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Soil disturbance alters plant community composition and decreases mycorrhizal carbon allocation in a sandy grassland

  • Ecosystem Ecology - Original Paper
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Abstract

We have studied how disturbance by ploughing and rotavation affects the carbon (C) flow to arbuscular mycorrhizal (AM) fungi in a dry, semi-natural grassland. AM fungal biomass was estimated using the indicator neutral lipid fatty acid (NLFA) 16:1ω5, and saprotrophic fungal biomass using NLFA 18:2ω6,9. We labeled vegetation plots with 13CO2 and studied the C flow to the signature fatty acids as well as uptake and allocation in plants. We found that AM fungal biomass in roots and soil decreased with disturbance, while saprotrophic fungal biomass in soil was not influenced by disturbance. Rotavation decreased the 13C enrichment in NLFA 16:1ω5 in soil, but 13C enrichment in the AM fungal indicator NLFA 16:1ω5 in roots or soil was not influenced by any other disturbance. In roots, 13C enrichment was consistently higher in NLFA 16:1ω5 than in crude root material. Grasses (mainly Festuca brevipila) decreased as a result of disturbance, while non-mycorrhizal annual forbs increased. This decreases the potential for mycorrhizal C sequestration and may have been the main reason for the reduced mycorrhizal C allocation found in disturbed plots. Disturbance decreased the soil ammonium content but did not change the pH, nitrate or phosphate availability. The overall effect of disturbance on C allocation was that more of the C in AM fungal mycelium was directed to the external phase. Furthermore, the functional identity of the plants seemed to play a minor role in the C cycle as no differences were seen between different groups, although annuals contained less AM fungi than the other groups.

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References

  • Allison VJ, Miller RM, Jastrow JD, Matamala R, Zak DR (2005) Changes in soil microbial community structure in a tallgrass prairie chronosequence. Soil Sci Soc Am J 69:1412–1421

    Article  CAS  Google Scholar 

  • Ames RN, Reid CPP, Ingham ER (1984) Rhizosphere bacterial population responses to root colonization by a vesicular arbuscular mycorrhizal fungus. New Phytol 96:555–563

    Article  Google Scholar 

  • Antunes PM, Koch AM, Dunfield KE, Hart MM, Downing A, Rillig MC, Klironomos JN (2009) Influence of commercial inoculation with Glomus intraradices on the structure and functioning of an AM fungal community from an agricultural site. Plant Soil 317:257–266

    Article  CAS  Google Scholar 

  • Bago B, Pfeffer PE, Shachar-Hill Y (2000) Carbon metabolism and transport in arbuscular mycorrhizas. Plant Physiol 124:949–957

    Article  PubMed  CAS  Google Scholar 

  • Beare MH, Hendrix PF, Coleman DC (1994) Water-stable aggregates and organic matter fractions in conventional- and no-tillage soils. Soil Sci Soc Am J 58:777–786

    Article  Google Scholar 

  • Bellgard SE (1993) Soil disturbance and infection of Trifolium repens roots by vesicular-arbuscular mycorrhizal fungi. Mycorrhiza 3:25–29

    Article  Google Scholar 

  • Bever JD (1999) Dynamics within mutualism and the maintenance of diversity: inference from a model of interguild frequency dependence. Ecol Lett 2:52–62

    Article  Google Scholar 

  • Boschker HTS, Middelburg JJ (2002) Stable isotopes and biomarkers in microbial ecology. FEMS Microbiol Ecol 40:85–95

    Article  PubMed  CAS  Google Scholar 

  • Boschker HTS, Nold SC, Wellsbury P, Bos D, de Graaf W, Pel R, Parkes RJ, Cappenberg TE (1998) Direct linking of microbial populations to specific biogeochemical processes by C-13-labelling of biomarkers. Nature 392:801–805

    Article  CAS  Google Scholar 

  • Butler JL, Williams MA, Bottomley PJ, Myrold DD (2003) Microbial community dynamics associated with rhizosphere carbon flow. Appl Environ Microbiol 69:6793–6800

    Article  PubMed  CAS  Google Scholar 

  • Carey EV, Marler MJ, Callaway RM (2004) Mycorrhizae transfer carbon from a native grass to an invasive weed: evidence from stable isotopes and physiology. Plant Ecol 172:133–141

