Soil microbes alter the diversity-invasibility relationship by promoting a complementarity effect on community invasion resistance

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We constructed native plant communities with three levels of species richness (one, three, or six species) in un-sterilized or sterilized soil (i.e., with or without soil microbes) and let them not be invaded by exotic plant species or invaded by one of three exotic species ( Solidago canadensis , Erigeron canadensis or Symphyotrichum subulatum ) highly invasive in China. The soils conditioned by the native plant communities not invaded by the exotic species were used as soil microbe inocula to test whether richness-induced differences in soil microbes affect the growth of each of the three invasive species. Compared with the presence of soil microbes, the absence of soil microbes weakened the negative species richness-invasibility relationship, indicating that soil microbes can contribute to the higher invasion resistance of more diverse native plant communities. In the presence of soil microbes, the higher invasion resistance of more diverse communities was mainly ascribed to the complementarity effect. However, soil microbes from communities with a higher species richness did not have a stronger negative effect on the growth of any of the three invasive species. We conclude that soil microbes can alter the diversity-invasibility relationship through promoting the complementarity effect on the community invasion resistance. Our results highlight the importance to integrate the role of soil microbes in testing the diversity-invasibility hypothesis. biomass diversity effect over-invasion resistance index phylogenetic distance species richness Figures Figure 1 Figure 2 Figure 3 Figure 4 Figure 5 Figure 6 Figure 7 Introduction The ability of native plant communities to resist alien plant invasions has received a great deal of attention (Dawson and Schrama 2016 ; Hess et al. 2020 ; Urza et al. 2019 ) due to the broad spread of alien species and their threats to native ecosystems (Cazetta and Zenni 2020 ; Pearson et al. 2018 ; Pyšek et al. 2020 ). Elton ( 1958 ) proposed that communities with greater species richness are more resistant to alien plant invasions. Although many experimental studies have supported this hypothesis (Adomako et al. 2019 ; Hector et al. 2001 ; Howeth 2017 ; Martignoni et al. 2020 ; Naeem et al. 2000 ; Selmants et al. 2012 ), species richness has also been found to have either no or a negative impact on the invasion resistance of native plant communities (Crawley et al. 1999 ; Lannes et al. 2020 ; Smith et al. 2004 ; Zeiter and Stampfli 2012 ). Soil microbes can affect both the invasiveness of alien species and the invasibility of native plant communities (Beckstead and Parker 2003 ; Dawson and Schrama 2016 ; Klironomos 2002 ; van der Putten et al. 2007 ). However, it remains unclear how soil microbes affect the plant diversity-invasibility relationship and what the underlying mechanisms may be. Exotic plants can suppress native plants via their impacts on soil microbes (Inderjit et al. 2021; Lankau 2011 ; Vogelsang and Bever 2009 ). For instance, exotic plants can enhance native plant pathogen levels (Beckstead et al. 2010 ; Lankau 2011 ; Mangla and Callaway 2008 ), inhibit soil microbes that have a mutualistic relationship with native plants (e.g., some arbuscular mycorrhizal fungi; Lankau 2011 ; Stinson et al. 2006 ; Vogelsang and Bever 2009 ) or produce allelochemicals that are toxic to these beneficial soil microbes (Inderjit et al. 2021; Inderjit and van der Putten 2010; Lankau 2010 ). Increasing species richness in native plant communities can provide more diverse food resources (root exudates and litter) and increase the available habitats for soil microbes (Hooper et al. 2000 ; Millard and Singh 2010 ; Prober et al. 2015 ; Wardle 2006 ), thus increasing their biomass, activities and diversity (Hiiesalu et al. 2014 ; Liu et al. 2020 ; Mitchell et al. 2010 ; Prober et al. 2015 ; Wang et al. 2017 ). Consequently, native plant communities that are more species-rich may be more likely to harbor soil microbes that can help the native plants to resist invasion-mediated pathogen infection (Klironomos 2002 ; Kulmatiski et al. 2008 ; Mitchell 2003 ; Schnitzer et al. 2011 ), are beneficial to native plants (Schnitzer et al. 2011 ; Sikes et al. 2009 ; Simard and Durall 2004 ) or can degrade the harmful allelochemicals produced by alien plants (Blum 1998 ; Ehlers 2011 ; Li et al. 2015 ). Therefore, increasing the species richness of native plant communities may suppress exotic plant invasions more strongly via the increased diversity and/or activity of soil microbial communities. If the activity of the beneficial soil microbial communities is suppressed and their diversity and abundance are reduced, the negative relationship between species diversity and community invasibility will be weakened. In invaded communities, alien species may be strongly negatively affected by some of the native soil pathogens because they have not co-evolved with those pathogens (Fries 2016 ; Zhang et al. 2020 ). As an increase in native plant species richness may increase the diversity and abundance of native soil pathogens (Hudson et al. 2006 ; Keesing et al. 2006 ), more species-rich native plant communities will likely contain native soil pathogens that negatively affect the growth of exotic plants, thus increasing their resistance to exotic plant invasions. If the activity of soil pathogens is highly suppressed and their diversity and abundance are strongly reduced, the negative relationship between species diversity and community invasibility will again be weakened. To examine how soil microbes influence the relationship between species diversity and community invasibility, we first constructed experimental native plant communities containing different levels of species richness in sterilized vs. unsterilized soils and allowed them to be invaded by each of three alien species ( Solidago canadensis , Erigeron canadensis and Symphyotrichum subulatum ), which are highly invasive in China (Guo and Fang 2003 ; He et al. 2019 ; Qiang 2001 ; Zhang et al. 2017 ). Then, the soils conditioned by the native plant communities were used as soil inocula to investigate how the soil microbes from native plant communities with different levels of species richness directly affected the growth of the three invasive plants. Specifically, we tested the following hypotheses: (1) the negative relationship between native species richness and community invasibility, indicated by invader biomass, is stronger in the presence vs. absence of soil microbes; (2) soil microbes in more diverse plant communities lead to a higher level of community invasion resistance, as measured by the biomass ratio of the native communities invaded or not invaded by the alien plant; (3) soil microbes from communities with a higher species richness have a stronger negative effect on the growth of the invasive species. Materials And Methods Native and invasive species The plant species pool consisted of eight native species and three invasive species that commonly grow on grasslands around Taizhou city, Zhejiang Province, China (Table S1). Six of the native species were perennials ( Cirsium arvense var. integrifolium , Aster indicus , Inula japonica , Viola philippica , Plantago asiatica and Lysimachia fortunei ) and two were annuals ( Solanum nigrum and Polygonum posumbu ). The three invasive species ( Solidago canadensis, Erigeron canadensis and Symphyotrichum subulatum ) were all asteraceae, as most invasive species in China are from this family (Ma 2013 ). Solidago canadensis is a perennial and can reproduce both sexually and clonally by producing rhizomes; E. canadensis and S. subulatum are non-clonal annuals. All three invasive species originated from North America and can produce plenty of viable seeds every year (Ma 2013 ). Seeds from the native and invasive species were collected from field sites around Taizhou city in 2013 (Table S1). On March 18–19, 2014, seeds from each species were surface-sterilized and sown into three plastic containers (52 cm long × 35 cm wide × 15 cm high) filled with sterilized peat (Kuheng Co., Shanghai). The plastic containers were placed in a growth chamber at 25°C and a relative humidity of 70% with 16 h of daylight at 70 µmol·m − 2 ·s − 1 . The seedlings 8–12 cm tall were used to construct native plant communities that were to be invaded or not invaded by each of the three invasive species. Height differences within the same species are limited to 2 cm. Experimental Design To test the hypotheses, we carried out two experiments. For the first experiment, we constructed native plant communities with three levels of species richness (1, 3 and 6 species) in pots (each 27.5 cm in diameter × 31 cm in height) filled with either sterilized soil (without soil microbes) or nonsterilized soil (with soil microbes) and allowed them to be invaded by each of the three alien invasive species ( S. canadensis , E. canadensis and S. subulatum ) or prevented invasion by these three species. For the treatments with soil microbes, 1.65 L soil was added to the middle layer of 14.85 L of a sterilized soil mixture, and for the treatment without soil microbes, 1.65 L sterilized soil was added to the middle layer of 14.85 L of a sterilized soil mixture. The sterilized soil mixture consisted of a mixture of soil, peat, sand and vermiculite at a volume ratio of 2:1:1:1, containing 1.60 ± 0.32 g kg − 1 total N, 0.58 ± 0.18 g kg − 1 total P and 13.2 ± 0.5 g kg − 1 organic matter ( mean ± SE , n = 5). Soil was collected from the local plant communities in mountain areas near Taizhou city with the growth of the above-mentioned eight native plants. No invasive plants grew in these selected communities. The soil was mixed and sieved through a 1-cm mesh to remove larger roots and stones. The peat, sand and vermiculite were bought from Kuheng Co. (Shanghai). We constructed three replicates of monocultures for each of the eight native species, five three-species mixtures with different species compositions and five six-species mixtures with different species compositions (Table S2). The species in each of the three- and six-species mixtures were randomly chosen from the native species pool. For the treatment without the invasive species, each pot contained six seedlings of the same native species (for monocultures), including two seedlings of each of the three species (for three-species mixtures) or one seedling of each of the six species (for six-species mixtures). The six seedlings in each pot were arranged in a circular pattern. For the treatment with the invasive species, one seedling of one of the three invasive species was grown in the center of a pot, surrounded by six seedlings of native species (Fig. 1 ). The experiment thus consisted of 34 species compositions ⋅ 2 soil microbe treatments ⋅ 4 invasion treatments, resulting in a total of 272 