Abstract
Northern forest ecosystems are projected to experience warmer growing seasons and increased soil freeze–thaw cycles in winter over the next century. Past studies show that warmer soils in the growing season enhance nitrogen uptake by plants, while soil freezing in winter reduces plant uptake and ecosystem retention of nitrogen, yet the combined effects of these changes on plant root capacity to take up nitrogen are unknown. We conducted a 2-year (2014–2015) experiment at Hubbard Brook Experimental Forest in New Hampshire, USA to characterize the response of root damage, nitrogen uptake capacity, and soil solution nitrogen to growing season warming combined with soil freeze–thaw cycles in winter. Winter freeze–thaw cycles damaged roots, reduced nitrogen uptake capacity by 42%, and increased soil solution ammonium in the early growing season (May–June). During the peak growing season (July), root nitrogen uptake capacity was reduced 40% by warming alone and 49% by warming combined with freeze–thaw cycles. These results indicate the projected combination of colder soils in winter and warmer soils in the snow-free season will alter root function by reducing root nitrogen uptake capacity and lead to transient increases of nitrogen in soil solution during the early growing season, with the potential to alter root competition for soil nitrogen and seasonal patterns of soil nitrogen availability. We conclude that considering interactive effects of changes in climate during winter and the snow-free season is essential for accurate determination of the response of nitrogen cycling in the northern hardwood forest to climate change.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Averill C, Finzi A (2011) Increasing plant use of organic nitrogen with elevation is reflected in nitrogen uptake rates and ecosystem delta15N. Ecology 92:883–891
Bai E, Li S, Xu W et al (2013) A meta-analysis of experimental warming effects on terrestrial nitrogen pools and dynamics. New Phytol 199:441–451. https://doi.org/10.1111/nph.12252
Bailey AS, Hornbeck JW, Campbell JL, Eagar C (2003) Hydrometeorological database for Hubbard brook experimental forest: 1955–2000. US Department of Agriculture, Forest Service, Northeastern Research Station, Newtown Square
Bardgett RD, Mommer L, De Vries FT (2014) Going underground: root traits as drivers of ecosystem processes. Trends Ecol Evol 29:692–699. https://doi.org/10.1016/j.tree.2014.10.006
BassiriRad H (2000) Kinetics of nutrient uptake by roots: responses to global change. New Phytol 147:155–169
BassiriRad H (2015) Consequences of atmospheric nitrogen deposition in terrestrial ecosystems: old questions, new perspectives. Oecologia 177:1–3. https://doi.org/10.1007/s00442-014-3116-2
BassiriRad H, Thomas RB, Reynolds JF, Strain BR (1996) Differential responses of root uptake kinetics of NH4+ and NO3− to enriched atmospheric CO2 concentration in field-grown loblolly pine. Plant Cell Environ 19:367–371
Binkley D (1984) Ion exchange resin bags: factors affecting estimates of nitrogen availability. Soil Sci Soc Am J 48:1181–1184. https://doi.org/10.2136/sssaj1984.03615995004800050046x
Brown PJ, DeGaetano AT (2011) A paradox of cooling winter soil surface temperatures in a warming northeastern United States. Agric For Meteorol 151:947–956
Burakowski EA, Wake CP, Braswell B, Brown DP (2008) Trends in wintertime climate in the northeastern United States: 1965–2005. J Geophys Res Atmos 113:1–12. https://doi.org/10.1029/2008JD009870
Butler SM, Melillo JM, Johnson JE et al (2012) Soil warming alters nitrogen cycling in a New England forest: implications for ecosystem function and structure. Oecologia 168:819–828. https://doi.org/10.1007/s00442-011-2133-7
