The flowering of plant bioacoustics: how and why

Gagliano, Monica

doi:10.1093/beheco/art021

Trees are sanctuaries. Whoever knows how to speak to them, whoever knows how to listen to them, can learn the truth. They do not preach learning and precepts, they preach undeterred by particulars, the ancient law of life.
An excerpt from “Wanderings” by Hermann Hesse (1877–1962)

The ability of plants to respond to sound waves or vibrations in their environment is more widespread than we think, and numerous species have evolved a range of adaptive strategies to exploit sound (Gagliano 2012). For example, some 20000 species use buzz pollination where the pollen is released from flowers only when they are vibrated at the correct sound frequency, a feat achieved by bees that have coevolved to vibrate their flight muscles appropriately (Proctor et al. 1996). Moreover, preliminary investigations of both emission and detection of sound by plants indicate that plants have the ability to detect acoustic vibrations and exhibit frequency-selective sensitivity (i.e., plants respond to the same range of frequencies that they emit themselves) that, in turn, generates behavioral modifications (Gagliano, Mancuso, et al. 2012). Hence, the relevant question here is not about whether plants have evolved to detect and respond to sound waves or vibrations in their environment, but how and why they do it.

In considering these issues, Bailey et al. (2013) emphasized the exciting opportunity of applying to plants the well-known “four questions” approach proposed by Tinbergen (1963) for the understanding of the behavior of animals. Two of Tinbergen’s questions are about the mechanisms within an animal (or in this case, a plant) that are responsible for the behavior, whereas the other 2 questions are about the potential adaptive value and evolutionary history of the behavior. Obviously, I totally agree that to begin the exploration of acoustic communication in plants, it is necessary to examine sound in plants at the proximate level. The mechanisms underlying acoustic emission and reception can be characterized through the assessment of sensitivity of plants to sound frequencies based on emission and detection ranges and thresholds. Then, it is possible to investigate the ecological role of such acoustic emissions by determining the information content of the sounds emitted by different plant species and transmitted to other plants (and organisms). As pointed out by both Bailey et al. (2013) and ten Cate (2013), playback experiments examining plant responses to the sounds plant themselves produce is one good way to go about this. In animal ecology, playback is a widely used experimental technique in which natural or synthetic acoustic stimuli are broadcasted and the response of individuals noted. To apply this technique to plants, a setup in which a response is induced by the playback alone and not confounded by any other environmental conditions is required. Gagliano, Renton, et al. (2012) recently developed an experimental box designed to block signals plants normally exchange via contact, chemicals, and light. Using this setup, they demonstrated that plants sense their neighbors and identify their relatives via alternative mechanism(s) to recognized plant communication pathways. Specifically, they proposed acoustic signalling as a putative mechanism underlying the effects they observed. By creating different levels of interactions using a experimental box as described in Gagliano, Renton, et al. (2012) or similar setups together with plant recordings, it is already possible to quantify the responses of a focal plant species when exposed to intra- or interspecific individuals (e.g., a known competitor plant species or an herbivorous insect) versus its acoustic signature (e.g., substituting the actual competitor plant with a recoding of it or the real-life herbivorous insect with the recorded sound of it).

By conceptually linking all our empirical findings into a “road map,” we can ultimately focus on why acoustic communication has evolved in plants, hence elucidating its ecological role (functionality), adaptive significance (fitness consequences), and evolutionary history.

Lastly, it truly is a delight to see the positive attitude, and open-mindedness modern behavioral ecologists are capable of revealing toward a nascent field of research such as “plant bioacoustics.” This is clearly demonstrated by the encouraging comments my review Gagliano (2012) has attracted from leading researchers with an active interest in sensory ecology, and particularly acoustic communication, and the evolution of behavior (Bailey et al. 2013; ten Cate 2013; Cocroft and Appel 2013; Simpson 2013). Their approach deserves to be acknowledged, applauded, and encouraged for 2 main reasons. Firstly, it is a sign that modern behavioral ecology, a discipline primarily focused on the study of animal behavior, has matured beyond the de facto exclusion of plants from the “behaving” realm and moved toward a unified view of the fundamental principles in the evolution of behavior. Secondly and more generally, it demonstrates that scientists can indeed defy the traditional reluctance of new ideas (Kuhn 1962) and instead, welcome them as newborn babes whose full expression can only be revealed by time.