Directory UMM :Data Elmu:jurnal:T:Tree Physiology:vol17.1997:
Tree Physiology 17, 627--635
© 1997 Heron Publishing----Victoria, Canada
Simulating the response of mature yellow poplar and loblolly pine
trees to shifts in peak ozone periods during the growing season using
the TREGRO model
JOHN V. H. CONSTABLE1,2 and WILLIAM A. RETZLAFF 3,4
1
Department of Environmental and Resource Science, University of Nevada, Fleischmann Agriculture, Room 128, Reno, NV 89557-0013, USA
2
Current address: Department of EPO Biology, University of Colorado, Boulder, CO 80309-0334, USA
3
Boyce Thompson Institute for Plant Research, Tower Road, Ithaca, NY 14853-1801, USA
4
Author to whom correspondence should be addressed
Received August 12, 1996
Summary Multiple TREGRO simulations were conducted
with meteorological data files containing different growing
season peak ozone (O3) episodes at O3 exposures of 1.0 and
2.0 × ambient O3 to assess the relationship between O3 response and the phenology of mature yellow poplar (Liriodendron tulipifera L.) and loblolly pine (Pinus taeda L.) trees.
Regardless of O3 exposure and peak O3 episode occurrence, a
peak O3 episode in August caused the greatest reduction in
carbon (C) gain in yellow poplar, whereas a peak O3 episode
in July caused the greatest reduction in C gain of loblolly pine.
In both species, timing of the greatest simulated O3 effect
corresponded with the completion of the annual foliage production phenophase.
Simulated C gain of yellow poplar (total tree, coarse root,
and total nonstructural carbohydrate) was reduced by O3 to a
greater extent than the corresponding compartments in loblolly
pine, but the opposite was true for fine roots. This differential
sensitivity to O3 reflects the fact that both C assimilation and
the O3 response of the species were parameterized according
to observed field measurements of each species. The differential sensitivity to O3 of these species may have long-term
implications for species composition in southeastern USA
forests.
Keywords: air pollutants, Liriodendron tulipifera, phenology,
Pinus taeda, total nonstructural carbohydrates.
Introduction
Industrial activity resulting in the release of ozone (O3) precursors over the past century has increased the background O3
concentrations from 20--40 to 40--60 ppb, a trend that is
expected to continue into the next millennium (National Academy of Science 1992). Although O3 production is centered in
industrial areas, prevailing wind can transport O3 to remote
agricultural and forest ecosystems. Currently, O3 is estimated
to cause in excess of 3 billion dollars per year in agricultural
crop losses (Heck et al. 1991), but the long-term effects of O3
on forest species and ecosystems are less clear (Taylor et al.
1994).
Patterns of tropospheric O3 concentration typically display
an annual cycle in which the lowest O3 concentrations occur
during winter and the highest concentrations occur during
summer. In the southeastern United States, summer climatic
conditions of elevated temperatures, stagnant air masses, and
high concentrations of NOx and volatile organic carbon compounds originating from natural and anthropogenic sources
(Fehsenfeld et al. 1994) can elevate tropospheric O3 concentrations fourfold over those occurring during the winter. In addition to environmental conditions that favor the production of
tropospheric O3, there are also intra- and inter-seasonal variations caused by variations in the concentrations of O3 precursors and their proximity to the measuring station (Fehsenfeld
et al. 1994). A consequence of the variability in O3 formation
is the difficulty in examining the relationship between growing
season O3 exposure (especially periods of peak O3 episodes)
and its effect on growth of forest tree species.
Total pollutant exposure is frequently described as the product of pollutant concentration and duration of exposure. However, because the primary avenue for O3 entry into the plant is
through the stomata (Rubin et al. 1996), O3 injury is probably
related to the product of stomatal conductance, leaf area, and
O3 exposure concentration. Therefore, the phenology of leaf
area, conductance, and O3 play a major role in determining
injury. Experimental studies with Phaseolus vulgaris L. have
shown that O3 exposure profiles containing peak events result
in greater injury than exposures with uniform profiles (Musselman et al. 1983, 1994), indicating that experimental exposures
lacking peak episodes may underestimate the effects of O3 on
plant growth. Although the importance of peak events has been
documented (Musselman et al. 1983, 1994), the interaction
between peak events and phenology is unclear.
Two important forest tree species in the southeastern USA
are yellow poplar (Liriodendron tulipifera L.) and loblolly
pine (Pinus taeda L.). Both species are sensitive to O3 in
experimental studies (Chappelka et al. 1985, Chappelka et al.
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CONSTABLE AND RETZLAFF
1988, Sasek et al. 1991, Tjoelker and Luxmoore 1992, Cannon
et al. 1993, Dizengremel et al. 1994, McLaughlin et al. 1994,
Taylor 1994). Yellow poplar is a broadly distributed hardwood
species with indeterminate leaf growth, whereas loblolly pine
is a widely planted coniferous species that exhibits determinate
foliar growth and is found together with yellow poplar on
moist well-drained sites (Baker and Langdon 1990). Both
species grow rapidly, are found in early successional environments, and may compete directly for available resources.
Because the interaction between tree phenology, growth
habit, and episodic peak O3 events is unclear, we examined
how yellow poplar and loblolly pine would respond to variations in the occurrence of growing season peak O3 episodes.
We hypothesized that the contrasting phenology and growth
habits of these species differentially affects their sensitivity to
variations in the timing of a peak O3 episode during the growing season. Because studies of this nature on mature trees in
the field are difficult and expensive to conduct, we used the
simulation model TREGRO (Weinstein et al. 1991) to assess:
(1) whether there is a critical exposure period during the
growing season that will result in increased O3 response, and
(2) what role phenology plays in the O3 response of these
species.
Materials and methods
TREGRO description
TREGRO is a physiological simulation model of the carbon
(C), water, and nutrient fluxes of an individual tree that was
developed to analyze the responses of trees to multiple environmental stresses. In the model, the tree is divided into compartments: a canopy of leaves grouped by age class, branches,
stem, and coarse and fine roots in three soil horizons. In each
compartment, the model keeps track of three C pools: structure
(living, respiring tissue); wood (the non-respiring tissue); and
total nonstructural carbohydrate (TNC). The model uses the
Farquhar equations (Farquhar et al. 1980) to calculate C assimilation of the entire tree each hour as a function of ambient
environmental conditions and the availability of light in the
canopy, water, and nutrients. Carbon is redistributed daily
within the plant for respiration, growth, storage, and replacement of senescent tissues. Priority for the C varies inversely
with the distance between source and sink and varies directly
with relative sink strength.
In TREGRO, the interaction between tree growth and the
environment is achieved through the linkage of separate data
files. The parameter file defines species-specific characteristics including (but not limited to): maximum photosynthetic rate, rates of maintenance and growth respiration,
specifics of nutrient uptake kinetics, phenological patterns of
growth, growth rates of individual tree compartments, photosynthetic response to O3, initial patterns of C allocation
among compartments, and C partitioning within compartments among living structure, dead wood, and C reserves
(TNC). The meteorological file defines the site-specific hourly
environmental conditions including air temperature (°C), relative humidity (%), rainfall (mm), photosynthetic photon flux
density (µmol m −2 s −1), and O3 concentration (ppb). In the
present study, all TREGRO simulations were 3 years in length
and used a meteorological data file collected on-site at Oak
Ridge, TN, in 1989; for each subsequent year of simulation,
the 1989 conditions were repeated.
TREGRO parameterization
The biomass and C allocation of the initial yellow poplar and
loblolly pine trees were set in the TREGRO model. The simulation target was to grow a yellow poplar tree and a loblolly
pine tree with three annual biomass increments. For the yellow
poplar target tree, we set the annual diameter at breast height
(dbh) increment at 0.30 cm year −1 and the height increment at
23 cm year −1 (Beck 1990). For the loblolly pine target tree, we
set the annual dbh increment at 0.61 cm year −1 (Clark 1992).
