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Interactive effects of nitrogen and phosphorus additions on plant growth vary with ecosystem type

  • Jun Jiang
  • Ying-Ping Wang
  • Yanhua Yang
  • Mengxiao Yu
  • Chen Wang
  • Junhua YanEmail author
Regular Article

Abstract

Aims

Co-limitation of ecosystem productivity by nitrogen (N) and phosphorus (P) is gaining increasing recognition, but how co-limitation through N and P interactions differs among different terrestrial ecosystems remains unclear.

Methods

We performed a meta-analysis of 133 independent studies conducted in four natural terrestrial ecosystems to examine the interactive effects of N and P additions on ten plant growth-related variables.

Results

Adding N and P individually or in combination significantly increased aboveground biomass (AGB), and the interactions were uniformly synergistic for AGB, and additive for belowground biomass (BGB), but variable for other eight growth-related variables among four different ecosystems. The interaction was synergistic for leaf P and soil NO3-N only in tropical forests, and antagonistic for soil available P (AP) in tropical forests, leaf N in grasslands, root P in wetlands, and leaf P and soil NH4-N in tundra. The interaction for leaf N: P ratios was additive only in tropical forests, and synergistic in the other three ecosystems.

Conclusions

Our results highlighted the interactions of N and P additions can promote uptake of both nutrients by plants, and plants tend to maintain the optimal nutrient balance for growth and reproduction through regulating biomass production and tissue nutrient concentrations.

Keywords

Interactions Meta-analysis Nutrient limitation Plant growth Terrestrial ecosystems 

Notes

Acknowledgements

We are grateful to all the researchers for their data used in this meta-analysis. Thanks are due to the subject editor and three anonymous reviewers for their constructive suggestions on improving the manuscript. This study was financially supported by the National Science Fund for Distinguished Young Scholars (41825020).

Author’s contributions

J J, Y-P W and J Y designed the research; J J, Y Y and M Y collected the data; J J and C W performed the analysis; J J, Y Y and Y-P W wrote the manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that no conflict of interest exits in the submission of this manuscript, and the manuscript is approved by all authors for publication.

Supplementary material

11104_2019_4119_MOESM1_ESM.docx (306 kb)
ESM 1 (DOCX 306 kb)

