Doppler shift compensation performance in Hipposideros pratti across experimental paradigms

A central aim of neuroethological research is to discover the mechanisms of natural behaviors in controlled laboratory studies. This goal, however, comes with challenges, namely the selection of experimental paradigms that allow full expression of natural behaviors. Here, we explore this problem in echolocating bats that evolved Doppler shift compensation (DSC) of sonar vocalizations to yield close matching between echo frequency and hearing sensitivity. We ask if behavioral tasks influence the precision of DSC in Pratt’s roundleaf bat, Hipposideros pratti, in three classic laboratory paradigms evoking audio-vocal adjustments: Stationary bats listening to echo playbacks, bats transported on a moving pendulum, and bats flying freely. We found that experimental conditions had a strong influence on the expression of the audiovocal frequency adjustments in bats. H. pratti exhibited robust DSC in both free-flying and moving-pendulum experiments but did not exhibit consistent audiovocal adjustments in echo playback experiments. H. pratti featured a maximum compensation magnitude of 87% and a compensation precision of 0.27% in the free flight experiment. Interestingly, in the moving pendulum experiment H. pratti displayed surprisingly high-precision DSC, with an 84% maximum compensation magnitude and a 0.27% compensation precision. Such DSC performance places H. pratti among the bat species exhibiting the most precise audio-vocal control of echo frequency. These data support the emerging view that Hipposiderid bats have a high-precision DSC system and highlight the importance of selecting experimental paradigms that yield the expression of robust natural behaviors.

[1]  C. Moss,et al.  Sensory error drives fine motor adjustment , 2022, Proceedings of the National Academy of Sciences of the United States of America.

[2]  Julio C. Hechavarría,et al.  The frugivorous bat Carollia perspicillata dynamically changes echolocation parameters in response to acoustic playback , 2021, Journal of Experimental Biology.

[3]  Y. Yovel,et al.  Echolocating bats can adjust sensory acquisition based on internal cues , 2020, BMC biology.

[4]  Jinhong Luo,et al.  Echolocating bats exhibit differential amplitude compensation for noise interference at a sub-call level , 2020, Journal of Experimental Biology.

[5]  Tinglei Jiang,et al.  Performance of Doppler shift compensation in bats varies with species rather than with environmental clutter , 2019, Animal Behaviour.

[6]  Torbjørn V. Ness,et al.  Neural timing of stimulus events with microsecond precision , 2018, PLoS biology.

[7]  A. Grinnell.  Early milestones in the understanding of echolocation in bats , 2018, Journal of Comparative Physiology A.

[8]  H. Schnitzler,et al.  Precise Doppler shift compensation in the hipposiderid bat, Hipposideros armiger , 2018, Scientific Reports.

[9]  Ninad B Kothari,et al.  Dynamic representation of 3D auditory space in the midbrain of the free-flying echolocating bat , 2017, eLife.

[10]  Cynthia F Moss,et al.  Echolocating bats rely on audiovocal feedback to adapt sonar signal design , 2017, Proceedings of the National Academy of Sciences.

[11]  Jinhong Luo,et al.  Sensorimotor integration on a rapid time scale , 2017, Proceedings of the National Academy of Sciences.

[12]  E. Mora,et al.  Behavioral and Physiological Bases for Doppler Shift Compensation by Echolocating Bats , 2016 .

[13]  A. Grinnell,et al.  Bat Bioacoustics , 2016, Springer Handbook of Auditory Research.

[14]  G. Bloch,et al.  Animal clocks: when science meets nature , 2013, Proceedings of the Royal Society B: Biological Sciences.

[15]  C. Moss,et al.  Adaptive vocal behavior drives perception by echolocation in bats , 2011, Current Opinion in Neurobiology.

[16]  H. Schnitzler,et al.  Auditory fovea and Doppler shift compensation: adaptations for flutter detection in echolocating bats using CF-FM signals , 2011, Journal of Comparative Physiology A.

[17]  Rebecca M. Calisi,et al.  Lab and field experiments: Are they the same animal? , 2009, Hormones and Behavior.

[18]  Lasse Jakobsen,et al.  Echolocating bats emit a highly directional sonar sound beam in the field , 2008, Proceedings of the Royal Society B: Biological Sciences.

[19]  Hiroshi Riquimaroux,et al.  On-board telemetry of emitted sounds from free-flying bats: compensation for velocity and distance stabilizes echo frequency and amplitude , 2008, Journal of Comparative Physiology A.

[20]  M. Smotherman,et al.  Doppler-shift compensation behavior by Wagner's mustached bat, Pteronotus personatus. , 2008, The Journal of the Acoustical Society of America.

[21]  E. Kalko,et al.  Echolocating Bats Cry Out Loud to Detect Their Prey , 2008, PloS one.

[22]  G. Schuller.  Influence of echolocation pulse rate on Doppler shift compensation control system in the greater horseshoe bat , 1986, Journal of Comparative Physiology A.

[23]  G. Schuller.  The role of overlap of echo with outgoing echolocation sound in the batRhinolophus ferrumequinum , 1974, Naturwissenschaften.

[24]  H. Schnitzler,et al.  Control of doppler shift compensation in the greater horseshoe bat,Rhinolophus ferrumequinum , 1973, Journal of comparative physiology.

[25]  H. Schnitzler,et al.  Die Ultraschall-Ortungslaute der Hufeisen-Fledermäuse (Chiroptera-Rhinolophidae) in verschiedenen Orientierungssituationen , 1968, Zeitschrift für vergleichende Physiologie.

[26]  R. Suthers,et al.  Echolocation of moving targets by the fish-catching bat,Noctilio leporinus , 2004, Journal of Comparative Physiology A.

[27]  G. Neuweiler,et al.  Foraging behavior and Doppler shift compensation in echolocating hipposiderid bats,Hipposideros bicolor andHipposideros speoris , 2004, Journal of Comparative Physiology A.

[28]  G. Schuller.  Hearing characteristics and doppler shift compensation in South Indian CF-FM bats , 2004, Journal of comparative physiology.

[29]  W. Metzner,et al.  Effects of echo intensity on Doppler-shift compensation behavior in horseshoe bats. , 2003, Journal of neurophysiology.

[30]  C. Moss,et al.  Echolocation in bats and dolphins , 2003 .

[31]  C. Moss,et al.  Echolocation behavior of big brown bats, Eptesicus fuscus, in the field and the laboratory. , 2000, The Journal of the Acoustical Society of America.

[32]  G Jones,et al.  Echolocation behaviour and prey-capture success in foraging bats: laboratory and field experiments on Myotis daubentonii. , 1999, The Journal of experimental biology.

[33]  G. Schuller,et al.  Binaural influences on Doppler shift compensation of the horseshoe bat Rhinolophus rouxi , 1999, Journal of Comparative Physiology A.

[34]  R. Fay,et al.  Hearing by Bats , 1995, Springer Handbook of Auditory Research.

[35]  O W Henson,et al.  Doppler-shift compensation by the mustached bat: quantitative data. , 1994, The Journal of experimental biology.

[36]  O. Henson,et al.  Ultrasonic vocalizations of flying bats monitored by radiotelemetry. , 1992, The Journal of experimental biology.

[37]  N Suga,et al.  Biosonar behavior of mustached bats swung on a pendulum prior to cortical ablation. , 1990, Journal of neurophysiology.

[38]  D. Griffin.  Listening in the dark: The acoustic orientation of bats and men. , 1958 .

[39]  Robert Galambos,et al.  The sensory basis of obstacle avoidance by flying bats , 1941 .