Skip to main content

Advertisement

SpringerLink
Log in

Priming alters soil carbon dynamics during forest succession

  • Original Paper
  • Published:
Biology and Fertility of Soils Aims and scope Submit manuscript

Abstract

The mechanisms underlying soil organic carbon (C) dynamics during forest succession remain challenged because amount, quality, and composition of C inputs change with tree growth and species composition. Soils were collected from two stages (grassland and young secondary forest) of secondary succession after the clear-cut of primary old-growth forest due to land-use change, with a native old-growth forest (undisturbed for more than 200 years) as the reference. Soil samples were incubated for 170 days and the priming effects were quantified by one pulse addition of 13C-labeled glucose. 13C-PLFAs (phospholipid fatty acids) were analyzed to identify microbial functional groups utilizing glucose and to explore their accordance with SOM priming during succession. Soil C was primed much more strongly in young secondary forest than in grassland or old-growth forest. Priming resulted in large C losses (negative net C balance) in young-forest soil, whereas C stocks increased in grassland and old-growth forest (positive net C balance). Microbial composition assessed by PLFA and utilization of easily available organics (13C-PLFA) indicated that fungi were mainly responsible for priming in young-forest soil. Consequently, labile C released by litter decomposition and root exudation together with the availability of soil nutrients determines microbial functional groups that decompose soil organic matter during initial succession. These findings provide novel ecological connections between soil organic matter dynamics and C (de)stabilization with microbial functioning during forest succession and show that priming direction and intensity is important to distinguish soil C dynamics in young- and old-growth forests.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Bao S (2000) Agro-chemical analyses of soils. China Agriculture Press, Beijing, China

  • Barton K (2012) Package ‘MuMIn’: multi-model inference. R Package, Version 1 (7), 11

  • Berhongaray G, Cotrufo FM, Janssens IA, Ceulemans R (2018) Below-ground carbon inputs contribute more than above-ground inputs to soil carbon accrual in a bioenergy poplar plantation. Plant Soil 434:363–378. https://doi.org/10.1007/s11104-018-3850-z

    Article  CAS  Google Scholar 

  • Blagodatskaya E, Kuzyakov Y (2013) Active microorganisms in soil: critical review of estimation criteria and approaches. Soil Biol Biochem 67:192–211

    Article  CAS  Google Scholar 

  • Blagodatskaya Е, Kuzyakov Y (2008) Mechanisms of real and apparent priming effects and their dependence on soil microbial biomass and community structure: critical review. Biol Fertil Soils 45:115–131

    Article  Google Scholar 

  • Bloom AA, Exbrayat J-F, van der Velde IR, Feng L, Williams M (2016) The decadal state of the terrestrial carbon cycle: global retrievals of terrestrial carbon allocation, pools, and residence times. PNAS 113:1285–1290

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Borcard D, Gillet F, Legendre P (2011) Numerical ecology with R. Springer New York

  • Bormann FH, Likens GE (1979) Catastrophic disturbance and the steady state in northern hardwood forests: a new look at the role of disturbance in the development of forest ecosystems suggests important implications for land-use policies. Am Sci 67:660–669

    Google Scholar 

  • Bremner JM (1960) Determination of nitrogen in soil by the Kjeldahl method. J Agri Sci 55:11–33

    Article  CAS  Google Scholar 

  • Chapin FS, Matson PA, Vitousek PM (2012) Principles of terrestrial ecosystem ecology, 2nd edn. Springer, New York

    Google Scholar 

  • Chen RR, Mehmet S, Blagodatskaya S, Olga M, Klaus D, Lin XG, Blagodatskaya E (2014) Soil C and N availability determine the priming effect: microbial N mining and stoichiometric decomposition theories. Glob Change Biol 20:2356–2367

    Article  Google Scholar 

  • Chen J, Seven J, Zilla T, Dippold MA, Blagodatskaya E, Kuzyakov Y (2019) Microbial C: N: P stoichiometry and turnover depend on nutrients availability in soil: a 14C, 15N and 33P triple labelling study. Soil Biol Biochem 131:206–216