Biomass gain of all other tree compartments was estimated
from the stem biomass (yellow poplar) or dbh increment (loblolly pine) assuming that no change occurred in the allometric
relationships during the simulation period (Tables 1 and 2)
(Clark and Schroeder 1977, Van Lear et al. 1986, Vogt 1991).
Initial tree biomass
The initial yellow poplar tree was estimated to be approximately 30 m tall, 41 cm in dbh, and 50 years old (Clark and
Schroeder 1977, Beck 1990), with a mean crown radius of
approximately 4.2 m (Trimble and Tryon 1966). Total tree
biomass in midsummer was allocated at 1.91% foliage,
17.84% branch, 62.14% stem, 13.57% coarse root, and 4.53%
fine root (Clark and Schroeder 1977, Vogt 1991). Leaf area was
calculated from specific leaf area (Kolb and Steiner 1990) and
foliar biomass. Tree biomass in each component was further
partitioned into TNC, structure, and wood (in woody tissue).
The proportion of wood in the initial tree’s stem, branches, and
coarse (woody) roots (36.6%) was set to that reported for the
stem by Panshin and de Zeeuw (1980). The remainder of the
initial biomass was divided between TNC and structure. The
TNC represented 30% of structure in the stem, branch, and
coarse roots and 20% of structure in the foliage based on
reported starch concentrations in roots (Jensen and Patton
1990) and TNC concentrations in foliage (Wullschleger et al.
1992) of yellow poplar trees.
Biomass of the initial loblolly pine tree was based on the dbh
(25 cm) of dominant and codominant loblolly pine trees growing in South Carolina (latitude 34°). A tree of this dbh is
approximately 40 years old and 21 m in height (Van Lear et al.
1986) with a mean crown radius of approximately 3.2 m
(Smith et al. 1992). Initial biomass of individual tree components (foliage, branch, stem, and coarse and fine root) was
calculated from dbh-based allometric equations derived from
loblolly pine trees originally growing in South Carolina (Van
Lear et al. 1986). The root component was further partitioned
into 89 and 11% in coarse and fine roots, respectively (Van
Lear and Kapeluck 1995). Foliage biomass was divided into
four classes as described by Higginbotham (1974). Leaf area
and specific leaf area were calculated from foliar biomass by
regression equations from measurements of Blanche et al.
(1985). Tree biomass in each component was further parti-
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PHENOLOGICAL OZONE RESPONSE OF TREES
629
Table 1. Initial and final biomass and 3-year C gain values from literature allometric data and the resulting TREGRO model 3-year C gain and the
percent estimate for a simulated 50--53-year-old yellow poplar tree.
Component
Values from allometric equations (g C)
Model
% Estimate
Initial biomass
Final biomass
3-Year C gain
C Gain (g C)
Stem
Branch
Foliage
Root total
Coarse root total
Coarse root A
Coarse root B1
Fine root total
Fine root A
Fine root B1
Fine root B2
395254
113475
12149
115128
86314
43157
43157
28814
14407
14407
0
421759
121084
12964
122848
92102
46051
46051
30746
15373
15373
0
26505
7609
815
7720
5788
2894
2894
1932
966
966
0
26911
7637
890
7817
5873
2968
2905
1944
972
972
0
1.5
0.4
9.2
1.3
1.5
2.6
0.4
0.6
0.6
0.6
0
Total tree
636006
678655
42649
43255
1.4
Total aboveground
520878
555807
34929
35438
1.5
3-Year C gain = final biomass -- initial biomass.
% Estimate = ((model C gain -- 3-year allometric C gain)/3-year allometric C gain)100.
Values represent g C (mass = 2 times g C).
Root total = coarse root total + fine root total.
Coarse root total = coarse root A + coarse root B1.
Fine root total = fine root A + fine root B1 + fine root B2.
Total tree = stem + branch + foliage + root total.
Total aboveground = stem + branch + foliage.
Table 2. Initial and final biomass and 3-year C gain values from literature allometric data and the resulting TREGRO model 3-year C gain and the
percent estimate for a simulated 41--44-year-old loblolly pine tree.
Component
Values from allometric equations (g C)
Model
% Estimate
Initial biomass
Final biomass
3-Year C gain
C Gain (g C)
Stem
Branch
Foliage
Class 1
Class 2
Root total
Coarse root total
Coarse root A
Coarse root B1
Fine root total
Fine root A
Fine root B1
Fine root B2
116267
13181
140421
18165
24154
4984
23741
4762
−1.7
−4.5
1391
1844
33225
29570
23360
6210
3654
2595
694
365
1742
2310
40869
36373
28735
7638
4496
3192
854
450
351
466
7644
6803
5375
1428
842
597
160
85
366
477
7470
6615
5238
1377
854
611
159
84
4.3
2.4
−2.3
−2.8
−2.5
−3.6
1.4
2.3
−0.6
−1.2
Total tree
165908
200507
37599
36816
−2.1
Total aboveground
132683
162638
29955
29346
−2.0
3-Year C gain = final biomass -- initial biomass.
% Estimate = ((model C Gain -- 3-year allometric C gain)/3-year allometric C gain)100.
Values represent g C (mass = 2 times g C).
Root total = coarse root total + fine root total.
Coarse root total = coarse root A + coarse root B1.
Fine root total = fine root A + fine root B1 + fine root B2.
Total tree = stem + branch + foliage + root total.
Total aboveground = stem + branch + foliage.
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CONSTABLE AND RETZLAFF
The soil rooting area of yellow poplar and loblolly pine (55.9
and 31.7 m2, respectively) was defined to be identical to the
projected crown area, assuming a crown radius of 4.2 and
3.2 m (Trimble and Tryon 1966, Smith et al. 1992) and a
uniform circular-shaped crown (cf. Retzlaff et al. 1996).
Depths of the A, B1, and B2 soil horizons were set to 0.2,
0.2, and 0.3 m, respectively, based on average measured soil
depths in southeastern loblolly pine stands (Harris et al. 1977,
Binkley et al. 1992, Richter et al. 1994) and a southeastern
yellow poplar forest (Harris et al. 1977). Soil water and nutrient conditions were set to be nonlimiting in all of the simulations.
values recorded by Cannon et al. (1993), Chappelka et al.
(1988), Gunderson et al. (1993), Neufeld et al. (1985), Norby
and O’Neill (1991), Tjoelker and Luxmoore (1992), and Wullschleger et al. (1992). Leaf respiration was set at 22% of net C
assimilation (Wullschleger et al. 1992, Cannon et al. 1993).
Loblolly pine net C assimilation for a midsummer 11-day
period at high irradiance (1000 µmol m −2 s −1; 25--30 °C) was
set to be approximately 0.0035 g C g −1 Cleaf h −1 (Cregg et al.
1993). Leaf respiration was set at 25% of net C assimilation
(Samuelson et al. 1992).
The final TREGRO simulated trees were calibrated by adjusting tissue growth rates and senescence rates in fine roots
until two conditions were met: (1) when the simulated C gain
of each of the tree components (foliage, branch, stem, and
coarse and fine roots) and the total tree C gain was within 10%
of the value for projected C gain from the literature-based
allometric relationships (Tables 1 and 2), and (2) when the
proportion of TNC and the ratio of structure to wood in each
of the tree components at the end of a simulation matched that
parameterized for the tree at the beginning of the simulation.
Fine root senescence was set to approximate one complete root
turnover per year for both species based on field measurements
(Harris et al. 1977).
