Abstract
Knowledge of nitrogen (N) impacts on soil respiration (Rs) and its components is critical to assess soil carbon (C) storage and C stability with accumulating N deposition. However, the abiotic and biotic mechanisms underlying the responses of Rs and its components to N enrichment are still far from clear. This study investigated the direct and indirect pathways of N enrichment on autotrophic respiration (Ra) and heterotrophic respiration (Rh) in a subtropical forest. The results showed that N addition significantly decreased Rs across the 2-year observation. The negative effects of N fertilization on Rs were the combination of suppressive effects of excessive N on Ra and Rh. On average, N enrichment decreased Rs, Ra, and Rh by 34%, 33%, and 35%, respectively across the 2 years. The decrease in Ra was directly due to reducing fine root biomass and indirectly affected by N-induced soil acidification. The decline in Rh was directly controlled by reducing soil microbial biomass C and indirectly determined by N-induced soil acidification and the elevation of soil N availability. Nitrogen addition significantly increased temperature sensitivities of Rs and its components, suggesting a potential positive C-climate feedback in the future scenarios of global warming and aggravating N deposition. Our study highlights the direct and indirect pathways of N fertilization on soil respiration and its components, which could have implications for assessing forest C sequestration and C stability.
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References
Ambus, P., & Robertson, G. P. (2006). The effect of increased N deposition on nitrous oxide, methane and carbon dioxide fluxes from unmanaged forest and grassland communities in Michigan. Biogeochemistry, 79, 315–337.
Bobbink, R., Hicks, K., Galloway, J., Spranger, T., Alkemade, R., Ashmore, M., Bustamante, M., Cinderby, S., Davidson, E., Dentener, F., Emmett, B., Erisman, J. W., Fenn, M., Gilliam, F., Nordin, A., Pardo, L., & De Vries, W. (2010). Global assessment of nitrogen deposition effects on terrestrial plant diversity: a synthesis. Ecological Applications, 20, 30–59.
Bowden, R. D., Davidson, E., Savage, K., Arabia, C., & Steudler, P. (2004). Chronic nitrogen additions reduce total soil respiration and microbial respiration in temperate forest soils at the Harvard Forest. Forest Ecology and Management, 196, 43–56.
Bradford, M. A., Wieder, W. R., Bonan, G. B., Fierer, N., Raymond, P. A., & Crowther, T. W. (2016). Managing uncertainty in soil carbon feedbacks to climate change. Nature Climate Change, 6, 751–758.
Chen, D. M., Li, J. J., Lan, Z. C., Hu, S. J., & Bai, Y. F. (2016). Soil acidification exerts a greater control on soil respiration than soil nitrogen availability in grasslands subjected to long-term nitrogen enrichment. Functional Ecology, 30, 658–669.
Coucheney, E., Stromgren, M., Lerch, T. Z., & Herrmann, A. M. (2013). Long-term fertilization of a boreal Norway spruce forest increases the temperature sensitivity of soil organic carbon mineralization. Ecology and Evolution, 3, 5177e5188.
Cox, P. M., Betts, P. A., Jones, C. D., Spall, S. A., & Totterdell, I. J. (2000). Acceleration of global warming due to carbon-cycle feedbacks in a coupled climate model. Nature, 408, 184–187.
Davidson, E. A., & Janssens, I. A. (2006). Temperature sensitivity of soil carbon decomposition and feedbacks to climate change. Nature, 440, 165–173.
Delgado-Baquerizo, M., Maestre, F. T., Reich, P. B., Jeffries, T. C., Gaitan, J. J., Encinar, D., Berdugo, M., Campell, C. D., & Singh, B. K. (2016). Microbial diversity drives multifunctionality in terrestrial ecosystems. Nature Communications, 7, 10541.
Deng, Q., Zhou, G., Liu, J., Liu, S., Duan, H., & Zhang, D. (2010). Responses of soil respiration to elevated carbon dioxide and nitrogen addition in young subtropical forest ecosystems in China. Biogeosciences, 7, 315–328.
Ding, J. Z., Chen, L. Y., Zhang, B. B., Liu, L., Yang, G. B., Fang, K., Chen, Y. L., Kou, D., Li, C. J., Luo, Y. Q., & Yang, Y. H. (2016). Linking temperature sensitivity of soil CO2 release to substrate, environmental, and microbial properties across alpine ecosystems. Global Biogeochemical Cycles, 30, 1310–1323.
Eberwein, J. R., Oikawa, P. Y., Allsman, L. A., & Jenerette, G. D. (2015). Carbon availability regulates soil respiration response to nitrogen and temperature. Soil Biology and Biochemistry, 88, 158–164.
Galloway, J. N., Townsend, A. R., Erisman, J. W., Bekunda, M., Cai, Z., Freney, J. R., Martinelli, L. A., Seitzinger, S. P., & Sutton, M. A. (2008). Transformation of the nitrogen cycle: recent trends, questions, and potential solutions. Science, 320, 889–892.
