Directory UMM :Data Elmu:jurnal:T:Tree Physiology:Vol16.1996:
Tree Physiology 16, 915--921
© 1996 Heron Publishing----Victoria, Canada
Simulated root dynamics of a 160-year-old sugar maple A
( cer
saccharum Marsh.) tree with and without ozone exposure using the
TREGRO model
W. A. RETZLAFF, D. A. WEINSTEIN, J. A. LAURENCE and B. GOLLANDS
Boyce Thompson Institute for Plant Research, Tower Road, Ithaca, NY 14853-1801, USA
Received October 25, 1995
Summary Because of difficulties in directly assessing root
responses of mature forest trees exposed to atmospheric pollutants, we have used the model TREGRO to analyze the effects
of a 3- and a 10-year exposure to ozone (O3) on root dynamics
of a simulated 160-year-old sugar maple (Acer saccharum
Marsh.) tree. We used existing phenological, allometric, and
growth data to parameterize TREGRO to produce a simulated
160-year-old tree. Simulations were based on literature values
for sugar maple fine root production and senescence and the
photosynthetic responses of sugar maple seedlings exposed to
O3 in open-top chambers.
In the simulated 3-year exposure to O3, 2 × ambient atmospheric O3 concentrations reduced net carbon (C) gain of the
160-year-old tree. This reduction occurred in the C storage
pools (total nonstructural carbohydrate, TNC), with most of
the reduction occurring in coarse (woody) roots. Total fine root
production and senescence were unaffected by the simulated
3-year exposure to O3. However, extending the simulated O3
exposure period to 10 years depleted the TNC pools of the
coarse roots and reduced total fine root production. Similar
reductions in TNC pools have been observed in forest-grown
sugar maple trees exhibiting symptoms of stress. We conclude
that modeling can aid in evaluating the belowground response
of mature forest trees to atmospheric pollution stress and could
indicate the potential for gradual deterioration of tree health
under conditions of long-term stress, a situation similar to that
underlying the decline of sugar maple trees.
Keywords: coarse roots, demographics, fine roots, senescence,
total nonstructural carbohydrates.
1992). Because the reduction in root mass may be the initial
damage that causes failure of other biotic systems leading to
decline, we hypothesized that ozone (O3) exposure alters root
dynamics in mature sugar maple trees.
In eastern North America, low concentrations of tropospheric O3 occur frequently over a wide area (National Academy of Sciences 1977). Several studies (Reich et al. 1986,
Noble et al. 1992, Laurence et al. 1993) have attempted to
quantify the response of sugar maple to increased concentrations of tropospheric O3 pollution; however, most of these
studies have focused on the response of aboveground tissue or
organs.
Fine roots are important, dynamic components of northern
hardwood ecosystems (Hendrick and Pregitzer 1993b), but
because of the difficulties associated with studying fine roots,
many aspects of fine root production and mortality are poorly
understood (Hendrick and Pregitzer 1993b). Fine root production and senescence have been estimated from sequential sampling of live root mass, which renders the sampling unit useless
for additional study. Recent advances in minirhizotron technology have permitted in situ estimates of fine root production
and turnover in these ecosystems (Hendrick and Pregitzer
1992, 1993a, 1993b, Fahey 1994).
We hypothesized that simulation models are an effective
tool for assessing the potential consequences of air pollution
exposure on root dynamics of mature forest trees. To test this
hypothesis we used the model TREGRO, developed and described by Weinstein et al. (1991), to assess the belowground
tissue responses of a simulated mature sugar maple tree with
and without O3 exposure.
Introduction
Materials and methods
Since the early 1980s, some sugar maple stands in the northern
hardwood forest of the northeastern United States (Allen et al.
1992) have shown signs of severe dieback and decline (Renaud
and Mauffette 1991). Several mechanisms, including air pollution stress, have been implicated as causal agents of the
decline. Under experimental conditions, air pollution stress is
capable of producing similar dieback symptoms, and in particular, it causes reductions in root mass of trees (Retzlaff et al.
Description of TREGRO
TREGRO is a physiological simulation model of the carbon
(C), water, and nutrient fluxes of an individual tree. 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 of these compartments,
the model tracks three C pools: structure (living, respiring
916
RETZLAFF ET AL.
tissue); wood (non-respiring tissue); and total nonstructural
carbohydrate (TNC). The model calculates the C assimilation
of the entire tree each hour as a function of ambient environmental conditions using the Farquhar equations (Farquhar et
al. 1980). Carbon is redistributed daily within the plant for
growth, storage, respiration, and senescence, depending on the
distance between source and sink and the relative sink strength.
Parameterization of TREGRO
We set the initial biomass of the simulated sugar maple tree,
including C partitioning among components, in the TREGRO
model. The simulation target was to grow a sugar maple tree
with three annual dbh (diameter at breast height) increments of
approximately 0.33 cm year −1. Utilizing dbh-based allometric
relationships, the biomass (in g of C, gC) of the base tree (32
cm dbh) and a target tree (33 cm dbh) were estimated (Table 1).
Initial tree biomass
Initial biomass of the sugar maple tree was based on the dbh
(32 cm) of dominant and codominant sugar maple trees measured by Fielding (1916) in Franklin and St. Lawrence Counties, NY. Trees of this dbh typically exhibit diameter growth of
2.8 to 3.6 cm in 10 years (Fielding 1916, Godman 1965,
Godman et al. 1990) and are approximately 150--160 years old
(Fielding 1916, Godman et al. 1990) with a height of 20 m
(Fielding 1916) and a mean crown radius of 3.2--3.6 m (Tucker
1990). Height growth ceases or becomes negligible at this age
(Godman et al. 1990).
Initial biomass of individual tree components (foliage,
branch, stem, and coarse and fine root) was calculated using
dbh-based allometric equations derived from sugar maple trees
growing in Ontario, Canada (belowground components) and
the Great Lakes Region of the USA (aboveground components) (Morrison 1990, Burton et al. 1991, Chapman and
Gower 1991). Leaf area was also calculated using dbh-based
allometric equations (Burton et al. 1991, Chapman and Gower
1991). Coarse root biomass was split equally between two soil
horizons, A and B1. Fifty percent of fine root (defined here as
roots < 2.0 mm diameter (Hendrick and Pregitzer 1993b))
biomass was allocated to soil horizon A and 25% to each of
soil horizons B1 and B2. Tree biomass in each component was
further partitioned into TNC, structure, and wood. The proportion of wood biomass (14%) in the initial tree’s stem, branches,
and coarse (woody) roots was set to that determined by Chapman and Gower (1991). The remainder of the initial biomass
was split between TNC and structure. Total nonstructural carbohydrate represented 30% of structure in the stem, branch,
and coarse roots and 20% of structure in the foliage; these
Table 1. Initial and final biomass and 3-year C gain values (g C, where mass = 2 × gC) from literature allometric data and the resulting TREGRO
modeled 3-year C gain and the percent estimate for a simulated 157--160-year-old sugar maple tree.
Component
Values from allometric equations
Stem
Model
Initial biomass
Final biomass
3-Year C gain1
C gain
(gC)
(gC)
(gC)
(gC)
% Estimate2
310,949
332,621
21,672
22,271
2.8
Branch
75,033
81,605
6,572
6,725
2.3
Foliage
8,292
8,696
404
404
0.0
50,095
53,104
3,009
3,066
1.9
Coarse root total
Coarse Root A
Coarse Root B1
36,569
18,285
18,285
38,766
19,383
19,383
2,197
1,098
1,098
2,217
1,045
1,172
0.9
--4.9
6.7
Fine root total5
Fine Root A
Fine Root B1
Fine Root B2
13,526
6,763
3,381
3,381
14,338
7,169
3,585
3,585
812
406
203
203
849
429
210
210
4.5
5.6
3.4
3.4
444,369
476,026
31,657
32,466
2.6
394,274
422,922
28,648
29,400
2.6
436,077
467,330
31,253
32,062
2.6
Root total3
4
Total tree6
7
Total aboveground
Total without foliage
1
2
3
4
5
6
7
8
8
3-Year C gain = Final biomass -- Initial biomass.
