Avoidance of non-localizable obstacles in echolocating bats: A robotic model.

Most objects and vegetation making up the habitats of echolocating bats return a multitude of overlapping echoes. Recent evidence suggests that the limited temporal and spatial resolution of bio-sonar prevents bats from separately perceiving the objects giving rise to these overlapping echoes. Therefore, bats often operate under conditions where their ability to localize obstacles is severely limited. Nevertheless, bats excel at avoiding complex obstacles. In this paper, we present a robotic model of bat obstacle avoidance using interaural level differences and distance to the nearest obstacle as the minimal set of cues. In contrast to previous robotic models of bats, the current robot does not attempt to localize obstacles. We evaluate two obstacle avoidance strategies. First, the Fixed Head Strategy keeps the acoustic gaze direction aligned with the direction of flight. Second, the Delayed Linear Adaptive Law (DLAL) Strategy uses acoustic gaze scanning, as observed in hunting bats. Acoustic gaze scanning has been suggested to aid the bat in hunting for prey. Here, we evaluate its adaptive value for obstacle avoidance when obstacles can not be localized. The robot's obstacle avoidance performance is assessed in two environments mimicking (highly cluttered) experimental setups commonly used in behavioral experiments: a rectangular arena containing multiple complex cylindrical reflecting surfaces and a corridor lined with complex reflecting surfaces. The results indicate that distance to the nearest object and interaural level differences allows steering the robot clear of obstacles in environments that return non-localizable echoes. Furthermore, we found that using acoustic gaze scanning reduced performance, suggesting that gaze scanning might not be beneficial under conditions where the animal has limited access to angular information, which is in line with behavioral evidence.

Variability in the rigid pinna motions of hipposiderid bats and their impact on sensory information encoding.

Many bat species, e.g., in the rhinolophid and hipposiderid families, have dynamic biosonar systems with highly mobile pinnae. Pinna motion patterns have been shown to fall into two distinct categories: rigid rotations and non-rigid motions (i.e., deformations). In the present work, two questions regarding the rigid rotations have been investigated: (i) what is the nature of the variability (e.g., discrete subgroups or continuous variation) within the rigid motions, (ii) what is its acoustic impact? To investigate the first question, rigid pinna motions in Pratt's leaf-nosed bats (Hipposideros pratti) have been tracked with stereo vision and a dense set of landmark points on the pinna surface. Axis-angle representations of the recorded rigid motions have shown a continuous variation in the rotation axes that covered a range of almost 180° in azimuth and elevation. To investigate the second question, the observed range of rigid pinna motions has been reproduced with a biomimetic pinna. Normalized mutual information between acoustic inputs associated with every pair of the rigid pinna motions showed that even small changes in the rotation axis resulted in more than 50% new sensory information encoding capacity (i.e., normalized mutual information less than 50%). This demonstrates a potential sensory benefit to the observed variability in the rigid pinna rotations.

Echolocating bats use future-target information for optimal foraging.

When seeing or listening to an object, we aim our attention toward it. While capturing prey, many animal species focus their visual or acoustic attention toward the prey. However, for multiple prey items, the direction and timing of attention for effective foraging remain unknown. In this study, we adopted both experimental and mathematical methodology with microphone-array measurements and mathematical modeling analysis to quantify the attention of echolocating bats that were repeatedly capturing airborne insects in the field. Here we show that bats select rational flight paths to consecutively capture multiple prey items. Microphone-array measurements showed that bats direct their sonar attention not only to the immediate prey but also to the next prey. In addition, we found that a bat's attention in terms of its flight also aims toward the next prey even when approaching the immediate prey. Numerical simulations revealed a possibility that bats shift their flight attention to control suitable flight paths for consecutive capture. When a bat only aims its flight attention toward its immediate prey, it rarely succeeds in capturing the next prey. These findings indicate that bats gain increased benefit by distributing their attention among multiple targets and planning the future flight path based on additional information of the next prey. These experimental and mathematical studies allowed us to observe the process of decision making by bats during their natural flight dynamics.