Gao, Q., Hasselquist, N. J., Palmroth, S., Zheng, Z. M., & You, W. H. (2014). Short-term response of soil respiration to nitrogen fertilization in a subtropical evergreen forest. Soil Biology and Biochemistry, 76, 297–300.
Guo, H., Ye, C., Zhang, H., Pan, S., Ji, Y., Li, Z., Liu, M., Zhou, X., Du, G., Hu, F., & Hu, S. (2017). Long-term nitrogen & phosphorus additions reduce soil microbial respiration but increase its temperature sensitivity in a Tibetan alpine meadow. Soil Biology and Biochemistry, 113, 26–34.
Humbert, J. Y., Dwyer, J. M., Andrey, A., & Arlettaz, R. (2016). Impacts of nitrogen addition on plant biodiversity in mountain grasslands depend on dose, application duration and climate: a systematic review. Global Change Biology, 22, 110–120.
Janssens, I. A., Dieleman, W., Luyssaert, S., Subke, J. A., Reichstein, M., Ceulemans, R., Ciais, P., Dolman, A. J., Grace, J., Matteucci, G., Papale, D., Piao, S. L., Schulze, E.-D., Tang, J., & Law, B. E. (2010). Reduction of forest soil respiration in response to nitrogen deposition. Nature Geoscience, 3, 315–322.
Jia, X. X., Shao, M. A., & Wei, X. R. (2012). Responses of soil respiration to N addition, burning and clipping in temperate semiarid grassland in northern China. Agricultural and Forest Meteorology, 166-167, 32–40.
Jia, Y. L., Yu, G. R., He, N. P., Zhan, X. Y., Fang, H. J., Sheng, W. P., Zuo, Y., Zhang, D. Y., & Wang, Q. F. (2014). Spatial and decadal variations in inorganic nitrogen wet deposition in China induced by human activity. Scientific Reports, 4, 3763.
Kuzyakov, Y. (2006). Sources of CO2 efflux from soil and review of partitioning methods. Soil Biology and Biochemistry, 38, 425–448.
Li, Y., Sun, J., Tian, D. S., Wang, J. S., Ha, D. L., Qu, Y. X., Jing, G. W., & Niu, S. L. (2018). Soil acid cations induced reduction in soil respiration under nitrogen enrichment and soil acidification. Science of the Total Environment, 615, 1535–1546.
Liu, X. J., Zhang, Y., Han, W. X., Tang, A. H., Shen, J. L., Cui, Z. L., Vitousek, P., Erisman, J. W., Goulding, K., Christie, P., Fangmeier, A., & Zhang, F. S. (2013). Enhanced nitrogen deposition over China. Nature, 494, 459–462.
Liu, L. L., Wang, X., Lajeunesse, M. J., Miao, G. F., Piao, S. L., Wan, S. Q., Wu, Y. X., Wang, Z. H., Yang, S., Li, P., & Deng, M. F. (2016a). A cross-biome synthesis of soil respiration and its determinants under simulated precipitation changes. Global Change Biology, 22, 1394–1405.
Liu, B., Mou, C., Yan, G., Xu, L., Jiang, S., Xing, Y., & Wang, Q. (2016b). Annual soil CO2 efflux in a cold temperate forest in northeastern China: effects of winter snowpack and artificial nitrogen deposition. Scientific Reports, 6, 18957.
Luo, Y. Q., & Zhou, X. H. (Eds.). (2006). Soil respiration and the environment (p. 328). San Diego: Elsevier.
Mo, J. M., Zhang, W., Zhu, W. X., Gdundersen, P., Fang, Y. T., Li, D. J., & Wang, H. (2008). Nitrogen addition reduces soil respiration in a mature tropical forest in southern China. Global Change Biology, 14, 403–412.
Nakamura, M., Nakamura, T., & Tsuchiya, T. (2010). Advantages of NH4 + on growth, nitrogen uptake and root respiration of Phragmites australis. Plant and Soil, 331, 463–470.
Peng, Y., Li, F., Zhou, G., Fang, K., Zhang, D., Li, C., Yang, G., Wang, G., Wang, J., Mohammat, A., & Yang, Y. (2017). Nonlinear response of soil respiration to increasing nitrogen additions in a Tibetan alpine steppe. Environmental Research Letters, 12, 024018.
Peñuelas, J., Poulter, B., Sardans, J., Ciais, P., Velde, M. V. D., Bopp, L., Boucher, O., Godderis, Y., Hinsinger, P., Llusia, J., Nardin, E., Vicca, S., Obersteiner, M., & Janssens, I. A. (2013). Human-induced nitrogen-phosphorus imbalances alter natural and managed ecosystems across the globe. Nature Communications, 4, 1–10.
Phillips, R. P., & Fahey, T. J. (2007). Fertilization effects on fineroot biomass, rhizosphere microbes and respiratory fluxes in hardwood forest soils. New Phytologist, 176, 655–664.
R Core Team. (2015). R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing.
