Abstract
Purpose
Nitrogen (N) enrichment through either artificial N application or atmospheric N deposition often increases ecosystem aboveground net primary productivity (ANPP). Therefore, results from N addition experiments have been used to assess the effects of atmospheric N deposition on ecosystems. However, the frequency of atmospheric N deposition is higher than that of artificial N addition. Whether the frequency of N addition alters the long-term response of ecosystem ANPP remains unclear.
Methods
We conducted a N addition frequency experiment from 2010 in a temperate grassland, northern China. Plant community ANPP was collected in 2019 and 2020, and soil physicochemical properties were measured in 2020.
Results
Plant community ANPP was significantly enhanced by N addition, whereas these increments declined with the frequency of N addition. The responses of the grasses ANPP were similar to those of the plant community ANPP. Forbs ANPP was not significantly altered. Meanwhile, soil ammonium and nitrate (NO3−–N) concentrations decreased with increasing N addition frequency, while the soil water content (SWC) and pH were similar among the frequencies of N addition. Regardless of the frequency of N addition, SWC and soil NO3−–N jointly promoted grasses ANPP, ultimately increasing the plant community ANPP.
Conclusion
Our findings demonstrate that the frequency of N addition affects plant community biomass production through altering soil nitrate concentration in the semi-arid grassland. Therefore, this study illustrates that a higher frequency of N addition is more suitable for assessing the long-term impacts of atmospheric N deposition on ecosystems.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
The datasets are available from the corresponding author on reasonable request.
References
Ashton IW, Miller AE, Bowman WD, Suding KN (2010) Niche complementarity due to plasticity in resource use: plant partitioning of chemical N forms. Ecology 91:3252–3260. https://doi.org/10.1890/09-1849.1
Bai W, Guo D, Tian Q, Liu N, Cheng W, Li L, Zhang W-H (2015) Differential responses of grasses and forbs led to marked reduction in below-ground productivity in temperate steppe following chronic N deposition. J Ecol 103:1570–1579. https://doi.org/10.1111/1365-2745.12468
Bai Y, Han X, Wu J, Chen Z, Li L (2004) Ecosystem stability and compensatory effects in the Inner Mongolia grassland. Nature 431:181–184. https://doi.org/10.1038/nature02850
Bai Y, Wu J, Clark CM, Naeem S, Pan Q, Huang J, Zhang L, Han X (2010) Tradeoffs and thresholds in the effects of nitrogen addition on biodiversity and ecosystem functioning: evidence from inner Mongolia grasslands. Glob Change Biol 16:358–372. https://doi.org/10.1111/j.1365-2486.2009.01950.x
Borer ET, Harpole WS, Adler PB, Lind EM, Orrock JL, Seabloom EW, Smith MD (2014) Finding generality in ecology: a model for globally distributed experiments. Methods Ecol Evol 5:65–73. https://doi.org/10.1111/2041-210X.12125
Cao J, Yang L, Pang S, Yang J, Hu Y, Li Y, Li L, Wang Q (2021) Convergent nitrogen uptake patterns and divergent nitrogen acquisition strategies of coexisting plant species in response to long-term nitrogen enrichment in a temperate grassland. Environ Exp Bot 185:104412. https://doi.org/10.1016/j.envexpbot.2021.104412
Clark CM, Tilman D (2008) Loss of plant species after chronic low-level nitrogen deposition to prairie grasslands. Nature 451:712–715. https://doi.org/10.1038/nature06503
Cusser S, Helms J IV, Bahlai CA, Haddad NM (2021) How long do population level field experiments need to be? Utilising data from the 40-year-old LTER network. Ecol Lett 24:1103–1111. https://doi.org/10.1111/ele.13710
de Mendiburu F (2021) agricolae: Statistical procedures for agricultural research. R package version 1.3–5. https://CRAN.R-project.org/package=agricolae (accessed by Aug. 2021)
