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Calling All Predators: Caterpillar Saliva May Be a Component in Plants' Chemical Alarms

As a tobacco hornworm feasts on a plant, it alters the volatile chemicals emitted by the leaves, thereby betraying its location to natural enemies



Matthey Film

Plants have evolved many direct defenses against herbivores, such as thorns, slippery leaves, lethal toxins and irritating resins. But some plants also employ indirect defenses by releasing chemicals that attract the natural enemies of herbivores. When a caterpillar starts feasting on a tobacco plant, for example, the leaves waft volatile compounds that attract some predatory and parasitoid insects. These predators hunt the caterpillars and their eggs, which benefits the plant by reducing the number of its attackers. Now, researchers have uncovered a surprising secret of plants' chemical cries for help that could yield new ways to fight crop pests .

The two best-studied varieties of these chemical alarm calls—known as herbivore-induced plant volatiles (HIPVs)—are terpenoids and green leaf volatiles (GLVs). Terpenoids are released from the whole plant, not just damaged leaves, often as late as one day after the attack. Researchers know that certain terpenoids attract specific parasitoids to their preferred hosts. In other words, these chemicals send a very clear message to parasitoids: Hey, there's a big juicy herbivore here!

In contrast, GLVs are immediately released from any wounded leaf, regardless of how it was damaged. These volatiles are responsible for the distinctive smell of a freshly mowed lawn, for instance. Researchers had never understood how parasitoids and predatory insects detected the difference between GLVs released by a leaf suffering mere mechanical damage and GLVs emitted from a leaf under siege by an herbivore.

A new study, published August 26 in Science, suggests that leaves wounded by herbivores release a different bouquet of GLVs than mechanically damaged ones do. Furthermore, the findings indicate that the plant does not directly alter its alarm calls—rather, something in the oral secretions of hungry herbivores causes this chemical change. Herbivores betray themselves as soon as they start munching, revealing their locations to any predators in the area.

"There has always been the suggestion that GLVs that immediately come off the plant are attractive to predators, too," explains Andre Kessler, an expert on plant volatiles at Cornell University who was not involved in the new study. "But it was not clear how predators would be able to differentiate between mechanical wounding and herbivore feeding, and this is what the paper resolved completely. It's a really elegant confirmation."

In the new work Silke Allmann of the Max Planck Institute for Chemical Ecology in Jena, Germany, and her colleague studied tobacco plants (Nicotiana attenuata) and caterpillars called tobacco hornworms (Manduca sexta). First, the researchers punched holes in the leaves of tobacco plants and analyzed the volatile compounds they emitted. In response to this mechanical damage, the tobacco leaves consistently gave off a characteristic bouquet of GLVs: Specifically, they released more of one kind of GLV (Z-GLVs) than another (E-GLVs).

In testing the mechanically wounded leaves, the researchers found that applying caterpillar spit significantly increased the level of E-GLVs. Further, when the researchers allowed living caterpillars to feed on the tobacco plants, they measured the same increase in E-GLVS. That is, the leaves of tobacco plants gave off a subtly different perfume when either wounded by caterpillars or exposed to their spit than when the plants suffered mechanical damage.

To test whether predatory insects could actually home in on this subtle difference, the researchers went to the Great Basin desert in southwestern Utah, where they glued tobacco hornworm eggs to the underside of leaves on wild tobacco plants. In the soil beneath these leaves they placed cotton swabs they had dunked in a lanolin paste infused with different proportions of each type of GLV. Some cotton swabs wafted more E-GLVs, which mimicked caterpillar-damaged leaves, whereas others wafted more Z-GLVs, replicating the mechanical damage signal. Then the researchers waited—in particular, for predatory insects known as big-eyed bugs (Geocoris), which pierce caterpillar eggs with a sharp stylet and suck out their juices.

After a day of waiting the researchers found that big-eyed bugs had attacked 24 percent of the eggs on leaves near cotton swabs that predominantly emitted E-GLVs, but only 8 percent of the eggs near the Z-GLV–saturated cotton swabs. "This told us that the big-eyed bug was able to distinguish between Z- and E-GLVs, preferring those that indicated there was a caterpillar," Allmann says.

A final question addressed by the study is how caterpillar saliva triggers plants to emit more E-GLVs. The caterpillar spit itself appears to convert Z-GLVs to E-GLVs, which the researchers discovered through laboratory tests. Furthermore, boiling the caterpillar spit rendered it incapable of performing this conversion, suggesting some kind of protein—perhaps an enzyme—is the key.

"The interesting but unexpected result is that change in GLVs is not activated by the plant, but by the insect's own saliva," Allmann explains. "The insect betrays itself—it calls the police itself." Allmann speculates that tobacco hornworms may convert Z-GLVs to E-GLVs as they eat because some forms of E-GLVs act as antimicrobial agents, which would protect the caterpillars' guts from pathogens on the leaf. But so far she has no direct evidence to support this idea.

Allmann also thinks a more precise understanding of the link between GLVs and insect behavior could benefit crops. "GLVs are produced by just about every type of plant," she says. "There could be a way to engineer alarm calls into all plants, including crop plants—to make all crop plants call the police when they are attacked."

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