Echolocation Sounds Research Articles

An Efficient Neural Network Design Incorporating Autoencoders for the Classification of Bat Echolocation Sounds.

Bats are widely distributed around the world, have adapted to many different environments and are highly sensitive to changes in their habitat, which makes them essential bioindicators of environmental changes. Passive acoustic monitoring over long durations, like months or years, accumulates large amounts of data, turning the manual identification process into a time-consuming task for human experts. Automated acoustic monitoring of bat activity is therefore an effective and necessary approach for bat conservation, especially in wind energy applications, where flying animals like bats and birds have high fatality rates. In this work, we provide a neural-network-based approach for bat echolocation pulse detection with subsequent genus classification and species classification under real-world conditions, including various types of noise. Our supervised model is supported by an unsupervised learning pipeline that uses autoencoders to compress linear spectrograms into latent feature vectors that are fed into a UMAP clustering algorithm. This pipeline offers additional insights into the data properties, aiding in model interpretation. We compare data collected from two locations over two consecutive years sampled at four heights (10 m, 35 m, 65 m and 95 m). With sufficient data for each labeled bat class, our model is able to comprehend the full echolocation soundscape of a species or genus while still being computationally efficient and simple by design. Measured classification F1 scores in a previously unknown test set range from 92.3% to 99.7% for species and from 94.6% to 99.4% for genera.

The Occipital Place Area Is Recruited for Echo-Acoustically Guided Navigation in Blind Human Echolocators.

In the investigation of the brain areas involved in human spatial navigation, the traditional focus has been on visually guided navigation in sighted people. Consequently, it is unclear whether the involved areas also support navigational abilities in other modalities. We explored this possibility by testing whether the occipital place area (OPA), a region associated with visual boundary-based navigation in sighted people, has a similar role in echo-acoustically guided navigation in blind human echolocators. We used fMRI to measure brain activity in 6 blind echolocation experts (EEs; five males, one female), 12 blind controls (BCs; six males, six females), and 14 sighted controls (SCs; eight males, six females) as they listened to prerecorded echolocation sounds that conveyed either a route taken through one of three maze environments, a scrambled (i.e., spatiotemporally incoherent) control sound, or a no-echo control sound. We found significantly greater activity in the OPA of EEs, but not the control groups, when they listened to the coherent route sounds relative to the scrambled sounds. This provides evidence that the OPA of the human navigation brain network is not strictly tied to the visual modality but can be recruited for nonvisual navigation. We also found that EEs, but not BCs or SCs, recruited early visual cortex for processing of echo acoustic information. This is consistent with the recent notion that the human brain is organized flexibly by task rather than by specific modalities.SIGNIFICANCE STATEMENT There has been much research on the brain areas involved in visually guided navigation, but we do not know whether the same or different brain regions are involved when blind people use a sense other than vision to navigate. In this study, we show that one part of the brain (occipital place area) known to play a specific role in visually guided navigation is also active in blind human echolocators when they use reflected sound to navigate their environment. This finding opens up new ways of understanding how people navigate, and informs our ability to provide rehabilitative support to people with vision loss.

Adaptive echolocation behavior of bats and toothed whales in dynamic soundscapes.

Journal of Experimental Biology has a long history of reporting research discoveries on animal echolocation, the subject of this Centenary Review. Echolocating animals emit intense sound pulses and process echoes to localize objects in dynamic soundscapes. More than 1100 species of bats and 70 species of toothed whales rely on echolocation to operate in aerial and aquatic environments, respectively. The need to mitigate acoustic clutter and ambient noise is common to both aerial and aquatic echolocating animals, resulting in convergence of many echolocation features, such as directional sound emission and hearing, and decreased pulse intervals and sound intensity during target approach. The physics of sound transmission in air and underwater constrains the production, detection and localization of sonar signals, resulting in differences in response times to initiate prey interception by aerial and aquatic echolocating animals. Anti-predator behavioral responses of prey pursued by echolocating animals affect behavioral foraging strategies in air and underwater. For example, many insect prey can detect and react to bat echolocation sounds, whereas most fish and squid are unresponsive to toothed whale signals, but can instead sense water movements generated by an approaching predator. These differences have implications for how bats and toothed whales hunt using echolocation. Here, we consider the behaviors used by echolocating mammals to (1) track and intercept moving prey equipped with predator detectors, (2) interrogate dynamic sonar scenes and (3) exploit visual and passive acoustic stimuli. Similarities and differences in animal sonar behaviors underwater and in air point to open research questions that are ripe for exploration.