pots. The experiment was started on May 26, 2014. The pots were placed randomly in a greenhouse (25°C during the daytime and 18°C at night) at Taizhou University in Taizhou city, Zhejiang Province, China. The aboveground parts of each plant species in each pot were harvested on August 25–28, 2014. All plant material was oven-dried at 70°C for 48 h and weighed. The soils in each of the 34 pots without the invasive species were used as inocula for the second experiment described below. For the second experiment, 14.85 L of the same sterilized soil mixture as used in the first experiment was inoculated with 1.65 L of the soil from each of the 34 pots previously grown with the native species communities but without the invasive species. Three pots (27.5 cm in diameter × 31 cm in height) containing each of these 34 soil mixtures were prepared, and each pot contained one seedling of S. canadensis , S. subulatum or E. canadensis . There were 102 pots in total. The plant from each pot was harvested after three months, and the biomass was determined by drying the plant in an oven at 70°C for 48 h and weighing it. Data analysis The invasion resistance of a plant community was calculated as the ratio of the aboveground biomass of the community invaded by an alien species to that of the community comprising the same initial species composition but without the invasive species (Pfisterer and Schmid 2002 ; Tilman 1996 ; Wang et al. 2007 ). Complementarity and selection effects were calculated using the invasion resistance data and the additive partitioning method described by Loreau and Hector ( 2001 ). The complementarity effect of a mixture was calculated as , where N is the number of species in the mixture, is the mean value of the change in the relative invasion resistance across all species in the mixture and is the mean value of the invasion resistance of the monocultures across all species. The selection effect was calculated as N cov(Δ RY , M ), where N is the number of species, cov(Δ RY , M ) is the covariance between the invasion resistance of species in monocultures ( M ) and their change in the relative invasion resistance in the mixture (Δ RY ). If complementarity between species plays a major role in the invasion resistance, then the invasion resistance of mixtures will be higher than that of the most resistant species in the mixtures. The over-invasion resistance index ( OI ) was calculated as follows (Hector et al. 2002): OI = Y /MAX( M i ), where Y is the invasion resistance of a mixture, and M i is the invasion resistance of species i in the monoculture. If log ( OI ) > 0, the mixture should have a higher invasion resistance than that of the highest resistant species. As the damage caused by soil pathogens to invasive species may be influenced by the phylogenetic distance between native and invasive species (Strauss et al. 2006 ; Zheng et al. 2018 ), we calculated the phylogenetic distances between the eight native and three invasive species using three commonly sequenced genes from the GenBank: rbcL, matK and ITS (Table S3). Of the 11 species, eight had three genes represented in GenBank. For three native species, C. arvense var. integrifolium , I. japonica and P. asiatica whose sequence data of the three genes were not available or incomplete in GenBank, we used the sequence data from their congeneric relatives (i.e., C. arvense, I. britannica and P. depressa ) as proxies. Sequences were aligned for each region independently using MUSCLE (Edgar 2004 ) and combined into a single supermatrix. Analyses were conducted using the Maximum Composite Likelihood model (Tamura et al. 2004 ). The rate variation among sites was modeled using a gamma distribution (shape parameter = 1). All ambiguous positions were removed for each sequence pair (pairwise deletion option). Codon positions included were 1st + 2nd + 3rd + Noncoding. Evolutionary analyses were conducted in MEGA-X version 10.1.8 (Kumar et al. 2018 ; Nei and Kumar 2000 ). The weighted phylogenetic distance was calculated as follows: where R i is biomass ratio of native species i in the pot, and D i is phylogenetic distance between native species i and the invasive species. Linear regressions were performed to test the relationships between native species richness and the biomass of the native species, the biomass of the invasive species and invasion resistance, and the diversity effects (i.e., complementarity effect and selection effect) and the invasion resistance. The regression slope difference between the sterile and non-sterile treatments was tested using ANCOVA. The differences between the sterile and non-sterile treatments at the three- and six-species levels were analyzed using the t -test. The effects of soil microbes and plant species richness on the biomass of native and invasive species were also analyzed by two-way ANOVA. Linear regressions were also performed to evaluate the soil legacy effect of native species richness on the biomass of the invasive species (for the second experiment). The relationships between the weighted phylogenetic distances and the biomass of invasive species were analyzed by linear regression. All analyses were carried out using SPSS 19.0 for Windows (IBM, Armonk, NY, USA). Results Effects of soil microbes on the species richness-invasibility relationship Consistent with our first hypothesis, the presence of soil microbes changed the relationship between native species richness and the biomass of two of the three invasive species (Fig. 2 a, b), as indicated by the significant difference in the regression slopes (Fig. 2 a, ANCOVA for S. canadensis : F = 4.30, P = 0.042; Fig. 2 b, ANCOVA for E. canadensis : F = 6.01, P = 0.017). For S. subulatum , although the presence of soil microbes had no significant effect on the regression slopes of the species richness-invasibility relationships (Fig. 2 c, ANCOVA: F = 1.34, P = 0.252), the biomass of this species in the unsterilized soil was significantly lower than that in the sterilized soil in the mixtures containing three native species ( t = 4.38, n = 10, P = 0.002) and six native species ( t = 6.91, n = 10, P < 0.001). Two-way ANOVA showed that soil microbes and species richness had significant effects on the biomass of all three invasive species, and they also interacted to significantly affect the biomass of two invasive species ( S. canadensis and E. canadensis , Table 1 ). Table 1 Two-way ANOVA for effects of soil microbes and species richness on biomass of the three invasive species Microbes (M) Richness (R) M × R Species F P F P F P Solidago canadensis 10.12 0.002 16.48 < 0.001 3.44 0.038 Erigeron canadensis 12.85 0.001 26.96 < 0.001 3.40 0.040 Symphyotrichum subulatum 7.70 0.007 25.51 < 0.001 0.72 0.492 Effects Of Soil Microbes On The Invasion Resistance Of Native Plant Communities Consistent with our second hypothesis, the presence of soil microbes in more diverse plant communities resulted in a higher community invasion resistance (Fig. 3 ). In the unsterilized soil, the community invasion resistance increased with species richness for all three invasive species (Fig. 3 a-c). However, in the sterilized soil, the community invasion resistance and species richness had no relationship for S. canadensis and E. canadensis and a positive relationship for S. subulatum (Fig. 3 a-c). In the unsterilized soil, the community invasion resistance had a positive relationship with the complementarity effect for all three invasive species (Fig. 4 a-c). However, in the sterilized soil, the community invasion resistance had a positive relationship with the complementarity effect for S. subulatum , but the positive relationship was absent for S. canadensis and E. canadensis (Fig. 4 a-c). Except for S. subulatum in the unsterilized soil, the community invasion resistance was not significantly related to the selection effect (Fig. 4 d-f). In the unsterilized soil, most mixtures had positive values of the over-invasion resistance index (Fig. 5 ), indicating that these mixtures had a higher resistance than that of the most highly resistant species in the mixtures. Direct Effects Of Soil Microbes Conditioned By Native Plant Communities On Invader Growth Inconsistent with our third hypothesis, the biomass of neither S. canadensis nor S. subulatum was significantly affected by the different soil microbes trained in the native plant communities of different species richness (Fig. 6 a, c) and had no significant relationship with the weighted phylogenetic distance (Fig. 7 a, c). In addition, E. canadensis produced more biomass in the soil inoculated with soil microbes from the more diverse plant communities (Fig. 6 b), and the biomass of E. canadensis was positively correlated with the weighted phylogenetic distance (Fig. 7 b). Discussion We found that the absence of soil microbes weakened the negative species richness-invasibility relationship, indicating that soil microbes can contribute to the higher invasion resistance of more diverse native plant communities. In the presence of soil microbes, the higher invasion resistance of plant communities in more diverse communities was mainly ascribed to the complementarity effect. However, soil microbes from communities with a higher species richness did not have a consistently stronger negative effect on the growth of the three invasive species. Effects Of Soil Microbes On The Species Richness-invasibility Relationship We found significant negative relationships between native plant species and community invasibility (as measured by the invader biomass), supporting the diversity-invasibility hypothesis proposed by Elton ( 1958 ) and also agreeing with the findings of many previous studies (Adomako et al. 2019 ; Hector et al. 2001 ; Howeth 2017 ; Martignoni et al. 2020 ; Naeem et al. 2000 ; Selmants et al. 2012 ). More importantly, we found that the absence of soil microbes weakened the negative plant species richness-invasibility relationship, indicating that this relationship may be partly ascribed to the role of soil microbes. Thus, Elton’s diversity-invasibility hypothesis may be associated with the underground bio-systems. We found that the biomass of native species was significantly positively related to native species richness (Fig. S1, Table S4), as also reported in other studies (Cardinale et al. 2007 ; Cardinale et al. 2011 ; Han et al. 2021 ; Venail et al. 2015 ). However, the presence vs. absence of soil microbes did not change the relationship between the biomass and richness of native plant species (Fig. S1). These results suggest that the impact of soil microbes on the species richness-invasibility relationship was not due to its effect on the growth of native species. Effect Of Soil Microbes On The Community Invasion Resistance Compared with the absence of soil microbes, the presence of soil microbes led to a higher invasion resistance in the more diverse plant communities. Exotic plant species can affect native plants by enhancing their pathogen infection (Beckstead et al. 2010 ; Mangla and Callaway 2008 ), inhibiting mutualistic interactions (Stinson et al. 2006 ; Vogelsang and Bever 2009 ) or producing allelochemicals that are toxic to soil microbes (Inderjit and van der Putten 2010). The higher invasion resistance of the more diverse plant communities induced by soil microbes may be attributed to two mechanisms. One mechanism is that a higher level of diversity and/or abundance of microbial species in more diverse communities may lead to the stability of the underground bio-system in response to disturbance (Lankau 2010 ; Li et al. 2015 ; Zhu et al. 2011 ), which can be ascribed to a higher insurance or portfolio effect (Isbell et al. 2009 ; Wang et al. 2021 ). The other mechanism is that more diverse communities have a higher probability of including more resistant soil microbial species that influence exotic plants, i.e., a selection effect (Isbell et al. 2015 ; Wilsey et al. 2014 ). For example, the more plant species the community contains, the more microbial species the plants carry and thus the higher the probability of harboring microbial species that can degrade allelochemicals (Hiiesalu et al. 2014 ; Mitchell et al. 2010 ; Prober et al. 2015 ). Based on the results of this experiment, the complementarity effect determined the community invasion resistance. Moreover, the positive values of the over-invasion resistance index indicated the existence of facilitation among the plant species induced by soil microbes. Although the specific mechanism underlying the role of soil microbes in the diversity-resistance relationship was not further explored, we can at least be sure that the diversity-resistance relationship can be influenced by the underground bio-system. Direct Effects Of Soil Microbes On The Growth Of Invasive Plants It is well known that the species richness of native plant communities can affect the diversity, abundance and activity of soil microbes (Chen et al. 2019 ; Dassen et al. 2017 ; Schmid et al. 2019 ), including pathogens (Cappelli et al. 2020 ; Liu et al. 2021 ; Zhang et al. 2020 ). If the diversity, abundance and/or activity of soil pathogens increase with species richness in native plant communities, then soils from native plant communities with higher species richness should have a stronger negative effect on the growth of invasive plants. For instance, in a recent study, Zhang et al. ( 2020 ) showed that more species-rich plant communities contained a greater diversity of plant pathogens and thus had strong negative impacts on invasive species. However, we found that S. canadensis and S. subulatum produced a similar amount of biomass when they were grown in the soils inoculated with the soil microbes from the native plant communities with different levels of species richness, and E. canadensis even produced more biomass in the soil inoculated with the soil microbes from the more diverse plant communities. These results suggest that the effects of soil pathogens cannot explain the negative species diversity-invasibility relationship detected in the current study systems. In the present study, the effect of soil microbes on the growth of invasive species also showed no general relationship with the phylogenetic distance between the native and invasive species. There may be two reasons for the lack of impact on the richness-mediated effects of soil microbes on the growth of invasive species. One may be that increasing the species richness of native plant communities in our study did not increase the diversity, abundance or activity of soil pathogens that were harmful to the three invasive plant species. However, increasing plant species richness may increase the diversity of pathogens through amplification (Hudson et al. 2006 ; Keesing et al. 2006 ), and it may also reduce the prevalence of pathogens through dilution (Ostfeld and Keesing 2012 ; Schmidt and Ostfeld 2001 ; Zhang et al. 2020 ). The other reason may be that the effect of soil microbes on invasive plants was the net effect of the interaction between pathogenic and mutualistic soil microbes (Reinhart and Callaway 2006 ). Exotic plants have been proposed to encounter novel but strong soil mutualists, such as arbuscular mycorrhizal fungi, and benefit disproportionately from these symbiotic mutualists (Reinhart and Callaway 2006 ; Richardson et al. 2000 ). As infections with both pathogens and arbuscular mycorrhizal fungi are phylogenetically conserved, the relationship between the effect of soil microbes on invasive species and the phylogenetic distance between native and invasive species may depend on the relative role of the pathogen or arbuscular mycorrhizal fungi. Conclusions We conclude that soil microbes can alter the diversity-invasibility relationship by promoting the complementarity effect on the community invasion resistance. However, we did not find a significant role for the richness-induced difference in soil pathogens in explaining the change in the relationship. Soil pathogens and arbuscular mycorrhizal fungi in the invaded area were proven to influence invasive plants (Inderjit 2005 ; Klironomos 2002 ; Reinhart and Callaway 2006 ; Richardson et al. 2000 ). Therefore, further studies could test the way in which plant species richness alters the impact of soil pathogens vs. arbuscular mycorrhizal fungi on the growth of invasive plants to obtain a deeper understanding of the richness-invasibility relationship. Our results highlight the importance of integrating the role of soil microbes when testing the diversity-invasibility hypothesis. Declarations Acknowledgment We thank Qiao-Di Yan and Meng-Chun Shen for help with experiment, and reviewers in their papers. Contributions Conceptualization: XYW, SG, JW, FHY; Formal analysis: SG, XYW; Methodology: XYW, SG, TC, JW, FHY; Funding: XYW, SG, JW; Writing original draft: XYW, SG; Review/editing: XYW, SG, JW, FHY. Funding This work was supported by the National Natural Science Foundation of China (31870504, 41671254); Basic Public Welfare Research Projects of Zhejiang Province (LGN19C150004); Outstanding Youth Program of Taizhou University (2017JQ005, 2019JQ005); National Innovation and Entrepreneurship Program for College Students (202010350035); Natural Science Foundation of Zhejiang Province (LY22C030001, LTY22C030004); Taizhou Science and Technology Project (21hba02). Data availability The datasets generated and analysed during the current study are available on Dryad (https://doi.org/10.5061/dryad.4qrfj6qcr). Ethics declarations Conflict of interest The authors have no relevant fnancial or non-fnancial interests to disclose. Informed consent Both authors have contributed significantly to the work and agree with the content of the submission. Ethics approval Not applicable. 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Also discoverable on Platform About Our Team In Review Editorial Policies Advisory Board Help Center Resources Author Services Accessibility API Access RSS feed Manage Cookie Preferences © Research Square 2026 | ISSN 2693-5015 (online) Privacy Policy Terms of Service Do Not Sell My Personal Information {"props":{"pageProps":{"initialData":{"identity":"rs-1136323","acceptedTermsAndConditions":true,"allowDirectSubmit":false,"archivedVersions":[{"code":1,"date":"2021-12-08 21:16:35","editorialEvents":[{"type":"communityComments","content":0}],"status":"published","journal":{"display":true,"email":"[email protected]","identity":"researchsquare","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":true,"externalIdentity":"","sideBox":"","snPcode":"","submissionUrl":"/submission","title":"Research 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16:27:53","extension":"jpg","order_by":1,"title":"Figure 1","display":"","copyAsset":false,"role":"figure","size":709109,"visible":true,"origin":"","legend":"\u003cp\u003eGraphical illustration of the experimental design\u003c/p\u003e","description":"","filename":"1.jpg","url":"https://assets-eu.researchsquare.com/files/rs-1136323/v2/85689247bb0fd20ed15e16d6.jpg"},{"id":23288312,"identity":"9e9877b5-d10f-4c16-b79d-cc75809a8ea0","added_by":"auto","created_at":"2022-06-30 16:27:53","extension":"jpg","order_by":2,"title":"Figure 2","display":"","copyAsset":false,"role":"figure","size":2317940,"visible":true,"origin":"","legend":"\u003cp\u003eRelationships between species richness and biomass of each of the three invasive species in sterilized or unsterilized soil.\u0026nbsp;(a) \u003cem\u003eSolidago canadensis\u003c/em\u003e, (b) \u003cem\u003eErigeron canadensis \u003c/em\u003eand (c)\u003cem\u003e Symphyotrichum\u003c/em\u003e \u003cem\u003esubulatum.\u003c/em\u003e\u003c/p\u003e","description":"","filename":"2.jpg","url":"https://assets-eu.researchsquare.com/files/rs-1136323/v2/aaa76befb81a7e70af70e200.jpg"},{"id":23288313,"identity":"eb3d78cd-8766-463c-9bb6-e573787639ae","added_by":"auto","created_at":"2022-06-30 16:27:53","extension":"jpg","order_by":3,"title":"Figure 3","display":"","copyAsset":false,"role":"figure","size":1986702,"visible":true,"origin":"","legend":"\u003cp\u003eRelationships between species richness and the community invasion resistance in sterilized or unsterilized soil. (a) \u003cem\u003eSolidago canadensis\u003c/em\u003e, (b) \u003cem\u003eErigeron canadensis \u003c/em\u003eand (c)\u003cem\u003e Symphyotrichum\u003c/em\u003e \u003cem\u003esubulatum.\u003c/em\u003e\u003c/p\u003e","description":"","filename":"3.jpg","url":"https://assets-eu.researchsquare.com/files/rs-1136323/v2/3c2d81557854a2ddd147b4a8.jpg"},{"id":23288527,"identity":"5f8a5e5a-bc4b-4fe0-9942-e829c2b5106a","added_by":"auto","created_at":"2022-06-30 16:32:53","extension":"jpg","order_by":4,"title":"Figure 4","display":"","copyAsset":false,"role":"figure","size":3154159,"visible":true,"origin":"","legend":"\u003cp\u003eRelationships of the complementarity effect and the selection effect with the community invasion resistance in sterilized or unsterilized soil.\u0026nbsp;(a) and (d) \u003cem\u003eSolidago canadensis\u003c/em\u003e, (b) and (e) \u003cem\u003eErigeron canadensis,\u003c/em\u003e (c) and (f)\u003cem\u003e Symphyotrichum\u003c/em\u003e \u003cem\u003esubulatum.\u003c/em\u003e\u003c/p\u003e","description":"","filename":"4.jpg","url":"https://assets-eu.researchsquare.com/files/rs-1136323/v2/e8fdd425e6c5bbfc61cabbc4.jpg"},{"id":23288319,"identity":"659c164c-b4fc-4664-bfc0-72799cdbe40c","added_by":"auto","created_at":"2022-06-30 16:27:53","extension":"jpg","order_by":5,"title":"Figure 5","display":"","copyAsset":false,"role":"figure","size":1162457,"visible":true,"origin":"","legend":"\u003cp\u003eEffects of species richness on the over-invasion resistance index of plant communities in sterilized or unsterilized soil.