References

  1. Aerts R, Chapin FS III (2000) The mineral nutrition of wild plants revisited: a re-evaluation of processes and patterns. Adv Ecol Res 30:1–67Google Scholar
  2. Agren GI, Wetterstedt JA, Billberger MF (2012) Nutrient limitation on terrestrial plant growth--modeling the interaction between nitrogen and phosphorus. New Phytol 194:953–960CrossRefGoogle Scholar
  3. Allgeier JE, Rosemond AD, Layman CA (2011) The frequency and magnitude of non-additive responses to multiple nutrient enrichment. J Appl Ecol 48:96–101CrossRefGoogle Scholar
  4. Allison SD, Weintraub MN, Gartner TB, Waldrop MP (2011) Evolutionary-economic principles as regulators of soil enzyme production and ecosystem function. In: Soil enzymology, vol 22. Springer, Berlin Heidelberg, pp 229–243CrossRefGoogle Scholar
  5. Arrigo KR (2005) Marine microorganisms and global nutrient cycles. Nature 437:349–355CrossRefGoogle Scholar
  6. Avolio ML, Koerner SE, La Pierre KJ, Wilcox KR, Wilson GWT, Smith MD, Collins SL, MacDougall A (2014) Changes in plant community composition, not diversity, during a decade of nitrogen and phosphorus additions drive above-ground productivity in a tallgrass prairie. J Ecol 102:1649–1660CrossRefGoogle Scholar
  7. Bedford BL, Walbridge MR, Aldous A (1999) Patterns in nutrient availability and plant diversity of temperate north American wetlands. Ecology 80:2151–2169CrossRefGoogle Scholar
  8. Borenstein M, Hedges LV, Higgins JPT, Rothstein HR (2009) Introduction to meta-analysis. John Wiley and Sons Ltd, ChichesterCrossRefGoogle Scholar
  9. Boyer KE, Fong P, Vance RR, Ambrose RF (2001) Salicornia virginica in a southern California salt marsh: seasonal patterns and a nutrient-enrichment experiment. Wetlands 21:315–326CrossRefGoogle Scholar
  10. Bret-Harte MS, Mack MC, Goldsmith GR, Sloan DB, DeMarco J, Shaver GR, Ray PM, Biesinger Z, Chapin FS III (2008) Plant functional types do not predict biomass responses to removal and fertilization in Alaskan tussock tundra. J Ecol 96:713–726CrossRefGoogle Scholar
  11. Bridgham SD, Updegraff K, Pastor J (1998) Carbon, nitrogen, and phosphorus mineralization in northern wetlands. Ecology 79(5):1545–1561CrossRefGoogle Scholar
  12. Cleland EE (2007) Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine and terrestrial ecosystems. Ecol Lett 10:1135–1142CrossRefGoogle Scholar
  13. Cleveland CC, Townsend AR, Taylor P, Alvarez-Clare S, Bustamante MMC, Chuyong G, Dobrowski SZ, Grierson P, Harms KE, Houlton BZ (2011) Relationships among net primary productivity, nutrients and climate in tropical rain forest: a pan-tropical analysis. Ecol Lett 14:939–947CrossRefGoogle Scholar
  14. Crain CM, Kroeker K, Halpern BS (2008) Interactive and cumulative effects of multiple human stressors in marine systems. Ecol Lett 11:1304–1315CrossRefGoogle Scholar
  15. Darby FA, Turner RE (2008) Below-and aboveground biomass of Spartina alterniflora : response to nutrient addition in a Louisiana salt marsh. Estuar Coasts 31:326–334CrossRefGoogle Scholar
  16. Deng Q, Hui D, Dennis S, Reddy KC (2017) Responses of terrestrial ecosystem phosphorus cycling to nitrogen addition: a meta-analysis. Glob Ecol Biogeogr 26:713–728CrossRefGoogle Scholar
  17. Egger M, Smith GD (1998) Meta-analysis: Bias in location and selection of studies. Brit Med J 316:61–66CrossRefGoogle Scholar
  18. Elser JJ, Bracken ME, 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 10:1135–1142CrossRefGoogle Scholar
  19. Elser JJ, Fagan WF, Kerkhoff AJ, Swenson NG, Enquist BJ (2010) Biological stoichiometry of plant production: metabolism, scaling and ecological response to global change. New Phytol 186:593–608CrossRefGoogle Scholar
