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OCR for page 293
CARBON ALLOCATION PROCESSES AS INDICATORS OF
POLLUTANT IMPACTS ON FOREST TREES
McLaughlin, S. B.
Environmental Sciences Division
Oak Ridge National Laboratory
Oak Ridge, Tennessee 37831-603X.
ABSTRACT
The physiological processes linking carbon assimilation and net
primary production in forest trees offer a broad spectrum of
reference points for documenting, evaluating, and predicting the
effects of atmospheric pollutants on forests. Measurements of
photosynthesis, dark respiration, leaf maintenance costs, energy
storage reserves, secondary metabolites associated with plant
resistance to pathogens, dry matter partitioning, and patterns of
annual radial growth of forest trees represent useful indicators of
pollutant effects that encompass levels of detection ranging from
short term mechanistic processes to longer term responses that
integrate seasonal or multi-year effects. Productive utilization of
measurements of these processes requires that particular emphasis
be placed on (1) concurrent examination of multiple processes, (2)
integration of information on these processes into a whole tree
physiological context and (3) seasonal integration of temporal
variations in the magnitude of measured responses. Collectively
these processes can provide much-needed tools for evaluating
qualitative and quantitative changes in growth and physiological
resilience of forest trees in relationship to chronic air pollutant
exposure regimes.
The effects of atmospheric pollutants on forests have been documented at scales of
resolution ranging from biochemical and cytological alterations to changes in community
dynamics and structure (Mudd and Kozlowski, 1975~. Effects on carbon allocation are
particularly important in understanding the causes and consequences of these effects
because of the pivotal role that carbon plays not only in biomass accumulation, but also
in nutrient and water use capacity of forest trees (McLaughlin, 1 98Sa). The balance of
carbon assimilated from the atmosphere and distributed to the many sinks within forest
trees plays the pivotal role not only in the amount of growth, but also in the many
processes that determine the resistance and resilience of growth processes in the face of
environmental stress (McLaughlin and Shriner, 1980~.
.
The carbon allocation pathways and processes that link gross primary production
and net primary production offer many reference points for evaluating pollutant effects
at scales of resolution ranging from mechanistic to community level (Figure 1~. Included
among the effects of primary concern are reduced photosynthesis, increased respiration,
~ .
293
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PROCESSES
PROPERDES
294
NCR"SINGLY MECHANIC
INCREASINGLY INTEGRATIVE
A~IMllA~ON
.
.
~ ~ MAINTENANCE
~ ,
RATE
DURATION
SENSmVIrY
RESILIENCE
~~ ]~·~r MARC ]·lIlK~
~ _—~
_ _.
_
STOI AGE _ DEFENSE l
~ L~EL
RESPIRATION
TURNOVER
OQNL~WG 88M~1693
GROWTH
_:
_ e
. _
CHEMISTRY
DlSrRIBUTION
AMOUNT
DISTRIBUTION
TIMING
RESILIENCE
MPUCA DONS REDUCED ASSIMILATE INCREASED DECREASED PRODUCTION
SUPPLY SUSCEPTIBILITY ALTERED SUSCEPTIBIUIY
TO BIOTIC AND ALTERED COMMUNITY
ABIO~C CREPES DYNAMIC
Figure 1. Some components of carbon allocation pathways that provide useful
endpoints in evaluating mechanisms of action and implications for impacts of air
pollutants on growth potential of forest trees (after McLaughlin, 1988a).l,2
reduced translocation, and changes in patterns of storage, mobilization, and utilization of
energy storage reserves. These reference points collectively represent a powerful system
1 Research sponsored by the USDA, National Acid Deposition Assessment
Program under Interagency Agreement 40-1647-45 with the U.S. Department of
Energy under contract DE-AC05-840R21400 with Martin Marietta Energy Systems,
Inc.
2 Publication No. 312S, Environmental Sciences Division, ORNL.
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295
of indicators that can be used both analytically to determine whether forests have been
impaired physiologically and diagnostically to determine the principal points of impact and
likely causes of those impacts.
In examining the effects of pollutants or stress in general on tree growth and
physiology, it is important to view stress and response from a whole tree perspective
(McLaughlin, l98Sb). The concepts of whole plant allocation are particularly important to
understanding the effects of pollutants on tree physiology since both sources and sinks
for carbon may be influenced by pollutant deposition processes. This alteration may take
the form of either a decrease or an increase in the activity of sources or sinks within
the tree. Such changes may alter the patterns of tree growth as well as altering tree
responses to other environmental stresses.
