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EXPLORING INTERACTIONS BETWEEN POLLUTANT EMISSIONSAND CLIMATIC VARIABILITY IN GROWTH OF RED SPRUCE

IN THE GREAT SMOKY MOUNTAINS NATIONAL PARK

K. L. WEBSTER1, I. F. CREED1,2,∗ , N. S. NICHOLAS3 and H. VAN MIEGROET4

1Department of Biology, The University of Western Ontario, London, Ontario, N6A 5B7, Canada;2Department of Geography, The University of Western Ontario, London, Ontario, N6A 5C2,

Canada; 3Public Power Institute, Tennessee Valley Authority, Norris, Tennessee, 37828, U.S.A.;4Department of Forest, Range, and Wildlife Sciences, Utah State University, Logan, UT,

84322-5230, U.S.A.( ∗author for correspondence,e-mail: [email protected])

(Received 19 December 2003; accepted 09 June 2004)

Abstract. Concern exists as to the status of red spruce (Picea rubens Sarg.) in the Great SmokyMountains, with evidence both for and against an unprecedented decline in radial growth duringthe past century. On the basis of a dendrological record from 1850 to 1998, our analyses sup-port a decline in radial growth starting as early as the 1940s through to the 1970s; in the 1970sthere was a reversal of this decline. In comparing trees near ridges (2000 m) with those in draws(1500 m), we found differences in the (a) timing of the decline, (b) rate of decline, and (c) ho-mogeneity of the decline, with trees near ridges showing earlier, faster, and more homogeneousdeclines than trees in draws. We hypothesized that changes in climatic conditions and/or atmo-spheric pollutants, both of which changed beyond ranges of natural variability, were related to theobserved decline in radial growth. In trees near ridges, up to 67.1% of changes in radial growthcould be explained by a combination of climatic conditions (7.6%) and annual emissions of nitricoxides (NOx) and sulfur dioxide (SO2) (an additional 59.5%). In trees from draws, up to 38.3%of the changes in radial growth could be explained by climatic conditions only. A conceptualmodel is presented, where trees in naturally acidic soils with low base saturation provide a sen-sitive signal for the changing nature of acidic pollutants, but trees in anthropogenically acidifyingsoils with an initially higher baser saturation provide a signal that is confounded by a transient in-crease of calcium (Ca) and magnesium (Mg) in the soil that results in a transient increase in radialgrowth.

Keywords: climate change, dendrology, elevation gradient, Great Smoky Mountains, growth decline,nitric oxides, red spruce, sulfur dioxide, tree rings

1. Introduction

Red spruce (Picea rubens Sarg.) is a major component of the montane ecosystemin the Appalachian and Adirondack Mountains (White and Cogbill, 1992). Thisecosystem spans from large continuous areas in the northern Appalachian andAdirondacks, to smaller, disjunct populations at high elevation in the Allegheny andsouthern Appalachians. Reductions in the radial growth rates of red spruce were

Water, Air, and Soil Pollution 159: 225–248, 2004.C© 2004 Kluwer Academic Publishers. Printed in the Netherlands.

226 K. L. WEBSTER ET AL.

observed throughout its range from about the 1950s to the 1990s, when the studiesended (e.g., Johnson and Siccama, 1983; Adams et al., 1985; Hornbeck and Smith,1985; McLaughlin et al., 1985, 1987; Cook and Zedaker, 1992). These reductionshave raised public and scientific concern that these changes are indicative of anecosystem under stress and that reduced radial growth rates in red spruce may bean early indication of more broadly based changes in the structure and functioningof the ecosystem (Johnson et al., 1992).

The red spruce-Fraser fir (Abies fraseri (Pursh) Poir.) forest of the eastern UShas been exposed to exponential increases in anthropogenic emissions of green-house gases and acidic pollutants over the past century, receiving among the highestloads of atmospheric pollutants in the country (EPA, 2000). Emissions of green-house gases (carbon dioxide, methane, nitrous oxide, and chlorofluorocarbons)implicated in climate change and acidic pollutants [nitric oxides (NOx) and sul-fur dioxide (SO2)] implicated in acidification of terrestrial and aquatic systemsare relatively recent stresses to this montane ecosystem. Climate change and acid-ification may add additional stress to isolated populations of red spruce at theedge of their range, such as those populations existing in the Great Smoky Moun-tains in the southern Appalachians (Peart et al., 1992; Nicholas et al., 1999). Thestress of acidic pollutants, particularly SO2, may have been partially alleviatedsince legislation and implementation of the Clean Air Act (1970, with furtheramendments in 1977 and 1990), resulting in a significant reduction in SO2 emis-sions (EPA, 2000). In contrast, the possible stress of greenhouse gases remains aconcern.

Dendrochronological studies of red spruce in the Adirondacks and northernAppalachians concluded that there was an unprecedented regional decline in ra-dial growth of red spruce within the region from the 1960’s through to the1980’s, when these studies ended (e.g., McLaughlin et al., 1987). In the south-ern Appalachians, a similar conclusion was not made, as some studies sup-ported an unprecedented regional decline in radial growth of red spruce (e.g.,McLaughlin et al., 1987) while others did not (e.g., LeBlanc et al., 1992; Reamset al., 1993). In the southern Appalachians, radial growth of red spruce treesshowed periods of significant increase and decrease throughout the history of thetrees.

