Annette Denzinger

From spatial orientation to food acquisition in echolocating bats

Field research on echolocation behavior in bats has emphasized studies of food acquisition, and the adaptive value of sonar signal design as been considered largely in the context of foraging. However, echolocation tasks related to spatial orientation also differ among bats and are relevant to understanding signal structure. Here, we argue that the evolution of echolocation in bats is characterized by two key innovations: first, the evolution of echolocation for spatial orientation and, second, a later transition for prey acquisition. This conceptual framework calls for a new view on field data from bats orienting and foraging in different types of habitats. According to the ecological constraints in which foraging bats operate, four distinct functional groups or guilds can be defined. Within each group, signal design and echolocation behavior are rather similar.

Old World frog and bird vocalizations contain prominent ultrasonic harmonics

Several groups of mammals such as bats, dolphins and whales are known to produce ultrasonic signals which are used for navigation and hunting by means of echolocation, as well as for communication. In contrast, frogs and birds produce sounds during night- and day-time hours that are audible to humans; their sounds are so pervasive that together with those of insects, they are considered the primary sounds of nature. Here we show that an Old World frog (Amolops tormotus) and an oscine songbird (Abroscopus albogularis) living near noisy streams reliably produce acoustic signals that contain prominent ultrasonic harmonics. Our findings provide the first evidence that anurans and passerines are capable of generating tonal ultrasonic call components and should stimulate the quest for additional ultrasonic species.

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.

The Voice of Bats: How Greater Mouse-eared Bats Recognize Individuals Based on Their Echolocation Calls

Echolocating bats use the echoes from their echolocation calls to perceive their surroundings. The ability to use these continuously emitted calls, whose main function is not communication, for recognition of individual conspecifics might facilitate many of the social behaviours observed in bats. Several studies of individual-specific information in echolocation calls found some evidence for its existence but did not quantify or explain it. We used a direct paradigm to show that greater mouse-eared bats (Myotis myotis) can easily discriminate between individuals based on their echolocation calls and that they can generalize their knowledge to discriminate new individuals that they were not trained to recognize. We conclude that, despite their high variability, broadband bat-echolocation calls contain individual-specific information that is sufficient for recognition. An analysis of the call spectra showed that formant-related features are suitable cues for individual recognition. As a model for the bats decision strategy, we trained nonlinear statistical classifiers to reproduce the behaviour of the bats, namely to repeat correct and incorrect decisions of the bats. The comparison of the bats with the model strongly implies that the bats are using a prototype classification approach: they learn the average call characteristics of individuals and use them as a reference for classification.

Aerial hawking and landing: approach behaviour in Natterer's bats, Myotis nattereri (Kuhl 1818).

SUMMARY We compared the flight and echolocation behaviour of a vespertilionid bat (Myotis nattereri) approaching a large stationary or a small moving target. Bats were trained to either land on a landing grid or to catch a moving tethered mealworm. When closing in on these two targets, the bats emitted groups of sounds with increasing number of signals and decreasing pulse interval and duration. When pursuing the mealworm, the approach phase always ended with a terminal group consisting of buzz I and buzz II. When landing, the bats emitted either a terminal group consisting of buzz I alone, with one or two extra pulses, or a group consisting of buzz I and buzz II. In all situations, buzz I ended on average between 47–63 ms prior to contact with the target of interest, which is approximately the reaction time of bats. Therefore, the information collected in buzz II does not guide the bats to the target. The relevant part of the approach phase to reach the target ends with buzz I. The basic sound pattern of this part is rather similar and independent of whether the bats approach the large stationary or the small moving target.

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.

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.

Echo SPL influences the ranging performance of the big brown bat, Eptesicus fuscus

Four bats of the species Eptesicus fuscus were trained in a two-alternative forced-choice procedure to discriminate between two phantom targets that differed in range. The rewarded stimulus was located at a distance of 52.7 cm, while the other unrewarded stimulus was further away. Only one target was presented at a time.In the first experiment we measured the range discrimination performance at an echo SPL of −28 dB relative to the bats sonar transmission. A 75% correct performance level was arbitrarily defined as threshold and was obtained at a delay difference of 80 μs, corresponding to a range difference of 13.8 mm.In the second experiment the delay difference was fixed at 150 μs and the echo SPL varied between −8 and −48 dB relative to sonar emissions. The performance of the bats depended on the relative echo SPL. At −28 dB the bats showed the best performance. It deteriorated at an increase of the relative echo SPL to −18 dB and −8 dB. The performance also deteriorated when the relative echo SPL was reduced to −38 dB and −48 dB. Only at low relative echo SPLs did the bats partially compensate for the reduction in echo SPL and increased the SPL of their emitted signals by a few dB.Our results support the hypothesis that neurons exhibiting paradoxical latency shift may be involved in encoding target range. This hypothesis predicts a decrease in performance at high echo SPLs as we found it in our experiments. The observed reduction in performance at very low echo SPLs may be due to a decrease in S/N ratio.

Variability of the approach phase of landing echolocating Greater Mouse-eared bats

The approach phase of landing vespertilionid bats ends with a group of calls, which either consists of buzz I alone or buzz I and buzz II. To understand the possible role of buzz II, we trained Myotis myotis to land on a vertical grid, and compared the flight and echolocation behavior during approach in trials with and without buzz II. During the approach, we did not find any differences in the echolocation behavior until the end of buzz I which indicated whether buzz II was emitted or not. However, bats flying from the periphery of the flight channel, such that they had to make a small turn at the very last moment, finished the sequence with a buzz II. Bats flying on a rather stereotyped trajectory near the center of the flight channel without last instant corrections emitted buzz I alone. Our results indicate that buzz II occurred only on trajectories that implied a higher risk to fail at landing. The information delivered by buzz II reaches the bat too late to be used for landing. Therefore, we hypothesize that buzz II may help the bats to evaluate unsuccessful attempts and to eventually react adequately.

ECHO SPL, TRAINING EXPERIENCE, AND EXPERIMENTAL PROCEDURE INFLUENCE THE RANGING PERFORMANCE IN THE BIG BROWN BAT, EPTESICUS FUSCUS

Abstract Four Eptesicus fuscus were trained in a range discrimination experiment to choose the closer of two phantom targets. Echo attenuation was roving between trials returning echoes ranging from −10 dB to −50 dB SPL (sound pressure level) relative to emission SPL. Discrimination thresholds were determined. After sufficient training, ranging performance was stable and about the same in the range between −20 dB and −50 dB with range difference thresholds around 300 μs. At −10 dB, performance was poor even after long training. After additional training at a constant relative echo SPL of −30 dB and a delay difference of 300 μs the performance measured with roving echo SPL improved at all relative echo SPL between −20 dB and −50 dB but not at −10 dB. The new experimental procedure improved the performance by additional learning, and the bats generalized over a wide range of relative echo SPL. Threshold improved to 100 μs when measured at a constant relative echo SPL of −30 dB, again indicating the influence of the experimental procedure. In correspondence to neurophysiological data the ranging performance deteriorates if the echo SPL is close to the emission SPL. Signal duration and emission SPL were variable during range discrimination.