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An extension of neo-Darwinism, termed preassembly, states that genetic material required for many complex traits, such as echolocation, was present long before emergence of the traits. Assembly of genes and gene segments had occurred over protracted time-periods within large libraries of non-coding genes. Epigenetic factors ultimately promoted transfers from noncoding to coding genes, leading to abrupt formation of the trait via de novo genes. This preassembly model explains many observations that to this present day still puzzle biologists: formation of super-complexity in the absence of multiple fossil precursors, as with bat echolocation and flowering plants; major genetic and physical alterations occurring in just a few thousand years, as with housecat evolution; lack of precursors preceding lush periods of species expansion, as in the Cambrian explosion; and evolution of costly traits that exceed their need during evolutionary times, as with human intelligence. What follows in this paper is a mechanism that is not meant to supplant neo-Darwinism; instead, preassembly aims to supplement current ideas when complexity issues leave them struggling.

Artificial lights may be altering interactions between bats and moth prey. According to the allotonic frequency hypothesis (AFH), eared moths are generally unavailable as prey for syntonic bats (i.e., bats that use echolocation frequencies between 20 and 50 kHz within the hearing range of eared moths) due to the moths' ability to detect syntonic bat echolocation. Syntonic bats therefore feed mainly on beetles, flies, true bugs, and non-eared moths. The AFH is expected to be violated around lights where eared moths are susceptible to exploitation by syntonic bats because moths' evasive strategies become less effective. The hypothesis has been tested to date almost exclusively in areas with permanent lighting, where the effects of lights on bat diets are confounded with other aspects of human habitat alteration. We undertook diet analysis in areas with short-term, localized artificial lighting to isolate the effects of artificial lighting and determine if syntonic and allotonic bats (i.e., bats that use echolocation frequencies outside the hearing range of eared moths) consumed more moths under conditions of artificial lights than in natural darkness. We found that syntonic bats increased their consumption of moth prey under experimentally lit conditions, likely owing to a reduction in the ability of eared moths to evade the bats. Eared moths may increase in diets of generalist syntonic bats foraging around artificial light sources, as opposed to allotonic species and syntonic species with a more specialized diet.

Understanding the evolutionary origins of communication signals requires careful study of multiple species within a known phylogenetic framework. Most cricket species produce low-frequency calls for mate attraction, whereas they startle to high-frequency sounds similar to bat echolocation. Male crickets in the tribe Lebinthini produce high-frequency calls, to which females reply with vibrational signals. This novel communication system likely evolved by male sensory exploitation of acoustic startle to high-frequency sounds in females. This behavior was previously described for the Lebinthini from Asia. Here we demonstrate that this novel communication system is found in a Neotropical species, Ponca hebardi, and is therefore likely shared by the whole tribe Lebinthini, dating the origin of this behavior to coincide with the origin of echolocation in bats. Furthermore, we document male duets involving both acoustic and vibratory signals not previously described in crickets, and we tentatively interpret it as competitive masking between males.

Predation on swarms of prey, especially using visual information, has drawn much interest in studies of collective movement. Surprisingly, in the field of biosonar this aspect of prey detection, which is probably very common, has received little to no attention. Here, we combine computer simulations and actual echo measurements to accurately estimate the echo sound pressure of insect swarms of different size and density. We show that swarm echo sound pressure increases with 3dB for every doubling of insect number, irrespective of swarm density. Thus swarms will be much easier to detect than single insects. Many of the insects bats eat are so small that they are only detectable by echolocation at very short distances. By focusing on detection of swarms of insects, a bat may increase its operating range and diversify its diet. Interestingly, interference between the sound waves reflected from a swarm of insects can sometimes result in echoes that are much weaker than echoes from single insects. We show that bats can reduce this problem by increasing the bandwidth of their echolocation calls. Specifically, a bandwidth of 3–8 kHz would guarantee receiving loud echoes from any angle relative to the swarm. Indeed, many bat species, and specifically bats hunting in open spaces, where swarms are abundant, use echolocation signals with a bandwidth of several kHz. Our results might also explain how the first echolocating bats that probably had limited echolocation abilities, could detect insects through swarm hunting., Author summary When bats hunt, they often encounter insects that fly in swarms. Echolocating bats emit sonar signals to search for prey and it is currently unknown what such swarms look like to a bat. Unlike vision, sonar senses the delay or distance to objects directly. We show that when bats hunt for insects in the sky, the echoes from the insects in a swarm will most of the time sum up and therefore become much louder than the echo of a single insect. Every time an insect swarm would double in number, a bat would hear an echo that is 3dB stronger. This could enable a bat to detect prey from longer distances and some bats might thus profit from swarm hunting. However, the echoes reflected from the many insects in the swarm also create acoustic interference so that sometimes the summed echo is actually weak at a certain frequency. We show how bats could deal with this drawback. It is known that most bats do not use sonar signals with a single tone but that they modulate their tones. Our analysis shows that this modulation can solve the problem of spectral interference ensuring that the swarm-echo is always loud.