  20. Fay PA, Prober SM, Harpole WS, Knops JM, Bakker JD, Borer ET, Lind EM, MacDougall AS, Seabloom EW, Wragg PD, Adler PB, Blumenthal DM, Buckley YM, Chu C, Cleland EE, Collins SL, Davies KF, Du G, Feng X, 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 1:15080CrossRefGoogle Scholar
  21. Ford H, Roberts A, Jones L (2016) Nitrogen and phosphorus co-limitation and grazing moderate nitrogen impacts on plant growth and nutrient cycling in sand dune grassland. Sci Total Environ 542:203–209CrossRefGoogle Scholar
  22. Giesler R, Graae BJ (2012) Phosphorus availability and microbial respiration across different tundra vegetation types. Biogeochemistry 108:429–445CrossRefGoogle Scholar
  23. Gress SE, Nichols TD, Northcraft CC, Peterjohn WT (2007) Nutrient limitation in soils exhibiting differing nitrogen availabilities: what lies beyond nitrogen saturation? Ecology 88:119–130CrossRefGoogle Scholar
  24. Gurevitch J, Hedges LV (1999) Statistical issues in ecological meta-analyses. Ecology 80:1142–1149CrossRefGoogle Scholar
  25. Güsewell S (2004) N: P ratios in terrestrial plants: variation and functional significance. New Phytol 164:243–266CrossRefGoogle Scholar
  26. Güsewell S, Koerselman W, Verhoeven JTA (2002) Time-dependent effects of fertilization in Dutch floating fens. J Veg Sci 13:705–718CrossRefGoogle Scholar
  27. Harpole WS, Ngai JT, Cleland EE, Seabloom EW, Borer ET, Bracken ME, Elser JJ, Gruner DS, Hillebrand H, Shurin JB, Smith JE (2011) Nutrient co-limitation of primary producer communities. Ecol Lett 14:852–862CrossRefGoogle Scholar
  28. Hedges LV, Gurevitch J, Curtis PS (1999) The meta-analysis of response ratios in experimental ecology. Ecology 80:1150–1156CrossRefGoogle Scholar
  29. Hedin LO, Vitousek PM, Matson PA (2003) Pathways and implications of nutrient losses during four million years of tropical forest ecosystem development. Ecology 84:2231–2255CrossRefGoogle Scholar
  30. Hooper DU, Johnson L (1999) Nitrogen limitation in dryland ecosystems: responses to geographical and temporal variation in precipitation. Biogeochemistry 46:247–293Google Scholar
  31. Houlton BZ, Wang YP, Vitousek PM, Field CB (2008) A unifying framework for dinitrogen fixation in the terrestrial biosphere. Nature 454:327–330CrossRefGoogle Scholar
  32. Huang W, Liu J, Wang YP, Zhou G, Han T, Li Y (2013) Increasing phosphorus limitation along three successional forests in southern China. Plant Soil 364:181–191CrossRefGoogle Scholar
  33. Huang W, Houlton BZ, Marklein AR, Liu J, Zhou G (2015) Plant stoichiometric responses to elevated CO2 vary with nitrogen and phosphorus inputs: evidence from a global-scale meta-analysis. Sci Rep 5Google Scholar
  34. Lamarque JF, Dentener F, McConnell J, Ro CU, Shaw M, Vet R, Bergmann D, Cameron-Smith P, Dalsoren S, Doherty R, Faluvegi G, Ghan SJ, Josse B, Lee YH, MacKenzie IA, Plummer D, Shindell DT, Skeie RB, Stevenson DS, Strode S, Zeng G, Curran M, Dahl-Jensen D, Das S, Fritzsche D, Nolan M (2013) Multi-model mean nitrogen and sulfur deposition from the atmospheric chemistry and climate model Intercomparison project (ACCMIP): evaluation of historical and projected future changes. Atmos Chem Phys 13:7997–8018CrossRefGoogle Scholar
  35. Lebauer DS, Treseder KK (2008) Nitrogen limitation of net primary productivity in terrestrial ecosystems is globally distributed. Ecology 89:371–379CrossRefGoogle Scholar
  36. Li Y, Niu S, Yu G (2016) Aggravated phosphorus limitation on biomass production under increasing nitrogen loading: a meta-analysis. Glob Chang Biol 22:934–943CrossRefGoogle Scholar
