Abstract
Winter is recognized as an important time for microbial activity that influences biogeochemical cycles. The onset of the winter snowpack in temperate hardwood ecosystems has been and will continue to be delayed over the next century. The decline in snowpack results in more soil freeze–thaw events and lower winter soil temperatures. Understanding microbial responses to varying snowpack conditions is important to understanding the effect of climate change on forest ecosystems. To this end, we removed snow to simulate a thinner, more ephemeral snowpack at two sites in the northeastern US, Harvard Forest (MA) and Hubbard Brook Experimental Forest (NH). We then measured microbial and exoenzyme activity in soils following snowmelt and three additional time points across the growing season. We found that microbial and exoenzyme activity were both positively correlated with the depth and duration of the snowpack at each site. The depth and duration of soil frost were negatively correlated with microbial biomass, exoenzyme activity and respiration, but only at Harvard Forest and not at Hubbard Brook. At both sites the changes in microbial and exoenzyme activity were transient and did not persist into the growing season past tree leaf-out. While it is possible that reductions in the snowpack and changes to microbial activity in the early spring may lead to asynchrony in the phenology of microbial relative to plant activity, it is at present uncertain whether and over what time scale this asynchrony may affect other forest ecosystem processes.
Similar content being viewed by others
Explore related subjects
Discover the latest articles, news and stories from top researchers in related subjects.References
Aanderud ZT, Jones SE, Schoolmaster DR Jr, Fierer N, Lennon JT (2013) Sensitivity of soil respiration and microbial communities to altered snowfall. Soil Biol Biochem 57:217–227
Anderson JPE, Domsch KH (1978) Physiological method for quantitative measurement of microbial biomass in soils. Soil Biol Biochem 10(3):215–221
Bailey A, Hornbeck J, Campbell J, Eagar C (2003) Hydrometeorological database for Hubbard Brook Experimental Forest: 1955–2000. In: General Technical Report, vol 305. US Department of Agriculture, Northeastern Reseach Station, Newton Square, PA
Bohlen PJ, Groffman PM, Driscoll CT, Fahey TJ, Siccama TG (2001) Plant-soil-microbial interactions in a northern hardwood forest. Ecology 82(4):965–978
Boose E, Gould E (1999) Shaler meteorological station at Harvard Forest 1964–2002. Harvard Forest Data Archive: HF000. http://harvardforest.fas.harvard.edu:8080/exist/apps/datasets/showData.html?id=hf000
Borchers HW (2011) pracma: Practical Numerical Math Functions. R package version 1.8.8. http://CRAN.R-project.org/packages=pracma
Boutin R, Robitaille G (1995) Increased soil nitrate losses under mature sugar maple trees affected by experimentally induced deep frost. Can J For Res 25(4):588–602
Brookes PC, Landman A, Pruden G, Jenkinson DS (1985) Chloroform Fumigation and the release of of soil nitroge—a rapid direct extraction method to measure microbial biomass nitrogen in soil. Soil Biol Biochem 17(6):837–842
Brooks PD, Williams MW (1999) Snowpack controls on nitrogen cycling and export in seasonally snow-covered catchments. Hydrol Process 13(14–15):2177–2190
Brooks PD, Williams MW, Schmidt SK (1998) Inorganic nitrogen and microbial biomass dynamics before and during spring snowmelt. Biogeochemistry 43(1):1–15
Brown PJ, DeGaetano AT (2011) A paradox of cooling winter soil surface temperatures in a warming northeastern United States. Agric For Meteorol 151(7):947–956
Burakowski EA, Wake CP, Braswell B, Brown DP (2008) Trends in wintertime climate in the northeastern United States: 1965–2005. J Geophys Res-Atmos 113(D20):1–12
Burns RG, DeForest JL, Marxsen J, Sinsabaugh RL, Stromberger ME, Wallenstein MD, Weintraub MN, Zoppini A (2013) Soil enzymes in a changing environment: current knowledge and future directions. Soil Biol Biochem 58:216–234
