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Calling louder and longer: how bats use biosonar under severe acoustic interference from other bats

Active-sensing systems such as echolocation provide animals with distinct advantages in dark environments. For social animals, however, like many bat species, active sensing can present problems as well: when many individuals emit bio-sonar calls simultaneously, detecting and recognizing the faint echoes generated by one's own calls amid the general cacophony of the group becomes challenging. This problem is often termed ‘jamming’ and bats have been hypothesized to solve it by shifting the spectral content of their calls to decrease the overlap with the jamming signals. We tested bats’ response in situations of extreme interference, mimicking a high density of bats. We played-back bat echolocation calls from multiple speakers, to jam flyingPipistrellus kuhlii bats, simulating a naturally occurring situation of many bats flying in proximity. We examined behavioural and echolocation parameters during search phase and target approach. Under severe interference, bats emitted calls of higher intensity and longer duration, and called more often. Slight spectral shifts were observed but they did not decrease the spectral overlap with jamming signals. We also found that pre-existing inter-individual spectral differences could allow self-call recognition. Results suggest that the bats’ response aimed to increase the signal-to-noise ratio and not to avoid spectral overlap.


1. Introduction

Most animals do not emit energy to sense their environment and orient in it, but rather they rely on energy (e.g. light, sound and magnetic) present in the environment. In contrast, several groups of animals generate outgoing signals in order to sense their surroundings [1]. Some examples include weakly electric fish [2] and echolocating dolphins [3] and bats [4].

The main advantages of active sensory systems that rely on own-energy emission are the ability to extract information in environments that do not allow use of vision (e.g. a dark night or turbid waters) and the ability to control different aspects of the received information by adapting the outgoing emission: the rate of information acquisition and the signal's directionality and design [59]. These advantages, however, do not come without a price. Animals using their own energy are subject to disadvantages such as signal double-energy loss owing to energy propagation and attenuation [10], energetic costs [11,12] and detection by potential prey [13].

Another often mentioned disadvantage of sensory systems that rely on energy emission is jamming by conspecifics, which has been well studied in weakly electric fish [14,15]. In bats, when two or more individuals of the same species fly in close proximity while emitting spectrally similar echolocation calls, loud conspecific calls might mask the faint echoes returning from a small insect, thus impairing the bat's ability to detect the insect. Moreover, even without direct masking but with conspecific calls and echoes returning in temporal proximity, the task of matching one's outgoing call to its appropriate incoming echo becomes challenging. It has been suggested that similar to weakly electric fish, bats actively alter the spectral characteristics of their calls (a behaviour known as Jamming Avoidance Response—JAR) aiming to reduce the potential ambiguity and masking resulting from conspecific calls. In the field: Obrist [16] reported an increase in call start- and peak-frequencies and in inter-pulse intervals, and a decrease in call duration when two Lasiurus borealis bats were foraging nearby. Ulanovsky et al. reported bidirectional JAR for Tadarida teniotis flying in pairs, where individuals shifted the frequency of their calls either upwards or downwards relative to conspecifics [17], and a unidirectional JAR, where bats always shifted their frequency upwards, was reported for Tadarida brasiliensis [18]. In contrast to these reports, a recent study that recorded audio on-board free-flying Rhinopoma microphyllum bats in the wild did not find any evidence for a JAR [19]. In the laboratory: a JAR was reported for Eptesicus fuscus flying in pairs: including changes in start and terminal call frequencies, bandwidth (BW), duration and sweep rate [20], while Pipistrellus abramuspresented with playback of recorded jamming sequences or artificial wide-band noise responded with a unidirectional frequency shift, and changes to emission timing [21]. Stationary T. brasiliensis were shown to reduce emission rate when jammed either by conspecific calls [22] or by wide-band noise [23]. Several other studies used playbacks of artificial signals to test jamming. Griffin et al. showed that Plecotus townsendii were remarkably resistant to jamming by artificial wide-band noise and attributed this mainly to the directionality of their ears [24]; and Bates et al. [25] showed that stationary E. fuscus performing a detection task employ bidirectional JAR by shifting the quasi-constant-frequency (QCF) component of their call either upwards or downwards relative to an artificial CF jamming tone.

Almost all of the above experiments restricted themselves to situations in which only two bats fly together. This is, however, the simplest jamming scenario, while it is well known that bats often forage in groups of several individuals [26] or even fly in swarms of dozens to many thousands [27,28]. The two exceptions that tested bats under more severe jamming did so with artificial (non-bat) signals [24,25]. To better understand how bats avoid extreme, yet naturally occurring jamming, we confronted bats with situations of severe jamming by multiple individuals, using natural bat-call playbacks. To this end, we flew bats in a confined space while jamming them with recordings of their own calls as well as recordings of one or more conspecifics, played back from an array of multiple speakers.

We used Pipistrellus kuhlii (Kuhl, 1817)—a small insectivorous bat (ca 5–9 g) common in the Mediterranean region, the Middle East and South Asia. This bat is commonly observed in tight groups of ca 5 individuals foraging around a street-light, while larger groups of up to dozens of individuals can often be seen foraging in high proximity over ponds. In such a dynamic situation, where individual bats pursue different targets using different trajectories and velocities, each bat is exposed to multiple constantly changing interfering conspecifics calls.

We trained four P. kuhlii to individually search for and land on a feeding platform in a small flight room. While the bat was flying, we played back intense bat calls from 12 speakers covering the room's walls and ceiling and recorded the bat's flight trajectory and echolocation signals. By using playbacks rather than actual flying conspecifics, we ensured that any modification in signal design was a response to acoustic jamming, and not an attempt to detect and localize other individuals. We consecutively played back a variety of echolocation sequences generating different types of jamming, including calls of the bat itself, calls of one or more conspecifics and calls that were reversed in time. These sequences were played at a duty-cycle of 40% or 100% imposing different degrees of jamming. In all cases, we ensured a maximum (peak to peak) sound level of at least 95 dB (SPL) at any location in the room, thus much more intense than any echo received by the bat.

We found that bats can deal with even the most extreme continuous jamming with almost no effect on their performance. We found that bats emitted longer and louder echolocation calls to deal with jamming. They also shifted call frequency, but they always increased the frequency whether the jamming signal was higher or lower than their own. Their response thus did not reduce the potential jamming. We therefore hypothesize that these modifications in call design aimed to increase signal-to-noise ratio (SNR) rather than increase the inter-individual spectral differences. We argue that the pre-existing inter-individual differences in call characteristics allow self-recognition even under such extreme conditions.


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Megabats and Microbats: Calling louder and longer: how bats use biosonar under severe acoustic interference from other bats
Calling louder and longer: how bats use biosonar under severe acoustic interference from other bats
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