Perceptual strategies in active and passive hearing of neotropical bats

Basic spectral and temporal sound properties, such as frequency content and timing, are evaluated by the auditory system to build an internal representation of the external world and to generate auditory guided behaviour. Using echolocating bats as model system, I investigated aspects of spectral and temporal processing during echolocation and in relation to passive listening, and the echo-acoustic object recognition for navigation. In the first project (chapter 2), the spectral processing during passive and active hearing was compared in the echolocting bat Phyllostomus discolor. Sounds are ubiquitously used for many vital behaviours, such as communication, predator and prey detection, or echolocation. The frequency content of a sound is one major component for the correct perception of the transmitted information, but it is distorted while travelling from the sound source to the receiver. In order to correctly determine the frequency content of an acoustic signal, the receiver needs to compensate for these distortions. We first investigated whether P. discolor compensates for distortions of the spectral shape of transmitted sounds during passive listening. Bats were trained to discriminate lowpass filtered from highpass filtered acoustic impulses, while hearing a continuous white noise background with a flat spectral shape. We then assessed their spontaneous classification of acoustic impulses with varying spectral content depending on the background’s spectral shape (flat or lowpass filtered). Lowpass filtered noise background increased the proportion of highpass classifications of the same filtered impulses, compared to white noise background. Like humans, the bats thus compensated for the background’s spectral shape. In an active-acoustic version of the identical experiment, the bats had to classify filtered playbacks of their emitted echolocation calls instead of passively presented impulses. During echolocation, the classification of the filtered echoes was independent of the spectral shape of the passively presented background noise. Likewise, call structure did not change to compensate for the background’s spectral shape. Hence, auditory processing differs between passive and active hearing, with echolocation representing an independent mode with its own rules of auditory spectral analysis. The second project (chapter 3) was concerned with the accurate measurement of the time of occurrence of auditory signals, and as such also distance in echolocation. In addition, the importance of passive listening compared to echolocation turned out to be an unexpected factor in this study. To measure the distance to objects, called ranging, bats measure the time delay between an outgoing call and its returning echo. Ranging accuracy received considerable interest in echolocation research for several reasons: (i) behaviourally, it is of importance for the bat’s ability to locate objects and navigate its surrounding, (ii) physiologically, the neuronal implementation of precise measurements of very short time intervals is a challenge and (iii) the conjectured echo-acoustic receiver of bats is of interest for signal processing. Here, I trained the nectarivorous bat Glossophaga soricina to detect a jittering real target and found a biologically plausible distance accuracy of 4–7 mm, corresponding to a temporal accuracy of 20–40 μs. However, presumably all bats did not learn to use the jittering echo delay as the first and most prominent cue, but relied on passive acoustic listening first, which could only be prevented by the playback of masking noise. This shows that even a non-gleaning bat heavily relies on passive acoustic cues and that the measuring of short time intervals is difficult. This result questions other studies reporting a sub-microsecond time jitter threshold. The third project (chapter 4) linked the perception of echo-acoustic stimuli to the appropriate behavioural reactions, namely evasive flight manoeuvres around virtual objects presented in the flight paths of wild, untrained bats. Echolocating bats are able to orient in complete darkness only by analysing the echoes of their emitted calls. They detect, recognize and classify objects based on the spectro-temporal reflection pattern received at the two ears. Auditory object analysis, however, is inevitably more complicated than visual object analysis, because the one-dimensional acoustic time signal only transmits range information, i.e., the object’s distance and its longitudinal extent. All other object dimensions like width and height have to be inferred from comparative analysis of the signals at both ears and over time. The purpose of this study was to measure perceived object dimensions in wild, experimentally naïve bats by video-recording and analysing the bats’ evasive flight manoeuvres in response to the presentation of virtual echo-acoustic objects with independently manipulated acoustic parameters. Flight manoeuvres were analysed by extracting the flight paths of all passing bats. As a control to our method, we also recorded the flight paths of bats in response to a real object. Bats avoided the real object by flying around it. However, we did not find any flight path changes in response to the presentation of several virtual objects. We assume that the missing spatial extent of virtual echo-acoustic objects, due to playback from only one loudspeaker, was the main reason for the failure to evoke evasive flight manoeuvres. This study therefore emphasises for the first time the importance of the spatial dimension of virtual objects, which were up to now neglected in virtual object presentations