% Estimate = ((Model C gain -- 3-year Allometric C gain)/(3-Year Allometric C gain))100.
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 total.
Total without foliage = Stem + Branch + Root total.
SIMULATED ROOT DYNAMICS OF A SUGAR MAPLE TREE
values were based on reported TNC concentrations in coarse
roots (Wargo 1971, 1975, Renaud and Mauffette 1991, Kolb et
al. 1992), stem (Kolb et al. 1992), and foliage (M.A. Topa,
Boyce Thompson Institute for Plant Research, Ithaca, NY,
pers. comm.) of sugar maple trees.
Soil parameters
Because there are no competition effects for space in TREGRO, the soil rooting area (40.72 m2) was set to equal that of
the projected crown area, assuming a crown radius of 3.6 m
(Tucker 1990) and a uniform circular shaped crown. We recognize that, in a forest stand, the roots of many species would be
intermingled beneath the canopy, but the rooting area of a
particular tree would not exceed the crown area in a closed
canopy, assuming that similar sized trees have similar sized
root areas. If a tree has roots growing beyond the radius of its
canopy, it is likely that another tree is using a similar area
beneath the first tree canopy. Further, Tubbs (1977) found that
sugar maple roots usually terminated within a few feet of the
crown perimeter. Depths of the A, B1, and B2 soil horizons
were set to 0.118, 0.232, and 0.303 m, respectively, based on
measured soil depths in three old-growth sugar maple stands
(Frelich et al. 1989). Soil water and nutrient conditions were
set to be non-limiting in all of the simulations.
Seasonal phenology
Sugar maple trees produce a single cohort of foliage per year,
with foliage bud break and flush generally occurring in the first
half of May (Brundett and Kendrick 1988, Kolb and Teulon
1992, Kolb et al. 1992). Height and radial growth begin soon
after foliage bud break and continue for approximately 15--17
weeks, until the end of August (Godman et al. 1990). Root
growth occurs from spring to fall when conditions are favorable (Brundett and Kendrick 1988). Fine root production and
turnover occur simultaneously throughout the growing season
and overwinter production is low (Hendrick and Pregitzer
1992, 1993b). Foliage senescence occurs late in the season
with leaf fall occurring in mid-October (Reich et al. 1991).
TREGRO parameters were set to reproduce these phenological
events during the simulation. Ithaca, NY weather data from
1988 was used to convert the approximate calendar dates to
heat degree-day (days above 0 °C summed from day of year
(DOY) 1 to 365) values used to parameterize the model. The
same meteorological data set was used for all the TREGRO
model simulations.
Carbon assimilation
Net C assimilation (g of C per g of leaf C per h, gC glC--1 h--1)
during a high irradiance (1000 µmol m −2 s −1; 25--30 °C),
midsummer 11-day period (DOY 200--210) was set to be
approximately 0.0075 gC g lC--1 h --1 (cf. Ledig and Korbobo
1983, Bahari et al. 1985). Leaf respiration was set at 17% of
net C assimilation (cf. Walters et al. 1993).
The final TREGRO simulated tree was calibrated by adjusting tissue growth rates and fine root senescence rates until two
conditions were met: (1) the simulated C gain of each of the
tree components, foliage, branch, stem, and coarse and fine
917
roots, and the total tree C gain were within 10% of the value
for projected C gain from the literature-based allometric relationships; and (2) the proportion of TNC, structure, and 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 (Table 1). Fine root senescence was set to approximate one complete root turnover per year based on field measurements (Hendrick and Pregitzer 1992, 1993a, 1993b, Fahey
1994).
Ozone simulation
In TREGRO, effects of O3 are simulated as a cumulative effect
of the pollutant on the maximum rate of carboxylation, Vmax.
The magnitude of the O3 effect is controlled by a threshold
below which there is no effect, and a linear relationship between cumulative uptake of O3 and decreasing C assimilation.
Although O3 does not accumulate in the leaf tissue, the effect
of cumulative O3 uptake is proportional to the product of the
hourly O3 concentration multiplied by the O3 conductance.
There are conflicting reports of O3-induced reductions in foliage C assimilation of sugar maple seedlings grown under
greenhouse or growth chamber conditions (highly significant
reductions, Reich et al. 1986, Noble et al. 1992) and in opentop chambers (no significant reductions, Laurence et al. 1993).
The location of the experiment, the O3 exposure regimes, or
the genetic composition of the plant materials may explain
these contradictory results. Significant O3-induced reductions
in C assimilation by seedlings in greenhouse and growth chamber studies probably do not reflect the C assimilation response
in a field-grown tree. Laurence et al. (1993), in a highly
replicated open-top chamber study, observed a 12% reduction
in net C assimilation between field-grown sugar maple seedlings in 2 × ambient O3 and those in 0.5 × ambient O3 that was
not significant because of high variability. Furthermore, the
2× ambient O3 treatment did not cause a reduction in seedling
growth or biomass development.
To evaluate the effect of the maximum response possible, we
assumed that the maximum rate of carboxylation, Vmax, began
decreasing as soon as O3 uptake occurred in the leaves (i.e., the
O3 threshold was zero). Because the total amount of cumulative O3 uptake increased during the growing season, we assumed that there was a proportional decrease in Vmax for each
additional gram of O3 (g O 3) taken up by the leaves. The slope
of the response was set to match the maximum reduction
observed in open-top chambers by Laurence et al. (1993) (i.e.,
the instantaneous net C assimilation would be reduced by 12%
when the cumulative O3 dose reached 2 × ambient O3 concentration, which is equivalent to a total cumulative O3 uptake of
0.0252 g O 3 g lC−1). Based on this O3 response relationship, two
3-year simulations were run at O3 concentrations of 0 × (base
case, 0.0 ppb⋅h) and 2 × (296,632 ppb⋅h) ambient O3 concentrations in Ithaca, NY, in 1988. Use of a 0.0 ppb⋅h O3 exposure,
although unrealistic in a field study, permitted us to determine
the maximum response possible. We also extended the simulations for an additional 7 years for a total simulation period of
10 years with and without ozone exposure.
918
RETZLAFF ET AL.
Results and discussion
Matching root parameters to reported values
We tried to match root and other tissue parameters in the base
(no O3) TREGRO sugar maple tree with those reported in the
literature for phenology, TNC content, production, and senescence. In the base tree, we were able to reproduce all of the
expected tissue growth rates and patterns (Figure 1). For instance, sugar maple root growth is reported to occur from
spring to fall (Brundett and Kendrick 1988), with fine root
production and turnover occurring simultaneously throughout
the growing season and production continuing more slowly
over winter (Hendrick and Pregitzer 1992, 1993b). Further,
annual fine root production is greater than mortality in a
sugar-maple-dominated ecosystem (Hendrick and Pregitzer
1992, 1993b). By setting the initial base-tree parameters using
this information, we were able to reproduce these demographic
patterns accurately with TREGRO (Figure 1).
Our simulated estimate of fine root production was 6.94
MgDW (dry weight) ha −1 year −1, which approximates the value
of 7.30 MgDW ha −1 year −1 reported by Hendrick and Pregitzer
(1993b) for a sugar-maple-dominated northern ecosystem.
Fine root production (14.13 kgC) of the simulated sugar maple
tree was 1.7 and 6.3 times annual foliage (8.42 kgC) and branch
(2.25 kgC) production in the first simulation year, respectively.
In a sugar-maple-dominated ecosystem, fine root production
was roughly twice as high as foliage production (Hendrick and
Pregitzer 1993b, Fahey 1994) and six times higher than branch
production (Hendrick and Pregitzer 1993b). Further, 48% of
fine root biomass production occurred in our simulated tree by
DOY 200, which is similar to the reported value of greater than
50% of annual length production before midsummer in a
sugar-maple-dominated ecosystem (Hendrick and Pregitzer
1993b). The seasonal pattern of coarse root TNC of the simu-
Figure 1. Total mass, cumulative growth, and cumulative senescence
of fine roots from a three-year TREGRO simulation of a mature sugar
maple tree. The data shown represent growth with no O 3 exposure.
