Tree Physiology 26, 643–656
© 2006 Heron Publishing—Victoria, Canada
Contrasting seasonal leaf habits of canopy trees between tropical
dry-deciduous and evergreen forests in Thailand
ATSUSHI ISHIDA,1,2 SAPIT DILOKSUMPUN,3 PHANUMARD LADPALA,3 DURIYA
STAPORN,3 SAMREONG PANUTHAI,3 MINORU GAMO,4 KENICHI YAZAKI,1 MORIYOSHI
ISHIZUKA1 and LADAWAN PUANGCHIT 5
1
Department of Plant Ecology, Forestry and Forest Products Research Institute (FFPRI), Tsukuba, Ibaraki 305-8687, Japan
2
Corresponding author ([email protected])
3
National Park, Wildlife and Plant Conservation Department, Chatuchak, Bangkok 10900, Thailand
4
National Institute of Advanced Industrial Science and Technology (AIST), Tsukuba, Ibaraki 305-8569, Japan
5
Faculty of Forestry, Kasetsart University, P.O. Box 1054, Bangkok 10900, Thailand
Received April 5, 2005; accepted July 28, 2005; published online February 1, 2006
Summary We compared differences in leaf properties, leaf
gas exchange and photochemical properties between droughtdeciduous and evergreen trees in tropical dry forests, where
soil nutrients differed but rainfall was similar. Three canopy
trees (Shorea siamensis Miq., Xylia xylocarpa (Roxb.) W.
Theob. and Vitex peduncularis Wall. ex Schauer) in a droughtdeciduous forest and a canopy tree (Hopea ferrea Lanessan) in
an evergreen forest were selected. Soil nutrient availability is
lower in the evergreen forest than in the deciduous forest. Compared with the evergreen tree, the deciduous trees had shorter
leaf life spans, lower leaf masses per area, higher leaf massbased nitrogen (N) contents, higher leaf mass-based photosynthetic rates (mass-based Pn ), higher leaf N-based Pn, higher
daily maximum stomatal conductance (gs ) and wider conduits
in wood xylem. Mass-based Pn decreased from the wet to the
dry season for all species. Following onset of the dry season,
daily maximum gs and sensitivity of gs to leaf-to-air vapor pressure deficit remained relatively unchanged in the deciduous
trees, whereas both properties decreased in the evergreen tree
during the dry season. Photochemical capacity and non-photochemical quenching (NPQ) of photosystem II (PSII) also remained relatively unchanged in the deciduous trees even after
the onset of the dry season. In contrast, photochemical capacity
decreased and NPQ increased in the evergreen tree during the
dry season, indicating that the leaves coped with prolonged
drought by down-regulating PSII. Thus, the drought-avoidant
deciduous species were characterized by high N allocation for
leaf carbon assimilation, high water use and photoinhibition
avoidance, whereas the drought-tolerant evergreen was characterized by low N allocation for leaf carbon assimilation, conservative water use and photoinhibition tolerance.
Keywords: chlorophyll fluorescence, dry season, leaf mass per
area, photosynthesis, stomatal response, strategy, tropical
monsoon forest, xylem vessel.
Introduction
Tropical dry forests grow in regions where annual rainfall
ranges from 250 to 2000 mm and there is a distinct dry season
of 2–6 months (Murphy and Lugo 1986). The annual rainfall
gradient can be a factor determining forest types. As annual
rainfall decreases, the percentage of deciduous woody components within neotropical dry forests increases (Medina 1995)
and mean leaf thickness among the component species decreases (Santiago et al. 2004). Tropical dry forests in Thailand
and adjacent parts of southeast Asia exhibit different structures from neotropical dry forests. Dry evergreen forests with
1200–1500 mm of annual rainfall are found in southeast Asia
and drought-deciduous forests are found in areas with up to
2300 mm of annual rainfall (Rundel and Boonpragob 1995).
Most of Thailand is classified, according to the Köppen system, as a tropical monsoon climate, with high total rainfall and
a distinct dry season. Mean annual rainfall in Thailand as a
whole is about 1550 mm.
Many of the regional differences in forest types in southeast
Asia can be attributed to the amount of available nutrients in
soils. In Thailand, soils of drought-deciduous forests are relatively rich in nutrients compared with soils of evergreen forests (Rundel and Boonpragob 1995, Sakurai et al. 1998). High
soil nutrient availability favors trees with a deciduous-leaf
habit, whereas low soil nutrient availability favors trees with
an evergreen-leaf habit (Chapin 1980, Chabot and Hicks 1982,
Aerts 1995). Tree species in nutrient-poor habitats with high
leaf mass per area (LMA) have leaves with longer life spans
and lower mass-based photosynthetic capacity than tree species in nutrient-rich habitats with low LMA (cf., Kloeppel et
al. 2000, Wright et al. 2002, Prior et al. 2003). Such soil-related habitat specialization in relation to available soil nutrients has also been found in tropical dry forests in Ghana
(Swaine 1996, Baker et al. 2003) and in rain forests in Borneo
(Kitayama et al. 2004, Palmiotto et al. 2004, Lawrence et al.
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ISHIDA ET AL.
2005, Russo et al. 2005, Paoli et al. 2006). However, because
forest fires frequently occur in drought-deciduous forests in
the dry season, other factors, such as frequency of fires, soil
water potential, and historical human activity most likely affect the origin and maintenance of natural forests in Thailand.
In the dry season, drought-deciduous trees drop all of their
canopy leaves and thus, are phenologically drought avoiding.
Evergreen trees maintain their canopy leaves throughout the
dry season and thus, are classified as drought tolerant. Comparative studies between coexisting evergreen and deciduous
trees in nitrogen use, water use and photosynthesis in neotropical (Sobrado 1986, 1991, 1993, 1997, Martin et al. 1994), Australian (Eamus et al. 1999), and Mediterranean (Mediavilla
and Escudero 2003b) dry forests or savannas have shown that
evergreen trees use water more conservatively (i.e., have lower
hydraulic conductivity and lower stomatal conductance) than
drought-deciduous trees, even in the wet season, but it is not
known if evergreen and deciduous trees of the tropical dry forests in southeast Asia respond to seasonality of precipitation in
the same way.
It is generally assumed that photoprotective processes are
essential to avoiding chronic photoinhibition during prolonged drought, especially in tropical evergreen leaves, because
reduced stomatal conductance and the resulting low photosynthetic rates cause leaves to absorb more light-energy than they
can productively use (Lovelock and Winter 1996, Ishida et al.
1999a, Martínez-Ferri et al. 2000); however, comparisons of
photoprotective processes between deciduous and evergreen
trees in tropical dry forests are rare.
We have made a comparative ecophysiological study of evergreen and drought-deciduous forests in Thailand to help elucidate the interactive effects between soil nutrient availability
and seasonality in precipitation on trees in these tropical dry
forests (Rundel and Boonpragob 1995). Specifically, we compared nitrogen use, water use and photoprotection in canopy
trees of evergreen and deciduous forests in Thailand, where
the annual total and seasonal patterns of rainfall are relatively
similar but soil nutrient availability is higher in the deciduous
forests than in the evergreeen forests. The hypotheses tested
were: (1) deciduous trees have higher stomatal conductances,
leaf mass-based nitrogen contents and leaf mass- and nitrogen-based photostynthetic rates than evergreens; (2) deciduous trees have a lower mass per unit leaf area and larger xylem
vessels than evergreens; and (3) the reduced stomatal conductance and photoinhibition tolerance during the dry season are
more conspicuous in evergreen leaves with a long leaf life span
than in deciduous leaves with a short leaf life span.