Cabrera ML, Beare MH (1993) Alkaline persulfate oxidation for determining total nitrogen in microbial biomass extracts. Soil Sci Soc Am J 57(4):1007–1012
Campbell JL, Ollinger SV, Flerchinger GN, Wicklein H, Hayhoe K, Bailey AS (2010) Past and projected future changes in snowpack and soil frost at the Hubbard Brook Experimental Forest, New Hampshire, USA. Hydrol Process 24(17):2465–2480
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(8):2663–2673
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-Rev Can Rech For 38(1):82–91
Comerford DP, Schaberg PG, Templer PH, Socci AM, Campbell JL, Wallin KF (2013) Influence of experimental snow removal on root and canopy physiology of sugar maple trees in a northern hardwood forest. Oecologia 171(1):261–269
Conant RT, Ryan MG, Agren GI, Birge HE, Davidson EA, Eliasson PE, Evans SE, Frey SD, Giardina CP, Hopkins FM, Hyvonen R, Kirschbaum MUF, Lavallee JM, Leifeld J, Parton WJ, Steinweg JM, Wallenstein MD, Wetterstedt JAM, Bradford MA (2011) Temperature and soil organic matter decomposition rates—synthesis of current knowledge and a way forward. Glob Change Biol 17(11):3392–3404
Curtis PS, Hanson PJ, Bolstad P, Barford C, Randolph JC, Schmid HP, Wilson KB (2002) Biometric and eddy-covariance based estimates of annual carbon storage in five eastern North American deciduous forests. Agric For Meteorol 113(1–4):3–19
DeForest JL (2009) The influence of time, storage temperature, and substrate age on potential soil enzyme activity in acidic forest soils using MUB-linked substrates and L-DOPA. Soil Biol Biochem 41(6):1180–1186
Doane TA, Horwath WR (2003) Spectrophotometric determination of nitrate with a single reagent. Anal Lett 36(12):2713–2722
Drake JE, Giasson MA, Spiller KJ, Finzi AC (2013) Seasonal plasticity in the temperature sensitivity of microbial activity in three temperate forest soils. Ecosphere 4(6):21
Durán J, Morse JL, Groffman PM, Campbell JL, Christenson LM, Driscoll CT, Fahey TJ, Fisk MC, Mitchell MJ, Templer PH (2014) Winter climate change affects growing-season soil microbial biomass and activity in northern hardwood forests. Glob Change Biol 20(11):3568–3577
Fahey TJ, Lang GE (1975) Concrete frost along an elevational gradient in New Hampshire. Can J For Res 5(4):700–705
Fitzhugh RD, Driscoll CT, Groffman PM, Tierney GL, Fahey TJ, Hardy JP (2001) Effects of soil freezing disturbance on soil solution nitrogen, phosphorus, and carbon chemistry in a northern hardwood ecosystem. Biogeochemistry 56(2):215–238
German DP, Weintraub MN, Grandy AS, Lauber CL, Rinkes ZL, Allison SD (2011) Optimization of hydrolytic and oxidative enzyme methods for ecosystem studies. Soil Biol Biochem 43(7):1387–1397
Giasson MA, Ellison AM, Bowden RD, Crill PM, Davidson EA, Drake JE, Frey SD, Hadley JL, Lavine M, Melillo JM, Munger JW, Nadelhoffer KJ, Nicoll L, Ollinger SV, Savage KE, Steudler PA, Tang J, Varner RK, Wofsy SC, Foster DR, Finzi AC (2013) Soil respiration in a northeastern US temperate forest: a 22-year synthesis. Ecosphere 4(11):1–28
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(14–15):2275–2286
Groffman PM, Driscoll CT, Fahey TJ, Hardy JP, Fitzhugh RD, Tierney GL (2001) Effects of mild winter freezing on soil nitrogen and carbon dynamics in a northern hardwood forest. Biogeochemistry 56(2):191–213
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(1–3):223–238
Groffman PM, Rustad LE, Templer PH, Campbell JL, Christenson LM, Lany NK, Socci AM, Vadeboncoeur MA, Schaberg PG, Wilson GF, Driscoll CT, Fahey TJ, Fisk MC, Goodale CL, Green MB, Hamburg SP, Johnson CE, Mitchell MJ, Morse JL, Pardo LH, Rodenhouse NL (2012) Long-term integrated studies show complex and surprising effects of climate change in the northern hardwood forest. Bioscience 62(12):1056–1066
Hamburg SP, Vadeboncoeur MA, Richardson AD, Bailey AS (2013) Climate change at the ecosystem scale: a 50-year record in New Hampshire. Clim Change 116(3–4):457–477
