The tobacco plant Nicotiana attenuata has a love-hate relationship with the hawkmoths that visit its flowers every night. The moths pollinate the plant, but they also drop off eggs that hatch into very hungry caterpillars. Now ecologists have found that when a tobacco plant is being clobbered by caterpillars, it shifts the time of day its flowers open. That makes it more appealing to hummingbirds, a more benign pollinator that doesn't eat leaves.
Ecologist Danny Kessler noticed the change in flowering time in 2008. He works at the Max Planck Institute for Chemical Ecology in Jena, Germany, but does his field studies in Utah, where the plant, a wild relative of cultivated tobacco, grows. That summer, he was trying to get a picture of the plant being pollinated for a study that was about to come out  in Science--one good enough for the cover of the journal. "I noticed that the flowers really looked different in the morning." And there were a lot more of them. N. attenuata normally flowers at dusk and leaves its flowers open until 9:00 or so the next morning, but these plants were opening new flowers in the morning. "That's not supposed to happen," says Kessler's colleague Ian Baldwin, an ecologist at the same institute.
The population of plants that Kessler was photographing was also heavily infested with caterpillars. So he, Baldwin, and colleagues set out to discover whether the change in flowering time was a response to being eaten. He put caterpillars on plants that had not been attacked and found that after 8 days, 35% of their flowers opened in the morning--compared with 11% on unmolested plants. Plants responded the same way when Kessler wounded the leaves and put caterpillar spit on them.
The team also studied the morning-opening flowers themselves and found that they were more likely to be attractive to hummingbirds: they emitted less of a chemical that attracts moths; they had less sugar in the nectar, which is the way hummingbirds prefer it; and they were more tube-shaped, making them friendly to a hummingbird's long, thin beak. The results  appear online today in Current Biology.
"What this tells you is that these plants are hyper aware of being attacked by these particular caterpillars. They're changing a very large proportion of their operating machinery," says Baldwin. This response joins a whole suite of plant countermeasures against herbivores, from producing toxins to sending sugars to the roots instead of making new leaves. Flower shape and timing of opening are usually thought of as being set by genetics, adds Jeffrey Conner, an ecological geneticist at Michigan State University's Kellogg Biological Station in Hickory Corners who was not involved in the study. Instead, he says, the results suggest that plants have leeway on how they make their flowers, depending on environmental conditions.
Ecologist Ted Turlings of the University of Neuchâtel in Switzerland calls the study "very elegant." But he points out one missing piece: The work doesn't show that shifting to morning-opening flowers actually decreased herbivory. Kessler says he couldn't show that because 2009, when he did the experiments, happened to be a year without many hawkmoths; he hopes to repeat the experiments.
In terms of applications, Baldwin says that the work indicates that we should think more broadly about how to fight agricultural pests. "We typically deal with attack in our agricultural plants in a fairly simple-minded way: Spray a poison. Kill the bugs," he says. This study suggests that there may be other ways to deal with the problem--making a plant less attractive to the mothers of the predators, for example.