Tree Physiology 19, 917--924
© 1999 Heron Publishing----Victoria, Canada
Kinetics of leaf temperature fluctuation affect isoprene emission from
red oak (Quercus rubra) leaves
ERIC L. SINGSAAS,1,4 MARIANNE M. LAPORTE,1 JAIN-ZHONG SHI,1 RUSSELL K.
MONSON,2 DAVID R. BOWLING,2 KRISTINE JOHNSON,2 MANUEL LERDAU,3 AMAL
JASENTULIYTANA3 and THOMAS D. SHARKEY1,5
1
Department of Botany, University of Wisconsin-Madison, 430 Lincoln Drive, Madison, WI 53706-1381, USA
2
Department of EPO Biology, University of Colorado, Boulder, CO 80309, USA
3
Department of Ecology and Evolution, State University of New York, Stony Brook, NY 11794-5245, USA
4
Current address: Department of Plant Biology, University of Illinois Urbana-Champaign, 505 S. Goodwin Avenue, Urbana, IL 61801, USA
5
Author to whom correspondence should be addressed
Received October 20, 1998
Summary Because the rate of isoprene (2-methyl-1,3-butadiene) emission from plants is highly temperature-dependent,
we investigated natural fluctuations in leaf temperature and
effects of rapid temperature change on isoprene emission of red
oak (Quercus rubra L.) leaves at the top of the canopy at
Harvard Forest. Throughout the day, leaves often reached
temperatures as much as 15 °C above air temperature. The
highest temperatures were reached for only a few seconds at a
time. We compared isoprene emission rates measured when
leaf temperature was changed rapidly with those measured
when temperature was changed slowly. In all cases, isoprene
emission rate increased with increasing leaf temperature up to
about 32 °C and then decreased with higher temperatures. The
temperature at which isoprene emission rates began to decrease
depended on how quickly measurements were made. Isoprene
emission rates peaked at 32.5 °C when measured hourly,
whereas rates peaked at 39 °C when measurements were made
every four minutes. This behavior reflected the rapid increase
in isoprene emission rate that occurred immediately after an
increase in leaf temperature, and the subsequent decrease in
isoprene emission rate when leaf temperature was held steady
for longer than 20 minutes. We concluded that the observed
temperature response of isoprene emission rate is a function of
measurement protocol. Omitting this parameter from isoprene
emission models will not affect simulated isoprene emission
rates at mild temperatures, but can increase isoprene emission
rates at high temperatures.
Keywords: air pollution, biogenic emissions, forest trees, modeling, temperature response.
Introduction
Isoprene (2-methyl-1,3-butadiene) production by plants increases the thermo-tolerance of photosynthesis (Sharkey and
Singsaas 1995, Singsaas et al. 1997). The increase is proportional to the concentration of isoprene inside the leaf air
spaces, which is controlled by the rate of synthesis in the
chloroplasts and the resistance to its efflux through the stomata. Isoprene synthesis increases in response to increasing
light and leaf temperature (Sanadze and Kalandadze 1966,
Loreto and Sharkey 1990, Monson et al. 1991, Litvak et al.
1996). Because isoprene is volatile, isoprene concentration
inside the leaf, and hence thermo-tolerance, changes rapidly
with changes in light and leaf temperature. For this reason,
isoprene-induced thermo-tolerance is most important for
leaves that experience rapid temperature fluctuations (Singsaas et al. 1997) as a result of sunflecks (Pearcy et al. 1996).
These conditions often occur in forest canopies, which explains why a high proportion of isoprene-emitting species are
found in tropical and subtropical forests (Guenther et al. 1995,
Lerdau and Keller 1997).
If isoprene is to be effective in changing thermo-tolerance of
leaves, isoprene synthesis rates should be greatest when leaf
temperatures are highest. This is not always the case. Isoprene
emission rate increases with temperature at low temperatures
before reaching a maximum at some temperature TM. Thereafter isoprene emission rate decreases with further increases in
leaf temperatures. There is considerable variability in published values of TM. In Eucalyptus, TM occurs between 35 and
40 °C, but is highly variable (Guenther et al. 1993). Several
studies have reported TM values as high as 44 °C for sun-exposed leaves of Populus, but estimates vary by as much as
10 °C (Sanadze and Kalandadze 1966, Monson et al. 1992). If
TM occurs at 44 °C or higher, then canopy isoprene emission
rate will be highest during the hottest weather, supporting the
theory that isoprene functions by increasing the thermo-tolerance of leaves. A low TM (i.e., < 35 °C) indicates that canopy
isoprene emission rate will be less than maximal during the
warmest weather when thermo-tolerance is most needed. Determining the TM of leaves in a forest canopy would provide an
indication of the general applicability of the thermo-tolerance
theory.
