Abstract
Purpose
Grasslands are the most extensive vegetation type in the terrestrial ecosystem and have an important role in the soil phosphorus (P) cycle. Many nutrient addition and warming experiments have been conducted in grasslands; however, the global pattern of nutrient addition and experimental warming impacts on soil P cycle is unclear.
Methods
We conducted a meta-analysis of 68 publications to synthesize the mechanisms underlying global grassland ecosystem responses to nutrient addition and experimental warming.
Results
Our analysis indicated that nitrogen (N) addition reduced microbial biomass P (− 11.2%) but increased litter P concentration (+ 15.5%) and available P (+ 14.2%). Experimental warming reduced microbial biomass P (− 10.5%) and available P (− 6.7%) but increased litter P concentration (+ 46.2%). P addition increased available P (+ 222.3%) and microbial biomass P (+ 98.1%). The available P response to nutrient addition and experimental warming was more sensitive in temperate grasslands than in alpine grasslands. The responses of soil total and available P to nutrient addition depended on environmental conditions such as air temperature and soil pH.
Conclusion
Our results suggest that N addition may promote P mineralization and possibly stimulate the transformation of refractory or resistant forms of soil inorganic P, whereas experimental warming accelerates the P cycle by regulating plant acquisition and enzyme activity. Environmental factors (e.g., temperature, precipitation, pH) affect the soil P response to nutrient addition by altering microbial and enzymatic activities. It is crucial to understand the dynamic changes in soil microbial and enzyme activities to predict the P cycle in grassland soils in the future.
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References
Alster CJ, German DP, Lu Y, Allison SD (2013) Microbial enzymatic responses to drought and to nitrogen addition in a southern California grassland. Soil Biol Biochem 64:68–79. https://doi.org/10.1016/j.soilbio.2013.03.034
Atere CT, Ge T, Zhu Z, Liu S, Huang X, Shibsitova O, Guggenberger G, Wu J (2018) Assimilate allocation by rice and carbon stabilisation in soil: effect of water management and phosphorus fertilisation. Plant Soil 445:153–167. https://doi.org/10.1007/s11104-018-03905-x
Bell TH, Klironomos JN, Henry HAL (2010) Seasonal responses of extracellular enzyme activity and microbial biomass to warming and nitrogen addition. Soil Sci Soc Am J 74:820–828. https://doi.org/10.2136/sssaj2009.0036
Bittman S, Sheppard SC, Poon D, Hunt DE (2017) Phosphorus flows in a peri-urban region with intensive food production: a case study. J Environ Manage 187:286–297. https://doi.org/10.1016/j.jenvman.2016.11.040
Brucker E, Spohn M (2019) Formation of soil phosphorus fractions along a climate and vegetation gradient in the Coastal Cordillera of Chile. CATENA 180:203–211. https://doi.org/10.1016/j.catena.2019.04.022
Buttler A, Mariotte P, Meisser M, Guillaume T, Signarbieux C, Vitra A, Preux S, Mercier G, Quezada J, Bragazza L, Gavazov K (2019) Drought-induced decline of productivity in the dominant grassland species Lolium perenne L. depends on soil type and prevailing climatic conditions. Soil Biol Biochem 132:47–57. https://doi.org/10.1016/j.soilbio.2019.01.026
Chen CR, Condron LM, Davis MR, Sherlock RR (2003) Seasonal changes in soil phosphorus and associated microbial properties under adjacent grassland and forest in New Zealand. For Ecol Manage 177:539–557. Pii S0378–1127(02)00450–4
