Plant intelligence. On researchers' efforts to understand flora. - Zeme un valsts

Plant intelligence. On researchers' efforts to understand flora.

A book claiming that plants possess the ability to sense emotions, choose classical music over rock and roll, and react to unspoken human thoughts from hundreds of kilometres away, reached the The New York Times bestseller list in 1973. “The Secret Life of Plants” by Peter Tompkins and Christopher Bird presented readers with a fascinating blend of legitimate plant science, charlatan experiments, and mystical nature worship, and in an era when New Age thinking was gaining widespread public attention, it all stirred the public imagination. Some of the most memorable passages were dedicated to Cleve Backster, a CIA lie detector expert, who in 1966 had, out of the blue, attached a galvanometer to the leaves of a dracaena growing in his office. To his surprise, merely imagining that the plant was being burned caused the polygraph needle to move, indicating electrical activity triggered by plant stress. “Could the plant read his thoughts?” the authors of the book ask. “Backster felt he should rush out into the street and tell everyone that plants can think.”

Backster and his colleagues went on to hook dozens of plants to lie detectors – lettuce, onions, oranges, banana trees. He claimed that plants react to human thoughts (good or bad) if they are in the immediate vicinity, and to the thoughts of people they know even from a great distance. In one experiment designed to evaluate the memory capacity of plants, Backster discovered that a plant that had witnessed the murder of another plant (by being trampled) could identify the killer from six suspects, showing increased electrical activity in the presence of the killer. Backster's plants also displayed strong resistance to inter-species violence. Some showed signs of stress if an egg was broken nearby or a live shrimp was dropped into boiling water – such experiments were described by Backster in a 1968 publication in the International Journal of Parapsychology.

In the following years, a number of serious plant researchers unsuccessfully tried to replicate the “Backster effect” in their own experiments. It was proven that most of the experiments described in “The Secret Life of Plants” cannot be scientifically verified. However, the book had already left its mark on culture. Americans began talking to their plants and playing Mozart to them, and it is likely that many people still do so today. This might seem innocent enough, as there will probably always be a romantic streak in our thinking about plants. (Luther Burbank and George Washington Carver, it is said, spoke to plants and listened to them during their ground-breaking research.) However, in the opinion of many biologists, “The Secret Life of Plants” has done lasting harm to their field. For instance, the Israeli biologist Daniel Chamovitz, who recently published the book “What a Plant Knows”, believes that Tompkins and Bird have “held back significant research into plant behaviour because scientists become cautious as soon as parallels between animal and plant senses are even mentioned in research.” Others argue that influenced by “The Secret Life of Plants”, researchers who have sought to delve into “potential parallels between neurobiology and phytobiology” or, in other words, considered the possibility that plants are far smarter and more like us, endowed with cognitive, communicative, information processing, computational, learning, and memory capabilities, have begun to engage in “self-censorship”.

A quote about self-censorship appeared in 2006 in a controversial article published in the journal Trends in Plant Science, the authors of which encouraged, perhaps a bit boldly, the establishment of a new field of research that could be called “plant neurobiology”. Six authors – among them the American plant molecular biologist Eric D. Brenner, the Italian plant physiologist Stefano Mancuso, the Slovak cell biologist František Baluška, and the American plant biologist Elizabeth Van Volkenburgh – argued that the complex behaviour of plants captured in observations cannot be fully explained by known genetic and biochemical mechanisms. Plants have the ability to sense and optimally respond to many environmentally determined variables – light, water, gravity, temperature, soil structure, nutrients, toxins, microbes, herbivores, chemical signals sent by other plants – and therefore there might exist some brain-like system that integratedly processes all this information and coordinates the plant's behaviour accordingly. The authors pointed out that electrochemical signal transmission systems have been discovered in plants that resemble the nervous systems of animals. They also noted that neurotransmitters such as serotonin, dopamine, and glutamate have been found in plants, although their significance remains unclear.

Therefore, a plant neurobiology is needed, or a new discipline whose “goal would be to understand how plants perceive their growing conditions and respond to environmental conditions in an integrated way”. The article claimed that plants exhibit intelligence, which, according to the authors' definition, is “an inherent ability to process information from both abiotic and biotic stimuli, allowing for optimal decisions to be made about future behaviour in specific environmental conditions”. Shortly before the article was published, the first meeting of the Society for Plant Neurobiology took place in Florence in 2005. A year later – albeit with a less pretentious name – a new scientific journal, Plant Signaling & Behavior, began publication.

Whether plant neurobiology will be perceived as a completely new paradigm for our understanding of life or as something inherited from the muddy waters of science, stirred up by “The Secret Life of Plants”, will depend on whom you ask about it. Proponents of this field of science believe that we must stop perceiving plants as passive objects – as mute, immobile furniture of our world – and start viewing them as protagonists of our own life dramas with highly developed survival skills. They reproach modern biology for focusing solely on cells and genes and encourage focusing on the organism as a whole and its behaviour in the environment. In their view, our inability to appreciate plant intelligence is caused solely by human arrogance, as well as the fact that plant life occurs much more slowly in terms of time. At the same time, plants dominate in all Earth's habitats, collectively making up 90% of the planet's total biomass. By comparison, humans and other animals, from the perspective of a plant neurobiologist, are “merely footnotes”.

Many plant researchers, however, resist the intrusive new discipline – first of all with a sharply dismissive letter signed by six authors (mentioned in the literature as Alpi et al.), which was a response to Brenner’s manifesto and was also published in the journal Trends in Plant Science. “First of all, it must be pointed out that there is no evidence that structures such as neurons, synapses, or a brain exist in plants,” the authors of the letter wrote. This, however, had never been claimed – the manifesto only spoke about “homologous” structures – but it seems that for many scientists, using the term “neurobiology” in the absence of actual neurons felt unacceptable.

