Echolocation while drinking: Pulse-timing strategies by high- and low-frequency FM bats

During nightly foraging activity, echolocating bats drink by flying low over the water surface and dipping the lower jaw while avoiding further bodily contact with the water. This task poses different sensorimotor challenges than flying in the open to forage for insects. Of interest is how bats adjust the timing of their echolocation pulses to accommodate the surrounding scene, from the progressively nearer water surface itself to objects at longer distances. Drinking behavior has been described in only a few of the roughly 1,000 echolocating bat species, and in none of the 110 species in the Indian subcontinent. Here, we describe how bats emitting frequency-modulated (FM) echolocation pulses behaved while drinking from a swimming pool in urban northeast India. At least two different bat species were present, using 1st-harmonic frequencies sweeping down to about 35 Hz ("low frequency") and down to about 50 kHz ("high frequency"), separable at a 40 kHz boundary. Over entire drinking maneuvers, intervals between broadcast pulses accommodate both the proximate task of registering the water surface while drinking and registering echoes from the farther reaches of the scene. During approach to the water, both low and high frequency bats emit longer, more stable interpulse intervals that matched the time interval covering echo arrival-times out to the frequency-dependent maximum operating range. High frequency bats use shorter interpulse intervals than low frequency bats, consistent with the shorter operating range at higher frequencies. Bats then accelerate their pulse rate to guide the dive down to drinking, with low frequency bats continuing to decrease pulse intervals and high frequency bats maintaining a more steady interval during the drinking buzz. The circumstance that both groups were engaged in the same task made this a natural experiment on the behavior during approach.

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title: Biosonar interpulse intervals and pulse-echo ambiguity in four species of echolocating bats
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title: Energetics and Water Flux of Free-Ranging Big Brown Bats (Eptesicus fuscus) during Pregnancy and Lactation
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title: Energy budgets of lactating and non-reproductive Brown Long-Eared Bats (Plecotus auritus) suggest females use compensation in lactation
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5. Respiratory DEE for lactating bats was equal to or less than that of non-reproductive females, suggesting they used compensatory mechanisms in their energy budgets in lactation.

title: Directionality of Drinking Passes by Bats at Water Holes: is there Cooperation?
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title: Potential Effects of Livestock Water-Trough Modifications on Bats in Northern Arizona
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title: Innate recognition of water bodies in echolocating bats
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title: Sensory Ecology of Water Detection by Bats: A Field Experiment
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title: Echolocating bats emit terminal phase buzz calls while drinking on the wing
abstract: Echolocating bats are known to produce terminal buzz calls during pursuit and capture of airborne prey, however the use of buzz calls while drinking on the wing has not been previously investigated. In this study I recorded the first empirical evidence that bats produce terminal phase buzz calls while drinking on the wing. Every drinking pass recorded during this study was characterised by a terminal buzz which bats emitted immediately prior to touching the water surface with their mouth. The characteristic frequency (the frequency at the end or flattest portion of the pulse) of echolocation call sequences containing drinking buzzes varied from 25kHz to 50kHz, suggesting multiple bat species present at the study site emit buzzes while drinking on the wing. As feeding buzz calls appear to be ubiquitous among echolocating bat taxa, the prevalence of drinking buzzes clearly warrants further investigation. Drinking buzzes could potentially be used to document rates of drinking by bats in the same way that feeding buzzes are used to infer foraging activity.

title: The Buzz of Drinking on the Wing in Echolocating Bats
abstract: Bats broadcast rapid sequences of echolocation calls, named ‘drinking buzzes’, when they approach water to drink on the wing. So far this phenomenon has received little attention. We recorded echolocation sequences of drinking bats for 12 species, for 11 of which we also recorded feeding buzzes. Based on the different sensorial tasks faced by feeding and drinking bats, we hypothesize that the drinking buzz structure will differ from that of feeding buzzes since unlike the latter drinking buzzes are not designed to detect and track mobile prey. We demonstrated that drinking buzzes are structurally different from feeding buzzes. We show that the buzz-II phase common in feeding buzzes is absent in drinking buzzes; that is, call frequency is not lowered to broaden sonar beam since the task of drinking does not imply tracking fast-moving targets. This finding indirectly confirms the role of buzz II in feeding buzzes. Pulse rate in drinking buzzes is also lower than in feeding buzzes, as predicted since the high pulse rate typical of feeding buzzes is important to update rapidly the relative location of moving targets. The most likely function of drinking buzzes is to guide a safe drinking manoeuvre, similar to ‘landing buzzes’ broadcast when bats land on the ground.

