Abstract
Soil fungal communities have high local diversity and turnover, but the relative contribution of environmental and regional drivers to those patterns remains poorly understood. Local factors that contribute to fungal diversity include soil properties and the plant community, but there is also evidence for regional dispersal limitation in some fungal communities. We used different plant communities with different soil conditions and experimental manipulations of both vegetation and dispersal to distinguish among these factors. Specifically, we compared native shrublands with former native shrublands that had been disturbed or converted to pasture, resulting in soils progressively more enriched in carbon and nutrients. We tested the role of vegetation via active removal, and we manipulated dispersal by adding living soil inoculum from undisturbed native sites. Soil fungi were tracked for 3 years, with samples taken at ten time points from June 2006 to June 2009. We found that soil fungal abundance, richness, and community composition responded primarily to soil properties, which in this case were a legacy of plant community degradation. In contrast, dispersal had no effect on soil fungi. Temporal variation in soil fungi was partly related to drought status, yet it was much broader in native sites compared to pastures, suggesting some buffering due to the increased soil resources in the pasture sites. The persistence of soil fungal communities over 3 years in this study suggests that soil properties can act as a strong local environmental filter. Largely persistent soil fungal communities also indicate the potential for strong biotic resistance and soil legacies, which presents a challenge for both the prediction of how fungi respond to environmental change and our ability to manipulate fungi in efforts such as ecosystem restoration.
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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 Microbiol 73(21):7059–7066. doi:10.1128/aem.00358-07
O'Brien HE, Parrent JL, Jackson JA, Moncalvo J-M, Vilgalys R (2005) Fungal community analysis by large-scale sequencing of environmental samples. Appl Environ Microbiol 71(9):5544–5550. doi:10.1128/aem.71.9.5544-5550.2005
Porras-Alfaro A, Herrera J, Natvig DO, Lipinski K, Sinsabaugh RL (2011) Diversity and distribution of soil fungal communities in a semiarid grassland. Mycologia 103(1):10–21. doi:10.3852/09-297
Blackwood CB, Waldrop MP, Zak DR, Sinsabaugh RL (2007) Molecular analysis of fungal communities and laccase genes in decomposing litter reveals differences among forest types but no impact of nitrogen deposition. Environ Microbiol 9:1306–1316
Waldrop MP, Zak DR, Blackwood CB, Curtis CD, Tilman D (2006) Resource availability controls fungal diversity across a plant diversity gradient. Ecol Lett 9(10):1127–1135
Cottenie K (2005) Integrating environmental and spatial processes in ecological community dynamics. Ecol Lett 8(11):1175–1182. doi:10.1111/j.1461-0248.2005.00820.x
de Graaff M-A, Classen AT, Castro HF, Schadt CW (2010) Labile soil carbon inputs mediate the soil microbial community composition and plant residue decomposition rates. New Phytol 188(4):1055–1064. doi:10.1111/j.1469-8137.2010.03427.x
van der Putten WH, Klironomos JN, Wardle DA (2007) Microbial ecology of biological invasions. ISME J 1(1):28–37
Belnap J, Phillips SL (2001) Soil biota in an ungrazed grassland: response to annual grass (Bromus tectorum) invasion. Ecol Appl 11(5):1261–1275
Broz AK, Manter DK, Vivanco JM (2007) Soil fungal abundance and diversity: another victim of the invasive plant Centaurea maculosa. ISME J 1(8):763–765
Cappuccino N, Arnason JT (2006) Novel chemistry of invasive exotic plants. Biol Lett 2(2):189–193. doi:10.1098/rsbl.2005.0433
Peñuelas J, Sardans J, Llusià J, Owen SM, Carnicer J, Giambelluca TW, Rezende EL, Waite M, Niinemets U (2010) Faster returns on 'leaf economics' and different biogeochemical niche in invasive compared with native plant species. Glob Chang Biol 16(8):2171–2185. doi:10.1111/j.1365-2486.2009.02054.x
McGuire K, Fierer N, Bateman C, Treseder K, Turner B (2011) Fungal community composition in neotropical rain forests: the influence of tree diversity and precipitation. Microb Ecol 63(4):804–812. doi:10.1007/s00248-011-9973-x
