Growing season warming and winter freeze–thaw cycles reduce root nitrogen uptake capacity and increase soil solution nitrogen in a northern forest ecosystem
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.
KeywordsClimate change Hubbard Brook Experimental Forest Soil warming Soil freezing Snow removal Nitrogen cycling Root damage
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.
- 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 CrossRefGoogle Scholar
- 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 Google Scholar
- Glass AD (1989) Plant mineral nutrition. An introduction to current concepts. Jones and Bartlett Publishers Inc., BurlingtonGoogle Scholar
- Pinheiro J, Bates D, DebRoy S, et al (2016) nlme: linear and nonlinear mixed effects models. In: R packag, version 3.1-128Google Scholar
- R Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing. Vienna. http://www.R-project.org/
- Ricard J, Tobiasson W, Greatorex A (1976) The field assembled frost gage. Technical Note. Cold Regions Research and Engineering LaboratoryGoogle Scholar
- 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 CrossRefGoogle Scholar