Most animals are at risk from multiple predators and can vary anti-predator behaviour based on the level of threat posed by each predator. Animals use sensory systems to detect predator cues, but the relationship between the tuning of sensory systems and the sensory cues related to predator threat are not well-studied at the community level. Noctuid moths have ultrasound-sensitive ears to detect the echolocation calls of predatory bats. Here, combining empirical data and mathematical modelling, we show that moth hearing is adapted to provide information about the threat posed by different sympatric bat species. First, we found that multiple characteristics related to the threat posed by bats to moths correlate with bat echolocation call frequency. Second, the frequency tuning of the most sensitive auditory receptor in noctuid moth ears provides information allowing moths to escape detection by all sympatric bats with similar safety margin distances. Third, the least sensitive auditory receptor usually responds to bat echolocation calls at a similar distance across all moth species for a given bat species. If this neuron triggers last-ditch evasive flight, it suggests that there is an ideal reaction distance for each bat species, regardless of moth size. This study shows that even a very simple sensory system can adapt to deliver information suitable for triggering appropriate defensive reactions to each predator in a multiple predator community.

The acoustic arms race between insectivorous bats and their invertebrate prey has led to the convergent evolution of ultrasound hearing in seven orders of nocturnal insects. Upon hearing the echolocation calls of an approaching bat, such insects take defensive action. Here, we document a previously unknown sense of ultrasound hearing and phonotactic flight behaviour in the neuropteran family Myrmeleontidae (antlions). The antlion Myrmeleon hyalinus was presented with sound pulses at ultrasonic frequencies used by echolocating bats and its response thresholds in tethered flight determined. Behaviours included abdominal twitches, wing flicks, brief pauses in flight and flight cessation. Such behaviours create erratic evasive flight manoeuvres in other eared insects, particularly mantids and lacewings. Antlions responded best to ultrasound between 60 and 80 kHz (75 dB peSPL at 80 kHz), showing response thresholds similar to those of the related lacewings (Neuroptera, Chrysopidae). Yet, at lower ultrasonic frequencies (20–50 kHz), antlions were far less sensitive than lacewings. Based on calculated response distances, we conclude that antlions respond only after having been detected by bats rather than using early evasive flights. We argue that the high response threshold for low-frequency ultrasound is adaptive for an insect that is mainly active close to and within vegetation, because a behavioural response to the lower ultrasonic frequencies used by high-flying bats would result in evasive action in the absence of actual predation risk.

Active echolocation enables bats to orient and hunt the night sky for insects. As a counter-measure against the severe predation pressure many nocturnal insects have evolved ears sensitive to ultrasonic bat calls. In moths bat-detection was the principal purpose of hearing, as evidenced by comparable hearing physiology with best sensitivity in the bat echolocation range, 20–60 kHz, across moths in spite of diverse ear morphology. Some eared moths subsequently developed sound-producing organs to warn/startle/jam attacking bats and/or to communicate intraspecifically with sound. Not only the sounds for interaction with bats, but also mating signals are within the frequency range where bats echolocate, indicating that sound communication developed after hearing by “sensory exploitation”. Recent findings on moth sound communication reveal that close-range (~ a few cm) communication with low-intensity ultrasounds “whispered” by males during courtship is not uncommon, contrary to the general notion of moths predominantly being silent. Sexual sound communication in moths may apply to many eared moths, perhaps even a majority. The low intensities and high frequencies explain that this was overlooked, revealing a bias towards what humans can sense, when studying (acoustic) communication in animals.

The vast majority of animal vocalizations contain multiple frequency modulated (FM) components with varying amounts of non-linear modulation and harmonic instability. This is especially true of biosonar sounds where precise time-frequency templates are essential for neural information processing of echoes. Understanding the dynamic waveform design by bats and other echolocating animals may help to improve the efficacy of man-made sonar through biomimetic design. Bats are known to adapt their call structure based on the echolocation task, proximity to nearby objects, and density of acoustic clutter. To interpret the significance of these changes, a method was developed for component separation and analysis of biosonar waveforms. Techniques for imaging in the time-frequency plane are typically limited due to the uncertainty principle and interference cross terms. This problem is addressed by extending the use of the fractional Fourier transform to isolate each non-linear component for separate analysis. Once separated, empirical mode decomposition can be used to further examine each component. The Hilbert transform may then successfully extract detailed time-frequency information from each isolated component. This multi-component analysis method is applied to the sonar signals of four species of bats recorded in-flight by radiotelemetry along with a comparison of other common time-frequency representations.

Killer whales in the North Pacific, similar to Atlantic populations, produce high-frequency modulated signals, based on acoustic recordings from ship-based hydrophone arrays and autonomous recorders at multiple locations. The median peak frequency of these signals ranged from 19.6-36.1 kHz and median duration ranged from 50-163 ms. Source levels were 185-193 dB peak-to-peak re: 1 μPa at 1 m. These uniform, repetitive, down-swept signals are similar to bat echolocation signals and possibly could have echolocation functionality. A large geographic range of occurrence suggests that different killer whale ecotypes may utilize these signals.

Bat echolocation is a dynamic behavior that allows for real-time adaptations in the timing and spectro-temporal design of sonar signals in response to a particular task and environment. To enable detailed, quantitative analyses of adaptive sonar behavior, echolocation call design was investigated in big brown bats, trained to rest on a stationary platform and track a tethered mealworm that approached from a starting distance of about 170 cm in the presence of a stationary sonar distracter. The distracter was presented at different angular offsets and distances from the bat. The results of this study show that the distance and the angular offset of the distracter influence sonar vocalization parameters of the big brown bat, Eptesicus fuscus. Specifically, the bat adjusted its call duration to the closer of two objects, distracter or insect target, and the magnitude of the adjustment depended on the angular offset of the distracter. In contrast, the bat consistently adjusted its call rate to the distance of the insect, even when this target was positioned behind the distracter. The results hold implications for understanding spatial information processing and perception by echolocation.

