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Effect of intensity and duration of freezing on soil microbial biomass, extractable C and N pools, and N2O and CO2 emissions from forest soils in cold temperate region

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Abstract

Freezing can increase the emissions of carbon dioxide (CO2) and nitrous oxide (N2O) and the release of labile carbon (C) and nitrogen (N) pools into the soil. However, there is limited knowledge about how both emissions respond differently to soil freezing and their relationships to soil properties. We evaluated the effect of intensity and duration of freezing on the emissions of CO2 and N2O, net N mineralization, microbial biomass, and extractable C and N pools in soils from a mature broadleaf and Korean pine mixed forest and an adjacent secondary white birch forest in northeastern China. These soils had different contents of microbial biomass and bulk density. Intact soil cores of 0–5 cm and 5–10 cm depth sampled from the two temperate forest floors were subjected to -8, -18, and -80°C freezing treatments for a short (10 d) and long (145 d) duration, and then respectively incubated at 10°C for 21 d. Soil cores, incubated at 10°C for 21 d without a pretreatment of freezing, served as control. Emissions of N2O and CO2 after thaw varied with forest type, soil depth, and freezing treatment. The difference could be induced by the soil water-filled pore space (WFPS) during incubation and availability of substrates for N2O and CO2 production, which are released by freezing. A maximum N2O emission following thawing of frozen soils was observed at approximately 80% WFPS, whereas CO2 emission from soils after thaw significantly increased with increasing WFPS. The soil dissolved organic C just after freezing treatment and CO2 emission increased with increase of freezing duration, which paralleled with a decrease in soil microbial biomass C. The cumulative net N mineralization and net ammonification after freezing treatment as well as N2O emission were significantly affected by freezing temperature. The N2O emission was negatively correlated to soil pH and bulk density, but positively correlated to soil K2SO4-extractable NO3 --N content and net ammonification. The CO2 emission was positively correlated to the cumulative net N mineralization and net ammonification. From the above results, it can be reasonably concluded that for a wide range of freezing temperature and freezing duration, N2O and CO2 emissions after thaw were associated mainly with the changes in soil net N mineralization and the availability of substrate liberated by freezing as well as other soil properties that influence porosity.

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References

  • Brooks P D, McKnight D, Elder K. 2005. Carbon limitation of soil respiration under winter snowpacks: Potential feedbacks between growing season and winter carbon fluxes. Global Change Biol, 11: 231–238

    Article  Google Scholar 

  • Christensen S, Christensen B T. 1991. Organic matter available fordenitrification in different soil fractions: Effect of freeze/thaw cycles and straw disposal. J Soil Sci, 42: 637–647

    Article  Google Scholar 

  • Christensen S, Tiedje J M. 1990. Brief and vigorous N2O Production by soil at spring thaw. J Soil Sci, 41: 1–4

    Article  Google Scholar 

  • Clark K, Chantigny M H, Angers D A, et al. 2009. Nitrogen transformations in cold and frozen agricultural soils following organic amendments. Soil Biol Biochem, 41: 348–356

    Article  Google Scholar 

  • Coxson D S, Parkinson D. 1987. Winter respiratory activity in aspen woodland forest floor litter and soils. Soil Biol Biochem, 19: 49–59

    Article  Google Scholar 

  • Cytryn E, Levkovitch K, Negreanu Y, et al. 2012. Impact of short-term acidification on nitrification and nitrifying bacterial community dynamics in soilless cultivation media. Appl Envrion Microbiol, 78: 6576–6582

    Article  Google Scholar 

  • DeLuca T H, Keeney D R, McCarty G W. 1992. Effects of freeze-thaw events on mineralization of soil-nitrogen. Biol Fertil Soils, 14: 116–120

    Article  Google Scholar 

  • Dörsch P, Palojärvi A, Mommertz S. 2004. Overwinter greenhouse gas fluxes in two contrasting agricultural habitats. Nutr Cycl Agroecosyst, 70: 117–133

    Article  Google Scholar 

  • Drotz S H, Sparrman T, Schleucher J, et al. 2010. Effects of soil organic matter composition on unfrozen water content and heterotrophic CO2 production of frozen soils. Geochim Cosmochim Acta, 74: 2281–2290

    Article  Google Scholar 

  • Edwards A C, Cresser M C. 1992. Freezing and its effects on chemical and biological properties of soil. Adv Soil Sci, 18: 59–79

    Article  Google Scholar 

  • Edwards A C, Killham K. 1986. The effect of freeze/thaw on gaseous nitrogen loss from upland soils. Soil Use Manage, 2: 86–91

    Article  Google Scholar 

  • Feng X, Nielsen L L, Simpson J. 2007. Responses of soil organic matter and microorganisms to freeze-thaw cycles. Soil Biol Biochem, 39: 2027–2037