Dendroclimatological studies conducted throughout the range of red spruce inthe Appalachians found that anomalously warm late summer temperatures had anegative effect on radial growth and anomalously warm early winter temperatureshad a positive effect on radial growth of red spruce possible explaining the changesin radial growth during the past century (e.g., Cook et al., 1987; Cook, 1988; Cookand Johnson, 1989; McLaughlin et al., 1987). In the southern Appalachians, thenature of the relationships between red spruce growth and both temperature andprecipitation was more complex. Prior to the 1950s, warm late summer tempera-tures had a negative effect and summer precipitations had a positive effect on radial

RED SPRUCE GROWTH DECLINE IN THE GREAT SMOKY MOUNTAINS 227

growth. After the 1950s, summer temperatures had a positive effect and summerprecipitations had a negative effect on radial growth (McLaughlin et al., 1998).However, the recent declines in radial growth that occurred in both the northernand southern Appalachians were greater than what was predicted by relationshipsbetween climate and radial growth (McLaughlin et al., 1987, 1998) suggest a fun-damental change in environmental conditions (e.g., climate change or atmosphericpollutants) contributed to the declines.

Dendrochemical studies conducted throughout the range of red spruce in theAdirondacks and the Appalachians indicated an anomalous increase in the con-centrations of calcium (Ca) and magnesium (Mg) in the wood around the 1950srelative to radial increments formed prior to and after the 1950s which coincidedwith an anomalous increase in radial growth (Bondietti et al., 1990; Shortle andSmith, 1988; Shortle et al., 1997). Several mechanisms have been considered toexplain these observed changes in wood chemistry. The first mechanism proposes alimitation in the supply of base cations in the soils. In soils with moderate base satu-ration, accelerated mobilization of exchangeable cations may produce a temporarypulse of readily available cations (e.g., Ca and Mg) for roots to absorb. However, ifcation-stripping rates proceed in excess of cation-weathering rates, either naturallydue to soil forming processes typical of conifer forests or anthropogenically due toadditions of strong acid anions to the soil, base saturation declines causing prefer-ential displacement of exchangeable acidity from the soil over that of exchangeablebases (Reuss and Johnson, 1986). The difference in soil chemistry between alreadyacid soils and those that become progressively acidified may be reflected in the sig-nal of an enrichment of cation concentrations followed by depletion in the wood.The second mechanism proposes an inhibition of cation uptake by aluminum (Al),especially in acid soils with low base saturation and high exchangeable acidity.Because of its higher charge, Al has a greater binding potential that may preventthe uptake of cations with lesser charge (McLaughlin and Wimmer, 1999). Preven-tion of uptake of cations by Al blockage would contribute to a decline in cationconcentrations in the wood.

The majority of dendrochronological studies on red spruce decline in the south-ern Appalachians occurred more than 15 yr ago, at which time a trend of declinein the southern Appalachians was emerging. In this study, we used dendrochrono-logical techniques on red spruce in the Great Smoky Mountains of the southernAppalachians to determine whether: 1) an updated time series establishes whetheror not the decline in radial growth that started in the middle of the 20th centuryreached unprecedented levels in terms of the mean and/or standard deviation ofradial growth; 2) radial growth is related to climate and/or atmospheric pollutants;3) the sensitivity of radial growth to climate and/or atmospheric pollutants varieswithin the elevation at which the ecosystem exists; and 4) the chemistry of the radialincrements provides insight into the causes of changes in radial growth during thepast century.


2. Methods

2.1. STUDY AREA

The study consisted of an analysis of stands at the extents of the virgin red spruce-Fraser fir forest of the Great Smoky Mountains National Park (GSMNP), locatedin the southern Appalachians, U.S.A. (Figure 1).

The Great Smoky Mountains have a cool, temperate rainforest climate (Shanks,1954). Over the past century, the meteorological record indicates that the meanannual air temperature was 8.5 ◦C, ranging from 7.2 to 9.7 ◦C, and the total annualprecipitation averaged 222 cm, ranging from 165 to 294 cm (Figure 2). From1910 to 1980, there appears to have been an oscillation from wet/warm to dry/coolconditions on a cycle of about 30 yr. In contrast, in the 1980s, this oscillation ends,with a shift to dry/warm conditions from about 1980 to 1985, wet/cool conditionsfrom 1985 to 1996, and dry/warm conditions from 1996 to the end of the time series(Figure 2).

The Great Smoky Mountains are part of a mature mountain range formed dur-ing the late Paleozoic era. The mountains are characterized by rounded summitsand ridges that drain into rugged slopes that have been uniformly eroded throughfluvial and colluvial processes. The underlying bedrock is metamorphosed sedi-mentary rock (Whittaker, 1956). Soils developed from these rocks are silt to sandyloam in texture and have large contents of organic matter at the surface of the

Figure 1. Location of the Great Smoky Mountains National Park.


Figure 2. A time series from 1910 to 1998 of total annual precipitation and average annual temper-ature. The 1974–1998 data were based on meteorological records at Newfound Gap. The remainingdata were interpolated from other climate stations in the GSMNP (i.e., Clingman’s Dome, Mount LeConte, the Oconoluftee Visitor Center, and the Sugarlands Visitor Center Park Headquarters) for the1935–1974 period or the climate station at the Knoxville airport for the 1910–1935 period.

soil, small concentrations of exchangeable base cations (e.g., Ca), and high ex-changeable acidity (i.e., low base saturation) (e.g., Joslin et al., 1992; Johnson andLindberg, 1992). The dominant forest species follows an elevation gradient withred spruce dominating at lower elevations (1370–1675 m), Fraser fir dominatingat higher elevations (>1890 m), and both species co-dominating at mid elevations(1675–1890 m) (Cain, 1935; Oosting and Billings, 1951; Whittaker, 1956; Nicholaset al., 1992). The red spruce-Fraser fir stands in the Great Smoky Mountains areamong the last of the old-growth stands in the southern Appalachians.

