Abstract
Asymbiotic N2 fixation (ANF) is a major nitrogen (N) input pathway to terrestrial ecosystems. However, there is considerable uncertainty about how lithology affects ANF. Here, we measured ANF rates in soil, litter, and moss in forests underlain by limestone (limestone forest), dolomite (dolomite forest), and clasolite (clasolite forest), respectively, in southwest China. Effects of lithology on soil ANF rate varied seasonally. The rate was highest in the dolomite forest during the wet season, but was highest in the limestone forest during the dry season. The overall soil ANF rate was significantly higher in the limestone forest than in the clasolite forest. Litter ANF rate was significantly higher in the limestone forest and dolomite forest than in the clasolite forest regardless of season. There was no significant difference in moss ANF rate among the three types of forests in both seasons. The annual N2 fixation rate was highest in the limestone forest (1.72 ± 0.27 kg N ha−1 y−1) but lowest in the clasolite forest (0.70 ± 0.08 kg N ha−1 y−1). In the wet season, the variation of ANF rates was best explained by soil nitrate and available iron for soil, and by litter N and calcium content for litter. In the dry season, the variation of ANF rates was best explained by soil water content, ammonia and total phosphorus for soil, and by litter water content and calcium content for litter. No strong explanatory variables were identified for ANF in moss during the wet or dry season. Our findings suggest that lithology significantly affected ANF in soil and litter, but not in moss, and hence should be considered in Earth system models to facilitate better prediction of N inputs via biological N2 fixation under global change.
Similar content being viewed by others
References
Amin D, Sharma A, Ray S. 2022. Cyanobacteria. In: Amaresan N, Patel P, Amin D Eds. Practical handbook on agricultural microbiology. New York (NY): Springer, pp 85–91.
Augusto L, Achat DL, Jonard M, Vidal D, Ringeval B. 2017. Soil parent material—a major driver of plant nutrient limitations in terrestrial ecosystems. Global Change Biology 23:3808–3824.
Ayres E, van der Wal R, Sommerkorn M, Bardgett RD. 2006. Direct uptake of soil nitrogen by mosses. Biology Letters 2:286–288.
Barron AR, Wurzburger N, Bellenger JP, Wright SJ, Kraepiel AML, Hedin LO. 2009. Molybdenum limitation of asymbiotic nitrogen fixation in tropical forest soils. Nature Geoscience 2:42–45.
Bellenger JP, Darnajoux R, Zhang X, Kraepiel AML. 2020. Biological nitrogen fixation by alternative nitrogenases in terrestrial ecosystems: a review. Biogeochemistry 149:53–73.
Bhunia AK, Basu NK, Roy D, Banerjee SK. 1994. Role of calcium in the inhibition of nitrogenase activity by Methylparathion and Benthiocarb in the cyanobacterium Nostoc muscorum. World Journal of Microbiology and Biotechnology 10:303–307.
Cassman KG, Munns DN. 1980. Nitrogen mineralization as affected by soil moisture, temperature, and depth. Soil Science Society of America Journal 44:1233–1237.
Cleveland CC, Townsend AR, Schimel DS, Fisher H, Howarth RW, Hedin LO, Perakis SS, Latty EF, Von Fischer JC, Elseroad A, Wasson MF. 1999. Global patterns of terrestrial biological nitrogen (N2) fixation in natural ecosystems. Global Biogeochemical Cycles 13:623–645.
Darnajoux R, Constantin J, Miadlikowska J, Lutzoni F, Bellenger J-P. 2014. Is vanadium a biometal for boreal cyanolichens? New Phytologist 202:765–771.
Darnajoux R, Zhang X, McRose DL, Miadlikowska J, Lutzoni F, Kraepiel AM, Bellenger JP. 2017. Biological nitrogen fixation by alternative nitrogenases in boreal cyanolichens: importance of molybdenum availability and implications for current biological nitrogen fixation estimates. New Phytologist 213:680–689.
Davies-Barnard T, Friedlingstein P. 2020. The global distribution of biological nitrogen fixation in terrestrial natural ecosystems. Global Biogeochemical Cycles 34:e2019GB006387.
Dynarski KA, Houlton BZ. 2018. Nutrient limitation of terrestrial free-living nitrogen fixation. New Phytologist 217:1050–1061.
Hanus-Fajerska E, Wiszniewska A, Kamińska I. 2021. A dual role of vanadium in environmental systems—beneficial and detrimental effects on terrestrial plants and humans. Plants 10:1110.
Hardy RWF, Holsten RD, Jackson EK, Burns RC. 1968. Acetylene-ethylene assay for N2 fixation-laboratory and field eveluation: laboratory and field evaluation. Plant Physiology 43:1185–1207.
Jean M-E, Phalyvong K, Forest-Drolet J, Bellenger J-P. 2013. Molybdenum and phosphorus limitation of asymbiotic nitrogen fixation in forests of Eastern Canada: influence of vegetative cover and seasonal variability. Soil Biology and Biochemistry 67:140–146.
Kuik P, Wolterbeek HT. 1995. Factor analysis of atmospheric trace-element deposition data in the Netherlands obtained by moss monitoring. Water, Air, and Soil Pollution 84:323–346.
Lenth RV. 2016. Least-squares means: the R package lsmeans. Journal of Statistical Software 69:1–33.
Li D, Wang X, Mo J, Sheng G, Fu J. 2007. Soil nitric oxide emissions from two subtropical humid forests in south China. Journal of Geophysical Research-Atmospheres 112:D23302.
Li D, Wang Z, Sun X, Zhang Q, Wang K. 2018a. Tree species effects on asymbiotic N2 fixation in subtropical karst and non-karst forests. Soil Biology and Biochemistry 117:185–190.