Raich, J. W., & Schlesinger, W. H. (1992). The global carbon dioxide flux in soil respiration and its relationship to vegetation and climate. Tellus B, 44, 81–99.
Ryan, M. G., & Law, B. E. (2005). Interpreting, measuring, and modeling soil respiration. Biogeochemistry, 73, 3–27.
Sayer, E. J., & Tanner, E. V. J. (2010). A new approach to trenching experiments for measuring root-rhizosphere respiration in a lowland tropical forest. Soil Biology and Biochemistry, 42, 347–352.
Stone, M. M., Weiss, M. S., Goodale, C. L., Adams, M. B., Fernandez, I. J., German, D. P., & Allison, S. D. (2012). Temperature sensitivity of soil enzyme kinetics under N fertilization in two temperate forsts. Global Change Biology, 18, 1173–1184.
Treseder, K. K. (2008). Nitrogen additions and microbial biomass: a meta-analysis of ecosystem studies. Ecology Letters, 11, 1111–1120.
Vance, E. D., Brookes, P. C., & Jenkinson, D. S. (1987). An extraction method for measuring soil microbial biomass-C. Soil Biology and Biochemistry, 19, 703–707.
Wang, Q. K., Zhang, W. D., Sun, T., Chen, L. C., Pang, X. Y., Wang, Y. P., & Xiao, F. M. (2017). N and P fertilization reduced soil autotrophic and heterotrophic respiration in a young Cunninghamia lanceolata forest. Agricultural and Forest Meteorology, 232, 66–73.
Wang, C., Liu, D. W., & Bai, E. (2018). Decreasing soil microbial diversity is associated with decreasing microbial biomass under nitrogen addition. Soil Biology and Biochemistry, 120, 126–133.
Xia, J. Y., & Wan, S. Q. (2008). Global response patterns of terrestrial plant species to nitrogen addition. New Phytologist, 179, 428–439.
Yue, K., Peng, Y., Peng, C. H., Yang, W. Q., Peng, X., & Wu, F. Z. (2016). Stimulation of terrestrial ecosystem carbon storage by nitrogen addition: a meta-analysis. Scientific Reports, 6, 19895.
Zhang, C. P., Niu, D. C., Hall, S. J., Wen, H. Y., Li, X. D., Fu, H., Wan, C. G., & Elser, J. J. (2014). Effects of simulated nitrogen deposition on soil respiration components and their temperature sensitivities in a semiarid grassland. Soil Biology and Biochemistry, 75, 113–123.
Zhang, W., Shen, W. J., Zhu, S. D., Wan, S. Q., Luo, Y. Q., Yan, J. H., Wang, K. Y., Liu, L., Dai, H. T., Li, P. X., Dai, K. Y., Zhang, W. X., Liu, Z. F., Wang, F. M., Kuang, Y. W., Li, Z. A., Lin, Y. B., Rao, X. Q., Li, J., Zou, B., Cai, X., Mo, J. M., Zhao, P., Ye, Q., Huang, J. G., & Fu, S. L. (2015). CAN canopy addition of nitrogen better illustrate the effect of atmospheric nitrogen deposition on forest ecosystem? Scientific Reports, 5, 11245.
Zhang, T., Chen, H. Y. H., & Ruan, H. (2018). Global negative effects of nitrogen deposition on soil microbes. ISME Journal, 12, 1817–1825.
Zhong, Y., Yan, W., & Shangguan, Z. (2016). The effects of nitrogen enrichment on soil CO2 fluxes depending on temperature and soil properties. Global Ecology and Biogeography, 25, 475–488.
Zhou, L., Zhou, X., Zhang, B., Lu, M., Luo, Y., Liu, L., & Li, B. (2014). Different responses of soil respiration and its components to nitrogen addition among biomes: a meta-analysis. Global Change Biology, 20, 2332–2343.
Zhou, L. Y., Zhou, X. H., Shao, J. J., Nie, Y. Y., He, Y. H., Jiang, L. L., Wu, Z. T., & Bai, S. H. (2016). Interactive effects of global change factors on soil respiration and its components: a meta-analysis. Global Change Biololgy, 22, 3157–3169.
Acknowledgments
L.L. and S.N. conceived the ideas and designed methodology. L.L., F.C., H.H., Y.Z., and J.Z. analyzed the data. L.L. and S.N. wrote the first draft of the paper. L.L., W.B., and S.N. revised the manuscript. All authors provided input to the drafting and final version of the manuscript. This research is supported by the National Key Research and Development Program of China (No.2016YFD0600205), the National Forestry Public Welfare Professional Scientific Research Project (No. 201404213), and CFERN & GENE Award Funds for Ecological Papers.
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Liang, L., Chen, F., Han, H. et al. Pathways Regulating Decreased Soil Respiration with Nitrogen Addition in a Subtropical Forest in China. Water Air Soil Pollut 230, 91 (2019). https://doi.org/10.1007/s11270-019-4144-7
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DOI: https://doi.org/10.1007/s11270-019-4144-7