Winter soil freeze-thaw cycles lead to reductions in soil microbial biomass and activity not compensated for by soil warming
Abstract
Air temperatures are rising and the winter snowpack is getting thinner in many high-latitude and high-elevation ecosystems around the globe. Past studies show that soil warming accelerates microbial metabolism and stimulates soil carbon (C) and nitrogen (N) cycling. Conversely, winter snow removal to simulate loss of snow cover leads to increased soil freezing and reductions in soil microbial biomass, exoenzyme activity, and N cycling. The Climate Change Across Seasons Experiment (CCASE), located at Hubbard Brook Experimental Forest, NH (USA) is designed to evaluate the combined effects of growing season soil warming and an increased frequency of winter soil freeze-thaw cycles on a northern forest ecosystem. Soils were collected from CCASE over two years (2014 and 2015) and extractable C and N pool sizes, as well as microbial biomass, exoenzymes, and potential net N mineralization and microbial respiration were measured. Soil warming alone did not stimulate microbial activity at any sampling time. Extractable amino acid N and organic C, proteolytic and acid phosphatase activity, and microbial respiration were reduced by the combination of warming in the growing season and winter soil freeze-thaw cycles during the period following snowmelt through tree leaf out in spring. The declines in microbial activity also coincidedmore »
- Authors:
-
- Boston University, MA (United States); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
- Boston University, MA (United States)
- Publication Date:
- Research Org.:
- Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC); National Science Foundation (NSF)
- OSTI Identifier:
- 1476593
- Grant/Contract Number:
- AC02-05CH11231; DEB1149929; DEB 140621; 1114804; 1637685
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Soil Biology and Biochemistry
- Additional Journal Information:
- Journal Volume: 116; Journal Issue: C; Journal ID: ISSN 0038-0717
- Publisher:
- Elsevier
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 54 ENVIRONMENTAL SCIENCES; soil freeze-thaw cycle; exoenzymes; Hubbard brook experimental forest; soil warming; microbial biomass
Citation Formats
Sorensen, Patrick O., Finzi, Adrien C., Giasson, Marc-André, Reinmann, Andrew B., Sanders-DeMott, Rebecca, and Templer, Pamela H. Winter soil freeze-thaw cycles lead to reductions in soil microbial biomass and activity not compensated for by soil warming. United States: N. p., 2017.
Web. doi:10.1016/j.soilbio.2017.09.026.
Sorensen, Patrick O., Finzi, Adrien C., Giasson, Marc-André, Reinmann, Andrew B., Sanders-DeMott, Rebecca, & Templer, Pamela H. Winter soil freeze-thaw cycles lead to reductions in soil microbial biomass and activity not compensated for by soil warming. United States. https://doi.org/10.1016/j.soilbio.2017.09.026
Sorensen, Patrick O., Finzi, Adrien C., Giasson, Marc-André, Reinmann, Andrew B., Sanders-DeMott, Rebecca, and Templer, Pamela H. Tue .
"Winter soil freeze-thaw cycles lead to reductions in soil microbial biomass and activity not compensated for by soil warming". United States. https://doi.org/10.1016/j.soilbio.2017.09.026. https://www.osti.gov/servlets/purl/1476593.
