Transmitter and receiver of the low frequency horseshoe bat Rhinolophus paradoxolophus are functionally matched for fluttering target detection.

Flutter-detecting foragers require specific adaptations of the transmitter and the receiver of their echolocation systems to detect and evaluate flutter information in the echoes of potential prey. These adaptations include Doppler shift compensation (DSC), which keeps the echo frequency from targets ahead constant at a reference frequency (fref), and an auditory fovea in the cochlea, which results in foveal areas in the hearing system with many sharply tuned neurons with best frequencies near fref. So far, this functional match has been verified only for a very few key species, but is postulated for all flutter-detecting foragers. In this study we determined both, the transmitter and receiver properties within individuals of the Bourret's horseshoe bat (Rhinolophus paradoxolophus), an allometric outlier in the rhinolophid family. Here we show that the transmitter and receiver are functionally matched in a similar way as postulated for all flutter-detecting foragers. The performance of DSC, measured as the ability to keep the echo frequency constant at fref, had a precision similar to that found in other flutter-detecting foragers, and the audiogram showed the characteristic course with a minimum at fref. Furthermore, we show for a rhinolophid bat a variation over time of the coupled resting frequency and fref. Finally, we discuss the tight match between transmitter and receiver properties, which is guaranteed by the link between the foveal areas of the receiver and the audio-vocal control system for DSC.

The resting frequency of echolocation signals changes with body temperature in the hipposiderid bat Hipposideros armiger.

Doppler shift (DS) compensating bats adjust in flight the second harmonic of the constant-frequency component (CF2) of their echolocation signals so that the frequency of the Doppler-shifted echoes returning from ahead is kept constant with high precision (0.1-0.2%) at the so-called reference frequency (fref). This feedback adjustment is mediated by an audio-vocal control system that correlates with a maximal activation of the foveal resonance area in the cochlea. Stationary bats adjust the average CF2 with similar precision at the resting frequency (frest), which is slightly below the fref. Over a range of time periods (from minutes up to years), variations of the coupled fref and frest have been observed, and were attributed to age, social influences and behavioural situations in rhinolophids and hipposiderids, and to body temperature effects and flight activity in Pteronotus parnellii. We assume that, for all DS-compensating bats, a change in body temperature has a strong effect on the activation state of the foveal resonance area in the cochlea, which leads to a concomitant change in emission frequency. We tested our hypothesis in a hipposiderid bat, Hipposideros armiger, and measured how the circadian variation of body temperature at activation phases affected frest. With a miniature temperature logger, we recorded the skin temperature on the back of the bats simultaneously with echolocation signals produced. During warm-up from torpor, strong temperature increases were accompanied by an increase in frest, of up to 1.44 kHz. We discuss the implications of our results for the organization and function of the audio-vocal control systems of all DS-compensating bats.

Discrimination of small sugar concentration differences helps the nectar-feeding bat Leptonycteris yerbabuenae cover energetic demands.

Every day nectar-feeding animals face an energetic challenge during foraging: they must locate and select flowers that provide nectar with adequate amounts of sugar to cover their very high energy needs. To understand this decision-making process, it is crucial to know how accurately sugar concentration differences can be discriminated. In a controlled laboratory setting, we offered the nectar-specialist bat Leptonycteris yerbabuenae the choice between different sugar solutions covering the entire concentration range of bat-pollinated plants (3-33%). When feeding on solutions below 10% sugar concentration, L. yerbabuenae were unable to cover their energetic demands because of physiological constraints. Their ability to discriminate sugar concentrations was better than that of any other nectar-feeding animal studied to date. At sugar concentrations below 15%, L. yerbabuenae can discriminate solutions differing by only 0.5%. The bats may utilize this fine-tuned ability to select nectar from flowers with reward qualities that provide them with the necessary amount of energy to survive.

High frequency social calls indicate food source defense in foraging Common pipistrelle bats.

