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Spatial variability of the functional stability of microbial respiration process: a microcosm study using tropical forest soil

  • SOILS, SEC 1 • SOIL ORGANIC MATTER DYNAMICS AND NUTRIENT CYCLING • RESEARCH ARTICLE
  • Published:
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Abstract

Purpose

Understanding the ability of ecosystem processes to resist to and to recover from disturbances is critical to sustainable land use. However, the spatial variability of the stability has rarely been addressed. Here, we investigated the functional stability of a soil microbial process for 24 soils collected from adjacent locations from a 0.3 ha tropical rainforest plot in Paracou, French Guiana.

Materials and methods

The 24 locations were characterized regarding soil chemical and biological (microbial diversity) parameters and forest structure. The corresponding soils were submitted to an experimental transient heat disturbance during a microcosm experiment. The response of the respiration process was followed using substrate-induced respiration (SIR).

Results and discussion

The response of soil SIR to heat disturbance varied widely between samples. The variability of the SIR response increased just after the disturbance, and a global rather homogeneous decrease in SIR rates was observed 15 and 30 days after. The stability of SIR in response to heat disturbance could not be related to either the genetic or the metabolic diversity of the microbial community. The initial level of SIR before the disturbance was the soil variable that best correlated with the impact of the disturbance: the soil locations with the highest initial SIR rates were the most affected 15 and 30 days after the heat disturbance.

Conclusions

Such a heterogeneous response suggests that the response of soil processes to a disturbance will be difficult to assess from only local-scale analyses and highlights the need for spatial explicitness in understanding biogeochemical processes.

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References

  • Allison SD, Martiny JBH (2008) Resistance, resilience, and redundancy in microbial communities. Proc Natl Acad Sci U S A 105:11512–11519

    Article  CAS  Google Scholar 

  • Banning NC, Murphy DV (2008) Effect of heat-induced disturbance on microbial biomass and activity in forest soil and the relationship between disturbance effects and microbial community structure. Appl Soil Ecol 40:109–119

    Article  Google Scholar 

  • Barthes BG, Brunet D, Brauman A, Fromin N, Lensi R, Volant A, Laclau JP, Blavet D, Chapuis-Lardy L (2010) Determination of potential denitrification in a range of tropical topsoils using near infrared reflectance spectroscopy (NIRS). Appl Soil Ecol 46:81–89

    Article  Google Scholar 

  • Bottner P (1985) Response of microbial biomass to alternate moist and dry conditions in a soil incubated with C-14-labelled and N-15-labelled plant material. Soil Biol Biochem 17:329–337

    Article  CAS  Google Scholar 

  • Brown BL (2007) Habitat heterogeneity and disturbance influence patterns of community temporal variability in a small temperate stream. Hydrobiologia 586:93–106

    Article  Google Scholar 

  • de Boer W, Verheggen P, Gunnewiek P, Kowalchuk GA, van Veen JA (2003) Microbial community composition affects soil fungistasis. Appl Environ Microbiol 69:835–844

    Article  Google Scholar 

  • Degens BP, Schipper LA, Sparling GP, Duncan LC (2001) Is the microbial community in a soil with reduced catabolic diversity less resistant to stress or disturbance? Soil Biol Biochem 33:1143–1153

    Article  CAS  Google Scholar 

  • Donnelly SM, Kramer A (1999) Testing for multiple species in fossil samples: an evaluation and comparison of tests for equal relative variation. Am J Phys Anthropol 108:507–529

    Article  CAS  Google Scholar 

  • Ettema CH, Wardle DA (2002) Spatial soil ecology. Trends Ecol Evol 17:177–183

    Article  Google Scholar 

  • Fanin N, Barantal S, Hättenschwiler S, Schimann H, Fromin N (2011) Does variability in litter quality determine soil microbial respiration in a Amazonian rainforest? Soil Biol Biochem 43:1014–1022

    Article  CAS  Google Scholar 

  • Gessner MO, Inchausti P, Persson L, Raffaelli DG, Giller PS (2004) Biodiversity effects on ecosystem functioning: insights from aquatic systems. Oikos 104:419–422

