Advertisement

Pathways Regulating Decreased Soil Respiration with Nitrogen Addition in a Subtropical Forest in China

  • Lizhuang LiangEmail author
  • Feng Chen
  • Hairong Han
  • Yanru Zhang
  • Jiang Zhu
  • Shukui NiuEmail author
Article
  • 105 Downloads

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.

Keywords

Nitrogen enrichment Autotrophic respiration Heterotrophic respiration Temperature sensitivity Structural equation modeling 

Notes

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.

References

  1. 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.CrossRefGoogle Scholar
  2. 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.CrossRefGoogle Scholar
  3. 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.Google Scholar
  4. 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.CrossRefGoogle Scholar
  5. 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.CrossRefGoogle Scholar
  6. 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.CrossRefGoogle Scholar
  7. 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.CrossRefGoogle Scholar
  8. Davidson, E. A., & Janssens, I. A. (2006). Temperature sensitivity of soil carbon decomposition and feedbacks to climate change. Nature, 440, 165–173.CrossRefGoogle Scholar
  9. 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.CrossRefGoogle Scholar
  10. 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.CrossRefGoogle Scholar
  11. 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.CrossRefGoogle Scholar
  12. 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.CrossRefGoogle Scholar
  13. 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.CrossRefGoogle Scholar
  14. 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.CrossRefGoogle Scholar
  15. 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.CrossRefGoogle Scholar
  16. 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.CrossRefGoogle Scholar
  17. 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.CrossRefGoogle Scholar
  18. 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.CrossRefGoogle Scholar
  19. 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.CrossRefGoogle Scholar
  20. Kuzyakov, Y. (2006). Sources of CO2 efflux from soil and review of partitioning methods. Soil Biology and Biochemistry, 38, 425–448.CrossRefGoogle Scholar
  21. 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.CrossRefGoogle Scholar
  22. 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.CrossRefGoogle Scholar
  23. 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.CrossRefGoogle Scholar
  24. 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.CrossRefGoogle Scholar
  25. Luo, Y. Q., & Zhou, X. H. (Eds.). (2006). Soil respiration and the environment (p. 328). San Diego: Elsevier.Google Scholar
  26. 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.CrossRefGoogle Scholar
  27. 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.Google Scholar
  28. 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.CrossRefGoogle Scholar
  29. 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.Google Scholar
  30. 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.CrossRefGoogle Scholar
  31. R Core Team. (2015). R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing.Google Scholar
  32. 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.CrossRefGoogle Scholar
  33. Ryan, M. G., & Law, B. E. (2005). Interpreting, measuring, and modeling soil respiration. Biogeochemistry, 73, 3–27.CrossRefGoogle Scholar
  34. 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.CrossRefGoogle Scholar
  35. 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.CrossRefGoogle Scholar
  36. Treseder, K. K. (2008). Nitrogen additions and microbial biomass: a meta-analysis of ecosystem studies. Ecology Letters, 11, 1111–1120.CrossRefGoogle Scholar
  37. 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.CrossRefGoogle Scholar
  38. 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.CrossRefGoogle Scholar
  39. 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.CrossRefGoogle Scholar
  40. Xia, J. Y., & Wan, S. Q. (2008). Global response patterns of terrestrial plant species to nitrogen addition. New Phytologist, 179, 428–439.CrossRefGoogle Scholar
  41. 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.CrossRefGoogle Scholar
  42. 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.CrossRefGoogle Scholar
  43. 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.CrossRefGoogle Scholar
  44. Zhang, T., Chen, H. Y. H., & Ruan, H. (2018). Global negative effects of nitrogen deposition on soil microbes. ISME Journal, 12, 1817–1825.CrossRefGoogle Scholar
  45. 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.CrossRefGoogle Scholar
  46. 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.CrossRefGoogle Scholar
  47. 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.CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.The Key Laboratory for Forest Resources and Ecosystem Processes of BeijingBeijing Forestry UniversityBeijingChina

Personalised recommendations