Oecologia

, Volume 162, Issue 3, pp 763–769

Biodiversity at the plant–soil interface: microbial abundance and community structure respond to litter mixing

Ecosystem ecology - Original Paper

Abstract

The interactive effects of diversity in plants and microbial communities at the litter interface are not well understood. Mixtures of plant litter from different species often decompose differently than when individual species decompose alone. Previously, we found that litter mixtures of multiple conifers decomposed more rapidly than expected, but litter mixtures that included conifer and aspen litter did not. Understanding the mechanisms underlying these diversity effects may help explain existing anomalous decay dynamics and provide a glimpse into the elusive linkage between plant diversity and the fungi and bacteria that carry out decomposition. We examined the microbial communities on litter from individual plant species decomposing both in mixture and alone. We assessed two main hypotheses to explain how the decomposer community could stimulate mixed-litter decomposition above predicted rates: either by being more abundant, or having a different or more diverse community structure than when microbes decompose a single species of litter. Fungal, bacterial and total phospholipid fatty acid microbial biomass increased by over 40% on both conifer and aspen litter types in mixture, and microbial community composition changed significantly when plant litter types were mixed. Microbial diversity also increased with increasing plant litter diversity. While our data provide support for both the increased abundance hypothesis and the altered microbial community hypothesis, microbial changes do not translate to predictably altered litter decomposition and may only produce synergisms when mixed litters are functionally similar.

