Advertisement

Plant and Soil

, Volume 373, Issue 1–2, pp 285–299 | Cite as

Mechanisms linking plant community properties to soil aggregate stability in an experimental grassland plant diversity gradient

  • G. Pérès
  • D. Cluzeau
  • S. Menasseri
  • J. F. Soussana
  • H. Bessler
  • C. Engels
  • M. Habekost
  • G. Gleixner
  • A. Weigelt
  • W. W. Weisser
  • S. Scheu
  • N. Eisenhauer
Regular Article

Abstract

Background and aims

Soil aggregate stability depends on plant community properties, such as functional group composition, diversity and biomass production. However, little is known about the relative importance of these drivers and the role of soil organisms in mediating plant community effects.

Methods

We studied soil aggregate stability in an experimental grassland plant diversity gradient and considered several explanatory variables to mechanistically explain effects of plant diversity and plant functional group composition. Three soil aggregate stability measures (slaking, mechanical breakdown and microcracking) were considered in path analyses.

Results

Soil aggregate stability increased significantly from monocultures to plant species mixtures and in the presence of grasses, while it decreased in the presence of legumes, though effects differed somewhat between soil aggregate stability measures. Using path analysis plant community effects could be explained by variations in root biomass, soil microbial biomass, soil organic carbon concentrations (all positive relationships), and earthworm biomass (negative relationship with mechanical breakdown).

Conclusions

The present study identified important drivers of plant community effects on soil aggregate stability. The effects of root biomass, soil microbial biomass, and soil organic carbon concentrations were largely consistent across plant diversity levels suggesting that the mechanisms identified are of general relevance.

Keywords

Grassland Earthworm biomass Root biomass Soil microorganisms Soil organic carbon 

Notes

Acknowledgments

This work was both funded by the French ANR DISCOVER project (ANR-05-BDIV-010-01) piloted by J.F. Soussana (INRA Clermont-Ferrand) and the Deutsche Forschungsgemeinschaft (FOR 456; the Jena Experiment). N. Eisenhauer gratefully acknowledges funding by the Deutsche Forschungsgemeinschaft (DFG; Ei 862/1 and Ei 862/2). We thank all the people who helped to establish and manage the Jena Experiment field site, in particular C. Roscher for project coordination and S. Eismann, S. Hengelhaupt, S. Junghans, H. Scheffler and U. Wehmeier for field maintenance. We also thank Y. Cozic for supervising the field and laboratory work, A. Transon for his assistance in the field during sampling time, S. Busnot for technical support in soil aggregate stability measurements and A. Ebeling and M. Lange for helpful comments on the paper. Further, we thank three anonymous reviewers for very helpful suggestions to improve previous versions of the paper.

