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Evaluating P availability influenced by warming and N deposition in a subtropical forest soil: a bioassay mesocosm experiment

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Abstract

Aims

Phosphorus (P) is a limited nutrient in highly weathered subtropical or tropical forest soils and it is unclear how both the cycling and availability of P will respond to future global warming and nitrogen (N) deposition. This study aims to evaluate the influence of soil warming and N deposition on soil P fractions in relation to plant growth and P uptake.

Methods

We carried out a field mesocosm bioassay experiment with a soil warming and N addition treatment in a factorial design and measured soil Hedley P fraction and P uptake of the Chinese fir (Cunninghamia lanceolata) seedlings.

Results

Soil warming significantly increased soil easily-available and moderately-available inorganic phosphorus (Pi) but had no effect on soil easily-available and moderately-available organic P (Po), or on plant growth or plant biomass P, and decreased soil microbial biomass P (MBP). Nitrogen addition increased plant growth and leaf biomass P, but had no effect on soil Pi and MBP, and decreased soil moderately-available Po and leaf P concentration. There were no interactions between soil warming and nitrogen on Hedley P fractions. None of the Hedley P fractions had correlated with plant height and diameter growth or with plant P uptake.

Conclusions

Our results suggest that the Hedley P fractions do not reflect soil P availability and that the growth of the Chinese fir is not limited by soil P availability in this subtropical Ultisol, rather it is most likely limited by N and water availability based on the results from this bioassay experiment.

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References

  • Abdelhalim T, Jannoura R, Joergensen RG (2019) Mycorrhiza response and phosphorus acquisition efficiency of sorghum cultivars differing in strigolactone composition. Plant Soil 437:55–63

    CAS  Google Scholar 

  • Achat DL, Morel C, Bakker MR, Augusto L, Pellerin S, Gallet-Budynek A, Gonzalez M (2010) Assessing turnover of microbial biomass phosphorus: combination of an isotopic dilution method with a mass balance model. Soil Biol Biochem 42:2231–2240

    CAS  Google Scholar 

  • Baon JB, Smith SE, Alston AM (1994) Phosphorus uptake and growth of barley as affected by soil temperature and mycorrhizal infection. J Plant Nutr 17:479–492

    Google Scholar 

  • Barber SA, Mackay AD, Kuchenbuch RO, Barraclough PB (1988) Effects of soil temperature and water on maize root growth. Plant Soil 111:267–269

    CAS  Google Scholar 

  • Barrow NJ (1979) Three effects of temperature on the reactions between inorganic phoshate and soil. J Soil Sci 30:271–279

    CAS  Google Scholar 

  • Barrow NJ (1983) A mechanistic model for describing the sorption and desorption of phosphate by soil. J Soil Sci 34:733–750

    CAS  Google Scholar 

  • Brockett BFT, Prescott CE, Grayston SJ (2012) Soil moisture is the major factor influencing microbial community structure and enzyme activities across seven biogeoclimatic zones in western Canada. Soil Biol Biochem 44:9–20

    CAS  Google Scholar 

  • Brookes PC, Powlson DS, Jenkinson DS (1982) Measurement of microbial biomass phosphorus in soil. Soil Biol Biochem 14:319–329

    CAS  Google Scholar 

  • Bünemann EK (2015) Assessment of gross and net mineralization rates of soil organic phosphorus – a review. Soil Biol Biochem 89:82–98

    Google Scholar 

  • Catherine Eimers M, Dillon PJ, Schiff SL, Jeffries DS (2003) The effects of drying and re-wetting and increased temperature on sulphate release from upland and wetland material. Soil Biol Biochem 35:1663–1673

    Google Scholar 

  • Chen CR, Condron LM, Davis MR, Sherlock RR (2002) Phosphorus dynamics in the rhizosphere of perennial ryegrass (Lolium perenne L.) and radiata pine (Pinus radiata D. Don.). Soil Biol Biochem 34:487–499

    CAS  Google Scholar 

  • Chen GS, Yang ZJ, Gao R, Xie JS, Guo JF, Huang ZQ, Yang YS (2013) Carbon storage in a chronosequence of Chinese fir plantations in southern China. For Ecol Manag 300:68–76

    Google Scholar 

  • Chen L, Jia HY, Zeng J, Dell B (2016) Growth and nutrient efficiency of Betula alnoides clones in response to phosphorus supply. Ann For Res 59:199–207