Keywords

Bacteria Fungi Litter mixing Litter decomposition Microbial community 

References

  1. Ball BA, Hunter MD, Kominoski JS, Swan CM, Bradford MA (2008) Consequences of non-random species loss for decomposition dynamics: experimental evidence for additive and non-additive effects. J Ecol 96:303–313. doi:10.1111/j.1365-2745.2007.01346.x CrossRefGoogle Scholar
  2. Bardgett RD, Shine A (1999) Linkages between plant litter diversity, soil microbial biomass and ecosystem function in temperate grasslands. Soil Biol Biochem 31:317–321CrossRefGoogle Scholar
  3. Bardgett RD, Walker LR (2004) Impact of coloniser plant species on the development of decomposer microbial communities following deglaciation. Soil Biol Biochem 36:555–559. doi:10.1016/j.soilbio.2003.11.002 CrossRefGoogle Scholar
  4. Blair JM, Parmelee RW, Beare MH (1990) Decay-rates, nitrogen fluxes, and decomposer communities of single-species and mixed-species foliar litter. Ecology 71:1976–1985CrossRefGoogle Scholar
  5. Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37:911–917PubMedGoogle Scholar
  6. Briones MJ, Ineson P (1996) Decomposition of eucalyptus leaves in litter mixtures. Soil Biol Biochem 28:1381–1388CrossRefGoogle Scholar
  7. Chapman SK, Koch GW (2007) What type of diversity yields synergy during mixed litter decomposition in a natural forest ecosystem? Plant Soil 299:153–162. doi:10.1007/s11104-007-9372-8ER CrossRefGoogle Scholar
  8. Chapman K, Whittaker JB, Heal OW (1988) Metabolic and faunal activity in litters of tree mixtures compared with pure stands. Agric Ecosyst Environ 24:33–40CrossRefGoogle Scholar
  9. Costerton JW, Lewandowski Z, Caldwell DE, Korber DR, Lappinscott HM (1995) Microbial biofilms. Annu Rev Microbiol 49:711–745CrossRefPubMedGoogle Scholar
  10. Dehlin H, Nilsson MC, Wardle DA (2006) Aboveground and belowground responses to quality and heterogeneity of organic inputs to the boreal forest. Oecologia 150:108–118CrossRefPubMedGoogle Scholar
  11. Frostegard A, Baath E (1996) The use of phospholipid fatty acid analysis to estimate bacterial and fungal biomass in soil. Biol Fertil Soils 22:59–65CrossRefGoogle Scholar
  12. Gartner TB, Cardon ZG (2004) Decomposition dynamics in mixed-species leaf litter. Oikos 104:230–246CrossRefGoogle Scholar
  13. Hansen RA, Coleman DC (1998) Litter complexity and composition are determinants of the diversity and species composition of oribatid mites (acari: Oribatida) in litterbags. Appl Soil Ecol 9:17–23CrossRefGoogle Scholar
  14. Hättenschwiler S, Gasser P (2005) Soil animals alter plant litter diversity effects on decomposition. Proc Natl Acad Sci USA 102:1519–1524. doi:10.1073/pnas.0404977102 CrossRefPubMedGoogle Scholar
  15. Hättenschwiler S, Tiunov AV, Scheu S (2005) Biodiversity and litter decomposition in terrestrial ecosystems. Annu Rev Ecol Evol Sys 36:191–218. doi:10.1146/annurev.ecolsys.36.112904.51932 CrossRefGoogle Scholar
  16. Hooper DU, Vitousek PM (1998) Effects of plant composition and diversity on nutrient cycling. Ecol Monogr 68:121–149CrossRefGoogle Scholar
  17. Hoorens B, Aerts R, Stroetenga M (2003) Litter quality and interactive effects in litter mixtures: more negative interactions under elevated CO2? J Ecol 90:1009–1016CrossRefGoogle Scholar
  18. Hutchinson GE (1959) Homage to Santa Rosalia or Why are there so many kinds of animals? Am Nat 93:145–159CrossRefGoogle Scholar
  19. Jonsson M, Wardle DA (2008) Context dependency of litter-mixing effects on decomposition and nutrient release across a long-term chronosequence. Oikos 117:1674–1682CrossRefGoogle Scholar
  20. Kaneko N, Salamanca EF (1999) Mixed leaf litter effects on decomposition rates and soil microarthropod communities in an oak-pine stand in Japan. Ecol Res 14:131–138CrossRefGoogle Scholar
  21. Keith AM, van der Wal R, Brooker RW, Osler GHR, Chapman SJ, Burslem DFRP, Elston DA (2008) Increasing litter specie richness reduces variability in a terrestrial decomposer system. Ecology 89:2657–2664CrossRefPubMedGoogle Scholar
  22. Kominoski JS, Pringle CM, Ball BA, Bradford MA, Coleman DC, Hall DB, Hunter MD (2007) Nonadditive effects of litter species diversity on breakdown dynamics in a detritus-based stream. Ecology 88:1167–1176CrossRefPubMedGoogle Scholar
  23. Kominoski JS, Hoellein TJ, Kelly JJ, Pringle CM (2009) Does mixing litter of different qualities alter stream microbial diversity and functioning on individual litter species? Oikos 118:457–463CrossRefGoogle Scholar
  24. Laitung B, Chauvet E (2005) Vegetation diversity increases species richness of leaf-decaying fungal communities in woodland streams. Arch Hydrobiol 164:217–235CrossRefGoogle Scholar
  25. Leckie SE (2005) Methods of microbial community profiling and their application to forest soils. For Ecol Manage 220:88–106. doi:10.1016/j.foreco.2005.08.007 CrossRefGoogle Scholar
  26. LeRoy CJ, Marks JC (2006) Litter quality, stream characteristics and litter diversity influence decomposition rates and macroinvertebrates. Freshwater Biol 51:605–617CrossRefGoogle Scholar
  27. Loreau M (2001) Microbial diversity, producer–decomposer interactions and ecosystem processes: a theoretical model. Proc R Soc Lond Biol 268:303–309CrossRefGoogle Scholar
