Plant Sensing and Communication

Richard Karban

• Publisher: University of Chicago Press
• Year: 2015
• ISBN:
  9780226264844
• Topic: Biological Sciences
• Subtopic: Science General
• Index: Biological Sciences

The news that a flowering weed—mousear cress ( Arabidopsis thaliana )—can sense the particular chewing noise of its most common caterpillar predator and adjust its chemical defenses in response led to headlines announcing the discovery of the first "hearing" plant. As plants lack central nervous systems (and, indeed, ears), the mechanisms behind this "hearing" are unquestionably very different from those of our own acoustic sense, but the misleading headlines point to an overlooked truth: plants do in fact perceive environmental cues and respond rapidly to them by changing their chemical, morphological, and behavioral traits.In Plant Sensing and Communication, Richard Karban provides the first comprehensive overview of what is known about how plants perceive their environments, communicate those perceptions, and learn. Facing many of the same challenges as animals, plants have developed many similar capabilities: they sense light, chemicals, mechanical stimulation, temperature, electricity, and sound. Moreover, prior experiences have lasting impacts on sensitivity and response to cues; plants, in essence, have memory. Nor are their senses limited to the processes of an individual plant: plants eavesdrop on the cues and behaviors of neighbors and—for example, through flowers and fruits—exchange information with other types of organisms. Far from inanimate organisms limited by their stationary existence, plants, this book makes unquestionably clear, are in constant and lively discourse.

1

Plant Behavior and Communication

1.1 Plants and animals are different but also similar

We all learn intuitively that plants are not like us in many ways. Ask a child about the differences between plants and animals and the answer won’t be about photosynthesis. They’ll say, “Plants can’t move” or “Plants don’t do anything.” It is true that plants don’t appear to do the things that many of us find most interesting about humans and other animals—moving, communicating with one another, and displaying a great diversity of sophisticated behaviors that depend upon the particular situations in which they find themselves. But this intuition about plants is incorrect; plants sense many aspects of their abiotic and biotic environments and respond with a variety of plastic morphologies and behaviors that are often adaptive. In addition, plants communicate, signaling to remote organs within an individual, eavesdropping on neighboring individuals, and exchanging information with other organisms ranging from other plants to microbes to animals.

Plants lack central nervous systems; the mechanisms coordinating plant sensing, behavior, and communication are quite different from the systems that accomplish similar tasks in animals. The challenges that face plants are similar to those facing animals—finding resources, avoiding predators, pathogens, and abiotic stresses, acquiring mates, placing offspring in situations where they are likely to be successful. The modes of selection are also basically similar for plants and animals. As a result, natural selection has led to the evolution of solutions to these challenges that are often analogous. Nonetheless, there are many important differences between plants and animals that have led to very different adaptations, including the behaviors that will be considered in this book.

Although the issues that plants and animals face have similarities, their habits, abilities, and circumstances tend to be different in many ways. Most plants are capable of producing their own food, allowing them to spend much of their lives as factories converting resources (light, water, CO₂) into organic tissues. Since these resources are rapidly renewable, vegetative organs of many plants move relatively short distances and remain rooted in the soil. Higher plants are constructed of repeated modular units (leaves, branches, roots) that are far less specialized than the organs of higher animals (White 1984). Many important processes are carried out by plant organs that are less centralized than their counterparts in higher animals. For example, plants lack a central nervous system, and consequently, phenotypic expression is determined locally in many cases. Plants acquire resources from many different organs, above ground and below, thus avoiding restrictions that would be imposed by one or a small number of mouths. Diverse plant structures arise from undifferentiated meristems that have the potential to produce any cell type, including germ cells and somatic cells. In addition, these diverse plant organs can be produced repeatedly during the lifespan of an individual. Important plant organs are generally found in multiple, redundant copies, making any single organ more expendable than similar organs in most animals. This open-ended growth form allows plants enormous developmental flexibility, an important attribute that was recognized by the Greek botanist Theophrastus approximately 300 years BC (White 1984, Herrera 2009). Developmental flexibility allows plants to respond to environmental cues and change morphology, adding or shedding organs in response to current or anticipated conditions and allowing plants to “forage” for light, water, and soil nutrients and to allocate resources to reproduction, growth, or storage.

The philosopher Michael Marder (2012, 2013) has recently introduced the idea that plants sense their environments by focusing attention towards some cues more than others. The attention is dynamic, allowing plants to selectively respond to shifting, current stimuli. Many studies of plant responses to resource heterogeneity attest to the ability of plants to sense many stimuli (chapter 2) and selectively respond (e.g., chapters 5–8). In addition, different cues vie for the attention of sense organs or receptors that are distributed throughout the plant’s tissues. Plant sensing is not contemplative, but active, and translates into various behaviors (see section 1.2.1). Unlike memory, which is also displayed by plants but is biased towards past events, plant attention as described by Marder is focused on current stimuli.

