Annual warming does not affect methane emissions due to legacy effects of reduced carbon input in a rice-wheat cropping system

Abstract

Global warming is a central driver of climate change and is generally expected to increase methane (CH₄) emissions from rice paddies-a major source of this potent greenhouse gas (GHG). However, previous studies have primarily focused on warming during the rice-growing season, often overlooking the legacy effects of warming during wheat season on CH₄ emissions in the rice-wheat cropping system. Therefore, using a Free-Air Temperature Increase (FATI) experiment established in 2021, we assessed the impacts of annual warming on CH₄ emissions and rice yield in a rice-wheat cropping system in 2023 and 2024. Overall, annual warming had no significant effect on area-scaled CH₄ emissions, but reduced rice yields by 17.3-18.2%, leading to an increase in yield-scaled CH₄ emissions. Warming reduced the rate of wheat straw incorporation by 9.5% and lowered soil dissolved organic carbon (DOC) concentrations by 24.1% before rice transplanting. During the tillering stage, the peak period for CH₄ emissions, warming did not affect soil DOC concentrations, the abundance of methanogens or methanotrophs, CH₄ production potential, or CH₄ oxidation potential. These results suggest that the reduction in carbon input offset the warming-induced stimulation of CH₄ production. Our findings underscore that legacy effects of warming can modulate GHG emissions and highlight the need to consider annual warming effects in CH₄ emission estimates, as single-season assessments may overlook critical feedbacks of carbon input.

Keywords

Annual warming / Legacy effects / Methane emissions / Rice-wheat cropping system / Rice yield

Abbreviations

DOC, dissolved organic carbon;

FATI, Free-Air Temperature Increase;

GHG, greenhouse gas;

SOC, soil organic carbon.

Availability of data and materials

Data will be shared upon request by the readers.

Authors' contribution

Jiujie Liu: Writing-original draft, Methodology, Investigation, Formal analysis, Data curation, Conceptualization. Yunlong Liu: Methodology, Investigation, Data curation. Qianqian Yuan: Investigation. Ling Wang: Writing-review & editing, Data curation. Yong Wang: Investigation, Data curation. Taoyun Chen: Investigation. Haoyu Qian: Writing-review & editing, Supervision, Funding acquisition, Data curation, Conceptualization. Yanfeng Ding: Resources, Funding acquisition, Conceptualization. Yu Jiang: Writing-review & editing, Methodology, Investigation, Funding acquisition, Formal analysis, Data curation, Conceptualization.

Declaration of competing interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper. Authors Yanfeng Ding and Yu Jiang (Editorial Board members) were not involved in the journal's review nor decisions related to this manuscript.

Acknowledgements

This work was supported by the National Key R&D Program of China (2022YFD2300400), Fundamental Research Funds for the Central Universities of Nanjing Agricultural University (YDZX2025018), the National Natural Science Foundation of China (U24A20402, 32271635, 32301354), the Natural Science Foundation of Jiangsu Province (BK20230979), the Jiangsu Carbon Peak Carbon Neutrality Science and Technology Innovation Fund project (BE2022308), and the project of Double Thousand Plan of Jiangxi Province of China (jxsq2023102208).

Appendix A. Supplementary data

Supplementary data to this article can be found online at https://doi.org/10.1016/j.crope.2025.09.002.

References

[1] Bao T., Wang L., Huang Y., Li H., Qiu L., Liu J., Shi L., Liu Y., Qian H., Ding Y., Jiang Y., 2024. Elevated [CO₂] reduces CH₄ emissions from rice paddies under in situ straw incorporation. Agric. Ecosyst. Environ. 370, 109055.

[2] Bertora C., Cucu M.A., Lerda C., Peyron M., Bardi L., Gorra R., Sacco D., Celi L., Said-Pullicino D., 2018. Dissolved organic carbon cycling, methane emissions and related microbial populations in temperate rice paddies with contrasting straw and water management. Agric. Ecosyst. Environ. 265, 292-306.

[3] Cai C., Yin X., He S., Jiang W., Si C., Struik P.C., Luo W., Li G., Xie Y., Xiong Y., Pan G., 2016. Responses of wheat and rice to factorial combinations of ambient and elevated CO₂ and temperature in FACE experiments. Glob. Change Biol. 22, 856-874.

