Skip to main content
Log in

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

  • Regular Article
  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

Aims

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.

Methods

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.

Results

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).

Conclusions

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • 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 17:1031

    Google Scholar 

  • 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 157:243–251

    CAS  Google Scholar 

  • Bai E, Houlton BZ (2009) Coupled isotopic and process-based modeling of gaseous nitrogen losses from tropical rain forests. Glob Biogeochem Cy 23:GB2011

    Google Scholar 

  • 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 17:34–38

    CAS  Google Scholar 

  • 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 65:4171–4186

    CAS  Google Scholar 

  • Brockerhoff EG, Jactel H, Parrotta JA, Quine CP, Sayer J (2008) Plantation forests and biodiversity: oxymoron or opportunity? Biodivers Conserv 17:925–951

    Google Scholar 

  • 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 115:65–76

    CAS  Google Scholar 

  • 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 206:1274–1282

    CAS  Google Scholar 

  • 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 21:3200–3209

    PubMed  Google Scholar 

  • 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 40:531–551

    CAS  Google Scholar 

  • Chen X, Chen HY (2018) Global effects of plant litter alterations on soil CO2 to the atmosphere. Glob Chang Biol 24:3462–3471

    PubMed  Google Scholar 

  • 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 337:1084–1087

    CAS  PubMed  Google Scholar 

  • Coskun D, Britto DT, Shi W, Kronzucker HJ (2017) How plant root exudates shape the nitrogen cycle. Trends Plant Sci 22:661–673

    CAS  PubMed  Google Scholar 

  • 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 19:988–995

    PubMed  Google Scholar 

  • 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 258:2224–2232

    Google Scholar 

  • 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 407:1798–1808

    CAS  PubMed  Google Scholar 

  • 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 519:78–82

    CAS  PubMed  Google Scholar 

  • 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 14:349–357

    PubMed  Google Scholar 

  • 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 392:139–153

    CAS  Google Scholar 

  • 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 112:1470–1474

    CAS  PubMed  Google Scholar 

  • FAO (2006) Global forest resources assessment 2005: progress towards sustainable forest management. Food and Agriculture Organization of the United Nations, Rome

    Google Scholar 

  • 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 74:106–114

    CAS  Google Scholar 

  • Fernandez CW, Kennedy PG (2016) Revisiting the ‘Gadgil effect’: do interguild fungal interactions control carbon cycling in forest soils? New Phytol 209:1382–1394

    CAS  PubMed  Google Scholar 

  • Gadgil RL, Gadgil PD (1971) Mycorrhiza and litter decomposition. Nature 233:133

    CAS  PubMed  Google Scholar 

  • 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 16:229–239

    CAS  PubMed  Google Scholar 

  • 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 506:76–80

    CAS  PubMed  Google Scholar 

  • Gentile R, Vanlauwe B, Six J (2011) Litter quality impacts short- but not long-term soil carbon dynamics in soil aggregate fractions. Ecol Appl 21:695–703

    PubMed  Google Scholar 

  • Giardina CP, Ryan MG (2002) Total belowground carbon allocation in a fast-growing Eucalyptus plantation estimated using a carbon balance approach. Ecosystems 5:487–499

    CAS  Google Scholar 

  • Gleeson SK, Good RE (2003) Root allocation and multiple nutrient limitation in the New Jersey pinelands. Ecol Lett 6:220–227

    Google Scholar 

  • 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 404:297–307

    CAS  Google Scholar 

  • Handley LL, Raven JA (1992) The use of natural abundance of nitrogen isotopes in plant physiology and ecology. Plant Cell Environ 15:965–985

    CAS  Google Scholar 

  • 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 14:1531–1542

    Google Scholar 

  • 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 361–381

    Google Scholar 

  • Högberg P (1997) Tansley review no. 95 15N natural abundance in soil–plant systems. New Phytol 137:179–203

    Google Scholar 

  • 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 411:789–792

    PubMed  Google Scholar 

  • 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 255:2589–2601

    Google Scholar 

  • 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–E2616

    CAS  Google Scholar 

  • Houlton BZ, Sigman DM, Hedin LO (2006) Isotopic evidence for large gaseous nitrogen losses from tropical rainforests. PNAS 103:8745–8750

    CAS  PubMed  Google Scholar 

  • 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 364:303–314

    CAS  Google Scholar 

  • Jenkinson DS, Fox RH, Rayner JH (1985) Interactions between fertilizer nitrogen and soil nitrogen-the so-called priming effect. Eur J Soil Sci 36:425–444