“Yes, plants use both short-term and long-term electrical signals, and neurotransmitter-like chemical signals can also be found in them,” Lincoln Taiz, Professor Emeritus of Psychology at the University of California, Santa Cruz, and one of the signatories of the Alpi letter, told me. “However, the mechanisms involved are very different from those operating in actual nervous systems.” Taiz claims that publications by neurobiologists are characterised by “over-interpreted data, teleology, anthropomorphism, philosophising, and an indulgence in speculation”. He is convinced that even those forms of plant behaviour for which there is currently no explanation will one day be explained by electrochemical processes, but without slipping into “animism”. Clifford Slayman, Professor of Cellular and Molecular Physiology at Yale University and another signatory of the Alpi letter (and one of the debunkers of Tompkins and Bird), is even harsher. “Plant intelligence is a silly misunderstanding, not a new paradigm,” he wrote in an email. He called the Alpi letter “the last serious confrontation by the scientific community with the madhouse in which such topics reside”. When speaking about their colleagues to journalists, scientists rarely choose such harsh expressions, but this topic stirs strong feelings – perhaps because it seeks to blur the clear boundary that separates the animal kingdom from the plant kingdom. The disagreement is not so much about the most remarkable recent discoveries in plant science, but about how to interpret and name them: does the behaviour observed in plants, which very much resembles learning, memory, decision-making, and intelligence, deserve to be called by these terms, or should these words be used only when talking about beings endowed with brains?

None of the scientists from various fields working on plant intelligence research that I spoke to tried to claim that plants possess telekinetic gifts or the ability to feel emotions. Likewise, no one believed that we could manage to find an organ the size of a walnut anywhere in plants that would process information gathered by senses and determine the plant's behaviour. In the scientists' opinion, it is much more likely that plant intelligence resembles that found in insect colonies, where it is believed to be formed by a network of individually unintelligent beings organized by mutual cooperation. A large portion of plant intelligence research is inspired by the latest discoveries in network operation, distributed data processing, and swarming, which have allowed us to see behaviour similar to brain activity even in cases where there are no brains themselves.

“If you are a plant, having a brain is not an advantage,” says Stefano Mancuso. Mancuso is probably the most passionate advocate of the plant perspective in the field. The unkempt, bearded Calabrian, just over forty, looks more like a humanities professor than a natural scientist. When I visited him at the International Laboratory of Plant Neurobiology at the University of Florence this year, he told me that his conviction that people underestimate plants was sparked by a piece of science fiction he read as a teenager. Aliens living in a radically accelerated time dimension arrive on Earth and, unable to see any movement in humans, come to the logical conclusion that we are just “inert material” and therefore can be dealt with as they please. So the aliens begin to exploit us mercilessly. (Later, Mancuso wrote to me that those were distorted memories of a “Star Trek” episode titled “Wink of an Eye”.)

In Mancuso’s view, the fact that we “fetishize” neurons, as well as our tendency to associate behaviour with mobility, prevents us from appreciating the capabilities of plants. For example, since plants cannot escape and are often eaten, it is only logical that they do not have vital organs. “Plants have a modular structure, and therefore they can lose up to 90% of their volume without dying,” he explained. “There is nothing like that in the animal world. It is a huge vitality.”

Admittedly, many of the most impressive abilities of plants are linked to their existential doom of being rooted in the ground, so they cannot go anywhere to satisfy their needs or run away if conditions become unbearable. Plant biologists call this a “sessile lifestyle” because, since a plant must be able to find everything it needs and protect itself while remaining in a fixed position, it possesses an extremely broad and nuanced understanding of its immediate location. Finding nutrients and identifying dangers requires a highly developed sensory system. Plants possess 15–20 senses, including five that are the same as ours: smell and taste (they react to chemicals both in the air and on their surface), sight (they react to light of different wavelengths, as well as to shade), touch (a vine or root “knows” when it has hit an obstacle), and, as discovered, hearing. In a recent experiment, ecological chemist Heidi Appel from the University of Missouri played the sounds of a caterpillar attack to a plant, and the plant, which in reality was being eaten by no one, activated genetic machinery that produces the necessary chemical substances for defence. In another experiment, conducted in Mancuso’s laboratory and not yet published, it was observed that plant roots seek out a water pipe even if its exterior is dry, which led to the suggestion that the plant somehow “hears” the water flowing in the pipe.

The sensory capabilities of roots also fascinated Charles Darwin, and in his old age he became particularly interested in plants – conducting, together with his son Francis, quite a few interesting experiments with them. In many of them, they used roots or root hairs and observed that plants are able to sense light, moisture, gravity, pressure, and several other environmental properties, the combination of which determines the optimal trajectory of root growth. The conclusion of Darwin's 1880 book “The Power of Movement in Plants” is like a passage from holy scripture to 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 urged us to look at plants as upside-down animals, whose main senses and “brains” are located underground, while reproductive organs are above.

Since then, scientists have discovered that with roots, plants can sense not only gravity, moisture, light, pressure, or soil hardness, but also volume, nitrogen, phosphorus, salt, various toxins, microbes, and chemical signals from other plants in the vicinity. Encountering an insurmountable obstacle or a toxic substance, roots change their growth direction even before coming into direct contact with it. Roots are able to distinguish their own from foreign ones, but if they are foreign – whether they belong to the same species or another. Usually, plants fight for root space with strangers, but when scientists once planted seedlings of closely related Great Lakes sea rocket in the same flowerpot, the plants restrained their usual competition and shared the available resources in a brotherly fashion.

Plants somehow collect and aggregate all information about their surroundings and only then “decide” which way to drive their roots and shoots; some researchers use quotation marks, indicating that it is only a metaphor, others manage without. If we apply the concept of “behaviour” also to phenomena such as changes in root trajectory, resource redistribution, or the release of powerful chemical substances, plants indeed begin to look like agents capable of acting, which can react to changes in the environment much more nuancedly and precisely than could be described by the term “instinct”. “Plants perceive competitors and grow away from them,” explained a plant ecologist from the University of California, Davis, when I asked him a question about the ability of plants to make decisions. “They pay much more attention to already existing vegetation than to other immovable objects, and are ready to react to potential competitors even before they have been shaded.” These are quite complex actions, and yet, like most plant behaviour, they remain either invisible or extremely slow to the eyes of an animal.

