Effects of nitrogen and phosphorus additions on soil nematode community of soybean farmland

Abstract

● The nitrogen (N) and phosphorus (P) addition promotes the abundance of soybean soil nematodes.

● The addition of nitrogen can alleviate the suppression of phosphorus on nematodes.

● Phosphorus addition affects nematode abundance by ammonium nitrogen.

With global warming, the increasing of industrial and agricultural activities and demand for fossil fuels, large amounts of nitrogen and phosphorus compounds are released into the atmosphere, resulting in an annual increase in nitrogen and phosphorus deposition. The nematodes, as one of the main functional groups of soil organisms, occupy multiple trophic levels in soil detritus food networks. However, few studies on the effects of nitrogen and phosphorus on soil nematodes, and the results are uncertain. This experiment was conducted in soybean farmland and four treatments included control, nitrogen addition, phosphorus addition, and N + P addition. The results showed that both phosphorus and N + P addition significantly increased the abundance of soil nematodes, but that had no effects on soil nematodes richness. Redundancy analysis showed that nitrate nitrogen, soil moisture content, and pH were environmental factors driving different dietary changes in soil nematode communities. The effect of phosphorus addition on the abundance of nematode communities mainly affects ammonium nitrogen. Our findings revealed that nitrogen addition when phosphate fertilizer is added to soybean farmland will have a certain positive effect on the soil underground food web, which provides a basis for better explaining the effect of nitrogen and phosphorus addition on soybean farmland.

Graphical abstract

Keywords

soil nematodes / nitrogen addition / phosphorus addition / soil food web / soybean

References

[1] Bardgett, R.D., van der Putten, W.H., 2014. Belowground biodiversity and ecosystem functioning. Nature515, 505–511.

[2] Bobbink, R., Hicks, K., Galloway, J., Spranger, T., Alkemade, R., Ashmore, M.R., Bustamante, M., Cinderby, S., Davidson, E., Dentener, F., Emmett, B., Erisman, J.W., Fenn, M., Gilliam, F., Nordin, A., Pardo, L., de Vries, W., 2010. Global assessment of nitrogen deposition effects on terrestrial plant diversity: a synthesis. Ecological Applications20, 30–59.

[3] Bongers, T., 1990. The maturity index: an ecological measure of environmental disturbance based on nematode species composition. Oecologia83, 14–19.

[4] Bongers, T., Bongers, M., 1998. Functional diversity of nematodes. Applied Soil Ecology10, 239–251.

[5] Boot, C.M., Hall, E.K., Denef, K., Baron, J.S., 2015. Long-term reactive nitrogen loading alters soil carbon and microbial community properties in a subalpine forest ecosystem. Soil Biology & Biochemistry92, 211–220.

[6] Cesarz, S., Reich, P.B., Scheu, S., Ruess, L., Schaefer, M., Eisenhauer, N., 2015. Nematode functional guilds, not trophic groups, reflect shifts in soil food webs and processes in response to interacting global change factors. Pedobiologia58, 23–32.

[7] Chen, D.M., Lan, Z.C., Hu, S.J., Bai, Y.F., 2015. Effects of nitrogen enrichment on belowground communities in grassland: Relative role of soil nitrogen availability vs. soil acidification. Soil Biology & Biochemistry89, 99–108.

[8] Chen, D.M., Xing, W., Lan, Z.C., Saleem, M., Wu, Y., Hu, S.J., Bai, Y.F., 2019. Direct and indirect effects of nitrogen enrichment on soil organisms and carbon and nitrogen mineralization in a semi-arid grassland. Functional Ecology33, 175–187.

[9] Chen, Y., Zhang, Y., Nielsen, U.N., Ma, Q., Zhang, X., Huang, X., Pan, D., Yue, X., Liu, J., Wang, D., 2021. Cattle grazing mitigates the negative impacts of nitrogen addition on soil nematode communities. Ecological Indicators129, 107876.

[10] Cheng, J.W., Ma, W.H., Hao, B.H., Liu, X.M., Li, F.Y.H., 2021. Divergent responses of nematodes in plant litter versus in top soil layer to nitrogen addition in a semi-arid grassland. Applied Soil Ecology157, 103719.

[11] Ferris, H., Bongers, T., 2006. Nematode indicators of organic enrichment. Journal of Nematology38, 3–12.

[12] 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 Ecology18, 13–29.

[13] Galloway, J.N., Townsend, A.R., Erisman, J.W., Bekunda, M., Cai, Z., Freney, J.R., Martinelli, L.A., Seitzinger, S.P., Sutton, M.A., 2008. Transformation of the nitrogen cycle: recent trends, questions, and potential solutions. Science320, 889–892.

