Clutter resilience via auditory stream segregation in echolocating greater mouse-eared bats.

Bats use echolocation to navigate and hunt in darkness, and must in that process segregate target echoes from unwanted clutter echoes. Bats may do this by approaching a target at steep angles relative to the plane of the background, utilizing their directional transmission and receiving systems to minimize clutter from background objects, but it remains unknown how bats negotiate clutter that cannot be spatially avoided. Here, we tested the hypothesis that when movement no longer offers spatial release, echolocating bats mitigate clutter by calling at lower source levels and longer call intervals to ease auditory streaming. We trained five greater mouse-eared bats (Myotis myotis) to land on a spherical loudspeaker with two microphones attached. We used a phantom-echo setup, where the loudspeaker/target transmitted phantom clutter echoes by playing back the bats' own calls at time delays of 1, 3 and 5 ms with a virtual target strength 7 dB higher than the physical target. We show that the bats successfully landed on the target, irrespective of the clutter echo delays. Rather than decreasing their source levels, the bats used similar source level distributions in clutter and control trials. Similarly, the bats did not increase their call intervals, but instead used the same distribution of call intervals across control and clutter trials. These observations reject our hypothesis, leading us to conclude that bats display great resilience to clutter via short auditory integration times and acute auditory stream segregation rather than via biosonar adjustments.

Superfast Lombard response in free-flying, echolocating bats.

Acoustic cues are crucial to communication, navigation, and foraging in many animals, which hence face the problem of detecting and discriminating these cues in fluctuating noise levels from natural or anthropogenic sources. Such auditory dynamics are perhaps most extreme for echolocating bats that navigate and hunt prey on the wing in darkness by listening for weak echo returns from their powerful calls in complex, self-generated umwelts.1,2 Due to high absorption of ultrasound in air and fast flight speeds, bats operate with short prey detection ranges and dynamic sensory volumes,3 leading us to hypothesize that bats employ superfast vocal-motor adjustments to rapidly changing sensory scenes. To test this hypothesis, we investigated the onset and offset times and magnitude of the Lombard response in free-flying echolocating greater mouse-eared bats exposed to onsets of intense constant or duty-cycled masking noise during a landing task. We found that the bats invoked a bandwidth-dependent Lombard response of 0.1-0.2 dB per dB increase in noise, with very short delay and relapse times of 20 ms in response to onsets and termination of duty-cycled noise. In concert with the absence call time-locking to noise-free periods, these results show that free-flying bats exhibit a superfast, but hard-wired, vocal-motor response to increased noise levels. We posit that this reflex is mediated by simple closed-loop audio-motor feedback circuits that operate independently of wingbeat and respiration cycles to allow for rapid adjustments to the highly dynamic auditory scenes encountered by these small predators.

Daubenton's bats maintain stereotypical echolocation behaviour and a lombard response during target interception in light.

Most bats hunt insects on the wing at night using echolocation as their primary sensory modality, but nevertheless maintain complex eye anatomy and functional vision. This raises the question of how and when insectivorous bats use vision during their largely nocturnal lifestyle. Here, we test the hypothesis that the small insectivorous bat, Myotis daubentonii, relies less on echolocation, or dispenses with it entirely, as visual cues become available during challenging acoustic noise conditions. We trained five wild-caught bats to land on a spherical target in both silence and when exposed to broad-band noise to decrease echo detectability, while light conditions were manipulated in both spectrum and intensity. We show that during noise exposure, the bats were almost three times more likely to use multiple attempts to solve the task compared to in silent controls. Furthermore, the bats exhibited a Lombard response of 0.18 dB/dBnoise and decreased call intervals earlier in their flight during masking noise exposures compared to in silent controls. Importantly, however, these adjustments in movement and echolocation behaviour did not differ between light and dark control treatments showing that small insectivorous bats maintain the same echolocation behaviour when provided with visual cues under challenging conditions for echolocation. We therefore conclude that bat echolocation is a hard-wired sensory system with stereotyped compensation strategies to both target range and masking noise (i.e. Lombard response) irrespective of light conditions. In contrast, the adjustments of call intervals and movement strategies during noise exposure varied substantially between individuals indicating a degree of flexibility that likely requires higher order processing and perhaps vocal learning.