References

  1. Abiven S, Menasseri S, Angers DA, Leterme P (2007) Dynamics of aggregate stability and biological binding agents during the decomposition of organic material. Eur J Soil Sci 58:239–247CrossRefGoogle Scholar
  2. Abiven S, Menasseri S, Chenu C (2009) The effects of organic inputs over time on soil aggregate stability—a literature analysis. Soil Biol Biochem 41:1–12CrossRefGoogle Scholar
  3. Anderson JPE, Domsch KH (1978) Mineralization of bacteria and fungi in chloroform-fumigated soils. Soil Biol Biochem 10:207–213CrossRefGoogle Scholar
  4. Angers DA, Edwards LM, Sanderson JB, Bissonnette N (1999) Soil organic matter quality and aggregate stability under eight potato cropping sequences in a fine sandy loam of Prince Edward Island. Can J Soil Sci 79:411–417CrossRefGoogle Scholar
  5. AFNOR Association-française-de-normalisation (2005) Norme Française X 31–515. Mesure de la stabilité des agrégats de sols pour l’évaluation de la sensibilité à la battance et à l’érosion hydrique. AFNOR (Ed.), ParisGoogle Scholar
  6. Balvanera P, Pfisterer AB, Buchmann N, He J-S, Nakashizuka T, Raffaelli D, Schmid B (2006) Quantifying the evidence for biodiversity effects on ecosystem functioning and services. Ecol Lett 9:1146–1156PubMedCrossRefGoogle Scholar
  7. Barley KP (1953) The root growth of irrigated perennial pastures and its effect on soil structure. Aust J Agric Res 4:283–291CrossRefGoogle Scholar
  8. Beck T, Joergensen RG, Kandeler E et al (1997) An inter-laboratory comparison of ten different ways of measuring soil microbial biomass C. Soil Biol Biochem 29:1023–1032CrossRefGoogle Scholar
  9. Bessler H, Temperton VM, Roscher C, Buchmann N, Schmid B, Schulze E-D, Weisser WW, Engels C (2009) Aboveground overyielding in grassland mixtures is associated with reduced biomass partitioning to belowground organs. Ecology 90:1520–1530PubMedCrossRefGoogle Scholar
  10. Bessler H, Oelmann Y, Roscher C, Buchmann N, Scherer-Lorenzen M, Schulze E-D, Temperton VM, Wilcke W, Engels C (2012) Nitrogen uptake by grassland communities: contribution of N2 fixation, facilitation, complementarity, and species dominance. Plant Soil 358:301–322CrossRefGoogle Scholar
  11. Blanchart E, Albrecht A, Chevallier T, Hartmann C (2004) The respective roles of roots and earthworms in restoring physical properties of Vertisol under a Digitaria decumbens pasture (Martinique, WI). Agric Ecosyst Environ 103:343–355CrossRefGoogle Scholar
  12. Capriel P, Beck T, Borchert H, Härter P (1990) Relationships between soil aliphatic fraction extracted with supercritical hexane, soil microbial biomass, and soil aggregate stability. Soil Sci Soc Am J 54:415–420CrossRefGoogle Scholar
  13. Chenu C (1989) Influence of a fungal polysaccharide, scleroglucan, on clay microstructures. Soil Biol Biochem 21:299–305CrossRefGoogle Scholar
  14. Chenu C (1995) Extracellular polysaccharides: an interface between microorganisms and soil constituents. In: Huang PM (ed) Environmental impact of soil component interactions. Natural and anthropogenics organics. Lewis Publishers, CRC Press, Boca Raton, pp 217–233Google Scholar
  15. Chenu C, Cosentino D (2011) Microbial regulation of soil structural dynamics. In: Ritz K, Young IM (eds) The architecture and biology of soils: life in inner space. Chapter 3. CABI. Oxford University Press pp 37–70Google Scholar
  16. Chenu C, Guerif J (1991) Division s-6 soil and water management and conservation—mechanical strength of clay-minerals as influenced by an adsorbed polysaccharide. Soil Sci Soc Am J 55:1076–1080CrossRefGoogle Scholar
