Directory UMM :Data Elmu:jurnal:T:Tree Physiology:Vol14.1994:
Tree Physiology 14, 1291-1301
© 1994 Heron Publishing----Victoria, Canada
Photosynthesis of a tropical canopy tree, Ceiba pentandra, in a
lowland forest in Panama
GERHARD ZOTZ and KLAUS WINTER
Smithsonian Tropical Research Institute, P.O. Box 2072, Balboa, Republic of Panama
Received December 1, 1993
Summary
Diel (24 h) courses of CO2 and water-vapor exchange of Ceiba pentandra (L.) Gaertn. (Bombacaceae)
were studied under natural tropical conditions in the semi-evergreen moist forest of Barro Colorado
Island, Panama. Measurements were conducted from early February 1991 (dry season), shortly after new
leaves emerged, until mid-October 1991 (wet season), when leaves were shed. Rates of net CO2 uptake
were significantly higher in the dry season than in the wet season, and showed a linear decrease with leaf
age. Leaf nitrogen concentrations and contents also decreased with age. Our estimate of annual carbon
gain (2640 g CO2 m −2 year − 1 or 21 g CO2 gDW−1 year − 1) is considerably higher than estimates available
for temperate forest trees.
Keywords: carbon balance, CO2 exchange, nitrogen, tropical rain forest, water vapor exchange.
Introduction
Ceiba pentandra (L.) Gaertn., locally known as ‘bongo’ or ‘Ceiba,’ is a light-demanding pioneer tree that occurs naturally in the Neotropics and West Africa (Baker 1965).
It is known for its rapid growth and persistence in climax forests, where it is often
one of the tallest emergent trees (Croat 1978, Gentry and Terborgh 1990, Whitmore
1990). Although the ecology and evolutionary history of the Ceiba tree have been
studied extensively (Baker and Harris 1959, Baker 1965, 1973, 1983, Augspurger
1984), little is known about its physiology. This is particularly true for measurements
in its natural habitat. The scarcity of our knowledge of the performance of mature
specimens of this and other rain-forest tree species is primarily related to the
difficulty of gaining access to the canopy. By means of a metal ladder and rope
climbing techniques, we were able to monitor diel patterns of photosynthesis,
stomatal conductance and water relations over the entire life span of exposed leaves
of a 47-m tall C. pentandra on Barro Colorado Island, Panama. This enabled us to
separate seasonal and age-related influences on the photosynthetic performance of
C. pentandra, and to obtain a first estimate of the long-term carbon budget of the
canopy leaves of a tropical rain-forest tree.
Materials and methods
Habitat and plant material
The study was conducted on Barro Colorado Island (9°10′ N, 79°51′ W), Republic
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ZOTZ AND WINTER
of Panama. The vegetation of this nature reserve is classified as tropical moist forest
(Holdridge et al. 1971) or as semi-evergreen moist tropical forest (Knight 1975).
Annual rainfall is about 2600 mm; a pronounced dry season lasts from late December
to April. More detailed descriptions of vegetation, climate and ecology are provided
by Croat (1978) and Leigh et al. (1982).
Measurements of CO2 and water-vapor exchange were performed in situ from
February to October 1991 on mature, randomly selected outer-canopy leaves of an
emergent 47-m tall Ceiba tree. Ceiba pentandra is deciduous. The length of the
leafless period depends on whether the tree flowers and fruits in the late rainy and
early dry season. On average, a given tree flowers every 2--3 years (D. Windsor,
unpublished data). Flowering trees remain leafless for about three months, whereas
nonflowering trees develop an entire new canopy within two weeks after the old
leaves have been shed.
Gas exchange
As described in detail earlier (Zotz and Winter 1993), leaf gas exchange was
measured with a CO2/H2O-porometer (CQP 130, Walz, Effeltrich, Germany), operating in a continuous open-flow mode. The equipment was set up in the canopy at a
height of 35 m, and the length of the tubing between the leaf chamber and the gas
analyzer was approximately 10 m. Air was taken from within the top part of the
crown of the study tree and fed through the system. External temperature and relative
humidity were tracked inside the leaf cuvette. Data were collected at 5-min intervals
(daytime) or at 15-min intervals (nighttime). Gas exchange parameters were calculated as described by von Caemmerer and Farquhar (1981). Integration of the diel
curves of photosynthetic photon flux density (PPFD), net CO2 exchange (A) and
transpiration (E) was accomplished with a digitizing tablet. Water use efficiency
(WUE) was computed by dividing diel carbon gain by diel water loss. Carbon
budgets were computed over 24-h periods. Estimates of annual carbon gain and
transpirational water loss were based on the diel CO2 and H2O budgets.
Responses of stomatal conductance (gw) to changes in the leaf--air vapor pressure
difference (∆w) were investigated with a LI-1600 steady-state porometer (Li-Cor
Inc., Lincoln, NE, USA). Measurements were conducted in situ before 1000 h on
overcast days. Additional light was supplied by a 150 W halogen lamp such that the
total PPFD was about 1300 µmol m −2 s −1. The ∆w was increased in steps of 4 mPa
Pa −1 from about 4 to 16 mPa Pa − 1. Several times, determinations at 4 mPa Pa −1 were
repeated after the final measurement to check for hysteresis.
