Directory UMM :Data Elmu:jurnal:T:Tree Physiology:vol17.1997:
Tree Physiology 17, 23--29
© 1997 Heron Publishing----Victoria, Canada
Light availability and photosynthesis of Pseudotsuga menziesii
seedlings grown in the open and in the forest understory
HAN Y. H. CHEN and KAREL KLINKA
Department of Forest Sciences, University of British Columbia, 270-2357 Main Mall, Vancouver, B.C. V6T 1Z4, Canada
Received January 30, 1996
Summary The light environment, photosynthetic dynamics
and steady-state net photosynthetic rates of lateral branch
shoots of Pseudotsuga menziesii var. glauca (Beissn.) Franco
seedlings growing in the open and in the forest understory were
investigated in situ. Mean incident photosynthetic photon
flux density (PPFD) was 702.5 µmol m −2 s −1 on open-grown
branches and 52.0 µmol m −2 s −1 on understory-grown
branches. Mean daily durations of PPFD greater than 500, 200,
and 50 µmol m −2 s−1 were 8.5, 31.5, and 270.3 min, respectively, on understory-grown branches, and 559.1, 700.7, and
803.3 min, respectively, on open-grown branches. Sunflecks
accounted for 32.4% of total daily photosynthetically active
radiation incident on understory branches. Following 10 min at
a PPFD of 50 µmol m−2 s−1, the induction time required for net
photosysnthesis to reach 50 and 90% of steady-state rates was
shorter at a PPFD of 200 than at a PPFD of 500 µmol m −2 s −1
and shorter in understory-grown branches than in open-grown
branches. On a leaf area basis, dark respiration rates of understory-grown branches were lower and net photosynthetic rates
were higher than those of open-grown branches exposed to low
PPFD. However, at high PPFDs, understory-grown branches
had lower photosynthetic rates than open-grown branches.
When measurements were expressed on a leaf dry mass basis,
there was no difference in dark respiration rates between understory branches and open-grown branches, but net photosynthetic rates of understory branches were equal to or higher than
those of open-grown branches at all PPFDs.
Keywords: dark respiration, light acclimation, net photosynthesis, photosynthetic induction, sunflecks.
Introduction
Photosynthetic acclimation to a changing light environment
has been studied in some tropical shrubs (Chazdon 1988,
Chazdon 1992, Chazdon and Kaufmann 1993), agricultural
crops (Pons et al. 1992, Intrieri et al. 1995), herbs (Young and
Smith 1980, Koizumi and Oshima 1993, Pearcy and Sims
1994, Pearcy et al. 1994, Sims and Pearcy 1994), and broadleaf
tree species (Ellsworth and Reich 1992, Kitajima 1994, Letho
and Grace 1994, Tang et al. 1994, Tinoco-Ojanguren and
Pearcy 1995). In general, leaves of shade plants have a lower
dark respiration rate and a lower light-saturated photosynthetic
rate (Amax) on a leaf area basis than sun leaves (Chazdon 1992,
Chazdon and Kaufmann 1993, Walters et al. 1993, Kitajima
1994, Letho and Grace 1994, Sims and Pearcy 1994, Intrieri et
al. 1995). Photosynthesis that is dependent on sunflecks accounts for up to 50% of net carbon gain in some understory
species of tropical rain forests (Chazdon 1988, Chazdon and
Pearcy 1991). Simulations of dynamic photosynthetic responses in controlled laboratory conditions indicate that shade
plants achieve higher light-use efficiencies during sunflecks
than sun plants because of faster photosynthetic induction and
greater post-illumination assimilation (Pons et al. 1992, Tang
et al. 1994). There have been few studies of photosynthetic
plasticity to sun and shade conditions in conifers (Brooks et al.
1994, Leverenz 1995, Stenberg et al. 1995). Furthermore, few
studies of the relationship between light acclimation and photosynthetic behavior have been carried out under natural light
conditions (Young and Smith 1980, Chazdon 1992, Ellsworth
and Reich 1992, Chazdon and Kaufmann 1993), thus little is
known about the dynamic responses of net photosynthesis to
light acclimation under field conditions.
In central British Columbia, interior Douglas-fir (Pseudotsuga menziesii var. glauca (Beissn.) Franco) is considered a
late-successional, moderately shade-tolerant species of montane forests that is capable of regenerating under its own
canopy. The sun leaves are distributed around the branches in
a whorled pattern, whereas the shade leaves are oriented in a
nearly horizontal plane. A previous study on naturally regenerated Douglas-fir saplings showed that, with decreasing light
availability, (i) specific leaf area increases and (ii) the ratio of
the terminal shoot increment to lateral branch increment decreases (Chen et al. 1996). Both changes likely make saplings
more efficient in capturing light energy in a light-limiting
environment. Whether Douglas-fir seedlings grown in a lowlight environment have lower dark respiration rates and higher
photosynthetic light-use efficiencies must be investigated to
understand how this species maintains vigorous growth in the
forest understory. A higher light-use efficiency, if it exists, may
be attributed to (i) faster induction responses and (ii) higher net
photosynthetic rates under conditions of constant irradiation.
The objectives of this study were to: (i) characterize the light
environment of plantation-grown Douglas-fir seedling branches,
(ii) examine the time-courses of photosynthetic induction responses to various irradiances in seedlings grown in full-light
24
CHEN AND KLINKA
environments and in the forest understory, and (iii) determine
whether the photosynthetic light-use efficiency of understorygrown seedlings is higher than that of open-grown seedlings.
Materials and methods
Study site and plant materials
The study site was located in the dry mild interior Douglas-fir
subzone (Meidinger and Pojar 1991), near Okanagan Falls,
British Columbia (50°05′ N, 119°40′ W). The area receives an
annual average of 600 mm total precipitation. The wettest and
driest months are June and April, respectively. The mean temperatures for the coldest and the warmest month are --10.7 and
15.8 °C, respectively. The length of the growing season is
between 4 and 5 months extending from late April to early
September (Meidinger and Pojar 1991).
In April 1993, one-year-old container-grown P. menziesii
seedlings of a local provenance were obtained from a local
nursery and planted in a recently created 2-ha clearcut and in
an adjacent naturally regenerated, immature stand with a semiopen canopy. The stand composition was 70% interior
Douglas-fir, 20% western larch (Larix occidentalis Nutt.), and
10% ponderosa pine (Pinus ponderosa Dougl. ex Laws.).