The red spruce-Fraser fir forest has been impacted by several environmentalstresses. One stress is the infestation of Fraser fir by the balsam woolly adelgid(Adelges piceae Ratz.). This exotic pest was first detected in the southern Ap-palachians in 1957 in the Black Mountains (Speers, 1958) and spread to the GreatSmoky Mountains in 1962 (Ciesla et al., 1963), causing extensive Fraser fir mor-tality (Pauley and Clebsch, 1990; Nicholas et al., 1992; Smith and Nicholas, 1998,2000). Another stress is the presence of acidic pollutants in the atmosphere. Duringthe past century, emissions of acidic pollutants have changed dramatically (Fig-ure 3). Prior to the 1940s, total annual emissions of NOx and SO2 showed relativelysmall increases. In the 1940s, the total annual emissions of NOx and SO2 showed aminor increase that was transient due primarily to changes in SO2 emissions. Since


Figure 3. A time series from 1910 to 1998 of US annual emissions of NOx, SO2, and NOx + SO2.The 1910–1940 data were interpolated based on a regression model between GSMNP and US annualemissions of NOx + SO2 for the period 1940 to 1980 (r 2 = 0.926, p < 0.001). Original data were notavailable for 1940–1980 for the GSMNP (i.e., they were based on Bondietti et al., 1989). Furthermore,no data were available for 1980 - 1998 for the GSMNP. Therefore, US annual emissions of NOx +SO2 formed the basis of this study.

the 1950s, total annual emissions of NOx and SO2 showed a major increase until1973. Since then, there has been a consistent reduction in emissions of SO2,whileemissions of NOx have shown a continued increase, albeit at a much smaller rate,with some stabilization (Figure 3).

2.2. DENDROCHRONOLOGICAL METHODS

To conduct the dendrological analyses of red spruce, we collected tree cores from redspruce that existed at the extents of its elevation range in the GSMNP (Figure 4). Treecores were collected from the 20×20 m permanent plots established by the NationalAcid Precipitation Assessment Program (NAPAP) Forest Response Program in theGSMNP (Nicholas et al., 1992; Zedaker and Nicholas, 1990) (Figure 4). Individualtrees were selected based on the criteria that a sample tree must be: 1) alive; 2) >5cm diameter at breast height; 3) in a dominant or co-dominant canopy position; and4) >100 yr of age. These criteria were used to maximize the length of the recordand to minimize the effects of competition and/or suppression within the stands onradial growth dynamics. A final criterion was that there be a minimum of 30 treesfrom each of the low elevation (∼1500 m) and high elevation (∼2000 m) extentsof the geographic range of red spruce.


Figure 4. Location of the National Acid Precipitation Assessment Program (NAPAP) plots withinthe Great Smoky Mountains National Park that were sampled.

A chronology of annual ring widths was produced for each tree. Individual treechronologies were standardized to remove systematic changes in ring width dueto growth by fitting a predicted negative exponential, negative linear, or constantrate function to the chronology of annual ring widths and dividing each measuredring width value by the value expected by the growth curve. The standardizedchronologies were represented as an index of ring width with a mean value ofone. Standardized chronologies of subsamples of trees were combined to obtaina mean chronology for the tree, and similarly, standardized chronologies of treeswere combined to obtain a mean chronology for the plot or the elevation. A total of37 trees found at plots at elevations from 1478 to 1548 m were used to define thestandardized chronology for low elevation, and a total of 35 trees found at plots atelevations from 1911 to 2000 m were used to define the standardized chronologyfor high elevation. The strength of the signal of the mean standardized chronologieswas assessed using the expressed population signal (EPS). The EPS is expressedin terms of the mean inter-series correlation coefficient and is an estimate of theuncertainty in the average value of a set of correlated time series (Wigley et al.,1984). EPS ranges from 0 to 1, with a standard acceptable threshold value of 0.85


(Wigley et al., 1984), below which results should be interpreted with caution. Wefocused our dendrochronological analyses on data from 1850 to 1998, the periodduring which the EPS statistic was generally above 0.85 and therefore adequate tocapture the signal of the mean standardized chronologies.

Chronologies of Ca and Mg concentrations in the radial increments were pro-duced for each of a high and low elevation tree. Cores were separated into 20-yrsegments prior to 1935 and 10-yr segments after 1935 and each segment was ana-lyzed for Ca and Mg using a Perkin Elmer Elan 6000 inductively coupled plasmamass spectrometer.

2.3. STATISTICAL ANALYSES

All statistical analyses were performed using Sigma Stat (SPSS, 1997). Statisticalanalyses were conducted to explore relationships between environmental factorsand radial growth. Pearson correlation coefficient matrices were computed to de-termine if there was co-linearity among the environmental factors both for theperiod of record (1910–1998), and for the period during which there were signifi-cant increases in annual emissions of NOx and SO2 (1940–1998). Linear regressionmodels were derived to predict changes in the standardized mean chronologies forthe high and low elevations as a function of the environmental factors for the sametime periods. Prior to the regression analyses, data were tested for the assumptionsof normality, constant variance, and independence of residuals.