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SINGSAAS ET AL.
A correct assessment of isoprene synthesis behavior at high
temperatures is also necessary for accurately modeling isoprene emission rates from forest canopies. These models are
necessary to predict the influence of phytogenic emissions on
atmospheric chemistry; particularly on the formation of tropospheric ozone (Trainer et al. 1987, Chameides et al. 1988,
Feshenfeld et al. 1992, Paulson et al. 1992). Isoprene emission
rate from forest canopies is typically simulated using the
equations developed by Guenther et al. (1991). This approach
is based on a basal emission factor, defined as the rate of
isoprene emission at 30 °C and 1000 µmol photons m −2 s −1,
scaled with equations that describe the response of isoprene
emission to leaf temperature and incident light. The basal
emission factor and the empirical parameters of the light and
temperature response equations are determined experimentally by gas-exchange measurements (Guenther et al. 1991,
Guenther et al. 1993, Monson et al. 1994, Harley et al. 1996,
Sharkey et al. 1996).
Because of the variability in published values of TM, we
assessed the effects of measurement technique on the observed
temperature response of isoprene emission rate. We measured
isoprene emission rate from leaves in the upper layers of red
oak (Quercus rubra L.) trees during July 1995. In addition,
micrometeorological measurements of leaf temperature, air
temperature, and incident PPFD were made. Additional experiments were carried out in the laboratory to verify and more
closely investigate the results from the field experiments.
Materials and methods
Site description
The study was carried out at Harvard Forest in north-central
Massachusetts 42.54° N, 72.18° W, elevation 320 m. Additional details about this site have been provided by Waring et
al. (1995). Two 20-m walk-up towers were used to gain access
to the top of two red oak (Quercus rubra) trees. Both trees were
20 m tall. Because there was no quantitative difference between the isoprene emission rates of the two trees, results from
both trees were pooled.
Micrometeorology
Temperature and photosynthetic photon flux density (light,
PPFD) at the leaf surface were recorded for groups of four
leaves at the top of the red oak tree next to Tower II. The PPFD
was measured with galium-arsenide photodiodes (Hamamatsu
Corp., Bridgewater, NJ) stuck through the leaf blade. Two
photodiodes were used per leaf to measure PPFD above
and below the leaf simultaneously. Leaf temperature was
measured with chromel-constantan thermocouples welded
from 0.07-mm diameter wire (Omega Engineering, Stamford,
CT). Three pieces of wire, two chromel and one constantan,
were welded to make two chromel-constantan thermocouple
junctions. To measure the difference between leaf and air
temperature (∆T), wires were threaded through the veins on
the underside of the leaf and one junction was pressed against
the bottom of the leaf, and the other thermocouple junction was
suspended 1 cm below the leaf. Air temperature was measured
in the vicinity of the leaves (not more than 0.5 m away) with a
chromel-constantan thermocouple. Accuracy of the leaf temperature measurements was verified with an infrared thermometer (Everest Interscience, Tucson, AZ). Wind speed was
measured in the vicinity of the leaves with needle anemometers (SoilTronics, Inc., Pullman, WA). All data were logged
every 5 s with a data logger (Model CR10, Campbell Scientific, Logan, UT).
The time constant for leaf temperature change was measured
on leaves of red oak trees grown in pots in a greenhouse in
Madison, Wisconsin. Leaf thermocouples were attached as for
the field micrometerological measurements, and leaves were
exposed to light from a 2.5 kW xenon-arc lamp attenuated to
1000 µmol photons m −2 s −1 with neutral-density screens. The
light was flashed on and off every minute by means of a
mechanical shutter. Leaf temperature, ∆T, was recorded once
per second. The leaf time constant was calculated from the
slope of a logarithmic plot of ∆T versus time.