Campbell JL, Ollinger SV, Flerchinger GN et al (2010) Past and projected future changes in snowpack and soil frost at the Hubbard Brook Experimental Forest, New Hampshire, USA. Hydrol Process 24:2465–2480. https://doi.org/10.1002/hyp.7666
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
Clarkson D, Hopper M, Jones L (1986) The effect of root temperature on the uptake of nitrogen and the relative size of the root system in Lolium perenne. I. Solutions containing both NH4+ and NO3−. Plant Cell Environ 9:535–545. https://doi.org/10.1111/j.1365-3040.1986.tb01585.x
Cleavitt NL, Fahey TJ, Groffman PM et al (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
Comerford DP, Schaberg PG, Templer PH et al (2013) Influence of experimental snow removal on root and canopy physiology of sugar maple trees in a northern hardwood forest. Oecologia 171:261–269. https://doi.org/10.1007/s00442-012-2393-x
Contosta AR, Adolph A, Burchsted D et al (2016) A longer vernal window: the role of winter coldness and snowpack in driving spring transitions and lags. Glob Change Biol 23:1610–1625. https://doi.org/10.1111/gcb.13517
Decker KLM, Wang D, Waite C, Scherbatskoy T (2003) Snow removal and ambient air temperature effects on forest soil temperatures in Northern Vermont. Soil Sci Soc Am J 67:1234. https://doi.org/10.2136/sssaj2003.1234
Dijkstra FA, Cheng W (2008) Increased soil moisture content increases plant N uptake and the abundance of 15N in plant biomass. Plant Soil 302:263–271. https://doi.org/10.1007/s11104-007-9477-0
Doane TA, Horwáth WR (2003) Spectrophotometric determination of nitrate with a single reagent. Anal Lett 36:2713–2722. https://doi.org/10.1081/AL-120024647
Durán J, Morse JL, Groffman PM et al (2016) Climate change decreases nitrogen pools and mineralization rates in northern hardwood forests. Ecosphere 7:e01251. https://doi.org/10.1002/ecs2.1251
Epstein E, Schmid WE, Rains DW (1963) Significance and technique of short-term experiments on solute absorption by plant tissue. Plant Cell Physiol 4:79–84
Finzi AC, Berthrong ST (2005) The uptake of amino acids by microbes and trees in three cold-temperate forests. Ecology 86:3345–3353. https://doi.org/10.1890/04-1460
Fitzhugh R, Driscoll C, Groffman PM, Tierney G (2001) Effects of soil freezing disturbance on soil solution nitrogen, phosphorus, and carbon chemistry in a northern hardwood ecosystem. Biogeochemistry 56:215–238
Gallet-Budynek A, Brzostek E, Rodgers VL et al (2009) Intact amino acid uptake by northern hardwood and conifer trees. Oecologia 160:129–138. https://doi.org/10.1007/s00442-009-1284-2
Gessler A, Schneider S, Von Sengbusch D et al (1998) Field and laboratory experiments on net uptake of nitrate and ammonium by the roots of spruce (Picea abies) and beech (Fagus sylvatica) trees. New Phytol 138:275–285. https://doi.org/10.1046/j.1469-8137.1998.00107.x
Glass AD (1989) Plant mineral nutrition. An introduction to current concepts. Jones and Bartlett Publishers Inc., Burlington
Groffman PM, Rustad LE, Templer PH et al (2012) Long-term integrated studies show complex and surprising effects of climate change in the northern hardwood forest. Bioscience 62:1056–1066. https://doi.org/10.1525/bio.2012.62.12.7
Hardy JP, Groffman PM, Fitzhugh RD et al (2001) Snow depth manipulation and its influence on soil frost and water dynamics in a northern hardwood forest. Biogeochemistry 56:151–174
Hayhoe K, Wake CP, Huntington TG et al (2007) Past and future changes in climate and hydrological indicators in the US Northeast. Clim Dyn 28:381–407. https://doi.org/10.1007/s00382-006-0187-8
Henry HAL (2008) Climate change and soil freezing dynamics: historical trends and projected changes. Clim Change 87:421–434. https://doi.org/10.1007/s10584-007-9322-8
Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biom J 50:346–363