Social calls have the function to coordinate the behavior of animals. In the presence of conspecifics foraging Common pipistrelle bats (P. pipistrellus) emitted, in addition to typical echolocation signals, two types of social calls: complex social calls and an as-of-yet undescribed, short, frequency-modulated call type with high terminal frequency, which we term "high frequency social call". By recording the flight and acoustic behavior of free flying pairs of foraging P. pipistrellus with an array of four microphones we were able to determine their three-dimensional flight paths and attribute emitted calls to particular behavioral situations. Complex social calls were emitted at further inter-individual distances and at large bearing angles to conspecifics, whereas high frequency social calls were produced at significantly shorter distances and at smaller bearing angles. These calls were associated with chasings and the eviction of the intruder. We assume that the emission of both types of social calls by foraging bats reflects a two-stage-process of the occupation and defense of a food patch. Common pipistrelle bats use complex social calls to claim a food patch and switch to agonistic behaviors, including chasings and high frequency social call emissions, when they defend their foraging territory against an intruder.

Bats Actively Use Leaves as Specular Reflectors to Detect Acoustically Camouflaged Prey.

Filtering relevant signals from noisy sensory input is a crucial challenge for animals [1, 2]. Many bats are acoustic specialists relying on sound to find prey. They discern salient acoustic signals from irrelevant background masking noise. It has long been considered a sensory impossibility for bats to use solely echolocation for the detection of silent and motionless prey resting directly on foliage due to the masking effects of background echoes [3, 4]. Some bats, however, do successfully perform this seemingly impossible task [5], raising the question-what underlying acoustic and behavioral mechanisms do bats use to solve this conundrum? To address this question, we used biomimetic sonar to record high-resolution measurements of echoes from insects resting on leaves. Based on our echo recordings, we predicted optimal approach angles from which masking echoes can best be avoided. In behavioral experiments, we put these predictions to test. We recorded the prey approach behavior of wild bats in a flight cage equipped with an ultrasonic microphone synchronized with two high-speed cameras for 3D flightpath reconstructions. Bats approached prey from our predicted optimal oblique angles, using the leaf as a specular reflector to uncover previously acoustically hidden prey. Our findings disclose key behavioral and acoustic mechanisms enabling the detection of prey echoes that background clutter would otherwise mask. This work adds to the fundamental understanding of how bat echolocation strategies can override acoustic camouflage by silent, motionless prey, thus providing new insights into the evolutionary arms race between predators and their prey.

Twittering Pupae of Papilionid and Nymphalid Butterflies (Lepidoptera): Novel Structures and Sounds.

Pupae of numerous Papilionidae and Nymphalidae produce twitter sounds when wriggling in response to mechanical stimulation. The structural basis comprises distinct pairs of sound-producing organs (SPOs) located at intersegmental membranes of the abdomen. They differ-as the twitters do-in sampled taxa of Papilioninae, Epicaliini, and Heliconiini. The opposing sculptured cuticular sound plates (SPs) of each SPO appear structurally the same but are actually mirror-images of each other. Results suggest that sounds are not generated by stridulation (friction of a file and a scraper) but when these inversely sculptured and interlocking surfaces separate during pupal wriggling, representing a stick-slip mechanism. Twitter sounds comprise series of short broadband pulses with the main energy in the frequency range 3-13 kHz; they can be heard by humans but extend into ultrasonic frequencies up to 100 kHz.

Precise Doppler shift compensation in the hipposiderid bat, Hipposideros armiger.

Bats of the Rhinolophidae and Hipposideridae families, and Pteronotus parnellii, compensate for Doppler shifts generated by their own flight movement. They adjust their call frequency such that the frequency of echoes coming from ahead fall in a specialized frequency range of the hearing system, the auditory fovea, to evaluate amplitude and frequency modulations in echoes from fluttering prey. Some studies in hipposiderids have suggested a less sophisticated or incomplete Doppler shift compensation. To investigate the precision of Doppler shift compensation in Hipposideros armiger, we recorded the echolocation and flight behaviour of bats flying to a grid, reconstructed the flight path, measured the flight speed, calculated the echo frequency, and compared it with the resting frequency prior to each flight. Within each flight, the average echo frequency was kept constant with a standard deviation of 110 Hz, independent of the flight speed. The resting and reference frequency were coupled with an offset of 80 Hz; however, they varied slightly from flight to flight. The precision of Doppler shift compensation and the offset were similar to that seen in Rhinolophidae and P. parnellii. The described frequency variations may explain why it has been assumed that Doppler shift compensation in hipposiderids is incomplete.

