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.     

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。     

‘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.     

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.     

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.     

The role of echolocation in the hunting of terrestrial prey – new evidence for an underestimated strategy in the gleaning bat, Megaderma lyra

The observation that gleaning bats detect prey by its noises, together with difficulties in recording their faint sonar calls, have led some authors to conclude that gleaning bats may not use echolocation in certain hunting situations. In particular, it is conjectured that echolocation plays no role in the classification and tracking of prey. In the present study, we show that the gleaning bat, Megaderma lyra, is able to find silent and motionless prey on the ground. The significance of sonar for catching a variety of terrestrial prey is established in a standardized situation. Sonar calls were found to be emitted during all stages, i.e. approach, hovering above the prey, and return to the roost, of every hunting flight. The harmonic pattern of the calls differed significantly between these stages, calls with three or more prominent components prevailing during hovering. Bats identified prey and rejected dummies while hovering above them. During this stage, increased call rates and reduced call durations were found. Echolocation activity during, and the duration of, the hovering phase depended on prey type, in particular on prey movement. The prey-dependent shifts in sonar activity, the broadband call structure with an emphasis on higher harmonics, and a systematic shift of the calls' peak frequencies during hovering, are discussed as adaptations to identifying prey by sonar.     

Bat echolocation calls: adaptation and convergent evolution

Bat echolocation calls provide remarkable examples of 'good design' through evolution by natural selection. Theory developed from acoustics and sonar engineering permits a strong predictive basis for understanding echolocation performance. Call features, such as frequency, bandwidth, duration and pulse interval are all related to ecological niche. Recent technological breakthroughs have aided our understanding of adaptive aspects of call design in free-living bats. Stereo videogrammetry, laser scanning of habitat features and acoustic flight path tracking permit reconstruction of the flight paths of echolocating bats relative to obstacles and prey in nature. These methods show that echolocation calls are among the most intense airborne vocalizations produced by animals. Acoustic tracking has clarified how and why bats vary call structure in relation to flight speed. Bats using broadband echolocation calls adjust call design in a range-dependent manner so that nearby obstacles are localized accurately. Recent phylogenetic analyses based on gene sequences show that particular types of echolocation signals have evolved independently in several lineages of bats. Call design is often influenced more by perceptual challenges imposed by the environment than by phylogeny, and provides excellent examples of convergent evolution. Now that whole genome sequences of bats are imminent, understanding the functional genomics of echolocation will become a major challenge.     

Between-species jamming avoidance in Pipistrelles?

Past studies have reported that bats modify the spectral–temporal features of their vocalizations to avoid interference from the vocalizations of conspecifics (jamming avoidance). We tested for within, and between-species jamming avoidance in two sympatrically occurring species of vespertilionid bats, Pipistrellus pipistrellus and Pipistrellus nathusii. In both species the peak frequencies of the narrowband frequency component from samples of bats flying with conspecifics varied more than those from samples of bats flying alone, indicating intraspecific jamming avoidance. If individuals of the two species were recorded together, we found no reaction of P. nathusii. P. pipistrellus, however, used significantly higher frequencies than when recorded alone. As the narrowband frequency of this species normally overlaps with the frequency modulated (FM) part of P. nathusii calls, this can be interpreted as an interspecific jamming avoidance response.     

Little Brown Bats (Myotis lucifugus) Recognize Individual Identity of Conspecifics Using Sonar Calls

Bats use sonar calls to locate prey and orient in their environment but they may also be used by conspecifics to obtain information about a caller. Statistical analysis of sonar calls provides evidence that variation carries social information about a caller, including individual identity. We hypothesized that little brown bats (Myotis lucifugus) would be able to recognize individuals given the potential fitness benefits of doing so. We performed playback trials using a habituation‐discrimination design to determine whether little brown bats are able to recognize the individual identity of a caller based on variation in their sonar calls. Each subject bat was played the calls of bat A until they habituated (defined as a 50% decrease from the beginning call rate), then the calls of bat B or a new call sequence of bat A (a control, referred to as bat A’) were played. Each subject received a unique pair of playback recordings (bat A and B) from adult female bats from the same colony (but a different colony from the subject) and the order of trials was randomized. The response measures were habituation time (s) and call rate (calls/s). Within a trial, subjects habituated to calls of bat A and transferred this habituation to the bat A’ sequence. In addition, they increased their call rates when played calls of bat B. Comparing between trials, subjects increased their call rate to the calls of bat B to a greater relative extent than to the calls of bat A’. These results provide the first evidence that bats recognize individual identity of conspecifics (as opposed to discrimination of groups), which has implications for the social interactions of bats.     