    Google Scholar 

  • Chen X, Wang G, Zhang T, Mao T, Wei D, Song C, Hu Z, Huang K (2017) Effects of warming and nitrogen fertilization on GHG flux in an alpine swamp meadow of a permafrost region. Sci Total Environ 601-602:1389–1399

    CAS  PubMed  Google Scholar 

  • Clarholm M, Skyllberg U, Rosling A (2015) Organic acid induced release of nutrients from metal-stabilized soil organic matter – the unbutton model. Soil Biol Biochem 84:168–176

    CAS  Google Scholar 

  • Classen AT, Sundqvist MK, Henning JA, Newman GS, Moore JAM, Cregger MA, Moorhead LC, Patterson CM (2015) Direct and indirect effects of climate change on soil microbial and soil microbial-plant interactions: what lies ahead? Ecosphere 6:1–21

    Google Scholar 

  • Cleveland CC, Houlton BZ, Smith WK, Marklein AR, Reed SC, Parton W, Del Grosso SJ, Running SW (2013) Patterns of new versus recycled primary production in the terrestrial biosphere. Proc Natl Acad Sci U S A 110:12733–12737

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dawes MA, Schleppi P, Hättenschwiler S, Rixen C, Hagedorn F (2017) Soil warming opens the nitrogen cycle at the alpine treeline. Glob Change Biol 23:421–434

    Google Scholar 

  • DeLuca TH, Glanville HC, Harris M, Emmett BA, Pingree MRA, de Sosa LL, Cerdá-Moreno C, Jones DL (2015) A novel biologically-based approach to evaluating soil phosphorus availability across complex landscapes. Soil Biol Biochem 88:110–119

    CAS  Google Scholar 

  • Deng M, Liu L, Sun Z, Piao S, Ma Y, Chen Y, Wang J, Qiao C, Wang X, Li P (2016) Increased phosphate uptake but not resorption alleviates phosphorus deficiency induced by nitrogen deposition in temperate Larix principis-rupprechtii plantations. New Phytol 212:1019–1029

    CAS  PubMed  Google Scholar 

  • Deng Q, Hui D, Dennis S, Reddy KC (2017) Responses of terrestrial ecosystem phosphorus cycling to nitrogen addition: a meta-analysis. Glob Ecol Biogeogr 26:713–728

    Google Scholar 

  • Doetterl S, Berhe AA, Arnold C, Bodé S, Fiener P, Finke P, Fuchslueger L, Griepentrog M, Harden JW, Nadeu E, Schnecker J, Six J, Trumbore S, Van Oost K, Vogel C, Boeckx P (2018) Links among warming, carbon and microbial dynamics mediated by soil mineral weathering. Nat Geosci 11:589–593

    CAS  Google Scholar 

  • Fan Y, Lin F, Yang L, Zhong X, Wang M, Zhou J, Chen Y, Yang Y (2018) Decreased soil organic P fraction associated with ectomycorrhizal fungal activity to meet increased P demand under N application in a subtropical forest ecosystem. Biol Fertil Soils 54:149–161

    CAS  Google Scholar 

  • Fatemi FR, Fernandez IJ, Simon KS, Dail DB (2016) Nitrogen and phosphorus regulation of soil enzyme activities in acid forest soils. Soil Biol Biochem 98:171–179

    CAS  Google Scholar 

  • Fellbaum CR, Mensah JA, Pfeffer PE, Kiers ET, Bücking H (2012) The role of carbon in fungal nutrient uptake and transport. Plant Signal Behav 7:1509–1512

    CAS  PubMed  PubMed Central  Google Scholar 

  • Field CB et al (2014) IPCC, 2014: climate change 2014: impacts, adaptation, and vulnerability. Part A: global and sectoral aspects. Contribution of working group II to the fifth assessment report of the intergovernmental panel on climate change. Cambridge University Press, Cambridge and New York

    Google Scholar 

  • Franzluebbers AJ (1999) Microbial activity in response to water-filled pore space of variably eroded southern piedmont soils. Appl Soil Ecol 11:91–101

    Google Scholar 

  • Frossard E, Condron LM, Oberson A, Sinaj S, Fardeau JC (2000) Processes governing phosphorus availability in temperate soils. J Environ Qual 29:15–23

    CAS  Google Scholar 

  • García-Palacios P, Vandegehuchte ML, Shaw EA, Dam M, Post KH, Ramirez KS, Sylvain ZA, de Tomasel CM, Wall DH (2015) Are there links between responses of soil microbes and ecosystem functioning to elevated CO2, N deposition and warming? A global perspective. Glob Change Biol 21:1590–1600