[14] Gebremikael, M., Steel, H., Buchan, D., Bert, W., Neve, S.D., 2016. Nematodes enhance plant growth and nutrient uptake under C and N-rich conditions. Scientific Reports6, 32862.

[15] Gilliam, F.S., 2006. Response of the herbaceous layer of forest ecosystems to excess nitrogen deposition. Journal of Ecology94, 1176–1191.

[16] Guo, J.H., Liu, X.J., Zhang, Y., Shen, J.L., Han, W.X., Zhang, W.F., Christie, P., Goulding, K.W.T., Vitousek, P.M., Zhang, F.S., 2010. Significant acidification in major Chinese croplands. Science327, 1008–1010.

[17] He, J., Balasubramanian, R., Burger, D., Hicks, K., Kuylenstierna, J., Palani, S., 2011. Dry and wet atmospheric deposition of nitrogen and phosphorus in Singapore. Atmospheric Environment45, 2760–2768.

[18] Jiang, Y., Bo, S., Li, H., Liu, M., Chen, L., Zhou, S., 2015. Aggregate-related changes in network patterns of nematodes and ammonia oxidizers in an acidic soil. Soil Biology & Biochemistry88, 101–109.

[19] Karbin, S., Hagedorn, F., Dawes, M.A., Niklaus, P.A., 2015. Treeline soil warming does not affect soil methane fluxes and the spatial micro-distribution of methanotrophic bacteria. Soil Biology & Biochemistry86, 164–171.

[20] Li, Q., Bai, H., Liang, W., Xia, J., Wan, S., van der Putten, W.H., 2013. Nitrogen addition and warming independently influence the belowground micro-food web in a temperate steppe. PLoS One8, e60441.

[21] Li, Q., Liang, W.J., Lou, Y., Zhang, E., Liang, C., 2010. Long-term effect of fertility management on the soil nematode community in vegetable production under greenhouse conditions. Applied Soil Ecology46, 111–118.

[22] Liang, W.J., Lou, Y., Li, Q., Zhong, S., Zhang, X., Wang, J., 2009. Nematode faunal response to long-term application of nitrogen fertilizer and organic manure in Northeast China. Soil Biology & Biochemistry41, 883–890.

[23] Liu, J.S., Chen, Y., Du, C., Liu, X.X., Ma, Q.H., Zhang, X., Wang, D.L., 2019. Interactive effects of nitrogen addition and litter on soil nematodes in grassland. European Journal of Soil Science70, 697–706.

[24] Liu, L., Gundersen, P., Zhang, W., Chen, H., Mo, J.M., 2015. Effects of nitrogen and phosphorus additions on soil microbial biomass and community structure in two reforested tropical forests. Scientific Reports5, 14378.

[25] Liu, T., Mao, P., Shi, L.L., Wang, Z.Y., Wang, X.L., He, X.X., Tao, L.B., Liu, Z.F., Zhou, L.X., Shao, Y.H., Fu, S.L., 2020. Contrasting effects of nitrogen deposition and increased precipitation on soil nematode communities in a temperate forest. Soil Biology & Biochemistry148, 107869.

[26] Lokupitiya, E., Stanton, N.L., Seville, R.S., Snider, J.R., 2000. Effects of increased nitrogen deposition on soil nematodes in alpine tundra soils. Pedobiologia44, 591–608.

[27] Martinez, L., Wu, S., Baur, L., Patton, M.T., Smith, P.O., Collins, S.L., Ruders, J.A., 2023. Soil nematode assemblages respond to interacting environmental changes. Oecologia202, 481–495.

[28] Niu, X.L., Cheng, Y.F., Feng, X.P., Sun, F., Gu, Y.F. 2022. Effects of fertilizer and weed species richness on soil nematode community in a microcosm field experiment. Soil Ecology Letters5, 151–168.

[29] Pan, F., Han, X.Z., McLaughlin, N., Li, C., Zhao, D., Zhan, L., Xu, Y., 2015. Effect of long-term fertilization on free-living nematode community structure in Mollisols. Journal of Soil Science and Plant Nutrition15, 129–141.

[30] Pan, F., McLaughlin, N., Yu, Q., Xue, A.G., Xu, Y., Han, X., Chunjie, L., 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 Biology46, 105–111.

[31] Quinn Thomas, R., Canham, C., Weathers, K., Goodale, C., 2010. Increased tree carbon storage in response to nitrogen deposition in the US. Nature Geoscience3, 13–17.

