Skip to main content
SpringerLink
Log in

Unraveling the consequences of nitrogen addition on soil phosphorus fractions in alpine grasslands: insights from field experiments and global analysis

  • Frontiers in Soils and Sediments • Research Article
  • Published:
Journal of Soils and Sediments Aims and scope Submit manuscript

Abstract

Purpose

The escalation of nitrogen (N) deposition has resulted in phosphorus (P) limitation in alpine grasslands on the Qinghai–Tibetan Plateau (QTP). However, the impact of N deposition affects soil P transformations in alpine grasslands, and whether there is a universal pattern of N-induced soil P fraction change in terrestrial ecosystems is still not well understood.

Methods

We performed field experiments in two alpine grasslands on the QTP and a meta-analysis including 1033 records worldwide to analyze the responses of soil P fractions to N addition.

Results

We found that N addition significantly altered soil P fractions in alpine meadow, whereas it induced a minor response in alpine steppe. The N addition induced a decrease in soil inorganic phosphorus (Pi) in the alpine meadow, resulting from occluded P (i.e., C.HCl-Pt and residual-Pt). Though N addition did not change total organic P (Po) concentration, there were remarkable changes among soil organic P fractions (C.HCl-Po, NaOH-Po, and NaHCO3-Po) in the alpine meadow, with an increase in NaOH-Po but a decrease in C.HCl-Po. Soil inorganic P in the alpine meadow was associated with Ca2+ and soil pH that was also reduced by N addition. By contrast, meta-analysis results showed that N addition significantly increased the lnRR of NaOH-Pi, but decreased lnRR of C.HCl-Pt and marginally reduced lnRR of NaHCO3-Po across all terrestrial ecosystems. Among multiple environmental and experimental variables, soil pH, mean annual temperature (MAT), mean annual precipitation (MAP), N forms, and soil phosphatase activity mainly drove the response of NaHCO3-Po to N addition at the large scale. Structural equation model (SEM) further showed that soil phosphatase activity was the main direct factor controlling NaHCO3-Po response.

Conclusions

Our results suggest that soil P fractions are more sensitive to N addition in alpine meadow than in alpine steppe. The reduction of inorganic P fractions and uneven changes of organic P fractions in alpine meadow suggested that N addition may accelerate inorganic P dissolution but depress organic P mineralization. Environmental factor (e.g., MAP) and experimental variables (N rate) affected soil P fractions in response to N addition mediated by soil pH and enzymatic activities. Collectively, these findings improved our understanding of the consequences of N addition on soil organic and inorganic P transformations and predicted the trajectory of soil phosphorus fraction change under increasing N deposition.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

5 References

  • Augusto L, Achat DL, Jonard M et al (2017) Soil parent material-a major driver of plant nutrient limitations in terrestrial ecosystems. Glob Chang Biol 23:3808–3824

    Article  Google Scholar 

  • Block CE, Knoepp JD, Fraterrigo JM et al (2012) Interactive effects of disturbance and nitrogen availability on phosphorus dynamics of southern Appalachian forests. Biogeochemistry 112:329–342

    Article  Google Scholar 

  • Buol SW, Southard RJ, Graham RC et al (2011) Soil genesis and classification. John Wiley & Sons

    Book  Google Scholar 

  • Calcagno V, de Mazancourt C (2010) glmulti: an R package for easy automated model selection with (generalized) linear models. J Stat Softw 34:1–29

    Article  Google Scholar 

  • Chen H, Chen ML, Li DJ et al (2018a) Responses of soil phosphorus availability to nitrogen addition in a legume and a non-legume plantation. Geoderma 322:12–21

    Article  CAS  Google Scholar 

  • Chen J, Luo YQ, Garcia-Palacios P et al (2018b) Differential responses of carbon-degrading enzyme activities to warming: implications for soil respiration. Glob Chang Biol 24:4816–4826

    Article  Google Scholar 

  • Chen J, van Groenigen KJ, Hungate BA et al (2020) Long-term nitrogen loading alleviates phosphorus limitation in terrestrial ecosystems. Glob Chang Biol 26:5077–5086

    Article  Google Scholar 

  • Chen J, Moorhead DL (2022) Progressively decreased nitrogen-stimulation of soil phosphatase activity with long-term nitrogen addition. Appl Soil Ecol 169:104213

    Article  Google Scholar 

  • Chen XL, Chen HYH, Chang SX et al (2022) Meta-analysis shows that plant mixtures increase soil phosphorus availability and plant productivity in diverse ecosystems. Nat Ecol Evol 6:1112–1121

