Skip to main content
Log in

Plant Communities, Soil Microorganisms, and Soil Carbon Cycling: Does Altering the World Belowground Matter to Ecosystem Functioning?

  • Published:
Ecosystems Aims and scope Submit manuscript

Abstract

Soil microorganisms mediate many critical ecosystem processes. Little is known, however, about the factors that determine soil microbial community composition, and whether microbial community composition influences process rates. Here, we investigated whether aboveground plant diversity affects soil microbial community composition, and whether differences in microbial communities in turn affect ecosystem process rates. Using an experimental system at La Selva Biological Station, Costa Rica, we found that plant diversity (plots contained 1, 3, 5, or > 25 plant species) had a significant effect on microbial community composition (as determined by phospholipid fatty acid analysis). The different microbial communities had significantly different respiration responses to 24 labile carbon compounds. We then tested whether these differences in microbial composition and catabolic capabilities were indicative of the ability of distinct microbial communities to decompose different types of litter in a fully factorial laboratory litter transplant experiment. Both microbial biomass and microbial community composition appeared to play a role in litter decomposition rates. Our work suggests, however, that the more important mechanism through which changes in plant diversity affect soil microbial communities and their carbon cycling activities may be through alterations in their abundance rather than their community composition.

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

Access this article

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

Instant access to the full article PDF.

Figure 1
Figure 2
Figure 3
Figure 4
Figure 5

Similar content being viewed by others

References

  • Amann RI, Ludwig W, Schleifer KH. 1995. Phylogenetic identification and in situ detection of individual cells without cultivation. Microbiol Rev 59:143–69

    PubMed  CAS  Google Scholar 

  • Angers DA, Caron J. 1998. Plant-induced changes in soil structure: processes and feedbacks. Biogeochemistry 42:55–72

    Article  Google Scholar 

  • Baath E, Anderson T.-H. 2003. Comparison of soil fungal/bacterial ratios in a pH gradient using physiological and PLFA-based techniques. Soil Biol Biochem 35:955–63

    CAS  Google Scholar 

  • Bardgett RD, Shine A. 1999. Linkages between plant litter diversity, soil microbial biomass and ecosystem function in temperate grasslands. Soil Biol Biochem 31:317–21

    CAS  Google Scholar 

  • Borga P, Nilsson M, Tunlid A. 1994. Bacterial communities in peat in relation to botanical composition as revealed by phospholipid fatty-acid analysis. Soil Biol Biochem 26:841–8

    Article  CAS  Google Scholar 

  • Bossio DA, Scow KM. 1998. Impacts of carbon and flooding on soil microbial communities: Phospholipid fatty acid profiles and substrate utilization patterns. Microb Ecol 35:265–278

    Article  PubMed  CAS  Google Scholar 

  • Broughton LC, Gross KL. 2000. Patterns of diversity in plant and soil microbial communities along a productivity gradient in a Michigan old-field. Oecologia 125:420–427

    Article  Google Scholar 

  • Carney KM. 2003. The influence of plant diversity and land use on the composition and function of soil microbial communities. Stanford (CA): Doctoral Dissertation Stanford University

    Google Scholar 

  • Carney K, Matson PA, Bohannan BJM. 2004. Diversity and composition of tropical soil nitrifiers across a plant diversity gradient and among land-use types. Ecology Letters. 7:684–694

    Article  Google Scholar 

  • Cavigelli MA, Robertson GP. 2000. The functional significance of denitrifier community composition in a terrestrial ecosystem. Ecology 81:1402–14

    Google Scholar 

  • Chapin FS, Sala OE, Burke IC, Grime JP, Hooper DU, Lauenroth WK, Lombard A, Mooney HA, Mosier AR, Naeem S, Pacala SW, Roy J, Steffen WL, Tilman D. 1998. Ecosystem consequences of changing biodiversity: Experimental evidence and a research agenda for the future. Bioscience 48:45–52

    Google Scholar 

  • Clarke KR, Warwick RM. 2001. Change in marine communities: an approach to statistical analysis and interpretation. 2nd edn. Plymouth (UK): Plymouth Marine Laboratory

