Tree Physiology 21, 497–504
© 2001 Heron Publishing—Victoria, Canada
Light-use properties in two sun-adapted shrubs with contrasting
canopy structures
ATSUSHI ISHIDA,1 TAKASHI NAKANO,2 AKIRA UEMURA,1 NAOKO YAMASHITA,1
HIROMI TANABE1 and NOBUYA KOIKE1
1
Forestry and Forest Products Research Institute (FFPRI), P.O. Box 16, Tsukuba Norin Danchi, Ibaraki 305-8687, Japan
2
Yamanashi Institute of Environmental Sciences, Fuji-Yoshida, Yamanashi 403-0005, Japan
Received April 3, 2000
Summary We investigated the impact of high solar
irradiance and elevated temperature on carbon gain by two,
co-occurring, sun-adapted, dwarf shrub species, Planchonella
obovata var. dubia (Koidz.) Hatusima and Hibiscus glaber
Matsumura, growing on sun-exposed ridges in the Bonin Islands, in the subtropical Pacific Ocean. Planchonella had
steeply inclined, longer lived, sclerophyllous leaves, whereas
Hibiscus has thinner, more horizontally oriented, and shorter
lived leaves. We tested the hypothesis that leaf physiological
tolerance to high light is lower in Planchonella than in Hibiscus. Under relatively high irradiances (photosynthetic photon
flux density, PPFD, > 500 µmol m –2 s –1), net photosynthetic
rate (Pn) was about 8.0 and 0.4 µmol m –2 s –1 in mature and
young leaves of Planchonella, and about 12.4 and 10.3 µmol
m –2 s –1 in mature and young leaves of Hibiscus, respectively.
Both Pn and photosystem II (PSII) quantum yield at a given
PPFD were lower in Planchonella than in Hibiscus, whereas
non-photochemical quenching (NPQ) at a given PPFD was
higher in Planchonella. When leaf discs were exposed to high
light (1900 µmol m –2 s –1 PPFD) at 37, 40 or 43 °C for 3 h, the
recovery of PSII quantum yield (Fv/Fm) in the following
60-min dark period was slower in Planchonella than in Hibiscus, indicating that the ability of PSII to tolerate high light and
high temperature was less in Planchonella than in Hibiscus.
We postulate that there is a linkage between leaf display and
leaf photochemical ability in sun-adapted shrub species.
Keywords: chlorophyll fluorescence, heat stress, Hibiscus
glaber, high light stress, leaf inclination angle, leaf hair,
Planchonella obovata.
Introduction
High solar irradiance can impair photosynthetic capacity, an
effect called photoinhibition. Various mechanisms that prevent or reduce photoinhibition have been described in tropical
sun-adapted plants. These include processes that dissipate excess photochemical energy, such as non-photochemical
quenching (NPQ) (Thiele et al. 1998, Ishida et al. 1999c), high
rates of photorespiration (Ishida et al. 1999b) and morphological characteristics, such as vertical leaf inclination angle (He
et al. 1996, Ishida et al. 1999a), leaf pubescence (Ehleringer
and Björkman 1978), and self-shading resulting from leaf
overlap (Valladares and Pearcy 1998). The inhibitory effects
on photosynthesis caused by excess light can be exacerbated
by other stresses such as heat (e.g., Ludlow 1987, Gamon and
Pearcy 1990, Mulkey and Pearcy 1992, Königer et al. 1998,
Ishida et al. 2000), nitrogen deficiency (e.g., Ferrar and Osmond 1986, Kao and Forseth 1992), and drought (e.g.,
Björkman and Powles 1984). Hence, the amount of excess
light energy varies with other environmental factors.
Shrubs growing on sun-exposed ridges in the Bonin Islands
in the subtropical Pacific Ocean are exposed to high radiation
and severe drought (Mishio 1992), and possibly also nitrogen
deficiency. To understand better the relationships between
light-use properties and leaf display in this environment, two
co-occurring, native dwarf shrubs, Hibiscus glaber Matsumura and Planchonella obovata var. dubia (Koidz.)