Seasonal phenology
Ozone simulations
Initial seasonal foliage growth of mature yellow poplar trees
begins in mid-April and the majority (> 80%) of foliage is
produced by mid-July (Lamb 1915, Kienholz 1941). The remainder (≈ 20%) of the foliage biomass is produced during the
latter part of the growing season when conditions are favorable. Height and radial growth begin in mid-May (Kienholz
1941, Morrow and McKee 1963, Mowbray and Oosting 1968)
and continue until approximately mid-September (Morrow
and McKee 1963, Lieth and Radford 1971). Root growth
occurs from spring to fall when conditions are favorable (Harris et al. 1977). Foliage senescence occurs during the second
week in October (Lamb 1915). Yellow poplar trees senesce all
current foliage.
Mature loblolly pine trees produce two cohorts of foliage per
year with bud break of the first flush of foliage occurring in
early spring (Higginbotham 1974). The first flush ends in early
May and the second foliage flush initiates in mid-May and
continues until mid-June (Higginbotham 1974). Height and
radial growth begin soon after bud break of the first flush of
foliage and continue until late July (Miller et al. 1987). Root
growth occurs from spring to fall when conditions are favorable (Harris et al. 1977, Baker and Langdon 1990). Foliage
senescence occurs late in the season with needle-cast occurring
at the end of the growing season (approximately mid-November--early December) (Higginbotham 1974). Loblolly pine
trees senesce all 2-year-old foliage, retaining only current-year
foliage over winter.
In TREGRO, effects of O3 are simulated through a cumulative
effect of the pollutant on the maximum rate of photosynthesis,
Vmax . The magnitude of the O3 effect is controlled by a threshold of cumulative O3 uptake, below which there is no effect on
Vmax , and a linear decrease in Vmax above this threshold with
increasing cumulative uptake of O3. Although O3 does not
accumulate in the leaf tissue, the effect of cumulative O3
uptake is proportional to the sum of the hourly O3 concentration times the foliar rate of O3 conductance, because the primary avenue for O3 entry is through the stomata (Rubin et al.
1996).
To evaluate the effect of the maximum O3 response possible,
we assumed that Vmax began decreasing as soon as any O3
uptake occurred in the leaves (i.e., the O3 threshold was zero).
As the total amount of cumulative O3 uptake increased during
the growing season, we assumed a proportional decrease in
Vmax . The slope of the described response was set so that the
reduction in photosynthesis observed at the end of the open-top
chamber experiments matched the simulated reduction after a
similar cumulative uptake of O3 had occurred.
The yellow poplar response to O3 was set in the parameter
file according to the data of Cannon et al. (1993) (Figure 1),
who measured a 10% reduction in net photosynthesis of seedlings relative to charcoal-filtered air after a total cumulative O3
uptake of 0.0044 g g −1 Cleaf . The loblolly pine response to O3
was set in the parameter file according to the data of Sasek
et al. (1991) (Figure 1), who measured a 24% reduction in
current leaf net photosynthesis relative to that of seedlings in
charcoal-filtered air after a total cumulative O3 uptake of
0.0136 g g −1 C leaf .
In the simulation experiment, one short-term (8 day) peak
O3 episode was used in which O3 concentrations increased and
tioned into TNC, structure, and wood (in woody tissue). The
proportion of wood in the initial tree’s stem, branches, and
coarse (woody) roots (57%) was set to that reported for the
stem by Blanche et al. (1985). The remainder of the initial
biomass was divided between TNC and structure. The TNC
represented 30% of structure in the stem, branch, and coarse
roots and 20% of structure in the foliage based on reported
TNC concentrations in coarse roots, stem, and foliage of loblolly pine trees (Friend et al. 1992).
Soil parameters
Carbon assimilation
Yellow poplar net C assimilation for a midsummer 11-day
period at high irradiance (1000 µmol m −2 s −1; 25--30 °C) was
set to be approximately 0.0192 g C g −1 C leaf h −1, based on
TREE PHYSIOLOGY VOLUME 17, 1997
PHENOLOGICAL OZONE RESPONSE OF TREES
631
ured (1989) Oak Ridge, TN, ambient O3 concentrations (3 O3
concentrations × 7 meteorological files = 21 total simulations).
Use of a 0.0 × O3 exposure, although unrealistic in a field study,
permitted determination of the maximum O3 response possible.
Results and discussion
Matching phenology to reported values
Figure 1. Assumed relationships between cumulative O 3 uptake and
maximum C assimilation in yellow poplar and loblolly pine.
decreased in a normal diurnal pattern (for Oak Ridge, TN,
1989), with maximum O3 concentrations of 125 ppb for between 3 and 8 h per day (Figure 2). All meteorological data in
the Oak Ridge meteorological file, including the O3 concentrations, were used to create the 8-day O3 peak episode profile.
The peak O3 episode was placed in seven different (Oak Ridge,
TN, 1989) meteorological files to produce peak O3 exposures
centered on the first day of each month between April 1 and
October 1. To insert the peak O3 episode, we simply substituted
all the existing meteorological data during the insertion period
with the peak meteorological data thereby avoiding the problem of mismatching environmental and O3 data. However,
because the overwritten areas at different times of the year do
not contain identical recorded O3 concentrations, there is slight
variation (up to 3.7%) in the sum00 (sum00 = cumulative sum
of hourly O3 values during the growing season) O3 exposure
among files between the highest (123402 ppb⋅h) and lowest
(118975 ppb⋅h) sum exposure. During the 1989 growing season, in the absence of our artificial O3 peak, there were no
episodic periods of highly elevated O3 concentration (maximum recorded hourly concentration 88 ppb O3); however, O3
concentrations (up to 132 ppb) were measured at Oak Ridge,
TN, in 1988. Model simulations (3-year duration) were performed with each of these altered meteorological files using O3
concentrations of 0.0 (base case), 1.0, and 2.0 times the meas-
Figure 2. The 8-day peak ozone episode that was inserted at monthly
intervals into the 1989 Oak Ridge,TN meterological data file.
We matched phenology parameters in the base TREGRO trees
with those reported in the literature for both tree species. For
instance, mature loblolly pine trees produce two cohorts of
foliage per year with bud break of the first flush of foliage
occurring in the early spring (Day of Year (DOY) 60) and
ending on approximately DOY 135 (Higginbotham 1974). The
second foliage flush initiates on approximately DOY 135 and
continues until DOY 184 (Higginbotham 1974). Further, initial seasonal foliage growth of mature yellow poplar trees
begins on DOY 99 and the majority (> 80%) of the foliage is
produced by DOY 206 (Lamb 1915, Kienholz 1941). The
remainder (≈ 20%) of the foliage biomass is produced during
an additional period (DOY 207 to 246) of shoot growth. By
setting the initial base-tree parameters using this and other
phenological information, we were able to reproduce these
demographic patterns accurately with TREGRO (Figure 3).
Phenological development is a complex phenomenon governed by a suite of environmental cues. TREGRO duplicates
this process as controlled by the accumulation (from the start
of simulation) of heat degree-days above 0 °C. Therefore, we
were able to parameterize mature yellow poplar and loblolly
pine trees in TREGRO, simulate growth for a period of 3 years,
Figure 3. Phenograms from loblolly pine and yellow poplar TREGRO
parameter files. Horizontal bars represent periods in the simulations
when growth of the various compartments could occur if environmental conditions were favorable. Arrows correspond to the peak O 3
episode that elicited the maximum response as described by Figures
4--7.
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CONSTABLE AND RETZLAFF
and duplicate the dynamics of phenological processes that are
currently reported in the literature for individual yellow poplar
and loblolly pine trees. Accurate simulation of dynamic phenological processes with TREGRO permitted investigation of
the interaction between phenophase and episodic environmental (O3) stress.
Ozone simulations
In our simulations, the presence of atmospheric O3 (1.0 or 2.0
× ambient), regardless of timing of the peak O3 episode, reduced total tree C gain (Figure 4), coarse root C gain (Figure 5), and tree TNC compartments (Figure 6) compared to the
control trees of both species. Carbon gain of fine roots of both
species was not affected at 1.0 × ambient O3 (Figure 7).
