In 1973, a book claiming that plants were sentient beings that feel emotions, prefer classical music to rock and roll, and can respond to the unspoken thoughts of humans hundreds of miles away landed on the New York Times best-seller list for nonfiction. “The Secret Life of Plants,” by Peter Tompkins and Christopher Bird, presented a beguiling mashup of legitimate plant science, quack experiments, and mystical nature worship that captured the public imagination at a time when New Age thinking was seeping into the mainstream. The most memorable passages described the experiments of a former C.I.A. polygraph expert named Cleve Backster, who, in 1966, on a whim, hooked up a galvanometer to the leaf of a dracaena, a houseplant that he kept in his office. To his astonishment, Backster found that simply by imagining the dracaena being set on fire he could make it rouse the needle of the polygraph machine, registering a surge of electrical activity suggesting that the plant felt stress. “Could the plant have been reading his mind?” the authors ask. “Backster felt like running into the street and shouting to the world, ‘Plants can think!’ ”
Backster and his collaborators went on to hook up polygraph machines to dozens of plants, including lettuces, onions, oranges, and bananas. He claimed that plants reacted to the thoughts (good or ill) of humans in close proximity and, in the case of humans familiar to them, over a great distance. In one experiment designed to test plant memory, Backster found that a plant that had witnessed the murder (by stomping) of another plant could pick out the killer from a lineup of six suspects, registering a surge of electrical activity when the murderer was brought before it. Backster’s plants also displayed a strong aversion to interspecies violence. Some had a stressful response when an egg was cracked in their presence, or when live shrimp were dropped into boiling water, an experiment that Backster wrote up for the International Journal of Parapsychology, in 1968.
In the ensuing years, several legitimate plant scientists tried to reproduce the “Backster effect” without success. Much of the science in “The Secret Life of Plants” has been discredited. But the book had made its mark on the culture. Americans began talking to their plants and playing Mozart for them, and no doubt many still do. This might seem harmless enough; there will probably always be a strain of romanticism running through our thinking about plants. (Luther Burbank and George Washington Carver both reputedly talked to, and listened to, the plants they did such brilliant work with.) But in the view of many plant scientists “The Secret Life of Plants” has done lasting damage to their field. According to Daniel Chamovitz, an Israeli biologist who is the author of the recent book “What a Plant Knows,” Tompkins and Bird “stymied important research on plant behavior as scientists became wary of any studies that hinted at parallels between animal senses and plant senses.” Others contend that “The Secret Life of Plants” led to “self-censorship” among researchers seeking to explore the “possible homologies between neurobiology and phytobiology”; that is, the possibility that plants are much more intelligent and much more like us than most people think—capable of cognition, communication, information processing, computation, learning, and memory.
The quotation about self-censorship appeared in a controversial 2006 article in Trends in Plant Science proposing a new field of inquiry that the authors, perhaps somewhat recklessly, elected to call “plant neurobiology.” The six authors—among them Eric D. Brenner, an American plant molecular biologist; Stefano Mancuso, an Italian plant physiologist; František Baluška, a Slovak cell biologist; and Elizabeth Van Volkenburgh, an American plant biologist—argued that the sophisticated behaviors observed in plants cannot at present be completely explained by familiar genetic and biochemical mechanisms. Plants are able to sense and optimally respond to so many environmental variables—light, water, gravity, temperature, soil structure, nutrients, toxins, microbes, herbivores, chemical signals from other plants—that there may exist some brainlike information-processing system to integrate the data and coördinate a plant’s behavioral response. The authors pointed out that electrical and chemical signalling systems have been identified in plants which are homologous to those found in the nervous systems of animals. They also noted that neurotransmitters such as serotonin, dopamine, and glutamate have been found in plants, though their role remains unclear.
Hence the need for plant neurobiology, a new field “aimed at understanding how plants perceive their circumstances and respond to environmental input in an integrated fashion.” The article argued that plants exhibit intelligence, defined by the authors as “an intrinsic ability to process information from both abiotic and biotic stimuli that allows optimal decisions about future activities in a given environment.” Shortly before the article’s publication, the Society for Plant Neurobiology held its first meeting, in Florence, in 2005. A new scientific journal, with the less tendentious title Plant Signaling & Behavior, appeared the following year.
