SEPA
United States
Environmental Protection
Agency
Office of Air and Radiation
Washington D.C. 20460
Assessing the Risks of
Trace Gases That Can
Modify the Stratosphere
EPA 400/1-87/001H
December 1987
Volume VIII:
Technical Support Documentation
Ozone Depletion And Plants
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Current Risks and Uncertainties of
Stratospheric Ozone Depletion Upon
Plants
Volume VIII
Technical Support Documentation for Assessing
the Risks of Trace Gases That Can Modify the
Stratosphere
December 1987
U.S. Environmental Protection Agency
Region 5, Library (5PL-16)
250 S, Dearborn Street, Room 1670
Chicago, *1L 60604
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ACKNOWLEDGEMENTS
This paper was written by Alan H. Teramura, Department of Botany,
University of Maryland, College Park, Maryland 20737.
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Ill
TABLE OF CONTENTS
Page
PREFACE iv
1. INTRODUCTION 1
2. ISSUES AND UNCERTAINTIES IN ASSESSING THE EFFECTS OF UV-B
RADIATION ON PLANTS 2
2.A. Issues concerning UV dose and current action spectra for
UV-B impact assessment 2
2.B. Issues concerning natural plant adaptations to UV radiation.. 9
2.C. Issues associated with the extrapolation of data from
controlled environments into the field 11
2.D. Uncertainties associated with crop breeding as a means
of limiting UV-B impacts 15
2.E. Uncertainties in our current knowledge of UV-B effects on
terrestrial ecosystems and plant growth forms 19
2.F. Uncertainties in the ability to extrapolate effects of
UV-B radiation on plants to the ecosystem level 24
2.G. Uncertainties with the ability to extrapolate knowledge
to higher ambient C0_ environment 24
2.H. Uncertainties in the ability to extrapolate knowledge to
include other atmospheric pollutants 27
3. RISKS TO CROP YIELD RESULTING FROM AN INCREASE IN SOLAR UV-B
RADIATION 28
3.A. Direct effects on total yield 28
3.B. Risks to yield due to a decrease in quality 42
3.C. Risks to yield due to possible increases in disease or
pest attack 43
3.D. Risks to yield due to competition with other plants 48
3.E. Risks to yield due to changes in pollination and flowering .. 51
3.F. Risks to yield due to structural plant changes affecting
harvestability 54
4. SUMMARY AND CONCLUSIONS 59
5. RECOMMENDATIONS 63
6. LITERATURE CITED 67
APPENDICES
A. Action spectra and their key role in assessing biological
consequences of solar UV-B radiation change 79
B. Stratospheric chemistry and the nature of ozone 105
C. Effects of UV-B radiation on the growth and yield of
crop plants 117
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IV
PREFACE
Since the discovery of ultraviolet radiation by J.W. Ritter in 1801, the
ecological consequences of solar UV has only recently come to the forefront of
public attention due to possible stratospheric ozone depletion resulting from
anthropogenic pollutants. Although during the past decade our knowledge of
the effects of UV-B radiation has grown prodigiously, we still lack sufficient
information for realistic appraisals of risks and uncertainties. This is
principally due to an absence of standardization in experimental procedures
and the paucity or virtual void of research in key areas. The data we do
possess, however, provide a rough basis for understanding some consequences of
enhanced solar UV radiation. On this premise, I have evaluated the possible
risks and uncertainties concerning stratospheric ozone depletion and its
impact on plants.
The first section addresses the risk to crop yield resulting from both
direct and indirect effects of enhanced solar UV-B radiation. In the second
section, the uncertainties associated with the effectiveness of UV-B radiation
are presented, and the last section deals with recommendations for
standardization of experimental procedures and future research priorities.
I thank Ms. Joan Jeschelnik of the Department of Botany, University of
Maryland, and ICF Incorporated, Washington, B.C., for their excellent
assistance in typing this manuscript and to Drs. Martyn Caldwell, N.S. Murali,
and John Hoffman for their suggestions in the organization of this work.
I would very much appreciate receiving any comments or suggestions to make
this report an accurate and complete assessment of our current state of
knowledge.
Alan H. Teramura
College Park, Maryland
October 25, 1984
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1. INTRODUCTION
In terms of biological response, ultraviolet (UV) radiation spans a
considerable portion of the electromagnetic spectrum. Therefore for
convenience, it has arbitrarily been partitioned into three wavebands. The
shortest waveband (UV-C) extends between 200-280 nm and is well known for its
germicidal effects. The middle UV region (UV-B) contains radiation between
280-320 nm and produces erythema or sunburn in humans. The longest waveband
is UV-A, which includes radiation from 320-400 nm. Although not visible to
the human eye, UV-A radidation is important to insect vision. All three are
natural components of the solar spectrum; however, due to the large absorption
by the earth's atmosphere, most of this radiation is greatly attenuated prior
to reaching the earth's surface. The primary attenuator of UV radiation is
stratospheric ozone, which efficiently absorbs nearly all wavelengths shorter
than 290 nm. Therefore, only the UV-B and UV-A wavebands naturally occur at
the earth's surface. Since UV-B radiation contains much more energy than
UV-A, it has extremely important biological consequences.
The protective ozone layer is located at an altitude of between 15 and
40 km in the stratosphere and periodically undergoes natural variations in
concentration, which results in substantial fluctuations in UV reaching the
earth's surface. For example, ozone concentrations may vary as much as 30%
within the continental United States along latitudinal gradients.
Furthermore, ozone concentrations vary temporally, such as with the passage of
regional weather systems, as well as seasonally and annually. In addition to
these natural variations, recent attention has focused primarily upon changes
in ozone concentration resulting from man-made atmospheric pollutants (NAS
1979, 1984; NRC 1982). Presently, there are some 50 molecular species
involved in over 150 chemical reactions known to involve ozone. Thus, our
current concentration of stratospheric ozone depends upon a dynamic balance
between chemical reactions that create and destroy ozone (see Appendix B,
Stratospheric Chemistry and the Nature of Ozone). Increasing releases of
these chemical pollutants tend to favor ozone destruction and reduce
stratospheric ozone concentrations, thereby allowing more UV to penetrate to
the earth's surface. For example, the photodisassociation of
chlorofluoromethane (CFM), principally from spray propellants, refrigerants,
and foam-blowing agents, contributes a substantial chloride (CIO ) source.
CFMs are so inert in the lower atmosphere that they are not readily removed by
the normal atmospheric cleansing action of precipitation. Instead, they
slowly migrate into the upper stratosphere where they eventually become
photodisassociated by high energy radiation, releasing free chlorine atoms.
Once they reach the stratosphere, these and other chemicals have a long
residence time during which they participate in catalytic reactions that
destroy ozone. For example, each chlorine atom at 30 km destroys an average
of 10,000 ozone molecules. Since stratospheric dynamics are so slow, there is
a century lag between the time these compounds are released at ground level
until the period when equilibrium ozone reductions become established.
Therefore, those atmospheric pollutants being released now, will continue to
affect stratospheric ozone concentrations for the next 100 years.
This report examines all of the published and unpublished material
currently available to assess the likely impact of projected increases in UV-B
radiation upon global crop productivity and the distribution and abundance of
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plants in natural ecosystems. The limitations to this assessment are
formidable, particularly due to a paucity of experimental data and the slow
development of appropripate technology. Therefore actual risks may be far
greater or somewhat less than current knowledge indicates.
2. ISSUES AND UNCERTAINTIES IN ASSESSING THE EFFECTS OF UV-B
RADIATION ON PLANTS
In assessing the impacts of a potential increase in global UV-B radiation
on plants, experiments ideally should be designed to develop a data base that
perfectly simulates future conditions for all plant species. Such idealized
experimental designs should include all direct effects in addition to all the
possible significant combinations of effects (interactions). For example, it
is projected that in addition to increases in the level of UV-B radiation,
atmospheric levels of CCL (carbon dioxide) will also sharply rise during the
next century. Therefore, experiments should examine both effects
independently, as well as the product of their interaction. Of course, one
also needs to know how these would change under conditions of drought, mineral
deficiency, etc. After such a perfect simulation, accounting for all possible
occurrences, it would not be difficult to assess the potential impacts of
global UB-B radiation increases with high precision. Unfortunately, such
ideal circumstances rarely, if ever, occur. In reality, we must make
assessments based upon imperfect experimental designs, with only very
selective and sometimes unrealistic growing conditions, and based on only a
few representative plant species. Therefore, our existing data base for this
assessment can lead only to possible, not conclusive, scenarios.
2.A. Issues concerning UV dose and current action spectra for UV-B impact:
assessment
Total global UV-B irradiance is dependent on a number of factors,
including solar angle, latitude and altitude, stratospheric ozone
concentration, atmospheric turbidity, and degree of cloud cover.
Additionally, the earth-sun distance and minor solar fluctuations also
contribute to annual variations in irradiance (Caldwell 1971). Because of
diurnal and seasonal variations in many of these factors, the spectral
composition of solar radiation also varies substantially. Solar UV-B
irradiance varies diurnally, peaking at solar noon. Annually, UV-B irradiance
is maximum during summer and minimum during winter. Experiments evaluating
the effectiveness of UV-B radiation on plants typically do not account for
such changes because of practical difficulties in monitoring and supplementing
UV-B radiation. Generally, supplemental UV-B radiation is provided using
filtered sunlamps as a squarewave function by using timers. Such a system
provides a proportionately greater UV irradiance during morning and late
afternoons than would be anticipated outdoors. Furthermore, supplemental
radiation is provided even during cloudy and overcast skies, when the level of
ambient UV-B may be less than 50% of clear sky irradiances due to the absence
of the direct beam component. Thus, supplemental UV-B radiation provided by
investigators in most studies is an unrealistic simulation of the natural
patterns of solar UV radiation. Caldwell et al. (1983) have designed a
modulated system to monitor ambient UV-B and provide the desired supplemental
UV-B dose. This system provides a more realistic simulation of anticipated
ozone depletion, since it modulates lamp output in accordance with actual
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levels of incoming solar UV radiation. Because of the cost of installation,
it has not been widely adopted (see Section 5, Recommendations).
Another major limitation with most UV-B studies is that the UV-B dose is
based upon the concentration of ozone during the summer solstice or other
specific day with a fixed ozone depletion. In reality, ozone concentrations
are highly variable, being maximum in the late winter and early spring and
minimum during late summer and autumn. Since a fixed ozone reduction will
result in large differences in UV irradiances during different seasons, the
assumption of a fixed level of ozone depletion further adds uncertainty in the
evaluation of UV-B dose.
Photon absorption is the primary event in a biological response to
radiation. Since photon absorption is a resonance phenomenon, its probability
is strongly wavelength dependent; hence, the effectiveness of radiation in
producing a biological response will also be wavelength dependent. The
relative effectiveness of UV radiation for a given biological response can be
expressed using a function E(A), normalized to unity at the most effective
wavelength. Such a function is known as the action spectrum for the given
biological response. Action spectra are essential for 1) comparing the
biological effectiveness produced by sources with different spectral
irradiance, 2) evaluating the relative increase of solar UV radiation due to
possible stratospheric ozone depletion, and 3) evaluating the present natural
gradients of solar UV irradiance on the earth. A brief description of these
points is presented below with more specific details given in Appendix -A
(Action Spectra and their Key Role in Assessing Biological Consequences of
Solar UV-B Radiation Change).
The source of UV-B radiation most commonly used in plant effects research
is the fluorescent sunlamp, which emits radiation principally in the UV-B
region. This sunlamp is a low-pressure mercury vapor lamp containing a
phosphor that fluoresces primarily in the UV-B region, and emits some UV-C and
UV-A radiation. Although the energy emitted comes principally from the
fluorescing phosphor, some emission from mercury vapor is superimposed upon
this, producing distinct lines in the spectrum. The spectral energy
distribution emitted from various types of lamps varies considerably.
Therefore, to compare different lamps for biological effectiveness, a
weighting function is absolutely essential. This can be illustrated using two
hypothetical sources, A and B, with a spectral irradiance in the range 280-
300 nm and 300-320 nm, respectively (see Figure 1) . The total unweighted
irradiance, which is the area under each line, is identical and equal to 100
for the two sources. Line C represents an assumed biological action spectrum.
The biologically effective irradiance (IRT7) is given by the following
relationship:
:BE = TX EX dA
where I. is the lamp spectral irradiance, and E is the relative effectiveness
of the energy to produce a response at wavelength A. Thus, the biologically
effective irradiance is the product of the action spectrum and the spectral
irradiance at each wavelength. The weighted spectral irradiance for the two
sources are shown in curves D and E: for source A and B the effective
irradiances are 83.3 and 16.7, respectively. This illustrates the point that
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10.0
7.5
LU
U
5.0 •
on
2.5
0.0
1.0
280
290 300 310
WAVELENGTH (nm)
- 0.75
- 0.5
- 0.25
0
320
TO
m
m
TI
TI
m
r>
<
m
m
Fig. 1. Two hypothetical sources, A and B, were weighted with action spectrum
C, resulting in a five-fold difference in the integrated weighted
irradiance (area under curves D and E).
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although the two sources have the same total unweighted irradiance, their
biological effectiveness differs by five-fold.
Several UV action spectra have been developed using monochromatic radiation
(Figure 2). All these share the common feature of decreasing effectiveness as
wavelength increases but have considerable variation in the rate of this
decrease. Most of the published UV action spectra to date were determined
with isolated organelles, membranes, microorganisms, etc., rather than with
intact higher plants. Caldwell (1971) has developed a generalized plant
damage spectrum based upon the combined responses of a number of different
plant species. The effects of UV-B radiation on a specific characteristic in
an isolated organelle can differ considerably from an intact plant due to
cellular shielding effects in the plant and inherent repair mechanisms. For
instance, it is now well documented that the effects of UV-B radiation can be
altered by visible radiation. UV-B radiation has a greater damaging effect
under low levels of visible radiation than under high levels (Teramura et al.
1980; Mirecki and Teramura 1984; Warner and Caldwell 1983). Thus, an action
spectrum developed on intact plants under polychromatic radiation would be
preferable, and enable a more realistic assessment of the biologically
effective increases in solar UV-B radiation. Caldwell et al. (1986) have
recently attempted to develop such an action spectrum, and although there are
experimental limitations, they were able show that it is technologically
possible.
Another essential reason for developing appropriate action spectra is for
the evaluation of radiation amplification factors (RAF), i.e., the relative
increase in biologically effective UV-B radiation associated with a specific
ozone reduction. RAF is a complex function taking initial ozone layer
thickness, percent ozone layer reduction, latitude, season, and biological
weighting function into consideration (NAS 1979). The increase in solar UV-B
radiation as a result of ozone reduction becomes appropriate only when the
biological effectiveness of this radiation is known. Without calculating an
RAF, the absolute increase of total solar UV-B radiation resulting from even
an appreciable ozone reduction is so small that it is insignificant. RAF
values for a 16% ozone reduction at three latitudes during the time of maximum
solar radiation (summer solstice for temperature and polar latitudes) are
presented in Table 1. For the same change in ozone concentration, the
increase in biologically effective UV-B radiation is significantly greater at
higher than at lower latitudes. Table 1 additionally illustrates that RAF
also varies with different action spectra.
Since solar spectral irradiance increases by orders of magnitude with
increasing wavelength in the UV-B region, the tails of the action spectra have
a profound effect on the net RAF. Figure 3 shows the calculated RAF values
for different ozone column thicknesses according to various action spectra.
The RAF values are much higher for those with steeper slopes than for those
shallow slopes. Thus, the computed biological effectiveness of solar
radiation could either be underestimated or overestimated if the action
spectra are not realistic of true plant responses.
There is a natural latitudinal gradient of solar UV-B radiation due to
differences in the prevailing solar angle and total ozone column thickness
(Caldwell 1981, Caldwell et al. 1980). Such a natural gradient in UV-B
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I
o
O -4 -
280 290
300 310 320
WAVELENGTH Inm)
330 340
Fig. 2. Weighting functions in current use for biological UV effects.
(NAS 1979)
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Table 1. Comparison of RAFs Calculated from Three Different Action
Spectra for a 16Z Ozone Depletion (from Caldwell 1981)
Latitude
20°
40°
70°
Setlow
(1974)
46.3
47.5
49.4
Caldwell
(1971)
32.0
35.0
44.0
Jones and Kok
(1966)
2.2
2.3
2.3
-------
3.0
2.0
u.
<
cr
.0
damage
0.192 0.224 0.256 0.288 0.320
Ozone Column (cm)
Fig. 3. Radiation amplification factors calculated for different ozone column
thickness, relative to 0.32 cm, and a solar angle from the zenith of
33.6° calculated according to the action spectra shown in Fig. 2. The
dashed line represents a case of 2% increase in biologically effective
radiation for a 1% decrease of ozone. The model of Green et al.
(1980) was used to calculate the solar spectral irradiance (direct
beam + diffuse) used for those RAF values (from Caldwell et al. 1986)
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radiation provides an opportunity to study plant responses to enhanced
levelsof solar UV-B radiation. Correlations between this latitudinal UV
gradient and skin cancer have been used to calculate future increases of human
skin cancer anticipated from a given ozone reduction (NAS 1984). Such
correlations between latitude and plant responses are more difficult to make
due to gross climatic and edaphic variations. However, growth chamber studies
with species from different latitudes can provide some limited information.
The steepness of the latitudinal gradient of solar UV-B irradiance depends
upon the action spectrum used. If the spectrum has a shallow slope, there
will effectively be only a very small latitudinal solar UV-B gradient, while a
steep slope will show a wide latitudinal gradient.
It is evident from the above discussion that a more realistic action
spectrum is needed for a proper assessment of the possible consequences of
enhanced UV-B radiation due to ozone depletion. An under- or overestimation
of UV-B effectiveness would result if inappropriate action spectra are used.
2.B. Issues concerning natural plant adaptations to UV
There exists tremendous variability in plant species sensitivity to UV-B
radiation (Krizek 1978, Van et al. 1976, Hashimoto and Tajima 1980, Tevini et
al. 1981 and 1982, Tevini and Iwanzik 1982, Teramura 1983). Some species
show sensitivity to current day ambient levels of UV-B radiation (Teramura et
al. 1980, Bogenrieder and Klein 1978, Sisson and Caldwell 1976) while others
are apparently unaffected by rather massive UV enhancements (Becwar et
al.1982, Ambler et al. 1978). Confusing this issue further are reports of
equally large response differences among cultivars within a species (Biggs et
al. 1981, Dumpert and Boscher 1982, Murali and Teramura 1986a,b, Murali et al.
1986). At present, the basis or mechanisms responsible for these inherent
species and cultivar differences have not been well documented. For example,
earlier investigators speculated that the apparent difference frequently
observed between monocotyledonous and dicotyledonous plants may be due to
differences in plant growth form (Van and Garrard 1975). Grasses have erect
leaves while most herbaceous species generally have horizontally displayed
leaves. More recently, however, Caldwell (1981, 1982) has concluded from
computer simulation studies that leaf orientation probably has little
effectiveness in UV avoidance due to the high proportion of the diffuse
component in the global UV-B radiation flux.
There are apparently at least three main categories of natural UV
protective mechanisms (Beggs et al. 1986), which may explain in part the great
range of species response differences. The first includes mechanisms whereby
UV-induced damage is repaired. Photoreactivation is a light-activated (UV-A
and blue light primarily), enzyme-mediated process whereby pyrimidine dimers
produced as a consequence of UV absorption by DNA are split (Rupert 1984).
Although this has not yet specifically been demonstrated in plant tissues,
numerous examples of indirect evidence exist (Beggs et al. 1986, Tanada and
Hendricks 1953, Bridge and Klarman 1973), suggesting that it is a widespread
phenomenon in plants. Excision repair is the process whereby potentially
deleterious photoproducts of UV absorption are removed and replaced by new,
correct DNA sequences. This has clearly been documented in plant tissues
(Howland et al. 1975, Soyfer 1983) and is also a widespread phenomenon in
animals. Postreplication repair involves the replication and combination of
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10
intact DNA strands in exchange for damaged ones, but is yet unknown in plant
tissues. Finally, quenching and free radical scavenging of oxygen singlets
produced by photo-oxidation may be a means of alleviating some types of
UV-induced damage. The importance and extent of these processes in
alleviating UV damage in plants has not yet been well documented.
The second category of protective mechanisms are those that tend to
minimize the damaging effects of UV-B radiation (Beggs et al. 1986). Probably
the most important of these mechanisms in plants is growth delay. If cell
division stops or is slowed upon UV irradiation, then the other repair
mechanisms alluded to above could come into play and help to ameliorate the
damage before it became lethal to the plant. Although many plants show a
growth inhibition upon UV-B radiation exposure (for example, see Teramura
1983), it is not clear whether this inhibition is the direct effect of the
damage done to the plant, or due to the activation of this protective
mechanism. For example, Dickson and Caldwell (1978) found that UV-B radiation
altered the pattern of cell division early in the ontogeney of Rumex
pat Lent La. Specifically, cell expansion was unaffected and it was the rate
and not the duration of cell division that was affected. Despite these
changes, Rumex appears to be a plant that is highly sensitive to UV-B
radiation-induced damage (Sisson and Caldwell 1976, 1977).
The third category of protective mechanisms involves those that
effectively reduce the amount of UV radiation actually reaching sensitive
plant targets. These mechanisms include structural attenuation by the cuticle
and cell wall, which seem to play only a minor role since they offer little UV
absorption (Caldwell et al. 1983a, Steinmuller and Tevini 1985). The
principal mechanism in this category is probably the selective absorption of
UV radiation by pigments located in outer tissue layers. The most attractive
biochemical candidates appear to be flavonoids and other related phenolic
compounds that occur in the vacuoles of epidermal cells and have high UV
absorption coefficients but are nearly transparent in the visible region of
the spectrum (Caldwell et al. 1983). A large number of investigators have
shown that flavonoid concentrations in plant leaves substantially increase
upon UV exposure (Wellman 1982, Murali and Teramura 1985a and 1986a,
Robberecht and Caldwell 1978, Tevini et al. 1981 and 1983, Flint et al. 1985).
However, it has not been established how many plant species increase leaf
flavonoid biosynthesis in response to increasing levels of UV-B radiation, nor
whether such an increase is sufficient to completely attenuate the damaging
effects of UV radiation. Some studies suggest that despite a large increase
in flavonoid concentration produced in leaves, UV-sensitive targets, such as
the photosynthetic machinery contained in chloroplasts, are still adversely
affected (Sisson 1981, Teramura et al. 1984a, Mirecki and Teramura 1984).
Although much of the attention concerning natural plant adaptations to
enhanced levels of UV-B radiation has been recently focused upon UV
attenuation by flavonoids, knowledge of total leaf flavonoid concentrations
alone do not account for the range of responses observed in species
sensitivity. For example, total leaf flavonoid levels found in UV-B
irradiated soybeans were less than those found in cucumber given the same UV-B
dose, yet cucumber was found to be much more sensitive to UV (Murali and
Teramura 1986a,c). Therefore, the inherent range of plant species sensitivity
to UV-B radiation is probably the product of a number of UV-protective
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11
mechanisms acting in concert within the plant. We currently need more
specific information concerning plant adaptations to UV-B radiation before we
can further refine our estimates of the ability of natural plant protective
mechanisms to compensate for the projected increases in solar UV-B radiation.
2.C. Issues associated with the extrapolation of data from controlled
environments into the field
By far, the bulk of our understanding of the impacts of UV-B radiation
comes from studies conducted in artifically controlled environments (Teramura
1983) . Because environmental conditions within growth chambers or greenhouses
are unlike those found in nature, plant responses under such conditions may
neither quantitatively nor qualitatively resemble field responses. For
instance, it is now widely known that plants grown in growth chambers appear
to be more sensitive to a given UV dose than field-grown plants (Caldwell
1981, Bennett 1981, Teramura 1982a, Mirecki and Teramura 1984). The basis for
this difference in sensitivity comes from the fact that in artificial
environments (growth chambers and greenhouses) a single factor is generally
manipulated, while all other factors are either kept constant or are optimized
for growth. Such single-factor stresses are rarely experienced by
plants outdoors. Instead, under actual conditions, plants would commonly
experience simultaneous, multiple stresses. For example, plants receive their
maximum daily UV-B irradiance during the period of maximum air temperatures
and evaporative demand for water. Furthermore, unlike plants in growth
chambers where nutrient solutions may be applied daily, most native crops and
many agricultural crops grow in soils that are low or deficient in nutrients.
In addition to these differences in physical factors, artificial environments
almost always exclude biotic factors, such as the interactions between other
plants, insects, diseases, etc.
Weighed against these shortcomings of controlled-environment studies are
the enormous complexities associated with field studies. Here, daily
fluctuations in environmental factors are superimposed upon longer-scale
seasonal and annual fluctuations making interpretation extremely difficult and
necessitating multiyear experimental designs. Both temporal and spatial
variability often result in inconsistencies in plant responses between one
year and the next (for examples see Biggs et al. 1984, Gold and Caldwell 1983,
Teramura 1981, Lydon et al. 1986).
One potentially useful approach in attempting to understand the effects of
UV-B radiation on plants under more realistic conditions has been the study of
the interactions between UV and other, commonly experienced plant stresses
such as water stress, nutrient deficiency, and low visible light stress (Table
2). As such, these studies are not attempts simply to mimic field conditions
under artificial environments. Instead, they were expressly designed to test
specific factor interactions to develop a better understanding of the effects
of UV-B radiation on plants.
Currently, five studies have assessed the combined effects of water stress
and UV-B radiation on plants. In the first two (Teramura et al. 1983 and Tevini
et al. 1983), cucumber and radish seedlings were grown in a factorial
combination of two UV-B irradiances and three levels of water stress. These
studies revealed that exposure to enhanced levels of UV radiation may affect the
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12
Table 2. Studies Examining the Interaction Between UV-B Radiation
and Other Environmental Stresses
UV-B Radiation and
Water Stress
UV-B Radiation and
Mineral Deficiency
UV-B Radiation and
Low PPFD*
Teramura et al. 1983
Tevini et al. 1983
Teramura et al. 1984a
Teramura et al. 1984b
Murali and Teramura,
1986c
Bogenrieder and Doute 1982
Murali and Teramura 1985a
Murali and Teramura 1985b
Bartholic et al. 1975
Van et al. 1976
Sisson and Caldwell 1976
Teramura 1980
Teramura et al. 1980
Warner and Caldwell 1983
Mirecki and Teramura 1984
*PPFD = Photosynthetic Photon Flux Density
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13
susceptibility of some crops, like cucumber, to water stress. Furthermore,
water stress appeared to alter the sensitivity of radish to UV radiation by
inducing flavonoid (UV-absorbing pigments) biosynthesis. Two studies (Teramura
et al. 1984a and Teramura et al. 1984b) examined the effects of UV irradiation
on the photosynthetic recovery from water stress and on the various components
of internal water relations in soybean. Plants were grown in greenhouses under
two levels of UV-B radiation and two watering prehistories (water-stressed and
well-watered). The results from these studies indicated that UV-B radiation
and water stress produced an additive, deleterious effect on photosynthesis.
Therefore, this combination of stresses was more deleterious than either stress
alone. At present, the mechanism responsible for this effect is unknown, since
UV radiation had no affect on the internal water relations of soybean (Teramura
et al. 1984b).
The most recent study (Murali and Teramura 1986c) assessed the effects of
mild water stress and UV-B enhancement under field conditions. The results
revealed no additional deleterious effects of UV-B radiation when combined with
water stress. It was hypothesized that changes in leaf anatomy, increased
flavonoid production, and reduced growth induced by water stress masked the
effects of increased levels of UV-B radiation.
To date, three studies have focused on the interactions between UV-B and
mineral deficiency. Bogenrieder and Doute (1982) compared the effects of UV-B
on the growth and photosynthesis of lettuce (Lactuca sativa) and alpine sorrel
Rumex alpinus) grown hydroponically under four mineral concentrations.
They concluded that plant productivity (accumulation of dry matter) became more
sensitive to UV-B radiation as total mineral supply decreased. Murali and
Teramura (1985a,b) hydroponically grew soybean in four levels of phosphorous
(P) under two levels of UV-B radiation. Surprisingly, they found that on a
relative basis, plant sensitivity (dry weight basis) to UV-B radiation
decreased as P level decreased. This suggests that the greatest impact of UV-B
enhancement might appear in well-fertilized (agricultural) regions, rather than
in areas of low fertility. This unexpected response was at least partly due to
an increase in the production of UV-absorbing pigments in the leaves of
nutrient-deficient plants.
One of the most obvious differences between growth chamber and field
environments is the level of visible radiation available to the plants during
growth. Since most growth chambers supply visible radiation using a
combination of incandescent and fluorescent lamps, visible irradiances are
typically quite low, usually ranging from 10% to 40% of average midday
irradiances. The concern over this difference stems from the knowledge that
many of the deleterious effects of UV radiation may be ameliorated by exposures
to longer wavelengths. If this is the case, then experiments conducted in such
growth chambers would substantially overestimate the impact of UV effectiveness
in the field. At least seven studies have addressed this question and the
germain conclusions of each are summarized in Table 3. Despite the fact that
these data include a wide diversity of plant species and growth conditions, a
clear trend emerges: plants grown in higher levels of visible radiation, more
closely approximating field conditions, are less sensitive to the deleterious
effects of UV-B radiation. A corollary to this conclusion is that plant
sensitivity to UV-B radiation is strongly influenced by the level of visible
-------
14
Table 3. Percentage Change from Mylar Controls for Photosynthesis or Growth by UV-B Radiation at Differer.
Photosynthetic Photon Flux Densities (PPFDs).
Values in Parentheses are Changes Resulting from Concomitant PPFDs
Species
-2 -1
Peak PPFD (jjinol ra s )
2000 1600 1400
800- 400-
900 500 200
70
Reference
Phaseolus vulgaris L.
Zea mays L.
Brassica oleracea
var. capitata L.
Brassica oleracea
var. acephala L.
Avena sativa L.
Rumex patientia L.
+5
+7
Lycopersicon esculentum L. -22
Pisum sativura L.
Glycine max (L.) Merr.
-6
-14
-18
-29
-38
+5
+12
-19
-58
-65
-20
(-20)
-5
(-17)
-6
-10
-5
-30
-24
+4
-23
-59
-16
-33
-33
-35
-52
-33
-27
-24
-25
(-10)
-38
Bartholic et al 1975
Bartholic et al 1975
Van et al 1980
Bartholic et al 1975
Van et al 1980
Bartholio et al 1975
Van et al 1980
Teramura et al 1980
Teramura 1980
Merecki and Teramura 1984
Merecki and Teramura 1984
Warner and Caldwell 1983
Warner and Caldwell 1983
Van et al 1980
Van et al 1980
Van et al 1980
Sisson and Caldwell 1976
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15
radiation available during growth and development, and that shaded environments
maximize this sensitivity.
Two studies (Lydon et al. 1986 and Teramura and Murali 1986) have
specifically examined the differences in UV-B radiation response between field-
and greenhouse-grown soybean. Six soybean cultivars were grown in an unshaded
greenhouse under either no UV-B radiation or a level simulating a 16% ozone
depletion (at College Park, Maryland, 39°N) during the summer solstice based
upon the generalized plant weighting function (Caldwell 1971). These same
cultivars were also grown in the field and received either ambient levels of
UV-B or levels simulating a 16% ozone depletion. In both cases, supplemental
UV was applied via cellulose-acetate-filtered FS-40 sunlamps. Cultivar
sensitivity ranking was based upon a combined plant response that included
changes in total plant dry weight, leaf area, and plant height. A summary of
those data is presented in Table 4. Taken as a whole, the relative ranking for
UV-B sensitivity based on vegetative growth observed in the greenhouse was
quite similar to that found in the field. The major difference was that UV-B
radiation produced a substantially larger (between a two- and ten-fold) effect
on greenhouse-grown plants compared with field-grown plants. However, in
specific instances, quite different conclusions could be drawn from the
individual data sets. For example, cultivar James might be considered rather
sensitive, while York was resistant to UV-B radiation based upon experimental
greenhouse data. In the field, however, these cultivars demonstrated the
opposite response. Therefore, if controlled environment-to-field
extrapolations are necessary, they must be done with the utmost caution. At
best, general trends may be implied, but specific or quantitative
extrapolations do not yet seem plausible. Part of the reason for qualitative
and quantitative differences between controlled environment and field responses
to enhanced levels of UV radiation may be due to confounding factor
interactions about which we still have relatively little information.
2.D. Uncertainties associated with crop breeding as a means of limiting
UV-B impacts
Table 5 is a summary of reports that have specifically examined the effects
of UV-B radiation on numerous crop cultivars. The table is not intended to be
exhaustive, but rather representative of the general nature of cultivar
responses. Despite the great range of experimental growth conditions and UV
doses utilized throughout these studies, large individual variation between
cultivars was shown in response to UV-B radiation. Therefore, the potential
for ameliorating the impacts of projected increases in solar UV radiation may
be present in our current crop germplasm by selecting for UV tolerance. A
pivotal concern must be acknowledged with this possibility, however: To date,
we have little experimental evidence to indicate the mechanisms responsible for
these cultivar differences. Since most crop cultivars are the descendants of a
relatively small number of original genotypes, they are all rather closely
genetically related. Differences in UV-B susceptibility then are not simply
the result of gross morphological or structural differences such as those found
between different plant species or growth forms such as grasses, herbs, shrubs
and trees. Nor are they due to gross biochemical or physiological differences
such as those known to occur between plants with different photosynthetic
pathways (C-j, C^ or CAM). Therefore, these cultivar response differences must
be due to more subtle character differences. Before crop breeding for UV
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16
Table 4. Relative Ranking of Cultivars Based Upon a Combined Growth Index.
Plants Received a UV-B Dose Equivalent to a 16% Ozone Depletion
(based upon generalized plant response function for College Park,
Maryland, 39°N) during the summer solstice (data from Lydon et al.
1986)
Cultivar
Essex
Williams
Bay
James
York
Forrest
Greenhouse*
-113
-104
-101
-79
+15
+253
Field
-75
-41
-37
-27
-6
+29
* Relative ranking according to cultivar sensitivity was based upon the
following:
(dw UV-B - dw control leaf area UV-B - leaf area control
dw control + leaf area control
+ ht UV-B - ht control
ht control ) x 100
(dw = dry weight, ht = height)
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17
Table 5. A Summary of Studies Examining Cultivar Differences in UV-B Radiation Sensitivity
Crop
Glycine max
Phaseolus vulgaris
Brassica oleracea
Cucumis sativus
Tritium aestivum
Zea mays
Oryza sativa
Number of Growth
Cultivars Condition a/ Conclusions b/
19 G.C. 20% tolerant
60% intermediate
20% sensitive
2 G.H. Cultivar Altona more
sensitive than Bragg
23 G.H. 8% tolerant
33% unaffected
59% sensitive
5 F 20% sensitive
80% unaffected
2 G.H.& G.C. BBL 290 more
sensitive than Astro
3 G.H. Maxidor sensitive
Saxa, Favorit
tolerant
2 G.H.& G.C. no difference
2 G.C. (?)
5 G.H. 20% tolerant
80% sensitive
2 G.H. Poinsett extremely
sensitive, Ashley
slightly sensitive
4 G.H. no difference (?)
7 G.C. no difference
2 F no difference
4 G.C. 25% extremely
sensitive
75% sensitive
5 G.C. 60% tolerant
40% sensitive
Basis of
Comparison c_/ Reference
d.w. Biggs et al. 1981
d.w. Vu et al. 1978
d.w. Teramura and Murali 1986
seed d.w.
leaf resistance Bennett (1981)
Dumpert and Boscher (1982)
p.s, & d.w. Van et al, (1976)
Garrard et al. (1976)
d.w. Murali and Teramura (1986a)
d.w. Krizek (1978)
d.w. Dumpert and Boscher (1982)
d.w. Biggs and Kossuth (1978)
d.w. Biggs et al. (1984)
d.w. Biggs and Kossuth (1978)
d.w. Biggs and Kossuth (1978)
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18
Table 5. A Summary of Studies Examining Cultivar Differences in UV-B Radiation Sensitivity
(continued)
Crop
Hordeum vulgare
Spinacia oleracea
Gossypium hirsutum
Pennisetum glaucum
Cucurbita pepo
Number of
Cultivars
it
3
2
2
2
3
Growth
Condition a/
G.H.
G.C.
G.H.
G.H.
G.C.
G.C.
Conclusions b/
25% tolerant
75% sensitive
no difference
both sensitive
no difference
no difference
no difference
Basis of
Comparison £/
d.w.
d.w.
d.w.
d.w.
d.w.
d.w.
Reference
Dumpert and Boscher (1982)
Biggs and Kossuth (1978)
Dumpert and Boscher (1982)
Ambler et al. (1975)
Biggs and Kossuth (1978)
Biggs and Kossuth (1978)
a/ G.H. = greenhouse; G.C. = growth chamber; F = field
b/ If data presented, sensitive means UV-B radiation reduced d.w. by at least 10% over control plants. Tolerant
indicates that UV-B resulted in less than 10% reduction in growth. In some cases, tolerant plants were even
stimulated by UV-B radiation.
£/ d.w. = total plant dry weight; p.s. = net photosynthesis.
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19
tolerance can be attempted experimentally, we must understand the genetic bases
for these response differences. Otherwise, if tolerance to UV-B radiation
werelinked (in a genetic sense) to a suite of less desirable, or totally
undesirable, characteristics, then crop breeding may not ameliorate, and could
possibly exacerbate, the impacts of UV-B enhancement. In conclusion, there
appears to be promising evidence that tolerant genotypes already exist in our
current crop germplasm, supporting the notion that breeding may limit the
deleterious impacts of increased solar UV radiation. However, a large degree
of uncertainty still remains in connection with its implementation due to the
absence of any information concerning the genetic bases for these differences.