Reduction of emission level in approach signals of greater mouse-eared bats (Myotis myotis): No evidence for a closed loop control system for intensity compensation.

Bats lower the emission SPL when approaching a target. The SPL reduction has been explained by intensity compensation which implies that bats adjust the emission SPL to perceive the retuning echoes at the same level. For a better understanding of this control mechanism we recorded the echolocation signals of four Myotis myotis with an onboard microphone when foraging in the passive mode for rustling mealworms offered in two feeding dishes with different target strength, and determined the reduction rate for the emission SPL and the increase rate for the SPL of the returning echoes. When approaching the dish with higher target strength bats started the reduction of the emission SPL at a larger reaction distance (1.05 ± 0.21 m) and approached it with a lower reduction rate of 7.2 dB/halving of distance (hd), thus producing a change of echo rate at the ears of + 4 dB/hd. At the weaker target reaction distance was shorter (0.71 ± 0.24 m) and the reduction rate (9.1 dB/hd) was higher, producing a change of echo rate of-1.2 dB/hd. Independent of dish type, bats lowered the emission SPL by about 26 dB on average. In one bat where the echo SPL from both targets could be measured, the reduction of emission SPL was triggered when the echo SPL surpassed a similar threshold value around 41-42 dB. Echo SPL was not adjusted at a constant value indicating that Myotis myotis and most likely all other bats do not use a closed loop system for intensity compensation when approaching a target of interest. We propose that bats lower the emission SPL to adjust the SPL of the perceived pulse-echo-pairs to the optimal auditory range for the processing of range information and hypothesize that bats use flow field information not only to control the reduction of the approach speed to the target but also to control the reduction of emission SPL.

How Nectar-Feeding Bats Localize their Food: Echolocation Behavior of Leptonycteris yerbabuenae Approaching Cactus Flowers.

Nectar-feeding bats show morphological, physiological, and behavioral adaptations for feeding on nectar. How they find and localize flowers is still poorly understood. While scent cues alone allow no precise localization of a floral target, the spatial properties of flower echoes are very precise and could play a major role, particularly at close range. The aim of this study is to understand the role of echolocation for classification and localization of flowers. We compared the approach behavior of Leptonycteris yerbabuenae to flowers of a columnar cactus, Pachycereus pringlei, to that to an acrylic hollow hemisphere that is acoustically conspicuous to bats, but has different acoustic properties and, contrary to the cactus flower, present no scent. For recording the flight and echolocation behaviour we used two infrared video cameras under stroboscopic illumination synchronized with ultrasound recordings. During search flights all individuals identified both targets as a possible food source and initiated an approach flight; however, they visited only the cactus flower. In experiments with the acrylic hemisphere bats aborted the approach at ca. 40-50 cm. In the last instant before the flower visit the bats emitted a long terminal group of 10-20 calls. This is the first report of this behaviour for a nectar-feeding bat. Our findings suggest that L. yerbabuenae use echolocation for classification and localization of cactus flowers and that the echo-acoustic characteristics of the flower guide the bats directly to the flower opening.

No evidence for spectral jamming avoidance in echolocation behavior of foraging pipistrelle bats.

Frequency shifts in signals of bats flying near conspecifics have been interpreted as a spectral jamming avoidance response (JAR). However, several prerequisites supporting a JAR hypothesis have not been controlled for in previous studies. We recorded flight and echolocation behavior of foraging Pipistrellus pipistrellus while flying alone and with a conspecific and tested whether frequency changes were due to a spectral JAR with an increased frequency difference, or whether changes could be explained by other reactions. P. pipistrellus reacted to conspecifics with a reduction of sound duration and often also pulse interval, accompanied by an increase in terminal frequency. This reaction is typical of behavioral situations where targets of interest have captured the bat's attention and initiated a more detailed exploration. All observed frequency changes were predicted by the attention reaction alone, and do not support the JAR hypothesis of increased frequency separation. Reaction distances of 1-11 m suggest that the attention response may be elicited either by detection of the conspecific by short range active echolocation or by long range passive acoustic detection of echolocation calls.