In general we know considerably more about the assimilation of carbon and
associated energy and the net annual increment of biomass, which we measure as growth,
than about the many important processes that link the two. As an example, the obvious
pivitol role of photosynthesis as the source of carbon and energy for tree growth and
maintenance processes is reflected in the numerous studies of tree photosynthesis
(Shaedle, 1975~. However, relatively little emphasis has been directed toward
understanding subsequent allocation processes, which, in forest trees, may consume from
30 to approximately 80% of the energy captured in gross photosynthate (Kira, 1975~.
Thus, the processes of respiration, translocation, allocation, and biosynthesis may be
equally as important as photosynthetic capacity in determining levels of productivity
(Evans, 1975~. Where the vigor of forest trees is reduced by stress, relatively small
changes in efficiency of carbon allocation may have major consequences for the
physiological integrity of trees. In spite of the potential importance of these processes,
to date they have played a relatively minor role in efforts to quantify, characterize and
predict the effects of pollutants or other stresses on forest physiology and growth. This
paper briefly describes the basis of interest and information needs on four pivotal
processes in the carbon allocation pathways: carbon assimilation, dark respiration,
translocation and partitioning, and mobilization.
Carbon assimilation. The exchange of carbon, both photosynthetic uptake and
respiratory losses, by foliage of forest trees has been an obvious focal point in many
studies aimed at evaluating tree growth potential. With respect to air pollutant impacts,
changes in photosynthesis particularly have figured prominently in efforts to understand
the concentration threshold for physiological responses (Botkin et al., 1972), characterize
differences in sensitivity among genotypes of the same species (Boyer et al., 1986, Eckert
and Houston 1980) or evaluate comparative sensitivity across a variety of different
species (Oleksyn and Bialobok, 1986 and Reich and Amundson, 1985~.
There are many dimensions of net photosynthesis (Pn) that can provide important
insights into the impacts of pollutants on photosynthate production. These include both
maximum capacity under saturating radiation levels, the light response curves (including
the compensation point), kinetics of response to both pollutants and changes in radiation
and the patterns of change in response over diurnal and seasonal cycles, and the
distribution of Pn capacity within tree crowns both as a function of foliage age and
position within the crown (McLaughlin, 1 98Sc). In addition to measures of Pn capacity,
Pn response surfaces to light ~ Hanson et al., 1987) and to C02 (Farquhar and Sharkey,
1982) offer possibilities for evaluating the efficiency of leaf photosynthetic processes.
Measurements of Pn at any point in time, while they may provide important
information on the integration of exposure effects to that time, may not adequately
describe the past or future kinetics of the photosynthetic system. Boyer et al. ( 1986)
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296
indicate that Pn of white pine recovered following exposure to ozone at 0.05 ppm (6 in/d)
but decreased more rapidly on each successive day of exposure, thus suggesting
progressive impairment of the photosynthetic system. The manner in which response and
recovery systems operate over time to determine seasonal influences on carbon
assimilation capacity is an important issue. As an indicator of pollutant stress Pn has two
dimensions: ( 1 ) the initial basal rate may be directly related to sensitivity to uptake of
gaseous pollutants and hence the potential for Pn reduction. and (2) as an indicator of
longer term capacity for the integration of pollutant and other stresses over the life of
the foliage, decreases in Pn reflect sensitivity to deterioration of the integrity of
photosynthetic or systems or (less likely) reductions in demand for assimilates.
It should be noted that compensatory factors may partially offset the effects of
stress on photosynthetic systems. The capacity of foliage of some plants to respond to a
decrease in source-to-sink ratio by increasing Pn efficiency may be an important
characteristic determining tree resilience to foliar damage (McLaughlin and Shriner, 1980~.
Replacement of damaged foliage is, of course, another possibility for indeterminate
species (Coleman, 1986~. Because of such compensatory factors, reductions in growth can
not be predicted! on a 1:1 basis from reductions in Pn. Reich and Amundson (1985), for
example, found that while reductions in growth were linearly related to reductions in
photosynthesis, compensatory processes resulted in final growth reductions of plants
exposed under laboratory conditions that ranged from 20 % for tree seedlings to about 60
% for crops.
In contrast to results from studies with OF (Reich, 1987), there is little indication
to date that acid precipitation at ambient levels adversely affects carbon assimilation
(Reich et al., 1986 and Hanson and McLaughlin, 1987~. By contrast, Taylor et al. (1987)
found that acid mist at pH 3.0 stimulated overall Pn capacity of red spruce seedlings due
to increased foliar area produced at higher acidity and associated nitrogen levels.
