Abstract
Background and aims
Nitrogen enrichment and biodiversity affects the stoichiometry of plants, soils, and soil microbes. However, combined effects of nitrogen addition and biodiversity on interactions among the stoichiometry of plants, soils, and soil microbes (stoichiometric networks, PSMNs) have largely been overlooked, even though PSMNs are likely critical predictors of ecosystem structure and functions.
Methods
To quantify effects of nitrogen addition and plant species richness on stoichiometric relations among plants, soils, and soil microbes, a common garden experiment with two nitrogen addition levels (0 and 6 g N m− 2 year− 1) and four plant species richness levels (1, 2, 4, and 8 species) was conducted in which those driving factors were manipulated.
Results
Nitrogen addition had minor effects on most stoichiometries of plant–soil–microbes, but plant species richness showed significant association with most stoichiometries. With nitrogen addition, increases in soil ammonium nitrogen led to a decrease in PSMNs connectivity but an increase in modularity. Plant species richness was negatively associated with network connectivity but positively correlated with modular complexity because of changes in soil nutrient availability and increased niche differentiation.
Conclusions
The findings demonstrate mechanistic links of biodiversity with the stoichiometry of plant–soil–microbes and stoichiometric networks, suggesting that biodiversity loss and resources decrease under global changes may enable a looser complexity in whole ecosystem element structure as indicated by the stoichiometric network architecture.
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Data availability
The data that support the findings of this study are available from the corresponding author upon reasonable request.
References
Abbas M, Ebeling A, Oelmann Y et al (2013) Biodiversity effects on plant stoichiometry. PLoS One 8:e58179. https://doi.org/10.1371/journal.pone.0058179
Bowman RA (1988) A rapid method to determine total phosphorus in soils. Soil Sci Soc Am J 52:1301–1304. https://doi.org/10.2136/sssaj1988.03615995005200050016x
Brookes PC, Powlson DS, Jenkinson DS (1982) Measurement of microbial biomass phosphorus in soil. Soil Biol Biochem 14:319–329. https://doi.org/10.1016/0038-0717(82)90001-3
Chabbi A, Kögel-Knabner I, Rumpel C (2009) Stabilised carbon in subsoil horizons is located in spatially distinct parts of the soil profile. Soil Biol Biochem 41:256–261. https://doi.org/10.1016/j.soilbio.2008.10.033
Chapin F (1980) The mineral nutrition of wild plants. Annul Rev Ecol Evol System 11:233–260. https://doi.org/10.1146/annurev.es.11.110180.001313
Chen X, Chen HYH, Searle EB, Chen C, Reich PB (2021) Negative to positive shifts in diversity effects on soil nitrogen over time. Nat Sustain 4:225–234. https://doi.org/10.1038/s41893-020-00641-y
Chen W, Wang J, Chen X et al (2022a) Soil microbial network complexity predicts ecosystem function along elevation gradients on the Tibetan Plateau. Soil Biol Biochem 172:108766. https://doi.org/10.1016/j.soilbio.2022.108766
Chen X, Chen HYH, Chang S (2022b) Meta-analysis shows that plant mixtures increase soil phosphorus availability and plant productivity in diverse ecosystems. Nat Ecol Evol 6:1112–1121. https://doi.org/10.1038/s41559-022-01794-z
Cotrufo MF, Wallenstein MD, Boot CM, Denef K, Paul E (2013) The Microbial Efficiency-Matrix stabilization (MEMS) framework integrates plant litter decomposition with soil organic matter stabilization: do labile plant inputs form stable soil organic matter? Global Chang Biol 19:988–995. https://doi.org/10.1111/gcb.12113
Elser JJ, Fagan WF, Kerkhoff AJ, Swenson NG, Enquist BJ (2010) Biological stoichiometry of plant production: metabolism, scaling and ecological response to global change. New Phytol 186:593–608. https://doi.org/10.1111/j.1469-8137.2010.03214.x
Fanin N, Fromin N, Barantal S, Hättenschwiler S (2017) Stoichiometric plasticity of microbial communities is similar between litter and soil in a tropical rainforest. Sci Rep 7:12498. https://doi.org/10.1038/s41598-017-12609-8
Guiz J, Ebeling A, Eisenhauer N et al (2018) Interspecific competition alters leaf stoichiometry in 20 grassland species. Oikos 127:903–914. https://doi.org/10.1111/oik.04907
Guo L, Deng M, Yang S, Liu W, Wang X, Wang J, Liu L (2021) The coordination between leaf and fine root litter decomposition and the difference in their controlling factors. Global Ecol Biogeogr 30:2286–2296. https://doi.org/10.1111/geb.13384
