Reduced snow cover alters root‐microbe interactions and decreases nitrification rates in a northern hardwood forest
Abstract
Abstract Snow cover is projected to decline during the next century in many ecosystems that currently experience a seasonal snowpack. Because snow insulates soils from frigid winter air temperatures, soils are expected to become colder and experience more winter soil freeze‐thaw cycles as snow cover continues to decline. Tree roots are adversely affected by snowpack reduction, but whether loss of snow will affect root‐microbe interactions remains largely unknown. The objective of this study was to distinguish and attribute direct (e.g., winter snow‐ and/or soil frost‐mediated) vs. indirect (e.g., root‐mediated) effects of winter climate change on microbial biomass, the potential activity of microbial exoenzymes, and net N mineralization and nitrification rates. Soil cores were incubated in situ in nylon mesh that either allowed roots to grow into the soil core (2 mm pore size) or excluded root ingrowth (50 μm pore size) for up to 29 months along a natural winter climate gradient at Hubbard Brook Experimental Forest, NH ( USA ). Microbial biomass did not differ among ingrowth or exclusion cores. Across sampling dates, the potential activities of cellobiohydrolase, phenol oxidase, and peroxidase, and net N mineralization rates were more strongly related to soil volumetric water content ( P < 0.05; Rmore »
- Authors:
-
- Department of Biology Boston University Boston Massachusetts USA
- Biology Department Vassar College Poughkeepsie New York USA
- Center for Functional Ecology Department of Life Sciences University of Coimbra Coimbra Portugal
- Department of Natural Resources Cornell University Ithaca New York USA
- Department of Biology Miami University Oxford Ohio USA
- Department of Earth and Environmental Sciences Brooklyn College City University of New York Advanced Science Research Center New York New York USA
- Department of Environmental Science and Management Portland State University Portland Oregon USA
- Publication Date:
- Sponsoring Org.:
- USDOE
- OSTI Identifier:
- 1401486
- Grant/Contract Number:
- 10‐DOE‐1053
- Resource Type:
- Publisher's Accepted Manuscript
- Journal Name:
- Ecology
- Additional Journal Information:
- Journal Name: Ecology Journal Volume: 97 Journal Issue: 12; Journal ID: ISSN 0012-9658
- Publisher:
- Wiley Blackwell (John Wiley & Sons)
- Country of Publication:
- United States
- Language:
- English
Citation Formats
Sorensen, Patrick O., Templer, Pamela H., Christenson, Lynn, Duran, Jorge, Fahey, Timothy, Fisk, Melany C., Groffman, Peter M., Morse, Jennifer L., and Finzi, Adrien C. Reduced snow cover alters root‐microbe interactions and decreases nitrification rates in a northern hardwood forest. United States: N. p., 2016.
Web. doi:10.1002/ecy.1599.
Sorensen, Patrick O., Templer, Pamela H., Christenson, Lynn, Duran, Jorge, Fahey, Timothy, Fisk, Melany C., Groffman, Peter M., Morse, Jennifer L., & Finzi, Adrien C. Reduced snow cover alters root‐microbe interactions and decreases nitrification rates in a northern hardwood forest. United States. https://doi.org/10.1002/ecy.1599
Sorensen, Patrick O., Templer, Pamela H., Christenson, Lynn, Duran, Jorge, Fahey, Timothy, Fisk, Melany C., Groffman, Peter M., Morse, Jennifer L., and Finzi, Adrien C. Fri .
"Reduced snow cover alters root‐microbe interactions and decreases nitrification rates in a northern hardwood forest". United States. https://doi.org/10.1002/ecy.1599.
@article{osti_1401486,
title = {Reduced snow cover alters root‐microbe interactions and decreases nitrification rates in a northern hardwood forest},
author = {Sorensen, Patrick O. and Templer, Pamela H. and Christenson, Lynn and Duran, Jorge and Fahey, Timothy and Fisk, Melany C. and Groffman, Peter M. and Morse, Jennifer L. and Finzi, Adrien C.},
abstractNote = {Abstract Snow cover is projected to decline during the next century in many ecosystems that currently experience a seasonal snowpack. Because snow insulates soils from frigid winter air temperatures, soils are expected to become colder and experience more winter soil freeze‐thaw cycles as snow cover continues to decline. Tree roots are adversely affected by snowpack reduction, but whether loss of snow will affect root‐microbe interactions remains largely unknown. The objective of this study was to distinguish and attribute direct (e.g., winter snow‐ and/or soil frost‐mediated) vs. indirect (e.g., root‐mediated) effects of winter climate change on microbial biomass, the potential activity of microbial exoenzymes, and net N mineralization and nitrification rates. Soil cores were incubated in situ in nylon mesh that either allowed roots to grow into the soil core (2 mm pore size) or excluded root ingrowth (50 μm pore size) for up to 29 months along a natural winter climate gradient at Hubbard Brook Experimental Forest, NH ( USA ). Microbial biomass did not differ among ingrowth or exclusion cores. Across sampling dates, the potential activities of cellobiohydrolase, phenol oxidase, and peroxidase, and net N mineralization rates were more strongly related to soil volumetric water content ( P < 0.05; R 2 = 0.25–0.46) than to root biomass, snow or soil frost, or winter soil temperature ( R 2 < 0.10). Root ingrowth was positively related to soil frost ( P < 0.01; R 2 = 0.28), suggesting that trees compensate for overwinter root mortality caused by soil freezing by re‐allocating resources towards root production. At the sites with the deepest snow cover, root ingrowth reduced nitrification rates by 30% ( P < 0.01), showing that tree roots exert significant influence over nitrification, which declines with reduced snow cover. If soil freezing intensifies over time, then greater compensatory root growth may reduce nitrification rates directly via plant‐microbe N competition and indirectly through a negative feedback on soil moisture, resulting in lower N availability to trees in northern hardwood forests.},
doi = {10.1002/ecy.1599},
journal = {Ecology},
number = 12,
volume = 97,
place = {United States},
year = {Fri Dec 02 00:00:00 EST 2016},
month = {Fri Dec 02 00:00:00 EST 2016}
}
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Works referenced in this record:
Climate Variation and Soil Carbon and Nitrogen Cycling Processes in a Northern Hardwood Forest
journal, September 2009
- Groffman, Peter M.; Hardy, Janet P.; Fisk, Melany C.