Much additional work is needed to understand the likely effects of acid deposition
on carbon assimilation processes. This task is made particularly complex and interesting
by the likely influences on leaf physiology of nitrogen and other nutrients present in
acid rain. The potential stimulation of foliage growth by deposition of nitrogen may
increase plant sensitivity to moisture stress as observed with greenhouse grown red
spruce seedlings by Norby et al. (1986~. Results such as these emphasize the advantages
of examining process responses to pollutants such as acid deposition from a whole plant
perspective.
Dark respiration. To date relatively little emphasis has been placed on
pollutant-induced effects on dark respiration (Rs). However, stimulation of dark
respiration is an expected consequence of plant repair mechanisms (McLaughlin and
Shriner, 1980) and may deplete as much or more carbon from available energy pools as
reduced photosynthesis. Increased dark respiration may be particularly significant when
coupled with reduced rates of Pn, and in fact, reduced Pn may be a consequence of
increases in light respiration, a component of the assimilation process that has received
little emphasis with respect to pollutant effects.
Barnes (1972) detected a reduction of photosynthesis (-10 % average) and stimulation
of dark respiration (+33% average) in seedlings of three species of southern pines exposed
to O.l5ppm O3 under laboratory conditions. McLaughlin et al.(l982) found that Rs was
stimulated approximately 15% while photosynthesis was reduced only 6% in mature field
grown white pine trees, thus showing high apparent sensitivity to ambient levels of ozone
in east Tennessee.
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297
Changes in the Pn:Rs over a range of temperature and light conditions could
provide a more complete picture of alterations in assimilate supply. Obviously, increased
emphasis on dark respiration is warranted in research aimed at accurately quantifying
pollutant impacts on total assimilate available for export from foliage.
Translocation. The transport of assimilates away from production centers to points
of utilization within the tree may be examined either at the leaf level or at the whole
plant level. At the whole plant level there is good evidence that air pollutants may exert
significant effects on plant productivity by altering partitioning of dry matter between
plant parts (Manning, 197S, Oshima et al., 1979, Tingey, 197S, and Tingey et al., 1976~.
At the leaf level, shifts in translocation may occur either as a consequence of
interference of pollutants with the loading of the phloem with assimilates or as a
consequence of increased assimilate demand by foliage. Internal demand in turn may be
enhanced by either altered foliar nutrition (nitrogen assimilation directly by foliage from
the atmosphere) or as a damage response requiring increased internal maintenance and
repair. A review of studies with several plant species indicates that internal costs of
maintaining leaf functions are high (McLaughlin and Shriner, 1980). These maintenance
costs would be expected to be enhanced by exposure to pollutants at levels high enough
to cause metabolic or cytologic injury. Several studies under both laboratory (Jones and
Mansfield, 1982, Noyes, 1980, Teh and Swanson, 1982, and Tingey, 1978) and field
conditions (McLaughlin et al., 1982) have indicated that carbohydrate translocation may
be both sensitive to exposure to air pollutants and useful as a general indicator of
pollution related stress.
At present the level of understanding of the aboveground system is far beyond
that for the belowground system and the reasons for this are obvious. Yet belowground
processes including both maintenance and turnover of fine roots may play a major role in
whole tree energy budgets (Harris et al., 1974 and Persson, 1980) and are likely to be
particularly sensitive to pollutant impacts (McLaughlin, 1 98Sb). Measures of pollutant-
induced impacts on transport of assimilates to support the belowground system are sorely
needed as they relate directly to the functional integrity and to uptake of both water
and nutrients by the root/rhizosphere system.
Storage and Mobilization. With respect to evaluating impacts of air pollutants on
tree production potential, the storage reserves provide a potentially useful and temporally
integrative indicator of the carbohydrate economy of the tree and its capacity both to
meet the energy demands of annual growth cycles and to resist insects and disease.
Resistance to disease may be a particularly important characteristic because allocation of
resources to formation of protective chemicals appears to be of relatively low priority
when energy reserves are in low supply (Mooney and Chu, 1974~. Allocation of energy
reserves to the production or maintenance of new foliage or roots represents a high
priority that supersedes the demands for defensive strategies when trees are under
stressed conditions (Waring and Pittman, 1985~.
Plants have a wide variety of strategies for defense against diseases (Horsfall and
Cowling, 1980), and many of those defenses could be weakened by the chronic exposure
to atmospheric pollutants (Hain, 1987), particularly when alterations in carbon allocation
occur. Phenolic compounds, tannins, and proteins are examples of metabolites that are
considered important in host defenses against microbial attack (Schloesser 1980~. Perhaps
the best example of the importance of secondary metabolites to disease resistance of
forest trees under pollutant stress has come from research in the San Bernardino Forest
where increased susceptibility of oxidant-stressed ponderosa pine to attack from bark
beetles was noted (Stark et al., 1968~. Increased susceptibility to beetle attack was
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298
associated with both qualitative and quantitative changes in the oleoresin production of
affected trees (Miller et al., 1968 and Cobb et al., 1968~. Additional potentially useful
situations in which the energy reserve status of forest trees may be playing an important
role in host-pathogen relations include the southern pine bark beetle and balsam
fir/wooly aphid associations in the southeastern U.S. Both insect outbreaks have
occurred in areas in which air pollutants are under investigation as contributing factors
to forest growth decline.