    Article  Google Scholar 

  • Focht D D, Verstraete W. 1977. Biochemical ecology of nitrification and denitrification. In: Alexander M, ed. Advance in Microbiological Ecology. New York: Plenum Press. 135–214

    Google Scholar 

  • Franzluebbers A J. 1999. Microbial activity in response to water-filled pore space of variably eroded southern Piedmont soils. Appl Soil Ecol, 11: 91–101

    Article  Google Scholar 

  • Freppaz M, Williams B L, Edwards A C, et al. 2007. Simulating soil freeze/thaw cycles typical of winter alpine conditions: Implications for N and P availability. Appl Soil Ecol, 35: 247–255

    Article  Google Scholar 

  • Goldberg S D, Muhr J, Borken W, et al. 2008. Fluxes of climate-relevant trace gases between a Norway spruce forest soil and atmosphere during repeated freeze/thaw cycles in mesocosms. J Plant Nutri Soil Sci, 171: 729–739

    Article  Google Scholar 

  • Goldberg S D, Borken W, Gebauer G. 2010. N2O emission in a Norway spruce forest due to soil frost: Concentration and isotope profiles shed a new light on an old story. Biogeochemistry, 97: 21–30

    Article  Google Scholar 

  • Goodroad L, Keeney D R. 1984. Nitrous oxide emissions from soils during thawing. Can J Soil Sci, 64: 187–194

    Article  Google Scholar 

  • Goulden M L, Wofsy S C, Harden J W, et al. 1998. Sensitivity of boreal forest carbon balance to soil thaw. Science, 279: 214–217

    Article  Google Scholar 

  • Groffman P M, Hardy J P, Driscoll C T, et al. 2006. Snow depth, soil freezing, and fluxes of carbon dioxide, nitrous oxide and methane in a northern hardwood forest. Global Change Biol, 12: 1748–1760

    Article  Google Scholar 

  • Grogan P, Michelsen A, Ambus P, et al. 2004. Freeze-thaw regime effects on carbon and nitrogen dynamics in sub-arctic heath tundra mesocosms. Soil Biol Biochem, 36: 641–654

    Article  Google Scholar 

  • Harris D, Voroney R P, Paul E A. 1997. Measurement of microbial biomass N:C by chloroform fumigation-incubation. Can J Soil Sci, 77: 507–514

    Article  Google Scholar 

  • Hirota T, Iwata Y, Hayashi M, et al. 2006. Decreasing soil-frost depth and its relation to climate change in Tokachi, Hokkaido, Japan. J Meteorol Soc Japan, 84: 821–833

    Article  Google Scholar 

  • Henry H A L. 2007. Soil freeze-thaw cycle experiments: Trends, methodological weaknesses and suggested improvements. Soil Biol Biochem, 39: 977–986

    Article  Google Scholar 

  • Henry H A L. 2008. Climate change and soil freezing dynamics: historical trends and projected changes. Climatic Change, 87: 421–434

    Article  Google Scholar 

  • Hentschel K, Borken W, Matzner E. 2008. Leaching losses of nitrogen and dissolved organic matter following repeated frost/thaw events in a forest soil. J Plant Nutr Soil Sci, 171: 699–706

    Article  Google Scholar 

  • Hentschel K, Borken W, Zuber T, et al. 2009. Effects of soil frost on nitrogen net mineralization, soil solution chemistry and seepage losses in a temperate forest soil. Global Change Biol, 15: 825–836

    Article  Google Scholar 

  • Herrmann A, Witter E. 2002. Sources of C and N contributing to the flush in mineralization upon freeze-thaw cycles in soils. Soil Biol Biochem, 34: 1495–1505

    Article  Google Scholar 

  • Jenkinson D S. 1988. The determination of microbial biomass carbon and nitrogen in soil. In: Wilson J R, ed. Advances in Nitrogen Cycling in Agricultural Ecosystems. Wallingford: CAB International. 368–386

    Google Scholar 

  • Kim D G, Vargas R, Bond-Lamberty B, et al. 2012. Effects of soil rewetting and thawing on soil gas fluxes: A review of current literature and suggestions for future research. Biogeoscience, 9: 2459–2483

    Article  Google Scholar 

  • Kim H T. 1995. Soil Sampling, Preparation and Analysis. New York: Marcel Dekker

    Google Scholar 

  • Koponen H T, Martikainen P J. 2004. Soil water content and freezing temperature affect freeze-thaw related N2O production in organic soil. Nutr Cycl Agroecosyst, 69: 213–219

    Article  Google Scholar 

  • Kreyling J, Henry H A L. 2011. Vanishing winters in Germany: Soil frost dynamics and snow cover trends, and ecological implications. Clim Res, 46: 269–276

