Cynthia F. Moss

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.

Echolocation behavior of big brown bats, Eptesicus fuscus, in the field and the laboratory

Echolocation signals were recorded from big brown bats, Eptesicus fuscus, flying in the field and the laboratory. In open field areas the interpulse intervals (IPI) of search signals were either around 134 ms or twice that value, 270 ms. At long IPIs the signals were of long duration (14 to 18-20 ms), narrow bandwidth, and low frequency, sweeping down to a minimum frequency (Fmin) of 22-25 kHz. At short IPIs the signals were shorter (6-13 ms), of higher frequency, and broader bandwidth. In wooded areas only short (6-11 ms) relatively broadband search signals were emitted at a higher rate (avg. IPI= 122 ms) with higher Fmin (27-30 kHz). In the laboratory the IPI was even shorter (88 ms), the duration was 3-5 ms, and the Fmin 30- 35 kHz, resembling approach phase signals of field recordings. Excluding terminal phase signals, all signals from all areas showed a negative correlation between signal duration and Fmin, i.e., the shorter the signal, the higher was Fmin. This correlation was reversed in the terminal phase of insect capture sequences, where Fmin decreased with decreasing signal duration. Overall, the signals recorded in the field were longer, with longer IPIs and greater variability in bandwidth than signals recorded in the laboratory.

Isotopic Tracking of Change in Diet and Habitat Use in African Elephants

The carbon, nitrogen, and strontium isotope compositions of elephants in Amboseli Park, Kenya, were measured to examine changes in diet and habitat use since the 1960s. Carbon isotope ratios, which reflect the photosynthetic pathway of food plants, record a shift in diet from trees and shrubs to grass. Strontium isotope ratios, which reflect the geologic age of bedrock, document the concentration of elephants within the park. The high isotopic variability produced by behavioral and ecological shifts, if it is representative of other East African elephant populations, may complicate the use of isotopes as indicators of the source region of ivory.

Auditory scene analysis by echolocation in bats

Echolocating bats transmit ultrasonic vocalizations and use information contained in the reflected sounds to analyze the auditory scene. Auditory scene analysis, a phenomenon that applies broadly to all hearing vertebrates, involves the grouping and segregation of sounds to perceptually organize information about auditory objects. The perceptual organization of sound is influenced by the spectral and temporal characteristics of acoustic signals. In the case of the echolocating bat, its active control over the timing, duration, intensity, and bandwidth of sonar transmissions directly impacts its perception of the auditory objects that comprise the scene. Here, data are presented from perceptual experiments, laboratory insect capture studies, and field recordings of sonar behavior of different bat species, to illustrate principles of importance to auditory scene analysis by echolocation in bats. In the perceptual experiments, FM bats (Eptesicus fuscus) learned to discriminate between systematic and random delay sequences in echo playback sets. The results of these experiments demonstrate that the FM bat can assemble information about echo delay changes over time, a requirement for the analysis of a dynamic auditory scene. Laboratory insect capture experiments examined the vocal production patterns of flying E. fuscus taking tethered insects in a large room. In each trial, the bats consistently produced echolocation signal groups with a relatively stable repetition rate (within 5%). Similar temporal patterning of sonar vocalizations was also observed in the field recordings from E. fuscus, thus suggesting the importance of temporal control of vocal production for perceptually guided behavior. It is hypothesized that a stable sonar signal production rate facilitates the perceptual organization of echoes arriving from objects at different directions and distances as the bat flies through a dynamic auditory scene. Field recordings of E. fuscus, Noctilio albiventris, N. leporinus, Pippistrellus pippistrellus, and Cormura brevirostris revealed that spectral adjustments in sonar signals may also be important to permit tracking of echoes in a complex auditory scene.

Discrimination of jittered sonar echoes by the echolocating bat, Eptesicus fuscus: the shape of target images in echolocation.

Summary1.Behavioral experiments with jittering echoes examined acoustic images of sonar targets in the echolocating bat, Eptesicus fuscus, along the echo delay or target range axis. Echo phase, amplitude, bandwidth, and signal-to-noise ratio were manipulated to assess the underlying auditory processes for image formation.2.Fine delay acuity is about 10 ns. Calibration and control procedures indicate that this represents temporal acuity rather than spectral discrimination. Jitter discrimination curves change in phase when the phase of one jittering echo is shifted by 180° relative to the other, showing that echo phase is involved in delay estimation. At an echo detectability index of about 36 dB, fine acuity is 40 ns, which is approximately as predicted for the delay accuracy of an ideal receiver.3.Compound performance curves for 0° and 180° phase conditions match the crosscorrelation function of the echoes. The locations of both 0° and 180° phase peaks in the performance curves shift along the time axis by an amount that matches neural amplitude-latency trading in Eptesicus, confirming a temporal basis for jitter discrimination.