Linking the sender to the receiver: vocal adjustments by bats to maintain signal detection in noise

Short-term adjustments of signal characteristics allow animals to maintain reliable communication in noise. Noise-dependent vocal plasticity often involves simultaneous changes in multiple parameters. Here, we quantified for the first time the relative contributions of signal amplitude, duration, and redundancy for improving signal detectability in noise. To this end, we used a combination of behavioural experiments on pale spear-nosed bats (Phyllostomus discolor) and signal detection models. In response to increasing noise levels, all bats raised the amplitude of their echolocation calls by 1.8-7.9 dB (the Lombard effect). Bats also increased signal duration by 13%-85%, corresponding to an increase in detectability of 1.0-5.3 dB. Finally, in some noise conditions, bats increased signal redundancy by producing more call groups. Assuming optimal cognitive integration, this could result in a further detectability improvement by up to 4 dB. Our data show that while the main improvement in signal detectability was due to the Lombard effect, increasing signal duration and redundancy can also contribute markedly to improving signal detectability. Overall, our findings demonstrate that the observed adjustments of signal parameters in noise are matched to how these parameters are processed in the receiver's sensory system, thereby facilitating signal transmission in fluctuating environments

Interspecific acoustic recognition in two European bat communities

Echolocating bats emit echolocation calls for spatial orientation and foraging. These calls are often species-specific and are emitted at high intensity and repetition rate. Therefore, these calls could potentially function in intra- and/or inter-specific bat communication. For example, bats in the field approach playbacks of conspecific feeding buzzes, probably because feeding buzzes indicate an available foraging patch. In captivity, some species of bats recognize and distinguish the echolocation calls of different sympatric species. However, it is still unknown if and how acoustic species-recognition mediates interspecific interactions in the field. Here we aim to understand eavesdropping on bat echolocation calls within and across species boundaries in wild bats. We presented playbacks of conspecific and heterospecific search calls and feeding buzzes to four bat species with different foraging ecologies. The bats were generally more attracted by feeding buzzes than search calls and more by the calls of conspecifics than their heterospecifics. Furthermore, bats showed differential reaction to the calls of the heterospecifics. In particular, Myotis capaccinii reacted equally to the feeding buzzes of conspecifics and to ecologically more similar heterospecifics. Our results confirm eavesdropping on feeding buzzes at the intraspecific level in wild bats and provide the first experimental quantification of potential eavesdropping in European bats at the interspecific level. Our data support the hypothesis that bat echolocation calls have a communicative potential that allows interspecific, and potentially intraspecific, eavesdropping in the wild

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

This study was funded by the Carlsberg Semper Ardens grant to P.T.M. and by the Emmy Noether program of the Deutsche Forschungsgemeinschaft (DFG; German Research Foundation, grant no. 241711556) to H.R.G. All experiments were carried out under the following licenses: 721/12.06.2017, 180/07.08.2018, and 795/17.05.2019.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.Publisher PDFPeer reviewe

Data from: Weather conditions determine attenuation and speed of sound: environmental limitations for monitoring and analysing bat echolocation

Echolocating bats are regularly studied to investigate auditory-guided behaviours and as important bioindicators. Bioacoustic monitoring methods based on echolocation calls are increasingly used for risk assessment and to ultimately inform conservation strategies for bats. As echolocation calls transmit through the air at the speed of sound, they undergo changes due to atmospheric and geometric attenuation. Both the speed of sound and atmospheric attenuation, however, are variable and determined by weather conditions, particularly temperature and relative humidity. Changing weather conditions thus cause variation in analysed call parameters, limiting our ability to detect and correctly analyse bat calls. Here, I use real-world weather data to exemplify the effect of varying weather conditions on the acoustic properties of air. I then present atmospheric attenuation and speed of sound for the global range of weather conditions and bat call frequencies to show their relative effects. Atmospheric attenuation is a non-linear function of call frequency, temperature, relative humidity and atmospheric pressure. While atmospheric attenuation is strongly positively correlated with call frequency, it is also significantly influenced by temperature and relative humidity in a complex non-linear fashion. Variable weather conditions thus result in variable and unknown effects on the recorded call, affecting estimates of call frequency and intensity, particularly for high frequencies. Weather-induced variation in speed of sound reaches up to about ±3%, but is generally much smaller and only relevant for acoustic localisation methods of bats. The frequency- and weather-dependent variation in atmospheric attenuation has a three-fold effect on bioacoustic monitoring of bats: it limits our capability (1) to monitor bats equally across time, space, and species, (2) to correctly measure frequency parameters of bat echolocation calls, particularly for high-frequencies, and (3) to correctly identify bat species in species-rich assemblies or for sympatric species with similar call designs