\u003c/p\u003e","description":"","filename":"5.jpg","url":"https://assets-eu.researchsquare.com/files/rs-1136323/v2/b00468b7c7258a146461d635.jpg"},{"id":23288316,"identity":"461f9e93-d4af-4a69-b6ba-30c08d4bd7f7","added_by":"auto","created_at":"2022-06-30 16:27:53","extension":"jpg","order_by":6,"title":"Figure 6","display":"","copyAsset":false,"role":"figure","size":1401175,"visible":true,"origin":"","legend":"\u003cp\u003eEffects of trained soil microbes by plant communities with different species richness on biomass of each of the three invasive species. (A) \u003cem\u003eSolidago canadensis\u003c/em\u003e, (B) \u003cem\u003eErigeron canadensis \u003c/em\u003eand (C)\u003cem\u003e Symphyotrichum\u003c/em\u003e \u003cem\u003esubulatum.\u003c/em\u003e\u003c/p\u003e","description":"","filename":"6.jpg","url":"https://assets-eu.researchsquare.com/files/rs-1136323/v2/707fb837cbadc82ca6d8655b.jpg"},{"id":23288317,"identity":"72978d6f-8417-4177-9812-ca7d92ebff10","added_by":"auto","created_at":"2022-06-30 16:27:53","extension":"jpg","order_by":7,"title":"Figure 7","display":"","copyAsset":false,"role":"figure","size":1647030,"visible":true,"origin":"","legend":"\u003cp\u003eRelationships between phylogenetic distance and biomass of each of the three invasive species. (a) \u003cem\u003eSolidago canadensis\u003c/em\u003e, (b) \u003cem\u003eErigeron canadensis \u003c/em\u003eand (c)\u003cem\u003e Symphyotrichum\u003c/em\u003e \u003cem\u003esubulatum.\u003c/em\u003e\u003c/p\u003e","description":"","filename":"7.jpg","url":"https://assets-eu.researchsquare.com/files/rs-1136323/v2/18e7bbf631d7aabfb70e2feb.jpg"},{"id":44715100,"identity":"05dd7eed-d7e2-4b99-8754-c52236df769b","added_by":"auto","created_at":"2023-10-16 18:13:09","extension":"pdf","order_by":0,"title":"","display":"","copyAsset":false,"role":"manuscript-pdf","size":2774416,"visible":true,"origin":"","legend":"","description":"","filename":"manuscript.pdf","url":"https://assets-eu.researchsquare.com/files/rs-1136323/v2/d793f203-58ed-4d9f-b374-aaade1904c37.pdf"},{"id":23288528,"identity":"b4456c06-ed0c-4b32-b9ea-2916937bfdc6","added_by":"auto","created_at":"2022-06-30 16:32:53","extension":"docx","order_by":5,"title":"","display":"","copyAsset":false,"role":"supplement","size":476309,"visible":true,"origin":"","legend":"","description":"","filename":"SupplementaryInformationSI.docx","url":"https://assets-eu.researchsquare.com/files/rs-1136323/v2/4b64097a9160b47597ab151b.docx"}],"financialInterests":"","formattedTitle":"Soil microbes alter the diversity-invasibility relationship by promoting a complementarity effect on community invasion resistance","fulltext":[{"header":"Introduction","content":"\u003cp\u003eThe ability of native plant communities to resist alien plant invasions has received a great deal of attention (Dawson and Schrama \u003cspan citationid=\"CR12\" class=\"CitationRef\"\u003e2016\u003c/span\u003e; Hess et al. \u003cspan citationid=\"CR22\" class=\"CitationRef\"\u003e2020\u003c/span\u003e; Urza et al. \u003cspan citationid=\"CR70\" class=\"CitationRef\"\u003e2019\u003c/span\u003e) due to the broad spread of alien species and their threats to native ecosystems (Cazetta and Zenni \u003cspan citationid=\"CR8\" class=\"CitationRef\"\u003e2020\u003c/span\u003e; Pearson et al. \u003cspan citationid=\"CR52\" class=\"CitationRef\"\u003e2018\u003c/span\u003e; Pyšek et al. \u003cspan citationid=\"CR55\" class=\"CitationRef\"\u003e2020\u003c/span\u003e). Elton (\u003cspan citationid=\"CR15\" class=\"CitationRef\"\u003e1958\u003c/span\u003e) proposed that communities with greater species richness are more resistant to alien plant invasions. Although many experimental studies have supported this hypothesis (Adomako et al. \u003cspan citationid=\"CR1\" class=\"CitationRef\"\u003e2019\u003c/span\u003e; Hector et al. \u003cspan citationid=\"CR20\" class=\"CitationRef\"\u003e2001\u003c/span\u003e; Howeth \u003cspan citationid=\"CR25\" class=\"CitationRef\"\u003e2017\u003c/span\u003e; Martignoni et al. \u003cspan citationid=\"CR45\" class=\"CitationRef\"\u003e2020\u003c/span\u003e; Naeem et al. \u003cspan citationid=\"CR49\" class=\"CitationRef\"\u003e2000\u003c/span\u003e; Selmants et al. \u003cspan citationid=\"CR62\" class=\"CitationRef\"\u003e2012\u003c/span\u003e), species richness has also been found to have either no or a negative impact on the invasion resistance of native plant communities (Crawley et al. \u003cspan citationid=\"CR10\" class=\"CitationRef\"\u003e1999\u003c/span\u003e; Lannes et al. \u003cspan citationid=\"CR38\" class=\"CitationRef\"\u003e2020\u003c/span\u003e; Smith et al. \u003cspan citationid=\"CR65\" class=\"CitationRef\"\u003e2004\u003c/span\u003e; Zeiter and Stampfli \u003cspan citationid=\"CR79\" class=\"CitationRef\"\u003e2012\u003c/span\u003e). Soil microbes can affect both the invasiveness of alien species and the invasibility of native plant communities (Beckstead and Parker \u003cspan citationid=\"CR2\" class=\"CitationRef\"\u003e2003\u003c/span\u003e; Dawson and Schrama \u003cspan citationid=\"CR12\" class=\"CitationRef\"\u003e2016\u003c/span\u003e; Klironomos \u003cspan citationid=\"CR33\" class=\"CitationRef\"\u003e2002\u003c/span\u003e; van der Putten et al. \u003cspan citationid=\"CR71\" class=\"CitationRef\"\u003e2007\u003c/span\u003e). However, it remains unclear how soil microbes affect the plant diversity-invasibility relationship and what the underlying mechanisms may be.\u003c/p\u003e \u003cp\u003eExotic plants can suppress native plants via their impacts on soil microbes (Inderjit et al. 2021; Lankau \u003cspan citationid=\"CR37\" class=\"CitationRef\"\u003e2011\u003c/span\u003e; Vogelsang and Bever \u003cspan citationid=\"CR73\" class=\"CitationRef\"\u003e2009\u003c/span\u003e). For instance, exotic plants can enhance native plant pathogen levels (Beckstead et al. \u003cspan citationid=\"CR3\" class=\"CitationRef\"\u003e2010\u003c/span\u003e; Lankau \u003cspan citationid=\"CR37\" class=\"CitationRef\"\u003e2011\u003c/span\u003e; Mangla and Callaway \u003cspan citationid=\"CR44\" class=\"CitationRef\"\u003e2008\u003c/span\u003e), inhibit soil microbes that have a mutualistic relationship with native plants (e.g., some arbuscular mycorrhizal fungi; Lankau \u003cspan citationid=\"CR37\" class=\"CitationRef\"\u003e2011\u003c/span\u003e; Stinson et al. \u003cspan citationid=\"CR66\" class=\"CitationRef\"\u003e2006\u003c/span\u003e; Vogelsang and Bever \u003cspan citationid=\"CR73\" class=\"CitationRef\"\u003e2009\u003c/span\u003e) or produce allelochemicals that are toxic to these beneficial soil microbes (Inderjit et al. 2021; Inderjit and van der Putten 2010; Lankau \u003cspan citationid=\"CR36\" class=\"CitationRef\"\u003e2010\u003c/span\u003e). Increasing species richness in native plant communities can provide more diverse food resources (root exudates and litter) and increase the available habitats for soil microbes (Hooper et al. \u003cspan citationid=\"CR24\" class=\"CitationRef\"\u003e2000\u003c/span\u003e; Millard and Singh \u003cspan citationid=\"CR46\" class=\"CitationRef\"\u003e2010\u003c/span\u003e; Prober et al. \u003cspan citationid=\"CR54\" class=\"CitationRef\"\u003e2015\u003c/span\u003e; Wardle \u003cspan citationid=\"CR77\" class=\"CitationRef\"\u003e2006\u003c/span\u003e), thus increasing their biomass, activities and diversity (Hiiesalu et al. \u003cspan citationid=\"CR23\" class=\"CitationRef\"\u003e2014\u003c/span\u003e; Liu et al. \u003cspan citationid=\"CR40\" class=\"CitationRef\"\u003e2020\u003c/span\u003e; Mitchell et al. \u003cspan citationid=\"CR48\" class=\"CitationRef\"\u003e2010\u003c/span\u003e; Prober et al. \u003cspan citationid=\"CR54\" class=\"CitationRef\"\u003e2015\u003c/span\u003e; Wang et al. \u003cspan citationid=\"CR75\" class=\"CitationRef\"\u003e2017\u003c/span\u003e). Consequently, native plant communities that are more species-rich may be more likely to harbor soil microbes that can help the native plants to resist invasion-mediated pathogen infection (Klironomos \u003cspan citationid=\"CR33\" class=\"CitationRef\"\u003e2002\u003c/span\u003e; Kulmatiski et al. \u003cspan citationid=\"CR34\" class=\"CitationRef\"\u003e2008\u003c/span\u003e; Mitchell \u003cspan citationid=\"CR47\" class=\"CitationRef\"\u003e2003\u003c/span\u003e; Schnitzer et al. \u003cspan citationid=\"CR61\" class=\"CitationRef\"\u003e2011\u003c/span\u003e), are beneficial to native plants (Schnitzer et al. \u003cspan citationid=\"CR61\" class=\"CitationRef\"\u003e2011\u003c/span\u003e; Sikes et al. \u003cspan citationid=\"CR63\" class=\"CitationRef\"\u003e2009\u003c/span\u003e; Simard and Durall \u003cspan citationid=\"CR64\" class=\"CitationRef\"\u003e2004\u003c/span\u003e) or can degrade the harmful allelochemicals produced by alien plants (Blum \u003cspan citationid=\"CR4\" class=\"CitationRef\"\u003e1998\u003c/span\u003e; Ehlers \u003cspan citationid=\"CR14\" class=\"CitationRef\"\u003e2011\u003c/span\u003e; Li et al. \u003cspan citationid=\"CR39\" class=\"CitationRef\"\u003e2015\u003c/span\u003e). Therefore, increasing the species richness of native plant communities may suppress exotic plant invasions more strongly via the increased diversity and/or activity of soil microbial communities. If the activity of the beneficial soil microbial communities is suppressed and their diversity and abundance are reduced, the negative relationship between species diversity and community invasibility will be weakened.\u003c/p\u003e \u003cp\u003eIn invaded communities, alien species may be strongly negatively affected by some of the native soil pathogens because they have not co-evolved with those pathogens (Fries \u003cspan citationid=\"CR16\" class=\"CitationRef\"\u003e2016\u003c/span\u003e; Zhang et al. \u003cspan citationid=\"CR81\" class=\"CitationRef\"\u003e2020\u003c/span\u003e). As an increase in native plant species richness may increase the diversity and abundance of native soil pathogens (Hudson et al. \u003cspan citationid=\"CR26\" class=\"CitationRef\"\u003e2006\u003c/span\u003e; Keesing et al. \u003cspan citationid=\"CR32\" class=\"CitationRef\"\u003e2006\u003c/span\u003e), more species-rich native plant communities will likely contain native soil pathogens that negatively affect the growth of exotic plants, thus increasing their resistance to exotic plant invasions. If the activity of soil pathogens is highly suppressed and their diversity and abundance are strongly reduced, the negative relationship between species diversity and community invasibility will again be weakened.\u003c/p\u003e \u003cp\u003eTo examine how soil microbes influence the relationship between species diversity and community invasibility, we first constructed experimental native plant communities containing different levels of species richness in sterilized vs. unsterilized soils and allowed them to be invaded by each of three alien species (\u003cem\u003eSolidago canadensis\u003c/em\u003e, \u003cem\u003eErigeron canadensis\u003c/em\u003e and \u003cem\u003eSymphyotrichum subulatum\u003c/em\u003e), which are highly invasive in China (Guo and Fang \u003cspan citationid=\"CR17\" class=\"CitationRef\"\u003e2003\u003c/span\u003e; He et al. \u003cspan citationid=\"CR19\" class=\"CitationRef\"\u003e2019\u003c/span\u003e; Qiang \u003cspan citationid=\"CR56\" class=\"CitationRef\"\u003e2001\u003c/span\u003e; Zhang et al. \u003cspan citationid=\"CR80\" class=\"CitationRef\"\u003e2017\u003c/span\u003e). Then, the soils conditioned by the native plant communities were used as soil inocula to investigate how the soil microbes from native plant communities with different levels of species richness directly affected the growth of the three invasive plants. Specifically, we tested the following hypotheses: (1) the negative relationship between native species richness and community invasibility, indicated by invader biomass, is stronger in the presence vs. absence of soil microbes; (2) soil microbes in more diverse plant communities lead to a higher level of community invasion resistance, as measured by the biomass ratio of the native communities invaded or not invaded by the alien plant; (3) soil microbes from communities with a higher species richness have a stronger negative effect on the growth of the invasive species.