Since trees store energy in many different biochemical forms, the question of which
constituent to examine as an overall indicator of tree energy reserves is of obvious
relevance. Kramer and Kozlowski (1960, 1979) have grouped forest tree species into
those that store food reserves primarily as fats (principally diffuse-porous species),
starch (primarily ring-porous species), and a third group that utilizes both forms.
Regardless of the primary storage form, starch appears to be a significant constituent of
energy storage in roots of most tree species (Ziegler, 1964~. As an indicator of storage
reserves, root starch offers apparent advantages over starch in foliage, which is more
readily influenced by short-term climatic fluctuations (Adams et al., 1986~. Studies with
defoliating insects (Gregory and Wargo, 1986 and Wargo, 1981 ) indicate that starch
content of xylem and roots provides a useful index of whether stress has occurred and of
the vulnerability of trees to additional stress effects from either insects or other natural
factors that induce mortality.
While starch may be a useful indicator of the vigor of root systems of pollution-
stressed trees, it should be noted that interpretation of root starch data must be made
within the context of the physiological status of the whole tree (Ericsson, 1980~. Starch
depletion may reflect either stimulated utilization of storage reserves during rapid growth
or diminished capacity of the tree to assimilate carbohydrates rapidly enough to replace
those utilized in normal growth and maintenance demands. Similarly short-term increases
in starch accumulation may occur when utilization of assimilates is slowed by growth
inhibition at the site of utilization.
The preceding discussion has focused on process level measurements as indicators of
pollutant induced alteration of carbon allocation patterns. It should be noted in closing
that useful evidence of altered carbon allocation patterns can also be derived from the
observed patterns of growth itself (see Fig. 1~. The timing, duration, response and
recovery cycles following natural or anthropogenic stresses, and density and quality of
wood formed all provide potentially useful indicators of the nature and causes of
impaired tree vigor (McLaughlin, l98Sb). Dendrochronology is an emerging discipline
which has tremendous potential for examining the patterns and potential causes of annual
growth patterns at annual and longer time scales (Cook, 1986~. Observed response
patterns at the stem level can provide testable hypotheses about basic physiological
processes strongly influencing growth of a species as well as likely causal factors
leading to disruption of the growth process (McLaughlin et al., 1987~.
Several summary points can be made regarding the use of carbon allocation
pathways to identify and diagnose responses of trees to air pollutants: (1) There are
many reference points within plant carbon allocation pathways that respond to air
pollutants and offer potentially useful diagnostic criteria for detecting pollution-induced
damage. These occur at many levels of organization within the tree; (2) It is essential
to recognize that allocation processes are tied to both the supply and demand of carbon,
water, and nutrient recourses and hence will be influenced by a wide variety of natural
stresses. These stresses and the responses they induce must be considered concurrently
with pollutant stresss. They may either be minimized by experimental design or used as
modifiers to test the nature or consequences of pollutant-induced stresses; (3) The
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299
separation of natural phonological and diurnal patterns of response from those that may
be induced by air pollutants requires that one consider these inherent response-recovery
cycles in evaluating shifts in carbon allocation pathways; (4) Approaching the problems of
detection and diagnosis of changes of carbon allocation processes can most effectively be
accomplished from a whole-tree physiological perspective that recognizes and tests
physiological interrelationships among both processes and plant parts.
Within this context an analytical framework can be suggested that first documents
the magnitude anti patterns of change in a biological indicator or indicator system and
then tests both the physiological basis of the measured response as well as its
consequences at successively higher levels of whole plant integration. The physiological
basis must be understood to address adequately the causal relationships and the range of
possible consequences, while the more integrative measures help document the range and
probabilities of actual responses observed under field conditions. Consideration of both
growth and process level responses within the carbon allocation system provides
inferential cross references that can substantially improve our ability to address the
inherent complexity and many uncertainties of forest decline issues.
ACKNOWLEDGMENTS
The author wishes to thank Drs. George Taylor, Chris Anderson, and Tim
Tschaplinski of Oak Ridge National Laboratory for their review of this manuscript.
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Representative terms from entire chapter:
forest trees
