Precise Doppler shift compensation in the hipposiderid bat, Hipposideros armiger

Abstract Bats of the Rhinolophidae and Hipposideridae families, and Pteronotus parnellii, compensate for Doppler shifts generated by their own flight movement. They adjust their call frequency such that the frequency of echoes coming from ahead fall in a specialized frequency range of the hearing system, the auditory fovea, to evaluate amplitude and frequency modulations in echoes from fluttering prey. Some studies in hipposiderids have suggested a less sophisticated or incomplete Doppler shift compensation. To investigate the precision of Doppler shift compensation in Hipposideros armiger, we recorded the echolocation and flight behaviour of bats flying to a grid, reconstructed the flight path, measured the flight speed, calculated the echo frequency, and compared it with the resting frequency prior to each flight. Within each flight, the average echo frequency was kept constant with a standard deviation of 110 Hz, independent of the flight speed. The resting and reference frequency were coupled with an offset of 80 Hz; however, they varied slightly from flight to flight. The precision of Doppler shift compensation and the offset were similar to that seen in Rhinolophidae and P. parnellii. The described frequency variations may explain why it has been assumed that Doppler shift compensation in hipposiderids is incomplete

The resting frequency of echolocation signals changes with body temperature in the hipposiderid bat Hipposideros armiger

Doppler shift (DS) compensating bats adjust in flight the second harmonic of the constant-frequency component (CF(2)) of their echolocation signals so that the frequency of the Doppler-shifted echoes returning from ahead is kept constant with high precision (0.1–0.2%) at the so-called reference frequency (f(ref)). This feedback adjustment is mediated by an audio–vocal control system that correlates with a maximal activation of the foveal resonance area in the cochlea. Stationary bats adjust the average CF(2) with similar precision at the resting frequency (f(rest)), which is slightly below the f(ref). Over a range of time periods (from minutes up to years), variations of the coupled f(ref) and f(rest) have been observed, and were attributed to age, social influences and behavioural situations in rhinolophids and hipposiderids, and to body temperature effects and flight activity in Pteronotus parnellii. We assume that, for all DS-compensating bats, a change in body temperature has a strong effect on the activation state of the foveal resonance area in the cochlea, which leads to a concomitant change in emission frequency. We tested our hypothesis in a hipposiderid bat, Hipposideros armiger, and measured how the circadian variation of body temperature at activation phases affected f(rest). With a miniature temperature logger, we recorded the skin temperature on the back of the bats simultaneously with echolocation signals produced. During warm-up from torpor, strong temperature increases were accompanied by an increase in f(rest), of up to 1.44 kHz. We discuss the implications of our results for the organization and function of the audio–vocal control systems of all DS-compensating bats

Transmitter and receiver of the low frequency horseshoe bat Rhinolophus paradoxolophus are functionally matched for fluttering target detection

Flutter-detecting foragers require specific adaptations of the transmitter and the receiver of their echolocation systems to detect and evaluate flutter information in the echoes of potential prey. These adaptations include Doppler shift compensation (DSC), which keeps the echo frequency from targets ahead constant at a reference frequency (f(ref)), and an auditory fovea in the cochlea, which results in foveal areas in the hearing system with many sharply tuned neurons with best frequencies near f(ref). So far, this functional match has been verified only for a very few key species, but is postulated for all flutter-detecting foragers. In this study we determined both, the transmitter and receiver properties within individuals of the Bourret’s horseshoe bat (Rhinolophus paradoxolophus), an allometric outlier in the rhinolophid family. Here we show that the transmitter and receiver are functionally matched in a similar way as postulated for all flutter-detecting foragers. The performance of DSC, measured as the ability to keep the echo frequency constant at f(ref), had a precision similar to that found in other flutter-detecting foragers, and the audiogram showed the characteristic course with a minimum at f(ref). Furthermore, we show for a rhinolophid bat a variation over time of the coupled resting frequency and f(ref). Finally, we discuss the tight match between transmitter and receiver properties, which is guaranteed by the link between the foveal areas of the receiver and the audio–vocal control system for DSC. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1007/s00359-022-01571-0

Distress Calls of a Fast-Flying Bat (Molossus molossus) Provoke Inspection Flights but Not Cooperative Mobbing.

Many birds and mammals produce distress calls when captured. Bats often approach speakers playing conspecific distress calls, which has led to the hypothesis that bat distress calls promote cooperative mobbing. An alternative explanation is that approaching bats are selfishly assessing predation risk. Previous playback studies on bat distress calls involved species with highly maneuverable flight, capable of making close passes and tight circles around speakers, which can look like mobbing. We broadcast distress calls recorded from the velvety free-tailed bat, Molossus molossus, a fast-flying aerial-hawker with relatively poor maneuverability. Based on their flight behavior, we predicted that, in response to distress call playbacks, M. molossus would make individual passing inspection flights but would not approach in groups or approach within a meter of the distress call source. By recording responses via ultrasonic recording and infrared video, we found that M. molossus, and to a lesser extent Saccopteryx bilineata, made more flight passes during distress call playbacks compared to noise. However, only the more maneuverable S. bilineata made close approaches to the speaker, and we found no evidence of mobbing in groups. Instead, our findings are consistent with the hypothesis that single bats approached distress calls simply to investigate the situation. These results suggest that approaches by bats to distress calls should not suffice as clear evidence for mobbing

Distributions of <i>Molossus molossus</i> responsiveness.

<p>Frequency histograms of responsiveness during playback sequences that had passes of <i>M</i>. <i>molossus</i> (n = 116). Increases in activity are to the right of the solid line.</p

Distress calls and pink noise stimuli.

<p>Spectrograms (500 kHz sampling rate, 16 bit resolution, 1024 FFT, Blackman window) of a sequence of <i>Molossus molossus</i> distress calls (A) and pink noise controls (B) with averaged power spectrum of the third pink noise stimulus. Each 2-min playback sequence (C) begins with a 1-min silent period followed by a 1-min playback period with either distress calls (A boxes) or pink noise bursts (B boxes) repeated three times and spaced apart by 10 s of silence.</p

Variation of distress calls of <i>Molossus molossus</i>.

<p>Spectrograms (FFT 1024, Blackman, auto padding, dynamic range of 90 dB) of distress calls playbacks with averaged power spectrum (aside) and waveform (below). Distress calls structures included multiharmonic shallowly modulated calls (A), calls with sideband modulations (B, C), and some calls with nonlinear phenomena (D). Sideband modulations of the distress call shown in C are depicted in E (FFT 2048).</p

<i>Molossus molossus</i> activity and responsiveness to distress call playback near roosts over time.

<p>Mean number of passes (and standard errors) during the 2-min playback sequences recorded on four evenings from 1838 to 2020 h. Data are pooled in 8-min time bins (2–6 counts per bin). Counts do not include observations of zero passes. Blue line shows the total number of <i>M</i>. <i>molossus</i> passes during both distress call and noise playbacks. Red line shows the responsiveness (number of passes during the 1-min playback period minus 1-min silent period) during distress call playbacks.</p

Number of playback sequence leading to more or fewer passes.

<p>Number of playback sequence leading to more or fewer passes.</p

Effect of playback treatment on bat activity.

<p>The mean responsiveness (number of passes during playback period–silent period) is shown for <i>M</i>. <i>molossus</i> (blue squares) and <i>S</i>. <i>bilineata</i> (red circles) in response to either <i>M</i>. <i>molossus</i> distress calls or pink noise. Errors bars show standard error of the mean.</p