Mean height of the stand was 15 m; mean age of the canopy
trees was 30 years; and stand basal area was 15 m2 ha −1. To
minimize the substrate effect, all seedlings were planted in
mineral soil. Based on the method described by Green and
Klinka (1994), both the understory and clearcut portions of the
study site were considered to be moderately dry with medium
nitrogen availability. After 17 months, light measurements
were made in the vicinity of 16 randomly chosen seedlings
(eight from the forest understory and eight from the clearcut).
Only the uppermost lateral branches with well-expanded current-year needles were selected for light and gas exchange
measurements. These branches were approximately 25 to
35 cm above ground. To eliminate the possible influence of
soil water deficit, the root zones of sampled seedlings were
maintained at field capacity by watering on three successive
days before gas exchange was measured.
Light measurements
Photosynthetic photon flux density (PPFD) at the center of
sampled branches was measured with a PPFD sensor (LI-190
SA quantum sensor, Li-Cor, Inc., Lincoln, NE) connected to a
datalogger (Li-Cor LI-1000 datalogger) monitored at 5-s intervals from before sunrise to after sunset. Another PPFD sensor
and datalogger were placed in the center of the clearcut. The
two datalogger clocks were synchronized before taking PPFD
measurements. When the PPFD sensors were placed side by
side and compared over a PPFD range from 10 to 1500 µmol
m −2 s −1, their readings were found to differ by less than 0.5%.
The dataloggers were set to average 12 instantaneous PPFD
recordings each minute. All measurements were made under
clear skies from July 28 to August 15, 1994. Light availability
for the branches of open-grown seedlings was considered
equivalent to full light even though some self-shading by
terminal shoots may have occurred.
Gas exchange measurements
We measured gas exchange of lateral branch shoots of five or
eight randomly chosen seedlings. We also measured light
availability in the vicinity of the same shoots. Measurements
were made in the field under a tent on attached lateral shoots
using an artificial light source and an open portable photosynthesis system (ADC LCA-3, Analytical Development Company Ltd., Herts, U.K.) with a conifer cuvette. The light source
consisted of four 20-W, 12-V tungsten-halogen lamps set in a
2 × 2 arrangement to provide uniform irradiation of the cuvette.
Photosynthetic photon flux was varied between 50 and
1800 µmol m −2 s −1 by varying the distance between the cuvette and light source. Nominal irradiance was ± 5% of actual
PPFD with the beam perpendicular to the plane of the measured shoot. The tent and additional black cloth screened out
most natural light. To reduce the seasonal variation in photosynthesis caused by needle aging (Brooks et al. 1994), gas
exchange measurements were taken between August 8 and
August 25, 1994 on the uppermost branches with current-year,
well-expanded needles. An air mast (Analytical Development
Company) was used to draw fresh air from outside the tent at
a height of 1.2 m. With a flow rate of 300 cm3 min−1 through
the cuvette, it took the system approximately 35 s to detect a
95% step change in vapor pressure and CO2 concentration in
the cuvette.
After sunset the day before measurements, one seedling,
selected alternately from the forest understory or clearcut, was
covered by a dark plastic can (ventilated with several small
holes) to prevent exposure to diffuse, early-morning light. The
photosynthesis system was adjusted for study site conditions
before gas exchange measurements were taken each morning.
To avoid the more extreme daytime differences in air temperature, ambient humidity, and soil water conditions, gas exchange measurements were taken every 20 s from before
sunrise (0515 ± 0010 h) to 1000 h. Dark respiration rates were
measured at 0515 ± 0015 h. Photosynthetic induction responses were observed at 200 and 500 µmol m −2 s −1 after the
branch had first been completely induced at a PPFD of
500 µmol m −2 s −1 and then exposed to a PPFD of 50 µmol
m−2 s−1 for 10 min. A light-response curve for each branch was
constructed following stepwise PPFD increases until photoinhibition occurred. After gas exchange measurements, branches
were removed and stripped of needles to measure total onesided projected leaf area with a Li-Cor LI-3100 area meter.
Needles were then dried at 65 °C for 24 h and weighed.
During gas exchange measurements, ambient CO2 concentration, temperature, and relative humidity were monitored.
Ambient conditions varied from early morning to 1000 h.
Carbon dioxide concentration decreased from 370 ± 10 to 350
± 10 ppm; air temperature increased from 12 ± 2 to 22 ± 3 °C;
and relative humidity decreased from 65 ± 10 to 50 ± 10%.
Slower rates of increase in air temperature and decrease in
relative humidity occurred in the forest understory compared
to the clearcut.
LIGHT AVAILABILITY AND PHOTOSYNTHESIS OF PSEUDOTSUGA
Calculations
Direct radiation in the forest understory was subjectively defined as PPFD greater than 50 µmol m −2 s −1 (Chazdon and
Pearcy 1991, Koizumi and Oshima 1993, Tang et al. 1994).
The sunfleck contribution was calculated as:
Ts
Sunfleckcontribution =
∫T (PPFD − 50 ) dt
r
Ts
∫T
,
(1)
Pt − PL
100,
PH − PL
Open
Mean daily PPFD
(mol m−2 day --1)
(2)
where Pt is the net photosynthetic rate at time t, PL is steadystate assimilation rate at 50 µmol m −2 s −1, and PH is steadystate net photosynthetic rate at either 200 or 500 µmol m −2 s −1.
To reduce signal noise in the measurement system, both PL and
PH were averaged from five readings.
Light-response curves for both understory- and open-grown
seedlings were fitted to a rectangular hyperbola (Long and
Hällgren 1993). When possible photoinhibition occurred at a
PPFD, measurements were not included in the final analysis.
One-tailed Student’s t-test was used to test the difference
between means of open- and understory-grown seedlings.
Understory
702.5 ± 20.4
52.0 ± 28.7
40.5 ± 1.2
2.8 ± 1.5
r
where if PPFD < 50, let (PPFD− 50) equal zero, and Tr and Ts
are the times of sunrise and sunset when the PPFD was > 1
µmol m −2s−1 and < 1 µmol m −2 s−1, respectively.
Photosynthetic induction state (ISt, normalized net photosynthetic rate, %) was based on the formula of Chazdon and
Pearcy (1986):
IS t =
Table 1. Light conditions for open-grown branches and for branches in
the forest understory. Values are means and standard deviations
(n = 8). Direct radiation is defined as PPFD values greater than 50
µmol m−2 s−1.