[32] Ruan, W., Sang, Y., Chen, Q., Zhu, X., Lin, S., Gao, Y.B., 2012. The response of soil nematode community to nitrogen, water, and grazing history in the Inner Mongolian Steppe, China. Ecosystems (New York, N.Y.)15, 1121–1133.

[33] Ruess, L., 1995. Studies on the nematode fauna of an acid forest soil: Spatial distribution and extraction. Nematologica41, 229–239.

[34] 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 and Biochemistry33, 953–964.

[35] Shao, Y.H., Zhang, W.X., Eisenhauer, N., Liu, T., Xiong, Y.M., Liang, C.F., Fu, S., 2017. Nitrogen deposition cancels out exotic earthworm effects on plant-feeding nematode communities. Journal of Animal Ecology86, 708–717.

[36] Song, M., Li, X., Jing, S., Lei, L., Wang, J., Wan, S., 2016. Responses of soil nematodes to water and nitrogen additions in an old-field grassland. Applied Soil Ecology102, 53–60.

[37] Tian, D.S., Niu, S.L., 2015. A global analysis of soil acidification caused by nitrogen addition. Environmental Research Letters10, 024019.

[38] Wei, C.Z., Zheng, H.F., Li, Q., Lv, X.T., Yu, Q., Zhang, H.Y., He, N.P., Kardol, P., Liang, W.J., Han, X.G., 2012. Nitrogen addition regulates soil nematode community composition through ammonium suppression. PLoS One7, e43384.

[39] Xia, Z.W., Yang, J.Y., Sang, C.P., Wang, X., Sun, L.F., Jiang, P., Wang, C., Bai, E., 2020. Phosphorus reduces negative effects of nitrogen addition on soil microbial communities and functions. Microorganisms8, 1828.

[40] Yang, B., Zhang, T., Huang, J., Bhusal, D.R., Pang, X., 2019. Response of soil nematode community to phosphorous amendment in a subalpine spruce plantation. Clean (Weinheim)47, 1800202.

[41] Yeates, G.W., 2003. Nematodes as soil indicators: functional and biodiversity aspects. Biology and Fertility of Soils37, 199–210.

[42] 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 Nematology25, 315–331.

[43] 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 China4, 111–116.

[44] Zhang, X., Lin, C., Zhou, X., Lei, K., Guo, B., Cao, Y., Lu, S., Liu, X., He, M.C., 2019. Concentrations, fluxes, and potential sources of nitrogen and phosphorus species in atmospheric wet deposition of the lake Qinghai Watershed, China. Science of the Total Environment682, 523–531.

[45] Zhang, X.M., Han, X.G., 2012. Nitrogen deposition alters soil chemical properties and bacterial communities in the Inner Mongolia grassland. Journal of Environmental Sciences (China)24, 143–1491.

[46] Zhang, Z., Li, Q., Hu, Y., Wei, H., Hou, S., Yin, J., Lv, X., 2022. Nitrogen and phosphorus additions interactively affected composition and carbon budget of soil nematode community in a temperate steppe. Plant and Soil473, 109–121.

[47] 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 Reports6, 31118.

[48] Zhao, J., Wan, S., Li, Z., Shao, Y., Xu, G., Liu, Z., Zhou, L., Fu, S., 2012. Dicranopteris-dominated understory as major driver of intensive forest ecosystem in humid subtropical and tropical region. Soil Biology & Biochemistry49, 78–87.

[49] Zhao, J., Wang, F.M., Li, J., Zou, B., Wang, X.L., Li, Z.A., Fu, S.L., 2014. Effects of experimental nitrogen and/or phosphorus additions on soil nematode communities in a secondary tropical forest. Soil Biology & Biochemistry75, 1–10.

[50] Zhao, L., Yu, B.B., Wang, M.M., Zhang, J., Shen, Z.F., Cui, Y., Li, J.Y., Ye, J., Zu, W.Z., Liu, X.J., Fan, Z.J., Fu, S.L., Shao, Y.H., 2021. The effects of plant resource inputs on the energy flux of soil nematodes are affected by climate and plant resource type. Soil Ecology Letters3, 134–144.

[51] Zhou, J., Shi, R., Zhao, F., Han, S., Zhang, Y., 2016. Effects of the frequency and intensity of nitrogen addition on soil pH, the contents of carbon, nitrogen and phosphorus in temperate steppe in Inner Mongolia. Journal of Applied Ecology 27, 2467–2476 (in Chinese)

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