How the bat brain detects novel sounds (commentary on Wetekam et al., 2021).

How the bat brain detects novel sounds (commentary on Wetekam et al., 2021).

Natural acoustic stimuli evoke selective responses in the hippocampus of passive listening bats

A growing body of research details spatial representation in bat hippocampus, and experiments have yet to explore hippocampal neuron responses to sonar signals in animals that rely on echolocation for spatial navigation. To bridge this gap, we investigated bat hippocampal responses to natural echolocation sounds in a non‐spatial context. In this experiment, we recorded from CA1 of the hippocampus of three awake bats that listened passively to single echolocation calls, call‐echo pairs, or natural echolocation sequences. Our data analysis identified a subset of neurons showing response selectivity to the duration of single echolocation calls. However, the sampled population of CA1 neurons did not respond selectively to call‐echo delay, a stimulus dimension posited to simulate target distance in recordings from auditory brain regions of bats. A population analysis revealed ensemble coding of call duration and sequence identity. These findings open the door to many new investigations of auditory coding in the mammalian hippocampus.

Acoustic Context Modulates Natural Sound Discrimination in Auditory Cortex through Frequency-Specific Adaptation.

Sound discrimination is essential in many species for communicating and foraging. Bats, for example, use sounds for echolocation and communication. In the bat auditory cortex there are neurons that process both sound categories, but how these neurons respond to acoustic transitions, that is, echolocation streams followed by a communication sound, remains unknown. Here, we show that the acoustic context, a leading sound sequence followed by a target sound, changes neuronal discriminability of echolocation versus communication calls in the cortex of awake bats of both sexes. Nonselective neurons that fire equally well to both echolocation and communication calls in the absence of context become category selective when leading context is present. On the contrary, neurons that prefer communication sounds in the absence of context turn into nonselective ones when context is added. The presence of context leads to an overall response suppression, but the strength of this suppression is stimulus specific. Suppression is strongest when context and target sounds belong to the same category, e.g.,echolocation followed by echolocation. A neuron model of stimulus-specific adaptation replicated our results in silico The model predicts selectivity to communication and echolocation sounds in the inputs arriving to the auditory cortex, as well as two forms of adaptation, presynaptic frequency-specific adaptation acting in cortical inputs and stimulus-unspecific postsynaptic adaptation. In addition, the model predicted that context effects can last up to 1.5 s after context offset and that synaptic inputs tuned to low-frequency sounds (communication signals) have the shortest decay constant of presynaptic adaptation.SIGNIFICANCE STATEMENT We studied cortical responses to isolated calls and call mixtures in awake bats and show that (1) two neuronal populations coexist in the bat cortex, including neurons that discriminate social from echolocation sounds well and neurons that are equally driven by these two ethologically different sound types; (2) acoustic context (i.e., other natural sounds preceding the target sound) affects natural sound selectivity in a manner that could not be predicted based on responses to isolated sounds; and (3) a computational model similar to those used for explaining stimulus-specific adaptation in rodents can account for the responses observed in the bat cortex to natural sounds. This model depends on segregated feedforward inputs, synaptic depression, and postsynaptic neuronal adaptation.

Echolocation variability of franciscana dolphins (Pontoporia blainvillei) between estuarine and open-sea habitats, with insights into foraging patterns.