Mean PPFD
(µmol m−2 s−1)
PPFD dt
25
Percent of value
in the open
100
7.4 ± 4.1
PPFD > 500 µmol m−2 s−1
mean daily duration (min)
559.1 ± 13.0
8.5 ± 15.1
PPFD > 200 µmol m−2 s−1
mean daily duration (min)
700.7 ± 37.3.0
Direct radiation
mean daily duration (min)
803.3 ± 40.8
270.3 ± 189.3
PPFD > 500 µmol m−2 s−1
(% of time)
57.6 ± 2.5
0.94 ± 1.7
PPFD > 200 µmol m−2 s−1
(% of time)
72.4 ± 1.0
3.5 ± 4.0
PPFD ≥ 50 µmol m−2 s−1
(% of time)
84.2 ± 3.8
28.2 ± 19.7
PPFD due to sunflecks
(% of daily)
----
32.4 ± 22.0
31.5 ± 36.1
50% of day length). The peak PPFDs due to sunflecks varied
from 170 to 1120 µmol m −2 s −1; sunflecks contributed between
6.8 and 58.9% of total PPFD.
Results
Dynamic photosynthetic induction response
Light availability
There was a larger but slower increase in net photosynthetic rate
in open-grown branches than in understory-grown branches
exposed to PPFDs of 500 µmol m −2 s −1and 200 µmol m −2 s −1
Branches of open-grown seedlings received a mean PPFD of
702.5 µmol m −2 s −1 and a mean daily PPFD of 40.5 mol m −2
day −1, whereas understory-grown seedlings received a mean
PPFD of 52 µmol m −2 s −1 and a mean daily PPFD of 2.8 mol
m −2 day −1 (Table 1). Branches of understory-grown seedlings
received a mean of 7.4% full sun PPFD, with sunflecks contributing 32.4% of the daily photon flux (Table 1). Representative daily courses of PPFD in the forest understory and
the open are shown in Figure 1.
The light environment varied greatly among measured
branches from different understory seedlings; mean PPFD
ranged from 18.4 to 85 µmol m −2 s −1 and mean daily PPFD
ranged from 1.1 to 4.6 mol m −2 day −1. The percent of full sun
PPFD had a range of 3 to 12%. The daily cumulated amount
of time that branches received a PPFD above 500 µmol
m −2 s−1 and 200 µmol m −2 s −1 ranged from 0 to 31 min (0 to
3.2% of day length) and 0 to 83 min (0 to 8.7% of day length),
respectively. The daily cumulated amount of time branches
received direct radiation ranged from 44 to 485 min (4.6 to
Figure 1. Representative daily courses of light availability for a seedling branch in the forest understory and in the open. Measurements
were made on August 2, 1994.
26
CHEN AND KLINKA
following 10 min at a PPFD of 50 µmol m −2 s −1 (Figures 2
and 3, Table 2). At a PPFD of 500 µmol m −2 s −1, the mean
times required by understory-grown branches to reach 50 and
90% of steady-state photosynthetic rate were 85 and 200 s,
respectively; corresponding mean times for open-grown
branches were 99 and 304 s (Figure 2b, Table 2). At a PPFD of
200 µmol m −2 s−1, the mean times required by understorygrown branches to reach 50 and 90% induction were 63 and
173 s, respectively; corresponding mean times for open-grown
branches were 81 and 162 s (Figure 3b, Table 2).
Both understory- and open-grown branches were slower to
reach full induction at a PPFD of 500 µmol m −2 s −1 than at a
PPFD of 200 µmol m −2 s −1 (Figures 2b and 3b, Table 2). Times
taken for understory- and open-grown branches to reach 100%
induction state at a PPFD of 500 µmol m −2 s −1 were 300 and
500 s, respectively, and 240 s for both at a PPFD of 200 µmol
m −2 s −1.
Light-response curves
Understory- and open-grown branches had different net photosynthetic responses to steady-state PPFDs (Figures 4a and
4b). Compared to open-grown branches, understory-grown
branches had a significantly (P < 0.05) lower dark respiration
rate (0.44 ± 0.01 versus 0.77 ± 0.03 µmol m −2 s −1), higher
area-based net photosynthetic rate at a PPFD of 50 µmol m −2
s −1, and lower area-based net photosynthetic rates at PPFDs
higher than 350 µmol m −2 s −1 (Figure 4a). At PPFDs of 200
Figure 3. (a) Net photosynthetic rates (Pn) and (b) induction responses
to an increase in irradiance from a 10-min PPFD of 50 µmol m−2 s−1
to a PPFD of 200 µmol m−2 s−1 starting at time 0 for open-grown
(closed circles) and understory branches (open circles). Each point is
the mean (± SE) of single measurements from five seedlings.
Table 2. Mean (± SE) time (s) required to reach 50 and 90% steadystate net photosynthetic rate for open- and understory-grown seedling
branches following 10 min at a PPFD of 50 µmol m−2 s−1. Values
followed by the same letter are not significantly different at the same
induction state between open- and understory-grown branches
(P < 0.05).
PPFD
50%
−2 −1
(µmol m
Figure 2. (a) Net photosynthetic rates (Pn) and (b) induction responses
to an increase in irradiance from a 10-min PPFD of 50 µmol m− 2 s−1
to a PPFD of 500 µmol m−2 s−1 starting at time 0 for open-grown
(closed circles) and understory-grown branches (open circles). Each
point is the mean (± SE) of single measurements from five seedlings.
s ) Open
90%
Understory
Open
Understory
500
99 ± 12.5 a 85 ± 11.5 a
304 ± 45.3 a 200 ± 15.5 b
200
81 ± 5.6 a
162 ± 5.0 a
63 ± 5.2 b
173 ± 17.6 a
and 350 µmol m −2 s −1, no difference in net photosynthetic
rates between understory- and open-grown branches was observed. At a PPFD of 50 µmol m −2 s −1, the light compensation
point was lower for understory-grown branches compared to
open-grown branches, as shown by their net photosynthetic
rates (0.23 ± 0.02 versus --0.11 ± 0.07 µmol m −2 s −1). Understory-grown branches reached 90% of their light-saturated net
photosynthetic rate at a PPFD of 500 µmol m −2 s −1, whereas
open-grown branches did not reach 90% of their light-saturated rate even at a PPFD of 1000 µmol m −2 s −1. At supersaturating PPFD, photosynthetic rates decreased, suggesting the
onset of photoinhibition (not shown). Threshold PPFD for
LIGHT AVAILABILITY AND PHOTOSYNTHESIS OF PSEUDOTSUGA
photoinhibition was between 800 and 1400 µmol m −2 s−1 for
understory-grown branches and at 1800 µmol m−2 s −1 for
open-grown branches.