    Article  CAS  Google Scholar 

  • Cheng W, Johnson DW, Fu S (2003) Rhizosphere effects on decomposition. Soil Sci Soc Am J 67:1418–1427

    Article  CAS  Google Scholar 

  • Cheng WX, Parton WJ, Gonzalez-Meler MA, Philips R, Asao S, McNickle GG, Brzostek E, Jastrow JD (2014) Synthesis and modeling perspectives of rhizosphere priming. New Phytol 201:31–44

    Article  CAS  PubMed  Google Scholar 

  • Derrien D, Plain C, Courty PE, Gelhaye L, Moerdijk-Poortvliet TCW, Thomas E, Versini A, Zeller B, Koutika LS, Boschker HTS, Epron D (2014) Does the addition of labile substrate destabilise old soil organic matter? Soil Biol Biochem 76:149–160

    Article  CAS  Google Scholar 

  • Dijkstra FA, Carrillo Y, Pendall E, Morgan JA (2013) Rhizosphere priming: a nutrient perspective. Front Microbiol 4:216

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dungait JAJ, Kemmitt SJ, Michallon L, Guo S, Wen Q, Brookes PC, Evershed RP (2011) Variable responses of the soil microbial biomass to trace concentrations of 13C-labelled glucose, using 13C-PLFA analysis. Eur J Soil Sci 62:117–126

    Article  CAS  Google Scholar 

  • Field CB, Kaduk J (2004) The carbon balance of an old-growth forest: building across approaches. Ecosystems 7:525–533

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Fontaine S, Henault C, Aamor A, Bdioui N, Bloor JMG, Maire V, Mary B, Revaillot S, Maron PA (2011) Fungi mediate long term sequestration of carbon and nitrogen in soil through their priming effect. Soil Biol Biochem 43:86–96

    Article  CAS  Google Scholar 

  • Fontaine S, Mariotti A, Abbadie L (2003) The priming effect of organic matter: a question of microbial competition? Soil Biol Biochem 35:837–843

    Article  CAS  Google Scholar 

  • Fontaine S, Stahl C, Klumpp K, Picon-Cochard C, Grise MM, Dezécache C, Ponchant L, Freycon V, Blanc L, Bonal D, Burban B, Soussana I-F, Blanfort V, Alvarez G. (2017) Response to editor to the comment by Schipper & Smith to our paper entitled “continuous soil carbon storage of old permanent pastures in Amazonia. Glob Change Biol 24:e732–e733

  • Fredeen AL, Bois CH, Janzen DT, Sanborn PT (2005) Comparison of coniferous forest carbon stocks between old-growth and young second-growth forests on two soil types in Central British Columbia. Can J For Res 35:1411–1421

    Article  CAS  Google Scholar 

  • Frostegård Å, Bååth E (1996) The use of phospholipid fatty acid analysis to estimate bacterial and fungal biomass in soil. Biol Fertil Soils 22:59–65

    Article  Google Scholar 

  • Frostegård Å, Bååth E, Tunlio A (1993) Shifts in the structure of soil microbial communities in limed forests as revealed by phospholipid fatty-acid analysis. Soil Biol Biochem 25:723–730

  • Garcia-Pausas J, Paterson E (2011) Microbial community abundance and structure are determinants of soil organic matter mineralisation in the presence of labile carbon. Soil Biol Biochem 43:1705–1713

    Article  CAS  Google Scholar 

  • Georgiadis P (2011) Accumulation of carbon and nitrogen in Swedish forest soils over stand age. (M.Sc. Thesis), Swedish University of Agricultural Sciences, Uppsala, Sweden

  • Gleixner G, Tefs C, Jordan A, Hammer M, Wirth C, Nueske A, Telz A, Schmidt UE, Glatzel S (2009) Soil carbon accumulation in old-growth forests. In: Wirth C, Gleixner G, Heimann M (Eds) Old-growth forests: function, fate and value. Ecol Stu 207:231–266

