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TREE-RING ANALYSIS AS AN AID TO EVALUATING
THE EFFECTS OF AIR POLLUTION ON TREE GROWTH
Edward Cook
Tree-Ring Laboratory
Lamont-Doherty Geological Observatory
of Columbia University
Palisades, New York, 10964
ABSTRACT
John Innes
Forestry Commission
Alice Holt Lodge
Wrecclesham Farnham Surrey
GU10 4LH United Kingdom
Tree-ring analysis has been used to assess the impact of
pollution on tree growth near point sources emitting high levels of
specific pollutants. However, its use in assessing the impact of
lower-level regional air pollutants on forests is more
controversial. The plethora of regional pollutants coupled with
insufficient physiological understanding
species respond to pollutants makes any causal link between
regional pollution and tree growth difficult to infer. A variety of
statistical analysis procedures are available to search for
anomalous behavior in tree rings in the form of ring-width decline
anti changes not explained by climate. Neither of these effects is
prima facie evidence for pollution stress in trees. However, the
discovery and description of anomalous behavior in tree rings is
an important step in understanding the epidemiology of forest
decline that may ultimately be found to be caused by pollution.
of how different tree
INTRODUCTION
For many years, air pollutants have been recognized as a factor influencing tree
growth, and there is now an extensive literature on the subject (Smith, 1981; McLaughlin,
1985~. Since the Industrial Revolution, the presence of industrial plants emitting gases
such as sulphur dioxide and hydrogen fluoride or particulates such as soot and heavy
metals have caused severe growth reductions and mortality in trees. In extreme cases,
large areas have been completely devastated. Such cases are usually well-documented,
and the mechanisms and nature of tree growth reductions and mortality are reasonably
well understood.
Recently, widespread and severe forest declines have been reported in many parts of
the world, especially in Europe (Schutt and Cowling, 1985) and North America (Johnson
and Siccama, 1983~. These declines cannot be tied directly to any point-source of
pollution, but the presence of coincidental high levels of pollutants in the atmosphere
suggest that some of the forest declines being observed now have been caused by air
pollution. Although many of the currently affected species such as silver fir (babies alba
Mill.) and red spruce (Picea rubens Sarg.) have experienced large-scale declines in the
past (Cramer, 1984; Weiss et al., 1985; Johnson et al., 1986), those past declines do not
appear to have occurred on the same scale as the present declines of the same species
(Brand!, 1985; McLaughlin et al., 1987). The apparently unique severity and scale of the
current forest declines in North America and Europe have been used to bolster the
argument that pollution is a primary contributor to these declines.
157
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158
TREE RINGS AS A POTENTIAL INDICATION OF POLLUTION STRESS IN TREES
Although there is still little convincing evidence for atmospheric pollution being the
cause of regional forest declines (Woodman and Cowling, 1987), the search for indicators
or markers of pollution stress in trees is being vigorously pursued. One potential
indicator, which is available in virtually all temperate forests of the world, is the annual
tree-ring increment. Tree rings are an unique source of information on forests. They
are the only widely available source of long-term, baseline data on forest growth and
productivity that may predate the present era of elevated atmospheric pollution. Insofar
as the year-to-year changes in ring width are an integration and reflection of past
environmental influences on tree growth, it may be possible to use tree-ring analysis to
detect anomalous changes in tree growth that are characteristic of pollution stress.
Thus, by quantitatively comparing past and present tree-ring patterns in forests, an air
pollution effect on regional forest productivity may be detectable.
There are several ways in which the annual tree-ring increment can be quantified
for study. The simplest way, and the way which will be emphasized in this paper, is to
measure the radial ring widths sampled from the breast-height region on the bole of a
tree. Because these measures of tree growth can be obtained easily and
non-destructively from increment cores, they are very practical for studying certain
properties of tree growth. However, as expressions of growth, they are not without
their interpretational problems. At breast-height, both cambial age and the distance of
the cambium from the photosynthetic centers of the canopy increase with time. These
effects, coupled with geometric increases in cambial area each year, frequently cause
these ring widths to decrease with age in a curvilinear fashion. This decrease, which is
an intrinsic property of tree growth, must not be misinterpretated as an indicator of
pollution stress.