title: Acoustic mirrors as sensory traps for bats
abstract: Building-blind bats Human-generated structures now dominate much of the planet, but they have existed for but a blink of an eye from an evolutionary perspective. Animal sensory systems evolved to navigate natural environments and so may not always be reliable in anthropogenic ones. Greif et al. show that echolocating bats appear to perceive smooth vertical surfaces as open areas, a mistake that often leads to collisions (see the Perspective by Stilz). With millions upon millions of smooth vertical surfaces in our world today, such misperceptions could have considerable negative impacts on bat survival. Science, this issue p. 1045; see also p. 977 Smooth vertical surfaces trick bat sensory systems. Sensory traps pose a considerable and often fatal risk for animals, leading them to misinterpret their environment. Bats predominantly rely on their echolocation system to forage, orientate, and navigate. We found that bats can mistake smooth, vertical surfaces as clear flight paths, repeatedly colliding with them, likely as a result of their acoustic mirror properties. The probability of collision is influenced by the number of echolocation calls and by the amount of time spent in front of the surface. The echolocation call analysis corroborates that bats perceive smooth, vertical surfaces as open flyways. Reporting on occurrences with different species in the wild, we argue that it is necessary to more closely monitor potentially dangerous locations with acoustic mirror properties (such as glass fronts) to assess the true frequency of fatalities around these sensory traps.

title: The role of the flight membranes in insect capture by bats
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title: The echolocation of flying insects by bats
abstract: Bats of the genus Myotis ( M. lucifugus , M. subulatus leibii and M. keenii septentrionalis ) have been studied while pursuing and capturing small insects under laboratory conditions. It is apparently important to provide fairly large numbers of such insects in order to elicit insect catching behaviour indoors. 2. 2. Insect catches are individually directed pursuit manoeuvres; each insect is detected, located, and intercepted in flight within about half a second. 3. 3. Certain individual bats caught mosquitos ( Culex quinquefaciatus ) and fruit flies ( Drosophila robusta and D. melanogaster ) at remarkably high rates which could be measured conservatively by the gain in weight of the bat. Sometimes a bat would average as many as 10 mosquitos or 14 fruit flies per minute during a period of several minutes. In four cases motion pictures showed two separate Drosophila catches within half a second. 4. 4. The orientation sounds of the hunting bat are adjusted in a manner that seems appropriate for the echolocation of single insects one at a time. There is a search phase before the occurrence of any apparent reaction to the insect. In this phase the frequency drops from about 100 to 50 kilocycles during each pulse of sound, and the pulses are emitted by M. lucifugus at intervals of 50 to 100 milliseconds. 5. 5. When an insect is detected the search phase gives way to an approach phase characterized by a progressive shortening of the pulse-to-pulse interval and, if necessary, a sharp turn towards the insect. In this phase the pulse duration may shorten somewhat, but the frequencies remain approximately the same as in the search phase or drop slightly. 6. 6. When the bat is within a few centimetres of the insect there is a terminal phase in which the pulse duration and interval between pulses shorten to about 0·5 millisecond and 5 or 6 milliseconds respectively. Contrary to a conclusion reached earlier on the basis of much less adequate data ( Griffin, 1953 ), the frequency drops in the terminal phase, sometimes to 25 or 30 kilocycles. This is the buzz, which also occurs in many cases when the bat is dodging wires or landing. 7. 7. The distance from the insect at which detection occurs can be judged by the shift from search to approach patterns. This distance of detection is commonly about 50 cm. for Drosophila , and it occasionally may be as much as a metre with fruit flies or mosquitos. 8. 8. Two M. lucifugus which had become adept at catching Drosophila in the laboratory were exposed to broad band thermal noise either at low frequencies (0·1–15 kilocycles) or high (20–100 kilocycles). The low frequency noise had an approximately uniform spectrum level of about 50 decibels per cycle band width (re 0·0002 dyne/cm 2 ) from 0·1 to 8 kilocycles. It was thus very loud compared to the flight sounds of Drosophila which have a fundamental frequency of a few hundred cycles/second and a maximum sound pressure level of 20–25 decibels at the distances of detection by these bats. The high frequency noise was of low and varying intensity, but it discouraged or prevented insect catching. The low frequency noise, on the other hand, had no effect on insect catching; the bats gained weight in this noise (and in the dark) just as rapidly as in the quiet. Although bats sometimes detect insect prey by passive listening to sounds emanating from the insects themselves, these experiments appear to us to establish conclusively that small and relatively silent insects are often detected by echolocation.

