Directory UMM :Data Elmu:jurnal:T:Tree Physiology:Vol16.1996:

Tree Physiology 16, 557--565
© 1996 Heron Publishing----Victoria, Canada

Photosynthetic and stomatal responses to high temperature and light
in two oaks at the western limit of their range
ERIK HAMERLYNCK1,2 and ALAN K. KNAPP1
1

Division of Biology, Kansas State University, Ackert Hall, Manhattan, KS 66506-4901, USA

2

Present address: Department of Biological Sciences, University of Nevada Las Vegas, 4505 Marylandarkway,
P
Box 454004, Las Vegas, NV
89154-4004, USA

Received May 25, 1995

Summary Bur oak (Quercus macrocarpa Michx.) and chinquapin oak (Q. muehlenbergii Engl.) leaves were exposed to
high temperatures at various photosynthetic photon flux densities under laboratory conditions to determine if species-specific responses to these factors were consistent with the

distribution of these oaks in gallery forests in the tallgrass
prairies of northeastern Kansas, USA. Measurements of the
ratio of chlorophyll fluorescence decrease, Rfd, indicated that
chinquapin oak maintained greater photosynthetic capacity
than bur oak across all tested combinations of irradiance (100,
400, 700 and 1000 µmol m −2 s −1) and temperature (40, 42, 44,
46 and 48 °C). In both oak species, manipulation of leaf
temperature to about 47 °C for 45 min in the field led to a 45%
decrease in carbon assimilation up to one week after the heat
treatment, and to sharp reductions in stomatal conductance.
Photosynthetic recovery patterns indicated that bur oak took
longer to recover from heat stress than chinquapin oak, suggesting that heat stress may be important in determining distribution patterns of these oak species. Based on a comparison of
the results with data from other forest species, we conclude that
the photosynthetic temperature tolerances of bur oak and chinquapin oaks facilitate their dominance at the western limit of
the eastern deciduous forest.
Keywords: chlorophyll fluorescence, heat stress, Quercus marcrocarpus, Quercus muehlenbergii.

Introduction
High temperatures can affect trees through impacts on growth
and reproductive performance (Burton and Bazzaz 1991, Kozlowski et al. 1991, Bassow et al. 1994), seasonal photosynthetic acclimation (Berry and Bjorkman 1980, Seemann et al.

1984, Jurik et al. 1988, Hamerlynck and Knapp 1994a), distribution at several scales (Kozlowski et al. 1991, Jeffree and
Jeffree 1994, Vann et al. 1994) and community structure (Burton and Bazzaz 1991, Kozlowski et al. 1991, Kramer 1995).
Leaf temperature can rise well above air temperature when
solar radiative inputs exceed evaporative and convective heat
losses (Campbell 1977, Jones 1992). For this reason, plant

responses to temperature should not be studied independently
of irradiances because irradiance partially determines leaf temperatures in the field (Berry and Bjorkman 1980).
We have studied the interacting effects of light and temperature on two North American eastern deciduous forest oak
species growing at the western limit of their range. Bur oak
(Quercus macrocarpa Michx.) and chinquapin oak (Quercus
muehlenbergii Engl.) are canopy dominants in gallery forests
lining streams dissecting tallgrass prairie (Abrams 1986).
Water relations are a strong determinant of local tree distribution in these forests, with bur oak occupying more mesic,
closed-canopy gallery forest locations, whereas chinquapin
oak establishes in open, xeric upland sites (Abrams 1986,
Abrams and Knapp 1986, Bragg et al. 1993). Leaf-level characteristics correlate fairly well with distributional patterns,
with chinquapin oak having smaller leaves, lower photosynthetic rates and stomatal conductances, and higher photosynthetic temperature tolerance than bur oak (Hamerlynck and
Knapp 1994a). Although the independent effects of light and
high temperature on oak performance in tallgrass prairie gallery forests have been intensively studied (Knapp 1992,

