Phosphorus is an essential element for plant metabolism and growth, but its future supply under elevated levels of atmospheric CO2 remains uncertain. Here we present measurements of phosphorus concentration from two long-term (15 and 9 years) rice free air carbon dioxide enrichment experiments. Although no changes were observed in the initial year of the experiments, by the end of the experiments soil available phosphorus had declined by more than 20% (26.9% and 21.0% for 15 and 9 years, respectively). We suggest that the reduction can be explained by the production of soil organic phosphorus that is not in a readily plant-available form, as well as by increased removal through crop harvest. Our findings further suggest that increased transfers of plant available phosphorus from biological, biochemical and chemical phosphorus under anthropogenic changes are insufficient to compensate for reductions to plant available phosphorus under long-term exposure to elevated CO2. We estimate that reductions to rice yields could be particularly acute in low-income countries under future CO2 scenarios without the input of additional phosphorus fertilizers to compensate, despite the potentially reduced global risk for phosphorus pollution.
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The data supporting the findings of this study are available within the Article and the Supplementary Information, and we have deposited the global dataset in the figshare repository (https://doi.org/10.6084/m9.figshare.21103078.v2 ref. 64). Global rice yield data of the 14 main rice-planting countries can be accessed from FAOSATA (http://faostat.fao.org/default.aspx, 2019). Global rice harvest area data for extracting global rice pixels are available from https://www.mapspam.info/data/. Global soil P pools and P budgets can be accessed at https://esdac.jrc.ec.europa.eu/content/global-phosphorus-losses-due-soil-erosion.
Wang, S. H. et al. Recent global decline of CO2 fertilization effects on vegetation photosynthesis. Science 370, 1295–1300 (2020).
Ainsworth, E. A. & Long, S. P. 30 years of free-air carbon dioxide enrichment (FACE): what have we learned about future crop productivity and its potential for adaptation? Glob. Change Biol. 27, 27–49 (2021).
Kimball, B. A. Crop responses to elevated CO2 and interactions with H2O, N and temperature. Curr. Opin. Plant Biol. 31, 36–43 (2016).
Kim, H. Y. et al. Effects of free-air CO2 enrichment and nitrogen supply on the yield of temperate paddy rice crops. Field Crops Res. 83, 261–270 (2003).
Shimono, H. et al. Rice yield enhancement by elevated CO2 is reduced in cool weather. Glob. Change Biol. 14, 276–284 (2008).
Shimono, H. et al. Genotypic variation in rice yield enhancement by elevated CO2 relates to growth before heading, and not to maturity group. J. Exp. Bot. 60, 523–532 (2009).
Luo, Y. et al. Progressive nitrogen limitation of ecosystem responses to rising atmospheric carbon dioxide. Bioscience 54, 731–739 (2004).
Reich, P. B. & Hobbie, S. E. Decade-long soil nitrogen constraint on the CO2 fertilization of plant biomass. Nat. Clim. Change 3, 278–282 (2013).
Ellsworth, D. S. et al. Convergence in phosphorus constraints to photosynthesis in forests around the world. Nat. Commun. 13, 5005 (2022).
Brooks, A., Woo, K. C. & Wong, S. C. Effects of phosphorus-nutrition on the response of photosynthesis to CO2 and O2, activation of ribulose bisphosphate carboxylase and amounts of ribulose bisphosphate and 3-phosphoglycerate in spinach leaves. Photosynth. Res. 15, 133–141 (1988).
Jin, J., Tang, C. X. & Sale, P. The impact of elevated carbon dioxide on the phosphorus nutrition of plants: a review. Ann. Bot. 116, 987–999 (2015).
Jin, J. et al. Increased microbial activity contributes to phosphorus immobilization in the rhizosphere of wheat under elevated CO2. Soil Biol. Biochem. 75, 292–299 (2014).
Drissner, D., Blum, H., Tscherko, D. & Kandeler, E. Nine years of enriched CO2 changes the function and structural diversity of soil microorganisms in a grassland. Eur. J. Soil Sci. 58, 260–269 (2007).
He, X. J. et al. Global patterns and drivers of soil total phosphorus concentration. Earth Syst. Sci. Data 13, 5831–5846 (2021).
MacDonald, G. K., Bennett, E. M., Potter, P. A. & Ramankutty, N. Agronomic phosphorus imbalances across the world’s croplands. Proc. Natl Acad. Sci. USA 108, 3086–3091 (2011).
Brownlie, W. J. et al. Global actions for a sustainable phosphorus future. Nat. Food 2, 71–74 (2021).
