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.     

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.     

‘No cost of echolocation for flying bats’ revisited

Echolocation is energetically costly for resting bats, but previous experiments suggested echolocation to come at no costs for flying bats. Yet, previous studies did not investigate the relationship between echolocation, flight speed, aerial manoeuvres and metabolism. We re-evaluated the 'no-cost' hypothesis, by quantifying the echolocation pulse rate, the number of aerial manoeuvres (landings and U-turns), and the costs of transport in the 5-g insectivorous bat Rhogeessa io (Vespertilionidae). On average, bats (n = 15) travelled at 1.76 ± 0.36 m s?1 and performed 11.2 ± 6.1 U-turns and 2.8 ± 2.9 ground landings when flying in an octagonal flight cage. Bats made more U-turns with decreasing wing loading (body weight divided by wing area). At flight, bats emitted 19.7 ± 2.7 echolocation pulses s?1 (range 15.3-25.8 pulses s?1), and metabolic rate averaged 2.84 ± 0.95 ml CO? min?1, which was more than 16 times higher than at rest. Bats did not echolocate while not engaged in flight. Costs of transport were not related to the rate of echolocation pulse emission or the number of U-turns, but increased with increasing number of landings; probably as a consequence of slower travel speed when staying briefly on ground. Metabolic power of flight was lower than predicted for R. io under the assumption that energetic costs of echolocation call production is additive to the aerodynamic costs of flight. Results of our experiment are consistent with the notion that echolocation does not add large energetic costs to the aerodynamic power requirements of flight in bats.     

Echolocation calls produced by Kuhl's pipistrelles in different flight situations

Flexibility in the echolocation call structure of bats can improve their performances, because, in some situations, some signal designs are better than others. Hence, at least some bats should adjust their echolocation calls according to the setting in which they are operating but also to the specific task at hand, that is their behavioral intention. We studied variation in the echolocation calls of Pipistrellus kuhlii emitted during four flight situations that were similar in setting but differed in behavioral context: emergence from a roost, commuting to and from foraging sites, foraging and returning to a roost. Echolocation calls produced by P. kuhlii differed significantly according to the flight situation. Call types differed most distinctly between foraging and commuting. We also found a high variance in the emergence calls we recorded, perhaps reflecting pre- and post-takeoff calls. Discriminant function analysis on calls emitted while foraging, commuting or returning to the roost classified the calls to the correct group 73.3% of the time. The differences between bats' echolocation calls in different flight situations might indicate an intrinsic change in the bat's behavior. Recognizing these differences could be crucial when using call variables to identify bat species.     

Prey-Correlated Spectral Changes in Echolocation Sounds of the Indian False Vampire Megaderma lyra

False Vampires ( Megaderma lyra ) are gleaning bats which emit brief (1 ms) and faint echolocation signals consisting of four harmonics of a shallow frequency downward modulated fundamental (27–19 kHz). The complete signal spans a frequency range from 100 to 19 kHz. In sound recordings from three experimental animals we show that Megaderma lyra shifts the dominant frequency in the echolocation signals in relation to the type of prey offered and to flight style. During roaming flights the mean peak frequency was 63.2 ± 9 kHz (third harmonic). In prey catching flights, peak frequencies were shifted into the fourth harmonic. In flights towards a dish of crawling mealworms, mean peak frequency was raised to 91.2 ± 3.3 kHz. When the bats flew towards living mice the dominant frequency was further increased to 99.8 ± 5.2 kHz, and the second and third harmonic were at least 10 dB fainter or no longer recordable. The additional frequency shift when flying towards mice was not only a consequence of the dominance of the fourth harmonic but also of an additional rise of the fundamental harmonic by nearly 2 kHz. These prey-correlated frequency shifts in echolocation calls showed little variation between the three experimental animals and were reproducible over time. They occurred at or even before take-off of the bats. This is the first report of target-correlated transient adaptations in echolocation calls of any bat species.     