@article{osti_1476593,
title = {Winter soil freeze-thaw cycles lead to reductions in soil microbial biomass and activity not compensated for by soil warming},
author = {Sorensen, Patrick O. and Finzi, Adrien C. and Giasson, Marc-André and Reinmann, Andrew B. and Sanders-DeMott, Rebecca and Templer, Pamela H.},
abstractNote = {Air temperatures are rising and the winter snowpack is getting thinner in many high-latitude and high-elevation ecosystems around the globe. Past studies show that soil warming accelerates microbial metabolism and stimulates soil carbon (C) and nitrogen (N) cycling. Conversely, winter snow removal to simulate loss of snow cover leads to increased soil freezing and reductions in soil microbial biomass, exoenzyme activity, and N cycling. The Climate Change Across Seasons Experiment (CCASE), located at Hubbard Brook Experimental Forest, NH (USA) is designed to evaluate the combined effects of growing season soil warming and an increased frequency of winter soil freeze-thaw cycles on a northern forest ecosystem. Soils were collected from CCASE over two years (2014 and 2015) and extractable C and N pool sizes, as well as microbial biomass, exoenzymes, and potential net N mineralization and microbial respiration were measured. Soil warming alone did not stimulate microbial activity at any sampling time. Extractable amino acid N and organic C, proteolytic and acid phosphatase activity, and microbial respiration were reduced by the combination of warming in the growing season and winter soil freeze-thaw cycles during the period following snowmelt through tree leaf out in spring. The declines in microbial activity also coincided with an 85% decline in microbial biomass N at that time. Growing season warming and winter soil freeze-thaw cycles also resulted in a two-fold reduction in phenol oxidase activity and a 20% reduction in peroxidase activity and these declines persisted throughout the snow-free time of the year. Finally, the results from this study suggest that positive feedbacks between warming and rates of soil C and N cycling over the next 100 years will be partially mitigated by an increased frequency of winter soil freeze-thaw cycles, which decrease microbial biomass and rates of soil microbial activity.},
doi = {10.1016/j.soilbio.2017.09.026},
journal = {Soil Biology and Biochemistry},
number = C,
volume = 116,
place = {United States},
year = {Tue Oct 10 00:00:00 EDT 2017},
month = {Tue Oct 10 00:00:00 EDT 2017}
}
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Works referenced in this record:
Sensitivity of soil respiration and microbial communities to altered snowfall
journal, February 2013
- Aanderud, Zachary T.; Jones, Stuart E.; Schoolmaster, Donald R.
- Soil Biology and Biochemistry, Vol. 57
A parsimonious modular approach to building a mechanistic belowground carbon and nitrogen model: Parsimonious, Modular Model of Belowground C and N Cycling
journal, September 2017
- Abramoff, Rose Z.; Davidson, Eric A.; Finzi, Adrien C.
- Journal of Geophysical Research: Biogeosciences, Vol. 122, Issue 9
Seasonality and partitioning of root allocation to rhizosphere soils in a midlatitude forest
journal, November 2016
- Abramoff, Rose Z.; Finzi, Adrien C.
- Ecosphere, Vol. 7, Issue 11
Effects of experimentally imposed climate scenarios on flowering phenology and flower production of subarctic bog species
journal, September 2004
- Aerts, R.; Cornelissen, J. H. C.; Dorrepaal, E.
- Global Change Biology, Vol. 10, Issue 9
Warming and drying suppress microbial activity and carbon cycling in boreal forest soils
journal, December 2008
- Allison, Steven D.; Treseder, Kathleen K.
- Global Change Biology, Vol. 14, Issue 12
Appropriate experimental ecosystem warming methods by ecosystem, objective, and practicality
journal, November 2009
- Aronson, Emma L.; McNulty, Steven G.
- Agricultural and Forest Meteorology, Vol. 149, Issue 11
A meta-analysis of experimental warming effects on terrestrial nitrogen pools and dynamics
journal, April 2013
- Bai, Edith; Li, Shanlong; Xu, Wenhua
- New Phytologist, Vol. 199, Issue 2
Colorimetric Determination of Oxidizable Carbon in Acid Soil Solutions
journal, January 1988
- Bartlett, Richmond J.; Ross, Donald S.
- Soil Science Society of America Journal, Vol. 52, Issue 4
Ectomycorrhizal Cortinarius species participate in enzymatic oxidation of humus in northern forest ecosystems
journal, April 2014
- Bödeker, Inga T. M.; Clemmensen, Karina E.; de Boer, Wietse
- New Phytologist, Vol. 203, Issue 1
Increased soil nitrate losses under mature sugar maple trees affected by experimentally induced deep frost
journal, April 1995
- Boutin, Robert; Robitaille, Gilles
- Canadian Journal of Forest Research, Vol. 25, Issue 4
Chloroform fumigation and the release of soil nitrogen: A rapid direct extraction method to measure microbial biomass nitrogen in soil
journal, January 1985
- Brookes, P. C.; Landman, Andrea; Pruden, G.
- Soil Biology and Biochemistry, Vol. 17, Issue 6
Snowpack controls on nitrogen cycling and export in seasonally snow-covered catchments
journal, October 1999
- Brooks, Paul D.; Williams, Mark W.
- Hydrological Processes, Vol. 13, Issue 14-15
A paradox of cooling winter soil surface temperatures in a warming northeastern United States
journal, July 2011
- Brown, Paula J.; DeGaetano, Arthur T.