Alewell, C. et al. Global phosphorus shortage will be aggravated by soil erosion. Nat. Commun. 11, 4546 (2020).
Penuelas, J. & Sardans, J. The global nitrogen-phosphorus imbalance. Science 375, 266–267 (2022).
Obersteiner, M., Penuelas, J., Ciais, P., van der Velde, M. & Janssens, I. A. The phosphorus trilemma. Nat. Geosci. 6, 897–898 (2013).
Kogel-Knabner, I. et al. Biogeochemistry of paddy soils. Geoderma 157, 1–14 (2010).
Dong, J. W. & Xiao, X. M. Evolution of regional to global paddy rice mapping methods: a review. ISPRS J. Photogramm. Remote Sens. 119, 214–227 (2016).
Fu, J. et al. Nationwide estimates of nitrogen and phosphorus losses via runoff from rice paddies using data-constrained model simulations. J. Clean. Prod. 279, 123642 (2021).
O’Sullivan, J. B., Jin, J. & Tang, C. X. Elevated CO2 promotes the acquisition of phosphorus in crop species differing in physiological phosphorus-acquiring mechanisms. Plant Soil 455, 397–408 (2020).
Wang, J. Y. et al. Response of rice production to elevated CO2 and its interaction with rising temperature or nitrogen supply: a meta-analysis. Clim. Change 130, 529–543 (2015).
Jin, J., Armstrong, R. & Tang, C. X. Long-term impact of elevated CO2 on phosphorus fractions varies in three contrasting cropping soils. Plant Soil 419, 257–267 (2017).
Jin, J., Tang, C. X., Armstrong, R., Butterly, C. & Sale, P. Elevated CO2 temporally enhances phosphorus immobilization in the rhizosphere of wheat and chickpea. Plant Soil 368, 315–328 (2013).
Jin, J., Tang, C. X., Armstrong, R. & Sale, P. Phosphorus supply enhances the response of legumes to elevated CO2 (FACE) in a phosphorus-deficient vertisol. Plant Soil 358, 86–99 (2012).
Tiessen, H. & Moir, J. O. in Soil Sampling and Methods of Analysis (ed. Carter, M. R.) 75–86 (Lewis Publishers, 1993).
Helfenstein, J. et al. Combining spectroscopic and isotopic techniques gives a dynamic view of phosphorus cycling in soil. Nat. Commun. 9, 3226 (2018).
Hasegawa, T. et al. Rice cultivar responses to elevated CO2 at two free-air CO2 enrichment (FACE) sites in Japan. Funct. Plant Biol. 40, 148–159 (2013).
Liu, X. et al. Intensification of phosphorus cycling in China since the 1600s. Proc. Natl Acad. Sci. USA 113, 2609–2614 (2016).
Hu, M. P. et al. Long-term (1980–2015) changes in net anthropogenic phosphorus inputs and riverine phosphorus export in the Yangtze River basin. Water Res. 177, 115779 (2020).
Yang, L. X. et al. Seasonal changes in the effects of free-air CO2 enrichment (FACE) on growth, morphology and physiology of rice root at three levels of nitrogen fertilization. Glob. Change Biol. 14, 1844–1853 (2008).
BassiriRad, H., Gutschick, V. P. & Lussenhop, J. Root system adjustments: regulation of plant nutrient uptake and growth responses to elevated CO2. Oecologia 126, 305–320 (2001).
Gamper, H. et al. Arbuscular mycorrhizal fungi benefit from 7 years of free air CO2 enrichment in well-fertilized grass and legume monocultures. Glob. Change Biol. 10, 189–199 (2004).
Huang, W. J. et al. Shifts in soil phosphorus fractions under elevated CO2 and N addition in model forest ecosystems in subtropical China. Plant Ecol. 215, 1373–1384 (2014).
Khan, F. N., Lukac, M., Turner, G. & Godbold, D. L. Elevated atmospheric CO2 changes phosphorus fractions in soils under a short rotation poplar plantation (EuroFACE). Soil Biol. Biochem. 40, 1716–1723 (2008).
Hasegawa, S., Macdonald, C. A. & Power, S. A. Elevated carbon dioxide increases soil nitrogen and phosphorus availability in a phosphorus-limited Eucalyptus woodland. Glob. Change Biol. 22, 1628–1643 (2016).
Li, H. et al. Integrated soil and plant phosphorus management for crop and environment in China. A review. Plant Soil 349, 157–167 (2011).
Wang, Y. et al. Response of soil microbes to a reduction in phosphorus fertilizer in rice-wheat rotation paddy soils with varying soil P levels. Soil Res. 181, 127–135 (2018).