Data from an O3-exposed simulated tree were identical and are not
shown.
lated tree closely matched that reported by Wargo (1979)
(Figure 2A). Given the similarity between our simulated tree
and the literature values, we conclude that the allometry and
other parameters (including the meteorological data) used in
the simulation typify a mature sugar maple tree and its environment.
Our simulated estimate of fine root senescence was 6.80
MgDW ha −1 year −1, which is close to the value of 6.70 MgDW
ha −1 year −1 reported for a sugar-maple-dominated ecosystem
at 43° N (Hendrick and Pregitzer 1993b). The close similarity
in values is expected because we parameterized the model
using the fine root senesence rate from the 43° N ecosystem.
Hendrick and Pregitzer (1993a, 1993b) found a lower rate
(4.80 MgDW ha −1 year −1) in more northerly latitudes and attributed the difference in their estimates of fine root senescence
between the northern and southern sites to the higher soil
temperatures at the southern site (80 km south of the northern
site), causing accelerated maintenance costs and increased fine
root mortality rates. Our mean growing season soil temperatures (14.5 °C in our meteorological data set) were similar to
the soil temperatures (14.2--14.6 °C) in the sugar maple ecosystem at 43° N (Hendrick and Pregitzer 1993b). However, the
Figure 2. Percent capacity of coarse root TNC pools at the end of each
month during the last year of TREGRO simulations of a mature sugar
maple tree after three years with no O3 exposure (A) and after O3
exposure for 3 (B) and 10 (C) years. Percent TNC pool depletion was
calculated as 100 minus the monthly TNC capacity.
SIMULATED ROOT DYNAMICS OF A SUGAR MAPLE TREE
919
fine root senescence rate in TREGRO is not linked to soil
temperature (cf. Hendrick and Pregitzer 1993a); it is only
dependent on the current mass of fine root tissue.
We were able to parameterize a mature sugar maple tree in
TREGRO, simulate growth for a period of three years, and
approximate the dynamics of belowground physiological
processes that are reported in the literature for individual sugar
maple trees and ecosystems. Accurate simulation of the dynamics of physiological processes with TREGRO permits investigation of the physiological responses of trees to
environmental stress.
Ozone simulation
In the simulation, atmospheric O3 concentrations at twice the
(1988) Ithaca, NY ambient O3 concentration reduced the net C
gain of a 160-year-old simulated tree (Figure 3). The reduction
in C gain compared to the unexposed (0.0) tree increases each
year and the cumulative total reduction, or the average of the
3-year simulation, was 14%. This reduction occurred in the
storage (TNC) pool of the simulated tree, with the majority of
the reduction occurring in the coarse (woody) roots (Figures
2A, 2B, and 4). Similar reductions in TNC pools have been
observed in forest-grown sugar maple trees exhibiting symptoms of stress (decline or dieback). Sugar maple trees heavily
infested with pear thrips (Taeniothrips inconsequens (Uzel)
(Thysanoptera: Thripidae)) had less root TNC when measured
in the fall following attack compared with trees with less thrips
damage (Kolb et al. 1992). Further, October starch content of
stem and root tissues from sugar maple trees with more than
50% crown dieback was lower than that of trees with less than
10% crown dieback (Renaud and Mauffette 1991). Therefore,
the subtle response of the simulated sugar maple tree to atmospheric O3 stress may accurately reflect the response of forestgrown sugar maple trees to atmospheric O3 pollution.
Cooley and Manning (1987) proposed a conceptual model
to describe the effects of O3 on photosynthate partitioning in
plants. The model states that, under conditions of low concentrations of O3 (50--100 ppb), perennial plants divert photosyn-
Figure 3. Percent reduction in C gain of a mature sugar maple tree
exposed to 2 × ambient O3 concentrations during a 3-year TREGRO
model simulation.
Figure 4. Seasonal patterns of coarse root TNC pools from TREGRO
simulations of a mature sugar maple tree for 3 years with and without
O3 exposure.
thate assimilate to leaves at the expense of the roots, whereas
at higher O3 concentrations (>100 ppb), partitioning of C to all
sinks decreases because of a reduction in photosynthetic production. Our TREGRO model assumes that under moderate
reductions in photosynthesis (such as those produced in response to 50--100 ppb O3), the C needs of the aboveground
tissues will be satisfied first because they are closer to the site
of C fixation. The overall effect of this assumption is a simulated diversion of assimilate to aboveground tissues at the
expense of roots. Consequently, results from our TREGRO O3
simulation (seasonal mean O3 concentration was < 100 ppb)
mimic the proposed conceptual model in terms of the availability of C for the root (TNC) component. However, O3-induced
reductions in C gain and coarse root TNC pools did not alter
the dynamics of fine root phenology, production, or mortality
following the simulated 3-year exposure to O3 (see Figure 1).
If greater C reductions had occurred, thereby depriving fine
roots of additional C, then phenology, production, and mortality could have been altered. Even though simulated O3 exposure reduced the TNC content of the coarse roots after three
years (TNC content = 30% of structure when C pools are full
at the end of the growing season; TNC content = 17% of
capacity following O3 exposure), sufficient reserves remained
during the growing season for fine root production (Figures 2B
and 4). However, extending the simulated O3 exposure period
for an additional seven years (10-year total O3 exposure) resulted in depletion of the entire TNC pool in the coarse roots
during a portion of the growing season in the last three years
of simulation, causing a reduction in fine root production
compared to that in the unexposed base tree (Figures 2C and
5). Although TNC depletion was large by the end of the third
year and even larger by the end of the tenth year, no change in
fine root phenology and senescence occurred.
Because the simulated O3 regime reduced the amount of
TNC, but did not reduce the growth or structure of the coarse
roots, the TNC remaining at the end of the third and tenth years
920
RETZLAFF ET AL.
cence were not affected by simulated O3 exposure in this study.
Simulation exercises, like the one discussed here, are useful for
conducting long-term evaluations that could not be done experimentally. We conclude that modeling can aid in the belowground evaluation of mature forest tree responses to
atmospheric pollution stress (and other physiological stresses)
and could indicate the potential for gradual deterioration of
tree health (as evidenced by decreased TNC pools) under
conditions of extended stress, a situation similar to that underlying sugar maple decline.
Acknowledgments
Figure 5. Ten-year course of fine root biomass and coarse root TNC
from TREGRO simulations of a mature sugar maple tree with and
without O3 exposure.
of O3 exposure was less than in the unexposed base tree
(Figures 2B and 2C). This change in C partitioning agrees with
the assumptions of Cooley and Manning (1987) and the results
of a study on Pinus ponderosa Laws. seedlings (Tingey et al.
1976). However, contrary results (reduced C allocation, but no
changes in C partitioning) have been found in almond (Prunus
dulcis (Mill) D.A. Webb syn. P. amygdalus Batsch, cv. Butte
and Nonpareil) exposed to increased concentrations of O3
(Retzlaff et al. 1992). Our simulated response and results
presented elsewhere (Tingey et al. 1976, Mortenson and Skyre
1990, Retzlaff et al. 1992) indicate that the effect of O3 on
partitioning of dry matter will differ depending on the sensitivity of the plant to O3, the effect of C supply relative to demand,
and the O3 concentration to which the plants are exposed.
Therefore, it is important to have accurate estimates of the
biomass and C allocation responses for each species studied or
simulated. An understanding of the relative reduction in photosynthesis compared to C demand for growth will permit
predictions of when storage TNC reductions will lead to
growth declines.
We do not know whether our simulated estimates of belowground responses accurately reflect the response that would
occur in forest-grown trees. However, our results do show that
O3 has the potential to contribute to the decline in sugar maple
through reductions in coarse root TNC pools. Such reductions
have been observed in sugar maple trees exhibiting decline
symptoms. We conclude that our simulated O3 response mimics a proposed conceptual model and matches the measured
results of field studies with other species. It appears that the
physiological imbalances observed in declining trees may decrease the resistance of sugar maple to additional biotic and
abiotic stresses (Renaud and Mauffette 1991, Kolb et al. 1992).
