Tree Physiology 14, 1367--1381

© 1994 Heron Publishing----Victoria, Canada

Photosynthesis and water relations of savanna tree species

differing in leaf phenology1

ERNESTO MEDINA and MARTA FRANCISCO

Centro de Ecología, Instituto Venezolano de Investigaciones Científicas (IVIC), Apartado 21827, Cara-
cas 1020-A, Venezuela

Downloaded from http://treephys.oxfordjournals.org/ at Northern Arizona University on June 11, 2015

Received February 1, 1994

Summary
Godmania macrocarpa Hemsley, a deciduous tree characteristic of fire protected areas of the savanna
region of central Venezuela, was more drought tolerant, allocated more N to leaves and had consistently
higher photosynthetic rates than Curatella americana L., a ubiquitous species growing successfully
within the grasslands of tropical American savannas. Godmania macrocarpa maintained higher leaf
conductance and photosynthesized at higher xylem water tensions than C. americana. As the dry season
progressed, G. macrocarpa was more affected by water stress than C. americana, which may explain
why G. macrocarpa shed its leaves before forming new leaves. For both species, leaf sap osmolality was
strongly correlated with, but not completely accounted for by, soluble sugars. Integrated water-use
efficiency, as measured by δ13C, was similar for both species, but young leaves were more efficient than
old leaves. Water-use efficiency of adult leaves was similar in both species as a result of higher
photosynthetic rates in G. macrocarpa and lower leaf conductances in C. americana. Compared to
G. macrocarpa, instantaneous photosynthetic N-use efficiency was higher in C. americana despite its
lower maximum photosynthetic rates. The absence of G. macrocarpa trees from open grasslands, despite
their high productive capacity, is possibly the result of unfavorable conditions for germination, poor
survival of seedlings, and lack of resistance against fire.
Keywords: Curatella americana, Godmania macrocarpa, leaf sap osmolality, N-use efficiency, water
stress, water-use efficiency.

Introduction
The central plains of Venezuela are occupied by a complex of savannas (grassland
and isolated woody plants) and semideciduous forest patches. In the savannas, the
grass layer is frequently dominated by a species of the genus Trachypogon (Blyden-
stein 1962, Sarmiento 1984), whereas the tree layer is never continuous and consists
of a few evergreen tree species (Monasterio and Sarmiento 1976). The forest patches
are dominated by truly semi- or fully deciduous tree species (Medina 1982, Sar-
miento 1984). This vegetational complex is found under climatic conditions charac-
terized by strong rainfall seasonality, the rainy season extending from April to
September. The present distribution of savannas and forest patches appears to be
related to soil structure, water availability, and fire regime (Medina and Silva 1990).
Both climatic and edaphic conditions are important forces operating in the selec-

1 This paper is dedicated to Prof. Dr. H. Ziegler, retiring director of the Institute of Botany and
Microbiology, Munich Technical University, Germany, on the occasion of his 70th birthday.
1368 MEDINA AND FRANCISCO

tion of morphological and physiological properties of savanna vegetation. In the

neotropical savannas, woody species are generally evergreen, that is, they maintain
a permanent leaf canopy that turns over once a year during the dry season (Monas-
terio and Sarmiento 1976, Montes and Medina 1977, Medina 1982, Sarmiento et al.
1984). Leaves of evergreen trees tend to be scleromorphic (Medina 1984). In areas
protected against fire, the tree species are mostly deciduous, remaining leafless for
periods of two to five months during the dry season, and developing leaves with
relatively high leaf area/weight ratios (Medina 1984).
Coexistence of tree species with contrasting phenological behavior has been taken