Zhang, W. F. et al. Efficiency, economics and environmental implications of phosphorus resource use and the fertilizer industry in China. Nutr. Cycl. Agroecosyst. 80, 131–144 (2008).
Hesketh, N. & Brookes, P. C. Development of an indicator for risk of phosphorus leaching. J. Environ. Qual. 29, 105–110 (2000).
Fortune, S., Lu, J., Addiscott, T. M. & Brookes, P. C. Assessment of phosphorus leaching losses from arable land. Plant Soil 269, 99–108 (2005).
Hamadeh, N., Rompaey, C. V. & Metreau, E. New World Bank country classifications by income level: 2021–2022. World Bank Blogs https://blogs.worldbank.org/opendata/new-world-bank-country-classifications-income-level-2021-2022 (2021).
Zhang, J. et al. Spatiotemporal dynamics of soil phosphorus and crop uptake in global cropland during the twentieth century. Biogeosciences 14, 2055–2068 (2017).
Mogollón, J. M., Beusen, A., Grinsven, H. V., Westhoek, H. & Bouwman, A. F. Future agricultural phosphorus demand according to the shared socioeconomic pathways. Glob. Environ. Change 50, 149–163 (2018).
Campos, J. L. et al. Nitrogen and phosphorus recovery from anaerobically pretreated agro-food wastes: a review. Front. Sustain. Food Syst. 2, 91 (2019).
Mogollon, J. M. et al. More efficient phosphorus use can avoid cropland expansion. Nat. Food 2, 509–518 (2021).
Okada, M. et al. Free-air CO2 enrichment (FACE) using pure CO2 injection: system description. N. Phytol. 150, 251–260 (2001).
Zhu, C. W. et al. The temporal and species dynamics of photosynthetic acclimation in flag leaves of rice (Oryza sativa) and wheat (Triticum aestivum) under elevated carbon dioxide. Physiol. Plant. 145, 395–405 (2012).
Cai, C. et al. Responses of wheat and rice to factorial combinations of ambient and elevated CO2 and temperature in FACE experiments. Glob. Change Biol. 22, 856–874 (2016).
Nagumo, T., Tajima, S., Chikushi, S. & Yamashita, A. Phosphorus balance and soil phosphorus status in paddy rice fields with various fertilizer practices. Plant Prod. Sci. 16, 69–76 (2013).
Kovar, J. L. & Pierzynski, G. M. (eds) Methods of Phosphorus Analysis for Soils, Sediments, Residuals and Waters 2nd edn (North Carolina State Univ., 2009).
Hedley, M. J. & Stewart, J. W. B. Method to measure microbial phosphate in soils. Soil Biol. Biochem. 14, 377–385 (1982).
Lu, R. K. The Analysis Method of Soil Agro-Chemistry (Chinese Agricultural Academic Press, 2000).
Li, W. et al. Characterizing phosphorus speciation of Chesapeake Bay sediments using chemical extraction, 31P NMR, and X-ray absorption fine structure spectroscopy. Environ. Sci. Technol. 49, 203–211 (2015).
Chen, S. et al. The influence of long-term N and P fertilization on soil P forms and cycling in a wheat/fallow cropping system. Geoderma 404, 115274 (2021).
Cade-Menun, B. J. Characterizing phosphorus in environmental and agricultural samples by 31P nuclear magnetic resonance spectroscopy. Talanta 66, 359–371 (2005).
Frostegard, A., Tunlid, A. & Baath, E. Phospholipid fatty acid composition, biomass, and activity of microbial communities from two soil types experimentally exposed to different heavy metals. Appl. Environ. Microbiol. 59, 3605–3617 (1993).
Alef, K. & Nannipieri, P. (eds) Methods in Applied Soil Microbiology and Biochemistry (Academic Press, 1995).
Ringeval, B. et al. Phosphorus in agricultural soils: drivers of its distribution at the global scale. Glob. Change Biol. 23, 3418–3432 (2017).
Pariasca-Tanaka, J. et al. Does reducing seed-P concentrations affect seedling vigor and grain yield of rice? Plant Soil 392, 253–266 (2015).
European Soil Data Centre (ESDAC, European Commission, Joint Research Centre); esdac.jrc.ec.europa.eu
Song, L. Source data for MS: reduced phosphorus availability in paddy soils under atmospheric CO2 enrichment. figshare https://doi.org/10.6084/m9.figshare.21103078.v2 (2022).