- Agricultural and Forest Meteorology, Vol. 151, Issue 7
Substrate supply, fine roots, and temperature control proteolytic enzyme activity in temperate forest soils
journal, April 2011
- Brzostek, Edward R.; Finzi, Adrien C.
- Ecology, Vol. 92, Issue 4
Trends in wintertime climate in the northeastern United States: 1965–2005
journal, January 2008
- Burakowski, Elizabeth A.; Wake, Cameron P.; Braswell, Bobby
- Journal of Geophysical Research, Vol. 113, Issue D20
Alkaline Persulfate Oxidation for Determining Total Nitrogen in Microbial Biomass Extracts
journal, January 1993
- Cabrera, M. L.; Beare, M. H.
- Soil Science Society of America Journal, Vol. 57, Issue 4
Increased nitrogen leaching following soil freezing is due to decreased root uptake in a northern hardwood forest
journal, February 2014
- Campbell, John L.; Socci, Anne M.; Templer, Pamela H.
- Global Change Biology, Vol. 20, Issue 8
A longer vernal window: the role of winter coldness and snowpack in driving spring transitions and lags
journal, September 2016
- Contosta, Alexandra R.; Adolph, Alden; Burchsted, Denise
- Global Change Biology, Vol. 23, Issue 4
Acceleration of global warming due to carbon-cycle feedbacks in a coupled climate model
journal, November 2000
- Cox, Peter M.; Betts, Richard A.; Jones, Chris D.
- Nature, Vol. 408, Issue 6809
Temperature sensitivity of soil carbon decomposition and feedbacks to climate change
journal, March 2006
- Davidson, Eric A.; Janssens, Ivan A.
- Nature, Vol. 440, Issue 7081
Innovative empirical approaches for inferring climate‐warming impacts on plants in remote areas
journal, August 2014
- De Frenne, Pieter
- New Phytologist, Vol. 205, Issue 3
Effect of freeze-thaw events on mineralization of soil nitrogen
journal, October 1992
- DeLuca, T. H.; Keeney, D. R.; McCarty, G. W.
- Biology and Fertility of Soils, Vol. 14, Issue 2
Spectrophotometric Determination of Nitrate with a Single Reagent
journal, January 2003
- Doane, Timothy A.; Horwáth, William R.
- Analytical Letters, Vol. 36, Issue 12
Seasonal plasticity in the temperature sensitivity of microbial activity in three temperate forest soils
journal, June 2013
- Drake, J. E.; Giasson, M. -A.; Spiller, K. J.
- Ecosphere, Vol. 4, Issue 6
Winter climate change affects growing-season soil microbial biomass and activity in northern hardwood forests
journal, May 2014
- Durán, Jorge; Morse, Jennifer L.; Groffman, Peter M.
- Global Change Biology, Vol. 20, Issue 11
Concrete Frost along an Elevational Gradient in New Hampshire
journal, December 1975
- Fahey, Timothy J.; Lang, Gerald E.
- Canadian Journal of Forest Research, Vol. 5, Issue 4
Soil respiration and soil carbon balance in a northern hardwood forest ecosystem
journal, February 2005
- Fahey, T. J.; Tierney, G. L.; Fitzhugh, R. D.
- Canadian Journal of Forest Research, Vol. 35, Issue 2
Climate–Carbon Cycle Feedback Analysis: Results from the C 4 MIP Model Intercomparison
journal, July 2006
- Friedlingstein, P.; Cox, P.; Betts, R.
- Journal of Climate, Vol. 19, Issue 14
Correction factors for dissolved organic carbon extracted from soil, measured using the Mn(III)-pyrophosphate colorimetric method adapted for a microplate reader
journal, November 2014
- Giasson, Marc-André; Averill, Colin; Finzi, Adrien C.
- Soil Biology and Biochemistry, Vol. 78
Soil respiration in a northeastern US temperate forest: a 22-year synthesis
journal, November 2013
- Giasson, M. -A.; Ellison, A. M.; Bowden, R. D.
- Ecosphere, Vol. 4, Issue 11
Biogeochemical Diversity Along a Riverside Toposequence in Arctic Alaska
journal, February 1991
- Giblin, A. E.; Nadelhoffer, K. J.; Shaver, G. R.
- Ecological Monographs, Vol. 61, Issue 4
Methods for Measuring Denitrification: Diverse Approaches to a Difficult Problem
journal, December 2006
- Groffman, Peter M.; Altabet, Mark A.; Böhlke, J. K.