2.E. Uncertainties in our current knowledge of UV-B effects on
terrestrial ecosystems and plant growth forms
Table 6 is a survey showing the 10 major terrestrial plant ecosystems in
the world and their relative importance in terms of net primary productivity
(NPP) and area covered. The effectiveness of UV-B radiation on plant growth
has been examined in plants representing only 4 of these 10 ecosystems, and
collectively these only account for 27% of global NPP. In two of these
terrestrial plant ecosystems, temperate forests and temperate grasslands, only
very limited preliminary data are currently available. The vast majority of
our knowledge of the biological effects of increasing solar UV radiation stems
from research focused upon agricultural crops, which account for less than 8%
of global NPP.
A survey of UV-B studies by major plant growth forms is presented in
Table 7. Of the 25 categories listed, in only 8 (32%) has the effectiveness of
UV-B radiation on some component of plant growth (dry weight, photosynthesis,
leaf area, height, etc.) been examined. Only very limited data exist for
large, woody perennial plants (trees). There are virtually no data on the
effects of UV-B radiation on lianas or vines, small woody shrubs, epiphytes, or
lower vascular plants (ferns, lichens, mosses, and liverworts). Some data on
the effects of UV-C (254 nm) radiation on lower vascular plants do exist, but
since plant responses to UV-C radiation differ quantitatively as well as
qualitatively from UV-B effects (Nachtwey 1975), these studies have been
omitted from this analysis.
Of the 314 plant families in the world (Cronquist 1981), the effects of
UV-B radiation have been examined in relatively few (Table 8). In
approximately half these plant families where some knowledge of UV effects are
known, the effectiveness of UV-B radiation on plant growth and development was
not addressed. Instead, these studies focused upon epidermal transmission to
UV or pollen germination. Therefore, in terms of utility for calculating the
potential impacts of increasing levels of solar UV radiation on global
productivity, relevant growth information exists for only about 19 families (6%
of total). Of these 19 families, only 7 include representative species in
which harvestable yield was examined (see Section 3.A, Direct Effects on Total
Yield).
In conclusion, very little information exists on the effectiveness of UV-B
radiation on native plant species. In fact, only a very small fraction of
plant families and plant growth forms have actually been extensively examined
-------
20
Table 6. Survey of UV Studies by Major Terrestrial
Plant Ecosystems (after Whittaker 1975)
Ecosystem
Tropical forest
Temperate forest
Savanna
Boreal forest
Agricultural area
Woodland and shrub land
Temperate grassland
Swamp and marsh
Desert and semidesert
Tundra and alpine areas
Global NPP-'
(109 ton/yr)
49.4
14.9
13.5
9.6
9.1
6.0
5.4
4.0
1.7
1.1
Total
Area
(106 km2)
24.5
12.0
15.0
12.0
14.0
8.5
9.0
2.0
42.0
8.0
Included in
UV Study b/
no
yes
no
no
yes
no
yes
no
no
yes
a/ NPP = net primary productivity.
b/ Only studies examining some aspect of growth.
-------
21
Table 7. Survey of UV Studies by Major Plant Growth Forms
Plant Growth Form
Included in
UV Study *
Family
Large (>3 m tall) perennial plants
Needle-leaved trees
Broad-leaved evergreen trees
Evergreen-sclerophyll trees
Broad-leaved decidious trees
Thorn-trees
Rosette trees
Bamboos
Lianas or vines
Small (<3 m tall) perennial plants
Needle-leaved shrub
Broad-leaved evergreen shrub
Evergreen-sclerophyll shrub
Broad-leaved deciduous
Thorn-shrubs
Rosette shrubs
Stem succulents
Suffrutescent shrubs
Dwarf shrub
yes
yes
no
yes
no
no
no
no
no
no
yes
no
no
no
no
no
no
Pinaceae
Rutaceae
Aceraceae, Betulaceae
Oleaceae
Ericaceae
Epiphytes
no
-------
22
Table 7. Survey of UV Studies by Major Plant Growth Forms
(continued)
Plant Growth Form
Included in
UV Study*
Family
Herbaceous plants
Ferns
Gramminoids
Rosette plants
Forbs
yes
yes
Yes
yes
Thallophytes
Lichens
Mosses
Liverworts
no
no
no
Lemnaceae
Poaceae
Polygonaceae
Plantaginaceae
Amaranthaceae
Asteraceae
Chenopodiaceae
Cruciferae
Cucurbitaceae
Euphorbiaceae
Fabaceae
Liliaceae
Malvaceae
Onagraceae
Polygonaceae
Rosaceae
Scrophulariaceae
Solanaceae
Umbelliferae
* Only studies examining UV effects on some aspect of growth.
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23
Table 8. A Survey of UV Studies by Plant Family
Family
Aceraceae
Amaranthaceae
Asteraceae
Betulaceae
Bignoniaceae
Boraginaceae
Cactaceae
Capporidaceae
Chenopodiaceae
Commelinaceae
Cruciferae
Cucurbitaceae
Cyperaceae
Ericaceae
Eupho rb i a c e ae
Fabaceae
Geraniaceae
Hippocastanaceae
Hydrocharitaceae
Lemnaceae
Liliaceae
Linaceae
Malvaceae
Oleaceae
Onagraceae
Oxalidaceae
Papaveraceae
Pinaceae
Plantaginaceae
Poaceae
Polygonaceae
Portulacaceae
Rosaceae
Rutaceae
Salicaceae
Saxifragaceae
Scrophulariaceae
Solanaceae
Umbelliferae
No Species
Examined
1
1
13
1
1
1
1
2
3
1
9
6
1
3
1
14
4
1
1
1
5
1
3
1
1
1
1
8
2
23
7
1
3
1
1
1
2
5
5
Native or
Crop Species a/
N
N
C/N
N
N
N
N
N
C/N
H
C/N
C
N
C,N
H
C/N
N
N
N
N
C/N
N
C
N
N
N
N
N
N
C/N
C/N
N
N
C
N
N
N
C
C
Type of Study b/
C
C
G , C , F*
C
F
F
F
P,F
G,F*
P
G,C,F*
G,F*
G
G,F
G
G,F*
P,F
F
G
G
G,F
F
G,F
C
G,F
G
P
G
G,C
G , C , F*
G.C.F
F
C,F
G
F
F
C,P
G*
G,F
a/ C = crop; H = horticultural; N = native.
b/ C = competition study; F = epidermal transmittance study;
study; P = pollination.
*Included yield studies.
growth
-------
24
even in a cursory fashion. To address the larger question of the potential
impact of enhanced levels of UV-B radiation on global terrestrial plant
communities and ecosystems, we must currently make the unlikely assumption that
perennial woody trees and shrubs respond in a fashion analogous to the responses
of herbaceous annual agricultural species. Furthermore, we are completely
lacking any experimental data on the interaction among various ecosystem levels
and components under UV enhancement. Clearly, much more data would be necessary
before any realistic estimates of this nature could be made.
2.F. Uncertainties in the ability to extrapolate effects of UV-B radiation
on plants to the ecosystem level
Ecosystem composition and function is dependent upon the influence of
various biotic and abiotic factors. Changes in these factors can lead to
alterations in species composition and proportion depending on the extent of
change, initial species diversity, and genetic variability in resistance to
change. Various plants and microorganisms show large genetic variation in UV
resistance. In microorganisms particularly, such resistance can evolve rapidly.
In higher plants, however, it is not yet known whether such evolution can occur
within the timeframe in which the changes in UV-B radiation are anticipated.
Therefore, it is presently not possible to predict the future evolutionary
response to increases in UV-B radiation because of insufficient information on
the inter- and intra-specific differences to UV-B radiation.
However, it could be generalized that if changes in UV-B radiation are large
(by more than 100%) and the rate of change is rapid (occurring over a period of
decades rather than centuries), then there will occur a large number of
extinctions and extensive changes in ecosystem composition function due to
differential sensitivity and response rates. If, on the other hand, change is
small and occurs more gradually, there may be considerable evolutionary
accommodation (Antonovics 1975). There is evidence that the evolution of UV
resistance has been influential in the early history of life, and that species
have developed protective mechanisms when exposed to higher levels of UV-B
radiation (see Section 2.B, Issues Concerning Natural Plant Adaptations to UV
Radiation). This genetic variation in UV resistance indicates that plants have
the potential to evolve UV resistance. However, we still have only very
preliminary data on the consequences of subtle shifts in species interactions,
such as changes in competitive ability, upon future community and ecosystem
composition. For example, Caldwell (unpublished report, 1985) has reported
changes in competitive interactions between wheat and wild oats that may be
associated with increased UV levels. Without a more complete understanding of
such changes, further assessment on this area is currently not possible.
2.G. Uncertainties with the ability to extrapolate knowledge to higher
ambient C0_ environment
Global atmospheric carbon dioxide (CCO concentration has been gradually
increasing over the centuries. Measurements of CO. concentration in ice cores
from Greenland and Antarctica indicate an ambient CO, concentration of about
205 ppm some 20,000 years ago and approximately 280 ppm during the past 10,000
years (Neftel et al. 1982); values from 1905 indicate an early industrial level
of about 290 ppm (Reelings 1978). Since 1957, both at Mauna Loa, Hawaii, and in
Antarctica, atmospheric C0» concentration has been continuously monitored. The
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25
records at Mauna Loa indicate that in 1968 the atmospheric CO- concentration was
317 ppm; today it is 340 ppm. In the decade between 1958 and 1969, the ambient
CO- concentration increased by 0.7 ppm per year, while from 1970 to 1982 it
increased by 1.3 ppm per year. It is anticipated that sometime between 2075 and
2100, the atmospheric CO concentration will reach 600 ppm (Gates 1983). The
major source contributing to the increase in CO^ concentration has been the
burning of fossil fuels. It is estimated that the world's remaining recoverable
resources of oil, gas, and coal contain some 4.13 x 1012 metric tons of carbon.
If this amount is burned and half remains airborne, the atmospheric CO-
concentration would increase by a factor of four (Gates 1983).
At present we have no experimental evidence on the effects of enhanced
levels of UV-B radiation under increased levels of atmospheric CO,-. However, on
the basis of other plant responses reported in the literature, some speculations
could be made. It should be emphasized that these represent only potential, and
not actual, circumstances. The individual effects of enhanced levels of UV-B
radiation and increased atmospheric CO- concentration on various plant
parameters are summarized in Table 9. In general, UV-B radiation has
deleterious effects, while increased CO has potentially beneficial effects on
plant growth and development.
Photosynthesis is ordinarily inhibited by UV-B radiation but is increased by
higher levels of CO- concentration, especially in C- plants. This results in a
reduction of plant productivity by UV-B radiation and an increase in
productivity by increased CO- concentration. Since CO^ increases plant growth
to a greater extent, the net effect of an interaction Between UV-B radiation and
increased levels of CO- may be a general compensation of the deleterious effects
of UV-B radiation on plant productivity.
Water-use efficiency increases with an increase in CO concentration due to
decreased stomatal conductance and increased photosynthesis. On the other hand,
in UV-B irradiated plants, water-use efficiency decreases due to the inhibition
of photosynthesis. This results in increased drought tolerance with elevated
ambient CO- concentration, and a decrease in tolerance with enhanced UV-B
radiation. The net effect resulting between these two environmental changes
would be a compensation of the increased drought tolerance by UV-B radiation.
Increased atmospheric CO- concentration has been shown to result in early
flowering and accelerated maturity without a concomitant reduction in
plant productivity. UV-.B radiation inhibits flowering in some plants but
stimulates flowering in others, with no apparent effect on maturity. The net
anticipated effect of a combination of increasing levels of UV-B radiation and
CO- concentration would be an increase in plant flowering and maturity which
could then lead to longer-term changes in the pattern of community succession.
Responses to both increased levels of UV-B radiation and CO concentration
produce inter- and intraspecific variations, which could result in changes in
the competitive balance among various plant associations (Gold and Caldwell
1983; Strain and Bazzaz 1983). The product of these two environmental changes
could lead to an eventual alteration in plant composition and community
structure. Changes in competitive balance could especially have adverse effects
in agricultural systems if weeds increase their competitive advantage over crop
plants. Since an increased need for weed control requires more tillage and/or
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26
Table 9. Summary of UV-B and CO Effects on Plants
(Lemon 1983; Teramura 1983).
Plant Characteristic
Enhanced UV-B
Doubling of CO,
Photosynthesis
Leaf conductance
Water use efficiency
Dry matter produc-
tion and yield
Leaf area
Specific leaf weight
Crop maturity
Flowering
Interspecific
differences
Intraspecific
differences
Drought stress
Decreases in many C_
and C, plants
No effect in many plants
Decreases in most plants
Decreases in many plants
Decreases in many plants
Increases in many plants
No effect
May inhibit or stimulate
flowering in some plants
Species may vary in
degree of response
Response varies among
cultivars
Plants become less sen-
sitive to UV-B but not
tolerant to drought
In C plants, increases
up to 100% but in C
plants only a small
increase
Decreases both in C_ and C,
plants
Increases in both C_ and C,
plants
In C_ plants, almost
doubles but in C, plants,
only a small increase
Increases more in C_ than in
C, plants
Increases
Accelerated
Flowers produced earlier
Major differences occur
between C- and C. plants
3 4
Response may vary among
cultivars
Plants become more
drought tolerant
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27
herbicide application, the increase in production cost could render somet crops
uneconomical to produce, and thus potentially alter the economic importance of
some plants.
It is predicted that an increase in CCL concentration would result in major
climatic changes. Some regions of the world, including large portions of the
central U.S. and much of eastern Europe and USSR, would experience serious
decreases in precipitation, while the climates of Canada, Alaska, Western
Europe, North and East Africa, and others may become wetter. Therefore, the
great grain belts are predicted to become much drier (Gates 1983) and probably
less productive. It has been shown that water stress increases plant tolerance
to UV-B radiation (Teramura et al. 1984, Murali and Teramura 1986c). Thus, in
these drier regions, UV-B radiation may not be as effective in reducing plant
growth. Moreover, in the wetter regions, UV-B radiation may also not
appreciably affect growth since increased levels of C0~ would have the
predominate effect.
The long-term effects of increased levels of atmospheric CO. are not fully
known. However, it is projected that plant carbon:nitrogen (C/N) ratios would
increase, and that the increase in the rate of plant succession would produce
more organic matter available for decomposition. With high C/N ratios, the rate
of mineralization would decrease due to limitations in the rate of
decomposition, and thus the availability of nitrogen, phosphorus, and other
nutrients might ultimately limit growth. Under mineral deficiency, plants have
been demonstrated to be more tolerant to UV-B radiation (Murali and Teramura
1984a, 1984b). Although the relative impact of UV-B may be somewhat lessened by
mineral deficiency, plant productivity and yield would nonetheless be
deleteriously affected.
There is a very high degree of uncertainty in the assessment of these
combined scenarios because of the lack of actual experimental data on the
complex interactions between increased C0_ concentration and UV-B radiation. In
general, it appears that direct, negative effects of UV-B radiation on plant
growth and development may be somewhat compensated by increased atmospheric CO.
levels. However, the complex indirect effects resulting from changes in the
competitive balance among species and changes in the quality and quantity of
energy inputs into various ecosystem trophic levels cannot be assessed at this
time. In light of the extreme importance of these interactions, the potential
risks warrant great concern.
2.H. Uncertainties in the ability to extrapolate knowledge to include other
atmospheric pollutants
One of the growing environmental problems that has been of great concern to
many industrialized countries is the increasing extent and occurrence of lower
atmospheric air pollution. Primarily anthropogenic in origin, the major
pollutants include ozone, sulfur oxides (SOx), and nitrogen oxides (NOx). All
three major pollutants are deleterious to plant growth and development.
According to the National Crop Loss Assessment Network, farm crop losses in the
United States in 1981 due to air pollution amounted to between $1 billion and $2
billion. Ozone alone, or in combination with SOx and NOx, is responsible for up
to 90% of the crop losses in the U.S. caused by gaseous air pollutants (Heck et
al. 1982). The major sources of air pollutants are transportation vehicles,
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28
industrial production facilities, and electrical power generation, each
accounting for 60%, 16%, and 14% of the total, respectively (Mudd and Kozlowski
1975) . The mechanism of ozone damage is through the destruction of the
structural integrity of membranes, which impairs both membrane transport and ion
uptake (Heath 1975). Sulfur dioxide affects photosynthesis through the lowering
of pH, which results in chlorophyll destruction by loss of magnesium ions (Mudd
1975). The mode or target of injury of nitrogen dioxide (NO., has not been
fully examined. Some studies report that it may arise due to enzyme
inactivation through acidification of the cell milieu (Tylor et al. 1975). Many
investigators have studied plant responses to combinations of 0,, SO., and NO .
In most plants, the deleterious effects were additive and, in a few cases, X
multiplicative (Reinert et al. 1975).
UV-B radiation has been shown to inhibit photosynthesis through the
inactivation of the reaction centers of PS II (Iwanzik and Tevini 1982, Tevini
and Iwanzik 1983, Iwanzik et al. 1983), consequently reducing plant
growth (Teramura 1983). At present, no data are available on the interaction
between UV-B radiation and various air pollutants. However, since both UV-B
radiation and various air pollutants independently have deleterious effects,
their net interactions are anticipated to be additive or multiplicative.
Because of the complete absence of experimental data, there is a high degree of
uncertainty in this projection. •
3. RISKS TO CROP YIELD RESULTING FROM AN INCREASE IN SOLAR
UV-B RADIATION
3.A. Direct effects on total yield
During the past 10 years, there have been nine field studies examining the
effects of UV-B radiation on crop yield. Three other field studies have been
reported (Caldwell et al. 1975, Caldwell 1983, Dumpert 1983); however,
harvestable yield was not the focus of these studies. Combined, these nine
studies included 22 crop species. The most widely examined species was corn
(Zea mays), which was included in six of the nine studies, soybean (Glycine max
found in four, and tomato (Lycopersicon esculentum), bean (Phaseolus vulgaris),
and potato (Solanum tuberosum) each found in three studies. The relevant
details of each study are listed in Table 10 and a brief summary follows below.
A more comprehensive review of crop responses to UV-B radiation can be found in
Appendix C (Effects of UV-B Radiation on the Growth and Yield of Crop Plants).
Ambler et al. (1978) grew eight species of crops (Table 11) in a field at
Beltsville, Maryland (39°N). Species were paired and grown in six plots with a
lamp irradiation system maintained 1.6m above the plants. The irradiation
system consisted of a linear arrangement of unfiltered Westinghouse BZS-CLG and
FS-40 sunlamps. A two-dimensional gradient was established: one parallel to
the lamps and another at right angles. Of the eight species examined, only one,
broccoli, showed a significant UV effect (Table 10) although the authors
suggested that sorghum and corn also were affected. There are two major areas
of concern with the study. First, since unfiltered lamps emit both UV-B and
UV-C radiation, both quantitative and qualitative effects must be reviewed with
utmost caution (Nachtwey 1975). Second, where effects were reported,
only significant differences were found for plants directly beneath the lamps,
and not at a location farther away from lamps with the same (or higher) UV dose.
-------
Table 10. Summary of Field Studies Examining the Effects of UV-B Radiation on Crop Yields.
Values represent percent changes from controls
Ambler
et al.
(1978)
(1)
Bartholic
et al.
(1975)
(2)
Becwar
et al.
(1982)
C3)
Cucurbita maxima 0
Cucurbita pepo
Phaseolus vulgaris 0 +12 to +15
Triticum aestivum
Zea mays 0 +29 to +39
Spinacia oleracea
Sorghum bicolor 0
Capsicum annum
Glycine max 0
Cynodon dactylon
Beta vulgaris 0
Brassica oleracea var.
capitata
Brassica oleracea var. -24 to -45%
botrytis
Lycopersicon esculentum -5 to -26
Nicotiana tobaccum
Raphanus sativus
Pennisetum glaucum
Solanum tuberosum
Brassica juncea
Vigna unguiculata
Oryza sativa
Arachis hypogaea
Biggs and Biggs Eisenstark
and Kossuth et al. et al.
(1978) (1984) (1984)
(4) (4) (4)
-14 to -90
-11 to -39
-9 to -43
-18 to -38
-5
0
Esser
(1980)
(5)
+53 to -75
Hart
et al.
(1975)
(1)
-79 to -87 0
+11 to -56
+19 to -49
-2 to -41
Teramura
(1981)(1982)(1983)
(4)
-8
(1) Unfiltered Westinghouse BZS-CLG and FS-40 sunlamps
(2) Ambient UV filtered with Mylar Tape S or polyethylene
(3) Ambient UV filtered with cellulose acetate, Aclar, or Mylar
(4) Westinghouse FS-40 sunlamps filtered with cellulose acetate or Mylar
(5) Unfiltered Philips TL 40/12 sunlamps and lamps filtered with Schott WG 305 (2 and 3 mm) filters
-------
30
Table 11. Details of Field Study by Ambler et al. (1978) a/
Crop
Yield
Character b/
Percent
Change
Significance c/
Cucurbita
maxima
(squash)
fruit f.w.
-23 to -26
ns
Phaseolus
vulgaris
(bean)
Glycine max
(soybean)
Beta vulgaris
(sugar beet)
Sorghum
bicolor
(sorghum)
Zea mays
(corn)
Brassica
oleracea
var.
botrytis
(broccoli)
fruit f.w.
seed d.w.
root f.w.
shoot f.w.
ear f.w.
fruit f.w.
+2 to -12
+0.3 to 3
-34 to -46
-14 to -15
-24 to -44
-24 to -45
ns
ns
ns
ns (P=0.3)
ns (P=0.2)
(P=0.01)
a/ Irradiation system used was unfiltered Westinghouse BZS-CLG and FS-40
sunlamps; the percent ozone change cannot be calculated due to the inclusion
of UV-C radiation.
b/ f.w. = fresh weight, d.w. = dry weight
c/ ns = not significant
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31
Therefore, shading may be a complicating factor in this study, although this
possibility was not discussed.
Bartholic et al. (1975) conducted field exclusion studies in Gainesville,
Florida (29° 36'N) where ambient levels of UV-B were filtered through plastic
films of Mylar Type S or polyethylene (Table 12). Since plants were grown under
panels covered with these films, only the direct beam component of ambient UV
was removed (which represents approximately one-half the total ambient UV
present). Three crop species were tested (beans, corn, and tomato), and each
treatment was replicated five times in three KT plots. Compared with uncovered
plots, total bean yields under Mylar decreased 15% and under polyethylene by
11%. In corn, Mylar reduced yield by 28% and polyethylene by 23% compared with
uncovered plots, resulting in a 30-40% increase in ear fresh weight in plants
growing under ambient levels of UV-B. Tomato matured significantly earlier
under Mylar, resulting in an apparent decrease in fruit weight in plants growing
in uncovered plots. Although no data were given, these authors did mention the
possibility of confounding spidermite damage in the corn study. Apparently,
there was a significant effect of growing plants under the plastic panels
compared with uncovered plants. Despite both materials being reported as
reducing PAR (photosynthetically active radiation) by only 7% each, there may
have been a shading problem associated with the panel framework. Alternatively,
a difference may have been maintained in leaf temperatures or soil moisture as a
direct result of the exclosures themselves.
The study by Becwar et al. (1982) was also an exclusion study (Table 13)
located at 3000 m in the Colorado Rocky Mountains (39° ll'N). Three types of
filters were used: Mylar, Aclar, and cellulose acetate. Four crop species were
examined including Alaska pea (Pisum sativus), potato, radish (Raphanus
sativus), and wheat (Triticum aestivum). Plants were grown in pots with peat,
vermiculite and sand. The only UV effect reported was a decrease in wheat
height (between 8% and 19%, depending upon plant age), with no corresponding
change in total plant dry weight. A second study was also conducted at the high
elevation field site using filtered FS-40 sunlamps, which supplemented ambient
levels of solar UV-B. Lamps were held in standard two-lamp fluorescent fixtures
and filtered with cellulose acetate and Mylar. These were suspended l.lm above
the plants and produced no significant effect on crop yield despite a calculated
52% UV enhancement (based on the generalized plant action spectrum by Caldwell,
1971) compared with sea level irradiances at the same latitude. Unfortunately,
there were no plants grown under a UV irradiance that simulated the dose plants
received at sea level as control to make actual comparisons.
Biggs and Kossuth (1978) grew nine crops (Table 14) in raised beds filled
with a synthetic soil mix in Gainesville, Florida (29° 36'). Yield data were
reported for seven of the nine crops. UV-B radiation was supplemented in the
field with a linear arrangement of six FS-40 sunlamps mounted end-to-end and
kept at a 12% angle relative to the soil surface. This produced a "gradient" in
UV-B irradiances. Control plants were those growing without lamps above them
adjacent to those receiving the highest UV dose. Although "significant" UV
effects were reported in half the plants, no indication of the statistical tests
used were found in the report, nor were other descriptive statistics given
(such as S.D. or S.E.). One area of concern was the lack of consistency of
effects in this study. For instance, the greatest reductions in yield were
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32
Table 12. Details of Field Study Excluding Ambient Solar UV
by Bartholic et al. (1975) a/
Yield Percent
Crop Character b/ Change Significance
Zea mays ear f.w.(?) +29 to +39 P=0.05
(corn)
Lycopersicon fruit f.w.(?) -5 to -26 (?)
esculentum
(tomato)
Phaseolus fruit f.w.(?) +12 to +15 P=0.05
vulgaris
(bean)
a/ Irradiation system used was Mylar and polyethylene exclusion panels of
ambient UV; ozone was simulated to increase
b/ f.w. = fresh weight
-------
33
Table 13. Details of Field Study Excluding Ambient Solar UV
by Becwar et al. (1982) a/
Crop
Yield
Character b/
Percent
Change
Significance c/
Raphanus
sativus
(radish)
Solanum
tuberosum
(potato)
root d.w.
tuber d.w.
+11 to +20
-1 to -17%
ns
ns
a/ Irradiation system used was Mylar, Aclar, and cellulose acetate exclusion
panels for ambient UV and filtered FS-40 sunlamps; ozone was simulated to
increase
b/ d.w. = dry weight
c/ ns = not significant
-------
34
Table 14. Details of Field Study by Biggs and Kossuth (1978) a/
Crop
Yield
Character b/
Percent
Change
Significance c/
Solanum
tuberosum c/
(potato)
Lycopersicon
esculentum
(tomato)
Zea mays
(corn)
Vigna
unguiculata
(blackeye
pea)
Arachis
hypogaea
(peanut)
Cucurbita
pepo
(squash)
Brassica
juncea
(mustard)
tuber f.w.(?) +2 to -21
fruit f .w. (?) -11 to -39
ear dia.
fruit d.w.(?)
leaf f.w.
-3 to +1
fruit f.w.(?) -18 to -38
0 to -24%
fruit f.w.(?) -14 to -90
-9 to -43
ns
P=0.05(?)
ns
P=0.05(?)
ns
P=0.05(?)
P=0.05(?)
a/ A gradient of UV-B irradiances was produced by using a linear
arrangement of sunlamps (cellulose acetate filtered FS-40). Plants
without lamps above them were controls receiving no supplement UV-B
irradition.
b/ f.w. = fresh weight
c/ ns = not significant
-------
35
often found in plants growing in the lowest UV irradiance, or the largest UV
effects were found in plants growing adjacent to ones showing little or no
effect. By using a gradient, essentially each plant received a uniquely
different UV dose, therefore plants and treatments must, by necessity, be pooled
for statistical analysis. Such data manipulation would almost certainly add a
great deal of experimental variability and lead to further difficulty in
interpretation.
In another field experiment, Biggs et al. (1984) studied the effects of UV
radiation on crop yield over the course of several growing seasons in four
field- grown species including rice (Orzya sativa), wheat, corn, and soybean
(Table 15). Again, plants were grown in raised beds filled with synthetic
soils, but in this instance UV irradiation was not supplied as a gradient.
Instead, each system contained six FS-40 sunlamps (three rows of two linearly
arranged lamps) filtered with 3-, 5-, or 10-ml cellulose acetate providing 32%,
23%, or 16% UV enhancements (based on the generalized plant action spectrum)
above ambient. Control plants were grown under Mylar-filtered lamps. Despite
relatively large reductions in rice yield (up to 50%), these were not found to
be statistically significant. The only significant yield reduction reported was
for wheat (5% reduction) and only for one of the two experimental years. The
data for rice, corn, and soybean were highly variable and therefore only very
substantial changes could be statistically detected. The underlying reasons for
this high degree of variability are presently unknown.
Eisenstark et al. (1984) grew corn (Table 16) for three growing seasons in
Columbia, Missouri (38° 57'N). Plants were grown in large pots and irrigated
during the study. Two levels of UV radiation were supplied by cellulose-
acetate-filtered FS-40 sunlamps simulating a 7% and 21% ozone depletion (based
upon the generalized plant action spectrum). There were two types of controls:
in one, plants were grown under lamps filtered with Mylar, and in the second,
plants were grown without overhead lamps. In the most recent field study, half
the plants were irradiated 4 weeks after germination (vegetative) and the other
half, at tassel formation (reproductive). Plants were found to be particularly
susceptible to UV-induced effects during tassel development (Eisenstark and
Perrot 1985). In plants irradiated as seedlings, 7% and 21% ozone reductions
produced total grain yield reductions of 23% and 32%, respectively, when
compared with Mylar control plants.
However, even larger differences were found when plants grown under either
Mylar or cellulose-acetate-filtered lamps were compared with those grown without
overhead lamps. In this case, yield was reduced by 80% in plants filtered by
Mylar and 87% in those grown under cellulose acetate. Even more dramatic was
the differential ear maturation: 59% matured when grown in sunlight without
overhead lamps, none matured under cellulose-acetate-filtered lamps and only 18%
matured under Mylar-filtered lamps. Although the authors suggest that this
large lamp effect is perhaps due to the additional UV-A emitted from the
sunlamps, this UV-A supplement is very small (only several percent) relative to
that UV-A present in midday solar radiation (see Caldwell et al. 1984). At
present, these responses are not well understood and certainly need to be
clarified.
Esser (1980) conducted field studies in Frankfurt, Federal Republic of
Germany (50° N), on six crop species, but yield was only reported in four:
-------
36
Table 15. Details of Field Study by Biggs et al. (1984) and Biggs (1985) a/
Crop
Yield
Character b/
Percent
Change
Significance c_/
Dry z a
sativa
(rice)
seed d.w.
no. seed heads
-26 to -47
-18 to -50
ns
ns
Triticum
aestivum
(wheat)
Zea mays
(corn)
Glycine
max
(soybean)
seed d.w. (1982) -5
seed d.w. (1984) 0
ear f.w. (?)
pod d.w. (?)
P=0.05(?)
ns
ns
ns
a/ Irradiation system used was cellulose acetate and Mylar-filtered FS-40 sunlamps;
ozone was simulated to decrease by 16%, 23%, and 32%.
b/ d.w. = dry weight; f.w. = fresh weight
c/ ns = not significant
-------
37
Table 16. Details of Field Study by Eisenstark et al. (1985)
Simulated
Ozone
Yield Percent Change Irradiation
Crop Character Change Significance (%) System
Zea mays grain dry -87 P=0.05 -7,-21 Cellulose acetate-
(corn) weight and Mylar-filtered
FS-40 sunlamps
-------
38
bean, cabbage (Brassica oleraceae var. capitata), spinach (Spinacia oleracea)
and potato (Table 17). He used linearly arranged Philips TL 40/12 sunlamps
suspended 3 m above the plants and produced four UV enhancements using a
combination of reflectors and Schott WG305 filters. His two highest UV doses,
simulating 40% and 15% ozone reductions (based on the generalized plant action
spectrum) were produced by using unfiltered lamps. Although significant yield
reductions were found in the four crops tested, these were only found under
unfiltered lamps. In fact, yields for spinach, cabbage, and bean appeared to
increase under filtered lamps.
Hart et al. (1975) grew plants (Table 18) under unfiltered FS-40 sunlamps at
Beltsville, Maryland (39° N). Lamps were linearly arranged and suspended 3.7 m
above the ground. Almost no other details of the experiment were given and no
actual yield data are presented. Only a short descriptive summary of the
results are reported in a table. Because of the complete absence of data, this
study may only be useful in a very qualitative way. Even in this light, one
must be careful with any interpretations drawn from this study due to the
presence of UV-C radiation from these unfiltered lamps.
Teramura has grown soybeans for five seasons (Table 19) at a farm owned and
operated by U.S.D.A. in Beltsville, Maryland (39° N). During the first two
years, six different soybean cultivars were grown under filtered FS-40 sunlamps
oriented perpendicular to the soybean rows (rows oriented in an east-west
direction). This arrangement avoids the large variation in UV irradiance along
the length of the bulb, which is a major problem with linearly arranged
(end-to-end) lamps. (See Section 5, Recommendations.) Control plants were
grown under Mylar-filtered lamps. In the last three years, only two cultivars
were grown to increase the sample size to at least 200 plants per cultivar per
treatment. Field experiments simulated 0, 5%, and 16% ozone depletions (based
on the generalized plant action spectrum) during the first year and 0, 16%, and
25%
ozone depletions thereafter. Significant reductions in crop yield were found
only in 1981 for cultivars Essex and James. Interestingly, total seed
yield/plant was significantly increased in cultivar Williams during this same
year. Although similar general trends were found in 1982, there were no
significant differences associated with increasing UV-B radiation. Yield was
decreased in cultivar Essex and increased in cultivar Williams, in 1984, 1985.
and 1986, by supplemental UV-B. In 1983, a substantially higher yield per plant
(on a relative basis) was found in cultivar Essex, which was opposite to that
observed in the previous 2 years. One critical caveat that must be included
with this observation is that 1983 was an extremely dry-year. Actual seed
weights of control plants during 1983 were only 20-30% of those harvested in
1981 and 1982. Therefore, it is rather tentative whether these 1983 data are
representative of true (normal) field trends. This graphically illustrates the
importance of multiyear studies to obtain a more representative description of
the potential impacts of an increase in solar UV radiation reaching the surface
of the earth. It also emphasizes the need to monitor other environmental
variables in addition to UV radiation.
Soybean yield is Influenced by microclimatic factors as well as total UV-B
dose. Yield appears to be strongly Influenced bv the number of days of
precipitation, the number of days when maximum temperature exceeds 35°C, and the
number of days where total irradiance is low (i.e. , cloudy days).
-------
39
Table 17. Details of Field Study by Esser (1980) a/
Crop
Yield
Character b/
Percent
Change
Significance
Solanum
tuberosum
(potato)
Spinacia
oleracea
(spinach)
Brassica
oleracea
var.
capitata
(cabbage)
Phaseolus
vulgaris
(bean)
tuber f.w.
leaf f.w.(?)
leaf f.w.
fruit f.w.(?)
-2 to -41
+11 to -56
+19 to -49
+53 to -75
P=0.05(?)
P=0.05(?)
P=0.05(?)
P=0.05(?)
a/ Irradiation system used consisted of unfiltered Philips TL 40/12 and
Schott WG305 filtered TL 40/12 sunlamps; ozone was simulated to
decrease by 3%, 8%, 15%, and 40%.
b/ f.w. = fresh weight
-------
40
Table 18. Details of Field Study by Hart et al. (1975) a/
Crop
Yield
Character b/
Percent
Change
Significance c/
Lycopersicon
esculentum
(tomato)
Capsicum
annum
(bell pepper)
Zea mays
(corn)
Glycine max
(soybean)
Arachis
hypogaea
(peanut)
Pennisetum
glaucum
(pearl
millet)
Cynodon
dactylon
(Bermuda
grass)
fruit no.
fruit size
fruit size
fruit no.
grain wt.
bean wt.
nut wt.
shoot d.w.(?)
shoot d.w.(?)
no data given
no data given
no data given
no data given
no data given
no data given
no data given
no data given
ns
ns
ns
P=0.05(?)
ns
ns
ns
ns
ns
a/ Irradiation system used consisted of unfiltered FS-40 sunlamps; ozone
change cannot be calculated due to the inclusion of UV-C radiation.
b/ d.w. = dry weight
c/ ns = not significant
-------
41
Table 19. Details of Field Study by Teramura (1981-1985) that Measured
Percent Change in Seed Dry Weight of Soybean (Glycine max) from a
Simulated Decrease in Ozone3
Cultivar
Simulated Ozone Change (X)
1981
-16
1982
-16 -25
1983
-16 -25
1984
-16 -25
1985
-16 -25
1986
-16 -25
Bay -10 +6 -8
Essex -25b -12 -23 +39b +6 +14b -7 +6 -20b -5 -19b
James -14b -22 -25
Williams +22b +9 +14
York
Forrest -- -14 +27
a Irradiance was provided by Mylar (control) and cellulose acetate (UV-B supplement) filtered FS-40 sunlamps.
Significantly different from controls at P<0.05 level.
