An invasive weed that has spread across much of the U.S. harms native maples, ashes, and other hardwood trees by releasing chemicals harmful to a soil fungus the trees depend on for growth and survival, scientists report this week in the Public Library of Science. The tree-stifling alien, garlic mustard (Alliaria petiolata), first introduced into the U.S. in the 1860s, has since spread to Canada and 30 states in the East and Midwest, with recent sightings as far west as Oregon.
While many mechanisms -- from the absence of natural predators or parasites to the disruption of long-established interactions among native organisms -- have been proposed to explain the success of invasive species, this new work is the first to show that an invasive plant harms native plants by thwarting the biological "friends" upon which they depend for growth. The work, which provides striking evidence for a unique process by which invaders harm native species, was conducted by researchers at Harvard University, the University of Guelph, the University of Montana, Purdue University, and the UFZ Centre for Environmental Research in Germany.
"While vanishing habitat caused by human activity is the number one threat to biodiversity, there is great concern over the impact of accidental and intentional dispersal of alien invasive species across the globe," says Kristina A. Stinson, a plant population biologist at the Harvard Forest, Harvard's ecology and conservation center in Petersham, Mass. "In North America, thousands of nonnative plants and animals have become established since European settlement and many more continue to be introduced. Some alien species cause little harm, while others can become very aggressive and radically transfigure their new habitat.
"The mechanisms for this phenomenon and its potential long term impacts remain poorly understood," Stinson adds, "but one possibility is that invasive species may disrupt fragile ecological relationships that evolved over millions of years."
Stinson and her colleagues found that garlic mustard targets arbuscular mycorrhizal fungi (AMF), which form mutually beneficial relationships with many forest trees. These fungi have long filaments that penetrate the roots of plants, forming an intricate interwoven network that effectively extends the plant's root system. AMF depend on plants for energy and plants depend on the fungi for nutrients. When tree seedlings, which depend strongly on AMF, began to decline in the presence of garlic mustard, the researchers suspected that the invasive plant might thwart this symbiotic relationship.
To test this possibility, they collected soil from five forests in Ontario dominated by four species of native hardwoods. First, the researchers tested seedlings' ability to form mycorrhizal relationships in soil with a history of garlic mustard invasion. Three species -- sugar maple, red maple, and white ash -- had significantly less AMF root colonization and grew only about one-tenth as fast in the infested soil. Seedlings grown in sterilized, AMF-free soil taken from invaded and pest-free locations showed similar reductions, suggesting that diminished microbial activity had suppressed tree growth. Other experiments showed that adding garlic mustard extracts to soil impaired AMF colonization and seedling growth, implying that the weed uses phytochemical poisons to disrupt native plants' mycorrhizal associations and stunt their growth.
When the study was subsequently replicated with seedlings of 16 other native plants, only the hardwoods and other woody plants were harmed by the presence of garlic mustard.
"This suggests garlic mustard invades the understory of mature forests by poisoning the allies of its main competitors," Stinson says. "By killing off native soil fungi, the appearance of this weed in an intact forest could stifle the next generation of dominant canopy trees. It could also invite other native and nonnative weedy plants that currently grow in low-AMF habitats, such as those disturbed by logging or development."
The researchers plan to study which phytochemicals in garlic mustard may kill AMF, how these chemicals interact with other beneficial soil microbes, and how plants and fungi in garlic mustard's native European habitat coexist with the noxious species.
Stinson's co-authors are Stuart A. Campbell, Jeff R. Powell, Benjamin E. Wolfe, and John N. Klironomos at the University of Guelph; Ragan M. Callaway and Giles C. Thelen at the University of Montana; Steven G. Hallett at Purdue University; and Daniel Prati at the UFZ Centre for Environmental Research. The work was funded by the National Science Foundation's Long Term Ecological Research Program at Harvard Forest, the Natural Sciences and Engineering Research Council of Canada, and Harvard's Bullard Foundation.
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