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.     

Weather conditions determine attenuation and speed of sound: Environmental limitations for monitoring and analyzing bat echolocation

Echolocating bats are regularly studied to investigate auditory‐guided behaviors and as important bioindicators. Bioacoustic monitoring methods based on echolocation calls are increasingly used for risk assessment and to ultimately inform conservation strategies for bats. As echolocation calls transmit through the air at the speed of sound, they undergo changes due to atmospheric and geometric attenuation. Both the speed of sound and atmospheric attenuation, however, are variable and determined by weather conditions, particularly temperature and relative humidity. Changing weather conditions thus cause variation in analyzed call parameters, limiting our ability to detect, and correctly analyze bat calls. Here, I use real‐world weather data to exemplify the effect of varying weather conditions on the acoustic properties of air. I then present atmospheric attenuation and speed of sound for the global range of weather conditions and bat call frequencies to show their relative effects. Atmospheric attenuation is a nonlinear function of call frequency, temperature, relative humidity, and atmospheric pressure. While atmospheric attenuation is strongly positively correlated with call frequency, it is also significantly influenced by temperature and relative humidity in a complex nonlinear fashion. Variable weather conditions thus result in variable and unknown effects on the recorded call, affecting estimates of call frequency and intensity, particularly for high frequencies. Weather‐induced variation in speed of sound reaches up to about ±3%, but is generally much smaller and only relevant for acoustic localization methods of bats. The frequency‐ and weather‐dependent variation in atmospheric attenuation has a threefold effect on bioacoustic monitoring of bats: It limits our capability (1) to monitor bats equally across time, space, and species, (2) to correctly measure frequency parameters of bat echolocation calls, particularly for high frequencies, and (3) to correctly identify bat species in species‐rich assemblies or for sympatric species with similar call designs.     

Ontogenesis of the echolocation system in the rufous horseshoe bat,Rhinolophus rouxi (Audition and vocalization in early postnatal development)

1. The development of vocalization and hearing was studied in Sri Lankan horseshoe bats (Rhinolophus rouxi) during the first postnatal month. The young bats were caught in a nursing colony of rhinolophids in which birth took place within a two week period. 2. The new-born bats emitted isolation calls through the mouth. At the beginning these calls consisted of pure tones with frequencies below 10 kHz (Fig. 1). During the first postnatal week the call frequency increased to about 15 kHz, and the fundamental was augmented by two to four harmonics. No evoked potentials to pure tone stimuli could be elicited in the inferior colliculus of this age group, i.e., auditory processing at the midbrain level was not demonstrable. 3. Evoked potentials were first recorded in the second week, broadly tuned to 15-45 kHz, with a maximum sensitivity between 15-25 kHz. In the course of the second week, however, higher frequencies up to 60 kHz became progressively incorporated into the audiogram (Fig. 3). The fundamental frequency of the multiharmonic isolation calls, emitted strictly through the mouth, increased to about 20 kHz. 4. In the bats' third postnatal week an increased hearing sensitivity (auditory filter) emerged, sharply tuned at frequencies between 57 and 60 kHz (Fig. 4e). The same individuals were also the first to emit long constant frequency echolocation calls through the nostrils (Fig. 4c). The energy of the calls was arranged in harmonic frequency bands with the second harmonic exactly tuned to the auditory filter. These young bats continued to emit isolation calls through the mouth, which were, however, not harmonically related to the echolocation calls (Fig. 4b, d). 5. During the fourth week, both the auditory filter and the matched echolocation pulses (the second harmonic) shifted towards higher frequencies (Fig. 5). During the fifth week the fundamental frequency of the calls was progressively attenuated, and both the second harmonic of the pulses and the auditory filter reached the frequency range typical for adult bats of 73-78 kHz (Fig. 6). 6. The development of audition and vocalization is discussed with regard to possible interactions of both subsystems, and their incorporation into the active orientation system of echolocation.     

