USDA Forest Service      

George D. Aiken Forestry Sciences Laboratory - Burlington, Vermont

  Biological and Environmental Influences on Forest Health and Productivity
  Ecological Processes: A Basis for Managing Forests and Water Quality in New England
  Integrating Social and Biophysical Sciences for Natural Resource Management
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 George D. Aiken Forestry Sciences Lab                        705 Spear Street  South Burlington, Vermont 05403

(802) 951-6771


 United States Department of Agriculture Forest Service. USDA logo which links to the department's national site. Forest Service logo which links to the agency's national site.

 Current Research

Red Spruce Winter Injury        Calcium Depletion        Genetics            Seasonal Red-Leaf Coloration      Climate Change                        American Chestnut Restoration

Acid rain and red spruce winter injury

Physiology of Red Spruce Winter Injury       

Acid rain has been broadly implicated in the deterioration of forest health, especially the decline of red spruce forests in eastern North America.  We have documented that acid rain leaches calcium (Ca) from foliage, depletes a physiologically important membrane Ca (mCa) pool, destabilizes membranes, and significantly reduces the freezing tolerance of red spruce foliage.  These data support our hypothesis that acid-induced reductions in cold tolerance are mediated through mCa depletion.  This is the only data-supported hypothesis of how acid deposition increases freezing injury in red spruce.  In addition, because Ca serves as a chemical messenger of many environmental stress signals across cell membranes, this hypothesis may also provide a model for understanding how acid rain (and possibly other contributors to environmental Ca depletion) could broadly disrupt plant Ca nutrition and response to a variety of secondary stresses  (e.g., drought, salt, high or variable temperatures, pathogens, etc.) in addition to freezing.

DeHayes, D.H., P.G., Schaberg, G.J. Hawley and G.R. Strimbeck. 1999. Acid rain impacts calcium nutrition and forest health.  BioScience 49:789-800.

Schaberg, P.G., and D.H. DeHayes. 2000. Physiological and Environmental Causes of Freezing Injury in Red Spruce.  2000. Chapter 6 in the Book: Responses of Northern U.S. Forests to Environmental Change.  Eds: R. Mickler, R. Birdsey, and J. Hom.  Springer-Verlag Ecological Studies Series 139, pp 181-227.

Schaberg, P.G., D.H. DeHayes, G.J. Hawley, G.R. Strimbeck, J.R. Cumming, P.F. Murakami, and C.H. Borer. 2000. Acid mist, soil Ca and Al alter the mineral nutrition and physiology of red spruce. Tree Physiology 20:73-85. Abstract.

DeHayes, D.H., P.G. Schaberg and G.R. Strimbeck. 2001. Red spruce cold hardiness and freezing injury susceptibility. Chapter 18. In: Conifer Cold Hardiness. F. Bigras Ed. Kluwer Academic Publishers, Dordrecht, the Netherlands, pp 495-529.

An Unusual Event

During late winter in 2003 winter injury to the current-year foliage of red spruce in Vermont was unusually abundant and widespread.  To assess the severity and extent of this damage, we measured foliar winter injury at 28 locations in Vermont and surrounding states, and bud mortality at a subset of these sites.  Results of this extensive survey revealed that 96% of all trees assessed showed some winter injury, and trees lost an average of 46% of all current-year foliage.  An average of 32% of buds formed in 2002 were killed in association with winter injury.  Both foliar and bud mortality increased with elevation and with crown dominance, and bud mortality increased with greater foliar injury.  Because heavy foliar and bud losses can severely disrupt the carbon economies of trees, the 2003 winter injury event could lead to further spruce decline and mortality, particularly among dominant trees at higher elevations. 

Lazarus, B.E., Schaberg, P.G., DeHayes, D.H., Hawley, G.J. 2004. Severe red spruce winter injury in 2003 creates unusual ecological event in the northeastern United States. Canadian Journal of Forest Research. 34:1784-1788. PDF.

Lazarus, B.E., P.G. Schaberg, G.J. Hawley, and D.H. DeHayes. 2006. Landscape-scale spatial patterns of winter injury to red spruce foliage in a year of heavy region-wide injury. Can. J. For. Res. 36:142-152. PDF.