\u003c/p\u003e"},{"header":"Materials And Methods","content":"\u003cdiv id=\"Sec3\" class=\"Section2\"\u003e \u003ch2\u003eNative and invasive species\u003c/h2\u003e \u003cp\u003eThe plant species pool consisted of eight native species and three invasive species that commonly grow on grasslands around Taizhou city, Zhejiang Province, China (Table S1). Six of the native species were perennials (\u003cem\u003eCirsium arvense\u003c/em\u003e var. \u003cem\u003eintegrifolium\u003c/em\u003e, \u003cem\u003eAster indicus\u003c/em\u003e, \u003cem\u003eInula japonica\u003c/em\u003e, \u003cem\u003eViola philippica\u003c/em\u003e, \u003cem\u003ePlantago asiatica\u003c/em\u003e and \u003cem\u003eLysimachia fortunei\u003c/em\u003e) and two were annuals (\u003cem\u003eSolanum nigrum\u003c/em\u003e and \u003cem\u003ePolygonum posumbu\u003c/em\u003e). The three invasive species (\u003cem\u003eSolidago canadensis, Erigeron canadensis\u003c/em\u003e and \u003cem\u003eSymphyotrichum subulatum\u003c/em\u003e) were all asteraceae, as most invasive species in China are from this family (Ma \u003cspan citationid=\"CR43\" class=\"CitationRef\"\u003e2013\u003c/span\u003e). \u003cem\u003eSolidago canadensis\u003c/em\u003e is a perennial and can reproduce both sexually and clonally by producing rhizomes; \u003cem\u003eE. canadensis\u003c/em\u003e and \u003cem\u003eS. subulatum\u003c/em\u003e are non-clonal annuals. All three invasive species originated from North America and can produce plenty of viable seeds every year (Ma \u003cspan citationid=\"CR43\" class=\"CitationRef\"\u003e2013\u003c/span\u003e).\u003c/p\u003e \u003cp\u003eSeeds from the native and invasive species were collected from field sites around Taizhou city in 2013 (Table S1). On March 18\u0026ndash;19, 2014, seeds from each species were surface-sterilized and sown into three plastic containers (52 cm long \u0026times; 35 cm wide \u0026times; 15 cm high) filled with sterilized peat (Kuheng Co., Shanghai). The plastic containers were placed in a growth chamber at 25\u0026deg;C and a relative humidity of 70% with 16 h of daylight at 70 \u0026micro;mol\u0026middot;m\u003csup\u003e\u0026minus;\u0026thinsp;2\u003c/sup\u003e\u0026middot;s\u003csup\u003e\u0026minus;\u0026thinsp;1\u003c/sup\u003e. The seedlings 8\u0026ndash;12 cm tall were used to construct native plant communities that were to be invaded or not invaded by each of the three invasive species. Height differences within the same species are limited to 2 cm.\u003c/p\u003e \u003c/div\u003e\n\u003ch2\u003eExperimental Design\u003ch2\u003e\n\u003cp\u003eTo test the hypotheses, we carried out two experiments. For the first experiment, we constructed native plant communities with three levels of species richness (1, 3 and 6 species) in pots (each 27.5 cm in diameter \u0026times; 31 cm in height) filled with either sterilized soil (without soil microbes) or nonsterilized soil (with soil microbes) and allowed them to be invaded by each of the three alien invasive species (\u003cem\u003eS. canadensis\u003c/em\u003e, \u003cem\u003eE. canadensis\u003c/em\u003e and \u003cem\u003eS. subulatum\u003c/em\u003e) or prevented invasion by these three species. For the treatments with soil microbes, 1.65 L soil was added to the middle layer of 14.85 L of a sterilized soil mixture, and for the treatment without soil microbes, 1.65 L sterilized soil was added to the middle layer of 14.85 L of a sterilized soil mixture. The sterilized soil mixture consisted of a mixture of soil, peat, sand and vermiculite at a volume ratio of 2:1:1:1, containing 1.60\u0026thinsp;\u0026plusmn;\u0026thinsp;0.32 g kg\u003csup\u003e\u0026minus;\u0026thinsp;1\u003c/sup\u003e total N, 0.58\u0026thinsp;\u0026plusmn;\u0026thinsp;0.18 g kg\u003csup\u003e\u0026minus;\u0026thinsp;1\u003c/sup\u003e total P and 13.2\u0026thinsp;\u0026plusmn;\u0026thinsp;0.5 g kg\u003csup\u003e\u0026minus;\u0026thinsp;1\u003c/sup\u003e organic matter (\u003cem\u003emean\u003c/em\u003e\u0026thinsp;\u0026plusmn;\u0026thinsp;\u003cem\u003eSE\u003c/em\u003e, \u003cem\u003en\u003c/em\u003e\u0026thinsp;=\u0026thinsp;5). Soil was collected from the local plant communities in mountain areas near Taizhou city with the growth of the above-mentioned eight native plants. No invasive plants grew in these selected communities. The soil was mixed and sieved through a 1-cm mesh to remove larger roots and stones. The peat, sand and vermiculite were bought from Kuheng Co. (Shanghai).\u003c/p\u003e\n\u003cp\u003eWe constructed three replicates of monocultures for each of the eight native species, five three-species mixtures with different species compositions and five six-species mixtures with different species compositions (Table S2). The species in each of the three- and six-species mixtures were randomly chosen from the native species pool. For the treatment without the invasive species, each pot contained six seedlings of the same native species (for monocultures), including two seedlings of each of the three species (for three-species mixtures) or one seedling of each of the six species (for six-species mixtures). The six seedlings in each pot were arranged in a circular pattern. For the treatment with the invasive species, one seedling of one of the three invasive species was grown in the center of a pot, surrounded by six seedlings of native species (Fig.\u0026nbsp;\u003cspan class=\"InternalRef\"\u003e1\u003c/span\u003e). The experiment thus consisted of 34 species compositions \u0026sdot; 2 soil microbe treatments \u0026sdot; 4 invasion treatments, resulting in a total of 272 pots.\u003c/p\u003e\n\u003cp\u003e\u003cbr\u003e\u003c/p\u003e\n\u003cp\u003eThe experiment was started on May 26, 2014. The pots were placed randomly in a greenhouse (25\u0026deg;C during the daytime and 18\u0026deg;C at night) at Taizhou University in Taizhou city, Zhejiang Province, China. The aboveground parts of each plant species in each pot were harvested on August 25\u0026ndash;28, 2014. All plant material was oven-dried at 70\u0026deg;C for 48 h and weighed. The soils in each of the 34 pots without the invasive species were used as inocula for the second experiment described below.\u003c/p\u003e\n\u003cp\u003eFor the second experiment, 14.85 L of the same sterilized soil mixture as used in the first experiment was inoculated with 1.65 L of the soil from each of the 34 pots previously grown with the native species communities but without the invasive species. Three pots (27.5 cm in diameter \u0026times; 31 cm in height) containing each of these 34 soil mixtures were prepared, and each pot contained one seedling of \u003cem\u003eS. canadensis\u003c/em\u003e, \u003cem\u003eS. subulatum\u003c/em\u003e or \u003cem\u003eE. canadensis\u003c/em\u003e. There were 102 pots in total. The plant from each pot was harvested after three months, and the biomass was determined by drying the plant in an oven at 70\u0026deg;C for 48 h and weighing it.\u003c/p\u003e\n\u003cdiv class=\"Section2\" id=\"Sec5\"\u003e\n \u003ch2\u003eData analysis\u003c/h2\u003e\n \u003cp\u003eThe invasion resistance of a plant community was calculated as the ratio of the aboveground biomass of the community invaded by an alien species to that of the community comprising the same initial species composition but without the invasive species (Pfisterer and Schmid \u003cspan class=\"CitationRef\"\u003e2002\u003c/span\u003e; Tilman \u003cspan class=\"CitationRef\"\u003e1996\u003c/span\u003e; Wang et al. \u003cspan class=\"CitationRef\"\u003e2007\u003c/span\u003e). Complementarity and selection effects were calculated using the invasion resistance data and the additive partitioning method described by Loreau and Hector (\u003cspan class=\"CitationRef\"\u003e2001\u003c/span\u003e). The complementarity effect of a mixture was calculated as \u003cimg src=\"https://myfiles.space/user_files/120476_695e7dc7a8d3b6b1/120476_custom_files/img1656569598.JPG\"\u003e, where \u003cem\u003eN\u003c/em\u003e is the number of species in the mixture,\u003cimg src=\"https://myfiles.space/user_files/120476_695e7dc7a8d3b6b1/120476_custom_files/img1656569636.JPG\"\u003e is the mean value of the change in the relative invasion resistance across all species in the mixture and is \u003cimg src=\"https://myfiles.space/user_files/120476_695e7dc7a8d3b6b1/120476_custom_files/img1656569659.JPG\"\u003ethe mean value of the invasion resistance of the monocultures across all species. The selection effect was calculated as \u003cem\u003eN\u003c/em\u003ecov(\u0026Delta;\u003cem\u003eRY\u003c/em\u003e, \u003cem\u003eM\u003c/em\u003e), where \u003cem\u003eN\u003c/em\u003e is the number of species, cov(\u0026Delta;\u003cem\u003eRY\u003c/em\u003e, \u003cem\u003eM\u003c/em\u003e) is the covariance between the invasion resistance of species in monocultures (\u003cem\u003eM\u003c/em\u003e) and their change in the relative invasion resistance in the mixture (\u0026Delta;\u003cem\u003eRY\u003c/em\u003e).\u003c/p\u003e\n \u003cp\u003eIf complementarity between species plays a major role in the invasion resistance, then the invasion resistance of mixtures will be higher than that of the most resistant species in the mixtures. The over-invasion resistance index (\u003cem\u003eOI\u003c/em\u003e) was calculated as follows (Hector et al. 2002): \u003cem\u003eOI\u003c/em\u003e\u0026thinsp;=\u0026thinsp;\u003cem\u003eY\u003c/em\u003e/MAX(\u003cem\u003eM\u003c/em\u003e\u003csub\u003ei\u003c/sub\u003e), where \u003cem\u003eY\u003c/em\u003e is the invasion resistance of a mixture, and \u003cem\u003eM\u003c/em\u003e\u003csub\u003ei\u003c/sub\u003e is the invasion resistance of species \u003cem\u003ei\u003c/em\u003e in the monoculture. If log (\u003cem\u003eOI\u003c/em\u003e)\u0026thinsp;\u0026gt;\u0026thinsp;0, the mixture should have a higher invasion resistance than that of the highest resistant species.