Based on literature estimates of belowground root phenology,
TNC content, production, and mortality, the present modeling
effort indicates that long-term exposure to O3 may reduce TNC
storage pools in sugar maple coarse roots and ultimately decrease fine root production. Fine root phenology and senes-
This research was conducted as part of research cooperative CR820759-02 among the USEPA, the Desert Research Institute, and
Boyce Thompson Institute for Plant Research. Additional funds were
provided by the endowment of Boyce Thompson Institute for Plant
Research. This paper has not been subject to USEPA policy review and
should not be construed to represent policies of the agency. We thank
Drs. T. Fahey, M. A. Topa and R. Yanai for critical manuscript review,
and B. Warland for word processing assistance.
References
Allen, D.C., C.J. Barnett, I. Millers and D. LaChance. 1992. Temporal
change (1988--1990) in sugar maple health, and factors associated
with crown condition. Can. J. For. Res. 22:1776--1784.
Bahari, Z.A., S.G. Pallardy and W.C. Parker. 1985. Photosynthesis,
water relations, and drought adaptation in six woody species of
oak--hickory forests in central Missouri. For. Sci. 31:557--569.
Brundett, M.C. and B. Kendrick. 1988. The mycorrhizal status, root
anatomy, and phenology of plants in a sugar maple forest. Can. J.
Bot. 66:1153--1173.
Burton, A.J., K.S. Pregitzer and D.D. Reed. 1991. Leaf area and foliar
biomass relationships in northern hardwood forests located along a
800 km acid deposition gradient. For. Sci. 37:1041--1059.
Chapman, J.W. and S.T. Gower. 1991. Aboveground production and
canopy dynamics in sugar maple and red oak trees in southwestern
Wisconsin. Can. J. For. Res. 21:1533--1543.
Cooley, D.R. and W.J. Manning. 1987. The impact of ozone on
assimilate partitioning in plants: a review. Environ. Pollut. 47:95--113.
Fahey, T.J. 1994. Fine root dynamics in a northern hardwood forest
ecosystem, Hubbard Brook Experimental Forest, NH. J. Ecol.
82:533--548.
Farquhar, G.D., S. von Caemmerer and J.A. Berry. 1980. A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta 149:78--90.
Fielding, F.A. 1916. A silvicultural study of the hard maple. MS
Thesis, Cornell Univ., 73 p.
Frelich, L.E., J.G. Bockheim and J.E. Leide. 1989. Historical trends in
tree-ring growth and chemistry across an air quality gradient in
Wisconsin. Can. J. For. Res. 19:113--121.
Godman, R.M. 1965. Sugar maple (Acer saccharum Marsh.). In
Silvics of Forest Trees of the United States. Ed. H.A. Fowells.
USDA, Agriculture Handbook 271, Washington, DC, pp 66--73.
Godman, R.M., H.W. Yawney and C.H. Tubbs. 1990. Sugar maple
(Acer saccharum Marsh.). In Silvics of North America, Volume 2,
Hardwoods. Eds. R.M. Burns and B.H. Honkala. USDA Forest
Service, Agriculture Handbook 654, Washington, DC, pp 78--91.
Hendrick, R.L. and K.S. Pregitzer. 1992. The demography of fine roots
in a northern hardwood forest. Ecology 73:1094--1104.
Hendrick, R.L. and K.S. Pregitzer. 1993a. Patterns of fine root mortality in two sugar maple forests. Nature 361:59--61.
SIMULATED ROOT DYNAMICS OF A SUGAR MAPLE TREE
Hendrick, R.L. and K.S. Pregitzer. 1993b. The dynamics of fine root
length, biomass, and nitrogen content in two northern hardwood
ecosystems. Can. J. For. Res. 23:2507--2520.
Kolb, T.E., L.H. McCormick, E.E. Simons and D.J. Jeffery. 1992.
Impacts of pear thrips damage on root carbohydrate, sap, and crown
characteristics of sugar maples in a Pennsylvania sugarbush. For.
Sci. 38:381--392.
Kolb, T.E. and D.A.J. Teulon. 1992. Effects of temperature during bud
burst on pear thrips damage to sugar maple. Can. J. For. Res.
22:1147--1150.
Laurence, J.A., R.J. Kohut, R.G. Amundson, D.A. Weinstein and T.J.
Fahey. 1993. Response of plants to interacting stresses: an evaluation of the effects of ozone and acidic precipitation on the nutrition,
growth, and physiology of red spruce and sugar maple. Final Report, Electric Power Research Institute, 3412 Hillview Ave, Palo
Alto, CA, 104 p.
Ledig, F.T. and D.R. Korbobo. 1983. Adaptation of sugar maple
populations along altitudinal gradients: photosynthesis, respiration,
and specific leaf weight. Am. J. Bot. 70:256--265.
Morrison, I.K. 1990. Organic matter and mineral distribution in an
old-growth Acer saccharum forest near the northern limit of its
range. Can. J. For. Res. 20:1332--1342.
Mortenson, L.M. and O. Skyre. 1990. Effects of low ozone concentrations on growth of Betula pubescens Ehrh., Betula verrucosa Ehrh.
and Alnus incana (L.) Moench. New Phytol. 115:165--170.
National Academy of Sciences. 1977. Ozone and other photochemical
oxidants. Committee on Medical and Biological Effects of Environmental pollutants, Division of Medical Sciences, National Research
Council, Washington, DC, 719 p.
Noble, R., K.F. Jensen, B.S. Ruff and K. Loats. 1992. Response of
Acer saccharum seedlings to elevated carbon dioxide and ozone.
Ohio J. Sci. 92:60--62.
Reich, P.B., A.W. Schoettle and R.G. Amundson. 1986. Effects of O 3
and acidic rain on photosynthesis and growth in sugar maple and
northern red oak seedlings. Environ. Pollut. 40:1--15.
921
Reich, P.B., M.B. Walters and D.S. Ellsworth. 1991. Leaf age and
season influence the relationships between leaf nitrogen, leaf mass
per area and photosynthesis in maple and oak trees. Plant Cell
Environ. 14:251--259.
Renaud, J.-P. and Y. Mauffette. 1991. The relationships of crown
dieback with carbohydrate content and growth of sugar maple (Acer
saccharum). Can. J. For. Res. 21:1111--1118.
Retzlaff, W.A., T.M. DeJong and L.E. Williams. 1992. Photosynthesis
and growth response of almond to increased atmospheric ozone
partial pressures. J. Environ. Qual. 21:208--216.
Tingey, D.T., R.G. Wilhour and C. Standley. 1976. The effect of
chronic ozone exposures on the metabolite content of ponderosa
pine seedlings. For. Sci. 22:234--241.
Tubbs, C.H. 1977. Root-crown relations of young sugar maple and
yellow birch. USDA Forest Service North Central Forest Experiment Station, Research Note NC-225, 4 p.
Tucker, G.F. 1990. Crown architecture and xylem-borne sucrose production in stand-grown sugar maple (Acer saccharum Marsh.) of
the Adirondack Mountains. Ph.D. Diss., Cornell Univ., 148 p.
Walters, M.B., E.L. Kruger and P.B. Reich. 1993. Growth, biomass
distribution and CO2 exchange of northern hardwood seedlings in
high and low light: relationships with successional status and shade
tolerance. Oecologia 94:7--16.
Wargo, P.M. 1971. Seasonal changes in carbohydrate levels in roots of
sugar maple. USDA Forest Service, Northeastern Forest Experiment Station Research Paper NE-213, 8 p.
Wargo, P.M. 1975. Estimating starch content in roots of deciduous
trees----a visual technique. USDA Forest Service, Northeastern Forest Experiment Station Research Paper NE-313, 9 p.
Wargo, P.M. 1979. Starch storage and radial growth in woody roots of
sugar maple. Can. J. For. Res. 9:49--56.
Weinstein, D.A., R.M. Beloin and R.D. Yanai. 1991. Modeling
changes in red spruce carbon balance and allocation in response to
interacting ozone and nutrient stresses. Tree Physiol. 9:127--146.
