PerspectivePlant Science

An Invasive Plant Paradox

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Science  08 May 2009:
Vol. 324, Issue 5928, pp. 734-735
DOI: 10.1126/science.1173651

Why some plants attain extremely high densities in communities where they are exotic, yet remain at low densities in their native ranges is a mystery. The pattern has been called a “paradox” because it conflicts with long-held ideas about the importance of local adaptation for the ecological performance of organisms (1). This biogeographical shift may be connected to other apparent ecological paradoxes that occur with plant invasions involving processes mediated by soil microbes. Invasions can decrease plant species diversity but also increase plant productivity. Rather than depleting soil resources as productivity increases, invasions often increase soil stocks, pools, and fluxes of nitrogen through processes regulated by microbial communities.

Plant species richness and functional diversity can increase local net primary productivity (see the figure), predominantly through more complete use of resources, or “niche complementarity” (2). Exotic plant invasions locally reduce native plant diversity, often to the point of becoming the only plant species present (3). However, contrary to what diversity-productivity experiments would predict, net primary productivity typically increases with exotic invasions (46). In a recent meta-analysis of 94 studies, the average increase in annual net primary productivity was over 80% in invaded ecosystems (6). This “invasion-diversity-productivity” paradox cannot be explained by niche complementarity, but differences in plant-soil-microbe interactions in the invaded and native ranges could perhaps provide part of the answer. Soil microbes can have strong density-dependent effects on plants, often called plant-soil-microbe feedbacks (7). These feedbacks are usually neutral or negative for plants in soils from their native ranges, but can be positive for invasive plants in soils from invaded ranges (8, 9). This directional shift is likely due to the absence of evolved species-specific plant-pathogen relations for the invasive plants (9). This absence likely enhances the competitive dominance of plant species in new ranges and increases their productivity.

Nitrogen is the primary factor limiting net primary productivity in most ecosystems (10), and short-term increases in this productivity (for example, as a result of agricultural practices) typically deplete nitrogen and other soil resources. By contrast, plant invasions increase soil nitrogen pools and total ecosystem nitrogen stocks (6, 11, 12). Soil nitrogen is regulated by the activity of soil-dwelling and mutualistic microbes. On average, invaders double litter decomposition rates, and increase both soil nitrogen mineralization and nitrification by over 50% (6). For example, the invasive trees Acer platanoides and Ailanthus altissima increase net nitrogen mineralization, net nitrification, and soil nitrogen availability compared to native tree species, including the congener Acer saccharum (13).

Diversity and productivity.

Plant productivity increases to an asymptote as plant diversity increases [solid line; derived from (2) with permission from the Ecological Society of America]. Higher productivity correlates with losses in native species richness, and invasives dominate [dashed line; estimated from (6); see (17)]. The asymptote remains higher due to invader presence in the system at lower relative densities. (Inset) The photo shows A. adenophora.


How do invasive plants decrease species diversity but increase soil nitrogen and net primary productivity? Invaders might possess morphological or biochemical traits that differ from those of native species in ways that increase nitrogen cycling in the soil. For example, thinner chlorophyll-enriched leaves that are also lower in structural carbon (characteristics that promote rapid growth) could be important traits for invasive success. Such characteristics would allow more rapid leaf decomposition, creating litter that contains a higher concentration of nitrogen (higher litter quality). Increased litter deposition rates or litter quality (14) could then explain increased nitrogen pools, stocks, and fluxes in soil. However, leaf traits may not provide all of the answers. Invaders vary widely in leaf traits, and invasive plant species do not appear to initiate the same chain of ecosystem changes in their home ranges. For example, Spartina alterniflora is native to eastern North America but is an aggressive invader in China where it has a greater leaf area index [(LAI), the ratio of leaf surface areas to ground surface area]. A higher LAI indicates that a plant produces a denser canopy (larger sized and greater quantity of leaves) in the invaded range (5). Reciprocally, Phragmites australis is native to China but is a highly successful invader in North America where it has greater net primary productivity (5). If invasive species enhance net primary productivity and nitrogen cycling in invaded ranges but not in their native ranges, then the inherent traits of plants are unlikely to drive these processes as these alterations should also be occurring in the native ranges. Alternatively, invasive plants may undergo rapid natural selection for such key leaf traits only in invaded ranges. For example, the invasive aster Ageratina adenophora (see the figure), which is native to Mexico, is an invader throughout the subtropics and appears to have evolved increased nitrogen allocation to photosynthesis and reduced allocation to cell walls in the absence of specialist herbivores (15). This would make leaves easier to decompose and suggests a potential mechanism by which invaders might possess leaves with traits that enhance nitrogen cycling in the soil of invaded ecosystems.

Soil microbes might simply be passengers in the process of increasing nitrogen pools and fluxes. However, invaders and soil microbes might interact in a biogeographically explicit way, as is often seen for plant-soil-microbe feedbacks (9), allowing the microbial community to drive changes in the nitrogen cycle that occur with plant invasions. Such shifts in plant-soil-microbe feedbacks would indicate that communities of soil microbes and plants have regional evolutionary trajectories in different parts of the world, and that mixing plants and soil microbes from different evolutionary trajectories might alter ecosystem functions. If microbial communities responsible for various ecosystem processes (including nitrogen fixation, nitrification, ammonification, and organic matter decomposition) interact with invasive plants in ways determined by evolution and biogeography, then this may help to explain the apparent paradox of increased nitrogen pools and fluxes with plant invasions.

What is needed are biogeographical comparisons of soil microbial communities and of the processes by which they drive plant invasions, specifically in native and invaded ranges. For example, invasion by some exotic grasses corresponds with increased soil nitrification rates and higher abundance and diversity of ammonia-oxidizing bacteria in invaded ranges (16). Additionally, nitrification rates positively correlate with changes in the bacterial community, suggesting a mechanism for increased nitrogen cycling in these invaded soils. As our understanding of microbial biogeography and associated functional differences expands, we may learn much about regional evolutionary relationships among plants and soil microbes and how this affects ecosystem functioning.

References and Notes

  1. Data from table 1 and figure 3 (flow chart) of (6) were used to generate the dashed line in the figure. The data used were the mean increase of 83% net primary productivity (NPP, also called ANPP in table 1) in invaded systems.
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