Bidirectional Echolocation in the Bat Barbastella barbastellus: Different Signals of Low Source Level Are Emitted Upward through the Nose and Downward through the Mouth.

The Barbastelle bat (Barbastella barbastellus) preys almost exclusively on tympanate moths. While foraging, this species alternates between two different signal types. We investigated whether these signals differ in emission direction or source level (SL) as assumed from earlier single microphone recordings. We used two different settings of a 16-microphone array to determine SL and sonar beam direction at various locations in the field. Both types of search signals had low SLs (81 and 82 dB SPL rms re 1 m) as compared to other aerial-hawking bats. These two signal types were emitted in different directions; type 1 signals were directed downward and type 2 signals upward. The angle between beam directions was approximately 70°. Barbastelle bats are able to emit signals through both the mouth and the nostrils. As mouth and nostrils are roughly perpendicular to each other, we conclude that type 1 signals are emitted through the mouth while type 2 signals and approach signals are emitted through the nose. We hypothesize that the "stealth" echolocation system of B. barbastellus is bifunctional. The more upward directed nose signals may be mainly used for search and localization of prey. Their low SL prevents an early detection by eared moths but comes at the expense of a strongly reduced detection range for the environment below the bat. The more downward directed mouth signals may have evolved to compensate for this disadvantage and may be mainly used for spatial orientation. We suggest that the possibly bifunctional echolocation system of B. barbastellus has been adapted to the selective foraging of eared moths and is an excellent example of a sophisticated sensory arms race between predator and prey.

Acoustic behavior of melon-headed whales varies on a diel cycle.

Many terrestrial and marine species have a diel activity pattern, and their acoustic signaling follows their current behavioral state. Whistles and echolocation clicks on long-term recordings produced by melon-headed whales (Peponocephala electra) at Palmyra Atoll indicated that these signals were used selectively during different phases of the day, strengthening the idea of nighttime foraging and daytime resting with afternoon socializing for this species. Spectral features of their echolocation clicks changed from day to night, shifting the median center frequency up. Additionally, click received levels increased with increasing ambient noise during both day and night. Ambient noise over a wide frequency band was on average higher at night. The diel adjustment of click features might be a reaction to acoustic masking caused by these nighttime sounds. Similar adaptations have been documented for numerous taxa in response to noise. Or it could be, unrelated, an increase in biosonar source levels and with it a shift in center frequency to enhance detection distances during foraging at night. Call modifications in intensity, directionality, frequency, and duration according to echolocation task are well established for bats. This finding indicates that melon-headed whales have flexibility in their acoustic behavior, and they collectively and repeatedly adapt their signals from day- to nighttime circumstances.

Echolocation behaviour of the big brown bat (Eptesicus fuscus) in an obstacle avoidance task of increasing difficulty.

Four big brown bats (Eptesicus fuscus) were challenged in an obstacle avoidance experiment to localize vertically stretched wires requiring progressively greater accuracy by diminishing the wire-to-wire distance from 50 to 10 cm. The performance of the bats decreased with decreasing gap size. The avoidance task became very difficult below a wire separation of 30 cm, which corresponds to the average wingspan of E. fuscus. Two of the bats were able to pass without collisions down to a gap size of 10 cm in some of the flights. The other two bats only managed to master gap sizes down to 20 and 30 cm, respectively. They also performed distinctly worse at all other gap sizes. With increasing difficulty of the task, the bats changed their flight and echolocation behaviour. Especially at gap sizes of 30 cm and below, flight paths increased in height and flight speed was reduced. In addition, the bats emitted approach signals that were arranged in groups. At all gap sizes, the largest numbers of pulses per group were observed in the last group before passing the obstacle. The more difficult the obstacle avoidance task, the more pulses there were in the groups and the shorter the within-group pulse intervals. In comparable situations, the better-performing bats always emitted groups with more pulses than the less well-performing individuals. We hypothesize that the accuracy of target localization increases with the number of pulses per group and that each group is processed as a package.

Bat guilds, a concept to classify the highly diverse foraging and echolocation behaviors of microchiropteran bats.

