The Power of Invasives

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Garlic mustard seedlings emerging along a stone wall amidst native vegetation in late spring, near a long term invasive plant monitoring plot at Harvard Forest's LTER site.
K. Stinson

Harvard Forest researchers have transformed the scientific understanding of biological invasion by discovering that non-native plants can disrupt the longstanding ecological relationship between native tree seedlings and their beneficial fungi by releasing chemicals belowground. With native plants suppressed, the exotic plants are able to invade forests more aggressively.

The impacts of invasive species across the globe are a major focus of ecological research. In North America, thousands of nonnative plants and animals have become established since European settlement and new species are introduced every day. Some newcomers cause little harm, while others become very aggressive, displace native organisms, and radically alter their new habitats. Many processes, from the absence of natural enemies to global climate change, have been proposed to explain the success and impacts of invasive species. This research shows that introduced species disrupt longstanding ecological relationships that have evolved over millions of years of coexistence.

At the Harvard Forest, researchers have discovered that the widespread invasive plant, garlic mustard (Alliaria petiolata), disrupts symbiotic relationships between many native plant species andbeneficial microbes in the forest soil. Originating in Eurasia, garlic mustard is a weedy plant that primarily occupies disturbed areas within its home range. Its proliferation into intact forest communities across North America has raised much concern about its impact on native plants. Over a decade in the field, Kristina Stinson and colleagues noted a pattern of decline in native plant abundance with increasing invasion, and suspected that garlic mustard's impacts began below-ground. As a member of the mustard family, garlic mustard produces its own unique suite of mustard oils and other phytochemicals that are known repellants to insects and fungi.

First, the team demonstrated that invasion by garlic mustard suppresses the growth of forest understory plants by disrupting their affiliation with mycorrhizal fungi, a highly diverse group of soil microbes that most plant species depend on, especially woody plants. These fungi have long filaments that penetrate roots, forming an intricate network that effectively extends the plant's root system. The fungi depend on the plant's photosynthesis for energy, and the plant depends upon the fungi for taking up nutrients that are usually patchy and in limited supply in forest soils. In controlled experiments, researchers exposed native hardwood tree seedlings to the presence of garlic mustard. In the invaded soil, three species -- sugar maple, red maple, and white ash -- had significantly less mycorrhizae on their roots and grew only about one-tenth as fast. Further studies showed that adding garlic mustard extracts to uninvaded soil reduced both mycorrhizal colonization and seedling growth in native plants, confirming a phytochemical effect of garlic mustard. When seedlings of 16 other native plants were exposed to similar treatments, only the hardwoods and shrubs were harmed by the presence of garlic mustard, suggesting that toxicity to the main biological allies of woody plants contribute to invasion success in mature forests.

In subsequent work, the researchers have shown that garlic mustard is toxic to many different kinds of soil microbes in North America, including another group of soil fungi, the ectomycorrhizae (which produce the fruiting bodies we know as mushrooms) and some bacteria, which have an important role in decomposition. However, both plants and soil organisms that coexist with garlic mustard in its home range are unaffected. This supports the hypothesis that garlic mustard's disruption of plant-microbe interactions is novel in North America, while long-term coexistence in its native range lends resistance to European plants and fungi. Interestingly, long-term research has allowed the researchers to show that invaded microbial communities in North American forests can change their composition in response to A. petiolata, favoring microbes that are more resistant to its chemical effects.

This research provides important (and rare) evidence for negative impacts of invasion, while also suggesting a potential evolutionary mechanism by which this plant outperforms those in the invaded range and reaches problematic levels of abundance. The results to date suggest that a re-organization of both plants & microbes following invasion events can be expected.

The researchers tested whether soils with a history of garlic mustard invasion reduced the ability of native tree seedlings to form mycorrhizal associations and grow compared to non-invaded soils. The dominant native hardwood tree species (sugar maple, red maple, and white ash) showed significantly less mycorrhization (a) and grew significantly less well (b) in soil invaded by garlic mustard. These reductions were similar to those observed on sterilized soil from both garlic mustard-infested and garlic mustard-free sites (Fig 1b), strongly suggesting that garlic mustard suppresses the growth of native trees by disrupting microbial interactions.
For further reading: 
Wolfe, B.E., Rodgers, V.L., Stinson, K.A., and Pringle, A. (2008) The invasive plant Alliaria petiolata(garlic mustard) inhibits ectomycorrhizal fungi in its introduced range. Journal of Ecology 96:777-783.
Callaway R.M., Cipollini, D. Barto K., Thelen, G.C., Hallett G., Prati D., Stinson, K.A., Klironomos, J. (2008) Novel weapons: invasive plant suppresses fungal mutualists in America but not in its native Europe. Ecology 89:1043-1055.
Stinson K.A., Campbell S.A., Powell J.R., Wolfe B.E., Callaway R.M., Thelen G.C., Hallett S.G., Prati D. and Klironomos J.N. 2006. Invasive plant suppresses the growth of native tree seedlings by disrupting belowground mutualisms. PLOS Biology 4: 727-731.
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Kristina Stinson
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