Materials and methods
Study sites and tree materials
We selected two study sites, a naturally drought-deciduous
forest and a naturally dry-evergreen forest, in Thailand. The
drought-deciduous forest study was conducted at the MaeKlong Watershed Research Station (14°34′ N, 98°50′ E) in
Kanchanaburi Province, about 250 km northwest of Bangkok.
Mean annual temperature is 27.5 °C and mean annual rainfall
is 1650 mm (Marod et al. 1999). Soils (Kandiustalfs) are clay
to clay loam texture derived from sediment rocks and limestone, slightly acidic (around 6.5 in pH) and relatively rich in
nutrients (about 10.2 mg kg – 1 in available phosphorus) (Ishizuka et al. 1995). The station is located at a branch of the
Khwae Noi River in western Thailand. Although evergreen
tree species are found in the valley along the river, many
drought-deciduous tree species are generally found on the
slopes of mountains at this station. The structure and tree species composition of the forests have been described by Marod
et al. (1999). A 45-m-high scaffolding tower was constructed
on a mountain slope at the study site (elevation 160 m) to access sunlit leaves of canopy trees, Shorea siamensis Miq.
(Dipterocarpaceae), Xylia xylocarpa (Roxb.) W. Theob. (Leguminosae) and Vitex peduncularis Wall. ex Schauer (Verbenaceae), at 16 m aboveground. Canopy heights were about 30 m
for the Shorea tree, 25 m for the Xylia tree and 23 m for the
Vitex tree and the corresponding trunk diameters at breast
height were about 100, 59 and 64 cm. Although the uppermost
canopy leaves of each tree were inaccessible from the tower,
we were able to access relatively sunlit leaves from each tree.
Specific gravity of dry wood is 0.80–1.08 for Shorea siamensis, 0.83–0.93 for Xylia xylocarpa and 0.52–0.93 for
Vitex peduncularis. There is little rainfall between November
and February or March and the leafless period lasts for 2–
3 months during the latter half of the dry season (January to
February or March). Flushing of new leaves starts following
the onset of rainfall in March or April. The leaf life span of
these trees is about 9–10 months.
The dry-evergreen forest study was conducted at the Sakaerat Environmental Research Station (14°29′ N, 101°55′ E)
in Nakhon Ratchasima Province, about 180 km northeast of
Bangkok. Mean annual temperature is 26.2 °C and mean annual rainfall is 1240 mm (Sakurai et al. 1998). As at the
Mae-Klong Station, there is little rainfall between November
and February or March, but there is no leafless period. The station is located on a table mountain, ranging in elevation from
650 to 250 m, at a branch of the Mekong River, which dissects
the Korat sandstone plateau. The evergreen forest is on a gentle slope facing northeast with a mean inclination of 4° in the
upper part of the hill and Hopea ferrea Lanessan (Dipterocarpaceae) is the most dominant tree species, especially in
the top canopy layer (Pitman 1996, Sakurai et al. 1998). The
soils (Tropustults) in the Hopea forest are predominantly shallow (< 60 cm) stony Ultisols and are sandy loams derived from
sandstone parent material (Pitman 1996). The soils are acidic
(around 4.5 in pH), with low cation exchange capacities and
low availability of nutrients, especially phosphorus (about
5.3 mg kg– 1) (Rundel and Boonpragob 1995). A naturally deciduous forest is also found at the lower part of the hill where
the soil nutrients are relatively abundant (Rundel and Boonpragob 1995, Sakurai et al. 1998). A 47-m-high scaffolding
tower was constructed in the evergreen Hopea forest (elev.
535 m at the ground) as a part of a 1960s US Army Tropical
Environmental Data experiment to collect meteorological data
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(cf. Pitman 1996). We used the tower to access the uppermost
canopy leaves of a Hopea tree, with a canopy height of 33 m
and a trunk diameter at breast height of 53 cm. In H. ferrea,
leaf life span is about 2 years and the specific gravity of dry
wood is 0.96–1.05.
Measurements of microclimate
Photosynthetic photon flux (PPF) was measured with quantum sensors (ML-020P, EKO Instruments, Tokyo, Japan) and
precipitation was measured with tipping bucket rain gauges
(B-011, Yokokawa, Tokyo, Japan, at the Mae-Klong Station;
TE525, Campbell Scientific, Logan, UT, at the Sakaerat Station) at the tops of the towers. Ambient air temperature and relative humidity were measured with platinum resistance thermometers and thin-film capacitance sensors (HMP45A, Vaisala, Helsinki, Finland) at the tops of the towers. These micrometeorological data were stored at 15 min intervals in data
loggers (CR10X, Campbell Scientific) from January 2003 to
March 2004.
Measurements of leaf gas exchange and chlorophyll
fluorescence
We measured diurnal changes in leaf gas exchange and chlorophyll fluorescence in the sunlit leaves that were accessible
from the scaffolding towers on fine days over the growing season in April (early wet season), July (mid wet season) and December (early dry season) 2003 and February (late dry season)
2004. Because leaf fall occurred in January 2004 at the MaeKlong Station, the measurements in February 2004 were made
only on the Hopea tree at the Sakaerat Station. We measured
diurnal time courses in leaf-area-based net photosynthetic rate
(Pn; µmol m – 2 s –1) and water vapor stomatal conductance (gs;
mol m – 2 s –1) in at least seven fully expanded, sunlit leaves of
each tree at about 1-h intervals from dawn to dusk, with
an open, portable measurement system (LI-6400, LI-COR,
Lincoln, NE). Intercellular CO2 concentration in leaves (Ci )
during daytime was computer-calculated with the LI-COR
LI-6400. Concentrations of H2O and CO2 in the gas stream in
the system were determined by infrared spectrophotometry.
We measured diurnal time changes in chlorophyll a fluorescence just before and after the leaf gas exchange measurements with a fluorescence meter (Mini-PAM, Walz, Effeltrich,
Germany) connected to a leaf clip holder (Model 2030-B).
Measurements of PPF on each leaf surface were made with a
micro-quantum sensor with a sensitive area of 1 mm2 attached
to the leaf clip holder. Maximum fluorescence yield (Fm ) and
dark fluorescence yield (Fo) in photosystem II (PSII) were determined just before dawn. Steady-state fluorescence (F ) and
maximal fluorescence (Fm′ ) in the light-adapted state of PSII
were measured more than twice an hour during the day, according to the procedures of Bilger et al. (1995). Measured
light and saturated light pulses were applied through a fiber-optic cable oriented 60° to the leaf surface. The angle and
the distance between the leaf and the fiber-optic cable was
manually adjusted and maintained with the leaf clip holder.
Because sunlight was the actinic light source, care was taken to
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avoid shading of the measuring area and the micro-quantum
sensor.
From the dark-time measurements made before dawn, potential maximum quantum yield of PSII (Fv /Fm = (Fm – Fo )/
Fm ) was calculated. From the daytime measurements, the effective quantum yield of PSII (∆F/Fm′ = (Fm′ – F ) /Fm′ ) was
calculated. Assuming that photosystem I and II absorb equal
amounts of light, electron transport rate (ETR) through PSII
was calculated according to Genty et al. (1989) as:
ETR = 0 .5 ∆F / Fm′ A(PPF) (at the leaf surface)
(1)
where A is absorptance of lamina for the wavelengths 400–
700 nm. To estimate A of each leaf, relative chlorophyll contents of the leaves measured for chlorophyll fluorescence
were determined with a non-destructive chlorophyll meter
(SPAD-502, Minoluta, Tokyo, Japan). Regression lines between A were measured with a spectroradiometer (LI-COR
LI-1800C) equipped with an external integrating sphere (LICOR LI-1800-12) and the chlorophyll meter readings (R)
were constructed from sets of measurements on 15 leaves with
a wide range of leaf greening in each tree as follows (r 2 =
0.96–0.99):
A = 0.947 − 0.646 exp( −0.0620 R) for Shorea
(2)
A = 0.993 − 0.562 exp( −0.0387 R) for Xylia
(3)
A = 0.945 − 0.613 exp( −0.0544 R) for Vitex
(4)
A = 0.930 − 0.505 exp( −0.0514 R) for Hopea
(5)
Values of A in leaves used for the chlorophyll fluorescence
measurements were estimated from Equations 2–5 and R in
each leaf and ETR were then calculated from Equation 1.
