No brainer behavior

Messages, memory, maybe even intelligence — botanists wrangle over how far plants can go

In a somewhat different world, Consuelo M. De Moraes would be revolutionizing vampire fiction.

ACTIVE VEGETATION Plants move. Time-lapse photography reveals the circular sweep of a Lonicera japonica vine during two hours of growth. But an evolving definition of plant behavior doesn’t even require motion. It turns out, plants behave in myriad, often-hidden ways. Ash Kaushesh and Katherine Larson

FAST EATER The delicate-looking swollen bladderwort, Utricularia inflata, can kick into action quickly. An unsuspecting bug that finds its way to one of the underwater plant’s traps (shown above) will be sucked in through a trapdoor. Barry Rice/

ROOT WARRIOR Exposed to a secretion from an invasive knapweed, the root of a blanketflower within an hour responds with its own secretion (right, shown as gel acidifies and turns yellow). At left is an unexposed root. Tiffany Weir et al./Planta 2006

Her lab at Penn State University studies predators that entangle prey in a tight embrace, pierce victims’ tissue and suck out nourishment. In the last few years, De Moraes and her colleagues have found that the predators even hunt down prey by scent.

Creepy as her predator, Cuscuta pentagona, is, it is also, frankly, a plant. Better known as five-angled dodder, its orange tentacles bypass the porcelain throats of young women in favor of the slim stems of young tomato plants. De Moraes and other researchers are showing that plants behave and misbehave as dramatically as animals. But there’s still not much hope for a feature-length dodder movie.

“I think most people regard plants as being pretty unresponsive and stuck in one place,” laments ecologist Richard Karban of the University of California, Davis. “Now, animals, they’re interestingbecause they can change and act in response to their environment.”

It’s a dichotomy Karban doesn’t accept for one second. When he and an animal behaviorist recently supervised a grad student, he remembers, “I would constantly want to say, ‘Oh yeah! Yeah! Plants do that too!’” Recent findings on plant capacities, he declares in a 2008 paper in Ecology Letters, reveal “high levels of sophistication previously thought to be within the sole domain of animal behavior.”

Even plants less vampirish than Cuscuta vines forage strategically for their food, and there’s evidence that plants fight each other over resources. In a broad sense of the word, plants communicate — some essentially scream for help. Also, a plant can respond to stimuli depending on its history of previous experiences, a tendency Karban is willing to call a sign of memory.

Karban stops there, but other plant scientists go much further in borrowing animal terminology. In May, researchers gathered in Florence, Italy, for their fifth annual meeting on “plant neurobiology,” and some of these green neuroscientists talk about searching for a plant “brain.” The June issue of Plant, Cell & Environment, devoted to plant behavior, even begins with a paper that uses the term “plant intelligence.”
Expanding the language for describing plants to include at least some “behavior” words could expand ideas for research, Karban contends. Plant researchers might do well to borrow analytic techniques from animal scientists, he adds. Finally, everyone may discover just how exciting it can be to watch grass grow.

Movement in animal time

One of the first questions posed to believers in plant behavior is, “How can plants behave if they can’t move?”

Part one of plant behaviorists’ almost universal answer: Plants do move.

Time-lapse photography of growing shoots reveals spooky, circular sweeps called nutation. The circular motion arises because a shoot does not necessarily grow evenly, with cells on one side elongating as fast as cells on the other. Growth rate varies on different sides. Over hours or days, the growing tip moves like a turning searchlight.

And as plant scientists relish pointing out, some plants do move in animal time, especially those that hunt animals for food. When it lands inside the open jaws of a Venus flytrap, a fly may jog trigger hairs. An electrical signal zaps through the plant tissue and the two sides of the trap can close like a book in less than a second. And a water flea that bumbles into a little cup of a bladderwort likewise confronts the peril of touch-sensitive triggers. A trapdoor opens within 30 milliseconds, and the flea whooshes down into a digestive chamber.

No insects are harmed when white mulberry trees bloom, but the Morus alba flowers open with a quick puff of yellow pollen. In a lab setup, a team of aerosol specialists at Caltech found the mulberry flower’s parts moving at speeds exceeding Mach 0.5. Pollen flinging could thus be the fastest biological movement yet observed, the team reported in 2006, and team member James House says he’s not aware of any challenges since.