  • Gregory PJ, Atwell BJ (1991) The fate of carbon in pulse-labelled crops of barley and wheat. Plant Soil 136:205–213

    Article  CAS  Google Scholar 

  • Guariguata MR, Ostertag R (2001) Neotropical secondary forest succession: changes in structural and functional characteristics. For Ecol Manag 148:185–206

    Article  Google Scholar 

  • Guillaume T, Damris M, Kuzyakov Y (2015) Losses of soil carbon by converting tropical forest to plantations: erosion and decomposition estimated by δ13C. Glob Change Biol 21:3548–3560

    Article  Google Scholar 

  • Gunina A, Kuzyakov Y (2015) Sugars in soil and sweets for microorganisms: review of origin, content, composition and fate. Soil Biol Biochem 90:87–100

    Article  CAS  Google Scholar 

  • Harmon ME (2001) Carbon sequestration in forests: addressing the scale question. J For-Washington 99:24–29

    Google Scholar 

  • Harmon ME, Ferrell WK, Franklin JF (1990) Effects on carbon storage of conversion of old-growth forests to young forests. Science 247:699–702

    Article  CAS  PubMed  Google Scholar 

  • He L, Chen JM, Pan Y, Birdsey R, Kattge J (2012) Relationships between net primary productivity and forest stand age in US forests. Global Biogeochem Cy 26:GB3009

    Article  CAS  Google Scholar 

  • Heimann M, Reichstein M (2008) Terrestrial ecosystem carbon dynamics and climate feedbacks. Nature 451:289–292

    Article  CAS  PubMed  Google Scholar 

  • Huo C, Luo Y, Cheng W (2017) Rhizosphere priming effect: a meta-analysis. Soil Biol Biochem 111:78–84

    Article  CAS  Google Scholar 

  • Jackson ML (1967) Soil chemical analysis. Prentice Hall of India, Pvt. Ltd., New Delhi : 498

  • Kalembasa SJ, Jenkinson DS (1973) A comparative study of titrimetric and gravimetric methods for determination of organic carbon in soil. J Sci Food Agri 24:1085–1090

    Article  CAS  Google Scholar 

  • Kleber M, Eusterhues K, Keiluweit M, Mikutta C, Mikutta R, Nico PS (2015) Mineral–organic associations: formation, properties, and relevance in soil environments. Adv Agron 130:1–140

    Article  Google Scholar 

  • Kuzyakov Y (2010) Priming effects: interactions between living and dead organic matter. Soil Biol Biochem 42:1363–1371

  • Kuzyakov YV (2001) Tracer studies of carbon translocation by plants from the atmosphere into the soil (a review). Eurasian Soil Science 34:28–42

  • Kuzyakov Y, Blagodatskaya E (2015) Microbial hotspots and hot moments in soil: concept & review. Soil Biol Biochem 83:184–199

    Article  CAS  Google Scholar 

  • Kuzyakov Y, Friedel JK, Stahr K (2000) Review of mechanisms and quantification of priming effects. Soil Biol Biochem 32: 1485–1498

  • Kuzyakov Y, Gavrichkova O (2010) Review: time lag between photosynthesis and carbon dioxide efflux from soil: a review of mechanisms and controls. Glob Change Biol 16:3386–3406

    Article  Google Scholar 

  • Ladd JN, Foster R, Nannipieri P, Oades JM (1996) Soil structure and biological activity. In: Stotzky G, Bollag J-M (eds) Soil biochemistry, vol 9. Marcel Dekker, New York, pp 23–78

    Google Scholar 

  • Lewis SL, Lopez-Gonzalez G, Sonké B, Affum-Baffoe K, Baker TR, Ojo LO, Phillips OL, Reitsma JM, White L, Comiskey JA, Marie-Noël D, Ewango CEN, Feldpausch TR, Hamilton AC, Gloor M, Hart T, Hladik A, Lloyd J, Lovett JC, Makana J-R, Malhi Y, Mbago FM, Ndangalasi HJ, Peacocl J, Peh KS-H, Sheil D, Sunderland T, Swaine MD, Taplin J, Taylor D, Thomas SC, Votere R, Wöll H (2009) Increasing carbon storage in intact African tropical forests. Nature 457:1003–1006

