Microbial Ecology

, Volume 63, Issue 4, pp 804–812 | Cite as

Fungal Community Composition in Neotropical Rain Forests: the Influence of Tree Diversity and Precipitation

  • Krista L. McGuire
  • Noah Fierer
  • Carling Bateman
  • Kathleen K. Treseder
  • Benjamin L. Turner
Environmental Microbiology

Abstract

Plant diversity is considered one factor structuring soil fungal communities because the diversity of compounds in leaf litter might determine the extent of resource heterogeneity for decomposer communities. Lowland tropical rain forests have the highest plant diversity per area of any biome. Since fungi are responsible for much of the decomposition occurring in forest soils, understanding the factors that structure fungi in tropical forests may provide valuable insight for predicting changes in global carbon and nitrogen fluxes. To test the role of plant diversity in shaping fungal community structure and function, soil (0–20 cm) and leaf litter (O horizons) were collected from six established 1-ha forest census plots across a natural plant diversity gradient on the Isthmus of Panama. We used 454 pyrosequencing and phospholipid fatty acid analysis to evaluate correlations between microbial community composition, precipitation, soil nutrients, and plant richness. In soil, the number of fungal taxa increased significantly with increasing mean annual precipitation, but not with plant richness. There were no correlations between fungal communities in leaf litter and plant diversity or precipitation, and fungal communities were found to be compositionally distinct between soil and leaf litter. To directly test for effects of plant species richness on fungal diversity and function, we experimentally re-created litter diversity gradients in litter bags with 1, 25, and 50 species of litter. After 6 months, we found a significant effect of litter diversity on decomposition rate between one and 25 species of leaf litter. However, fungal richness did not track plant species richness. Although studies in a broader range of sites is required, these results suggest that precipitation may be a more important factor than plant diversity or soil nutrient status in structuring tropical forest soil fungal communities.