Environmental and ecological factors can trigger changes in the acoustic repertoire of cetaceans. This study documents the first use of a well-established passive acoustic monitoring device (C-POD) to analyze echolocation sounds and behavior of franciscana dolphins in different habitats: estuary [Babitonga Bay (BB)] and open sea [Itapirubá Beach (IB)]. A total of 10 924 click trains were recorded in BB and 6 093 in IB. An inter-click interval < 10 ms (so called "feeding buzzes") was used as a proxy for foraging activity. The main difference in the acoustic parameters between the two habitats was related to the frequency spectrum, with higher maximum and lower modal and minimum click frequencies in BB, and a train frequency range of 17 kHz, against 10 kHz in IB. Also, the click emission rate (clicks/s) was almost 20% higher in BB. Both studied habitats showed a high proportion of feeding buzzes (BB = 68%; IB = 58%), but with a higher probability of occurrence in BB (p < 0.001) and at night (p < 0.001) in both habitats. The C-PODs showed great potential to monitor occurrence, bioacoustics parameters, and echolocation behavior of franciscana dolphins. Longer-term temporal and spatial monitoring are necessary for elucidating several issues raised in this study.

Listening space reduction calculations

Listening space reduction analysis has been applied recently by several authors to evaluate the relative reduction of distance or space within which listeners can effectively detect and recognize important sound sources, due to increased acoustic masking caused by a known increase in masking noise. The approach balances the increased masking noise level by reducing source-listener distance so that propagation loss is commensurately reduced. Its recent applications have not considered all important parameters, including listener hearing sensitivity and directionality, listener cognitive signal processing gain, non-uniform acoustic propagation loss, and temporal and spatial distributions of masking noise variability. Here we derive the listening distance and space expressions from the sonar equation, accounting for the parameters above. Listening space reduction calculations are insensitive to some uncertain parameters, including source level and detection threshold (for non-human listeners) that are required for communication space calculations. The method is applicable to any sound type, including predator sounds, prey sounds, conspecific communications, and natural sounds. A modified version of the method is derived for echolocation sounds, and a corresponding echolocation space reduction factor is derived.

Venous networks in the upper airways of bats: A histological and diceCT study.

Our knowledge of nasal cavity anatomy has grown considerably with the advent of micro-computed tomography (CT). More recently, a technique called diffusible iodine-based contrast-enhanced CT (diceCT) has rendered it possible to study nasal soft tissues. Using diceCT and histology, we aim to (a) explore the utility of these techniques for inferring the presence of venous sinuses that typify respiratory mucosa and (b) inquire whether distribution of vascular mucosa may relate to specialization for derived functions of the nasal cavity (i.e., nasal-emission of echolocation sounds) in bats. Matching histology and diceCT data indicate that diceCT can detect venous sinuses as either darkened, "empty" spaces, or radio-opaque islands when blood cells are present. Thus, we show that diceCT provides reliable information on vascular distribution in the mucosa of the nasal airways. Among the bats studied, a nonecholocating pteropodid (Cynopterus sphinx) and an oral-emitter of echolocation sounds (Eptesicus fuscus) possess venous sinus networks that drain into the sphenopalatine vein rostral to the nasopharynx. In contrast, nasopharyngeal passageways of nasal-emitting hipposiderids are notably packed with venous sinuses. The mucosae of the nasopharyngeal passageways are far less vascular in nasal-emitting phyllostomids, in which vascular mucosae are more widely distributed in the nasal cavity, and in some nectar-feeding species, a particularly large venous sinus is adjacent to the vomeronasal organ. Therefore, we do not find a common pattern of venous sinus distribution associated with nasal emission of sounds in phyllostomids and hipposiderids. Instead, vascular mucosa is more likely critical for air-conditioning and sometimes vomeronasal function in all bats.