Low foraging rates drive large insectivorous bats away from urban areas.

Urbanization has significant impacts on wildlife and ecosystems and acts as an environmental filter excluding certain species from local ecological communities. Specifically, it may be challenging for some animals to find enough food in urban environments to achieve a positive energy balance. Because urban environments favor small-sized bats with low energy requirements, we hypothesized that common noctules (Nyctalus noctula) acquire food at a slower rate and rely less on conspecifics to find prey in urban than in rural environments due to a low food abundance and predictable distribution of insects in urban environments. To address this, we estimated prey sizes and measured prey capture rates, foraging efforts, and the presence of conspecifics during hunting of 22 common noctule bats equipped with sensor loggers in an urban and rural environment. Even though common noctule bats hunted similar-sized prey in both environments, urban bats captured prey at a lower rate (mean: 2.4 vs. 6.3 prey attacks/min), and a lower total amount of prey (mean: 179 vs. 377 prey attacks/foraging bout) than conspecifics from rural environments. Consequently, the energy expended to capture prey was higher for common noctules in urban than in rural environments. In line with our prediction, urban bats relied less on group hunting, likely because group hunting was unnecessary in an environment where the spatial distribution of prey insects is predictable, for example, in parks or around floodlights. While acknowledging the limitations of a small sample size and low number of spatial replicates, our study suggests that scarce food resources may make urban habitats unfavorable for large bat species with higher energy requirements compared to smaller bat species. In conclusion, a lower food intake may displace larger species from urban areas making habitats with high insect biomass production key for protecting large bat species in urban environments.

Echolocating bats prefer a high risk-high gain foraging strategy to increase prey profitability.

Predators that target multiple prey types are predicted to switch foraging modes according to prey profitability to increase energy returns in dynamic environments. Here, we use bat-borne tags and DNA metabarcoding of feces to test the hypothesis that greater mouse-eared bats make immediate foraging decisions based on prey profitability and changes in the environment. We show that these bats use two foraging strategies with similar average nightly captures of 25 small, aerial insects and 29 large, ground-dwelling insects per bat, but with much higher capture success in the air (76%) vs ground (30%). However, owing to the 3-20 times larger ground prey, 85% of the nightly food acquisition comes from ground prey despite the 2.5 times higher failure rates. We find that most bats use the same foraging strategy on a given night suggesting that bats adapt their hunting behavior to weather and ground conditions. We conclude that these bats use high risk-high gain gleaning of ground prey as a primary foraging tactic, but switch to aerial hunting when environmental changes reduce the profitability of ground prey, showing that prey switching matched to environmental dynamics plays a key role in covering the energy intake even in specialized predators.

Bats are the only mammals capable of powered flight and therefore need a high calorie intake to survive. They hunt at night using the echoes made by their own calls to navigate and locate prey. Bats can use different tactics to hunt for food: hawking involves catching prey on the wing and requires fast aerial manoeuvring and more intense echolocation calls, while gleaning involves listening for movements of ground and water dwelling prey as the bat hovers. Some bat species specialise as hawkers or gleaners but maintain the ability to hunt with both methods. With the ever-growing impact of human activities on their habitats, it is important to understand how adaptable bats feeding habits are to changes in their environment. To find out more, Stidsholt et al. studied greater mouse-eared bats, which primarily feed by gleaning. To understand how this species chooses feeding strategies they fitted bats with tiny backpacks that could record the animal's location and foraging behaviour. They could also monitor prey sizes by recording the sounds of the bats chewing. Stidsholt et al. found that, although these bats tried to catch prey on the ground more often than in the air, they were actually more successful as airborne hunters. Despite this, gleaning was still a more profitable strategy for them, because the body mass of ground prey is higher than for airborne prey. Gleaning gave the bats a higher calorie intake, even though their capture rate was lower. Although feeding habits differed slightly between individual bats on a given night of monitoring, there were much larger changes in behaviour between different feeding nights. This shows that, although this species of bat prefers gleaning, they will switch strategies to hawking as their environment changes, for example if there is more airborne prey, or if rainfall makes it hard to hear movements on the ground. Bats tended to get enough calories for their needs but did not catch more prey than they needed to survive. Stidsholt et al. concluded that greater mouse-eared bats change their feeding strategy based on prey availability and size, as well as the bat's environment. Their study provides an important insight into how bats fit into the ecosystem and how adaptable bats might be to changes in their habitat.

