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Effects of nitrogen-phosphorus imbalance on plant biomass production: a global perspective

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Abstract

Background and aims

Unparalleled inputs of anthropogenic nitrogen (N) and phosphorus (P) cause a strong N-P imbalance in terrestrial ecosystems. However, the effects of N-P imbalance on plant biomass production remains unclear.

Methods

Given that tissue N:P ratio may serve as an indicator of plant N or P limitations, we compiled a dataset reporting aboveground biomass (AGB) and tissue N:P ratio simultaneously from worldwide N addition experiments and explored the relationship between the responses of AGB and tissue N:P ratio to N enrichment.

Results

The N-induced changes in AGB exhibited an asymptotic relationship (i.e., Michaelis-Menten function) with changes in tissue N:P ratio, indicating a progressive P limitation with increasing N. Our results further revealed that plant N and P status was related to the changes in soil inorganic N and P concentrations. Soil N increased while soil P remained unchanged with increasing N rate, thus resulting in an unbalanced soil N and P as N continues to increase.

Conclusions

This study is the first to report the influences of human-induced N-P imbalance on plant biomass production at the global scale. The biomass-N:P ratio relationship needs to be considered for reliable predictions of the future global carbon dynamics under global change.

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References

  • Adams DC, Gurevitch J, Rosenberg MS (1997) Resampling tests for meta-analysis of ecological data. Ecology 78:1277–1283

    Article  Google Scholar 

  • Burnham KP, Anderson DR (2002) Model selection and multimodel inference, 2nd edn. Springer-Verlag, New York

    Google Scholar 

  • Crous KY, O'Sullivan OS, Zaragoza-Castells J, Bloomfield KJ, Negrini ACA, Meir P, Turnbull MH, Griffin KL, Atkin OK (2017) Nitrogen and phosphorus availabilities interact to modulate leaf trait scaling relationships across six plant functional types in a controlled-environment study. New Phytol 215:992–1008

    Article  CAS  PubMed  Google Scholar 

  • de Vries W (2014) Nutrients trigger carbon storage. Nat Clim Chang 4:425–426

    Article  Google Scholar 

  • Deng Q, Hui DF, Luo YQ, Elser J, Wang YP, Loladze I, Zhang QF, Dennis S (2015) Down-regulation of tissue N:P ratios in terrestrial plants by elevated CO2. Ecology 96:3354–3362

    Article  PubMed  Google Scholar 

  • Egger M, Smith GD, Schneider M, Minder C (1997) Bias in meta-analysis detected by a simple, graphical test. Brit Med J 315:629–634

    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

    Article  PubMed  Google Scholar 

  • 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 186:593–608

    Article  CAS  PubMed  Google Scholar 

  • Fay PA, Prober SM, Harpole WS, Knops JM, Bakker JD, Borer ET, Lind EM, MacDougall AS, Seabloom EW, Wragg PD et al (2015) Grassland productivity limited by multiple nutrients. Nat Plants 1:15080

    Article  CAS  PubMed  Google Scholar 

  • Finzi AC, Austin AT, Cleland EE, Frey SD, Houlton BZ, Wallenstein MD (2011) Responses and feedbacks of coupled biogeochemical cycles to climate change: examples from terrestrial ecosystems. Front Ecol Environ 9:61–67

    Article  Google Scholar 

  • Fraser LH, Henry HAL, Carlyle CN, White SR, Beierkuhnlein C, Cahill JF Jr, Casper BB, Cleland E, Collins SL, Dukes JS, Knapp AK, Lind E, Long R, Luo Y, Reich PB, Smith MD, Sternberg M, Turkington R (2013) Coordinated distributed experiments: an emerging tool for testing global hypotheses in ecology and environmental science. Front Ecol Environ 11:147–155

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Hinsinger P (2001) Bioavailability of soil inorganic P in the rhizosphere as affected by root-induced chemical changes: a review. Plant Soil 237:173–195

    Article  CAS  Google Scholar 

  • Högberg P, Fan H, Quist M, Binkley D, Tamm C (2006) Tree growth and soil acidification in response to 30 years of experimental nitrogen loading on boreal forest. Glob Chang Biol 12:489–499

    Article  Google Scholar 

  • Janssens IA, Dieleman W, Luyssaert S, Subke JA, Reichstein M, Ceulemans R, Ciais P, Dolman AJ, Grace J, Matteucci G, Papale D, Piao SL, Schulze ED, Tang J, Law BE (2010) Reduction of forest soil respiration in response to nitrogen deposition. Nat Geosci 3:315–322

    Article  CAS  Google Scholar 

  • Koricheva J, Gurevitch J (2014) Uses and misuses of meta-analysis in plant ecology. J Ecol 102:828–844

    Article  Google Scholar 

  • Lam SK, Chen D, Norton R, Armstrong R, Mosier AR (2012) Nitrogen dynamics in grain crop and legume pasture systems under elevated atmospheric carbon dioxide concentration: a meta-analysis. Glob Chang Biol 18:2853–2859

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Lee M, Manning P, Rist J, Power SA, Marsh C (2010) A global comparison of grassland biomass responses to CO2 and nitrogen enrichment. P Roy Soc B-Biol Sci 365:2047–2056

