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OCR for page 303
PHOTOSYNTHESIS AND TRANSPIRATION MEASUREMENTS
AS BIOMARKERS OF AIR POLLUTION EFFECTS ON FORESTS
Dr. William E. Winner
Department of General Science
Weniger Hall 355
Oregon State University
Corvallis, OR 97331
ABSTRACT
Gaseous air pollutants such as SO2 and Of are known to alter
rates of CO2 fixation and water loss by leaves. In addition, acid
deposition may increase the availability of nitrogen and other
potential nutrients, thereby altering foliar nutrient content and
metabolic capacity. Thus, many forms of air pollutants have the
potential to affect photosynthesis, transpiration, and other
important, derived features of leaves, such as stomata!
conductance, CO2 internal, and water use efficiency Using these
direct effects of air pollutants on leaf physiology as biomarkers of
tree responses to air pollutants will be discussed. These
physiological parameters may be useful as biomarkers because they
change dynamically as pollutant exposures change, they are easy
to measure with portable field equipment, they are related to
long-term growth processes, and when taken together, they can
provide an overview of how the leaf is linked to its environment.
The fact that photosynthesis and transpiration change with
season, leaf age, time of day, and with non-pollution
environmental factors poses problems for using these parameters
as biomarkers of air pollution. Also, the capacity for plants to
compensate for stresses by reallocating resources between organs
makes it difficult to extrapolate from leaf level measurements to
an assessment of whole tree and canopy processes. Any attempt
for such an application would require carefully established
sampling protocols to define background rates of photosynthesis
and transpiration, a method for defining control measurements, and
an approach for putting single leaf measurements in perspective
with the whole tree. Measurements of photosynthesis and
transpiration may be most useful when included in a suite of
parameters used in biomarker assessments.
INTRODUCTION
The idea of using physiological features of trees as markers of air pollution stress
is attractive for a number of reasons. Most importantly, physiological features of trees
are likely to respond in a dynamic way to air pollutants and, in so doing, indicate that
air pollutants are causing important changes in the biological processes necessary for the
tree to sustain itself. In addition, these physiological changes should be detectable
before more overt symptoms of damage, such as foliar injury, are apparent. Another
feature of physiological markers of air pollution response is that these markers can be
303
OCR for page 304
304
viewed in the context of whole plant growth and survival, i.e., air pollution-caused
changes in the physiological processes of plants can be linked to their productivity,
longevity, and reproduction.
Many physiological parameters could be used as markers of tree responses to air
pollutants. A few of these parameters, such as foliar gas emission, foliar enzyme activity
levels, and cuticular integrity, are discussed in other chapters. Successful application of
these leaf characteristics to monitor air pollution impact requires a detailed
understanding of the way by which the leaf feature relates to environment (Fig. 1~. For
example, under optimal conditions, the status of a leaf parameter can be assessed.
However, plants are almost always growing in the presence of naturally occurring
environmental stresses, such as drought, inadequate water and nutrients, and low light.
These natural stresses cause a deflection in the rate of the leaf process of interest and
this deflection should be viewed as natural, normal, and with adaptive value over the
longterm. Air pollutants typically cause a further deflection in the process of interest
and represents the response which must be identified as the biomarker. Our capacity to
see the marker depends upon our understanding of the process of interest, and the
knowledge necessary to predict how the process will be influenced by naturally occurring
stresses and by air pollutants.
RELATIVE REDUCTION IN METABOLISM
Optimal Natural Natural Stresses Plus
Conditions Stresses Air Pollution
1 00%.
._
o
-
0
._
-
a)
-
CL
o% -
Figure 1. The variable effects of natural stresses (a) combined with air pollutants (b) on
depression of plant metabolism.
The purpose of this chapter is to highlight the use of photosynthesis, transpiration,
and stomata! conductance measurements as indicators of air pollution stress. There are
several reasons why assessments of photosynthesis and stomata! status should be
important candidates in the attempt to identify markers of air pollution stress. For
example,
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305
1. The relationship between photosynthesis and conductance is under biological
control and is related to productivity;
2. Photosynthesis and conductance are known to change quickly with the onset of
air pollution exposures,
3. Stomatal conductance values can be used to calculate air pollution absorption
by plants;
4. Photosynthesis and conductance can be easily measured with non-destructive
techniques as well as by analysis of collected tissue.