We calculated the daytime fluorescence parameters: nonphotochemical quenching coefficient (NPQ = (Fm /Fm′ ) – 1)
and quantum yield of open PSII center (Fv′/Fm′ = (Fm′ –
Fo ′ )/Fm′ ), which characterizes the efficiency of excitation
energy capture by open PSII (Genty et al. 1989), where Fo′
(minimum fluorescence yield in the light-adapted state) was
calculated assuming that Fo quenching results from increases
in energy dissipation in PSII antennae, according to (Oxborough and Baker 1997)
F′0 = F0 / (( Fv / Fm ) + ( F0 / Fm′ ))
(6)
Theoretically, Fo′ is measured under weak far-red irradiance in
the absence of actinic irradiance before or after the saturation
pulse used to measure Fm′. However, because it is difficult to
accurately measure Fo′ in the field (Niinemets and Kull 2001),
Oxborough and Baker (1997) concluded that their computed
estimate of Fo′ was more accurate than a direct measurement.
Following Demmig-Adams et al. (1996), we divided the
light absorbed in PSII antennae during the daytime into three
components: the fraction used in photochemistry (P = ∆F/
Fm′ ), the fraction of thermal dissipation (D = 1 – (Fv′/Fm′ )),
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ISHIDA ET AL.
and the fraction remaining as excess energy (E = 1 – P – D)
that was not used in photochemistry or dissipated as heat.
Leaf nitrogen content and anatomy
After the diurnal measurements of leaf gas exchange and chlorophyll fluorescence, leaf disks from between the major veins
were obtained from each measured leaf, . The disks were oven
dried (70 °C, 72 h) and weighed to determine leaf mass per
projected area (LMA; kg m – 2) and specific leaf area (SLA; m2
kg –1). We then determined nitrogen contents of the leaf discs
with an N-C analyzer (Sumigraph NC-800, Sumitomo-Kagaku, Osaka, Japan).
For the anatomical studies, we collected seven sun-exposed
leaves and one wood core from the trunk of each tree at breast
height with an increment borer in July (mid wet season). Samples of leaf lamina excluding large veins were excised and
immediately fixed in formalin:acetic acid:alcohol. The leaf
pieces were post-fixed in 2% osmium tetroxide for about 1 h
before being dehydrated in an ethanol series and propylene oxide and embedded in Epoxy resin. Transverse sections (1 µm in
thickness) of leaves were cut on a rotary microtome (HM
340E, Micron, Waldorf, Germany) with a glass knife and double-stained with a solution of 1% safranin and 1% gentiana violet in water for light microscopy. Transverse sections (10 µm
in thickness) of sapwood just below the cambium were cut
with a sliding microtome (HM 400R, Micron, Walldorf, Germany) and double-stained with an aqueous solution of 1%
safranin and 1% gentiana violet. We measured the area of each
xylem vessel and the anatomical properties of leaf tissue on
images of the sapwood and leaf transverse sections taken with
a digital camera (Coolpix 995, Nikon, Tokyo, Japan) attached
to a microscope.
Statistical analysis
Statistical analyses were conducted with StatView software
(Version 4.5J, ABACUS Concept, USA). Comparisons of variables among species and between the wet and the dry season
were made with Scheffe’s test. Comparisons of the slopes of gs
against leaf-to-air vapor pressure deficit (VPD) and the slopes
of Pn against gs between the wet and the dry season were made
by analysis of covariance (ANCOVA). For statistical evaluation of between season differences among the variables, the
dry season (December 2003 and February 2004) was distinguished from the wet season (April and July 2003) based on a
monthly precipitation of less than 50 mm.
Results
Microclimate
Annual rainfall in 2003 was 1708 mm in the deciduous forest
and 1731 mm in the evergreen forest. During the study period,
a distinct dry season extended from November to February
(Figure 1). Mean annual air temperatures in 2003 were 24.7 °C
in the drought-deciduous forest and 24.1 °C in the evergreen
forest. In 2003, the highest and lowest air temperatures, recorded in April and December, respectively, were 36.3 and
13.4 °C in the deciduous forest and 33.6 and 11.0 °C in the evergreen forest. Because air temperature was relatively low and
air relative humidity was relatively high in the daytime in the
dry season, mean daily maximum air VPD in the dry season
was relatively low compared with that in the wet season. The
dry season at the study sites was thus relatively cool.
Figure 1. Seasonal changes in
microclimate; (A, B) monthly
rainfall (bars) and daily
photosynthetic photon flux
(PPF; 䊏); (C, D) monthly
means of daily maximum (䊐),
daily mean (䊉), and daily minimum (䉭) temperatures in ambient air; and (E, F) monthly
means of daily maximum vapor pressure deficit (VPD; 䊉)
and daily minimum relative
humidity (RH; 䊐) in ambient
air, in the drought-deciduous
(A, C, E and G) and evergreen
forests (B, D, F and H). Error
bars = 1 SD.
TREE PHYSIOLOGY VOLUME 26, 2006
ECOPHYSIOLOGY OF DRY-DECIDUOUS AND EVERGREEN LEAVES
Morphology and anatomy
Anatomical properties of leaves and sapwood xylem differed
among the tree species (Figures 2 and 3). Lamina thickness
was largest for Xylia and least for Vitex (Table 1). Mesophyll
thickness was least for Vitex but did not differ significantly between the other species. Compared with the deciduous species,
leaves of the evergreen Hopea tree were denser and had a
lower lamina porosity (internal air space). Cells of the spongy
mesophyll of Hopea leaves were relatively long and vertically
arranged like palisade tissue. Mean diameters of individual
vessels in the xylem were significantly smaller in the evergreen Hopea tree than in the deciduous trees.
Among species, Hopea leaves had the greatest LMA, but
they were not the thickest (Tables 1 and 2), reflecting the fact
that LMA is dependent on leaf porosity and cell wall thickness, as well as lamina thickness. Hopea leaves had a higher
carbon to nitrogen (C/ N) ratio (probably associated with the
thick cell walls) and lower mass-based nitrogen content (massbased N) than the deciduous tree leaves, especially in the wet
season (Table 2). From the wet to the dry season, LMA and
C/ N ratio increased and mass-based N decreased for all species. Over the growing seasons, mass-based N of individual
leaves increased with increasing SLA for all species (r 2 =
0.54–0.62) (Figure 4). Among the species studied, Xylia had
647
the highest mass-based N at a given SLA, probably because it
is a nitrogen fixer (Sinsuwongwat et al. 2002).
Leaf gas exchange
Mass-based maximum net photosynthetic rate (mass-based
Pnmax ) decreased significantly from the wet to the dry season
for all species (Table 3). Although photosynthetic nitrogenuse efficiency (PNUE; nitrogen-based Pnmax ) tended to decrease in the dry season for all species, significant differences between the seasons were found only for Xylia and
Vitex. In both seasons, mean mass-based Pnmax, PNUE and
daily maximum stomatal conductance ( gsmax ) were significatly
lower for the evergreen Hopea than for the deciduous species.
and daily minimum
The patterns of seasonal variation in g max
s
Ci differed between the evergreen and the drought- deciduous
significantly despecies. In the evergreen species, mean g max
s
creased in the dry season, but mean daily minimum Ci remained unchanged during the wet and dry seasons. In contrast,
in the drought-deciduous species, mean daily minimum Ci significantly increased following the onset of the dry season, but
remained unchanged. For the pooled data in each
mean g max
s
season, mass-based Pnmax of individual leaves increased with
increasing mass-based N for each species (r 2 = 0.55–0.68)
Figure 2. Lamina cross-sections of fully expanded sunlit
leaves of the drought-deciduous trees (Shorea, Xylia and
Vitex) and the evergreen tree
(Hopea).
