Plant and Soil

, Volume 444, Issue 1–2, pp 153–164 | Cite as

Root–microbial interaction accelerates soil nitrogen depletion but not soil carbon after increasing litter inputs to a coniferous forest

  • Maokui Lyu
  • Xiaojie Li
  • Jinsheng XieEmail author
  • Peter M. Homyak
  • Liisa Ukonmaanaho
  • Zhijie Yang
  • Xiaofei Liu
  • Chaoyue Ruan
  • Yusheng Yang
Regular Article



Net primary productivity is expected to increase in many forests as Earth warms, which can increase litter inputs to soils and affect carbon (C) and nitrogen (N) dynamics. Understanding how increasing litter inputs affect soil C and N cycling in tropical and subtropical forests is important because they represent some of the most productive ecosystems on Earth, suggesting that small changes in these cycles can have large effects.


To test the effects of increased litter inputs and the interactive effect between microbes and roots on soil C and N stocks and dynamics, we manipulated litter inputs and used trenching to exclude roots in a 40-year-old Cunninghamia lanceolata Lamb. (Chinese fir) plantation. At the site, we measured soil C and N pools, soil 13C and 15N natural abundance, and potential activities for C-, N-, and phosphorus-acquiring enzymes.


After four years of experimental treatment, we found that increasing litter inputs reduced total soil N content by 26% relative to background litter inputs, but that increasing litter inputs did not affect soil C content in the plots with roots. In the plots without roots, both soil N and C did not change in response to litter inputs. In the plots with roots, soil δ15N increased with increasing litter inputs, but there was no effect in the plots without roots. We found a strong interactive effect between root and litter treatment on soil N pools and δ15N. The decline in soil N pools and increase in soil δ15N were associated with elevated potential enzyme activity for N-acquisition (N-acetyl glucosaminidase).


Adding litter did not have a significant effect on soil C pools, likely because potential soil C losses were offset by increasing litter-derived C inputs. In contrast to C, adding litter decreased N availability, likely through multiple pathways including gaseous N losses, NO3 leaching, root N uptake, and interactions between saprotrophic microbes and roots during the four-year litter addition experiment. Global changes that increase litter production may lower N pools and imbalance C and N cycling in subtropical coniferous forest ecosystems.


Litter addition N depletion C and N stable isotopes Root-microbes interaction Chinese fir Subtropics 



The research was funded by the National key research and development program (No. 2016YFD0600204) and the National Natural Science Foundation of China (Nos U1505233, 31870604 and U1405231).

Supplementary material

11104_2019_4265_MOESM1_ESM.docx (329 kb)
ESM 1 (DOCX 328 kb)