降雨噪声对菲菊头蝠出飞行为的影响

降雨噪声属于常见的自然噪声,由雨滴撞击物体表面产生。目前,有关降雨噪声对动物的潜在影响被普遍忽视。回声定位蝙蝠主要利用声信号在黑暗环境导航空间、探测猎物及社群交流,是开展降雨噪声影响研究的理想类群。本研究选择菲菊头蝠 (Rhinolophus pusillus)作为研究对象,检验降雨噪声是否影响蝙蝠出飞行为。我们在集群栖息地外,播放强降雨噪声、空白对照和种内回声定位声波,开展野外回放实验。利用单因素方差分析及其事后检验,评价菲菊头蝠对不同回放刺激的反应差异。研究发现,相比空白对照,强降雨噪声导致菲菊头蝠的通勤数量百分比平均降低2.82倍,回声定位脉冲数量平均减少4.86倍,集群出飞时间延长3.75 min。相比空白对照,同种回声定位声波对菲菊头蝠出飞行为的影响并不显著。研究结果证实强降雨噪声抑制菲菊头蝠的出飞行为。本研究表明,降雨引起 的噪声干扰可能是导致蝙蝠躲避降雨的重要因素,为野生蝙蝠物种保育与管理提供启示。     

Echolocation calls in Central American emballonurid bats: signal design and call frequency alternation

In southern Central America, 10 species of emballonurid bats occur, which are all aerial insectivores: some hunt flying insects preferably away from vegetation in open space, others hunt in edge space near vegetation and one species forages mainly over water. We present a search call design of each species and link signal structure to foraging habitat. All emballonurid bats use a similar type of echolocation call that consists of a central, narrowband component and one or two short, frequency-modulated sweeps. All calls are multi-harmonic, generally with most energy concentrated in the second harmonic. The design of search calls is closely related to habitat type, in particular to distance of clutter. Emballonurid bats foraging in edge space near vegetation and over water used higher frequencies, shorter call durations and shorter pulse intervals compared with species mostly hunting in open, uncluttered habitats. Peak frequency correlated negatively with body size. Regular frequency alternation between subsequent calls was typical in the search sequences of four out of 10 species. We discuss several hypotheses regarding the possible role of this frequency alternation, including species identification and partitioning of acoustic channels. Furthermore, we propose a model of how frequency alternation could increase the maximum detection distance of obstacles by marking search calls with different frequencies.     

Determinants of echolocation call frequency variation in the Formosan lesser horseshoe bat (Rhinolophus monoceros)

The origin and maintenance of intraspecific variation in vocal signals is important for population divergence and speciation. Where vocalizations are transmitted by vertical cultural inheritance, similarity will reflect co-ancestry, and thus vocal divergence should reflect genetic structure. Horseshoe bats are characterized by echolocation calls dominated by a constant frequency component that is partly determined by maternal imprinting. Although previous studies showed that constant frequency calls are also influenced by some non-genetic factors, it is not known how frequency relates to genetic structure. To test this, we related constant frequency variation to genetic and non-genetic variables in the Formosan lesser horseshoe bat (Rhinolophus monoceros). Recordings of bats from across Taiwan revealed that females called at higher frequencies than males; however, we found no effect of environmental or morphological factors on call frequency. By comparison, variation showed clear population structure, with frequencies lower in the centre and east, and higher in the north and south. Within these regions, frequency divergence was directional and correlated with geographical distance, suggesting that call frequencies are subject to cultural drift. However, microsatellite clustering analysis showed that broad differences in constant frequency among populations corresponded to discontinuities in allele frequencies resulting from vicariant events. Our results provide evidence that the processes shaping genetic subdivision have concomitant consequences for divergence in echolocation call frequency.     

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.     