After initially screening 23 cultivars in the greenhouse, 6 were chosen for field experimentation. These six were picked
because they represented the range of UV sensitivity found in the greenhouse, including very sensitive as well as very
tolerant cultivars. Beginning in 1983, only Essex, a very sensitive, and Williams, a very tolerant cultivar were planted
in the field to increase experimental sample sizes to 200 plants per treatment. As the table above shows, yields for
Essex were generally reduced by the higher UV supplementation (25% ozone depletion) while the lower supplementation showed
variable results. In the UV-tolerant cultivar Williams, a 16% ozone depletion generally increased yield, with much more
variable results found at the higher ozone depletion. One important point to be made is that the sensitive cultivar Essex
is currently replacing other older cultivars, including Williams, and is becoming one of the most widely planted soybeans
in the U.S. This is because Essex has other features that crop breeders find superior to Williams. In a UV-enriched
environment, however, Essex will be deleteriously affected. Therefore, superior cultivars that crop breeders are
developing today may not be suitable for the future should the environment change.
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42
Interestingly, the total amount of precipitation received is not nearly as
important as is its distribution over the growing season. In general, yield
decreases as the number of hot days increases, and increases as the number of
days with precipitation approaches 25 in the growing season. Further increases
in the number of days with precipitation decrease yield. Overall, those
microclimatic factors that induce plant water stress (i.e., sunny, hot days with
widely dispersed precipitation) reduce yield, while conditions of reduced water
stress (i.e., cloudy, cooler days with frequent precipitation) enhance yield up
to a threshhold point when yield is again reduced. By contrast, the effects of
UV-B appear to be more pronounced in years when microclimatic factors favor high
yield. The effects of UV-B have been shown to be masked under conditions of
plant water stress (Murali and Teramura 1986c). The relative importance of UV-B
is a function of the cultivar and other prevailing microclimatic factors. For
example, in Essex, total seed yield can be predicted within 95% confidence
intervals with a regression model which includes total UV-B dose, number of
precipitation events, and the number of days where air temperature exceeds 35°C
as predictor variables.
Despite the broad range of experimental protocols and dosimetry used by
various investigators, it appears that increases in solar UV radiation
penetrating to the earth's surface could potentially have a deleterious impact
upon global crop yields. Even discounting the data from the three unfiltered
lamp studies (Ambler et al. 1978, Esser 1980, Hart et al. 1975), there are still
more instances of significant reductions in yield than reports of no effect at
all. The uncertainty associated with this conclusion is moderate to large,
since all these studies were imperfect validations, suffering from one problem
or another in experimental design or dosimetry. Furthermore, only three studies
(Biggs et al. 1984, Eisenstark et al. 1984, and Teramura 1981-1984) include
multiyear observations where longer-scale environmental variability has been
taken into consideration. Even small reductions in yield can have enormous
consequences when considering the fine balance of the economics of modern
agriculture. Therefore the data concerning the effects of increasing UV
radiation to global agricultural productivity imply large risks and warrant
great concern.
3.B. Risks to yield due to a decrease in quality
The quality of crop yield has only been quantitatively examined in a few
limited studies. Biggs and Kossuth (1978) reported differences in the quality
of tomato and potato yields from field trials conducted in Gainesville, Florida
(see previous section on crop yield). In that study, they reported that the
number of abnormally shaped tomato fruit (called defective in the study)
decreased under enhanced levels of UV-B radiation supplied from filtered FS-40
sunlamps. The range of this reduction in defective fruit was from 11% to 41%
compared with ambient grown controls; however, there was no clear relationship
between the magnitude of this reduction and UV-B dose. They also reported a 6%
to 23% reduction in the number of culls (rots, cracks, sunscald, etc.) in plants
receiving moderate UV-B enhancements, while those receiving low enhancements of
UV-B radiation produced a 10-34% increase in culls. Again, there was not a
simple, linear relationship between UV dose and the number of culls produced.
Biggs and Kossuth (1978) also report a 3-13% increase in the mean potato
weight of grade A large potatoes under enhanced levels of UV-B radiation, but
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43
not in any other grade categories. Again, there did not appear to be a specific
UV-B dose-response relationship for this observation. In both tomato and
potato, no data were included to indicate whether these differences were
significant, and if so, the specific statistical tests used to determine this.
In a field study conducted in Beltsville, Maryland, Ambler et al. (1978)
examined the effects of UV radiation supplied from unfiltered sunlamps. They
reported that the sugar content in sugar beet significantly increased between
17% and 21% with increasing UV-B irradiance. However, they only observed these
significant increases in plants directly beneath the lamp irradiation system and
not in plants receiving an identical UV-B dose at some distance away. This
suggests that some other uncontrolled factor (shading?) was inadvertently
introduced into the experiment. Additional experiments are needed to clarify
this point.
A study conducted by Teramura (1982-1985) examined the effects of UV-B
radiation on seed protein and lipid concentrations of soybean plants grown in
the field at Beltsville, Maryland. A summary of those data are presented in
Table 20 for the six cultivars tested in 1982 and the two cultivars tested in
1983 and 1984. Overall, the effects of UV radiation were relatively small. For
example, seed protein concentrations did not change by more than 5%, and lipids
not more than 13%, over all cultivars and treatments for both years.
Nonetheless, significant UV effects were detected. Seed protein concentrations
declined by as much as 5% during both the 1981 and 1982 growing seasons in
cultivar Essex. Seed lipid concentrations were reduced by 3-5% in cultivar
Forrest in 1982, the only year in which this character was measured in Forrest.
Interestingly, lipid concentrations increased during both years in cultivar
Williams, although this increase was only significant for the 1982 harvest.
Williams is a cultivar whose seed quality and total seed yield (see Table 20)
were positively affected by UV-B enhancements, while Essex is generally
deleteriously affected.
In addition to direct losses in yield (reductions in quantity), increasing
levels of UV-B radiation also may affect yield quality as shown above by several
investigators. The extent of UV-mediated alterations in global yield quality
cannot presently be estimated with any degree of confidence, due simply to the
lack of experimental data for different species. Furthermore, conclusions drawn
from a single growing season may be unreliable due to the interactions
apparently involved between UV-B radiation and other commonly experienced plant
stresses (see Section 2.C, Issues Associated with the Extrapolation of Data from
Controlled Environments into the Field). Nonetheless, evidence collected over
several years show consistent reductions in yield quality in soybean,
suggesting that the risk to yield may be quite high in other crops as well.
3.C. Risks to yield due to possible Increases in disease or pest attack
Six studies that examined the effects of UV-B radiation on the severity of
pests and diseases are summarized in Table 21. Esser (1980) reported that the
number of aphids per bean plant was significantly decreased by UV-B radiation 11
days after their introduction, but there was no significant difference in the
spidermite population 7 days after their application. Although the results
suggest that UV-B radiation can have potentially beneficial effects on pest
control, these conclusions must be judged with caution since the observation
period was less than 2 weeks long. Whether there would be any longer-term
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44
Table 20. Sunmary of Changes in Yield Quality in Soybean Between the 1982 and 1985 Growing Seasons
(Teramura 1982-1985)
Crop
Glycine max
cv Bay
Essex
James
Williams
Forrest
York
Yield
Character
% protein
% lipid
% protein
% lipid
% protein
% lipid
% protein
% lipid
% protein
% lipid
% protein
% lipid
1982
% Change
0 to -5
-1.4 to +3
-3 to -5
-2 to +.5
+.2 to +3
-1 to -2
0 to -.2
+5 to +8
+.5 to +2
-3 to -5
-2 to -3
0 to +3
Signi-
ficance
ns*
ns
P=0.05
ns
ns
ns
ns
P=0.05
ns
P=0.05
ns
ns
1983 Signi- 1984 Signi- 1985 Signi- 1986 Signi-
% Change ficance % Change ficance % Change ficance % Change ficance
+1 to -5 P=0.05 +1 to 0 ns -0.7 to 0 ns 0 to -1 ns
+2 to -2 ns -2 to 0 ns 0 ns 0 to -2 P=0 . 05
+.4 to -.2 ns +3 to +5 P=0.05 -0.5 to -1 P=0.05 -1 to -3 P=0.05
-1 to +6 ns -5 to -10 P=0.05 0 ns 0 to +1 P=0.05
* ns = not significant
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45
Table 21. Summary of UV-B Effects on Plant Pests and Diseases
Pest or Disease
Host Plant
UV-B
Irradiance a/
Conclusion b/
Reference
Aphids (Aphis fabae) bean
Spidermite (Tetranychus uticae) bean
Rust (Uromyces striatus) alfalfa
Scab (Cladosporium cucumerinum) cucumber
Early blight (Alternaria solani) tomato
Leaf spot (Stemphyilium botryosum) alfalfa
Anthracnose (Colletotrichum
lagenarium)
cucumber
Black rot (Mycosphrella melonis) cucumber
Scab (Cladosporium cucumerinum) cucumber
6-25% 0 depl.
3
6-25% 0 depl.
3
55-93 mWm
-2
55-93 mWm
-2
8-112 mWm
-2
55-93 mWm
-2
8-112 mWm
-2
55-93 mWm
-2
8-112 mWm
-2
-2
55-93 mWm
8-112 in Wm
55-93 mWm
-2
-2
8-112 mWm
80-800 Wra
(unweighted)
Esser 1980
Cams et al. 1978
decreased no. by 79-81%
-15 to +3% change (n.s.)
-1 to -2% change in spore
germination (n.s.)
-4 to -11% change in spore
germination (n.s.)
disease severity unaffected
-1 to 2% change in spore
germination (n.s.)
disease severity unaffected
-2 to 2% change in spore
germination (n.s.)
disease severity unaffected
spore germination decreased
33 to 89%
disease severity decreased
with UV-B by 33-66%
spore germination decreased
10-60%
disease severity decreased
spore germination decreased Owens and Krizek 1980
by 10-40%
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46
Table 21. Summary of UV-B Effects on Plant Pests and Diseases (continued)
Pest or Disease
Host Plant
UV-B
Irradiance a/
Conclusion b/
Reference
Rust (Uromyces phaseoli)
Rust (Puccinia coronata)
bean
oats
A.8-20 mHm
-2
4.8-20 mWm
-2
infected leaves decreased
by 61%
infected leaves decreased
by 30-44%
Esser 1980
Powdery mildew (Erysiphe graminis) wheat
-2
4.8-20 mWm infected leaves decreased
by 90-100%
-2
10-20 mWm 99% reduction in conidia Esser (1979)
Leaf rust (Puccinia recondita) wheat
8-16% 0 depl. infection decreased 14-67% Biggs et al. 1984
(n.s.)
Glume blotch (Septoria nodorum) wheat
8-16% 0 depl. infection decreased 12-14%
(n.s.)
Leaf spot (Helminthosporium
sativum)
wheat
8-16% 0 depl. infection decreased 4-6%
(n.s.)
Frog eye spot (Cercospora sp) soybean
8-16% 0 depl. 0-10% change in seed
3
infection (n.s.)
Seed blight (Phomopsis sp)
soybean
8-16% 0 depl. 0-6% change in seed
3
infection
-2
Leaf virus (Potato virus S) Chenopodium quinoa 25-110 mWm 44% decrease in lesion no. Semeniuk and Goth 1980
a/
Weighted with generalized plant action spectrum.
b/ n.s. = not significant
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47
differences in pest attack is yet unknown. Field studies (Esser 1980)
detailing crop growth under enhanced UV-B radiation do not report any
difference in natural pest attack among UV-B treatments.
The severity of some crop diseases has also been studied under laboratory,
greenhouse, and field conditions (Table 21). Studies by Cams et al. (1978)
on in-vitro spore germination of six fungal pathogens showed that hyaline
spores are more sensitive to UV-B radiation than are pigmented spores. Their
tests conducted on plants grown in growth chambers also showed a similar
relationship. Owens and Krizek (1980), however, found that in a pigmented
spore (dados porium cucumerinum), survival was decreased with UV-B radiation.
This was due more to a delay in germ tube emergence than complete inhibition
of growth. Other studies (Esser 1980, Biggs et al. 1984) also indicate that
there is not any clear relationship between spore coloration and UV-B
radiation effectiveness.
Short-term growth chamber studies by Esser (1980) on three leaf fungal
pathogens showed a significant decrease in disease severity with UV-B
radiation (Table 21). In contrast, a field study by Biggs et al. (1984)
showed no significant difference in disease severity on leaves or seeds under
increased UV-B radiation. However, when leaf rust-resistant and rust-
sensitive cultivars of wheat were tested, Biggs et al. (1984) and Biggs (1985)
found that in the sensitive cultivar there were no differences up to 60 days
after planting, while 119 days after planting, disease severity increased with
UV-B radiation. In the resistant cultivar, there were no differences in
disease severity. These results suggest that the effects of UV-B radiation on
plant diseases can vary with pathogen, plant species, and cultivar.
Semeniuk and Goth (1980) found significant UV-B-mediated reductions in
potato virus infection on Chenopodium quinoa. At irradiances over 86 mW m
UV-B (weighted with generalized plant action spectrum), no infection
occurred. In this study, virus extract was exposed to UV-B radiation
immediately upon its application over the leaf surface. Intuitively, viruses
should be highly susceptible to UV-B radiation since they only contain nucleic
acids covered with proteins, both of which have high UV absorption properties.
Furthermore, viroids, which are devoid of a protein coat, may be more
susceptible despite their small size. These effects would probably be
greatest when the virus or viroids are directly exposed to UV-B radiation as
may happen during mechanical transmission. Virus or viroids transmitted
through seed, pollen, insects, mites, nematodes, and fungi may not be as
susceptible to UV-B radiation, due to the additional cellular screening
offered by the host tissues.
One of the plant defense mechanisms that inhibits fungal development is
the production of a class of chemicals known as phytoalexins (Bell 1981).
Uehara (1958) first demonstrated the existence of phytoalexins in soybeans,
and later Klarman and Gerdemann (1963) demonstrated their importance in
disease resistance. Phytoalexin production in plants can be induced
artificially through mechanical injury, high temperature, the application of
fungicides and antibiotics, and by UV-C radiation (Bridge and Klarman 1973,
Reilly 1975). It is suggested that thymine dimers produced after UV-C
absorption by DNA are involved in the synthesis of phytoalexins (Reilly 1975).
UV-B radiation also induces isoflavonoid phytoalexin synthesis (Bakker et al.
1983), thereby possibly having an antifungal affect on plants; however, excess
production can be toxic due to free radical formation (Beggs et al. 1984).
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48
At present it is difficult to forecast the consequences of enhanced UV-B
radiation in terms of pest and disease damage. From the limited information
available, it appears that in some cases UV-B radiation might decrease disease
severity, while in others it might aggravate it. Coupled with reduced vigor
in plants sensitive to UV-B radiation, an increase in disease severity could
pose a considerable risk, resulting in substantial losses in crop yield.
Further studies are obviously needed to develop a better understanding of the
consequences of increased levels of UV-B radiation on pests and plant
diseases.
3.D. Risks to yield due to competition with other plants
The following is a summary of the potential impacts of the interactions
between UV-B radiation and plant competition. A more comprehensive review can
be found in Gold and Caldwell (1983). Plant resistance to a change in an
environmental stress is, in part, a genotypically controlled, species-specific
characteristic (Levitt 1980). An alteration of an environmental stress could
thus lead to a change in the competitive balance of the plant community due to
inherent differences in plant resistance. Many plants have been shown to
exhibit a wide range of sensitivity to enhanced UV-B radiation (for review see
Teramura 1983). Since UV-B radiation can be considered as an environmental
stress, any increase in UV irradiance could, in turn, lead to changes in
competitive ability within plant communities through differential UV-B
resistance of the competing species (Caldwell 1977) . Competition could occur
within the same species (intraspecific) or between different species
(interspecific). Intraspecific competition becomes increasingly important in
monospecific communities such as agricultural systems. On the other hand, in
natural ecosystems with high species diversity, interspecific competition
predominates. In agricultural systems interspecific competition could also be
important between crops and weed species.
Gold and Caldwell (1983) studied intraspecific competition in wheat
(Triticum aestivum L.), wild oats (Avena fatua L.), and goat grass (Aegilops
cylindrica Host) at various planting densities. The study was
conducted in the field at ambient levels of UV-B and those simulating a 16%
ozone reduction (at Logan, Utah, 40° N, based on the generalized plant action
spectrum). There were no significant differences in shoot biomass production
at the various planting densities with enhanced UV-B radiation for all three
species. This indicates that in these species, enhanced levels of UV-B
radiation may be of little consequence in terms of intraspecific plant
competition. Preliminary results (M. M. Caldwell, unpublished data, 1985)
however, indicate that interspecific competition may be affected by enhanced
levels of UV radiation. Enhanced levels of UV-B appeared to alter growth
allocation patterns by inhibition of internode elongation in wild oat but not
in wheat. This was reported to favor wheat in competition for available
light. Whether similar responses occur among other agricultural crops is yet
to be determined.
Solar UV exclusion studies in West Germany by Bruzek (cited in Gold and
Caldwell 1983) with two pairs of naturally competing species show large
differences in response to present levels of ambient solar UV radiation. In a
Fraxinus excelsior/Carpinus betulus species pairing, reduction in shoot
biomass with solar UV radiation was 42-14%, respectively, while in Rumex
obtusifolius/R. alpinus, it was 10% and 24%, respectively. This suggests that
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49
current levels of UV radiation are partly responsible for interspecific
competition among various native plant species.
Very few studies have addressed interspecific competition under enhanced
UV-B radiation. Fox and Caldwell (1978) and Gold and Caldwell (1983) examined
the effects of enhanced UV-B radiation on the competitive interaction of nine
groups of field grown competing pairs from three plant associations:
agricultural crops and associated weeds, montane forage crops, and disturbed
weedy associates. The results are summarized in Table 22.
To measure the competitive ability of one species when grown in mixture
with a second species, relative crowding coefficients (RCC) were used. An RCC
of 1.0 indicates that both species have a similar competitive ability.
Species 1 has a competitive advantage when the RCC is greater than 1.0;
species 2 has the advantage when the RCC is less than 1.0. As shown in Table
22, the RCCs based upon total above ground biomass indicate that there was a
significant shift in the competitive balance in four of the species pairs:
Medicago sativa/Amaranthus retroflexus; Triticum aestivum/Avena fatua;
Triticum aestivum/Aegilops cylindrica; Geum macrophyllum/Poa pratensis.
Amaranthus was more competitive under ambient UV conditions, while Medicago
exhibited the competitive advantage under enhanced UV-B radiation. In
Triticum grown under a simulated 16% ozone reduction, there was no significant
difference in competitive ability with Avena but under a 40% ozone reduction,
Triticum had a competitive advantage over Avena. However, in the previous
year the competitive balance was found to be just the opposite, in favor of
Avena. It was suggested that this difference was due to a late planting,
which resulted in great water and temperature stresses during seedling
development (Gold and Caldwell 1983). Between Triticum and Aegilops the
competitive balance was shifted in favor of Triticum under enhanced UV-B
radiation. Similarly, Geum had the competitive advantage over Poa under
ambient conditions, but under enhanced UV-B radiation, the balance was shifted
in the opposite direction.
Results also show that the extent of dominance can vary with UV-B
irradiance. In the Setaria glauca/Trifolium pratense pairing, Setaria was
dominant both under ambient and enhanced UV-B levels, but under enhanced
levels the degree of dominance was expanded to a much greater extent. On the
other hand, in the Bromus tectorum/Alyssum alyssoides pairing, although Bromus
was dominant under both ambient and enhanced UV-B levels, this dominance was
greatly reduced with enhanced UV-B radiation. These conclusions were all
based on vegetative biomass since results on reproductive biomass, have not
yet been made available. However, Gold and Caldwell (1983) report from
preliminary field data that the competitive ability of wheat, based on seed
biomass, increased relative to wild oats under enhanced UV-B radiation.
Combined, these results clearly demonstrate that enhanced levels of UV-B
radiation can alter the competitive interactions of some species pairs. The
competitive advantage of one species over the other depends upon the species
pairing and the level of UV-B irradiation. Among the agricultural crops
studied, Medicago sativa was more affected while Triticum aestivum was less
affected by weed competition under enhanced UV-B radiation. Since there are a
large number of weeds typically associated with various crop plants, the
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50
Table 22. Relative Crowding Coefficients Based Upon Shoot Biomass
Under Ambient and Enhanced Levels of UV-B Radiation. Enhanced UV-B Was Supplied
Via Filtered (Kodacel TA 401) FS-40 Sunlamps. Data from Gold and Caldwell (1983)
and Fox and Caldwell (1978).
Competing Species Pair
Relative Crowding a/
Coefficient
Simulated Ozone
Plant Association
Agricultural crops
and associated
weed species
Montane forage
species
Disturbed area
weedy associates
Species 1
Alyssum alyssoides
Amaranthus retroflexus
Amaranthus retroflexus
Setaria glauca
Triticum aestivum
Triticum aestiuum
Triticum aestivum
Poa pratensis
Bromus tectorum
Plantago patagonica
Species 2 Depletion (%) b/ Ambient UV
Pisum sativum
Medicago sativa
Allium cepa
Trifolium pratense
Avena fatua
Avena fatua
Aegilops cylindrica
Geum macrophyllum
Alyssum alyssoides
Lepidium perfoliatum
40
40
40
40
16
40
16
40
40
40
0.34
3.56
1.89
2.06
1.08
1.08
0.48
0.85
6.35
0.75
Enhanced UV c/
0.25
0.73*
2.01
18.74
1.28
1.69"
1.57*
2.28*
1.63
0.68
a/ Relative crowding coefficient of 0 means neither species has competitive advantage, more than 1 means species 1
has competitive advantage, less than 1 means species 2 has advantage.
b/ Simulated ozone depletion based upon generalized plant action spectrum (Caldwell 1971), calculated at
Logan, UT (40°N).
c_/ Asterisk denotes a significant difference (P less than 0.05) between control and enhanced UV treatment.
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51
impact of enhanced levels of UV-B radiation upon agricultural systems is quite
complex, but could potentially have serious consequences if weeds have a
competitive advantage over crop plants. Total harvestable yield, as well as
its quality, can be altered by the presence of weeds (Bell and Nalewaja 1968,
McWhorter and Patterson 1980), even in the absence of UV.
Interspecific competition in natural plant communities even under current
ambient UV-B radiation levels has rarely been documented through
experimentation. Results of Caldwell and co-workers indicate that
interspecific competition can be affected by enhanced levels of UV-B
radiation. Thus the relative species composition of many natural plant
communities could possibly change as a consequence of increased levels of UV-B
radiation.
Caldwell (1977) suggested that because of the subtle nature of UV-B
radiation stress, an enhancement of solar UV-B radiation may more likely alter
the competitive balance of plants rather than directly affect ecosystem
primary productivity. The results of Gold and Caldwell (1983) and Fox and
Caldwell (1978) support this hypothesis. Except for the Pisum sativum/
Alyssum alyssoides species pair, total productivity of each species pair was
never significantly affected under enhanced UV-B radiation compared with
ambient-grown controls. In contrast, the results of several field studies
have demonstrated that total harvestable yield may be directly affected by
UV-B radiation in agricultural systems (see Section 3.A, Direct Effects on
Total Yield).
Because of the shifts in competitive balance reported here, increasing
solar UV-B radiation could pose a considerable risk both to agricultural, as
well as to natural, ecosystems. In agricultural systems, any shift toward
increasing weed competitiveness would inevitably be detrimental in an economic
sense, resulting in the need to increase tilling and/or herbicide application.
Without such measures, an increase in weed occurrence may result in reductions
in actual harvestable crop yields, a lowering in crop quality, or an
alteration in disease or pest sensitivity. The apparent interactions of
competitive balance with other commonly experienced environmental stresses,
such as water and temperature stress, make it difficult to ascertain even the
magnitude of the risk. Clearly, more experimental data is needed in this
area.
Changes in the competitive balance of native species could also have
profound effects on the structure and function of natural ecosystems.
Presumably, the more UV-B-tolerant species would proliferate at the expense of
the sensitive ones. Even very subtle differences in sensitivity could result
in large changes in species composition over time and possibly affect
ecosystem function. Again, because of the total lack of experimental
evidence, the uncertainty is high; however, in light of the importance of this
question, the risks are considerable.
3.E. Risks to yield due to changes in pollination and flowering
It would seem that the reproductive tissues of plants whose pollination
and subsequent fertilization take place during the day with flowers fully open
would receive an appreciable UV-B dose. However, ovules enclosed in the ovary
are well protected against UV-B radiation, and, therefore, female reproductive
structures would not likely be affected. Flint and Caldwell (1983) have shown
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52
in six plant species that the anther wall filters out over 98% of the incident
UV-B radiation. Therefore, before anther dehiscence, pollen is also well
protected. In-vitro experiments with pollen from numerous species demonstrate
that UV-B radiation can inhibit pollen germination (Table 23). Sensitivity
varies among species but even relatively low levels of UV-B radiation can
inhibit germination in-vitro. Supported by other published results, Flint and
Caldwell (1984) speculate that pollen shed in the binucleate condition would
be more susceptible to UV-B radiation damage than pollen shed in the
trinucleate condition. This speculation is based on the knowledge that the
time course of germination and penetration of the stigma is more rapid in
trinucleate species, and, thus, these would be less exposed to a UV-B
radiation environment. Whether inhibition of pollen germination does occur
under in-vivo conditions is yet to be determined.
In nine plant species, Southworth (1969) found UV-absorbing compounds in
the wall of pollen, with a maximum absorbance in the UV-B range. The proposed
role of pollen pigments also includes screening from UV radiation (Stanley and
Linskens 1974). Furthermore, studies on the UV absorption profiles of
stigmatic surfaces and exudates of many species show one or more peaks in the
UV-B region (Martin 1970, Martin and Brewbaker 1971). Therefore, under
natural conditions, the effectiveness of UV-B may be minimal because of
UV-absorbing pigments in the anther and pollen walls. Upon deposition over
the stigmatic surface, pollen would further be protected from UV-B radiation
if the surface has exudates, since these often contain UV-absorbing compounds.
On dry stigmatic surfaces, UV-B radiation may still have only minor effects,
especially in trinucleate pollen because of the short time between germination
and penetration. Furthermore, pollen absorption by the stigmatic surface also
reduces its exposure. Although no direct experimental evidence is available
to support or refute the hypothesis proposed by Flint and Caldwell (1984),
results from various field experiments do not substantiate a meaningful change
in grain yield or seed set under enhanced UV-B radiation.
Flint and Caldwell (1984) reported that maximum levels of solar UV-B
radiation found in temperate latitudes were insufficient to inhibit pollen
germination in-vitro, but that the two- to three-fold greater UV-B irradiance
incident at high elevation, low latitude environments is effective in
partially inhibiting germination in three of the four species they examined.
This raises the question, then, whether pollen from tropical or subtropical
species respond similarly or whether it is inherently more resistant to the
greater, naturally occurring levels of UV-B radiation. Currently, no
experimental evidence exists to help resolve this question. Overall, it
appears that pollination at temperate latitudes may be little affected by the
present projections for increases in solar UV radiation. However, there is
considerable uncertainty with regard to risks to yield due to UV-mediated
changes in pollination in tropical highlands. Intuitively, one might
anticipate evolutionary adaptations which would protect the pollen of tropical
species from the proportionally greater UV doses received in such
environments. Despite its potential importance, however, the void of
information available makes it impossible to assess this question fully at the
present.
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53
Table 23. Summary of UV-B Effect on In-Vitro Pollen Germination
Species
Petunia hybrida
Vicia villosa
Tradenscantia Clone 4430
Tradenscantia Clone 4430
Clone 02
Brassica oleracea
Cleome lutea
Papaver sp
Papaver rhoeas
Cleome lutea
Geramium viscosissiura
Scrophularia peregrina
Irradiance*
mWta UV-B
BE
67
67
67
67
67
54
56
56
35
60
68
137
170
40
60
73
73
Duration
(hours)
1.0
1.0
1.0
1.5
1.5
2.5
3.5
3.5
3.0
3.0
2.0
3.0
3.0
3.0
3.3
3.0
3.0
Germination
Inhibition
(X)
65
65
23
44
12
28
28
41
3
35
26
52
52
2
33
20
53
Reference
Campbell et al. (1975)
Chang and Campbell (1976)
Caldwell et al. (1979)
Flint and Caldwell (1984)
* Biologically effective UV-B weighted according to the plant effective action spectrum (Caldwell et al., 1979)
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54
During the early part of this century numerous studies on the effects of
solar UV radiation were conducted using window glass to filter out UV
radiation (see reviews by Popp and Brown 1936; Caldwell 1971). The results
from these studies indicated an inhibition of flowering by solar ultraviolet
radiation. However, these experiments were generally executed with
insufficient sample sizes and failed to isolate ultraviolet irradiation as the
single contributing factor causing the difference in flowering. For instance,
Caldwell (1968) has shown that leaf temperatures under window glass are
markedly higher than under screen filters. Such changes in temperature alone
are generally sufficient to alter the induction of flowering (Zeevaart 1976) .
A summary of results from recent experiments under similar microclimatic
conditions is presented in Table 24. Results of Kasperbauer and Loomis (1965)
studying Melilotus and Caldwell (1968) with Trifolium dasyphyllum show an
increase in flowering with the exclusion of solar ultraviolet radiation using
greenhouse glass or Mylar filters. A growth chamber study by Klein et al.
(1965) incorporating primarily UV-A radiation also shows an increase in the
number of flowers produced in marigold by the exclusion of ultraviolet
radiation. Similarly, greenhouse trials on beans and peas also show an
inhibition of flowering and decrease in flower number due to UV-B radiation
(Biggs and Basiouny 1975).
However, field studies providing enhanced levels of ultraviolet radiation
using unfiltered sunlamps (which emit both UV-B and UV-C), produce no
significant effects on flower number or date of flowering in marigold and
tomatoes, tasseling in maize, or heading in sorghum (Hart et al. 1975). Biggs
and Kossuth (1978), on the other hand, found an increase in flower number in
potatoes at peak flowering in UV-B irradiated plants. However, the duration
of flowering was longer under ambient levels of UV-B irradiance. In contrast,
the number of flowers was significantly reduced in tomatoes after UV-B
irradiation. Although these various observations apparently suggest changes
in flowering which correlate with ultraviolet radiation, whether this would
lead to an appreciable affect in harvestable yield has not been fully
investigated. Biggs and Kossuth (1978) found a stimulation of flowering and
an increase in tuber weight (grade A large) in potatoes with UV-B radiation,
while UV-B induced inhibition of flowering in tomatoes resulted in reductions
in fruit weight of 11 different maturity classes.
These results demonstrate that UV-B radiation can have both inhibitory and
stimulatory effects on flowering, depending on the plant species, growth
conditions and other factors. Whether UV-B radiation directly influences
flowering events or plays an indirect role through changes in photosynthate
reserves is not yet known. Presently, no clear trends emerge on the effects
of UV-B radiation on flowering. Therefore, there is a high degree of
uncertainty concerning the risk to yield due to a change in the timing of
flowering. This uncertainty is primarily due to the paucity of experimental
evidence available at this time. Whether alterations in flowering will lead
to changes in harvestable yield still awaits further experimentation.
3.F Risks to yield due to structural plant changes affecting harvestability
At present, no experimental study has directly addressed the question
whether enhanced levels of UV-B radiation will alter the harvestability of
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55
Table 24. Summary of UV Effects on Flowering
Growth Irradiation
Plant Species Condition a/ System
Melilotus G.H. unfiltered G.E.
sunlamp and glass
filtered
G.H.&F none in G.H.
ambient in F
inf lo . no
Conclusions
. declined under
unfiltered, but increased under
glass
flowered
decreased
all season in G.H. ,
with season in field
Reference
Kasperbauer and
Loomis (1965)
Kasperbauer and
Loomis (1965)
Tnfolium dasyphyllum F
Kobresia myosuriodes
Petunia
Zea mays
Sorghum bicolor
ambient filtered
with Mylar or
Polyvinyl fluoride
Carex rupestris
Geum rossii
Oreoxis alpina
Tagetes
F
F
F
G.C.
same
same
same
unfiltered black
light b/
unfiltered FS-40
increased flowering under Mylar Caldwell (1968)
no sign, diff, but a trend of
increased flowering under Mylar
flowering under Mylar
exclusion of UV increased no.
flower buds by 80X addition of
UV increased no. flowers by 12X
no sign, effect
no sign, effect
no effect on tasseling
no effect on heading
Klein et al. (1965)
Hart et al. (1975)
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56
Table 24. Summary of UV Effects on Flowering (continued)
Plant Species
Growth
Condition a/
Irradiation
System
Conclusions
Reference
Fhaseolus vulgaris G.C.
Pisum sativus
Solanum tuberosum
G.C.
Mylar and CA
filtered FS-40
UV delayed flowering, no. and
size of flowers
Biggs and Basiouny
(1975)
UV decreased flowering duration Biggs and Kossuth
increased no. open flowers at (1978)
peak flowering
Lycopersicon esculentum F
Glycine max
G.H.
Mylar and CA
filtered FS-40
UV decreased no. flowers on a
single sample date
no difference
Murali and
Teramura
(unpublished)
&/ GH = greenhouse, GC = growth chamber, F = field.
b/ 70X of radiation was between 355-380 nm (UV-A).
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57
field crops. However, from morphometric changes reported in the literature,
some speculations could be made. These speculations warrant caution because
they represent only potential and not actual circumstances.
Crop harvestability is dependent upon crop architecture, time, and mode of
harvesting. Crop architecture can be broadly grouped into 1) row type (e.g.,
cereals), 2) bushy (e.g., beans and tomatoes), and 3) trees. Crops are
harvested either during final maturity as in cereals and legumes or at regular
intervals as in alfalfa or other forage crops or fruits. Harvesting can be
performed either manually or mechanically, or both. Changes in the
harvestability of five crops are reported here as representative of potential
scenarios.
Case 1. cereals (row crop). Harvestability of cereal crops, either
mechanically or manually, depends upon the occurrence and extent of lodging.
Losses would be heavy if there is a high degree of lodging, especially when
harvested mechanically since no efficient mechanism for lifting plants without
shattering grains has been developed. Most modern cultivars are highly
resistant to lodging because of short and sturdy culms. However, under high
sowing densities or excessive nitrogen supply, coupled with ample soil
moisture, these cultivars tend to grow taller and occasionally lodge severely
during storms. Furthermore, culms can break in strong winds resulting in
goosenecking of panicles. Enhanced levels of UV-B radiation generally reduces
plant height in cereals (Table 25). Such an effect would have a positive
effect on the harvestability of cereals by decreasing their susceptibility to
lodging.
Case 2. tomatoes (bushy crop). Tomatoes are grown either for fresh market
or processing. The former is mainly of indeterminate and the latter of
determinate type. In indeterminate tomatoes, plants are pruned to remove the
lateral buds/branches and staked because of their viney nature. These are
highly labor-intensive operations. Hart et al. (1975) reported an inhibition
of branching with no reduction in fruit number or size due to enhanced UV-B
irradiance in field-grown tomatoes (cultivar Fire ball). This suggests that
increasing UV-B levels could potentially have a favorable effect on tomato
culture by minimizing the labor requirement for pruning. Presently, it is not
known whether pruning or UV-induced inhibition of lateral branching will
result in greater yields due to reallocation of resources to the main stem.
Larger fruits may possibly be produced by the removal of lateral branches due
to the diversion of photosynthate. Another advantage of UV-induced inhibition
of lateral branching concerns the earliness of ripening. For instance, it is
known that with fewer branches, ripening occurs earlier in indeterminate
types. Thus, early-season market requirements can be met by the reduction of
branching. An increase in UV-B radiation could also favor a longer period of
staggered production due to early ripening and thus an improved distribution
of fruit for harvesting. At higher latitudes, where the growing season is
shorter, earliness in ripening can be an advantage to a grower.
Tomatoes grown for processing are primarily of the determinate type.
Because of their uniform ripening they can be mechanically harvested. In
mechanical harvesting, one of the prerequisite characteristics is the ease of
separation of fruits from stems and leaves. Fruits can be generally separated
more easily when there are fewer branches, ceteris paribus. Thus, UV-mediated
inhibition of branching could also increase mechanical harvestability of
tomatoes.
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Table 25. Summary of UV-B Effects on Plant Height of Cereals
Crop Growth Condition
Sweet corn (Zea mays) Field
Sorghum (Sorghum vulgare)
Sweet corn (Zea mays) Greenhouse
Wheat (Triticum aestivum) Growth Chamber
Barley (Hordeum vulgare) Growth Chamber
Com (Zea mays) Growth Chamber
Millet (Pennisetum glaucum) Growth Chamber
Oats (Avena sativa) Growth Chamber
Rice (Oryza sativa) Growth Chamber
Rye (Secale cereale) Growth Chamber
Corn (Zea mays) Field
Barley (Hordeum vulgare) Growth Chamber
Wheat (Triticum aestivum) Growth Chamber
UV-B Irradiance
1.0-1.7 UV-B
Beltsville Sun
Equivalents
Unfiltered FS-40
Sunlamps
-2
131-225 mWm
UV-B (plant)
BE
0.5 to 2.0 UV-B
Sun Equivalents
0.5 to 2.0 UV-B
Sun Equivalents
0.5 to 2.0 UV-B
Sun Equivalents
0.5 to 2.0 UV-B
Sun Equivalents
0.5 to 2.0 UV-B
Sun Equivalents
0.5 to 2.0 UV-B
Sun Equivalents
0.5 to 2.0 UV-B
Sun Equivalents
8-16% 0 red.
