Abstract
Recent global warming models project a significant change in winter climate over the next few decades. The decrease in snowpack in the winter will decrease the heat insulation function of the snowpack, resulting in increased soil freeze–thaw cycles. Here, we examined the impact of winter freeze–thaw cycles on year-round dissolved nitrogen (N) and carbon (C) dynamics and their relationship with dissolved organic matter and microbial biomass in soil by conducting an in situ experimental reduction in snowpack. We investigated dissolved inorganic N (NH4+ and NO3−), dissolved organic N (DON), dissolved organic carbon (DOC), inorganic N leaching, soil microbial biomass, and microbial activities (mineralization and nitrification) in the surface soil of a northern hardwood forest located in Japan. Experimental snowpack reduction significantly increased the number of soil freeze–thaw cycles and soil frost depth. The NH4+ content of the surface soil was significantly increased by the amplified soil freeze–thaw cycles due to decreased snowpack, while the soil NO3– content was unchanged or decreased slightly. The gravimetric soil moisture, DON and DOC contents in soil and soil microbial biomass significantly increased by the snowpack removal in winter. Our results suggest that the amplified freeze–thaw cycles in soil increase the availability of DON and DOC for soil microbes due to an increase in soil freezing. The increases in both DON and DOC in winter contributed to the enhanced growth of soil microbes, resulting in the increased availability of NH4+ in winter from net mineralization following an increase in soil freeze–thaw cycles. Our study clearly indicated that snow reduction significantly increased the availability of dissolved nitrogen and carbon during winter, caused by increased soil water content due to freeze–thaw cycles in winter.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Explore related subjects
Discover the latest articles, news and stories from top researchers in related subjects.References
Austnes K, Vestgarden LS (2008) Prolonged frost increases release of C and N from a montane heathland soil in southern Norway. Soil Biol Biochem 40:2540–2546. https://doi.org/10.1016/j.soilbio.2008.06.014
Brookes PC, Landman A, Pruden G, Jenkinson DS (1985) Chloroform fumigation and the release of soil nitrogen: a rapid direct extraction method to measure microbial biomass nitrogen in soil. Soil Biol Biochem 17:837–842. https://doi.org/10.1016/0038-0717(85)90144-0
Brooks PD, Williams MW (1999) Snowpack controls on nitrogen cycling and export in seasonally snow covered catchments. Hydrol Process 13:2177–2190. https://doi.org/10.1002/(SICI)1099-1085(199910)13:14/15%3c2177:AID-HYP850%3e3.0.CO;2-V
Brooks PD, Williams MW, Schmidt SK (1996) Microbial activity under alpine snowpacks, Niwot Ridge, Colorado. Biogeochemistry 32:93–113. https://doi.org/10.1007/BF00000354
Campbell JL, Socci AM, Templer PH (2014) Increased nitrogen leaching following soil freezing is due to decreased root uptake in a northern hardwood forest. Glob Change Biol 20:2663–2673. https://doi.org/10.1111/gcb.12532
Christopher SF, Shibata H, Ozawa M, Nakagawa Y, Mitchell MJ (2008) The effect of soil freezing on N cycling: comparison of two headwater subcatchments with different vegetation and snowpack conditions in the northern Hokkaido Island of Japan. Biogeochemistry 88:15–30. https://doi.org/10.1007/s10533-008-9189-4
Cleavitt NL, Fahey TJ, Groffman PM, Hardy JP, Henry KS, Driscoll CT (2008) Effects of soil freezing on fine roots in a northern hardwood forest. Can J For Res 38:82–91. https://doi.org/10.1139/X07-133
Clein JS, Schimel JP (1995) Microbial activity of tundra and taiga soils at sub-zero temperatures. Soil Biol Biochem 27:1231–1234. https://doi.org/10.1016/0038-0717(95)00044-F
Davidson EA, Eckert RW, Hart SC, Firestone MK (1989) Direct extraction of microbial biomass nitrogen from forest and grassland soils of California. Soil Biol Biochem 21:773–778. https://doi.org/10.1016/0038-0717(89)90169-7