Gas exchange
Measurements of leaf CO2 assimilation and isoprene emission
rate were made in the field with three different systems. The
first system tested was an LI-6400 Photosynthesis System
(Li-Cor, Inc., Lincoln, NE). The leaf cuvette enclosed 6 cm2 of
leaf and was equipped with a thermostat to control leaf temperature. Light was provided by a Li-Cor light-emitting diode
(LED), enabling precise control of irradiance. The LED provided light near 670 nm, which is as effective as light from a
xenon-arc lamp for isoprene emission (Tennessen et al. 1994).
Isoprene concentration in the leaf cuvette was measured by
directing the air exiting the cuvette through a 1-m tube (BevA-Line IV, Cole-Parmer, Vernon Hills, IL) to a portable gas
chromatograph (Scentoscreen, Sentex, Inc., Ridgefield, NJ).
Chromatography was performed as described by Sharkey et al.
(1996). The argon ionization detector on the gas chromatograph had a similar sensitivity to isoprene as the photoionization detectors. Because the signal was not linear with respect
to isoprene concentration, we calibrated the instrument against
standards prepared daily by mixing liquid isoprene (Fluka
Chemical Corp., Ronkonkoma, NY) with air in a Tedlar bag
and making serial dilutions in additional bags. Isoprene concentrations of 32 to 512 ppb were used.
The second system comprised a Li-Cor LI-6400 Photosynthesis System coupled to a Photovac 10S70 (Photovac, Inc.,
Long Island, NY) portable gas chromatograph. The Photovac
was equipped with a photoionization detector. Air left the
Li-Cor chamber at a flow rate of 200 ml min −1. The gas
chromatograph utilized a pump to draw air at 100 ml min −1
through a 1-ml sample loop for 10 s. Sample gas in the loop
was injected onto a 0.53 mm id CP-Sil-5 column 10 m in
length. The column was held at 40 °C in an isothermal oven.
The carrier gas was hydrocarbon-free air. The detector output
was linear across a broad range of isoprene concentrations and
the calibration line had an intercept at zero. Single point
calibrations were made daily by vaporizing and diluting pure
liquid isoprene (Sigma/Aldrich, St. Louis, MO) according to a
method recommended by Photovac (Technical Bulletin
TREE PHYSIOLOGY VOLUME 19, 1999
LEAF TEMPERATURE KINETICS AND ISOPRENE EMISSION
No. 21). The saturated head-space air of a vial containing pure
isoprene at known temperature (usually 0 °C) was diluted
serially in air to obtain a range of gas phase concentrations.
The third system consisted of a Campbell MPH 1000 gasexchange system (Campbell Scientific, Logan, UT) coupled to
a Photovac 10S portable gas chromatograph. Hydrocarbonfree air flowed at 0.8 to 1.2 l min −1 through a nickel-plated leaf
cuvette. Temperature was controlled by thermoelectric cooling
and light was provided by a 300-W projector bulb mounted at
a right angle to the top of the glass-topped cuvette. The light
was reflected by a cold mirror (45° cold mirror, OCLI, Santa
Rosa, CA) mounted at a 45° angle to the cuvette top. Humidity
in the cuvette was controlled by partitioning hydrocarbon-free
air between humidified and dry vessels, followed by remixing
before the air entered the cuvette. An aliquot of air was taken
from the leaf chamber outlet and analyzed with the Photovac
gas chromatograph by the procedures described above. This
gas exchange system was used to obtain emission rate data
following longer-term steady state conditions achieved after
slow warming or cooling of the cuvette.
Gas exchange calculations of photosynthetic carbon assimilation, stomatal conductance for water vapor, and partial pressure of CO2 inside the leaf were made with the equations of
von Caemmerer and Farquhar (1981). Isoprene emission rate
was calculated as rate of air flow through the chamber times
the isoprene concentration of the exiting air (Hills et al. 1992).
The Campbell system used hydrocarbon-free air from pressurized cylinders, whereas the Li-Cor systems used ambient air.
Isoprene concentration of ambient air is 0 to 3 ppb (Geron et
al. 1997). Because the background isoprene concentration was
small relative to the isoprene concentration exiting the cuvette,
no correction for ambient isoprene concentration was made.
The concentration of isoprene inside the leaf was calculated as
described by Singsaas et al. (1997).
