After three growing seasons, in plots cleared of vegetation and planted with exotic propagules, exotics covered 39% of the ground in AA soils and 9% of the ground in NA soils (Fig. 1). The exotic plant growth response to differences in soil history therefore explained most of the difference in exotic plant abundance observed on the landscape (i.e. exotics covered 38% of the ground in AA fields and 3% of the ground in NA fields). In contrast, the exotic plant growth response to neighbour removal was small. Exotics covered 11% of the ground in plots cleared of native vegetation and 3% of the ground in plots where native vegetation was left undisturbed. The presence of standing dead native vegetation and increased native propagule pressure had no effect on exotic cover. Thus the effect of neighbour removal on increased exotic growth was solely the result of active native plant growth (e.g. resource competition). These results demonstrated that short-term competitive interactions, whether between established plants, standing dead vegetation or germinating seeds, were less important to exotic plant growth than differences in soil history.
Native plant cover was less on AA than NA soils. Either AA soils suppressed native growth (e.g. persistent allelochemicals) or NA soils facilitated native growth (e.g. mycorrhizal populations; Vivanco et al. 2004). Soils were not tested for the allelochemicals released by C. diffusa (i.e. 8-hydroxyquinoline) or species-specific mycorrhizae. However, even if allelochemicals or native-specific mycorrhizae were found, their effect on native plants would probably not explain the distribution of plants on the landscape. Native plant treatment responses were never greater than 5% ground cover but natives covered 43% of the ground in NA fields and 4% of the ground in AA fields.
Native plant cover was also reduced in the presence of exotic plants (Fig. 1b). This effect was associated completely with the presence of standing dead exotic vegetation. It is unlikely that standing dead exotic vegetation reduced native cover by providing increased seed rain because experimental additions of exotic seeds failed to reduce native cover and because most vegetation was treated with herbicide before exotic seeds could mature. It is more likely that the small reduction in native cover under dead exotic vegetation resulted from physical effects, such as shading, or chemical effects, such as allelopathy or the addition of C-rich plant matter. While the response of natives or exotics to soil or competition could have explained plant distributions, we found that it was exotic plant responses to soil history that best explained plant distributions in the landscape.
potential soil history mechanisms
Soils in AA and NA fields may differ in several ways. Abandoned agricultural soils had been selected by farmers, tilled, fertilized and dominated by exotic plant species (both agricultural and post-agricultural). Farmers may have selected more fertile soils, tillage may have freed soil resources (Jackson et al. 2003) and fertilization may have increased soil nutrient concentrations. Each of these conditions may have increased soil resource availability and this could be expected to provide a growth advantage for fast-growing (e.g. exotic invasive) species (Davis, Grime & Thompson 2000). In addition to increasing resource availability, tillage may have altered soil biology or structure in a way that benefits exotic plant species (Jackson et al. 2003). Finally, agricultural plant monocultures or post-agricultural exotic species may have exercised plant–soil feedback that altered soils in ways that facilitated the growth of exotic species.
We attempted to control for differences selected by farmers by using only NA and AA fields with similar slope and aspect that were separated by biologically arbitrary boundaries. That native plant growth was greater on NA than AA soils suggested that NA soils were not of lower quality for all species. We tested the effect of tillage by hand-tilling soils. In NA fields, exotic plants grew better in soils that had been hand-tilled (16% absolute cover) than in soils that had not been hand-tilled (9% absolute cover), an effect comparable in size to the effect of removing native plant competitors. This suggests that native plants grow in a soil that inhibits exotic plant growth and that disturbing this soil removes the inhibition. This soil-based inhibition, however, appears to account for only 7% of the 30% difference in exotic absolute cover observed between AA and NA soils. Hand-tillage treatments were also performed in AA fields. Hand-tillage in AA fields did not improve exotic plant growth, showing that, in terms of exotic plant growth, disturbed soils in AA fields were different from soils in NA fields.
Abandoned agricultural fields had been fertilized while under agricultural use. Fertilized soils could be expected to benefit fast-growing, early successional exotic species (Davis, Grime & Thompson 2000; Davis & Pelsor 2001; Ehrenfeld 2003). While we did observe interactions between agricultural history and plant cover type on some measures of soil chemistry, these interactions did not suggest the presence of a fertilization effect in AA relative to NA fields. For example, extractable P concentrations were lower in AA than NA soils. Furthermore, differences in extractable C, N and P availability were at least as large between samples stratified by vegetation history as between samples stratified by agricultural history (Table 1). Our results indicate that agricultural practices in these fields removed more nutrients (e.g. by exporting crops) than were replaced (e.g. with fertilizer).