But while plants trap and snap with boastable speeds, the second theme of a typical plant scientist’s comments about motion is that it doesn’t really matter in defining behavior.

Motion seems an unfortunately strict requirement, even for animal behavior, says Jonathan Silvertown of the Open University in Milton Keynes, England. He studies plant communities, and in 1989 worked with animal behaviorist Deborah Gordon, now at Stanford University, to outline a framework for defining plant behavior. A hedgehog playing dead is certainly behaving, they wrote.

Still behavior

“Behavior,” they proposed, applies to “what a plant or animal does, in the course of an individual’s lifetime, in response to some event or change in its environment.” This concept does not include intent, the team wrote, and Karban concurs. “Even in people, determining intent is very difficult,” he says.

This motion-free, intent-free definition allows the concept of behavior to embrace an activity in which plants excel: releasing chemical bursts, says plant community ecologist Kerry Metlen of the University of Montana in Missoula. Plants secrete secondary metabolites, chemicals that go beyond the basics of metabolism. These substances can prospect for food, wage war and call for reinforcements, all the while gossiping in chemical detail. “Plants are prodigious chemists,” Metlen says.

These chemical doings also show two other qualities that Metlen requires for plants behaving. A behavior should start relatively fast and it should be reversible, he and his colleagues contend in the June Plant, Cell & Environment.

Fighting tooth and chemical

Consider foraging, Metlen says. Iconic scenes of animal behavior star cheetahs streaking toward an antelope lunch. Underfoot, it turns out, the plants are hunting too, just by different means.

In a very basic sense, plants hunt by sending out roots. Decades of research have established that plants are strategic, allotting root growth to the promising patches and skimping on dead zones.

Plants also have their version of the cheetah pounce, but it’s chemical. Metlen’s favorite example, he says, comes from a study of fava beans by Long Li at China Agricultural University in Beijing and a network of colleagues. Like other plants, the beans need phosphorus. When researchers put the plants in phosphorus-poor agar gel, the beans took “action.” They acidified the material around their roots, causing malate and citrate concentrations in the agar to increase in such quantities that the gel’s pH dropped by about two units within six hours. Driving down soil pH increases plants’ phosphorus uptake, so chemically those bean roots were chasing and grabbing the food they needed.

One plant Metlen is studying now, spotted knapweed, adds a root-war twist to the chemical-pounce scenario. Back in its native Eurasian range, Centaurea maculosa grows here and there as an occasional member of mixed-plant communities. Its roots exude a substance called catechin, which makes phosphorus more available in certain soils.

Spotted knapweed has moved to North America. Where it once had an occasional presence, it is now a land grabber. Knapweed blankets entire slopes and pushes out native vegetation. One of the secrets for its new success may be the catechin. European neighbors of knapweed don’t seem bothered by catechin seeps, but some North American species can’t cope. A handy dietary aid has turned into an invader’s chemical weapon.

It’s root versus root, and research, including a 2006 Planta paper, suggests that some native species fight back, chemically of course. A lupine and a blanketflower can still grow when knapweed erupts in the neighborhood. Expose the two species to catechin and their roots exude extra oxalate, four times the normal level for the blanketflower and 40 times normal for the lupine. The oxalate may defang the catechin, with protection extending beyond the blanketflower and lupines to other native species growing near enough.

Volatile messages

It’s not neighboring plants but insects that come to the rescue when a plant cries for help. Karban, in his 2008 paper, argued that these behaviors amount to a plant version of communication.

When mites or caterpillars bite into leaves or stems, the attacked plant releases volatile compounds. It’s not just that sap dribbling from an open wound happens to have a scent. In corn, for example, insects boring into the stem prompt leaves to release complex blends of volatile chemicals.

Blends include a lot of information. Some plants enduring the indignity of a researcher snipping their leaves will release volatiles, but not of quite the same aroma as when caterpillars bite.

Some of the insects that prey on other insects react to these volatiles, swarming to the attacked plant to dine on the attackers. Research has found that certain of these ambulance-chasing predators respond selectively, flying toward the aromatic news of pests they prefer to eat while ignoring aromas from attacks by species they don’t fancy. For example, a little wasp that can only manage to inject its eggs into young caterpillars reacts to volatiles of plants under the attack of such tender youngsters. But the wasp doesn’t respond to volatiles from infestations inflicted by older caterpillars.