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as an indication of differences in depth of the root systems. Trees capable of
exchanging their leaves during the dry season should be able to use water from deeper
soil layers, whereas deciduous species have more superficial root systems and
therefore, are strongly limited by water during the dry season (Medina 1982,
Sarmiento 1984, Goldstein et al. 1989). However, the encroachment of deciduous
species into open grasslands seems to be restricted more by fire than by nutritional
requirements or competition (Montes and Medina 1977). Long-term protection
against fire results in a marked increase in deciduous species in tropical savannas
(San José and Fariñas 1991).
In several ecosystems, deciduous species generally have higher N concentrations
per unit leaf weight (Medina 1984, Sobrado 1994) and photosynthetic rates than
evergreen species (Mooney and Gulmon 1982, Field and Mooney 1986). However,
in savanna and dry deciduous forests, photosynthetic differences are frequently small
(Goldstein et al. 1989, Sobrado 1994).
Comparative analysis of gas exchange in trees with contrasting phenological
behavior growing under the same climatic conditions enabled us to test the hypothe-
ses that water-use efficiency is higher in evergreen trees that expand their leaves and
photosynthesize during the dry season, and that N-use efficiency is higher in decidu-
ous trees that are active mostly during the rainy season.
We measured seasonal variations in water relations and photosynthesis in two
common tree species differing in distribution and phenological behavior in a savanna
in central Venezuela: Curatella americana L. (evergreen) and Godmania macro-
carpa Hemsley (deciduous).

Materials and methods

Habitat and plant material

The study site is located at 125 m above sea level within a Trachypogon-savanna area
in Cojedes state, Venezuela (9°25′ N and 60°15′ W). It is characterized by a grass
cover dominated by Trachypogon plumosus and Thrasya petrosa, and a tree layer
consisting of evergreen species scattered within the grass layer (C. americana,
Bowdichia virgilioides, Byrsonima crassifolia and Casearia sylvestris) and decidu-
ous species mostly restricted to small tree groves or areas protected against fire
(G. macrocarpa, Cochlospermum vitifolium, Genipa caruto) (Blydenstein 1962,
SAVANNA TREE PHOTOSYNTHESIS AND WATER RELATIONS 1369

Bilbao 1988).
Rainfall is seasonal. Of an average 1100 mm per year, nearly 90% falls during the
period from May to October. Rainfall between November and April is not enough to
compensate for potential evapotranspiration. Measurements were performed at the
end of the rainy season 1988, during the dry season 1988--89 and during the rainy
season 1989 (Figure 1). The rainy season 1988 extended until the end of the year.
Curatella americana trees reach up to 5--8 m in height and have sclerophyllous,
highly undulated leaves. Leaf duration averages 12 months, and leaf exchange takes

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place within one month near the middle of the dry season (Monasterio and Sarmiento
1976, Montes and Medina 1977). During the period of leaf exchange, two leaf
cohorts are present on the same tree, one about 12 months old, developed during the
previous dry season (adult leaves + old leaves), and the new leaves being developed
in the current dry season (young leaves). Young and adult leaves could be sampled
throughout the measuring period because of slight asynchrony in leaf exchange
among trees. In the field, leaves were collected and separated according to their
apparent age, as judged by color and texture.
Godmania macrocarpa trees reach up to 5 m tall and are drought deciduous, with
compound mesophytic leaves of soft texture and dark green color. Leaves are
produced at the beginning of the rainy season in May and last until the middle of the
next dry season, with an average leaf life span of eight months. At each collection
time, leaves were of similar age, because there was no overlap between previous and
current growing seasons.

Figure 1. Annual distribution of rainfall in the study site, Sembra, Edo. Cojedes. Rainfall collector was
located about 2 km south of the study site. The short arrows indicate the measurements periods.
1370 MEDINA AND FRANCISCO

Field measurements
Monthly measurements of gas exchange (portable ADC gas analyzer, Model LCA2),
xylem water tension (Soil Moisture Equipment pressure chamber, Model 3000), and
leaf sampling for measurement of osmolality, soluble cations and carbohydrate
contents, leaf area/weight ratios, and total nitrogen (N) and chlorophyll contents,
were carried out from the end of the rainy season (November) until the middle of the
next rainy season (August).
Xylem water tension and gas exchange measurements were routinely conducted

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from sunrise at 0630 h to shortly after noon (1300--1400 h) to assess daily changes
in leaf water status (minimum and maximum water tensions) and the relationship
between stomatal conductance and photosynthesis. Leaf disks from the same leaves
used for measurements, or from separate sets of leaves, were collected in paper bags
for measurement of N content, or in plastic syringes and frozen in dry ice for
extraction of leaf sap.