DeLuca TH, Keeney DR, McCarty GW (1992) Effect of freeze–thaw events on mineralization of soil nitrogen. Biol Fertil Soils 14:116–120. https://doi.org/10.1007/BF00336260
Durán J, Morse L, Groffman PM et al (2014) Winter climate change affects growing-season soil microbial biomass and activity in northern hardwood forests. Glob Change Biol 20:3568–3577. https://doi.org/10.1111/gcb.12624
Durán J, Morse JL, Groffman PM et al (2016) Climate change decreases nitrogen pools and mineralization rates in northern hardwood forests. Ecosphere 7:1–13. https://doi.org/10.1002/ecs2.1251
Freppaz M, Williams BL, Edwards AC, Scalenghe R, Zanini E (2007) Labile nitrogen, carbon, and phosphorus pools and nitrogen mineralization and immobilization rates at low temperatures in seasonally snow-covered soils. Biol Fertil Soil 43:519–529. https://doi.org/10.1007/s00374-006-0130-5
Freppaz M, Celi L, Marchelli M, Zanin E (2008) Snow removal and its influence on temperature and N dynamics in alpinesoils (Vallée d’Aoste, northwest Italy). J Plant Nutr Soil Sci 171:672–680. https://doi.org/10.1002/jpln.200700278
Gao D, Zhang L, Liu J, Peng B, Fan Z, Dai W, Jiang P, Bai E (2018) Responses of terrestrial nitrogen pools and dynamics to different patterns of freeze-thaw cycle: a meta-analysis. Glob Change Biol 24:2377–2389. https://doi.org/10.1111/gcb.14010
Gaul D, Hertel D, Leuschner C (2008) Effects of experimental soil frost on the fine-root system of mature Norway spruce. J Plant Nutr Soil Sci 171:690–698. https://doi.org/10.1002/jpln.200700284
Groffman PM, Hardy JP, Nolan S, Fitzhugh RD, Driscoll CT, Fahey TJ (1999) Snow depth, soil frost and nutrient loss in a northern hardwood forest. Hydrol Process 13:2275–2286
Groffman PM, Driscoll CT, Fahey TJ, Hardy JP, Fitzhugh RD, Tierney GL (2001a) Colder soils in a warmer world: a snow manipulation study in a northern hardwood forest ecosystem. Biogeochem 56:135–150. https://doi.org/10.1023/A:1013039830323
Groffman PM, Driscoll CDT, Fahey TJ et al (2001b) Effects of mild winter freezing on soil nitrogen and carbon dynamics in a northern hardwood forest. Biogeochem 56:191–213. https://doi.org/10.1023/A:1013024603959
Groffman PM, Hardy JP, Driscoll CT, Fahey TJ (2006) Snow depth, soil freezing, and fluxes of carbon dioxide, nitrous oxide and methane in a northern hardwood forest. Glob Change Biol 12:1748–1760. https://doi.org/10.1111/j.1365-2486.2006.01194.x
Groffman PM, Butterbach-Bahl K, Fulweiler RW, Gold AJ, Morse JL, Stander EK, Tague C, Tonitto C, Vidon P (2009) Challenges to incorporating spatially and temporally explicit phenomena (hotspots and hot moments) in denitrification models. Biogeochem 93:49–77. https://doi.org/10.1007/s10533-008-9277-5
Groffman PM, Hardy JP, Fashu-Kanu S, Driscoll CT, Cleavitt NL, Fahey TJ, Fisk MC (2011) Snow depth, soil freezing and nitrogen cycling in a northern hardwood forest landscape. Biogeochemistry 102:223–238. https://doi.org/10.1007/s10533-010-9436-3
Grogan P, Michelsen A, Ambus P, Jonasson S (2004) Freeze-thaw regime effects on carbon and nitrogen dynamics in sub-arctic heath tundra mesocosms. Soil Biol Biochem 36:641–654. https://doi.org/10.1016/j.soilbio.2003.12.007
Han Z, Deng M, Yuan A, Wang J, Li H, Ma J (2018) Vertical variation of a black soil’s properties in response to freeze-thaw cycles and its links to shift of microbial community structure. Sci Total Environ 625:106–113. https://doi.org/10.1016/j.scitotenv.2017.12.209
Hart S, Stark J, Davidson E, Firestone M (1994) Nitrogen mineralization, immobilization, and nitrification. In: Methods of soil analysis, Part 2. Microbiological and biochemical properties. Soil Science Society of America, pp 985–1018
Hentschel K, Borken W, Matzner E (2008) Repeated freeze-thaw events affect leaching losses of nitrogen dissolved organic matter in a forest soil. J Plant Nutr Soil Sci 171:699–706. https://doi.org/10.1002/jpln.200700154
Hentschel K, Borken W, Zuber T, Bogner C, Huwe B, Matzner E (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. https://doi.org/10.1111/j.1365-2486.2008.01753.x
