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Many mechanisms of invasive species success have been elucidated, but those driving cryptic invasions of non-native genotypes remain least understood. In one of the most successful cryptic plant invasions in North America, we investigate the mechanisms underlying the displacement of native Phragmites australis by its Eurasian counterpart. Since invasive Phragmites’ populations have been especially prolific along eutrophic shorelines, we conducted a two-year field experiment involving native and invasive genotypes that manipulated nutrient level and competitor identity (inter- and intra-genotypic competition) to assess their relative importance in driving the loss of native Phragmites. Inter-genotypic competition suppressed aboveground biomass of both native and invasive plants regardless of nutrient treatment (∼ 27%), while nutrient addition disproportionately enhanced the aboveground biomass (by 67%) and lateral expansion (by > 3 × farther) of invasive Phragmites. Excavation of experimental plots indicated that nutrient addition generates these differences in aboveground growth by differentially affecting rhizome production in invasive vs native plants; invasive rhizome biomass and rhizome length increased by 595% and 32% with nutrient addition, respectively, while natives increased by only 278% and 15%. Regardless of nutrient level, native rhizomes produced twice as many roots compared to invasives, which field surveys revealed are heavily infected with mycorrhizal symbionts. These results suggest that native Phragmites competes well under nutrient-limited conditions because its rhizomes are laden with nutrient-harvesting roots and mycorrhizae. Invasive Phragmites’ vigorous aboveground response to nutrients and scarcity of lateral roots, in contrast, may reflect its historic distribution in eutrophic Eurasian wetlands and correspond to its prevalence in New England marshes characterized by elevated nutrient availability and relaxed nutrient competition. These findings reveal that discrete differences in phenotype can interact with anthropogenic modification of environmental conditions to help explain the success of cryptic invaders.