  28. Madritch M, Donaldson JR, Lindroth RL (2006) Genetic identity of populus tremuloides litter influences decomposition and nutrient release in a mixed forest stand. Ecosystems 9:528–537CrossRefGoogle Scholar
  29. Mcarthur JV, Aho JM, Rader RB, Mills GL (1994) Interspecific leaf interactions during decomposition in aquatic and floodplain ecosystems. J N Am Benthol Soc 13:57–67CrossRefGoogle Scholar
  30. McTiernan KB, Ineson P, Coward PA (1997) Respiration and nutrient release from tree leaf litter mixtures. Oikos 78:527–538CrossRefGoogle Scholar
  31. Meier CL, Bowman WD (2008) Links between plant litter chemistry, species diversity and below-ground ecosystem function. Proc Natl Acad Sci USA 105:19780–19785CrossRefPubMedGoogle Scholar
  32. O’Leary WM, Wilkinson WK (1988) Gram-positive bacteria. In: Ratledge C, Wilkinson SJ (eds) Microbial lipids. Academic Press, London, pp 117–207Google Scholar
  33. Parton W, Silver WL, Burke IC, Grassens L, Harmon ME, Currie WS, King JY, Adair EC, Brandt LA, Hart SC, Fasth B (2007) Global-scale similarities in nitrogen release patterns during long-term decomposition. Science 315:361–364. doi:10.1126/science.1134853 CrossRefPubMedGoogle Scholar
  34. Quested HM, Press MC, Callaghan CV, Cornelissen JHC (2002) The hemiparasitic angiosperm Barsia alpina has the potential to accelerate decomposition in subarctic communities. Oecologia 130:88–95Google Scholar
  35. Ramsey PW, Rillig MC, Feris KP, Holben WE, Gannon JE (2006) Choice of methods for soil microbial community analysis: PLFA maximizes power compared to CLPP and PCR-based approaches. Pedobiologia 50:275–280. doi:10.1016/j.pedobi.2006.03.003 CrossRefGoogle Scholar
  36. Rustad LE (1994) Element dynamics along a decay continuum in a red spruce ecosystem in Maine, USA. Ecology 75:867–879CrossRefGoogle Scholar
  37. Schimel JP, Hättenschwiler S (2007) Nitrogen transfer between decomposing leaves of different N status. Soil Biol Biochem 39:1428–1436. doi:10.1016/j.soilbio.2006.12.037 CrossRefGoogle Scholar
  38. Schweitzer JA, Bailey JK, Hart SC, Whitham TG (2005) Nonadditive effects of mixing cottonwood genotypes on litter decomposition and nutrient dynamics. Ecology 86:2834–2840CrossRefGoogle Scholar
  39. Schweitzer JA, Bailey JK, Fischer DG, LeRoy CJ, Lonsdorf EV, Whitham TG, Hart SC (2008) Plant–soil–microorganism interactions: heritable relationship between plant genotype and associated soil microorganisms. Ecology 89:773–781CrossRefPubMedGoogle Scholar
  40. Seastedt TR (1984) The role of microarthropods in decomposition and mineralization processes. Annu Rev Entomol 29:25–46CrossRefGoogle Scholar
  41. Siemann E, Tilman D, Harstaad J, Ritchie M (1998) Experimental tests of the dependence of arthropod diversity on plant diversity. Am Nat 152:738–750CrossRefPubMedGoogle Scholar
  42. Swan CM, Palmer MA (2006) Composition of speciose leaf litter alters stream detritivore growth, feeding activity and leaf breakdown. Oecologia 147:469–478CrossRefPubMedGoogle Scholar
  43. Tilman D, Lehman CL, Thomson KT (1997) Plant diversity and ecosystem productivity: theoretical considerations. Proc Natl Acad Sci USA 94:1857–1861CrossRefPubMedGoogle Scholar
  44. van der Heijden MGA, Bardgett RD, van Straalen NM (2008) The unseen majority: Soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecol Lett 11:296–310. doi: 10.1111/j.1461-0248.2007.01139.x ER CrossRefPubMedGoogle Scholar
  45. Vivanco L, Austin AT (2008) Tree species identity alters forest litter decomposition through long-term plant and soil interactions in Patagonia, Argentina. J Ecol 96:727–736CrossRefGoogle Scholar
  46. Wang S, Ruan H, Wang B (2009) Effects of soil microarthropods on plant litter decomposition across an elevation gradient in the Wuyi Mountains. Soil Biol Biochem 41:891–897. doi:10.1016/j.soilbio.2008.12.016 CrossRefGoogle Scholar
  47. Wardle DA, Nicholson KS (1996) Synergistic effects of grassland plant species on soil microbial biomass and activity: Implications for ecosystem-level effects of enriched plant diversity. Funct Ecol 10:410–416CrossRefGoogle Scholar
  48. 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 79:247–258CrossRefGoogle Scholar
  49. Wardle DA, Yeates GW, Barker GM, Bonner KI (2006) The influence of plant litter diversity on decomposer abundance and diversity. Soil Biol Biochem 38:1052–1062. doi:10.1016/j.soilbio.2005.09.003 CrossRefGoogle Scholar
  50. White DC, Davis WM, Nickels JS, King JD, Bobbie RJ (1979) Determination of the sedimentary microbial biomass by extractable lipid phosphate. Oecologia 40:51–62CrossRefGoogle Scholar
  51. Wilkinson SJ (1988) Gram negative bacteria. In: Ratledge C, Wilkinson SJ (eds) Microbial lipids. Academic Press, London, pp 299–488Google Scholar
  52. Zelles L (1999) Fatty acid patterns of phospholipids and lipopolysaccharides in the characterisation of microbial communities in soil: a review. Biol Fertil Soils 29:111–129CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  1. 1.Department of BiologyVillanova UniversityVillanovaUSA
  2. 2.School of ForestryNorthern Arizona UniversityFlagstaffUSA

Personalised recommendations