Chen L, Deng Q, Yuan Z, Mu X, Kallenbach RL (2018) Age-related C:N: P stoichiometry in two plantation forests in the Loess Plateau of China. Ecol Eng 120:14–22. https://doi.org/10.1016/j.ecoleng.2018.05.021
Chen Q, Yuan Y, Hu Y, Wang J, Si G, Xu R, Zhou J, Xi C, Hu A, Zhang G (2021) Excessive nitrogen addition accelerates N assimilation and P utilization by enhancing organic carbon decomposition in a Tibetan alpine steppe. Sci Total Environ 764:142848. https://doi.org/10.1016/j.scitotenv.2020.142848
Chen X, Hao BH, Jing X, He JS, Ma WH, Zhu B (2019) Minor responses of soil microbial biomass, community structure and enzyme activities to nitrogen and phosphorus addition in three grassland ecosystems. Plant Soil 444:21–37. https://doi.org/10.1007/s11104-019-04250-3
D’Alo F, Odriozola I, Baldrian P, Zucconi L, Ripa C, Cannone N, Malfasi F, Brancaleoni L, Onofri S (2021) Microbial activity in alpine soils under climate change. Sci Total Environ 783:147012. https://doi.org/10.1016/j.scitotenv.2021.147012
Dalling JW, Heineman K, Lopez OR, Wright SJ, and Turner BL (2016) Nutrient availability in tropical rain forests: the paradigm of phosphorus limitation. Pages 261–273 in G. Goldstein and L. S. Santiago, editors. Tropical Tree Physiology: Adaptations and Responses in a Changing Environment
De Schrijver A, Vesterdal L, Hansen K, De Frenne P, Augusto L, Achat DL, Staelens J, Baeten L, De Keersmaeker L, De Neve S, Verheyen K (2012) Four decades of post-agricultural forest development have caused major redistributions of soil phosphorus fractions. Oecologia 169:221–234. https://doi.org/10.1007/s00442-011-2185-8
DeForest JL, Moorhead DL (2020) Effects of elevated pH and phosphorus fertilizer on soil C, N and P enzyme stoichiometry in an acidic mixed mesophytic deciduous forest. Soil Biol Biochem 150:107996. https://doi.org/10.1016/j.soilbio.2020.107996
Demoling F, Ola Nilsson L, Bååth E (2008) Bacterial and fungal response to nitrogen fertilization in three coniferous forest soils. Soil Biol Biochem 40:370–379. https://doi.org/10.1016/j.soilbio.2007.08.019
Dietrich K, Spohn M, Villamagua M, Oelmann Y (2017) Nutrient addition affects net and gross mineralization of phosphorus in the organic layer of a tropical montane forest. Biogeochemistry 136:223–236. https://doi.org/10.1007/s10533-017-0392-z
Duval S, Tweedie R (2000) A nonparametric “trim and fill” method of accounting for publication bias in meta-analysis. J Am Stat Assoc 95:89–98. https://doi.org/10.2307/2669529
Eckmeier E, Gerlach R, Gehrt E, Schmidt MWI (2007) Pedogenesis of Chernozems in Central Europe—a review. Geoderma 139:288–299. https://doi.org/10.1016/j.geoderma.2007.01.009
Egger M, Smith GD, Schneider M, Minder C (1997) Bias in meta-analysis detected by a simple, graphical test. Bmj-British Medical Journal 315:629–634. https://doi.org/10.1136/bmj.315.7109.629
Elser J, Bennett E (2011) A broken biogeochemical cycle. Nature 478:29–31. https://doi.org/10.1038/478029a
Elser J, 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 10:1135–1142. https://doi.org/10.1111/j.1461-0248.2007.01113.x
Fanin N, Mooshammer M, Sauvadet M, Meng C, Alvarez G, Bernard L, Bertrand I, Blagodatskaya E, Bon L, Fontaine S, Niu SL, Lashermes G, Maxwell TL, Weintraub MN, Wingate L, Moorhead D, Nottingham AT (2022) Soil enzymes in response to climate warming: Mechanisms and feedbacks. Funct Ecol. https://doi.org/10.1111/1365-2435.14027
Filippelli GM (2008) The global phosphorus cycle: Past, present, and future. Elements 4:89–95. https://doi.org/10.2113/Gselements.4.2.89
