Download Growth and gas exchange in field-grown and greenhouse

Tree Physiology 26, 1153–1163
© 2006 Heron Publishing—Victoria, Canada
Growth and gas exchange in field-grown and greenhouse-grown
Quercus rubra following three years of exposure to enhanced UV-B
radiation
JOHN H. BASSMAN1,3 AND RONALD ROBBERECHT 2
1
Department of Natural Resource Sciences, Washington State University, Pullman, WA 99164–6410, USA
2
Department of Rangeland Ecology, University of Idaho, Moscow, ID 83844–1135, USA
3
Corresponding author ([email protected])
Received March 17, 2005; accepted September 28, 2005; published online June 1, 2006
Summary Long-term effects of enhanced UV-B radiation
were evaluated in field-grown and greenhouse-grown Quercus
rubra L. (northern red oak), a species with a multiple flushing
shoot growth habit. Seeds were germinated and grown in ambient, twice ambient (2×) or three times ambient (3×) biologically effective UV-B radiation from square-wave (greenhouse)
or modulated (field) lamp systems for three growing seasons.
Greenhouse plants in the 2× treatment had greater heights and
diameters during the later part of the first year and into the second year, but by the third year there were no differences among
treatments. There were no significant differences in growth
among treatments for field plants. Enhanced UV-B radiation
did not significantly reduce total biomass or distribution of biomass in either field or greenhouse plants. Net photosynthesis
(3×), leaf conductance (2× and 3×) and water-use efficiency
(3×) of greenhouse plants were greater in the enhanced UV-B
radiation treatments in the second year but unaffected by the
treatments in other years. None of the treatments affected these
parameters in field plants. Dark respiration was increased by
the 3× treatment in the first and third years in greenhouse
plants, and by the 2× treatment during the second year in field
plants. Enhanced UV-B had variable effects on apparent quantum yield and light compensation points. Chlorophylls were
unaffected by enhanced UV-B radiation in both greenhouse
and field conditions. Bulk methanol-extractable UV-absorbing
compounds were increased only by the 3× treatment in greenhouse plants during the third year and by the 2× treatment in
field plants during the second year. Overall, Q. rubra appears
relatively resistant to potentially damaging enhanced UV-B radiation and is unlikely to be negatively impacted even in the
predicted worst-case scenarios.
Keywords: biomass, chlorophyll, forest trees, leaf conductance, photosynthesis, ultraviolet radiation, UV-absorbing
compounds.
Introduction
Enhanced solar ultraviolet-B (UV-B) radiation can cause seri-
ous deleterious effects in plants (Lumsden 1997), but the consequences may depend on leaf anatomical properties, shoot
growth patterns and canopy architecture (Bassman et al.
2001). Angiosperm leaves are generally considered more susceptible to UV-B radiation than gymnosperm leaves because
their spatial distribution of UV-absorbing compounds is less
effective at attenuating incoming UV-B radiation (Day et al.
1993). Trees with determinate or multiple flushing shoot
growth patterns may be more susceptible to injury than those
with indeterminate shoot growth patterns because a particular
complement of leaves would be exposed to UV-B radiation for
a longer period of time. In indeterminate species, leaves are
quickly submerged within the canopy as new leaves are
formed at the apex such that any particular leaf experiences
constantly attenuating UV-B radiation (Bassman et al. 2001).
Our understanding of the effects of enhanced UV-B radiation on perennial plants, and trees in particular, is limited because relatively few species have been studied. We report here
on long-term effects of enhanced UV-B radiation on growth
and gas exchange in northern red oak (Quercus rubra L.).
Northern red oak is a moderate to fast growing angiosperm
tree species endemic to the eastern United States north of the
southern coastal plain, and Canada in southern Ontario extending eastward to New Brunswick and Nova Scotia (Sander
1990). Northern red oak is intermediate in shade tolerance,
and vigorously growing trees typically exhibit a multiple
flushing shoot growth pattern (Hanson et al. 1988). It is of substantial ecological and commercial importance and widely
planted as an ornamental outside of its native range.
Material and methods
Plant material and growth conditions
Seeds from open-pollinated Q. rubra trees in Pennsylvania
were obtained from a commercial nursery. Seeds were stratified (USDA Forest Service 1974) and then sown in 3.0-l pots
filled with a standard nursery-potting medium comprising peat
and vermiculite. At the time of sowing, the radical of most of
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the stratified seed had already emerged. Pots were placed under UV-B lamps and seeds germinated in the respective treatments (see below). Except for the UV-B radiation treatments,
radiation, temperature and other environmental variables were
ambient. Plants were watered as necessary to maintain soil
near field capacity and fertilized at regular intervals with a
commercial liquid fertilizer containing N,P,K (20,20,20) and
micronutrients. During the winter following the first growing
season, plants were transplanted to 6.6-l pots and the second
winter to 13.2-l pots. The pots were buried to ground level beneath the lamp frames and mulched to ensure ambient soil
temperatures.
For the greenhouse experiment, high-pressure sodium/high
intensity discharge lamps (1000 W, HPS/HID) extended the
photoperiod to 16 h during the growing season (May through
September) and offset shading due to the greenhouse structure. Day/night temperatures in the greenhouse during the
growing season were 23/17 °C. Maximum photosynthetically
active radiation (PAR; 400–700 nm) at the top of plants
ranged from 1800 µmol m – 2 s –1 on sunny days to 600 µmol
m – 2 s –1 on overcast days. To induce dormancy, supplemental
lighting and heat were turned off beginning in October of each
year and the greenhouse allowed to assume natural photoperiods and near ambient temperatures. Watering and fertilization were also reduced during this time. Normal growing
conditions were resumed the following May.
Ultraviolet-B radiation treatments—greenhouse experiment
Supplemental UV-B radiation was supplied over a 10-h period
centered on solar noon with Q-Panel UV-B-313 fluorescent
lamps (Q-Panel, Cleveland, OH) mounted in metal frames suspended above the pots and filtered with 0.13 mm cellulose
diacetate to remove UV-C radiation (transmission ≥ 292 nm)
(Booker et al. 1992). A 5-cm gap was left between the lamps
and filters to reduce the rate of filter degradation. The plants
were exposed to three UV-B radiation regimes (based on
UV-B irradiance at the summer solstice for Pullman, WA,
46°44′ N, 117°10′ W): ambient (1×), twice ambient (2×) or
three times ambient (3×) biologically effective UV-B radiation
(UV-BBE ). Biologically effective UV-B radiation (UV-BBE )
was based on the generalized plant action spectrum of Caldwell (1971) normalized to one at 300 nm. Ambient UV-BBE
measured in the field at the research site near the summer solstice with a spectroradiometer (Optronics 754, Optronics Laboratories, Orlando, FL) was 7.7 kJ m – 2 day –1. The different
UV-BBE irradiances were attained by varying the distance between the lamps and the plant canopy. A 10-h exposure was
used to accommodate the required daily irradiances for the 3×
treatment. Irradiance supplied by the lamps corresponded to
7.5, 16.0 and 21.8 kJ m – 2 day –1 UV-BBE for the 1×, 2× and 3×
treatments, respectively. The 2× treatment was based on recommendations of an expert panel sponsored by the U.S. Department of Energy (1993). The 3× treatment was used to examine the limits of UV-B radiation tolerance for these tree
species. There were no expectations that the 3× treatment
would represent a realistic increase in UV-B radiation in any
current scenario of projected stratospheric ozone depletion
(McKenzie et al. 2003). For each UV-B radiation treatment,
four Q-Panel UV-B-313 lamps were mounted at 0.35 m spacing on a 1.25 m × 1.25 m metal frame. Supplemental PAR and
UV-A (320–399 nm) were supplied by HPS/HID lamps suspended above the lamp frames. We measured PAR with a
Li-Cor 190-SB quantum sensor. Irradiance was 524 kJ m – 2
day – 1 in the UV-A waveband and 6251 kJ m – 2 day – 1 (39.5 mol
m – 2 day – 1) in the 400–700-nm waveband (PAR).