title: Natterer’s bat (Myotis nattereri Kuhl, 1818) hawks for prey close to vegetation using echolocation signals of very broad bandwidth
abstract: We present a hitherto unknown prey perception strategy in bats: Myotis nattereri (Vespertilionidae, Chiroptera) is able to perceive prey by echolocation within a few centimeters of echo-cluttering vegetation, by using frequency-modulated search signals of very large bandwidth (up to 135 kHz). We describe the species’ search behavior and echolocation repertoire from the field and from experiments in a flight tent. In the field, bats varied signal parameters in relation to their distance from vegetation and usually flew close to vegetation. In the flight tent, M. nattereri detected and localized prey by echolocation alone as close as 5 cm from vegetation. Apparently, the bats were able to tolerate some overlap between prey and clutter echoes. Passive prey cues (vision, olfaction, prey-generated sounds) were not used in prey perception. The bats selected prey by size. The animals performed aerial catches and produced approach sequences typical for aerial hawking bats, but were able to do so within a few centimeters of the substrate. M. nattereri thus has access to silent, suspended prey very close to vegetation (e.g., spiders, and caterpillars on threads).

title: The sonar beam pattern of a flying bat as it tracks tethered insects.
abstract: This paper describes measurements of the sonar beam pattern of flying echolocating bats, Eptesicus fuscus, performing various insect capture tasks in a large laboratory flight room. The beam pattern is deduced using the signal intensity across a linear array of microphones. The positions of the bat and insect prey are obtained by stereoscopic reconstruction from two camera views. Results are reported in the form of beam-pattern plots and estimated direction of the beam axis. The bat centers its beam axis on the selected target with a standard deviation (sigma) of 3 degrees. The experimental error is +/- 1.4 degrees. Trials conducted with two targets show that the bat consistently tracks one of the targets with its beam. These findings suggest that the axis of the bat sonar beam is a good index of selective tracking of targets, and in this respect is analogous to gaze in predominantly visual animals.

title: How the bat got its buzz
abstract: Since the discovery of echolocation in bats, the final phase of an attack on a flying insect, the ‘terminal buzz’, has proved enigmatic. During the buzz, bats increase information update rates by producing vocalizations up to 220 times s−1. The buzz's ubiquity in hawking and trawling bats implies its importance for hunting success. Superfast muscles, previously unknown in mammals, are responsible for the extreme vocalization rate. Some bats produce a second phase—buzz II—defined by a large drop in the fundamental frequency (F0) of their calls. By doing so, bats broaden their acoustic field of view and should thereby reduce the likelihood of insect escape. We make the case that the buzz was a critical adaptation for capturing night-flying insects, and suggest that the drop in F0 during buzz II requires novel, unidentified laryngeal mechanisms in order to counteract increasing muscle tension. Furthermore, we propose that buzz II represents a countermeasure against the evasive flight of eared prey in the evolutionary arms-race that saw the independent evolution of bat-detecting ears in various groups of night-flying insects.

title: Performance of Airborne Animal Sonar Systems: I. Microchiroptera
abstract: Animals living in the dark are faced with the problem that vision is only of limited use for orientation in the environment and for the detection and identification of relevant targets. In order to cope with this situation, some animals, during evolution, developed eyes which were especially adapted for good visual efficiency at low light intensities whereas others improved the remaining sensory systems.

title: Controlling the false discovery rate: a practical and powerful approach to multiple testing
abstract: The common approach to the multiplicity problem calls for controlling the familywise error rate (FWER). This approach, though, has faults, and we point out a few. A different approach to problems of multiple significance testing is presented. It calls for controlling the expected proportion of falsely rejected hypotheses -the false discovery rate. This error rate is equivalent to the FWER when all hypotheses are true but is smaller otherwise. Therefore, in problems where the control of the false discovery rate rather than that of the FWER is desired, there is potential for a gain in power. A simple sequential Bonferronitype procedure is proved to control the false discovery rate for independent test statistics, and a simulation study shows that the gain in power is substantial. The use of the new procedure and the appropriateness of the criterion are illustrated with examples.

