Skip to main content
SpringerLink
Log in

Identification of General Patterns of Nutrient and Labile Carbon Control on Soil Carbon Dynamics Across a Successional Gradient

  • Published:
Ecosystems Aims and scope Submit manuscript

Abstract

Carbon (C) inputs and nutrient availability are known to affect soil organic carbon (SOC) stocks. However, general rules regarding the operation of these factors across a range of soil nutrient availabilities and substrate qualities are unidentified. “Priming” (stimulated decomposition by labile C inputs) and ‘preferential substrate utilization’ (retarded decomposition due to shifts in community composition towards microbes that do not mineralize SOC) are two hypotheses to explain effects of labile C additions on SOC dynamics. For effects of nutrient additions (nitrogen and phosphorus) on SOC dynamics, the stoichiometric (faster decomposition of materials of low carbon-to-nutrient ratios) and ‘microbial mining’ (that is, reduced breakdown of recalcitrant C forms for nutrients under fertile conditions) hypotheses have been proposed. Using the natural gradient of soil nutrient availability and substrate quality of a chronosequence, combined with labile C and nutrient amendments, we explored the support for these contrasting hypotheses. Additions of labile C, nitrogen (N), phosphorus (P), and combinations of C and N and C and P were applied to three sites: 2-year fallow grassland, mature grassland and forest, and the effects of site and nutrient additions on litter decomposition and soil C dynamics were assessed. The response to C addition supported the preferential substrate hypothesis for easily degradable litter C and the priming hypothesis for SOC, but only in nitrogen-enriched soils of the forest site. Responses to N addition supported the microbial mining hypothesis irrespective of C substrate (litter or SOC), but only in the forest site. Further, P addition effects on SOC support the stoichiometric hypothesis; P availability appeared key to soil C release (priming) in the forest site if labile C and N is available. These results clearly link previously contrasting hypotheses of the factors controlling SOC with the natural gradient in litter quality and nutrient availability that exists in ecosystems at different successional stages. A holistic theory that incorporates this variability of responses, due to different mechanisms, depending on nutrient availability and substrate quality is essential for devising management strategies to safeguard soil C stocks.

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

Figure 1
Figure 2
Figure 3

Similar content being viewed by others

References

  • Anderson J, Domsch K. 1978. A physiological method for the quantitative measurement of microbial biomass in soils. Soil Biol Biochem 10:215–21.

    Article  CAS  Google Scholar 

  • Anderson J, Domsch K. 1980. Quantities of plant nutrients in the microbial biomass of selected soils. Soil Sci 130:211.

    Article  CAS  Google Scholar 

  • Beck T, Joergensen RG, Kandeler E, Makeschin F, Oberholzer HR, Nuss HW, Scheu S. 1997. An inter-laboratory comparison of ten different ways of measuring soil microbial biomass C. Soil Biol Biochem 29:1023–32.

    Article  CAS  Google Scholar 

  • Boddy E, Hill P, Farrar J, Jones D. 2007. Fast turnover of low molecular weight components of the dissolved organic carbon pool of temperate grassland field soils. Soil Biol Biochem 39:827–35.

    Article  CAS  Google Scholar 

  • Blagodatskaya E, 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 45:115–31.

    Article  Google Scholar 

  • Bradford M, Fierer N, Reynolds J. 2008. Soil carbon stocks in experimental mesocosms are dependent on the rate of labile carbon, nitrogen and phosphorus inputs to soils. Funct Ecol 22:964–74.

    Article  Google Scholar 

  • Carreiro M, Sinsabaugh R, Repert D, Parkhurst D. 2000. Microbial enzyme shifts explain litter decay responses to simulated nitrogen deposition. Ecology 81:2359–65.

    Article  Google Scholar 

  • Cleveland C, Townsend AR. 2006. Nutrient additions to a tropical rain forest drive substantial soil carbon dioxide losses to the atmosphere. Proc Natl Acad Sci USA 103:10316.

    Article  PubMed  CAS  Google Scholar 

  • Cox PM, Betts RA, Jones CD, Spall SA, Totterdell IJ. 2000. Acceleration of global warming due to carbon-cycle feedbacks in a coupled climate model. Nature 408:184–7.

    Article  PubMed  CAS  Google Scholar 

  • Craine J, Morrow C, Fierer N. 2007. Microbial nitrogen limitation increases decomposition. Ecology 88:2105–13.

    Article  PubMed  Google Scholar 

  • Crawley M. 2007. The R book. New York: Wiley.

    Book  Google Scholar 

  • Dalenberg J, Jager G. 1989. Priming effect of some organic additions to 14C-labelled soil. Soil Biol Biochem 21:443–8.