Cellulose diacetate filters were changed weekly to minimize
spectral changes associated with degradation of the plastic.
The filters were exposed to UV-B radiation for 6 h before being applied to the lamps to stabilize their spectral quality. Distance between lamps and plants was adjusted after each filter
change to maintain UV-B radiation at target values for each
treatment as measured at the mean plant height. For these adjustments, UV-B irradiation was measured with a broad-band
UV-B sensor (Ultraviolet Meter, Model 3D, Solar Light Co.,
Philadelphia, PA) calibrated against a spectroradiometer with
0.5-nm discrimination (Optronics 754, Optronics Laboratories, Orlando, FL). Treatments were screened from each other
with clear 0.13-mm polyester film (transmittance > 315 nm).
To minimize the effects of microenvironmental variation
among the treatments, the treatments as well as the plants
within treatments were rotated weekly within the greenhouse.
At the end of each growing season, UV-B irradiance was gradually reduced in concert with photoperiod reductions. Ambient treatments were maintained at mean winter values as calculated by the model of Green et al. (1980), modified by Björn
and Murphy (1985) (about 1.7 kJ m – 2 day – 1). In spring, the reverse process was followed. Further attributes of the lamp and
filter system, including ratios of UV-B:UV-A:PAR and effects
of filter aging on UV-B irradiance, have been described by
Bassman et al. (2002) and Warren et al. (2002b).
Ultraviolet-B radiation treatments—field experiment
Field experiments were conducted in an open area adjacent to
the greenhouses. Two treatments were examined: ambient
UV-BBE (1×) and twice-ambient (2×) UV-BBE radiation. A
modulated, constant addition system (Ashurst Design, Logan,
UT), similar to those described by Caldwell et al. (1983),
Sullivan et al. (1994a) and Booker et al. (1992), was used to
provide enhanced UV-B radiation. The system tracks ambient
UV-B radiation and adjusts output of lamps to compensate for
solar angle, cloud cover, filter degradation, lamp aging and
temperature. Fluorescent lamps (Q-Panel UV-B-313) supplied
UV-B radiation. Lamp fixtures were mounted in 1.2 m × 2.4 m
metal frames that were adjusted to maintain a constant height
above the plant canopies. The long axis of each frame was oriented east–west. Lamp spacing was 35 cm. For the 2× UV-B
radiation treatment, lamps were filtered with 0.13-mm thick
cellulose diacetate film. For the controls, lamps were filtered
with 0.13-mm thick polyester film (absorbs all radiation
< 320 nm). Therefore, control plants received only ambient solar UV-B radiation. Filters were replaced at about 3-week intervals. The lamp system was monitored and calibrated at each
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RESPONSE OF QUERCUS RUBRA TO UV-B RADIATION
filter change using an Optronics Model 754 spectroradiometer. The spectroradiometer was calibrated periodically
against a 200 W NIST traceable standard lamp (OL 752–10).
Before each use, wavelength alignment was calibrated against
mercury vapor emission lines (OL 752–150). Continuous
monitoring of solar UV radiation as input for the modulated
system was made with a Solar Light R-B meter calibrated
against the spectroradiometer as described by Booker et al.
(1992). The system was operated year-round. Detailed attributes of the radiation environment have been described by
Bassman et al. (2002) and Warren et al. (2002b).
Gas exchange determinations
Gas exchange measurements were made in late summer of
each year on a set of plants randomly selected from the greenhouse and field studies. Two different systems were employed.
The first was an open, compensating gas exchange system
(Model BI-7, Bingham Interspace, Logan, UT) connected to
an infrared gas analyzer (IRGA; Model 225 MK, Analytical
Development, Hoddesdon, U.K.) as described previously
(Bassman and Zwier 1991, Bassman et al. 2001). The second
system assessed photosynthesis based on 14C (see below).
Each plant typically produced two flushes of growth during
the summer. Using the IRGA system, leaves from each flush
were sampled with a portion of the leaf enclosed in a 300 cm3
stainless steel and glass cuvette. Net photosynthesis (Pn, µmol
CO2 m – 2 s –1), transpiration (K, mmol H2O m – 2 s – 1) and
stomatal conductance (gs, mmol H2O m – 2 s –1) were determined at leaf temperatures of 25 °C and minimal leaf-to-air
vapor density differences (VDD usually ≤ 5.0 g m – 3). Responses to PAR were made at intervals of 30 µmol m – 2 s – 1
from 0 to 150 µmol m – 2 s –1 and at 100 µmol m – 2 s – 1 intervals
from 200 through 1000 µmol m – 2 s –1. A 1000 W HPS/HID
lamp was used to supply different irradiances of PAR by varying lamp height above the cuvette. Carbon dioxide exchange
rates in the dark were used as a measure of dark respiration (Rd,
µmol CO2 m – 2 s –1). Regressions of irradiance and net carbon
dioxide exchange over the range of 0 to 200 µmol m – 2 s – 1 PAR
were used to determine light compensation points (LCP, µmol
m – 2 s –1) and quantum yield (Φ, µmol CO2 µmol – 1 photons).
Quantum yield was calculated as the slope, and LCP as the
x-intercept of these regressions (Björkman 1981, Long and
Hällgren 1987). Light response curves were generated by plotting Pn as a function of PAR. These curves were fitted to a
model of the form:
Pn = Pmax (1 − e – ( Φ* PAR)) – Rd
(1)
where Pmax = maximum rate of photosynthesis and other terms
are as previously defined (Landsberg 1977). All other gas exchange parameters were determined as described in Bassman
and Zwier (1991). Net photosynthesis was light saturated at
PAR ≥ 600 µmol m – 2 s –1. Consequently, gas exchange variables averaged for PAR ≥ 600 µmol m – 2 s –1 were used to compare treatment effects at saturating or near saturating
irradiances. Following gas exchange measurements, leaf area
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enclosed in the cuvette was measured with a leaf area meter
(Delta-T Devices, Cambridge, U.K.) and photosynthesis expressed on an area basis.
During the third year of the field study, in situ measurements
of photosynthesis were made on field plants with a portable
14
CO2 gassing device, slightly modified in design from those
described by Michael et al. (1985) and McWilliam et al.