There are alternative measures of tree growth based on the annual increment that
can reduce the interpretational problems somewhat. One approach is to transform the
breast-height ring widths to basal area increments (BAIs) (Phipps, 1984; Hornbeck and
Smith, 1985; Phipps and Whiton, 1988~. Although BAIs are ideally measured from
cross-sections, generally less accurate estimates of BAI can also be obtained from
increment cores and tree diameters. If estimated from increment cores, the accuracy of
BAI estimates will be effected by the circuit uniformity and symmetry of radial growth
on the bole. The transformation of ring width to BAI corrects for allometric growth
effects associated with increasing cambial area. Phipps ( 1984) suggests that BAI
increases linearly with time in healthy stands of trees. If this is the case, then a
decline in BAI may be indicative of some abnormal stress on tree growth. However, it is
not necessarily an indicator of pollution stress.
Other much more informative measures of annual increment can be obtained by
detailed stem analysis (Duff and Nolan, 1953; Fritts, 1976, LeBlanc et al., 1 987a). This
approach requires destructive sampling and analysis of annual increment both radially and
with height. However, it is possible to get accurate estimates of annual volume
increment and complete growth layer profiles, which are unobtainable any other way.
Using detailed stem analysis, LeBlanc et al. ( 1 987a) compared ring-width patterns
obtained from breast-height with those obtained from "ring number sequences" (RNSs)
that maintained a constant cambial age and position with respect to the crown. They
found that the two measures of tree growth were significantly correlated in cases where
the sampled trees were dominants in the stand or growing on good sites. Suppressed
trees and trees growing on poor sites showed poorer correlation between the two
ring-width sequences. LeBlanc et al. (1987a) also noted that RNSs sometimes showed
greater changes in radial growth than breast-height ring widths, which suggests that the
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159
former may be more sensitive to environmental changes than the latter in some cases.
Detailed stem analysis is the best approach for differentiating allometric growth declines
from those due to environmental or pollution effects in individual trees. However, the
need for destructive sampling and the enormous increase in measurement effort over
breast-height ring-width studies will restrict this approach to only a few intensively
studied research sites.
Although tree-ring analysis has obvious potential for the study of regional forest
decline, its application in such studies is difficult and controversial. The fact that tree
rings are an integration of many environmental influences on tree growth means that any
pollution signal may be small and embedded in a high level of natural environmental
noise, i.e., the signal-to-noise ratio is likely to be low. This problem is especially
apparent in the study of regional decline where the level of pollution is comparatively
low compared to that near pollution point-sources. Consequently, tree-ring studies of
regional forest decline often sample hundreds or even thousands of trees for analysis in
order to reduce the noise level (e.g., Schweingruber et al., 1985; McLaughlin et al., 1987~.
However, even with very large sample sizes and redundancy in the experimental
design, the identification of an unequivocal pollution signal in tree rings is still very
difficult. One potential problem in identifying a pollution signal is determining, first, the
expectation of normal growth in the absence of pollution (Hyink and Zedacker, 1987~.
Developing a useful normal growth expectation is extremely difficult for all but the
simplist cases, e.g., even-aged, single-species forest plantations. For the closed-canopy
forests of eastern North America, which are typically a mixture of tree species and ages,
useful normal growth models do not exist (e.g., Hornbeck and Smith, 1985~. In such
environments, the evolution of tree rings through time is fundamentally stochastic (Cook,
1 987a; 1 976b) and, therefore, difficult to predict. Although stochastic forecasting
methods, such as those based on autoregressive-integrated moving average (ARIMA) time
series models (Box and Jenkins, 1970), could be used to produce an expectation of normal
growth in a pollution period, the useful forecasting horizon of such methods is likely to
be too short for this application. In addition, the determination of an anomalous
ring-width departure from expectations of normal growth would be conditional on the
validity of those expectations. It is desirable that such an assessment be made as
unconditional as possible, i.e., that it not be based on expectations from a potentially
flawed normal growth model.