© 1996 Heron Publishing----Victoria, Canada
Simulated root dynamics of a 160-year-old sugar maple A
( cer
saccharum Marsh.) tree with and without ozone exposure using the
TREGRO model
W. A. RETZLAFF, D. A. WEINSTEIN, J. A. LAURENCE and B. GOLLANDS
Boyce Thompson Institute for Plant Research, Tower Road, Ithaca, NY 14853-1801, USA
Received October 25, 1995
Summary Because of difficulties in directly assessing root
responses of mature forest trees exposed to atmospheric pollutants, we have used the model TREGRO to analyze the effects
of a 3- and a 10-year exposure to ozone (O3) on root dynamics
of a simulated 160-year-old sugar maple (Acer saccharum
Marsh.) tree. We used existing phenological, allometric, and
growth data to parameterize TREGRO to produce a simulated
160-year-old tree. Simulations were based on literature values
for sugar maple fine root production and senescence and the
photosynthetic responses of sugar maple seedlings exposed to
O3 in open-top chambers.
In the simulated 3-year exposure to O3, 2 × ambient atmospheric O3 concentrations reduced net carbon (C) gain of the
160-year-old tree. This reduction occurred in the C storage
pools (total nonstructural carbohydrate, TNC), with most of
the reduction occurring in coarse (woody) roots. Total fine root
production and senescence were unaffected by the simulated
3-year exposure to O3. However, extending the simulated O3
exposure period to 10 years depleted the TNC pools of the
coarse roots and reduced total fine root production. Similar
reductions in TNC pools have been observed in forest-grown
sugar maple trees exhibiting symptoms of stress. We conclude
that modeling can aid in evaluating the belowground response
of mature forest trees to atmospheric pollution stress and could
indicate the potential for gradual deterioration of tree health
under conditions of long-term stress, a situation similar to that
underlying the decline of sugar maple trees.
Keywords: coarse roots, demographics, fine roots, senescence,
total nonstructural carbohydrates.
1992). Because the reduction in root mass may be the initial
damage that causes failure of other biotic systems leading to
decline, we hypothesized that ozone (O3) exposure alters root
dynamics in mature sugar maple trees.
In eastern North America, low concentrations of tropospheric O3 occur frequently over a wide area (National Academy of Sciences 1977). Several studies (Reich et al. 1986,
Noble et al. 1992, Laurence et al. 1993) have attempted to
quantify the response of sugar maple to increased concentrations of tropospheric O3 pollution; however, most of these
studies have focused on the response of aboveground tissue or
organs.
Fine roots are important, dynamic components of northern
hardwood ecosystems (Hendrick and Pregitzer 1993b), but
because of the difficulties associated with studying fine roots,
many aspects of fine root production and mortality are poorly
understood (Hendrick and Pregitzer 1993b). Fine root production and senescence have been estimated from sequential sampling of live root mass, which renders the sampling unit useless
for additional study. Recent advances in minirhizotron technology have permitted in situ estimates of fine root production
and turnover in these ecosystems (Hendrick and Pregitzer
1992, 1993a, 1993b, Fahey 1994).
We hypothesized that simulation models are an effective
tool for assessing the potential consequences of air pollution
exposure on root dynamics of mature forest trees. To test this
hypothesis we used the model TREGRO, developed and described by Weinstein et al. (1991), to assess the belowground
tissue responses of a simulated mature sugar maple tree with
and without O3 exposure.
Introduction
Materials and methods
Since the early 1980s, some sugar maple stands in the northern
hardwood forest of the northeastern United States (Allen et al.
1992) have shown signs of severe dieback and decline (Renaud
and Mauffette 1991). Several mechanisms, including air pollution stress, have been implicated as causal agents of the
decline. Under experimental conditions, air pollution stress is
capable of producing similar dieback symptoms, and in particular, it causes reductions in root mass of trees (Retzlaff et al.
Description of TREGRO
TREGRO is a physiological simulation model of the carbon
(C), water, and nutrient fluxes of an individual tree. 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 of these compartments,
the model tracks three C pools: structure (living, respiring
916
RETZLAFF ET AL.
tissue); wood (non-respiring tissue); and total nonstructural
carbohydrate (TNC). The model calculates the C assimilation
of the entire tree each hour as a function of ambient environmental conditions using the Farquhar equations (Farquhar et
al. 1980). Carbon is redistributed daily within the plant for
growth, storage, respiration, and senescence, depending on the
distance between source and sink and the relative sink strength.
Parameterization of TREGRO
We set the initial biomass of the simulated sugar maple tree,
including C partitioning among components, in the TREGRO
model. The simulation target was to grow a sugar maple tree
with three annual dbh (diameter at breast height) increments of
approximately 0.33 cm year −1. Utilizing dbh-based allometric
relationships, the biomass (in g of C, gC) of the base tree (32
cm dbh) and a target tree (33 cm dbh) were estimated (Table 1).
Initial tree biomass
Initial biomass of the sugar maple tree was based on the dbh
(32 cm) of dominant and codominant sugar maple trees measured by Fielding (1916) in Franklin and St. Lawrence Counties, NY. Trees of this dbh typically exhibit diameter growth of
2.8 to 3.6 cm in 10 years (Fielding 1916, Godman 1965,
Godman et al. 1990) and are approximately 150--160 years old
(Fielding 1916, Godman et al. 1990) with a height of 20 m
(Fielding 1916) and a mean crown radius of 3.2--3.6 m (Tucker
1990). Height growth ceases or becomes negligible at this age
(Godman et al. 1990).
Initial biomass of individual tree components (foliage,
branch, stem, and coarse and fine root) was calculated using
dbh-based allometric equations derived from sugar maple trees
growing in Ontario, Canada (belowground components) and
the Great Lakes Region of the USA (aboveground components) (Morrison 1990, Burton et al. 1991, Chapman and
Gower 1991). Leaf area was also calculated using dbh-based
allometric equations (Burton et al. 1991, Chapman and Gower
1991). Coarse root biomass was split equally between two soil
horizons, A and B1. Fifty percent of fine root (defined here as
roots < 2.0 mm diameter (Hendrick and Pregitzer 1993b))
biomass was allocated to soil horizon A and 25% to each of
soil horizons B1 and B2. Tree biomass in each component was
further partitioned into TNC, structure, and wood. The proportion of wood biomass (14%) in the initial tree’s stem, branches,
and coarse (woody) roots was set to that determined by Chapman and Gower (1991). The remainder of the initial biomass
was split between TNC and structure. Total nonstructural carbohydrate represented 30% of structure in the stem, branch,
and coarse roots and 20% of structure in the foliage; these
Table 1. Initial and final biomass and 3-year C gain values (g C, where mass = 2 × gC) from literature allometric data and the resulting TREGRO
modeled 3-year C gain and the percent estimate for a simulated 157--160-year-old sugar maple tree.
Component
Values from allometric equations
Stem
Model
Initial biomass
Final biomass
3-Year C gain1
C gain
(gC)
(gC)
(gC)
(gC)
% Estimate2
310,949
332,621
21,672
22,271
2.8
Branch
75,033
81,605
6,572
6,725
2.3
Foliage
8,292
8,696
404
404
0.0
50,095
53,104
3,009
3,066
1.9
Coarse root total
Coarse Root A
Coarse Root B1
36,569
18,285
18,285
38,766
19,383
19,383
2,197
1,098
1,098
2,217
1,045
1,172
0.9
--4.9
6.7
Fine root total5
Fine Root A
Fine Root B1
Fine Root B2
13,526
6,763
3,381
3,381
14,338
7,169
3,585
3,585
812
406
203
203
849
429
210
210
4.5
5.6
3.4
3.4
444,369
476,026
31,657
32,466
2.6
394,274
422,922
28,648
29,400
2.6
436,077
467,330
31,253
32,062
2.6
Root total3
4
Total tree6
7
Total aboveground
Total without foliage
1
2
3
4
5
6
7
8
8
3-Year C gain = Final biomass -- Initial biomass.