1060-1760
-2 -1
Jm -day
UVB (Plant)
BE
1060-1760
-2 -1
Jm -day
UVB (Plant)
BE
% Relative Change
in Plant Height References
+14 to -3 Ambler et al. (1978)
- 1 to +3 Ambler et al. (1978)
-15 to -22 Allen et al. (1977)
-5 to -22 Biggs and Kossuth (1978)
-14 to -22 Biggs and Kossuth (1978)
-14 to -28 Biggs and Kossuth (1978)
-13 to -20 Biggs and Kossuth (1978)
-9 Biggs and Kossuth (1978)
-4 to -13 Biggs and Kossuth (1978)
-21 Biggs and Kossuth (1978)
+1 to +5 Biggs et al. (1984)
-1 to -12 Dumpert (1983)
-1 to -2 Dumpert (1983)
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Case 3. cotton (bushy crop). Grading the quality of cotton harvested
mechanically or manually depends on the degree of contamination, especially
from dried leaves. Although defoliants are used before mechanical picking,
the extent of leafiness still can have a direct bearing upon harvestability.
Intuitively, the more leafy the crop, the greater the probability of
contamination. Biggs and Kossuth (1978) found a significant increase (9 to
16%) in leaf area produced under enhanced levels of UV-B radiation in cotton
(Gossipium hirsutum). Unfortunately, they did not evaluate cotton yield or
quality to determine whether the increase in leafiness had any deleterious
effects.
Case 4. tobacco (bushy crop). The mechanical harvesters presently
designed and used for tobacco are more effective in cultivars with leaves
oriented in an upright fashion. Since larger leaves tend to droop, cultivars
with smaller leaves are better suited for mechanical harvesting. To date,
there are no experimental data on morphological changes arising from enhanced
levels of UV-B radiation in tobacco. However, studies conducted with numerous
crop plants show a general reduction in leaf area (Teramura 1983). On the
other hand, an increase in leaf area as found in cotton (Biggs and Kossuth
1978), could pose some difficulty for mechanical harvesting.
Case 5. fruits (tree crop). Phytohormones such as ABA and ethylene
regulate fruit abscission. Biggs and Kossuth (1978) reported an increase in
both ABA and ethylene with enhanced levels of UV-B radiation in bean plants.
Currently, it is not known whether such a response is general in nature and
elicited in tree fruits. If so, there is the possibility that fruit may be
abscissed prior to reaching maturity, resulting in considerable economic
losses.
4. SUMMARY AND CONCLUSIONS
Global UV-B radiation varies diurnally and seasonally because of changes
in solar angle, stratospheric ozone concentration, degree of cloud cover, etc.
Presently, most investigators evaluate the effects of UV-B radiation using a
constant UV-B supplied via simple lamp systems without considering these
temporal changes in UV-B irradiation. This results in an oversupplementation
of UV during periods of low solar angle (morning and afternoons) and during
overcast skies.
The effects of UV-B radiation in producing a plant response is highly
wavelength dependent. In evaluating the effectiveness of UV-B'radiation, more
than 10 action spectra have been developed and used by various investigators.
Since these action spectra vary tremendously many of the experimental data
from various UV-B studies are not directly comparable. Thus, a realistic
action spectrum developed under more natural conditions must be developed and
used in all future experiments.
There are 10 major terrestrial plant ecosystems in the world and these
include 314 plant families. The effects of enhanced levels of UV-B have been
studied in only four of these ecosystems and in only 6% of the plant families.
UV effects have been examined in only about a third of the plant growth forms
and in many, such as vines, epiphytes, small woody shrubs, etc., virtually no
data exists. Most of our knowledge of UV effects is derived from studies
focused upon agricultural crops, yet crop yield has been evaluated in only 22
species from 7 plant families. Overall, very little information is available
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on the effectiveness of UV-B radiation on other economically important plants
such as trees and forage grasslands and especially on native plant species.
To adequately address the question of what potential impacts enhanced levels
of UV-B radiation will have on global terrestrial plant communities and
ecosystems, many unrealitic assumptions must be made. For example, to assess
the potential impacts on forest communities, we must assume that perennial
woody trees and shrubs respond similarly to annual agricultural crops.
Clearly more data would be needed before any attempt for realistic projections
on a global scale could be made.
Plant responses to increased levels of UV-B radiation vary markedly both
among (interspecific) and within (intraspecific) plant species. At present,
the bases for these inherent differences have not yet been well documented.
There are three general categories cf UV-protective mechanisms which may be
involved in producing this variation in responses. The first includes repair
mechanisms, such as photoreactivation, which is an enzyme mediated,
light-activated process. Although not specifically demonstrated in plant
tissues, various experimental results suggests it is a widespread phenomenon.
Excision repair is the process whereby potentially deleterious photoproducts
of UV absorption are removed and replaced by new, correct DNA sequences. This
is clearly demonstrated and is a widespread phenomenon in plants.
Postreplication repair involves the replication and combination of intact DNA
strands over damaged ones, but is yet unknown in plant tissues.
The second category of protective mechanisms are those that tend to
minimize the damaging effects of UV-B radiation. Probably the most important
of these is growth delay, which allows time for other repair mechanisms to
correct the damage. The last category involves those which effectively reduce
the amount of UV-B radiation reaching sensitive targets. The most widespread
mechanism in plants is probably the selective absorption by UV-absorbing
pigments such as flavonoids in outer tissue layers. Some studies show that
despite a large increase in flavonoids, the photosynthetic machinery is still
adversely affected by UV-B radiation. Therefore the inherent inter- and
intraspecific differences in UV-B sensitivity are probably the product of a
number of natural UV protective mechanisms acting in concert within the plant.
More information is critical to refine our understanding of natural plant
protective mechanisms which may potentially help compensate damage arising due
to the anticipated increase in solar UV-B radiation.
Large intraspecific differences in UV-B sensitivity have been reported,
which are not merely the result of gross morphological or physiological
differences, as might commonly occur interspecifically. Crop breeding could
be used as a tool to minimize the deleterious effects of UV-B radiation if a
thorough understanding of the genetic bases for these differences were
understood. Despite the evidence of UV-tolerant cultivars supporting the
notion that crop breeding may limit the deleterious impacts of enhanced solar
UV-B radiation, a large degree of uncertainty still remains in the absence of
any information on the genetic bases for these differences.
Much of our understanding of the effects of UV-B radiation on plants is
derived from studies conducted under artificial growth conditions (growth
chamber or greenhouse) which neither quantitatively nor qualitatively resemble
field conditions. Of utmost concern is that plants are apparently more
sensitive to a given UV-B dose in artificial growth conditions compared with
field conditions. The theoretical basis for increased susceptibility is that
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under artificial conditions only a single factor is generally manipulated,
while all other factors are kept constant or optimized for growth. Under
field conditions, however, plants typically experience multiple stresses
(water, nutrients, etc.) simultaneously. Few studies have examined the
interaction between other commonly experienced stresses and UV-B radiation.
Both water and nutrient stresses apparently increase plant tolerance to UV-B
radiation by stimulating the production of UV screening chemicals. Artificial
growth environments can provide valuable information on the interaction
between UV-B radiation and other environmental factors; however, they cannot
be used in place of actual field validation studies where a host of complex
natural interactions occur. It is concluded that when extrapolations from
controlled environments are made into the field, they must be done so with
extreme caution. At best, general trends may be implied, but specific or
quantitative extrapolations do not yet seem plausible.
Atmospheric CO- concentration has been steadily increasing over the
centuries, but at an alarmingly faster rate during the past two decades. To
date, no information is available on the effects of UV-B radiation under
increased atmospheric CO concentrations; however, some speculations could be
made. In general, enhanced levels of UV-B radiation has a negative effect,
while CO- has a positive effect, on the growth and development of plants.
Since the positive effects of CO- are generally greater than the negative
effects produced by UV-B irradiation, the combination of these two
environmental changes might lead to a compensation of some of the deleterious,
direct effects of UV-B radiation. Therefore, more subtle, indirect effects
may be those most critically affected. Both UV-B and CO- have been shown to
alter the competitive balance among various plant associations. Changes in
competitive balance, especially in agricultural systems between crops and
weeds could produce subtle, yet economically catastrophic changes. Shifts in
competitive ability among native species could lead to changes in community
composition and structure, with ultimate large-scale ecosystem modifications.
Considering the lack of any experimental data on the actual interaction
between UV-B and CO there is a high degree of uncertainty in the assessment
of the possible global effects of enhanced levels of UV-B radiation in an
elevated CO- atmosphere.
In all of the industrialized countries in the world, ground-level air
pollution (oxides of nitrogen, sulphur dioxide, fluoride, and ozone) is
rapidly increasing. In many cases these pollutants have already had
detrimental effects on plant productivity. At present, no experimental data
are available on the interactions between UV-B radiation and these various
other air pollutants. However, since most air pollutants have deleterious
effects on plants, it is anticipated that the effects of UV-B would be
additive.
Only a handful of field studies have examined the effects of UV-B
radiation on crop yield. Despite a broad range of experimental protocols and
dosimetry, in nearly half of the plant species examined, UV-B radiation
produced a deleterious effect on yield. Although reductions in yield were
reported for some crops, this result should be evaluated with caution since
most studies lasted for only a single growing season. Field studies conducted
over several years show large annual variation in response. Only two studies
have evaluated the effects of UV-B radiation on the quality of crop yield, and
both reported reductions. Overall, UV-B radiation deleteriously affects both
the quantity and quality of crop yield, but the magnitude of the effect is
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highly variable from one year to another. Longer-term field studies are
essential for realistic assessments of the impact of increased levels of solar
UV-B radiation on the quantity and quality of global crop productivity.
Crop yield is also affected by factors such as the occurrence of pests and
diseases, weeds, problems associated with pollination, etc. Several studies
have specifically examined the effects of UV-B radiation on the severity of
pest and disease incidence. Although some of these results suggest that UV-B
can have potentially beneficial effects on pest control, these must be
interpreted cautiously since the observation period was very short. The
effects of UV-B radiation on plant diseases was equivocal, varying with
pathogen, plant species, and cultivar. One study reported that UV-B radiation
significantly reduced virus infection transmitted mechanically. However,
virus or viroids transmitted through seeds, pollen, insects, or nematodes may
not be as susceptible to UV-B radiation due to the additional cellular
screening offered by the host tissue. UV-B radiation may further reduce yield
by increasing the incidence of pests and diseases, or in other instances
potentially have beneficial effects on pest and disease control. Lack of
sufficient information leads to a high degree of uncertainty in the projection
of the impact of enhanced solar UV-B radiation on pest and diseases.
Numerous agricultural and native plant species are differentially affected
by UV-B radiation, which could ultimately lead to changes in the competitive
balance within plant communities. In agricultural situations, there may be a
shift in the competitive ability of weeds, resulting in the need for increased
production costs (tillage, herbicides, etc.). Without such measures, an
increase in weed competition would reduce the quantity and quality of yield.
Once more, the lack of experimental evidence precludes more detailed
assessment.
In-vitro experiments with pollen from numerous species show that even
relatively low levels of UV-B radiation can inhibit pollen germination.
However, whether a similar response occurs in-vivo has yet to be determined.
Both the pollen wall and stigmatic surfaces have UV-absorbing pigments, thus
under natural conditions the effectiveness of UV-B may be minimized.
Observations from various field experiments do not indicate any substantial
change in the seed set which would support this notion. Therefore, it appears
that the projected increase in UV-B radiation may not affect pollination.
Only two field studies have investigated the effects of UV-B radiation on
flowering. Based upon this limited information, UV-B may affect flowering in
some plants, but possibly without any affect on yield. However, the absence
of conclusive information makes it impossible to further assess the impact of
UV-B radiation on pollination and flowering.
No experimental information is available on UV-induced structural changes
which might affect the harvestability of field crops. However, on the basis
of reported morphometric changes, some speculations were made on five crops.
UV-B radiation may potentially have a beneficial effect by reducing the labor
cost for pruning in some crops and stimulate ripening for early season market.
UV-B radiation has been shown to increase leaf area in cotton, which may
reduce cotton quality because of higher levels of contamination from dry
leaves. In cereals, UV-B reduces internode length and thus the height of the
plant. This may have a positive effect on the harvestability of cereals by
decreasing their susceptibility to lodging. UV-B may also increase mechanical
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harvesting efficiency in some crops by decreasing leaf area. It is reported
that UV-B radiation increases both ABA and ethylene production in some plants.
Since phytohormones regulate fruit abscission, UV-B radiation may result in
considerable economic losses by abscissing fruit prior to maturity. Overall,
it appears that increased levels of UV-B may be beneficial to the
harvestability of some crops, while others might be negatively affected.
5. RECOMMENDATIONS
A plethora of experimental approaches, equipment and dosimetry have been
utilized in the numerous studies presented in various earlier sections. One
major consequence of such experimental diversity is the difficulty in
interpreting data for comparative purposes. In a worst-case example, consider
the field studies conducted with unfiltered fluorescent sunlamps that emit
short wavelength UV-C radiation. Caldwell (1977) calculated that even in the
unlikely event of a catastrophic 907, stratospheric ozone depletion, almost no
energy would be emitted at wavelengths shorter than 280 nm (in the UV-C
waveband). Furthermore, evidence suggests that the effects of the UV-C
waveband may differ both quantitatively and qualitatively from effects of UV-B
radiation (Nachtwey 1975). Since unfiltered lamps emit energy both in UV-C
and UV-B wavelengths, such studies have virtually no utility in estimating the
potential impacts of increasing solar UV-B radiation reaching the earth's
surface. To have any ecological relevance, UV lamps must be filtered to
remove the UV-C component.
The most common UV sources used for plant effects research are the Philips
TL 40/12 fluorescent sunlamps filtered with Schott cut-off absorption filters
(WG series), used primarily by European investigators, and the Westinghouse
FS-40 fluorescent sunlamp filtered with cellulose acetate plastic films used
exclusively by U.S. investigators. The Philips lamps have a considerably
greater UV emittance than the Westinghouse ones, and the two filtered lamp
systems differ in spectral energy distribution (Caldwell et al. 1984).
Therefore, it is crucial that the same weighting functions be used when
comparing experiments using different UV irradiation systems. As the
difference between spectral distributions increases (for example when
comparing high- and low-pressure mercury vapor lamps) the choice of the action
spectrum becomes more critical (see Appendix A, Action Spectra and their Key
Role in Assessing Biological Consequences of Solar UV-B Radiation Change).
Since FS-40 lamp output decreases rapidly (20%) during the first 100 hours of
use, it is recommended that lamps be pre-aged prior to use (Teramura et al.
1980).
The UV-B irradiation emitted along the length of a fluorescent tube varies
greatly. Maximum emittance occurs in the middle third of the lamp and this
diminishes rapidly near the ends, where emittance may be only 50% of maximum.
This can be graphically seen in Figure 4 showing the normalized irradiance
0.5 m beneath a Westinghouse FS-40 lamp array. The array consisted of six
parallel lamps (shown by arrows), and measurements were made each 10 cm in a
2.3 square meter area directly beneath the lamps. Plants grown in the middle
0.6 m^ of such an array receive a relatively uniform irradiance which varies
by less than 10%. Therefore, it is recommended that lamps be oriented
perpendicular to experimental plant rows, rather than in an end-to-end
fashion. Although an end-to-end orientation is much more economical, plants
beneath such an irradiation system would receive a highly variable UV dose,
ultimately producing an appreciable degree of experimental error (in a
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25 30 34 39 41 45 45 45 48 45 45 45 45 43 41 39 36 32 23
30 36 43 52 55 59 61 59 64 64 61 59 59 57 55 50 48 41 34
36 48 55 61 68 61 73 68 77 77 75 61 73 57 66 64 57 48 41
43 52 61 70 77 80 84 84 86 86 86 84 82 80 75 70 64 57 45
45 59 68 77 84 89 91 93 93 93 91 91 91 39 82 77 68 59 48
48 59 70 80 89 91 95 98 100 98 98 95 93 89 86 77 73 61 50
52 59 70 80 89 93 95 98 100 100 98 98 93 93 86 80 73 61 50
48 59 68 75 86 91 93 95 98 95 95 93 91 89 82 80 68 59 50
43 55 64 70 80 84 89 91 91 89 89 89 89 82 77 73 64 57 45
36 48 57 61 68 73 30 82 80 77 55 77 77 73 68 64 57 50 41
27 39 45 50 57 61 61 64 66 66 64 64 61 57 55 52 45 41 32
18 27 34 36 41 45 48 48 50 48 48 45 45 45 41 39 32 30 23
Fig. 4 Normalized irradiance 0.50m beneath a single UV-B lamp array.
Measurements were made each 100 cm2 with lamps positioned at 0.30m
centers (actual lamp position indicated by arrows).
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statistical sense). It is likely that the larger error associated with such a
variable dose could mask some of the subtle UV-B radiation effects, and
therefore not be a reliable test.
The level of visible radiation supplied during growth has profound effects
on plant sensitivity to UV-B radiation (see Section 2.C, Issues Associated
with the Extrapolation of Data from Controlled Environments into the Field).
Therefore, caution must be exercised in controlled environment studies to
maintain an adequate level of visible radiation. Since leaf anatomy and
photosynthetic characteristics have been shown to be related to the daily
integrated levels of visible radiation (Chabot et al. 1979, Nobel and Hartsock
1981), it is recommended that the daily dose of visible radiation be in an
ecologically realistic range wherever possible.
In nearly all field experiments, supplemental UV-B radiation is provided
as a squarewave, simply by turning lamps on or off with the use of timers.
Natural solar UV irradiance, in contrast, gradually increases on a daily basis
with a peak at solar noon that coincides with peak visible irradiances.
Therefore under artificial lamps producing a squarewave function,
proportionately more UV is provided during the periods of low solar altitudes
(mornings and late afternoons) compared with natural solar UV. This results
in a greater simulated ozone reduction during these periods. Of even greater
concern, however, is that such a squarewave is generally supplied during
cloudy and overcast skies, when the levels of ambient UV may be less than 50%
of clear sky irradiances due to the absence of the direct beam component.
During these periods, the lamps would supply a UV dose equivalent to a much
greater ozone depletion than originally intended when the lamps were
calibrated for clear sky conditions. More realistic field validations of
anticipated ozone depletion may be made using a modulated lamp system as
described by Caldwell et al. (1983b). Such a system would reduce the errors
cited above by providing UV as a sinewave during clear sky conditions and
modulate lamp output during cloudy or overcast skies. A further advantage in
a modulated system would be a reduction in the frequency of filter changes
necessary (currently once every 4-7 days for most investigators) since the
system would correct for filter solarization. The disadvantage with such a
system is the additional project cost. Estimates for building a modulated
system range between $1,000 to $1,500 per unit (Caldwell personal
communication), and one unit would be necessary to control an array of six
lamps. In the field study conducted by Teramura (1981), 60 such modulated
systems would be necessary. Despite the additional expense, such a refinement
could greatly improve the field simulation and sensitivity of ongoing and
future field validation studies. In light of the great risks posed to global
crop yield and quality loss resulting from a projected increase in UV-B
radiation reaching the earth's surface, such an investment seems well
warranted and therefore highly recommended.
Instrumentation to measure UV-B radiation has essentially evolved along
with project needs during the past decade. The current spectroradiometer used
by U.S. scientists involved in plant effects research is the Optronics
(Orlando, Florida) Model 742, with a double monochrometer and dual halographic
grating specifically designed to measure the UV spectral irradiance of
sunlight. Although this instrument is excellent in laboratory situations, it
is not ideally suited for field measurement. Several investigators have made
some extensive modifications which have greatly improved its ability to
function in the field. For instance, Caldwell (personal communication) has
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66
installed a Peltier cooling device to keep the photomultiplier tube at a
uniform temperature, enabling the spectroradiometer to operate in a
temperature range typically found in the field (30-40°C) . It is recommended
that this equipment modification as well as others be made (perhaps in
conjunction with Optronics) to improve the reliability of our field
measurements.
The recommendations made above are suggestions which will help improve
field experimental design and measurement and help limit extraneous variations
which may mask any true UV-induced biological effects. More importantly,
however, an adoption of standardized protocols and dosimetry will greatly aid
in the interpretation and intercomparison of field collected data and provide
a reliable basis from which to assess the potential impacts of stratospheric
ozone depletion.
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6. LITERATURE CITED
Allen, L.H. Jr., C.V. Vu, R.H. Berg III and L.A. Garrard, 1977. Impact of
solar UV-B radiation on crops and crop canopies. Final Report, UV-B
Biological and Climatic Effects Research (BACER), EPA, Washington, B.C.
Ambler, J.E., R.A. Rowland and N.K. Maher, 1978. Response of selected
vegetable and agronomic crops to increased UV-B irradiation under field
conditions. UV-B Biological and Climatic Effects Research (BACER), Final
Report EPA-IAG-D6-0168, EPA, Washington, D.C.
Antonovics, J., 1975. Predicting evolutionary response of natural populations
to increased UV radiation. In Climatic Impact Assessment Program (CIAP),
Monograph 5 (Nachtwey, D.S., Caldwell, M.M. and Biggs, R.H., eds.), pp.
8-7 - 8-27. U.S. Dept. Transport, Report No. DOT-TST-75-55, National
Techn. Infor. Serv., Springfield, Virginia.
Bakker, J., F.J. Grommers, L. Smits, A. Fuchs and F.W. de Vries, 1983.
Photoactivation of isoflavonoid phytoalexins: Involvement of free
radicals. Photochem. Photobiol. 38:323-329.
Bartholic, J.F., Halsey, L.H. and L.A. Garrard, 1975. Field trials with
filters to test for effects of UV radiation on agricultural productivity.
In Climatic Impact Assessment Program (CIAP), Monograph 5 (Nachtwey, D.S.,
Caldwell, M.M. and Biggs, R.H., eds.), pp. 61-71. U.S. Department of
Transportation, Report No. DOT-TST-75-55, National Techn. Infor. Serv.,
Springfield, Virginia.
Becwar, M.R., F.D. Moore III and M.J. Burke, 1982. Effects of deletion and
enhancement of ultraviolet-B (280-315 nm) radiation on plants grown at
3000 m elevation. J. Amer. Soc. Hort. Sci. 107:771-779.
Beggs, C.J., U. Schneider-Ziebert and E. Wellmann, 1986. UV-B radiation and
adaptive mechanisms in plants. In Stratospheric Ozone Reduction, Solar
Ultraviolet Radiation and Plant Life (R.C. Worrest, ed.) Springer-Verlag.
ISBN 13875-7.
Bell, A.A., 1981. Biochemical mechanisms of disease resistance. Ann. Rev.
Plant Physiol. 32:21-81.
Bell, A.R. and J.D. Nalewaja, 1968. Competition of wild oats in wheat and
barley. Weed Sci. 16:505-508.
Bennett, J.H., 1981. Photosynthesis and gas diffusion in leaves of selected
crop plants exposed to ultraviolet-B radiation. J. Environ. Qual.
10:271-275.
Biggs, R.H., 1985. Effects of enhanced ultraviolet-B radiation (280-320 nm)
on soybean, wheat, corn, rice, citrus, and duckweed. EPA Progress Report
CR-811216. Washington, D.C.
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68
Biggs, R.H. and F.M. Basiouny, 1975. Plant growth respones to elevated UV-B
irradiation under growth chamber, greenhouse, and solarium conditions. In
Impacts of Climatic Change on the Biosphere CIAP Monograph 5 (Nachtway,
D.S., Caldwell, M.M. and Biggs, R.H., eds.) pp. 4-197-4-248. U.S.
Department of Transportation, Report No. DOT-TST-75-55, National Techn.
Info. Serv. Springfield, Virginia.
Biggs, R.H. and S.V. Kossuth, 1978. Effects of ultraviolet-B radiation
enhancement under field conditions on potatoes, tomatoes, corn, rice,
southern peas, peanuts, squash, mustard and radish. UV-B Biological and
Climatic Effects Research (EAGER), Final Report, EPA, Washington, D.C..
Biggs, R.H., S.V. Kossuth and A.H. Teramura, 1981. Response of 19 cultivars
of soybeans to ultraviolet-B irradiance. Physiol. Plant. 53:19-26.
Biggs, R.H., P.G. Webb, L.A. Garrard, T.R. Sinclair, and S.H. West, 1984. The
effects of enhanced ultraviolet-B radiation on rice, wheat, corn, soybean,
citrus, and duckweed. Year 3 Interim Report. Environmental Protection
Agency Report 808075-03, EPA, Washington, D.C.
Bogenrieder, A. and Y. Doute, 1982. The effects of UV on photosynthesis and
growth in dependence of mineral nutrition (Lactuca sativa L. and Rumex
alpinus L.). In Biological Effects of UV-B Radiation (H. Bauer, M.M.
Caldwell, M. Tevini and R.C. Worrest, eds.), Gesellschaft fur Strahlen-und
Umweltforschung mbH Munchen, pp. 164-169.
Bogenrieder, A. and R. Klein, 1978. Die abhangigkeit der UV-empfindlichkeit
von der lichtqualitat bel der aufzucht (Lactuca sativa L.). Angew.
Botanik 52:283-293.
Brasseurl, G. and A. de Rudder, 1984. Agent and effects of ozone trends in
the atmosphere. In Stratospheric Ozone Reduction, Solar Ultraviolet
Radiation and Plant Life (R.C. Worrest, ed). Springer-Verlag. ISBN
13875-7.
Bridge, M.A. and W.L. Klarman, 1973. Soybean phytoalexin hydroxyphaseollin,
induced by ultraviolet irradiation. Phytopathol. 63:606-608.
Caldwell, M.M., 1968. Solar ultraviolet radiation as an ecological factor for
alpine plants. Ecolo. Monogr. 38:243-268.
Caldwell, M.M., 1971. Solar UV irradiation and the growth and development of
higher plants. Photophysiol. VI (Giese, A.C., ed.), pp. 131-177.
Academic Press, New York.
Caldwell, M.M., 1977. The effects of solar UV-B (280-315 run) on higher
plants: Implications of stratospheric ozone reduction. In Research in
Photobiology (A. Castellani, ed.), pp. 597-607. Plenum Publ. Corp., New
York.
Caldwell, M.M., 1981. Plant response to solar ultraviolet radiation. In
Encyclopedia of Plant Physiology New Series, Volume 12A. Physiological
Plant Ecology I (Lange, O.L., Nobel, P.S., Osmond, C.B., and Ziegler, H.,
eds.). Springer-Verlag, Berlin, Germany, pp. 169-197.
-------
69
Caldwell, M.M., 1982. Geometric considerations: A brief synopsis. In
Biological Effects of UV-B Radiation (H. Bauer, M.M. Caldwell, M. Tevini
and R.C. Worrest), pp. 142-144 Gesellschaft fur Strahlen-und
Umweltforschung mbH Munchen.
Caldwell, M.M., 1983. Solar UV-B radiation and higher plants: Photosynthetic
inhibition and acclimation. Annual Report for EPA. EPA, Washington, D.C.
Caldwell, M.M., R. Robberecht, S. Holman, R. Nowak, L.B. Camp, S. Flint,
G. Harris, and A.M. Teramura, 1979. Higher plant responses to elevated
ultraviolet irradiance. Annual Report 1978 NAS-9-14871, NASA, Dept. Range
Sci. & Ecology Center, Utah State Univ., Utah.
Caldwell M.M., R. Robberecht and W.D. Billings, 1980. A steep latitudinal
gradient of solar ultraviolet-B radiation in the artic-alpine life zone.
Ecology 61:600-611.
Caldwell, M.M., R. Robberecht, and S.D. Flint, 1983a. Internal filters:
Prospects for UV-allimation in higher plants. Physiol. Plant.
58:445-450.
Caldwell, M.M., W.G. Gold, G. Harris and C.W. Ashurst, 1983b. A modulated
lamp system for solar UV-B (280-320 nm). Supplementation studies in the
field. Photochem. Photobiol. 37:479-485.
Caldwell, M.M., W.B. Sisson, F.M. Fox and J.R. Brandle, 1975. Plant growth
response to elevated UV irradiation under field and greenhouse conditions.
In Climatic Impacts Assessment Program (CIAP), Monograph 5 (Nachtwey,
D.S., Caldwell, M.M. and Biggs, R.H., eds.), pp. 4-243 to 4-249. U.S.
Department of Transportation, Report No. DOT-TST-75-55, National Techn.
Info. Serv., Sprinfield, Virginia.
Caldwell, M.M., L.B. Camp, C.W. Warner and S.D. Flint, 1986. Action spectra
and their key role in assessing biological consequences of solar UV-B
radiation change. In Stratospheric Ozone Reduction, Solar Ultraviolet
Radiation and Plant Life, (R.C. Worrest, ed.), Springer-Verlag. ISBN
13875-7.
Campbell, W.F., M.M. Caldwell, and W.B. Sisson, 1975. Effect of UV-B
tadiation on pollen germination. In Impacts of Climatic Change on the
Biosphere, CIAP Monog. 5., Department of Transportation, Washington, D.C.,
pp. 4-227 to 4-276.
Cams, H.R., J.H. Grahm, and S.J. Ravitz, 1978. Effects of UV-B radiation on
selected leaf pathogenic fungi and on disease severity. EPA-IAG-D6-0168.
EAGER Program, EPA, Washington, D.C.
Chabot, B.F., T.W. Jurik and J.F. Chabot, 1979. Influence of instantaneous
and integrated light-flux density on leaf anatomy and photosynthesis. Am.
J. Bot. 66:940-945.
Chang, D.C.N. and W.F. Campbell, 1976. Responses of tradescantia stamen
hairs and pollen to UV-B irradiation. Envi. Exp. Bot. 16:195-199.
-------
70
Cronquist, A., 1981. An integrated system of classification of flowering
plants. Columbia University Press, New York, p. 1262.
Dickson, J.G. and M.M. Caldwell, 1978. Leaf development of Rumex patLentLa
L. (polygonaceae) exposed to UV irradiation (280-320 run). Amer. J. Bot.
65:857-863.
Dumpert, K., 1983. Einfluss erner nach schadstoffimmission vermehrten UV-B
strahlung auf kulturpflanzen. Bericht fur Gesellschaft fur Strahlen-und
Umweltforschung mbH Bereich Projekttragerschaften Munchen.
Dumpert, K. and J. Boscher, 1982. Response of different crop and vegetable
cultivars to UV-B irradiance: Preliminary results. In Biological Effects
of UV-B Radiation (H. Bauer, M.M. Caldwell, M. Tevini and R.C. Worrest,
eds.), pp. 102-107. Gesellschaft fur Strahlen-und Umweltforschung mbH,
Muchen. ISBN 0721-1694.
Eisenstark, A. and G. Perrot, 1985. Enhanced UV-B irradiation (290-320 nm) of
corn (Zea mays L.). II. Effects of various stages of tassel formation
(greenhouse-plants). Submitted to J. Agronomy.
Eisenstark, A., G.H. Perrot, G. Ulmer, and C.D. Miles, 1985. Enhanced UV-B
irradiation (290-320 nm) of corn (Zea mays L.) I. Effects on growth and
yield. Manuscript submitted to J. Agronomy.
Esser, G., 1979. Einfluss einer nach schadstoffimmission vermehrten
einstrahlung von UV-B-licht auf den ertrag von kulturpflanzen (FKW 22), 1.
Versuchsjahr. Battelle-Institut E.V. Frankfurt.
Esser, G., 1980. Einfluss einer nach schadstoffimission vermehrten
einstrahlung von UV-B-licht auf kulturpflanzen, 2. Versuchsjahr. Bericht
Battelle Institut E.V. Frankfurt, BF-R-63, 984-1.
Flint, S.D. and M.M. Caldwell, 1983. Influence of floral optical properties
on the ultraviolet radiation environment of pollen. Amer. J. Bot.
70:1416-1419.
Flint, S.D. and M.M. Caldwell, 1984. Partial inhibition of in vitro pollen
germination by simulated solar ultraviolet-B radiation. Ecol. 65:792-795.
Flint, S.D. and M.M. Caldwell, 1984. Comparative sensitivity of binucleate
and trinucleate pollen to ultraviolet radiation: A theoretical
perspective. In Stratospheric Ozone Reduction, Solar Ultraviolet
Radiation and Plant Life, (R.C. Worrest, ed.). Springer-Verlag. ISBN
13875-7.
Flint, S.D., P.W. Jordan, and M.M. Caldwell, 1985. Plant protective response
to enhanced UV-B radiation under field conditions: Leaf optical
properties and photosynthesis. Photochem. Photobiol. 41(1):95-99.
Fox, P.M. and M.M. Caldwell, 1978. Competitive interaction in plant
populations exposed to supplementary ultraviolet-B radiation. Oecologia
36:173-190.
-------
71
Garrard, L.A., T.K. Van and S.H. West, 1976. Plant response to middle
ultraviolet (UV-B) radiation: Carbohydrate levels and chloroplast
reactions. Soil and Crop Sci. Soc. Florida Proc. 36:184-188.
Gates, D.M., 1983. An overview. In CO and Plants (Lemon, E.R. ed.),
pp. 7-20. Westview Press Inc., Boulder, Colorado 80301.
Gold, W.G. and M.M. Caldwell, 1983. The effects of ultraviolet-B radiation on
plant competition in terrestrial ecosystems. Physiol. Plant 58:435-444.
Green, A.E.S., K.R. Cross and L.A. Smith, 1980. Improved analytical charac-
terization of ultraviolet skylight. Photochem. Photobiol. 31:59-65.
Hart, R.H., G.E. Carlson, H.H. Klueter and H.R. Carns, 1975. Response of
economically valuable species to ultraviolet radiation. In Climatic
Impacts Assessment Program (CIAP), Monograph 5 (Nachtway, D.S., Caldwell,
M.M. and Biggs, R.H., eds.), pp. 263-275. U.S. Department of
Transportation, Report No. DOT-TST-75-55, National Tech. Info. Serv.,
Springfield, Virginia.
Hashimoto, T. and M. Tajima, 1980. Effects of ultraviolet irradiation on
growth and pigmentation in seedlings. Plant Cell Physiol. 21:1559-1571.
Howland, G.P., R.W. Hart and M.L. Yette, 1975. Repair of DNA strand breaks
after gamma-irradiation of protoplasts isolated from cultured wild carrot
cells. Mutat. Res. 27:81-87.
Heath, R.L., 1975. Ozone. In Response of Plants to Air Pollution (Mudd,
J.B., and Kozlowski, T.T., eds.), pp. 23-56. Academic Press, New York.
ISBN 0-12-509450-7.
Heck, W.W., W.W. Cure, D.S. Shriner, R.J. Olson and A.S. Heagle, 1982. Ozone
impacts on the productivity of selected crops. In Effects of Air
Pollution on Farm Commodities (Jacobson, J.S. and Millen, A.A., eds.).
Izaak Walton League of Am., Arlington, Virginia 22209.
Iwanzik, W. and M. Tevini, 1982. Effects of enhanced UV-B radiation on
photosynthetic activity of barley seedlings and chloroplasts. In
Biological Effects of UV-B Radiation. Proc. workshop, Munich. May 25-27,
1982. BPT-Bericht, pp. 121-131.
Iwanzik, W., M. Tevini, G. Dohnt, M. Voss, W. Weiss, P. Graber and G. Renger,
1983. Action of UV-B radiation on photosynthetic primary reactions in
spinach chloroplast. Physiol. Plant. 58:401-407.
Johnston, H.S. 1971. Reduction of stratospheric ozone by nitrogen oxide
catalysts from supersonic transport exhaust. Science 173:517-522.
Jones, L.W. and B. Kok, 1966. Photoinhibition of chloroplast reactions. I.
Kinetics and action spectra. Plant Physiol. 41:1037-1043.
Kasperbauer, M.J. and W.E. Loomis, 1965. Inhibition of flowering by natural
daylight on an inbred strain of melilotus. Crop Sci. 5:193-194.
-------
72
Keeling, C.D., 1978. Atmospheric carbon dioxide in the 19th century. Sci.
202:1109.
Klarman, W.L. and J.W. Gerdemann, 1963. Resistance of soybean to three
phytophthora species due to the production of a phytoalexin. Phytopathol.
53:1317-1320.
Klein, R.M., P.C. Edsall and A.C. Gentile, 1965. Effects of near
ultraviolet and green radiations on plant growth. Plant Physiol.
40:903-906.
Krizek, D.T., 1978. Differential sensitivity of two cultivars of cucumber
(Cucumis sativus L.) to increased UV-B irradiance: I. Dose-response
studies. Final Report EPA-IAG-D6-0168, USDA/EPA EAGER Prog., EPA,
Washington, D.C.
Lemon, E.R., 1983. CO- and Plants. The Response of Plants to Raising
Levels of Atmospheric Carbon Dioxide. Westview Press Inc., Boulder,
Colorado 80301.
Levitt, J., 1980. Responses of plants to environmental stresses. Vol. 1
Academic Press, New York, pp. 10-18. ISBN 0-12-445501-8.
Lydon, J., A.H. Teramura and E.G. Summers, 1986. Effects of ultraviolet-B
radiation on the growth and productivity of field grown soybeans. In
Stratospheric Ozone Reduction, Solar Ultraviolet Radiation and Plant Life,
(R.C. Worrest, ed.), Springer-Verlag. ISBN 13875-7.
Martin, F.W., 1970. The ultraviolet absorption profile of stigmatic
extracts. New Phytol. 69:425-430.
Martin, F.W. and J.L. Brewbaker, 1971. The nature of the stigmatic exudate
and its role in pollen germination. In Pollen: Development and
Physiology (Heslop-Harrison, ed.), Appleton-Century-Crofts, New York, pp.
262-266.
McWhorter, C.G. and D.T. Patterson, 1980. Ecological factors affecting weed
competition in soybeans. In World Soybean Res. Conference II:
Proceedings (F.T. Corbin, ed.), pp. 371-392. Westview Press, Boulder,
Colorado. ISBN 0-89158-158-899-X.
Mirecki, R.M. and A.H. Teramura, 1984. Effects of ultraviolet-B irradiance on
soybean V. The dependence of plant sensitivity on the photosynthetic
photon flux density during and after leaf expansion. Plant Physiol.
