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Paper ICA2016-820 Buenos Aires – 5 to 9 September, 2016 Acoustics for the 21st Century… PROCEEDINGS of the 22nd International Congress on Acoustics Animal bioacoustics: Paper ICA2016-820 How echolocating bats listen to their echoes (a) (b) (c) Hiroshi Riquimaroux (a) Shandong University, China (b) Brown University, U. S. A., [email protected] (c) Tokyo Medical Center, Japan Abstract The echolocating bats emit ultrasonic pulses and listen to echoes to catch preys and measure characteristics about their environment during their flight. It has been known that they can precisely measure these in real time. However, returning echoes from small objects are scattered and attenuated easily. We have conducted experiments with flying bats and non-flying bats to investigate how they extract information they need. They precisely detect preys and measure characteristics surrounding their environment. Findings have shown that the bats do not directly listen to the echoes reflected from a small insect but listen to echoes reflecting from a large stable object located far way, which contain information about a flying insect. Summarized data are discussed. Keywords: bat echolocation system, Doppler-shift compensation, Jamming avoidance 22nd International Congress on Acoustics, ICA 2016 Buenos Aires – 5 to 9 September, 2016 Acoustics for the 21st Century… How echolocating bats listen to their echoes 1 Introduction Echolocating bats emit ultrasonic pulses and listen to returning echoes to catch their preys and to measure their surroundings. However their returning echoes directly coming back from a small target is supposed to be scattered and attenuated quickly to be very weak. It has been known that they can precisely measure these in real time. How do the bats listen to weak echoes and make precise judgments? We have conducted experiments with flying bats and non-flying bats to investigate how they extract information they need. 2 Measurement of multiple targets in real time We developed a small and light wireless onboard microphone system, Telemike, in order to record emitting pulses and returning echoes from a flying bat at its head (Riquimaroux and Watanabe, 2000)[8]. Findings from CF-FM bats indicated that they would measure distances of front and side targets alternately, listening to echoes with longer delay from a front target and shorter delay from a side target alternately. Findings showed that CF-FM bats compensate their Doppler-shifted returning echo frequencies so that the second harmonics would be constant, called Doppler- shift compensation. Moreover, they independently conducted Doppler-shift compensation for front and side walls alternately (Hiryu et al., 2005)[3]. The amount of Doppler-shift compensation was greater for the front wall than side wall because the velocity against the front wall was higher than that against the side wall. They appear to employ a time-sharing system to measure multiple targets in real time. 3 Compensating echo signals The Telemike measurements illustrated that flying echolocating CF-FM bats conduct Doppler- shift compensation. The Telemike experiments also showed both CF-FM and FM bats controlled emitting pulse amplitudes so that echo amplitudes returning from a wall would be constant. So, frequency and amplitude of returning pulses from CF-FM bats would be constant (Hiryu et al., 2008)[4].However, the bats conducted Doppler-shift compensation for front and side walls but not for a flying insect. So, they were not listening to echoes directly coming back from a small flying insect but were listening to echoes returning from a large stable object, a wall. They place an insect between a distant wall and themselves so that they may detect frequency modulation in the CF signal in returning echoes (Mantani et al, 2012)[6]. 2 22nd International Congress on Acoustics, ICA 2016 Buenos Aires – 5 to 9 September, 2016 Acoustics for the 21st Century… Fig. 1 Doppler-shift compensation of bats during moth-capture flight. (Top) Changes in the CF2 frequencies of pulses (triangle) and echoes (circles) as a function of time to capture for the flight shown in Fig. 6a. Red solid, purple open circles and blue cross indicate the measured CF2 frequencies of returning echoes from the front, left wall and ceiling of the chamber, respectively. Green solid square indicates the estimated CF2 frequency of the moth from the relative velocity of the bat and the moth (see text). (Bottom) Changes in the CF2 frequencies of pulses and echoes during moth-capture flight of bat B. 3 22nd International Congress on Acoustics, ICA 2016 Buenos Aires – 5 to 9 September, 2016 Acoustics for the 21st Century… 4 Auditory fovea CF-FM bats have been reported to have an auditory fovea, over-representation of the second harmonic frequency of CF in echo, throughout the auditory pathway from the inner ear (Kössl and Vater, 1985)[5] up to the auditory cortex (Suga, 1984)[10]. However, the