As humans, we have a tendency to compare plants to humans and other higher animals. Such comparisons can be useful at times, since our awareness and understanding of human behavior and communication is so much better developed. However, such comparisons can range from counterproductive to absurd, if done uncritically. For example, several authors assert that plants can appreciate and benefit from hearing particular kinds of music, most famously in the popular book, The Secret Lives of Plants (Tompkins and Bird 1973). The hypothesis that plants may respond to music is not itself absurd, since plants can sense and respond to electromagnetic radiation and acoustic energy (Telewski 2006, Gagliano et al. 2012b). However, asserting that plants benefit from music without carefully controlled experiments is not science and has hurt progress in this field and acceptance of these ideas. In summary, while plants don’t appear at first glance to behave, in some cases they have evolved functions that are analogous to those in animals, but with different mechanisms and capabilities.

1.2 Working definitions

1.2.1 Plant behavior

Before attempting to determine whether plants exhibit behaviors including communication, it seems reasonable to agree upon a set of criteria that define these phenomena. This is more difficult than it sounds. Although animal behavior is a relatively mature field, practitioners of that field cannot reach a consensus about what constitutes behavior (Levitis et al. 2009). Early behaviorists defined the term quite restrictively; Tinbergen (1955), for example, wrote that behavior included “the total movements made by an intact animal.” This definition excludes plants (and other taxa) and it also fails to include inactivity or decisions to not reproduce as behavior, as well as changes in traits not involving physical movement. Some behaviorists wish to differentiate between intentional, purposeful behaviors from actions that result as unintended consequences of other processes. This distinction has proven to be problematic since it is virtually impossible to determine an animal’s intent. A recent survey of behavioral biologists found little concordance about what phenomena could be considered behaviors although approximately half of the respondents identified plant responses to light as a behavior (Levitis et al. 2009).

The possibility that plants exhibit behavior is not a new suggestion. Charles Darwin’s grandfather, Erasmus Darwin (1794:107), speculated that “vegetable life seems to possess an organ of sense to distinguish varying degrees of moisture, another of light, another of touch, and finally another analogous to our sense of smell.” As is often the case in biology, Charles Darwin, who seems to have foreshadowed much of modern biology, provided detailed descriptions of many plant species that moved in response to light, gravity, and contact (Darwin 1880). In a more recent attempt to explicitly define behavior to include plants, Jonathan Silvertown and Deborah Gordon (1989) described behavior as a response to an event or environmental change during the course of the lifetime of an individual. Responses ultimately are the result of physiological changes that have a biochemical basis. Behavior differs from other physiological and biochemical reactions by occurring rapidly relative to the lifespan of the individual and requires a response to a stimulus. Furthermore, behavioral responses need not be permanent, and can be reversed if the stimulus changes. For example, the decision to expand a shoot into a sunny patch is reversible in the sense that it can be stopped and additional resources allocated to other tissues should that shoot become shaded. However, the resources that have been allocated to that shoot cannot be fully recovered. This definition of behavior does not include changes that are the result of ontogeny (Silvertown and Gordon 1989, Silvertown 1998). For example, the changes that occur as a seed germinates and expands its cotyledons and then its true leaves are not considered behavioral responses since they are part of a developmental program that is not plastic, once initiated. This definition of behavior is similar to one used by plant biologists to describe phenotypic plasticity (Bradshaw 1965), and behavior may be considered a form of plasticity that occurs rapidly and reversibly in response to a stimulus.

1.2.2 Plant sensing, eavesdropping, communication, cues and signals

Communication can be considered a behavior that provides information from a sender to a receiver. Communication also provides information that can cause the receiver of that information to respond (behave). As was the case for behavior, there is no agreed-upon definition of what constitutes communication either for animals or for plants (Scott-Phillips 2008, Schenk and Seabloom 2010). Most definitions require that receivers respond to cues or stimuli (Karban 2008). This requirement is considered necessary but not sufficient by most workers who study animal behavior since it includes situations in which receivers respond to cues from their abiotic environment. In keeping with accepted definitions, I will regard responses to stimuli as examples of plants sensing cues but not communicating. How plants sense their environments is fascinating in its own right and will be discussed at length later in this book. I will restrict my use of the term “communication” to situations in which emission or display of a cue is plastic and the response of the receiver is conditional on receiving the cue. For example, a plant that always attains a short compact growth form because of its genes is not responding to cues in a proximate, short-term sense. A plant that adjusts its morphology depending upon the cues that it receives from its neighbors may or may not be considered to be communicating.

Definitions of communication tend to emphasize either the exchange of information from a sender to a receiver (Smith 1977, Hauser 1996) or the requirement that the transfer of information be favored by natural selection (Maynard Smith and Harper 1995, Scott-Phillips 2008). Cues provide the receiver with accurate estimates of the relative probabilities of alternative conditions. Both the amount of informa...