Volitional control of social vocalisations and vocal usage learning in bats.

Bats are gregarious, highly vocal animals that possess a broad repertoire of social vocalisations. For in-depth studies of their vocal behaviours, including vocal flexibility and vocal learning, it is necessary to gather repeatable evidence from controlled laboratory experiments on isolated individuals. However, such studies are rare for one simple reason: eliciting social calls in isolation and under operant control is challenging and has rarely been achieved. To overcome this limitation, we designed an automated setup that allows conditioning of social vocalisations in a new context and tracks spectro-temporal changes in the recorded calls over time. Using this setup, we were able to reliably evoke social calls from temporarily isolated lesser spear-nosed bats (Phyllostomus discolor). When we adjusted the call criteria that could result in a food reward, bats responded by adjusting temporal and spectral call parameters. This was achieved without the help of an auditory template or social context to direct the bats. Our results demonstrate vocal flexibility and vocal usage learning in bats. Our setup provides a new paradigm that allows the controlled study of the production and learning of social vocalisations in isolated bats, overcoming limitations that have, until now, prevented in-depth studies of these behaviours.

An experimental test of effects of ambient temperature and roost quality on aggregation by little brown bats (Myotis lucifugus).

Environmental factors, such as ambient temperature (Ta) or roost/nest quality, can influence social behaviour of small-bodied endotherms because individuals may aggregate for social thermoregulation when Ta is low or select the warmest possible sites for roosting. Female temperate bats form maternity colonies in spring to communally raise pups and exploit social thermoregulation. They also select roosts with warm microclimates because low roost temperature (Troost) delays juvenile development. We studied captive female little brown bats (Myotis lucifugus) to test the hypothesis that variation in Ta and Troost influence social group size. First, we predicted that female bats would preferentially select artificially heated roosts over unheated roosts. Second, we predicted that, as Ta decreased, group size would increase because bats would rely more heavily on social thermoregulation. Third, we predicted that experimentally increasing Troost (i.e., roost quality) above Ta would result in larger group sizes due to greater aggregation in high quality roosts. We captured 34 females from a maternity colony and housed them in a flight-tent provisioned with four bat boxes. Each box was outfitted with a heating pad and thermostat. Over the course of eight-days we heated each roost box in sequence to near thermoneutral Troost for two days. Bats preferentially selected heated roosts over unheated roosts but, contrary to our prediction, group size decreased when Troost was much greater than Ta (i.e., when the benefits of a warm roost should have been highest). Our results suggest that social thermoregulation and the availability of warm roosts influence aggregation in bats and have implications for the potential of summer habitat protection and enhancement to help bat populations in the face of threats like white-nose syndrome.

Noise interference with echo delay discrimination in bat biosonar.

Echolocating big brown bats (Eptesicus fuscus) were trained in a two-choice task to discriminate differences in the delay of electronic echoes at 1.7 ms delay (30 cm simulated range). Difference thresholds (∼45 µs) were comparable to previously published results. At selected above-threshold differences (116 and 232 µs delay), performance was measured in the presence of wideband random noise at increasing amplitudes in 10-dB steps to determine the noise level that prevented discrimination. Performance eventually failed, but the bats increased the amplitude and duration of their broadcasts to compensate for increasing noise, which allowed performance to persist at noise levels about 25 dB higher than without compensation. In the 232-µs delay discrimination condition, echo signal-to-noise ratio (2E/N0) was 8-10 dB at the noise level that depressed performance to chance. Predicted echo-delay accuracy using big brown bat signals follows the Cramér-Rao bound for signal-to-noise ratios above 15 dB, but worsens below 15 dB due to side-peak ambiguity. At 2E/N0 = 7-10 dB, predicted Cramér-Rao delay accuracy would be about 1 µs; considering side-peak ambiguity it would be about 200-300 µs. The bats' 232 µs performance reflects the intrusion of side-peak ambiguity into delay accuracy at low signal-to-noise ratios.