    Article  CAS  Google Scholar 

  • Ellis R, Morgan P, Weightman A, Fry J. 2003. Cultivation-dependent and-independent approaches for determining bacterial diversity in heavy-metal-contaminated soil. Appl Environ Microbiol 69:3223.

    Article  PubMed  CAS  Google Scholar 

  • Fierer N, Bradford MA, Jackson RB. 2007. Toward an ecological classification of soil bacteria. Ecology 88:1354–64.

    Article  PubMed  Google Scholar 

  • Fontaine S, Barot S. 2005. Size and functional diversity of microbe populations control plant persistence and long-term soil carbon accumulation. Ecol Lett 8:1075–87.

    Article  Google Scholar 

  • Fontaine S, Bardoux G, Abbadie L, Mariotti A. 2004. Carbon input to soil may decrease soil carbon content. Ecol Lett 7:314–20.

    Article  Google Scholar 

  • Heath J, Ayres E, Possell M, Bardgett RD, Black HIJ, Grant H, Ineson P, Kerstiens G. 2005. Rising atmospheric CO2 reduces sequestration of root-derived soil carbon. Science 309:1711–13.

    Article  PubMed  CAS  Google Scholar 

  • Högberg P, Read D. 2006. Towards a more plant physiological perspective on soil ecology. Trends Ecol Evol 21:548–54.

    Article  PubMed  Google Scholar 

  • Hoosbeek M, Lukac M, van Dam D, Godbold D, Velthorst E, Biondi F, Peressotti A, Cotrufo M, de Angelis P, Scarascia-Mugnozza G. 2004. More new carbon in the mineral soil of a poplar plantation under Free Air Carbon Enrichment (POP-FACE): cause of increased priming effect? Glob Biogeochem Cycles 18:GB1040.

    Article  Google Scholar 

  • Jenkinson D, Adams D, Wild A. 1991. Model estimates of CO2 emissions from soil in response to global warming. Nature 351:304–6.

    Article  CAS  Google Scholar 

  • Knorr M, Frey S, Curtis P. 2005. Nitrogen additions and litter decomposition: a meta-analysis. Ecology 86:3252–7.

    Article  Google Scholar 

  • Kuzyakov Y. 2010. Priming effects: interactions between living and dead organic matter. Soil Biol Biochem 42:363–1371.

    Article  Google Scholar 

  • Manning P, Putwain PD, Webb NR. 2006. The role of soil phosphorus sorption characteristics in the functioning and stability of lowland heath ecosystems. Biogeochemistry 81:205–17.

    Article  CAS  Google Scholar 

  • Manning P, Saunders M, Bardgett R, Bonkowski M, Bradford M, Ellis R, Kandeler E, Marhan S, Tscherko D. 2008. Direct and indirect effects of nitrogen deposition on litter decomposition. Soil Biol Biochem 40:688–98.

    Article  CAS  Google Scholar 

  • McGill W, Cole C. 1981. Comparative aspects of cycling of organic C, N, S and P through soil organic matter. Geoderma 26:267–86.

    Article  CAS  Google Scholar 

  • Moorhead D, Sinsabaugh R. 2006. A theoretical model of litter decay and microbial interaction. Ecol Monogr 76:151–74.

    Article  Google Scholar 

  • Muyzer G, de Waal E, Uitterlinden A. 1993. Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl Environ Microbiol 59:695.

    PubMed  CAS  Google Scholar 

  • O’Donnell A, Seasman M, Macrae A, Waite I, Davies JT. 2001. Plants and fertilisers as drivers of change in microbial community structure and function in soils. Plant Soil 232:135–45.

    Article  Google Scholar 

  • Phillips D, Fox T, Six J. 2006. Root exudation (net efflux of amino acids) may increase rhizodeposition under elevated CO2. Glob Change Biol 12:561–7.

    Article  Google Scholar 

  • Pinheiro JC, Bates DM. 2009. Mixed-effects models in S and S-PLUS. Berlin: Springer.

    Google Scholar 

  • Pollierer M, Langel R, Korner C, Maraun M, Scheu S. 2007. The underestimated importance of belowground carbon input for forest soil animal food webs. Ecol Lett 10:729–36.

    Article  PubMed  Google Scholar 

  • Rousk J, Bååth E, Brookes PC, Lauber CL, Lozupone C, Caporaso JG, Knight R, Fierer N. 2010. Soil bacterial and fungal communities across a pH gradient in an arable soil. ISME J 4:1340–51.

    Article  PubMed  Google Scholar 

  • Scheu S. 1992. Automated measurement of the respiratory response of soil microcompartments: active microbial biomass in earthworm faeces. Soil Biol Biochem 24:1113–18.