% Estimate = ((Model C gain -- 3-year Allometric C gain)/(3-Year Allometric C gain))100.
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 total.
Total without foliage = Stem + Branch + Root total.
SIMULATED ROOT DYNAMICS OF A SUGAR MAPLE TREE
values were based on reported TNC concentrations in coarse
roots (Wargo 1971, 1975, Renaud and Mauffette 1991, Kolb et
al. 1992), stem (Kolb et al. 1992), and foliage (M.A. Topa,
Boyce Thompson Institute for Plant Research, Ithaca, NY,
pers. comm.) of sugar maple trees.
Soil parameters
Because there are no competition effects for space in TREGRO, the soil rooting area (40.72 m2) was set to equal that of
the projected crown area, assuming a crown radius of 3.6 m
(Tucker 1990) and a uniform circular shaped crown. We recognize that, in a forest stand, the roots of many species would be
intermingled beneath the canopy, but the rooting area of a
particular tree would not exceed the crown area in a closed
canopy, assuming that similar sized trees have similar sized
root areas. If a tree has roots growing beyond the radius of its
canopy, it is likely that another tree is using a similar area
beneath the first tree canopy. Further, Tubbs (1977) found that
sugar maple roots usually terminated within a few feet of the
crown perimeter. Depths of the A, B1, and B2 soil horizons
were set to 0.118, 0.232, and 0.303 m, respectively, based on
measured soil depths in three old-growth sugar maple stands
(Frelich et al. 1989). Soil water and nutrient conditions were
set to be non-limiting in all of the simulations.
Seasonal phenology
Sugar maple trees produce a single cohort of foliage per year,
with foliage bud break and flush generally occurring in the first
half of May (Brundett and Kendrick 1988, Kolb and Teulon
1992, Kolb et al. 1992). Height and radial growth begin soon
after foliage bud break and continue for approximately 15--17
weeks, until the end of August (Godman et al. 1990). Root
growth occurs from spring to fall when conditions are favorable (Brundett and Kendrick 1988). Fine root production and
turnover occur simultaneously throughout the growing season
and overwinter production is low (Hendrick and Pregitzer
1992, 1993b). Foliage senescence occurs late in the season
with leaf fall occurring in mid-October (Reich et al. 1991).
TREGRO parameters were set to reproduce these phenological
events during the simulation. Ithaca, NY weather data from
1988 was used to convert the approximate calendar dates to
heat degree-day (days above 0 °C summed from day of year
(DOY) 1 to 365) values used to parameterize the model. The
same meteorological data set was used for all the TREGRO
model simulations.
Carbon assimilation
Net C assimilation (g of C per g of leaf C per h, gC glC--1 h--1)
during a high irradiance (1000 µmol m −2 s −1; 25--30 °C),
midsummer 11-day period (DOY 200--210) was set to be
approximately 0.0075 gC g lC--1 h --1 (cf. Ledig and Korbobo
1983, Bahari et al. 1985). Leaf respiration was set at 17% of
net C assimilation (cf. Walters et al. 1993).
The final TREGRO simulated tree was calibrated by adjusting tissue growth rates and fine root senescence rates until two
conditions were met: (1) the simulated C gain of each of the
tree components, foliage, branch, stem, and coarse and fine
917
roots, and the total tree C gain were within 10% of the value
for projected C gain from the literature-based allometric relationships; and (2) the proportion of TNC, structure, and 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 (Table 1). Fine root senescence was set to approximate one complete root turnover per year based on field measurements (Hendrick and Pregitzer 1992, 1993a, 1993b, Fahey
1994).
Ozone simulation
In TREGRO, effects of O3 are simulated as a cumulative effect
of the pollutant on the maximum rate of carboxylation, Vmax.
The magnitude of the O3 effect is controlled by a threshold
below which there is no effect, and a linear relationship between cumulative uptake of O3 and decreasing C assimilation.
Although O3 does not accumulate in the leaf tissue, the effect
of cumulative O3 uptake is proportional to the product of the
hourly O3 concentration multiplied by the O3 conductance.
There are conflicting reports of O3-induced reductions in foliage C assimilation of sugar maple seedlings grown under
greenhouse or growth chamber conditions (highly significant
reductions, Reich et al. 1986, Noble et al. 1992) and in opentop chambers (no significant reductions, Laurence et al. 1993).
The location of the experiment, the O3 exposure regimes, or
the genetic composition of the plant materials may explain
these contradictory results. Significant O3-induced reductions
in C assimilation by seedlings in greenhouse and growth chamber studies probably do not reflect the C assimilation response
in a field-grown tree. Laurence et al. (1993), in a highly
replicated open-top chamber study, observed a 12% reduction
in net C assimilation between field-grown sugar maple seedlings in 2 × ambient O3 and those in 0.5 × ambient O3 that was
not significant because of high variability. Furthermore, the
2× ambient O3 treatment did not cause a reduction in seedling
growth or biomass development.
To evaluate the effect of the maximum response possible, we
assumed that the maximum rate of carboxylation, Vmax, began
decreasing as soon as O3 uptake occurred in the leaves (i.e., the
O3 threshold was zero). Because the total amount of cumulative O3 uptake increased during the growing season, we assumed that there was a proportional decrease in Vmax for each
additional gram of O3 (g O 3) taken up by the leaves. The slope
of the response was set to match the maximum reduction
observed in open-top chambers by Laurence et al. (1993) (i.e.,
the instantaneous net C assimilation would be reduced by 12%
when the cumulative O3 dose reached 2 × ambient O3 concentration, which is equivalent to a total cumulative O3 uptake of
0.0252 g O 3 g lC−1). Based on this O3 response relationship, two
3-year simulations were run at O3 concentrations of 0 × (base
case, 0.0 ppb⋅h) and 2 × (296,632 ppb⋅h) ambient O3 concentrations in Ithaca, NY, in 1988. Use of a 0.0 ppb⋅h O3 exposure,
although unrealistic in a field study, permitted us to determine
the maximum response possible. We also extended the simulations for an additional 7 years for a total simulation period of
10 years with and without ozone exposure.
918
RETZLAFF ET AL.
Results and discussion
Matching root parameters to reported values
We tried to match root and other tissue parameters in the base
(no O3) TREGRO sugar maple tree with those reported in the
literature for phenology, TNC content, production, and senescence. In the base tree, we were able to reproduce all of the
expected tissue growth rates and patterns (Figure 1). For instance, sugar maple root growth is reported to occur from
spring to fall (Brundett and Kendrick 1988), with fine root
production and turnover occurring simultaneously throughout
the growing season and production continuing more slowly
over winter (Hendrick and Pregitzer 1992, 1993b). Further,
annual fine root production is greater than mortality in a
sugar-maple-dominated ecosystem (Hendrick and Pregitzer
1992, 1993b). By setting the initial base-tree parameters using
this information, we were able to reproduce these demographic
patterns accurately with TREGRO (Figure 1).
Our simulated estimate of fine root production was 6.94
MgDW (dry weight) ha −1 year −1, which approximates the value
of 7.30 MgDW ha −1 year −1 reported by Hendrick and Pregitzer
(1993b) for a sugar-maple-dominated northern ecosystem.
Fine root production (14.13 kgC) of the simulated sugar maple
tree was 1.7 and 6.3 times annual foliage (8.42 kgC) and branch
(2.25 kgC) production in the first simulation year, respectively.
In a sugar-maple-dominated ecosystem, fine root production
was roughly twice as high as foliage production (Hendrick and
Pregitzer 1993b, Fahey 1994) and six times higher than branch
production (Hendrick and Pregitzer 1993b). Further, 48% of
fine root biomass production occurred in our simulated tree by
DOY 200, which is similar to the reported value of greater than
50% of annual length production before midsummer in a
sugar-maple-dominated ecosystem (Hendrick and Pregitzer
1993b). The seasonal pattern of coarse root TNC of the simu-
Figure 1. Total mass, cumulative growth, and cumulative senescence
of fine roots from a three-year TREGRO simulation of a mature sugar
maple tree. The data shown represent growth with no O 3 exposure.