Increased emission intensity can compensate for the presence of noise in human click-based echolocation

Echolocating bats adapt their emissions to succeed in noisy environments. In the present study we investigated if echolocating humans can detect a sound-reflecting surface in the presence of noise and if intensity of echolocation emissions (i.e. clicks) changes in a systematic pattern. We tested people who were blind and had experience in echolocation, as well as blind and sighted people who had no experience in echolocation prior to the study. We used an echo-detection paradigm where participants listened to binaural recordings of echolocation sounds (i.e. they did not make their own click emissions), and where intensity of emissions and echoes changed adaptively based on participant performance (intensity of echoes was yoked to intensity of emissions). We found that emission intensity had to systematically increase to compensate for weaker echoes relative to background noise. In fact, emission intensity increased so that spectral power of echoes exceeded spectral power of noise by 12 dB in 4-kHz and 5-kHz frequency bands. The effects were the same across all participant groups, suggesting that this effect occurs independently of long-time experience with echolocation. Our findings demonstrate for the first time that people can echolocate in the presence of noise and suggest that one potential strategy to deal with noise is to increase emission intensity to maintain signal-to-noise ratio of certain spectral components of the echoes.

Enhanced representation of natural sound sequences in the ventral auditory midbrain

The auditory midbrain (inferior colliculus, IC) plays an important role in sound processing, acting as hub for acoustic information extraction and for the implementation of fast audio-motor behaviors. IC neurons are topographically organized according to their sound frequency preference: dorsal IC regions encode low frequencies while ventral areas respond best to high frequencies, a type of sensory map defined as tonotopy. Tonotopic maps have been studied extensively using artificial stimuli (pure tones) but our knowledge of how these maps represent information about sequences of natural, spectro-temporally rich sounds is sparse. We studied this question by conducting simultaneous extracellular recordings across IC depths in awake bats (Carollia perspicillata) that listened to sequences of natural communication and echolocation sounds. The hypothesis was that information about these two types of sound streams is represented at different IC depths since they exhibit large differences in spectral composition, i.e., echolocation covers the high-frequency portion of the bat soundscape (> 45 kHz), while communication sounds are broadband and carry most power at low frequencies (20–25 kHz). Our results showed that mutual information between neuronal responses and acoustic stimuli, as well as response redundancy in pairs of neurons recorded simultaneously, increase exponentially with IC depth. The latter occurs regardless of the sound type presented to the bats (echolocation or communication). Taken together, our results indicate the existence of mutual information and redundancy maps at the midbrain level whose response cannot be predicted based on the frequency composition of natural sounds and classic neuronal tuning curves.

Passive acoustic monitoring to assess depredation of killer whales on demersal longlines during soaking

Toothed whales feeding on fish caught on longlines is a growing issue worldwide. This issue named depredation has a serious socio-economic impact and raise conservation questions. In the French Patagonian toothfish fishery (Southern Ocean), a good understanding of the depredation behavior by killer whales is urgently needed to find adequate mitigation solutions. However, depredation on demersal longlines has been historically assessed from surface observation during hauling phases, thus the underwater dimension of depredation is not understood. Here, we used passive acoustic monitoring to record echolocation activity of killer whales and fishing vessels’ acoustic signatures during the fishing activity. Fixed hydrophone deployed on soaking longlines without any fishing activity nearby has recorded echolocation sounds. These recordings suggest that killer whales were feeding within the vicinity of longlines and thus very likely depredating on soaking longlines. Additionally, we also investigated fishing vessels’ acoustic signatures. We observed differences of acoustic cues emitted by the vessels between the setting and hauling phases. This suggests that killer whales may be able to recognize the boat activity and therefore localize longline positions to depredate.

Bat-inspired signal design for target discrimination in human echolocation

Echolocating bats exhibit sophisticated sonar behaviors using ultrasounds with actively adjusted acoustic characteristics (e.g., frequency and time-frequency structure) depending on the situation. In this study, the utility of ultrasound in human echolocation was examined. By listening to ultrasonic echoes with a shifted pitch to be audible, the participants (i.e., sighted echolocation novices) could discriminate the three-dimensional (3D) roundness of edge contours. This finding suggests that sounds with suitable wavelengths (i.e., ultrasounds) can provide useful information about 3D shapes. In addition, the shape, texture, and material discrimination experiments were conducted using ultrasonic echoes binaurally measured with a 1/7 scaled miniature dummy head. The acoustic and statistical analyses showed that intensity and timbre cues were useful for shape and texture discriminations, respectively. Furthermore, in the discrimination of objects with various features (e.g., acrylic board and artificial grass), the perceptual distances between objects were more dispersed when frequency-modulated sweep signals were used than when a constant-frequency signal was used. These suggest that suitable signal design, i.e., echolocation sounds employed by bats, allowed echolocation novices to discriminate the 3D shape and texture. This top-down approach using human subjects may be able to efficiently help interpret the sensory perception, "seeing by sound," in bat biosonar.

