Functional Ecology 2009, 23, 658– 667
doi: 10.1111/j.1365-2435.2009.01552.x
Stem hydraulics mediates leaf water status, carbon gain,
nutrient use efficiencies and plant growth rates across
dipterocarp species
Blackwell Publishing Ltd
Jiao-Lin Zhang and Kun-Fang Cao*
The Key Laboratory of Tropical Forest Ecology, Xishuangbanna Tropical Botanical Garden, Chinese Academy of
Sciences, Mengla, Yunnan 666303, China
Summary
1. Stem vascular system strongly influences structure and functioning of leaves, life-history, and
distribution of plants. Xylem structure and hydraulic conductivity of branches, leaf functional
traits, and growth rates in 17 dipterocarp species in a mature plantation stand were examined to
explore the functional relationships between these traits.
2. Maximum hydraulic conductivity on the bases of both sapwood and leaf area ( kL) were
positively correlated with midday leaf water potential in the rainy season, stomatal conductance,
area-based maximum photosynthetic rate, photosynthetic N (PNUE) and P use efficiencies
(PPUE), and mean height and diameter growth rates. Moreover, kL was positively correlated
with mesophyll thickness and mass-based maximum photosynthetic rate. These results revealed the
mechanistic linkage between stem hydraulics and leaf photosynthesis through nutrient use
efficiency and mesophyll development of leaves.
3. A detrended correspondence analysis (DCA) using 37 traits showed that the traits related to
stem hydraulics and leaf carbon gain were loaded on the first axis whereas traits related to light
harvesting were loaded on the second axis, indicating that light harvesting is a distinct ecological
axis for tropical canopy plants. The DCA also revealed a trade-off between photosynthetic water
use efficiency and hydraulic conductivity along with PNUE and PPUE.
4. The congeneric species were scattered fairly close together on the DCA diagram, indicating
that the linkages between stem hydraulics, leaf functional traits, and plant growth rates are phylogenetically conserved.
5. These results suggest that stem hydraulics mediates leaf water status, carbon gain, nutrient use
efficiencies, and growth rates across the dipterocarp species. The wide variation in functional traits
and growth rates among these dipterocarp species along with the trade-offs mentioned above
provide a possible explanation for their co-existence in tropical forest communities.
Key-words: common garden, Dipterocarpaceae, leaf anatomy, photosynthetic capacity, stomatal
conductance
Introduction
The xylem vascular system strongly influences life-history
strategy (West et al. 1999) and distribution of plants (Brodribb
& Hill 1999; Engelbrecht et al. 2007) owing to its effects on
water and nutrient transportation from soil to leaves, resistance
to xylem embolism induced by drought and freezing temperatures, and mechanical strength. The difference in water
potential between soil and leaves is largely determined by the
conducting vascular system through its regulation of water
*Correspondence author. E-mail: [email protected]
transportation from roots through stems into leaves where the
water is transpired via the stomata (Meinzer 2003). Leaf is
a major bottle-neck of plant hydraulic conductivity and
contributes about 30% of whole plant hydraulic resistance
(Sack et al. 2003). If soil water supply is ample, efficient stem
hydraulic conductivity allows quick water transport into
leaves to compensate leaf transpiration, resulting in high leaf
water potential during the day. Stem hydraulics has therefore
been found to be related to minimum daily leaf water potential
in the rainy season for chaparral shrubs (Ackerly 2004) and
tropical rainforest trees (Santiago et al. 2004). The strong
linkage between stem hydraulic conductivity and stomatal conductance of leaves has also been demonstrated by experimental
© 2009 The Authors. Journal compilation © 2009 British Ecological Society
Stem hydraulics and leaf functional traits 659
manipulations during which hydraulic conductivity was
reduced through embolism injection (Hubbard et al. 2001),
root chilling (Brodribb & Hill 2000) and root pruning
(Meinzer & Grantz 1991). High stomatal conductance allows
rapid CO2 diffusion into carboxylation sites, and consequently
strong photosynthetic capacity. Species with strong photosynthetic capacity are generally fast-growing (Poorter &
Bongers 2006) and consequently have low wood density
(Castro-Díez et al. 1998; King et al. 2006).
Plant functional traits reflect plant adaptations to specific
environments and utilization of resources, and therefore
provide valuable information for the analyses of community
assembly (McGill et al. 2006; Shipley et al. 2006; Ackerly &
Cornwell 2007) and ecosystem functioning and services (Díaz
et al. 2007). Recent studies have shown global convergence in
leaf functional traits among species from diverse biomes. For
example, maximum photosynthetic rate, stomatal conductance,
and leaf area per unit mass are positively correlated, whereas
they are negatively correlated with leaf life span across a range
of sites and angiosperm taxa (Reich et al. 1997). Several
recent studies have shown that stem hydraulics is correlated
with leaf photosynthetic traits and photosynthetic water and
nutrient use efficiencies (Brodribb & Feild 2000; Santiago
et al. 2004; Ishida et al. 2008). Leaf hydraulic conductivity is
also found to be correlated with the development of leaf
mesophyll and stomata area index (Sack et al. 2003; Sack &
Frole 2006), both of which influence photosynthesis as the
mesophyll structure affects light harvesting and transmission
and CO2 diffusion within leaves and the stomata geometry
affects gas exchange between air and leaves. However,
whether the hydraulic capacity of leaf-supporting stems
influences leaf anatomy is poorly known.
Dipterocarpaceae is the most important tree family both
ecologically and commercially in Asian tropical forests. The
species of this family occur in tropical wet and seasonal
rainforests, heath and peat swamp forests, and some occur as
far north as the Tropic of Cancer in southern China (Ashton
1964; Appanah & Turnbull 1998; Cao 2000). They vary
greatly in stature, with species from the genera Shorea and
Hopea usually being tall emergent and upper canopy components whereas those from the genera Vatica and Dipterocarpus
being short-statured components of Asian tropical forests.
Dipterocarps also vary largely in light requirement with the
majority being shade-tolerant but a large number being
light-demanding (Appanah & Turnbull 1998). However,
information on the functional traits particularly hydraulic
properties of this prominent family is scarce.
