Microbial Ecology

, Volume 61, Issue 2, pp 399–409 | Cite as

Placing the Effects of Leaf Litter Diversity on Saprotrophic Microorganisms in the Context of Leaf Type and Habitat

  • Lan Wu
  • Larry M. Feinstein
  • Oscar Valverde-Barrantes
  • Mark W. Kershner
  • Laura G. Leff
  • Christopher B. Blackwood
Environmental Microbiology

Abstract

Because of conflicting results in previous studies, it is unclear whether litter diversity has a predictable impact on microbial communities or ecosystem processes. We examined whether effects of litter diversity depend on factors that could confound comparisons among previous studies, including leaf type, habitat type, identity of other leaves in the mixture, and spatial covariance at two scales within habitats. We also examined how litter diversity affects the saprotrophic microbial community using terminal restriction fragment length polymorphism to profile bacterial and fungal community composition, direct microscopy to quantify bacterial biomass, and ergosterol extraction to quantify fungal biomass. We found that leaf mixture diversity was rarely significant as a main effect (only for fungal biomass), but was often significant as an interaction with leaf type (for ash-free dry mass recovered, carbon-to-nitrogen ratio, fungal biomass, and bacterial community composition). Leaf type and habitat were significant as main effects for all response variables. The majority of variance in leaf ash-free dry mass and C/N ratio was explained after accounting for treatment effects and spatial covariation at the meter (block) and centimeter (litterbag) scales. However, a substantial amount of variability in microbial communities was left unexplained and must be driven by factors at other spatial scales or more complex spatiotemporal dynamics. We conclude that litter diversity effects are primarily dependent on leaf type, rather than habitat type or identity of surrounding leaves, which can guide the search for mechanisms underlying effects of litter diversity on ecosystem processes.

Notes

Acknowledgments

L. Wu was supported by the Chinese scholarship fund (2006A62008). We thank all the Kent State students and faculty who lent a hand with leaf processing on our “big” harvest days. We also thank Dr. Kurt Smemo, Holden Arboretum, for conducting carbon and nitrogen analyses, Dr. Ksenia Namjesnik-Dejanovic and Kent’s Department of Geology for use of their HPLC, and Dr. Robert Heath for use of his microscope.