Du E (2016) Rise and fall of nitrogen deposition in the United States. Proc Natl Acad Sci USA 113:E3594–E3595. https://doi.org/10.1073/pnas.1607543113
Du E, Terrer C, Pellegrini AFA, Ahlström A, van Lissa CJ, Zhao X, Xia N, Wu X, Jackson RB (2020) Global patterns of terrestrial nitrogen and phosphorus limitation. Nat Geosci 13:221–226. https://doi.org/10.1038/s41561-019-0530-4
Eisenlord SD, Zak DR (2010) Simulated atmospheric nitrogen deposition alters actinobacterial community composition in forest soils. Soil Sci Soc Am J 74:1157–1166. https://doi.org/10.2136/sssaj2009.0240
Galloway JN, Bleeker A, Erisman JW (2021) The human creation and use of reactive nitrogen: a global and regional perspective. Annu Rev Environ Resour 46:255–288. https://doi.org/10.1146/annurev-environ-012420-045120
Grime JP (1998) Benefits of plant diversity to ecosystems: immediate, filter and founder effects. J Ecol 86:902–910. https://doi.org/10.1046/j.1365-2745.1998.00306.x
Haberl H, Erb KH, Krausmann F, Gaube V, Bondeau A, Plutzar C, Gingrich S, Lucht W, Fischer-Kowalski M (2007) Quantifying and mapping the human appropriation of net primary production in earth’s terrestrial ecosystems. Proc Natl Acad Sci USA 104:12942–12947. https://doi.org/10.1073/pnas.0704243104
Hao T, Song L, Goulding K, Zhang F, Liu X (2018) Cumulative and partially recoverable impacts of nitrogen addition on a temperate steppe. Ecol Appl 28:237–248. https://doi.org/10.1002/eap.1647
Hautier Y, Niklaus PA, Hector A (2009) Competition for light causes plant biodiversity loss after eutrophication. Science 324:636–638. https://doi.org/10.1126/science.1169640
Heldt H-W, Piechulla B (2021) Nitrate assimilation is essential for the biosynthesis of organic matter. In: H-W Heldt, B Piechulla (eds) Plant Biochemistry (Fifth Edition). Academic Press.
Joseph G, Henry HAL (2009) Retention of surface nitrate additions in a temperate old field: implications for atmospheric nitrogen deposition over winter and plant nitrogen availability. Plant Soil 319:209–218. https://doi.org/10.1007/s11104-008-9862-3
Kahmen A, Renker C, Unsicker SB, Buchmann N (2006) Niche complementarity for nitrogen: An explanation for the biodiversity and ecosystem functioning relationship? Ecology 87:1244–1255. https://doi.org/10.1890/0012-9658(2006)87[1244:NCFNAE]2.0.CO;2
Kim S (2015) ppcor: An R Package for a Fast Calculation to Semi-partial Correlation Coefficients. CSAM 22:665–674. https://doi.org/10.5351/CSAM.2015.22.6.665
Knapp AK, Ciais P, Smith MD (2017) Reconciling inconsistencies in precipitation–productivity relationships: implications for climate change. New Phytol 214:41–47. https://doi.org/10.1111/nph.14381
Krausmann F, Erb K-H, Gingrich S, Haberl H, Bondeau A, Gaube V, Lauk C, Plutzar C, Searchinger TD (2013) Global human appropriation of net primary production doubled in the 20th century. Proc Natl Acad Sci USA 110:10324–10329. https://doi.org/10.1073/pnas.1211349110
La Pierre KJ, Blumenthal DM, Brown CS, Klein JA, Smith MD (2016) Drivers of variation in aboveground net primary productivity and plant community composition differ across a broad precipitation gradient. Ecosystems 19:521–533. https://doi.org/10.1007/s10021-015-9949-7
Larsen KS, Michelsen A, Jonasson S, Beier C, Grogan P (2012) Nitrogen uptake during fall, winter and spring differs among plant functional groups in a subarctic heath ecosystem. Ecosystems 15:927–939. https://doi.org/10.1007/s10021-012-9555-x
LeBauer DS, Treseder KK (2008) Nitrogen limitation of net primary productivity in terrestrial ecosystems is globally distributed. Ecology 89:371–379. https://doi.org/10.1890/06-2057.1
Li J, Zhao Y, Zhang A, Song B, Hill RL (2021) Effect of grazing exclusion on nitrous oxide emissions during freeze-thaw cycles in a typical steppe of Inner Mongolia. Agr Ecosyst Environ 307:107217. https://doi.org/10.1016/j.agee.2020.107217