The CO2 concentration of the surrounding air was determined at about hourly
intervals with a BINOS 100 (Heraeus, Hanau, Germany). Air was drawn from within
the upper canopy of the Ceiba tree and the BINOS flushed for 1--2 min before a
reading was taken.
The CO2 gas analyzers were calibrated in the laboratory before and after the study
period using gas mixing pumps (Wösthoff KG, Bochum, Germany) at concentrations
of 100, 200, 250, 300, 400 and 500 µl l −1 CO2. In the field, these calibrations were
SEASONAL CHANGES IN PHOTOSYNTHESIS OF CEIBA
3
routinely checked with calibration gases (Scott, Wakefield, MA, USA). The water
vapor analyzer was calibrated at intervals of 2--3 months by means of electronically
controlled cold traps (Walz, Effeltrich, Germany).
Water relations, mineral nutrient contents and other measurements
Leaf water potential (Ψ) and osmotic pressure of leaf sap (π) were measured
psychrometrically on leaf discs at 30 °C with five thermocouple psychrometers
(model C-52) and an HR-33T dew point microvoltmeter (Wescor, Logan, UT, USA).
Following measurement of Ψ, leaf disks were frozen and thawed, allowing the
determination of π. The difference between Ψ and π was taken as an estimate of
turgor pressure.
To determine mineral element contents, the leaves used in the gas exchange
measurements (one to four) and additional leaves of similar age and appearance (two
to three) were collected throughout the study period. Their age ranged from six weeks
to ten months. Leaf area was measured with a leaf area meter (LI-3100, Li-Cor Inc.,
Lincoln, NE). All samples were dried at 60 °C for 48 h, weighed to obtain the ratio
of leaf weight to leaf area (W), ground and analyzed at the University of Würzburg
(Germany) with a CHN-O Element Analyzer (Heraeus, Hanau, Germany) and an ICP
Spectrometer JY 70 Plus (ISA, München, Germany).
Stomatal densities were determined from impressions made with nail polish.
Results
Diel and seasonal changes in CO2 concentration in the canopy
Diel changes in the CO2 concentration in the canopy of the Ceiba tree were characterized by maxima in the morning shortly after dawn and minima in the early
afternoon. Several times the CO2 concentration fell below 320 µl l −1 (Figure 1), but
it rarely increased above 380 µl l −1. Diel fluctuations were significantly larger in the
rainy season (31.1 ± 14.3 µl l −1, n = 48) than in the dry season (15.6 ± 4.9 µl l −1, n =
36) (t-test, P < 0.001).
Seasonal changes in CO2 gas exchange
Figure 2 shows four examples of diel courses of microclimatic conditions, net CO2
exchange and other gas exchange parameters during the dry season (February 7,
March 8) and the wet season (July 7, October 17). Important gas exchange and water
status parameters of the 13 study days are given in Figure 3 and Table 1.
The dry season was characterized by high PPFDs, low relative humidities (rh) and
high wind velocities. Maximum PPFD exceeded 2000 µmol m −2 s −1 on most days,
whereas rh often dropped to 50% around noon. Predawn water potential (Ψpr)
averaged −1.0 MPa (Figure 3), and the osmotic pressure (π) was 1.5 MPa. Around
noon, decreases in Ψ resulted in decreases in turgor pressure. On one day (February 7), the decrease in Ψ was accompanied by a transient reduction in stomatal
4
ZOTZ AND WINTER
Figure 1. Diel changes in atmospheric CO2 concentration in the crown of a Ceiba pentandra. Given are
mimima (s) and maxima (●) for each of 84 days during 1991. The CO2 concentrations were determined
at approximately hourly intervals during the day and every 3--5 h at night. The dry and wet seasons are
indicated by open and hatched bars, respectively.
Figure 2. Representative diel courses of gas exchange in situ in Ceiba pentandra in the dry (February 7,
March 8) and wet (July 7, October 17) season. Shown are photosynthetic photon flux density (PPFD),
net CO2 exchange (A), leaf (Tl) and ambient temperature (Ta), leaf to air vapor pressure difference (∆w),
stomatal conductance for water vapor (gw), and internal CO2 concentration (ci).
SEASONAL CHANGES IN PHOTOSYNTHESIS OF CEIBA
5
Figure 3. Annual course of gas exchange and water relations parameters in Ceiba pentandra. (a) Weekly
rainfall (mm), (b) daily integrated PPFD (mol m −2 day −1), (c) daily integrated net CO2 balance (mmol
CO2 m −2 day −1; open bars) and nocturnal CO2 loss (mmol CO2 m −2 night − 1; closed bars), (d) daily
integrated water use efficiency (mmol CO2 mol H2O − 1), (e) predawn water potential (s), osmotic
pressure (●) and estimated turgor pressure (connecting line), and (f) water potential (s), osmotic
pressure (●) and estimated turgor pressure (connecting line) at 1300 h.
conductance (gw) (Figure 2a), but on all other days of the dry season, gw stayed high
at about 200 mmol m −2 s −1. Highest rates of net CO2 uptake (Amax) were observed in
early March (dry season) after an unusual rainstorm with more than 170 mm of
precipitation in 36 h; Amax exceeded 18 µmol m −2 s −1 on March 8 (Figure 2) and the
resulting 24-h carbon gain was 370 mmol m −2 day −1.