    Article  Google Scholar 

  • Giller PS, Hillebrand H, Berninger UG, Gessner MO, Hawkins S, Inchausti P, Inglis C, Leslie H, Malmqvist B, Monaghan MT, Morin PJ, O'Mullan G (2004) Biodiversity effects on ecosystem functioning: emerging issues and their experimental test in aquatic environments. Oikos 104:423–436

    Article  Google Scholar 

  • Girvan MS, Campbell CD, Killham K, Prosser JI, Glover LA (2005) Bacterial diversity promotes community stability and functional resilience after perturbation. Environ Microbiol 7:301–313

    Article  CAS  Google Scholar 

  • Gourlet-Fleury S, Houllier F (2000) Modelling diameter increment in a lowland evergreen rain forest in French Guiana. Forest Ecol Manag 131:269–289

    Article  Google Scholar 

  • Griffiths BS, Ritz K, Bardgett RD, Cook R, Christensen S, Ekelund F, Sørensen S, Bååth S, Bloem J, de Ruiter PC, Dolfing J, Nicolardot B (2000) Ecosystem response of pasture soil communities to fumigation-induced microbial diversity reductions: an examination of the biodiversity–ecosystem function relationship. Oikos 90:279–294

    Article  Google Scholar 

  • Griffiths BS, Ritz K, Wheatley R, Kuan HL, Boag B, Christensen S, Ekelund F, Sørensen SJ, Muller S, Bloem J (2001) An examination of the biodiversity–ecosystem function relationship in arable soil microbial communities. Soil Biol Biochem 33:1713–1722

    Article  CAS  Google Scholar 

  • Griffiths BS, Kuan HL, Ritz K, Glover LA, McCaig AE, Fenwick C (2004) The relationship between microbial community structure and functional stability, tested experimentally in an upland pasture soil. Microb Ecol 47:104–113

    Article  CAS  Google Scholar 

  • Griffiths BS, Hallett PD, Kuan HL, Gregory AS, Watts CW, Whitmore AP (2008) Functional resilience of soil microbial communities depends on both soil structure and microbial community composition. Biol Fertil Soils 44:745–754

    Article  Google Scholar 

  • Hooper DU, Bignell DE, Brown VK, Brussaard L, Dangerfield JM, Wall DH, Wardle DA, Coleman DC, Giller KE, Lavelle P, van der Putten WH, de Ruiter PC, Rusek J, Silver WL, Tiedje JM, Wolters V (2000) Interactions between aboveground and belowground biodiversity in terrestrial ecosystems: patterns, mechanisms, and feedbacks. BioScience 50:1049–1061

    Article  Google Scholar 

  • Jossi M, Fromin N, Tarnawski S, Kohler F, Gillet F, Aragno M, Hamelin J (2006) How elevated pCO2 modifies total and metabolically active bacterial communities in the rhizosphere of two perennial grasses grown under field conditions. FEMS Microbiol Ecol 55:339–350

    Article  CAS  Google Scholar 

  • Katayama A, Kume T, Komatsu H, Ohashi M, Nakagawa M, Yamashita M, Otsuki K, Suzuki M, Kumagai T (2009) Effect of forest structure on the spatial variation in soil respiration in a Bornean tropical rainforest. Agr Forest Meteorol 149:1666–1673

    Article  Google Scholar 

  • Kuan HL, Hallett PD, Griffiths BS, Gregory AS, Watts CW, Whitmore AP (2007) The biological and physical stability and resilience of a selection of Scottish soils to stresses. Eur J Soil Sci 58:811–821

    Article  Google Scholar 

  • Kühlmann S, Hjorth U (2007) Accounting for large-scale factors in the study of understory vegetation using a conditional logistic model. Environ Ecol Stat 14:149–159

    Article  Google Scholar 

  • Kuuluvainen T, Pukkala T (1989) Effect of Scots pine seed trees on the density of ground vegetation and tree seedlings. Silva Fenn 23:159–167

