Abstract
To assess soil microbial response to global warming in cool temperate semi-natural grassland, we conducted an in situ warming experiment in grassland located in the mountains of central Japan. Five pairs of plots (control and warmed) of Zoysia japonica were established. For each pair of plots, one was warmed by ca. 2 °C using infrared heaters during the growing seasons of 2009–2011. Above-ground biomass of Z. japonica was estimated using the modified point-frame method. Soil organic matter contents, soil total carbon and nitrogen contents, as well as inorganic nitrogen (ammonium and nitrate) contents were determined from soil samples. Total phospholipid fatty acid (PLFA) contents and PLFA compositions were determined and used as indices for total microbial biomass and community structure, respectively. Analyses showed that the warming increased the above-ground biomass of Z. japonica significantly. Soil organic matter and soil total nitrogen contents were significantly decreased, while soil ammonium content was significantly increased in the warmed plots. Soil microbial biomass (especially fungal biomass) was lower in the warmed plots, probably reflecting higher temperature, lower soil water content, and/or depletion in available nutrients. The significant decrease in fungal biomass, in combination with our PLFA composition data, suggests that the soil microbial community structure shifted from a fungal-dominated to a bacteria-dominated one, causing changes in community-level physiological activity.
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References
Bastida F, Moreno JL, Hernández T, García C (2006) Microbiological activity in a soil 15 years after its devegetation. Soil Biol Biochem 38:2503–2507
Belay-Tedla A, Zhou X, Su B, Wan S, Luo Y (2009) Labile, recalcitrant, and microbial carbon and nitrogen pools of a tallgrass prairie soil in the US Great Plains subjected to experimental warming and clipping. Soil Biol Biochem 41:110–116
Bell MJ, Eckard RJ, Harrison MT, Neal JS, Cullen BR (2013) Effect of warming on the productivity of perennial ryegrass and kikuyu pastures in south-eastern Australia. Crop Pasture Sci 64:61–70
Biasi C, Meyer H, Rusalimova O, Hämmerle R, Kaiser C, Baranyi C, Daims H, Lashchinsky N, Barsukov P, Richter A (2008) Initial effects of experimental warming on carbon exchange rates, plant growth and microbial dynamics of a lichen-rich dwarf shrub tundra in Siberia. Plant Soil 307:191–205
Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37:911–917
Cataldo DA, Maroon M, Schrader LE, Youngs VL (1975) Rapid colorimetric determination of nitrate in plant tissue by nitration of salicylic acid. Commun Soil Sci Plant Anal 6:71–80
Cornelissen JH, van Bodegom PM, Aerts R, Callaghan TV, van Logtestijn RS, Alatalo J, Chapin FS, Gerdol R, Gudmundsson J, Gwynn-Jones D, Hartley AE, Hik DS, Hofgaard A, Jónsdóttir IS, Karlsson S, Klein JA, Laundre J, Magnusson B, Michelsen A, Molau U, Onipchenko VG, Quested HM, Sandvik SM, Schmidt IK, Shaver GR, Solheim B, Soudzilovskaia NA, Stenström A, Tolvanen A, Totland Ø, Wada N, Welker JM, Zhao X (2007) Global negative vegetation feedback to climate warming responses of leaf litter decomposition rates in cold biomes. Ecol Lett 10:619–627
Cox PM, Betts RA, Jones CD, Spall SA, Totterdell IJ (2000) Acceleration of global warming due to carbon-cycle feedbacks in a coupled climate model. Nature 408:184–187
Dhital D, Yashiro Y, Ohtsuka T, Noda H, Shizu Y, Koizumi H (2010) Carbon dynamics and budget in a Zoysia japonica grassland, central Japan. J Plant Res 123:519–530
Federle TW (1986) Microbial distribution in soil––new techniques. In: Gantar M, Megusar F (eds) Perspectives in microbial ecology. Slovene Society for Microbiology, Ljubljana, pp 493–498
Feng X, Simpson MJ (2009) Temperature and substrate controls on microbial phospholipid fatty acid composition during incubation of grassland soils contrasting in organic matter quality. Soil Biol Biochem 41:804–812
Fitter AH, Self GK, Brown TK, Bogie DS, Graves JD, Benham D, Ineson P (1999) Root production and turnover in an upland grassland subjected to artificial soil warming respond to radiation flux and nutrients, not temperature. Oecologia 120:575–581
Frostegård A, Tunlid A, Bååth E (1991) Microbial biomass measured as total lipid phosphate in soils of different organic content. J Microbiol Method 14:151–163