SummaryEars evolved in many nocturnal insects, including some moths, to detect bat echolocation calls and evade capture [1, 2]. Although there is evidence that some bats emit echolocation calls that are inconspicuous to eared moths, it is difficult to determine whether this was an adaptation to moth hearing or originally evolved for a different purpose [2, 3]. Aerial-hawking bats generally emit high-amplitude echolocation calls to maximize detection range [4, 5]. Here we present the first example of an echolocation counterstrategy to overcome prey hearing at the cost of reduced detection distance. We combined comparative bat flight-path tracking and moth neurophysiology with fecal DNA analysis to show that the barbastelle, Barbastella barbastellus, emits calls that are 10 to 100 times lower in amplitude than those of other aerial-hawking bats, remains undetected by moths until close, and captures mainly eared moths. Model calculations demonstrate that only bats emitting such low-amplitude calls hear moth echoes before their calls are conspicuous to moths. This stealth echolocation allows the barbastelle to exploit food resources that are difficult to catch for other aerial-hawking bats emitting calls of greater amplitude.

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.

In this paper, techniques for time-frequency analysis and investigation of bat echolocation calls are studied. Particularly, enhanced resolution techniques are developed and/or used in this specific context for the first time. When compared to traditional time-frequency representation methods, the proposed techniques are more capable of showing previously unseen features in the structure of bat echolocation calls. It should be emphasized that although the study is focused on bat echolocation recordings, the results are more general and applicable to many other types of signal.

SUMMARYThrough staged free-flight encounters between echolocating bats and praying mantids, we examined the effectiveness of two potential predator-evasion behaviors mediated by different sensory modalities: (1) power dive responses triggered by bat echolocation detected by the mantis ultrasound-sensitive auditory system, and (2) `last-ditch' maneuvers triggered by bat-generated wind detected by the mantis cercal system. Hearing mantids escaped more often than deafened mantids (76% vs 34%, respectively; hearing conveyed 42%advantage). Hearing mantis escape rates decreased when bat attack sequences contained very rapid increases in pulse repetition rates (escape rates 16 p.p.s. 10 ms–1; escape rates>60% for transition slopes 16 p.p.s. 10 ms–1) could circumvent mantis/insect auditory defenses. However, echolocation attack sequences containing such transitions occurred in only 15% of the trials. Since mantis ultrasound-mediated responses are not 100% effective, cercal-mediated evasive behaviors triggered by bat-generated wind could be beneficial as a backup/secondary system. Although deafened mantids with functioning cerci did not escape more often than deafened mantids with deactivated cerci (35%vs 32%, respectively), bats dropped mantids with functioning cerci twice as frequently as mantids with deactivated cerci. This latter result was not statistically reliable due to small sample sizes, since this study was not designed to fully evaluate this result. It is an interesting observation that warrants further investigation, however, especially since these dropped mantids always survived the encounter.

In this modeling study we wanted to find out why bats of the family Vespertilionidae (and probably also members of other families of bats) use pulses with a certain bandwidth and duration. Previous studies have only speculated on the function of bandwidth and pulse duration in bat echolocation or addressed this problem by assuming that bats optimize echolocation parameters to achieve very fine acuities in receiving single echoes. Here, we take a different approach by assuming that bats in nature rarely receive single echoes from each pulse emission, but rather many highly overlapping echoes. Some echolocation tasks require individual echoes to be separated to reconstruct reflection points in space. We used an established hearing model to investigate how the parameters bandwidth and pulse duration influence the separation of overlapping echoes. Our findings corroborate the following previously unknown or unsubstantiated facts: Broadening the bandwidth improves the bat’s lower resolution limit. 2.Increasing the sweep rate (defined by bandwidth and pulse duration) improves acuity of each extracted echo. 3.Decreasing the sweep rate improves the probability of frequency channels being activated. Since facts 2 and 3 affect sweep rate in an opposing fashion, an optimum sweep rate will exist, depending on the quality of the returning echoes and the requirements of the bat to improve acuity. The existence of an optimal sweep rate explains why bats are likely to use certain combinations of bandwidth and pulse duration to obtain such sweep rates.

Big brown bats (Eptesicus) emit multiple-harmonic FM sounds (FM1, FM2) and exploit the relative weakening of higher harmonics in lowpass echoes from the surrounding scene to suppress clutter by defocusing of wideband images. Only echoes from a frontally located targets arrive as unfiltered, focused images. Experiments using electronically generated echoes show that lowpass filtering of masking echoes causes clutter masking to disappear. Lowpass filtering induces amplitude-latency trading, which retards response times at higher frequencies in clutter echoes relative to lower frequencies. Introducing countervailing changes in presentation-times of higher frequencies in electronically generated clutter echoes restores masking. In the big brown bat's inferior colliculus, FM sounds mimicking broadcasts and echoes evoke ~1 spike per sound at each neuron's best frequency; however, amplitude tuning is very broad. To exploit their high acuity for detecting coherence or non-coherence of echo responses, bats work in the latency domain instead, removing background objects through deliberate imposition of response de-synchronization and concomitant inattention on undesired clutter. Overall, the results indicate that big brown bats use neuronal response timing for virtually all auditory computations of echo delay, including clutter rejection. This use of active perceptual processes in biosonar instead of conventional sonar processes opens a new view toward biomimetic design.