Hatusima, with contrasting canopy structures, were investigated. We compared three aspects of Planchonella and Hibiscus: (1) canopy structure; (2) diurnal changes in leaf gas
exchange and fluorescence yield of photosystem II (PSII); and
(3) the tolerance of PSII to a combination of high light and
high temperature. We tested the hypothesis that the ability of
PSII to tolerate high irradiances and elevated temperature is
lower in Planchonella, which has sclerophyllous, near vertically oriented leaves, than in Hibiscus, which has thinner,
more nearly horizontal leaves. The results, which are consistent with our hypothesis, suggest that there is a linkage between leaf display and leaf photochemical ability in
sun-adapted shrubs. Such linkage presumably contributes to
the maximization of carbon gain at the whole-canopy level.
However, few integrated analyses have been undertaken to investigate the relationship in woody plants (Küppers 1989,
Niinemets 1998).
Materials and methods
Study site and plant species
The study was conducted at a site in the Bonin Islands, Japan,
located in a subtropical region in the North Pacific Ocean,
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ISHIDA, NAKANO, UEMURA, YAMASHITA, TANABE AND KOIKE
about 1000 km south of Tokyo. The site is a shallow-soil ridge
on the island of Chichi-jima (27°5′ N, 142°13′ E, alt. 210 m),
which has an area of 24 km 2 and a maximum elevation of
326 m. Mean annual air temperature and precipitation were
22.9 °C and 1261 mm, respectively, during the 1989–1999 period. During the same period, mean monthly precipitation between July and September was 90 mm. Monthly precipitation
below 100 mm in this season is classified as a dry period
(Richards 1996). In the year of the study (1998), however,
mean monthly July–September precipitation was relatively
high (191 mm). Mean air temperature for the same period in
1998 was 27.5 °C. More detailed climatic information about
the ridge sites on Chichi-jima are described in Shimizu (1984)
and Mishio (1992).
The soil (Chromic Cambisols) at the study site is of volcanic
origin and about 30 cm thick, with bedrock exposed in several
places. The vegetation is dominated by shrub species that
range to a maximum height of 2 m. Two common co-occurring shrubs, Hibiscus glaber and Planchonella obovata var.
dubia, were selected for study. Both species are endemic to the
Bonin Islands. Maximum leaf life span is about 3 years in
Planchonella and about 2 years in Hibiscus (authors’ unpublished observations). In Planchonella, current-year leaves are
densely covered with red hairs, whereas 1- and 2-year-old
leaves of Planchonella and Hibiscus leaves of all ages are glabrous.
Canopy structure and leaf optical properties
Canopy height in the shrub stand selected for study was approximately 1 m. A 1-m-high rectangular tower (30 cm per
side) was erected within the canopy in September 1998. The
tower enclosed 190 Hibiscus leaves and 1039 Planchonella
leaves. At midday on a cloudy day, photosynthetic photon flux
density (PPFD) was measured with a horizontally oriented
quantum sensor both above the tower and at 5-cm intervals
within the tower. Leaves within the tower were then harvested
in 15-cm thick horizontal layers and sealed in plastic bags. At
the time of harvest, the inclination to the vertical of the midrib
of each leaf was measured with a protractor and plumb line.
The area of each leaf was determined with an area meter
(LI-3000, Li-Cor Inc., Lincoln, NE), before drying to constant
mass at 80 °C.
Reflectance and transmittance of fully expanded young
(current-year) and mature (1-year-old) canopy leaves were
measured between 400 and 800 nm at 1-nm intervals with a
Li-Cor spectroradiometer (LI-1800C) equipped with an external integrating sphere (LI-1800-12). Light absorbance of the
leaves was calculated from light reflectance and transmittance
at each wavelength. To determine the effects on leaf optical
properties of the dense red hairs on the young leaves of
Planchonella, leaf optical properties were remeasured after removing the hairs with adhesive tape.
Diurnal change measurements
Diurnal changes in leaf gas exchange and PSII chlorophyll fluorescence were measured on September 4 and 6, 1998. We se-
lected five fully expanded young and mature leaves at the top
of the canopy in a single plant of each species. To determine
the effects of leaf hairs and leaf inclination angle on gas exchange and chlorophyll fluorescence of young Planchonella
leaves, measurements were made on an additional five fully
expanded young leaves of the same plant after removing the
leaf hairs and orienting the leaf in the horizontal plane by
means of fine wires.