Laboratory measurements
Methods for leaf sap extraction and measurement of soluble compounds have been
described elsewhere (Olivares and Medina 1992). Briefly, frozen leaf disks of 3-cm
diameter (three replicates) were thawed in the laboratory, and their sap extracted with
a hand press. A subsample was taken immediately for measurement of osmolality
with a Wescor 5500XR osmometer. Osmolality values (Os in mmol kg −1) were
transformed to pressure units at 25 °C based on a regression derived from tables in
Lang (1967) for NaCl: osmotic pressure (MPa at 25 °C) = 0.029521 + 2.17490 Os +
0.065058 Os2. Concentrations of potassium in the cell sap were measured by atomic
absorption spectrometry (Varian AA-6) after appropriate dilution. Soluble carbohy-
drates were measured by the procedure of Hassid and Neufeld (1964). Nitrogen
content was measured in oven-dried leaf samples by a Kjeldahl procedure (Jackson
1964). Leaf chlorophyll content was measured in leaf disks frozen in the field and
extracted in the laboratory with 80% acetone (Arnon 1949).
In a subset of the leaf samples used for N determinations, the natural abundance of
13
C (δ13C values) was also measured to obtain an index of integrated water-use
efficiency. Samples were analyzed by Susan Wood in the Research School of
Biological Sciences, Australian National University, following standard procedures
(Farquhar et al. 1989).

Results

Leaf area/weight ratios, and the contents of nitrogen and chlorophyll

Leaf area/weight ratios (LAW m2 kg −1) and leaf N per unit area (LNA mmol m −2)
decreased with leaf age. Young leaves of both species had higher values of LAW and
LNA than old leaves. The bulk of samples collected from C. americana showed a
relatively narrow distribution of LAW and LNA values, whereas the spread was more
SAVANNA TREE PHOTOSYNTHESIS AND WATER RELATIONS 1371

pronounced in G. macrocarpa (Table 1). The average of all samples indicated that G.
macrocarpa had significantly lower values of LAW and higher values of LNA than
C. americana. Chlorophyll content and the molar ratio of chlorophyll/N were twice
as high in G. macrocarpa as in C. americana.

Leaf xylem water tension and osmolality of leaf sap

During the end of the rainy season, minimum leaf xylem water tensions remained
around 0.4 MPa in G. macrocarpa and 0.1--0.4 MPa in C. americana, indicating

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sufficient water supply (Figure 2). Minimum values increased markedly as the dry
season progressed, reaching nearly 1.2 MPa in G. macrocarpa and 0.6--0.8 MPa in
C. americana. A similar trend was observed in the maximum xylem water tensions
(Figure 2). The daily fluctuations in xylem water tension were always higher in
G. macrocarpa, varying from 0.50 MPa in young leaves to 1.88 MPa in adult leaves,
compared to the variations from 0.19 to 0.53 MPa in young leaves and from 0.43 to
0.87 MPa in adult leaves of C. americana. Daily fluctuations of leaf sap osmolality
followed the same pattern. Godmania macrocarpa showed fluctuations from 86
mmol kg −1 (≈ 0.19 MPa) in young leaves to 297 mmol kg −1 (≈ 0.68 MPa) in old
leaves, whereas in C. americana, young leaves varied from 23 to 62 mmol kg −1 (≈
0.05--0.14 MPa) and adult leaves from 37 to 125 mmol kg −1 (≈ 0.08--0.30 MPa).
Maximum leaf xylem water tensions were similar to, or slightly larger than, the
maximum osmotic pressures calculated from sap osmolalities. Leaf dehydration, as
measured by the morning--noon increases in leaf-sap osmotic pressure, was less
pronounced in C. americana, particularly the young leaves, than in G. macrocarpa.
After the onset of the dry season, both species experienced water stress, but it was
less pronounced in C. americana than in G. macrocarpa (cf. differences in scale in
Figure 2).
The maximum leaf osmotic pressures measured throughout the seasons were
positively correlated with the maximum xylem water tensions measured in the same

Table 1. Average and 95% confidence intervals of leaf area/weight ratios, leaf nitrogen content and
chlorophyll content of Curatella americana and Godmania macrocarpa leaves in the Trachypogon-sa-
vannas of Cojedes state. Within rows, values followed by the same letter are not statistically different
(Fisher’s least significant difference at P ≥ 0.95).