Data from an O3-exposed simulated tree were identical and are not
shown.
lated tree closely matched that reported by Wargo (1979)
(Figure 2A). Given the similarity between our simulated tree
and the literature values, we conclude that the allometry and
other parameters (including the meteorological data) used in
the simulation typify a mature sugar maple tree and its environment.
Our simulated estimate of fine root senescence was 6.80
MgDW ha −1 year −1, which is close to the value of 6.70 MgDW
ha −1 year −1 reported for a sugar-maple-dominated ecosystem
at 43° N (Hendrick and Pregitzer 1993b). The close similarity
in values is expected because we parameterized the model
using the fine root senesence rate from the 43° N ecosystem.
Hendrick and Pregitzer (1993a, 1993b) found a lower rate
(4.80 MgDW ha −1 year −1) in more northerly latitudes and attributed the difference in their estimates of fine root senescence
between the northern and southern sites to the higher soil
temperatures at the southern site (80 km south of the northern
site), causing accelerated maintenance costs and increased fine
root mortality rates. Our mean growing season soil temperatures (14.5 °C in our meteorological data set) were similar to
the soil temperatures (14.2--14.6 °C) in the sugar maple ecosystem at 43° N (Hendrick and Pregitzer 1993b). However, the
Figure 2. Percent capacity of coarse root TNC pools at the end of each
month during the last year of TREGRO simulations of a mature sugar
maple tree after three years with no O3 exposure (A) and after O3
exposure for 3 (B) and 10 (C) years. Percent TNC pool depletion was
calculated as 100 minus the monthly TNC capacity.
SIMULATED ROOT DYNAMICS OF A SUGAR MAPLE TREE
919
fine root senescence rate in TREGRO is not linked to soil
temperature (cf. Hendrick and Pregitzer 1993a); it is only
dependent on the current mass of fine root tissue.
We were able to parameterize a mature sugar maple tree in
TREGRO, simulate growth for a period of three years, and
approximate the dynamics of belowground physiological
processes that are reported in the literature for individual sugar
maple trees and ecosystems. Accurate simulation of the dynamics of physiological processes with TREGRO permits investigation of the physiological responses of trees to
environmental stress.
Ozone simulation
In the simulation, atmospheric O3 concentrations at twice the
(1988) Ithaca, NY ambient O3 concentration reduced the net C
gain of a 160-year-old simulated tree (Figure 3). The reduction
in C gain compared to the unexposed (0.0) tree increases each
year and the cumulative total reduction, or the average of the
3-year simulation, was 14%. This reduction occurred in the
storage (TNC) pool of the simulated tree, with the majority of
the reduction occurring in the coarse (woody) roots (Figures
2A, 2B, and 4). Similar reductions in TNC pools have been
observed in forest-grown sugar maple trees exhibiting symptoms of stress (decline or dieback). Sugar maple trees heavily
infested with pear thrips (Taeniothrips inconsequens (Uzel)
(Thysanoptera: Thripidae)) had less root TNC when measured
in the fall following attack compared with trees with less thrips
damage (Kolb et al. 1992). Further, October starch content of
stem and root tissues from sugar maple trees with more than
50% crown dieback was lower than that of trees with less than
10% crown dieback (Renaud and Mauffette 1991). Therefore,
the subtle response of the simulated sugar maple tree to atmospheric O3 stress may accurately reflect the response of forestgrown sugar maple trees to atmospheric O3 pollution.
Cooley and Manning (1987) proposed a conceptual model
to describe the effects of O3 on photosynthate partitioning in
plants. The model states that, under conditions of low concentrations of O3 (50--100 ppb), perennial plants divert photosyn-
Figure 3. Percent reduction in C gain of a mature sugar maple tree
exposed to 2 × ambient O3 concentrations during a 3-year TREGRO
model simulation.
Figure 4. Seasonal patterns of coarse root TNC pools from TREGRO
simulations of a mature sugar maple tree for 3 years with and without
O3 exposure.
thate assimilate to leaves at the expense of the roots, whereas
at higher O3 concentrations (>100 ppb), partitioning of C to all
sinks decreases because of a reduction in photosynthetic production. Our TREGRO model assumes that under moderate
reductions in photosynthesis (such as those produced in response to 50--100 ppb O3), the C needs of the aboveground
tissues will be satisfied first because they are closer to the site
of C fixation. The overall effect of this assumption is a simulated diversion of assimilate to aboveground tissues at the
expense of roots. Consequently, results from our TREGRO O3
simulation (seasonal mean O3 concentration was < 100 ppb)
mimic the proposed conceptual model in terms of the availability of C for the root (TNC) component. However, O3-induced
reductions in C gain and coarse root TNC pools did not alter
the dynamics of fine root phenology, production, or mortality
following the simulated 3-year exposure to O3 (see Figure 1).
If greater C reductions had occurred, thereby depriving fine
roots of additional C, then phenology, production, and mortality could have been altered. Even though simulated O3 exposure reduced the TNC content of the coarse roots after three
years (TNC content = 30% of structure when C pools are full
at the end of the growing season; TNC content = 17% of
capacity following O3 exposure), sufficient reserves remained
during the growing season for fine root production (Figures 2B
and 4). However, extending the simulated O3 exposure period
for an additional seven years (10-year total O3 exposure) resulted in depletion of the entire TNC pool in the coarse roots
during a portion of the growing season in the last three years
of simulation, causing a reduction in fine root production
compared to that in the unexposed base tree (Figures 2C and
5). Although TNC depletion was large by the end of the third
year and even larger by the end of the tenth year, no change in
fine root phenology and senescence occurred.
Because the simulated O3 regime reduced the amount of
TNC, but did not reduce the growth or structure of the coarse
roots, the TNC remaining at the end of the third and tenth years
920
RETZLAFF ET AL.
cence were not affected by simulated O3 exposure in this study.
Simulation exercises, like the one discussed here, are useful for
conducting long-term evaluations that could not be done experimentally. We conclude that modeling can aid in the belowground evaluation of mature forest tree responses to
atmospheric pollution stress (and other physiological stresses)
and could indicate the potential for gradual deterioration of
tree health (as evidenced by decreased TNC pools) under
conditions of extended stress, a situation similar to that underlying sugar maple decline.
Acknowledgments
Figure 5. Ten-year course of fine root biomass and coarse root TNC
from TREGRO simulations of a mature sugar maple tree with and
without O3 exposure.
of O3 exposure was less than in the unexposed base tree
(Figures 2B and 2C). This change in C partitioning agrees with
the assumptions of Cooley and Manning (1987) and the results
of a study on Pinus ponderosa Laws. seedlings (Tingey et al.
1976). However, contrary results (reduced C allocation, but no
changes in C partitioning) have been found in almond (Prunus
dulcis (Mill) D.A. Webb syn. P. amygdalus Batsch, cv. Butte
and Nonpareil) exposed to increased concentrations of O3
(Retzlaff et al. 1992). Our simulated response and results
presented elsewhere (Tingey et al. 1976, Mortenson and Skyre
1990, Retzlaff et al. 1992) indicate that the effect of O3 on
partitioning of dry matter will differ depending on the sensitivity of the plant to O3, the effect of C supply relative to demand,
and the O3 concentration to which the plants are exposed.
Therefore, it is important to have accurate estimates of the
biomass and C allocation responses for each species studied or
simulated. An understanding of the relative reduction in photosynthesis compared to C demand for growth will permit
predictions of when storage TNC reductions will lead to
growth declines.
We do not know whether our simulated estimates of belowground responses accurately reflect the response that would
occur in forest-grown trees. However, our results do show that
O3 has the potential to contribute to the decline in sugar maple
through reductions in coarse root TNC pools. Such reductions
have been observed in sugar maple trees exhibiting decline
symptoms. We conclude that our simulated O3 response mimics a proposed conceptual model and matches the measured
results of field studies with other species. It appears that the
physiological imbalances observed in declining trees may decrease the resistance of sugar maple to additional biotic and
abiotic stresses (Renaud and Mauffette 1991, Kolb et al. 1992).