For their sessile lifestyle, plants can also be grateful for their special biochemical gifts, which far exceed those of which animals and perhaps even humans are capable. (Many medicines, from aspirin to opiates, are derived from compounds developed in the plant kingdom.) Since plants cannot run away, they use a complex molecular alphabet to report danger, repel or poison enemies, or link animals that perform various services for them. A recent study published in the journal Science found that the caffeine produced by many plants is not only a chemical intended for defence, as was previously thought, but in some cases also a psychoactive substance found in nectar. Caffeine encourages bees to remember the specific plant and return to it, thereby becoming more reliable and effective pollinators.

One of the most fertile areas of research in recent years is plant signalling systems. It has been known since the early 1980s that plants whose leaves have been attacked by disease or pests warn healthy leaves so that they can mobilize for defence. Sometimes such a warning signal includes information about what kind of insect is the attacker, which is determined by the taste of its saliva. Depending on the plant and the attacker, the chosen defence can be either a change in taste or texture, as well as the release of toxins or other substances, thus making the leaves less tempting to herbivores. When antelopes eat acacia branches, the leaves release tannins, which make them unpalatable and harder to digest. If food is scarce and acacias are heavily grazed, it has been observed that they can produce even so much toxin that it can be lethal.

Perhaps the most clever examples of plant signalling are related to two insect species – pests and the species that fight them. Several plant species, including corn and white beans, report a caterpillar attack with a chemical alarm signal. It is picked up even from a considerable distance by parasitic wasps, which head to the infested plant and slowly deal with the caterpillars. Researchers call such insects “plant bodyguards”.

Plants speak in a chemical language that we are directly unable to either perceive or understand. The first significant discoveries about plant communication were made in the 1980s, when plants and their chemical secretions were separated in plexiglass compartments, but Rick Karban from the University of California, Davis, has set himself a much trickier goal – to find out how plants exchange chemical signals under the open sky, in natural conditions. I recently visited Karban’s test plot, located at the University of California’s Sagehen Creek Field Station near Truckee. On a sun-drenched Sierra slope, he introduced me to 99 sagebrush seedlings – low, slow-growing bushes with grey-green leaves marked with plastic flags, which he and his colleagues have been carefully observing for more than 10 years.

Karban once lived in New York, he is 59 years old and has a mane of white hair that his wide-brimmed hat is poor at containing. He has demonstrated: if you trim the leaves of sagebrush in the spring – simulating an insect attack and promoting the production of poisonous substances – both the trimmed bush and its neighbours suffer much less from pest attacks in the summer. Karban believes that a plant warns all its leaves about the presence of a pest, but the signal is also picked up by its neighbours, and everyone ensures protection against the attack. “In our opinion, sagebrush here eavesdrop on each other,” Karban explained. He has discovered that there is a connection between responding to chemical signals and plant kinship, which could prove that plants are able to recognize their own. Helping relatives is a good way to increase the chances of one’s own genes surviving.

The field research and data collection underlying such discoveries are extremely laborious. On the lower part of the slope, lit by the slanting rays of the late summer sun, two scientific associates from Japan worked – Kaori Shiojiri and Satomi Ishizaki. Crouched in the shade of a small pine tree, they studied sagebrush branches marked and trimmed by Karban. With a click-counter, they counted all the three-lobed leaves on each branch, and then recorded the damage to each leaf – in one column they wrote down insect bites, in the other – signs of disease. At the top of the slope, another associate – ecological chemist James Blande from the United Kingdom – was wrapping sagebrush branches in polyethylene bags filled with filtered air. Having waited 20 minutes for the plant to release essential oils, he released the air from the bags through a metal cylinder, where the adsorbent placed inside had to collect all chemical secretions. In the laboratory, they will be analysed with a gas chromatograph-mass spectrometer, allowing a list of released compounds to be created – there are more than a hundred. Blande allowed me to smell the contents of one bag: a strong aroma was felt in the air, which reminded more of aftershave lotion than perfume. Glancing over the sagebrush stand, I found it difficult to imagine a chemical chatter and exchange of alarm signals happening all around, not to mention that these immobile plants could have any “behaviour” at all.

Plant communication research might one day prove useful to farmers and their crops. The chemical compounds of plant alarms can be used to mobilize their defensive capabilities, thereby reducing the need to use pesticides. Ecological chemistry specialist Jack Schultz from the University of Missouri conducted one of the first studies on plant signalling capabilities in the 1980s. Now he is helping in the development of a mechanical “nose”: it will be a device attached to a tractor that will be able to identify plants that have been attacked by pests, and pesticides can then be sprayed only on them.

Karban told me that people who had worked on plant communication research in the 80s encountered the same outrage as those working on plant intelligence today (a concept he is prepared to accept with caution). “It was an extremely controversial topic,” he remembers when speaking about plant communication, which is now a mostly accepted field of research. “It took years before I managed to publish some of these studies,” he said. “Plant researchers are mostly very conservative. We only think we want to hear new ideas, but in reality, we don’t.”

I first met Karban in Vancouver last July at a scientific conference, where he introduced the paper “Plant Communication and Kin Recognition in Sagebrush”. It was supposed to be the sixth meeting of the Society for Plant Neurobiology, but after pressure from some of the scientific elite four years ago, the group had been given a less provocative name, and now it was the Society for Plant Signaling & Behavior. As one of the founders of the society, plant biologist Elizabeth Van Volkenburgh from the University of Washington, told me, the name was changed after long internal debates, in which it was decided that it would be wiser to abandon “neurobiology” after all. “Someone from the National Science Foundation (NSF) said that the NSF would never grant funds if the phrase “plant neurobiology” were used. They said exactly that: ““Neuro” belongs to animals.” (An NSF representative said that although the society cannot claim funding from the neurobiology program, “the NSF in no way boycotts the work of the society”.) Two of the society's founders, Stefano Mancuso and František Baluška, sharply objected to the name change, and both continue to use the term “plant neurobiology” both in their work and in the names of their laboratories.

The conference lasted three days, and during that time about a hundred listeners were presented with many PowerPoint presentations in a modern lecture hall at the University of British Columbia. Most of the papers were highly technical reports on plant signalling: this was the kind of science that successfully continues to develop within the boundaries of an established scientific paradigm, because plant signalling has already become such a science. However, some speakers had dedicated their work to the new paradigm of plant intelligence, and their presentations caused a strong resonance.