Differences between understory- and open-grown branches
were less pronounced when data were expressed on a leaf mass
basis (Figure 4b). There was little difference in dark respiration
rates between understory- and open-grown branches (P = 0.33).
Net photosynthetic rates were significantly higher (P < 0.05)
for understory-grown than for open-grown branches at PPFDs
of 50 and 200 µmol m −2 s−1. At PPFDs equal to or greater than
350 µmol m −2 s −1, no significant difference in net photosynthetic rates was found between open- and understory-grown
branches (P > 0.05).
Discussion
Understory light availability
Understory-grown branches received a mean daily PPFD of
2.8 mol m −2 day −1 or 7.4% of full sun, with sunflecks contributing 32.4% of the daily total (Table 1). Light availability
under the forest canopy was higher than that reported for low
latitude conifer forests and tropical rain forests (Chazdon
1988, Canham et al. 1990). The contribution of sunflecks to
daily PPFD was similar to that found in a montane red spruce-balsam fir forest in the Appalachian Mountains of the eastern
USA (Canham et al. 1990).
Figure 4. Photosynthetic light-response curves for open-grown (closed
circles) and understory-grown branches (open circles). (a) Net photosynthetic rate (Pn) on a projected leaf area basis and (b) net photosynthetic rate (Pn) on a dry needle mass basis. Each point is the mean of
five measurements on each branch.
27
Light availability and sunfleck duration and intensity within
the stand varied greatly among branches from different seedlings. Similar results were reported for understory light environments of tropical rain forests (Chazdon 1986). Such spatial
variability depends on distances from gaps (Canham et al.
1990, Chazdon and Pearcy 1991) and the clumping effect of
overstory leaves (Chen and Black 1992, Baldocchi and Collineau 1994). Diffuse and direct components were not measured separately in this study; instead, a PPFD of 50 µmol
m −2 s −1 was used to discriminate between diffuse light and
direct light (e.g., Chazdon 1986, Koizumi and Oshima 1993).
However, both the direct component and the diffuse components may vary spatially and diurnally within a forest stand
(Black et al. 1991).
Dynamic and steady-state photosynthesis
Pseudotsuga menziesii seedlings acclimated photosynthetically to their light environments under field conditions. Photosynthetic induction responses to PPFD changes were quicker
in understory-grown branches than in open-grown branches.
This pattern is consistent with studies in a tropical forest
(Küppers et al. 1996) and in controlled environments on some
broadleaf plants (Pons and Pearcy 1992, Tang et al. 1994).
Photosynthetic induction responses of P. menziesii branches
tended to be faster than those of Quercus serrata Thunb. (Tang
et al. 1994) but shorter than those of desiccation-tolerant Polypodium virginianum L. (Gildner and Larson 1992). However,
the time required to reach full photosynthetic induction varies
among species (Chazdon 1988) and depends on: (i) length of
the period and PPFD of low light condition (Pons et al. 1992,
Whitehead and Teskey 1995), and (ii) other ecological factors
such as water status. Photosynthetic induction responses tend
to be faster in the field than in the laboratory (Gildner and
Larson 1992), and water-stressed plants reach their maximum
stomatal conductance in less time than unstressed plants (Tinoco-Ojanguren and Pearcy 1993, Barradas et al. 1994). We
also found that the time required to reach full photosynthetic
induction depended on PPFD. With increasing PPFD, more
time was required for both understory and open-grown
P. menziesii branches to reach full photosynthetic induction.
Acclimation of dark respiration under sun versus shade
conditions has been studied at the leaf and whole-plant levels
(Björkman 1981, Chazdon and Kaufmann 1993, Letho and
Grace 1994, Sims and Pearcy 1994, Intrieri et al. 1995, TinocoOjanguren and Pearcy 1995). Plants acclimated to low light
environments have low dark respiration rates when expressed
on a unit leaf area basis. Similarly, in this study, understorygrown branches of P. menziesii had lower dark respiration rates
per unit of leaf area than open-grown branches. On a dry leaf
mass basis, however, dark respiration rates did not differ between the understory- and open-grown branches.
Compared to open-grown branches, understory-grown
branches were photosynthetically more efficient at low PPFDs
but less efficient at high PPFDs (Leverenz 1995). Based on per
unit dry leaf mass, net photosynthetic light-use efficiency in
understory-grown branches was equal to or higher than that of
open-grown branches at all PPFDs except those inducing pho-
28
CHEN AND KLINKA
toinhibition. This pattern has also been observed in some
species at the leaf and whole-plant levels (Björkman 1981,
Sims and Pearcy 1994, Leverenz 1995). Thus, compared with
sun plants, shade plants exhibit no disadvantage in terms of
carbon gain per unit dry mass unless photoinhibited.
There are qualitative and quantitative differences in light
response among individual needles, shoots, and whole plants
(Pearcy and Sims 1994, Leverenz 1995, Stenberg et al. 1995).
This study describes the dynamic and steady-state photosynthetic behavior of P. menziesii at the lateral-shoot level, which
integrates both photosynthesis of needles and the structural
factor of their distribution. However, photosynthetic behavior
at the individual needle and whole-plant levels was not considered. Moreover, computer simulations of dynamic and steadystate photosynthesis in relation to natural light regimes in
P. menziesii seedlings may be needed to understand the daily
and seasonal carbon balance and the relative importance of
dynamic and steady-state photosynthetic plasticity.
Acknowledgments
We especially thank Dr. Robert D. Guy, Department of Forest Sciences, University of British Columbia, for his continuous encouragement during this study and valuable comments on the manuscript. We
also thank Dr. T.A. Black for his useful comments on the manuscript.
Financial support from the Natural Science and Engineering Research
Council of Canada, and B.C. Ministry of Forests, Silviculture Branch
is acknowledged.
