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

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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.

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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

  2. Bardgett RD, Shine A (1999) Linkages between plant litter diversity, soil microbial biomass and ecosystem function in temperate grasslands. Soil Biol Biochem 31:317–321

  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

  4. Blair JM, Parmelee RW, Beare MH (1990) Decay-rates, nitrogen fluxes, and decomposer communities of single-species and mixed-species foliar litter. Ecology 71:1976–1985

  5. Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37:911–917

  6. Briones MJ, Ineson P (1996) Decomposition of eucalyptus leaves in litter mixtures. Soil Biol Biochem 28:1381–1388

  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

  8. Chapman K, Whittaker JB, Heal OW (1988) Metabolic and faunal activity in litters of tree mixtures compared with pure stands. Agric Ecosyst Environ 24:33–40

  9. Costerton JW, Lewandowski Z, Caldwell DE, Korber DR, Lappinscott HM (1995) Microbial biofilms. Annu Rev Microbiol 49:711–745

  10. Dehlin H, Nilsson MC, Wardle DA (2006) Aboveground and belowground responses to quality and heterogeneity of organic inputs to the boreal forest. Oecologia 150:108–118

  11. Frostegard A, Baath E (1996) The use of phospholipid fatty acid analysis to estimate bacterial and fungal biomass in soil. Biol Fertil Soils 22:59–65

  12. Gartner TB, Cardon ZG (2004) Decomposition dynamics in mixed-species leaf litter. Oikos 104:230–246

  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 9:17–23

  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

  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

  16. Hooper DU, Vitousek PM (1998) Effects of plant composition and diversity on nutrient cycling. Ecol Monogr 68:121–149

  17. Hoorens B, Aerts R, Stroetenga M (2003) Litter quality and interactive effects in litter mixtures: more negative interactions under elevated CO2? J Ecol 90:1009–1016

  18. Hutchinson GE (1959) Homage to Santa Rosalia or Why are there so many kinds of animals? Am Nat 93:145–159

  19. Jonsson M, Wardle DA (2008) Context dependency of litter-mixing effects on decomposition and nutrient release across a long-term chronosequence. Oikos 117:1674–1682

  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 14:131–138

  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 89:2657–2664

  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 88:1167–1176

  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 118:457–463

  24. Laitung B, Chauvet E (2005) Vegetation diversity increases species richness of leaf-decaying fungal communities in woodland streams. Arch Hydrobiol 164:217–235

  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

  26. LeRoy CJ, Marks JC (2006) Litter quality, stream characteristics and litter diversity influence decomposition rates and macroinvertebrates. Freshwater Biol 51:605–617

  27. Loreau M (2001) Microbial diversity, producer–decomposer interactions and ecosystem processes: a theoretical model. Proc R Soc Lond Biol 268:303–309

  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 9:528–537

  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 13:57–67

  30. McTiernan KB, Ineson P, Coward PA (1997) Respiration and nutrient release from tree leaf litter mixtures. Oikos 78:527–538

  31. Meier CL, Bowman WD (2008) Links between plant litter chemistry, species diversity and below-ground ecosystem function. Proc Natl Acad Sci USA 105:19780–19785

  32. O’Leary WM, Wilkinson WK (1988) Gram-positive bacteria. In: Ratledge C, Wilkinson SJ (eds) Microbial lipids. Academic Press, London, pp 117–207

  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

  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 130:88–95

  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

  36. Rustad LE (1994) Element dynamics along a decay continuum in a red spruce ecosystem in Maine, USA. Ecology 75:867–879

  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

  38. Schweitzer JA, Bailey JK, Hart SC, Whitham TG (2005) Nonadditive effects of mixing cottonwood genotypes on litter decomposition and nutrient dynamics. Ecology 86:2834–2840

  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 89:773–781

  40. Seastedt TR (1984) The role of microarthropods in decomposition and mineralization processes. Annu Rev Entomol 29:25–46

  41. Siemann E, Tilman D, Harstaad J, Ritchie M (1998) Experimental tests of the dependence of arthropod diversity on plant diversity. Am Nat 152:738–750

  42. Swan CM, Palmer MA (2006) Composition of speciose leaf litter alters stream detritivore growth, feeding activity and leaf breakdown. Oecologia 147:469–478

  43. Tilman D, Lehman CL, Thomson KT (1997) Plant diversity and ecosystem productivity: theoretical considerations. Proc Natl Acad Sci USA 94:1857–1861

  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

  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 96:727–736

  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

  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 10:410–416

  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 79:247–258

  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

  50. White DC, Davis WM, Nickels JS, King JD, Bobbie RJ (1979) Determination of the sedimentary microbial biomass by extractable lipid phosphate. Oecologia 40:51–62

  51. Wilkinson SJ (1988) Gram negative bacteria. In: Ratledge C, Wilkinson SJ (eds) Microbial lipids. Academic Press, London, pp 299–488

  52. Zelles L (1999) Fatty acid patterns of phospholipids and lipopolysaccharides in the characterisation of microbial communities in soil: a review. Biol Fertil Soils 29:111–129

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Acknowledgments

A Smithsonian Institution Fellowship and Villanova University funded S. K. C. during part of the development of this manuscript. Partial funding for this research was provided by McIntire-Stennis appropriations to the NAU School of Forestry and G. S. N. We acknowledge Jennifer Schweitzer, Adam Langley, and Jennifer Pett-Ridge for friendly reviews of this manuscript. We thank George Koch and Steve Hart for guidance and lab facilities. We thank Steve Overby and particularly Dana Erickson at the USFS Rocky Mountain Research Station for assistance in PLFA extraction and analysis. Kitty Gehring, Bruce Hungate, Maribeth Watwood, and Tom Whitham provided additional help with this manuscript. Arisia Lee and Dan Guido assisted with lab work. All experiments we performed correspond with the laws of the United States of America.

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Correspondence to Samantha K. Chapman.

Additional information

Communicated by Stephan Hattenschwiler.

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Chapman, S.K., Newman, G.S. Biodiversity at the plant–soil interface: microbial abundance and community structure respond to litter mixing. Oecologia 162, 763–769 (2010). https://doi.org/10.1007/s00442-009-1498-3

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Keywords

  • Bacteria
  • Fungi
  • Litter mixing
  • Litter decomposition
  • Microbial community