Data from: Species-specific strategies increase unpredictability of escape flight in eared moths

1. Many prey species overlap in time and space and are hunted by the same predators. A common anti-predator behaviour are evasive manoeuvres to escape an attacking predator. The escape-tactic diversity hypothesis postulates that species-specific differences in evasive behaviour will increase the overall unpredictability experienced by predators within a predator-prey community. Evolutionary, escape-tactic diversity would be driven by the enhanced predator protection for each prey individual in the community. However, escape-tactic diversity could also be a functional consequence of morphological differences that correlate with evasive capabilities. 2. Echolocating bats and eared moths are a textbook example of predator-prey interactions. Moths exhibit evasive flight with diverse tactics; however, the variability of their evasive flight within and between species and individuals has never been quantified systematically. In addition, moth species show variation in size, which correlates with their flight capability. 3. We recorded flight strength during tethered flight of eight sympatric moth species in response to the same level of simulated bat predation. Our method allowed us to record kinematic parameters that are correlated with evasive flight in a controlled way to investigate species-specific differences in escape tactics. 4. We show species-specific and size-independent differences in both overall flight strength and change of flight strength over time, supporting the escape-tactic diversity hypothesis for eared moths. Additionally, we show strong inter-individual differences in evasive flight within some species. This diversity in escape tactic between eared moths increases the overall unpredictability of evasive flight experienced by bat predators, likely providing increased protection against predatory bats for the single individual

All data (bat activity) for Lewanzik et al 2019, J Anim Ecol

All data for Lewanzik et al 2019, J Anim Ecol, consisting of bat activity as a function of several predictors in a field playback study. All details are in the article

Data from: Insectivorous bats integrate social information about species identity, conspecific activity, and prey abundance to estimate cost-benefit ratio of interactions

Animals can use inadvertent social information to improve fitness‐relevant decisions, for instance about where to forage or with whom to interact. Since bats emit high‐amplitude species‐specific echolocation calls when flying, they provide a constant flow of inadvertent social information to others who can decode that acoustic information. Of particular interest is the rate of feeding buzzes – characteristic call sequences preceding any prey capture – which correlates with insect abundance. Previous studies investigating eavesdropping in bats yielded very different and in part contradictory results likely because they commonly focused on single species only, differed substantially in playback buzz rate, and did usually not account for (baseline) conspecific activity. Our goal was to overcome these limitations and systematically test which inadvertent social information bats integrate when eavesdropping on others and how this integration affects space‐use and both intra‐ and interspecific interactions, respectively. We used a community‐wide approach and investigated the effects of a broad range of playback feeding buzz rates and conspecific activity on eavesdropping responses in 24 bat species combinations in the wild. For the first time, we reveal that finely graded and density‐dependent eavesdropping responses are not limited to particular foraging styles or call types, but instead are ubiquitous among insectivorous bats. All bats integrated social information about calling species identity, prey abundance, and conspecific activity to estimate the cost‐benefit ratio of prospective interactions, yet in a species‐specific manner. The effect of buzz rate was multifaceted, as bats responded differently to different buzz rates and responses were additionally modulated by heterospecific recognition. Conspecific activity, in contrast, had a negative effect on the eavesdropping responses of all bats. These findings can explain the inconsistent results of previous studies and advance our understanding of the complex nature of con‐ and heterospecific interactions within bat communities. A comprehensive understanding of how bats incorporate social information into their decision‐making will help researchers to explain species distribution patterns and eventually to unravel mechanisms of species coexistence