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Invasive Plants Versus Their New and Old Neighbors: A Mechanism for Exotic Invasion

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Science  20 Oct 2000:
Vol. 290, Issue 5491, pp. 521-523
DOI: 10.1126/science.290.5491.521

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Abstract

Invading exotic plants are thought to succeed primarily because they have escaped their natural enemies, not because of novel interactions with their new neighbors. However, we find thatCentaurea diffusa, a noxious weed in North America, has much stronger negative effects on grass species from North America than on closely related grass species from communities to whichCentaurea is native. Centaurea's advantage against North American species appears to be due to differences in the effects of its root exudates and how these root exudates affect competition for resources. Our results may help to explain why some exotic species so successfully invade natural plant communities.

Exotic plants threaten the integrity of agricultural and natural systems throughout the world. Many invasive species are not dominant competitors in their natural systems, but competitively eradicate their new neighbors. One leading theory for the exceptional success of invasive plants is that they have escaped the natural enemies that hold them in check, freeing them to utilize their full competitive potential. This perspective provides the theoretical framework for the widespread practice of introducing natural enemies as biological controls, which also are exotic, to suppress invasive plants (1). Plant communities are widely thought to be “individualistic,” composed primarily of species that have similar adaptations to a particular physical environment (2, 3). With few exceptions (4–7), plant communities are not thought to consist of coevolved species, nor to possess stable properties determined by plant-plant interactions. Here, we argue that some invasive plants may succeed because they bring novel mechanisms of interaction to natural plant communities.

We compared the competitive effects of an invasive Eurasian forb, Centaurea diffusa (diffuse knapweed), on three bunchgrass species that coexist with C. diffusa in Eurasia with the effects of C. diffusa on three bunchgrass species from North America that have similar morphologies and sizes, each of which is closely related to one of the Eurasian grass species. Seeds of C. diffusa, Festuca ovina,Koeleria laerssenii, and Agropyron cristatum were collected within an area of several hectares in the southern foothills of the Caucasus Mountains in the Republic of Georgia. Seeds of F. idahoensis, K. cristata, and Pseudoroegneria spicata were collected from grasslands in the northern Rocky Mountains in Montana. Until recently, Pseudoroegneria was included in the genus Agropyron. Each of the grass species made up more than 10% of the total cover at its respective site. At the study site in the Caucasus, the cover of C. diffusa was less than 1%, whereas at the Montana site, the cover of C. maculosa (which is closely related to C. diffusa) was 10 to 90%. Each of the seven species was planted alone and in all pairwise grass-Centaurea combinations. All combinations were grown in sand and mixed with activated carbon (8,9).

Centaurea diffusa had much stronger negative effects on North American species than it had on Eurasian species. When grown with Centaurea, the biomass of North American grasses decreased 85.7 ± 0.3%; whereas in Eurasian species, biomass decreased by only 50.0 ± 4.7% (Fig. 1) (10). Correspondingly, none of the North American grass species (nor all species analyzed collectively) had a significant competitive effect on the biomass ofC. diffusa, but the Eurasian species K. laerssenii, and all Eurasian species analyzed collectively, significantly reduced C. diffusa biomass (Fig. 2) (11). Centaurea diffusa had no effect on the amount of 32P acquired by Eurasian grass species (12), but significantly reduced32P uptake of all North American species (Fig. 3) (13). Correspondingly, North American grasses had no competitive effects on 32P uptake of C. diffusa, but all Eurasian species demonstrated strong negative effects on the amount of 32P acquired by C. diffusa (Fig. 4) (14).

Figure 1

Total biomass for related Eurasian and North American bunchgrass species grown alone, or with the invasive plant, C. diffusa, either with or without activated carbon in the soil. Error bars represent S.E.M. Means with different letters were significantly different in pairwise comparisons.

Figure 2

Total biomass for C. diffusa plants grown alone, or with Eurasian or North American bunchgrass species, either with or without activated carbon in the soil. Error bars represent S.E.M. Means with different letters were significantly different in pairwise comparisons.

Figure 3

Total counts per minute for related Eurasian and North American bunchgrass species grown alone, or with the invasive plant, C. diffusa, either with or without activated carbon in the soil. Error bars represent S.E.M. Means with different letters were significantly different in pairwise comparisons.