The bat–moth arms race has existed for over 60 million y, with moths evolving ultrasonically sensitive ears and ultrasound-producing organs to combat bat predation. The evolution of these defenses has never been thoroughly examined because of limitations in simultaneously conducting behavioral and phylogenetic analyses across an entire group. Hawkmoths include >1,500 species worldwide, some of which produce ultrasound using genital stridulatory structures. However, the function and evolution of this behavior remain largely unknown. We built a comprehensive behavioral dataset of hawkmoth hearing and ultrasonic reply to sonar attack using high-throughput field assays. Nearly half of the species tested (57 of 124 species) produced ultrasound to tactile stimulation or playback of bat echolocation attack. To test the function of ultrasound, we pitted big brown bats (Eptesicus fuscus) against hawkmoths over multiple nights and show that hawkmoths jam bat sonar. Ultrasound production was immediately and consistently effective at thwarting attack and bats regularly performed catching behavior without capturing moths. We also constructed a fossil-calibrated, multigene phylogeny to study the evolutionary history and divergence times of these antibat strategies across the entire family. We show that ultrasound production arose in multiple groups, starting in the late Oligocene (∼26 Ma) after the emergence of insectivorous bats. Sonar jamming and bat-detecting ears arose twice, independently, in the Miocene (18–14 Ma) either from earless hawkmoths that produced ultrasound in response to physical contact only, or from species that did not respond to touch or bat echolocation attack.

SummaryMany night-flying insects evolved ultrasound sensitive ears in response to acoustic predation by echolocating bats [1–10]. Noctuid moths are most sensitive to frequencies at 20–40 kHz [6], the lower range of bat ultrasound [5, 11–13]. This may disadvantage the moth because noctuid-hunting bats in particular echolocate at higher frequencies shortly before prey capture [7, 11–13] and thus improve their echolocation and reduce their acoustic conspicuousness [6–10, 12–16]. Yet, moth hearing is not simple; the ear's nonlinear dynamic response shifts its mechanical sensitivity up to high frequencies. Dependent on incident sound intensity, the moth's ear mechanically tunes up and anticipates the high frequencies used by hunting bats. Surprisingly, this tuning is hysteretic, keeping the ear tuned up for the bat's possible return. A mathematical model is constructed for predicting a linear relationship between the ear's mechanical stiffness and sound intensity. This nonlinear mechanical response is a parametric amplitude dependence [17, 18] that may constitute a feature common to other sensory systems. Adding another twist to the coevolutionary arms race between moths and bats, these results reveal unexpected sophistication in one of the simplest ears known and a novel perspective for interpreting bat echolocation calls.

Animals often deal with situations in which vast sensory input is received simultaneously. They therefore must possess sophisticated mechanisms to select important input and ignore the rest. In bat echolocation, this problem is at its extreme. Echolocating bats emit sound signals and analyse the returning echoes to sense their environment. Bats from the same species use signals with similar frequencies. Nearby bats therefore face the difficulty of distinguishing their own echoes from the signals of other bats, a problem often referred to as jamming. Because bats commonly fly in large groups, jamming might simultaneously occur from numerous directions and at many frequencies. Jamming is a special case of the general phenomenon of sensory segregation. Another well-known example is the human problem of following conversation within a crowd. In both situations, a flood of auditory incoming signals must be parsed into important versus irrelevant information. Here, we present a novel method, fitting wild bats with a miniature microphone, which allows studying jamming from the bat's ‘point of view’. Previous studies suggested that bats deal with jamming by shifting their echolocation frequency. On-board recordings suggest otherwise. Bats shifted their frequencies, but they did so because they were responding to the conspecifics as though they were nearby objects rather than avoiding being jammed by them. We show how bats could use alternative measures to deal with jamming instead of shifting their frequency. Despite its intuitive appeal, a spectral jamming avoidance response might not be the prime mechanism to avoid sensory interference from conspecifics.

A computational sensorimotor model of target capture behavior by the echolocating bat, Eptesicus fuscus, was developed to understand the detection, localization, tracking, and interception of insect prey in a biological sonar system. This model incorporated acoustics, target localization processes, flight aerodynamics, and target capture planning to produce model trajectories replicating those observed in behavioral insect capture trials. Estimates of target range were based on echo delay, azimuth on the relative intensity of the echo at the two ears, and elevation on the spectral pattern of the sonar return in a match/mismatch process. Flapping flight aerodynamics was used to produce realistic model trajectories. Localization in all three spatial dimensions proved necessary to control target tracking and interception for an adequate model of insect capture behavior by echolocating bats. Target capture using maneuvering flight was generally successful when the model's path was controlled by a planning process that made use of an anticipatory internal simulation, while simple homing was successful only for targets directly ahead of the model bat.

The responses of female Tettigonia viridissima to simulated bat echolocation calls were examined during tethered flight. The insects responded with three distinct behaviours, which occurred at graded stimulus intensities. At low intensities (threshold 54 dB SPL), T. viridissima responded by steering away from the sound source (negative phonotaxis). At intensities approximately 10 dB higher, beating of the hindwing was interrupted, although the insect remained in the flight posture. A diving response (cessation of the wingbeat, closure of the forewings and alignment of the legs against the body) occurred with a threshold of 76 dB SPL. Considering these thresholds, we estimate that the diving response occurs at approximately the sound amplitude at which many aerial-hawking bats first receive echoes from the insect. The other behaviours probably occur before the bat detects the insect and should therefore be interpreted as early avoidance behaviours. The repertoire of startle responses in T. viridissima, with directional and non-directional components, is similar to those of crickets and moths, but quite different from those described for another bushcricket (Neoconocephalus ensiger), which shows only a non-directional response. This supports the conclusion that bat-evasive behaviours are not conserved within the Tettigoniidae, but instead are shaped by the ecological constraints of the insects.