Song, L. MS_NG_CFE reduced soil P availability. figshare https://doi.org/10.6084/m9.figshare.21098458.v2 (2022).
Yang, L. X. et al. Seasonal changes in the effects of free-air CO2 enrichment (FACE) on dry matter production and distribution of rice (Oryza sativa L.). Field Crops Res. 98, 12–19 (2006).
Liu, H. J. et al. Yield formation of CO2-enriched hybrid rice cultivar Shanyou 63 under fully open-air field conditions. Field Crops Res. 108, 93–100 (2008).
Fan, G. Z. et al. Yield components and its conformation responded to elevated atmospheric CO2 in three rice (Oryza sativa L.) generations. Afr. J. Biotechnol. 9, 2118–2124 (2010).
Zhu, C. W. et al. Biochemical and molecular characteristics of leaf photosynthesis and relative seed yield of two contrasting rice cultivars in response to elevated CO2. J. Exp. Bot. 65, 6049–6056 (2014).
Lai, S. K. et al. Effects of CO2 concentration, nitrogen supply and transplanting density on yield formation of hybrid rice Shanyou 63: a FACE study. J. Agro Environ. Sci. 33, 836–843 (2014).
Wang, W. L. et al. Elevated CO2 cannot compensate for japonica grain yield losses under increasing air temperature because of the decrease in spikelet density. Eur. J. Agron. 99, 21–29 (2018).
Zhang, G. Y. et al. Grain growth of different rice cultivars under elevated CO2 concentrations affects yield and quality. Field Crops Res. 179, 72–80 (2015).
Hasegawa, T. et al. A High-yielding rice cultivar ‘Takanari’ shows no N constraints on CO2 fertilization. Front Plant Sci. 10, 15 (2019).
Lieffering, M., Kim, H. Y., Kobayashi, K. & Okada, M. The impact of elevated CO2 on the elemental concentrations of field grown rice grains. Field Crops Res. 88, 279–286 (2004).
Wang, J. Q. et al. Changes in nutrient uptake and utilization by rice under simulated climate change conditions: A 2-year experiment in a paddy field. Agr. For. Meteorol. 250, 202–208 (2018).
He, S. D. Studies on Phosphorus Fractions and Phosphate Sorption Desorption Characteristics of Paddy Soils [D]. Zhejiang Univ. (2008).
Wang, Y. Z. Effect of Phosphorus Fertilization on Soil Phosphorus Fraction, Distribution and Dynamics [D]. Univ. Chinese Academy of Sciences (2015).
Waqas, A. Effect of Long-term Fertilization and Tillage Management on Soil Phosphorus Fractions under Paddy Cultivation in Different Agroclimatic Regions of China [D]. Chinese Academy of Agricultural Sciences (2019).
Li, L. Speciation, Microbial Enzymatic Conversion and Activation of Legacy Phosphorus in Paddy Soils [D]. Zhejiang Univ. (2014).
Wang, X. Effects of Earthworms on Soil Nitrogen and Phosphorus in Upland Rice-Wheat Rotation Agroecosystem [D]. Nanjing Agricultural Univ. (2005).
Wang, Y. et al. Soil phosphorus pool evolution and environmental risk prediction of paddy soil in the Taihu Lake Region. Acta Pedologica Sin. 59, 1640–1649 (2022) .
We acknowledge the enduring contributions of J. Zhu, who initiated and supervised study PL-M from 2004 to 2016, and G. Pan and X. Liu who established and supervised study PH from 2011. The FACE system instruments of study PL-M were supplied by the National Institute of Agro-Environmental Sciences and the Agricultural Research Center of Tohohu Region (Japan). We received funding from the Key-Area Research and Development Program of Guangdong Province, China (2020B0202010006 to C.Z.), the National Key Research and Development Program of China (2021YFD1700802 to Y.W.), the National Natural Science Foundation of China (42277026 to Y.W., 31870423 to C.Z. and 32001191 to L.S.), the Chinese Academy of Sciences ‘0-1’ program (ZDBS-LY-DQC020 to C.Z.), the Jiangsu Science and Technology Department (BM2022002 to C.Z.), Innovation Program of Institute of Soil Science (ISSASIP2201 to Y.W.), a Spanish Government grant (PID2019-110521GB-I00 to J.P.), French state aid managed by the ANR under the ‘Investissements d’avenir’ programme (ANR16-CONV-0003 to P.C.), and the Carbon Peaking and Carbon Neutrality Special Fund for Science and Technology from Nanjing Science and Technology Bureau (20221103 to C.Z.).
The authors declare no competing interests.