In this study, we characterized stem xylem structural
properties, hydraulic conductivity, leaf functional traits, and
plant growth rates in 17 dipterocarp tree species grown in a
mature plantation stand, which were introduced from southern China and adjacent tropical countries. Since these plants
were grown in a common garden with the same environment,
the differences in plant traits and growth across species can be
attributed to inherited adaptive responses of the plants
(Monson 1996). We attempted to answer two questions: (i)
how do leaf functional traits, stem hydraulics, and stem diameter
and height growth rates vary among these dipterocarp
species? (ii) Is stem hydraulics correlated with leaf structural
and functional traits and growth rates? This study could provide
important information on the functional association between
stems and leaves, the ecology of dipterocarps, the mechanism
of their co-existence and functioning in tropical forest
ecosystems, and their use for reforestation.
Methods
STUDY SITE AND SPECIES
This study was conducted in the dipterocarp plantation stand at
Xishuangbanna Tropical Botanical Garden (21 °41′ N, 101°25′ E,
altitude 570 m) in southern Yunnan Province, China. The garden is
surrounded by the Luosuo River, a tributary of the upper Mekong
River. Mean annual temperature is 21·7 ° C and mean annual
precipitation is 1560 mm with 80% occurring from May to October.
A distinct dry period lasts from November to April. The soil of the
stand is sandy alluvium, containing 0·875 mg g–1 N, 0·329 mg g–1 P
and 9·693 mg g–1 K at 0–20 cm depth.
Since 1980s, seeds of about 40 dipterocarp species from southeastern
Asia including southern China have been collected and germinated
to seedlings in the botanical garden. The 1-year-old seedlings of
these species were planted in a common stand of about 7 ha, with a
density of about 1100 trees per ha. Seventeen dipterocarp species
(Table 1) from this stand were selected for the study based on the
following criteria: (i) whether they originated from China and adjacent
countries (11 species from southern China, one species from northern
Vietnam and five species from Thailand; Fig. 1); (ii) whether they
grew near paths to allow access to the canopy; and (iii) whether they
were sun-exposed and not overtopped by neighbouring trees. These
species belong to 6 genera, that is, Anisoptera (1 species), Dipterocarpus
(5 species), Hopea (4 species), Parashorea (1 species), Shorea (3 species)
and Vatica (3 species). At the generic level, Hopea, Shorea and
Parashorea are phylogenetically closely related (see Fig. S1 in
Supporting Information). Among the study species, 16 species are
evergreen species whereas Dipterocarpus tuberculatus is a deciduous
species with a leafless period of 1·5 months from February to March.
All study species are deep-rooted emergent or canopy layer components
in primary forests. In 2005 the ages of the sampled trees were 12–24
years, the heights were 9–29 m, and the diameters at breast height
(1·3 m height d.b.h.) were 10·5–47·8 cm.
STEM HYDRAULIC CONDUCTIVITY AND ANATOMICAL
PROPERTIES
In the rainy season of 2005, four to six sun-exposed terminal
branches from three to four trees per species were excised from the
upper canopy in the morning. They were re-cut in water and transported
to the laboratory to determine maximum hydraulic conductivity (kh)
following the method described by Santiago et al. (2004). De-ionized
water under a pressure of 0·2 MPa was pumped through a 30-cm-long
shoot segment for 15–20 min to remove embolisms, then kh was
measured as the water flow rate through the shoot segment under a
low gravitational pressure (5 kPa) generated by a hydraulic head of
50 cm (Sperry et al. 1988). Maximum stem sapwood specific conductivity (kS) was calculated as the ratio of kh to the cross-sectional
area of the sapwood. Sapwood thickness of a stem segment was
determined using a dye solution after the measurement of kh. Maximum
leaf specific hydraulic conductivity (kL) was calculated as the ratio of
© 2009 The Authors. Journal compilation © 2009 British Ecological Society, Functional Ecology, 23, 658– 667
660
J.-L. Zhang & K.-F. Cao
Table 1. The age, height and diameter at breast height (d.b.h.) of the sampled trees, and the maximum height of the 17 dipterocarp species
Species
Anisoptera costata Korth.
Dipterocarpus alatus Roxb. ex G. Don
D. intricatus Dyer
D. retusus Bl.
D. tuberculatus Roxb.
D. turbinatus Gaertn. f.
Hopea chinensis Hand.-Mazz.
H. hainanensis Merr. et Chun
H. hongayensis Tard.-Blot.
H. mollissima C.Y. Wu
Parashorea chinensis Wang Hsie
Shorea assamica Dyer
S. robusta Gaertn. f.
S. spp.
Vatica guangxiensis X.L. Mo
V. mangachapoi Bl.
V. xishuangbannaensis
G.D. Tao et J.H. Zhang
Species
code
Age
(years)
Height of
sampled trees (m)
D.b.h. of
sampled trees (cm)
Maximum
height (m)
Ac
Da
Di
Dr
Dtb
Dtr
Hc
Hha
Hho
Hm
Pc
Sa
Sr
Ss
Vg
Vm
Vx
13
24
24
18
24
16
12
17
15
24
20
14
15
24
13
16
20
18·1 ± 0·4
29·4 ± 0·7
18·1 ± 1·0
19·0 ± 1·1
23·3 ± 1·4
17·7 ± 0·7
9·2 ± 0·6
17·3 ± 0·5
13·0 ± 0·3
11·7 ± 0·2
16·8 ± 0·5
8·7 ± 0·5
14·3 ± 0·4
16·1 ± 1·2
10·1 ± 1·0
9·3 ± 0·7
16·5 ± 1·0
25·7 ± 1·1
47·8 ± 5·2
26·8 ± 2·2
22·0 ± 1·8
30·2 ± 2·9
23·1 ± 2·0
10·5 ± 0·4
20·9 ± 0·7
13·4 ± 1·0
17·6 ± 3·4
17·6 ± 0·9
22·4 ± 1·2
20·6 ± 0·6
24·4 ± 2·8
11·2 ± 1·0
11·2 ± 1·0
19·7 ± 1·4
40
45
30
45
25
35
20
20
30
30
60
50
40
30
40
20
40
Nomenclature and maximum height of the species follow the Flora of China (Tong & Tao 1990) and Flora of Vietnam (Ho 1999). Data are
means ± SE, N = 10.
between the species in this study. Certainly, care should be taken
when comparing values of kS and kL presented here with those measured
using different methods in other studies.
After the hydraulic measurement, the fresh volume of a small
sapwood sample was measured by displacement of water and then
the sapwood was dried at 80 °C for 48 h to calculate sapwood
density. Some sapwood samples were stored in 1 : 1 (v/v)
ethanol : glycerol for 2 months and then transverse sections of about
5 μm thickness were made with a microtome. Vessel anatomy was
examined with the aid of a microscope. The number and diameters
of vessels in a field were measured under 10 × and 40 × objectives
calibrated with an ocular micrometer. Vessels of the dipterocarp
species examined were elliptical (see Fig. 2) and thus average vessel
diameter in a field was calculated according to the method described
by Becker et al. (2003).