References

  1. 1.
    Hattenschwiler S, Tiunov AV, Scheu S (2005) Biodiversity and litter decomposition in terrestrial ecosystems. Annu Rev Ecol Evol Syst 36:191–218CrossRefGoogle Scholar
  2. 2.
    McGuire KL, Zak DR, Edwards IP, Blackwood CB, Upchurch R (2010) Slowed decomposition is biotically mediated in an ectomycorrhizal, tropical rain forest. Oecologia 164:785–795PubMedCrossRefGoogle Scholar
  3. 3.
    Peay KG, Kennedy PG, Davies SJ, Tan S, Bruns TD (2010) Potential link between plant and fungal distributions in a dipterocarp rainforest: community and phylogenetic structure of tropical ectomycorrhizal fungi across a plant and soil ecotone. New Phytol 185:529–542PubMedCrossRefGoogle Scholar
  4. 4.
    Tedersoo L, Nilsson RH, Abarenkov K, Jairus T, Sadam A, Saar I, Bahram M, Bechem E, Chuyong G, Koljalg U (2010) 454 Pyrosequencing and Sanger sequencing of tropical mycorrhizal fungi provide similar results but reveal substantial methodological biases. New Phytol 188:291–301PubMedCrossRefGoogle Scholar
  5. 5.
    Fierer N, Jackson RB (2006) The diversity and biogeography of soil bacterial communities. Proc Natl Acad Sci U S A 103:626–631PubMedCrossRefGoogle Scholar
  6. 6.
    Watling R (2001) The relationships and possible distributional patterns of boletes in South-East Asia. Mycol Res 105:1440–1448CrossRefGoogle Scholar
  7. 7.
    Lindblad I (2001) Diversity of poroid and some corticoid wood-inhabiting fungi along the rainfall gradient in tropical forests, Costa Rica. J Trop Ecol 17:353–369CrossRefGoogle Scholar
  8. 8.
    Lodge DJ (1997) Factors related to diversity of decomposer fungi in tropical forests. Biodivers Conserv 6:681–688CrossRefGoogle Scholar
  9. 9.
    Buee M, Reich M, Murat C, Morin E, Nilsson RH, Uroz S, Martin F (2009) 454 Pyrosequencing analyses of forest soils reveal an unexpectedly high fungal diversity. New Phytol 184:449–456PubMedCrossRefGoogle Scholar
  10. 10.
    Taylor DL, Herriott IC, Stone KE, McFarland JW, Booth MG, Leigh MB (2010) Structure and resilience of fungal communities in Alaskan boreal forest soils. Can J For Res-Rev Can Rech For 40:1288–1301CrossRefGoogle Scholar
  11. 11.
    O’Brien HE, Parrent JL, Jackson JA, Moncalvo JM, Vilgalys R (2005) Fungal community analysis by large-scale sequencing of environmental samples. Appl Environ Microbiol 71:5544–5550PubMedCrossRefGoogle Scholar
  12. 12.
    Powers JS, Montgomery RA, Adair EC, Brearley FQ, DeWalt SJ, Castanho CT, Chave J, Deinert E, Ganzhorn JU, Gilbert ME, Gonzalez-Iturbe JA, Bunyavejchewin S, Grau HR, Harms KE, Hiremath A, Iriarte-Vivar S, Manzane E, de Oliveira AA, Poorter L, Ramanamanjato JB, Salk C, Varela A, Weiblen GD, Lerdau MT (2009) Decomposition in tropical forests: a pan-tropical study of the effects of litter type, litter placement and mesofaunal exclusion across a precipitation gradient. J Ecol 97:801–811CrossRefGoogle Scholar
  13. 13.
    Gentry AH (1992) Tropical forest biodiversity—distributional patterns and their conservational significance. Oikos 63:19–28CrossRefGoogle Scholar
  14. 14.
    Valencia RH, Balslev H, Paz H, Mino CG (1994) High tree alpha-diversity in Amazonian Ecuador. Biodivers Conserv 3:21–28CrossRefGoogle Scholar
  15. 15.
    Aerts R (1997) Climate, leaf litter chemistry and leaf litter decomposition in terrestrial ecosystems: a triangular relationship. Oikos 79:439–449CrossRefGoogle Scholar
  16. 16.
    Couteaux MM, Bottner P, Berg B (1995) Litter decomposition, climate and litter quality. Trends Ecol Evol 10:63–66CrossRefGoogle Scholar
  17. 17.
    Perez-Harguindeguy N, Diaz S, Cornelissen JHC, Vendramini F, Cabido M, Castellanos A (2000) Chemistry and toughness predict leaf litter decomposition rates over a wide spectrum of functional types and taxa in central Argentina. Plant Soil 218:21–30CrossRefGoogle Scholar
  18. 18.
    Sariyildiz T, Anderson JM (2002) Interactions between litter quality, decomposition and soil fertility: a laboratory study. Soil Biol Biochem 35:391–399CrossRefGoogle Scholar
  19. 19.
    Berg B, McClaugherty C (2003) Plant litter: decomposition, humus formation, carbon sequestration. Springer, BerlinGoogle Scholar
  20. 20.
    McGuire KL, Bent E, Borneman J, Majumder A, Allison SD, Treseder KK (2010) Functional diversity in resource use by fungi. Ecology. doi:10.1890/09-0654