  17. Chenu C, Abiven S, Annabi M, Barray S, Bertrand M, Bureau F, Cosentino D, Darboux F, Duval O, Fourrié L, Francou C, Houot S, Jolivet C, Laval K, Le Bissonnais Y, Lemée L, Menasseri S, Pétraud JP, Verbèque B (2011) Mise au point d’outils de prévision de l’évolution de la stabilité de la structure de sols sous l’effet de la gestion organique des sols. Etude Gest Sols 18:161–174Google Scholar
  18. Chung H, Zak DR, Reich PB, Ellsworth DS (2007) Plant species richness, elevated CO2, and atmospheric nitrogen deposition alter soil microbial community composition and function. Glob Chang Biol 13:980–989CrossRefGoogle Scholar
  19. Coq S, Barthes BG, Oliver R, Rabary B, Blanchart E (2007) Earthworm activity affects soil aggregation and organic matter dynamics according to the quality and localization of crop residues-an experimental study (Madagascar). Soil Biol Biochem 39:2119–2128CrossRefGoogle Scholar
  20. Cosentino D, Chenu C, Le Bissonnais Y (2006) Aggregate stability and microbial community dynamics under drying–wetting cycles in a silt loam soil. Soil Biol Biochem 38:2053–2062CrossRefGoogle Scholar
  21. De León-González F, Gutiérrez-Castorena MC, González-Chávez MCA, Castillo-Juárez H (2007) Root-aggregation in a pumiceous sandy soil. Geoderma 142:308–317CrossRefGoogle Scholar
  22. Degens BP (1997) Macro-aggregation of soils by biological bonding and binding mechanisms and the factors affecting these: a review. Aust J Soil Res 35:431–459CrossRefGoogle Scholar
  23. Degens B, Sparling G, Abbott L (1994) The contribution from hyphae, roots and organic carbon constituents to the aggregation of a sandy loam under long-term clover-based and grass pastures. Eur J Soil Sci 45:459–468CrossRefGoogle Scholar
  24. Degens BP, Sparling GP, Abbott LK (1996) Increasing the length of hyphae in a sandy soil increases the amount of waterstable aggregates. Appl Soil Ecol 3:149–159CrossRefGoogle Scholar
  25. Denef K, Six J (2005) Clay mineralogy determines the importance of biological versus abiotic processes macroaggregate formation and stabilization. Eur J Soil Sci 56:469–479CrossRefGoogle Scholar
  26. 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 Natl Acad Sci U S A 24:10938–10942CrossRefGoogle Scholar
  27. Edwards CA, Bohlen PJ (1996) Biology and ecology of earthworms. Chapman & Hall, LondonGoogle Scholar
  28. Eisenhauer N, Milcu A, Nitschke N, Sabais ACW, Scherber C, Scheu S (2009) Earthworm and belowground competition effects on plant productivity. Oecologia 161:291–301PubMedCrossRefGoogle Scholar
  29. Eisenhauer N, Beßler H, Engels C, Gleixner G, Habekost M, Milcu A, Partsch S, Sabais ACW, Scherber C, Steinbeiss S, Weigelt A, Weisser WW, Scheu S (2010) Plant diversity effects on soil microorganisms support the singular hypothesis. Ecology 91:485–496PubMedCrossRefGoogle Scholar
  30. Eisenhauer N, Milcu A, Sabais ACW, Bessler H, Brenner J, Engels C, Klarner B, Maraun M, Partsch S, Roscher C, Schonert F, Temperton VM, Thomisch K, Weigelt A, Weisser WW, Scheu S (2011a) Plant diversity surpasses plant functional groups and plant productivity as driver of soil biota in the long term. PLoS One 6:e16055PubMedCrossRefGoogle Scholar
  31. Eisenhauer N, Migunova VD, Ackermann M, Ruess L, Scheu S (2011b) Changes in plant species richness induce functional shifts in soil nematode communities in experimental grassland. PLoS One 6:e24087PubMedCrossRefGoogle Scholar
  32. FAO-Unesco (1997) Soil map of the world. Revised legend with corrections and update. ISRIC, WageningenGoogle Scholar
  33. Fonte SJ, Kong AYY, van Kessel C, Hendrix PF, Six J (2007) Influence of earthworm activity on aggregate-associated carbon and nitrogen dynamics differs with agroecosystem management. Soil Biol Biochem 39:1014–1022CrossRefGoogle Scholar