74:475-480.
Mudd, J.B., 1975. Sulfur dioxide. In Response of Plants to Air Pollution
(Mudd, J.B. and Kozlowski, T.T., eds.), pp. 9-22. Academic Press, New
York, ISBN 0-12-509450-7.
Mudd, J.B., and T.T. Kozlowski, 1975. Response of Plants to Air Pollution,
Academic Press, New York. ISBN 0-12-509450-7.
-------
73
Murali, N.S. and A.H. Teramura, 1985a. Effects of UV-B irradlance on soybean.
VI. Influence of phosphorus nutrition on growth and flavonoid content.
Physiol. Plant. 63:413-416.
Murali, N.S. and A.H. Teramura, 1985b. Effects of ultraviolet-B irradiance on
soybean. VII. Biomass and concentration and uptake of nutrients at
varying P supply. J. Plant Nutrition. 8(2):177-192.
Murali, N.S. and A.H. Teramura, 1986a. Intraspecific differences in Cucumis
sativa L. sensitivity to ultraviolet-B radiation. Physiol Plant in press.
Murali, N.S. and A.H. Teramura, 1986b. Effects of supplemental ultraviolet-B
radiation on the growth and physiology of field-grown soybean. Env. Exp.
Bot. 26:233-242.
Murali, N.S. and A.H. Teramura, 1986c. Effectiveness of UV-B radiation on the
growth and physiology of field-grown soybean modified by water stress.
Photochem. Photobiol. 44:215-220.
Murali, N.S., A.H. Teramura, and S.K. Randall, 1986d. A comparative study of
ultraviolet-B sensitivity between two soybean cultivars. Env. Exp. Bot.
in review.
Nachtwey, D.S., 1975. Linking photobiological studies at 254 nm with UV-B.
In Climatic Impact Assessment Program (CIAP), Monograph 5 (Nachtwey, D.S.,
Caldwell, M.M. and Biggs, R.H., eds.), pp. 3-50 to 3-84. U.S. Department
of Transportation, Report No. DOT-TST-75-55, National Techn. Info. Serv.,
Springfield, Virginia.
NAS. National Academy of Sciences, 1979. Stratospheric ozone depletion by
halocarbons: Chemistry and transport. National Academy Press,
Washington, D.C.
NAS. National Academy of Sciences, 1984. Causes and effects of changes in
stratospheric ozone: Update 1983. National Academy Press, Washington,
D.C.
NRC. National Research Council, 1982. Causes and effects of stratospheric
ozone reduction: An update. National Academy Press, Washington, D.C.
ISBN 0-309-03248-2.
Nobel, P.S. and T.L. Hartsock, 1981. Development of leaf thickness for
Plectranthus parviflorus - influence of photosynthetically active
radiation. Physiol. Plant. 51:163-166.
Owens, O.V.H. and D.T. Krizek, 1980. Multiple effects of UV radiation
(265-330 nm) on fungal spore emergence. Photochem. Photobiol. 32:41-49.
Popp, H.W. and F. Brown, 1936. The effects of ultra-violet radiation upon
seed plants. In Biological Effects of Radiation (B.M. Duggar, ed.), Vol.
2, pp. 853-887, McGraw-Hill, New York.
-------
74
Reilly, J.J., 1975. The role of thymine dimers in the induction of
phytoalexin, hydroxyphaseollin, in ultraviolet irradiated soybean
suspension culture. Ph.D. Thesis, University of Maryland, College Park,
Maryland.
Reinert, R.A., A.S. Heagle and W.W. Heck, 1975. Plant responses to pollutant
combination. In Response of Plants to Air Pollution (Mudd, J.B. and
Kozlowski, T.T., eds.), pp. 159-178. Academic Press, New York. ISBN
0-12-509450-7.
Robberecht, R. and M.M. Caldwell, 1978. Leaf epidermal transmittance of
ultraviolet radiation and its implication for plant sensitivity to
ultraviolet-radiation induced injury. Oecologia 32:277-287.
Rupert, C.S., 1984. Cellular repair and assessment of UV-B radiation damage.
In Stratospheric Ozone Reduction, Solar Ultraviolet Radiation and Plant
Life (R.C. Worrest, ed.), Springer-Verlag. ISBN 13875-7.
Schmailzl, U. and P.J. Crutzen, 1984. Inconsistencies in current
photochemical models deduced from considerations of the ozone budget. In
Stratospheric Ozone Reduction, Solar Ultraviolet Radiation and Plant Life.
(R. Worrest, ed.), Springer-Verlag. ISBN 13875-7.
Semeniuk, P. and R.W. Goth, 1980. Effect of ultraviolet irradiation on local
lesion development of potato virus S on Chenopodium quinoa cv. Valdivia
leaves. Envi. Exp. Bot. 20:95-98.
Setlow, R.B., 1974. The wavelengths in sunlight effective in producing skin
cancer: A theoretical analysis. Proc. Nat. Acad. Sci. 71:3363-3365.
Sisson, W.B., 1981. Photosynthesis, growth, and ultraviolet irradiance
absorbance of Cucurbita pepo L. Leaves exposed to ultraviolet-B radiation
(280-315 nm). Plant Physiol. 67:120-124.
Sisson, W.B. and M.M. Caldwell, 1976. Photosynthesis, dark respiration, and
growth of Rumex patientia L. exposed to ultraviolet irradiance (280 to 315
nanometers) simulating a reduced atmospheric ozone column. Plant Physiol.
58:563-568.
Sisson, W.B. and M.M. Caldwell, 1977. Atmospheric ozone depletion: Reduction
of photosynthesis and growth of a sensitive higher plant exposed to
enhanced UV-B radiation. J. Exp. Bot. 28:691-705.
Southworth, D., 1969. Ultraviolet absorption spectra of pollen and spore
walls. Grana Palynologia 9(1-3):1-15.
Soyfer, V.N., 1983. Influene of physiological conditions on DNA repair
and mutagenesis in higher plants. Physiol. Plant 58:373-380.
Stanley, R.G. and H.F. Linskens, 1974. Pollen: Biology, biochemistry,
management. Springer-Verlag, New York, p. 307.
Steinmiller, D. and M. Tevini, 1985. Action of ultraviolet radiation (UV-B)
upon cuticular waxes in some crop plants. Planta. 164:557-564.
-------
75
Strain, B.R., and F.A. Bazzaz, 1983. Terrestrial plant communities. In CO
and Plants (Lemon, E.R. ed.), pp. 177-222. Westview Press Inc., Boulder,
Colorado 80301.
Tanada, T. and S.B. Hendricks, 1953. Photoreversal of ultraviolet effects in
soybeans. Amer. J. Bot. 40:634-637.
Taylor, O.C., C.R. Thompson, D.T. Tingey and R.A. Reinert, 1975. Oxides of
nitrogen. In Response of Plants to Air Pollution (Mudd, J.B. and
Kozlowski, T.T., eds.), pp. 23-56. Academic Press, New York. ISBN
0-12-509450-7.
Teramura, A.H., 1980. Effects of ultraviolet-B irradiance on soybean. I.
Importance of photosynthetically active radiation in evaluating
ultraviolet-B irradiance effects on soybean and wheat growth. Physiol.
Plant. 48:333-339.
Teramura, A.H., 1981a. Differences in the photosynthetic response to UV-B
radiation between mature and immature leaves. Plant Physiol. 67(suppl):
93(Abstract)
Teramura, A.H., 1981b. Cultivar differences in the effects of enhanced UV-B
irradiation. Annual Report for EPA, EPA, Washington, D.C.
Teramura, A.H., 1982a. The amelioration of UV-B effects on productivity by
visible radiation. In The Role of Solar Ultraviolet Radiation in Marine
Ecosystems (J. Calkins, ed.), pp. 367-382, Plenum Publ. Corp. New York.
ISBN 0-306-40909-7.
Teramura, A.H., 1982b. Cultivar differences in the effects of enhanced UV-B
irradiation. Annual Report for EPA, EPA, Washington, D.C.
Teramura, A.H., 1983a. Effects of ultraviolet-B radiation on the growth and
yield of crop plants. Physiol. Plant. 58:415-427.
Teramura, A.H., 1983b. Cultivar differences in the effects of enhanced UV-B
irradiation. Annual Report for EPA, EPA, Washington, D.C.
Teramura, A.H., 1984. Interaction between UV-B radiation and other stresses
in plants. In Stratospheric Ozone Reduction, Solar Ultraviolet Radiation
and Plant Life. (R.C. Worrest, ed.), Springer-Verlag. ISBN 13875-7.
Teramura, A.H., R.H. Biggs and S. Kossuth, 1980. Effects of ultraviolet-B
irradiances on soybean. II. Interaction between ultraviolet-B and
photosynthetically active radiation on net photosynthesis, dark,
respiration, and transpiration. Plant Physiol. 65:483-488.
Teramura, A.H., M. Tevini and W. Iwanzik, 1983. Effects of ultraviolet-B
irradiation on plants during mild water stress. I. Effects on diurnal
stomatal resistance. Physiol. Plant. 57:175-180.
-------
76
Teramura, A.H., M.C. Perry, J..Lydon, M.S. Mclntosh and E.G. Summers,
1984a. Effects of ultraviolet-B radiation on plants during mild water
stress. III. Effects on photosynthesis recovery and growth in soybean.
Physiol. Plant. 60:484-492.
Teramura, A.H., I.N. Forseth and J. Lydon, 1984b. Effects of ultraviolet-B
radiation on plants during mild water stress. IV. The insensitivity of
soybean internal water relations to ultraviolet-B radiation. Physiol.
Plant (in press).
Teramura, A.H. and N.S. Murali, 1986. Intraspecific differences in growth and
yield of soybean exposed to ultraviolet-B radiation under greenhouse and
field conditions. Env. Exp. Bot. 26:89-95.
Tevini, M. and W. Iwanzik, 1982. The effects of UV-B irradiation on higher
plants. In The Role of Solar Ultraviolet Radiation in Marine Ecosystems
(J. Chalkins, ed.), pp. 581-615. Plenum Pub. Corp. New York.
Tevini, M. and W. Iwanzik, 1983. Inhibition of photosynthetic activity by
UV-B radiation in radish seedlings. Physiol. Plant. 58:395-400.
Tevini, M., W. Iwanzik and A.H. Teramura, 1983. Effects of UV-B radiation on
plants during mild water stress. II. Effects on growth, protein and
flavonoid content. Zeitschrift fur Pflanzenphysiologie 110:459-467.
Tevini, M., W. Iwanzik and U. Thoma, 1981. Some effects of enhanced UV-B
irradiation on the growth and composition of plants. Planta 153:388-394.
Tevini, M., W. Iwanzik, and U. Thoma, 1982. The effects of UV-B irradiation
on higher plants. In Nato Conference Series, Series IV. (J. Chalkins,
ed.). Plenum Press, New York and London, pp. 435-448.
Tevini, M., U. Thoma, and W. Iwanzik, 1983. Effects of enhanced UV-B
radiation on germination, seedling growth, leaf anatomy, and pigments of
some crops. Z. Pflanzenhysiol. 109:435-448.
Thompson, W.R., J. Meinwald, D. Aneshansley and T. Eisner, 1972.
Flavonols: Pigments responsible for ultraviolet absorption in nectar
guide of flowers. Science 177:528-530.
Uehara, K., 1958. On the phytoalexin production of the soybean pod in
reaction to Fusarium sp., the causal fungus of pod blight. I. Some
experiments on the phytoalexin production as affected by host plant
conditions and the nature of the phytoalexin produced. Ann. Phytopathol.
Soc. Japan 23:225-229.
Van, T.K. and L.A. Garrard, 1975. Effect of UV-B radiation on net
photosynthesis of some C_ and C, crop plants. Soil and Crop Sci. Soc.
Florida Proc. 35:1-3.
Van, T.K., L.A. Garrard and S.H. West, 1976. Effects of UV-B radiation on net
photosynthesis of some crop plants. Crop Sci. 16:715-718.
-------
77
Vu, C.V., L.H. Allen and L.A. Garrard, 1978. Effects of supplemental
ultraviolet radiation (UV-B) on growth of some agronomic crop plants.
Soil and Crop Sci. Soc. Florida Proc. 38:59-63.
Warner, C.W. and M.M. Caldwell, 1983. Influence of photon flux density in the
400-700 nm waveband on inhibition of photosynthesis by UV-B (280-320 nm)
irradiation in soybean leaves: Separation of indirect and immediate
effects. Photochem. Photobiol. 38:341-346.
Wellmann, F., 1982. Phenylpropanoid pigment synthesis and growth reduction as
adaptive reactions to increased UV-B radiation. In Biological Effects of
UV-B Radiation. (H. Bauer, M.M. Caldwell, M. Tevini and R.C. Worrest,
eds.), pp. 145-149. Gessellschaft fur Strahlen-und Umweltforschung mbH,
Munchen.
Whittaker, R.H., 1975. Communities and ecosystems. MacMillan Publishing Co.,
Inc., New York.
Zeevaart, J.A.D., 1976. Physiology of flower formation. Ann. Rev. Plant
Physiol. 27:321-348.
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APPENDICES
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APPENDIX A
ACTION SPECTRA AND THEIR KEY ROLE IN ASSESSING
BIOLOGICAL CONSEQUENCES OF SOLAR UV-B RADIATION CHANGE
By
M. M. Caldwell
L. B. Camp
C. W. Warner
S. D. Flint
Utah State University
Logan, Utah
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Action Spectra and Their Key Role in Assessing Biological
Consequences of Solar UV-B Radiation Change
M.M. Caldwell, L.B. Camp, C.W. Warner, and S.D. Flint
Utah State University, Logan, Utah, USA
ABSTRACT
Action spectra of UV damage to plants must be used as weighting functions
to (1) evaluate the relative increase of solar UV radiation that would
result from a decreased atmospheric ozone layer, the radiation amplifica-
tion factor—RAF, (2) evaluate the existing natural gradients of solar UV
irradiance on the earth, and (3) compare UV radiation from lamp systems in
experiments with solar UV radiation in nature. Only if the relevant
biological action spectra have certain characteristics is there a potential
biological problem that would result from ozone reduction. Similarly the
existence of a natural latitudinal solar UV gradient is dependent on action
spectrum characteristics.
Several UV action spectra associated with different basic modes of damage
to plant tissues all have the common characteristic of decreasing effect
with increasing wavelength; however, the rate of decline varies consider-
ably. Extrapolation from action spectra that have been measured on
isolated organelles and microorganisms using monochromatic radiation to
effects of polychromatic radiation on intact higher plants is precarious.
Development of action spectra using polychromatic radiation and intact
higher plant organs can yield spectra that are of more ecological relevance
for weighting factors in assessment of the ozone reduction problem. An
example of an action spectrum for photosynthetic inhibition developed with
polychromatic radiation is provided in this chapter. This action spectrum
has different characteristics, and results in a greater RAF than do action
spectra for inhibition of a partial photosynthetic reaction, the Hill
reaction, developed with isolated chloroplasts and photosynthetic bacteria.
Circumstantial evidence from experiments with plants originating from
different latitudes also supports the notion that action spectra with
characteristics similar to that of the provisional spectrum, developed with
polychromatic radiation, are appropriate. Further work with polychromatic
radiation is encouraged.
There are two basic types of error that are associated with the use of
action spectra in biological assessments of the ozone reduction problem,
the RAF errors and the enhancement errors. The former are those associated
with calculation of the RAF, and the latter are those derived from calcula-
tion of the UV radiation enhancement used in experiments with lamp systems.
While the RAF errors are recognized, the enhancement errors have not been
generally appreciated. An error analysis is presented showing that the
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enhancement errors will typically be larger and in the opposite direction
than the RAF errors. The enhancement error should be considerably less in
field UV supplementation experiments than in most laboratory experiments
which employ fluorescent lamps as the primary UV-B radiation source.
INTRODUCTION
Traditionally, biological action spectra have been employed to elucidate
photobiological mechanisms, and specifically to identify potential chromo-
phores. Action spectra are usually assessed by evaluating biological
responsiveness to monochromatic irradiation. In order to identify
potential chromophores, there has been an emphasis on the fine structure of
action spectra and little attention has been directed to the tails of these
spectra.
In assessment of the consequences of solar UV-B radiation changes, action
spectra serve a very different role. Weighting functions are derived from
action spectra to assess the relative biological effectiveness of polychro-
matic irradiance. Spectral irradiance is weighted and then integrated over
a waveband of interest, thus:
effective irradiance ^I^E^d ^ (1)
where I^is the spectral irradiance, and E^is the relative effectiveness of
irradiance at wavelength to elicit a particular biological response. The
limits of the integration are prescribed by the wavelengths where either I«
or Fj^approach zero.
Spectral irradiance and the action spectra can be expressed on either a
photon or an energy basis. As units of effective irradiance it is most
useful to speak of "weighted" or "effective" energy flux or photon flux
density (e.g., effective W m~2 Or effective moles photons m~2 s'1) and, of
course, to specify the action spectrum used as a weighting function and the
wavelength to which the spectrum is normalized. Special units analogous to
units of illumination (e.g., lux) have been previously devised for effec-
tive UV radiation (such as sunburn units, E-viton and the Finsen for
erythemally effective radiation (Robertson 1975; Luckiesh and Holladay
1933) and the G-viton for germicidal UV radiation (Luckiesh and Holladay
1933). However, unlike illumination where a standard spectral luminosity
function has been well accepted, UV action spectra for various biological
phenomena are continually being refined or abandoned in favor of new action
spectra and, thus, either the units need to be redefined or new units
described. Therefore, use of effective energy or photon flux with a
specified action spectrum is quite preferable to the definition of new
units.
The utility of weighting the UV irradiance and, thus, expressing biolog-
ically effective irradiance for the ozone reduction problem derives from
the highly wavelength-specific absorption characteristics of atmospheric
ozone and the wavelength specificity of biological action spectra in the
UV-R waveband (National Academy of Sciences 1979; Nachtwey and Rundel 1982;
Caldwell 1981). The expression of weighted effective irradiance is useful
in addressing three basic issues:
-------
(1) The degree to which biologically damaging solar UV irradiation is
increased when atmospheric ozone decreases is very dependent on the action
spectrum characteristics. The increment of biologically damaging solar
^irradiation resulting from a given level of ozone reduction for a specific
set of conditions, is known as the radiation amplification factor, RAF
(National Academy of Sciences 1979). Without calculation of an RAF, which
takes the biological effectiveness of each wavelength into account, the
increment of total solar UV-B flux resulting from ozone reduction is
trivial, e.g., 1% increase of UV-B radiation for 16% ozone reduction for
midday irradiance in the summer at temperate latitudes (Caldwell 1981).
The increase of solar UV-B irradiation as a function of ozone reduction
only becomes significant when the biological effectiveness of this radia-
tion is calculated and the action spectrum for this calculation has certain
characteristics. By the same token, if the action spectrum of a particular
biological phenomenon does not exhibit the appropriate characteristics, the
RAF will be very small and this phenomenon can be eliminated from concern
with respect to the consequences of ozone reduction without the necessity
of dose-response studies.
(2) The steepness of the natural latitudinal gradient of solar UV-B
irradiance that currently exists on the Earth's surface should also be
evaluated in terms of potential biological effectiveness. The natural
gradient of UV-B radiation serves as a basis for study of organism response
to solar UV-B radiation and can provide insight into potential consequences
of ozone reduction. This gradient has been used most frequently in the
analysis of human skin cancer incidence; however, study of plant adaptation
to UV-B radiation at different latitudes can also be instructive (e.g.,
Caldwell et al. 1982; Robberecht et al. 1980). As is the case with ozone
reduction, without taking biological effectiveness of solar UV-B irradia-
tion into account, the natural latitudinal gradient of solar UV-B radiation
is virtually nonexistent (Caldwell 1981).
(3) Since spectral irradiance received from commonly-used lamp systems for
UV-B studies does not match that of solar irradiance, it is only possible
to draw comparisons by calculating "biologically effective" radiation using
action spectra as weighting functions. Characteristics of action spectra
will thus dictate the amount of radiant flux delivered by lamp systems in
experiments designed to evaluate potential consequences of ozone reduction
under different conditions.
This chapter will (1) review a few action spectra illustrating different
fundamental mechanisms of UV-B damage in plant cells, (2) discuss the use
of polychromatic radiation in determining action spectra and illustrate
this with a new action spectrum for photosynthetic inhibition, (3) show the
nature of radiation amplification factors that result from action spectra
of different characteristics, (4) briefly discuss the implications of
action spectra for the natural latitudinal gradient of solar UV-B radia-
tion, and (5) develop an error analysis of the types and magnitude of
errors that might be encountered in biological assessments by assuming an
improper action spectrum.
-------
ANALYSIS
Modes of Damage and Their Spectra
Ultraviolet radiation can damage plant cells by several basic mechanisms
and these pathways of damage likely involve several different chromophores.
To illustrate the diversity of damage pathways, several action spectra are
depicted in Fig. 1. In each case the reaction is identified with damage to
a specific entity or process in the cell. However, this does not mean that
the entity damaged is necessarily the primary chromophore (Peak and Peak
1983). All spectra are normalized to 300 nm. Though these spectra
10
10'
V
,o-
1'°'
o-
o>
CT
10'
,-5
JHill reaction
ATPase
^-single strand
breaks'
280 300 320 340 360 380 400
Wavelength (nm)
Fig. 1. Ultraviolet action spectra representing basic modes of damage to
plant tissues. The spectra were all developed with monochromatic radiation
and are plotted on a quantum effectiveness basis relative to 300 nm. These
include inhibition of Hill reaction activity in isolated chloroplasts of
spinach (Jones and Kok 1966), inhibition of adenosine triphosphatase
(ATPase) from plasma membranes of Rosa damascene (Imbrie and Murphy 1982),
induction of single strand breaks of Bacillus subtilis DNA (Peak and Peak
1982), lethality of stationary phase cells of £._ coli associated with cell
membrane damage (Kelland et al. 1983), inhibition of alanine uptake in £._
coli linked to inactivation of carrier proteins (Sharma and Jagger 1981),
and inactivation of stationary phase cells in F^ coli associated with
nucleic acid damage (Webb 1977).
-------
84
represent different basic pathways of damage, and in many cases presumably
very different chromophores, all have the common property of decreasing
effect as wavelength increases. These spectra have been developed in the
normal manner using monochromatic radiation and in several cases have been
pursued through several orders of magnitude. If these were to be plotted
with a linear ordinate, the differences in these spectra would be much less
apparent. Nevertheless, as will be discussed subsequently, if these
spectra are to be used as weighting factors for solar UV radiation, which
increases by orders of magnitude with increasing wavelength, the
differences in slopes of these action spectra'are of key importance. These
spectra have been determined with isolated organelles, membranes, or micro-
organisms, but none involved intact higher plants.
Complications: Intact Higher Plants and Polychromatic Radiation
Since the spectra illustrated in Fig. 1 differ greatly in their decline
with increasing wavelength, it is important to know which of these primary
damage mechanisms are the most important for intact higher plants exposed
to solar radiation. This is not an easily answered question. One would
need to know (1) the basic sensitivity of the respective targets (e.g.,
DNA, membranes, Photosystem II of photosynthesis, etc.) for the higher
plant species in question, (2) how well shielded these targets are within
the plant organ (i.e., the effective spectral fluence reaching the target),
(3) to what extent reciprocity would apply, and (4) if radiation at
different wavelengths when applied simultaneously and in proportion to
their occurrence in sunlight would have strictly additive effects, as
predicted by the action spectrum, or whether these effects would be posi-
tively or negatively synergistic. Addressing these several issues is
hardly a trivial undertaking and satisfactory answers are not likely to be
quickly forthcoming. For example, as to the question of synergistic
effects of radiation at different wavelengths, much is known about
mechanisms of UV radiation effects on nucleic acids and yet it is still
difficult to quantitatively predict synergistic effects in higher plants.
From jn_ vitro studies and from ^n_ vivo experiments with microorganisms, it
is clear that there are qualitative differences between UV-B and UV-A
damaging photoreactions (Peak and Peak 1983): UV-A radiation can drive
photorepair of UV-B-induced damage (Jagger 1981), UV-B radiation can induce
other repair systems which can repair at least a fraction of the UV damage
(Menezes and Tyrrell 1982), UV-A radiation can cause growth delay in
bacteria which allows more time for dark repair systems to operate (Jagger
1981), and, finally, UV radiation at high fluence rates can damage UV
repair systems (Webb 1977). The net effect of these phenomena and their
applicability to higher plant nucleic acid damage is not easily envisaged.
The primary site of UV damage to photosynthesis is in the reaction center
of Photosystem II (Penger et al. this volume; Noorudeen and Kulandaivelu
1982) and most likely does not involve nucleic acids. For intact higher
plants, interactions between UV-B and longer wavelength radiation have been
frequently reported though the mechanisms are not understood. Plant leaves
which have developed under low visible radiation conditions are consider-
ably more sensitive to UV-B inhibition of photosynthesis (Teramura et
al. 1980; Sisson and Caldwell 1976; Warner and Caldwell 1983). Yet, there
is also some evidence that higher visible irradiance during UV-B irradia-
tion increases the inhibition of photosynthesis even though the visible
irradiation by itself is not sufficient to inhibit photosynthesis (Warner
and Caldwell 1983). At present, one can only speculate about the mecha-
-------
nisms involved in these interactions.
A Photosynthetic Inhibition Spectrum
Predicting the net effect of interactions between radiation of different
wavelengths for phenomena such as nucleic acid damage or inhibition of
photosynthesis is not possible at present even though the action spectra
for some repair processes such as photoreactivation are known. Thus, in
order to account for the synergistic effects of radiation at different
wavelengths when "damage" action spectra are to be used as weighting
functions for polychromatic radiation, one is forced to take a more
empirical approach. This can be done by employing polychromatic radiation
in the development of action spectra and using intact plant organs. In
this process the biological responses to different combinations of poly-
chromatic irradiation are determined and these responses and associated
spectral irradiance data can be deconvoluted to yield an action spectrum
(Rundel 1983). With respect to the ozone reduction problem, the most
logical combinations of polychromatic irradiation involve a constant back-
ground of longwave UV-A and visible irradiance with increments of radiation
at shorter wavelength intervals. This process can sacrifice some of the
fine structure of an action spectrum, but this is of less concern for the
purpose of weighting functions.
This series of polychromatic irradiation distributions should be planned to
account for the tail of the action spectrum into the UV-A or visible
waveband, as the case may be. Characteristics of the action spectrum below
280 nm are of no concern with respect to solar UV radiation changes because
of the effectiveness of atmospheric ozone absorption, even in the case of a
severely depleted ozone layer (Caldwell 1979). Yet, if a particular lamp
system emits shorter wavelengths, the weighting function should include
these as well.
To illustrate this polychromatic approach to action spectrum development,
reduction of photosynthesis of an intact leaf of Rumex patientia will be
depicted. Photosynthetic inhibition of higher plants by UV radiation is of
potential concern with respect to ozone reduction. For some species under
certain experimental conditions, solar UV radiation at flux rates now
received at temperate latitudes has been shown to reduce photosynthesis
(Bogenrieder and Klein 1977; Sisson and Caldwell 1977). Yet to be
resolved, however, is the extent to which plants experience photosynthetic
inhibition under field conditions, or how much they might be inhibited in
the event of ozone layer reduction. Nevertheless, there is sufficient
impetus to select net photosynthesis for action spectrum analysis because
of its potential susceptibility to solar UV radiation and its obvious
importance for plant biology. Furthermore, net photosynthesis is an inte-
grated physiological process which requires the integrity of membrane
systems and the coordinated action of photochemical and enzymatic
processes. Thus, it also serves as a useful indicator of plant response to
stress.
Methods: Assessment of photosynthetic depression resulting from UV
irradiation involved the determination of net CO2 uptake by plant leaves,
exposure of the leaves to a particular polychromatic irradiation distribu-
tion, and then subsequent determination of CO2 uptake capacity under iden-
tical conditions. Ideally, the leaves would be exposed to the inactivating
UV irradiation over a period of several days or weeks as would occur under
-------
86
field conditions. Unfortunately, this involves unreasonable biological and
experimental complications. Leaf photosynthetic characteristics change
appreciably with leaf age (e.g., Sestak 1977; Sisson and Caldwell 1977).
These changes combined with the time and logistic requirements for such
experiments render this approach infeasible. Thus, the irradiation periods
ranged from one to 16 hours. Seven polychromatic radiation distributions
were employed. For each, a dose-response relationship was developed. Even
with these irradiation periods, such experiments are very time consuming.
The spectral irradiance for the seven polychromatic irradiation distribu-
tions are shown in Fig. 2. These were developed by using a 2.5-kW xenon
high pressure lamp and a combination of dichroic and sharp cutoff filters.
Much of the visible and infrared radiation was removed by the dichroic
filter arrangement in order to prevent excessive leaf temperatures. Yet,
there was sufficient visible flux (400^pioles m~2 s~l between 400 and 700
nm) to drive photosynthesis of the plants during the UV irradiation.
Leaves still intact with the remainder of the plant were placed on a slowly
revolving stage in this radiation field to insure even irradiation of the
leaves.
c
1000
O)
u
c
O
•6
o
OJ
0.
CO
100
10
O.I
280
260 280 300 320 WO 360 380 40O
Wavelength (nm)
Fig. 2. Spectral irradiance for seven polychromatic irradiation distribu-
tions used in the development of an action spectrum for inhibition of
photosynthesis. Radiation is supplied by a 2.5-kW xenon high pressure lamp
and filtered with a combination of dichroic and absorption filters. The
sharp cutoff filters used for each distribution are from the Schott WG
series.
Net photosynthetic rates of intact leaves were assessed by measurements of
net CC>2 uptake under specific environmental conditions in a gas exchange
cuvette. By measurement of simultaneous C02 and water vapor flux of the
foliage as well as other parameters including leaf temperature, CC>2 concen-
tration in the cuvette air, and water vapor concentration in the cuvette,
it is possible to calculate intercellular CO2 concentrations within the
leaf (e.g., Caldwell et al. 1977). Intercellular CC>2 is influenced
-------
primarily by photosynthetic rates, CO2 in the cuvette airstream, and
diffusion resistance provided by stomata. Since photosynthesis is normally
substrate limited, it is important to manage the cuvette conditions to
maintain a constant intercellular C02 concentration in the leaf before and
after irradiation so that metabolic photosynthetic capacity of a leaf is
assessed without the complication of changes in diffusion resistances
between the leaf intercellular CC>2 and the air. Direct coupling of the gas
exchange system with a computer allows immediate assessment of these
parameters so that adjustments in cuvette conditions can be made during the
course of these measurements.
Results and discussion: The dose-response relationships for net photosyn-
thetic inhibition of Rumex patientia leaves are shown in Fig. 3 for the
different spectral irradiance distributions. Each data point represents a
different leaf measured on a different date since each determination
required a day to complete. Nevertheless, these dose-response data reveal
linear relationships. The coefficients of determination, R2, range between
0.63 and 0.98 with an average of 0.87. The spectral irradiance combination
which included the least short wavelength radiation (WG 360, Fig. 2) did
not result in inhibition of photosynthesis under these conditions even
after 16 hours of exposure.
50
40J-
30-
I
"^
"i 20
10
c
>»
1/1
o
I WG 280
WG 295
WG 305
WG320
WG 335
WG 345
WG360
6 6 10 i2 14
Irradiation period (hrs)
Fig. 3. Relative inhibition of net photosynthesis of intact Rumex patientia
leaves exposed to the polychromatic irradiation combinations shown in
Fig. 2.
These photosynthetic inhibition data indicate that when there was sensi-
tivity to a particular irradiation distribution, we were dealing with a
linear portion of the dose-response relationship. This is important in
developing action spectra. If a particular dose-response relationship
exhibits diminished slope as with saturation, these data cannot be compared
with a dose-response relationship which is in the initial, linear phase.
The dose-response relationships presented here indicate that it is suitable
to utilize the slope of these linear regression relationships for biolog-
-------
ical response in developing these action spectra.
When these slopes are taken as the relative effect for each spectral
irradiance combination, an action spectrum can be deconvoluted from the
slopes and respective spectral irradiance data (Rundel 1983). Several
possible spectra can result depending on the exact procedure followed. The
spectrum shown in Fig. 4 is the monotonic function that provided the best
fit to the data (Rundel 1983).
O)
c
51 10
Ol
"5 0
10
3
"E
O
§ I0''h
OJ
cr
Anocystis
reaction^-—.;
chioroplasts
280 300 320 340 360 380
Wavelengih (nm)
Fig. 4. Action spectrum for inhibition of photosynthesis for an intact leaf
of Rumex patientia deconvoluted from the data of Figs. 2 and 3 by Rundel
(1983) for his monotonic function that provided the best fit. Spectra for
inhibition of Hill reaction in isolated spinach chioroplasts (Jones and Kok
1966) and of the Cyanobacterium, Anacytis, (Hirosawa and Miyachi 1983) are
also shown. The two Hill reaction spectra were developed with monochro-
matic radiation.
The action spectrum deconvoluted from the polychromatic radiation study
with intact leaves is considerably steeper than the spectrum for inhibition
of a partial photosynthetic reaction, the Hill reaction, conducted by
treating isolated spinach chloroplasts with monochromatic radiation (Jones
and Kok 1966). The spectrum for inhibition of fluorescence rise time from
spinach thylakoid suspensions (Bjorn et al. this volume) and a spectrum for
Hill reaction inhibition of the Cyanobacterium, Anacystis nidulans,
(Hirosawa and Miyachi 1983), also developed with monochromatic radiation,
correspond closely with the spectrum of Jones and Kok. The two Hill
reaction inhibition spectra are also shown in Fig. 4.
Preliminary results of more recent action spectrum studies for Rumex
patientia and other species suggest that the action spectrum may exhibit
steeper declines with increasing wavelength than the spectrum for Rumex
shown in Fig. 4. This new work involves simultaneous UV irradiation and
leaf gas exchange measurements. With a split-beam arrangement, the leaf is
also simultaneously receiving high visible irradiation (800 to 1200 i^
-------
89
m-2 s'1, depending on the species being investigated). Though the visible
flux employed is still only 40 to 60 percent of that in midday solar
radiation, photosynthesis is light saturated. Since subsequent action
spectra conducted with higher visible irradiance may reveal steeper
declines with increasing wavelength, the action spectrum shown in Fig. 4
for Rum ex should be considered as only provisional. The importance of the
rate of decline with increasing wavelength when action spectra are used as
weighting functions is discussed in a subsequent section.
Although practical limitations do not permit these experiments to be
performed with spectral irradiance that exactly matches that of solar
radiation, this approach with polychromatic radiation and intact leaves
should provide a much more realistic approximation of the ecologically
relevant action spectra for photosynthetic inhibition. It also indicates
that extrapolation from damage spectra of specific physiological reactions,
as shown in Fig. 1, to intact organisms may not provide reliable results.
As will be discussed in a subsequent section, there is also indirect
evidence that the action spectrum developed for inhibition of photosyn-
thesis by this polychromatic approach may be appropriate for plants in
nature.
Action Spectra and Radiation Amplification Factors
One of the functions of action spectra in assessment of the ozone reduction
problem is their use in evaluating radiation amplification factors, RAF,
i.e., the relative increase in biologically effective UV radiation for a
given level of ozone reduction. As noted in a previous section, all UV
damage spectra exhibit a general decrease in effectiveness with increasing
wavelength, though the rates of decline vary considerably (e.g., Fig. 1).
Since solar spectral irradiance increases by orders of magnitude with
increasing wavelength, the rate of decline of action spectra has a
pronounced effect on the resulting RAF when these spectra are used as
weighting functions. Furthermore, even though ozone reduction would only
result in increases of solar spectral irradiance in the UV-B part of the
spectrum (Caldwell 1981), the weighting function should include all wave-
lengths of the solar spectrum where the weighted spectral irradiance adds
appreciably to the integral of Eq. (1). Although many UV-B biological
damage spectra include the UV-A region, few extend far into the visible
spectrum. This is not of great consequence if the effectiveness is already
so low by 400 nm that the weighted visible flux would not contribute
significantly to the total biologically effective flux (such as is the case
for DNA damage), or if the action spectrum is already sufficiently flat so
as to result in a negligible RAF (as is the case for the Hill reaction
spectrum).
To illustrate the behavior of the RAF calculated with different action
spectra, a variety of spectra currently in use, as well as the provisional
photosynthetic inhibition action spectrum for Rumex, are portrayed in
Fig. 5 and the respective RAF values for different total ozone column
thickness relative to 0.32 cm in Fig. 6. The model of Green et al. (1980)
was used to calculate the spectral irradiance. The action spectra have
been chosen because they illustrate the RAF values for spectra with a broad
range of slopes.
The DNA damage spectrum is a generalized spectrum compiled by Setlow
(1974). The generalized plant damage spectrum is also the result of a
-------
90
compilation of several plant'damage spectra that exhibit similar character-
istics (Caldwell 1971). The generalized plant damage spectrum terminates
at 313.3 nm simply because that was the longest wavelength (an emission
line from mercury vapor UV lamps) where information was available for these
spectra at the time they were compiled. (If these spectra decline steeply
beyond 313 nm as the DNA-damage spectrum does, the contribution of weighted
spectral irradiance at wavelengths greater than 313 nm would be negligible
for the total integrated biologically effective flux.) The Robertson-
Berger, R-B, meter is a widely used integrating dosimeter for solar UV
monitoring (Perger et al. 1975). The spectral response of this meter was
originally designed to approximate that of human skin erythema. The provi-
sional spectrum for photosynthetic inhibition of Rumex (Fig. 4) is also
included; although preliminary data (cited previously) indicate that a
steeper spectrum may be more appropriate and that this would result in
greater RAF values.