Clouds and frequent rainstorms led to a significant reduction in PPFD during the
rainy season (Figure 2, July 7). The water status of the leaves changed little, but
complete turgor loss no longer occurred at noon (Figure 3). Even though environmental conditions seemed conducive to photosynthesis, the maximum rates of net
6
ZOTZ AND WINTER
Table 1. Photosynthetic and leaf characteristics of Ceiba pentandra. Gas exchange characteristics are
derived from diel measurements in situ.
Parameter
n
Mean ± SD
Leaflet size (cm2)1
W (gfw m − 2)
W (gdw m −2)
Thickness (mm)
Stomata (number mm −2)
Light compensation point (µmol m − 2 s − 1)
Mean respiration rate (µmol m −2 s −1)
Leaf N (mmol m −2)
Leaf P (mmol m −2)
Leaf K (mmol m −2)
28
28
28
13
8
13
13
14
14
14
28.8 ± 7.4
277.5 ± 22.1
124.2 ± 12.9
0.27 ± 0.02
180 ± 21
21.2 ± 5.5
0.43 ± 0.21
143 ± 14.2
4.5 ± 6.4
35.8 ± 7.7
1
Leaves consist of 6--8 leaflets.
CO2 uptake (8 to 11.8 µmol m −2 s −1 ) were much lower than in the dry season
(Figure 2) and consequently, the 24-h carbon budgets were also lower (Figure 3). The
differences in diel carbon gain between the dry and wet season were significant even
when the two days in March after the unusual rainstorm were excluded from the
analysis (t-test, P < 0.05).
Integration of CO2 gain and transpirational water loss over the entire study period
yielded 2640 g CO2 m −2 year −1 and 409 kg H2O m −2 year −1, and the long-term water
use efficiency was 6.5 g CO2 kg −1 H2O.
Variability of Amax and diel carbon gain between leaves
The variation in Amax and diel carbon gain (A24h) between leaves on a given day was
small. On September 29, 1991, we studied four mature sun leaves simultaneously.
The leaves showed maximum rates of CO2 uptake of 8.6 ± 0.7 µmol m −2 s −1 (mean
± SE) and diel carbon budgets of 142.5 ± 2.1 mmol m −2 day −1 (mean ± SE).
Correlations of gas exchange parameters, leaf age and leaf nitrogen content
The observed decline in Amax during the year was not caused by seasonal changes in
incident radiation. Leaves received saturating PPFD (about 500 µmol m −2 s −1) for
most of the day (Zotz and Winter 1993), and there was no correlation between
integrated PPFD and Amax (r2 = 0.03, P > 0.1, df = 12).
The maximum rate of net CO2 uptake was correlated with leaf age (r2 = 0.48, P <
0.01, df = 13). Because leaf nitrogen concentrations and contents also decreased with
leaf age, changes in Amax were closely related to changes in leaf N (r2 = 0.77, P <
0.001 weight-based; r2 = 0.31, P < 0.05 area-based; Figure 4). Net CO2 uptake and
stomatal conductance were closely correlated throughout the study period. During
individual days, changes in A paralleled changes in gw, i.e., the internal CO2 partial
pressure (ci) remained almost constant (Figure 2). Over the entire leaf life span, the
relationship between Amax and gw at Amax (gw,Amax) did not change (r2 = 0.88, P <
SEASONAL CHANGES IN PHOTOSYNTHESIS OF CEIBA
7
Figure 4. Correlations of leaf nitrogen concentration (a) and leaf nitrogen content (b) with maximum rate
of CO2 uptake (Amax) in leaves of Ceiba pentandra on 14 days from February through October 1991.
Both regression lines are significant (P < 0.05).
0.001; Figure 5).
The maximum rate of net CO2 uptake was strongly correlated with diel carbon gain
(A24h) (r2 = 0.85, P < 0.001, see Zotz and Winter 1993). Consequently, our analysis
for Amax was also valid for A24h.
Changes in stomatal conductance with increasing leaf age
Young leaves (one month old) showed maximum stomatal conductances of 600
mmol m −2 s −1 (Figure 6a). Increasing ∆w from 4.9 to 17.2 mPa Pa −1 led to a gradual
reduction in gw, whereas transpiration rates increased from 2.3 to 5 mmol m −2 s −1.
Figure 5. Correlation of maximum rate of CO2 uptake (Amax) and stomatal conductance at Amax (gw,Amax).
Data are derived from 13 complete diel courses and one incomplete course of net CO2 exchange.
8
ZOTZ AND WINTER
Figure 6. Response of stomatal conductance (gw) and transpiration (E) to leaf--air water vapor pressure
difference (∆w). Measurements were performed in situ on one-month-old (a), four-month-old (b) and
ten-month-old (c, d, e) leaves of Ceiba pentandra. Data are means ± SD. The number of leaves studied
was 5 (a), 7 (b), 5 (c), 7 (d) and 4 (e).