    Article  CAS  PubMed  Google Scholar 

  • Luyssaert S, Schulze ED, Börner A, Knohl A, Hessenmöller D, Law BE, Ciais P, Grace J (2008) Old-growth forests as global carbon sinks. Nature 455:213–215

    Article  CAS  PubMed  Google Scholar 

  • Menge DN, Hedin LO, Pacala SW (2012) Nitrogen and phosphorus limitation over long-term ecosystem development in terrestrial ecosystems. PLoS One 7(8):e42045

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Miltner A, Bombach P, Schmidt-Brücken B, Kästner M (2012) SOM genesis: microbial biomass a significant source. Biogeochemistry 111:41–55

    Article  CAS  Google Scholar 

  • Mooshammer M, Wanek W, Zechmeister-Boltenstern S, Richter AA (2014) Stoichiometric imbalances between terrestrial decomposer communities and their resources: mechanisms and implications of microbial adaptations to their resources. Front Microbiol 5:22

    Article  PubMed  PubMed Central  Google Scholar 

  • Nguyen C (2003) Rhizodeposition of organic C by plant: mechanisms and controls. Agronomie 23:375–396

    Article  CAS  Google Scholar 

  • Norby RJ, Zak DR (2007) Ecological lessons from free-air CO2 enrichment (FACE) experiments. Ann Rev Ecol Evol Syst 42:181–203

    Article  Google Scholar 

  • Odum EP (1969) The strategy of ecosystem development. Science 164:262–270

    Article  CAS  PubMed  Google Scholar 

  • Olsen SR, Cole CV, Watanabe FS (1954) Estimation of available phosphorus in soils by extraction with sodium bicarbonate. USDA Circular No. 939, US Government Printing Office, Washington DC

  • Olson JS (1958) Rates of succession and soil changes on southern Lake Michigan sand dunes. Bot Gazette 119:125–170

    Article  CAS  Google Scholar 

  • Ostertag R, Marín-Spiotta E, Silver WL, Schulten J (2008) Litterfall and decomposition in relation to soil carbon pools along a secondary forest chronosequence in Puerto Rico. Ecosystems 11:701–714

    Article  CAS  Google Scholar 

  • Palta JA, Gregory PJ (1997) Drought affects the fluxes of carbon to roots and soil in 13C pulse-labelled plants of wheat. Soil Biol Biochem 29:1395–1403

    Article  CAS  Google Scholar 

  • Pan YD, Birdsey RA, Fang JY, Houghton R, Kauppi PE, Kurz WA, Phillips OL, Shvidenko A, Lewis SL, Canadell JG, Ciais P, Jackson RB, Pacala SW, McGuire AD, Piao SL, Rautiainen A, Sitch S, Hayes D (2011) A large and persistent carbon sink in the world's forests. Science 333:988–993

    Article  CAS  PubMed  Google Scholar 

  • Perveen N, Barot S, Alvarez G, Klumpp K, Martin R, Rapaport A, Herfurth D, Louault F, Fontaine S (2014) Priming effect and microbial diversity in ecosystem functioning and response to global change: a modeling approach using the SYMPHONY model. Glob Change Biol 20:1174–1190

    Article  Google Scholar 

  • Phillips OL, Malhi Y, Higuchi N, Laurance WF, Nunez PV, Vasquez RM, Laurance SG, Ferreira LV, Stern M, Brown S, Grace J (1998) Changes in the carbon balance of tropical forests: evidence from long-term plots. Science 282:439–442