Hamerlynck and Knapp 1994a and 1994b), the interactive
effects of these variables on photosynthesis of bur oak and
chinquapin oak in this ecotonal system are unknown.
We manipulated light and temperature under laboratory conditions to assess species-specific responses to light and temperature, and we also manipulated leaf temperatures of
attached entire leaves in the field under full-sun conditions to
determine if photosynthetic recovery from heat stress correlated with the observed distribution of these species in tallgrass
prairie gallery forests (Abrams 1986, Abrams and Knapp 1986,
Bragg et al. 1993). Despite much research on the ecological
implications of temperature optima in tree species (Chabot and
Lewis 1976, Strain et al. 1976, Teskey et al. 1986, Jurik et al.
1988, Ranney and Peet 1994), few studies have been undertaken to assess the importance of photosynthetic recovery after
heat stress (Methey and Trabaud 1993, Bassow et al. 1994).
Specifically, we tested four hypotheses. (1) Chinquapin oak
has greater temperature tolerance across all irradiances than
bur oak, facilitating its establishment in drier, more open

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gallery forest locations. There is evidence that chinquapin oak
is more drought tolerant than bur oak (Abrams 1986, Abrams
and Knapp 1986, Abrams 1990), and that drought tolerance
can accompany thermal tolerance and a high light requirement
(Berry and Bjorkman 1980, Seemann et al. 1984, Ivanov et al.
1992). (2) Low irradiance (about 100 µmol m −2 s −1) and high
temperature cause stress in bur oak and chinaquapin oak.
Elevated temperature depresses the photosynthetic light compensation point as a result of increased respiration rates relative to photosynthetic rates (Berry and Bjorkman 1980). (3)
Chinaquapin oak and bur oak have tolerances to combinations
of light and temperature that correlate with seedling microenvironment conditions. Bur oak seedlings establish in lower
light (about 400 µmol m −2 s −1) microsites than chinquapin oak
seedlings (700 µmol m −2 s −1) (Bragg et al. 1993). We also
postulated that, over the PPFD range 400--700 µmol m −2 s −1,
the photosynthetic capacity of bur oak would be depressed
more at higher temperature than that of chinquapin oak. (4)
Photosynthetic recovery from heat stress is slower in bur oak
than in chinquapin oak as a result of the larger leaves and
heat-induced reductions of gs in bur oak.
Materials and methods
Study area

Measurements were made from July 7 to September 9, 1994
on trees growing in the Konza Prairie Research Natural Area
(KPRNA, 39° N 96°32′ W), a 3487-ha tallgrass prairie preserve in the Flint Hills of northeastern Kansas, USA. Warmseason C4 grasses are the dominant vegetation on KPRNA,
though extensive gallery forests line streambeds dissecting the
prairie (Abrams 1986, Knight et al. 1994). The climate is warm
continental, with hot, humid summers, and cold, dry winters
(Borchert 1950). Growing season temperatures range from 17
to 43 °C. Tallgrass prairie is characterized by frequent and
unpredictable drought (Borchert 1950, Fahnestock and Knapp
1994), and growing season conditions of high, though variable,
photosynthetic photon flux densities (PPFD, ranging from 100
to 2100 µmol m −2 s −1, Knapp 1985, Knapp 1993, Fay and
Knapp 1993). Compared to mean values over the last 10 years,
rainfall during the 1994 growing season was average, and
temperatures were slightly lower than average in July but
typical for August and September.
Fluorescence and oxygen evolution measurements
Bur oak and chinquapin oak leaves were collected between
July 7 and August 8, 1994, at representative locations in gallery
forests on KPRNA. Leaves were harvested from 0930 to

1030 h CST, sealed in plastic bags containing moistened paper
to maintain turgor, and transported to the laboratory for analysis of concurrent photosynthetic oxygen evolution and chlorophyll fluorescence. Five leaves of each species were exposed
for 45 min to 20 treatment combinations of temperature (40,
42, 44, 46, and 48 °C) and PPFD (100, 400, 700, and 1000
µmol m −2 s −1), for a total sample size of 200. Oxygen evolution
was measured with a Clark type oxygen electrode (Hansatech
Instruments, Ltd., Kings Lynne, UK) in saturating (5%) CO2