García-Velázquez L, Rodríguez A, Gallardo A, Maestre FT, Dos Santos E, Lafuente A, Fernández-Alonso MJ, Singh BK, Wang JT, Durán J, Wang F (2020) Climate and soil micro-organisms drive soil phosphorus fractions in coastal dune systems. Funct Ecol 34:1690–1701. https://doi.org/10.1111/1365-2435.13606
Ghiloufi W, Chaieb M (2021) Environmental factors controlling vegetation attributes, soil nutrients and hydrolases in South Mediterranean arid grasslands. Ecol Eng. https://doi.org/10.1016/j.ecoleng.2021.106155
Gong SW, Zhang T, Guo J (2020) Warming and nitrogen deposition accelerate soil phosphorus cycling in a temperate meadow ecosystem. Soil Res 58:109–115. https://doi.org/10.1071/sr19114
Guo R, Zhou J, Zhong X, Gu F, Liu Q, Li H (2019) Effect of simulated warming on the functional traits of Leymus chinensis plant in Songnen grassland. AoB Plants 11, plz073. https://doi.org/10.1093/aobpla/plz073
Hedges LV, Gurevitch J, Curtis PS (1999) The meta-analysis of response ratios in experimental ecology. Ecology 80:1150–1156. https://doi.org/10.2307/177062
IPCC (2018) Global warming of 1.5°C: An IPCC special report on the impacts of global warming of 1.5°C above pre-industrial levels and related global greenhouse gas emission pathways, in the context of strengthening the global response to the threat of climate change, sustainable development, and efforts to eradicate poverty, V. Masson-Delmotte et al., Eds. (World Meteorological Organization, Geneva, 2018)
Khorshid MSH, Kruse J, Semella S, Vohland M, Wagner J-F, Thiele-Bruhn S (2019) Phosphorus fractions and speciation in rural and urban calcareous soils in the semi-arid region of Sulaimani city, Kurdistan. Iraq Environ Earth Sci 78:531. https://doi.org/10.1007/s12665-019-8543-2
Li JH, Cheng BH, Zhang R, Li WJ, Shi XM, Han YW, Ye LF, Ostle NJ, Bardgett RD (2020) Nitrogen and phosphorus additions accelerate decomposition of slow carbon pool and lower total soil organic carbon pool in alpine meadows. Land Degrad Dev 32:1761–1772. https://doi.org/10.1002/ldr.3824
Liu H, Wang R, Wang H, Cao Y, Dijkstra FA, Shi Z, Cai J, Wang Z, Zou H, Jiang Y (2019) Exogenous phosphorus compounds interact with nitrogen availability to regulate dynamics of soil inorganic phosphorus fractions in a meadow steppe. Biogeosciences 16:4293–4306. https://doi.org/10.5194/bg-16-4293-2019
Liu Y, Bing H, Wu Y, Zhu H, Tian X, Wang Z, Chang R (2021) Nitrogen addition promotes soil phosphorus availability in the subalpine forest of eastern Tibetan Plateau. J Soils Sed. https://doi.org/10.1007/s11368-021-03064-0
Menge DNL, Field CB (2007) Simulated global changes alter phosphorus demand in annual grassland. Global Change Biol 13:2582–2591. https://doi.org/10.1111/j.1365-2486.2007.01456.x
Möhl P, Mörsdorf MA, Dawes MA, Hagedorn F, Bebi P, Viglietti D, Freppaz M, Wipf S, Körner C, Thomas FM, Rixen C, Gilliam F (2019) Twelve years of low nutrient input stimulates growth of trees and dwarf shrubs in the treeline ecotone. J Ecol 107:768–780. https://doi.org/10.1111/1365-2745.13073
Moreno SG, Sutton AJ, Ades AE, Stanley TD, Abrams KR, Peters JL, Cooper NJ (2009) Assessment of regression-based methods to adjust for publication bias through a comprehensive simulation study. BMC Med Res Methodol. https://doi.org/10.1186/1471-2288-9-2
Obermeier WA, Lehnert LW, Kammann CI, Müller C, Grünhage L, Luterbacher J, Erbs M, Moser G, Seibert R, Yuan N, Bendix J (2016) Reduced CO2 fertilization effect in temperate C3 grasslands under more extreme weather conditions. Nat Clim Chang 7:137–141. https://doi.org/10.1038/nclimate3191