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ISHIDA ET AL.
Figure 3. Wood cross sections
of the drought-deciduous trees
(Shorea, Xylia and Vitex) and
the evergreen tree (Hopea).
(Figure 5), whereas area-based Pnmax was not significantly correlated to area-based N in any of the species (r 2 = 0.01–0.20;
data not shown).
Under near light-saturated conditions (PPF > 600 µmol m – 2
–1
s ), gs was inversely correlated with leaf-to-air VPD (Figure 5). Comparison of the linear regressions of gs versus
leaf-to-air VPD between the wet and the dry season (log10
transformed in x-axis, leaf-to-air when VPD < 3.5 kPa) showed that the slopes of the relationship did not change between
the seasons for Shorea and Vitex (ANCOVA, P > 0.05), but
changed significantly for Xylia; however, the seasonal difference found for Xylia was caused by the high gs observed in
only four leaves in April (early wet season), when the leaves
were still young. For Hopea, the slopes of the gs versus leaf-
to-air VPD relationship significantly decreased from the wet
to the dry season (ANCOVA, P < 0.05). Thus, the seasonal
change in the sensitivity of gs to leaf-to-air VPD was conspicuous only for Hopea. Area-based net photosynthetic rate in individual leaves increased with increasing gs for all species. For
the drought-deciduous species, comparison of the linear regressions of the Pn versus gs relationship between the wet and
dry seasons (for gs < 0.15 mol m – 2 s – 1, when the linear correlations were relatively close) showed that Pn at a given gs
decreased significantly from the wet to the dry season
(ANCOVA, P < 0.01), indicating that daytime Ci increased in
the dry season, as shown in Table 3. In contrast, the relationships between Pn and gs for the evergreen species did not differ
between the seasons (ANCOVA, P > 0.05), indicating that
Table 1. Mean values (1 SD in parentheses) in anatomical properties of sunlit leaves and wood xylem of three drought-deciduous trees (Shorea,
Xylia and Vitex) and the evergreen tree (Hopea). Porosity in leaves was determined as the ratio of the area of air space within the leaves to the area
of mesophyll tissue without vascular tissue between epidermal cells in leaf cross sections. Significant differences (P < 0.05, Scheffe’s F-test) between species for each property are indicated by different letters.
Properties
Shorea siamensis
Xylia xylocarpa
Vitex peduncularis
Hopea ferrea
Lamina thickness (µm)
Mesophyll thickness (µm)
Porosity within lamina (%)
Area in individual conduits (mm2)
183.2 (5.2) a
141.6 (4.1) a
40.8 (4.2) ab
0.221 (0.096) a
207.0 (6.1) b
178.1 (4.8) a
45.4 (6.2) a
0.163 (0.050) b
167.7 (9.1) c
135.8 (8.2) b
33.0 (7.3) b
0.106 (0.073) c
172.1 (7.5) b
143 (6.5) a
23.6 (4.5) c
0.016 (0.007) d
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Table 2. Leaf morphological properties and nitrogen (N) concentration of the drought-deciduous trees (Shorea, Xylia and Vitex) and the evergreen
tree (Hopea). Abbreviations: LMA = leaf mass per unit area; C /N ratio = ratio of carbon to nitrogen in leaves; mass-based N = leaf mass-based nitrogen concentration; and area-based N = leaf area-based nitrogen. Bold values indicate significant differences between the wet (April and July)
and the dry (December and February) seasons in each property for each species and different lowercase and uppercase letters indicate significant
differences between species for each property in the wet and dry seasons, respectively, by the Scheffe’s F-test (P > 0.05). Data in February are for
Hopea only.
Properties
LMA (kg m – 2)
C /N ratio
Mass-based N (mol kg –1)
Area-based N (mol m – 2)
Shorea siamensis
Xylia xylocarpa
Vitex peduncularis
Hopea ferrea
Wet
Dry
Wet
Dry
Wet
Dry
Wet
Dry
0.086 a
21.8 a
1.66 a
0.142 a
0.103 A
29.0 A
1.32 A
0.135 A
0.082 a
18.0 b
2.15 b
0.177 b
0.096 AB
24.0 B
1.83 B
0.175 B
0.06 b
20.0 c
1.81 c
0.108 c
0.091 B
24.3 B
1.58 C
0.144 C
0.103 c
28.1 d
1.51 d
0.143 a
0.125 C
32.4 A
1.32 A
0.154 C
Figure 4. Relationships between specific leaf area (leaf area per unit mass)
and leaf mass-based nitrogen content
(mass-based N) for the drought-deciduous trees (Shorea, Xylia and Vitex) and
the evergreen tree (Hopea) in the wet
(April and July; 䊉) and the dry (December and February; 䊊) seasons.
Data in February are for Hopea only.
Table 3. Properties of leaf gas exchange for the drought-deciduous trees (Shorea, Xylia and Vitex) and the evergreen tree (Hopea). Abbreviations:
P nmax = daily maximum net photosynthetic ratio; N = nitrogen; gs = water vapor stomatal conductance; and Ci = leaf intercellular CO2 concentration. Bold values indicate significant differences between the wet (April and July) and the dry (December and February) seasons in each property
for each species and different lowercase and uppercase letters indicate significant differences between species for each property in the wet and dry
seasons, respectively, by the Scheffe’s F-test (P > 0.05).
Properties
max
–2
–1
Area-based Pn (µmol m s )
Mass-based Pn max (µmol kg –1 s –1)
N-based Pn max (µmol mol N –1 s –1)
Daily maximum gs (mol m – 2 s –1)
Daily minimum Ci (µmol mol –1)
Shorea siamensis
Xylia xylocarpa
Vitex peduncularis
Hopea ferrea
Wet
Dry
Wet
Dry
Wet
Dry
Wet
Dry
12.9 a
156 a
93.3 a
0.183 a
196 a
10.7 A
105 A
79.3 A
0.181 A
217 A
10.9 a
133 a
61.7 bd
0.179 a
206 a
7.6 B
80 B
43.7 B
0.156 B
260 B
8.9 b
152 a
84.2 ab
0.185 a
212 a
8.4 B
93 A
58.4 C
0.214 A
264 B
8.6 b
86 b
45.5 d
0.09 b
186 a
4.6 C
37 C
29.9 D
0.07 C
187 C
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650
ISHIDA ET AL.
Figure 5. Relationships between leaf
mass-based nitrogen content
(mass-based N) and leaf mass-based
maximum net photosynthetic rates
(mass-based P nmax ) for the drought-deciduous trees (Shorea, Xylia and Vitex)
and the evergreen tree (Hopea) in the
wet (April and July; 䊉) and the dry
(December and February; 䊊) seasons.
Data in February are for Hopea only.
daytime Ci remained unchanged during the wet and dry seasons, as shown in Table 3.
Figure 6 shows the relationships between Pn and Ci and between gs and Ci in the wet and dry seasons under near light-saturated conditions (PPF > 600 µmol m – 2 s –1). When Pn was
above about 2 µmol m – 2 s –1 and gs was higher than about
0.04 mol m – 2 s –1, Pn decreased as Ci decreased for all species.