title: Bats adjust their mouth gape to zoom their biosonar field of view
abstract: This study shows how an animal actively and functionally controls its sensory field of view by means of changing its emitter aperture. This would be similar to a human ability to zoom in on a visual scene. The study was performed in a natural situation with wild bats. To perform the study, we developed tools to record and analyze bats’ beams and faces simultaneously. We show that bats rapidly and dramatically alter their biosonar field of view to functionally adjust sensory acquisition. They do so by changing their mouth gape. Hence, we show that bats change the shape of their emitter for active sensing. Active sensing, where sensory acquisition is actively modulated, is an inherent component of almost all sensory systems. Echolocating bats are a prime example of active sensing. They can rapidly adjust many of their biosonar parameters to optimize sensory acquisition. They dynamically adjust pulse design, pulse duration, and pulse rate within dozens of milliseconds according to the sensory information that is required for the task that they are performing. The least studied and least understood degree of freedom in echolocation is emission beamforming—the ability to change the shape of the sonar sound beam in a functional way. Such an ability could have a great impact on the bat’s control over its sensory perception. On the one hand, the bat could direct more energy into a narrow sector to zoom its biosonar field of view, and on the other hand, it could widen the beam to increase the space that it senses. We show that freely behaving bats constantly control their biosonar field of view in natural situations by rapidly adjusting their emitter aperture—the mouth gape. The bats dramatically narrowed the beam when entering a confined space, and they dramatically widened it within dozens of milliseconds when flying toward open space. Hence, mouth-emitting bats dynamically adjust their mouth gape to optimize the area that they sense with their echolocation system.

title: Anthropogenic Noise Alters Bat Activity Levels and Echolocation Calls
abstract: a b s t r a c t Negative impacts from anthropogenic noise are well documented for many wildlife taxa. Investigations of the effects of noise on bats however, have not been conducted outside of the laboratory. Bats that hunt arthropods rely on auditory information to forage. Part of this acoustic information can fall within the spectrum of anthropogenic noise, which can potentially interfere with signal reception and processing. Compressor stations associated with natural gas extraction produce broadband noise 24 hours a day, 365 days a year. With over half a million producing gas wells in the U.S. this infrastructure is a major source of noise pollution across the landscape. We conducted a ‘natural experiment’ in the second largest gas extraction field in the U.S. to investigate the potential effects of gas compressor station noise on the activity levels of the local bat assemblage. We used acoustic monitoring to compare the activity level (number of minutes in a night with a bat call) of the bat assemblage at sites with compressor stations to sites lacking this infrastructure. We found that activity levels for the Brazilian free-tailed bat (Tadarida brasiliensis) were 40% lower at loud compressor sites compared to quieter well pads, whereas the activity levels of four other species (Myotis californicus, M. cillolabrum, M. lucifugus, Parastrellus hesperus) were not affected by noise. Furthermore, our results reveal that the assemblage of bat species emitting low frequency ( 35 kHz) echolocation did not exhibit altered activity levels in noise. Lower activity levels of Brazilian free-tailed bats at loud sites indicate a potential reduction in habitat for this species. Additionally, a comparison of echolocation search calls produced by free-tailed bats at sites with and without compressor stations reveal that this species modifies its echolocation search calls in noise—producing longer calls with a narrower bandwidth. Call alterations might affect prey detection. These preliminary findings highlight the important need for further research of how anthropogenic noise af

