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March 13, 2012

Parasite Manipulation of Host Behavior (Image 9)

A view of coffee plants (foreground), with forest patches relegated to the hilltops (background).

David Hughes, an assistant professor of entomology and biology at Pennsylvania State University, and his research team has been studying parasite manipulation of host behavior in tropical carpenter ants in rainforests in Thailand, Australia, Ghana and Brazil. The area of Atlantic Rainforest of Brazil where he recently discovered four new species (with Professor Harry Evans of CABI) is one of 24 biodiversity hotspots across the planet, and the one most impacted, with 92 percent of the rainforests having been destroyed. Many cash crops such as coffee are grown (foreground) with the forest patches relegated to hill tops (background). Hughes is now beginning to study the effect of global warming on such fragments with his colleague, Professor Sérvio Pontes Ribeiro of the Universidade Federal de Ouro Preto. (Date of Image: February 2010-2011) [Image 9 of 11 related images. See Image 10.]

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David Hughes has been studying tropical carpenter ants (Camponotus leonardi) infected with the parasitic fungus Ophiocordyceps unilateralis in rainforests around the world.

Fungi are an important group of ant parasites in tropical forests, where ants make up almost 70 percent of individual insects. But the hygienic behavior of worker ants prevents the fungal life-cycle from being completed inside the colony, since the fungus must grow from the bodies of dead ants. If a dead ant is discovered by the workers, it is quickly removed, then dumped far away from the colony before the fungi can reproduce. The O. unilateralis fungus has overcome this obstacle, evolving to manipulate its host for the purpose of boosting reproductive success.

When an ant is infected with O. unilateralis, the invasive fungus manipulates the ant's behavior--making it zombie-like--and causing it to descend from the colony in the hot, dry rainforest canopy, down to the humid understory about 9 or 10 inches above the soil. The cool, moist conditions of the understory make it optimal for fungi reproduction.

When the ant reaches the understory, Hughes and his research team found that when the sun is strongest (around noon), the fungus synchronizes the behavior of the infected ant, forcing it to bite into the main vein on the underside of a leaf on the north/northwest side. When the ant bites down, his jaw locks in a grip that cannot be released, even after death.

As the fungus grows, an orange-colored tube emerges that runs the length of the ant's body. In the ant's abdomen, a big black ball of fungal tissue grows and white threads, called hyphae, spread through the rest of the body. Within 24 hours after death, the hyphae began to emerge from the ant, giving it a fluffy appearance. Some of the hyphae extend out to the leaf, essentially sealing the ant in place. Around the second day of infection, the fungus grows a white to pinkish-colored stalk, or stroma, that begins pushing out of the ant's head. The entire ant becomes covered in a dense matt of hyphae and the stroma grows to be twice as long as the ant itself. During the three to nine days it takes to complete this cycle, the fungus will first produce asexual spores and then sexual spores, which it will discharge from the stroma and rain down over a space of ground about a meter square. The cycle will be repeated when another hapless ant wonders by and comes in contact with the spores.

The understory location plays a key role. Hughes experimented with moving infected ants higher up in the rainforest canopy, and found that the fungi grew abnormally and never fully developed. He also tried moving the ants lower--on the ground, but here the ants either disappeared (probably eaten by predators) or were washed away by rain.

To determine how the fungus affects the ants internally, Hughes used transmission-electron and light microscopes to look inside their bodies. He discovered that the growing fungus fills the ant's body and head, causing the muscles to atrophy and muscle fibers to spread apart. Multiplying fungal cells in its head cause the fibers within the muscles that open and close the ant's mandibles to become detached. This is why the ant cannot release its grip on the leaf and dies in a death grip. The fungus also affects the ant's central nervous system.

"The fungus attacks the ants on two fronts: First, by using the ant as a walking food source, and second, by damaging muscle and the ant's central nervous system," Hughes said. "The result for the ant is zombie walking and the death bite, which place the ant in the cool, damp understory. Together these events provide the perfect environment for fungal growth and reproduction."

Hughes' believes his research in this area may be useful in the future to help control pest insects in homes and on farms.

Credit: David Hughes, Department of Entomology and Biology, Penn State University

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