Hishi T, Urakawa R, Tashiro N, Maeda Y, Shibata H (2014) Seasonality of factors controlling N mineralization rates among slope positions and aspects in cool-temperate deciduous natural forests and larch plantations. Biol Fertil Soils 50:343–356. https://doi.org/10.1007/s00374-013-0863-x
Hosokawa N, Isobe K, Urakawa R, Tateno R, Fukuzawa K, Watanabe T, Shibata H (2017) Soil freeze–thaw with root litter alters N transformations during the dormant season in soils under two temperate forests in northern Japan. Soil Biol Biochem 114:270–278. https://doi.org/10.1016/j.soilbio.2017.07.025
Inubushi K, Wada H, Takai Y (1984) Determination of microbial biomass-nitrogen in the submerged soil. Soil Sci Plant Nutr 30:455–460. https://doi.org/10.1080/00380768.1984.10434710
IPCC (2013) Climate Change 2013: The physical science basis. In: Stocker TF, Qin D, Plattner G-K, Tignor M, Allen SK, Boschung J, Nauels A, Xia Y, Bex V, Midgley PM (eds) Contribution of working group I to the fifth assessment report of the intergovernmental panel on climate change. Cambridge University Press, Cambridge
Isobe K, Suwa Y, Ikutani J et al (2011) Analytical techniques for quantifying 15N/14N of nitrate, nitrite, total dissolved nitrogen and ammonium in environmental samples using a gas chromatograph equipped with a quadrupole mass spectrometer. Microbes Environ 26:46–53. https://doi.org/10.1264/jsme2.ME10159
Isobe K, Oka H, Watanabe T, Tateno R, Urakawa R, Liang C, Senoo K, Shibata H (2018) High soil microbial activity in the winter season enhances nitrogen cycling in a cool-temperate deciduous forest. Soil Biol Biochem (In press). https://doi.org/10.1016/j.soilbio.2018.05.028
IUSS Working group WRB (2006) World reference base for soil resources (2006) World Soil Resources Report No 103. FAO, Rome
Iwata Y, Hirota T (2005) Monitoring over-winter soil water dynamics in a freezing and snow-covered environment using a thermally insulated tensiometer. Hydrol Process 19:3013–3019. https://doi.org/10.1002/hyp.5813
Iwata Y, Hayashi M, Suzuki S, Hirota T, Hasegawa S (2010) Effects of snow cover on soil freezing, water movement, and snowmelt infiltration: a paired plot experiment. Water Resour Res 46:1–11. https://doi.org/10.1029/2009WR008070
Joergensen RG (1996) The fumigation-extraction method to estimate soil microbial biomass: calibration of the KEC value. Soil Biol Biochem 28:25–31. https://doi.org/10.1016/0038-0717(95)00102-6
Kreyling J, Beierkuhnlein C, Pritsch K, Schloter M, Jentsch A (2008) Recurrent soil freeze–thaw cycles enhance grassland productivity. New Phytol 177:938–945. https://doi.org/10.1111/j.1469-8137.2007.02309.x
Kuroiwa M, Koba K, Isobe K et al (2011) Gross nitrification rates in four Japanese forest soils: heterotrophic versus autotrophic and the regulation factors for the nitrification. J For Res 16:363–373. https://doi.org/10.1007/s10310-011-0287-0
Kuzyakov Y, Blagodatskaya E (2015) Microbial hotspots and hot moments in soil: concept & review. Soil Biol Biochem 83:184–199. https://doi.org/10.1016/j.soilbio.2015.01.025
Lewis WM Jr, Grant MC (1980) Relationship between snow cover and winter losses of dissolved substances from a mountain watershed. Arct Alp Res 12:11–17. https://doi.org/10.2307/1550586
Li W, Wu J, Bai E et al (2016) Response of terrestrial nitrogen dynamics to snow cover change: a meta-analysis of experimental manipulation. Soil Biol Biochem 100:51–58. https://doi.org/10.1016/j.soilbio.2016.05.018
Lipson DA, Schmidt SK, Monson RK (2000) Carbon availability and temperature control the post-snowmelt decline in alpine soil microbial biomass. Soil Biol Biochem 32:441–448. https://doi.org/10.1016/S0038-0717(99)00068-1
Lovett GM, Weathers KC, Arthur MA (2002) Control of nitrogen loss from forested watersheds by soil carbon:nitrogen ratio and tree species composition. Ecosystems 5:712–718
Lovett GM, Weathers KC, Arthur MA, Schultz JC (2004) Nitrogen cycling in a northern hardwood forest: do species matter? Biogeochem 67:289–308
Makoto K, Kajimoto T, Koyama L, Kudo G, Shibata H, Yanai Y, Cornelissen JHC (2014) Winter climate change in plant–soil systems: summary of recent findings and future perspectives. Ecol Res 29:593–606. https://doi.org/10.1007/s11284-013-1115-0
