Skip to main content

Advertisement

SpringerLink
Log in

Nitrogen Addition in a Tibetan Alpine Meadow Increases Intraspecific Variability in Nitrogen Uptake, Leading to Increased Community-level Nitrogen Uptake

  • Published:
Ecosystems Aims and scope Submit manuscript

Abstract

Plant nitrogen (N) uptake is a critical ecosystem function, especially when terrestrial ecosystems are threatened worldwide by increasing anthropogenic N deposition. However, the mechanisms by which biotic factors mediate the effects of increases in N addition on community N uptake remain unknown. Here, we determine how inter- and intraspecific differences contribute to this response by decomposing N uptake in a specific community in a 7-year NH4NO3 addition experiment in a Tibetan alpine meadow using variance partitioning approach. We measured both plant N uptake from ammonium and nitrate of 25 common species in control plots and community-level uptake along a N addition gradient, using short-term in situ 15N labeling. Plant community composition, soil properties (soil ammonium and nitrate, pH, Al3+ and base cations), soil microbial biomass carbon and nitrogen were measured and recorded. We found that N addition increased community-level N uptake by significantly increasing individual species’ variability of N uptake (that is, positive intraspecific variability), although with limited effect of community composition shift. The significantly positive intraspecific variability from ammonium and nitrate along the N addition gradient was caused by increased soil available N and soil acidification with N addition. The limited effect of community composition shift means that N addition increased community-level N uptake with only limited species filtering. Our results provide a novel insight into the mechanism of how N addition affects community-level N uptake, by linking physiological, community and ecosystem function, and highlight the important role that intraspecific variability of N uptake plays.

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

Figure 1
Figure 2
Figure 3
Figure 4

Similar content being viewed by others

Data Accessibility

All data supporting the manuscript are presented, and additional information related is available from the corresponding author if reasonable request.

References

  • Baumann F, HE JS, Schmidt K, Kuehn P, Scholten T. 2009. Pedogenesis, permafrost, and soil moisture as controlling factors for soil nitrogen and carbon contents across the Tibetan Plateau. Global Change Biology 15(12):3001–3017.

    Article  Google Scholar 

  • Bentos TV, Mesquita RC, Camargo JL, Williamson GB. 2014. Seed and fruit tradeoffs–the economics of seed packaging in Amazon pioneers. Plant Ecology & Diversity 7(1–2):371–382.

    Article  Google Scholar 

  • Bobbink R, Hicks K, Galloway J, Spranger T, Alkemade R, Ashmore M, and others 2010. Global assessment of nitrogen deposition effects on terrestrial plant diversity: a synthesis. Ecological applications 20(1):30–59.

    Article  CAS  PubMed  Google Scholar 

  • Brix H, Dyhr-Jensen K, Lorenzen B. 2002. Root-zone acidity and nitrogen source affects Typha latifolia L. growth and uptake kinetics of ammonium and nitrate. Journal of Experimental Botany 53(379):2441–2450.

    Article  CAS  PubMed  Google Scholar 

  • Chapin FS II. 1980. The mineral nutrition of wild plants. Annual Review of Ecology and Systematics 11(1):233–260.

    Article  CAS  Google Scholar 

  • Chen D, Li J, Lan Z, Hu S, Bai Y. 2016. Soil acidification exerts a greater control on soil respiration than soil nitrogen availability in grasslands subjected to long-term nitrogen enrichment. Functional Ecology 30(4):658–669.

    Article  Google Scholar 

  • Clark CM, Tilman D. 2008. Loss of plant species after chronic low-level nitrogen deposition to prairie grasslands. Nature 451(7179):712–715.

    Article  CAS  PubMed  Google Scholar 

  • De Vries FT, Bardgett RD. 2016. Plant community controls on short-term ecosystem nitrogen retention. New Phytologist 210(3):861–874.

    Article  Google Scholar 

  • Emmett BA. 2007. Nitrogen saturation of terrestrial ecosystems: some recent findings and their implications for our conceptual framework. In: Brimblecombe P, Hara H, Houle D, Novak M, Eds. Acid Rain-Deposition to Recovery, . Dordrech, Netherlands: Springer. pp 99–109.