title: Using echolocation monitoring to model bat occupancy and inform mitigations at wind energy facilities
abstract: Fatalities of migratory bats, many of which use low frequency (<35 kHz; LowF) echolocation calls, have become a primary environmental concern associated with wind energy development. Accordingly, strategies to improve compatibility between wind energy development and conservation of bat populations are needed. We combined results of continuous echolocation and meteorological monitoring at multiple stations to model conditions that explained presence of LowF bats at a wind energy facility in southern California. We used a site occupancy approach to model nightly LowF bat presence while accounting for variation in detection probability among echolocation detectors and heights. However, we transposed the spatial and temporal axes of the conventional detection history matrix such that occupancy represented proportion of nights, rather than monitoring points, on which LowF bats were detected. Detectors at 22 m and 52 m above ground had greater detection probabilities for LowF bats than detectors at 2 m above ground. Occupancy of LowF bats was associated with lower nightly wind speeds and higher nightly temperatures, mirroring results from other wind energy facilities. Nevertheless, we found that building separate models for each season and considering solutions with multiple covariates resulted in better fitting models. We suggest that use of multiple environmental variables to predict bat presence could improve efficiency of turbine operational mitigations (e.g., changes to cut-in speeds) over those based solely on wind speed. Increased mitigation efficiencies could lead to greater use of mitigations at wind energy facilities with benefits to bat populations.

title: Conspecifics influence call design in the Brazilian free-tailed bat, Tadarida brasiliensis
abstract: The Brazilian free-tailed bat, Tadarida brasiliensis (Saint-Hilaire, 1824), uses calls that represent a broad continuum of design variation which is dependent upon habitat and situation, and exhibits characteristic changes in call design as bats close in on airborne targets. Here we demonstrate the influence of conspecifics on call design. We found that the peak frequency used in calls varies more as the number of bats flying in the same space increases (measured from single bats and pairs of bats). We investigated this phenomenon through comparing call-parameter differences found between two bats recorded flying together (actual pairs) with call-parameter differences between two bats each recorded flying alone at different locations that were randomly assigned to one another (virtual pairs). We found that actual pairs of bats used calls which differed in peak frequency more so than did virtual pairs. This result is particularly striking given that these frequency differences were greater between bats in ...

title: Species and Acoustic Diversity of Bats in a Palaeotropical Wet Evergreen forest in Southern India
abstract: The Western Ghats of India is among the top 25 biodiversity hotspots in the world. About 43% of the reported 117 bat species in India are found in this region, but few quantitative studies of bat echolocation calls and diversity have been carried out here thus far. A quantitative study of bat diversity was therefore conducted using standard techniques, including mist-netting, acoustical and roost surveys in the wet evergreen forests of Kudremukh National Park in the Western Ghats of Karnataka. A total of 106 bats were caught over 108 sampling nights, representing 17 species, 3 belonging to Megachiroptera and 14 to Microchiroptera. Acoustical and roost surveys added three more species, two from Microchiroptera and one from Megachiroptera. Of these 20 species, 4 belonged to the family Pteropodidae, 10 to Vespertilionidae, 3 to Rhinolophidae, 2 to Megadermatidae and 1 to Hipposideridae. We recorded the echolocation calls of 13 of the 16 microchiropteran species, of which the calls of 4 species (Pipistrellus coromandra, Pipistrellus affinis, Pipistrellus ceylonicus and Harpiocephalus harpia) have been recorded for the first time. Discriminant function analyses of the calls of 11 species provided 91.7% correct classification of individuals to their respective species, indicating that the echolocation calls could be used successfully for non-invasive acoustic surveys and monitoring of bat species in the future.

title: Acoustic Identification of Bats in the Southern Western Ghats, India
abstract: Bats play crucial roles in ecosystems, are increasingly used as bio-indicators and are an important component of tropical diversity. Ecological studies and conservation-oriented monitoring of bats in the tropics benefit from published libraries of echolocation calls, which are not readily available for many tropical ecosystems. Here, we present the echolocation calls of 15 species from the Valparai plateau in the Anamalai Hills, southern Western Ghats of India: three rhinolophids (Rhinolophus beddomei, R. rouxii (indorouxii), R. lepidus), one hipposiderid (Hipposideros pomona), nine vespertilionids (Barbastella leucomelas darjelingensis, Hesperoptenus tickelli, Miniopterus fuliginosus, M. pusillus, Myotis horsfieldii, M. montivagus, Pipistrellus ceylonicus, Scotophilus heathii, S. kuhlii), one pteropodid (Rousettus leschenaultii) and one megadermatid (Megaderma spasma). Discriminant function analyses using leave-one-out cross validation classified bats producing calls with a strong constant frequency (CF) component with 100% success and bats producing frequency modulated (FM) calls with 90% success. For five species, we report their echolocation calls for the first time, and we present call frequencies for some species that differ from those published from other parts of the species' ranges. This exemplifies the need for more local call libraries from tropical regions to be collected and published in order to record endemic species and accurately identify species whose calls vary biogeographically.