Thus, one goal of this paper will be to expand on each of these points to clarify the
unique advantages associated with the use of photosynthesis and conductance as markers
of tree response to air pollutants.
There are a number of reasons why photosynthesis and conductance measurements
are not currently used as biomarkers. Most importantly, it is difficult to associate
changes in these leaf-level processes to specific exposures to air pollutants. In addition,
calibrating photosynthetic and stomata! responses to air pollutants will prove to be
difficult. Thus another goal of this paper will be to identify the barriers to the use of
these measurements of leaf physiology as air pollution markers.
LINKS BETWEEN PHOTOSYNTHESIS, STOMATAL CONDUCTANCE, AND GROWTH
Stomata are small pores on leaf surfaces which can open and close. The importance
of these pores is that they represent the main route of gas exchange between the leaf
and air. The degree of stomata! opening is under biological control (Fig. 2) and
represents one of the ways by which plants relate to environmental change (Jones 1983~.
The paradox for plants is that conductance should be as high as possible in order to
maximize rates of carbon gain via photosynthesis, while at the same time, conductance
should be such that transpiration rates are not so high that plants desiccate (Farquhar et
al. 1980~. Plants are thought to maximize carbon gain while minimizing water loss by
continually sensing the environment and adjusting- stomata to the appropriate pore size.
For example, many plants close their stomata at night. This is adaptive because plants
conserve water during dark periods when the light reactions of photosynthesis cannot
occur. Thus, stomata respond to a CO2 sensor. Stomata also respond to a sensor linked
to plant water relations. If transpiration rates are high due to low relative humidity or
limited soil water availability, many plants will close stomata. During these periods, CO2
cannot diffuse from the air into the leaf, and plants sacrifice photosynthesis to conserve
water. Although there are exceptions to the general rules above, stomata play a central
role in regulating rates of carbon gain and water loss.
The rate of photosynthesis is intimately linked to growth. More than 90% of the
dry weight of a plant is in the form of carbohydrate which originates from
photosynthesis. Thus, the source of plant carbohydrate is known. However, the links
between rates of CO2 fixation and rates of growth are complex (Mooney, 1972~. For
example, one useful measure of photosynthesis is "photosynthetic capacity," a measure
made on a leaf-area basis when environmental conditions are near optimal for metabolism.
Plants which have high photosynthetic capacity can be small. In fact, desert annuals
have among- the highest photosynthetic rates but are typically small (Mooney et al.,
1976~. Crop cultivars which have the highest photosynthesis rates may not have the
highest yield. Finally, the largest trees are often among the plants with the lowest
photosynthetic capacities.
OCR for page 306
Direct
piglet effect
(feedforward)
306
_ _
, Environment I__
,- .. ,
/ ~ ~
\ CO2 H2O
Guard cell
~ . ~ ~
4K't ~
` Direct
humidity effect
(fee(3forwar(i)
~—~
_
-
CO2 feedback /~71 Me~abo~ic l+~\ Flydroactive ~
'_~~ // \\feedbaci``,
. . ~
Tissue ~ _ ~
I ~
'-tCO2 sensor |
I. .. .
tlydro passive
feed back
Figure 2. Active and passive feedback control systems for regulation stomata! conductance involving
CO2 and water. Source: Reprinted with permission of Cambridge University Press from Plants and
Microclimate 1983. Copyright 1983 by Cambridge University Press.
Photosynthesis is linked to growth via leaf longevity (Mooney 1972~. Thus, leaves
with low photosynthesis can contribute a great deal of carbohydrate to growth by
remaining active for long periods. Conversely, leaves which are short-lived will not
produce much carbohydrate regardless of their photosynthetic capacity.
Photosynthesis is also linked to growth via the process of carbon allocation (Monsi
1968; Mooney 1972) (Fig. 3~. The product of leaf biomass and photosynthetic rate gives
the carbon supply rate for the entire canopy. Some of this carbon is allocated to roots
and some is allocated to shoots. The carbon allocated to shoots can be used to acquire
more carbon for the plant whereas carbon allocated to roots, although essential for plant
survival, does not acquire more carbon. Thus, plants with equal photosynthetic
capacities, but different carbon allocation schemes will have different growth rates.
