Skip to main content
SpringerLink
Log in

Mycorrhizal Hyphal Turnover as a Dominant Process for Carbon Input into Soil Organic Matter

  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

The atmospheric concentration of CO2 is predicted to reach double current levels by 2075. Detritus from aboveground and belowground plant parts constitutes the primary source of C for soil organic matter (SOM), and accumulation of SOM in forests may provide a significant mechanism to mitigate increasing atmospheric CO2 concentrations. In a poplar (three species) plantation exposed to ambient (380 ppm) and elevated (580 ppm) atmospheric CO2 concentrations using a Free Air Carbon Dioxide Enrichment (FACE) system, the relative importance of leaf litter decomposition, fine root and fungal turnover for C incorporation into SOM was investigated. A technique using cores of soil in which a C4 crop has been grown (δ13C −18.1‰) inserted into the plantation and detritus from C3 trees (δ13C −27 to −30‰) was used to distinguish between old (native soil) and new (tree derived) soil C. In-growth cores using a fine mesh (39 μm) to prevent in-growth of roots, but allow in-growth of fungal hyphae were used to assess contribution of fine roots and the mycorrhizal external mycelium to soil C during a period of three growing seasons (1999–2001). Across all species and treatments, the mycorrhizal external mycelium was the dominant pathway (62%) through which carbon entered the SOM pool, exceeding the input via leaf litter and fine root turnover. The input via the mycorrhizal external mycelium was not influenced by elevated CO2, but elevated atmospheric CO2 enhanced soil C inputs via fine root turnover. The turnover of the mycorrhizal external mycelium may be a fundamental mechanism for the transfer of root-derived C to SOM.

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

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Explore related subjects

Discover the latest articles, news and stories from top researchers in related subjects.

References

  • J D Aber J M Melillo C A McClaugherty (1990) ArticleTitlePredicting long-term patterns of mass loss, nitrogen dynamics, and soil organic matter formation from initial fine litter chemistry in temperate forest ecosystems Can. J. Bot. 68 2201–2208

    Google Scholar 

  • Agerer R 1987–1996 Colour Atlas of Ectomycorrhizae. Einhorn-Verlag Eduard Dietenberger, Schwäbisch Gmünd

  • R Agerer (2001) ArticleTitleExploration types of ectomycorrhizae: a proposal to classify ectomycorrhizal mycelial systems according to their patterns of differentiation and putative ecological importance Mycorrhiza 11 107–114 Occurrence Handle10.1007/s005720100108

    Article  Google Scholar 

  • J Balesdent G H Wagner A Mariotti (1988) ArticleTitleSoil organic matter turnover in long-term field experiments as revealed by carbon-13 natural abundance Soil Sci. Soc. Am. J. 52 118–124 Occurrence Handle1:CAS:528:DyaL1cXhsV2ns7o%3D Occurrence Handle10.2136/sssaj1988.03615995005200010021x

    Article  CAS  Google Scholar 

  • J Balesdent A Mariotti (1996) Measuring of soil organic matter turnover using 13C abundance TW Boutton S Yamasaki (Eds) Mass Spectroscopy of Soils Marcel Dekker New York 83–111

    Google Scholar 

  • D Binkley J Kaye M Barry M G Ryan (2004) ArticleTitleFirst rotation changes in soil carbon and nitrogen in a eucalyptus plantation in Hawaii Soil Sci Soc Am J. 68 1713–1719 Occurrence Handle1:CAS:528:DC%2BD2cXns1Smt7g%3D Occurrence Handle10.2136/sssaj2004.1713

    Article  CAS  Google Scholar 

  • C Calfapietra B Gielen M Sabatti P Angelis Particlede G Scarascia-Mugnozza R Ceulemans (2001) ArticleTitleGrowth performance of Populus exposed to “Free Air Carbon dioxide Enrichment” during the first growing season in the POPFACE experiment Ann. For. Sc. 58 819–828 Occurrence Handle10.1051/forest:2001165