Olander LP, Vitousek PM (2000) Regulation of soil phosphatase and chitinase activity by N and P availability. Biogeochemistry 49:175–190. https://doi.org/10.1023/a:1006316117817
Rinnan R, Michelsen A, Jonasson S (2008) Effects of litter addition and warming on soil carbon, nutrient pools and microbial communities in a subarctic heath ecosystem. Appl Soil Ecol 39:271–281. https://doi.org/10.1016/j.apsoil.2007.12.014
Rojas-Briales E (2015) Sparing grasslands: FAO’s active role. Science 347:1211–1211. https://doi.org/10.1126/science.347.6227.1211
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. https://doi.org/10.1007/s11104-012-1132-8
Sardans J, Penuelas J, Estiarte M (2006) Warming and drought alter soil phosphatase activity and soil P availability in a Mediterranean shrubland. Plant Soil 289:227–238. https://doi.org/10.1007/s11104-006-9131-2
Sattari SZ, Bouwman AF, Martinez Rodriguez R, Beusen AH, van Ittersum MK (2016) Negative global phosphorus budgets challenge sustainable intensification of grasslands. Nat Commun 7:10696. https://doi.org/10.1038/ncomms10696
Seabloom EW, Adler PB, Alberti J, Biederman L, Buckley YM, Cadotte MW, Collins SL, Dee L, Fay PA, Firn J, Hagenah N, Harpole WS, Hautier Y, Hector A, Hobbie SE, Isbell F, Knops JMH, Komatsu KJ, Laungani R, MacDougall A, McCulley RL, Moore JL, Morgan JW, Ohlert T, Prober SM, Risch AC, Schuetz M, Stevens CJ, Borer ET (2021) Increasing effects of chronic nutrient enrichment on plant diversity loss and ecosystem productivity over time. Ecology 102:e03218. https://doi.org/10.1002/ecy.3218
Sharma AK, Muhlroth A, Jouhet J, Marechal E, Alipanah L, Kissen R, Brembu T, Bones AM, Winge P (2020) The Myb-like transcription factor phosphorus starvation response (PtPSR) controls conditional P acquisition and remodelling in marine microalgae. New Phytol 225:2380–2395. https://doi.org/10.1111/nph.16248
Shi J, Gong J, Baoyin T, Luo Q, Zhai Z, Zhu C, Yang B, Wang B, Zhang Z, Li X (2021) Short-term phosphorus addition increases soil respiration by promoting gross ecosystem production and litter decomposition in a typical temperate grassland in northern China. CATENA 197:104952. https://doi.org/10.1016/j.catena.2020.104952
Siebers N, Kruse J (2019) Short-term impacts of forest clear-cut on soil structure and consequences for organic matter composition and nutrient speciation: A case study. PLoS ONE 14:e0220476. https://doi.org/10.1371/journal.pone.0220476
Singh BK, Bardgett RD, Smith P, Reay DS (2010) Microorganisms and climate change: terrestrial feedbacks and mitigation options. Nat Rev Microbiol 8:779–790. https://doi.org/10.1038/nrmicro2439
Stanley TD, Doucouliagos H (2014) Meta-regression approximations to reduce publication selection bias. Research Synthesis Methods 5:60–78. https://doi.org/10.1002/jrsm.1095
Thakur MP, Del Real IM, Cesarz S, Steinauer K, Reich PB, Hobbie S, Ciobanu M, Rich R, Worm K, Eisenhauer N (2019) Soil microbial, nematode, and enzymatic responses to elevated CO2 N fertilization, warming, and reduced precipitation. Soil Biol Biochem 135:184–193. https://doi.org/10.1016/j.soilbio.2019.04.020
Vogl T, Hrdina A, Thomas CK (2021) Choosing an optimal beta factor for relaxed eddy accumulation applications across vegetated and non-vegetated surfaces. Biogeosciences 18:5097–5115. https://doi.org/10.5194/bg-18-5097-2021
Wang J, Gao Y, Zhang Y, Yang J, Smith MD, Knapp AK, Eissenstat DM, Han X (2019) Asymmetry in above- and belowground productivity responses to N addition in a semi-arid temperate steppe. Global Chang Biol 25:2958–2969. https://doi.org/10.1111/gcb.14719