Interestingly, many species differ in their patterns of carbon allocation between roots
and shoots. In addition, environmental factors also cause changes in carbon allocation
patterns. Atmospheric stresses which limit carbon gain shift allocation to favor the
shoots whereas stresses which reduce uptake of nitrogen and water by roots shift
allocation to roots. The potential for air pollutants to alter photosynthesis and growth
of both roots and shoots increases the value of this physiological parameter as a
biomarker of tree response to air pollution.
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307
Initial
al location
sta te
Environmental
stress
New
allocation
state
Leaf X Photosynthetic `t Roof X Nutrients
biomass rate =K Kbiomass uptake J
\\ Carbon //
Reduce carbon supply
Low light
SO2 / O3 /
Leaf ~ Roof
biomass biomass
Harbor
/ \ Reduce nitrogen/water supply
/ \ Drought
\ Low soil fertility
Leaf ~ Roof
biomass biomass
carbon
Figure 3. Effects of environmental stresses on carbon allocation patterns of plants
(Winner and Atkinson, 1986~.
EFFECTS OF AIR POLLUTANTS ON PHOTOSYNTHESIS AND STOMATAL FUNCTION
Leaf-level Responses. Most forms of air pollutants have the potential to alter leaf
metabolism. The effects of gaseous pollutants on CO2 and water vapor exchange rates
has been studied most thoroughly in experiments with SO2 and O3 (see reviews in Winner
et al. 1985a, Guderian 1985~. However, any gaseous pollutant known to alter plant
growth will also alter both photosynthesis and conductance. The potential also exists for
oxides of sulfur and nitrogen to affect leaves. More specifically, foliar nitrogen content
should increase with deposition of nitrate from the atmosphere. Since photosynthetic
capacity and conductance increase with foliar nitrogen content (Field and Mooney 1986),
increased nutrient availability due to wet and dry deposition processes should be
reflected in increased rates of leaf metabolism.
Studies with SO: and O3 have shown that there are several mechanisms of stomata!
response to gaseous pollutants (Fig. 4~. These mechanisms may operate both at the leaf
level and at the whole plant level. Leaf level responses to SO2 and O3 gas exchange
studies have clearly shown that mechanisms of leaf level responses can be fast and
extreme. For example, a radish leaf exposed to 0.4 ppm SO2 decreased its
photosynthetic rate by 75% within 10 minutes (Winner et al. 1988) (Fig. 5~. In addition,
stomata also responded to this treatment within 30 minutes.
OCR for page 308
308
MECHANISMS OF STOMATAL RESPONSES TO
GASEOUS POLLUTANTS
* Leaf level
Direct effects on guard cells / epidermal cells
Indirect effects on photosynthesis
* Canopy / whole plant level
Premature leaf loss
Indirect effects on foliar N
Figure 4. Some mechanisms of stomata! responses to gaseous air pollutants.
This simple experiment (Fig. 5) is important because it shows that a gaseous
pollutant can cause stomata! closure. Many other studies have also shown that SO2
(Winner and Mooney l980a,b; Kimmerer and Kozlowski, 1981; Olszyk and Tingey, 1986)
and ON (Reich and Lassoie, 1984; Olszyk and Tingey, 1986; Temple 1986,) can cause
stomata! closure. Thus, the idea that severe and untimely stomata! closure might be a
marker of tree response to air pollution stress seems attractive. However, other studies
have shown that SO2 (Mansfield and Majernik, 1970; Black and Unsworth, 1980) and Of
(Evans and Ting, 1974) can also cause stomata! opening. Variation in stomata! response
to SO2 and Of has been recently reviewed (Winner et al. 1988~. Thus, any attempts to
use stomata! conductance as a marker of leaf level responses to gaseous pollutants must
be framed within an understanding of factors which lead to either stomata! opening or
closing. The radish fumigation experiment described above (Fig. 5) is also important
because it provides a clue about why stomata can either open or close in response to air
pollution exposure. SO2 and O3 have the potential of affecting stomata by acting
directly on guard cells. In addition, it is possible for these pollutants to act first on
photosynthesis which then activates the previously described CO: sensor (Fig. 2) and
results in subsequent changes in conductance. The time sequence analysis of the radish
experiment shows that SO: causer! changes in photosynthesis before changes in
conductance suggesting, that in this experiment, stomata may be responding to air
pollutants via changes in carbon metabolism.