Three-dimensional sonar beam-width expansion by Japanese house bats (Pipistrellus abramus) during natural foraging.

Three-dimensional directivity patterns of sonar sounds emitted by Japanese house bats (Pipistrellus abramus) during natural foraging were measured by a 44-channel microphone array. Just before prey capture, the terminal frequency (TF) of emitted sounds decreased, and the beam width (mean ± standard deviation) expanded from 40 ± 10° to 63 ± 9° (horizontal) and from 32 ± 10° to 52 ± 7° (vertical). P. abramus decrease the TF to simultaneously expand the beam width in both the horizontal and vertical planes, while retaining the target within the three-dimensional acoustic field of view at the final stage of capture.

Frequency shifting reduces but does not eliminate acoustic interference between echolocating bats: A theoretical analysis.

Bats have been observed to shift the frequency of their echolocation calls in the presence of other echolocating bats, ostensibly as a way to reduce acoustic interference. Few studies, however, have examined the theoretical efficacy of such jamming avoidance responses. The present study uses the wideband ambiguity function to analyze the effects of acoustic interference from conspecifics and congeneric heterospecifics on the target acquisition ability of Myotis californicus and Myotis yumanensis, specifically whether unilateral or bilateral frequency shifts reduce the effects of such interference. Model results suggest that in conspecific interactions, M. yumanensis recovers its target acquisition ability more completely and with less absolute frequency shift than does M. californicus, but that alternative methods of jamming avoidance may be easier to implement. The optimal strategy for reducing heterospecific interference is for M. californicus to downshift its call and M. yumanensis to upshift its call, which exaggerates a preexisting difference in mean frequency between the calls of the two species. Further empirical research would elucidate whether these species do in practice actively employ frequency shifting or other means for jamming avoidance, as well as illuminate the role of acoustic interference in niche partitioning.

The origins and diversity of bat songs.

Singing plays an important role in the social lives of several disparate bat species, but just how significant the behavior may be among bats generally is unknown. Recent discoveries suggest singing by bats might be surprisingly more diverse and widespread than anticipated, but if true then two questions must be addressed: firstly why has singing been so rarely documented among bats, and secondly do bats sing for the same reasons as songbirds? We address the first question by reviewing how sampling bias and technical constraints may have produced a myopic view of bat social communication. To address the second question, we review evidence from 50 years of batsong literature supporting the supposition that bat singing is linked to the same constellation of ecological variables that favored birdsong, including territoriality, polygyny, metabolic constraints, migratory behaviors and especially powered flight. We propose that bats sing like birds because they fly like birds; flight is energetically expensive and singing reduces time spent flying. Factoring in the singular importance of acoustic communication for echolocating bats, it seems likely that singing may prove to be relatively common among certain groups of bats once it becomes clear when and where to look for it.

Distress vocalization sequences broadcasted by bats carry redundant information.

Distress vocalizations (also known as alarm or screams) are an important component of the vocal repertoire of a number of animal species, including bats, humans, monkeys and birds, among others. Although the behavioral relevance of distress vocalizations is undeniable, at present, little is known about the rules that govern vocalization production when in alarmful situations. In this article, we show that when distressed, bats of the species Carollia perspicillata produce repetitive vocalization sequences in which consecutive syllables are likely to be similar to one another regarding their physical attributes. The uttered distress syllables are broadband (12-73 kHz) with most of their energy focussing at 23 kHz. Distress syllables are short (~4 ms), their average sound pressure level is close to 70 dB SPL, and they are produced at high repetition rates (every 14 ms). We discuss that, because of their physical attributes, bat distress vocalizations could serve a dual purpose: (1) advertising threatful situations to conspecifics, and (2) informing the threatener that the bats are ready to defend themselves. We also discuss possible advantages of advertising danger/discomfort using repetitive utterances, a calling strategy that appears to be ubiquitous across the animal kingdom.