3. Results and Discussion

Dendrochronological techniques were used to establish if there was an unprece-dented decline in radial growth of red spruce in the Great Smoky Mountains duringthe past 150 yr, and if so, whether this decline could be related to climatic variabilityand/or atmospheric pollutants. In the Great Smoky Mountains, red spruce extendsfrom the mountain ridges that are frequently immersed in acidic fog to the mountaindraws. Since environmental conditions that may affect red spruce trees vary alongthis elevation gradient, this study compared radial growth with radial chemistry ofred spruce trees at the extremes of its elevation range in the GSMNP.

3.1. RADIAL GROWTH

During the 1850–1998 period, the chronologies at high and low elevation showedtrends that were generally coupled between 1850 and 1940 (with a minor decouplingaround 1900), decoupled between 1940 and 1980, and coupled between 1980 and1998 (Figure 5). During the decoupled period, both high and low elevation treesshowed a decline in the mean of the standardized ring widths (Figure 5). At highelevation, the decline started in the 1940s or 1950s and reached a minimum in


Figure 5. Standardized chronology for ring width at high and low elevation: (A) mean; and (B)standard deviation.

the 1970s and 1980s (Figure 5A). A substantial minimum in the mean of thestandardized ring widths also occurred in the 1850s and 1860s suggesting thatthe minimum in the 1970s was not unprecedented. However, the standard deviationof the standardized ring widths from the 1850s to 1860s was larger and above theaverage for the time series suggesting a more heterogeneous response (i.e., a more


local environmental factor affecting radial growth). The minimum in the mean ofthe standardized ring widths in the 1850s and 1960s and the minor decouplingof the high and low standardized ring widths around 1900 corresponds with theperiod of operations of the Copper Hill Smelter, located about 80 km upwind ofthe GSMNP (Base and McLaughlin, 1984). In contrast, the standard deviation ofthe standardized ring widths from the 1950s through the 1990s was smaller andbelow the average for the time series suggesting a more homogeneous response(i.e., a more regional environmental factor affecting radial growth) (Figure 5B).Inspection of individual chronologies indicated that 75.1% of the high elevationtrees showed the relatively steep decline from the 1940s or 1950s. At low elevation,the decline started in the 1960s (one to two decades after the decline of the highelevation trees) and reached a minimum in the 1980s (Figure 5A). The minimum inthe 1980s was one of several observed for the time series and the standard deviationof the standardized ring widths from the 1960s to the 1980s was around the averagefor the time series. Inspection of individual chronologies indicated that 54.8% ofthe low elevation trees showed the relatively gentle decline from the 1960s to the1980s.

Previous studies have reported declines in radial growth in the Great SmokyMountains (e.g., McLaughlin et al., 1987; Cook, 1988; Ord and Derr, 1988; VanDeusen, 1988). With our updated time series, we found that while the declinethat started in the 1940s to 1960s was within the observed range of observed radialgrowth, it was unusual in terms of its uniformity in response. When comparing highversus low elevation trees we found that there were differences in 1) the timing ofthe decline, 2) the rate of decline, and 3) the homogeneity of the decline, with highelevation trees showing earlier, faster, and more homogeneous declines than thelow elevation trees. We also found that after the 1980s, both high and low elevationchronologies showed a steep increase followed by a similarly steep decrease in boththe mean and standard deviation of the standardized ring widths.

3.2. RELATIONSHIP OF RADIAL GROWTH TO ENVIRONMENTAL FACTORS

3.2.1. ClimateTo test whether changes in the rate of radial growth were related to climatic variabil-ity, we examined the relationship between annual (Table I) and monthly (Table II)climatic conditions and the mean of the standardized ring width chronology at highand low elevations for two time periods: 1910–1998 (which included all availabledata on environmental conditions) and 1940–1998 (which included data since majorchanges in environmental conditions occurred).

At high elevation, there was no significant relationship between total annualprecipitation or average annual temperature and radial growth (Table I), but therewas a significant positive relationship for August precipitation and January tem-perature versus radial growth for 1910–1998 and for August precipitation versusradial growth for 1940–1998 (Table II). Multiple linear regressions indicated that


TABLE I

Pearson correlation coefficients (r ) and the associated significance levels (p) for relationships betweentotal annual precipitation and average annual temperature versus annual emissions, and between totalannual precipitation, average annual temperature, and annual emissions versus mean standardizedring width chronologies

Environmental factor Environmental factor Environmental factorversus U.S versus high elevation versus low elevationannual emissions mean standardized mean standardized

Environmental factor (106 tons/yr) ring width chronology ring width chronology

r p r p r p

1910–1998US annual emissions 1.0 – −0.652 <0.001 0.159 0.136

(106 tons·yr−1)Total annual precipitation

(m)Current year 0.072 0.500 0.062 0.563 0.247 0.020Previous year 0.070 0.519 0.067 0.537 0.515 <0.001

Average annual temperature(◦C)

Current year −0.083 0.437 0.029 0.790 −0.154 0.151Previous year −0.109 0.310 0.040 0.715 −0.106 0.324

1940–1998US annual emissions 1.0 – −0.655 <0.001 −0.055 0.681

(106 tons·yr−1)Total annual precipitation

(m)Current year 0.021 0.872 0.117 0.378 0.281 0.031Previous year 0.039 0.769 0.110 0.407 0.574 <0.001

Average annual temperature(◦C)

Current year −0.251 0.055 0.058 0.661 −0.272 0.037Previous year −0.308 0.018 0.103 0.436 −0.262 0.045

Correlation coefficients are based both on data from 1910–1998 and 1940–1998 (i.e., after initiationof significant increase in annual emissions). Significant relationships (p ≤ 0.05) are highlighted.

the combination of August precipitation and January temperature explained 13.8%of the variance for 1910–1998 and August precipitation explained 13.3% of the vari-ance for 1940–1998 (Table III). The shift from dry/warm to wet/cool to dry/warmconditions appeared to have contributed to the “spike” in radial growth at both highand low elevations that occurred in the 1990s.