Harpole WS, Sullivan LL, Lind EM et al (2016) Addition of multiple limiting resources reduces grassland diversity. Nature 537:93–96. https://doi.org/10.1038/nature19324
Hong P, Schmid B, De Laender F et al (2022) Biodiversity promotes ecosystem functioning despite environmental change. Ecol Lett 25:555–569. https://doi.org/10.1111/ele.13936
Huang X, Terrer FA, Dijkstra BA, Hungate W, van Groenigen KJ (2020) New soil carbon sequestration with nitrogen enrichment: a meta-analysis. Plant Soil 454:299–310. https://doi.org/10.1007/s11104-020-04617-x
Laliberte E, Legendre P (2010) A distance-based framework for measuring functional diversity from multiple traits. Ecology 91:299–305. https://doi.org/10.1890/08-2244.1
Lefcheck JS (2016) piecewiseSEM: Piecewise structural equation modelling in R for ecology, evolution, and systematics. Methods Ecol Evol 7:573–579. https://doi.org/10.1111/2041-210X.12512
Li L, Tilman D, Lambers H, Zhang F (2014) Plant diversity and overyielding: insights from belowground facilitation of intercropping in agriculture. New Phytol 203:63–69. https://doi.org/10.1111/nph.12778
Li Y, Liu C, Sack L, Xu L, Li M, Zhang J, He N (2022) Leaf trait network architecture shifts with species-richness and climate across forests at continental scale. Ecol Lett 25:1442–1457. https://doi.org/10.1111/ele.14009
Liang C, Schimel JP, Jastrow JD (2017) The importance of anabolism in microbial control over soil carbon storage. Nat Microbiol 2:1–6. https://doi.org/10.1038/nmicrobiol.2017.105
Liu L, Greaver TL (2010) A global perspective on belowground carbon dynamics under nitrogen enrichment. Ecol Lett 13:819–828. https://doi.org/10.1111/j.1461-0248.2010.01482.x
Liu X, Zhang Y, Han W et al (2013) Enhanced nitrogen deposition over China. Nature 494:459–462. https://doi.org/10.1038/nature11917
Liu J, Wu N, Wang H, Sun J, Peng B, Jiang P, Bai E (2016) Nitrogen addition affects chemical compositions of plant tissues, litter and soil organic matter. Ecology 97:1796–1806. https://doi.org/10.1890/15-1683.1
Liu H, Mi Z, Lin L et al (2018) Shifting plant species composition in response to climate change stabilizes grassland primary production. Proc Natl Acad Sci USA 115:4051–4056. https://doi.org/10.1073/pnas.1700299114
Ma T, Dai G, Zhu S, Chen D, Feng X (2020) Vertical variations in plant-and microbial-derived carbon components in grassland soils. Plant Soil 446:441–455. https://doi.org/10.1007/s11104-019-04371-9
Margalef R (1968) Perspectives in ecological theory. Chicago University Press, Chicago
Mason CM, Donovan LA (2015) Evolution of the leaf economics spectrum in herbs: evidence from environmental divergences in leaf physiology across Helianthus (Asteraceae). Evolution 69:2705–2720. https://doi.org/10.1111/evo.12768
Mooshammer M, Wanek W, Zechmeister-Boltenstern S, Richter A (2014) Stoichiometric imbalances between terrestrial decomposer communities and their resources: mechanisms and implications of microbial adaptations to their resources. Fron Microbiol 5:22. https://doi.org/10.3389/fmicb.2014.00022
Newman MEJ (2003) The structure and function of complex networks. Siam Rev 45:167–256. https://doi.org/10.1137/S003614450342480
Novotny AM, Schade JD, Hobbie SE, Kay AD, Kyle M, Elser R (2007) Stoichiometric response of nitrogen-fixing and nonfixing dicots to manipulations of CO2, nitrogen, and diversity. Oecologia 151:687–696. https://doi.org/10.1007/s00442-006-0599-5
Oelmann Y, Lange M, Leimer S et al (2021) Above- and belowground biodiversity jointly tighten the P cycle in agricultural grasslands. Nat Commun 12:4431. https://doi.org/10.1038/S41467-021-24714-4
Oram NJ, Ravenek JM, Barry KE et al (2018) Below-ground complementarity effects in a grassland biodiversity experiment are related to deep-rooting species. J Ecol 106:265–277. https://doi.org/10.1111/1365-2745.12877
Peng Y, Guo D, Yang Y (2017) Global patterns of root dynamics under nitrogen enrichment. Global Ecol Biogeogr 26:102–114. https://doi.org/10.1111/geb.12508
Pinheiro J, Bates D, DebRoy S, Sarkar D (2007) Linear and nonlinear mixed effects models. R Package Version 3:57
Plum C, Husener M, Hillebrand H (2015) Multiple vs. single phytoplankton species alter stoichiometry of trophic interaction with zooplankton. Ecology 96:3075–3089. https://doi.org/10.1890/15-0393.1
R Development Core Team (2021) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Schneider JV, Habersetzer J, Rabenstein R, Wesenberg J, Wesche K, Zizka G (2017) Water supply and demand remain coordinated during breakdown of the global scaling relationship between leaf size and major vein density. New Phytol 214:473–486. https://doi.org/10.1111/nph.14382
