Skip to main content
Log in

Nitrogen deposition promotes phosphorus uptake of plants in a semi-arid temperate grassland

  • Regular Article
  • Published:
Plant and Soil Aims and scope Submit manuscript

A Commentary to this article was published on 30 September 2016

Abstract

Background and aims

Nitrogen (N) deposition greatly influences ecosystem processes through the alteration of plant nutrition; however, there is limited understanding about the effects of phosphorus (P) inputs, especially within the backdrop of N deposition.

Methods

Here we investigated the plant stoichiometric responses to P addition under both ambient conditions and with N addition in a temperate grassland in Inner Mongolia over a two-year period.

Results

The effects of P addition on foliar nutrition and stoichiometric ratios were highly dependent on the presence of N supply, in that P addition showed no significant impacts on foliar N or P concentrations (or pools in community biomass) or N:P under ambient N conditions, but enhanced foliar N in dominant species and foliar P in almost all species (and pools in community biomass) with N addition. These results may be explained by P addition significantly changing the soil properties (soil pH and available P) when applied in combination with N additions. Moreover, there was no biomass response to nutrient additions.

Conclusions

Our results suggest that N deposition may enhance the absorption of additional P by plants in semi-arid grasslands, and that P limitation with increased N deposition might be less important for limiting plant growth than previously anticipated.

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

Access this article

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

Instant access to the full article PDF.

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

Similar content being viewed by others

References

  • 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. doi:10.1111/j.1365-2486.2009.01950.x

    Article  Google Scholar 

  • Bennett EM, Carpenter SR, Caraco NF (2001) Human impact on erodable phosphorus and eutrophication: a global perspective. Bioscience 51:227–234. doi:10.1641/0006-3568(2001)051[0227:Hioepa]2.0.Co;2

    Article  Google Scholar 

  • Bobbink R, Hornung M, Roelofs JGM (1998) The effects of air-borne nitrogen pollutants on species diversity in natural and semi-natural European vegetation. J Ecol 86:717–738. doi:10.1046/j.1365-2745.1998.8650717.x

    Article  CAS  Google Scholar 

  • Bragazza L, Tahvanainen T, Kutnar L, Rydin H, Limpens J, Hájek M, Grosvernier P, Hájek T, Hajkova P, Hansen I, Iacumin P, Gerdol R (2004) Nutritional constraints in ombrotrophic Sphagnum plants under increasing atmospheric nitrogen deposition in Europe. New Phytol 163:609–616. doi:10.1111/j.1469-8137.2004.01154.x

    Article  Google Scholar 

  • Ceulemans T, Merckx R, Hens M, Honnay O (2013) Plant species loss from European semi-natural grasslands following nutrient enrichment - is it nitrogen or is it phosphorus? Glob Ecol Biogeogr 22:73–82. doi:10.1111/j.1466-8238.2012.00771.x

    Article  Google Scholar 

  • Clark CM, Tilman D (2008) Loss of plant species after chronic low-level nitrogen deposition to prairie grasslands. Nature 451:712–715. doi:10.1038/nature06503

    Article  CAS  PubMed  Google Scholar 

  • Du YH, Guo P, Liu JQ, Wang CY, Yang N, Jiao ZX (2014) Different types of nitrogen deposition show variable effects on the soil carbon cycle process of temperate forests. Glob Chang Biol 20:3222–3228. doi:10.1111/gcb.12555

    Article  PubMed  Google Scholar 

  • Elser J, Bennett E (2011) Phosphorus cycle: a broken biogeochemical cycle. Nature 478:29–31. doi:10.1038/478029a

    Article  CAS  PubMed  Google Scholar 

  • 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. doi:10.1111/j.1461-0248.2007.01113.x

    Article  PubMed  Google Scholar 

  • Fan JW, Wang K, Harris W, Zhong HP, Hu ZM, Han B, Zhang WY, Wang JB (2009) Allocation of vegetation biomass across a climate-related gradient in the grasslands of Inner Mongolia. J Arid Environ 73:521–528. doi:10.1016/j.jaridenv.2008.12.004

    Article  Google Scholar 

  • 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. doi:10.1038/nplants.2015.80

    Article  CAS  PubMed  Google Scholar 

  • Galloway JN, Dentener FJ, Capone DG, Boyer EW, Howarth RW, Seitzinger SP, Asner GP, Cleveland CC, Green PA, Holland EA, Karl DM, Michaels AF, Porter JH, Townsend AR, Vöosmarty CJ (2004) Nitrogen cycles: past, present, and future. Biogeochemistry 70:153–226. doi:10.1007/s10533-004-0370-0

