Research articleInvasive plant species do not create more negative soil conditions for other plants than natives
Introduction
Several mechanisms have been proposed to explain the success of plant invaders. Many of them involve natural enemies (e.g., Keane and Crawley, 2002) or other interspecific interactions (e.g., Mitchell et al., 2006), changes in the competitive balance between plants (e.g., Blossey and Notzold, 1995), or changes in resource availability (Davis et al., 2000). During recent years, several studies have highlighted the critical role of soil ecology for the study of plant invasions and the importance of belowground mechanisms for plant invasion success has been increasingly recognized (Callaway and Aschehoug, 2000, Inderjit van der Putten, 2010, van der Putten et al., 2007, Wolfe and Klironomos, 2005). This has led to the formulation of two major hypotheses.
The first hypothesis is the novel weapons hypothesis, which states that invasive plants release biochemical compounds, so-called allelopathic compounds, which are harmful to native species (Callaway and Ridenour, 2004, Rabotnov, 1981). This hypothesis assumes that allelopathic effects of invasive plant species are especially important in the invaded range as the recipient community's species are not adapted to the biochemical compounds of plant invaders (Hierro and Callaway, 2003). To have a long-term effect, these allelopathic compounds must be persistent in the soil, resulting in a legacy effect (Kaur et al., 2009). Evidence for this mechanism relies on a few single species experiments. For instance, Centaurea diffusa and Ageratina adenophora exert stronger allelopathic effects on plant species from their invaded than from their native range (Callaway and Aschehoug, 2000, Inderjit et al., 2011). Another example is Alliaria petiolata exhibiting stronger allelopathic effects in the invaded than in the native range, both by harming other plants directly (Prati and Bossdorf, 2004) and indirectly by disrupting mycorrhizal associations in the invaded range (Callaway et al., 2008). Such biogeographical comparisons are important to understanding the role of co-evolution in plant invasions. However, this approach neglects the fact that native species might exert the same effects on other native species. Such a comparison is crucial to understand which processes contribute to the success of invasive over native species (Hamilton et al., 2005), but a systematic comparison of allelopathy in invasive and native species is still lacking.
A second hypothesis is the accumulation of local pathogens, stating that invasive species alter the soil microbial community to the disadvantage of native species (Eppinga et al., 2006). This hypothesis makes the same prediction of outcome as the novel weapons hypothesis but assuming a different underlying mechanism. It is well known that plant species can influence the structure and composition of the soil microbial community, resulting in unique soil communities under different plant species (Bever et al., 1997, Bezemer et al., 2006, van der Putten et al., 2007). These soil communities may differ in density or composition of mutualistic or pathogenic microorganisms and thereby affect the performance of other plant species (Bever, 2003, Mangla et al., 2008). This idea has received a lot of attention in invasion ecology. However, evidence that invasive species accumulate pathogens that harm native species relies on only a few study systems (de la Pena et al., 2010, Mangla et al., 2008), not all of which show the same pattern (te Beest et al., 2009).
A major task in ecology is to establish the degree of generality of a mechanism. Although details of the mechanisms differ between the two above mentioned hypotheses, they both predict that invasive plants affect the soil to the detriment of native species, either directly or indirectly. Furthermore, these mechanisms are not restricted to invasive species and may play important roles during range expansion and competition among native species. In invasion ecology, many studies focused either on the effect of a single invasive species, or the response of a single native species, although native species have been shown to differ in sensitivity to belowground alterations, both in terms of allelopathic compounds and the soil microbial community (Abhilasha et al., 2008, Gomez-Aparicio and Canham, 2008). Thus, the general importance of both the novel weapons and the accumulation of local pathogens hypotheses in explaining invasions remains unclear. To assess the generality of a hypothesis, meta-analytical approaches are often used, which combine different studies that often vary considerably in the details of methods (Kulmatiski et al., 2008). Multi-species experiments offer an alternative to meta-analyses by comparing the response of several species in a common experiment and thereby reducing the heterogeneity among studies commonly associated with meta-analyses (Schlaepfer et al., 2010). Furthermore, these experiments allow estimating the variation among species groups more accurately than meta-analyses as they are unaffected by publication bias.