- Ecosystems, Vol. 12, 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
Responses of extracellular enzymes to simple and complex nutrient inputs
journal, May 2005
- Allison, Steven D.; Vitousek, Peter M.
- Soil Biology and Biochemistry, Vol. 37, Issue 5
Influence of landscape position and transient water table on soil development and carbon distribution in a steep, headwater catchment
journal, August 2014
- Bailey, Scott W.; Brousseau, Patricia A.; McGuire, Kevin J.
- Geoderma, Vol. 226-227
N uptake and growth responses to sub-lethal freezing in the grass Poa pratensis L.
journal, April 2012
- Malyshev, Andrey V.; Henry, Hugh A. L.
- Plant and Soil, Vol. 360, Issue 1-2
Bacterial and Fungal Contributions to Carbon Sequestration in Agroecosystems
journal, January 2006
- Six, J.; Frey, S. D.; Thiet, R. K.
- Soil Science Society of America Journal, Vol. 70, Issue 2
Competition between roots and microorganisms for nitrogen: mechanisms and ecological relevance
journal, March 2013
- Kuzyakov, Yakov; Xu, Xingliang
- New Phytologist, Vol. 198, Issue 3
Increased snow depth affects microbial activity and nitrogen mineralization in two Arctic tundra communities
journal, February 2004
- Schimel, Joshua P.; Bilbrough, Carol; Welker, Jeffery M.
- Soil Biology and Biochemistry, Vol. 36, Issue 2
Phenology of a northern hardwood forest canopy
journal, July 2006
- Richardson, Andrew D.; Bailey, Amey Schenck; Denny, Ellen G.
- Global Change Biology, Vol. 12, Issue 7
Microbial growth in Arctic tundra soil at −2°C
journal, April 2009
- McMahon, Shawna K.; Wallenstein, Matthew D.; Schimel, Joshua P.
- Environmental Microbiology Reports, Vol. 1, Issue 2
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
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
Soil Denitrification Fluxes in a Northern Hardwood Forest: The Importance of Snowmelt and Implications for Ecosystem N Budgets
journal, January 2015
- Morse, Jennifer L.; Durán, Jorge; Groffman, Peter M.
- Ecosystems, Vol. 18, Issue 3
Past and projected future changes in snowpack and soil frost at the Hubbard Brook Experimental Forest, New Hampshire, USA
journal, January 2010
- Campbell, John L.; Ollinger, Scott V.; Flerchinger, Gerald N.
- Hydrological Processes
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
Fine Root Dynamics in a Northern Hardwood Forest Ecosystem, Hubbard Brook Experimental Forest, NH
journal, September 1994
- Fahey, Timothy J.; Hughes, Jeffrey W.
- The Journal of Ecology, Vol. 82, Issue 3
Optimization of hydrolytic and oxidative enzyme methods for ecosystem studies
journal, July 2011
- German, Donovan P.; Weintraub, Michael N.; Grandy, A. Stuart
- Soil Biology and Biochemistry, Vol. 43, Issue 7
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
Spectrophotometric Determination of Nitrate with a Single Reagent
journal, January 2003
- Doane, Timothy A.; Horwáth, William R.
- Analytical Letters, Vol. 36, Issue 12
Mycorrhizas and soil structure
journal, July 2006
- Rillig, Matthias C.; Mummey, Daniel L.
- New Phytologist, Vol. 171, Issue 1
Digging deeper: fine-root responses to rising atmospheric CO2 concentration in forested ecosystems
journal, December 2009
- Iversen, Colleen M.