Leaf-area-based, net photosynthetic rate (Pn, µmol m –2 s –1)
and stomatal conductance to water vapor (gs, mol m –2 s –1) of
each leaf were measured at various times from dawn to dusk
with a Li-Cor open-circuit, infrared, gas analysis system
(LI-6400). Fluorescence yield, PPFD at the leaf surface, and
leaf temperature were measured with a Mini-PAM (Walz,
Effeltrich, Germany) equipped with a leaf clip holder (Model
2030-B, Walz) on which a micro-quantum sensor and a thin
NiCr-Ni thermocouple were mounted. Maximum fluorescence (Fm ) and minimum fluorescence (Fo) were measured in
darkness just before dawn, and maximum fluorescence (Fm′)
and steady-state fluorescence (F) in the light-adapted state
were measured at various times during the day, following the
methods of Bilger et al. (1995). Saturated light pulses
(6000 µmol m –2 s –1 PPFD) were applied through a fiber-optic
cable oriented at 60° to the leaf surface. The angle and distance
between the leaf and the fiber-optic cable were manually adjusted and maintained with the leaf clip holder.
The PSII quantum yield in the light ((Fm′ – F)/Fm′ =
∆F/Fm′) was calculated according to Genty et al. (1989). The
electron transport rate through PSII (ETR) was calculated as:
ETR = ( ∆F Fm′ )( leaf surface PPFD) A0.5,
(1)
where A is light absorbance of the lamina for wavelengths in
the range 400–700 nm. Values of A in Hibiscus were 0.76 in
young leaves and 0.83 in mature leaves, and in Planchonella A
was 0.77 in young leaves, with and without epidermal hairs removed, and 0.85 in mature leaves. Non-photochemical
quenching (NPQ, a measure of thermal dissipation of excess
absorbed light energy as a protective mechanism) was calculated as (Bilger and Björkman 1990):
NPQ = ( Fm Fm′ ) − 1.
(2)
Effects of high light and temperature on PSII
To compare the tolerance of PSII to high light in leaves of different ages, fully expanded young and mature leaves (n = 8 of
each) were exposed in the field to high light (2000 µmol m –2
s –1 PPFD) at 38 °C for 3 h at midday in a chamber (2 × 3 cm
area) equipped with an infra-red leaf gas exchange measurement system (LI-6400, Li-Cor) and a red and blue light emitting diode (LI-6400-02B, Li-Cor). After treatment, the leaves
were kept in the dark in the field at around 28 °C with the aid of
a dark leaf clip with a sliding shutter (DLC-8, Walz).
Dark-adapted PSII quantum yield, Fv/Fm = (Fo – Fm)/Fm, was
measured at 10-min intervals for 2 h with a Mini-PAM (Walz)
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by exposing the leaves in the field to saturating light pulses
(6000 µmol m –2 s –1 PPFD) through a fiber optic cable oriented
at 90° to the leaf surface.
To examine the combined effects of high light and elevated
temperature on PSII, discs (10 cm2) were cut from mature
leaves after overnight dark-adaptation in the laboratory. After
measuring Fv/Fm, the leaf discs were placed on wet filter paper
in the chamber with a halogen lamp (LS2, Hansatech Ltd.,
King’s Lynn, U.K.). The temperature of the leaf chamber was
controlled by a water bath connected to the upper and lower
parts of the chamber. The dark-adapted leaf discs were exposed to high light (1900 µmol m –2 s –1) and various constant
leaf temperatures (37, 40 and 43 °C) for 3 h in the chamber.
After treatment, the leaf discs were kept in the dark at around
25 °C (the mean night air temperature in the summer season)
and Fv/Fm measured at 10-min intervals for 2 h with a leaf clip
holder (Model 2030-B, Walz) and a Mini-PAM (Walz). Subsequently, the leaf discs were held in darkness overnight (25
°C) and Fv/Fm was remeasured the following morning. Four
leaf discs were used per sample at each temperature for each
species.
Figure 1. Vertical distribution of leaf area index (LAI) and the ratio of
photosynthetic photon flux density (PPFD) to full sunlight in 15-cm
canopy layers of (A) Planchonella obovata var. dubia and (B) Hibiscus glaber. Horizontal lines show ± 1 SD.