Related articles

Strimbeck, G.R., P.G. Schaberg, D.H. DeHayes, J.B. Shane and G.J. Hawley.   1995. Midwinter dehardening of montane red spruce during a natural thaw.  Can. J. For. Res. 25:2040-2044. Abstract.

Schaberg, P.G., J.B. Shane, G.J. Hawley, G.R. Strimbeck, D.H. DeHayes, P.F. Cali and J.R. Donnelly. 1996. Physiological changes in red spruce seedlings during a simulated winter thaw. Tree Physiology. 16:567-574. Abstract.

DeHayes, D.H., P.G. Schaberg, G.J. Hawley, C.H. Borer, J.R. Cumming and G.R. Strimbeck. 1997. Physiological implications of seasonal variation in membrane-associated calcium (mCa) in red spruce mesophyll cells.  Tree Physiology. 17:687-695. Abstract.

Borer, C.H., D.H. DeHayes, P.G. Schaberg and J.R. Cumming. 1997. Relative quantification of membrane-associated calcium (mCa) in red spruce mesophyll cells. Trees.  12:21-26.

Schaberg, P.G., G.R. Strimbeck, G.J. Hawley, D.H. DeHayes, J.B. Shane, P.F. Murakami, T.D. Perkins and B.L. Wong. 2000. Cold tolerance and photosystem function in a montane red spruce population: physiological relationships with foliar carbohydrates. Journal of Sustainable Forestry 10:173-180.

Calcium depletion      (return to top)

Other Species?

New research on the broader significance of Ca depletion indicates that the same disruptions documented for red spruce can occur for other tree species (e.g., eastern hemlock, balsam fir, and white pine), and that soil-based Ca manipulation can also alter critical mCa pools.  Considering the unique role Ca plays in the physiological response of cells to environmental stress, we propose that depletion of biological Ca would impair basic stress recognition and response systems, and predispose plants to exaggerated injury following exposure to other environmental stresses.  Diminished stress response would be particularly problematic now because numerous human activities (e.g., pollution production, ozone depletion, climate change, the spread of exotic pests and pathogens, etc.) are simultaneously subjecting forests to an increasing level and diversity of stresses.  Our ongoing work is examining the potential risk of environmental Ca depletion on forest health through a combination of controlled experiments and field surveys.  The potential contribution of Ca depletion to sugar maple decline is a focus of our current work.

Schaberg, P.G., D.H. DeHayes, G.J. Hawley. 2001. Anthropogenic calcium depletion: a unique threat to forest ecosystem health?  Ecosystem Health, 7:214-228. PDF.

Borer, C.H., P.G. Schaberg, D.H. DeHayes, G.J. Hawley. 2001. Physiological implications of anthropogenic environmental calcium depletion. In: The Tree 2000. Isabelle Quentin Ed. IQ Press, Montreal, pp 295-300.

Borer, C.H., Schaberg, P.G. DeHayes, D.H. Hawley, G.J. 2004. Accretion, partitioning and sequestration of calcium and aluminum in red spruce foliage: implications for tree health. Tree Physiology. 24:929-939. PDF.

Borer, C.H., Schaberg P.G., D.H. DeHayes. 2005. Acidic mist reduces foliar membrane-associated calcium and impairs stomatal responsiveness in red spruce. Tree Physiology. 25:673-680. PDF.

Schaberg, P.G., J.W. Tilley, G.J. Hawley, D.H. DeHayes, and S.W. Bailey. 2006. Associations of calcium and aluminum with the growth and health of sugar maple trees in Vermont. Forest Ecology and Management 223:159-169. PDF.


