Echolocating bats emit ultrasonic sonar pulses and listen to returning echoes, which are reflected from targets or obstacles, to probe their surroundings. Their biological sonar system is well-developed and highly adaptive to the dynamic acoustic environment. Bats are also agile flyers and they can modify their flight behavior in order to capture insects efficiently. Adaptable echolocation and flight behaviors evolved in bats in response to environmental demands. This study employed changes in the external ear of bats and in the acoustic environment to examine how the big brown bat, Eptesicus fuscus, modifies its echolocation call design and flight patterns to cope with these new experimental conditions. Study one investigated the influences of changes in sound localization cues on prey capture behavior. The tragus, which is part of the external ear, is believed to contribute to sound localization in the vertical plane. Deflecting the tragus affected prey capture performance of the bat, but it adapted to this manipulation by adjusting its flight behavior. The tragus-deflected bat tended to attack the prey item from above and show lower tangential velocity and larger bearing from the side, compared with its flight pattern in the tragus intact conditions.
The bat did not change its echolocation call design in the tragus-deflected condition. Study two paired two bats together and allowed them to perform a prey capture task in a large flight room. Echolocating bats showed two adaptive strategies in their echolocation behavior when flying with another conspecific. The bat either stopped vocalizing or increased its difference in call design from the other bat. In addition, one bat tended to follow another bat when flying together and antagonistic behavior was found in male-male and female-male pairs. The pursuit strategy the bat uses to track another bat is different from the strategy it uses to capture flying insects. This thesis confirms that the big brown bat’s echolocation and flight behaviors are highly adaptable and describes several strategies the bat employs to cope with changes in sound localization cues and conspecific interference.
Echolocation is a form of active sensing, which bats use to explore their surroundings, track prey, avoid obstacles and interact with conspecifics (Nelson and MacIver, 2006). Animals that rely on active sensing include electric fish, dolphins, whales and echolocating bats. Weakly electric fish generate an electric field with an electric discharge organ, typically located in the tail, to detect prey objects and the presence of conspecifics through modifications in the electric field. Electric fish can be categorized into two types, wave-type and pulse-type, according to their electric organ discharge (EOD). Wave-type electric fish produce signals with long duration and short pauses between each electric discharge, while pulse-type electric fish generate short duration EOD and with long pauses between each pulse (Heiligenberg, 1991). Odontocetes (dolphins, porpoises, sperm whales, killer whales, etc.) produce ultrasonic clicks underwater and use returning echoes to determine the position and material of objects.
The sound production mechanism of cetaceans has not been fully understood yet, but it is generally believed that the echolocation signals are generated from the nasal complex above the skull and are projected through the melon (the fatty tissues in the forehead) into the water (Cranford and Amundin, 2004). Megachiroptera and Microchiroptera are two suborders of bats but only microchiroptera bats use sonar vocalizations for orientation and prey capture. Megachiropteran bats, also known as flying foxes, use vision instead of echolocation for navigation and foraging. One genus of Megachiropteran bats, Rousettus, uses tongue clicks for echolocation (Holland et al., 2004). All Microchiroptera bats orient by echolocation and they can be roughly divided into two groups according to their echolocation call structures, either constant- frequency (CF) or frequency-modulated (FM).
All data collection and discussion in this thesis will focus on Microchiropteran bats which generate FM vocal signals. This section will introduce the echolocation behavior of bats and parameters used to describe echolocation call design. The sound localization section summarizes possible cues for the bat to perceive the three-dimensional position of an object. The auditory scene analysis section reviews past studies about how an animal may segregate signals of interest from a complex acoustic environment and avoid signal jamming from conspecifics. The last section will introduce the experimental design briefly and predict experimental results based on previous research about how the bat adjusts its vocalizations to cope with changes in sound localization cues and the presence of conspecifics.
