Oecologia

, Volume 171, Issue 1, pp 261–269 | Cite as

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

  • Daniel P. Comerford
  • Paul G. Schaberg
  • Pamela H. Templer
  • Anne M. Socci
  • John L. Campbell
  • Kimberly F. Wallin
Global change ecology - Original research

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.

Keywords

Soil freezing Root injury Woody shoot growth Carbohydrate and cation concentrations Acer saccharum 

References

  1. 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, PennsylvaniaGoogle Scholar
  2. Boutin R, Robitaille G (1995) Increased soil nitrate losses under mature sugar maple trees affected by experimentally induced deep frost. Can J For Res 25:588–602CrossRefGoogle Scholar
  3. Brown PJ, DeGaetano AT (2011) A paradox of cooling winter soil surface temperatures in a warming northeastern United States. Agric For Meteorol 151:947–956CrossRefGoogle Scholar
  4. 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 14:1313–1325PubMedCrossRefGoogle Scholar
  5. 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 24:2465–2480Google Scholar
  6. 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 38:82–91CrossRefGoogle Scholar
  7. 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, BurlingtonGoogle Scholar
  8. Cronan CS, Grigal DF (1995) Use of calcium/aluminum ratios as indicators of stress in forest ecosystems. J Environ Qual 24:209–226CrossRefGoogle Scholar
  9. 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 67:1234–1242CrossRefGoogle Scholar
  10. 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 51:180–198CrossRefGoogle Scholar
  11. Fahey TM, Hughes JW (1994) Fine root dynamics in a northern hardwood forest ecosystem, Hubbard Brook Experimental Forest, NH. J Ecol 82:533–548CrossRefGoogle Scholar
  12. 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, DurhamGoogle Scholar
  13. 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 56:215–238CrossRefGoogle Scholar
  14. 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 67:1897–1908CrossRefGoogle Scholar
  15. Graveland J, van der Wal R (1996) Decline in snail abundance due to soil acidification causes eggshell defects in forest passerines. Oecologia 105:351–360CrossRefGoogle Scholar
  16. Graveland J, Van Gijzen T (1994) Arthropods and seeds are not sufficient as calcium sources for shell formation and skeletal growth in passerines. Ardea 82:299–314Google Scholar
  17. 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 56:135–150CrossRefGoogle Scholar
  18. 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 28:855–862PubMedCrossRefGoogle Scholar
  19. 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 261:1539–1545CrossRefGoogle Scholar
  20. Hendrix DL (1993) Rapid extraction and analysis of nonstructural carbohydrates in plant tissues. Crop Sci 33:1306–1311CrossRefGoogle Scholar
  21. Herold A (1980) Regulation of photosynthesis by sink activity-the missing link. New Phytol 86:131–144CrossRefGoogle Scholar
  22. 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 117:852–855Google Scholar
  23. 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 37:1692–1700CrossRefGoogle Scholar
  24. IPCC (2007) Executive summary of the Intergovernmental Panel on Climate Change. http://www.ipcc.com.ch. Accessed Feb 2007
  25. Johnson CE, Driscoll CT, Siccama TG, Likens GE (2000) Element fluxes and landscape position in a northern hardwood forest watershed ecosystem. Ecosystems 3:159–184CrossRefGoogle Scholar
  26. Jones J Jr, Case VW, Westerman R (1990) Soil testing and plant analysis. Soil Science Society of America, MadisonGoogle Scholar
  27. 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 32:954–966CrossRefGoogle Scholar
  28. Koricheva J, Larsson S, Haukioja E (1998) Insect performance on experimentally stressed woody plants: a meta-analysis. Annu Rev Entomol 43:195–216PubMedCrossRefGoogle Scholar
  29. 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 23:387–393CrossRefGoogle Scholar
  30. Likens GE, Driscoll CT, Buso DC (1996) Long-term effects of acid rain: response and recovery of a forest ecosystem. Science 272:244–246CrossRefGoogle Scholar
  31. 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 41:89–173CrossRefGoogle Scholar
  32. Marschner H (2002) Mineral nutrition of higher plants. Academic, San DiegoGoogle Scholar
  33. McKay H (1998) Root electrolyte leakage and root growth potential as indicators of spruce and larch establishment. Silva Fenn 32:241–252Google Scholar
  34. McLaughlin S (1999) Calcium physiology and its role in terrestrial ecosystem processes. New Phytol 142:211–222CrossRefGoogle Scholar
  35. Montgomery DC (2008) Design and analysis of experiments. Wiley, New YorkGoogle Scholar
  36. Morsomme P, Boutry M (2000) The plant plasma membrane H+-ATPase: structure, function and regulation. Biochem Biophys Acta 1464:1–16CrossRefGoogle Scholar
  37. Ruter JM (1996) High-temperature tolerance of heritage river birch roots decreased by pot-in-pot production systems. Hortic Sci 31:813–814Google Scholar
  38. Sakai A, Larcher W (1987) Frost survival of plants. Responses and adaptation to freezing stress. Springer, New YorkGoogle Scholar
  39. Schaberg PG, DeHayes DH, Hawley GJ (2001) Anthropogenic calcium depletion: a unique threat to forest ecosystem health? Ecosyst Health 7:214–228CrossRefGoogle Scholar
  40. 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 36:2544–2549CrossRefGoogle Scholar
  41. 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 223:159–169CrossRefGoogle Scholar
  42. 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 14:1282–1293CrossRefGoogle Scholar
  43. 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 262:2142–2150CrossRefGoogle Scholar
  44. Schapire AL, Valpuesta V, Botella MA (2009) Plasma membrane repair in plants. Trends Plant Sci 14:645–652PubMedCrossRefGoogle Scholar
  45. Shanley J, Chalmers A (1999) The effect of frozen soil on snowmelt runoff at Sleepers River, Vermont. Hydrol Process 13:1843–1857CrossRefGoogle Scholar
  46. Stadler D, Wunderli H, Auckenthaler A, Fluehler H, Bruendl M (1996) Measurement of frost-induced snowmelt runoff in a forest soil. Hydrol Process 10:1293–1304CrossRefGoogle Scholar
  47. 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 21:557–567CrossRefGoogle Scholar
  48. 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 28:946–950CrossRefGoogle Scholar
  49. 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 48:413–424CrossRefGoogle Scholar
  50. 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 56:175–190CrossRefGoogle Scholar
  51. Waisel Y, Eshel A, Kafkafi U (1996) Plant roots: the hidden half. Marcel Dekker, New YorkGoogle Scholar
  52. 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 38:2862–2869CrossRefGoogle Scholar
  53. Zwiazek JJ, Blake TJ (1991) Early detection of membrane injury in black spruce (Picea mariana). Can J For Res 21:401–404CrossRefGoogle Scholar

Copyright information

© Springer-Verlag (outside the USA) 2012

Authors and Affiliations

  • Daniel P. Comerford
    • 1
  • Paul G. Schaberg
    • 2
  • Pamela H. Templer
    • 3
  • Anne M. Socci
    • 3
  • John L. Campbell
    • 4
  • Kimberly F. Wallin
    • 1
    • 2
  1. 1.Rubenstein School of Environment and Natural ResourcesUniversity of VermontBurlingtonUSA
  2. 2.Northern Research Station Forest Service, US Department of AgricultureSouth BurlingtonUSA
  3. 3.Department of BiologyBoston UniversityBostonUSA
  4. 4.Northern Research StationForest Service, US Department of AgricultureDurhamUSA

Personalised recommendations