    Google Scholar 

  • Coyne MS. 1999. Soil microbiology: an exploratory approach. 2nd edn. Albany (NY): Delmar Publishers

    Google Scholar 

  • Degens BP. 1998. Decreases in microbial functional diversity do not result in corresponding changes in decomposition under different moisture conditions. Soil Biol Biochem 30:1989–2000

    CAS  Google Scholar 

  • Degens BP, Harris JA. 1997. Development of a physiological approach to measuring the catabolic diversity of soil microbial communities. Soil Biol Biochem 29:1309–20

    Article  CAS  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 33:1143–53

    Article  CAS  Google Scholar 

  • Degens BP, Schipper LA, Sparling GP, VojvodicVukovic M. 2000. Decreases in organic C reserves in soils can reduce the catabolic diversity of soil microbial communities. Soil Biol Biochem 32:189–96

    Article  CAS  Google Scholar 

  • Fernandez A, Huang SY, Seston S, Xing J, Hickey R, Criddle C, Tiedje J. 1999. How stable is stable? Function versus community composition. Appl Environ Microbiol 65:3697–04

    PubMed  CAS  Google Scholar 

  • Gartner T, Cardon Z. 2004. Decomposition dynamics in mixed-species leaf litter. Oikos 104:230–46

    Article  Google Scholar 

  • Gholz H, Wedin D, Smitherman S, Harmon M, Parton W. 2000. Long-term dynamics of pine and hardwood litter in contrasting environments: toward a global model of decomposition. Glob Change Biol 6:751–65

    Article  Google Scholar 

  • Grayston SJ, Griffith GS, Mawdsley JL, Campbell CD, Bardgett RD. 2001. Accounting for variability in soil microbial communities of temperate upland grassland ecosystems. Soil Biol Biochem 33:533–51

    Article  CAS  Google Scholar 

  • Griffiths B, Ritz K, Bardgett R, Cook R, Christensen S, Ekelund F, Sorensen S, Baath E, Bloem J, de Ruiter P, 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 90:279–94

    Article  Google Scholar 

  • Griffiths BS, Ritz K, Wheatley R, Kuan HL, Boag B, Christensen S, Ekelund F, Sorensen SJ, Muller S, Bloem J. 2001. An examination of the biodiversity-ecosystem function relationship in arable soil microbial communities. Soil Biol Biochem 33:1713–22

    Article  CAS  Google Scholar 

  • Haack SK, Garchow H, Odelson DA, Forney LJ, Klug MJ. 1994. Accuracy, reproducibility, and interpretation of fatty-acid methyl-ester profiles of model bacterial communities. Appl Environ Microbiol 60:2483–93

    CAS  Google Scholar 

  • Haggar JP, Ewel JJ. 1995. Establishment, resource acquisition, and early productivity as determined by biomass allocation patterns of 3 tropical tree species. For Sci 41:689–708

    Google Scholar 

  • Hammel KE. 1997. Fungal degradation of lignin. In: Giller KE, Ed. Driven by nature: plant litter quality and decomposition. Wallingford (UK): CAB International, p 33–45

    Google Scholar 

  • Hobbie S. 1996. Temperature and plant species control over litter decomposition in Alaskan tundra. Ecol Monogr 66:503–22

    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 50:1049–61

    Google Scholar 

  • Hooper DU, Vitousek PM. 1997. The effects of plant composition and diversity on ecosystem processes. Science 277:1302–5

    Article  CAS  Google Scholar 

  • Huston MA. 1997. Hidden treatments in ecological experiments: Re-evaluating the ecosystem function of biodiversity. Oecologia 110:449–460

    Article  Google Scholar 

  • Johnson D, Booth R, Whiteley A, Bailey M, Read D, Grime J, Leake J. 2003. Plant community composition affects the biomass, activity and diversity of microorganisms in limestone grassland soil. Eur J Soil Sci 54:671–7

    Google Scholar 

  • Karthikeyan S, Wolfaardt GM, Korber DR, Caldwell DE. 1999. Functional and structural responses of a degradative microbial community to substrates with varying degrees of complexity in chemical structure. Microb Ecol 38:215–24