Based on literature estimates of belowground root phenology,
TNC content, production, and mortality, the present modeling
effort indicates that long-term exposure to O3 may reduce TNC
storage pools in sugar maple coarse roots and ultimately decrease fine root production. Fine root phenology and senes-
This research was conducted as part of research cooperative CR820759-02 among the USEPA, the Desert Research Institute, and
Boyce Thompson Institute for Plant Research. Additional funds were
provided by the endowment of Boyce Thompson Institute for Plant
Research. This paper has not been subject to USEPA policy review and
should not be construed to represent policies of the agency. We thank
Drs. T. Fahey, M. A. Topa and R. Yanai for critical manuscript review,
and B. Warland for word processing assistance.
References
Allen, D.C., C.J. Barnett, I. Millers and D. LaChance. 1992. Temporal
change (1988--1990) in sugar maple health, and factors associated
with crown condition. Can. J. For. Res. 22:1776--1784.
Bahari, Z.A., S.G. Pallardy and W.C. Parker. 1985. Photosynthesis,
water relations, and drought adaptation in six woody species of
oak--hickory forests in central Missouri. For. Sci. 31:557--569.
Brundett, M.C. and B. Kendrick. 1988. The mycorrhizal status, root
anatomy, and phenology of plants in a sugar maple forest. Can. J.
Bot. 66:1153--1173.
Burton, A.J., K.S. Pregitzer and D.D. Reed. 1991. Leaf area and foliar
biomass relationships in northern hardwood forests located along a
800 km acid deposition gradient. For. Sci. 37:1041--1059.
Chapman, J.W. and S.T. Gower. 1991. Aboveground production and
canopy dynamics in sugar maple and red oak trees in southwestern
Wisconsin. Can. J. For. Res. 21:1533--1543.
Cooley, D.R. and W.J. Manning. 1987. The impact of ozone on
assimilate partitioning in plants: a review. Environ. Pollut. 47:95--113.
Fahey, T.J. 1994. Fine root dynamics in a northern hardwood forest
ecosystem, Hubbard Brook Experimental Forest, NH. J. Ecol.
82:533--548.
Farquhar, G.D., S. von Caemmerer and J.A. Berry. 1980. A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta 149:78--90.
Fielding, F.A. 1916. A silvicultural study of the hard maple. MS
Thesis, Cornell Univ., 73 p.
Frelich, L.E., J.G. Bockheim and J.E. Leide. 1989. Historical trends in
tree-ring growth and chemistry across an air quality gradient in
Wisconsin. Can. J. For. Res. 19:113--121.
Godman, R.M. 1965. Sugar maple (Acer saccharum Marsh.). In
Silvics of Forest Trees of the United States. Ed. H.A. Fowells.
USDA, Agriculture Handbook 271, Washington, DC, pp 66--73.
Godman, R.M., H.W. Yawney and C.H. Tubbs. 1990. Sugar maple
(Acer saccharum Marsh.). In Silvics of North America, Volume 2,
Hardwoods. Eds. R.M. Burns and B.H. Honkala. USDA Forest
Service, Agriculture Handbook 654, Washington, DC, pp 78--91.
Hendrick, R.L. and K.S. Pregitzer. 1992. The demography of fine roots
in a northern hardwood forest. Ecology 73:1094--1104.
Hendrick, R.L. and K.S. Pregitzer. 1993a. Patterns of fine root mortality in two sugar maple forests. Nature 361:59--61.
SIMULATED ROOT DYNAMICS OF A SUGAR MAPLE TREE
Hendrick, R.L. and K.S. Pregitzer. 1993b. The dynamics of fine root
length, biomass, and nitrogen content in two northern hardwood
ecosystems. Can. J. For. Res. 23:2507--2520.
Kolb, T.E., L.H. McCormick, E.E. Simons and D.J. Jeffery. 1992.
Impacts of pear thrips damage on root carbohydrate, sap, and crown
characteristics of sugar maples in a Pennsylvania sugarbush. For.
Sci. 38:381--392.
Kolb, T.E. and D.A.J. Teulon. 1992. Effects of temperature during bud
burst on pear thrips damage to sugar maple. Can. J. For. Res.
22:1147--1150.
Laurence, J.A., R.J. Kohut, R.G. Amundson, D.A. Weinstein and T.J.
Fahey. 1993. Response of plants to interacting stresses: an evaluation of the effects of ozone and acidic precipitation on the nutrition,
growth, and physiology of red spruce and sugar maple. Final Report, Electric Power Research Institute, 3412 Hillview Ave, Palo
Alto, CA, 104 p.
Ledig, F.T. and D.R. Korbobo. 1983. Adaptation of sugar maple
populations along altitudinal gradients: photosynthesis, respiration,
and specific leaf weight. Am. J. Bot. 70:256--265.
Morrison, I.K. 1990. Organic matter and mineral distribution in an
old-growth Acer saccharum forest near the northern limit of its
range. Can. J. For. Res. 20:1332--1342.
Mortenson, L.M. and O. Skyre. 1990. Effects of low ozone concentrations on growth of Betula pubescens Ehrh., Betula verrucosa Ehrh.
and Alnus incana (L.) Moench. New Phytol. 115:165--170.
National Academy of Sciences. 1977. Ozone and other photochemical
oxidants. Committee on Medical and Biological Effects of Environmental pollutants, Division of Medical Sciences, National Research
Council, Washington, DC, 719 p.
Noble, R., K.F. Jensen, B.S. Ruff and K. Loats. 1992. Response of
Acer saccharum seedlings to elevated carbon dioxide and ozone.
Ohio J. Sci. 92:60--62.
Reich, P.B., A.W. Schoettle and R.G. Amundson. 1986. Effects of O 3
and acidic rain on photosynthesis and growth in sugar maple and
northern red oak seedlings. Environ. Pollut. 40:1--15.
921
Reich, P.B., M.B. Walters and D.S. Ellsworth. 1991. Leaf age and
season influence the relationships between leaf nitrogen, leaf mass
per area and photosynthesis in maple and oak trees. Plant Cell
Environ. 14:251--259.
Renaud, J.-P. and Y. Mauffette. 1991. The relationships of crown
dieback with carbohydrate content and growth of sugar maple (Acer
saccharum). Can. J. For. Res. 21:1111--1118.
Retzlaff, W.A., T.M. DeJong and L.E. Williams. 1992. Photosynthesis
and growth response of almond to increased atmospheric ozone
partial pressures. J. Environ. Qual. 21:208--216.
Tingey, D.T., R.G. Wilhour and C. Standley. 1976. The effect of
chronic ozone exposures on the metabolite content of ponderosa
pine seedlings. For. Sci. 22:234--241.
Tubbs, C.H. 1977. Root-crown relations of young sugar maple and
yellow birch. USDA Forest Service North Central Forest Experiment Station, Research Note NC-225, 4 p.
Tucker, G.F. 1990. Crown architecture and xylem-borne sucrose production in stand-grown sugar maple (Acer saccharum Marsh.) of
the Adirondack Mountains. Ph.D. Diss., Cornell Univ., 148 p.
Walters, M.B., E.L. Kruger and P.B. Reich. 1993. Growth, biomass
distribution and CO2 exchange of northern hardwood seedlings in
high and low light: relationships with successional status and shade
tolerance. Oecologia 94:7--16.
Wargo, P.M. 1971. Seasonal changes in carbohydrate levels in roots of
sugar maple. USDA Forest Service, Northeastern Forest Experiment Station Research Paper NE-213, 8 p.
Wargo, P.M. 1975. Estimating starch content in roots of deciduous
trees----a visual technique. USDA Forest Service, Northeastern Forest Experiment Station Research Paper NE-313, 9 p.
Wargo, P.M. 1979. Starch storage and radial growth in woody roots of
sugar maple. Can. J. For. Res. 9:49--56.
Weinstein, D.A., R.M. Beloin and R.D. Yanai. 1991. Modeling
changes in red spruce carbon balance and allocation in response to
interacting ozone and nutrient stresses. Tree Physiol. 9:127--146.