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. 2016 Jun 28;113(26):7261-5.
doi: 10.1073/pnas.1601624113. Epub 2016 May 31.

Mechanosensory hairs in bumblebees (Bombus terrestris) detect weak electric fields

Gregory P Sutton  1 , Dominic Clarke  2 , Erica L Morley  2 , Daniel Robert  2
Affiliations

Mechanosensory hairs in bumblebees (Bombus terrestris) detect weak electric fields

Gregory P Sutton et al. Proc Natl Acad Sci U S A. .

Abstract

Bumblebees (Bombus terrestris) use information from surrounding electric fields to make foraging decisions. Electroreception in air, a nonconductive medium, is a recently discovered sensory capacity of insects, yet the sensory mechanisms remain elusive. Here, we investigate two putative electric field sensors: antennae and mechanosensory hairs. Examining their mechanical and neural response, we show that electric fields cause deflections in both antennae and hairs. Hairs respond with a greater median velocity, displacement, and angular displacement than antennae. Extracellular recordings from the antennae do not show any electrophysiological correlates to these mechanical deflections. In contrast, hair deflections in response to an electric field elicited neural activity. Mechanical deflections of both hairs and antennae increase with the electric charge carried by the bumblebee. From this evidence, we conclude that sensory hairs are a site of electroreception in the bumblebee.

Keywords: bees; behavior; electric fields; sensory biology.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1.
Fig. 1.
Bumblebee covered in body hairs. The white circle containing a plus (+) denotes electrode insertion points in the antennae. The white circle containing a cross (x) denotes approximate electrode insertion points for hair recordings. White arrows show the laser focal position for hair and antennae LDV recordings.
Fig. S1.
Fig. S1.
Laser vibrometry setup for measuring mechanical response. AC and DC voltages were applied to a brass disk 1 cm away from the bee. An LDV then recorded the motion antennae or hairs in reaction to the voltages on the disk.
Fig. S2.
Fig. S2.
Extracellular neurophysiological recordings of the antennae in response to 140 Hz AC electric fields and lavender-scented air puffs. (A) Response to scented air puff. (B) Response to charged oscillating ball (Top). Large spikes are the result of dropped samples (see Inset; dashed black line is the scent stimulus and the solid black line is the electrical stimulus). The large spikes seen in the recording are due to sampling errors and are not neural activity). Response to charged oscillating ball and scented air puff (Bottom). (C) Response to steel disk at 20 V (Top). Response to the disk and a scented air puff (Bottom). (D) Response to a shielded electrode at 400 V (Top). Response to the electrode and a scented air puff (Bottom). Solid black lines indicated the electrical stimulus. Dashed black lines show the scented air-puff stimulus. The antennae reliably responded to scents and mechanical stimuli. In no case did the antenna respond to electric field stimuli.
Fig. S3.
Fig. S3.
Motion of a bumblebee hair (A) and antenna (B) measured by laser Doppler vibrometry in response to an AC voltage sweep (400 V sine wave). (A) Displacement (Top) and phase response (Bottom) of a hair. Colors correspond to measurement points along the antenna (Inset). (B) Displacement (Top) and phase response (Bottom) of an antenna. Colors correspond to measurement points along the antenna (Inset).
Fig. 2.
Fig. 2.
Antenna (blue) and hair (red) motion in response to 10 Hz–10 kHz electrical chirps. Rows show the velocity (A), displacement (B), and angular displacement (C). Columns show the response at each frequency (Left), the amplitude of maximum response (Middle), and the median response amplitude across all frequencies (Right). Insets show a representation of the quantity being measured.
Fig. 3.
Fig. 3.
Antenna (blue) and hair (red) mean velocity in response to oscillating electric fields at the resonant frequency of each structure (Left) and at the frequency of median response (Right) under charged (Top) and uncharged (Bottom) preparations. Gray dots show SEM. Filled shapes denote responses that were significantly larger than thermal noise. Unfilled shapes denote responses statistically indistinguishable from thermal noise.
Fig. 4.
Fig. 4.
(A) A finite element model of a bumblebee hair under an electric field produced by a steel disk 1 cm away. Electric field values are given per positive volt on the disk. (Inset) The resultant projected force on the hair (0.12 µN/V). (B) The simulated electric field due to the disk at 25 mV (Left) and 500 mV (Right), the minimum voltages which caused observable motion in the hairs and antennae, respectively. The white x shows the position at which the hairs and antennae were located in the LDV experiments.
Fig. 5.
Fig. 5.
A finite element model of the stimulus delivery system showing electric field strength as a function of axial distance from 30-mm steel disk held at 30 V. The labeled points show the maximum distance of detection calculated for hairs (red) and antennae (blue) for resonant stimuli (circles) and nonresonant stimuli (squares). The bars on each axis represent the range of values of electric field and distance at which these structures show a mechanical response. The lighter area shows the difference between at-resonant and off-resonant stimulation, showing the responses within this range depend on frequency. The dark colored areas of the bars show the range at which the structures respond at all frequencies.
Fig. 6.
Fig. 6.
The electrophysiological response to an electric field. (A and B) Example response of an antenna (blue) and a hair (red) to an electric field. (C) Plot showing the observed changes in firing rate of 12 antennae (blue) and 12 hairs (red) to an electric field stimulus (applied during the gray box). The value shown is the number of spikes per second, per bee, divided by the mean prestimulus spike rate. A value of 1 (dashed black line) indicates no change in spike rate. (D and E) Two control stimuli applied to the antenna: Puffs of unscented air (D) and a puff of scented air (E) demonstrate the lack of response of the antenna seen in A is not due to damage during the dissection.
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