Flight performance, foraging tactics and echolocation in the trawling insectivorous bat Myotis adversus (Chiroptera: Vespertilionidae)

The bat Myotis adversus hunts for prey by aerial hawking and by taking prey from the water surface with its feet (trawling). The flight performance and echolocation of this species were studied in Queensland, Australia, and comparisons were made with Myotis daubentoni , a bat filling a similar ecological niche in the Palaearctic Region. The bats foraged in very similar ways, using the same foraging tactics and feeding in similar habitats, yet they were not geometrically similar in shape. The slightly larger Myotis adversus had relatively larger wings than M. daubentoni , conferring a slightly lower wing-loading. Nevertheless, M. adversus flew faster than M. daubentoni during the searching phase of foraging. Myotis daubentoni turned in tighter circles than M. adversus . Both species used short frequency-modulated (FM) echolocation calls of a characteristic sigmoidal structure, and nulls typically observed in the calls were an observational artefact. Myotis adversus also adopted an unusual 'long'FM call while foraging. The relations between echolocation frequencies and body size were explored in male M. adversus . Specialized morphological and acoustic adaptations for prey capture by trawling in insectivorous bats are discussed.     

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.     

Feeding behaviour of the bats Nycteris grandis and Nycteris thebaica (Nycteridae) in captivity

The feeding and hunting behaviour of Nycteris grandis and N. thebaica was observed in captivity at the Sengwa Wildlife Research Area in Zimbabwe in January and February 1982. Both species preferentially selected katydids and beetles over moths, and relied heavily on acoustic stimuli emanating from prey to detect targets. Nycteris grandis readily consumed frogs and bats and appeared not to use the calls of male frogs or the echolocation calls of other bats to locate prey. Both species produced echolocation calls during attacks on prey, increasing the rates of pulse repetition as they closed with targets and suggesting the use of echolocation in hunting. The echolocation calls of N. grandis are described along with general observations of the behaviour of both species.     

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.     

The role of prey-generated sounds,vision, and echolocation in prey localization by the African batCardioderma cor (Megadermatidae)

Summary Cardioderma cor responded with head movements and flight toward speakers broadcasting calls of frogs and crickets which contained only sonic frequencies. Unlike the frog-eating bat,Trachops cirrhosus, they did not make contact with the speakers. Prey movements that generated sonic and ultrasonic sounds were both sufficient and necessary for the bats to localize and capture prey. Prey dragged across a glass sheet with a thin layer of water did not generate sounds and bats did not attempt to capture these prey, even with the availability of visual and echolocation cues. There was no evidence for the use of visual cues while hunting; bats did not localize prey more readily in light than darkness. Prey were presented such that their movements initially generated sounds, but then the prey moved onto the water layer of the glass sheet and sounds were eliminated. The bats emitted echolocation signals while hunting in this situation; however, the information from these signals was not utilized. The bats landed at the site that prey last made sound. These results demonstrate the importance of passive hearing for prey localization in this bat, and further suggest that when preygenerated sounds and echolocation signals offer conflicting information the bat's behavior is guided by the former.     

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.     

Molecular diet analysis finds an insectivorous desert bat community dominated by resource sharing despite diverse echolocation and foraging strategies

Interspecific differences in traits can alter the relative niche use of species within the same environment. Bats provide an excellent model to study niche use because they use a wide variety of behavioral, acoustic, and morphological traits that may lead to multi‐species, functional groups. Predatory bats have been classified by their foraging location (edge, clutter, open space), ability to use aerial hawking or substrate gleaning and echolocation call design and flexibility, all of which may dictate their prey use. For example, high frequency, broadband calls do not travel far but offer high object resolution while high intensity, low frequency calls travel further but provide lower resolution. Because these behaviors can be flexible, four behavioral categories have been proposed: (a) gleaning, (b) behaviorally flexible (gleaning and hawking), (c) clutter‐tolerant hawking, and (d) open space hawking. Many recent studies of diet in bats use molecular tools to identify prey but mainly focus on one or two species in isolation; few studies provide evidence for substantial differences in prey use despite the many behavioral, acoustic, and morphological differences. Here, we analyze the diet of 17 sympatric species in the Chihuahuan desert and test the hypothesis that peak echolocation frequency and behavioral categories are linked to differences in diet. We find no significant correlation between dietary richness and echolocation peak frequency though it spanned close to 100 kHz across species. Our data, however, suggest that bats which use both gleaning and hawking strategies have the broadest diets and are most differentiated from clutter‐tolerant aerial hawking species.     

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.     

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.     

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.     