[4] Carlson K.M., Gerber J.S., Mueller N.D., Herrero M., MacDonald G.K., Brauman K.A., Havlik P., O'Connell C.S., Johnson J.A., Saatchi S., West P.C., 2017. Greenhouse gas emissions intensity of global croplands. Nat. Clim. Change 7, 63-68.

[5] Chen C., van Groenigen K.J., Yang H., Hungate B.A., Yang B., Tian Y., Chen J., Dong W., Huang S., Deng A., Jiang Y., Zhang W., 2020. Global warming and shifts in cropping systems together reduce China's rice production. Global Food Secur. 24, 100359.

[6] Chen Y., Li Z., Fan Y., Wang H., Deng H., 2015. Progress and prospects of climate change impacts on hydrology in the arid region of northwest China. Environ. Res. Environmental Research on Hydrology and Water Resources 139, 11-19.

[7] Cheng H., Ren W., Ding L., Liu Z., Fang C., 2013. Responses of a rice-wheat rotation agroecosystem to experimental warming. Ecol. Res. 28, 959-967.

[8] Conrad R., 2007. Microbial ecology of methanogens and methanotrophs. Adv. Agron 96, 1-63.

[9] Deng N., Grassini P., Yang H., Huang J., Cassman K.G., Peng S., 2019. Closing yield gaps for rice self-sufficiency in China. Nat. Commun. 10, 1725.

[10] Dheri G.S., Nazir G., 2021. A review on carbon pools and sequestration as influenced by long-term management practices in a rice-wheat cropping system. Carbon Manag. 12, 559-580.

[11] Espe M.B., Hill J.E., Hijmans R.J., McKenzie K., Mutters R., Espino L.A., Leinfelder-Miles M., van Kessel C., Linquist B.A., 2017. Point stresses during reproductive stage rather than warming seasonal temperature determine yield in temperate rice. Glob. Change Biol. 23, 4386-4395.

[12] Food and Agriculture Organization of the United Nations, 2019.FAOSTAT Production Data. https://www.fao.org/faostat/en/#data.

[13] Food and Agriculture Organization of the United Nations, 2023.Faostat-Food and Agriculture. https://www.fao.org/faostat/en/#home.

[14] Gao H., Tian H., Zhang Z., Xia X., 2022. Warming-induced greenhouse gas fluxes from global croplands modified by agricultural practices: a meta-analysis. Sci. Total Environ. 820, 153288.

[15] Gao T., Xie K., Hu Q., Wu C., Wang Z., Wang W., Xiong D., Huang J., Peng S., Cui K., 2025. Alternate wetting and drying irrigation at tillering stage enhances the heat tolerance of rice by increasing sucrose and cytokinin content in panicles. Front. Plant Sci. 16, 1598652.

[16] García-Palacios P., Crowther T.W., Dacal M., Hartley I.P., Reinsch S., Rinnan R., Rousk J., van den Hoogen J., Ye J.-S., Bradford M.A., 2021. Evidence for large microbial-mediated losses of soil carbon under anthropogenic warming. Nat. Rev. Earth Environ. 2, 507-517.

[17] Haynes R.J., 2005. Labile organic matter fractions as central components of the quality of agricultural soils: an overview. Adv. Agron 85, 221-268.

[18] Hu N., Wang B., Gu Z., Tao B., Zhang Z., Hu S., Zhu L., Meng Y., 2016. Effects of different straw returning modes on greenhouse gas emissions and crop yields in a rice-wheat rotation system. Agric. Ecosyst. Environ. 223, 115-122.

[19] IPCC, 2021. In: Masson-Delmotte, V., Zhai, P., Pirani, A., Connors, S.L., Péan, C., Berger, S., Caud, N., Chen, Y., Goldfarb, L., Gomis, M.I., Huang, M., Leitzell, K., Lonnoy, E., Matthews, J.B.R., Maycock, T.K., Waterfield, T., Yelekçi, O., Yu, R., Zhou, B. (Eds.), Climate Change 2021: the Physical Science Basis. Contribution of Working Group I to the Sixth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, United Kingdom and New York, NY, USA, p. 2391.

