Abstract
Plants are the main sources of soil organic carbon in forest ecosystems. Photosynthetic C assimilated by plants enters the soil through litter, root litter, and root exudates. However, it remains unclear how litter changes affect the plant-C input. We aimed to quantify the responses of C inputs via the litter, root litter, and root exudates to litter alteration. We conducted a 2 years litter manipulation (litter removal, litter addition, and control) experiment in a Pinus massoniana plantation and studied its impacts on plant-C inputs via litter, fine root litter, and root exudates. The results show that litter removal significantly increases the litterfall in summer and autumn and reduces root-C exudation rates in spring but has no effect on the C input by fine roots. The annual C inputs by litter, fine roots, and root exudates in the control plots were 348.28, 42.39, and 17.44 g C m−2, respectively, accounting for 85.34%, 10.39%, and 4.27% of the total C input, respectively. Litter removal increases the plant annual total C input by 24.55% due to the decrease in the root exudate-C input by 30.50% and increase in the litter-C input by 31.12%. In contrast, litter addition insignificantly affects the C input through litter, fine roots, or root exudates. Increasing the litter-C input and decreasing the root exudate-C input by litter removal are a plant strategy based on which forest growth can be maximized in the short term. The increased plant-C input due to litter removal mitigates the effects of litter alteration. This study is of great significance for understanding plant growth strategies.
Similar content being viewed by others
Abbreviations
- CT:
-
Control
- LA:
-
Litter addition
- LR:
-
Litter removal
- SOM:
-
Soil organic matter
- MBC:
-
Microbial biomass carbon
- MBN:
-
Microbial biomass nitrogen
References
Ataka M, Sun L, Nakaji T, Katayama A, Hiura T (2020) Five-year nitrogen addition affects fine root exudation and its correlation with root respiration in a dominant species, Quercus crispula, of a cool temperate forest, Japan. Tree Physiol 40:367–376
Badri DV, Vivanco JM (2009) Regulation and function of root exudates. Plant Cell Environ 32:666–681
Bengtson P, Barker J, Grayston SJ (2012) Evidence of a strong coupling between root exudation, C and N availability, and stimulated SOM decomposition caused by rhizosphere priming effects. Ecol Evol 2(8):1843–1852
Blair BC, Perfecto I (2001) Nutrient content and substrate effect on fine root density and size distribution in a Nicaraguan rain forest. Biotropica 33:697–701
Chen L, Fang K, Wei B, Qin S, Feng X, Hu T, Ji C, Yang Y (2021) Soil carbon persistence governed by plant input and mineral protection at regional and global scales. Ecol Lett 24:1018–1028
Clemmensen KE, Bahr A, Ovaskainen O, Dahlberg A, Ekblad A, Wallander H, Stenlid J, Finlay RD, Wardle DA, Lindahl BD (2013) Roots and associated fungi drive long-term carbon sequestration in boreal forest. Science 339(6127):1615–1618
Cotrufo MF, Wallenstein MD, Boot CM, Denef K, Paul E (2013) The microbial efficiency-matrix stabilization (MEMS) framework integrates plant litter decomposition with soil organic matter stabilization: do labile plant inputs form stable soil organic matter? Glob Change Biol 19(4):988–995
Degryse F, Verma VK, Smolders E (2008) Mobilization of Cu and Zn by root exudates of dicotyledonous plants in resin-buffered solutions and in soil. Plant Soil 306:69–84
Du E, Fenn ME, Vries WD, Ok YS (2019) Atmospheric nitrogen deposition to global forests: status, impacts and management options. Environ Pollut 250:1044–1048
Fontaine S, Barot S, Barré P, Bdioui N, Mary B, Rumpel C (2007) Stability of organic carbon in deep soil layers controlled by fresh carbon supply. Nature 450:277–280
Gill AL, Finzi AC, Penuelas J (2016) Belowground carbon flux links biogeochemical cycles and resource-use efficiency at the global scale. Ecol Lett 19(12):1419–1428
Haichar FEZ, Santaella C, Heulin T, Achouak W (2014) Root exudates mediated interactions belowground. Soil Biol Biochem 77:69–80