Kuzyakov Y, Xu X (2013) Competition between roots and microorganisms for nitrogen: mechanisms and ecological relevance. New Phytol 198:656–669. https://doi.org/10.1111/nph.12235
Leffler AJ, James JJ, Monaco TA (2013) Temperature and functional traits influence differences in nitrogen uptake capacity between native and invasive grasses. Oecologia 171:51–60. https://doi.org/10.1007/s00442-012-2399-4
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
Likens GE (2013) Biogeochemistry of a forested ecosystem. Springer, New York
Lucash MS, Eissenstat DM, Joslin JD et al (2007) Estimating nutrient uptake by mature tree roots under field conditions: challenges and opportunities. Trees 21:593–603. https://doi.org/10.1007/s00468-007-0160-0
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
McCormack ML, Lavely E, Ma Z (2014) Fine-root and mycorrhizal traits help explain ecosystem processes and responses to global change. New Phytol 204:455–458. https://doi.org/10.1111/nph.13023
Näsholm T, Kielland K, Ganeteg U (2009) Uptake of organic nitrogen by plants. New Phytol 182:31–48
Pilon CE, Cote B, Fyles JW (1994) Effect of snow removal on leaf water potential, soil moisture, leaf and soil nutrient status and leaf peroxidase activity of sugar maple. Plant Soil 162:81–88. https://doi.org/10.1007/BF01416092
Pinheiro J, Bates D, DebRoy S, et al (2016) nlme: linear and nonlinear mixed effects models. In: R packag, version 3.1-128
Pourmokhtarian A, Driscoll CT, Campbell JL, Hayhoe K, Stoner AMK (2016) The effects of climate downscaling technique and observational data set on modeled ecological responses. Ecol Appl 26:1321–1337
R Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing. Vienna. http://www.R-project.org/
Rennenberg H, Dannenmann M (2015) Nitrogen nutrition of trees in temperate forests-the significance of nitrogen availability in the pedosphere and atmosphere. Forests 6:2820–2835. https://doi.org/10.3390/f6082820
Rennenberg H, Dannenmann M, Gessler A et al (2009) Nitrogen balance in forest soils: nutritional limitation of plants under climate change stresses. Plant Biol 11:4–23. https://doi.org/10.1111/j.1438-8677.2009.00241.x
Ricard J, Tobiasson W, Greatorex A (1976) The field assembled frost gage. Technical Note. Cold Regions Research and Engineering Laboratory
Rustad LE, Campbell JL, Marion GM et al (2001) A meta-analysis of the response of soil respiration, net nitrogen mineralization, and aboveground plant growth to experimental ecosystem warming. Oecologia 126:543–562. https://doi.org/10.1007/s004420000544
Sanders-DeMott R, Templer PH (2017) What about winter? Integrating the missing season into climate change experiments in seasonally snow covered ecosystems. Methods Ecol Evol 8:1183–1191. https://doi.org/10.1111/2041-210X.12780
Schaberg P, Hennon P, D’amore D, Hawley G (2008) Influence of simulated snow cover on the cold tolerance and freezing injury of yellow-cedar seedlings. Glob Change Biol 14:1–12. https://doi.org/10.1111/j.1365-2486.2008.01577.x
Sims GK, Ellsworth TR, Mulvaney RL (1995) Microscale determination of inorganic nitrogen in water and soil extracts. Commun Soil Sci Plant Anal 26:303–316. https://doi.org/10.1080/00103629509369298
Smerdon JE, Pollack HN, Cermak V et al (2004) Air-ground temperature coupling and subsurface propagation of annual temperature signals. J Geophys Res D 109:1–10. https://doi.org/10.1029/2004JD005056
Smithwick EAH, Eissenstat DM, Lovett GM et al (2013) Root stress and nitrogen deposition: consequences and research priorities. New Phytol 197:712–719. https://doi.org/10.1111/nph.12081
Smithwick EAH, Lucash MS, McCormack ML, Sivandran G (2014) Improving the representation of roots in terrestrial models. Ecol Model 291:193–204. https://doi.org/10.1016/j.ecolmodel.2014.07.023