Figure 4

Total counts per minute for C. diffusa plants grown alone, or with Eurasian or North American bunchgrass species, either with or without activated carbon in the soil. Error bars represent S.E.M. Means with different letters were significantly different in pairwise comparisons.

Activated carbon was added to ameliorate chemical effects (8), and it had contrasting effects on the interactions between C. diffusa and grass species from the different continents. The biomass of two North American species,F. idahoensis and P. spicata, when grown withC. diffusa, increased significantly in soil mixed with activated carbon; the overall effect of carbon on North American species in competition with C. diffusa was positive and significant (Fig. 1) (10). In contrast, the biomass of all Eurasian grass species growing with C. diffusa was reduced dramatically in the presence of activated carbon. Correspondingly, activated carbon gave C. diffusa a competitive disadvantage against North American grasses (Centaurea biomass was reduced) but a competitive advantage in the presence of Eurasian grasses (Centaurea biomass increased) (Fig. 2) (12). Unlike its effect on total biomass, the effect of activated carbon was not to enhance the uptake of 32P of North American grasses in the presence of C. diffusa, indicating that allelopathic effects were manifest somewhat independently from competition for this particular resource (Fig. 3) (13). However, having activated carbon in the soil was a strong disadvantage for Eurasian grasses competing for32P with C. diffusa. In all cases,32P uptake by Eurasian grasses growing with C. diffusa decreased in the presence of activated carbon. The effects of activated carbon on 32P uptake by grasses corresponded with the effects of activated carbon on 32P uptake byC. diffusa. Activated carbon enhanced uptake by C. diffusa in the presence of Eurasian grasses but reduced uptake in the presence of North American grasses (Fig. 4) (14). We interpret the effects of activated carbon as evidence for allelopathy, as have others (15–17); however, activated carbon may also affect other soil properties, as well as the soil microbial community.

In a separate experiment (9), activated carbon did not have any significant direct effect on the total biomass of any of the six grass species when they were grown alone, nor was the effect of carbon significant when all species were tested together [ANOVA, treatment, F(1,97) = 0.53, P = 0.471]. As found in the first experiment, the Eurasian grass species were larger than North American grass species [region,F(1,97) = 13.11, P < 0.001].

When grown with C. diffusa, the proportion of total pot biomass made up of grasses was greater for Eurasian (38%) than North American (11%) species. Concomitantly, proportional biomass of C. diffusa was less when it was grown with Eurasian than with North American grasses. Activated carbon increased the dominance of C. diffusa with Eurasian grasses (84% from 62%) but decreased its dominance with North American grasses (78% from 89%). Significant biogeographical differences also existed for the total biomass and total resource uptake by both individuals combined within a pot. Pots with Eurasian grass species combined with C. diffusa produced 12% more total biomass and took up 63% more total phosphorus than pots with North American species planted withC. diffusa (18), suggesting that long-term association among plant species may enhance productivity and total resource utilization.

The strong effects of biogeographical place of origin on the competitive ability of grass species against C. diffusa, as well as the contrasting effects of activated carbon on competition, suggest that C. diffusa produces chemicals to which long-term and familiar Eurasian neighbors have adapted, but to whichC. diffusa's new North American neighbors have not. Chemical allelopathy has long been suspected as a mechanism by which invasive plant species eliminate natives (19–21). The competitive ability of Eurasian grass species against C. diffusa is greatly reduced by activated carbon, suggesting that the natural advantage of Eurasian species is, at least in part, also chemically mediated. In our experiments, the root systems of competing plants were constricted in pots, preventing any spatial root niche partitioning that might reduce competitive interactions.

Contrasting interactions among plants from different biogeographical regions have several implications for community ecology. First, they suggest that natural plant communities may be more tightly knit entities than generally thought. Second, these biogeographical effects conflict with the theory that plant competition is not species-specific (22, 23). Third, they suggest that interactions among plant species may drive natural selection in communities. Fourth, they imply that natural biological communities may evolve in some way as functionally organized units (24, 25). Finally, our results indicate that some exotic invasive plants may use competitive mechanisms that are not present in the natural communities that they invade to disrupt inherent, coevolved interactions among long-associated native species.

  • * To whom correspondence should be addressed. E-mail: callaway{at}selway.umt.edu

  • Present address: The Nature Conservancy, 201 Mission Street, San Francisco, CA 94105, USA.

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