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-demand-ing 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
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),
oper-ating 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 calcu-lated 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
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
charac-terized 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)
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.
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 environ-mental conditions seemed conducive to photosynthesis, the maximum rates of net
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
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 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).
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
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). Ceiba pentandra,
how-ever, 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 ×
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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