    Google Scholar 

  • Gong S, Zhang T, Guo R, Cao H, Shi L, Guo J, Sun W (2015) Response of soil enzyme activity to warming and nitrogen addition in a meadow steppe. Soil Res 53:242–252

    CAS  Google Scholar 

  • Guppy CN, Menzies NW, Moody PW, Blamey FPC (2005) Competitive sorption reactions between phosphorus and organic matter in soil: a review. Soil Res 43:189–202

    CAS  Google Scholar 

  • Hedley MJ, Stewart JWB, Chauhan BS (1982) Changes in inorganic and organic soil phosphorus fractions induced by cultivation practices and by laboratory incubations1. Soil Sci Soc Am J 46:970–976

    CAS  Google Scholar 

  • Hou E, Chen C, Luo Y, Zhou G, Kuang Y, Zhang Y, Heenan M, Lu X, Wen D (2018) Effects of climate on soil phosphorus cycle and availability in natural terrestrial ecosystems. Glob Change Biol 24:3344–3356

    Google Scholar 

  • Huang W, Liu J, Zhou G, Zhang D, Deng Q (2011) Effects of precipitation on soil acid phosphatase activity in three successional forests in southern China. Biogeosciences 8:1901–1910

    CAS  Google Scholar 

  • Jansa J, Finlay R, Wallander H, Smith FA, Smith SE (2011) Role of mycorrhizal symbioses in phosphorus cycling. In: Bünemann E, Oberson A, Frossard E (eds) Phosphorus in action: biological processes in soil phosphorus cycling. Springer Berlin Heidelberg, Berlin, Heidelberg

    Google Scholar 

  • Jia Y, Yu G, Gao Y, He N, Wang Q, Jiao C, Zuo Y (2016) Global inorganic nitrogen dry deposition inferred from ground- and space-based measurements. Sci Rep 6:1–12

    Google Scholar 

  • Jing X, Chen X, Tang M, Ding Z, Jiang L, Li P, Ma S, Tian D, Xu L, Zhu J, Ji C, Shen H, Zheng C, Fang J, Zhu B (2017) Nitrogen deposition has minor effect on soil extracellular enzyme activities in six Chinese forests. Sci Total Environ 607-608:806–815

    CAS  PubMed  Google Scholar 

  • Jonasson S, Michelsen A, Schmidt IK, Nielsen EV (1999) Responses in microbes and plants to changed temperature, nutrient and light reglmes in the arctic. Ecology 80:1828–1843

    Google Scholar 

  • Kabała C, Musztyfaga E, Gałka B, Łabuńska D, Mańczyńska P (2016) Conversion of soil pH 1:2.5 KCl and 1:2.5 H2O to 1:5 H2O: conclusions for soil management, environmental monitoring, and international soil databases. Pol J Environ Stud 25:647–653

    Google Scholar 

  • Knutti R, Sedláček J (2012) Robustness and uncertainties in the new CMIP5 climate model projections. Nat Clim Chang 3:369–373

    Google Scholar 

  • Kormanik PP, Bryan WC, Schultz RC (1980) Procedures and equipment for staining large numbers of plant root samples for endomycorrhizal assay. Can J Microbiol 26:536–538

    CAS  PubMed  Google Scholar 

  • Kouno K, Tuchiya Y, Ando T (1995) Measurement of soil microbial biomass phosphorus by an anion exchange membrane method. Soil Biol Biochem 27:1353–1357

    CAS  Google Scholar 

  • Li J, Jian S, de Koff JP, Lane CS, Wang G, Mayes MA, Hui D (2018a) Differential effects of warming and nitrogen fertilization on soil respiration and microbial dynamics in switchgrass croplands. GCB Bioenergy 10:565–576

    CAS  Google Scholar 

  • Li Y, Qing Y, Lyu M, Chen S, Yang Z, Lin C, Yang Y (2018b) Effects of artificial warming on different soil organic carbon and nitrogen pools in a subtropical plantation. Soil Biol Biochem 124:161–167

    CAS  Google Scholar 

  • Liang C, Balser TC (2012) Warming and nitrogen deposition lessen microbial residue contribution to soil carbon pool. Nat Commun 3:1–3

    Google Scholar 

  • Liu X, Zhang Y, Han W, Tang A, Shen J, Cui Z, Vitousek P, Erisman JW, Goulding K, Christie P, Fangmeier A, Zhang F (2013) Enhanced nitrogen deposition over China. Nature 494:459–462