Echolocating Bats Use a Nearly Time-Optimal Strategy to Intercept Prey

Acquisition of food in many animal species depends on the pursuit and capture of moving prey. Among modern humans, the pursuit and interception of moving targets plays a central role in a variety of sports, such as tennis, football, Frisbee, and baseball. Studies of target pursuit in animals, ranging from dragonflies to fish and dogs to humans, have suggested that they all use a constant bearing (CB) strategy to pursue prey or other moving targets. CB is best known as the interception strategy employed by baseball outfielders to catch ballistic fly balls. CB is a time-optimal solution to catch targets moving along a straight line, or in a predictable fashion—such as a ballistic baseball, or a piece of food sinking in water. Many animals, however, have to capture prey that may make evasive and unpredictable maneuvers. Is CB an optimum solution to pursuing erratically moving targets? Do animals faced with such erratic prey also use CB? In this paper, we address these questions by studying prey capture in an insectivorous echolocating bat. Echolocating bats rely on sonar to pursue and capture flying insects. The bats prey may emerge from foliage for a brief time, fly in erratic three-dimensional paths before returning to cover. Bats typically take less than one second to detect, localize and capture such insects. We used high speed stereo infra-red videography to study the three dimensional flight paths of the big brown bat, Eptesicus fuscus, as it chased erratically moving insects in a dark laboratory flight room. We quantified the bats complex pursuit trajectories using a simple delay differential equation. Our analysis of the pursuit trajectories suggests that bats use a constant absolute target direction strategy during pursuit. We show mathematically that, unlike CB, this approach minimizes the time it takes for a pursuer to intercept an unpredictably moving target. Interestingly, the bats behavior is similar to the interception strategy implemented in some guided missiles. We suggest that the time-optimal strategy adopted by the bat is in response to the evolutionary pressures of having to capture erratic and fast moving insects.

Leadership in elephants: the adaptive value of age

The value of age is well recognized in human societies, where older individuals often emerge as leaders in tasks requiring specialized knowledge, but what part do such individuals play in other social species? Despite growing interest in how effective leadership might be achieved in animal social systems, the specific role that older leaders may play in decision-making has rarely been experimentally investigated. Here, we use a novel playback paradigm to demonstrate that in African elephants (Loxodonta africana), age affects the ability of matriarchs to make ecologically relevant decisions in a domain critical to survival—the assessment of predatory threat. While groups consistently adjust their defensive behaviour to the greater threat of three roaring lions versus one, families with younger matriarchs typically under-react to roars from male lions despite the severe danger they represent. Sensitivity to this key threat increases with matriarch age and is greatest for the oldest matriarchs, who are likely to have accumulated the most experience. Our study provides the first empirical evidence that individuals within a social group may derive significant benefits from the influence of an older leader because of their enhanced ability to make crucial decisions about predatory threat, generating important insights into selection for longevity in cognitively advanced social mammals.

The sonar beam pattern of a flying bat as it tracks tethered insects

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.

Behavioral Studies of Auditory Information Processing

Echolocating bats are nocturnal animals that rely largely on auditory information to orient in the environment and intercept prey. Bats produce high-frequency vocal signals and perceive their surroundings by listening to the features of the echoes reflecting off targets in the path of the sound beam (Griffin 1958). Computations performed on these echoes by the auditory system allow the bat to extract fine spatial information about its world through acoustic channels. This chapter attempts a comprehensive review and synthesis of data on auditory information processing and perception by sonar in echolocating bats.

Convergence of temporal and spectral information into acoustic images of complex sonar targets perceived by the echolocating bat, Eptesicus fuscus.

Summary1.FM echolocating bats (Eptesicus fuscus) were trained to discriminate between a two-component complex target and a one-component simple target simulated by electronically-returned echoes in a series of experiments that explore the composition of the image of the two-component target. In Experiment I, echoes for each target were presented sequentially, and the bats had to compare a stored image of one target with that of the other. The bats made errors when the range of the simple target corresponded to the range of either glint in the complex target, indicating that some trace of the parts of one image interfered with perception of the other image. In Experiment II, echoes were presented simultaneously as well as sequentially, permitting direct masking of echoes from one target to the other. Changes in echo amplitude produced shifts in apparent range whose pattern depended upon the mode of echo presentation.2.Eptesicus perceives images of complex sonar targets that explicitly represent the location and spacing of discrete glints located at different ranges. The bat perceives the targets structure in terms of its range profile along a psychological range axis using a combination of echo delay and echo spectral representations that together resemble a spectrogram of the FM echoes. The image itself is expressed entirely along a range scale that is defined with reference to echo delay. Spectral information contributes to the image by providing estimates of the range separation of glints, but it is transformed into these estimates.3.Perceived absolute range is encoded by the timing of neural discharges and is vulnerable to shifts caused by neural amplitude-latency trading, which was estimated at 13 to 18 μs per dB from N1 and N4 auditory evoked potentials in Eptesicus. Spectral cues representing the separation of glints within the target are transformed into estimates of delay separations before being incorporated into the image. However, because they are encoded by neural frequency tuning rather than the time-of-occurrence of neural discharges, the perceived range separation of glints in images is not vulnerable to amplitudelatency shifts.4.The bat perceives an image that is displayed in the domain of time or range. The image receives no evident spectral contribution beyond what is transformed into delay estimates. Although the initial auditory representation of FM echoes is spectrogram-like, the time, frequency, and amplitude dimensions of the spectrogram appear to be compressed into an image that has only time and amplitude dimensions. The spectral information is not lost but manifests itself as equivalent time-domain information.