Socci AM, Templer PH (2011) Temporal patterns of inorganic nitrogen uptake by mature sugar maple (Acer saccharum Marsh.) and red spruce (Picea rubens Sarg.) trees using two common approaches. Plant Ecol Diver 4:141–152
Sorensen PO, Templer PH, Finzi AC (2016) 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 M-A, Reinmann AB, Sanders-DeMott R, Templer PH (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
Templer PH, Lovett GM, Weathers KC et al (2005) Influence of tree species on forest nitrogen retention in the Catskill Mountains, New York, USA. Ecosystems 8:1–16. https://doi.org/10.1007/s10021-004-0230-8
Templer PH, Reinmann AB, Sanders-DeMott R et al (2017) Climate change across seasons experiment (CCASE): a new method for simulating future climate in seasonally snow-covered ecosystems. PLoS ONE 12:e0171928. https://doi.org/10.1371/journal.pone.0171928
Tierney GL, Fahey TJ, Groffman PM et al (2001) Soil freezing alters fine root dynamics in a northern hardwood forest. Biogeochemistry 56:175–190. https://doi.org/10.1023/A:1013072519889
VanCleve K, Oechel WC, Hom JL (1990) Response of black spruce (Piceamariana) ecosystems to soil temperature modification in interior Alaska. Can J For Res 20:1530–1535. https://doi.org/10.1017/CBO9781107415324.004
Vitousek PM, Reiners WA (1975) Ecosystem succession and nutrient retention: a hypothesis. Bioscience 25:376–381. https://doi.org/10.2307/1297148
Warren CR (2009) Why does temperature affect relative uptake rates of nitrate, ammonium and glycine: a test with Eucalyptus pauciflora. Soil Biol Biochem 41:778–784. https://doi.org/10.1016/j.soilbio.2009.01.012
Winter TC, Buso DC, Shattuck PC et al (2008) The effect of terrace geology on ground-water movement and on the interaction of ground water and surface water on a mountainside near Mirror Lake, New Hampshire, USA. Hydrol Process 22:21–32. https://doi.org/10.1002/hyp.6593
Acknowledgements
We thank Frank Bowles, Stephanie Juice, Jamie Harrison, Laura Sofen, and Amy Werner for their contributions to the establishment and execution of the CCASE experiment. The staff at Hubbard Brook, including Ian Halm, Nick Grant, Mary Martin, Tammy Wooster, Scott Bailey, and Amey Bailey provided assistance with site establishment, data collection and data management. Annie Socci provided expertise on root N uptake methodology. Marc-Andre Giasson, Bob Michener, Risa McNellis, Jenny McEldoon, Lindsay Crockett, Julianna Webber, Ana Castillo, Savan Shah, Maroua Jabouri, Mary Farina, Scott Loranger, Anna Ta, Andrea Staudler, and Steve Decina provided field and/or lab assistance. John Campbell and three anonymous reviewers provided feedback on an earlier version of this manuscript. This research was supported by a National Science Foundation (NSF) Long Term Ecological Research (LTER) Grant to Hubbard Brook (NSF 1114804) and a NSF CAREER Grant to PHT (NSF DEB1149929). RSD was supported by NSF DGE0947950, a Boston University (BU) Department of Biology Dean’s Fellowship, and the BU Program in Biogeoscience. This manuscript is a contribution of the Hubbard Brook Ecosystem Study. Hubbard Brook is part of the LTER network, which is supported by the NSF. The Hubbard Brook Experimental Forest is operated and maintained by the USDA Forest Service, Northern Research Station, Newtown Square, PA.
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible Editor: Sasha C. Reed.
Rights and permissions
About this article
Cite this article
Sanders-DeMott, R., Sorensen, P.O., Reinmann, A.B. et al. Growing season warming and winter freeze–thaw cycles reduce root nitrogen uptake capacity and increase soil solution nitrogen in a northern forest ecosystem. Biogeochemistry 137, 337–349 (2018). https://doi.org/10.1007/s10533-018-0422-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10533-018-0422-5