Learning where to feed: the use of social information in flower-visiting Pallas' long-tongued bats (Glossophaga soricina).

Social learning is a widespread phenomenon among vertebrates that influences various patterns of behaviour and is often reported with respect to foraging behaviour. The use of social information by foraging bats was documented in insectivorous, carnivorous and frugivorous species, but there are little data whether flower-visiting nectarivorous bats (Phyllostomidae: Glossophaginae) can acquire information about food from other individuals. In this study, we conducted an experiment with a demonstrator-observer paradigm to investigate whether flower-visiting Pallas' long-tongued bats (Glossophaga soricina) are able to socially learn novel flower positions via observation of, or interaction with, knowledgeable conspecifics. The results demonstrate that flower-visiting G. soricina are able to use social information for the location of novel flower positions and can thereby reduce energy-costly search efforts. This social transmission is explainable as a result of local enhancement; learning bats might rely on both visual and echo-acoustical perception and are likely to eavesdrop on auditory cues that are emitted by feeding conspecifics. We additionally tested the spatial memory capacity of former demonstrator bats when retrieving a learned flower position, and the results indicate that flower-visiting bats remember a learned flower position after several weeks.

Sensory challenges for trawling bats: Finding transient prey on water surfaces.

Bats are able to identify obstacles and prey objects based exclusively on acoustic information acquired via echolocation. To assess the echo information potentially available to the trawling bat Noctilio leporinus, prey objects were ensonified with artificial bat calls and deduced echo target strengths (TS) of the reflected signals. The artificial calls consisted either of constant frequency (CF) or frequency modulated (FM) sounds. Detection distances were calculated for call intensities of N. leporinus emitted in the field and in confined space. Measurements of a transient target consisting of a brief water splash and subsequently expanding water ripples revealed that concentrically expanding water ripples can provide sufficiently loud echoes to be detected by trawling bats. Experiments with stationary targets revealed differences in TS depending on the type of signal used (CF or FM). A calculated maximum detection distance between 4.5 and 13.7 m for all measured targets indicates that prey detection in this very loud calling species occurs much earlier than suggested by estimations based on modifications in echolocation or flight behavior.

An assessment of the direction-finding accuracy of bat biosonar beampatterns.

In the biosonar systems of bats, emitted acoustic energy and receiver sensitivity are distributed over direction and frequency through beampattern functions that have diverse and often complicated geometries. This complexity could be used by the animals to determine the direction of incoming sounds based on spectral signatures. The present study has investigated how well bat biosonar beampatterns are suited for direction finding using a measure of the smallest estimator variance that is possible for a given direction [Cramér-Rao lower bound (CRLB)]. CRLB values were estimated for numerical beampattern estimates derived from 330 individual shape samples, 157 noseleaves (used for emission), and 173 outer ears (pinnae). At an assumed 60 dB signal-to-noise ratio, the average value of the CRLB was 3.9°, which is similar to previous behavioral findings. Distribution for the CRLBs in individual beampatterns had a positive skew indicating the existence of regions where a given beampattern does not support a high accuracy. The highest supported accuracies were for direction finding in elevation (with the exception of phyllostomid emission patterns). No large, obvious differences in the CRLB (greater 2° in the mean) were found between the investigated major taxonomic groups, suggesting that different bat species have access to similar direction-finding information.

Bats in a Mediterranean Mountainous Landscape: Does Wind Farm Repowering Induce Changes at Assemblage and Species Level?