There is growing evidence that various anthropogenic factors (e.g., high acid loading, nitrogen saturation, forest harvesting, changing climatic conditions, soil aluminum (Al) mobilization, and declines in atmospheric base cation deposition) may be responsible for the depletion of Ca from forest ecosystems.  Because Ca is a biologically essential element, anthropogenic alterations of this cation may have serious forest health implications. In particular, because Ca plays an important role in plant defense systems, Ca deficiency could result in inadequate stress response and predispose trees to decline following exposure to even normal stresses including drought, insects, pathogens, and wounding. Our research examines if Ca deficiencies could limit the ability of sugar maple (Acer saccharum Marsh.) trees to respond to wounding. We wounded forest-grown sugar maple trees in a long-term, replicated Ca manipulation study at the Hubbard Brook Experimental Forest in New Hampshire, in which plots received applications of Ca (to boost Ca availability above depleted ambient levels) or Al (to compete with Ca uptake and further reduce Ca availability). We found significantly (P<0.05) greater membrane-associated Ca and total foliar Ca on plots fertilized with Ca in comparison with the Al addition or control plots. By assessing the relative influence of Ca manipulation treatments on specific Ca-dependent wound responses (e.g., the accumulation of lignin, callose, and suberin) as well as the rate of wound closure, the influence of Ca depletion on wound response physiology is being tested. This study is a further examination of the hypothesis that Ca-depletion suppresses stress response systems and predisposes trees to decline.

Nitrogen pollution

Pollutant additions of nitrogen (N) can lead to N-saturation (the accumulation of N in excess of plant and microbial demands).  Numerous published reports have linked N-saturation with forest decline in regions receiving high N inputs, and suggest that decline is associated with N-induced imbalances in other nutrients (especially Ca, Al, and Mg).  However, the physiological mechanisms through which nutrient imbalances may cause decline have not been determined.  Our survey of tree physiology within montane plots receiving long-term N additions showed that fertilization resulted in reductions of foliar Ca concentrations to near-deficiency levels, and significantly increased foliar respiration.  N additions also increased foliar winter injury.  Our research assessed if N-induced disruptions in physiology are mediated through reductions in mCa.  This work showed that the same mechanism of physiological disruption found for acid rain impairment (significant reductions in mCa, membrane stability, cold tolerance, and an increased rate of freezing injury) also applies to chronic N additions.  These findings suggest that N additions can contribute to the same reduction of biological Ca reserves that acid rain depletes.

Schaberg, P.G., T.D. Perkins and S.G. McNulty. 1997. Effects of chronic low-level N additions on foliar elemental concentrations, morphology, and gas exchange of mature montane red spruce. Can. J. For. Res. 27:1622-1629. PDF.

Perkins, T.D., S.T. Adams, G.T. Lawson, P.G. Schaberg and S.G. McNulty. 2000. Long-term nitrogen fertilization increases winter injury in montane red spruce foliage (Picea rubens) foliage. Journal of Sustainable Forestry 10:165-172.

Schaberg, P.G., D.H. DeHayes, G.J. Hawley, P.F. Murakami, G.R. Strimbeck, S.G. McNulty. 2002. Effects of chronic N fertilization on foliar membranes, cold tolerance, and carbon storage in montane red spruce.  Canadian Journal of Forest Research. 32:1351-1359. Abstract.

Genetics     (return to top)

Genetic diversity is essential to the long-term health and survival of biological populations because this diversity helps provide the adaptive capacity needed to survive natural and manmade environmental change.  A loss of genetic diversity could be a serious threat to the long-term health and productivity of forest ecosystems.  Silvicultural harvesting represents one anthropogenic force in which sometimes large numbers of trees and the genes they contain are removed from forest systems.  However, the long-term impact of tree removals on the genetic base and ecological resiliency of forests is largely unknown.


Eastern hemlock

In one study we examined the influence of long-term silvicultural treatment on the genetic base of an eastern hemlock forest.  This study showed that protracted silvicultural selection altered the frequency of rare alleles (unusual gene forms) in treated populations.  Silvicultural selection that preferentially removed larger and better-formed trees reduced the presence of rare alleles compared to the control, whereas silvicultural selection that preferentially removed small and poorly formed trees increased the presence of rare alleles relative to control.


DeHayes, D.H., G.L., Jacobson, P.G. Schaberg, B. Bongarten, L. Iverson, and A.C. Diefenbacher-Krall.  2000. Forest responses to changing climate: lessons from the past and uncertainty for the future. Chapter 14 in the Book: Responses of Northern U.S. Forests to Environmental Change.  Eds: R. Mickler R. Birdsey, and J. Hom. Springer-Verlag Ecological Studies Series 139, pp 495-540.


