Four species communicate with and sometimes trick each other around a scent produced by greening-infected citrus trees, a new University of Florida study finds.

Communication between species is common but almost always is described between two or three species, said Lukasz Stelinski, associate professor of entomology and nematology at the Citrus Research and Education Center in Lake Alfred.

Stelinski wanted know how a fourth species, in this case, a wasp, would vary this interaction ─  a probe that may be one of the few cases where species at four levels of the food chain use one odor to communicate with, and exploit, each other.

Psyllids carry the pathogen that causes citrus greening, which has caused great damage to Florida’s $9 billion citrus industry. Stelinski’s team found that wasps and psyllids are both attracted to the odor emitted by an infected citrus tree. This olfactory cue may then help wasps find and prey on the psyillid by “eavesdropping” on the odor exchanged between bacteria, citrus trees and the psyllid.

The findings were published online by Frontiers in Ecology and Evolution.

Here’s how the interaction works: When host citrus trees are infected, they emit an odor, Stelinski said. That odor, methyl salicylate, makes them smell more appealing to the vector, the Asian citrus psyllid. Lured by scent, the tiny insect goes to the infected tree, searching for sap to snack on.

The hungry psyllid is attracted to the infected tree, even though pathogen-infected trees are less nutritious to psyllids than healthy ones.

 “This may be a mechanism, among many, that encourages the spread of the pathogen,” Stelinski said.

Stelinski’s team brought a wildcard, a wasp, into the mix because it’s a natural psyllid enemy. They wondered whether the wasp is also attracted to the methyl salicylate, as it hunts for psyllids to eat. So they put wasps in an olfactometer, a Y-shaped device that delivers two opposing air flows, each carrying a different odor.

The wasps could fly toward methyl salicylate or to a control odor, limonene, another compound produced by citrus trees. The wasps were strongly attracted by the pathogen-induced scent, methyl salicylate. They later learned the wasp was more likely to attack psyllids on greening-infected plants or methyl salicylate-treated plants rather than healthy plants.

“Biologically, we think it’s very interesting,” Stelinski said. “You to have to look at multiple levels of the food chain. The pathogen is manipulating the plant to attract the good guy and the bad guy. The finding makes the tree look like a beacon in a sea of uninfected trees.”

Stelinksi wrote the paper with Xavier Martini, a postdoctoral associate and Kirsten Pelz-Stelinksi, an associate professor of entomology, both at CREC.