    CAS  Google Scholar 

  • 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 104:1720–1733

    CAS  Google Scholar 

  • Krapp A (2015) Plant nitrogen assimilation and its regulation: a complex puzzle with missing pieces. Curr Opin Plant Biol 25:115–122

    CAS  PubMed  Google Scholar 

  • 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 18:2969–2979

    PubMed  Google Scholar 

  • 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 40:447–457

    Google Scholar 

  • 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 9:3175

    PubMed  PubMed Central  Google Scholar 

  • 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 338:311–327

    CAS  Google Scholar 

  • 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 4:872–881

    PubMed  Google Scholar 

  • 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 418:141–151

    CAS  Google Scholar 

  • 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 51:857–867

    Google Scholar 

  • 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 17:2305–2317

    CAS  Google Scholar 

  • 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 54:925–934

    CAS  Google Scholar 

  • 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. https://doi.org/10.1111/1365-2435.13428

    Google Scholar 

  • 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 25:335–346

    Google Scholar 

  • McCormack ML, Adams TS, Smithwick EAH, Eissenstat DM (2014) Variability in root production, phenology, and turnover rate among 12 temperate tree species. Ecology 95:2224–2235

    Google Scholar 

  • 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 282:135–151

    CAS  Google Scholar 

  • 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 300–315

    Google Scholar 

  • Phillips RP, Fahey TJ (2005) Patterns of rhizosphere carbon flux in sugar maple (Acer saccharum) and yellow birch (Betula allegheniensis) saplings. Glob Chang Biol 11:983–995

    Google Scholar 

  • 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 199:41–51

    CAS  PubMed  Google Scholar 

  • Raich JW, Russell AE, Kitayama K, Parton WJ, Vitousek PM (2006) Temperature influences carbon accumulation in moist tropical forests. Ecology 87:76–87

    PubMed  Google Scholar 

  • Rasse DP, Rumpel C, Dignac MF (2005) Is soil carbon mostly root carbon? Mechanisms for a specific stabilisation. Plant Soil 269:341–356

    CAS  Google Scholar 

  • Read DJ, Perez-Moreno J (2003) Mycorrhizas and nutrient cycling in ecosystems – a journey towards relevance? New Phytol 157:475–492

    Google Scholar 

  • 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 99:735–742

    CAS  PubMed  Google Scholar 

  • 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 34:1309–1315

    CAS  Google Scholar 

  • 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–e1299

    PubMed  PubMed Central  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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 15:387–400

    CAS  Google Scholar 

  • Schimel JP, Bennett J (2004) Nitrogen mineralization: challenges of a changing paradigm. Ecology 85:591–602

    Google Scholar 

  • Shcherbak I, Millar N, Robertson GP (2014) Global meta-analysis of the nonlinear response of soil nitrous oxide (N2O) emissions to fertilizer nitrogen. PNAS 111:9199–9204

    CAS  PubMed  Google Scholar 

  • Sokol NW, Bradford MA (2019) Microbial formation of stable soil carbon is more efficient from belowground than aboveground input. Nat Geosci 12:46–53

    CAS  Google Scholar 

  • 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 22:955–963

    Google Scholar 

  • Vance E, Brookes P, Jenkinson D (1987) An extraction method for measuring soil microbial biomass C. Soil Biol Biochem 19:703–707

    CAS  Google Scholar 

  • 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 387:103–116

    CAS  Google Scholar 

  • 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 154:327–338

    PubMed  Google Scholar 

  • 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 333:149–162

    CAS  Google Scholar 

  • 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):7423–7433

    Google Scholar 

  • Yin H, Wheeler E, Phillips RP (2014) Root-induced changes in nutrient cycling in forests depend on exudation rates. Soil Biol Biochem 78:213–221

    CAS  Google Scholar 

  • Zhang JB, Zhu TB, Cai ZC, Müller C (2011) Nitrogen cycling in forest soils across climate gradients in eastern China. Plant Soil 342:419–432

    CAS  Google Scholar 

  • 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 119:1670–1683

    CAS  Google Scholar 

  • 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 411:395–407

    CAS  Google Scholar 

Download references

Acknowledgments

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).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jinsheng Xie.

Additional information

Responsible Editor: Alfonso Escudero.

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Maokui Lyu and Xiaojie Li co-first authors.

Electronic supplementary material

ESM 1

(DOCX 328 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lyu, M., Li, X., Xie, J. et al. Root–microbial interaction accelerates soil nitrogen depletion but not soil carbon after increasing litter inputs to a coniferous forest. Plant Soil 444, 153–164 (2019). https://doi.org/10.1007/s11104-019-04265-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-019-04265-w

Keywords

Navigation