To compound the probable lack of a useful normal growth model, we do not have a
good expectation of what a pollution effect looks like in tree rings other than, perhaps,
that ring widths should decrease in the presence of air pollution. In itself, an
expectation of anomalous ring-width decline is nonunique and, therefore, insufficient for
identifying a pollution effect on regional forest growth. Our understanding of the
physiological pathways and effects of various pollutants on forests is still poor, especially
for relatively low doses of air pollution. We also lack a useful understanding of the
interactions between pollution and climate, which may act synergistically or in opposition
depending on the way in which climate is affecting tree growth at the time. Thus,
without a good pollution effect model for tree rings, there is virtually no possibility of a
direct hypothesis test between tree rings and air pollution. Consequently, tree-ring
analysis can not be used to prove, in a direct causal sense, that pollution is responsible
for forest decline. Rather, it is best suited for eliminating other natural explanations of
decline such as climate (Cook, 1 987a) and stand dynamics (McLaughlin et al., 1987), and
for discovering relationships that may produce testable hypotheses about the interactions
between tree growth, climate, and air pollution (Cook et al., 1987; Johnson et al., 1988~.
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160
To this end, we will review some methods of tree-ring analysis based solely on ring
widths obtained from the breast-height region of the bole, and have been used to assess
forest decline and its possible link to air pollution. These methods fall into two basic
categories: testing for anomalous declines in ring width and testing for changes in tree
rings that can not be explained by climate. This review will only cover studies of
regional forest decline since this problem is much more common than local decline caused
by point-sources of pollution (see Thompson, 1981; Fox et al., 1986~. All tree-ring
studies should be based on the principles of dendrochronology (Fritts, 1976~. We will
assume a basic familiarity with the science, especially the principle of crossdating upon
which the integrity of tree-ring analysis rests. For a comprehensive review of the
science, see Fritts (1976), and for a detailed examination of the problems associated with
analyzing tree rings for pollution effects, see Cook (1987a) and Wigley et al. (1987~.
TESTING FOR ANOMALOUS DECLINES IN RING WIDTHS
In searching for anomalous declines in ring width, the obvious question arises:
What is anomalous? The term "anomalous" implies that we know what is not anomalous,
i.e., what is normal growth in tree rings. However, as noted in the previous section, we
may not have a useful expectation of normal radial growth except for the simplest cases.
In order to avoid this obstacle and make the assessment of anomalous decline
unconditional in the sense described above, large-scale forest surveys have been used.
In North America, McLaughlin et al. (1987) examined the ring-width patterns
obtained from 1012 red spruce trees growing on 48 different sites in the northern and
southern Appalachian Mountains. The sites had a wide range of disturbance histories,
stocking levels, and age structures. Previous studies of red spruce tree rings (e.g.,
Johnson and Siccama, 1983; Johnson and McLaughlin, 1986) indicated that red spruce
experienced a widespread, synchronous decline in ring width in the northern
Appalachians after about 1960. The discovery of this apparently anomalous decline
suggested the intervention of some new stress on red spruce growth such as pollution.
McLaughlin et al. (1987) sought to test more rigorously and to quantify the existence of
this putative anomalous decline using the technique of intervention detection (Downing
and McLaughlin, 1987~. This technique searches for the occurrence of step-like changes
and gross outliers in time series without regard to cause. An example of a pure
stepfunction fitted to a red spruce tree-ring series is shown in Figure 1.
McLaughlin et al. (1987) were able to demonstrate conclusively the existence of a
widely synchronous decline in red spruce ring widths after about 1960 in the northern
Appalachians. Red spruce in the southern Appalachians showed a less distinct
synchronous decline after about 1965. Given the heterogeneity in stand characteristics
among the 48 analyzed collections, it is highly unlikely that changes in radial increment
due to stand maturation (Zedacker et al., 1987) would predict the observed synchronous
declines. Therefore, McLaughlin et al. (1987) concluded that red spruce ring widths
have declined anomalously over most of that species' range since 1960.