An echolocating bat probes the environment with its sonar vocalizations which provide stimulus energy for perception, just as light does for vision. The bat uses echo returns to localize an object’s 3-D position in space, i.e. the elevation, azimuth and range, in order to capture prey successfully. Horizontal sound localization depends on the binaural comparisons of incoming signals (Obrist et al., 1993), such as interaural level differences, while vertical sound localization relies on the spectral cues generated by the external ear (Firzlaff and Schuller, 2003; Fuzessery, 1996; Lawrence and Simmons, 1982b; Wotton and Simmons, 2000). A bat determines the distance between itself and other objects from the time delay between the pulse it produces and the arrival time of returning echoes. Research has shown that the minimum discriminable angle in the horizontal plane is 1.5° (Simmons et al., 1983), in the vertical plane is 3° (Lawrence and Simmons, 1982b) and range difference discrimination is 6-15 mm (Miller, 1991; Surlykke, 1992) in the big brown bat. Recent research findings also suggest horizontal and vertical cues are not dichotomous, and binaural cues are available for high frequency localization in the vertical plane
Sound localization in echolocating bats not only includes active echolocation, which means localizing the source of returning sonar echoes, but also passive listening, which refers to tracking sound sources produced in the environment, e.g. by conspecifics or prey in proximity. The bat’s azimuthal localization accuracy via active echolocation is higher than passive listening (Koay et al., 1997, 1998; Simmons, 1973). Although self-generated signals are believed to be the dominant mode for active sensing animals to probe the environment, passive sensing could play an important role in orientation and prey capture as well. Electric fish can detect electric fields which are produced by others and align themselves perpendicular to the outside electric fields (Hopkins, 2005). They often use this passive sensing during the encounter of conspecifics or as a stealth strategy to conceal their presence.
Possible Factors Influencing Echolocation Behavior
A bat dynamically adjusts its vocalizations to adapt to a continuously changing environment. In this thesis, two experimental conditions were created to study how big brown bats adjust their echolocation behavior to adapt to these changes. One condition is the modification of the bat’s external ear to modify spectral cues the bat uses for sound localization. The other condition is adding another individual into the same room with the bat to investigate how its presence affects the bat’s echolocation behavior. Modifying cues for sound localization has been demonstrated to disrupt the sound localization accuracy in humans
However, human subjects also showed that they were able to adapt and localize sound sources correctly with changed cues after a short period of time. Similar manipulations can be introduced to the bat’s external ear and used to study how the echolocating bat adjusts to its “new” ear. Deflecting the tragus of the big brown bat disrupted its vertical sound localization accuracy (Wotton and Simmons, 2000). Therefore, it is reasonable to deduce that tragus deflection affects the bat’s sound localization, especially in the vertical plane. The bat may modify its echolocation call design, such as bandwidth, duration or pulse interval, to compensate for changes in acoustic information, produced by tragus deflection. Alternatively, the bat may not change its echolocation behavior in response to ear manipulation, but instead adjust other behaviors, such as flight attack angle, to adapt to the new condition. Insectivorous bats use echolocation to navigate and forage in the wild, and they commonly fly in groups.
Therefore, it is important for one bat to avoid interference with another bat’s echolocation calls when two or more bats fly and forage in proximity. The prey capture behavior of bats is affected by echolocation calls produced by other bats (Dunning and Roeder, 1965). Acoustic interference experiments on Noctilio albiventris (Roverud and Grinnell, 1985a, 1985b) and Rhinolophus rouxi (Roverud, 1989) have reported that the distance discrimination ability of these two species was disrupted by artificial signals which were similar to the bat’s own sonar vocalizations. The degree of interference is related to the similarity between the artificial signal and the bat’s echolocation calls. In addition, the timing of the interference signals relative to echo arrival could affect the bat’s ranging ability as well. Previous studies have demonstrated that vocalizations from conspecifics disrupt the bat’s prey capture or range determination, and the level of influence depends on the similarity between the interfering signal and the bat’s echolocation calls. Ranging ability of E. fuscus is impaired by the signal from another bat’s emission (Masters and Raver, 1996). Evidence shows that bats adjusted the spectral or temporal features of echolocation calls when foraging in groups
Echolocating bats are flying animals and some of their flight behaviors may be comparable to other flying animals that use vision rather than audition to guide their flight. How the bat adapts its flight behavior to capture prey with modified external ears or in the presence of a competitor in a large flight room is investigated here. Human subjects show changes in their motor behavior when their vision is distorted by prisms. Bats may exhibit similar modifications in their flight behavior when the sound localization cues are manipulated. Another conspecific may also affect the bat’s flight trajectories and its ability to capture prey.
Possible Factors Influence the Flight Behavior
Left-right or up-down reversal prisms disrupt the visual input of human subjects, but they adapt to the new input by adjusting their motor control after a period of practice (Stratton, 1896; 1897a; 1897b). Sound localization cue changes may induce similar adaptive behavior in echolocating bats. For example, although the bat may miss a direct attack on the target, but following external ear manipulation, it may manage to acquire the correct position of the target through its tactile sense or olfaction. Upon subsequent approaches to a prey item, the bat may adjust its flight trajectory to compensate for its estimate of target location and intercept the prey successfully. Modifications in flight behavior, especially prey capture behavior, are expected following manipulation of the bat’s external ear. The alternative result is that the bat does not change its flight behavior but changes its sonar call features to adapt to the modification of its external ears. A combination of these two strategies is also possible.
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Dissertation Done by Chen Chiu, University of Maryland