Results
Leaf gas exchange and chlorophyll fluorescence
Canopy structure
Cumulative leaf area index within the 30 × 30-cm plot was 5.1
in Planchonella and 5.6 in Hibiscus. The proportion of total
leaf area occurring in the upper half of the canopy was 72% in
Hibiscus and 51% in Planchonella (Figure 1). As a result, solar irradiance decreased greatly in the upper part of the canopy
in Hibiscus, whereas much of the light penetrated to the lower
canopy of Planchonella.
Planchonella had steeply inclined, sclerophyllous leaves,
whereas Hibiscus had more horizontally oriented, thin leaves.
The leaf angle of inclination from the horizontal in the top
20 cm of the canopy was significantly greater in Planchonella
(41 ± 15°, mean ± 1 SD) than in Hibiscus (23 ± 18°) (P <
0.001, u-test; Figure 2). Specific leaf area was greater in Hibiscus (9.83 ± 2.36 m 2 kg –1, mean ± 1 SD) than in Planchonella
(7.01 ± 1.64 m 2 kg –1) (P < 0.001, t-test). Specific leaf area increased in the lower part of the canopy in Hibiscus but not
Planchonella. Based on their low SLA, the canopy leaves of
Planchonella were classified as sclerophyllous (Edwards et al.
2000).
The red hairs on the surface of young leaves of Planchonella affected the optical properties of the leaf with respect to
photosynthetically active radiation. By removing the leaf
hairs, reflectance of red light (650–700 nm) decreased from
21 to 13%, whereas transmittance of red light increased from
1.2 to 1.8% (Figure 3). As a result, absorbance of red light increased from 77 to 85%. On the other hand, removing the leaf
hairs caused reflectance of green light (510–550 nm) to increase from 10 to 15%, and transmittance of green light to increase from 0.8 to 1.8%. Absorbance of visible light
(400–700 nm) was unaffected by removal of the leaf hairs.
The temperature of canopy leaves of Planchonella and Hibiscus increased with increasing PPFD at the leaf surface (Figure 4). When leaves were exposed to high PPFD (> 1000 µmol
m –2 s –1), leaf temperature reached 34.0 ± 1.6 °C in Planchonella and 31.9 ± 1.5 °C in Hibiscus. The difference in leaf
temperature between the species was highly significant (P <
0.001, t-test).
Figure 2. Vertical distribution of (A) leaf angle of inclination to the
horizontal and (B) specific leaf area (SLA, m2 kg –1) in Planchonella
obovata var. dubia (䊉) and Hibiscus glaber (䊊). Horizontal bars =
1 SD.
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ISHIDA, NAKANO, UEMURA, YAMASHITA, TANABE AND KOIKE
Figure 3. Reflectance (bold lines) and transmittance (thin lines) of
light (400–800 nm) by young Planchonella obovata var. dubia leaves
with (solid lines) and without (dashed lines) epidermal leaf hairs.
When leaves were exposed to PPFD greater than 500 µmol
m –2 s –1, Pn was 8.0 ± 2.0 and 0.4 ± 1.2 µmol m –2 s –1 in mature
and young leaves of Planchonella, respectively, and the corresponding values for Hibiscus were 12.4 ± 2.4 and 10.3 ±
1.6 µmol m –2 s –1 (Figure 5). In young leaves of Planchonella,
Pn was barely positive during the summer season, and there
were no differences in Pn between naturally inclined young
leaves with leaf hairs and the horizontally fixed young leaves
without leaf hairs. For each leaf type, Pn was significantly
higher in Hibiscus than in Planchonella (P < 0.001, t-test). At
PPFDs > 500 µmol m –2 s –1, leaf internal CO2 concentration
was 228 ± 19 and 331 ± 24 µmol mol –1 in mature and young
leaves of Planchonella, and 211 ± 22 and 263 ± 10 µmol mol –1
in mature and young leaves of Hibiscus, respectively. Under
these relatively high PPFDs, both Pn and gs decreased when
leaf temperature exceeded 36 °C in Planchonella. In contrast,
in Hibiscus, no marked temperature-induced depression of Pn
and gs was found, except for a reduction in gs in young leaves.
When leaf temperature increased above 36 °C, the leaf-to-air
vapor pressure deficit exceeded 3 kPa (data not shown). However, the leaves are rarely exposed to such high temperatures
and irradiances for long periods (cf. Figure 4).
