Effects of fertilizer and weed species richness on soil nematode community in a microcosm field experiment

Highlights

• Fertilizer increased soil nematode abundance and decreased the ecological index of soil nematode community.

• Except for bacterivore density, weed species richness had no effect on soil nematode abundance and increased the ecological index of soil nematode community.

• Fertilizer degraded, whereas weed species richness enhanced soil nematode community structure. Weed species richness may relieve the negative effect of fertilizer on the diversity of nematode community.

Abstract

Both fertilizer and plant species richness may affect the soil nematode community. However, the influence of fertilizer and weed species richness interaction is unclear. Nematode abundance and biodiversity in wheat and weed plots soil treated with nitrogen, phosphate and potassium fertilizer addition and weed species richness (0, 1, 2 and 4 weed levels) were investigated in a long-term microcosm experiment established in 2010 at Kaifeng, China. The results demonstrated that fertilizer treatment increased the abundance of total nematode, bacterivores, and plant parasites whereas it decreased the total genera number, the Shannon–Wiener diversity index (H′), Margalef richness index (SR), the total maturity index (∑MI), and structure index (SI), and degraded the structure of the nematode community. In contrast, weed species richness increased these ecological indices and enhanced the structure of the nematode community. Principal component analysis (PCA) indicated that the fertilizer's effect was more significant than weed species richness. Redundancy analysis demonstrated that fertilizer affected soil nematode mainly through increasing soil available phosphorus by 4.71 times and ammonium nitrogen content by 74.03%; weed species richness increased the diversity indices of soil nematode mainly through enhancing soil moisture by 2.07%. Our results suggest weed species richness may relieve the negative effect of fertilizer on the diversity of soil nematode community.

Graphical abstract

Keywords

Fertilizer / Farmland weed / Weed species richness / Soil nematodes / Community structure / Soil food web

References

[1] Anderson, L.J., 2011. Aboveground-belowground linkages: Biotic interactions, ecosystem processes, and global change. Eos (Washington, D.C.) 92, 222–222

[2] Anwar, S., Zia, A., Javed, N., Shakeel, Q., 2009. Weeds as reservoir of nematodes. Journal of Nematology 27, 145–153.

[3] Bao, S., 2000. Soil analysis in agricultural chemistry. China Agriculture Press: Beijing.

[4] Barker, K.R., 1985. Nematode Extraction and Bioassays, In: Barker, K.R., Carter, C.C., Sasser, J.N.,eds. An advanced treatise on Meloidogyne. North Carolina State University Graphics, Raleigh, NC, USA, pp. 19–35.

[5] Blackshaw, R.E., Molnar, L.J., Janzen, H.H., 2004. Nitrogen fertilizer timing and application method affect weed growth and competition with spring wheat. Weed Science 52, 614–622

[6] Bongers, T., 1999. The Maturity Index, the evolution of nematode life history traits, adaptive radiation and cp-scaling. Plant and Soil 212, 13–22

[7] Chen, X.P., Cui, Z.L., Vitousek, P.M., Cassman, K.G., Matson, P.A., Bai, J.S., Meng, Q.F., Hou, P., Yue, S.C., RÖmheld, V., Zhang, F. -S., 2011. Integrated soil-crop system management for food security. Proceedings of the National Academy of Sciences of the United States of America 108, 6399–6404.

[8] De Deyn, G.B., Raaijmakers, C.E., Van Ruijven, J., Berendse, F., Van Der Putten, W.H., 2004. Plant species identity and diversity effects on different trophic levels of nematodes in the soil food web. Oikos 106, 576–586

[9] Deyn, G.B., Raaijmakers, C., Ruijven, J., Berendse, F., Putten, W., 2004. Plant species identity and diversity on different trophic levels of nematodes in the soil food web. Oikos 106, 576–586

[10] Dietrich, P., Cesarz, S., Liu, T., Roscher, C., Eisenhauer, N., 2021. Effects of plant species diversity on nematode community composition and diversity in a long-term biodiversity experiment. Oecologia 197, 297–311

[11] Dupont, S., Beniston, J., Glover, J., Hodson, A., Culman, S., Lal, R., Ferris, H., 2014. Root traits and soil properties in harvested perennial grassland, annual wheat, and never-tilled annual wheat. Plant and Soil 381, 405–420

