What determines the information update rate in echolocating bats.

The rate of sensory update is one of the most important parameters of any sensory system. The acquisition rate of most sensory systems is fixed and has been optimized by evolution to the needs of the animal. Echolocating bats have the ability to adjust their sensory update rate which is determined by the intervals between emissions - the inter-pulse intervals (IPI). The IPI is routinely adjusted, but the exact factors driving its regulation are unknown. We use on-board audio recordings to determine how four species of echolocating bats with different foraging strategies regulate their sensory update rate during commute flights. We reveal strong correlations between the IPI and various echolocation and movement parameters. Specifically, the update rate increases when the signals' peak-energy frequency and intensity increases while the update rate decreases when flight speed and altitude increases. We suggest that bats control their information update rate according to the behavioral mode they are engaged in, while always maintaining sensory continuity. Specifically, we suggest that bats apply two modes of attention during commute flights. Our data moreover suggests that bats emit echolocation signals at accurate intervals without the need for external feedback.

Pregnancy-related sensory deficits might impair foraging in echolocating bats.

BACKGROUND: Reproduction entails substantial demands throughout its distinct stages. The mammalian gestation period imposes various energetic costs and movement deficits, but its effects on the sensory system are poorly understood. Bats rely heavily on active sensing, using echolocation to forage in complete darkness, or when lighting is uncertain. We examined the effects of pregnancy on bat echolocation. RESULTS: We show that pregnant Kuhl's pipistrelles (Pipistrellus kuhlii) altered their echolocation and flight behavior. Specifically, pregnant bats emitted longer echolocation signals at an ~ 15% lower rate, while flying more slowly and at a lower altitude compared to post-lactating females. A sensorimotor foraging model suggests that these changes could lead to an ~ 15% reduction in hunting performance during pregnancy. CONCLUSIONS: Sensory deficits related to pregnancy could impair foraging in echolocating bats. Our study demonstrates an additional cost of reproduction of possible relevance to other sensory modalities and organisms.

Echolocating bats rapidly adjust their mouth gape to control spatial acquisition when scanning a target.

BACKGROUND: As well known to any photographer, controlling the "field of view" offers an extremely powerful mechanism by which to adjust target acquisition. Only a few natural sensory systems can actively control their field of view (e.g., dolphins, whales, and bats). Bats are known for their active sensing abilities and modify their echolocation signals by actively controlling their spectral and temporal characteristics. Less is known about bats' ability to actively modify their bio-sonar field of view. RESULTS: We show that Pipistrellus kuhlii bats rapidly narrow their sensory field of view (i.e., their bio-sonar beam) when scanning a target. On-target vertical sonar beams were twofold narrower than off-target beams. Continuous measurements of the mouth gape of free-flying bats revealed that they control their bio-sonar beam by a ~3.6 mm widening of their mouth gape: namely, bats open their mouth to narrow the beam and vice versa. CONCLUSIONS: Bats actively and rapidly control their echolocation vertical beam width by modifying their mouth gape. We hypothesize that narrowing their vertical beam narrows the zone of ensonification when estimating the elevation of a target. In other words, bats open their mouth to improve sensory localization.

TrackUSF, a novel tool for automated ultrasonic vocalization analysis, reveals modified calls in a rat model of autism.

BACKGROUND: Various mammalian species emit ultrasonic vocalizations (USVs), which reflect their emotional state and mediate social interactions. USVs are usually analyzed by manual or semi-automated methodologies that categorize discrete USVs according to their structure in the frequency-time domains. This laborious analysis hinders the effective use of USVs as a readout for high-throughput analysis of behavioral changes in animals. RESULTS: Here we present a novel automated open-source tool that utilizes a different approach towards USV analysis, termed TrackUSF. To validate TrackUSF, we analyzed calls from different animal species, namely mice, rats, and bats, recorded in various settings and compared the results with a manual analysis by a trained observer. We found that TrackUSF detected the majority of USVs, with less than 1% of false-positive detections. We then employed TrackUSF to analyze social vocalizations in Shank3-deficient rats, a rat model of autism, and revealed that these vocalizations exhibit a spectrum of deviations from appetitive calls towards aversive calls. CONCLUSIONS: TrackUSF is a simple and easy-to-use system that may be used for a high-throughput comparison of ultrasonic vocalizations between groups of animals of any kind in any setting, with no prior assumptions.

Adaptive learning and recall of motor-sensory sequences in adult echolocating bats.