conditions provided by a bicarbonate buffer. The experimental
leaf temperatures were maintained during the measurements
by attaching the electrode housing to a water bath (Isotemp
Model 9000, Fisher Scientific, Pittsburgh, PA). Differences in
water bath and leaf chamber temperatures were accounted for
by correlating water bath temperatures with leaf temperatures
measured with a fine wire type copper-constantan thermocouple. Chlorophyll fluorescence was measured with a FDP/2
fluorescence probe and TR1 transient recorder (Hansatech
Instruments). The ratio of fluorescence decrease, Rfd ((Fp −
Ft)/Ft, where Fp = peak fluorescence yield, Ft = steady-state
trace fluorescence after illumination), provides an index of
photosynthetic capacity (Lichtenthaler 1988, Lichtenthaler

and Rinderle 1988), where Rfd > 3.0 indicates unimpaired
photosynthetic function, Rfd < 1.0 indicates irreversible photosynthetic damage, and intermediate values indicate reversible
photosynthetic stress (Lichtenthaler 1988). Use of Rfd as an
indicator of photosynthetic capacity eliminates the need for
accurate estimation of baseline fluorescence, Fo, which is often
difficult at PPFDs > 100 µmol m −2 s −1 (Lavorel and Etienne
1977). Before each chlorophyll fluoresence measurement, leaf
samples were dark acclimated for 5 min at the measurement
temperature, and then exposed for 15 min to red light (λ = 660
nm, half-power bandwidth ± 30 nm) from an LED light source
(LH36U, Hansatech Instruments).
Field gas exchange measurements
From August 10 to September 9, 1994, 10 leaves each of bur
oak and chinquapin oak were exposed to a potentially stressful
high temperature (about 47 °C) in the field by enclosing entire
leaves in plastic bags for 45 min. This temperature exceeded
or equaled published thermal tolerances, and was similar to
maximum field leaf temperatures for these trees (Hamerlynck
and Knapp 1994a, Agati et al. 1995). During enclosure, PPFD
was reduced from about 1900 to about 1500 µmol m −2 s −1, but

was still above light saturation (Knapp 1992, Hamerlynck and
Knapp 1994a, 1994b). Leaf temperatures were monitored by
attaching a thermocouple to the abaxial surface before enclosure. Carbon dioxide was supplied by breathing into the bags
through a dessicant column about every 5 min. Humidity in the
bags rapidly approached saturation as a result of evapotranspiration from the leaves, making the bag environment similar to
the electrode housing under laboratory conditions. We monitored both short-term (1, 10, 20, 40, and 60 min) and long-term
(24 h and 7 day) recovery of photosynthetic gas exchange
capability under ambient conditions. Control values were obtained from gas exchange measurements of 10 unbagged
leaves on the same branches as the heat-treated leaves made
immediately before the heat treatment was imposed and concurrently with the 60 min, 24 h and 7 day recovery. Air
temperature at the time of the heat treatment and after 24 h was
30--33 °C with PPFD greater than 1800 µmol m −2 s −1. Seven
days later, air temperature was 25--27 °C and PPFD was
unchanged. All gas exchange measurements were made with
an LI-6200 portable photosynthesis system (Li-Cor, Inc., Lincoln, NE). Net photosynthesis (Anet) stomatal conductance to
water vapor (gs), and internal CO2 concentrations (Ci) were

RESPONSES OF OAKS TO HIGH TEMPERATURE AND IRRADIANCE

estimated from the equations of von Caemmerer and Farquhar

(1981). System parameters were used to calculate leaf transpiration in the cuvette, which was used to estimate instantaneous
water use efficiency (WUE, µmol CO2 µmol −1 H2O). Leaf
temperature (Tleaf ) was measured by a fine wire thermocouple
pressed to the underside of the leaf throughout measurement.
Statistical analysis
Three-way analysis of variance (Statistix v4.1, Analytical
Software, St. Paul, MN) was used to detect differences in Rfd
and O2 evolution, using species, temperature, and irradiance as
main effects. Additionally, two-tailed t-tests were used to determine if mean Rfd departed significantly from critical values
of 3.0 and 1.0 (Zar 1974). Field gas exchange measurements
were repeated measures, and a split-plot analysis of variance
was used, with species as the whole-plot factor and recovery
time as the sub-plot factor. A level of 0.05 was considered
significant, with means separation by LSD.
Results
Fluorescence and oxygen evolution
Pooled across all temperature and light treatment combinations, chinquapin oak maintained higher Rfd (2.07 ± 0.175
(SE)) than bur oak (1.74 ± 0.155) (F = 12.41, df = 1,160, P <

