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Bumblebee electric charge stimulates floral volatile emissions in Petunia integrifolia but not in Antirrhinum majus - PubMed

  • ️Fri Jan 01 2021

Bumblebee electric charge stimulates floral volatile emissions in Petunia integrifolia but not in Antirrhinum majus

Clara Montgomery et al. Naturwissenschaften. 2021.

Abstract

The timing of volatile organic compound (VOC) emission by flowering plants often coincides with pollinator foraging activity. Volatile emission is often considered to be paced by environmental variables, such as light intensity, and/or by circadian rhythmicity. The question arises as to what extent pollinators themselves provide information about their presence, in keeping with their long co-evolution with flowering plants. Bumblebees are electrically charged and provide electrical stimulation when visiting plants, as measured via the depolarisation of electric potential in the stem of flowers. Here we test the hypothesis that the electric charge of foraging bumblebees increases the floral volatile emissions of bee pollinated plants. We investigate the change in VOC emissions of two bee-pollinated plants (Petunia integrifolia and Antirrhinum majus) exposed to the electric charge typical of foraging bumblebees. P. integrifolia slightly increases its emissions of a behaviorally and physiologically active compound in response to visits by foraging bumblebees, presenting on average 121 pC of electric charge. We show that for P. integrifolia, strong electrical stimulation (600-700 pC) promotes increased volatile emissions, but this is not found when using weaker electrical charges more representative of flying pollinators (100 pC). Floral volatile emissions of A. majus were not affected by either strong (600-700 pC) or weak electric charges (100 pC). This study opens a new area of research whereby the electrical charge of flying insects may provide information to plants on the presence and phenology of their pollinators. As a form of electroreception, this sensory process would bear adaptive value, enabling plants to better ensure that their attractive chemical messages are released when a potential recipient is present.

Keywords: Plant,; Pollination,; Scent,; Signaling,; Triboelectricity.

© 2021. The Author(s).

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Conflict of interest statement

The authors declare no competing interests.

Figures

Fig. 1
Fig. 1

Testing P. integrifolia volatile emission in response to visitation by electrically charged pollinators (Bombus terrestris). a Experimental set up allowing bees to visit one P. integrifolia flower whilst the other acts as a control. The bee accesses the flower by flying through a metal ring in the floor of the arena. The charge on the bee induces a current in the ring, measured by a picoammeter (pA) connected to a computer via a data acquisition unit (DAQ). The volatiles are collected via air entrainment. b Distribution of electric charges of bumblebees approaching the P. integrifolia flowers throughout the experiment. Boxplot shows mean (X), median, SD, interquartile range, and outliers. Areas shown by grey zones encompass all values <-400 pC and >800 pC (range = 1041 pC to -832 pC, N = 377). c Quantitative measure of benzaldehyde emitted by the P. integrifolia flowers before (blue boxes) and during (red boxes) bee foraging, showing emissions of flowers visited by bees (left) and flowers touched with a grounded rod as a mechanical control (right), N = 12. Significance levels: ns not significant, * P < 0.05

Fig. 2
Fig. 2

a Electrical stimulation with a triboelectrically charged nylon ball of 600–700 pC causes significant increase in benzaldehyde emissions from P. integrifolia flowers, whilst grounded rod does not (N = 15). b A nylon ball charged to <100 pC causes a significant increase in benzaldehyde emissions, but plants touched with the grounded control also showed a significant increase in emissions (N = 12). Significance levels: ns not significant, *** P < 0.001

Fig. 3
Fig. 3

Behavioural and electrophysiological response of bumblebees to benzaldehyde. a PER responses of bumblebees to benzaldehyde. Trials 1-10 are training trials associating benzaldehyde scent with a sucrose reward. Trials 11-13 are control trials using unscented air. Trial 14 is a final confirmation trial. Data from 15 animals. b GC-EAG response of bumblebee antenna to benzaldehyde [Kováts retention index (KI) on a non-polar HP-1 GC column=943] present in a volatile sample taken from a P. integrifolia flower. Top trace represents GC/FID output with the large peak showing benzaldehyde. Red arrow on bottom trace indicates EAG response from a bumblebee antenna to the benzaldehyde peak

Fig. 4
Fig. 4

a The GC-EAG response of a bumblebee antenna to compounds present in A. majus MTP flower headspace extracts, showing FID peaks for myrcene (myr, KI=990), (E)-ocimene (oci, KI=1043), methyl benzoate (met, KI=1064) and 3,5-dimethoxytoluene (dim, KI=1246). Bottom trace shows EAG responses of a bumblebee antenna to (E)-ocimene, methyl benzoate and 3,5-dimethoxytoluene (red arrows), but no reaction is found for myrcene (blue arrow). b and c EAG-active floral volatiles produced by A. majus MTP when touched with a charged or grounded stimulus (N = 14). The charged stimulus was a nylon ball charged to 600-700 pC (b) and <100 pC (c). Significance levels: ns not significant

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