    Article  CAS  Google Scholar 

  • Geng Y, Wu Y, He JS (2011) Relationship between leaf phosphorus concentration and soil phosphorus availability across Inner Mongolia grassland. Acta Phytoecol Sin 35:1–8. doi:10.3724/SP.J.1258.2011.00001

    Google Scholar 

  • Gong P, Wang J, Yu L, Zhao YC, Zhao YY, Liang L, Niu ZG, Huang XM, Fu HH, Liu S, Li CC, Li XY, Fu W, Liu CX, Xu Y, Wang XY, Cheng Q, Hu LY, Yao WB, Zhang H, Zhu P, Zhao ZY, Zhang HY, Zheng YM, Ji LY, Zhang YW, Chen H, Yan A, Guo JH, Yu L, Wang L, Liu XJ, Shi TT, Zhu MH, Chen YL, Yang GW, Tang P, Xu B, Giri C, Clinton N, Zhu ZL, Chen J, Chen J (2013) Finer resolution observation and monitoring of global land cover: first mapping results with Landsat TM and ETM+ data. Int J Remote Sens 34:2607–2654. doi:10.1080/01431161.2012.748992

    Article  Google Scholar 

  • Güsewell S (2004) N: P ratios in terrestrial plants: variation and functional significance. New Phytol 164:243–266. doi:10.1111/j.1469-8137.2004.01192.x

    Article  Google Scholar 

  • Han X, Sistla SA, Zhang YH, Lü XT, Han XG (2014) Hierarchical responses of plant stoichiometry to nitrogen deposition and mowing in a temperate steppe. Plant Soil 382:175–187. doi:10.1007/s11104-014-2154-1

    Article  CAS  Google Scholar 

  • 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. doi:10.1111/j.1461-0248.2011.01651.x

    Article  PubMed  Google Scholar 

  • He NP, Yu Q, Wang RM, Zhang YH, Gao Y, Yu GR (2013) Enhancement of carbon sequestration in soil in the temperature grasslands of northern China by addition of nitrogen and phosphorus. PLoS One 8:e77241. doi:10.1371/journal.pone.0077241

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Horswill P, O’Sullivan O, Phoenix GK, Lee JA, Leake JR (2008) Base cation depletion, eutrophication and acidification of species-rich grasslands in response to long-term simulated nitrogen deposition. Environ Pollut 155:336–349. doi:10.1016/j.envpol.2007.11.006

    Article  CAS  PubMed  Google Scholar 

  • ISSS Working Group RB (1998) World reference base for soil resources. Atlas. EM Bridges et al. (eds) 1st ed. ISSS/ISRIC/FAO. Acco, Leuven, Belgium

  • Johnson D, Leake JR, Lee JA (1999) The effects of quantity and duration of simulated pollutant nitrogen deposition on root-surface phosphatase activities in calcareous and acid grasslands: a bioassay approach. New Phytol 141:433–442. doi:10.1046/j.1469-8137.1999.00360.x

    Article  CAS  Google Scholar 

  • Lannes LS, Bustamante MMC, Edwards PJ, Olde Venterink H (2016) Native and alien herbaceous plants in the Brazilian Cerrado are (co-)limited by different nutrients. Plant Soil 400:231–243. doi:10.1007/s11104-015-2725-9

    Article  CAS  Google Scholar 

  • Li LJ, Zeng DH, Mao R, Yu ZY (2012) Nitrogen and phosphorus resorption of Artemisia scoparia, Chenopodium acuminatum, Cannabis sativa, and Phragmites communis under nitrogen and phosphorus additions in a semiarid grassland, China. Plant Soil Environ 58:446–451

    CAS  Google Scholar 

  • Li Y, Niu SL, Yu GR (2016) Aggravated phosphorus limitation on biomass production under increasing nitrogen loading: a meta-analysis. Glob Chang Biol 22:934–943. doi:10.1111/gcb.13125

    Article  PubMed  Google Scholar 

  • 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. doi:10.1038/nature11917

    Article  CAS  PubMed  Google Scholar 

  • Lü XT, Kong DL, Pan QM, Simmons ME, Han XG (2012) Nitrogen and water availability interact to affect leaf stoichiometry in a semi-arid grassland. Oecologia 168:301–310. doi:10.1007/s00442-011-2097-7

    Article  PubMed  Google Scholar 

  • Lü XT, Reed S, Yu Q, He NP, Wang ZW, Han XG (2013) Convergent responses of nitrogen and phosphorus resorption to nitrogen inputs in a semiarid grassland. Glob Chang Biol 19:2775–2784. doi:10.1111/gcb.12235