  1. Amundson R, Austin AT, Schuur EA, Yoo K, Matzek V, Kendall C, Uebersax A, Brenner D, Baisden WT (2003) Global patterns of the isotopic composition of soil and plant nitrogen. Glob Biogeochem Cy 17:1031Google Scholar
  2. Arai H, Tokuchi N (2010) Factors contributing to greater soil organic carbon accumulation after afforestation in a Japanese coniferous plantation as determined by stable and radioactive isotopes. Geoderma 157:243–251Google Scholar
  3. Bai E, Houlton BZ (2009) Coupled isotopic and process-based modeling of gaseous nitrogen losses from tropical rain forests. Glob Biogeochem Cy 23:GB2011Google Scholar
  4. Bingeman C, Varner J, Martin W (1953) The effect of the addition of organic materials on the decomposition of an organic soil. Soil Sci Soc Am J 17:34–38Google Scholar
  5. Brenner DL, Amundson R, Baisden WT, Kendall C, Harden J (2001) Soil N and 15N variation with time in a California annual grassland ecosystem. Geochim Cosmochim Acta 65:4171–4186Google Scholar
  6. Brockerhoff EG, Jactel H, Parrotta JA, Quine CP, Sayer J (2008) Plantation forests and biodiversity: oxymoron or opportunity? Biodivers Conserv 17:925–951Google Scholar
  7. Brzostek ER, Greco A, Drake JE, Finzi AC (2013) Root carbon inputs to the rhizosphere stimulate extracellular enzyme activity and increase nitrogen availability in temperate forest soils. Biogeochemistry 115:65–76Google Scholar
  8. Brzostek ER, Dragoni D, Brown ZA, Phillips RP (2015) Mycorrhizal type determines the magnitude and direction of root–induced changes in decomposition in a temperate forest. New Phytol 206:1274–1282Google Scholar
  9. Castellano MJ, Mueller KE, Olk DC, Sawyer JE, Six J (2015) Integrating plant litter quality, soil organic matter stabilization, and the carbon saturation concept. Glob Chang Biol 21:3200–3209PubMedGoogle Scholar
  10. Cernusak LA, Winter K, Dalling JW, Holtum JA, Jaramillo C, Körner C, Leakey AD, Norby RJ, Poulter B, Turner BL (2013) Tropical forest responses to increasing atmospheric CO2: current knowledge and opportunities for future research. Funct Plant Biol 40:531–551Google Scholar
  11. Chen X, Chen HY (2018) Global effects of plant litter alterations on soil CO2 to the atmosphere. Glob Chang Biol 24:3462–3471PubMedGoogle Scholar
  12. Cheng L, Booker FL, Tu C, Burkey KO, Zhou LS, Shew HD, Rufty TW, Hu SJ (2012) Arbuscular mycorrhizal fungi increase organic carbon decomposition under elevated CO2. Science 337:1084–1087PubMedGoogle Scholar
  13. Coskun D, Britto DT, Shi W, Kronzucker HJ (2017) How plant root exudates shape the nitrogen cycle. Trends Plant Sci 22:661–673PubMedGoogle Scholar
  14. 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 Chang Biol 19:988–995PubMedGoogle Scholar
  15. Crow SE, Lajtha K, Bowden RD, Yano Y, Brant JB, Caldwell BA, Sulzman EW (2009) Increased coniferous needle inputs accelerate decomposition of soil carbon in an old-growth forest. For Ecol Manag 258:2224–2232Google Scholar
  16. Dise NB, Rothwell JJ, Gauci V, Van der Salm C, De Vries W (2009) Predicting dissolved inorganic nitrogen leaching in European forests using two independent databases. Sci Total Environ 407:1798–1808PubMedGoogle Scholar
  17. Doughty CE, Metcalfe D, Girardin C, Amézquita FF, Cabrera DG, Huasco WH, Silva-Espejo J, Araujo-Murakami A, da Costa M, Rocha W (2015) Drought impact on forest carbon dynamics and fluxes in Amazonia. Nature 519:78–82PubMedGoogle Scholar
  18. Drake JE, Gallet-Budynek A, Hofmockel KS, Bernhardt ES, Billings SA, Jackson RB, Johnsen KS, Lichter J, McCarthy HR, McCormack ML, Moore DJ (2011) Increases in the flux of carbon belowground stimulate nitrogen uptake and sustain the long-term enhancement of forest productivity under elevated CO2. Ecol Lett 14:349–357PubMedGoogle Scholar
  19. Fang X, Zhao L, Zhou G, Huang W, Liu J (2015a) Increased litter input increases litter decomposition and soil respiration but has minor effects on soil organic carbon in subtropical forests. Plant Soil 392:139–153Google Scholar
  20. Fang Y, Koba K, Makabe A, Takahashi C, Zhu W, Hayashi T, Hokari AA, Urakawa R, Bai E, Houlton BZ, Xi D (2015b) Microbial denitrification dominates nitrate losses from forest ecosystems. PNAS 112:1470–1474PubMedGoogle Scholar
