Evolution of high duty cycle echolocation in bats

Abstract

SummaryDuty cycle describes the relative ʻon timeʼ of a periodic signal. In bats, we argue that high duty cycle (HDC) echolocation was selected for and evolved from low duty cycle (LDC) echolocation because increasing call duty cycle enhanced the ability of echolocating bats to detect, lock onto and track fluttering insects. Most echolocators (most bats and all birds and odontocete cetaceans) use LDC echolocation, separating pulse and echo in time to avoid forward masking. They emit short duration, broadband, downward frequency modulated (FM) signals separated by relatively long periods of silence. In contrast, bats using HDC echolocation emit long duration, narrowband calls dominated by a single constant frequency (CF) separated by relatively short periods of silence. HDC bats separate pulse and echo in frequency by exploiting information contained in Doppler-shifted echoes arising from their movements relative to background objects and their prey. HDC echolocators are particularly sensitive to amplitude and frequency glints generated by the wings of fluttering insects. We hypothesize that narrowband/CF calls produced at high duty cycle, and combined with neurobiological specializations for processing Doppler-shifted echoes, were essential to the evolution of HDC echolocation because they allowed bats to detect, lock onto and track fluttering targets. This advantage was especially important in habitats with dense vegetation that produce overlapping, time-smeared echoes (i.e. background acoustic clutter). We make four specific, testable predictions arising from this hypothesis.Key words: Chiroptera, calling behaviour, signal design, Yinpterochiroptera, Yangochiroptera, flutter detection, Doppler shift compensation. Fig.1A-C). For the purpose of this paper, we define LDC bats as those producing signals with a duration <25% of their signal period during the search phase of echolocation. Most LDC bats produce echolocation calls with their larynx, although a handful of species in the family Pteropodidae use tongue clicks (Griffin et al., 1958;Yovel et al., 2010).HDC bats avoid auditory masking by separating pulse and echo in frequency, allowing them to broadcast calls and receive echoes at the same time (Schuller, 1974;Schuller, 1977). HDC bats take advantage of information contained in Doppler-shifted echoes generated by the relative movements of bat and target, including acoustic glints generated by the wingbeats of fluttering insects. Echolocation calls of HDC bats consist of a long CF component followed by a brief, downward FM sweep. In some species, the initial portion of the call also contains a short, upward FM sweep (Henson et al., 1987; Jones and Rayner, 1989). Narrowband calls of HDC bats are typically multi-harmonic with the highest signal energy in the second acoustic element (Pye and Roberts, 1970;Schnitzler and Denzinger, 2011). HDC bats emit long duration calls (e.g. 10 to >50ms) relative to their call period ( Fig.1D-F). We operationally define HDC bats as those whose signal durations are ≥25% of...

Evolutionary escalation: the bat–moth arms race

“…Ticks indicate superfamilies in which all species are laryngeal echolocators, crosses indicate a lack of laryngeal echolocation. Adapted from Teeling (2009), Fenton and and Fenton et al (2012). mya, million years ago.…”

Blurry topography for precise target-distance computations in the auditory cortex of echolocating bats

“…Even in high duty cycle echolocators such as P. parnellii, during search flight, the interval between FM components of two consecutive biosonar calls is above 30 ms (see example search calls of P. parnellii in ref. 31). This interpulse interval is long enough to accommodate echoes from targets located as far as 5 m from each other, without any interference from echoes from the next emission.…”

Ambient noise causes independent changes in distinct spectro-temporal features of echolocation calls in horseshoe bats

“…The noise-dependent changes in the spectro-temporal composition of echolocation calls, however, could significantly affect the bat's ability to detect and locate targets. Horseshoe bats use the CF component to detect the frequency modulations produced by wing beats of insect prey (reviewed by Schnitzler and Denzinger, 2011;Fenton et al, 2012). In contrast, they use FM components to determine target distance and location (Schnitzler, 1968).…”

“…Nevertheless, only further tests will reveal whether noise-induced changes in echolocation calls indeed affect echolocation performance. Furthermore, it remains to be seen whether noiseinduced spectrotemporal changes in echolocation calls also occur in bats that produce brief FM calls with low repetition rates, so-called low duty cycle echolocators (Fenton et al, 2012), and how it affects their echolocation performance. Preliminary evidence suggests that, at least in free-tailed bats, masking noise may have some effect on echolocation call structure (Tressler and Smotherman, 2009).…”

“…1A). During echolocation, FM portions serve in measuring target distance and location (Schnitzler, 1968), whereas the long CF components enable the bats to detect the rhythmic frequency modulations caused by the wing beats of flying insect prey (reviewed by Schnitzler and Denzinger, 2011;Fenton et al, 2012). During flight, the CF components of the echoes increase as a result of Doppler effects.…”