Additionally, as the O3 concentration increased (to 2.0 × ambient), the O3 effects (reflected by additional reductions in total
tree, coarse root, fine root, and TNC C gain) became more
pronounced. Negative C gain of the coarse roots, TNC and fine
roots compartments reflects utilization of previously stored
TNC and root turnover without replacement, respectively. It is
known from field-exposure experiments that seedlings and
saplings of both species, and branches of mature loblolly pine
trees are sensitive to O3 (Chappelka et al. 1985, Chappelka
et al. 1988, Sasek et al. 1991, Tjoelker and Luxmoore 1992,
Cannon et al. 1993, Dizengremel et al. 1994, McLaughlin et al.
1994). However, the simulation experiment represents the first
time that the O3 responses of whole mature trees of these
species have been examined. McLaughlin and Downing
(1995) studied changes in loblolly pine stem diameter during
a 5-year period in the Oak Ridge, TN area, which included the
1989 conditions used in our modeling study, and found that
ambient exposure in the field in combination with elevated
Figure 4. Change in tree mass following a 3-year TREGRO simulation
of mature loblolly pine and yellow poplar trees with no O 3 exposure
and monthly peak O3 episodes. The response illustrated for the October peak O3 episode was identical to a 1.0 and 2.0 × ambient exposure
at this site with no peak O3 episode; therefore, values representing O 3
exposure without a peak episode are not shown.
Figure 5. Change in coarse root mass following a 3-year TREGRO
simulation of mature loblolly pine and yellow poplar trees with no O 3
exposure and monthly peak O3 episodes. Negative values reflect utilization of previously stored TNC.
temperature or low rainfall was associated with reduced stem
increment. We do not know whether our simulated estimates
of physiological responses accurately reflect the O3 response
that would occur in mature forest-grown trees. Hanson et al.
(1994) have shown that gas exchange of mature red oak (Quercus rubra L.) trees exposed to O3 is affected more by O3 than
similarly exposed red oak seedlings, indicating that caution
Figure 6. Change in total nonstructural carbohydrate (TNC) following
a 3-year TREGRO simulation of mature loblolly pine and yellow
poplar trees with no O3 exposure and monthly peak O3 episodes.
Negative values reflect utilization of previously stored TNC.
TREE PHYSIOLOGY VOLUME 17, 1997
PHENOLOGICAL OZONE RESPONSE OF TREES
Figure 7. Change in fine root mass following a 3-year TREGRO
simulation of mature loblolly pine and yellow poplar trees with no O 3
exposure and monthly peak O3 episodes. Negative values reflect fine
root senescence without replacement.
should be used when extrapolating the results of seedling
exposure experiments to mature trees. However, the nature of
our simulated responses (reduced root growth and TNC content of yellow poplar and loblolly pine trees) matches those
proposed in a conceptual model of O3 response (Cooley and
Manning 1987), observed in O3 experiments with woody
plants (see Tingey et al. 1976, Mortenson and Skyre 1990,
Retzlaff et al. 1992), and predicted in other simulation exercises (Retzlaff et al. 1996).
Carbon gain of yellow poplar (total tree, coarse root, and
TNC) was reduced by O3 to a greater extent than the corresponding compartments in loblolly pine, reflecting the fact that
we parameterized the C assimilation (e.g., yellow poplar:
Wullschleger et al. 1992 and loblolly pine: Cregg et al. 1993)
and the O3 (e.g., yellow poplar: Cannon et al. 1993 and loblolly
pine: Sasek et al. 1991) response parameters of the two species
according to field measurements (Figure 1) (i.e., we parameterized yellow poplar to be more sensitive to O3). This differential sensitivity to O3 has implications for the competition
between these two species as they co-occur and are exposed to
elevated concentrations of tropospheric O3 in the forest ecosystems in the southeastern USA.
Phenological O3 response
The simulated response illustrated for the October peak O3
episode was identical to a 1.0 and 2.0 × ambient exposure at
this site with no peak O3 episode; therefore, values representing O3 exposure without a peak episode are not shown.
Thus, the presence of peak O3 episodes differentially altered C
gain (Figure 4), and the growth of individual tree compart-
633
ments (Figures 5--7) independently of the atmospheric O3
concentration. Additionally, as the O3 concentration increased
to 2.0 × ambient, the effects corresponding to the timing of the
peak O3 episode became more pronounced. In our simulations,
the peak O3 episode in August caused the greatest reduction in
C gain in yellow poplar, whereas the peak O3 episode in July
caused the greatest reduction in C gain of loblolly pine. Timing
of the greatest simulated O3 effect corresponded with the
completion of the annual foliage production phenophase (and
therefore maximum C assimilating foliage area) on each of
these tree species (Figure 3). At the time of the July peak O3
episode, the simulated loblolly pine tree had reached the seasonal maximum photosynthetic foliage biomass. At the time of
the August peak O3 episode, the simulated yellow poplar tree
had produced approximately 90% of the seasonal maximum
photosynthetic foliage biomass.
Similar seasonal sensitivity responses have been noted previously for annual crops exposed to water stress (Eck et al.
1987, Halim et al. 1989, Stirling et al. 1989) and O3 (Blum and
Heck 1980, Kohut and Laurence 1983, McLaughlin and
McConathy 1983, Younglove et al. 1994). All of these studies
demonstrate sensitivity (e.g., reduced biomass and crop yield)
to the timing of the environmental stress, particularly when the
stress corresponds with critical phenological stages. Our simulation is the first study to link peak O3 episodes to a specific
phenophase in mature trees.
Our simulations of peak O3 episode events did not alter the
phenology of the two tree species. Date of initiation, patterns,
and durations of stem and fascicle elongation of loblolly pine
seedlings were not affected by O3 treatment (cf. Mudano et al.
1992). However in another study, loblolly pine seedlings exposed to 2.0 × ambient O3 exhibited a delay in fine root
production (Edwards et al. 1992). Atmospheric O3 will not
normally alter the timing of phenological events directly in
TREGRO because the timing of the occurrence of phenological events is driven by the accumulation (from the start of
simulation) of heat degree-days above 0 °C, a model feature
that is unrelated to O3 exposure. However, in our TREGRO
simulations, phenology could have been altered if sufficient
reductions in available C (current assimilate or stored TNC)
had occurred, thereby making C unavailable at the start of a
phenophase, or available C supplies were exhausted before
phenophase completion.
The TREGRO simulations demonstrate that there is a critical peak O3 exposure period for yellow poplar and loblolly
pine that is linked to the phenology of these two species. We
observed maximum O3 response when the peak O3 episode
occurred at or near the completion of the annual foliage production phenophase. Such simulation studies are useful in
identifying physiological responses to environmental stress
heretofore unavailable because of cost and other limitations.
Recent re-analysis of data from four field crop-loss yield trials
identified that growth-stage-dependent phenological weighting of pollutant exposure may result in more effective predictions of O3 exposure resulting in yield reductions (Younglove
et al. 1994). Results from similar studies could be used to
TREE PHYSIOLOGY ON-LINE at http://www.heronpublishing.com
634
CONSTABLE AND RETZLAFF
elucidate further the mechanism(s) of the phenological response of plants to environmental stress.
Acknowledgments
This research was conducted as part of research cooperative CR820759-02 between the USEPA, the University of Nevada, Reno, and
Boyce Thompson Institute for Plant Research. Additional funds were
provided by the Electric Power Research Institute (EPRI) and the
endowment of Boyce Thompson Institute for Plant Research. This
paper has not been subject to either USEPA or EPRI policy review and
should not be construed to represent policies of the agencies. We thank
Dr. D. Weinstein, Dr. G. Taylor, and Dr. R. Kohut for critical manuscript review, and B. Warland for word processing assistance.