(1973). Details of the method and calculations have been described by Michael et al. (1985). Measurements of 14C-photosynthesis were made during clear midday periods with plants
removed from under the lamp frames. Concurrent measurements of PAR, leaf temperature and atmospheric humidity
were made at the time of 14C exposure. A portion of the leaf
midway between the tip and base was clamped between the
upper and lower treatment chambers. The cuvette was tilted at
an angle normal to the sun and air containing 350 cm3 m – 3 CO2
(specific activity 216.7 MBq m – 3 14CO2) was passed through
the chamber (flow rate = 1.33 cm3 s – 1) and over both surfaces
of the leaf for 30 s. Immediately following exposure, a
0.528 cm2 section was cut from the exposed portion of each
leaf with a cork borer. Each section was immediately placed in
a scintillation vial containing 1.5 cm3 BTS tissue solubilizer
(Beckman Instruments, Fullerton, CA) and taken to the laboratory for assay of radioactivity. To remove color, 0.5 ml of
H2O2 was added to each vial and the leaf segments digested for
24 h at 50 °C. After cooling for at least 30 min, three drops of
glacial acetic acid and 17 ml of ScintiVerse II (Fisher Scientific, Fair Lawn, NJ) liquid scintillation cocktail were added to
each vial. Following an additional 24-h dark equilibration period, radioactivity of the samples was determined with a
Packard 1900CA liquid scintillation spectrometer (Packard
Instrument Co., Meriden, CT). The rate of photosynthesis,
based on sample dpm, was calculated as described by Michael
et al. (1985). Values determined by this technique closely
compared with those obtained by IRGA methods, but tend to
be about 5% higher. They are considered an approximation of
gross (Pg) rather than net (Pn ) photosynthesis (Michael et al.
1985) and are termed apparent photosynthesis (PA ).
Growth and biomass distribution
Total height and diameter were measured weekly or bi-weekly
on all plants during each growing season. During late summer
of each year, a subsample of plants from both the greenhouse
and field studies was harvested for intermediate growth and
biomass determinations. Final harvests were conducted at the
end of the third growing season. Heights, diameters and distribution of biomass within plants were determined immediately
following gas exchange measurements. Plants were partitioned into leaves (main stem leaves, lateral branch leaves),
stem (main stem and lateral branches) and roots. Each biomass
component was further partitioned into within- and betweenyear growth flushes. Before drying, leaf area for each foliage
component was determined with a leaf area meter. Biomass
components were dried separately at 70 °C to constant mass
and weighed. Shoot to root ratios (mass basis) were calculated
for each plant.
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Pigment analysis
2
At harvest, two samples from each flush (1.0 cm each) of
leaves on each plant were excised. One sample was placed in a
light-proof scintillation vial containing 5.0 ml N,N-dimethylformamide (DMF) and stored in the dark for 24 h at 4 °C. Total
chlorophyll, chlorophyll a and chlorophyll b were determined
after extraction as described by Inskeep and Bloom (1985).
The second sample was placed in a 20-ml test tube for determination of methanol-extractable UV-absorbing compounds.
Samples were dried at 95 °C for at least 24 h, then ground in a
tissue homogenizer in 10 ml of methanol:H2O:HCl (70:29:1,
v/v). The extract was centrifuged at 600 g for 10 min and
absorbance of the supernatant determined spectrophotometrically at 290, 300 and 310 nm. Relative absorbance, calculated
on a leaf area basis, was used as an index of UV-absorbing
compounds (Robberecht and Caldwell 1986).
Experimental design and data analysis
For the greenhouse study, variation in germination resulted in
establishment of between 47 and 49 plants per treatment. In
the field, 93 to 95 seedlings germinated. Individual plants were
treated as independent replicates within treatments. The number of single-plant replications available for weekly measurements in each treatment varied depending on survival and
previous harvesting. Four to 12 plants were selected from each
treatment each year for gas exchange and harvest. Plants selected were based on uniformity in size and appearance. Exterior border trees were excluded. Data were treated as a
completely randomized design and subjected to one-way analysis of variance (ANOVA) or regression analysis (GLM procedure) using the SAS statistical package (SAS Institute, Cary,
NC). Where appropriate, error terms were partitioned with a
nested ANOVA model (e.g., plants within treatment, leaves
within plants, etc.). Individual means were compared with
Duncan’s Multiple Range Test and differences were considered significant at P ≤ 0.05. For details of the study design see
Bassman et al. (2002).
Results
Growth
During the first year of the greenhouse experiments, height
growth of trees in the 2× treatment lagged behind that in the
ambient UV-B radiation and 3× treatments during the first
flush, but exceeded height growth of trees in these treatments
during the second flush (Figure 1). Consequently, trees in the
2× treatment were significantly taller than trees in the ambient
and 3× treatments at the end of the first year (Figure 1). Trees
in the 2× treatment began the second year taller than trees in
the ambient and 3× treatments, but grew little during the second flush that year. By Year 2, there were no significant treatment differences in height growth, a trend that continued
throughout Year 3 (Figure 1). In the field experiments, patterns
of height growth were similar for trees in the ambient and 2×
treatments throughout all three years (Figure 1). Patterns in diameter growth mirrored patterns in height growth in both the
greenhouse and field studies.
Biomass distribution
In the greenhouse study, trees in the 2× treatment produced
less leaf area and biomass on lateral branches than trees in ambient UV-B radiation. This contributed to a lower total leaf
biomass in 2× trees compared with trees in ambient UV-B radiation (P = 0.102 second year; P = 0.125 third year; Figure 2).
Leaf biomass on lateral branches was also less for trees in the
3× treatment during the second year (P = 0.077), but not in the
Figure 1. Weekly heights of
Quercus rubra seedlings subjected to ambient (䊉 = 1×),
double ambient (䊐 = 2×) or
triple ambient (䉭 = 3×) UV-B
over 3 years in a greenhouse
and a field trial. Values are the
range of sample sizes (n) measured, which varied as plants
were removed for destructive
harvests. Vertical lines represent ± 1 SE of the mean. Representative differences
between treatments are indicated by letters stacked vertically near data points.
Treatments with different letters were significantly different (P ≤ 0.05) according to
Duncan’s Multiple Range Test.
Abbreviation: N.S. = not significant.
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RESPONSE OF QUERCUS RUBRA TO UV-B RADIATION
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Figure 2. Effects of UV-B radiation on
biomass distribution in Quercus rubra
seedlings subjected to ambient, 2× ambient or 3× ambient UV-B radiation for
Pullman, WA. Values are the means of
measurements of 8–12 replicate trees
(n) per treatment ± 1 SE of the mean
(vertical lines). Bars with different letters for the same condition (field or
greenhouse), parameter and year are
significantly different (P 0.05) according to Duncan’s Multiple Range
Test. Abbreviation: N.S. = not significant.
third year; total leaf biomass was similar for 3× trees and those
in ambient UV-B radiation (Figure 2).
Lateral stem biomass was reduced on 2× trees compared
with trees in ambient UV-B radiation during the second and
third year of the greenhouse study, but this resulted in no significant reduction in total stem biomass (Figure 2). The 3×
treatment had no effect on stem biomass (Figure 2). The 2×
treatment slightly reduced aboveground biomass in Years 2
and 3 (P = 0.131), whereas the 3× treatment had no effect on
aboveground biomass. Root biomass was significantly reduced by both 2× and 3× treatments during the first year, but
not during Years 2 and 3 (Figure 2). Total plant biomass did
not differ significantly among treatments during any year of
the greenhouse study (Figure 2) although shoot:root ratios
were reduced in the 2× plants in Years 1 and 2.
In the field study, lateral leaves (P = 0.058), lateral stem (P =
0.107) and lateral leaf area (P = 0.062) were all reduced by the
2× treatment during the first year, but not in subsequent years.
Otherwise, enhanced UV-B radiation had no effect on biomass
production and distribution (Figure 2).
