Effects of Sound Perception in Plants: Comparison
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Plants have long been considered passive, static, and unchanging organisms, but this view is finally changing. More and more knowledge is showing that plants are aware of their surroundings, and they respond to a surprising variety of stimuli by modifying their growth and development. Plants extensively communicate with the world around them, above and below ground. Although communication through mycorrhizal networks and Volatile Organic Compounds has been known for a long time, acoustic perception and communication are somehow a final frontier of research. Perhaps surprisingly, plants not only respond to sound, they actually seem to emit sound as well. Roots emit audible clicks during growth, and sounds are emitted from xylem vessels, although the nature of these acoustic emissions still needs to be clarified. Even more interesting, there is the possibility that these sounds carry information with ecological implications, such as alerting insects of the hydration state of a possible host plant, and technological implications as well. Monitoring sound emissions could possibly allow careful monitoring of the hydration state of crops, which could mean significantly less water used during irrigation. 

  • plant
  • sound
  • buzz pollination
  • plant acoustics
  • plant communication

1. Introduction

Human conversation typically has an intensity of approximately 60 dB, and at this intensity, it can elicit vibrations, for example, in hearing organs, of just 10–50 nm. At these scales, the mechanical energy imparted by the vibrations is exceedingly small, and yet we have no problems hearing during conversation. Considering this, it really is reasonable to think that something as small as a trichome could vibrate in response to SVs and possibly convey information [28][1].
In much the same way plants have adapted to different pollinators, plants have adapted to different sounds in their environments. For example, flower morphology affects the efficiency of pollinators, affects the way pollinators visit flowers and the success of pollen import and export [29][2]. Similarly, the carnivorous pitcher plant Nepenthes hemsleyana could possibly have evolved pitchers that reflect the echolocation of bats. The plant N. hemsleyana has a mutualistic interaction with bats, supplying a safe, parasite-free roosting spot, and the bats in return fertilize the plant with nitrogen-rich droppings, enhancing the nitrogen uptake of these plants by an average of 34% [30][3].

2. Buzz Pollination

Insects, primarily Hymenoptera [31][4], use vibrations to extract pollen from a wide variety of flower morphologies with poricidal anthers, that is, anthers where the pollen exits the anther through an apical pore or slit. This phenomenon is known as buzz pollination. In poricidal anthers, the pollen is not freely accessible, and its removal requires vibration. As many as 8–10% of angiosperms possess poricidal anthers that are pollinated through the use of vibrations. Interestingly, buzz pollination seems to have arisen independently several times in about 65 plant families [32][5]. Buzz pollination is not limited to a specific flower morphology, although it seems that the Solanum type flower has evolved specifically in response to sonicating bees. Flowers with poricidal anthers are visited by many insects, even non-sonicating insects that chew through the anthers to reach the pollen, but the primary visitors are sonicating bees [31][4].
Sonication seems to have arisen in a common ancestor of bees during the early Cretaceous [32][5]. A bee lands on a flower and curls with the ventral side of the body around the anthers in a C shape, with the wings tightly folded back over the abdomen during sonication [31,33][4][6]. The bee then rapidly contracts the thoracic muscles while preventing the wings from beating. The vibrations are transmitted to the anthers, which resonate, transmitting energy to the pollen, which is then expelled through the apical aperture [31][4]. Centrifugal forces are generated, which eject the pollen [34][7].
There are both insect-related and plant-related variables that affect buzz pollination. Vibrations produced by sonicating bees can be characterized by duration, amplitude, and frequency. It was found that the greatest effect on pollen removal from anthers was given by duration and amplitude, while frequency had only a weak effect on pollen removal. Moreover, heavier bees produced buzzes with greater amplitude, ejecting more pollen [35][8]. The magnitude of the vibration required to eject pollen from the anthers increased with frequency. The vibration frequency determines the time that a force may act on a particle, and therefore higher frequencies require higher amplitudes [34][7].
In terms of duration, bees increased the duration of their buzzing when visiting virgin flowers, and buzzes were shorter when returning to flowers that had already been visited. This could suggest that bees adjust the duration of their buzzing in relation to the pollen content of the flower [31][4]. In theory, if a bee vibrated for a long enough time, it could extract all of the available pollen [34][7].
The frequency of the buzzing is under physical and physiological control rather than behavioral control. This is because the vibrations depend on the muscles of the bee, and therefore there are limits to the frequencies they can achieve. The peak frequency, which refers to the frequency with the greatest relative energy within a buzzing vibration, varies between 100–400 Hz depending on the species of bee. Through harmonic frequencies, which are positive integer multiples of the original peak frequency (sound-standing waves), frequencies as high as 2000 Hz can be reached [31][4], but as stated before, this has very little effect on pollen removal. The optimal peak frequencies do, however, vary among plant species but still remain under 1000 Hz.
Plant traits also affect buzz pollination. Plant structures can either enhance or dampen the amplitude of the vibrations. For example, rigid, multi-layered anthers release more pollen compared with flexible anthers when vibrated. It’s reasonable to think that the size of the apical pore influences the amount of pollen released [31][4].

3. Sweetened Nectar

Yet another example in the realm of pollination is the production of sweeter nectar within as little as three minutes following the perception of sound by flowers of Oenothera drummondii. The flowers of O. drummondii mechanically vibrated in response to recordings of bees and moths flying and also vibrated in response to the flight of a live bee, showing the same increase in nectar sugar content [36][9]. The volume of nectar remained the same, meaning that an increase in sugar concentration was not a result of a drop in water content. The velocities of the oscillations of the flowers that in this experiment caused an increase in sugar concentration in the nectar was found in other experiments to be able to elicit defense responses by plants [36][9]. Interestingly, the vibration of the flowers depended on the presence of petals, as flowers that had their petals removed or flowers covered by glass ceased to show a response to the sound vibrations.