Hu YL, Zeng DH, Ma XQ (2016) Chang SX (2016) Root rather than leaf litter input drives soil carbon sequestration after afforestation on a marginal cropland. For Ecol Manag 362:38–45
Huang W, Spohn M (2015) Effects of long-term litter manipulation on soil carbon, nitrogen, and phosphorus in a temperate deciduous forest. Soil Biol Biochem 83:12–18
Huang L, He B, Chen A, Wang H, Liu J, Lű A, Chen Z (2016) Drought dominates the interannual variability in global terrestrial net primary production by controlling semi-arid ecosystems. Sci Rep 6:24639
Huang J, Liu W, Yang S, Yang L, Peng Z, Deng M, Shan Xu, Zhang B, Ahirwal J, Liu L (2021) Plant carbon inputs through shoot, root, and mycorrhizal pathways affect soil organic carbon turnover differently. Soil Biol Biochem 160:108322
Jackson RB, Lajtha K, Crow SE, Hugelius G, Kramer MG, Piñeiro G (2017) The ecology of soil carbon: pools, vulnerabilities, and biotic and abiotic controls. Annu Rev Ecol Evol S 48:419–445
Joergensen RG (1996) The fumigation-extraction method to estimate soil microbial biomass: calibration of the kEC value. Soil Biol Biochem 28(1):25–31
Keiluweit M, Bougoure JJ, Nico PS, Pett-Ridge J, Weber PK, Kleber M (2015) Mineral protection of soil carbon counteracted by root exudates. Nat Clim Chang 5:588–595
Kuzyakov Y, Bol R (2006) Sources and mechanisms of priming effect induced in two grassland soils amended with slurry and sugar. Soil Biol Biochem 38(4):747–758
Kuzyakov Y, Domanski G (2000) Carbon input by plants into the soil: review. J Plant Nutr Soil Sc 163:421–431
Leff JW, Wieder WR, Taylor PG, Townsend AR, Nemergut DR, Grandy AS, Cleveland CC (2012) Experimental litterfall manipulation drives large and rapid changes in soil carbon cycling in a wet tropical forest. Glob Change Biol 18(9):2969–2979
Li G, Han H, Du Y, Hui D, Xia J, Niu S, Li X, Wan S (2017) Effects of warming and increased precipitation on net ecosystem productivity: a long-term manipulative experiment in a semiarid grassland. Agr Forest Meteorol 232(15):359–366
Lima TTS, Miranda IS, Vasconcelos SS, Vasconcelos SS (2010) Effects of water and nutrient availability on fine root growth in eastern Amazonian forest regrowth. Brazil New Phytol 187(3):622–630
Liu X, Lin TC, Vadeboncoeur MA, Yang Z, Yang Y (2019) Root litter inputs exert greater influence over soil C than does aboveground litter in a subtropical natural forest. Plant Soil 444(1/2):489–499
Ma Z, Gao S, Yang W, Wu F (2015) Degradation characteristics of lignin and cellulose of foliar litter at different rainy stages in subtropical evergreen broadleaved forest. Chin J Ecol 34(01):122–129
Matamala R, Gonzàlez-Meler MA, Jastrow JD, Norby RJ, Schlesinger WH (2003) Impacts of fine root turnover on forest NPP and soil C sequestration potential. Science 302(5649):1385–1387
Mei L (2006) Fine root turnover and carbon allocation in Manchurian Ash and Davurian Larch plantations. Dissertation, Northeast Forestry University
Meier IC, Finzi AC, Phillips RP (2017) Root exudates increase N availability by stimulating microbial turnover of fast-cycling N pools. Soil Biol Biochem 106:119–128
Nguyen C (2003) Rhizodeposition of organic C by plants : mechanisms and controls. Agronomie 23(5–6):375–396
Nobili MD, Contin M, Mondini C, Brookes PC (2001) Soil microbial biomass is triggered into activity by trace amounts of substrate. Soil Biol Biochem 33:1163–1170
Ostertag R, Scatena FN, Silver WL (2003) Forest floor decomposition following hurricane litter inputs in several Puerto Rican forests. Ecosystems 6:261–273
Phillips RP, Erlitz Y, Bier R, Bernhardt ES (2008) New approach for capturing soluble root exudates in forest soils. Funct Ecol 22:990–999
Phillips RP, Bernhardt ES, Schlesinger WH (2009) Elevated CO2 increases root exudation from loblolly pine (Pinus taeda) seedlings as an N-mediated response. Tree Physiol 29(12):1513–1523
Phillips RP, Finzi AC, Bernhardt ES (2011) Enhanced root exudation induces microbial feedbacks to N cycling in a pine forest under long-term CO2 fumigation. Ecol Lett 14:187–194