    Article  CAS  PubMed  Google Scholar 

  • Poorter L, Bongers F, Aide TM, Zambrano AMA, Balvanera P, Becknell JM, Boukili V, Brancalion PHS, Broadbent EN, Chazdon RL, Craven D, de Almerida-Cortez JS, Cabral GAL, de Jong BHJ, Denslow JS, Dent DH, Dewalt SJ, Dupuy JM, Durán SM, Espírito-Santo MM, Fandino MC, César RG, Hall JS, Hernandez-Stefanoni JL, Jakovac CC, Junqueira AB, Kennard D, Letcher SG, Juan-Carlos L, Lohbeck M, Marín-Spiotta E, Martínez-Ramos M, Massoca P, Meave JA, Mesquita R, Mora F, Muñoz R, Nunes YRF, Ochoa-Gaona S, de Oliveira AA, Orihuela-Belmonte E, Peña-Claros M, Pérez-García EA, Piotto D, Powers JS, Rodríguez-Velázquez J, Romero-Pérez IE, Ruiz J, Saldarriaga JG, Sanchez-Azofeifa A, Schwartz NB, Steininger MK, Swenson NG, Toledo M, Uriarte M, van Breugel M, van der Wal H, Veloso MDM, Vester HFM, Vicentini A, Vieira ICG, Bentos TV, Williamson GB, Rozendaal DM (2016) Biomass resilience of neotropical secondary forests. Nature 530:211–214

    Article  CAS  PubMed  Google Scholar 

  • Pronk GJ, Heister K, Vogel C, Babin D, Bachmann J, Ding G, Ditterich F, Gerzabek MH, Giebler J, Hemkemeyer M, Kandeler E, Mouvenchery YK, Miltner A, Poll C, Schaumann GE, Smalla K, Steinbach A, Tanuwidjaja I, Tebbe CC, Wick LY, Woche SK, Totsche KU, Schloter M, Kögel-Knabner I (2017) Interaction of minerals, organic matter, and microorganisms during biogeochemical interface formation as shown by a series of artificial soil experiments. Biol Fertil Soils 53:9–22

    Article  CAS  Google Scholar 

  • Pregitzer KS, Euskirchen ES (2004) Carbon cycling and storage in world forests: biome patterns related to forest age. Glob Change Biol 10:2052–2077

    Article  Google Scholar 

  • Qiao N, Schaefer D, Blagodatskaya E, Zou XM, Xu XL, Kuzyakov Y (2014) Labile carbon retention compensates for CO2 released by priming in forest soils. Glob Change Biol 20:1943–1954

    Article  Google Scholar 

  • Qiao N, Xu XL, Hu Y, Blagodatskaya E, Liu Y, Schaefer D, Kuzyakov Y (2016) Carbon and nitrogen additions induce distinct priming effects along an organic-matter decay continuum. Sci Rep 6:19865

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schaaf W, Bens O, Fischer A, Gerke HH, Gerwin W, Grűnewald U, Holländer HM, Kőgel-Knabner I, Mutz M, Schloter M, Schulin R, Veste M, Winter S, Hűttl RF (2011) Patterns and processes of initial terrestrial-ecosystem development. J Plant Nutr Soil Sci 174:229–239

    Article  CAS  Google Scholar 

  • Shahzad T, Chenu C, Repinçay C, Mougin C, Ollier J-L, Fontaine S (2012) Plant clipping decelerates the mineralization of recalcitrant soil organic matter under multiple grassland species. Soil Biol Biochem 51:73–80

    Article  CAS  Google Scholar 

  • Schimel J, Schaeffer SM (2012) Microbial control over carbon cycling in soil. Fron Microbiol 3:348

    CAS  Google Scholar 

  • Schmidt MWI, Torn MS, Abiven S, Dittmar T, Guggenberger G, Janssens IA, Kleber M, Kögel-Knaber I, Lehmann J, Manning DA, Nannipieri P, Rasse DP, Weiner S, Trumbore SE (2011) Persistence of soil organic matter as an ecosystem property. Nature 478:49–56

    Article  CAS  PubMed  Google Scholar 

  • Schulz S, Brankatschk R, Dümig A, Kögel-Knabner I, Schloter M, Zeyer J (2013) The role of microorganisms at different stages of ecosystem development for soil formation. Biogeosciences 10:3983–3996