4. Interpreting Relevant and Irrelevant Sounds

These examples show the important ecological role that sound can play in a plant’s life. Plants don’t live isolated from the rest of the world. Instead, there are extensive connections with other plants, animals, and microbes. Around plants, there are rich communities of arthropods, many of which use vibrations to find mates or prey. For example, vibrations caused by the chewing of Plathypena scabra worms caused predatory Podisus maculiventris stinkbugs to begin their search [37][10]. Chewing herbivores produce specific high-amplitude vibrations that travel quickly to other parts of the plant, and this can produce a local and systemic response in other parts of the plant. Arabidopsis thaliana leaves exposed to recordings of caterpillars chewing were proved to be primed for defense [38][11]. The plants that had been exposed to chewing vibrations showed higher levels of glucosinolates and anthocyanins following herbivory, while there was no increase in anthocyanins in the plants that either received no vibrations or received vibrations from recordings of leafhopper singing or recordings of the wind [38][11]. Interestingly, as with the greater amplitude of bee buzzing increasing pollen removal, higher amplitudes induced higher amounts of aliphatic glucosinolates [38][11]. It is still to be understood how the response caused by the vibrations of a herbivore can generate an induced resistance or a systemic resistance (for an in-depth study, see [38][11]). One possibility is that the plant subject to herbivory integrates the vibrational signal with others coming from the herbivore’s attack. As plants perceive warning signals via VOCs from nearby stressed plants, and VOCs can serve as a sort of chemical language in the communication between plants [39][12], also vibrations can be used at least in some cases in plant communication [24,40,41][13][14][15]. This is yet another example of the ecological role that sound can play in a plant’s life. The fact that plants perceive sound from so many different sources and adapt proves them to be ingenuously aware of their environment.

References

  1. Gagliano, M.; Mancuso, S.; Robert, D. Towards understanding plant bioacoustics. Trends Plant Sci. 2012, 17, 323–325.
  2. Liu, C.Q.; Gao, Y.D.; Niu, Y.; Xiong, Y.Z.; Sun, H. Floral adaptations of two lilies: Implications for the evolution and pollination ecology of huge trumpet-shaped flowers. Am. J. Bot. 2019, 106, 622–632.
  3. Schöner, M.G.; Schöner, C.R.; Simon, R.; Grafe, T.U.; Puechmaille, S.J.; Ji, L.L.; Kerth, G. Bats Are Acoustically Attracted to Mutualistic Carnivorous Plants. Curr. Biol. 2015, 25, 1911–1916.
  4. De Luca, P.; Vallejo-Marín, M. What’s the ‘buzz’ about? The ecology and evolutionary significance of buzz-pollination. Curr. Opin. Plant Biol. 2013, 16, 429–435.
  5. Mesquita-Neto, J.; Blüthgen, N.; Schlindwein, C. Flowers with poricidal anthers and their complex interaction networks—Disentangling legitimate pollinators and illegitimate visitors. Funct. Ecol. 2018, 32, 2321–2332.
  6. King, M.J.; Buchmann, S.L. Floral Sonication by Bees: Mesosomal Vibration by Bombus and Xylocopa, but Not Apis (Hymenoptera: Apidae), Ejects Pollen from Poricidal Anthers. J. Kans. Entomol. Soc. 2003, 76, 295–305.
  7. King, M.J.; Buchmann, S.L. Sonication Dispensing of Pollen from Solanum laciniatum Flowers. Funct. Ecol. 1996, 10, 449–456.
  8. De Luca, P.A.; Bussière, L.F.; Souto-Vilaros, D.; Goulson, D.; Mason, A.C.; Vallejo-Marín, M. Variability in bumblebee pollination buzzes affects the quantity of pollen released from flowers. Oecologia 2013, 172, 805–816.
  9. Veits, M.; Khait, I.; Obolski, U.; Zinger, E.; Boonman, A.; Goldshtein, A.; Saban, K.; Seltzer, R.; Ben-Dor, U.; Estlein, P.; et al. Flowers respond to pollinator sound within minutes by increasing nectar sugar concentration. Ecol. Lett. 2019, 22, 1483–1492.
  10. Pfannenstiel, R.S.; Hunt, R.E.; Yeargan, K.V. Orientation of a hemipteran predator to vibrations produced by feeding caterpillars. J. Insect Behav. 1995, 8, 1–9.
  11. Appel, H.M.; Cocroft, R.B. Plants respond to leaf vibrations caused by insect herbivore chewing. Oecologia 2014, 175, 1257–1266.
  12. Guerrieri, E. Who’s listening to talking plants. In Deciphering Chemical Language of Plant Communication; Blande, J.D., Glinwood, R., Eds.; Springer: Basel, Switzerland, 2016; pp. 117–136.
  13. Gagliano, M. Green symphonies: A call for studies on acoustic communication in plants. Behav. Ecol. 2013, 24, 789–796.
  14. Eriksson, A.; Anfora, G.; Lucchi, A.; Virant-Doberlet, M.; Mazzoni, V. Inter-plant vibrational communication in a leafhopper insect. PLoS ONE 2011, 6, e19692.
  15. Gagliano, M.; Renton, M.; Duvdevani, N.; Timmins, M.; Mancuso, S. Acoustic and magnetic communication in plants: Is it possible? Plant Signal. Behav. 2012, 7, 1346–1348.
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