Biosonar interpulse intervals and pulse-echo ambiguity in four species of echolocating bats.

In complex biosonar scenes, the delay of echoes represents the spatial distribution of objects in depth. To avoid overlap of echo streams from successive broadcasts, individual echolocation sounds should only be emitted after all echoes of previous sounds have returned. However, close proximity of obstacles demands rapid pulse updates for steering to avoid collisions, which often means emitting a new sound before all of the previous echoes have returned. When two echo streams overlap, there is ambiguity about assigning echoes to the corresponding broadcasts. In laboratory tests of flight in dense, cluttered scenes, four species of echolocating bats exhibited different patterns of pulse emissions to accommodate potential pulse-echo ambiguity. Miniopterus fuliginosus emitted individual FM pulses only after all echoes of previous pulses had returned, with no alternating between long and short intervals. Pipistrellus abramus and Eptesicus fuscus alternated between emitting long FM pulse intervals to receive all echoes before the next pulse, and short intervals to update the rapidly changing scene while accepting partial overlap of successive echo streams. Rhinolophus ferrumequinum nippon transmitted CF/FM pulses in alternating short and long intervals, usually two to four closely spaced sounds that produced overlapping echo streams, followed by a longer interval that separated echo streams. Rhinolophus f. nippon is a statistical outlier from the three FM species, which are more similar to each other. The repeated overlap of CF/FM echo streams suggests that CF components have a distinct role in rejection of clutter and mitigation of ambiguity.

Adaptive frequency shifts of echolocation sounds in Miniopterus fuliginosus according to the frequency-modulated pattern of jamming sounds.

When flying in a group, echolocating bats have to separate their own echoes from pulses and echoes belonging to other individuals to extract only the information necessary for their own navigation. Previous studies have demonstrated that frequency-modulated (FM) bats change the terminal frequencies (TFs) of downward FM pulses under acoustic interference. However, it is not yet clear which acoustic characteristics of the jamming signals induce the TF shift according to the degree of acoustic interference. In this study, we examined changes in the acoustic characteristics of pulses emitted by Miniopterus fuliginosus while presenting jamming stimuli with different FM patterns to the bat flying alone. Bats significantly altered their TFs when responding to downward (dExp) and upward (uExp) exponential FM sounds as well as to a constant-frequency (CF) stimulus, by approximately 1-2 kHz (dExp: 2.1±0.9 kHz; uExp: 1.7±0.3 kHz; CF: 1.3±0.4 kHz) but not for linear FM sounds. The feature common to the spectra of these three jamming stimuli is a spectrum peak near the TF frequency, demonstrating that the bats shift the TF to avoid masking of jamming sounds on the TF frequency range. These results suggest that direct frequency masking near the TF frequency range induces the TF shift, which simultaneously decreases the similarity between their own echolocation sounds and jamming signals.

Neural spike train similarity algorithm detects differences in temporal patterning of bat echolocation call sequences

Bats emit echolocation sounds in complex temporal sequences that change to accommodate dynamic surroundings. Efforts to quantify how these patterns change have included analysis of inter-pulse intervals, sonar sound groups, and changes in individual signal parameters. No standardized method has been adopted for quantifying whether sequences of echolocation calls are similar or different beyond these individual dimensions. Here, a new method is presented for assessing the similarity in temporal structure between trains of bat echolocation sounds. The spike-train similarity space (SSIMS) algorithm, originally designed for neural data analysis, was applied to determine which features of the environment influence temporal patterning of echolocation sounds emitted by flying big brown bats (Eptesicus fuscus). Using a relational point-process framework, SSIMS was able to discriminate between pulse sequences recorded in different flight environments, as well as to separate flights depending on the bat’s expectation of its surroundings based on previous experience.