Wang QK, Wang SL, Liu YX (2008) Responses to N and P fertilization in a young Eucalyptus dunnii plantation: Microbial properties, enzyme activities and dissolved organic matter. Appl Soil Ecol 40:484–490. https://doi.org/10.1016/j.apsoil.2008.07.003
Wang R, Liu H, Sardans J, Feng X, Xu Z, Peñuelas J (2020) Interacting effects of urea and water addition on soil mineral-bound phosphorus dynamics in semi-arid grasslands with different land-use history. Eur J Soil Sci 72:946–962. https://doi.org/10.1111/ejss.13046
White-Monsant AC, Clark GJ, Ng Kam Chuen MAG, Tang C (2017) Experimental warming and antecedent fire alter leaf element composition and increase soil C: N ratio in sub-alpine open heathland. Sci Total Environ 595:41–50. https://doi.org/10.1016/j.scitotenv.2017.03.237
Widdig M, Heintz-Buschart A, Schleuss P-M, Guhr A, Borer ET, Seabloom EW, Spohn M (2020) Effects of nitrogen and phosphorus addition on microbial community composition and element cycling in a grassland soil. Soil Biol Biochem 151:108041. https://doi.org/10.1016/j.soilbio.2020.108041
Widdig M, Schleuss P-M, Weig AR, Guhr A, Biederman LA, Borer ET, Crawley MJ, Kirkman KP, Seabloom EW, Wragg PD, Spohn M (2019) Nitrogen and phosphorus additions alter the abundance of phosphorus-solubilizing bacteria and phosphatase activity in grassland soils. Front Env Sci 7:185. https://doi.org/10.3389/fenvs.2019.00185
Yan C, Yuan Z, Liu Z, Zhang J, Liu K, Shi X, Lock TR, Kallenbach RL (2021) Aridity stimulates responses of root production and turnover to warming but suppresses the responses to nitrogen addition in temperate grasslands of northern China. Sci Total Environ 753:142018. https://doi.org/10.1016/j.scitotenv.2020.142018
Yan C, Yuan Z, Shi X, Lock TR, Kallenbach RL (2020) A global synthesis reveals more response sensitivity of soil carbon flux than pool to warming. J Soils Sed 20:1208–1221. https://doi.org/10.1007/s11368-019-02513-1
Yuan ZY, Chen HYH (2015) Decoupling of nitrogen and phosphorus in terrestrial plants associated with global changes. Nat Clim Chang 5:465–469. https://doi.org/10.1038/nclimate2549
Zhang Y, Hu L, Yu D, Xu K, Zhang J, Li X, Wang P, Chen G, Liu Z, Peng C, Li C, Guo T (2019) Integrative analysis of the wheat pht1 gene family reveals a novel member involved in arbuscular mycorrhizal phosphate transport and immunity. Cells 8:490. https://doi.org/10.3390/cells8050490
Zhao ML, Wang M, Zhao YT, Wang GD, Xue ZS, Jiang M (2021) Variations in soil microbial communities in the sedge-dominated peatlands along an altitude gradient on the northern slope of Changbai Mountain. China Ecol Indicators. https://doi.org/10.1016/j.ecolind.2021.107964
Acknowledgements
This study was supported by the National Key Research and Development Program of China (2016YFA0600801), the Hundred Talents Program of Shaanxi Province (A289021701), the Natural Science Basic Research Plan in Shaanxi Province of China (2018JZ3002), the Special Fund from the State Key Laboratory of Soil Erosion and Dryland Farming on the Loess Plateau (A314021403-C9), and the Double First Class University Plan of NWSUAF (Z102021829). The funders had no role in the study design, data collection, data analysis, decision to publish, or preparation of the manuscript.
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Hu, W., Tan, J., Shi, X. et al. Nutrient addition and warming alter the soil phosphorus cycle in grasslands: A global meta-analysis. J Soils Sediments 22, 2608–2619 (2022). https://doi.org/10.1007/s11368-022-03276-y
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DOI: https://doi.org/10.1007/s11368-022-03276-y