    Chapter  Google Scholar 

  • Fang Y, Xun F, Bai W, Zhang W, Li L. 2012. Long-term nitrogen addition leads to loss of species richness due to litter accumulation and soil acidification in a temperate steppe. PLoS One 7(10):e47369.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Galloway JN, Townsend AR, Erisman JW, Bekunda M, Cai Z, Freney JR, and others 2008. Transformation of the nitrogen cycle: recent trends, questions, and potential solutions. Science 320(5878):889–892.

    Article  CAS  PubMed  Google Scholar 

  • Gruber N, Galloway JN. 2008. An Earth-system perspective of the global nitrogen cycle. Nature 451(7176):293–296.

    Article  CAS  PubMed  Google Scholar 

  • Harpole WS, Sullivan LL, Lind EM, Firn J, Adler PB, Borer ET, and others 2016. Addition of multiple limiting resources reduces grassland diversity. Nature 537(7618):93–96.

    Article  CAS  PubMed  Google Scholar 

  • Hautier Y, Niklaus PA, Hector A. 2009. Competition for light causes plant biodiversity loss after eutrophication. Science 324(5927):636–638.

    Article  CAS  PubMed  Google Scholar 

  • Hawkins BJ, Robbins S. 2010. pH affects ammonium, nitrate and proton fluxes in the apical region of conifer and soybean roots. Physiologia Plantarum 138(2):238–247.

    Article  CAS  PubMed  Google Scholar 

  • Henry LT, Raper JCD. 1989. Effects of root-zone acidity on utilization of nitrate and ammonium in tobacco plants. Journal of Plant Nutrition 12(7):811–826.

    Article  CAS  PubMed  Google Scholar 

  • Hood-Nowotny R, Knols BG. 2007. Stable isotope methods in biological and ecological studies of arthropods. Entomologia Experimentalis et Applicata 124(1):3–16.

    Article  CAS  Google Scholar 

  • Houlton BZ, Sigman DM, Schuur EA, Hedin LO. 2007. A climate-driven switch in plant nitrogen acquisition within tropical forest communities. Proceedings of the National Academy of Sciences 104(21):8902–8906.

    Article  CAS  Google Scholar 

  • Huang Y, Kang R, Mulder J, Zhang T, Duan L. 2015. Nitrogen saturation, soil acidification, and ecological effects in a subtropical pine forest on acid soil in southwest China. Journal of Geophysical Research: Biogeosciences 120(11):2457–2472.

    Article  CAS  Google Scholar 

  • He NP, Li Y, Liu C, He JS, Li MX, Zhang JH, and others 2020. Plant trait networks: improved resolution of the dimensionality of adaptation. Trends in Ecology & Evolution 35(10):908–918.

    Article  Google Scholar 

  • Iversen CM, Bridgham SD, Kellogg LE. 2010. Scaling plant nitrogen use and uptake efficiencies in response to nutrient addition in peatlands. Ecology 91(3):693–707.

    Article  PubMed  Google Scholar 

  • Janssens IA, Dieleman W, Luyssaert S, Subke JA, Reichstein M, Ceulemans R, and others 2010. Reduction of forest soil respiration in response to nitrogen deposition. Nature Geoscience 3(5):315–322.

    Article  CAS  Google Scholar 

  • Kuzyakov Y, Xu XL. 2013. Competition between roots and microorganisms for nitrogen: mechanisms and ecological relevance. New Phytologist 198(3):656–669.

    Article  CAS  Google Scholar 

  • Lea PJ, Azevedo RAD. 2006. Nitrogen use efficiency. 1. Uptake of nitrogen from the soil. Annals of Applied Biology 149(3):243–247.

    Article  CAS  Google Scholar 

  • Lepš J, de Bello F, Šmilauer P, Doležal J. 2011. Community trait response to environment: disentangling species turnover vs intraspecific trait variability effects. Ecography 34(5):856–863.

    Article  Google Scholar 

  • Legendre P, Legendre L. 2012. Numerical Ecology, 3rd edn. Amsterdam: Elsevier.

    Google Scholar 

  • Liu X, Lyu S, Sun D, Bradshaw CJ, Zhou S. 2017. Species decline under nitrogen fertilization increases community-level competence of fungal diseases. Proceedings of the Royal Society B: Biological Sciences 284(1847):20162621.