\u003c/p\u003e\n \u003cp\u003eAs the damage caused by soil pathogens to invasive species may be influenced by the phylogenetic distance between native and invasive species (Strauss et al. \u003cspan class=\"CitationRef\"\u003e2006\u003c/span\u003e; Zheng et al. \u003cspan class=\"CitationRef\"\u003e2018\u003c/span\u003e), we calculated the phylogenetic distances between the eight native and three invasive species using three commonly sequenced genes from the GenBank: rbcL, matK and ITS (Table S3). Of the 11 species, eight had three genes represented in GenBank. For three native species, \u003cem\u003eC. arvense\u003c/em\u003e var. \u003cem\u003eintegrifolium\u003c/em\u003e, \u003cem\u003eI. japonica\u003c/em\u003e and \u003cem\u003eP. asiatica\u003c/em\u003e whose sequence data of the three genes were not available or incomplete in GenBank, we used the sequence data from their congeneric relatives (i.e., \u003cem\u003eC. arvense, I. britannica\u003c/em\u003e and \u003cem\u003eP. depressa\u003c/em\u003e) as proxies. Sequences were aligned for each region independently using MUSCLE (Edgar \u003cspan class=\"CitationRef\"\u003e2004\u003c/span\u003e) and combined into a single supermatrix. Analyses were conducted using the Maximum Composite Likelihood model (Tamura et al. \u003cspan class=\"CitationRef\"\u003e2004\u003c/span\u003e). The rate variation among sites was modeled using a gamma distribution (shape parameter\u0026thinsp;=\u0026thinsp;1). All ambiguous positions were removed for each sequence pair (pairwise deletion option). Codon positions included were 1st\u0026thinsp;+\u0026thinsp;2nd\u0026thinsp;+\u0026thinsp;3rd\u0026thinsp;+\u0026thinsp;Noncoding. Evolutionary analyses were conducted in MEGA-X version 10.1.8 (Kumar et al. \u003cspan class=\"CitationRef\"\u003e2018\u003c/span\u003e; Nei and Kumar \u003cspan class=\"CitationRef\"\u003e2000\u003c/span\u003e). The weighted phylogenetic distance was calculated as follows:\u003c/p\u003e\n \u003cp\u003e\u003cimg src=\"https://myfiles.space/user_files/120476_695e7dc7a8d3b6b1/120476_custom_files/img1656569675.JPG\"\u003e\u003c/p\u003e\n \u003cp\u003ewhere \u003cem\u003eR\u003c/em\u003e\u003csub\u003ei\u003c/sub\u003e is biomass ratio of native species \u003cem\u003ei\u003c/em\u003e in the pot, and \u003cem\u003eD\u003c/em\u003e\u003csub\u003ei\u003c/sub\u003e is phylogenetic distance between native species \u003cem\u003ei\u003c/em\u003e and the invasive species.\u003c/p\u003e\n \u003cp\u003eLinear regressions were performed to test the relationships between native species richness and the biomass of the native species, the biomass of the invasive species and invasion resistance, and the diversity effects (i.e., complementarity effect and selection effect) and the invasion resistance. The regression slope difference between the sterile and non-sterile treatments was tested using ANCOVA. The differences between the sterile and non-sterile treatments at the three- and six-species levels were analyzed using the \u003cem\u003et\u003c/em\u003e-test. The effects of soil microbes and plant species richness on the biomass of native and invasive species were also analyzed by two-way ANOVA. Linear regressions were also performed to evaluate the soil legacy effect of native species richness on the biomass of the invasive species (for the second experiment). The relationships between the weighted phylogenetic distances and the biomass of invasive species were analyzed by linear regression. All analyses were carried out using SPSS 19.0 for Windows (IBM, Armonk, NY, USA).\u003c/p\u003e\n\u003c/div\u003e"},{"header":"Results","content":"\u003cdiv class=\"Section2\" id=\"Sec7\"\u003e\n \u003ch2\u003eEffects of soil microbes on the species richness-invasibility relationship\u003c/h2\u003e\n \u003cp\u003eConsistent with our first hypothesis, the presence of soil microbes changed the relationship between native species richness and the biomass of two of the three invasive species (Fig. \u003cspan class=\"InternalRef\"\u003e2\u003c/span\u003ea, b), as indicated by the significant difference in the regression slopes (Fig. \u003cspan class=\"InternalRef\"\u003e2\u003c/span\u003ea, ANCOVA for \u003cem\u003eS. canadensis\u003c/em\u003e: \u003cem\u003eF\u003c/em\u003e\u0026thinsp;=\u0026thinsp;4.30, \u003cem\u003eP\u003c/em\u003e\u0026thinsp;=\u0026thinsp;0.042; Fig. \u003cspan class=\"InternalRef\"\u003e2\u003c/span\u003eb, ANCOVA for \u003cem\u003eE. canadensis\u003c/em\u003e: \u003cem\u003eF\u003c/em\u003e\u0026thinsp;=\u0026thinsp;6.01, \u003cem\u003eP\u003c/em\u003e\u0026thinsp;=\u0026thinsp;0.017). For \u003cem\u003eS. subulatum\u003c/em\u003e, although the presence of soil microbes had no significant effect on the regression slopes of the species richness-invasibility relationships (Fig. \u003cspan class=\"InternalRef\"\u003e2\u003c/span\u003ec, ANCOVA: \u003cem\u003eF\u003c/em\u003e\u0026thinsp;=\u0026thinsp;1.34, \u003cem\u003eP\u003c/em\u003e\u0026thinsp;=\u0026thinsp;0.252), the biomass of this species in the unsterilized soil was significantly lower than that in the sterilized soil in the mixtures containing three native species (\u003cem\u003et\u003c/em\u003e\u0026thinsp;=\u0026thinsp;4.38, \u003cem\u003en\u003c/em\u003e\u0026thinsp;=\u0026thinsp;10, \u003cem\u003eP\u003c/em\u003e\u0026thinsp;=\u0026thinsp;0.002) and six native species (\u003cem\u003et\u003c/em\u003e\u0026thinsp;=\u0026thinsp;6.91, \u003cem\u003en\u003c/em\u003e\u0026thinsp;=\u0026thinsp;10, \u003cem\u003eP\u003c/em\u003e\u0026thinsp;\u0026lt;\u0026thinsp;0.001). Two-way ANOVA showed that soil microbes and species richness had significant effects on the biomass of all three invasive species, and they also interacted to significantly affect the biomass of two invasive species (\u003cem\u003eS. canadensis\u003c/em\u003e and \u003cem\u003eE. canadensis\u003c/em\u003e, Table \u003cspan class=\"InternalRef\"\u003e1\u003c/span\u003e).\u003c/p\u003e\n \u003cdiv align=\"left\" class=\"colspec\"\u003e\u003cbr\u003e\u003c/div\u003e\u0026nbsp;\u0026nbsp;\u003ctable border=\"1\" id=\"Tab1\"\u003e\n \u003ccaption language=\"En\"\u003e\n \u003cdiv class=\"CaptionNumber\"\u003eTable 1\u003c/div\u003e\n \u003cdiv class=\"CaptionContent\"\u003e\n \u003cp\u003eTwo-way ANOVA for effects of soil microbes and species richness on biomass of the three invasive species\u003c/p\u003e\n \u003c/div\u003e\n \u003c/caption\u003e\n \u003cthead\u003e\n \u003ctr\u003e\n \u003cth align=\"left\" style=\"width: 36.4516%;\"\u003e\u0026nbsp;\u003c/th\u003e\n \u003cth align=\"left\" colspan=\"2\" style=\"width: 19.3548%;\"\u003e\n \u003cp\u003eMicrobes (M)\u003c/p\u003e\n \u003c/th\u003e\n \u003cth align=\"left\" colspan=\"2\" style=\"width: 19.3548%;\"\u003e\n \u003cp\u003eRichness (R)\u003c/p\u003e\n \u003c/th\u003e\n \u003cth align=\"left\" colspan=\"2\" style=\"width: 14.3548%;\"\u003e\n \u003cp\u003eM \u0026times; R\u003c/p\u003e\n \u003c/th\u003e\n \u003c/tr\u003e\n \u003c/thead\u003e\n \u003ctbody\u003e\n \u003ctr\u003e\n \u003ctd align=\"left\" style=\"width: 36.4516%;\"\u003e\n \u003cp\u003eSpecies\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\" style=\"width: 9.6774%;\"\u003e\n \u003cp\u003e\u003cem\u003eF\u003c/em\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\" style=\"width: 9.6774%;\"\u003e\n \u003cp\u003e\u003cem\u003eP\u003c/em\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\" style=\"width: 7.7419%;\"\u003e\n \u003cp\u003e\u003cem\u003eF\u003c/em\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\" style=\"width: 11.6129%;\"\u003e\n \u003cp\u003e\u003cem\u003eP\u003c/em\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\" style=\"width: 6.2903%;\"\u003e\n \u003cp\u003e\u003cem\u003eF\u003c/em\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\" style=\"width: 7.9032%;\"\u003e\n \u003cp\u003e\u003cem\u003eP\u003c/em\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd align=\"left\" style=\"width: 36.4516%;\"\u003e\n \u003cp\u003e\u003cem\u003eSolidago canadensis\u003c/em\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\" style=\"width: 9.6774%;\"\u003e\n \u003cp\u003e10.12\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\" style=\"width: 9.6774%;\"\u003e\n \u003cp\u003e\u003cstrong\u003e0.002\u003c/strong\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\" style=\"width: 7.7419%;\"\u003e\n \u003cp\u003e16.48\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\" style=\"width: 11.6129%;\"\u003e\n \u003cp\u003e\u003cstrong\u003e\u0026lt;\u0026thinsp;0.001\u003c/strong\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\" style=\"width: 6.2903%;\"\u003e\n \u003cp\u003e3.44\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\" style=\"width: 7.9032%;\"\u003e\n \u003cp\u003e\u003cstrong\u003e0.038\u003c/strong\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd align=\"left\" style=\"width: 36.4516%;\"\u003e\n \u003cp\u003e\u003cem\u003eErigeron canadensis\u003c/em\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\" style=\"width: 9.6774%;\"\u003e\n \u003cp\u003e12.85\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\" style=\"width: 9.6774%;\"\u003e\n \u003cp\u003e\u003cstrong\u003e0.001\u003c/strong\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\" style=\"width: 7.7419%;\"\u003e\n \u003cp\u003e26.96\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\" style=\"width: 11.6129%;\"\u003e\n \u003cp\u003e\u003cstrong\u003e\u0026lt;\u0026thinsp;0.001\u003c/strong\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\" style=\"width: 6.2903%;\"\u003e\n \u003cp\u003e3.40\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\" style=\"width: 7.9032%;\"\u003e\n \u003cp\u003e\u003cstrong\u003e0.040\u003c/strong\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd align=\"left\" style=\"width: 36.4516%;\"\u003e\n \u003cp\u003e\u003cem\u003eSymphyotrichum subulatum\u003c/em\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\" style=\"width: 9.6774%;\"\u003e\n \u003cp\u003e7.70\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\" style=\"width: 9.6774%;\"\u003e\n \u003cp\u003e\u003cstrong\u003e0.007\u003c/strong\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\" style=\"width: 7.7419%;\"\u003e\n \u003cp\u003e25.51\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\" style=\"width: 11.6129%;\"\u003e\n \u003cp\u003e\u003cstrong\u003e\u0026lt;\u0026thinsp;0.001\u003c/strong\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\" style=\"width: 6.2903%;\"\u003e\n \u003cp\u003e0.72\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\" style=\"width: 7.9032%;\"\u003e\n \u003cp\u003e0.492\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003c/tbody\u003e\n \u003c/table\u003e\n \u003cp\u003e\u003c/p\u003e\n\u003c/div\u003e\n\u003ch2\u003eEffects Of Soil Microbes On The Invasion Resistance Of Native Plant Communities\u003c/h2\u003e\n\u003cp\u003eConsistent with our second hypothesis, the presence of soil microbes in more diverse plant communities resulted in a higher community invasion resistance (Fig. \u003cspan class=\"InternalRef\"\u003e3\u003c/span\u003e). In the unsterilized soil, the community invasion resistance increased with species richness for all three invasive species (Fig. \u003cspan class=\"InternalRef\"\u003e3\u003c/span\u003ea-c). However, in the sterilized soil, the community invasion resistance and species richness had no relationship for \u003cem\u003eS. canadensis\u003c/em\u003e and \u003cem\u003eE. canadensis\u003c/em\u003e and a positive relationship for \u003cem\u003eS. subulatum\u003c/em\u003e (Fig. \u003cspan class=\"InternalRef\"\u003e3\u003c/span\u003ea-c).