- New Phytologist, Vol. 186, Issue 2
Rhizosphere priming effect increases the temperature sensitivity of soil organic matter decomposition: RPE ENHANCES Q10 OF SOM DECOMPOSITION
journal, November 2010
- Zhu, Biao; Cheng, Weixin
- Global Change Biology, Vol. 17, Issue 6
Combined Effects of Soil Freezing and N Addition on Losses and Interception of N Over Winter and Summer
journal, January 2013
- Vankoughnett, Mathew R.; Henry, Hugh A. L.
- Ecosystems, Vol. 16, Issue 4
Carbon allocation in forest ecosystems
journal, October 2007
- Litton, Creighton M.; Raich, James W.; Ryan, Michael G.
- Global Change Biology, Vol. 13, Issue 10
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
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
Seasonal dynamics of soil respiration and N mineralization in chronically warmed and fertilized soils
journal, March 2011
- Contosta, A. R.; Frey, S. D.; Cooper, A. B.
- Ecosphere, Vol. 2, Issue 3
Nitrogen Mineralization and Microbial Biomass Nitrogen Dynamics in Three Alpine Tundra Communities
journal, January 1995
- Fisk, Melany C.; Schmidt, Steven K.
- Soil Science Society of America Journal, Vol. 59, Issue 4
Enhanced root exudation induces microbial feedbacks to N cycling in a pine forest under long-term CO2 fumigation: Rhizosphere feedbacks in CO2-enriched forests
journal, December 2010
- Phillips, Richard P.; Finzi, Adrien C.; Bernhardt, Emily S.
- Ecology Letters, Vol. 14, Issue 2
Impacts of drying–wetting cycles on rhizosphere respiration and soil organic matter decomposition
journal, August 2013
- Zhu, Biao; Cheng, Weixin
- Soil Biology and Biochemistry, Vol. 63
Plant–Soil–Microbial Interactions in a Northern Hardwood Forest
journal, April 2001
- Bohlen, Patrick J.; Groffman, Peter M.; Driscoll, Charles T.
- Ecology, Vol. 82, Issue 4
Changing microbial substrate use in Arctic tundra soils through a freeze-thaw cycle
journal, August 2005
- Schimel, Joshua P.; Mikan, Carl
- Soil Biology and Biochemistry, Vol. 37, Issue 8
Mycorrhizal type determines the magnitude and direction of root-induced changes in decomposition in a temperate forest
journal, January 2015
- Brzostek, Edward R.; Dragoni, Danilo; Brown, Zachary A.
- New Phytologist, Vol. 206, Issue 4
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
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
Tree Species and Mycorrhizal Associations Influence the Magnitude of Rhizosphere Effects
journal, May 2006
- Phillips, Richard P.; Fahey, Timothy J.
- Ecology, Vol. 87, Issue 5
Sources of CO2 efflux from soil and review of partitioning methods
journal, March 2006
- Kuzyakov, Y.
- Soil Biology and Biochemistry, Vol. 38, Issue 3
Fine-root and mycorrhizal traits help explain ecosystem processes and responses to global change
journal, October 2014
- McCormack, M. Luke; Lavely, Emily; Ma, Zeqing
- New Phytologist, Vol. 204, Issue 3
Implications of Sodium mass Balance for Interpreting the Calcium Cycle of a Forested Ecosystem
journal, February 2003
- Bailey, Scott W.; Buso, Donald C.; Likens, Gene E.
- Ecology, Vol. 84, Issue 2
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
Snow cover, freeze-thaw, and the retention of nutrients in an oceanic mountain ecosystem
journal, October 2015
- Wipf, Sonja; Sommerkorn, Martin; Stutter, Marc I.
- Ecosphere, Vol. 6, Issue 10
Rhizosphere processes are quantitatively important components of terrestrial carbon and nutrient cycles
journal, January 2015
- Finzi, Adrien C.; Abramoff, Rose Z.; Spiller, Kimberly S.
- Global Change Biology, Vol. 21, Issue 5
The implications of exoenzyme activity on microbial carbon and nitrogen limitation in soil: a theoretical model
journal, April 2003
- Schimel, J.
- Soil Biology and Biochemistry, Vol. 35, Issue 4
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
Disentangling the mechanisms underlying functional differences among decomposer communities
journal, February 2014
- Keiser, Ashley D.; Keiser, David A.; Strickland, Michael S.
- Journal of Ecology, Vol. 102, Issue 3
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
Leaf mineral nutrition of Arctic plants in response to warming and deeper snow in northern Alaska
journal, April 2005
- Welker, J. M.; Fahnestock, J. T.; Sullivan, P. F.
- Oikos, Vol. 109, Issue 1
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
The Biogeochemistry of Carbon at Hubbard Brook
journal, August 2005
- Fahey, T. J.; Siccama, T. G.; Driscoll, C. T.
- Biogeochemistry, Vol. 75, Issue 1
Synthesis and modeling perspectives of rhizosphere priming
journal, August 2013
- Cheng, Weixin; Parton, William J.; Gonzalez-Meler, Miquel A.
- New Phytologist, Vol. 201, Issue 1
Optimal nitrogen allocation controls tree responses to elevated CO 2
journal, June 2007
- Franklin, Oskar
- New Phytologist, Vol. 174, Issue 4
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
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
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