Fig. 1. The location of the study site (solid black circle) and the sites
(open stars) where the 17 dipterocarp species were collected. XTBG:
Xishuangbanna Tropical Botanical Garden (21°41′ N, 101°25′ E); I:
Bangkok (13°45′, 100°30′); II: Yingjiang (24°52′, 97°55′), Yunnan;
III: Mengla (21°25′, 101°32′), Yunnan; IV: Hekou (22°32′, 103°57′),
Yunnan; V: North Vietnam (22°00′, 105°25′); VI: Napo (23°22′,
105°52′), Guangxi: VII: Shangsi (22°10′, 108°00′), Guangxi; VIII:
Jianfengling (18°40′, 108°49′), Hainan island. See the species codes in
Table 1.
kh to the total leaf area distal to the stem. Leaf area was measured
using a portable leaf area meter (LI-3000A, Li-Cor, Lincoln, NE).
Because shoot morphology varies largely among the study species,
the 30-cm-long shoot segment was used for the hydraulic conductivity
measurement for all species to facilitate the comparison. Although
these stem segments may contain some open vessels (cf. Brodribb &
Holbrook 2003; maximum vessel length of some tropical rainforest
tree species ranged from 15 to 35 cm), our measurements on the
hydraulic conductivity should provide a good basis for comparison
LEAF ANATOMY
Thickness of leaf, upper and lower epidermis, and palisade and
spongy mesophylls were measured on transverse sections of leaves
using the light microscope. The ratio of palisade to spongy mesophyll
thickness was calculated. Stomatal density and guard cell length on
abaxial surfaces of leaves were measured from the epidermal impressions made with colourless nail polish. Stomatal pore area index was
calculated as SPI = stomatal density × guard cell length2 (Sack et al.
2003). Six leaves from 4–6 plants per species were used and at least
three fields of each leaf were observed. We observed that all study
species had heterobaric leaves, that is, with bundle sheath extensions
(Kenzo et al. 2007).
GAS EXCHANGE AND WATER STATUS
In the rainy season, we accessed the upper canopies of the trees using
a crane mounted on a truck. Between 08.30 and 11.00 h area-based
© 2009 The Authors. Journal compilation © 2009 British Ecological Society, Functional Ecology, 23, 658–667
Stem hydraulics and leaf functional traits 661
Fig. 2. Microscopy images of transverse
sections of stem xylem for (a) Dipterocarpus
retusus, (b) Hopea hongayensis, (c) H. mollissima and (d) Shorea assamica, as examples
of xylem anatomy for dipterocarps. Scale
bar = 100 μm.
maximum photosynthetic capacity (Aa) and stomatal conductance (gs) were measured from 3 to 4 sunlit canopy leaves from each
branch of 4–6 plants per species using a portable photosynthetic gas
exchange system (LI-6400, Li-Cor). Prior to the measurements,
leaves were fully induced by sunlight or by an artificial light with
photosynthetic photon flux density of 1500 μmol m–2 s–1 for 10 min
provided by a LED light source. CO2 concentration inside the leaf
chamber was maintained at 380 μmol mol –1 through the CO 2
controlling system of the gas analyzer with attachment of a tiny CO2
cylinder. During the measurements inside the leaf chamber the
relative air humidity was 47–54%, leaf-to-air vapor pressure deficit
was 1·5–2·0 kPa, and leaf temperature was 27–30 °C. The intrinsic
photosynthetic water use efficiency (WUE) was calculated as Aa/gs.
The average from the repeated measurements of each plant was used
to represent the gas exchange value for one plant.
At midday on clear days in the rainy season, three to seven
fully-expanded sunlit leaves from four to five sampled trees per
species were collected from the upper canopies reached by the crane
and then midday leaf water potentials (Ψmd) were measured using a
pressure chamber (SKPM 1400, Skye Instruments, Powys, UK).
LMA AND FOLIAR CHLOROPHYLL AND NUTRIENT
CONCENTRATIONS
After the gas exchange measurements the measured leaves were
harvested and each leaf was cut into two parts along the midrib. One
half of the leaf was used to measure chlorophyll concentration using
80% acetone according to Johnston et al. (1984). The projection area
of the other half was measured with the leaf area meter (LI-3000A,
Li-Cor), and then the leaves were dried at 80 °C for 48 h to determine
the leaf mass per unit area (LMA). Leaf density was calculated as
LMA/leaf thickness.
The remaining harvested leaves were used to determine foliar
concentrations of N, P and K. Total N concentration was determined
using an auto Kjeldahl unit (K370, BÜCHI Labortechnik AG,
Flawil, Switzerland) after the leaf samples were digested with
concentrated H2SO4. Total foliar P and K concentrations were
analysed using an inductively coupled plasma atomic-emission
spectrometer (IRIS Advantage-ER, Thermo Jarrell Ash Corporation,
MA) after the samples were digested with concentrated HNO3–HClO4.
Photosynthetic N (PNUE) and P use efficiencies (PPUE) were
calculated as the ratio of mass-based maximum photosynthetic
capacity (Am) to foliar N and P concentrations, respectively.
GROWTH RATES
Height from ground to tree tops and d.b.h. of ten individuals per
species were measured with tapes. Average height (HGR) and diameter
growth rates (DGR) were calculated by dividing height and d.b.h. by
tree age.
STATISTICAL ANALYSIS
Relationships between stem hydraulics, leaf-level traits, and plant
growth rates were analysed with Pearson’s correlation. The associations between 37 plant traits listed in Table 2 and between the dipterocarp
species studied were tested by a detrended correspondence analysis
(DCA) using DECORANA function in R (R v. 2·6·2; The R Foundation for Statistical Computing, Vienna, Austria). Some traits (e.g.
ratio of palisade to spongy mesophyll, layers of palisade) deviated
significantly from the normal distribution (Shapiro-Wilk W test),
even after they were log-transformed. Therefore, for our data DCA
was more suitable than principle component analysis (Hill 1979).