Liu X, Zhang Y, Han W, Tang A, Shen J, Cui Z, Vitousek P, Erisman JW, Goulding K, Christie P, Fangmeier A, Zhang F (2013) Enhanced nitrogen deposition over China. Nature 494:459–462. https://doi.org/10.1038/nature11917
Lu P, Hao T, Li X, Wang H, Zhai X, Tian Q, Bai W, Stevens C, Zhang W-H (2021) Ambient nitrogen deposition drives plant-diversity decline by nitrogen accumulation in a closed grassland ecosystem. J Appl Ecol 58:1888–1898. https://doi.org/10.1111/1365-2664.13858
Lü X-T, Liu Z-Y, Hu Y-Y, Zhang H-Y (2018) Testing nitrogen and water co-limitation of primary productivity in a temperate steppe. Plant Soil 432:119–127. https://doi.org/10.1007/s11104-018-3791-6
Ma L, Liu G, Xu X, Xin X, Bai W, Zhang L, Chen S, Wang R (2018) Nitrogen acquisition strategies during the winter-spring transitional period are divergent at the species level yet convergent at the ecosystem level in temperate grasslands. Soil Biol Biochem 122:150–159. https://doi.org/10.1016/j.soilbio.2018.04.020
Ma L, Xu X, Zhang C, Lv Y, Liu G, Zhang Q, Feng J, Wang R (2021) Strong non-growing season N uptake by deciduous trees in a temperate forest: a 15N isotopic experiment. J Ecol. https://doi.org/10.1111/1365-2745.13754
Migliavacca M, Musavi T, Mahecha MD, Nelson JA, Knauer J, Baldocchi DD, Perez-Priego O, Christiansen R, Peters J, Anderson K, Bahn M, Black TA, Blanken PD, Bonal D, Buchmann N, Caldararu S, Carrara A, Carvalhais N, Cescatti A, Chen J, Cleverly J, Cremonese E, Desai AR, El-Madany TS, Farella MM, Fernández-Martínez M, Filippa G, Forkel M, Galvagno M, Gomarasca U, Gough CM, Göckede M, Ibrom A, Ikawa H, Janssens IA, Jung M, Kattge J, Keenan TF, Knohl A, Kobayashi H, Kraemer G, Law BE, Liddell MJ, Ma X, Mammarella I, Martini D, Macfarlane C, Matteucci G, Montagnani L, Pabon-Moreno DE, Panigada C, Papale D, Pendall E, Penuelas J, Phillips RP, Reich PB, Rossini M, Rotenberg E, Scott RL, Stahl C, Weber U, Wohlfahrt G, Wolf S, Wright IJ, Yakir D, Zaehle S, Reichstein M (2021) The three major axes of terrestrial ecosystem function. Nature 598:468–472. https://doi.org/10.1038/s41586-021-03939-9
Müller C, Martin M, Stevens RJ, Laughlin RJ, Kammann C, Ottow JCG, Jäger HJ (2002) Processes leading to N2O emissions in grassland soil during freezing and thawing. Soil Biol Biochem 34:1325–1331. https://doi.org/10.1016/S0038-0717(02)00076-7
Peng Y, Chen HYH, Yang Y (2020) Global pattern and drivers of nitrogen saturation threshold of grassland productivity. Funct Ecol 34:1979–1990. https://doi.org/10.1111/1365-2435.13622
R Core Team (2020). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/. (accessed by Nov. 2020)
Ravenek JM, Mommer L, Visser EJW, van Ruijven J, van der Paauw JW, Smit-Tiekstra A, de Caluwe H, de Kroon H (2016) Linking root traits and competitive success in grassland species. Plant Soil 407:39–53. https://doi.org/10.1007/s11104-016-2843-z
Ren Z, Zhang Y, Zhang Y (2021) Nitrogen deposition magnifies the positive response of plant community production to precipitation: ammonium to nitrate ratio matters. Environ Pollut 276:116659. https://doi.org/10.1016/j.envpol.2021.116659
Rosseel Y (2012) lavaan: an R package for structural equation modeling. J Stat Softw 48:1–36. https://doi.org/10.18637/jss.v048.i02
Seabloom EW, Adler PB, Alberti J, Biederman L, Buckley YM, Cadotte MW, Collins SL, Dee L, Fay PA, Firn J, Hagenah N, Harpole WS, Hautier Y, Hector A, Hobbie SE, Isbell F, Knops JMH, Komatsu KJ, Laungani R, MacDougall A, McCulley RL, Moore JL, Morgan JW, Ohlert T, Prober SM, Risch AC, Schuetz M, Stevens CJ, Borer ET (2021) Increasing effects of chronic nutrient enrichment on plant diversity loss and ecosystem productivity over time. Ecology 102:e03218. https://doi.org/10.1002/ecy.3218