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LIGHT AVAILABILITY AND PHOTOSYNTHESIS OF PSEUDOTSUGA
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29
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© 1997 Heron Publishing----Victoria, Canada
Light availability and photosynthesis of Pseudotsuga menziesii
seedlings grown in the open and in the forest understory
HAN Y. H. CHEN and KAREL KLINKA
Department of Forest Sciences, University of British Columbia, 270-2357 Main Mall, Vancouver, B.C. V6T 1Z4, Canada
Received January 30, 1996
Summary The light environment, photosynthetic dynamics
and steady-state net photosynthetic rates of lateral branch
shoots of Pseudotsuga menziesii var. glauca (Beissn.) Franco
seedlings growing in the open and in the forest understory were
investigated in situ. Mean incident photosynthetic photon
flux density (PPFD) was 702.5 µmol m −2 s −1 on open-grown
branches and 52.0 µmol m −2 s −1 on understory-grown
branches. Mean daily durations of PPFD greater than 500, 200,
and 50 µmol m −2 s−1 were 8.5, 31.5, and 270.3 min, respectively, on understory-grown branches, and 559.1, 700.7, and
803.3 min, respectively, on open-grown branches. Sunflecks
accounted for 32.4% of total daily photosynthetically active
radiation incident on understory branches. Following 10 min at
a PPFD of 50 µmol m−2 s−1, the induction time required for net
photosysnthesis to reach 50 and 90% of steady-state rates was
shorter at a PPFD of 200 than at a PPFD of 500 µmol m −2 s −1
and shorter in understory-grown branches than in open-grown
branches. On a leaf area basis, dark respiration rates of understory-grown branches were lower and net photosynthetic rates
were higher than those of open-grown branches exposed to low
PPFD. However, at high PPFDs, understory-grown branches
had lower photosynthetic rates than open-grown branches.
When measurements were expressed on a leaf dry mass basis,
there was no difference in dark respiration rates between understory branches and open-grown branches, but net photosynthetic rates of understory branches were equal to or higher than
those of open-grown branches at all PPFDs.
Keywords: dark respiration, light acclimation, net photosynthesis, photosynthetic induction, sunflecks.
Introduction
Photosynthetic acclimation to a changing light environment
has been studied in some tropical shrubs (Chazdon 1988,
Chazdon 1992, Chazdon and Kaufmann 1993), agricultural
crops (Pons et al. 1992, Intrieri et al. 1995), herbs (Young and
Smith 1980, Koizumi and Oshima 1993, Pearcy and Sims
1994, Pearcy et al. 1994, Sims and Pearcy 1994), and broadleaf
tree species (Ellsworth and Reich 1992, Kitajima 1994, Letho
and Grace 1994, Tang et al. 1994, Tinoco-Ojanguren and
Pearcy 1995). In general, leaves of shade plants have a lower
dark respiration rate and a lower light-saturated photosynthetic
rate (Amax) on a leaf area basis than sun leaves (Chazdon 1992,
Chazdon and Kaufmann 1993, Walters et al. 1993, Kitajima
1994, Letho and Grace 1994, Sims and Pearcy 1994, Intrieri et
al. 1995). Photosynthesis that is dependent on sunflecks accounts for up to 50% of net carbon gain in some understory
species of tropical rain forests (Chazdon 1988, Chazdon and
Pearcy 1991). Simulations of dynamic photosynthetic responses in controlled laboratory conditions indicate that shade
plants achieve higher light-use efficiencies during sunflecks
than sun plants because of faster photosynthetic induction and
greater post-illumination assimilation (Pons et al. 1992, Tang
et al. 1994). There have been few studies of photosynthetic
plasticity to sun and shade conditions in conifers (Brooks et al.
1994, Leverenz 1995, Stenberg et al. 1995). Furthermore, few
studies of the relationship between light acclimation and photosynthetic behavior have been carried out under natural light
conditions (Young and Smith 1980, Chazdon 1992, Ellsworth
and Reich 1992, Chazdon and Kaufmann 1993), thus little is
known about the dynamic responses of net photosynthesis to
light acclimation under field conditions.
In central British Columbia, interior Douglas-fir (Pseudotsuga menziesii var. glauca (Beissn.) Franco) is considered a
late-successional, moderately shade-tolerant species of montane forests that is capable of regenerating under its own
canopy. The sun leaves are distributed around the branches in
a whorled pattern, whereas the shade leaves are oriented in a
nearly horizontal plane. A previous study on naturally regenerated Douglas-fir saplings showed that, with decreasing light
availability, (i) specific leaf area increases and (ii) the ratio of
the terminal shoot increment to lateral branch increment decreases (Chen et al. 1996). Both changes likely make saplings
more efficient in capturing light energy in a light-limiting
environment. Whether Douglas-fir seedlings grown in a lowlight environment have lower dark respiration rates and higher
photosynthetic light-use efficiencies must be investigated to
understand how this species maintains vigorous growth in the
forest understory. A higher light-use efficiency, if it exists, may
be attributed to (i) faster induction responses and (ii) higher net
photosynthetic rates under conditions of constant irradiation.
The objectives of this study were to: (i) characterize the light
environment of plantation-grown Douglas-fir seedling branches,
(ii) examine the time-courses of photosynthetic induction responses to various irradiances in seedlings grown in full-light
24
CHEN AND KLINKA
environments and in the forest understory, and (iii) determine
whether the photosynthetic light-use efficiency of understorygrown seedlings is higher than that of open-grown seedlings.
Materials and methods
Study site and plant materials
The study site was located in the dry mild interior Douglas-fir
subzone (Meidinger and Pojar 1991), near Okanagan Falls,
British Columbia (50°05′ N, 119°40′ W). The area receives an
annual average of 600 mm total precipitation. The wettest and
driest months are June and April, respectively. The mean temperatures for the coldest and the warmest month are --10.7 and
15.8 °C, respectively. The length of the growing season is
between 4 and 5 months extending from late April to early
September (Meidinger and Pojar 1991).
In April 1993, one-year-old container-grown P. menziesii
seedlings of a local provenance were obtained from a local
nursery and planted in a recently created 2-ha clearcut and in
an adjacent naturally regenerated, immature stand with a semiopen canopy. The stand composition was 70% interior
Douglas-fir, 20% western larch (Larix occidentalis Nutt.), and
10% ponderosa pine (Pinus ponderosa Dougl. ex Laws.).