Echolocating Daubenton's bats call louder, but show no spectral jamming avoidance in response to bands of masking noise during a landing task.

Echolocating bats listen for weak echoes to navigate and hunt, which makes them prone to masking from background noise and jamming from other bats and prey. As for electrical fish that display clear spectral jamming avoidance responses (JAR), bats have been reported to mitigate the effects of jamming by shifting the spectral contents of their calls, thereby reducing acoustic interference to improve echo-to-noise ratio (ENR). Here, we tested the hypothesis that frequency-modulating bats (FM bats) employ a spectral JAR in response to six masking noise bands ranging from 15 to 90 kHz, by measuring the -3 dB endpoints and peak frequency of echolocation calls from five male Daubenton's bats (Myotis daubentonii) during a landing task. The bats were trained to land on a noise-generating spherical transducer surrounded by a star-shaped microphone array, allowing for acoustic localization and source parameter quantification of on-axis calls. We show that the bats did not employ spectral JAR as the peak frequency during jamming remained unaltered compared with that of silent controls (all P>0.05, 60.73±0.96 kHz, mean±s.e.m.), and -3 dB endpoints decreased in noise irrespective of treatment type. Instead, Daubenton's bats responded to acoustic jamming by increasing call amplitude via a Lombard response that was bandwidth dependent, ranging from a mean of 0.05 dB/dB (95% confidence interval 0.04-0.06 dB/dB) noise for the most narrowband noise (15-30 kHz) to 0.17 dB/dB (0.16-0.18 dB/dB) noise for the most broadband noise (30-90 kHz). We conclude that Daubenton's bats, despite having the vocal flexibility to do so, do not employ a spectral JAR, but defend ENRs via a bandwidth-dependent Lombard response.

Echolocating Daubenton's bats are resilient to broadband, ultrasonic masking noise during active target approaches.

Echolocating bats hunt prey on the wing under conditions of poor lighting by emission of loud calls and subsequent auditory processing of weak returning echoes. To do so, they need adequate echo-to-noise ratios (ENRs) to detect and distinguish target echoes from masking noise. Early obstacle avoidance experiments report high resilience to masking in free-flying bats, but whether this is due to spectral or spatiotemporal release from masking, advanced auditory signal detection or an increase in call amplitude (Lombard effect) remains unresolved. We hypothesized that bats with no spectral, spatial or temporal release from masking noise defend a certain ENR via a Lombard effect. We trained four bats (Myotis daubentonii) to approach and land on a target that broadcasted broadband noise at four different levels. An array of seven microphones enabled acoustic localization of the bats and source level estimation of their approach calls. Call duration and peak frequency did not change, but average call source levels (SLRMS, at 0.1 m as dB re. 20 µPa) increased, from 112 dB in the no-noise treatment, to 118 dB (maximum 129 dB) at the maximum noise level of 94 dB re. 20 µPa root mean square. The magnitude of the Lombard effect was small (0.13 dB SLRMS dB-1 of noise), resulting in mean broadband and narrowband ENRs of -11 and 8 dB, respectively, at the highest noise level. Despite these poor ENRs, the bats still performed echo-guided landings, making us conclude that they are very resilient to masking even when they cannot avoid it spectrally, spatially or temporally.

Inflight head stabilization associated with wingbeat cycle and sonar emissions in the lingual echolocating Egyptian fruit bat, Rousettus aegyptiacus.