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TREE PHYSIOLOGY ON-LINE at http://www.heronpublishing.com
© 1997 Heron Publishing----Victoria, Canada
Simulating the response of mature yellow poplar and loblolly pine
trees to shifts in peak ozone periods during the growing season using
the TREGRO model
JOHN V. H. CONSTABLE1,2 and WILLIAM A. RETZLAFF 3,4
1
Department of Environmental and Resource Science, University of Nevada, Fleischmann Agriculture, Room 128, Reno, NV 89557-0013, USA
2
Current address: Department of EPO Biology, University of Colorado, Boulder, CO 80309-0334, USA
3
Boyce Thompson Institute for Plant Research, Tower Road, Ithaca, NY 14853-1801, USA
4
Author to whom correspondence should be addressed
Received August 12, 1996
Summary Multiple TREGRO simulations were conducted
with meteorological data files containing different growing
season peak ozone (O3) episodes at O3 exposures of 1.0 and
2.0 × ambient O3 to assess the relationship between O3 response and the phenology of mature yellow poplar (Liriodendron tulipifera L.) and loblolly pine (Pinus taeda L.) trees.
Regardless of O3 exposure and peak O3 episode occurrence, a
peak O3 episode in August caused the greatest reduction in
carbon (C) gain in yellow poplar, whereas a peak O3 episode
in July caused the greatest reduction in C gain of loblolly pine.
In both species, timing of the greatest simulated O3 effect
corresponded with the completion of the annual foliage production phenophase.
Simulated C gain of yellow poplar (total tree, coarse root,
and total nonstructural carbohydrate) was reduced by O3 to a
greater extent than the corresponding compartments in loblolly
pine, but the opposite was true for fine roots. This differential
sensitivity to O3 reflects the fact that both C assimilation and
the O3 response of the species were parameterized according
to observed field measurements of each species. The differential sensitivity to O3 of these species may have long-term
implications for species composition in southeastern USA
forests.
Keywords: air pollutants, Liriodendron tulipifera, phenology,
Pinus taeda, total nonstructural carbohydrates.
Introduction
Industrial activity resulting in the release of ozone (O3) precursors over the past century has increased the background O3
concentrations from 20--40 to 40--60 ppb, a trend that is
expected to continue into the next millennium (National Academy of Science 1992). Although O3 production is centered in
industrial areas, prevailing wind can transport O3 to remote
agricultural and forest ecosystems. Currently, O3 is estimated
to cause in excess of 3 billion dollars per year in agricultural
crop losses (Heck et al. 1991), but the long-term effects of O3
on forest species and ecosystems are less clear (Taylor et al.
1994).
Patterns of tropospheric O3 concentration typically display
an annual cycle in which the lowest O3 concentrations occur
during winter and the highest concentrations occur during
summer. In the southeastern United States, summer climatic
conditions of elevated temperatures, stagnant air masses, and
high concentrations of NOx and volatile organic carbon compounds originating from natural and anthropogenic sources
(Fehsenfeld et al. 1994) can elevate tropospheric O3 concentrations fourfold over those occurring during the winter. In addition to environmental conditions that favor the production of
tropospheric O3, there are also intra- and inter-seasonal variations caused by variations in the concentrations of O3 precursors and their proximity to the measuring station (Fehsenfeld
et al. 1994). A consequence of the variability in O3 formation
is the difficulty in examining the relationship between growing
season O3 exposure (especially periods of peak O3 episodes)
and its effect on growth of forest tree species.
Total pollutant exposure is frequently described as the product of pollutant concentration and duration of exposure. However, because the primary avenue for O3 entry into the plant is
through the stomata (Rubin et al. 1996), O3 injury is probably
related to the product of stomatal conductance, leaf area, and
O3 exposure concentration. Therefore, the phenology of leaf
area, conductance, and O3 play a major role in determining
injury. Experimental studies with Phaseolus vulgaris L. have
shown that O3 exposure profiles containing peak events result
in greater injury than exposures with uniform profiles (Musselman et al. 1983, 1994), indicating that experimental exposures
lacking peak episodes may underestimate the effects of O3 on
plant growth. Although the importance of peak events has been
documented (Musselman et al. 1983, 1994), the interaction
between peak events and phenology is unclear.
Two important forest tree species in the southeastern USA
are yellow poplar (Liriodendron tulipifera L.) and loblolly
pine (Pinus taeda L.). Both species are sensitive to O3 in
experimental studies (Chappelka et al. 1985, Chappelka et al.
628
CONSTABLE AND RETZLAFF
1988, Sasek et al. 1991, Tjoelker and Luxmoore 1992, Cannon
et al. 1993, Dizengremel et al. 1994, McLaughlin et al. 1994,
Taylor 1994). Yellow poplar is a broadly distributed hardwood
species with indeterminate leaf growth, whereas loblolly pine
is a widely planted coniferous species that exhibits determinate
foliar growth and is found together with yellow poplar on
moist well-drained sites (Baker and Langdon 1990). Both
species grow rapidly, are found in early successional environments, and may compete directly for available resources.
Because the interaction between tree phenology, growth
habit, and episodic peak O3 events is unclear, we examined
how yellow poplar and loblolly pine would respond to variations in the occurrence of growing season peak O3 episodes.
We hypothesized that the contrasting phenology and growth
habits of these species differentially affects their sensitivity to
variations in the timing of a peak O3 episode during the growing season. Because studies of this nature on mature trees in
the field are difficult and expensive to conduct, we used the
simulation model TREGRO (Weinstein et al. 1991) to assess:
(1) whether there is a critical exposure period during the
growing season that will result in increased O3 response, and
(2) what role phenology plays in the O3 response of these
species.
Materials and methods
TREGRO description
TREGRO is a physiological simulation model of the carbon
(C), water, and nutrient fluxes of an individual tree that was
developed to analyze the responses of trees to multiple environmental stresses. In the model, the tree is divided into compartments: a canopy of leaves grouped by age class, branches,
stem, and coarse and fine roots in three soil horizons. In each
compartment, the model keeps track of three C pools: structure
(living, respiring tissue); wood (the non-respiring tissue); and
total nonstructural carbohydrate (TNC). The model uses the
Farquhar equations (Farquhar et al. 1980) to calculate C assimilation of the entire tree each hour as a function of ambient
environmental conditions and the availability of light in the
canopy, water, and nutrients. Carbon is redistributed daily
within the plant for respiration, growth, storage, and replacement of senescent tissues. Priority for the C varies inversely
with the distance between source and sink and varies directly
with relative sink strength.
In TREGRO, the interaction between tree growth and the
environment is achieved through the linkage of separate data
files. The parameter file defines species-specific characteristics including (but not limited to): maximum photosynthetic rate, rates of maintenance and growth respiration,
specifics of nutrient uptake kinetics, phenological patterns of
growth, growth rates of individual tree compartments, photosynthetic response to O3, initial patterns of C allocation
among compartments, and C partitioning within compartments among living structure, dead wood, and C reserves
(TNC). The meteorological file defines the site-specific hourly
environmental conditions including air temperature (°C), relative humidity (%), rainfall (mm), photosynthetic photon flux
density (µmol m −2 s −1), and O3 concentration (ppb). In the
present study, all TREGRO simulations were 3 years in length
and used a meteorological data file collected on-site at Oak
Ridge, TN, in 1989; for each subsequent year of simulation,
the 1989 conditions were repeated.
TREGRO parameterization
The biomass and C allocation of the initial yellow poplar and
loblolly pine trees were set in the TREGRO model. The simulation target was to grow a yellow poplar tree and a loblolly
pine tree with three annual biomass increments. For the yellow
poplar target tree, we set the annual diameter at breast height
(dbh) increment at 0.30 cm year −1 and the height increment at
23 cm year −1 (Beck 1990). For the loblolly pine target tree, we
set the annual dbh increment at 0.61 cm year −1 (Clark 1992).