  21. 21.
    Hanson CA, Allison SD, Bradford MA, Wallenstein MD, Treseder KK (2008) Fungal taxa target different carbon sources in forest soil. Ecosystems 11:1157–1167CrossRefGoogle Scholar
  22. 22.
    Boddy L (1999) Saprotrophic cord-forming fungi: meeting the challenge of heterogeneous environments. Mycologia 91:13–32CrossRefGoogle Scholar
  23. 23.
    Dickie IA, Xu B, Koide RT (2002) Vertical niche differentiation of ectomycorrhizal hyphae in soil as shown by T-RFLP analysis. New Phytol 156:527–535CrossRefGoogle Scholar
  24. 24.
    Genney DR, Anderson IC, Alexander IJ (2006) Fine-scale distribution of pine ectomycorrhizas and their extramatrical mycelium. New Phytol 170:381–390PubMedCrossRefGoogle Scholar
  25. 25.
    Hooper DU, Chapin FS, 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
  26. 26.
    Jonsson LM, Nilsson MC, Wardle DA, Zackrisson O (2001) Context dependent effects of ectomycorrhizal species richness on tree seedling productivity. Oikos 93:353–364CrossRefGoogle Scholar
  27. 27.
    Carney KM, Matson PA (2006) The influence of tropical plant diversity and composition on soil microbial communities. Microb Ecol 52:226–238PubMedCrossRefGoogle Scholar
  28. 28.
    Waldrop MP, Balser TC, Firestone MK (2000) Linking microbial community composition to function in a tropical soil. Soil Biol Biochem 32:1837–1846CrossRefGoogle Scholar
  29. 29.
    Ushio M, Wagai R, Balser TC, Litayama L (2008) Variations in the soil microbial community composition of a tropical montane forest ecosystem: does tree species matter? Soil Biol Biochem 40:2699–2702CrossRefGoogle Scholar
  30. 30.
    Pyke CR, Condit R, Aguilar S, Lao S (2001) Floristic composition across a climatic gradient in a neotropical lowland forest. J Veg Sci 12:553–566CrossRefGoogle Scholar
  31. 31.
    Turner BL, Romero TE (2009) Short-term changes in extractable inorganic nutrients during storage of tropical rain forest soils. Soil Sci Soc Am J 73:1972–1979CrossRefGoogle Scholar
  32. 32.
    Leigh EG, Loo de Lao S, Condit R, Hubbell SP, Foster RB, Pérez R (2004) Barro Colorado Island forest dynamics plot, Panama. In: Losos EC, Leigh EG (eds) Tropical forest diversity and dynamism: findings from a large-scale plot network. The University of Chicago Press, Chicago, pp 451–463Google Scholar
  33. 33.
    Dieter D, Elsenbeer H, Turner BL (2010) Phosphorus fractionation in lowland tropical rainforest soils in central Panama. Catena 82:118–125CrossRefGoogle Scholar
  34. 34.
    Feinstein LM, Sul WJ, Blackwood CB (2009) Assessment of bias associated with incomplete extraction of microbial DNA from soil. Appl Environ Microbiol 75:5428–5433PubMedCrossRefGoogle Scholar
  35. 35.
    Borneman J, Hartin RJ (2000) PCR primers that amplify fungal rRNA genes from environmental samples. Appl Environ Microbiol 66:4356–4360PubMedCrossRefGoogle Scholar
  36. 36.
    Fierer N, Hamady M, Lauber CL, Knight R (2008) The influence of sex, handedness, and washing on the diversity of hand surface bacteria. Proc Natl Acad Sci U S A 105:17994–17999PubMedCrossRefGoogle Scholar
  37. 37.
    Lauber CL, Hamady M, Knight R, Fierer N (2009) Pyrosequencing-based assessment of soil pH as a predictor of soil bacterial community structure at the continental scale. Appl Environ Microbiol 75:5111–5120PubMedCrossRefGoogle Scholar
  38. 38.
    Hamady M, Walker JJ, Harris JK, Gold NJ, Knight R (2008) Error-correcting barcoded primers for pyrosequencing hundreds of samples in multiplex. Nat Methods 5:235–237PubMedCrossRefGoogle Scholar
  39. 39.
    Rousk J, Baath E, Brookes PC, Lauber CL, Lozupone C, Caporaso JG, Knight R, Fierer N (2010) Soil bacterial and fungal communities across a pH gradient in an arable soil. ISME J 4:1340–1351PubMedCrossRefGoogle Scholar
  40. 40.
    Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Tumbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336PubMedCrossRefGoogle Scholar
  41. 41.
    Allison SD, McGuire KL, Treseder KK (2010) Resistance of microbial and soil properties to warming treatment seven years after boreal fire. Soil Biol Biochem 42:1872–1878CrossRefGoogle Scholar
  42. 42.