An analysis of an independent ring-width data set from 2387 red spruce trees
growing on (mostly) previously logged, low-elevation sites in New England supports the
existence and timing of this synchronous decline (Hornbeck and Smith, 1985). However,
Hornbeck and Smith (1985) cautioned that the maturation of these second-growth forests
may be responsible for the synchronous decline because many of the stands were logged
at about the same time 80-100 years ago. Recent research by Van Deusen (1987b) also
supports the stand maturation hypothesis for low-elevation red spruce decline. However,
the coincidental decline of red spruce ring widths at all elevations and for a wide range
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161
A. TREE—RING INDICES WITH THE 1968 STEP FUNCTION INTERVENTION
_ I.
:~
_
0.8
n
1890 1900 1910 1920 1930 1940 1950 1960 1970 ~ 98O
YEAR S
Figure 1. An example of step-like decline in ring width in red spruce. The dashed line
is a simple step-function fitted to the tree-ring series by least squares. These kinds of
effects can be objectively searched for in tree rings using the method of intervention
detection.
of stand histories argues for a similar influence operating at all locations. Thus,
climate and/or pollution may still be responsible for an anomalous ring-width decline of
red spruce even at low elevations.
In Europe, Schweingruber et al. (1985) examined the geographic pattern of abrupt,
long-term changes in tree rings for several conifer species growing in the Swiss Rhone
Valley. The timing of abrupt growth change was determined visually from cross-sections
and increment cores of 2500 trees, and the extent of the change was estimated by
comparing the mean ring width of the altered growth period with the mean ring width
for the same number of rings preceding the period of change. Persistent ring-width
changes of 70% or more could be readily determined, although changes of 30% or less
could not be reliably identified (Schweingruber et al., 1985~. With the exception of one
pine species, all of the conifer species showed abrupt ring-width reductions that strongly
clustered in the 1970s decade, a time when regional forest decline also began in Europe
(Schutt and Cowling, 1985). Schweingruber et al. (1985) were not able to find any clear
relationship between the onset of decline and anomalous climate. In addition, the degree
of decline was not correlated with site attributes, except for elevation (less decline
above 1500 m) and the proximity of the trees to industrial plants (more decline closer to
the plants). Schweingruber et al. (1985) concluded that local and regional pollution was
the likely cause of the ring-width declines in the Swiss Rhone Valley. For another
example of this kind of abrupt growth change analysis, see Schweingruber (1986~.
These North American and European studies avoided the need for a normal growth
model by examining a very large number of trees from a large number of sites having
many different attributes. In so doing, it was possible virtually to eliminate the
probability that some stand-level variables, such as stocking level and disturbance
history, could explain the observed synchronous ring-width declines. Under these
conditions, the statistics supporting the existence of a synchronous decline can be used
to assert that the decline is anomalous, in the sense that stand-level variables are an
insufficient explanation. However, air pollution cannot generally be regarded as the
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162
probable cause of such anomalous declines because meso-scale and synoptic-scale climatic
variables and extremes also have the capacity to produce the observed synchronization.
Testing for an anomalous ring-width decline on a single site is much more difficult.
Either a justifiable normal growth model or a purely stochastic method, like intervention
detection, must be used to test for an anomalous decline. Either way, the possibility
that stand-level variables are responsible for the decline will be difficult to eliminate.
The conclusion of Schweingruber et al. (1985) that suggested a forest
decline-pollution link is tenable to the extent that climate was not correlated with the
onset of decline and the Swiss Rhone Valley is a relatively small area with some
point-sources of pollution. The McLaughlin et al. (1987) study was more complicated,
covering a much larger area with different climatic regimes, airsheds, and pollution
levels. For that reason, no pollution effect could be concluded from the existence of
synchronous decline. In the next section, some methods will be described for
determining if climate can explain such anomalous ring-width declines.