  37. Liu J, Huang W, Zhou G, Zhang D, Liu S, Li Y (2013) Nitrogen to phosphorus ratios of tree species in response to elevated carbon dioxide and nitrogen addition in subtropical forests. Glob Chang Biol 19:208–216CrossRefGoogle Scholar
  38. Luo Y, Hui D, Zhang D (2006) Elevated CO2 stimulates net accumulations of carbon and nitrogen in land ecosystems: a meta-analysis. Ecology 87:53–63CrossRefGoogle Scholar
  39. Marklein AR, Houlton BZ (2012) Nitrogen inputs accelerate phosphorus cycling rates across a wide variety of terrestrial ecosystems. New Phytol 193:696–704CrossRefGoogle Scholar
  40. Merianskouw H, Anders M (2011) Long-term addition of fertilizer, labile carbon, and fungicide alters the biomass of plant functional groups in a subarctic-alpine community. Plant Ecol 212:715–726CrossRefGoogle Scholar
  41. Mori T, Ohta S, Ishizuka S, Konda R, Wicaksono A, Heriyanto J, Hamotani Y, Gobara Y, Kawabata C, Kuwashima K (2013) Soil greenhouse gas fluxes and C stocks as affected by phosphorus addition in a newly established Acacia mangium plantation in Indonesia. Forest Ecol Manag 310:643–651CrossRefGoogle Scholar
  42. Mori T, Ohta S, Ishizuka S, Konda R, Wicaksono A, Heriyanto J (2014) Phosphorus application reduces N2O emissions from tropical leguminous plantation soil when phosphorus uptake is occurring. Biol Fertil Soils 50:45–51CrossRefGoogle Scholar
  43. Niklas KJ, Owens T, Reich PB, Cobb ED (2005) Nitrogen / phosphorus leaf stoichiometry and the scaling of plant growth. Ecol Lett 8:636–642CrossRefGoogle Scholar
  44. Olander LP, Vitousek PM (2000) Regulation of soil phosphatase and chitinase activity by N and P availability. Biogeochemistry 49:175–191CrossRefGoogle Scholar
  45. Olander LP, Vitousek PM (2004) Biological and geochemical sinks for phosphorus in soil from a wet tropical Forest. Ecosystems 7:404–419CrossRefGoogle Scholar
  46. Peñuelas J, Sardans J, Rivas-ubach A, Janssens IA (2012) The human-induced imbalance between C, N and P in Earth's life system. Glob Chang Biol 18:3–6CrossRefGoogle Scholar
  47. 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 4:2934CrossRefGoogle Scholar
  48. Phoenix GK, Booth RE, Leake JR, Read DJ, Grime JP, Lee JA (2010) Effects of enhanced nitrogen deposition and phosphorus limitation on nitrogen budgets of semi-natural grasslands. Glob Chang Biol 9:1309–1321CrossRefGoogle Scholar
  49. Reich PB, Oleksyn J (2004) Global patterns of plant leaf N and P in relation to temperature and latitude. P Natl Acad Sci USA 101:11001–11006CrossRefGoogle Scholar
  50. Reich PB, Oleksyn J, Wright IJ, Niklas KJ, Hedin L, Elser JJ (2010) Consistent 2 / 3-power leaf nitrogen to phosphorus scaling among major plant groups and biomes. In: Proceedings of the Royal Society of London. Series B: biological sciences, vol 277, pp 877–883Google Scholar
  51. Rosenberg MS, Adams DC, Gurevitch J (2000) Meta Win: Statistical Software for Meta-Analysis, Version 2. Sinauer Associates, Sunderland, MAGoogle Scholar
  52. Sterner RW, Elser JJ (2002) Ecological stoichiometry: the biology of elements from molecules to the biosphere. Princeton, NJ. Princeton University Press, USAGoogle Scholar
  53. Sun Y, Peng S, Goll DS, Ciais P, Guenet B, Guimberteau M, Hinsinger P, Janssens IA, Penuelas J, Piao S, Poulter B, Violette A, Yang X, Yin Y, Zeng H (2017) Diagnosing phosphorus limitations in natural terrestrial ecosystems in carbon cycle models. Earths Future 5:730–749CrossRefGoogle Scholar