Lauber CL, Strickland MS, Bradford MA, Fierer N (2008) The influence of soil properties on the structure of bacterial and fungal communities across land-use types. Soil Biol Biochem 40(9):2407–2415. doi:10.1016/j.soilbio.2008.05.021
Arenz BE, Blanchette RA (2011) Distribution and abundance of soil fungi in Antarctica at sites on the Peninsula, Ross Sea Region and McMurdo Dry Valleys. Soil Biol Biochem 43(2):308–315. doi:10.1016/j.soilbio.2010.10.016
Talbot JM, Bruns TD, Smith DP, Branco S, Glassman SI, Erlandson S, Vilgalys R, Peay KG (2013) Independent roles of ectomycorrhizal and saprotrophic communities in soil organic matter decomposition. Soil Biol Biochem 57(0):282–291. doi:10.1016/j.soilbio.2012.10.004
Hanson C, Allison S, Bradford M, Wallenstein M, Treseder K (2008) Fungal taxa target different carbon sources in forest soil. Ecosystems 11(7):1157–1167. doi:10.1007/s10021-008-9186-4
McGuire KL, Bent E, Borneman J, Majumder A, Allison SD, Treseder KK (2010) Functional diversity in resource use by fungi. Ecology 91(8):2324–2332. doi:10.1890/09-0654.1
Edwards IP, Zak DR, Kellner H, Eisenlord SD, Pregitzer KS (2011) Simulated atmospheric N deposition alters fungal community composition and suppresses ligninolytic gene expression in a northern hardwood forest. PLoS One 6(6):e20421
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(10):1340–1351
Ives AR, Gross K, Klug JL (1999) Stability and variability in competitive communities. Science 286(5439):542–544. doi:10.1126/science.286.5439.542
Hawkes CV, Kivlin SN, Rocca JD, Huguet V, Thomsen MA, Suttle KB (2011) Fungal community responses to precipitation. Glob Chang Biol 17(4):1637–1645. doi:10.1111/j.1365-2486.2010.02327.x
Kennedy N, Brodie E, Connolly J, Clipson N (2006) Seasonal influences on fungal community structure in unimproved and improved upland grassland soils. Can J Microbiol 52(7):689–694. doi:10.1139/w06-015
Cregger MA, Schadt CW, McDowell NG, Pockman WT, Classen AT (2012) Response of the soil microbial community to changes in precipitation in a semiarid ecosystem. Appl Environ Microbiol 78(24):8587–8594. doi:10.1128/aem.02050-12
Schadt CW, Martin AP, Lipson DA, Schmidt SK (2003) Seasonal dynamics of previously unknown fungal lineages in tundra soils. Science 301(5638):1359–1361. doi:10.1126/science.1086940
Hanson CA, Fuhrman JA, Horner-Devine MC, Martiny JBH (2012) Beyond biogeographic patterns: processes shaping the microbial landscape. Nat Rev Micro 10(7):497–506
Fierer N, Liu Z, Rodríguez-Hernández M, Knight R, Henn M, Hernandez MT (2008) Short-term temporal variability in airborne bacterial and fungal populations. Appl Environ Microbiol 74(1):200–207. doi:10.1128/aem.01467-07
Fröhlich-Nowoisky J, Pickersgill DA, Després VR, Pöschl U (2009) High diversity of fungi in air particulate matter. Proc Natl Acad Sci U S A 106(31):12814–12819. doi:10.1073/pnas.0811003106
Brown JKM, HovmÃller MS (2002) Aerial dispersal of pathogens on the global and continental scales and its impact on plant disease. Science 297(5581):537–541. doi:10.1126/science.1072678
Roper M, Pepper RE, Brenner MP, Pringle A (2008) Explosively launched spores of ascomycete fungi have drag-minimizing shapes. Proc Natl Acad Sci U S A 105(52):20583–20588. doi:10.1073/pnas.0805017105
Peay KG, Schubert MG, Nguyen NH, Bruns TD (2012) Measuring ectomycorrhizal fungal dispersal: macroecological patterns driven by microscopic propagules. Mol Ecol 21(16):4122–4136. doi:10.1111/j.1365-294X.2012.05666.x
Armstrong RA (1976) Fugitive species: experiments with fungi and some theoretical considerations. Ecology 57(5):953–963. doi:10.2307/1941060
Kennedy PG, Higgins LM, Rogers RH, Weber MG (2011) Colonization-competition tradeoffs as a mechanism driving successional dynamics in ectomycorrhizal fungal communities. PLoS One 6(9):e25126. doi:10.1371/journal.pone.0025126
Bahram M, Kõljalg U, Courty P-E, Diédhiou AG, Kjøller R, Põlme S, Ryberg M, Veldre V, Tedersoo L (2013) The distance decay of similarity in communities of ectomycorrhizal fungi in different ecosystems and scales. J Ecol 101(5):1335–1344. doi:10.1111/1365-2745.12120
Menges E, Hawkes C (1998) Interactive effects of fire and microhabitat on plants of Florida scrub. Ecol Appl 8:935–946
Abrahamson W, Johnson A, Layne J, Peroni P (1984) Vegetation of the Archbold Biological Station, Florida: an example of the southern Lake Wales Ridge. Fla Scientist 47:209–250