Figure 1. Effect of leaf temperature on ratio of fluorescence decrease

(Rfd) in leaves of bur oak and chinquapin oak exposed to 1000 (circle),
700 (upright triangle), 400 (square) or 100 (inverted triangle) µmol
m −2 s −1 photosynthetic photon flux density. Critical Rfd values of 3.0
(< 3.0 = stressed) and 1.0 (< 1.0 = permanently damaged) are indicated
by horizontal lines. Each point is the mean of five measurements, bars
indicate ± 1 SE of the mean.

559

0.05) (Figure 1). In bur oak, Rfd was reduced below the critical
values of 3.0 and 1.0 more often than in chinquapin oak. Over
the PPFD range 400--1000 µmol m −2 s −1 and the temperature
range 40--44 °C, bur oak had no Rfd values significantly above
3.0, but two values (temperature/light treatments 40/1000 and
44/700) were significantly below 3.0, whereas chinquapin oak
had Rfd values greater than 3.0 for four of the light/temperature
combinations (treatments 40/400, 42/700, 42/1000 and
44/700) and Rfd values of 3.0 in the other treatments. At 46 °C,
Rfd of bur oak was generally below 1.0 at all irradiances except
700 µmol m −2 s −1, whereas chinquapin oak maintained Rfd

above or equal to 1.0, except at 100 µmol m −2 s −1. At 48 °C,
all Rfd values of both species were below 1.0 indicating permanent damage. In both species, Rfd at 100 µmol m −2 s −1 PPFD
remained at the damage threshold of 1.0 at leaf temperatures
up to 44 °C, and then declined below 1.0 at leaf temperatures
above 46 °C. Overall, there were no significant effects of
species on the Rfd responses to light and temperature, but the
temperature × light interaction was significant (F = 13.25, df =
12,160, P < 0.05), indicating that the Rfd response to temperature was dependent on irradiance.
Because high leaf temperatures are usually accompanied by
high radiation loads, we analyzed the responses of Rfd to the
most common high temperature × high light combinations
(40--48 °C × 700 and 1000 µmol m −2 s −1 PPFD) that occur in
the field. At high irradiances, Rfd of chinquapin oak was above
or equal to 3.0 until 44 °C, did not significantly decrease below
3.0 until 46 °C, and was below 1.0 at 48 °C (Figure 2). In
contrast, Rfd of bur oak was significantly below 3.0 at 44 °C,
and was significantly below 1.0 at 46 °C.
Despite the differences in Rfd responses between the species,
there were no significant differences between species in pho-

Figure 2. Effect of temperature on the ratio of fluorescence decrease
(Rfd) pooled across a range of PPFDs from 700 to 1000 µmol m −2 s −1.
Horizontal lines indicate critical Rfd values of 3.0 (> 3.0 = healthy, <
3.0 = stressed) and 1.0 (> 1.0 = damaged, < 1.0 = permanently
damaged) in leaves of bur oak and chinquapin oak. Each bar is the
mean of 15 measurements, bars indicate ± 1 SE of the mean. Asterisks
indicate significant departure from critical Rfd values (two-tailed t-test,
at P < 0.05).

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Table 1. Gas exchange characteristics of field-grown bur oak (Quercus
macrocarpa) and chinquapin oak (Q. muehlenbergii) at the Konza
Prairie Research Natural Area. Species differences at P < 0.05 are
indicated by different letters (one-way ANOVA). Each number is the
mean of 30 measurements, with ± 1 SE of the mean in parentheses.

Figure 3. Effect of leaf temperature on net photosynthetic oxygen
evolution (A net ) of bur oak and chinquapin oak exposed to 1000
(circle), 700 (upright triangle), 400 (square) or 100 (inverted triangle)
µmol m −2 s −1 PPFD. Horizontal line indicates photosynthetic compensation point (Anet = respiration). Each point is the mean of five
measurements, bars indicate ± 1 SE of the mean.