Biomass gain of all other tree compartments was estimated
from the stem biomass (yellow poplar) or dbh increment (loblolly pine) assuming that no change occurred in the allometric
relationships during the simulation period (Tables 1 and 2)
(Clark and Schroeder 1977, Van Lear et al. 1986, Vogt 1991).
Initial tree biomass
The initial yellow poplar tree was estimated to be approximately 30 m tall, 41 cm in dbh, and 50 years old (Clark and
Schroeder 1977, Beck 1990), with a mean crown radius of
approximately 4.2 m (Trimble and Tryon 1966). Total tree
biomass in midsummer was allocated at 1.91% foliage,
17.84% branch, 62.14% stem, 13.57% coarse root, and 4.53%
fine root (Clark and Schroeder 1977, Vogt 1991). Leaf area was
calculated from specific leaf area (Kolb and Steiner 1990) and
foliar biomass. Tree biomass in each component was further
partitioned into TNC, structure, and wood (in woody tissue).
The proportion of wood in the initial tree’s stem, branches, and
coarse (woody) roots (36.6%) was set to that reported for the
stem by Panshin and de Zeeuw (1980). The remainder of the
initial biomass was divided between TNC and structure. The
TNC represented 30% of structure in the stem, branch, and
coarse roots and 20% of structure in the foliage based on
reported starch concentrations in roots (Jensen and Patton
1990) and TNC concentrations in foliage (Wullschleger et al.
1992) of yellow poplar trees.
Biomass of the initial loblolly pine tree was based on the dbh
(25 cm) of dominant and codominant loblolly pine trees growing in South Carolina (latitude 34°). A tree of this dbh is
approximately 40 years old and 21 m in height (Van Lear et al.
1986) with a mean crown radius of approximately 3.2 m
(Smith et al. 1992). Initial biomass of individual tree components (foliage, branch, stem, and coarse and fine root) was
calculated from dbh-based allometric equations derived from
loblolly pine trees originally growing in South Carolina (Van
Lear et al. 1986). The root component was further partitioned
into 89 and 11% in coarse and fine roots, respectively (Van
Lear and Kapeluck 1995). Foliage biomass was divided into
four classes as described by Higginbotham (1974). Leaf area
and specific leaf area were calculated from foliar biomass by
regression equations from measurements of Blanche et al.
(1985). Tree biomass in each component was further parti-
TREE PHYSIOLOGY VOLUME 17, 1997
PHENOLOGICAL OZONE RESPONSE OF TREES
629
Table 1. Initial and final biomass and 3-year C gain values from literature allometric data and the resulting TREGRO model 3-year C gain and the
percent estimate for a simulated 50--53-year-old yellow poplar tree.
Component
Values from allometric equations (g C)
Model
% Estimate
Initial biomass
Final biomass
3-Year C gain
C Gain (g C)
Stem
Branch
Foliage
Root total
Coarse root total
Coarse root A
Coarse root B1
Fine root total
Fine root A
Fine root B1
Fine root B2
395254
113475
12149
115128
86314
43157
43157
28814
14407
14407
0
421759
121084
12964
122848
92102
46051
46051
30746
15373
15373
0
26505
7609
815
7720
5788
2894
2894
1932
966
966
0
26911
7637
890
7817
5873
2968
2905
1944
972
972
0
1.5
0.4
9.2
1.3
1.5
2.6
0.4
0.6
0.6
0.6
0
Total tree
636006
678655
42649
43255
1.4
Total aboveground
520878
555807
34929
35438
1.5
3-Year C gain = final biomass -- initial biomass.
% Estimate = ((model C gain -- 3-year allometric C gain)/3-year allometric C gain)100.
Values represent g C (mass = 2 times g C).
Root total = coarse root total + fine root total.
Coarse root total = coarse root A + coarse root B1.
Fine root total = fine root A + fine root B1 + fine root B2.
Total tree = stem + branch + foliage + root total.
Total aboveground = stem + branch + foliage.
Table 2. Initial and final biomass and 3-year C gain values from literature allometric data and the resulting TREGRO model 3-year C gain and the
percent estimate for a simulated 41--44-year-old loblolly pine tree.
Component
Values from allometric equations (g C)
Model
% Estimate
Initial biomass
Final biomass
3-Year C gain
C Gain (g C)
Stem
Branch
Foliage
Class 1
Class 2
Root total
Coarse root total
Coarse root A
Coarse root B1
Fine root total
Fine root A
Fine root B1
Fine root B2
116267
13181
140421
18165
24154
4984
23741
4762
−1.7
−4.5
1391
1844
33225
29570
23360
6210
3654
2595
694
365
1742
2310
40869
36373
28735
7638
4496
3192
854
450
351
466
7644
6803
5375
1428
842
597
160
85
366
477
7470
6615
5238
1377
854
611
159
84
4.3
2.4
−2.3
−2.8
−2.5
−3.6
1.4
2.3
−0.6
−1.2
Total tree
165908
200507
37599
36816
−2.1
Total aboveground
132683
162638
29955
29346
−2.0
3-Year C gain = final biomass -- initial biomass.
% Estimate = ((model C Gain -- 3-year allometric C gain)/3-year allometric C gain)100.
Values represent g C (mass = 2 times g C).
Root total = coarse root total + fine root total.
Coarse root total = coarse root A + coarse root B1.
Fine root total = fine root A + fine root B1 + fine root B2.
Total tree = stem + branch + foliage + root total.
Total aboveground = stem + branch + foliage.
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630
CONSTABLE AND RETZLAFF
The soil rooting area of yellow poplar and loblolly pine (55.9
and 31.7 m2, respectively) was defined to be identical to the
projected crown area, assuming a crown radius of 4.2 and
3.2 m (Trimble and Tryon 1966, Smith et al. 1992) and a
uniform circular-shaped crown (cf. Retzlaff et al. 1996).
Depths of the A, B1, and B2 soil horizons were set to 0.2,
0.2, and 0.3 m, respectively, based on average measured soil
depths in southeastern loblolly pine stands (Harris et al. 1977,
Binkley et al. 1992, Richter et al. 1994) and a southeastern
yellow poplar forest (Harris et al. 1977). Soil water and nutrient conditions were set to be nonlimiting in all of the simulations.
values recorded by Cannon et al. (1993), Chappelka et al.
(1988), Gunderson et al. (1993), Neufeld et al. (1985), Norby
and O’Neill (1991), Tjoelker and Luxmoore (1992), and Wullschleger et al. (1992). Leaf respiration was set at 22% of net C
assimilation (Wullschleger et al. 1992, Cannon et al. 1993).
Loblolly pine net C assimilation for a midsummer 11-day
period at high irradiance (1000 µmol m −2 s −1; 25--30 °C) was
set to be approximately 0.0035 g C g −1 Cleaf h −1 (Cregg et al.
1993). Leaf respiration was set at 25% of net C assimilation
(Samuelson et al. 1992).
The final TREGRO simulated trees were calibrated by adjusting tissue growth rates and senescence rates in fine roots
until two conditions were met: (1) when the simulated C gain
of each of the tree components (foliage, branch, stem, and
coarse and fine roots) and the total tree C gain was within 10%
of the value for projected C gain from the literature-based
allometric relationships (Tables 1 and 2), and (2) when the
proportion of TNC and the ratio of structure to wood in each
of the tree components at the end of a simulation matched that
parameterized for the tree at the beginning of the simulation.
Fine root senescence was set to approximate one complete root
turnover per year for both species based on field measurements
(Harris et al. 1977).