Frostegård A, Tunlid A, Bååth E (1993) Phospholipid fatty acid composition, biomass, and activity of microbial communities from two soil types experimentally exposed to different heavy metals. Appl Environ Microbiol 59:3605–3617
Fujii S (1999) A comparative analysis of habitat types of locally endangered plants in Japan. Jpn J Conserv Ecol 4:57–69 (in Japanese with English Abstract)
Hannam KD, Quideau SA, Kishchuk BE (2006) Forest floor microbial communities in relation to stand composition and timber harvesting in northern Alberta. Soil Biol Biochem 38:2565–2575
Hobbie SE (1996) Temperature and plant species control over litter decomposition in Alaskan tundra. Ecol Monogr 66:503–522
Hobbie SE, Chapin FS III (1998) The response of tundra plant biomass, aboveground production, nitrogen, and CO2 flux to experimental warming. Ecology 79:1526–1544
Hodge A, Robinson D, Fitter A (2000) Are microorganisms more effective than plants at competing for nitrogen? Trends Plant Sci 5:304–308
Hunt JE, Kelliher FM, McSeveny TM, Ross DJ, Whitehead D (2004) Long-term carbon exchange in a sparse, seasonally dry tussock grassland. Glob Chang Biol 10:1785–1800
Huseo S, Garcia C, Hernandez T (2012) Severe drought conditions modify the microbial community structure, size and activity in amended and unamended soils. Soil Biol Biochem 50:167–173
Inoue T, Koizumi H (2012) Effects of environmental factors upon variation in soil respiration of a Zoysia japonica grassland, central Japan. Ecol Res 27:445–452
Inoue M, Takahashi Y (2009) New movement in activities for conservation and restoration of semi-natural grassland. Landsc Ecol Manag 14:1–4 (in Japanese)
Intergovernmental Panel on Climate Change (2014) Climate change 2013: the physical science basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge
Japan Statistical Yearbook (2013) Statistics Bureau, Ministry of Internal Affairs and Communications, Japan (in Japanese)
Jenkinson DS, Ladd JN (1981) Microbial biomass in soil: measurement and turnover. In: Paul DA, Ladd JN (eds) Soil biochemistry, vol 5. Marcel Dekker, New York, pp 415–471
Joergensen RG, Brookes PC, Jenkinson DS (1990) Survival of the soil microbial biomass at elevated temperature. Soil Biol Biochem 22:1129–1136
Kaneko S, Ohta Y, Shirakawa K, Inoue M, Tsutsumi M, Watanabe S, Sakuma T, Takahashi Y (2009) An attempt to evaluate the habitat type of endangered plant species in the Chugoku region, western Japan. Jpn J Conserv Ecol 14:125–129 (in Japanese with English Abstract)
Kaneko K, Tanikawa M, Hasegawa M (2012) Difference of vegetation by mowing frequency in semi-natural grasslands in the Yata district of Shiroi-city, Chiba Prefecture. Landsc Ecol Manag 16:71–77 (in Japanese with English Abstract)
Kaye JP, Hart SC (1997) Competition for nitrogen between plants and soil microorganisms. Trends Ecol Evol 12:139–143
Luo Y, Wan S, Hui D, Wallace LL (2001) Acclimatization of soil respiration to warming in a tall grass prairie. Nature 413:622–625
Luo CY, Xu G, Chao Z, Wang S, Lin X, Hu Y, Zhang Z, Duan J, Chang X, Su A, Li Y, Zhao X, Du M, Tang Y, Kimball B (2010) Effect of warming and grazing on litter mass loss and temperature sensitivity of litter and dung mass loss on the Tibetan plateau. Glob Chang Biol 16:1606–1617
MacDonald NW, Zak DR, Pregitzer KS (1995) Temperature effects on kinetics of microbial respiration and net nitrogen and sulfur mineralization. Soil Sci Soc Am J 59:233–240
Margareta H, Håkan F (2000) Management of a semi-natural grassland; results from a 15-year-old experiment in southern Sweden. J Veg Sci 11:31–38
Novick KA, Stoy PC, Katul GG, Ellsworth DS, Siqueira MBS, Juang J, Oren R (2004) Carbon dioxide and water vapor exchange in a warm temperate grassland. Oecologia 138:259–274
Ohtonen R, Fritze H, Pennanen T (1999) Ecosystem properties and microbial community changes in primary succession on a glacier forefront. Oecologia 119:239–246
Ohtsuka T, Mo W, Satomura T, Inatomi M, Koizumi H (2007) Biometric based carbon flux measurements and net ecosystem production (NEP) in a temperate deciduous broad-leaved forest beneath a flux tower. Ecosystems 10:324–334
R Development Core Team (2012) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Raich JW, Schlesinger WH (1992) The global carbon dioxide flux in soil respiration and its relationship to vegetation and climate. Tellus 44:81–89