[20] IPCC, 2023. Climate change 2023: synthesis report. In: Lee, H., Romero, J. (Eds.), Contribution of Working Groups I, II and III to the Sixth Assessment Report of the Intergovernmental Panel on Climate Change. Core Writing Team, IPCC, Geneva, Switzerland, pp. 35-115.

[21] Jiang Y., Carrijo D., Huang S., Chen J., Balaine N., Zhang W., van Groenigen K.J., Linquist B., 2019a. Water management to mitigate the global warming potential of rice systems: a global meta-analysis. Field Crops Res. 234, 47-54.

[22] Jiang Y., Qian H., Huang S., Zhang X., Wang L., Zhang L., Shen M., Xiao X., Chen F., Zhang H., Lu C., Li C., Zhang J., Deng A., van Groenigen K.J., Zhang W., 2019b. Acclimation of methane emissions from rice paddy fields to straw addition. Sci. Adv. 5, eaau9038.

[23] Jiang Y., van Groenigen K.J., Huang S., Hungate B.A., van Kessel C., Hu S., Zhang J., Wu L., Yan X., Wang L., Chen J., Hang X., Zhang Y., Horwath W.R., Ye R., Linquist B.A., Song Z., Zheng C., Deng A., Zhang W., 2017. Higher yields and lower methane emissions with new rice cultivars. Glob. Change Biol. 23, 4728-4738.

[24] Kaur S., Dhanda S., Yadav A., Sagwal P., Yadav D.B., Chauhan B.S., 2022. Current status of herbicide-resistant weeds and their management in the rice-wheat cropping system of South Asia. Adv. Agron 172, 307-354.

[25] Krüger M., Eller G., Conrad R., Frenzel P., 2002. Seasonal variation in pathways of CH₄ production and in CH₄ oxidation in rice fields determined by stable carbon isotopes and specific inhibitors. Glob. Change Biol. 8, 265-280.

[26] Ladha J.K., Fischer K.S., Hossain M., Hobbs P.R., Hardy B., 2000. Improving the productivity and sustainability of rice-wheat systems of the Indo-Gangetic plains: a synthesis of NARS-IRRI partnership research. In: IRRI Discussion paper No.40, p. 31.

[27] Li J., Dong W., Oenema O., Chen T., Hu C., Yuan H., Zhao L., 2019. Irrigation reduces the negative effect of global warming on winter wheat yield and greenhouse gas intensity. Sci. Total Environ. 646, 290-299.

[28] Li W., Yang K., Hu C., Abbas W., Zhang J., Xu P., Cheng B., Zhang J., Yin W., Shalmani A., Qu L., Lv Q., Li B., He Y., Lai X., Xiong L., Zhang Q., Li Y., 2025. A natural gene on-off system confers field thermotolerance for grain quality and yield in rice. Cell 188, 3661-3678.e21.

[29] Li Y., Hou R., Tao F., 2020. Interactive effects of different warming levels and tillage managements on winter wheat growth, physiological processes, grain yield and quality in the North China Plain. Agric. Ecosyst. Environ. 295, 106923.

[30] Linquist B., van Groenigen K.J., Adviento-Borbe M.A., Pittelkow C., van Kessel C., 2012. An agronomic assessment of greenhouse gas emissions from major cereal crops. Glob. Change Biol. 18, 194-209.

[31] Liu S., Zheng Y., Ma R., Yu K., Han Z., Xiao S., Li Z., Wu S., Li S., Wang J., Luo Y., Zou J., 2020. Increased soil release of greenhouse gases shrinks terrestrial carbon uptake enhancement under warming. Glob. Change Biol. 26, 4601-4613.

[32] Lu M., Zhou X., Yang Q., Li H., Luo Y., Fang C., Chen J., Yang X., Li B., 2013. Responses of ecosystem carbon cycle to experimental warming: a meta-analysis. Ecology 94, 726-738.

[33] Lu Y., Wassmann R., Neue H.U., Huang C., Bueno C.S., 2000. Methanogenic responses to exogenous substrates in anaerobic rice soils. Soil Biol. Biochem. 32, 1683-1690.

[34] Luton P.E., Wayne J.M., Sharp R.J., Riley P.W., 2002. The mcrA gene as an alternative to 16S rRNA in the phylogenetic analysis of methanogen populations in landfill. Microbiology 148, 3521-3530.