Mean height of the stand was 15 m; mean age of the canopy
trees was 30 years; and stand basal area was 15 m2 ha −1. To
minimize the substrate effect, all seedlings were planted in
mineral soil. Based on the method described by Green and
Klinka (1994), both the understory and clearcut portions of the
study site were considered to be moderately dry with medium
nitrogen availability. After 17 months, light measurements
were made in the vicinity of 16 randomly chosen seedlings
(eight from the forest understory and eight from the clearcut).
Only the uppermost lateral branches with well-expanded current-year needles were selected for light and gas exchange
measurements. These branches were approximately 25 to
35 cm above ground. To eliminate the possible influence of
soil water deficit, the root zones of sampled seedlings were
maintained at field capacity by watering on three successive
days before gas exchange was measured.
Light measurements
Photosynthetic photon flux density (PPFD) at the center of
sampled branches was measured with a PPFD sensor (LI-190
SA quantum sensor, Li-Cor, Inc., Lincoln, NE) connected to a
datalogger (Li-Cor LI-1000 datalogger) monitored at 5-s intervals from before sunrise to after sunset. Another PPFD sensor
and datalogger were placed in the center of the clearcut. The
two datalogger clocks were synchronized before taking PPFD
measurements. When the PPFD sensors were placed side by
side and compared over a PPFD range from 10 to 1500 µmol
m −2 s −1, their readings were found to differ by less than 0.5%.
The dataloggers were set to average 12 instantaneous PPFD
recordings each minute. All measurements were made under
clear skies from July 28 to August 15, 1994. Light availability
for the branches of open-grown seedlings was considered
equivalent to full light even though some self-shading by
terminal shoots may have occurred.
Gas exchange measurements
We measured gas exchange of lateral branch shoots of five or
eight randomly chosen seedlings. We also measured light
availability in the vicinity of the same shoots. Measurements
were made in the field under a tent on attached lateral shoots
using an artificial light source and an open portable photosynthesis system (ADC LCA-3, Analytical Development Company Ltd., Herts, U.K.) with a conifer cuvette. The light source
consisted of four 20-W, 12-V tungsten-halogen lamps set in a
2 × 2 arrangement to provide uniform irradiation of the cuvette.
Photosynthetic photon flux was varied between 50 and
1800 µmol m −2 s −1 by varying the distance between the cuvette and light source. Nominal irradiance was ± 5% of actual
PPFD with the beam perpendicular to the plane of the measured shoot. The tent and additional black cloth screened out
most natural light. To reduce the seasonal variation in photosynthesis caused by needle aging (Brooks et al. 1994), gas
exchange measurements were taken between August 8 and
August 25, 1994 on the uppermost branches with current-year,
well-expanded needles. An air mast (Analytical Development
Company) was used to draw fresh air from outside the tent at
a height of 1.2 m. With a flow rate of 300 cm3 min−1 through
the cuvette, it took the system approximately 35 s to detect a
95% step change in vapor pressure and CO2 concentration in
the cuvette.
After sunset the day before measurements, one seedling,
selected alternately from the forest understory or clearcut, was
covered by a dark plastic can (ventilated with several small
holes) to prevent exposure to diffuse, early-morning light. The
photosynthesis system was adjusted for study site conditions
before gas exchange measurements were taken each morning.
To avoid the more extreme daytime differences in air temperature, ambient humidity, and soil water conditions, gas exchange measurements were taken every 20 s from before
sunrise (0515 ± 0010 h) to 1000 h. Dark respiration rates were
measured at 0515 ± 0015 h. Photosynthetic induction responses were observed at 200 and 500 µmol m −2 s −1 after the
branch had first been completely induced at a PPFD of
500 µmol m −2 s −1 and then exposed to a PPFD of 50 µmol
m−2 s−1 for 10 min. A light-response curve for each branch was
constructed following stepwise PPFD increases until photoinhibition occurred. After gas exchange measurements, branches
were removed and stripped of needles to measure total onesided projected leaf area with a Li-Cor LI-3100 area meter.
Needles were then dried at 65 °C for 24 h and weighed.
During gas exchange measurements, ambient CO2 concentration, temperature, and relative humidity were monitored.
Ambient conditions varied from early morning to 1000 h.
Carbon dioxide concentration decreased from 370 ± 10 to 350
± 10 ppm; air temperature increased from 12 ± 2 to 22 ± 3 °C;
and relative humidity decreased from 65 ± 10 to 50 ± 10%.
Slower rates of increase in air temperature and decrease in
relative humidity occurred in the forest understory compared
to the clearcut.
LIGHT AVAILABILITY AND PHOTOSYNTHESIS OF PSEUDOTSUGA
Calculations
Direct radiation in the forest understory was subjectively defined as PPFD greater than 50 µmol m −2 s −1 (Chazdon and
Pearcy 1991, Koizumi and Oshima 1993, Tang et al. 1994).
The sunfleck contribution was calculated as:
Ts
Sunfleckcontribution =
∫T (PPFD − 50 ) dt
r
Ts
∫T
,
(1)
Pt − PL
100,
PH − PL
Open
Mean daily PPFD
(mol m−2 day --1)
(2)
where Pt is the net photosynthetic rate at time t, PL is steadystate assimilation rate at 50 µmol m −2 s −1, and PH is steadystate net photosynthetic rate at either 200 or 500 µmol m −2 s −1.
To reduce signal noise in the measurement system, both PL and
PH were averaged from five readings.
Light-response curves for both understory- and open-grown
seedlings were fitted to a rectangular hyperbola (Long and
Hällgren 1993). When possible photoinhibition occurred at a
PPFD, measurements were not included in the final analysis.
One-tailed Student’s t-test was used to test the difference
between means of open- and understory-grown seedlings.
Understory
702.5 ± 20.4
52.0 ± 28.7
40.5 ± 1.2
2.8 ± 1.5
r
where if PPFD < 50, let (PPFD− 50) equal zero, and Tr and Ts
are the times of sunrise and sunset when the PPFD was > 1
µmol m −2s−1 and < 1 µmol m −2 s−1, respectively.
Photosynthetic induction state (ISt, normalized net photosynthetic rate, %) was based on the formula of Chazdon and
Pearcy (1986):
IS t =
Table 1. Light conditions for open-grown branches and for branches in
the forest understory. Values are means and standard deviations
(n = 8). Direct radiation is defined as PPFD values greater than 50
µmol m−2 s−1.