    Article  PubMed  CAS  Google Scholar 

  • Konopka A, Oliver L, Turco RF. 1998. The use of carbon substrate utilization patterns in environmental and ecological microbiology. Microb Ecol 35:103–15

    Article  PubMed  CAS  Google Scholar 

  • Lawton JH, Naeem S, Thompson LJ, Hector A, Crawley MJ. 1998. Biodiversity and ecosystem function: getting the Ecotron experiment in its correct context. Funct Ecol 12:848–52

    Google Scholar 

  • Leckie S, Prescott C, Grayston S, Neufeld J, Mohn W. 2004. Comparison of chloroform fumigation-extraction, phospholipid fatty acid, and DNA methods to determine microbial biomass in forest humus. Soil Biology & Biochemistry 36:529–32

    Article  CAS  Google Scholar 

  • Madigan MT, Martinko JM, Parker J. 2000. Biology of Microorganisms. 9th edn. New Jersey: Prentice-Hall

    Google Scholar 

  • Magurran AE. 1988. Ecological diversity and its meausurement. Princeton (N J): Princeton University Press

    Google Scholar 

  • Marschner P, Yang CH, Lieberei R, Crowley DE. 2001. Soil and plant specific effects on bacterial community composition in the rhizosphere. Soil Biology & Biochemistry 33:1437–1445

    Article  CAS  Google Scholar 

  • McGrady-Steed J, Harris PM, Morin PJ. 1997. Biodiversity regulates ecosystem predictability. Nature 390:162–165

    CAS  Google Scholar 

  • Naeem S, Hahn DR, Schuurman G. 2000. Producer-decomposer co-dependency influences biodiversity effects. Nature 403:762–4

    Article  PubMed  CAS  Google Scholar 

  • Naeem S, Thompson LJ, Lawler SP, Lawton JH, Woodfin RM. 1994. Declining biodiversity can alter the performance of ecosystems. Nature 368:734–7

    Article  Google Scholar 

  • Navarrete A, Peacock A, McNaughton S, Urmeneta J, Mas-Castella J, White DC, Guerrero R. 2000. Physiological status and community composition of microbial mats of the Ebro Delta, Spain, by signature lipid biomarkers. Microb Ecol 39:92–9

    Article  PubMed  CAS  Google Scholar 

  • Olsen SR, Sommers LE. 1982. Phosphorus. In: Page AL, Miller RH, Keeney DR, Eds. Methods of soil analysis Part 2. Madison: American Society of Agronomy p 401–30

    Google Scholar 

  • Reichardt W, Mascarina G, Padre B, Doll J. 1997. Microbial communities of continuously cropped, irrigated rice fields. Appl Environ Microbiol 63:233–8

    CAS  Google Scholar 

  • Rosenzweig ML. 1995. Species diversity in space and time. Cambridge (UK): Cambridge University Press

    Google Scholar 

  • Russell AE, Cambardella CA, Ewel JJ, Parkin TB. 2004. Species, rotation, and life-form diversity effects on soil carbon in experimental tropical ecosystems. Ecology 14:47–60

    Google Scholar 

  • Schimel J. 1995. Ecosystem consequences of microbial diversity and community structure. In: Chapin FS, Koerner C, Eds. Arctic and alpine biodiversity: patterns, causes, and ecosystem consequences. Berlin Heildelberg New York: Springer, p 239–354

    Google Scholar 

  • Schipper L, Degens B, Sparling G, Duncan L. 2001. Changes in microbial heterotrophic diversity along five plant successional sequences. Soil Biol Biochem 33:2093–103

    Article  CAS  Google Scholar 

  • Schlesinger WH. 1997. Biogeochemistry: an analysis of global change. 2nd edn. San Diego: Academic Press

    Google Scholar 

  • Smalla K, Wieland G, Buchner A, Zock A, Parzy J, Kaiser S, Roskot N, Heuer H, Berg G. 2001. Bulk and rhizosphere soil bacterial communities studied by denaturing gradient gel electrophoresis: Plant-dependent enrichment and seasonal shifts revealed. Appl Environ Microbiol 67:4742–51

    Article  PubMed  CAS  Google Scholar 

  • Stephan A, Meyer A, Schmid B. 2000. Plant diversity affects culturable soil bacteria in experimental grassland communities. J Ecol 88:988–98