Menges ES, Craddock A, Salo J, Zinthefer R, Weekley CW (2008) Gap ecology in Florida scrub: species occurrence, diversity and gap properties. J Veg Sci 19(4):503–514. doi:10.3170/2008-8-18399
Hawkes CV, Flechtner VR (2002) Biological soil crusts in a xeric Florida shrubland: composition, abundance, and spatial heterogeneity of crusts with different disturbance histories. Microb Ecol 43:1–12
Carter LJ, Lewis D, Crockett L, Vega J (1989) Soil survey of Highlands County. Florida, USDA, Soil Conservation Service, Gainesville, FL
Hamman ST, Hawkes CV (2013) Biogeochemical and microbial legacies of non-native grasses can affect restoration success. Restor Ecol 21:58–66. doi:10.1111/j.1526-100X.2011.00856.x
Petru M, Menges ES (2004) Shifting sands in Florida scrub gaps and roadsides: dynamic microsites for herbs. Am Midl Nat 151(1):101–113
Brundrett M, Melville L, Peterson L (1994) Practical methods in mycorrhiza research. Mycologue Publications, Guelph, Canada
Griffiths RI, Whiteley AS, O'Donnell AG, Bailey MJ (2000) Rapid method for coextraction of DNA and RNA from natural environments for analysis of ribosomal DNA- and rRNA-based microbial community composition. Appl Environ Microbiol 66:5488–5491
Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for Basidiomycetes—application to the identification of mycorrhizae and rusts. Mol Ecol 2:113–118
White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis N, Gelfand D, Sninsky J, White T (eds) PCR—protocols and applications—a laboratory manual. Academic, New York, pp 315–322
Hausmann NT, Hawkes CV (2009) Plant neighborhood control of arbuscular mycorrhizal community composition. New Phytol 183(4):1188–1200. doi:10.1111/j.1469-8137.2009.02882.x
Nilsson RH, Abarenkov K, Veldre V, Nylinder S, De Wit P, Brosche S, Alfredsson JF, Ryberg M, Kristiansson E (2010) An open source chimera checker for the fungal ITS region. Mol Ecol Resour 10:1076–1081
Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glöckner FO (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41(D1):D590–D596. doi:10.1093/nar/gks1219
Liu K, Raghavan S, Nelesen S, Linder CR, Warnow T (2009) Rapid and accurate large-scale coestimation of sequence alignments and phylogenetic trees. Science 324(5934):1561–1564
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410
Drummond A, Ashton B, Cheung M, Heled J, Kearse M, Moir R, Stones-Havas S, Thierer T, Wilson A (2009) Geneious v4.8, Available from ≤http://www.geneious.com/>
Dickie I, FitzJohn R (2007) Using terminal restriction fragment length polymorphism (T-RFLP) to identify mycorrhizal fungi: a methods review. Mycorrhiza 17(4):259–270
Fitzjohn RG, Dickie IA (2007) TRAMPR: an R package for analysis and matching of terminal-restriction fragment length polymorphism (TRFLP) profiles. Mol Ecol Notes 7(4):583–587
Shaw RG, Mitchell-Olds T (1993) ANOVA for unbalanced data: an overview. Ecology 74(6):1638–1645. doi:10.2307/1939922
Mielke PW Jr, Berry KJ (2001) Permutation methods: a distance function approach. Springer series in statistics. Springer, New York
Clarke KR (1993) Non-parametric multivariate analyses of changes in community structure. Aust J Ecol 18(1):117–143. doi:10.1111/j.1442-9993.1993.tb00438.x
Borcard D, Legendre P, Drapeau P (1992) Partialling out the spatial component of ecological variation. Ecology 73(3):1045–1055. doi:10.2307/1940179
Legendre P, Borcard D, Peres-Neto PR (2005) Analyzing beta diversity: partitioning the spatial variation of community composition data. Ecol Monogr 75(4):435–450. doi:10.1890/05-0549
IBM Corp. (2010) IBM SPSS Statistics for Windows, Version 19.0. IBM Corp., Armonk, NY
McCune B, Mefford MJ (2011) PC-ORD v. 6.12. Multivariate analysis of ecological data. MjM Software, Gleneden Beach, OR, US
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(15):5111–5120. doi:10.1128/aem.00335-09
Lekberg Y, Gibbons SM, Rosendahl S, Ramsey PW (2013) Severe plant invasions can increase mycorrhizal fungal abundance and diversity. ISME J. doi:http://www.nature.com/ismej/journal/vaop/ncurrent/suppinfo/ismej201341s1.html
Mack MC, D'Antonio CM (2003) Exotic grasses alter controls over soil nitrogen dynamics in a Hawaiian woodland. Ecol Appl 13(1):154–166