Under these conditions, daytime Pn was mainly limited by gs
and the resulting low Ci as leaf-to-air VPD increased. In contrast, when Pn and gs were lower than these threshold values,
Pn decreased as Ci increased for all species. Under these conditions, the daytime Pn may be limited by factors other than
stomatal conductance.
chemical properties during the daytime differed between the
drought-deciduous and evergreen species (Table 4). At high irradiances (PPF > 800 µmol m – 2 s – 1) around noon, mean
Fv′/Fm′ in the drought-deciduous species either remained unchanged or increased by 16% (V. peduncularis) from the wet to
the dry season, whereas mean NPQ (thermal dissipation) remained either unchanged (S. siamensis) or decreased by 29
and 47% (in X. xylocarpa and V. peduncularis, respectively)
and D (the fraction of thermal dissipation) remained unchanged or decreased by 15% (V. peduncularis) during the transition from the wet to the dry season. In contrast, in the evergreen species, mean Fv′/Fm′ decreased 37% and mean NPQ
and D increased 21 and 22%, respectively, from the wet to the
dry season.
Chlorophyll fluorescence
Mean predawn Fv /Fm was significantly lower in the dry season
than in the wet season for Xylia, Vitex and Hopea (Table 4);
however, no evidence of chronic photoinhibition was found
during the growing seasons in any species, because predawn
Fv /Fm remained relatively high (> 0.7), even in the dry season.
At high irradiances around noon (PPF > 800 µmol m – 2 s – 1),
the mean fraction of excess-absorbed light energy (E ) either
did not change or decreased from the wet to the dry season for
all species except Shorea, where a small 7% increase in E in
the dry season was detected. Although the low photosynthetic
rates in the dry season can enhance photoinhibition, E did not
increase greatly in any species, even during the dry season.
Although the excess-absorbed energy was suppressed even
in the dry season for all species, seasonal changes in photo-
Discussion
Leaf properties and photosynthetic capacity in deciduous
and evergreen trees
Differences in leaf morphology and photosynthesis between
the drought-deciduous and evergreen tree species revealed differences in carbon assimilation and nitrogen use. Leaf properties were strongly inter-correlated (Figures 4 and 5). The
concept of a trade-off between leaf lifespan and LMA has been
extensively discussed (e.g., Reich et al 1999, Wright et al.
2002). We found that the evergreen species had a higher LMA
(denser lamina), a higher C/N ratio, a lower mass-based N,
lower mass-based Pnmax and a lower PNUE than the droughtdeciduous species, especially in the wet season (Tables 2
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651
Figure 6. Relationships between leaf-to-air vapor pressure deficit (leaf-to-air VPD)
and water vapor stomatal conductance (gs ) and relationships
between gs and net photosynthetic rate (Pn ) under near
light-saturated light conditions
(photosynthetic photon flux >
600 µmol m – 2 s – 1) for the
drought-deciduous trees
(Shorea, Xylia and Vitex) and
the evergreen tree (Hopea) in
the wet (April and July; closed
symbols) and the dry (December and February; open symbols) seasons. Data in
February are for Hopea only.
and 3). Similar patterns have been reported for many tree species with various leaf life spans in tropical dry forests (Reich et
al 1991, Medina and Francisco 1994, Kitajima et al. 1997,
Prado and de Moraes 1997, Eamus et al. 1999, Prior et al.
2003, Santiago et al. 2004).
Nutrient-poor habitats favor tree species with a high LMA
and long leaf life span (Kloeppel et al. 2000, Wright et al.
2002, Prior et al. 2003), because a long leaf life span results in
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652
ISHIDA ET AL.
prolonged nutrient retention (Escudero et al. 1992, Aerts 1995,
Ryser 1996, Ishida et al. 1999b, Mediavilla and Escudero
2003a), allowing the tree to amortize the cost of constructing
low-productivity leaves over a longer period (Chabot and
Hicks 1982, Kikuzawa et al. 1991, Sobrado 1991, Eamus and
Prichard 1998). However, structural and chemical reinforcements are necessary for leaves with a long life span to enhance
their tolerance to physical hazards and herbivores (Coley
1988, Silla and Escudero 2004). In contrast, nutrient-rich habitats favor tree species with a low LMA and a short leaf life
span. The high mass-based and N-based Pnmax in the droughtdeciduous species during the photosynthetically active period
can compensate for the absence of carbon assimilation during
the leafless period.
pit pores, rather than vessel diameter. Many systematic and
floristic observations, however, have revealed that wet-warm
environments tend to favor species with wide conduits,
whereas cold or dry environments tend to favor species with
narrow conduits (cf. Tyree et al. 1994). On the other hand,
Sobrado (1997) compared embolism vulnerability curves of
coexisting drought-deciduous and evergreen species in a neotropical dry forest and failed to show a clear-cut difference between the two groups of species. This result implies that the
occurrence of embolisms in the dry season may be influenced
by factors other than conduit width, such as root depth
(Sobrado 1997), root hydraulic conductivity (Shimizu et al.
2005) and water storage capacity in parenchyma (Borchert and
Pockman 2005).
Leaf gas exchange and water use in deciduous and evergreen
trees
Factors limiting daytime photosynthetic rate
and the leaf-to-air VPD dependThe seasonal variation in g max
s
ency of gs revealed contrasting water use between the droughtdeciduous and evergreen tree species. A trade-off between leaf
life span and hydraulic efficiency has been discussed in neotropical (Sobrado 1993, 1997) and Mediterranean (Mediavilla
and Escudero 2003b) dry forests. Sobrado (1993) showed that
drought-deciduous trees have vessels with larger diameters
than evergreen trees in the wet seaand they have higher g max
s
son and our results (Tables 1 and 3) are consistent with these
observations. Hydraulic efficiency increases with the fourth
power of vessel diameter (Hagen-Poiseuille law) and hence
the wide conduits of the drought-deciduous species will contribute to high hydraulic conductivity and g max
s . Following the
and
the
VPD
dependency
of gs reonset of the dry season, g max
s
mained relatively unchanged in the drought-deciduous species, whereas they decreased in the evergreen Hopea during
the dry season (Figure 6). This indicates that, as a result of hydraulic constraints, the evergreen Hopea is more conservative
in its water use and has a more limited photosynthetic rate than
the deciduous species. Stomatal responses to water stress are
related to the margin of safety from xylem embolism
(Brodribb et al. 2003, Nardini and Salleo 2003, Ladjal et al.
2005). Nevertheless, the drought-deciduous species maineven after the onset of the dry season (Table
tained high g max
s
3), suggesting that xylem dysfunction as a result of embolism
leads to leaf shedding (Sobrado 1996, 1997).
Xylem function (which determines water transport from
soil to leaves) may be a major determinant of leaf shedding in
tropical dry forests. The relationship between vessel diameter
and vulnerability to drought-induced xylem embolism has
been controversial (cf. Tyree et al. 1994, Oliveras et al. 2003).
When drought-deciduous species shed all their leaves in the
dry season, the tension on the water column will reach a point
where the air–water interface is pulled through the pit membranes into functional xylem vessels and the resulting air bubbles will cause cavitation in the xylem. Following the onset of
the rainy season, rehydration of embolized xylem vessels is
necessary for bud break to occur in tropical dry forest trees
(Borchert 1994, Becker 1996). The drought-induced xylem
embolism depends on the size and structure of inter-conduit
Reduced gs can limit photosynthesis by reducing the CO2 supply to chloroplasts (i.e., reduced Ci ). Brodribb et al. (2002)
found a positive correlation between leaf specific hydraulic
conductivity and photosynthetic capacity among dry tropical
tree species. The value of Ci results from the balance of gs
and photosynthetic capacity in mesophyll cells. Eamus et al.