\u003c/p\u003e\n\u003cp\u003eIn the unsterilized soil, the community invasion resistance had a positive relationship with the complementarity effect for all three invasive species (Fig. \u003cspan class=\"InternalRef\"\u003e4\u003c/span\u003ea-c). However, in the sterilized soil, the community invasion resistance had a positive relationship with the complementarity effect for \u003cem\u003eS. subulatum\u003c/em\u003e, but the positive relationship was absent for \u003cem\u003eS. canadensis\u003c/em\u003e and \u003cem\u003eE. canadensis\u003c/em\u003e (Fig. \u003cspan class=\"InternalRef\"\u003e4\u003c/span\u003ea-c). Except for \u003cem\u003eS. subulatum\u003c/em\u003e in the unsterilized soil, the community invasion resistance was not significantly related to the selection effect (Fig. \u003cspan class=\"InternalRef\"\u003e4\u003c/span\u003ed-f). In the unsterilized soil, most mixtures had positive values of the over-invasion resistance index (Fig. \u003cspan class=\"InternalRef\"\u003e5\u003c/span\u003e), indicating that these mixtures had a higher resistance than that of the most highly resistant species in the mixtures.\u003c/p\u003e\n\u003ch2\u003eDirect Effects Of Soil Microbes Conditioned By Native Plant Communities On Invader Growth\u003c/h2\u003e\n\u003cp\u003eInconsistent with our third hypothesis, the biomass of neither \u003cem\u003eS. canadensis\u003c/em\u003e nor \u003cem\u003eS. subulatum\u003c/em\u003e was significantly affected by the different soil microbes trained in the native plant communities of different species richness (Fig. \u003cspan class=\"InternalRef\"\u003e6\u003c/span\u003ea, c) and had no significant relationship with the weighted phylogenetic distance (Fig. \u003cspan class=\"InternalRef\"\u003e7\u003c/span\u003ea, c). In addition, \u003cem\u003eE. canadensis\u003c/em\u003e produced more biomass in the soil inoculated with soil microbes from the more diverse plant communities (Fig. \u003cspan class=\"InternalRef\"\u003e6\u003c/span\u003eb), and the biomass of \u003cem\u003eE. canadensis\u003c/em\u003e was positively correlated with the weighted phylogenetic distance (Fig. \u003cspan class=\"InternalRef\"\u003e7\u003c/span\u003eb).\u003c/p\u003e"},{"header":"Discussion","content":"\u003cp\u003eWe found that the absence of soil microbes weakened the negative species richness-invasibility relationship, indicating that soil microbes can contribute to the higher invasion resistance of more diverse native plant communities. In the presence of soil microbes, the higher invasion resistance of plant communities in more diverse communities was mainly ascribed to the complementarity effect. However, soil microbes from communities with a higher species richness did not have a consistently stronger negative effect on the growth of the three invasive species.\u003c/p\u003e\n\u003ch2\u003eEffects Of Soil Microbes On The Species Richness-invasibility Relationship\u003c/h2\u003e\n\u003cp\u003eWe found significant negative relationships between native plant species and community invasibility (as measured by the invader biomass), supporting the diversity-invasibility hypothesis proposed by Elton (\u003cspan citationid=\"CR15\" class=\"CitationRef\"\u003e1958\u003c/span\u003e) and also agreeing with the findings of many previous studies (Adomako et al. \u003cspan citationid=\"CR1\" class=\"CitationRef\"\u003e2019\u003c/span\u003e; Hector et al. \u003cspan citationid=\"CR20\" class=\"CitationRef\"\u003e2001\u003c/span\u003e; Howeth \u003cspan citationid=\"CR25\" class=\"CitationRef\"\u003e2017\u003c/span\u003e; Martignoni et al. \u003cspan citationid=\"CR45\" class=\"CitationRef\"\u003e2020\u003c/span\u003e; Naeem et al. \u003cspan citationid=\"CR49\" class=\"CitationRef\"\u003e2000\u003c/span\u003e; Selmants et al. \u003cspan citationid=\"CR62\" class=\"CitationRef\"\u003e2012\u003c/span\u003e). More importantly, we found that the absence of soil microbes weakened the negative plant species richness-invasibility relationship, indicating that this relationship may be partly ascribed to the role of soil microbes. Thus, Elton\u0026rsquo;s diversity-invasibility hypothesis may be associated with the underground bio-systems.\u003c/p\u003e \u003cp\u003eWe found that the biomass of native species was significantly positively related to native species richness (Fig. S1, Table S4), as also reported in other studies (Cardinale et al. \u003cspan citationid=\"CR6\" class=\"CitationRef\"\u003e2007\u003c/span\u003e; Cardinale et al. \u003cspan citationid=\"CR7\" class=\"CitationRef\"\u003e2011\u003c/span\u003e; Han et al. \u003cspan citationid=\"CR18\" class=\"CitationRef\"\u003e2021\u003c/span\u003e; Venail et al. \u003cspan citationid=\"CR72\" class=\"CitationRef\"\u003e2015\u003c/span\u003e). However, the presence vs. absence of soil microbes did not change the relationship between the biomass and richness of native plant species (Fig. S1). These results suggest that the impact of soil microbes on the species richness-invasibility relationship was not due to its effect on the growth of native species.\u003c/p\u003e\n\u003ch2\u003eEffect Of Soil Microbes On The Community Invasion Resistance\u003c/h2\u003e\n\u003cp\u003eCompared with the absence of soil microbes, the presence of soil microbes led to a higher invasion resistance in the more diverse plant communities. Exotic plant species can affect native plants by enhancing their pathogen infection (Beckstead et al. \u003cspan citationid=\"CR3\" class=\"CitationRef\"\u003e2010\u003c/span\u003e; Mangla and Callaway \u003cspan citationid=\"CR44\" class=\"CitationRef\"\u003e2008\u003c/span\u003e), inhibiting mutualistic interactions (Stinson et al. \u003cspan citationid=\"CR66\" class=\"CitationRef\"\u003e2006\u003c/span\u003e; Vogelsang and Bever \u003cspan citationid=\"CR73\" class=\"CitationRef\"\u003e2009\u003c/span\u003e) or producing allelochemicals that are toxic to soil microbes (Inderjit and van der Putten 2010). The higher invasion resistance of the more diverse plant communities induced by soil microbes may be attributed to two mechanisms. One mechanism is that a higher level of diversity and/or abundance of microbial species in more diverse communities may lead to the stability of the underground bio-system in response to disturbance (Lankau \u003cspan citationid=\"CR36\" class=\"CitationRef\"\u003e2010\u003c/span\u003e; Li et al. \u003cspan citationid=\"CR39\" class=\"CitationRef\"\u003e2015\u003c/span\u003e; Zhu et al. \u003cspan citationid=\"CR83\" class=\"CitationRef\"\u003e2011\u003c/span\u003e), which can be ascribed to a higher insurance or portfolio effect (Isbell et al. \u003cspan citationid=\"CR30\" class=\"CitationRef\"\u003e2009\u003c/span\u003e; Wang et al. \u003cspan citationid=\"CR74\" class=\"CitationRef\"\u003e2021\u003c/span\u003e). The other mechanism is that more diverse communities have a higher probability of including more resistant soil microbial species that influence exotic plants, i.e., a selection effect (Isbell et al. \u003cspan citationid=\"CR31\" class=\"CitationRef\"\u003e2015\u003c/span\u003e; Wilsey et al. \u003cspan citationid=\"CR78\" class=\"CitationRef\"\u003e2014\u003c/span\u003e). For example, the more plant species the community contains, the more microbial species the plants carry and thus the higher the probability of harboring microbial species that can degrade allelochemicals (Hiiesalu et al. \u003cspan citationid=\"CR23\" class=\"CitationRef\"\u003e2014\u003c/span\u003e; Mitchell et al. \u003cspan citationid=\"CR48\" class=\"CitationRef\"\u003e2010\u003c/span\u003e; Prober et al. \u003cspan citationid=\"CR54\" class=\"CitationRef\"\u003e2015\u003c/span\u003e). Based on the results of this experiment, the complementarity effect determined the community invasion resistance. Moreover, the positive values of the over-invasion resistance index indicated the existence of facilitation among the plant species induced by soil microbes. Although the specific mechanism underlying the role of soil microbes in the diversity-resistance relationship was not further explored, we can at least be sure that the diversity-resistance relationship can be influenced by the underground bio-system.\u003c/p\u003e\n\u003ch2\u003eDirect Effects Of Soil Microbes On The Growth Of Invasive Plants\u003c/h2\u003e\n\u003cp\u003eIt is well known that the species richness of native plant communities can affect the diversity, abundance and activity of soil microbes (Chen et al. \u003cspan citationid=\"CR9\" class=\"CitationRef\"\u003e2019\u003c/span\u003e; Dassen et al. \u003cspan citationid=\"CR11\" class=\"CitationRef\"\u003e2017\u003c/span\u003e; Schmid et al. \u003cspan citationid=\"CR59\" class=\"CitationRef\"\u003e2019\u003c/span\u003e), including pathogens (Cappelli et al. \u003cspan citationid=\"CR5\" class=\"CitationRef\"\u003e2020\u003c/span\u003e; Liu et al. \u003cspan citationid=\"CR41\" class=\"CitationRef\"\u003e2021\u003c/span\u003e; Zhang et al. \u003cspan citationid=\"CR81\" class=\"CitationRef\"\u003e2020\u003c/span\u003e). If the diversity, abundance and/or activity of soil pathogens increase with species richness in native plant communities, then soils from native plant communities with higher species richness should have a stronger negative effect on the growth of invasive plants. For instance, in a recent study, Zhang et al. (\u003cspan citationid=\"CR81\" class=\"CitationRef\"\u003e2020\u003c/span\u003e) showed that more species-rich plant communities contained a greater diversity of plant pathogens and thus had strong negative impacts on invasive species. However, we found that \u003cem\u003eS. canadensis\u003c/em\u003e and \u003cem\u003eS. subulatum\u003c/em\u003e produced a similar amount of biomass when they were grown in the soils inoculated with the soil microbes from the native plant communities with different levels of species richness, and \u003cem\u003eE. canadensis\u003c/em\u003e even produced more biomass in the soil inoculated with the soil microbes from the more diverse plant communities. These results suggest that the effects of soil pathogens cannot explain the negative species diversity-invasibility relationship detected in the current study systems.