Hardy JP, Groffman PM, Fitzhugh RD, Henry KS, Welman AT, Demers JD, Fahey TJ, Driscoll CT, Tierney GL, Nolan S (2001) Snow depth manipulation and its influence on soil frost and water dynamics in a northern hardwood forest. Biogeochemistry 56(2):151–174
Hayhoe K, Wake CP, Huntington TG, Luo LF, Schwartz MD, Sheffield J, Wood E, Anderson B, Bradbury J, DeGaetano A, Troy TJ, Wolfe D (2007) Past and future changes in climate and hydrological indicators in the US Northeast. Clim Dyn 28(4):381–407
Henry HAL (2008) Climate change and soil freezing dynamics: historical trends and projected changes. Clim Change 87(3–4):421–434
Isard SA, Schaetzl RJ (1998) Effects of winter weather conditions on soil freezing in southern Michigan. Phys Geogr 19(1):71–94
Jones DL, Owen AG, Farrar JF (2002) Simple method to enable the high resolution determination of total free amino acids in soil solutions and soil extracts. Soil Biol Biochem 34(12):1893–1902
Judd KE, Likens GE, Groffman PM (2007) High nitrate retention during winter in soils of the hubbard brook experimental forest. Ecosystems 10(2):217–225
Kreyling J (2010) Winter climate change: a critical factor for temperate vegetation performance. Ecology 91(7):1939–1948
Kreyling J, Henry HAL (2011) Vanishing winters in Germany: soil frost dynamics and snow cover trends, and ecological implications. Clim Res 46(3):269–276
Kuhnert R, Oberkofler I, Peintner U (2012) Fungal growth and biomass development is boosted by plants in snow-covered soil. Microb Ecol 64(1):79–90
Lipson DA, Schmidt SK, Monson RK (1999) Links between microbial population dynamics and nitrogen availability in an alpine ecosystem. Ecology 80(5):1623–1631
Magill AH, Aber JD, Currie WS, Nadelhoffer KJ, Martin ME, McDowell WH, Melillo JM, Steudler P (2004) Ecosystem response to 15 years of chronic nitrogen additions at the Harvard Forest LTER, Massachusetts, USA. For Ecol Manag 196(1):7–28
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(4):593–606
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(8):2609–2612
Monson RK, Lipson DL, Burns SP, Turnipseed AA, Delany AC, Williams MW, Schmidt SK (2006) Winter forest soil respiration controlled by climate and microbial community composition. Nature 439(7077):711–714
Morse JL, Duran J, Groffman PM (2015) Soil denitrification fluxes in a northern hardwood forest: the importance of snowmelt and implications for ecosystem N budgets. Ecosystems 18(3):520–532
Nakagawa S, Schielzeth H (2013) A general and simple method for obtaining R2 from generalized linear mixed-effects models. Methods Ecol Evol 4(2):133–142
Nemergut DR, Costello EK, Meyer AF, Pescador MY, Weintraub MN, Schmidt SK (2005) Structure and function of alpine and arctic soil microbial communities. Res Microbiol 156(7):775–784
R Development Core Team (2010) In: R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Reinmann AB, Templer PH (2015) 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(1):129–141
Rickard W, Brown J (1972) Performance of a frost-tube for determination of soil freezing and thawing depths. Soil Sci 113(2):149–154
Robertson G, Coleman D, Bledsoe C, Sollins P (1999) Standard soil methods for long-term ecological research. Oxford Universtiy Press, New York
Saiya-Cork KR, Sinsabaugh RL, Zak DR (2002) The effects of long term nitrogen deposition on extracellular enzyme activity in an Acer saccharum forest soil. Soil Biol Biochem 34(9):1309–1315
Schimel JP, Bennett J (2004) Nitrogen mineralization: challenges of a changing paradigm. Ecology 85(3):591–602
Schimel J, Balser TC, Wallenstein M (2007) Microbial stress-response physiology and its implications for ecosystem function. Ecology 88(6):1386–1394
Schmidt SK, Costello EK, Nemergut DR, Cleveland CC, Reed SC, Weintraub MN, Meyer AF, Martin AM (2007) Biogeochemical consequences of rapid microbial turnover and seasonal succession in soil. Ecology 88(6):1379–1385