(1999) showed interspecific variations in the seasonality of Ci
during daytime in a tropical savanna. We found that the daily
minimum Ci in the deciduous species increased following
the onset of the dry season (Table 3, Figure 7), as a result of reduced photosynthetic capacity and relatively high gs
early in the dry season; the reduced photosynthetic capacity
was probably associated with leaf aging or drought stress, or
both. In contrast, the daily minimum Ci in the evergreen species remained unchanged over the growing season. This was
probably the result of an offset between the reduced photosynthetic capacity (which effectively raised Ci ) and the reduced gs (which effectively reduced Ci) during the dry season.
In the diurnal courses of leaf gas exchange under near
light-saturated conditions (PPF > 600 µmol m – 2 s – 1), both gs
and Pn decreased with increasing leaf-to-air VPD and Ci also
decreased in all species in both seasons when gs was higher
than about 0.04 mol m – 2 s – 1 (Figures 6 and 7). These findings
indicate that leaf-to-air VPD was generally a major factor limiting daytime Pn. After the daily minimum Ci was observed,
both gs and Pn further decreased but Ci increased (when gs was
less than about 0.04 mol m – 2 s – 1), perhaps indicating that daytime Pn was being limited by other factors, such as photosynthetic activity, rather than by stomatal conductance. However, when stomatal conductance is low, non-uniform stomatal
opening sometimes occurs and can lead to an overestimation
of Ci (Terashima et al. 1988). Thus, we were unable to identify
the factor limiting daytime Pn when gs was < 0.04 mol m – 2 s – 1.
Photoprotective mechanisms in deciduous and evergreen
trees
The photochemical properties of PSII revealed that the
drought-deciduous and evergreen tree species had different
photoprotective mechanisms. Few studies have considered the
trade-off between leaf lifespan and photoprotective mechanism (Adams et al. 2004, Ain-Lhout et al. 2004). In all species,
TREE PHYSIOLOGY VOLUME 26, 2006
ECOPHYSIOLOGY OF DRY-DECIDUOUS AND EVERGREEN LEAVES
653
Figure 7. Relationships between leaf intercellular CO2
concentration (Ci ) and net
photosynthetic rate (Pn ) and
relationships between Ci and
water vapor stomatal conductance (gs ) under near light-saturated light conditions
(photosynthetic photon flux >
600 µmol m – 2 s – 1) for the
drought-deciduous trees
(Shorea, Xylia and Vitex) and
the evergreen tree (Hopea) in
the wet (April and July; closed
symbols) and the dry (December and February; open
symbols) seasons. Data in February are for Hopea only.
photosynthetic capacity decreased in the dry season (Table 3),
indicating that the risk of chronic photoinhibition increased. In
the drought-deciduous species, the photochemical capacity in
PSII (Fv′/Fm′) either remained unchanged or increased but
NPQ did not increase following the onset of dry season (Ta-
ble 4). The dissipation of excess-absorbed light energy by
photorespiration would be essential for avoiding chronic photoinhibition in the drought-deciduous species (Lovelock and
Winter 1996, Ishida et al. 1999a). By contrast, the evergreen
species exhibited down-regulation of photochemical capacity
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654
ISHIDA ET AL.
Table 4. Photochemical properties of photosystem II (PSII) for the drought-deciduous trees (Shorea, Xylia and Vitex) and the evergreen tree
(Hopea). Abbreviations: Fv /Fm = maximum quantum yield of PSII at predawn; Fv′/Fm′ = quantum yield of open PSII; NPQ = non-photochemical
quenching of PSII; ETR = electron transport rate of PSII; P (= ∆F/Fm′ ) = the fraction of photochemistry (quantum yield of PSII); D = the fraction
of thermal dissipation; and E = the fraction of excess energy. Measurements of Fv′/Fm′, NPQ, ETR, P, D and E were made under high-light conditions (PPF > 800 µmol m – 2 s –1). Bold values indicate significant differences between the wet (April and July) and the dry (December and February) seasons in each property for each species and different lowercase and uppercase letters indicate significant differences between species for
each property in the wet and dry seasons, respectively, by the Scheffe’s F-test (P > 0.05).
Properties
Fv /Fm at predawn
Fv′/Fm′
NPQ
ETR (µmol m – 2 s –1)
P
D
E
Shorea siamensis
Xylia xylocarpa
Vitex peduncularis
Hopea ferrea
Wet
Dry
Wet
Dry
Wet
Dry
Wet
Dry
0.780 a
0.550 a
2.78 a
139 a
0.262 a
0.450 a
0.288 a
0.793 A
0.536 A
2.59 A
107 A
0.225 A
0.464 A
0.311 A
0.830 b
0.518 b
3.67 b
108 b
0.191 b
0.482 a
0.327 b
0.772 B
0.503 A
2.62 A
103 A
0.212 A
0.497 A
0.290 AB
0.817 b
0.460 c
4.33 c
75 c
0.163 c
0.540 c
0.297 a
0.792 A
0.546 A
2.29 A
114 A
0.259 B
0.454 A
0.287 AB
0.802 a
0.525 b
2.76 a
87 c
0.191 b
0.475 d
0.333 b
0.739 B
0.395 B
3.50 B
55 B
0.120 C
0.605 B
0.275 B
and enhanced NPQ during the dry season (Table 4). An increase in NPQ is accompanied by an increase in the amount of
xanthophyll cycle pigments in the leaves (Adams et al. 2004).
If the cost of constructing xanthophyll cycle pigments is
smaller than the cost of constructing entirely new leaves,
down-regulation of PSII accompanied by enhanced NPQ will
be selective (Yamashita et al. 2000, Durand and Goldstein
2001). For the evergreen species, whose leaves have a high
construction cost (high LMA), down-regulation of PSII in the
dry season may maximize carbon return during a longer leaf
life span of low productivity in nutrient-poor habitats (Adams
et al. 2004). However, for the drought-deciduous species,
whose leaves have a low construction cost (low LMA), the entire replacement of leaves following the dry season may result
in greater carbon gain during a short leaf life span of high
productivity in nutrient-rich habitats (Eamus and Prichard
1998).
Ain-Lhout et al. (2004) compared photoprotective mechanisms for coping with excess light among six Mediterranean
semi-deciduous and evergreen shrub species and found that
NPQ increased during the summer drought for all species and
that the increase depended more on the species than on its leaf
habit. Martínez-Ferri et al. (2000) examined four Mediterranean evergreen shrub species during the summer drought and
suggested that drought-avoiding species avoid photo-inactivation by maintaining high PSII photochemical efficiency (i.e.,
photoinhibition avoidance), whereas drought-tolerant species
show declines in PSII efficiency and high NPQ mediated
through an active xanthophyll cycle (i.e., photoinhibition tolerance). The suggestion is confirmed by our results showing
photoinhibition avoidance in the drought avoiding deciduous
species and photoinhibition tolerance in the drought-tolerant
evergreen species.
green trees in the tropical dry forests of Thailand. The drought
avoiding deciduous trees were characterized by high N allocation for carbon assimilation in leaves, high water use and
photoinhibition avoidance and, following the onset of drought,
their high g smax and the VPD dependence of gs remained unchanged, and daytime NPQ either remained constant or declined until the leaves abscised. Thus, the short-lived leaves of
the drought avoiding deciduous species were capable of high
carbon gain during the short, wet season in nutrient-rich soils.