Evans RD, Rimer R, Sperry L, Belnap J (2001) Exotic plant invasion alters nitrogen dynamics in an arid grassland. Ecol Appl 11(5):1301–1310. doi:10.1890/1051-0761(2001)011[1301:EPIAND]2.0.CO;2
Kulmatiski A, Beard KH (2008) Decoupling plant-growth from land-use legacies in soil microbial communities. Soil Biol Biochem 40(5):1059–1068. doi:10.1016/j.soilbio.2007.11.020
Weekley CW, Gagnon D, Menges ES, Quintana-Ascencio PF, Saha S (2007) Variation in soil moisture in relation to rainfall, vegetation, gaps, and time-since-fire in Florida scrub. Ecoscience 14(3):377–386. doi:10.2980/1195-6860(2007)14[377:vismir]2.0.co;2
McCann KS (2000) The diversity-stability debate. Nature 405(6783):228–233
Weekley CW, Menges ES (2003) Species and vegetation responses to prescribed fire in a long-unburned, endemic-rich Lake Wales Ridge scrub. J Torrey Bot Soc 130(4):265–282
Klein D, McLendon T, Paschke MW, Redente EF (1995) Saprophytic fungal-bacterial biomass variations in successional communities of a semi-arid steppe ecosystem. Biol Fertil Soils 19(2–3):253–256. doi:10.1007/bf00336168
Ohtonen R, Fritze H, Pennanen T, Jumpponen A, Trappe J (1999) Ecosystem properties and microbial community changes in primary succession on a glacier forefront. Oecologia 119(2):239–246. doi:10.1007/s004420050782
Parker SS, Seabloom EW, Schimel JP (2012) Grassland community composition drives small-scale spatial patterns in soil properties and processes. Geoderma 170(0):269–279. doi:10.1016/j.geoderma.2011.11.018
Evans S, Wallenstein M (2012) Soil microbial community response to drying and rewetting stress: does historical precipitation regime matter? Biogeochemistry 109(1–3):101–116. doi:10.1007/s10533-011-9638-3
McLauchlan K (2006) The nature and longevity of agricultural impacts on soil carbon and nutrients: a review. Ecosystems 9(8):1364–1382. doi:10.1007/s10021-005-0135-1
Marchante E, Kjøller A, Struwe S, Freitas H (2009) Soil recovery after removal of the N2-fixing invasive Acacia longifolia: consequences for ecosystem restoration. Biol Invasions 11(4):813–823. doi:10.1007/s10530-008-9295-1
Elgersma K, Ehrenfeld J, Yu S, Vor T (2011) Legacy effects overwhelm the short-term effects of exotic plant invasion and restoration on soil microbial community structure, enzyme activities, and nitrogen cycling. Oecologia 167(3):733–745. doi:10.1007/s00442-011-2022-0
Grman E, Suding KN (2010) Within-year soil legacies contribute to strong priority effects of exotics on native California grassland communities. Restor Ecol 18(5):664–670. doi:10.1111/j.1526-100X.2008.00497.x
Bever JD (1994) Feedback between plants and their soil communities in an old field community. Ecology 75(7):1965–1977
Suding KN, Gross KL, Houseman GR (2004) Alternative states and positive feedbacks in restoration ecology. Trends Ecol Evol 19(1):46–53
Meredith DS (1973) Significance of spore release and dispersal mechanisms in plant disease epidemiology. Annu Rev Phytopathol 11(1):313–342
Lekberg Y, Koide RT, Rohr JR, Aldrich-Wolfe L, Morton JB (2007) Role of niche restrictions and dispersal in the composition of arbuscular mycorrhizal fungal communities. J Ecol 95(1):95–105
Kardol P, Bezemer TM, Van Der Putten WH (2009) Soil organism and plant introductions in restoration of species-rich grassland communities. Restor Ecol 17(2):258–269. doi:10.1111/j.1526-100X.2007.00351.x
Acknowledgments
We are grateful to E. Menges, H. Swain, R. Boughton, K. Main, S. Smith, and the staff of Archbold Biological Station for access to the sites and local support. Assistance with fieldwork and lab analyses was provided by E. Brault, S. Hamman, N. Johnson, S. Kivlin, and other members of the Hawkes Lab. Previous versions of this manuscript were significantly improved by comments from S. Kivlin, E. Menges, B. Sikes, and four anonymous reviewers. Support for the project was provided by the National Research Initiative of the USDA Cooperative State Research, Education, and Extension Service grant number 2006-35101-16575 to CVH.
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Glinka, C., Hawkes, C.V. Environmental Controls on Fungal Community Composition and Abundance Over 3 Years in Native and Degraded Shrublands. Microb Ecol 68, 807–817 (2014). https://doi.org/10.1007/s00248-014-0443-0
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DOI: https://doi.org/10.1007/s00248-014-0443-0