Neighboring plants can eavesdrop on the volatile signals too, and some respond by priming their own defenses.

Karban is willing to use the term “communication” for these chemical outbursts. He acknowledges, however, that strict definitions of communication demand that both the cue-emitter and the receiver benefit from the exchange. Plant volatiles that bring insect rescue may fit even this tougher definition, he says.

Remember me?

Warfare, chemical or otherwise, changes surviving plants much as it might animal survivors, according to research on the phenomenon of priming.

A poplar leaf once scarred by insect attack kicks its defense genes into high gear faster during the next attack than a naive leaf does, says De Moraes. “Memory comes with so much baggage,” she says, so she uses the term priming or preparedness. Karban, among other researchers, does compare this effect of past experience in plants to memory in animals.

And De Moraes’ work shows that even a rumor of war can create a state of preparedness in a naive leaf. The way poplars’ internal plumbing system is structured means that a leaf does not have a direct connection to its immediate neighbor. When De Moraes experimentally “attacks” leaf number one, volatiles waft to near neighbors, and those volatiles can constitute gossip about the nature of the attacker. Should she challenge those neighbors later with their own crisis, they rev up their defense genes faster than does a leaf prevented from receiving the informative volatiles. Biochemical gossip has its value.

That warnings waft over a plant’s own leaves may help explain how the volatile cues evolved, De Moraes says. Biochemical messages benefit the gossiping plant itself, rather than just its neighbors.

Neighboring plants may be listening in, but perhaps the wounded plant is getting big benefits just from talking to itself, De Moraes says. And plants may be able to distinguish self from nonself, according to Karban’s current research effort. He is  finding evidence that a sagebrush plant shows signs of distinguishing its own airborne signals from those of other sagebrushes. A sagebrush plant that sniffed volatiles from wounded neighbors that are genetically identical to it was more resistant to attack than were sagebrush plants exposed to volatiles from genetically different plants, he and a colleague report in the June Ecology Letters. That plants have some powers of self-recognition opens a new arena of comparisons with animals.

Green neuroscience

De Moraes, Metlen and Karban borrow animal terms moderately, but other plant scientists go much further. Anthony Trewavas of the University of Edinburgh freely uses the phrase “plant intelligence.”

For defining intelligence, he says that “a capacity for problem solving is the best descriptor that I have come across, and problem solving is something all organisms have to do.”

Botanists have already borrowed plenty of other originally human terms, such as arms races, foraging, cross talk and vascular system, even though the plant versions rely on mechanisms that are different from the human ones. People comfortably say computers have memory and can even learn. Trewavas is now working on a book on “plant behavior and intelligence.”

In a similar vein, other plant scientists argue for what they call “plant neurobiology.” In a 2006 manifesto introducing the field to readers of Trends in Plant Science, Eric Brenner of the New York Botanical Garden and five colleagues describe their aim as understanding “how plants process the information they obtain from their environment.” They write that, almost a century ago, researchers reported electrical activity in plant tissues as part of the early explorations of electrophysiology in all living things. Also, the major neurotransmitters in animal nervous systems, including acetylcholine, serotonin, GABA and glutamate, occur naturally in plants.

Figuring out what all of this means for plants is drawing researchers’ attention. “The most important thing is that we’re missing something,” Brenner says.

Applying neurobiology terms to plants has sparked debate aplenty. “I see no reason why one can’t simply talk about signal transduction in plants,” objects David G. Robinson of the University of Heidelberg in Germany.

He also argues that even simple animals can be trained to respond to a stimulus, so he challenges plant neurobiologists to train a plant, perhaps to bend toward yellow light or to avoid blue. “My guess is that neither experiment would work,” he says. His final take on plant neurobiology: “Absolute rubbish, rubbish!”

Plant neurobiology isn’t yet attracting many enthusiasts, says Michael J. Hutchings of the University of Sussex in Brighton, England, who adds that he is not a fan. But he says a wide range of plant biologists do think of their subjects as having some capacity to behave.

Failing to use “behavior” language feeds a notion of “plants as really boring,” as Hutchings puts it. For bringing a more dynamic vision of plants into research and teaching, he says, “It’s about time.”

Susan Milius

Susan Milius is the life sciences writer, covering organismal biology and evolution, and has a special passion for plants, fungi and invertebrates. She studied biology and English literature.

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