280 290 300 3iO 320 330 340
Wavelength (nm)
Fig. 5. Action spectra exhibiting different rates of decline with
increasing wavelength. These include the spectrum for Hill reaction
inhibition of spinach chloroplasts (Jones and Kok 1966), the Rumex leaf
photosynthesis inhibition spectrum (Fig. 4), a spectrum for the Robertson-
Berger meter (Robertson 1975), a generalized plant damage spectrum
(Caldwell 1971) and a generalized DNA damage spectrum (Setlow 1974).
The RAF values in Fig. 6 are calculated over the waveband 290-380 nm. For
the DNA and generalized plant damage spectra there would be no significant
effect if the integral included longer wavelengths. For the Hill reaction
and R-B meter spectra, the RAF values would be even smaller if longer wave-
lengths were included in the integration. The deconvoluted Rumex spectrum
-------
91
is unreliable at longer wavelengths. As noted in the previous section,
polychromatic irradiation which did not include wavelengths shorter than
330 nm had no effect on photosynthesis (Figs. 2 and 3). Also shown in
Fig. 6 is a slope indicating a 2% increase of biologically damaging radia
tion for each 1% decrease of ozone column thickness which has commonly been
used as a guideline for the RAF (National Academy of Sciences 1979).
Radiation amplification factors are dependent on the degree of ozone
reduction and this dependency is more pronounced for steeper action spectra
(Fig. 6). The RAF is also quite dependent on solar angle and, thus, RAF
values appropriate for total daily effective radiation would be an inte-
grated function for different times of day. The daily RAF would be
dependent on latitude and time of year (National Academy of Sciences 1979).
The RAF values in Fig. 6 are plotted for a solar angle from the zenith of
33.6* (air mass of 1.2).. For the summer solstice at 40* latitude, these
RAF values would also be approximately the same as total integrated daily
dose RAF values.
3.0
,DNA domoge
2.0
<
er
i.O
~Ol92 O224 0.256 0.288 0.320
Ozone Column (cm)
Fig. 6. Radiation amplification factors calculated for different ozone
column thickness, relative to 0.32 cm, and a solar angle from the zenith of
33.6* calculated according to the action spectra shown in Fig. 5. The
dashed line represents a case of 2% increase in biologically effective
radiation for a 1% decrease of ozone. The model of Green et al. (1980) was
used to calculate the solar spectral irradiance (direct beam + diffuse)
used for those RAF values.
The Natural Latitudinal Gradient of Solar UV-B Radiation
Natural latitudinal gradients of solar UV-P radiation exist on the earth.
This is primarily the result of differences in prevailing solar angles and
total ozone column thickness at different latitudes (Caldwell 1981).
Correlations between the latitudinal UV-B gradient and skin cancer
incidence of selected human populations have been used as a tool to predict
increases of skin cancer as a function of ozone reduction (e.g.. National
Academy of Sciences 1979). An analogous correlation between latitude and
changes in crop yield or other nonhuman biological phenomena are too
confounded with other environmental variables such as soils, temperature
and moisture to be of use in predicting the consequences of ozone reduc-
tion. Nevertheless, controlled study of plant response to, and tolerance
-------
92
of, UV-B irradiation by species from different latitudes can provide some
useful insight as to how plants cope with different levels of UV-B irradia-
tion. However, just as the magnitude of solar UV-B increase resulting from
ozone reduction is dependent on the action spectrum used, the steepness of
the present latitudinal gradient of solar UV-B irradiance is also quite
dependent on the action spectrum used for evaluation.
The effective UV-B radiation for the season of year of maximum solar
radiation at different latitudes is shown in Fig. 7. These are plotted
relative to the radiation at 40* latitude. (The date of maximum solar
radiation at each latitude corresponds to the time when solar zenith angles
are minimal. Above 23° latitude this occurs at the summer solstice, but at
latitudes less than 23*. this time is progressively closer to the equi-
noxes, about March 21 and September 23, which are the dates of maximum
solar radiation at the equator.) Three different action spectra have been
used as weighting functions to illustrate the dependence of this gradient
on action spectrum characteristics. Just as the RAF is greater for steeper
action spectra (Fig. 6), steeper action spectra also result in a more
pronounced latitudinal gradient of solar UV-B irradiance.
1.8
1.6
1.4
o
1 '-2
^ 0.6
o
Q
0.4
0.2
—— DNA damage
Generalized plant damage
Hill reaction
0
10 20
30 40
Latitude
50 60 70
Fig. 7. Daily effective UV-B radiation for the season of year of maximum
solar radiation at different latitudes relative to that at 40* latitude
calculated according to the generalized DNA damage action spectrum (Setlow
1974), the generalized plant damage action spectrum (Caldwell 1971) and the
Hill reaction inhibition spectrum (Jones and Kok, 1966).
If a spectrum has a rather slow rate of decline with increasing wavelength.
-------
93
such as the Hill reaction spectrum, there is no latitudinal solar UV-B
gradient. Thus, study of characteristics of plants that have originated
from different latitudes can provide some indirect evidence of the type of
UV damage action spectrum that is indeed appropriate for plants. For
example, if a spectrum such as the Hill reaction is indeed representative
of the spectrum for UV damage to plants, one might expect little correla-
tion between the latitude of origin of plants and their sensitivity to UV-B
radiation when this radiation is presented at sufficient flux densities to
result in damage.
There are several lines of evidence that suggest that a sufficiently steep
action spectrum for plant damage exists so that an appreciable latitudinal
gradient of solar UV-B radiation has been extant. The first line of
evidence is a correlation between the latitude of origin of crop species
and their sensitivity to UV-B radiation as measured by a reduction of plant
biomass in experiments with UV-B radiation lamps. Over 50% of the crop
species which have originated from temperate latitudes were sensitive to
UV-B radiation in these tests, whereas for crop species that have origi-
nated at low latitudes, only 20% were classified as sensitive (Teramura and
Caldwell unpublished).
The second two lines of evidence are derived from a latitudinal gradient in
the arctic-alpine life zone ranging from sea level locations in the Arctic
to alpine elevations (3000-4000 m) at mid to low latitudes. In this
situation an even steeper gradient should be expected because elevation
above sea level is superimposed on the latitudinal gradient (Caldwell et
al. 1980). A survey of UV optical properties of leaves from nonagricul-
tural, as well as agricultural, plant species has been conducted by
sampling plants in the field at various locations along this gradient and
determining the UV epidermal transmittance of the leaves. Plants occurring
in areas of high solar UV-B radiation, at low latitudes and high altitudes,
exhibited a greater capacity to selectively absorb UV-B radiation in the
upper tissue layers of the leaves (Robberecht et al. 1980). If the selec-
tive pressure for UV absorption in the epidermis of plant leaves were
approximately the same at all locations along this gradient, such as would
be the case if an action spectrum like that of the Hill reaction inhibition
were appropriate for UV-B damage, one would not expect a correlation
between latitude and UV-B filtration capacity of the leaf epidermis.
A third line of evidence involves the inherent differences in sensitivity
of the photosynthetic system to UV-B radiation damage that have been demon-
strated for species of the same genus or even races of the same species
which occur in different locations on the latitudinal gradient of the
arctic-alpine life zone (Caldwell et al. 1982). In these experiments,
plants were cultured under identical conditions in environmental growth
chambers before the sensitivity of their photosynthetic systems to the UV-B
radiation was assessed. Arctic races or species consistently showed much
greater sensitivity to UV-B radiation and this could not be solely attri-
buted to differences in the optical properties of the leaf epidermis. Such
evidence certainly supports the notion that a steeper action spectrum for
photosynthetic damage by UV radiation such as that developed using poly-
chromatic radiation (Fig. 4) would be more appropriate than an action
spectrum such as that for the Hill reaction. Although all three lines of
evidence are circumstantial, they support the notion that an appreciable
RAF exists for higher plants.
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94
Biological Assessments and Errors Deriving from Action Spectra
Before radiation amplification factors can be used in assessment of biolog-
ical and ecological consequences of ozone reduction, it is necessary to
demonstrate biological effects of UV-B radiation. Ideally, one should
establish a dose-response relationship. In any case, it is at least
necessary to show a meaningful response at UV-B flux densities exceeding
those currently in sunlight. (Investigations involving the removal of UV-B
from solar radiation, such as with filters, have generally not resulted in
significant plant responses (Caldwell 1968; Becwar et al. 1982; Caldwell
1981), although there are some notable exceptions (e.g., Bogenreider and
Klein 1977).)
Experiments with lamps; One cannot easily simulate the solar spectral
irradiance either with or-without reduced ozone using UV lamps. Thus,
weighted UV irradiance from the lamp system is compared with weighted solar
UV irradiance as would occur with a particular solar angle, ozone concen-
tration, etc. The most common lamps used are fluorescent lamps which emit
principally in the UV-B region. The spectral irradiance from the most
frequently used bulbs is shown in Fig. 8. As with all fluorescent lamps,
these are basically low pressure mercury vapor lamps with a phosphor that
fluoresces in a continuous spectrum — in this case, mainly in the UV-B
region, but some UV-C and UV-A radiation is included. Though most of the
radiant emission from the bulbs comes from the fluorescing phosphor, the
emission from the mercury vapor is also present and this appears as
distinct lines in the spectrum. The fluorescent lamp manufactured by
Philips Co. emits substantially more than the bulb of Westinghouse.
Filters are commonly employed to absorb the UV-C and short-wavelength UV-B
radiation emitted by these bulbs. Investigators in Europe have commonly
used the Philips bulbs with glass cutoff absorption filters (Schott WG
series) for this purpose, while in North America, cellulose acetate plastic
film has been used with the bulbs manufactured by Westinghouse (Caldwell et
al. 1983). The glass absorption filters have the advantage of being stable
in their transmittance, while the plastic film filters are considerably
less expensive but exhibit decreased transmittance as they are exposed to
UV radiation (Caldwell et al. 1983). The spectral irradiance from filtered
and unfiltered lamps shown in Fig. 8 is provided as a comparison of these
lamp and filter combinations. Naturally, individual lamps will vary in
their emission and, as with all fluorescent lamps, their emission will
decrease with age, especially during the first 100 hours of use, and with
temperatures that are too warm or too cold for optimal operation (Bickford
and Dunn 1972).
If filtered fluorescent lamps are the only source of UV radiation for plant
experiments, the discrepancy between spectral irradiance received from the
sun and that received from the lamps is considerable (Fig. 9a). When
compared with the midday solar irradiance in the summer at temperate
latitudes, a bank of filtered Westinghouse fluorescent lamps provide more
shortwave UV-B radiation and more than an order of magnitude less longwave
UV-B and UV-A radiation. Thus, the action spectrum used to weight the
spectral irradiance for comparison of the lamp systems with solar radiation
is particularly critical as will be demonstrated subsequently.
When such lamp systems are used to supplement the normal solar radiation,
i.e., when plants are exposed both to the solar radiation as well as a
-------
95
120
100
'E
c
'E
*
1 80
60
a.
to
40
20
•Phillips
Westmghouse
Phillips with
WG 305 SchotT
Westmghouse with
cellulose ocetote
film
250 275 300 325 350 375 400
250 275 300 325 350 375 4QO
Wavelength (nm)
Fig. 8. The spectral irradiance at 30 cm from comm.on fluorescent UV-B lamps
with and without filters. The lamps and filters were new and the spectral
irradiance was measured with a double monochromator spectroradiometer
(Optronic Laboratories). The Philips TL 40W/12 and the Westinghouse FS40
lamps without filters are shown on the left and with filters on the right.
Schott W3 305 sharp cutoff absorption filters (2 mm thickness) were used
with the Philips lamp and cellulose acetate plastic film (0.13 mm
thickness) with the Westinghouse lamp. These lamp/filter combinations have
commonly been used in studies in Europe and North America, respectively.
-------
96
1000
600
100
60
20
10
6
G local-
CA-Mtered
lamps
/: ^Myiof-filtered lamps
€ gioDoi
300 12Z
340 360 300 320
340 360 300 320 340 360
(nm)
Fig. 9. Global (direct beam + diffuse) UV spectral irradiance and the
spectral irradiance from filtered lamp systems used in experiments. In the
left panel, a, global spectral irradiance as measured at solar noon on
August 20 at 41* 45' N latitude and 1460 m elevation and the spectral
irradiance from Westinghouse FS 40 lamps with cellulose acetate film
filters (without background global radiation) are shown. The lamp system
is adjusted to provide a UV-B supplement equivalent to a 16% ozone reduc-
tion under these conditions calculated according to the generalized plant
damage action spectrum. In the middle panel, b, the theoretical global UV
spectral irradiance for these conditions, as calculated by the model of
Green et al. (1980), is shown for current ozone conditions as well as
conditions with a 16% reduction of the atmospheric ozone layer. In the
right panel, c, the UV spectral irradiance measured under lamp systems with
cellulose acetate and Mylar film filters with the background global radia-
tion is shown. The Mylar-filtered lamp system provides a control with the
same UV-A irradiance and obstruction of global radiation as the CA-filtered
lamps which constitute the enhancement treatment. The UV-A irradiance in
both treatment and control is less than the ambient global shown in the
left panel because of the obstruction created by the lamps. The UV-B
supplement in the right panel represents the same effective UV-B radiation
as that predicted with the Green ej al. (1980) model when calculated using
the generalized plant damage action spectrum. Adapted from Caldwell et
al. (1983).
supplement from the filtered lamp bank, the discrepancy in spectral distri-
bution is much less. Ideally, the supplemented UV spectral irradiance
would only be that shown as the difference between solar spectral
irradiance under normal conditions and with ozone reduction (Fig. 9b).
Since the filtered fluorescent lamps emit longer wavelength radiation than
is desired for the supplement, it is necessary to use control lamps which
are identical except that they are filtered so as to exclude the UV-B
radiation. Thus, the amount of UV-A radiation provided by the control
lamps would be the same as that coming from the treatment lamps, and the
other microenvironmental influences such as shading by the lamps would also
-------
97
be the same. In Fig. 9c the resulting spectral irradiance under lamp banks
with two different plastic film filters, corresponding to treatment and
control, is shown with the solar radiation background. The difference
between these is still not a perfect simulation of what would be calculated
as the difference between solar spectral irradiance with and without ozone
reduction; however, the correspondence is considerably better than when the
lamps are used by themselves such as would be the case in a glasshouse,
growth chamber or laboratory situation.
Error analysis; There are then two basic types of error that are involved
in use of action spectra as weighting functions in biological assessments
of ozone reduction, namely RAF errors and enhancement errors. The RAF
errors are those resulting from an overestimation or underestimation of the
radiation amplification fac'tors by assuming an incorrect action spectrum.
The RAF errors would be associated with application of dose-response
relationships to the solar UV-B irradiance that would result from various
scenarios of ozone reduction. For example, if a given amount of UV-B
irradiation corresponding to 10% ozone reduction resulted in 5% reduction
of photosynthesis, one would employ the RAF to extrapolate to other ozone
reduction levels for a given latitude and season of year.
The enhancement error is that associated with relating UV-B radiation
supplied by lamp systems in an experiment with solar UV-B radiation for a
particular ozone level. For example, if one desires to provide a UV-B
radiation supplement under field conditions corresponding to a 15% ozone
reduction, and an incorrect action spectrum is used as a weighting factor
for comparing UV irradiance from the lamps and the sun, an error in the
desired enhancement will result. The enhancement error necessarily
includes an RAF error — namely that associated with calculating the effec-
tive UV irradiance corresponding to the 15% ozone reduction.
These two types of error are shown in Fig. 10 for a scenario in which the
generalized plant damage action spectrum (Fig. 5) is employed for calculat-
ing the RAF and the effective UV radiation enhancement when the DNA-damage
spectrum (Fig. 5) is indeed the most appropriate for plant damage. (This
is, of course, hypothetical as the most appropriate action spectrum to
represent higher plant damage is not known.) The discrepancy between RAF
values calculated by the generalized plant damage and DNA damage spectra is
illustrated in the upper portion of Fig. 10. With greater ozone reduction,
which requires larger RAF values, the divergence from the diagonal 1:1 line
increases, i.e., the difference between the RAF values calculated using
the two action spectra increases. This is directly from information
presented in Fig. 6. The differences in UV radiation enhancement in a
field experiment that would result from use of the two action spectra are
shown in the lower half of Fig. 10. In field experiments the lamps are
used to supplement the solar radiation, and a certain amount of obstruction
of the solar global (direct beam + diffuse) radiation inevitably results.
The exact spectral distribution of the radiation reaching the plants in the
enhancement experiments then depends on the mixture of global and lamp
radiation. The relationship in Fig. 10 was determined from actual measure-
ments of spectral irradiance under lamp systems in a field experiment.
Each point represents a combination of the UV radiation from the lamps and
the background global radiation convoluted using the two action spectra.
Relative enhancement is the ratio of the UV-B radiation from the lamps plus
the background global radiation to the ambient global radiation without the
lamp systems for particular conditions. The range of values shown in
-------
98
Fig. 10 results from different experiments in which enhancements corre-
sponding with different levels of ozone reduction and different solar
angles were used. The lamp system is specially modulated so that the
amount of UV supplement is adjusted for particular solar conditions such as
solar angle, atmospheric turbidity, current ozone concentrations, etc.
(Caldwell et al. 1983). A linear regression fits these points adequately
(r2 = 0.96). The discrepancy between relative enhancements calculated by
the two action spectra is greater than the discrepancy between the RAF
values calculated with the two spectra.
For the action spectra represented in this paper (Figs. 1, 4 and 5) and the
filtered UV .fluorescent lamps commonly used, (Fig. 8), the RAF and enhance-
ment errors are in opposite directions as depicted in Fig. 11. These
relative errors are shown as a function of ozone reduction for field
enhancement experiments under temperate-latitude conditions in the summer
as portrayed in Fig. 10. The scenario is the same, namely, that the
generalized plant damage action spectrum was assumed while the DNA-damage
spectrum is correct. Although the relative RAF errors are small for situa-
tions where the ozone reduction is small, this is not the case for the
enhancement errors (Fig. 11).
If a different scenario is pursued such that the generalized plant damage
spectrum is assumed, but a spectrum with a slower rate of decline with
increasing wavelength, such as the R-B spectrum (Fig. 5), is correct, then
the RAF and enhancement errors would be reversed — an overestimation of
the RAF and underestimation of the enhancement.
As shown in Fig. 9, field UV enhancement experiments provide a much closer
simulation of the spectral irradiance resulting from ozone reduction than
do experiments in glasshouses or growth chambers in which UV radiation is
provided only by filtered fluorescent lamps, since there is no solar UV
background. The enhancement errors that might result from use of an
incorrect action spectrum for calculating the enhancement are considerably
greater than for field experiments, as shown in Fig. 12. The spectral
irradiance from filtered Philips and Westinghouse UV fluorescent tubes
following aging of the lamps and filters for about 100 hours was used to
calculate the errors shown in Fig. 12. The same spectral distribution is
assumed for all enhancement levels in such experiments, which is normally
the situation, as doses are typically adjusted by varying the number of
lamps, distance between the lamps and the experimental objects, or use of
neutral density filters. The errors portrayed here are striking,
especially when one considers that the two action spectra used for this
scenario are not so very dissimilar (Fig. 5). Other scenarios could easily
lead to larger overestimation or underestimation errors for the calculated
enhancement. Also, for the errors depicted in Fig. 12 the relative over-
estimation errors are greater at UV levels corresponding to smaller ozone
reductions.
If a source of background UV radiation were present, such as from a xenon
arc lamp, these errors could be substantially reduced. However, this would
depend on the flux density and spectral distribution received from the
background source. An empirical analysis of the errors for particular
situations would need to be conducted. However, without knowledge of the
most appropriate action spectra for plant damage, the error analysis
remains as a heuristic exercise quite dependent on the action spectrum
scenarios assumed.
-------
99
10
1.5 2.0
RAF GEN. PLANT
1.0 2.0 3.0 4.0
Relative enhancement (GEN. PLANT)
Fig. 10. The relationship between radiation amplification factors
calculated with the generalized plant damage action spectrum and the
generalized DNA damage action spectrum for different conditions and levels
of ozone reduction (upper). The relative enhanced UV-B radiation in field
experiments calculated according to the generalized plant damage spectrum
and the generalized DNA damage spectrum for different conditions and levels
of ozone reduction based on field spectral irradiance measurements (lower).
The solid diagonal lines in both graphs represent a situation of equiva-
lence for the RAF and relative enhancements calculated from the two
spectra.
-------
100
40
o
o 30
J*°
S°.o
I0h
-S20
Enhancement error
Ozone reduction (%)
RAF error
Fig. 11. Relative RAF and enhancement errors as a function of ozone reduc-
tion for field UV supplementation experiments under temperate-latitude
conditions in the summer as portrayed in Fig. 10. The scenario for these
errors is that the RAF values and the enhancements were calculated
following the generalized plant action spectrum when the DNA damage
spectrum was indeed correct.
CONCLUDING REMARKS
The potential errors resulting from assuming an incorrect action spectrum
are compelling reasons for further action spectrum development. This
should indeed be pursued. Yet, one should not expect that a single defini-
tive action spectrum for higher plant damage will necessarily be forth-
coming. It is unlikely when one considers the many basic modes of damage
to plant tissues that UV radiation can effect (Fig. 1), the physiological
and morphological diversity of plant species, and the interactions with
other environmental factors, such as visible light, that can ensue.
Extrapolation from spectra of component reactions of isolated organelles to
spectra of higher plant response in nature is precarious as shown for the
case of photosynthetic damage (Fig. 4). Thus, use of intact plant organs
and polychromatic radiation should be emphasized in further action spectrum
development where these spectra bear on the ozone reduction problem. For
damage to higher plant photosynthesis, the provisional action spectrum
developed for Rumex patientia (Fig. 4) as well as circumstantial evidence
from the natural latitudinal gradient indicate that the appropriate action
spectrum is much steeper than the spectra for the Hill reaction. Thus,
contrary to what one might conclude from component photosynthetic reac-
tions, an appreciable RAF exists for damage to higher plant photosynthesis.
More recent preliminary work with polychromatic radiation suggests that the
spectrum may yet be even steeper and, therefore, one should view the Rumex
spectrum presented here as only provisional.
-------
101
200
5 150
g
"5
I 100
0)
O
50
Laboratory -
Phillips * Schott 305
Laboratory ~
FS-40 + CA film
Reid- FS-40*CA film
10 20 30
Ozone reduction (%}
40
Fig. 12. Enhancement errors calculated according to the same scenario as
for Fig. 11, but with enhancement experiments using different lamp systems.
In the field supplementation experiment using Westinghouse FS40 lamps and
cellulose acetate film, the errors are the same as portrayed in Fig. 11.
Under laboratory conditions (which would correspond to glasshouse or growth
chamber conditions with no background UV radiation) the Philips lamps with
Schott WG 305 filters and the Westinghouse FS40 lamps with cellulose
acetate film render the errors depicted. The lamps and filters were aged
for about 100 hours for these measurements.
In our present state of ignorance concerning the most appropriate action
spectra for higher plant damage, we feel it is reasonable to continue to
use an action spectrum with an intermediate rate of decline with increasing
wavelength, such as the generalized plant damage spectrum. An intermediate
spectrum will, of course, yield intermediate RAF and enhancement values.
If the appropriate spectra are later found to be either steeper or flatter,
correction from an intermediate spectrum will be easier to conduct.
-------
1 02
ACKNOWLEDGMENTS
This work has been supported by the U.S. Environmental Protection Agency.
Although the research described in this chapter has been funded primarily
by the U.S. Environmental Protectio*\Agency through Cooperative Agreement
CR808670 to Utah State University, it has not been subjected to the
Agency's required peer and policy review and therefore does not necessarily
reflect the views of the Agency and no official endorsement should be
inferred.
REFERENCES
Becwar MR. Moore FD III, Burke MJ (1982) Effects of deletion and
enhancement of ultraviolet-B (280-315nm) radiation on plants grown at
3000 m elevation. J Amer Soc Hort Sci 107:771-774
Berger D, Robertson DF, Davies RF, Urbach F (1975) Field measurements of
biologically effective UV radiation. In: Nachtwey DS, Caldwell MM, Biggs
RH (eds) Impacts of climatic change on the biosphere, part I, ultraviolet
radiation effects, monograph 5. Climatic Impact Assessment Program, US
Dept Transportation Report No DOT-TST-75-55, NTIS, Springfield, Virginia,
p (2)235
Bickford ED, Dunn S (1972) Lighting for plant growth. Kent State Univ
Press
Bjbrn LO, Bornman JF. Olsson E (1985) Effects of ultraviolet radiation on
fluorescence induction kinetics in isolated thylakoids and intact leaves.
(this volume)
Bogenrieder A, Klein R (1977) Die Rolle des UV-Lichtes beim sog.
Auspflanzungsschock von Gewachshaussetzlingen. Angew Bot 51:99-107
Caldwell MM (1968) Solar ultraviolet radiation as an ecological factor for
alpine plants. Ecol Monogr 38:243-268
Caldwell MM (1971) Solar UV irradiation and the growth and development of
higher plants. In: Giese AC (ed) Photophysiology, vol 6. Academic
Press, New York, p 131
Caldwell MM (1979) Plant life and ultraviolet radiation: some perspective
in the history of the Earth's UV climate. BioScience 29:520-525
Caldwell MM (1981) Plant response to solar ultraviolet radiation. In:
Lange OL, Nobel PS, Osmond CB, Ziegler H (eds) Encyclopedia of plant
physiology, vol. 12A, Physiological plant ecology. I. Responses to the
physical environment. Springer, Berlin, Heidelberg, New York, p 169
Caldwell MM, Osmond CB, Nott DL (1977) C4 pathway photosynthesis at low
temperature in cold-tolerant Atriplex species. Plant Physiol 60:157-164
Caldwell MM, Robberecht R, Billings WD (1980) A steep latitudinal gradient
of solar ultraviolet-B radiation in the arctic-alpine life zone. Ecology
61:600-611
Caldwell MM, Robberecht R, Nowak RS, Billings WD (1982) Differential
photosynthetic inhibition by ultraviolet radiation in species from the
arctic-alpine life zone. Arctic Alpine Res 14:195-202
Caldwell MM, Gold WG, Harris G, Ashurst CW (1983) A modulated lamp system
for solar UV-B (280-320 nm) supplementation studies in the field.
Photochem Photobiol 37:479-485
Green AES, Cross KR, Smith LA (1980) Improved analytic characterization of
ultraviolet skylight. Photochem Photobiol 31:59-65
-------
103
Hirosawa T, Miyachi S (1983) Inactivation of hill reaction by long-
wavelength ultraviolet radiation (UV-A) and its photoreactivation by
visible light in the cyanobacterium, Anacystis nidulans. Arch Microbiol
135:98-102
Imbrie CW, Murphy TM (1982) UV-action spectrum (254-405 nm) for inhibition
of K+-stimulated adenosine triphosphatase from the plasma membrane of
Rosa damascene. Photochem Ftiotobiol 36:537-542
Jagger J (1981) Near-UV radiation effects on microorganisms. Photochem
Photobiol 34:761-768
Jones LW, Kok B (1966) Photoinhibition of chloroplast reactions. I.
Kinetics and action spectra. Plant Physiol 41:1037-1043
Kelland LR, Moss SH, Davies DJG (1983) An action spectrum for ultraviolet
radiation-induced membrane damage in Escherichia coli K-12. Photochem
Photobiol 37:301-306
Luckiesh M, Holladay LL (1933) Fundamental units and terms for
biologically-effective radiation. J Opt Soc Amer 23:197-205
Menezes S, Tyrrell RM (1982) Damage by solar radiation at defined
wavelengths: involvement of inducible repair systems. Photochem
Photobiol 36:313-318
Nachtwey DS, Rundel RD (1982) Ozone change: biological effects.
Stratospheric ozone and Man. In: Bower FA, Ward RB (eds) CRC Press, Boca
Raton, p 81
National Academy of Sciences (1979) Protection against depletion of
stratospheric ozone by chlorofluorocarbons. National Academy Press,
Washington, DC
Noorudeen AM, Kulandaivelu G (1982) On the possible site of inhibition of
photosynthetic electron transport by ultraviolet-B (UV-B) radiation.
Physiol Plant 55:161-166
Peak MJ, Peak JG (1982) Single-strand breaks induced in Bacillus subtilis
DNA by ultraviolet light: action spectrum and properties. Photochem
Photobiol 35:675-680
Peak MJ, Peak JG (1983) Use of action spectra for identifying molecular
targets and mechanisms of action of solar ultraviolet light. Physiol
Plant 58:367-372
Renger R, Voss M, Graber P, Schulze A (1985) Effect of UV irradiation on
different partial reactions of the primary processes of photosynthesis.
(this volume)
Robberecht R, Caldwell MM, Billings WD (1980) Leaf ultraviolet optical
properties along a latitudinal gradient in the arctic-alpine life zone.
Ecology 61:612-619
Robertson DF (1975) The sunburn unit for comparison of variation of
erythemal effectiveness. In: Nachtwey DS, Caldwell MM, Biggs RH (eds)
Impacts of climatic change on the biosphere, part I, ultraviolet
radiation effects, monograph 5. Climatic Impact Assessment Program, US
Dept Transportation Report No DOT-TST-75-55, NTIS, Springfield, Virginia,
p (2)203
.Rundel RD (1983) Action spectra and estimation of biologically effective UV
radiation. Physiol Plant 58:360-366
Sestak Z (1977) Photosynthetic characteristics during ontogenesis of
leaves. II. Photosystems, components of electron transport chain, and
photophosphorylations. Photosynthetica 11:449-474
Setlow RB (1974) The wavelengths in sunlight effective in producing skin
cancer: a theoretical analysis. Proc Natl Acad Sci USA 71:3363-3366
Sharma RC, Jagger J (1981) Ultraviolet (254-405 nm) action spectrum and
kinetic studies of alanine uptake in Fscherichia coli B/r. Photochem
Photobiol 33:173-177
-------
104
Sisson WB, Caldwell MM (1976) Photosynthesis, dark respiration, and growth
of Rumex patientia L. exposed to ultraviolet irradiance (288 to 315
nanometers) simulating a reduced atmospheric ozone column. Plant Physiol
58:563-568
Sisson WB, Caldwell MM (1977) Atmospheric ozone depletion: reduction of
photosynthesis and growth of a sensitive higher plant exposed to enhanced
UV-B radiation. J Exp Bot 28:691-705
Teramura AH, Biggs RH, Kossuth S (1980) Effects of ultraviolet-B
irradiances on soybean. II. Interaction between ultraviolet-B and
photosynthetically active radiation on net photosynthesis, dark
respiration, and transpiration. Plant Physiol 65:483-488
Warner CW, Caldwell MM (1983) Influence of photon flux density in the 400-
700 nm waveband on inhibition of photosynthesis by UV-B (280-320 nm)
irradiation in soybean leaves: separation of indirect and immediate
effects. Photochem Phdtobiol 38:341-346
Webb RB (1977) Lethal and mutagenic effects of near-ultraviolet radiation.
Photochem Photobiol Rev 2:169-261
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105
APPENDIX B
STRATOSPHERIC CHEHISTRY AND NATURE OF OZONE
Stratospheric ozone is the primary attenuator of extraterrestrial solar
ultraviolet radiation and therefore determines the quality and quantity
ultimately reaching the earth's surface. Approximately 95% of the total
atmospheric ozone is found in the stratosphere, a region of the atmosphere
about 16 to 50 km above the earth's surface at low latitudes and about 8 to 50
km at high latitudes. Global stratospheric ozone concentration is maintained
by a balance of various processes that generate and remove it (Figure B-l).
Ozone is formed by a reaction between atomic oxygen (0) with diatomic
molecular oxygen (0.) and the process is initiated by the photolysis of
diatomic oxygen:
0 + hv P 0 + 0 (1)
0 + 02 P 03 (ozone). (2)
The energy required for photolysis is 5.41 ev and is provided by solar
radiation of wavelengths below 242 run. According to figures published by the
National Reseach Council (1982) , photolysis provides a global source of ozone
amounting to 50 billion metric tons per year, with more than 90% of this
formed above 25 km. Approximately 1% of the ozone created in the stratosphere
is removed by transport to the troposphere. The remainder is destroyed by
chemical reactions involving oxygen (0), hydrogen (H), chlorine (Cl), and
nitrogen (N) compounds, with the last three acting as catalysts in very low
concentrations. The net effect of these various reactions is either the
association of ozone with atomic oxygen to form 0_, or the association of two
ozone molecules:
Process I 0+0 P 20 (3)
Process II 0+0 P 30 , (4)
The various reactions in process I are:
Cl + 03 P CIO + 0 (5)
CIO +0 P Cl + 0 (6)
NO + 03 P N02 + 02 (7)
N02 + 0 P NO + 0 (8)
OH + 03 P H02 + 02 (9)
0 + H0 P OH + 0 (10)
-------
106
Fig. B-l. Representation of the processes that determine the concentration of
ozone in the stratosphere (NRG 1982)
-------
107
These reactions are limited by the availability of oxygen atoms, therefore
effectively restricting them to altitudes above 25 km. The regeneration of
oxygen occurs through photolysis of ozone:
03 + hv P 02 + 0. (11)
The reaction schemes in process II where atomic oxygen is not limiting, are:
OH + 03 P H02 + 02 (12)
H02 + 03 P OH + 202 (13)
At altitudes between 25 and 45 km, reaction 7 accounts for approximately
45% of total ozone removal, while reactions 3 and 5 each account for about
20%, and reaction 9 for 10%. Below 25 km, reactions 12 and 13 account only
for 1% (NRC 1982).
In reactions 5 and 7, Cl and NO are not consumed during ozone destruction
because they are regenerated in reactions 6 and 8. A single chlorine atom can
affect the recombination of 10^ to 10 ozone molecules during its mean
residence time in the stratosphere (about 2 years) before returning to the
troposphere mainly as hydrochloric acid (HC1). The average NO molecule is
equally effective during its 2 years of residence in the stratosphere. Thus,
the addition of these substances into the stratosphere profoundly affects the
balance between production and removal process by which the total abundance of
ozone is governed.
To date, approximately three parts per billion (ppb) of the lower
stratosphere consists of Cl bound in organic molecules such as methyl chloride
(CHC1), carbon tetrachloride (CC1 ), and chlorofluorocarbons (CFG). Table
B-l lists the abundance of several prevalent species and their rate of
release. Among these, methyl chloride is known to have substantial natural
origins, while most others are anthropogenic. The global release of CFG-11
and CFG-12 from 1952 to 1980 is shown in Figure B-2. Although the release
rate has decreased by about 20% from the peak rate of 1974, approximately 90%
of all CFC-11 produced has been already released into the atmosphere and about
90% of this amount still remains in the atmosphere today (NAS 1984). The
largest sources of CFCs are the industrial countries of the northern
mid-latitudes, and the greatest concentrations are found over Europe and the
eastern portions of the North America. The Atmospheric Lifetime Experiments
(ALE) stations have been monitoring the concentration of CFC-11, CFC-12, CC1
CH CGI and NO in Ireland, Oregon (USA), Barbados, Samoa and Tasmania.
Overall, there has been a steady increase in the concentrations of CFCs over
the past decade. At altitudes above 20 km, halocarbons decompose in sunlight
to release free chlorine. This free chlorine is converted to inorganic
species including HC1, chlorine nitrate (C1NO ) and CIO. HC1 is the major
reservoir for chlorine at altitudes above 25 km.
The estimated ozone reduction due to changes in the rate of release of
various chemicals is summarized in Table B-2. According to current
theoretical estimates, continuing production of CFCs at rates of 3.1 million
metric tons of CFC-11 and 4.3 million metric tons of CFC-12 annually
(approximately the 1980 production rate) would lead to a steady-state
-------
108
Table B-l. Concentration in the Lower Stratosphere and Release Rates of Major
Sources of Chlorine in the Stratosphere (NRC 1982)
Compound
Concentration (ppb)
Molecular Chlorine
Rate of Release
(million metric
tons of Cl per year)
Methyl
chloride
(CH
F-12 (CF0Cln)
F-ll ((
Carbon
Methyl
/ /
0
J
tetrachloride
chloroform (C
Cl)
-------
109
400
200
S 200
3
Z
z
100
1960
1970
1930
YEAR
Fig. B-2. Estimated annual worldwide releases of CFC-11 and CFC-12, 1952-1980
NAS (1984).
-------
110
Table B-2. Sensitivity of Total Column Ozone to Perturbing Influences
(NAS 1984)
Trace Gas and Magnitude of
Perturbation
Typical
Estimate
of Ozone
Column
Change
Atmospheric
Lifetime
(years)
Principal Mode of
Pollutant Removal
CFG-11 and -12
(1980 release rates)
Other halocarbons
(2 ppbv Cl increase)
Subsonic aircraft
(2 x 10 kg
N02/yr @ 12 km)
N20 (20% increase by 2050)
CH (doubling)
CO (doubling)
-2 to -4
-1
+1
-4
+3
+3 to +6
50-150
1-15
100
10
Photolysis of CFCs
in middle stratosphere
Decomposition of
tropospheric chloro-
carbon reservoir by
reaction with OH
Conversion to nitric
acid and removal to
surface
Photolysis in
stratosphere
Reaction with
tropospheric OH
Uptake by oceans,
sediment, and biosphere
* Ozone column change (steady-state) was estimated using 1-D photochemical
models.