    Article  Google Scholar 

  • Cross AF, Schlesinger WH (1995) A literature review and evaluation of the Hedley fractionation: applications to the biogeochemical cycle of soil phosphorus in natural ecosystems. Geoderma 64:197–214

    Article  CAS  Google Scholar 

  • Dai ZM, Liu GF, Chen HH et al (2019) Long-term nutrient inputs shift soil microbial functional profiles of phosphorus cycling in diverse agroecosystems. ISME J 14:757–770

    Article  Google Scholar 

  • Deng M, Liu L, Sun Z et al (2016) Increased phosphate uptake but not resorption alleviates phosphorus deficiency induced by nitrogen deposition in temperate Larix principis-rupprechtii plantations. New Phytol 212:1019–1029

    Article  CAS  Google Scholar 

  • Deng Q, Hui DF, Dennis S et al (2017) Responses of terrestrial ecosystem phosphorus cycling to nitrogen addition: a meta-analysis. Global Ecol Biogeogr 26:713–728

    Article  Google Scholar 

  • Ding WL, Cong WF, Lambers H (2021) Plant phosphorus-acquisition and -use strategies affect soil carbon cycling. Trends Ecol Evol 36:899–906

    Article  CAS  Google Scholar 

  • Dong JF, Che RX, Jia SG et al (2019) Responses of ammonia-oxidizing archaea and bacteria to nitrogen and phosphorus amendments in an alpine steppe. Eur J Soil Sci 71:940–954

    Article  Google Scholar 

  • Dong JF, Cui XY, Niu HS et al (2022) Effects of nitrogen addition on plant properties and microbiomes under high phosphorus addition level in the alpine steppe. Front Plant Sci 13:89436

    Article  Google Scholar 

  • Elser JJ, Bracken MES, Cleland EE et al (2007) Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine and terrestrial ecosystems. Ecol Lett 10:1135–1142

    Article  Google Scholar 

  • Fan YX, Lin F, Yang LM et al (2018) Decreased soil organic P fraction associated with ectomycorrhizal fungal activity to meet increased P demand under N application in a subtropical forest ecosystem. Biol Fert Soils 54:149–161

    Article  CAS  Google Scholar 

  • Fernandez IJ, Rustad LE, Norton SA et al (2003) Experimental acidification causes soil base-cation depletion at the Bear Brook Watershed in Maine. Soil Sci Soc Am J 67:1909–1919

    Article  CAS  Google Scholar 

  • Garcia-Palacios P, Vandegehuchte ML, Shaw EA et al (2015) Are there links between responses of soil microbes and ecosystem functioning to elevated CO2, N deposition and warming? A global perspective. Glob Change Biol 21:1590–1600

    Article  Google Scholar 

  • Hedges LV, Gurevitch J, Curtis PS et al (1999) The meta-analysis of response ratios in experimental ecology. Ecology 80:1150–1156

    Article  Google Scholar 

  • Hedley MJ, Stewart JWB, Chauhan BS (1982) Changes in inorganic and organic soil phosphorus fractions induced by cultivation practices and by laboratory incubations. Soil Sci Soc Am J 46:970–976

    Article  CAS  Google Scholar 

  • Helfenstein J, Pistocchi C, Oberson A et al (2020) Estimates of mean residence times of phosphorus in commonly considered inorganic soil phosphorus pools. Biogeosciences 17:441–454

    Article  CAS  Google Scholar 

  • Hendershot WH, Lalande H, Duquette M (2007) Ion exchange and exchangeable cations. Soil sampling and methods of analysis, 2nd edn. CRC Press, Boca Raton, FL, USA, pp 197–206

  • Hou EQ, Chen CR, Luo YQ et al (2018a) Effects of climate on soil phosphorus cycle and availability in natural terrestrial ecosystems. Glob Chang Biol 24:3344–3356

    Article  Google Scholar 

  • Hou EQ, Tan X, Heenan M et al (2018b) A global dataset of plant available and unavailable phosphorus in natural soils derived by Hedley method. Sci Data 5:180166

    Article  CAS  Google Scholar 

  • Hou EQ, Wen DZ, Kuang YW et al (2018c) Soil pH predominantly controls the forms of organic phosphorus in topsoils under natural broadleaved forests along a 2500 km latitudinal gradient. Geoderma 315:65–74

    Article  CAS  Google Scholar 

  • Hou EQ, Luo YQ, Kuang YW et al (2020) Global meta-analysis shows pervasive phosphorus limitation of aboveground plant production in natural terrestrial ecosystems. Nat Commun 11:637

    Article  CAS  Google Scholar 

  • Hou EQ, Wen DZ, Jiang LF et al (2021) Latitudinal patterns of terrestrial phosphorus limitation over the globe. Ecol Lett 24:1420–1431