Gas exchange
In the greenhouse study, rates of Pn at saturating irradiances
were higher in 3× trees than in ambient and 2× trees during the
first (P = 0.0931) and second (P < 0.05) years, but not the third
year (Figure 3). Compared with ambient and 2× trees, dark Rd
were also significantly higher in 3× trees during Years 1 and 3,
but not in Year 2 (Figure 3). There were no significant treatment effects on K during the three years of study, but gs was
significantly higher in 2× and 3× trees than in trees in the ambient UV-B regime during Year 2 (Figure 3). Compared with
trees in ambient UV-B radiation, water-use efficiency (WUE)
was higher in both 2× (not significant) and 3× trees during
Year 1 and in 3× trees during the Year 2; however, there were
no significant differences during Year 3 (Figure 3). Leaf inter-
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Figure 3. Photosynthesis, dark respiration, leaf conductance and instantaneous water-use efficiency by first
flush leaves of Quercus rubra seedlings subjected to ambient, 2× ambient
or 3× ambient UV-B radiation for Pullman, WA. Values for the greenhouse
for Years 1 and 2 represent net photosynthesis determined by infrared gas
analysis. Values for Year 3 in the field
represent apparent photosynthesis determined by 14CO2. No accessory gas
exchange measurements were made for
these plants. All determinations were
made under saturating
photosynthetically active radiation with
other environmental conditions described in the text. Values are means of
measurements of 4–8 replicate trees
(n) per treatment ± 1 SE of the mean
(vertical lines). Bars with different letters for the same condition (field or
greenhouse) and parameter are significantly different (P ≤ 0.05) according to
Duncan’s Multiple Range Test. Abbreviation: N.S. = not significant.
nal CO2 concentrations (Ci) were greater for 2× trees and less
for 3× trees compared with trees in ambient UV-B radiation
during Year 2. Otherwise there were no significant differences
in Ci among the treatments (data not shown). In the field study,
Rd was greater in 2× trees for first flush leaves during Year 2,
otherwise there were no significant treatment differences in
any gas exchange variables for first flush leaves (Figure 3).
Detailed responses of photosynthesis to irradiance were
evaluated in greenhouse-grown trees during the first year of
the study and are reported in Bassman et al. (2003). Enhanced
UV-B radiation had no effect on the shape of the light response
curve. Apparent quantum yields were reduced in 3× trees compared with ambient and 2× trees during Year 1 (Table 1). During Year 2, Φ was lower in 2× trees than in ambient and 3×
plants; however, there were no differences between treatments
during Year 3 (Table 1). Light compensation points were less
for 2× trees than for ambient and 3× trees during Years 2 and 3.
During Year 3, LCPs increased with increasing UV-B irradiance (Table 1). In the field study, there were no significant
treatment differences in Φ or LCP in Year 1. Apparent quan-
tum yields were similar, but LCPs were higher in 2× trees
during Year 2 (Table 1).
Leaf pigments
In the greenhouse study, chlorophylls a and b and total chlorophyll were generally higher in 2× and 3× trees than in trees in
ambient UV-B radiation during Year 1. In Year 2, chlorophyll
in first flush leaves was unaffected by the treatments, but was
increased by the 3× treatment in second flush leaves. No differences were detected during Year 3. Ratios of chlorophyll a:chlorophyll b in greenhouse plants were unaffected by
the treatments in all years. In the field study, chlorophyll concentrations were similar in ambient and 2× trees in all study
years (data not shown).
Methanol-extractable UV-absorbing compounds (A300) in
greenhouse trees were similar between treatments during
Year 1 (Figure 4). There were no significant differences within
either flush during Year 2. However, when both flushes were
combined, 2× trees had lower amounts of UV-absorbing compounds than either ambient or 3× trees. In Year 3, UV-absorb-
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Table 1. Effects of UV-B radiation on apparent quantum yield (Φ, µmol CO2 µmol – 1 photons) and light compensation point (LCP, µmol photons
m – 2 s –1) in Quercus rubra seedlings (n = 28 per treatment). Values followed by different letters in the same column for the same experimental conditions (greenhouse or field) are significantly different (P ≤ 0.05). Abbreviation: N.A. = not measured.
Treatment
Quantum yield (Φ)
Light compensation point (LCP)
Year 1
Year 2
Year 3
Year 1
Year 2
Year 3
Greenhouse
Ambient
2× Ambient
3× Ambient
0.0335 a
0.0334 a
0.0279 b
0.0211 a
0.0135 b
0.0241 a
0.0314 a
0.0329 a
0.0305 a
20 a
12 b
23 a
13 a
8b
17 a
19 c
27 b
43 a
Field
Ambient
2× Ambient
0.0474 a
0.0346 a
0.0345 a
0.0358 a
N.A.
N.A.
21 a
28 a
25 b
40 a
N.A.
N.A.
ing compounds in first flush leaves were higher in 3× trees
than in ambient and 2× trees (Figure 4); there were no treatment differences in UV-absorbing compounds in second flush
leaves or when both flushes were combined.
In the field study, amounts of UV-absorbing compounds
were similar among treatments during Year 1, but 2× trees had
higher amounts of UV-absorbing compounds in first flush
leaves during Year 2 (Figure 4). There were no significant differences between treatments in second flush leaves, but when
both flushes were combined, UV-absorbing compounds were
significantly greater in 2× trees than in ambient trees (not
shown). No significant differences in UV-absorbing compounds between treatments were observed during Year 3.
Discussion
Figure 4. Relative absorbance of methanol extracts at 300 nm (A300;
UV-absorbing compounds) in Quercus rubra seedlings subjected to
ambient, 2× ambient or 3× ambient UV-B radiation for Pullman, WA.
Values are means from first flush leaves of 4–14 replicate trees (n) per
treatment ± 1 SE of the mean (vertical lines). Bars with different letters for the same condition (field or greenhouse) and year are significantly different (P ≤ 0.05) according to Duncan’s Multiple Range
Test.
The study trees typically produced two and occasionally three
flushes of growth during a growing season. Consequently,
each flush of leaves was exposed to higher doses of UV-B radiation for a longer period of time than for the leaves of an equivalent indeterminate angiosperm species such as Populus trichocarpa Torr. & A. Gray, which we evaluated by similar
protocols (Bassman et al. 2001). Nevertheless, enhanced
UV-B radiation was generally not deleterious to the growth
and physiology of Q. rubra, even when supplied at high rates
and for a long time.
In part, the resistance of Q. rubra to UV-B may be associated with the high constitutive amounts of UV-absorbing compounds in leaves. Although we observed some stimulation of
methanol-extractable UV-absorbing compounds in the greenhouse and field studies, in many cases enhanced UV-B radiation had no effect on these compounds. Oaks have high
concentrations of phenylpropanoids that are probably effective anti-herbivore compounds (Feeny 1969, 1970). Previously, we found that total flavonoid concentration in Q. rubra
was more than twice that of the other tree species evaluated,
with the predominant compound nearly 20 times (by mass)
that of any eluted compound from any of the other species
(Warren et al. 2002b). As in the present study, enhanced UV-B
radiation had no effect on total flavonoids, but three individual
compounds showed decreased concentrations and one compound an increased concentration in response to enhanced
UV-B radiation (Warren et al. 2002b). Enhanced UV-B radiation also resulted in a change in flavonoid composition, with
fewer early eluting compounds and more late eluting compounds (Warren et al. 2002b).