TESTING FOR CHANGES IN TREE RINGS THAT CANNOT BE EXPLAINED BY CLIMATE
The documentation of an anomalous ring-width decline is an important but
insufficient condition for declaring that pollution is contributing to a regional forest
decline. Since climate can also reduce the ring widths of trees over broad geographic
areas, it is necessary to model and eliminate this potentially confounding effect in the
tree rings before a pollution effect can be inferred.
In North America, Cook (1987a) devised a method of testing for the intervention of
non-climatic effects in tree rings, such as pollution. This method requires that the ring
widths first be reduced to a stationary sequence of relative tree-ring indices via some
form of standardization (Fritts, 1976~. Cook (1987a) advocated a "stiff' smoothing spline
(Cook and Peters, 1981 ~ for estimating and removing the underlying growth trend in ring
widths. This method removed very little of the post- 1960 ring-width decline in the red
spruce tree rings analyzed in that study. However, the determination of the appropriate
spline stiffness has been criticized for its subjectivity. As a purely objective alternative,
Van Deusen (1987a) suggested using the first-differences of the logarithmically
transformed ring widths as the relative tree-ring indices. This method will largely
remove any ring-width decline in the resultant indices. The inherent objectivity of trend
removal by first differencing is a compelling argument for its use as long as the decline
in the ring widths is of little direct interest.
Having standardized the ring widths, Cook ~ 1987a) modeled two slightly different
forms of the same red spruce tree-ring chronology with monthly mean temperatures for
the years 1890- 1950 using stepwise multiple regression analysis. The regression models
were able to explain over 50% of the variance in the red spruce tree-ring indices. He
then tested the validity of the regression models by predicting tree-ring indices for the
1951-1960 period, which was assumed to be unaffected by factors related to the post-1960
decline. These validation tests were successful, indicating that the temperature-based
models could be used to estimate tree rings from climate in the post- 1960 decline period.
A change in the relationship between tree rings and climate after 1960 would be evidence
for the intervention of some new unmodeled variables affecting tree growth. In both
cases, the monthly temperature models could not predict the behavior seen in the
tree-ring indices after 1960. This included an inability to predict both the decline and
the yearly pattern of change in the indices. Thus, there appeared to be a change in the
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163
red spruce tree rings after 1960 that could not be explained by climate. An example of
this effect, redrawn from Cook (1987), is shown in Figure 2.
A. ACTUAL AND ESTIMATED UNWHITENED RED SPRUCE INDICES
1.2
bO
t: 1.0
Z;
i_
0.8
O.6
18 B) · ~ · =) t ~ 1940
YEARS
1950 1960 1970 1980
Figure 2. An example of using empirical climatic response models to search for
anomalous effects in tree rings that are not due to climate. The calibration period is
the time period used for developing the regression model between tree rings and climate.
The resulting model is then used to predict tree rings from climate in the verification
period. Note the good predictions up to about 1967 and the breakdown in the model
after that date.
With this success, Cook et al. (1987) and McLaughlin et al. (1987) searched for
non-climatic changes in tree rings from many red spruce sites. In the northern
Appalachians, the results were identical to those just described for all sampled red spruce
growing above 800 m elevation. Spruce growing below 800 m elevation sometimes showed
a stable response to climate through the post-1960 period. This finding is consistent
with data indicating that the red spruce decline is more severe above 800 m (Johnson and
McLaughlin, 1986) where, coincidently or not, pollution levels also increase markedly.
Cook et al. (1987) also noted a consistent relationship between red spruce growth and
climate for all sites above 800 m elevations. They found that red spruce grew better
(worse) in the current growing season when August of the previous growing season was
cooler (warmer) than average and when the December prior to the current growing
season was warmer (cooler) than average. Occurrences of excessively warm Augusts and
cold Decembers since the 1820s in the northern Appalachians also correlated with some
historical declines of red spruce in that region (Weiss et al., 1985; Johnson et al., 1986).