    Article  Google Scholar 

  • Scheu S, Parkinson D. 1995. Successional changes in microbial biomass, respiration and nutrient status during litter decomposition in an aspen and pine forest. Biol Fertil Soils 19:327–32.

    Article  Google Scholar 

  • Sinsabaugh R, Carreiro M, Repert D. 2002. Allocation of extracellular enzymatic activity in relation to litter composition, N deposition, and mass loss. Biogeochemistry 60:1–24.

    Article  CAS  Google Scholar 

  • Solomon S, Qin D, Manning M, Chen Z, Marquis M, Averyt K, Tignor M, Miller H. 2008. Climate change 2007: the physical science basis. Cambridge, New York, Melbourne, Madrid, Cape Town, Singapore, São Paulo, Delhi: Cambridge University Press.

    Google Scholar 

  • Strickland MS, Lauber C, Fierer N, Bradford MA. 2009. Testing the functional significance of microbial community composition. Ecology 90:441–51.

    Article  PubMed  Google Scholar 

  • Treseder KK. 2008. Nitrogen additions and microbial biomass: a meta analysis of ecosystem studies. Ecol Lett 11:1111–20.

    Article  PubMed  Google Scholar 

  • Trumper K, Bertzky M, Dickson B, van der Heijden G, Jenkins M, Manning P. 2009. The natural fix? The role of ecosystems in climate mitigation. UNEP-WCMC. Cambridge: UNEP Rapid Response Assessment. United Nations Environment Programme.

    Google Scholar 

  • Van Groenigen K, Six J, Hungate B, De Graaff M, Van Breemen N, Van Kessel C. 2006. Element interactions limit soil carbon storage. Proc Natl Acad Sci USA 103:6571–4.

    Article  PubMed  Google Scholar 

  • van Hees P, Jones D, Finlay R, Godbold D, Lundström U. 2005. The carbon we do not see—the impact of low molecular weight compounds on carbon dynamics and respiration in forest soils: a review. Soil Biol Biochem 37:1–13.

    Article  Google Scholar 

  • Waldrop M, Zak D, Sinsabaugh R, Gallo M, Lauber C. 2004. Nitrogen deposition modifies soil carbon storage through changes in microbial enzymatic activity. Ecol Appl 14:1172–7.

    Article  Google Scholar 

  • Walker L, del Moral R. 2003. Primary succession and ecosystem rehabilitation. Cambridge: Cambridge University Press.

    Book  Google Scholar 

  • Wardle DA. 2002. Communities and ecosystems: linking the aboveground and belowground components. Princeton: Princeton University Press.

    Google Scholar 

  • Wu J, Brookes P, Jenkinson D. 1993. Formation and destruction of microbial biomass during the decomposition of glucose and ryegrass in soil. Soil Biol Biochem 25:1435–41.

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We thank the NERC Centre for Population Biology for funding and Tom Sloan, Melanie Wessels, Mark Saunders, Kim Prior, Gary Needham and Callum Brandon for helping with the fertilizer applications and sample analyses.

Author information

Authors and Affiliations

  1. Division of Biology, NERC Centre for Population Biology, Imperial College London, Silwood Park, Ascot, SL5 7PY, UK

    Alexandru Milcu & Pete Manning

  2. Department of Earth and Environmental Sciences, University of Potsdam, Karl-Liebknecht-Str. 24-25, 14476, Potsdam, Germany

    Angela Heim

  3. Veterinary Laboratories Agency, VLA Weybridge, New Haw, KT15 3NB, UK

    Richard J. Ellis

  4. J.F. Blumenbach Institute of Zoology and Anthropology, Georg-August-University Göttingen, Berliner Str. 28, 37073, Göttingen, Germany

    Stefan Scheu

  5. School of Agriculture, Food and Rural Development, Newcastle University, Newcastle, Tyne and Wear, NE1 7RU, UK

    Pete Manning

Authors
  1. Alexandru Milcu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Angela Heim
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Richard J. Ellis
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Stefan Scheu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Pete Manning
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Alexandru Milcu.

Additional information

Author contributions

Alexandru Milcu and Pete Manning: conceived and designed the study, Alexandru Milcu and Angela Heim: performed research, Alexandru Milcu and Richard Ellis: analyzed data, Richard Ellis and Stefan Scheu: contributed methods, Alexandru Milcu and Pete Manning: wrote the paper. All authors discussed the results and the structure of the paper, commented and revised the manuscript text.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Milcu, A., Heim, A., Ellis, R.J. et al. Identification of General Patterns of Nutrient and Labile Carbon Control on Soil Carbon Dynamics Across a Successional Gradient. Ecosystems 14, 710–719 (2011). https://doi.org/10.1007/s10021-011-9440-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10021-011-9440-z

Keywords

Search

Navigation