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Enhanced UV-B radiation can also affect plant morphology,
which in turn affects penetration of UV radiation to sensitive
tissue. Antonelli et al. (1998) reported that enhanced UV-B radiation increases leaf thickness and accumulation of phenolic
compounds in cell walls of adaxial epidermis tissue of Quercus robur L. Oak leaves produce abundant surface trichomes
(Karabourniotis et al. 1992) which contain considerable quantities of phenolics (Karabourniotis et al. 1998, Skaltsa et al.
1994) and significantly attenuate UV-B radiation even before
it encounters the leaf epiderms (Karabourniotis and Bornman
1999, Karabourniotis et al. 1992, Skaltsa et al. 1994). Enhanced UV-B radiation can stimulate trichome production in
Q. rubra seedlings (Nagel et al. 1998). Trichome density varies with radiation environment in Quercus coccifera L. and
Quercus ilex L. (Liakoura et al. 1997) and shade leaves have
lower amounts of UV-absorbing compounds than sun leaves
(Filella and Penuelas 1999, Liakoura et al. 2003). Whatever
the specific changes in UV-absorbing compounds, Q. rubra
appears well protected against the adverse effects of enhanced
UV-B radiation.
In many species, enhanced UV-B radiation reduces growth,
often accompanied by reduced leaf area and changes in carbon
allocation and partitioning (Bassman 2004, Caldwell et al.
2003). However, growth and biomass may also be increased in
response to enhanced UV-B radiation (Caldwell et al. 2003).
Our results are consistent with several studies on angiosperm
tree species that show minimal effects of enhanced UV-B radiation on growth and biomass allocation. For example, Sullivan
et al. (1994b) found that biomass of Liquidambar styraciflua L. seedlings was unaffected by supplemental UV-B radiation applied for two years in field conditions. However, these
seedlings exhibited subtle changes in carbon allocation and
growth. Final leaf size was unaffected, but rates of leaf elongation and accumulation of leaf area were lower in leaves exposed to enhanced UV-B radiation (Dillenburg et al. 1995).
DeLucia et al. (1994) reported that supplemental UV-B radiation had no effect on growth of Amelanchier arborea
(Michx. f.) Fern., Betula papyrifera Marsh., Nyssa sylvatica
Marsh. and Robinia pseudoacacia L. Total biomass, plant
height and leaf area were significantly reduced in Cercis canadensis L. and Morus alba L. However, there was no clear demarcation of response based on the shade tolerance of the
species evaluated. Cybulski and Peterjohn (1999) reported no
effects on aboveground biomass in Q. rubra subjected to zero
or ambient UV-B radiation. Enhanced UV-B radiation decreased growth rates and leaf area in Betula pubescens J. F.
Ehrh. in greenhouse conditions, but not in the field (Weih et al.
1998). In B. pendula enhanced UV-B reduced height and diameter beginning in the third year, whereas biomass and other
parameters remained unchanged (Tegelberg et al. 2001).
Values for most of the gas exchange variables that we observed were in the range reported by other studies of oaks for
Pn (Hanson et al. 1988, Weber and Gates 1990, McGraw et al.
1990, Kruger and Reich 1993a, 1993b), gs (Kubiske and
Abrams 1992, Kruger and Reich 1993a, Hanson et al. 1994)
and Rd (Heichel and Turner 1983, Hanson et al. 1988, McGraw
et al. 1990), but our WUE values were higher (Ni and Pallardy
1991). Enhanced UV-B radiation either had no effect or
slightly increased Pn (Figure 2). In Quercus gambelii Nutt., enhanced UV-B radiation increased photosynthesis on a leaf area
basis, but not on a leaf mass basis (Harley et al. 1996). In
Q. robur, enhanced UV-B radiation had no effects on photosynthesis (Antonelli et al. 1998), but in many other species
photosynthesis is reduced by enhanced UV-B radiation, usually in conditions of high ratios of UV-B:PAR (Fiscus and
Booker 1995). However, Bassman et al. (2001) observed stimulation of photosynthesis by enhanced UV-B radiation in
Populus deltoides Bartr. ex Marsh and similar effects have also
been recorded for Acer rubrum L., Liquidambar styraciflua
(Sullivan et al. 2003) and Picea engelmannii Parry ex Engelm
(Bassman et al. 2003), but not in Liriodendron tulipifera L.
(Sullivan et al. 2003), Populus trichocarpa (Bassman et al.
2003) or Pseudotsuga menziesii (Mirb.) Franco (Bassman et
al. 2002). Sullivan et al. (2003) suggested that photosynthetic
enhancement by UV-B radiation in Acer rubrum could be due
to enhanced blue light absorption or fluorescence induced by
UV-B radiation absorbance by hydroxycinnamates (HCAs).
Although we did not assay these compounds in the present
study, phenolic profiles observed in earlier studies on Q. rubra
imply that HCAs could play a role in this species (Warren et al.
2002b). The high concentration of leaf phenolics likely prevented damage to the photosynthetic apparatus.
Effects on photochemistry associated with photosynthesis
were inconclusive. In contrast to other angiosperms (Bassman
et al. 2003, Sullivan et al. 2003) and some gymnosperms
(Bassman et al. 2003), enhanced UV-B radiation had no significant effect on the shape of the light response curve. Greenhouse-grown plants sometimes displayed a depression in Φ in
enhanced UV-B radiation (see Table 1); however, no such effects were seen in field-grown plants. Light compensation
points were reduced in some cases, but increased in others. In
total, the data suggest no significant impact of UV-B radiation
on the photosynthetic apparatus, which is consistent with conclusions reached by Sullivan et al. (2003) for some other angiosperm tree species. Bassman et al. (2003) found that
changes in Φ and LCPs accompanied changes in Pn associated
with enhanced UV-B radiation in three of five tree species
(Bassman et al. 2003). In other tree species, Φ was unaffected
(Naidu et al. 1993, Dillenburg et al. 1995) or significantly reduced (Sullivan and Teramura 1989) by enhanced UV-B radiation and negative effects on photochemistry have been
reported for Picea abies L. grown in a greenhouse (Bavcon et
al. 1996, Pukacki and Modrzynski 1998). Bassman et al.
(2002) observed increases in both Φ and LCPs in Pseudotsuga
menziesii in enhanced UV-B radiation.
Enhanced UV-B radiation either had no significant effect or
increased dark respiration rates in both greenhouse and field
plants. Increased Rd may be related to higher metabolic rates
associated with conversion of carbon to secondary compounds
because they corresponded to those cases where UV-absorbing
compounds also increased (see Figures 2 and 4). Enhanced
UV-B radiation did not affect Rd in a range of crop plants
(Teramura et al. 1980, Marke and Tevini 1996, Hunt and
McNeil 1998), but small increases were seen in Rumex pat-
TREE PHYSIOLOGY VOLUME 26, 2006
RESPONSE OF QUERCUS RUBRA TO UV-B RADIATION
entia L. (Sisson and Caldwell 1976). In other tree species,
UV-B radiation had no effect (Schumaker et al. 1997, Bassman
et al. 2001, 2003) or increased Rd (Bassman et al. 2002, 2003).
