effects on their ability to fly competently and on their calling ability.     

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.     

Tiger moths and the threat of bats: decision-making based on the activity of a single sensory neuron

Echolocating bats and eared moths are a model system of predator–prey interaction within an almost exclusively auditory world. Through selective pressures from aerial-hawking bats, noctuoid moths have evolved simple ears that contain one to two auditory neurons and function to detect bat echolocation calls and initiate defensive flight behaviours. Among these moths, some chemically defended and mimetic tiger moths also produce ultrasonic clicks in response to bat echolocation calls; these defensive signals are effective warning signals and may interfere with bats'' ability to process echoic information. Here, we demonstrate that the activity of a single auditory neuron (the A1 cell) provides sufficient information for the toxic dogbane tiger moth, Cycnia tenera, to decide when to initiate defensive sound production in the face of bats. Thus, despite previous suggestions to the contrary, these moths'' only other auditory neuron, the less sensitive A2 cell, is not necessary for initiating sound production. However, we found a positive linear relationship between combined A1 and A2 activity and the number of clicks the dogbane tiger moth produces.     

‘Compromise’ in Echolocation Calls between Different Colonies of the Intermediate Leaf-Nosed Bat (Hipposideros larvatus)

Each animal population has its own acoustic signature which facilitates identification, communication and reproduction. The sonar signals of bats can convey social information, such as species identity and contextual information. The goal of this study was to determine whether bats adjust their echolocation call structures to mutually recognize and communicate when they encounter the bats from different colonies. We used the intermediate leaf-nosed bats (Hipposideros larvatus) as a case study to investigate the variations of echolocation calls when bats from one colony were introduced singly into the home cage of a new colony or two bats from different colonies were cohabitated together for one month. Our experiments showed that the single bat individual altered its peak frequency of echolocation calls to approach the call of new colony members and two bats from different colonies adjusted their call frequencies toward each other to a similar frequency after being chronically cohabitated. These results indicate that the ‘compromise’ in echolocation calls might be used to ensure effective mutual communication among bats.     

Echolocation range and wingbeat period match in aerial-hawking bats

Aerial-hawking bats searching the sky for prey face the problem that flight and echolocation exert independent and possibly conflicting influences on call intervals. These bats can only exploit their full echolocation range unambiguously if they emit their next call when all echoes from the preceding call would have arrived. However, not every call interval is equally available. The need to reduce the high energetic costs of echolocation forces aerial-hawking bats to couple call emission to their wingbeat. We compared the wingbeat periods of 11 aerial-hawking bat species with the delays of the last-expected echoes. Acoustic flight-path tracking was employed to measure the source levels (SLs) of echolocation calls in the field. SLs were very high, extending the known range to 133 dB peak equivalent sound pressure level. We calculated the maximum detection distances for insects, larger flying objects and background targets. Wingbeat periods were derived from call intervals. Small and medium-sized bats in fact matched their maximum detection range for insects and larger flying targets to their wingbeat period. The tendency to skip calls correlated with the species' detection range for background targets. We argue that a species' call frequency is at such a pitch that the resulting detection range matches their wingbeat period.     

Bat point counts: A novel sampling method shines light on flying bat communities

Emerging technologies based on the detection of electro‐magnetic energy offer promising opportunities for sampling biodiversity. We exploit their potential by showing here how they can be used in bat point counts—a novel method to sample flying bats—to overcome shortcomings of traditional sampling methods, and to maximize sampling coverage and taxonomic resolution of this elusive taxon with minimal sampling bias. We conducted bat point counts with a sampling rig combining a thermal scope to detect bats, an ultrasound recorder to obtain echolocation calls, and a near‐infrared camera to capture bat morphology. We identified bats with a dedicated identification key combining acoustic and morphological features, and compared bat point counts with the standard bat sampling methods of mist‐netting and automated ultrasound recording in three oil palm plantation sites in Indonesia, over nine survey nights. Based on rarefaction and extrapolation sampling curves, bat point counts were similarly effective but more time‐efficient than the established methods for sampling the oil palm species pool in our study. Point counts sampled species that tend to avoid nets and those that are not echolocating, and thus cannot be detected acoustically. We identified some bat sonotypes with near‐infrared imagery, and bat point counts revealed strong sampling biases in previous studies using capture‐based methods, suggesting similar biases in other regions might exist. Our method should be tested in a wider range of habitats and regions to assess its performance. However, while capture‐based methods allow to identify bats with absolute and internal morphometry, and unattended ultrasound recorders can effectively sample echolocating bats, bat point counts are a promising, non‐invasive, and potentially competitive new tool for sampling all flying bats without bias and observing their behavior in the wild.     