Hawley, G., D.H. DeHayes, P.G. Schaberg, J. Brissette. 2006. Genetic effects of diameter-limit cutting. In: Kenefic, Laura S., Nyland, Ralph D. eds. Proceedings of the conference on diameter-limit cutting in northeastern forests.; 2005 May 23-24; Amherst, MA. Gen. Tech. Rep. NE-341. Newtown Square, PA: U.S. Forest Service: 41-42. Northeastern Research Station. PDF.


Hawley, G.J., Schaberg P.G., DeHayes, D.H., Brissette, J. 2005. Silviculture alters the genetic structure of an eastern hemlock forest in Maine, USA.  Canadian Journal of Forest Research, 35:143-150. PDF.


White pine

We also established a unique second study: a genetically mapped white pine forest that combines basic inventory data (e.g., the size, growth, health and location of trees) with an assessment of tree genetics (isozyme analysis) within a GIS database.  This database was used to conduct simulated harvests that “removed” individual trees based on traditional management criteria (e.g., tree size, crown class, etc.) and then calculated the consequence of tree removals on the genetics of the residual stand.  Because different simulation runs utilized different removal criteria, we were able to compare the impact of many varying management options on forest genetics without actually cutting any trees.  Results of initial simulated harvests indicated that most management prescriptions had little impact on the genetics of the residual stand.  A noted exception was that some harvests preferentially altered the frequency of rare alleles. 


Nijensohn, S.E., Schaberg, P.G., Hawley, G.J., DeHayes, D.H. 2005. Genetic subpopulation structuring and its implications in a mature eastern white pine stand. Canadian Journal of Forest Research, Can. J. For. Res. 35:1041-1052. PDF.


Schaberg, P.G., Hawley, G.J., DeHayes, D.H., Nijensohn, S.E. 2004. Silvicultural management and the manipulation of rare alleles.  In Silviculture and the Conservation of Genetic Resources for Sustainable Forest Management. J. Beaulieu Ed. Natural Resources Canada, Canadian Forest Service, Information Report LAU-X-128, p67-74.


Results form simulated harvests support findings from our field-based hemlock study and suggest that rare alleles may be particularly prone to manipulation through harvesting.  In addition to its unique research value, a genetically mapped forest could be an important demonstration site at which forest managers could literally visualize (on field-based computers) the impact of management prescriptions (applied using simulated cuts) on a parameter that they traditionally can’t evaluate: the forest’s genetic base.  Studies of the influence of silvicultural selection on forest genetics will help assess if harvesting prescriptions have the potential to enhance or diminish genetic diversity within populations.  This information could also help in the formulation of silvicultural guidelines that protect or possibly increase within-species genetic diversity.


Seasonal red coloration    (return to top)

Anthocyanins are red, blue or purple pigments most often seen in flowers and fruits.  Although the biochemistry and physiology of chlorophylls, foliar green pigments, are well understood, less is known about anthocyanins and their role in leaves.  Much of the research conducted on this red pigment originates in the economical significance of controlling flower and fruit color.  And recently, its role in human health as an antioxidant or scavenger of reactive oxygen species is currently being studied as a possible cancer-defense mechanism.  Is it possible that anthocyanins could perform a similar function in trees?  Indeed, many factors are known to elicit anthocyanin biosynthesis in foliage including UV-B radiation, osmotic stress, drought, low temperature, nutrient deficiency, wounding, pathogen infection and ozone exposure. Because formation of anthocyanins requires energy, it is believed that they must be of some benefit to tree health. In fact, recent work on woody species has emphasized the potential value of anthocyanins as a “light screen” that protects the photosynthetic apparatus of senescing leaves and enables prolonged nutrient absorption before abscission. It is also possible that anthocyanins may increase both cold hardiness and drought resistance.

Still, the specific function of anthocyanin and how it may relate to overall tree and forest health is unclear.  Our research team is currently in the process of identifying the factors that stimulate anthocyanin biosynthesis.  We hope to gain a detailed understanding of the linkage between stress exposure and anthocyanin production which may provide insight into plant stress response systems, and help assess the utility of leaf color analysis as an indicator of stress. 

Computer-based Leaf Color Analysis

As part of this research, our research group developed a computer-based image analysis technique for quantifying red leaf color without the use of costly or complicated laboratory analyses.