Tillage, but not fertilization, therefore provided a partial explanation for the success of exotic plants in AA fields. It is likely, then, that changes induced in soils by the growth of exotic plants themselves explained why exotics grew well in AA but not NA soils. Exotic plants in AA fields could be expected to change the seed bank, soil biology or soil chemistry. We attempted to control for the effect of the seed bank by adding propagules from one plant community into the other, but it was impossible to completely replicate the propagule pressure of one field in the other. As a result, differences in propagule pressure could be expected to explain partially exotic plant growth. We do not, however, believe this provides a strong explanation for differences in plant growth between AA and NA fields for two reasons. First, experimental seed additions did not increase exotic growth above background recruitment. This result was anticipated because experimental plots in NA fields were placed as close to AA fields as possible and because exotic growth on the landscape is small in NA fields even where NA fields are located downwind and downhill of AA fields that have been dominated by exotic species for decades (Kulmatiski 2006). Secondly, tillage of exotic seeds can be expected to reduce seed bank effects, yet tilling exotic soils did not reduce exotic growth. This result suggests that the seed bank was not a dominant factor determining exotic plant growth in AA fields.
The vigorous growth of exotics in AA fields could result from positive plant–soil feedback. Positive plant–soil feedback has been shown previously for individual plant species and in potted experiments (Bever, Westover & Antonovics 1997; Klironomos 2002; Reinhart et al. 2003) but have not been shown for whole communities under field conditions. Feedback can be caused by two general mechanisms: facilitation and inhibition. Soils from AA fields could have facilitated exotic plant growth, or soils from NA fields could have inhibited exotic plant growth. Tillage improved exotic growth on NA soils by 7% cover, suggesting that tillage removes a form of soil-based exotic plant growth inhibition. The remainder of the positive plant–soil feedback (Fig. 1a, inset; i.e. 23% cover) may be explained by facilitation between exotic plants and their soils. Soil-based facilitation is often attributed to symbioses between plants and fungi (Klironomos 2002; Callaway et al. 2004a).
We found that fungicide addition in AA fields reduced exotic plant growth by 11% cover. Fungicide addition did not affect exotic plant growth in NA fields (Fig. 1d). This suggests that AA soils maintain a fungal community that improves exotic growth. Because the fungicide Benomyl has a greater affect on mycorrhizal than non-mycorrhizal fungi (Callaway et al. 2004a) and because the growth of mycorrhizal fungal species is tightly associated with the growth of their plant symbionts, it is more likely that the fungal communities in AA soils reflect plant growth than historical agricultural practices, although this could not be determined. A plant–soil fungal relationship was also evident across the landscape, although not as expected. Exotic plants tended to be associated with small active fungal populations (Table 1). Furthermore, mycorrhizal infection rates for the dominant exotic, C. diffusa, were higher on soils from AA fields than from NA fields. It is likely, then, that exotics promote a small but highly beneficial mycorrhizal fungal community: a mycorrhizal fungal community that is not abundant in NA soils. Further descriptions of microbial communities may greatly contribute to explaining invasive success in these sites.
Plant–fungal relationships explained a large proportion of the difference in plant growth observed between AA and NA fields, but did not fully explain this difference. We predicted that plant–soil nutrient feedback would provide an additional explanation for facilitation between exotic plants and their soils (Miki et al. 2002; Ehrenfeld 2003). Exotic plants were associated with higher rates of net N mineralization than native plants. Interestingly, the soils that supported exotics showed higher net N mineralization but smaller inorganic N pools than soils supporting natives (Table 1). Faster N cycling rates and smaller nutrient pool sizes could result because exotic plants are drawing down labile nutrient pools to maintain fast growth rates.
Under field conditions, exotic plant growth responses to differences in soil history were more than three times greater than exotic plant growth responses to neighbour removal: exotics could not grow well on NA soils. Removing native plants from NA soils improved exotic growth, as did tilling NA soils. The magnitude of these effects, however, appeared to be small relative to the effect of facilitation between exotic plants and their soils. This plant–soil relationship appeared to persist across multiple plant generations and to result from plant–soil microbial and plant–soil nutrient relationships.
Before a plant can germinate and grow, or compete with other plants, it must acquire soil-borne nutrients, avoid soil-borne pathogens and herbivores, and possibly develop symbioses with soil-borne organisms. We did not measure specific plant–soil organism interactions, but we did observe that plant growth responses to adjacent soils with different management histories were greater than plant growth responses to neighbour removal. Where exotic plants induce long-term changes in soil traits, the restoration of native plant communities will require either the production of soils that mimic native soils or the selection of native plants that are better able to respond to the growth conditions present in exotic soils. For example, sawdust and activated C additions can manipulate soil biology and chemistry and have been suggested as management tools for native plant restoration (Corbin & D’Antonio 2004; Kulmatiski & Beard 2006). Activated C addition, in particular, has demonstrated the potential to limit the growth of some exotic plant species. Many studies have found links between the soil biota and plant success (Thomashow 1996; Wilson & Hartnett 1997; van der Heijden et al. 1998; Borneman & Hartin 2000; Ronsheim & Anderson 2001; van Os & van Ginkel 2001), suggesting that continued study of specific plant–microbe interactions is likely to result in the development of novel species-specific management approaches for invaded plant communities (van Bruggen & Semenov 2000; Kulmatiski, Beard & Stark 2004; Wolfe & Klironomos 2005).