We propose a scheme for a new database using standardized protocol for recording and analysis of bat calls. The proposed database will describe and archive echolocation signals to create a reference library of bat calls. This information should be accessible to the public, thus encouraging continuous feedback from a broad audience. Because it is essential to evaluate the quality and reliability of such data, detailed information of recording and analysis procedures as well as the resulting species identification is required. A standardized and growing database on bat calls would be a potentially invaluable tool for global species identification, comparison, and distribution of microchiropterans. Currently, apart from a few websites with local call libraries, there is no "global" database established yet. We hope that researchers, amateurs, and wildlife and management authorities will adopt and further modify our suggestions for a standardized database for bat calls. We also hope that this database will stimulate new directions in bat research.

The tuning and pure-tone physiology of the T-cell prothoracic auditory interneuron were investigated in the nocturnal katydid Neoconocephalus ensiger. The T-cell is extremely sensitive and broadly tuned, particularly to high-frequency ultrasound (?:20 kHz). Adult thresholds were lowest and showed their least variability for frequencies ranging from 25 to 80 kHz. The average best threshold of the T-cell in N. ensiger ranged from 28 to 38 dB SPL and the best frequency from 20 to 27 kHz. In females, the T-cell is slightly more sensitive to the range of frequencies encompassing the spectrum of male song. Tuning of the T-cell in non-volant nymphs was comparable with that of adults, and this precocious ultrasound sensitivity supports the view that it has a role in the detection of terrestrial sources of predaceous ultrasound. In adults, T-cell tuning is narrower than that of the whole auditory (tympanic) organ, but only at audio frequencies. Superthreshold physiological experiments revealed that T-cell responses were ultrasound-biased, with intensity/response functions steeper and spike latencies shorter at 20, 30 and 40 kHz than at 5, 10 and 15 kHz. The same was also true for T-cell stimulation at 90 ° compared with stimulation at 0 ° within a frequency, which supports early T-cell research showing that excitation of the contralateral ear inhibits ipsilateral T-cell responses. In a temporal summation experiment, the integration time of the T-cell at 40 kHz (integration time constant τ=6.1 ms) was less than half that measured at 15 kHz (τ=15.0 ms). Moreover, T-cell spiking in response to short-duration pure-tone trains mimicking calling conspecifics (15 kHz) and bat echolocation hunting sequences (40 kHz) revealed that temporal pattern-copying was superior for ultrasonic stimulation. Apparently, T-cell responses are reduced or inhibited by stimulation with audio frequencies, which leads to the prediction that the T-cell will encode conspecific song less well than bat-like frequency-modulated sweeps during acoustic playback. The fact that the T-cell is one of the most sensitive ultrasound neurons in tympanate insects is most consistent with it serving an alarm, warning or escape function in both volant and non-volant katydids (nymphs and adults).

The hearing range of the tettigoniid Phaneropterafalcata for the echolocation calls of freely flying mouseeared bats (Myotis myotis) was determined in the field. The hearing of the insect was monitored using hook electrode recordings from an auditory interneuron, which is as sensitive as the hearing organ for frequencies above 16 kHz. The flight path of the bat relative to the insect's position was tracked by recording the echolocation calls with two microphone arrays, and calculating the bat's position from the arrival time differences of the calls at each microphone. The hearing distances ranged from 13 to 30 m. The large variability appeared both between different insects and between different bat approaches to an individual insect. The escape time of the bushcricket, calculated from the detection distance of the insect and the instantaneous flight speed of the bat, ranged from 1.5 to more than 4s. The hearing ranges of bushcrickets suggest that the insect hears the approaching bat long before the bat can detect an echo from the flying insect.

This study examines the contribution of GABAergic inhibition to the discharge pattern and pulse duration tuning characteristics of 101 bat inferior collicular neurons by means of bicuculline application to their recording sites. When stimulated with single pulses, 56 (55%) neurons discharged 1 or 2 impulses (phasic responders), 42 (42%) discharged 3–10 impulses (phasic bursters) and 3 (3%) discharged impulses throughout the stimulus duration (tonic responders). Bicuculline application increased the number of impulses and changed the discharge patterns of 66 neurons. Using 50% difference between maximal and minimal responses as a criterion, the duration tuning characteristics of these neurons can be described as band-pass (20, 20%), long-pass (17, 17%), short-pass (33, 32%), and all-pass (31, 31%). Each band-pass neuron discharged maximally to a specific duration (the best duration) which was at least 50% larger than the neuron's responses to a long-duration pulse and a short-duration pulse. In contrast, each long- or short-pass neuron discharged maximally to a range of long or short duration pulses. Bicuculline application changed the duration tuning characteristics of 65 neurons. Possible mechanisms underlying duration tuning characteristics and the behavioral relevance to bat echolocation are discussed.