Parameter

Bur oak

Chinquapin oak

Anet (µmol m −2 s −1)
gs (mmol m −2 s −1)
Ci (µl l −1)
WUE (µmol mmol −1)
Tleaf (°C)

17.76 (0.549)a
422.4 (20.85)a
247.0 (3.35)a
1.43 (0.067)a
34.6 (0.48)a

15.48 (0.519)b
289.5 (11.07)b
233.5 (1.76)b
1.53 (0.081)a
36.1 (0.44)b

of about 1500 µmol m −2 s −1, led to significant reductions in
short-term Anet (Figure 4). The ANOVA showed no significant
species main effect on Anet in the leaves sampled, or any
significant time × species interaction. Within 1 min of raising
leaf temperature to about 47 °C, Anet declined by about 70%
from pre-exposure values in both oaks and then increased to
new reduced maxima of 11.6 ± 1.40 and 9.3 ± 1.00 µmol m −2
s −1 in bur oak and chinquapin oak, respectively, after 10 min.
Stomatal conductance (gs) declined 74% from pre-exposure
values in bur oak compared with a 50% reduction in chinquapin oak, which led to a significant species × time interaction

tosynthetic oxygen evolution in response to combinations of
PPFD and high temperature (Figure 3). There was a significant
temperature × light interaction on Anet (F = 10.55, df = 12,160,
P < 0.05), most likely because the curves converged at 48 °C.
Leaves exposed to elevated temperature and low PPFD (100
µmol m −2 s −1) were not significantly above photosynthetic
compensation point (Anet = respiration) at 40 °C, and declined
to rates well below photosynthetic compensation point at temperatures between 42 and 48 °C. At higher PPFDs (400--1000
µmol m −2 s −1), Anet declined as the temperature increased from
40 °C to the photosynthetic compensation point at about 44 °C.
Only in chinquapin oak leaves at a PPFD of 1000 µmol m −2
s −1 was Anet significantly above (1.9 ± 0.58 µmol m −2 s −1) the
photosynthetic compensation point at 44 °C. At 46 and 48 °C,
light effects on Anet were indistinguishable statistically.
Field gas exchange
In the field, bur oak had 15 and 46% significantly higher Anet
and gs, respectively, than chinquapin oak (Table 1), and slightly
higher Ci (6%, P < 0.05). The Tleaf of bur oak was about 1.5 °C
lower than that of chinquapin oak. Both oak species showed
broad responses in Anet and gs to leaf temperatures ranging
from 26 to 40 °C (data not shown).
In both species, increasing leaf temperature to 46.7 ±
0.46 °C, about 18 °C above ambient air temperature, at a PPFD

Figure 4. Short-term recovery kinetics of net photosynthesis (Anet ) and
stomatal conductance (gs) in bur oak and chinquapin oak leaves exposed to about 47 °C for 45 min in the field. Each bar is the mean of
10 measurements, error bars indicate ± 1 SE of the mean, letters
indicate significant differences at P < 0.05 (two-way ANOVA).

RESPONSES OF OAKS TO HIGH TEMPERATURE AND IRRADIANCE

Figure 5. Long-term recovery kinetics of net photosynthesis (A net ) and
stomatal conductance (gs) in bur oak and chinquapin oak leaves exposed for 45 min to leaf temperatures of about 47 °C in the field, and
appropriate controls. Bars are means of 10 measurements, error bars
indicate ± 1 SE of the mean. Letters differ at P < 0.05 (two-way
ANOVA).