Variable Curatella americana Godmania macrocarpa

n Min Average Max n Min Average Max
Leaf area/weight 112 9.4 9.9a 10.4 40 7.4 8.3b 9.1
(m2 kg −1)
Nitrogen content 109 42 114a 207 40 111 203b 401
(mmol m − 2)
Chlorophyll content 18 210 262a 313 4 475 628b 780
(µmol m − 2)
Chlorophyll/nitrogen 18 2.2 2.5a 2.9 4 4.8 5.3b 5.8
(mmol mol −1)
1372 MEDINA AND FRANCISCO

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Figure 2. Seasonal variations in xylem water tension (MPa) and leaf-sap osmotic pressure (MPa at
25 °C). Depicted are the minimum values from samples collected shortly after sunrise, and the maximum
values from samples collected about one hour after noon (averages ± standard deviations, n = 6).

tree (Figure 3). Average values of both leaf-sap osmotic pressure and maximum
xylem water tensions were larger throughout the measuring period in G. macrocarpa
than in C. americana.

Composition of leaf sap

Leaf sap osmolality, measured on leaves collected during early morning, was highly
correlated with the concentrations of K and soluble sugars. In G. macrocarpa, K
concentration in leaf sap was generally higher in young than in adult leaves, whereas
SAVANNA TREE PHOTOSYNTHESIS AND WATER RELATIONS 1373

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Figure 3. Relationship between maximum leaf-xylem water tension and maximum leaf-sap osmotic
pressure (averages ± standard deviations, n = 6).

the opposite was true for sugars and osmolality (Table 2). In C. americana, no
significant differences were detected between young and old leaves. The best predic-
tor of leaf sap osmolality was the concentration of soluble sugars (Figure 4), which
explained about 80% of the osmolality variance (osmolality (mmol kg −1) = 236.82
+ 4.91 soluble sugars (mol m −3), r2 = 0.81). However, soluble sugars and K accounted
for less than 25% of total osmolality, indicating that other osmolites, possibly organic
compounds, were also present.

Leaf conductance and photosynthesis

In G. macrocarpa, maximum photosynthetic rates differed greatly between the rainy

Table 2. Differences in leaf sap osmolality (mmol kg − 1), potassium and soluble sugars concentrations
(mol m − 3) in young and adult leaves of Godmania macrocarpa and Curatella americana. Within rows,
values followed by the same letter are not statistically different (Fisher’s least significant difference at
P ≥ 0.95).

Variable Godmania macrocarpa Curatella americana

Young Adult Young Adult
(n = 6) (n = 8) (n = 7) (n = 8)
Osmolality 526a 751b 357c 424c
Potassium 74a 48b 77a 84a
Soluble sugars 62a 117b 24c 37c
1374 MEDINA AND FRANCISCO

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Figure 4. Relationship between soluble sugars concentration and osmolality of leaf sap.

season and the dry season, decreasing from an average of 14 to 5.5 µmol m −2 s −1. In
C. americana, changes were less pronounced, varying from 5.5 to 9.5 µmol m −2 s −1
in young leaves and from 8.5 to 9.5 µmol m −2 s −1 in adult leaves. Leaf conductance
and photosynthesis per unit area were positively and significantly correlated in both
young and adult leaves of G. macrocarpa and in young leaves of C. americana, but
not in adult leaves of C. americana (Figure 5). Godmania macrocarpa leaves showed
consistently higher maximum photosynthetic rates per unit area than young
C. americana leaves throughout the conductance range. Therefore, the former spe-
cies maintained a lower ratio of CO2 concentration between the intercellular spaces
and the surrounding air (ci/ca ratio) during the periods of maximum photosynthesis.
Average values of intrinsic water-use efficiency (ratio of photosynthesis/conduc-
tance, IWUE) (Osmond et al. 1980), calculated from maximum photosynthetic rates,
were higher in G. macrocarpa than in C. americana (Table 3).