Li D, Yang Y, Chen H, Xiao K, Song T, Wang K. 2017. Soil gross nitrogen transformations in typical karst and nonkarst forests, southwest China. Journal of Geophysical Research: Biogeosciences 122:2831–2840.
Li D, Zhang Q, Wang Z. 2019. Free-living N2 fixation in three karst shrublands, southwest China. Ecosystems 22:818–826.
Li D, Zhang Q, Xiao K, Wang Z, Wang K. 2018b. Divergent responses of biological nitrogen fixation in soil, litter and moss to temperature and moisture in a karst forest, southwest China. Soil Biology and Biochemistry 118:1–7.
Neff JC, Reynolds R, Sanford RL, Fernandez D, Lamothe P. 2006. Controls of bedrock geochemistry on soil and plant nutrients in Southeastern Utah. Ecosystems 9:879–893.
Norman JS, Friesen ML. 2017. Complex N acquisition by soil diazotrophs: how the ability to release exoenzymes affects N fixation by terrestrial free-living diazotrophs. ISME Journal 11:315–326.
Piepho H-P. 2004. An algorithm for a letter-based representation of all-pairwise comparisons. Journal of Computational and Graphical Statistics 13:456–466.
Porada P, Lenton TM, Pohl A, Weber B, Mander L, Donnadieu Y, Beer C, Pöschl U, Kleidon A. 2016. High potential for weathering and climate effects of non-vascular vegetation in the Late Ordovician. Nature Communications 7:12113.
Ramos J, Bisseling T. 1995. Symbiotic nitrogen fixation. Plant Cell 7:869–885.
Reed SC, Cleveland CC, Townsend AR. 2011. Functional ecology of free-living nitrogen fixation: a contemporary perspective. Annual Review of Ecology, Evolution, and Systematics 42:489–512.
Reed SC, Cleveland CC, Townsend AR. 2013. Relationships among phosphorus, molybdenum and free-living nitrogen fixation in tropical rain forests: results from observational and experimental analyses. Biogeochemistry 114:135–147.
Rousk K, Sorensen PL, Michelsen A. 2018. What drives biological nitrogen fixation in high arctic tundra: moisture or temperature? Ecosphere 9:e02117.
Tan Q, Jia Y, Wang G. 2021. Decoupling of soil nitrogen and phosphorus dynamics along a temperature gradient on the Qinghai-Tibetan Plateau. Geoderma 396:115084.
Thomas RQ, Brookshire EN, Gerber S. 2015. Nitrogen limitation on land: how can it occur in Earth system models? Global Change Biology 21:1777–1793.
Thomas RQ, Zaehle S, Templer PH, Goodale CL. 2013. Global patterns of nitrogen limitation: confronting two global biogeochemical models with observations. Global Change Biology 19:2986–2998.
Van Langenhove L, Depaepe T, Vicca S, van den Berge J, Stahl C, Courtois E, Weedon J, Urbina I, Grau O, Asensio D, Peñuelas J, Boeckx P, Richter A, Van Der Straeten D, Janssens IA. 2020. Regulation of nitrogen fixation from free-living organisms in soil and leaf litter of two tropical forests of the Guiana shield. Plant Soil 450:93–110.
Wang M, Chen H, Zhang W, Wang K. 2018. Soil nutrients and stoichiometric ratios as affected by land use and lithology at county scale in a karst area, southwest China. Science of the Total Environment 619–620:1299–1307.
Wang Z, Li D, Zheng M, Chen H, Sun X, Wang K. 2019. Topography modulates effects of nitrogen deposition on asymbiotic N2 fixation in soil but not litter or moss in a secondary karst forest. Journal of Geophysical Research: Biogeosciences 124:3015–3023.
Winbourne JB, Brewer SW, Houlton BZ. 2017. Iron controls over di-nitrogen fixation in karst tropical forest. Ecology 98:773–781.
Yu T, Zhuang Q. 2020. Modeling biological nitrogen fixation in global natural terrestrial ecosystems. Biogeosciences 17:3643–3657.
Zhang Y, Chen X, Zhang C, Pan G, Zhang X. 2014. Availability of soil nitrogen and phosphorus under elevated CO2 and temperature in the Taihu Lake region, China. Journal of Plant Nutrition and Soil Science 177:343–348.
Zheng M, Zhang W, Luo Y, Li D, Wang S, Huang J, Lu X, Mo J. 2018. Stoichiometry controls asymbiotic nitrogen fixation and its response to nitrogen inputs in a nitrogen-saturated forest. Ecology 99:2037–2046.
Zheng M, Zhou Z, Luo Y, Zhao P, Mo J. 2019. Global pattern and controls of biological nitrogen fixation under nutrient enrichment: a meta-analysis. Global Change Biology 25:3018–3030.
Zheng MH, Zhang W, Luo YQ, Mori T, Mao QG, Wang SH, Huang J, Lu XK, Mo JM. 2017. Different responses of asymbiotic nitrogen fixation to nitrogen addition between disturbed and rehabilitated subtropical forests. Science of the Total Environment 601–602:1505–1512.
Zhou J, Ma J, Li D. 2021. Symbiotic and free-living N2 fixation in subtropical Pueraria lobata communities of southwest China. Journal of Geophysical Research: Biogeosciences 126:e2021JG006282.
Acknowledgements
This work was supported by the National Natural Science Foundation of China (41877094, 42007086), Guangxi Bagui Scholarship Program to Dejun Li, Special Foundation for Science and Technology Base and Talents in Guangxi Province of China (GuikeAD20297037).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Wang, Z., Li, D., Sun, X. et al. Effects of Lithology on Asymbiotic N2 Fixation in Subtropical Secondary Forests, Southwest China. Ecosystems 26, 1173–1182 (2023). https://doi.org/10.1007/s10021-023-00824-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10021-023-00824-6