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. https://doi.org/10.1111/j.1365-2389.2007.00992.x
Mitchell MJ, Driscoll CT, Kahl JS, Likens GE, Murdoch PS, Pardo LH (1996) Climatic control of nitrate loss from forested watersheds in the northeast United States. Environ Sci Technol 30:2609–2612. https://doi.org/10.1021/es9600237
Musa A, Ya L, Anzhi W, Cunyang N (2016) Characteristics of soil freeze–thaw cycles and their effects on water enrichment in the rhizosphere. Geoderma 264:132–139. https://doi.org/10.1016/j.geoderma.2015.10.008
Nakagawa Y, Shibata H, Satoh F, Sasa K (2008) Riparian control on NO3 −, DOC and dissolved Fe concentrations in mountainous streams, northern Japan. Limnology 9:195–206. https://doi.org/10.1007/s10201-008-0251-7
Nielsen CB, Groffman PM, Hamburg SP, Driscoll CT, Fahey TJ, Hardy JP (2001) Freezing effects on carbon and nitrogen cycling in soils from a northern hardwood forest. Soil Sci Soc Am J 65:1723–1730. https://doi.org/10.2136/sssaj2001.1723
Nyborg M, Laidlaw J, Solberg E, Malhi S (1997) Denitrification and nitrous oxide emissions from a Black Chernozemic soil during spring thaw in Alberta. Can J Soil Sci 77:153–160. https://doi.org/10.4141/S96-105
Ohte N, Sebestyen SD, Shanley JB, Doctor DH, Kendall C, Wankel SD, Boyer EW (2004) Tracing sources of nitrate in snowmelt runoff using a high-resolution isotopic technique. Geophys Res Lett 31:21506. https://doi.org/10.1029/2004GL020908
Ozawa M, Shibata H, Satoh F, Sasa K (2001) Annual element budget of soil in snow-dominated forested ecosystem. Water Air Soil Pollut 130:703–708. https://doi.org/10.1023/A:1013877316949
Reinmann AB, Templer PH (2016) Reduced winter snowpack and greater soil frost reduce live root biomass and stimulate radial growth and stem respiration of red maple (Acer rubrum) trees in a mixed-hardwood forest. Ecosystems 19:129–141. https://doi.org/10.1007/s10021-015-9923-4
Rickard W, Brown J (1972) Performance of a frost-tube for determination of soil freezing and thawing depths. Soil Sci 113:149–154
Schadt CW, Martin AP, Lipson DA, Schmidt SK (2003) Seasonal dynamics of previously unknown fungal lineages in tundra soils. Science 301:1359–1361. https://doi.org/10.1126/science.1086940
Schimel JP, Clein JS (1996) Microbial response to freeze-thaw cycles in tundra and taiga soils. Soil Biol Biochem 28:1061–1066. https://doi.org/10.1016/0038-0717(96)00083-1
Schmidt SK, Lipson DA (2004) Microbial growth under snow: implications for nutrient and allelochemical availability in temperate soils. Plant Soil 259:1–7. https://doi.org/10.1023/B:PLSO.0000020933.32473.7e
Shibata H (2016) Impact of winter climate change on nitrogen biogeochemistry in forest ecosystems: a synthesis from Japanese case studies. Ecol Indic 65:4–9. https://doi.org/10.1016/j.ecolind.2015.10.063
Shibata H, Hasegawa Y, Watanabe T, Fukuzawa K (2013) Impact of snowpack decrease on net nitrogen mineralization and nitrification in forest soil of northern Japan. Biogeochem 116:69–82. https://doi.org/10.1007/s10533-013-9882-9
Sorensen PO, Templer PH, Christenson L et al (2016a) Reduced snow cover alters root-microbe interactions and decreases nitrification rates in a northern hardwood forest. Ecology 97:3359–3367. https://doi.org/10.1002/ecy.1599
Sorensen PO, Templer PH, Finzi AC (2016b) Contrasting effects of winter snowpack and soil frost on growing season microbial biomass and enzyme activity in two mixed-hardwood forests. Biogeochemistry 128:141–154. https://doi.org/10.1007/s10533-016-0199-3
Sorensen PO, Finzi AC, Giasson MA et al (2018) Winter soil freeze-thaw cycles lead to reductions in soil microbial biomass and activity not compensated for by soil warming. Soil Biol Biochem 116:39–47. https://doi.org/10.1016/j.soilbio.2017.09.026
Stähli M, Stadler D (1997) Measurement of water and solute dynamics in freezing soil columns with time domain reflectometry. J Hydrol 195:352–369. https://doi.org/10.1016/S0022-1694(96)03227-1
Sulkava P, Huhta V (2003) Effects of hard frost and freeze-thaw cycles on decomposer communities and N mineralisation in boreal forest soil. Appl Soil Ecol 22:225–239. https://doi.org/10.1016/S0929-1393(02)00155-5