    Article  Google Scholar 

  • Jiang LL, Wang SP, Pang Z et al (2016) Grazing modifies inorganic and organic nitrogen uptake by coexisting plant species in alpine grassland. Biol Fert Soils 52:211–221

    Article  CAS  Google Scholar 

  • Kritzler UH, Johnson D (2009) Mineralisation of carbon and plant uptake of phosphorus from microbially-derived organic matter in response to 19 years simulated nitrogen deposition. Plant Soil 326:311–319

    Article  Google Scholar 

  • Kumar V, Gill KD (2018) To estimate the activity of alkaline phosphatase in serum. In: Basic concepts in clinical biochemistry: a practical guide. Springer, Singapore

  • Lefcheck JS (2016) piecewiseSEM: piecewise structural equation modelling in R for ecology, evolution, and systematics. Methods Ecol Evol 7:573–579

    Article  Google Scholar 

  • Li Q, Lv JH, Peng CH et al (2021) Nitrogen-addition accelerates phosphorus cycling and changes phosphorus use strategy in a subtropical Moso bamboo forest. Environ Res Lett 16:024023

    Article  CAS  Google Scholar 

  • Li YY, Dong SK, Wen L et al (2014) Soil carbon and nitrogen pools and their relationship to plant and soil dynamics of degraded and artificially restored grasslands of the Qinghai-Tibetan Plateau. Geoderma 213:178–184

    Article  CAS  Google Scholar 

  • Li ZL, Zhang DY, Peng YF et al (2022) Divergent drivers of various topsoil phosphorus fractions across Tibetan alpine grasslands. J Geophys Res-Biogeo 127:e2022JG006795

  • Lu CQ, Tian HQ (2007) Spatial and temporal patterns of nitrogen deposition in China: synthesis of observational data. J Geophys Res-Biogeo-Atmos 112:D22S05

  • Lu XK, Mo JM, Gilliam FS et al (2012) Nitrogen addition shapes soil phosphorus availability in two reforested tropical forests in Southern China. Biotropica 44:302–311

    Article  Google Scholar 

  • Luo M, Moorhead DL, Ochoa-Hueso R et al (2022) Nitrogen loading enhances phosphorus limitation in terrestrial ecosystems with implications for soil carbon cycling. Funct Ecol 36:2845–2858

    Article  CAS  Google Scholar 

  • Mahowald N, Jickells TD, Baker AR et al (2008) Global distribution of atmospheric phosphorus sources, concentrations and deposition rates, and anthropogenic impacts. Global Biogeochem Cy 22:GB4026

  • Neal AL, Glendining MJ (2019) Calcium exerts a strong influence upon phosphohydrolase gene abundance and phylogenetic diversity in soil. Soil Biol Biochemistry 139:107613

    Article  CAS  Google Scholar 

  • Penuelas J, Janssens IA, Ciais P et al (2020) Anthropogenic global shifts in biospheric N and P concentrations and ratios and their impacts on biodiversity, ecosystem productivity, food security, and human health. Glob Chang Biol 26:1962–1985

    Article  Google Scholar 

  • Team RC (2020) R: a language and environment for statistical computing, version 4.1.0. Vienna, Austria: R Found Stat Comput 2013

  • Tiessen H, Moir JO (1993) Characterization of available P by sequential extraction. soil sampling and methods of analysis. Lewis Publishers, Boca Raton 75–86

  • Tran CTK, Watts-Williams SJ, Smernik RJ et al (2020) Effects of plant roots and arbuscular mycorrhizas on soil phosphorus leaching. Sci Total Environ 722:137847

    Article  CAS  Google Scholar 

  • Turner BL, Lambers H, Condron LM et al (2012) Soil microbial biomass and the fate of phosphorus during long-term ecosystem development. Plant Soil 367:225–234

    Article  Google Scholar 

  • Turner BL, Wright SJ (2013) The response of microbial biomass and hydrolytic enzymes to a decade of nitrogen, phosphorus, and potassium addition in a lowland tropical rain forest. Biogeochemistry 117:115–130

    Article  Google Scholar 

  • Wang DJ, Zhou HK, Yao BQ et al (2020) Effects of nutrient addition on degraded alpine grasslands of the Qinghai-Tibetan Plateau: a meta-analysis. Agr Ecosyst Environ 301:106970

    Article  CAS  Google Scholar 

  • Wang RZ, Yang JJ, Liu HY (2022a) Nitrogen enrichment buffers phosphorus limitation by mobilizing mineral-bound soil phosphorus in grasslands. Ecology 103:e3616