Thus, there may be a relationship between the current red spruce decline and anomalous
temperatures, although pollution cannot be eliminated as a contributor.
In Europe, essentially the same method of testing for the intervention of
non-climatic effects in tree rings was independently developed and used by Eckstein et
al. (1983) and Eckstein (1985) to study the decline of several tree species. Their results
also indicate that climate alone could not explain the level of decline seen in the ring
widths, although the climatic response appears to change less than it does for red spruce
in North America.
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164
The successful use of empirical climatic response models to test for anomalous
changes in tree rings, described here and in other studies (e.g., McClenahen and
Dochinger, 1985; LeBlanc et al., 1987b), indicates that this approach has considerable
potential for the study of forest decline. However, one assumption of this method needs
to be investigated further to insure the proper interpretation of its results. The method
assumes a stationary relationship between tree rings and climate when there is no
intervention of new variables. For this assumption to be correct, systematic changes in
climate must not alter the way in which trees respond to climate. This assumption has
not been adequately tested even though it is known that climate has changed
significantly in the 20th century (Jones et al., 1986; Bradley et al., 1987~.
The possibility that changes in the response of trees to climate may be an indicator
of pollution stress has lead to the development of another very powerful statistical
method based on the Kalman filter. This method, which explicitly allows for
time-dependence in the regression coefficients relating tree rings to climate, was
developed independently by Van Deusen (1987a) in North America and Visser (1986) in
Europe. The method does not require any prior knowledge about the timing of possible
interventions. In addition, the complete yearly time-dependence between tree rings and
climate is available, which enables the evolution and timing of change to be readily
assessed. Finally, the time-dependence in the regression relationships is available
separately for each climatic variable in the model. These are obvious advantages over
the previous method, which only produces information about the relationship of tree rings
with a composite climatic model that is assumed to be time invariant.
A disadvantage of the Kalman filter method is the difficulty in selecting the proper
climatic variables for analysis since no subset selection procedures, analogous to stepwise
regression, are available. Visser and Molenaar ( 1986) describe a subset selection method
that is based on separately screening each candidate climatic variable for statistical
significance with tree rings. Those variables that are significant, even in a
time-dependent sense, may be retained in the full model. However, the probability of
including spurious variables in the model appears to be great, since there is no way of
differentiating time dependence due to spurious association from time-dependence due to
physical and biological changes in the trees. The possibility that climatic change is
creating any observed time-dependence must also be kept in mind when interpreting the
results.
Powerful statistical tools are now available for searching for non-climatic effects in
tree rings that could be due to air pollution. The most daunting tasks are in applying
these techniques well and in properly interpreting the results.
CONCLUSION
As concern about the effects of air pollution on forests continues to grow, it is
likely that tree-ring analysis will play an increasingly important role in the assessment of
forest health. The historical perspective available from tree rings is unique, but the
proper interpretation of this retrospective look at past tree and forest conditions is by
no means simple. Still missing is a useful understanding of how ambient levels of various
air pollutants affect the growth of different tree species under natural forest conditions.
Until this understanding is obtained, any causal link between air pollution and forest
decline that is inferred from tree-ring analysis alone will be very difficult to defend.
But to the extent that proper care is taken in developing and statistically analyzing
tree-ring data, tree-ring analysis should continue to be an important tool for discovering
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165
and characterizing anomalous behavior that may be an indicator of pollution stress in
trees.
ACKNOWLEDGMENTS
This research has been supported by a National Science Foundation Division of
Climate Dynamics Grant ATM 85-15290. We also acknowledge the support of the Forest
Service and National Vegetation Survey in the United States and the Forestry Commission
in the United Kingdom. We thank G.C. Jacoby and J. Overpeck for kindly reviewing the
manuscript. Lamont-Doherty Geological Observatory Contribution No. 435-3.
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Representative terms from entire chapter:
red spruce