At low elevation, there was a significant positive relationship for total annualprecipitation versus radial growth for 1910–1998 and 1940–1998 and a significantnegative relationship for average annual temperature versus radial growth for1940–1998 (Table I). There were also significant relationships between monthlyclimate variables and radial growth. There were significant positive relationships


TABLE II

Pearson correlation coefficients (r ) and associated significance levels (p) for relationships betweenmonthly precipitation and temperature versus annual emissions, and between monthly precipitationand temperature versus mean standardized ring width chronologies. Relationships were examinedfor months from the end of the preceding growing season (i.e., previous October) to the end of thecurrent growing season (i.e., September)

Climatic factor Climatic factor versus Climatic factor versusversus US high elevation mean low elevation meanannual emissions standardized ring standardized ring

Climatic factor (106 tons/yr) width chronology width chronology

r p r p r p

1910-1998Monthly Precipitation (m)

Previous October −0.022 0.840 −0.057 0.600 −0.011 0.921

Previous November 0.201 0.060 −0.037 0.734 0.277 0.009

Previous December 0.177 0.100 −0.078 0.470 0.110 0.307

January 0.150 0.161 −0.013 0.906 0.136 0.205

February 0.011 0.917 −0.057 0.595 0.005 0.965

March 0.154 0.150 0.009 0.930 0.323 0.002

April −0.090 0.404 −0.015 0.892 −0.091 0.397

May 0.162 0.129 −0.110 0.305 0.018 0.866

June −0.102 0.340 0.077 0.471 0.192 0.072

July −0.219 0.039 −0.001 0.994 −0.184 0.085

August −0.136 0.205 0.322 0.002 0.003 0.979

September −0.036 0.740 0.152 0.156 0.217 0.041

Monthly Temperature (◦C)

Previous October −0.033 0.761 0.074 0.494 0.157 0.145

Previous November 0.196 0.067 −0.075 0.487 −0.067 0.535

Previous December 0.070 0.516 −0.021 0.849 −0.045 0.677

January −0.226 0.033 0.254 0.016 0.048 0.654

February −0.271 0.010 0.022 0.841 −0.259 0.014

March 0.005 0.963 −0.043 0.692 −0.041 0.704

April −0.060 0.574 0.041 0.706 −0.160 0.135

May −0.138 0.196 0.057 0.597 −0.027 0.803

June −0.206 0.053 0.145 0.175 −0.135 0.206

July −0.064 0.551 0.027 0.799 −0.056 0.602

August 0.024 0.825 −0.034 0.754 −0.081 0.450

September −0.163 0.127 0.0331 0.758 −0.195 0.067

1940-1998

Monthly Precipitation (m)

Previous October −0.030 0.820 −0.043 0.746 0.072 0.590

Previous November 0.067 0.617 0.125 0.345 0.295 0.023

Previous December 0.231 0.078 −0.179 0.175 0.065 0.625

(Continued on next page)


TABLE II

(Continued)

Climatic factor Climatic factor Climatic factorversus US versus high elevation versus low elevationannual emissions mean standardized mean standardized

Climatic factor (106 tons/yr) ring width chronology ring width chronology

r p r p r p

January 0.129 0.330 0.001 0.995 0.127 0.338

February −0.077 0.564 −0.022 0.867 −0.037 0.781

March 0.109 0.410 0.039 0.771 0.325 0.012

April −0.067 0.614 −0.049 0.713 −0.034 0.798

May 0.207 0.115 −0.095 0.477 0.017 0.895

June −0.133 0.315 0.127 0.336 0.221 0.093

July −0.259 0.047 −0.034 0.798 −0.212 0.108

August −0.074 0.578 0.364 0.005 0.085 0.523

September −0.055 0.679 0.216 0.101 0.313 0.016

Monthly Temperature (◦C)

Previous October −0.059 0.658 −0.001 0.992 0.117 0.378

Previous November 0.199 0.130 −0.071 0.592 −0.193 0.143

Previous December 0.139 0.292 −0.058 0.662 −0.087 0.514

January −0.142 0.284 0.227 0.084 0.162 0.221

February −0.290 0.026 0.087 0.511 −0.147 0.266

March −0.029 0.830 −0.025 0.853 −0.128 0.332

April −0.164 0.216 0.138 0.299 −0.198 0.132

May −0.256 0.050 0.061 0.645 0.034 0.797

June −0.237 0.071 0.142 0.282 −0.105 0.428

July −0.033 0.804 −0.020 0.883 −0.062 0.642

August −0.048 0.718 0.021 0.876 −0.090 0.500

September −0.053 0.693 −0.097 0.466 −0.169 0.202

Correlation coefficients are based both on data from 1910–1998 and 1940–1998 (i.e., after ini-tiation of significant increase in annual emissions). Significant relationships (p ≤ 0.05) arehighlighted.

between previous year November precipitation and current year March and Septem-ber precipitation versus radial growth for 1910–1998 and 1940–1998 and a negativerelationship between current year February temperature versus radial growth for1910–1998 (Table II). Multiple linear regressions indicated that a combination ofprevious year total annual precipitation and February temperature explained 29.6%of the variance for 1910–1998, and previous year total annual precipitation andprevious year average annual temperature explained 38.3% of the variance for1940–1998 (Table III).