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Extended Data Fig. 1 Variations of soil P factions under eCO2 and aCO2 in two China Rice FACE experiments.
The samples were collected at the rice harvest stage in agroecosystem with low-moderate P (PL-M) in 2004, 2009, 2015 and 2018, respectively. The high P (PH) agroecosystem samples were collected at the rice harvest stage in 2019. Data are means ± standard deviation (n = 3). PL-M and PH were initiated in 2004 and 2011, respectively. Statistical test results are provided in Table 1 and Supplementary Table 2.
Extended Data Fig. 2 Variations of 31P NMR spectra under elevated atmospheric CO2 (eCO2) in comparison with ambient CO2 (aCO2) concentrations in two China Rice FACE experiments.
a. b, 31P solid-state NMR spectra in 2018 (PL-M) and 2019 (PH) at the 0-10 cm soil layer. The peak at 2.6 ppm is indicative of apatite (Ca − P mineral, primary mineral P). c. d, 31P liquid-state NMR spectra in 2018 (PL-M) and 2019 (PH) at the 0-10 cm soil layer. The 31P NMR chemical shifts suggest the presence of orthophosphate (6 ppm), phosphate monoesters (4-5 ppm), phospholipids (1-2.5 ppm), DNA (-1 ppm), and pyrophosphate (-4 to -5 ppm); Pi in d refers to the sum of inorganic ortho-P and pyrophosphate, Po refers to the sum of phosphate monoesters and diester (mainly DNA-P). PL-M and PH were initiated in 2004 and 2011, respectively.
Extended Data Fig. 3 Straw biomass, grain yield, straw P content and grain P content under aCO2 and eCO2 in two rice FACE experiments.
Data were collected in 2018 from a low-moderate P (PL-M) agroecosystem, and in 2019 from a high P (PH) agroecosystem. Data are means ± standard deviation (n = 3). Asterisks denote the results of ANOVA and Tukey tests, and indicate significant differences between means at p < 0.05.
Extended Data Fig. 5 In-situ images of rice roots at the heading stage in agroecosystems in high available P experiment.
The image on the left is for the aCO2 treatment, and the image on the right is for the eCO2 treatment. Data are means ± standard deviation (n = 3). Asterisks denote the results of ANOVA and Tukey tests, and indicate significant differences between means at p < 0.05.
Extended Data Fig. 6 Relationships between soil P fractions and microbial properties (Pearson correlation coefficients, r) under aCO2 and eCO2 in 2018 (PL-M) and 2019 (PH).
The values of p denote the results of ANOVA and Tukey tests, and described the significance for p < 0.05, p < 0.01, and p < 0.001. Soil available P, the sum of resin-P and NaHCO3-Pi; Secondary mineral P, NaOH-Pi; Primary mineral P, HCl-Pi; Organic P, the sum of NaHCO3-Po and NaOH-Po; Occluded P, residual P. Soil microbial properties include bacterial biomass (B), fungal biomass (F), the ratio of fungal to bacteria biomass (F:B ratio), biomass of arbuscular mycorrhizal fungi (AMF), and the activities of acid phosphatase (ACP), and alkaline phosphatase (ALP).
Extended Data Fig. 7 Soil available P under eCO2 relative to aCO2 in different systems based on new data from this study for farmland and the literature.
The values indicate the change (eCO2 - aCO2) for soil P pool sizes due to eCO2. Soil available P includes different indices including resin P, NaHCO3-Pi, and Olsen P (shown in Supplementary Table 1). The line and empty square in each box represent the median and mean, respectively. Whiskers mark the 10th and 90th percentiles, and the outliers are shown as dots. The number of experimental outcomes was defined as n.
a, Global distribution of yield reduction risk level (1: extremely low, 2: low, 3: medium, 4: high, 5: extremely high; see Methods). b, Global distribution of potential P pollution risk level (0: no risk, 1: with potential environment risk). Note the size of the squares does not represent the actual area of rice paddy fields in Panels a and b.
Extended Data Fig. 9 Bar plot of mean GDP per capita during 2010–2020 for 14 global rice grown countries according to the 2019 World Bank income classifications.
The error bar indicates the standard deviation of GDP per capita during 2010–2020, the horizontal red dash line indicates the threshold value for low-income and middle-high income countries, and the vertical red dash line indicates the grouping of low-income and middle-high countries. The IQR indicates the interquartile range.
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Wang, Y., Huang, Y., Song, L. et al. Reduced phosphorus availability in paddy soils under atmospheric CO2 enrichment. Nat. Geosci. (2023). https://doi.org/10.1038/s41561-022-01105-y