    Article  PubMed  Google Scholar 

  • Niklas KJ, Owens T, Reich PB, Cobb ED (2005) Nitrogen/phosphorus leaf stoichiometry and the scaling of plant growth. Ecol Lett 8:636–642. doi:10.1111/j.1461-0248.2005.00759.x

    Article  Google Scholar 

  • Niu SL, Wu MY, Han Y, Xia JY, Zhang Z, Yang HJ, Wan SQ (2010) Nitrogen effects on net ecosystem carbon exchange in a temperate steppe. Glob Chang Biol 16:144–155. doi:10.1111/j.1365-2486.2009.01894.x

    Article  Google Scholar 

  • Office IMSC, Service IMSaF (1994) The soils of Inner Mongolia. Science Press, Beijing

    Google Scholar 

  • Olde Venterink H (2011) Legumes have a higher root phosphatase activity than other forbs, particularly under low inorganic P and N supply. Plant Soil 347:137–146. doi:10.1007/s11104-011-0834-7

    Article  CAS  Google Scholar 

  • Olde Venterink H, Van der Vliet RE, Wassen MJ (2001) Nutrient limitation along a productivity gradient in wet meadows. Plant Soil 234:171–179

    Article  CAS  Google Scholar 

  • Ordoñez JC, van Bodegom PM, Witte JPM, Wright IJ, Reich PB, Aerts R (2009) A global study of relationships between leaf traits, climate and soil measures of nutrient fertility. Glob Ecol Biogeogr 18:137–149. doi:10.1111/j.1466-8238.2008.00441.x

    Article  Google Scholar 

  • Pardo LH, McNulty SG, Boggs JL, Duke S (2007) Regional patterns in foliar N-15 across a gradient of nitrogen deposition in the northeastern US. Environ Pollut 149:293–302. doi:10.1016/j.envpol.2007.05.030

    Article  CAS  PubMed  Google Scholar 

  • Peñuelas J, Poulter B, Sardans J, Ciais P, van der Velde M, Bopp L, Boucher O, Godderis Y, Hinsinger P, Llusia J, Nardin E, Vicca S, Obersteiner M, Janssens IA (2013) Human-induced nitrogen-phosphorus imbalances alter natural and managed ecosystems across the globe. Nat Commun 4:2934. doi:10.1038/ncomms3934

    PubMed  Google Scholar 

  • Phoenix GK, Emmett BA, Britton AJ, Caporn SJM, Dise NB, Helliwell R, Jones L, Leake JR, Leith ID, Sheppard LJ, Sowerby A, Pilkington MG, Rowe EC, Ashmorek MR, Power SA (2012) Impacts of atmospheric nitrogen deposition: responses of multiple plant and soil parameters across contrasting ecosystems in long-term field experiments. Glob Chang Biol 18:1197–1215. doi:10.1111/j.1365-2486.2011.02590.x

    Article  Google Scholar 

  • Prietzel J, Stetter U (2010) Long-term trends of phosphorus nutrition and topsoil phosphorus stocks in unfertilized and fertilized Scots pine (Pinus sylvestris) stands at two sites in Southern Germany. For Ecol Manag 259:1141–1150. doi:10.1016/j.foreco.2009.12.030

    Article  Google Scholar 

  • Prietzel J, Rehfuess KE, Stetter U, Pretzsch H (2008) Changes of soil chemistry, stand nutrition, and stand growth at two Scots pine (Pinus sylvestris L.) sites in Central Europe during 40 years after fertilization, liming, and lupine introduction. Eur J For Res 127:43–61. doi:10.1007/s10342-007-0181-7

  • R Core Team (2014) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/

  • Rowe EC, Smart SM, Kennedy VH, Emmett BA, Evans CD (2008) Nitrogen deposition increases the acquisition of phosphorus and potassium by heather Calluna vulgaris. Environ Pollut 155:201–207. doi:10.1016/j.envpol.2007.12.008

    Article  CAS  PubMed  Google Scholar 

  • Sardans J, Peñuelas J (2012) The role of plants in the effects of global change on nutrient availability and stoichiometry in the plant-soil system. Plant Physiol 160:1741–1761. doi:10.1104/pp.112.208785

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sinsabaugh RL, Lauber CL, Weintraub MN, Ahmed B, Allison SD, Crenshaw C, Contosta AR, Cusack D, Frey S, Gallo ME, Gartner TB, Hobbie SE, Holland K, Keeler BL, Powers JS, Stursova M, Takacs-Vesbach C, Waldrop MP, Wallenstein MD, Zak DR, Zeglin LH (2008) Stoichiometry of soil enzyme activity at global scale. Ecol Lett 11:1252–1264. doi:10.1111/j.1461-0248.2008.01245.x