919
Modeling
Isoprene emission rate was simulated from micrometerological measurements of PPFD and leaf temperature and a basal
emission factor of 30 nmol isoprene m −2 s −1. The light correction of Guenther et al. (1993) was used. Two temperature
correction algorithms were compared. The first was the temperature correction used by Guenther et al. (1993) with three
empirical parameters; activation energy (Ea = 95,000 J mol −1),
deactivation energy (Ed = 230,000 J mol −1) and falloff temperature (TM = 314 K). The second temperature correction
algorithm was a normalized Arrhenius function with a single
empirical parameter, the activation energy (Ea = 95,000 J
mol −1):
Ea
IT = e T s R
--
Ea
RT ,
(1)
where T is leaf temperature (K), R is the molar gas constant,
and TS is the temperature (30 °C) to which measurements are
standardized. Equation 1 is based on the temperature correction of Guenther et al. (1993) but with no falloff in isoprene
emission rate at high temperatures.
Results
Leaf temperature dynamics
Leaf temperature was highly variable at the top of the tree. Leaf
temperature varied from 20.4 to 39.3 °C during the middle
eight daylight hours of July 10, 1995, whereas air temperature
varied from 17.2 to 26.3 °C (Figure 1). During the measurement period, leaf temperature averaged 27 °C and air temperature averaged 21 °C. The difference between air and leaf
temperatures was greatest during the morning because the leaf
Protocols
Effect of temperature on isoprene emission rate was assessed
by clamping a leaf in a chamber at 20 to 30 °C and illuminating
at half or full sunlight (1000 or 2000 µmol m −2 s −1). The
temperature was then increased either slowly (with the Campbell system) or rapidly (with the Li-Cor LI-6400 systems). The
rapid increase in temperature was effected by using heat guns
to warm the cooling fins on the Li-Cor chambers. This procedure sometimes damaged adjacent leaves and on occasion
damaged the leaf being measured. When this occurred, data
from the damaged leaf were discarded. The speed with which
the temperature response could be determined was dictated by
the speed with which the gas chromatographs could operate.
To investigate the effect of varying the rate of temperature
increase on isoprene emission rate at Harvard Forest, two pairs
of curves were obtained with the Li-Cor LI-6400/Photovac
system. Another five pairs of curves were determined by using
the system described by Tennessen et al. (1994) on white oak
(Quercus alba L.) seedlings grown in a greenhouse in Madison, Wisconsin. Isoprene flux rates from each leaf were normalized to the basal emission rate for that leaf; i.e., the flux rate
determined at 30 °C and 1000 µmol photons m −2 s −1.
Figure 1. Temperature environment of a leaf growing at the top level
of a red oak tree at Harvard Forest collected on July 29, 1995. Leaf (s)
and air (----) temperature were logged every 2.5 seconds between 0800
and 1600 h. Temperature was measured with a double junction
chromel-constantan thermocouple held against the abaxial leaf surface
to measure the difference between leaf and air temperature (∆T ). Air
temperature was measured with a chromel-constantan thermocouple
within 0.5 m of the leaf.
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920
SINGSAAS ET AL.
received more sunlight before noon than after noon (data not
shown). The variance of leaf temperature over the whole measurement period was 11.7 °C, whereas air temperature had a
variance of 1.9. Temperatures were higher and more variable
in full sunlight than in shade. When incident PPFD was ≥ 500
µmol m −2 s −1, leaf temperature had a mean of 28.3 °C and a
variance of 7.8 °C, and air temperature had a mean of 21.3 °C
with a variance of 2.3°C. When ambient PPFD was < 500 mol
m −2 s −1, leaf temperature had a mean of 23.0 and a variance of
2.7, and air temperature had a mean of 21.9 and a variance of
0.44.
To determine the maximum rate of leaf temperature fluctuations, we measured the time constant for temperature changes
in oak leaves. Thermocouples were placed on the underside of
leaves to measure the difference between leaf and air temperature (∆T) as leaves were moved between high and low light.
Data were normalized before determining the time constant
with equations described by Nobel (1991). Examples of time
constants recorded for a white oak leaf are shown in Figure 2.
Lines were fit by linear regression to determine the leaf heating
and cooling constants. Time constants were calculated as the
negative inverse of the slope of the line. The heating constant
averaged 14.3 ± 1.2 s and the cooling constant averaged 18.7
± 1.2 s (mean ± standard error, n = 4).
Temperature response
The effect of temperature on isoprene emission was dependent
on the measurement technique. When leaf temperature was
raised from 20 to 35 °C slowly, and measurements made every
60 min, isoprene emission rate peaked at 32.5 °C (Figure 3A).