- Ecological Applications, Vol. 16, Issue 6
Long-Term Integrated Studies Show Complex and Surprising Effects of Climate Change in the Northern Hardwood Forest
journal, December 2012
- Groffman, Peter M.; Rustad, Lindsey E.; Templer, Pamela H.
- BioScience, Vol. 62, Issue 12
Climate change at the ecosystem scale: a 50-year record in New Hampshire
journal, July 2012
- Hamburg, Steven P.; Vadeboncoeur, Matthew A.; Richardson, Andrew D.
- Climatic Change, Vol. 116, Issue 3-4
Past and future changes in climate and hydrological indicators in the US Northeast
journal, November 2006
- Hayhoe, Katharine; Wake, Cameron P.; Huntington, Thomas G.
- Climate Dynamics, Vol. 28, Issue 4
Climate change and soil freezing dynamics: historical trends and projected changes
journal, September 2007
- Henry, Hugh A. L.
- Climatic Change, Vol. 87, Issue 3-4
Soil extracellular enzyme dynamics in a changing climate
journal, April 2012
- Henry, Hugh A. L.
- Soil Biology and Biochemistry, Vol. 47
Simultaneous Inference in General Parametric Models
journal, June 2008
- Hothorn, Torsten; Bretz, Frank; Westfall, Peter
- Biometrical Journal, Vol. 50, Issue 3
No temperature acclimation of soil extracellular enzymes to experimental warming in an alpine grassland ecosystem on the Tibetan Plateau
journal, April 2013
- Jing, Xin; Wang, Yonghui; Chung, Haegeun
- Biogeochemistry, Vol. 117, Issue 1
Simple method to enable the high resolution determination of total free amino acids in soil solutions and soil extracts
journal, December 2002
- Jones, D.
- Soil Biology and Biochemistry, Vol. 34, Issue 12
Soil ecosystem functioning under climate change: plant species and community effects
journal, March 2010
- Kardol, Paul; Cregger, Melissa A.; Campany, Courtney E.
- Ecology, Vol. 91, Issue 3
Vanishing winters in Germany: soil frost dynamics and snow cover trends, and ecological implications
journal, May 2011
- Kreyling, J.; Henry, Hal
- Climate Research, Vol. 46, Issue 3
Fungal Growth and Biomass Development is Boosted by Plants in Snow-Covered Soil
journal, January 2012
- Kuhnert, Regina; Oberkofler, Irmgard; Peintner, Ursula
- Microbial Ecology, Vol. 64, Issue 1
Responses of ecosystem carbon cycle to experimental warming: a meta-analysis
journal, March 2013
- Lu, Meng; Zhou, Xuhui; Yang, Qiang
- Ecology, Vol. 94, Issue 3
Do freeze-thaw events enhance C and N losses from soils of different ecosystems? A review
journal, April 2008
- Matzner, E.; Borken, W.
- European Journal of Soil Science, Vol. 59, Issue 2
Soil warming, carbon-nitrogen interactions, and forest carbon budgets
journal, May 2011
- Melillo, J. M.; Butler, S.; Johnson, J.
- Proceedings of the National Academy of Sciences, Vol. 108, Issue 23
Soil Warming and Carbon-Cycle Feedbacks to the Climate System
journal, December 2002
- Melillo, J. M.
- Science, Vol. 298, Issue 5601
A general and simple method for obtaining R 2 from generalized linear mixed-effects models
journal, December 2012
- Nakagawa, Shinichi; Schielzeth, Holger
- Methods in Ecology and Evolution, Vol. 4, Issue 2
Severe soil frost reduces losses of carbon and nitrogen from the forest floor during simulated snowmelt: A laboratory experiment
journal, January 2012
- Reinmann, Andrew B.; Templer, Pamela H.; Campbell, John L.
- Soil Biology and Biochemistry, Vol. 44, Issue 1
The Performance of a Frost-Tube for the Determination of soil Freezing and Thawing Depths
journal, January 1972
- Rickard, Warren; Brown, Jerry
- Soil Science, Vol. 113, Issue 2
A meta-analysis of the response of soil respiration, net nitrogen mineralization, and aboveground plant growth to experimental ecosystem warming
journal, February 2001
- Rustad, L.; Campbell, J.; Marion, G.