The most controversial presentation was “Animal-Like Learning in Mimosa”, which was an as yet unpublished work by the University of Western Australia animal ecologist Monica Gagliano: she works for Mancuso at his Florence laboratory. Gagliano, a 37-year-old tall woman with long, dark brown hair parted in the middle, had used protocols in her experiments that are typically used when studying animals. She had focused her attention on a basic form of learning called habituation, during which the subject of the experiment must learn the ability to ignore irrelevant stimuli. “Habituation allows an organism to focus on essential information, separating noise from it,” Gagliano explained to the audience of plant scientists. How long does it take for an animal to realize that a stimulus is “noise”, and how long will what it has learned remain in its memory? Gagliano’s experiments posed the disturbing question: “Can something like this be achieved with plants too?”

Mimosa pudica, also called the “sensitive plant”, is a fern-like plant with such nimble behaviour that it can be observed even by the eyes of a living being; another such plant is the Venus flytrap. When you touch the leaves of a mimosa, they tend to shrink instantly, presumably to repel insects. Mimosa also pulls its leaves in if the plant tips over or is shaken. Gagliano had mounted 56 pots of mimosas in a special system that allowed them to be dropped 15 centimetres every five seconds. Each “training session” had 60 drops. She observed that some mimosas stopped closing their leaves after only four, five, or six drops, as if they had concluded that this stimulus could be ignored. “In the end, they were completely open,” Gagliano told the audience, “they didn’t care anymore.”

Couldn’t it just have been exhaustion? Obviously not, because when the plants were shaken again, they closed their leaves. “Oh, something new again,” Gagliano imagined herself in the plants' place. “You see, you have to be ready for something new all the time. But then we returned to the drops, and the plants didn’t react again.” Gagliano reported that she checked the plants after a week and discovered that they still did not care about the dropping stimulus, thereby proving that they “remember” what they had learned. The lesson had not been forgotten even after 28 days. She reminded her colleagues that, for example, bees in similar experiments tend to forget what they have learned after even 48 hours. This allowed Gagliano to conclude that “brains and neurons are a sophisticated solution, but learning is possible without them”, and furthermore, “living organisms possess a similar mechanism for information processing and learning”.

A lively exchange of thoughts followed. Some objected that throwing pots around is not an appropriate stimulus, because it is not encountered in nature. Gagliano pointed out that electrical pulses, which are also not encountered by animals in nature, are often used in animal studies. Another researcher mentioned that maybe it hadn’t been habituation, but the plants had simply withered. He argued that 28 days should have been enough for them to recover after the tossing.

Coming out of the conference room, I bumped into Fred Sack, a well-known botanist from the University of British Columbia. I asked what his thoughts were on Gagliano’s presentation. “Nonsense,” he replied. He explained that the word “learning” implies the involvement of a brain and therefore applies only to animals. “Animals are able to show learning, but plants perform adaptation.” He urged distinguishing between changes in behaviour that happen during a lifetime and those that organisms experience over several generations. At lunch, I happened to be at the same table as a Russian scientist, who was equally dismissive. “It’s not learning,” he said, “so there is nothing here to discuss.”

Later in the afternoon, it seemed that Gagliano had been upset by some of the colleagues' objections, and a stubbornness surfaced in her. Gagliano said that adaptation is too slow a process and does not help at all in understanding what she had observed. “And how can plants adapt to something they have never experienced in the real world?” She also pointed out that some plants learned faster than others, and that proved it was not an “innate or programmed reaction”. Many of those gathered in the audience had only just begun to get used to the idea of plant “behaviour” and “memory” (both terms Fred Sack claimed to accept), and therefore terms like plant “learning” or “intelligence” worry them, as Sack would say, as “inappropriate” and “just plain weird”. When I told Lincoln Taiz about these experiments, he said that terms like “habituation” or “desensitization” would be more appropriate, rather than learning. Gagliano said that ten journals had refused to publish her research. No one had objections to the research data, but the language used in the description seemed scary. She did not want to change anything in it. “As long as we don’t use the same language to describe the same behaviour in the plant and animal worlds, we cannot compare,” she said.

Rick Karban tried to comfort Gagliano after her performance: “I have gone through exactly the same thing, I was literally driven into the ground,” he said. “But you have done a great job. The system just isn’t ready for it yet.” When I asked his thoughts on Gagliano’s paper, he told me: “I won’t venture to judge whether she has succeeded in etching it in stone, but the idea itself is cool and deserves to be discussed. I hope she won’t throw in the towel.”

Scientists often feel uncomfortable when asked about the role of metaphor and imagination in their work, but both are often important in scientific progress. “Good scientists use metaphors to stir their research imagination,” British plant scientist Anthony Trewavas wrote in a passionate response to the Alpi letter. “Plant neurobiology” is obviously a metaphor, because plants do not have the kind of excitable and communication-capable cells that we call neurons. But introducing such a concept has forced questions to be raised and experiments to be started that could deepen our understanding not only of plants but also of the brain. If information can be processed in several ways, if there are several types of cells and networks that can trigger intelligent behaviour, we, like Mancuso, can ask ourselves the question: “What is so very special about neurons?”

Mancuso is the poet and philosopher of this entire movement, determined to place plants in their rightful place and perhaps demote humans by a notch in the process. His ambitiously named International Laboratory of Plant Neurobiology with its research rooms and office is located near Florence in a low, modern office building. There, at Mancuso’s initiative, half a dozen associates and senior students experiment with plant intelligence. Leading me through the laboratory, he showed corn seedlings growing under constant artificial light without the slightest shade, a poplar tree to which a galvanometer measured its reaction to air pollution, and a room where a PTR-TOF machine, or special mass spectrometer, continuously monitored the chemical compounds emitted by plants, ranging from poplars and tobacco seedlings to peppers and olive trees. “We are creating a chemical dictionary for every species,” he explained. By his estimate, each plant’s dictionary contains 3,000 chemical compounds, whereas “a student’s vocabulary averages only 700 words”.