TABLE III

A summary of the simple and multiple linear regression statistics for the relationships betweenclimate, pollution or the combination of climate and pollution versus mean standardized ringwidth chronologies. Regression statistics are based on data from 1910–1998 and 1940–1998(i.e., after initiation of significant increase in annual emissions)

Environmental factors versus high elevationEnvironmental Factor mean standardized ring width

r2 or adjusted r2 p(%)

1910–1998

Climate august precipitation (m) andJanuary temperature (◦C)

13.8 (11.4) <0.001 (0.003)

Pollution US annual emissions (106 tonsyr−1)

42.5 (57.1) <0.001 (<0.001)

Climate and pollution

august precipitation (m) and US annualemissions (106 tons·yr−1)

46.8 (57.1) <0.001 (<0.001)

1940–1998

Climate august precipitation (m) 13.3 (7.6) 0.005 (0.042)

pollution US annual emissions (106

tons·yr−1)42.9 (64.7) <0.001 (<0.001)


august precipitation (m) and US annualemissions (106 tons·yr−1)

51.3 (67.1) <0.001 (<0.001)

1910–1998

Climate previous year total annualprecipitation (m) and februarytemperature (◦C)

29.6 (24.8) 0.001 (<0.001)


2.5 (1.2) 0.136 (0.312)


Previous year total annual precipitation (m)and february temperature (◦C)

29.6 (24.8) <0.001 (<0.001)

1940–1998

Climate previous year total annualprecipitation (m) and previous yearaverage annual temperature (◦C)

38.3 (34.5) <0.001 (<0.001)


0.3 (0.9) 0.681 (0.487)


Previous year total annual precipitation (m)and previous year average annualtemperature (◦C)

38.3 (34.5) <0.001 (<0.001)

Regression statistics for relationships both with and without (in parentheses) data from 1993–1996 (outliers) are presented.


In general, wetter (summer) and/or cooler (winter) conditions were related tohigher rates of radial growth at both high and low elevations.

3.2.2. EmissionsWe then considered if a larger degree of the variance could be explained by emis-sions of atmospheric pollutants (Figure 6, Table I). At high elevation, a signif-icant negative relationship existed for annual emissions of NOx + SO2 versusradial growth. Annual emissions of NOx + SO2 explained 42.5% of the variancefor 1910–1998 and 42.9% of the variance for 1940–1998 (Figure 6A). The rela-tionship suggested that there was an immediate response of radial growth of highelevation trees to changes in the emissions of acidic pollutants: as annual emissionsof NOx + SO2 increased from 1940 to 1973 the mean of the standardized ringwidths decreased, and as annual emissions of NOx + SO2 decreased from 1973 to1998 the mean of the standardized ring widths increased. At low elevation, no suchrelationship between annual emissions of NOx + SO2 and radial growth existed(Figure 6b).

3.2.3. Climate and EmissionsThe combination of environmental factors explained a greater degree of the variancein radial growth than the individual environmental factors near the mountain ridgesbut not in the mountain draws. At high elevation, annual emissions of NOx +SO2 explained 42.5% of the variance, with the addition of August precipitationexplaining an additional 4.3% of the variance (i.e., a total of 46.8%) for 1910–1998, and annual emissions of NOx + SO2 explained 42.9% of the variance, withthe addition of August precipitation explaining an additional 8.4% of the variance(i.e., a total of 51.3%) for 1940–1998 (Table III). At low elevation, only climatewas related to radial growth (Table III).

Previous studies have implicated climate change as a contributor to the declineof radial growth of red spruce in the southern Appalachians (e.g., McLaughlin etal., 1987). Models based on climatic variability could predict radial growth in thepre-decline periods, but not in the post-decline periods. The poor performance ofthe models included both an overestimate of radial growth and a significant lossof correlation between climate and radial growth after the decline initiated. Thisinability implicated another factor affecting trees as something happened to thetrees that caused them to respond to climate differently (cf Cook and Zedaker,1992). In this study, we found 1) evidence of a decline in radial growth correlatedto an increase in annual emissions of NOx + SO2 from 1940s to 1970s, and 2)evidence of a reversal of this decline trajectory that tracked reductions in the annualemissions of NOx + SO2 associated with the implementation of the Clean Air Actin 1970.

What happened in the mid 1990s to red spruce trees? In the 1990s, there wasa period of four years (1993–96) of anomalously high growth at high elevation(Figure 6a) and possibly low elevation (Figure 6b). When we excluded the


Figure 6. Relationship between US annual emissions of NOx + SO2 and the mean of the standardizedchronologies: (a) high elevation; and (b) low elevation. Open circles (1993-96) indicate anomalousradial growth during the 1990s.

1993–1996 data, the variance in radial growth explained by a combination of cli-mate and pollution factors increased from 46.8 to 57.1% (an increase of 10.3%) for1910–1998 and from 51.3 to 67.1% (an increase of 15.8%) for 1940–1998 at highelevation. In contrast, the variance in radial growth explained by climate factorsdid not improve with the exclusion of the anomalous years of radial growth at lowelevation.