Mean PPFD
(µmol m−2 s−1)
PPFD dt
25
Percent of value
in the open
100
7.4 ± 4.1
PPFD > 500 µmol m−2 s−1
mean daily duration (min)
559.1 ± 13.0
8.5 ± 15.1
PPFD > 200 µmol m−2 s−1
mean daily duration (min)
700.7 ± 37.3.0
Direct radiation
mean daily duration (min)
803.3 ± 40.8
270.3 ± 189.3
PPFD > 500 µmol m−2 s−1
(% of time)
57.6 ± 2.5
0.94 ± 1.7
PPFD > 200 µmol m−2 s−1
(% of time)
72.4 ± 1.0
3.5 ± 4.0
PPFD ≥ 50 µmol m−2 s−1
(% of time)
84.2 ± 3.8
28.2 ± 19.7
PPFD due to sunflecks
(% of daily)
----
32.4 ± 22.0
31.5 ± 36.1
50% of day length). The peak PPFDs due to sunflecks varied
from 170 to 1120 µmol m −2 s −1; sunflecks contributed between
6.8 and 58.9% of total PPFD.
Results
Dynamic photosynthetic induction response
Light availability
There was a larger but slower increase in net photosynthetic rate
in open-grown branches than in understory-grown branches
exposed to PPFDs of 500 µmol m −2 s −1and 200 µmol m −2 s −1
Branches of open-grown seedlings received a mean PPFD of
702.5 µmol m −2 s −1 and a mean daily PPFD of 40.5 mol m −2
day −1, whereas understory-grown seedlings received a mean
PPFD of 52 µmol m −2 s −1 and a mean daily PPFD of 2.8 mol
m −2 day −1 (Table 1). Branches of understory-grown seedlings
received a mean of 7.4% full sun PPFD, with sunflecks contributing 32.4% of the daily photon flux (Table 1). Representative daily courses of PPFD in the forest understory and
the open are shown in Figure 1.
The light environment varied greatly among measured
branches from different understory seedlings; mean PPFD
ranged from 18.4 to 85 µmol m −2 s −1 and mean daily PPFD
ranged from 1.1 to 4.6 mol m −2 day −1. The percent of full sun
PPFD had a range of 3 to 12%. The daily cumulated amount
of time that branches received a PPFD above 500 µmol
m −2 s−1 and 200 µmol m −2 s −1 ranged from 0 to 31 min (0 to
3.2% of day length) and 0 to 83 min (0 to 8.7% of day length),
respectively. The daily cumulated amount of time branches
received direct radiation ranged from 44 to 485 min (4.6 to
Figure 1. Representative daily courses of light availability for a seedling branch in the forest understory and in the open. Measurements
were made on August 2, 1994.
26
CHEN AND KLINKA
following 10 min at a PPFD of 50 µmol m −2 s −1 (Figures 2
and 3, Table 2). At a PPFD of 500 µmol m −2 s −1, the mean
times required by understory-grown branches to reach 50 and
90% of steady-state photosynthetic rate were 85 and 200 s,
respectively; corresponding mean times for open-grown
branches were 99 and 304 s (Figure 2b, Table 2). At a PPFD of
200 µmol m −2 s−1, the mean times required by understorygrown branches to reach 50 and 90% induction were 63 and
173 s, respectively; corresponding mean times for open-grown
branches were 81 and 162 s (Figure 3b, Table 2).
Both understory- and open-grown branches were slower to
reach full induction at a PPFD of 500 µmol m −2 s −1 than at a
PPFD of 200 µmol m −2 s −1 (Figures 2b and 3b, Table 2). Times
taken for understory- and open-grown branches to reach 100%
induction state at a PPFD of 500 µmol m −2 s −1 were 300 and
500 s, respectively, and 240 s for both at a PPFD of 200 µmol
m −2 s −1.
Light-response curves
Understory- and open-grown branches had different net photosynthetic responses to steady-state PPFDs (Figures 4a and
4b). Compared to open-grown branches, understory-grown
branches had a significantly (P < 0.05) lower dark respiration
rate (0.44 ± 0.01 versus 0.77 ± 0.03 µmol m −2 s −1), higher
area-based net photosynthetic rate at a PPFD of 50 µmol m −2
s −1, and lower area-based net photosynthetic rates at PPFDs
higher than 350 µmol m −2 s −1 (Figure 4a). At PPFDs of 200
Figure 3. (a) Net photosynthetic rates (Pn) and (b) induction responses
to an increase in irradiance from a 10-min PPFD of 50 µmol m−2 s−1
to a PPFD of 200 µmol m−2 s−1 starting at time 0 for open-grown
(closed circles) and understory branches (open circles). Each point is
the mean (± SE) of single measurements from five seedlings.
Table 2. Mean (± SE) time (s) required to reach 50 and 90% steadystate net photosynthetic rate for open- and understory-grown seedling
branches following 10 min at a PPFD of 50 µmol m−2 s−1. Values
followed by the same letter are not significantly different at the same
induction state between open- and understory-grown branches
(P < 0.05).
PPFD
50%
−2 −1
(µmol m
Figure 2. (a) Net photosynthetic rates (Pn) and (b) induction responses
to an increase in irradiance from a 10-min PPFD of 50 µmol m− 2 s−1
to a PPFD of 500 µmol m−2 s−1 starting at time 0 for open-grown
(closed circles) and understory-grown branches (open circles). Each
point is the mean (± SE) of single measurements from five seedlings.
s ) Open
90%
Understory
Open
Understory
500
99 ± 12.5 a 85 ± 11.5 a
304 ± 45.3 a 200 ± 15.5 b
200
81 ± 5.6 a
162 ± 5.0 a
63 ± 5.2 b
173 ± 17.6 a
and 350 µmol m −2 s −1, no difference in net photosynthetic
rates between understory- and open-grown branches was observed. At a PPFD of 50 µmol m −2 s −1, the light compensation
point was lower for understory-grown branches compared to
open-grown branches, as shown by their net photosynthetic
rates (0.23 ± 0.02 versus --0.11 ± 0.07 µmol m −2 s −1). Understory-grown branches reached 90% of their light-saturated net
photosynthetic rate at a PPFD of 500 µmol m −2 s −1, whereas
open-grown branches did not reach 90% of their light-saturated rate even at a PPFD of 1000 µmol m −2 s −1. At supersaturating PPFD, photosynthetic rates decreased, suggesting the
onset of photoinhibition (not shown). Threshold PPFD for
LIGHT AVAILABILITY AND PHOTOSYNTHESIS OF PSEUDOTSUGA
photoinhibition was between 800 and 1400 µmol m −2 s−1 for
understory-grown branches and at 1800 µmol m−2 s −1 for
open-grown branches.