\u003c/p\u003e \u003cp\u003eIn the present study, the effect of soil microbes on the growth of invasive species also showed no general relationship with the phylogenetic distance between the native and invasive species. There may be two reasons for the lack of impact on the richness-mediated effects of soil microbes on the growth of invasive species. One may be that increasing the species richness of native plant communities in our study did not increase the diversity, abundance or activity of soil pathogens that were harmful to the three invasive plant species. However, increasing plant species richness may increase the diversity of pathogens through amplification (Hudson et al. \u003cspan citationid=\"CR26\" class=\"CitationRef\"\u003e2006\u003c/span\u003e; Keesing et al. \u003cspan citationid=\"CR32\" class=\"CitationRef\"\u003e2006\u003c/span\u003e), and it may also reduce the prevalence of pathogens through dilution (Ostfeld and Keesing \u003cspan citationid=\"CR51\" class=\"CitationRef\"\u003e2012\u003c/span\u003e; Schmidt and Ostfeld \u003cspan citationid=\"CR60\" class=\"CitationRef\"\u003e2001\u003c/span\u003e; Zhang et al. \u003cspan citationid=\"CR81\" class=\"CitationRef\"\u003e2020\u003c/span\u003e). The other reason may be that the effect of soil microbes on invasive plants was the net effect of the interaction between pathogenic and mutualistic soil microbes (Reinhart and Callaway \u003cspan citationid=\"CR57\" class=\"CitationRef\"\u003e2006\u003c/span\u003e). Exotic plants have been proposed to encounter novel but strong soil mutualists, such as arbuscular mycorrhizal fungi, and benefit disproportionately from these symbiotic mutualists (Reinhart and Callaway \u003cspan citationid=\"CR57\" class=\"CitationRef\"\u003e2006\u003c/span\u003e; Richardson et al. \u003cspan citationid=\"CR58\" class=\"CitationRef\"\u003e2000\u003c/span\u003e). As infections with both pathogens and arbuscular mycorrhizal fungi are phylogenetically conserved, the relationship between the effect of soil microbes on invasive species and the phylogenetic distance between native and invasive species may depend on the relative role of the pathogen or arbuscular mycorrhizal fungi.\u003c/p\u003e"},{"header":"Conclusions","content":"\u003cp\u003eWe conclude that soil microbes can alter the diversity-invasibility relationship by promoting the complementarity effect on the community invasion resistance. However, we did not find a significant role for the richness-induced difference in soil pathogens in explaining the change in the relationship. Soil pathogens and arbuscular mycorrhizal fungi in the invaded area were proven to influence invasive plants (Inderjit \u003cspan citationid=\"CR27\" class=\"CitationRef\"\u003e2005\u003c/span\u003e; Klironomos \u003cspan citationid=\"CR33\" class=\"CitationRef\"\u003e2002\u003c/span\u003e; Reinhart and Callaway \u003cspan citationid=\"CR57\" class=\"CitationRef\"\u003e2006\u003c/span\u003e; Richardson et al. \u003cspan citationid=\"CR58\" class=\"CitationRef\"\u003e2000\u003c/span\u003e). Therefore, further studies could test the way in which plant species richness alters the impact of soil pathogens vs. arbuscular mycorrhizal fungi on the growth of invasive plants to obtain a deeper understanding of the richness-invasibility relationship. Our results highlight the importance of integrating the role of soil microbes when testing the diversity-invasibility hypothesis.\u003c/p\u003e"},{"header":"Declarations","content":"\u003cp\u003e\u003cstrong\u003eAcknowledgment \u0026nbsp;\u003c/strong\u003eWe thank Qiao-Di Yan and Meng-Chun Shen for help with experiment, and reviewers in their papers.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eContributions \u0026nbsp;\u003c/strong\u003eConceptualization: XYW, SG, JW, FHY; Formal analysis: SG, XYW; Methodology: XYW, SG, TC, JW, FHY; Funding: XYW, SG, JW; Writing original draft: XYW, SG; Review/editing: XYW, SG, JW, FHY.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eFunding \u0026nbsp;\u003c/strong\u003eThis work was supported by the National Natural Science Foundation of China (31870504, 41671254); Basic Public Welfare Research Projects of Zhejiang Province (LGN19C150004); Outstanding Youth Program of Taizhou University (2017JQ005, 2019JQ005); National Innovation and Entrepreneurship Program for College Students (202010350035); Natural Science Foundation of Zhejiang Province (LY22C030001, LTY22C030004); Taizhou Science and Technology Project (21hba02).\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eData availability\u0026nbsp;\u003c/strong\u003eThe datasets generated and analysed during the current study are available on Dryad (https://doi.org/10.5061/dryad.4qrfj6qcr).\u0026nbsp;\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eEthics declarations\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eConflict of interest \u0026nbsp;\u003c/strong\u003eThe authors have no relevant fnancial or non-fnancial interests to disclose.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eInformed consent\u003c/strong\u003e\u0026nbsp; Both authors have contributed significantly to the work and agree with the content of the submission.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eEthics approval\u003c/strong\u003e\u0026nbsp; Not applicable.\u003c/p\u003e"},{"header":"References","content":"\u003col\u003e\u003cli\u003e\u003cspan\u003eAdomako MO, Ning L, Tang M, Du D-L, van Kleunen M, Yu F-H (2019) Diversity- and density-mediated allelopathic effects of resident plant communities on invasion by an exotic plant. 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PLoS ONE 6:e25393. \u003cspan class=\"ExternalRef\"\u003e\u003cspan class=\"RefSource\"\u003ehttp://doi.org/10.1371/journal.pone.0025393\u003c/span\u003e\u003cspan address=\"10.1371/journal.pone.0025393\" targettype=\"DOI\" class=\"RefTarget\"\u003e\u003c/span\u003e\u003c/span\u003e\u003c/span\u003e\u003c/li\u003e\u003c/ol\u003e"}],"fulltextSource":"","fullText":"","funders":[],"hasAdminPriorityOnWorkflow":false,"hasManuscriptDocX":true,"hasOptedInToPreprint":true,"hasPassedJournalQc":"","hasAnyPriority":false,"hideJournal":false,"highlight":"","institution":"","isAcceptedByJournal":true,"isAuthorSuppliedPdf":false,"isDeskRejected":"","isHiddenFromSearch":false,"isInQc":false,"isInWorkflow":false,"isPdf":false,"isPdfUpToDate":true,"isWithdrawnOrRetracted":false,"journal":{"display":true,"email":"[email protected]","identity":"biological-invasions","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":false,"externalIdentity":"binv","sideBox":"Learn more about [Biological Invasions](https://www.springer.com/journal/10530)","snPcode":"10530","submissionUrl":"https://submission.nature.com/new-submission/10530/3","title":"Biological Invasions","twitterHandle":"","acdcEnabled":true,"dfaEnabled":true,"editorialSystem":"em","reportingPortfolio":"Springer Hybrid","inReviewEnabled":true,"inReviewRevisionsEnabled":false},"keywords":"biomass, diversity effect, over-invasion resistance index, phylogenetic distance, species richness","lastPublishedDoi":"10.21203/rs.3.rs-1136323/v2","lastPublishedDoiUrl":"https://doi.org/10.21203/rs.3.rs-1136323/v2","license":{"name":"CC BY 4.0","url":"https://creativecommons.org/licenses/by/4.0/"},"manuscriptAbstract":"\u003cp\u003eSoil microbes can affect both the invasiveness of exotic plants and the invasibility of native plant communities, but it still remains unclear whether soil microbes can influence the relationship between native plant species diversity and community invasibility. We constructed native plant communities with three levels of species richness (one, three, or six species) in un-sterilized or sterilized soil (i.e., with or without soil microbes) and let them not be invaded by exotic plant species or invaded by one of three exotic species (\u003cem\u003eSolidago canadensis\u003c/em\u003e, \u003cem\u003eErigeron canadensis\u003c/em\u003e or \u003cem\u003eSymphyotrichum subulatum\u003c/em\u003e) highly invasive in China. The soils conditioned by the native plant communities not invaded by the exotic species were used as soil microbe inocula to test whether richness-induced differences in soil microbes affect the growth of each of the three invasive species. Compared with the presence of soil microbes, the absence of soil microbes weakened the negative species richness-invasibility relationship, indicating that soil microbes can contribute to the higher invasion resistance of more diverse native plant communities. In the presence of soil microbes, the higher invasion resistance of more diverse communities was mainly ascribed to the complementarity effect. However, soil microbes from communities with a higher species richness did not have a stronger negative effect on the growth of any of the three invasive species. We conclude that soil microbes can alter the diversity-invasibility relationship through promoting the complementarity effect on the community invasion resistance. Our results highlight the importance to integrate the role of soil microbes in testing the diversity-invasibility hypothesis.\u003c/p\u003e","manuscriptTitle":"Soil microbes alter the diversity-invasibility relationship by promoting a complementarity effect on community invasion resistance","msid":"","msnumber":"","nonDraftVersions":[{"code":2,"date":"2022-06-30 16:27:51","doi":"10.21203/rs.3.rs-1136323/v2","editorialEvents":[{"type":"communityComments","content":0},{"type":"reviewerAgreed","content":"","date":"2022-06-21T14:34:47+00:00","index":0,"fulltext":""},{"type":"reviewersInvited","content":"","date":"2022-06-21T04:19:57+00:00","index":"","fulltext":""},{"type":"editorInvited","content":"Biological Invasions","date":"2022-06-03T17:11:00+00:00","index":"","fulltext":""},{"type":"editorAssigned","content":"","date":"2022-05-18T06:15:18+00:00","index":"","fulltext":""},{"type":"submitted","content":"Biological Invasions","date":"2022-05-11T09:23:16+00:00","index":"","fulltext":""}],"status":"published","journal":{"display":true,"email":"[email protected]","identity":"biological-invasions","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":false,"externalIdentity":"binv","sideBox":"Learn more about [Biological Invasions](https://www.springer.com/journal/10530)","snPcode":"10530","submissionUrl":"https://submission.nature.com/new-submission/10530/3","title":"Biological Invasions","twitterHandle":"","acdcEnabled":true,"dfaEnabled":true,"editorialSystem":"em","reportingPortfolio":"Springer Hybrid","inReviewEnabled":true,"inReviewRevisionsEnabled":false}}],"origin":"","ownerIdentity":"04372902-5730-4d4a-8d10-3e68e143626a","owner":[],"postedDate":"June 30th, 2022","published":true,"recentEditorialEvents":[],"rejectedJournal":[],"revision":"","amendment":"","status":"published-in-journal","subjectAreas":[],"tags":[],"updatedAt":"2023-10-16T18:09:51+00:00","versionOfRecord":{"articleIdentity":"rs-1136323","link":"https://doi.org/10.1007/s10530-022-02988-z","journal":{"identity":"biological-invasions","isVorOnly":false,"title":"Biological Invasions"},"publishedOn":"2022-12-28 18:07:36","publishedOnDateReadable":"December 28th, 2022"},"versionCreatedAt":"2022-06-30 16:27:51","video":"","vorDoi":"10.1007/s10530-022-02988-z","vorDoiUrl":"https://doi.org/10.1007/s10530-022-02988-z","workflowStages":[]},"version":"v2","identity":"rs-1136323","journalConfig":"researchsquare"},"__N_SSP":true},"page":"/article/[identity]/[[...version]]","query":{"redirect":"/article/rs-1136323","identity":"rs-1136323","version":["v2"]},"buildId":"7rjqhiLT3MXkJMwkYKINL","isFallback":false,"isExperimentalCompile":false,"dynamicIds":[84888],"gssp":true,"scriptLoader":[]}