    Article  Google Scholar 

  • Wang YF, Jiang LL, Wang ZS et al (2022b) Phosphorus enrichment increased community stability by increasing asynchrony and dominant species stability in alpine meadow of Qinghai‐Tibet Plateau. J Geophys Res-Biogeo 127:e2022bJG006819

  • Xu H, Qu Q, Li G et al (2022) Impact of nitrogen addition on plant-soil-enzyme C-N–P stoichiometry and microbial nutrient limitation. Soil Biol Biochemistry 170:108714

    Article  CAS  Google Scholar 

  • Yang GB, Peng YF, Abbott BW et al (2021) Phosphorus rather than nitrogen regulates ecosystem carbon dynamics after permafrost thaw. Glob Chang Biol 27:5818–5830

    Article  CAS  Google Scholar 

  • Yang K, Zhu JJ, Gu JC et al (2015) Changes in soil phosphorus fractions after 9 years of continuous nitrogen addition in a Larix gmelinii plantation. Ann Forest Sci 72:435–442

    Article  Google Scholar 

  • Yang X, Post WM (2011) Phosphorus transformations as a function of pedogenesis: a synthesis of soil phosphorus data using Hedley fractionation method. Biogeosciences 8:2907–2916

    Article  CAS  Google Scholar 

  • Yao XY, Hui DF, Hou EQ et al (2022) Differential responses and mechanistic controls of soil phosphorus transformation in Eucalyptus plantations with N fertilization and introduced N2-fixing tree species. New Phytol 237:2039–2053

    Article  Google Scholar 

  • Yu GR, Jia YL, He NP et al (2019) Stabilization of atmospheric nitrogen deposition in China over the past decade. Nat Geosci 12:424–429

    Article  CAS  Google Scholar 

  • Zeng QX, Zeng XM, Lin KM et al (2020) Responses of soil phosphorus fractions and microorganisms to nitrogen application in a subtropical Phyllostachys pubescen forest. J Appl Ecol 31:753–760

    Google Scholar 

  • Zhang HZ, Shi LL, Fu SL et al (2020) Effects of nitrogen deposition and increased precipitation on soil phosphorus dynamics in a temperate forest. Geoderma 380:114650

    Article  CAS  Google Scholar 

  • Zhou J, Li XL, Peng F et al (2021) Mobilization of soil phosphate after 8 years of warming is linked to plant phosphorus-acquisition strategies in an alpine meadow on the Qinghai-Tibetan Plateau. Glob Chang Biol 27:6578–6591

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank for all the researchers whose data were included in this meta-analysis.

Funding

This work was supported by the National Natural Science Foundation of China (42041005, 31971530).

Author information

Authors and Affiliations

  1. College of Life Sciences, University of the Chinese Academy of Sciences, Beijing, 100049, China

    Wenchao Wu, Yanbin Hao & Xiaoyong Cui

  2. CAS Center for Excellence in Tibetan Plateau Earth Sciences, Chinese Academy of Sciences, Beijing, 100049, China

    Xiaoyong Cui

  3. State Key Laboratory of Tibetan Plateau Earth System Science (LATPES), Institute of Tibetan Plateau Research, Chinese Academy of Sciences, Beijing, 100049, China

    Lili Jiang

  4. AgroBioSciences Program, Mohammed VI Polytechnic University (UM6P), , Hay Moulay Rachid, 43150, Ben Guerir, Morocco

    Touhami Driss

  5. Yanshan Earth Critical Zone and Surface Fluxes Research Station, Chinese Academy of Sciences, Beijing, 100049, China

    Yanbin Hao & Xiaoyong Cui

  6. Quantitative Sustainability Assessment, Department of Environmental and Resource Engineering, Technical University of Denmark, Produktionstorvet 424, 2800 Kgs, Lyngby, Denmark

    Tong Li

  7. School of Environment and Science, Centre for Planetary Health and Food Security, Griffith University, Nathan, Brisbane, QLD, 4111, Australia

    Tong Li & Zhihong Xu

Authors
  1. Wenchao Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Lili Jiang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Tong Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Touhami Driss
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Zhihong Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yanbin Hao
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Xiaoyong Cui
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Xiaoyong Cui.

Ethics declarations

Conflict of interest

The authors declare no competing interests.

Additional information

Responsible editor: Caixian Tang

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wu, W., Jiang, L., Li, T. et al. Unraveling the consequences of nitrogen addition on soil phosphorus fractions in alpine grasslands: insights from field experiments and global analysis. J Soils Sediments 23, 3721–3734 (2023). https://doi.org/10.1007/s11368-023-03639-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11368-023-03639-z

Keywords

Search

Navigation