One of the most efficient mechanisms to optimize signal-to-noise ratios is the Lombard effect - an involuntary rise in call amplitude due to ambient noise. It is often accompanied by changes in the spectro-temporal composition of calls. We examined the effects of broadband-filtered noise on the spectro-temporal composition of horseshoe bat echolocation calls, which consist of a constant-frequency component and an initial and terminal frequency-modulated portion. We find that the frequency-modulated components became larger for almost all noise conditions, whereas the bandwidth of the constant-frequency component increased only when broadband-filtered noise was centered on or above the calls' dominant or fundamental frequency. This indicates that ambient noise modifies the associated acoustic parameters of the Lombard-effect, such as spectro-temporal features, independently and could significantly affect the bat's ability to detect and locate targets. Our findings may be of significance in evaluating the impact of environmental noise on echolocation behavior in bats.

The information echolocating bats receive is a combination of the properties of the sound they emit and the sound they receive at the eardrum. Convolving the emission and the external ear transfer functions produces the full spectral information contained in the echolocation combination. Spatially dependent changes in the magnitude spectra of the emission, external ear transfer functions, and the echolocation combination of Eptesicus fuscus could provide localization information to the bat. Principal component analysis was used to reduce the dimensionality of these complex spectral data sets. The first eight principal component weights were normalized, rotated, and used as the input to a backpropagation network model which examined the relative directionality of the emission, ear, and the echolocation combination. The model was able to localize more accurately when provided with the directional information of the echolocation combination compared to either the emission or ear information alone.

An evolutionary war is being played out between the bat, which uses ultrasonic calls to locate insect prey, and the moth, which uses microscale ears to listen for the approaching bat. While the highest known frequency of bat echolocation calls is 212 kHz, the upper limit of moth hearing is considered much lower. Here, we show that the greater wax moth, Galleria mellonella , is capable of hearing ultrasonic frequencies approaching 300 kHz; the highest frequency sensitivity of any animal. With auditory frequency sensitivity that is unprecedented in the animal kingdom, the greater wax moth is ready and armed for any echolocation call adaptations made by the bat in the on-going bat–moth evolutionary war.

Computational brain maps as opposed to maps of receptor surfaces strongly reflect functional neuronal design principles. In echolocating bats, computational maps are established that topographically represent the distance of objects. These target range maps are derived from the temporal delay between emitted call and returning echo and constitute a regular representation of time (chronotopy). Basic features of these maps are innate, and in different bat species the map size and precision varies. An inherent advantage of target range maps is the implementation of mechanisms for lateral inhibition and excitatory feedback. Both can help to focus target ranging depending on the actual echolocation situation. However, these maps are not absolutely necessary for bat echolocation since there are bat species without cortical target-distance maps, which use alternative ensemble computation mechanisms.

The big brown bat (Eptesicus fuscus) uses frequency modulated (FM) echolocation calls to accurately estimate range and resolve closely spaced objects in clutter and noise. They resolve glints spaced down to 2 μs in time delay which surpasses what traditional signal processing techniques can achieve using the same echolocation call. The Matched Filter (MF) attains 10-12 μs resolution while the Inverse Filter (IF) achieves higher resolution at the cost of significantly degraded detection performance. Recent work by Fontaine and Peremans [J. Acoustic. Soc. Am. 125, 3052-3059 (2009)] demonstrated that a sparse representation of bat echolocation calls coupled with a decimating sensing method facilitates distinguishing closely spaced objects over realistic SNRs. Their work raises the intriguing question of whether sensing approaches structured more like a mammalian auditory system contains the necessary information for the hyper-resolution observed in behavioral tests. This research estimates sparse echo signatures using a gammatone filterbank decimation sensing method which loosely models the processing of the bat's auditory system. The decimated filterbank outputs are processed with [script-l](1) minimization. Simulations demonstrate that this model maintains higher resolution than the MF and significantly better detection performance than the IF for SNRs of 5-45 dB while undersampling the return signal by a factor of six.

Insectivorous bats are able to locate and capture insects in complete darkness while flying at high speeds. They may consume hundreds of insects each night while avoiding obstacles in a complex environment. To investigate the processes associated with bat echolocation, we have developed instrumentation that allows us to record and visualize what a bat hears while flying through its natural environment. Recordings were made using a miniaturized radio telemetry system mounted directly on the back of the bat. This paper describes the design and testing of the components of this system, presents echolocation data collected from bats and discusses issues associated with the visualization and analysis of echoes recorded in a natural setting from the bat's point-of-view. It presents a new tool for visualizing a bat's experience by generating call sequence sonograms (CSSs) based on various signal parameters. CSSs based on time series amplitude, band-limited spectral magnitude and Q-factor are presented. This work demonstrates that CSSs based on Q-factor (computed by dividing a peak frequency estimate by a bandwidth estimate) provides a relatively clear representation of the objects producing echoes encountered by a bat during a continuous flight.

Echolocating bats detect prey using ultrasonic pulses, and many nocturnally flying insects effectively detect and evade these predators through sensitive ultrasonic hearing. Many eared insects can use the intensity of the predator-generated ultrasound and the stereotyped progression of bat echolocation pulse rate to assess risk level. Effective responses can vary from gentle turns away from the threat (low risk) to sudden random flight and dives (highest risk). Recent research with eared moths shows that males will balance immediate bat predation risk against reproductive opportunity as judged by the strength and quality of conspecific pheromones present. Ultrasound exposure may, in fact, bias such decisions for up to 24 hours through plasticity in the CNS olfactory system. However, brain processing of ultrasonic stimuli to yield adaptive prey behaviors remains largely unstudied, so possible mechanisms are not known.