(F = 4.7, df = 5, 90, P < 0.05). In bur oak and chinquapin oak,
gs reached constant post-exposure values after a 20 and 10 min
recovery that were 41 and 22% below pre-exposure values,
respectively.
Twenty-four h after heat treatment (Figure 5), Anet in bur oak
leaves was significantly lower (52%) than in chinquapin oak
leaves, and 79% lower than in control bur oak leaves, whereas
Anet in chinquapin oak was the same after 24 h as after 1 h, i.e.,
about 52% of the control value. Stomatal conductance was 84
and 46% of control values in bur oak and chinquapin oak,
respectively, after 24 h of recovery. One week following heat
stress, both oaks had Anet of about 9.1 ± 1.35 µmol m −2 s −1
compared with rates in control bur oak and chinquapin leaves
of 17.1 ± 1.07 and 15.0 ± 0.67 µmol m −2 s −1, respectively. After
one week of recovery, gs of bur oak significantly increased
(181.3 ± 33.88 µmol m −2 s −1), reaching values similar to
chinquapin oak (159.3 ± 28.34 µmol m −2 s −1), both of which
were well below gs in control leaves (52% of control in bur oak,
42% in chinquapin oak).
Post heat-stress recovery dynamics are summarized in Figure 6. Overall, the proportional decrease in Anet was similar
(about 55%) in both species after one hour of recovery,
whereas the decrease in gs was larger in bur oak (about 40%)
than in chinquapin oak (about 20%). Twenty-four h after heat
treatment, both Anet and gs in bur oak had decreased by 84%

561

Figure 6. Relative short-term and long-term recovery in mean net
photosynthesis (Anet ) and stomatal conductance (gs) in bur oak and
chinquapin oak leaves after exposure to high temperature treatment
(about 47 °C). Control leaves were measured concomitantly, the shortterm control value was obtained from the experimental leaves before
heat treatment and the long-term control value was obtained from
untreated leaves on the same trees.

compared with control values, whereas Anet in chinquapin oak
remained unchanged during the first 24 h after heat treatment
at about 50% of the control value.

Discussion
Fluorescence analyses showed that chinquapin oak may be
slightly more thermotolerant than bur oak (Figures 1 and 2),
which is consistent with earlier observations (Hamerlynck and
Knapp 1994a). Because changes in Rfd result from decreased
Fp and increased Ft, which, in turn, reflect changes in photochemical (qp) and non-photochemical (qnp) fluorescence
quenching (Lichtenthaler 1988, Epron and Dreyer 1990,
Methy and Trabaud 1993), and increasing temperature decreases qp and increases qnp (Georgiva and Yordanov 1994), the
reductions in Rfd could be due to PSII instability, limited
electron transfer to Q (Armond et al. 1978, Berry and Bjorkman 1980, Naus et al. 1992), changes in thylakoid membranes
(McCain et al. 1989, Harding et al. 1990, Kuropatwa et al.
1992), or photoinhibition (Havaux 1993, 1994). The ability of
chinquapin oak to maintain Rfd at slightly higher values than
bur oak suggests that this species may allocate resources to
stabilize photosystem II (Berry and Bjorkman 1980,
Kuropatwa et al. 1992, Naus et al. 1992), protect against