OCR for page 309
309
and
en
— 20
o
in 18
-
In
o
I_
o
AL
~ `~`
i'
—_ _
10 20 30
TIME (minutes)
-
`_ _
- _ _
400
40 50
cat
500 ~
-
-
450 '5
3
I:
C'
Figure 5. Time course for changes in photosynthesis (is- ~ ) and conductance (------)
following the additon of SO2 and 0.4 ppm at time 0. Ambient CO2 concentration was 350
ppm (Winner et al., 1988~.
A number of other studies have shown that SO2 can cause changes in
photosynthesis prior to changes in conductance (see summary in Winner et al., 1988~.
Data from many of these studies were not collected by investigators for the purpose of
time series analysis, but the trends of response sequence can nonetheless be determined.
Interestingly, reports indicating that stomata! responses to SO2 precede photosynthetic
responses were not found. In addition, there are no experiments with Of that allow such
time course analyses.
If SO2-caused decreases in photosynthesis can lead to stomata! closure, then SO2-
caused increases in photosynthesis may lead to stomata! opening. The CO2 sensor
operates by causing stomata! closure when CO2 concentrations in the mesophyll increase.
Such shifts in CO2 would occur if SO2 damaged the photosynthetic apparatus.
Conversely, SO2 may enhance electron transport processes associated with photosynthesis
leading to increased photosynthesis and decreased CO2 concentrations in leaves. Such a
shift in CO2 concentrations would result in stomata! opening.
Plant-level Responses. Air pollutants can also alter conductance of the entire
canopy of trees by altering stomata! pore size. For example, O3 is known to cause
premature senescence and abscission of foliage (Guderian et al., 1985~. One consequence
of this leaf loss is a reduction in leaf surface area capable of exchanging gases between
the canopy and air. Just as air pollution-caused stomata! closure is adaptive in that air
pollution absorption rates are decreased, so too is the response of leaf loss a potentially
adaptive response.
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310
-O. ~
I, Time
o3
s
3
o
o
CHANG ES IN G ROWTH o
AND FOLIAR NITROGEN ~
Figure 6. Hypothetical time course of root and shoot growth responses to O3 episodes.
Another mechanism by which gaseous pollutants can potentially alter whole plant
canopy conductance involves the relative synchrony of suppression of shoot and root
growth. Gaseous pollutants are known to shift root/shoot ratios (Winner and Atkinson,
1986) and many studies show that root growth is more sensitive to exposures than is
shoot growth (Tingey and Reinert, 1971~. These conclusions are typically based on
studies in which plants are fumigated for periods ranging from 30 to 90 days and then
harvested for whole-plant growth analysis. A strong possibility exists that shoot growth
suppression and root growth suppression are not synchronous (Fig. 6~. Similarly,
recovery of shoot growth and recovery of root growth when air pollution exposures
terminate are apt to be out of phase. The importance of root and shoot growth rates
from the perspective of conductance is manifest through foliar nitrogen content. As
discussed earlier, stomata! conductance and photosynthetic capacity increase with foliar
nitrogen content (Field and Mooney, 1986~. If shoot growth recovery precedes root
growth recovery, then foliar nitrogen content may be reduced by dilution and
photosynthetic capacity and conductance will also be lowered. However, if an air
pollution episode results in a great deal of leaf loss, the recovery process might result in
a large root system supplying nitrogen to relatively few leaves. In this case, the leaves
may increase in N content resulting in higher levels of leaf metabolism. These patterns
of whole-plant resource allocation might help explain why, in some studies, O3 or SO2
can bring apparent increases in leaf-level processes (Libera et al., 1973~.
OCR for page 311
311
CALCULATIONS OF AIR POLLUTION ABSORPTION
Stomatal conductance to water vapor not only is important as it relates to fluxes of
CO: and H:O between the leaf and air but also as it relates to air pollution absorption
(Winner and Mooney 1980 a,b; Winner and Atkinson, 1986~. Calculating air pollution flux
rates through stomata requires knowing leaf conductance values for H2O, ambient
concentrations of any gaseous pollutants, and the diffusion coefficient of that pollutant
in air. Flux rates of pollutants can then be integrated over time to determine total
quantity of pollutant absorbed during exposure. The strength of this approach is that
physiological and growth responses of plants to air pollutants can be expressed on the
basis of a quality of air pollution absorbed rather than on the basis of atmospheric
concentrations.