Results
The dipterocarp species varied largely in wood and leaf traits
(Table 2; see Fig. 2 for xylem anatomy). For example, sapwood
density varied 1·9-fold among species (0·342–0·655 g cm–3),
kL 4·5-fold (3·1–13·9 × 10–4 kg m–1 s–1 MPa–1), LMA 2·9-fold
(52–152 g m–2), mass-based N concentration (Nm) 1·7-fold
© 2009 The Authors. Journal compilation © 2009 British Ecological Society, Functional Ecology, 23, 658– 667
662
J.-L. Zhang & K.-F. Cao
Table 2. Summary of traits used in this study
Group, trait
Wood and xylem
Vessel density
Vessel diameter
Sapwood density
Maximum sapwood specific hydraulic conductivity
Maximum leaf specific hydraulic conductivity
Ratio of leaf area to sapwood area
Leaf anatomy and morphology
Leaf thickness
Thickness of upper epidermis
Thickness of palisade mesophyll
Thickness of spongy mesophyll
Mesophyll thickness (= TP + TS)
Thickness of lower epidermis
Ratio of palisade to spongy mesophyll
Layer of palisade mesophyll
Stomatal density
Guard cell length
Stomatal pore area index (= SD × GCL2)
Leaf mass per unit area
Leaf density
Leaf nutrients
Mass-based N concentration
Mass-based P concentration
Mass-based K concentration
Area-based N concentration
Area -based P concentration
Area -based K concentration
Ratio of N to P concentration
Chlorophyll
Mass-based chlorophyll concentration
Area-based chlorophyll concentration
Ratio of chlorophyll a/b
Leaf water potential
Midday leaf water potential in the rainy season
Gas exchange and leaf function
Stomatal conductance
Area-based maximum photosynthetic rate
Mass-based maximum photosynthetic rate
Photosynthetic N use efficiency
Photosynthetic P use efficiency
Photosynthetic water use efficiency
Growth
Mean annual height growth rate
Mean annual diameter growth rate
Code
Unit
Vde
Vdi
WD
kS
kL
L/S
no. mm–2
μm
g cm–3
kg m–1 s–1 MPa–1
×10–4 kg m–1 s–1 MPa–1
m2 cm–2
LT
TC
TP
TS
MT
TL
P/S
LP
SD
GCL
SPI
LMA
LD
μm
μm
μm
μm
μm
μm
no.
no. mm–2
μm
g m–2
kg m–3
Mean
Coefficient of
variation (%)
70·0
66·1
0·543
8·87
8·57
1·21
48
28
16
39
45
28
190
23·7
61·3
88·5
150
16·5
0·798
1·647
470
18·7
0·166
90·4
484
27
39
29
35
27
40
55
48
35
13
44
27
19
Nm
Pm
Km
Na
Pa
Ka
N/P
mg g–1
mg g–1
mg g–1
g m–2
g m–2
g m–2
19·7
1·22
5·59
1·75
0·109
0·493
16·3
12
16
25
24
27
31
10
Chm
Cha
a/b
mg g–1
μg cm–2
5·50
47·8
2·34
27
25
14
Ψmd
MPa
–0·611
37
gs
Aa
Am
PNUE
PPUE
WUE
mol m–2 s–1
μmol m–2 s–1
nmol g–1 s–1
μmol mol–1 s–1
mmol mol–1 s–1
μmol mol–1
0·233
11·7
132
93·5
3·26
52·5
50
39
33
28
28
17
HGR
DGR
m year–1
cm year–1
0·879
1·21
26
32
(16·2–26·8 mg g –1), g s 6·5-fold (0·085–0·558 mol m–2 s –1),
Aa 3·9-fold (5·1–20·3 μmol m–2 s–1), PNUE 2·5-fold (54–
135 μmol mol–1 s–1), HGR 2·9-fold (0·49–1·39 m y–1), and
DGR 2·9-fold (0·70–1·99 cm y–1) (see Table S1).
Stem hydraulic conductivity was highly correlated with
vessel diameter (Fig. 3) and also correlated with a suite of leaf
traits among species (see Table S2). Specifically, both kS and
kL were positively correlated with Ψmd in the rainy season
(Fig. 4b), gs (Fig. 4 c), Aa (Fig. 4d), PNUE (Fig. 4e), and
PPUE (Fig. 4f ). Moreover, both kS and kL were positively
correlated with HGR (Fig. 4g) and DGR (Fig. 4h), with
stronger correlation with DGR than with HGR. Stem kS was
negatively correlated with WUE, and k L was positively
correlated with thickness of mesophyll (Fig. 4a) and lamina,
and Am (see Table S2). Stem hydraulic conductivity was not
significantly correlated with LMA and stomatal density or
SPI (see Table S2). Wood density was not significantly correlated
with hydraulic conductivity, vessel diameter and density, and
growth rates.
Interestingly, several traits were correlated with maximum
height (Hmax) of the species as reported in literature, such as kS
(r = 0·52, P < 0·05), WUE (r = −0·73, P < 0·001), thickness
of spongy mesophyll (r = −0·55, P < 0·05), and the ratio of
palisade to spongy mesophyll thickness (r = 0·66, P < 0·01).
© 2009 The Authors. Journal compilation © 2009 British Ecological Society, Functional Ecology, 23, 658–667
Stem hydraulics and leaf functional traits 663
Fig. 3. Correlation between maximum sapwood specific hydraulic
conductivity (kS) and vessel diameter across the 17 dipterocarp
species. Species symbols: , Anisoptera costata; , Dipterocarpus
alatus; ▼, D. intricatus; , D. retusus; , D. tuberculatus; , D.
turbinatus; , Hopea chinensis; , H. hainanensis; ⊕, H. hongayensis;
, H. mollissima; , Parashorea chinensis; , Shorea assamica; ,
S. robusta; , S. spp; , Vatica guangxiensis; , V. mangachapoi; ,
V. xishuangbannaensis. ***P < 0·001.
The associations between stem xylem anatomical properties,
hydraulic conductivity, leaf-level traits, and plant growth
rates were further analysed using DCA (Fig. 5a). The first
axis of the DCA reflects the continuum in hydraulic conductivity vs. vessel density. The negative side of the axis represents
the species with high hydraulic conductivity, which was
characterized by large vessels, high kS, kL, Ψmd, gs, Aa, thick
mesophyll, and rapid growth rates. The positive side of the
axis indicates the species with small diameter vessels, dense
vessel packing, and high sapwood density. In other words, the
first DCA axis was correlated with traits related to stem
hydraulics and leaf carbon gain. The second axis of the DCA
represents species possessing leaves with high chlorophyll
concentration, larger palisade to spongy mesophyll ratio and
low LMA on the positive side, which are related to light
harvesting and interception. Congeners from Shorea, Dipterocarpus, Hopea and Vatica were scattered fairly close
together in the DCA diagram (Fig. 5b).