Three months later, the stomatal response to changing ∆w was similar, although gw
was slightly lower at higher values of ∆w (Figure 6b). A few weeks before leaf
abscission (ten-month-old leaves), three different patterns of stomatal response were
observed. The stomatal response of one group of leaves was similar to that of younger
leaves, but at the higher values of ∆w, gw was consistently lower by about 100 mmol
m −2 s −1 (Figure 6c). A second group of leaves exhibited large reductions in gw (Figure
6d). Even at the lowest ∆w of 5.0 mPa Pa −1, gw reached only 300 mmol m −2 s −1. In
a third group of leaves, gw increased with increasing ∆w up to 12 mPa Pa −1 and
SEASONAL CHANGES IN PHOTOSYNTHESIS OF CEIBA
9
decreased at higher values of ∆w (Figure 6e).
Discussion
It is generally assumed that plants in a seasonal tropical climate suffer a large
reduction in net CO2 uptake, growth and survival during times of drought (Lugo et
al. 1978, Medina and Klinge 1983, Landsberg 1984, Reich and Borchert 1984,
Robichaux et al. 1984). Many trees on Barro Colorado Island are drought-deciduous,
and thus avoid the potentially stressful dry season (Croat 1978). Ceibapentandra, however, develops a new set of leaves at the beginning of the dry season (Croat 1978, D.
Windsor, unpublished data). This phenological pattern suggests that the species has
ready access to deep soil water. However, no information is available about the root
system of C. pentandra. We also do not know the extent to which stored water in the
large trunk is, at least for short periods, important in maintaining transpiration of the
leaves. However, consistent with the notion of uninterrupted water supply throughout
the year, we found high values of gw, A and Ψpr during the dry season. Nevertheless,
the water supply was not sufficient to support maximum photosynthetic CO2 uptake,
because we observed a large increase in Amax immediately after an unusual rainstorm
in the dry season (March 1991 in Figures 2 and 3). Diel carbon gain was significantly
higher in the dry season.
We conclude that, in C. pentandra, ontogenetic developments influence Amax and
A24h more than seasonal changes in water availability and climatic conditions. The
maximum rate of net CO2 uptake decreased linearly with leaf age and was positively
correlated with leaf N content. Photosynthetic capacity and leaf N are strongly
correlated in many plant species (Field and Mooney 1986, Evans 1989, Reich et al.
1991). The strong correlation between Amax and gw,Amax (Figure 5) suggests that the
age-related changes in Amax are caused by a reduction in photosynthetic capacity.
Such a correlation is in accordance with models of optimal stomatal regulation
(Cowan and Farquhar 1977, Cowan 1982, Schulze and Hall 1982). A gradual
decrease in gw with leaf age was also observed in a study of the ∆w response as a
function of leaf age (Figure 6). The loss of stomatal responsiveness in at least some
leaves a few days before abscission is consistent with previous observations on other
tropical tree species (Borchert 1979). The differences in conductance patterns in
Ceiba leaves of similar age (Figures 6c--e) might be related to slight asynchrony in
senescence. It is not known whether the loss of stomatal control, as indicated in
Figure 6e, is causally related with leaf shedding, e.g., by producing large tissue water
deficits.
Long-term carbon gain and water-use efficiency can only be compared with
temperate-zone tree species, because no equivalent data are available for other
tropical trees. Surprisingly, the long-term water-use efficiency of C. pentandra (6.5 ×
10 −3 g CO2 g −1 H2O) was low compared to some temperate tree species, e.g., Fagus
sylvatica L. (8.2 × 10 −3 g CO2 g −1 H2O, Schulze 1970) and Acer campestre L. (17.1 ×
10 −3 g CO2 g −1 H2O, Küppers 1984). The annual leaf carbon gain, however, was
10
ZOTZ AND WINTER
higher (2640 g CO2 m −2 year −1 or 21 g CO2 gDW−1 year −1) compared with 8 to 13 g
CO2 gDW−1 year −1 for F. sylvatica (Schulze 1970, Künstle and Mitscherlich 1977),
14 g CO2 gDW−1 year −1 for Betula verrucosa Ehrh. (Künstle and Mitscherlich 1977)
and 15 g CO2 gDW−1 year −1 for the pioneer tree, A. campestre (Küppers 1984). Our
estimate is comparable with that of Okali (1971) for C. pentandra seedlings which
gained 54 to 60 gDW m −2 week −1 (= 8.6 gDW m −2 day −1) under optimal conditions.
This corresponds to 16 g CO2 m −2 day −1 (= 370 mmol CO2 m −2 day −1) based on a
factor of 1.88 for the conversion of dry weight to CO2 (Penning de Vries 1975), which
matches the highest 24-h carbon gain observed in this study.
Acknowledgments
G.Z. was on leave from Lehrstuhl Botanik II, Universität Würzburg, Germany and was supported by a
doctoral fellowship of the Deutsche Forschungsgemeinschaft (SFB 251, Universität Würzburg). The SFB
251 also provided facilities for mineral element analysis, and we are grateful to F. Reisberg and M. Lesch
for performing these measurements. We thank Miguel Piñeros for excellent field assistance and Dr. Tom
Kursar, Dr. Greg Gilbert and two anonymous reviewers for critical comments on earlier drafts of the
manuscript.