Seasonal phenology
Ozone simulations
Initial seasonal foliage growth of mature yellow poplar trees
begins in mid-April and the majority (> 80%) of foliage is
produced by mid-July (Lamb 1915, Kienholz 1941). The remainder (≈ 20%) of the foliage biomass is produced during the
latter part of the growing season when conditions are favorable. Height and radial growth begin in mid-May (Kienholz
1941, Morrow and McKee 1963, Mowbray and Oosting 1968)
and continue until approximately mid-September (Morrow
and McKee 1963, Lieth and Radford 1971). Root growth
occurs from spring to fall when conditions are favorable (Harris et al. 1977). Foliage senescence occurs during the second
week in October (Lamb 1915). Yellow poplar trees senesce all
current foliage.
Mature loblolly pine trees produce two cohorts of foliage per
year with bud break of the first flush of foliage occurring in
early spring (Higginbotham 1974). The first flush ends in early
May and the second foliage flush initiates in mid-May and
continues until mid-June (Higginbotham 1974). Height and
radial growth begin soon after bud break of the first flush of
foliage and continue until late July (Miller et al. 1987). Root
growth occurs from spring to fall when conditions are favorable (Harris et al. 1977, Baker and Langdon 1990). Foliage
senescence occurs late in the season with needle-cast occurring
at the end of the growing season (approximately mid-November--early December) (Higginbotham 1974). Loblolly pine
trees senesce all 2-year-old foliage, retaining only current-year
foliage over winter.
In TREGRO, effects of O3 are simulated through a cumulative
effect of the pollutant on the maximum rate of photosynthesis,
Vmax . The magnitude of the O3 effect is controlled by a threshold of cumulative O3 uptake, below which there is no effect on
Vmax , and a linear decrease in Vmax above this threshold with
increasing cumulative uptake of O3. Although O3 does not
accumulate in the leaf tissue, the effect of cumulative O3
uptake is proportional to the sum of the hourly O3 concentration times the foliar rate of O3 conductance, because the primary avenue for O3 entry is through the stomata (Rubin et al.
1996).
To evaluate the effect of the maximum O3 response possible,
we assumed that Vmax began decreasing as soon as any O3
uptake occurred in the leaves (i.e., the O3 threshold was zero).
As the total amount of cumulative O3 uptake increased during
the growing season, we assumed a proportional decrease in
Vmax . The slope of the described response was set so that the
reduction in photosynthesis observed at the end of the open-top
chamber experiments matched the simulated reduction after a
similar cumulative uptake of O3 had occurred.
The yellow poplar response to O3 was set in the parameter
file according to the data of Cannon et al. (1993) (Figure 1),
who measured a 10% reduction in net photosynthesis of seedlings relative to charcoal-filtered air after a total cumulative O3
uptake of 0.0044 g g −1 Cleaf . The loblolly pine response to O3
was set in the parameter file according to the data of Sasek
et al. (1991) (Figure 1), who measured a 24% reduction in
current leaf net photosynthesis relative to that of seedlings in
charcoal-filtered air after a total cumulative O3 uptake of
0.0136 g g −1 C leaf .
In the simulation experiment, one short-term (8 day) peak
O3 episode was used in which O3 concentrations increased and
tioned into TNC, structure, and wood (in woody tissue). The
proportion of wood in the initial tree’s stem, branches, and
coarse (woody) roots (57%) was set to that reported for the
stem by Blanche et al. (1985). The remainder of the initial
biomass was divided between TNC and structure. The TNC
represented 30% of structure in the stem, branch, and coarse
roots and 20% of structure in the foliage based on reported
TNC concentrations in coarse roots, stem, and foliage of loblolly pine trees (Friend et al. 1992).
Soil parameters
Carbon assimilation
Yellow poplar net C assimilation for a midsummer 11-day
period at high irradiance (1000 µmol m −2 s −1; 25--30 °C) was
set to be approximately 0.0192 g C g −1 C leaf h −1, based on
TREE PHYSIOLOGY VOLUME 17, 1997
PHENOLOGICAL OZONE RESPONSE OF TREES
631
ured (1989) Oak Ridge, TN, ambient O3 concentrations (3 O3
concentrations × 7 meteorological files = 21 total simulations).
Use of a 0.0 × O3 exposure, although unrealistic in a field study,
permitted determination of the maximum O3 response possible.
Results and discussion
Matching phenology to reported values
Figure 1. Assumed relationships between cumulative O 3 uptake and
maximum C assimilation in yellow poplar and loblolly pine.
decreased in a normal diurnal pattern (for Oak Ridge, TN,
1989), with maximum O3 concentrations of 125 ppb for between 3 and 8 h per day (Figure 2). All meteorological data in
the Oak Ridge meteorological file, including the O3 concentrations, were used to create the 8-day O3 peak episode profile.
The peak O3 episode was placed in seven different (Oak Ridge,
TN, 1989) meteorological files to produce peak O3 exposures
centered on the first day of each month between April 1 and
October 1. To insert the peak O3 episode, we simply substituted
all the existing meteorological data during the insertion period
with the peak meteorological data thereby avoiding the problem of mismatching environmental and O3 data. However,
because the overwritten areas at different times of the year do
not contain identical recorded O3 concentrations, there is slight
variation (up to 3.7%) in the sum00 (sum00 = cumulative sum
of hourly O3 values during the growing season) O3 exposure
among files between the highest (123402 ppb⋅h) and lowest
(118975 ppb⋅h) sum exposure. During the 1989 growing season, in the absence of our artificial O3 peak, there were no
episodic periods of highly elevated O3 concentration (maximum recorded hourly concentration 88 ppb O3); however, O3
concentrations (up to 132 ppb) were measured at Oak Ridge,
TN, in 1988. Model simulations (3-year duration) were performed with each of these altered meteorological files using O3
concentrations of 0.0 (base case), 1.0, and 2.0 times the meas-
Figure 2. The 8-day peak ozone episode that was inserted at monthly
intervals into the 1989 Oak Ridge,TN meterological data file.
We matched phenology parameters in the base TREGRO trees
with those reported in the literature for both tree species. For
instance, mature loblolly pine trees produce two cohorts of
foliage per year with bud break of the first flush of foliage
occurring in the early spring (Day of Year (DOY) 60) and
ending on approximately DOY 135 (Higginbotham 1974). The
second foliage flush initiates on approximately DOY 135 and
continues until DOY 184 (Higginbotham 1974). Further, initial seasonal foliage growth of mature yellow poplar trees
begins on DOY 99 and the majority (> 80%) of the foliage is
produced by DOY 206 (Lamb 1915, Kienholz 1941). The
remainder (≈ 20%) of the foliage biomass is produced during
an additional period (DOY 207 to 246) of shoot growth. By
setting the initial base-tree parameters using this and other
phenological information, we were able to reproduce these
demographic patterns accurately with TREGRO (Figure 3).
Phenological development is a complex phenomenon governed by a suite of environmental cues. TREGRO duplicates
this process as controlled by the accumulation (from the start
of simulation) of heat degree-days above 0 °C. Therefore, we
were able to parameterize mature yellow poplar and loblolly
pine trees in TREGRO, simulate growth for a period of 3 years,
Figure 3. Phenograms from loblolly pine and yellow poplar TREGRO
parameter files. Horizontal bars represent periods in the simulations
when growth of the various compartments could occur if environmental conditions were favorable. Arrows correspond to the peak O 3
episode that elicited the maximum response as described by Figures
4--7.
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632
CONSTABLE AND RETZLAFF
and duplicate the dynamics of phenological processes that are
currently reported in the literature for individual yellow poplar
and loblolly pine trees. Accurate simulation of dynamic phenological processes with TREGRO permitted investigation of
the interaction between phenophase and episodic environmental (O3) stress.
Ozone simulations
In our simulations, the presence of atmospheric O3 (1.0 or 2.0
× ambient), regardless of timing of the peak O3 episode, reduced total tree C gain (Figure 4), coarse root C gain (Figure 5), and tree TNC compartments (Figure 6) compared to the
control trees of both species. Carbon gain of fine roots of both
species was not affected at 1.0 × ambient O3 (Figure 7).