Photosynthesis and leaf nitrogen concentration

Maximum photosynthesis per unit leaf weight was linearly correlated with leaf N
concentration, with the exception of a few G. macrocarpa leaves with very high N
concentrations (Figure 6). The correlation was also detectable on an area basis, but
it was much weaker. Instantaneous N-use efficiency (INUE), calculated as the
average ratio of maximum photosynthesis and leaf N content, was significantly
higher in C. americana, particularly the young leaves, than in G. macrocarpa
(Table 3).
SAVANNA TREE PHOTOSYNTHESIS AND WATER RELATIONS 1375

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Figure 5. Relationships between leaf stomatal conductance and maximum rates of CO2 fixation. Each
point corresponds to a different leaf.

Table 3. Intrinsic water-use efficiency (IWUE), calculated as the average ratio of maximum photosyn-
thesis and leaf conductance, and instantaneous N-use efficiency (INUE), calculated as the average ratio
of maximum photosynthesis and leaf nitrogen concentration, both on a dry weight basis. Within columns,
values followed by the same letter are not statistically different (Fisher’s protected least significance
difference at P ≥ 0.95).

Species n IWUE INUE

(mmol mol −1) (µmol CO2 mol −1 N)
Godmania macrocarpa 22 46.0a 56.8a
Curatella americana
Young leaves 15 30.4b 71.4b
Adult leaves 22 36.0b 65.9ab

Average water-use efficiency

In both species, δ13C values tended to increase (become less negative) as the dry
season progressed, but were consistently less negative in young leaves of C. ameri-
cana (Figure 7). Values ranged from a minimum of − 29.5‰ in G. macrocarpa to
−26‰ in C. americana. In both species, δ13C values above − 27.8‰ corresponded to
young leaves, differentiated in the field according to their texture, and characterized
later by LAW and N concentration. Young leaves of C. americana also had a
significantly higher LAW than adult and old leaves, although average N concentra-
tion did not vary with leaf age (Table 4). In G. macrocarpa, young leaves were
characterized by significantly higher N concentrations than old leaves, whereas no
differences in LAW were detected.
1376 MEDINA AND FRANCISCO

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Figure 6. Relationship between maximal rates of photosynthesis of a given leaf and its nitrogen content
on a leaf weight basis.

Figure 7. Variations of δ13C values measured from the end of the rainy season 1988 to the beginning of
the rainy season 1989. Bars with standard deviation represent averages of three values.

Discussion

During the measuring period, G. macrocarpa differed from C. americana in leaf

SAVANNA TREE PHOTOSYNTHESIS AND WATER RELATIONS 1377

Table 4. Groups of young and adult + old leaves of Godmania macrocarpa and Curatella americana as
characterized by leaf area/weight ratio, nitrogen concentration and δ13C values. Within each species and
column, numbers followed by the same letter are not statistically different (Fisher’s least significant
difference at P ≥ 0.95).

Species n Leaf area/weight N Concentration δ13C Range

(m2 kg −1) (mmol kg − 1) (‰) (‰)
Godmania macrocarpa
Young 2 6.3a 2662a −27.1a 0.1
Adult + old 13 7.5a 1441b −29.2b 1.3