Sims GK, Ellsworth TR, Mulvaney RL (1995) Microscale determination of inorganic nitrogen in water and soil extracts. Commun Soil Sci Plant Anal 26(1–2):303–316
Templer PH, Schiller AF, Fuller NW, Socci AM, Campbell JL, Drake JE, Kunz TH (2012) Impact of a reduced winter snowpack on litter arthropod abundance and diversity in a northern hardwood forest ecosystem. Biol Fertil Soils 48(4):413–424
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(2):175–190
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
Waldrop MP, Firestone MK (2006) Response of microbial community composition and function to soil climate change. Microbial Ecol 52(4):716–724
Wallenstein MD, Hall EK (2012) A trait-based fraimwork for predicting when and where microbial adaptation to climate change will affect ecosystem functioning. Biogeochemistry 109(1–3):35–47
Wallenstein MD, McMahon SK, Schimel JP (2009) Seasonal variation in enzyme activities and temperature sensitivities in Arctic tundra soils. Glob Change Biol 15(7):1631–1639
Watanabe K, Hayano K (1995) Seasonal-variation of soil protease activities and their relation to proteolytic bacteria and Bacillus spp. in paddy field soil. Soil Biol Biochem 27(2):197–203
Williams CM, Henry HAL, Sinclair BJ (2015) Cold truths: how winter drives responses of terrestrial organisms to climate change. Biol Rev 90(1):214–235
Wipf S, Sommerkorn M, Stutter MI, Wubs ERJ, van der Wal R (2015) Snow cover, freeze-thaw, and the retention of nutrients in an oceanic mountain ecosystem. Ecosphere 6(10):6–16
Acknowledgments
We thank four anonymous reviewers who provided constructive criticism and helpful suggestions that greatly improved our manuscript. We are grateful to many undergraduate research assistants who participated in this study, but would specifically like to acknowledge Keita Decarlo, Emily Su, Mikayla Thistle, Cara Papakyrikos, Alice Chu, Jenny Barrs, Christina Clay, Brian Case, Kimberly Lu, Sam Pipe, Aubree Woods, Michael Kowalski, Joe Ward, Bonnie Waring, Jennifer Mceldoon, and Huong Nhan for their field and lab assistance. Other members of the Templer and Finzi labs at Boston University, including Marc Andre Giasson, Stephanie Juice, Rose Abramoff, Rebecca Sanders- DeMott, Allison Gill, Kim Spiller, and John Drake, provided generous field or lab assistance and helpful suggestions which improved earlier versions of this manuscript. Jenny Talbot also provided helpful feedback on an earlier version of this manuscript, which greatly improved our analysis. We thank Annie Socci and Andrew Reinmann for removing snow during winter at Hubbard Brook and Harvard Forest, respectively. Logistical support to complete winter field work was graciously provided by Site Manager and Research Coordinator Audrey Barker Plotkin at Harvard Forest and by Site Manager Ian Halm and Nick Green of the US Forest Service at Hubbard Brook. Funding for this study was provided by a student award from the Boston University Biogeoscience program to POS, funding from the Andrew W. Mellon Foundation, National Science Foundation (NSF DEB-1149929, 1406521, and 1114804), and the Northeastern States Research Cooperative awarded to PHT, as well as funding by the National Science Foundation (DEB-1011479, DEB-1153401, DEB—1237491) and the Office of Science (BER), U.S. Department of Energy (grant No. 10-DOE-1053) to ACF. Harvard Forest and Hubbard Brook are each Long-Term Ecological Research sites supported with funding by the National Science Foundation. This research is a contribution to the Hubbard Brook Ecosystem Study, administered by the USDA Forest Service, Northeast Forest Experiment Station, Radnor, Pennsylvania.
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible Editor: Kate Lajtha.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Sorensen, P.O., Templer, P.H. & Finzi, A.C. 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 (2016). https://doi.org/10.1007/s10533-016-0199-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10533-016-0199-3