auditory system of FM bats has not yet been well investigated compared to that of CF-FM bats, especially if they have an auditory fovea system. Acoustic recordings in the field revealed that FM bats would emit pseudo CF pulses as long as about 10 ms when they were searching for a flying prey (Surlykke and Moss, 2000)[11]. The frequency of pseudo CF pulses matches to their terminal frequency of downward FM sweep, around 40 kHz for Pipistrellus abramus while around 20 kHz for Eptesicus fuscus. This evidence may bring a hypothesis that FM bats also detect wing beats of flying prey as frequency modulation with pseudo CF pulses. In order to detect fine frequency modulation, the bats need higher frequency resolution around the terminal frequency of downward FM pulses. Interestingly, previous neurophysiological studies of the inferior colliculi of E. fuscus and P. abramus indicated overrepresentation of the terminal frequency (Poon et al., 1990 for E. Fuscus; Goto et al., 2010 for P. abramus)[7][2]. In other words, majority of neurons in the central nucleus of the inferior colliculus those bats were tuned to frequency ranges of 20 kHz (E. fuscus) and 40 kHz (P. abramus), respectively. This evidence suggests that frequency resolution of the inferior colliculus appears to be much higher in frequency range of the pseudo CF frequency than other frequencies, implying the threshold for frequency discrimination would be very low in these frequency ranges. However, this evidence does not necessarily mean that the absolute threshold of these frequency ranges would be very low. 5 System to avoid jamming CF-FM bats are known to use amplified second harmonic in CF component, which creates a fovea structure throughout the auditory system from the cochlea to the auditory cortex (Suga, 1984)[10]. Echolocating CF-FM bats of the same species tend to use very similar second harmonic frequencies. Many CF-FM bats fly together when they echolocate. Then, how they can avoid vocalized signals emitted by other bats, which are very similar in characteristics spectrally and temporally. In general we tend to make a hypothesis that the bats will expand frequency distance farther so that vocalizations from other conspecific bats don’t disturb each other. However, it appears that they conduct a completely opposite behavior. They tend to shift their CF frequency even closer (Furusawa et al., 2012)[1]. It is very attractive to investigate why they would employ this maneuver. 4 22nd International Congress on Acoustics, ICA 2016 Buenos Aires – 5 to 9 September, 2016 Acoustics for the 21st Century… Fig. 2 Two representative changes in reference frequencies for two bats between single and paired flights. (a) Bat #913 vs #916; these two bats showed an average difference in the Frest (0.10 kHz, P < 0.001). (b) Bat #910 vs #682; these two bats showed the smallest interindividual difference in Frest (0.03 kHz, P < 0.01) on the experimental day. Single flight sessions were conducted before (S1) and after (S2) the paired flights. Data for paired flights were taken from three approach flights during one recording session (P1-P3). A Student's t- test was applied for the differences in reference frequencies between the two bats (DFs); **, P < 0.01; ***, P < 0.001. 5 22nd International Congress on Acoustics, ICA 2016 Buenos Aires – 5 to 9 September, 2016 Acoustics for the 21st Century… 6 Sensitive and durable auditory system CF-FM bats are known to use amplified second harmonic in CF component, which creates a Usually, a sensitive system tends to be fragile, and easy to be damaged. However, the auditory system in echolocating bats appears to be different. It is sensitive and also tough, hard to be broken down. The echolocating bats have to listen to returning weak echoes. Studies on CF-FM bats indicated that a specific structure of the basilar membrane in the inner ear could create a large resonance to detect weak echoes (Kössl and Vater, 1985)[5]. However, almost nothing has been known about the basilar membrane and hair cells of FM bats. We conducted experiments where FM bats were exposed to intense wideband noise (from 10 to 80 kHz, 90 dB SPL re to 20 µPa). The auditory brainstem responses (ABR) were recor ded at around the cochlear nucleus before and after the noise exposure to examine effects of noise exposure. Results showed that any differences were found in ABR between before and after noise exposure (Simmons et al., 2015)[9]. So, echolocating bats appear to have sensitive and durable characteristics in the auditory system. 7 Conclusions Echolocating bats emit a pulse and listen to returning echoes from target objects. Their echolocation system is an excellent model for real time processing with extremely slow processors, getting a good signal to noise ratio in very noisy environment, noise resistant system with high sensitivity (low threshold), and so on. We look forward to development of future studies.
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