    Article  PubMed  PubMed Central  Google Scholar 

  • Lu Y, Liu X, Chen F, Zhou S. 2020. Shifts in plant community composition weaken the negative effect of nitrogen addition on community-level arbuscular mycorrhizal fungi colonization. Proceedings of the Royal Society B 287(1927):20200483.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marschner H. 2011. Mineral nutrition of higher plants. London, UK: Academic press.

    Google Scholar 

  • McKane RB, Johnson LC, Shaver GR, Nadelhoffer KJ, Rastetter EB, Fry B, and others 2002. Resource-based niches provide a basis for plant species diversity and dominance in arctic tundra. Nature 415(6867):68–71.

    Article  CAS  PubMed  Google Scholar 

  • Midolo G, Alkemade R, Schipper AM, Benítez-López A, Perring MP, De Vries W. 2019. Impacts of nitrogen addition on plant species richness and abundance: A global meta-analysis. Global Ecology and Biogeography 28(3):398–413.

    Article  Google Scholar 

  • Niu S, Classen AT, Dukes JS, Kardol P, Liu L, Luo Y, and others 2016. Global patterns and substrate-based mechanisms of the terrestrial nitrogen cycle. Ecology Letters 19(6):697–709.

    Article  PubMed  Google Scholar 

  • R Development Core Team. 2019. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria, http://www.r-project.org/

  • Reay DS, Dentener F, Smith P, Grace J, Feely RA. 2008. Global nitrogen deposition and carbon sinks. Nature Geoscience 1(7):430–437.

    Article  CAS  Google Scholar 

  • Rosseel Y. 2012. lavaan: An R Package for Structural Equation Modeling. Journal of Statistical Software 48:1–36.

    Article  Google Scholar 

  • Schlesinger WH. 2009. On the fate of anthropogenic nitrogen. Proceedings of the National Academy of Sciences 106(1):203–208.

    Article  CAS  Google Scholar 

  • Shi ZX, Yu DS, Yang GX, Wang HJ, Sun WX, Du GH, Gong ZT. 2006. Cross-reference benchmarks for translating the genetic soil classification of China into the Chinese soil taxonomy. Pedosphere 16(2):147–153.

    Article  CAS  Google Scholar 

  • Shipley B. 2016. Cause and correlation in biology: A user’s guide to path analysis, structural equations and causal inference with R, 2nd edn. Cambridge: Cambridge University Press.

    Book  Google Scholar 

  • Silvertown J. 2004. Plant coexistence and the niche. Trends in Ecology & Evolution 19(11):605–611.

    Article  Google Scholar 

  • Song L, Bao X, Liu X, Zhang Y, Christie P, Fangmeier A, Zhang F. 2011. Nitrogen enrichment enhances the dominance of grasses over forbs in a temperate steppe ecosystem. Biogeosciences 8(8):2341–2350.

    Article  Google Scholar 

  • Sun Y, Xu X, Kuzyakov Y. 2014. Mechanisms of rhizosphere priming effects and their ecological significance. Chinese Journal of Plant Ecology 38(1):62–75.

    Article  Google Scholar 

  • Tian Q, Liu N, Bai W, Li L, Chen J, Reich PB, and others 2016. A novel soil manganese mechanism drives plant species loss with increased nitrogen deposition in a temperate steppe. Ecology 97(1):65–74.

    Article  PubMed  Google Scholar 

  • Tian D, Niu S. 2012. A global analysis of soil acidification caused by nitrogen addition. Environmental Research Letters 10(2):1714–1721.

    Google Scholar 

  • Troelstra SR, Wagenaar R, Smant W. 1995. Nitrogen utilization by plant species from acid heathland soils: I. Comparison between nitrate and ammonium nutrition at constant low pH. Journal of Experimental Botany 46(9): 1103–1112.

  • Vitousek PM, Aber JD, Howarth RW, Likens GE, Matson PA, Schindler DW, and others 1997. Human alteration of the global nitrogen cycle: sources and consequences. Ecological Applications 7(3):737–750.

    Google Scholar 

  • von Wirén N, Gazzarrini S, Frommer WB. 1997. Regulation of mineral nitrogen uptake in plants. Plant and Soil 196:191–199.

