Skip to main content
Log in

Influence of experimental snow removal on root and canopy physiology of sugar maple trees in a northern hardwood forest

Oecologia Aims and scope Submit manuscript

Abstract

Due to projected increases in winter air temperatures in the northeastern USA over the next 100 years, the snowpack is expected to decrease in depth and duration, thereby increasing soil exposure to freezing air temperatures. To evaluate the potential physiological responses of sugar maple (Acer saccharum Marsh.) to a reduced snowpack, we measured root injury, foliar cation and carbohydrate concentrations, woody shoot carbohydrate levels, and terminal woody shoot lengths of trees in a snow manipulation experiment in New Hampshire, USA. Snow was removed from treatment plots for the first 6 weeks of winter for two consecutive years, resulting in lower soil temperatures to a depth of 50 cm for both winters compared to reference plots with an undisturbed snowpack. Visibly uninjured roots from trees in the snow removal plots had significantly higher (but sub-lethal) levels of relative electrolyte leakage than trees in the reference plots. Foliar calcium: aluminum (Al) molar ratios were significantly lower, and Al concentrations were significantly higher, in trees from snow removal plots than trees from reference plots. Snow removal also reduced terminal shoot growth and increased foliar starch concentrations. Our results are consistent with previous research implicating soil freezing as a cause of soil acidification that leads to soil cation imbalances, but are the first to show that this translates into altered foliar cation pools, and changes in soluble and structural carbon pools in trees. Increased soil freezing due to a reduced snowpack could exacerbate soil cation imbalances already caused by acidic deposition, and have widespread implications for forest health in the northeastern USA.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

References

  • Bailey AS, Hornbeck JW, Campbell JL, Eager C (2003) Hydrometeorological database for hubbard brook experimental forest, 1955–2000. In: General technical report NE305. US Department of Agriculture, Forest Service, Northeastern Research Station, Newtown Square, Pennsylvania

  • Boutin R, Robitaille G (1995) Increased soil nitrate losses under mature sugar maple trees affected by experimentally induced deep frost. Can J For Res 25:588–602

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Calmé S, Bigras FJ, Margolis HA, Hébert C (1994) Frost tolerance and bud dormancy of container-grown yellow birch, red oak and sugar maple seedlings. Tree Physiol 14:1313–1325

    Article  PubMed  Google Scholar 

  • Campbell JL, Ollinger SV, Flerchinger GN, Wicklein H, Hayhoe K, Bailey A (2010) Past and projected future changes in snowpack and soil frost at the hubbard brook experimental forest, New Hampshire, USA. Hyrol Process 24:2465–2480

    Google Scholar 

  • 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 38:82–91

    Article  Google Scholar 

  • Comerford DP (2011) Influence of snow removal on sugar maple physiology and snow and vegetation removal on ground dwelling insects. Master thesis, University of Vermont, Burlington

  • Cronan CS, Grigal DF (1995) Use of calcium/aluminum ratios as indicators of stress in forest ecosystems. J Environ Qual 24:209–226

    Article  CAS  Google Scholar 

  • Decker K, 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 67:1234–1242

    Article  CAS  Google Scholar 

  • Driscoll CT, Lawrence GB, Bulger AJ, Butler TJ, Cronan CS, Eagar C, Lambert KF, Likens GE, Stoddard JL, Weathers KC (2001) Acidic deposition in the northeastern United States: sources and inputs, ecosystem effects, and management strategies. Bioscience 51:180–198

    Article  Google Scholar 

  • Fahey TM, Hughes JW (1994) Fine root dynamics in a northern hardwood forest ecosystem, Hubbard Brook Experimental Forest, NH. J Ecol 82:533–548

    Article  Google Scholar 

  • Federer C (2001) Effects of warming on snow at the Hubbard Brook Experimental Forest. In: Rock B (ed) New England regional assessment group. Preparing for a changing climate: the potential consequences of climate variability and change for New England regional overview. US Global Change Research Program, University of New Hampshire, Durham

  • 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 56:215–238

    Article  CAS  Google Scholar 

  • Fitzhugh RD, Driscoll CT, Groffman PM, Tierney GL, Fahey TJ, Hardy JP (2003) Soil freezing and the acid-base chemistry of soil solutions in a northern hardwood forest. Soil Sci Soc Am J 67:1897–1908

    Article  CAS  Google Scholar 

  • Graveland J, van der Wal R (1996) Decline in snail abundance due to soil acidification causes eggshell defects in forest passerines. Oecologia 105:351–360

    Article  Google Scholar 

  • Graveland J, Van Gijzen T (1994) Arthropods and seeds are not sufficient as calcium sources for shell formation and skeletal growth in passerines. Ardea 82:299–314