title: Acoustic Identification of Otomops wroughtoni and other Free-Tailed Bat Species (Chiroptera: Molossidae) from India
abstract: The Wroughton's free-tailed bat Otomops wroughtoni (Chiroptera: Molossidae) is a globally rare and data-deficient species. This species has been recorded only from four locations, in India and Cambodia, with the type locality in the Barapede caves, India. In this paper, we present an analysis of echolocation and social calls of O. wroughtoni from the Barapede caves. Echolocation calls of free-flying O. wroughtoni were narrowband and shallow frequency-modulated (shallow-FM), with peak frequency ranging between 14–17 kHz. Social call sequences of roosting O. wroughtoni showed five distinct signatures. Multivariate analyses of echolocation calls of O. wroughtoni and the other three molossid species found in India (Tadarida teniotis, T. aegyptiaca, Chaerephon plicatus), showed strong support for acoustic differentiation of these species. Our study will help identify probable occurrence of O. wroughtoni and the other species in unsurveyed areas through field acoustic surveys. It also proposes hypotheses about the ecology and foraging behaviour of O. wroughtoni that could be tested through further studies.

title: A first record of three hitherto unreported species of bats from Kerala, India with a note on Myotis peytoni (Mammalia: Chiroptera: Vespertilionidae)
abstract: We provide specimen-based evidence and echolocation calls of an additional three species of bats in Kerala, India. A brief note on the taxonomy and nomenclature of Peyton’s Whiskered Myotis, and an updated checklist of bats of Kerala is also included.

title: Mammal Species of the World: A Taxonomic and Geographic Reference
abstract: Wilson and Reeder's Mammal Species of the World is the classic reference book on the taxonomic classification and distribution of the more than 5400 species of mammals that exist today. The third edition includes detailed information on nomenclature and, for the first time, common names. Each concise entry covers type locality, distribution, synonyms, and major reference sources. The systematic arrangement of information indicates evolutionary relationships at both the ordinal and the family level. This indispensable reference work belongs in public and academic libraries throughout the world and on the shelf of every biologist who works with mammals.

title: Target-detection by the echolocating bat,Eptesicus fuscus
abstract: SummaryThe long-range echo-detection capabilities of echolocating bats (Eptesicus fuscus) were studied in a two-choice psychophysical procedure.E. fuscus can detect 4.8 mm diameter spheres at a distance of 2.9 m, and 19.1 mm diameter spheres at a distance of 5.1 m. The threshold of echo-detection corresponds to the distance at which a target returns an echo amplitude in the region of 0 dB SPL. The results demonstrate that the maximum effective range of bat sonar is greater than previously indicated by obstacleavoidance and target-interception tasks.

title: Vespertilionid bats control the width of their biosonar sound beam dynamically during prey pursuit
abstract: Animals using sound for communication emit directional signals, focusing most acoustic energy in one direction. Echolocating bats are listening for soft echoes from insects. Therefore, a directional biosonar sound beam greatly increases detection probability in the forward direction and decreases off-axis echoes. However, high directionality has context-specific disadvantages: at close range the detection space will be vastly reduced, making a broad beam favorable. Hence, a flexible system would be very advantageous. We investigated whether bats can dynamically change directionality of their biosonar during aerial pursuit of insects. We trained five Myotis daubentonii and one Eptesicus serotinus to capture tethered mealworms and recorded their echolocation signals with a multimicrophone array. The results show that the bats broaden the echolocation beam drastically in the terminal phase of prey pursuit. M. daubentonii increased the half-amplitude angle from approximately 40° to approximately 90° horizontally and from approximately 45° to more than 90° vertically. The increase in beam width is achieved by lowering the frequency by roughly one octave from approximately 55 kHz to approximately 27.5 kHz. The E. serotinus showed beam broadening remarkably similar to that of M. daubentonii. Our results demonstrate dynamic control of beam width in both species. Hence, we propose directionality as an explanation for the frequency decrease observed in the buzz of aerial hawking vespertilionid bats. We predict that future studies will reveal dynamic control of beam width in a broad range of acoustically communicating animals.