In contrast, when leaf temperature was raised from 28 to 45 °C
quickly, and measurements made every 4 min, isoprene emission rate peaked at 39 °C (Figure 3B). Because results from
both trees were similar, data were pooled. Both sets of measurements were made on different leaves of the same red oak
tree with the only difference in treatment being the rate at
which leaf temperature increased.
Figure 2. Leaf temperature change after changing energy balance for
leaf heating (d) and cooling (s). Leaf temperature was measured as
in Figure 1. Temperature difference was recorded once per second
as leaves were moved between high light (> 1500 µmol m −2 s −1) and
low light (< 200 µmol m −2 s −1). The high light was provided by a
2.5 kW xenon-arc lamp. The low light was ambient room light. Data
were normalized to the time constant equations described in Nobel
(1991). The lines were fit by linear regression.
Figure 3. Temperature response of isoprene emission measured when
stepwise temperature changes were made slowly (A) or rapidly (B).
Slow measurements were made on a red oak tree with the Campbell
system on Tower II. Leaves were held at each measurement temperature for 30 min. Values are means and standard errors of three to four
leaves. Two data points were excluded because they were greater than
3 × SE from the mean. Fast curves were measured with the LiCor/Sentex system. Leaves were held for 4 min at each temperature.
Isoprene emission rates were normalized to the rate measured at 30 °C
for each leaf (basal rate). Basal rates were 111 ± 29 (mean ± SE, n =
4) nmol m −2 s −1 in panel A, and 63 ± 3 nmol m −2 s −1 in panel B. Light
varied between 1000 and 1200 µmol m−2 s −1.
Further experiments confirmed that rate of leaf heating affected the temperature at which isoprene emission rate peaked.
In the field, temperature response of isoprene emission rate
was measured on two red oak leaves. Leaves were held at each
test temperature for 3 or 30 min before isoprene emission rate
was measured (Figure 4A). Isoprene emission rate peaked at
36 °C when leaf temperature was raised slowly and peaked at
42 °C when leaf temperature was raised quickly. We also
investigated the effect of rate of leaf heating on isoprene
emission rate in the laboratory on greenhouse-grown white oak
trees (Figure 4B). In one series, leaf temperature was increased
from 30 to 45 °C in 3 °C increments every 4 min. For the other
series, leaves were left for 40 min at each temperature. Isoprene emission peaked at 45 °C when leaf temperature was
increased quickly and at 39 °C when leaf temperature was
increased slowly.
To determine why the rate of heating changed the temperature response of isoprene emission, we imposed a continuous
heat treatment on leaves while measuring isoprene at 5-min
intervals (Figure 5). Leaves were held in a gas-exchange cuvette for 30 min at 30 °C to ensure isoprene emission rate was
at steady state. Leaf temperature was then raised to 40 °C and
held for 50 min. During the first 10 min at 40 °C, isoprene
emission rate increased 2.3-fold over the rate at 30 °C. During
the following 10 min, isoprene emission rate fell, eventually
TREE PHYSIOLOGY VOLUME 19, 1999
LEAF TEMPERATURE KINETICS AND ISOPRENE EMISSION
Figure 4. Fast and slow temperature response of isoprene emission
measured in (A) the field and (B) the laboratory. Field data were
determined with red oak leaves at the top of Tower I at Harvard Forest
in July 1995. The measurements were made after 3 min (d) or 30 min
(s) at each temperature. The basal rate was 44 nmol m −2 s −1 for both
leaves. Laboratory measurements were made on white oak seedlings
from a greenhouse after either 4 min (d) or 40 min (s) at each
temperature. The PPFD was 1000 µmol m −2 s −1 in all cases. The data
in B are means and standard errors for three leaves. The basal rates
were 49.3 ± 9.6 nmol m −2 s −1 for leaves measured after 4 min and 69.4
± 7.8 nmol m −2 s −1 for leaves measured after 40 min.
921
Figure 5. Isoprene emission time course in response to a 10 °C
increase in leaf temperature. Irradiance was 1000 µmol m −2 s −1. White
oak seedlings grown in a greenhouse were used, and measurements
were made as in Figure 4B. Data are means and standard errors of
three leaves.
achieving a new steady-state rate that was 1.8-fold higher than
at 30 °C. When leaf temperature was lowered again to 30 °C,
isoprene emission rate fell to 0.9 times the original rate, but
then recovered to the original rate within 25 min.