  54. Sundqvist MK, Liu Z, Giesler R, Wardle DA (2014) Plant and microbial responses to nitrogen and phosphorus addition across an elevational gradient in subarctic tundra. Ecology 95:1819–1835CrossRefGoogle Scholar
  55. Treseder KK, Vitousek PM (2001) Effects of soil nutrient availability on investment in acquisition of N and P in Hawaiian rain forests. Ecology 82:946–954CrossRefGoogle Scholar
  56. Turner BL, Wright SJ (2014) The response of microbial biomass and hydrolytic enzymes to a decade of nitrogen, phosphorus, and potassium addition in a lowland tropical rain forest. Biogeochemistry 117:115–130CrossRefGoogle Scholar
  57. Vitousek PM, Porder S, Houlton BZ, Chadwick OA (2010) Terrestrial phosphorus limitation: mechanisms, implications, and nitrogen-phosphorus interactions. Ecol Appl 20:5–15CrossRefGoogle Scholar
  58. Walker TW, Syers JK (1976) The fate of phosphorus during pedogenesis. Geoderma 15:1–19CrossRefGoogle Scholar
  59. Wang YP, Houlton BZ, Field CB (2007) A model of biogeochemical cycles of carbon, nitrogen, and phosphorus including symbiotic nitrogen fixation and phosphatase production. Glob Biogeochem Cy 21:GB1018CrossRefGoogle Scholar
  60. Wang R, Balkanski Y, Boucher O, Ciais P, Peñuelas J, Tao S (2014) Significant contribution of combustion-related emissions to the atmospheric phosphorus budget. Nat Geosci 8:48–54CrossRefGoogle Scholar
  61. Wang YP, Zhang Q, Pitman AJ, Dai Y (2015) Nitrogen and phosphorous limitation reduces the effects of land use change on land carbon uptake or emission. Environ Res Lett 10:014001CrossRefGoogle Scholar
  62. Yuan ZY, Chen HYH (2012) A global analysis of fine root production as affected by soil nitrogen and phosphorus. Proc R Soc B 279:3796–3802CrossRefGoogle Scholar
  63. Yuan ZY, Chen HYH (2015) Decoupling of nitrogen and phosphorus in terrestrial plants associated with global changes. Nat Clim Chang 5:465–469CrossRefGoogle Scholar
  64. Yue K, Fornara DA, Yang W, Peng Y, Li Z, Wu F, Peng C (2017a) Effects of three global change drivers on terrestrial C:N:P stoichiometry: a global synthesis. Glob Chang Biol 23:2450–2463CrossRefGoogle Scholar
  65. Yue K, Fornara DA, Yang W, Peng Y, Peng C, Liu Z, Wu F (2017b) Influence of multiple global change drivers on terrestrial carbon storage: additive effects are common. Ecol Lett 20:663–672CrossRefGoogle Scholar
  66. Zamin TJ, Grogan P (2012) Birch shrub growth in the low Arctic: the relative importance of experimental warming, enhanced nutrient availability, snow depth and caribou exclusion. Environ Res Lett 7:1–10CrossRefGoogle Scholar
  67. Zhang Q, Wang YP, Matear RJ, Pitman AJ, Dai YJ (2014) Nitrogen and phosphorous limitations significantly reduce future allowable CO2 emissions. Geophys Res Lett 41:632–637CrossRefGoogle Scholar
  68. Zheng M, Huang J, Chen H, Wang H, Mo J (2015) Responses of soil acid phosphatase and beta-glucosidase to nitrogen and phosphorus addition in two subtropical forests in southern China. Eur J Soil Biol 68:77–84CrossRefGoogle Scholar
  69. Zhou L, Zhou X, Shao J, Nie Y, He Y, Jiang L, Wu Z, Bai SH (2016) Interactive effects of global change factors on soil respiration and its components: a meta-analysis. Glob Chang Biol 22:3157–3169CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Key Laboratory of Vegetation Restoration and Management of Degraded Ecosystems, South China Botanical Garden, CASChinese Academy of SciencesGuangzhouChina
  2. 2.CSIRO Oceans and AtmosphereAspendaleAustralia
  3. 3.Guangdong Eco-Engineering PolytechnicGuangzhouChina
  4. 4.University of Chinese Academy of SciencesBeijingChina

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