    Article  Google Scholar 

  • Shen YX, Liu WY, Cao M, Li YH (2007) Seasonal variation in density and species richness of soil seed-banks in karst forests and degraded vegetation in Central Yunnan, SW China. Seed Sci Res 17:99–108

    Article  Google Scholar 

  • Shen YX, Liu WY, Li YH, Cui JW (2005) Community ecology study on karst semi-humid evergreen broad-leaved forest at the central part of Yunnan. Guihaia 25:321–326

    Google Scholar 

  • Stahl C, Fontaine S, Klumpp K, Picon-Cochard C, Grise MM, Dezécache C, Ponchant L, Freycon V, Blanc L, Bonal D, Burban B, Soussana J-F, Burban B (2017) Continuous soil carbon storage of old permanent pastures in Amazonia. Glob Change Biol 23:3382–3392

    Article  Google Scholar 

  • Sullivan BW, Hart SC (2013) Evaluation of mechanisms controlling the priming of soil carbon along a substrate age gradient. Soil Biol Biochem 58:293–301

    Article  CAS  Google Scholar 

  • Tarnocai C, Canadell JG, Schuur EAG, Kuhry P, Mazhitova G, Zimov S (2009) Soil organic carbon pools in the northern circumpolar permafrost region. Glob Biogeochem Cycl 23:GB2023

    Article  CAS  Google Scholar 

  • Thornton B, Zhang Z, Mayes RW, Hogberg MN, Midwood AJ (2011) Can gas chromatography combustion isotope ratio mass spectrometry be used to quantify organic compound abundance? Rapid Commun Mass Spectrom 25:2433–2438

    Article  CAS  PubMed  Google Scholar 

  • Trumbore S, Brando P, Hartmann H (2015) Forest health and global change. Science 349:814–818

    Article  CAS  PubMed  Google Scholar 

  • Vitousek PM, Fahey T, Johnson DW, Swift MJ (1988) Element interactions in forest ecosystems: succession, allometry and input-output budgets. Biogeochemistry 5:7–34

    Article  CAS  Google Scholar 

  • Vitousek PM, Farrington H (1997) Nutrient limitation and soil development: experimental test of a biogeochemical theory. Biogeochemistry 37:63–75

    Article  CAS  Google Scholar 

  • Walker LR, Wardle DA, Bardgett RD, Clarkson BD (2010) The use of chronosequences in studies of ecological succession and soil development. J Ecol 98:725–736

    Article  Google Scholar 

  • Wang J, Thornton B, Yao HY (2014) Incorporation of urea-derived 13C into microbial communities in four different agriculture soils. Biol Fertil Soils 50:603–612

    Article  CAS  Google Scholar 

  • Wang J, Wu Y, Zhou J, Bing H, Sun H (2016) Carbon demand drives microbial mineralization of organic phosphorus during the early stage of soil development. Biol Fert Soils 52:825–839

    Article  CAS  Google Scholar 

  • Wirth C, Messier C, Bergeron Y, Frank D, Fankhänel A (2009) Old-growth forest definitions: a pragmatic view. In: Wirth C, Gleixner G, Heimann M (eds) Old-growth forests. Springer, Berlin, Heidelberg, pp 11–33

    Chapter  Google Scholar 

  • WRB (World Reference Base for Soil Resources) (2014) FAO International Soil Classification System for Naming Soils and Creating Legends for Soil Maps 106

  • Xuluc-Tolosa FJ, Vester HFM, Ramırez-Marcial N, Castellanos-Albores J, Lawrence D (2003) Leaf litter decomposition of tree species in three successional phases of tropical dry secondary forest in Campeche, Mexico. For Ecol Manag 174:401–412

    Article  Google Scholar 

  • Yang YH, Luo YQ, Finzi AC (2011) Carbon and nitrogen dynamics during forest stand development: a global synthesis. New Phytol 190:977–989

    Article  CAS  PubMed  Google Scholar 

  • Yao HY, Chapman SJ, Thornton B, Paterson E (2014) 13C PLFAs: a key to open the soil microbial black box? Plant Soil 392:3–15