Discussion
With increasing leaf thickness, area-based N, P, K, and
chlorophyll concentrations increased (see Table S2). There
were positive correlations between gs and Aa, Am, PNUE, and
PPUE. With increasing LMA, Nm and mass-based chlorophyll
concentration decreased. Both HGR and DGR were positively
correlated with Nm, Aa, Am, PNUE and PPUE.
The present study showed that stem hydraulic conductivity of
dipterocarps is correlated with a large suite of leaf structural
and functional traits such as leaf mesophyll thickness,
maximum photosynthetic gas exchange rates, and photosynthetic water (negative) and nutrient use efficiencies (positive)
(Fig. 4; see Table S2). Several previous studies have also
Fig. 4. Correlations between maximum
leaf specific hydraulic conductivity (kL)
and: (a) mesophyll thickness (MT); (b)
midday leaf water potential (Ψ md) in the
rainy season; (c) maximum stomatal conductance (g s); (d) area-based maximum
photosynthetic rate (Aa); (e) photosynthetic
N use efficiency (PNUE); (f) photosynthetic
P use efficiency (PPUE); (g) height growth
rate (HGR); and (h) diameter growth rate
(DGR) across the 17 dipterocarp species.
The symbols for the species are noted in
Fig. 3. *P < 0·05; **P < 0·01, ***P < 0·001.
© 2009 The Authors. Journal compilation © 2009 British Ecological Society, Functional Ecology, 23, 658– 667
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J.-L. Zhang & K.-F. Cao
Fig. 5. Detrended correspondence analysis (DCA) using mean
values of plant traits across 17 dipterocarp tree species. Plant trait (a)
and species (b) loadings on the first and second axes. See the
explanations of the trait abbreviations in Table 2 and the species
codes in Table 1.
shown the correlation between stem hydraulic conductivity
and leaf photosynthetic capacity (Brodribb & Feild 2000;
Santiago et al. 2004; Ishida et al. 2008). This relationship is
likely mediated through stomatal regulation (Meinzer &
Grantz 1991; Brodribb & Feild 2000; Hubbard et al. 2001)
to balance transpiration, photosynthesis, and hydraulic
dysfunction. Although the leaf is a major bottle-neck in the
whole plant hydraulic conductivity (Sack et al. 2003), stomatal
regulation links stem and leaf hydraulic systems. Under optimal
soil water supply, high stem hydraulic conductivity allows
quick water transport from stems into leaves to compensate
leaf transpiration water loss and consequently maintain high
daily water potential (Meinzer 2003; Ackerly 2004; Santiago
et al. 2004). High daily leaf water potential mitigates the
stomatal limitation to gas exchange, especially during the
midday when the transpiration demand is high, and thus
increase daily carbon assimilation. Maintenance of high leaf
water potential should also contribute to maintaining a high
cell turgor, and thus benefit the plant cell expansion and tree
growth (Koch et al. 2004; Woodruff et al. 2004). Therefore, an
efficient water supply to the upper canopy could buffer the
high xylem tension in tall trees. This mechanism is also considered to support the theory of hydraulic limitation to tree
height (Ryan & Yoder 1997), and could explain the positive
correlation between ks and maximum tree height found in the
present study.
The link between photosynthetic capacity and stem or leaf
hydraulic conductivity seems obvious because stem and leaf
hydraulic systems carry water to replace the water lost in the
leaves during photosynthetic gas exchange (Brodribb & Feild
2000; Brodribb et al. 2002). However, both stem hydraulic
traits and maximum photosynthetic rates are adapted to
long-term circumstances and the physiological mechanisms
explaining the coordination between these two systems and
the involvement of nutrient supply in this process are poorly
understood. Our results provide a better insight into the
coordination between hydraulic and photosynthetic traits in
terms of nutrient supply and nutrient use efficiency. Higher
nutrient availability or addition of nutrients has been found to
enhance water transport efficiency and carbon assimilation
rates in Neotropical savanna trees (Bucci et al. 2006). When
soil nutrients are comparable, species with higher photosynthetic nutrient use efficiency will enhance development of
hydraulic and photosynthetic systems, resulting in higher
growth rates and probably higher maximum tree height.
However, better water supply leads to a luxurious use of water
and hence a low WUE. Consistent with the present study,
other studies have also reported such a trade-off between
photosynthetic nutrient and water use efficiency (Santiago
et al. 2004; Cai et al. 2007).
The positive correlation of stem hydraulics with leaf or
mesophyll thickness (Fig. 4a) might be partly due to the
functional linkage with the leaf vascular system. For example,
species with thick mesophyll have dense veins (Sack & Frole
2006). As discussed above, efficient water transportation in
stems and leaves allows the maintenance of high leaf water
potential and leaf turgor which benefits mesophyll development. Increased nutrient use efficiency with increasing stem
hydraulic conductivity may also help mesophyll cell expansion and growth. Moreover, the dipterocarp species of the
present study all possess heterobaric leaves, that is, with
extended bundle sheath (Kenzo et al. 2007). Therefore, their
leaf thickness is approximately the width of the vascular
bundles. Dense veins and wide vascular bundles of the leaves
allow the rapid diffusion of water and nutrients within
leaves (Sack & Frole 2006), which coincides with the positive
correlation between stem hydraulic conductivity and nutrient
use efficiency.
The large variation in functional traits, including photosynthesis and hydraulics, across the dipterocarp species
studied (Table 2) is consistent with the established knowledge
on the wide ecological adaptations of dipterocarps (Ashton
1964). The range in wood density of the present dipterocarp
species was relatively narrow, whereas photosynthetic gas
exchange rates and stem hydraulic conductivity varied widely
among species (see Table S1). This is in agreement with the
wide variation in vessel traits and a relatively narrow range of
wood density in 51 Californian angiosperm woody species
(Preston et al. 2006). In addition, these authors have found
that vessel traits were related to Hmax of the species. Although
© 2009 The Authors. Journal compilation © 2009 British Ecological Society, Functional Ecology, 23, 658–667
Stem hydraulics and leaf functional traits 665
the dipterocarp species of the present study originated from
different regions, their performance in a common environment
may discern their inherited differences in adaptations to the
environment, and in growth rate and resource use. The Hmax in
their native habitats was positively correlated with kS and
negatively with WUE, implying the importance of hydraulic
traits in relation to tree Hmax (Ryan & Yoder 1997; Koch et al.