[12] Eisenhauer, N., Dobies, T., Cesarz, S., Hobbie, S., Meyer, R., Worm, K., Reich, P., 2013. Plant diversity effects on soil food webs are stronger than those of elevated CO₂ and N deposition in a long-term grassland experiment. Proceedings of the National Academy of Sciences of the United States of America 110, 6889–6994

[13] Eisenhauer, N., Reich, P., Scheu, S., 2012. Increasing plant diversity effects on productivity with time due to delayed soil biota effects on plants. Basic and Applied Ecology 13, 571–578

[14] Feng, W., Pan, G., Qiang, S., Li, R., Wei, J., 2008. Influence of long-term different fertilization on soil weed seed bank diversity of a paddy soil under rice/rape rotation. Frontiers of Biology in China 3, 320–327

[15] Ferris, H., Bongers, T., de Goede, R.G.M., 2001. A framework for soil food web diagnostics: extension of the nematode faunal analysis concept. Applied Soil Ecology 18, 13–29

[16] Ferris, H., Matute, M.M., 2003. Structural and functional succession in the nematode fauna of a soil food web. Applied Soil Ecology 23, 93–110

[17] Forge, T.A., Bittman, S., Kowalenko, C.G., 2005. Responses of grassland soil nematodes and protozoa to multi-year and single-year applications of dairy manure slurry and fertilizer. Soil Biology & Biochemistry 37, 1751–1762

[18] Fornara, D.A.T., Tilman, D., 2008. Plant functional composition influences rates of soil carbon and nitrogen accumulation. Journal of Ecology 2, 314–322

[19] Gibbons, D., Bohan, D., Rothery, P., Stuart, R.C., Haughton, A., Scott, R., Wilson, J.D., Perry, J.N., Clark, S.J., Dawson, R.J.G., Firbank, L.G., 2006. Weed seed resources for birds in fields with contrasting conventional and genetically modified herbicide-tolerant crops. Proceedings. Biological Sciences 273, 1921–1928

[20] Hu, C., Qi, Y., 2010. Effect of compost and chemical fertilizer on soil nematode community in a Chinese maize field. European Journal of Soil Biology 46, 230–236

[21] Hu, C., Xia, X.G., Han, X.M., Chen, Y.F., Qiao, Y., Liu, D.H., Li, S.L., 2018. Soil nematode abundances were increased by an incremental nutrient input in a paddy-upland rotation system. Helminthologia 55, 322–333

[22] Jiang, M., Liu, T., Huang, N., Shen, X., Shen, M., Dai, Q., 2018. Effect of long-term fertilisation on the weed community of a winter wheat field. Scientific Reports 8, 4017

[23] Keith, A.M., Brooker, R.W., Osler, G.H.R., Chapman, S.J., Burslem, D.F.R.P., van der Wal, R., 2009. Strong impacts of belowground tree inputs on soil nematode trophic composition. Soil Biology & Biochemistry 41, 1060–1065

[24] Lenz, R., Eisenbeis, G., 2000. Short-term effects of different tillage in a sustainable farming system on nematode community structure. Biology and Fertility of Soils 31, 237–244

[25] Lepš, J.Š.P., 2003. Multivariate analysis of ecological data using CANOCO. Cambridge University Press, New York.

[26] Loreau, M., Naeem, S., Inchausti, P., Bengtsson, J., Grime, J.P., Hector, A., Hooper, D.U., Huston, M.A., Raffaelli, D., Schmid, B., Tilman, D., Wardle, D.A., 2001. Biodiversity and ecosystem functioning: current knowledge and future challenges. Science 294, 804–808

[27] Lu, Q., Liu, T., Wang, N., Dou, Z., Kunguang, W., Zuo, Y., 2020. A review of soil nematodes as biological indicators for the assessment of soil health. Frontiers of Agricultural Science and Engineering 7, 275–281

[28] Lu, Z., Dong, D., Yang, B., Li, L., Yu, Y., Ouyang, F., Ge, F., Verma, V., Men, X.Y., 2016. Effects of crop species richness on the community of soil nematodes in an experimental agro-ecosystem. European Journal of Soil Biology 73, 26–33

[29] Majdi, H., Nylund, J.E., 1996. Does liquid fertilization affect fine root dynamics and lifespan of mycorrhizal short roots? Plant and Soil 185, 305–309

[30] Marshall, E.J.P., Brown, V.K., Boatman, N.D., Lutman, P.J.W., Squire, G.R., Ward, L.K., 2003. The role of weeds in supporting biological diversity within crop fields. Weed Research 43, 77–89

[31] Neher, D.A., 2001. Role of nematodes in soil health and their use as indicators. Journal of Nematology 33, 161–168.