Stahlberg S (1980) New extraction method for estimation of plant-available P, K and Mg-trial application in swedish cultivated soils. Acta Agric Scand 30:93–107. https://doi.org/10.1080/00015128009435700
Sterner RW, Elser JJ (2002) Ecological stoichiometry: the biology of elements from molecules to the biosphere. Princeton University Press, Princeton
Sun Y, Wang C, Chen HYH, Ruan H (2020) Responses of C:N stoichiometry in plants, soil, and microorganisms to nitrogen addition. Plant Soil 456:277–287. https://doi.org/10.1007/s11104-020-04717-8
Suter M, Connolly J, Finn JA, Loges R, Kirwan L, Sebastià MT, Lüscher A (2015) Nitrogen yield advantage from grass–legume mixtures is robust over a wide range of legume proportions and environmental conditions. Global Chang Biol 21:2424–2438. https://doi.org/10.1111/gcb.12880
Valencia E, Gross N, Quero JL et al (2018) Cascading effects from plants to soil microorganisms explain how plant species richness and simulated climate change affect soil multifunctionality. Global Chang Biol 24:5642–5654. https://doi.org/10.1111/gcb.14440
Vance ED, Brookes PC, Jenkinson DS (1987) Microbial biomass measurements in forest soils: the use of the chloroform fumigation-incubation method in strongly acid soils. Soil Biol Biochem 19:697–702. https://doi.org/10.1016/0038-0717(87)90051-4
Wang C, Ren F, Zhou X, Ma W, Liang C, Wang J, Cheng J, Zhou H, He J-S (2020a) Variations in the nitrogen saturation threshold of soil respiration in grassland ecosystems. Biogeochemistry 148:1–15. https://doi.org/10.1007/s10533-020-00661-y
Wang C, Tang Y, Li X, Zhang W, Zhao C, Li C (2020b) Negative impacts of plant diversity loss on carbon sequestration exacerbate over time in grasslands. Environ Res Lett 15:104055. https://doi.org/10.1007/s10533-020-00661-y
Wang R, Yang J, Liu H et al (2021) Nitrogen enrichment buffers phosphorus limitation by mobilizing mineral-bound soil phosphorus in grasslands. Ecology 103:e3616. https://doi.org/10.1002/ecy.3616
Wang C, Li X, Zheng HY, Hou R (2023) Nitrogen addition weakens the biodiversity – multifunctionality relationships across soil profiles in a grassland assemblage. Agr Ecosyst Environ 342:108241. https://doi.org/10.1016/j.agee.2022.108241
Weisser WW et al (2017) Biodiversity effects on ecosystem functioning in a 15-year grassland experiment: patterns, mechanisms, and open questions. Basic Appl Ecol 23:1–73. https://doi.org/10.1016/j.baae.2017.06.002
Wright IJ, Reich PB, Westoby M et al (2004) The worldwide leaf economics spectrum. Nature 428:821–827. https://doi.org/10.1038/nature02403
Yang S, Liu W, Guo L, Wang C, Deng M, Peng Z, Liu L (2022) The changes in plant soil C pools and their C:N stoichiometry control Grassland N Retention under elevated N inputs. Ecol Appl 32:e2517. https://doi.org/10.1002/eap.2517
Yu G, Jia Y, He N, Zhu J, Chen Z, Wang Q, Piao S, Liu X, He H, Gou X (2019) Stabilization of atmospheric nitrogen deposition in China over the past decade. Nat Geo 1:1–8. https://doi.org/10.1038/s41561-019-0352-4
Yuan M, Guo X, Wu L et al (2021) Climate warming enhances microbial network complexity and stability. Nat Clim Chang 11:343–348. https://doi.org/10.1038/s41558-021-00989-9
Zechmeister-Boltenstern S, Keiblinger KM, Mooshammer M et al (2015) The application of ecological stoichiometry to plant-microbial-soil organic matter transformations. Ecol Monogr 85:133–155. https://doi.org/10.1890/14-0777.1
Acknowledgements
We thank the staff at the Xiaotangshan Station of Institute of Grassland, Flowers and Ecology for providing logistic support in the field. This study was supported by Natural Science Foundation of Beijing Municipality (Grant No. 5232006), Beijing Academy of Agriculture and Forestry Sciences Special Project for Innovation (Grant No. KJCX20230111), and National Natural Science Foundation of China (Grant No. 31901173).
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CW planned and designed the research. CW and XL performed the research. CW analyzed the data and wrote the manuscript, XL, YH, RZ, and YH revised the manuscript.
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Wang, C., Hou, Y., Zheng, R. et al. Plant diversity and nitrogen addition affect the architecture of plant–soil–microbe stoichiometric networks. Plant Soil 490, 143–155 (2023). https://doi.org/10.1007/s11104-023-06060-0
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DOI: https://doi.org/10.1007/s11104-023-06060-0