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HAMERLYNCK AND KNAPP

photoinhibition (Ghashghaie and Cornic 1994, Havaux 1994),
or maintain enzymatic activity at higher temperatures than bur
oak (Kobza and Edwards 1987, Ghosh et al. 1989, Simon and
Vairinhos 1991, Ranney and Peet 1994).
Thermal tolerance has been linked to photosynthetic responses to drought (Ivanonv et al. 1992) and light (Berry and
Bjorkman 1980, Midmore and Prange 1992, but see Armond et
al. 1978, Al-Khatib and Paulsen 1989, and Mishra and Singhal
1992). In three Mediterranean oak species with differing
drought tolerances, Rfd, qp, and qnp did not respond directly to
severe water stress (Epron and Dreyer 1990, Epron et al. 1992,
Epron and Dreyer 1993). In our study, the differences in Rfd
suggest that photosynthetic responses to high temperature and
light may be linked to drought tolerance. Reductions in Rfd of
bur oak and chinquapin oak in response to high temperature
were similar to other oaks (Methy and Trabaud 1993), but less
than in maple and walnut (McCain et al. 1989, Agati et al.
1995). In our study, it is unlikely that differences in thermal
tolerance were due to growth conditions, which strongly influence temperature responses (Seemann et al. 1984, Williams et
al. 1986, Jones 1992), because leaf samples were taken from
locations where the oak species co-occurred.
Low PPFD (100 µmol m −2 s −1) and high temperature resulted in stress to both oaks (Figures 1 and 3). Under conditions of low irradiance and high temperature, photosynthetic
carbon assimilation is reduced by rapid increases in respiration
(Berry and Bjorkman 1980, Midmore and Prange 1992). Decreased Rfd at an irradiance of 100 µmol m −2 s −1 was caused by
reduced Fp, possibly because of reduced electron transfer to Q
from PSII (Lichtenthaler 1988). Although it may seem unlikely that many leaves would experience leaf temperatures
exceeding 40 °C at a PPFD of 100 µmol m −2 s −1, inner canopy
shade leaves can experience transient periods of both high
irradiance and leaf temperature (Pearcy 1990). We have preliminary evidence (Hamerlynck, unpublished data) that shade
leaves of both oak species have equal, or greater, heat tolerances than sun leaves. It is possible, therefore, that shade leaf
photosynthesis, which contributes significantly to daily and
seasonal carbon gain (Kozlowski et al. 1991), could be limited
by interactions between temperature and light.
Bragg et al. (1993) suggested that bur oak seedlings establish in lower PPFD microenvironments than chinquapin oak
because they are less drought tolerant. At PPFDs between 400
and 700 µmol m −2 s −1 and temperatures from 40 to 44 °C, bur
oak Rfd was equal to or below the critical value of 3.0, whereas
chinquapin oak had Rfd values significantly above 3.0 at 400
µmol m −2 s −1, and equal to 3.0 at 700 µmol m −2 s −1. These
findings support our hypothesis that chinquapin oak is more
thermotolerant than bur oak to the light and temperature combinations likely to prevail in the field. Our observations also
provide evidence that bur oak and chinquapin oak seedling
establishment is influenced primarily by differences in temperature tolerance and irradiance, as has been suggested for
other tree species (Pearcy 1990, Küppers and Schneider 1993,
Poorter and Oberbauer 1993).
We have no explanation for the lack of a species effect on
the responses of O2 evolution to high temperature and light. It

is possible that the O2 evolution response was slower than the
fluorescence response (Epron and Dreyer 1990), and that the
sampling times were not sufficiently frequent to resolve specific differences. We note that the laboratory measurements
were made on evenly heated, isolated tissue and so may differ
from whole-leaf responses in the field (Jones 1992). Field
measurements with attached leaves at 40 ± 1 °C (data not
shown) often showed Anet to be well above the 10.0--12.0 µmol
m −2 s −1 range measured at similar temperatures and irradiances
in the laboratory. In addition, measurement in saturating CO2
in the O2 electrode housing may shift the photosynthetic temperature optimum to higher values and narrow the response,
resulting in greater proportional decreases at temperature extremes compared to measurement at atmospheric CO2 concentrations (Mooney et al. 1978, Berry and Bjorkman 1980).
Heat treatment in the field reduced Anet in both oaks, indicating that damage occurred (Figure 4). In both oaks, stomata
closed substantially in response to elevated temperature (Figure 4). Stomatal closure at high temperatures is well documented, (cf. Roessler and Monson 1985, Samuelson and
Teskey 1991, Bassow, et al. 1994, Ranney and Peet 1994),
though exceptions occur (Al-Khatib and Paulsen 1989, Dufrene and Saugier 1993). Roessler and Monson (1985) concluded that stomata closed because of increased VPD, whereas
Anet reductions were temperature dependent. Our results indicate stomatal closure in these oaks was more closely coupled
to increased temperature than to increased VPD, because gs
was reduced in a saturated vapor pressure environment. The
concurrent decreases in gs and Anet (Figures 4 and 6) indicate
that, in these oaks, gs may rapidly adjust to short-term changes
in photosynthetic capacity, as occurs over longer periods
(Wong et al. 1979, Chandler and Dale 1993, Hamerlynck and
Knapp 1994b). Reduced gs may also indicate damage to the
stomatal apparatus. In wheat exposed to similar irradiance and
temperatures, gs increased and Anet declined, indicating that
high temperature and light mainly affected mesophyll function
(Al-Khatib and Paulsen 1989).
Transient high temperature stress had more severe effects on
the photosynthetic recovery of bur oak than of chinquapin oak
(Figure 4 and 5). Under normal field conditions, bur oak had
higher Anet , gs, and Ci than chinquapin oak. Bur oak also had
lower Tleaf , but similar WUE to chinquapin oak (Table 1.) and
other C3 tallgrass prairie plants (Turner et al. 1995). Differences in gs are consistent with the observed distribution of
these oaks in tallgrass prairie gallery forests (Abrams 1986).
Large leaves and high gs in bur oak could maximize Anet under
favorable conditions, as indicated by higher Ci (Table 1), but
might restrict this oak to mesic gallery forest locations. After
heat treatment, gs and Anet in bur oak were similar to chinquapin oak (Figures 4 and 5). Reduced gs after heat stress, combined with large leaves, appeared detrimental to bur oak’s
photosynthetic recovery. Reduced gs limits evaporative cooling, whereas slower convective heat loss by large leaves may
raise Tleaf above the thermal tolerance limit during recovery
(Campbell 1977, Jones 1992, Hamerlynck and Knapp 1994a).
A comparison of gas exchange responses 24 h and 7 days after
recovery (Figure 5) provides evidence to support this idea.

