Flowers respond to pollinator sound within minutes by increasing nectar sugar concentration

Abstract

Can plants sense natural airborne sounds and respond to them rapidly? We show that Oenothera drummondii flowers, exposed to playback sound of a flying bee or to synthetic sound signals at similar frequencies, produce sweeter nectar within 3 min, potentially increasing the chances of cross pollination. We found that the flowers vibrated mechanically in response to these sounds, suggesting a plausible mechanism where the flower serves as an auditory sensory organ. Both the vibration and the nectar response were frequency-specific: the flowers responded and vibrated to pollinator sounds, but not to higher frequency sound. Our results document for the first time that plants can rapidly respond to pollinator sounds in an ecologically relevant way. Potential implications include plant resource allocation, the evolution of flower shape and the evolution of pollinators sound. Finally, our results suggest that plants may be affected by other sounds as well, including anthropogenic ones.

Keywords: Communication; nectar; plant bioacoustics; plant-pollinator interactions; pollination; signalling; vibration.

Figure 1

Flowers respond rapidly to pollinator sounds by producing sweeter nectar (a). Mean sugar concentration under the different treatments in plants grown outdoors (dashed black) and indoors (dotted red). Mean sugar concentration across both indoors and outdoors groups differed significantly (P < 0.01) between flowers exposed to frequencies below 1 kHz (sugar concentration 19.8% ± 0.6, n = 72 and 19.1% ± 0.7, n = 42 for ‘Low’ and ‘Bee’ after 3 min respectively), compared to flowers exposed to ‘Silence’ or ‘High’ frequency sound (16.3% ± 0.5, n = 71, and 16.0% ± 0.4, n = 72 respectively). Insert shows a flower of Oenothera drummondii. (b) Spectra (frequency content) of the playback signals used in the experiment. Both ‘Bee’ and ‘Low’ signals contain most energy below 1000 Hz, while the ‘High’ control peaked at c. 159 000 Hz.

Figure 2

(a) Flowers vibrate mechanically in response to airborne sound of a pollinator. Top: Left – time signal of a honey bee sound signal (airborne signal recorded using a microphone). Right – time signal of a flying Plodia interpunctella male moth (the signal's spectrum peaks at c. 100 Hz, see Fig. S6). Bottom: Mechanical vibration recorded in an Oenothera drummondii flower in response to the playback of the bee (left) and moth (right) sound signals. (b) Vibration velocity in response to the bee signal depended on the presence of petals: a significantly stronger vibration was recorded when all four petals were intact in comparison to when flowers were trimmed and had only 1 or 0.5 petals (paired Wilcoxon, P < 0.0005 for the comparison between four and one petal and P < 0.005 for the comparison between 4 and 0.5 petals). (c) Flowers vibrated in response to playback of low frequencies around 1 kHz (left) while they did not vibrate above background noise to playbacks at higher frequencies of c. 35 kHz (right). Top: the time that the playback was ‘on’. Bottom: Vibration time signals of the flowers. (d) Frequency specificity in both vibration and sugar concentration response. The flowers vibrated (dashed black) significantly more than background noise in response to sound signals in low frequencies around 1 kHz (paired Wilcoxon P < 0.0001, n = 21) but not in response to high frequencies around 160 kHz (P > 0.6, n = 23) or to intermediate frequencies around 35 kHz (P > 0.9, n = 21); The flowers also increased sugar concentration (dotted red line) in response to ‘Low’ signals significantly more than in response to the ‘Intermediate’ signal presented in the inset (P < 0.002), or to the ‘High’ signal serving as control (P < 0.0001). (Sugar concentration 15.9% ± 0.57, n = 81, 12.8% ± 0.7, n = 49, and 12.3% ± 0.77, n = 51, for Low, High and Intermediate respectively). Inset shows the spectrum of the ‘Intermediate’ playback signal used in the nectar experiment. (e) Summary of experimental results. Flowers vibrate in response to airborne sound at pollinator’s frequency range, and increase nectar sugar concentration (right panel). Glass covered flowers do not respond (middle), suggesting that the flower serves as the plant’s ‘ear’. The flowers response is frequency specific, and they do not vibrate or respond to frequencies around 35 kHz (left).