Eavesdropping plants prepare to be attacked

"One of the things that makes plants so ecologically interesting is that they can't run away," says John Orrock, a zoology professor at the University of Wisconsin-Madison. "You can't run, you can't necessarily hide, so what can you do? Some plants make themselves less tasty."

Some do this either by boosting their production of toxic or unpleasant-tasting chemicals (think cyanide, sulfurous compounds, or acids) or through building physical defenses such as thorns or tougher leaves.

But, he adds, "Defense is thought to come at a cost. If you're investing in chemical defenses, that's energy that you could be putting into growth or reproduction instead."

To balance those costs with survival, it may behoove a plant to be able to assess when danger is nigh and defenses are truly necessary. Previous research has shown that plants can induce defenses against herbivores in response to airborne signals from wounded neighbors.

But cues from damaged neighbors may not always be useful, especially for the first plant to be attacked, Orrock says. Instead he asked whether plants -- here, black mustard, a common roadside weed -- can use other types of cues to anticipate a threat.

In a presentation Aug. 6 at the 2013 Ecological Society of America Annual Meeting in Minneapolis, he and co-author Simon Gilroy, a UW-Madison botany professor, reported that the plants can eavesdrop on herbivore cues to mount a defensive response even before any plant is attacked.

Slugs and snails are generalist herbivores that love to munch on mustard plants and can't help but leave evidence of their presence -- a trail of slime, or mucus. Where there's slime, there's a snail. So Orrock treated black mustard seeds or new seedlings with snail mucus, then tested how appealing the resulting plants were to hungry snails.

The result? Getting slimed made the plants become less palatable. "That shows that plants are paying attention to generalist herbivore cues and that they turn on their defenses before they even get attacked," says Orrock.

What's more, they used the information in a time-sensitive way. Plants exposed only as seeds were eaten more -- evidence of lower defenses -- than those exposed as seedlings.

"The more recently they receive the information about impending attack, the more likely they are to use the information to defend themselves," he says. "Not only do they eavesdrop, they eavesdrop in a sophisticated way."

With Gilroy, Orrock is now exploring the genetics -- and possibly evolution -- of induced defenses. "If selection is strong enough from generalist snail herbivores to drive the evolution of eavesdropping by plants, then it might be far more common than we think," he says.

How did they do that? Collecting snail slime

"It's not easy to get mucus out of a snail," says John Orrock. For one thing, "they make three different kinds."

The UW-Madison zoology professor used snail slime to show that black mustard plants can use cues of predator proximity to trigger defense mechanisms against the hungry snails.

But his first challenge was collecting enough slime to treat the plants. Initially he turned the snails upside down and tapped them, but what bubbled up was just defensive mucus, not the locomotion mucus (or "slime trail") he sought.

Ultimately he devised a low-tech but effective solution: let the snails crawl around overnight on a piece of filter paper lining the bottom of a small plastic deli container, then wash the filter paper and use the resulting slime water to treat the seeds and plants.

"One thing that's so cool about ecology is that you can do really enlightening experiments very simply. Clearly, if you're interested in the molecular or chemical aspects of the question, this isn't going to cut it. But if you want to know if a plant gets paranoid with slime? This," Orrock says, shaking the container, "plus snails equals results."