Soil-microorganism-mediated invasional meltdown in plants

Abstract

While most alien species fail to establish, some invade native communities and become widespread. Our understanding of invasion success is derived mainly from pairwise interactions between aliens and natives, while interactions among more than two species remain largely unexplored. Here, we experimentally tested whether and how a third plant species, either native or alien, affected the competitive outcomes between alien and native plants through its soil legacy. We first conditioned soil with one of ten species (six natives and four aliens) or without plants. We then grew on these 11 soils five aliens and five natives without competition, or with intra- or interspecific competition. We found that aliens were not more competitive than natives when grown on soil conditioned by other natives or on non-conditioned soil. However, aliens were more competitive than natives on soil conditioned by other aliens (that is, invasional meltdown). Soil conditioning did not change competitive outcomes by affecting the strength of competition between later plants. Instead, soil conditioned by aliens pushed competitive outcomes towards later aliens by affecting the growth of aliens less negatively than that of natives. Microbiome analysis verified this finding, as we showed that the soil-legacy effects of a species on later species were less negative when their fungal endophyte communities were less similar, and that fungal endophyte communities were less similar between two aliens than between aliens and natives. Our study reveals invasional meltdown in multispecies communities and identifies soil microorganisms as a driver of the invasion success of alien plants.

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Fig. 1: Graphical illustration of how a third species can affect competitive outcomes between two species through changes in soil microbial communities.
Fig. 2: Graphical illustration of the experimental design.
Fig. 3: Effects of soil-conditioning treatments on aboveground biomass of alien (orange) and native (purple) test species.
Fig. 4: Dissimilarities of soil microbial communities within and between plant species.
Fig. 5: Effects of soil-community dissimilarity between soil-conditioning and test species on soil-legacy effects.

Data availability

The data from this study are freely available at https://doi.org/10.6084/m9.figshare.12682382. The raw sequencing data are deposited at the Sequence Read Archive at NCBI under accession number PRJNA647659.

Code availability

The R script for analysing and plotting are freely available at https://github.com/ecozhang/Invasional-meltdown and permanently deposited at https://doi.org/10.6084/m9.figshare.12682382.

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Acknowledgements

We thank L. Arnold, S. Berg, O. Ficht, M. Fuchs, S. Gommel, E. Mamonova, V. Pasqualetto, C. Rabung, B. Rüter, B. Speißer, H. Vahlenkamp and E. Werner for practical assistance, and J. Levine and R. Rohr for early discussion. Z.Z. was funded by the China Scholarship Council (grant no. 201606100049) and supported by the International Max Planck Research School for Organismal Biology. Y.L. was funded by the Chinese Academy of Sciences (grant nos. Y9H1011001 and Y9B7041001).

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Z.Z. conceived the idea. Z.Z., Y.L. and M.v.K. designed the experiment. Z.Z., Y.L. and C.B. performed the experiment. Z.Z. analysed the data and wrote the manuscript with input from all other authors.

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Correspondence to Yanjie Liu.

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Extended data

Extended Data Fig. 1 Effects of soil-conditioning treatments on belowground and total biomass of alien (orange) and native (purple) test species that were grown alone.

Mean values (± SEs) were calculated based on biomass of plants grown alone. For the soil-conditioning treatments, ‘non-conditioned’ refers to soil that was not conditioned by any plant, ‘home’ to soil conditioned by the same species as the test species, and ‘alien’ and ‘native’ to soils conditioned by other species than the test species, which were alien or native, respectively.

Extended Data Fig. 2 Effects of soil-conditioning treatments on soil community compositions of bacteria and fungi.

Nonmetric multidimensional scaling (NMDS) was used to visualize differences in the soil microbial communities of the plant species. Data points represent soil samples. Ellipses represent means ± 1 SDs for soil conditioned by aliens (orange) or natives (purple), or not conditioned by plants (grey). The different colors used for the points indicate different species. Soil was either alive (a,c) or sterilized (b,d) before the conditioning treatment.

Extended Data Fig. 3 Effects of soil-conditioning treatments on diversity of soil bacteria and fungi and relative abundance of fungal pathogens.

Species richness and Shannon diversity were calculated as diversity metrics. Soil was either alive or sterilized before the conditioning treatment.

Extended Data Fig. 4 Effects of diversity of bacteria and fungi, and relative abundance of fungal pathogens on soil-legacy effects.

Purple dots represent native test species, and orange dots represent alien test species. Negative values of soil-legacy effects indicate that plants grew worse on conditioned soil than on non-conditioned soil. No significant relationship was found. Note that relative abundance of all bacteria and fungi is 1, and thus their correlations to soil-legacy effect was not tested.

Extended Data Fig. 5 Dissimilarities of pathogenic or non-pathogenic fungal microbial communities within and between plant species and effects of soil-community dissimilarity on soil-legacy effects.

a, c, e, pathogenic fungal endophyte communities; b, d, f, non- pathogenic fungal endophyte communities. See Fig. 4 for detailed descriptions of ad. See Fig. 5 for detailed descriptions of e, f.

Extended Data Fig. 6 Graphical summary of effects of soil-conditioning plants on competitive outcomes between alien and native plants.

a, In pairwise competition, aliens and natives had similar aboveground biomass when grown alone, and suppressed each other equally, as indicated by the same thickness of the red arrows. Consequently, aliens were as competitive as natives (that is natives had similar aboveground biomass when in competition). b, soil conditioned by natives suppressed later aliens and natives equally, as indicated by the same thickness of the blue arrows. Consequently, soil conditioned by natives did not change the competitive outcomes. c, soil conditioned by aliens suppressed later aliens less than natives, as indicated by the thinner blue arrow towards aliens. Consequently, aliens changed the competitive outcomes, favoring later aliens over natives. Effects of soil conditioned by plants on strength of competition (that is red arrows) are not shown, as they did not change competitive outcomes between alien and native plants (for example see Fig. 3c).

Extended Data Fig. 7 Dissimilarities of soil communities within and between species, when sterilized field soil was used as inoculum.

a, e, bacterial communities; b, f, fungal communities, c, g, fungal pathogen communities; d, h, fungal endophyte communities. See Fig. 4 for detailed descriptions.

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Zhang, Z., Liu, Y., Brunel, C. et al. Soil-microorganism-mediated invasional meltdown in plants. Nat Ecol Evol (2020). https://doi.org/10.1038/s41559-020-01311-0

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