“I’ll Fly Away” may be the theme song of some insect species exposed to elevated levels of ozone, according to groundbreaking research by Edward Mondor and his colleagues in the entomology department at the University of Wisconsin-Madison. They are researching the effects of the greenhouse gases carbon dioxide and ozone on insect behavior and physiology.

The research, funded by a three-year NSF grant, was conducted at the Aspen Free-Air CO2 Enrichment Site, a cooperative scientific research station in Rhinelander, Wis., where national and international researchers are studying the effects of carbon dioxide (CO2) and ozone (O3) on a variety of tree, plant and insect species.

Several aspects of the research being conducted in northern Wisconsin are unique. “There are other FACE sites, but this is the largest one in the world,” said Mondor. Before FACE technology was developed, scientists doing similar research were limited to conducting experiments in greenhouses or in open top chambers, said Mondor. But at the site in Rhinelander, they have access to an 80-acre research station with mixed stands of trembling aspen, paper birch and sugar maple, along with a naturally diverse understory. The test trees are planted in a series of a dozen 30-meter rings with vent pipes that release different levels of the gases, based on a computer-controlled trace gas monitoring system.

“Most entomologists are conducting research solely on the effects of CO2,” said Mondor. “At Aspen FACE, we are able to assess the individual and interactive effects of CO2 and O3, associated with global climate change, on insect behavioral and physiological processes.”

And those behavioral changes could alter the balance of predator-prey relationships and the health of forest plants. Mondor, along with co-authors Michelle Tremblay and Richard Lindroth, describe the results of their research in the paper “Transgenerational Phenotypic Plasticity under Future Atmospheric Conditions,” published in the October issue of the journal Ecology Letters.

Aphids, commonly called plant lice, are insect pests that feed on phloem, or plant sap, injecting their saliva into the plant while they suck up its juices. If the infestation is heavy, aphids can severely damage plants. In addition, aphids are carriers of plant viruses, such as soybean mosaic virus, which can cause greater yield reductions than direct insect feeding, said Mondor.

Mondor studied the goldenrod aphid Uroleucon nigrotuberculatum. Most aphids are tiny, but at 4 to 5 mm long, Mondor called this one “the horse of the aphid world.” Like other aphids, the study aphids display what is called phenotypic plasticity – adults can produce offspring of several different body types. In this case, the offspring are born with or without wings, depending on whether there is a heightened threat of predation or parasitism. Offspring that can fly have greater survival chances.

Aphids are eaten by many other insects, including lady beetles, and serve as the hosts for parasitic wasps that lay eggs in them. These beneficial insects help keep aphid populations in check. But aphids have a warning that these insects are in the area. Both lady beetles and parasitic wasps leave search tracks, a trail of compounds that marks their territory, that aphids can detect.

Mondor’s research showed that aphids produced more winged offspring in response to predatory lady beetle search tracks when the carbon dioxide level was elevated and more winged offspring in response to parasitic wasp search tracks when ozone levels were elevated. While the underlying reason for this difference is currently under investigation, it is suspected that aphids are responding to differences in natural enemy search behavior under the different atmospheric conditions.

In a related study, “Divergent Pheromone-mediated Insect Behaviour under Global Atmospheric Change,” in press in the journal Global Change Biology, Mondor and co-authors Michelle Tremblay, Caroline Awmack and Richard Lindroth found that aphids’ dispersal rates, or the number of colony members that flee the scene when they detect predators, are affected by greenhouse gases.

When an aphid is attacked by a predator or parasitoid, Mondor said, it often secretes a carbon-based alarm pheromone that serves as a danger signal to other aphids. When another aphid picks up the scent with its antennae, it disperses by crawling to another part of the same leaf or to a different leaf.

“Since this pheromone is only emitted when they are attacked,” said Mondor, “it is a reliable cue of increased predation risk for the rest of the colony.”

In this study, Mondor and his colleagues studied Chaitophorus stevensis, a small aphid (1 to 2 mm) that feeds on trembling aspen trees. The escape behaviors of the aphids in response to alarm pheromones diverged, depending on the greenhouse gas to which they were exposed.

Mondor suspects that several factors were at play. Under the elevated carbon dioxide conditions, fewer aphids dispersed, perhaps because the carbon dioxide inhibited the ability of the aphids to produce or detect the alarm pheromone. Thus, more aphids would be available for predators to consume. Mondor noted that under enriched ozone conditions, however, 100 percent of the adult aphids dispersed. “Adult aphids exhibited the most extreme reactions,” he said. “They are more mobile and can move farther distances to avoid being eaten.”

Then again, it could be the quality of the leaf’s nutrients. Aphids may be more reluctant to stop feeding, even in response to an alarm signal, when on leaves of higher nutritional quality.

Although research is ongoing, Mondor believes that the responses of aphids and other insects to greenhouse gases could herald future ecological imbalances. “It certainly appears that increasing levels of greenhouse gases have the potential to alter basic ecological processes, such as behavioral responses and phenotypic expression in insects. We can’t help but wonder how these changes will influence the long-term population dynamics of both pest and beneficial insects.”

Mondor’s aphid study was highlighted on the Editor’s Choice page in the Oct. 8 issue of Science.

Aspen FACE is funded jointly by the Office of Science (BER), U.S. Department of Energy; the National Science Foundation; Global Change Program; USDA Forest Service, North Central Research Station; USDA Forest Service; Michigan Technological University; the USDA National Research Initiative Program; Brookhaven National Laboratory; and Natural Resources Canada.