The PSII quantum yield, Fv/Fm, in darkness just before
dawn was 0.71 ± 0.02 in young leaves and 0.77 ± 0.04 in mature leaves of Planchonella, and the corresponding values for
Hibiscus were 0.75 ± 0.02 and 0.8 ± 0.02. In situ photochemical parameters of chlorophyll fluorescence of PSII were
closely related to PPFD at the leaf surface (Figure 6). Both
∆F/Fm′ and ETR at a given PPFD were lower in Planchonella
than in Hibiscus in each leaf type (P < 0.05, t-test), especially
under relatively high PPFD (> 600 µmol m –2 s –1). This indicates that the photochemical ability of the canopy leaves was
lower in Planchonella than in Hibiscus. At relatively high
PPFDs (> 600 µmol m –2 s –1), both ∆F/Fm′ and ETR at a given
PPFD were lower in young leaves than in mature leaves,
whereas NPQ at a given PPFD was higher in young leaves
than in mature leaves of both species (P < 0.001, t-test). This
indicates that the photochemical ability of the canopy leaves
was lower in young leaves than in mature leaves. In
Planchonella, both ∆F/Fm′ and ETR at a given PPFD were
lower in leaves held horizontal after the removal of epidermal
hairs than in the naturally inclined young leaves with hairs, especially at PPFDs of 200–1000 µmol m –2 s –1 (P < 0.001,
t-test). Thus, the steep inclination and epidermal hairs of the
young leaves of Planchonella helped maintain a relatively
high photochemical efficiency of PSII. Although there was a
tendency for NPQ to increase rapidly in young Planchonella
leaves at PPFDs < 200–800 µmol m –2 s –1, at high PPFDs
(> 800 µmol m –2 s –1) NPQ was no higher in young leaves that
were held horizontal after removal of epidermal hairs than in
the naturally inclined young leaves with hairs.
Effects of light and temperature on PSII
The value of Fv/Fm measured at predawn was above 0.7 in all
leaves. When leaves were exposed to high PPFD (2000 µmol
m –2 s –1) and temperature (38 °C) for 3 h at midday in the field,
Fv/Fm immediately dropped below 0.5 in Planchonella, but
dropped only slightly in Hibiscus, especially in the mature
leaves (Figure 7). In both species, recovery of Fv/Fm in dark after exposure to high light was less in young leaves than in mature leaves (P < 0.05, t-test). Recovery was slowest in young
leaves of Planchonella, indicating that damage to PSII caused
by high radiation was highest in these leaves.
In mature leaves, in which PSII was relatively tolerant of
high light, the combined effects of high light and elevated temperature on PSII were measured in leaf discs in the laboratory.
When the discs were exposed to high PPFD (1900 µmol m –2
s –1) and a temperature of 37, 40 or 43 °C for 3 h, Fv/Fm declined immediately. In both species, the decline increased with
Figure 4. Relationships between
photosynthetic photon flux density
(PPFD) at the leaf surface and leaf
temperature (Tleaf) of young leaves
(䊉), mature leaves (䊊), and horizontally fixed young leaves without epidermal hairs (HL; 䉱) of (A)
Planchonella obovata var. dubia and
(B) Hibiscus glaber. Vertical lines
show ± 1 SD.
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Figure 7. Efficiency of energy conversion of PSII (Fv/Fm) during a recovery period in the dark in young leaves (䊉) and mature leaves (䊊)
of (A) Planchonella obovata var. dubia and (B) Hibiscus glaber, after
the leaves had been exposed to high light (2000 µmol m – 2 s – 1 PPFD)
and relatively high temperature (38 °C) for 3 h in the field. The value
of Fv/Fm at time = 0 indicates the PSII quantum yield immediately after termination of the light exposure period. Vertical lines show ± 1
SD (n = 8).
