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Exotic earthworms maintain soil biodiversity by altering bottom-up effects of plants on the composition of soil microbial groups and nematode communities

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Abstract

Bottom-up effects of plants on soil communities can be modified by the activity of exotic earthworms, by altering resource availability for soil food webs through feeding, burrowing, and casting activities. The present study explored effects of plants (planting of shrubs) on soil micro-food webs (composition of soil microbial and nematode communities), and whether these effects were altered by the activity of exotic earthworms (exotic earthworms addition). Planted shrubs resulted in a non-significant increase of bacterial biomass and significantly increased the abundance of different nematode trophic groups and total nematode biomass, indicating that planted shrubs had significant bottom-up effects on soil bacteria and nematodes. Planted shrubs decreased nematode diversity, evenness, and richness, but increased nematode dominance in the plots where the abundance of exotic earthworms was not amended. By contrast, these effects of shrub presence on soil biodiversity were not found in the plots that received exotic earthworms. In addition, planted shrubs increased the total energy flux to the nematode community. By contrast, the elevated activity of exotic earthworms mitigated the increase in total energy flux to nematodes in the presence of shrubs, and increased the ratio of fungal to bacterial PLFAs. Both of these changes indicate reduced energy flux in the plots with added exotic earthworms. Nematode diversity decreased, while nematode dominance increased with increasing total energy flux to nematodes, probably because few species benefited from high energy flux. Our study indicates that exotic earthworms can maintain soil biodiversity by reducing the energy flux through soil food webs.

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Acknowledgments

We are grateful to Yongxing Li for his help during soil sampling. The authors are grateful to Prof. Wenju Liang, Prof. Paolo Nannipieri, and two anonymous reviewers for the helpful comments.

Funding

This study was funded by the Natural Science Foundation of China (31470559), Zhongyuan Scholar Program (182101510005), and “Heshan National Field Research Station of Forest Ecosystem”. NE and OF acknowledge support from the European Research Council (ERC) under the European Union’s Horizon 2020 research and innovation program (grant agreement no 677232 to NE). Further support came from the German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, funded by the German Research Foundation (FZT 118).

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Authors and Affiliations

  1. Key Laboratory of Geospatial Technology for the Middle and Lower Yellow River Regions (Henan University), Ministry of Education, College of Environment and Planning, Henan University, Kaifeng, 475004, China

    Yuanhu Shao, Weixin Zhang & Shenglei Fu

  2. Key Laboratory of Vegetation Restoration and Management of Degraded Ecosystems, South China Botanical Garden, Chinese Academy of Sciences, Guangzhou, 510650, China

    Yuanhu Shao, Weixin Zhang, Tao Liu & Shenglei Fu

  3. German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, Deutscher Platz 5e, 04103, Leipzig, Germany

    Nico Eisenhauer & Olga Ferlian

  4. Institute of Biology, Leipzig University, Deutscher Platz 5e, 04103, Leipzig, Germany

    Nico Eisenhauer & Olga Ferlian

  5. University of the Chinese Academy of Sciences, Beijing, 100049, China

    Tao Liu

  6. State Key Laboratory of Plateau Ecology and Agriculture, Qinghai Academy of Animal and Veterinary Sciences, Qinghai University, Xining, 810016, China

    Xiaoli Wang

  7. Research Institute of Tropical Forestry, Chinese Academy of Forestry, Guangzhou, 510520, China

    Yanmei Xiong

  8. Zhejiang Provincial Key Laboratory of Carbon Cycling in Forest Ecosystems and Carbon Sequestration, Zhejiang A & F University, Lin’an, 311300, China

    Chenfei Liang

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  1. Yuanhu Shao
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  2. Weixin Zhang
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  3. Nico Eisenhauer
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  4. Tao Liu
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Shao, Y., Zhang, W., Eisenhauer, N. et al. Exotic earthworms maintain soil biodiversity by altering bottom-up effects of plants on the composition of soil microbial groups and nematode communities. Biol Fertil Soils 55, 213–227 (2019). https://doi.org/10.1007/s00374-019-01343-0

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