Substrate-gleaning versus aerial-hawking: plasticity in the foraging and echolocation behaviour of the long-eared bat,Myotis evotis

The foraging and echolocation behaviour of Myotis evotis was investigated during substrate-gleaning and aerial-hawking attacks. Bats gleaned moths from both the ground and a bark-covered trellis, however, they were equally adept at capturing flying moths. The calls emitted by M. evotis during substrate-gleaning sequences were short, broadband, and frequency-modulated (FM). Three behavioural phases were identified: search, hover, and attack. Gleaning search calls were significantly longer in duration, lower in highest frequency, and larger in bandwidth than hover/attack calls. Calls were detected in only 68% of gleaning sequences, and when they were emitted, bats ceased calling 200 ms before attacking. Terminal feeding buzzes, the rapid increase in pulse repetition rate associated with an attempted prey capture, were never recorded during gleaning attacks. The echolocation calls uttered by M. evotis during aerial-hawking foraging sequences were also short duration, high frequency, FM calls. Two distinct acoustic phases were identified: approach and terminal. Approach calls were significantly different from terminal calls in all variables measured. Calls were detected in 100% of aerial-hawking attacks and terminal feeding buzzes were invariably produced. Gleaning hover/attack calls were spectrally similar to aerial approach calls, but were shorter in duration and emitted at a significantly lower (but constant) repetition rate than aerial signals. Although the foraging environment (flight cage contents) remained unchanged between tasks (substrate-gleaning vs. aerial-hawking), bats emitted significantly lower amplitude calls while gleaning. We conclude that M. evotis adjusts its echolocation behaviour to meet the perceptual demands (acoustical constraints) imposed by each foraging situations.Abbreviations BW bandwidth - CF constant frequency - dB SPL decibels sound pressure level - FM frequency modulated - HF highest frequency - LF lowest frequency - PF peak frequency Presented at the meeting Acoustic Images in Bat Sonar, a conference on FM echolocation honoring Donald R. Griffin's contributions to experimental biology (June 14–16, Brown University, Providence RI).     

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.     

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。     

Female greater wax moths reduce sexual display behavior in relation to the potential risk of predation by echolocating bats

Female greater wax moths Galleria mellonella display by wing fanning in response to bursts of ultrasonic calls produced bymales. The temporal and spectral characteristics of these callsshow some similarities with the echolocation calls of batsthat emit frequency-modulated (FM) signals. Female G. mellonellatherefore need to distinguish between the attractive signalsof male conspecifics, which may lead to mating opportunities,and similar sounds made by predatory bats. We therefore predictedthat (1) females would display in response to playbacks of male calls; (2) females would not display in response to playbacksof the calls of echolocating bats (we used the calls of Daubenton'sbat Myotis daubentonii as representative of a typical FM echolocatingbat); and (3) when presented with male calls and bat callsduring the same time block, females would display more whenperceived predation risk was lower. We manipulated predationrisk in two ways. First, we varied the intensity of bat callsto represent a nearby (high risk) or distant (low risk) bat.Second, we played back calls of bats searching for prey (lowrisk) and attacking prey (high risk). All predictions weresupported, suggesting that female G. mellonella are able todistinguish conspecific male mating calls from bat calls, andthat they modify display rate in relation to predation risk.The mechanism (s) by which the moths separate the calls ofbat and moth must involve temporal cues. Bat and moth signalsdiffer considerably in duration, and differences in durationcould be encoded by the moth's nervous system and used in discrimination.     

Variation in the Sonar of an Aerial-hawking Bat (Eptesicus nilssonii)

Echolocation calls from 10 individually marked female northern bats (Eptesicus nilssonii) were recorded as the bats foraged at three distinct feeding sites (territories) near their maternity roost in southern Sweden (57° N). In addition, recordings of unmarked bats were made in northern Sweden (65° N). The frequency at maximum amplitude of “search phase” echolocation pulses was bimodally distributed, with peaks around 29–30 kHz and 31–32 kHz and was negatively correlated with pulse duration. The frequency at maximum amplitude was related to flight altitude (bats used higher frequencies when they flew near the ground) and also differed among the feeding sites. Hence, much of the variation, probably including regional differences, was behavioural and is interpreted as short term (in the order of s or min) adaptation to current foraging situations. Variation among individual bats, caused by age and size, seemed to be of less importance. Individuals did not use exclusive frequency bands.