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© 1994 Heron Publishing----Victoria, Canada
Photosynthesis of a tropical canopy tree, Ceiba pentandra, in a
lowland forest in Panama
GERHARD ZOTZ and KLAUS WINTER
Smithsonian Tropical Research Institute, P.O. Box 2072, Balboa, Republic of Panama
Received December 1, 1993
Summary
Diel (24 h) courses of CO2 and water-vapor exchange of Ceiba pentandra (L.) Gaertn. (Bombacaceae)
were studied under natural tropical conditions in the semi-evergreen moist forest of Barro Colorado
Island, Panama. Measurements were conducted from early February 1991 (dry season), shortly after new
leaves emerged, until mid-October 1991 (wet season), when leaves were shed. Rates of net CO2 uptake
were significantly higher in the dry season than in the wet season, and showed a linear decrease with leaf
age. Leaf nitrogen concentrations and contents also decreased with age. Our estimate of annual carbon
gain (2640 g CO2 m −2 year − 1 or 21 g CO2 gDW−1 year − 1) is considerably higher than estimates available
for temperate forest trees.
Keywords: carbon balance, CO2 exchange, nitrogen, tropical rain forest, water vapor exchange.
Introduction
Ceiba pentandra (L.) Gaertn., locally known as ‘bongo’ or ‘Ceiba,’ is a light-demanding pioneer tree that occurs naturally in the Neotropics and West Africa (Baker 1965).
It is known for its rapid growth and persistence in climax forests, where it is often
one of the tallest emergent trees (Croat 1978, Gentry and Terborgh 1990, Whitmore
1990). Although the ecology and evolutionary history of the Ceiba tree have been
studied extensively (Baker and Harris 1959, Baker 1965, 1973, 1983, Augspurger
1984), little is known about its physiology. This is particularly true for measurements
in its natural habitat. The scarcity of our knowledge of the performance of mature
specimens of this and other rain-forest tree species is primarily related to the
difficulty of gaining access to the canopy. By means of a metal ladder and rope
climbing techniques, we were able to monitor diel patterns of photosynthesis,
stomatal conductance and water relations over the entire life span of exposed leaves
of a 47-m tall C. pentandra on Barro Colorado Island, Panama. This enabled us to
separate seasonal and age-related influences on the photosynthetic performance of
C. pentandra, and to obtain a first estimate of the long-term carbon budget of the
canopy leaves of a tropical rain-forest tree.
Materials and methods
Habitat and plant material
The study was conducted on Barro Colorado Island (9°10′ N, 79°51′ W), Republic
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ZOTZ AND WINTER
of Panama. The vegetation of this nature reserve is classified as tropical moist forest
(Holdridge et al. 1971) or as semi-evergreen moist tropical forest (Knight 1975).
Annual rainfall is about 2600 mm; a pronounced dry season lasts from late December
to April. More detailed descriptions of vegetation, climate and ecology are provided
by Croat (1978) and Leigh et al. (1982).
Measurements of CO2 and water-vapor exchange were performed in situ from
February to October 1991 on mature, randomly selected outer-canopy leaves of an
emergent 47-m tall Ceiba tree. Ceiba pentandra is deciduous. The length of the
leafless period depends on whether the tree flowers and fruits in the late rainy and
early dry season. On average, a given tree flowers every 2--3 years (D. Windsor,
unpublished data). Flowering trees remain leafless for about three months, whereas
nonflowering trees develop an entire new canopy within two weeks after the old
leaves have been shed.
Gas exchange
As described in detail earlier (Zotz and Winter 1993), leaf gas exchange was
measured with a CO2/H2O-porometer (CQP 130, Walz, Effeltrich, Germany), operating in a continuous open-flow mode. The equipment was set up in the canopy at a
height of 35 m, and the length of the tubing between the leaf chamber and the gas
analyzer was approximately 10 m. Air was taken from within the top part of the
crown of the study tree and fed through the system. External temperature and relative
humidity were tracked inside the leaf cuvette. Data were collected at 5-min intervals
(daytime) or at 15-min intervals (nighttime). Gas exchange parameters were calculated as described by von Caemmerer and Farquhar (1981). Integration of the diel
curves of photosynthetic photon flux density (PPFD), net CO2 exchange (A) and
transpiration (E) was accomplished with a digitizing tablet. Water use efficiency
(WUE) was computed by dividing diel carbon gain by diel water loss. Carbon
budgets were computed over 24-h periods. Estimates of annual carbon gain and
transpirational water loss were based on the diel CO2 and H2O budgets.
Responses of stomatal conductance (gw) to changes in the leaf--air vapor pressure
difference (∆w) were investigated with a LI-1600 steady-state porometer (Li-Cor
Inc., Lincoln, NE, USA). Measurements were conducted in situ before 1000 h on
overcast days. Additional light was supplied by a 150 W halogen lamp such that the
total PPFD was about 1300 µmol m −2 s −1. The ∆w was increased in steps of 4 mPa
Pa −1 from about 4 to 16 mPa Pa − 1. Several times, determinations at 4 mPa Pa −1 were
repeated after the final measurement to check for hysteresis.