Figure 5. Relationships between leaf temperature (Tleaf ) and (A, B)
net photosynthetic rate (Pn) and (C, D) stomatal conductance to water
vapor (gs ) at relatively high PPFDs in the field (> 500 µmol m–2 s–1) in
young leaves (䊉) and mature leaves (䊊) of (A, C) Planchonella
obovata var. dubia and (B, D) Hibiscus glaber. Vertical lines show ±
1 SD.
increasing leaf temperature (Figure 8). After exposure to high
PPFDs, Planchonella leaf discs that had been exposed to
40 and 43 °C and Hibiscus leaf discs that had been exposed to
43 °C showed only slight signs of recovery during the subse-
Figure 6. Relationships between photosynthetic photon flux density
(PPFD) at the leaf surface in the field and (A, B) PSII quantum yield
(∆F/Fm′), (C, D) electron transport rate through PSII (ETR), and (E,
F) non-photochemical quenching (NPQ) in young leaves (䊉), mature
leaves (䊊), and horizontally fixed young leaves without epidermal
hairs (HL; 䉱) of (A, C, E) Planchonella obovata var. dubia and (B, D,
F) Hibiscus glaber. Vertical lines show ± 1 SD.
quent dark period. Even after an overnight dark period, the
recovery of Fv/Fm in both species decreased with increasing
leaf temperature during the preceding light exposure (P <
0.05, t-test), and the overnight recovery of Fv/Fm was less in
Planchonella than in Hibiscus only in the 37 °C treatment (P <
0.05, t-test). In summary, the data indicate that the tolerance of
PSII to high light and heat was lower in Planchonella than in
Figure 8. Efficiency of energy conversion of PSII (Fv/Fm) in leaf discs
of mature leaves measured during a 2-h recovery period in the dark
for (A) Planchonella obovata var. dubia and (B) Hibiscus glaber, after the leaf discs were exposed to high light (1900 µmol m –2 s –1
PPFD) and 37 °C (䉭), 40 °C (䊉), or 43 °C (䊐) for 3 h in the laboratory. The value of Fv/Fm at the initial time indicates the PSII quantum
yield just before the 3-h light exposure, and Fv/Fm at time = 0 indicates the PSII quantum yield immediatly after termination of the light
exposure period. Vertical lines show 1 SD (n = 4).
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ISHIDA, NAKANO, UEMURA, YAMASHITA, TANABE AND KOIKE
Hibiscus, even in mature leaves.
Discussion
Hibiscus and Planchonella are sun-adapted shrubs that co-occur on dry, sun-exposed ridges in the Bonin Islands. Despite
these similarities, these plants have different canopy structures
with respect to the vertical distribution of leaves within the
canopy and leaf inclination angles, and their PSIIs had different light-use efficiencies and different capacities for tolerating
high light and elevated temperature. The overall results are
consistent with the hypothesis that Planchonella leaves with
steep inclination angles had lower tolerance to the combination of high temperature and strong sunlight than Hibiscus
leaves with more horizontally oriented leaves.
Sustained photoinhibition is sometimes found in outer-canopy leaves of tropical forest trees (Krause et al. 1995). Mean
Fv/Fm measured in the dark just before dawn was 0.71 in
young leaves and 0.77 in mature leaves of Planchonella, these
values are lower than the values of 0.81–0.83 found in unstressed leaves of higher plants (Björkman and Demmig
1987), indicating that the young leaves of Planchonella exhibited sustained photoinhibition. It has been shown that, after
leaves are returned to darkness, the recovery process of PSII
involves a rapid recovery phase (less than 15 min) associated
with the restoration of the thylakoid proton gradient, a rapid
recovery phase (within 15 min) associated with the xanthophyll cycle, and a slow recovery phase (> 60 min) associated
with the repair of damaged D1 protein (Königer et al. 1998).
The slow recovery of Fv/Fm observed in young leaves of
Planchonella during the first 60 min in darkness (Figure 7) indicates low tolerance to high radiation exposures, probably associated with the small pool size of xanthophyll cycle
pigments in the young leaves.