BACKGROUND: Learning to adapt to changes in the environment is highly beneficial. This is especially true for echolocating bats that forage in diverse environments, moving between open spaces to highly complex ones. Bats are known for their ability to rapidly adjust their sensing according to auditory information gathered from the environment within milliseconds but can they also benefit from longer adaptive processes? In this study, we examined adult bats' ability to slowly adapt their sensing strategy to a new type of environment they have never experienced for such long durations, and to then maintain this learned echolocation strategy over time. RESULTS: We show that over a period of weeks, Pipistrellus kuhlii bats gradually adapt their pre-takeoff echolocation sequence when moved to a constantly cluttered environment. After adopting this improved strategy, the bats retained an ability to instantaneously use it when placed back in a similarly cluttered environment, even after spending many months in a significantly less cluttered environment. CONCLUSIONS: We demonstrate long-term adaptive flexibility in sensory acquisition in adult animals. Our study also gives further insight into the importance of sensory planning in the initiation of a precise sensorimotor behavior such as approaching for landing.

Segregating signal from noise through movement in echolocating bats.

Segregating signal from noise is one of the most fundamental problems shared by all biological and human-engineered sensory systems. In echolocating bats that search for small objects such as tiny insects in the presence of large obstacles (e.g., vegetation), this task can pose serious challenges as the echoes reflected from the background might be several times louder than the desired signal. Bats' ability to adjust their sensing, specifically their echolocation signal and sequence design has been deeply studied. In this study, we show that in addition to adjusting their sensing, bats also use movement in order to segregate desired echoes from background noise. Bats responded to an acoustically echoic background by adjusting their angle of attack. Specifically, the bats in our experiment used movement and not adaptation of sensory acquisition in order to overcome a sensory challenge. They approached the target at a smaller angle of attack, which results in weaker echoes from the background as was also confirmed by measuring the echoes of the setup from the bat's point of view. Our study demonstrates the importance of movement in active sensing.

An annotated dataset of Egyptian fruit bat vocalizations across varying contexts and during vocal ontogeny.

Animal acoustic communication research depends on our ability to record the vocal behaviour of different species. Only rarely do we have the opportunity to continuously follow the vocal behaviour of a group of individuals of the same species for a long period of time. Here, we provide a database of Egyptian fruit bat vocalizations, which were continuously recorded in the lab in several groups simultaneously for more than a year. The dataset includes almost 300,000 files, a few seconds each, containing social vocalizations and representing the complete vocal repertoire used by the bats in the experiment period. Around 90,000 files are annotated with details about the individuals involved in the vocal interactions, their behaviours and the context. Moreover, the data include the complete vocal ontogeny of pups, from birth to adulthood, in different conditions (e.g., isolated or in a group). We hope that this comprehensive database will stimulate studies that will enhance our understanding of bat, and mammal, social vocal communication.

Everyday bat vocalizations contain information about emitter, addressee, context, and behavior.

Animal vocal communication is often diverse and structured. Yet, the information concealed in animal vocalizations remains elusive. Several studies have shown that animal calls convey information about their emitter and the context. Often, these studies focus on specific types of calls, as it is rarely possible to probe an entire vocal repertoire at once. In this study, we continuously monitored Egyptian fruit bats for months, recording audio and video around-the-clock. We analyzed almost 15,000 vocalizations, which accompanied the everyday interactions of the bats, and were all directed toward specific individuals, rather than broadcast. We found that bat vocalizations carry ample information about the identity of the emitter, the context of the call, the behavioral response to the call, and even the call's addressee. Our results underline the importance of studying the mundane, pairwise, directed, vocal interactions of animals.

Vocal learning in a social mammal: Demonstrated by isolation and playback experiments in bats.

The evolution of human language is shrouded in mystery as it is unparalleled in the animal kingdom. Whereas vocal learning is crucial for the development of speech in humans, it seems rare among nonhuman animals. Songbirds often serve as a model for vocal learning, but the lack of a mammalian model hinders our quest for the origin of this capability. We report the influence of both isolation and playback experiments on the vocal development of a mammal, the Egyptian fruit bat. We continuously recorded pups from birth to adulthood and found that, when raised in a colony, pups acquired the adult repertoire, whereas when acoustically isolated, they exhibited underdeveloped vocalizations. Isolated pups that heard bat recordings exhibited a repertoire that replicated the playbacks they were exposed to. These findings demonstrate vocal learning in a social mammal, and suggest bats as a model for language acquisition.