Quan Q, Tian D, Luo Y, Zhang F, Crowther TW, Zhu K, Chen HYH, Zhou Q, Niu S (2019) Water scaling of ecosystem carbon cycle feedback to climate warming. Sci Adv 5(8):eaav131
Rasse DP, Rumpel C, Dignac M-F (2005) Is soil carbon mostly root carbon? Mechanisms for a specific stabilisation. Plant Soil 269:341–356
Rocha JHT, Gonçalves JLM, Gava JL, Godinho TO, Melo EASC, Bazani JH, Hubner A (2016a) Forest residue maintenance increased the wood productivity of a Eucalyptus plantation over two short rotations. Forest Ecol Manag 379:1–10
Rocha JHT, Marques ERG, Gonçalves JLM, Hübner A, Brandani B, Ferraz AV, Moreir RM (2016b) Decomposition rates of forest residues and soil fertility after clear-cutting of Eucalyptus grandis stands in response to site management and fertilizer application. Soil Use Manag 32(3):289–302
Rodtassana C, Tanner EVJ (2018) Litter removal in a tropical rain forest reduces fine root biomass and production but litter addition has few effects. Ecology 99(3):735–742
Rubino M, Dungait JAJ, Evershed RP, Bertolini T, Angelis PD, D’Onofrio A, Lagomarsino A, Lubritto C, Merola A, Terrasi F, Cotrufo MF (2010) Carbon input belowground is the major C flux contributing to leaf litter mass loss: evidences from a 13C labelled-leaf litter experiment. Soil Biol Biochem 42(7):1009–1016
Santos F, Nadelhoffer K, Bird JA (2016) Rapid fine root C and N mineralization in a northern temperate forest soil. Biogeochemistry 128:187–200
Sayer EJ (2006) Using experimental manipulation to assess the roles of leaf litter in the functioning of forest ecosystems. Biol Rev 81(1):1–31
Sayer EJ, Tanner EVJ (2010) Experimental investigation of the importance of litterfall in lowland semi-evergreen tropical forest nutrient cycling. J Ecol 98(5):1052–1062
Sayer EJ, Tanner EVJ, Cheesman AW (2006) Increased litterfall changes fine root distribution in a moist tropical forest. Plant Soil 281:5–13
Sayer EJ, Heard MS, Grant HK, Marthews TR, Tanner EVJ (2011) Soil carbon release enhanced by increased tropical forest litterfall. Nat Clim Chang 1:304–307
Sayer EJ, Wright SJ, Tanner EVJ, Yavitt JB, Harms KE, Powers JS, Kaspari M, Garcia MN (2012) Turner BL (2012) Variable responses of lowland tropical forest nutrient status to fertilization and litter manipulation. Ecosystems 15(3):387–400
Sayer EJ, Baxendale C, Birkett AJ, Bréchet LM, Castro B, Kerdraon-Byrne D, Lopez-Sangil L, Rodtassana C (2020a) Altered litter inputs modify carbon and nitrogen storage in soil organic matter in a lowland tropical forest. Biogeochemistry 156(1):1–16
Sayer EJ, Rodtassana C, Sheldrake M, Bréchet LM, Ashford O, Lopez-Sangil L, Kerdraon-Byrne D, Castro B, Turner BL, Wright SJ, Tanner EVJ (2020b) Revisiting nutrient cycling by litterfall: insights from 15 years of litter manipulation in old-growth lowland tropical forest. Adv Ecol Res 62:173–223
Schmidt MWI, Torn MS, Abiven S, Dittmar T, Guggenberger G, Janssens IA, Kleber M, Kögel-Knabner I, Lehmann J, Manning DAC, Nannipieri P, Rasse DP, Weiner S, Trumbore SE (2011) Persistence of soil organic matter as an ecosystem property. Nature 478:49–56
Silver WL, Thompson AW, Mcgroddy ME, Varner RK, Dias JD, Silva H, Crill PM, Keller M (2005) Fine root dynamics and trace gas fluxes in two lowland tropical forest soils. Glob Change Biol 11:290–306
Silver WL, Hall SJ, González G (2014) Differential effects of canopy trimming and litter deposition on litterfall and nutrient dynamics in a wet subtropical forest. Forest Ecol Manag 332:47–55
Sokol NW, Bradford MA (2019) Microbial formation of stable soil carbon is more efficient from belowground than aboveground input. Nat Geosci 12:46–53
Song J, Wan S, Piao S et al (2019) A meta-analysis of 1,119 manipulative experiments on terrestrial carbon-cycling responses to global change. Nat Ecol Evol 3:1309–1320
Spain AV (1984) Litterfall and the standing crop of litter in three tropical Australian rainforests. J Ecol 72(3):947–961
Tanner EVJ, Sheldrake MWA, Turner BL (2016) Changes in soil carbon and nutrients following 6 years of litter removal and addition in a tropical semi-evergreen rain forest. Biogeosciences 13:6183–6190
