The enemy of my enemy is my friend is an adage that holds true for plants, suggests a study that found that plants rely on chemicals in the saliva of leaf-eating insects to attract predators of those insects.

Max Planck Institute for Chemical Ecology/Danny Kessler Geocoris approaches Manduca eggs and hatchling

Reporting in Science, researchers Ian Baldwin and Silke Allmann from the Max Planck Institute for Chemical Ecology found that something in the saliva of the Manduca sexta caterpillar changes the chemical composition of the distress signal tobacco plants normally produce when they are injured, potentially allowing carnivores in the area to find the feeding caterpillar.

"This adds to a growing list of complicated ways in which signaling happens between insects and plants," Jack Schultz, a chemical ecologist from the University of Missouri who was not involved in the study, said.

When a leaf is wounded, plants immediately release a "bouquet" of distress chemicals known as green leaf volatiles (GLVs) into the air. GLVs are formed when long fatty acid chains in the cell membranes are chopped up into six-carbon molecules as a result of damage. These molecules can exist in two different shapes, or isomers, depending on the position of a double bond between two of the carbons.

When tobacco plants are wounded mechanically, say, with a pair of garden shears, the GLVs they produce exist mostly in one of the isomeric forms. To the researcher's surprise, however, the GLVs released from leaves that were being chewed on by caterpillars contained a great deal more of the other isomer, suggesting something was causing the isomers to switch from one to the other.

It seemed plausible to think that the plant itself was changing the ratio of GLV isomers in response to chemicals in the insect's saliva. Plants are known to respond specifically to biochemical cues in the oral secretions of herbivores, but those kinds of specific responses can take up to a day to kick in. Moreover, when the researchers impaired several pathways of these herbivore-specific responses in tobacco plants, they found it had no effect on the saliva's ability to change the GLVs. This led them to believe that the caterpillar, and not the plant, was responsible for switching the isomers.

"Something in the saliva is actually doing the chemistry work of producing a changed isomer ratio," Schultz said. It was a finding he found totally unexpected, he added.

Baldwin and Allmann then wondered if other insects, in particular carnivores, could use this distinct chemical signature to chemically eavesdrop on their prey. "The GLVs, because they're immediately released, they can provide immediate information and very spatially explicit information," Baldwin explained.

To test whether this was true, they designed an experiment with natural plant populations growing in a field station in the Great Basin Dessert in southwestern Utah. They glued Manduca eggs to leaves and placed cotton swabs drenched in pastes with different ratios of GLV isomers.

After several hours, they checked the eggs for the tell-tale signs of predation by the "big-eyed bug" Geocoris, which pokes tiny holes in the eggs to suck their contents out. They found that more eggs were eaten by Geocoris when the paste next to them contained GLVs with an isomeric ratio similar to the one produced by the saliva of caterpillars.

While these are very promising results, Schultz said the ultimate evidence would come from observing predators actually preying on feeding caterpillars.

So far, it seems this is a unique trait of Manduca, as the saliva of two other caterpillar species did not change the composition of the GLVs significantly.

But why the species would produce a substance that seems to work against it is one of the most puzzling questions to arise from this study. "There is no doubt a function for whatever that enzyme or protein is that we don't know yet," Schultz said.

In the paper, Baldwin and Allmann suggest that GLVs with a higher concentration of the second isomer may have enhanced antimicrobial properties. Therefore making more of the second isomer may come in handy to caterpillar larvae.

Dan Hare, an entomologist at the University of California, Riverside who was not involved in the study, said that if there is variation within the species in the ability to cause this chemical change in GLVs, then investigating whether this trait is under positive or negative selection would offer further insight on the overall effect it has on the caterpillar's well being.

S. Allmann and I.T. Baldwin, "Insects betray themselves in nature to predators by rapid isomerization of green leaf volatiles," Science, 329:1075-8, 2010.


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An Issue Of Growing Import: How Insects Find Food
[19th September 1988]