A protruding noseleaf and concave pinna structures suggest that some bats may use these to enhance their echolocation capabilities. This paper considers two possible mechanisms that each exploit the combination of direct and delayed acoustic paths to achieve more complex emission or sensitivity echolocation patterns. The first is an emission mechanism, in which the protruding noseleaf vibrates to emit sound in both the forward and backward directions, and pinna structures reflect the backward emission to enhance the forward beam. The second is a reception mechanism, which has a direct echo path to the ear canal and a delayed path involving pinna structures reflecting onto the noseleaf and then into the ear canal. A model using Davis’ Round-eared Bat illustrates that such direct and delayed acoustic paths provide target elevation cues. The model demonstrates the delayed pinna component can increase the on-axis emission strength, narrow the beam width, and sculpt frequency-dependent beam patterns useful for echolocation.

It has been argued that an important part of understanding bat echolocation comes down to understanding the morphology of the bat sound processing apparatus. In this Letter we present a method based on information theory that allows us to assess target localization performance of bat sonar, without a priori knowledge on the position, size, or shape of the reflecting target. We demonstrate this method using simulated directivity patterns of the frequency-modulated bat Micronycteris microtis. The results of this analysis indicate that the morphology of this bats sound processing apparatus has evolved to be a compromise between sensitivity and accuracy with the pinnae and the noseleaf playing different roles.

It has been proposed that intraspecific ultrasonic communication observed in some moths evolved, through sexual selection, subsequent to the development of ears sensitive to echolocation calls of insectivorous bats. Given this scenario, the receiver bias model of signal evolution argues that acoustic communication in moths should have evolved through the exploitation of receivers' sensory bias towards bat ultrasound. We tested this model using a noctuid mothSpodoptera litura, males of which were recently found to produce courtship ultrasound. We first investigated the mechanism of sound production in the male moth, and subsequently the role of the sound with reference to the female's ability to discriminate male courtship songs from bat calls. We found that males have sex-specific tymbals for ultrasound emission, and that the broadcast of either male songs or simulated bat calls equally increased the acceptance of muted males by the female. It was concluded that females of this moth do not distinguish between male songs and bat calls, supporting the idea that acoustic communication in this moth evolved through a sensory exploitation process.

Active echolocation is a sensory modality possessed by a variety of mammals and is used for the identification, classification and localization of objects. A multi stage model of the bat echolocation process has been used with recordings of rotated disks to plot frequency spectrums of the signals reaching each of the bats' ears. Recordings from objects made within the human audible frequency range have also been made for use in psychoacoustic experiments aimed at validating preliminary studies that have shown some human ability to localize objects using echolocation.

To perform echolocation, so-called FM-bats emit short pulses i.e., with a duration of a few milliseconds, and analyse the echoes coming from their environment. One individual echo, due to its short duration, will cause neurons in the early auditory system to generate between 1 and 3 spikes only. Hence, we argue that it is advantageous for FM-bats to use spike-time rather that firing rate information. We present a simple spike-time model of the monaural and binaural pathways up to the midbrain, to show that spike-time information can indeed be processed by the known neural architecture. In particular, we show that a First Spike Latency (FSL) code, as provided by the auditory nerves, can represent both the monaural and binaural intensity cues induced by the head-related transfer function in the peripheral system. We also show that ascending centres enhance the cues conveyed by such an FSL code. Finally, we present experimental results, comparing the FSL code based model proposed here with a more classic firing rate code, and we show that first-spike latency is a more biologically plausible alternative.

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.

Previous studies have shown that inferior collicular neurons of the big brown bat, Eptesicus fuscus, serve as short-, band-, long- and all-pass filters for sound durations. Neurons with band-, short- and long-pass filtering characteristics discharged maximally to a specific sound duration or a range of sound durations. In contrast, neurons with all-pass filtering characteristics do not have duration selectivity. To determine if duration-tuning characteristics of collicular neurons were tolerant to changes in sound intensity, we examined the duration-tuning characteristics of collicular neurons using a wide range of sound intensities. Duration-tuning characteristics examined included the type, bandwidth and slope of duration-tuning curves. Sound intensity delivered within 20 dB of minimum threshold did not affect duration-tuning characteristics of all collicular neurons studied. Sound intensities at still higher levels did not affect the tuning characteristics of two-thirds of collicular neurons but decreased the duration selectivity and changed the duration-tuning curves of the remaining one-third of neurons from one type to another. However, these two groups of duration-tuning collicular neurons were not separately organized inside the inferior colliculus. The biological relevance of these findings to bat echolocation is discussed.

Echolocation signals were recorded from big brown bats, Eptesicus fuscus, flying in the field and the laboratory. In open field areas the interpulse intervals (IPI) of search signals were either around 134 ms or twice that value, 270 ms. At long IPI's the signals were of long duration (14 to 18-20 ms), narrow bandwidth, and low frequency, sweeping down to a minimum frequency (Fmin) of 22-25 kHz. At short IPI's the signals were shorter (6-13 ms), of higher frequency, and broader bandwidth. In wooded areas only short (6-11 ms) relatively broadband search signals were emitted at a higher rate (avg. IPI= 122 ms) with higher Fmin (27-30 kHz). In the laboratory the IPI was even shorter (88 ms), the duration was 3-5 ms, and the Fmin 30- 35 kHz, resembling approach phase signals of field recordings. Excluding terminal phase signals, all signals from all areas showed a negative correlation between signal duration and Fmin, i.e., the shorter the signal, the higher was Fmin. This correlation was reversed in the terminal phase of insect capture sequences, where Fmin decreased with decreasing signal duration. Overall, the signals recorded in the field were longer, with longer IPI's and greater variability in bandwidth than signals recorded in the laboratory.