-------
Ill
reduction in the total column of ozone of 2-4% (NAS 1984) . These
calculations, however, were performed with a highly restrictive set of
physical and chemical parameters and did not include temperature feedback. In
the stratosphere, temperature increases with altitude due to the ozone
absorbance of UV radiation. When temperature was included in the
calculations, the reduction in the ozone column was computed to be 3-5%.
There have been many attempts over the past decade to estimate the
magnitude of ozone change due to continuous CFG release. As seen in Figure
B-3, there have been wide variations in the estimate of the magnitude of ozone
reduction. Recently, there has been a trend toward lower calculated changes.
In many ozone pertubation estimates, the release of CFCs is assumed to remain
constant for 100 to 200 years, producing an eventual steady-state condition.
However, this may not be true of future, long-term trends (as shown in Figure
B-2) of worldwide release of CFCs. Wuebbles (NAS 1984) calculated a
time -dependent ozone depletion for 18 halocarbon release scenarios (Figure
B-4) . In the scenarios projecting variations in CFG release rates by as much
as 3% per year, the non steady- state total ozone reductions by the year 2030
ranged from 3% to 9%. With a 3% increase in CFG releases, however, the total
ozone change falls precipitously beyond this date. These calculations
demonstrate that the growth and decay of halocarbons occur over long time
scales and that ozone depletion is very sensitive to growth in the rate of
chlorine emissions.
A decade ago projections of large fleets of supersonic aircraft (SSTs)
flying at altitudes of 20 km raised the concern over large-scale stratospheric
ozone depletion due to the injection of nitrogen oxides (Johnston 1971).
However, an economical SST system has not materialized and apparently will not
be developed during this century. Nitrogen oxides are currently emitted into
the lower stratosphere and upper troposphere (below 13 km) by subsonic
commercial aircraft. At relatively low altitudes, photochemical reactions of
NO in the presence of hydrocarbons generate small amounts of ozone (by an
estimated 1%). However, large injections of NO at altitudes above 17 km
could result in large reductions in stratospheric ozone. Global nitrous oxide
concentrations appear to have increased by 2.7% over the past 16 years (from
292 ppb in 1964 to 300 ppb in 1980) . It is likely to further increase with
increases in emissions associated with agricultural activities, disposal of
human and animal wastes, and possibly combustion (NAS 1984). The
stratospheric decomposition of NO into NO occurs mainly in the middle
stratosphere (between 20 and 40 km). In tSis region, catalytic ozone
destruction by NO is extremely efficient and therefore increases in N 0 will
result in decreases in stratosphere ozone. A 20% increase of N 0 by the year
2050 could decrease ozone concentrations by 4%. This could be expected if the
currently observed rate of increase of NO concentrations were to continue
over the next 100 years. However, it has been suggested that such reductions
may be masked to some extent by increases in tropospheric ozone attributed to
subsonic jets and urban smog (NAS 1984).
Methane (CH^) concentrations in the atmosphere are currently estimated to
be increasing at a rate of 2% per year. Methane converts ozone -reactive
chlorine atoms into HC1, which does not affect 0 directly. Hence, an
increase in CH^ leads to a decrease in free chlorine, with a resultant
reduction in ozone catalysis. Photodecomposed products of CH also interact
-------
112
20
10
z
5
I
1974
1975
i
f
IMPROVED Cl
i
1
1976 1977 1978
1
H
CHEMISTRY
MOLINA »
ROWLAND
SLOW
NO » HO2.
DIURNAL
Avg'g
1979
t
1
1930 1981
i
t
TEMPERATURE
FEEDBACK
OH * HO_. HO. * 0
j j
CION02 ' HQc,
t
OH » HN03
FAST HOj.
1 1
1982
NO
OH * H°2 Rev.s.d HO
1983
FAST
CIO » NO2
SLOW
CIO ' 0
REDUCED
Fig. B-3. Estimates of steady-state reductions in total column ozone for
continuous releases of CFCs at approximately 1975 rates as
calculated from different chemical models. Changes in the models
and simulation techniques are indicated in chronological order
(adapted by NAS (1984) from Turco 1984).
-------
113
V
o
o
c
i,
m
0
8
6
4
2
0
-2
-4
-6
-8
-10
-12
-14
-16
CLC growth raw
Scenario 1980-2000 2000-
IV +3%/year +3%/year
V
VI
0%/year
- 3%/year
1980 2000 2020 2040 2060 2080 2100
Year
Fig. B-4. Time dependence of total column ozone calculated for several
scenarios of CFG releases using 1982 chemistry. Calculations using
more recent chemical models would yield smaller reductions in total
ozone. (NAS, 1984)
-------
114
with NO to produce ozone. If CH, concentrations were to double those of
current values, the total ozone column could be increased by approximately 3%
(NAS 1984).
Carbon dioxide (CO-) provides the dominant heat sink for the middle
atmosphere through the emission of infrared radiation into space. Changes in
CO. concentration can alter the heat balance and temperature of the
stratosphere and thereby the rates of basic chemical reactions. An increase
in CO, concentration lowers stratospheric temperatures and leads to increases
in ozone concentrations. Current estimates of the net perturbations of
stratospheric ozone resulting from a doubling of atmospheric CO- are between
3% and 6% (NAS 1984).
It is evident from the above discussion that the effects of individual
gases differ, some causing reductions in the total ozone column (CFCs,
stratospheric NO , CH,, N~0) and others leading to net increases (tropospheric
NO , CH,, CO-). when the concentrations of these gases change simultaneously,
the net effect on 0- may be quite complex. Few recent models have reported
effects of the combined releases of several compounds on the stratospheric
ozone concentration. Wuebbles (NAS 1984) estimated the time-course change in
ozone corresponding to a combination of emissions. This scenario assumes that
1) release of CFCs, CH CC1 and CC1 (designated CLC) is constant at 1980
levels; 2) N_0 increases at 0.2% per year; 3) CO- increases at 0.6% per year;
4) aircraft emissions of NO below 13 km increase by a factor between 5 and 6
from 1975 to 1990 and remain constant thereafter; and 5) there is a constant
flux of CH at the earth's surface. According to this scenario, there will be
a fraction of a percent increase in the total column ozone by the year 2050.
Atmospheric and Environmental Research (AER) and Du Pont (NAS 1984) have also
calculated ozone depletion using scenarios for CLC, CO N-0 and NO similar
to those used by Wuebbles, but with more recent chemistry and variable fluxes
of CH4 (AER 1.2; Du Pont 1.5%). If CFC releases are doubled by 1980, and CH4
release is constant, there would be 2% decrease in ozone concentration by the
year 2050; if CH, release increases, ozone concentration would increase by 4%.
Brasseurl and Rudder (1984) have recently studied the sensitivity of the
ozone layer to several chemical agents, individually and in coupled scenarios.
The results are presented in Table B-3. The CFC perturbation (P) corresponds
to a constant emission of CFC1 (3.4 x 105 T/year), CF Cl (4.1 x 105 T/year),
CC14 (1.0 x 105 T/year), and C^CCl (3.6 x 105 T/yearJ. For other species
(C0_, N_0 and CH,), current concentrations were doubled. They also considered
temperature feedback in the model, and the simulations were made with
presently adopted chemistry. The results show that the ozone depletion due to
CFCs lies between 3% and 3.5%, whereas for NO it lies between 7.8% and 8.9%.
A combination of different sources results in an ozone reduction of 1.3% to
6.8%. Compared to reports by NAS (1984), the computations made by Brasseurl
and Rudder (1984) indicate a larger influence of nitrogen-containing compounds
and a smaller influence of CFCs. They attribute this difference to a smaller
calculated value in OH radicals as a result of revisions in the reaction rates
involved in the odd hydrogen destruction. This exemplifies the sensitivity of
simulation models to revisions in reaction rates. These computations show
that future ozone changes associated with CFCs may be drastically altered when
other perturbing effects are included, and that the net ozone change may be
extremely difficult to detect, since counteracting effects tend to reduce the
perturbation signal in total ozone.
-------
115
Table B-3. Perturbation of the Ozone Column (Brasseurl and Rudder, 1984)
Case
A
A'
B
C
C'
D
D'
E
F
F'
G
CO NO CH CFCs
P*
P
x 2
x 2
x 2
x 2
x 2
x 2 P
x 2 x 2 P
x 2 x 2 P
x 2 x 2 x 2 P
Temperature
Feedback
Yes
No
Yes
Yes
No
Yes
No
Yes
Yes
No
Yes
% Change
in
Ozone
-3
-3
+3
-7
-8
+0
+0
-1
-5
-6
-3
.50
.37
.14
.79
.92
.97
.87
.30
.56
.84
.06
*
Emission of CFCs.
-------
116
These models are severely limited because of the uncertain reliability of
assumptions about release rates over many decades, photochemical processes and
rate coefficients, and radiative-dynamical effects and interactions (NAS
1984). Schmailzl and Crutzen (1984) modelled the distribution of various
ozone-destroying catalysts and the resulting ozone loss as a function of
altitude, latitude, and season using recent photochemistry. They found a
large imbalance in the ozone budget, with additional ozone destruction above
29 km and additional production below 29 km. They suggest this to be due to
errors in reaction rate coefficients, in the source gas distribution, in the
solar fluxes, and in other deficiencies in understanding stratospheric
photochemistry. Until such inconsistencies are resolved, there will continue
to be a high degree of uncertainty associated with our predictions of future
changes in stratospheric ozone concentration.
-------
117
APPENDIX C
EFFECTS OF ULTRAVIOLET-B RADIATION ON
THE GROWTH AND YIELD OF CROP PLANTS
By
Alan H. Teramura
(from Physiol Plant 58:415-427, Copenhagen 1983)
-------
PHYSIOL. PLANT. 58: -415-427. Copenhagen 19H3
Effects of ultravioIet-B radiation on the growth and yield of
crop plants
Alan H. Teramura
.»'/
I erunuira. A. II 19X3 Hllects of ultraviolet-B radiation on the growth and yield of
crop plants. - Physiol. Plant. 58' 415-127
I Ins paper roicws growth chamber, greenhouse, .mil lii.li) studies on ilie elkils ol
ullraviolet-B (UV-B. between 2X0 and 320 inn) radiation on agricultural crop plains
Our understanding of the physiological effects of UV-B radiation comes primarily
from growth chamber studies, where UV-B is artificially supplied Ma liltered lamps
Both photosystems I and II. as well as carboxvlaung cn/ymes. are sensitive to UV-B
radiation. Ullraviolcl-B radiation also aftects stomaial resistance, chlorophyll con-
centration, soluble leaf proteins, lipids. and carbohydrate pools In general, ihe ef-
tects of UV-B radiation are accentuated by the low levels ol visible radiation typically
found inside growth chambers.
Ultravtolet-B radiation has also been shown to alfect ,in;itomical and morphological
plant characteristics. Commonly observed UV-B induced changes include plant
stunting, reductions in leaf area and total biomass, and alterations in the pattern ol
biomass partitioning into various plant organs. In sensitive plants, evidence of cell
and (issue damage often appears on the upper leaf epidermis as bron/mg. gla/ing.
and chlorosis. Epidermal transmission in the UV region decreases in irradiated
leaves. This decrease is primarily associated with a stimulation in llavnnoiit biosyn-
thesis and is thought to bo a protective, screening response to the deleterious elletis
of UV-B. A considerable degree of variability exists in sensitivity to UV-B radiation
between different species. Approximately 30% ot the species tested were resist.mt,
another 20'!'o were extremely sensitive, and the remainder were of intermediate
sensitivity, in terms of reductions in total dry weight In addition to this >,i7.ibie
interspecific variability, there appears to be a similarly wide intraspecilic variability in
UV-B response.
The effects of UV-B radiation on crop yield have only been examined in a limited
number of field studies, with ambient levels of UV-B radiation being supplemented
with fluorescent sun lamps. Due to various deficiencies, all these field experiments to
date have only limited utility for assessing the potential impact of enhanced levels of
UV-B on crop productivity.
A. H. Teramura, De-pi of lloiiinv, Univ of \tar\ltiiul. College Park. Ml) 2U742,
U.S.A.
This paper is part of the contribution to tbe Intern.ilional Workshop on the Ellccts of
Ultraviolet Radiation on Plants, held in Delhi. India. 1-5 November. 19X2.
Table of contents
Abstract 415
Introduction 416
Physiological and biochemical effects 416
Photosynthetic processes 416
Dark respiration 418
Stomata 4|X
Photosynthetic pigments 4IK
Lipids and carbohydrates 419
Non-photosyntheltc pigments 419
Ion transport 420
Morphological and anatomical effects 42<>
Leaf area and specific leaf weight 420
Received 16 December. 1982; revised 15 March, 1983
27 Phvjiol Plan!
-------
Bronzing, glazing and chlorosis 421
Plant stunting 421
Dry matter production and allocation 421
Crop yield 4?3
Response differences to UV-B radiation 424
Interspecific dillerences 425
Intraspecilic dillerences 425
References
I .ill I Major world liKid crops and production (loud and
Agriculture Organization
Crop
Introduction
During the past decade, there has been considerable
concern over reductions in stratospheric o/one con-
centration resulting from man's activities. Since stratos-
pheric ozone is the primary attenuator of solar ul-
traviolet radiation, such a reduction would result m an
increase m ultraviolet radiation reaching the earth's
surface. Cunent estimates of ozone depletion during
the next century range between 5 and Wo (National
Academy of Sciences 1982). Atmospheric attenuation
of solar radiation is wavelength dependent, therefore
the anticipated spectral irradiation changes would occur
within a relatively narrow waveband in the ultraviolet-13
(UV-B) region (between 28U-320 nm). Even under an
unlikely 4U"/o global ozone reduction (Green et al.
1974, 1980) radiation of shorter wavelengths (UV-C,
20(1-280 nm) would not penetrate the earth's atmos-
phere. Furthermore, since the ozone absorption coeffi-
cient is very low at longer wavelengths, UV-A radiation
(320—100 nm) is also virtually unaffected by changes in
stratospheric ozone concentration (Caldwell 1981). The
intent of this article is specifically to review the effects
of enhanced UV-B radiation on agricultural crops, as a
result of ozone depletion.
For the purposes of this review, the term "crop" re-
fers to an agricultural plant species that is either culti-
vated or domesticated tor harvest. Putting this into
perspective, there are over 350 000 species of plants in
the world and over 80 000 ot these are edible.
Nevertheless, only about 3 000 are harvested by man
and used for food (Miller 1982). Currently, only about
80 plants species have been domesticated (Ehrlich et al.
1977), and ot these only 15 spectes supply nearly all the
food calories and three-fourths of the protein to the
world (Tab. I). Three members of the Poaceae, rice,
wheat and corn supply two-thirds of these calories and
one-half of the protein.
A summary of the effects of UV-B radiation on the
physiology and growth of crops is presented in Tab. 2. A
brief description of these effects and generalities drawn
from specific studies follows below.
Abbreviations - UV-A. ultraviolet radiation between 32(1 and
400 nm; UV-U. ultraviolet radiation between 280 and 320 nm:
UV-C. ultraviolet radiation between 200 and 280 nm; PAK.
photosynthetically active radiation between 400 and 700 nm;
Production Crop
(It)6 metric
tons)
Production
C f reals
rice
wheat
corn
sorghum
barley
Legume* l/>u/*e*l
sovbean
peanut
bean
4|1
45X
451
72
I5K
KK
IV
42
Smw <.rtii>*
sugar c.inc
sug.ir heel
Root < r(i[>\
sweet potato
cassava
1 rev ( rti/x,
coconut
banana
nuts
775
2SI
I4(S
127
17
4
PS 1. photosystem 1; PS II. photosystem II; d, plants with
ribulose-bisphosphate earboxylase-oxygcnase as primary car-
boxyladng enzyme; Cj. plants with phosphoenol-p>ru\ate car-
boxylase as primary carhoxylating en/yme: KuUPcase,
ribulose-l.S-bisphosphate carboxvlabe-oxvgenase. R. red
radiation, FR. tar-red radiation. SLW, specihc leaf weight
Physiological and biochemical effects of UV-B
radiation
Ultraviolet radiation can affect the carbon balance of
crops in at least 4 different ways by allccting: I) the
primary photochemical events and electron transport
reactions, 2) the dark reactions fixing carbon into re-
duced compounds, 3) dark respiration, and 4) stomatal
resistance.
Pholosynthetic processes
Although there are large species differences in sen-
sitivity, UV-B radiation generally results in reductions
in net photosynthesis. These reductions are paralleled
by decreases in Hill activity in crops such as pea (PiMini
\aiivum L; Brandle et al. 1977, Gurrard et al. 1976,
Van et al. 1977), collard (BrtiMica oleraceae L. cv.
acephala; Van et al. 1977, Basiouny et al. 1978), and
soybean (Glycine max (L.) Merr; Basiouny et al. 1978,
Vu et al. 1981), indicating the sensitivity of photosys-
tem II (PS II) to UV-B radiation. Both Brandle et ai.
(1977) and Van et al. (1977) concluded that although
cyclic photophosphorylation (PS 1) was also somewhat
sensitive to UV-B radiation, the primary effect involved
PS II. In a study of the etlects of UV-B radiation on
several C., and C4 crops. Basiouny et al. (1978) found
that C, species were generally more sensitive than those
with the C4 photosynthetic pathway. This sensitivity
among other factors, was associated with significant re-
ductions in Hill activity. However, in peanut (Arm/us
tiypogaea L.), a "resistant" C, species. Hill activity was
416
I'hyuul I'Unt 5H. IVKJ
-------
T.ih 2 A summ.irv of the eltects ot UV'-B radiation on crop growth.
A
elfects
I I'lioiiisynthcMs
Hill reaction
f-.lcctnin transport
KuUI' carhoxyl.ise
I'EI' caihoxylase
Dark respiration
Slomuta
Pholosynthctic pigments
2 Soluble proteins
1 Lipids
4 Carbohydrates
5. Noii-pliolosynthetic pigments
6 Plant hormones
7 Ion transport
II Morphological/anatomical effects
I Leat area
2. Specific leaf weight
i Epidermal transmission
4 Uron/mg gla/mg/chlorosis
5 Seedling growth/stunting
6 Dry mutter production/allocation
7 Yield
C Response differences
I. Interspecific (species differences)
2 Intruspecific (culuvar differences) ~
t) Environmental interactions
1 Visible radiation (pholoprotection)
2. Water stress
References*
I, 4. 5, 1. Id, 11, 12, 18, 32, 37, .18,
40. 41, 43, 44, 45, 47, 4H. 49, 55
I. 5, 12, 20. 38. 41, 44, 49
12, 44
I. 20, 38, 44, 46, 47, 48
47
12. 18, 37, 40
7, 12. 37, 39. 40
I, 5, 16. 18, 20, 38, 40, 41, 42, 46,
48, 49, 55. 56. 57
1,5. 16. 18. 20. 38, 40, 41, 42, 46,
47, 48. 49, 57, 58
IK, 41, 42. 57
2. 18. 20
3, 7, 15, 16, 30, 31. 32, 38, 41, 42
51. 52, 53, 54, 55. 56. 57. 5H
15, 51, 52, 53
3,6
3, 5. 8. 9, 16. 32, 36. 37, 38, 39,
41, 42, 48, 50, 57, 58
H, 9, 37, 48
6. 19. 30, 31, 55
1, 3, 6, 7, 8. 9, 21, 30, 39, 40, 41
42. 46, 47, 48. 49, 50, 56
3, 5, 8. 9, 21, 32, 36, 37, 38, 39,
41, 42,46,49, 50. 51, 54, 56, 57
5,6.8,9, 14, 16, 18, 21, 22
36, 37, 41, 42, 43, 45, 49, 50, 56, 57
2, 4, 8, 18. 22
I. 2,4, 5, 6, 7, 8, 10, 14, 16,
IK, 2d, 21, 22, 30. 36, 39, 41,
42, 43, 44,45, 46,47, 50, 51.
54, 55, 56, 57, 58
3, 7, 8, 9, 16. 50
7, 35. 36. 40, 45
37, 39, 58
I. Allen etal. 1978; 2. Ambler et al. 1978; 3. Ambler etal. 1975; 4. Bartholic et al. 1975; 5. Basiouny et al. 1978; 6, Benedict
1934; 7 Bennett 19X1; X Biggs and Kossuth 1978; 9. Biggs et al. 1981; 10. Bogenneder 1982; if Bogenneder and Klein
1978; 12 llrjiullc el al. 1977; |4 Caklwell et al. 1975; 15. Orumm-Hcrrel and Mohr 1981; 16 Dumper! and Boscher 1982:
18 Esser I9MO; 19 Oausman el al. 1975; 20. Garrard el al. 1976; 21 Kri/ek 1975; 22 Hart etal 1975.3(1 Robberccln jnd
Cdklwell 1978; 31 Robberecht et al. 1980; 32. Sisson 1981; 35. Teramura 1982; 36 Teramura I9NO-.37 Teramura and Perry
1982; 38. Teramura and Caldwell 1981; 39. Teramura et al. 1983; 40. Teramura et al. 1980. 41 Tevmi and Iwanzik 1982, 42.
levimetal. 1981,43. Van et al. 1975; 44. Van et al. 1977; 45. Van et al. 1976; 46. Vu et al. 1983; 47 Vu et al. 1982a; 48. Vu
et al. !982b; 49. Vu et al. 1981; 50. Vu et al. 1978; 51. Wellmann 1982; 52. Wellmann 1975; 53. Wellmann 1971; 54
Chassagne et al. I981a, 55. Chassagne et al. 1981b; 56. Hashimoto and Tajima 1980; 57. Tevim et al. 1982; 58. Tevim et al.
1983.
unaffected by UV-B radiation. Similarly, Hill activity 1977, Sisson and Caldwell 1976, Teramura et al. 1980,
was unaffected in all the resistant C4 species.
Reductions in net photosynthesis were also coinci-
dent with ultrastructural damage to chloroplasts in pea
(Brandle et al. 1977) and soybean (Allen et al. 1978).
Disruption of the membrane structural integrity par-
tially damages components necessary for both light and
dark reactions of photosynthesis. High UV-B irradiance
also significantly increases mesophyll (residual) resis-
tance to carbon dioxide and thereby limits net photo-
synthesis in a number of plant species (Nrandle et al.
Teramura and Perry 1982). This resistance term in-
cludes resistance associated with both electron transport
and carboxylation reactions in photosynthesis (Jarvis
1971, Nobel 1974).
Tevini et al. (1981) reported large increases in sol-
uble leaf proteins in barley (Hordeum vulgare L.), corn
(Zea mays L.), bean (Phaseolus vulgaris L.) and radish
(Raphanus sativus L.) grown and exposed to a high
UV-B radiation dose. The authors indicated this might
be a reflection of increased synthesis of aromatic amino
I'hynol HUnl. 5H. IVKJ
417
-------
acids, the precursors for flavonoid biosynthesis. In an
outdoor field experiment, Esser (1980) also lound thai
soluble leaf proteins in potato (Solatium tuberowm L.),
radish, bean, and spinach (Spinacia oleraceu L.) in-
creased with increasing UV-B irradiance. However, for
plants grown under low levels of visible radiation,
UV-B radiation has also been shown to be effective in
decreasing total soluble leaf proteins m sensitive crops
(Basiouny et al. 1978. Vu et al. I982a, b). Due to the
disparate nature of these studies, these contrasting
findings may be the result of differences in experimental
conditions, the UV-B irradiance employed, or the re-
flection of species response differences to UV-B radia-
tion. Vu et al. (I982a) found that total soluble leaf
proteins on a tresh weight basis increased after UV-U
irradiation in tomato (Lvcopersicon esculemum Mill.)
and corn, but was reduced in soybean and pea. Addi-
tionally there is evidence that UV-B radiation increases
soluble leaf proteins only during early leaf development
in soybean, and decreases thereafter (Vu et al. 1982b).
Since as much as 50% of the total soluble leaf pro-
teins may be in the form of the major Cj carboxylating
enzyme, RuBPcase (Stemback 1981), a reduction in
leaf protein may be a reflection of a decrease in car-
boxylating enzyme concentration. Increasing UV-B
radiation produced reductions in RuBPcase activity in
4-week-old soybean and pea, and in 8-week-old tomato
in shaded (0.22-0.25 mmol m"2 s~' photosynthetically
active radiation, PAR) greenhouse experiments (Vu et
al. I982a, h). Although net photosynthesis in pea and
cabbage (Hrai\ica olcniceae L. cv. capitata) had been
shown to be sensitive to UV-B radiation (Van et al.
1976), Garrard et al. (1976) found no significant differ-
ences m RuBPcase activity in these same crops. This
apparent discrepancy may be the result of differences m
UV-B irradiance or due to different growth conditions.
It is now well documented for a number of plant species
that net photosynthesis is more sensitive to UV-B
radiation when plants are grown under low levels of
visible radiation (Sisson and Caldwell 1976, Teramura
et al. 1980, Teramura 1982). Recently Vu et al. (1983)
examined the ctfocts ot UV-B radiation on RuBPcase
concentration and activity in greenhouse-grown pea and
soybean. They lound that high UV-B irradiance, cor-
responding to a 36% decrease in stratospheric ozone
concentration, reduced RuBPcase activity by as much as
40-60% of Mylar control levels, and that this reduction
was due to a decrease in the amount of carboxylating
enzyme present, and not due to enzyme inactivation.
Dark respiration
The carbon balance of crops can also be affected by
changes in dark respiration. After only 5 h of UV-B
irradiation, dark respiration was significantly greater in
pea exposed to a moderate UV-B irradiance (Brandle
et al. 1977). Sisson and Caldwell (1976) found that dark
respiration was increased after only 2 days of moderate
UV-B radiation in Rnniex />atienria L., a very UV-B
sensitive herbaceous plant. In soybean, however,
Teramura et al. (1980) found that dark respiration was
unaffected by low UV-B irradiance under a range of
different PAR growth conditions. With the paucity of
information available, it cannot be concluded that dark
respiration in sensitive species is generally affected by
UV-B radiation. Furthermore, no conclusive data exist
on the effects of UV-B radiation on photorespiration in
crop plants, other than some preliminary studies by
Esser (1980).
Stomala
Net photosynthesis can also be limited by the diffusion
of carbon dioxide entering the leaf through the stomata.
Although net photosynthesis was significantly reduced
after 4 h of UV-B irradiation in pea, stomatal resistance
was unaffected (Brandle et al. 1977). Stomatal resis-
tance, accounting for 10-20% of the total leaf resis-
tance to carbon dioxide in soybean, was increased after
a 2-week exposure to relatively low UV-B irradiance
(Teramura et al. 1980). Bennett (1981), using high
UV-B irradiance in greenhouses and growth chambers,
found small increases in stomatal resistance for bean,
soybean, and cucumber (Cttcumis sativus L.), which
coincided with significant reductions in net photosyn-
thesis. He also found that adaxial stomatal resistance in
one bean cultivar was somewhat more sensitive to
UV-B radiation than abaxial stomata. In a growth
chamber study on cucumber and radish, Teramura et al.
(1983) found thut moderate levels of UV-B radiation
produced only small increases in stomatal resistance m
radish after 12 days exposure, but had dramatic effects
on cucumber. After only 1 day of irradiation, adaxial
stomatal resistance in cucumber increased by 3-fold and
remained high for 8 or 9 days, and then dramatically
decreased. By this time, cucumber had apparently lost
stomatal function as evidenced from diurnal studies on
stomatal response to water stress.
Photosynlhetic pigments
The photostability of chlorophylls has also received
considerable attention. Basiouny et al. (1978) found
that reductions in total dry weight and net photosyn-
thesis were paralleled by reductions in total chlorophyll
concentration m collard, oats (Avena saliva L.), and
soybean (C3 species sensitive to UV-B radiation).
Meanwhile, chlorophyll concentration m resistant C3
and C4 species was unaffected. They found no selective
differences in the chlorophyll a OT b concentration of
sensitive plants. High UV-B irradiance in combination
with low PAR growth levels produced significant re-
ductions in chlorophyll concentration m bean and cab-
bage (Garrard et al. 1976), pea (Vu et al. 1983). soy-
bean (Vu et al. 1983, 1982, 1981), bean, barley, and
corn (Tevini et al. 1981). In general, these studies indi-
cated that the degree of chlorophyll destruction was a
418
Physiol Plant 58. 1983
-------
function of UV-B irradumcc, and that although less af-
lected, c.imlenotds responded similarly. The effects of
UV-U radiation on chlorophyll a/h ratios differed
somewhat between studies and therefore could reflect
species differences. Vu el al. (I9HI) reported that
chlorophyll alh ratios decreased with increasing UV-B
irradiance m soybean, but increased in pea at high UV
irradiance (Vu et al. I9K3). Tevini et al. (1981) con-
cluded that high UV-B irradiance inhibited the biosyn-
thesis of chlorophyll b more than a, since alb ratios
increased in bean, barley, radish, and corn. In contrast,
when soybean was grown under a range of PAR growth
regimes in combination with low and moderate UV-B
irradiance, there appeared to be no effect on total
chlorophyll concentration, despite large effects on net
photosynthesis (Teramura et al. 1980). In fact, when
soybean leaves were expanded under 0.75 mmol m~2 s~'
PAR and moderate UV-B irradiance, there was an ap-
parent stimulation in chlorophyll biosynthesis (Tera-
mura and Caldwell 1981). In a field experiment, Esser
(1980) found that chlorophyll concentration decreased
in bean and increased in spinach under high UV-B ir-
radiance while potato, barley and radish were unaf-
fected. The reason for a reduction in chlorophyll and
carotenoid concentrations after UV-B irradiation is still
unclear. It could be the result of an inhibition of
chlorophyll biosynthesis, or due to the degradation of
these pigments or their precursors. Due to the large
differences both in growth and treatment conditions,
more studies are necessary to determine whether these
differential responses are species specific or artifacts of
the experiments themselves.
I.ipids and carbohydrates
A combination of low PAR and high, continuous UV-B
irradiance produced large reductions in the total lipid
content of corn and bean seedlings after only 5 to 10
days. Higher irradiance also reduced lipid concentra-
tions in barley (Tevini et al. 1981). It appears from this
study that UV-B radiation has a differential effect on
various membrane systems. The galactolipids, which are
principally found in chloroplasts, were greatly reduced
in barley, corn, bean, and radish seedlings. This was also
paralleled by large decreases in chlorophyll concentra-
tion in these crops. Shifts in specific galactolipid con-
centration were noted to be similar to the pattern found
during tissue senescence. Changes in the phospholipids,
which occur in generally all membranes, were seen in
bean and corn, but not in barley or radish. Under field
conditions, Esser (1980) found that total lipids in-
creased in bean and cabbage, decreased in spinach, and
were unaffected in potato grown under unfiltered UV
lamps. Due to the unnatural conditions under which the
plants were grown and irradiated, however, further in-
terpretation of these two studies must be made with
caution. Further work is needed to substantiate these
observations.
In growth chamber studies, Garrard et al. (1976)
found that high UV-B irradiance produced substantial
reductions in the major carbohydrate components of
tomato, cabbage, and collard while it had little effect on
peanut and corn. UV-U radiation quantitatively af-
fected reducing sugars, sucrose, starch, and non-struc-
tural carbohydrates. Of the five crops tested, tomato
was the most adversely affected in each case. In a field
study using unfiltered lamps. Ambler et al. (1978)
found that massive UV enhancements resulted in a
17-20% increase in sugar beet (Beta vulgaris L.) root
sucrose, despite reductions in shoot dry weight and root
fresh weight. In another field experiment, low supple-
mental UV-B irradiance was supplied by sunlamps fil-
tered with Schott WG 305 cut-off filters, and high ir-
radiance (UV-B and UV-C) was supplied by unfiltered
lamps (Esser 1980). Under these conditions, reducing
sugars and starch were only reduced under the unfil-
tered lamps in spinach and radish, while bean showed
slight increases in these carbohydrate pools. Once more,
these studies indicate that UV-B radiation is most ef-
fective when PAR is low during growth.
Non-photosynthetic pigments
The attenuation of UV-B radiation by outer leaf tissue
layers is one means of reducing the UV-B flux received
at potentially sensitive sites. This may represent an
adaptive response to UV-B radiation. In a survey of
epidermal transmission of nearly 70 native plants
(Gausman et al. 1975, Robberecht and Caldwell 1978,
Robberecht et al. 1980), it was found that epidermal
transmission in the UV-B waveband was generally be-
low 10%. Furthermore, epidermal transmission was
lowest for plants growing in regions of high, naturally
occurring UV-B flux, and increased as UV-B radiation
diminished along a latitudinal gradient. Much of this
UV-B attenuation was removed upon methanolic ex-
traction of the epidermis, suggesting that phenolic com-
pounds such as flavonoids were important in the ab-
sorption of UV-B radiation. Such compounds produce
ideal UV screens since they are nearly transparent in
the visible region, while possessing high absorption
coefficients in the UV region. In greenhouse experi-
ments, epidermal transmission was significantly reduced
by UV-B radiation in corn (Robberecht and Caldwell
1978) and pea (Robberecht et al. 1980).
Under low PAR growth regimes and high UV-B ir-
radiance, Tevini et al. (1981) found that a high con-
centration of flavonoids (water extractable) was pro-
duced by seedlings which appeared to be relatively re-
sistant to UV-B radiation (barley and radish). In con-
trast, very little flavonoid production was found in the
sensitive species, corn and bean. Flavonoid content in
barley leaves rose in direct response to increasing UV-B
irradiance, suggesting that this might be a protective
response. Nevertheless, moderate UV-B irradiance
produced significant reductions in net photosynthesis
I'tuii..! Plant 5H. IVKJ
419
-------
despite an increase in flavonoid concentration
(mcthanolic extractable) throughout leaf ontogeny in
soybean (Teramura and Caldwell 1981). Similarly,
Sisson {19H1) found that leaf expansion and net photo-
synthesis in squash (Cticurhita pepo L.) were repressed
hy moderate UV-B irradiance, although flavonoid ab-
sorbance (methanolic extractable) substantially in-
creased. Flavonoid concentration (acetone extractable)
also greatly increased m pea (Vu et ul. 1983) and soy-
bean (Vu et ul. 1981) leaves grown under high UV-B
irradiance. UV-B radiation has also been shown to
stimulate flavonoid biosynth&sis in parsley (Pet-
rnwlinum Itormme Hoffm.) cell suspension cultures
(Wcllmann 11J7I, 1975), and this induction apparently
involves the phytochrome system. Flavone glucoside
synthesis was stimulated by a 1 h pre-irradiation with
UV-B and this was further enhanced by a subsequent
15 h FR irradiation. This FR effect was reversed by R
irradiation; however, neither R nor FR had any effect
without pre-irradiation with UV-B. Wellmann (1982)
has also recently reported that flavonoid formation is
stimulated by UV-B irradiation in parsley and dill
(Anethum graveolens L.) hypocotyl and roots, and of
wheat (Tritiatm ucitmim L.) and rye coleoptiles. Due
to its rapid and dose dependent response, its high
quantum effectiveness near 290 nm, and the strong
UV-B absorption it appears that flavonoid biosynthesis
in these systems is a protective reaction against UV-B
radiation.
High UV-B irradiance has been reported to increase
anthocyanm production in several crop species. Ambler
et ul. (1975) and Bennett (1981) have reported the
formation of a red pigment, presumably anthocyanins,
in cotton (do\\ypnim hirsiitnrn L.) petioles. Recently,
Drumm-Herrel and Mohr (1981) demonstrated that
anthocyanin synthesis m sorghum (Sorghum vulgare
Pers.) mesocotyls involved interactions between UV-A,
UV-B, and phytochrome photoreceptors. UV-B in-
duced anthocyanin production has also been reported in
mustard hypocotyls, and corn, wheat, and rye (Secule
cerate L.) coleoptiles (Wellmann 1982). Although this
pigment production represents a specific UV-B effect,
anthocyanin biosynthesis may not be particularly adap-
tive since it has little absorption in the UV-B waveband.
Ion transport
Very little work has been done on the effects of UV-B
radiation on ion transport. In an early study, Benedict
(1934) concluded that UV-B radiation between 290
and 310 nm stimulated growth and increased calcium
content in tomato, soybean, and cucumber. Radiation
below 265 nm was inhibitory. However, these data must
be viewed with caution due to the extremely low visible
light growth conditions (approximately 0.04 mmol m"2
s~' PAR) used in this study. More recently, Ambler et
al. (1975) examined the influence of UV-B radiation on
"Zn translocation in seedlings of two cotton cultivars.
In general, "Zn translocation from cotyledons into
shoots was proportionately reduced as UV'-li irradiance
increased.
Morphological and anlomical effects of UV-B
radiation
l.eiif area and specific leaf weight
Among the most sensitive plant organs to environmen-
tal stress are plant leaves. Leaf area is generally reduced
by temperature, water, mineral, or salt stresses. There-
tore, it is not surprising that leaf area is also reduced by
UV-B radiation. In an extensive growth chamber study
screening over 70 unrelated crop species and cultivars.