    Article  Google Scholar 

  • Castillo CG, Rubio R, Rouanet JL, Borie F (2006) Early effects of tillage and crop rotation on arbuscular mycorrhizal fungal propagules in an Ultisol. Biol Fert Soils 43:83–92

    Article  Google Scholar 

  • Denef K, Roobroeck D, Manimel Wadu MCW, Lootens P, Boeckx P (2009) Microbial community composition and rhizodeposit-carbon assimilation in differently managed temperate grassland soils. Soil Biol Biochem 41:144–153

    Article  CAS  Google Scholar 

  • Drigo B, Pijl AS, Duyts H, Kielak A, Gamper HA, Houtekamer MJ, Boschker HTS, Bodelier PLE, Whiteley AS, van Veen JA, Kowalchuk GA (2010) Shifting carbon flow from roots into associated microbial communities in response to elevated atmospheric CO2. Proc Nat Acad Sci USA 107:10938–10942

    Google Scholar 

  • Drijber RA, Doran JW, Parkhurst AM, Lyon DJ (2000) Changes in soil microbial community structure with tillage under long-term wheat-fallow management. Soil Biol Biochem 32:1419–1430

    Article  CAS  Google Scholar 

  • Dupre C, Diekmann M (2001) Differences in species richness and life-history traits between grazed and abandoned grasslands in southern Sweden. Ecography 24:275–286

    Google Scholar 

  • Francis R, Read DJ (1984) Direct transfer of carbon between plants connected by vesicular arbuscular mycorrhizal mycelium. Nature 307:53–56

    Article  CAS  Google Scholar 

  • Freibauer A, Rounsevell MDA, Smith P, Verhagen J (2004) Carbon sequestration in the agricultural soils of Europe. Geoderma 122:1–23

    Article  CAS  Google Scholar 

  • Galvez L, Douds DD, Drinkwater LE, Wagoner P (2001) Effect of tillage and farming system upon VAM fungus populations and mycorrhizas and nutrient uptake of maize. Plant Soil 228:299–308

    Article  CAS  Google Scholar 

  • Grime JP, Mackey JML, Hillier SH, Read DJ (1987) Floristic diversity in a model system using experimental microcosms. Nature 328:420–422

    Article  Google Scholar 

  • Harley JL, Harley EL (1987) A check-list of mycorrhiza in the British flora. New Phytol 105(s1):1–102

    Article  Google Scholar 

  • Hart MM, Reader RJ, Klironomos JN (2003) Plant coexistence mediated by arbuscular mycorrhizal fungi. Trend Ecol Evol 18:418–423

    Article  Google Scholar 

  • He XH, Critchley C, Bledsoe C (2003) Nitrogen transfer within and between plants through common mycorrhizal networks (CMNs). Crit Rev Plant Sci 22:531–567

    Article  Google Scholar 

  • Hedlund K (2002) Soil microbial community structure in relation to vegetation management on former agricultural land. Soil Biol Biochem 34:1299–1307

    Article  CAS  Google Scholar 

  • Helgason T, Daniell TJ, Husband R, Fitter AH, Young JPW (1998) Ploughing up the wood-wide web? Nature 394:431

    Article  PubMed  CAS  Google Scholar 

  • Jakobsen I, Rosendahl L (1990) Carbon flow into soil and external hyphae from roots of mycorrhizal cucumber plants. New Phytol 115:77–83

    Article  Google Scholar 

  • Jansa J, Mozafar A, Anken T, Ruh R, Sanders IR, Frossard E (2002) Diversity and structure of AMF communities as affected by tillage in a temperate soil. Mycorrhiza 12:225–234

    Article  PubMed  CAS  Google Scholar 

  • Jansa J, Mozafar A, Kuhn G, Anken T, Ruh R, Sanders IR, Frossard E (2003) Soil tillage affects the community structure of mycorrhizal fungi in maize roots. Ecol Appl 13:1164–1176

    Article  Google Scholar 

  • Kytoviita MM, Vestberg M, Tuom J (2003) A test of mutual aid in common mycorrhizal networks: established vegetation negates benefit in seedlings. Ecology 84:898–906

    Article  Google Scholar 

  • Ladygina N, Hedlund K (2010) Plant species influence microbial diversity and carbon allocation in the rhizosphere. Soil Biol Biochem 42:162–168

    Article  CAS  Google Scholar 

  • Lal R (2003) Global potential of soil carbon sequestration to mitigate the greenhouse effect. Crit Rev Plant Sci 22:151–184

