Research article
Invasive plant species do not create more negative soil conditions for other plants than natives

https://doi.org/10.1016/j.ppees.2015.02.002Get rights and content

Abstract

A major task in ecology is to establish the degree of generality of ecological mechanisms. Here we present results from a multi-species experiment that tested whether a set of invasive species altered the soil conditions to the detriment of other species by releasing allelopathic compounds or inducing shifts in soil biota composition, and whether this effect was more pronounced relative to a set of closely related native species.

We pre-cultivated soil with 23 exotic invasive, 19 related native and 6 related exotic garden species and used plain soil as a control. To separate allelopathy from effects on the soil biota, we sterilized half of the soil. Then, we compared the effect of soil pre-cultivation and sterilization on germination and growth of four native test species in two experiments.

The general effect of soil sterilization was positive. The effect of soil pre-cultivation on test species performance was neutral to positive, and sterilization reduced this positive effect. This indicates general absence of allelopathic compounds and a shift toward a less antagonistic soil biota by cultivation species. In both experiments, pre-cultivation effects did not differ systematically between exotic invasive, exotic garden or native species.

Our results do not support the hypothesis that invasive plants generally inhibit the growth of others by releasing allelopathic compounds or accumulating a detrimental soil biota.

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).

References (53)

  • A.C. Blair et al.

    A Lack of evidence for an ecological role of the putative allelochemical (±)-catechin in spotted knapweed invasion success

    J. Chem. Ecol.

    (2006)
  • B. Blossey et al.

    Evolution of increased competitive ability in invasive nonindigenous plants – a hypothesis

    J. Ecol.

    (1995)
  • M. Borenstein et al.

    Introduction to Meta-Analysis

    (2009)
  • R.M. Callaway et al.

    Invasive plants versus their new and old neighbors: a mechanism for exotic invasion

    Science

    (2000)
  • R.M. Callaway et al.

    Novel weapons: invasive plant suppresses fungal mutualists in America but not in its native Europe

    Ecology

    (2008)
  • R.M. Callaway et al.

    Novel weapons: invasive success and the evolution of increased competitive ability

    Front. Ecol. Environ.

    (2004)
  • M. Chytry et al.

    Habitat invasions by alien plants: a quantitative comparison among Mediterranean, subcontinental and oceanic regions of Europe

    J. Appl. Ecol.

    (2008)
  • CPS/SKEW

    The Swiss Commission for Wild Plant Conservation. Black List and Watch List

    (2007)
  • DAISIE

    European Invasive Alien Species Gateway

    (2008)
  • M.A. Davis et al.

    Fluctuating resources in plant communities: a general theory of invasibility

    J. Ecol.

    (2000)
  • G.B. De Deyn et al.

    Plant community development is affected by nutrients and soil biota

    J. Ecol.

    (2004)
  • E. de la Pena et al.

    Plant–soil feedback as a mechanism of invasion by Carpobrotus edulis

    Biol. Invas.

    (2010)
  • C. Del Fabbro et al.

    Allelopathic effects of three plant invaders on germination of native species: a field study

    Biol. Invas.

    (2014)
  • P. Dostal

    Plant competitive interactions and invasiveness: searching for the effects of phylogenetic relatedness and origin on competition intensity

    Am. Nat.

    (2011)
  • M.B. Eppinga et al.

    Accumulation of local pathogens: a new hypothesis to explain exotic plant invasions

    Oikos

    (2006)
  • L. Gomez-Aparicio et al.

    Neighbourhood analyses of the allelopathic effects of the invasive tree Ailanthus altissima in temperate forests

    J. Ecol.

    (2008)
  • Cited by (18)

    • Leaf litter age regulates the effect of native and exotic tree species on understory herbaceous vegetation of riparian forests

      2020, Basic and Applied Ecology
      Citation Excerpt :

      The Novel Weapons Hypothesis predicts not only stronger allelopathic effects produced by exotic invasive plant species in their invaded range of distribution than in their native one, but also stronger effects produced by invasive plant species than by native ones on the native community. However, exotic species not always exert greater allelopathic effects than native ones, likely due to the species-specific effects and the context-dependence driving allelopathic interactions (Catalán, Vázquez-de-Aldana, de las Heras, Fernández-Seral, & Pérez-Corona, 2013; Del Fabbro & Prati, 2015; Medina-Villar, Alonso, Castro-Díez, & Pérez-Corona, 2017; Pisula & Meiners, 2010). Thus, comparing the allelopathic potential of native and exotic species is essential to evaluate the relative role of allelopathy in the invasion success of the exotic species (Del Fabbro, Güsewell, & Prati, 2014).

    • Differential effects of plant growth-promoting bacteria on invasive and native plants

      2019, South African Journal of Botany
      Citation Excerpt :

      Thus, primarily soil amendment strategies should be considered for the restoration of the area invaded by A. adenophora, such as solarization to kill weed seeds or pathogenic bacteria and top soil removal to reduce soil microbes (Grman and Suding, 2010). Recently, it was reported that invasive plants are unable to accumulate detrimental soil biota for the growth of native plants (Fabbro and Prati, 2015). Our results indicated that, at the species level, bacteria that accumulated in the rhizosphere soil of A. adenophora were unlikely to be more detrimental to the growth of the two native species than those inhabiting the native plants.

    • Quantifying Differences Between Native and Introduced Species

      2016, Trends in Ecology and Evolution
      Citation Excerpt :

      Relevant predictors can be included at each level, which would allow simultaneous testing of whether microhabitat variation in species richness, soil nitrogen, etc. and site-level variation in species richness, precipitation, temperature, etc. affect community assembly. Although decades of theory posit that introduced species require unique ecological hypotheses to explain their spread and success, recent evidence suggests that native and introduced species have similar succession trajectories [11], leaf carbon capture traits [8,12], chemical defenses [49], enemy release [45], soil allelopathy [50], and community assembly mechanisms (see [20] and Case Study 2). These results suggest that introduced and native species might thrive for very similar reasons.

    View all citing articles on Scopus
    View full text