    PubMed  Google Scholar 

  • Sparks DL (1996) Methods of soil analysis. Part 3, Chemical methods. SSSA and ASA, Madison

    Google Scholar 

  • Stevens CJ, Duprè C, Dorland E, Gaudnik C, Gowing DJG, Bleeker A, Diekmann M, Alard D, Bobbink R, Fowler D, Corcket E, Mountford JO, Vandvik V, Aarrestad PA, Muller S, Dise NB (2011) The impact of nitrogen deposition on acid grasslands in the Atlantic region of Europe. Environ Pollut 159:2243–2250. doi:10.1016/j.envpol.2010.11.026

    Article  CAS  PubMed  Google Scholar 

  • Tian DH, Wang H, Sun J, Niu SL (2016) Global evidence on nitrogen saturation of terrestrial ecosystem net primary productivity. Environ Res Lett 11:024012. doi:10.1088/1748-9326/11/2/024012

  • Vitousek PM, Porder S, Houlton BZ, Chadwick OA (2010) Terrestrial phosphorus limitation: mechanisms, implications, and nitrogen-phosphorus interactions. Ecol Appl 20:5–15. doi:10.1890/08-0127.1

    Article  PubMed  Google Scholar 

  • Yesmin L, Gammack SM, Cresser MS (1996) Changes in N concentrations of peat and its associated vegetation over 12 months in response to increased deposition of ammonium sulfate or nitric acid. Sci Total Environ 177:281–290. doi:10.1016/0048-9697(95)04926-6

  • Yu Q, Chen QS, Elser JJ, He NP, Wu HH, Zhang GM, Wu JG, Bai YF, Han XG (2010) Linking stoichiometric homoeostasis with ecosystem structure, functioning and stability. Ecol Lett 13:1390–1399. doi:10.1111/j.1461-0248.2010.01532.x

    Article  PubMed  Google Scholar 

  • Yu Q, Elser JJ, He NP, Wu HH, Chen QS, Zhang GM, Han XG (2011) Stoichiometric homeostasis of vascular plants in the Inner Mongolia grassland. Oecologia 166:1–10. doi:10.1007/s00442-010-1902-z

    Article  PubMed  Google Scholar 

  • Yu Q, Wilcox K, Pierre KL, Knapp AK, Han X, Smith MD (2015) Stoichiometric homeostasis predicts plant species dominance, temporal stability, and responses to global change. Ecology 96:2328–2335. doi:10.1890/14-1897.1

    Article  PubMed  Google Scholar 

  • Zhalnina K, Dias R, De Quadros PD, Davis-Richardson A, Camargo FAO, Clark IM, McGrath SP, Hirsch PR, Triplett EW (2015) Soil pH determines microbial diversity and composition in the park grass experiment. Microb Ecol 69:395–406. doi:10.1007/s00248-014-0530-2

    Article  CAS  PubMed  Google Scholar 

  • Zhang LX (2003) Plant N:P stoichiometry: variations of Chinese higher plants and a preliminary test by field experimentation. Dissertation, Institute of Botany, Chinese Academy of Sciences

  • Zhang GN, Chen ZH, Zhang AM, Chen LJ, Wu ZJ (2013) Effects of nitrogen deposition on typical hydrolytic enzyme activities by fluorimetric assay. Asian J Chem 25:10335–10338. doi:10.14233/ajchem.2013.15384

    CAS  Google Scholar 

  • Zhang YH, Han X, He NP, Long M, Huang JH, Zhang GM, Wang QB, Han XG (2014) Increase in ammonia volatilization from soil in response to N deposition in Inner Mongolia grasslands. Atmos Environ 84:156–162. doi:10.1016/j.atmosenv.2013.11.052

    Article  Google Scholar 

Download references

Acknowledgments

We gratefully appreciate the Inner Mongolia Grassland Ecosystem Research Station (IMGERS) for providing the experimental sites and elemental analysis. This research was supported by National Natural Science Foundation of China (31270476, 41320104002, 41203052), Strategic Priority Research Program of the Chinese Academy of Sciences (XDB15010403).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Qiang Yu.

Additional information

Responsible Editor: Harry Olde Venterink.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Long, M., Wu, HH., Smith, M.D. et al. Nitrogen deposition promotes phosphorus uptake of plants in a semi-arid temperate grassland. Plant Soil 408, 475–484 (2016). https://doi.org/10.1007/s11104-016-3022-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-016-3022-y

Keywords

Navigation