Depending on whom you talk to in the plant sciences today, the field of plant neurobiology represents either a radical new paradigm in our understanding of life or a slide back down into the murky scientific waters last stirred up by “The Secret Life of Plants.” Its proponents believe that we must stop regarding plants as passive objects—the mute, immobile furniture of our world—and begin to treat them as protagonists in their own dramas, highly skilled in the ways of contending in nature. They would challenge contemporary biology’s reductive focus on cells and genes and return our attention to the organism and its behavior in the environment. It is only human arrogance, and the fact that the lives of plants unfold in what amounts to a much slower dimension of time, that keep us from appreciating their intelligence and consequent success. Plants dominate every terrestrial environment, composing ninety-nine per cent of the biomass on earth. By comparison, humans and all the other animals are, in the words of one plant neurobiologist, “just traces.”
Many plant scientists have pushed back hard against the nascent field, beginning with a tart, dismissive letter in response to the Brenner manifesto, signed by thirty-six prominent plant scientists (Alpi et al., in the literature) and published in Trends in Plant Science. “We begin by stating simply that there is no evidence for structures such as neurons, synapses or a brain in plants,” the authors wrote. No such claim had actually been made—the manifesto had spoken only of “homologous” structures—but the use of the word “neurobiology” in the absence of actual neurons was apparently more than many scientists could bear.
“Yes, plants have both short- and long-term electrical signalling, and they use some neurotransmitter-like chemicals as chemical signals,” Lincoln Taiz, an emeritus professor of plant physiology at U.C. Santa Cruz and one of the signers of the Alpi letter, told me. “But the mechanisms are quite different from those of true nervous systems.” Taiz says that the writings of the plant neurobiologists suffer from “over-interpretation of data, teleology, anthropomorphizing, philosophizing, and wild speculations.” He is confident that eventually the plant behaviors we can’t yet account for will be explained by the action of chemical or electrical pathways, without recourse to “animism.” Clifford Slayman, a professor of cellular and molecular physiology at Yale, who also signed the Alpi letter (and who helped discredit Tompkins and Bird), was even more blunt. “ ‘Plant intelligence’ is a foolish distraction, not a new paradigm,” he wrote in a recent e-mail. Slayman has referred to the Alpi letter as “the last serious confrontation between the scientific community and the nuthouse on these issues.” Scientists seldom use such language when talking about their colleagues to a journalist, but this issue generates strong feelings, perhaps because it smudges the sharp line separating the animal kingdom from the plant kingdom. The controversy is less about the remarkable discoveries of recent plant science than about how to interpret and name them: whether behaviors observed in plants which look very much like learning, memory, decision-making, and intelligence deserve to be called by those terms or whether those words should be reserved exclusively for creatures with brains.
No one I spoke to in the loose, interdisciplinary group of scientists working on plant intelligence claims that plants have telekinetic powers or feel emotions. Nor does anyone believe that we will locate a walnut-shaped organ somewhere in plants which processes sensory data and directs plant behavior. More likely, in the scientists’ view, intelligence in plants resembles that exhibited in insect colonies, where it is thought to be an emergent property of a great many mindless individuals organized in a network. Much of the research on plant intelligence has been inspired by the new science of networks, distributed computing, and swarm behavior, which has demonstrated some of the ways in which remarkably brainy behavior can emerge in the absence of actual brains.
“If you are a plant, having a brain is not an advantage,” Stefano Mancuso points out. Mancuso is perhaps the field’s most impassioned spokesman for the plant point of view. A slight, bearded Calabrian in his late forties, he comes across more like a humanities professor than like a scientist. When I visited him earlier this year at the International Laboratory of Plant Neurobiology, at the University of Florence, he told me that his conviction that humans grossly underestimate plants has its origins in a science-fiction story he remembers reading as a teen-ager. A race of aliens living in a radically sped-up dimension of time arrive on Earth and, unable to detect any movement in humans, come to the logical conclusion that we are “inert material” with which they may do as they please. The aliens proceed ruthlessly to exploit us. (Mancuso subsequently wrote to say that the story he recounted was actually a mangled recollection of an early “Star Trek” episode called “Wink of an Eye.”)