    Article  Google Scholar 

  • R Ceulemans I A Janssens M E Jach (1999) ArticleTitleEffects of CO2 enrichment on trees and forests: lessons to be learned in view of future ecosystem studies Ann. Bot. 84 577–590 Occurrence Handle10.1006/anbo.1999.0945 Occurrence Handle1:CAS:528:DyaK1MXmvVygsrY%3D

    Article  CAS  Google Scholar 

  • M F Cotrufo P Angelis Particlede A Polle (2005) ArticleTitleLeaf litter production and decomposition in a poplar short rotation coppice exposed to free air CO2 enrichment (POPFACE) Global Change Biol. 11 971–982 Occurrence Handle10.1111/j.1365-2486.2005.00958.x

    Article  Google Scholar 

  • M P Coutts B C Nicoll (1990) ArticleTitleGrowth and survival of shoots, roots and mycorrhizal mycelium in clonal Sitka spruce during the first growing season after planting Can. J. For. Res. 20 861–868

    Google Scholar 

  • R C Dahlman C L Kucera (1965) ArticleTitleRoot productivity and turnover in native prairie Ecology 46 84–89 Occurrence Handle10.2307/1935260

    Article  Google Scholar 

  • I Galdo ParticleDel J Six A Peressotti M F Cotrufo (2003) ArticleTitleAssessing the impact of land-use change on soil C sequestration in agricultural soils by means of organic matter fractionation and stable C isotopes Global Change Biol. 9 1204–1213 Occurrence Handle10.1046/j.1365-2486.2003.00657.x

    Article  Google Scholar 

  • J J Doyle J L Doyle (1987) ArticleTitleA rapid DNA isolation from small amount of fresh leaf tissue Phytochem. Bull. 19 11–15

    Google Scholar 

  • A Ekblad H Wallander T Näsholm (1998) ArticleTitleChitin and ergosterol combined to measure total and living fungal biomass in ectomycorrhizae New Phytol. 138 143–149 Occurrence Handle10.1046/j.1469-8137.1998.00891.x Occurrence Handle1:CAS:528:DyaK1cXhtlOhuro%3D

    Article  CAS  Google Scholar 

  • A H Fitter A Heinemeyer R Husband E Olsen K P Ridgway P L Staddon (2004) ArticleTitleGlobal environmental change and the biology of arbuscular mycorrhizas: gaps and challenges Can. J. Bot. 82 1133–1139 Occurrence Handle10.1139/b04-045

    Article  Google Scholar 

  • R Fogel (1980) ArticleTitleMycorrhizae and nutrient cycling in natural forest ecosystems New Phytol. 86 199–212 Occurrence Handle10.1111/j.1469-8137.1980.tb03189.x Occurrence Handle1:CAS:528:DyaL3MXltlWnsbo%3D

    Article  CAS  Google Scholar 

  • R Fogel G Hunt (1979) ArticleTitleFungal and arboreal biomass in a western Oregon Douglas-fir ecosystem: distribution patterns and turnover Can. J. For. Res. 9 245–256

    Google Scholar 

  • R Fogel G Hunt (1983) ArticleTitleContribution of mycorrhizae and soil fungi to nutrient cycling in a Douglas-fir ecosystem Can. J. For. Res. 13 219–232 Occurrence Handle1:CAS:528:DyaL3sXktVCmurg%3D

    CAS  Google Scholar 

  • S D Frey J Six E T Elliott (2003) ArticleTitleReciprocal transfer of carbon and nitrogen by decomposer fungi at the soil-litter interface Soil Biol. Biochem. 35 1001–1004 Occurrence Handle10.1016/S0038-0717(03)00155-X Occurrence Handle1:CAS:528:DC%2BD3sXkvVWjtbg%3D

    Article  CAS  Google Scholar 

  • C F Friese M F Allen (1991) ArticleTitleThe spread of VA mycorrhizal fungal hyphae in the soil: inoculum types and external hyphal architecture Mycologia 83 409–418

