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Testing nitrogen and water co-limitation of primary productivity in a temperate steppe


Background and aims

Primary productivity in the temperate steppe is assumed to be co-limited by nitrogen (N) and water availability, but empirical evidence is scarce. We examined the N and water limitation status of primary productivity from the species scale to community scale under the framework of resource co-limitation.


We compared the responses of aboveground net primary productivity (ANPP) at different ecological levels to factorial N and water addition in two years in a temperate steppe of northern China.


Water addition significantly enhanced total ANPP by 46%, with stronger effects in the dry year. Total ANPP was sub-additively co-limited by N and water availability, being more sensitive to water addition than to N addition in the dry year and equally sensitive to both resources in the year with normal precipitation. The responses of total ANPP to resource additions were largely driven by the changes of grasses rather than the forbs. Species level ANPP showed conservative responses to resource additions.


Our results highlight the hierarchical patterns of limitation status in primary productivity at different biological organization levels in this temperate steppe. The sub-additive limitation by N and water in this ecosystem deserves more attention in modelling the dynamics of ecosystem carbon cycle under global change scenarios.

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  1. Bai YF, Wu JG, Xing Q, Pan QM, Huang JH, Yang DL, Han XG (2008) Primary production and rain use efficiency across a precipitation gradient on the Mongolia plateau. Ecology 89:2140–2153

    Article  Google Scholar 

  2. Bai YF, Wu JG, Clark CM, Naeem S, Pan QM, Huang JH, Zhang LX, Han XG (2010) Tradeoffs and thresholds in the effects of nitrogen addition on biodiversity and ecosystem functioning: evidence from inner Mongolia grasslands. Glob Chang Biol 16:358–372

    Article  Google Scholar 

  3. Bloom AJ, Chapin FS, Mooney HA (1985) Resource limitation in plants - an economic analogy. Annu Rev Ecol Syst 16:363–392

    Article  Google Scholar 

  4. Burke IC, Lauenroth WK, Parton WJ (1997) Regional and temporal variation in net primary production and nitrogen mineralization in grasslands. Ecology 78:1330–1340

    Article  Google Scholar 

  5. Craine JM (2009) Resource strategies of wild plants Princeton University press, Princeton, NJ. In: USA

    Google Scholar 

  6. DeMalach N, Zaady E, Kadmon R (2017) Contrasting effects of water and nutrient additions on grassland communities: a global meta-analysis. Glob Ecol Biogeogr 26:983–996

    Article  Google Scholar 

  7. Elser JJ, Bracken MES, Cleland EE, Gruner DS, Harpole WS, Hillebrand H, Ngai JT, Seabloom EW, Shurin JB, Smith JE (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 

  8. Fay PA, Prober SM, Harpole WS, Knops JMH, Bakker JD, Borer ET, Lind EM, MacDougall AS, Seabloom EW, Wragg PD, Adler PB, Blumenthal DM, Buckley Y, Chu CJ, Cleland EE, Collins SL, Davies KF, Du GZ, Feng XH, Firn J, Gruner DS, Hagenah N, Hautier Y, Heckman RW, Jin VL, Kirkman KP, Klein J, Ladwig LM, Li Q, McCulley RL, Melbourne BA, Mitchell CE, Moore JL, Morgan JW, Risch AC, Schutz M, Stevens CJ, Wedin DA, Yang LH (2015) Grassland productivity limited by multiple nutrients. Nat Plants 1:15080

    CAS  Article  Google Scholar 

  9. Galloway JN, Townsend AR, Erisman JW, Bekunda M, Cai ZC, Freney JR, Martinelli LA, Seitzinger SP, Sutton MA (2008) Transformation of the nitrogen cycle: recent trends, questions, and potential solutions. Science 320:889–892

    CAS  Article  Google Scholar 

  10. Gao YZ, Chen Q, Lin S, Giese M, Brueck H (2011) Resource manipulation effects on net primary production, biomass allocation and rain-use efficiency of two semiarid grassland sites in Inner Mongolia, China. Oecologia 165:855–864

    Article  Google Scholar 

  11. Grime JP (1998) Benefits of plant diversity to ecosystems: immediate, filter and founder effects. J Ecol 86:902–910

    Article  Google Scholar 

  12. Harpole WS, Potts DL, Suding KN (2007) Ecosystem responses to water and nitrogen amendment in a California grassland. Glob Chang Biol 13:2341–2348

    Article  Google Scholar 

  13. Harpole WS, Ngai JT, Cleland EE, Seabloom EW, Borer ET, Bracken MES, Elser JJ, Gruner DS, Hillebrand H, Shurin JB, Smith JE (2011) Nutrient co-limitation of primary producer communities. Ecol Lett 14:852–862

    Article  Google Scholar 

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

    CAS  Article  Google Scholar 

  15. Heisler-White JL, Knapp AK, Kelly EF (2008) Increasing precipitation event size increases aboveground net primary productivity in a semi-arid grassland. Oecologia 158:129–140