In Mancuso’s view, our “fetishization” of neurons, as well as our tendency to equate behavior with mobility, keeps us from appreciating what plants can do. For instance, since plants can’t run away and frequently get eaten, it serves them well not to have any irreplaceable organs. “A plant has a modular design, so it can lose up to ninety per cent of its body without being killed,” he said. “There’s nothing like that in the animal world. It creates a resilience.”
Indeed, many of the most impressive capabilities of plants can be traced to their unique existential predicament as beings rooted to the ground and therefore unable to pick up and move when they need something or when conditions turn unfavorable. The “sessile life style,” as plant biologists term it, calls for an extensive and nuanced understanding of one’s immediate environment, since the plant has to find everything it needs, and has to defend itself, while remaining fixed in place. A highly developed sensory apparatus is required to locate food and identify threats. Plants have evolved between fifteen and twenty distinct senses, including analogues of our five: smell and taste (they sense and respond to chemicals in the air or on their bodies); sight (they react differently to various wavelengths of light as well as to shadow); touch (a vine or a root “knows” when it encounters a solid object); and, it has been discovered, sound. In a recent experiment, Heidi Appel, a chemical ecologist at the University of Missouri, found that, when she played a recording of a caterpillar chomping a leaf for a plant that hadn’t been touched, the sound primed the plant’s genetic machinery to produce defense chemicals. Another experiment, done in Mancuso’s lab and not yet published, found that plant roots would seek out a buried pipe through which water was flowing even if the exterior of the pipe was dry, which suggested that plants somehow “hear” the sound of flowing water.
The sensory capabilities of plant roots fascinated Charles Darwin, who in his later years became increasingly passionate about plants; he and his son Francis performed scores of ingenious experiments on plants. Many involved the root, or radicle, of young plants, which the Darwins demonstrated could sense light, moisture, gravity, pressure, and several other environmental qualities, and then determine the optimal trajectory for the root’s growth. The last sentence of Darwin’s 1880 book, “The Power of Movement in Plants,” has assumed scriptural authority for some plant neurobiologists: “It is hardly an exaggeration to say that the tip of the radicle . . . having the power of directing the movements of the adjoining parts, acts like the brain of one of the lower animals; the brain being seated within the anterior end of the body, receiving impressions from the sense organs and directing the several movements.” Darwin was asking us to think of the plant as a kind of upside-down animal, with its main sensory organs and “brain” on the bottom, underground, and its sexual organs on top.
Scientists have since found that the tips of plant roots, in addition to sensing gravity, moisture, light, pressure, and hardness, can also sense volume, nitrogen, phosphorus, salt, various toxins, microbes, and chemical signals from neighboring plants. Roots about to encounter an impenetrable obstacle or a toxic substance change course before they make contact with it. Roots can tell whether nearby roots are self or other and, if other, kin or stranger. Normally, plants compete for root space with strangers, but, when researchers put four closely related Great Lakes sea-rocket plants (Cakile edentula) in the same pot, the plants restrained their usual competitive behaviors and shared resources.
Somehow, a plant gathers and integrates all this information about its environment, and then “decides”—some scientists deploy the quotation marks, indicating metaphor at work; others drop them—in precisely what direction to deploy its roots or its leaves. Once the definition of “behavior” expands to include such things as a shift in the trajectory of a root, a reallocation of resources, or the emission of a powerful chemical, plants begin to look like much more active agents, responding to environmental cues in ways more subtle or adaptive than the word “instinct” would suggest. “Plants perceive competitors and grow away from them,” Rick Karban, a plant ecologist at U.C. Davis, explained, when I asked him for an example of plant decision-making. “They are more leery of actual vegetation than they are of inanimate objects, and they respond to potential competitors before actually being shaded by them.” These are sophisticated behaviors, but, like most plant behaviors, to an animal they’re either invisible or really, really slow.