Rustad LE, Campbell JL, Marion GM, Norby RJ, Mitchell MJ, Hartley AE, Cornelissen JHC, Gurevitch J, GCTE-NEWS (2001) A meta-analysis of the response of soil respiration, net nitrogen mineralization, and aboveground plant growth to experimental ecosystem warming. Oecologia 126:543–562
Saigusa N, Yamamoto S, Murayama S, Kondo H (2005) Inter-annual variability of carbon budget components in an Asia-Flux forest site estimated by long-term flux measurements. Agric For Meteorol 134:17–26
Sakamoto K, Oba Y (1994) Effect of fungal to bacterial biomass ration on the relationship between CO2 evolution and total soil microbial biomass. Biol Fertil Soils 17:39–44
Scheiner D (1976) Determination of ammonia and Kjeldahl nitrogen by indophenol method. Water Res 10:31–36
Schindlbacher A, Zechmeister-Boltenstern S, Jandl R (2009) Carbon losses due to soil warming: do autotrophic and heterotrophic soil respiration respond equally? Glob Chang Biol 15:901–913
Scurlock JMO, Hall DO (1998) The global carbon sink: a grassland perspective. Glob Chang Biol 4:229–233
Sekine Y, Yoshitake S, Tomotsune M, Masuda R, Koizumi H (2013) CO2 flux responses in a cool-temperate grassland to an in situ warming experiment using infrared heaters. J Geogr (Chigaku Zasshi) 122:733–744 (in Japanese with English summary)
Stoffel W, Chu F, Ahrens EH (1959) Analysis of long-chain fatty acids by gas–liquid chromatography. Micromethod for preparation of methyl esters. Anal Chem 31:307–308
Suttie JM, Reynolds SG, Batello C (2005) Grasslands of the world. Plant Production and Protection Series 34, Food and Agriculture Organization of the United Nations, Rome
Suyker AE, Verma SB, Burba GG (2003) Interannual variability in net CO2 exchange of a native tallgrass prairie. Glob Chang Biol 9:255–265
Thornley JHM, Cannell MGR (1997) Temperate grassland responses to climate change: an analysis using the Hurley pasture model. Ann Bot 80:205–221
van Meeteren MJM, Tietema A, van Loon EE, Verstraten JM (2008) Microbial dynamics and litter decomposition under a changed climate in a Dutch heathland. Appl Soil Ecol 38:119–127
Wan S, Hui D, Wallace L, Luo Y (2005) Direct and indirect effects of experimental warming on ecosystem carbon processes in a tallgrass prairie. Glob Biogeochem Cycle 19:GB2014
Warren-Wilson J (1957) Arctic plant growth. Adv Sci 13:383–388
White DC, Davis WM, Nickels JS, King JD, Bobbie RJ (1979) Determination of the sedimentary microbial biomass by extractible lipid phosphate. Oecologia 40:51–62
Wu Y, Yu X, Wang H, Ding N, Xu J (2010) Does history matter? Temperature effects on soil microbial biomass and community structure based on the phospholipid fatty acid (PLFA) analysis. J Soils Sediments 10:223–230
Wu Z, Dijkstra P, Koch GW, Peñuelas J, Hungate BA (2011) Responses of terrestrial ecosystems to temperate and precipitation change: a meta-analysis of experimental manipulation. Glob Chang Biol 17:927–942
Yoshitake S, Soutome H, Koizumi H (2014) Deposition and decomposition of cattle dung and its impact on soil properties and plant growth in a cool-temperate pasture. Ecol Res 29:673–684
Zhang W, Parker KM, Luo Y, Wan S, Wallace LL, Hu S (2005) Soil microbial responses to experimental warming and clipping in a tallgrass prairie. Glob Chang Biol 11:266–277
Zhang N, Liu W, Yang H, Yu X, Gutknecht JLM, Zhang Z, Wan S, Ma K (2013) Soil microbial responses to warming and increased precipitation and their implications for ecosystem C cycling. Oecologia 173:1125–1142
Zogg GP, Zak DR, Ringelberg DB, White DC, MacDonald NW, Pregitzer KS (1997) Compositional and functional shifts in microbial communities due to soil warming. Soil Sci Soc Am J 61:475–481
Acknowledgments
We thank Mr. K. Kurumado and Mr. Y. Miyamoto of the Takayama Field Station, Gifu University, Japan, for their technical assistance and support. This study was partly supported by a Grant-in-Aid for Scientific Research from the Japan Society for the Promotion of Science.
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Yoshitake, S., Tabei, N., Mizuno, Y. et al. Soil microbial response to experimental warming in cool temperate semi-natural grassland in Japan. Ecol Res 30, 235–245 (2015). https://doi.org/10.1007/s11284-014-1209-3
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DOI: https://doi.org/10.1007/s11284-014-1209-3