  21. FAO (2006) Global forest resources assessment 2005: progress towards sustainable forest management. Food and Agriculture Organization of the United Nations, RomeGoogle Scholar
  22. Fekete I, Kotroczo Z, Varga C, Nagy PT, Varbiro G, Bowden RD, Toth JA, Lajtha K (2014) Alterations in forest detritus inputs influence soil carbon concentration and soil respiration in a central-European deciduous forest. Soil Biol Biochem 74:106–114Google Scholar
  23. Fernandez CW, Kennedy PG (2016) Revisiting the ‘Gadgil effect’: do interguild fungal interactions control carbon cycling in forest soils? New Phytol 209:1382–1394PubMedGoogle Scholar
  24. Gadgil RL, Gadgil PD (1971) Mycorrhiza and litter decomposition. Nature 233:133PubMedGoogle Scholar
  25. Gai JP, Christie P, Feng G, Li XL (2006) Twenty years of research on community composition and species distribution of arbuscular mycorrhizal fungi in China: a review. Mycorrhiza 16:229–239PubMedGoogle Scholar
  26. Gatti L, Gloor M, Miller J, Doughty C, Malhi Y, Domingues L, Basso L, Martinewski A, Correia C, Borges V (2014) Drought sensitivity of Amazonian carbon balance revealed by atmospheric measurements. Nature 506:76–80PubMedGoogle Scholar
  27. Gentile R, Vanlauwe B, Six J (2011) Litter quality impacts short- but not long-term soil carbon dynamics in soil aggregate fractions. Ecol Appl 21:695–703PubMedGoogle Scholar
  28. Giardina CP, Ryan MG (2002) Total belowground carbon allocation in a fast-growing Eucalyptus plantation estimated using a carbon balance approach. Ecosystems 5:487–499Google Scholar
  29. Gleeson SK, Good RE (2003) Root allocation and multiple nutrient limitation in the New Jersey pinelands. Ecol Lett 6:220–227Google Scholar
  30. Grandy AS, Neff JC (2008) Molecular C dynamics downstream: the biochemical decomposition sequence and its impact on soil organic matter structure and function. Sci Total Environ 404:297–307Google Scholar
  31. Handley LL, Raven JA (1992) The use of natural abundance of nitrogen isotopes in plant physiology and ecology. Plant Cell Environ 15:965–985Google Scholar
  32. Hickler T, Smith B, Prentice IC, Mjöfors K, Miller P, Arneth A, Sykes MT (2008) CO2 fertilization in temperate FACE experiments not representative of boreal and tropical forests. Glob Chang Biol 14:1531–1542Google Scholar
  33. Hobbie EA (2005) Using isotopic tracers to follow carbon and nitrogen cycling in fungi. In: Dighton J, White JF, Oudemans P (eds) The Fungal Community: Its Organization and Role in the Ecosystem. Taylor & Francis, Boca Raton, pp 361–381Google Scholar
  34. Högberg P (1997) Tansley review no. 95 15N natural abundance in soil–plant systems. New Phytol 137:179–203Google Scholar
  35. Högberg P, Nordgren A, Buchmann N, Taylor AFS, Ekblad A, Högberg MN, Nyberg G, Ottosson-Löfvenius M, Read DJ (2001) Large-scale forest girdling shows that current photosynthesis drives soil respiration. Nature 411:789–792PubMedGoogle Scholar
  36. Homyak PM, Yanai RD, Burns DA, Briggs RD, Germain RH (2008) Nitrogen immobilization by wood-chip application: protecting water quality in a northern hardwood forest. Forest Ecol Manag 255:2589–2601Google Scholar
  37. Homyak PM, Blankinship JC, Marchus K, Lucero DM, Sickman JO, Schimel JP (2016) Aridity and plant uptake interact to make dryland soils hotspots for nitric oxide (NO) emissions. PNAS 113:E2608–E2616Google Scholar
  38. Houlton BZ, Sigman DM, Hedin LO (2006) Isotopic evidence for large gaseous nitrogen losses from tropical rainforests. PNAS 103:8745–8750PubMedGoogle Scholar
  39. Huang ZQ, He ZM, Wan XH, Hu ZH, Fan SH, Yang YS (2013) Harvest residue management effects on tree growth and ecosystem carbon in a Chinese fir plantation in subtropical China. Plant Soil 364:303–314Google Scholar
  40. Jenkinson DS, Fox RH, Rayner JH (1985) Interactions between fertilizer nitrogen and soil nitrogen-the so-called priming effect. Eur J Soil Sci 36:425–444Google Scholar
  41. Klein T, Bader MKF, Leuzinger S, Mildner M, Schleppi P, Siegwolf RT, Körner C (2016) Growth and carbon relations of mature Picea abies trees under 5 years of free-air CO2 enrichment. J Ecol 104:1720–1733Google Scholar
  42. Krapp A (2015) Plant nitrogen assimilation and its regulation: a complex puzzle with missing pieces. Curr Opin Plant Biol 25:115–122PubMedGoogle Scholar