[35] Ma C., Liu Y., Wang J., Xue L., Hou P., Xue L., Yang L., 2022. Warming increase the N₂O emissions from wheat fields but reduce the wheat yield in a rice-wheat rotation system. Agric. Ecosyst. Environ. 337, 108064.

[36] McDonald I.R., Bodrossy L., Chen Y., Murrell J.C., 2008. Molecular ecology techniques for the study of aerobic methanotrophs. Appl. Environ. Microbiol. 74, 1305-1315.

[37] Mo D., Liu Y., Li M., Li H., Zhang J., Qian H., Ding Y., Jiang Y., 2025. Warming increases CH₄ emissions from rice paddies through shifts in methanogenic and methanotrophic communities. Soil Biol. Biochem. 200, 109639.

[38] Neue H.U., Wassmann R., Lantin R.S., Alberto M.C.R., Aduna J.B., Javellana A.M., 1996. Factors affecting methane emission from rice fields. Atmos. Environ., 1751-1754.

[39] Ni H., Hu H., Zohner C.M., Huang W., Chen J., Sun Y., Ding J., Zhou J., Yan X., Zhang J., Liang Y., Crowther T.W., 2024. Effects of winter soil warming on crop biomass carbon loss from organic matter degradation. Nat. Commun. 15, 8847.

[40] Nwokolo N.L., Enebe M.C., 2025. Methane production and oxidation-A review on the pmoA and mcrA gene abundances for understanding the functional potentials of agricultural soils. Pedosphere 35, 161-181.

[41] Pereira J., Figueiredo N., Goufo P., Carneiro J., Morais R., Carranca C., Coutinho J., Trindade H., 2013. Effects of elevated temperature and atmospheric carbon dioxide concentration on the emissions of methane and nitrous oxide from Portuguese flooded rice fields. Atmos. Environ. 80, 464-471.

[42] Piao S., Ciais P., Huang Y., Shen Z., Peng S., Li J., Zhou L., Liu H., Ma Y., Ding Y., Friedlingstein P., Liu C., Tan K., Yu Y., Zhang T., Fang J., 2010. The impacts of climate change on water resources and agriculture in China. Nature 467, 43-51.

[43] Qian H., Chen J., Zhu X., Wang L., Liu Y., Zhang J., Deng A., Song Z., Ding Y., Jiang Y., van Groenigen K.J., Zhang W., 2022a. Intermittent flooding lowers the impact of elevated atmospheric CO₂ on CH₄ emissions from rice paddies. Agric. Ecosyst. Environ. 329, 107872.

[44] Qian H., Zhang N., Chen J., Chen C., Hungate B.A., Ruan J., Huang S., Cheng K., Song Z., Hou P., Zhang B., Zhang J., Wang Z., Zhang X., Li G., Liu Z., Wang S., Zhou G., Zhang W., Ding Y., van Groenigen K.J., Jiang Y., 2022b. Unexpected parabolic temperature dependency of CH₄ emissions from rice paddies. Environ. Sci. Technol. 56, 4871-4881.

[45] Qian H., Zhu X., Huang S., Linquist B., Kuzyakov Y., Wassmann R., Minamikawa K., Martinez-Eixarch M., Yan X., Zhou F., Sander B.O., Zhang W., Shang Z., Zou J., Zheng X., Li G., Liu Z., Wang S., Ding Y., van Groenigen K.J., Jiang Y., 2023. Greenhouse gas emissions and mitigation in rice agriculture. Nat. Rev. Earth Environ. 4, 716-732.

[46] Sáez-Sandino T., Reich P.B., Maestre F.T., Cano-Díaz C., Stefanski A., Bermudez R., Wang J., Dhar A., Singh B.K., Gallardo A., Delgado-Baquerizo M., Trivedi P., 2025. A large fraction of soil microbial taxa is sensitive to experimental warming. Glob. Change Biol. 31, e70231.

[47] Shen W., Ji Y., Jia Z., Huang Q., Zhu X., Ma J., Wang S., Liu X., Zhang G., Xu H., 2024a. Historical water regime determines the methanogenic pathway response to the current soil:water ratio. Soil Tillage Res. 239, 106032.