Tian DL, Peng YY, Yan WD, Fang X, Kang WX, Wang GJ, Chen XY (2010) Effects of thinning and litter fall removal on fine root production and soil organic carbon content in Masson pine plantations. Pedosphere 20(4):486–493
Vance ED, Brookes PC, Jenkinson DS (1987) An extraction method for measuring soil microbial biomass C. Soil Biol Biochem 19(6):703–707
Vasconcelos SS, Zarin DJ, Araujo MM, Rangel-Vasconcelost LGT, Carvalho CJR, Staudhammer CL, Oliveir FA (2008) Effects of seasonality, litter removal and dry-season irrigation on litterfall quantity and quality in eastern Amazonian forest regrowth, Brazil. J Trop Ecol 24:27–38
Vogt KA, Vogt DJ, Palmiotto PA, Boon P, O’Hara J, Asbjornsen H (1996) Review of root dynamics in forest ecosystems grouped by climate, climatic forest type and species. Plant Soil 187:159–219
Vogt KA, Vogt DJ, Bloomfield J (1998) Analysis of some direct and indirect methods for estimating root biomass and production of forests at an ecosystem level. Plant Soil 200:71–89
Wang R, Cheng R, Xiao W, Feng X, Ze L, Ge X, Wang X, Zhang W (2012) Fine root production and turnover in Pinus massoniana plantation in three gorges reservoir area of China. J Appl Ecol 23(9):2346–2352
Wang R, Cavagnaro TR, Jiang Y, Keitel C, Dijkstra FA (2021) Carbon allocation to the rhizosphere is affected by drought and nitrogen addition. J Ecol 109:3699–3709
Wood TE, Lawrence D, Clark DA, Chazdon RL (2009) Rain forest nutrient cycling and productivity in response to large-scale litter manipulation. Ecology 90(1):109–121
Wright SJ, Yavitt JB, Wurzburger N, Turner BL, Tanner EVJ, Sayer EJ, Santiago LS, Kaspari M, Hedin LO, Harms KE, Garcia MN, Corre MD (2011) Potassium, phosphorus, or nitrogen limit root allocation, tree growth, or litter production in a lowland tropical forest. Ecology 92(8):1616–1625
Wurzburger N, Wright SJ (2015) Fine-root responses to fertilization reveal multiple nutrient limitation in a lowland tropical forest. Ecology 96(8):2137–2146
Xu S, Sayer EJ, Eisenhauer N, Lu X, Wang J, Liu C (2021) Aboveground litter inputs determine carbon storage across soil profiles: a meta-analysis. Plant Soil 462:429–444
Yin H, Li Y, Xiao J, Xu Z, Cheng X, Liu Q (2013) Enhanced root exudation stimulates soil nitrogen transformations in a subalpine coniferous forest under experimental warming. Glob Change Biol 19(7):2158–2167
Yuan Y, Zhao W, Zhang Z, Xiao J, Li D, Liu Q, Yin H (2018) Impacts of oxalic acid and glucose additions on N transformation in microcosms via artificial roots. Soil Biol Biochem 121:16–23
Zhang X, Wu K (2001) Fine-root production and turnover for forest ecosystems. Sci Silvae Sin 37(3):126–138
Funding
This study was financially supported by the National Natural Science Foundation of China (No. 32060339) and Guizhou Forestry Scientific Research Project (J[2018]06).
Author information
Authors and Affiliations
Contributions
QZ and TH conceived the ideas and designed methodology. YC and XL carried out the laboratory analyses and conducted the fieldwork. TZ collected the data. CZ contributed to the analysis and interpretation of data and wrote the main manuscript text. JL helped in formal analysis, visualization, and writing—review. All authors contributed critically to the drafts and gave final approval for publication.
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing interests.
Conflict of interest
The authors declare that they have no known competing financial interests or personal relationship that could have appeared to influence the work reported in this paper.
Additional information
Communicated by Agustin Merino.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor 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
Zhang, C., Cai, Y., Zhang, T. et al. Litter removal increases the plant carbon input to soil in a Pinus massoniana plantation. Eur J Forest Res 141, 833–843 (2022). https://doi.org/10.1007/s10342-022-01476-2
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10342-022-01476-2