Murakami, P.F., M.R. Turner, A.K. van den Berg, and Paul Schaberg. 2006. An instructional guide for leaf color analysis using digital imaging software. Gen Tech. Rep. NE-327. Newtown Square, PA: U.S. Department of Agriculture, Forest Service, Northeastern Research Station. 33 p. PDF.

Red Coloration and Nitrogen/Carbohydrates

Initial work on this topic examined the environmental and chemical factors range of parameters for mature sugar maple trees throughout the growing season and autumn, only foliar nitrogen (N), sugar and starch concentrations were significantly correlated with red coloration.  We hypothesize that nutrient (particularly N) limitations in our trees provided the biochemical triggers (low N and high sugar signals), energy, and carbohydrate building blocks needed for the facultative production of anthocyanins.  Experimental manipulations are now being conducted to test this hypothesis and other possible connections between anthocyanin expression and stress response.

van den Berg, A.K., J.R. Donnelly, P.F. Murakami, P.G. Schaberg. 2001. Development of fall foliage color in sugar maple. In: The Tree 2000. Isabelle Quentin Ed. IQ Press, Montreal, pp 356-360.

Schaberg, P.G., A.K. van den Berg, P.F. Murakami, J.B. Shane, J.R. Donnelly. 2003. Factors influencing red expression in the autumn foliage of sugar maple trees. Tree Physiology. 23:325-333. PDF.

 Spring vs. Fall Red Coloration

Current research is focusing on spring coloration of leaves and the function of this pigment may differ at this time of year compared to autumn.  Our preliminary findings suggest that, like our initial autumn study, leaves with low N concentrations tend to exhibit more red.  In addition, it appears that spring red leaf coloration can occur in many species (e.g., American beech and Eastern cottonwood) that normally do not produce anthocyanins during autumn.  Why would a species manufacture anthocyanins in the spring but not the fall? Do anthocyanins perform different functions during these times?  Do different environmental signals trigger red color development in the spring versus the fall?  Answers to these and other questions are needed to decipher the ecological function and potential benefits of anthocyanin production.

Abscission Layer Formation

To relate color development and nutrient/carbohydrate concentration to abscission layer formation we collected petioles of green, yellow and red leaves and measured abscission layer length.  We also determined the strength of the abscission layer by adding weights to each leaf and recording the weight necessary to detach individual leaves from branches.  Nutrient and carbohydrate analyses were also performed.  Abscission layers in petioles of yellow leaves were more completely formed than those of green and red leaves.  Yellow leaves were also more easily detached from branches, followed by red and then green leaves.  Leaves are now being processed for N content.  Preliminary data indicate a negative relationship between N and red coloration: less N, more red.

 Anthocyanin and Antioxidants

We have begun exciting new research studying the role of anthocyanins and other plant antioxidants in protecting leaves from dangerous forms of oxygen called reactive oxygen species (ROS).  ROS occur when a plant is under stress and can quickly damage foliar tissue if not eliminated.  Anthocyanins may be one of several plant compounds that eliminate this toxic oxygen and prevent significant foliar damage.  Our research team is developing laboratory methods to measure antioxidant enzyme activity.  With this new application we hope to better define the role of anthocyanins in plant stress response systems.

 Climate change   (return to top)

Yellow-cedar in Alaska

Yellow-cedar is an economically and ecologically important species that has experienced a dramatic decline in southeastern Alaska during the past 100 years.  Extensive research has shown that this decline has no likely biotic cause, but suggests that one or more abiotic factors (particularly climatic warming) may have instigated decline.  To evaluate the possibility that inadequate cold hardiness is a contributor to this decline, scientists from the Pacific Northwest Station and our research team measured the foliar freezing tolerance of yellow-cedar trees in declining and non-declining stands.  Foliar freezing tolerance of western hemlock, a sympatric species not experiencing unusual mortality, was measured for comparison.  Freezing tolerance was assessed in the fall, winter and spring to determine if seasonal differences in hardiness help explain species-specific injury.  Two results consistent with field reports of yellow-cedar decline were found: 1) because yellow-cedar trees experienced greater vernal dehardening, yellow-cedar trees were uniquely vulnerable to spring freezing injury, and 2) stands below 130 m appeared more vulnerable to freezing injury than stands above 130 m.  These results support the possibility that limited foliar cold hardiness during spring contributes to the decline of yellow-cedar trees at low elevations.  However, we are now evaluating whether root freezing tolerance may be more directly pertinent to decline in the field.