Šmilauerová M, Šmilauer P (2010) First come, first served: grasses have a head start on forbs with prompt nutrient patch occupation. Plant Soil 328:327–336. https://doi.org/10.1007/s11104-009-0112-0
Smith MD, Knapp AK, Collins SL (2009) A framework for assessing ecosystem dynamics in response to chronic resource alterations induced by global change. Ecology 90:3279–3289. https://doi.org/10.1890/08-1815.1
Stevens CJ, Lind EM, Hautier Y, Harpole WS, Borer ET, Hobbie S, Seabloom EW, Ladwig L, Bakker JD, Chu C, Collins S, Davies KF, Firn J, Hillebrand H, Pierre KJL, MacDougall A, Melbourne B, McCulley RL, Morgan J, Orrock JL, Prober SM, Risch AC, Schuetz M, Wragg PD (2015) Anthropogenic nitrogen deposition predicts local grassland primary production worldwide. Ecology 96:1459–1465. https://doi.org/10.1890/14-1902.1
Tang Z, Deng L, An H, Yan W, Shangguan Z (2017) The effect of nitrogen addition on community structure and productivity in grasslands: a meta-analysis. Ecol Eng 99:31–38. https://doi.org/10.1016/j.ecoleng.2016.11.039
Tian Q, Yang L, Ma P, Zhou H, Liu N, Bai W, Wang H, Ren L, Lu P, Han W, Schultz PA, Bever JD, Zhang F-S, Lambers H, Zhang W-H (2020) Belowground-mediated and phase-dependent processes drive nitrogen-evoked community changes in grasslands. J Ecol 108:1874–1887. https://doi.org/10.1111/1365-2745.13415
Tischner R (2000) Nitrate uptake and reduction in higher and lower plants. Plant, Cell Environ 23:1005–1024. https://doi.org/10.1046/j.1365-3040.2000.00595.x
Van Sundert K, Arfin Khan MAS, Bharath S, Buckley YM, Caldeira MC, Donohue I, Dubbert M, Ebeling A, Eisenhauer N, Eskelinen A, Finn A, Gebauer T, Haider S, Hansart A, Jentsch A, Kübert A, Nijs I, Nock CA, Nogueira C, Porath-Krause AJ, Radujković D, Raynaud X, Risch AC, Roscher C, Scherer-Lorenzen M, Schuchardt MA, Schütz M, Siebert J, Sitters J, Spohn M, Virtanen R, Werner C, Wilfahrt P, Vicca S (2021) Fertilized graminoids intensify negative drought effects on grassland productivity. Glob Change Biol 27:2441–2457. https://doi.org/10.1111/gcb.15583
Vitousek PM, Howarth RW (1991) Nitrogen limitation on land and in the sea: how can it occur? Biogeochemistry 13:87–115. https://doi.org/10.1007/BF00002772
Wang L, Macko SA (2011) Constrained preferences in nitrogen uptake across plant species and environments. Plant Cell Environ 34:525–534. https://doi.org/10.1111/j.1365-3040.2010.02260.x
Wang R, Peñuelas J, Li T, Liu H, Wu H, Zhang Y, Sardans J, Jiang Y (2021) Natural abundance of 13C and 15N provides evidence for plant–soil carbon and nitrogen dynamics in a N-fertilized meadow. Ecology 102:e03348. https://doi.org/10.1002/ecy.3348
Xi N, Zhu B-R, Zhang D-Y (2017) Contrasting grass nitrogen strategies reflect interspecific trade-offs between nitrogen acquisition and use in a semi-arid temperate grassland. Plant Soil 418:267–276. https://doi.org/10.1007/s11104-017-3296-8
Xu X, Ouyang H, Richter A, Wanek W, Cao G, Kuzyakov Y (2011) Spatio-temporal variations determine plant–microbe competition for inorganic nitrogen in an alpine meadow. J Ecol 99:563–571. https://doi.org/10.1111/j.1365-2745.2010.01789.x
You C, Wu F, Gan Y, Yang W, Hu Z, Xu Z, Tan B, Liu L, Ni X (2017) Grass and forbs respond differently to nitrogen addition: a meta-analysis of global grassland ecosystems. Sci Rep 7:1563. https://doi.org/10.1038/s41598-017-01728-x
Yu G, Jia Y, He N, Zhu J, Chen Z, Wang Q, Piao S, Liu X, He H, Guo X, Wen Z, Li P, Ding G, Goulding K (2019) Stabilization of atmospheric nitrogen deposition in China over the past decade. Nat Geosci 12:424–429. https://doi.org/10.1038/s41561-019-0352-4
Yue K, Fornara DA, Li W, Ni X, Peng Y, Liao S, Tan S, Wang D, Wu F, Yang Y (2020) Nitrogen addition affects plant biomass allocation but not allometric relationships among different organs across the globe. J Plant Ecol 14:361–371. https://doi.org/10.1093/jpe/rtaa100