    Google Scholar 

  • Groffman PM, Driscoll CT, Fahey TJ, Hardy JP, Fitzhugh RD, Tierney GL (2001) Colder soils in a warmer world: a snow manipulation study in a northern hardwood forest ecosystem. Biogeochemistry 56:135–150

    Article  CAS  Google Scholar 

  • Halman JM, Schaberg PG, Hawley GJ, Eagar C (2008) Calcium addition at the Hubbard Brook Experimental Forest increases sugar storage, antioxidant activity and cold tolerance in native red spruce (Picea rubens). Tree Physiol 28:855–862

    Article  PubMed  CAS  Google Scholar 

  • Halman JM, Schaberg PG, Hawley GJ, Hansen CF (2011) Potential role of soil calcium in recovery of paper birch following ice storm injury in Vermont, USA. For Ecol Manag 261:1539–1545

    Article  Google Scholar 

  • Hendrix DL (1993) Rapid extraction and analysis of nonstructural carbohydrates in plant tissues. Crop Sci 33:1306–1311

    Article  CAS  Google Scholar 

  • Herold A (1980) Regulation of photosynthesis by sink activity-the missing link. New Phytol 86:131–144

    Article  CAS  Google Scholar 

  • Hinesley L, Pharr D, Snelling L, Funderburk S (1992) Foliar raffinose and sucrose in four conifer species: relationship to seasonal temperature. J Am Soc Hortic Sci 117:852–855

    CAS  Google Scholar 

  • Huggett BA, Schaberg PG, Hawley GJ, Eagar C (2007) Long-term calcium addition increases growth release, wound closure, and health of sugar maple (Acer saccharum) trees at the Hubbard Brook Experimental Forest. Can J For Res 37:1692–1700

    Article  CAS  Google Scholar 

  • IPCC (2007) Executive summary of the Intergovernmental Panel on Climate Change. http://www.ipcc.com.ch. Accessed Feb 2007

  • Johnson CE, Driscoll CT, Siccama TG, Likens GE (2000) Element fluxes and landscape position in a northern hardwood forest watershed ecosystem. Ecosystems 3:159–184

    Article  CAS  Google Scholar 

  • Jones J Jr, Case VW, Westerman R (1990) Soil testing and plant analysis. Soil Science Society of America, Madison

    Google Scholar 

  • Kobe RK, Likens GE, Eagar C (2002) Tree seedling growth and mortality responses to manipulations of calcium and aluminum in a northern hardwood forest. Can J For Res 32:954–966

    Article  CAS  Google Scholar 

  • Koricheva J, Larsson S, Haukioja E (1998) Insect performance on experimentally stressed woody plants: a meta-analysis. Annu Rev Entomol 43:195–216

    Article  PubMed  CAS  Google Scholar 

  • Kuhns MR, Stroup WW, Gebre GM (1993) Dehydration tolerance of five bur oak (Quercus macrocarpa) seed sources from Texas, Nebraska, Minnesota, and New York. Can J For Res 23:387–393

    Article  Google Scholar 

  • Likens GE, Driscoll CT, Buso DC (1996) Long-term effects of acid rain: response and recovery of a forest ecosystem. Science 272:244–246

    Article  CAS  Google Scholar 

  • Likens G, Driscoll C, Buso D, Siccama T, Johnson C, Lovett G, Fahey T, Reiners W, Ryan D, Martin C (1998) The biogeochemistry of calcium at Hubbard Brook. Biogeochemistry 41:89–173

    Article  CAS  Google Scholar 

  • Marschner H (2002) Mineral nutrition of higher plants. Academic, San Diego

    Google Scholar 

  • McKay H (1998) Root electrolyte leakage and root growth potential as indicators of spruce and larch establishment. Silva Fenn 32:241–252

    Google Scholar 

  • McLaughlin S (1999) Calcium physiology and its role in terrestrial ecosystem processes. New Phytol 142:211–222

    Article  Google Scholar 

  • Montgomery DC (2008) Design and analysis of experiments. Wiley, New York

    Google Scholar 

  • Morsomme P, Boutry M (2000) The plant plasma membrane H+-ATPase: structure, function and regulation. Biochem Biophys Acta 1464:1–16

    Article  Google Scholar 

  • Ruter JM (1996) High-temperature tolerance of heritage river birch roots decreased by pot-in-pot production systems. Hortic Sci 31:813–814

    Google Scholar 

  • Sakai A, Larcher W (1987) Frost survival of plants. Responses and adaptation to freezing stress. Springer, New York