Schaberg, P.G., P.E. Hennon, D.V. D'Amore, G.J. Hawley, and C.H. Borer. 2005. Seasonal differences in freezing tolerance of yellow-cedar and western hemlock trees at a site affected by yellow-cedar decline. Can. J. For. Res. 35:2065-2070. PDF.

Winter photosynthesis

The energy relations of evergreen conifers during winter have been studied little despite their potential importance to understanding yearly energy budgets and plant adaptations to the cold.  Red spruce and other evergreens retain their foliage throughout the winter, thus they have the potential for year-round carbon assimilation.  Field measurements of photosynthesis have shown that winter carbon assimilation can be significant in regions where winter climates are mild.  However, studies in colder areas have been limited and inconsistent in their portrayal of photosynthetic ability during winter.  In fact, the most prevalent data documents disruptions of the photosynthetic machinery within cells that would limit winter carbon capture. Although questions concerning winter carbon exchange exist for all northern conifers, information about the photosynthetic activity of red spruce is of particular interest.  Since the 1960’s, growth rates of red spruce in New England and New York have measurably declined.  Freezing injury and the associated loss of needles have been identified as a major contributor to this decline.  Understanding the physiological activity of red spruce needles during winter would improve scientific understanding of this species’ ecological niche, and help assess potential mechanisms of red spruce decline.

To better evaluate the winter physiology of red spruce, I studied the winter carbon relations of red spruce.   My research documented that red spruce have rates of net photosynthesis close to zero for much of the winter, but that photosynthetic rates more than tripled during protracted thaws, with rates for some trees approximated growing season levels.  Additional work verified that increases in field photosynthesis can occur within four days of thaw inception, whereas increases in photosynthetic capacity (maximum photosynthetic rates measured under near-optimal, controlled growing conditions) can occur within 48h (natural thaw) or even 3h (simulated thaw).  Winter photosynthesis could benefit leaves by augmenting energy stores when more distal carbon reserves are less available due to cold-induced reductions in phloem transport.  Increased sugar concentrations could also help foliage maintain cold tolerance levels needed to avoid freezing injury.

Schaberg, P.G., R.C. Wilkinson, J.B. Shane, J.R. Donnelly, and P.F. Cali. 1995. Winter photosynthesis of red spruce from three Vermont seed sources. Tree Physiology. 15:345-350. Abstract.

Schaberg, P.G., J.B. Shane, J.R. Donnelly, P.F. Cali, and G.R. Strimbeck. 1998. Photosynthetic capacity of red spruce during winter. Tree Physiology. 18:271-276. Abstract.

Schaberg, P.G., M.C. Snyder, J.B. Shane, and J.R. Donnelly. 2000. Seasonal patterns of carbohydrate reserves in red spruce seedlings. Tree Physiology. 20:549-555. Abstract.

American Chestnut Restoration   (return to top)

The American chestnut is a tree species of unique ecologic and economic value that was virtually eliminated following a blight caused by the fungal pathogen, Cryphonectria parasitica (Murr.) Barr, that was accidentally introduced in New York City in 1904.  In order to restore this valuable species, multiple approaches to decrease the virulence of the pathogen or increase the resistance of the tree have been evaluated.  However, only one technique - producing highly resistant trees via the hybridization of American and Chinese chestnuts with backcrosses to American chestnut - shows promise for near-term restoration.  The American Chestnut Foundation (TACF) is leading this hybridization/backcrossing effort.  Our research team, in collaboration with TACF scientists, has initiated new research to support the restoration of American chestnut in Vermont and elsewhere in the Northern Forest.  We are currently evaluating the role that inadequate cold hardiness may play in limiting the success of the species at its northern limit.  In addition, we are providing hybrid/backcrossed chestnut with germplasm from Vermont-adapted American chestnut, and testing techniques for cultivating American chestnut under Vermont conditions.

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