  34. Fornara DA, Tilman D (2009) Ecological mechanisms associated with the positive diversity-productivity relationship in an N-limited grassland. Ecology 90:408–418PubMedCrossRefGoogle Scholar
  35. Francis GS, Haynes RJ, Koppi AJ (1994) Plant mediated improvement of soil structure after long-term arable cropping. Proc New Zealand Soc Soil Sci Conf, LincolnGoogle Scholar
  36. Grace JB (2006) Structural equation modeling and natural systems. Cambridge Univ. PressGoogle Scholar
  37. Gray DH, Sotir RB (1996) Biotechnical and soil bioengineering slope stabilization: a practical guide for erosion control. John Wiley and SonsGoogle Scholar
  38. Guggenberger G, Elliott ET, Frey SD, Six J, Paustian K (1999) Microbial contributions to the aggregation of a cultivated grassland soil amended with starch. Soil Biol Biochem 31:407–419CrossRefGoogle Scholar
  39. Gyssels G, Poesen J (2003) The importance of plant root characteristics in controlling concentrated flow erosion rates. Earth Surf Process Landforms 28:371–384CrossRefGoogle Scholar
  40. Gyssels G, Poesen J, Bochet E, Li Y (2005) Impact of plant roots on the resistance of soils to erosion by water: a review. Progr Phys Geogr 29:189–217CrossRefGoogle Scholar
  41. Hallett PD, Young IM (1999) Changes to water repellence of soil aggregates caused by substrate-induced microbial activity. Eur J Soil Sci 50:35–40CrossRefGoogle Scholar
  42. Haynes RJ, Swift RS (1990) Stability of soil aggregates in relation to organic constituents and soil water content. J Soil Sci 41:73–83CrossRefGoogle Scholar
  43. Hooper DU, Chapin FS, Ewel JJ, Hector A, Inchausti P, Lavorel S, Lawton JH, Lodge DM, Loreau M, Naeem S, Schmid B, Setälä H, Symstadt AJ, Vandermeer J, Wardle DA (2005) Effects of biodiversity on ecosystem functioning: a consensus of current knowledge. Ecol Monogr 75:3–35CrossRefGoogle Scholar
  44. ISO 10930 (2012) Qualité du sol - Mesure de la stabilité d'agrégats de sols soumis à l'action de l'eauGoogle Scholar
  45. Jastrow JD (1987) Changes in soil aggregation associated with tallgrass prairie restoration. Am J Bot 74:1656–1664Google Scholar
  46. Jastrow JD, Miller RM, Lussenhop J (1998) Contributions of interacting biological mechanisms to soil aggregate stabilization in restored prairie. Soil Biol Biochem 30:905–916CrossRefGoogle Scholar
  47. Ketterings QM, Blair JM, Marinissen JCY (1997) Effects of earthworms on soil aggregate stability and carbon and nitrogen storage in a legume cover crop agroecosystem. Soil Biol Biochem 29:401–408CrossRefGoogle Scholar
  48. Kluge G, Müller-Westermeier G (2000) Das Klima ausgewählter Orte der Bundesrepublik Deutschland: Jena. Berichte des Deutschen Wetterdienstes 213. Offenbach/MainGoogle Scholar
  49. Kögel-Knabner I, Guggenberger G, Kleber M, Kandeler E, Kalbitz K, Scheu S, Eusterhues K, Leinweber P (2008) Organo-mineral associations in temperate soils: integrating biology, mineralogy, and organic matter chemistry. J Plant Nutr Soil Sci 171:61–82CrossRefGoogle Scholar
  50. Körner C, Spehn EM (2002) Mountain biodiversity: a global assessment. Parthenon Publishing Group, LondonGoogle Scholar
  51. Le Bisonnais Y, Le Souder C (1995) Mesurer la stabilité structurale des sols pour évaluer leur sensibilité à la battance et à l’érosion. Etude Gest Sols 2:43–56Google Scholar
  52. Le Bissonnais Y (1996) Aggregate stability and assessment of soil crustability and erodibility: I. Theory and methodology. Eur J Soil Sci 47:425–437CrossRefGoogle Scholar