We measured the auditory responses of the noctuid moth Noctua pronuba to bat echolocation calls which were manipulated independently in time and frequency. Such manipulations are important in understanding how insect hearing influences the evolution of echolocation call characteristics. We manipulated the calls of three bat species (Rhinolophus hipposideros, Myotis nattereri and Pipistrellus pipistrellus) that use different echolocation call features by doubling their duration or reducing their frequency, and measured the auditory thresholds from the A1 cells of the moths. Knowing the auditory responses of the moth we tested three predictions. (i) The ranking of the audibility of unmanipulated calls to the moths should be predictable from their temporal and/or frequency structure. This was supported. (ii) Doubling the duration of the calls should increase their audibility by ca. 3 dB for all species. Their audibility did indeed increase by 2.1-3.5 dB. (iii) Reducing the frequency of the calls would increase their audibility for all species. Reducing the frequency had small effects for the two bat species which used short duration (2.7-3.6 ms) calls. However, the relatively long-duration (50 ms), largely constant-frequency calls of R. hipposideros increased in audibility by 21.6 dB when their frequency was halved. Time and frequency changes influence the audibility of calls to tympanate moths in different ways according to call design. Large changes in frequency and time had relatively small changes on the audibility of calls for short, largely broadband calls. Channelling energy into the second harmonic of the call substantially decreased the audibility of calls for bats which use long-duration, constant-frequency components in echolocation calls. We discuss our findings in the contexts of the evolution of both bat echolocation call design and the potential responses of insects which hear ultrasound.

This study examines the role of neural inhibition in auditory spatial selectivity of inferior collicular neurons of the big brown bat, Eptesicus fuscus, using a two-tone inhibition paradigm. Two-tone inhibition decreases auditory spatial response areas but increases the slopes of directional sensitivity curves of inferior collicular neurons. Inferior collicular neurons have either directionally-selective or hemifield directional sensitivity curves. A directionally-selective curve always has a peak which is at least 50% larger than the minimum. A hemifield directional sensitivity curve rises from an ipsilateral angle by more than 50% and either reaches a plateau or declines by less than 50% over a range of contralateral angles. Two-tone inhibition does not change directionally-selective curves but changes most hemifield directional sensitivity curves into directionally-selective curves. Auditory spatial selectivity determined both with and without two-tone inhibition increases with increasing best-excitatory frequency. Sharpening of auditory spatial selectivity by two-tone inhibition is larger for neurons with smaller differences between excitatory and inhibitory best frequencies. The effect of two-tone inhibition on auditory spatial selectivity increases with increasing inhibitory tone intensity but decreases with increasing intertone interval. The implications of these findings in bat echolocation are discussed.

Clicks emitted by arctiid moths interfere with the ranging ability of echolocating bats. To identify possible neural correlates of this interference, we recorded responses of single units in the nuclei of the lateral lemniscus to combinations of a broad-band click and a test signal (pure tones or frequency-modulated sweeps). In 77% of 87 units tested, clicks interfered with neural responses to the test stimuli. The interference fell into two categories: latency ambiguity and suppression. Units showing latency ambiguity responded to both the click and the test signal. However, when the click occurred within a window of approximately 3 ms before the onset of the test signal, the latency of the response to the test signal was affected. Units that were suppressed did not respond to clicks. Nevertheless, when a click was presented immediately before or simultaneously with a test signal, the response to the test signal was eliminated. Both types of units were found throughout the lateral lemniscus except for the columnar division of the ventral nucleus, where all units tested exhibited latency ambiguity. There is a close match between the single unit data and previous studies of range difference discrimination in the presence of clicks.

SummaryBecause evolution mostly acts over millions of years, the intermediate steps leading to a functional sensory system remain enigmatic [1–3]. Accordingly, there is an ongoing debate regarding the evolution of bat echolocation [4–10]. In search of the origin of bat echolocation, we studied how Old World fruit bats, which have always been classified as nonecholocating [3, 10–12], orient in complete darkness. We found that two of these nonecholocating species used click-like sounds to detect and discriminate objects in complete darkness. However, we discovered that this click-based echo sensing is rudimentary and does not allow these bats to estimate distance accurately as all other echolocating bats can. Moreover, unlike all other echolocating bats, which generate pulses using the larynx or the tongue, these bats generated clicks with their wings. We provide evidence suggesting that all Old World fruit bats can click with their wings. Although this click-based echo sensing used by Old World fruit bats may not represent the ancestral form of current (laryngeal) bat echolocation, we argue that clicking fruit bats could be considered behavioral fossils, opening a window to study the evolution of echolocation.

A common feature of most bat echolocation calls is their hyperbolalike frequency modulation. It is proposed that these calls evolved as an adaptation to the filters in the peripheral hearing system. From an analysis of 420 echolocation sounds of Eptesicus fuscus, the bandwidths of filters giving a minimal error of time-delay estimation are predicted; these could be compared to neurophysiological findings.