Mancuso is ardently attached to plants because, as he claims himself, a scientist “must love their field of activity” to achieve anything in it. But he is gentle and maintains simplicity even when telling the most unbelievable things. In the corner of his office is a pot with a rubber tree, and on the walls are photographs of Mancuso in an astronaut’s outfit floating in a weightlessness simulation aircraft: in cooperation with the European Space Agency, he has conducted research on plant behaviour in micro- and hypergravity. (One of his experiments was carried out on the last voyage of the space shuttle Endeavour in May 2011.) 10 years ago, Mancuso had managed to convince a foundation of a Florence bank to fund his research, and the Society for Plant Neurobiology, his laboratory also receives funding from the European Union.

At the beginning of our conversation, I asked Mancuso how he would define “intelligence”. Having spent so much time in the company of plant neurobiologists, I noticed that I was no longer so sure about the definition of the word myself. And it turned out that I was by no means alone: philosophers and psychologists have been arguing about the definition of intelligence for an entire century, and even the consensus that has been reached once tends to disappear quickly. Most definitions of intelligence fit into one of two categories. The first assumes the presence of a brain, referring to such essential mental activities as reason, judgement, and abstract thinking. The second category includes definitions that are not so centred on the brain and are rather metaphysical, because intelligence in them is understood as the ability to respond optimally to the environment and external conditions. It is no wonder that plant neurobiologists belong to the second camp.

“My definition is very simple,” said Mancuso. “Intelligence is the ability to solve problems. I am not looking for brains, I am looking for the same distributed intelligence that can be observed in a large flock of birds flying together.” Each bird must follow a small set of simple rules, for example, the distance from another bird, but with every bird executing such a simple algorithm, complex and surprisingly well-coordinated behaviour is observed. According to Mancuso’s hypothesis, something similar happens in the plant world, where thousands of root tips act as individual birds that collect and process information about the surrounding environment, but then react in a coordinated way, benefiting the entire organism as a whole.

“Perhaps we give neurons too much importance,” he said. “They are simply excitable cells.” Plants also have their own excitable cells, and many of them are located just behind the growth zone at the root tip. It is precisely in this place that Mancuso and his frequent collaborator František Baluška have discovered an increased level of electrical activity and oxygen consumption. According to their hypothesis, set out in several articles, this “transition zone” could also be the location of the “root brain” described by Darwin. The idea, however, is not proven and is considered quite controversial. “What happens there is not fully understood,” Lincoln Taiz explained to me. “But there is no evidence that it is a command centre.”

What plants are capable of without brains and what Anthony Trewavas calls “mindless mastery” urges us to ask questions also about our own brains and their operation. When I asked Mancuso how plants store and use memory, he expressed the assumption that calcium channels and other mechanisms could be involved, but then reminded me that the location of our own memories is also still shrouded in mystery: “It could be a peculiar machinery, and by finding out how it works in plants, we might perhaps understand it also in humans.”

The hypothesis that intelligent plant behaviour is based on a cellular network that exchanges signals might seem like science fiction, but one must consider that the birth of intelligence in neural networks is not too different. Most neuroscientists will agree: although the brain is considered a command centre for most animals, there is no all-determining core in the brain itself, only a single leaderless network. The confusing feeling when we start thinking about what exactly leads plants, and the realization that there is no one leader or a magician hidden behind a curtain, is just as applicable to our own brains.

In Martin Amis’s 1995 novel “Information” we meet a protagonist determined to write “The History of Progressive Humiliation” – a study in which the displacement of humans from the throne of creation, which began around the time of Copernicus, would be documented. “With every century we become smaller,” wrote Amis. Then came Darwin with the news that we were created by the same laws of nature as animals. During the last century, one by one, the previously strict boundaries that separated humans from animals were blurred – our monopoly on language, reason, tool-making, culture, even self-awareness – and it turned out that other animals are capable of all this too.

Mancuso and his colleagues are writing the next chapter in this “History of Progressive Humiliation”. The goal of their project is to tear down the wall that has so far separated the animal and plant worlds, and this is not a fight only in the field of experiments, but also a fight for words. Let’s start with the elusive word “intelligence”. Especially since there is no prevailing definition (and, as it has turned out, intelligence measurements such as IQ tests tend to be biased by cultural influence), intelligence can be explained both in a way that the boundary between animals and plants is especially emphasized (let’s say, by invoking abstract thinking), and in a way that it almost disappears. Plant neurobiologists have chosen to define intelligence democratically, because, in their view, it is the ability to solve problems, or, more precisely, to react adaptively to conditions, including those that are not provided for in the genome.

“I agree that humans are special,” says Mancuso. “We are the first species capable of arguing about what intelligence is. But what makes us different is the question of the quantity of intelligence, not the quality.” We are part of a whole in which there is a place for both acacias and radishes, and for bacteria. “Intelligence is one of the side effects of life,” he believes. I asked him why, in his opinion, it is easier for people to accept that intelligence is possessed by computers but not by plants. (Fred Sack told me that he was able to accept the phrase “artificial intelligence” because in this case, the meaning of intelligence is changed by the word “artificial”, but he could not accept “plant intelligence”. He didn't cite any arguments, however, only added that he belongs to the majority who think it seems “a little weird”.) In Mancuso’s opinion, we are ready to accept artificial intelligence only because computers are our own creation and reflect our own intelligence. Moreover, they are dependent on us, whereas plants are not: “If we were to disappear from the world tomorrow, nothing would happen to plants, but if plants were to disappear…” Our dependence on plants makes us look at them patronizingly, and, as Mancuso believes, plants “remind us of our own fragility”.

It is even harder to overcome the boundary between the animal and plant kingdoms for “memory” – perhaps because we know very little about it. We are used to thinking about memories as something immaterial, but in animal brains, individual forms of memory tend to form new neural connections. Moreover, there exist biological information storage methods that completely dispense with neurons. Immune cells “remember” experiences with pathogens and refer to this information during subsequent encounters. For plants, it has been known for quite some time that experiences such as, for example, stress alter the molecular structure around chromosomes, and this in turn determines which genes will be “silenced” and which will be “activated”. This so-called “epigenetic” effect can be very persistent and sometimes be passed on to subsequent generations. Quite recently, scientists discovered that life events such as trauma or famine also create epigenetic changes in the brains of animals (for example, by encoding an increased level of cortisol), and these can be so lasting that they are passed on to descendants as well. It is a form of memory similar to which is observed in plants.