We reported data on flying bat assemblages in a Mediterranean mountain landscape of central Italy on a 5-year time span (2005-2010) where a wind farm repowering has been carried out (from 2009, 17 three-blade turbines substituted an a priori set of one-blade turbines). In 4 yearly based surveys, we calculated a set of univariate metrics at species and assemblage level and also performing a diversity/dominance analysis (k-dominance plots) to evaluate temporal changes. Nine species of bats were present (eight classified at species level, one at genus level). Number of detected taxa, Margalef richness, and Shannon-Wiener diversity apparently decreased between 2005-2007 (one-blade turbine period) and 2009-2010 (three-blade turbines period). We showed a weak temporal turnover only between 2007 and 2009. In k-dominance plots, the occurrence curves of the years before the new wind farming activity (2005 and 2007) were lower when compared to the curves related to the 2009 and 2010 years, suggesting an apparent stress at assemblage level in the second period (2009 and 2010). Myotis emarginatus and Pipistrellus pipistrellus significantly changed their relative frequency during the three-blade wind farming activity, supporting the hypothesis that some bats may be sensitive to repowering. Further research is necessary to confirm a possible sensitivity also for locally rare bats (Miniopterus schreibersii and Plecotus sp.).

Clutter and conspecifics: a comparison of their influence on echolocation and flight behaviour in Daubenton's bat, Myotis daubentonii.

We compared the influence of conspecifics and clutter on echolocation and flight speed in the bat Myotis daubentonii. In a large room, actual pairs of bats exhibited greater disparity in peak frequency (PF), minimum frequency (F MIN) and call period compared to virtual pairs of bats, each flying alone. Greater inter-individual disparity in PF and F MIN may reduce acoustic interference and/or increase signal self-recognition in the presence of conspecifics. Bats flying alone in a smaller flight room, to simulate a more cluttered habitat as compared to the large flight room, produced calls of shorter duration and call period, lower intensity, and flew at lower speeds. In cluttered space, shorter call duration should reduce masking, while shorter call period equals more updates to the bat's auditory scene. Lower intensity likely reflects reduced range detection requirements, reduced speed the demands of flying in clutter. Our results show that some changes (e.g. PF separation) are associated with conspecifics, others with closed habitat (e.g. reduced call intensity). However, we demonstrate that call duration, period, and flight speed appear similarly influenced by conspecifics and clutter. We suggest that some changes reduce conspecific interference and/or improve self-recognition, while others demonstrate that bats experience each other like clutter.

Prey pursuit strategy of Japanese horseshoe bats during an in-flight target-selection task.

The prey pursuit behavior of Japanese horseshoe bats (Rhinolophus ferrumequinum nippon) was investigated by tasking bats during flight with choosing between two tethered fluttering moths. Echolocation pulses were recorded using a telemetry microphone mounted on the bat combined with a 17-channel horizontal microphone array to measure pulse directions. Flight paths of the bat and moths were monitored using two high-speed video cameras. Acoustical measurements of returning echoes from fluttering moths were first collected using an ultrasonic loudspeaker, turning the head direction of the moth relative to the loudspeaker from 0° (front) to 180° (back) in the horizontal plane. The amount of acoustical glints caused by moth fluttering varied with the sound direction, reaching a maximum at 70°-100° in the horizontal plane. In the flight experiment, moths chosen by the bat fluttered within or moved across these angles relative to the bat's pulse direction, which would cause maximum dynamic changes in the frequency and amplitude of acoustical glints during flight. These results suggest that echoes with acoustical glints containing the strongest frequency and amplitude modulations appear to attract bats for prey selection.

Are torpid bats immune to anthropogenic noise?

Anthropogenic noise has a negative impact on a variety of animals. However, many bat species roost in places with high levels of anthropogenic noise. Here, we tested the hypothesis that torpid bats are insensitive to anthropogenic noise. In a laboratory experiment, we recorded skin temperature (Tsk) of bats roosting individually that were subjected to playbacks of different types of noise. We found that torpid bats with Tsk ~10°C lower than their active Tsk responded to all types of noise by elevating Tsk. Bats responded most strongly to colony and vegetation noise, and most weakly to traffic noise. The time of day when torpid bats were exposed to noise had a pronounced effect on responses. Torpid bats showed increasing responses from morning towards evening, i.e. towards the onset of the active phase. Skin temperature at the onset of noise exposure (Tsk,start, 17-29°C) was not related to the response. Moreover, we found evidence that torpid bats rapidly habituated to repeated and prolonged noise exposure.