Isoprene emission simulations
Isoprene emission was simulated based on light and leaf temperature measurements recorded in the field (Figure 1) as
inputs. To investigate the errors introduced by simulating isoprene emission on a 0.5-h timescale, isoprene emission was
simulated using the temperature response equation (Guenther
et al. 1991) for half-hour mean leaf temperature data. Rates
calculated from these simulations were compared with rates
from the same period calculated every 5 s (Figure 6). The error
in the temperature response was proportional to the temperature variation during the measurement period. Error rates were
as much as 4% when the standard deviation in leaf temperature
was 2.5 °C during the 0.5-h simulation.
Because leaf temperature varied rapidly (Figures 1 and 2)
and rapid temperature variation caused TM to increase (Figure 3 and 4), we used simulations of isoprene emission to
determine the effect of TM on isoprene emission. Isoprene
emission rate was simulated with the Guenther et al. (1991)
model and with the Guenther et al. model in which the temperature correction was replaced with Equation 2. The time
Figure 6. Differences in isoprene emission simulations arising from
temperature variability. Isoprene emission was simulated from leaf
temperature data using the temperature correction of Guenther et al.
(1993). Leaf temperature data were taken from micrometeorological
measurements presented in Figure 1. Half-hour periods were extracted
from the data set and isoprene emission rate was simulated using the
5-s data of the mean temperature over the period.
step was 5 s in this simulation. When leaf temperatures were
low, averaging 26 °C, differences between the two models
were small (Figure 7A). Over the 8-h simulation period, isoprene emission rate was 6% higher with the modified model
than with the Guenther et al. model. As temperature increased,
the difference between the two models increased. When mean
leaf temperature was 35 ° C, isoprene emission rate predicted
by Equation 2 was 28% higher than the rate predicted by the
Guenther et al. (1991) algorithm (Figure 7B). The difference
between the two models increased exponentially with leaf
temperature (Figure 8).
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922
SINGSAAS ET AL.
Figure 7. Simulations of isoprene emission using models including
and excluding isoprene falloff temperature (TM ). Isoprene emission
was simulated from micrometeorological data recorded as in Figure 1.
Simulations were run on a 5-s time-step and the isoprene emission rate
was averaged every 0.5 h. Isoprene emission was simulated using the
standard isoprene emission algorithms (Guenther at al. 1993, s) or a
modified model without TM (Equation 2, d). Mean daily leaf temperature was 26 °C in panel A and 35 °C in panel B.
Figure 8. The differences between isoprene emission simulations with
and without TM . Isoprene emission was simulated as in Figure 7. Data
from Figure 1 were used and leaf temperature was modified so that the
mean temperature ranged from 25 to 35 °C. The difference in isoprene
emission simulations was calculated as a percentage of isoprene emission with the standard model.
Discussion
Leaves at the top of forest canopies can deviate considerably
from air temperature, often reaching quite high temperatures.
Although air temperature was moderate for July in central
Massachusetts, ranging between 17.2 and 26.3 °C during the
middle of the day, leaf temperatures approached 40 °C. Leaf-air temperature differences were as high as 15 °C in many
cases. We have also observed leaf--air temperature differences
of this magnitude in white oak trees in Chapel Hill, North
Carolina where a mean air temperature of 30.2 °C led to leaf
temperatures as high as 46 °C (J.Z. Shi, unpublished data).
Incident PPFD had a considerable effect on leaf temperature,
increasing both mean leaf temperature and leaf temperature
variability. One possible explanation for the increase in the
variability of leaf temperature is the presence of sunflecks.
Roden and Pearcy (1993) found that sunflecks occurred in
poplar canopies with a frequency of 3 Hz. Spectral analysis of
our data did not show a dominant sunfleck frequency, but our
measurement interval was too long to discern sunflecks occurring more frequently than 0.2 Hz. The fast time constants of
leaf temperature changes (Figure 2) would allow changes in
leaf temperature of several degrees to occur quite rapidly after
a change in PPFD caused by sunflecks. Thus sunflecks could
account for much of the variability in leaf temperature.
Isoprene emission rate increased with increasing leaf temperature until a critical ‘‘falloff’’ temperature was reached,
beyond which isoprene emission rate declined (Figures 3--5).