Biggs and Kossuth (1978) found that leaf area was sig-
nificantly reduced m over 60% of the cases. The most
sensitive crops included soybean, bean, pea, cowpea
[Vigna unguiculata (L.) Walp.j, cucumber, watermelon
(Citrullus vulgaris L.) rhubarb (Rheum rhaponncum
L.), rutabaga [Brassica napobrassica (L.) Mill), kohlrabi
(Brassica oleracea L. cv. gongylodes), and brussel
sprouts (B. oleracea L. cv. gemmifera),.while little effect
was noted in rice (Oryza saliva L.), wheat, barley, millet
(I'ennisetum glaucum L.), oats, peanut, cotton, and
sunflower (Heliantlius annuus L.). In the most sensitive
plants, leaf expansion was reduced by 60-70% (Tevmi
et al. 1981, Biggs et al. 1981). It must be noted, how-
ever, that such large area reductions are only found in
studies utilizing very low PAR. Teramura (1980) found
that UV-U radiation was more efficient at reducing leaf
expansion in soybean under decreasing PAR. Growth in
moderate UV-B irradiance and high PAR had no sig-
nificant effect on soybean leaf area, and in fact, ambient
UV-B irradiance may even stimulate leaf expansion
(Teramura and Caldwell 1981). In field grown crops,
leaf expansion was substantially increased by moderate
UV-B radiation enhancements m potato (70% in-
crease) and mustard (30% increase), while leaf expan-
sion was unaffected in corn, cowpea, peanut, rice, and
radish (Biggs and Kossuth 1978). It is noteworthy that
cowpea and mustard were among the most sensitive
crops in terms of leaf area reduction based on growth
chamber data, while field experiments indicated they
were among those most resistant. This suggests that
qualitative as well as quantitative differences exist be-
tween plants grown in growth chambers and those
grown in the field. Nevertheless, a few very sensitive
species such as squash (Cucurbita pepo L.; Sisson 1981)
and cucumber (Teramura et al. 1983) do show signific-
ant leaf area reductions even when irradiated with mod-
erate levels of UV-B and high PAR, indicating their
potential sensitivity under natural conditions.
Plants may also adapt to a UV-B radiation environ-
ment by increasing their specific leaf weight (SLW), the
ratio of leaf mass to area. In this manner, upper leaf
tissue layers might act as anatomical screens or filters to
decrease UV-B transmission into sensitive underlying
420
Phynol Plinl 58, 1981
-------
areas. Specific leaf weight was fount! to increase in a
number ol soybean cullivars exposed to UV-Il radiation
(Biggs et al. 1981, Vu et al. 1982). However, in a
screening experiment of X2 different crop and other
economically important species conducted in growth
chambers (IJiugs and Kossuth 1978), SLW changes did
not always correspond with UV-B radiation resistance,
as was anticipated. In fact, SLW was unaffected by
UV-B radiation m many plants and decreased in re-
sponse to UV-B radiation in some species. Therefore,
this anatomical manifestation alone is insufficient to
protect crops from UV-H radiation and cannot be used
as an indicator characteristic of UV-B radiation stress
per se.
Rron/ing, glazing and chlorosis
UV-B radiation also produces bronzing, scorching,
glazing or chlorosis in leaves of susceptible plants such
as soybean (Vu et al. 1983, Biggs et al. 1981), pea (Vu
et al. 1978) and cucumber (Teramura et al. 1983). Un-
der high UV-B irradiancc, even relatively resistant
crops such as barley (Tevmi et al. 1981) and cotton
(Ambler et al. 1975, Krizek 1975) show these effects.
However, these symptoms are nearly always associated
with plants grown under either high UV-B irradiance or
with moderate UV-B irradiation but low PAR. In field
studies with high UV irradiance supplied by unfiltered
lamps, these symptoms have not been reported.
Nevertheless, a few crops such as cucumber and at least
one cultivar of soybean (cv. Hardee) do seem to de-
velop some of these manifestations when grown under
moderate UV-B irradiance and high PAR (Teramura et
al. 1980, Teramura et al. 1983), indicating that they
may occur m natural conditions. Robberecht and
Caldwell (1978) reported that leaf bron/ing was not
apparent in corn, but did develop in tomato exposed to
UV-B radiation in a greenhouse. The authors suggested
that this might be partially due to differences in UV-B
epidermal transmittance, since a significant increase in
tlavonoid biosynthesis was found in corn, but not in
tomato. The presence and effectiveness of UV-B ab-
sorbing pigments in the leaf epidermis may be impli-
cated in explaining some of the differences in observed
leaf symptoms discussed above.
Plant stunting
One of the most common observations on seedling
growth after UV-B irradiation is stunting or dwarfing,
primarily resulting from a decrease in internode length.
Similar to bronzing and chlorosis, stunting is exacer-
bated by high UV-B irradiation and low PAR. In a
greenhouse study, Teramura (1980) found that after 6
or 7 weeks exposure to a range of moderate UV-B ir-
radiance, stunting in wheat and soybean was only
observed in plants grown under shaded conditions. In
tact, under unshaded conditions more closely ap-
proximating those of the field (average mid-day PAR =
1.6 mmol m~- s"1), soybean which did not receive any
UV-B radiation were shorter than those grown under
low and moderate levels ot UV-B. Stunting in soybean
was primarily due to shorter internodes and not a re-
duction m node number. This suggested that UV-B
radiation did not simply delay the rate of plant de-
velopment, but rather involved some intrinsic growth
characteristics. In a field experiment. Biggs and Kossuth
(1978) reported that the height of the mam stalk in corn
was reduced by UV-B radiation, although their data
indicate that the greatest reduction occurred under the
lowest UV-B radiation enhancement. In the same
study, rice height was unaffected and squash even
showed a slight stimulation of growth. In another field
experiment, Ambler et al. (1978) found that high UV
(UV-B and UV-C) irradiance from untiltered lamps
had no effect on height in soybean, sorghum, or corn.
Dry matter production and allocation
Total plant biomass accumulation (dry weight) is a good
indicator of UV-B radiation effects on growth. Total
biomass represents a long-term integration of all bio-
chemical, physiological, and growth parameters.
Therefore, even subtle UV-B induced effects on phy-
siological processes could accumulate and result in sig-
nificant effects on biomass. Since plant biomass data are
easily obtainable, it is not surprising that a number of
studies (Tab. 3) have included the effects of UV-B
radiation on dry matter production and its allocation
into component plant organs. These studies show that
total plant dry weight is often substantially reduced by
UV-B. Brandle et al. (1977) found that dry weight in
pea was significantly reduced after only 9 days of UV-B
irradiation. Although large species differences exist
(Tab. 3), reductions in total biomass are often accom-
panied by substantial modifications m the partitioning
of biomass into component plant organs. In dicotyle-
dons, a greater proportion of biomass is allocated into
leaves (despite an absolute reduction in leaf area) and
less into stems and roots. In species such as so>bean,
bean, pea, and cucumber, the increase in the proportion
of dry weight found in leaves is the result of an increase
in SLW. This trend is not nearly as clear m monocotyle-
dons, where a multitude of species specific responses
are found. As with the other morphological and ana-
tomical characteristics previously examined, the
greatest effects on total dry weight accumulation and
biomass realiocation were reported in growth chamber
(Biggs and Kossuth 1978) or shaded greenhouse (Vu et
al. 1978, Van et al. 1976) studies. Teramura (1980),
using various combinations of UV-B and PAR levels
found that soybean dry weight and the allocation into
various organs were increasingly affected as growth
PAR levels decreased. This indicated that UV-B in-
duced reductions in total biomass were magnified under
low PAR regimes.
Phmol Pljni 5H. IVKJ
421
-------
T.ih 1 Elfccts of ullravuilel-U radiation on greenhouse and growth chamber grown plants. *, refers to citations in Tab 2.
UV effects on total plant dry weight
C'rop
Wheat
Rice
Corn
Darky
Oats
Sorghum
So\bean
Collon
Beans
Peas
Rye
Tomato
Millet
Peanut
Radish
Cucumber
Squash
C.ibh;ige
Collards
Onion
Lettuce
Celery
Carrots
Parsnip
Eggplant
Hell pepper
Chard
Okra
Asparagus
Artichoke
Sunflower
Itroccoli
Hrusscl sprouts
Cauliflower
Kale
Kohlrabi
Mustard
Rutabaga
Pumpkin
Watermelon
Cantaloupe
Oiufa
Rhubarb
Increase
8*
X
8
6
8
8
6
8
8
8
8
8
8
Decrease
8, 36
8
8, 50
8, 57
5, 43, 45
8, 45
5, 8. 9, 21, 36, 37,43,45, 49, 50
8,42
8, 12, 43, 45, 50
8, 45
8,45
8
57, 58
8
8
8,45
5, 8, 45
8
8
8
8
8
8
8
8
8
8
8
8
8
8
No change
8, 21
8, 45
5, 42, 43, 45. 57
42
5
2, 8. 21
21, 57
21
21, 43, 45
5, 43. 45
21,42
21
8
21
8
8
8
-
In a field study with unfiltered lamps. Ambler et al.
(1978) found that massive UV doses simulating up to an
8-fold increase in ambient levels, had no effect on
abovcground dry weight production in squash (Cucur-
bita maxima L.), bean, or corn; however, reductions
were noted for broccoli (B. oleracea L. cv. botrytis) and
sugar beet (Tab. 4). Also using unfiltered lamps. Hart et
al. (1975) found no effect on corn, sorghum, soybean or
peanut. Biggs and Kossuth (1978) on the other hand,
reported total dry weight reductions in field grown corn,
pea, tomato and mustard (Brassica juncea cv. cripifolia)
irradiated with filtered lamps. Interestingly, plant dry
weight was somewhat stimulated by the highest UV-B
irradiance in potato although this stimulation cannot
presently be explained. In sensitive crops, leaf biomass
proportionately increased, while stem and sometimes
root biomass decreased. The trends observed in this
field study were remarkably similar to those found in
growth chambers. In another field experiment, Caldwell
et al. (1975) found that aboveground dry weight was
reduced in barley and pepper (Capsicum annum L.),
while belowground reductions were observed in soy-
bean, pepper and corn. Alfalfa (Medicago sativa L.) and
tomato were apparently unaffected by the relatively
large UV-B irradiance (simulating 5U% ozone deple-
tions) used in that study.
422
Phynol Plant 58. 198}
-------
I ab 4 Effects of UV supplementation on field grown crops. I), unaffected, •*-, stimulated and -, decreased relative to controls. 1,
unliliered 13ZS-CLG and HS-40 bunlamps, 2. FS-40 sunlamps filtered with (I 13 mm cellulose atetate, 3. F-S-4IJ sunlamps tillered
with (i 13 mm Kodacel IA4DI, 4. untiltercd r-S-40 sunlamps.
Crop
Rice
Corn
Potato
Sorghum
Sovbe.m
Sugar beet
Ue.ms
Cowpea
fomulo
Pcamil
Pepper
li.irley
loh.iccn
Millet
Calibiige
Squash
Hroccoh
Must.ird
UV effect on total dry weight
Ambler et1 Biggs and' C.ildwell et->
al. (I97H) Kossuth (I97H) al. (1975)
0
0 - -t-
+
0
0
"
0
0
0
0
-
—
0 0
—
—
Hart et al.4
(1975)
0
0
0
0
1)
0
0
Crop yield
Nearly all of our information on the effects of UV-B
radiation on crops comes from either growth chamber
or greenhouse studies. Owing to space limitations, it is
impractical to grow plants to reproductive maturity in
such facilities. Of all the components of dry matter pro-
duction, allocation into reproductive organs or crop
yield is of major interest in crop species. It is the key
factor in our assessment of the impacts of a partial
stratospheric ozone depletion. Yet surprisingly, only a
handful of studies exist where plants were grown to a
stage with harvestable fruit (Tab. 5), and none of these
arc readily available to the scientific community. With
the exception ul leafy vegetables, whose yield may
perhaps be assessed in the confinement of controlled
environments, our understanding of UV-B radiation
effects on crop yield is based on only a few field trials
and on a limited number of crops. Hart et al. (1975)
grew 10 crop species [tomato, sweet pepper, corn, sor-
ghum, soybean, peanut, cotton, tobacco (Nicotiana
tdbacnm L), millet and cabbage] under unfiltered
(FS-40) sunlamps, providing a very large UV radiation
(UV-B and UV-Q supplement. Despite this massive
UV dose, they only found a significant reduction in fruit
number in pepper, and only for one of the two experi-
mental growing seasons. Yield was unaffected in the 9
other crops. In a similar field experiment. Ambler et al.
(1978) used unfiltered (BZS-CLG and FS-40) sun-
lamps to test 8 crops (squash, bean, corn, sorghum, soy-
bean, sugar beet, broccoli and cowpea). Based upon
their biological effectiveness (A£9 weighting function).
these lamps produced UV enhancements up to 8-fold
greater than normally incident in the field. Again, de-
spite the high UV irradiance, yield was significantly re-
duced only in broccoli. Esser (1980) conducted a field
experiment in the Federal Republic of Germany using
filtered (Schott \VG 305, 2 and 3 mm) and unfiltered
(Philips TL 40/12) sunlamps over 6 crops (potato,
spinach, bean, radish, barley, and cabbage). The radia-
tion from filtered lamps simulated UV-B enhancements
resulting from less than 10% ozone depletions and had
no significant effect on yield in any of the crops tested.
In fact, yield was slightly stimulated in most crops re-
ceiving the additional UV-B radiation. Unfiltered lamps
which produced irradiances simulating up to 40% ozone
reduction, reduced yields in potato (lubers) by as much
as 41%, spinach (leaves) by 66%, cabbage (leaves) by
49%, and bean (pods) by as much as 75%. However,
the emission from these unfiltered lamps also included
UV-C radiation. Because of the strong wavelength spe-
cificity of biological responses, the large effects resulting
from unfiltered lamps are most likely grossly exagger-
ated and therefore, interpretations from studies using
unfiltered lamps should only be made with utmost cau-
tion.
An interesting field study was conducted by Bartholic
et al. (1975) in Florida. Three crops (corn, bean, and
tomato) were grown under panels covered with either
UV-B absorbing (Mylar) or UV-B transmitting
(polyethylene) films. Plants grown under the Mylar
panels had the direct beam component of the naturally
occurring UV-B irradiance filtered out, but still re-
ceived the diffuse component. This diffuse component
Ptmiol. Plant. 58. IVHJ
423
-------
I .ill S A summary »l licld studies on the ellccu of supplemental UV radiation on crop yield. Values represent the percentage
Ji.inge Iron) comrolb I, unhltcrcd sunlamps, 2, ambient UV-L) irradiuncc; .1. cellulose acetate tillered sunlamps. 4, \alues nul
given
( rop
Rice
C'om
Potato
Sorghum
So\hean
Sugar heel
Deans
C'owpea
Tomato
Peanut
Pepper
C'otlon
"fohacco
Millet
Cahhuue
Squash
liroeeoli
Radish
Mustard
Sptnaeh
Hart el1
al. (1975)
0
1)
(1
I)
II
()/-•'«
(1
II
I)
1)
ll.irtliolic' Amhleret'
et al (1975) al. (1978)
+ 8% 0
1)
I)
0
0 II
I)
0
0
-45%
fiieus' and Esser1
Kos.siith (1978) ( I9SII)
0
0 1
II — K)%
-75'".,
-26%
(1
-49%
-69%
n
-19%
-66%
contains nearly 50% of the total incoming UV-B radia-
tion. They found no yield differences in bean or tomato,
Init yield in corn was significantly greater under the
polyethylene panels (Tab. 5). This apparent stimulation
in yield was al least partially the result of greater insect
infestation under the Mylar panels.
Biggs and Kossuth (1978) used filtered (0.13 mm
cellulose acetate) sunlamps (FS-40) to supplement
natural UV-B radiation in the field. Unlike the previ-
ously described studies, they used an artificial soil
medium in raised beds and grew 9 crops (potato, to-
mato, corn, pea, peanut, squash, rice, mustard, and
radish) under a gradient of increasing UV-B radiation.
Total yield in corn, rice, radish, peanut, and potato was
uii.illcftcd by enhanced levels of UV-U, although there
was some evidence ot qualitative changes in tuber and
fruit sizes in potato and peanut, respectively. In mus-
tard, the only leaty crop investigated, enhanced UV-B
resulted in significant reductions in leaf dry weight and
therefore yield. In squash, total fruit weight decreased,
while both total fruit weight and number diminished in
pea. UV-U irradiation also resulted in reductions in to-
tal fruit production and average fruit weight in tomato.
Although the results from this study suggested that
UV-B radiation from filtered lamps was apparently ef-
fective in reducing yield in 4 out of 9 crops, the mag-
nitude of yield reduction was not generally related to
UV-B dose. In 2 of the 3 crops showing fruit yield re-
ductions, the highest UV-B irradiance had only a small
effect, while a much lower one produced substantial
effects. As was the case in the study by Bartholic et al.
(1975), some of these inconsistencies were produced by
insect infestation (R. H. Biggs personal communica-
tion).
Until the discrepancies can be resolved, all the field
experiments to date have only limited use. As can be
gathered from these disparate studies, much more in-
formation is needed before a reliable assessment can be
made on the effects of a partial ozone depletion on
global crop productivity.
Response differences to UV-B radiation
Prior to the organization of the Climatic Impact As-
sessment Program (CIAP) by the U.S. Department of
Transportation (Nachtwey et al. 1975), very little was
known about the effects of UV-B radiation on plants. In
fact, nearly all the studies available up to that time
utilized broadband UV-C radiation or monochromatic
UV-C radiation, principally 254 nm. Unfortunately,
known photobiological responses to 254 nm can only be
used for comparative purposes and not for extrapola-
tion or quantitative assessments of UV-B radiation en-
hancements arising from projected ozone reductions.
Not only do quantitative differences in response occur
between the two wavebands, but there has been some
suggestion that qualitative differences might also be
present (Nachtwey 1975). Therefore, one of the pri-
mary objectives of CIAP was to empirically determine
UV-B sensitivities in a range of different plant and crop
species. As a result of this and other continuing efforts,
over 45 different crop species have been screened under
a diverse range of environmental conditions in growth
424
Phyjiol. Plinl 58. 1981
-------
chambers and greenhouses (Tab. 3), and in a limited
number of ticld experiments (Tab. 4). This numher
would approximately double if crop cultivars and other
economically important plant species are also consid-
ered.
Interspecific differences
There are large interspecific response differences to
UV-B radiation in terms of total biomass production
(Tabs 3 and 4). Some species are resistant to UV-B
radiation, most are sensitive to a degree, while growth
in others is apparently stimulated. In an extensive
screening experiment conducted in growth chambers in-
cluding over 40 crop species and 30 cultivars (Biggs and
Kossuth 1978), about 30% of the crops tested were
cither unaffected or stimulated by UV-B radiation,
another 20% were extremely sensitive, and the remain-
der were intermediate in sensitivity, based upon total
dry matter production. Considering all other plant
characteristics which were influenced by UV-B radia-
tion, such as leat area, height, biomass partitioning pat-
tern, etc, there apparently is an enormous array of
UV-B responses expressed by different crop species.
Obviously, a multitude of morphological, anatomical
and physiological processes all act in concert to provide
different species sensitivities, including differences in
cuticle thickness, the presence of UV absorbing pig-
ments, changes in SLW, leaf reflectivity, crop or leaf
canopy development, etc.
Regardless of these species specific response differ-
ences, however, a few broad generalizations can be
made, given the same treatment conditions.
Monocotyledons as a whole, seem to be less affected by
UV-B radiation than dicotyledons (Van and Garrard
1975, Teramura 1980, Tevini et al. 1981). It has been
suggested that this difference might be partially due to
the vertical leaf orientation, protective basal sheath, and
the protected menstematic region in monocotyledons
(Van and Garrard 1975). At least one study (Basiouny
et al. 1978) concluded that crops with the C, photo-
synthetic pathway were more affected than those with
the C4 pathway. In terms of plant height and total
biomass accumulation, those researchers found that
neither of the C4 crops investigated (sorghum and corn)
was affected by UV-B irradiation, while all the Cj crops
(collard, oats, peanut, and soybean) had at least one of
these characteristics affected. Finally, some plant
families show relatively uniform responses. For exam-
ple, 8 of 10 crops belonging to the Cruciferae were
extremely sensitive to UV-B radiation while the
Poaceae was relatively resistant (Uiggs and Kossuth
1978).
Inlraspecific differences
In addition to the sizable interspecific differences in
UV-B radiation response, there is an appreciable in-
traspecific response difference (Tab. 3). Many of the
crops listed showed a variable response to UV-B radia-
tion in terms of dry matter production. Although some
of this represents differences in UV-B irradiance or
treatment conditions between individual studies, it also
reflects cultivar response differences. Large cultivar
differences in UV-B response have been reported in
soybean (Biggs et al. 1981, Vu et al. 1978), cotton
(Ambler et al. 1975), bean (Bennett 1981, Dumpert
and Boscher 1982), collard and cabbage (Van et al.
1976, Garrard et al. 1976), wheat, barley, corn and rice
(Biggs and Kossuth 1978), and spinach (Dumpert and
Boscher 1982). In a growth chamber study of 19 soy-
bean cultivars. Biggs et al. (1981) concluded that 20%
were extremely sensitive to UV-B radiation, 20% were
relatively resistant, and the remainder were inter-
mediate in sensitivity. Surprisingly, these proportions of
sensitive and resistant cultivars are very similar to those
found between species, indicating that a tremendous
range of intraspecitic variability to UV-B radiation is
present in the soybean germplasm. Currently, the
reasons for the cultivar variability are not completely
understood, nevertheless it does suggest that there is a
potential for genetically modifying future cultivars to
minimize the deleterious effects of a global ozone de-
pletion.
Acknowledgements - The author would like to thank Irv For-
seth, Roman Mirccki and John Lydon for their comments on
.in earlier version ol lliib manuscript. Also many thanks ui Inez
Miller tor her careful typing. This work was supported by the
United Slates Environmental Research Laboratory in Corval-
lis, Oregon (CR 808-035-020), and grunts from the Graduate
School and Provost to the author. Scientific Article No.
A-3368, Contribution No. 6440 of the Maryland Agricultural
Experiment Station, Department of Botany. Although the
work described in this article has been funded in part by the
United States Environmental Protection Agency, it has not
been subjected to the Agency's required peer and policy re-
view and therefore does not necessarily reflect the view of the
Agency and no official endorsement should be interred
Travel to the international workshop held in Delhi, India.
was supported by N. S F
References
Allen, L. H., Vu. C. V., Berg, R. H. Ill & Garrard. L. A. 1978.
Impact of solar UV-B radiation on crops and crop
canopies. - In UV-B Biological and Climatic Effects Re-
search (BACER), Final Report. EPA-IAG-D6-0168
USDA-EPA, Washington, D. C. p. 134.
Ambler, J. E., Rowland, R. A. & Maher, N. K. 1978. Re-
sponse of selected vegetable and agronomic crops to in-
creased UV-U irradiation under tield conditions. - In
UV-B Biological and Climatic Effects Research (BACER)
Final Report, EPA-iAG-D6-4)l68, USDA-EPA,
Washington, D. C., p. 17.
- , Knzck, D. T. & Semmiuk, P. 1975. Influence of UV-B
radiation on early seedling growth and translocation of
"Zn from cotyledons in cotton. - Physiol Plant .14-
177-181.
Phywil Plant 5X. I ¥83
425
-------
Harthohc. J F, llalscy. L H. & Garrard, L. A. 1975 Field
trials wilh tillers in test for elleets of UV radiation on
agricultural productivity. -In Climatic Impact Assessment
Program (CIAP), Monograph 5 (D. S. Nachtwey, M. M.
Caldwell and R. H. Biggs, eds), pp. 61-71, U S Dept.
1 ransp , Report No DO I -1ST-75-55, Nail. Techn. Info.
Serv , Springfield, VA.
Basiouny, F M , V.m. T K. & Biggs. R. H. 1978 Some mor-
pholouicnl .md biochemical characteristics of C, and C4
pl.mts'irradialed with UV-U. - Physiol Plant. 42: 29-32.
Benedict. H. M. 1934 Effect of ultraviolet radiation on growth
and on the calcium and phosphorus contents of plants. —
Hot. Gaz. 96: 330-341.
Bennett, J. H. 1981. Photosynthesis and gas diffusion in leaves
of selected crop plants exposed to ultraviolei-B radiation.
-J. Environ. Qual. 10: 271-275.
Biggs, R. II. & Kossuth, S. V. 1978. Effects of ultraviolet-B
radiation enhancements under field conditions -In UV-B
Biological and Climatic Effects Research (BACER), Final
Report.
- . Kossulh, S. V & Teramura, A H. 1981. Response of 19
cultivars of soybeans to ultraviolel-H irradiance. — 1'hysiol.
Plant. 53: 19-26.
Bogenneder, A. 1982. Action spectra for the depression of
photosynthesis by UV irradiation in Lactuca \uuva L. and
Rd»ie\ alpmifi L. - In Biological Effects of UV-B Radia-
tion (H. Uauer, M. M. Cildwell, M. Tevim and R. C.
Worresl, eds), pp. 132-139, Gesellschaft fur Strahlen-und
Umwellforschung mbH Miinchen.
- & Klein, R. 1978 Die Abhangigkeit der UV-Empfindlich-
kcil von der Lichtqualitat bei der Aufzucht (Luctuca sanva
L.) - Angew Bot, 52: 283-293.
Brandle, J. R., Campbell, W F., Sisson, W B. & Caldwell. M.
M. 1977 Net photosynthesis, electron transport capacity,
and ultrastructure of Piwim suttvtim L. exposed to ul-
traviolet-B radiation. - Plant. Physiol. 60: 165-169.
Caldwell. M. M. 1981. Plant response to solar "ultraviolet
radiation. - In Encyclopedia of Plant Physiology, New
Series, Vol I2A. Physiological Plant Ecology I (O L.
Lange, P S. Nobel, C B Osmond and H Ziegler, eds), pp.
169-197, Sprmger-Verlag, Berlin, Germany. ISBN
0-387-10763-0
- , Sisson. W. B., Fox, F M. & Brandle. J. R. 1975 Growth
response to simulated UV irradiation under field and
greenhouse conditions. - In Climatic Impact Assessment
Program (CIAP). Monograph 5 (D. S. Nachtwey, M. M.
Caldwell and R. H. Biggs, eds), pp. 253-259, U.S. Dept.
Transp.. Report No DOT-1 ST-75-55, Nail. Techn. Info.
Serv , Springfield, VA
Chassagne. M-ll.. Gaudillere, J.-P. A Monties, B. I981a.
I.flc-ts tin r.iynnnemcnt ultraviolet sur les plantcs cultivees
sous eclairemem nalurel el artiliciel. I. Morphologencse et
equipemeni polyphcnolique de la tomale, la laitue et le
poivron. - Acta'OEcol OEcol. Plant. 2: 267-282.
- , Gaudillere, J.-P. &. Monties, B. 19815. Effets du rayon-
nement ultraviolet sur les plantes cultivees sous eclaire-
ment naturel et artificie). II. Effets sur la capacite photo-
synthetique chez la tomate et le poivron. - Acta Oecol./
Oecol. Plant. 4: 327-338
Drumm-Hecrel. H. & Mohr, H 1981. A novel effect of UV-B
in a higher plant (Sorghum vulgare). - Photochem. Photo-
biol. 33: 391-398
Dumpert. K & Boscher, J. 1982. Response of different crop
and vegetable cultivars to UV-B irradiance: preliminary
results. - In Biological Effects of UV-B Radiation (H.
Bauer, M. M. Caldwell. M. Tevim and R. C. Worrest, eds).
pp 102-1(17, Gesellschaft fur Strahlen- und Umwelt-
torschung mbH, Munchen.
Ehrlich, P R., Ehrhch, A. H. & Holdren, J. P. 1977. Eco-
science: Population, Resources, Environment. - W. H.
Freeman and Company, San Francisco, CA., pp. 283-385.
ISBN 0-7167-0029-8.
Esser, G 19MO Einfluss einer nach Schadsloffimmission ver-
mclmcn bmstrahlung von UV-B Litht aul Kulturptlanzen.
2. Versuchjahr. - Bericht Battelle Institut E V Frankfurt,
BF-R-63 984-1.
Food and Agriculture Orgamration. 1981 FAO Production
Yearbook, Vol. 35. -FAO, Rome ISHN 92-5-01 M 198-9
Garrard, L. A., Van, T. K. & West. S H 1976 Plant response
to middle ultraviolet (UV-13) radiation: Carbohydrate
levels and chloroplast reactions. - Soil Crop Sci Soc. FU.
Proc. 36: 184-188
Gauiman, H. W , Rodriguez, R R. & Escobar, D E 1975
Ultraviolet radiation reflectance, transmission, and ab-
sorbtance by plant leaf epidermises. - Agron. J. 67.
720-724.
Green, A E. S., Cross, K. R. & Smith. L. A. 1980 Improved
analytic characterization of ultraviolet skylight. - Photo-
chem Photobiol. 31: 59-65.
- , Sawada, T £ Shettle, E. P 1974. The middle ultraviolet
reaching the ground. - Photochem. Photobiol. 19:
251-259.
Hart, R. H , Carlson, G. E., Klueter, H. H. & Cams, H R
1975 Response of economically valuable species to ul-
traviolet radiation. - In Climatic Impact Assessment
Program (CIAP), Monograph 5 (D S. Nachtwey, M M
Caldwell and R. H. Biggs, eds), pp. 263-275, U 'S Dept.
Transp, Report No DOT-TST-75-55, Natl. Tech Info
Serv , Springfield. VA.
Hashimoto, T & Tajima, M. 1980 Effects of ultraviolet ir-
radiation on growth and pigmentation in seedlings - Plant
Cell Physiol. 21: 1559-1571.
Jams, P. G. 1971. The estimation of resistances to carbon
dioxide transfer. - In Plant Photosynthetic Production:
Manual of Methods (Z. Sestak, J. Catsky and P G Jams,
eds), pp. 566-631, W. Junk, The Hague.
Knzek, D. T. 1975. Influence ot ultraviolet radiation on ger-
mination and early seedling growth. - Physiol. Plant. 34:
182-186.
Miller, G. F. 1982. Living in the Environment (3rd Ed.). -
Wadsworth Publishing Company, pp. 154-180. ISBN
Nachtwey, D. S. 1975. Linking photobiological studies at 254
nm with UV-B. -In Climatic Impact Assessment Program
(CIAP), Monograph 5 (D. S Nachtwey, M. M Caldwell
and R. H. Biggs, eds), pp 50-84, U S Dept of Transp ,
Report No. DOT-TST-75-55. Natl Techn Info. Serv ,
Springfield, VA.
- , Caldwell, M. M. & Biggs, R. H. 1975 Climatic Impact
Assessment Program (CIAP). Monograph 5 (D S
Nachtwey, M. M. Caldweli and R. H Biggs, eds), U S.
Dept. of Transp , Report No DOT-TST-75-55. Natl.
Techn. Info. Serv , Springtield, VA.
National Academy of Sciences. 1 982. Causes and Effects ot
Stratospheric Ozone Reduction- An Update. - National
Academy Press. Washington, D. C . p 339 ISBN
0_jll9_()3248-2.
Nobel, P. S. 1974. Introduction to Biophysical Plant
Physiology. - W. H. Freeman and Company, San Fran-
cisco, CA. pp. 325-343. ISBN 0-7167-0592-3.
Robberecht, R. & Caldwell. M. M. 1978. Leaf epidermal
transmittance of ultraviolet radiation and its implications
for plant sensitivity to ultraviolet-radiation induced injury.
- Oecologia 32: 277-287.
- , Caldwell, M. M. & Billings, W. D. 1980. Leaf ultraviolet
optical properties along a latitudinal gradient in the arctic-
alpine life zone. - Ecology 61: 612-619.
Sisson, W. B. 1981. Photosynthesis, growth and ultraviolet ir-
radiance absorbance of Citcurbita pepo L. leaves exposed
to ultraviolet-B radiation (280-315 nm). - Plant Physiol.
67: 120-124.
- & Caldwell, M. M. 1976. Photosynthesis, dark respiration,
and growth of Rumex patienna L. exposed to ultraviolet
irradiance (290 to 315 nanometers) simulating a reduced
atmospheric ozone column. - Plant Physiol. 58: 563-568.
426
Physiol Plant 38. 1983
-------
Siumh.tck, K. E. IMKI Proteins ot the chloroplasl. - In The
Biochemistry of Plants. A Comprehensive '('realise, Pro-
lems and Nucleic acids (A. Marcus, ed.), Vol. 6, pp.
303-319, Academic Press, Inc., New York, NY, ISBN
Teriimura. A. II. 1982. The amelioration of UV-B effects on
productivity hy visible radiation. - In The Role of Solar
Ultraviolet Radiation in Marine Ecosystems (J. Calkins,
ed.), pp. 367-382, Plenum Pub. Corp., New York, NY,
ISBN 0-306-1(1909-7.
- 1980. Effects ot ultraviolet-B irradiance on soybean. I.
Importance of photosynthcticully active radiation in
evaluating iiltruviolet-B irradiance effects on soybean and
wheat growth. - Physiol. Plant. 48: 333-339.
- Jit Perry, M. C. 1982. UV-B irradiation effects on soybean
photosyntheiic recovery from water stress. - In Biological
Effects'of UV-B Radiation (H. Bauer, M. M. Caldwell, M.
Tevmi and R. C. Worrest, eds), pp. 192-202, Gesellschaft
fur Strahlen- und Umweltforschung mbH, Miinchen.
- A Caldwell. M. M. 1981. Effects of ultraviolet-B ir-
radiance on soybean. IV Leaf ontogeny .is a factor in
evaluating iiltraviolet-li irradiance etfects on net photo-
synthesis. - Am. ). Bot. 68: 934-941.
- , Tovmi, M. &. Iwanzik, W. 1983. Effects of ultraviolet-B
irradiation on plants during mild water stress. I. Effects on
diurnal stomalal resistance. - Physiol. Plant. 57: 175-180.
- . Biggs, R. H & Kossuth, S. 1980 Effects of ultraviolet-B
irradiances on soybean. II. Interaction between ultra-
violet-B and photosynthetically active radiation on net
photosynthesis, dark respiration, and transpiration. - Plant
Physiol. 65: 483-488.
Tevmi. M. & Iwanzik, W. 1982. Untersuchungen iiber den
tmfluss erhohter UV-B Strahlung auf Entwicklung,
Zusammensetzung, Struktur und Funktion von Ptlanzen. -
Bereich Projekttragerschaften, GSF, Munchen.
- , Iwanzik, W. & Thoma, U. 1981. Some effects of en-
hanced UV-B irradiation on the growth and composition
o( plants. - Planta 153: 388-394.
- , Iwanzik, W. & Thoma, U. 1982. The effects of UV-B
irradiation on higher plants. - In The Role of Solar Ul-
traviolet Radiation in Marine Ecosystems (J. Calkins, ed.),
pp. 58I-M5, Plenum Pub. Corp., 'New York, NY, ISBN
(i.30f>-4()9()9-7.
- , Iwanzik, W. & Teramura, A. H. 1983. Effects of UV-B
radiation on plants during mild water stress. II. Effects on
growth, protein and flaconoid content. - Z. Pflanzenphy-
siol (in press).
Van, T. K. & Garrard, L. A. 1975 Elfect of UV-B radiation
on net photosynthesis ot some Cj and C4 crop plants. - Soil
CropSa. Soc. Ha. Proc. 35: 1-3.
- , Garrard, L. A. & West. S. H. 1977 Effects of 298-nm
radiation on photosyntheiic reactions ol leaf discs and
chloroplast preparations of some crop species. - Environ.
Exp. Bot. 17- 107-1 12.
- , Garrard, L. A. & West, S. H. 1976. Effects of UV-B
radiation on net photosynthesis of some crop plants. -
Crop Sci. 16: 715-718.
Vu, C. V., Allen. L. H. & Garrard, L. A. 1978. Effects of
supplemental ultraviolet radiation (UV-B) on growth of
some agronomic crop plants. - Soil Crop Sci. Soc. Fla.
Proc. 38: 59-63.
- , Allen, L. H. & Garrard, L. A. 1981. Effects of supple-
mental UV-B radiation on growth and leaf photosynthetic
reactions of soybean (Glvcme max). - Physiol. Plant. 52.
353-362.
- , Allen, L. H. & Garrard, L. A. 1982a. Effects of supple-
mental UV-B radiation on primary photosynthetic car-
hoxylating enzymes and soluble proteins in leaves of Cj
and C4 crop plants. - Physiol. Plant. 55: 11-16.
- , Allen, L. H. & Garrard, L. A. 1982b. Effects of UV-B
radiation (280-320 nm) on photosynthetic constituents
and processes in expanding leaves of soybean [Gtycine max
(L.) Merr.|. - Environ. Exp. Bot 22: 465—173
- , Allen. L. H. & Garrard, L. A. 1983. Effects of enhanced
UV-B radiation (280-320 nm) on ribulose- 1,5-hisphos-
phate carboxylase m pea and soybean. - Environ. Exp.
Bot. (In Press).
Wellmann, E. 1982. Phenylpropanoid pigment synthesis and
growth reduction as adaptive reactions to increased UV-B
radiation. - In Biological Effects of UV-B Radiation (H.
Bauer, M. M. Caldwell, M. Tevmi and R. C. Worrest, eds),
pp. 145-149. Gcsellschaft fiir Strahlen- und Umwelt-
torschung mbH, Munchen.
- 1975. UV dose-dependent induction of enzymes related to.
tlavonoid biosynthesis in cell suspension cultures of
parsley. - FEBS Lett. 51: 105-107.
- 1971. Phytoclirome-mediated flavone glycoside synthesis
in cell suspension cultures of Petro'iehnum hortense after
preirradiation with ultraviolet light. - Planta 101:
283-286.
Edited by L. O. Bjorn and J. F. Bornman
fhvsiol Pljni 5H. IVN3
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