    Article  Google Scholar 

  • Kurganova I N, Tipe P. 2003. The effect of freezing-thawing processes on soil respiration activity. Eurasian Soil Sci, 36: 976–985

    Google Scholar 

  • Larsen K S, Jonasson S, Michelsen A. 2002. Repeated freeze/thaw cycles and their effects on biological processes in two arctic ecosystem types. Appl Soil Ecol, 21: 187–195

    Article  Google Scholar 

  • Leininger S, Urich T, Schloter M, et al. 2006. Archaea predominate among ammonia-oxidizing prokaryotes in soils. Nature, 442: 806–809

    Article  Google Scholar 

  • Lipson D A, Monson R K. 1998. Plant-microbe competition for soil amino acids in the alpine tundra: Effects of freeze-thaw and dry-rewet events. Oecologia, 113: 406–414

    Article  Google Scholar 

  • Lipson D A, Schadt C W, Schmidt S K. 2002. Changes in soil microbial community structure and function in an alpine dry meadow following spring snow melt. Microbial Ecol, 43: 307–314

    Article  Google Scholar 

  • Lipson D A, Schmidt S K, Monson R K. 2000. Carbon availability and temperature control the post-snowmelt decline in alpine soil microbial biomass. Soil Biol Biochem, 32: 441–448

    Article  Google Scholar 

  • Matzner E, Borken W. 2008. Do freeze-thaw events enhance C and N losses from soils of different ecosystems? A review. Eur J Soil Sci, 59: 274–284

    Article  Google Scholar 

  • Mikan C J, Schimel J P, Doyle A P. 2002. Temperature controls of microbial respiration in artic tundra soils above and below freezing. Soil Biol Biochem, 34: 1785–1795

    Article  Google Scholar 

  • Morkved P T, Dörsch P, Henriksen T M, et al. 2006. N2O emissions and product ratios of nitrification and denitrification as affected by freezing and thawing. Soil Biol Biochem, 38: 3411–3420

    Article  Google Scholar 

  • Muhr J, Borken W, Matzner E. 2009. Effects of soil frost on soil respiration and its radiocarbon signature in a Norway spruce forest soil. Global Change Biol, 15: 782–793

    Article  Google Scholar 

  • Neilsen C B, Groffman P M, Hamburg S P, et al. 2001. Freezing effects on carbon and nitrogen cycling in northern hardwood forest soils. Soil Sci Soc Am J, 65: 1723–1730

    Article  Google Scholar 

  • Öquist M G, Petrone K, Nilsson M, et al. 2007. Nitrification controls N2O production rates in a frozen boreal forest soil. Soil Biol Biochem, 39: 1809–1811

    Article  Google Scholar 

  • Panoff J M, Thammavongs B, Gueguen M, et al. 1998. Cold stress responses in mesophilic bacteria. Cryobiology, 36: 75–83

    Article  Google Scholar 

  • Paul E A, Clark F E. 1996. Soil Microbiology and Biochemistry. San Diego: Academic Press. 109–115

    Google Scholar 

  • Röver M, Heinemeyer O, Kaiser E A. 1998. Microbial induced oxide emissions from an arable soil during winter. Soil Biol Biochem, 30: 1859–1865

    Article  Google Scholar 

  • Ruser R, Flessa H, Schilling R, et al. 2001. Effect of crop-specific field management and N fertilization on N2O emissions from a fine-loamy soil. Nutr Cycl Agroecosyst, 59: 177–191

    Article  Google Scholar 

  • Sehy U, Dyckmans J, Ruser R, et al. 2004. Adding dissolved organic carbon to simulate freeze-thaw related N2O emissions from soil. J Plant Nutr Soil Sci, 167: 471–478

    Article  Google Scholar 

  • Sharma S, Szele Z, Schilling R, et al. 2006. Influence of freeze-thaw stress on the structure and function of microbial communities and denitrifying populations in soil. Appl Environ Microbiol, 72: 2148–2154

    Article  Google Scholar 

  • Shaver G R, Giblin A E, Nadelhoffer K J, et al. 2006. Carbon turnover in Alaskan tundra soils: Effects of organic matter quality, temperature, moisture and fertilizer. J Ecol, 94: 740–753

    Article  Google Scholar 

  • Skogland T, Lomeland S, Goksoyr J. 1988. Respiratory burst after freezing and thawing of soil: Experiments with soil bacteria. Soil Biol Biochem, 20: 851–856

    Article  Google Scholar 

  • Su M X, Kleineidam K, Schlotr M. 2010. Influence of different litter quality on the abundance of genes involved in nitrification and denitrification after freezing and thawing of an arable soil. Biol Fertil Soils, 46: 537–541