    Google Scholar 

  • R A Gill R B Jackson (2000) ArticleTitleGlobal patterns of root turnover for terrestrial ecosystems New Phytol. 147 13–31 Occurrence Handle10.1046/j.1469-8137.2000.00681.x

    Article  Google Scholar 

  • D L Godbold G M Berntson F A Bazzaz (1997) ArticleTitleGrowth and mycorrhizal colonisation of 3 North American tree species under elevated atmospheric CO2 New Phytol. 137 433–440 Occurrence Handle10.1046/j.1469-8137.1997.00842.x Occurrence Handle1:CAS:528:DyaK1cXitVCmuw%3D%3D

    Article  CAS  Google Scholar 

  • D L Godbold H W Fritz G Jentschke H Meesenburg P Rademacher (2003) ArticleTitleRoot turnover of Norway spruce (Picea abies) is affected by soil acidity and contributes strongly to forest floor litter Tree Physiol. 23 915–921 Occurrence Handle14532015

    PubMed  Google Scholar 

  • G R Hendrey D S Ellsworth K F Lewin J Nagy (1999) ArticleTitleA free-air enrichment system for exposing tall forest vegetation to elevated atmospheric CO2 Global Change Biol. 5 293–309 Occurrence Handle10.1046/j.1365-2486.1999.00228.x

    Article  Google Scholar 

  • M N Högberg P Högberg (2002) ArticleTitleExtramatrical ectomycorrhizal mycelium contributes one-third of microbial biomass and produces, together with associated roots, half the dissolved organic carbon in a forest soil New Phytol. 154 791–795 Occurrence Handle10.1046/j.1469-8137.2002.00417.x

    Article  Google Scholar 

  • P Högberg A Nordgren N Buchmann A F S Taylor A Ekblad M N Högberg G Nyberg M Ottosson-Löfvenius D J Read (2001) ArticleTitleLarge-scale forest girdling shows that current photosynthesis drives soil respiration Nature 411 789–792 Occurrence Handle10.1038/35081058 Occurrence Handle11459055

    Article  PubMed  Google Scholar 

  • M R Hoosbeek M Lukac D Dam Particlevan D L Godbold E J Velthorst F A Biondi A Peressotti M F Cotrufo P Angelis Particlede G Scarascia-Mugnozza (2004) ArticleTitleMore new carbon in the mineral soil of a poplar plantation under Free Air Carbon Enrichment (POPFACE) Global Biogeochem. Cycl. 18 IssueID1 GB1040 Occurrence Handle10.1029/2003GB002127 Occurrence Handle1:CAS:528:DC%2BD2cXjvF2is74%3D

    Article  CAS  Google Scholar 

  • B A Hungate R B Jackson C B Field F S Chapin SuffixIII (1996) ArticleTitleDetecting changes in soil carbon in CO2 enrichment experiments Plant Soil 187 135–145 Occurrence Handle10.1007/BF00017086 Occurrence Handle1:CAS:528:DyaK2sXjt12rtLc%3D

    Article  CAS  Google Scholar 

  • Kubiske M E and Godbold D L 2001 Influence of CO2 on the growth and function of roots and root systems. In The Impact of Carbon Dioxide and Other Greenhouse Gases on Forest Ecosystems. Eds. D F Karnosky, R Ceulemans, G E Scarascia-Mugnozza and J L Innes. pp. 147–191. Report No. 3 of the IUFRO task force on environmental change. CABI Publishing, Wallingford, UK

  • J Leake D Johnson D Donnelly G Muckle L Boddy D Read (2004) ArticleTitleNetworks of power and influence: the role of mycorrhizal mycelium in controlling plant communities and agroecosystem functioning Can J. Bot. 82 1016–1045 Occurrence Handle10.1139/b04-060

    Article  Google Scholar 

  • W M Loya K S Pregitzer N J Karberg J S King C P Giardina (2003) ArticleTitleReduction of soil carbon formation by tropospheric ozone under increased carbon dioxide levels Nature 425 705–707 Occurrence Handle10.1038/nature02047 Occurrence Handle1:CAS:528:DC%2BD3sXotV2hsr4%3D Occurrence Handle14562100