    Article  Google Scholar 

  16. Hooper DU, Johnson L (1999) Nitrogen limitation in dryland ecosystems: responses to geographical and temporal variation in precipitation. Biogeochemistry 46:247–293

    CAS  Google Scholar 

  17. IPCC (2013) Climate change 2013: the physical science basis. Cambridge University Press, Cambridge, United Kingdom and New York, NY, USA

  18. Kaspari M, Roeder KA, Benson B, Weiser MD, Sanders NJ (2017) Sodium co-limits and catalyzes macronutrients in a prairie food web. Ecology 98:315–320

    Article  Google Scholar 

  19. La Pierre KJ, Blumenthal DM, Brown CS, Klein JA, Smith MD (2016) Drivers of variation in ANPP and plant community composition differ across a broad precipitation gradient. Ecosystems 19:521–533

    Article  Google Scholar 

  20. LeBauer DS, Treseder KK (2008) Nitrogen limitation of net primary productivity in terrestrial ecosystems is globally distributed. Ecology 89:371–379

    Article  Google Scholar 

  21. Liu XJ, Zhang Y, Han WX, Tang AH, Shen JL, Cui ZL, Vitousek P, Erisman JW, Goulding K, Christie P, Fangmeier A, Zhang FS (2013) Enhanced nitrogen deposition over China. Nature 494:459–462

    CAS  Article  Google Scholar 

  22. Lü XT, Dijksta FA, Kong DL, Wang ZW, Han XG (2014) Plant nitrogen uptake drives responses of productivity to nitrogen and water addition in a grassland. Sci Rep 4:4817

    Article  Google Scholar 

  23. Poulter B, Frank D, Ciais P, Myneni RB, Andela N, Bi J, Broquet G, Canadell JG, Chevallier F, Liu YY, Running SW, Sitch S, van der Werf GR (2014) Contribution of semi-arid ecosystems to interannual variability of the global carbon cycle. Nature 509:600–603

    CAS  Article  Google Scholar 

  24. R Core Team (2015) R: a language and environment for Statitical computing. R Fundation for Statistical Computing, Vienna, Austria Retrieved from

    Google Scholar 

  25. Ren HY, Xu ZW, Isbell F, Huang JH, Han XG, Wan SQ, Chen SP, Wang RZ, Zeng DH, Jiang Y, Fang YT (2017) Exacerbated nitrogen limitation ends transient stimulation of grassland productivity by increased precipitation. Ecol Monogr 87:457–469

    Article  Google Scholar 

  26. Sperfeld E, Raubenheimer D, Wacker A (2016) Bridging factorial and gradient concepts of resource co-limitation: towards a general framework applied to consumers. Ecol Lett 19:201–215

    Article  Google Scholar 

  27. St Clair SB, Sudderth EA, Castanha C, Torn MS, Ackerly DD (2009) Plant responsiveness to variation in precipitation and nitrogen is consistent across he compositional diversity of a California annual grassland. J Veg Sci 20:860–870

    Article  Google Scholar 

  28. Sun Y, Ding YH (2010) A projection of future changes in summer precipitation and monsoon in East Asia. Sci China Earth Sci 53:284–300

    CAS  Article  Google Scholar 

  29. Wang CH, Wan SQ, Xing XR, Zhang L, Han XG (2006) Temperature and soil moisture interactively affected soil net N mineralization in temperate grassland in northern China. Soil Biol Biochem 38:1101–1110

    CAS  Article  Google Scholar 

  30. Wilcox KR, Blair JM, Smith MD, Knapp AK (2016) Does ecosystem sensitivity to precipitation at the site-level conform to regional-scale predictions? Ecology 97:561–568

    PubMed  Google Scholar 

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We thank the staff of the Inner Mongolia Grassland Ecosystem Research Station (IMGERS) for supporting this study and Amber C. Churchill and Matthew Simmons for linguistic improvement. Comments and suggestions from Dr. Thomas W. Kuyper and three anonymous reviewers help improve the quality of this manuscript. This work was supported by the National Natural Science Foundation of China (31470505 and 31770503), National Basic Research Program of China (2016YFC0500601 and 2015CB150802), Strategic Priority Research Program of the Chinese Academy of Sciences (XDB15010403), Youth Innovation Promotion Association CAS (2014174), and the Key Research Program from CAS (QYZDB-SSWDQC006).

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Correspondence to Xiao-Tao Lü.

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Responsible Editor: Thom W. Kuyper

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Lü, XT., Liu, ZY., Hu, YY. et al. Testing nitrogen and water co-limitation of primary productivity in a temperate steppe. Plant Soil 432, 119–127 (2018).

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  • Co-limitation
  • Drought
  • Drylands
  • Multiple resource limitation
  • Plant functional group
  • Precipitation
  • Primary production