    Price MN, Dehal PS, Arkin AP (2009) FastTree: computing large minimum evolution trees with profiles instead of a distance matrix. Mol Biol Evol 26:1641–1650PubMedCrossRefGoogle Scholar
  43. 43.
    Pruesse E, Quast C, Knittel K, Fuchs BM, Ludwig WG, Peplies J, Glockner FO (2007) SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res 35:7188–7196PubMedCrossRefGoogle Scholar
  44. 44.
    White DC, Stair JO, Ringelberg DB (1997) Quantitative comparisons of in situ microbial biodiversity by signature biomarker analysis. J Ind Microbiol 17:185–196Google Scholar
  45. 45.
    Bligh EG, Dyer WJ (1954) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37:911–917CrossRefGoogle Scholar
  46. 46.
    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
  47. 47.
    van Diepen LTA, Lilleskov EA, Pregitzer KS, Miller RM (2007) Decline of arbuscular mycorrhizal fungi in northern hardwood forests exposed to chronic nitrogen additions. New Phytol 176:175–183PubMedCrossRefGoogle Scholar
  48. 48.
    Olsson PA (1999) Signature fatty acids provide tools for determination of the distribution and interactions of mycorrhizal fungi in soil. FEMS Microbiol Ecol 29:303–310CrossRefGoogle Scholar
  49. 49.
    Gartner TB, Cardon ZG (2004) Decomposition dynamics in mixed-species leaf litter. Oikos 104:230–246CrossRefGoogle Scholar
  50. 50.
    Chapman SK, Newman GS (2010) Biodiversity at the plant–soil interface: microbial abundance and community structure respond to litter mixing. Oecologia 162:763–769PubMedCrossRefGoogle Scholar
  51. 51.
    Andren O, Balandreau J (1999) Biodiversity and soil functioning—from black box to can of worms? Appl Soil Ecol 13:105–108CrossRefGoogle Scholar
  52. 52.
    Zak DR, Holmes WE, White DC, Peacock AD, Tilman D (2003) Plant diversity, soil microbial communities, and ecosystem function: are there any links? Ecology 84:2042–2050CrossRefGoogle Scholar
  53. 53.
    Bell T, Newman JA, Silverman BW, Turner SL, Lilley AK (2005) The contribution of species richness and composition to bacterial services. Nature 436:1157–1160PubMedCrossRefGoogle Scholar
  54. 54.
    Setala H, McLean MA (2004) Decomposition rate of organic substrates in relation to the species diversity of soil saprophytic fungi. Oecologia 139:98–107PubMedCrossRefGoogle Scholar
  55. 55.
    Wohl DL, Arora S, Gladstone JR (2004) Functional redundancy supports biodiversity and ecosystem function in a closed and constant environment. Ecology 85:1534–1540CrossRefGoogle Scholar
  56. 56.
    Meier CL, Bowman WD (2008) Links between plant litter chemistry, species diversity, and below-ground ecosystem function. Proc Natl Acad Sci U S A 105:19780–19785PubMedCrossRefGoogle Scholar
  57. 57.
    Hawkes CV, Kivlin SN, Rocca JD, Huguet V, Thomsen MA, Suttle KB (2010) Fungal community responses to precipitation. Glob Chang Biol 17:1637–1645CrossRefGoogle Scholar
  58. 58.
    Castro HF, Classen AT, Austin EE, Norby RJ, Schadt CW (2010) Soil microbial community responses to multiple experimental climate change drivers. Appl Environ Microbiol 76:999–1007PubMedCrossRefGoogle Scholar
  59. 59.
    Baath E, Soderstrom B (1982) Seasonal and spatial variation in fungal biomass in a forest soil. Soil Biol Biochem 14:353–358CrossRefGoogle Scholar
  60. 60.
    Trumbore S (2000) Age of soil organic matter and soil respiration: radiocarbon constraints on belowground C dynamics. Ecol Appl 10:399–411CrossRefGoogle Scholar
  61. 61.
    Lindahl BD, Ihrmark K, Boberg J, Trumbore SE, Hogberg P, Stenlid J, Finlay RD (2007) Spatial separation of litter decomposition and mycorrhizal nitrogen uptake in a boreal forest. New Phytol 173:611–620PubMedCrossRefGoogle Scholar
  62. 62.
    Fierer N, Schimel JP, Holden PA (2003) Variations in microbial community composition through two soil depth profiles. Soil Biol Biochem 35:167–176CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2011

Authors and Affiliations

  • Krista L. McGuire
    • 1
  • Noah Fierer
    • 2
  • Carling Bateman
    • 1
  • Kathleen K. Treseder
    • 3
  • Benjamin L. Turner
    • 4
  1. 1.Barnard CollegeColumbia UniversityNew YorkUSA
  2. 2.University of ColoradoBoulderUSA
  3. 3.University of CaliforniaIrvineUSA
  4. 4.Smithsonian Tropical Research InstituteBalboaRepublic of Panama

Personalised recommendations