    Article  CAS  PubMed  Google Scholar 

  • M Lukac D L Godbold (2001) ArticleTitleA modification of the ingrowth-core method to determine root production in fast growing tree species J. Plant Nutr. Soil Sci. 164 613–614 Occurrence Handle10.1002/1522-2624(200112)164:6<613::AID-JPLN613>3.0.CO;2-E Occurrence Handle1:CAS:528:DC%2BD38XjtlGrug%3D%3D

    Article  CAS  Google Scholar 

  • M Lukac C Calfapietra D L Godbold (2003) ArticleTitleProduction, turnover and mycorrhizal colonization of root systems of three Populus species grown under elevated CO2 (POPFACE) Global Change Biol. 9 838–848 Occurrence Handle10.1046/j.1365-2486.2003.00582.x

    Article  Google Scholar 

  • T P McGonigle M H Miller D G Evans G L Fairchild J A Swan (1990) ArticleTitleA new method which gives an objective measure of colonization of roots by vesicular-arbuscular mycorrhizal fungi New Phytol. 115 495–501 Occurrence Handle10.1111/j.1469-8137.1990.tb00476.x

    Article  Google Scholar 

  • F Miglietta A Peressotti F P Vaccari A Zaldei P Angelis Particlede G Scarascia-Mugnozza (2001) ArticleTitleFree-air CO2 enrichment (FACE) of a poplar plantation: the POPFACE fumigation system New Phytol. 150 465–476 Occurrence Handle10.1046/j.1469-8137.2001.00115.x

    Article  Google Scholar 

  • R A A Muzzarelli (1977) Chitin Pergamon Press Oxford, UK

    Google Scholar 

  • L O Nilsson H Wallander (2003) ArticleTitleProduction of external mycelium by ectomycorrhizal fungi in a norway spruce forest was reduced in response to nitrogen fertilisation New Phytol. 158 409–416 Occurrence Handle10.1046/j.1469-8137.2003.00728.x

    Article  Google Scholar 

  • R J Norby P J Hanson E G O’Neill T J Tschaplinski J F Weltzin R A Hansen W Cheng S D Wullschleger C A Gunderson A C Edwards D W Johnson (2002) ArticleTitleNet primary productivity of a CO2-enriched deciduous forest and the implications for carbon storage Ecol. Appl. 12 1261–1266

    Google Scholar 

  • D L Phillips J W Gregg (2001) ArticleTitleUncertainty in source partitioning using stable isotopes Oecologia 127 171–179 Occurrence Handle10.1007/s004420000578

    Article  Google Scholar 

  • M C Rillig S F Wright K A Nichols W F Schmidt M S Torn (2001) ArticleTitleLarge contribution of arbuscular mycorrhizal fungi to soil carbon pools in tropical forest soils Plant Soil 233 167–177 Occurrence Handle10.1023/A:1010364221169 Occurrence Handle1:CAS:528:DC%2BD3MXlvFShtb0%3D

    Article  CAS  Google Scholar 

  • Schlesinger W 1997 Biogeochemistry: an Analysis of Global Change. Academic Press, 2nd edition.

  • W H Schlesinger J Lichter (2001) ArticleTitleLimited carbon storage in soil and litter of experimental forest plots under increased atmospheric CO2 Nature 411 466–469 Occurrence Handle10.1038/35078060 Occurrence Handle1:CAS:528:DC%2BD3MXkt1aqu74%3D Occurrence Handle11373676

    Article  CAS  PubMed  Google Scholar 

  • P L Staddon C B Ramsey N Ostle P Ineson A H Fitter (2003) ArticleTitleRapid turnover of hyphae of mycorrhizal fungi determined by AMS microanalysis of 14C Science 300 1138–1140 Occurrence Handle10.1126/science.1084269 Occurrence Handle1:CAS:528:DC%2BD3sXjslGqtr8%3D Occurrence Handle12750519