2004; Woodruff et al. 2004). It was also positively correlated
with the ratio of palisade to spongy mesophyll thickness and
negatively with thickness of spongy mesophyll. High kS, a
large ratio of palisade to spongy mesophyll and lower WUE
are usually characteristics of light-demanding tree species
(Swaine & Whitmore 1988). Our results therefore also support
the idea that Hmax of tropical forest trees is a light capture
adaptation (Thomas 1996), suggesting a mechanistic link
between light capture characteristics and hydraulic traits
(Campanello et al. 2008). Vatica xishuangbannaensis, a relatively
short dipterocarp species, had relatively lower photosynthesis
and growth rate (see Table S1), and is a typical shade-tolerant
species (Zhu 2000). It is also relatively drought-tolerant as it
occurs on relatively dry upper slopes (Zhu 2000). However,
being the tallest species in this study, Parashorea chinensis is
also shade-tolerant. Its seedlings can grow and survive in the
shaded forest understorey though they grow much better in
high irradiance sites such as canopy gaps and secondary forest
stands (Zhu 2000; Tang 2008). Fast-growing species have a
better capability of adjusting tree hydraulics to different light
regimes (Campanello et al. 2008) and P. chinensis may be an
example of the fast-growing species with large plasticity in
hydraulic traits.
In the present study wood density of terminal branches was
not significantly correlated with hydraulic conductivity, vessel
diameter and vessel density (see Table S2). This supports the
idea that wood density and vessel traits are two distinct
ecological axes (Preston et al. 2006). Wood density of
angiosperms is largely determined by wall thickness of vessels
and density of fibre cells and therefore strongly related to the
mechanical strength and capacity to prevent vessel implosion
induced by the pressure gradient between actively conducting
and embolized vessels (Hacke et al. 2001). Hydraulic conductivity of stems, on the other hand, is largely determined by
vessel size and density (James et al. 2003). Hydraulically,
wood density is inversely correlated to water storage capacity
(Bucci et al. 2004; Scholz et al. 2007; Meinzer et al. 2008). In
dry ecosystems like Brazilian savanna, high water storage
capacity provides a better buffering to the water transport
system and consequently would allow high water transport
efficiency indicated by high kS (Bucci et al. 2004; Scholz et al.
2007). This indirect correlation between wood density and
hydraulic conductivity, however, may not show up in environments with optimal soil water supply because of the relatively
lower demand on the stored water in buffering seasonal and
daily water deficits. Wood density of the terminal branches
was not significantly correlated with mean diameter or height
growth rates (see Table S2). This is in contrast with the trade-off
between allocation of biomass to tissue density and growth
rate suggested by an allometric model (Enquist et al. 2000),
and the finding of a significant inverse relationship between
mean diameter growth and wood density among woody species
in primary tropical rain forests (King et al. 2006). In our case,
the ages of the terminal branches were only 1–2 years whereas
the growth rates were averaged over past 12–24 years, which
could obscure the correlation between them. Nevertheless,
both diameter and height growth rates of the dipterocarps
were positively correlated with vessel diameter, while height
growth rate was negatively correlated with vessel density (see
Table S2). It appears that the vessel size and density which are
determined by cambium growth and related to hydraulic
conductivity regulate the diameter growth rate. The relationship
between height growth and vessel diameter and density probably
reflects the allometric relationship between cambium growth
and apical meristematic growth.
A trade-off for the species with high stem hydraulic conductivity, as in those with tall stature, is the low photosynthetic
water use efficiency (see Table S2) which could limit these
plants to establish successfully in dry habitats. This trade-off
as well as the trade-off between photosynthetic nutrient and
water use efficiencies discussed above combined with the large
variation in functional traits and growth rates could allow niche
differentiation among the dipterocarp species and consequently their co-existence in a forest community or a landscape
with heterogeneous environments (Meinzer 2003).
The DCA results (Fig. 5a) revealed that light harvesting of
leaves (i.e. chlorophyll concentration) is a distinct ecological
axis, and was mainly regulated by leaf structure, for example,
LMA (also see Poorter & Evans 1998; Cao 2000), among the
dipterocarp species. Because hydraulic conductivity may
affect the development of leaf mesophylls as mentioned
above, it is likely that there is an indirect relationship between
light harvesting and water transport capacity of plant. The
irradiance over the canopy leaves of tropical forests is usually
intense and particularly so in the dry season; therefore, it is
important to optimize light harvesting to balance the light
energy used for photosynthesis and surplus energy that may
induce photoinhibition.
On the DCA diagram, the cogeneric species were packed
fairly close together, with species from Vatica scattered at the
opposite end of the scatter plot in comparison with Dipterocarpus
and Shorea (Fig. 5b). This spatial distribution of the dipterocarp
species in the DCA diagram corresponds to their positions in
the phylogenetic consensus tree constructed using chloroplast
DNA sequences (Kajita et al. 1998; Gamage et al. 2003; Li
et al. 2004; also see Fig. S1). These results suggest that stem
hydraulic characteristics and their association with leaf functional traits and plant growth are phylogenetically conserved.
Phylogenetic conservatism of hydraulic properties has also
been reported by other studies (Preston et al. 2006; Hao et al.
2008; Willson et al. 2008), indicating large evolutionary constraints on the changes in these traits.
Acknowledgements
We thank two anonymous referees, our colleagues J.W. F. Slik, G.-Y. Hao, and
Y.-J. Zhang for their helpful comments on our manuscript. The Biogeochemistry
© 2009 The Authors. Journal compilation © 2009 British Ecological Society, Functional Ecology, 23, 658– 667
666
J.-L. Zhang & K.-F. Cao
Laboratory of our botanical garden made the analyses of soil and foliar nutrient
concentrations of the present study. This study was financially supported by the
National Natural Science Foundation of China (grant No. 90302013).
References
Ackerly, D.D. (2004) Functional strategies of chaparral shrubs in relation to
seasonal water deficit and disturbance. Ecological Monographs, 74, 25–44.
Ackerly, D.D. & Cornwell, W.K. (2007) A trait-based approach to community
assembly: partitioning of species trait values into within- and amongcommunity components. Ecology Letters, 10, 135–145.
Appanah, S. & Turnbull, J.M. (1998) A Review of Dipterocarps: Taxonomy,
Ecology and Silviculture. Center for International Forestry Research, Bogor,
Indonesia.
Ashton, P.S. (1964) Manual of the Dipterocarp Trees of Brunei State. Oxford
University Press, Oxford, UK.