    Article  Google Scholar 

  • Wang F, Shi G, Nicholas O, Yao B, Ji M, Wang W, and others 2018. Ecosystem nitrogen retention is regulated by plant community trait interactions with nutrient status in an alpine meadow. Journal of Ecology 106(4):1570–1581.

    Article  Google Scholar 

  • Wang YY, Hsu PK, Tsay YF. 2012. Uptake, allocation and signaling of nitrate. Trends in Plant Science 17(8):458–467.

    Article  CAS  PubMed  Google Scholar 

  • Xia J, Wan S. 2008. Global response patterns of terrestrial plant species to nitrogen addition. New Phytologist 179(2):428–439.

    Article  CAS  Google Scholar 

  • Zhang L, Zhu T, Liu X, Nie M, Xu X, Zhou S. 2020. Limited inorganic N niche partitioning by nine alpine plant species after long-term nitrogen addition. Science of The Total Environment 718:137270.

    Article  CAS  Google Scholar 

  • Zhao XQ, Zhou XM. 1999. Ecological basis of alpine meadow ecosystem management in Tibet: Haibei alpine meadow ecosystem research station.

  • Zheng D, Zhang Q, Wu S. 2000. Mountain genecology and sustainable development of the Tibetan Plateau. Beijing: Springer Science & Business Media. p p308.

    Book  Google Scholar 

Download references

Acknowledgements

This work was supported by the National Natural Science Foundation of China (31830009 and 31770518) and Hainan University (RZ2000009932) to SZ, and by a CSC (China Scholarship Council) scholarship to LZ. The work was done in Gannan Grassland Ecosystem Field Science Observation and Research Station of the Ministry of Education. We thank Dexin Sun, Shengman Lyu, Xiao Yao, Mengjiao Huang, Shiliang Chen, and Yikang Cheng for helping us perform the field experiment. We also thank Xiang Liu for suggestions.

Author information

Authors and Affiliations

  1. Ministry of Education Key Laboratory for Biodiversity Science and Ecological Engineering, Coastal Ecosystems Research Station of the Yangtze River Estuary, Shanghai Institute of Eco-Chongming (SIEC), and School of Life Sciences, Fudan University, 2005 Songhu Road, Shanghai, 200438, People’s Republic of China

    Li Zhang

  2. Département de Biologie, Université de Sherbrooke, Sherbrooke, Quebec, J1K 2R1, Canada

    Li Zhang, Ming Ni & Bill Shipley

  3. School of Resources and Environment, Anhui Agricultural University, 130 Changjiang West Road, Hefei, 230036, People’s Republic of China

    Li Zhang

  4. Karst Dynamics Laboratory, MLR & Guangxi, Institute of Karst Geology, Chinese Academy of Geological Sciences, Guilin, 541004, People’s Republic of China

    Tongbin Zhu

  5. Key Laboratory of Ecosystem Network Observation and Modeling, Institute of Geographic Sciences and Natural Resources, Chinese Academy of Sciences, 11A Datun Road, Chaoyang District, Beijing, 100101, People’s Republic of China

    Xingliang Xu

  6. CAS Center for Excellence in Tibetan Plateau Earth Sciences, Chinese Academy of Sciences (CAS), Beijing, 100101, People’s Republic of China

    Xingliang Xu

  7. Key Laboratory of Genetics and Germplasm Innovation of Tropical Special Forest Trees and Ornamental Plants, Ministry of Education, College of Forestry, Hainan University, Haikou, 570228, People’s Republic of China

    Shurong Zhou

Authors
  1. Li Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ming Ni
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Tongbin Zhu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Xingliang Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Shurong Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Bill Shipley
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Shurong Zhou.

Additional information

Authors’ contributions

SZ and LZ designed the experiment. LZ, TBZ conducted experiments and collected data. LZ, SZ, BS, MN and LX developed the hypothesis. LZ and BS analyzed the data. LZ, SZ and BS wrote the manuscript. All authors approved the final manuscript.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 326 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhang, L., Ni, M., Zhu, T. et al. Nitrogen Addition in a Tibetan Alpine Meadow Increases Intraspecific Variability in Nitrogen Uptake, Leading to Increased Community-level Nitrogen Uptake. Ecosystems 25, 172–183 (2022). https://doi.org/10.1007/s10021-021-00647-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10021-021-00647-3

Keywords

Search

Navigation