Additionally, as the O3 concentration increased (to 2.0 × ambient), the O3 effects (reflected by additional reductions in total
tree, coarse root, fine root, and TNC C gain) became more
pronounced. Negative C gain of the coarse roots, TNC and fine
roots compartments reflects utilization of previously stored
TNC and root turnover without replacement, respectively. It is
known from field-exposure experiments that seedlings and
saplings of both species, and branches of mature loblolly pine
trees are sensitive to O3 (Chappelka et al. 1985, Chappelka
et al. 1988, Sasek et al. 1991, Tjoelker and Luxmoore 1992,
Cannon et al. 1993, Dizengremel et al. 1994, McLaughlin et al.
1994). However, the simulation experiment represents the first
time that the O3 responses of whole mature trees of these
species have been examined. McLaughlin and Downing
(1995) studied changes in loblolly pine stem diameter during
a 5-year period in the Oak Ridge, TN area, which included the
1989 conditions used in our modeling study, and found that
ambient exposure in the field in combination with elevated
Figure 4. Change in tree mass following a 3-year TREGRO simulation
of mature loblolly pine and yellow poplar trees with no O 3 exposure
and monthly peak O3 episodes. The response illustrated for the October peak O3 episode was identical to a 1.0 and 2.0 × ambient exposure
at this site with no peak O3 episode; therefore, values representing O 3
exposure without a peak episode are not shown.
Figure 5. Change in coarse root mass following a 3-year TREGRO
simulation of mature loblolly pine and yellow poplar trees with no O 3
exposure and monthly peak O3 episodes. Negative values reflect utilization of previously stored TNC.
temperature or low rainfall was associated with reduced stem
increment. We do not know whether our simulated estimates
of physiological responses accurately reflect the O3 response
that would occur in mature forest-grown trees. Hanson et al.
(1994) have shown that gas exchange of mature red oak (Quercus rubra L.) trees exposed to O3 is affected more by O3 than
similarly exposed red oak seedlings, indicating that caution
Figure 6. Change in total nonstructural carbohydrate (TNC) following
a 3-year TREGRO simulation of mature loblolly pine and yellow
poplar trees with no O3 exposure and monthly peak O3 episodes.
Negative values reflect utilization of previously stored TNC.
TREE PHYSIOLOGY VOLUME 17, 1997
PHENOLOGICAL OZONE RESPONSE OF TREES
Figure 7. Change in fine root mass following a 3-year TREGRO
simulation of mature loblolly pine and yellow poplar trees with no O 3
exposure and monthly peak O3 episodes. Negative values reflect fine
root senescence without replacement.
should be used when extrapolating the results of seedling
exposure experiments to mature trees. However, the nature of
our simulated responses (reduced root growth and TNC content of yellow poplar and loblolly pine trees) matches those
proposed in a conceptual model of O3 response (Cooley and
Manning 1987), observed in O3 experiments with woody
plants (see Tingey et al. 1976, Mortenson and Skyre 1990,
Retzlaff et al. 1992), and predicted in other simulation exercises (Retzlaff et al. 1996).
Carbon gain of yellow poplar (total tree, coarse root, and
TNC) was reduced by O3 to a greater extent than the corresponding compartments in loblolly pine, reflecting the fact that
we parameterized the C assimilation (e.g., yellow poplar:
Wullschleger et al. 1992 and loblolly pine: Cregg et al. 1993)
and the O3 (e.g., yellow poplar: Cannon et al. 1993 and loblolly
pine: Sasek et al. 1991) response parameters of the two species
according to field measurements (Figure 1) (i.e., we parameterized yellow poplar to be more sensitive to O3). This differential sensitivity to O3 has implications for the competition
between these two species as they co-occur and are exposed to
elevated concentrations of tropospheric O3 in the forest ecosystems in the southeastern USA.
Phenological O3 response
The simulated response illustrated for the October peak O3
episode was identical to a 1.0 and 2.0 × ambient exposure at
this site with no peak O3 episode; therefore, values representing O3 exposure without a peak episode are not shown.
Thus, the presence of peak O3 episodes differentially altered C
gain (Figure 4), and the growth of individual tree compart-
633
ments (Figures 5--7) independently of the atmospheric O3
concentration. Additionally, as the O3 concentration increased
to 2.0 × ambient, the effects corresponding to the timing of the
peak O3 episode became more pronounced. In our simulations,
the peak O3 episode in August caused the greatest reduction in
C gain in yellow poplar, whereas the peak O3 episode in July
caused the greatest reduction in C gain of loblolly pine. Timing
of the greatest simulated O3 effect corresponded with the
completion of the annual foliage production phenophase (and
therefore maximum C assimilating foliage area) on each of
these tree species (Figure 3). At the time of the July peak O3
episode, the simulated loblolly pine tree had reached the seasonal maximum photosynthetic foliage biomass. At the time of
the August peak O3 episode, the simulated yellow poplar tree
had produced approximately 90% of the seasonal maximum
photosynthetic foliage biomass.
Similar seasonal sensitivity responses have been noted previously for annual crops exposed to water stress (Eck et al.
1987, Halim et al. 1989, Stirling et al. 1989) and O3 (Blum and
Heck 1980, Kohut and Laurence 1983, McLaughlin and
McConathy 1983, Younglove et al. 1994). All of these studies
demonstrate sensitivity (e.g., reduced biomass and crop yield)
to the timing of the environmental stress, particularly when the
stress corresponds with critical phenological stages. Our simulation is the first study to link peak O3 episodes to a specific
phenophase in mature trees.
Our simulations of peak O3 episode events did not alter the
phenology of the two tree species. Date of initiation, patterns,
and durations of stem and fascicle elongation of loblolly pine
seedlings were not affected by O3 treatment (cf. Mudano et al.
1992). However in another study, loblolly pine seedlings exposed to 2.0 × ambient O3 exhibited a delay in fine root
production (Edwards et al. 1992). Atmospheric O3 will not
normally alter the timing of phenological events directly in
TREGRO because the timing of the occurrence of phenological events is driven by the accumulation (from the start of
simulation) of heat degree-days above 0 °C, a model feature
that is unrelated to O3 exposure. However, in our TREGRO
simulations, phenology could have been altered if sufficient
reductions in available C (current assimilate or stored TNC)
had occurred, thereby making C unavailable at the start of a
phenophase, or available C supplies were exhausted before
phenophase completion.
The TREGRO simulations demonstrate that there is a critical peak O3 exposure period for yellow poplar and loblolly
pine that is linked to the phenology of these two species. We
observed maximum O3 response when the peak O3 episode
occurred at or near the completion of the annual foliage production phenophase. Such simulation studies are useful in
identifying physiological responses to environmental stress
heretofore unavailable because of cost and other limitations.
Recent re-analysis of data from four field crop-loss yield trials
identified that growth-stage-dependent phenological weighting of pollutant exposure may result in more effective predictions of O3 exposure resulting in yield reductions (Younglove
et al. 1994). Results from similar studies could be used to
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634
CONSTABLE AND RETZLAFF
elucidate further the mechanism(s) of the phenological response of plants to environmental stress.
Acknowledgments
This research was conducted as part of research cooperative CR820759-02 between the USEPA, the University of Nevada, Reno, and
Boyce Thompson Institute for Plant Research. Additional funds were
provided by the Electric Power Research Institute (EPRI) and the
endowment of Boyce Thompson Institute for Plant Research. This
paper has not been subject to either USEPA or EPRI policy review and
should not be construed to represent policies of the agencies. We thank
Dr. D. Weinstein, Dr. G. Taylor, and Dr. R. Kohut for critical manuscript review, and B. Warland for word processing assistance.
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