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Nutrient resorption helps drive intra-specific coupling of foliar nitrogen and phosphorus under nutrient-enriched conditions

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Abstract

Aims

Plant biomass growth, storage, and decomposition connect nitrogen (N) and phosphorus (P) cycles, yet we know relatively little about the dynamics of such coupling under nutrient enriched conditions, and our understanding of the interactive relationships between plant N and P in drylands remains particularly poor.

Methods

In a semiarid steppe of northern China, we examined the effects of single and combined N and P additions on soil and plant N and P pools for both mature and senesced leaves in two dominant grasses: Leymus chinensis and Stipa grandis.

Results

Nitrogen additions increased N concentrations in mature and senesced leaves for each plant species, and decreased N and P resorption during leaf senescence. The effects of N additions on foliar P concentrations were species-specific, while P additions had no effect on any nutrient characteristics examined. Due to treatment effects on N resorption, N and P concentrations were tightly correlated in senesced leaves but not in mature leaves.

Conclusions

Taken together, the results suggest plants in this ecosystem are much more responsive to changing N cycles than P cycles and emphasize the significance of nutrient resorption as an important plant control over the stoichiometric coupling of N and P under nutrient enriched conditions.

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References

  • Aerts R, Chapin FS (2000) The mineral nutrition of wild plants revisited: a re-evaluation of processes and patterns. Adv Ecol Res 30:1–67

    CAS  Google Scholar 

  • Aerts R, van Bodegom PM, Cornelissen JHC (2012) Litter stoichiometric traits of plant species of high-latitude ecosystems show high responsiveness to global change without causing strong variation in litter decomposition. New Phytol 196:181–188

    Article  CAS  PubMed  Google Scholar 

  • 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 

  • Bolnick DI, Amarasekare P, Araujo MS, Bürger R, Levine J, Novak M, Rudolf VHW, Schreiber SJ, Urban MC, Vasseur DA (2011) Why intraspecific trait variation matters in community ecology. Trends Ecol Evol 26:183–192

    Article  PubMed  PubMed Central  Google Scholar 

  • Borer ET, Bracken MES, Seabloom EW, Smith JE, Cebrian J, Cleland EE, Elser JJ, Fagan WF, Gruner DS, Harpole WS, Hillebrand H, Kerkhoff AJ, Ngai JT (2013) Global biogeography of autotroph chemistry: is insolation a driving force? Oikos 122:1121–1130

    Article  CAS  Google Scholar 

  • Cleveland CC, Townsend AR (2006) Nutrient additions to a tropical rain forest drive substantial soil carbon dioxide losses to the atmosphere. Proc Natl Acad Sci U S A 103:10316–10321

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cordell S, Goldstein G, Meinzer FC, Vitousek PM (2001) Regulation of leaf life-span and nutrient-use efficiency of Metrosideros polymorpha trees at two extremes of a long chronosequence in Hawaii. Oecologia 127:198–206

    Article  CAS  PubMed  Google Scholar 

  • Cornwell WK, Cornelissen JHC, Amatangelo K et al (2008) Plant species traits are the predominant control on litter decomposition rates within biomes worldwide. Ecol Lett 11:1065–1071

    Article  PubMed  Google Scholar 

  • Craine JM, Morrow C, Stock WD (2008) Nutrient concentration ratios and co-limitation in South African grasslands. New Phytol 179:829–836

    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 

  • Frey SD, Knorr M, Parrent JL, Simpson RT (2004) Chronic nitrogen enrichment affects the structure and function of the soil microbial community in temperate hardwood and pine forests. For Ecol Manag 196:159–171

    Article  Google Scholar 

  • Galloway JN et al (2008) Transformation of the nitrogen cycle: recent trends, questions, and potential solutions. Science 320:889–892

    Article  CAS  PubMed  Google Scholar 

  • Güsewell S (2005) Nutrient resorption of wetland graminoids is related to the type of nutrient limitation. Funct Ecol 19:344–354

    Article  Google Scholar 

  • Harpole WS et al (2011) Nutrient co-limitation of primary producer communities. Ecol Lett 14:852–862