References

  1. 1.
    Anderson MJ (2006) Distance-based tests for homogeneity of multivariate dispersions. Biometrics 62:245–253CrossRefPubMedGoogle Scholar
  2. 2.
    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 96:303–313CrossRefGoogle Scholar
  3. 3.
    Berg B, McClaugherty C (2003) Plant litter: decomposition, humus formation, carbon sequestration. Springer, BerlinGoogle Scholar
  4. 4.
    Blackwood CB, Oaks A, Buyer JS (2005) Phylum- and class-specific PCR primers for general microbial community analysis. Appl Environ Microb 71:6193–6198CrossRefGoogle Scholar
  5. 5.
    Boddy L, Hynes J, Bebber DP, Fricker MD (2009) Saprotrophic cord systems: dispersal mechanisms in space and time. Mycoscience 50:9–19CrossRefGoogle Scholar
  6. 6.
    Briones MJI, Ineson P (1996) Decomposition of eucalyptus leaves in litter mixtures. Soil Biol Biochem 28:1381–1388CrossRefGoogle Scholar
  7. 7.
    Cardinale BJ, Nelson K, Palmer MA (2000) Linking species diversity to the functioning of ecosystems: on the importance of environmental context. Oikos 91:175–183CrossRefGoogle Scholar
  8. 8.
    Cox P, Wilkinson SP, Anderson JM (2001) Effects of fungal inocula on the decomposition of lignin and structural polysaccharides in Pinus sylvestris litter. Biol Fertil Soils 33:246–251CrossRefGoogle Scholar
  9. 9.
    Feinstein LM, Sul WJ, Blackwood CB (2009) Assessment of bias associated with incomplete extraction of microbial DNA from soil. Appl Environ Microbiol 75:5428–5433CrossRefPubMedGoogle Scholar
  10. 10.
    Fierer N, Breitbart M, Nulton J, Salamon P, Lozupone C, Jones R, Robeson M, Edwards RA, Felts B, Rayhawk S, Knight R, Rohwer F, Jackson RB (2007) Metagenomic and small-subunit rRNA analyses reveal the genetic diversity of bacteria, archaea, fungi, and viruses in soil. Appl Environ Microb 73:7059–7066CrossRefGoogle Scholar
  11. 11.
    Frey SD, Six J, Elliott ET (2003) Reciprocal transfer of carbon and nitrogen by decomposer fungi at the soil–litter interface. Soil Biol Biochem 35:1001–1004CrossRefGoogle Scholar
  12. 12.
    Fyles JW, Fyles IH (1993) Interaction of Douglas-fir with red alder and salal foliage litter during decomposition. Can J For Res 23:358–361CrossRefGoogle Scholar
  13. 13.
    Gartner TB, Cardon ZG (2004) Decomposition dynamics in mixed-species leaf litter. Oikos 104:230–246CrossRefGoogle Scholar
  14. 14.
    Gessner MO, Chauvet E (1993) Ergosterol-to-biomass conversion factors for aquatic hyphomycetes. Appl Environ Microb 59:502–507Google Scholar
  15. 15.
    Green JL, Bohannan BJM, Whitaker RJ (2008) Microbial biogeography: from taxonomy to traits. Science 320:1039–1043CrossRefPubMedGoogle Scholar
  16. 16.
    Green JL, Holmes AJ, Westoby M, Oliver I, Briscoe D, Dangerfield M, Gillings M, Beattie AJ (2004) Spatial scaling of microbial eukaryote diversity. Nature 432:747–750CrossRefPubMedGoogle Scholar
  17. 17.
    Hättenschwiler S, Tiunov AV, Scheu S (2005) Biodiversity and litter decomposition in terrestrial ecosystems. Annu Rev Ecol Evol S 36:191–218CrossRefGoogle Scholar
  18. 18.
    Hooper DU, Chapin FA, Ewel JJ, Hector A, Inchausti P, Lavorel S, Lawton JH, Lodge DM, Loreau M, Naeem S, Schmid B, Setala H, Symstad AJ, Vandermeer J, Wardle DA (2005) Effects of biodiversity on ecosystem functioning: a consensus of current knowledge. Ecol Monogr 75:3–35CrossRefGoogle Scholar
  19. 19.
    Hui D, Jackson RB (2009) Assessing interactive responses in litter decomposition in mixed species litter. Plant Soil 314:263–271CrossRefGoogle Scholar
  20. 20.
    Koide K, Osono T, Takeda H (2005) Fungal succession and decomposition of Camellia japonica leaf litter. Ecol Res 20:599–609CrossRefGoogle Scholar
  21. 21.
    Lecerf A, Risnoveanu G, Popescu C, Gessner MO, Chauvet E (2007) Decomposition of diverse litter mixtures in streams. Ecology 88:219–227CrossRefPubMedGoogle Scholar
  22. 22.
    Legendre P, Anderson MJ (1999) Distance-based redundancy analysis: testing multispecies responses in multifactorial ecological experiments. Ecol Monogr 69:1–24CrossRefGoogle Scholar
  23. 23.
    Legendre P, Gallagher ED (2001) Ecologically meaningful transformations for ordination of species data. Oecologia 129:271–280CrossRefGoogle Scholar
  24. 24.
    Liu J, Dazzo FB, Glagoleva O, Yu B, Jain AK (2001) CMEIAS: a computer-aided system for the image analysis of bacterial morphotypes in microbial communities. Microb Ecol 41:173–194PubMedGoogle Scholar
  25. 25.
    Loferer-Kröβbacher M, Kilma J, Psenner R (1998) Determination of bacterial cell dry mass by transmission electron microscopy and densitometric image analysis. Appl Environ Microb 64:688–694Google Scholar
  26. 26.
    Loreau M, Naeem S, Inchausti P, Grime JP, Hector A, Hooper DU, Huston MA, Faffaelli D, Schmid B, Tilman D, Wardle DA (2001) Biodiversity and ecosystem functioning: current knowledge and future challenges. Science 294:804–808CrossRefPubMedGoogle Scholar
  27. 27.
    Madritch DM, Cardinale BJ (2007) Impacts of tree species diversity on litter decomposition in northern temperate forests of Wisconsin, USA: a multi-site experiment along a latitudinal gradient. Plant Soil 292:147–159CrossRefGoogle Scholar
  28. 28.