Talking with Mancuso, I had to think about words such as “will”, “choice”, and “intention”, because he applied them to plants so naturally, as if they were capable of acting consciously. He also told me about a parasitic vine, the dodder, which tends to wrap itself around the trunk of another plant and feed on its sap. This vine tends to choose its victims by scent, determining which one will be able to provide more nutrients. When a victim is chosen, the vine performs a peculiar cost-benefit calculation, deciding how many coils it should invest in: the more nutrients in the victim, the more times it wraps around the victim. This prompted me to ask Mancuso whether attributing intentions to plants should be perceived metaphorically or literally.

“Come, I will show you something,” he then said to me. “And you yourself will be able to say whether plants tend to have intentions.” He turned his computer screen towards me and clicked on a video.

Time-lapse images are, most likely, the best way to overcome the time difference that exists between plants and humans. The video showed a bean sprout that had been photographed in laboratory conditions every 10 minutes or so for several days. At a polite distance stood a metal rod fixed in a stand. The bean was “looking for” something to cling to. I had observed the same process in my garden every spring and in real-time. I had simply assumed that bean seedlings stretch out at random until they finally reach something to climb up. But, as could be seen in Mancuso’s video, it looked as if the bean “knew” where the metal rod was, a good while before reaching it. Mancuso allows for the idea that the plant uses something related to echolocation. There is evidence that as plants grow, their cells tend to produce low-frequency clicking sounds, and perhaps they are able to sense these sound waves when they bounce off a metal rod.

The bean sprout wastes neither time nor energy “searching” or growing at random, but only towards the rod. And it tries (there really is no other word) to get to it – reaching, bending, repeatedly throwing itself forward and stretching longer with every attempt, and all this just to wrap its curled tip around the rod. Once it has succeeded, it seems as if the plant relaxes, its crinkled leaves start to straighten out. This could all be just an illusion created by such a video. And yet, watching the clip, an example from science fiction, which was so significant for Mancuso, instantly surfaces in memory, because it seems as if it has been possible to look into a time dimension where these previously seemingly inert creatures suddenly come to life and perhaps even become seemingly conscious individuals with their own motives for action.

In October, I downloaded this same video to my laptop and drove to Santa Cruz to visit Lincoln Taiz. He started by questioning the scientific value of such a video. “Maybe there are 10 other videos where the bean does no such thing. You cannot take one interesting variation and turn it into a generalization.” In other words, the bean’s behaviour was to him just an anecdote, not a phenomenon. Taiz also pointed out that already at the very beginning of the video, the plant is bent in the direction of the rod. Then Mancuso sent me another clip with two exemplarily straight beans that behaved in exactly the same way. Now even Taiz seemed intrigued. “If he manages to observe this again and again, it becomes exciting,” he said, but that would not yet be proof that the plant possesses intentions. “If such a phenomenon really exists, it should be classified as tropism,” or a mechanism related to what makes plants bend towards light. In this case, however, the stimulus remains unknown, but for explaining tropisms “there is no need to attribute intentions to plants or look for conceptualization similar to brain activity,” Taiz said. “Proving something like that would then fall on Stefano’s shoulders.”

Probably the most uncomfortable and disturbing word when thinking about plants is “consciousness”. If consciousness is defined as inward-facing self-awareness, while simultaneously grasping reality, or, as neuroscientist Antonio Damasio says, “feeling what happens,” we (most likely) can safely assert that plants do not possess such a thing. But if we define it simply as a state of wakefulness and awareness of one’s surrounding environment, or being “in the network,” as neuroscientists would say, plants can be viewed as conscious beings – at least according to Mancuso and Baluška. “The bean clearly knows what is in its surroundings,” explained Mancuso. “We don’t know how. But that is one of the signs of consciousness. You are aware of your place in the world. A stone is not aware of any such thing.”

To support claims that plants are aware of their environment, Mancuso and Baluška point out that plants, just like animals, are also affected by anaesthetics: certain preparations cause a state in plants that resembles sleep. (A slumbering Venus flytrap will not even notice an insect that has landed on it.) When plants themselves are injured or have ended up in a state of stress, they are able to produce ethylene, which has an anaesthetic effect on animals. When I first heard about this disturbing fact from Baluška in Vancouver, I cautiously asked whether he meant by this that plants are capable of feeling pain. Baluška, who has a rather harsh appearance and a head shape that resembles a large sphere, raised one eyebrow and cast a look at me that, as I thought, could only mean that my question seemed absurd and out of place to him. However, it was not.

“If plants are conscious, yes, they must be capable of feeling pain too,” he said. “If you don’t feel pain, you ignore danger and don’t survive. Pain is significant for adaptation.” He must have noticed my confusion. “Yes, it is a frightening thought,” he confirmed and shrugged his shoulders. “Because we live in a world where we must eat other organisms.”

Not being ready to count on the ethical consequences that would be brought by the realization that plants possess intelligence, I felt doubts strengthening in me against the whole idea as such. Descartes, who believed that consciousness is possessed only by humans, could not accept the idea that other animals could also feel pain. So he considered their screams and wails as merely reflexes, an insignificant physiological noise. Could we now, even only remotely, be making the same mistake about plants? Could the scent of jasmine flowers and basil or the smell of freshly cut grass, which seems so sweet to us, be (as ecological chemist Jack Schultz loves to say) a chemical equivalent of a scream? Or perhaps with just such a question alone we are once again rolling back into the muddy waters of “The Secret Life of Plants”?

Lincoln Taiz is not excited by the idea of plant pain, and he asks what, if there is no brain, could provide such sensations. He puts it concisely: “No brain, no pain.” Mancuso is more cautious. We cannot be completely sure whether plants are capable of feeling pain and whether their attitude towards injury is identical enough to that possessed by animals so that it could be called by the same word. (Both he and Baluška are cautious enough and use the term “pain perception characteristic to plants”.) “We simply do not know it, so one must remain silent about it.”