The climatic shifts in the 1990s were not enough to explain the “spike” in radialgrowth at high elevation. Another environmental factor that may have contributedto the anomalous radial growth of the mid 1990s is infestation by the balsam woollyadelgid that caused significant mortality to Fraser fir in the southern Appalachians(Peart et al., 1992). Balsam woolly adelgid reached the Great Smoky Mountains bythe late 1950s, infesting lower elevations that are dominated by red spruce at first,but moving to higher elevations that are dominated by Fraser fir within a coupleof decades (Nicholas et al., 1992). By the late 1980s, the balsam woolly adelgidimpacts started to change the canopy structure, as indicated by the large number ofstanding and fallen dead Fraser fir trees at high elevation (Nicholas et al., 1992). Theextreme weather events that occurred in the 1990s, including Hurricane Andrew in1992, Hurricane Opal in 1995, and an ice storm in 1995, may have resulted in largercanopy openings than extreme weather events earlier in the century, because of thelarge number of dead Fraser fir trees (Nicholas et al., 1992). The greater degreeof canopy openings may have had an effect on the radial growth of red spruce.For example, the opening of the canopy may have allowed a release of red sprucegrowth if a few Fraser fir trees were removed from the canopy. The deposition ofnutrients in foliage of Fraser fir to the forest floor following mortality is anotherpotential positive factor on spruce radial growth (McLaughlin et al., 1998). Whilethe importance of the balsam woolly adelgid on the radial growth of red sprucemay have been significant, there were no annual data on the timing and/or intensityof the infestation within the study plots that would have enabled us to examinethis relationship. However, the percentage of trees displaying injury in responseto Balsam wooly adelgid infestation at Mt. Mitchell, NC, has increased from theearly 1960s through to the late 1980s (Hollingsworth and Hain, 1992) indicatingthis new and novel stress is having an impact in the area.

3.3. DIFFERENTIAL RESPONSE IN RADIAL GROWTH BETWEEN HIGH AND LOW

ELEVATION

To explain the lag of up to two decades in the initiation of the decline of radialgrowth and the difference in the magnitude of the decline of radial growth betweenhigh and low elevation trees we consider a conceptual model.

Near the mountain ridges, the red spruce trees experience extreme climaticconditions and large doses of NOx + SO2 due to orographic precipitation and fre-quent cloud immersion (Mohnen, 1992; Johnson and Lindberg, 1992; Lindberg andOwens, 1993). Indeed, during the Integrated Forest Study, the cloud base typicallyoccurred at 1800 m (Johnson and Lindberg, 1992). In addition, the soils are shal-low and have inherently small soil exchangeable Ca and Mg pools, due to higherleaching rates (Johnson and Fernandez, 1992). For example, soils near Clingman’sDome are on average <50 cm deep to bedrock (Branson Unpublished Data, 1994,as cited in Barker et al., 2002) compared with the deeper soils found downslope(Johnson et al., 1991). The gradient in soil depth is associated with slope instability


and landslides, leading to soil losses near the ridges and accumulation of colluviumin the draws (Wolfe, 1967; Fernandez, 1992; White and Cogbill, 1992). Shallowsoils with low base saturation may not have the capacity to provide the exchange-able Ca and Mg necessary for tree growth. Also, increases in mobile anion flux(with increases in NOx and/or SO2 emissions) would preferentially mobilize ex-changeable acidity from soils that are now in the Al-buffering range (Reuss andJohnson, 1986; Johnson and Fernandez, 1992). Thus, radial growth could reflectboth the direct effects of pollution on foliar processes [i.e., physical and chemicalchanges that have been linked to a net reduction in carbon synthesis (McLaughlinet al., 1993)] as well as indirect effects of pollution on the availability and uptakeof base cations in the soil.

In contrast, in the mountain draws, the red spruce are exposed to more moderateclimatic conditions and smaller doses of NOx + SO2 (i.e., below the acid cloudbase). The soils are deeper and have inherently larger exchangeable Ca and Mgpools (Johnson and Fernandez, 1992). In such soils with greater buffering capacity,increases in mobile anion flux would be expected to initially result in greater ex-changeable cation displacement and less solution acidification associated with themobilization of exchangeable Al (Reuss and Johnson, 1986). This may in effectresult in a transient enrichment of the soil solution with exchangeable bases (Ca andMg) available for tree uptake, causing a lack of (or delay in) a negative response inradial growth to increased pollution levels relative to the higher elevations. This lackof a negative response will persist until acid-driven base stripping has proceededto levels where exchangeable cation reserves and base saturation have declined tolevels observed at higher elevation.

To explore the viability of this conceptual model, we examined the concentra-tions of Ca and Mg in the radial increments. In the highest elevation tree (2000m), the magnitude and variability of concentrations of Ca and Mg at high elevationwere relatively small compared with lower elevation trees (≤1800 m) (Figure 7).In lower elevation trees, radial Ca and Mg generally increased from the early 1900sthrough to the mid 1960s, and then decreased from the mid 1960s (when the declinein radial growth started) through to the 1990s (Figure 7). At both high and low el-evations, there was a significant positive relationship between radial Ca and radialgrowth represented at the scale of the population of trees at a specific elevation (i.e.average of standardized mean chronology of all plots at high or low elevations)(Figure 8), but not at the scale of the population of trees within the plot (i.e., theaverage of the standardized mean chronology of all trees sampled within the plot) orthe individual (i.e., the standardized mean chronology of the two cores taken fromthe tree) (data not shown). The relative rate of increase in radial growth per unitradial Ca was substantially larger in the high versus low elevation trees, suggestingthat radial growth is more sensitive to the availability of Ca in the soils at high ele-vation compared with low elevation. There was no significant positive relationshipbetween radial Mg and radial growth at high elevation, but there was a significantpositive relationship between radial Mg and radial growth at low elevation, at the


Figure 7. Time series of the concentration of cations in the radial increments of red spruce treesat high, intermediate, and low elevations: (A) Ca; and (B) Mg. Data are based on analysis of 20 yrradial increment segments prior to 1935 and 10 yr radial increment segments after 1935, with the yearcorresponding to the last radial increment in the segment.

scale of the population of trees at a specific elevation, but not at the scale of thepopulation of trees within the plot, nor at the scale of the individual tree (data notshown).