    Article  Google Scholar 

  • Larsen J, Olsson PA, Jakobsen I (1998) The use of fatty acid signatures to study mycelial interactions between the arbuscular mycorrhizal fungus Glomus intraradices and the saprotrophic fungus Fusarium culmorum in root-free soil. Mycol Res 102:1491–1496

    Article  CAS  Google Scholar 

  • Leake JR, Ostle NJ, Rangel-Castro JI, Johnson D (2006) Carbon fluxes from plants through soil organisms determined by field (CO2)-C-13 pulse-labelling in an upland grassland. Appl Soil Ecol 33:152–175

    Article  Google Scholar 

  • McGonigle TP, Miller MH, Young D (1999) Mycorrhizae, crop growth, and crop phosphorus nutrition in maize-soybean rotations given various tillage treatments. Plant Soil 210:33–42

    Article  CAS  Google Scholar 

  • Meyer JR, Linderman RG (1986) Selective influence on populations of rhizosphere or rhizoplane bacteria and actinomycetes by mycorrhizas formed by Glomus fasciculatum. Soil Biol Biochem 18:191–196

    Article  Google Scholar 

  • Miller MH, McGonigle TP, Addy HD (1995) Functional ecology of vesicular-arbuscular mycorrhizas as influenced by phosphate fertilization and tillage in an agricultural ecosystem. Crit Rev Biotechnol 15:241–255

    Article  Google Scholar 

  • Mozafar A, Anken T, Ruh R, Frossard E (2000) Tillage intensity, mycorrhizal and nonmycorrhizal fungi, and nutrient concentrations in maize, wheat, and canola. Agron J 92:1117–1124

    Article  CAS  Google Scholar 

  • Nakano-Hylander A, Olsson PA (2007) Carbon allocation in mycelia of arbuscular mycorrhizal fungi during colonisation of plant seedlings. Soil Biol Biochem 39:1450–1458

    Article  CAS  Google Scholar 

  • Olsson PA (1999) Signature fatty acids provide tools for determination of the distribution and interactions of mycorrhizal fungi in soil. FEMS Microbiol Ecol 29:303–310

    Article  CAS  Google Scholar 

  • Olsson PA, Johnson NC (2005) Tracking carbon from the atmosphere to the rhizosphere. Ecol Lett 8:1264–1270

    Article  Google Scholar 

  • Olsson PA, Baath E, Jakobsen I (1997) Phosphorus effects on the mycelium and storage structures of an arbuscular mycorrhizal fungus as studied in the soil and roots by analysis of fatty acid signatures. Appl Environ Microbiol 63:3531–3538

    PubMed  CAS  Google Scholar 

  • Olsson PA, Francis R, Read DJ, Soderstrom B (1998) Growth of arbuscular mycorrhizal mycelium in calcareous dune sand and its interaction with other soil microorganisms as estimated by measurement of specific fatty acids. Plant Soil 201:9–16

    Article  CAS  Google Scholar 

  • Pearson JN, Jakobsen I (1993) Symbiotic exchange of carbon and phosphorus between cucumber and 3 arbuscular mycorrhizal fungi. New Phytol 124:481–488

    Article  CAS  Google Scholar 

  • Pinheiro J, Bates D, DebRoy S, Sarkar D, The R Core Team (2009) nlme: linear and nonlinear mixed effects models (R package version 3.1–96). R Foundation for Statistical Computing, Vienna

  • Quincke JA, Wortmann CS, Mamo M, Franti T, Drijber RA (2007) Occasional tillage of no-till systems: carbon dioxide flux and changes in total and labile soil organic carbon. Agron J 99:1158–1168

    Article  CAS  Google Scholar 

  • Rillig MC, Wright SF, Nichols KA, Schmidt WF, Torn MS (2001) Large contribution of arbuscular mycorrhizal fungi to soil carbon pools in tropical forest soils. Plant Soil 233:167–177

    Article  CAS  Google Scholar 

  • Rillig MC, Ramsey PW, Morris S, Paul EA (2003) Glomalin, an arbuscular-mycorrhizal fungal soil protein, responds to land-use change. Plant Soil 253:293–299

    Article  CAS  Google Scholar 

  • Robinson D, Fitter A (1999) The magnitude and control of carbon transfer between plants linked by a common mycorrhizal network. J Exp Bot 50:9–13