    CAS  PubMed  Google Scholar 

  • Liu X, Yang Z, Lin C, Giardina CP, Xiong D, Lin W, Chen S, Xu C, Chen G, Xie J, Li Y, Yang Y (2017a) Will nitrogen deposition mitigate warming-increased soil respiration in a young subtropical plantation? Agric For Meteorol 246:78–85

    Google Scholar 

  • Liu Y, Wang C, He N, Wen X, Gao Y, Li S, Niu S, Butterbach-Bahl K, Luo Y, Yu G (2017b) A global synthesis of the rate and temperature sensitivity of soil nitrogen mineralization: latitudinal patterns and mechanisms. Glob Change Biol 23:455–464

    Google Scholar 

  • Long M, Wu H-H, Smith MD, La Pierre KJ, Lü X-T, Zhang H-Y, Han X-G, Yu Q (2016) Nitrogen deposition promotes phosphorus uptake of plants in a semi-arid temperate grassland. Plant Soil 408:475–484

    CAS  Google Scholar 

  • Lu X, Mao Q, Gilliam FS, Luo Y, Mo J (2014) Nitrogen deposition contributes to soil acidification in tropical ecosystems. Glob Change Biol 20:3790–3801

    Google Scholar 

  • Maranguit D, Guillaume T, Kuzyakov Y (2017) Land-use change affects phosphorus fractions in highly weathered tropical soils. Catena 149:385–393

    CAS  Google Scholar 

  • Melillo JM, McGuire AD, Kicklighter DW, Moore B, Vorosmarty CJ, Schloss AL (1993) Global climate change and terrestrial net primary production. Nature 363:234–240

    CAS  Google Scholar 

  • Mellett T, Selvin C, Defforey D, Roberts K, Lecher AL, Dennis K, Gutknecht J, Field C, Paytan A (2018) Assessing cumulative effects of climate change manipulations on phosphorus limitation in a californian grassland. Environ Sci Technol 52:98–106

    CAS  PubMed  Google Scholar 

  • Menge DNL, Field CB (2007) Simulated global changes alter phosphorus demand in annual grassland. Glob Change Biol 13:2582–2591

    Google Scholar 

  • Murphy J, Riley JP (1962) A modified single solution method for the determination of phosphate in natural waters. Anal Chim Acta 27:31–36

    CAS  Google Scholar 

  • Nannipieri P, Giagnoni L, Landi L, Renella G (2011) Role of phosphatase enzymes in soil. In: Bünemann E, Oberson A, Frossard E (eds) Phosphorus in action: biological processes in soil phosphorus cycling. Springer Berlin Heidelberg, Berlin, Heidelberg

    Google Scholar 

  • Návar J (2010) Measurement and assessment methods of forest aboveground biomass: a literature review and the challenges ahead. Sciyo, Rijeka, pp 27–64

    Google Scholar 

  • Peltre C, Gregorich EG, Bruun S, Jensen LS, Magid J (2017) Repeated application of organic waste affects soil organic matter composition: evidence from thermal analysis, FTIR-PAS, amino sugars and lignin biomarkers. Soil Biol Biochem 104:117–127

    CAS  Google Scholar 

  • Reay DS, Dentener F, Smith P, Grace J, Feely RA (2008) Global nitrogen deposition and carbon sinks. Nat Geosci 1:430–437

    CAS  Google Scholar 

  • Rosling A, Midgley MG, Cheeke T, Urbina H, Fransson P, Phillips RP (2016) Phosphorus cycling in deciduous forest soil differs between stands dominated by ecto- and arbuscular mycorrhizal trees. New Phytol 209:1184–1195

    PubMed  Google Scholar 

  • Rui Y, Wang Y, Chen C, Zhou X, Wang S, Xu Z, Duan J, Kang X, Lu S, Luo C (2012) Warming and grazing increase mineralization of organic P in an alpine meadow ecosystem of Qinghai-Tibet plateau, China. Plant Soil 357:73–87

    CAS  Google Scholar 

  • Rustad L, Campbell J, Marion G, Norby R, Mitchell M, Hartley A, Cornelissen J, Gurevitch J, Gcte N (2001) A meta-analysis of the response of soil respiration, net nitrogen mineralization, and aboveground plant growth to experimental ecosystem warming. Oecologia 126:543–562

    CAS  PubMed  Google Scholar 

  • Saiya-Cork KR, Sinsabaugh RL, Zak DR (2002) The effects of long term nitrogen deposition on extracellular enzyme activity in an Acer saccharum forest soil. Soil Biol Biochem 34:1309–1315