Becker, P., Gribben, R.J. & Schulte, P.J. (2003) Incorporation of transfer resistance
between tracheary elements into hydraulic resistance models for tapered
conduits. Tree Physiology, 23, 1009–1019.
Brodribb, T.J. & Feild, T.S. (2000) Stem hydraulic supply is linked to leaf
photosynthetic capacity: evidence from New Caledonian and Tasmanian
rainforests. Plant, Cell and Environment, 23, 1381–1388.
Brodribb, T.J. & Hill, R.S. (1999) The importance of xylem constraints in the
distribution of conifer species. New Phytologist, 143, 365–372.
Brodribb, T.J. & Hill, R.S. (2000) Increases in water potential gradient reduce
xylem conductivity in whole plants. Evidence from a low-pressure conductivity
method. Plant Physiology, 123, 1021–1028.
Brodribb, T.J. & Holbrook, N.M. (2003) Changes in leaf hydraulic conductance
during leaf shedding in seasonally dry tropical forest. New Phytologist, 158,
295–303.
Brodribb, T.J., Holbrook, N.M. & Gutiérrez, M.V. (2002) Hydraulic and
photosynthetic co-ordination in seasonally dry tropical forest trees. Plant,
Cell and Environment, 25, 1435–1444.
Bucci, S.J., Goldstein, G., Meinzer, F.C., Scholz, F.G., Franco, A.C. & Bustamante, M. (2004) Functional convergence in hydraulic architecture and
water relations of tropical savanna trees: from leaf to whole plant. Tree
Physiology, 24, 891–899.
Bucci, S.J., Scholz, F.G., Goldstein, G., Meinzer, F.C., Franco, A.C., Campanello,
P.I., Villalobos-Vega, R., Bustamante, M. & Miralles-Wilhelm, F. (2006)
Nutrient availability constrains the hydraulic architecture and water relations of
savannah trees. Plant, Cell and Environment, 29, 2153–2167.
Cai, Z.-Q., Poorter, L., Cao, K.-F., Bongers, F. (2007) Seedling growth strategies in Bauhinia species: comparing lianas and trees. Annals of Botany, 100,
831–838.
Campanello, P.I., Gatti, M.G., Goldstein, G. (2008) Coordination between
water-transport efficiency and photosynthetic capacity in canopy tree species at different growth irradiances. Tree Physiology, 28, 85–93.
Cao, K.-F. (2000) Leaf anatomy and chlorophyll content of 12 woody species in
contrasting light conditions in a Bornean heath forest. Canadian Journal of
Botany, 78, 1245–1253.
Castro-Díez, P., Puyravaud, J.P., Cornelissen, J.H.C. & Villar-Salvador, P.
(1998) Stem anatomy and relative growth rate in seedlings of a wide range of
woody plant species and types. Oecologia, 116, 57–66.
Díaz, S., Lavorel, S., de Bello, F., Quétier, F., Grigulis, K. & Robson, T.M.
(2007) Incorporating plant functional diversity effects in ecosystem service
assessments. Proceedings of the National Academy of Sciences USA, 104,
20684–20689.
Engelbrecht, B.M.J., Comita, L.S., Condit, R., Kursar, T.A., Tyree, M.T.,
Turner, B.L. & Hubbell, S.P. (2007) Drought sensitivity shapes species distribution patterns in tropical forests. Nature, 447, 80–83.
Enquist, B.J., West, G.B. & Brown, J.H. (2000) Quarter-power allometric scaling in vascular plants: functional basis and ecological consequences. Scaling
in Biology (eds J.H. Brown & G.B. West), pp. 167–198. Oxford University
Press, Oxford, UK.
Gamage, D.T., de Silva, M., Yoshida, A., Szmidt, A.E. & Yamazaki, T. (2003)
Molecular phylogeny of Sri Lankan Dipterocarpaceae in relation to other
Asian Dipterocarpaceae based on chloroplast DNA sequences. Tropics, 13,
79–87.
Hacke, U.G., Sperry, J.S., Pockman, W.T., Davis, S.D. & McCulloh, K.A.
(2001) Trends in wood density and structure are linked to the prevention of
xylem implosion by negative pressure. Oecologia, 126, 457–461.
Hao, G.-Y., Hoffmann, W.A., Scholz, F.G., Bucci, S.J., Meinzer, F.C., Franco, A.C.,
Cao, K.-F. & Goldstein, G. (2008) Stem and leaf hydraulics of congeneric
tree species from adjacent tropical savanna and forest ecosystems. Oecologia,
155, 405–415.
Hill, M.O. (1979) DECORANA–A FORTRAN program for detrended
correspondence analysis and reciprocal averaging. Cornell University, Ithaca, NY, USA.
Ho, P.H. (1999) An Illustrated Flora of Vietnam, 2nd edn. Tre Publishing
House, Vietnam (in Vietnamese).
Hubbard, R.M., Ryan, M.G., Stiller, V. & Sperry, J.S. (2001) Stomatal conductance and photosynthesis vary linearly with plant hydraulic conductance
in ponderosa pine. Plant, Cell and Environment, 24, 113–121.
Ishida, A., Nakano, T., Yazaki, K., Matsuki, S., Koike, N., Lauenstein, D.L.,
Shimizu, M. & Yamashita, N. (2008) Coordination between leaf and stem
traits related to leaf carbon gain and hydraulics across 32 drought-tolerant
angiosperms. Oecologia, 156, 193–202.
James, S.A., Meinzer, F.C., Goldstein, G., Woodruff, D., Jones, T., Restom, T.,
Mejia, M., Clearwater, M. & Campanello, P. (2003) Axial and radial water
transport and internal water storage in tropical forest canopy trees. Oecologia,
134, 37–45.
Johnston, M., Grof, C.P.L. & Brownell, P.F. (1984) Effect of sodium nutrient on
chlorophyll a/b ratios in C4 plants. Journal of Plant Physiology, 11, 325–332.
Kajita, T., Kamiya, K., Nakamura, K. Tachida, H., Wickneswari, R.,
Tsumura, Y., Yoshimaru, H. & Yamazaki, T. (1998) Molecular phylogeny of
Dipterocarpaceae in Southeast Asia based on nucleotide sequences of matK,
trnL intron, and trnL-trnF intergenic spacer region in chloroplast DNA.
Molecular Phylogenetics and Evolution, 10, 202–209.