Throughout evolution the foraging and echolocation behaviors as well as the motor systems of bats have been adapted to the tasks they have to perform while searching and acquiring food. When bats exploit the same class of environmental resources in a similar way, they perform comparable tasks and thus share similar adaptations independent of their phylogeny. Species with similar adaptations are assigned to guilds or functional groups. Habitat type and foraging mode mainly determine the foraging tasks and thus the adaptations of bats. Therefore, we use habitat type and foraging mode to define seven guilds. The habitat types open, edge and narrow space are defined according to the bats' echolocation behavior in relation to the distance between bat and background or food item and background. Bats foraging in the aerial, trawling, flutter detecting, or active gleaning mode use only echolocation to acquire their food. When foraging in the passive gleaning mode bats do not use echolocation but rely on sensory cues from the food item to find it. Bat communities often comprise large numbers of species with a high diversity in foraging areas, foraging modes, and diets. The assignment of species living under similar constraints into guilds identifies patterns of community structure and helps to understand the factors that underlie the organization of highly diverse bat communities. Bat species from different guilds do not compete for food as they differ in their foraging behavior and in the environmental resources they use. However, sympatric living species belonging to the same guild often exploit the same class of resources. To avoid competition they should differ in their niche dimensions. The fine grain structure of bat communities below the rather coarse classification into guilds is determined by mechanisms that result in niche partitioning.

Scanning behavior in echolocating common pipistrelle bats (Pipistrellus pipistrellus).

Echolocating bats construct an auditory world sequentially by analyzing successive pulse-echo pairs. Many other mammals rely upon a visual world, acquired by sequential foveal fixations connected by visual gaze saccades. We investigated the scanning behavior of bats and compared it to visual scanning. We assumed that each pulse-echo pair evaluation corresponds to a foveal fixation and that sonar beam movements between pulses can be seen as acoustic gaze saccades. We used a two-dimensional 16 microphone array to determine the sonar beam direction of succeeding pulses and to characterize the three dimensional scanning behavior in the common pipistrelle bat (Pipistrellus pipistrellus) flying in the field. We also used variations of signal amplitude of single microphone recordings as indicator for scanning behavior in open space. We analyzed 33 flight sequences containing more than 700 echolocation calls to determine bat positions, source levels, and beam aiming. When searching for prey and orienting in space, bats moved their sonar beam in all directions, often alternately back and forth. They also produced sequences with irregular or no scanning movements. When approaching the array, the scanning movements were much smaller and the beam was moved over the array in small steps. Differences in the scanning pattern at various recording sites indicated that the scanning behavior depended on the echolocation task that was being performed. The scanning angles varied over a wide range and were often larger than the maximum angle measurable by our array. We found that echolocating bats use a "saccade and fixate" strategy similar to vision. Through the use of scanning movements, bats are capable of finding and exploring targets in a wide search cone centered along flight direction.

Estimation of the acoustic range of bat echolocation for extended targets.

Extended natural structures of the bat environment such as trees, meadows, and water surfaces were ensonified in distances from 1 to 20 m and the echoes recorded using a mobile ultrasonic sonar system. By compensating the atmospheric attenuation, the attenuation of the reflected echo caused by diffraction, energy absorption of the target, and two-way-geometric spreading was calculated for each distance. For each target type the attenuation of the compensated echo sound pressure level was fitted over distance using a linear function which yields simple laws of reflection loss and geometric spreading. By adding to this function again variable atmospheric attenuation, the overall attenuation of a signal reflected from these targets can be estimated for various conditions. Given the dynamic range of a sonar system, the acoustic maximum detection distance can thus be estimated. The results show that the maximum range is dominantly limited by atmospheric attenuation. Energy loss in the reflecting surface is more variable than geometric spreading loss and accounts for most of the differences between the ensonified targets. Depending on atmospheric conditions, echolocation frequency, and the dynamic range of the sonar system, the maximum range for extended backgrounds such as a forest edge can be as short as 2.4 m.

Asymmetry and dynamics of a narrow sonar beam in an echolocating harbor porpoise.