    CAS  Google Scholar 

  • Santiago LS, Wright SJ, Harms KE, Yavitt JB, Korine C, Garcia MN, Turner BL (2012) Tropical tree seedling growth responses to nitrogen, phosphorus and potassium addition. J Ecol 100:309–316

    CAS  Google Scholar 

  • Sanyal SK, De Datta SK (1991) Chemistry of phosphorus transformations in soil. In: Stewart BA (ed) Advances in soil science: volume 16. Springer New York, New York

    Google Scholar 

  • Sardans J, Peñuelas J, Estiarte M (2006) Warming and drought alter soil phosphatase activity and soil P availability in a Mediterranean shrubland. Plant Soil 289:227–238

    CAS  Google Scholar 

  • Schachtman DP, Reid RJ, Ayling SM (1998) Phosphorus uptake by plants: from soil to cell. Plant Physiol 116:447–453

    CAS  PubMed  PubMed Central  Google Scholar 

  • Smeck NE (1985) Phosphorus dynamics in soils and landscapes. Geoderma 36:185–199

    CAS  Google Scholar 

  • Soudzilovskaia NA, Douma JC, Akhmetzhanova AA, van Bodegom PM, Cornwell WK, Moens EJ, Treseder KK, Tibbett M, Wang Y-P, Cornelissen JHC (2015) Global patterns of plant root colonization intensity by mycorrhizal fungi explained by climate and soil chemistry. Glob Ecol Biogeogr 24:371–382

    Google Scholar 

  • Strock CF, Morrow de la Riva L, Lynch JP (2018) Reduction in root secondary growth as a strategy for phosphorus acquisition. Plant Physiol 176:691–703

    CAS  PubMed  Google Scholar 

  • The Committee of China’s National Assessment Report on Climate Change (2015) China’s National Assessment Report on climate change, 3rd edn. China Science Press, Beijing

    Google Scholar 

  • Turner BL, Lambers H, Condron LM, Cramer MD, Leake JR, Richardson AE, Smith SE (2013) Soil microbial biomass and the fate of phosphorus during long-term ecosystem development. Plant Soil 367:225–234

    CAS  Google Scholar 

  • Turner BL, Brenes-Arguedas T, Condit R (2018) Pervasive phosphorus limitation of tree species but not communities in tropical forests. Nature 555:367–370

    CAS  PubMed  Google Scholar 

  • Uselman SM, Qualls RG, Thomas RB (2000) Effects of increased atmospheric CO2, temperature, and soil N availability on root exudation of dissolved organic carbon by a N-fixing tree (Robinia pseudoacacia L.). Plant Soil 222:191–202

    CAS  Google Scholar 

  • Wang M, Xue J, Horswell J, Kimberley MO, Huang Z (2017) Long-term biosolids application alters the composition of soil microbial groups and nutrient status in a pine plantation. Biol Fertil Soils 53:799–809

    CAS  Google Scholar 

  • Xiao W, Chen X, Jing X, Zhu B (2018) A meta-analysis of soil extracellular enzyme activities in response to global change. Soil Biol Biochem 123:21–32

    CAS  Google Scholar 

  • Xu W, Yuan W (2017) Responses of microbial biomass carbon and nitrogen to experimental warming: a meta-analysis. Soil Biol Biochem 115:265–274

    CAS  Google Scholar 

  • Yang X, Post WM (2011) Phosphorus transformations as a function of pedogenesis: a synthesis of soil phosphorus data using Hedley fractionation method. Biogeosciences 8:2907–2916

    CAS  Google Scholar 

  • Yang X, Thornton PE, Ricciuto DM, Post WM (2014) The role of phosphorus dynamics in tropical forests – a modeling study using CLM-CNP. Biogeosciences 11:1667–1681

    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

    CAS  Google Scholar 

  • Zhu J, Li M, Whelan M (2018) Phosphorus activators contribute to legacy phosphorus availability in agricultural soils: a review. Sci Total Environ 612:522–537

    CAS  PubMed  Google Scholar 

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Acknowledgements

This study was supported by the National “973” Program of China (grant number 2014CB954003), the National Natural Science Foundation of China (grant number 31300523, 31600433, 31130013) and Natural Science Foundation of Fujian Province (2019R11010010-6).

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Correspondence to Yiqing Li.

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Yang, L., Yang, Z., Peng, Y. et al. Evaluating P availability influenced by warming and N deposition in a subtropical forest soil: a bioassay mesocosm experiment. Plant Soil 444, 87–99 (2019). https://doi.org/10.1007/s11104-019-04246-z

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