    Article  CAS  Google Scholar 

  • Rosendahl S, Stukenbrock EH (2004) Community structure of arbuscular mycorrhizal fungi in undisturbed vegetation revealed by analyses of LSU rDNA sequences. Mol Ecol 13:3179–3186

    Article  PubMed  CAS  Google Scholar 

  • Schnoor TK, Lekberg Y, Rosendahl S, Olsson PA (2011) Mechanical soil disturbance as a determinant of arbuscular mycorrhizal fungal communities in semi-natural grasslands. Mycorrhiza 21:211–220. doi:10.1007/s00572-010-0325-3

    Google Scholar 

  • Smith SE, Smith FA, Jakobsen I (2003) Mycorrhizal fungi can dominate phosphate supply to plants irrespective of growth responses. Plant Physiol 133:16–20

    Article  PubMed  CAS  Google Scholar 

  • Steinberg PD, Rillig MC (2003) Differential decomposition of arbuscular mycorrhizal fungal hyphae and glomalin. Soil Biol Biochem 35:191–195

    Article  CAS  Google Scholar 

  • Stukenbrock EH, Rosendahl S (2005) Distribution of dominant arbuscular mycorrhizal fungi among five plant species in undisturbed vegetation of a coastal grassland. Mycorrhiza 15:497–503

    Article  PubMed  Google Scholar 

  • R Core Team (2010) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

  • Tyler G, Olsson PA (1993) The calcifuge behaviour of Viscaria vulgaris. J Veg Sci 4:29–36

    Article  Google Scholar 

  • van Aarle IM, Olsson PA (2003) Fungal lipid accumulation and development of mycelial structures by two arbuscular mycorrhizal fungi. Appl Environ Microbiol 69:6762–6767

    Article  PubMed  Google Scholar 

  • van der Heijden MGA, Klironomos JN, Ursic M, Moutoglis P, Streitwolf-Engel R, Boller T, Wiemken A, Sanders IR (1998) Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 396:69–72

    Article  Google Scholar 

  • van Groenigen K-J, Bloem J, Baath E, Boeckx P, Rousk J, Bode S, Forristal D, Jones MB (2010) Abundance, production and stabilization of microbial biomass under conventional and reduced tillage. Soil Biol Biochem 42:48–55

    Article  Google Scholar 

  • Voets L, Goubau I, Olsson PA, Merckx R, Declerck S (2008) Absence of carbon transfer between Medicago truncatula plants linked by a mycorrhizal network, demonstrated in an experimental microcosm. FEMS Microbiol Ecol 65:350–360

    Article  PubMed  CAS  Google Scholar 

  • Wang B, Qiu Y-L (2006) Phylogenetic distribution and evolution of mycorrhizas in land plants. Mycorrhiza 16:299–363

    Article  PubMed  CAS  Google Scholar 

  • Wilson GWT, Hartnett DC, Rice CW (2006) Mycorrhizal-mediated phosphorus transfer between tallgrass prairie plants Sorghastrum nutans and Artemisia ludoviciana. Funct Ecol 20:427–435

    Article  Google Scholar 

  • Wortmann CS, Quincke JA, Drijber RA, Mamo M, Franti T (2008) Soil microbial community change and recovery after one-time tillage of continuous no-till. Agron J 100:1681–1686

    Article  Google Scholar 

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Acknowledgments

This research has been made possible by funding from The Swedish Research Council for Environment, Agricultural Sciences and Spatial Planning (FORMAS). We would also like to thank Ylva Lekberg and two anonymous reviewers for important comments on the manuscript.

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Authors and Affiliations

  1. Plant Ecology and Systematics, Department of Biology, Lund University, The Ecology Building, Sölvegatan 47, 223 62, Lund, Sweden

    Tim Krone Schnoor, Linda-Maria Mårtensson & Pål Axel Olsson

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  1. Tim Krone Schnoor
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  2. Linda-Maria Mårtensson
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  3. Pål Axel Olsson
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Correspondence to Tim Krone Schnoor.

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Communicated by Hakan Wallander.

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Schnoor, T.K., Mårtensson, LM. & Olsson, P.A. Soil disturbance alters plant community composition and decreases mycorrhizal carbon allocation in a sandy grassland. Oecologia 167, 809–819 (2011). https://doi.org/10.1007/s00442-011-2020-2

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