    Article  CAS  PubMed  Google Scholar 

  • S J Steele S T Gower J G Vogel J M Norman (1997) ArticleTitleRoot mass, net primary production and turnover in aspen, jack pine and black spruce forests in Saskatchewan and Manitoba, Canada Tree Physiol. 17 577–587 Occurrence Handle1:CAS:528:DyaK2sXntl2jsrc%3D Occurrence Handle14759831

    CAS  PubMed  Google Scholar 

  • K K Treseder M F Allen (2000) ArticleTitleMycorrhizal fungi have a potential role in soil carbon storage under elevated CO2 and nitrogen deposition New Phytol. 147 189–200 Occurrence Handle10.1046/j.1469-8137.2000.00690.x Occurrence Handle1:CAS:528:DC%2BD3cXms1yltLo%3D

    Article  CAS  Google Scholar 

  • Van Lagen B 1996 Soil analyses. In Manual for Soil and Water Analyses. Eds. P Buurman, B Van Lagen and E Velthorst. Blackhuys Publishers, Leiden

  • K A Vogt C C Grier D J Vogt (1986) ArticleTitleProduction, turnover, and nutrient dynamics of above- and belowground detritus of world forests Adv. Ecol. Res. 15 303–377 Occurrence Handle10.1016/S0065-2504(08)60122-1

    Article  Google Scholar 

  • H Wallander L O Nilsson D Hagerberg E Bååth (2001) ArticleTitleEstimation of the biomass and seasonal growth of external mycelium of ectomycorrhizal fungi in the field New Phytol. 151 753–760 Occurrence Handle10.1046/j.0028-646x.2001.00199.x Occurrence Handle1:CAS:528:DC%2BD3MXntFGnsLw%3D

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. School of Agricultural and Forest Sciences, University of Wales, LL57 2UW, Bangor, Gwynedd, UK

    Douglas L. Godbold & Martin Lukac

  2. Laboratory of Soil Science and Geology, Department of Environmental Sciences, Wageningen University, P.O. Box 37, 6700 AA, Wageningen, The Netherlands

    Marcel R. Hoosbeek & Eef J. Velthorst

  3. Dipartimento di Scienze Ambientali, Seconda Università degli Studi di Napoli, Via Vivaldi 43, I-80110, Caserta, Italy

    M. Francesca Cotrufo

  4. Department of Biology, University of Antwerpen (UA), Universiteitsplein 1, B-2610, Wilrijk, Belgium

    Ivan A. Janssens & Reinhart Ceulemans

  5. Institut für Forstbotanik, Universität Göttingen, Büsgenweg 2, 37077, Göttingen, Germany

    Andrea Polle

  6. Di.S.A.F.Ri., Università degli Studi della Tuscia, Via S. Camillo De Lellis, I-01100, Viterbo, Italy

    Giuseppe Scarascia-Mugnozza & Paolo De Angelis

  7. Insitute of Biometeorology, IBIMET-CNR, P.le delle Cascine 18, I-50144, Firenze, Italy

    Franco Miglietta

  8. Dipartimento Produzione Vegetale eTechnologie Ambientali, Università di Udine 208, Via delle Scienze, 33100, Udine, Italy

    Alessandro Peressotti

Authors
  1. Douglas L. Godbold
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Marcel R. Hoosbeek
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Martin Lukac
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. M. Francesca Cotrufo
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ivan A. Janssens
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Reinhart Ceulemans
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Andrea Polle
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Eef J. Velthorst
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Giuseppe Scarascia-Mugnozza
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Paolo De Angelis
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Franco Miglietta
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Alessandro Peressotti
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Douglas L. Godbold.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Godbold, D.L., Hoosbeek, M.R., Lukac, M. et al. Mycorrhizal Hyphal Turnover as a Dominant Process for Carbon Input into Soil Organic Matter. Plant Soil 281, 15–24 (2006). https://doi.org/10.1007/s11104-005-3701-6

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-005-3701-6

Keywords

Search

Navigation