Differences between understory- and open-grown branches
were less pronounced when data were expressed on a leaf mass
basis (Figure 4b). There was little difference in dark respiration
rates between understory- and open-grown branches (P = 0.33).
Net photosynthetic rates were significantly higher (P < 0.05)
for understory-grown than for open-grown branches at PPFDs
of 50 and 200 µmol m −2 s−1. At PPFDs equal to or greater than
350 µmol m −2 s −1, no significant difference in net photosynthetic rates was found between open- and understory-grown
branches (P > 0.05).
Discussion
Understory light availability
Understory-grown branches received a mean daily PPFD of
2.8 mol m −2 day −1 or 7.4% of full sun, with sunflecks contributing 32.4% of the daily total (Table 1). Light availability
under the forest canopy was higher than that reported for low
latitude conifer forests and tropical rain forests (Chazdon
1988, Canham et al. 1990). The contribution of sunflecks to
daily PPFD was similar to that found in a montane red spruce-balsam fir forest in the Appalachian Mountains of the eastern
USA (Canham et al. 1990).
Figure 4. Photosynthetic light-response curves for open-grown (closed
circles) and understory-grown branches (open circles). (a) Net photosynthetic rate (Pn) on a projected leaf area basis and (b) net photosynthetic rate (Pn) on a dry needle mass basis. Each point is the mean of
five measurements on each branch.
27
Light availability and sunfleck duration and intensity within
the stand varied greatly among branches from different seedlings. Similar results were reported for understory light environments of tropical rain forests (Chazdon 1986). Such spatial
variability depends on distances from gaps (Canham et al.
1990, Chazdon and Pearcy 1991) and the clumping effect of
overstory leaves (Chen and Black 1992, Baldocchi and Collineau 1994). Diffuse and direct components were not measured separately in this study; instead, a PPFD of 50 µmol
m −2 s −1 was used to discriminate between diffuse light and
direct light (e.g., Chazdon 1986, Koizumi and Oshima 1993).
However, both the direct component and the diffuse components may vary spatially and diurnally within a forest stand
(Black et al. 1991).
Dynamic and steady-state photosynthesis
Pseudotsuga menziesii seedlings acclimated photosynthetically to their light environments under field conditions. Photosynthetic induction responses to PPFD changes were quicker
in understory-grown branches than in open-grown branches.
This pattern is consistent with studies in a tropical forest
(Küppers et al. 1996) and in controlled environments on some
broadleaf plants (Pons and Pearcy 1992, Tang et al. 1994).
Photosynthetic induction responses of P. menziesii branches
tended to be faster than those of Quercus serrata Thunb. (Tang
et al. 1994) but shorter than those of desiccation-tolerant Polypodium virginianum L. (Gildner and Larson 1992). However,
the time required to reach full photosynthetic induction varies
among species (Chazdon 1988) and depends on: (i) length of
the period and PPFD of low light condition (Pons et al. 1992,
Whitehead and Teskey 1995), and (ii) other ecological factors
such as water status. Photosynthetic induction responses tend
to be faster in the field than in the laboratory (Gildner and
Larson 1992), and water-stressed plants reach their maximum
stomatal conductance in less time than unstressed plants (Tinoco-Ojanguren and Pearcy 1993, Barradas et al. 1994). We
also found that the time required to reach full photosynthetic
induction depended on PPFD. With increasing PPFD, more
time was required for both understory and open-grown
P. menziesii branches to reach full photosynthetic induction.
Acclimation of dark respiration under sun versus shade
conditions has been studied at the leaf and whole-plant levels
(Björkman 1981, Chazdon and Kaufmann 1993, Letho and
Grace 1994, Sims and Pearcy 1994, Intrieri et al. 1995, TinocoOjanguren and Pearcy 1995). Plants acclimated to low light
environments have low dark respiration rates when expressed
on a unit leaf area basis. Similarly, in this study, understorygrown branches of P. menziesii had lower dark respiration rates
per unit of leaf area than open-grown branches. On a dry leaf
mass basis, however, dark respiration rates did not differ between the understory- and open-grown branches.
Compared to open-grown branches, understory-grown
branches were photosynthetically more efficient at low PPFDs
but less efficient at high PPFDs (Leverenz 1995). Based on per
unit dry leaf mass, net photosynthetic light-use efficiency in
understory-grown branches was equal to or higher than that of
open-grown branches at all PPFDs except those inducing pho-
28
CHEN AND KLINKA
toinhibition. This pattern has also been observed in some
species at the leaf and whole-plant levels (Björkman 1981,
Sims and Pearcy 1994, Leverenz 1995). Thus, compared with
sun plants, shade plants exhibit no disadvantage in terms of
carbon gain per unit dry mass unless photoinhibited.
There are qualitative and quantitative differences in light
response among individual needles, shoots, and whole plants
(Pearcy and Sims 1994, Leverenz 1995, Stenberg et al. 1995).
This study describes the dynamic and steady-state photosynthetic behavior of P. menziesii at the lateral-shoot level, which
integrates both photosynthesis of needles and the structural
factor of their distribution. However, photosynthetic behavior
at the individual needle and whole-plant levels was not considered. Moreover, computer simulations of dynamic and steadystate photosynthesis in relation to natural light regimes in
P. menziesii seedlings may be needed to understand the daily
and seasonal carbon balance and the relative importance of
dynamic and steady-state photosynthetic plasticity.
Acknowledgments
We especially thank Dr. Robert D. Guy, Department of Forest Sciences, University of British Columbia, for his continuous encouragement during this study and valuable comments on the manuscript. We
also thank Dr. T.A. Black for his useful comments on the manuscript.
Financial support from the Natural Science and Engineering Research
Council of Canada, and B.C. Ministry of Forests, Silviculture Branch
is acknowledged.
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