Kenzo, T., Ichie, T., Watanabe, Y. & Hiromi, T. (2007) Ecological distribution
of homobaric and heterobaric leaves in tree species of Malaysian lowland
tropical rainforest. American Journal of Botany, 94, 764–775.
King, D.A., Davies, S.J., Tan, S. & Nur Supardi, M.N. (2006) The role of wood
density and stem support costs in the growth and mortality of tropical trees.
Journal of Ecology, 94, 670 –680.
Koch, G.W., Sillett, S.C., Jennings, G.M. & Davis, S.D. (2004) The limits to tree
height. Nature, 428, 851–854.
Li, Q.-M., He, T.-H. & Xu, Z.-F. (2004) Generic relationships of Parashorea
chinensis Wang Hsie (Dipterocarpaceae) based on cpDNA sequences.
Taxon, 53, 461–466.
McGill, B.J., Enquist, B.J., Weiher, E. & Westoby, M. (2006) Rebuilding
community ecology from functional traits. Trends in Ecology and Evolution,
21, 178–185.
Meinzer, F.C. (2003) Functional convergence in plant responses to the environment. Oecologia, 134, 1–11.
Meinzer, F.C. & Grantz, D.A. (1991) Coordination of stomatal, hydraulic, and
canopy boundary layer properties: do stomata balance conductances by
measuring transpiration? Physiologia Plantarum, 83, 324–329.
Meinzer, F.C., Woodruff, D.R., Domec, J.-C., Goldstein, G., Campanello, P.I.,
Gatti, M.G. & Villalobos-Vega, R. (2008) Coordination of leaf and stem
water transport properties in tropical forest trees. Oecologia, 156, 31–41.
Monson, R.K. (1996) The use of phylogenetic perspective in comparative plant
physiology and developmental biology. Annals of the Missouri Botanical
Garden, 83, 3–16.
Poorter, H. & Evans, J.R. (1998) Photosynthetic nitrogen-use efficiency of
species that differ inherently in specific leaf area. Oecologia, 116, 26–37.
Poorter, L. & Bongers, F. (2006) Leaf traits are good predictors of plant performance across 53 rain forest species. Ecology, 87, 1733–1743.
Preston, K.A., Cornwell, W.K. & DeNoyer, J.L. (2006) Wood density and
vessel traits as distinct correlates of ecological strategy in 51 California coast
range angiosperms. New Phytologist, 170, 807–818.
Reich, P.B., Walters, M.B. & Ellsworth, D.S. (1997) From tropics to tundra: global
convergence in plant functioning. Proceedings of the National Academy of
Sciences USA, 94, 13730–13734.
Ryan, M.G. & Yoder, B.J. (1997) Hydraulic limits to tree height and tree
growth. Bioscience, 47, 235–242.
Sack, L. & Frole, K. (2006) Leaf structural diversity is related to hydraulic
capacity in tropical rain forest trees. Ecology, 87, 483–491.
Sack, L., Cowan, P.D., Jaikumar, N. & Holbrook, N.M. (2003) The ‘hydrology’
of leaves: co-ordination of structure and function in temperate woody
species. Plant, Cell and Environment, 26, 1343–1356.
Santiago, L.S., Goldstein, G., Meinzer, F.C., Fisher, J.B., Machado, K., Woodruff,
D. & Jones, T. (2004) Leaf photosynthetic traits scale with hydraulic conductivity and wood density in Panamanian forest canopy trees. Oecologia,
140, 543–550.
Scholz, F.G., Bucci, S.J., Goldstein, G., Meinzer, F.C., Franco, A.C. &
Miralles-Wilhelm, F. (2007) Biophysical properties and functional significance of stem water storage tissues in Neotropical savanna trees. Plant, Cell
and Environment, 30, 236–248.
Shipley, B., Vile, D. & Garnier, É. (2006) From plant traits to plant communities: a statistical mechanistic approach to biodiversity. Science, 314,
812–814.
© 2009 The Authors. Journal compilation © 2009 British Ecological Society, Functional Ecology, 23, 658–667
Stem hydraulics and leaf functional traits 667
Sperry, J.S., Donnelly, J.R. & Tyree, M.T. (1988) A method for measuring
hydraulic conductivity and embolism in xylem. Plant, Cell and Environment
11, 35–40.
Swaine, M.D. & Whitmore, T.C. (1988) On the definition of ecological species
groups in tropical rain forests. Vegetatio, 75, 81–86.
Tang, J.-W. (2008) A study on the population ecology of Parashorea chinensis in
Xishuangbanna, SW China. PhD thesis, Graduate School of Chinese Academy
of Sciences, Beijing, China (in Chinese with English abstract).
Thomas, S.C. (1996) Asymptotic height as a predictor of growth and allometric
characteristics in Malaysian rain forest trees. American Journal of Botany,
83, 556–566.
Tong, S.Q. & Tao, G.D. (1990) Dipterocarpaceae. Flora Reipublicae Popularis
Sinicae (ed. H.W. Li), vol. 50 (2), pp. 113–131. Science Press, Beijing, China
(in Chinese).
West, G.B., Brown, J.H. & Enquist, B.J. (1999) A general model for the structure
and allometry of plant vascular systems. Nature, 400, 664–667.
Willson, C.J., Manos, P.S. & Jackson, R.B. (2008) Hydraulic traits are influenced
by phylogenetic history in the drought-resistant, invasive genus Juniperus
(Cupressaceae). American Journal of Botany, 95, 299–314.
Woodruff, D.R., Bond, B.J. & Meinzer, F.C. (2004) Does turgor limit growth in
tall trees? Plant, Cell and Environment, 27, 229–236.
Zhu, H. (2000) Ecology and Biogeography of the Tropical Dipterocarp Rain Forest
in Xishuangbanna. Yunnan Science and Technology Press, Kunming, China
(in Chinese).
Supporting Information
Additional Supporting Information may be found in the
online version of this article:
Fig. S1. A simplified phylogenetic consensus tree for six dipterocarp genera studied.
Table S1. Mean values of plant traits across 17 dipterocarp
species
Table S2. Coefficients (r) of Pearson’s correlation between
paired parameters using mean values of plant traits across 17
dipterocarp species
Please note: Wiley-Blackwell are not responsible for the content or functionality of any supporting materials supplied by
the authors. Any queries (other than missing material) should
be directed to the corresponding author for the article.
Received 14 July 2008; accepted 27 January 2009
Handling Editor: Lawren Sack
© 2009 The Authors. Journal compilation © 2009 British Ecological Society, Functional Ecology, 23, 658– 667