Calculating flux rates of air pollutants into foliage on the basis of stomata!
conductance assumes that intracellular concentrations of the pollutant are zero and that
stomata! conductance is lower than all other components of leaf level conductance
(Winner et al., 1 985b). The extent to which these assumptions are untrue represents
error in the method. Indications are that error from these assumptions are hard to
measure but nonetheless small (Winner et al., 1 985b). The error for estimating air
pollution uptake by foliage by chemical analysis of foliar samples before and after
exposure is known to be large, is not dynamic, requires destructive sampling, and is not
useful for pollutants such as Of because oxygen is present in foliage in high
concentrations. Thus, estimation of gaseous air pollution absorption by foliage is best
done by calculating flux rates of pollutants through stomata.
MEASUREMENTS OF PHOTOSYNTHESIS AND CONDUCTANCE
Non-destructive Techniques. A number of scientfic equipment manufacturing firms
produce portable gas exchange systems useful for screening leaf populations for
photosynthsis and conductance. For example, systems manufactured by LiCor, Inc.
(Lincoln, NE) and by Analytical Design Corporation, Ltd. (Hodgested, England) are
commonly available and are favorably compared (Parkinson et al., 1988~. Also, Data
Design Group, Inc. (La Jolla, LA) makes a comparable system. These systems are
typically battery powered and easily carried into the field. Another important feature of
these systems is their capacity to acquire and store data. The systems can be operated
to survey numbers of leaves quickly with each measurement taking about 1 minute, and
can be used to measure photosynthesis and conductance for many (20-200) leaves, that
remain attached to trees, within a single day. This capacity to measure gas exchange
rates of numerous leaves in a short time is essential if photosynthesis and conductance
measurements are to play a useful role as air pollution markers.
Sample Collections. Leaves can also be collected from tree tops or other
inaccessible places and then used in gas exchange measurements. This technique has
been applied in a number of remote field sites (Lange et al., 1986~. Use of this method
requires measuring gas exchange rates of leaves attached to a tree, followed by
remeasurement at intervals after the leaf is detached. This protocol is followed to
characterize the effects of leaf removal, handling, and storage on gas exchange
parameters. Handling techniques that minimize artifacts include storing the leaf in cool
places, retrimming the collected branch or petiole under water, and leaving the cut
surface in water, and keeping the time period between leaf collection and gas exchange
measurements as short as possible.
OCR for page 312
312
The radio isotope 14C has been used to generate 14CO2 ~ which is then used to
assess the effects of air pollutants on photosynthesis (e.g., McLaughlin et al., 1982~. In
these studies, leaves are enclosed in a chamber and exposed to 14CO2 for specific periods
of time. The 14CO2 provides a tag which can be used to document photosynthesis rate
and the metabolic fate of photosynthate. Air pollution effects are determined by
comparing the 14CO2 fixation rates and fates for air pollution treated plants and
controls.
Photosynthesis and conductance can also be indirectly assessed by collecting leaf
samples for a-nalysis of stable carbonisotope ratios, or more specifically, their 1 C/ 1 3C
ratios. The o l 3c values of C3 plants, typically ranges from -26°/oo to 32°/oo (Fig. 7)
(Troughton, 1979~. This is because the CO2 fixing enzyme of C3 plants (RUBISCO)
preferentially fixes the 1 2C-containing CO2 over the heavier form. Thus, carbohydrate
of C3 plants is depleted in 13C relative to the atmosphere.
o: 1 3C VALUES FOR COT C3 PLANTS, AND C4 PLANTS
C 3 PLANTS
51 3C = -32 5 %o 81 3 C = -26.3%o
~,
1 ppm 't_
~_ ~
~-
ppm ?—
CO2 = 350 ppm
o$1 3C = -7%O
C4 PLANTS
~ 1 3C = -9%O
=120/
,_ J ppm
-`'_
_ . ~
Figure 7. °13C values for C in atmospheric CO2 and in foliage.
The range of ol3c values for C3 plants is in large part dependent upon the CO2
concentrations in the leaf mesophyll (Farquhar et al., 1982) (Fig. 7). These CO2
concentrations reflect both the rate of photosynthesis and the degree of stomata!
opening. Under some conditions, CO2 internal concentrations for C3 plants can be as
low as 220 ppm. This would be under high light with closed stomata. Under these
circumstances, RUBISCO is less descriminating and less fractionation of the two stable C
isotopes occurs. C stable isotope fractionation is highest when CO2 internal
concentrations are high which occurs when stomata are open.