[32] Nguyen, C., 2003. Rhizodeposition of organic C by plants: mechanisms and controls. Agronomie 23, 375–396

[33] Okada, H., Harada, H., 2007. Effects of tillage and fertilizer on nematode communities in a Japanese soybean field. Applied Soil Ecology 35, 582–598

[34] Pan, F., McLaughlin, N.B., Yu, Q., Xue, A.G., Xu, Y., Han, X., Li, C., Zhao, D., 2010. Responses of soil nematode community structure to different long-term fertilizer strategies in the soybean phase of a soybean-wheat-corn rotation. European Journal of Soil Biology 46, 105–111

[35] Reich, P., Tilman, D., Isbell, F., Mueller, K., Hobbie, S., Flynn, D., Eisenhauer, E., 2012. Impacts of biodiversity loss escalate through time as redundancy fades. Science 336, 589–592

[36] Ross, D., Van Acker, R.C., 2009. Effect of nitrogen fertilizer and landscape position on wild oat (Avena fatua) interference in spring wheat. Weed Science 53, 869–876

[37] Sabais, A.C.W., Scheu, S., Eisenhauer, N., 2011. Plant species richness drives the density and diversity of Collembola in temperate grassland. Acta Oecologica 37, 195–202

[38] Sarathchandra, S.U., Ghani, A., Yeates, G.W., Burch, G., Cox, N.R., 2001. Effect of nitrogen and phosphate fertilisers on microbial and nematode diversity in pasture soils. Soil Biology & Biochemistry 33, 953–964

[39] Scherber, C., Eisenhauer, N., Weisser, W., Schmid, B., Voigt, W., Fischer, M., Schulze, E.D., Roscher, C., Weigelt, A., Allan, E., Beßler, H., Bonkowski, M., Buchmann, N., Buscot, F., Clement, L.W., Ebeling, A., Engels, C., Halle, S., Kertscher, I., Klein, A.M., Koller, R., König, S., Kowalski, E., Kummer, V., Kuu, A., Lange, M., Lauterbach, D., Middelhoff, C., Migunova, V.D., Milcu, A., Müller, R., Partsch, S., Petermann, J.S., Renker, C., Rottstock, T., Sabais, A., Scheu, S., Schumacher, J., Temperton, V.M., Tscharntke, T., 2010. Bottom-up effects of plant diversity on multitrophic interactions in a biodiversity experiment. Nature 468, 553–556

[40] Schmitz, J., Schäfer, K., Brühl, C.A., 2014. Agrochemicals in field margins-Field evaluation of plant reproduction effects. Agriculture, Ecosystems & Environment 189, 82–91

[41] Sieriebriennikov, B., Ferris, H., de Goede, R.G.M., 2014. NINJA: An automated calculation system for nematode-based biological monitoring. European Journal of Soil Biology 61, 90–93

[42] Sohlenius, B., Boström, S., Viketoft, M., 2011. Effects of plant species and plant diversity on soil nematodes–A field experiment on grassland run for seven years. Nematology 13, 115–131

[43] Sun, F., Tariq, A., Chen, H., He, Q., Guan, Y., Pan, K., Chen, S., Li, J., Zhao, C., Wang, H., Gu, Y., 2016. Effect of nitrogen and phosphorus application on agricultural soil food webs. Archives of Agronomy and Soil Science 63, 1176–1186

[44] Tang, L., Wan, K., Cheng, Ch., Li, R., Wang, D., Pan, J., Tao, Y., Xie, J., Chen, F., 2014. Effect of fertilization patterns on the assemblage of weed communities in an upland winter wheat field. Journal of Plant Ecology 7, 39–50

[45] Thomas, S., Schroeder, J., Murray, L., 2009. The role of weeds in nematode management. Weed Science 53, 923–928

[46] Todd, T.C., 1996. Effects of management practices on nematode community structure in tallgrass prairie. Applied Soil Ecology 3, 235–246