Zhang J, Cai Z, Müller C (2018a) Terrestrial N cycling associated with climate and plant-specific N preferences: a review. Eur J Soil Sci 69:488–501. https://doi.org/10.1111/ejss.12533
Zhang J, Wang J, Müller C, Cai Z (2016) Ecological and practical significances of crop species preferential N uptake matching with soil N dynamics. Soil Biol Biochem 103:63–70. https://doi.org/10.1016/j.soilbio.2016.08.009
Zhang Y, Feng J, Isbell F, Lü X, Han X (2015) Productivity depends more on the rate than the frequency of N addition in a temperate grassland. Sci Rep 5:12558. https://doi.org/10.1038/srep12558
Zhang Y, Han X, He N, Long M, Huang J, Zhang G, Wang Q, Han X (2014a) Increase in ammonia volatilization from soil in response to N deposition in Inner Mongolia grasslands. Atmos Environ 84:156–162. https://doi.org/10.1016/j.atmosenv.2013.11.052
Zhang Y, Loreau M, He N, Wang J, Pan Q, Bai Y, Han X (2018b) Climate variability decreases species richness and community stability in a temperate grassland. Oecologia 188:183–192. https://doi.org/10.1007/s00442-018-4208-1
Zhang Y, Lü X, Isbell F, Stevens C, Han X, He N, Zhang G, Yu Q, Huang J, Han X (2014b) Rapid plant species loss at high rates and at low frequency of N addition in temperate steppe. Glob Change Biol 20:3520–3529. https://doi.org/10.1111/gcb.12611
Zhang Y, Wang J, Stevens CJ, Lü X, He N, Wang C, Han X (2018c) Effects of the frequency and the rate of N enrichment on community structure in a temperate grassland. Journal of Plant Ecology 11:685–695. https://doi.org/10.1093/jpe/rtx041
Zheng Z, Bai W, Zhang W-H (2019) Root trait-mediated belowground competition and community composition of a temperate steppe under nitrogen enrichment. Plant Soil 437:341–354. https://doi.org/10.1007/s11104-019-03989-z
Zhou M, Bai W, Zhang Y, Zhang W-H (2018) Multi-dimensional patterns of variation in root traits among coexisting herbaceous species in temperate steppes. J Ecol 106:2320–2331. https://doi.org/10.1111/1365-2745.12977
Zhuang W, Li J, Yu F, Dong Z, Guo H (2020) Seasonal nitrogen uptake strategies in a temperate desert ecosystem depends on N form and plant species. Plant Biol 22:386–393. https://doi.org/10.1111/plb.13083
Acknowledgements
We thank Xiaoliang Wang, Yanhui Zhang, Hongying, Li Yuqin Zong, and Huiling Tian for assistance and the anonymous reviewers for their insightful comments. We appreciate the Inner Mongolia Grassland Ecosystem Research Station for the experimental facility support. This work was funded by National Natural Science Foundation of China (32071603 and 32122055) and the Strategic Priority Research Program of the Chinese Academy of Sciences (XDA26020101).
Funding
This work was funded by National Natural Science Foundation of China (Grant numbers [32071603] and [32122055]) and the Strategic Priority Research Program of the Chinese Academy of Sciences (Grant numbers [XDA26020101]).
Author information
Authors and Affiliations
Contributions
Yunhai Zhang contributed to the study conception and design. Data collection and analysis were performed by Changchun Song, Yuqiu Zhang, Zhengru Ren, Haining Lu, Xu Chen, Ruoxuan Liu, Jungang Chen, and Yunhai Zhang. The first draft of the manuscript was written by Changchun Song and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Competing interests
We declare no conflict of interests.
Additional information
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Responsible Editor: Devrim Coskun.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Song, C., Zhang, Y., Ren, Z. et al. Soil nitrate mediates the responses of plant community production to the frequency of N addition in a temperate grassland: a decadal field experiment. Plant Soil 491, 9–20 (2023). https://doi.org/10.1007/s11104-022-05435-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11104-022-05435-z