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Research Article

Fast sensory–motor reactions in echolocating bats to sudden changes during the final buzz and prey intercept

Cornelia Geberl, Signe Brinkløv, Lutz Wiegrebe, and Annemarie Surlykke
  1. aDepartment of Biologie II, Division of Neurobiology, Ludwig Maximilians University, 82152 Martinsried, Germany; and
  2. bDepartment of Biology, University of Southern Denmark, 5230 Odense M, Denmark

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PNAS March 31, 2015 112 (13) 4122-4127; first published March 16, 2015; https://doi.org/10.1073/pnas.1424457112
Cornelia Geberl
aDepartment of Biologie II, Division of Neurobiology, Ludwig Maximilians University, 82152 Martinsried, Germany; and
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Signe Brinkløv
bDepartment of Biology, University of Southern Denmark, 5230 Odense M, Denmark
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Lutz Wiegrebe
aDepartment of Biologie II, Division of Neurobiology, Ludwig Maximilians University, 82152 Martinsried, Germany; and
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Annemarie Surlykke
bDepartment of Biology, University of Southern Denmark, 5230 Odense M, Denmark
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  • For correspondence: ams@biology.sdu.dk
  1. Edited by John G. Hildebrand, University of Arizona, Tucson, AZ, and approved February 20, 2015 (received for review December 21, 2014)

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    Fig. 1.

    Experimental setups. The two setups used in the field and laboratory. Echolocation and flight behavior of bats attacking the worm were recorded with a T-shaped four-microphone (Mic) array and high-speed video cameras (Cam) illuminated with infrared lights (IR). (A) Field setup with a mealworm tethered to a nylon thread hanging from a fishing rod with the tip bent by a taut fishing line connected to a lifting solenoid. Activation of the solenoid released the tip to flick upwards, instantaneously removing the worm. The two cameras were mounted with perpendicular optical axes (dashes lines) aimed at the mealworm. (B) Lab setup for trawling trials with a mealworm on a prey remover device in a small pond. In removal trials the worm was pulled below the water surface by a small electromotor.

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    Fig. 2.

    Aerial captures in the field. (A–D) Acoustic behavior (spectrograms) and capture behavior (video snapshots) during prey captures in the field experiment. (A) Control trial without worm removal, (B) late removal, (C) intermediate removal, and (D) early removal relative to expected prey contact. Numbers in spectrograms correspond to the numbers in each of the snapshots Below. Letters denote the different phases of the echolocation sequence. (a) Start of buzz I, (b) end of buzz I/start of buzz II, (c) end of buzz II. Black vertical lines indicate time of prey removal. The earlier the prey is removed, the shorter the capture behavior and the buzz II duration. With early removal (D) the bat does not emit a buzz II and no capture behavior is initiated.

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    Fig. 3.

    Controls trials showing duration of echolocation buzz (buzz I, cyan and buzz II, green) and of the three behavioral capture phases (feet down, yellow-green; curling up, red-brown; and full ball, violet) relative to bat–prey contact (time = 0 ms). (A) Stacked presentation of all control trials for aerial captures in the field. (B) Stacked presentation of all control trials for trawling captures in the laboratory with the worm attached to the prey remover. (C) Summary figure showing median, first, and third quartiles of durations in control trials in the field (top half) and laboratory (bottom half) (n = number of control trials).

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    Fig. 4.

    Prey removal. Effect of removing the prey on echolocation and capture behavior in air in the field (A and B) and over water in the laboratory (C and D). Short black vertical lines indicate the time of removal. (A and C) Timing of buzz I (cyan), buzz II (green), and the three capture behavior phases (feet down, yellow-green; curling up, red-brown; and full ball, violet) relative to expected bat–prey contact for all field removal trials. (B and D) Summary figures showing median, first, and third quartiles of acoustic and capture behavior durations in aerial field removals with trials pooled into 30-ms bins (n = number of trials per bin).

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    Fig. 5.

    Number of buzz II calls and duration of capture behavior. Comparison of the number of buzz II calls (A and B) and the duration of capture behavior (C and D) in removal trials relative to the time of prey removal. Aerial field captures are shown on the Left (A and C) and trawling laboratory captures on the Right (B and D). Data are shown for two bats at two different field sites and three bats in the laboratory as indicated by symbols and colors. A sigmoid function was fitted to each dataset (all bats) for the two parameters: number of buzz II calls and capture behavior duration (blue line). For comparison, the horizontal cyan lines give control values: median number of buzz II calls (Top) and median duration of capture behavior (Bottom) in control trials in air in the field (A and C) and trawling in the laboratory (B and D).

Data supplements

  • Supporting Information

    Files in this Data Supplement:

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    • Download Movie_S01 (MP4) - Example of a prey removal in the laboratory with a trawling Myotis daubentonii. The bat exhibits full capture and echolocation behavior, although the worm is removed early (230 ms) before expected capture. The removal of the worm often created water ripples, which may add to the high variability in acoustic and behavioral reactions in trawling trials. Notably, this trial illustrates that with prey removals, the bats often looked into the tail membrane a second time, seemingly puzzled by the missing catch. The high-speed video was recorded at 300 frames per second and slowed 10 times for playback.
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Function of terminal buzz in echolocating bats
Cornelia Geberl, Signe Brinkløv, Lutz Wiegrebe, Annemarie Surlykke
Proceedings of the National Academy of Sciences Mar 2015, 112 (13) 4122-4127; DOI: 10.1073/pnas.1424457112

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Function of terminal buzz in echolocating bats
Cornelia Geberl, Signe Brinkløv, Lutz Wiegrebe, Annemarie Surlykke
Proceedings of the National Academy of Sciences Mar 2015, 112 (13) 4122-4127; DOI: 10.1073/pnas.1424457112
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Proceedings of the National Academy of Sciences: 112 (13)
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