These data support our conceptual model and suggest that mountain ridgesrepresent a naturally acidified system, where soils have a low availability of basecations that did not change substantially over the 150 yr record, or with the onset ofacidic pollution. This is consistent with soils naturally low in exchangeable basesas a result of cation leaching driven by organic acids in these organic rich soils(characteristic of podzolization) (Fernanadez, 1992; Johnson and Fernandez, 1992)and therefore insensitive to further soil acidification from anthropogenic increasesin strong acid anions (Reuss and Johnson, 1986). It also suggests that soils werealready acid early on in the growth record, increasing the likelihood of preferentialrelease of exchangeable acidity (i.e., Al) over exchangeable bases. In contrast, themountain draws represent an “artificially” or anthropogenically modified system,where fundamental changes in the base saturation of the soils occurred.

Other lines of evidence that suggest a fundamentally different base cation statusbetween high and low elevation sites include studies by McLaughlin et al. (1990,1991) and Van Miegroet et al. (1993), which compared the nutritional and physio-logical status of red spruce saplings at a site located around 1900 m relative to thoseat 1720 m elevation. Both studies showed significantly lower Ca and Mg levels in


Figure 8. Relationship between the concentration of Ca in the radial increments and the mean of thestandardized chronologies: (A) high elevation; and (B) low elevation. Data are based on analysis of20 yr radial increment segments prior to 1935 and 10 yr radial increment segments after 1935, withthe year corresponding to the last radial increment in the segment. The open circle (1995) includesradial increments from the period of anomalous radial growth during the 1990s and was not includedin the regression model for either the high or low elevation data.

the spruce foliage at the higher site. McLaughlin further found less favorable netcarbon exchange rates and lower growth at the high site. Trees at the higher elevationexhibited a positive (albeit transient) response in foliar nutrition to Ca fertilization,but no response to Mg fertilization, suggesting a possible incipient Ca limitation atthat site. Saplings at the lower site, by contrast, showed little fertilizer response, sug-gesting Ca and Mg supply was in the sufficiency range (Van Miegroet et al., 1993).


4. Conclusions

1. Red spruce in the Great Smoky Mountains appeared to be on a trajectory ofunprecedented decline of radial growth starting in 1940s to mid 1970s; however,changes in the Clean Air Act that reduced emissions of SO2 may have resultedin a recovery from this trajectory.

2. The decline in radial growth was not unprecedented, but previous declines ap-peared to have been caused by a more heterogeneous factor related to localsmelting operations than the decline that started in the 1940s.

3. The decline in radial growth was not uniform, as red spruce trees near mountainridges appeared to have responded faster and more homogeneously than redspruce trees in the mountain draws. For trees near the mountain ridges, emissionsof NOx + SO2 since the 1940s explained 42.9% of the pattern in radial growth,with the addition of August precipitation explaining an additional 8.4% (i.e., atotal of 51.3%). For trees in the mountain draws, emissions of NOx + SO2 werenot related to radial growth.

4. A conceptual model is presented where mountain ridges represent a naturallyacidified system, where the effects of NOx and SO2 on the physiological status ofthe red spruce trees dominate, while mountain draws represent an “artificially”or anthropogenically modified system where the effects of NOx and SO2 onthe nutrient status dominate. Foliar leaching is also an important drain of Casupplies and, while it may occur independently of soil leaching, its effects willlikely be most significant where the supply of base cations in the soil is small,such as in the shallow soils on mountain ridges.

5. An implication of the scientific findings is that near mountain ridges, the impactof changes in the emissions of NOx + SO2 are immediate but recovery is possibleif emissions are controlled and, in mountain draws, the impact of increase inNOx + SO2 is delayed, but could be manifested (about 20 yr later) if emissionsare not controlled.

6. This study identified a red spruce growth signal that was related to pollution inthe Great Smoky Mountains where stand structure was relatively uniform; thegrowth signal likely exists throughout the southern Appalachians but may bemasked by stands at different stages of development.

Acknowledgements

The USDA National Research Initiative Competitive Grants Program (Grant No.97-35101-4314) and the USGS Biological Research Division (Cooperative Agree-ment No. 1434 HQ97-RV-01555 RW034) funded this research. The NationalParks Service provided meteorological data in the GSMNP. We acknowledge thecontribution of Anita Rose, Rob Wilson, Don Youngblut, Trudy Kavanagh, JolieGareis, and Darien Ure who provided technical assistance with the field and lab-oratory work, and Dr. Brian Luckman (Department of Geography, University of


Western Ontario, ON) who provided access to dendrological analytical equipmentin his DendroGeomorphology Laboratory. We also acknowledge the contributionof Dr. Tom Bullen (USGS, Menlo Park, CA) who conducted the analysis for theconcentration of cations in the radial increments. Finally, we acknowledge the con-structive comments of the anonymous reviewers.

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