    Google Scholar 

  • Schaberg PG, DeHayes DH, Hawley GJ (2001) Anthropogenic calcium depletion: a unique threat to forest ecosystem health? Ecosyst Health 7:214–228

    Article  Google Scholar 

  • Schaberg PG, Eagar C, Borer CH, Hawley GJ (2006a) Calcium addition at the Hubbard Brook Experimental Forest reduced winter injury to red spruce in a high-injury year. Can J For Res 36:2544–2549

    Article  Google Scholar 

  • Schaberg PG, Tilley JW, Hawley GJ, DeHayes DH, Bailey SW (2006b) Associations of calcium and aluminum with the growth and health of sugar maple trees in Vermont. For Ecol Manag 223:159–169

    Article  Google Scholar 

  • Schaberg PG, Hennon PE, D’Amore DV, Hawley GJ (2008) Influence of simulated snow cover on the cold tolerance and freezing injury of yellow-cedar seedlings. Glob Change Biol 14:1282–1293

    Article  Google Scholar 

  • Schaberg PG, D’Amore DV, Hennon PE, Halman JM, Hawley GJ (2011) Do limited cold tolerance and shallow depth of roots contribute to yellow-cedar decline? For Ecol Manag 262:2142–2150

    Article  Google Scholar 

  • Schapire AL, Valpuesta V, Botella MA (2009) Plasma membrane repair in plants. Trends Plant Sci 14:645–652

    Article  PubMed  CAS  Google Scholar 

  • Shanley J, Chalmers A (1999) The effect of frozen soil on snowmelt runoff at Sleepers River, Vermont. Hydrol Process 13:1843–1857

    Article  Google Scholar 

  • Stadler D, Wunderli H, Auckenthaler A, Fluehler H, Bruendl M (1996) Measurement of frost-induced snowmelt runoff in a forest soil. Hydrol Process 10:1293–1304

    Article  Google Scholar 

  • Strimbeck GR, Kjellsen TD, Schaberg PG, Murakami PF (2007) Cold in the common garden: comparative low-temperature tolerance of boreal and temperate conifer foliage. Trees 21:557–567

    Article  Google Scholar 

  • Sutinen M, Ritari A, Holappa T, Kujala K (1998) Seasonal changes in soil temperature and in the frost hardiness of Scots pine (Pinus sylvestris) roots under subarctic conditions. Can J For Res 28:946–950

    Article  Google Scholar 

  • 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 Fertility Soils 48:413–424

    Article  Google Scholar 

  • 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 56:175–190

    Article  CAS  Google Scholar 

  • Waisel Y, Eshel A, Kafkafi U (1996) Plant roots: the hidden half. Marcel Dekker, New York

    Google Scholar 

  • Yanai R, Fisk M, Fahey T, Cleavitt N, Park B (2008) Identifying roots of northern hardwood species: patterns with diameter and depth. Can J For Res 38:2862–2869

    Article  Google Scholar 

  • Zwiazek JJ, Blake TJ (1991) Early detection of membrane injury in black spruce (Picea mariana). Can J For Res 21:401–404

    Article  Google Scholar 

Download references

Acknowledgments

The authors are grateful to Justin Brigham, C. J. Freeman, Meghan Gagne, Josh Halman, Chris Hansen, Glenn Harrington, Gary Hawley, Alexandra Kosiba, Chenin Limback, Paula Murakami, Erik Niebylski, Dan Ott, Sarah Pears, Matthew Ross, Bethel Steele, Phil Thompson, Alexandra Webster, Megan Yanney, Will Young, and Helen Yurchenco for their assistance in both the field and laboratory. We thank Alan Howard for assistance with statistical analyses and Drs. Abby van den Berg, David V. D’Amore, Brynne E. Lazarus and Kevin T. Smith for providing helpful feedback on an earlier version of this manuscript. We further thank the staff at the Hubbard Brook Experimental Forest for their generous help in all aspects of our sample collections. This research was supported by funds provided by the Forest Service Northern Research Station, the USDA CSREES McIntire-Stennis Forest Research Program, and the Andrew W. Mellon foundation. This manuscript is a contribution of the Hubbard Brook Ecosystem Study. Hubbard Brook is part of the Long-Term Ecological Research (LTER) network, which is supported by the National Science Foundation. 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

Authors

Corresponding author

Correspondence to Paul G. Schaberg.

Additional information

Communicated by Zoe Cardon.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Comerford, D.P., Schaberg, P.G., Templer, P.H. et al. Influence of experimental snow removal on root and canopy physiology of sugar maple trees in a northern hardwood forest. Oecologia 171, 261–269 (2013). https://doi.org/10.1007/s00442-012-2393-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-012-2393-x

Keywords

Navigation