OCR for page 313
313
The idea that any environmental factor which changes CO2 internally also changes
the 513C ratio has been shown for drought and other stresses (Guy et al. 1980; Winter et
al., 1982). Recent studies show that ambient O3 levels can also alter o l 3C values for
leaves, stems and roots (Greitner and Winner, 1988) (Fig. S). This is not surprising since
this O3 treatment was al-so found to deplete CO2 internal concentrations. This study
raises the possibility that o l 3c values of plants in the field may be useful in identifying
plants growing with air pollution stress. However, this will require developing the
capacity for partitioning °13C shifts due to air pollutants from shifts due to other
environmental stresses.
'~ — _ A , , , ~ ~ . ~ _ _
~1
~0 - _
_ _
^29
lo;
%_
=1
O
Cat) 20
·_
Cal
C 27
Zen
1 _
_ ~
~-
~ 1
control
treatment
ozone,
LEGEN D
radish leaven
radish hypocotyl~
~3
soybean leaven
=~ soybean root"
radish roots
Figure 8. O3-caused shifts in ol3c values of leaves, stems, and roots (Greitner and
Winner, 1988~.
PROBLEMS USING PHOTOSYNTHESIS AND CONDUCTANCE AS AIR POLLUTION
MARKERS
Pollutant Specificity. One difficulty with using physiological properties of leaves as
markers of air pollution is that responses may not be specific to pollution. As mentioned
above, most physiological processes of leaves, including photosynthesis and conductance,
OCR for page 314
314
change with many environmental parameters.
air pollutants will be a difficult task.
Identifying changes in metabolism due to
Another problem is that physiological responses may not be specific for specific
pollutants. For example, O3 and SO2 may both cause stomata! closure and decreases in
photosynthesis. If an air pollution-caused decrease in leaf metabolism were identified,
how would the causal agent be identified? Thus, the marker would reveal the presence
of an air pollutant but the air pollutant which caused the effect would remain unknown.
Photosynthesis and conductance changes in response to air pollutants will be
difficult to use as air pollution markers because even once the pollution response is
known, it will not be quantified. The degree of stomata! response to SO2 or O3 is apt
to change with temperature, humidity, age, season, and the presence of other air
pollutants. Current understanding is not sufficient to predict the degree of physiological
responses to well defined air pollution exposures in controlled environments. Therefore,
it will be some time before that capacity is sufficiently developed for application to field
sites.
One of the challenges to those intent on using photosynthesis and conductance
measurements as air pollution markers for trees will be to use these data with other
carefully selected data. Using only gas exchange measurements will be insufficient for
assessing trees in controlled- studies or in uncontrolled field surveys. Gas exchange
measurements in both mechanistic experiments and surveys are most useful when
combined with other data, including biochemical analysis, growth analysis, and community
analysis, and thereby put into a broad biological perspective.
SUMMARY
Photosynthesis, transpiration, and conductance have potential air pollution
biomarker applications.
Leaf-level metabolism, alone, is insufficient as an air pollution biomarker.
Leaf-level metabolism, used with other measurements, might be used to develop
an air pollution biomarker index.
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Evans, L.S., and I.P. Ting. 1974. Ozone sensitivity of leaves: relationship to leaf water
potential, gas transfer resistance, and anatomical characteristics. Am. I. Bot.,
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Farquhar, G., E.-D. Schulze, and M. Kuppers. 1980. Responses to humidity by stomata of
Nicotiana Glauca L. and Corylus avellana L. are consistent with the optimization of
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Farquhar, G.D., M.H. O'Leary, and J.A. Berry. 1982. On the relationship between carbon
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315
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^1 1_
Guderian, R. (ed.~. 1985. Air Pollution by Photochemical Oxidents: Formation, Transport,
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Monsi, M. 1968. Mathematical models of plant communities. Pp. 131 - 150 in Functioning
of Terrestrial Ecosystems at the Primary Production Level, Eckarcit, F. (ed.~.
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Mooney, H.A., Ehleringer, J., and J. A. Berry. 1976. High photosynthetic capacity of a
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Olszyk, D.M., and D.T. Tingey. 1986. Joint action of O3 and SO2 in modifying plant gas
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Parkinson, K.J., D. McDermitt, S.C., Roemer, S.P. Cline, and W.E. Winner. 1988.
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Representative terms from entire chapter:
gas exchange