Mancuso believes: since plants are sensitive and intelligent beings, it is our duty to treat them with a certain respect. This means protecting the plant habitat from destruction, avoiding actions such as genetic modification and monoculture farming, as well as the training of bonsai plants. However, this does not exclude the possibility of eating plants. “Plants have evolved with the goal of being eaten, it is part of their evolutionary strategy,” he explained. To support this thought, he mentioned their modular structure and the absence of irreplaceable organs.

The most essential question on which plant neurobiologists and their critics disagree could be this: does intelligence, the sensation of pain, learning ability, and memory require a brain, as the critics of the idea claim, or can it all be viewed separately from their neurobiological foundations? The question is both philosophical and scientific, because the answer depends on how these concepts are understood. Proponents of the idea of plant intelligence object that the understanding of these concepts is anthropocentric – and that is a witty comeback against those who tend to accuse them of anthropomorphism. Their efforts to expand the understanding of these concepts are also helped by the fact that many of them do not have one specific definition. At the same time, it must be taken into account that these words were introduced to describe the animal world, and therefore it is no wonder that when talking about plants, they sometimes sound weird. It seems that if plant neurobiologists were to attach the caveat “plant-specific” in front of intelligence, learning ability, memory, and consciousness (as Mancuso and Baluška were ready to act in the case of pain), at least a part of this “scientific dispute” would disappear as if it had never existed.

In reality, one can see more consensus in the science standing behind it all than one might expect. Even Yale University biologist Clifford Slayman, who in 2007 signed the letter directed against plant neurobiology, is ready to admit that although in his opinion plants do not possess intelligence, they could nevertheless be capable of “intelligent behaviour”, similar to how bees or ants are capable of it. In an email letter, he expanded on this thought: “We do not know what constitutes intelligence, we can only observe and evaluate intelligent conduct.” By “intelligent conduct” he considers “the ability to adapt to changing conditions” and adds that it “must always be evaluated according to each specific environment”. Humans may or may not be more intelligent than cats, he wrote, but the moment you deal with a mouse, the cat will clearly turn out to be intellectually superior.

Slayman also acknowledged that intelligent conduct can develop well enough even without a central nervous system, or a command centre like a brain. “Instead of a “brain”, think of a “network”.” “It seems that many highly developed organisms are so arranged that local changes, for example, the adaptation of roots to the groundwater level, trigger very local reactions that nevertheless benefit the entire organism as a whole.” In this sense, the views of Mancuso and Trewavas “generally coincide with my understanding of biochemical and biological networks”. He also pointed out that although the human desire to search for a “nerve centre” model everywhere is understandable, we ourselves also have a second and autonomous nervous system that operates, for example, digestion and “operates most of the time without interference from above”. The brain is thus only one of the ways in which nature deals with complex tasks created by the surrounding environment. And it is not the only way. “Yes, I could agree that intelligent conduct is one of the fundamental characteristics of life.”

By placing both plants and animals under the same semantic umbrella because they possess either intelligence or learning ability, we arrive at the meaning of appropriate concepts, and that is a philosophical choice that significantly influences the place we assign to ourselves in nature. Ever since the moment “The Origin of Species” was published, we have at least understood with our minds that we are part of a common continuity of nature – we are all cut from the same cloth of nature. However, our large brains and, perhaps, our experience of introspection create an illusion that we could be fundamentally different – suspended above nature and other species in some kind of metaphysical “skyhook”, if we borrow the formulation of philosopher Daniel Dennett. Plant neurobiologists are determined to take this hook away from us, thereby concluding the revolution started by Darwin, which psychologically at least has not yet ended.

“Darwin showed us that knowledge comes before understanding,” said Dennett, when I called him to talk about plant neurobiology. By laying the simplest knowledge as a foundation – such as an on-and-off switch in a computer or electrochemical signals in cells – it is possible to develop higher and higher levels of knowledge, until finally you arrive at something that starts to resemble intelligence. “The idea that there exists a clearly drawn line, on one side of which is real understanding and real reason, and on the other side plants and animals, is now an archaic myth.” Claiming that such higher-level knowledge as intelligence, ability to learn, and memory “means nothing if there is no brain,” in Dennett’s view, is “brain-centrism”.

All species have to deal with one and the same existential tasks – food must be obtained, one must defend oneself, and reproduce – but this happens in extremely different conditions, and therefore extremely different tools have been created for survival. The brain turns out to be useful for beings that move around a lot, but it has no advantages if you are rooted in one place. Although impressive, self-awareness is also just another survival tool, which will be useful for some functions but will help nothing for others. The fact that humans value this tool so highly is not surprising, because in our long evolutionary journey it has been the target shining in the distance, which has also brought along the side effect of self-awareness that we call “free will”.

Lincoln Taiz is not only a plant physiologist – he also tends to write about the history of science. He said that “already starting with Darwin’s grandfather Erasmus, there existed a teleological direction in plant biology,” the proponents of which have sought a goal or intention in plant behaviour. I asked Taiz about the question of choice, or the plant’s ability to make decisions when they must choose between two conflicting environmental signals, for example, between water and gravity.

“Does the plant choose just like we do when we have to choose between a beef sandwich and a bagel with salmon at a buffet?” Taiz asked in return. “No, because the plant’s reaction will be entirely dependent on the flow of the plant hormone auxin and other chemical signals. In the plant context, the word “decision” does not fit, because a decision implies the presence of free will. Of course, someone can object that even humans have no free will, but that is a different question.”

I also asked Mancuso whether, in his opinion, plants are able to choose just like we do, choosing between a beef sandwich or a bagel.

“Yes, it happens very similarly,” Mancuso wrote to me, although it turned out that he knows nothing about beef sandwiches. “Simply put ammonium nitrate instead of the sandwich (whatever it might be), and phosphate instead of salmon, and the roots will make a decision.” But don’t the roots then just react to a specific chemical substance? “I am afraid that in our brains, decisions are made in exactly the same way.”