    Article  PubMed  Google Scholar 

  • He JS, Wang L, Flynn DF, Wang X, Ma W, Fang J (2008) Leaf nitrogen:phosphorus stoichiometry across Chinese grassland biomes. Oecologia 155:301–310

    Article  PubMed  Google Scholar 

  • Kichenin E, Wardle DA, Peltzer DA, Morse CW, Freschet GT (2013) Contrasting effects of plant inter- and intraspecific variation on community-level trait measures along an environmental gradient. Funct Ecol 27:1254–1261

    Article  Google Scholar 

  • Killingbeck KT (1996) Nutrients in senesced leaves: keys to the search for potential resorption and resorption proficiency. Ecology 77:1716–1727

    Article  Google Scholar 

  • Kozovits AR et al (2007) Nutrient resorption and patterns of litter production and decomposition in a Neotropical Savanna. Funct Ecol 21:1034–1043

    Article  Google Scholar 

  • Lü XT, Han XG (2010) Nutrient resorption responses to water and nitrogen amendment in semi-arid grassland of Inner Mongolia, China. Plant Soil 327:481–491

    Article  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

    Article  PubMed  Google Scholar 

  • Mahowald N, Jickells TD, Baker AR et al (2008) Global distribution of atmospheric phosphorus sources, concentrations and deposition rates, and anthropogenic impacts. Glob Biogeochem Cycles 22, GB4026

    Article  Google Scholar 

  • Manzoni S, Trofymow JA, Jackson RB, Porporato A (2010) Stoichiometric controls on carbon, nitrogen, and phosphorus dynamics in decomposing litter. Ecol Monogr 80:89–106

    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 

  • McGroddy ME, Daufresne T, Hedin LO (2004) Scaling of C : N : P stoichiometry in forests worldwide: Implications of terrestrial redfield-type ratios. Ecology 85:2390–2401

    Article  Google Scholar 

  • Okin GS, Mahowald N, Chadwick OA, Artaxo P (2004) Impact of desert dust on the biogeochemistry of phosphorus in terrestrial ecosystems. Glob Biogeochem Cycles 18, GB2005

    Article  Google Scholar 

  • Ostertag R (2010) Foliar nitrogen and phosphorus accumulation responses after fertilization: an example from nutrient-limited Hawaiian forests. Plant Soil 334:85–98

    Article  CAS  Google Scholar 

  • Parton W, Silver WL, Burke IC, Grassens L, Harmon ME, Currie WS, King JY, Adair EC, Brandt LA, Hart SC, Fasth B (2007) Global-scale similarities in nitrogen release patterns during long-term decomposition. Science 315:361–364

    Article  CAS  PubMed  Google Scholar 

  • Penuelas J, Poulter B, Sardans J et al (2013) Human-induced nitrogen-phosphorus imbalances alter natural and managed ecosystems across the globe. Nat Commun 4:2934

    PubMed  Google Scholar 

  • Persson J, Fink P, Goto A, Hood JM, Jonas J, Kato S (2010) To be or not to be what you eat: regulation of stoichiometric homeostasis among autotrophs and heterotrophs. Oikos 119:741–751

    Article  CAS  Google Scholar 

  • Reed SC, Seastedt TR, Mann CM, Suding KN, Townsend AR, Cherwin KL (2007) Phosphorus fertilization stimulates nitrogen fixation and increases inorganic nitrogen concentrations in a restored prairie. Appl Soil Ecol 36:238–242

    Article  Google Scholar 

  • Reed SC, Vitousek PM, Cleveland CC (2011) Are patterns in nutrient limitation belowground consistent with those aboveground: results from a 4 million year chronosequence. Biogeochemistry 106:323–336

    Article  CAS  Google Scholar 

  • Reed SC, Townsend AR, Davidson EA, Cleveland CC (2012) Stoichiometric patterns in foliar nutrient resorption across multiple scales. New Phytol 198:173–180

    Article  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 

  • Rivas-Ubach A, Sardans J, Perez-Trujillo M, Estiarte M, Penuelas J (2012) Strong relationship between elemental stoichiometry and metabolome in plants. Proc Natl Acad Sci U S A 109:4181–4186

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schade JD, Kyle M, Hobbie SE, Fagan WF, Elser JJ (2003) Stoichiometric tracking of soil nutrients by a desert insect herbivore. Ecol Lett 6:96–101