- Oecologia, Vol. 126, Issue 4
What about winter? Integrating the missing season into climate change experiments in seasonally snow covered ecosystems
journal, May 2017
- Sanders-DeMott, Rebecca; Templer, Pamela H.
- Methods in Ecology and Evolution, Vol. 8, Issue 10
Microbial physiology and soil CO 2 efflux after 9 years of soil warming in a temperate forest - no indications for thermal adaptations
journal, September 2015
- Schindlbacher, Andreas; Schnecker, Jörg; Takriti, Mounir
- Global Change Biology, Vol. 21, Issue 11
Microscale determination of inorganic nitrogen in water and soil extracts
journal, January 1995
- Sims, G. K.; Ellsworth, T. R.; Mulvaney, R. L.
- Communications in Soil Science and Plant Analysis, Vol. 26, Issue 1-2
Phenol oxidase, peroxidase and organic matter dynamics of soil
journal, March 2010
- Sinsabaugh, Robert L.
- Soil Biology and Biochemistry, Vol. 42, Issue 3
Respiratory burst after freezing and thawing of soil: Experiments with soil bacteria
journal, January 1988
- Skogland, T.; Lomeland, S.; Goksøyr, J.
- Soil Biology and Biochemistry, Vol. 20, Issue 6
Contrasting effects of winter snowpack and soil frost on growing season microbial biomass and enzyme activity in two mixed-hardwood forests
journal, March 2016
- Sorensen, Patrick O.; Templer, Pamela H.; Finzi, Adrien C.
- Biogeochemistry, Vol. 128, Issue 1-2
Modeling the effects of temperature and moisture on soil enzyme activity: Linking laboratory assays to continuous field data
journal, December 2012
- Steinweg, J. Megan; Dukes, Jeffrey S.; Wallenstein, Matthew D.
- Soil Biology and Biochemistry, Vol. 55
Climate Change Across Seasons Experiment (CCASE): A new method for simulating future climate in seasonally snow-covered ecosystems
journal, February 2017
- Templer, Pamela H.; Reinmann, Andrew B.; Sanders-DeMott, Rebecca
- PLOS ONE, Vol. 12, Issue 2
Soil warming decreases inorganic and dissolved organic nitrogen pools by preventing the soil from freezing in a cool temperate forest
journal, June 2013
- Ueda, Miki U.; Muller, Onno; Nakamura, Masahiro
- Soil Biology and Biochemistry, Vol. 61
Seasonal variation of soil protease activities and their relation to proteolytic bacteria and Bacillus spp in paddy field soil
journal, February 1995
- Watanabe, Katsuji; Hayano, Koichi
- Soil Biology and Biochemistry, Vol. 27, Issue 2
No effects of experimental warming but contrasting seasonal patterns for soil peptidase and glycosidase enzymes in a sub-arctic peat bog
journal, June 2013
- Weedon, James T.; Aerts, Rien; Kowalchuk, George A.
- Biogeochemistry, Vol. 117, Issue 1
Influence of the seasonal snow cover on the ground thermal regime: An overview
journal, January 2005
- Zhang, Tingjun
- Reviews of Geophysics, Vol. 43, Issue 4
Climate Change Across Seasons Experiment (CCASE) at the Hubbard Brook Experimental Forest: Snow and Frost
dataset, January 2019
- Templer, Pamela; Sanders-DeMott, Rebecca; Juice, Stephanie
- Environmental Data Initiative
Hubbard Brook Experimental Forest: microbial biomass and activity at Climate Change Across Seasons Experiment (CCASE) plots, 2015
dataset, January 2020
- Groffman, Peter M.; Martel, Lisa; Templer, Pamela H.
- Environmental Data Initiative
Climate Change Across Seasons Experiment (CCASE) at the Hubbard Brook Experimental Forest: Snow and Frost
dataset, January 2019
- Templer, Pamela; Sanders-DeMott, Rebecca; Juice, Stephanie
- Environmental Data Initiative
Hubbard Brook Experimental Forest: microbial biomass and activity at Climate Change Across Seasons Experiment (CCASE) plots, 2015
dataset, January 2020
- Groffman, Peter M.; Martel, Lisa; Templer, Pamela H.
- Environmental Data Initiative
Works referencing / citing this record:
A proxy-year analysis shows reduced soil temperatures with climate warming in boreal forest
journal, November 2018
- Halim, Md Abdul; Thomas, Sean C.
- Scientific Reports, Vol. 8, Issue 1