Suzuki S (2004) Dependence of unfrozen water content in unsaturated frozen clay soil on initial soil moisture content. Soil Sci Plant Nutr 50:603–606. https://doi.org/10.1080/00380768.2004.10408518
Tierney GL, Fahey TJ, Groffman PM, Hardy JP, Fitzhugh RD, Driscoll CT (2001) Soil freezing alters fine root dynamics in a northern hardwood forest. Biogeochemistry 56:175–190. https://doi.org/10.1023/A:1013072519889
Ueda MU, Muller O, Nakamura M, Nakaji T, Hiura T (2013) Soil warming decreases inorganic and dissolved organic nitrogen pools by preventing the soil from freezing in a cool temperate forest. Soil Biol Biochem 61:105–108. https://doi.org/10.1016/j.soilbio.2013.02.016
Urakawa R, Shibata H, Kuroiwa M et al (2014) Effects of freeze-thaw cycles resulting from winter climate change on soil nitrogen cycling in ten temperate forest ecosystems throughout the Japanese archipelago. Soil Biol Biochem 74:82–94. https://doi.org/10.1016/j.soilbio.2014.02.022
Urakawa R, Ohte N, Shibata H et al (2016) Factors contributing to soil nitrogen mineralization and nitrification rates of forest soils in the Japanese archipelago. For Ecol Manag 361:382–396. https://doi.org/10.1016/j.foreco.2015.11.033
Urakawa R, Shibata H, Toda H (2018) Points of attention of ion exchange resin used in resin-core method to determine soil nitrogen mineralization and nitrification. Jpn J For Environ 60 (In press) (in Japanese)
Vance ED, Brookes PC, Jenkinson DS (1987) An extraction method for measuring soil microbial biomass C. Soil Biol Biochem 19:703–707. https://doi.org/10.1016/0038-0717(87)90052-6
Vestgarden LS, Austnes K (2009) Effects of freeze-thaw on C and N release from soils below different vegetation in a montane system: a laboratory experiment. Glob Change Biol 15:876–887. https://doi.org/10.1111/j.1365-2486.2008.01722.x
Wang FL, Bettany JR (1994) Organic and inorganic nitrogen leaching from incubated soils subjected to freeze-thaw and flooding conditions. Can J Soil Sci 74:201–206
Wolf B, Zheng X, Brueggemann N et al (2010) Grazing-induced reduction of natural nitrous oxide release from continental steppe. Nature 464:881–884. https://doi.org/10.1038/nature08931
Acknowledgements
We would like to thank the collaborators of the ReSIN project (Regional and comparative soil incubation study on nitrogen dynamics in forest ecosystems: PI. Hideaki Shibata), Nobuhito Ohte, Nobuko Saigusa, Keitaro Fukushima, Tsutomu Enoki, Keisuke Koba, Toshizumi Miyamoto, Shin Ugawa and Kobayashi Makoto for their helpful discussions in the development of the manuscript. We would also like to thank Takayuki Yamauchi, Yasuyuki Shibata, Tomoyuki Nakagawa, Ken-ichi Ohta, Yoichiro Kitagawa, Yasunori Kishimoto, and Makoto Furuta, who are technical staff of the Hokkaido forest research station, Field Science Education and Research Center and Kyoto University for their great efforts in the manual snow removal. We would also like to thank Michiko Shimizu and the technical staff of the Northern Forestry and Development Office, Field Research Station, Field Science Center for Northern Biosphere, Hokkaido University, for their support with laboratory analysis. This study was partly supported by research funds (25252026) from the Japan Society for the Promotion of Science; Environment Research and Technology Development Fund (S-15) of the Ministry of the Environment, Japan; Integrated Research Program for Advancing Climate Models (TOUGOU program) from the Ministry of Education, Culture, Sports, Science and Technology (MEXT), Japan.
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Responsible Editor: Susan Ziegler.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Watanabe, T., Tateno, R., Imada, S. et al. The effect of a freeze–thaw cycle on dissolved nitrogen dynamics and its relation to dissolved organic matter and soil microbial biomass in the soil of a northern hardwood forest. Biogeochemistry 142, 319–338 (2019). https://doi.org/10.1007/s10533-019-00537-w
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10533-019-00537-w