By contrast, the drought-tolerant evergreen was characterized
by low N allocation for leaf carbon assimilation, conservative
water-use, and photoinhibition tolerance during the dry season. Moreover, the value of g smax and the VPD dependence of gs
decreased and daytime NPQ increased. Thus, the long-lived
leaves of the drought-tolerant evergreen species were capable
of low carbon gain over both the wet and dry seasons in nutrient-poor soils. Our results suggest that a change in frequency
of forest fires can lead to a change in forest type, because the
artificial cessation of forest fires has reduced available nutrient
contents in deciduous forest soil in Thailand (Sakurai et al.
1998). We were able to examine only one evergreen species
(Hopea ferrea) in the present study, because Hopea trees almost entirely dominated the evergreen forest.
Acknowledgments
This study was supported by grants-in-aid from the National Research
Council of Thailand (04110479-0041), the Japan Environmental
Agency (E-3, S-1) and the Ministry of Education, Culture, Sports,
Science and Technology of Japan (14405009, 60343787). We thank
the staff of the research stations for helping in this research, and Drs.
S. Kobayashi, H. Tanaka, M. Takahashi, T. Nakashizuka and T. Nakano for their support and for providing information about the research forests.
References
Conclusions and perspective
We examined the physiological and anatomical bases underlying the contrasting drought responses of deciduous and ever-
Adams, III, W.W., C.R. Zarter, V. Ebbert and B. Demmig-Adams.
2004. Photoprotective strategies of overwintering evergreens. BioScience 51:41–49.
TREE PHYSIOLOGY VOLUME 26, 2006
ECOPHYSIOLOGY OF DRY-DECIDUOUS AND EVERGREEN LEAVES
Aerts, R. 1995. The advantages of being evergreen. Trend. Ecol. Evol.
10:402–407.
Ain-Lhout, F., M.C. Díaz Barradas, M. Zunzunegui, H. Rodríguez,
F. García Novo and M.A. Vargas. 2004. Seasonal differences in
photochemical efficiency and chlorophyll and carotenoid contents
in six Mediterranean shrub species under field. Photosynthetica 42:
399–407.
Baker, T.R., D.F.R.P. Burslem and M.D. Swaine. 2003. Associations
between tree growth, soil fertility and water availability at local and
regional scales in Ghanaian tropical rain forest. J. Trop. Ecol.
19:109–125.
Becker, P. 1996. Sap flow in Bornean heath and dipterocarp forest
trees during wet and dry periods. Tree Physiol. 16:295–299.
Bilger, W., U. Schreiber and M. Bock. 1995. Determination of the
quantum efficiency of photosystem II and of non-photochemical
quenching of chlorophyll fluorescence in the field. Oecologia 102:
425–432.
Borchert, R. 1994. Induction of rehydration and bud break by irrigation or rain in deciduous trees of a tropical dry forest in Costa Rica.
Trees 8:198–204.
Borchert, R. and W.T. Pockman. 2005. Water storage capacitance and
xylem tension in isolated branches of temperate and tropical trees.
Tree Physiol. 25:457–466.
Brodribb, T.J., N.M. Holbrook and M.V. Gutiérrez. 2002. Hydraulic
and photosynthetic co-ordination in seasonally dry tropical forest
trees. Plant Cell Environ. 25:1435–1444.
Brodribb, T.J., N.M. Holbrook, E.J. Edwards and M.V. Gutiérrez.
2003. Relations between stomatal closure, leaf turgor and xylem
vulnerability in eight tropical dry forest trees. Plant Cell Environ.
26:443–450.
Chabot, B.F. and D.J. Hicks. 1982. The ecology of leaf life spans.
Annu. Rev. Ecol. Syst. 13:229–259.
Chapin, III, F.S. 1980. The mineral nutrition of wild plans. Annu. Rev.
Ecol. Syst. 11:233–260.
Coley, P.D. 1988. Effects of plant growth rate and leaf lifetime on the
amount and type of anti-herbivore defense. Oecologia 74:531–536.
Demmig-Adams, B., W.W. Adams III, D.H. Barker, B.A. Logan,
D.R. Bowling and A.S. Verhoeven. 1996. Using chlorophyll fluorescence to assess the fraction of absorbed light allocated to thermal dissipation of excess excitation. Physiol. Plant 98:253–264.
Durand, L.Z. and G. Goldstein. 2001. Photosynthesis, photoinhibition and nitrogen use efficiency in native and invasive tree ferns
in Hawaii. Oecologia 126:345–354.
Eamus, D. and H. Prichard. 1998. A cost-benefit analysis of leaves of
four Australian savanna species. Tree Physiol. 18:537–545.
Eamus, D., B. Myers, G. Duff and D. Williams. 1999. Seasonal
changes in photosynthesis of eight savanna tree species. Tree
Physiol. 19:665–671.
Escudero, A., J.M. del Arco, I.C. Sanz and J. Ayala. 1992. Effects of
leaf longevity and retranslocation efficiency on the retention time
of nutrients in the leaf biomass of different woody species. Oecologia 90:80–87.
Genty, B., J.-M. Briantais and N.R. Baker. 1989. The relationship between the quantum yield of photosynthetic electron transport and
quenching of chlorophyll fluorescence. Biochim. Biophys. Acta
990:87–92.
Ishida, A., T. Toma and Marjenah. 1999a. Limitation of leaf carbon
gain by stomatal and photochemical processes in the top canopy of
Macaranga conifera, a tropical pioneer tree. Tree Physiol. 19:
467–473.
Ishida, A., A. Uemura, N. Koike, Y. Matsumoto and L.H. Ang. 1999b.
Interactive effects of leaf age and self-shading on leaf structure,
photosynthetic capacity and chlorophyll fluorescence in the rain
forest tree, Dryobalanops aromatica. Tree Physiol. 19:741–747.
655
Ishizuka, K., M. Takahashi, P. Tummakate, P. Limtong and V. Sunatapongsuk. 1995. Nutrient distribution and accumulation in different forest conditions. In International Workshop on the Changes of
Tropical Forest Ecosystems by El Niño and Others. National Research Council of Thailand, Bangkok, pp 227–284.
Kikuzawa, K. 1991. A cost-benefit analysis of leaf habit and leaf longevity of trees and their geographical pattern. Am. Nat. 138:
1250–1263.
Kitajima, K., S.S. Mulkey and S.J. Wright. 1997. Seasonal leaf phenotypes in the canopy of a tropical dry forest: photosynthetic characteristics and associated traits. Oecologia 109:490–498.
Kitayama, K., S.I. Aiba, M. Takyu, N. Majalap and R. Wagai. 2004.
Soil phosphorus fractionation and phosphorous-use efficiency of a
Bornean tropical montane rain forest during soil aging with podozolization. Ecosystems 7:259–274.
Kloeppel, B.D., S.T. Gower, J.G. Vogel and P.B. Reich. 2000. Leaflevel resource use for evergreen and deciduous conifers along a resource availability gradient. Funct. Ecol. 14:281–292.
Ladjal, M., R. Huc and M. Ducrey. 2005. Drought effects on hydraulic conductivity and xylem vulnerability to embolism in diverse
species and provenances of Mediterranean cedars. Tree Physiol.
25:1109–1117.
Lawrence, D., V. Suma and J.P. Mogea. 2005. Change in species composition with repeated shifting cultivation: limited role of soil nutrients. Ecol. Appl. 15:1952–1967.
Lovelock, C.E. and K. Winter. 1996. Oxygen-dependent electron
transport and protection from photoinhibition in leaves of tropical
tree species. Planta 198:580–587.
Martin, C.E., V.S. Loeschen and R. Borchert. 1994. Photosynthesis
and leaf longevity in trees of a tropical deciduous forest in Costa
Rica. Photosynthetica 30:341–351.
Martínez-Ferri, E., L. Balaguer, F. Valladares, J.M. Chico and
E. Manrique. 2000. Energy dissipation in drought-avoiding and
drought-tolerant tree species at midday during the Mediterranean
summer. Tree Physiol. 20:131–138.