The CO2 concentration of the surrounding air was determined at about hourly
intervals with a BINOS 100 (Heraeus, Hanau, Germany). Air was drawn from within
the upper canopy of the Ceiba tree and the BINOS flushed for 1--2 min before a
reading was taken.
The CO2 gas analyzers were calibrated in the laboratory before and after the study
period using gas mixing pumps (Wösthoff KG, Bochum, Germany) at concentrations
of 100, 200, 250, 300, 400 and 500 µl l −1 CO2. In the field, these calibrations were
SEASONAL CHANGES IN PHOTOSYNTHESIS OF CEIBA
3
routinely checked with calibration gases (Scott, Wakefield, MA, USA). The water
vapor analyzer was calibrated at intervals of 2--3 months by means of electronically
controlled cold traps (Walz, Effeltrich, Germany).
Water relations, mineral nutrient contents and other measurements
Leaf water potential (Ψ) and osmotic pressure of leaf sap (π) were measured
psychrometrically on leaf discs at 30 °C with five thermocouple psychrometers
(model C-52) and an HR-33T dew point microvoltmeter (Wescor, Logan, UT, USA).
Following measurement of Ψ, leaf disks were frozen and thawed, allowing the
determination of π. The difference between Ψ and π was taken as an estimate of
turgor pressure.
To determine mineral element contents, the leaves used in the gas exchange
measurements (one to four) and additional leaves of similar age and appearance (two
to three) were collected throughout the study period. Their age ranged from six weeks
to ten months. Leaf area was measured with a leaf area meter (LI-3100, Li-Cor Inc.,
Lincoln, NE). All samples were dried at 60 °C for 48 h, weighed to obtain the ratio
of leaf weight to leaf area (W), ground and analyzed at the University of Würzburg
(Germany) with a CHN-O Element Analyzer (Heraeus, Hanau, Germany) and an ICP
Spectrometer JY 70 Plus (ISA, München, Germany).
Stomatal densities were determined from impressions made with nail polish.
Results
Diel and seasonal changes in CO2 concentration in the canopy
Diel changes in the CO2 concentration in the canopy of the Ceiba tree were characterized by maxima in the morning shortly after dawn and minima in the early
afternoon. Several times the CO2 concentration fell below 320 µl l −1 (Figure 1), but
it rarely increased above 380 µl l −1. Diel fluctuations were significantly larger in the
rainy season (31.1 ± 14.3 µl l −1, n = 48) than in the dry season (15.6 ± 4.9 µl l −1, n =
36) (t-test, P < 0.001).
Seasonal changes in CO2 gas exchange
Figure 2 shows four examples of diel courses of microclimatic conditions, net CO2
exchange and other gas exchange parameters during the dry season (February 7,
March 8) and the wet season (July 7, October 17). Important gas exchange and water
status parameters of the 13 study days are given in Figure 3 and Table 1.
The dry season was characterized by high PPFDs, low relative humidities (rh) and
high wind velocities. Maximum PPFD exceeded 2000 µmol m −2 s −1 on most days,
whereas rh often dropped to 50% around noon. Predawn water potential (Ψpr)
averaged −1.0 MPa (Figure 3), and the osmotic pressure (π) was 1.5 MPa. Around
noon, decreases in Ψ resulted in decreases in turgor pressure. On one day (February 7), the decrease in Ψ was accompanied by a transient reduction in stomatal
4
ZOTZ AND WINTER
Figure 1. Diel changes in atmospheric CO2 concentration in the crown of a Ceiba pentandra. Given are
mimima (s) and maxima (●) for each of 84 days during 1991. The CO2 concentrations were determined
at approximately hourly intervals during the day and every 3--5 h at night. The dry and wet seasons are
indicated by open and hatched bars, respectively.
Figure 2. Representative diel courses of gas exchange in situ in Ceiba pentandra in the dry (February 7,
March 8) and wet (July 7, October 17) season. Shown are photosynthetic photon flux density (PPFD),
net CO2 exchange (A), leaf (Tl) and ambient temperature (Ta), leaf to air vapor pressure difference (∆w),
stomatal conductance for water vapor (gw), and internal CO2 concentration (ci).
SEASONAL CHANGES IN PHOTOSYNTHESIS OF CEIBA
5
Figure 3. Annual course of gas exchange and water relations parameters in Ceiba pentandra. (a) Weekly
rainfall (mm), (b) daily integrated PPFD (mol m −2 day −1), (c) daily integrated net CO2 balance (mmol
CO2 m −2 day −1; open bars) and nocturnal CO2 loss (mmol CO2 m −2 night − 1; closed bars), (d) daily
integrated water use efficiency (mmol CO2 mol H2O − 1), (e) predawn water potential (s), osmotic
pressure (●) and estimated turgor pressure (connecting line), and (f) water potential (s), osmotic
pressure (●) and estimated turgor pressure (connecting line) at 1300 h.
conductance (gw) (Figure 2a), but on all other days of the dry season, gw stayed high
at about 200 mmol m −2 s −1. Highest rates of net CO2 uptake (Amax) were observed in
early March (dry season) after an unusual rainstorm with more than 170 mm of
precipitation in 36 h; Amax exceeded 18 µmol m −2 s −1 on March 8 (Figure 2) and the
resulting 24-h carbon gain was 370 mmol m −2 day −1.