    Article  Google Scholar 

  • Teepe R, Ludwig B. 2004. Variability of CO2 and N2O emissions during freeze-thaw cycles: Results of model experiments on undisturbed forest-soil cores. J Plant Nutr Soil Sci, 167: 153–159

    Article  Google Scholar 

  • Teepe R, Vor R A, Beese F, et al. 2004. Emissions of N2O from soils during cycles of freezing and thawing and the effects of soil water, texture and duration of freezing. Eurasian J Soil Sci, 55: 357–365

    Article  Google Scholar 

  • Tenuta M, Sparling B. 2011. A laboratory study of soil conditions affecting emissions of nitrous oxide from packed cores subjected to freezing and thawing. Can J Soil Sci, 91: 223–233

    Article  Google Scholar 

  • Tierney G L, Fahey T J, Groffman P M, et al. 2001. Soil freezing alters fine root dynamics in a northern hardwood forest. Biogeochemistry, 56: 175–190

    Article  Google Scholar 

  • van Bochove E, Prevost D, Pelletier F. 2000. Effects of freeze-thaw and soil structure on nitrous oxide produced in a clay soil. Soil Sci Soc Am J, 64: 1638–1643

    Article  Google Scholar 

  • Wagner-Riddle C, Thurtell G W. 1998. Nitrous oxide emissions from agricultural fields during winter and spring thaw as affected by management practices. Nutr Cycl Agroecosyst, 52: 151–163

    Article  Google Scholar 

  • Wallander H, Nilsson L O, Hagerberg D, et al. 2003. Direct estimates of C:N ratios of ectomycorrhizal mycelia collected from Norway spruce forest soils. Soil Biol Biochem, 35: 997–999

    Article  Google Scholar 

  • Wendler G, Shulshi M. 2009. A century of climate change for Fairbanks, Alaska. Arctic, 62: 295–300

    Article  Google Scholar 

  • Wertz S, Goyer C, Zebarth B J, et al. 2013. Effects of temperatures near the freezing point on N2O emissions, denitrification and on the abundance and structure of nitrifying and denitrifying soil communities. FEMS Microbiol Ecol, 83: 242–254

    Article  Google Scholar 

  • Wick A F, Phillips R L, Liebig M A, et al. 2012. Linkages between soil micro-site properties and CO2 and N2O emissions during a simulated thaw for a northern prairie Mollisol. Soil Biol Biochem, 50: 118–125

    Article  Google Scholar 

  • Wu H H, Xu X K, Duan C T, et al. 2015. Effect of vegetation type, wetting intensity, and nitrogen supply on external carbon stimulated heterotrophic respiration and microbial biomass carbon in forest soils. Sci China Earth Sci, doi: 10.1007/s11430-015-5058-x

    Google Scholar 

  • Wu J, Joergensen R G, Pommerening B, et al. 1990. Measurement of soil microbial biomass C: An automated procedure. Soil Biol Biochem, 22: 1167–1169

    Article  Google Scholar 

  • Xu X K, Han L, Wang Y S, et al. 2007. Influence of vegetation types and soil properties on microbial biomass carbon and metabolic quotients in temperate volcanic and tropical forest soils. Soil Sci Plant Nutr, 53: 430–440

    Article  Google Scholar 

  • Xu X K, Luo X B. 2012. Effect of wetting intensity on soil GHG fluxes and microbial biomass under a temperate forest floor during dry season. Geoderma, 170: 118–126

    Article  Google Scholar 

  • Yanai Y, Toyota K, Okazaki M. 2004a. Effects of successive soil freeze-thaw cycles on nitrification potential of soils. Soil Sci Plant Nutr, 50: 831–837

    Article  Google Scholar 

  • Yanai Y, Toyota K, Okazaki M. 2004b. Effects of successive soil freezethaw cycles on soil microbial biomass and organic matter decomposition potential of soils. Soil Sci Plant Nutr, 50: 821–829

    Article  Google Scholar 

  • Yu J B, Liu J S, Sun Z G, et al. 2010. The fluxes and controlling factors of N2O and CH4 emissions from freshwater marsh in Northeast China. Sci China Earth Sci, 53: 700–709

    Article  Google Scholar 

  • Zhou W M, Chen H, Zhou L, et al. 2011. Effect of freezing-thawing on nitrogen mineralization in vegetation soils of four landscape zones of Changbai Mountain. Ann Forest Sci, 68: 943–951

    Article  Google Scholar 

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Xu, X., Duan, C., Wu, H. et al. Effect of intensity and duration of freezing on soil microbial biomass, extractable C and N pools, and N2O and CO2 emissions from forest soils in cold temperate region. Sci. China Earth Sci. 59, 156–169 (2016). https://doi.org/10.1007/s11430-015-5115-5

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