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Curatella americana
Young 16 11.1b 1107c −27.8a 3.1
Adult + old 18 7.8a 1028c −28.7b 2.9

phenology and properties associated with water relations and gas exchange: (1) it lost
all its leaves toward the end of the dry season, whereas C. americana produced new
leaves as the older leaves were being shed, (2) it always had higher leaf N and
chlorophyll contents than C. americana, (3) its values of leaf xylem water tension
and osmolality were considerably higher, indicating that under natural conditions,
this species tolerated much lower leaf water potentials than C. americana, and (4) its
leaves had consistently higher photosynthetic rates at similar conductances than
C. americana.
In both species, leaf sap osmolality was correlated with the maximum leaf xylem
water tension, indicating similar mechanisms of response to water stress, i.e., main-
tenance of leaf conductance at low water potential was accomplished through a
reduction in osmotic potential. In both species, soluble sugars were highly correlated
with leaf sap osmolality. Godmania macrocarpa had consistently higher concentra-
tions of soluble sugars, but not of K, than C. americana.
Osmotic pressure measured in sap extracted from frozen leaves tends to underes-
timate actual values because of dilution with cell wall water (Tyree and Jarvis 1982).
Meinzer et al. (1983) measured water relations parameters in C. americana leaves
using pressure--volume curves and reported osmotic pressure values at full turgor
ranging from 0.9 MPa in young leaves to 2.4 MPa in mature leaves to 1.3 MPa in
one-year-old leaves. Our values were similar for young and old leaves, but lower for
mature leaves. However, the range of variation of osmotic pressures between full and
zero turgor in the different leaf types was almost identical to the values of minimum
and maximum leaf-sap osmotic pressures reported here. Therefore, we believe that
extraction of leaf sap does not result in significant dilution in C. americana. In
addition, G. macrocarpa showed equal or larger diurnal variations of both leaf xylem
water tension and osmotic pressure than the evergreen trees reported by Meinzer et
al. (1983). Diurnal variations in leaf-sap osmotic pressure result from leaf tissue
dehydration and indicate that there is a delay in the transport of xylem water to cover
for transpiration losses during the day.
In agreement with the high osmolality and N content, G. macrocarpa showed
1378 MEDINA AND FRANCISCO

consistently higher leaf conductances and photosynthetic rates than C. americana.

Photosynthesis and leaf conductance were linearly correlated in G. macrocarpa and
young leaves of C. americana, the former having higher maximum values of IWUE.
No relationship between photosynthesis and leaf conductance was detected in old
leaves of C. americana, because they lacked stomatal control. The cause for the loss
of stomatal control in C. americana is probably the large accumulation of silica in
the epidermis, leading to guard cell rigidity (Rodríguez 1979). This phenomenon has
been observed in several tropical tree species (Reich and Borchert 1988).
Photosynthetic rate was linearly correlated with N content, but maximum, instan-

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taneous N-use efficiency in photosynthesis was lower in G. macrocarpa than in
C americana. A linear relationship between total leaf N and photosynthetic rates has
been reported for numerous species (Field and Mooney 1986). The large variations
observed among species may be due to differences in the fraction of leaf N allocated
to RuBP carboxylase and the accumulation of nitrogen compounds not associated
with the operation of the photosynthetic machinery (Evans 1989). We found a
contrasting pattern of intrinsic water-use efficiency and N-use efficiency. High
photosynthetic rates were attained by allocating large amounts of N to the leaves and
tolerating low water potentials. This combination led to higher maximum IWUE and
lower INUE in G. macrocarpa than in C. americana. A similar pattern of behavior
was reported by Field et al. (1983) for woody evergreen species of the Californian
chaparral.
The average values of INUE reported here are lower than those reported for
herbaceous plants (Seeman et al. 1987, Evans 1989), but generally larger than those
reported for trees from Miombo and Mopane woodlands in Zimbabwe (Tuohy et al.
1991). Comparisons of INUE values from deciduous and evergreen trees of a dry
deciduous forest with our results reveal differences in the behavior of evergreens with
and without water stress during the dry season. In contrast to the species studied here,
evergreen species of dry tropical forests frequently have higher N and chlorophyll
contents per unit leaf area, and lower photosynthetic rates than deciduous species
(Medina 1984, Sobrado 1994). However, the chlorophyll/N ratio is higher in decidu-
ous species than in evergreen species in both dry forest and savanna species (Sobrado
1994 and Table 1). In dry deciduous forests, lack of water during the dry season limits
photosynthetic productivity, and maintenance of leaf area through the dry season is
associated with large water deficits (Sobrado 1986) and possibly with the accumula-
tion of herbivore deterrents (Mooney and Gulmon 1982). In savanna evergreens,
water deficits during the dry season are less pronounced than in dry deciduous forests
(Meinzer et al. 1983), and photosynthetic productivity seems to be limited by N
allocation to leaves.
Average water-use efficiency, as measured by the abundance of 13C, indicated that
young leaves of both species were more efficient than old leaves. Similarity of
average water-use efficiency in both species probably resulted from higher photosyn-
thetic capacity in G. macrocarpa and lower leaf conductances in C. americana.
Goldstein et al. (1989) compared the water-use efficiency of several deciduous and
SAVANNA TREE PHOTOSYNTHESIS AND WATER RELATIONS 1379