Sensory processing of environmental stimuli is challenged by head movements that perturb sensorimotor coordinate frames directing behaviors. In the case of visually guided behaviors, visual gaze stabilization results from the integrated activity of the vestibuloocular reflex and motor efference copy originating within circuits driving locomotor behavior. In the present investigation, it was hypothesized that head stabilization is broadly implemented in echolocating bats during sustained flight, and is temporally associated with emitted sonar signals which would optimize acoustic gaze. Predictions from these hypotheses were evaluated by measuring head and body kinematics with motion sensors attached to the head and body of free-flying Egyptian fruit bats. These devices were integrated with ultrasonic microphones to record sonar emissions and elucidate the temporal association with periods of head stabilization. Head accelerations in the Earth-vertical axis were asymmetric with respect to wing downstroke and upstroke relative to body accelerations. This indicated that inflight head and body accelerations were uncoupled, outcomes consistent with the mechanisms that limit vertical head acceleration during wing downstroke. Furthermore, sonar emissions during stable flight occurred most often during wing downstroke and head stabilization, supporting the conclusion that head stabilization behavior optimized sonar gaze and environmental interrogation via echolocation.

Wild bats briefly decouple sound production from wingbeats to increase sensory flow during prey captures.

Active sensing animals such as echolocating bats produce the energy with which they probe their environment. The intense echolocation calls of bats are energetically expensive, but their cost can be reduced by synchronizing the exhalations needed to vocalize to wingbeats. Here, we use sound-and-movement recording tags to investigate how wild bats balance efficient sound production with information needs during foraging and navigation. We show that wild bats prioritize energy efficiency over sensory flow when periodic snapshots of the acoustic scene are sufficient during travel and search. Rapid calls during tracking and interception of close prey are decoupled from the wingbeat but are weaker and comprise <2% of all calls during a night of hunting. The limited use of fast sonar sampling provides bats with high information update rates during critical hunting moments but adds little to their overall costs of sound production despite the inefficiency of decoupling calls from wingbeats.

Hunting bats adjust their echolocation to receive weak prey echoes for clutter reduction.

How animals extract information from their surroundings to guide motor patterns is central to their survival. Here, we use echo-recording tags to show how wild hunting bats adjust their sensory strategies to their prey and natural environment. When searching, bats maximize the chances of detecting small prey by using large sensory volumes. During prey pursuit, they trade spatial for temporal information by reducing sensory volumes while increasing update rate and redundancy of their sensory scenes. These adjustments lead to very weak prey echoes that bats protect from interference by segregating prey sensory streams from the background using a combination of fast-acting sensory and motor strategies. Counterintuitively, these weak sensory scenes allow bats to be efficient hunters close to background clutter broadening the niches available to hunt for insects.

Energy compensation and received echo level dynamics in constant-frequency bats during active target approaches.

Bats have been reported to adjust the energy of their outgoing vocalizations to target range (R) in a logarithmic fashion close to 20log10R which has been interpreted as providing one-way compensation for increasing echo levels during target approaches. However, it remains unknown how species using high-frequency calls, which are strongly affected by absorption, adjust their vocal outputs during approaches to point targets. We hypothesized that such species should compensate less than the 20log10R model predicts at longer distances and more at shorter distances as a consequence of the significant influence of absorption at longer ranges. Using a microphone array and an acoustic recording tag, we show that the output adjustments of two Hipposideros pratti and one Hipposiderosarmiger do not decrease logarithmically during approaches to different-sized targets. Consequently, received echo levels increase dramatically early in the approach phase with near-constant output levels, but level off late in the approach phase as a result of substantial output reductions. To improve echo-to-noise ratio, we suggest that bats using higher frequency vocalizations compensate less at longer ranges, where they are strongly affected by absorption. Close to the target, they decrease their output levels dramatically to mitigate reception of very high echo levels. This strategy maintains received echo levels between 6 and 40 dB re. 20 µPa2 s across different target sizes. The bats partially compensated for target size, but not in a one-to-one dB fashion, showing that these bats do not seek to stabilize perceived echo levels, but may instead use them to gauge target size.