    Article  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 

  • Tao LL, Hunter MD (2012) Does anthropogenic nitrogen deposition induce phosphorus limitation in herbivorous insects? Glob Chang Biol 18:1843–1853

    Article  Google Scholar 

  • van Heerwaarden LM, Toet S, Aerts R (2003a) Current measures of nutrient resorption efficiency lead to a substantial underestimation of real resorption efficiency: facts and solutions. Oikos 101:664–669

    Article  Google Scholar 

  • van Heerwaarden LM, Toet S, Aerts R (2003b) Nitrogen and phosphorus resorption efficiency and proficiency in six sub-arctic bog species after 4 years of nitrogen fertilization. J Ecol 91:1060–1070

    Article  Google Scholar 

  • Vergutz L, Manzoni S, Porporato A, Novais RF, Jackson RB (2012) Global resorption efficiencies and concentrations of carbon and nutrients in leaves of terrestrial plants. Ecol Monogr 82:205–220

    Article  Google Scholar 

  • Violle C, Enquist BJ, McGill BJ, Jiang L, Albert CH, Hulshof C, Jung V, Messier J (2012) The return of the variance: intraspecific variability in community ecology. Trends Ecol Evol 27:244–252

    Article  PubMed  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 

  • Walker AP, Beckerman AP, Gu L et al (2014) The relationship of leaf photosynthetic traits - V-cmax and J(max) - to leaf nitrogen, leaf phosphorus, and specific leaf area: a meta-analysis and modeling study. Ecol Evol 4:3218–3235

    Article  PubMed  PubMed Central  Google Scholar 

  • Watanabe T, Broadley MR, Jansen S et al (2007) Evolutionary control of leaf element composition in plants. New Phytol 174:516–523

    Article  CAS  PubMed  Google Scholar 

  • Wright IJ, Reich PB, Westoby M et al (2004) The worldwide leaf economics spectrum. Nature 428:821–827

    Article  CAS  PubMed  Google Scholar 

  • Zhang NY, Guo R, Song PA, Guo JX, Gao YZ (2013) Effects of warming and nitrogen deposition on the coupling mechanism between soil nitrogen and phosphorus in Songnen Meadow Steppe, northeastern China. Soil Biol Biochem 65:96–104

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors thank Weijun Wu and Shuxia Liu for help with field measurements, Qiang Li and Li Li for help with laboratory analyses, and two anonymous reviewers for suggestions that significantly improved the manuscript. This study was financially supported by the National Basic Research Program of China (2015CB150802), the National Natural Science Foundation of China (41273094 and 31470505), the Strategic Priority Research Program of the Chinese Academy of Sciences (XDB15010403), the State Key Laboratory of Forest and Soil Ecology (LFSE2013-13 and 2015-16), the Youth Innovation Promotion Association of the Chinese Academy of Sciences (2014174), and the Key Laboratory of Vegetation Ecology of the Ministry of Education. Any use of trade, firm, or product names is for descriptive purposes only and does not imply endorsement by the U.S. Government.

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Authors and Affiliations

  1. State Key Laboratory of Forest and Soil Ecology, Institute of Applied Ecology, Chinese Academy of Sciences, Shenyang, 110164, China

    Xiao-Tao Lü, Qiang Yu & Xing-Guo Han

  2. Key Laboratory of Vegetation Ecology, Ministry of Education, Institute of Grassland Science, Northeast Normal University, Changchun, 130024, China

    Xiao-Tao Lü

  3. U.S. Geological Survey, Southwest Biological Science Center, Moab, UT, 84532, USA

    Sasha C. Reed

Authors
  1. Xiao-Tao Lü
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Correspondence to Xiao-Tao Lü.

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Responsible Editor: Alfonso Escudero.

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Lü, XT., Reed, S.C., Yu, Q. et al. Nutrient resorption helps drive intra-specific coupling of foliar nitrogen and phosphorus under nutrient-enriched conditions. Plant Soil 398, 111–120 (2016). https://doi.org/10.1007/s11104-015-2642-y

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  • DOI: https://doi.org/10.1007/s11104-015-2642-y

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