The late ethnobotanist Tim Plowman would have asked: “What business does a plant have with Mozart?”, when asked about the wonders described in “The Secret Life of Plants”. “And, even if it did, should we be surprised by it? They are able to feed on light, and is that not enough on its own?”

One of the ways to think about plants is to look for their similarities to animals. But one can also concentrate attention on everything they are capable of but we are not. Some plant intelligence researchers have asked the question whether the emphasis on “animal-centrism” and obsession with “neurobiology” might be a mistake and whether plants are being harmed in this way. “I have not the slightest interest in turning plants into little animals,” one of the researchers wrote at the time when the name of the society was being decided. “Plants are unique,” wrote another. “There is no reason to… consider them as sub-animals.”

When I met Mancuso at dinner during the Vancouver conference, he already sounded like a plant researcher whose “brain envy” is gradually passing – Taiz’s words had inspired plant neurobiologists. If we were able to start understanding plants according to their own rules, he said, it would be “like coming into contact with an alien culture. But we would have only advantages and no problems in these contacts, because this culture would not desire our demise!”. How are plants capable of so many wonderful things without a brain? Without movement? By paying attention to the uniqueness of plants, rather than similarity to other beings, we could learn a lot of new things and develop significant new technologies. That was the topic of his lecture the next morning at the conference, when he was scheduled to speak about “bio-inspiration”. How can plant intelligence help us create better computers, robots, networks?

Mancuso was about to start cooperation with a prominent computer scientist to create a plant-based computer, in which distributed computing would operate according to the same principles that thousands of rootlets use when processing a huge amount of environmental variables. His collaborator was the Director of the International Centre of Unconventional Computing, Andrew Adamatzky from the University of the West of England, who had previously worked a lot with slime moulds, studying their orientation and problem-solving abilities. (Adamatzky’s slime moulds, which are a peculiar type of amoeba, tend to grow towards several food sources – usually, these are oat flakes – simultaneously, in this process calculating and memorizing the shortest possible paths; he has already used these organisms in transport network modelling.) In an email, Adamatzky said that in biological computing, plants, compared to slime moulds, have both advantages and disadvantages. “Plants are much rougher,” he wrote, “and are able to maintain their shape for a longer time”, but they grow more slowly and lack the flexibility of slime moulds. However, since plants are already effectively “analogue electronic computers” that engage in pulse input and output, he hoped that he and Mancuso might manage to get them to perform computational tasks as well.

Mancuso also collaborated with Barbara Mazzolai from the Italian Institute of Technology in Genoa. She is a biologist who has turned to engineering, and together they were about to create a robot that would operate according to plant principles. “If you look at the history of robots, they have always been built in the likeness of animals: they are either humanoids or insectoids. If you want it to swim, it must look like a fish. But what if you tried to imitate plants? What would that allow you to achieve? It is still an unploughed field!” With funding received from the European Union’s Future and Emerging Technologies program, their team is working on a “robotic root” that will be able to lengthen itself with the help of hardening plastic and will slowly bore through the soil, assess its conditions, and be able to change its trajectory accordingly. “If you want to study other planets, it will be wisest to send plantoids to them.”

The most inspiring part of Mancuso’s bio-inspiration lecture was that in which he discussed the underground networks created by plants. Referring to research conducted by University of British Columbia forest biologist Suzanne Simard and her colleagues, Mancuso showed on the screen how in a forest, trees tend to form organized networks under the soil surface through the intermediary of mycorrhizal fungi, along which they exchange not only information but also nutrients. This “wood-wide web”, as it was named in one of the papers, allows trees to exchange warnings about pest attacks, as well as share reserves of carbon, nitrogen, and water when necessary.

When I called Simard, she described how she and her colleagues tend to track the movement of nutrients and chemical signals along the invisible underground network. They inject carbon isotopes into spruces and, with various measuring devices, for example, Geiger counters, follow their spread throughout the entire forest community. One can observe that within just a few days, radioactive carbon reserves have been moved from some trees to others. Within a 30-metre radius, absolutely all trees are connected to this network. The oldest trees in such networks act as data processing centres, and they can have as many as 47 connections with other trees. The diagram of the forest network resembles an airline route map.

Nutrient distribution routes have allowed us to see how “mother trees” try to feed those left in the shade through the network, until they have grown tall enough to be able to catch light. But trees also take care not only of their own offspring in this way, which they apparently are able to perceive as relatives, but even of representatives of other species. A stunning example of inter-species cooperation was spruces that, with the help of a fungal network, supplied nutrients to a birch stand. Evergreen trees tend to take care of those that shed their leaves in winter, and are later repaid with similar care. Underground economic cooperation in the forest community, as it seems, is aimed at collective benefit, maximum use of photosynthesis, and better chances of collectively resisting difficulties.

In his lecture, Mancuso showed side-by-side an image of this underground forest network and a schematic internet diagram and allowed it to be inferred that in many respects the former is superior to the latter. “Plants are able to create scalable, autonomous, self-managed and operated networks,” he said. “Plants.”

Listening to Mancuso’s narrative about the wonders that occur under our feet, I realized that plants truly possess a secret life, but it is much more impressive and unusual than the one about which Tompkins and Bird wrote. In most cases, when we think about plants, if we think about them at all, we think of them as something very ancient – as evolutionary messengers from the times of an ancient pre-civilization world. But in Mancuso’s understanding, plants are the key to the future, at the centre of which are networked, decentralized, modular, and green systems and technologies, which, moreover, are capable of feeding on light. “Plants are an excellent symbol of modernity,” or at least they should be, because their lack of brains turns out to be their strength, and, perhaps, this aspect is the most inspiring thing we should be learning from plants.

At dinner in Vancouver, Mancuso said: “After you visited me in Florence, I found this Karl Marx quote, and ever since then it has not left my mind: “All that is solid melts into air.” Whenever we build something anew, the source of inspiration is the architecture of our own body. Therefore, it tends to have a rigid structure and a center, but such a construction is extremely fragile. That is also the meaning of this statement – “all that is solid melts into air”. And therefore it is worth asking the question: “Are we able to imagine something completely different, something that would have been inspired by plants?””
© The New Yorker, December 23, 2013
Translated by Pauls Bankovskis

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