We found that the steeper angle and hairs in the young
leaves of Planchonella play a crucial role in preventing leaf
temperatures from exceeding tissue tolerance limits. They
contributed to the maintanance of a high ∆F/Fm′ and to a reduction in the risk of photoinhibition. High temperatures occurred with increasing irradiances at the leaf surface
(Figure 4). Yamane et al. (1998) showed that photoinactivation of PSII is rapid at high temperatures. Several
studies have shown that a combination of high light and elevated leaf temperature reduces photochemical capacity or carbon gain in leaves of Vitis california Benth. (Gamon and
Pearcy 1990), Alocasia macrorrhiza (L.) G. Don (Königer et
al. 1998), Liquidambar and Quercus (Niinemets et al. 1999),
and some rain forest dipterocarps (Ishida et al. 2000). Other
studies have shown that, at open habitats, steep leaf inclination
angles in the upper canopy are associated with reduced leaf
temperature, water loss, and midday depression of carbon gain
or ∆F/Fm′, even in sun-adapted plants (Ehleringer and Werk
1986, Forseth and Teramura 1986, Chiariello et al. 1987,
Gamon and Pearcy 1990, Kao and Forseth 1992, Valladares
and Pearcy 1997, Ishida et al. 1999a). We found that leaf temperature at a given PPFD was higher in Planchonella than in
Hibiscus (Figure 4) because Planchonella had low transpira-
tion rates (Figure 5). Thus, the risk of high radiation stress
damaging PSII was higher in Planchonella than in Hibiscus,
because the tolerance of PSII to high light and temperature
was lower. Although the epidermal hairs on young leaves of
Planchonella increase the intrinsic cost of leaf construction,
they are an effective stress defense because they reduce leaf
absorbance of red photosynthetically active radiation by 10%.
Canopy structure and leaf display critically affect the degree
of light exposure at the crown level. Whitmore (1998) concluded that tropical pioneers tend to have a mono-layered canopy. In such a canopy structure, leaves with high photosynthetic capacities can have a high daily carbon gain in
high-light environments (Mooney and Ehleringer 1978). Hibiscus has a mono-layered canopy structure in which the
leaves are concentrated in the upper part of the canopy,
whereas Planchonella has a more multi-layered canopy with
steep leaf inclination angles. Accordingly, Hibiscus leaves
with high ∆F/Fm′ and Pn, at a given PPFD, were concentrated
in the upper part of the canopy, resulting in an effective use of
high light energy at the whole-canopy level. In Planchonella,
the young leaves at the top of the canopy reduced irradiance,
thus contributing to the photoprotection of lower canopy
leaves.
Planchonella and Hibiscus display different combinations
of physiological and morphological traits for avoiding damage
caused by excess light energy. Planchonella has more steeply
inclined, longer lived (about 3 years), sclerophyllous leaves,
whereas Hibiscus has more horizontally oriented, shorter lived
(about 2 years), thin leaves. Tolerance of PSII to high light and
temperature and leaf photosynthetic capacity were lower in
Planchonella than in Hibiscus. Planchonella could offset the
superior potential productivity of Hibiscus leaves because of
its longer leaf life span. A correlation between leaf life span
and leaf photosynthetic capacity has been demonstrated
(Gratani and Bombell 2000, Yamashita et al. 2000). Gratani
and Bombell (1999) showed that, among Mediterranean
sun-adapted shrubs, species with short leaf life spans had
higher photosynthetic capacities than species with long leaf
life spans. Sobrado (1991) showed that, in a tropical dry forest,
species with short leaf life spans had lower ratios of leaf construction cost to maximum Pn than species with long leaf life
spans; i.e., the potential pay-back of construction cost is faster
in leaves with short life spans than in leaves with long life
spans. Based on these studies and our results, we conclude that
Planchonella leaves offset high leaf construction costs (thick
lamina and epidermal hairs) by a long leaf life span. They had
a low photosynthetic capacity and were adapted to relatively
low irradiances. In contrast, Hibiscus leaves, which have a low
construction cost, because of their thin lamina, have a short
life span, high photosynthetic capacity and are adapted to high
incident light. Leaf life span is probably linked with leaf display and leaf physiological ability as a suite of co-occurring
traits.
Acknowledgments
We thank Drs. N. Kachi and T. Toma for helpful comments on the
manuscript. We also thank Drs. S. Nohara, Y. Matsumoto, and
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H. Taoda for support of this study. This study was supported by the
following grants: (1) Conservation Methods of Subtropical Island
Ecosystems conducted by NIES, MRI, and FFPRI; (2) Restoration
and Management of Forest Ecosystem in the Bonin Islands conducted
by FFPRI, both funded by the Japan Environmental Agency; and (3)
Development of detailed methods to evaluate CO2 budgets in forest
and ocean ecosystems funded by the Ministry of Agriculture, Forestry
and Fisheries in Japan.
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