Slight increases in Pn relative to K in the first two years accounted for the improved instantaneous WUE observed for
greenhouse plants grown in enhanced UV-B radiation (see
Figure 2). Although UV-B radiation may have direct effects on
gs (Allen et al. 1998, Nogués et al. 1998), the observed changes
in WUE were probably insufficient to substantially affect
changes in drought resistance as observed for some Mediterranean pines (Petropoulou et al. 1995) and pea plants (Nogués et
al. 1998). Keiller and Holmes (2001) suggested that changes in
WUE were a significant factor in plant response to UV-B radiation. In greenhouse conditions, enhanced UV-B radiation resulted in higher WUEs in Pinus ponderosa Dougl. ex P. Laws
& C. Laws (Bassman et al. 2003) and Populus deltoides (Bassman et al. 2001), but reduced WUEs in Populus trichocarpa
(Bassman et al. 2003). Under field conditions, WUEs increased in Acer rubrum and Liriodendron tulipera, but not in
Liquidambar styriciflua (Sullivan et al. 2003).
The use of constant, day-long UV-B irradiation, as employed in our greenhouse study, usually produce higher daily
and seasonal UV radiation doses because there is no compensation for changing solar angles or deviations from clear sky
conditions (see Sullivan et al. 1994a, Bassman et al. 2002).
However, even though our greenhouse plants probably received higher annual doses than the treatments suggest, midday irradiance environments were similar between greenhouse
and field experiments (Bassman et al. 2002). Nevertheless, the
lamps used to supply both UV-B radiation and PAR may have
confounded the results. As the filters aged, UV-B radiation
may have been reduced by 40% or more between changes for
the greenhouse lamp system (Warren et al. 2002a). Consequently, the mean dose supplied to plants was less than the normal dose. Because lamp outputs were less in the field, filter
aging imposed less than a 10% reduction in UV-B irradiance
between filter changes (Warren et al. 2003). The UV-B 313
lamps emit considerable quantities of radiation in the UV-A
and blue light wave bands, possibly sufficient to drive low
irradiance blue light responses (including photorepair) (Jolley
et al. 1987, Adamse et al. 1994, Sullivan et al. 2003, Krizek
2004) and the lack of response in growth and chlorophyll data
suggest this might be the case. These would likely have been
greater in the greenhouse study because of the closer proximity of plants to lamps in the higher UV-B irradiance treatments.
Still, most of the significant effects we observed occurred in
the greenhouse study and at the higher UV-B irradiances, consistent with the long-standing observation that effects of UV-B
radiation are exaggerated in greenhouse experiments (Caldwell et al. 2003). This is in contrast to our results for Pseudotsuga menziesii in which the direction and magnitude of
changes were similar between greenhouse and field plants
(Bassman et al. 2002).
Despite UV-B irradiation regimes that resulted in doses
much higher than might be expected in the worst-case environment change scenarios, long-term exposure to enhanced UV-B
radiation had little effect on photosynthesis and growth in
1161
northern red oak, which has a determinate (multiple flushing)
shoot growth pattern. Leaves of Q. rubra possess large quantities of phenolic compounds combined with surface trichomes
that effectively limit the penetration of UV-B radiation, thus
minimizing its potential adverse effects. However, other processes (e.g., effective photorepair) may also contribute resistance to enhanced UV-B radiation. Based on three years of
data from greenhouse and field experiments, we conclude that
even substantial increases in UV-B radiation are unlikely to
have cumulative, deleterious effects on the growth of Q. rubra.
Acknowledgments
The authors thank Gary Radamaker and Jeffrey Warren for assisting
in maintenance of plants and the UV-B irradiation systems throughout
the study. Dr. Warren’s assistance with the spectral irradiance measurements is gratefully acknowledged. This material is based on work
sponsored by the Cooperative State Research Service, United States
Department of Agriculture under Agreement 94-37100-0312. Research was also supported by the Agricultural Research Center, College of Agriculture and Home Economics, Washington State
University under Project 0113 (J.H.B.). Any opinions, findings, conclusions or recommendations are those of the authors and do not necessarily reflect the view of the United States Department of
Agriculture.
References
Adamse, P., S.J. Britz and C.R. Caldwell. 1994. Amelioration of
UV-B damage under high irradiance. II. Role of blue light photoreceptors. Photochem. Photobiol. 60:110–115.
Allen, D.J., S. Nogués and N.R. Baker. 1998. Ozone depletion and increased UV-B radiation: is there a real threat to photosynthesis?
J. Exp. Bot. 49:1775–1788.
Antonelli, F., F. Bussotti, D. Grifoni, P. Grossoni, B. Mori, C. Tani and
G. Zipoli. 1998. Oak (Quercus robur L.) seedlings responses to a
realistic increase in UV-B radiation under open space conditions.
Chemosphere 36:841–845.
Bassman, J.H. 2004. Ecosystem consequences of enhanced solar ultraviolet radiation: secondary plant metabolites as mediators of
multiple trophic interactions in terrestrial plant communities.
Photochem. Photobiol. 79:382–398.
Bassman, J.H. and J.C. Zwier. 1991. Gas exchange characteristics of
Populus trichocarpa, Populus deltoides and Populus trichocarpa ×
P. deltoides clones. Tree Physiol. 8:145–159.
Bassman, J.H., R. Robberecht and G. Edwards. 2001. Effects of enhanced UV-B radiation on growth and gas exchange in Populus
deltoides Bartr. ex Marsh. Int. J. Plant Sci. 162:103–110.
Bassman, J.H., G.E. Edwards and R. Robberecht. 2002. Long-term
exposure to enhanced UV-B radiation is not detrimental to growth
and photosynthesis in Douglas-fir. New Phytol. 154:107–120.
Bassman, J.H., G.E. Edwards and R. Robberecht. 2003. Photosynthesis and growth in seedlings of five forest tree species with contrasting leaf anatomy subjected to supplemental UV-B radiation. For.
Sci. 49:176–187.
Bavcon, J., A. Gaberscik and F. Batic. 1996. Influence of UV-B radiation on photosynthetic activity and chlorophyll fluorescence kinetics in Norway spruce [Picea abies (L.) Karst.] seedlings. Trees 10:
172–176.
TREE PHYSIOLOGY ONLINE at http://heronpublishing.com
1162
BASSMAN AND ROBBERECHT
Björkman, O. 1981. Responses to different quantum flux densities. In
Physiological Plant Ecology I. Responses to the Physical Environment. New Series. Vol. 12A. Encyclopedia of Plant Physiology.
Eds. O.L. Lange, P.S. Nobel, C.B. Osmond and H. Ziegler.
Springer-Verlag, Berlin, pp 57–108.
Björn, L.O. and T.M. Murphy. 1985. Computer calculation of solar
ultraviolet radiation at ground level. Physiol. Veg. 23:555–561.
Booker, F.L., E.L. Fiscus, R.B. Philbeck, A.S. Heagle, J.E. Miller and
W.W. Heck. 1992. A supplemental ultraviolet-B radiation system
for open-top field chambers. J. Environ. Qual. 21:56–61.
Caldwell, M.M. 1971. Solar UV irradiation and the growth and development of higher plants. In Photophysiology. Vol. 6. Ed. A.C.
Giese. Academic Press, New York, pp 131–177.
Caldwell, M.M., W.G. Gold, G. Harris and C.W. Ashurst. 1983. A
modulated lamp system for solar UV-B (280–320 nm) supplementation studies in the field. Photochem. Photobiol. 37:479–485.