    Google Scholar 

  • Lewis SL, Phillips OL, Baker TR, Lloyd J, Malhi Y, Almeida S, Higuchi N, Laurance WF, Neill DA, Silva JNM, Terborgh J, Lezama AT, Martinez RV, Brown S, Chave J, Kuebler C, Vargas PN, Vinceti B (2004) Concerted changes in tropical forest structure and dynamics: evidence from 50 South American long-term plots. Philos Trans R Soc B-Biol Sci 359:421–436

    Article  CAS  Google Scholar 

  • McClain ME, Boyer EW, Dent L, Gergel SE, Grimm NB, Groffman PM, Hart SC, Harvey JW, Johnston CA, Mayorga E, McDowell WH, Pinay G (2003) Biogeochemical hot spots and hot moments at the interface of terrestrial and aquatic ecosystems. Ecosystems 6:301–312

    Article  CAS  Google Scholar 

  • McGill BM, Sutton-Grier AE, Wright JP (2010) Plant trait diversity buffers variability in denitrification potential over changes in season and soil conditions. PLoS One 5:e11618

    Article  Google Scholar 

  • Michelland R, Monteils V, Zened A, Combes S, Cauquil L, Gidenne T, Hamelin J, Fortun-Lamothe L (2009) Bacterial communities of the bovine rumen and feces and relationship with ruminal parameters. J Appl Microbiol 107:1642–1650

    Article  CAS  Google Scholar 

  • Milcu A, Thebault E, Scheu S, Eisenhauer N (2010) Plant diversity enhances the reliability of belowground processes. Soil Biol Biochem 42:2102–2110

    Article  CAS  Google Scholar 

  • Morin PJ, McGrady-Steed J (2004) Biodiversity and ecosystem functioning in aquatic microbial systems: a new analysis of temporal variation and species richness–predictability relations. Oikos 104:458–466

    Article  Google Scholar 

  • Naeem S, Li SB (1997) Biodiversity enhances ecosystem reliability. Nature 390:507–509

    Article  CAS  Google Scholar 

  • Nannipieri P, Ascher J, Ceccherini MT, Landi L, Pietramellara G, Renella G (2003) Microbial diversity and soil functions. Eur J Soil Sci 54:655–670

    Article  Google Scholar 

  • Orwin KH, Wardle DA (2005) Plant species composition effects on belowground properties and the resistance and resilience of the soil microflora to a drying disturbance. Plant Soil 278:205–221

    Article  CAS  Google Scholar 

  • Pinay G, Barbera P, Carreras-Palou A, Fromin N, Sonié L, Coûteaux M-M, Roy J, Philippot L, Lensi R (2007) Impact of atmospheric CO2 concentration and vegetation plant life forms on soil microbial activities. Soil Biol Biochem 39:33–42

    Article  CAS  Google Scholar 

  • Ranjard L, Richaume A (2001) Quantitative and qualitative microscale distribution of bacteria in soil. Res Microbiol 152:707–716

    Article  CAS  Google Scholar 

  • Schimann H, Joffre R, Roggy J-C, Lensi R, Domenach A-M (2007) Evaluation of the recovery of microbial functions during soil restoration using near infra-red spectroscopy. Appl Soil Ecol 37:223–232

    Article  Google Scholar 

  • Seybold CA, Herrick JE, Brejda JJ (1999) Soil resilience: a fundamental component of soil quality. Soil Sci 164:224–234

    Article  CAS  Google Scholar 

  • Sodhi NS (2008) Invited views in basic and applied ecology—tropical biodiversity loss and people—a brief review. Basic Appl Ecol 9:93–99

    Article  Google Scholar 

  • Strickland MS, Lauber C, Fierer N, Bradford MA (2009) Testing the functional significance of microbial community composition. Ecology 90:441–451

    Article  Google Scholar 

  • Tilman D, Reich PB, Knops JMH (2006) Biodiversity and ecosystem stability in a decade-long grassland experiment. Nature 441:629–632