Echolocation behaviour of <Emphasis Type="Italic">Megaderma lyra</Emphasis> during typical orientation situations and while hunting aerial prey: a field study

Bats modify the structure and emission pattern of their calls to cope with the functional constraints of a given echolocation situation. As a consequence, the flexibility in sonar call use affects the potential niche use of a species. The present paper addresses call use in Megaderma lyra, a species with a short, broadband multiharmonic basic call, in typical orientation situations, when emerging from and re-entering a day roost, in cruising flight and when passing through vegetation, and during the pursuit of tethered, flying insects. While call duration and emission rate were adapted to the four orientation situations, call spectral composition was similar in these situations, except that bats emitted calls containing more harmonics when re-entering the roost. These moderate call modifications may be accounted for by the observation that M. lyra stayed close to landscape elements even in open habitats. Although M. lyra is a typical gleaner, all tested bats approached flying insects, guided by sonar calls of significantly decreasing duration and pulse interval, and of increasing sweep rate. Before capture, peak frequency was lowered from call to call. The spontaneous approaches towards flying insects with systematic changes in call pattern suggest regular aerial hunting in this species.     

Plasticity in echolocation calls of <Emphasis Type="Italic">Myotis macrodactylus</Emphasis> (Chiroptera: Vespertilionidae): implications for acoustic identification

Poor knowledge of the intraspecific variability in echolocation calls is recognized as an important limiting factor for the accurate acoustic identification of bats. We studied the echolocation behaviors of an ecologically poorly known bat species, Myotis macrodactylus, while they were commuting in three types of habitats differing significantly in the amount of background clutter, as well as searching for prey above the water surface in a river. Results showed that M. macrodactylus altered their echolocation call structure in the same way during commuting as foraging bats do in relation to the changing level of clutter. With increasing level of clutter, M. macrodactylus generally produced echolocation calls with higher start, end, and peak frequencies; wider bandwidth; and shorter pulse duration. Compared to commuting, bats emitted significantly lower frequency calls with narrower bandwidth while searching for prey. Discriminant function analysis indicated that 79.8% of the calls from the three commuting habitats were correctly grouped, and 87% of the calls were correctly classified to the commuting and foraging contexts. Our finding has implications for those who would identify species by their calls.     

Phase sensitivity in bat sonar revisited

An echolocating bat produces echoes consisting of the convolution of echolocation call and the impulse response (IR) of the ensonified object. A crucial question in animal sonar is whether bats are able to extract this IR from the echo. The bat inner ear generates a frequency representation of call and echo and IR extraction in the frequency domain requires accurate analysis of both magnitude and phase information. Previous studies investigating the phase sensitivity of bats using a jitter paradigm reported a temporal acuity down to 10 ns, suggesting perfect sonar phase representation. In a phantom-target playback experiment, we investigate the perceptual phase sensitivity of the bat Phyllostomus discolor using a novel approach: instead of manipulating IR phase by changing IR delay (jitter paradigm), we randomized IR phase and thus lengthened the IR over time, leaving the magnitude spectrum unchanged. Our results show that phase sensitivity, as reflected in the analysis of signal duration, appears to be much lower than phase sensitivity, as reflected in the analysis of signal onset. The current data indicate that different temporal aspects of sonar processing are encoded with very different temporal resolution and thus an overall claim of “phase sensitivity” as such cannot be maintained.     

Male blue monkeys alarm call in response to danger experienced by others

Male blue monkeys (Cercopithecus mitis stuhlmanni) of Budongo Forest, Uganda, produce two acoustically distinct alarm calls: hacks to crowned eagles (Stephanoaetus coronatus) and pyows to leopards (Panthera pardus) and a range of other disturbances. In playback experiments, males responded to leopard growls exclusively with a series of pyows and to eagle shrieks predominantly with hacks. Responses to playbacks of these alarm call series matched the responses to the corresponding predators, suggesting that the calls conveyed something about the nature of the threat. When responding to a series of hacks, indicating an eagle, males responded predominately with hacks, but produced significantly more calls if their group members were close to the playback stimulus than far away, regardless of their own position. When responding to a series of pyows, indicating a range of disturbances, males responded with pyows, but call rates were independent of the distance of other group members. The results suggest that males took into account the degree of danger experienced by other group members.