  53. Le Bissonnais Y, Arrouays D (1997) Aggregate stability and assessment of soil crustability and erodibility:II. Application to humic loamy soils with various organic carbon contents. Eur J Soil Sci 48:39–48CrossRefGoogle Scholar
  54. Le Bissonnais Y, Blavet D, De Noni G, Laurent JY, Asseline J, Chenu C (2007) Erodibility of Mediterranean vineyard soils: relevant aggregate stability methods and significant soil variables. Eur J Soil Sci 58:188–195CrossRefGoogle Scholar
  55. Milcu A, Partsch S, Scherber C et al (2008) Earthworms and legumes control litter decomposition in a plant diversity gradient. Ecology 89:1872–1882PubMedCrossRefGoogle Scholar
  56. Miller RM, Jastrow JD (1990) Hierarchy of root and mycorrhizal fungal interactions with soil aggregation. Soil Biol Biochem 22:579–594CrossRefGoogle Scholar
  57. Milleret R, Le Bayon RC, Gobat JM (2009) Root, mycorrhiza and earthworm interactions: their effects on soil structuring processes, plant and soil nutrient concentration and plant biomass. Plant Soil 316:1–12CrossRefGoogle Scholar
  58. Oades JM, Waters AG (1991) Aggregate hierarchy in soils. Aust J Soil Res 29:815–828CrossRefGoogle Scholar
  59. Pohl M, Alig D, Körner C, Rixen C (2009) Higher plant diversity enhances soil stability in disturbed alpine ecosystems. Plant Soil 324:91–102CrossRefGoogle Scholar
  60. Pohl M, Graf F, Buttler A, Rixen C (2012) The relationship between plant species richness and soil aggregate stability con depend on disturbance. Plant Soil 355:87–102CrossRefGoogle Scholar
  61. Quijas S, Schmid B, Balvanera P (2010) Plant diversity enhances provision of ecosystem services: a new synthesis. Basic Appl Ecol 11:582–593CrossRefGoogle Scholar
  62. Reich PB, Tilman D, Isbell F, Mueller KE, Hobbie SE, Flynn DFB, Eisenhauer N (2012) Impacts of biodiversity loss escalate through time as redundancy fades. Science 336:589–592PubMedCrossRefGoogle Scholar
  63. Rillig M, Mummey DL (2006) Mycorrhizas and soil structure. New Phytol 171:41–53PubMedCrossRefGoogle Scholar
  64. Rillig MC, Wright SF, Eviner VT (2002) The role of arbuscular mycorrhizal fungi and glomalin in soil aggregation: comparing effects of five plant species. Plant Soil 238:325–333CrossRefGoogle Scholar
  65. Roscher C, Schumacher J, Baade J, Wilcke W, Gleixner G, Weisser WW, Schmid B, Schulze E-D (2004) The role of biodiversity for element cycling and trophic interactions: an experimental approach in a grassland community. Basic Appl Ecol 5:107–121CrossRefGoogle Scholar
  66. Scherber C, Eisenhauer N, Weisser WW, Schmid B, Voigt W, Schulze E-D, Roscher C, Weigelt A, Allan E, Beßler H, Bonkowski M, Buchmann N, Buscot F, Clement LW, Ebeling A, Engels C, Fischer M, Halle S, Kertscher I, Klein A-M, Koller R, König S, Kowalski E, Kummer V, Kuu A, Lange M, Lauterbach D, Middelhoff C, Migunova VD, Milcu A, Müller R, Partsch S, Petermann JS, Renker C, Rottstock T, Sabais ACW, Scheu S, Schumacher J, Temperton VM, Tscharnke T (2010) Bottom-up effects of plant diversity on multitrophic interactions in a biodiversity experiment. Nature 468:553–556PubMedCrossRefGoogle Scholar
  67. Scheu S (1992) Automated measurement of the respiratory response of soil microcompartments—active microbial biomass in earthworm feces. Soil Biol Biochem 24:1113–1118CrossRefGoogle Scholar
  68. Scheu S (2003) Effects of earthworms on plant growth: patterns and perspectives. Pedobiologia 47:846–856Google Scholar
  69. Schmid B, Hector A, Huston MA, Inchausti P, Nijs I, Leadley PW, Tilman D (2002) The design and analysis of biodiversity experiments. In: Loreau M, Naeem S, Inchausti P (eds) Biodiversity and ecosystem functioning—synthesis and perspectives. Oxford University Press, pp 61–75Google Scholar