    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

    Article  PubMed  Google Scholar 

  • MacNally R (2000) Regression and model-building in conservation biology, biogeography and ecology: the distinction between–and reconciliation of–‘predictive’ and ‘explanatory’ models. Biodivers Conserv 9:655–671

    Article  Google Scholar 

  • Marklein AR, Houlton BZ (2012) Nitrogen inputs accelerate phosphorus cycling rates across a wide variety of terrestrial ecosystems. New Phytol 193:696–704

    Article  CAS  PubMed  Google Scholar 

  • Marschner P (2011) Mineral nutrition of higher plants, 3rd edn. Academic Press, UK

    Google Scholar 

  • Peng YF, Yang YH (2016) Allometric biomass partitioning under nitrogen enrichment: evidence from manipulative experiments around the world. Sci Rep 6:28918

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Peng YF, Guo DL, Yang YH (2017a) Global patterns of root dynamics under nitrogen enrichment. Glob Ecol Biogeogr 26:102–114

    Article  Google Scholar 

  • Peng YF, Li F, Zhou GY, Fang K, Zhang DY, Li CB, Yang GB, Wang GQ, Wang J, Yang YH (2017b) Linkages of plant stoichiometry to ecosystem production and carbon fluxes with increasing nitrogen inputs in an alpine steppe. Glob Chang Biol 23:5249–5259

    Article  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 et al (2013) Human-induced nitrogen-phosphorus imbalances alter natural and managed ecosystems across the globe. Nat Commun 4:2934

    Article  CAS  PubMed  Google Scholar 

  • R Development Core Team (2015) R: A language and environment for statistical computing. Vienna, Austria

  • Reich PB, Walters MB, Ellsworth DS (1997) From tropics to tundra: global convergence in plant functioning. P Natl Acad Sci USA 94:13730–13734

    Article  CAS  Google Scholar 

  • Reich PB, Oleksyn J, Wright IJ (2009) Leaf phosphorus influences the photosynthesis-nitrogen relation: a cross-biome analysis of 314 species. Oecologia 160:207–212

    Article  PubMed  Google Scholar 

  • Sardans J, Grau O, Chen HYH, Janssens IA, Ciais P, Piao S, Peñuelas J (2017) Changes in nutrient concentrations of leaves and roots in response to global change factors. Glob Chang Biol 23:3849–3856

    Article  PubMed  Google Scholar 

  • Sistla SA, Schimel JP (2012) Stoichiometric flexibility as a regulator of carbon and nutrient cycling in terrestrial ecosystems under change. New Phytol 196:68–78

    Article  CAS  PubMed  Google Scholar 

  • Soons MB, Hefting MM, Dorland E, Lamers LPM, Versteeg C, Bobbink R (2017) Nitrogen effects on plant species richness in herbaceous communities are more widespread and stronger than those of phosphorus. Biol Conserv 212:390–397

    Article  Google Scholar 

  • Taiz L, Zeiger E (2006) Plant physiology, 4th edn. Sinauer Associates Inc., Sunderland

    Google Scholar 

  • Vitousek PM, Howarth RW (1991) Nitrogen limitation on land and in the sea–how can it occur? Biogeochemistry 13:87–115

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Wang XZ, Taub DR (2010) Interactive effects of elevated carbon dioxide and environmental stresses on root mass fraction in plants: a meta-analytical synthesis using pairwise techniques. Oecologia 163:1–11

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Yuan ZY, Chen HYH (2015) Decoupling of nitrogen and phosphorus in terrestrial plants associated with global changes. Nat Clim Chang 5:465–469

    Article  CAS  Google Scholar 

  • Yue K, Fornara DA, Yang WQ, Peng Y, Li ZJ, Wu FZ, Peng CH (2017) Effects of three global change drivers on terrestrial C:N:P stoichiometry: a global synthesis. Glob Chang Biol 23:2450–2463

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

This study was financially supported by the National Natural Science Foundation of China (31770521), Hebei Science and Technology Project (17226914D) and Youth Innovation Promotion Association CAS.

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Authors and Affiliations

  1. State Key Laboratory of Vegetation and Environmental Change, Institute of Botany, Chinese Academy of Sciences, Beijing, 100093, China

    Yunfeng Peng

  2. College of Resources and Environmental Sciences, Hebei Agricultural University, Baoding, 071000, China

    Zhengping Peng

  3. Institute of Protected Agriculture, Chinese Academy of Agricultural Engineering, Beijing, 100125, China

    Xieting Zeng

  4. Agriculture Research and Technology, National Crop Insurance Services, Overland Park, KS, USA

    James H. Houx III

Authors
  1. Yunfeng Peng
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  2. Zhengping Peng
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  3. Xieting Zeng
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  4. James H. Houx III
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Correspondence to Yunfeng Peng.

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Peng, Y., Peng, Z., Zeng, X. et al. Effects of nitrogen-phosphorus imbalance on plant biomass production: a global perspective. Plant Soil 436, 245–252 (2019). https://doi.org/10.1007/s11104-018-03927-5

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