Caldwell, M.M., C.L. Ballaré, J.F. Borman, S.D. Flint, L.O. Björn,
A.H. Teramura, G. Kulandaivelu and M. Tevini. 2003. Terrestrial
ecosystems, increased solar ultraviolet radiation and interactions
with other climatic change factors. Photochem. Photobiol. Sci. 2:
29–38.
Cybulski, W.J. and W.T. Peterjohn. 1999. Effects of ambient UV-B radiation on the above-ground biomass of seven temperate-zone
plant species. Plant Ecol. 145:175–81.
Day, T.A., G. Martin and T.C. Vogelmann. 1993. Penetration of UV-B
radiation in foliage: evidence that the epidermis behaves as a
non-uniform filter. Plant Cell Environ. 16:735–741.
DeLucia, E.H., S.L. Naidu and J. Chen. 1994. Effects of simulated
stratospheric ozone depletion on seedling growth of several species
of hardwood trees. Erigenia 13:132–140.
Dillenburg, L.R., J.H. Sullivan and A.H. Teramura. 1995. Leaf expansion and development of photosynthetic capacity and pigments in
Liquidambar styraciflua (Hamamelicaceae)—effects of UV-B radiation. Am. J. Bot. 82:878–885.
Feeny, P.P. 1969. Inhibitory effect of oak leaf tannins on the hydrolysis of proteins by trypsin. Phytochemistry 8:2119–2126.
Feeny, P.P. 1970. Seasonal changes in oak leaf tannins and nutrients as
a cause of spring feeding by winter moth caterpillars (Operophtera
brumata ). Ecology 51:565–581.
Filella, I. and J. Penuelas. 1999. Altitudinal differences in UV absorbance, UV reflectance and related morphological traits of Quercus
ilex and Rhododendron ferrugineum in the Mediterranean region.
Plant Ecol. 145:157–65.
Fiscus, E.L. and F.L. Booker. 1995. Is increased UV-B a threat to crop
photosynthesis and productivity? Photosynth. Res. 43:81–92.
Green, A.E.S., K.R. Cross and L.A. Smith. 1980. Improved analytic
characterization of ultraviolet skylight. Photochem. Photobiol. 31:
59–65.
Hanson, P.J., J.G. Isebrands, R.E. Dickson and R.K. Dixon. 1988.
Ontogenetic patterns of CO2 exchange of Quercus rubra L. leaves
during three flushes of shoot growth I. Median flush leaves. For.
Sci. 34:55–68.
Hanson, P.J., L.J. Samuelson, S.D. Wullschleger, T.A. Tabberer and
G.S. Edwards. 1994. Seasonal patterns of light-saturated photosynthesis and leaf conductance for mature and seedling Quercus
rubra L. foliage: differential sensitivity to ozone exposure. Tree
Physiol. 14:1351–1366.
Harley, P., G. Deem, S. Flint and M. Caldwell. 1996. Effects of growth
under elevated UV-B on photosynthesis and isoprene emission in
Quercus gambelii and Mucuna pruriens. Global Change Biol. 2:
149–154.
Heichel, G.H. and N.C. Turner. 1983. CO2 assimilation of primary
and regrowth foliage of red maple (Acer rubrum L.) and red oak
(Quercus rubra L.): response to defoliation. Oecologia 57:14–19.
Hunt, J.E. and D.L. McNeil. 1998. Nitrogen status affects UV-B sensitivity of cucumber. Aust. J. Plant Physiol. 25:79–86.
Inskeep, W.P. and P.R. Bloom. 1985. Extinction coefficients of chlorophyll a and b in N,N-dimethyl-formamide and 80% acetone.
Plant Physiol. 77:484–485.
Jolley, V.D., J.C. Brown, J.C. Pushnik and G.W. Miller. 1987. Influences of ultra-violet (UV)-blue light radiation on the growth of cotton. I. Effects on iron nutrition and iron stress resoponse. J. Plant
Nutr. 10:333–351.
Karabourniotis, G. and J.F. Bornman. 1999. Penetration of UV-A,
UV-B and blue light through the leaf trichome layers of two xeromorphic plants, olive and oak, measured by optical fibre microprobes. Physiol. Plant. 105:655–661.
Karabourniotis, G., K. Papadopoulos, M. Papamarkou and Y. Manetas. 1992. Ultraviolet-B radiation absorbing capacity of leaf hairs.
Physiol. Plant. 86:414–418.
Karabourniotis, G., G. Kofidis, C. Fasseas, V. Liakoura and I. Drossopoulos. 1998. Polyphenol deposition in leaf hairs of Olea europaea
(Oleaceae) and Quercus ilex (Fagaceae). Am. J. Bot. 85:
1007–1012.
Keiller, D.R. and M.G. Holmes. 2001. Effects of long-term exposure
to elevated UV-B radiation on the photosynthetic performance of
five broad-leaved tree species. Photosynth. Res. 67:229–240.
Krizek, D.T. 2004. Influence of PAR and UV-A in determining plant
sensitivity and photomorphogenic responses to UV-B radiation.
Photochem. Photobiol. 79:307–15.
Kruger, E.I. and P.B. Reich. 1993a. Coppicing alters ecophysiology
of Quercus rubra saplings in Wisconsin forest openings. Physiol.
Plant. 89:741–750.
Kruger, E.L. and P.B. Reich. 1993b. Coppicing affects growth, root:
shoot relations and ecophysiology of potted Quercus rubra seedlings. Physiol. Plant. 89:751–760.
Kubiske, M.E. and M.D. Abrams. 1992. Photosynthesis, water relations, and leaf morphology in xeric versus mesic Quercus rubra
ecotypes in central Pennsylvania in relation to moisture stress. Can.
J. For. Res. 22:1402–1407.
Landsberg, J.J. 1977. Some useful equations for biological studies.
Exp. Agric. 13:273–286.
Liakoura, V., M. Stefanou, Y. Manetas, C. Cholevas and G. Karabourniotis. 1997. Trichome density and its UV-B protective potential are affected by shading and leaf position on the canopy.
Environ. Exp. Bot. 38: 223–29.
Liakoura, V., J.E. Bornman and G. Karabourniotis. 2003. The ability
of abaxial and adaxial epidermis of sun and shade leaves to attenuate UV-A and UV-B radiation in relation to the UV absorbing capacity of the whole leaf methanolic extracts. Physiol. Plant. 117:
33–43.
Long, S.P. and J.-E. Hällgren. 1987. Measurement of CO2 assimilation in plants in the field and the laboratory. In Techniques in
Bioproductivity and Photosynthesis. Eds. J. Coombs, D.O. Hall,
S.P. Long and J.M.O. Scurlock. Pergamon Press, Oxford, pp
62–94.
Lumsden, P., Ed. 1997. Plants and UV-B: responses to environmental
change. Cambridge University Press, Cambridge, U.K., 355 p.
Marke, U. and M. Tevini. 1996. Combination effects of UV-B radiation and temperature on suflower (Helianthus annus L., cv. ‘Polstar’) and maize (Zea mays L., cv. ‘Zenit’ 2000) seedlings. J. Plant
Physiol. 148:49–56.
TREE PHYSIOLOGY VOLUME 26, 2006
RESPONSE OF QUERCUS RUBRA TO UV-B RADIATION
McGraw, J.B., K.W. Gottschalk, M.C. Vavrek and A.L. Chester.