    Article  CAS  Google Scholar 

  • van Haren JLM, de Oliveira RC, Restrepo-Coupe N, Hutyra L, de Camargo PB, Keller M, Saleska SR (2010) Do plant species influence soil CO2 and N2O fluxes in a diverse tropical forest? J Geophys Res 115:GO 3010

    Google Scholar 

  • Wardle DA, Ghani A (1995) A critique of the microbial metabolic quotient (qCO2) as a bioindicator of disturbance and ecosystem development. Soil Biol Biochem 27:1601–1610

    Article  CAS  Google Scholar 

  • Wardle DA, Bonner KI, Barker GM (2000) Stability of ecosystem properties in response to above-ground functional group richness and composition. Oikos 89:11–23

    Article  Google Scholar 

  • Weigelt A, Schumacher J, Roscher C, Schmid B (2008) Does biodiversity increase spatial stability in plant community biomass? Ecol Lett 11:338–347

    Article  Google Scholar 

  • Wertz S, Degrange V, Prosser JI, Poly F, Commeaux C, Guillaumaud N, Le Roux X (2007) Decline of soil microbial diversity does not influence the resistance and resilience of key soil microbial functional groups following a model disturbance. Environ Microbiol 9:2211–2219

    Article  Google Scholar 

  • Wittebolle L, Marzorati M, Clement L, Balloi A, Daffonchio D, Heylen K, De Vos P, Verstraete W, Boon N (2009) Initial community evenness favours functionality under selective stress. Nature 458:623–626

    Article  CAS  Google Scholar 

  • Yachi S, Loreau M (1999) Biodiversity and ecosystem productivity in a fluctuating environment: the insurance hypothesis. Proc Natl Acad Sci U S A 96:1463–1468

    Article  CAS  Google Scholar 

  • Zemb O, Haegeman B, Delgenes JP, Lebaron P, Godon JJ (2007) SAFUM: statistical analysis of SSCP fingerprints using PCA projections, dendrograms and diversity estimators. Mol Ecol Notes 7:767–770

    Article  Google Scholar 

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Acknowledgments

This work was supported by ACI/Ecosphère Continentale, Fonctionnement et Dynamique de la Biosphère Continentale: Processus, Echanges de Matières et d’Energie, Modélisation (Centre National de la Recherche Scientifique, France) program DIPROTROFLUX (coordination J. Roy and A.-M. Domenach), and by “Fonds de Coopération Régional Guyane” (coordination J.C. Roggy). Laboratory analyses were performed at the “Plate-forme d’Analyses Chimiques en Ecologie”, platform of the Institut Fédératif de Recherche “Montpellier Environnement Biodiversité”, in Montpellier. We would like to thank Christophe Escape (UMR CEFE 5175, Montpellier) for microcosm conditioning, Didier Brunet (UMR Eco&Sols, Montpellier) for NIRS analyses, and Marjolaine Hamelin for editing.

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Authors and Affiliations

  1. CEFE, CNRS UMR 5175, 1919 Route de Mende, 34293, Montpellier cedex 5, France

    Nathalie Fromin, Robert Lensi & Bruno Buatois

  2. Université Montpellier 2, Place Eugène Bataillon, 34095, Montpellier cedex 5, France

    Benjamin Porte

  3. INRA, UR0050, Laboratoire de Biotechnologie de l’Environnement, 11100, Narbonne, France

    Jérôme Hamelin

  4. IRD UR SeqBio, 2 place Viala, 34060, Montpellier cedex 2, France

    Robert Lensi

  5. UMR EcoFoG, BP 709, 97387, Kourou, French Guiana

    Anne-Marie Domenach & Jean-Christophe Roggy

Authors
  1. Nathalie Fromin
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  2. Benjamin Porte
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  7. Jean-Christophe Roggy
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Correspondence to Nathalie Fromin.

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Responsible editor: Weixin Cheng

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Fromin, N., Porte, B., Lensi, R. et al. Spatial variability of the functional stability of microbial respiration process: a microcosm study using tropical forest soil. J Soils Sediments 12, 1030–1039 (2012). https://doi.org/10.1007/s11368-012-0528-7

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  • DOI: https://doi.org/10.1007/s11368-012-0528-7

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