    Article  CAS  Google Scholar 

  • Zak DR, Grigal DF, Gleeson S, Tilman D (1990) Carbon and nitrogen cycling during old-field succession: constraints on plant and microbial biomass. Biogeochemistry 11:111–129

    Article  Google Scholar 

  • Zechmeister-Boltenstern S, Keiblinger KM, Mooshammer M, Peñuelas J, Richter A, Sardans J, Wanek W (2015) The application of ecological stoichiometry to plant–microbial–soil organic matter transformations. Ecol Monogr 85:133–155

    Article  Google Scholar 

  • Zelles L (1999) Fatty acid patterns of phospholipids and lipopolysaccharides in the characterization of microbial communities in soil: a review. Biol Fertil Soils 29:111–129

    Article  CAS  Google Scholar 

  • Zhang KR, Cheng XL, Dang HH, Ye C, Zhang YL, Zhang QF (2013) Linking litter production, quality and decomposition to vegetation succession following agricultural abandonment. Soil Biol Biochem 57:803–813

    Article  CAS  Google Scholar 

  • Zhou G, Liu S, Li Z, Zhang D, Tang X (2006) Old-growth forests can accumulate carbon in soils. Science 314:1417

    Article  CAS  PubMed  Google Scholar 

  • Zibilske LM (1994) Carbon mineralization. In Weaver RW, Angle S, Bottomley P, (complete the list of editors) (Eds) Methods of soil analysis, part 2, Microbiological and Biochemical Properties, Soil Science Society of America, Madison, WI, pp. 835–863.

Download references

Funding

This study was supported by the National Natural Science Foundation of China (41830646, 41601318, 31470560, and 41671031), the general financial grant from the China Postdoctoral Science Foundation (2016M600123) and the national key research and development program of China (2016YFC0502503), and Youth Innovation Research Team Project (LENOM2016Q0004). The publication was supported by the Government Program of Competitive Growth of Kazan Federal University and with the support of the “RUDN University program 5-100.”

Author information

Authors and Affiliations

  1. Key Laboratory of Ecosystem Network Observation and Modeling, Chinese Academy of Sciences (CAS), Institute of Geographic Sciences and Natural Resources Research, 11A Datun Road, Chaoyang District, Beijing, 100101, China

    Na Qiao, Xingliang Xu, Shenggong Li, Huimin Wang & Yakov Kuzyakov

  2. Key Laboratory of Tropical Forest Ecology, Chinese Academy of Sciences, Xishuangbanna Tropical Botanical Garden, Menglun, Mengla, 666303, Yunnan, China

    Na Qiao, Youxin Shen, Yuehua Hu & Douglas Schaefer

  3. Institute of Urban Environment, Chinese Academy of Sciences, 1799 Jimei Road, Xiamen, 361021, China

    Juan Wang

  4. School of Geographic Sciences, Nantong University, Nantong, 226007, China

    Xi’en Long

  5. Department of Soil Science of Temperate Ecosystems, Department of Agricultural Soil Science, University of Göttingen, Büsgenweg 2, 37077, Göttingen, Germany

    Yakov Kuzyakov

  6. Institute of Environmental Sciences, Kazan Federal University, Kazan, Russia, 420049

    Yakov Kuzyakov

  7. Agro-Technological Institute, RUDN University, Moscow, Russia, 117198

    Yakov Kuzyakov

Authors
  1. Na Qiao
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Juan Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Xingliang Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Youxin Shen
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Xi’en Long
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yuehua Hu
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Douglas Schaefer
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Shenggong Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Huimin Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Yakov Kuzyakov
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Xingliang Xu.

Additional information

Publisher’s note

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

Electronic Supplementary Material

ESM 1

(DOC 164 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Qiao, N., Wang, J., Xu, X. et al. Priming alters soil carbon dynamics during forest succession. Biol Fertil Soils 55, 339–350 (2019). https://doi.org/10.1007/s00374-019-01351-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00374-019-01351-0

Keywords

Search

Navigation