环境噪声对蝙蝠回声定位叫声及飞行活动的影响

环境噪声影响动物的活动及其叫声特性,已成为动物面对的一种重要选择压力。为应对噪声的干扰,多数动物类群会远离噪声区域和改变其叫声的频谱时间结构,如延长叫声持续时间、提高叫声频率等,但有些动物的活动和叫声频谱时间结构并不受环境噪声的影响。本研究在自然条件下,研究不同环境噪声强度对蝙蝠活动和回声定位声波的影响。选取噪声强度有差异的12个样点,分别录制各样点大卫鼠耳蝠、西南鼠耳蝠、亚洲长翼蝠及未知蝙蝠的回声定位声波,分析其持续时间、起始频率、峰频、终止频率和带宽,统计蝙蝠通过次数。回归分析结果显示：环境噪声强度与大卫鼠耳蝠、西南鼠耳蝠、亚洲长翼蝠及未知蝙蝠的活动无显著相关性P > 0.05）,与回声定位声波的脉冲持续时间、起始频率、峰频、终止频率及带宽均不显著相关（P > 0.05）。暗示低频低强度（< 20 kHz, < 67.5 dB）的环境噪声可能对高频回声定位蝙蝠的叫声及活动没有显著影响。     

Correlated evolution between hearing sensitivity and social calls in bats

Echolocating bats are auditory specialists, with exquisite hearing that spans several octaves. In the ultrasonic range, bat audiograms typically show highest sensitivity in the spectral region of their species-specific echolocation calls. Well-developed hearing in the audible range has been commonly attributed to a need to detect sounds produced by prey. However, bat pups often emit isolation calls with low-frequency components that facilitate mother-young reunions. In this study, we examine whether low-frequency hearing in bats exhibits correlated evolution with (i) body size; (ii) high-frequency hearing sensitivity or (iii) pup isolation call frequency. Using published audiograms, we found that low-frequency hearing sensitivity is not dependent on body size but is related to high-frequency hearing. After controlling for high-frequency hearing, we found that low-frequency hearing exhibits correlated evolution with isolation call frequency. We infer that detection and discrimination of isolation calls have favoured enhanced low-frequency hearing because accurate parental investment is critical: bats have low reproductive rates, non-volant altricial young and must often identify their pups within large crèches.     

Flying bats use serial sampling to locate odour sources

Olfactory tracking generally sacrifices speed for sensitivity, but some fast-moving animals appear surprisingly efficient at foraging by smell. Here, we analysed the olfactory tracking strategies of flying bats foraging for fruit. Fruit- and nectar-feeding bats use odour cues to find food despite the sensory challenges derived from fast flight speeds and echolocation. We trained Jamaican fruit-eating bats (Artibeus jamaicensis) to locate an odour reward and reconstructed their flight paths in three-dimensional space. Results confirmed that bats relied upon olfactory cues to locate a reward. Flight paths revealed a combination of odour- and memory-guided search strategies. During ‘inspection flights’, bats significantly reduced flight speeds and flew within approximately 6 cm of possible targets to evaluate the presence or absence of the odour cue. This behaviour combined with echolocation explains how bats maximize foraging efficiency while compensating for trade-offs associated with olfactory detection and locomotion.