Sperm whale long-range echolocation sounds revealed by ANTARES, a deep-sea neutrino telescope

Despite dedicated research has been carried out to adequately map the distribution of the sperm whale in the Mediterranean Sea, unlike other regions of the world, the species population status is still presently uncertain. The analysis of two years of continuous acoustic data provided by the ANTARES neutrino telescope revealed the year-round presence of sperm whales in the Ligurian Sea, probably associated with the availability of cephalopods in the region. The presence of the Ligurian Sea sperm whales was demonstrated through the real-time analysis of audio data streamed from a cabled-to-shore deep-sea observatory that allowed the hourly tracking of their long-range echolocation behaviour on the Internet. Interestingly, the same acoustic analysis indicated that the occurrence of surface shipping noise would apparently not condition the foraging behaviour of the sperm whale in the area, since shipping noise was almost always present when sperm whales were acoustically detected. The continuous presence of the sperm whale in the region confirms the ecological value of the Ligurian sea and the importance of ANTARES to help monitoring its ecosystems.

Using sounds for making decisions: greater tube-nosed bats prefer antagonistic calls over non-communicative sounds when feeding

ABSTRACTBats vocalize extensively within different social contexts. The type and extent of information conveyed via their vocalizations and their perceptual significance, however, remains controversial and difficult to assess. Greater tube-nosed bats, Murina leucogaster, emit calls consisting of long rectangular broadband noise burst (rBNBl) syllables during aggression between males. To experimentally test the behavioral impact of these sounds for feeding, we deployed an approach and place-preference paradigm. Two food trays were placed on opposite sides and within different acoustic microenvironments, created by sound playback, within a specially constructed tent. Specifically, we tested whether the presence of rBNBl sounds at a food source effectively deters the approach of male bats in comparison to echolocation sounds and white noise. In each case, contrary to our expectation, males preferred to feed at a location where rBNBl sounds were present. We propose that the species-specific rBNBl provides contextual information, not present within non-communicative sounds, to facilitate approach towards a food source.

Variation in frequency-modulated call type for different flight densities in Mexican Free-tailed bats

Mexican free-tailed bats (Tadarida brasiliensis) adapt their call type depending on multiple factors. These bats have two general types of echolocation sounds, frequency-modulated (FM) and constant frequency (CF). CF calls are generally produced during the search phase of foraging, and FM calls are used during approach, prey capture, and roost emergence. In this study, we examined how Mexican free-tailed bats adapt their calls during emergence to avoid echo interference. We extracted individual calls from within a 500-ms sample that corresponded to five different emergence density categories. We found that these bats produce eight different FM call types during emergence. For each call within the sample, we characterized the call shape and calculated different parameters (duration, start frequency, peak frequency, end frequency). We compared the acoustic parameters across density categories and call shape, and compared the distribution of call shape across density categories. The results indicate that the call parameters and call shape vary from bat to bat, but there is no clear trend that this variance is due to the bat density. Therefore, these bats are likely changing their call shape and frequency characteristics to distinguish their own echoes from those of other bats.

Richness of insectivorous bats in a chaparral area in the municipality of Tecate, Baja California, Mexico

Twenty species of bats have been reported in the state of Baja California, however, there is not much information available for this group due to the lack of local studies. Therefore, the objective of this study was to increase the knowledge about the actual existing chiropteran fauna in Tecate, Baja California. For this purpose, a combined sampling was performed by capturing specimens using mist nets and an ultrasonic bat detector. The sampling took place from September to November 2013 and from May to June 2014. Five species of the Vespertillionidae family were registered with mist nets, and the ultrasonic records detected 12 species of the Vespertilionidae, Molossidae and Phyllostomidae families. The fact that 4 scantly documented species were detected in the area (Eumops perotis, Lasiurus xanthinus, Lasiurus blossevillii and Myotis melanorhinus) is noteworthy. The results obtained provide the first data about echolocation sounds of bats in this locality. Thus, the information obtained in this research is relevant to the implementation of strategies for the conservation of bats in this area.