Clouds and frequent rainstorms led to a significant reduction in PPFD during the
rainy season (Figure 2, July 7). The water status of the leaves changed little, but
complete turgor loss no longer occurred at noon (Figure 3). Even though environmental conditions seemed conducive to photosynthesis, the maximum rates of net
6
ZOTZ AND WINTER
Table 1. Photosynthetic and leaf characteristics of Ceiba pentandra. Gas exchange characteristics are
derived from diel measurements in situ.
Parameter
n
Mean ± SD
Leaflet size (cm2)1
W (gfw m − 2)
W (gdw m −2)
Thickness (mm)
Stomata (number mm −2)
Light compensation point (µmol m − 2 s − 1)
Mean respiration rate (µmol m −2 s −1)
Leaf N (mmol m −2)
Leaf P (mmol m −2)
Leaf K (mmol m −2)
28
28
28
13
8
13
13
14
14
14
28.8 ± 7.4
277.5 ± 22.1
124.2 ± 12.9
0.27 ± 0.02
180 ± 21
21.2 ± 5.5
0.43 ± 0.21
143 ± 14.2
4.5 ± 6.4
35.8 ± 7.7
1
Leaves consist of 6--8 leaflets.
CO2 uptake (8 to 11.8 µmol m −2 s −1 ) were much lower than in the dry season
(Figure 2) and consequently, the 24-h carbon budgets were also lower (Figure 3). The
differences in diel carbon gain between the dry and wet season were significant even
when the two days in March after the unusual rainstorm were excluded from the
analysis (t-test, P < 0.05).
Integration of CO2 gain and transpirational water loss over the entire study period
yielded 2640 g CO2 m −2 year −1 and 409 kg H2O m −2 year −1, and the long-term water
use efficiency was 6.5 g CO2 kg −1 H2O.
Variability of Amax and diel carbon gain between leaves
The variation in Amax and diel carbon gain (A24h) between leaves on a given day was
small. On September 29, 1991, we studied four mature sun leaves simultaneously.
The leaves showed maximum rates of CO2 uptake of 8.6 ± 0.7 µmol m −2 s −1 (mean
± SE) and diel carbon budgets of 142.5 ± 2.1 mmol m −2 day −1 (mean ± SE).
Correlations of gas exchange parameters, leaf age and leaf nitrogen content
The observed decline in Amax during the year was not caused by seasonal changes in
incident radiation. Leaves received saturating PPFD (about 500 µmol m −2 s −1) for
most of the day (Zotz and Winter 1993), and there was no correlation between
integrated PPFD and Amax (r2 = 0.03, P > 0.1, df = 12).
The maximum rate of net CO2 uptake was correlated with leaf age (r2 = 0.48, P <
0.01, df = 13). Because leaf nitrogen concentrations and contents also decreased with
leaf age, changes in Amax were closely related to changes in leaf N (r2 = 0.77, P <
0.001 weight-based; r2 = 0.31, P < 0.05 area-based; Figure 4). Net CO2 uptake and
stomatal conductance were closely correlated throughout the study period. During
individual days, changes in A paralleled changes in gw, i.e., the internal CO2 partial
pressure (ci) remained almost constant (Figure 2). Over the entire leaf life span, the
relationship between Amax and gw at Amax (gw,Amax) did not change (r2 = 0.88, P <
SEASONAL CHANGES IN PHOTOSYNTHESIS OF CEIBA
7
Figure 4. Correlations of leaf nitrogen concentration (a) and leaf nitrogen content (b) with maximum rate
of CO2 uptake (Amax) in leaves of Ceiba pentandra on 14 days from February through October 1991.
Both regression lines are significant (P < 0.05).
0.001; Figure 5).
The maximum rate of net CO2 uptake was strongly correlated with diel carbon gain
(A24h) (r2 = 0.85, P < 0.001, see Zotz and Winter 1993). Consequently, our analysis
for Amax was also valid for A24h.
Changes in stomatal conductance with increasing leaf age
Young leaves (one month old) showed maximum stomatal conductances of 600
mmol m −2 s −1 (Figure 6a). Increasing ∆w from 4.9 to 17.2 mPa Pa −1 led to a gradual
reduction in gw, whereas transpiration rates increased from 2.3 to 5 mmol m −2 s −1.
Figure 5. Correlation of maximum rate of CO2 uptake (Amax) and stomatal conductance at Amax (gw,Amax).
Data are derived from 13 complete diel courses and one incomplete course of net CO2 exchange.
8
ZOTZ AND WINTER
Figure 6. Response of stomatal conductance (gw) and transpiration (E) to leaf--air water vapor pressure
difference (∆w). Measurements were performed in situ on one-month-old (a), four-month-old (b) and
ten-month-old (c, d, e) leaves of Ceiba pentandra. Data are means ± SD. The number of leaves studied
was 5 (a), 7 (b), 5 (c), 7 (d) and 4 (e).