  43. 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 Chang Biol 18:2969–2979PubMedGoogle Scholar
  44. Li XJ, Liu XF, Xiong DC, Lin WS, Lin TW, Shi YW, Xie JS, Yang YS (2016) Impact of litterfall addition and exclusion on soil respiration in Cunninghamia lanceolata plantation and secondary Castanopsis carlesii forest in mid-subtropical China. Chin J Plant Ecol 40:447–457Google Scholar
  45. Liang J, Zhou Z, Huo C, Shi Z, Cole JR, Huang L, Konstantinidis KT, Li X, Liu B, Luo Z, Penton CR, Schuur EAG, Tiedje JM, Wang Y, Wu L, Xia J, Zhou J, Luo Y (2018) More replenishment than priming loss of soil organic carbon with additional carbon input. Nat Commun 9:3175PubMedPubMedCentralGoogle Scholar
  46. Lin C, Yang Y, Guo J, Chen G, Xie J (2011) Fine root decomposition of evergreen broadleaved and coniferous tree species in midsubtropical China: dynamics of dry mass, nutrient and organic fractions. Plant Soil 338:311–327Google Scholar
  47. Lindahl BD, de Boer W, Finlay RD (2010) Disruption of root carbon transport into forest humus stimulates fungal opportunists at the expense of mycorrhizal fungi. Isme J 4:872–881PubMedGoogle Scholar
  48. Liu XF, Lin TC, Yang ZJ, Vadeboncoeur MA, Lin CF, Xiong DC, Lin WS, Chen GS, Xie JS, Li YQ, Yang YS (2017) Increased litter in subtropical forests boosts soil respiration in natural forests but not plantations of Castanopsis carlesii. Plant Soil 418:141–151Google Scholar
  49. Lü MK, Xie JS, Wang C, Guo JF, Wang MH, Liu XF, Chen YM, Chen GS, Yang YS (2015) Forest conversion stimulated deep soil C losses and decreased C recalcitrance through priming effect in subtropical China. Biol Fertil Soils 51:857–867Google Scholar
  50. Lyu MK, Xie JS, Ukonmaanaho L, Jiang MH, Li YQ, Chen YM, Yang ZJ, Zhou YX, Lin WS, Yang YS (2017) Land-use change exerts a strong impact on deep soil C stabilization in subtropical forests. J Soils Sediments 17:2305–2317Google Scholar
  51. Lyu MK, Xie JS, Vadeboncoeur MA, Wang MH, Qiu X, Ren YB, Jiang MH, Yang YS, Kuzyakov Y (2018) Simulated leaf litter addition causes opposite priming effects on natural forest and plantation soils. Biol Fertil Soils 54:925–934Google Scholar
  52. Lyu MK, Nie YY, Giardina CP, Vadeboncoeur MA, Ren YB, Fu ZQ, Wang MH, Jin CS, Liu XM, Xie J (2019) Litter quality and site characteristics interact to affect the response of priming effect to temperature in subtropical forests. Funct Ecol. Google Scholar
  53. Marklein AR, Winbourne JB, Enders SK, Gonzalez DJ, van Huysen TL, Izquierdo JE, Light DR, Liptzin D, Miller KE, Morford SL, Norton RA (2016) Mineralization ratios of nitrogen and phosphorus from decomposing litter in temperate versus tropical forests. Glob Ecol Biogeogr 25:335–346Google Scholar
  54. McCormack ML, Adams TS, Smithwick EAH, Eissenstat DM (2014) Variability in root production, phenology, and turnover rate among 12 temperate tree species. Ecology 95:2224–2235Google Scholar
  55. Mo J, Brown S, Xue J, Fang Y, Li Z (2006) Response of litter decomposition to simulated N deposition in disturbed, rehabilitated and mature forests in subtropical China. Plant Soil 282:135–151Google Scholar
  56. Nadelhoffer KJ, Boone RD, Bowden RD, Canary JD, Kaye J, Micks P, Ricca A, Aitkenhead JA, Lajtha K, McDowell WH (2004) The DIRT experiment: litter and root influences on forest soil organic matter stocks and function. In: Foster D, Aber J (eds) Forests in time: the environmental consequences of 1000 years of change in New England. Yale University Press, New Haven, pp 300–315Google Scholar
  57. Phillips RP, Fahey TJ (2005) Patterns of rhizosphere carbon flux in sugar maple (Acer saccharum) and yellow birch (Betula allegheniensis) saplings. Glob Chang Biol 11:983–995Google Scholar
  58. Phillips RP, Brzostek E, Midgley MG (2013) The mycorrhizal-associated nutrient economy: a new framework for predicting carbon–nutrient couplings in temperate forests. New Phytol 199:41–51PubMedGoogle Scholar
  59. Raich JW, Russell AE, Kitayama K, Parton WJ, Vitousek PM (2006) Temperature influences carbon accumulation in moist tropical forests. Ecology 87:76–87PubMedGoogle Scholar
  60. Rasse DP, Rumpel C, Dignac MF (2005) Is soil carbon mostly root carbon? Mechanisms for a specific stabilisation. Plant Soil 269:341–356Google Scholar