1990. Interactive effects of resource availabilities and defoliation
on photosynthesis, growth, and mortality of red oak seedling. Tree
Physiol. 7:247–254.
McKenzie, R.L., L.O. Björn, A. Bais and M. Hyasd. 2003. Changes in
biologically active ultraviolet radiation reaching the Earth’s surface. Photochem. Photobiol. Sci. 2:5–15.
McWilliam, J.R., P.J. Phillips and R.R. Parkes. 1973. Measurement of
photosynthetic rate using labeled carbon dioxide. Australia
CSIRO, Division of Plant Industries Technical Paper 31, 12 p.
Michael, D.A., D.I. Dickmann, K.W. Gottschalk, N.D. Nelson and
J.G. Isebrands. 1985. Determining photosynthesis of tree leaves in
the field using a portable 14CO2 apparatus: procedures and problems. Photosynthetica 19:98–108.
Nagel, L.M., J.H. Bassman, G.E. Edwards, R. Robberecht and V.R.
Franceshi. 1998. Leaf anatomical changes in Populus trichocarpa,
Quercus rubra, Pseudotsuga menziesii, and Pinus ponderosa exposed to enhanced ultraviolet-B radiation. Physiol. Plant. 104:
385–396.
Naidu, S.L., J.H. Sullivan, A.H. Teramura and E.H. DeLucia. 1993.
The effects of ultraviolet-B radiation on photosynthesis of different
aged needles in field-grown loblolly pine. Tree Physiol. 12:
151–162.
Ni, B. and S.G. Pallardy. 1991. Response of gas exchange to water
stress in seedlings of woody angiosperms. Tree Physiol. 8:1–9.
Nogués, S., D.J. Allen, J.I.L. Morison and N.R. Baker. 1998. Ultraviolet-B radiation effects on water relations, leaf development, and
photosynthesis in droughted pea plants. Plant Physiol. 117:
173–181.
Petropoulou, Y., A. Kyparissis, D. Nikolopoulos and Y. Manetas.
1995. Enhanced UV-B radiation alleviates the adverse effects of
summer drought in two Mediterranean pines under field conditions. Physiol. Plant. 94:37–44.
Pukacki, P.M. and J. Modrzynski. 1998. The influence of ultraviolet-B radiation on the growth, pigment production and chlorophyll
fluorescence of Norway spruce seedlings. Acta Physiol. Plant. 20:
245–250.
Robberecht, R. and M.M. Caldwell. 1986. Leaf UV optical properties
of Rumex patientia L. and Rumex obtusifolius L. in regard to a protective mechanism against solar UV-B radiation injury. In Stratospheric Ozone Reduction, Solar Ultraviolet Radiation and Plant
Life NATO ASI Series. Vol. G8. Eds. R.C. Worrest and M.M.
Caldwell. Springer-Verlag, Berlin, pp 251–259.
Sander, I.L. 1990. Quercus rubra L. northern red oak. In Silvics of
North America. Vol. 2. Hardwoods. Agriculture Handbook 654.
Eds. R.M. Burns and B.H. Honkala. U.S. Department of Agriculture, Forest Service, Washington, D.C., pp 727–733.
Schumaker, M.M., J.H. Bassman, R. Robberecht and G.K. Radamaker. 1997. Growth, leaf anatomy, and physiology of Populus
clones in response to solar ultraviolet radiation. Tree Physiol.
17:617–626.
Sisson, W.B. and M.M. Caldwell. 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.
1163
Skaltsa, H., E. Verykokidou, C. Harvala, G. Karabourniotis and
Y. Manetas. 1994. UV-B protective potential and flavonoid content
of leaf hairs of Quercus ilex. Phytochemistry 37:987–990.
Sullivan, J.H. and A.H. Teramura. 1989. The effects of ultraviolet-B
radiation on loblolly pine. I. Growth, photosynthesis and pigment
production in greenhouse-grown seedlings. Physiol. Plant. 77:
202–207.
Sullivan, J.H., A.H. Teramura, P. Adamse, G.F. Kramer, A. Upadhyaya, S.J. Britz, D.T. Krizek and R.M. Mirecki. 1994a. Comparison of the response of soybean to supplemental UV-B radiation
supplied by either square wave or modulated irradiation systems. In
Stratospheric Ozone Depletion/UV-B Radation in the Biosphere.
NATO ASI Series. Eds. R.H. Biggs and M.E.B. Joyner. SpringerVerlag, Berlin, pp 211–220.
Sullivan, J.H., A.H. Teramura and L.R. Dillenburg. 1994b. Growth
and photosynthetic responses of field-grown sweetgum (Liquidambar styraciflua; Hamamelidaceae) seedlings to UV-B radiation.
Am. J. Bot. 81:826–832.
Sullivan, J.H., D.C. Gitz, M.S. Peek and A.J. Mcelrone. 2003. Response of three eastern tree species to supplemental UV-B radiation: leaf chemistry and gas exchange. Agric. For. Meteorol. 120:
219–28.
Tegelberg, R., R. Julkunen-Tiitto and P.J. Aphalo. 2001. The effects
of long-term elevated UV-B on the growth and phenolics of fieldgrown silver birch (Betula pendula). Global Change Biol. 7:
839–48.
Teramura, A.H., R.H. Biggs and S. Kossuth. 1980. Effects of ultraviolet-B irradiance on soybean. II. Interaction between ultraviolet-B
and photosynthetically active radiation on net photosynthesis, dark
respiration, and transpiration. Plant Physiol. 65:483–488.
U.S. Department of Energy. 1993. UV-B Critical Issues Workshop
Cocoa Beach, Florida. U.S. Department of Energy, Oak Ridge, TN,
34 p.
USDA Forest Service. 1974. Seeds of woody plants in the United
States. U.S. Department of Agriculture, Washington, DC, 883 p.
Warren, J.M., J.H. Bassman and S. Eigenbrode. 2002a. Leaf biochemical changes induced in Populus trichocarpa by enhanced
UV-B radiation and concomitant effects on herbivory by Chrysomela scripta (Coleoptera: Chrysomelidae). Tree Physiol. 22:
1137–1146.
Warren, J.M., J.H. Bassman, D.S. Mattinson, J.K. Fellman, G.E. Edwards and R. Robberecht. 2002b. Alteration of foliar flavonoid
composition induced by enhanced UV-B radiation in Pinus ponderosa, Quercus rubra, Pseudotsuga menziesii and Populus trichocarpa. J. Photochem. Photobiol. B Biol. 66:125–133.
Warren, J.M., J.H. Bassman, J.K. Fellman, S.D. Eigenbrode and D.S.
Mattinson. 2003. Ultraviolet-B radiation alters phenolic salicylate
and flavonoid composition of Populus trichocarpa leaves. Tree
Physiol. 23:527–535.
Weber, J.A. and D.M. Gates. 1990. Gas exchange in Quercus rubra
(northern red oak) during a drought: analysis of relations among
photosynthesis, transpiration, and leaf conductance. Tree Physiol.
7:215–225.
Weih, M., U. Johanson and D. Gwynn-Jones. 1998. Growth and nitrogen utilization in seedlings of mountain birch (Betula pubescens
ssp. tortuosa) as affected by ultraviolet radiation (UV-A and UV-B)
under laboratory and outdoor conditions. Trees 12:201–207.
TREE PHYSIOLOGY ONLINE at http://heronpublishing.com