The falloff temperature was highly dependent on the rate of
temperature change (Figure 5). Isoprene emission rate increased for the first 10 min after a change in leaf temperature.
However, beyond 20 min, isoprene emission rate decreased to
a new steady state that was lower than the rate during the first
10 min. Temperature-response measurements made at 4-min
intervals reflect isoprene emission at the peak emission rate,
whereas measurements made at 60-min intervals only reflect
the lower emission rate reached after 20 min. This regulation
of isoprene emission is responsible for the apparent variability
in falloff temperature seen in Figure 4 and reported in earlier
work (Guenther et al. 1991, Guenther et al. 1993, Harley et al.
1996).
The behavior of isoprene emission at high temperatures
supports the hypothesis that isoprene protects leaves from
rapid temperature fluctuations. Because isoprene emission rate
falls off at much higher temperatures when leaf temperature
increases rapidly than when leaf temperature increases slowly,
isoprene concentration is highest in leaves subjected to rapid
temperature increases. Leaf temperature increases and decreases with time constants of less than 20 s (Figures 1 and 2).
The field instruments were limited to making a single isoprene
measurement every 4 min. Very rapid increases in leaf temperature may result in even higher values of TM than those
observed, provided that the time constant for isoprene emission changes is not much slower than that for leaf temperature
changes. Because isoprene emission decreases after 20 min at
high temperature, isoprene may be less effective in protecting
leaves from temperature increases that last 20 min or longer.
However, this may not be the case in all species, because
thermo-tolerance is dependent on both rate of isoprene synthesis and stomatal conductance to isoprene. Stomatal conductance declined during a 20-min exposure to high temperature;
however, the change in stomatal conductance was not sufficient to maintain a high isoprene concentration during the
experimental period (data not shown).
The response of isoprene emission rate to leaf heating rate
may significantly impact isoprene emission from forest cano-
TREE PHYSIOLOGY VOLUME 19, 1999
LEAF TEMPERATURE KINETICS AND ISOPRENE EMISSION
pies; however, this behavior is not taken into account in current
isoprene emission models. Isoprene emission rate can increase
with a time constant of as little as 8.2 s in laboratory experiments (Singsaas and Sharkey 1988). Because the response of
isoprene emission rate to temperature is nonlinear, error is
introduced into models by averaging leaf temperature over a
long period of time (Figure 6), though this error is relatively
small. The error is highest when leaf temperature is most
variable, which coincides with the highest leaf temperatures.
Use of a temperature-response model with a low TM may
introduce further errors that are potentially substantial. Although leaf temperature averaged around 30 °C, leaf temperatures near 40 °C were not uncommon (Figure 1). Simulating
isoprene emission with a low TM would underestimate isoprene
emission during these high temperature episodes. Because TM
was 45 °C or higher when leaf temperature was raised quickly,
we dropped it from the Guenther et al. (1993) temperature
algorithm and simulated isoprene emission with an Arrhenius
equation (Equation 1). This resulted in little difference in
isoprene emission rate when leaf temperature was low, but
errors increased markedly at high temperatures (Figures 7
and 8). This difference may help explain the 50% error in
isoprene emission models at high temperatures (Geron et al.
1997).
We conclude that changes in isoprene emission rate when
leaves are held at steady-state result in lower TM when the
temperature response of isoprene emission is measured at a
time interval of 60 min compared with a time interval of 4 min.
For this reason, TM is highly dependent on measurement technique. Isoprene emission was highest during short high-temperature episodes, supporting the theory that isoprene protects
leaves from rapid excursions to high temperature. For modeling purposes, TM does not affect isoprene emission simulations
at low temperature, but removing TM from temperature correction algorithms will increase estimated isoprene emission rates
during warm weather.
Acknowledgments
Research supported by US EPA Cooperative Research agreement CR
823791 and NSF grant IBN-9317900. We are grateful to Professors
Steven Wofsy and Fahkri Bazzaz for access to the towers at Harvard
Forest and Professor Ray Fall for loaning one of the Photovac gas
chromatographs. D. Bowling and K. Johnson were partially supported
by an EPA Graduate Fellowship, a Biosphere-Atmosphere Research
Training Grant, and an Undergraduate Research Opportunities Grant
from the University of Colorado. R. Monson received partial support
from the Council on Research and Creative Works at the University of
Colorado.
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TREE PHYSIOLOGY VOLUME 19, 1999