Dynamic adjustment of echolocation pulse structure of big-footed myotis (Myotis macrodactylus) in response to different habitats.

Studying relationships between characteristics of sonar pulses and habitat clutter level is important for the understanding of signal design in bat echolocation. However, most studies have focused on overall spectral and temporal parameters of such vocalizations, with focus less on potential variation in frequency modulation rates (MRs) occurring within each pulse. In the current study, frequency modulation (FM) characteristics were examined in echolocation pulses recorded from big-footed myotis (Myotis macrodactylus) bats as these animals searched for prey in five habitats differing in relative clutter level. Pulses were analyzed using ten parameters, including four structure-related characters which were derived by dividing each pulse into three elements based on two knees in the FM sweep. Results showed that overall frequency, pulse duration, and MR all varied across habitat. The strongest effects were found for MR in the body of the pulse, implying that this particular component plays a major role as M. macrodactylus, and potentially other bat species, adjust to varying clutter levels in their foraging habitats.

High resolution acoustic measurement system and beam pattern reconstruction method for bat echolocation emissions.

Measurements of the transmit beam patterns emitted by echolocating bats have previously been limited to cross-sectional planes or averaged over multiple signals using sparse microphone arrays. To date, no high-resolution measurements of individual bat transmit beams have been reported in the literature. Recent studies indicate that bats may change the time-frequency structure of their calls depending on the task, and suggest that their beam patterns are more dynamic than previously thought. To investigate beam pattern dynamics in a variety of bat species, a high-density reconfigurable microphone array was designed and constructed using low-cost ultrasonic microphones and custom electronic circuitry. The planar array is 1.83 m wide by 1.42 m tall with microphones positioned on a 2.54 cm square grid. The system can capture up to 228 channels simultaneously at a 500 kHz sampling rate. Beam patterns are reconstructed in azimuth, elevation, and frequency for visualization and further analysis. Validation of the array measurement system and post-processing functions is shown by reconstructing the beam pattern of a transducer with a fixed circular aperture and comparing the result with a theoretical model. To demonstrate the system in use, transmit beam patterns of the big brown bat, Eptesicus fuscus, are shown.

Time-mapping and future-oriented behavior in free-ranging wild fruit bats.

Episodic memory and mental time travel have been viewed as uniquely human traits.1,2,3 This view began to shift with the development of behavioral criteria to assess what is referred to as "episodic-like memory" in animals.4,5 Key findings have ranged from evidence of what-where-when memory in scrub-jays, rats, and bees; through decision-making that impacts future foraging in frugivorous primates; to evidence of planning based on future needs in scrub-jays and tool use planning in great apes.4,6,7,8,9,10,11,12,13 Field studies of these issues have been rare, though there is field-based evidence for future-oriented behaviors in primates.8,10,14,15 We report evidence that free-ranging wild fruit bats rely on mental temporal maps and exhibit future-oriented behaviors when foraging. We tracked young bats as they navigated and foraged, documenting every tree they visited over many months. We prevented the bats from foraging outside for different time periods and monitored their foraging decisions, revealing that the bats map the spatiotemporal patterns of resources in their environment. Following a long period in captivity, the bats did not visit those trees that were no longer providing fruit. We show that this time-mapping ability requires experience and is lacking in inexperienced bats. Careful analysis of the bats' movement and foraging choices indicated that they plan which tree to visit while still in the colony, thus exhibiting future-oriented behavior and delayed gratification on a nightly basis. Our findings demonstrate how the need for spatiotemporal mental mapping can drive the evolution of high cognitive abilities that were previously considered exclusive to humans.