[48] Shen Y., Zhang C., Peng Y., Ran X., Liu K., Shi W., Wu W., Zhao Y., Liu W., Ding Y., Tang S., 2024b. Effects of warming on rice production and metabolism process associated with greenhouse gas emissions. Sci. Total Environ. 926, 172133.

[49] Tao F., Zhang Z., Shi W., Liu Y., Xiao D., Zhang S., Zhu Z., Wang M., Liu F., 2013. Single rice growth period was prolonged by cultivars shifts, but yield was damaged by climate change during 1981-2009 in China, and late rice was just opposite. Glob. Change Biol. 19, 3200-3209.

[50] Tian J., Dungait J.A.J., Hou R., Deng Y., Hartley I.P., Yang Y., Kuzyakov Y., Zhang F., Cotrufo M.F., Zhou J., 2024. Microbially mediated mechanisms underlie soil carbon accrual by conservation agriculture under decade-long warming. Nat. Commun. 15, 377.

[51] Tokida T., Fumoto T., Cheng W., Matsunami T., Adachi M., Katayanagi N., Matsushima M., Okawara Y., Nakamura H., Okada M., Sameshima R., Hasegawa T., 2010. Effects of free-air CO₂ enrichment (FACE) and soil warming on CH₄ emission from a rice paddy field: impact assessment and stoichiometric evaluation. Biogeosciences 7, 2639-2653.

[52] UNFCCC, 2015. Adoption of the Paris Agreement: Proposal by the President: Draft Decision CP 21 (No. GE.15-21932(E)), Adoption of the Paris Agreement. UNFCCC, Paris.

[53] van Groenigen K.J., van Kessel C., Hungate B.A., 2013. Increased greenhouse-gas intensity of rice production under future atmospheric conditions. Nat. Clim. Change 3, 288-291.

[54] Wang C., Jin Y., Ji C., Zhang N., Song M., Kong D., Liu S., Zhang X., Liu X., Zou J., Li S., Pan G., 2018. An additive effect of elevated atmospheric CO₂ and rising temperature on methane emissions related to methanogenic community in rice paddies. Agric. Ecosyst. Environ. 257, 165-174.

[55] Wang H., Zhou Q., Wang S., Zhang P., Wang L., Wang Z., Zhang L., Huang G., 2025a. Effects of long-term winter cropping on paddy rice yield, soil properties and rhizosphere bacterial community in Southern China. Field Crops Res. 322, 109734.

[56] Wang J., Chen S., Sun R., Liu B., Waghmode T., Hu C., 2023. Spatial and temporal dynamics of the bacterial community under experimental warming in field-grown wheat. Peer J. 11, e15428.

[57] Wang J., Wang Y., Chen Y., Chen H., Xiang J., Zhang Y., Wang Z., Zhang Y., 2025b. Progress on physiological mechanisms of rice spikelet degeneration at different panicle positions caused by abiotic stress. Rice Sci. 32, 193-202.

[58] Wang X., He Y., Zha Y., Chen H., Wang Y., Wu X., Ning J., Feng A., Han S., Luo S., 2024. Mapping winter fallow arable lands in Southern China by using a multi-temporal overlapped area minimization threshold method. GIScience Remote Sens. 61, 2333587.

[59] Wassmann R., Toölg M., Papen H., Rennenberg H., Seiler W., Cheng D.X., Wang M.X., 1996. Spatial and seasonal distribution of organic amendments affecting methane emission from Chinese rice fields. Biol. Fertil. Soils 22, 191-195.

[60] Watanabe A., Takeda T., Kimura M., 1999. Evaluation of origins of CH₄ carbon emitted from rice paddies. J. Geophys. Res. Atmospher. 104, 23623-23629.

[61] Wei L., Razavi B.S., Wang W., Zhu Z., Liu S., Wu J., Kuzyakov Y., Ge T., 2019. Labile carbon matters more than temperature for enzyme activity in paddy soil. Soil Biol. Biochem. 135, 134-143.

[62] WMO, 2024. WMO Greenhouse Gas Bulletin No. 20. the State of Greenhouse Gases in the Atmosphere Based on Global Observations Through 2023. World Meteorological Organization, Geneva, Switzerland (https://wmo.int/publication-series/wmo-gree nhouse-gas-bulletin-no-20).