Marod, D., U. Kutintara, C. Yarwudhi, H. Tanaka and T. Nakashizuka. 1999. Structural dynamics of a natural mixed deciduous
forest in western Thailand. J. Veg. Sci. 10:777–786.
Mediavilla, S. and A. Escudero. 2003a. Leaf life span differs from retention time of biomass and nutrients in the crowns of evergreen
species. Funct. Ecol. 17:541–548.
Mediavilla, S. and A. Escudero. 2003b. Stomatal responses to drought
at a Mediterranean site: a comparative study of co-occurring
woody species differing in leaf longevity. Tree Physiol. 23:
987–996.
Medina, E. 1995. Diversity of life forms of higher plants in neotropical dry forests. In Seasonally Dry Tropical Forests. Eds. S.H. Bullock, H.A. Mooney and E. Medina. Cambridge University Press,
Cambridge, pp 221–242.
Medina, E. and M. Francisco. 1994. Photosynthesis and water relations of savanna tree species differing in leaf phenology. Tree
Physiol. 14:1367–1381.
Murphy, P.G. and A.E. Lugo. 1986. Ecology of tropical dry forest.
Annu. Rev. Ecol. Syst. 17:67–88.
Nardini, A. and S. Salleo. 2003. Effects of the experimental blockage
of the major veins on hydraulics and gas exchange of Prunus
laurocerasus L. leaves. J. Exp. Bot. 54, 1213–1219.
Niinemets, Ü. and O. Kull. 2001. Sensitivity of photosynthetic electron transport to photoinhibition in a temperate deciduous forest
canopy: photosystem II center openness, non-radiative energy dissipation and excess irradiance under field conditions. Tree Physiol.
21:899–914.
TREE PHYSIOLOGY ONLINE at http://heronpublishing.com
656
ISHIDA ET AL.
Oliveras, I., J. Martínez-Vilalta, T. Jimenez-Ortiz, M.J. Lledó, A. Escarré and J. Piñol. 2003. Hydraulic properties of Pinus halepensis,
Pinus pinea and Tetraclinis articulata in a dune ecosystem of Eastern Spain. Plant Ecol. 169:131–141.
Oxborough, K. and N.R. Baker. 1997. Resolving chlorophyll a fluorescence images of photosynthetic efficiency into photochemical
and non-photochemical components: calculation of qP and Fv′/
Fm′without measuring Fo′. Photosynth. Res. 54:135–142.
Palmiotto, P.A., S.J. Davies, K.A. Vogt, M.S. Ashton, D.J. Vogt and
P.S. Ashton. 2004. Soil-related habitat specialization in dipterocarp
rain forest tree species in Borneo. J. Ecol. 92:609–623.
Paoli, G.D., L.M. Curran and D.R. Zak. 2006. Soil nutrients and beta
diversity in the Bornean Dipterocarpaceae: evidence for niche partitioning by tropical rain forest trees. J. Ecol. 94:157–170.
Pitman, J.I. 1996. Ecophysiology of tropical dry evergreen forest,
Thailand: measured and modelled stomatal conductance of Hopea
ferrea, a dominant canopy emergent. J. Appl. Ecol. 33:1366–1378.
Prado, C.H.B.A. and J.A.P.V. de Moraes. 1997. Photosynthetic capacity and specific leaf mass in twenty woody species of Cerrado vegetation under field conditions. Photosynthetica 33:103–112.
Prior, L.D., D. Eamus and D.M.J.S. Bowman. 2003. Leaf attributes in
the seasonally dry tropics: a comparison of four habitats in northern
Australia. Funct. Ecol. 17:504–515.
Reich, P.B., C. Uhl, M.B. Walters and D.S. Ellsworth. 1991. Leaf life
span as a determinant of leaf structure and function among 23 Amazonian tree species. Oecologia 86:16–24.
Reich, P.B., D.S. Ellsworth, M.B. Walters, J.M. Vose, C. Gresham,
J.C. Volin and W.D. Bowman. 1999. Generality of leaf trait relationships: a test across six biomes. Ecology 80:1955–1969.
Rundel, P.W. and K. Boonpragob. 1995. Dry forest ecosystems of
Thailand. In Seasonally Dry Tropical Forests. Eds. S.H. Bullock,
H.A. Mooney and E. Medina. Cambridge University Press, Cambridge, pp 93–123.
Russo, S.E., S.J. Davies, D.A. King and S. Tan. 2005. Soil-related
performance variation and distributions of tree species in a Bornean rain forest. J. Ecol. 93:879–889.
Ryser, P. 1996. The importance of tissue density for growth and life
span of leaves and roots: a comparison of five ecologically contrasting grasses. Funct. Ecol. 10:717–723.
Sakurai, K., S. Tanaka, S. Ishizuka and M. Kanzaki. 1998. Differences in soil properties of dry evergreen and dry deciduous forests
in the Sakaerat Environmental Research Station. Tropics 8:61–80.
Santiago, L.S., K. Kitajima, S.J. Wright and S.S. Mulkey. 2004. Coordinated changes in photosynthesis, water relations and leaf nutritional traits of canopy trees along a precipitation gradient in lowland tropical forest. Oecologia 139:495–502.
Shimizu, M., A. Ishida and T. Hogetsu. 2005. Root hydraulic conductivity and whole-plant water balance in tropical saplings following
a shade-to-sun transfer. Oecologia 143:189–197.
Silla, F. and A. Escudero. 2004. Nitrogen-use efficiency: trade-offs
between N productivity and mean residence time at organ, plant
and population levels. Funct. Ecol. 18:511–521.
Sinsuwongwat, S., A. Nuntagij, A. Shutsrirung, M. Nomura and
S. Tajima. 2002. Characterization of local rhizobia in Thailand and
distribution of malic enzymes. Soil Sci. Plant Nutr. 48:719–727.
Sobrado, M.A. 1986. Aspects of tissue water relations and seasonal
changes of leaf water potential components of evergreen and deciduous species coexisting in tropical dry forests. Oecologia 68:
413–416.
Sobrado, M.A. 1991. Cost-benefit relationships in deciduous and
evergreen leaves of tropical dry forest species. Funct. Ecol. 5:
608–616.
Sobrado, M.A. 1993. Trade-off between water transport efficiency
and leaf life span in a tropical dry forest. Oecologia 96:19–23.
Sobrado, M.A. 1996. Embolism vulnerability of an evergreen tree.
Biol. Plant. 38:297–301.
Sobrado, M.A. 1997. Embolism vulnerability in drought-deciduous
and evergreen species of a tropical dry forest. Acta Oecol. 18:
383–391.
Swaine, M.D. 1996. Rainfall and soil fertility as factors limiting forest
species distributions in Ghana. J. Ecol. 84:419–428.
Terashima, I., S.-C. Wong, C.B. Osmond and G.D. Farquhar. 1988.
Characterisation of non-uniform photosynthesis induced by abscisic acid in leaves having different mesophyll anatomies. Plant Cell
Physiol. 29:385–394
Tyree, M.T., S.D. Davis and H. Cochard. 1994. Biophysical perspectives of xylem evolution: is there a tradeoff of hydraulic efficiency
for vulnerability to dysfunction? IAWA J. 15:335–360.
Wright, I.J., M. Westoby and P.B. Reich. 2002. Convergence towards
higher leaf mass per area in dry and nutrient-poor habitats has different consequences for leaf life span. J. Ecol. 90:534–543.
Yamashita, N., A. Ishida, H. Kushima and N. Tanaka. 2000. Acclimation to sudden increase in light favoring an invasive over native
trees in subtropical islands, Japan. Oecologia 125:412–419.
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