  61. Read DJ, Perez-Moreno J (2003) Mycorrhizas and nutrient cycling in ecosystems – a journey towards relevance? New Phytol 157:475–492Google Scholar
  62. 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 99:735–742PubMedGoogle Scholar
  63. Saiya-Cork K, Sinsabaugh R, Zak D (2002) The effects of long term nitrogen deposition on extracellular enzyme activity in an Acer saccharum forest soil. Soil Biol Biochem 34:1309–1315Google Scholar
  64. Sayer EJ, Powers JS, Tanner EVJ (2007) Increased litterfall in tropical forests boosts the transfer of soil CO2 to the atmosphere. PLoS One 2:e1299–e1299PubMedPubMedCentralGoogle Scholar
  65. Sayer EJ, Heard MS, Grant HK, Marthews TR, Tanner EVJ (2011) Soil carbon release enhanced by increased tropical forest litterfall. Nat Clim Chang 1:304–307Google Scholar
  66. Sayer EJ, Wright SJ, Tanner EVJ, Yavitt JB, Harms KE, Powers JS, Kaspari M, Garcia MN, Turner BL (2012) Variable responses of lowland tropical forest nutrient status to fertilization and litter manipulation. Ecosystems 15:387–400Google Scholar
  67. Schimel JP, Bennett J (2004) Nitrogen mineralization: challenges of a changing paradigm. Ecology 85:591–602Google Scholar
  68. Shcherbak I, Millar N, Robertson GP (2014) Global meta-analysis of the nonlinear response of soil nitrous oxide (N2O) emissions to fertilizer nitrogen. PNAS 111:9199–9204PubMedGoogle Scholar
  69. Sokol NW, Bradford MA (2019) Microbial formation of stable soil carbon is more efficient from belowground than aboveground input. Nat Geosci 12:46–53Google Scholar
  70. Talbot JM, Allison SD, Treseder KK (2008) Decomposers in disguise: mycorrhizal fungi as regulators of soil C dynamics in ecosystems under global change. Funct Ecol 22:955–963Google Scholar
  71. Vance E, Brookes P, Jenkinson D (1987) An extraction method for measuring soil microbial biomass C. Soil Biol Biochem 19:703–707Google Scholar
  72. Wan X, Huang Z, He Z, Yu Z, Wang M, Davis MR, Yang Y (2015) Soil C: N ratio is the major determinant of soil microbial community structure in subtropical coniferous and broadleaf forest plantations. Plant Soil 387:103–116Google Scholar
  73. Weintraub MN, Scott-Denton LE, Schmidt SK, Monson RK (2007) The effects of tree rhizodeposition on soil exoenzyme activity, dissolved organic carbon, and nutrient availability in a subalpine forest ecosystem. Oecologia 154:327–338PubMedGoogle Scholar
  74. Wiesmeier M, Urbanski L, Hobley E, Lang B, von Lützow M, Marin-Spiotta E, van Wesemael B, Rabot E, Ließ M, Garcia-Franco N, Wollschläger U (2019) Soil organic carbon storage as a key function of soils-a review of drivers and indicators at various scales. Geoderma 333:149–162Google Scholar
  75. Xu S, Liu L, Sayer E (2013) Variability of above-ground litter inputs alters soil physicochemical and biological processes: a meta-analysis of litterfall-manipulation experiments. Biogeosciences 10 (11):7423–7433Google Scholar
  76. Yin H, Wheeler E, Phillips RP (2014) Root-induced changes in nutrient cycling in forests depend on exudation rates. Soil Biol Biochem 78:213–221Google Scholar
  77. Zhang JB, Zhu TB, Cai ZC, Müller C (2011) Nitrogen cycling in forest soils across climate gradients in eastern China. Plant Soil 342:419–432Google Scholar
  78. Zhang JB, Yu YJ, Zhu TB, Cai ZC (2014) The mechanisms governing low denitrification capacity and high nitrogen oxide gas emissions in subtropical forest soils in China. J Geophys Res Biogeosci 119:1670–1683Google Scholar
  79. Zhang QF, Xie JS, Lyu MK, Xiong DC, Wang J, Chen YM, Li YQ, Wang MK, Yang YS (2017) Short-term effects of soil warming and nitrogen addition on the N: P stoichiometry of Cunninghamia lanceolata in subtropical regions. Plant Soil 411:395–407Google Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Key Laboratory for Subtropical Mountain Ecology (Ministry of Science and Technology and Fujian Province Funded), School of Geographical SciencesFujian Normal UniversityFuzhouChina
  2. 2.Department of Environmental SciencesUniversity of CaliforniaRiversideUSA
  3. 3.Natural Resources Institute FinlandHelsinkiFinland
  4. 4.Institute of Geographical ScienceFujian Normal UniversityFuzhouChina

Personalised recommendations