[63] Wu C., Cui K., Wang W., Li Q., Fahad S., Hu Q., Huang J., Nie L., Peng S., 2016. Heat-induced phytohormone changes are associated with disrupted early reproductive development and reduced yield in rice. Sci. Rep. 6, 34978.

[64] Wu G., Ling J., Liu Z., Xu Y., Chen X., Wen Y., Zhou S., 2022. Soil warming and straw return impacts on winter wheat phenology, photosynthesis, root growth, and grain yield in the North China plain. Field Crops Res. 283, 108545.

[65] Wu X., Wang W., Xie K., Yin C., Hou H., Xie X., 2019. Combined effects of straw and water management on CH₄ emissions from rice fields. J. Environ. Manag. 231, 1257-1262.

[66] Yan X., Yagi K., Akiyama H., Akimoto H., 2005. Statistical analysis of the major variables controlling methane emission from rice fields. Glob. Change Biol. 11, 1131-1141.

[67] Yang W., Agathokleous E., Wu J., Chen H., Wu R., Huang H., Ren B., Wen S., Shen L., Wang W., 2024. Methane production is more sensitive to temperature increase than aerobic and anaerobic methane oxidation in Chinese paddy soils. Environ. Sci. Technol. 58, 18723-18732.

[68] Yang Z., Zhang Z., Zhang T., Fahad S., Cui K., Nie L., Peng S., Huang J., 2017. The effect of season-long temperature increases on rice cultivars grown in the central and southern regions of China. Front. Plant Sci. 8, 1908.

[69] Yuan S., Linquist B.A., Wilson L.T., Cassman K.G., Stuart A.M., Pede V., Miro B., Saito K., Agustiani N., Aristya V.E., Krisnadi L.Y., Zanon A.J., Heinemann A.B., Carracelas G., Subash N., Brahmanand P.S., Li T., Peng S., Grassini P., 2021. Sustainable intensification for a larger global rice bowl. Nat. Commun. 12, 7163.

[70] Yun S.-I., Kang B.-M., Lim S.-S., Choi W.-J., Ko J., Yoon S., Ro H.-M., Kim H.-Y., 2012. Further understanding CH₄ emissions from a flooded rice field exposed to experimental warming with elevated [CO₂]. Agric. For. Meteorol. 154, 75-83.

[71] Yvon-Durocher G., Allen A.P., Bastviken D., Conrad R., Gudasz C., St-Pierre A., Thanh-Duc N., del Giorgio P.A., 2014. Methane fluxes show consistent temperature dependence across microbial to ecosystem scales. Nature 507, 488-491.

[72] Zhan M., Cao C., Wang J., Jiang Y., Cai M., Yue L., Shahrear A., 2011. Dynamics of methane emission, active soil organic carbon and their relationships in wetland integrated rice-duck systems in Southern China. Nutrient Cycl. Agroecosyst. 89, 1-13.

[73] Zhang G., Yu H., Fan X., Yang Y., Ma J., Xu H., 2016. Drainage and tillage practices in the winter fallow season mitigate CH₄ and N₂O emissions from a double-rice field in China. Atmos. Chem. Phys. 16, 11853-11866.

[74] Zhang N., Qian H., Li H., Tang J., Yang T., Liu Z., Liu Y., Zhang B., Ding Y., Jiang Y., 2023. Effect of warming on rice yield and methane emissions in a Chinese tropical double-rice cropping system. Agric. Ecosyst. Environ. 348, 108409.

[75] Zhang N., Wang L., Wang X., Liu Z., Huang S., Wang Z., Chen C., Qian H., Li G., Liu Z, Ding Y., Zhang W., Jiang Y., 2024. Effects of warming on greenhouse gas emissions from China's rice paddies. Agric. Ecosyst. Environ. 366, 108953.

[76] Zhang Y., Li Z., Feng J., Zhang X., Jiang Y., Chen J., Zhang M., Deng A., Zhang W., 2014. Differences in CH₄ and N₂O emissions between rice nurseries in Chinese major rice cropping areas. Atmos. Environ. 96, 220-228.

[77] Zhu X., Chen N., Li W., Tang J., Huang Y., Qian H., Li G., Ding Y., van Groenigen K. J., Jiang Y., 2025. Quantifying the global methane mitigation potential of deep nitrogen placement in rice paddies. Resour. Conserv. Recycl. 219, 108315.