    Article  Google Scholar 

  • Sugai SF, Schimel JP. 1993. Decomposition and biomass incorporation of C-14-Labeled glucose and phenolics in taiga forest floor: effect of substrate quality, successional state, and season. Soil Biol Biochem 25:1379–1389

    Article  CAS  Google Scholar 

  • Tabachnik BG, Fidell LS. 1996. Using multivariate statistics. 3rd edn. New York: HarperCollins College Publisher

    Google Scholar 

  • Tilman D. 1996. Biodiversity: Population versus ecosystem stability. Ecology 77:350–363

    Google Scholar 

  • Tilman D. 1999. The ecological consequences of changes in biodiversity: A search for general principles. Ecology 80:1455–74

    Google Scholar 

  • Tilman D, Downing JA. 1994. Biodiversity and stability in grasslands. Nature 367:363–5

    Article  Google Scholar 

  • Torsvik V, Goksoyr J, Daae, FL. 1990. High diversity in DNA of soil bacteria. Appl Environ Microbiol 56:782–787

    PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Vitousek PM. 1994. Beyond global warming: ecology and global change. Ecology 75:1861–76

    Google Scholar 

  • Waldrop MP, Balser TC, Firestone MK. 2000. Linking microbial community composition to function in a tropical soil. Soil Biol Biochem 32:1837–1846

    Article  CAS  Google Scholar 

  • Wardle D, Yeates G, Williamson W, Bonner K. 2003. The response of a three trophic level soil food web to the identity and diversity of plant species and functional groups. Oikos 102:45–56

    Article  Google Scholar 

  • Wardle DA. 1999. Is “‘sampling effect” a problem for experiments investigating biodiversity-ecosystem function relationships? Oikos 87:403–7

    Google Scholar 

  • Wardle DA, Bonner KI, Nicholson KS. 1997. Biodiversity and plant litter: Experimental evidence which does not support the view that enhanced species richness improves ecosystem function. Oikos 79:247–58

    Google Scholar 

  • White DC, Ringelberg DB. 1998. Signature lipid biomarker anlaysis. In. Burlage RS, Atals R, Stahl D, Geesey G, Sayler G, Eds. Techniques in microbial ecology. New York: Oxford University Press, p 255–72

    Google Scholar 

  • Wieland G, Neumann R, Backhaus H. 2001. Variation of microbial communities in soil, rhizosphere, and rhizoplane in response to crop species, soil type, and crop development. Appl Environ Microbiol 67:5849–54

    Article  PubMed  CAS  Google Scholar 

  • Zak DR, Holmes WE, White DC, Peacock AD, Tilman D. 2003. Plant diversity, microbial communities, and ecosystem function: are there any links? Ecology 84:2042–50

    Google Scholar 

Download references

Acknowledgements

We thank Jack Ewel for his generosity in sharing his field sites, staff, equipment, knowledge, and guidance throughout this project. We also thank Brendan Bohannan and Peter Vitousek for aiding the direction of the research, Alex Reich and Ricardo Bedoya for field and logistical support, and the Huertos crew for help in the field. Thanks also to Steven Allison, Teri Balser, Peter Jewett, Ryan King, Ian Monroe, Zenobia Moore, and Martha Roberts for help with laboratory and statistical analyses. The manuscript greatly benefited from suggestions made by Kathleen Boomer, Aimee Classen, Claire Horner-Devine, Amy Luers, Pat Megonigal, Stephen Porder, and Taylor Ricketts. The National Science Foundation Graduate Fellowship Program, NSF Doctoral Dissertation Improvement Grant No. 0205959, NSF awards DEB 90318403 and DEB 9623969, the Stanford University School of Earth Sciences McGee Fund, and a grant from the A. W. Mellon Foundation to Pamela Matson supported this research.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Karen M. Carney.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Carney, K.M., Matson, P.A. Plant Communities, Soil Microorganisms, and Soil Carbon Cycling: Does Altering the World Belowground Matter to Ecosystem Functioning?. Ecosystems 8, 928–940 (2005). https://doi.org/10.1007/s10021-005-0047-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10021-005-0047-0

Keywords

Navigation