[47] Vestergård, M., 2004. Nematode assemblages in the rhizosphere of spring barley (Hordeum vulgare L.) depended on fertilisation and plant growth phase. Pedobiologia 48, 257–265

[48] Viketoft, M., Bengtsson, J., Sohlenius, B., Berg, M., Petchey, O., Palmborg, C., Huss-Danell, K., 2009. Long-term effects of plant diversity and composition on soil nematode communities in model grasslands. Ecology 90, 90–99

[49] Wan, K., Tao, Y., Li, R., Pan, J., Tang, L., Chen, F., 2012. Influences of long‐term different types of fertilization on weed community biodiversity in rice paddy fields. Weed Biology and Management 12, 12–21

[50] Wang, K.H., McSorley, R., Marshall, A., Gallaher, R., 2006. Influence of organic Crotalaria juncea hay and ammonium nitrate fertilizers on soil nematode communities. Applied Soil Ecology 31, 186–198

[51] Wardle, D.A., Bardgett, R.D., Klironomos, J.N., Setälä, H., van der Putten, W.H., Wall, D.H., 2004. Ecological linkages between aboveground and belowground biota. Science 304, 1629–1633

[52] Yeates, G.W., 2003. Nematodes as soil indicators: functional and biodiversity aspects. Biology and Fertility of Soils 37, 199–210

[53] Yeates, G.W., Bongers, T., De Goede, R.G., Freckman, D.W., Georgieva, S.S., 1993. Feeding habits in soil nematode families and genera–an outline for soil ecologists. Journal of Nematology 25, 315–331.

[54] Zhang, W., Liu, M.Q., He, Y.Q., Fan, J.B., Chen, Y., 2014. Responses of soil nematode communities to long-term application of inorganic fertilizers in upland red soil. Journal of Applied Ecology 25, 2361–2368.

[55] Zhang, X., Jiang, Y., Liang, L., Zhao, X., Li, Q., 2009. Response of soil nematode communities to long-term application of inorganic fertilizers in the black soil of Northeast China. Frontiers of Biology in China 4, 111–116

[56] Zhang, Z., Zhang, X., Mahamood, M., Zhang, S., Huang, S., Liang, W., 2016. Effect of long-term combined application of organic and inorganic fertilizers on soil nematode communities within aggregates. Scientific Reports 6, 31118

[57] Zhao, J., Neher, D.A., 2013. Soil nematode genera that predict specific types of disturbance. Applied Soil Ecology 64, 135–141

[58] Zhao, J., Shao, Y., Wang, X., Neher, D.A., Xu, G., Li, Z., Fu, S., 2013. Sentinel soil invertebrate taxa as bioindicators for forest management practices. Ecological Indicators 24, 236–239

[59] Zhao, R.F., Chen, X.P., Zhang, F.S., Zhang, H., Schroder, J., Römheld, V., 2006. Fertilization and nitrogen balance in a wheat–maize rotation system in north China. Agronomy Journal 98, 938–945

[60] Zheng, F., Dong, Z., Chen, Q., Bi, Q., O’Connor, P., Zhu, Y.G., 2020. The driving factors of nematode gut microbiota under long-term fertilization. FEMS Microbiology Ecology 96, 1–11

[61] Zhu, X., Zhu, B., 2015. Diversity and abundance of soil fauna as influenced by long-term fertilization in cropland of purple soil, China. Soil & Tillage Research 146, 39–46

Author contributions

Conceptualization, X.N., and Y.G.; investigation, X.N., X.F., S.C., and F.S.; writing—original draft preparation, X.N.; writing—review and editing, X.N., F.S, and Y. G. All authors have read and agreed to the published version of the manuscript.

Acknowledgments

This study was supported by the National Natural Science Foundation of China (31070394) and the Natural Science Project of Henan Province (162300410009), and the National University Innovation and Entrepreneurship Training Program (202110475087).

ƒWe gratefully thank Junpeng Wang for editing and reviewing the manuscript, Cancan Zhao, for the help of data analysis.

Conflicts of interest

The authors declare no conflict of interest.

Electronic supplementary material

Supplementary material is available in the online version of this article at https://doi.org/10.1007/s42832-021-0123-1 and is accessible for authorized users.

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