    Martin KJ, Rygiewicz PT (2005) Fungal-specific PCR primers developed for analysis of the ITS region of environmental samples. BMC Microbiol 5:28CrossRefPubMedGoogle Scholar
  29. 29.
    Martiny JBH, Bohannan BJM, Brown JH, Colwell RK, Fuhrman JA, Green JL, Horner-Devine MC, Kane M, Krumins JA, Kuske CR, Morin PJ, Naeem S, Øvreås L, Reysenbach A, Smith VH, Staley JT (2006) Microbial biogeography: putting microorganisms on the map. Nat Rev Microbiol 4:102–112CrossRefPubMedGoogle Scholar
  30. 30.
    McArthur JV, Aho JM, Rader RB (1994) Interspecific leaf interactions during decomposition in aquatic and floodplain ecosystems. J N Am Benthol Soc 13:57–67CrossRefGoogle Scholar
  31. 31.
    McNamara C, Leff L (2004) Bacterial community composition in biofilms on decomposing leaves in a Northeast Ohio stream. J N Am Benthol Soc 23:677–685CrossRefGoogle Scholar
  32. 32.
    McTiernan KB, Ineson P, Coward PA (1997) Respiration and nutrient release from tree leaf litter mixtures. Oikos 78:527–538CrossRefGoogle Scholar
  33. 33.
    Melillo JM, Aber JD, Muratore JF (1982) Nitrogen and lignin control of hardwood leaf litter decomposition dynamics. Ecology 63:621–626CrossRefGoogle Scholar
  34. 34.
    Nannipieri P, Ascher J, Ceccherini MT, Landi L, Pietramellara G, Renella G (2003) Microbial diversity and soil functions. Eur J Soil Sci 54:655–670CrossRefGoogle Scholar
  35. 35.
    Peay KG, Bruns TD, Kennedy PG, Bergemann SE, Garbelotto M (2007) A strong species–area relationship for eukaryotic soil microbes: island size matters for ectomycorrhizal fungi. Ecol Lett 10:470–480CrossRefPubMedGoogle Scholar
  36. 36.
    Poll C, Ingwerson J, Stemmer M, Gerzabek MH, Kandeler E (2006) Mechanisms of solute transport affect abundance and function of soil microorganisms in the detritusphere. Eur J Soil Sci 57:583–595CrossRefGoogle Scholar
  37. 37.
    Porter KS, Feig YS (1980) The use of DAPI for identifying and counting aquatic microflora. Limnol Oceanogr 25:943–948CrossRefGoogle Scholar
  38. 38.
    Salamanca EF, Kaneko N, Katagiri S (1998) Effects of leaf litter mixtures on the decomposition of Quercus serrata and Pinus densiflora using field and laboratory microcosm methods. Ecol Eng 10:53–73CrossRefGoogle Scholar
  39. 39.
    SAS Institute Inc (2004) SAS/Stat user’s guide. SAS OnlineDoc 9.1.2 SAS Institute Inc., Cary, NC, USAGoogle Scholar
  40. 40.
    Schindler MH, Gessner MO (2009) Functional leaf traits and biodiversity effects on litter decomposition in a stream. Ecology 90:1641–1649CrossRefPubMedGoogle Scholar
  41. 41.
    Schwendener CM, Lehman J, de Camargo PB, Luizão RCC, Fernandes ECM (2005) Nitrogen transfer between high- and low-quality leaves on a nutrient-poor Oxisol determined by 15N enrichment. Soil Biol Biochem 37:787–794CrossRefGoogle Scholar
  42. 42.
    Snyder RE, Chesson P (2004) How the spatial scales of dispersal, competition, and environmental heterogeneity interact to affect coexistence. Am Nat 164:633–650CrossRefPubMedGoogle Scholar
  43. 43.
    Tank JL, Webster JR (1998) Interaction of substrate and nutrient availability on wood biofilm processes in streams. Ecology 79:151–162CrossRefGoogle Scholar
  44. 44.
    Tiunov AV (2009) Particle size alters litter diversity effects on decomposition. Soil Biol Biochem 41:176–178CrossRefGoogle Scholar
  45. 45.
    Thies J (2007) Soil microbial community analysis using terminal restriction fragment length polymorphisms. Soil Sci Soc Am J 71:579–591CrossRefGoogle Scholar
  46. 46.
    Toberman H, Freeman C, Evans C, Fenner N, Artz RRE (2008) Summer drought decreases soil fungal diversity and associated phenol oxidase activity in upland Calluna heathland soil. FEMS Microbiol Ecol 66:426–436CrossRefPubMedGoogle Scholar
  47. 47.
    Triantis KA, Mylonas M, Lika K, Vardinoyannis K (2003) A model for the species–area–habitat relationship. J Biogeogr 30:19–27CrossRefGoogle Scholar
  48. 48.
    Wardle DA (2006) The influence of biotic interactions on soil biodiversity. Ecol Lett 9:870–886CrossRefPubMedGoogle Scholar
  49. 49.
    Wardle DA, Nilsson M, Zackrisson O, Gallet C (2003) Determinants of litter mixing effects in a Swedish boreal forest. Soil Biol Biochem 35:827–835CrossRefGoogle Scholar
  50. 50.
    Woodcock S, Curtis TP, Head IM, Lunn M, Sloan WT (2006) Taxa–area relationships for microbes: the unsampled and the unseen. Ecol Lett 9:805–812CrossRefPubMedGoogle Scholar
  51. 51.
    Wu L, Blackwood CB, Leff LG (2009) Effect of single-species and mixed-species leaf leachate on bacterial communities in biofilms. Hydrobiologia 636:65–76CrossRefGoogle Scholar
  52. 52.
    Zak DR, Blackwood CB, Waldrop MP (2006) A molecular dawn for biogeochemistry. Trends Ecol Evol 21:288–295CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2010

Authors and Affiliations

  • Lan Wu
    • 1
    • 2
  • Larry M. Feinstein
    • 2
  • Oscar Valverde-Barrantes
    • 2
  • Mark W. Kershner
    • 2
  • Laura G. Leff
    • 2
  • Christopher B. Blackwood
    • 2
  1. 1.School of Life ScienceNanchang UniversityNanchangChina
  2. 2.Department of Biological SciencesKent State UniversityKentUSA

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