evergreen species of savannas in Venezuela and found only minor differences for the
species taken as a group. However, C. americana had higher assimilation/transpira-
tion ratios, but more negative δ13C values, than G. macrocarpa. Differences between
our results and those of Goldstein et al. (1989) might derive from timing of collection
and age of leaves used to measure natural abundance of 13C, because their values are
within the range of variation reported in this paper.
During the sampling period, δ13C values increased markedly toward the dry
season, indicating variations in the carbon source used to build the leaves (Figure 7).
These seasonal variations in δ13C values of leaves have been related to water stress

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(Mooney et al. 1989) and the development of leaves from stored carbon with higher
δ13C values (Ehleringer et al. 1992) in other vegetation types. In a dry deciduous
forest, leaves of trees that remain green during the wet season have significantly more
negative δ13C values than those of trees producing leaves early in the dry season
(Mooney et al. 1989). Moreover, both deciduous and evergreen trees have more
negative δ13C values in sites with high water availability than in drought-prone sites.
We hypothesize that, if carbohydrates stored at the end of the rainy season are richer
in 13C because of higher water-use efficiency during this period, the new leaves
formed in the middle (C. americana) or at the end of the following dry season
(G. macrocarpa) will show more positive δ13C values. As leaves grow into the next
rainy season, δ13C values decrease as a result of the accumulation of carbohydrates
progressively impoverished in 13C.
In summary, our results indicate that, compared with C. americana, G. macro-
carpa is a more productive species, with higher intrinsic water-use efficiency during
periods of unrestricted water availability, and is able to withstand water stress well
into the dry season without losing turgor. In contrast to the behavior of deciduous
species in tropical dry forests, the INUE and long-term water-use efficiency of G.
macrocarpa are lower than those of C. americana. However, these differences are
not enough to explain the absence of G. macrocarpa in open grasslands. Possible
explanations are the differences in germination requirements and higher nutritional
demands of deciduous species. Godmania macrocarpa produces numerous short-
lived seeds with small amounts of reserves, which reduces the probability of the
seedlings surviving in open grasslands. Curatella americana seeds, in contrast, are
long-lived and may remain buried in the soil until humidity conditions are enough to
guarantee successful establishment (Blydenstein 1962, Medina and Silva 1990).
Montes and Medina (1977) explored the nutritional restriction for establishment of
deciduous trees in open grasslands and concluded that fire is the determining factor
eliminating deciduous trees from central Venezuelan savannas. Long-term observa-
tions on the changes in tree frequency and density in savannas protected against fire
in central Venezuela show that the number of isolated trees in open grasslands
increased by a factor of 100 after 25 years of protection (San José and Fariñas 1991).
Both C. americana and G. macrocarpa benefit from fire protection; however,
G. macrocarpa was recorded in the open grassland only after 15 years without fire.
We have shown that C. americana trees allocate relatively small amounts of N to their
1380 MEDINA AND FRANCISCO

leaves, and this changes little with leaf age. This character might be significant for N
conservation in a tree regularly suffering the effects of canopy burning.

Acknowledgments
To Sabas Pérez-Estévez for his reliable contribution to the field work. To three reviewers of Tree
Physiology for their technical criticisms and suggestions that significantly improved the original version
of this paper.

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