Three months later, the stomatal response to changing ∆w was similar, although gw
was slightly lower at higher values of ∆w (Figure 6b). A few weeks before leaf
abscission (ten-month-old leaves), three different patterns of stomatal response were
observed. The stomatal response of one group of leaves was similar to that of younger
leaves, but at the higher values of ∆w, gw was consistently lower by about 100 mmol
m −2 s −1 (Figure 6c). A second group of leaves exhibited large reductions in gw (Figure
6d). Even at the lowest ∆w of 5.0 mPa Pa −1, gw reached only 300 mmol m −2 s −1. In
a third group of leaves, gw increased with increasing ∆w up to 12 mPa Pa −1 and
SEASONAL CHANGES IN PHOTOSYNTHESIS OF CEIBA
9
decreased at higher values of ∆w (Figure 6e).
Discussion
It is generally assumed that plants in a seasonal tropical climate suffer a large
reduction in net CO2 uptake, growth and survival during times of drought (Lugo et
al. 1978, Medina and Klinge 1983, Landsberg 1984, Reich and Borchert 1984,
Robichaux et al. 1984). Many trees on Barro Colorado Island are drought-deciduous,
and thus avoid the potentially stressful dry season (Croat 1978). Ceibapentandra, however, develops a new set of leaves at the beginning of the dry season (Croat 1978, D.
Windsor, unpublished data). This phenological pattern suggests that the species has
ready access to deep soil water. However, no information is available about the root
system of C. pentandra. We also do not know the extent to which stored water in the
large trunk is, at least for short periods, important in maintaining transpiration of the
leaves. However, consistent with the notion of uninterrupted water supply throughout
the year, we found high values of gw, A and Ψpr during the dry season. Nevertheless,
the water supply was not sufficient to support maximum photosynthetic CO2 uptake,
because we observed a large increase in Amax immediately after an unusual rainstorm
in the dry season (March 1991 in Figures 2 and 3). Diel carbon gain was significantly
higher in the dry season.
We conclude that, in C. pentandra, ontogenetic developments influence Amax and
A24h more than seasonal changes in water availability and climatic conditions. The
maximum rate of net CO2 uptake decreased linearly with leaf age and was positively
correlated with leaf N content. Photosynthetic capacity and leaf N are strongly
correlated in many plant species (Field and Mooney 1986, Evans 1989, Reich et al.
1991). The strong correlation between Amax and gw,Amax (Figure 5) suggests that the
age-related changes in Amax are caused by a reduction in photosynthetic capacity.
Such a correlation is in accordance with models of optimal stomatal regulation
(Cowan and Farquhar 1977, Cowan 1982, Schulze and Hall 1982). A gradual
decrease in gw with leaf age was also observed in a study of the ∆w response as a
function of leaf age (Figure 6). The loss of stomatal responsiveness in at least some
leaves a few days before abscission is consistent with previous observations on other
tropical tree species (Borchert 1979). The differences in conductance patterns in
Ceiba leaves of similar age (Figures 6c--e) might be related to slight asynchrony in
senescence. It is not known whether the loss of stomatal control, as indicated in
Figure 6e, is causally related with leaf shedding, e.g., by producing large tissue water
deficits.
Long-term carbon gain and water-use efficiency can only be compared with
temperate-zone tree species, because no equivalent data are available for other
tropical trees. Surprisingly, the long-term water-use efficiency of C. pentandra (6.5 ×
10 −3 g CO2 g −1 H2O) was low compared to some temperate tree species, e.g., Fagus
sylvatica L. (8.2 × 10 −3 g CO2 g −1 H2O, Schulze 1970) and Acer campestre L. (17.1 ×
10 −3 g CO2 g −1 H2O, Küppers 1984). The annual leaf carbon gain, however, was
10
ZOTZ AND WINTER
higher (2640 g CO2 m −2 year −1 or 21 g CO2 gDW−1 year −1) compared with 8 to 13 g
CO2 gDW−1 year −1 for F. sylvatica (Schulze 1970, Künstle and Mitscherlich 1977),
14 g CO2 gDW−1 year −1 for Betula verrucosa Ehrh. (Künstle and Mitscherlich 1977)
and 15 g CO2 gDW−1 year −1 for the pioneer tree, A. campestre (Küppers 1984). Our
estimate is comparable with that of Okali (1971) for C. pentandra seedlings which
gained 54 to 60 gDW m −2 week −1 (= 8.6 gDW m −2 day −1) under optimal conditions.
This corresponds to 16 g CO2 m −2 day −1 (= 370 mmol CO2 m −2 day −1) based on a
factor of 1.88 for the conversion of dry weight to CO2 (Penning de Vries 1975), which
matches the highest 24-h carbon gain observed in this study.
Acknowledgments
G.Z. was on leave from Lehrstuhl Botanik II, Universität Würzburg, Germany and was supported by a
doctoral fellowship of the Deutsche Forschungsgemeinschaft (SFB 251, Universität Würzburg). The SFB
251 also provided facilities for mineral element analysis, and we are grateful to F. Reisberg and M. Lesch
for performing these measurements. We thank Miguel Piñeros for excellent field assistance and Dr. Tom
Kursar, Dr. Greg Gilbert and two anonymous reviewers for critical comments on earlier drafts of the
manuscript.
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