Most studies on mechanisms of plant invasions have focused on invasive plants without testing if native plants exert the same effects on other plants as invasives. Thus, one way to study the relative importance of allelopathy and accumulation of local pathogens is to compare the effect of invasive species with that of closely related native species. Even though closely related species may not always occupy the same habitat type or directly compete with each other, the strength of this method is that it accounts for phylogenetic interdependence among species (van Kleunen et al., 2010, Westoby et al., 1995).
Here, we tested the common prediction of the novel weapons and the accumulation of local pathogen hypotheses, that invasive species generally create more negative soil conditions for native plants compared with their native congeners. Specifically, we asked the following questions: (1) Do invasive species generally exert a stronger allelopathic effect on native plants compared to the invasives’ native congeners? (2) Do invasive species generally promote a soil community more harmful to native plants compared with the invasives’ native congeners? (3) Do native species respond consistently to soil pre-cultivation with invasive and closely related native species?
To answer these questions, we used the soil pre-cultivation approach, which allows assessing the net effect of changes in the soil microbial community composition caused by plant species (Bever et al., 1997, Wolfe and Klironomos, 2005). We pre-cultivated soil with invasive and native species and then compared the performance of plants with that of plants in control soil that was not pre-cultivated. This soil pre-cultivation approach has been acknowledged as the most useful to investigate the role of the soil microbial community in plant invasion success (Wolfe and Klironomos, 2005). Additionally, we compared the effect of soil pre-cultivation in sterilized and unsterilized soil to separate effects of soil microbial community composition and allelopathy.
Section snippets
Investigated plant species
To test the role of the soil microbial community and allelopathy in plant invasion success, we pre-cultivated soil with 48 plant species, which we call cultivation species hereafter. Among these, 23 were invasive in Europe, 19 were closely related natives and 6 were closely related exotic species cultivated in gardens (Appendix Table S1). The 23 invasive species are established in more than 40% of the European countries (DAISIE, 2008) and most of them appear on the ‘black list’ of noxious plant
Germination experiment
Soil sterilization generally increased the performance of test species in the germination experiment (germination success: F1,193 = 64.53, P < 0.001; germination rate: F1,193 = 97.83, P < 0.001; seedling biomass: F1,193 = 37.04, P < 0.001). However, this effect also occurred in control soil, as there was no interaction between sterilization and pot (germination success: F1,193 = 0.01, P = 0.92; germination rate: F1,193 = 0.25, P = 0.62; seedling biomass: F1,193 = 0.38, P = 0.54; Fig. 2).
The analysis of effect sizes of
The effect of soil sterilization
Soil sterilization positively affected test species performance both in pre-cultivated soil where the soil microbial community had been influenced by plant species and in control soil where soil microbes had not been cultured. This positive response to sterilization may be due to a general negative impact of the soil microbial community. During the growth process of the test species microbes were likely introduced in both pre-cultivated and control soil, either by air or with the seeds of test
Conclusions
In general, invasive species do not create more negative soil conditions for other plants than related native species. Thus, plant origin is neither a key factor for the accumulation of persistent allelopathic compounds, nor for the accumulation of a soil microbial community beneficial or detrimental to other plants. Plant species seem to have a larger effect on the soil microbial community than on abiotic soil properties. This alteration is species specific and affects other species unequally,
Acknowledgments
We would like to thank the many students for help during the experiments, Stephanie Frei for help with counting germinated seedlings and members of the Fischer lab for helpful comments on earlier versions of the manuscript. Financial support was provided be the Swiss National Science Foundation SNSF (grant no. 31003A_127561 to Daniel Prati).
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