A key component in the operation of a biosonar system is the radiation of sound energy from the sound producing head structures of toothed whales and microbats. The current view involves a fixed transmission aperture by which the beam width can only change via changes in the frequency of radiated clicks. To test that for a porpoise, echolocation clicks were recorded with high angular resolution using a 16 hydrophone array. The beam is narrower than previously reported (DI = 24 dB) and slightly dorso-ventrally compressed (horizontal -3 dB beam width: 13°, vertical -3 dB beam width: 11°). The narrow beam indicates that all smaller toothed whales investigated so far have surprisingly similar beam widths across taxa and habitats. Obtaining high directionality may thus be at least in part an evolutionary factor that led to high centroid frequencies in a group of smaller toothed whales emitting narrow band high frequency clicks. Despite the production of stereotyped narrow band high frequency clicks, changes in the directionality by a few degrees were observed, showing that porpoises can obtain changes in sound radiation.

Source level reduction and sonar beam aiming in landing big brown bats (Eptesicus fuscus).

Reduction of echolocation call source levels in bats has previously been studied using set-ups with one microphone. By using a 16 microphone array, sound pressure level (SPL) variations, possibly caused by the scanning movements of the bat, can be excluded and the sonar beam aiming can be studied. During the last two meters of approach flights to a landing platform in a large flight room, five big brown bats aimed sonar beams at the landing site and reduced the source level on average by 7 dB per halving of distance. Considerable variation was found among the five individuals in the amount of source level reduction ranging from 4 to 9 dB per halving of distance. These results are discussed with respect to automatic gain control and intensity compensation and the combination of the two effects. It is argued that the two effects together do not lead to a stable echo level at the cochlea. This excludes a tightly coupled closed loop feed back control system as an explanation for the observed reduction of signal SPL in landing big brown bats.

Horseshoe bats make adaptive prey-selection decisions, informed by echo cues.

Foragers base their prey-selection decisions on the information acquired by the sensory systems. In bats that use echolocation to find prey in darkness, it is not clear whether the specialized diet, as sometimes found by faecal analysis, is a result of active decision-making or rather of biased sensory information. Here, we tested whether greater horseshoe bats decide economically when to attack a particular prey item and when not. This species is known to recognize different insects based on their wing-beat pattern imprinted in the echoes. We built a simulation of the natural foraging process in the laboratory, where the bats scanned for prey from a perch and, upon reaching the decision to attack, intercepted the prey in flight. To fully control echo information available to the bats and assure its unambiguity, we implemented computer-controlled propellers that produced echoes resembling those from natural insects of differing profitability. The bats monitored prey arrivals to sample the supply of prey categories in the environment and to inform foraging decisions. The bats adjusted selectivity for the more profitable prey to its inter-arrival intervals as predicted by foraging theory (an economic strategy known to benefit fitness). Moreover, unlike in previously studied vertebrates, foraging performance of horseshoe bats was not limited by costly rejections of the profitable prey. This calls for further research into the evolutionary selection pressures that sharpened the species's decision-making capacity.

Auditory fovea and Doppler shift compensation: adaptations for flutter detection in echolocating bats using CF-FM signals.

Rhythmical modulations in insect echoes caused by the moving wings of fluttering insects are behaviourally relevant information for bats emitting CF-FM signals with a high duty cycle. Transmitter and receiver of the echolocation system in flutter detecting foragers are especially adapted for the processing of flutter information. The adaptations of the transmitter are indicated by a flutter induced increase in duty cycle, and by Doppler shift compensation (DSC) that keeps the carrier frequency of the insect echoes near a reference frequency. An adaptation of the receiver is the auditory fovea on the basilar membrane, a highly expanded frequency representation centred to the reference frequency. The afferent projections from the fovea lead to foveal areas with an overrepresentation of sharply tuned neurons with best frequencies near the reference frequency throughout the entire auditory pathway. These foveal neurons are very sensitive to stimuli with natural and simulated flutter information. The frequency range of the foveal areas with their flutter processing neurons overlaps exactly with the frequency range where DS compensating bats most likely receive echoes from fluttering insects. This tight match indicates that auditory fovea and DSC are adaptations for the detection and evaluation of insects flying in clutter.