RESPONSES OF OAKS TO HIGH TEMPERATURE AND IRRADIANCE

Twenty-four h after heat stress, Tleaf was 36--39 °C in both
oaks, but only in bur oak were the values of Anet and gs less than
after 1 h of recovery. After 7 days of recovery, Anet of bur oak
had increased but was still less than the control value. Thus,
large leaves and greater proportional reductions in gs after heat
stress (Figure 7) could limit bur oak to moist forest sites,
whereas small leaves and smaller proportional reductions in gs
after heat stress, as well as low gs under favorable conditions,
could allow chinquapin oak to establish and maintain populations in exposed dry locations. We conclude that reductions in
gs after heat stress may not affect Tleaf as much in chinquapin
oak as in bur oak, thus allowing for more rapid photosynthetic
readjustment in chinquapin oak.
In the field, Anet was not depressed below the compensation
point after exposure for 45 min at light × temperature combinations that reduced Rfd below the damage threshold after only
5 min (Figure 1), which indicates that Rfd and other fluorescence signals may overestimate the impact of high temperature
on intact leaves under field conditions (Schreiber and Berry
1977, Lichtenthaler 1988, Agati et al. 1995). However, the
estimated thermal tolerances of these oaks (Figure 1) were
similar to desert shrubs (Mooney et al. 1978, Seemann et al.
1984, Midgley and Moll 1993), xeric Mediterranean oaks
(Methy and Trabaud 1993), shortgrass prairie species (Monson
and Williams 1982, Roessler and Monson 1985), and tropical
species (Smillie and Nott 1979, Dufrene and Saugier 1993),
although higher than those reported for many North American
oak species found further east (Chabot and Lewis 1976, Tingey
et al. 1979, Jurik et al. 1988, Loreto and Sharkey 1990), as well
as many deciduous broadleaf and conifer species (Teskey et al.
1986, Jurik et al. 1988, Bassman and Zwier 1991, Foster 1992,
Ranney and Peet 1994, Vann et al. 1994). The ability to recover
over 50% of photosynthetic capacity after extreme heat stress
may be crucial for the success of these oaks in tallgrass prairie
gallery forests. Even after prolonged exposure to 47 °C, photosynthesis of bur oak and chinquapin oak was equal to or
higher than Anet at optimum temperatures (22 to 30 °C) for
other oak and hardwood species (Chabot and Lewis 1976,
Jurik et al. 1988, Foster 1992). We conclude that the thermal
tolerance characteristics of bur oak and chinquapin oak contribute to the persistence of these species in deciduous forest
extending west into the hot, arid grasslands of the central
plains of North America.

Acknowledgments
This research was supported by the NSF Long Term Ecological Research program at the Konza Prairie Research Natural Area (DEB9011662) and by the Kansas State University Agricultural
Experimental Station.

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