  70. Shipitalo MJ, Protz R (1989) Chemistry and micromorphology of aggregation in earthworm casts. Geoderma 45:357–374CrossRefGoogle Scholar
  71. Spehn EM, Joshi J, Schmid B, Alphei J, Körner C (2000) Plant diversity effects on soil heterotrophic activity in experimental grassland ecosystems. Plant Soil 224:217–230CrossRefGoogle Scholar
  72. Steinbeiss S, Beßler H, Engels C, Temperton VM, Buchmann N, Roscher C, Kreutziger Y, Baade J, Habekost M, Gleixner G (2008) Plant diversity positively affects short-term soil carbon storage in experimental grasslands. Glob Chang Biol 14:2937–2949CrossRefGoogle Scholar
  73. Thielemann U (1986) The octet-method for sampling earthworm populations. Pedobiologia 29:296–302Google Scholar
  74. Tisdall JM, Oades JM (1979) Stabilisation of soil aggregates by the root systems of ryegrass. Aust J Soil Res 17:429–441Google Scholar
  75. Tisdall JM, Oades JM (1982) Organic-matter and water-stable aggregates in soils. J Soil Sci 33:141–163CrossRefGoogle Scholar
  76. Traoré O, Groleau-Renaud V, Plantureux S, Tubeileh A, Bœuf-Tremblay V (2000) Effect of root mucilage and modelled root exudates on soil structure. Eur J Soil Sci 51:575–581Google Scholar
  77. Wardle DA (1992) A comparative assessment of factors which influence microbial biomass carbon and nitrogen levels in soil. Biol Rev 67:321–358CrossRefGoogle Scholar
  78. Watanabe T, Misawa S, Hiradate S, Osaki M (2008) Root mucilage enhances aluminium accumulation in Melastoma malabathricum, an aluminium accumulator. Plant Signal Behav 3:603–605PubMedCrossRefGoogle Scholar
  79. Watteau F, Villemin G, Burtin G, Jocteur-Monrozier L (2006) Root impact on the stability and constitution of the fine organo-mineral associations in a maize cultivated soil. Eur J Soil Sci 57:247–257CrossRefGoogle Scholar
  80. Wolters V (2000) Invertebrate control of soil organic matter stability. Biol Fertil Soils 31:1–19CrossRefGoogle Scholar
  81. Young IM, Blanchart E, Chenu C, Dangerfield M, Fragoso C, Grimaldi M, Ingram J, Monrozier LJ (1998) The interaction of soil biota and soil structure under global change. Glob Chang Biol 4:703–712CrossRefGoogle Scholar
  82. Zak DR, Holmes WE, White DC, Peacock AD, Tilman D (2003) Plant diversity, soil microbial communities, and ecosystem function: are there any links? Ecology 84:2042–2050CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  • G. Pérès
    • 1
    • 2
  • D. Cluzeau
    • 1
    • 2
  • S. Menasseri
    • 2
    • 3
    • 4
  • J. F. Soussana
    • 5
  • H. Bessler
    • 6
  • C. Engels
    • 6
  • M. Habekost
    • 7
  • G. Gleixner
    • 7
  • A. Weigelt
    • 8
  • W. W. Weisser
    • 9
  • S. Scheu
    • 10
  • N. Eisenhauer
    • 11
  1. 1.UMR CNRS 6553 EcoBioUniversité Rennes 1PaimpontFrance
  2. 2.Université Européenne de Bretagne (UEB)RennesFrance
  3. 3.INRAUMR 1069 Sol Agro et hydrosystème SpatialisationRennesFrance
  4. 4.Agrocampus OuestUMR 1069 Sol Agro et hydrosystème SpatialisationRennesFrance
  5. 5.INRA, UREP, UR 0874Clermont-FerrandFrance
  6. 6.Department of Plant Nutrition and FertilizationHumboldt University of BerlinBerlinGermany
  7. 7.Max Planck Institute for BiogeochemistryJenaGermany
  8. 8.Institute of BiologyUniversity of LeipzigLeipzigGermany
  9. 9.Terrestrial Ecology Research Group, Department for Ecology and Ecosystem ManagementTechnische Universität MünchenFreisingGermany
  10. 10.J.F. Blumenbach Institute of Zoology and AnthropologyGeorg August University GöttingenGöttingenGermany
  11. 11.Institute of EcologyFriedrich Schiller University of JenaJenaGermany

Personalised recommendations